The role of nitric oxide in the neural control of breathing

Respiratory Physiology and Neurobiology

Volumn 164, Issue 1-2, 2008, Pages 143-150

  Reeves, Stephen R ^a   Simakajornboon, Narong ^b   Gozal, David ^a  

^a University of Louisville School of Medicine   (United States)

^b CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

Author keywords

Carotid body; Control of ventilation; Nitric oxide; Respiratory control; S nitrosothiols; Synaptic plasticity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID; NITRIC OXIDE; S NITROSOGLUTATHIONE; S NITROSOTHIOL;

ARTICLE; BREATHING; CAROTID BODY; CENTRAL NERVOUS SYSTEM; CHEMORECEPTOR; HYPOXIA; LUNG VENTILATION; MOLECULAR INTERACTION; NERVE CELL PLASTICITY; NEUROMODULATION; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; RESPIRATION CONTROL; SIGNAL TRANSDUCTION;

ANIMALS; CENTRAL NERVOUS SYSTEM; CHEMORECEPTOR CELLS; HUMANS; NEUROTRANSMITTER AGENTS; NITRIC OXIDE; RESPIRATION;

EID: 53849131646     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2008.08.006     Document Type: Article

References (90)

1. Anbar M. Nitric oxide: a synchronizing chemical messenger. Experientia 51 (1995) 545-550
2. Andersson K.E. Erectile physiological and pathophysiological pathways involved in erectile dysfunction. J. Urol. 170 (2003) S6-S13
3. Arancio O., Kiebler M., Lee C.J., Lev-Ram V., Tsien R.Y., Kandel E.R., and Hawkins R.D. Nitric oxide acts directly in the presynaptic neuron to produce long-term potentiation in cultured hippocampal neurons. Cell 87 (1996) 1025-1035
4. Bogdanov M.B., and Wurtman R.J. Possible involvement of nitric oxide in NMDA-induced glutamate release in the rat striatum: an in vivo microdialysis study. Neurosci. Lett. 221 (1997) 197-201
5. Boulton C.L., Southam E., and Garthwaite J. Nitric oxide-dependent long-term potentiation is blocked by a specific inhibitor of soluble guanylyl cyclase. Neuroscience 69 (1995) 699-703
6. Bredt D.S., Hwang P.M., and Snyder S.H. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 347 (1990) 768-770
7. Bredt D.S., and Snyder S.H. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 682-685
8. Brenman J.E., and Bredt D.S. Synaptic signaling by nitric oxide. Curr. Opin. Neurobiol. 7 (1997) 374-378
9. Briggs C.A. Potentiation of nicotinic transmission in the rat superior cervical sympathetic ganglion: effects of cyclic GMP and nitric oxide generators. Brain Res. 573 (1992) 139-146
10. Campanucci V.A., Fearon I.M., and Nurse C.A. A novel O2-sensing mechanism in rat glossopharyngeal neurones mediated by a halothane-inhibitable background K+ conductance. J. Physiol. 548 (2003) 731-743
11. Campanucci V.A., and Nurse C.A. Biophysical characterization of whole-cell currents in O2-sensitive neurons from the rat glossopharyngeal nerve. Neuroscience 132 (2005) 437-451
12. Campanucci V.A., and Nurse C.A. Autonomic innervation of the carotid body: role in efferent inhibition. Respir. Physiol. Neurobiol. 157 (2007) 83-92
13. Chiueh C.C., and Rauhala P. The redox pathway of S-nitrosoglutathione, glutathione and nitric oxide in cell to neuron communications. Free Radic. Res. 31 (1999) 641-650
14. Chugh D.K., Katayama M., Mokashi A., Bebout D.E., Ray D.K., and Lahiri S. Nitric oxide-related inhibition of carotid chemosensory nerve activity in the cat. Respir. Physiol. 97 (1994) 147-156
15. Culotta E., and Koshland Jr. D.E. NO news is good news. Science 258 (1992) 1862-1865
