Dual effects of 5-HT1a receptor activation on breathing in neonatal mice

Journal of Neuroscience

Volumn 34, Issue 1, 2014, Pages 51-59

  Corcoran, Andrea E ^a,b,c   Commons, Kathryn G ^d   Wu, Yuanming ^g   Smith, Jeffrey C ^e   Harris, Michael B ^a   Richerson, George B ^b,f,g  

^a UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^b YALE UNIVERSITY   (United States)

^c DARTMOUTH MEDICAL SCHOOL   (United States)

^d BOSTON CHILDREN S HOSPITAL   (United States)

^e NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^f VETERANS AFFAIRS MEDICAL CENTER   (United States)

^g UNIVERSITY OF IOWA   (United States)

Author keywords

8 OH DPAT; Lmx1b; Serotonin

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; 3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL) PYRIDAZINIUM BROMIDE; AUTORECEPTOR; BENZYL [3 [[1 (3, 4 DICHLOROPHENYL) ETHYL] AMINO] 2 HYDROXYPROPYL] PHOSPHINIC ACID; SEROTONIN 1A RECEPTOR; STRYCHNINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR LMX1B; TRYPTOPHAN HYDROXYLASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BREATHING; CONTROLLED STUDY; FEMALE; GENOTYPE; HYPOGLOSSAL NERVE; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NEWBORN; NONHUMAN; PLETHYSMOGRAPHY; PRIORITY JOURNAL; RESPIRATORY BURST; SPIKE WAVE; SYNAPTIC INHIBITION; TIDAL VOLUME;

EID: 84891399868     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0864-13.2014     Document Type: Article

References (52)

