NO in the caudal NTS modulates the increase in respiratory frequency in response to chemoreflex activation in awake rats

Respiratory Physiology and Neurobiology

Volumn 166, Issue 1, 2009, Pages 32-40

  Granjeiro, Érica M ^a   Machado, Benedito H ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Autonomic nervous system; l NAME; N PLA; Nitric oxide synthase; Peripheral chemoreflex

Indexed keywords

NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

ANIMAL EXPERIMENT; ARTERIAL PRESSURE; ARTICLE; AUTONOMIC INNERVATION; BREATHING RATE; CAUDAL NUCLEUS TRACTUS SOLITARIUS; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RESPIRATION CONTROL; SOLITARY TRACT NUCLEUS;

ANILIDES; ANIMALS; ARGININE; BLOOD PRESSURE; ENZYME INHIBITORS; HEART RATE; MALE; MICROINJECTIONS; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; PLETHYSMOGRAPHY, WHOLE BODY; RATS; RATS, WISTAR; REFLEX; RESPIRATION; SOLITARY NUCLEUS; WAKEFULNESS;

EID: 62749186886     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2009.01.003     Document Type: Article

References (58)

1. Abu-Soud H.M., Rousseau D.L., and Stuehr D.J. Nitric oxide binding to the heme of neuronal nitric-oxide synthase links its activity to changes in oxygen tension. J. Biol. Chem. 271 (1996) 32515-32518
2. Accorsi-Mendonça D., Leão R.M., Aguiar J.F., Varanda W.A., and Machado B.H. Urethane inhibits the GABAergic neurotransmission in the nucleus of the solitary tract of rat brain stem slices. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292 (2007) R396-R402
3. Almado C.E., and Machado B.H. Respiratory and autonomic responses to microinjection of NMDA and AMPA into the commissural subnucleus of the NTS of awake rats. Brain Res. 1063 (2005) 59-68
4. Antunes V.R., Bonagamba L.G.H., and Machado B.H. Hemodynamic and respiratory responses to microinjection of ATP into the intermediate and caudal commissural NTS of awake rats. Brain Res. 1032 (2005) 85-93
5. Barraco R.A., O'Lear D.S., Ergene E., and Scislo T.J. Activation of purinergic receptor subtypes in the nucleus tractus solitarius elicits specific regional vascular response patterns. J. Auton. Nerv. Syst. 59 (1996) 113-124
6. Barros R.A., Bonagamba L.G.H., Okamoto-Canesin R., de Oliveira M., Branco L.G.S., and Machado B.H. Cardiovascular responses to chemoreflex activation with potassium cyanide or hypoxic hypoxia in awake rats. Auton. Neurosci.: Basic Clin. 97 (2002) 110-115
7. Bartlett, and Tenney S.M. Control of breathing in experimental anemia. Respir. Physiol. 10 (1970) 384-395
8. Braccialli A.L., Bonagamba L.G., and Machado B.H. Glutamatergic and purinergic mechanisms on respiratory modulation in the caudal NTS of awake rats. Respir. Physiol. Neurobiol. 31 161 (2008) 246-252
9. Braga V.A., Soriano R.N., Braccialli A.L., de Paula P.M., Paton J.F.R., and Machado B.H. Involvement of l-glutamate and ATP in the neurotransmission of sympatheexcitatory component of the chemoreflex in the commissural NTS of awake rats and in the working heart brainstem preparation. J. Physiol. 581 (2007) 1129-1145
10. Chitravanshi V.C., and Sapru H.N. Chemoreceptor-sensitive neurons in commissural subnucleus of nucleus tractus solitarius of the rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 268 (1995) R851-R858
11. Ciriello J., Hochstenbach S.L., and Roder S. Central projections of baroreceptor and chemoreceptor afferent fibers in the rat. In: Robin I., and Barraco A. (Eds). Nucleus of the Solitary Tract (1994), CRC Press, Boca Raton, USA
12. de Paula P.M., Antunes V.R., Bonagamba L.G.H., and Machado B.H. Cardiovascular responses to microinjection of ATP into the nucleus tractus solitarri of awake rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 (2004) R1164-R1171
13. Dias A.C.R., Colombari E., and Mifflin S.W. Effect of nitric oxide on excitatory amino acid-evoked discharge in NTS. Am. J. Physiol. Heart Circ. Physiol. 284 (2003) H234-H240
