The role of TGF-β2 and bone morphogenetic proteins in the trabecular meshwork and glaucoma

Journal of Ocular Pharmacology and Therapeutics

Volumn 30, Issue 2-3, 2014, Pages 154-162

  Wordinger, Robert J ^a   Sharma, Tasneem ^a   Clark, Abbot F ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 5; BONE MORPHOGENETIC PROTEIN 6; COLLAGEN; CONNECTIVE TISSUE GROWTH FACTOR; FIBRONECTIN; GELATINASE A; GELATINASE B; GLYCOGEN SYNTHASE KINASE 3BETA; LATENCY ASSOCIATED PEPTIDE; LATENT TRANSFORMING GROWTH FACTOR BETA BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE P38; OSTEOGENIC PROTEIN 1; OSTEOGENIN; PLASMIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROCOLLAGEN C PROTEINASE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; PROTEIN SERINE THREONINE KINASE; PROTEOGLYCAN; SMAD2 PROTEIN; SMAD3 PROTEIN; STRESS ACTIVATED PROTEIN KINASE; THROMBOSPONDIN 1; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

AMINO ACID COMPOSITION; APOPTOSIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; EXTRACELLULAR MATRIX; GENE EXPRESSION; HUMAN; LIGAND BINDING; NONHUMAN; OPEN ANGLE GLAUCOMA; PATHOPHYSIOLOGY; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PSEUDOEXFOLIATION; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TARGET CELL; TRABECULAR MESHWORK; ANIMAL; AQUEOUS HUMOR; COMPLICATION; INTRAOCULAR PRESSURE; METABOLISM; PATHOLOGY; PHYSIOLOGY; RISK FACTOR;

ANIMALS; AQUEOUS HUMOR; BONE MORPHOGENETIC PROTEINS; EXTRACELLULAR MATRIX; GLAUCOMA, OPEN-ANGLE; HUMANS; INTRAOCULAR PRESSURE; RISK FACTORS; SIGNAL TRANSDUCTION; TRABECULAR MESHWORK; TRANSFORMING GROWTH FACTOR BETA2;

EID: 84898733409     PISSN: 10807683     EISSN: 15577732     Source Type: Journal    
DOI: 10.1089/jop.2013.0220     Document Type: Review

References (82)