16. de Paula P.M., and Branco L.G. Nitric oxide in the rostral ventrolateral medulla modulates hyperpnea but not anapyrexia induced by hypoxia. Brain Res. 977 (2003) 231-238
17. de Vente J., and Steinbusch H.W. On the stimulation of soluble and particulate guanylate cyclase in the rat brain and the involvement of nitric oxide as studied by cGMP immunocytochemistry. Acta Histochem. 92 (1992) 13-38
18. Eldridge F.L., and Millhorn D.E. Oscillation, gating, and memory in the respiratory control system. Control of Breathing. Handbook of Physiology vol. 2 (1986), American Physiological Society, Bethesda, MD, USA pp. 93-114
19. Fabris G., Steiner A.A., nselmo-Franci J.A., and Branco L.G. Role of nitric oxide in rat locus coeruleus in hypoxia-induced hyperventilation and hypothermia. Neuroreport 11 (2000) 2991-2995
20. Fujimori H., and Pan-Hou H. Effect of nitric oxide on l-[3H]glutamate binding to rat brain synaptic membranes. Brain Res. 554 (1991) 355-357
21. Fuller D.D., Zabka A.G., Baker T.L., and Mitchell G.S. Phrenic long-term facilitation requires 5-HT receptor activation during but not following episodic hypoxia. J. Appl. Physiol. 90 (2001) 2001-2006
22. Fung M.L., Ye J.S., and Fung P.C. Acute hypoxia elevates nitric oxide generation in rat carotid body in vitro. Pflugers Arch. 442 (2001) 903-909
23. Furchgott R.F., and Zawadzki J.V. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 288 (1980) 373-376
24. Gaston B., Singel D., Doctor A., and Stamler J.S. S-nitrosothiol signaling in respiratory biology. Am. J. Respir. Crit Care Med. 173 (2006) 1186-1193
25. Gozal D. Potentiation of hypoxic ventilatory response by hyperoxia in the conscious rat: putative role of nitric oxide. J. Appl. Physiol. 85 (1998) 129-132
26. Gozal D., and Gozal E. Episodic hypoxia enhances late hypoxic ventilation in developing rat: putative role of neuronal NO synthase. Am. J. Physiol. 276 (1999) R17-R22
27. Gozal D., Gozal E., Gozal Y.M., and Torres J.E. Nitric oxide synthase isoforms and peripheral chemoreceptor stimulation in conscious rats. Neuroreport 7 (1996) 1145-1148
28. Gozal D., Gozal E., Torres J.E., Gozal Y.M., Nuckton T.J., and Hornby P.J. Nitric oxide modulates ventilatory responses to hypoxia in the developing rat. Am. J. Respir. Crit. Care Med. 155 (1997) 1755-1762
29. Gozal D., Torres J.E., Gozal Y.M., and Littwin S.M. Effect of nitric oxide synthase inhibition on cardiorespiratory responses in the conscious rat. J. Appl. Physiol. 81 (1996) 2068-2077
30. Gruetter C.A., Barry B.K., McNamara D.B., Gruetter D.Y., Kadowitz P.J., and Ignarro L. Relaxation of bovine coronary artery and activation of coronary arterial guanylate cyclase by nitric oxide, nitroprusside and a carcinogenic nitrosoamine. J. Cyclic Nucleotide Res. 5 (1979) 211-224
31. Gruetter C.A., Barry B.K., McNamara D.B., Kadowitz P.J., and Ignarro L.J. Coronary arterial relaxation and guanylate cyclase activation by cigarette smoke. N′-nitrosonornicotine and nitric oxide. J. Pharmacol. Exp. Ther. 214 (1980) 9-15
32. Hamalainen M.M., and Lovick T.A. Involvement of nitric oxide and serotonin in modulation of antinociception and pressor responses evoked by stimulation in the dorsolateral region of the periaqueductal gray matter in the rat. Neuroscience 80 (1997) 821-827
33. Haxhiu M.A., Chang C.H., Dreshaj I.A., Erokwu B., Prabhakar N.R., and Cherniack N.S. Nitric oxide and ventilatory response to hypoxia. Respir. Physiol. 101 (1995) 257-266
