β1 Integrin-Focal Adhesion Kinase (FAK) Signaling Modulates Retinal Ganglion Cell (RGC) Survival

PLoS ONE

Volumn 7, Issue 10, 2012, Pages

  Santos, Andrea Rachelle C ^a   Corredor, Raul G ^a   Obeso, Betty Albo ^a   Trakhtenberg, Ephraim F ^a,b   Wang, Ying ^a   Ponmattam, Jamie ^a   Dvoriantchikova, Galina ^a   Ivanov, Dmitry ^a   Shestopalov, Valery I ^a   Goldberg, Jeffrey L ^a,b   Fini, Mary Elizabeth ^a,c   Bajenaru, Michaela Livia ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA1 INTEGRIN; BETA1 INTEGRIN RECEPTOR; FOCAL ADHESION KINASE; GELATINASE B; INTEGRIN; INTEGRIN RECEPTOR; LAMININ; PROTEIN ANTIBODY; PROTEIN BCL XL; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INTERACTION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; IN VITRO STUDY; IN VIVO STUDY; NEUROPROTECTION; NONHUMAN; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RAT; REPERFUSION INJURY; RETINA GANGLION CELL; RETINA ISCHEMIA; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTIGENS, CD29; APOPTOSIS; CELL ADHESION; CELL SURVIVAL; FEMALE; FOCAL ADHESION PROTEIN-TYROSINE KINASES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LAMININ; MATRIX METALLOPROTEINASE 9; NEURITES; RATS; RATS, SPRAGUE-DAWLEY; REPERFUSION INJURY; RETINAL GANGLION CELLS; SIGNAL TRANSDUCTION;

RATTUS;

EID: 84868295061     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0048332     Document Type: Article

References (89)

1. Barros CS, Franco SJ, Muller U, (2011) Extracellular matrix: functions in the nervous system. Cold Spring Harb Perspect Biol 3: a005108.
2. Libby RT, Brunken WJ, Hunter DD, (2000) Roles of the extracellular matrix in retinal development and maintenance. Results Probl Cell Differ 31: 115-140.
3. Libby RT, Champliaud MF, Claudepierre T, Xu Y, Gibbons EP, et al. (2000) Laminin expression in adult and developing retinae: evidence of two novel CNS laminins. J Neurosci 20: 6517-6528.
4. Morissette N, Carbonetto S, (1995) Laminin alpha 2 chain (M chain) is found within the pathway of avian and murine retinal projections. J Neurosci 15: 8067-8082.
5. Sarthy PV, Fu M, (1990) Localization of laminin B1 mRNA in retinal ganglion cells by in situ hybridization. J Cell Biol 110: 2099-2108.
6. Goldberg JL, Espinosa JS, Xu Y, Davidson N, Kovacs GT, et al. (2002) Retinal ganglion cells do not extend axons by default: promotion by neurotrophic signaling and electrical activity. Neuron 33: 689-702.
7. Chintala SK, Zhang X, Austin JS, Fini ME, (2002) Deficiency in matrix metalloproteinase gelatinase B (MMP-9) protects against retinal ganglion cell death after optic nerve ligation. J Biol Chem 277: 47461-47468.
8. Zhang X, Cheng M, Chintala SK, (2004) Kainic acid-mediated upregulation of matrix metalloproteinase-9 promotes retinal degeneration. Invest Ophthalmol Vis Sci 45: 2374-2383.
9. Manabe S, Gu Z, Lipton SA, (2005) Activation of matrix metalloproteinase-9 via neuronal nitric oxide synthase contributes to NMDA-induced retinal ganglion cell death. Invest Ophthalmol Vis Sci 46: 4747-4753.
10. Guo L, Moss SE, Alexander RA, Ali RR, Fitzke FW, et al. (2005) Retinal ganglion cell apoptosis in glaucoma is related to intraocular pressure and IOP-induced effects on extracellular matrix. Invest Ophthalmol Vis Sci 46: 175-182.
11. Aplin AE, Howe A, Alahari SK, Juliano RL, (1998) Signal transduction and signal modulation by cell adhesion receptors: the role of integrins, cadherins, immunoglobulin-cell adhesion molecules, and selectins. Pharmacol Rev 50: 197-263.
