Rac1 GTPase-deficient mouse lens exhibits defects in shape, suture formation, fiber cell migration and survival

Developmental Biology

Volumn 360, Issue 1, 2011, Pages 30-43

  Maddala, Rupalatha ^a   Chauhan, Bharesh K ^b   Walker, Christopher ^a   Zheng, Yi ^b   Robinson, Michael L ^c   Lang, Richard A ^b   Rao, Ponugoti V ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c MIAMI UNIVERSITY   (United States)

Author keywords

Cell adhesion; Conditional knockout; Lens fibers; Migration; Rac1 GTPase

Indexed keywords

ABI 2 PROTEIN; BETA CATENIN; CELL PROTEIN; COLLAGEN TYPE 4; CRE RECOMBINASE; FIBRONECTIN; GENE PRODUCT; LAMININ; NECTIN; NERVE CELL ADHESION MOLECULE; NEURAL WISKOTT ALDRICH SYNDROME PROTEIN; NUCLEOSOME ASSEMBLY PROTEIN 1; RAC1 PROTEIN; RAP1 PROTEIN; SCLEROPROTEIN; UNCLASSIFIED DRUG; WAVE2 PROTEIN;

ACTIN POLYMERIZATION; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ELONGATION; CELL INTERACTION; CELL JUNCTION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; CYTOARCHITECTURE; GENE DELETION; GENE INACTIVATION; KNOCKOUT MOUSE; LENS; LENS CAPSULE; LENS DEVELOPMENT; LENS EPITHELIUM; LENS FIBER; LENS SHAPE; LENS SUTURE FORMATION; MORPHOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSGENIC MOUSE;

MUS; MUS MUSCULUS;

EID: 80755153156     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.09.004     Document Type: Article

References (84)

