Serotonin 1A auto-receptors are not sufficient to modulate anxiety in mice

European Journal of Neuroscience

Volumn 38, Issue 4, 2013, Pages 2621-2627

  Piszczek, Lukasz ^a   Schlax, Kevin ^a   Wyrzykowska, Anna ^a   Piszczek, Agnieszka ^a   Audero, Enrica ^a,b   Thilo Gross, Cornelius ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

^b CHAMPALIMAUD CENTRE FOR THE UNKNOWN   (Portugal)

Author keywords

Anxiety; Serotonin; Serotonin 1A receptor; Transgenic mice

Indexed keywords

SEROTONIN 1A RECEPTOR; TRYPTOPHAN HYDROXYLASE 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CONTROLLED STUDY; FEMALE; HOPELESSNESS; HYPOTHERMIA; MALE; MOUSE; NEGATIVE FEEDBACK; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEROTONINERGIC NERVE CELL; TRANSGENIC MOUSE;

EID: 84882581609     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12260     Document Type: Article

References (47)

1. Albert, P.R. (2012) Transcriptional regulation of the 5-HT1A receptor: implications for mental illness. Philos. T. Roy. Soc. B., 367, 2402-2415.
2. Audero, E., Mlinar, B., Baccini, G., Skachokova, Z., Corradetti, R. & Gross, C. (2013) Suppression of serotonin neuron firing increases aggression in mice. J. Neurosci., 33, 8678-8688.
3. Aznar, S., Qian, Z., Shah, R., Rahbek, B. & Knudsen, G.M. (2003) The 5-HT1A serotonin receptor is located on calbindin- and parvalbumin-containing neurons in the rat brain. Brain Res., 959, 58-67.
4. Bailey, S.J. & Toth, M. (2004) Variability in the benzodiazepine response of serotonin 5-HT1A receptor null mice displaying anxiety-like phenotype: evidence for genetic modifiers in the 5-HT-mediated regulation of GABA(A) receptors. J. Neurosci., 24, 6343-6351.
5. Beck, S.G., Pan, Y.-Z., Akanwa, A.C. & Kirby, L.G. (2004) Median and dorsal raphe neurons are not electrophysiologically identical. J. Neurophysiol., 91, 994-1005.
6. Béïque, J.-C., Campbell, B., Perring, P., Hamblin, M.W., Walker, P., Mladenovic, L. & Andrade, R. (2004) Serotonergic regulation of membrane potential in developing rat prefrontal cortex: coordinated expression of 5-hydroxytryptamine (5-HT)1A, 5-HT2A, and 5-HT7 receptors. J. Neurosci., 24, 4807-4817.
7. Blier, P., Piñeyro, G., El Mansari, M., Bergeron, R. & De Montigny, C. (1998) Role of somatodendritic 5-HT autoreceptors in modulating 5-HT neurotransmission. Ann. NY Acad. Sci., 861, 204-216.
8. Bonnavion, P., Bernard, J.-F., Hamon, M., Adrien, J. & Fabre, V. (2010) Heterogeneous distribution of the serotonin 5-HT(1A) receptor mRNA in chemically identified neurons of the mouse rostral brainstem: implications for the role of serotonin in the regulation of wakefulness and REM sleep. J. Comp. Neurol., 518, 2744-2770.
9. Bortolozzi, A., Castañé, A., Semakova, J., Santana, N., Alvarado, G., Cortés, R., Ferrés-Coy, A., Fernández, G., Carmona, M.C., Toth, M., Perales, J.C., Montefeltro, A. & Artigas, F. (2012) New antidepressant strategy based on acute siRNA silencing of 5-HT1A autoreceptors. Mol. Psychiatr., 17, 567.
10. Carola, V., Frazzetto, G., Pascucci, T., Audero, E., Puglisi-Allegra, S., Cabib, S., Lesch, K. & Gross, C. (2008) Identifying molecular substrates in a mouse model of the serotonin transporter × environment risk factor for anxiety and depression. Biol. Psychiat., 63, 840-846.
11. Casanovas, J.M., Hervás, I. & Artigas, F. (1999) Postsynaptic 5-HT1A receptors control 5-HT release in the rat medial prefrontal cortex. NeuroReport, 10, 1441-1445.
12. Ceci, A., Baschirotto, A. & Borsini, F. (1994) The inhibitory effect of 8-OH-DPAT on the firing activity of dorsal raphe serotoninergic neurons in rats is attenuated by lesion of the frontal cortex. Neuropharmacology, 33, 709-713.
13. Celada, P., Puig, M.V., Casanovas, J.M., Guillazo, G. & Artigas, F. (2001) Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: involvement of serotonin-1A, GABA(A), and glutamate receptors. J. Neurosci., 21, 9917-9929.
