Nitric oxide and carbon monoxide synthesizing enzymes and soluble guanylyl cyclase within neurons of adult human cardiac ganglia

Autonomic Neuroscience: Basic and Clinical

Volumn 145, Issue 1-2, 2009, Pages 93-98

  Singh, Sanjay ^a   Gray, Thackery ^a   Wurster, Robert D ^a,b  

^a LOYOLA UNIVERSITY MEDICAL CENTER   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Carbon monoxide; Cardiac ganglia; Human; Nitric oxide; Parasympathetic nervous system; Postganglionic cells; Soluble guanylyl cyclase

Indexed keywords

CARBON MONOXIDE; GUANYLATE CYCLASE; HEME OXYGENASE 2; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE;

ADULT; AGED; ARTICLE; AUTOPSY; CHOLINERGIC SYSTEM; FEMALE; HEART FUNCTION; HEART NERVE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NEUROMODULATION; NEUROTRANSMISSION; POSTGANGLIONIC NERVE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT; AGED; ATRIOVENTRICULAR NODE; CARBON MONOXIDE; CELLS, CULTURED; FEMALE; GANGLIA, PARASYMPATHETIC; GUANYLATE CYCLASE; HEME OXYGENASE (DECYCLIZING); HUMANS; MALE; MIDDLE AGED; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SINOATRIAL NODE; YOUNG ADULT;

EID: 58149466169     PISSN: 15660702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.autneu.2008.11.008     Document Type: Article

References (37)