34. He L., Chen J., Liu X., Dinger B., and Fidone S. Enhanced nitric oxide-mediated chemoreceptor inhibition and altered cyclic GMP signaling in rat carotid body following chronic hypoxia. Am. J. Physiol. Lung Cell Mol. Physiol. 293 (2007) L1463-L1468
35. Hedrick M.S., and Morales R.D. Nitric oxide as a modulator of central respiratory rhythm in the isolated brainstem of the bullfrog (Rana catesbeiana). Comp. Biochem. Physiol. A Mol. Integr. Physiol. 124 (1999) 243-251
36. Hevel J.M., White K.A., and Marletta M.A. Purification of the inducible murine macrophage nitric oxide synthase. Identification as a flavoprotein. J. Biol. Chem. 266 (1991) 22789-22791
37. Holscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity. Trends Neurosci. 20 (1997) 298-303
38. Honda Y., Tani H., Masuda A., Kobayashi T., Nishino T., Kimura H., Masuyama S., and Kuriyama T. Effect of prior O2 breathing on ventilatory response to sustained isocapnic hypoxia in adult humans. J. Appl. Physiol. 81 (1996) 1627-1632
39. Huang P.L., Dawson T.M., Bredt D.S., Snyder S.H., and Fishman M.C. Targeted disruption of the neuronal nitric oxide synthase gene. Cell 75 (1993) 1273-1286
40. Ignarro L.J., Buga G.M., Wood K.S., Byrns R.E., and Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 84 (1987) 9265-9269
41. Jia L., Bonaventura C., Bonaventura J., and Stamler J.S. S-nitrosohaemoglobin: a dynamic activity of blood involved in vascular control. Nature 380 (1996) 221-226
42. Katsuki S., Arnold W., Mittal C., and Murad F. Stimulation of guanylate cyclase by sodium nitroprusside, nitroglycerin and nitric oxide in various tissue preparations and comparison to the effects of sodium azide and hydroxylamine. J. Cyclic Nucleotide Res. 3 (1977) 23-35
43. Kline D.D., Overholt J.L., and Prabhakar N.R. Mutant mice deficient in NOS-1 exhibit attenuated long-term facilitation and short-term potentiation in breathing. J. Physiol. 539 (2002) 309-315
44. Kline D.D., and Prabhakar N.R. Peripheral chemosensitivity in mutant mice deficient in nitric oxide synthase. Adv. Exp. Med. Biol. 475 (2000) 571-579
45. Kline D.D., Yang T., Huang P.L., and Prabhakar N.R. Altered respiratory responses to hypoxia in mutant mice deficient in neuronal nitric oxide synthase. J. Physiol. 511 Pt 1 (1998) 273-287
46. Kline D.D., Yang T., Premkumar D.R., Thomas A.J., and Prabhakar N.R. Blunted respiratory responses to hypoxia in mutant mice deficient in nitric oxide synthase-3. J. Appl. Physiol. 88 (2000) 1496-1508
47. Kuriyama K., and Ohkuma S. Role of nitric oxide in central synaptic transmission: effects on neurotransmitter release. Jpn. J. Pharmacol. 69 (1995) 1-8
48. Kusakabe T., Matsuda H., Harada Y., Hayashida Y., Gono Y., Kawakami T., and Takenaka T. Changes in the distribution of nitric oxide synthase immunoreactive nerve fibers in the chronically hypoxic rat carotid body. Brain Res. 795 (1998) 292-296
49. Lahiri S., Roy A., Baby S.M., Hoshi T., Semenza G.L., and Prabhakar N.R. Oxygen sensing in the body. Prog. Biophys. Mol. Biol. 91 (2006) 249-286
50. Lancaster Jr. J.R. A tutorial on the diffusibility and reactivity of free nitric oxide. Nitric Oxide 1 (1997) 18-30
51. Leger L., Charnay Y., Burlet S., Gay N., Schaad N., Bouras C., and Cespuglio R. Comparative distribution of nitric oxide synthase- and serotonin-containing neurons in the raphe nuclei of four mammalian species. Histochem. Cell Biol. 110 (1998) 517-525
