Optimization of isolated perfused/ventilated mouse lung to study hypoxic pulmonary vasoconstriction

Pulmonary Circulation

Volumn 3, Issue 2, 2013, Pages 396-405

  Yoo, Hae Young ^a   Zeifman, Amy ^a   Ko, Eun A ^a   Smith, Kimberly A ^a   Chen, Jiwang ^a   Machado, Roberto F ^a   Zhao, You Yang ^a   Minshall, Richard D ^a   Yuan, Jason X J ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Endothelial nitric oxide synthase; Hypoxia; Mouse lung; Pulmonary artery; Pulmonary vasoconstriction

Indexed keywords

EID: 85009831032     PISSN: 20458932     EISSN: 20458940     Source Type: Journal    
DOI: 10.4103/2045-8932.114776     Document Type: Article

References (84)

1. von Euler US, Liljestrand G. Observations on the pulmonary arterial blood pressure in the cat. Acta Physiol Scand 1946;12:301-20.
2. Sylvester JT, Shimoda LA, Aaronson PI, Ward JP. Hypoxic pulmonary vasoconstriction. Physiol Rev 2012;92:367-520.
3. Yuan JX, editor. Hypoxic Pulmonary Vasoconstriction: Cellular and Molecular Mechanisms. Boston: Kluwer Academic Publishers; 2004.
4. Archer SL, Wu XC, Thébaud B, Nsair A, Bonnet S, Tyrrell B, et al. Preferential expression and function of voltage-gated, O2-sensitive K+ channels in resistance pulmonary arteries explains regional heterogeneity in hypoxic pulmonary vasoconstriction: Ionic diversity in smooth muscle cells. Circ Res 2004;95:308-18.
5. Osipenko ON, Tate RJ, Gurney AM. Potential role for Kv3.1b channels as oxygen sensors. Circ Res 2000;86:534-40.
6. Sham JS, Crenshaw BR Jr., Deng LH, Shimoda LA, Sylvester JT. Effects of hypoxia in porcine pulmonary arterial myocytes: Roles of KV channel and endothelin-1. Am J Physiol Lung Cell Mol Physiol 2000;279:L262-72.
7. Brayden JE, Nelson MT. Regulation of arterial tone by activation of calciumdependent potassium channels. Science 1992;256:532-5.
8. Hirenallur S D, Detweiler N D, Haworth S T, Leming J T, Gordon JB, Rusch NJ. Furegrelate, a thromboxane synthase inhibitor, blunts the development of pulmonary arterial hypertension in neonatal piglets. Pulm Circ 2012;2:193-200.
9. Howard LS, Crosby A, Vaughan P, Sobolewski A, Southwood M, Foster ML, et al. Distinct responses to hypoxia in subpopulations of distal pulmonary artery cells contribute to pulmonary vascular remodeling in emphysema. Pulm Circ 2012;2:241-9.
10. 2-sensor in resistance artery smooth muscle cells. J Mol Cell Cardiol 2004;37:1119-36.
11. Moudgil R, Michelakis ED, Archer SL. Hypoxic pulmonary vasoconstriction. J Appl Physiol 2005;98:390-403.
12. 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 2012;2:41-53.
13. Pham I, Wuerzner G, Richalet JP, Peyrard S, Azizi M. Bosentan effects in hypoxic pulmonary vasoconstriction: Preliminary study in subjects with or without high altitude pulmonary edema-history. Pulm Circ 2012;2:28-33.
14. Pozeg ZI, Michelakis ED, McMurtry MS, Thébaud B, Wu XC, Dyck JR, et al. In vivo gene transfer of the O2-sensitive potassium channel Kv1.5 reduces pulmonary hypertension and restores hypoxic pulmonary vasoconstriction in chronically hypoxic rats. Circulation 2003;107:2037-44.
