Elevation of intraocular pressure in rodents using viral vectors targeting the trabecular meshwork

Experimental Eye Research

Volumn 141, Issue , 2015, Pages 33-41

  Pang, Iok Hou ^a   Millar, J Cameron ^a   Clark, Abbot F ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

Author keywords

Animal models; Glaucoma; Viral vectors

Indexed keywords

DICKKOPF 1 PROTEIN; GREM1 PROTEIN; HERMES ANTIGEN; MYOCILIN; PROTEIN; SECRETED FRIZZLED RELATED PROTEIN 1; TRANSFORMING GROWTH FACTOR BETA2; UNCLASSIFIED DRUG; VIRUS VECTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EXPERIMENTAL MODEL; EYE; EYE INFLAMMATION; GENE EXPRESSION; GLAUCOMA; HUMAN ADENOVIRUS 5; INTRAOCULAR HYPERTENSION; INTRAOCULAR PRESSURE; MOUSE; MUTANT; NONHUMAN; OPEN ANGLE GLAUCOMA; PATHOGENESIS; PRIORITY JOURNAL; TRABECULAR MESHWORK; TRANSGENE; TROPISM; ANIMAL; DISEASE MODEL; GENE VECTOR; GENETICS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VIROLOGY; VIRUS;

ANIMALS; DISEASE MODELS, ANIMAL; GENETIC VECTORS; GLAUCOMA; INTRAOCULAR PRESSURE; MICE, TRANSGENIC; TRABECULAR MESHWORK; TRANSGENES; VIRUSES;

EID: 84945443586     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.04.003     Document Type: Article

References (105)

1. Acland G.M., Aguirre G.D., Bennett J., Aleman T.S., Cideciyan A.V., Bennicelli J., Dejneka N.S., Pearce-Kelling S.E., Maguire A.M., Palczewski K., Hauswirth W.W., Jacobson S.G. Long-term restoration of rod and cone vision by single dose rAAV-mediated gene transfer to the retina in a canine model of childhood blindness. Mol. Ther. 2005, 12(6):1072-1082.
2. Acland G.M., Aguirre G.D., Ray J., Zhang Q., Aleman T.S., Cideciyan A.V., Pearce-Kelling S.E., Anand V., Zeng Y., Maguire A.M., Jacobson S.G., Hauswirth W.W., Bennett J. Gene therapy restores vision in a canine model of childhood blindness. Nat. Genet. 2001, 28(1):92-95.
3. AGIS The Advanced Glaucoma Intervention Study (AGIS): 7. The relationship between control of intraocular pressure and visual field deterioration.The AGIS Investigators. Am. J. Ophthalmol. 2000, 130(4):429-440.
4. Aihara M., Lindsey J.D., Weinreb R.N. Experimental mouse ocular hypertension: establishment of the model. Invest Ophthalmol. Vis. Sci. 2003, 44(10):4314-4320.
5. Aihara M., Lindsey J.D., Weinreb R.N. Ocular hypertension in mice with a targeted type I collagen mutation. Invest Ophthalmol. Vis. Sci. 2003, 44(4):1581-1585.
6. Alba R., Bosch A., Chillon M. Gutless adenovirus: last-generation adenovirus for gene therapy. Gene Ther. 2005, 12(Suppl. 1):S18-S27.
7. Alward W.L., Fingert J.H., Coote M.A., Johnson A.T., Lerner S.F., Junqua D., Durcan F.J., McCartney P.J., Mackey D.A., Sheffield V.C., Stone E.M. Clinical features associated with mutations in the chromosome 1 open-angle glaucoma gene (GLC1A). N. Engl. J. Med. 1998, 338(15):1022-1027.
8. Anderson M.G., Libby R.T., Gould D.B., Smith R.S., John S.W. High-dose radiation with bone marrow transfer prevents neurodegeneration in an inherited glaucoma. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(12):4566-4571.
