Neonatal caffeine induces sex-specific developmental plasticity of the hypoxic respiratory chemoreflex in adult rats

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 295, Issue 3, 2008, Pages

  Montandon, Gaspard ^a,b   Bairam, Aida ^b   Kinkead, Richard ^b  

^a UNIVERSITY OF TORONTO   (Canada)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

Caffeine; Control of breathing; Development; Sexual dimorphism

Indexed keywords

4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; CAFFEINE; DOPAMINE 2 RECEPTOR; MESSENGER RNA; TYROSINE 3 MONOOXYGENASE; ALPHA 2 ADRENERGIC RECEPTOR; CENTRAL STIMULANT AGENT; RECEPTOR, ADRENERGIC, ALPHA 2A; RECEPTOR, ADRENERGIC, ALPHA-2A; TRIAZINE DERIVATIVE; TRIAZOLE DERIVATIVE;

ADULT ANIMAL; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY PLETHYSMOGRAPHY; BREATHING; CAROTID BODY; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HYPOXIA; LUNG VENTILATION; MALE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASTICITY; PRIORITY JOURNAL; RAT; RESPIRATION CONTROL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SEXUAL DEVELOPMENT; ANESTHESIA; ANIMAL; ANOXIA; COMPARATIVE STUDY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; NERVE CELL INHIBITION; PATHOPHYSIOLOGY; PHRENIC NERVE; PHYSIOLOGY; REFLEX; SPRAGUE DAWLEY RAT;

ANESTHESIA; ANIMALS; ANIMALS, NEWBORN; ANOXIA; CAFFEINE; CAROTID BODY; CENTRAL NERVOUS SYSTEM STIMULANTS; FEMALE; GENE EXPRESSION; MALE; NEURAL INHIBITION; PHRENIC NERVE; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, DOPAMINE D2; REFLEX; RESPIRATION; RNA, MESSENGER; SEX CHARACTERISTICS; TRIAZINES; TRIAZOLES; TYROSINE 3-MONOOXYGENASE;

EID: 54049154290     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00059.2008     Document Type: Article

References (67)

