Epithelial morphogenesis: The mouse eye as a model system1

Current Topics in Developmental Biology

Volumn 111, Issue , 2015, Pages 375-399

  Chauhan, Bharesh ^a   Plageman, Timothy ^b   Lou, Ming ^c   Lang, Richard ^d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c LAMAR UNIVERSITY   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

Author keywords

Apical constriction; Cytoskeleton; Eye cup; Filopodia; GTPase; Lamellipodia; Lens placode; Morphogenesis

Indexed keywords

ACTIN FILAMENT; ANIMAL; BIOLOGICAL MODEL; CELL SHAPE; CYTOLOGY; EMBRYOLOGY; EYE; MORPHOGENESIS; MOUSE; PHYSIOLOGY; PIGMENT EPITHELIUM;

ACTIN CYTOSKELETON; ANIMALS; CELL SHAPE; EYE; MICE; MODELS, BIOLOGICAL; MORPHOGENESIS; RETINAL PIGMENT EPITHELIUM;

EID: 84922838709     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.ctdb.2014.11.011     Document Type: Chapter

References (128)

1. Altmann C.R., Chow R.L., Lang R.A., Hemmati-Brivanlou A. Lens induction by Pax-6 in Xenopus laevis. Developmental Biology 1997, 185(1):119-123. 10.1006/dbio.1997.8573.
2. Ashery-Padan R., Marquardt T., Zhou X., Gruss P. Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes & Development 2000, 14(21):2701-2711.
3. Azevedo D., Antunes M., Prag S., Ma X., Hacker U., Brodland G.W., et al. DRhoGEF2 regulates cellular tension and cell pulsations in the Amnioserosa during Drosophila dorsal closure. PLoS One 2011, 6(9):e23964. 10.1371/journal.pone.0023964.
4. Bailey A.P., Streit A. Sensory organs: Making and breaking the pre-placodal region. Current Topics in Developmental Biology 2006, 72:167-204. 10.1016/S0070-2153(05)72003-2.
5. Banzai Y., Miki H., Yamaguchi H., Takenawa T. Essential role of neural Wiskott-Aldrich syndrome protein in neurite extension in PC12 cells and rat hippocampal primary culture cells. Journal of Biological Chemistry 2000, 275(16):11987-11992.
6. Berg J.S., Cheney R.E. Myosin-X is an unconventional myosin that undergoes intrafilopodial motility. Nature Cell Biology 2002, 4(3):246-250. 10.1038/ncb762.
7. Bishop A.L., Hall A. Rho GTPases and their effector proteins. Biochemical Journal 2000, 348(Pt. 2):241-255.
8. Blanchard G.B., Murugesu S., Adams R.J., Martinez-Arias A., Gorfinkiel N. Cytoskeletal dynamics and supracellular organisation of cell shape fluctuations during dorsal closure. Development 2010, 137(16):2743-2752. 10.1242/dev.045872.
9. Borges R.M., Lamers M.L., Forti F.L., Santos M.F., Yan C.Y. Rho signaling pathway and apical constriction in the early lens placode. Genesis 2011, 49(5):368-379. 10.1002/dvg.20723.
10. Bresnick A.R. Molecular mechanisms of nonmuscle myosin-II regulation. Current Opinion in Cell Biology 1999, 11(1):26-33.
11. Burridge K., Wennerberg K. Rho and Rac take center stage. Cell 2004, 116(2):167-179.
12. Carpenter A.C., Smith A.N., Wagner H., Wallace V.A., Ashery-Padan R., Lang R.A. Wnt ligands from the embryonic surface ectoderm regulate "bimetallic strip" optic cup morphogenesis in the mouse 2014, Development, in press.
13. Charlton-Perkins M., Brown N.L., Cook T.A. The lens in focus: A comparison of lens development in Drosophila and vertebrates. Molecular Genetics & Genomics 2011, 286(3-4):189-213. 10.1007/s00438-011-0643-y.