1. Moustakas, A., and Heldin, C.H. Non-Smad TGF-b signals. J. Cell Sci. 118:3573-3584, 2005.
2. Wu, M.Y., and Hill, C.S. TGF-beta superfamily signaling in embryonic development and homeostasis. Dev. Cell. 16: 329-343, 2009.
3. Heldin, C.-H., and Moustakas, A. Role of Smads in TGFb signaling. Cell Tissue Res. 347:21-36, 2012.
4. Ikushima, H., and Miyazono, K. Biology of transforming growth factor-b signaling. Curr. Pharm. Biotechnol. 12: 2099-2107, 2010.
5. Moustakas, A., and Heldin, C.H. The regulation of TGFbeta signal transduction. Development. 136:3699-3714, 2009.
6. Granstein, R.D., Staszewski, R., Knisley, T.L., et al. Aqueous humor contains transforming growth factor-b and a small. J. Immunol (1990) 144, 3021-3027.
7. Jampel, H.D., Roche, N., Stark, W.J., et al. Transforming growth factor-b in human aqueous humor. Curr. Eye Res. 9:963-969, 1990.
8. Cousins, S.W., McCabe, M.M., and Danielpour, D. Identification of transforming growth factor-beta as an immunosuppressive factor in aqueous humor. Invest. Ophthalmol. Vis. Sci. 32:2201-2211, 1991.
9. Zhu, H.J., and Burgess, A.W. Regulation of transforming growth factor-beta signaling. Mol. Cell Biol. Res. Commun. 4:321-330, 2001.
10. Verrecchia, F., and Mauviel, A. Transforming growth factor-beta signaling through the Smad pathway: role in extracellular matrix gene expression and regulation. J. Invest. Dermatol. 118:211-215. 2002.
11. Annes, J.P., Munger, J.S., and Rifkin, D.B. Making sense of TGFbeta activation. J. Cell Sci. 116:217-224, 2003.
12. Sporn, M.B., Roberts, A.B., Wakefield, L.M., and de Crombrugghe, B. Some recent advances in the chemistry and biology of transforming growth factor beta. J. Cell Biol. 105:1039-1045, 1987.
13. Sato, Y., and Rifkin, D.B. Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta-1 like molecule by plasmin during co-culture. J. Cell Biol. 109:309-315, 1989.
14. Schultz-Cherry, S., Lawler, J., Murphy-Ullrich, J.E., et al. The type 1 repeats of thrombospondin-1 activate transforming growth factor-beta. J. Biol. Chem. 269:26783-26788, 1994.
15. Crawford, S.E., Stellmach, V., Murphy-Ullrich, J.E., et al. Thrompospondin-1 is a major activator of TGF-beta1 in vivo. Cell. 93:1159-1170, 1998.
16. Murphy-Ullrich, J.E., and Poczatek, M. Activation of latent TGF-beta by thrombospondin-1: mechanisms and physiology. Cytokine Growth Factor. 11:59-69, 2000.
17. Flugel-Koch, C., Ohlmann, A., Fuchshofer, R., et al. Thrombospondin-1 in the trabecular meshwork: Localization in normal and glaucomatous eyes, and induction by TGF-b1 and dexamethasone in vitro. Exp. Eye Res. 79:649-663, 2004.
18. Fuchshofer, R., Yu, A.H.L., Welge-Lussen, U., et al. Bone morphogenetic protein-7 is an antagonist of transforming growth factor-b2 in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 48:715-726, 2007.
19. Bragdon, B., Moseychuk, O., Saldanha, S., et al. Bone morphogenetic proteins: a critical review. Cell. Signal. 23:609-620, 2011.
20. Wang, E.A., Rosen, V., Cordes, P., et al. Purification and characterization of other distinct bone-inducing factors. Proc. Natl. Acad. Sci. U. S. A. 85:9484-9488, 1988.
21. Balemans, W., and Van Hul, W. Extracellular regulation of BMP signaling in vertebrates: a cocktail of modulators. Dev. Biol. 250:231-250, 2002.
22. Wordinger, R.J., and Clark, A.F. Bone morphogenetic proteins and their receptors in the eye. Exp. Biol. Med. 232: 979-992, 2007.
23. Mazerbourg, S., and Hsueh, A.J. Genomic analyses facilitate identification of receptors and signaling pathways for growth differentiation factor 9 and related orphan bone morphogenetic/growth differentiation factor ligands. Hum. Reprod. Update. 12:373-383, 2006.
24. Von Bubnoff, A., and Cho, C.W. Intracellular BMP signaling regulation in vertebrates: pathway or network. Dev. Biol. 239:1-14, 2001.
25. Ge, G., and Greenspan, D. BMP1 controls TGFbeta1 activation via cleavage of latent TGFbeta-binding protein. J. Cell Biol. 175: 111-120, 2006.
26. Hopkins, D.R., Keles, K., et al. The bone morphogenetic protein 1/Tolloid-like metalloproteinases. Matrix Biol. 26: 508-523, 2007.
27. Xiao, Y.T., Xiang, L.X., and Shao, J.Z. Bone morphogenetic protein. Biochem. Biophys. Res. Commun. 362:550-553, 2007.
28. Sieber, C., Kopf, J., Hiepen, C., et al. Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev. 20:343-355, 2009.
29. Nelsen, S.M., and Christian, J.L. Site specific cleavage of BMP4 by furin, PC6 and PC7. J. Biol. Chem. 284:27157-27166, 2009.