14. Dias A.C., Vitela M., Colombari E., and Mifflin S.W. Nitric oxide modulation of glutamatergic, baroreflex, and cardiopulmonary transmission in the nucleus of the solitary tract. Am. J. Physiol. Heart Circ. Physiol. 288 (2005) H256-H262
15. Donoghue S., Felder R., Jordan D., and Spyer K.M. The central projection of carotid baroreceptor and chemoreceptor in the cat: a neurophysiological study. J. Physiol. 340 (1984) 397-410
16. Ergene E., Dunbar J.C., O'Leary D.S., and Barraco R.A. Activation of P2-purinoceptors in the nucleus tractus solitarius mediates depressor responses. Neurosci. Lett. 174 (1994) 188-192
17. Florenzano F., Viscomi M.T., Amadio S., D'Ambrosi N., Volonté C., and Molinari M. Do ATP and NO interact in the CNS?. Prog. Neurobiol. 84 (2008) 40-56
18. Franchini K.G., and Krieger E.M. Carotid chemoreceptors influence arterial pressure in intact and aortic denervated rat. Am. J. Physiol. Regul. Integr. Comp. Physiol. 262 (1992) R677-R683
19. Franchini K.G., and Krieger E.M. Cardiovascular responses of conscious rats to carotid body chemoreceptor stimulation by intravenous KCN. J. Auton. Nerv. Syst. 42 (1993) 63-70
20. 2 breathing is modulated by nNOS activity in the conscious rat. J. Appl. Physiol. 85 (1998) 129-132
21. 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
22. Gozal D., Gozal E., and Simakajornboon N. Signaling pathways of the acute hypoxic ventilatory response in the nucleus tractus solitarius. Respir. Physiol. 121 (2000) 209-221
23. Haibara A.S., Colombari E., Chianca-Jr D.A., Bonagamba L.G.H., and Machado B.H. NMDA receptors in NTS are involved in bradycardic but not in pressor response of chemoreflex. Am. J. Physiol. Regul. Integr. Comp. Physiol. 269 (1995) H1421-H1427
24. Haibara A.S., Bonagamba L.H.G., and Machado B.H. Sympathoexcitatory neurotransmission of the chemoreflex in the NTS of awake rats. Am. J. Physiol. 276 (1999) R69-R80
25. Haxhiu M.A., Cha 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
26. Hines T.R.N., and Mifflin S.W. Nitric oxide mediation of cardiac receptor reflex responses in the pregnant rat. Am. J. Obstet. Gynecol. 177 (1997) 1502-1508
27. Kittner H., Franke H., Fischer W., Schultheis N., Krügel U., and Illes P. Stimulation of P2Y1 receptors causes anxiolytic-like effects in the rat elevated plus-maze: implications for the involvement of P2Y1 receptor-mediated nitric oxide production. Neuropsychopharmacology 28 (2003) 435-444
28. 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 (1998) 273-287
29. Lewis S.J., Machado B.H., Ohta H., and Talman W.T. Processing of cardiopulmonary afferent input within the nucleus tractus solitarii involves activation of soluble guanylate cyclase. Eur. J. Pharmacol. 203 (1991) 327-328
30. Lin L.H., Cassell M.D., Sandra A., and Talman W.T. Direct evidence for nitric oxide synthase in vagal afferents to the nucleus tractus solitarii. Neuroscience 84 (1998) 549-558
31. Lin H.C., Wan F.J., and Tseng C.J. Modulation of cardiovascular effects produced by nitric oxide and ionotropic glutamate receptor interaction in the nucleus tractus solitarii of rats. Neuropharmacology 38 (1999) 935-941
32. Lin H.C., Kang B.H., Wan F.J., Huang S.T., and Tseng C.J. Reciprocal regulation of nitric oxide and glutamate in the nucleus tractus solitarii of rats. Eur. J. Pharmacol. 407 (2000) 83-89
33. Lin L.H., Taktakishvili O., and Talman W.T. Identification and localization of cell types that express endothelial and neuronal nitric oxide synthase in the rat nucleus tractus solitarii. Brain Res. 1171 (2007) 42-51
34. Machado B.H., and Bonagamba L.G. Microinjection of S-nitrosocysteine into the nucleus tractus solitarii of conscious rats decreases arterial pressure but l-glutamate does not. Eur. J. Pharmacol. 221 (1992) 179-182
35. Machado B.H., and Bonagamba L.G.H. Microinjection of l-glutamate into the nucleus tractus solitarii increases arterial pressure in conscious rats. Brain Res. 576 (1992) 131-138
36. Matsumura K., Tsuchihashi T., Kagiyama S., Abe I., and Fujishima M. Role of nitric oxide in the nucleus of the solitary tract of rats. Brain Res. 798 (1998) 232-238