12. Clegg DO, Wingerd KL, Hikita ST, Tolhurst EC, (2003) Integrins in the development, function and dysfunction of the nervous system. Front Biosci 8: d723-750.
13. Hynes RO, (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
14. Stupack DG, Cheresh DA, (2002) Get a ligand, get a life: integrins, signaling and cell survival. J Cell Sci 115: 3729-3738.
15. Frisch SM, Screaton RA, (2001) Anoikis mechanisms. Curr Opin Cell Biol 13: 555-562.
16. Luque A, Gomez M, Puzon W, Takada Y, Sanchez-Madrid F, et al. (1996) Activated conformations of very late activation integrins detected by a group of antibodies (HUTS) specific for a novel regulatory region (355-425) of the common beta 1 chain. J Biol Chem 271: 11067-11075.
17. Junk AK, Mammis A, Savitz SI, Singh M, Roth S, et al. (2002) Erythropoietin administration protects retinal neurons from acute ischemia-reperfusion injury. Proc Natl Acad Sci U S A 99: 10659-10664.
18. Selles-Navarro I, Villegas-Perez MP, Salvador-Silva M, Ruiz-Gomez JM, Vidal-Sanz M, (1996) Retinal ganglion cell death after different transient periods of pressure-induced ischemia and survival intervals. A quantitative in vivo study. Invest Ophthalmol Vis Sci 37: 2002-2014.
19. Neufeld AH, Kawai S, Das S, Vora S, Gachie E, et al. (2002) Loss of retinal ganglion cells following retinal ischemia: the role of inducible nitric oxide synthase. Exp Eye Res 75: 521-528.
20. Ju WK, Kim KY, Neufeld AH, (2003) Increased activity of cyclooxygenase-2 signals early neurodegenerative events in the rat retina following transient ischemia. Exp Eye Res 77: 137-145.
21. Otsuka K, Ohshima M, Kaku M, Kajima T, Fukuoka M, et al. (1997) An improved assay method for fibroblast gelatinolytic enzyme. J Nihon Univ Sch Dent 39: 182-190.
22. Barres BA, Silverstein BE, Corey DP, Chun LL, (1988) Immunological, morphological, and electrophysiological variation among retinal ganglion cells purified by panning. Neuron 1: 791-803.
23. Hu Y, Cho S, Goldberg JL, (2010) Neurotrophic effect of a novel TrkB agonist on retinal ganglion cells. Invest Ophthalmol Vis Sci 51: 1747-1754.
24. Meyer-Franke A, Kaplan MR, Pfrieger FW, Barres BA, (1995) Characterization of the signaling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15: 805-819.
25. Buchi ER, Suivaizdis I, Fu J, (1991) Pressure-induced retinal ischemia in rats: an experimental model for quantitative study. Ophthalmologica 203: 138-147.
26. Kaneda K, Kashii S, Kurosawa T, Kaneko S, Akaike A, et al. (1999) Apoptotic DNA fragmentation and upregulation of Bax induced by transient ischemia of the rat retina. Brain Res 815: 11-20.
27. Lam TT, Abler AS, Tso MO, (1999) Apoptosis and caspases after ischemia-reperfusion injury in rat retina. Invest Ophthalmol Vis Sci 40: 967-975.
28. Zhang Y, Cho CH, Atchaneeyasakul LO, McFarland T, Appukuttan B, et al. (2005) Activation of the mitochondrial apoptotic pathway in a rat model of central retinal artery occlusion. Invest Ophthalmol Vis Sci 46: 2133-2139.
29. Limb GA, Daniels JT, Pleass R, Charteris DG, Luthert PJ, et al. (2002) Differential expression of matrix metalloproteinases 2 and 9 by glial Muller cells: response to soluble and extracellular matrix-bound tumor necrosis factor-alpha. Am J Pathol 160: 1847-1855.
