Protein kinase G-I deficiency induces pulmonary hypertension through Rho A/Rho kinase activation

American Journal of Pathology

Volumn 180, Issue 6, 2012, Pages 2268-2275

  Zhao, Yidan D ^a   Cai, Lei ^a,b   Mirza, Muhammad K ^a   Huang, Xiaojia ^a   Geenen, Dave L ^a   Hofmann, Franz ^c   Yuan, Jason X J ^a   Zhao, You Yang ^a  

^a UNIVERSITY OF ILLINOIS   (United States)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

FASUDIL; RHO KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME DEFICIENCY; ENZYME PHOSPHORYLATION; HEART RIGHT VENTRICLE PRESSURE; MICROANGIOGRAPHY; MOUSE; NONHUMAN; PATHOGENESIS; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN KINASE G 1 DEFICIENCY; PULMONARY HYPERTENSION; SYSTOLIC BLOOD PRESSURE;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANIMALS; ANTIHYPERTENSIVE AGENTS; CELLS, CULTURED; CYCLIC GMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; HYPERTENSION, PULMONARY; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; PROTEIN KINASE INHIBITORS; PULMONARY ARTERY; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION; VASOCONSTRICTION;

EID: 84861632141     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.02.016     Document Type: Article

References (49)

1. L.J. Rubin Primary pulmonary hypertension N Engl J Med 336 1997 111 117
2. G. Simonneau, I.M. Robbins, M. Beghetti, R.N. Channick, M. Delcroix, C.P. Denton, C.G. Elliott, S.P. Gaine, M.T. Gladwin, Z.C. Jing, M.J. Krowka, D. Langleben, N. Nakanishi, R. Souza Updated clinical classification of pulmonary hypertension J Am Coll Cardiol 54 2009 S43 S54
3. S. Rich The current treatment of pulmonary arterial hypertension: time to redefine success Chest 130 2006 1198 1202
4. H.W. Farber The status of pulmonary arterial hypertension in 2008 Circulation 117 2008 2966 2968
5. K.A. Lucas, G.M. Pitari, S. Kazerounian, I. Ruiz-Stewart, J. Park, S. Schulz, K.P. Chepenik, S.A. Waldman Guanylyl cyclases and signaling by cyclic GMP Pharmacol Rev 52 2000 375 414
6. F. Hofmann, R. Feil, T. Kleppisch, J. Schlossmann Function of cGMP-dependent protein kinases as revealed by gene deletion Physiol Rev 86 2006 1 23
7. J. Xu, L. Liu The role of calcium desensitization in vascular hyporeactivity and its regulation after hemorrhagic shock in the rat Shock 23 2005 576 581
8. J. Nishimura, H. Setoguchi, H. Kanaide Regulation of vascular tone by the modulation of Ca2+ sensitivity [Japanese] Clin Calcium 11 2001 411 417
9. W. Wernet, V. Flockerzi, F. Hofmann The cDNA of the two isoforms of bovine cGMP-dependent protein kinase FEBS Lett 251 1989 191 196
10. R. Feil, S.M. Lohmann, H. de Jonge, U. Walter, F. Hofmann Cyclic GMP-dependent protein kinases and the cardiovascular system: insights from genetically modified mice Circ Res 93 2003 907 916
11. R.S. Stephens, O. Rentsendorj, L.E. Servinsky, A. Moldobaeva, R. Damico, D.B. Pearse cGMP increases antioxidant function and attenuates oxidant cell death in mouse lung microvascular endothelial cells by a protein kinase G-dependent mechanism Am J Physiol Lung Cell Mol Physiol 299 2010 L323 L333
12. R.W. McMichael Jr, J.C. Lagarias Phosphopeptide mapping of Avena phytochrome phosphorylated by protein kinases in vitro Biochemistry 29 1990 3872 3878
13. N. Sawada, H. Itoh, J. Yamashita, K. Doi, M. Inoue, K. Masatsugu, Y. Fukunaga, S. Sakaguchi, M. Sone, K. Yamahara, T. Yurugi, K. Nakao cGMP-dependent protein kinase phosphorylates and inactivates RhoA Biochem Biophys Res Commun 280 2001 798 805
14. V. Sauzeau, H. Le Jeune, C. Cario-Toumaniantz, A. Smolenski, S.M. Lohmann, J. Bertoglio, P. Chardin, P. Pacaud, G. Loirand Cyclic GMP-dependent protein kinase signaling pathway inhibits RhoA-induced Ca2+ sensitization of contraction in vascular smooth muscle J Biol Chem 275 2000 21722 21729
