BIOLOGY

OF

REPRODUCTION

8,

158-182

(1973)

Cytology

of the Corpus
ALLEN C. ENDERS Medical

Luteum

Anatomy

Department,

Washington

University

School,

St.

Louis,

Missouri

63110

EARLY DIRECTIONS MORPHOLOGICAL Morphological luteum since Although it may in an the have in appear orderly taken briefly that fashion, initial studies a number description

IN STUDIES of of the of this corpus directions organ.

osmium atives for concerned tions per lipids these nature Corners from terization came
an
iii

tetroxide some

or Osmium-containing of their studies and

fixwere

not only with structural observase but also with observing the
order

to relate to the gland. lutea,

the yellowish Following

appearance

of

outlining the studies it should

these trends have gone be underof a new continue to

droplets of the (1930) corpora of

active

or luteal Allen and characcells Some presence carbonyl by histoa useful bein-

extraction the within of that lipid point

of progesterone cytological luteal interest. the

stood that approach, be new classic reviewed gation He of pointed used

after the introduction previous approaches with or on without Corner the pig 70 of early that

assimilation (1919), corpus years this of

of in his luteum, investi-

information. paper the the

vestigators cholesterol groups chemical means cells, ence Deane, of this try the proach final of could

thought and methods characterizing

of

previous histology out

of lipids in which be demonstrated was not only

structure. histological with granucon-

steroid-secreting the prescells. Helen advocates histochemisadministered battery in the ap1958 way paper things,

studies were the controversy losal fused origin by of the

principally over the this gland, problem

concerned thecal or and of were

but actually of ketosteroids who battery coup with had cell de her among regions of fatty carbonyl

demonstrated in these been one to the also to the

of the

determining

approach lipids, grace summary other

whether the structure rived from an atretic cle that had undergone

examined was defollicle or from a follinormal ovulation. of as of of of subexprisiCorner used

158

of steroid

Of the earlier work, the investigations Sobotta (1896, 1897, 1906) stand out an example of relating the histological structure of the corpus luteum to time ovulation. concerning the some sequent ception theca individual to Corner considered Although the interna extent to the species, have granulosa cells. including Strict (1912), there of is still corpus investigators almost without cells the confusion luteum contribution

discussing, by which groups) dized In to

of unsaturation acid molecules groups years, during cytological

(ethylene were oxifixation. and of a!., of

subsequent

cytochemical lutein cells Deane 1962; quently and Deane many

approaches took two her and coworkers Rubin, others,

to the study different pathways. (Deane 1965), took and advantage et subse-

cipal source of lutein Many investigators, (1919) and van der

the introduction method for the dehydrogenases

of the Wattenberg (1958) study of 3-/3-hydroxysteroid to demonstrate the pres-

Copyright All righth

#{174} 1973 by of reproduction

The

Society in any

for form

the Study reserved.

of

Reproduction

CYTOLOGY

OF

CORPUS

LUTEUM

159 et al., 1969;

ence of enzymes of pregnenolone hydroepiandrosterone

to

catalysing progesterone to to

the

oxidation or of de-

1966a; Cavazos
1970).

Bjersing et a!.,

androstenedione.

Although
different the which for duced exact enzymes synthesis,

this method
substrates

can
involved

be used
any in it

with
of

demonstrate

CELL
Steroid Synthesis present understanding corpus of cataloged different These and luteum active

BIOLOGY
and
we

dehydrogenases it has unfortunately intracellular involved. is oxidized, is the the

steroid Secretion are the the cells at a stage of been

a number render The but reduced TPNH reduced the

of disadvantages unsuitable of dye the in

the

localization substrate azo as and dye

At
our

the

time

introhydro-

of where lutein

structure cytological have

gen acceptor oxidation of by In the original addition,

a result of not directly complex. or formazan is somegeneral is

features
well

enzyme-substrate protein, and in

for tions. viewed

and continue species and features discussed will in

to accumulate different condibe a briefly subsequent re-

adheres times not be

to neighboring dissolved in lipid,

section.

so sufficiently associated remains level. the same

well localized with specific or membranes. highly time of that useful

that it can intracellular The on system, the for in histhe the

It must
that ogy and text thesis both

be pointed
our understanding

out here, however,

of the cell bioland secretion structural conduring synThis to cell is our in

compartments however, tological At synthetic steroids scopic duced. an and a suffered ture Enders eral microscopy cells of recently al., the lutein of 1958; most cells agranular and vesicular demonstration

of progesterone our understanding of intracellular and secretion

synthesis of the movements are the

methods involved

rudimentary. contribution steroid

enzymes

pathways were being examination The relative from origin profiles (1962) took in to a number described Christensen abundant were those endoplasmic earliest paucity confusion of

of biologically used, electron of lutein studies cells was

active microintrocells but na-

lack of morphological understanding of marked contrast to protein and the case of these can lar pathway association

to the situation gylcoprotein latter substances, be followed through into the

with regard secretions. In the the acids of this as the chains through celluinitial

demonstrated in lutein

abundance

of membranes

from amino

of ribosomes, concerning the many membranous (Lever, of the of that in seen advantage methods

of individual

with the reand site and

the

the ribosomes, forming peptide ticulum, subsequent of

any

passage endoplasmic within such side

1956). genlutein

its

segregation compartments, of saccharide (in the

improvements

electron

addition sulfation of the

demonstrate

terminal

sugars

Golgi),

of species, as in other steroid cells (Ross et and Fawcett, membranes of a tubular reticulum. 1961), within system After

tion gration release brane

that might still segregated

occur, condensamolecules, misurface, cell by and memavailand princiand

in vesicles to the apical to the exterior of the

WThy

fusion. isnt

this

type secretion

of information of progesterone?

cytological studies nical and critical gators began to tered 1964; 1968) with corpora Rennels, and steroid

achieved a better techfooting, many investistudy experimentally al(Enders Crisp and and Lyons, Browning,

able The the pally

concerning differences solubilities responsible.

in synthetic pathways of the products are As have pointed concerning of some Christensen

lutea
1966;

to directly synthetic

correlate structure activity (Blanchette,

Gillim (1969) tion is available ultracentrifugation

out, informalocalization by of the enzymes

160 involved ever, tron try in monitoring microscopy has been the synthetic of in example attempted being the addition only the pathway. fractions to by rarely, localization How-

ENDERS

ing tures

consideration of this gland.

of

the

cytological

fea-

electhe

biochemisCYTOLOGICAL
Granulosa Lutein Cells

FEATURES
of Early Pregnancy

outstanding

of 11-/3- hydroxylase of the mitochondria (Dodge

in

in the inner membrane of the adrenal cortex although synthesis the are are or extremely early additive, stages the with

Fawcett

et

a!. fine

(1969) and Gillim structure lutein of the

and of

more (1969) steroid The of

espehave serethe

et al., 1970).

Furthermore, cholesterol the the there to enzymes either tions, and tion to the The involve chain, genation easily A synthesis involved

cially Christensen reviewed the creting view cells that

including follows concentrates of early

cells. cytology

associated

microsomal steps are appears

soluble fracnumerous, segregacomparable into the cisterof pro-

corpus luteum losa lutein cells

on the pregnancy,

granuso that to re-

to be of a peptide

no simple

a single passage

compartment

the features observed those of cells actively leasing trates details vidual more progesterone. on of the species detailed general
cytology

may be restricted synthesizing and In addition The cells obtained 1. A number stage of of it concenspecific features.
of lutein

of the terminal

rough endoplasmic reactions in formation from cholesterol of than group difficulty the the the unsaturation,
via

reticulum.

