Connective tissue growth factor regulates retinal neovascularization through p53 protein-dependent transactivation of the matrix metalloproteinase (MMP)-2 gene

Journal of Biological Chemistry

Volumn 287, Issue 48, 2012, Pages 40570-40585

  Chintala, Hembindu ^a   Liu, Haibo ^a   Parmar, Rahul ^a   Kamalska, Monika ^a   Kim, Yoon Ji ^a   Lovett, David ^c   Grant, Maria B ^d   Chaqour, Brahim ^a,b  

^a State University of New York Health Science Center   (United States)

^b Downstate Health Sciences University   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; BINDING SEQUENCE; CONNECTIVE TISSUE GROWTH FACTOR; CULTURED CELL; ECTOPIC EXPRESSIONS; MATRICELLULAR PROTEIN; MATRIX METALLOPROTEINASES; MATRIX PROTEINS; NEOVASCULARIZATION; PATHOLOGICAL CHANGES; RETINAL VASCULATURE; SIGNALING NETWORKS; TRANSACTIVATION; VASCULAR PATTERNS; VASCULAR REMODELING;

COLLAGEN; ENDOTHELIAL CELLS; EYE PROTECTION; GENES; GENETIC ENGINEERING; MAMMALS; MUSCULOSKELETAL SYSTEM; OPHTHALMOLOGY; OXYGEN; SIGNALING; TRANSCRIPTION FACTORS;

DIGITAL STORAGE;

CONNECTIVE TISSUE GROWTH FACTOR; GELATINASE A; OXYGEN; PROTEIN P53;

AMINO ACID SEQUENCE; ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL INJURY; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; CTGF GENE; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; GENE FUNCTION; GENE LOCATION; GENE TARGETING; GENETIC ASSOCIATION; GENETIC CONSERVATION; MATRIX METALLOPROTEINASE 2 GENE; MOUSE; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; RETINA ISCHEMIA; RETINA NEOVASCULARIZATION; TRANSACTIVATION; TUMOR SUPPRESSOR GENE; VASCULAR DISEASE;

ANIMALS; CONNECTIVE TISSUE GROWTH FACTOR; HUMANS; HYPEROXIA; MATRIX METALLOPROTEINASE 2; MICE; MICE, INBRED C57BL; RETINA; RETINAL NEOVASCULARIZATION; TRANSCRIPTIONAL ACTIVATION; TUMOR SUPPRESSOR PROTEIN P53;

LENTIVIRUS; MURINAE; MUS;

EID: 84870044156     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.386565     Document Type: Article

References (69)