15. J. Feng, M. Ito, K. Ichikawa, N. Isaka, M. Nishikawa, D.J. Hartshorne, T. Nakano Inhibitory phosphorylation site for Rho-associated kinase on smooth muscle myosin phosphatase J Biol Chem 274 1999 37385 37390
16. M. Sausbier, R. Schubert, V. Voigt, C. Hirneiss, A. Pfeifer, M. Korth, T. Kleppisch, P. Ruth, F. Hofmann Mechanisms of NO/cGMP-dependent vasorelaxation Circ Res 87 2000 825 830
17. A. Pfeifer, P. Klatt, S. Massberg, L. Ny, M. Sausbier, C. Hirneiss, G.X. Wang, M. Korth, A. Aszodi, K.E. Andersson, F. Krombach, A. Mayerhofer, P. Ruth, R. Fassler, F. Hofmann Defective smooth muscle regulation in cGMP kinase I-deficient mice EMBO J 17 1998 3045 3051
18. K. Persson, R.K. Pandita, A. Aszodi, M. Ahmad, A. Pfeifer, R. Fassler, K.E. Andersson Functional characteristics of urinary tract smooth muscles in mice lacking cGMP protein kinase type I Am J Physiol Regul Integr Comp Physiol 279 2000 R1112 R1120
19. L. Ny, A. Pfeifer, A. Aszodi, M. Ahmad, P. Alm, P. Hedlund, R. Fassler, K.E. Andersson Impaired relaxation of stomach smooth muscle in mice lacking cyclic GMP-dependent protein kinase I Br J Pharmacol 129 2000 395 401
20. P. Hedlund, A. Aszodi, A. Pfeifer, P. Alm, F. Hofmann, M. Ahmad, R. Fassler, K.E. Andersson Erectile dysfunction in cyclic GMP-dependent kinase I-deficient mice Proc Natl Acad Sci U S A 97 2000 2349 2354
21. K. Yamahara, H. Itoh, T.H. Chun, Y. Ogawa, J. Yamashita, N. Sawada, Y. Fukunaga, M. Sone, T. Yurugi-Kobayashi, K. Miyashita, H. Tsujimoto, H. Kook, R. Feil, D.L. Garbers, F. Hofmann, K. Nakao Significance and therapeutic potential of the natriuretic peptides/cGMP/cGMP-dependent protein kinase pathway in vascular regeneration Proc Natl Acad Sci U S A 100 2003 3404 3409
22. Z. Li, X. Xi, M. Gu, R. Feil, R.D. Ye, M. Eigenthaler, F. Hofmann, X. Du A stimulatory role for cGMP-dependent protein kinase in platelet activation Cell 112 2003 77 86
23. J.D. Chiche, S.M. Schlutsmeyer, D.B. Bloch, S.M. de la Monte, J.D. Roberts Jr, G. Filippov, S.P. Janssens, A. Rosenzweig, K.D. Bloch Adenovirus-mediated gene transfer of cGMP-dependent protein kinase increases the sensitivity of cultured vascular smooth muscle cells to the antiproliferative and pro-apoptotic effects of nitric oxide/cGMP J Biol Chem 273 1998 34263 34271
24. W. Zhou, S. Negash, J. Liu, J.U. Raj Modulation of pulmonary vascular smooth muscle cell phenotype in hypoxia: role of cGMP-dependent protein kinase and myocardin Am J Physiol Lung Cell Mol Physiol 296 2009 L780 L789
25. W. Zhou, C. Dasgupta, S. Negash, J.U. Raj Modulation of pulmonary vascular smooth muscle cell phenotype in hypoxia: role of cGMP-dependent protein kinase Am J Physiol Lung Cell Mol Physiol 292 2007 L1459 L1466
26. Y.Y. Zhao, Y.D. Zhao, M.K. Mirza, J.H. Huang, H.H. Potula, S.M. Vogel, V. Brovkovych, J.X. Yuan, J. Wharton, A.B. Malik Persistent eNOS activation secondary to caveolin-1 deficiency induces pulmonary hypertension in mice and humans through PKG nitration J Clin Invest 119 2009 2009 2018
27. Y.D. Zhao, D.W. Courtman, Y. Deng, L. Kugathasan, Q. Zhang, D.J. Stewart Rescue of monocrotaline-induced pulmonary arterial hypertension using bone marrow-derived endothelial-like progenitor cells: efficacy of combined cell and eNOS gene therapy in established disease Circ Res 96 2005 442 450
28. Y.D. Zhao, H. Ohkawara, J. Rehman, K.K. Wary, S.M. Vogel, R.D. Minshall, Y.Y. Zhao, A.B. Malik Bone marrow progenitor cells induce endothelial adherens junction integrity by sphingosine-1-phosphate-mediated Rac1 and Cdc42 signaling Circ Res 105 2009 696 704 8 p following 704
29. M. Rolli-Derkinderen, V. Sauzeau, L. Boyer, E. Lemichez, C. Baron, D. Henrion, G. Loirand, P. Pacaud Phosphorylation of serine 188 protects RhoA from ubiquitin/proteasome-mediated degradation in vascular smooth muscle cells Circ Res 96 2005 1152 1160
30. T. Kitazawa, S. Semba, Y.H. Huh, K. Kitazawa, M. Eto Nitric oxide-induced biphasic mechanism of vascular relaxation via dephosphorylation of CPI-17 and MYPT1 J Physiol 587 2009 3587 3603