gesterone shift

pregnenolone

should descriptions

be

of indifrom the aucorpreg-

removal in rather marked further

cholesterol and addition of

side dehvdroan

of individual

thors referred to in Table Personal observations. pora lutea from an active nancy were sion (early selected in this

of molecules. in studying majority of the as well in the

steroid

is that

inter-

postimplantation from our collection study (Table 2). addition to providing and increasing the extraneous in methods from wild

stages) for incluThese illustrabreadth of of comcomplicaused animals fixed in from perfusion

by

mediate products are highly soluble normally rations dition, do roid product. Since to steroids, dence In terone that through quantities ejection lular The obstacles biology will eral be the for, addition in the membranes there secretion the aqueous continuing not used suitable steroid accumulate nor do they for cells

as progesterone organic solvents cytological lutein active a secretion permeable for, or of would in nor evidroplet. progessuggest PrepaIn adcells ste-

in making

corpora, in tive material species parison tion of

radioautography. such as the stores of the condense are readily is no by reason vesicle solubility media release

coverage,

serve as a means

without the differences

in and imM

different laboratories. Although material from human mersion in phosphate tory the aldehyde aldehyde cases, in 0.1 osmium buffer,
in
M

corpora lutea was 3% glutaraldehyde buffer, was aorta 0.1

M

0.1 labora-

the

material by with either

low

animals abdominal
in

fixed

via glutar-

3% glutarbuffer. In all washed in placed in 1% phosphate

of progesterone paucimolecular suitable

into

or 2% formaldehyde-2%% phosphate subsequently buffer, in in ethyl

oxide, and

membrane

would be more of a large droplet question of how to to our understanding of steroid should synthesis later. be discussed

the

than the intercelthese cell gendur-

material phosphate tetroxide dehydrated

propylene

was

postfixed 0.1
M

space. overcome of and the the in mind

alcohol, embedded

secretion

However, kept

araldite sectioning, examination

epoxy resin staining

in an

(Durcupan) with lead RCA EMU

prior to citrate, and 3G electron

problem

CYTOLOGY

OF

CORPUS

LUTEUM

161

TABLE
FINE

1
OF CORPORA LUTEA

STRUCTURAL

STU0IEs

Rodents rat: Breinl, Enders, Enders 1967 1962 and Lyons, and Brestoff, 1964 1966

Koizuini,
Lever, Rennels, 1956

1965

Flaks Friend
mouse: hamster: Crisp
Yamada

and
and
and

Gilula,
Browning,
Ishikawa,

1972
1968 1960

1966

guinea Rabbit
Artiodactyl pig: cow: sheep: deer: Carnivore dog: raccoon: Inink: badger:

pig:

et a!., 1967 Crombie et a!., 1971

Yates Blanchette, Koizumi, Belt Bjersing, 1966a,b 1965

et al.,

1970, 1967

1971

Bjersing

Cavazos 1968a,b

el a!., et a!.,

1970 1969

Priedkalns and Weber, Dingle et a!., 1968 Sinha et a!., 1971b

Crisp et a!., 1972 Sinha et a!., 1971a Enders, 1962 Canivenc, Adams Carsten, Crisp and 1965 1967 Hertig, 1969a,b

Enders,

R.

and

Enders,

A.,

1963

Primate
human: van Motta, Tokida, Vacek, 1965 1967 lljortkjier Faick lemur: Edentate armadillo: Sisson and Fahrenbach, Lennep 1966 1965 1967 Pederson Larsen, 1968 and and Madden, 1965

Gillim
Green

et a!., 1970 et a!., 1969

and Maqueo,

Enders,

1962,

1966

microscope microscope. Cell Size

or

Philips

300

electron

in thors

steroid-producing have cristae. as considered

cells. the

Subsequent question with these the

auof mitoregard cristae matrix

chondrial

to the lutein strictly

1-6;

shape, particularly In general when elongated tubes into they are described (the latter term the than projections When tubular, the

Granulosa the body end largest (Figs. of the

cells all figures Even

are

undoubtedly cell appear in at the the

project

endocrine

compartment, form or tubular larly long more erally these hand apt and when

as villiis particuare cristae are both are gen-

article).

in rodents,

where

lutein cells are only about 20 em diam, they are usually larger than cells of the zona the where they are fasciculata. human larger truely (Fig. lutein giants. In other 1) cells or are species ferret 40 m such (Fig. or more, as 2),

curving).

plate-like

they

referred to as lamelliform. designations are essentially terms encompassing wide organization. more small larger mitochondria lutein cells lutein there cells is more are the the

Both of shortvariations per unit rodents speevidence

in three-dimensional There area in

Mitochondria

of

Belt tion to

and the

Pease unusual

(1956) form

first drew attenof mitochondria

than cies.

in

of other

In

addition

182

ENDEBS

PLATE

1
of plastic-embedded corpora lutea.

Cranulosa

lutein

cells.

Azure

B-stained

sections

x425.

CYTOLOGY

OF

CORPUS

LUTEUM

163
TABLE 2
PERSONAL

both of

of clustering

and in the is the lutein found, is

of regional larger rule cell and often

exclusion cells. the

Animal
MATERIAL

mitochondria

ON

WHICH

Pleomorphism exception in Spherical, chondria cell. the cristae also tion vary that same are to can Variation cell most are

rather than mitochondria. elongated within the size tubular, one that generalizalutein with

OBSERVATIONS

ARE

BASED
Stage

cup-shaped,

mitosame within they cell mitolamellito the

Rodents

rat#{176}
mouse

early early early early early early

implantation implantation implantation, implantation, implantation, implantation

(Day (Day (Day

6,7) 6,9) 5)

in mitochondrial also common. The made never is commonly

Although

hamster
gerbil

midpregnancy midpregnancy

lamellar. be are neatly

mitochondria chondria form long axis cristae of the

rod-shaped

of uniform

diameter perpendicular

Euta in ias Microjus Zapus guinea pig Proech imys Carnivores niink
weasel

early early

implantation implantation,

midpregnancy

midpregnancy

mitochondrion.

In human lutein cells, mitochondria are larger in pregnancy (Crisp et a!., 1970) and (Adams
in

ferret Primate
human

delay, early implantation delayed implantation early implantation

6 weeks, secretory 10 weeks cycle gestation, mid

more and which

centrally Hertig, is contain Hertig, form of thecal (Fig. widely both Although some of 10). a there

situated 1969b). population some of

in

the of

cell cells large mitoChiroptera Thyroptera ]lfolossn

In some these

early early

implantation implantation

round chondria

mitochondria, also

Tadarida
Insectivore

early early
delay,

implantation implantation
early implantation

osmiophilic

granules

(Adams and most common lutein cells is tubular also been in shape cristae. tubular, coidal (Enders The fairly sistent (1968) chondria

1969b) (Fig. 11). The of cristae in human and The granulosal rat which origin has variation and of are elongated lamellar Breini, species largely discristae
1967).

Blarina
Edentate Dasypus
Marsupial

Philander

late

pregnancy
which corpora of three or more

studied shows of mitochondria the the cristae more have 1964; of most but Crisp the lutein

#{176} Animals from females have been

examined.

mitochondria and mitochondria dense matrix, in the rat. described of active Lyons,

as tubulovesicular.
mal pregnancy,

In corpora the cristae forms cristae mitochondria in hamster in present the as

of early are well have other at

nor(Figs.

tubular, a larger of the the time species.

have

with 7 and

a few 19). than

lamellar Some space is of of the

this is less conand Browning of the mito mouse cells in the

intracristal mouse Mitochondria

cristae

Ftc.
Ftc.
space the

1. Human

lutein

cells at 10 weeks
cells
some at the time intercellular

of gestation.
of space implantation can be (12 seen days between post coitus). the apposed The interstitial

2. Ferret
is large,

lutein and

cells.

Note

concentric
Ftc. 3. lutein
size

The

arrangement of dark-staining Corpus luteum of four-eyed cells show appreciable variation

regions. opossum (Philander) with in size, intensity of staining

Ftc.
small

4. Mouse
of these
size

corpus
and

luteum

in early
lutein cells.

implantation

stage

(Day

hind-limb-bud fetuses. and lipid accumulation. 6). Note the relatively

cells are roughly

subsequent

Ftc.
the

5. Hamster

same Ftc. 6. this species

corpus luteum at early implantation (Day 5). The lutein as those of a rat or mouse at a comparable stage. Guinea pig corpus luteum at early implantation (8 days post also the lutein cells are relatively small,

copulation).