9. Anderson M.G., Smith R.S., Hawes N.L., Zabaleta A., Chang B., Wiggs J.L., John S.W. Mutations in genes encoding melanosomal proteins cause pigmentary glaucoma in DBA/2J mice. Nat. Genet. 2002, 30(1):81-85.
10. Angers S., Moon R.T. Proximal events in Wnt signal transduction. Nat. Rev. Mol. Cell. Biol. 2009, 10(7):468-477.
11. Balaggan K.S., Binley K., Esapa M., Iqball S., Askham Z., Kan O., Tschernutter M., Bainbridge J.W., Naylor S., Ali R.R. Stable and efficient intraocular gene transfer using pseudotyped EIAV lentiviral vectors. J. Gene Med. 2006, 8(3):275-285.
12. Barraza R.A., McLaren J.W., Poeschla E.M. Prostaglandin pathway gene therapy for sustained reduction of intraocular pressure. Mol. Ther. 2010, 18(3):491-501.
13. Barraza R.A., Rasmussen C.A., Loewen N., Cameron J.D., Gabelt B.T., Teo W.L., Kaufman P.L., Poeschla E.M. Prolonged transgene expression with lentiviral vectors in the aqueous humor outflow pathway of nonhuman primates. Hum. Gene Ther. 2009, 20(3):191-200.
14. Bennett J., Anand V., Acland G.M., Maguire A.M. Cross-species comparison of in vivo reporter gene expression after recombinant adeno-associated virus-mediated retinal transduction. Methods Enzymol. 2000, 316:777-789.
15. Bennett J., Duan D., Engelhardt J.F., Maguire A.M. Real-time, noninvasive in vivo assessment of adeno-associated virus-mediated retinal transduction. Invest Ophthalmol. Vis. Sci. 1997, 38(13):2857-2863.
16. Benozzi J., Nahum L.P., Campanelli J.L., Rosenstein R.E. Effect of hyaluronic acid on intraocular pressure in rats. Invest Ophthalmol. Vis. Sci. 2002, 43(7):2196-2200.
17. Borras T., Xue W., Choi V.W., Bartlett J.S., Li G., Samulski R.J., Chisolm S.S. Mechanisms of AAV transduction in glaucoma-associated human trabecular meshwork cells. J. Gene Med. 2006, 8(5):589-602.
18. Budenz D.L., Bennett J., Alonso L., Maguire A. In vivo gene transfer into murine corneal endothelial and trabecular meshwork cells. Invest Ophthalmol. Vis. Sci. 1995, 36(11):2211-2215.
19. Buie L.K., Rasmussen C.A., Porterfield E.C., Ramgolam V.S., Choi V.W., Markovic-Plese S., Samulski R.J., Kaufman P.L., Borras T. Self-complementary AAV virus (scAAV) safe and long-term gene transfer in the trabecular meshwork of living rats and monkeys. Invest Ophthalmol. Vis. Sci. 2010, 51(1):236-248.
20. Buie L.K., Karim M.Z., Smith M.H., Borras T. Development of a model of elevated intraocular pressure in rats by gene transfer of bone morphogenic protein 2. Invest Ophthalmol. Vis. Sci. 2013, 54(8):5441-5455.
21. Cao Y., Wei H., Pfaffl M.W., Da B. Effect of transforming growth factor beta 2 on phagocytosis in cultured bovine trabecular meshwork cells. Ophthalmologe 2003, 100(7):535-538.
22. Challa P., Luna C., Liton P.B., Chamblin B.S., Wakefield J.K., Ramabhadran R., Epstein D.L., Gonzalez P. Lentiviral mediated gene delivery to the anterior chamber of rodent eyes. Mol. Vis. 2005, 11:425-430.
23. Choi J., Miller A.M., Nolan M.J., Yue B.Y., Thotz S.T., Clark A.F., Agarwal N., Knepper P.A. Soluble CD44 is cytotoxic to trabecular meshwork and retinal ganglion cells in vitro. Invest Ophthalmol. Vis. Sci. 2005, 46(1):214-222.
