Role of the RhoA/Rho-kinase pathway in the regulation of pulmonary vasoconstrictor function

Canadian Journal of Physiology and Pharmacology

Volumn 88, Issue 1, 2010, Pages 1-8

  Nossaman, Bobby D ^a,b   Nossaman, Vaughn E ^b   Murthy, Subramanyam N ^b   Kadowitz, Philip J ^b  

^a OCHSNER MEDICAL CENTER   (United States)

^b TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cardiovascular diseases; Fasudil; HA 1077; Inhibitors pharmacology; Intracellular signaling; Muscle; Peptides and proteins; Protein kinases; Pulmonary hypertension; Pulmonary vascular bed; RhoA Rho kinase pathway; Signal transduction; Smooth; Systemic vascular bed; Vascular; Y 27632

Indexed keywords

1,4 DIHYDRO 2,6 DIMETHYL 5 NITRO 4 [2 (TRIFLUOROMETHYL)PHENYL] 3 PYRIDINECARBOXYLIC ACID METHYL ESTER; 15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; 4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; FASUDIL; HYDROXYFASUDIL; ISRADIPINE; N(G) NITROARGININE METHYL ESTER; RHO KINASE; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN;

BLOOD VESSEL TONE; CALCIUM TRANSPORT; CARDIOVASCULAR DISEASE; CORONARY BLOOD VESSEL; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; INFLAMMATION; LUNG ARTERY PRESSURE; LUNG FUNCTION; LUNG VASOCONSTRICTION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; RESTENOSIS; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CONTRACTION; VASODILATATION;

ANIMALS; HUMANS; PULMONARY ARTERY; PULMONARY VEINS; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; VASOCONSTRICTION;

EID: 76149093554     PISSN: 00084212     EISSN: None     Source Type: Journal    
DOI: 10.1139/Y09-092     Document Type: Review

References (53)

