Distinct roles for N-Cadherin linked c-Src and fyn kinases in lens development

Developmental Dynamics

Volumn 242, Issue 5, 2013, Pages 469-484

  Leonard, Michelle ^a   Zhang, Liping ^a   Bleaken, Brigid M ^a   Menko, A Sue ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

C Src; Fyn; Lens differentiation; Morphogenesis; Src family kinases

Indexed keywords

NERVE CELL ADHESION MOLECULE; PROTEIN KINASE FYN; PROTEIN KINASE P60; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL ELONGATION; CELL JUNCTION; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; EPITHELIUM CELL; EYE DEVELOPMENT; LENS; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

EID: 84876502294     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.23935     Document Type: Article

References (74)

1. Andley UP. 2007. Crystallins in the eye: function and pathology. Prog Retin Eye Res 26:78-98.
2. Avizienyte E, Wyke AW, Jones RJ, McLean GW, Westhoff MA, Brunton VG, Frame MC. 2002. Src-induced de-regulation of E-cadherin in colon cancer cells requires integrin signalling. Nat Cell Biol 4:632-638.
3. Balsamo J, Arregui C, Leung T, Lilien J. 1998. The nonreceptor protein tyrosine phosphatase PTP1B binds to the cytoplasmic domain of N-cadherin and regulates the cadherin-actin linkage. J Cell Biol 143:523-532.
4. Blankenship TN, Hess JF, FitzGerald PG. 2001. Development- and differentiation-dependent reorganization of intermediate filaments in fiber cells. Invest Ophthalmol Vis Sci 42:735-742.
5. Bozulic LD, Dean WL, Delamere NA. 2004. The influence of Lyn kinase on Na, K-ATPase in porcine lens epithelium. Am J Physiol Cell Physiol 286:C90-96.
6. Brackenbury WJ, Davis TH, Chen C, Slat EA, Detrow MJ, Dickendesher TL, Ranscht B, Isom LL. 2008. Voltage-gated Na+ channel beta1 subunit-mediated neurite outgrowth requires Fyn kinase and contributes to postnatal CNS development in vivo. J Neurosci 28:3246-3256.
7. Braga VM. 2002. Cell-cell adhesion and signalling. Curr Opin Cell Biol 14:546-556.
8. Bromann PA, Korkaya H, Courtneidge SA. 2004. The interplay between Src family kinases and receptor tyrosine kinases. Oncogene 23:7957-7968.
9. Brown MT, Cooper JA. 1996. Regulation, substrates and functions of src. Biochim Biophys Acta 1287:121-149.
10. Calautti E, Missero C, Stein PL, Ezzell RM, Dotto GP. 1995. fyn tyrosine kinase is involved in keratinocyte differentiation control. Genes Dev 9:2279-2291.
11. Calautti E, Cabodi S, Stein PL, Hatzfeld M, Kedersha N, Paolo Dotto G. 1998. Tyrosine phosphorylation and src family kinases control keratinocyte cell-cell adhesion. J Cell Biol 141:1449-1465.
12. Cary LA, Han DC, Guan JL. 1999. Integrin-mediated signal transduction pathways. Histol Histopathol 14:1001-1009.
13. Colognato H, Ramachandrappa S, Olsen IM, ffrench-Constant C. 2004. Integrins direct Src family kinases to regulate distinct phases of oligodendrocyte development. J Cell Biol 167:365-375.
14. Crisanti-Combes P, Lorinet AM, Girard A, Pessac B, Wasseff M, Calothy G. 1982. Effects of Rous sarcoma virus on the differentiation of chick and quail neuroretina cells in culture. Adv Exp Med Biol 158:115-122.
15. Cvekl A, Duncan MK. 2007. Genetic and epigenetic mechanisms of gene regulation during lens development. Prog Retin Eye Res 26:555-597.
16. Duncan MK, Cui W, Oh DJ, Tomarev SI. 2002. Prox1 is differentially localized during lens development. Mech Dev 112:195-198.