14. Chauhan B.K., Disanza A., Choi S.Y., Faber S.C., Lou M., Beggs H.E. Cdc42- and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination. Development 2009, 136(21):3657-3667. 10.1242/dev.042242.
15. Chauhan B.K., Lou M., Zheng Y., Lang R.A. Balanced Rac1 and RhoA activities regulate cell shape and drive invagination morphogenesis in epithelia. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(45):18289-18294. 10.1073/pnas.1108993108.
16. Cho S.H., Cepko C.L. Wnt2b/beta-catenin-mediated canonical Wnt signaling determines the peripheral fates of the chick eye. Development 2006, 133(16):3167-3177.
17. Chow R.L., Altmann C.R., Lang R.A., Hemmati-Brivanlou A. Pax6 induces ectopic eyes in a vertebrate. Development 1999, 126(19):4213-4222.
18. Crosson C.E., Klyce S.D., Beuerman R.W. Epithelial wound closure in the rabbit cornea. A biphasic process. Investigative Ophthalmology & Visual Science 1986, 27(4):464-473.
19. D'Avino P.P., Savoian M.S., Glover D.M. Mutations in sticky lead to defective organization of the contractile ring during cytokinesis and are enhanced by Rho and suppressed by Rac. Journal of Cell Biology 2004, 166(1):61-71. 10.1083/jcb.200402157.
20. Darwin C. The origin of species 1859, John Murray, London.
21. David D.J., Tishkina A., Harris T.J. The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 2010, 137(10):1645-1655. 10.1242/dev.044107.
22. Dawes-Hoang R.E., Parmar K.M., Christiansen A.E., Phelps C.B., Brand A.H., Wieschaus E.F. folded gastrulation, cell shape change and the control of myosin localization. Development 2005, 132(18):4165-4178.
23. De Smet F., Segura I., De Bock K., Hohensinner P.J., Carmeliet P. Mechanisms of vessel branching: Filopodia on endothelial tip cells lead the way. Arteriosclerosis, Thrombosis, and Vascular Biology 2009, 29(5):639-649. 10.1161/ATVBAHA.109.185165.
24. Dimanlig P.V., Faber S.C., Auerbach W., Makarenkova H.P., Lang R.A. The upstream ectoderm enhancer in Pax6 has an important role in lens induction. Development 2001, 128(22):4415-4424.
25. Disanza A., Mantoani S., Hertzog M., Gerboth S., Frittoli E., Steffen A., et al. Regulation of cell shape by Cdc42 is mediated by the synergic actin-bundling activity of the Eps8-IRSp53 complex. Nature Cell Biology 2006, 8(12):1337-1347.
26. Dovas A., Couchman J.R. RhoGDI: Multiple functions in the regulation of Rho family GTPase activities. Biochemical Journal 2005, 390(Pt. 1):1-9. 10.1042/BJ20050104.
27. Egile C., Loisel T.P., Laurent V., Li R., Pantaloni D., Sansonetti P.J., et al. Activation of the CDC42 effector N-WASP by the Shigella flexneri IcsA protein promotes actin nucleation by Arp2/3 complex and bacterial actin-based motility. Journal of Cell Biology 1999, 146(6):1319-1332.
28. Eiraku M., Sasai Y. Mouse embryonic stem cell culture for generation of three-dimensional retinal and cortical tissues. Nature Protocols 2012, 7(1):69-79. 10.1038/nprot.2011.429.
29. Eiraku M., Takata N., Ishibashi H., Kawada M., Sakakura E., Okuda S. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 2011, 472(7341):51-56. 10.1038/nature09941.
30. Faber S.C., Dimanlig P., Makarenkova H.P., Shirke S., Ko K., Lang R.A. Fgf receptor signaling plays a role in lens induction. Development 2001, 128(22):4425-4438.
31. Faix J., Rottner K. The making of filopodia. Current Opinion in Cell Biology 2006, 18(1):18-25. 10.1016/j.ceb.2005.11.002.