1. Bairam A, Boutroy MJ, Badonnel Y, Vert P. Theophylline versus caffeine: comparative effects in treatment of idiopathic apnea in the preterm infant. J Pediatr 110: 636-639, 1987.
2. Bairam A, Carroll JL. Neurotransmitters in carotid body development. Respir Physiol Neurobiol 149: 217-232, 2005.
3. Bairam A, De GP, Dauphin C, Marchal F. Effects of caffeine on carotid sinus nerve chemosensory discharge in kittens and cats. J Appl Physiol 82: 413-418, 1997.
4. Bairam A, Joseph V, Lajeunesse Y, Kinkead R. Developmental pattern of M1 and M2 muscarinic gene expression and receptor levels in cat carotid body, petrosal and superior cervical ganglion. Neuroscience 139: 711-721, 2006.
5. Bairam A, Kinkead R, Joseph V. Neonatal environment and neuroendocrine programming of the peripheral respiratory control system. Curr Pediatr Rev 2: 199-208, 2006.
6. Barraco RA, el-Ridi MR, Ergene E, Phillis JW. Adenosine receptor subtypes in the brainstem mediate distinct cardiovascular response patterns. Brain Res Bull 26: 59-84, 1991.
7. Bhatt-Mehta V, Schumacher RE. Treatment of apnea of prematurity. Paediatr Drugs 5: 195-210, 2003.
8. Boulenger JP, Patel J, Post RM, Parma AM, Marangos PJ. Chronic caffeine consumption increases the number of brain adenosine receptors. Life Sci 32: 1135-1142, 1983.
9. Carrettiero DC, Fior-Chadi DR. Adenosine A1 receptor distribution in the nucleus tractus solitarii of normotensive and spontaneously hypertensive rats. J Neural Transm 111: 465-473, 2004.
10. Clancy B, Darlington RB, Finlay BL. Translating developmental time across mammalian species. Neuroscience 105: 7-17, 2001.
11. Comer AM, Perry CM, Figgitt DP. Caffeine citrate: a review of its use in apnoea of prematurity. Paediatr Drugs 3: 61-79, 2001.
12. Conde SV, Monteiro EC. Hypoxia induces adenosine release from the rat carotid body. J Neurochem 89: 1148-1156, 2004.
13. Conde SV, Obeso A, Vicario I, Rigual R, Rocher A, Gonzalez C. Caffeine inhibition of rat carotid body chemoreceptors is mediated by A2A and A2B adenosine receptors. J Neurochem 98: 616-628, 2006.
14. 2 modulates phrenic responses to specific carotid body hypoxia in an in situ dual perfused rat preparation. J Physiol 578: 843-857, 2007.
15. Drorbaugh JE, Fenn WO. A barometric method for measuring ventilation in newborn infants. Pediatrics 16: 81-87, 1955.
16. Enhorning G, van SS, Lundgren C, Vargas I. Whole-body plethysmography, does it measure tidal volume of small animals? Can J Physiol Pharmacol 76: 945-951, 1998.
17. Etzel BA, Guillet R. Effects of neonatal exposure to caffeine on adenosine A1 receptor ontogeny using autoradiography. Brain Res Dev Brain Res 82: 223-230, 1994.
18. Fastbom J, Fredholm BB. Effects of long-term theophylline treatment on adenosine A1-receptors in rat brain: autoradiographic evidence for increased receptor number and altered coupling to G-proteins. Brain Res 507: 195-199, 1990.
19. Finer NN, Higgins R, Kattwinkel J, Martin RJ. Summary proceedings from the apnea-of-prematurity group. Pediatrics 117: S47-S51, 2006.
20. Finlay BL, Darlington RB. Linked regularities in the development and evolution of mammalian brains. Science 268: 1578-1584, 1995.
21. Finley JC, Katz DM. The central organization of carotid body afferent projections to the brainstem of the rat. Brain Res 572: 108-116, 1992.
22. Fuxe K, Ferre S, Genedani S, Franco R, Agnati LF. Adenosine receptor-dopamine receptor interactions in the basal ganglia and their relevance for brain function. Physiol Behav 92: 210-217, 2007.
23. Gaytan SP, Saadani-Makki F, Bodineau L, Frugiere A, Larnicol N, Pasaro R. Effect of postnatal exposure to caffeine on the pattern of adenosine A(1) receptor distribution in respiration-related nuclei of the rat brainstem. Auton Neurosci 126-127: 339-346, 2006.
