Genetic approaches for understanding the role of serotonin receptors in mood and behavior

Current Opinion in Neurobiology

Volumn 23, Issue 3, 2013, Pages 399-406

  Donaldson, Zoe R ^a,b   Nautiyal, Katherine M ^a,b   Ahmari, Susanne E ^a,b   Hen, René ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RECEPTOR SUBTYPE; SEROTONIN; SEROTONIN 1A RECEPTOR; SEROTONIN RECEPTOR;

ANXIETY; BEHAVIOR; GENETIC ANALYSIS; GENETIC VARIABILITY; HUMAN; MOOD; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW;

AFFECT; ANIMALS; BEHAVIOR; BRAIN; HUMANS; MENTAL DISORDERS; MICE; MICE, KNOCKOUT; RECEPTOR, SEROTONIN, 5-HT1A;

EID: 84878356352     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2013.01.011     Document Type: Review

References (66)

1. Burns C.M., Chu H., Rueter S.M., Hutchinson L.K., Canton H., Sanders-Bush E., Emeson R.B. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 1997, 387:303-308.
2. Nichols D.E., Nichols C.D. Serotonin receptors. Chem Rev 2008, 108:1614-1641.
3. Blier P., Pineyro G., el Mansari M., Bergeron R., de Montigny C. Role of somatodendritic 5-HT autoreceptors in modulating 5-HT neurotransmission. Ann NY Acad Sci 1998, 861:204-216.
4. Gardier A.M., Malagie I., Trillat A.C., Jacquot C., Artigas F. Role of 5-HT1A autoreceptors in the mechanism of action of serotoninergic antidepressant drugs: recent findings from in vivo microdialysis studies. Fundam Clin Pharmacol 1996, 10:16-27.
5. Kobilka B.K., Frielle T., Collins S., Yang-Feng T., Kobilka T.S., Francke U., Lefkowitz R.J., Caron M.G. An intronless gene encoding a potential member of the family of receptors coupled to guanine nucleotide regulatory proteins. Nature 1987, 329:75-79.
6. De Vry J. 5-HT1A receptor agonists: recent developments and controversial issues. Psychopharmacology (Berl) 1995, 121:1-26.
7. Raymond J.R., Fargin A., Lohse M.J., Regan J.W., Senogles S.E., Lefkowitz R.J., Caron M.G. Identification of the ligand-binding subunit of the human 5-hydroxytryptamine1A receptor with N-(p-azido-m-[125I] iodophenethyl)spiperone, a high affinity radioiodinated photoaffinity probe. Mol Pharmacol 1989, 36:15-21.
8. Raymond J.R., Kim J., Beach R.E., Tisher C.C. Immunohistochemical mapping of cellular and subcellular distribution of 5-HT1A receptors in rat and human kidneys. Am J Physiol 1993, 264:F9-F19.
9. Aghajanian G Electrophysiology of serotonin receptor subtypes and signal transduction mechanisms. Psychopharmacology (The Fourth Generation of Progress) 1995, 451-460. Raven Press. F. Bloom, D. Kupfer (Eds.).
10. Pazos A., Cortes R., Palacios J.M. Quantitative autoradiographic mapping of serotonin receptors in the rat brain. II. Serotonin-2 receptors. Brain Res 1985, 346:231-249.
11. Barone P., Jordan D., Atger F., Kopp N., Fillion G. Quantitative autoradiography of 5-HT1D and 5-HT1E binding sites labelled by [3H]5-HT, in frontal cortex and the hippocampal region of the human brain. Brain Res 1994, 638:85-94.
12. Kung M.P., Frederick D., Mu M., Zhuang Z.P., Kung H.F. 4-(2'-Methoxy-phenyl)-1-[2'-(n-2'-pyridinyl)-p-iodobenzamido]-ethyl-piperazine ([125I]p-MPPI) as a new selective radioligand of serotonin-1A sites in rat brain: in vitro binding and autoradiographic studies. J Pharmacol Exp Ther 1995, 272:429-437.
13. Parks C.L., Robinson P.S., Sibille E., Shenk T., Toth M. Increased anxiety of mice lacking the serotonin1A receptor. Proc Natl Acad Sci U S A 1998, 95:10734-10739.
14. Heisler L.K., Chu H.M., Brennan T.J., Danao J.A., Bajwa P., Parsons L.H., Tecott L.H. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc Natl Acad Sci U S A 1998, 95:15049-15054.
15. Ramboz S., Oosting R., Amara D.A., Kung H.F., Blier P., Mendelsohn M., Mann J.J., Brunner D., Hen R. Serotonin receptor 1A knockout: an animal model of anxiety-related disorder. Proc Natl Acad Sci U S A 1998, 95:14476-14481.
16. Ansorge M.S., Zhou M., Lira A., Hen R., Gingrich J.A. Early-life blockade of the 5-HT transporter alters emotional behavior in adult mice. Science 2004, 306:879-881.
17. 2+/calmodulin-dependent protein kinase II contributes to the developmental programming of anxiety in serotonin receptor 1A knock-out mice. J Neurosci 2008, 28:6250-6257.
18. Vinkers C.H., Oosting R.S., van Bogaert M.J., Olivier B., Groenink L. Early-life blockade of 5-HT(1A) receptors alters adult anxiety behavior and benzodiazepine sensitivity. Biol Psychiatry 2010, 67:309-316.
19. Gross C., Zhuang X., Stark K., Ramboz S., Oosting R., Kirby L., Santarelli L., Beck S., Hen R. Serotonin1A receptor acts during development to establish normal anxiety-like behaviour in the adult. Nature 2002, 416:396-400.
