Overexpression of SPARC in human trabecular meshwork increases intraocular pressure and alters extracellular matrix

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 5, 2013, Pages 3309-3319

  Oh, Dong Jin ^a   Kang, Min Hyung ^a   Ooi, Yen Hoong ^b   Choi, Kyu Ryong ^c   Sage, E Helene ^d   Rhee, Douglas J ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NEW YORK DOWNTOWN HOSPITAL   (United States)

^c Mokdong Hospital   (South Korea)

^d BENAROYA RESEARCH INSTITUTE   (United States)

Author keywords

Adenovirus; Extracellular matrix; Intraocular pressure; Matrix metalloproteinases; Perfused anterior segment system; SPARC; Tissue inhibitors of matrix metalloproteinases

Indexed keywords

ADENOVIRUS VECTOR; COLLAGEN TYPE 1; COLLAGEN TYPE 4; COLLAGEN TYPE 6; FIBRONECTIN; GELATINASE B; INTERSTITIAL COLLAGENASE; LAMININ; MESSENGER RNA; OSTEONECTIN; STROMELYSIN; TISSUE INHIBITOR OF METALLOPROTEINASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1;

ADULT; ANTIBODY LABELING; ARTICLE; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; INTRAOCULAR PRESSURE; POLYACRYLAMIDE GEL ELECTROPHORESIS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOIMMUNOPRECIPITATION; TRABECULAR MESHWORK; ZYMOGRAPHY;

ADENOVIRUS; EXTRACELLULAR MATRIX; INTRAOCULAR PRESSURE; MATRIX METALLOPROTEINASES; PERFUSED ANTERIOR SEGMENT SYSTEM; SPARC; TISSUE INHIBITORS OF MATRIX METALLOPROTEINASES;

ADENOVIRIDAE; ADULT; AGED; AGED, 80 AND OVER; CELLS, CULTURED; COLLAGEN TYPE I; COLLAGEN TYPE IV; EXTRACELLULAR MATRIX; EXTRACELLULAR MATRIX PROTEINS; FIBRONECTINS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION REGULATION; GENETIC VECTORS; HUMANS; IMMUNOBLOTTING; INTRAOCULAR PRESSURE; MIDDLE AGED; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRABECULAR MESHWORK; TRANSFECTION; TUMOR SUPPRESSOR PROTEINS;

EID: 84877678635     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.12-11362     Document Type: Article

References (62)

