Effects of chronic hypoxia on soluble guanylate cyclase activity in fetal and adult ovine cerebral arteries

Journal of Applied Physiology

Volumn 107, Issue 1, 2009, Pages 192-199

  Pearce, William J ^a   Williams, James M ^a   White, Charles R ^a   Lincoln, Thomas M ^b  

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

^b UNIVERSITY OF SOUTH ALABAMA   (United States)

Author keywords

cGMP; Nitric oxide; Phosphodiesterase; Protein kinase G; Smooth muscle

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 (4 CHLOROPHENYLTHIO) CYCLIC GMP; CYCLIC GMP; GUANYLATE CYCLASE; NITRIC OXIDE;

ANIMAL EXPERIMENT; ARTICLE; BRAIN ARTERY; CHRONIC DISEASE; CONTROLLED STUDY; ENZYME ACTIVITY; HYPOXIA; MIDDLE CEREBRAL ARTERY; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN DEGRADATION; VASCULAR SMOOTH MUSCLE; VASODILATATION; WESTERN BLOTTING;

ALTITUDE SICKNESS; ANIMALS; ANOXIA; CEREBRAL ARTERIES; CHRONIC DISEASE; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; DISEASE MODELS, ANIMAL; ENDOTHELIUM-DEPENDENT RELAXING FACTORS; ENZYME INHIBITORS; FEMALE; FETUS; GUANYLATE CYCLASE; MUSCLE, SMOOTH, VASCULAR; NITRIC OXIDE; OXADIAZOLES; PREGNANCY; QUINOXALINES; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SHEEP; VASODILATION;

EID: 67650066337     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00233.2009     Document Type: Article

References (66)

