Low-density lipoprotein receptor-related protein-1 (LRP-1) expression in a rat model of oxygen-induced retinal neovascularization

Experimental Eye Research

Volumn 83, Issue 6, 2006, Pages 1378-1385

  Sánchez, María C ^a   Barcelona, Pablo F ^a   Luna, Jose D ^b   Ortiz, Susana G ^a   Juarez, Patricio C ^b   Riera, Clelia M ^a   Chiabrando, Gustavo A ^a  

^a UNIVERSIDAD NACIONAL DE CÓRDOBA   (Argentina)

^b Fundacion VER   (Argentina)

Author keywords

2 macroglobulin; cell proliferation; hypoxia; LDL receptors; metalloproteinases; oxygen induced retinal neovascularization; retina

Indexed keywords

ALPHA 2 MACROGLOBULIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 1; METALLOPROTEINASE; OXYGEN; UNCLASSIFIED DRUG;

AMBIENT AIR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATMOSPHERE; BIRTH; CELL MEMBRANE; CONTROLLED STUDY; DISEASE MODEL; ENZYME ACTIVITY; EXPOSURE; HYPOTHESIS; HYPOXIA; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INCUBATOR; MUELLER CELL; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; RAT; RAT STRAIN; RETINA; RETINA CELL; RETINA NEOVASCULARIZATION; WESTERN BLOTTING; ZYMOGRAPHY;

ALPHA-MACROGLOBULINS; ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; IMMUNOENZYME TECHNIQUES; LDL-RECEPTOR RELATED PROTEIN 1; MATRIX METALLOPROTEINASE 2; MATRIX METALLOPROTEINASE 9; OXYGEN; RATS; RATS, WISTAR; RETINA; RETINAL NEOVASCULARIZATION;

EID: 33751034139     PISSN: 00144835     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.exer.2006.07.016     Document Type: Article

References (57)

