Targeting neuronal nitric oxide synthase with gene transfer to modulate cardiac autonomic function

Progress in Biophysics and Molecular Biology

Volumn 84, Issue 2-3, 2004, Pages 321-344

  Mohan, R M ^a   Golding, S ^a   Heaton, D A ^a   Danson, E J ^a   Paterson, D J ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Autonomic nervous system; Gene transfer; Heart; Nitric oxide synthase

Indexed keywords

ADENOVIRIDAE;

EID: 1242276565     PISSN: 00796107     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pbiomolbio.2003.11.013     Document Type: Review

References (130)

1. Arnolda L.F., McKitrick D.J., Llewellyn-Smith I.J., Minson J.B. Nitric oxide limits pressure responses to sympathetic activation in rat spinal cord. Hypertension. 36:2000;1089-1092.
2. Ashley E.A., Sears C.E., Bryant S.M., Watkins H.C., Casadei B. Cardiac nitric oxide synthase 1 regulates basal and beta-adrenergic contractility in murine ventricular myocytes. Circulation. 105:2002;3011-3016.
3. Baek S., March K.L. Gene therapy for restenosis. getting nearer the heart of the matter Circ. Res. 82:1998;295-305.
4. Baker A.H., Mehta D., George S.J., Angelini G.D. Prevention of vein graft failure. potential applications for gene therapy Cardiovasc. Res. 35:1997;442-450.
5. Balligand J.L. Regulation of cardiac beta-adrenergic response by nitric oxide. Cardiovasc. Res. 43:1999;607-620.
6. Balligand J.L., Kelly R.A., Marsden P.A., Smith T.W., Michel T. Control of cardiac muscle cell function by an endogenous nitric oxide signaling system. Proc. Natl. Acad. Sci. U.S.A. 90:1993;347-351.
7. Bao S., Thrall B.D., Miller D.L. Transfection of a reporter plasmid into cultured cells by sonoporation in vitro. Ultrasound Med. Biol. 23:1997;953-959.
8. Barouch L.A., Harrison R.W., Skaf M.W., Rosas G.O., Cappola T.P., Kobeissi Z.A., Hobai I.A., Lemmon C.A., Burnett A.L., O'Rourke B., Rodriguez E.R., Huang P.L., Lima J.A., Berkowitz D.E., Hare J.M. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature. 416:2002;337-339.
9. Barry M.A., Dower W.J., Johnston S.A. Toward cell-targeting gene therapy vectors. selection of cell-binding peptides from random peptide-presenting phage libraries Nat. Med. 2:1996;299-305.
10. Bates T.E., Loesch A., Burnstock G., Clark J.B. Mitochondrial nitric oxide synthase. a ubiquitous regulator of oxidative phosphorylation? Biochem. Biophys. Res. Commun. 218:1996;40-44.
11. Biewenga J.E., Destree O.H., Schrama L.H. Plasmid-mediated gene transfer in neurons using the biolistics technique. J. Neurosci. Methods. 71:1997;67-75.
12. Bueler H. Adeno-associated viral vectors for gene transfer and gene therapy. Biol. Chem. 380:1999;613-622.
13. Calupca M.A., Vizzard M.A., Parsons R.L. Origin of neuronal nitric oxide synthase (NOS)-immunoreactive fibers in guinea pig parasympathetic cardiac ganglia. J. Comp. Neurol. 426:2000;493-504.
14. Casadei B., Paterson D.J. Should we still use nitrovasodilators to test baroreflex sensitivity? J. Hypertens. 18:2000;3-6.
15. Catala F., Wanner R., Barton P., Cohen A., Wright W., Buckingham M. A skeletal muscle-specific enhancer regulated by factors binding to E and CArG boxes is present in the promoter of the mouse myosin light-chain 1A gene. Mol. Cell. Biol. 15:1995;4585-4596.
16. Channon K.M., Blazing M.A., Shetty G.A., Potts K.E., George S.E. Adenoviral gene transfer of nitric oxide synthase. high level expression in human vascular cells Cardiovasc. Res. 32:1996;962-972.
17. Choate J.K., Paterson D.J. Nitric oxide inhibits the positive chronotropic and inotropic responses to sympathetic nerve stimulation in the isolated guinea-pig atria. J. Auton. Nerv. System. 75:1999;100-108.