30. Sivak JM, Fini ME, (2002) MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology. Prog Retin Eye Res 21: 1-14.
31. Halfter W, Dong S, Schurer B, Osanger A, Schneider W, et al. (2000) Composition, synthesis, and assembly of the embryonic chick retinal basal lamina. Dev Biol 220: 111-128.
32. Halfter W, Dong S, Dong A, Eller AW, Nischt R, (2008) Origin and turnover of ECM proteins from the inner limiting membrane and vitreous body. Eye (Lond) 22: 1207-1213.
33. Vachon PH, (2011) Integrin signaling, cell survival, and anoikis: distinctions, differences, and differentiation. J Signal Transduct 2011: 738137.
34. Parsons JT, (2003) Focal adhesion kinase: the first ten years. J Cell Sci 116: 1409-1416.
35. Mitra SK, Schlaepfer DD, (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr Opin Cell Biol 18: 516-523.
36. Gary DS, Mattson MP, (2001) Integrin signaling via the PI3-kinase-Akt pathway increases neuronal resistance to glutamate-induced apoptosis. J Neurochem 76: 1485-1496.
37. Zhao J, Guan JL, (2009) Signal transduction by focal adhesion kinase in cancer. Cancer Metastasis Rev 28: 35-49.
38. de Curtis I, Reichardt LF, (1993) Function and spatial distribution in developing chick retina of the laminin receptor alpha 6 beta 1 and its isoforms. Development 118: 377-388.
39. Brem RB, Robbins SG, Wilson DJ, O'Rourke LM, Mixon RN, et al. (1994) Immunolocalization of integrins in the human retina. Invest Ophthalmol Vis Sci 35: 3466-3474.
40. Finnemann SC, (2003) Focal adhesion kinase signaling promotes phagocytosis of integrin-bound photoreceptors. EMBO J 22: 4143-4154.
41. Cohen S, (1987) Epidermal growth factor. In Vitro Cell Dev Biol 23: 239-246.
42. Drazba J, Lemmon V, (1990) The role of cell adhesion molecules in neurite outgrowth on Muller cells. Dev Biol 138: 82-93.
43. Brocco MA, Panzetta P, (1999) Survival and process regrowth of purified chick retinal ganglion cells cultured in a growth factor lacking medium at low density. Modulation by extracellular matrix proteins. Brain Res Dev Brain Res 118: 23-32.
44. Gu Z, Cui J, Brown S, Fridman R, Mobashery S, et al. (2005) A highly specific inhibitor of matrix metalloproteinase-9 rescues laminin from proteolysis and neurons from apoptosis in transient focal cerebral ischemia. J Neurosci 25: 6401-6408.
45. Asahi M, Wang X, Mori T, Sumii T, Jung JC, et al. (2001) Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci 21: 7724-7732.
46. Asahi M, Sumii T, Fini ME, Itohara S, Lo EH, (2001) Matrix metalloproteinase 2 gene knockout has no effect on acute brain injury after focal ischemia. Neuroreport 12: 3003-3007.
47. Asahi M, Asahi K, Jung JC, del Zoppo GJ, Fini ME, et al. (2000) Role for matrix metalloproteinase 9 after focal cerebral ischemia: effects of gene knockout and enzyme inhibition with BB-94. J Cereb Blood Flow Metab 20: 1681-1689.
48. Zhang C, Lam TT, Tso MO, (2005) Heterogeneous populations of microglia/macrophages in the retina and their activation after retinal ischemia and reperfusion injury. Exp Eye Res 81: 700-709.
49. Grimpe B, Dong S, Doller C, Temple K, Malouf AT, et al. (2002) The critical role of basement membrane-independent laminin gamma 1 chain during axon regeneration in the CNS. J Neurosci 22: 3144-3160.
50. Tagami Y, Kurimoto T, Miyoshi T, Morimoto T, Sawai H, et al. (2009) Axonal regeneration induced by repetitive electrical stimulation of crushed optic nerve in adult rats. Jpn J Ophthalmol 53: 257-266.
51. Yurchenco PD (2011) Basement membranes: cell scaffoldings and signaling platforms. Cold Spring Harb Perspect Biol 3.
52. Bozzi M, Morlacchi S, Bigotti MG, Sciandra F, Brancaccio A, (2009) Functional diversity of dystroglycan. Matrix Biol 28: 179-187.