24. Genest SE, Gulemetova R, Laforest S, Drolet G, Kinkead R. Neonatal maternal separation and sex-specific plasticity of the hypoxic ventilatory response in awake rat. J Physiol 554: 543-557, 2004.
25. Gonzalez C, Almaraz L, Obeso A, Rigual R. Carotid body chemoreceptors: from natural stimuli to sensory discharges. Physiol Rev 74: 829-898, 1994.
26. Gourine AV, Llaudet E, Thomas T, Dale N, Spyer KM. Adenosine release in nucleus tractus solitarii does not appear to mediate hypoxia-induced respiratory depression in rats. J Physiol 544: 161-170, 2002.
27. Guillet R, Kellogg C. Neonatal exposure to therapeutic caffeine alters the ontogeny of adenosine A1 receptors in brain of rats. Neuropharmacology 30: 489-496, 1991.
28. Housley GD, Martin-Body RL, Dawson NJ, Sinclair JD. Brain stem projections of the glossopharyngeal nerve and its carotid sinus branch in the rat. Neuroscience 22: 237-250, 1987.
29. Iturriaga R, Alcayaga J. Neurotransmission in the carotid body: transmitters and modulators between glomus cells and petrosal ganglion nerve terminals. Brain Res Rev 47: 46-53, 2004.
30. Javaheri S. A mechanism of central sleep apnea in patients with heart failure. N Engl J Med 341: 949-954, 1999.
31. Johansson B, Georgiev V, Lindstrom K, Fredholm BB. A1 and A2A adenosine receptors and A1 mRNA in mouse brain: effect of long-term caffeine treatment. Brain Res 762: 153-164, 1997.
32. Kara T, Narkiewicz K, Somers VK. Chemoreflexes: physiology and clinical implications. Acta Physiol Scand 177: 377-384, 2003.
33. Kinkead R, Dupenloup L, Valois N, Gulemetova R. Stress-induced attenuation of the hypercapnic ventilatory response in awake rats. J Appl Physiol 90: 1729-1735, 2001.
34. Kinkead R, Gulemetova R, Bairam A. Neonatal maternal separation enhances phrenic responses to hypoxia and carotid sinus nerve stimulation in the adult anesthetised rat. J Appl Physiol 99: 189-196, 2005.
35. Kinkead R, Joseph V, Lajeunesse Y, Bairam A. Neonatal maternal separation enhances dopamine D(2)-receptor and tyrosine hydroxylase mRNA expression levels in carotid body of rats. Can J Physiol Pharmacol 83: 76-84, 2005.
36. Kobayashi S, Conforti L, Millhorn DE. Gene expression and function of adenosine A(2A) receptor in the rat carotid body. Am J Physiol Lung Cell Mol Physiol 279: L273-L282, 2000.
37. Koos BJ, Kawasaki Y, Kim YH, Bohorquez F. Adenosine A2A-receptor blockade abolishes the roll-off respiratory response to hypoxia in awake lambs. Am J Physiol Regul Integr Comp Physiol 288: R1185-R1194, 2005.
38. Lundblad LK, Irvin CG, Adler A, Bates JH. A reevaluation of the validity of unrestrained plethysmography in mice. J Appl Physiol 93: 1198-1207, 2002.
39. Lupica CR, Berman RF, Jarvis MF. Chronic theophylline treatment increases adenosine A1, but not A2, receptor binding in the rat brain: an autoradiographic study. Synapse 9: 95-102, 1991.
40. Marangos PJ, Boulenger JP, Patel J. Effects of chronic caffeine on brain adenosine receptors: regional and ontogenetic studies. Life Sci 34: 899-907, 1984.
41. Marchal F, Bairam A, Vert P. Neonatal apnea and apneic syndromes. Clin Perinatol 14: 509-529, 1987.
42. Martin RJ, Abu-Shaweesh JM, Baird TM. Apnoea of prematurity. Paediatr Respir Rev 5, Suppl A: S377-S382, 2004.
43. Maxwell DL, Fuller RW, Nolop KB, Dixon CM, Hughes JM. Effects of adenosine on ventilatory responses to hypoxia and hypercapnia in humans. J Appl Physiol 61: 1762-1766, 1986.
44. McQueen DS, Ribeiro JA. Pharmacological characterization of the receptor involved in chemoexcitation induced by adenosine. Br J Pharmacol 88: 615-620, 1986.
45. Montandon G, Bairam A, Kinkead R. Long-term consequences of neonatal caffeine on ventilation, occurrence of apneas, and hypercapnic chemoreflex in male and female rats. Pediatr Res 59: 519-524, 2006.