1. Abe, K., Shimokawa, H., Morikawa, K., Uwatoku, T., Oi, K., Matsumoto, Y., et al. 2004. Long-term treatment with a Rho-kinase inhibitor improves monocrotaline-induced fatal pulmonary hypertension in rats. Circ. Res. 94(3): 385-393. doi:10.1161/01. RES.00001118.34509.94. PMID:14670839.
2. Abe, K., Tawara, S., Oi, K., Hizume, T., Uwatoku, T., Fukumoto, Y., et al. 2006. Long-term inhibition of Rho-kinase ameliorates hypoxia-induced pulmonary hypertension in mice. J. Cardiovasc. Pharmacol. 48(6): 280-285. doi:10.1097/01.fjc.0000248244.64430.4a. PMID:17204906.
3. Badejo, A.M., Jr., Dhaliwal, J.S., Casey, D.B., Gallen, T.B., Greco, A.J., and Kadowitz, P.J. 2008. Analysis of pulmonary vasodilator responses to the Rho-kinase inhibitor fasudil in the anesthetized rat. Am. J. Physiol. Lung Cell. Mol. Physiol. 295(5): L828-L836. doi:10.1152/ajplung.00042.2008. PMID:18689606.
4. Bellan, J.A., Minkes, R.K., Hood, J.S., McMahon, T.J., Higuera, T.R., Nossaman, B.D., et al. 1992. Analysis of pulmonary and systemic vascular responses to platelet-activating factor in the cat. Am. J. Physiol. 263(1 Pt 2): H234-H243. PMID:1379004.
5. Broughton, B.R.S., Walker, B.R., and Resta, T.C. 2008. Chronic hypoxia induces Rho kinase-dependent myogenic tone in small pulmonary arteries. Am. J. Physiol. Lung Cell. Mol. Physiol. 294(4): L797-L806. doi:10.1152/ajplung. 00253.2007. PMID:18263668.
6. Casey, D.B., Badejo, A.M., Jr., Dhaliwal, J.S., Murthy, S.N., Hyman, A.L., Nossaman, B.D., and Kadowitz, P.J. 2009. Pulmonary vasodilator responses to sodium nitrite are mediated by an allopurinol-sensitive mechanism in the rat. Am. J. Physiol. Heart Circ. Physiol. 296(2): H524-H533. doi:10.1152/ajpheart.00543.2008. PMID:19074675.
7. Chapados, R., Abe, K., Ihida-Stansbury, K., McKean, D., Gates, A.T., Kern, M., et al. 2006. ROCK controls matrix synthesis in vascular smooth muscle cells: coupling vasoconstriction to vascular remodeling. Circ. Res. 99(8): 837-844. doi:10.1161/01.RES.0000246172.77441.f1. PMID:16990566.
8. DeWitt, B.J., Cheng, D.Y., McMahon, T.J., Nossaman, B.D., and Kadowitz, P.J. 1994. Analysis of responses to bradykinin in the pulmonary vascular bed of the cat. Am. J. Physiol. 266(6 Pt 2): H2256-H2267. PMID:7517646.
9. 2+ entry mediate increased pulmonary and systemic vascular resistance in L-NAME-treated rats. Am. J. Physiol. Lung Cell. Mol. Physiol. 293(5): L1306-L1313. doi:10.1152/ajplung.00189.2007. PMID:17766587.
10. Everett, A.D., Le Cras, T.D., Xue, C., and Johns, R.A. 1998. eNOS expression is not altered in pulmonary vascular remodeling due to increased pulmonary blood flow. Am. J. Physiol. Lung Cell. Mol. Physiol. 274: L1058-L1065.
11. Fagan, K.A., Oka, M., Bauer, N.R., Gebb, S.A., Ivy, D.D., Morris, K.G., and McMurtry. I.F. 2004. Attenuation of acute hypoxic pulmonary vasoconstriction and hypoxic pulmonary hypertension in mice by inhibition of Rho-kinase. Am. J. Physiol. Lung Cell. Mol. Physiol. 287(4): L656-L664. doi:10.1152/ajplung. 00090.2003. PMID:14977625.
12. Fukata, Y., Amano, M., and Kaibuchi, K. 2001. Rho-Rho-kinase pathway in smooth muscle contraction and cytoskeletal reorganization of non-muscle cells. Trends Pharmacol. Sci. 22(1): 32-39. doi:10.1016/S0165-6147(00)01596-0. PMID:11165670.
13. Fukui, S., Fukumoto, Y., Suzuki, J., Saji, K., Nawata, J., Tawara, S., et al. 2008. Long-term inhibition of Rho-kinase ameliorates diastolic heart failure in hypertensive rats. J. Cardiovasc. Pharmacol. 51(3): 317-326. doi:10.1097/FJC.0b013e31816533b7. PMID:18356698.