1. Armour J.A., Smith F.M., Losier A.M., Ellenberger H.H., and Hopkins D.A. Modulation of intrinsic cardiac neuronal activity by nitric oxide donors induces cardiodynamic changes. Am. J. Physiol. 268 (1995) R403-R413
2. Bredt D.S., Hwang P.M., Glatt C.E., Lowenstein C., Reed R.R., and Snyder S.H. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 351 (1991) 714-718
3. Canning B.J., and Fischer A. Localization of heme oxygenase-2 immunoreactivity to parasympathetic ganglia of human and guinea-pig airways. Am. J. Respir. Cell Mol. Biol. 18 (1998) 279-285
4. Choate J.K., Danson E.J., Morris J.F., and Paterson D.J. Peripheral vagal control of heart rate is impaired in neuronal NOS knockout mice. Am. J. Physiol. 281 (2001) H2310-H2317
5. Conlon K., and Kidd C. Neuronal nitric oxide facilitates vagal chronotropic and dromotropic actions on the heart. J. Auton. Nerv. Syst. 75 (1999) 136-146
6. De Belder A.J., Radomski M.W., Martin J.F., and Moncada S. Nitric oxide and the pathogenesis of heart muscle disease. Eur. J. Clin. Investig. 25 (1995) 1-8
7. Debruyne L.A., Magee J.C., Buelow R., and 1 Bromberg J.S. Gene transfer of immunomodulatory peptides correlates with heme oxygenase-1 induction and enhanced allograft survival. Transplantation 69 (2000) 120-128
8. Elvan A., Rubart M., and Zipes D.P. NO modulates autonomic effects on sinus discharge rate and AV nodal conduction in open-chest dogs. Am. J. Physiol. 272 (1997) H263-H271
9. Fukuchi M., Hussain S.N., and Giaid A. Heterogeneous expression and activity of endothelial and inducible nitric oxide synthases in end-stage human heart failure: their relation to lesion site and beta-adrenergic receptor therapy. Circulation 98 (1998) 132-139
10. Garcia S.B., Paula J.S., Giovannetti G.S., Zenha F., Ramalho E.M., Zucolota S., Silva J.S., and Cunha F.Q. Nitric oxide is involved in the lesions of the peripheral autonomic neurons observed in the acute phase of experimental Trypanosoma cruzi infection. Exp. Parasitol. 93 (1999) 191-197
11. Han X., Shimoni Y., and Giles W.R. An obligatory role for nitric oxide in autonomic control of mammalian heart rate. J. Physiol. (Lond.) 476 (1994) 309-314
12. Hassall C.J., and Hoyle C.H. Heme oxygenase-2 and nitric oxide synthase in guinea-pig intracardiac neurones. Neuroreport 8 (1997) 1043-1046
13. Horackova M., Armour J.A., Hopkins D.A., and Huang M.H. Nitric oxide modulates signaling between cultured adult peripheral cardiac neurons and cardiomyocytes. Am. J. Physiol. 269 (1995) C504-C510
14. Huang H., Chan J., Wittner M., Jelicks L.A., Morris S.A., Factor S.M., Weiss L.M., Braustein V.L., Bacchi C.J., Yarlett N., Chandra M., Shirani J., and Tanowitz H.B. Expression of cardiac cytokines and inducible form of nitric oxide synthase (NOS2) in Trypanosoma cruzi-infected mice. J. Mol. Cell. Cardiol. 31 (1999) 75-88
15. Kelly R.A., Balligand J.L., and Smith T.W. Nitric oxide and cardiac function. Circ. Res. 79 (1996) 363-380
16. Klimaschewski L., Kummer W., Mayer B., Couraud J.Y., Preissler U., Philippin B., and Heym C. Nitric oxide synthase in cardiac nerve fibers and neurons of rat and guinea pig heart. Circ. Res. 71 (1992) 1533-1537
17. Lewis N.P., Tsao P.S., Rickenbacher P.R., Xue C., John R.A., Haywood G.A., Hunt S.A., Billingham M.E., Valantine H.A., and Fowler M.B. Induction of nitric oxide synthase in the human cardiac allograft is associated with contractile dysfunction of the left ventricle. Circulation 93 (1996) 720-729
18. Maines M.D. The heme oxygenase system: a regulator of second messenger gases. Annu. Rev. Pharmacol. Toxicol. 37 (1997) 517-554
19. Markos F., Snow H.M., Kidd C., and Conlon K. Nitric oxide facilitates vagal control of heart rate via actions in the cardiac parasympathetic ganglia of the anesthetized dog. Exp. Physiol. 54 (2002) 47-54
20. Matsumoto T., Nakane M., Pollock J.S., Kuk J.E., and Forstermann U. A correlation between soluble brain nitric oxide synthase and NADPH-diaphorase activity is only seen after exposure of the tissue to fixative. Neurosci. Lett. 155 (1993) 61-64
21. Maulik N., Engelman D.T., Watanabe M., Engelman R.M., Roousou J.A., Flack J.E., Deaton D.W., Gorbunov N.V., Elsayed N.M., Kagan V.E., and Das D.K. Nitric oxide/carbon monoxide. A molecular switch for myocardial preservation during ischemia. Circulation 94 (1996) II398-II406
22. Mawe G.M., Talmage E.K., Lee K.P., and Parsons R.L. Expression of choline acetyltransferase immunoreactivity in guinea pig cardiac ganglia. Cell Tissue Res. 285 (1996) 281-286
23. Mohan R.M., Heaton D.A., Danson E.J., Krishnan S.P., Cai S., Channon K.M., and Paterson D.J. Neuronal nitric oxide synthase gene transfer promotes cardiac vagal gain of function. Circ. Res. 91 (2002) 1089-1091
24. Sears C.E., Choate J.K., and Paterson D.J. Effect of nitric oxide synthase inhibition on the sympatho-vagal control of heart rate. J. Auton. Nerv. Syst. 73 (1998) 63-73
25. Seki T., Naruse M., Naruse K., Yoshimoto T., Tanabe S., Seki M., Tago K., Imaki T., Demura R., and Demura H. Induction of heme oxygenase produces load-independent cardio-protective effects in hypertensive rats. Life Sci. 65 (1999) 1077-1086
26. Seshadri N., Dweik R.A., Laskowski D., Pothier C., Rodriquez L., Young J.B., and Migrino R.Q. Dysregulation of endogenous carbon monoxide and nitric oxide production in patients with advanced ischemic or nonischemic cardiomyopathy. Am. J. Cardiol. 92 (2002) 820-823
27. Singh S., Johnson P.I., Lee R.E., Orfei E., Lonchyna V.A., Sullivan H.J., Montoya A., Tran H., Wehrmacher W.H., and Wurster R.D. Topography of cardiac ganglia in the adult human heart. J. Thorac. Cardiovasc. Surg. 112 (1996) 943-953
28. Snyder S.H., Jaffrey S.R., and Zakhary R. Nitric oxide and carbon monoxide: parallel roles as neural messengers. Brain Res. Brain Res. Rev. 26 (1998) 167-175
29. Sosunov A.A., Hassall C.J., Loesch A., Turmaine M., and Burnstock G. Nitric oxide synthase-containing neurons and nerve fibers within cardiac ganglia of rat and guinea-pig: an electron-microscopic immunocytochemical study. Cell Tissue Res. 284 (1996) 19-28
30. Steele P.A., Gibbins I.L., Morris J.L., and Mayer B. Multiple populations of neuropeptide-containing intrinsic neurons in the guinea-pig heart. Neuroscience 62 (1994) 241-250
31. Tanaka K., and Chiba T. The vagal origin of preganglionic fibers containing nitric oxide synthase in the guinea-pig heart. Neurosci. Lett. 252 (1998) 135-138
32. Tanaka K., Hassall C.J., and Burnstock G. Distribution of intracardiac neurones and nerve terminals that contain a marker for nitric oxide, NADPH-diaphorase, in the guinea-pig heart. Cell Tissue Res. 273 (1993) 293-300
33. Tracey W.R., Nakane M., Pollock J.S., and Forstermann U. Nitric oxide synthases in neuronal cells, macrophages and endothelium are NADPH diaphorases, but represent only a fraction of total cellular NADPH diaphorase activity. Biochem. Biophys. Res. Commun. 195 (1993) 1035-1040
34. Traub R.J., Solodkin A., Meller S.T., and Gebhart G.F. Spinal cord NADPH-diaphorase histochemical staining but not nitric oxide synthase immunoreactivity increases following carrageenan-produced hindpaw inflammation in the rat. Brain Res. 668 (1994) 204-210
35. Vollerthun R., Hohler B., and Kummer W. Guinea-pig sympathetic postganglionic neurons contain haemoxygenase-2. Neuroreport 7 (1995) 173-176
36. Wang D., Yang X.P., Liu Y.H., Carretero O.A., and LaPointe M.C. Reduction of myocardial infarct size by inhibition of inducible nitric oxide synthase. Am. J. Hypertens. 12 (1999) 174-182
37. Yoshida K., and Toda N. NADPH diaphorase-positive neurons in the intracardiac plexus of human, monkey and canine right atria. Brain Res. 724 (1996) 256-259