30. Tarasewicz, E., and Jeruss, J.S. Phosphospecific Smad3 signaling: Impact of breast oncogenesis. Cell Cycle. 11: 2443-2451, 2012.
31. Massague, J. TGF-beta signal transduction. Annu. Rev. Biochem. 67:753-791, 1998.
32. Massague, J. How cells read TGF-beta signals. Nat. Rev. Mol. Cell Biol. 1:169-178, 2000.
33. Massague, J., and Chen, Y.G. Controlling TGF-beta signaling. Genes Dev. 14:627-644, 2000.
34. Flanders, K.C. Smad3 as a mediator of the fibrotic response. Int. J. Exp. Pathol. 85:47-64, 2004.
35. Roberts, A.B., Russo, A., Felici, A., et al. Smad3: a key player in pathogenetic mechanisms dependent on TGFbeta. Ann. N. Y. Acad. Sci. 995:1-10, 2003.
36. Ihn, H. Pathogenesis of fibrosis: Role of TGF-b and CTGF. Curr. Opin. Rheumatol. 14:681-685, 2002.
37. Leask, A., and Abraham, D.J. TGF-beta signaling and the fibrotic response. FASEB J. 18:816-827, 2004.
38. Tomarev, S.I., Wistow, G., Raymond, V., et al. Gene expression profile of the human trabecular meshwork: NEIBank sequence tag analysis. Invest. Ophthalmol. Vis. Sci. 44:2588-2596, 2003.
39. Van Setten, G.B., Blalock, T.D., Grotendorst, G., et al. Detection of connective tissue growth factor in human aqueous humor. Ophthalmic Res. 34:306-308, 2002.
40. Junglas, B., Yu, A.H., Welge-Lussen, U., et al. Connective tissue growth factor induces extracellular matrix deposition in human trabecular meshwork cells. Exp. Eye Res. 88: 1065-1075, 2009.
41. Nohe, A., Keating, E., Knaus, P., et al. Signal transduction of bone morphogenetic protein receptors. Cell Signal. 16: 291-203, 2004.
42. Cheifetz, S., Weatherbee, J.A., Tsang, M.L., et al. The transforming growth factor-beta system, a complex pattern of cross-reactive ligand and receptors. Cell. 48:409-415, 1987.
43. Gilboa, L., Nohe, A., Geissendorfer, T., et al. Bone morphogenetic protein receptor complexes on the surface of live cells: A new oligomerization mode for serine/threonine kinase receptors. Mol. Biol. Cell. 11:1023-1035, 2000.
44. Miyazono, K., Maeda, S., and Imamura, T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 16:251-263, 2005.
45. Yanagita, M. BMP antagonists: their roles in development and involvement in pathophysiology. Cytokine Growth Factor Rev. 16:309-317, 2005.
46. Onichtchouk, D., Chen, Y.G., Dosch, R., et al. Silencing TGF-beta signaling by the pseudoreceptor BAMBI. Nature. 401:480-485, 1999.
47. Matsuura, J., Denissova, N.G., Wang, G., et al. Cyclindependent kinases regulate the antiproliferative function of Smads. Nature. 430:226-231, 2004.
48. Kamaraju, A.K., and Roberts, A.B. Role of the Rho/ROCK and p38 MAP kinase pathways in transforming growth factor-b medicated Smad-dependent growth inhibition of human breast carcinoma cells in vivo. J. Biol. Chem. 280:1024-1036, 2005.
49. Mori, S., Matsuzaki, K., Yoshida, K., et al. TGF-b and HGF transmit the signals through JNK-dependent Smad2/3 phosphorylation at the linker regions. Oncogene. 23:7416-7429, 2004.
50. Kass, M.A., Heuer, D.K., Higginbotham, E.J., et al. The Ocular Hypertension Treatment Study: a randomized trial determines that topical ocular hypertensive medication delays or prevents the onset of primary open-angle glaucoma. Arch. Ophthalmol. 120:701-713, 2002.
51. Heijl, A., Leske, M.C., Bengtsson, B., et al., Reduction of intraocular pressure and glaucoma progression: results from the early manifest glaucoma trial. Arch. Ophthalmol. 120:1268-1279, 2002.
52. Wordinger, R.J., Clark, A.F., Agarwal, R., et al. Cultured human trabecularmeshwork cells express functional growth factor receptors. Invest. Ophthalmol. Vis. Sci. 39:1575-1589, 1998.
53. Fuchshofer, R., and Tamm, E.R. Modulation of extracellular matrix turnover in the trabecular meshwork. Exp. Eye Res. 88:683-688, 2009.
54. Prendes, M.A., Harris, A., Wirostko, B.M., et al. The role of transforming growth factor b in glaucoma and the therapeutic implications. Br. J. Ophthalmol. 97:680-686, 2013.
55. Min, S.H., Lee, T.I., Chung, Y.S., et al. Transforming growth factor-beta levels in human aqueous humor of glaucomatous, diabetic and uveitic eyes. Korean J. Ophthalmol. 20:162-165, 2006.
56. Tovar-Vidales, T., Roque, R., Clark, A.F., et al. Tissue transglutaminase expression and activity in normal and glaucomatous human trabecular meshwork cells and tissues. Invest. Ophthalmol. Vis. Sci. 49:622-628, 2008.
57. Gottanka, J., Chan, D., Eichhorn, M., et al. Effects of TGFbeta2 in perfused human eyes. Invest. Ophthalmol. Vis. Sci. 45:153-158, 2004.
