Ondansetron and fluoxetine reduce sleep apnea in mice lacking monoamine oxidase A

Respiratory Physiology and Neurobiology

Volumn 168, Issue 3, 2009, Pages 230-238

  Real, C ^a   Seif, I ^a   Adrien, J ^b,c   Escourrou, P ^a  

^a University of Paris XI   (France)

^b SORBONNE UNIVERSITÉ   (France)

^c PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Apnea; Breathing; Fluoxetine; MAOA; Mice; Ondansetron; Serotonin; Sleep

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; FLUOXETINE; NORADRENALIN; ONDANSETRON; SEROTONIN; SEROTONIN UPTAKE INHIBITOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREATHING PATTERN; CENTRAL SLEEP APNEA SYNDROME; CONTROLLED STUDY; DRUG DOSE COMPARISON; DRUG MECHANISM; MALE; MOUSE; NONHUMAN; NONREM SLEEP; POST SIGH APNEA; PRIORITY JOURNAL; REM SLEEP; SLEEP APNEA SYNDROME; TRANSGENIC MOUSE;

ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FLUOXETINE; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; MONOAMINE OXIDASE; ONDANSETRON; PLETHYSMOGRAPHY, WHOLE BODY; RESPIRATORY MECHANICS; SEROTONIN ANTAGONISTS; SEROTONIN UPTAKE INHIBITORS; SLEEP APNEA SYNDROMES; WAKEFULNESS;

EID: 69249209606     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2009.07.003     Document Type: Article

References (68)

