Cdc42- and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination

Development

Volumn 136, Issue 21, 2009, Pages 3657-3667

  Chauhan, Bharesh K ^a   Disanza, Andrea ^b   Choi, Sue Yeon ^c   Faber, Sonya C ^d   Lou, Ming ^e   Beggs, Hilary E ^c   Scita, Giorgio ^b   Zheng, Yi ^a   Lang, Richard A ^a,f  

^a CINCINNATI CHILDREN S HOSPITAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^e LAMAR UNIVERSITY   (United States)

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

Author keywords

Cdc42; Eye development; Filopodia; IRSp53 (Baiap2); Lens development; Morphogenesis; Mouse

Indexed keywords

F ACTIN; FOCAL ADHESION KINASE; GENE PRODUCT; PROTEIN CDC42; PROTEIN IRSP53; UNCLASSIFIED DRUG;

ACTIN MYOSIN INTERACTION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; EMBRYO; EMBRYO PATTERN FORMATION; EYE DEVELOPMENT; FILOPODIUM; GENE FUNCTION; LENS DEVELOPMENT; LENS EPITHELIUM; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; RETINA DEVELOPMENT;

ACTINS; ANIMALS; FOCAL ADHESION KINASE 1; LENS, CRYSTALLINE; MICE; MYOSINS; PSEUDOPODIA; RETINA; SPECIFIC PATHOGEN-FREE ORGANISMS;

ECHINOIDEA; VERTEBRATA;

EID: 70350179623     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.042242     Document Type: Article

References (89)

