Developmental and Comparative Immunology 39 (2013) 7278

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Developmental and Comparative Immunology

journal homepage: www.elsevier.com/locate/dci

Review

Maternal immunity in sh
Shicui Zhang a,, Zhiping Wang b, Hongmiao Wang a
a
b

Institute of Evolution and Marine Biodiversity and Department of Marine Biology, Ocean University of China, Qingdao 266003, China
Department of Life Science, Weinan Teachers University, Weinan 714000, China

a r t i c l e

i n f o

Article history:
Available online 28 February 2012
Keywords:
Fish
Maternal immunity
Maternal transfer
Egg
Yolk proteins

a b s t r a c t
Both innate and adaptive immune-relevant factors are transferred from mother to offspring in shes.
These maternally-transferred factors include IgM, lysozymes, lectin, cathelicidin and complement
components. Recently, yolk proteins, phosvitin and lipovitellin, have been shown to be maternallytransferred factors, functioning in the defense of teleost larvae against pathogens. Among these factors,
the mode of action of complement components and yolk proteins has been explored, whereas that of
all the other factors remains elusive. At present, the transfer mechanisms of maternally-derived immune
factors are largely unknown although those of IgM and yolk protein transmission from mother to offspring have been reported in some shes. Maternal transfer of immunity is affected by many elements,
including biological factors, such as age and maturation, and environmental conditions experienced by
brood sh, such as pathogens and nutritional supply. Practically, the manipulation of maternal immunity
transfer can be used to enhance the survival rate of sh larvae.
2012 Elsevier Ltd. All rights reserved.

Contents
1.
2.

3.
4.

5.

6.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Transfer of maternally-derived immune factors. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Vg-derived proteins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Complement components . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Mode of action of maternally-derived immune factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Mode of maternally-derived immune factor transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
IgM . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Yolk proteins . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Factors affecting maternal immunity transfer . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.1.
Nutrients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
5.2.
Pathogens. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Possible applications in fish culture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1. Introduction
Maternal immunity refers to the immunity transferred across
the placenta, colostrum, milk or eggs from mother to offspring,
which is supposed to play a key role to protect the vulnerable
Abbreviations: Vg, vitellogenin; Pv, phosvitin; Lv, lipovitellin; CP, classical
pathway; AP, alternative pathway; LP, lectin pathway; MBL, mannose-binding
lectin; PAMPs, pathogen-associated molecular patterns; LPS, lipopolysaccharide;
LTA, lipoteichoic acid; PGN, peptidoglycan.
Corresponding author. Address: Room 205, Ke Xue Guan, 5 Yushan Road, Ocean
University of China, Qingdao 266003, China. Tel.: +86 532 82032787.
E-mail address: sczhang@ouc.edu.cn (S. Zhang).
0145-305X/$ - see front matter 2012 Elsevier Ltd. All rights reserved.
doi:10.1016/j.dci.2012.02.009

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offspring against pathogenic attacks. Maternal immunity was initially described in mammals and birds more than 100 years ago
(Ehrlich, 1892; Klemperer, 1893), and has now been documented
among different vertebrates such as mammals (Leach et al., 1990;
Dardillat et al., 1978; Gustafsson et al., 1994; Sadeharju et al.,
2007), birds (Kissling et al., 1954; reviewed in Brambell, 1970;
Heller et al., 1990; Bencina et al., 2005; Hamal et al., 2006), reptiles
(Schumacher et al., 1999), amphibians (Poorten and Kuhn, 2009)
and shes (reviewed in Zapata et al., 2006; reviewed in Swain
and Nayak, 2009) as well as in invertebrates including insect
(Moret and Schmid-Hempel, 2001; Zanchi et al., 2011), shrimp
(Huang and Song, 1999) and amphioxus (Liang et al., 2009).

S. Zhang et al. / Developmental and Comparative Immunology 39 (2013) 7278

73

Fig. 1. A diagram showing the transfer and persistence of maternal immunity with respect to acquisition of immunocompetence at the different stages of development. Both
innate and adaptive immune-relevant factors are transferred from mother to offspring, which play a critical role to protect the vulnerable offspring against pathogenic attacks
before full development and maturation of immune system in sh.