52. Ling L., Karius D.R., Fiscus R.R., and Speck D.F. Endogenous nitric oxide required for an integrative respiratory function in the cat brain. J. Neurophysiol. 68 (1992) 1910-1912
53. Lipton A.J., Johnson M.A., Macdonald T., Lieberman M.W., Gozal D., and Gaston B. S-nitrosothiols signal the ventilatory response to hypoxia. Nature 413 (2001) 171-174
54. Lovick T.A. Role of nitric oxide in medullary raphe-evoked inhibition of neuronal activity in the periaqueductal gray matter. Neuroscience 75 (1996) 1203-1209
55. Ma S., Abboud F.M., and Felder R.B. Effects of l-arginine-derived nitric oxide synthesis on neuronal activity in nucleus tractus solitarius. Am. J. Physiol. 268 (1995) R487-R491
56. Mayer B., and Bohme E. Ca2+-dependent formation of an l-arginine-derived activator of soluble guanylyl cyclase in bovine lung. FEBS Lett. 256 (1989) 211-214
57. 2+-dependently converts l-arginine into an activator of soluble guanylyl cyclase. Biochem. Biophys. Res. Commun. 164 (1989) 678-685
58. Mizusawa A., Ogawa H., Kikuchi Y., Hida W., Kurosawa H., Okabe S., Takishima T., and Shirato K. In vivo release of glutamate in nucleus tractus solitarii of the rat during hypoxia. J. Physiol. 478 (1994) 55-66
59. Nei K., Matsuyama S., Shuntoh H., and Tanaka C. NMDA receptor activation induces glutamate release through nitric oxide synthesis in guinea pig dentate gyrus. Brain Res. 728 (1996) 105-110
60. Ogawa H., Mizusawa A., Kikuchi Y., Hida W., Miki H., and Shirato K. Nitric oxide as a retrograde messenger in the nucleus tractus solitarii of rats during hypoxia. J. Physiol. 486 Pt 2 (1995) 495-504
61. Ohkuma S., and Katsura M. Nitric oxide and peroxynitrite as factors to stimulate neurotransmitter release in the CNS. Prog. Neurobiol. 64 (2001) 97-108
62. Palacios M., Knowles R.G., Palmer R.M., and Moncada S. Nitric oxide from l-arginine stimulates the soluble guanylate cyclase in adrenal glands. Biochem. Biophys. Res. Commun. 165 (1989) 802-809
63. Palmer R.M., Ashton D.S., and Moncada S. Vascular endothelial cells synthesize nitric oxide from l-arginine. Nature 333 (1988) 664-666
64. Palmer R.M., Ferrige A.G., and Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327 (1987) 524-526
65. Palmer R.M., Rees D.D., Ashton D.S., and Moncada S. l-Arginine is the physiological precursor for the formation of nitric oxide in endothelium-dependent relaxation. Biochem. Biophys. Res. Commun. 153 (1988) 1251-1256
66. Pape H.C., and Mager R. Nitric oxide controls oscillatory activity in thalamocortical neurons. Neuron 9 (1992) 441-448
67. Pierrefiche O., Abdala A.P., and Paton J.F. Nitric oxide and respiratory rhythm in mammals: a new modulator of phase transition?. Biochem. Soc. Trans. 35 (2007) 1258-1263
68. Pierrefiche O., Maniak F., and Larnicol N. Rhythmic activity from transverse brainstem slice of neonatal rat is modulated by nitric oxide. Neuropharmacology 43 (2002) 85-94
69. Pollock J.S., Forstermann U., Mitchell J.A., Warner T.D., Schmidt H.H., Nakane M., and Murad F. Purification and characterization of particulate endothelium-derived relaxing factor synthase from cultured and native bovine aortic endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 88 (1991) 10480-10484
70. Prabhakar N.R. NO and CO as second messengers in oxygen sensing in the carotid body. Respir. Physiol. 115 (1999) 161-168
71. Prabhakar N.R., Kumar G.K., Chang C.H., Agani F.H., and Haxhiu M.A. Nitric oxide in the sensory function of the carotid body. Brain Res. 625 (1993) 16-22