32. Fazioli F., Minichiello L., Matoska V., Castagnino P., Miki T., Wong W.T., et al. Eps8, a substrate for the epidermal growth factor receptor kinase, enhances EGF-dependent mitogenic signals. The EMBO Journal 1993, 12(10):3799-3808.
33. Fuhrmann S. Wnt signaling in eye organogenesis. Organogenesis 2008, 4(2):60-67.
34. Fuhrmann S., Levine E.M., Reh T.A. Extraocular mesenchyme patterns the optic vesicle during early eye development in the embryonic chick. Development 2000, 127(21):4599-4609.
35. Fukumoto S., Miner J.H., Ida H., Fukumoto E., Yuasa K., Miyazaki H., et al. Laminin alpha5 is required for dental epithelium growth and polarity and the development of tooth bud and shape. Journal of Biological Chemistry 2006, 281(8):5008-5016. 10.1074/jbc.M509295200.
36. Furuta Y., Hogan B.L.M. BMP4 is essential for lens induction in the mouse embryo. Genes & Development 1998, 12(23):3764-3775.
37. Gallagher B.C. Branching morphogenesis in the avian lung: Electron microscopic studies using cationic dyes. Journal of Embryology and Experimental Morphology 1986, 94:189-205.
38. Gallo G., Letourneau P.C. Regulation of growth cone actin filaments by guidance cues. Journal of Neurobiology 2004, 58(1):92-102. 10.1002/neu.10282.
39. Gamell C., Osses N., Bartrons R., Ruckle T., Camps M., Rosa J.L., et al. BMP2 induction of actin cytoskeleton reorganization and cell migration requires PI3-kinase and Cdc42 activity. Journal of Cell Science 2008, 121(Pt. 23):3960-3970. 10.1242/jcs.031286.
40. Garcia C.M., Huang J., Madakashira B.P., Liu Y., Rajagopal R., Dattilo L., et al. The function of FGF signaling in the lens placode. Developmental Biology 2011, 351(1):176-185. 10.1016/j.ydbio.2011.01.001.
41. Gotoh N., Ito M., Yamamoto S., Yoshino I., Song N., Wang Y. Tyrosine phosphorylation sites on FRS2alpha responsible for Shp2 recruitment are critical for induction of lens and retina. Proceedings of the National Academy of Sciences of the United States of America 2004, 101(49):17144-17149. 10.1073/pnas.0407577101.
42. Grashoff C., Hoffman B.D., Brenner M.D., Zhou R., Parsons M., Yang M.T., et al. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 2010, 466(7303):263-266. 10.1038/nature09198.
43. Grocott T., Tambalo M., Streit A. The peripheral sensory nervous system in the vertebrate head: A gene regulatory perspective. Developmental Biology 2012, 370(1):3-23. 10.1016/j.ydbio.2012.06.028.
44. Gunhaga L. The lens: A classical model of embryonic induction providing new insights into cell determination in early development. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2011, 366(1568):1193-1203. 10.1098/rstb.2010.0175.
45. Haigo S.L., Hildebrand J.D., Harland R.M., Wallingford J.B. Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Current Biology 2003, 13(24):2125-2137.
46. Hardin J. The role of secondary mesenchyme cells during sea urchin gastrulation studied by laser ablation. Development 1988, 103(2):317-324.
47. Heasman S.J., Ridley A.J. Mammalian Rho GTPases: New insights into their functions from in vivo studies. Nature Reviews. Molecular Cell Biology 2008, 9(9):690-701. 10.1038/nrm2476.
48. Hendrix R.W., Zwaan J. Cell shape regulation and cell cycle in embryonic lens cells. Nature 1974, 247(437):145-147.
49. Hildebrand J.D. Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network. Journal of Cell Science 2005, 118(Pt. 22):5191-5203.
50. Hildebrand J.D., Soriano P. Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell 1999, 99(5):485-497.
51. Hill R.E., Favor J., Hogan B.L., Ton C.C., Saunders G.F., Hanson I.M., et al. Mouse small eye results from mutations in a paired-like homeobox-containing gene. Nature 1991, 354(6354):522-525.
