Involvement of the bone morphogenetic protein system in endothelin-and aldosterone-induced cell proliferation of pulmonary arterial smooth muscle cells isolated from human patients with pulmonary arterial hypertension

Hypertension Research

Volumn 33, Issue 5, 2010, Pages 435-445

  Yamanaka, Ryutaro ^a   Otsuka, Fumio ^a   Nakamura, Kazufumi ^a   Yamashita, Misuzu ^a   Otani, Hiroyuki ^a   Takeda, Masaya ^a   Matsumoto, Yoshinori ^a   Kusano, Kengo F ^a   Ito, Hiroshi ^a   Makino, Hirofumi ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Aldosterone; Bone morphogenetic protein; Endothelin; Mineralocorticoid receptor; Pulmonary arterial hypertension

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; ALDOSTERONE; BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN RECEPTOR; BOSENTAN; ENDOTHELIN; ENDOTHELIN 1; ENDOTHELIN 3; EPLERENONE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 9; OSTEOGENIC PROTEIN 1; PROTEIN C JUN; SMAD PROTEIN; STRESS ACTIVATED PROTEIN KINASE 1;

ADULT; ARTICLE; CASE REPORT; CELL ISOLATION; CELL PROLIFERATION; CELL TYPE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; LUNG ALVEOLUS CELL; MALE; MITOSIS; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PROTEIN EXPRESSION; PULMONARY ARTERY SMOOTH MUSCLE CELL; PULMONARY HYPERTENSION; SIGNAL TRANSDUCTION; UPREGULATION;

ALDOSTERONE; ANALYSIS OF VARIANCE; BLOTTING, WESTERN; BONE MORPHOGENETIC PROTEIN RECEPTORS, TYPE II; BONE MORPHOGENETIC PROTEINS; CELL CULTURE TECHNIQUES; CELL PROLIFERATION; CELLS, CULTURED; ENDOTHELINS; HUMANS; HYPERTENSION, PULMONARY; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PULMONARY ARTERY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 77951972229     PISSN: 09169636     EISSN: 13484214     Source Type: Journal    
DOI: 10.1038/hr.2010.16     Document Type: Article

References (48)