17. Falcone G, Alema S, Tato F. 1991. Transcription of muscle-specific genes is repressed by reactivation of pp60v-src in postmitotic quail myotubes. Mol Cell Biol 11:3331-3338.
18. Falcone G, Ciuffini L, Gauzzi MC, Provenzano C, Strano S, Gallo R, Castellani L, Alema S. 2003. v-Src inhibits myogenic differentiation by interfering with the regulatory network of muscle-specific transcriptional activators at multiple levels. Oncogene 22:8302-8315.
19. Ferreira-Cornwell MC, Veneziale RW, Grunwald GB, Menko AS. 2000. N-cadherin function is required for differentiation-dependent cytoskeletal reorganization in lens cells in vitro. Exp Cell Res 256:237-247.
20. Frame MC. 2004. Newest findings on the oldest oncogene; how activated src does it. J Cell Sci 117:989-998.
21. Frame MC, Fincham VJ, Carragher NO, Wyke JA. 2002. v-Src's hold over actin and cell adhesions. Nat Rev Mol Cell Biol 3:233-245.
22. Goodwin M, Kovacs EM, Thoreson MA, Reynolds AB, Yap AS. 2003. Minimal mutation of the cytoplasmic tail inhibits the ability of E-cadherin to activate Rac but not phosphatidylinositol 3-kinase: direct evidence of a role for cadherin-activated Rac signaling in adhesion and contact formation. J Biol Chem 278:20533-20539.
23. Goto J, Tezuka T, Nakazawa T, Sagara H, Yamamoto T. 2008. Loss of Fyn tyrosine kinase on the C57BL/6 genetic background causes hydrocephalus with defects in oligodendrocyte development. Mol Cell Neurosci 38:203-212.
24. Grant SG, O'Dell TJ, Karl KA, Stein PL, Soriano P, Kandel ER. 1992. Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258:1903-1910.
25. Guermah M, Gillet G, Michel D, Laugier D, Brun G, Calothy G. 1990. Down regulation by p60v-src of genes specifically expressed and developmentally regulated in postmitotic quail neuroretina cells. Mol Cell Biol 10:3584-3590.
26. Hamaguchi M, Matsuyoshi N, Ohnishi Y, Gotoh B, Takeichi M, Nagai Y. 1993. p60v-src causes tyrosine phosphorylation and inactivation of the N-cadherin-catenin cell adhesion system. Embo J 12:307-314.
27. Leonard M, Chan Y, Menko AS. 2008. Identification of a novel intermediate filament-linked N-cadherin/gamma-catenin complex involved in the establishment of the cytoarchitecture of differentiated lens fiber cells. Dev Biol 319:298-308.
28. Leonard M, Zhang L, Zhai N, Cader A, Chan Y, Nowak RB, Fowler VM, Menko AS. 2011. Modulation of N-cadherin junctions and their role as epicenters of differentiation-specific actin regulation in the developing lens. Dev Biol 349:363-377.
29. Liang X, Draghi NA, Resh MD. 2004. Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 24:7140-7149.
30. Lilien J, Balsamo J. 2005. The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of beta-catenin. Curr Opin Cell Biol 17:459-465.
31. Lowell CA, Soriano P. 1996. Knockouts of Src-family kinases: stiff bones, wimpy T cells, and bad memories. Genes Dev 10:1845-1857.
32. Marzia M, Sims NA, Voit S, Migliaccio S, Taranta A, Bernardini S, Faraggiana T, Yoneda T, Mundy GR, Boyce BF, Baron R, Teti A. 2000. Decreased c-Src expression enhances osteoblast differentiation and bone formation. J Cell Biol 151:311-320.
33. Matsuyoshi N, Hamaguchi M, Taniguchi S, Nagafuchi A, Tsukita S, Takeichi M. 1992. Cadherin-mediated cell-cell adhesion is perturbed by v-src tyrosine phosphorylation in metastatic fibroblasts. J Cell Biol 118:703-714.
34. McLachlan RW, Kraemer A, Helwani FM, Kovacs EM, Yap AS. 2007. E-cadherin adhesion activates c-Src signaling at cell-cell contacts. Mol Biol Cell 18:3214-3223.