24. Clark A.F., Steely H.T., Dickerson J.E., English-Wright S., Stropki K., McCartney M.D., Jacobson N., Shepard A.R., Clark J.I., Matsushima H., Peskind E.R., Leverenz J.B., Wilkinson C.W., Swiderski R.E., Fingert J.H., Sheffield V.C., Stone E.M. Glucocorticoid induction of the glaucoma gene MYOC in human and monkey trabecular meshwork cells and tissues. Invest Ophthalmol. Vis. Sci. 2001, 42(8):1769-1780.
25. Dudus L., Anand V., Acland G.M., Chen S.J., Wilson J.M., Fisher K.J., Maguire A.M., Bennett J. Persistent transgene product in retina, optic nerve and brain after intraocular injection of rAAV. Vis. Res. 1999, 39(15):2545-2553.
26. Epstein A.L. HSV-1-based amplicon vectors: design and applications. Gene Ther. 2005, 12(Suppl. 1):S154-S158.
27. Fleenor D.L., Shepard A.R., Hellberg P.E., Jacobson N., Pang I.H., Clark A.F. TGFbeta2-induced changes in human trabecular meshwork: implications for intraocular pressure. Invest Ophthalmol. Vis. Sci. 2006, 47(1):226-234.
28. Fraefel C., Mendes-Madeira A., Mabon O., Lefebvre A., Le Meur G., Ackermann M., Moullier P., Rolling F. In vivo gene transfer to the rat retina using herpes simplex virus type 1 (HSV-1)-based amplicon vectors. Gene Ther. 2005, 12(16):1283-1288.
29. Fuchshofer R., Birke M., Welge-Lussen U., Kook D., Lutjen-Drecoll E. Transforming growth factor-beta 2 modulated extracellular matrix component expression in cultured human optic nerve head astrocytes. Invest Ophthalmol. Vis. Sci. 2005, 46(2):568-578.
30. Fuchshofer R., Yu A.H., Welge-Lussen U., Tamm E.R. Bone morphogenetic protein-7 is an antagonist of transforming growth factor-beta2 in human trabecular meshwork cells. Invest Ophthalmol. Vis. Sci. 2007, 48(2):715-726.
31. Gao G.P., Alvira M.R., Wang L., Calcedo R., Johnston J., Wilson J.M. Novel adeno-associated viruses from rhesus monkeys as vectors for human gene therapy. Proc. Natl. Acad. Sci. U. S. A. 2002, 99(18):11854-11859.
32. Ginsberg H.S. The ups and downs of adenovirus vectors. Bull. N. Y. Acad. Med. 1996, 73(1):53-58.
33. Giovingo M., Nolan M., McCarty R., Pang I.H., Clark A.F., Beverley R.M., Schwartz S., Stamer W.D., Walker L., Grybauskas A., Skuran K., Kuprys P.V., Yue B.Y., Knepper P.A. sCD44 overexpression increases intraocular pressure and aqueous outflow resistance. Mol. Vis. 2013, 19:2151-2164.
34. Goff S.P., Berg P. Construction of hybrid viruses containing SV40 and lambda phage DNA segments and their propagation in cultured monkey cells. Cell 1976, 9(4 PT 2):695-705.
35. Gordon M.O., Beiser J.A., Brandt J.D., Heuer D.K., Higginbotham E.J., Johnson C.A., Keltner J.L., Miller J.P., Parrish R.K., Wilson M.R., Kass M.A. The ocular hypertension treatment Study: baseline factors that predict the onset of primary open-angle glaucoma. Arch. Ophthalmol. 2002, 120(6):714-720. discussion 829-730.
36. Gottanka J., Chan D., Eichhorn M., Lutjen-Drecoll E., Ethier C.R. Effects of TGF-beta2 in perfused human eyes. Invest Ophthalmol. Vis. Sci. 2004, 45(1):153-158.