15. Rodman DM, Yamaguchi T, O’Brien RF, McMurtry IF. Hypoxic contraction of isolated rat pulmonary artery. J Pharmacol Exp Ther 1989;248:952-9.
16. 2+signaling in hypoxic pulmonary vasoconstriction: Effects of myosin light chain and Rho kinase antagonists. Am J Physiol Lung Cell Mol Physiol 2007;293:L674-85.
17. +channels and pulmonary vasoconstriction: Role of protein kinase Czeta. Circ Res 2003;93:656-63.
18. Leach RM, Robertson TP, Twort CH, Ward JP. Hypoxic vasoconstriction in rat pulmonary and mesenteric arteries. Am J Physiol 1994;266:L223-31.
19. Murtha YM, Allen BM, Orr JA. The role of protein kinase C in thromboxane A2-induced pulmonary artery vasoconstriction. J Biomed Sci 1999;6:293-5.
20. Weissmann N, Dietrich A, Fuchs B, Kalwa H, Ay M, Dumitrascu R, et al. Classical transient receptor potential channel 6 (TRPC6) is essential for hypoxic pulmonary vasoconstriction and alveolar gas exchange. Proc Natl Acad Sci U S A 2006;103:19093-8.
21. Park SJ, Yoo HY, Earm YE, Kim SJ, Kim JK, Kim SD. Role of arachidonic acid-derived metabolites in the control of pulmonary arterial pressure and hypoxic pulmonary vasoconstriction in rats. Br J Anaesth 2011;106:31-7.
22. McMurtry IF, Davidson AB, Reeves JT, Grover RF. Inhibition of hypoxic pulmonary vasoconstriction by calcium antagonists in isolated rat lungs. Circ Res 1976;38:99-104.
23. McMurtry IF, Hookway BW, Roos S. Red blood cells play a crucial role in maintaining vascular reactivity to hypoxia in isolated rat lungs. Chest 1977;71:253-6.
24. McMurtry IF, Petrun MD, Reeves JT. Lungs from chronically hypoxic rats have decreased pressor response to acute hypoxia. Am J Physiol 1978;235:H104-9.
25. McMurtry IF, Rounds S, Stanbrook HS. Studies of the mechanism of hypoxic pulmonary vasoconstriction. Adv Shock Res 1982;8:21-33.
26. Weissmann N, Akkayagil E, Quanz K, Schermuly RT, Ghofrani HA, Fink L, et al. Basic features of hypoxic pulmonary vasoconstriction in mice. Respir Physiol Neurobiol 2004;139:191-202.
27. Rhoades RA. Isolated perfused lung preparation for studying altered gaseous environments. Environ Health Perspect 1984;56:43-50.
28. +channels, Kv1.5 and Kv2.1, in hypoxic pulmonary vasoconstriction and control of resting membrane potential in rat pulmonary artery myocytes. J Clin Invest 1998;101:2319-30.
29. 2+-dependent action potentials in small pulmonary arteries of the cat. J Appl Physiol 1985;59:1389-93.
30. Weir EK, Archer SL. The mechanism of acute hypoxic pulmonary vasoconstriction: The tale of two channels. FASEB J 1995;9:183-9.
31. 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 1993;264:L116-23.
32. Fagan KA, Oka M, Bauer NR, Gebb SA, Ivy DD, Morris KG, et al. Attenuation of acute hypoxic pulmonary vasoconstriction and hypoxic pulmonary hypertension in mice by inhibition of Rho-kinase. Am J Physiol Lung Cell Mol Physiol 2004;287:L656-64.
33. Zhao L, Mason NA, Morrell NW, Kojonazarov B, Sadykov A, Maripov A, et al. Sildenafil inhibits hypoxia-induced pulmonary hypertension. Circulation 2001;104:424-8.
34. Fagan KA, Fouty BW, Tyler RC, Morris KG Jr, Hepler LK, Sato K, et al. The pulmonary circulation of homozygous or heterozygous eNOS-null mice is hyperresponsive to mild hypoxia. J Clin Invest 1999;103:291-9.