In

164 of implantation resemble mouse of those of the

ENDEES

rat cells de-

more than the Mitochondria are good examples velopment mustelids other dog: clude 1971),

(Fig. 24). carnivore lutein of extensive not 13) Sinha lamellar pig 14), (Crombie and tubular only but

At the same time the tubular provides the least amount for covering be expected
conformational

shape, which of membrane would to the Hacken-

the enclosed volume, to offer more resistance shifts

reported

of the cristae, (Figs. 12 and

in the also in

by

families (raccoon: Crisp et al., 1972). with the bat largely (Fig. guinea

et a!., 1971a; cristae et armadillo rabbit cristae et a!. lutein with (1970) in cristae described inal.,

brock (1972) from the orthodox tion of energized mitochondria densed mitochondria. configuration of

configurato the conde-energized

Forms

Endoplasmic An reticulum cells studied. to considered ture of sen and reticulum lutein endoplasmic as the stretches doplasmic in the cell. doplasmic tributed, localized human; et al., cells. abundance has

Reticulum of been [This be the smooth reported structure most endoplasmic in is all lutein feagenerally

(Enders, 1962). Mitochondria of lutein cells contain both forms of (Blanchette, 1966a, b). Sinha (1971b) cells some pointed
of

describe as being out that tubular

the largely forms. the plates,

cristae Belt images could

of deer et seen be al.

lamelliform

consistent

steroid-producing Gillim, 1969).] in modest In many reticulum anastomosing reticulum, In other reticulum

cells (ChristenRough endoplasmic amounts species occurs with the generally animals the is less stacked in the is found the as smooth rough small enin

pig

mnitochondria
(1968a)

as perforated and Weber drial cristae

whereas Priedkalns describe the mitochoncow lutein cell

of

the

tubular. We have little limit in range

in steroid

information of forms cells. for

to explain of mitochondria The side

dispersed rough endiscisternae cell (e.g., Crisp between and can

generally

secreting

chain

cleavage enzymes terol to pregnenolone ated tensen in the and Gillim,

conversion of cholesare consistantly situfraction However (Chrisif we 1969).

but forms in small patches Adams 1970; Fig. of and 8).

Hertig, Continuities

1969b; portions reticulum

mitochondrial cells from

consider that lutein some progesterone mitochondrial that required It is therefore in particular mitochondria less ticular consistency cells,

are synthesizing acetate, then the is in excess of

the cisternae tubular smooth be

the rough endoplasmic

component

for steroid synthesis alone. surprising that lutein cells show the steroid cell type as apposed of this in which with type the changes to the somewhat corare 18and side and the in adrenal mitochondria at the to cholesterol both tubular

readily demonstrated in lutein cells. In larger lutein cells, and to a lesser extent in small lutein cells, it is characteristic the in gen-

of smooth endoplasmic reticulum to be most abundant cytoplasmic constituent the erally ally of sions) light type the 2). peripheral concentric produces
greater

region nature a series (other lesser described can be endoplasmic

of the

cell.

The distribution

of the reticulum of

of smooth

occasionlines incluin in (Fig. of this density areas ferret (1919) and

also involved 11-positions chain On cleavage. geometric

concentric ER) Corner

in addition grounds

organelles (smooth Concentric by seen in the

and were pig and

micrographs.

perforate plate type ratio of matrix space to intracristal The highly ticular brane exposed space tortuous the to the

cristae increase (inner compartment) (outer tubular area matrix compartment). type in of inner compartment.

parmem-

increases

Christensen and Gillim (1969) have pointed out that, as our methods of preservation have improved, it has become in-

CYTOLOGY

OF

CORPUS

LUTEUM

165
compartment,

creasingly plasmic branched fenestrated lar works lar form sheets

evident reticulum tubules, cisternae. may and to be (Figs.

that is The the

the in

smooth the branched form sheets,

endoof and tubunettubuare

plasmic

reticulum

the appear form

is

ranto of other

dom
be

tubular the

distribution

would predominant
reticulum

tubular

Even smooth

most efficient. when the

endoplasmic

constitute lutein fenestrated found 16, centered droplet approximated

anastomotic cell. The cisternae

random

throughout

tubules,
organelles

there
are

are

regions in this

from In study,

which the

excluded. of smooth

majority extensive recontwo cisin

more likely of lamellae not drion and clude cupied. organized are few rower are dna sional varied ject of usually cisternae, than wrapped (Figs. form and so exclusively or

as ordered stacks 18, 24), often but on (Figs. a that mitochon14 and they region 15), exochighly a nar-

of species areas ticulum trast to ternae

arrangement change of

reported present. regions around appears steroid

of whorls are the wrap

endoplasmic

a lipid closely

In these areas, where one or

other organelles These areas smooth peripherally some the around

from the of concentrated, endoplasmic situated. of the individual which tubular

a mitochondrion, inefficient for between the two appropriate, within the steroid lipid the protein generally progesterone simply using clear output pathway enzymes acetate microsomal from the the

the
inter-

or-

reticulum Often are mitochonenquite subIt encorcan such (Chrispersonal

ganelles. It would be for sequential steps ganelle, were of the Corpora to tate cent from et been tion. the and al., synthesis Despite pathway because steps abundance cells be able rather of the the 1969). of associated especially associated membrane with lutea to form than but total small the are with and

however, same oracted upon were component

if the

branched

portions,

enzymes component.

15 and 21). The three-dimenthat associations of smooth reticulum bizarre, and by can take is the has been Blanchette

associated

considered from circulating what (Savard in the have fracin

doplasmic

aceper comes

discussions

(1966b)

cholesterol,

it is not progesterone molecule

and by Christensen is curious that, when doplasmic pora often as the tensen lutea be reticulum of found a species, in

and Gillim (1969). whorls of smooth are other found similar steroid of the
1969;

in

the

Many cholesterol with

of the

whorls cells testis

interstitial and

cells Gillim,

the large number of synthesis of of the with of would of the cholesterol.

why lutein

of steps progesterone of so many fraction, more reticulum surpris-

observation). Although nothing ing the role of the of smooth plications differences. throughout tubular lum, mouse appear enzymes of synthesis smooth chondria, and the molecules between mitochondrial the form such (Fig. to be as 7) the is and the are endoplasmic the must cytoplasmic endoplasmic may The of smooth be

association the microsomal endoplasmic be even progesterone In

cells

is yet different derived general

known concernarrangements some from of a the distribution branched reticupregnant 12), would if the steps in the That and the the is, if forth the endomitoimthese

of these the ing

in lutein

reticulum,

if much

came particular are so cells,

from one much de-

circulating
wonders

cytoplasm found mink best in alternately reticulum, the in

endoplasmic (Fig. arrangement sequential situated

larger

than

other

steroid-secreting

spite the progesterone gens,

gised

relative simplicity of synthesis of as apposed to adrogens, estrocorticosteroids.

progesterone,

and
that

It

might

be

ar-

involved

recently mediate
must be

evolved in
produced

hormone, of
in

as a relatively and as an interother

relatively

synthesis to mass

hormones,
large

cytoplasm. pass back and

amounts reasoning stand the

compared is useful total

other of lutein

steroids. tissue,

This but

compartment,

in attempting

to under-

compartment,

Ftc.
tubular

7.

Mouse
An

lutein

cell

(Day
from

6 post
an

copulation).
lutein

The
cell

mitochondria
appears just

(M)
above

have
the

roughly
nucleus

cristae.

intrusion

adjacent

(N). Note membranes

this intrusion includes numerous lipid droplets (L) and that the adjacent a close junction at the arrow. The surrounding lutein cell has both smooth endoplasmic reticulum (SER) and rough endoplasmic reticulum (RER). The smooth ER of the included cell is dilated. At the top of the micrograph two processes of the same cell come together to form a close junction (paired arrows). x 35,800.

that fonn

166

Ftc. 8. Human lutein cell (10 weeks gestation). The smooth endoplasmic reticulum (SER) is in the branched tubular form. The rough endoplasmic reticulum (RER) is localized in the cell above. The membranes of the two cells come into close proximity (arrow). Lipid (L); lysosome-like granule (Ly). x45,100. Ftc. 9. Human lutein cell. An inclusion from an adjacent cell or cell process is seen at the left, bounded by closely associated cell membranes (arrow). In the middle of the picture is a region where the smooth endoplasmic reticulum has folded cistemae forming a membranous organelle. 10 weeks gestation; x44,300.
167

Ftc. 10. Human paralutein cell. In the cell at the top, the smooth endoplasmnic reticulum and rough endoplasmic reticulum are particularly clear. The tubular form of the cristae of the mitochondria can be seen (M). Note the increase in density in the associated cytoplasm indicative of rudimentary desmosomes (arrows). Lysosome-like granules (Ly). 10 weeks gestation; x 18,800. Ftc. 11. Lutein cell of human. The large spherical mitochondria (M) seen in this lutein cell contain numerous osmiophilic granules. Smooth endoplasmic reticulum (SER); lipid (L). 10 weeks gestation; X22,600.
168

Ftc. 12. Mink corpus luteum from late in delayed implantation. The mitochondria with their clearly tubular cristae are generally distributed throughout the cytoplasm, as is the branched tubular smooth endoplasmic reticulum. Note the surface folds, especially in the upper left, and the small dense granules. x21,400. Ftc. 13. Ferret lutein cell. In the Colgi region are stacks of cisternae (C) and numerous vesicles. The fine filaments characteristic of carnivore corpora lutea are seen in cross section (circle) and longitudinal section (bracket). Day 11 post copulation (pc); x 48,400.

