IGF-1 regulates the extracellular level of active MMP-2 and promotes müller glial cell motility

Investigative Ophthalmology and Visual Science

Volumn 56, Issue 11, 2015, Pages 6948-6960

  Lorenc, Valeria E ^a   Jaldín Fincati, Javier R ^a   Luna, José D ^b   Chiabrando, Gustavo A ^a   Sánchez, María C ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b Fundacion VER   (Argentina)

Author keywords

Cell migration; Glial cell; Metalloproteinases

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; BETA1 INTEGRIN; F ACTIN; GELATINASE; GELATINASE A; ILOMASTAT; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B; SOMATOMEDIN C;

ACTIN FILAMENT; ARTICLE; BIOTINYLATION; CELL LYSATE; CELL MIGRATION; CELL MIGRATION ASSAY; CELL MOTILITY; CONFOCAL MICROSCOPY; ENZYME ACTIVITY; FOCAL ADHESION; GLIA CELL; IMMUNOFLUORESCENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; WESTERN BLOTTING; ZYMOGRAPHY; CELL LINE; CELL MOTION; ENZYME ACTIVATION; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; MACROGLIA; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANTIGENS, CD29; BLOTTING, WESTERN; CELL LINE; CELL MOVEMENT; ENZYME ACTIVATION; EPENDYMOGLIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MATRIX METALLOPROTEINASE 2; MICROSCOPY, CONFOCAL; SIGNAL TRANSDUCTION;

EID: 84945927013     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-17496     Document Type: Article

References (76)

