Endothelin-1 contributes to increased NFATc3 activation by chronic hypoxia in pulmonary arteries

American Journal of Physiology - Cell Physiology

Volumn 301, Issue 2, 2011, Pages

  de Frutos, Sergio ^a   Diaz, Juan Manuel Ramiro ^a   Nitta, Carlos H ^a   Sherpa, Mingma L ^a   Gonzalez Bosc, Laura V ^a  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Cytoskeletal dynamics; Nuclear factor of activated T cells isoform c3; Pulmonary; Rho kinase; Smooth muscle

Indexed keywords

CALCINEURIN; CALCIUM CHANNEL L TYPE; CALCIUM ION; ENDOTHELIN 1; GREEN FLUORESCENT PROTEIN; LUCIFERASE; MESSENGER RNA; RHO KINASE; TRANSCRIPTION FACTOR NFAT3;

ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CELL LEVEL; CELL NUCLEUS; DEPHOSPHORYLATION; EX VIVO STUDY; HYPOXIA; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PULMONARY ARTERY; SMOOTH MUSCLE FIBER;

ACTINS; ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANOXIA; CALCINEURIN; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; CELLS, CULTURED; CHRONIC DISEASE; CYTOSKELETON; DISEASE MODELS, ANIMAL; ENDOTHELIN-1; GENES, REPORTER; HUMANS; MALE; MEMBRANE TRANSPORT MODULATORS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NFATC TRANSCRIPTION FACTORS; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PULMONARY ARTERY; RECEPTORS, ENDOTHELIN; RECOMBINANT FUSION PROTEINS; RHO GTP-BINDING PROTEINS; RHO-ASSOCIATED KINASES; RNA, MESSENGER; TIME FACTORS; TRANSCRIPTIONAL ACTIVATION; TRANSFECTION; UP-REGULATION;

MUS;

EID: 79960972329     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00029.2011     Document Type: Article

References (85)