52. Huang J., Rajagopal R., Liu Y., Dattilo L.K., Shaham O., Ashery-Padan R., et al. The mechanism of lens placode formation: A case of matrix-mediated morphogenesis. Developmental Biology 2011, 355(1):32-42. 10.1016/j.ydbio.2011.04.008.
53. Izzard C.S. Contractile filopodia and in vivo cell movement in the tunic of the ascidian, Botryllus schlosseri. Journal of Cell Science 1974, 15(3):513-535.
54. Jacinto A., Wood W., Woolner S., Hiley C., Turner L., Wilson C., et al. Dynamic analysis of actin cable function during Drosophila dorsal closure. Current Biology 2002, 12(14):1245-1250.
55. Jaffe A.B., Hall A. Rho GTPases: Biochemistry and biology. Annual Review of Cell and Developmental Biology 2005, 21:247-269.
56. Konstantinidis G., Moustakas A., Stournaras C. Regulation of myosin light chain function by BMP signaling controls actin cytoskeleton remodeling. Cellular Physiology and Biochemistry 2011, 28(5):1031-1044. 10.1159/000335790.
57. Kraynov V.S., Chamberlain C., Bokoch G.M., Schwartz M.A., Slabaugh S., Hahn K.M. Localized Rac activation dynamics visualized in living cells. Science 2000, 290(5490):333-337.
58. Krugmann S., Jordens I., Gevaert K., Driessens M., Vandekerckhove J., Hall A. Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Current Biology 2001, 11(21):1645-1655.
59. Kurisu S., Takenawa T. The WASP and WAVE family proteins. Genome Biology 2009, 10(6):226. 10.1186/gb-2009-10-6-226.
60. Lang R.A. Pathways regulating lens induction in the mouse. International Journal of Developmental Biology 2004, 48(8-9):783-791.
61. Lang R.A., Herman K., Reynolds A.B., Hildebrand J.D., Plageman T.F. p120-Catenin-dependent junctional recruitment of Shroom3 is required for apical constriction during lens pit morphogenesis. Development 2014, 141(16):3177-3187. 10.1242/dev.107433.
62. Lee C., Le M.P., Wallingford J.B. The shroom family proteins play broad roles in the morphogenesis of thickened epithelial sheets. Developmental Dynamics 2009, 238(6):1480-1491. 10.1002/dvdy.21942.
63. Lee-Hoeflich S.T., Causing C.G., Podkowa M., Zhao X., Wrana J.L., Attisano L. Activation of LIMK1 by binding to the BMP receptor, BMPRII, regulates BMP-dependent dendritogenesis. EMBO Journal 2004, 23(24):4792-4801. 10.1038/sj.emboj.7600418.
64. Leptin M. Gastrulation movements: The logic and the nuts and bolts. Developmental Cell 2005, 8(3):305-320. 10.1016/j.devcel.2005.02.007.
65. Linseman D.A., Loucks F.A. Diverse roles of Rho family GTPases in neuronal development, survival, and death. Frontiers in Bioscience 2008, 13:657-676.
66. Liu H., Mohamed O., Dufort D., Wallace V.A. Characterization of Wnt signaling components and activation of the Wnt canonical pathway in the murine retina. Developmental Dynamics 2003, 227(3):323-334. 10.1002/dvdy.10315.
67. Liu H., Thurig S., Mohamed O., Dufort D., Wallace V.A. Mapping canonical Wnt signaling in the developing and adult retina. Investigative Ophthalmology & Visual Science 2006, 47(11):5088-5097. 10.1167/iovs.06-0403.
68. Liu H., Xu S., Wang Y., Mazerolle C., Thurig S., Coles B.L. Ciliary margin transdifferentiation from neural retina is controlled by canonical Wnt signaling. Developmental Biology 2007, 308(1):54-67. 10.1016/j.ydbio.2007.04.052.
69. Machacek M., Hodgson L., Welch C., Elliott H., Pertz O., Nalbant P., et al. Coordination of Rho GTPase activities during cell protrusion. Nature 2009, 461(7260):99-103. 10.1038/nature08242.