1. Ashery-Padan, R., Marquardt, T., Zhou, X. and Gruss, P. (2000). Pax6 activity in the lens primordium is required for lens formation and for correct placement of a single retina in the eye. Genes Dev. 14, 2701-2711.
2. Banzai, Y., Miki, H., Yamaguchi, H. and Takenawa, T. (2000). Essential role of neural Wiskott-Aldrich syndrome protein in neurite extension in PC12 cells and rat hippocampal primary culture cells. J. Biol. Chem. 275, 11987-11992.
3. Beggs, H. E., Schahin-Reed, D., Zang, K., Goebbels, S., Nave, K. A., Gorski, J., Jones, K. R., Sretavan, D. and Reichardt, L. F. (2003). FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40, 501-514.
4. Boussadia, O., Kutsch, S., Hierholzer, A., Delmas, V. and Kemler, R. (2002). E-cadherin is a survival factor for the lactating mouse mammary gland. Mech. Dev. 115, 53-62.
5. Brahmbhatt, A. A. and Klemke, R. L. (2003). ERK and RhoA differentially regulate pseudopodia growth and retraction during chemotaxis. J. Biol. Chem. 278, 13016-13025.
6. Burridge, K. and Wennerberg, K. (2004). Rho and Rac take center stage. Cell 116, 167-179.
7. Chen, L., Liao, G., Yang, L., Campbell, K., Nakafuku, M., Kuan, C. Y. and Zheng, Y. (2006). Cdc42 deficiency causes Sonic hedgehog-independent holoprosencephaly. Proc. Natl. Acad. Sci. USA 103, 16520-16525.
8. Chow, R. L. and Lang, R. A. (2001). Early eye development in vertebrates. Annu. Rev. Cell Dev. Biol. 17, 255-296.
9. Davidson, L. A., Koehl, M. A., Keller, R. and Oster, G. F. (1995). How do sea urchins invaginate? Using biomechanics to distinguish between mechanisms of primary invagination. Development 121, 2005-2018.
10. Disanza, A., Mantoani, S., Hertzog, M., Gerboth, S., Frittoli, E., Steffen, A., Berhoerster, K., Kreienkamp, H. J., Milanesi, F., Di Fiore, P. P. et al. (2006). Regulation of cell shape by Cdc42 is mediated by the synergic actin-bundling activity of the Eps8-IRSp53 complex. Nat. Cell Biol. 8, 1337-1347.
11. Egile, C., Loisel, T. P., Laurent, V., Li, R., Pantaloni, D., Sansonetti, P. J. and Carlier, M. F. (1999). 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. J. Cell Biol. 146, 1319-1332.
12. Etienne-Manneville, S. (2004). Cdc42-the centre of polarity. J. Cell Sci. 117, 1291-1300.
13. Faber, S. C., Dimanlig, P., Makarenkova, H. P., Shirke, S., Ko, K. and Lang, R. A. (2001). Fgf receptor signaling plays a role in lens induction. Development 128, 4425-4438.
14. Faix, J. and Rottner, K. (2006). The making of filopodia. Curr. Opin. Cell Biol. 18, 18-25.
15. Fazioli, F., Minichiello, L., Matoska, V., Castagnino, P., Miki, T., Wong, W. T. and Di Fiore, P. P. (1993). Eps8, a substrate for the epidermal growth factor receptor kinase, enhances EGF-dependent mitogenic signals. EMBO J. 12, 3799-3808.
16. Furuta, Y. and Hogan, B. L. M. (1998). BMP4 is essential for lens induction in the mouse embryo. Genes Dev. 12, 3764-3775.
17. Gotoh, N., Ito, M., Yamamoto, S., Yoshino, I., Song, N., Wang, Y., Lax, I., Schlessinger, J., Shibuya, M. and Lang, R. A. (2004). Tyrosine phosphorylation sites on FRS2alpha responsible for Shp2 recruitment are critical for induction of lens and retina. Proc. Natl. Acad. Sci. USA 101, 17144-17149.
18. Grindley, J. C., Davidson, D. R. and Hill, R. E. (1995). The role of Pax-6 in eye and nasal development. Development 121, 1433-1442.
19. Gu, Y., Filippi, M. D., Cancelas, J. A., Siefring, J. E., Williams, E. P., Jasti, A. C., Harris, C. E., Lee, A. W., Prabhakar, R., Atkinson, S. J. et al. (2003). Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 302, 445-449.
20. Gumbiner, B. M. (2005). Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 6, 622-634.
21. Haigo, S. L., Hildebrand, J. D., Harland, R. M. and Wallingford, J. B. (2003). Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr. Biol. 13, 2125-2137.
22. Hardin, J. (1988). The role of secondary mesenchyme cells during sea urchin gastrulation studied by laser ablation. Development 103, 317-324.
23. Hardin, J. and Keller, R. (1988). The behaviour and function of bottle cells during gastrulation of Xenopus laevis. Development 103, 211-230.
24. Hardin, J. and McClay, D. R. (1990). Target recognition by the archenteron during sea urchin gastrulation. Dev. Biol. 142, 86-102.
25. Hendrix, R. W. and Zwaan, J. (1974). Cell shape regulation and cell cycle in embryonic lens cells. Nature 247, 145-147.
26. Higgs, H. N. and Pollard, T. D. (1999). Regulation of actin polymerization by Arp2/3 complex and WASp/Scar proteins. J. Biol. Chem. 274, 32531-32534.
27. Ishihara, H., Martin, B. L., Brautigan, D. L., Karaki, H., Ozaki, H., Kato, Y., Fusetani, N., Watabe, S., Hashimoto, K., Uemura, D. et al. (1989). Calyculin A and okadaic acid: inhibitors of protein phosphatase activity. Biochem. Biophys. Res. Commun. 159, 871-877.
28. Iwabu, A., Smith, K., Allen, F. D., Lauffenburger, D. A. and Wells, A. (2004). Epidermal growth factor induces fibroblast contractility and motility via a protein kinase C delta-dependent pathway. J. Biol. Chem. 279, 14551-14560.
