Effect of chronic perinatal hypoxia on the role of rho-kinase in pulmonary artery contraction in newborn lambs

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 304, Issue 2, 2013, Pages

  Blood, Arlin B ^a   Terry, Michael H ^b   Merritt, Travis A ^a   Papamatheakis, Demosthenes G ^c   Blood, Quintin ^a   Ross, Jonathon M ^a   Power, Gordon G ^a   Longo, Lawrence D ^a   Wilson, Sean M ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOMA LINDA UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO HEALTH SYSTEM   (United States)

Author keywords

Hypoxic pulmonary vasoconstriction; Rho kinase

Indexed keywords

CALCIUM CHANNEL L TYPE; RHO KINASE; SEROTONIN;

ALTITUDE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERIAL PH; ARTERY CONSTRICTION; ARTICLE; CARDIOPULMONARY HEMODYNAMICS; CONTROLLED STUDY; EXTRACELLULAR CALCIUM; FEMALE; GESTATIONAL AGE; HYPOXIC LUNG VASOCONSTRICTION; IN VITRO STUDY; INHIBITION KINETICS; LAMB; LUNG ARTERY PRESSURE; MALE; NEWBORN; NEWBORN HYPOXIA; NEWBORN PERIOD; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PULMONARY ARTERY; PULMONARY ARTERY OCCLUSION PRESSURE; VASCULAR RESISTANCE;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ALTITUDE; ANIMALS; ANIMALS, NEWBORN; ARTERIAL PRESSURE; CALCIUM CHANNEL BLOCKERS; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FETAL HYPOXIA; GESTATIONAL AGE; HUMANS; INFANT, NEWBORN; PERSISTENT FETAL CIRCULATION SYNDROME; PROTEIN KINASE INHIBITORS; PULMONARY ARTERY; RHO-ASSOCIATED KINASES; SEROTONIN; SHEEP; TIME FACTORS; VASOCONSTRICTION; VASOCONSTRICTOR AGENTS;

EID: 84872367915     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00126.2012     Document Type: Article

References (76)