1. Abman SH. Recent advances in the pathogenesis and treatment of persistent pulmonary hypertension of the newborn. Neonatology 91: 283-290, 2007.
2. Archer SL. Diversity of phenotype and function of vascular smooth muscle cells. J Lab Clin Med 127: 524-529, 1996.
3. Auffray C, Fogg D, Garfa M, Elain G, Join-Lambert O, Kayal S, Sarnacki S, Cumano A, Lauvau G, Geissmann F. Monitoring of blood vessels and tissues by a population of monocytes with patrolling behavior. Science 317: 666-670, 2007.
4. Belik J, Hehne N, Pan J, Behrends S. Soluble guanylate cyclase-dependent relaxation is reduced in the adult rat bronchial smooth muscle. Am J Physiol Lung Cell Mol Physiol 292: L699-L703, 2007.
5. Berkenbosch JW, Baribeau J, Perreault T. Decreased synthesis and vasodilation to nitric oxide in piglets with hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 278: L276-L283, 2000.
6. Breen E, Tang K, Olfert M, Knapp A, Wagner P. Skeletal muscle capillarity during hypoxia: VEGF and its activation. High Alt Med Biol 9: 158-166, 2008.
7. Burns RG, Islam K. Modulation of the kinetic parameters of microtubule assembly by MAP-2 phosphorylation, the GTP/GDP occupancy of oligomers, and the tubulin tyrosylation status. Ann NY Acad Sci 466: 340-356, 1986.
8. Butt E, Nolte C, Schulz S, Beltman J, Beavo JA, Jastorff B, Walter U. Analysis of the functional role of cGMP-dependent protein kinase in intact human platelets using a specific activator 8-para-chlorophenylthio-cGMP. Biochem Pharmacol 43: 2591-2600, 1992.
9. Cary SP, Winger JA, Derbyshire ER, Marletta MA. Nitric oxide signaling: no longer simply on or off. Trends Biochem Sci 31: 231-239, 2006.
10. Caudill TK, Resta TC, Kanagy NL, Walker BR. Role of endothelial carbon monoxide in attenuated vasoreactivity following chronic hypoxia. Am J Physiol Regul Integr Comp Physiol 275: R1025-R1030, 1998.
11. 2 sensing. J Biol Chem 275: 25130-25138, 2000.
12. Chicoine LG, Paffett ML, Girton MR, Metropoulus MJ, Joshi MS, Bauer JA, Nelin LD, Resta TC, Walker BR. Maturational changes in the regulation of pulmonary vascular tone by nitric oxide in neonatal rats. Am J Physiol Lung Cell Mol Physiol 293: L1261-L1270, 2007.
13. Crawley DE, Zhao L, Giembycz MA, Liu S, Barnes PJ, Winter RJ, Evans TW. Chronic hypoxia impairs soluble guanylyl cyclase-mediated pulmonary arterial relaxation in the rat. Am J Physiol Lung Cell Mol Physiol 263: L325-L332, 1992.
14. Diez-Marques ML, Ruiz-Torres MP, Griera M, Lopez-Ongil S, Saura M, Rodriguez-Puyol D, Rodriguez-Puyol M. Arg-Gly-Asp (RGD)-containing peptides increase soluble guanylate cyclase in contractile cells. Cardiovasc Res 69: 359-369, 2006.
15. Finer NN, Barrington KJ. Nitric oxide for respiratory failure in infants born at or near term. Cochrane Database Syst Rev: CD000399, 2006.
16. Frank DU, Horstman DJ, Morris GN, Johns RA, Rich GF. Regulation of the endogenous NO pathway by prolonged inhaled NO in rats. J Appl Physiol 85: 1070-1078, 1998.
17. Garbers DL. Purification of soluble guanylate cyclase from rat lung. J Biol Chem 254: 240-243, 1979.
18. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B. Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one. Mol Pharmacol 48: 184-188, 1995.
19. Gupte SA, Rupawalla T, Mohazzab-HKM, Wolin MS. Regulation of NO-elicited pulmonary artery relaxation and guanylate cyclase activation by NADH oxidase and SOD. Am J Physiol Heart Circ Physiol 276: H1535-H1542, 1999.
20. Hanasato N, Oka M, Muramatsu M, Nishino M, Adachi H, Fukuchi Y. E-4010, a selective phosphodiesterase 5 inhibitor, attenuates hypoxic pulmonary hypertension in rats. Am J Physiol Lung Cell Mol Physiol 277: L225-L232, 1999.
21. Hoehn T, Krause MF, Buhrer C. Meta-analysis of inhaled nitric oxide in premature infants: an update. Klin Padiatr 218: 57-61, 2006.
22. Hofmann F. The biology of cyclic GMP-dependent protein kinases. J Biol Chem 280: 1-4, 2005.
23. Humbert P, Niroomand F, Fischer G, Mayer B, Koesling D, Hinsch KD, Gausepohl H, Frank R, Schultz G, Bohme E. Purification of soluble guanylyl cyclase from bovine lung by a new immunoaffinity chromatographic method. Eur J Biochem 190: 273-278, 1990.
