Dedifferentiated human ventricular cardiac myocytes express inducible nitric oxide synthase mRNA but not protein in response to IL-1, TNF, IFN(γ), and LPS

Journal of Molecular and Cellular Cardiology

Volumn 29, Issue 4, 1997, Pages 1153-1165

  Luss, Hartmut ^a   Li, Ren Ke ^b,c   Shapiro, Richard A ^a   Tzeng, Edith ^a   McGowan, Francis X ^a   Yoneyama, Toshie ^a   Hatakeyama, Kazuyuki ^a   Geller, David A ^a   Mickle, Donald A G ^c   Simmons, Richard L ^a   Billiar, Timothy R ^a,d  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d PRESBYTERIAN UNIVERSITY HOSPITAL   (United States)

Author keywords

Cardiac myocytes; Messenger RNA; Molecular cloning; Nitric oxide; Translation

Indexed keywords

BIOPTERIN; COMPLEMENTARY DNA; GAMMA INTERFERON; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MESSENGER RNA; NITRIC OXIDE SYNTHASE; TETRAHYDROBIOPTERIN; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL LYSATE; HEART CELL CULTURE; HEART MUSCLE CELL; HEART VENTRICLE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; NORTHERN BLOTTING; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

BACTERIA (MICROORGANISMS);

EID: 0031127966     PISSN: 00222828     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmcc.1996.0349     Document Type: Article

References (56)