Fish eggs are in most cases cleidoic, i.e. closed free-living system
following fertilization; they are therefore supposed to depend
upon the maternal provision of immune-relevant molecules for
protection against invading pathogens before full maturation of
immunological systems (Fig. 1). In the past two decades, the massive increase in aquaculture has put a greater emphasis on studies
of the immune system and defense mechanisms against diseases
associated with sh. As a result, a great stride has been made in
recent years on the defense roles of maternally-derived factors in
embryos and larvae in shes, and our knowledge as such has
dramatically increased. Below we will discuss the transfer of
maternally-derived immune factors, mode of action of maternally-derived factors, mode of maternally-derived factor transfer,
factors affecting maternal immunity transfer and possible
application in sh culture, with a special emphasis on vitellogenin
(Vg)-derived proteins and complement.
2. Transfer of maternally-derived immune factors
Previous studies on several sh species have shown that maternal IgM is able to be transferred from mother to offspring
(Van Loon et al., 1981; Bly et al., 1986; Mor and Avtalion, 1990;
Fuda et al., 1992; Castillo et al., 1993; Breuil et al., 1997; Olsen
and Press, 1997; Hanif et al., 2004; Picchietti et al., 2004, 2006;
Swain et al., 2006). Likewise, maternal transfer of the innate immune factors including the complement component C3 (Ellingsen
et al., 2005; Huttenhuis et al., 2006; Lvoll et al., 2007; Wang
et al., 2008, 2009), lectins (Bildfell et al., 1992; Tateno et al.,
2002; Jung et al., 2003; Dong et al., 2004; Hasan et al., 2009),
lysozymes (Yousif et al., 1991, 1994; Wang and Zhang, 2010) and
cathelicidin (Seppola et al., 2009) to offspring has also been
reported in different teleost species. Moreover, immunization of
parents results in a signicant increase in IgM levels (Mor and
Avtalion, 1990; Sin et al., 1994; Oshima et al., 1996; Hanif et al.,
2004) and lysozyme activities (Hanif et al., 2004) in the eggs
compared to control. These maternally-derived immune factors
have been elegantly reviewed by Mulero et al. (reviewed in Mulero
et al., 2007) and Swain and Nayak (reviewed in Swain and Nayak,
2009). Here we will only describe the transfer of Vg-derived
proteins and complement components because their immunological function in sh embryos and larvae has been experimentally
tested.

2.1. Vg-derived proteins

Vg is an egg yolk precursor protein, present in the females of all
oviparous species including sh, amphibians, reptiles, birds, most
invertebrates and the platypus. Vg is usually synthesized extraovarianly and transported by the circulation system to the ovary,
where it is internalized into growing oocytes and proteolytically
cleaved to generate yolk proteins, phosvitin (Pv) and lipovitellin
(Lv), that are later used as the nutrients by developing embryos
(Arukwe and Goksyr, 2003; reviewed in Finn and Fyhn, 2010).
Vg was initially regarded as a female-specic protein (Pan et al.,
1969); however its synthesis, albeit in smaller quantities, has been
shown to occur in male and sexually immature animals (reviewed
in Engelmann, 1978; Piulacks et al., 2003). These suggest that Vg
may, in addition to being involved in yolk protein formation, play
a role independent of gender. Recently, Vg has been shown to be
an immune-relevant molecule involved in the defense of host
against the microbes including bacterium (Zhang et al., 2005; Shi
et al., 2006; Li et al., 2008, 2009; Liu et al., 2009; Tong et al.,
2010; reviewed in Zhang et al., 2011) and virus (Garcia et al., 2010).
Pv and Lv, that both are proteolytically cleaved products of Vg,
are naturally transferred from mother to eggs in sh. They are traditionally considered as the yolk reserves of nutrients essential for
growth and development (reviewed in Finn and Fyhn, 2010). As Vg
has been demonstrated to be an immune-relevant molecule, we
thus hypothesize that its derived proteins, Pv and Lv, may also play
an immunological role in developing embryos and larvae. As
expected, Pv was proven to possess an antimicrobial activity in
zebrash embryos and larvae (Wang et al., 2011). In line with this,
chicken egg yolk Pv was also shown to be able to inhibit the
growth of the Gram-negative bacterium Escherichia coli (Sattar
Khan et al., 2000). Similarly, sh native Lv was associated with
the immune defense of rosy barb embryos and larvae (Zhang and
Zhang, 2011). All these demonstrate that Pv and Lv are
maternally-transferred proteins involved in both nutritional
supply and immune defense in embryos and larvae in shes
(Fig. 1).
2.2. Complement components
Complement system consisting of approximately 35 plasma and
membrane-bound proteins comprises one of the rst lines of