1. Aaronson PI, Robertson TP, Knock GA, Becker S, Lewis TH, Snetkov V, Ward JPT. Hypoxic pulmonary vasoconstriction: mechanisms and controversies. J Physiol Online 570: 53-58, 2006.
2. Abe K, Tawara S, Oi K, Hizume T, Uwatoku T, Fukumoto Y, Kaibuchi K, Shimokawa H. Long-term inhibition of Rho-kinase ameliorates hypoxia-induced pulmonary hypertension in mice. J Cardiovasc Pharmacol 48: 280-285, 2006.
3. Abe K, Shimokawa H, Morikawa K, Uwatoku T, Oi K, Matsumoto Y, Hattori T, Nakashima Y, Kaibuchi K, Sueishi K, Takeshit A. Longterm treatment with a Rho-kinase inhibitor improves monocrotalineinduced fatal pulmonary hypertension in rats. Circ Res 94: 385-393, 2004.
4. Aguirre JI, Morrell NW, Long L, Clift P, Upton PD, Polak JM, Wilkins MR. Vascular remodeling and ET-1 expression in rat strains with different responses to chronic hypoxia. Am J Physiol Lung Cell Mol Physiol 278: L981-L987, 2000.
5. Amberg GC, Rossow CF, Navedo MF, Santana LF. NFATc3 regulates Kv2.1 expression in arterial smooth muscle. J Biol Chem 279: 47326-47334, 2004.
6. Bamburg JR, McGough A, Ono S. Putting a new twist on actin: ADF/cofilins modulate actin dynamics. Trends Cell Biol 9: 364-370, 1999.
7. Barman SA. Vasoconstrictor effect of endothelin-1 on hypertensive pulmonary arterial smooth muscle involves Rho-kinase and protein kinase C. Am J Physiol Lung Cell Mol Physiol 293: L472-L479, 2007.
8. Blumberg FC, Wolf K, Arzt M, Lorenz C, Riegger GAJ, Pfeifer M. Effects of ET-A receptor blockade on eNOS gene expression in chronic hypoxic rat lungs. J Appl Physiol 94: 446-452, 2003.
9. Bonnet S, Rochefort G, Sutendra G, Archer SL, Haromy A, Webster L, Hashimoto K, Bonnet SN, Michelakis ED. The nuclear factor of activated T cells in pulmonary arterial hypertension can be therapeutically targeted. PNAS 104: 11418-11423, 2007.
10. Bonvallet ST, Zamora MR, Hasunuma K, Sato K, Hanasato N, Anderson D, Sato K, Stelzner TJ. BQ123, an ETA-receptor antagonist, attenuates hypoxic pulmonary hypertension in rats. Am J Physiol Heart Circ Physiol 266: H1327-H1331, 1994.
11. Braz JC, Bueno OF, Liang Q, Wilkins BJ, Dai YS, Parsons S, Braunwart J, Glascock BJ, Klevitsky R, Kimball TF, Hewett TE, Molkentin JD. Targeted inhibition of p38 MAPK promotes hypertrophic cardiomyopathy through upregulation of calcineurin-NFAT signaling. J Clin Invest 111: 1475-1486, 2003.
12. Broughton BR, Walker BR, Resta TC. Chronic hypoxia induces Rho kinase-dependent myogenic tone in small pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 294: L797-L806, 2008.
13. 2+ sensitization in pulmonary vascular smooth muscle through superoxide-dependent stimulation of RhoA. Am J Physiol Lung Cell Mol Physiol 298: L232-L242, 2010.
14. Bubb MR, Senderowicz AM, Sausville EA, Duncan KL, Korn ED. Jasplakinolide, a cytotoxic natural product, induces actin polymerization and competitively inhibits the binding of phalloidin to F-actin. J Biol Chem 269: 14869-14871, 1994.
15. Chi AY, Waypa GB, Mungai PT, Schumacker PT. Prolonged hypoxia increases ROS signaling and RhoA activation in pulmonary artery smooth muscle and endothelial cells. Antioxid Redox Signal 12: 603-610, 2010.
16. Dai YP, Bongalon S, Mutafova-Yambolieva VN, Yamboliev IA. Distinct effects of contraction agonists on the phosphorylation state of cofilin in pulmonary artery smooth muscle. Adv Pharmacol Sci 2008: 362741, 2008.
17. De Frutos S, Caldwell E, Nitta CH, Kanagy NL, Wang J, Wang W, Walker MK, Gonzalez Bosc LV. NFATc3 contributes to intermittent hypoxia-induced arterial remodeling in mice. Am J Physiol Heart Circ Physiol 299: H356-H363, 2010.