1. Fleck, B. W., and McIntosh, N. (2008) Pathogenesis of retinopathy of prematurity and possible preventive strategies. Early Hum. Dev. 84, 83-88
2. Kalka, C., Asahara, T., Krone, W., and Isner, J. M. (2000) Angiogenesis and vasculogenesis. Therapeutic strategies for stimulation of postnatal neovascularization. Herz 25, 611-622
3. Quinn, G. E., Gilbert, C., Darlow, B. A., and Zin, A. (2010) Retinopathy of prematurity: an epidemic in the making. Chin. Med. J. 123, 2929-2937
4. Sapieha, P., Joyal, J. S., Rivera, J. C., Kermorvant-Duchemin, E., Sennlaub, F., Hardy, P., Lachapelle, P., and Chemtob, S. (2010) Retinopathy of prematurity. Understanding ischemic retinal vasculopathies at an extreme of life. J. Clin. Invest. 120, 3022-3032
5. Li Calzi, S., Neu, M. B., Shaw, L. C., Kielczewski, J. L., Moldovan, N. I., and Grant, M. B. (2010) EPCs and pathological angiogenesis. When good cells go bad. Microvasc. Res. 79, 207-216
6. McVicar, C. M., Colhoun, L. M., Abrahams, J. L., Kitson, C. L., Hamilton, R., Medina, R. J., Durga, D., Gardiner, T. A., Rudd, P. M., and Stitt, A. W. (2010) Differential modulation of angiogenesis by erythropoiesis-stimulating agents in a mouse model of ischaemic retinopathy. PLoS. One 5, e11870
7. Chen, C. C., and Lau, L. F. (2009) Functions and mechanisms of action of CCN matricellular proteins. Int. J. Biochem. Cell Biol. 41, 771-783
8. Liu, H., Yang, R., Tinner, B., Choudhry, A., Schutze, N., and Chaqour, B. (2008) Cysteine-rich protein 61 and connective tissue growth factor induce deadhesion and anoikis of retinal pericytes. Endocrinology 149, 1666-1677 (Pubitemid 351468326)
9. Chaqour, B., Yang, R., and Sha, Q. (2006) Mechanical stretch modulates the promoter activity of the profibrotic factor CCN2 through increased actin polymerization and NF-κB activation. J. Biol. Chem. 281, 20608-20622 (Pubitemid 44065832)
10. Hanna, M., Liu, H., Amir, J., Sun, Y., Morris, S. W., Siddiqui, M. A., Lau, L. F., and Chaqour, B. (2009) Mechanical regulation of the proangiogenic factor CCN1/CYR61 gene requires the combined activities of MRTF-A and CREB-binding protein histone acetyltransferase. J. Biol. Chem. 284, 23125-23136
11. Kireeva, M. L., Latinkić, B. V., Kolesnikova, T. V., Chen, C. C., Yang, G. P., Abler, A. S., and Lau, L. F. (1997) Cyr61 and Fisp12 are both ECM-associated signaling molecules. Activities, metabolism, and localization during development. Exp. Cell Res. 233, 63-77 (Pubitemid 27229982)
12. Kunz, M., Moeller, S., Koczan, D., Lorenz, P., Wenger, R. H., Glocker, M. O., Thiesen, H. J., Gross, G., and Ibrahim, S. M. (2003) Mechanisms of hypoxic gene regulation of angiogenesis factor Cyr61 in melanoma cells. J. Biol. Chem. 278, 45651-45660 (Pubitemid 37432707)
13. Twigg, S. M., Chen, M. M., Joly, A. H., Chakrapani, S. D., Tsubaki, J., Kim, H. S., Oh, Y., and Rosenfeld, R. G. (2001) Advanced glycosylation end products up-regulate connective tissue growth factor (insulin-like growth factor-binding protein-related protein 2) in human fibroblasts: a potential mechanism for expansion of extracellular matrix in diabetes mellitus. Endocrinology 142, 1760-1769 (Pubitemid 32405931)
14. Abreu, J. G., Ketpura, N. I., Reversade, B., and De Robertis, E. M. (2002) Connective-tissue growth factor (CTGF) modulates cell signaling byBMP and TGF-β. Nat. Cell Biol. 4, 599-604