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S. Zhang et al. / Developmental and Comparative Immunology 39 (2013) 7278

defense against pathogenic infection by alerting host the presence

of potential pathogens as well as clearing pathogens. There are
three pathways by which the complement system can be activated: the classical pathway (CP), alternative pathway (AP) and
lectin pathway (LP). The CP activation is initiated by binding of
antibody to the C1 complex, formed by C1q and two serine proteases (C1r and C1s), or by direct binding of the C1q component to
the pathogen surface, and requires both Ca2+ and Mg2+ (reviewed
in Ruddy, 1974; reviewed in Robertson, 1998; Kishore and Reid,
2000; reviewed in Trouw and Daha, 2011). The AP is mainly
triggered by the certain structures on microbial surface in an
antibody-independent manner, and requires Mg2+ alone (reviewed
in Yano, 1996; Zhang et al., 2003). The LP is activated by binding of
microbial polysaccharides to circulating lectins, such as mannosebinding lectin (MBL), and requires Ca2+ (reviewed in Morgan, 1995;
reviewed in Turner, 1996; Thiel et al., 1997; reviewed in Willment
and Brown, 2008). These three pathways merge at a common
amplication step involving the formation of unstable protease
complexes, named C3-convertases (C3bBb in alternative pathway
and C4b2a in classical/lectin pathways), and the cleavage of C3
to generate C3b and proceed through a terminal pathway that initiates the assembly of a membrane attack complex, which leads to
complement-mediated lysis. Different complement components
such as C3, C4, C5, C6, C7, factor B (Bf) and factor D have been demonstrated to be transmitted from mother to offspring in rainbow
trout (Lvoll et al., 2006), carp (Huttenhuis et al., 2006; Shen
et al., 2011), spotted wolfsh (Ellingsen et al., 2005) and Atlantic
salmon (Lvoll et al., 2007). Recently, we have found that both
C3 and Bf, the key factors functioning in the AP, are present in
the newly fertilized eggs of Danio rerio, providing the rst evidence
for a maternal transfer of the complement proteins in zebrash
(Wang et al., 2008, 2009).
Maternal complement components in sh eggs have been proposed to be associated with the early defense against pathogens
in developing embryos and larvae. However, rm evidence to support this is rather limited. We showed for the rst time that the
Gram-negative bacterium E. coli is sensitive to lysis by the cytosol
prepared from the fertilized eggs of zebrash, and the bacteriolytic
activity was abolished by pre-incubation of anti-C3 antibody with
the egg cytosol, a process that would cause the precipitation of the
central component of all known complement pathways, C3. Moreover, the lytic activity was depleted by heating at 45 C, a temperature known to inactivate sh complement (reviewed in Zarkadis
et al., 2001). Furthermore, maternal immunization caused a
remarkable increase in C3 and Bf in the mother and a corresponding increase in the offspring, and accordingly, the embryos derived
from immunized D. rerio were signicantly more tolerant to the
pathogenic bacterium Aeromonas hydrophila than those from
unimmunized mother (Wang et al., 2009). These data show that
complement factors are indeed transferred from mother to eggs,
and these maternally-transferred complement factors clearly
participate in the immune response protecting the developing
embryos from pathogenic attacks.
3. Mode of action of maternally-derived immune factors
Eggs of most sh are released and fertilized externally, and the
resulting embryos and larvae are therefore exposed to an aquatic
environment full of potential pathogens (reviewed in Zapata
et al., 2006). Maternally-transferred immunity can not only protect
sh embryos and larvae against pathogenic agents present in the
environment but also prevent them from vertical transfer from
mother to offspring. Although the exact mode of action of maternally-transferred immune factors in the early stages of sh remains to be studied, different factors appear to function in
different fashions. For example, maternally-transferred lysozymes

