Stress-induced hyperthermia and basal body temperature are mediated by different 5-HT1A receptor populations: A study in SERT knockout rats

European Journal of Pharmacology

Volumn 590, Issue 1-3, 2008, Pages 190-197

  Olivier, Jocelien D A ^a   Cools, Alexander R ^a   Olivier, Berend ^c,d   Homberg, Judith R ^a,e   Cuppen, Edwin ^e   Ellenbroek, Bart A ^a,b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b Evotec ^*  (Germany)

^c UTRECHT UNIVERSITY   (Netherlands)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e HUBRECHT INSTITUTE   (Netherlands)

Author keywords

(Knockout rat); 5 HT1A receptor; Serotonin transporter; Stress induced hyperthermia; Temperature

Indexed keywords

FLESINOXAN; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; SEROTONIN 1A RECEPTOR; SEROTONIN TRANSPORTER;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL BODY TEMPERATURE; CONTROLLED STUDY; CORE TEMPERATURE; GENOTYPE; HYPERTHERMIA; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; RAT STRAIN; RECEPTOR INTRINSIC ACTIVITY; SEROTONIN RELEASE; SEROTONINERGIC SYSTEM; STRESS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY TEMPERATURE; CIRCADIAN RHYTHM; FEVER; MALE; PIPERAZINES; PYRIDINES; RATS; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PSYCHOLOGICAL; TACHYCARDIA;

EID: 48049122651     PISSN: 00142999     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ejphar.2008.06.008     Document Type: Article

References (64)