169

Ftc. 14. Bat (Thyroptera) lutein cell from an early implantation stage. Note the extensive concentric lamellae in the lower right and the less extensive series of lamellae around one of the mitochondria in the upper left. The mitochondrial cristae of this species of bat are largely lamelliform. x21,200. Ftc. 15. Ferret lutein cell at the time of implantation. A series of concentric lamellae of smooth endoplasmic reticulum are around the mitochondrion in the upper left, whereas close association of only one layer of smooth endoplasmic reticulum is found around the other mitochondrion. Day 12 pc; X22,000. Ftc. 16. Ferret lutein cell. Folds at the periphery of the lutein cell create marginal compartmcnts. A blood vessel intersects the upper left corner. Day 12 pc; x21,000. 170

Ftc.
delimit

17.

Two

lutein
intercellular

cells lutein
cells. thickenings

from cell.
Day

abundant

space.

are
the the
arrow).

seen Ftc.
two Day

in the 18.
cells
Note

lower
of these

a ferret corpus luteum. Intrusions of cytoplasmic Fine filaments characteristic

X22,000.
between ferret

projections from the cells processes from adjacent cells of carnivore lutein cells traverse
cells. The junctions between

The

cytoplasm

12 pc; (large

Intercellular
show that 12 pc; at the there x20,200. is

compartment

lutein a

arrows) of a basal

and lamina

region
in

of
relationship

close

association
to the

(small

no

evidence

intercellular appears and close

space.
FIG.

19.
but

Mouse of the

lutein
right

cell.

unifonnly
is a

spaced
region of

separation
modification

of
of

the
the

two

cells

at

the

left,

(arrows)

cytoplasm

apposition

cell membranes.

Day

6 pc;

x47,000.
171

I
Ftc.
tubular 20. nature Lutein cell of the from smooth a ferret. endoplasmic of the Colgi of in other are space. Day In is seen the the basal 12 lower at the a Note the reticulum. region abundance Day of a 12 of pc; ferret fine filaments x67,000. lutein cell appears with the to show

and

the

branched

Ftc. 21. This continuity between

(arrow). drion. Ftc. The discerned. Day 22. folds (1972). where Ftc. of spacing 23. granular of the it abuts Note 12 are These also pc;

micrograph

the
the X61,500.

smooth
close

endoplasmic
association folds each indistinct

reticulum
smooth lutein by a lamina pc;

and
endoplasmic

the

margins
reticulum

of a Colgi

cisternae
mitochonspace. can Friend the lutein granules The close be and

Marginal separated

ectoplasmic from junctions an interstitial that the granular

cell uniform

of

ferret space

enclose in at which described the

a peripheral granules by of

septate-like is

contacts present

Gilula
cell

Note

margin and contained X38,400.

In the
junctions two

upper
can cell

portion
be membranes

of the
seen.

micrograph

x28,500. the uniform

left is a Ferret,

spacing cytoplasmic Day 12 pc;

protrusion.

arrow.

Ftc. on itself Ftc. small cells. cells. as a few

24.

Hamster
leaving

corpus a small opossum cisternae.

luteum space Lipid (L);

on (asterisk).

Day blood

5 pc.
The vessel corpus

The
smooth (BV); luteum

cytoplasm
endoplasmic nucleus in at (N); hind-limb-bud

of

this
reticulum X 22,400.

cell

folds
is

back
present

clustered 25. Four-eyed

(Philander)
(Gr) are reticulum

stage.

Numerous

membrane-bound Whorls of smooth x22,600.

granules endoplasmic

found,

especially are abundant

the margins of in other regions

the two lutein of these lutein

173

174 does not necessarily explain of individual lutein cells. Although it is the this article to discuss
it

ENDERS

the large size purpose lutein of cells,

the

Golgi

zones from the

tend

to have smooth

relatively endoplasmic

few re-

tubules

general active consider literature, to

ticulum, a relative in addition to above, and tion of the been (Crisp ple, cisternae, numerous 13). Fawcett in steroid types, the is in ternae. have Golgi tubular the (Fig. direct In often et a!. secreting smooth support observed

paucity of mitochondria the elements mentioned a more Coated discrete portubules have zone exam5-7 and (Fig. that

might lutein

be

useful cells

to

a recurrent namely have large reticulum a reduced factors may In and there rather steroid some 1969) of steroid than output. synprospeand less an Kiciwell, is a shift

point why amounts even level account cies, 1969; rabbit effective

of confusion of smooth

in the continue

constitute cytoplasm.

endoplasmic

observed et a!., individual

in this type of Golgi 1970). In the ferret, for elements usually dilated coated (1969) has have face, vesicles suggested

when there is apparently of progesterone. Three for especially Hashimoto (Strauss than this discrepancy. the rat and et at., (Wiest Wiest, 1972), a form progesterone, drop in total

a pronounced peripheral

of 20-a-progesterone, immediate

cells, unlike endoplasmic with this marginal of

other cell reticulum Golgi dilations ciswe of

communication

contention,

Secondly, it appears that cholesterol thesis does not decline as rapidly as gesterone ditions, but is synthesis so that not this converted under substance to a variety accumulates progesterone

of con-

cisternae which appear and assume the same smooth endoplasmic 21). even less information the possible role secreting
and

to become diameter as reticulum available the Golgi of mitoreticunot lack really of been cormicroknown conConaddi-

adjacent

(Guraya, 1971). Finally, examination of cells in older corpora indicates that when there has been an extensive development of mal and the smooth readily cytoplasmic the sheets and become interesting endoplasmic diminished. constituents tubules reticulum, Instead are the norreduced It stage assoit

There is concerning in steroid

chonciria

of that have

cells per and it is

than se

smooth because

endoplasmic of the not

is not

lum. related scopic whether taminate

Golgi

fractions and

examined,

of endoplasmic

biochemical studies,

electron membranes fractions. product and

reticulum would he these ciated Goli Most by the steroid in cated many volume. the plex have and wise In monly

isolated membranes. to know at what lose their various enzymes.

membranes steroidogenic Complex investigators large cells consists

any of the Golgi the microsomal of secretion

densation tion two

of terminal sugar common functions be to 1972) expected synthesis might cells, rate might cells. adrenal of but either turnover (1969) et a!. be glycoprotein we in in the

groups to a secretion, of the Golgi, would lutein cell have in cells. coats no surface lutein suggested in sulfation contrast of tend lutein that Golgi zone to cells, is not is A (Whaley significant information coats cells. that the in stehuman produce which sulfated, proporor major in relaet of saccharides functionally these

have

been

impressed complex lutein most elements in cells comloin

not role tion al.,

size of the Golgi in general and in This of of organelle a series of

particular.

in these concerning their Colgi roid fetal sulfated produce indicates Fawcett

at one side cells occupies In are in numerous lysosome-like similar some to animals the animals individual

the nucleus, and a nearly comparable small of the lutein Golgi

with

cells, comwhich vesicles,

elements regions coated

of cytoplasm and smooth but of large the are lutein rest

be involved However a cells, which and the

granules, with

othercells,

steroids, progesterone that

cytoplasm.