1. Aghajanian GK, Sanders-Bush E (2002) Serotonin. In: Neuropsychopharmocology: the fifth generation of progress (Davis KL, Charney D, Coyle JT, Nemeroff C, eds), pp 15-34. Philadelphia: Lippincott Williams and Wilkins.
2. Audero E, Coppi E, Mlinar B, Rossetti T, Caprioli A, Banchaabouchi MA, Corradetti R, Gross C (2008) Sporadic autonomic dysregulation and death associated with excessive serotonin autoinhibition. Science 321: 130-133. CrossRef Medline
3. Bard JA, Zgombick J, Adham N, Vaysse P, Branchek TA, Weinshank RL (1993) Cloning of a novel human serotonin receptor (5-HT7) positively linked to adenylate cyclase. J Biol Chem 268:23422-23426. Medline
4. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083-1152. CrossRef Medline
5. Bou-Flores C, Lajard AM, Monteau R, De Maeyer E, Seif I, Lanoir J, Hilaire G (2000) Abnormal phrenic motoneuron activity and morphology in neonatal monoamine oxidase A-deficient transgenic mice: possible role of a serotonin excess. J Neurosci 20:4646-4656. Medline
6. 2. Proc Natl Acad Sci U S A 107:16354-16359. CrossRef Medline
7. Crone SA, Viemari JC, Droho S, Mrejeru A, Ramirez JM, Sharma K (2012) Irregular breathing in mice following ablation of V2a neurons. J Neurosci 32:7895-7906. CrossRef Medline
8. Cummings KJ, Pendlebury JD, Sherwood NM, Wilson RJ (2004) Sudden neonatal death in PACAP-deficient mice is associated with reduced respiratory chemoresponse and susceptibility to apnoea. J Physiol 555:15-26. CrossRef Medline
9. Depuy SD, Kanbar R, Coates MB, Stornetta RL, Guyenet PG (2011) Control of breathing by raphe obscurus serotonergic neurons in mice. J Neurosci 31:1981-1990. CrossRef Medline
10. Ding YQ, Marklund U, Yuan W, Yin J, Wegman L, Ericson J, Deneris E, Johnson RL, Chen ZF (2003) Lmx1b is essential for the development of serotonergic neurons. Nat Neurosci 6:933-938. CrossRef Medline
11. Dutschmann M, Waki H, Manzke T, Simms AE, Pickering AE, Richter DW, Paton JFR (2009) The potency of different serotonergic agonists in counteracting opioid evoked cardiorespiratory disturbances. Philos Trans Lond B Biol Sci 364:2611-2623. CrossRef Medline
12. El-Khatib MF, Kiwan RA, JamaleddineGW (2003) Buspirone treatment for apneustic breathing in brain stem infarct. Respir Care 48:956-958. Medline
13. 1A receptor stimulation on contextual learning in mice. Eur J Pharmacol 596:107-110. CrossRef Medline
14. Faure C, Mnie-Filali O, Scarna H, Debonnel G, HaddjeriN (2006) Effects of the 5-HT7 receptor antagonist SB-269970 on rat hormonal and temperature responses to the 5-HT1A/7 receptor agonist 8-OH-DPAT. Neurosci Lett 404:122-126. CrossRef Medline
15. Guenther U, Manzke T, Wrigge H, Dutschmann M, Zinserling J, Putensen C, Hoeft A (2009) The counteraction of opioid-induced ventilatory depression by the serotonin 1A-agonist 8-OH-DPAT does not antagonize antinociception in rats in situ and in vivo. Anesth Analg 108:1169-1176. CrossRef Medline
16. Hedlund PB, Kelly L, Mazur C, Lovenberg T, Sutcliffe JG, Bonaventure P (2004) 8-OH-DPAT acts on both 5-HT1a and 5-HT7 receptors to induce hypothermia in rodents. Eur J Pharmacol 487:125-132. CrossRef Medline
17. Hilaire G, Duron B (1999) Maturation of the mammalian respiratory system. Physiol Rev 79:325-360. Medline
18. Hodges MR, Richerson GB (2008a) Contributions of 5-HT neurons to respiratory control: neuromodulatory and trophic effects. Respir Physiol Neurobiol 164:222-232. CrossRef Medline
19. Hodges MR, Richerson GB (2008b) Interaction between defects in ventilatory and thermoregulatory control in mice lacking 5-HT neurons. Respir Physiol Neurobiol 164:350-357. CrossRef Medline
20. Hodges MR, Tattersall GJ, Harris MB, McEvoy SD, Richerson DN, Deneris ES, Johnson RL, Chen ZF, Richerson GB (2008) Defects in breathing and thermoregulation in mice with near-complete absence of central serotonin neurons. J Neurosci 28:2495-2505. CrossRef Medline
21. Hodges MR, Wehner M, Aungst J, Smith JC, Richerson GB (2009) Transgenic mice lacking serotonin neurons have severe apnea and high mortality during development. J Neurosci 29:10341-10349. CrossRef Medline
22. Hodges MR, Best S, Richerson GB (2011) Altered ventilatory and thermoregulatory control in male and female adult Pet-1 null mice. RespIR Physiol Neurobiol 177:133-140. CrossRef Medline
23. Lalley PM (1986) Serotonergic and non-serotonergic responses of phrenic motoneurones to raphé stimulation in the cat. J Physiol 380:373-385. Medline
24. LalleyPM (1994) The excitability and rhythm of medullary respiratory neurons in the cat are altered by the serotonin receptor agonist 5-methoxy-N-N, dimethyltryptamin. Brain Res 648:87-98. CrossRef Medline
25. Lalley PM, Bischoff AM, Richter DW (1994) 5-HT-1A receptor-mediated modulation of medullary expiratory neurones in the cat. J Physiol 476: 117-130. Medline
26. Liu Q, Wong-RileyMT (2010) Postnatal changes in the expressions of serotonin 1A, 1B and 2A receptors in ten brain stem nuclei of the rat: implication for a sensitive period. Neuroscience 165:61-78. CrossRef Medline