1. Badr M.S., Grossman J.E., and Weber S.A. Treatment of refractory sleep apnea with supplemental carbon dioxide. Am. J. Respir. Crit. Care Med. 150 (1994) 561-564
2. Berry R.B., Yamaura E.M., Gill K., and Reist C. Acute effects of paroxetine on genioglossus activity in obstructive sleep apnea. Sleep 22 (1999) 1087-1092
3. Boutrel B., Evrard A., Seif I., De Maeyer E., Hamon M., and Adrien J. Circadian rhythms of sleep-wakefulness, motor activity and body temperature in mutant mice lacking monoamine oxidase A. J. Sleep Res. 9 (2000) 24
4. Burnet H., Bévengut M., Chakri F., Bou-Flores C., Coulon P., Gaytán S., Pásaro R., and Hilaire G. Altered respiratory activity and respiratory regulations in adult monoamine oxidase A-deficient mice. J. Neurosci. 21 (2001) 5212-5221
5. Cadogan A.K., Marsden C.A., Tulloch I., and Kendall D.A. Evidence that chronic administration of paroxetine or fluoxetine enhances 5-HT2 receptor function in the brain of the guinea pig. Neuropharmacology 32 (1993) 249-256
6. Carley D.W., and Radulovacki M. Role of peripheral serotonin in the regulation of central sleep apneas in rats. Chest 115 (1999) 1397-1401
7. 4 agonist, reduces sleep apneas in rats. Pharmacol. Biochem. Behav. 69 (2001) 283-289
8. Carley D.W., and Radulovacki M. Apnea suppression by ondansetron and fluoxetine alone and combined. Sleep 28 Abstract Supplement (2005) 12
9. Carley D.W., Olopade C., Ruigt G.S., and Radulovacki M. Efficacy of mirtazapine in obstructive sleep apnea syndrome. Sleep 30 (2007) 35-41
10. Carley D.W., and Radulovacki M. Pharmacology of vagal afferent influences on disordered breathing during sleep. Respir. Physiol. Neurobiol. 164 (2008) 197-203
11. Cases O., Seif I., Grimsby J., Gaspar P., Chen K., Pournin S., Müller U., Aguet M., Babinet C., Shih J.C., and De Maeyer E. Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 268 (1995) 1763-1766
12. Cases O., Lebrand C., Giros B., Vitalis T., De Maeyer E., Caron M.G., Price D.J., Gaspar P., and Seif I. Plasma membrane transporters of serotonin, dopamine, and norepinephrine mediate serotonin accumulation in atypical locations in the developing brain of monoamine oxidase A knock-outs. J. Neurosci. 18 (1998) 6914-6927
13. Chen K., Holschneider D.P., Wu W., Rebrin I., and Shih J.C. A spontaneous point mutation produces monoamine oxidase A/B knock-out mice with greatly elevated monoamines and anxiety-like behavior. J. Biol. Chem. 279 (2004) 39645-39652
14. Dempsey J.A., Smith C.A., Harms C.A., Chow C., and Saupe K.W. Sleep-induced breathing instability. Sleep 19 (1996) 236-247
15. Dempsey J.A. Crossing the apnoeic threshold: causes and consequences. Exp. Physiol. 90 (2005) 13-24
16. Eisensamer B., Rammes G., Gimpl G., Shapa M., Ferrari U., Hapfelmeier G., Bondy B., Parsons C., Gilling K., Zieglgänsberger W., Holsboer F., and Rupprecht R. Antidepressants are functional antagonists at the serotonin type 3 (5-HT3) receptor. Mol. Psychiatry 8 (2003) 994-1007
17. Eisensamer B., Uhr M., Meyr S., Gimpl G., Deiml T., Rammes G., Lambert J.J., Zieglgänsberger W., Holsboer F., and Rupprecht R. Antidepressants and antipsychotic drugs colocalize with 5-HT3 receptors in raft-like domains. J. Neurosci. 25 (2005) 10198-10206
18. El Yacoubi M., Bouali S., Popa D., Naudon L., Leroux-Nicollet I., Hamon M., Costentin J., Adrien J., and Vaugeois J.M. Behavioral, neurochemical, and electrophysiological characterization of a genetic mouse model of depression. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 6227-6232
19. Evrard A., Malagié I., Laporte A.M., Boni C., Hanoun N., Trillat A.C., Seif I., De Maeyer E., Gardier A., Hamon M., and Adrien J. Altered regulation of the 5-HT system in the brain of MAO-A knock-out mice. Eur. J. Neurosci. 15 (2002) 841-851
20. Fenik P., and Veasey S.C. Pharmacological characterization of serotonergic receptor activity in the hypoglossal nucleus. Am. J. Respir. Crit. Care Med. 167 (2003) 563-569
21. Franco P., Verheulpen D., Valente F., Kelmanson I., de Broca A., Scaillet S., Groswasser J., and Kahn A. Autonomic responses to sighs in healthy infants and in victims of sudden infant death. Sleep Med. 4 (2003) 569-577
22. Freedman S.B., Adler M., Seshadri R., and Powell E.C. Oral ondansetron for gastroenteritis in a pediatric emergency department. N. Engl. J. Med. 354 (2006) 1698-1705