14. De Almeida, J. & Mengod, G. (2008) Serotonin 1A receptors in human and monkey prefrontal cortex are mainly expressed in pyramidal neurons and in a GABAergic interneuron subpopulation: implications for schizophrenia and its treatment. J. Neurochem., 107, 488-496.
15. De Vivo, M. & Maayani, S. (1986) Characterization of the 5-hydroxytryptamine1a receptor-mediated inhibition of forskolin-stimulated adenylate cyclase activity in guinea pig and rat hippocampal membranes. J. Pharmacol. Exp. Ther., 238, 248-253.
16. El Mestikawy, S., Riad, M., Laporte, A.M., Vergé, D., Daval, G., Gozlan, H. & Hamon, M. (1990) Production of specific anti-rat 5-HT1A receptor antibodies in rabbits injected with a synthetic peptide. Neurosci. Lett., 118, 189-192.
17. Ermakova, O., Piszczek, L., Luciani, L., Cavalli, F.M.G., Ferreira, T., Farley, D., Rizzo, S., Paolicelli, R.C., Al-Banchaabouchi, M., Nerlov, C., Moriggl, R., Luscombe, N.M. & Gross, C. (2011) Sensitized phenotypic screening identifies gene dosage sensitive region on chromosome 11 that predisposes to disease in mice. EMBO Mol. Med., 3, 50-66.
18. Ferreira, T.A., Lo Iacono, L. & Gross, C.T. (2010) Serotonin receptor 1A modulates actin dynamics and restricts dendritic growth in hippocampal neurons. Eur. J. Neurosci., 32, 18-26.
19. Ferrés-Coy, A., Santana, N., Castañé, A., Cortés, R., Carmona, M.C., Toth, M., Montefeltro, A., Artigas, F. & Bortolozzi, A. (2012) Acute 5-HT(1A) autoreceptor knockdown increases antidepressant responses and serotonin release in stressful conditions. Psychopharmacology, 225, 61-74.
20. Gross, C. & Hen, R. (2004) The developmental origins of anxiety. Nat. Rev. Neurosci., 5, 545-552.
21. Gross, C., Zhuang, X., Stark, K., Ramboz, S., Oosting, R., Kirby, L., Santarelli, L., Beck, S. & Hen, R. (2002) Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature, 416, 396-400.
22. Gutknecht, L., Kriegebaum, C., Waider, J., Schmitt, A. & Lesch, K. (2009) Spatio-temporal expression of tryptophan hydroxylase isoforms in murine and human brain: convergent data from Tph2 knockout mice. Eur. Neuropsychopharm., 19, 266-282.
23. Hajós, M. (2003) In vivo inhibition of neuronal activity in the rat ventromedial prefrontal cortex by midbrain-raphe nuclei: role of 5-HT1A receptors. Neuropharmacology, 45, 72-81.
24. Hajós, M., Hajós-Korcsok, E. & Sharp, T. (1999) Role of the medial prefrontal cortex in 5-HT1A receptor-induced inhibition of 5-HT neuronal activity in the rat. Brit. J. Pharmacol., 126, 1741-1750.
25. Heisler, L.K., Chu, H.M., Brennan, T.J., Danao, J.A., Bajwa, P., Parsons, L.H. & Tecott, L.H. (1998) Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc. Natl. Acad. Sci. USA, 95, 15049-15054.
26. Kirby, L.G., Pernar, L., Valentino, R.J. & Beck, S.G. (2003) Distinguishing characteristics of serotonin and non-serotonin-containing cells in the dorsal raphe nucleus: electrophysiological and immunohistochemical studies. Neuroscience, 116, 669-683.
27. Klemenhagen, K.C., Gordon, J.A., David, D.J., Hen, R. & Gross, C.T. (2006) Increased fear response to contextual cues in mice lacking the 5-HT1A receptor. Neuropsychopharmacol., 31, 101-111.
28. Knobelman, D.A., Hen, R. & Lucki, I. (2001) Genetic regulation of extracellular serotonin by 5-hydroxytryptamine(1A) and 5-hydroxytryptamine(1B) autoreceptors in different brain regions of the mouse. J. Pharmacol. Exp. Ther., 298, 1083-1091.
29. Li, Q., Holmes, A., Ma, L., Van de Kar, L.D., Garcia, F. & Murphy, D.L. (2004) Medial hypothalamic 5-hydroxytryptamine (5-HT)1A receptors regulate neuroendocrine responses to stress and exploratory locomotor activity: application of recombinant adenovirus containing 5-HT1A sequences. J. Neurosci., 24, 10868-10877.
30. Lladó-Pelfort, L., Assié, M.-B., Newman-Tancredi, A., Artigas, F. & Celada, P. (2010) Preferential in vivo action of F15599, a novel 5-HT(1A) receptor agonist, at postsynaptic 5-HT(1A) receptors. Brit. J. Pharmacol., 160, 1929-1940.