18. De Frutos S, Duling L, Alo D, Berry T, Jackson-Weaver O, Walker M, Kanagy N, Gonzalez Bosc L. NFATc3 is required for intermittent hypoxia-induced hypertension. Am J Physiol Heart Circ Physiol 294: H2382-H2390, 2008.
19. De Frutos S, Nitta CH, Caldwell E, Friedman J, Gonzalez Bosc LV. Regulation of soluble guanylyl cyclase-α1 expression in chronic hypoxiainduced pulmonary hypertension: role of NFATc3 and HuR. Am J Physiol Lung Cell Mol Physiol 297: L475-L486, 2009.
20. De Frutos S, Spangler R, Alo D, Gonzalez Bosc LV. NFATc3 mediates chronic hypoxia-induced pulmonary arterial remodeling with α-actin upregulation. J Biol Chem 282: 15081-15089, 2007.
21. Dicarlo VS, Chen SJ, Meng QC, Durand J, Yano M, Chen YF, Oparil S. ETA-receptor antagonist prevents and reverses chronic hypoxia-induced pulmonary hypertension in rat. Am J Physiol Lung Cell Mol Physiol 269: L690-L697, 1995.
22. Eddahibi S, Raffestin B, Braquet P, Chabrier PE, Adnot S. Pulmonary vascular reactivity to endothelin-1 in normal and chronically pulmonary hypertensive rats. J Cardiovasc Pharmacol 17, Suppl 7: S358-S361, 1991.
23. Egermayer P, Town GI, Peacock AJ. Role of serotonin in the pathogenesis of acute and chronic pulmonary hypertension. Thorax 54: 161-168, 1999.
24. Esteve J, Launay JM, Kellermann O, Maroteaux L. Functions of serotonin in hypoxic pulmonary vascular remodeling. Cell Biochem Biophysics 47: 33-43, 2007.
25. Fagan KA, Oka M, Bauer NR, Gebb SA, Ivy DD, Morris KG, McMurtry IF. 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: L656-L664, 2004.
26. Fazal F, Bijli KM, Minhajuddin M, Rein T, Finkelstein JN, Rahman A. Essential role of cofilin-1 in regulating thrombin-induced RelA/p65 nuclear translocation and intercellular adhesion molecule 1 (ICAM-1) expression in endothelial cells. J Biol Chem 284: 21047-21056, 2009.
27. Ferri C, Bellini C, De Angelis C, De Siati L, Perrone A, Properzi G, Santucci A. Circulating endothelin-1 concentrations in patients with chronic hypoxia. J Clin Pathol 48: 519-524, 1995.
28. Fike CD, Slaughter JC, Kaplowitz MR, Zhang Y, Aschner JL. Reactive oxygen species from NADPH oxidase contribute to altered pulmonary vascular responses in piglets with chronic hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 295: L881-L888, 2008.
29. Filosa JA, Nelson MT, Gonzalez Bosc LV. Activity-dependent NFAT3 nuclear accumulation in pericytes from cortical parenchymal microvessel. Am J Physiol Cell Physiol 293: C1797-C1805, 2007.
30. Fujii T, Onohara N, Maruyama Y, Tanabe S, Kobayashi H, Fukutomi M, Nagamatsu Y, Nishihara N, Inoue R, Sumimoto H, Shibasaki F, Nagao T, Nishida M, Kurose H. Gα12/13-mediated Production of Reactive Oxygen Species Is Critical for Angiotensin Receptor-induced NFAT Activation in Cardiac Fibroblasts. J Biol Chem 280: 23041-23047, 2005.
31. Fujita H, Fukumoto Y, Saji K, Sugimura K, Demachi J, Nawata J, Shimokawa H. Acute vasodilator effects of inhaled fasudil, a specific Rho-kinase inhibitor, in patients with pulmonary arterial hypertension. Heart Vessels 25: 144-149, 2010.
32. 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 328: 1732-1739, 1993.
33. Gohla A, Schultz G, Offermanns S. Role for G(12)/G(13) in agonistinduced vascular smooth muscle cell contraction. Circ Res 87: 221-227, 2000.
34. 2+-dependent NFATc3 nuclear accumulation in vascular smooth muscle: role of JNK2 And Crm-1. J Biol Chem 278: 46847-46853, 2003.