18. Choate J.K., Danson E.J., Morris J.F., Paterson D.J. Peripheral vagal control of heart rate is impaired in neuronal NOS knockout mice. Am. J. Physiol. Heart Circ. Physiol. 281:2001;H2310-H2317.
19. Chowdhary S., Townend J.N. Role of nitric oxide in the regulation of cardiovascular autonomic control. Clin. Sci. 97:1999;5-17.
20. Chowdhary S., Harrington D., Bonser R.S., Coote J.H., Townend J.N. Chronotropic effects of nitric oxide in the denervated human heart. J. Physiol. 541:2002;645-651.
21. Coleman J.E., Huentelman M.J., Kasparov S., Metcalfe B.L., Paton J.F., Katovich M.J., Semple-Rowland S.L., Raizada M.K. Efficient large-scale production and concentration of HIV-1-based lentiviral vectors for use in vivo. Physiol. Genomics. 12:2003;221-228.
22. Conlon K., Kidd C. Neuronal nitric oxide facilitates vagal chronotropic and dromotropic actions on the heart. J. Auton. Nerv. System. 75:1999;136-146.
23. Danialou G., Comtois A.S., Dudley R.W., Nalbantoglu J., Gilbert R., Karpati G., Jones D.H., Petrof B.J. Ultrasound increases plasmid-mediated gene transfer to dystrophic muscles without collateral damage. Mol. Ther. 6:2002;687-693.
24. Danson E.J., Paterson D.J. Enhanced neuronal nitric oxide synthase expression is central to cardiac vagal phenotype in exercise-trained mice. J. Physiol. 546:2003;225-232.
25. DiFrancesco D., Tortora P. Direct activation of cardiac pacemaker channels by intracellular cyclic AMP. Nature. 351:1991;145-147.
26. Dimmeler S., Fleming I., Fisslthaler B., Hermann C., Busse R., Zeiher A.M. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature. 399:1999;601-605.
27. Doorbar J., Winter G. Isolation of a peptide antagonist to the thrombin receptor using phage display. J. Mol. Biol. 244:1994;361-369.
28. Dull T., Zufferey R., Kelly M., Mandel R.J., Nguyen M., Trono D., Naldini L. A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72:1998;8463-8471.
29. Einfeld D.A., Roelvink P.W. Advances towards targetable adenovirus vectors for gene therapy. Curr. Opin. Mol. Ther. 4:2002;444-451.
30. Elvan A., Rubart M., 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.
31. Farson D., Witt R., McGuinness R., Dull T., Kelly M., Song J., Radeke R., Bukovsky A., Consiglio A., Naldini L. A new-generation stable inducible packaging cell line for lentiviral vectors. Hum. Gene Ther. 12:2001;981-997.
32. Ferdinandy P., Schulz R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br. J. Pharmacol. 138:2003;532-543.
33. Feron O., Belhassen L., Kobzik L., Smith T.W., Kelly R.A., Michel T. Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J. Biol. Chem. 271:1996;22810-22814.
34. Fisher K.D., Stallwood Y., Green N.K., Ulbrich K., Mautner V., Seymour L.W. Polymer-coated adenovirus permits efficient retargeting and evades neutralising antibodies. Gene Ther. 8:2001;341-348.
35. Forstermann U., Closs E.I., Pollock J.S., Nakane M., Schwarz P., Gath I., Kleinert H. Nitric oxide synthase isozymes. Characterization, purification, molecular cloning, and functions. Hypertension. 23:1994;1121-1131.
36. French B.A., Mazur W., Ali N.M., Geske R.S., Finnigan J.P., Rodgers G.P., Roberts R., Raizner A.E. Percutaneous transluminal in vivo gene transfer by recombinant adenovirus in normal porcine coronary arteries, atherosclerotic arteries, and two models of coronary restenosis. Circulation. 90:1994;2402-2413.
37. Friebe A., Koesling D. Regulation of nitric oxide-sensitive guanylyl cyclase. Circ. Res. 93:2003;96-105.
38. 2+ in sea urchin eggs by stimulating cyclic ADP-ribose synthesis [see comments]. Nature. 365:1993;456-459.
39. Gehl J. Electroporation. theory and methods, perspectives for drug delivery, gene therapy and research Acta Physiol. Scand. 177:2003;437-447.