70. Mallarino R., Grant P.R., Grant B.R., Herrel A., Kuo W.P., Abzhanov A. Two developmental modules establish 3D beak-shape variation in Darwin's finches. Proceedings of the National Academy of Sciences of the United States of America 2011, 108(10):4057-4062. 10.1073/pnas.1011480108.
71. Mann I. The development of the human eye 1950, Grune and Stratton, New York.
72. Martin A.C., Kaschube M., Wieschaus E.F. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 2009, 457(7228):495-499. 10.1038/nature07522.
73. Martin-Blanco E., Pastor-Pareja J.C., Garcia-Bellido A. JNK and decapentaplegic signaling control adhesiveness and cytoskeleton dynamics during thorax closure in Drosophila. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(14):7888-7893.
74. McAvoy J.W. Cytoplasmic processes interconnect lens placode and optic vesicle during eye morphogenesis. Experimental Eye Research 1980, 31(5):527-534.
75. McClay D.R. The role of thin filopodia in motility and morphogenesis. Experimental Cell Research 1999, 253(2):296-301. 10.1006/excr.1999.4723.
76. Mckeehan M.S. Cytological aspects of embryonic lens induction in the chick. Journal of Experimental Zoology 1951, 117:31-64.
77. Miki H., Sasaki T., Takai Y., Takenawa T. Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 1998, 391(6662):93-96.
78. Miki H., Suetsugu S., Takenawa T. WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. The EMBO Journal 1998, 17(23):6932-6941.
79. Millard T.H., Martin P. Dynamic analysis of filopodial interactions during the zippering phase of Drosophila dorsal closure. Development 2008, 135(4):621-626. 10.1242/dev.014001.
80. Moores S.L., Sabry J.H., Spudich J.A. Myosin dynamics in live Dictyostelium cells. Proceedings of the National Academy of Sciences of the United States of America 1996, 93(1):443-446.
81. Nakano T., Ando S., Takata N., Kawada M., Muguruma K., Sekiguchi K., et al. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 2012, 10(6):771-785. 10.1016/j.stem.2012.05.009.
82. Nimnual A.S., Taylor L.J., Bar-Sagi D. Redox-dependent downregulation of Rho by Rac. Nature Cell Biology 2003, 5(3):236-241. 10.1038/ncb938.
83. Nishimura T., Takeichi M. Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 2008, 135(8):1493-1502.
84. Nobes C., Hall A. Regulation and function of the Rho subfamily of small GTPases. Current Opinion in Genetics & Development 1994, 4(1):77-81.
85. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81(1):53-62.
86. Nobes C.D., Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. Journal of Cell Biology 1999, 144(6):1235-1244.
87. Ohta Y., Hartwig J.H., Stossel T.P. FilGAP, a Rho- and ROCK-regulated GAP for Rac binds filamin A to control actin remodelling. Nature Cell Biology 2006, 8(8):803-814. ncb1437 [pii]. 10.1038/ncb1437.
88. Pang S.C., Daniels W.H., Buck R.C. Epidermal migration during the healing of suction blisters in rat skin: A scanning and transmission electron microscopic study. The American Journal of Anatomy 1978, 153(2):177-191. 10.1002/aja.1001530202.
89. Partridge M.A., Marcantonio E.E. Initiation of attachment and generation of mature focal adhesions by integrin-containing filopodia in cell spreading. Molecular Biology of the Cell 2006, 17(10):4237-4248. 10.1091/mbc.E06-06-0496.
90. Passey S., Pellegrin S., Mellor H. What is in a filopodium? Starfish versus hedgehogs. Biochemical Society Transactions 2004, 32(Pt. 6):1115-1117. 10.1042/BST0321115.
91. Peng J., Wallar B.J., Flanders A., Swiatek P.J., Alberts A.S. Disruption of the diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Current Biology 2003, 13(7):534-545.
92. Pfister R.R. The healing of corneal epithelial abrasions in the rabbit: A scanning electron microscope study. Investigative Ophthalmology 1975, 14(9):648-661.