35. Gomez MF, Stevenson AS, Bonev AD, Hill-Eubanks DC, Nelson MT. Opposing actions of inositol 1,4,5-trisphosphate and ryanodine receptors on nuclear factor of activated T-cells regulation in smooth muscle. J Biol Chem 277: 37756-37764, 2002.
36. Gonzalez Bosc LV, Wilkerson MK, Bradley KN, Eckman DM, Hill-Eubanks DC, Nelson MT. Intraluminal pressure is a stimulus for NFATc3 nuclear accumulation - Role of calcium, endothelium-derived nitric oxide, and cGMP-dependent protein kinase. J Biol Chem 279: 10702-10709, 2004.
37. Guignabert C, Izikki M, Tu LI, Li Z, Zadigue P, Barlier-Mur AM, Hanoun N, Rodman D, Hamon M, Adnot S, Eddahibi S. Transgenic mice overexpressing the 5-hydroxytryptamine transporter gene in smooth muscle develop pulmonary hypertension. Circ Res 98: 1323-1330, 2006.
38. Guilluy C, Sauzeau V, Rolli-Derkinderen M, Guerin P, Sagan C, Pacaud P, Loirand G. Inhibition of RhoA/Rho kinase pathway is involved in the beneficial effect of sildenafil on pulmonary hypertension. Br J Pharmacol 146: 1010-1018, 2005.
39. Gunst SJ, Zhang W. Actin cytoskeletal dynamics in smooth muscle: a new paradigm for the regulation of smooth muscle contraction. Am J Physiol Cell Physiol 295: C576-C587, 2008.
40. Hall A. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu Rev Cell Biol 10: 31-54, 1994.
41. Hill-Eubanks DC, Gomez MF, Stevenson AS, Nelson MT. NFAT regulation in smooth muscle. Trends Cardiovasc Med 13: 56-62, 2003.
42. Hirshman CA, Emala CW. Actin reorganization in airway smooth muscle cells involves Gq and Gi-2 activation of Rho. Am J Physiol Lung Cell Mol Physiol 277: L653-L661, 1999.
43. Hopkins N, McLoughlin P. The structural basis of pulmonary hypertension in chronic lung disease: remodelling, rarefaction or angiogenesis? J Anat 201: 335-348, 2002.
44. Iqbal J, Sanghia R, Das SK. Endothelin receptor antagonists: an overview of their synthesis and structure-activity relationship. Mini Rev MedChem 5: 381-408, 2005.
45. 2+ desensitization in pulmonary vascular smooth muscle through inhibition of RhoA/Rho kinase signaling. Am J Physiol Lung Cell Mol Physiol 287: L1220-L1229, 2004.
46. 2+ sensitization in pulmonary vascular smooth muscle following chronic hypoxia. Am J Physiol Lung Cell Mol Physiol 295: L515-L529, 2008.
47. Kalivendi SV, Konorev EA, Cunningham S, Vanamala SK, Kaji EH, Joseph J, Kalyanaraman B. Doxorubicin activates nuclear factor of activated T-lymphocytes and Fas ligand transcription: role of mitochondrial reactive oxygen species and calcium. Biochem J 389: 527-539, 2005.
48. Kawamura T, Ono K, Morimoto T, Akao M, Iwai-Kanai E, Wada H, Sowa N, Kita T, Hasegawa K. Endothelin-1-dependent nuclear factor of activated T lymphocyte signaling associates with transcriptional coactivator p300 in the activation of the B cell leukemia-2 promoter in cardiac myocytes. Circ Res 94: 1492-1499, 2004.
49. Ke Q, Li J, Ding J, Ding M, Wang L, Liu B, Costa M, Huang C. Essential role of ROS-mediated NFAT activation in TNF-α induction by crystalline silica exposure. Am J Physiol Lung Cell Mol Physiol 291: L257-L264, 2006.
50. Knappe D, Sill B, Tharun B, Koester R, Baldus S, Muenzel T, Meinertz T, Kahler J. Endothelin-1 in humans is increased by oxygenderived radicals ex vivo and in vivo. J Investig Med 55: 306-314, 2007.
51. Landsberg JW, Yuan JXJ. Calcium and TRP channels in pulmonary vascular smooth muscle cell proliferation. News Physiol Sci 19: 44-50, 2004.
