Elevated intraocular pressure induces Rho GTPase mediated contractile signaling in the trabecular meshwork

Experimental Eye Research

Volumn 136, Issue , 2015, Pages 29-33

  Pattabiraman, Padmanabhan P ^a   Inoue, Toshihiro ^a,c   Rao, P Vasantha ^a,b  

^a DUKE UNIVERSITY EYE CENTER   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Intraocular pressure; Mechanotransduction; Outflow resistance; Rho GTPase; Trabecular meshwork

Indexed keywords

MARCKS PROTEIN; MYOSIN II; MYOSIN LIGHT CHAIN; MYOSIN PHOSPHATASE TARGET SUBSTRATE 1; PAXILLIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO KINASE; UNCLASSIFIED DRUG; MEMBRANE PROTEIN; MYOSIN LIGHT CHAIN PHOSPHATASE; MYRISTOYLATED ALANINE-RICH C KINASE SUBSTRATE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SIGNAL PEPTIDE;

ACTIN FILAMENT; ANIMAL TISSUE; AQUEOUS HUMOR; AQUEOUS HUMOR OUTFLOW; ARTICLE; CONTROLLED STUDY; ENUCLEATION; ENZYME ACTIVATION; EXPERIMENTAL PIG; FOCAL ADHESION; INTRAOCULAR HYPERTENSION; INTRAOCULAR PRESSURE; MECHANOTRANSDUCTION; NONHUMAN; OPEN ANGLE GLAUCOMA; PERFUSION PRESSURE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRABECULAR MESHWORK; ANIMAL; METABOLISM; PHYSIOLOGY; PIG; SECRETION (PROCESS);

ANIMALS; AQUEOUS HUMOR; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRAOCULAR PRESSURE; MECHANOTRANSDUCTION, CELLULAR; MEMBRANE PROTEINS; MYOSIN LIGHT CHAINS; MYOSIN-LIGHT-CHAIN PHOSPHATASE; OCULAR HYPERTENSION; PAXILLIN; RHOA GTP-BINDING PROTEIN; SWINE; TRABECULAR MESHWORK;

EID: 84929173785     PISSN: 00144835     EISSN: 10960007     Source Type: Journal    
DOI: 10.1016/j.exer.2015.05.001     Document Type: Article

References (44)

