Pigment epithelium-derived factor is a substrate for matrix metalloproteinase type 2 and type 9: Implications for downregulation in hypoxia

Investigative Ophthalmology and Visual Science

Volumn 46, Issue 8, 2005, Pages 2736-2747

  Notari, Luigi ^a   Miller, Amanda ^a   Martínez, Alfredo ^b,d   Amaral, Juan ^a   Ju, Meihua ^c   Robinson, Gregory ^c   Smith, Lois E H ^c   Becerra, S Patricia ^a  

^a NATIONAL EYE INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c BOSTON CHILDREN S HOSPITAL   (United States)

^d INSTITUTO CAJAL   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GELATINASE A; GELATINASE B; MESSENGER RNA; PIGMENT EPITHELIUM DERIVED FACTOR; RECOMBINANT PROTEIN; VASCULOTROPIN; EYE PROTEIN; NERVE GROWTH FACTOR; OXYGEN; PIGMENT EPITHELIUM-DERIVED FACTOR; SERINE PROTEINASE INHIBITOR; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HYPOXIA; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PIGMENT EPITHELIUM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN INDUCTION; RETROLENTAL FIBROPLASIA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ZYMOGRAPHY; ANIMAL; ANOXIA; C57BL MOUSE; CELL CULTURE; CHICK EMBRYO; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; ENZYMOLOGY; GENETICS; HAMSTER; HUMAN; MACACA; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); NEWBORN; WESTERN BLOTTING;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; BLOTTING, WESTERN; CELLS, CULTURED; CHICK EMBRYO; CRICETINAE; DISEASE MODELS, ANIMAL; DOWN-REGULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EYE PROTEINS; HUMANS; INFANT, NEWBORN; MACACA; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; MICE; MICE, INBRED C57BL; NEOVASCULARIZATION, PATHOLOGIC; NERVE GROWTH FACTORS; OXYGEN; PIGMENT EPITHELIUM OF EYE; RETINOPATHY OF PREMATURITY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERPINS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 24644506292     PISSN: 01460404     EISSN: None     Source Type: Journal    
DOI: 10.1167/iovs.04-1489     Document Type: Article

References (78)