1. Banky Z., Molnar J., Csernus V., and Halasz B. Further studies on circadian hormone rhythms after local pharmacological destruction of the serotoninergic innervation of the rat suprachiasmatic region before the onset of the corticosterone rhythm. Brain Res. 445 (1988) 222-227
2. Baumgartner A., Hiedra L., Pinna G., Eravci M., Prengel H., and Meinhold H. Rat brain type II 5′-iodothyronine deiodinase activity is extremely sensitive to stress. J. Neurochem. 71 (1998) 817-826
3. Beitchman J.H., Baldassarra L., Mik H., De Luca V., King N., Bender D., Ehtesham S., and Kennedy J.L. Serotonin transporter polymorphisms and persistent, pervasive childhood aggression. Am. J. Psychiatry 163 (2006) 1103-1105
4. Bengel D., Murphy D.L., Andrews A.M., Wichems C.H., Feltner D., Heils A., Mossner R., Westphal H., and Lesch K.P. Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine ("Ecstasy") in serotonin transporter-deficient mice. Mol. Pharmacol. 53 (1998) 649-655
5. Benstaali C., Mailloux A., Bogdan A., Auzeby A., and Touitou Y. Circadian rhythms of body temperature and motor activity in rodents their relationships with the light-dark cycle. Life Sci. 68 (2001) 2645-2656
6. Berlin I., Warot D., Legout V., Guillemant S., Schollnhammer G., and Puech A.J. Blunted 5-HT1A-receptor agonist-induced corticotropin and cortisol responses after long-term ipsapirone and fluoxetine administration to healthy subjects. Clin. Pharmacol. Ther. 63 (1998) 428-436
7. Bill D.J., Knight M., Forster E.A., and Fletcher A. Direct evidence for an important species difference in the mechanism of 8-OH-DPAT-induced hypothermia. Br. J. Pharmacol. 103 (1991) 1857-1864
8. Blier P., and De Montigny C. Possible serotonergic mechanisms underlying the antidepressant and anti-obsessive-compulsive disorder responses. Biol. Psychiatry 44 (1998) 313-323
9. Blier P., Seletti B., Gilbert F., Young S.N., and Benkelfat C. Serotonin 1A receptor activation and hypothermia in humans: lack of evidence for a presynaptic mediation. Neuropsychopharmacology 27 (2002) 301-308
10. Bouwknecht J.A., Hijzen T.H., van der G.J., Maes R.A., and Olivier B. Stress-induced hyperthermia in mice: effects of flesinoxan on heart rate and body temperature. Eur. J. Pharmacol. 400 (2000) 59-66
11. Bouwknecht J.A., van der G.J., Hijzen T.H., Maes R.A., Hen R., and Olivier B. Corticosterone responses in 5-HT1B receptor knockout mice to stress or 5-HT1A receptor activation are normal. Psychopharmacology (Berl) 153 (2001) 484-490
12. Bouwknecht A.J., Olivier B., and Paylor R.E. The stress-induced hyperthermia paradigm as a physiological animal model for anxiety: a review of pharmacological and genetic studies in the mouse. Neurosci. Biobehav. Rev. 31 (2007) 41-59
13. Briley M., and Moret C. Neurobiological mechanisms involved in antidepressant therapies. Clin. Neuropharmacol. 16 (1993) 387-400
14. Caspi A., Sugden K., Moffitt T.E., Taylor A., Craig I.W., Harrington H., McClay J., Mill J., Martin J., Braithwaite A., and Poulton R. Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science 301 (2003) 386-389
15. Covault J., Tennen H., Armeli S., Conner T.S., Herman A.I., Cillessen A.H.N., and Kranzler H.R. Interactive effects of the serotonin transporter 5-HTTLPR polymorphism and stressful life events on college student drinking and drug use. Biol. Psychiatry 61 (2007) 609-616
16. Cryan J.F., Kelliher P., Kelly J.P., and Leonard B.E. Comparative effects of serotonergic agonists with varying efficacy at the 5-HT(1A) receptor on core body temperature: modification by the selective 5-HT(1A) receptor antagonist WAY 100635. J. Psychopharmacol. 13 (1999) 278-283
17. Davidson C., and Stamford J.A. Contrasting effects of chronic paroxetine on 5-HT1A control of dorsal raphe cell firing and 5-HT release. Neuroreport 9 (1998) 2535-2538
18. Delgado P.L., Charney D.S., Price L.H., Aghajanian G.K., Landis H., and Heninger G.R. Serotonin function and the mechanism of antidepressant action. Reversal of antidepressant-induced remission by rapid depletion of plasma tryptophan. Arch. Gen. Psychiatry 47 (1990) 411-418
19. De Vry J. 5-HT1A receptor agonists: recent developments and controversial issues. Psychopharmacology (Berl) 121 (1995) 1-26
20. Friedman B.H., and Thayer J.F. Autonomic balance revisited: panic anxiety and heart rate variability. J. Psychosom. Res. 44 (1998) 133-151
21. Goodwin G.M., De Souza R.J., and Green A.R. The pharmacology of the hypothermic response in mice to 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT). A model of presynaptic 5-HT1 function. Neuropharmacology 24 (1985) 1187-1194
22. Goodwin G.M., De Souza R.J., Green A.R., and Heal D.J. The pharmacology of the behavioural and hypothermic responses of rats to 8-hydroxy-2-(di-n-propylamino)tetralin (8-OH-DPAT). Psychopharmacology (Berl) 91 (1987) 506-511