53. Li S, Liquari P, McKee KK, Harrison D, Patel R, et al. (2005) Laminin-sulfatide binding initiates basement membrane assembly and enables receptor signaling in Schwann cells and fibroblasts. J Cell Biol 169: 179-189.
54. Weaver CD, Yoshida CK, de Curtis I, Reichardt LF, (1995) Expression and in vitro function of beta 1-integrin laminin receptors in the developing avian ciliary ganglion. J Neurosci 15: 5275-5285.
55. Cabodi S, Di Stefano P, Leal Mdel P, Tinnirello A, Bisaro B, et al. (2010) Integrins and signal transduction. Adv Exp Med Biol 674: 43-54.
56. Gary DS, Milhavet O, Camandola S, Mattson MP, (2003) Essential role for integrin linked kinase in Akt-mediated integrin survival signaling in hippocampal neurons. J Neurochem 84: 878-890.
57. McDonald PC, Fielding AB, Dedhar S, (2008) Integrin-linked kinase-essential roles in physiology and cancer biology. J Cell Sci 121: 3121-3132.
58. Guo S, Kim WJ, Lok J, Lee SR, Besancon E, et al. (2008) Neuroprotection via matrix-trophic coupling between cerebral endothelial cells and neurons. Proc Natl Acad Sci U S A 105: 7582-7587.
59. 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.
60. Ivankovic-Dikic I, Gronroos E, Blaukat A, Barth BU, Dikic I, (2000) Pyk2 and FAK regulate neurite outgrowth induced by growth factors and integrins. Nat Cell Biol 2: 574-581.
61. Robles E, Gomez TM, (2006) Focal adhesion kinase signaling at sites of integrin-mediated adhesion controls axon pathfinding. Nat Neurosci 9: 1274-1283.
62. Girault JA, Costa A, Derkinderen P, Studler JM, Toutant M, (1999) FAK and PYK2/CAKbeta in the nervous system: a link between neuronal activity, plasticity and survival? Trends Neurosci 22: 257-263.
63. Shi Y, Pontrello CG, DeFea KA, Reichardt LF, Ethell IM, (2009) Focal adhesion kinase acts downstream of EphB receptors to maintain mature dendritic spines by regulating cofilin activity. J Neurosci 29: 8129-8142.
64. Frisch SM, Vuori K, Ruoslahti E, Chan-Hui PY, (1996) Control of adhesion-dependent cell survival by focal adhesion kinase. J Cell Biol 134: 793-799.
65. Gibson RM, Craig SE, Heenan L, Tournier C, Humphries MJ, (2005) Activation of integrin alpha5beta1 delays apoptosis of Ntera2 neuronal cells. Mol Cell Neurosci 28: 588-598.
66. Sonoda Y, Matsumoto Y, Funakoshi M, Yamamoto D, Hanks SK, et al. (2000) Anti-apoptotic role of focal adhesion kinase (FAK). Induction of inhibitor-of-apoptosis proteins and apoptosis suppression by the overexpression of FAK in a human leukemic cell line, HL-60. J Biol Chem 275: 16309-16315.
67. Matter ML, Ruoslahti E, (2001) A signaling pathway from the alpha5beta1 and alpha(v)beta3 integrins that elevates bcl-2 transcription. J Biol Chem 276: 27757-27763.
68. Yu WM, Feltri ML, Wrabetz L, Strickland S, Chen ZL, (2005) Schwann cell-specific ablation of laminin gamma1 causes apoptosis and prevents proliferation. J Neurosci 25: 4463-4472.
69. Chen ZL, Haegeli V, Yu H, Strickland S, (2009) Cortical deficiency of laminin gamma1 impairs the AKT/GSK-3beta signaling pathway and leads to defects in neurite outgrowth and neuronal migration. Dev Biol 327: 158-168.
70. Kunzevitzky NJ, Almeida MV, Goldberg JL, (2010) Amacrine cell gene expression and survival signaling: differences from neighboring retinal ganglion cells. Invest Ophthalmol Vis Sci 51: 3800-3812.