14. Fukumoto, Y., Matoba, T., Ito, A., Tanaka, H., Kishi, T., Hayashidani. S., et al. 2005. Acute vasodilator effects of a Rho-kinase inhibitor, fasudil, in patients with severe pulmonary hypertension. Heart. 91(3): 391-392. doi:10.1136/hrt.2003.029470. PMID:15710736.
15. Guihert, C., Ducret, T., and Savineau, J.P. 2008. Voltage-independent calcium influx in smooth muscle. Prog. Biophys. Mol. Biol. 98(1): 10-23. doi:10.1016/j.pbiomolhio.2008.05.001. PMID:18614208.
16. Hampl, V., and Herget, J. 2000. Role of nitric oxide in the pathogenesis of chronic pulmonary hypertension. Physiol. Rev. 80(4): 1337-1372. PMID:1101S616.
17. Hennenberg, M., Biecker, E., Trehicka, J., Jochem, K., Zhou, Q., Schmidt, M., et al. 2006. Defective RhoA/Rho-kinase signaling contributes to vascular hypocontractility and vasodilation in cirrhotic rats. Gastroenterology. 130(3): 838-854. doi:10.1053/j.gastro.2005.11.029. PMID:16530523.
18. 2+ sensitivity in rabbit pulmonary artery smooth muscle. Pflugers Arch. Eur. J. Physiol. 417(1): 21-28. doi:10.1007/BF00370764.
19. Hizume, T., Morikawa. K., Takaki. A., Abe, K., Sunagawa, K., Amano, M., et al. 2006. Sustained elevation of serum cortisol level causes sensitization of coronary vasoconstricting responses in pigs in vivo: a possible link between stress and coronary vasospasm. Circ. Res. 99(7): 767-775. doi:10.1161/01.RES. 0000244093.69985.2f. PMID:16960099.
20. Hyman, A.L., Hao, Q., Tower, A., Kadowitz, P.J., Champion. H.C., Gumusel. B., et al. 1998. Novel catheterization technique for the in vivo measurement of pulmonary vascular responses in rats. Am. J. Physiol. Heart Circ. Physiol. 274: H1218-H1229.
21. Ishikura, K., Yarnada, N., Ito, M., Ota, S., Nakamura, M., Isaka, N., and Nakano, T. 2006. Beneficial acute effects of rho-kinase inhibitor in patients with pulmonary arterial hypertension. Circ. J. 70(2): 174-178. doi:10.1253/circj.70.174. PMID:16434811.
22. Janssen, L.J., Lu-Chao, H., and Netherton, S. 2001. Excitation- contraction coupling in pulmonary vascular smooth muscle involves tyrosine kinase and Rho kinase. Am. J. Physiol. Lung Cell. Mol. Physiol. 280(4): L666-L674. PMID:11238006.
23. 2+ desensitization in pulmonary vascular smooth muscle through inhibition of RhoA/Rho kinase signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 287(61): L1220-L1229. doi:10.1152/ajplung.00196.2004. PMID:15310556.
24. Jiang, B.H., Tawara, S., Abe, K., Takaki, A., Fukumoto, Y., and Shimokawa, H. 2007. Acute vasodilator effect of fasudil, a Rho-kinase inhibitor, in monocrotaline-induced pulmonary hypertension in rats. J. Cardiovasc. Pharmacol. 49(2): 85-89. doi:10.1097/FJC.0b013e31802df112. PMID:17312448.
25. Kandabashi, T., Shimokawa, H., Miyata, K., Kunihiro, I., Kawano, Y., Fukata, Y., et al. 2000. Inhibition of myosin phosphatase by upregulated rho-kinase plays a key role for coronary artery spasm in a porcine model with interleukin-1beta. Circulation, 101(11): 1319-1323. PMID:10725293.
26. Kandahashi, T., Shimokawa, H., Miyata, K., Kunihiro, I., Eto, Y., Morishige, K., et al. 2003. Evidence for protein kinase C-mediated activation of Rho-kinase in a porcine model of coronary artery spasm. Arterioscler. Thromb. Vasc. Riol. 23(12): 2209-2214. doi:10.1161/01.ATV.0000104010.87348.26. PMID: 14592852.