may catalyze hydrolysis of 1,4-beta-linkages of bacterial cell walls,

thereby causing bacterial lysis (Huttenhuis et al., 2006); maternally-transferred lectins may interact with pathogenic surface carbohydrates leading to opsonization, phagocytosis or activation of
complement (reviewed in Alexander and Ingram, 1992; Yousif
et al., 1994; Tateno et al., 1998); and maternally-transferred cathelicidin may exert an inhibitory effect on bacterial growth via
degrading into small peptides (Broekman et al., 2011; Lu et al.,
2011) or stimulating the release of cytokines enabling a more
effective response to invading pathogens (Bridle et al., 2011).
Immunoglobulins such as IgM can opsonize bacteria, resulting in
their degradation and eradication by phagocytic cells. Maternally-transferred IgM in eggs and embryos may also act as an
opsonin, facilitating the phagocytosis of opsonized bacteria by
phagocytes (reviewed in Holland and Lambris, 2002).
To explore the underlying mechanisms how Vg-derived yolk
proteins are involved in immune defense, we performed the protein-microbe interaction analysis and enzyme-linked immunosorbent assay. It was found that both Pv and Lv were able to
bind to the Gram-negative bacterium E. coli and the Gram-positive bacterium Staphylococcus aureus. In agreement, they were
also able to bind to the microbial conserved components, called
pathogen-associated molecular patterns (PAMPs), including lipopolysaccharide (LPS) of Gram-negative bacteria, peptidoglycan
(PGN) of both Gram-negative and positive bacteria and lipoteichoic acid (LTA) of Gram-positive bacteria (Wang et al., 2011;
Zhang and Zhang, 2011). These indicate that Pv and Lv are both
multivalent pattern recognition receptors (PRR) capable of recognizing Gram-negative as well as positive bacteria via interaction
with PAMPs. In addition, we showed by scanning electron
microscopy that Pv was able to cause lysis of both E. coli and
S. aureus (Wang et al., 2011), and by phagocytosis test that coating of E. coli and S. aureus with Lv facilitated the phagocytosis of
these bacteria by macrophages (Zhang and Zhang, 2011). These
denote that Pv is an effector molecule capable of killing bacteria
directly, whereas Lv is an opsonin capable of enhancing macrophage phagocytosis.
To determine how maternally-transferred complement factors
function in the early stages of zebrash, the antibodies against
C1q (a key component of CP), C4 (a key component of both CP
and LP) and Bf (a key component of AP) were utilized to block
the CP, LP or AP, respectively. It was found that precipitation of
C1q and C4 caused little loss of the bacteriolytic activity of the
egg cytosol, whereas precipitation of Bf resulted in a signicant
reduction of the lytic activity. Furthermore, addition of EGTA to
remove Ca2+ from the egg cytosol, which can inhibit both CP
and LP, induced little decrease in the bacteriolytic activity. In
contrast, pre-incubation of EDTA with the egg cytosol led to a
substantial reduction of the bacteriolytic activity, and saturation
of the chelator with Mg2+ was capable of restoring the lytic activity, but not by addition of Ca2+. Moreover, selective inhibition of
the AP by zymosan A induced a marked loss of bacteriolytic
activity, while addition of L-lysine, an inactivator of the CP, was
not inhibitory. All these clearly indicate that maternally-transferred complement components in sh eggs operate via the AP,
protecting embryos and larvae against pathogenic attack (Wang
et al., 2008).