52. Li KX, Fouty B, McMurtry IF, Rodman DM. Enhanced ETA-receptormediated inhibition of Kv channels in hypoxic hypertensive rat pulmonary artery myocytes. Am J Physiol Heart Circ Physiol 277: H363-H370, 1999.
53. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25: 402-408, 2001.
54. Lund AK, Goens MB, Kanagy NL, Walker MK. Cardiac hypertrophy in Aryl hydrocarbon receptor (AhR) null mice is correlated with elevated angiotensin II, endothelin-1 and mean arterial blood pressure. Hypertension 193: 177-187, 2003.
55. Miao L, Dai Y, Zhang J. Mechanism of RhoA/Rho kinase activation in endothelin-1- induced contraction in rabbit basilar artery. Am J Physiol Heart Circ Physiol 283: H983-H989, 2002.
56. Nagaoka T, Fagan KA, Gebb SA, Morris KG, Suzuki T, Shimokawa H, McMurtry IF, Oka M. Inhaled Rho kinase inhibitors are potent and selective vasodilators in rat pulmonary hypertension. Am J Respir Crit Care Med 171: 494-499, 2005.
57. Nagaoka T, Gebb SA, Karoor V, Homma N, Morris KG, McMurtry IF, Oka M. Involvement of RhoA/Rho kinase signaling in pulmonary hypertension of the fawn-hooded rat. J Appl Physiol 100: 996-1002, 2006.
58. Naik JS, Earley S, Resta TC, Walker BR. Pressure-induced smooth muscle cell depolarization in pulmonary arteries from control and chronically hypoxic rats does not cause myogenic vasoconstriction. J Appl Physiol 98: 1119-1124, 2005.
59. Negash S, Narasimhan SR, Zhou W, Liu J, Wei FL, Tian J, Raj JU. Role of cGMP-dependent protein kinase in regulation of pulmonary vascular smooth muscle cell adhesion and migration: effect of hypoxia. Am J Physiol Heart Circ Physiol 297: H304-H312, 2009.
60. Nieves-Cintron M, Amberg GC, Nichols CB, Molkentin JD, Santana LF. Activation of NFATC3 down-regulates the beta 1 subunit of large conductance, calcium-activated K+ channels in arterial smooth muscle and contributes to hypertension. J Biol Chem 282: 3231-3240, 2006.
61. Nilsson LM, Sun ZW, Nilsson J, Nordstrom I, Chen YW, Molkentin JD, Wide-Swensson D, Hellstrand P, Lydrup ML, Gomez MF. Novel blocker of NFAT activation inhibits IL-6 production in human myometrial arteries and reduces vascular smooth muscle cell proliferation. Am J Physiol Cell Physiol 292: C1167-C1178, 2007.
62. Oka M, Fagan KA, Jones PL, McMurtry IF. Therapeutic potential of RhoA/Rho kinase inhibitors in pulmonary hypertension. Br J Pharmacol 155: 444-454, 2008.
63. Oukka M, Ho IC, de la Brousse FC, Hoey T, Grusby MJ, Glimcher LH. The transcription factor NFAT4 is involved in the generation and survival of T cells. Immunity 9: 295-304, 1998.
64. Rabinovitch M, Gamble W, Nadas AS, Miettinen OS, Reid L. Rat pulmonary circulation after chronic hypoxia: hemodynamic and structural features. Am J Physiol Heart Circ Physiol 236: H818-H827, 1979.
65. Rao A, Luo C, Hogan PG. Transcription factors of the NFAT family: regulation and function. Annu Rev Immunol 15: 707-747, 1997.
66. Rattan S, Patel CA. Selectivity of ROCK inhibitors in the spontaneously tonic smooth muscle. Am J Physiol Gastrointest Liver Physiol 294: G687-G693, 2008.
67. Rivas FV, O'Keefe JP, Alegre ML, Gajewski TF. Actin cytoskeleton regulates calcium dynamics and NFAT nuclear duration. Mol Cell Biol 24: 1628-1639, 2004.
68. Shimoda LA, Sham JS, Sylvester JT. Altered pulmonary vasoreactivity in the chronically hypoxic lung. Physiol Res 49: 549-560, 2000.
69. 2+ by endothelin-1 in rat intrapulmonary arterial smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 278: L157-L164, 2000.