1. Weinreb RN. Glaucoma neuroprotection: what is it? Why is it needed? Can J Ophthalmol. 2007;42:396-398.
2. Quigley HA. Number of people with glaucoma worldwide. Br J Ophthalmol. 1996;80:389-393.
3. Friedman DS, Wolfs RC, O'Colmain BJ, et al.; and the Eye Diseases Prevalence Research Group. Prevalence of openangle glaucoma among adults in the United States. Arch Ophthalmol. 2004;122:532-538.
4. Kass MA, Heuer DK, Higginbotham EJ, et al.; and the Ocular Hypertension Treatment Study Group. The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypotensive medication delays or prevents the onset of primary open-angle glaucoma. Arch Ophthalmol. 2002;120:701-713.
5. Heijl A, Leske MC, Bengtsson B, Hyman L, Bengtsson B, Hussein M; for the Early Manifest Glaucoma Trial Group. Reduction of intraocular pressure and glaucoma progression. Arch Ophthalmol. 2002;120:1268-1279.
6. Collaborative Normal-Tension Glaucoma Study Group. Comparison of glaucomatous progression between untreated patients with normal-tension glaucoma and patients with therapeutically reduced intraocular pressures. Am J Ophthal- mol. 1998;126:487-497.
7. Larsson LI, Rettig ES, Brubaker RF. Aqueous flow in open-angle glaucoma. Arch Ophthalmol. 1995;113:283-286.
8. Brubaker RF. Clinical measurements of aqueous dynamics: implications for addressing glaucoma. In: Civan MM, ed. The Eye's Aqueous Humor: From Secretion to Glaucoma. Vol. 45. San Diego: Academic Press; 1998:233-284.
9. Knepper PA, Farbman AI, Telser AG. Exogenous hyaluronidas- es and degradation of hyaluronic acid in the rabbit eye. Invest Ophthalmol Vis Sci. 1984;25:286-293.
10. Barany EH, Scotchbrook S. Influence of testicular hyaluroni- dase on the resistance to flow through the angle of the anterior chamber. Acta Physiol Scand. 1954;30:240-272.
11. Bradley JMB, Vranka J, Colvis CM, et al. Effect of matrix metalloproteinases activity on outflow in perfused human organ culture. Invest Ophthalmol Vis Sci. 1996;39:2649-2658.
12. Keller KE, Bradley JM, Kelley MJ, Acott TS. Effects of modifiers of glycosaminoglycan biosynthesis on outflow facility in perfusion culture. Invest Ophthalmol Vis Sci. 2008;49:2495-2505.
13. Rohen JW, Lutjen-Drecoll E, Flugel C, Meyer M, Grierson I. Ultrastructure of the trabecular meshwork in untreated cases of primary open-angle glaucoma (POAG). Exp Eye Res. 1993; 56:683-692.
14. Keller KE, Aga M, Bradley JM, Kelley MJ, Acott TS. Extracellular matrix turnover and outflow resistance. Exp Eye Res. 2009;88: 672-682.
15. Rhee DJ, Haddadin RI, Kang MH, Oh DJ. Matricellular proteins in the trabecular meshwork. Exp Eye Res. 2009;88:694-703.
16. Vittal V, Rose A, Gregory KE, Kelley MJ, Acott TS. Changes in gene expression by trabecular meshwork cells in response to mechanical stretching. Invest Ophthalmol Vis Sci. 2005;46: 2857-2868.
17. Tomarev SI, Wistow G, Raymond V, Dubois S, Malyukova I. Gene expression profile of the human trabecular meshwork: NEIBank sequence tag analysis. Invest Ophthalmol Vis Sci. 2003;44:2588-2596.
18. Rhee DJ, Fariss RN, Brekken R, Sage EH, Russell P. The matricellular protein SPARC is expressed in human trabecular meshwork. Exp Eye Res. 2003;77:601-607.
19. Bollinger KE, Crabb JS, Yuan X, Putliwala T, Clark AF, Crabb JW. Quantitative Proteomics: TGFb2 signaling in trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2011;52:8287-8294.
20. Tripathi R, Li J, Chan W, Tripathi B. Aqueous humor in glaucomatous eyes contains an increased level of TGF-beta 2. Exp Eye Res. 1994;59:723-727.
21. Haddadin RI, Oh DJ, Filipoppopolous T, et al. SPARC-null mice exhibit lower intraocular pressures. Invest Ophthalmol Vis Sci. 2009;50:3771-3777.
22. Mocanu JD, Yip KW, Alajez NM, et al. Imaging the modulation of adenoviral kinetics and biodistribution for cancer gene therapy. Mol Ther. 2007;15:921-929.