35. Vanderpool RR, Naeije R, Chesler NC. Impedance in isolated mouse lungs for the determination of site of action of vasoactive agents and disease. Ann Biomed Eng 2010;38:1854-61.
36. Tuchscherer HA, Vanderpool RR, Chesler NC. Pulmonary vascular remodeling in isolated mouse lungs: effects on pulsatile pressure-flow relationships. J Biomech 2007;40:993-1001.
37. Spohr F, Busch CJ, Teschendorf P, Weimann J. Selective inhibition of guanylate cyclase prevents impairment of hypoxic pulmonary vasoconstriction in endotoxemic mice. J Physiol Pharmacol 2009;60:107-12.
38. Nelin LD, Dawson CA. The effect of N omega-nitro-L-arginine methylester on hypoxic vasoconstriction in the neonatal pig lung. Pediatr Res 1993;34:349-53.
39. Schnader J, Undem B, Peters S P, Sylvester J T. Effect so f nordihydroguaiuretic acid on sulfidopeptide leukotriene activity and hypoxic pulmonary vasoconstriction in the isolated sheep lung. Prostaglandins 1993;46:5-19.
40. Gordon JB, Hortop J, Hakim TS. Developmental effects of hypoxia and indomethacin on distribution of vascular resistances in lamb lungs. Pediatr Res 1989;26:325-9.
41. Drop LJ, Toal KW, Geffin GA, DD OK, Hoaglin DC, Daggett WM. Pulmonary vascular responses to hypercalcemia and hypocalcemia in the dog. Anesthesiology 1989;70:825-36.
42. Baek EB, Yoo HY, Park SJ, Kim HS, Kim SD, Earm YE, et al. Luminal ATPinduced contraction of rabbit pulmonary arteries and role of purinoceptors in the regulation of pulmonary arterial pressure. Pflugers Arch 2008;457:281-91.
43. Fuchs B, Rupp M, Ghofrani HA, Schermuly RT, Seeger W, Grimminger F, et al. Diacylglycerol regulates acute hypoxic pulmonary vasoconstriction via TRPC6. Respir Res 2011;12:20.
44. Yoo HY, Park SJ, Bahk JH, Kim SJ. Inhibition of hypoxic pulmonary vasoconstriction of rats by carbon monoxide. J Korean Med Sci 2010;25:1411-7.
45. Keserü B, Barbosa-Sicard E, Popp R, Fisslthaler B, Dietrich A, Gudermann T, et al. Epoxyeicosatrienoic acids and the soluble epoxide hydrolase are determinants of pulmonary artery pressure and the acute hypoxic pulmonary vasoconstrictor response. FASEB J 2008;22:4306-15.
46. Francis BN, Wilkins MR, Zhao L. Tetrahydrobiopterin and the regulation of hypoxic pulmonary vasoconstriction. Eur Respir J 2010;36:323-30.
47. +channels: Lung vascular effects of hypoxia. Am J Respir Crit Care Med 2009;180:353-64.
48. Spöhr F, Busch CJ, Reich C, Motsch J, Gebhard MM, Kuebler WM, et al. 4-Aminopyridine restores impaired hypoxic pulmonary vasoconstriction in endotoxemic mice. Anesthesiology 2007;107:597-604.
49. Bernal PJ, Leelavanichkul K, Bauer E, Cao R, Wilson A, Wasserloos KJ, et al. Nitric-oxide-mediated zinc release contributes to hypoxic regulation of pulmonary vascular tone. Circ Res 2008;102:1575-83.
50. Keserü B, Barbosa-Sicard E, Schermuly RT, Tanaka H, Hammock BD, Weissmann N, et al. Hypoxia-induced pulmonary hypertension: Comparison of soluble epoxide hydrolase deletion vs. inhibition. Cardiovasc Res 2010;85:232-40.
