Chronic hypoxia selectively enhances L- and T-type voltage-dependent Ca2+ channel activity in pulmonary artery by upregulating Cav1.2 and Cav3.2

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 305, Issue 2, 2013, Pages

  Wan, Jun ^a,b   Yamamura, Aya ^a   Zimnicka, Adriana M ^a   Voiriot, Guillaume ^a   Smith, Kimberly A ^a   Tang, Haiyang ^a   Ayon, Ramon J ^a   Choudhury, Moumita S R ^a   Ko, Eun A ^a   Wang, Jun ^b   Wang, Chen ^b,c   Makino, Ayako ^a   Yuan, Jason X J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b CAPITAL MEDICAL UNIVERSITY   (China)

^c BEIJING HOSPITAL   (China)

Author keywords

Calcium channel voltage dependent L type 1C subunit; Calcium channel voltage dependent T type 1H subunit; Hypoxia; Mouse; Pulmonary artery; Voltage dependent calcium ion channel

Indexed keywords

CALCIUM CHANNEL; CALCIUM CHANNEL CAV1.2; CALCIUM CHANNEL CAV3.2; CALCIUM CHANNEL L TYPE; CALCIUM CHANNEL T TYPE; MIBEFRADIL; NIFEDIPINE; OMEGA AGATOXIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CELL PROLIFERATION; CONTROLLED STUDY; HEART HEMODYNAMICS; HEART RIGHT VENTRICLE HYPERTROPHY; HISTOPATHOLOGY; HYPOXIA; IMMUNOHISTOCHEMISTRY; LUNG VASOCONSTRICTION; MALE; MESENTERIC ARTERY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; UPREGULATION;

CALCIUM CHANNEL VOLTAGE-DEPENDENT L-TYPE Α1C-SUBUNIT; CALCIUM CHANNEL VOLTAGE-DEPENDENT T-TYPE Α1H-SUBUNIT; HYPOXIA; MOUSE; PULMONARY ARTERY; VOLTAGE-DEPENDENT CALCIUM ION CHANNEL;

15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; 3-PYRIDINECARBOXYLIC ACID, 1,4-DIHYDRO-2,6-DIMETHYL-5-NITRO-4-(2-(TRIFLUOROMETHYL)PHENYL)-, METHYL ESTER; ANIMALS; ANOXIA; CALCIUM; CALCIUM CHANNEL AGONISTS; CALCIUM CHANNELS, L-TYPE; CALCIUM CHANNELS, T-TYPE; CHRONIC DISEASE; GENE EXPRESSION REGULATION; MALE; MESENTERIC ARTERIES; MICE; POTASSIUM; PULMONARY ARTERY; TIME FACTORS; VASOCONSTRICTOR AGENTS; VASODILATION;

EID: 84880159429     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00313.2012     Document Type: Article

References (65)