35. Menko AS. 2002. Lens epithelial cell differentiation. Exp Eye Res 75:485-490.
36. Menko AS, Boettiger D. 1988. Inhibition of chicken embryo lens differentiation and lens junction formation in culture by pp60v-src. Mol Cell Biol 8:1414-1420.
37. Menko AS, Klukas KA, Johnson RG. 1984. Chicken embryo lens cultures mimic differentiation in the lens. Dev Biol 103:129-141.
38. Menko AS, Klukas KA, Liu TF, Quade B, Sas DF, Preus DM, Johnson RG. 1987. Junctions between lens cells in differentiating cultures: structure, formation, intercellular permeability, and junctional protein expression. Dev Biol 123:307-320.
39. Mitra SK, Schlaepfer DD. 2006. Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18:516-523.
40. Muto M, Yoshimura M, Okayama M, Kaji A. 1977. Cellular transformation and differentiation. Effect of Rous sarcoma virus transformation on sulfated proteoglycan synthesis by chicken chondrocytes. Proc Natl Acad Sci USA 74:4173-4177.
41. Nakagawa M, Fukata M, Yamaga M, Itoh N, Kaibuchi K. 2001. Recruitment and activation of Rac1 by the formation of E-cadherin-mediated cell-cell adhesion sites. J Cell Sci 114:1829-1838.
42. Noren NK, Niessen CM, Gumbiner BM, Burridge K. 2001. Cadherin engagement regulates Rho family GTPases. J Biol Chem 276:33305-33308.
43. Osterhout DJ, Wolven A, Wolf RM, Resh MD, Chao MV. 1999. Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase. J Cell Biol 145:1209-1218.
44. Ozawa M, Ohkubo T. 2001. Tyrosine phosphorylation of p120(ctn) in v-Src transfected L cells depends on its association with E-cadherin and reduces adhesion activity. J Cell Sci 114:503-512.
45. Pedraza LG, Stewart RA, Li DM, Xu T. 2004. Drosophila Src-family kinases function with Csk to regulate cell proliferation and apoptosis. Oncogene 23:4754-4762.
46. Perez-Moreno M, Jamora C, Fuchs E. 2003. Sticky business: orchestrating cellular signals at adherens junctions. Cell 112:535-548.
47. Pierani A, Pouponnot C, Calothy G. 1993. Transcriptional downregulation of the retina-specific QR1 gene by pp60v-src and identification of a novel v-src-responsive unit. Mol Cell Biol 13:3401-3414.
48. Pontoriero GF, Smith AN, Miller LA, Radice GL, West-Mays JA, Lang RA. 2009. Co-operative roles for E-cadherin and N-cadherin during lens vesicle separation and lens epithelial cell survival. Dev Biol 326:403-417.
49. Relucio J, Tzvetanova ID, Ao W, Lindquist S, Colognato H. 2009. Laminin alters fyn regulatory mechanisms and promotes oligodendrocyte development. J Neurosci 29:11794-11806.
50. Roura S, Miravet S, Piedra J, Garcia de Herreros A, Dunach M. 1999. Regulation of E-cadherin/Catenin association by tyrosine phosphorylation. J Biol Chem 274:36734-36740.
51. Samayawardhena LA, Kapur R, Craig AW. 2007. Involvement of Fyn kinase in Kit and integrin-mediated Rac activation, cytoskeletal reorganization, and chemotaxis of mast cells. Blood 109:3679-3686.
52. Schnekenburger J, Mayerle J, Simon P, Domschke W, Lerch MM. 1999. Protein tyrosine dephosphorylation and the maintenance of cell adhesions in the pancreas. Ann NY Acad Sci 880:157-165.
53. Schwartzberg PL. 1998. The many faces of Src: multiple functions of a prototypical tyrosine kinase. Oncogene 17:1463-1468.
54. Shattil SJ. 2005. Integrins and Src: dynamic duo of adhesion signaling. Trends Cell Biol 15:399-403.