1. Rubin LJ. Primary pulmonary hypertension. N Engl J Med 1997; 336: 111-117.
2. Palevsky HI, Schloo B, Pietra GG, Weber KT, Janicki JS, Rubin E, Fishman AP. Primary pulmonary hypertesion: vascular structure, morphometry, and responsiveness to vasodilator agents. Circulation 1989; 80: 1207-1221.
3. Wilkins MR, Gibbs JS, Shovlin CL. A gene for primary pulmonary hypertension. Lancet 2000; 356: 1207-1208.
4. Nichols WC, Koller DL, Slovis B, Foroud T, Terry VH, Arnold ND, Siemieniak DR, Wheeler L, Phillips III JA, Newman JH, Conneally PM, Ginsburg D, Loyd JE. Localization of the gene for familial primary pulmonary hypertension to chromosome 2q31-32. Nat Genet 1997; 15: 277-280.
5. Deng Z, Morse JH, Slager SL, Cuervo N, Moore KJ, Venetos G, Kalachikov S, Cayanis E, Fischer SG, Barst RJ, Hodge SE, Knowles JA. Familial primary pulmonary hypertension (gene PPH1) is caused by mutations in the bone morphogenetic protein receptor-II gene. Am J Hum Genet 2000; 67: 737-744.
6. Lane KB, Machado RD, Pauciulo MW, Thomson JR, Phillips III JA, Loyd JE, Nichols WC, Trembath RC. Heterozygous germline mutations in BMPR2, encoding a TGF-beta receptor, cause familial primary pulmonary hypertension. The International PPH Consortium. Nat Genet 2000; 26: 81-84.
7. Thomson JR, Machado RD, Pauciulo MW, Morgan NV, Humbert M, Elliott GC, Ward K, Yacoub M, Mikhail G, Rogers P, Newman J, Wheeler L, Higenbottam T, Gibbs JS, Egan J, Crozier A, Peacock A, Allcock R, Corris P, Loyd JE, Trembath RC, Nichols WC. Sporadic primary pulmonary hypertension is associated with germline mutations of the gene encoding BMPR-II, a receptor member of the TGF-beta family. J Med Genet 2000; 37: 741-745.
8. Morrell NW, Yang X, Upton PD, Jourdan KB, Morgan N, Sheares KK, Trembath RC. Altered growth responses of pulmonary artery smooth muscle cells from patients with primary pulmonary hypertension to transforming growth factor-beta(1) and bone morphogenetic proteins. Circulation 2001; 104: 790-795.
9. Rudarakanchana N, Flanagan JA, Chen H, Upton PD, Machado R, Patel D, Trembath RC, Morrell NW. Functional analysis of bone morphogenetic protein type II receptor mutations underlying primary pulmonary hypertension. Hum Mol Genet 2002; 11: 1517-1525.
10. Runo JR, Loyd JE. Primary pulmonary hypertension. Lancet 2003; 361: 1533-1544.
11. Giaid A, Yanagisawa M, Langleben D, Michel RP, Levy R, Shennib H, Kimura S, Masaki T, Duguid WP, Stewart DJ. Expression of endothelin-1 in the lungs of patients with pulmonary hypertension. N Engl J Med 1993; 328: 1732-1739. (Pubitemid 23170122)
12. Jeffery TK, Morrell NW. Molecular and cellular basis of pulmonary vascular remodeling in pulmonary hypertension. Prog Cardiovasc Dis 2002; 45: 173-202.
13. Christman BW, McPherson CD, Newman JH, King GA, Bernard GR, Groves BM, Loyd JE. An imbalance between the excretion of thromboxane and prostacyclin metabolites in pulmonary hypertension. N Engl J Med 1992; 327: 70-75.
14. Giaid A. Nitric oxide and endothelin-1 in pulmonary hypertension. Chest 1998; 114: 208S-212S.
15. Ambalavanan N, Bulger A, Murphy-Ullrich J, Oparil S, Chen YF. Endothelin-A receptor blockade prevents and partially reverses neonatal hypoxic pulmonary vascular remodeling. Pediatr Res 2005; 57: 631-636.
16. Rosenberg AA, Kennaugh J, Koppenhafer SL, Loomis M, Chatfield BA, Abman SH. Elevated immunoreactive endothelin-1 levels in newborn infants with persistent pulmonary hypertension. J Pediatr 1993; 123: 109-114.
17. Kunichika N, Landsberg JW, Yu Y, Kunichika H, Thistlethwaite PA, Rubin LJ, Yuan JX. Bosentan inhibits transient receptor potential channel expression in pulmonary vascular myocytes. Am J Respir Crit Care Med 2004; 170: 1101-1107.
18. Davie N, Haleen SJ, Upton PD, Polak JM, Yacoub MH, Morrell NW, Wharton J. ET(A) and ET(B) receptors modulate the proliferation of human pulmonary artery smooth muscle cells. Am J Respir Crit Care Med 2002; 165: 398-405. (Pubitemid 34118516)
19. Abraham WT, Raynolds MV, Badesch DB, Wynne KM, Groves BM, Roden RL, Robertson AD, Lowes BD, Zisman LS, Voelkel NF, Bristow MR, Perryman MB. Angiotensin-converting enzyme DD genotype in patients with primary pulmonary hypertension: increased frequency and association with preserved haemodynamics. J Renin Angio-tensin Aldosterone Syst 2003; 4: 27-30.
20. Orte C, Polak JM, Haworth SG, Yacoub MH, Morrell NW. Expression of pulmonary vascular angiotensin-converting enzyme in primary and secondary plexiform pulmonary hypertension. J Pathol 2000; 192: 379-384.
21. Okada K, Bernstein ML, Zhang W, Schuster DP, Botney MD. Angiotensin-converting enzyme inhibition delays pulmonary vascular neointimal formation. Am J Respir Crit Care Med 1998; 158: 939-950.
22. Chung WK, Deng L, Carroll JS, Mallory N, Diamond B, Rosenzweig EB, Barst RJ, Morse JH. Polymorphism in the angiotensin II type 1 receptor (AGTR1) is associated with age at diagnosis in pulmonary arterial hypertension. J Heart Lung Transplant 2009; 28: 373-379.
23. Kouchi H, Nakamura K, Fushimi K, Sakaguchi M, Miyazaki M, Ohe T, Namba M. Manumycin A, inhibitor of ras farnesyltransferase, inhibits proliferation and migration of rat vascular smooth muscle cells. Biochem Biophys Res Commun 1999; 264: 915-920.