27. Kriseman, T., Underwood, D.C., Hyman, A.L., and Kadowitz, P.J. 1986. Analysis of airway responses to A23187 in the cat. J. Pharmacol. Exp. Ther. 239(2): 395-399. PMID:3095538.
28. Liao, J.K., Seto, M., and Noma, K. 2007. Rho kinase (ROCK) inhibitors. J. Cardiovasc. Phaimacol. 50(1): 17-24. doi:10.1097/ FJC.0b013e318070d1hd. PMID:17666911.
29. Liu, P.-Y., and Liao, J.K. 2008. A method for measuring Rho kinase activity in tissues and cells. Methods Enzymol. 439: 181-189. doi:10.1016/S0076-6879(07)004 14-4. PMID:18374165.
30. Martin, C., Göggel. R., Ressmeyer, A.R., and Uhlig, S. 2004. Pressor responses to platelet-activating factor and thromhoxane are mediated by Rho-kinase. Am. J. Physiol. Lung Cell. Mol. Physiol. 287(1): L250-L257. doi:10.1152/ajplung.00420.2003. PMID:15064228.
31. McMahon, T.J., Hood, J.S., Bellan. J.A., and Kadowitz, P.J. 1991. N ornega-nitro-L-arginine methyl ester selectively inhibits pulmonary vasodilator responses to acetyrlcholine and bradykinin. J. Appl. Physiol. 71(5): 2026-2031. PMID:1662200.
32. McMahon, T.J., Hood, J.S., Nossaman. B.D., and Kadowitz, P.J. 1993. Analysis of responses to serotonin in the pulmonary 'ascular bed of the cat. J. Appl. Physiol. 75(1): 93-102. PMID:8104177.
33. Nagaoka, T., Morio, Y., Casanova, N., Bauer, N., Gebb, S., McMurthy, I., and Oka. M. 2004. Rho/Rho kinase signaling mediates increased basal pulmonary vascular tone in chronically hypoxic rats. Am. J. Physiol. Lung Cell. Mol. Physiol. 287(4): L665-L672. doi:10.1152/ajplung.00050.2003. PMID:12959926.
34. Nagaoka, T., Fagan, K.A., Gebb, S.A., Morris, K.G., Suzuki, T., Shimokawa, H., et al. 2005. Inhaled Rho kinase inhibitors are potent and selective vasodilators in rat pulmonary hypertension. Am. J. Respir. Crit. Care Med. 171(5): 494-499. doi:10.1164/ rccm.200405-637OC. PMID:15563635.
35. Nossaman, B.D., McMahon, T.J., Ragheb, M.S., lbrahim, I.N., Babycos, C.R., Hood, J.S., and Kadowitz, P.J. 1992. Blockade of thromboxane/endoperoxide receptor-mediated responses in the pulmonary vascular bed of the cat by sulotrohan. Eur. J. Pharmacol. 213(1): 1-7. doi:10.1016/00l4-2999(92) 90225-S. PMID:1379928.
36. Oka, M., Homma, N., Taraseviciene-Stewart, L., Morris, K.G., Kraskauskas, D., Burns, N., et al. 2007. Rho kinase-mediated vasoconstriction is important in severe occlusive pulmonary arterial hypertension in rats. Circ. Res. 100(6): 923-929. doi:10.1161101.RES.0000261658.12024.18. PMID:17332430.
37. Parker, T.A., Roe, G., Grover, T.R., and Abman, S.H. 2006. Rho kinase activation maintains high pulmonary vascular resistance in the ovine fetal lung. Aim J. Physiol. Lung Cell. Mol. Physiol. 291(5): L976-L982. doi:10.1152/ajplung.005 12.2005. PMID:16815887.
38. Pyne-Geithman, G.J., Nair, S.G., Caudell, D.N., and Clark, J.F. 2008. PKC and Rho in vascular smooth muscle: activation by BOXes and SAH CSF. Front. Biosci. 13(13): 1526-1534. doi:10.2741/2778. PMID:17981646.
39. Robertson, T.P., Dipp, M., Ward, J.P., Aaronson, P.I., and Evans, A.M. 2000. Inhibition of sustained hypoxic vasoconstriction by Y-27632 in isolated intrapulmonary arteries and perfused lung of the rat. Br. J. Pharmacol. 131(1): 5-9. doi:10.1038/sj.bjp.0703537. PMID:10960061.
40. Salomonsson, M., Sorensen, C.M., Arendshorst, W.J., Steendahl, J., and Holstein-Rathlou, N.H. 2004. Calcium handling in afferent arterioles. Acta Physiol. Scand. 181(4): 421-429. doi:10.1111/j.1365-201X.2004.01314.x. PMID:15283754.