70. Shimoda LA, Sylvester JT, Sham JS. Inhibition of voltage-gated K+ current in rat intrapulmonary arterial myocytes by endothelin-1. Am J Physiol Lung Cell Mol Physiol 274: L842-L853, 1998.
71. Stevenson AS, Gomez MF, Hill-Eubanks DC, Nelson MT. NFAT4 movement in native smooth muscle. A role for differential Ca(2+) signaling. J Biol Chem 276: 15018-15024, 2001.
72. Strawbridge AB, Elmendorf JS. Phosphatidylinositol 4,5-bisphosphate reverses endothelin-1-induced insulin resistance via an actin-dependent mechanism. Diabetes 54: 1698-1705, 2005.
73. Suzuki E, Nishimatsu H, Satonaka H, Walsh K, Goto A, Omata M, Fujita T, Nagai R, Hirata Y. Angiotensin II induces myocyte enhancer factor 2- and calcineurin/nuclear factor of activated T Cell-dependent transcriptional activation in vascular myocytes. Circ Res 90: 1004-1011, 2002.
74. Tang DD, Anfinogenova Y. Physiologic properties and regulation of the actin cytoskeleton in vascular smooth muscle. J Cardiovasc Pharmacol Therap 13: 130-140, 2008.
75. Tjen AL, Ekman R, Osborn J, Keith I. Pulmonary vascular pressure effects by endothelin-1 in normoxia and chronic hypoxia: a longitudinal study. Am J Physiol Heart Circ Physiol 271: H2246-H2253, 1996.
76. Vega Lde L, Munóz E, Calzado MA, Lieb K, Candelario-Jalil E, Gschaidmeir H, Färber L, Mueller W, Stratz T, Fiebich BL. The 5-HT3 receptor antagonist tropisetron inhibits T cell activation by targeting the calcineurin pathway. Biochem Pharmacol 70: 369-380, 2005.
77. Vigorito E, Billadeu DD, Savoy D, McAdam S, Doody G, Fort P, Turner M. RhoG regulates gene expression and the actin cytoskeleton in lymphocytes. Oncogene 22: 330-342, 2003.
78. Vindis C, D'Angelo R, Mucher E, N-gre-Salvayre A, Parini A, Mialet-Perez J. Essential role of TRPC1 channels in cardiomyoblasts hypertrophy mediated by 5-HT2A serotonin receptors. Biochem Biophys Res Commun 391: 979-983, 2010.
79. Weigand L, Sylvester JT, Shimoda LA. Mechanisms of endothelin-1-induced contraction in pulmonary arteries from chronically hypoxic rats. Am J Physiol Lung Cell Mol Physiol 290: L284-L290, 2006.
80. Yaghi A, Sims SM. Constrictor-induced translocation of NFAT3 in human and rat pulmonary artery smooth muscle. Am J Physiol Lung Cell Mol Physiol 289: L1061-L1074, 2005.
81. Yang X, Chen W, Chen J. Change of level and expression of endothelin-1 in the lungs of rats with hypoxic pulmonary hypertension [published erratum appears in Chin Med J (Engl) 1997 Mar;110(3):186]. Chin Med J (Engl) 110: 104-108, 1997.
82. Yang Y, Gao M, Guo Y, Qiao J. Calcium antagonists, diltiazem and nifedipine, protect broilers against low temperature-induced pulmonary hypertension and pulmonary vascular remodeling. Anim Sci J 81: 494-500, 2010.
83. Yuyama H, Fujimori A, Sanagi M, Koakutsu A, Noguchi Y, Sudoh K, Sasamata M, Miyata K. A novel and selective endothelin ETA receptor antagonistYM598 prevents the development of chronic hypoxia-induced pulmonary hypertension in rats. Vasc Pharmacol 43: 40-46, 2005.
84. Zhang N, Agbor LN, Scott JA, Zalobowski T, Elased KM, Trujillo A, Duke MS, Wolf V, Walsh MT, Born JL, Felton LA, Wang J, Wang W, Kanagy NL, Walker MK. An activated renin-angiotensin system maintains normal blood pressure in aryl hydrocarbon receptor heterozygous mice but not in null mice. Biochem Pharmacol 80: 197-204, 2010.
85. Ziino AJA, Ivanovska J, Belcastro R, Kantores C, Xu EZ, Lau M, McNamara PJ, Tanswell AK, Jankov RP. Effects of Rho-kinase inhibition on pulmonary hypertension, lung growth, and structure in neonatal rats chronically exposed to hypoxia. Pediatr Res 67: 177-182, 2010.