1. Abud EM, Maylor J, Undem C, Punjabi A, Zaiman AL, Myers AC, Sylvester JT, Semenza GL, Shimoda LA. Digoxin inhibits development of hypoxic pulmonary hypertension in mice. Proc Natl Acad Sci USA 109: 1239-1244, 2012.
2. Akaike N, Kostyuk P, Osipchuk Y. Dihydropyridine-sensitive lowthreshold calcium channels in isolated rat hypothalamic neurones. J Physiol 412: 181-195, 1989.
3. 2+ current of mouse spermatogenic cells. Mol Pharmacol 53: 1104-1111, 1998.
4. Barst RJ. Recent advances in the treatment of pediatric pulmonary artery hypertension. Pediatr Clin North Am 46: 331-345, 1999.
5. Bonnet S, Dubuis E, Vandier C, Martin S, Marthan R, Savineau JP. Reversal of chronic hypoxia-induced alterations in pulmonary artery smooth muscle electromechanical coupling upon air breathing. Cardiovasc Res 53: 1019-1028, 2002.
6. Bonnet S, Hyvelin JM, Bonnet P, Marthan R, Savineau JP. Chronic hypoxia-induced spontaneous and rhythmic contractions in the rat main pulmonary artery. Am J Physiol Lung Cell Mol Physiol 281: L183-L192, 2001.
7. Cahill E, Rowan S, Sands M, Banahan M, Ryan D, Howell K, McLoughlin P. The pathophysiological basis of chronic hypoxic pulmonary hypertension in the mouse: vasoconstrictor and structural mechanisms contribute equally. Exp Physiol 97: 796-806, 2012.
8. Chaouat A, Bugnet AS, Kadaoui N, Schott R, Enache I, Ducolone A, Ehrhart M, Kessler R, Weitzenblum E. Severe pulmonary hypertension and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 172: 189-194, 2005.
9. Chen WS, Li XQ, Cao W, Xiao X, Dong L, Zhang JZ. Vardenafil ameliorates calcium mobilization in pulmonary artery smooth muscle cells from hypoxic pulmonary hypertensive mice. Arch Med Res 43: 265-273, 2012.
10. + channels and pulmonary vasoconstriction. Circ Res 93: 656-663, 2003.
11. + channels. Am J Physiol Lung Cell Mol Physiol 281: L1-L12, 2001.
12. Davidson A, Bossuyt A, Dab I. Acute effects of oxygen, nifedipine, and diltiazem in patients with cystic fibrosis and mild pulmonary hypertension. Pediatr Pulmonol 6: 53-59, 1989.
13. Fike CD, Kaplowitz MR. Nifedipine inhibits pulmonary hypertension but does not prevent decreased lung eNOS in hypoxic newborn pigs. Am J Physiol Lung Cell Mol Physiol 277: L449-L456, 1999.
14. Firth A, Remillard C, Platoshyn O, Fantozzi I, Ko E, Yuan J. Functional ion channels in human pulmonary artery smooth muscle cells: Voltage-dependent cation channels. Pulm Circ 1: 48-71, 2011.
15. Fishman AP. Hypoxia on the pulmonary circulation. How and where it acts. Circ Res 38: 221-231, 1976.
16. Fleischmann BK, Murray RK, Kotlikoff MI. Voltage window for sustained elevation of cytosolic calcium in smooth muscle cells. Proc Natl Acad Sci USA 91: 11914-11918, 1994.
17. Galie N, Hoeper MM, Humbert M, Torbicki A, Vachiery JL, Barbera JA, Beghetti M, Corris P, Gaine S, Gibbs JS, Gomez-Sanchez MA, Jondeau G, Klepetko W, Opitz C, Peacock A, Rubin L, Zellweger M, Simonneau G. Guidelines for the diagnosis and treatment of pulmonary hypertension. Eur Respir J 34: 1219-1263, 2009.
18. Hansen PB, Poulsen CB, Walter S, Marcussen N, Cribbs LL, Skott O, Jensen BL. Functional importance of L-and P/Q-type voltage-gated calcium channels in human renal vasculature. Hypertension 58: 464-470, 2011.
19. 2+-dependent action potentials in small pulmonary arteries of the cat. J Appl Physiol 59: 1389-1393, 1985.
20. 2+ channels. Jpn J Pharmacol 85: 339-350, 2001.
21. 2+ current in rat clonal (GH3) pituitary cells. J Neurophysiol 68: 213-232, 1992.
22. Hirenallur SD, Detweiler N, Haworth S, Leming J, Gordon J, Rusch N. Furegrelate, a thromboxane synthase inhibitor, blunts the development of pulmonary arterial hypertension in neonatal piglets. Pulm Circ 2: 193-200, 2012.