24. Ogawa A, Nakamura K, Matsubara H, Fujio H, Ikeda T, Kobayashi K, Miyazaki I, Asanuma M, Miyaji K, Miura D, Kusano KF, Date H, Ohe T. Prednisolone inhibits proliferation of cultured pulmonary artery smooth muscle cells of patients with idiopathic pulmonary arterial hypertension. Circulation 2005; 112: 1806-1812.
25. Takeda M, Otsuka F, Suzuki J, Kishida M, Ogura T, Tamiya T, Makino H. Involvement of activin/BMP system in development of human pituitary gonadotropinomas and non-functioning adenomas. Biochem Biophys Res Commun 2003; 306: 812-818.
26. Takeda M, Otsuka F, Nakamura K, Inagaki K, Suzuki J, Miura D, Fujio H, Matsubara H, Date H, Ohe T, Makino H. Characterization of the bone morphogenetic protein (BMP) system in human pulmonary arterial smooth muscle cells isolated from a sporadic case of primary pulmonary hypertension: roles of BMP type IB receptor (activin receptor-like kinase-6) in the mitotic action. Endocrinology 2004; 145: 4344-4354.
27. Von Bubnoff A, Cho KWY. Intracellular BMP signaling regulation in vertebrates: pathway or network? Dev Biol 2001; 239: 1-14.
28. Kourembanas S, Marsden PA, McQuillan LP, Faller DV. Hypoxia induces endothelin gene expression and secretion in cultured human endothelium. J Clin Invest 1991; 88: 1054-1057.
29. Wort SJ, Woods M, Warner TD, Evans TW, Mitchell JA. Endogenously released endothelin-1 from human pulmonary artery smooth muscle promotes cellular proliferation: relevance to pathogenesis of pulmonary hypertension and vascular remodeling. Am J Respir Cell Mol Biol 2001; 25: 104-110.
30. Channick RN, Simonneau G, Sitbon O, Robbins IM, Frost A, Tapson VF, Badesch DB, Roux S, Rainisio M, Bodin F, Rubin LJ. Effects of the dual endothelin-receptor antagonist bosentan in patients with pulmonary hypertension: a randomised placebo-controlled study. Lancet 2001; 358: 1119-1123. (Pubitemid 32971843)
31. Shichiri M, Kato H, Marumo F, Hirata Y. Endothelin-1 as an autocrine/paracrine apoptosis survival factor for endothelial cells. Hypertension 1997; 30: 1198-1203. (Pubitemid 27476179)
32. Wu-Wong JR, Chiou WJ, Dickinson R, Opgenorth TJ. Endothelin attenuates apoptosis in human smooth muscle cells. Biochem J 1997; 328(Pt 3): 733-737.
33. Remuzzi G, Perico N, Benigni A. New therapeutics that antagonize endothelin: promises and frustrations. Nat Rev Drug Discov 2002; 1: 986-1001.
34. Massague J. TGF-beta signal transduction. Annu Rev Biochem 1998; 67: 753-791.
35. Miyazono K, Kusanagi K, Inoue H. Divergence and convergence of TGF-beta/BMP signaling. J Cell Physiol 2001; 187: 265-276.
36. Aoki H, Fujii M, Imamura T, Yagi K, Takehara K, Kato M, Miyazono K. Synergistic effects of different bone morphogenetic protein type I receptors on alkaline phospha-tase induction. J Cell Sci 2001; 114: 1483-1489.
37. Barst RJ, Langleben D, Badesch D, Frost A, Lawrence EC, Shapiro S, Naeije R, Galie N. Treatment of pulmonary arterial hypertension with the selective endothelin-A receptor antagonist sitaxsentan. J Am Coll Cardiol 2006; 47: 2049-2056.
38. Rubin LJ, Badesch DB, Barst RJ, Galie N, Black CM, Keogh A, Pulido T, Frost A, Roux S, Leconte I, Landzberg M, Simonneau G. Bosentan therapy for pulmonary arterial hypertension. N Engl J Med 2002; 346: 896-903. (Pubitemid 34984638)
39. Star GP, Giovinazzo M, Langleben D. Effects of bone morphogenic proteins and transforming growth factor-beta on in-vitro production of endothelin-1 by human pulmonary microvascular endothelial cells. Vascul Pharmacol 2009; 50: 45-50.
40. Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. Science 1988; 242: 583-585.
41. Edwards CR, Stewart PM, Burt D, Brett L, McIntyre MA, Sutanto WS, de Kloet ER, Monder C. Localisation of 11 beta-hydroxysteroid dehydrogenase-tissue specific protector of the mineralocorticoid receptor. Lancet 1988; 2: 986-989.
42. Funder JW. The nongenomic actions of aldosterone. Endocr Rev 2005; 26: 313-321.
43. Nishihara A, Watabe T, Imamura T, Miyazono K. Functional heterogeneity of bone morphogenetic protein receptor-II mutants found in patients with primary pulmonary hypertension. Mol Biol Cell 2002; 13: 3055-3063.
44. Yamaguchi K, Shirakabe K, Shibuya H, Irie K, Oishi I, Ueno N, Taniguchi T, Nishida E, Matsumoto K. Identification of a member of the MAPKKK family as a potential mediator of TGF-6 signal transduction. Science 1995; 270: 2008-2011.
45. Yamaguchi K, Nagai S, Ninomiya-Tsuji J, Nishita M, Tamai K, Irie K, Ueno N, Nishida E, Shibuya H, Matsumoto K. XIAP, a cellular member of the inhibitor of apoptosis protein family, links the receptors to TAB 1-TAK1 in the BMP signaling pathway. EMBO J 1999; 18: 179-187.
46. Nakamura K, Shirai T, Morishita S, Uchida S, Saeki-Miura K, Makishima F. p38 Mitogen-activated protein kinase functionally contributes to chondrogenesis induced by growth/differentiation factor-5 in ATDC5 cells. Exp Cell Res 1999; 250: 351-363.
47. Piek E, Heldin CH, Ten Dijke P. Specificity, diversity, and regulation in TGF-6 superfamily signaling. FASEB J 1999; 13: 2105-2124.
48. Moore RK, Otsuka F, Shimasaki S. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J Biol Chem 2003; 278: 304-310.