Oxidant stress from uncoupled nitric oxide synthase impairs vasodilation in fetal lambs with persistent pulmonary hypertension

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 292, Issue 4, 2007, Pages

  Konduri, Girija G ^a,b   Bakhutashvili, Ivane ^a,b   Eis, Annie ^a   Pritchard Jr , Kirkwood ^a  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b CLEMENT J ZABLOCKI VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

ATP; Heat shock protein 90; Nitrotyrosine; Superoxide; Superoxide dismutase

Indexed keywords

ADENOSINE TRIPHOSPHATE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEAT SHOCK PROTEIN; N ACETYL S NITROSOPENICILLAMINE; N(G) NITROARGININE METHYL ESTER; TIRON;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; FETUS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PULMONARY HYPERTENSION; VASODILATATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; DISEASE MODELS, ANIMAL; ENZYME INHIBITORS; FEMALE; FETUS; HSP90 HEAT-SHOCK PROTEINS; HUMANS; INFANT, NEWBORN; LIGATION; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PERSISTENT FETAL CIRCULATION SYNDROME; PREGNANCY; PULMONARY ARTERY; S-NITROSO-N-ACETYLPENICILLAMINE; SHEEP; SUPEROXIDES; TYROSINE; VASODILATION;

EID: 34147118950     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00425.2006     Document Type: Article

References (37)