37. Gould D.B., Miceli-Libby L., Savinova O.V., Torrado M., Tomarev S.I., Smith R.S., John S.W. Genetically increasing myoc expression supports a necessary pathologic role of abnormal proteins in glaucoma. Mol. Cell. Biol. 2004, 24(20):9019-9025.
38. Hauswirth W.W., Lewin A.S., Zolotukhin S., Muzyczka N. Production and purification of recombinant adeno-associated virus. Methods Enzymol. 2000, 316:743-761.
39. Hoffman L.M., Maguire A.M., Bennett J. Cell-mediated immune response and stability of intraocular transgene expression after adenovirus-mediated delivery. Invest Ophthalmol. Vis. Sci. 1997, 38(11):2224-2233.
40. Howell G.R., Macalinao D.G., Sousa G.L., Walden M., Soto I., Kneeland S.C., Barbay J.M., King B.L., Marchant J.K., Hibbs M., Stevens B., Barres B.A., Clark A.F., Libby R.T., John S.W. Molecular clustering identifies complement and endothelin induction as early events in a mouse model of glaucoma. J. Clin. Invest 2011, 121(4):1429-1444.
41. Howell G.R., MacNicoll K.H., Braine C.E., Soto I., Macalinao D.G., Sousa G.L., John S.W. Combinatorial targeting of early pathways profoundly inhibits neurodegeneration in a mouse model of glaucoma. Neurobiol. Dis. 2014, 71:44-52.
42. Inatani M., Tanihara H., Katsuta H., Honjo M., Kido N., Honda Y. Transforming growth factor-beta 2 levels in aqueous humor of glaucomatous eyes. Graefes Arch. Clin. Exp. Ophthalmol. 2001, 239(2):109-113.
43. Jacobson N., Andrews M., Shepard A.R., Nishimura D., Searby C., Fingert J.H., Hageman G., Mullins R., Davidson B.L., Kwon Y.H., Alward W.L., Stone E.M., Clark A.F., Sheffield V.C. Non-secretion of mutant proteins of the glaucoma gene myocilin in cultured trabecular meshwork cells and in aqueous humor. Hum. Mol. Genet. 2001, 10(2):117-125.
44. Jampel H.D., Roche N., Stark W.J., Roberts A.B. Transforming growth factor-beta in human aqueous humor. Curr. Eye Res. 1990, 9(10):963-969.
45. Joe M.K., Sohn S., Hur W., Moon Y., Choi Y.R., Kee C. Accumulation of mutant myocilins in ER leads to ER stress and potential cytotoxicity in human trabecular meshwork cells. Biochem. Biophys. Res. Commun. 2003, 312(3):592-600.
46. Junglas B., Yu A.H., Welge-Lussen U., Tamm E.R., Fuchshofer R. Connective tissue growth factor induces extracellular matrix deposition in human trabecular meshwork cells. Exp. Eye Res. 2009, 88(6):1065-1075.
47. Junglas B., Kuespert S., Seleem A.A., Struller T., Ullmann S., Bosl M., Bosserhoff A., Kostler J., Wagner R., Tamm E.R., Fuchshofer R. Connective tissue growth factor causes glaucoma by modifying the actin cytoskeleton of the trabecular meshwork. Am. J. Pathol. 2012, 180(6):2386-2403.
48. Kang M.H., Oh D.J., Kang J.H., Rhee D.J. Regulation of SPARC by transforming growth factor beta2 in human trabecular meshwork. Invest Ophthalmol. Vis. Sci. 2013, 54(4):2523-2532.
49. Kim B.S., Savinova O.V., Reedy M.V., Martin J., Lun Y., Gan L., Smith R.S., Tomarev S.I., John S.W., Johnson R.L. Targeted disruption of the myocilin gene (Myoc) suggests that human glaucoma-causing mutations are gain of function. Mol. Cell. Biol. 2001, 21(22):7707-7713.
50. Knepper P.A., Mayanil C.S., Goossens W., Wertz R.D., Holgren C., Ritch R., Allingham R.R. Aqueous humor in primary open-angle glaucoma contains an increased level of CD44S. Invest Ophthalmol. Vis. Sci. 2002, 43(1):133-139.