31. 2+/calmodulin-dependent protein kinase II contributes to the developmental programming of anxiety in serotonin receptor 1A knock-out mice. J. Neurosci., 28, 6250-6257.
32. Martin, K.F., Phillips, I., Hearson, M., Prow, M.R. & Heal, D.J. (1992) 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. Brit. J. Pharmacol., 107, 15-21.
33. Martinez, D., Hwang, D., Mawlawi, O., Slifstein, M., Kent, J., Simpson, N., Parsey, R.V., Hashimoto, T., Huang, Y., Shinn, A., Van Heertum, R., Abi-Dargham, A., Caltabiano, S., Malizia, A., Cowley, H., Mann, J.J. & Laruelle, M. (2001) Differential occupancy of somatodendritic and postsynaptic 5HT(1A) receptors by pindolol: a dose-occupancy study with [11C]WAY 100635 and positron emission tomography in humans. Neuropsychopharmacol., 24, 209-229.
34. Martín-Ruiz, R. & Ugedo, L. (2001) Electrophysiological evidence for postsynaptic 5-HT(1A) receptor control of dorsal raphe 5-HT neurones. Neuropharmacology, 41, 72-78.
35. Newman-Tancredi, A., Martel, J.-C., Assié, M.-B., Buritova, J., Lauressergues, E., Cosi, C., Heusler, P., Bruins Slot, L., Colpaert, F.C., Vacher, B. & Cussac, D. (2009) Signal transduction and functional selectivity of F15599, a preferential post-synaptic 5-HT1A receptor agonist. Brit. J. Pharmacol., 156, 338-353.
36. Palchaudhuri, M. & Flügge, G. (2005) 5-HT1A receptor expression in pyramidal neurons of cortical and limbic brain regions. Cell Tissue Res., 321, 159-172.
37. Parks, C.L., Robinson, P.S., Sibille, E., Shenk, T. & Toth, M. (1998) Increased anxiety of mice lacking the serotonin1A receptor. Proc. Natl. Acad. Sci. USA, 95, 10734-10739.
38. Parsons, L.H., Kerr, T.M. & Tecott, L.H. (2001) 5-HT(1A) receptor mutant mice exhibit enhanced tonic, stress-induced and fluoxetine-induced serotonergic neurotransmission. J. Neurochem., 77, 607-617.
39. Pattij, T., Groenink, L., Hijzen, T.H., Oosting, R.S., Maes, R.A.A., Van der Gugten, J. & Olivier, B. (2002) Autonomic changes associated with enhanced anxiety in 5-HT(1A) receptor knockout mice. Neuropsychopharmacol., 27, 380-390.
40. Rabiner, E.A., Bhagwagar, Z., Gunn, R.N., Cowen, P.J. & Grasby, P.M. (2004) Preferential 5-HT1A autoreceptor occupancy by pindolol is attenuated in depressed patients: effect of treatment or an endophenotype of depression? Neuropsychopharmacol., 29, 1688-1698.
41. Ramboz, S., Oosting, R., Amara, D.A., Kung, H.F., Blier, P., Mendelsohn, M., Mann, J.J., Brunner, D. & Hen, R. (1998) Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc. Natl. Acad. Sci. USA, 95, 14476-14481.
42. Richardson-Jones, J.W., Craige, C.P., Nguyen, T.H., Kung, H.F., Gardier, A.M., Dranovsky, A., David, D.J., Guiard, B.P., Beck, S.G., Hen, R. & Leonardo, E.D. (2011) Serotonin-1A autoreceptors are necessary and sufficient for the normal formation of circuits underlying innate anxiety. J. Neurosci., 31, 6008-6018.
43. Santana, N., Bortolozzi, A., Serrats, J., Mengod, G. & Artigas, F. (2004) Expression of serotonin1A and serotonin2A receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb. Cortex, 14, 1100-1109.
44. Sotelo, C., Cholley, B., El Mestikawy, S., Gozlan, H. & Hamon, M. (1990) Direct immunohistochemical evidence of the existence of 5-HT1A autoreceptors on serotoninergic neurons in the midbrain raphe nuclei. Eur. J. Neurosci., 2, 1144-1154.
45. Tsetsenis, T., Ma, X., Lo Iacono, L., Beck, S.G. & Gross, C. (2007) Suppression of conditioning to ambiguous cues by pharmacogenetic inhibition of the dentate gyrus. Nat. Neurosci., 10, 896-902.
46. Verge, D., Daval, G., Patey, A., Gozlan, H., El Mestikawy, S. & Hamon, M. (1985) Presynaptic 5-HT autoreceptors on serotonergic cell bodies and/or dendrites but not terminals are of the 5-HT1A subtype. Eur. J. Pharmacol., 113, 463-464.
47. Walther, D.J., Peter, J., Bashammakh, S., Hörtnagl, H., Voits, M., Fink, H. & Bader, M. (2003) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science, 299, 76.