Rhoa gtpase-induced ocular hypertension in a rodent model is associated with increased fibrogenic activity in the trabecular meshwork

American Journal of Pathology

Volumn 185, Issue 2, 2015, Pages 496-512

  Pattabiraman, Padmanabhan P ^a   Rinkoski, Tommy ^c   Poeschla, Eric ^c   Proia, Alan ^b   Challa, Pratap ^a   Rao, Ponugoti V ^a,b  

^a DUKE UNIVERSITY EYE CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; COLLAGEN; COLLAGEN TYPE 1; F ACTIN; LENTIVIRUS VECTOR; MYOSIN LIGHT CHAIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; EYE PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA PROTEIN, HUMAN;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME INHIBITION; FIBROGENESIS; HUMAN; HUMAN CELL; INTRAOCULAR HYPERTENSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; TRABECULAR MESHWORK; AMINO ACID SUBSTITUTION; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; ENZYMOLOGY; FEMALE; GENETICS; METABOLISM; MISSENSE MUTATION; OCULAR HYPERTENSION; PATHOLOGY; SPRAGUE DAWLEY RAT;

AMINO ACID SUBSTITUTION; ANIMALS; COLLAGEN; EYE PROTEINS; FEMALE; HUMANS; MUTATION, MISSENSE; OCULAR HYPERTENSION; RATS; RATS, SPRAGUE-DAWLEY; RHOA GTP-BINDING PROTEIN; TRABECULAR MESHWORK;

EID: 84922311604     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.10.023     Document Type: Article

References (69)