37. Matsuo I., Hirooka Y., Hironaga K., Eshima K., Shigematsu H., Shihara M., Sakai K., and Takeshita A. Glutamate release via NO production evoked by NMDA in the NTS enhances hypotension and bradycardia in vivo. Am. J. Physiol. Regul. Integr. Comp. Physiol. 280 (2001) R1285-R1291
38. Michelini L.C., and Bonagamba L.G.H. Baroreceptor reflex modulation by vasopressin microinjected into the nucleus tractus solitarii of conscious rats. Hypertension 11 (1988) 75-79
39. Mifflin S.W. Arterial chemoreceptor input to nucleus tractus solitarius. Am. J. Physiol. Regul. Integr. Comp. Physiol. 263 (1992) R368-R375
40. Mizusawa A., Ogawa H., Kikuchi Y., Hida W., Kurosawa O., 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
41. 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 (1995) 495-504
42. Ohta A., Takagi T., Matsui T., Hamai Y., Lida S., and Esumi H. Localization of nitric oxide synthase-immunoreactive neurons in the solitary nucleus and ventrolateral medulla oblongata of the rat: their relation to catecholaminergic neurons. Neuroc. Lett. 158 (1993) 33-35
43. Patel G.M., Horstman D.J., Adams J.M., and Rich G.F. Nitric oxide synthase inhibitors alter ventilation in isoflurane anesthetized rats. Anesthesiology 88 (1998) 1240-1248
44. Paton J.F.R., Deuchars J., Ahmad Z., Wong L.F., Murphy D., and 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
45. Paton J.F.R., Deuchars J., Li Y.-W., and Kasparov S. Properties of solitary tract neurones responding to peripheral arterial chemoreceptor. Neuroscience 105 (2001) 231-248
46. Paton J.F.R., Lonergan T., Deuchars J., James P.E., and Kasparov S. Detection of angiotensin II mediated nitric oxide release within the nucleus of the solitary tract using electron-paramagnetic resonance (EPR) spectroscopy. Auton. Neurosci: Basic Clin. 126/127 (2006) 193-201
47. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (2007), Academic Press, New York
48. Phillis J.W., Scislo T.J., and O'Leary D.S. Purines and the nucleus tractus solitarius: effects on cardiovascular and respiratory function. Clin. Exp. Pharmacol. Physiol. 24 (1997) 738-742
49. Rengasamy A., and Johns R.A. Characterization of endothelium-derived relaxing factor/nitric oxide synthase from bovine cerebellum and mechanism of modulation by high and low oxygen tensions. J. Pharmacol. Exp. Ther. 259 (1991) 310-316
50. Rengasamy A., and Johns R.A. Determination of Km for oxygen of nitric oxide synthase isoforms. J. Pharmacol. Exp. Ther. 276 (1996) 30-33
51. Sakai K., Hirooka Y., Matsuo I., Eshima K., Shigematsu H., Shimokawa H., and Takeshita A. Overexpression of eNOS in NTS causes hypotension and bradycardia in vivo. Hypertension 36 (2000) 1023-1028
52. Sapru H.N., and Krieger A.J. Carotid and aortic chemoreceptor function in the rat. Am. J. Physiol. 42 (1977) 344-348
53. Scislo T.J., and O'Leary D.S. Differential control of renal vs adrenal sympathetic nerve activity by NTS and A2A and P2X purinoceptors. Am. J. Physiol. 275 (1998) H2130-H2139
54. Scislo T.J., Augustyniak R.A., Barraco R.A., Woodbury D.J., and O'Leary D.S. Activation of P2X-purinoceptors in the nucleus tractus solitarius elicits differential inhibition of lumbar and renal sympathetic nerve activity. J. Auton. Nerv. Syst. 62 (1997) 103-110
55. Scislo T.J., Ergene E., and O'Leary D.S. Impaired arterial baroreflex regulation of heart rate after blockade of P2-purinoceptors in nucleus tractus solitarius. Brain Res. Bull. 47 (1998) 63-67
56. Tseng C.J., Liu H.Y., Lin H.C., Ger L.P., Tung C.S., and Yen M.H. Cardiovascular effects of nitric oxide in the brain stem nuclei of rats. Hypertension 27 (1996) 36-42
57. Vitagliano S., Berrino L., D'Amico M., Maione S.N., and Rossi F. Involvement of nitric oxide in cardiorespiratory regulation in the nucleus tractus solitarii. Neuropharmacology 35 (1996) 625-631
58. Waki H., Murphy D., Yao S.T., Kasparov S., and Paton J.F. Endothelial NO synthase activity in nucleus tractus solitarii contributes to hypertension in spontaneously hypertensive rats. Hypertension 48 (2006) 644-650