23. Hanzel D.A., Proia N.G., and Hudgel D.W. Response of obstructive sleep apnea to fluoxetine and protriptyline. Chest 100 (1991) 416-421
24. Hendrickse W.A., Roffwarg H.P., Grannemann B.D., Orsulak P.J., Armitage R., Cain J.W., Battaglia J., Debus J.R., and Rush A.J. The effects of fluoxetine on the polysomnogram of depressed outpatients: a pilot study. Neuropsychopharmacology 10 (1994) 85-91
25. Hodges M.R., and Richerson G.B. Contributions of 5-HT neurons to respiratory control: neuromodulatory and trophic effects. Respir. Physiol. Neurobiol. 164 (2008) 222-232
26. Jacobs B.L., and Fornal C.A. Activity of serotonergic neurons in behaving animals. Neuropsychopharmacology 21 (1999) 9S-15S
27. Jacky J.P. A plethysmograph for long-term measurements of ventilation in unrestrained animals. J. Appl. Physiol. 45 (1978) 644-647
28. Kahn A., Blum D., Rebuffat E., Sottiaux M., Levitt J., Bochner A., Alexander M., Grosswasser J., and Muller M.F. Polysomnographic studies of infants who subsequently died of sudden infant death syndrome. Pediatrics 82 (1988) 721-727
29. Kobayashi T., Washiyama K., and Ikeda K. Inhibition of G protein-activated inwardly rectifying K+ channels by fluoxetine (Prozac). Br. J. Pharmacol. 138 (2003) 1119-1128
30. Kraiczi H., Hedner J., Dalhöf P., Ejnell H., and Carlson J. Effect of serotonin uptake inhibition on breathing during sleep and daytime symptoms in obstructive sleep apnea. Sleep 22 (1999) 61-67
31. Lajard A.M., Bou C., Monteau R., and Hilaire G. Serotonin levels are abnormally elevated in the fetus of the monoamine oxidase-A-deficient transgenic mouse. Neurosci. Lett. 261 (1999) 41-44
32. Léna C., Popa D., Grailhe R., Escourrou P., Changeux J.P., and Adrien J. Beta2-containing nicotinic receptors contribute to the organization of sleep and regulate putative micro-arousals in mice. J. Neurosci. 24 (2004) 5711-5718
33. Li Q., Muma N.A., Battaglia G., and Van de Kar L.D. Fluoxetine gradually increases [125I]DOI-labelled 5-HT2A/2C receptors in the hypothalamus without changing the levels of Gq- and G11-proteins. Brain Res. 775 (1997) 225-228
34. Linder A.E., Ni W., Szasz T., Burnett R., Diaz J., Geddes T.J., Kuhn D.M., and Watts S.W. A serotonergic system in veins: serotonin transporter-independent uptake. J. Pharmacol. Exp. Ther. 325 (2008) 714-722
35. Maudhuit C., Jolas T., Lainey E., Hamon M., and Adrien J. Effects of acute and chronic treatment with amoxapine and cericlamine on the sleep-wakefulness cycle in the rat. Neuropharmacology 33 (1994) 1017-1025
36. Monaca C., Boutrel B., Hen R., Hamon M., and Adrien J. 5-HT1A/1B receptor-mediated effects of the selective serotonin reuptake inhibitor, citalopram, on sleep: studies in 5-HT1A and 5-HT1B knockout mice. Neuropsychopharmacology 28 (2003) 850-856
37. Moreira T.S., Takakura A.C., Colombari E., West G.H., and Guyenet P.G. Inhibitory input from slowly adapting lung stretch receptors to retrotrapezoid nucleus chemoreceptors. J. Physiol. 580 (2007) 285-300
38. Moreira T.S., Takakura A.C., Colombari E., and Guyenet P.G. Activation of 5-hydroxytryptamine type 3 receptor-expressing C-fiber vagal afferents inhibits retrotrapezoid nucleus chemoreceptors in rats. J. Neurophysiol. 98 (2007) 3627-3637
39. Mössner R., Simantov R., Marx A., Lesch K.P., and Seif I. Aberrant accumulation of serotonin in dopaminergic neurons. Neurosci. Lett. 401 (2006) 49-54
40. Nakamura A., Fukuda Y., and Kuwaki T. Sleep apnea and effect of chemostimulation of breathing instability in mice. J. Appl. Physiol. 94 (2003) 525-532
41. Nakamura A., Zhang W., Yanagisawa M., Fukuda Y., and Kuwaki T. Vigilance state-dependent attenuation of hypercapnic chemoreflex and exaggerated sleep apnea in orexin knockout mice. J. Appl. Physiol. 102 (2007) 241-248
42. Ni Y.G., and Miledi R. Blockage of 5HT2C serotonin receptors by fluoxetine (Prozac). Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 2036-2040
43. Owesson C.A., Hopwood S.E., Callado L.F., Seif I., McLaughlin D.P., and Stamford J.A. Altered presynaptic function in monoaminergic neurons of monoamine oxidase-A knockout mice. Eur. J. Neurosci. 15 (2002) 1516-1522
44. Pace-Schott E.F., and Hobson J.A. The neurobiology of sleep: genetics, cellular physiology and subcortical networks. Nat. Rev. Neurosci. 3 (2002) 591-605
