Haxenna 2006 WD Gluco

Accepted Manuscript
Title: Tip cells: master regulators of tubulogenesis?
Author: Helen Weavers Helen Skaer
PII: S1084-9521(14)00080-9
DOI: http://dx.doi.org/doi:10.1016/j.semcdb.2014.04.009
Reference: YSCDB 1562
To appear in: Seminars in Cell & Developmental Biology
Received date: 4-3-2014

Revised date: 26-3-2014
Accepted date: 1-4-2014
Please cite this article as: Weavers H, Skaer H, Tip cells: master regulators
of tubulogenesis?, Seminars in Cell and Developmental Biology (2014),
http://dx.doi.org/10.1016/j.semcdb.2014.04.009
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Tip cells: master regulators of tubulogenesis?
Helen Weavers+,$ and Helen Skaer+,*
+
Department of Zoology, Downing Street, Cambridge CB2 3EJ, UK
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Current address: School of Biochemistry, Medical Sciences,• University Walk,
Bristol BS8 1TD, UK
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*
author for correspondence
Tel: 44-1223-763189
e-mail: hs17@cam.ac.uk
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Highlights
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Keywords
Page 1 of 30
Contents
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1.
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2.1
2.2
2.3
2.4
2.5
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2.6
2.7
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Page 2 of 30
Abstract
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Page 3 of 30
Introduction
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Dictyostelium
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Page 4 of 30
1. Tip cell specification and selection
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Drosophila
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Breathless
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Drosophila
Page 5 of 30
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achaete scute
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Dictyostelium
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Page 6 of 30
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C. elegans
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2. Tip cells regulate tubulogenesis
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Page 7 of 30
2.1 Mitogenic signalling: tip cells pattern cell proliferation
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C. elegans
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Page 8 of 30
Drosophila
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, Rhodnius
Drosophila
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2.2 Tip cell directed tube migration and navigation
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. C.elegans
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Drosophila
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Page 9 of 30
Drosophila
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2.3 Tip cells promote branching morphogenesis

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Page 10 of 30
,
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sprouty2, bmp2 & 4 and sonic hedgehog
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Page 11 of 30
2.4 Tip cell driven tube elongation by cell intercalation
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Drosophila
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Drosophila
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2.5 Tip cell anchorage and looping morphogenesis
Page 12 of 30
Drosophila
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Ptychoptera
, D. funebris
Page 13 of 30
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2.6 Fusion at the tips: creating tubular networks

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In the development of both the insect tracheal system and vertebrate vasculature, sets of
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discontinuous tubular elements must be connected to generate a fully functional tubular

network.
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In the Drosophila tracheal system, fusion cells are specified at the distal ends of the tracheal
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branches and act to interconnect independent or distant tracheal tubes (Figure 3D). The
processes underlying fusion are described by Luschnig in this issue and include fusion cell
contact through their dynamic filopodial activity, E-cadherin-mediated adhesion, followed by
cell contraction and apical membrane deposition to form a continuous lumen (Samakovlis et
al., 1996; Lee and Kolodziej, 2002; Gervais et al., 2012). Very similar events occur during
anastomosis (blood vessel fusion) in the vertebrate vasculature (Ellertsdóttir et al., 2010;
Lawson and Weinstein, 2002). Indeed recent real-time in vivo imaging studies in zebrafish
are beginning to elucidate the cellular mechanisms that govern vascular anastomosis (Herwig
et al., 2011).
Page 14 of 30
Drosophila melanogaster
D. funebris
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2.7 Tip cells as ‘master regulators’ in tubulogenesis
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C. elegans
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Drosophila
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Page 15 of 30
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3. Tip cell roles in tubule physiology
Page 16 of 30
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Acheta domestica
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Concluding remarks
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Acknowledgements
Page 17 of 30
Figure legends
Figure 1. Examples of tip cells
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Figure 2. Strategies for tip cell selection