72. Ramirez J.M., and Richter D.W. The neuronal mechanisms of respiratory rhythm generation. Curr. Opin. Neurobiol. 6 (1996) 817-825
73. Ramirez J.M., Telgkamp P., Elsen F.P., Quellmalz U.J., and Richter D.W. Respiratory rhythm generation in mammals: synaptic and membrane properties. Respir. Physiol. 110 (1997) 71-85
74. Reeves S.R., and Gozal D. Developmental plasticity of respiratory control following intermittent hypoxia. Respir. Physiol. Neurobiol. 149 (2005) 301-311
75. Reeves S.R., Gozal E., Guo S.Z., Sachleben Jr. L.R., Brittian K.R., Lipton A.J., and Gozal D. Effect of long-term intermittent and sustained hypoxia on hypoxic ventilatory and metabolic responses in the adult rat. J. Appl. Physiol. 95 (2003) 1767-1774
76. Rekling J.C., and Feldman J.L. PreBotzinger complex and pacemaker neurons: hypothesized site and kernel for respiratory rhythm generation. Annu. Rev. Physiol. 60 (1998) 385-405
77. Schmidt H.H., Hofmann H., Schindler U., Shutenko Z.S., Cunningham D.D., and Feelisch M. No.NO from NO synthase. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 14492-14497
78. Schuman E.M., and Madison D.V. Nitric oxide and synaptic function. Annu. Rev. Neurosci. 17 (1994) 153-183
79. Schwenke D.O., Pearson J.T., Kangawa K., and Shirai M. Does central nitric oxide chronically modulate the acute hypoxic ventilatory response in conscious rats?. Acta Physiol. (Oxf.) 186 (2006) 309-318
80. Tagawa T., Imaizumi T., Harada S., Endo T., Shiramoto M., Hirooka Y., and Takeshita A. Nitric oxide influences neuronal activity in the nucleus tractus solitarius of rat brainstem slices. Circ. Res. 75 (1994) 70-76
81. Taylor B.E., Harris M.B., Burk M., Smyth K., Lukowiak K., and Remmers J.E. Nitric oxide mediates metabolism as well as respiratory and cardiac responses to hypoxia in the snail lymnaea stagnalis. J. Exp. Zoolog. A Comp. Exp. Biol. 295 (2003) 37-46
82. Toda N., Toda H., and Hatano Y. Nitric oxide: involvement in the effects of anesthetic agents. Anesthesiology 107 (2007) 822-842
83. Tomita S., Nicoll R.A., and Bredt D.S. PDZ protein interactions regulating glutamate receptor function and plasticity. J. Cell Biol. 153 (2001) F19-F24
84. Torres J.E., Kreisman N.R., and Gozal D. Nitric oxide modulates in vitro intrinsic optical signal and neural activity in the nucleus tractus solitarius of the rat. Neurosci. Lett. 232 (1997) 175-178
85. Travagli R.A., and Gillis R.A. Nitric oxide-mediated excitatory effect on neurons of dorsal motor nucleus of vagus. Am. J. Physiol. 266 (1994) G154-G160
86. Trzebski A., Sato Y., Suzuki A., and Sato A. Inhibition of nitric oxide synthesis potentiates the responsiveness of carotid chemoreceptors to systemic hypoxia in the rat. Neurosci. Lett. 190 (1995) 29-32
87. Wang Z.Z., Bredt D.S., Fidone S.J., and Stensaas L.J. Neurons synthesizing nitric oxide innervate the mammalian carotid body. J. Comp. Neurol. 336 (1993) 419-432
88. Wang Z.Z., Dinger B.G., Stensaas L.J., and Fidone S.J. The role of nitric oxide in carotid chemoreception. Biol. Signals 4 (1995) 109-116
89. Wang Z.Z., Stensaas L.J., Bredt D.S., Dinger B., and Fidone S.J. Localization and actions of nitric oxide in the cat carotid body. Neuroscience 60 (1994) 275-286
90. Yetik-Anacak G., and Catravas J.D. Nitric oxide and the endothelium: history and impact on cardiovascular disease. Vascul. Pharmacol. 45 (2006) 268-276