15. Chen, C. C., Mo, F. E., and Lau, L. F. (2001) The angiogenic factor Cyr61 activates a genetic program for wound healing in human skin fibroblasts. J. Biol. Chem. 276, 47329-47337
16. Chen, C. C., and Lau, L. F. (2010) Deadly liaisons: fatal attraction between CCN matricellular proteins and the tumor necrosis factor family of cytokines. J Cell Commun. Signal. 4, 63-69
17. Chintalapudi, M. R., Markiewicz, M., Kose, N., Dammai, V., Champion, K. J., Hoda, R. S., Trojanowska, M., and Hsu, T. (2008) Cyr61/CCN1 and CTGF/CCN2 mediate the proangiogenic activity of VHL-mutant renal carcinoma cells. Carcinogenesis 29, 696-703 (Pubitemid 351494156)
18. Crean, J. K., Furlong, F., Mitchell, D., McArdle, E., Godson, C., and Martin, F. (2006) Connective tissue growth factor/CCN2 stimulates actin disassembly through Akt/protein kinase B-mediated phosphorylation and cytoplasmic translocation of p27(Kip-1). FASEB J. 20, 1712-1714
19. Hasan, A., Pokeza, N., Shaw, L., Lee, H. S., Lazzaro, D., Chintala, H., Rosenbaum, D., Grant, M. B., and Chaqour, B. (2011) The matricellular protein cysteine-rich protein 61 (CCN1/Cyr61) enhances physiological adaptation of retinal vessels and reduces pathological neovascularization associated with ischemic retinopathy. J. Biol. Chem. 286, 9542-9554
20. Katsube, K., Sakamoto, K., Tamamura, Y., and Yamaguchi, A. (2009) Role of CCN, a vertebrate-specific gene family, in development. Dev. Growth Differ. 51, 55-67
21. Kubota, S., and Takigawa, M. (2007) CCN family proteins and angiogenesis. From embryo to adulthood. Angiogenesis 10, 1-11 (Pubitemid 46356220)
22. Leask, A., Parapuram, S. K., Shi-Wen, X., and Abraham, D. J. (2009) Connective tissue growth factor (CTGF, CCN2) gene regulation: a potent clinical bio-marker of fibroproliferative disease? J. Cell Commun. Signal. 3, 89-94
23. Arnott, J. A., Lambi, A. G., Mundy, C., Hendesi, H., Pixley, R. A., Owen, T. A., Safadi, F. F., and Popoff, S. N. (2011) The role of connective tissue growth factor (CTGF/CCN2) in skeletogenesis. Crit. Rev. Eukaryot. Gene Expr. 21, 43-69
24. Ivkovic, S., Yoon, B. S., Popoff, S. N., Safadi, F. F., Libuda, D. E., Stephenson, R. C., Daluiski, A., and Lyons, K. M. (2003) Connective tissue growth factor coordinates chondrogenesis and angiogenesis during skeletal development. Development 130, 2779-2791 (Pubitemid 37069592)
25. Doherty, H. E., Kim, H. S., Hiller, S., Sulik, K. K., and Maeda, N. (2010) A mouse strain where basal connective tissue growth factor gene expression can be switched from low to high. PLoS ONE 5, e12909
26. Babic, A. M., Chen, C. C., and Lau, L. F. (1999) Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin αvβ3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol. Cell. Biol. 19, 2958-2966 (Pubitemid 29144541)
27. Kuiper, E. J., Roestenberg, P., Ehlken, C., Lambert, V., van Treslong-de Groot, H. B., Lyons, K. M., Agostini, H. J., Rakic, J. M., Klaassen, I., Van Noorden, C. J., Goldschmeding, R., and Schlingemann, R. O. (2007) Angiogenesis is not impaired in connective tissue growth factor (CTGF) knock-out mice. J. Histochem. Cytochem. 55, 1139-1147 (Pubitemid 350006296)
28. Shimo, T., Nakanishi, T., Nishida, T., Asano, M., Kanyama, M., Kuboki, T., Tamatani, T., Tezuka, K., Takemura, M., Matsumura, T., and Takigawa, M. (1999) Connective tissue growth factor induces the proliferation, migration, and tube formation of vascular endothelial cells in vitro, and angiogenesis in vivo. J. Biochem. 126, 137-145 (Pubitemid 29355403)