23. Groenink L., van der Gugten J., Zethof T.J., van der Heyden J.A., and Olivier B. Neuroendocrine effects of diazepam and flesinoxan in the stress-induced hyperthermia test in mice. Pharmacol. Biochem. Behav. 54 (1996) 249-254
24. Hahn M.K., and Blakely R.D. Monoamine transporter gene structure and polymorphisms in relation to psychiatric and other complex disorders. Pharmacogenomics. J. 2 (2002) 217-235
25. Hedlund P.B., Danielson P.E., Thomas E.A., Slanina K., Carson M.J., and Sutcliffe J.G. No hypothermic response to serotonin in 5-HT7 receptor knockout mice. Proc. Natl. Acad. Sci. U.S.A 100 (2003) 1375-1380
26. Higgins G.A., Bradbury A.J., Jones B.J., and Oakley N.R. Behavioural and biochemical consequences following activation of 5HT1-like and GABA receptors in the dorsal raphe nucleus of the rat. Neuropharmacology 27 (1988) 993-1001
27. Hillegaart V. Effects of local application of 5-HT and 8-OH-DPAT into the dorsal and median raphe nuclei on core temperature in the rat. Psychopharmacology (Berl) 103 (1991) 291-296
28. Hjorth S. Hypothermia in the rat induced by the potent serotoninergic agent 8-OH-DPAT. J. Neural Transm. 61 (1985) 131-135
29. Holmes A., Murphy D.L., and Crawley J.N. Abnormal behavioral phenotypes of serotonin transporter knockout mice: parallels with human anxiety and depression. Biol. Psychiatry 54 (2003) 953-959
30. Homberg J.R., Olivier J.D., Smits B.M., Mul J.D., Mudde J., Verheul M., Nieuwenhuizen O.F., Cools A.R., Ronken E., Cremers T., Schoffelmeer A.N., Ellenbroek B.A., and Cuppen E. Characterization of the serotonin transporter knockout rat: a selective change in the functioning of the serotonergic system. Neuroscience 146 (2007) 1662-1676
31. Le Poul E., Laaris N., Doucet E., Laporte A.M., Hamon M., and Lanfumey L. Early desensitization of somato-dendritic 5-HT1A autoreceptors in rats treated with fluoxetine or paroxetine. Naunyn Schmiedebergs Arch. Pharmacol. 352 (1995) 141-148
32. Lesch K.P. 5-HT1A receptor responsivity in anxiety disorders and depression. Prog. Neuropsychopharmacol. Biol. Psychiatry 15 (1991) 723-733
33. Li Q., Muma N.A., and Van De Kar L.D. Chronic fluoxetine induces a gradual desensitization of 5-HT1A receptors: reductions in hypothalamic and midbrain Gi and G(o) proteins and in neuroendocrine responses to a 5-HT1A agonist. J. Pharmacol. Exp. Ther. 279 (1996) 1035-1042
34. Li Q., Muma N.A., Battaglia G., and Van De Kar L.D. A desensitization of hypothalamic 5-HT1A receptors by repeated injections of paroxetine: reduction in the levels of G(i) and G(o) proteins and neuroendocrine responses, but not in the density of 5-HT1A receptors. J. Pharmacol. Exp. Ther. 282 (1997) 1581-1590
35. Li Q., Wichems C., Heils A., Van De Kar L.D., Lesch K.P., and Murphy D.L. Reduction of 5-hydroxytryptamine (5-HT)(1A)-mediated temperature and neuroendocrine responses and 5-HT(1A) binding sites in 5-HT transporter knockout mice. J. Pharmacol. Exp. Ther. 291 (1999) 999-1007
36. Martin K.F., Phillips I., Hearson M., Prow M.R., and Heal D.J. Characterization of 8-OH-DPAT-induced hypothermia in mice as a 5-HT1A autoreceptor response and its evaluation as a model to selectively identify antidepressants. Br. J. Pharmacol. 107 (1992) 15-21
37. Millan M.J., Rivet J.M., Canton H., Le Marouille-Girardon S., and Gobert A. Induction of hypothermia as a model of 5-hydroxytryptamine1A receptor-mediated activity in the rat: a pharmacological characterization of the actions of novel agonists and antagonists. J. Pharmacol. Exp. Ther. 264 (1993) 1364-1376
38. Moreno F.A., Rowe D.C., Kaiser B., Chase D., Michaels T., Gelernter J., and Delgado P.L. Association between a serotonin transporter promoter region polymorphism and mood response during tryptophan depletion. Mol. Psychiatry 7 (2002) 213-216
39. Murphy D.L. Neuropsychiatric disorders and the multiple human brain serotonin receptor subtypes and subsystems. Neuropsychopharmacology 3 (1990) 457-471
40. Murphy D.L., Andrews A.M., Wichems C.H., Li Q., Tohda M., and Greenberg B. Brain serotonin neurotransmission: an overview and update with an emphasis on serotonin subsystem heterogeneity, multiple receptors, interactions with other neurotransmitter systems, and consequent implications for understanding the actions of serotonergic drugs. J. Clin. Psychiatry 59 Suppl 15 (1998) 4-12
41. Nalivaiko E., Ootsuka Y., and Blessing W.W. Activation of 5-HT1A receptors in the medullary raphe reduces cardiovascular changes elicited by acute psychological and inflammatory stresses in rabbits. Am. J. Physiol. Regul. Integr. Comp. Physiol. 289 (2005) R596-R604
