Pertussis toxin-sensitive G proteins influence nitric oxide synthase III activity and protein levels in rat heart

Journal of Clinical Investigation

Volumn 101, Issue 6, 1998, Pages 1424-1431

  Hare, Joshua M ^a,b   Kim, Benjamin ^a   Flavahan, Nicholas A ^a   Ricker, Kelly M ^a   Peng, Xinqi ^a   Colman, Laurence ^a   Weiss, Robert G ^a   Kass, David A ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b JOHNS HOPKINS HOSPITAL   (United States)

Author keywords

L arginine; Muscarinic receptor; Myocardial contractility; Phospholipase C; adrenergic receptor

Indexed keywords

ACETYLCHOLINE; ARGININE; BETA ADRENERGIC RECEPTOR; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; ISOPRENALINE; MUSCARINIC RECEPTOR; NITRIC OXIDE SYNTHASE; PERTUSSIS TOXIN; PHOSPHOLIPASE C; PROTEIN;

ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; ENZYME ACTIVITY; HEART MUSCLE CONTRACTILITY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; TISSUE LEVEL;

EID: 0032521132     PISSN: 00219738     EISSN: None     Source Type: Journal    
DOI: 10.1172/JCI1012     Document Type: Article

References (51)

1. Henning, R.J., I.R. Khalil, and M.N. Levy. 1990. Vagal stimulation attenuates sympathetic enhancement of left ventricular function. Am. J. Physiol. 258: H1470-H1475.
2. Kelly, R.A., J.-L. Balligand, and T.W. Smith. 1996. Nitric oxide and cardiac function. Circ. Res. 79:363-380.
3. Hare, J.M., J.F. Keaney, Jr., J.-L. Balligand, J. Loscalzo, T.W. Smith, and W.S. Colucci. 1995. Role of nitric oxide in parasympathetic modulation of β-adrenergic myocardial contractility in normal dogs. J. Clin. Invest. 95:360-366.
4. Balligand, J.-L., L. Kobzik, X. Han, D.M. Kaye, L. Beihassen, D.S. O'Hara, R.A. Kelly, T.W. Smith, and T. Michel. 1995. Nitric oxide-dependent parasympathetic signaling is due to activation of constitutive endothelial (type III) nitric oxide synthase in cardiac myocytes. J. Biol. Chem. 270:14582-14586.
5. Balligand, J.-L., R.A. Kelly, P.A. Marsden, T.W. Smith, and T. Michel. 1993. Control of cardiac muscle cell function by an endogenous nitric oxide signaling system. Proc. Natl. Acad. Sci. USA. 90:347-351.
6. 2+ current. J. Biol. Chem. 268:26286-26295.
7. Belhassen, L., R.A. Kelly, T.W. Smith, and J.-L. Balligand. 1996. Nitric oxide synthase (NOS3) and contractile responsiveness to adrenergic and cholinergic agonists in the heart. J. Clin. Invest. 97:1908-1915.
8. Balligand, J.-L., D. Ungureanu-Longois, W.W. Simmons, L. Kobzik, C.J. Lowenstein, S. Lamas, R.A. Kelly, T.W. Smith, and T. Michel. 1995. Induction of NO synthase in rat cardiac microvascular endothelial cells by IL-1β and IFN-γ. Am. J. Physiol. 268:H1293-H1303.
9. Han, X., Y. Shimoni, and W.R. Giles. 1994. An obligatory role for nitric oxide in autonomic control of mammalian heart rate. J. Physiol. 476:309-314.
10. Han, X., Y. Shimoni, and W.R. Giles. 1995. A cellular mechanism for nitric oxide-mediated cholinergic control of mammalian heart rate. J. Gen. Physiol. 106:45-65.
11. Ca, by carbachol and sodium nitroprusside. Pflugers Arch. 426:419-426.
12. Fleming, J.W., T.D. Hodges, and A.M. Watanabe. 1988. Pertussis toxintreated dog: a whole animal model of impaired inhibitory regulation of adenylate cyclase. Circ. Res. 62:992-1000.
13. Adamson, P.B., S.S. Hull, Jr., E. Vanoli, G.M. De Ferrari, P. Wisler, R.D. Foreman, A.M. Watanabe, and P.J. Schwartz. 1993. Pertussis toxin-induced ADP ribosylation of inhibitor G proteins alters vagal control of heart rate in vivo. Am. J. Physiol. 265:H734-H740.