29. Kuiper, E. J., van Zijderveld, R., Roestenberg, P., Lyons, K. M., Goldschmeding, R., Klaassen, I., Van Noorden, C. J., and Schlingemann, R. O. (2008) Connective tissue growth factor is necessary for retinal capillary basal lamina thickening in diabetic mice. J. Histochem. Cytochem. 56, 785-792 (Pubitemid 351991091)
30. Garcia Abreu, J., Coffinier, C., Larraín, J., Oelgeschläger, M., and De Robertis, E. M. (2002) Chordin-like CR domains and the regulation of evolutionarily conserved extracellular signaling systems. Gene 287, 39-47 (Pubitemid 34454797)
31. Hinton, D. R., Spee, C., He, S., Weitz, S., Usinger, W., LaBree, L., Oliver, N., and Lim, J. I. (2004) Accumulation of NH2-terminal fragment of connective tissue growth factor in the vitreous of patients with proliferative diabetic retinopathy. Diabetes Care 27, 758-764 (Pubitemid 38280546)
32. Grotendorst, G. R., and Duncan, M. R. (2005) Individual domains of connective tissue growth factor regulate fibroblast proliferation and myofibroblast differentiation. FASEB J. 19, 729-738 (Pubitemid 40617377)
33. Yoon, P. O., Lee, M. A., Cha, H., Jeong, M. H., Kim, J., Jang, S. P., Choi, B. Y., Jeong, D., Yang, D. K., Hajjar, R. J., and Park, W. J. (2010) The opposing effects of CCN2 and CCN5 on the development of cardiac hypertrophy and fibrosis. J. Mol. Cell. Cardiol. 49, 294-303
34. Smith, L. E., Wesolowski, E., McLellan, A., Kostyk, S. K., D'Amato, R., Sullivan, R., and D'Amore, P. A. (1994) Oxygen-induced retinopathy in the mouse. Invest. Ophthalmol. Vis. Sci. 35, 101-111 (Pubitemid 24046832)
35. Harendza, S., Pollock, A. S., Mertens, P. R., and Lovett, D. H. (1995) Tissue- specific enhancer-promoter interactions regulate high level constitutive expression of matrix metalloproteinase 2 by glomerular mesangial cells. J. Biol. Chem. 270, 18786-18796
36. Pi, L., Xia, H., Liu, J., Shenoy, A. K., Hauswirth, W. W., and Scott, E. W. (2011) Role of connective tissue growth factor in the retinal vasculature during development and ischemia. Invest. Ophthalmol. Vis. Sci. 52, 8701-8710
37. Gauthier, R., Joly, S., Pernet, V., Lachapelle, P., and Di Polo, A. (2005) Brain-derived neurotrophic factor gene delivery to Muller glia preserves structure and function of light-damaged photoreceptors. Invest. Ophthalmol. Vis. Sci. 46, 3383-3392 (Pubitemid 44264329)
38. Kordower, J. H., Bloch, J., Ma, S. Y., Chu, Y., Palfi, S., Roitberg, B. Z., Emborg, M., Hantraye, P., Déglon, N., and Aebischer, P. (1999) Lentiviral gene transfer to the nonhuman primate brain. Exp. Neurol. 160, 1-16
39. Apte, R. S. (2010) Regulation of angiogenesis by macrophages. Adv. Exp. Med. Biol. 664, 15-19
40. Kociok, N., Radetzky, S., Krohne, T. U., Gavranic, C., and Joussen, A. M. (2006) Pathological but not physiological retinal neovascularization is altered in TNF-Rp55-receptor-deficient mice. Invest. Ophthalmol. Vis. Sci. 47, 5057-5065 (Pubitemid 46586413)
41. Weidemann, A., Krohne, T. U., Aguilar, E., Kurihara, T., Takeda, N., Dorrell, M. I., Simon, M. C., Haase, V. H., Friedlander, M., and Johnson, R. S. (2010) Astrocyte hypoxic response is essential for pathological but not developmental angiogenesis of the retina. Glia 58, 1177-1185
42. Vinores, S. A., Xiao, W. H., Shen, J., and Campochiaro, P. A. (2007) TNF-αis critical for ischemia-induced leukostasis, but not retinal neovascularization nor VEGF-induced leakage. J. Neuroimmunol. 182, 73-79 (Pubitemid 46039759)