40. Goins W.F., Krisky D.M., Wolfe D.P., Fink D.J., Glorioso J.C. Development of replication-defective herpes simplex virus vectors. Methods Mol. Med. 69:2002;481-507.
41. Goldberg N.D., Haddox M.K. Cyclic GMP metabolism and involvement in biological regulation. Annu. Rev. Biochem. 1997+ADs. 46:1977;823-896.
42. Goodson R.J., Doyle M.V., Kaufman S.E., Rosenberg S. High-affinity urokinase receptor antagonists identified with bacteriophage peptide display. Proc. Natl. Acad. Sci. USA. 91:1994;7129-7133.
43. Griffith T.M., Edwards D.H., Lewis M.J., Newby A.C., Henderson A.H. The nature of endothelium-derived vascular relaxant factor. Nature. 308:1984;645-647.
44. Grossin L., Cournil-Henrionnet C., Mir L.M., Liagre B., Dumas D., Etienne S., Guingamp C., Netter P., Gillet P. Direct gene transfer into rat articular cartilage by in vivo electroporation. FASEB J. 17:2003;829-835.
45. Hakim M.A., Hirooka Y., Coleman M.J., Bennett M.R., Dampney R.A. Evidence for a critical role of nitric oxide in the tonic excitation of rabbit renal sympathetic preganglionic neurons. J. Physiol. 482(Part 2):1995;401-407.
46. Han X., Shimoni Y., Giles W.R. An obligatory role for nitric oxide in autonomic control of mammalian heart rate. J. Physiol. (London). 476:1994;309-314.
47. 2+ current in adult rabbit atrioventricular nodal cells. Circ. Res. 78:1996;998-1008.
48. Han X., Kubota I., Feron O., Opel D.J., Arstall M.A., Zhao Y.Y., Huang P., Fishman M.C., Michel T., Kelly R.A. Muscarinic cholinergic regulation of cardiac myocyte ICa-L is absent in mice with targeted disruption of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U.S.A. 95:1998;6510-6515.
49. Heaton, D.A., Mohan, R.M., Krishnan, S.P., Everatt, L., Golding, S., Paterson, D.J., 2003. Cardiac nNOS gene transfer decreases beta-adrenergic hyper-responsiveness and enhances vagal function in spontaneously hypertensive rats. Circulation 108, S872.
50. Henry L., Xia D., Wilke M., Deisenhofer J., Gerard R. Characterization of the knob domain of the adenovirus type 5 fiber protein expressed in Escherichia coli. J. Virol. 68:1994;5239-5246.
51. Herring N., Paterson D.J. Nitric oxide-cGMP pathway facilitates acetylcholine release and bradycardia during vagal nerve stimulation in the guinea-pig in vitro. J. Physiol. 535:2001;507-518.
52. Herring N., Golding S., Paterson D.J. Pre-synaptic NO-cGMP pathway modulates vagal control of heart rate in isolated adult guinea pig atria. J. Mol. Cell. Cardiol. 32:2000;1795-1804.
53. Herring N., Danson E.J., Paterson D.J. Cholinergic control of heart rate by nitric oxide is site specific. News Physiol. Sci. 17:2002;202-206.
54. Hevel J.M., White K.A., Marletta M.A. Purification of the inducible murine macrophage nitric oxide synthase. Identification as a flavoprotein. J. Biol. Chem. 266:1991;22789-22791.
55. Hong S.S., Magnusson M.K., Henning P., Lindholm L., Boulanger P.A. Adenovirus stripping. a versatile method to generate adenovirus vectors with new cell target specificity Mol. Ther. 7:2003;692-699.
56. Hwang D.Y., Carlezon W.A. Jr., Isacson O., Kim K.S. A high-efficiency synthetic promoter that drives transgene expression selectively in noradrenergic neurons. Hum. Gene Ther. 12:2001;1731-1740.
57. Ignarro L.J. Signal transduction mechanisms involving nitric oxide. Biochem. Pharmacol. 41:1991;485-490.
58. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. USA. 84:1987;9265-9269.
59. Jiao S., Cheng L., Wolff J.A., Yang N.S. Particle bombardment-mediated gene transfer and expression in rat brain tissues. Biotechnology (N Y). 11:1993;497-502.