CYTOLOGY

OP

CORPUS (Sinha

LUTEUM

175
1971b).

tionally type. preciably thought granule to this 1971). Granules The dense lysosomes, appreciably. cies the drolases tion and tion the Nor

as large does bigger to formation

organelle

or larger the
in

in the zone cells relaxin, occur pig

latter appear which although in

cell apare

et to

at., these

Numerous seen in lutein (Fig.

granules cells of 25). Since

Golgi those does

in the

similar the

are
(1969)

four-eyed

opossum in the

secrete

relation
et

Tyndale-Biscoe ence of relaxin al., the Australian tempting to leap on these tenuous of the four-eyed

reported the prescorpus luteum of

(Belt

opossum,

Trichosurus,

it

is

the Pacific and suggest grounds that the granules opossum may also contain

number

of whose found
While,

small in the
in

membrane-bound resembles zone of these varies speGolgi most of the definitive has not of
it

relaxin.

bodies,

appearance

Lipid The cells cies, amount varies from of lipid in with none granulosa lutein

demonstration necessary for structures additional in the lutea bodies

are in

acid byidentificabeen made,

inter-

appreciably practically

different speto relatively droplets on are and to the state

of these of pigments

confusion is present,

accumula-

is still

abundant. In general lipid considered to be membrane-limited vary in osmiophuia depending of saturation (Christensen there early mulates Lipid
except

esting that, the corpora many dense of lysosomes of cells peroxisomes 1972) (Reddy (Beard,

most active stages of of almost all species, with the in the

Recent

and and relatively

method Gillim, little corpora

of preparation 1969). Usually lipid but present more of accuactive. activity If and later, is a seof lipid Blanin

appearance
discovery

is stages

present.

of pregnancy, when a useful comparison lipid in lipid as far only, if it be

adrenal 1972) the in active of

cortex interstitial suggest role of lutein

even is
in

remain

and
and

testicular

not

criterion

Svoboda,

that a comprehensive study peroxisomes and lysosomes cells The luteum somes should be undertaken. problem of regression and, in particular, of lutein cells and is beyond of the microscope level interesting corpora Quatacker, that is the corpus suggested with are

there numerous one

is little should

between stages. early pregnancy droplets that as the is occur there

large activity

suspicious

of the corpus the role of lysoof macrophages scope of has been than by construcbeginning
with
review

reduced cretion is from

progesterone if material amount extensive.

is concerned. one stage only

However

in this regression this chapter. Much done electron Dott, cerning tures
in

the work (see

is significant chette (1966b) in rabbit lutein

significance

at

the

light but

rather studies

discusses the role of lipid cell function and possible types within corpus of variation the granulosa luteum may se, whorl 1962; This been et a!., noted 1966). 1967). also seen. cell have In

microscope 1969), acid atretic

of the cells of the amount to lipid whorls isolated

myelin

Individual
population

phosphatase-containing 1971). not associated luteum. that the

to

a greater addition tion of through

frank

of lipid than droplets per or parasomes membrane (Enders,

others.

appear (e.g., A granule autolysis of the (1971) tion ules and is is sow have time

degeneraproceeds stage Blanmethod in to

membrane-bound

granule Belt et at. the distribuof these idea that are lutein in lutein the granthey often cells pig cells

figures Bjersing, has

chette, of other Nucleus

1966b; steroid

of appearance

degeneration

consistent

cells (Enders

contain relaxin. Small granules a common feature of carnivore and have granules been similar reported to in those deer

Short of the pycnotic changes with necrosis, only some of the

associated more gross

176 aspects certained with of the by cells well-being of electron can the be nucleus

ENDEBS

asIn

In

only

observations

abundance

some species greater than human, with from

however is that of most filaments the cell

and

their other

transmission

microscopy.

the case of lutein cells, we find that both small and large cells contain nuclei with well-developed matin, other present preciably those those nucleus and only nucleoli, a little dispersed heterochromatin sex chromatin membrane. Apis seen in lutein cells than general form to is that the chro-

cell types. In the marily associated with regions

(Adams 1970; In rudimentary

are prisurface,
with

desmosomes,

derived
and Gillim Hertig,

the

cell b; Crisp
filaments

surface et al.,
are

1969a, 1969).
however

than the inactive along the nuclear more heterochromatin animals with with large received, is in the small

et at.,
carnivores

the

characteristic They cently a!., and

they

of

the

granulosa

lutein of the Sinha

cells. reet

lutein cells. The however, morphological

have been reported in all studied species (raccoon: 1971a; ferret:

ramify

impression

dog: Crisp personal throughout abundance

et a!., observation) the (Figs.

1972;

mink where in 20). 17,

be expected in a cell in which both extensive DNA translation and ribonucleoprotein synthesis were being carried on. Some general the nucleus of by Christensen (1966) matinic lutein discuss
lacking

cytoplasm 13,

surprising Although in cell

siderable

considerations steroid cells and Gillim

concerning are presented (1969). Rennels

the role movement

attention,

of cytoplasmic has recently in carnivore preclude any

filaments gained conlutein cells

the spacial distribution to localized

of

the

filaments appear function.

points out the presence of perichrogranules in the nucleus of active cells the of the rat. Crisp and
lucent

would contractile

et halo

a!. in

(1970)

these granules electron

similar granules lutein luteum of pregobserved these

as well,

Surface For cialized can be microvilli,

Specialization.s convenience areas of the of description, surface the spe-

cells of the nancy. We

structures significance in

human corpus have commonly

other remains species unknown.

of lutein cells (including on other peripheral complexes micro pinoor

but

their little

In general, relatively

classified as projections projections intruding to form junctional presumptive

the

nucleus

has

received

attention. Filaments Some pear so few

significance. in

cells, folds tending other canaliculae), between cells, and cytotic vesides Projections. has projections creasing the
Hertig projections (1969b) in

of the the cells cells in

inclusions of so few those species

structures

of

lutein

cells which include

apthey the of

or caveolae. The surface of all lutein cells of total

human

species
in

or within general

one cell

sort or surface.
lutein cells

another, Adams
from

inand
one

are found osmiophilic human and from

that they are of doubtful

These

note that not only are there deeply into adjacent cells,

granules lutein cells, as

in

mitochondria mentioned organelle reticulum above,

cell

extending

the membranous smooth endoplasmic (Fig. 9). inclusions are

formed of this
in their

but that many to eventually

(1972) have

of these projections appear pinch off. Espey and Stuffs recently in demonstrated granulosa cells
are

species Other

lar so ubiquitous lutein cells of those speare found that it is diffithey can
in

phenomenon

a simiin the

follicles

distribution in the cies in which they cult ple to believe that

functional significance.

with
cytoplasm

of the rat. There double membranes

of

deep we some the

projections within the have sections adjacent majority studied the cell of

all 17,

species 23). but In with in

be
for

without
exam-

(Figs. connecting can be

7, 9,

Filaments

bridge observed,

are fairly widespread

lutein

cells.

the

CYTOLOGY

OF

CORPUS

LUTEUM

177

instances sections any the of of depth Espey Extensive also

it

it cannot. is not of and these

In the possible

absence to be are

of serial certain that but of the

rather complexes tors nep

ignorant were not been Madden have and

statement lacking.

that Other

junctional investigaVan Lensuggested

projections location, Stutts

together

isolated,

modification

so negligent. (1965) first

cytoplasm, isolation self

with the observations (1972), suggest that of a cell back on lutein cells (human: 1969b; Smaller These of mouse: projections small irregular
1962; it-

that tight junctions were present between human lutein cells. Adams and Hertig (1969a) (pentalaminar)
cells in

is possible.

report the in and this illustrate

both human. of species

desmosomes between et or at. tight and (1968) Gillim

and

tight lutein
(1969)

refolding occurs in

junctions presence

Adams hamster: to are

of

and Hertig, Fig. 24). ectoplasmic.

Fig. 7; tend folding

note tions (1970) Crisp out branes

the

close

juncet at.

Crisp earlier between areas densities

be

projections
Blanchette,

pentalaminar apposition lutein the had cells. described membranes, periodic and an in steroid Gilula cells, to on this the extensive septate-like
based

junctions. pointed memin

often in the form the surface (Enders, Priedkalns 1971a, urojections folds are Hertig, Where (mouse: more to likely canaliculae 1969b; lutein tissue Crisp cells space, In general b) and (Fig. are

Browning of close

areas Rennels

1966a;

Weber, 12). Crisp to be In and microvillous

1968; some

Sinha species rather

of mouse (1966) where apart,

them.

et a!., these than

1968).

rat bere-

lutein 200
tween

cells A

although (1972) study and cell

Browning,
type

microvillous (human: et at., are

projecin
1970).