4. Mode of maternally-derived immune factor transfer

The mode of IgM and yolk protein transfer from mother to offspring has been reported in some sh, but as a whole the mode of
maternally-derived immune factor transfer remains largely unknown. Here our discussion will focus on the mode of IgM and yolk
proteins in sh.

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4.1. IgM

5. Factors affecting maternal immunity transfer

In mammals, maternal immunoglobulin G (IgG) is transported

across the placenta from mother to fetus. IgG from breast milk in
many mammalian species (rodents, bovines, cats, ferrets, etc.) is
also transported across the intestinal epithelium into the neonatal
circulation. In contrast, maternal IgM is transferred from mother to
offspring through yolk in birds, reptiles and shes. Maternal transfer of IgM has been demonstrated in different shes. In oviparous
shes, maternal IgM is initially transferred via yolk to immature
oocytes during vitellogenesis and then to eggs and yolk sac larvae
in a sequential manner (Kanlis et al., 1995). In viviparous shes
such as Neoditrema ransonneti (Embiotocidae), IgM is secreted from
the epithelia of the ovigerous lamellae of pregnant females into
ovarian cavity uid and absorbed by enterocytes of the hypertrophied hindgut in fetus (Nakamura et al., 2006).
The transplacental transfer of mammalian IgG involves an Fc
receptor-mediated transcytosis of IgG across the syncytiotrophoblast barrier and a transcellular pathway through the endothelium
of fetal capillaries (reviewed in Simister, 2003; Fuchs and Ellinger,
2004). Analogously, maternal IgM is also transferred to piscine
eggs by the transcytosis across follicle cells (Picchietti et al.,
2006). In the entire IgM transfer process, follicular cells probably
play an active role because of the presence of IgM within thecal
and granulosa cells (and in the interposed basement membrane)
of pre-vitellogenic and vitellogenic follicles. Further studies should
be performed to dene if Fc receptors are present in the oocytes
and involved in the process of IgM transfer to the oocytes.
Maternal IgM can also be incorporated into sh oocytes
together with Vg. This is supported by the facts that IgM concentration in Pagrus major oocytes was increased throughout vitellogenesis (Kanlis et al., 1995) and detection of IgM was limited to
the mature ovary of Cyprinus carpio (Suzuki et al., 1994). However,
autogenous IgM synthesis and/or transfer of IgM mRNA are also
possible because a signicant level of IgM gene transcription has
been observed in teleost oocytes (Picchietti et al., 2006). Therefore,
a detailed study is needed to establish the mode of maternal IgM
transfer in different sh species.

Many factors affect the immunity of brood sh, thereby exerting an inuence on the transfer of maternal immunity to offspring,
especially when shes are experienced a pathogenic condition
prior to the egg production period. These factors include water pollution (reviewed in Schwedler et al., 1985), adverse environmental
conditions (Miller and Clen, 1984; reviewed in Zapata et al., 1992;
Swain et al., 2007; reviewed in Bowden et al., 2007; Valenzuela
et al., 2007) and stress conditions like handling (Ellsaesser and
Clem, 1986) and crowding (Klinger et al., 1983; Ortuno et al.,
2001) as well as some biological factors such as age, maturation
and reproduction (Slater and Schreck, 1993; Suzuki et al., 1996,
1997; reviewed in Harris and Bird, 2000). Here we only briey discuss the effects of nutrients and pathogens on brood sh immunity
and its transfer from mother to offspring.