60. Jumrussirikul P., Dinerman J., Dawson T.M., Dawson V.L., Ekelund U., Georgakopoulos D., Schramm L.P., Calkins H., Snyder S.H., Hare J.M., Berger R.D. Interaction between neuronal nitric oxide synthase and inhibitory G protein activity in heart rate regulation in conscious mice. J. Clin. Invest. 102:1998;1279-1285.
61. Kanai A.J., Pearce L.L., Clemens P.R., Birder L.A., VanBibber M.M., Choi S.Y., de Groat W.C., Peterson J. Identification of a neuronal nitric oxide synthase in isolated cardiac mitochondria using electrochemical detection. Proc. Natl. Acad. Sci. USA. 98:2001;14126-14131.
62. Kasparov S., Paton J.F. Differential effects of angiotensin II in the nucleus tractus solitarii of the rat - plausible neuronal mechanism. J. Physiol. 521(Part 1):1999;227-238.
63. Kaye D., Wiviott S., Balligand J., Smith T. Nitric oxide inhibits norepinephrine uptake in cardiac sympathetic neurons. Circulation. 92(Suppl I):1995;507.
64. Keaney J.F. Jr., Hare J.M., Balligand J.L., Loscalzo J., Smith T.W., Colucci W.S. Inhibition of nitric oxide synthase augments myocardial contractile responses to beta-adrenergic stimulation. Am. J. Physiol. 271:1996;H2646-H2652.
65. Kelly R.A., Balligand J.L., Smith T.W. Nitric oxide and cardiac function. Circ. Res. 79:1996;363-380.
66. Khan S.A., Skaf M.W., Harrison R.W., Lee K., Minhas K.M., Kumar A., Fradley M., Shoukas A.A., Berkowitz D.E., Hare J.M. Nitric oxide regulation of myocardial contractility and calcium cycling. independent impact of neuronal and endothelial nitric oxide synthases Circ. Res. 92:2003;1322-1329.
67. Kishi T., Hirooka Y., Sakai K., Shigematsu H., Shimokawa H., Takeshita A. Overexpression of eNOS in the RVLM causes hypotension and bradycardia via GABA release. Hypertension. 38:2001;896-901.
68. Klimaschewski L., Kummer W., Mayer B., Couraud J.Y., Preissler U., Philippin B., Heym C. Nitric oxide synthase in cardiac nerve fibers and neurons of rat and guinea pig heart. Circ. Res. 71:1992;1533-1537.
69. Koga N., Takano Y., Honda K., Saito R., Kamiya H. Roles of nitric oxide in the spinal cord in cardiovascular regulation in rats. Neurosci. Lett. 267:1999;173-176.
70. Krasnykh V., Dmitriev I., Mikheeva G., Miller C.R., Belousova N., Curiel D.T. Characterization of an adenovirus vector containing a heterologous peptide epitope in the HI loop of the fiber knob. J. Virol. 72:1998;1844-1852.
71. Krasnykh V., Belousova N., Korokhov N., Mikheeva G., Curiel D.T. Genetic targeting of an adenovirus vector via replacement of the fiber protein with the phage T4 fibritin. J. Virol. 75:2001;4176-4183.
72. Krukoff T.L. Central actions of nitric oxide in regulation of autonomic functions. Brain Res. Brain Res. Rev. 30:1999;52-65.
73. Lampert R., Ickovics J.R., Viscoli C.J., Horwitz R.I., Lee F.A. Effects of propranolol on recovery of heart rate variability following acute myocardial infarction and relation to outcome in the Beta-Blocker Heart Attack Trial. Am. J. Cardiol. 91:2003;137-142.
74. Lemarchand P., Jaffe H.A., Danel C., Cid M.C., Kleinman H.K., Stratford-Perricaudet L.D., Perricaudet M., Pavirani A., Lecocq J.P., Crystal R.G. Adenovirus-mediated transfer of a recombinant human alpha 1-antitrypsin cDNA to human endothelial cells. Proc. Natl. Acad. Sci. USA. 89:1992;6482-6486.
75. Lemarchand P., Jones M., Yamada I., Crystal R.G. In vivo gene transfer and expression in normal uninjured blood vessels using replication-deficient recombinant adenovirus vectors. Circ. Res. 72:1993;1132-1138.