14. Tucek, S., V. Dulezal, J. Folbergrova, S. Hynie, F. Kolar, and B. Ostadal. 1987. Pertussis toxin inhibits negative inotropic and negative chronotropic muscarinic cholinergic effects on the heart. Pflugers Arch. 408:167-172.
15. Boyer, J.L., M. Martinez-Carcamo, A. Monroy-Sanchez, J. Juarez-Ayala, G. Pastelin, C. Posadas, and J.A. Garcia-Sainz. 1986. Effect of pertussis toxin on the heart muscarinic-cholinergic receptors and their function. Life Sci. 39:603-610.
16. Neer, E.J. 1995. Heterotrimeric G proteins: organizers of transmembrane signals. Cell. 80:249-257.
17. Flavahan, N.A., H. Shimokawa, and P.M. Vanhoutte. 1991. Inhibition of endothelium-derived relaxations by phorbol myristate acetate in canine coronary arteries: role of a pertussis toxin-sensitive G-protein. J. Pharmacol. Exp. Ther. 256:50-55.
18. Miller, V.M., N.A. Flavahan, and P.M. Vanhoutte. 1991. Pertussis toxin reduces endothelium-dependent and independent responses to alpha-2 adrenergic stimulation in systemic canine arteries and veins. J. Pharmacol. Exp. Ther. 257:290-293.
19. Liao, J.K., and C.J. Homcy. 1993. The G proteins of the Gαi and Gαq family couple the bradykinin receptor to the release of endothelium-derived relaxing factor. J. Clin. Invest. 92:2168-2172.
20. Kuchan, M.J., H. Jo, and J.A. Frangos. 1994. Role of G proteins in shear stress-mediated nitric oxide production by endothelial cells. Am. J. Physiol. 267:C753-C758.
21. Sterin-Borda, L., A.V. Echague, C.P. Leiros, A. Genaro, and E. Borda. 1995. Endogenous nitric oxide signaling system and the cardiac muscarinic acetylcholine receptor-inotropic response. Br. J. Pharmacol. 115:1525-1531.
22. Weiss, R.G., C.P. de Albuquerque, K. Vandegaer, V.P. Chacko, and G. Gerstenblith. 1997. Attenuated glycogenolysis reduces glycolytic catabolite accumulation during ischemia in preconditioned rat hearts. Circ. Res. 79:435-446.
23. max and oxygen consumption in blood-perfused rabbit hearts. Circ. Res. 68:482-492.
24. Keaney, J.F., Jr., J.M. Hare, R.A. Kelly, J. Loscalzo, T.W. Smith, and W.S. Colucci. 1996. Inhibition of nitric oxide synthase potentiates the positive inotropic response to β-adrenergic stimulation in normal dogs. Am. J. Physiol. 271:H2646-H2652.
25. Berger, H.-J., S.K. Prasad, A.J. Davidoff, D. Pimental, O. Ellingsen, J.D. Marsh, T.W. Smith, and R.A. Kelly. 1994. Continual electric field stimulation preserves contractile function of adult ventricular myocytes in primary culture. Am. J. Physiol. 266:H341-H349.
26. Kapadia, S.R., H. Oral, J. Lee, M. Nakano, G.E. Taffet, and D.L. Mann. 1997. Hemodynamic regulation of tumor necrosis factor-α gene and protein expression in adult feline myocardium. Circ. Res. 81:187-195.
27. Bredt, D., and S. Snyder. 1990. Isolation of nitric oxide synthase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA. 87:682-685.
28. 2+)-independent nitric oxide synthase in the myocardium. Br. J. Pharmacol. 105:575-580.
29. Wallenstein, S., C. Zucker, and J. Fleiss. 1980. Some statistical methods useful in Circulation Research. Circ. Res. 47:1-9.
30. Hare, J.M., E. Loh, M.A. Creager, and W.S. Colucci. 1995. Nitric oxide inhibits the contractile response to β-adrenergic stimulation in humans with left ventricular dysfunction. Circulation. 92:2198-2203.
31. George, W.J., J.B. Polson, A.C. O'Toole, and N.D. Goldberg. 1970. Elevation of guanosine 3′,5′-cyclic phosphate in rat heart after perfusion with acetylcholine. Proc. Natl. Acad. Sci. USA. 66:398-403.