51. Knepper P.A., Miller A.M., Choi J., Wertz R.D., Nolan M.J., Goossens W., Whitmer S., Yue B.Y., Ritch R., Liebmann J.M., Allingham R.R., Samples J.R. Hypophosphorylation of aqueous humor sCD44 and primary open-angle glaucoma. Invest Ophthalmol. Vis. Sci. 2005, 46(8):2829-2837.
52. Leask A., Parapuram S.K., Xu S., Abraham D.J. Connective tissue growth factor (CTGF, CCN2) gene regulation: a potent clinical bio-marker of fibroproliferative disease?. J. Cell. Commun. Signal 2009, 3(2):89-94.
53. Levkovitch-Verbin H., Quigley H.A., Martin K.R., Valenta D., Baumrind L.A., Pease M.E. Translimbal laser photocoagulation to the trabecular meshwork as a model of glaucoma in rats. Invest Ophthalmol. Vis. Sci. 2002, 43(2):402-410.
54. Li G., Farsiu S., Qiu J., Dixon A., Song Ch, McKinnon S.J., Yuan F., Gonzalez P., Stamer W.D. Disease progression in iridocorneal angle tissues of BMP2-induced ocular hypertensive mice with optical coherence tomography. Mol. Vis. 2014, 20:1695-1709.
55. Li G., Gonzalez L.J., Camras L.J., Navarro I., Qui J., Challa P., Stamer W.D. Optimizing gene transfer to conventional outflow cells in living mouse eyes. Exp. Eye Res. 2013, 109:8-16.
56. Lipinski D.M., Barnard A.R., Charbel Issa P., Singh M.S., De Silva S.R., Trabalza A., Eleftheriadou I., Ellison S.M., Mazarakis N.D., MacLaren R.E. Vesicular stomatitis virus glycoprotein- and Venezuelan equine encephalitis virus-derived glycoprotein-pseudotyped lentivirus vectors differentially transduce corneal endothelium, trabecular meshwork, and human photoreceptors. Hum. Gene Ther. 2014, 25(1):50-62.
57. Liu X., Hu Y., Filla M.S., Gabelt B.T., Peters D.M., Brandt C.R., Kaufman P.L. The effect of C3 transgene expression on actin and cellular adhesions in cultured human trabecular meshwork cells and on outflow facility in organ cultured monkey eyes. Mol. Vis. 2005, 11:1112-1121.
58. Loewen N., Fautsch M.P., Peretz M., Bahler C.K., Cameron J.D., Johnson D.H., Poeschla E.M. Genetic modification of human trabecular meshwork with lentiviral vectors. Hum. Gene Ther. 2001, 12(17):2109-2119.
59. Loewen N., Fautsch M.P., Teo W.L., Bahler C.K., Johnson D.H., Poeschla E.M. Long-term, targeted genetic modification of the aqueous humor outflow tract coupled with noninvasive imaging of gene expression in vivo. Invest Ophthalmol. Vis. Sci. 2004, 45(9):3091-3098.
60. Logan C.Y., Nusse R. The Wnt signaling pathway in development and disease. Annu Rev. Cell. Dev. Biol. 2004, 20:781-810.
61. MacDonald B.T., Tamai K., He X. Wnt/beta-catenin signaling: components, mechanisms, and diseases. Dev. Cell. 2009, 17(1):9-26.
62. Mao B., Wu W., Li Y., Hoppe D., Stannek P., Glinka A., Niehrs C. LDL-receptor-related protein 6 is a receptor for Dickkopf proteins. Nature 2001, 411(6835):321-325.
63. Mao W., Millar J.C., Wang W.H., Silverman S.M., Liu Y., Wordinger R.J., Rubin J.S., Pang I.H., Clark A.F. Existence of the canonical Wnt signaling pathway in the human trabecular meshwork. Invest Ophthalmol. Vis. Sci. 2012, 53(11):7043-7051.