76. Li S., Benninger M. Applications of muscle electroporation gene therapy. Curr. Gene Ther. 2:2002;101-105.
77. Lin H.C., Wan F.J., Cheng K.K., Tseng C.J. Nitric oxide signaling pathway mediates the L-arginine-induced cardiovascular effects in the nucleus tractus solitarii of rats. Life Sci. 65:1999;2439-2451.
78. Lincoln T.M., Cornwell T.L. Intracellular cyclic GMP receptor proteins. FASEB J. 7:1993;328-338.
79. Lincoln T.M., Komalavilas P., Boerth N.J., MacMillan-Crow L.A., Cornwell T.L. cGMP signalling through cAMP- and cGMP-dependent protein kinases. Ignarro L., Murad F. Advances in Pharmacology: Nitric Oxide: Biochemistry, Molecular Biology and Therapeutic Implications. 1995;305-321 Academic Press, San Diego.
80. Magnusson M.K., Hong S.S., Boulanger P., Lindholm L. Genetic retargeting of adenovirus. novel strategy employing "deknobbing" of the fiber J. Virol. 75:2001;7280-7289.
81. Manome Y., Nakamura M., Ohno T., Furuhata H. Ultrasound facilitates transduction of naked plasmid DNA into colon carcinoma cells in vitro and in vivo. Hum. Gene Ther. 11:2000;1521-1528.
82. Markos F., Snow H.M., Kidd C., Conlon K. Nitric oxide facilitates vagal control of heart rate via actions in the cardiac parasympathetic ganglia of the anaesthetised dog. Exp. Physiol. 87:2002;49-52.
83. Mawe G.M., Talmage E.K., Lee K.P., Parsons R.L. Expression of choline acetyltransferase immunoreactivity in guinea pig cardiac ganglia. Cell Tissue Res. 285:1996;281-286.
84. Michel T., Feron O. Nitric oxide synthases. which, where, how and why? J. Clin. Invest. 100:1997;2146-2152.
85. Mohan R.M., Choate J.K., Golding S., Herring N., Casadei B., Paterson D.J. Peripheral pre-synaptic pathway reduces the heart rate response to sympathetic activation following exercise training. role of NO Cardiovasc. Res. 47:2000;90-98.
86. Mohan R.M., Heaton D.A., Danson E.J., Krishnan S.P., Cai S., Channon K.M., Paterson D.J. Neuronal nitric oxide synthase gene transfer promotes cardiac vagal gain of function. Circ. Res. 91:2002;1089-1091.
87. Murad F. Cyclic GMP. synthesis, metabolism, and function. Introduction and some historical comments Adv. Pharmacol. 26:1994;1-5.
88. Musialek P., Lei M., Brown H.F., Paterson D.J., Casadei B. Nitric oxide can increase heart rate by stimulating the hyperpolarization-activated inward current, I(f). Circ. Res. 81:1997;60-68.
89. Naciff J.M., Behbehani M.M., Misawa H., Dedman J.R. Identification and transgenic analysis of a murine promoter that targets cholinergic neuron expression. J. Neurochem. 72:1999;17-28.
90. Nakamura T., Sato K., Hamada H. Reduction of natural adenovirus tropism to the liver by both ablation of fiber-coxsackievirus and adenovirus receptor interaction and use of replaceable short fiber. J. Virol. 77:2003;2512-2521.
91. Ng P., Beauchamp C., Evelegh C., Parks R., Graham F.L. Development of a FLP/frt system for generating helper-dependent adenoviral vectors. Mol. Ther. 3:2001;809-815.
92. Nicklin S.A., White S.J., Watkins S.J., Hawkins R.E., Baker A.H. Selective targeting of gene transfer to vascular endothelial cells by use of peptides isolated by phage display. Circulation. 102:2000;231-237.
93. Nicklin S.A., Von Seggern D.J., Work L.M., Pek D.C., Dominiczak A.F., Nemerow G.R., Baker A.H. Ablating adenovirus type 5 fiber-CAR binding and HI loop insertion of the SIGYPLP peptide generate an endothelial cell-selective adenovirus. Mol. Ther. 4:2001;534-542.
94. Palmer R.M., Moncada S. A novel citrulline-forming enzyme implicated in the formation of nitric oxide by vascular endothelial cells. Biochem. Biophys. Res. Commun. 158:1989;348-352.