24. Hunter CJ, Blood AB, White CR, Pearce WJ, Power GG. Role of nitric oxide in hypoxic cerebral vasodilatation in the ovine fetus. J Physiol 549: 625-633, 2003.
25. Iesaki T, Gupte SA, Wolin MS. A flavoprotein mechanism appears to prevent an oxygen-dependent inhibition of cGMP-associated nitric oxideelicited relaxation of bovine coronary arteries. Circ Res 85: 1027-1031, 1999.
26. Jernigan NL, Resta TC. Chronic hypoxia attenuates cGMP-dependent pulmonary vasodilation. Am J Physiol Lung Cell Mol Physiol 282: L1366-L1375, 2002.
27. Kass DA, Takimoto E, Nagayama T, Champion HC. Phosphodiesterase regulation of nitric oxide signaling. Cardiovasc Res 75: 303-314, 2007.
28. Kontos HA. Nitric oxide and nitrosothiols in cerebrovascular and neuronal regulation. Stroke 24: I155-I158, 1993.
29. Lewicki JA, Brandwein HJ, Waldman SA, Murad F. Purified guanylate cyclase: characterization, iodination and preparation of monoclonal antibodies. J Cyclic Nucleotide Res 6: 283-296, 1980.
30. Li D, Laubach VE, Johns RA. Upregulation of lung soluble guanylate cyclase during chronic hypoxia is prevented by deletion of eNOS. Am J Physiol Lung Cell Mol Physiol 281: L369-L376, 2001.
31. Li D, Zhou N, Johns RA. Soluble guanylate cyclase gene expression and localization in rat lung after exposure to hypoxia. Am J Physiol Lung Cell Mol Physiol 277: L841-L847, 1999.
32. Longo LD, Hull AD, Long DM, Pearce WJ. Cerebrovascular adaptations to high-altitude hypoxemia in fetal and adult sheep. Am J Physiol Regul Integr Comp Physiol 264: R65-R72, 1993.
33. Loreal O, Haziza-Pigeon C, Troadec MB, Detivaud L, Turlin B, Courselaud B, Ilyin G, Brissot P. Hepcidin in iron metabolism. Curr Protein Pept Sci 6: 279-291, 2005.
34. Mbaku EM, Zhang L, Pearce WJ, Duckles SP, Buchholz J. Chronic hypoxia alters the function of NOS nerves in cerebral arteries of near-term fetal and adult sheep. J Appl Physiol 94: 724-732, 2003.
35. Mingone CJ, Gupte SA, Chow JL, Ahmad M, Abraham NG, Wolin MS. Protoporphyrin IX generation from delta-aminolevulinic acid elicits pulmonary artery relaxation and soluble guanylate cyclase activation. Am J Physiol Lung Cell Mol Physiol 291: L337-L344, 2006.
36. Mingone CJ, Gupte SA, Iesaki T, Wolin MS. Hypoxia enhances a cGMP-independent nitric oxide relaxing mechanism in pulmonary arteries. Am J Physiol Lung Cell Mol Physiol 285: L296-L304, 2003.
37. Molero L, Carrasco C, Marques M, Vaziri ND, Mateos-Caceres PJ, Casado S, Macaya C, Barrientos A, Lopez-Farre AJ. Involvement of endothelium and endothelin-1 in lead-induced smooth muscle cell dysfunction in rats. Kidney Int 69: 685-690, 2006.
38. Murata T, Yamawaki H, Hori M, Sato K, Ozaki H, Karaki H. Hypoxia impairs endothelium-dependent relaxation in organ cultured pulmonary artery. Eur J Pharmacol 421: 45-53, 2001.
39. Murray F, MacLean MR, Pyne NJ. Increased expression of the cGMP-inhibited cAMP-specific (PDE3) and cGMP binding cGMP-specific (PDE5) phosphodiesterases in models of pulmonary hypertension. Br J Pharmacol 137: 1187-1194, 2002.
40. Murthy KS. Modulation of soluble guanylate cyclase activity by phosphorylation. Neurochem Int 45: 845-851, 2004.
41. Ohlstein EH, Wood KS, Ignarro LJ. Purification and properties of heme-deficient hepatic soluble guanylate cyclase: effects of heme and other factors on enzyme activation by NO, NO-heme, and protoporphyrin IX. Arch Biochem Biophys 218: 187-198, 1982.
42. Oka M, Karoor V, Homma N, Nagaoka T, Sakao E, Golembeski SM, Limbird J, Imamura M, Gebb SA, Fagan KA, McMurtry IF. Dehydroepiandrosterone upregulates soluble guanylate cyclase and inhibits hypoxic pulmonary hypertension. Cardiovasc Res 74: 377-387, 2007.
43. Papapetropoulos A, Cziraki A, Rubin JW, Stone CD, Catravas JD. cGMP accumulation and gene expression of soluble guanylate cyclase in human vascular tissue. J Cell Physiol 167: 213-221, 1996.