Friend

tions tionship and

found

rela-

cently
type

published of junction these

In is

of this have conarticle, adrenal

Adams to
generally

called the tacts.

which

junctions the
principally

exposed there is

introduction

connective

a thin, often discontinuous basal lamina (Fin. 22). (Although corpora lutea are richly do not
species,

vascular, indent
but

the the
especially

sinusoidal cells
carnivores,

capillaries and in many

there

cortex of the rat but included other steroid cells, they state, In the order of increasing surface area occupied by contacts between adjacent cells, which zonulae and even there are, are focal in extensive extensive lutea pentalaminar maculae the rat; gap rather rudijuncfusions, than mentary at most,

lutein

is

appreciable cellular cells and tween spaces (Figs.

tensively intracellular rangement

interstitial spaces between

lamina tynes found: cells are
basal

space.)
is lacking

In the adjacent
(Figs.

interlutein
17 ar-

occludentes more corpora

desmosomes; of adhesion.
examining

a 18).

tions, zones
In

septate-like from differ-

Several

of canalicular enclosed spaces

(Fig. 18),

beent that
exin

adjacent
enclosed

peripheral processes are a partially cells

by 22), on cells et a!.,

refolding

cell

species there

for this report, are a large variety between not

epithelia.

it became clear of junctional cells which

found in

16 and folded lutein Crisp

and

where

relations or might
typical with are central

lutein
to Complete

might more

themselves, (Adams
1970).

relate

those

canaliculus,

especially

desmosomes

human 1969b;

and
Although

Hertig, some

rarely

disc and associated seen. Relatively small

can

filaments maculae
number of

of the canaliculae a number of spaces are Junctional

can sections, corn p!exes.

be

followed other
In

through peripheral pockets. earlier

adherentes

be of

found

in

species.
with

Rudimentary a fixed gap

desmosomes more than 100

(regions A and memis the

essentially

isolated

most

publications the tween granulosa

ignored. Enders

junctional relations belutein cells were largely (1962), having noted the desmosomes, made the

juxtaposed branes)
Of

densities on the adjacent can be found in all species.

greater significance

probably

wide

variety

of that

close can

associations be found

of between

cell

absence

of

typical

membranes

178

ENDEBS

lutein cells. In instances where there is a projection of cytoplasm from one lutein cell indenting another lutein the two proximity possible in many gap as of of to cell, a portion of the region where apposed is in close It is not always but distance, membranes (Figs. determine these cases are 7, 23). the the

plasmic

projections diffusion

with pathway. specific

minimal sequence of

blocktight,

ing

of the Although

the

gap, and desmosomal junction so common to the apical junctional complex of epithelia at this is not point found that
in lutein cells, it is clear

there of with

are rather these (in are of

nevertheless particular cells. Cursugform of to the

apposition has a A and is maintained tion ingly, occur tein with (1972), general

appoximately 20 a parallel associaInterestmay also the In and same agreement Cilula the are lu-

an impressive array junctions associated rent gests bands, the tute adjacent molecules, regions cell thought that not intercellular and of tight isolated that ion on

for appreciable areas of close when cell abut projections one of

distances. apposition from another. Friend

junctional junctions spots) passage gap exchange

complexes barriers water-soluble

observations

junctions from and

consticell McNutt, to

areas of close characteristics

apposition with of gap junctions

(Weinstein we lack coupling dye For gap are lutein and

more extensive than are regions association. (The limited areas association fied it as tight was not by Extensive suggested be
commonly Although

of closer of closer identisince acetate.) A gap to

were

1972). Unfortunately, concerning electrical cells, been between terization freeze-etch marker Clearly complexes nor used has these and methods an extensive of the tracer cells.

information of lutein Yellow characjunctions, diffusion useful. needed to

could junctions stained regions Friend

not

be with

positively material 200-300

adhesion

Procion

in our with and of

(Figs. spaced

to discern intercellular pathways complete tight of both

uranyl the Gilula 22

(1972) and
extracellu-

intercellular especially cells is

septate-like
the

zones
encountered irregularly

23).

study of the junctional

lar particles junction ally, gone uranyl could larly uniform junctions in none were of

characteristic seen our clearly preparations

of this peculiar only had occasionunderby pyro-

clarify our understanding of the interrelationships of lutein cells and of their peripheral compartments. Caveolae. The of the external
mally

enhancement acetate en staining. nevertheless the ferret spacing between

of the membranes bloc staining or by Since be corpus is a lutein some luteum, common cells observed,

majority an These
with

of structures

caveolae and are

are an norof

type coat.
associated

showing

internal

antimonate

granules particuand feature the in spe-

micropinocytosis

proteins, but have not been lutein cells. They can be found abundance associated in all both lutein with cells the

studied in moderate on the surface space

in

of most

cies, it is probable demonstrate that

that further this junctional

studies will association

interstitial

and with the intercellular spaces. FUTURE Although our steroid OF STUDIES contributions cell biology above, as mentioned to
of

is a characteristic feature of these steroid cells. It is important to note that these granular junctions (septate zones) are common not only between lutein cells but also in places back and
junctions

morphological of the have,

understanding secretion

where on the
are

processes have
areas

of lutein cells fold Friend that the granular but are open

cell of origin. Since shown

of adhesion

Cilula

been somewhat disappointing to date, a number of approaches currently in use or being developed should practice to lutein help of cells rectify this deficiency. The current granulosa cells

to diffusion, such regions, the wall of a canaliculus partment, would give

when involved in or peripheral comsupport to the cyto-

differentiating in vitro, as

CYTOLOGY

OF

CORPUS

LUTEUM

179 problems by Dietert cholesterol (1969) and about Simple

of

exemplified Channing

especially (1970),

by

the

work

of not

In order sion, digitonin by Scallen Combined cal ogy studies of obtaining useful.

to minimize at and complexing

of dispersuch as the used might morphologibe

offers an opportunity

attempts

stabilization

only for the separation tions of granulosa and but be mine produces terone passage interstitial solubility media, membranes, partments elaboration tively suggest carrier to leave large that the its may from fluid of the of the there lutein affinity also a good whether a be the permits system or substance loosely lutein to blood progesterone for presence cell the direct substrates, inhibitors, not

of steroidal functheca lutein cells introduction should try to to cells vessels. in the lipid of lateral and some diffuse for the type to to deterluteum progesduring through (The layer aqueous of conrelato of the its the low of also etc. It

biochemical offer information cells. important

in which the

advantages the cell monitoring the isolated the unexplored

in biolby fracby be isoin-

corpus which

lutein

bound

electron tions

microscopy

is important. of organellar would appear For reticulum fragments as

However, partial associations to offer example could in the

procedure which lated, formation. plasmic vesicular tion Not stacks synthetic but only be

homogenization, could even the smooth be isolated a microsomal stacks components of more

at the margin interstitial should to cell

of lutein cells, the space be enable and combine progesterone

endonot as fraccisternae. and of these their

surface,

associated

could

TCA-precipitable but could in addition be addition determined

mechanism

detergent-soluble analysed capacities

endothelial A number frozen (1971), make without tives vents. useful locate roid tion gated used The to or or, This when by

cell.) of techniques

sectioning in order to of material

tissue, such

as those of Christensen

with and cvtoplasmic These ination

without the components.

of other

are being developed possible thin sectioning subjecting more method attempts radioautography of steroids precursor. that serum specffic having (e.g., Mikhail it to either importantly, should are be being after

brief indications is to be gained of of few lutein the

of where inforconcerning our unhardly scratch approaches. that ones these their

aqueous organic particularly made

fixasolto ste-

derstanding the surface Hopefully the next

cells available

they make clear however years should be exciting ways cells by which perform

a particular introduc-

a variety determination with bovine create already assay 1970; labeling the species has for use

for discoveries of the large and enigmatic vital function.

of a tagged

steroids albumin antisteroid a major Midgley

conjucan be antiimpact and By

ADAMS,

REFERENCES
E. C., AND HERTIG, A. T. (1969a). Studies on the human corpus luteum. I. Observations on the ultrastructure of development and regression of the luteal cells during the menstrual cycle. I. Cell Biol. 41, 696-715. ADAMS, E. C., AND HEwrzc, A. T. (1969b). Studies on the human corpus luteum. II. Observations on the ultrastructure of luteal cells during pregnancy. 1. Cell Biol. 41, 716-735. ALLEN, W. M., AND CORNER, C. W. (1930). Physiology of the corpus luteum. VII. Maintenance of pregnancy in rabbit after very early castration, by corpus luteum extracts. Fed. Proc. Fed. Amer. Soc. Exper. Biol. 27, 403. BEuw, M. E. (1972). Identification of peroxisomes in the rat adrenal cortex. J. Histochem. C!,tochem. 20, 173-179.

bodies is on steroid Niswender, peroxidase ulin to antibody marker probably method there roid ticulum) is (for

et al.,

1970).

of an anti-gammaglobin which the steroid a cytochemical microscopy can if stethe re-

been formed, in electron

be created. should prove compartmentalization example of at any the by of the

Such a cytochemical especially useful of association endoplasmic stages of synthesis. the with

membranes

smooth

180
BELT, AND

ENDERS

W.