1. 2+ sensitization by PKC and rho proteins in ovine cerebral arteries: effects of artery size and age. Am J Physiol Heart Circ Physiol 275: H930-H939, 1998.
2. Badejo AM Jr, Dhaliwal JS, Casey DB, Gallen TB, Greco AJ, Kadowitz PJ. Analysis of pulmonary vasodilator responses to the Rho-kinase inhibitor fasudil in the anesthetized rat. Am J Physiol Lung Cell Mol Physiol 295: L828-L836, 2008.
3. 2+ exchange inhibitor 2-(2-(4-(4-nitrobenzyloxy)phenyl)ethyl)isothiourea methanesulfonate (KB-R7943) also blocks ryanodine receptors type 1 (RyR1) and type 2 (RyR2) channels. Mol Pharmacol 76: 560-568, 2009.
4. Clapham D, Nilius B, Owsianik G. Transient receptor potential channels. IUPHAR database (IUPHAR-DB), http://www.iuphar-db.org/DATABASE/FamilyMenuForward?familyId=78, 2010.
5. 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.
6. Fike CD, Kaplowitz MR. Effect of chronic hypoxia on pulmonary vascular pressures in isolated lungs of newborn pigs. J Appl Physiol 77: 2853-2862, 1994.
7. 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.
8. Fukumoto Y, Matoba T, Ito A, Tanaka H, Kishi T, Hayashidani S, Abe K, Takeshita A, Shimokawa H. Acute vasodilator effects of a Rho-kinase inhibitor, fasudil, in patients with severe pulmonary hypertension. Heart 91: 391-392, 2005.
9. Gao Y, Portugal AD, Liu J, Negash S, Zhou W, Tian J, Xiang R, Longo LD, Raj JU. Preservation of cGMP-induced relaxation of pulmonary veins of fetal lambs exposed to chronic high altitude hypoxia: role of PKG and Rho kinase. Am J Physiol Lung Cell Mol Physiol 295: L889-L896, 2008.
10. Gao Y, Portugal AD, Negash S, Zhou W, Longo LD, Usha Raj J. 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: L678-L684, 2007.
11. Goyal R, Creel KD, Chavis E, Smith GD, Longo LD, Wilson SM. Maturation of intracellular calcium homeostasis in sheep pulmonary arterial smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 295: L905-L914, 2008.
12. 2+ entry during serotoninmediated contractility in fetal ovine pulmonary arteries. Reprod Sci 18: 948-962, 2011.
13. Greenlees KJ, Tucker A. Hypoxic pressor responses in lungs from rats acutely exposed to simulated high altitude. Respiration 45: 169-174, 1984.
14. Guibert C, Marthan R, Savineau JP. 5-HT induces an arachidonic acid-sensitive calcium influx in rat small intrapulmonary artery. Am J Physiol Lung Cell Mol Physiol 286: L1228-L1236, 2004.
15. Guilluy C, Rolli-Derkinderen M, Tharaux PL, Melino G, Pacaud P, Loirand G. Transglutaminase-dependent RhoA activation and depletion by serotonin in vascular smooth muscle cells. J Biol Chem 282: 2918-2928, 2007.
16. Haworth SG, Hislop AA. Effect of hypoxia on adaptation of the pulmonary circulation to extra-uterine life in the pig. Cardiovasc Res 16: 293-303, 1982.
17. Herrera EA, Pulgar VM, Riquelme RA, Sanhueza EM, Reyes RV, Ebensperger G, Parer JT, Valdez EA, Giussani DA, Blanco CE, Hanson MA, Llanos AJ. High-altitude chronic hypoxia during gestation and after birth modifies cardiovascular responses in newborn sheep. Am J Physiol Regul Integr Comp Physiol 292: R2234-R2240, 2007.
18. Herrera EA, Riquelme RA, Ebensperger G, Reyes RV, Ulloa CE, Cabello G, Krause BJ, Parer JT, Giussani DA, Llanos AJ. Long-term exposure to high-altitude chronic hypoxia during gestation induces neonatal pulmonary hypertension at sea level. Am J Physiol Regul Integr Comp Physiol 299: R1676-R1684, 2010.