1. Arber S., Barbayannis F.A., Hanser H., Schneider C., Stanyon C.A., Bernard O., Caroni P. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 1998, 393:805-809.
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 Dev. 2000, 14:2701-2711.
3. Bassnett S., Missey H., Vucemilo I. Molecular architecture of the lens fiber cell basal membrane complex. J. Cell Sci. 1999, 112(Pt 13):2155-2165.
4. Bassnett S., Wilmarth P.A., David L.L. The membrane proteome of the mouse lens fiber cell. Mol. Vis. 2009, 15:2448-2463.
5. Baum B., Georgiou M. Dynamics of adherens junctions in epithelial establishment, maintenance, and remodeling. J. Cell Biol. 2011, 192:907-917.
6. Beebe D.C., Cerrelli S. Cytochalasin prevents cell elongation and increases potassium efflux from embryonic lens epithelial cells: implications for the mechanism of lens fiber cell elongation. Lens Eye Toxic. Res. 1989, 6:589-601.
7. Beebe D.C., Vasiliev O., Guo J., Shui Y.B., Bassnett S. Changes in adhesion complexes define stages in the differentiation of lens fiber cells. Invest. Ophthalmol. Vis. Sci. 2001, 42:727-734.
8. Benninger Y., Thurnherr T., Pereira J.A., Krause S., Wu X., Chrostek-Grashoff A., Herzog D., Nave K.A., Franklin R.J., Meijer D., Brakebusch C., Suter U., Relvas J.B. Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J. Cell Biol. 2007, 177:1051-1061.
9. Bokoch G.M. Biology of the p21-activated kinases. Annu. Rev. Biochem. 2003, 72:743-781.
10. Burridge K., Wennerberg K. Rho and Rac take center stage. Cell 2004, 116:167-179.
11. Cain S., Martinez G., Kokkinos M.I., Turner K., Richardson R.J., Abud H.E., Huelsken J., Robinson M.L., de Iongh R.U. Differential requirement for beta-catenin in epithelial and fiber cells during lens development. Dev. Biol. 2008, 321:420-433.
12. Chen Y., Stump R.J., Lovicu F.J., Shimono A., McAvoy J.W. Wnt signaling is required for organization of the lens fiber cell cytoskeleton and development of lens three-dimensional architecture. Dev. Biol. 2008, 324:161-176.
13. Chen L., Melendez J., Campbell K., Kuan C.Y., Zheng Y. Rac1 deficiency in the forebrain results in neural progenitor reduction and microcephaly. Dev. Biol. 2009, 325:162-170.
14. Chow R.L., Lang R.A. Early eye development in vertebrates. Annu. Rev. Cell Dev. Biol. 2001, 17:255-296.
15. Cooper M.A., Son A.I., Komlos D., Sun Y., Kleiman N.J., Zhou R. Loss of ephrin-A5 function disrupts lens fiber cell packing and leads to cataract. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:16620-16625.
16. Coso O.A., Chiariello M., Yu J.C., Teramoto H., Crespo P., Xu N., Miki T., Gutkind J.S. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 1995, 81:1137-1146.
17. Danysh B.P., Duncan M.K. The lens capsule. Exp. Eye Res. 2009, 88:151-164.
18. del Pozo M.A., Price L.S., Alderson N.B., Ren X.D., Schwartz M.A. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 2000, 19:2008-2014.
19. D'Souza-Schorey C., Boettner B., Van Aelst L. Rac regulates integrin-mediated spreading and increased adhesion of T lymphocytes. Mol. Cell. Biol. 1998, 18:3936-3946.
20. Eden S., Rohatgi R., Podtelejnikov A.V., Mann M., Kirschner M.W. Mechanism of regulation of WAVE1-induced actin nucleation by Rac1 and Nck. Nature 2002, 418:790-793.
21. Engers R., Springer E., Michiels F., Collard J.G., Gabbert H.E. Rac affects invasion of human renal cell carcinomas by up-regulating tissue inhibitor of metalloproteinases (TIMP)-1 and TIMP-2 expression. J. Biol. Chem. 2001, 276:41889-41897.
22. Etienne-Manneville S., Hall A. Rho GTPases in cell biology. Nature 2002, 420:629-635.
23. Fukata M., Kaibuchi K. Rho-family GTPases in cadherin-mediated cell-cell adhesion. Nat. Rev. Mol. Cell Biol. 2001, 2:887-897.
24. Fukuyama T., Ogita H., Kawakatsu T., Inagaki M., Takai Y. Activation of Rac by cadherin through the c-Src-Rap1-phosphatidylinositol 3-kinase-Vav2 pathway. Oncogene 2006, 25:8-19.
25. Girao H., Pereira P., Ramalho J., Quinlan R., Prescott A. Cholesterol oxides mediated changes in cytoskeletal organisation involves Rho GTPases small star, filled. Exp. Cell Res. 2003, 291:502-513.
26. Glogauer M., Marchal C.C., Zhu F., Worku A., Clausen B.E., Foerster I., Marks P., Downey G.P., Dinauer M., Kwiatkowski D.J. Rac1 deletion in mouse neutrophils has selective effects on neutrophil functions. J. Immunol. 2003, 170:5652-5657.