D.,
and D.,

CAVAZOS,

L.
M. levels

F.,
in

ANDERSON,

L.
Cytoplasmic corpora

L.,

CHRISTENSEN,

A.

K., of

AND

CILLIM,

S. emphasis

W. and

(1969). function on (K. Applethose W.

MELAMPY,

R. relaxin
CAVAZOS,

(1971). porcine

The in of

correlation steroid-secreting the gonads. Ed.),

fine cells,

structure

granules lutea.
BELT, AND

with
16, pp.

Endocrinology
T.
KEAELINC.,

89,
L. R. levels pregnancy 2, sites R.

1-10.
F., (1970). in the and C. (1956). steroid
ANDERSON,

In
Chapt.

The New York.

Gonads. 415-488.

L.
structure luteum hysterecMitochon-

L.,

McKerns,

Fine corpus after

ton-Century-Crofts,

and of
BELT,

progesterone the W. pig during

COHERE,
(1967). lule sesse.

C.,

BRECHENMACHER,

C.,
ultrastructures au

AND

MAYER,

C.
Ia celgrosof the

Variations lut#{233}ale chez Ia

des ratte

de de
origin

tomy. drial

Biol.
D., structure

Reprod.
AND PEASE,

98-113. D. of On secretion.

cours

Ia

I. Microscopie
C.
luteum theca intema.
AND

in (1967). lutein

I.
of corpus Z.
AND

CORNER,

W.

6, 657-670. (1919). On the

the sow from

Biophys.
BJER5ING,

Biochem.
L. With and 82,

Cytol.
cells in reference

Suppl.
the the

2,
porcine to

369-375.

corpus and
Cnisp,

of

both

granulosa

ultrastructure endoplasmic synthesis. R. activity, of on ovine regression Z. M.

Amer.
BROWNING,

I. Anat.
H. lutea in

26,
C.

117-183.
(1968). The transstimu-

grnulosa luteum. reticulum

T. M.,
structure of

special steroid 187-211.

HAY,

fine plants lation. Cmsp, (1972). corpus at

of mice
DENYS,

corpora following

ovarian

hormone F., Endocrine Moon,

luteotrophin

Zellforsch.
BJERSING, SHORT,

Amer.
T. M., luteum The

I. Aunt.
fine of
DESSOIJKY,

L.,
R. I. end V. and Further of E.

M.

122, 169-192. F. R., AND CHANNING,

structure early pregnancy. of the

C. P.
canine

(1970). ultrastructure

histocorpora

chemistry lutea. the

Aunt.
DENYS,

Rec. F. R.
human during cycle.

observations the oestrous (1968a). cycle. Ovarian

172,
CRISP,

Zellforsch
cells.

298. T. M.,
The luteum progestational

D. A.,
structure early phase 37-70.

AND

111,

437-457.

(1970).

fine of 127,
BURTON,

of the

the and

BLANCHE1-rE,

J.

steroid

corpus the

pregnancy of

I. Differentiation
granulosa stage
BLANCHETTE,

of
cell the under E.

the

lutein
the influence

cell
of

from
exogenous

the

menstrual
AND

follicle and

during

preovulatory

Amer.
CROMBIE,

I. Aunt.
P. (1971). of H. W. the R., The

R.

D.,
Z.

ACKLAND,

gonadotrophins.

I. Cell

Biol. Biol.

31,
Ovarian

501-516.
steroid cells.

N. luteum

ultrastructure guinea-pig.

of

the

corpus

J.
cell.

(1966b). I. Cell Zur

Zellforsch.
lipids: in

115,
their Cy-

II.
BREINL,

The H.

lutein (1967).

31,

517-542.
der luteinzeldes

473-493.
DEANE,

feinstruktur

(1958).

Intracellular

len

w#{228}hrend

verschiedener C.,

funktionsphasen

detection
tology. University
DEANE,

and
(S.

gelbkorpers
CANIVENC,

der ratte. B., COHERE,

Endokrinologie
AND

51,

1-18.

significance In Frontiers L. Palay, ed.), pp. 227-263.

New
LOBEL,

Yale S. L.
normal preg-

BRECHENMACHER,

Press,

Haven.

C.
de

(1967).
Ia cellule

Quelques CR.
M. bei im

aspects
le 264,
Sd.

lut#{233}ale chez

ultrastructuraux blaireau (Meles

1187-1189. von einschlus-

H. W.,
ovaries and the

B. L.,
the

AND

ROMNEY,

(1962). human nancy,

Enzymic of early
AND

histochemistry menstrual puerperiuni.

RUBIN.

of cycle,

meles
CARSTEN,

L.).
P.

Acad.
(1965).

Elektronenmikroskopische corpus L.
KRAELING,

Amer. (1965).
synthesize gonads species.
AND

J. OhIdentisteand pla-

probleme skorpern

strukturdentungen menschlichen 552-568.

stet.
DEANE,

luteum.
BELT,

Arch.
W. D.,
AND

Gynecol. H. W.,
and hormones of

83, 28 1-294. B. L.
cells adrenal, mammalian 54,
HAY,

Gynak.
CAVAZOS, HENRICKS,

200,
L. F.,

fication L., Fine corpus cycle. roid centae

control in various the

of

that

ANDERSON,

D.
B. the C. P. M. levels

M.,
in estrous (1970).

R.
structure luteum

R.,
of

Arch. R.
corpus

MEI1IPY, progesterone pig 83-108.

CHANNING,

(1969). the

and
the

Aunt.
DINGLE,

Microscop. J. T.,

49-66. M. F.,
function

Moon,
in the

M.

during

Biol.

Reprod. of the
upon culture. sections with

1, in

(1968). luteum
DODGE,

Lysosomal

Influences
environment cells in tissue 589-822. thin microscopy, and
AND

vivo Rec.
CHRISTENSEN,

and

in

vitro
of A.

hormonal

R.
tion 87,

of the sheep. 1. Endocri no!. 40, 325-336. A. H., CHRISTENSEN, A. K., AND CLAYTON, B. (1970). Localization of a steroid 11in rat adrenal the inner membrane subfracof mitochondria. LysoSomes and Pathology. eds.), pp.

luteinization

granulosa

p-hydroxylase 254-261.

Frog.
fresh

Hormone
K. for of A. pancreas K., tissue

Res.
(1971). electron

26,
Frozen

Endocrinology
and tract. lysosomal

of

Dorr,
enzymes somes and Holland,
ENDERS,

H.
in H.

M.
in

(1969).
the

a description

liver.
FAWCETT,

I. Cell Biol.
D.
of opossum

reproductive

In

LysoDingle North-

51,
(1961).

772-804. W.
The normal fine cells. structure

CHRIsFEN5EN,

Biology B. Fell, London.

(J.
330-360.

T.

testicular

interstitial

I. Biophys.

Biochem.

A.

C.

(1962).
cells.

Cytol.

9, 653-670.

structure

of lutein

Observations I. Cell Biol.

on the fine 12, 101-113.

CYTOLOGY

OF

COJIPUS

LUTEUM

181
luteum in
AND

ENDERS,

A.

(1966).

The
armadillo

the tion 295-310.

ENDER5,

nine-banded in Mammals. Academic A. C., on

AND

reproductive (Dasypus
Biology of York. R. (1964). of rat. I. lutein

cycle of novemReproduc-

of
VAN

the

corpus

rabbits
MADDEN,

and

rats.

Folio (1965).
involu-

Endocrinol.
LENNEP,

cinctus).

In Comparative (I.
Press,

Jap. 41, E. W.,

microscopic the D. of with human (1956). the earlier

994-1009.

L. M.
on of
on

W.
W.

Rowlands,
New

ed),

pp. Obsercells.

Electron tion tion.

LEVER,

observations corpus luteum

the

of

menstruaelectron and the comadrenal

LyoNs,
fine

Z. Zellforsch.

66, 365-380.
Remarks

vations

the hormone

structure

J.

the
on

II.

The

effects

of

hypophysectomy
in the

motrophic

and mamCell Biol. 22,

AND
WARREN,

microscopy parison cortex.

rat

corpus observations 11-126.

AND

luteum:

127-141.
ENDERS,

R.