19. Homma N, Nagaoka T, Morio Y, Ota H, Gebb SA, Karoor V, McMurtry IF, Oka M. Endothelin-1 and serotonin are involved in activation of RhoA/Rho kinase signaling in the chronically hypoxic hypertensive rat pulmonary circulation. J Cardiovasc Pharm 50: 697-702, 2007.
20. Hunter CJ, Dejam A, Blood AB, Shields H, Kim-Shapiro DB, Machado RF, Tarekegn S, Mulla N, Hopper AO, Schechter AN, Power GG, Gladwin MT. Inhaled nebulized nitrite is a hypoxia-sensitive NO-dependent selective pulmonary vasodilator. Nature Med 10: 1122-1127, 2004.
21. Hyvelin JM, Howell K, Nichol A, Costello CM, Preston RJ, McLoughlin P. Inhibition of Rho-kinase attenuates hypoxia-induced angiogenesis in the pulmonary circulation. Circ Res 97: 185-191, 2005.
22. Ishikura K, Yamada N, Ito M, Ota S, Nakamura M, Isaka N, Nakano T. Beneficial acute effects of rho-kinase inhibitor in patients with pulmonary arterial hypertension. Circ J 70: 174-178, 2006.
23. Janssen LJ, Lu-Chao H, Netherton S. Excitation-contraction coupling in pulmonary vascular smooth muscle involves tyrosine kinase and Rho kinase. Am J Physiol Lung Cell Mol Physiol 280: L666-L674, 2001.
24. Kantores C, McNamara PJ, Teixeira L, Engelberts D, Murthy P, Kavanagh BP, Jankov RP. Therapeutic hypercapnia prevents chronic hypoxia-induced pulmonary hypertension in the newborn rat. Am J Physiol Lung Cell Mol Physiol 291: L912-L922, 2006.
25. 2+ exchange inhibitor. Ann NY Acad Sci 1099: 529-533, 2007.
26. Knock GA, Snetkov VA, Shaifta Y, Drndarski S, Ward JP, Aaronson PI. Role of src-family kinases in hypoxic vasoconstriction of rat pulmonary artery. Cardiovasc Res, 2008.
27. 2+]i oscillations underlying tonic contraction in the rabbit inferior vena cava. J Physiol 534: 641-650, 2001.
28. Li F, Xia W, Yuan S, Sun R. Acute inhibition of Rho-kinase attenuates pulmonary hypertension in patients with congenital heart disease. Pediatr Cardiol 30: 363-366, 2009.
29. Li F, Xia W, Yuan S, Sun R. Acute inhibition of Rho-kinase attenuates pulmonary hypertension in patients with congenital heart disease. Pediatr Cardiol 30: 363-366, 2009.
30. Liao P, Yu D, Li G, Yong TF, Soon JL, Chua YL, Soong TW. A smooth muscle Cav1.2 calcium channel splice variant underlies hyperpolarized window current and enhanced state-dependent inhibition by nifedipine. J Biol Chem 282: 35133-35142, 2007.
31. MacLean MR, Sweeney G, Baird M, McCulloch KM, Houslay M, Morecroft I. 5-Hydroxytryptamine receptors mediating vasoconstriction in pulmonary arteries from control and pulmonary hypertensive rats. Br J Pharm 119: 917-930, 1996.
32. Mair KM, MacLean MR, Morecroft I, Dempsie Y, Palmer TM. Novel interactions between the 5-HT transporter, 5-HT1B receptors and Rho kinase in vivo and in pulmonary fibroblasts. Br J Pharm 155: 606-616, 2008.
33. McMurtry IF, Abe K, Ota H, Fagan KA, Oka M. Rho kinase-mediated vasoconstriction in pulmonary hypertension. Adv Expt Med Biol 661: 299-308, 2010.
34. McMurtry IF, Petrun MD, Reeves JT. Lungs from chronically hypoxic rats have decreased pressor response to acute hypoxia. Am J Physiol Heart Circ Physiol 235: H104-H109, 1978.
35. McNamara PJ, Murthy P, Kantores C, Teixeira L, Engelberts D, van Vliet T, Kavanagh BP, Jankov RP. Acute vasodilator effects of Rhokinase inhibitors in neonatal rats with pulmonary hypertension unresponsive to nitric oxide. Am J Physiol Lung Cell Mol Physiol 294: L205-L213, 2008.
36. Merritt JE, Armstrong WP, Benham CD, Hallam TJ, Jacob R, Jaxa-Chamiec A, Leigh BK, McCarthy SA, Moores KE, Rink TJ. SK and F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem J 271: 515-522, 1990.