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blistered escargot
Page 18 of 30
Figure 3. Tip cells regulate multiple steps of organogenesis
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References
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51
Page 19 of 30
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124
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74
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28
140
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341
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128
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362
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441
131
134
20
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2
21
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cr
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81
Page 22 of 30
12
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86
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129
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275
Page 23 of 30
204
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Page 24 of 30
Drosophila Submitted
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Highlights
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Page 27 of 30
Dictyostelium slug
A B
PstA
prespore cells PstO
PstAB
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Migrating slug
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Nematode gonad Insect tracheal and renal tubes
C E F membrane GFP
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D
ed
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Vertebrate vasculature Mammalian kidney Mammalian lung

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Figure 1
Page 28 of 30
A. Lateral inhibition within a competence group
e.g. insect renal tubules TC precursor

Wg AC-S TC precursor Tip
daughters Cell
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Tip cell selection High Wingless Competent cell Selection of Tip Asymmetric division
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in MpT buds signals confer tip cluster express Cell precursor by of Tip Cell precursor
cell competence achaete lateral inhibition biased by Numb
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B. High levels of signal interact with intrinsic determinants
e.g. insect tracheal system
blistered
terminal cell
determination
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FGF
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N/Dl
fusion cell
escargot
determination
ed
N/Dl
C. Signalling and movement to the developing tips

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e.g. mammalian kidney

Metanephric mesenchyme
GDNF
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Ret
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sorting
Ureteric
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bud
D. Lineage dependent
e.g. nematode gonad

Gonad primordium
asymmetric precursor
Z1 Z2 Z3 Z4
Z1 Z2 Z3 Z4
divisions
somatic gonad somatic gonad
-catenin -catenin
precursor precursor /TCF
DTC /TCF DTC
germline precursors other somatic gonadal cells
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Figure 2
Page 29 of 30
A. Mitogenic signalling
e.g. insect renal tubules
Tip Cell Tip Cell

EGF-R induced
Sibling Cell tubule proliferation
Tip Cell
secreted
EGF Spitz Tubule cells
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B. Cell migration and branching morphogenesis
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e.g. mammalian vasculature e.g. mammalian kidney
GDNF
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Tip
Stalk Metanephric
VEGF Ret mesenchyme
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UB
Increased proliferation
guided tip
and migration at UB tips
migration
Wolffian Duct

C. Tube elongationan
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FGF tensile stress
triggers Stalk Cell
Intercalation (SCI)
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tip cell
migration tip cell
migration
mechanical SCI
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strain
D. Looping morphogenesis
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e.g. insect renal tubules tubule Balanced forces

extension tip cell
muscle
hypothesis
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Tip cell
tip cell-muscle
anchorage D/V
Dpp-guided anterior
tubule movement
E. Tube fusion

Fusion Cells
extracellular lumen
anastomosis
lumen
formation
intracellular
lumen
fusion cell elongation
Figure 3
Page 30 of 30

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Accepted Manuscript

Title: Tip cells: master regulators of tubulogenesis?

Author: Helen Weavers Helen Skaer

To appear in: Seminars in Cell & Developmental Biology

Received date: 4-3-2014

Helen Weavers+,$ and Helen Skaer+,*

Bristol BS8 1TD, UK

2.3 Tip cells promote branching morphogenesis

2.5 Tip cell anchorage and looping morphogenesis

2.6 Fusion at the tips: creating tubular networks

discontinuous tubular elements must be connected to generate a fully functional tubular

3. Tip cell roles in tubule physiology

Figure 1. Examples of tip cells

Figure 2. Strategies for tip cell selection

Vertebrate vasculature Mammalian kidney Mammalian lung

e.g. insect renal tubules TC precursor

C. Signalling and movement to the developing tips

e.g. mammalian kidney

e.g. nematode gonad

Tip Cell Tip Cell

e.g. insect tracheal system

e.g. insect renal tubules tubule Balanced forces

e.g. insect tracheal system

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