27. Grove M., Demyanenko G., Echarri A., Zipfel P.A., Quiroz M.E., Rodriguiz R.M., Playford M., Martensen S.A., Robinson M.R., Wetsel W.C., Maness P.F., Pendergast A.M. ABI2-deficient mice exhibit defective cell migration, aberrant dendritic spine morphogenesis, and deficits in learning and memory. Mol. Cell. Biol. 2004, 24:10905-10922.
28. Halbleib J.M., Nelson W.J. Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 2006, 20:3199-3214.
29. Heasman S.J., Ridley A.J. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 2008, 9:690-701.
30. Hill C.S., Wynne J., Treisman R. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 1995, 81:1159-1170.
31. Hordijk P.L., ten Klooster J.P., van der Kammen R.A., Michiels F., Oomen L.C., Collard J.G. Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 1997, 278:1464-1466.
32. Hotchin N.A., Hall A. The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J. Cell Biol. 1995, 131:1857-1865.
33. Huang T.Y., DerMardirossian C., Bokoch G.M. Cofilin phosphatases and regulation of actin dynamics. Curr. Opin. Cell Biol. 2006, 18:26-31.
34. Kawakatsu T., Shimizu K., Honda T., Fukuhara T., Hoshino T., Takai Y. Trans-interactions of nectins induce formation of filopodia and Lamellipodia through the respective activation of Cdc42 and Rac small G proteins. J. Biol. Chem. 2002, 277:50749-50755.
35. Kheradmand F., Werner E., Tremble P., Symons M., Werb Z. Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science 1998, 280:898-902.
36. Kooistra M.R., Dube N., Bos J.L. Rap1: a key regulator in cell-cell junction formation. J. Cell Sci. 2007, 120:17-22.
37. Kunda P., Craig G., Dominguez V., Baum B. Abi, Sra1, and Kette control the stability and localization of SCAR/WAVE to regulate the formation of actin-based protrusions. Curr. Biol. 2003, 13:1867-1875.
38. Kuszak J.R.a.C.M.J. The structure of the vertebrate lens. Development of the Ocular lens 2004, 71-118. Cambridge Univ Press, Cambridge. F.J. Lovicu, M.L. Robinson (Eds.).
39. Kuszak J.R., Zoltoski R.K., Sivertson C. Fibre cell organization in crystalline lenses. Exp. Eye Res. 2004, 78:673-687.
40. Lovicu F.J., McAvoy J.W. Growth factor regulation of lens development. Dev. Biol. 2005, 280:1-14.
41. Maddala R., Peng Y.W., Rao P.V. Selective expression of the small GTPase RhoB in the early developing mouse lens. Dev. Dyn. 2001, 222:534-537.
42. Maddala R., Reddy V.N., Epstein D.L., Rao V. Growth factor induced activation of Rho and Rac GTPases and actin cytoskeletal reorganization in human lens epithelial cells. Mol. Vis. 2003, 9:329-336.
43. Maddala R., Deng P.F., Costello J.M., Wawrousek E.F., Zigler J.S., Rao V.P. Impaired cytoskeletal organization and membrane integrity in lens fibers of a Rho GTPase functional knockout transgenic mouse. Lab. Invest. 2004, 84:679-692.
44. Maddala R., Reneker L.W., Pendurthi B., Rao P.V. Rho GDP dissociation inhibitor-mediated disruption of Rho GTPase activity impairs lens fiber cell migration, elongation and survival. Dev. Biol. 2008, 315:217-231.
45. Maddala R., Skiba N.P., Lalane R., Sherman D.L., Brophy P.J., Rao P.V. Periaxin is required for hexagonal geometry and membrane organization of mature lens fibers. Dev. Biol. 2011, 357:179-190.
46. Malliri A., Collard J.G. Role of Rho-family proteins in cell adhesion and cancer. Curr. Opin. Cell Biol. 2003, 15:583-589.
47. McAvoy J.W. Induction of the eye lens. Differentiation 1980, 17:137-149.
48. Menko S.a.W.J.L. Role of matrix and cell adhesion molecules in lens differentiation 2004, 245-260. Cambridge University Press. F.L. Lovicu, M.L. Robinson (Eds.).
49. Minden A., Lin A., Claret F.X., Abo A., Karin M. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 1995, 81:1147-1157.
50. Mousa G.Y., Trevithick J.R. Differentiation of rat lens epithelial cells in tissue culture. II. Effects of cytochalasins B and D on actin organization and differentiation. Dev. Biol. 1977, 60:14-25.
51. Murga C., Zohar M., Teramoto H., Gutkind J.S. Rac1 and RhoG promote cell survival by the activation of PI3K and Akt, independently of their ability to stimulate JNK and NF-kappaB. Oncogene 2002, 21:207-216.
52. Nishida K., Kaziro Y., Satoh T. Anti-apoptotic function of Rac in hematopoietic cells. Oncogene 1999, 18:407-415.
53. Pollitt A.Y., Insall R.H. WASP and SCAR/WAVE proteins: the drivers of actin assembly. J. Cell Sci. 2009, 122:2575-2578.
54. Pontoriero G.F., Smith A.N., Miller L.A., Radice G.L., West-Mays J.A., Lang R.A. Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev. Biol. 2009, 326:403-417.