95. Pasqualini R., Ruoslahti E. Organ targeting in vivo using phage display peptide libraries. Nature. 380:1996;364-366.
96. Paton J.F., Boscan P., Murphy D., Kasparov S. Unravelling mechanisms of action of angiotensin II on cardiorespiratory function using in vivo gene transfer. Acta Physiol. Scand. 173:2001;127-137.
97. Paton J.F., Deuchars J., Ahmad Z., Wong L.F., Murphy D., Kasparov S. Adenoviral vector demonstrates that angiotensin II-induced depression of the cardiac baroreflex is mediated by endothelial nitric oxide synthase in the nucleus tractus solitarii of the rat. J. Physiol. 531:2001;445-458.
98. Paton J.F., Kasparov S., Paterson D.J. Nitric oxide and autonomic control of heart rate. a question of specificity Trends Neurosci. 25:2002;626-631.
99. Pinsky D.J., Patton S., Mesaros S., Brovkovych V., Kubaszewski E., Grunfeld S., Malinski T. Mechanical transduction of nitric oxide synthesis in the beating heart. Circ. Res. 81:1997;372-379.
100. Rajotte D., Arap W., Hagedorn M., Koivunen E., Pasqualini R., Ruoslahti E. Molecular heterogeneity of the vascular endothelium revealed by in vivo phage display. J. Clin. Invest. 102:1998;430-437.
101. Reynolds P.N., Zinn K.R., Gavrilyuk V.D., Balyasnikova I.V., Rogers B.E., Buchsbaum D.J., Wang M.H., Miletich D.J., Grizzle W.E., Douglas J.T., Danilov S.M., Curiel D.T. A targetable, injectable adenoviral vector for selective gene delivery to pulmonary endothelium in vivo. Mol. Ther. 2:2000;562-578.
102. Ruggeri P., Battaglia A., Ermirio R., Grossini E., Molinari C., Mary D.A., Vacca G. Role of nitric oxide in the control of the heart rate within the nucleus ambiguus of rats. Neuroreport. 11:2000;481-485.
103. Sakai K., Hirooka Y., Matsuo I., Eshima K., Shigematsu H., Shimokawa H., Takeshita A. Overexpression of eNOS in NTS causes hypotension and bradycardia in vivo. Hypertension. 36:2000;1023-1028.
104. Santis G., Legrand V., Hong S.S., Davison E., Kirby I., Imler J.L., Finberg R.W., Bergelson J.M., Mehtali M., Boulanger P. Molecular determinants of adenovirus serotype 5 fibre binding to its cellular receptor CAR. J. Gen. Virol. 80(Part 6):1999;1519-1527.
105. Schmidt H.H., Lohmann S.M., Walter U. The nitric oxide and cGMP signal transduction system. regulation and mechanism of action Biochim. Biophys. Acta. 1178:1993;153-175.
106. Schulz R., Smith J.A., Lewis M.J., Moncada S. Nitric oxide synthase in cultured endocardial cells of the pig. Br. J. Pharmacol. 104:1991;21-24.
107. Schwarz P., Diem R., Dun N.J., Forstermann U. Endogenous and exogenous nitric oxide inhibits norepinephrine release from rat heart sympathetic nerves. Circ. Res. 77:1995;841-848.
108. Sears C.E., Choate J.K., Paterson D.J. Effect of nitric oxide synthase inhibition on the sympatho-vagal control of heart rate. J. Auton. Nerv. System. 73:1998;63-73.
109. Sears C.E., Choate J.K., Paterson D.J. NO-cGMP pathway accentuates the decrease in heart rate caused by cardiac vagal nerve stimulation. J. Appl. Physiol. 86:1999;510-516.
110. Sears C.E., Bryant S.M., Ashley E.A., Lygate C.A., Rakovic S., Wallis H.L., Neubauer S., Terrar D.A., Casadei B. Cardiac neuronal nitric oxide synthase isoform regulates myocardial contraction and calcium handling. Circ. Res. 92:2003;e52-e59.
111. Sterin-Borda L., Genaro A., Perez Leiros C., Cremaschi G., Vila Echague A., Borda E. Role of nitric oxide in cardiac beta-adrenoceptor-inotropic response. Cell Signal. 10:1998;253-257.