1. Quigley HA, Broman AT: The number of people with glaucoma worldwide in 2010 and 2020. Br J Ophthalmol 2006, 90:262-267
2. Weinreb RN, Khaw PT: Primary open-angle glaucoma. Lancet 2004, 363:1711-1720
3. Kwon YH, Fingert JH, Kuehn MH, Alward WL: Primary open-angle glaucoma. N Engl J Med 2009, 360:1113-1124
4. Kass MA, Heuer DK, Higginbotham EJ, Johnson CA, Keltner JL, Miller JP, Parrish RK 2nd, Wilson MR, Gordon MO: 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. discussion 829-30
5. 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: 429-440
6. Lee AJ, Goldberg I: Emerging drugs for ocular hypertension. Expert Opin Emerg Drugs 2011, 16:137-161
7. Gabelt BT, Kaufman PL: Changes in aqueous humor dynamics with age and glaucoma. Prog Retin Eye Res 2005, 24:612-637
8. Tamm ER, Fuchshofer R: What increases outflow resistance in primary open-angle glaucoma? Surv Ophthalmol 2007, 52(Suppl 2): S101-S104
9. Johnson M: 'What controls aqueous humour outflow resistance?'. Exp Eye Res 2006, 82:545-557
10. Lutjen-Drecoll E: Functional morphology of the trabecular meshwork in primate eyes. Prog Retin Eye Res 1999, 18:91-119
11. Clark AF, Wordinger RJ: The role of steroids in outflow resistance. Exp Eye Res 2009, 88:752-759
12. Acott TS, Kelley MJ: Extracellular matrix in the trabecular meshwork. Exp Eye Res 2008, 86:543-561
13. Yue BY: The extracellular matrix and its modulation in the trabecular meshwork. Surv Ophthalmol 1996, 40:379-390
14. Lutjen-Drecoll E, Shimizu T, Rohrbach M, Rohen JW: Quantitative analysis of 'plaque material' in the inner- and outer wall of Schlemm's canal in normal- and glaucomatous eyes. Exp Eye Res 1986, 42:443-455
15. Tektas OY, Lutjen-Drecoll E: Structural changes of the trabecular meshwork in different kinds of glaucoma. Exp Eye Res 2009, 88: 769-775
16. Last JA, Pan T, Ding Y, Reilly CM, Keller K, Acott TS, Fautsch MP, Murphy CJ, Russell P: Elastic modulus determination of normal and glaucomatous human trabecular meshwork. Invest Ophthalmol Vis Sci 2011, 52:2147-2152
17. Zhou EH, Krishnan R, Stamer WD, Perkumas KM, Rajendran K, Nabhan JF, Lu Q, Fredberg JJ, Johnson M: Mechanical responsiveness of the endothelial cell of Schlemm's canal: scope, variability and its potential role in controlling aqueous humour outflow. J R Soc Interface 2012, 9:1144-1155
18. Keller KE, Aga M, Bradley JM, Kelley MJ, Acott TS: Extracellular matrix turnover and outflow resistance. Exp Eye Res 2009, 88:676-682
19. Mettu PS, Deng PF, Misra UK, Gawdi G, Epstein DL, Rao PV: Role of lysophospholipid growth factors in the modulation of aqueous humor outflow facility. Invest Ophthalmol Vis Sci 2004, 45:2263-2271
20. Rao PV, Deng P, Sasaki Y, Epstein DL: Regulation of myosin light chain phosphorylation in the trabecular meshwork: role in aqueous humour outflow facility. Exp Eye Res 2005, 80:197-206
21. Pattabiraman PP, Rao PV: Mechanistic basis of Rho GTPase-induced extracellular matrix synthesis in trabecular meshwork cells. Am J Physiol Cell Physiol 2010, 298:C749-C763
22. Iyer P, Maddala R, Pattabiraman PP, Rao PV: Connective tissue growth factor-mediated upregulation of neuromedin U expression in trabecular meshwork cells and its role in homeostasis of aqueous humor outflow. Invest Ophthalmol Vis Sci 2012, 53:4952-4962
23. Junglas B, Kuespert S, Seleem AA, Struller T, Ullmann S, Bösl M, Bosserhoff A, Köstler J, Wagner R, Tamm ER, Fuchshofer R: Connective tissue growth factor causes glaucoma by modifying the actin cytoskeleton of the trabecular meshwork. Am J Pathol 2012, 180:2386-2403
24. Iyer P, Lalane R 3rd, Morris C, Challa P, Vann R, Rao PV: Autotaxin-lysophosphatidic acid axis is a novel molecular target for lowering intraocular pressure. PLoS One 2012, 7:e42627
25. Browne JG, Ho SL, Kane R, Oliver N, Clark AF, O'Brien CJ, Crean JK: Connective tissue growth factor is increased in pseudoexfoliation glaucoma. Invest Ophthalmol Vis Sci 2011, 52:3660-3666