55. Stein PL, Vogel H, Soriano P. 1994. Combined deficiencies of Src, Fyn, and Yes tyrosine kinases in mutant mice. Genes Dev 8:1999-2007.
56. Takeda H, Nagafuchi A, Yonemura S, Tsukita S, Behrens J, Birchmeier W. 1995. V-src kinase shifts the cadherin-based cell adhesion from the strong to the weak state and beta catenin is not required for the shift. J Cell Biol 131:1839-1847.
57. Tamiya S, Delamere NA. 2005. Studies of tyrosine phosphorylation and Src family tyrosine kinases in the lens epithelium. Invest Ophthalmol Vis Sci 46:2076-2081.
58. Thomas SM, Brugge JS. 1997. Cellular functions regulated by Src family kinases. Annu Rev Cell Dev Biol 13:513-609.
59. Ukropec JA, Hollinger MK, Salva SM, Woolkalis MJ. 2000. SHP2 association with VE-cadherin complexes in human endothelial cells is regulated by thrombin. J Biol Chem 275:5983-5986.
60. Veracini L, Franco M, Boureux A, Simon V, Roche S, Benistant C. 2005. Two functionally distinct pools of Src kinases for PDGF receptor signalling. Biochem Soc Trans 33:1313-1315.
61. Volberg T, Geiger B, Dror R, Zick Y. 1991. Modulation of intercellular adherens-type junctions and tyrosine phosphorylation of their components in RSV-transformed cultured chick lens cells. Cell Regul 2:105-120.
62. Wadham C, Gamble JR, Vadas MA, Khew-Goodall Y. 2003. The protein tyrosine phosphatase Pez is a major phosphatase of adherens junctions and dephosphorylates beta-catenin. Mol Biol Cell 14:2520-2529.
63. Walker JL, Menko AS. 1999. alpha6 Integrin is regulated with lens cell differentiation by linkage to the cytoskeleton and isoform switching. Dev Biol 210:497-511.
64. Walker JL, Zhang L, Menko AS. 2002a. Transition between proliferation and differentiation for lens epithelial cells is regulated by Src family kinases. Dev Dyn 224:361-372.
65. Walker JL, Zhang L, Zhou J, Woolkalis MJ, Menko AS. 2002b. Role for alpha 6 integrin during lens development: Evidence for signaling through IGF-1R and ERK. Dev Dyn 223:273-284.
66. Weber GF, Menko AS. 2006a. Actin filament organization regulates the induction of lens cell differentiation and survival. Dev Biol 295:714-729.
67. Weber GF, Menko AS. 2006b. Phosphatidylinositol 3-kinase is necessary for lens fiber cell differentiation and survival. Invest Ophthalmol Vis Sci 47:4490-4499.
68. Wigle JT, Chowdhury K, Gruss P, Oliver G. 1999. Prox1 function is crucial for mouse lens-fibre elongation. Nat Genet 21:318-322.
69. Wolf RM, Wilkes JJ, Chao MV, Resh MD. 2001. Tyrosine phosphorylation of p190 RhoGAP by Fyn regulates oligodendrocyte differentiation. J Neurobiol 49:62-78.
70. Xie Z, Singleton PA, Bourguignon LY, Bikle DD. 2005. Calcium-induced human keratinocyte differentiation requires src- and fyn-mediated phosphatidylinositol 3-kinase-dependent activation of phospholipase C-gamma1. Mol Biol Cell 16:3236-3246.
71. Xu L, Overbeek PA, Reneker LW. 2002. Systematic analysis of E-, N- and P-cadherin expression in mouse eye development. Exp Eye Res 74:753-760.
72. Yoshimura M, Iwasaki Y, Kaji A. 1981. In vitro differentiation of chicken embryo skin cells transformed by Rous sarcoma virus. J Cell Physiol 109:373-385.
73. Zheng X, Resnick RJ, Shalloway D. 2008. Apoptosis of estrogen-receptor negative breast cancer and colon cancer cell lines by PTP alpha and src RNAi. Int J Cancer 122:1999-2007.
74. Zhou J, Menko AS. 2004. Coordinate signaling by Src and p38 kinases in the induction of cortical cataracts. Invest Ophthalmol Vis Sci 45:2314-2323.