A. (1966).

C.,

SCHLAFKE,

S.
of the armadillo. A. the Press, R.

J.,
fetal

MIDGLEY,

Aunt. A.

Rec. R.,

124,
JR.,

NISWENDER,

Cytology of the

zone

of

the

(1970).

Radioimmunassay

of 147,

steroids.

C. D. Acta EnVAN

adrenal

gland

Anat.
C. mink. ed.), H. cells (1963). tract

Rec.

154,
Morduring

docrinol.
MIKHAIL, DE

(Kbh.)

Suppl.

807-822.
ENDERS,

C.,
WIELE,
estrone Suppl. P.

Wu,
R.
and 147, delle

C. L.

R. K.,
of the

AND

ENDERS,

H., (1970).

FERIN,

phology delayed Implantation. University

E5PEY,

female in C. (A.

reproductive Enders,

of

estradiol. 347-365. Particolari cellule

320-331. M., AND Radioimmunoassay Acta Endocri

ultrastructurali

nol.
dei

implantation of Chicago
AND

In
pp.

Delayed
129-139. Exmem-

(Kbh)
MOTTA,

(1966).

Chicago. (1972). of the follicles.

mitocondri abile

luteiniche

Ioro

prob-

L.
of

L.,
granulosa

STurrs, between in rabbit

significato.

Boll.
AND WEBER,

Soc. A. F.
bovine A. analysis F.

Ital. (1968a).
graaflan (1968b). of the

Sper.

42, Ultrafollicle Quan-

change branes

cytoplasm

1269-1271.
PRIEDICALNS,

ovarian

Biol. A. L.

J.,

Reprod.
FAWCEYT,

6, 168-175. D. T., LONG,

The

structural

studies luteum.

of

the

J. A.,

AND

JONES,

and
PRIEDKALNS,

corpus

Z. Zellforsch.
WEBER,

91, 554-573.
follicular

(1969). glands.
FLAKS,

ultrastructure

of

endocrine Some oblutein

J.,

AND

Rec. B.,
of
im

Frog.
on the

Hormone
P. fine rat

Res.
structure ovary. N. rat

25, 315-380.
of the

titative

ultrastructural

BRESLOFF,

(1966).

servations cells

and luteal cells of Zellforsch. 91, 574-585.

QUATACKER,

the

bovine
Formation

ovary.
of corpus autoluteum

Z.

X-irradiated
AND,

I.
B. adrenal

Cell
(1972).

Biol.
A cortex.

J.
vacuoles

R.

(1971). during

30,
FRIEND,

227-236. D. S.,
cell

phagic
involution.

human

Cn.uLA,
in the

Z.

Zellforsch.
SVOBODA,

Mikrosk.
D. (1972). in

Aunt.
Microbodies interstitial

122,

distinctive

contact

479-487.
REDDY,

J. Cell Biol.
CILLIM, MCLENNAN,

S.
human

53, 148-163. W., CHRISTENSEN,

C. menstrual secretory
AND

J., AND
the testis.

A.
Fine luteum at

K.,
structure its

(peroxisomes)
AND

identification

cells

of
RENNELS,

E.

(1969). corpus activity.

of stage

J.
(1966).
luteal immature

Histochem. Observations
cells from rats.

Cytochem. on
PMS and

20,

the of 126,
GREEN,

140-142.

maximum 409-428.

Amer. M.
I.

I. Aunt.
Ultracell.

E.
treated M. H.,

C.
of

the

ul79,
AND

trastructure HCC

PMS-

J. A.,
of

MAQUEO,

(1965).
The luteal

Endocrinology
LANMAN,

structure

the

human

ovari.

373-386.
Ross,
LIND, PAPPAS,

Amer.
CURAYA,

J.
5. and

Obstet.
(1971).

Gynecol.
Morphology, of human
hormone

92,

946-957.
histochemistry ovarian compart-

C.
Electron

D.,

J. T.,
in

J.
on

(1958). the fetal 659-661.

microscope reticulum

observathe

tions human

endoplasmic adrenal.

and ments

biochemistry
steroid

synthesis.

Fhysiol.
ultraliver of mitoconto

J. W.,

Biophys.
AND

Biochem.
KUMARI,

Rev.
structural

51,

785-897.
C. R. (1972). in Energy-linked isolated Preservation compared transformations

Cytol.
SAVARD,

4,
K.,

LE
in (K.

MAmE,
the W. corpus McKerns,

L. The 5, pp. The York.

HACKENBROCK,

(1969). precursors Gonads. 119-133.

ScALLEN,

Progesterone

synthesis luteum. ed), S. E.

from

labeled

In
Chap. New (1969).

chondria
figurations chemical
HASHIMOTO,

and
by fixation.

mitoplasts.
freeze-cleaving I.
WIEST,

Appleton-Century-Crofts,

Cell
W.
mechanisms

Biol.
C.

I.,
and

AND

53, 450-485. (1989). Luteoin rat

trophic

luteolytic

corpora

lutea.
HJORTECAER SEN,

EndocrInology

84,

886-892.

T. J., AND DIrnzsT, quantitative retention of liver prepared for electron tion in a digitonin-containing A. A., (1971a). Fine of the raccoon Mikrosk. Mat.
SEAL,

cholesterol microscopy aldehyde

S.,
AND
DOE,

in

mouse
by fixasolution. R. P.

PEDERSEN, P. S., ANn FcK LARJ. (1988). The ultrastructure of the human granulosa lutein cell of the first trimester of gestation. Acta Endocrlnol. 58, 481-496.

1. Cell Biol. 40, 802-813.

SINHA,

U.

KIOZIJMI,

T.

(1965).

Electron

microscopic

study

structure of the during pregnancy. 117, 35-45.

corpus

luteum

Z. Zellforsch.

182
SINHA,

ENDEBS

A.

A.,

SEAL,

U.

S.,
of

AND

DoE,

R.

P.

tion

of

the

endometrium.

Folio

Morph.

(Praha)

(1971b).

Ultrastructure

the

corpus

of
Amer.
SISSON,

the J.,

white-tailed
1. Aunt.
AND

deer
189-208.

during
W. cells H.

luteum pregnancy.
Fine primate

15, 375-383.
WATTENDERG,

132,

tochemical
(1987). of a
hydrogenase

L. W. (1958). demonstration of
in tissue sections.

FARRENBACH,

Microscopic hissteroid-3-ol de1. Hi.stochem.

structure

of

steroidogenic

cutaneous organ. Amer. I. Aunt., 121, 337-368. SonorrA, J. (1896). Uber die bildung des corpus luteum bei der maus. Arch. Mikr. Aunt. 47, 261308. sOBorrA, J. (1897). Uber die bilding des corpus luteum beim kaninchen. Aunt. Hefte. 8, 469-521. SOBOTrA, J. (1906). Uber die bildung des corpus luteum beim meerschweinchen. Aunt. Heft. 32, 89-142. SmAuss, J. F. III, Foi.Fx, B., im STAMBAUGH, R. (1972). 20-a-Hydroxysteroid dehydrogenase activity in the rabbit ovary. Biol. Reprod. 6, 78-86. TOKIDA, A. (1965). Electron microscopic studies of the corpora lutea obtained from normal human ovaries. Mie Med. 1. 15, 27-76.
VACEK,

6, 225-232. WHALEY, W. C., DAUWALDER, M., AND KEPHART, J. E. (1972). Golgi apparatus: influence on cell surfaces. Science 175, 598-599. WEINSTEIN, R., AND McNurr, N. S. (1972). Cell junctions. New England J. Med. 286, 521-524. WIE5T, W. C., AND KIDWELL, W. R. (1989). The regulation of progesterone secretion by ovarian dehydrogenases. In The Conads. (K. W. McKerns, ed.), Chap. 11, pp. 295-320. Appleton-Century-Crofts, New York. YAMADA, E., AND ISHIKAWA, T. M. (1960). The fine structure of the corpus luteum in the mouse

Cytochem.

ovary
Kyushu
YATES,

as R. D.,

revealed
Sd.

by

electron

microscopy.

J. Med. Fine
of

11, 235-259.

Anr,
opaque

K.,
structure Syrian

AND

RAPPOPORT,

(1987).
position

and
cytoplasmic hamsters.

chemical
bodies

D. A. comof

Z.

(1967).

Ultrastructure

and

enzyme

histochemistry of the corpus luteum and its correlation to the decidual

graviditatis
transforma-

triparanol Res. 47,

treated 459-478.

Exp.

Cell