64. McDowell C.M., Luan T., Zhang Z., Putliwala T., Wordinger R.J., Millar J.C., John S.W., Pang I.H., Clark A.F. Mutant human myocilin induces strain specific differences in ocular hypertension and optic nerve damage in mice. Exp. Eye Res. 2012, 100:65-72.
65. McDowell C.M., Tebow H.E., Wordinger R.J., Clark A.F. Smad3 is necessary for transforming growth factor-beta2 induced ocular hypertension in mice. Exp. Eye Res. 2013, 116:419-423.
66. Millar J.C., Clark A.F., Pang I.H. Assessment of aqueous humor dynamics in the mouse by a novel method of constant-flow infusion. Invest Ophthalmol. Vis. Sci. 2011, 52(2):685-694.
67. Millar J.C., Pang I.H., Wang W.H., Wang Y., Clark A.F. Effect of immunomodulation with anti-CD40L antibody on adenoviral-mediated transgene expression in mouse anterior segment. Mol. Vis. 2008, 14:10-19.
68. Min S.H., Molday L.L., Seeliger M.W., Dinculescu A., Timmers A.M., Janssen A., Tonagel F., Tanimoto N., Weber B.H., Molday R.S., Hauswirth W.W. Prolonged recovery of retinal structure/function after gene therapy in an Rs1h-deficient mouse model of x-linked juvenile retinoschisis. Mol. Ther. 2005, 12(4):644-651.
69. Morrison J.C., Moore C.G., Deppmeier L.M., Gold B.G., Meshul C.K., Johnson E.C. A rat model of chronic pressure-induced optic nerve damage. Exp. Eye Res. 1997, 64(1):85-96.
70. Moustakas A., Heldin C.H. Non-Smad TGF-beta signals. J. Cell. Sci. 2005, 118(Pt 16):3573-3584.
71. Nguyen T.D., Chen P., Huang W.D., Chen H., Johnson D., Polansky J.R. Gene structure and properties of TIGR, an olfactomedin-related glycoprotein cloned from glucocorticoid-induced trabecular meshwork cells. J. Biol. Chem. 1998, 273(11):6341-6350.
72. Nolan M.J., Giovingo M.C., Miller A.M., Wertz R.D., Ritch R., Liebmann J.M., Allingham R.R., Herndon L.W., Wax M.B., Smolyak R., Hasan F., Barnett E.M., Samples J.R., Knepper P.A. Aqueous humor sCD44 concentration and visual field loss in primary open-angle glaucoma. J. Glaucoma 2007, 16(5):419-429.
73. Overby D.R., Bertrand J., Tektas O.Y., Boussommier-Calleja A., Schicht M., Ethier C.R., Woodward D.F., Stamer W.D., Lutjen-Drecoll E. Ultrastructural changes associated with dexamethasone-induced ocular hypertension in mice. Invest Ophthalmol. Vis. Sci. 2014, 55(8):4922-4933.
74. Peel A.L., Klein R.L. Adeno-associated virus vectors: activity and applications in the CNS. J. Neurosci. Methods 2000, 98(2):95-104.
75. Ralph G.S., Binley K., Wong L.F., Azzouz M., Mazarakis N.D. Gene therapy for neurodegenerative and ocular diseases using lentiviral vectors. Clin. Sci. (London) 2006, 110(1):37-46.
76. Roszko I., Sawada A., Solnica-Krezel L. Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin. Cell. Dev. Biol. 2009, 20(8):986-997.
77. Sappington R.M., Carlson B.J., Crish S.D., Calkins D.J. The microbead occlusion model: a paradigm for induced ocular hypertension in rats and mice. Invest Ophthalmol. Vis. Sci. 2010, 51(1):207-216.
78. Senatorov V., Malyukova I., Fariss R., Wawrousek E.F., Swaminathan S., Sharan S.K., Tomarev S. Expression of mutated mouse myocilin induces open-angle glaucoma in transgenic mice. J. Neurosci. 2006, 26(46):11903-11914.