1. ADACHI H, IIDA S, OGUCHI S, OHSHIMA H, SUZUKI H, NAGASAKI K, KAWASAKI H, SUGIMURA T, ESUMI H, 1993. Molecular cloning of a cDNA encoding an inducible calmodulin-dependent nitric oxide synthase from rat liver and its expression in COS 1 cells. Eur J Biochem 217: 37-43.
2. BALLIGAND JL, UNGUREANU D, KELLY RA, KOBZIK L, PIMENTAL D, MICHEL T, SMITH TW, 1993. Abnormal contractile function due to induction of nitric oxide synthesis in rat cardiac myocytes follows exposure to activated macrophage-conditioned medium. J Clin Invest 91: 2314-2319.
3. BALLIGAND JL, UNGUREANU-LONGROIS D, SIMMONS WW, PIMENTAL D, MALINSKI TA, KAPTURCZAK M, TAHA Z, LOWENSTEIN CJ, DAVIDOFF AJ, KELLY RA, SMITH TW, MICHEL T, 1994. Cytokine-inducible nitric oxide synthase (iNOS) expression in cardiac myocytes. J Biol Chem 269: 27580-27588.
4. BRADY AJB, POOLE-WILSON PA, HARDING SE, WARREN JB, 1992. Nitric oxide production within cardiac myocytes reduces their contractility in endotoxemia. Am J Physiol 263: H1963-H1966.
5. BREDT DS, HWANG PM, GLATT CE, LOWENSTEIN CJ, REED RR, SNYDER SH, 1991. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature (Lond.) 351: 714-718.
6. CHARLES IG, PALMER RM, HICKERY MS, BAYLISS MT, CHUBB AP, HALL VS, MOSS DW, MONCADA S, 1993. Cloning, characterization, and expression of a cDNA encoding an inducible nitric oxide synthase from the human chondrocyte. Proc Natl Acad Sci USA 90: 11419-11423.
7. CHARTRAIN NA, GELLER DA, KOTY PP, SITRIN NF, NUSSLER AK, HOFFMAN EP, BILLIAR TR, HUTCHINSON NI, MUDGETT JS, 1994. Molecular cloning, structure, and chromosomal localization of the human inducible nitric oxide synthase gene. J Biol Chem 269: 6765-6772.
8. CHENAIS B, YAPO A, LEPOIVRE M, TENU JP, 1991. High-performance liquid chromatographic analysis of the unusual pathway of oxidation of L-arginine to citrulline and nitric oxide in mammalian cells. J Chromatogr 539: 433-441.
9. CHOMCZYNSKI P, SACCHI N, 1987. Single step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159.
10. DE BELDER AJ, RADOMSKI MW, WHY HJF, RICHARDSON PJ, BUCKNALL CA, SALAS E, MARTIN JF, MONCADA S, 1993. Nitric oxide synthase activities in human myocardium. Lancet 341: 84-85.
11. FUKUSHIMA T, NIXON JC, 1980. Analysis of reduced forms of biopterin in biological tissues and fluids. Anal Biochem 102: 176-188.
12. GALEA E, REIS DJ, FEINSTEIN DL, 1994. Cloning and expression of inducible nitric oxide synthase from rat astrocytes. J Neurosci Res 37: 406-414.
13. GELLER DA, NUSSLER AK, DI SILVIO M, LOWENSTEIN CJ, SHAPIRO RA, WANG SC, SIMMONS RL, BILLIAR TR, 1993a. Cytokines, endotoxin, and glucocorticoids regulate the expression of inducible nitric oxide synthase in hepatocytes. Proc Natl Acad Sci USA 90: 522-526.
14. GELLER DA, LOWENSTEIN CJ, SHAPIRO RA, NUSSLER AK, DI SILVIO M WANG SC, NAKAYAMA DK, SIMMONS RL, SNYDER SH, BILLIAR TR, 1993b. Molecular cloning and expression of inducible nitric oxide synthase from human hepatocytes. Proc Natl Acad Sci USA 90: 3491-3495.
15. 15N) nitrate in biological fluids. J Anal Biochem 126: 131-138.
16. GROSS SS, LEVI R, 1992. Tetrahydrobiopterin synthesis. An absolute requirement for cytokine-induced nitric oxide generation by vascular smooth muscle. J Biol Chem 267: 25722-25729.
17. GUO FH, DERAEVE HR, RICE TW, STUEHR DJ, THUNNISSEN FB, ERZURUM SC, 1995. Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc Natl Acad Sci USA 92: 7809-7813.
18. GÜTLICH M, JAEGER E, RÜCKNAGEL KP, WERNER T, RÖDL W, ZIEGLER I, BACHER A, 1994. Human GTP cyclohydrolase I: only one out of three cDNA isoforms gives rise to the active enzyme. Biochem J 302: 215-221.
19. HABIB FM, SPRINGALL DR, DAVIES GJ, OAKLEY CM, YACOUB MH, POLAK JM, 1996. Tumor necrosis factor and inducible nitric oxide synthase in dilated cardiomyopathy. Lancet 347: 1151-1155.