23. Mesonero A, Suarez DL, van Santen E, Tang DC, Toro H. Avian influenza in ovo vaccination with replication defective recombinant adenovirus in chickens: vaccine potency, anti- body persistence, and maternal antibody transfer. Avian Dis. 2011;55:285-292.
24. Ethier CR, Wada S, Chan D, Stamer WD. Experimental and numerical studies of adenovirus delivery to outflow tissues of perfused human anterior segments. Invest Ophthalmol Vis Sci. 2004;45:1863-1870.
25. Atorrasagasti C, Malvicini M, Aquino JB, et al. Overexpression of SPARC obliterates the in vivo tumorigenicity of human hepatocellular carcinoma cells. Int J Cancer. 2010;126:2726-2740.
26. Moses RA, Grodzki WJ, Etheridge EL, Wilson CD. Schlemm's canal: the effect of intraocular pressure. Invest Ophthalmol Vis Sci. 1981;20:61-68.
27. Maepea O, Bill A. Pressures in the juxtacanalicular tissue and Schlemm's canal in monkeys. Exp Eye Res. 1992;54:879-883.
28. Maepea O, Bill A. The pressures in the episcleral veins, Schlemm's canal and trabecular meshwork in monkeys: effects of changes in intraocular pressure. Exp Eye Res. 1989;49:645-663.
29. Seiler T, Wollensak J. The resistance of the trabecular meshwork to aqueous humor outflow. Graefes Arch Clin Exp Ophthalmol. 1985;223:88-91.
30. Fuchshofer R, Tamm ER. Modulation of extracellular matrix turnover in the trabecular meshwork. Exp Eye Res. 2009;88: 683-388.
31. Liton PB, Gonzalez P, Epstein DL. The role of proteolytic cellular systems in trabecular meshwork homeostasis. Exp Eye Res. 2009;88:724-728.
32. Tian B, Gabelt BT, Geiger B, Kaufman PL. The role of the actomyosin system in regulating trabecular fluid outflow. Exp Eye Res. 2009;88:713-717.
33. Overby DR, Stamer WD, Johnson M. The changing paradigm of outflow resistance generation: towards synergistic models of the JCT and inner wall endothelium. Exp Eye Res. 2009;88: 656-670.
34. Ueda J, Wentz-Hunter K, Yue BY. Distribution of myocilin and extracellular matrix components in the juxtacanalicular tissue of human eyes. Invest Ophthalmol Vis Sci. 2002;43:1068-1076.
35. Yue BYJT. The extracellular matrix and its modulation in the trabecular meshwork. Surv Ophthalmol. 1996;40:379-390.
36. Rohen JW. Why is intraocular pressure elevated in chronic simple glaucoma? Anatomical considerations. Ophthalmology. 1983;90:758-765.
37. Johnson D, Gottanka J, Flugel C, Hoffmann F, Futa R, Lutjen- Drecoll E. Ultrastructural changes in the trabecular meshwork of human eyes treated with corticosteroids. Arch Ophthalmol. 1997;115:375-383.
38. Zhou L, Li Y, Yue BY. Glucocorticoid effects on extracellular matrix proteins and integrins in bovine trabecular meshwork cells in relation to glaucoma. Int J Mol Med. 1998;1:339-346.
39. Clark AF, Wilson K, de Kater AW, Allingham RR, McCartney MD. Dexamethasone-induced ocular hypertension in perfu- sion-culture human eyes. Invest Ophthalmol Vis Sci. 1995;36: 478-489.
40. Johnson DH, Bradley JM, Acott TS. The effect of dexameth- asone on glycosaminoglycans of human trabecular meshwork in perfusion organ culture. Invest Ophthalmol Vis Sci. 1990; 31:2568-2571.
41. Tane N, Dhar S, Roy S, Pinheiro A, Ohira A, Roy S. Effect of excess synthesis of extracellular matrix components by trabecular meshwork cells: possible consequence on aqueous outflow. Exp Eye Res. 2007;84:832-842.
42. Zhang M, Maddala R, Rao PV. Novel molecular insights into RhoA GTPase-induced resistance to aqueous humor outflow through the trabecular meshwork. Am J Physiol Cell Physiol. 2008;295:C1057-C1070.
43. Yue BYJT. The extracellular matrix and its modulation in the trabecular meshwork. Surv Ophthalmol. 1996;40:379-390.