1. Laviola L, Natalicchio A, Giorgino F. The IGF-I signaling pathway. Curr Pharm Des. 2007;13:663-669
2. Dupont J, LeRoith D. Insulin and insulin-like growth factorí receptors: similarities and differences in signal transduction. Horm Res. 2001;55(suppl 2):22-26
3. Bondy CA. TransientíGF-I gene expression during the maturation of functionally related central projection neurons. J Neurosci. 1991;11:3442-3455
4. Lieskovska J, Ling Y, Badley-Clarke J, Clemmons DR. The role of Src kinase in insulin-like growth factor-dependent mitogenic signaling in vascular smooth muscle cells. J Biol Chem. 2006; 281:25041-25053
5. Reinhardt RR, Bondy CA. Insulin-like growth factors cross the blood-brain barrier. Endocrinology. 1994;135:1753-1761
6. Wikstrand MH, Hård AL, Niklasson A, Hellström A. Birth weight deviation and early postnatal growth are related to optic nerve morphology at school age in children born preterm. Pediatr Res. 2010;6:325-329
7. Villacampa P, Haurigot V, Bosch F. Proliferative retinopathies: animal models and therapeutic opportunities. Curr Neurovasc Res. 2015;12:189-198
8. Meyer-Schwickerath R, Pfeiffer A, Blum WF, et al. Vitreous levels of the insulin-like growth factorsí andíI, and the insulin- like growth factor binding proteins 2 and 3, increase in neovascular eye disease. Studies in nondiabetic and diabetic subjects. J Clinínvest. 1993;92:2620-2625
9. Boulton M, Gregor Z, McLeod D, et al. Intravitreal growth factors in proliferative diabetic retinopathy: correlation with neovascular activity and glycaemic management. Br J Oph- thalmol. 1997;81:228-233
10. Waldbillig RJ, Jones BE, Schoen TJ, et al. Vitreal insulin-like growth factor binding proteins (IGFBPs) are increased in human and animal diabetics. Curr Eye Res. 1994;13:539-546
11. Hellstrom A, Smith LE, Dammann O. Retinopathy of prematurity. Lancet. 2013;382:1445-1457
12. Newman E, Reichenbach A. The Müller cell: a functional element of the retina. Trends Neurosci. 1996;19:307-312
13. Bringmann A, Pannicke T, Grosche J, et al. Müller cells in the healthy and diseased retina. Prog Retin Eye Res. 2006;25:397-424
14. Reichenbach A, Stolzenburg JU, Eberhardt W, Chao TI, Dettmer D, Hertz L. What do retinal Müller (glial) cells do for their neuronal ‘‘small siblings’’? J Chem Neuroanat. 1993; 6:201-213
15. Reichenbach A, Bringmann A. New functions of Müller cells. Glia. 2013;61:651-678
16. Morimoto T, Miyoshi T, Matsuda S, Tano Y, Fujikado T, Fukuda Y. Transcorneal electrical stimulation rescues axotomized retinal ganglion cells by activating endogenous retinalíGF-1 system. Invest Ophthalmol Vis Sci. 2005;46:2147-2155
17. Sato T, Fujikado T, Morimoto T, Matsushita K, Harada T, Tano Y. Effect of electrical stimulation oníGF-1 transcription by L-type calcium channels in cultured retinal Müller cells. Jpn J Ophthalmol. 2008;52:217-223
18. Mizutani M, Gerhardinger C, Lorenzi M. Müller cell changes in human diabetic retinopathy. Diabetes. 1998;47:445-449
19. Feist RM Jr., King JL, Morris R, Witherspoon CD, Guidry C. Myofibroblast and extracellular matrix origins in proliferative vitreoretinopathy. Graefes Arch Clin Exp Ophthalmol. 2014; 252:347-357
20. Hiscott P, Sheridan C, Magee RM, Grierson I. Matrix and the retinal pigment epithelium in proliferative retinal disease. Prog Retin Eye Res. 1999;18:167-190
21. Casaroli Marano RP, Preissner KT, Vilaro S. Fibronectin, laminin, vitronectin and their receptors at newly-formed capillaries in proliferative diabetic retinopathy. Exp Eye Res. 1995;60:5-17
22. Limb GA, Daniels JT, Pleass R, Charteris DG, Luthert PJ, Khaw PT. Differential expression of matrix metalloproteinases 2 and 9 by glial Müller cells: response to soluble and extracellular matrix-bound tumor necrosis factor-alpha. Am J Pathol. 2002; 160:1847-1855
23. Miyata Y, Kase M, Sugita Y, et al. Protein kinase C-mediated regulation of matrix metalloproteinase and tissue inhibitor of metalloproteinase production in a human retinal Müller cells. Curr Eye Res. 2012;37;842-849
24. Limb GA, Little BC, Meager A, et al. Cytokines in proliferative vitreoretinopathy. Eye (Lond). 1991;5(pt 6):686-693
25. Franks WA, Limb GA, Stanford MR, et al. Cytokines in human intraocular inflammation. Curr Eye Res. 1992;11(suppl):187-191
26. Limb GA, Alam A, Earley O, Green W, Chignell AH, Dumonde DC. Distribution of cytokine proteins within epiretinal membranes in proliferative vitreoretinopathy. Curr Eye Res. 1994;13:791-798