1. Ahmed F., Brown K.M., Stephan D.A., Morrison J.C., Johnson E.C., and Tomarev S.I. Microarray analysis of changes in mRNA levels in the rat retina after experimental elevation of intraocular pressure. Invest. Ophthalmol. Vis. Sci. 45 (2004) 1247-1258
2. Aiello L.P. Vascular endothelial growth factor: 20th-century mechanisms, 21st-century therapies. Invest. Ophthalmol. Vis. Sci. 38 (1997) 1647-1652
3. Bacskai B.J., Xia M.Q., Strickland D.K., Rebeck G.W., and Hyman B.T. The endocytic receptor protein LRP also mediates neuronal calcium signaling via N-methyl-d-aspartate receptors. Proc. Natl. Acad. Sci. U.S.A. 97 (2000) 11551-11556
4. Barmina O.Y., Walling H.W., Fiacco G.J., Freije J.M.P., Lopez-Otin C., Jeffrey J.J., and Partridge N.C. Collagenase-3 binds to a specific receptor and requires the low density lipoprotein receptor-related protein for internalisation. J. Biol. Chem. 274 (1999) 30087-30093
5. Birkenmeier G., Grosche J., and Reichenbach A. Immunocytochemical demonstration of alpha 2-M-R/LRP on Müller (glial) cells isolated from rabbit and human retina. Neuroreport 8 (1996) 149-151
6. Casey R., and Li W.W. Factors controlling ocular angiogenesis. Am. J. Ophthalmol. 124 (1997) 521-529
7. Chan-Ling T., Gock B., and Stone J. The effect of oxygen on vasoformative cell division. Evidence that 'physiological hypoxia' is the stimulus for normal retinal vasculogenesis. Invest. Ophthalmol. Vis. Sci. 36 (1995) 1201-1214
8. Chiabrando G.A., Vides M.A., and Sánchez M.C. Differential binding properties of human pregnancy zone protein- and alpha 2 macroglobulin-proteinase complexes to low-density lipoprotein receptor-related protein. Arch. Biochem. Biophys. 398 (2002) 73-78
9. 2-macroglobulin. J. Neurosci. Res. 70 (2002) 57-64
10. D'Amore P.A. Mechanisms of retinal and choroidal angiogenesis. Invest. Opthalmol. Vis. Sci. 35 (1994) 3974-3979
11. Das A., McLamore A., Song W., and McGuire P.G. Retinal neovascularization is suppressed with a matrix metalloproteinase inhibitor. Arch. Ophthalmol. 117 (1999) 498-503
12. Das A., and McGuire P.G. Retinal and choroidal angiogenesis: pathophysiology and strategies for inhibition. Prog. Retin. Eye Res. 22 (2003) 721-748
13. Dawson D.W., Volpert O.V., Gillis P., Crawford S.E., Xu H., Benedict W., and Bouck N.P. Pigment epithelium-derived factor: a potent inhibitor of angiogenesis. Science 285 (1999) 245-248
14. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., and Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16 (1996) 4604-4613
15. Gaultier A., Salicioni A.M., Arandjelovic S., and Gonias S.L. Regulation of the composition of the extracellular matrix by low density lipoprotein receptor-related protein-1. J. Biol. Chem. 281 (2006) 7332-7340
16. Gerber H.P., Condorelli F., Park J., and Ferrara N. Differential transcriptional regulation of the two vascular endothelial growth factor receptor genes. Flt-1, but not Flk-1/KDR, is up-regulated by hypoxia. J. Biol. Chem. 272 (1997) 23659-23667
17. Goretzki L., and Mueller B.M. Low-density-lipoprotein-receptor-related protein (LRP) interacts with a GTP-binding protein. Biochem. J. 336 (1998) 381-386
18. Hahn-Dantona E., Ruiz J.F., Bornstein P., and Strickland D.K. The low density lipoprotein receptor-related protein modulates levels of matrix metalloproteinase 9 (MMP-9) by mediating its cellular catabolism. J. Biol. Chem. 276 (2001) 15498-15503
19. Herz J., Kowal R.C., Goldstein J.L., and Brown M.S. Proteolytic processing of the 600 kD low density lipoprotein receptor related protein LRP occurs in a trans-Golgi compartment. EMBO J. 9 (1990) 1769-1776
20. Herz J., and Strickland D.K. LRP: a multifunctional scavenger and signalling receptor. J. Clin. Invest. 108 (2001) 779-784
21. Holmes J.M., and Duffner A. The effect of growth retardation on abnormal neovascularization in the oxygen exposed neonatal rat. Curr. Eye Res. 15 (1996) 403-409
22. Howell B.W., and Herz J. The LDL receptor gene family: signaling functions during development. Curr. Opin. Neurobiol. 11 (2001) 74-81
23. Hussain M.M., Strickland D.K., and Bakillah A. The mammalian low-density lipoprotein receptor family. Annu. Rev. Nutr. 19 (1999) 141-172
24. Juarez C.P., Muino J.C., Guglielmone H., Sambuelli R., Echenique J.R., Hernandez M., and Luna J.D. Experimental retinopathy of prematurity: angiostatic inhibition by nimodipine, ginkgo-biloba, and dipyridamole, and response to different growth factors. Eur. J. Ophthalmol. 10 (2000) 51-59
25. Kleiner D.E., and Stetler-Stevenson W. Quantitative zymography: detection of picogram quantities of gelatinases. Anal. Biochem. 218 (1994) 325-329
26. Koong A.C., Denko N.C., Hudson K.M., Schindler C., Swiersz L., Koch C., Evans S., Ibrahim H., Le Q.T., Terris D.J., and Giaccia A.J. Candidate genes for the hypoxic tumor phenotype. Cancer Res. 60 (2000) 883-887
27. Krishnamachary B., Berg-Dixon S., Kelly B., Agani F., Feldser D., Ferreira G., Iyer N., LaRusch J., Pak B., Taghavi P., and Semenza G.L. Regulation of colon carcinoma cell invasion by hypoxia-inducible factor 1. Cancer Res. 63 (2003) 1138-1143
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
29. Lopes M.B., Bogaev C.A., Gonias S.L., and VandenBerg S.R. Expression of alpha 2-macroglobulin receptor/low density lipoprotein receptor-related protein is increased in reactive and neoplastic glial cells. FEBS Lett. 338 (1994) 301-305