44. Aihara M, Lindsey JD, Weinreb RN. Ocular hypertension in mice with a targeted type I collagen mutation. Invest Ophthalmol Vis Sci. 2003;44:1581-1585.
45. Zanussi S, Doliana R, Segat D, Bonaldo P, Colombatti A. Thehuman type VI collagen gene. mRNA and protein variants of the alpha 3 chain generated by alternative splicing of an additional 5-end exon. J Biol Chem. 1992;267:24082-24089.
46. Chu ML, Zhang RZ, Pan TC, et al. Mosaic structure of globular domains in the human type VI collagen alpha 3 chain: similarity to von Willebrand factor, fibronectin, actin, salivary proteins and aprotinin type protease inhibitors. EMBO J. 1990; 9:385-393.
47. Pfaff M, Aumailley M, Specks U, Knolle J, Zerwes HG, Timpl R. Integrin and Arg-Gly-Asp dependence of cell adhesion to the native and unfolded triple helix of collagen type VI. Exp Cell Res. 1993;206:167-176.
48. Myint E, Brown DJ, Ljubimov AV, Kyaw M, Kenney MC. Cleavage of human corneal type VI collagen alpha 3 chain by matrix metalloproteinase-2. Cornea. 1996;15:490-496.
49. Lamandé SR, Sigalas E, Pan TC, et al. The role of the alpha3(VI) chain in collagen VI assembly. Expression of an alpha3(VI) chain lacking N-terminal modules N10-N7 restores collagen VI assembly, secretion, and matrix deposition in an alpha3(VI)- deficient cell line. J Biol Chem. 1998;273:7423-7430.
50. Martinek N, Shahab J, Sodek J, Ringuette M. Is SPARC anevolutionarily conserved collagen chaperone? J Dent Res. 2007;86:296-305.
51. Chlenski A, Guerrero LJ, Salwen HR, et al. Secreted protein acidic and rich in cysteine is a matrix scavenger chaperone. PLoS One. 2011;6:e23880.
52. Emerson RO, Sage EH, Ghoh JG, Clark JI. Chaperone-like activity revealed in the matricellular protein SPARC. J Cell Biochem. 2006;98:701-705.
53. Oh DJ, Martin JL, Williams AJ, et al. Analysis of expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human ciliary body following latanoprost. Invest Ophthalmol Vis Sci. 2006;47:453-463.
54. Oh DJ, Martin JL, Williams AJ, Russell P, Birk DE, Rhee DJ. Effect of latanoprost on the expression of matrix metalloproteinases and their tissue inhibitors in human trabecular meshwork cells. Invest Ophthalmol Vis Sci. 2006;47:3887-3895.
55. McCurdy S, Baicu CF, Heymans S, Bradshaw AD. Cardiac extracellular matrix remodeling: fibrillar collagens and Secreted Protein Acidic and Rich in Cysteine (SPARC). J Mol Cell Cardiol. 2010;48:544-549.
56. Hohenester E, Sasaki T, Guidici C, Farndale RW, Bachinger HP. Structural basis of sequence-specific collagen recognition by SPARC. Proc Natl Acad Sci U S A. 2008;105:18273-18277.
57. Kandalam V, Basu R, Moore L, et al. Lack of tissue inhibitor of metalloproteinases 2 leads to exacerbated left ventricular dysfunction and adverse extracellular matrix remodeling in response to biomechanical stress. Circulation. 2011;124: 2094-2105.
58. Chang W, Wei K, Jacobs SS, Upadhyay D, Weill D, Rosen GD. SPARC suppresses apoptosis of idiopathic pulmonary fibrosis fibroblasts through constitutive activation of beta-catenin. J Biol Chem. 2010;285:8196-8206.
59. Bhoopathi P, Chetty C, Gujrati M, Dinh DH, Rao JS, Lakka SS. The role of MMP-9 in the anti-angiogenic effect of secreted protein acidic and rich in cysteine. Br J Cancer. 2010;102: 530-540.
60. Arnold SA, Rivera LB, Miller AF, et al. Lack of host SPARC enhances vascular function and tumor spread in an orthotopic murine model of pancreatic carcinomas. Dis Model Mech. 2010;3:57-72.
61. Atorrasagasti C, Aquino JB, Hofman L, et al. SPARC down-stream attenuates the profibrogenic response of hepatic stellate cells induced by TGF-b1 and PDGF. Am J Physiol Gastrointest Liver Physiol. 2011;300:G739-G748.
62. Wei HY, Liu JL, Lv BJ, Xing L, Fu SY. SPARC modulates expression of extracellular matrix genes in human trabecular meshwork cells. Acta Ophthalmol. 2012;90:e138-e143.