44. Papapetropoulos A, Marczin N, Mora G, Milici A, Murad F, Catravas JD. Regulation of vascular smooth muscle soluble guanylate cyclase activity, mRNA, and protein levels by cAMP-elevating agents. Hypertension 26: 696-704, 1995.
45. Pearce WJ, Hull AD, Long DM, Longo LD. Developmental changes in ovine cerebral artery composition and reactivity. Am J Physiol Regul Integr Comp Physiol 261: R458-R465, 1991.
46. Pearce WJ, Williams JM, Hamade MW, Chang MM, White CR. Chronic hypoxia modulates endothelium-dependent vasorelaxation through multiple independent mechanisms in ovine cranial arteries. Adv Exp Med Biol 578: 87-92, 2006.
47. Powel V, Moreira GA, O'Donnell DC, Filippov G, Bloch KD, Gordon JB. Maturational changes in ovine pulmonary vascular responses to inhaled nitric oxide. Pediatr Pulmonol 27: 157-166, 1999.
48. Priest RM, Robertson TP, Leach RM, Ward JP. Membrane potentialdependent and -independent vasodilation in small pulmonary arteries from chronically hypoxic rats. J Pharmacol Exp Ther 285: 975-982, 1998.
49. Russwurm M, Koesling D. Isoforms of NO-sensitive guanylyl cyclase. Mol Cell Biochem 230: 159-164, 2002 Jan.
50. Sebkhi A, Strange JW, Phillips SC, Wharton J, Wilkins MR. Phosphodiesterase type 5 as a target for the treatment of hypoxia-induced pulmonary hypertension. Circulation 107: 3230-3235, 2003.
51. Sekar K. Inhaled nitric oxide in term and preterm infants. J Perinatol 26 Suppl 1: S4-S7; discussion S22-S23, 2006.
52. Semenza GL, Shimoda LA, Prabhakar NR. Regulation of gene expression by HIF-1. Novartis Found Symp 272: 2-8; discussion 8-14, 33-16, 2006.
53. Shah PS, Ohlsson A. Sildenafil for pulmonary hypertension in neonates. Cochrane Database Syst Rev: CD005494, 2007.
54. Stenmark KR, Fagan KA, Frid MG. Hypoxia-induced pulmonary vascular remodeling: cellular and molecular mechanisms. Circ Res 99: 675-691, 2006.
55. Takata M, Filippov G, Liu H, Ichinose F, Janssens S, Bloch DB, Bloch KD. Cytokines decrease sGC in pulmonary artery smooth muscle cells via NO-dependent and NO-independent mechanisms. Am J Physiol Lung Cell Mol Physiol 280: L272-L278, 2001.
56. Tomita T, Tsuyama S, Imai Y, Kitagawa T. Purification of bovine soluble guanylate cyclase and ADP-ribosylation on its small subunit by bacterial toxins. J Biochem (Tokyo) 122: 531-536, 1997.
57. Tulloh RM, Hislop AA, Haworth SG. Role of NO in recovery from neonatal hypoxic pulmonary hypertension. Thorax 54: 796-804, 1999.
58. Venema RC, Venema VJ, Ju H, Harris MB, Snead C, Jilling T, Dimitropoulou C, Maragoudakis ME, Catravas JD. Novel complexes of guanylate cyclase with heat shock protein 90 and nitric oxide synthase. Am J Physiol Heart Circ Physiol 285: H669-H678, 2003.
59. Wang T, El Kebir D, Blaise G. Inhaled nitric oxide in 2003: a review of its mechanisms of action. Can J Anaesth 50: 839-846, 2003.
60. White CR, Hao X, Pearce WJ. Maturational differences in soluble guanylate cyclase activity in ovine carotid and cerebral arteries. Pediatr Res 47: 369-375, 2000.
61. White CR, Pearce WJ. Effects of maturation on cyclic GMP metabolism in ovine carotid arteries. Pediatr Res 39: 25-31, 1996.
62. Williams JM, Hull AD, Pearce WJ. Maturational modulation of endothelium-dependent vasodilatation in ovine cerebral arteries. Am J Physiol Regul Integr Comp Physiol 288: R149-R157, 2005.
63. Williams JM, Pearce WJ. Age-dependent modulation of endotheliumdependent vasodilatation by chronic hypoxia in ovine cranial arteries. J Appl Physiol 100: 225-232, 2006.
64. Williams JM, White CR, Chang MM, Injeti ER, Zhang L, Pearce WJ. Chronic hypoxic decreases in soluble guanylate cyclase protein and enzyme activity are age dependent in fetal and adult ovine carotid arteries. J Appl Physiol 100: 1857-1866, 2006.
65. Yetik-Anacak G, Xia T, Dimitropoulou C, Venema RC, Catravas JD. Effects of hsp90 binding inhibitors on sGC-mediated vascular relaxation. Am J Physiol Heart Circ Physiol 291: H260-H268, 2006.
66. Zwiller J, Basset P, Mandel P. Rat brain guanylate cyclase. Purification, amphiphilic properties and immunological characterization. Biochim Biophys Acta 658: 64-75, 1981.