29. Iwadate, Y. and Yumura, S. (2008). Molecular dynamics and forces of a motile cell simultaneously visualized by TIRF and force microscopies. Biotechniques 44, 739-750.
30. Jaffe, A. B. and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269.
31. Jaffer, Z. M. and Chernoff, J. (2004). The cross-Rho'ds of cell-cell adhesion. J. Biol. Chem. 279, 35123-35126.
32. Jones, C. and Chen, P. (2008). Primary cilia in planar cell polarity regulation of the inner ear. Curr. Top. Dev. Biol. 85, 197-224.
33. Kaibuchi, K. (1999). Regulation of cytoskeleton and cell adhesion by Rho targets. Prog. Mol. Subcell. Biol. 22, 23-38.
34. Kasper, M. and Viebahn, C. (1992). Cytokeratin expression and early lens development. Anat. Embryol. (Berl.) 186, 285-290.
35. Kimberly, E. L. and Hardin, J. (1998). Bottle cells are required for the initiation of primary invagination in the sea urchin embryo. Dev. Biol. 204, 235-250.
36. Krugmann, S., Jordens, I., Gevaert, K., Driessens, M., Vandekerckhove, J. and Hall, A. (2001). Cdc42 induces filopodia by promoting the formation of an IRSp53:Mena complex. Curr. Biol. 11, 1645-1655.
37. Lecuit, T. and Lenne, P. F. (2007). Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 8, 633-644.
38. Lenhossek. (1902). Die Entwicklung des Glaskorpers Vortr. Kgl. Akad. Wissensch. Budapest.
39. Leptin, M. and Grunewald, B. (1990). Cell shape changes during gastrulation in Drosophila. Development 110, 73-84.
40. Limouze, J., Straight, A. F., Mitchison, T. and Sellers, J. R. (2004). Specificity of blebbistatin, an inhibitor of myosin II. J. Muscle Res. Cell Motil. 25, 337-341.
41. Macara, I. G. (2004). Parsing the polarity code. Nat. Rev. Mol. Cell Biol. 5, 220-231.
42. Machesky, L. M. and Insall, R. H. (1998). Scar1 and the related Wiskott-Aldrich syndrome protein, WASP, regulate the actin cytoskeleton through the Arp2/3 complex. Curr. Biol. 8, 1347-1356.
43. Maddala, R., Deng, P. F., Costello, J. M., Wawrousek, E. F., Zigler, J. S. and Rao, V. P. (2004). Impaired cytoskeletal organization and membrane integrity in lens fibers of a Rho GTPase functional knockout transgenic mouse. Lab. Invest. 84, 679-692.
44. Magitot, A. (1910). Etude sur le developpement de la retine humaine. Ann. Ocul. 143, 241-282.
45. Malinda, K. M., Fisher, G. W. and Ettensohn, C. A. (1995). Four-dimensional microscopic analysis of the filopodial behavior of primary mesenchyme cells during gastrulation in the sea urchin embryo. Dev. Biol. 172, 552-566.
46. Mann, I. (1928). The Development of the Human Eye. New York: Grune and Stratton.
47. Mann, I. (1950). The Development of the Human Eye. New York: Grune and Stratton.
48. Martin-Blanco, E., Pastor-Pareja, J. C. and Garcia-Bellido, A. (2000). JNK and decapentaplegic signaling control adhesiveness and cytoskeleton dynamics during thorax closure in Drosophila. Proc. Natl. Acad. Sci. USA 97, 7888-7893.
49. Martinez-Morales, J. R., Rembold, M., Greger, K., Simpson, J. C., Brown, K. E., Quiring, R., Pepperkok, R., Martin-Bermudo, M. D., Himmelbauer, H. and Wittbrodt, J. (2009). ojoplano-mediated basal constriction is essential for optic cup morphogenesis. Development 136, 2165-2175.
50. McAvoy, J. W. (1980). Cytoplasmic processes interconnect lens placode and optic vesicle during eye morphogenesis. Exp. Eye Res. 31, 527-534.
51. McClay, D. R. (1999). The role of thin filopodia in motility and morphogenesis. Exp. Cell Res. 253, 296-301.
52. McEwen, D. P., Jenkins, P. M. and Martens, J. R. (2008). Olfactory cilia: our direct neuronal connection to the external world. Curr. Top. Dev. Biol. 85, 333-370.
53. Medina-Martinez, O. and Jamrich, M. (2007). Foxe view of lens development and disease. Development 134, 1455-1463.
54. Miki, H. and Takenawa, T. (2003). Regulation of actin dynamics by WASP family proteins. J. Biochem. (Tokyo) 134, 309-313.
55. Miki, H., Sasaki, T., Takai, Y. and Takenawa, T. (1998). Induction of filopodium formation by a WASP-related actin-depolymerizing protein N-WASP. Nature 391, 93-96.
56. Miller, J., Fraser, S. E. and McClay, D. (1995). Dynamics of thin filopodia during sea urchin gastrulation. Development 121, 2501-2511.
57. Nemethova, M., Auinger, S. and Small, J. V. (2008). Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J. Cell Biol. 180, 1233-1244.
58. Nobes, C. D. and Hall, A. (1995). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
59. Odell, G. M., Oster, G., Alberch, P. and Burnside, B. (1981). The mechanical basis of morphogenesis. I. Epithelial folding and invagination. Dev. Biol. 85, 446-462.
60. Ogino, H., Fisher, M. and Grainger, R. M. (2008). Convergence of a head-field selector Otx2 and Notch signaling: a mechanism for lens specification. Development 135, 249-258.
61. Parmigiani, C. and McAvoy, J. W. (1984). Localisation of laminin and fibronectin during rat lens morphogenesis. Differentiation 28, 53-61.