112. Stuehr D.J., Griffith O.W. Mammalian nitric oxide synthases. Adv. Enzymol. Relat. Areas Mol. Biol. 65:1992;287-346.
113. Su E.J., Stevenson S.C., Rollence M., Marshall-Neff J., Liau G. A genetically modified adenoviral vector exhibits enhanced gene transfer of human smooth muscle cells. J. Vasc. Res. 38:2001;471-478.
114. Takehara Y., Kanno T., Yoshioka T., Inoue M., Utsumi K. Oxygen-dependent regulation of mitochondrial energy metabolism by nitric oxide. Arch. Biochem. Biophys. 323:1995;27-32.
115. Takita T., Ikeda J., Sekiguchi Y., Demachi J., Li S.L., Shirato K. Nitric oxide modulates sympathetic control of left ventricular contraction in vivo in the dog. J. Auton. Nerv. System. 71:1998;69-74.
116. Tanaka K., Chiba T. Nitric oxide synthase containing nerves in the atrioventricular node of the guinea pig heart. J. Auton. Nerv. System. 51:1995;245-253.
117. Teichert A.M., Miller T.L., Tai S.C., Wang Y., Bei X., Robb G.B., Phillips M.J., Marsden P.A. In vivo expression profile of an endothelial nitric oxide synthase promoter-reporter transgene. Am. J. Physiol. Heart Circ. Physiol. 278:2000;H1352-H1361.
118. Tomko R.P., Xu R., Philipson L. HCAR and MCAR. the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses PNAS. 94:1997;3352-3356.
119. Trong H.L., Beier N., Sonnenburg W.K., Stroop S.D., Walsh K.A., Beavo J.A., Charbonneau H. Amino acid sequence of the cyclic GMP stimulated cyclic nucleotide phosphodiesterase from bovine heart. Biochemistry. 29:1990;10280-10288.
120. van Beusechem V.W., van Rijswijk A.L., van Es H.H., Haisma H.J., Pinedo H.M., Gerritsen W.R. Recombinant adenovirus vectors with knobless fibers for targeted gene transfer. Gene Ther. 7:2000;1940-1946.
121. Vandecasteele G., Eschenhagen T., Scholz H., Stein B., Verde I., Fischmeister R. Muscarinic and beta-adrenergic regulation of heart rate, force of contraction and calcium current is preserved in mice lacking endothelial nitric oxide synthase. Nat. Med. 5:1999;331-334.
122. Watkins S.J., Mesyanzhinov V.V., Kurochkina L.P., Hawkins R.E. The 'adenobody' approach to viral targeting. specific and enhanced adenoviral gene delivery Gene Ther. 4:1997;1004-1012.
123. Wells J.M., Li L.H., Sen A., Jahreis G.P., Hui S.W. Electroporation- enhanced gene delivery in mammary tumors. Gene Ther. 7:2000;541-547.
124. White K.A., Marletta M.A. Nitric oxide synthase is a cytochrome P-450 type hemoprotein. Biochemistry. 31:1992;6627-6631.
125. Wu S.Y., Dun N.J. Calcium-activated release of nitric oxide potentiates excitatory synaptic potentials in immature rat sympathetic preganglionic neurons. J. Neurophysiol. 74:1995;2600-2603.
126. Wu S.Y., Dun N.J. Potentiation of IPSCs by nitric oxide in immature rat sympathetic preganglionic neurons in vitro. J. Physiol. 495(Part 2):1996;479-490.
127. Xia D., Henry L.J., Gerard R.D., Deisenhofer J. Crystal structure of the receptor-binding domain of adenovirus type 5 fiber protein at 1.7 A resolution. Structure. 2:1994;1259-1270.
128. Xu K.Y., Huso D.L., Dawson T.M., Bredt D.S., Becker L.C. Nitric oxide synthase in cardiac sarcoplasmic reticulum. Proc. Natl. Acad. Sci. U.S.A. 96:1999;657-662.
129. Zanzinger J. Role of nitric oxide in the neural control of cardiovascular function. Cardiovasc. Res. 43:1999;639-649.
130. Zhang L.Q., Mei Y.F., Wadell G. Human adenovirus serotypes 4 and 11 show higher binding affinity and infectivity for endothelial and carcinoma cell lines than serotype 5. J. Gen. Virol. 84:2003;687-695.