23. Hirenallur SDK, Haworth ST, Leming JT, Chang J, Hernandez G, Gordon JB, Rusch NJ. Upregulation of vascular calcium channels in neonatal piglets with hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 295: L915-L924, 2008.
24. Kennedy TP, Michael JR, Summer W. Calcium channel blockers in hypoxic pulmonary hypertension. Am J Med 78: 18-26, 1985.
25. 2+ channels in mouse pulmonary arterial smooth muscle cells: divergent effect of ROS. Am J Physiol Cell Physiol. doi:10.1152/ajpcell.00304.2012.
26. 2+ currents in rat aortic smooth muscle cells in primary culture. Circ Res 79: 14-19, 1996.
27. 2+ signaling. Am J Physiol Heart Circ Physiol 302: H1546-H1562, 2012.
28. Leach RM, Robertson TP, Twort CH, Ward JP. Hypoxic vasoconstriction in rat pulmonary and mesenteric arteries. Am J Physiol Lung Cell Mol Physiol 266: L223-L231, 1994.
29. 2+ channels in pulmonary arterial smooth muscle cells: a novel mechanism of hypoxic pulmonary hypertension. Circ Res 95: 496-505, 2004.
30. Maci'a M, Lozano R, Villarroya M, Garci'a AG, Ruiz-Torres A. On the antiatherogenity of calcium channel blockers: studies in proliferating vascular smooth muscle cells on age sensitivity, dose dependent inhibitory effect, and time of action. Arch Gerontol Geriatr 35: 51-57, 2002.
31. Madden JA, Dawson CA, Harder DR. Hypoxia-induced activation in small isolated pulmonary arteries from the cat. J Appl Physiol 59: 113-118, 1985.
32. Madden JA, Vadula MS, Kurup VP. Effects of hypoxia and other vasoactive agents on pulmonary and cerebral artery smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 263: L384-L393, 1992.
33. Marshall C, Mamary AJ, Verhoeven AJ, Marshall BE. Pulmonary artery NADPH-oxidase is activated in hypoxic pulmonary vasoconstriction. Am J Respir Cell Mol Biol 15: 633-644, 1996.
34. 2+ channels by Ro 40-5967. Circ Res 75: 144-148, 1994.
35. Murray TR, Chen L, Marshall BE, Macarak EJ. Hypoxic contraction of cultured pulmonary vascular smooth muscle cells. Am J Respir Cell Mol Biol 3: 457-465, 1990.
36. Oswald-Mammosser M, Weitzenblum E, Quoix E, Moser G, Chaouat A, Charpentier C, Kessler R. Prognostic factors in COPD patients receiving long-term oxygen therapy. Importance of pulmonary artery pressure. Chest 107: 1193-1198, 1995.
37. Peinado VI, Pizarro S, Barbera JA. Pulmonary vascular involvement in COPD. Chest 134: 808-814, 2008.
38. 2+]i signal stimulated by thromboxane A2 is partially resistant to NO. Pediatr Res 50: 508-514, 2001.
39. Platoshyn O, Brevnova EE, Burg ED, Yu Y, Remillard CV, Yuan JX. Acute hypoxia selectively inhibits KCNA5 channels in pulmonary artery smooth muscle cells. Am J Physiol Cell Physiol 290: C907-C916, 2006.
40. Platoshyn O, Yu Y, Golovina VA, McDaniel SS, Krick S, Li L, Wang JY, Rubin LJ, Yuan JX. Chronic hypoxia decreases KV channel expression and function in pulmonary artery myocytes. Am J Physiol Lung Cell Mol Physiol 280: L801-L812, 2001.
41. + channels in canine pulmonary artery. Novel mechanism for hypoxia-induced membrane depolarization. Circ Res 77: 131-139, 1995.
42. Post JM, Hume JR, Archer SL, Weir EK. Direct role for potassium channel inhibition in hypoxic pulmonary vasoconstriction. Am J Physiol Cell Physiol 262: C882-C890, 1992.
43. Rich S, Kaufmann E, Levy PS. The effect of high doses of calciumchannel blockers on survival in primary pulmonary hypertension. N Engl J Med 327: 76-81, 1992.