93. Plageman T.F., Chauhan B.K., Yang C., Jaudon F., Shang X., Zheng Y., et al. A Trio-RhoA-Shroom3 pathway is required for apical constriction and epithelial invagination. Development 2011, 138(23):5177-5188. 10.1242/dev.067868.
94. Plageman T.F., Chung M.I., Lou M., Smith A.N., Hildebrand J.D., Wallingford J.B., et al. Pax6-dependent Shroom3 expression regulates apical constriction during lens placode invagination. Development 2010, 137(3):405-415. 10.1242/dev.045369.
95. Raftopoulou M., Hall A. Cell migration: Rho GTPases lead the way. Developmental Biology 2004, 265(1):23-32. S001216060300544X [pii].
96. Raich W.B., Agbunag C., Hardin J. Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming. Current Biology 1999, 9(20):1139-1146. 10.1016/S0960-9822(00)80015-9.
97. Rajagopal R., Huang J., Dattilo L.K., Kaartinen V., Mishina Y., Deng C.X., et al. The type I BMP receptors, Bmpr1a and Acvr1, activate multiple signaling pathways to regulate lens formation. Developmental Biology 2009, 335(2):305-316. 10.1016/j.ydbio.2009.08.027.
98. Ridley A.J. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends in Cell Biology 2006, 16(10):522-529.
99. Roffers-Agarwal J., Xanthos J.B., Kragtorp K.A., Miller J.R. Enabled (Xena) regulates neural plate morphogenesis, apical constriction, and cellular adhesion required for neural tube closure in Xenopus. Developmental Biology 2008, 314(2):393-403.
100. Roh-Johnson M., Shemer G., Higgins C.D., McClellan J.H., Werts A.D., Tulu U.S., et al. Triggering a cell shape change by exploiting preexisting actomyosin contractions. Science 2012, 335(6073):1232-1235. 10.1126/science.1217869.
101. Rossman K.L., Der C.J., Sondek J. GEF means go: Turning on RHO GTPases with guanine nucleotide-exchange factors. Nature Reviews. Molecular Cell Biology 2005, 6(2):167-180. 10.1038/nrm1587.
102. Samakovlis C., Hacohen N., Manning G., Sutherland D.C., Guillemin K., Krasnow M.A. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 1996, 122(5):1395-1407.
103. Sawyer J.K., Harris N.J., Slep K.C., Gaul U., Peifer M. The Drosophila afadin homologue Canoe regulates linkage of the actin cytoskeleton to adherens junctions during apical constriction. Journal of Cell Biology 2009, 186(1):57-73. 10.1083/jcb.200904001.
104. Sawyer J.M., Harrell J.R., Shemer G., Sullivan-Brown J., Roh-Johnson M., Goldstein B. Apical constriction: A cell shape change that can drive morphogenesis. Developmental Biology 2010, 341(1):5-19. 10.1016/j.ydbio.2009.09.009.
105. Schmidt S., Diriong S., Mery J., Fabbrizio E., Debant A. Identification of the first Rho-GEF inhibitor, TRIPalpha, which targets the RhoA-specific GEF domain of Trio. FEBS Letters 2002, 523(1-3):35-42.
106. Shaham O., Menuchin Y., Farhy C., Ashery-Padan R. Pax6: A multi-level regulator of ocular development. Progress in Retinal and Eye Research 2012, 31(5):351-376. 10.1016/j.preteyeres.2012.04.002.
107. Smith A.N., Miller L.A., Radice G., Ashery-Padan R., Lang R.A. Stage-dependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis. Development 2009, 136(17):2977-2985. 10.1242/dev.037341.
108. Snapper S.B., Takeshima F., Anton I., Liu C.H., Thomas S.M., Nguyen D., et al. N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nature Cell Biology 2001, 3(10):897-904.
109. Sousa A.D., Cheney R.E. Myosin-X: A molecular motor at the cell's fingertips. Trends in Cell Biology 2005, 15(10):533-539. 10.1016/j.tcb.2005.08.006.