79. Sethi A., Jain A., Zode G.S., Wordinger R.J., Clark A.F. Role of TGFbeta/Smad signaling in gremlin induction of human trabecular meshwork extracellular matrix proteins. Invest Ophthalmol. Vis. Sci. 2011, 52(8):5251-5259.
80. Shareef S.R., Garcia-Valenzuela E., Salierno A., Walsh J., Sharma S.C. Chronic ocular hypertension following episcleral venous occlusion in rats. Exp. Eye Res. 1995, 61(3):379-382.
81. Shepard A.R., Jacobson N., Millar J.C., Pang I.H., Steely H.T., Searby C.C., Sheffield V.C., Stone E.M., Clark A.F. Glaucoma-causing myocilin mutants require the peroxisomal targeting signal-1 receptor (PTS1R) to elevate intraocular pressure. Hum. Mol. Genet. 2007, 16(6):609-617.
82. Shepard A.R., Millar J.C., Pang I.H., Jacobson N., Wang W.H., Clark A.F. Adenoviral gene transfer of active human transforming growth factor-{beta}2 elevates intraocular pressure and reduces outflow facility in rodent eyes. Invest Ophthalmol. Vis. Sci. 2010, 51(4):2067-2076.
83. Shinzato M., Yamashiro Y., Miyara N., Iwamatsu A., Takeuchi K., Umikawa M., Bayarjargal M., Kariya K., Sawaguchi S. Proteomic analysis of the trabecular meshwork of rats in a steroid-induced ocular hypertension model: downregulation of type I collagen C-propeptides. Ophthalmic Res. 2007, 39(6):330-337.
84. Spencer B., Agarwala S., Miskulin M., Smith M., Brandt C.R. Herpes simplex virus-mediated gene delivery to the rodent visual system. Invest Ophthalmol. Vis. Sci. 2000, 41(6):1392-1401.
85. Stone E.M., Fingert J.H., Alward W.L., Nguyen T.D., Polansky J.R., Sunden S.L., Nishimura D., Clark A.F., Nystuen A., Nichols B.E., Mackey D.A., Ritch R., Kalenak J.W., Craven E.R., Sheffield V.C. Identification of a gene that causes primary open angle glaucoma. Science 1997, 275(5300):668-670.
86. Su Y., Cheng J., Liu H., Wang F., Zhao S. Adenovirus conducted connective tissue growth factor on extracellular matrix in trabecular meshwork and its role on aqueous humor outflow facility. Mol. Biol. Rep. 2013, 40(11):6091-6096.
87. Swaminathan S.S., Oh D.J., Kang M.H., Shepard A.R., Pang I.H., Rhee D.J. TGF-beta2-mediated ocular hypertension is attenuated in SPARC-null mice. Invest Ophthalmol. Vis. Sci. 2014, 55(7):4084-4097.
88. Tomarev S.I., 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(6):2588-2596.
89. Tovar-Vidales T., Clark A.F., Wordinger R.J. Transforming growth factor-beta2 utilizes the canonical Smad-signaling pathway to regulate tissue transglutaminase expression in human trabecular meshwork cells. Exp. Eye Res. 2011, 93(4):442-451.
90. Tripathi R.C., Li J., Chan W.F., Tripathi B.J. Aqueous humor in glaucomatous eyes contains an increased level of TGF-beta 2. Exp. Eye Res. 1994, 59(6):723-727.
91. Ueyama K., Mori K., Shoji T., Omata H., Gehlbach P.L., Brough D.E., Wei L.L., Yoneya S. Ocular localization and transduction by adenoviral vectors are serotype-dependent and can be modified by inclusion of RGD fiber modifications. PLoS One 2014, 9(9):e108071.
92. Villarreal G., Chatterjee A., Oh S.S., Oh D.J., Kang M.H., Rhee D.J. Canonical wnt signaling regulates extracellular matrix expression in the trabecular meshwork. Invest Ophthalmol. Vis. Sci. 2014, 55(11):7433-7440.