44. Rodman D, Reese K, Harral J, Fouty B, Wu S, West J, Hoedt-Miller M, Tada Y, Li KX, Cool C, Fagan K, Cribbs L. Low-voltage-activated (T-type) calcium channels control proliferation of human pulmonary artery myocytes. Circ Res 96: 864-872, 2005.
45. Roe M, Lemasters J, Herman B. Assessment of Fura-2 for measurements of cytosolic free calcium. Cell Calcium 11: 63-73, 1990.
46. Schermuly RT, Dony E, Ghofrani HA, Pullamsetti S, Savai R, Roth M, Sydykov A, Lai YJ, Weissmann N, Seeger W, Grimminger F. Reversal of experimental pulmonary hypertension by PDGF inhibition. J Clin Invest 115: 2811-2821, 2005.
47. 2+]i, and ET-1-induced responses in chronically hypoxic pulmonary myocytes. Am J Physiol Lung Cell Mol Physiol 279: L884-L894, 2000.
48. Somlyo AP, Somlyo AV. Signal transduction by G-proteins, Rho-kinase and protein phosphatase to smooth muscle and non-muscle myosin II. J Physiol 522: 177-185, 2000.
49. Sung JY, Choi HC. Nifedipine inhibits vascular smooth muscle cell proliferation and reactive oxygen species production through AMP-activated protein kinase signaling pathway. Vasc Pharmacol 56: 1-8, 2012.
50. 2+ channels in mesenteric veins: mechanism of venous smooth muscle resistance to calcium channel blockers. Circ Res 106: 739-747, 2010.
51. 2+ channels in thromboxane A2 receptormediated contraction in rat aorta. J Pharmacol Exp Ther 284: 921-928, 1998.
52. Viana F, Van den Bosch L, Missiaen L, Vandenberghe W, Droogmans G, Nilius B, Robberecht W. Mibefradil (Ro 40-5967) blocks multiple types of voltage-gated calcium channels in cultured rat spinal motoneurones. Cell Calcium 22: 299-311, 1997.
53. + channel alpha subunits in pulmonary artery smooth muscle cells. J Clin Invest 100: 2347-2353, 1997.
54. Wang J, Weigand L, Wang W, Sylvester JT, Shimoda LA. Chronic hypoxia inhibits Kv channel gene expression in rat distal pulmonary artery. Am J Physiol Lung Cell Mol Physiol 288: L1049-L1058, 2005.
55. Wu JR, Liou SF, Lin SW, Chai CY, Dai ZK, Liang JC, Chen IJ, Yeh JL. Lercanidipine inhibits vascular smooth muscle cell proliferation and neointimal formation via reducing intracellular reactive oxygen species and inactivating Ras-ERK1/2 signaling. Pharmacol Res 59: 48-56, 2009.
56. 2+ currents in pancreatic beta-cells. J Pharmacol Exp Ther 292: 939-943, 2000.
57. Xu M, Platoshyn O, Makino A, Dillmann WH, Akassoglou K, Remillard CV, Yuan JX. Characterization of agonist-induced vasoconstriction in mouse pulmonary artery. Am J Physiol Heart Circ Physiol 294: H220-H228, 2008.
58. Yamamoto Y, Koike K. α1-Adrenoceptor subtypes in the mouse mesenteric artery and abdominal aorta. Brit J Pharmacol 134: 1045-1054, 2001.
59. 2+-sensing receptor function in idiopathic pulmonary arterial hypertension. Circ Res 111: 469-481, 2012.
60. Yoo H, Park S, Seo EY, Park K, Han JA, Kim K, Shin D, Earm Y, Zhang YH, Kim S. Role of thromboxane A2-activated nonselective cation channels in hypoxic pulmonary vasoconstriction of rat. Am J Physiol Cell Physiol 302: C307-C317, 2012.
61. + channels in pulmonary artery smooth muscle cells of patients with primary pulmonary hypertension. Circulation 98: 1400-1406, 1998.
62. 2+]i in pulmonary arterial myocytes. Circ Res 77: 370-378, 1995.
63. Yuan XJ, Goldman WF, Tod ML, Rubin LJ, Blaustein MP. Hypoxia reduces potassium currents in cultured rat pulmonary but not mesenteric arterial myocytes. Am J Physiol Lung Cell Mol Physiol 264: L116-L123, 1993.
64. Yuan XJ, Tod ML, Rubin LJ, Blaustein MP. Contrasting effects of hypoxia on tension in rat pulmonary and mesenteric arteries. Am J Physiol Heart Circ Physiol 259: H281-H289, 1990.
65. + channel gene transcription in primary pulmonary hypertension. Lancet 351: 726-727, 1998.