27. Limb GA, Chignell AH, Green W, LeRoy F, Dumonde DC. Distribution of TNF alpha and its reactive vascular adhesion molecules in fibrovascular membranes of proliferative diabetic retinopathy. Br J Ophthalmol. 1996;80:168-173
28. Barcelona PF, Jaldín-Fincati JR, Sánchez MC, Chiabrando GA. Activated alpha2-macroglobulin induces Müllerglial cell migration by regulating MT1-MMP activity through LRP1. FASEB J. 2013;27:3181-3197
29. Chesik D, De Keyser J, Bron R, Fuhler GM. Insulin-like growth factor binding protein-1 activates integrin-mediated intracellular signaling and migration in oligodendrocytes. J Neurochem. 2010;113:1319-1330
30. Faber-Elman A, Solomon A, Abraham JA, Marikovsky M, Schwartz M. Involvement of wound-associated factors in rat brain astrocyte migratory response to axonal injury: in vitro simulation. J Clinínvest. 1996;97:162-171
31. Jiang J, McMurtry J, Niedzwiecki D, Goldman SA. Insulin-like growth factor-1 is a radial cell-associated neurotrophin that promotes neuronal recruitment from the adult songbird edpendyma/subependyma. J Neurobiol. 1998;36:1-15
32. Long L, Navab R, Brodt P. Regulation of the Mr 72,000 typeíV collagenase by the typeí insulin-like growth factor receptor. Cancer Res. 1998;58:3243-3247
33. Zhang D, Bar-Eli M, Meloche S, Brodt P. Dual regulation of MMP-2 expression by the type 1 insulin-like growth factor receptor: the phosphatidylinositol 3-kinase/Akt and Raf/ERK pathways transmit opposing signals. J Biol Chem. 2004;279: 19683-19690
34. Stetler-Stevenson WG. The role of matrix metalloproteinases in tumor invasion, metastasis, and angiogenesis. Surg Oncol Clin N Am. 2001;10:383-392, x
35. Seiki M Yanaí. Roles of pericellular proteolysis by membrane type-1 matrix metalloproteinase in cancer invasion and angiogenesis. Cancer Sci. 2003;94:569-574
36. Sanchez MC, Luna JD, Barcelona PF, et al. Effect of retinal laser photocoagulation on the activity of metalloproteinases and the alpha(2)-macroglobulin proteolytic state in the vitreous of eyes with proliferative diabetic retinopathy. Exp Eye Res. 2007;85:644-650
37. Grant MB, Schmetz I, Russell B, Harwood HJ Jr., Silverstein J, Merimee TJ. Changes in insulin-like growth factorsí andíI and their binding protein after a single intramuscular injection of growth hormone. J Clin Endocrinol Metab. 1986;63:981-984
38. Limb GA, Salt TE, Munro PM, Moss SE, Khaw PT. In vitro characterization of a spontaneously immortalized human Müller cell line (MIO-M1). Invest Ophthalmol Vis Sci. 2002; 43:864-869
39. Kleiner DE, Stetler-Stevenson, WG. Quantitative zymography: detection of picogram quantities of gelatinases. Anal Biochem. 1994;218:325-329
40. Rivera S, Ogier C, Jourquin J, et al. Gelatinase B and TIMP-1 are regulated in a cell- and time-dependent manner in association with neuronal death and glial reactivity after global forebrain ischemia. Eur J Neurosci. 2002;15:19-32
41. Bolte S, Cordelieres, FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc. 2006; 224(pt 3):213-232
42. Li YM, Schacher DH, Liu Q, et al. Regulation of myeloid growth and differentiation by the insulin-like growth factorí receptor. Endocrinology. 1997;138:362-368
43. Strongin AY. Proteolytic and non-proteolytic roles of membrane type-1 matrix metalloproteinase in malignancy. Biochim Biophys Acta. 2010;1803:133-141
44. Frittoli E, Palamidessi A, Disanza A, Scita G. Secretory and endo/exocytic trafficking in invadopodia formation: the MT1- MMP paradigm. Eur J Cell Biol. 2011;90:108-114
45. Brooks PC, Strömblad S, Sanders LC, et al. Localization of matrix metalloproteinase MMP-2 to the surface of invasive cells by interaction with integrin alpha v beta 3. Cell. 1996;85: 683-693
46. Deryugina EI, Bourdon MA, Luo GX, Reisfeld RA, Strongin A. Matrix metalloproteinase-2 activation modulates glioma cell migration. J Cell Sci. 1997;110(pt 19):2473-2482
47. Mitra A, Chakrabarti J, Chatterjee A. Binding of alpha5 monoclonal antibody to cell surface alpha5beta1 integrin modulates MMP-2 and MMP-7 activity in B16F10 melanoma cells. J Environ Pathol Toxicol Oncol. 2003;22:167-178
48. Ogier C, Bernard A, Chollet AM, et al. Matrix metalloproteinase-2 (MMP-2) regulates astrocyte motility in connection with the actin cytoskeleton and integrins. Glia. 2006;54:272-284