1. Acott T.S., Kelley M.J., Keller K.E., Vranka J.A., Abu-Hassan D.W., Li X., Aga M., Bradley J.M. Intraocular pressure homeostasis: maintaining balance in a high-pressure environment. J.Ocular Pharmacol. Ther.: Off. J. Assoc. Ocular Pharmacol. Ther. 2014, 30:94-101.
2. Aderem A. The MARCKS family of protein kinase-C substrates. Biochem. Soc. Trans. 1995, 23:587-591.
3. Arbuzova A., Schmitz A.A., Vergeres G. Cross-talk unfolded: MARCKS proteins. Biochem. J. 2002, 362:1-12.
4. Battista S.A., Lu Z., Hofmann S., Freddo T., Overby D.R., Gong H. Reduction of the available area for aqueous humor outflow and increase in meshwork herniations into collector channels following acute IOP elevation in bovine eyes. Invest. Ophthalmol. Vis. Sci. 2008, 49:5346-5352.
5. Becker B., Constant M.A. The facility of aqueous outflow; a comparison of tonography and perfusion measurements invivo and invitro. AMA Arch. Ophthalmol. 1956, 55:305-312.
6. Boopathi E., Gomes C., Zderic S.A., Malkowicz B., Chakrabarti R., Patel D.P., Wein A.J., Chacko S. Mechanical stretch upregulates proteins involved in Ca2+ sensitization in urinary bladder smooth muscle hypertrophy. Am. J. Physiol. Cell Physiol. 2014, 307:C542-C553.
7. Borras T. Gene expression in the trabecular meshwork and the influence of intraocular pressure. Prog. Retin Eye Res. 2003, 22:435-463.
8. Brubaker R.F. The effect of intraocular pressure on conventional outflow resistance in the enucleated human eye. Invest. Ophthalmol. 1975, 14:286-292.
9. Chiquet M., Gelman L., Lutz R., Maier S. From mechanotransduction to extracellular matrix gene expression in fibroblasts. Biochim. Biophys. Acta 2009, 1793:911-920.
10. Dai Y., Lindsey J.D., Duong-Polk X., Nguyen D., Hofer A., Weinreb R.N. Outflow facility in mice with a targeted type I collagen mutation. Invest. Ophthalmol. Vis. Sci. 2009, 50:5749-5753.
11. Deakin N.O., Turner C.E. Paxillin comes of age. J.Cell Sci. 2008, 121:2435-2444.
12. Epstein D.L., Rowlette L.L., Roberts B.C. Acto-myosin drug effects and aqueous outflow function. Invest. Ophthalmol. Vis. Sci. 1999, 40:74-81.
13. Fukata Y., Amano M., Kaibuchi K. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 2001, 22:32-39.
14. Gabelt B.T., Kaufman P.L. Changes in aqueous humor dynamics with age and glaucoma. Prog. Retin Eye Res. 2005, 24:612-637.
15. Goldmann W.H. Mechanosensation: a basic cellular process. Prog. Mol. Biol. Transl. Sci. 2014, 126:75-102.
16. Hashimoto J.M., Epstein D.L. Influence of intraocular pressure on aqueous outflow facility in enucleated eyes of different mammals. Invest. Ophthalmol. Vis. Sci. 1980, 19:1483-1489.
17. Higashida C., Kiuchi T., Akiba Y., Mizuno H., Maruoka M., Narumiya S., Mizuno K., Watanabe N. F- and G-actin homeostasis regulates mechanosensitive actin nucleation by formins. Nat. Cell Biol. 2013, 15:395-405.
18. Huang X., Yang N., Fiore V.F., Barker T.H., Sun Y., Morris S.W., Ding Q., Thannickal V.J., Zhou Y. Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction. Am. J. Respir. Cell Mol. Biol. 2012, 47:340-348.
19. Inoue T., Tanihara H. Rho-associated kinase inhibitors: a novel glaucoma therapy. Prog. Retin Eye Res. 2013, 37:1-12.
20. 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, 180:2386-2403.
21. Kwon Y.H., Fingert J.H., Kuehn M.H., Alward W.L. Primary open-angle glaucoma. N.Engl. J. Med. 2009, 360:1113-1124.
22. Lee A.J., Goldberg I. Emerging drugs for ocular hypertension. Expert Opin. Emerg. Drugs 2011, 16:137-161.
23. Mammoto A., Mammoto T., Ingber D.E. Rho signaling and mechanical control of vascular development. Curr. Opin. Hematol. 2008, 15:228-234.
24. Mattias L., Haque A., Adnan N., Akaike T. The effects of artificial E-cadherin matrix-induced embryonic stem cell scattering on paxillin and RhoA activation via alpha-catenin. Biomaterials 2014, 35:1797-1806.
25. Nagumo H., Ikenoya M., Sakurada K., Furuya K., Ikuhara T., Hiraoka H., Sasaki Y. Rho-associated kinase phosphorylates MARCKS in human neuronal cells. Biochem. Biophys. Res. Commun. 2001, 280:605-609.
26. Pattabiraman P.P., Maddala R., Rao P.V. Regulation of plasticity and fibrogenic activity of trabecular meshwork cells by Rho GTPase signaling. J Cell Physiol. 2014 Jul, 229(7):927-942.
27. Pattabiraman P.P., Rao P.V. Mechanistic basis of Rho GTPase-induced extracellular matrix synthesis in trabecular meshwork cells. Am. J. Physiol. Cell Physiol. 2010, 298:C749-C763.
28. Pattabiraman P.P., Rinkoski T., Poeschla E., Proia A., Challa P., Rao P.V. RhoA GTPase-induced ocular hypertension in a rodent model is associated with increased fibrogenic activity in the trabecular meshwork. Am. J. Pathol. 2015 Feb, 185(2):496-512.
29. Provenzano P.P., Keely P.J. Mechanical signaling through the cytoskeleton regulates cell proliferation by coordinated focal adhesion and Rho GTPase signaling. J.Cell Sci. 2011, 124:1195-1205.
30. Quigley H.A. Open-angle glaucoma. N.Engl. J. Med. 1993, 328:1097-1106.
31. Rao P.V., Deng P.F., Kumar J., Epstein D.L. Modulation of aqueous humor outflow facility by the Rho kinase-specific inhibitor Y-27632. Invest. Ophthalmol. Vis. Sci. 2001, 42:1029-1037.
32. Schwarz U.S., Erdmann T., Bischofs I.B. Focal adhesions as mechanosensors: the two-spring model. Bio Syst. 2006, 83:225-232.
33. Shemesh T., Geiger B., Bershadsky A.D., Kozlov M.M. Focal adhesions as mechanosensors: a physical mechanism. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:12383-12388.
34. Somlyo A.P., Somlyo A.V. Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol. Rev. 2003, 83:1325-1358.
35. Stamer W.D., Acott T.S. Current understanding of conventional outflow dysfunction in glaucoma. Curr. Opin. Ophthalmol. 2012, 23:135-143.
36. Stamer W.D., Braakman S.T., Zhou E.H., Ethier C.R., Fredberg J.J., Overby D.R., Johnson M. Biomechanics of Schlemm's canal endothelium and intraocular pressure reduction. Prog. Retin Eye Res. 2015, 44C:86-98.
37. Tan H., Biechler S., Junor L., Yost M.J., Dean D., Li J., Potts J.D., Goodwin R.L. Fluid flow forces and rhoA regulate fibrous development of the atrioventricular valves. Dev. Biol. 2013, 374:345-356.
38. Turner C.E. Paxillin and focal adhesion signalling. Nat. Cell Biol. 2000, 2:E231-E236.
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. Weinreb R.N., Khaw P.T. Primary open-angle glaucoma. Lancet 2004, 363:1711-1720.
41. Williams R.D., Novack G.D., van Haarlem T., Kopczynski C., Group A.R.P.A.S. Ocular hypotensive effect of the Rho kinase inhibitor AR-12286 in patients with glaucoma and ocular hypertension. Am. J. Ophthalmol. 2011, 152:834-841. e831.
42. Zhang M., Maddala R., Rao P.V. 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. Zhao X.H., Laschinger C., Arora P., Szaszi K., Kapus A., McCulloch C.A. Force activates smooth muscle alpha-actin promoter activity through the Rho signaling pathway. J.Cell Sci. 2007, 120:1801-1809.
44. Zhou Y., Huang X., Hecker L., Kurundkar D., Kurundkar A., Liu H., Jin T.H., Desai L., Bernard K., Thannickal V.J. Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J.Clin. Invest. 2013, 123:1096-1108.