30. Luna J., Tobe T., Mousa S.A., Reilly T.M., and Campochiaro P.A. Antagonists of integrin alpha v beta 3 inhibit retinal neovascularization in a murine model. Lab. Invest. 75 (1996) 563-573
31. Lutty G.A., and McLeod D.S. Retinal vascular development and oxygen-induced retinopathy: a role for adenosine. Prog. Retin. Eye Res. 22 (2003) 95-111
32. Marzolo M.P., von Bernhardi R., Bu G., and Inestrosa N.C. Expression of alpha(2)-macroglobulin receptor/low density lipoprotein receptor-related protein (LRP) in rat microglial cells. J. Neurosci. Res. 60 (2000) 401-411
33. McGuire P.G., Jones T.R., Talarico N., Warren E., and Das A. The urokinase/urokinase receptor system in retinal neovascularization: inhibition by A6 suggests a new therapeutic target. Invest. Ophthalmol. Vis. Sci. 44 (2003) 2736-2742
34. Mignati P., and Rifkin D.B. Plasminogen activators and matrix metalloproteinases in angiogenesis. Enzyme Protein 49 (1996) 117-137
35. Ozkan H., Duman N., Kumral A., Kasap B., Ozer E.A., Lebe B., Yaman A., Berk T., Yilmaz O., and Ozer E. Inhibition of vascular endothelial growth factor-induced retinal neovascularization by retinoic acid in experimental retinopathy of prematurity. Physiol. Res. (Aug 5 2005)
36. Penn J.S., Henry M.M., and Tolman B.L. Exposure to alternating hypoxia and hyperoxia causes severe proliferative retinopathy in the newborn rat. Pediatr. Res. 36 (1994) 724-731
37. 2 variation determines the severity of oxygen-induced retinopathy in newborn rats. Invest. Ophthalmol. Vis. Sci. 36 (1995) 2063-2070
38. Phelps D.L. Oxygen and developmental retinal capillary remodeling in the kitten. Invest. Ophthalmol. Vis. Sci. 31 (1990) 2194-2200
39. Rarinaga M. Shedding light on blindness. Science 267 (1995) 452-453
40. Sánchez M.C., Chiabrando G.A., and Vides M.A. Pregnancy zone Protein-tissue-type plasminogen activator complexes bind to low density lipoprotein receptor-related protein (LRP). Arch. Biochem. Biophys. 389 (2001) 218-222
41. Semenza G.L., and Wang G.L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12 (1992) 5447-5454
42. Shafiee A., Roberts D.D., Penn J.S., and Blake D.A. Thrombospondin (TSP) peptides inhibit angiogenesis in retinal explant assay and rat model of retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 41 (2000) 2378-2388
43. Sivak J.M., and Fini M.E. MMPs in the eye: emerging roles for matrix metalloproteinases in ocular physiology. Prog. Retin. Eye Res. 21 (2002) 1-14
44. Spijkers P.P., da Costa Martins P., Westein E., Gahmberg C.G., Zwaginga J.J., and Lenting P.J. LDL-receptor-related protein regulates beta2-integrin-mediated leukocyte adhesion. Blood 105 (2005) 170-177
45. Strickland D.K., Gonias S.L., and Argraves W.S. Diverse roles for the LDL receptor family. Trends Endocrinol. Metab. 13 (2002) 66-74
46. Towbin H., Staehelin T., and Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. U.S.A. 76 (1979) 4350-4354
47. Ulery P.G., Beers J., Mikhailenko I., Tanzi R.E., Rebeck G.W., Hyman B.T., and Strickland D.K. Modulation of beta-amyloid precursor protein processing by the low density lipoprotein receptor-related protein (LRP). Evidence that LRP contributes to the pathogenesis of Alzheimer's disease. J. Biol. Chem. 275 (2000) 7410-7415
48. Vinores S.A., Youssri A.I., Luna J.D., Chen Y.-S., Bhargave S., Vinores M.A., Schoenfeld C.-L., Peng B., Chan C.-Ch., LaRochelle W., Green W.R., and Campochiaro P.A. Upregulation of vascular endothelial growth factor in ischemic and non-ischemic human and experimental retinal disease. Histol. Histopathol. 12 (1997) 99-109
49. Vinores S.A., Seo M.S., Okamoto N., Ashm J.D., Wawrousek E.F., Xiao W.H., Hudish T., Derevjanik N.L., and Campochiaro P.A. Experimental models of growth factor-mediated angiogenesis and blood-retinal barrier breakdown. Gen. Pharmacol. 35 (2002) 233-239
50. Williamson J.R., Chang K., and Frangos M. Hyperglycemic pseudohypoxia and diabetic complications. Diabetes 42 (1993) 801-813
51. Wolf B.B., Lopes M.B., VandenBerg S.R., and Gonias S.L. Characterization and immunohistochemical localization of α2-macroglobulin receptor (low-density lipoprotein receptor-related protein) in human brain. Am. J. Pathol. 141 (1992) 37-42
52. Wu L., Arandjelovic S., and Gonias S.L. Effects of low density lipoprotein receptor-related protein-1 on the expression of platelet-derived growth factor beta-receptor in vitro. J. Cell. Biochem. 93 (2004) 1169-1177
53. Wykoff C.C., Pugh C.W., Maxwell P.H., Harris A.L., and Ratcliffe P.J. Identification of novel hypoxia dependent and independent target genes of the von Hippel-Lindau (VHL) tumour suppressor by mRNA differential expression profiling. Oncogene 19 (2000) 6297-6305
54. Yang M., Huang H., Li J., Li D., and Wang H. Tyrosine phosphorylation of the LDL receptor-related protein (LRP) and activation of the ERK pathway are required for connective tissue growth factor to potentiate myofibroblast differentiation. FASEB J. 18 (2004) 1920-1921
55. Yang Z., Strickland D.K., and Bornstein P. Extracellular matrix metalloproteinase 2 levels are regulated by the low-density lipoprotein-related scavenger receptor and thrombospondin 2. J. Biol. Chem. 276 (2001) 8403-8408
56. Zhang W., Ito Y., Berlin E., Roberts R., and Berkowitz B.A. Role of hypoxia during normal retinal vessel development and in experimental retinopathy of prematurity. Invest. Ophthalmol. Vis. Sci. 44 (2003) 3119-3123
57. Zhuo M., Holtzman D.M., Li Y., Osaka H., DeMaro J., Jacquin M., and Bu G. Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J. Neurosci. 20 (2000) 542-549