93. Walsh M.M., Yi H., Friedman J., Cho K.I., Tserentsoodol N., McKinnon S., Searle K., Yeh A., Ferreira P.A. Gene and protein expression pilot profiling and biomarkers in an experimental mouse model of hypertensive glaucoma. Exp. Biol. Med. (Maywood) 2009, 234(8):918-930.
94. Wang F., Tang W., McGraw H.M., Bennett J., Enquist L.W., Friedman H.M. Herpes simplex virus type 1 glycoprotein e is required for axonal localization of capsid, tegument, and membrane glycoproteins. J. Virol. 2005, 79(21):13362-13372.
95. Wang W.H., McNatt L.G., Pang I.H., Millar J.C., Hellberg P.E., Hellberg M.H., Steely H.T., Rubin J.S., Fingert J.H., Sheffield V.C., Stone E.M., Clark A.F. Increased expression of the WNT antagonist sFRP-1 in glaucoma elevates intraocular pressure. J. Clin. Invest 2008, 118(3):1056-1064.
96. Whitlock N.A., McKnight B., Corcoran K.N., Rodriguez L.A., Rice D.S. Increased intraocular pressure in mice treated with dexamethasone. Invest Ophthalmol. Vis. Sci. 2010, 51(12):6496-6503.
97. Wordinger R.J., Agarwal R., Talati M., Fuller J., Lambert W., Clark A.F. Expression of bone morphogenetic proteins (BMP), BMP receptors, and BMP associated proteins in human trabecular meshwork and optic nerve head cells and tissues. Mol. Vis. 2002, 8:241-250.
98. Wordinger R.J., Clark A.F. Bone morphogenetic proteins and their receptors in the eye. Exp. Biol. Med. (Maywood) 2007, 232(8):979-992.
99. Wordinger R.J., Clark A.F., Agarwal R., Lambert W., McNatt L., Wilson S.E., Qu Z., Fung B.K. Cultured human trabecular meshwork cells express functional growth factor receptors. Invest Ophthalmol. Vis. Sci. 1998, 39(9):1575-1589.
100. Xue W., Wallin R., Olmsted-Davis E.A., Borras T. Matrix GLA protein function in human trabecular meshwork cells: inhibition of BMP2-induced calcification process. Invest Ophthalmol. Vis. Sci. 2006, 47(3):997-1007.
101. Yang Y., Nunes F.A., Berencsi K., Furth E.E., Gonczol E., Wilson J.M. Cellular immunity to viral antigens limits E1-deleted adenoviruses for gene therapy. Proc. Natl. Acad. Sci. U. S. A. 1994, 91(10):4407-4411.
102. Zeng Y., Takada Y., Kjellstrom S., Hiriyanna K., Tanikawa A., Wawrousek E., Smaoui N., Caruso R., Bush R.A., Sieving P.A. RS-1 gene delivery to an adult Rs1h knockout mouse model restores ERG b-wave with reversal of the electronegative waveform of X-linked retinoschisis. Invest Ophthalmol. Vis. Sci. 2004, 45(9):3279-3285.
103. Zhang Y.E. Non-Smad pathways in TGF-beta signaling. Cell. Res. 2009, 19(1):128-139.
104. Zode G.S., Kuehn M.H., Nishimura D.Y., Searby C.C., Mohan K., Grozdanic S.D., Bugge K., Anderson M.G., Clark A.F., Stone E.M., Sheffield V.C. Reduction of ER stress via a chemical chaperone prevents disease phenotypes in a mouse model of primary open angle glaucoma. J. Clin. Invest 2011, 121(9):3542-3553.
105. Zode G.S., Sharma A.B., Lin X., Searby C.C., Bugge K., Kim G.H., Clark A.F., Sheffield V.C. Ocular-specific ER stress reduction rescues glaucoma in murine glucocorticoid-induced glaucoma. J. Clin. Invest 2014, 124(5):1956-1965.