32. George, W.J., R.D. Wilkerson, and P.J. Kadowitz. 1973. Influence of acetylcholine on contractile force and cyclic nucleotide levels in the isolated perfused rat heart. J. Pharmacol. Exp. Ther. 184:228-235.
33. Krause, E., W. Halle, and A. Wollenberger. 1972. Effect of dibutyryl cyclic GMP on cultured beating rat heart cells. Adv. Cyclic Nucleotide Res. 1:301-305.
34. Shah, A.M., M.J. Lewis, and A.H. Henderson. 1991. Effects of 8-bromocyclic GMP on contraction and on inotropic response of ferret cardiac muscle. J. Mol. Cell. Cardiol. 23:55-64.
35. Watanabe, A.M., and H.R. Besch, Jr. 1975. Interaction between cyclic adenosine monophosphate and cyclic guanosine monophosphate in guinea pig ventricular myocardium. Circ. Res. 37:309-317.
36. 2+ current is regulated by cyclic GMP-dependent protein kinase in mammalian cardiac myocytes. Proc: Natl. Acad. Sci. USA. 88:1197-1201.
37. 2+ current in single heart cells. Nature. 323:273-275.
38. 2+ in intact cardiac myocytes. Circ. Res. 74:970-978.
39. Freeman, J.E., IV, W.Y. Kuo, G. Milligan, C.J. Lowenstein, M.A. Levine, and N.A. Flavahan. 1995. Analysis of pertussis toxin-sensitive receptor: G-protein interactions in native porcine endothelial cells. Endothelium. 3:321-330.
40. iα2. J. Biol. Chem. 268:19528-19533.
41. Liao, J.K., and C.J. Homcy. 1992. Specific receptor-guanine nucleotide binding protein interaction mediates the release of endothelium-derived relaxing factor. Circ. Res. 70:1018-1026.
42. i proteins by low density lipoprotein attenuates bradykinin-stimulated release of endothelial-derived nitric oxide. J. Biol. Chem. 269:12987-12992.
43. Feron, U., T.W. Smith, T. Michel, and R.A. Kelly. 1997. Dynamic targeting of the agonist-stimulated m2 muscarinic acetylcholine receptor to caveolae in cardiac myocytes. J. Biol. Chem. 272:17744-17748.
44. Fleming, J.W., P.L. Wisler, and A.M. Watanabe. 1992. Signal transduction by G proteins in cardiac tissues. Circulation. 85:420-133.
45. Ayajiki, K., M. Kindermann, M. Hecker, I. Fleming, and R. Busse. 1996. Intracellular pH and tyrosine phosphorylation but not calcium determine shear stress-induced nitric oxide production in native endothelial cells. Circ. Res. 78: 750-758.
46. Stamler, J.S., E. Loh, M. Roddy, K.E. Curríe, and M.A. Creager. 1994. Nitric oxide regulates basal systemic and pulmonary vascular resistance in healthy humans. Circulation. 89:2035-2040.
47. Klabunde, R.E., R.C. Ritger, and M.C. Helgren. 1991. Cardiovascular actions of inhibitors of endothelium-derived relaxing factor (nitric oxide) formation/release in anesthetized dogs. Eur. J. Pharmacol. 199:51-59.
48. Kojda, G., K. Kottenberg, P. Nix, K.D. Schluter, H.M. Piper, and E. Noack. 1996. Low increase in cGMP induced by organic nitrates and nitrovasodilators improves contractile response of rat ventricular myocytes. Circ. Res. 78:91-101.
49. Campbell, D.L., J.S. Stamler, and H.C. Strauss. 1996. Redox modulation of L-type calcium channels in ferret ventricular myocytes. Dual mechanism regulation by nitric oxide and S-nitrosothiols. J. Gen. Physiol. 108:277-293.
50. Cockcroft, S., and B.D. Gomperts. 1985. Role of guanine nucleotide binding protein in the activation of polyphosphoinositide phosphodiesterase. Nature. 314:534-536.
51. Vitale, N., D. Thierse, D. Aunis, and M.-F. Bader. 1993. Exocytosis in chromaffin cells: evidence for a MgATP-independent step that requires a pertussis toxin-sensitive GTP-binding protein. Biochem. J. 300:217-227.