27. Manzke T, Dutschmann M, Schlaf G, Mörschel M, Koch UR, Ponimaskin E, Bidon O, Lalley PM, Richter DW (2009) Serotonin targets inhibitory synapses to induce modulation of network functions. Philos Trans R Soc Lond B Biol Sci 364:2589-2602. CrossRef Medline
28. Marder E, Goaillard JM (2006) Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci 7:563-574. CrossRef Medline
29. McCall RB, Clement ME (1989) Identification of serotonergic and sympathetic neurons in medullary raphé nuclei. Brain Res 477:172-182. CrossRef Medline
30. 2 in newborn piglets. J Appl Physiol 96:1909-1919. CrossRef Medline
31. Meyer LC, Fuller A, Mitchell D (2006) Zacopride and 8-OH-DPAT reverse opioid-induced respiratory depression and hypoxia but not catatonic immobilization in goats. Am J Physiol Regul Integr Comp Physiol 290: R405-R413. CrossRef Medline
32. Muneoka KT, Takigawa M (2003) 5-Hydroxytryptamine7 (5-HT7) receptor immunoreactivity-positive "stigmoid body"-like structure in developing rat brains. Int J Dev Neurosci 21:133-143. CrossRef Medline
33. Nakamura K, Morrison SF (2007) Central efferent pathways mediating skin cooling-evoked sympathetic thermogenesis in brown adipose tissue. AmJ Physiol Regul Integr Comp Physiol 292:R127-R136. CrossRef Medline
34. Nucci TB, Branco LG, Gargaglioni LH (2008) 5-HT1A, but not 5-HT2 and 5-HT7, receptors in the nucleus raphémagnus modulate hypoxiainduced hyperpnoea. Acta Physiol (Oxf) 193:403-414. CrossRef Medline
35. Okabe S, Mackiewicz M, Kubin L (1997) Serotonin receptor mRNA expression in the hypoglossal motor nucleus. Respir Physiol 110:151-160. CrossRef Medline
36. Ootsuka Y, Blessing WW (2006) Thermogenesis in brown adipose tissue: increase by 5-HT2A receptor activation and decrease by 5-HT1A receptor activation in conscious rats. Neurosci Lett 395:170-174. CrossRef Medline
37. Peña F, Ramirez JM (2002) Endogenous activation of serotonin-2A receptors is required for respiratory rhythm generation in vitro. J Neurosci 22:11055-11064. Medline
38. Ptak K, Yamanishi T, Aungst J, Milescu LS, Zhang R, Richerson GB, Smith JC (2009) Raphé neurons stimulate respiratory circuit activity by multiple mechanisms via endogenously released serotonin and substance P. J Neurosci 29:3720-3737. CrossRef Medline
39. Raymond JR, Mukhin YV, Gettys TW, GarnovskayaMN (1999) The recombinant 5-HT1A receptor: G protein coupling and signaling pathways. Br J Pharmacol 127:1751-1764. CrossRef Medline
40. Richerson GB (2004) Serotonergic neurons as carbon dioxide sensors that maintain pH homeostasis. Nat Rev Neurosci 5:449-461. CrossRef Medline
41. Richter DW, Manzke T, Wilken B, Ponimaskin E (2003) Serotonin receptors: guardians of stable breathing. Trends Mol Med 9:542-548. CrossRef Medline
42. Sahibzada N, Ferreira M, Wasserman AM, Taveira-DaSilva AM, Gillis RA (2000) Reversal of morphine-induced apnea in the anesthetized rat by drugs that activate 5-hydroxytryptamine(1A) receptors. J Pharmacol Exp Ther 292:704-713. Medline
43. 1 agonists reduce 5-hydroxytryptamine release in rat hippocampus in vivo as determined by brain microdialysis. Br J Pharmacol 96:283-290. CrossRef Medline
44. Shevtsova NA, Manzke T, Molkov YI, Bischoff A, Smith JC, Rybak IA, Richter DW (2011) Computational modelling of 5-HT receptor-mediated reorganization of the brainstem respiratory network. Eur J Neurosci 34:1276-1291. CrossRef Medline
45. Smith JC, Ellenberger HH, Ballanyi K, Richter DW, Feldman JL (1991) Pre-Bötzinger complex: a brainstem region that may generate respiratory rhythm in mammals. Science 254:726-729. CrossRef Medline
46. Stettner GM, Zanella S, Hilaire G, Dutschmann M (2008) 8-OH-DPAT suppresses spontaneous central apneas in the C57BL/6J mouse strain. Respir Physiol Neurobiol 161:10-15. CrossRef Medline
47. Taylor NC, Li A, Nattie EE (2005) Medullary serotonergic neurones modulate the ventilatory response to hypercapnia, but not hypoxia in conscious rats. J Physiol 566:543-557. CrossRef Medline
48. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107. CrossRef Medline
49. Veasey SC, Fornal CA, Metzler CW, Jacobs BL (1995) Response of serotonergic caudal raphé neurons in relation to specific motor activities in freely moving cats. J Neurosci 15:5346-5359. Medline
50. Viemari JC, Garcia AJ 3rd, Doi A, Ramirez JM (2011) Activation of alpha-2 noradrenergic receptors is critical for the generation of fictive eupnea and fictive gasping inspiratory activities in mammals in vitro. Eur J Neurosci 33:2228-2237. CrossRef Medline
51. Wilken B, Lalley P, Bischoff AM, Christen HJ, Behnke J, Hanefeld F, Richter DW (1997) Treatment of apneustic respiratory disturbance with a serotonin-receptor agonist. J Pediatr 130:89-94. CrossRef Medline
52. Zhao ZQ, Scott M, Chiechio S, Wang JS, Renner KJ, GereauRW4th, Johnson RL, Deneris ES, Chen ZF (2006) Lmx1b is required for maintenance of central serotonergic neurons and mice lacking central serotonergic system exhibit normal locomotor activity. J Neurosci 26:12781-12788. CrossRef Medline