62. Partridge, M. A. and Marcantonio, E. E. (2006). Initiation of attachment and generation of mature focal adhesions by integrin-containing filopodia in cell spreading. Mol. Biol. Cell 17, 4237-4248.
63. Passey, S., Pellegrin, S. and Mellor, H. (2004). What is in a filopodium? Starfish versus hedgehogs. Biochem. Soc. Trans. 32, 1115-1117.
64. Peng, J., Wallar, B. J., Flanders, A., Swiatek, P. J. and Alberts, A. S. (2003). Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr. Biol. 13, 534-545.
65. Raich, W. B., Agbunag, C. and Hardin, J. (1999). Rapid epithelial-sheet sealing in the Caenorhabditis elegans embryo requires cadherin-dependent filopodial priming. Curr. Biol. 9, 1139-1146.
66. Ridley, A. J. (2006). Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16, 522-529.
67. Ridley, A. J. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
68. Ridley, A. J., Paterson, H. F., Johnston, C. L., Diekmann, D. and Hall, A. (1992). The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410.
69. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T. and Kirschner, M. W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231.
70. Rosenbaum, J. L., Cole, D. G. and Diener, D. R. (1999). Intraflagellar transport: the eyes have it. J. Cell Biol. 144, 385-388.
71. Sawallisch, C., Berhorster, K., Disanza, A., Mantoani, S., Kintscher, M., Stoenica, L., Dityatev, A., Sieber, S., Kindler, S., Morellini, F. et al. (2009). The insulin receptor substrate of 53 kDa (IRSp53) limits hippocampal synaptic plasticity. J. Biol. Chem. 284, 9225-9236.
72. Schroeder, T. E. (1970). Neurulation in Xenopus laevis: an analysis and model based upon light and electron microscopy. J. Embryol. Exp. Morphol. 23, 427-462.
73. Seifert, J. R. and Mlodzik, M. (2007). Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat. Rev. Genet. 8, 126-138.
74. Senju, Y. and Miyata, H. (2009). The role of actomyosin contractility in the formation and dynamics of actin bundles during fibroblast spreading. J. Biochem. 145, 137-150.
75. Silverman, M. A. and Leroux, M. R. (2009). Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends Cell Biol. 19, 306-316.
76. Smith, A. N., Miller, L. A., Song, N., Taketo, M. M. and Lang, R. A. (2005). The duality of beta-catenin function: a requirement in lens morphogenesis and signaling suppression of lens fate in periocular ectoderm. Dev. Biol. 285, 477-489.
77. Smith, A. N., Miller, L. A., Radice, G., Ashery-Padan, R. and Lang, R. A. (2009). Stage-dependent modes of Pax6-Sox2 epistasis regulate lens development and eye morphogenesis. Development 136, 2977-2985..
78. Snapper, S. B., Takeshima, F., Anton, I., Liu, C. H., Thomas, S. M., Nguyen, D., Dudley, D., Fraser, H., Purich, D., Lopez-Ilasaca, M. et al. (2001). N-WASP deficiency reveals distinct pathways for cell surface projections and microbial actin-based motility. Nat. Cell Biol. 3, 897-904.
79. Stevenson, B. R., Siliciano, J. D., Mooseker, M. S. and Goodenough, D. A. (1986). Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol. 103, 755-766.
80. Takashima, S. (2009). Phosphorylation of myosin regulatory light chain by myosin light chain kinase, and muscle contraction. Circ. J. 73, 208-213.
81. Wallingford, J. B. (2005). Neural tube closure and neural tube defects: studies in animal models reveal known knowns and known unknowns. Am. J. Med. Genet. C Semin. Med. Genet. 135C, 59-68.
82. Wawersik, S., Purcell, P., Rauchman, M., Dudley, A. T., Robertson, E. J. and Maas, R. (1999). BMP7 Acts in Murine Lens Placode Development. Dev. Biol. 207, 176-188.
83. Weiss, S. M., Ladwein, M., Schmidt, D., Ehinger, J., Lommel, S., Stading, K., Beutling, U., Disanza, A., Frank, R., Jansch, L. et al. (2009). IRSp53 links the enterohemorrhagic E. coli effectors Tir and EspFU for actin pedestal formation. Cell Host Microbe 5, 244-258.
84. Williams, S. C., Altmann, C. R., Chow, R. L., Hemmati-Brivanlou, A. and Lang, R. A. (1998). A highly conserved lens transcriptional control element from the Pax-6 gene. Mech. Dev. 73, 225-229.
85. Williams-Masson, E. M., Malik, A. N. and Hardin, J. (1997). An actin-mediated two-step mechanism is required for ventral enclosure of the C. elegans hypodermis. Development 124, 2889-2901.
86. Wood, W., Jacinto, A., Grose, R., Woolner, S., Gale, J., Wilson, C. and Martin, P. (2002). Wound healing recapitulates morphogenesis in Drosophila embryos. Nat. Cell Biol. 4, 907-912.
87. Yang, C., Hoelzle, M., Disanza, A., Scita, G. and Svitkina, T. (2009). Coordination of membrane and actin cytoskeleton dynamics during filopodia protrusion. PLoS ONE 4, e5678.
88. Yang, L., Wang, L. and Zheng, Y. (2006). Gene targeting of Cdc42 and Cdc42GAP affirms the critical involvement of Cdc42 in filopodia induction, directed migration, and proliferation in primary mouse embryonic fibroblasts. Mol. Biol. Cell 17, 4675-4685.
89. Yeh, T. C., Ogawa, W., Danielsen, A. G. and Roth, R. A. (1996). Characterization and cloning of a 58/53-kDa substrate of the insulin receptor tyrosine kinase. J. Biol. Chem. 271, 2921-2928.