45. Popa D., Léna C., Fabre V., Prenat C., Gingrich J., Escourrou P., Hamon M., and Adrien J. Contribution of 5-HT2 receptor subtypes to sleep-wakefulness and respiratory control and functional adaptations in knock-out mice lacking 5-HT2A receptors. J. Neurosci. 25 (2005) 11231-11238
46. Portas C.M., Bjorvatn B., Fagerland S., Gronli J., Mundal V., Sorensen E., and Ursin R. On-line detection of extracellular levels of serotonin in dorsal raphe nucleus and frontal cortex over the sleep/wake cycle in the freely moving rat. Neuroscience 83 (1998) 807-814
47. Radulovacki M., Trbovic S.M., and Carley D.W. Serotonin 5-HT3-receptor antagonist GR 38032F suppresses sleep apneas in rats. Sleep 21 (1998) 131-136 Erratum for Figure 3
48. Real C., Popa D., Seif I., Callebert J., Launay J.M., Adrien J., and Escourrou P. Sleep apneas are increased in mice lacking monoamine oxidase A. Sleep 30 (2007) 1295-1302
49. Sánchez C., and Hyttel J. Comparison of the effects of antidepressants and their metabolites on reuptake of biogenic amines and on receptor binding. Cell. Mol. Neurobiol. 19 (1999) 467-489
50. Saponjic J., Radulovacki M., and Carley D.W. Monoaminergic system lesions increase post-sigh respiratory pattern disturbance during sleep in rats. Physiol. Behav. 90 (2007) 1-10
51. Scott J.A., Wood M., and Flood P. The pronociceptive effect of ondansetron in the setting of P-glycoprotein inhibition. Anesth. Analg. 103 (2006) 742-746
52. Simpson K.H., Murphy P., Colthup P.V., and Whelan P. Concentration of ondansetron in cerebrospinal fluid following oral dosing in volunteers. Psychopharmacology (Berl.) 109 (1992) 497-498
53. Smith C.A., Nakayama H., and Dempsey J.A. The essential role of carotid body chemoreceptors in sleep apnea. Can. J. Physiol. Pharmacol. 81 (2003) 774-779
54. Smith I., Lasserson T.J., and Wright J. Drug therapy for obstructive sleep apnoea in adults. Cochrane Database Syst. Rev. 19 (2006) CD003002
55. Smith C.A., Chenuel B.J., Henderson K.S., and Dempsey J.A. The apneic threshold during non-REM sleep in dogs: sensitivity of carotid body vs. central chemoreceptors. J. Appl. Physiol. 103 (2007) 578-586
56. Stradling J., Smith D., Radulovacki M., and Carley D.W. Effect of ondansetron on moderate obstructive sleep apnoea, a single night, placebo-controlled trial. J. Sleep Res. 12 (2003) 169-170
57. Takakura A.C., Moreira T.S., Colombari E., West G.H., Stornetta R.L., and Guyenet P.G. Peripheral chemoreceptor inputs to retrotrapezoid nucleus (RTN) CO2-sensitive neurons in rats. J. Physiol. 572 (2006) 503-523
58. Tissier M.H., Lainey E., Fattaccini C.M., Hamon M., and Adrien J. Effects of ipsapirone, a 5-HT1A agonist, on sleep/wakefulness cycles: probable post-synaptic action. J. Sleep Res. 2 (1993) 103-109
59. Tuinier S., Verhoeven V.M.A., Scherders M.J.W.T., Fekkes D., and Pepplinkhuizen L. Neuropsychiatric and biochemical characteristics of X-linked MAO-A deficiency syndrome. A single case intervention study. New Trends Exp. Clin. Psychiatry 11 (1995) 99-107
60. Ursin R. Serotonin and sleep. Sleep Med. Rev. 6 (2002) 55-67
61. Veasey S.C., Fenik P., Panckeri K., Pack A.I., and Hendricks J.C. The effects of trazodone with l-tryptophan on sleep-disordered breathing in the English bulldog. Am. J. Respir. Crit. Care Med. 160 (1999) 1659-1667
62. Veasey S.C., Chachkes J., Fenik P., and Hendricks J.C. The effects of ondansetron on sleep-disordered breathing in the English bulldog. Sleep 24 (2001) 155-160
63. Veasey S.C. Serotonin agonists and antagonists in obstructive sleep apnea: therapeutic potential. Am. J. Respir. Med. 2 (2003) 21-29
64. Vossler D.G., Wyler A.R., Wilkus R.J., Gardner-Walker G., and Vlcek B.W. Cataplexy and monoamine oxidase deficiency in Norrie Disease. Neurology 46 (1996) 1258-1261
65. Wang D., Post M., and Cutz E. Expression of serotonin receptor 2c in rat type II pneumocytes. Am. J. Respir. Cell Mol. Biol. 20 (1999) 1175-1180
66. White D.P. Pathogenesis of obstructive and central sleep apnea. Am. J. Respir. Crit. Care Med. 172 (2005) 1363-1370
67. Xie A., Rankin F., Rutherford R., and Bradley T.D. Effects of inhaled CO2 and added dead space on idiopathic central sleep apnea. J. Appl. Physiol. 82 (1997) 918-926
68. Zhong H., Zhang M., and Nurse C.A. Electrophysiological characterization of 5-HT receptors on rat petrosal neurons in dissociated cell culture. Brain Res. 816 (1999) 544-553