20. HATAKEYAMA K, HARADA T, SUZUKI S, WATANABE Y, KAGAMIYAMA H, 1989. Purification and characterization of rat liver GTP cyclohydrolase I. Cooperative binding of GTP to the enzyme. J Biol Chem 264: 21660-21664.
21. HATAKEYAMA K, INOUE Y, HARADA T, KAGAMIYAMA H, 1991. Cloning and sequencing of cDNA encoding rat GTP cyclohydrolase I. The first enzyme of the tetrahydrobiopterin biosynthetic pathway. J Biol Chem 266: 765-769.
22. HAYWOOD GA, TSAO PS, VON DER LEYEH HE, MANN MJ, KEELING PJ, TRINDADE PT, LEWIS NP, BYRNE CD, RICKENBACHER PR, BISHOPRIC NH, COOKE JP, MCKENNA WJ, FOWLER MB, 1996. Expression of inducible nitric oxide synthase in human heart failure. Circulation 93: 1087-1094.
23. HOKARI A, ZENIYA M, ESUMI H, 1994. Cloning and functional expression of human inducible nitric oxide synthase (NOS) cDNA from a glioblastoma cell line A-172. J Biochem 116: 575-581.
24. JANSSENS SP, SHIMOUCHI A, QUERTERMOUS T, BLOCH DB, BLOCK KD, 1992. Cloning and expression of a cDNA encoding human endothelium-derived relaxing factor/ nitric oxide synthase. J Biol Chem 267: 14519-14522.
25. G-methyl-L-arginine inhibits tumor necrosis factor-induced hypotension: Implications for the involvement of nitric oxide. Proc Natl Acad Sci USA 87: 3629-3632.
26. G-monomethyl-L-arginine (NMA) restores arterial blood pressure but reduces cardiac output in a canine model of endotoxic shock. Biochem Biophys Res Commun 178: 1135-1140.
27. LAMAS S, MARSDEN PA, LI GK, TEMPST P, MICHEL T, 1992. Endothelial nitric oxide synthase: Molecular cloning and characterization of a distinct constitutive enzyme isoform. Proc Natl Acad Sci USA 89: 6348-6352.
28. LEWIS NP, TSAO PS, RICKENBACHER PR, XUE C, JOHNS RA, HAYWOOD GA, VON DER LEHEH H, TRINDADE PT, COOKE JP, HUNT SA, BILLINGHAM MG, VALANTINE HA, FOWLER MB, 1996. Induction of nitric oxide synthase in the human cardiac allograft is associated with contractile dysfunction of the left ventrical. Circulation 93: 720-729.
29. LI R-K, WEISEL RD, WILLIAMS WG, MICKLE DAG, 1992. Method of culturing cardiomyocytes from human pediatric ventricular myocardium. J Tiss Cult Meth 14: 93.
30. LI R-K, SHAIKH N, WEISEL RD, WILLIAMS WG, MICKLE DAG, 1994. Oxyradical-induced antioxidant and lipid changes in cultured human cardiomyocytes. Am J Physiol 266: H2204-H2211.
31. LOWENSTEIN CJ, GLATT CS, BREDT DS, SNYDER SH, 1992. Cloned and expressed macrophage nitric oxide synthase contrasts with the brain enzyme. Proc Natl Acad Sci USA 89: 6711-6715.
32. LOWRY OH, ROSEBROUGH NJ, FARR AL, RANDALL RJ, 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193: 265-275.
33. LUSS H, WATKINS SC, FREESWICK PD, IMRO AK, NUSSLER AK, BILLIAR TR, SIMMONS RL, DEL NIDO PJ, MCGOWAN FX JR, 1995. Characterization of inducible nitric oxide synthase expression in endotoxemic rat cardiac myocytes in vivo and following cytokine exposure in vitro. J Mol Cell Cardiol 27: 2015-2029.
34. LYONS CR, ORLOFF GJ, CUNNINGHAM JM, 1992. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J Biol Chem 267: 6370-6374.
35. MARSDEN PA, SCHAPPERT KT, CHEN HS, FLOWERS M, SUNDELL CL, WILCOX JN, LAMAS S, MICHEL T, 1992. Molecular cloning and characterization of human edothelial nitric oxide synthase. FEBS Lett 307: 287-293.
36. MORRIS SM JR, MONCMAN CL, HOLUB JS, HOD Y, 1989. Nutritional and hormonal regulation of mRNA abundance for arginine biosynthetic enzymes in kidney. Arch Biochem Biophys 273: 230-237.
37. NAKANE M, SCHMIDT HHHW, POLLOCK JS, FORSTERMANN U, MURAD F, 1993. Cloned human brain nitric oxide synthase is highly expressed in skeletal muscle. FEBS Lett 316: 175-180.
38. NAKAYAMA DK, GELLER DA, DI SILVIO M, BLOOMGARDEN G, DAVIES P, PITT BR, HATAKEYAMA K, KAGAMIYAMA H, SIMMONS RL, BILLIAR TR, 1994. Tetrahydrobiopterin synthesis and inducible nitric oxide production in pulmonary artery smooth muscle. Am J Physiol 266: L455-L460.