71. Kermer P, Klocker N, Labes M, Bahr M, (2000) Insulin-like growth factor-I protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 In vivo. J Neurosci 20: 2-8.
72. Park K, Luo JM, Hisheh S, Harvey AR, Cui Q, (2004) Cellular mechanisms associated with spontaneous and ciliary neurotrophic factor-cAMP-induced survival and axonal regeneration of adult retinal ganglion cells. J Neurosci 24: 10806-10815.
73. Tonges L, Ostendorf T, Lamballe F, Genestine M, Dono R, et al. (2011) Hepatocyte growth factor protects retinal ganglion cells by increasing neuronal survival and axonal regeneration in vitro and in vivo. J Neurochem 117: 892-903.
74. Diem R, Hobom M, Grotsch P, Kramer B, Bahr M, (2003) Interleukin-1 beta protects neurons via the interleukin-1 (IL-1) receptor-mediated Akt pathway and by IL-1 receptor-independent decrease of transmembrane currents in vivo. Mol Cell Neurosci 22: 487-500.
75. Kretz A, Happold CJ, Marticke JK, Isenmann S, (2005) Erythropoietin promotes regeneration of adult CNS neurons via Jak2/Stat3 and PI3K/AKT pathway activation. Mol Cell Neurosci 29: 569-579.
76. Dreixler JC, Hemmert JW, Shenoy SK, Shen Y, Lee HT, et al. (2009) The role of Akt/protein kinase B subtypes in retinal ischemic preconditioning. Exp Eye Res 88: 512-521.
77. Condic ML, Letourneau PC, (1997) Ligand-induced changes in integrin expression regulate neuronal adhesion and neurite outgrowth. Nature 389: 852-856.
78. Plantman S, Novikova L, Novikov L, Hammarberg H, Wallquist W, et al. (2005) Integrin messenger RNAs in the red nucleus after axotomy and neurotrophic administration. Neuroreport 16: 709-713.
79. Gardiner NJ, Fernyhough P, Tomlinson DR, Mayer U, von der Mark H, et al. (2005) Alpha7 integrin mediates neurite outgrowth of distinct populations of adult sensory neurons. Mol Cell Neurosci 28: 229-240.
80. Lemons ML, Condic ML, (2006) Combined integrin activation and intracellular cAMP cause Rho GTPase dependent growth cone collapse on laminin-1. Exp Neurol 202: 324-335.
81. Ivins JK, Yurchenco PD, Lander AD, (2000) Regulation of neurite outgrowth by integrin activation. J Neurosci 20: 6551-6560.
82. Ivins JK, Parry MK, Long DA, (2004) A novel cAMP-dependent pathway activates neuronal integrin function in retinal neurons. J Neurosci 24: 1212-1216.
83. Giancotti FG, Ruoslahti E, (1999) Integrin signaling. Science 285: 1028-1032.
84. Lemons ML, Condic ML, (2008) Integrin signaling is integral to regeneration. Exp Neurol 209: 343-352.
85. Tan CL, Kwok JC, Patani R, Ffrench-Constant C, Chandran S, et al. (2011) Integrin activation promotes axon growth on inhibitory chondroitin sulfate proteoglycans by enhancing integrin signaling. J Neurosci 31: 6289-6295.
86. Neugebauer KM, Reichardt LF, (1991) Cell-surface regulation of beta 1-integrin activity on developing retinal neurons. Nature 350: 68-71.
87. Schwartz MA, Schaller MD, Ginsberg MH, (1995) Integrins: emerging paradigms of signal transduction. Annu Rev Cell Dev Biol 11: 549-599.
88. Molina A, Ubeda M, Escribese MM, Garcia-Bermejo L, Sancho D, et al. (2005) Renal ischemia/reperfusion injury: functional tissue preservation by anti-activated {beta}1 integrin therapy. J Am Soc Nephrol 16: 374-382.
89. Savitz SI, Dhallu MS, Malhotra S, Mammis A, Ocava LC, et al. (2006) EDG receptors as a potential therapeutic target in retinal ischemia-reperfusion injury. Brain Res 1118: 168-175.