26. Wiederholt M, Thieme H, Stumpff F: The regulation of trabecular meshwork and ciliary muscle contractility. Prog Retin Eye Res 2000, 19:271-295
27. Tripathi RC, Li J, Chan WF, Tripathi BJ: Aqueous humor in glaucomatous eyes contains an increased level of TGF-beta 2. Exp Eye Res 1994, 59:723-727
28. Rao VP, Epstein DL: Rho GTPase/Rho kinase inhibition as a novel target for the treatment of glaucoma. BioDrugs 2007, 21:167-177
29. 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
30. Pattabiraman PP, Maddala R, Rao PV: Regulation of plasticity and fibrogenic activity of trabecular meshwork cells by Rho GTPase signaling. J Cell Physiol 2014, 229:927-942
31. Tsou PS, Haak AJ, Khanna D, Neubig RR: Cellular mechanisms of tissue fibrosis. 8. Current and future drug targets in fibrosis: focusing on Rho GTPase regulated gene transcription. Am J Physiol Cell Physiol 2014, 307:C2-C13
32. Goldhagen B, Proia AD, Epstein DL, Rao PV: Elevated levels of RhoA in the optic nerve head of human eyes with glaucoma. J Glaucoma 2012, 21:530-538
33. Lukas TJ, Miao H, Chen L, Riordan SM, Li W, Crabb AM, Wise A, Du P, Lin SM, Hernandez MR: Susceptibility to glaucoma: differential comparison of the astrocyte transcriptome from glaucomatous African American and Caucasian American donors. Genome Biol 2008, 9:R111
34. Amin E, Dubey BN, Zhang SC, Gremer L, Dvorsky R, Moll JM, Taha MS, Nagel-Steger L, Piekorz RP, Somlyo AV, Ahmadian MR: Rho-kinase: regulation, (dys)function, and inhibition. Biol Chem 2013, 394:1399-1410
35. Rath N, Olson MF: Rho-associated kinases in tumorigenesis: reconsidering ROCK inhibition for cancer therapy. EMBO Rep 2012, 13:900-908
36. Satoh K, Fukumoto Y, Shimokawa H: Rho-kinase: important new therapeutic target in cardiovascular diseases. Am J Physiol Heart Circ Physiol 2011, 301:H287-H296
37. de Godoy MA, Rattan S: Role of rho kinase in the functional and dysfunctional tonic smooth muscles. Trends Pharmacol Sci 2011, 32: 384-393
38. Loirand G, Pacaud P: The role of Rho protein signaling in hypertension. Nat Rev Cardiol 2010, 7:637-647
39. Uehata M, Ishizaki T, Satoh H, Ono T, Kawahara T, Morishita T, Tamakawa H, Yamagami K, Inui J, Maekawa M, Narumiya S: Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 1997, 389:990-994
40. Fukata Y, Amano M, Kaibuchi K: Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of nonmuscle cells. Trends Pharmacol Sci 2001, 22:32-39
41. Etienne-Manneville S, Hall A: Rho GTPases in cell biology. Nature 2002, 420:629-635
42. Heasman SJ, Ridley AJ: Mammalian RhoGTPases: newinsights into their functions from in vivo studies. Nat Rev Mol Cell Biol 2008, 9:690-701
43. Amano M, Nakayama M, Kaibuchi K: Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskeleton (Hoboken) 2010, 67:545-554
44. Honjo M, Tanihara H, Inatani M, Kido N, Sawamura T, Yue BY, Narumiya S, Honda Y: Effects of rho-associated protein kinase inhibitor Y-27632 on intraocular pressure and outflow facility. Invest Ophthalmol Vis Sci 2001, 42:137-144
45. Rao PV, Deng PF, Kumar J, Epstein DL: Modulation of aqueous humor outflow facility by the Rho kinase-specific inhibitor Y-27632. Invest Ophthalmol Vis Sci 2001, 42:1029-1037
46. Williams RD, Novack GD, van Haarlem T, Kopczynski C; AR-12286 Phase 2A Study Group: Ocular hypotensive effect of the Rho kinase inhibitor AR-12286 in patients with glaucoma and ocular hypertension. Am J Ophthalmol 2011, 152:834-841.e1
47. Rao PV, Deng P, Maddala R, Epstein DL, Li CY, Shimokawa H: Expression of dominant negative Rho-binding domain of Rho-kinase in organ cultured human eye anterior segments increases aqueous humor outflow. Mol Vis 2005, 11:288-297