31. U. Walter Physiological role of cGMP and cGMP-dependent protein kinase in the cardiovascular system Rev Physiol Biochem Pharmacol 113 1989 41 88
32. T.D. Warner, J.A. Mitchell, H. Sheng, F. Murad Effects of cyclic GMP on smooth muscle relaxation Adv Pharmacol 26 1994 171 194
33. D.L. Garbers, S.K. Dubois The molecular basis of hypertension Annu Rev Biochem 68 1999 127 155
34. M. Koeppen, R. Feil, D. Siegl, S. Feil, F. Hofmann, U. Pohl, C. de Wit cGMP-dependent protein kinase mediates NO- but not acetylcholine-induced dilations in resistance vessels in vivo Hypertension 44 2004 952 955
35. T.L. Cornwell, E. Arnold, N.J. Boerth, T.M. Lincoln Inhibition of smooth muscle cell growth by nitric oxide and activation of cAMP-dependent protein kinase by cGMP Am J Physiol 267 1994 C1405 C1413
36. G.A. Soff, T.L. Cornwell, D.L. Cundiff, S. Gately, T.M. Lincoln Smooth muscle cell expression of type I cyclic GMP-dependent protein kinase is suppressed by continuous exposure to nitrovasodilators, theophylline, cyclic GMP, and cyclic AMP J Clin Invest 100 1997 2580 2587
37. Y.Y. Zhao, A.B. Malik A novel insight into the mechanism of pulmonary hypertension involving caveolin-1 deficiency and endothelial nitric oxide synthase activation Trends Cardiovasc Med 19 2009 238 242
38. T.M. Lincoln, N.B. Dey, N.J. Boerth, T.L. Cornwell, G.A. Soff Nitric oxide-cyclic GMP pathway regulates vascular smooth muscle cell phenotypic modulation: implications in vascular diseases Acta Physiol Scand 164 1998 507 515
39. N.B. Dey, N.J. Boerth, J.E. Murphy-Ullrich, P.L. Chang, C.W. Prince, T.M. Lincoln Cyclic GMP-dependent protein kinase inhibits osteopontin and thrombospondin production in rat aortic smooth muscle cells Circ Res 82 1998 139 146
40. K. Abe, H. Shimokawa, K. Morikawa, T. Uwatoku, K. Oi, Y. Matsumoto, T. Hattori, Y. Nakashima, K. Kaibuchi, K. Sueishi, A. Takeshit Long-term treatment with a Rho-kinase inhibitor improves monocrotaline-induced fatal pulmonary hypertension in rats Circ Res 94 2004 385 393
41. K.A. Fagan, M. Oka, N.R. Bauer, S.A. Gebb, D.D. Ivy, K.G. Morris, I.F. McMurtry 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 2004 L656 L664
42. Y. Gao, A.D. Portugal, S. Negash, W. Zhou, L.D. Longo, J. Usha Raj Role of Rho kinases in PKG-mediated relaxation of pulmonary arteries of fetal lambs exposed to chronic high altitude hypoxia Am J Physiol Lung Cell Mol Physiol 292 2007 L678 L684
43. T. Nagaoka, Y. Morio, N. Casanova, N. Bauer, S. Gebb, I. McMurtry, M. Oka Rho/Rho kinase signaling mediates increased basal pulmonary vascular tone in chronically hypoxic rats Am J Physiol Lung Cell Mol Physiol 287 2004 L665 L672
44. V. Sauzeau, M. Rolli-Derkinderen, C. Marionneau, G. Loirand, P. Pacaud RhoA expression is controlled by nitric oxide through cGMP-dependent protein kinase activation J Biol Chem 278 2003 9472 9480
45. C.P. Mack, A.V. Somlyo, M. Hautmann, A.P. Somlyo, G.K. Owens Smooth muscle differentiation marker gene expression is regulated by RhoA-mediated actin polymerization J Biol Chem 276 2001 341 347
46. T. Gudi, J.C. Chen, D.E. Casteel, T.M. Seasholtz, G.R. Boss, R.B. Pilz cGMP-dependent protein kinase inhibits serum-response element-dependent transcription by inhibiting rho activation and functions J Biol Chem 277 2002 37382 37393
47. G. Loirand, M. Rolli-Derkinderen, P. Pacaud RhoA and resistance artery remodeling Am J Physiol Heart Circ Physiol 288 2005 H1051 H1056
48. T. Nagaoka, K.A. Fagan, S.A. Gebb, K.G. Morris, T. Suzuki, H. Shimokawa, I.F. McMurtry, M. Oka Inhaled Rho kinase inhibitors are potent and selective vasodilators in rat pulmonary hypertension Am J Respir Crit Care Med 171 2005 494 499
49. A.P. Somlyo, A.V. Somlyo Ca2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase Physiol Rev 83 2003 1325 1358