55. Price L.S., Leng J., Schwartz M.A., Bokoch G.M. Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 1998, 9:1863-1871.
56. Quinlan R.a.P.A. Lens cell cytoskeleton 2004, 173-187. Cambridge University Press. F.J. Lovicu, M.L. Robinson (Eds.).
57. Rafferty N.S., Scholz D.L. Development of actin polygonal arrays in rabbit lens epithelial cells. Curr. Eye Res. 1991, 10:637-643.
58. Raftopoulou M., Hall A. Cell migration: Rho GTPases lead the way. Dev. Biol. 2004, 265:23-32.
59. Ramaekers F.C., Boomkens T.R., Bloemendal H. Cytoskeletal and contractile structures in bovine lens cell differentiation. Exp. Cell Res. 1981, 135:454-461.
60. Rao P.V., Maddala R. The role of the lens actin cytoskeleton in fiber cell elongation and differentiation. Semin. Cell Dev. Biol. 2006, 17:698-711.
61. Rao P.V., Maddala R., John F., Zigler J.S. Expression of nonphagocytic NADPH oxidase system in the ocular lens. Mol. Vis. 2004, 10:112-121.
62. Ridley A.J. Rho family proteins: coordinating cell responses. Trends Cell Biol. 2001, 11:471-477.
63. Ridley A.J. Rho GTPases and cell migration. J. Cell Sci. 2001, 114:2713-2722.
64. Ridley A.J. Life at the leading edge. Cell 2011, 145:1012-1022.
65. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
66. Rivera C., Yamben I.F., Shatadal S., Waldof M., Robinson M.L., Griep A.E. Cell-autonomous requirements for Dlg-1 for lens epithelial cell structure and fiber cell morphogenesis. Dev. Dyn. 2009, 238:2292-2308.
67. Sander E.E., van Delft S., ten Klooster J.P., Reid T., van der Kammen R.A., Michiels F., Collard J.G. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 1998, 143:1385-1398.
68. Simirskii V.N., Wang Y., Duncan M.K. Conditional deletion of beta1-integrin from the developing lens leads to loss of the lens epithelial phenotype. Dev. Biol. 2007, 306:658-668.
69. Soderling S.H., Binns K.L., Wayman G.A., Davee S.M., Ong S.H., Pawson T., Scott J.D. The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat. Cell Biol. 2002, 4:970-975.
70. Stradal T.E., Rottner K., Disanza A., Confalonieri S., Innocenti M., Scita G. Regulation of actin dynamics by WASP and WAVE family proteins. Trends Cell Biol. 2004, 14:303-311.
71. Straub B.K., Boda J., Kuhn C., Schnoelzer M., Korf U., Kempf T., Spring H., Hatzfeld M., Franke W.W. A novel cell-cell junction system: the cortex adhaerens mosaic of lens fiber cells. J. Cell Sci. 2003, 116:4985-4995.
72. Takai Y., Miyoshi J., Ikeda W., Ogita H. Nectins and nectin-like molecules: roles in contact inhibition of cell movement and proliferation. Nat. Rev. Mol. Cell Biol. 2008, 9:603-615.
73. Takenawa T., Suetsugu S. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 2007, 8:37-48.
74. Vielkind S., Gallagher-Gambarelli M., Gomez M., Hinton H.J., Cantrell D.A. Integrin regulation by RhoA in thymocytes. J. Immunol. 2005, 175:350-357.
75. Walker J., Menko A.S. Integrins in lens development and disease. Exp. Eye Res. 2009, 88:216-225.
76. Wang L., Zheng Y. Cell type-specific functions of Rho GTPases revealed by gene targeting in mice. Trends Cell Biol. 2007, 17:58-64.
77. Weber G.F., Menko A.S. Actin filament organization regulates the induction of lens cell differentiation and survival. Dev. Biol. 2006, 295:714-729.
78. Weber G.F., Menko A.S. Phosphatidylinositol 3-kinase is necessary for lens fiber cell differentiation and survival. Invest. Ophthalmol. Vis. Sci. 2006, 47:4490-4499.
79. Wells C.M., Walmsley M., Ooi S., Tybulewicz V., Ridley A.J. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J. Cell Sci. 2004, 117:1259-1268.
80. Yamazaki D., Suetsugu S., Miki H., Kataoka Y., Nishikawa S., Fujiwara T., Yoshida N., Takenawa T. WAVE2 is required for directed cell migration and cardiovascular development. Nature 2003, 424:452-456.
81. Yang N., Higuchi O., Ohashi K., Nagata K., Wada A., Kangawa K., Nishida E., Mizuno K. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 1998, 393:809-812.
82. Yap A.S., Kovacs E.M. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell Biol. 2003, 160:11-16.
83. Zelenka P.S. Regulation of cell adhesion and migration in lens development. Int. J. Dev. Biol. 2004, 48:857-865.
84. Zhao H., Yang Y., Rizo C.M., Overbeek P.A., Robinson M.L. Insertion of a Pax6 consensus binding site into the alphaA-crystallin promoter acts as a lens epithelial cell enhancer in transgenic mice. Invest. Ophthalmol. Vis. Sci. 2004, 45:1930-1939.