46. Montandon G, Kinkead R, Bairam A. Disruption of adenosinergic modulation of ventilation at rest and during hypercapnia by neonatal caffeine in young rats: role of adenosine A1 and A2A receptors. Am J Physiol Regul Integr Comp Physiol 292: R1621-R1631, 2007.
47. Montandon G, Kinkead R, Lajeunesse Y, Bairam A. Neonatal caffeine augments the acute breathing frequency response to hypoxia and the adenosine and the dopamine receptor mRNA expression in the carotid body of adult rats. FASEB J A1215: 752.3, 2006.
48. Monteiro EC, Ribeiro JA. Ventilatory effects of adenosine mediated by carotid body chemoreceptors in the rat. Naunyn Schmiedebergs Arch Pharmacol 335: 143-148, 1987.
49. Mortola JP, Dotta A. Effects of hypoxia and ambient temperature on gaseous metabolism of newborn rats. Am J Physiol Regul Integr Comp Physiol 263: R267-R272, 1992.
50. Mortola JP, Frappell PB. On the barometric method for measurements of ventilation, and its use in small animals. Can J Physiol Pharmacol 76: 937-944, 1998.
51. Murray TF. Up-regulation of rat cortical adenosine receptors following chronic administration of theophylline. Eur J Pharmacol 82: 113-114, 1982.
52. Powell FL, Milsom WK, Mitchell GS. Time domains of the hypoxic ventilatory response. Respir Physiol 112: 123-134, 1998.
53. Prabhakar NR. O2 sensing at the mammalian carotid body: why multiple O2 sensors and multiple transmitters? Exp Physiol 91: 17-23, 2006.
54. Rosin DL, Robeva A, Woodard RL, Guyenet PG, Linden J. Immunohistochemical localization of adenosine A2A receptors in the rat central nervous system. J Comp Neurol 401: 163-186, 1998.
55. Runold M, Cherniack NS, Prabhakar NR. Effect of adenosine on isolated and superfused cat carotid body activity. Neurosci Lett 113: 111-114, 1990.
56. Schindler CW, Karcz-Kubicha M, Thorndike EB, Muller CE, Tella SR, Ferre S, Goldberg SR. Role of central and peripheral adenosine receptors in the cardiovascular responses to intraperitoneal injections of adenosine A1 and A2A subtype receptor agonists. Br J Pharmacol 144: 642-650, 2005.
57. Scislo TJ, Kitchen AM, Augustyniak RA, O'Leary DS. Differential patterns of sympathetic responses to selective stimulation of nucleus tractus solitarius purinergic receptor subtypes. Clin Exp Pharmacol Physiol 28: 120-124, 2001.
58. Scislo TJ, O'Leary DS. Purinergic mechanisms of the nucleus of the solitary tract and neural cardiovascular control. Neurol Res 27: 182-194, 2005.
59. Sebastiao AM, Ribeiro JA. Adenosine A2 receptor-mediated excitatory actions on the nervous system. Prog Neurobiol 48: 167-189, 1996.
60. Stephenson R, Liao KS, Hamrahi H, Horner RL. Circadian rhythms and sleep have additive effects on respiration in the rat. J Physiol 536: 225-235, 2001.
61. Szewczak JM, Powell FL. Open-flow plethysmography with pressure-decay compensation. Respir Physiol Neurobiol 134: 57-67, 2003.
62. Thomas T, St Lambert JH, Dashwood MR, Spyer KM. Localization and action of adenosine A2a receptors in regions of the brainstem important in cardiovascular control. Neuroscience 95: 513-518, 2000.
63. Vik T, Bakketeig LS, Trygg KU, Lund-Larsen K, Jacobsen G. High caffeine consumption in the third trimester of pregnancy: gender-specific effects on fetal growth. Paediatr Perinat Epidemiol 17: 324-331, 2003.
64. Warner G, Skatrud JB, Dempsey JA. Effect of hypoxia-induced periodic breathing on upper airway obstruction during sleep. J Appl Physiol 62: 2201-2211, 1987.
65. White DP. The pathogenesis of obstructive sleep apnea: advances in the past 100 years. Am J Respir Cell Mol Biol 34: 1-6, 2006.
66. Yamamoto M, Nishimura M, Kobayashi S, Akiyama Y, Miyamoto K, Kawakami Y. Role of endogenous adenosine in hypoxic ventilatory response in humans: a study with dipyridamole. J Appl Physiol 76: 196-203, 1994.
67. Yuan JS, Reed A, Chen F, Stewart CN Jr. Statistical analysis of real-time PCR data. BMC Bioinformatics 7: 85, 2006.