41. Shimokawa, H., Seto, M., Katsumata, N., Amano, M., Kozai, T., Yamawaki, T., et al. 1999. Rho-kinase-mediated pathway induces enhanced myosin light chain phosphorylations in a swine model of coronary artery spasm. Cardiovasc. Res. 43(4): 1029-1039. doi:10.1016/S0008-6363(99)00144-3. PMID:10615430.
42. Shimokawa, H., Morishige, K., Miyata, K., Kandahashi, T., Eto, Y., Ikegaki, I., et al. 2001. Long-term inhibition of Rho-kinase induces a regression of arteriosclerotic coronary lesions in a porcine model in vivo. Cardiovasc. Res. 51(1): 169-177. doi:10.1016/S0008-6363(01)00291-7. PMID:11399259.
43. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins. kinases, and myosin phosphatase. Physiol. Rev. 83(4): 1325-1358. PMID:14506307.
44. Uehata, M., Ishizaki, T., Satoh, H., Ono, T., Kawahara, T., Morishita, T., et al. 1997. Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature. 389(6654): 990-994. doi:10.1038/40187. PMID:9353125.
45. Underwood, D.C., Kriseman, T., McNamara, D.B., Hyman, A.L., and Kadowitz, P.J. 1987. Blockade of thromboxane responses in the airway of the cat by SQ 29.548. J. Appl. Physiol. 62(6): 2 193-2200. PMID:2440845.
46. Wang, Z., Jin, N., Ganguli, S., Swartz, D.R., Li, L., and Rhoades, R.A. 2001. Rho-kinase activation is involved in hypoxia-induced pulmonary vasoconstriction. Am. J. Respir. Cell Mol. Biol. 25(5): 628-635. PMID:11713106.
47. Wang, Z., Lanner, M.C., Jin. N., Swartz, D., Li, L., and Rhoades, R.A. 2003. Hypoxia inhibits myosin phosphatase in pulmonary arterial smooth muscle cells: role of Rho-kinase. Am. J. Respir. Cell Mol. Biol. 29(4): 465-471. doi:10.1165/rcmb.2002-0157OC. PMID:12714374.
48. 2+ signaling in hypoxic pulmonary vasoconstriction: effects of myosin light chain and Rho kinase antagonists. Am. J. Physiol. Lung Cell. Mol. Physiol. 293(3): L674-L685. doi:10.1152/ajplung.00141.2007. PMID:17575009.
49. Watanabe, Y., Faraci, F.M., and Heistad, D.D. 2005. Activation of Rho-associated kinase during augmented contraction of the basilar artery to serotonin after subarachnoid hemorrhage. Am. J. Physiol. Heart Circ. Physiol. 288(6): H2653-H2658. doi:10.1152/aipheart.00923.2004. PMID:15665056.
50. Wickman, G., Lan, C., and Vollrath, B. 2003. Functional roles of the rho/rho kinase pathway and protein kinase C in the regulation of cerebrovascular constriction mediated by hemoglobin: relevance to subarachnoid hemorrhage and vasospasm. Circ. Res. 92(7): 809-816. doi:10.1161/01.RES.0000066663. 12256.82. PM ID: 12637369.
51. Williams, J., Bogwu, J., and Oyekan, A. 2006. The role of the RhoA/Rho-kinase signaling pathway in renal vascular reactivity in endothelial nitric oxide synthase null mice. J. Hypertens. 24(7): 1429-1436. doi:10.1097/01.hjh.0000234125.01638.3b. PMID:16794494.
52. Xu, Z., Okamoto, H., Akino, M., Onozuka, H., Matsui, Y., and Tsutsui, H. 2008. Pravastatin attenuates left ventricular remodeling and diastolic dysfunction in angiotensin II-induced hypertensive mice. J. Cardiovasc. Pharmacol. 51(1): 62-70. doi:10.1097/ FJC.0b013e31815bb629. PMID:18209570.
53. Yi, S.L., Kantores, C., Belcastro, R., Cabacungan, J., Tanswell, A.K., and Jankov, R.P. 2006. 8-Isoprostane-induced endothelin1 production by infant rat pulmonary artery smooth muscle cells is mediated by Rho-kinase. Free Radic. Biol. Med. 41(6): 942-949. dol: 10.1016/j.freeradbiomed.2006.05.035. PMID:16934677.