39. NISHIDA K, HARRISON DG, NAVAS JP, FISHER AA, DOCKERY SP, UEMATSU M, NEREM RM, ALEXANDER RW, MURPHY TJ, 1992. Molecular cloning and characterization of the constitutive bovine aortic endothelial cell nitric oxide synthase. J Clin Invest 90: 2092-2096.
40. NUNOKAWA Y, ISHIDA N, TANAKA S, 1993. Cloning of inducible nitric oxide synthase in rat vascular smooth muscle cells. Biochem Biophys Res Commun 191: 89-94.
41. NUSSLER AK, DI SILVIO M, BILLIAR TR, HOFFMAN RA, GELLER DA, SELBY R, MADARIAGA J, SIMMONS RL, 1992. Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J Exp Med 176: 261-264.
42. NUSSLER AK, BILLIAR TR, 1993. Inflammation, immunoregulation, and inducible nitric oxide synthase. J Leukoc Biol 54: 171-178.
43. NUSSLER AK, BILLIAR TR, LIU ZZ, MORRIS SM JR, 1994. Coinduction of nitric oxide synthase and arginino-succinate synthetase in a murine macrophage cell line. Implications for regulation of nitric oxide production. J Biol Chem 269: 1257-1261.
44. PINSKY DJ, OZ MC, KOGA S, TAHA Z, BROEKMAN MJ, MARCUS AJ, LIAO H, NAKA Y, BRETT J, CANNON PJ, NOWYGROD R, MALINSKI T, STERN DM, 1994. Cardiac preservation is enhanced in a heterotopic rat transplant model by supplementing the nitric oxide pathway. J Clin Invest 93: 2291-2297.
45. PINSKY DJ, CAI B, YANG X, RODRIGUEZ C, SCIACCA RR, CANNON PJ, 1995. The lethal effects of cytokine-induced nitric oxide on cardiac myocytes are blocked by nitric oxide synthase antagonism or transforming growth factor β. J Clin Invest 95: 677-685.
46. 2+-independent nitric oxide synthase in the myocardium. Br J Pharmacol 105: 575-580.
47. SESSA WC, HARRISON JK, BARBER CM, ZENG D, DURIEUX ME, D'ANGELO DD, LYNCH KR, PEACH MJ, 1992. Molecular cloning and expression of a cDNA encoding endothelial cell nitric oxide synthase. J Biol Chem 267: 15274-15276.
48. SHERMAN PA, LAUBACH VE, REEP BR, WOOD ER, 1993. Purification and cDNA sequence of an inducible nitric oxide synthase from a human tumor cell line. Biochemistry 32: 11600-11605.
49. THIEMERMANN C, SZABO C, MITCHELL JA, VANE JR, 1993. Vascular hyporeactivity to vasoconstrictor agents and hemodynamic decompensation in hemorrhagic shock is mediated by nitric oxide. Proc Natl Acad Sci USA 90: 267-271.
50. TZENG E, SHEARS LL, ROBBINS PD, PITT BR, GELLER DA, WATKINS SC, SIMMONS RL, BILLIAR TR, 1996. Vascular gene transfer of the human inducible nitric oxide synthase: characterization of activity and effects on myointimal hyperplasia. Molec Med 2: 211-225.
51. UNGUREANU-LONGROIS D, BALLIGAND JL, OKADA I, SIMMONS WW, KOBZIK L, LOWENSTEIN CJ, KUNKEL SL, MICHEL T, KELLY RA, SMITH TW, 1995. Contractile responsiveness of ventricular myocytes to isoproterenol is regulated by induction of nitric oxide synthase activity in cardiac microvascular endothelial cells in heterotypic primary culture. Circ Res 77: 486-493.
52. VODOVOTZ Y, BOGDAN C, PAIK J, XIE Q-W, NATHAN C, 1993. Mechanisms of suppression of macrophage nitric oxide release by transforming growth factor β. J Exp Med 178: 605-613.
53. WERNER-FELMAYER G, WERNER ER, FUCHS D, HAUSEN A, REIBNEGGERG, WACHTER H, 1990. Tetrahydrobiopterin-dependent formation of nitrite and nitrate in murine fibroblasts. J Exp Med 172: 1599-1607.
54. WOOD ER, BERGER H JR, SHERMAN PA, LAPETINA EG, 1993. Hepatocytes and macrophages express an identical cytokine inducible nitric oxide synthase gene. Biochem Biophys Res Commun 191: 767-774.
55. XIE QW, CHO HJ, CALAYCAY J, MUMFORD RA, SWIDEREK KM, LEE TD, DING A, TROSO T, NATHAN C, 1992. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256: 225-228.
56. YANG X, CHOWDHURY N, CAI B, BRETT J, MARBOE C, SCIACCA RR, MICHLER R, CANNON PJ, 1994. Induction of myocardial nitric oxide synthase by cardiac allograft rejection. J Clin Invest 94: 714-721.