1. Abman SH, Chatfield BA, Hall SL, McMurtry IF. Role of endothelium-derived relaxing factor during transition of pulmonary circulation at birth. Am J Physiol Heart Circ Physiol 259: H1921-H1927, 1990.
2. Abman SH, Shanley PF, Accurso FJ. Failure of postnatal adaptation of the pulmonary circulation after chronic intrauterine pulmonary hypertension in fetal lambs. J Clin Invest 83: 1849-1858, 1989.
3. Alano MA, Ngougmna E, Ostrea EM, Konduri GG. Analysis of nonsteroidal antiinflammatory drugs in meconium and its relation to persistent pulmonary hypertension of the newborn. Pediatrics 107: 519-523, 2001.
4. Black SM, Johengen MJ, Soifer SJ. Coordinated regulation of genes of the nitric oxide and endothelin pathways during the development of pulmonary hypertension in fetal lambs. Pediatr Res 44: 821-830, 1998.
5. Brennan LA, Steinhorn RH, Wedgwood S, Mata-Greenwood E, Roark EA, Russell JA, Black SM. Increased superoxide generation is associated with pulmonary hypertension in fetal lambs: a role for NADPH oxidase. Circ Res 92: 683-691, 2003.
6. Cassin S, Dawes GS, Mott JC, Ross BB, Strang LB. The vascular resistance of the foetal and newly ventilated lung of the lamb. J Physiol 171: 61-79, 1964.
7. Dawes GS, Mott JC, Widdicombe JG, Wyatt DG. Changes in the lungs of the newborn lamb. J Physiol 121: 141-162, 1953.
8. Garcia-Cardena G, Fan R, Shah V, Sorrentino R, Cirino G, Papapetropoulos A, Sessa WC. Dynamic activation of endothelial nitric oxide synthase by Hsp90. Nature 392: 821-824, 1998.
9. Hammer LW, Ligan AL, Hester RL. ATP-mediated release of arachidonic acid metabolites from venular endothelium causes arteriolar dilation. Am J Physiol Heart Circ Physiol 280: H2616-H2622, 2001.
10. Kabakov AE, Gabai VL. Heat-shock proteins maintain the viability of ATP-deprived cells: what is the mechanism? Trends Cell Biol 4: 193-196, 1994.
11. Khoo JP, Zhao L, Alp NJ, Bendall JK, Nicoli T, Rockett K, Wilkins MR, Channon KM. Pivotal role for endothelial tetrahydrobiopterin in pulmonary hypertension. Circulation 111: 2126-2133, 2005.
12. Konduri GG, Bakhutashvili I, Frenn R, Chandrasekhar I, Jacobs ER, Khanna A. P2Y purine receptor responses and expression in the pulmonary circulation of juvenile rabbits. Am J Physiol Heart Circ Physiol 287: H157-H164, 2004.
13. Konduri GG, Gervasio CT, Theodorou AA. Role of adenosine triphosphate and adenosine in oxygen induced pulmonary vasodilation in fetal lambs. Pediatr Res 33: 533-539, 1993.
14. Konduri GG, Mattei J. Role of oxidative phosphorylation and ATP release in birth-related pulmonary vasodilation in fetal lambs. Am J Physiol Heart Circ Physiol 283: H1600-H1608, 2002.
15. Konduri GG, Mital S, Gervasio CT, Rotta AT, Forman K. Purine nucleotides contribute to pulmonary vasodilation caused by birth-related stimuli in the ovine fetus. Am J Physiol Heart Circ Physiol 272: H2377-H2384, 1997.
16. Konduri GG, Ou J, Shi Y, Pritchard KA Jr. Decreased association of HSP90 impairs endothelial nitric oxide synthase in fetal lambs with persistent pulmonary hypertension. Am J Physiol Heart Circ Physiol 285: H204-H211, 2003.
17. Melichar VO, Behr-Roussel D, Zabel U, Uttenthal LO, Rodrigo J, Rupin A, Verbeuren TJ, Kumar HSA, Schmidt HH. Reduced cGMP signaling associated with neointimal proliferation and vascular dysfunction in late-stage atherosclerosis. Proc Natl Acad Sci USA 101: 16671-16676, 2004.
18. Morin FC. Ligating the ductus arteriosus before birth causes persistent pulmonary hypertension in newborn lamb. Pediatr Res 25: 245-250, 1989.
19. Murata T, Sato K, Hori M, Ozaki H, Karaki H. Decreased endothelial nitric-oxide synthase (eNOS) activity resulting from abnormal interaction between eNOS and its regulatory proteins in hypoxia-induced pulmonary hypertension. J Biol Chem 277: 44085-44092, 2002.
20. Nandi M, Miller A, Stidwill R, Jacques TS, Lam AA, Haworth S, Heales S, Vallance P. Pulmonary hypertension in a GTP-cyclohydrolase 1-deficient mouse. Circulation 111: 2086-2090, 2005.
21. . bioactivity. Am J Physiol Heart Circ Physiol 286: H561-H569, 2004.
22. Ou J, Ou Z, Ackerman AW, Oldham KT, Pritchard KA Jr. Inhibition of heat shock protein 90 (hsp90) in proliferating endothelial cells uncouples endothelial nitric oxide synthase activity. Free Radic Biol Med 34: 269-276, 2003.
23. Pritchard KA, Ackerman AW, Gross ER, Stepp DW, Shi Y, Fontana JT, Baker JE, Sessa WC. Heat shock protein 90 mediates the balance of nitric oxide and superoxide anion from endothelial nitric oxide synthase. J Biol Chem 276: 17621-17624, 2001.
24. Reiter CD, Teng RJ, Beckman JS. Superoxide reacts with nitric oxide to nitrate tyrosine at physiological pH via peroxynitrite. J Biol Chem 275: 32460-32466, 2000.
25. + channels in vasodilator response to ATP in isolated pulmonary arteries from juvenile rabbits (Abstract). Pediatr Res 51: 397A, 2002.
26. Shaul PW, Farrar MA, Magness RR. Pulmonary endothelial nitric oxide production is developmentally regulated in the fetus and newborn. Am J Physiol Heart Circ Physiol 265: H1056-H1063, 1993.
27. Shaul PW, Yuhanna IS, German Z, Chen Z, Steinhorn RH, Morin FC. Pulmonary endothelial NO synthase gene expression is decreased in fetal lambs with pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 272: L1005-L1012, 1997.
28. Steinhorn RH, Albert G, Swartz DD, Russell JA, Levine CR, Davis JM. Recombinant human superoxide dismutase enhances the effect of inhaled nitric oxide in persistent pulmonary hypertension. Am J Respir Crit Care Med 164: 834-839, 2001.
29. Tiktinsky MH, Morin FC 3rd. Increasing oxygen tension dilates fetal pulmonary circulation via endothelium-derived relaxing factor. Am J Physiol Heart Circ Physiol 265: H376-H380, 1993.
30. Tzao C, Nickerson PA, Russell JA, Gugino SF, Steinhorn RH. Pulmonary hypertension alters soluble guanylate cyclase activity and expression in pulmonary arteries isolated from fetal lambs. Pediatr Pulmonol 31: 97-105, 2001.
31. Venema V, Marrero M, Venema R. Bradykinin-stimulated protein tyrosine phosphorylation promotes endothelial nitric oxide synthase translocation to the cytoskeleton. Biochem Biophys Res Commun 155: 801-807, 1996.
32. Villamor E, Le Cras TD, Horan MP, Halbower AC, Tuder RM, Abman SH. Chronic intrauterine pulmonary hypertension impairs endothelial nitric oxide synthase in the ovine fetus. Am J Physiol Lung Cell Mol Physiol 272: L1013-L1020, 1997.
33. Villanueva ME, Zaher FM, Svinarich DM, Konduri GG. Decreased gene expression of endothelial nitric oxide synthase in newborns with persistent pulmonary hypertension. Pediatr Res 44: 338-343, 1998.
34. Wallerath T, Kunt T, Forst T, Closs EI, Lehmann R, Flohr T, Gabriel M, Schafer D, Gopfert A, Pfutzner A, Beyer J, Forstermann U. Stimulation of endothelial nitric oxide synthase by proinsulin C-peptide. Nitric Oxide 9: 95-102, 2003.
35. Walsh-Sukys MC, Tyson JE, Wright L, Bauer C, Korones SB, Stevenson DK, Verter J, Stoll BJ, Lemons JA, Papile L-A, 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.
36. Wedgwood S, Steinhorn RH, Bunderson M, Wilham J, Lakshminrusimha S, Brennan LA, Black SM. Increased hydrogen peroxide downregulates soluble guanylate cyclase in the lungs of lambs with persistent pulmonary hypertension of the newborn. Am J Physiol Lung Cell Mol Physiol 289: L660-L666, 2005.
37. Winer BJ. Statistical Principles in Experimental Design. New York: McGraw-Hill, 1977, p. 514-603.