49. Mitra SK, Hanson DA, Schlaepfer DD. Focal adhesion kinase: in command and control of cell motility. Nat Rev Mol Cell Biol. 2005;6:56-68
50. LeRoith D, Werner H, Beitner-Johnson D, Roberts CT Jr. Molecular and cellular aspects of the insulin-like growth factorí receptor. Endocr Rev. 1995;16:143-163
51. Lehman JA, Gomez-Cambronero J. Molecular crosstalk between p70S6k and MAPK cell signaling pathways. Biochem Biophys Res Commun. 2002;293:463-469
52. Moelling K, Schad K, Bosse M, Zimmermann S, Schweneker M. Regulation of Raf-Akt cross-talk. J Biol Chem. 2002;277: 31099-31106
53. Zimmermann S, Moelling K. Phosphorylation and regulation of Raf by Akt (protein kinase B). Science. 1999;286:1741-1744
54. Risinger GM Jr., Hunt TS, Updike DL, Bullen EC, Howard EW. Matrix metalloproteinase-2 expression by vascular smooth muscle cells is mediated by both stimulatory and inhibitory signals in response to growth factors. J Biol Chem. 2006;281: 25915-25925
55. Stawowy P, Kallisch H, Kilimnik A, et al. Proprotein convertases regulate insulin-like growth factor 1-induced membrane-type 1 matrix metalloproteinase in VSMCs via endoproteolytic activation of the insulin-like growth factor-1 receptor. Biochem Biophys Res Commun. 2004;321:31-538
56. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 2006;66:3034-3043
57. Bravo-Cordero JJ, Marrero-Diaz R, Megías D, et al. MT1-MMP proinvasive activity is regulated by a novel Rab8-dependent exocytic pathway. EMBO J. 2007;26:1499-1510
58. Galardy RE, Cassabonne ME, Giese C, et al. Low molecular weight inhibitors in corneal ulceration. Ann N Y Acad Sci. 1994;732:315-323
59. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol. 2001;17: 463-516
60. Huttenlocher A, Horwitz, AR. Integrins in cell migration. Cold Spring Harb Perspect Biol. 2011;3:a005074
61. Wozniak MA, Modzelewska K, Kwong L, Keely PJ. Focal adhesion regulation of cell behavior. Biochim Biophys Acta. 2004;1692:103-119
62. Gleeson LM, Chakraborty C, McKinnon T, Lala PK. Insulin-like growth factor-binding protein 1 stimulates human trophoblast migration by signaling through alpha 5 beta 1 integrin via mitogen-activated protein Kinase pathway. J Clin Endocrinol Metab. 2001;86:2484-2493
63. Webb DJ, Parsons JT, Horwitz AF. Adhesion assembly, disassembly and turnover in migrating cells-over and over and over again. Nat Cell Biol. 2002;4:E97-E100
64. Ridley AJ, Schwartz MA, Burridge K, et al. Cell migration: integrating signals from front to back. Science. 2003;302: 1704-1709
65. Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol. 2010;188:11-19
66. Moreno-Layseca P, Streuli CH. Signalling pathways linking integrins with cell cycle progression. Matrix Biol. 2014;34: 144-153
67. Madamanchi A, Capozzi M, Geng L, et al. Mitigation of oxygen- induced retinopathy in alpha2beta1 integrin-deficient mice. Invest Ophthalmol Vis Sci. 2014;55:4338-4347
68. Park SW, Yun JH, Kim JH, Kim KW, Cho CH, Kim JH. Angiopoietin 2 induces pericyte apoptosis via alpha3beta1 integrin signaling in diabetic retinopathy. Diabetes. 2014;63: 3057-3068
69. Gueye Y, Ferhat L, Sbai O, et al. Trafficking and secretion of matrix metalloproteinase-2 in olfactory ensheathing glial cells: A role in cell migration? Glia. 2011;59:750-770
70. Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:283-290
71. Barber AJ, Gardner TW, Abcouwer SF. The significance of vascular and neural apoptosis to the pathology of diabetic retinopathy. Invest Ophthalmol Vis Sci. 2011;52:1156-1163
72. Sennlaub F, Courtois Y, Goureau O. Inducible nitric oxide synthase mediates retinal apoptosis in ischemic proliferative retinopathy. J Neurosci. 2002;22:3987-3993
73. Romo P, Madigan MC, Provis JM, Cullen KM. Differential effects of TGF-beta and FGF-2 on in vitro proliferation and migration of primate retinal endothelial and Müller cells. Acta Ophthalmol. 2011;89:e263-e268
74. Bull ND, Limb GA, Martin KR. Human Müller stem cell (MIO- M1) transplantation in a rat model of glaucoma: survival, differentiation, and integration. Invest Ophthalmol Vis Sci. 2008;49:3449-3456
75. Lawrence JM, Singhal S, Bhatia B, et al. MIO-M1 cells and similar Müllerglial cell lines derived from adult human retina exhibit neural stem cell characteristics. Stem Cells. 2007;25: 2033-2043
76. Tackenberg MA, Tucker BA, Swift JS, et al. Müller cell activation, proliferation and migration following laser injury. Mol Vis. 2009;15:1886-1896