37. 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.
38. Nagaoka T, Morio Y, Casanova N, Bauer N, Gebb S, McMurtry I, Oka M. Rho/Rho kinase signaling mediates increased basal pulmonary vascular tone in chronically hypoxic rats. Am J Physiol Lung Cell Mol Physiol 287: L665-L672, 2004.
39. 2+ entry pathways activated by store depletion or hypoxia in canine pulmonary arterial smooth muscle cells. Am J Physiol Cell Physiol 294: C313-C323, 2008.
40. 2+ entry in mouse pulmonary arterial smooth muscle cells. J Physiol 587: 2429-2442, 2009.
41. 2+ entry in isolated canine pulmonary arterial smooth muscle cells. J Physiol 563: 409-419, 2005.
42. 2+ entry by store depletion or hypoxia in canine pulmonary arterial smooth muscle cells. Br J Pharm 152: 101-111, 2007.
43. Niermeyer S. Cardiopulmonary transition in the high altitude infant. High Alt Med Biol 4: 225-239, 2003.
44. Niermeyer S, Andrade Mollinedo P, Huicho L. Child health and living at high altitude. Arch Dis Child 94: 806-811, 2009.
45. Niermeyer S, Moore LG. Hypoxic responses in infants. No known mechanism links hypoxia and sudden infant death syndrome. Br Med J 317: 675-676; author reply 677-678, 1998.
46. 2+ exchange inhibitor on membrane currents in guinea pig ventricular myocytes. Ann N Y Acad Sci 1099: 534-539, 2007.
47. 2+ exchange inhibitor in guinea pig cardiac ventricular myocytes. Eur J Pharmacol 573: 161-169, 2007.
48. Papamatheakis DG, Patel JJ, Blood Q, Merritt TT, Longo LD, Wilson SM. Depolarization-dependent contraction increase after birth and preservation following long-term hypoxia in sheep pulmonary arteries. Pulm Circ 2: 41-53, 2012.
49. Papamatheakis DG, Vemulakonda S, Blood Q, Goyal R, Rubalcava M, Vrancken K, Bennett A, Dawson A, Osman NJ, Blood AB, Pearce WJ, Longo LD, Wilson SM. Preservation of serotonin-mediated contractility in adult sheep pulmonary arteries following long-term high-altitude hypoxia. High Alt Med Biol 12: 253-264, 2011.
50. Parker TA, Roe G, Grover TR, Abman SH. Rho kinase activation maintains high pulmonary vascular resistance in the ovine fetal lung. Am J Physiol Lung Cell Mol Physiol 291: L976-L982, 2006.
51. 2+ entry in purinergically stimulated aorta smooth muscle cells. Circ Res 101: 1030-1038, 2007.
52. Ramsey IS, Delling M, Clapham DE. An introduction to TRP channels. Ann Rev Physiol 68: 619-647, 2006.
53. 2+ sensitization during sustained hypoxic pulmonary vasoconstriction is endothelium dependent. Am J Physiol Lung Cell Mol Physiol 284: L1121-L1126, 2003.
54. 2+ sensitization. Am J Physiol Heart Circ Physiol 268: H301-H307, 1995.
55. Robertson TP, Dipp M, Ward JP, Aaronson PI, Evans AM. Inhibition of sustained hypoxic vasoconstriction by Y-27632 in isolated intrapulmonary arteries and perfused lung of the rat. Br J Pharm 131: 5-9, 2000.
56. Rodat L, Savineau JP, Marthan R, Guibert C. Effect of chronic hypoxia on voltage-independent calcium influx activated by 5-HT in rat intrapulmonary arteries. Pflügers Arch 454: 41-51, 2007.
57. 2+-dependent activation of Rho and Rho kinase in membrane depolarization-induced and receptor stimulation-induced vascular smooth muscle contraction. Circ Res 93: 548-556, 2003.
58. Satoh S, Takayasu M, Kawasaki K, Ikegaki I, Hitomi A, Yano K, Shibuya M, Asano T. Antivasospastic effects of hydroxyfasudil, a Rhokinase inhibitor, after subarachnoid hemorrhage. J Pharmacol Sci 118: 92-98, 2012.