110. Steding G. Reasons for embryonic epithelial thickening. Acta Anatomica (Basel) 1967, 68(1):37-67.
111. Streit A. The cranial sensory nervous system: Specification of sensory progenitors and placodes 2008, StemBook, Cambridge, MA.
112. Takahashi K., Suzuki K. Membrane transport of WAVE2 and lamellipodia formation require Pak1 that mediates phosphorylation and recruitment of stathmin/Op18 to Pak1-WAVE2-kinesin complex. Cellular Signalling 2009, 21(5):695-703. 10.1016/j.cellsig.2009.01.007.
113. Tcherkezian J., Lamarche-Vane N. Current knowledge of the large RhoGAP family of proteins. Biology of the Cell 2007, 99(2):67-86. 10.1042/BC20060086.
114. Tilney L.G., Gibbins J.R. Microtubules and filaments in the filopodia of the secondary mesenchyme cells of Arbacia punctulata and Echinarachnius parma. Journal of Cell Science 1969, 5(1):195-210.
115. Tokuo H., Ikebe M. Myosin X transports Mena/VASP to the tip of filopodia. Biochemical and Biophysical Research Communications 2004, 319(1):214-220. 10.1016/j.bbrc.2004.04.167.
116. Trimarchi J.M., Cho S.H., Cepko C.L. Identification of genes expressed preferentially in the developing peripheral margin of the optic cup. Developmental Dynamics 2009, 238(9):2327-2329. 10.1002/dvdy.21973.
117. Vasioukhin V., Fuchs E. Actin dynamics and cell-cell adhesion in epithelia. Current Opinion in Cell Biology 2001, 13(1):76-84.
118. Villalonga P., Ridley A.J. Rho GTPases and cell cycle control. Growth Factors 2006, 24(3):159-164.
119. Wagner M.C., Barylko B., Albanesi J.P. Tissue distribution and subcellular localization of mammalian myosin I. Journal of Cell Biology 1992, 119(1):163-170.
120. Wakely J. Observations on the role of ectodermal spreading in the early stages of lens placode invagination in the chick embryo. Experimental Eye Research 1984, 38(6):627-636.
121. Wawersik S., Purcell P., Rauchman M., Dudley A.T., Robertson E.J., Maas R. BMP7 acts in murine lens placode development. Developmental Biology 1999, 207(1):176-188.
122. Westenskow P., Piccolo S., Fuhrmann S. Beta-catenin controls differentiation of the retinal pigment epithelium in the mouse optic cup by regulating Mitf and Otx2 expression. Development 2009, 136(15):2505-2510. 10.1242/dev.032136.
123. Williams-Masson E.M., Malik A.N., Hardin J. An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 1997, 124(15):2889-2901.
124. Wolf C., Gerlach N., Schuh R. Drosophila tracheal system formation involves FGF-dependent cell extensions contacting bridge-cells. EMBO Reports 2002, 3(6):563-568. 10.1093/embo-reports/kvf115.
125. Wood W., Jacinto A., Grose R., Woolner S., Gale J., Wilson C., et al. Wound healing recapitulates morphogenesis in Drosophila embryos. Nature Cell Biology 2002, 4(11):907-912.
126. Xu J., Wang F., Van Keymeulen A., Herzmark P., Straight A., Kelly K., et al. Divergent signals and cytoskeletal assemblies regulate self-organizing polarity in neutrophils. Cell 2003, 114(2):201-214.
127. Yeh T.C., Ogawa W., Danielsen A.G., Roth R.A. Characterization and cloning of a 58/53-kDa substrate of the insulin receptor tyrosine kinase. Journal of Biological Chemistry 1996, 271(6):2921-2928.
128. Zhang H., Berg J.S., Li Z., Wang Y., Lang P., Sousa A.D., et al. Myosin-X provides a motor-based link between integrins and the cytoskeleton. Nature Cell Biology 2004, 6(6):523-531. 10.1038/ncb1136.