43. Kowluru, R. A., and Kanwar, M. (2009) Oxidative stress and the development of diabetic retinopathy. Contributory role of matrix metalloproteinase-2. Free Radic. Biol. Med. 46, 1677-1685
44. Sternlicht, M. D., and Werb, Z. (2001) How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17, 463-516 (Pubitemid 33096184)
45. Tronc, F., Mallat, Z., Lehoux, S., Wassef, M., Esposito, B., and Tedgui, A. (2000) Role of matrix metalloproteinases in blood flow-induced arterial enlargement: interaction with NO. Arterioscler. Thromb. Vasc. Biol. 20, E120-E126
46. Bian, J., and Sun, Y. (1997) Transcriptional activation by p53 of the human type IV collagenase (gelatinase A or matrix metalloproteinase 2) promoter. Mol. Cell. Biol. 17, 6330-6338 (Pubitemid 27451177)
47. Di, Giovanni, S., and Rathore, K. (2012) p53-Dependent pathways in neurite outgrowth and axonal regeneration. Cell Tissue Res. 349, 87-95
48. Hall-Glenn, F., De Young, R. A., Huang, B. L., van Handel, B., Hofmann, J. J., Chen, T. T., Choi, A., Ong, J. R., Benya, P. D., Mikkola, H., Iruela- Arispe, M. L., and Lyons, K. M. (2012) CCN2/connective tissue growth factor is essential for pericyte adhesion and endothelial basement membrane formation during angiogenesis. PLoS One 7, e30562
49. Jun, J. I., and Lau, L. F. (2011) Taking aim at the extracellular matrix. CCN proteins as emerging therapeutic targets. Nat. Rev. Drug Discov. 10, 945-963
50. Sakimoto, S., Kidoya, H., Naito, H., Kamei, M., Sakaguchi, H., Goda, N., Fukamizu, A., Nishida, K., and Takakura, N. (2012) A role for endothelial cells in promoting the maturation of astrocytes through the apelin/APJ system in mice. Development 139, 1327-1335
51. Scott, A., Powner, M. B., Gandhi, P., Clarkin, C., Gutmann, D. H., Johnson, R. S., Ferrara, N., and Fruttiger, M. (2010) Astrocyte-derived vascular endothelial growth factor stabilizes vessels in the developing retinal vasculature. PLoS One 5, e11863
52. Watson, M. G., McDougall, S. R., Chaplain, M. A., Devlin, A. H., and Mitchell, C. A. (2012) Dynamics of angiogenesis during murine retinal development: a coupled in vivo and in silico study. J. R. Soc. Interface 9, 2351-2364
53. Suzuma, K., Naruse, K., Suzuma, I., Takahara, N., Ueki, K., Aiello, L. P., and King, G. L. (2000) Vascular endothelial growth factor induces expression of connective tissue growth factor via KDR, Flt1, and phosphatidylinositol 3-kinase-Akt-dependent pathways in retinal vascular cells. J. Biol. Chem. 275, 40725-40731 (Pubitemid 32054890)
54. Wunderlich, K., Senn, B. C., Todesco, L., Flammer, J., and Meyer, P. (2000) Regulation of connective tissue growth factor gene expression in retinal vascular endothelial cells by angiogenic growth factors. Graefes Arch. Clin. Exp. Ophthalmol. 238, 910-915
55. Samarin, J., Wessel, J., Cicha, I., Kroening, S., Warnecke, C., and Goppelt- Struebe, M. (2010) FoxO proteins mediate hypoxic induction of connective tissue growth factor in endothelial cells. J. Biol. Chem. 285, 4328-4336
56. He, S., Chen, Y., Khankan, R., Barron, E., Burton, R., Zhu, D., Ryan, S. J., Oliver, N., and Hinton, D. R. (2008) Connective tissue growth factor as a mediator of intraocular fibrosis. Invest. Ophthalmol. Vis. Sci. 49, 4078-4088
57. Inoki, I., Shiomi, T., Hashimoto, G., Enomoto, H., Nakamura, H., Makino, K., Ikeda, E., Takata, S., Kobayashi, K., and Okada, Y. (2002) Connective tissue growth factor binds vascular endothelial growth factor (VEGF) and inhibits VEGF-induced angiogenesis. FASEB J. 16, 219-221