51. Parker JC, Gillespie MN, Taylor AE, Martin SL. Capillary filtration coefficient, vascular resistance, and compliance in isolated mouse lungs. J Appl Physiol 1999;87:1421-7.
52. von Bethmann AN, Brasch F, Nüsing R, Vogt K, Volk HD, Müller KM, et al. Hyperventilation induces release of cytokines from perfused mouse lung. Am J Respir Crit Care Med 1998;157:263-72.
53. Littler CM, Morris KG Jr., Fagan KA, McMurtry IF, Messing RO, Dempsey EC. Protein kinase C-epsilon-null mice have decreased hypoxic pulmonary vasoconstriction. Am J Physiol Heart Circ Physiol 2003;284:H1321-31.
54. Mauban JR, Remillard CV, Yuan JX. Hypoxic pulmonary vasoconstriction: Role of ion channels. J Appl Physiol 2005;98:415-20.
55. Ward JP, Aaronson PI. Mechanisms of hypoxic pulmonary vasoconstriction: Can anyone be right? Respir Physiol 1999;115:261-71.
56. Bauer PM, Yu J, Chen Y, Hickey R, Bernatchez PN, Looft-Wilson R, et al. Endothelial-specific expression of caveolin-1 impairs microvascular permeability and angiogenesis. Proc Natl Acad Sci U S A 2005; 102:204-9.
57. Ju H, Zou R, Venema VJ, Venema RC. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 1997;272:18522-5.
58. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001;293:2449-52.
59. Zhao YY, Liu Y, Stan RV, Fan L, Gu Y, Dalton N, et al. Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc Natl Acad Sci U S A 2002;99:11375-80.
60. Wunderlich C, Schmeisser A, Heerwagen C, Ebner B, Schober K, Braun-Dullaeus RC, et al. Chronic NOS inhibition prevents adverse lung remodeling and pulmonary arterial hypertension in caveolin-1 knockout mice. Pulm Pharmacol Ther 2008;21:507-15.
61. Zhao YY, Zhao YD, Mirza MK, Huang JH, Potula HH, Vogel SM, et al. Persistent eNOS activation secondary to caveolin-1 deficiency induces pulmonary hypertension in mice and humans through PKG nitration. J Clin Invest 2009;119:2009-18.
62. Suzuki K, Naoki K, Kudo H, Nishio K, Sato N Aoki T, et al. Impaired hypoxic vasoconstriction in intraacinar microvasculature in hyperoxia-exposed rat lungs. Am J Respir Crit Care Med 1998;158:602-9.
63. Fagan KA, Tyler RC, Sato K, Fouty BW, Morris KG Jr, Huang PL, et al. Relative contributions of endothelial, inducible, and neuronal NOS to tone in the murine pulmonary circulation. Am J Physiol 1999;277:L472-8.
64. Nelson RS, Eichinger MR. Role of nitric oxide (NO) in pulmonary dysfunction associated with experimental cirrhosis. Respir Physiol 2001;126:65-74.
65. Vaughan D J, Brogan T V, Kerr M E, Deem S, Luchtel D L, Swenson ER. Contributions of nitric oxide synthase isozymes to exhaled nitric oxide and hypoxic pulmonary vasoconstriction in rabbit lungs. Am J Physiol Lung Cell Mol Physiol 2003;284:L834-43.
66. Nakamura T, Vollmar B, Menger MD, Inui K, Wada H, Schafers HJ. Heme oxygenase does not contribute to control of basal vascular tone in isolated blood-perfused rat lung. J Heart Lung Transplant 2004;23:599-605.
67. Yoo HY, Park SJ, Seo EY, Park KS, Han JA, Kim KS, et al. Role of thromboxane A2-activated nonselective cation channels in hypoxic pulmonary vasoconstriction of rat. Am J Physiol Cell Physiol 2012;302:C307-17.