1. Bouck N. PEDF: anti-angiogenic guardian of ocular function. Trends Mol Med. 2002;8:330-334.
2. Tombran-Tink J, Barnstable CJ. PEDF. a multifaceted neurotrophic factor. Nat Rev Neurosci. 2003;4:628-636.
3. King GL, Suzuma K. Pigment-epithelium-derived factor: a key coordinator of retinal neuronal and vascular functions. N Engl J Med. 2000;342:349-351.
4. Becerra SP, Fariss RN, Wu YQ, et al. Pigment epithelium-derived factor in the monkey retinal pigment epithelium and interphotoreceptor matrix: apical secretion and distribution. Exp Eye Res. 2004;78:223-234.
5. Perez-Mediavilla LA, Chew C, Campochiaro PA, et al. Sequence and expression analysis of bovine pigment epithelium-derived factor. Biochim Biophys Acta. 1998;1398:203-214.
6. Tombran-Tink J, Shivaram SM, Chader GJ, et al. Expression, secretion, and age-related downregulation of pigment epithelium-derived factor, a serpin with neurotrophic activity. J Neurosci. 1995; 15:4992-5003.
7. Yasui N, Mori T, Morito D, et al. Dual-site recognition of different extracellular matrix components by anti-angiogenic/neurotrophic serpin, PEDF. Biochemistry. 2003;42:3160-3167.
8. Meyer C, Notari L, Becerra SP. Mapping the type I collagen-binding site on pigment epithelium-derived factor. Implications for its antiangiogenic activity. J Biol Chem. 2002;277:45400-45407.
9. Alberdi E, Hyde CC, Becerra SP. Pigment epithelium-derived factor (PEDF) binds to glycosaminoglycans: analysis of the binding site. Biochemistry. 1998;37:10643-10652.
10. Cao W, Tombran-Tink J, Chen W, et al. Pigment epithelium-derived factor protects cultured retinal neurons against hydrogen peroxide-induced cell death. J Neurosci Res. 1999;57:789-800.
11. Mori K, Duh E, Gehlbach P, et al. Pigment epithelium-derived factor inhibits retinal and choroidal neovascularization. J Cell Physiol. 2001;188:253-263.
12. Stellmach V, Crawford SE, Zhou W, et al. Prevention of ischemia-induced retinopathy by the natural ocular antiangiogenic agent pigment epithelium-derived factor. Proc Natl Acad Sci USA. 2001; 98:2593-2597.
13. Takita H, Yoneya S, Gehlbach PL, et al. Retinal neuroprotection against ischemic injury mediated by intraocular gene transfer of pigment epithelium-derived factor. Invest Ophthalmol Vis Sci. 2003;44:4497-4504.
14. Wang L, Schmitz V, Perez-Mediavilla A, et al. Suppression of angiogenesis and tumor growth by adenoviral-mediated gene transfer of pigment epithelium-derived factor. Mol Ther. 2003;8:72-79.
15. Dawson DW, Volpert OV, Gillis P, et al. Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science. 1999; 285:245-248.
16. Gao G, Li Y, Fant J, et al. Difference in ischemic regulation of vascular endothelial growth factor and pigment epithelium-derived factor in brown Norway and Sprague Dawley rats contributing to different susceptibilities to retinal neovascularization. Diabetes. 2002;51:1218-1225.
17. Renno RZ, Youssri AI, Michaud N, et al. Expression of pigment epithelium-derived factor in experimental choroidal neovascularization. Invest Ophthalmol Vis Sci. 2002;43:1574-1580.
18. Spranger J, Osterhoff M, Reimann M, et al. Loss of the antiangiogenic pigment epithelium-derived factor in patients with angiogenic eye disease. Diabetes. 2001;50:2641-2645.
19. Becerra SP. Structure-function studies on PEDF: a noninhibitory serpin with neurotrophic activity. Adv Exp Med Biol. 1997;425:223-237.
20. Gettins PG, Simonovic M, Volz K. Pigment epithelium-derived factor (PEDF), a serpin with potent anti-angiogenic and neurite outgrowth-promoting properties. Biol Chem. 2002;383:1677-1682.
21. Simonovic M, Gettins PG, Volz K. Crystal structure of human PEDF, a potent anti-angiogenic and neurite growth-promoting factor. Proc Natl Acad Sci USA. 2001;98:11131-11135.
22. Becerra SP, Sagasti A, Spinella P, et al. Pigment epithelium-derived factor behaves like a noninhibitory serpin: neurotrophic activity does not require the serpin reactive loop. J Biol Chem. 1995;270:25992-25999.
23. Das A, McGuire PG. Retinal and choroidal angiogenesis: pathophysiology and strategies for inhibition. Prog Retin Eye Res. 2003; 22:721-748.
24. Noda K, Ishida S, Inoue M, et al. Production and activation of matrix metalloproteinase-2 in proliferative diabetic retinopathy. Invest Ophthalmol Vis Sci. 2003;44:2163-2170.
25. Plantner JJ, Jiang C, Smine A. Increase in interphotoreceptor matrix gelatinase A (MMP-2) associated with age-related macular degeneration. Exp Eye Res. 1998;67:637-645.