4.2. Yolk proteins

During oogenesis in the chicken, Vg is taken up into the growing
oocytes via a member of the low density lipoprotein receptor gene
family termed LR8 (Bujo et al., 1994). This ligand-receptor mediated endocytosis of Vg is accompanied by degradation of the yolk
precursor protein by cathepsin D, generating Pv and Lv deposited
in yolk granules (Barber et al., 1991; Schneider, 1996). The receptor
exists in two isoforms that differ by a so-called O-linked sugar domain; the shorter form (LR8 ) is present exclusively in the oocytes
proper, and the longer protein (LR8+) predominates in somatic cells
(Hermann et al., 2000). Vg receptor is localized in coated pits on
the surface of growing oocytes and is of vital importance to egglaying hen. Similarly, transfer of Vg into piscine growing oocytes
is also dependent upon their plasma membrane receptor for Vg.
Vg receptors from white perch, tilapia, salmon and rainbow trout
were shown to share key structural elements (e.g. an eight-repeat
ligand-binding domain) with Vg receptors from chicken (Stifani
et al., 1990; Hiramatsu et al., 2004a). Multiple ovarian Vg receptors
have been reported in white perch and rainbow trout (Tyler and
Lubberink, 1996; Hiramatsu et al., 2002; Reading et al., 2011), that
may be responsible for interaction with different types of Vg proteins. It has been found that the lipovitellin domain of teleost Vg
mediates its binding to the oocyte receptor (Stifani et al., 1990;
Hiramatsu et al., 2002, 2004b). Interestingly, Vg receptor can be
recycled to the oocyte surface during the vitellogenic growth phase
(Perazzolo et al., 1999; Hiramatsu et al., 2004a).

5.1. Nutrients
Role of nutrition and its effect on immunity and disease resistance have been established in sh as well as in other aquatic
animals (reviewed in Blazer, 1992; reviewed in Lall and Olivier,
1993). Thus, transfer of maternal immune factors from mother to
offspring is particularly sensitive to the availability of specic
nutrients or minerals that are required as materials or precursors
for the synthetic process of immune factors. Poor nutrient supply
or unreasonable proportioning of supplied nutrients will depress
the maternal synthesis of immune factors, and hence decrease their
quality and quantity transferred to offspring. Previous studies have
shown that availability of nutrients such as protein, vitamins, fat and
fatty acid all affects the growth, maturation, reproductive performances (including the process of vitellogenesis, fertilization and
hatchability) and immunity of brood sh (reviewed in Swain and
Nayak, 2009), and then impairs embryonic development and larval
health. For example, L-ascorbic acid supplementation in broodstock
diet has been correlated with lysozyme activity in sea bass embryos
and larvae (Cecchini et al., 2000). It is clear that the nutrients for female sh exert a profound inuence on the synthesis and vertical
transfer of maternal immune factors, and hence on the egg quality
and health status of offspring at early stages. However, information
as such is rather limited, and needs further study.
5.2. Pathogens
The environment experienced by brood sh during vitellogenesis affects the quality and quantity of the immune factors transferred to offspring. The females that have not been exposed to
particular pathogens will not synthesize antibody specic to those
pathogens and their immune responses remain at low levels, leading to the limited transfer of maternal immunity, therefore, their
offspring are susceptible to infection. In contrast, the mothers exposed to particular pathogens will synthesize more immune factors
including both adaptive and innate immune components, these factors can then be transferred to offspring, helping them to mount rapid and efcient immune responses when challenged with the same
pathogen. For example, immunization of female shes with different pathogens not only enhanced the vertical transfer of maternally-derived immune factors but also improved the survivability
of their offspring (Mor and Avtalion, 1990; Sin et al., 1994; Oshima
et al., 1996; Hanif et al., 2004; Swain et al., 2006; Wang et al., 2009).
6. Possible applications in sh culture
Signicant mortality is routinely recorded at larval and post
larval stages of shes over the world, and how to enhance the

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S. Zhang et al. / Developmental and Comparative Immunology 39 (2013) 7278

survival rate of sh larvae is a problem of practical importance.

Moreover, sh larvae have no or only limited immune response
ability before the maturation of their immune system, thus direct
immunization on them can not improve their immunity. As maternally-transferred immune factors have been proven to be able to
transfer from mother to offspring and enhance the immunity of
sh larvae, maternal immunity can therefore be used as an
alternative strategy to promote the immunity of sh larvae, thus
increasing their survival rate. Practically, this can be easily
achieved by feeding brood sh with specic nutrients like vitamins
or immunizing brood sh with vaccines like inactivated pathogens.
Acknowledgements
This work was supported by Grants of Ministry of Science and
Technology of China (2012CB114404) and Natural Science Foundation of China (30972274) to SCZ.
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