42. Neumeister A., Konstantinidis A., Stastny J., Schwarz M.J., Vitouch O., Willeit M., Praschak-Rieder N., Zach J., de Z.M., Bondy B., Ackenheil M., and Kasper S. Association between serotonin transporter gene promoter polymorphism (5HTTLPR) and behavioral responses to tryptophan depletion in healthy women with and without family history of depression. Arch. Gen. Psychiatry 59 (2002) 613-620
43. Nijsen M.J., Croiset G., Diamant M., Broekhoven M.H., De Wied D., and Wiegant V.M. Vagal activation in novelty-induced tachycardia during the light phase in the rat. Physiol. Behav. 63 (1998) 233-239
44. Nijsen M.J., Croiset G., Diamant M., Stam R., Delsing D., De Wied D., and Wiegant V.M. Conditioned fear-induced tachycardia in the rat: vagal involvement. Eur. J. Pharmacol. 350 (1998) 211-222
45. Olivier B., Tulp M.Th.M., and van der Poel A.M. Serotonergic receptors in anxiety and aggression: evidence from animal pharmacology. Hum. Psychopharmacol. 6 (1991) S73-S78
46. Olivier B., Zethof T.J., Ronken E., and van der Heyden J.A. Anxiolytic effects of flesinoxan in the stress-induced hyperthermia paradigm in singly-housed mice are 5-HT1A receptor mediated. Eur. J. Pharmacol. 342 (1998) 177-182
47. Olivier J.D., Van Der Hart M.G., Van Swelm R.P., Dederen P.J., Homberg J.R., Cremers T., Deen P.M., Cuppen E., Cools A.R., and Ellenbroek B.A. A study in male and female 5-HT transporter knockout rats: an animal model for anxiety and depression disorders. Neuroscience 152 (2008) 573-584
48. Ootsuka Y., and Blessing W.W. 5-Hydroxytryptamine 1A receptors inhibit cold-induced sympathetically mediated cutaneous vasoconstriction in rabbits. J. Physiol. 552 (2003) 303-314
49. Ootsuka Y., and Blessing W.W. Activation of 5-HT1A receptors in rostral medullary raphe inhibits cutaneous vasoconstriction elicited by cold exposure in rabbits. Brain Res. 1073-1074 (2006) 252-261
50. Pitchot W., Wauthy J., Hansenne M., Pinto E., Fuchs S., Reggers J., Legros J.J., and Ansseau M. Hormonal and temperature responses to the 5-HT1A receptor agonist flesinoxan in normal volunteers. Psychopharmacology (Berl) 164 (2002) 27-32
51. Pitchot W., Wauthy J., Legros J.J., and Ansseau M. Hormonal and temperature responses to flesinoxan in normal volunteers: an antagonist study. Eur. Neuropsychopharmacol. 14 (2004) 151-155
52. Reppert S.M., and Weaver D.R. Coordination of circadian timing in mammals. Nature 418 (2002) 935-941
53. Sargent P., Williamson D.J., Pearson G., Odontiadis J., and Cowen P.J. Effect of paroxetine and nefazodone on 5-HT1A receptor sensitivity. Psychopharmacology (Berl) 132 (1997) 296-302
54. Schmitz A., Hennig J., Kuepper Y., and Reuter M. The association between neurotism and the serotonin transporter polymorphism depends on structural differences between personality measures. Pers. Individ. Differ. 42 (2007) 789-799
55. Sgoifo A., Stilli D., Medici D., Gallo P., Aimi B., and Musso E. Electrode positioning for reliable telemetry ECG recordings during social stress in unrestrained rats. Physiol. Behav. 60 (1996) 1397-1401
56. Smits B.M., Mudde J., Plasterk R.H., and Cuppen E. Target-selected mutagenesis of the rat. Genomics 83 (2004) 332-334
57. Smits B.M., Mudde J.B., van de Belt J., Verheul M., Olivier J., Homberg J., Guryev V., Cools A.R., Ellenbroek B.A., Plasterk R.H., and Cuppen E. Generation of gene knockouts and mutant models in the laboratory rat by ENU-driven target-selected mutagenesis. Pharmacogenet. Genomics 16 (2006) 159-169
58. Sollars P.J., Ogilvie M.D., Rea M.A., and Pickard G.E. 5-HT1B receptor knockout mice exhibit an enhanced response to constant light. J. Biol. Rhythms 17 (2002) 428-437
59. Sollars P.J., Ogilvie M.D., Simpson A.M., and Pickard G.E. Photic entrainment is altered in the 5-HT1B receptor knockout mouse. J. Biol. Rhythms 21 (2006) 21-32
60. Stain-Malmgren R., Khoury A.E., berg-Wistedt A., and Tham A. Serotonergic function in major depression and effect of sertraline and paroxetine treatment. Int. Clin. Psychopharmacol. 16 (2001) 93-101
61. van Bogaert M.J., Groenink L., Oosting R.S., Westphal K.G., van der G.J., and Olivier B. Mouse strain differences in autonomic responses to stress. Genes Brain Behav. 5 (2006) 139-149
62. van Bogaert M.J., Oosting R., Toth M., Groenink L., van Oorschot R., and Olivier B. Effects of genetic background and null mutation of 5-HT1A receptors on basal and stress-induced body temperature: modulation by serotonergic and GABAA-ergic drugs. Eur. J. Pharmacol. 550 (2006) 84-90
63. van der Heyden J.A., Zethof T.J., and Olivier B. Stress-induced hyperthermia in singly housed mice. Physiol. Behav. 62 (1997) 463-470
64. Vinkers C.H., van Bogaert M., Klanker M., Korte S.M., Oosting R.S., Hanania T., Hopkins S., Olivier B., and Groenink L. Translational aspects of pharmacological research into anxiety disorders: the stress-induced hyperthermia (SIH) paradigm. Eur. J. Pharmacol. 585 (2008) 407-425