26. Bergers G, Brekken R, McMahon G, et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol. 2000;2:737-744.
27. Lambert V, Wielockx B, Munaut C, et al. MMP-2 and MMP-9 synergize in promoting choroidal neovascularization. FASEB J. 2003;17:2290-2292.
28. Chintala SK, Zhang X, Austin JS, et al. Deficiency in matrix metalloproteinase gelatinase B (MMP-9) protects against retinal ganglion cell death after optic nerve ligation. Biol Chem. 2002;277:47461-47468.
29. Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol. 2002;3:207-214.
30. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol. 2001;17:463-516.
31. McCawley LJ, Matrisian LM. Matrix metalloproteinases: they're not just for matrix anymore! Curr Opin Cell Biol. 2001;13:534-540.
32. Semenza GL. HIF-1: using two hands to flip the angiogenic switch. Cancer Metastasis Rev. 2000;19:59-65.
33. Semenza GL. Angiogenesis in ischemic and neoplastic disorders. Annu Rev Med. 2003;54:17-28.
34. Wary KK, Thakker GD, Humtsoe JO, et al. Analysis of VEGF-responsive genes involved in the activation of endothelial cells. Mol Cancer. 2003;2:25.
35. Lamoreaux WJ, Fitzgerald ME, Reiner A, et al. Vascular endothelial growth factor increases release of gelatinase A and decreases release of tissue inhibitor of metalloproteinases by microvascular endothelial cells in vitro. Microvasc Res. 1998;55:29-42.
36. Burbridge MF, Coge F, Galizzi JP, et al. The role of the matrix metalloproteinases during in vitro vessel formation. Angiogenesis. 2002;5:215-226.
37. Ohno-Matsui K, Morita I, Tombran-Tink J, et al. Novel mechanism for age-related macular degeneration: an equilibrium shift between the angiogenesis factors VEGF and PEDF. J Cell Physiol. 2001;189:323-333.
38. Ogata N, Nishikawa M, Nishimura T, et al. Unbalanced vitreous levels of pigment epithelium-derived factor and vascular endothelial growth factor in diabetic retinopathy. Am J Ophthalmol. 2002; 134:348-353.
39. Hanahan D, Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell. 1996;86:353-364.
40. Stratikos E, Alberdi E, Gettins PG, et al. Recombinant human pigment epithelium-derived factor (PEDF): characterization of PEDF overexpressed and secreted by eukaryotic cells. Protein Sci. 1996;5:2575-2582.
41. Zhang JW, Gottschall PE. Zymographic measurement of gelatinase activity in brain tissue after detergent extraction and affinity-support purification. J Neurosci Methods. 1997;76:15-20.
42. Smith LE, Wesolowski E, McLellan A, et al. Oxygen-induced retinopathy in the mouse. Invest Ophthalmol Vis Sci. 1994;35:101-111.
43. Garayoa M, Martinez A, Lee S, et al. Hypoxia-inducible factor-1 (HIF-1) up-regulates adrenomedullin expression in human tumor cell lines during oxygen deprivation: a possible promotion mechanism of carcinogenesis. Mol Endocrinol. 2000;14:848-862.
44. Wu YQ, Becerra SP. Proteolytic activity directed toward pigment epithelium-derived factor in vitreous of bovine eyes: implications of proteolytic processing. Invest Ophthalmol Vis Sci. 1996;37:1984-1993.
45. Plantner JJ, Smine A, Quinn TA. Matrix metalloproteinases and metalloproteinase inhibitors in human interphotoreceptor matrix and vitreous. Curr Eye Res. 1998;17:132-140.
46. Wu YQ, Notario V, Chader GJ, et al. Identification of pigment epithelium-derived factor in the interphotoreceptor matrix of bovine eyes. Protein Expr Purif. 1995;6:447-456.
47. Barber AJ, Nakamura M, Wolpert EB, et al. Insulin rescues retinal neurons from apoptosis by a phosphatidylinositol 3-kinase/Akt-mediated mechanism that reduces the activation of caspase-3. J Biol Chem. 2001;276:32814-32821.
48. Martinez A, Zudaire E, Portal-Nunez S, et al. Proadrenomedullin NH2-terminal 20 peptide is a potent angiogenic factor, and its inhibition results in reduction of tumor growth. Cancer Res. 2004; 64:6489-6494.
49. Martinez A, Vos M, Guedez L, et al. The effects of adrenomedullin overexpression in breast tumor cells. J Natl Cancer Inst. 2002;94:1226-1237.
50. Holekamp NM, Bouck N, Volpert O. Pigment epithelium-derived factor is deficient in the vitreous of patients with choroidal neovascularization due to age-related macular degeneration. Am J Ophthalmol. 2002;134:220-227.
51. Singh VK, Chader GJ, Rodriguez IR. Structural and comparative analysis of the mouse gene for pigment epithelium-derived factor (PEDF). Mol Vis. 1998;4:7.
52. Lynch CC, Matrisian LM. Matrix metalloproteinases in tumor-host cell communication. Differentiation. 2002;70:561-573.