58. Kuiper, E. J., Van Nieuwenhoven, F. A., de Smet, M. D., van Meurs, J. C., Tanck, M. W., Oliver, N., Klaassen, I., Van Noorden, C. J., Goldschmeding, R., and Schlingemann, R. O. (2008) The angio-fibrotic switch of VEGF and CTGF in proliferative diabetic retinopathy. PLoS ONE 3, e2675
59. Barnett, J. M., McCollum, G. W., Fowler, J. A., Duan, J. J., Kay, J. D., Liu, R. Q., Bingaman, D. P., and Penn, J. S. (2007) Pharmacologic and genetic manipulation of MMP-2 and -9 affects retinal neovascularization in rodent models of OIR. Invest. Ophthalmol. Vis. Sci. 48, 907-915 (Pubitemid 351260729)
60. Mohammad, G., and Kowluru, R. A. (2010) Matrix metalloproteinase-2 in the development of diabetic retinopathy and mitochondrial dysfunction. Lab. Invest. 90, 1365-1372
61. Suofu, Y., Clark, J. F., Broderick, J. P., Kurosawa, Y., Wagner, K. R., and Lu, A. (2012) Matrix metalloproteinase-2 or -9 deletions protect against hemorrhagic transformation during early stage of cerebral ischemia and reperfusion. Neuroscience 212, 180-189
62. Bergers, G., and Coussens, L. M. (2000) Extrinsic regulators of epithelial tumor progression. Metalloproteinases. Curr. Opin. Genet. Dev. 10, 120-127 (Pubitemid 30113715)
63. Chang, K. H., Chan-Ling, T., McFarland, E. L., Afzal, A., Pan, H., Baxter, L. C., Shaw, L. C., Caballero, S., Sengupta, N., Li Calzi, S., Sullivan, S. M., and Grant, M. B. (2007) IGF binding protein-3 regulates hematopoietic stem cell and endothelial precursor cell function during vascular development. Proc. Natl. Acad. Sci. U.S.A. 104, 10595-10600 (Pubitemid 47185710)
64. Ishida, S., Yamashiro, K., Usui, T., Kaji, Y., Ogura, Y., Hida, T., Honda, Y., Oguchi, Y., and Adamis, A. P. (2003) Leukocytes mediate retinal vascular remodeling during development and vaso-obliteration in disease. Nat. Med. 9, 781-788 (Pubitemid 36749230)
65. Dean, R. A., Butler, G. S., Hamma-Kourbali, Y., Delbé, J., Brigstock, D. R., Courty, J., and Overall, C. M. (2007) Identification of candidate angiogenic inhibitors processed by matrix metalloproteinase 2 (MMP-2) in cell-based proteomic screens: disruption of vascular endothelial growth factor (VEGF)/heparin affin regulatory peptide (pleiotrophin) and VEGF/connective tissue growth factor angiogenic inhibitory complexes by MMP-2 proteolysis. Mol. Cell. Biol. 27, 8454-8465
66. Bergman, M. R., Cheng, S., Honbo, N., Piacentini, L., Karliner, J. S., and Lovett, D. H. (2003) A functional activating protein 1 (AP-1) site regulates matrix metalloproteinase 2 (MMP-2) transcription by cardiac cells through interactions with JunB-Fra1 and JunB-FosB heterodimers. Biochem. J. 369, 485-496 (Pubitemid 36246232)
67. Lee, J. G., Dahi, S., Mahimkar, R., Tulloch, N. L., Alfonso-Jaume, M. A., Lovett, D. H., and Sarkar, R. (2005) Intronic regulation of matrix metalloproteinase- 2 revealed by in vivo transcriptional analysis in ischemia. Proc. Natl. Acad. Sci. U.S.A. 102, 16345-16350 (Pubitemid 41688916)
68. Yu, J., Zhang, L., Hwang, P. M., Rago, C., Kinzler, K. W., and Vogelstein, B. (1999) Identification and classification of p53-regulated genes. Proc. Natl. Acad. Sci. U.S.A. 96, 14517-14522 (Pubitemid 30000682)
69. Lee, T., Esemuede, N., Sumpio, B. E., and Gahtan, V. (2003) Thrombospondin- 1 induces matrix metalloproteinase-2 activation in vascular smooth muscle cells. J. Vasc. Surg. 38, 147-154 (Pubitemid 41123302)