48. Tanihara H, Inatani M, Honjo M, Tokushige H, Azuma J, Araie M: Intraocular pressure-lowering effects and safety of topical administration of a selective ROCK inhibitor, SNJ-1656, in healthy volunteers. Arch Ophthalmol 2008, 126:309-315
49. Lu Z, Overby DR, Scott PA, Freddo TF, Gong H: The mechanism of increasing outflow facility by rho-kinase inhibition with Y-27632 in bovine eyes. Exp Eye Res 2008, 86:271-281
50. Tian B, Kaufman PL: Effects of the Rho kinase inhibitor Y-27632 and the phosphatase inhibitor calyculin A on outflow facility in monkeys. Exp Eye Res 2005, 80:215-225
51. Tanihara H, Inoue T, Yamamoto T, Kuwayama Y, Abe H, Araie M; K-115 Clinical Study Group: Phase 2 randomized clinical study of a Rho kinase inhibitor, K-115, in primary open-angle glaucoma and ocular hypertension. Am J Ophthalmol 2013, 156:731-736
52. Llano M, Saenz DT, Meehan A, Wongthida P, Peretz M, Walker WH, Teo W, Poeschla EM: An essential role for LEDGF/p75 in HIV integration. Science 2006, 314:461-464
53. Loewen N, Poeschla EM: Lentiviral vectors. Adv Biochem Eng Biotechnol 2005, 99:169-191
54. Maddala R, Skiba NP, Lalane R 3rd, Sherman DL, Brophy PJ, Rao PV: Periaxin is required for hexagonal geometry and membrane organization of mature lens fibers. Dev Biol 2011, 357:179-190
55. Junqueira LC, Bignolas G, Brentani RR: Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 1979, 11:447-455
56. Moore CG, Johnson EC, Morrison JC: Circadian rhythm of intraocular pressure in the rat. Curr Eye Res 1996, 15:185-191
57. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A: Physiology of microglia. Physiol Rev 2011, 91:461-553
58. Zhou Y, Huang X, Hecker L, Kurundkar D, Kurundkar A, Liu H, Jin TH, Desai L, Bernard K, Thannickal VJ: Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J Clin Invest 2013, 123:1096-1108
59. Saito A: EMT and EndMT: regulated in similar ways? J Biochem 2013, 153:493-495
60. Geng H, Lan R, Singha PK, Gilchrist A, Weinreb PH, Violette SM, Weinberg JM, Saikumar P, Venkatachalam MA: Lysophosphatidic acid increases proximal tubule cell secretion of profibrotic cytokines PDGF-B and CTGF through LPA2- and Galphaq-mediated Rho and alphavbeta6 integrin-dependent activation of TGF-beta. Am J Pathol 2012, 181:1236-1249
61. Morita T, Mayanagi T, Sobue K: Dual roles of myocardin-related transcription factors in epithelial mesenchymal transition via slug induction and actin remodeling. J Cell Biol 2007, 179:1027-1042
62. Tumbarello DA, Turner CE: Hic-5 contributes to epithelialmesenchymal transformation through a RhoA/ROCK-dependent pathway. J Cell Physiol 2007, 211:736-747
63. Masszi A, Di Ciano C, Sirokmany G, Arthur WT, Rotstein OD, Wang J, McCulloch CA, Rosivall L, Mucsi I, Kapus A: Central role for Rho in TGF-beta1-induced alpha-smooth muscle actin expression during epithelial-mesenchymal transition. Am J Physiol Renal Physiol 2003, 284:F911-F924
64. Klein S, Van Beuge MM, Granzow M, Beljaars L, Schierwagen R, Kilic S, Heidari I, Huss S, Sauerbruch T, Poelstra K, Trebicka J: HSCspecific inhibition of Rho-kinase reduces portal pressure in cirrhotic rats without major systemic effects. J Hepatol 2012, 57:1220-1227
65. van Beuge MM, Prakash J, Lacombe M, Gosens R, Post E, Reker-Smit C, Beljaars L, Poelstra K: Reduction of fibrogenesis by selective delivery of a Rho kinase inhibitor to hepatic stellate cells in mice. J Pharmacol Exp Ther 2011, 337:628-635
66. Young RP, Hopkins R, Eaton TE: Pharmacological actions of statins: potential utility in COPD. Eur Respir Rev 2009, 18:222-232
67. Fried LF: Effects of HMG-CoA reductase inhibitors (statins) on progression of kidney disease. Kidney Int 2008, 74:571-576
68. Moriyama T, Nagatoya K: The Rho-ROCK system as a new therapeutic target for preventing interstitial fibrosis. Drug News Perspect 2004, 17:29-34
69. Gottanka J, Chan D, Eichhorn M, Lutjen-Drecoll E, Ethier CR: Effects of TGF-beta2 in perfused human eyes. Invest Ophthalmol Vis Sci 2004, 45:153-158