53. Sivak JM, Fini ME. MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology. Prog Retin Eye Res. 2002; 21:1-14.
54. Liu Z, Zhou X, Shapiro SD, et al. The serpin alpha1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell. 2000;102:647-655.
55. Mast AE, Enghild JJ, Nagase H, et al. Kinetics and physiologic relevance of the inactivation of alpha 1-proteinase inhibitor, alpha 1-antichymotrypsin, and antithrombin III by matrix metalloproteinases-1 (tissue collagenase), -2 (72-kDa gelatinase/type IV collagenase), and -3 (stromelysin). J Biol Chem. 1991;266:15810-15816.
56. Apte RS, Barreiro RA, Duh E, et al. Stimulation of neovascularization by the anti-angiogenic factor PEDF. Invest Ophthalmol Vis Sci. 2004;45:4491-4497.
57. Brockington A, Lewis C, Wharton S, et al. Vascular endothelial growth factor and the nervous system. Neuropathol Appl Neurobiol. 2004;30:427-446.
58. Carmeliet P, Storkebaum E. Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders. Semin Cell Dev Biol. 2002;13:39-53.
59. Yourey PA, Gohari S, Su JL, et al. Vascular endothelial cell growth factors promote the in vitro development of rat photoreceptor cells. J Neurosci. 2000;20:6781-6788.
60. Duh EJ, Yang HS, Haller JA, et al. Vitreous levels of pigment epithelium-derived factor and vascular endothelial growth factor: implications for ocular angiogenesis. Am J Ophthalmol. 2004;137:668-674.
61. Ogata N, Tombran-Tink J, Nishikawa M, et al. Pigment epithelium-derived factor in the vitreous is low in diabetic retinopathy and high in rhegmatogenous retinal detachment. Am J Ophthalmol. 2001;132:378-382.
62. Cayouette M, Smith SB, Becerra SP, et al. Pigment epithelium-derived factor delays the death of photoreceptors in mouse models of inherited retinal degenerations. Neurobiol Dis. 1999;6:523-532.
63. Pierce EA, Foley ED, Smith LE. Regulation of vascular endothelial growth factor by oxygen in a model of retinopathy of prematurity. Arch Ophthalmol. 1996;114:1219-1228.
64. Smith LE. Pathogenesis of retinopathy of prematurity. Growth Horm IGF Res. 2004;14(suppl A):S140-S144.
65. Miyamoto N, Mandai M, Takagi H, et al. Contrasting effect of estrogen on VEGF induction under different oxygen status and its role in murine ROP. Invest Ophthalmol Vis Sci. 2002;43:2007-2014.
66. Das A, McLamore A, Song W, et al. Retinal neovascularization is suppressed with a matrix metalloproteinase inhibitor. Arch Ophthalmol. 1999;117:498-503.
67. Majka S, McGuire P, Colombo S, et al. The balance between proteinases and inhibitors in a murine model of proliferative retinopathy. Invest Ophthalmol Vis Sci. 2001;42:210-215.
68. Zhang X, Sakamoto T, Hata Y, et al. Expression of matrix metalloproteinases and their inhibitors in experimental retinal ischemia-reperfusion injury in rats. Exp Eye Res. 2002;74:577-584.
69. Wangsa-Wirawan ND, Linsenmeier RA. Retinal oxygen: fundamental and clinical aspects. Arch Ophthalmol. 2003;121:547-557.
70. Osborne NN, Melena J, Chidlow G, et al. A hypothesis to explain ganglion cell death caused by vascular insults at the optic nerve head: possible implication for the treatment of glaucoma. Br J Ophthalmol. 2001;85:1252-1259.
71. Kaushik S, Pandav SS, Ram J. Neuroprotection in glaucoma. J Postgrad Med. 2003;49:90-95.
72. Heissig B, Hattori K, Friedrich M, et al. Angiogenesis: vascular remodeling of the extracellular matrix involves metalloproteinases. Curr Opin Hematol. 2003;10:136-141.
73. Siao CJ, Tsirka SE. Extracellular proteases and neuronal cell death. Cell Mol Biol (Noisy-le-grand). 2002;48:151-161.
74. Aiello LP, Pierce EA, Foley ED, et al. Suppression of retinal neovascularization in vivo by inhibition of vascular endothelial growth factor (VEGF) using soluble VEGF-receptor chimeric proteins. Proc Natl Acad Sci USA. 1995;92:10457-10461.
75. Jones BE, Moshyedi P, Gallo S, et al. Characterization and novel activation of 72-kDa metalloproteinase in retinal interphotoreceptor matrix and Y-79 cell culture medium. Exp Eye Res. 1994;59:257-269.
76. Holz FG and Miller DW. Pharmacological therapy for age-related macular degeneration: current developments and perspectives [in German]. Ophthalmologe. 2003;100:97-103.
77. Ohno-Matsui K, Uetama T, Yoshida T, et al. Reduced retinal angiogenesis in MMP-2-deficient mice. Invest Ophthalmol Vis Sci. 2003; 44:5370-5375.
78. Maslim J, Valter K, Egensperger R, et al. Tissue oxygen during a critical developmental period controls the death and survival of photoreceptors. Invest Ophthalmol Vis Sci. 1997;38:1667-1677.