58. Fleenor, D.L., Shepard, A.R., Hellberg, P.E., et al. TGFb2-induced changes in human trabecular meshwork: Implications for intraocular pressure. Invest. Ophthalmol. Vis. Sci. 47:226-234, 2006.
59. Shepard, A.R., Millar, J.C., Pang, I.H., et al. 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. 51: 2067-2076, 2010.
60. Last, J.A., Pan, T., Ding, Y., et al. Elastic modulus determination of normal and glaucomatous human trabecular meshwork. Invest. Ophthalmol. Vis. Sci. 52:2147-2152, 2011.
61. Sethi, A., Mao, W., Wordinger, R.J., et al. Transforming growth factor-beta induces extracellular matrix protein cross-linking lysyl oxidase (LOX) genes in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 52:5240-5250, 2011.
62. Tovar-Vidales, T., Clark, A.F., and 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. 93:442-451, 2011.
63. Ritch, R., and Schlotzer-Schrehardt, U. Exfoliation syndrome. Surv. Ophthalmol. 45:265-315, 2001.
64. Schlotzer-Schrehardt, U., and Naumann, G.O. Ocular and systemic pseudoexfoliation syndrome. Am. J. Ophthalmol. 141:921-937, 2006.
65. Ritch, R., and Schlotzer-Schrehardt, U. Exfoliation (pseudoexfoliation) syndrome: Towards a new understanding. Acta Ophthalmol. Scand. 79:213-217, 2001.
66. Schlotzer-Schrehardt, U., Zenkel, M., Kuchle, M., et al. Role of transforming growth factor-beta1 and its latent form binding protein in pseudoexfoliation syndrome. Exp. Eye Res. 73:765-780, 2001.
67. Decitre, M., Gleyzal, C., Raccurt, M., et al. Lysyl oxidaselike protein localizes to sites of de novo fibrin genesis in fibrosis and in the early stromal reaction of ductal breast carcinomas. Lab. Invest. 78:143-151, 1998.
68. Liu, X., Zhao, Y., Gao, J., et al. Elastic fiber homeostasis requires lysyl oxidase-like 1 protein. Nat. Genet. 36:178-182, 2004.
69. Elhawy, E., Kamthan, G., Dong, C.Q., et al. Pseudoexfoliation syndrome, a systemic disorder with ocular manifestations. Hum. Genomics. 6:22-32, 2012.
70. Maruhashi, T., Kii, I., Saito, M., et al. Interaction between periostin and BMP-1 promotes proteolytic activation of lysyl oxidase. J. Biol. Chem. 285:13294-13303, 2010.
71. Tovar-Vidales, T., Fitzgerald, A.M., Clark, A.F., et al. Transforming growth factor-b2 induces expression of biologically active bone morphogenetic protein-1 in human trabecular meshwork cells. Invest. Ophthalmol. Vis. Sci. 54:4741-4748, 2013.
72. Wordinger, R.J., Fleenor, D.L., Hellberg, P.E., et al. Effects of TGF-beta2, BMP-4 and gremlin in the trabecular meshwork: implications for glaucoma. Invest. Ophthalmol. Vis. Sci. 48:1191-1200, 2007.
73. Wordinger, R., Agarwal, R., Talati, M., et al. Expression of bone morphogenetic proteins (BMP),BMPreceptors, andBMP associated proteins in human trabecular meshwork and optic nerve heads cells and tissues. Mol. Vis. 15:241-250, 2002.
74. Fuchshofer, R., Stephan, D.A., Russell, P., et al. Gene expression profiling ofTGFb2-and/orBMP-7-treated trabecular meshwork cell: Identification of Smad7 as a critical inhibitor of TGF-b2 signaling. Exp. Eye Res. 88:1020-1032, 2009.
75. Park, S.H. Fine tuning and cross-talking of TGF-beta signal by inhibitory Smads. J. Biochem. Mol. Biol. 38:9-16, 2005.
76. Shimmi, O., and Neufeld, S.J. New insights into extracellular and post-translational regulation of TGF-b family signaling pathways. J. Biochem. 154:11-19, 2013.
77. Shimasaki, S., Moore, R.K., Otsuka, F., et al. The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25:72-101, 2004.
78. Sethi, A., Wordinger, R.J., and Clark, A.F. Gremlin utilizes canonical and non-canonical TGFb signaling to induce lysyl oxidase (LOX) genes in human trabecular meshwork cells. Exp. Eye Res. 113:117-127, 2013.
79. Shimasaki, S., Koga, M., Esch, F., et al. Primary structure of the human follistatin precursor and its genomic organization. Proc. Natl. Acad. Sci. U. S. A. 85:4218-4222, 1988.
80. Lin, S.Y., Morrison, J.R., Phillips, D.J., et al. Regulation of ovarian function by the TGF-beta superfamily and follistatin. Reproduction. 126:133-148, 2003.
81. Fitzgerald, A.M., Benz, C., Clark, A.F., et al. The effects of transforming growth factor-b2 on the expression of follistatin and activin A in normal and glaucomatous human trabecular meshwork cells and tissues. Invest. Ophthalmol. Vis. Sci. 53:7358-7369, 2012.
82. Agnihotri, N., Kumar, S., and Mehta, K. Tissue transglutaminase as a central mediator in inflammation-induced progression of breast cancer. Breast Cancer Res. 15:202-208, 2013.