68. Deem S, Min JH, Moulding JD, Eveland R, Swenson ER. Red blood cells prevent inhibition of hypoxic pulmonary vasoconstriction by nitrite in isolated, perfused rat lungs. Am J Physiol Heart Circ Physiol 2007;292:H963-70.
69. Deem S, Swenson ER, Alberts MK, Hedges RG, Bishop MJ. Red-bloodcell augmentation of hypoxic pulmonary vasoconstriction: Hematocrit dependence and the importance of nitric oxide. Am J Respir Crit Care Med 1998;157:1181-6.
70. Weissmann N, Winterhalder S, Nollen M, Voswinckel R, Quanz K, Ghofrani HA, et al. NO and reactive oxygen species are involved in biphasic hypoxic vasoconstriction of isolated rabbit lungs. Am J Physiol Lung Cell Mol Physiol 2001;280:L638-45.
71. Busch CJ, Spohr FA, Motsch J, Gebhard MM, Martin EO, Weimann J. Effects of ketamine on hypoxic pulmonary vasoconstriction in the isolated perfused lungs of endotoxaemic mice. Eur J Anaesthesiol 2010;27:61-6.
72. Gomez-Arroyo J, Saleem SJ, Mizuno S, Syed AA, Bogaard HJ, Abbate A, et al. A brief overview of mouse models of pulmonary arterial hypertension: Problems and prospects. Am J Physiol Lung Cell Mol Physiol 2012;302:L977-91.
73. Dumas JP, Goirand F, Bardou M, Dumas M, Rochette L, Advenier C, et al. Role of potassium channels and nitric oxide in the relaxant effects elicited by beta-adrenoceptor agonists on hypoxic vasoconstriction in the isolated perfused lung of the rat. Br J Pharmacol 1999;127:421-8.
74. Robertson TP, Ward JP, Aaronson PI. Hypoxia induces the release of a pulmonary-selective, Ca2+-sensitising, vasoconstrictor from the perfused rat lung. Cardiovasc Res 2001;50:145-50.
75. Grover RF, Vogel JH, Averill KH, Blount SG Jr. Pulmonary hypertension. individual and species variability relative to vascular reactivity. Am Heart J 1963;66:1-3.
76. Nelson MT, Quayle JM. Physiological roles and properties of potassium channels in arterial smooth muscle. Am J Physiol 1995;268:C799-822.
77. 2+]i in pulmonary arterial myocytes. Circ Res 1995;77:370-8.
78. Olschewski A, Li Y, Tang B, Hanze J, Eul B, Bohle RM, et al. Impact of TASK 1 in human pulmonary artery smooth muscle cells. Circ Res 2006;98:1072-80.
79. Gurney AM, Osipenko ON, MacMillan D, McFarlane KM, Tate RJ, Kempsill FE. Two-pore domain K channel, TASK-1, in pulmonary artery smooth muscle cells. Circ Res 2003;93:957-64.
80. Gurney AM, Joshi S. The role of twin pore domain and other K+ channels in hypoxic pulmonary vasoconstriction. Novartis Found Symp 2006;272:218-28.
81. Joshi S, Balan P, Gurney AM. Pulmonary vasoconstrictor action of KCNQ potassium channel blockers. Respir Res 2006;7:31.
82. Nelson MT, Patlak JB, Worley JF, Standen NB. Calcium channels, potassium channels, and voltage dependence of arterial smooth muscle tone. Am J Physiol 1990;259:C3-18.
83. 2+influx and contraction in rat pulmonary artery. Circ Res 2001;89:923-9.
84. Lobysheva I, Rath G, Sekkali B, Bouzin C, Feron O, Gallez B, et al. Moderate caveolin-1 downregulation prevents NADPH oxidase-dependent endothelial nitric oxide synthase uncoupling by angiotensin II in endothelial cells. Arterioscler Thromb Vasc Biol 2011;31:2098-105