59. Shibuya M, Suzuki Y, Sugita K, Saito I, Sasaki T, Takakura K, Nagata I, Kikuchi H, Takemae T, Hidaka H, Nakashima M. Effect of AT877 on cerebral vasospasm after aneurysmal subarachnoid hemorrhage. J Neurosurg 76: 571-577, 1992.
60. Shimokawa H, Seto M, Katsumata N, Amano M, Kozai T, Yamawaki T, Kuwata K, Kandabashi T, Egashira K, Ikegaki I, Asano T, Kaibuchi K, Takeshita A. Rho-kinase-mediated pathway induces enhanced myosin light chain phosphorylations in a swine model of coronary artery spasm. Cardiovasc Res 43: 1029-1039, 1999.
61. 2+ sensitivity of smooth muscle and nonmuscle myosin II: modulated by G proteins, kinases, and myosin phosphatase. Physiol Rev 83: 1325-1358, 2003.
62. Stenmark KR, Durmowicz AG, Roby JD, Mecham RP, Parks WC. Persistence of the fetal pattern of tropoelastin gene expression in severe neonatal bovine pulmonary hypertension. J Clin Invest 93: 1234-1242, 1994.
63. Sylvester JT, Shimoda LA, Aaronson PI, Ward JP. Hypoxic pulmonary vasoconstriction. Physiol Rev 92: 367-520, 2012.
64. Takahara A, Sugiyama A, Satoh Y, Yoneyama M, Hashimoto K. Cardiovascular effects of Y-27632, a selective Rho-associated kinase inhibitor, assessed in the halothane-anesthetized canine model. Euro J Pharm 460: 51-57, 2003.
65. Walsh-Sukys MC, Tyson JE, Wright LL, Bauer CR, Korones SB, Stevenson DK, Verter J, Stoll BJ, Lemons JA, Papile LA, Shankaran S, Donovan EF, Oh W, Ehrenkranz RA, Fanaroff AA. Persistent pulmonary hypertension of the newborn in the era before nitric oxide: practice variation and outcomes. Pediatrics 105: 14-20, 2000.
66. Wang J, Shimoda LA, Sylvester JT. Capacitative calcium entry and TRPC channel proteins are expressed in rat distal pulmonary arterial smooth muscle. Am J Physiol Lung Cell Mol Physiol 286: L848-L858, 2004.
67. 2+ entry. Am J Physiol Lung Cell Mol Physiol 288: L1059-L1069, 2005.
68. 2+ signaling in hypoxic pulmonary vasoconstriction: effects of myosin light chain and Rho kinase antagonists. Am J Physiol Lung Cell Mol Physiol 293: L674-L685, 2007.
69. Wang Z, Jin N, Ganguli S, Swartz DR, Li L, Rhoades RA. Rho-kinase activation is involved in hypoxia-induced pulmonary vasoconstriction. Am J Respir Cell Mol Biol 25: 628-635, 2001.
70. Wang Z, Lanner MC, Jin N, Swartz D, Li L, Rhoades RA. Hypoxia inhibits myosin phosphatase in pulmonary arterial smooth muscle cells: role of Rho-kinase. Am J Respir Cell Mol Biol 29: 465-471, 2003.
71. 2+ and nonselective cation channels. Am J Physiol Lung Cell Mol Physiol 289: L5-L13, 2005.
72. 2+ entry during 5-HT-induced vasoconstriction of canine pulmonary arteries. Br J Pharmacol 144: 252-264, 2005.
73. Xu EZ, Kantores C, Ivanovska J, Engelberts D, Kavanagh BP, McNamara PJ, Jankov RP. Rescue treatment with a Rho-kinase inhibitor normalizes right ventricular function and reverses remodeling in juvenile rats with chronic pulmonary hypertension. Am J Physiol Heart Circ Physiol 299: H1854-H1864, 2010.
74. 2+ entry in pulmonary artery smooth muscle cells from patients with idiopathic pulmonary arterial hypertension. Am J Physiol Cell Physiol 292: C2297-C2305, 2007.
75. 2+ in cultured human pulmonary artery smooth muscle cells. Am J Physiol Cell Physiol 288: C245-C252, 2005.
76. Zhu D, Medhora M, Campbell WB, Spitzbarth N, Baker JE, Jacobs ER. Chronic hypoxia activates lung 15-lipoxygenase, which catalyzes production of 15-HETE and enhances constriction in neonatal rabbit pulmonary arteries. Circ Res 92: 992-1000, 2003