20. Richardson-Jones J.W., Craige C.P., Guiard B.P., Stephen A., Metzger K.L., Kung H.F., Gardier A.M., Dranovsky A., David D.J., Beck S.G., et al. 5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 2010, 65:40-52.
21. 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., et al. Serotonin-1A autoreceptors are necessary and sufficient for the normal formation of circuits underlying innate anxiety. J Neurosci 2011, 31:6008-6018.
22. Carola V., Gross C. Mouse models of the 5-HTTLPR×stress risk factor for depression. Curr Top Behav Neurosci 2012, 12:59-72.
23. Albert P.R., Lemonde S. 5-HT1A receptors, gene repression, and depression: guilt by association. Neuroscientist 2004, 10:575-593.
24. Bortolozzi A., Castane A., Semakova J., Santana N., Alvarado G., Cortes R., Ferres-Coy A., Fernandez G., Carmona M.C., Toth M., et al. New antidepressant strategy based on acute siRNA silencing of 5-HT1A autoreceptors. Mol Psychiatry 2012, 17:567.
25. Blier P., Bergeron R. The use of pindolol to potentiate antidepressant medication. J Clin Psychiatry 1998, 59(Suppl 5):16-23. discussion 24-15.
26. Veenstra-VanderWeele J., Muller C.L., Iwamoto H., Sauer J.E., Owens W.A., Shah C.R., Cohen J., Mannangatti P., Jessen T., Thompson B.J., et al. Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior. Proc Natl Acad Sci U S A 2012, 109:5469-5474.
27. Stober G., Heils A., Lesch K.P. Serotonin transporter gene polymorphism and affective disorder. Lancet 1996, 347:1340-1341.
28. Albert P.R. Transcriptional regulation of the 5-HT1A receptor: implications for mental illness. Phil Trans Royal Soc Lond Ser B Biol Sci 2012, 367:2402-2415.
29. Shin L.M., Liberzon I. The neurocircuitry of fear, stress, and anxiety disorders. Neuropsychopharmacology 2010, 35:169-191.
30. Kheirbek M.A., Klemenhagen K.C., Sahay A., Hen R. Neurogenesis and generalization: a new approach to stratify and treat anxiety disorders. Nat Neurosci 2012, 15:1613-1620.
31. Graeff F.G. Serotonin, the periaqueductal gray and panic. Neurosci Biobehav Rev 2004, 28:239-259.
32. Holmes A. Genetic variation in cortico-amygdala serotonin function and risk for stress-related disease. Neurosci Biobehav Rev 2008, 32:1293-1314.
33. Hale M.W., Shekhar A., Lowry C.A. Stress-related serotonergic systems: implications for symptomatology of anxiety and affective disorders. Cell Mol Neurobiol 2012, 32:695-708.
34. Haddjeri N., Lavoie N., Blier P. Electrophysiological evidence for the tonic activation of 5-HT(1A) autoreceptors in the rat dorsal raphe nucleus. Neuropsychopharmacology 2004, 29:1800-1806.
35. He M., Sibille E., Benjamin D., Toth M., Shippenberg T. Differential effects of 5-HT1A receptor deletion upon basal and fluoxetine-evoked 5-HT concentrations as revealed by in vivo microdialysis. Brain Res 2001, 902:11-17.
36. Parsons L.H., Kerr T.M., Tecott L.H. 5-HT(1A) receptor mutant mice exhibit enhanced tonic, stress-induced and fluoxetine-induced serotonergic neurotransmission. J Neurochem 2001, 77:607-617.
37. Richer M., Hen R., Blier P. Modification of serotonin neuron properties in mice lacking 5-HT1A receptors. Eur J Pharmacol 2002, 435:195-203.
38. Ceci A., Baschirotto A., Borsini F. 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 1994, 33:709-713.
39. Casanovas J.M., Hervas I., Artigas F. Postsynaptic 5-HT1A receptors control 5-HT release in the rat medial prefrontal cortex. Neuroreport 1999, 10:1441-1445.
40. Peyron C., Petit J.M., Rampon C., Jouvet M., Luppi P.H. Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 1998, 82:443-468.
41. Araneda R., Andrade R. 5-Hydroxytryptamine2 and 5-hydroxytryptamine(1A) receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience 1991, 40:399-412.
42. Ashby C.R., Edwards E., Wang R.Y. Electrophysiological evidence for a functional interaction between 5-HT(1A) and 5-HT(2A) receptors in the rat medial prefrontal cortex: an iontophoretic study. Synapse 1994, 17:173-181.
43. Cai X., Gu Z., Zhong P., Ren Y., Yan Z. Serotonin 5-HT 1A receptors regulate AMPA receptor channels through inhibiting Ca 2+/calmodulin-dependent kinase II in prefrontal cortical pyramidal neurons. J Biol Chem 2002, 277:36553-36562.
44. Hamon M., Lanfumey L., el Mestikawy S., Boni C., Miquel M.C., Bolanos F., Schechter L., Gozlan H. The main features of central 5-HT1 receptors. Neuropsychopharmacology 1990, 3:349-360.
45. Barnes N.M., Sharp T. A review of central 5-HT receptors and their function. Neuropharmacology 1999, 38:1083-1152.
46. Rainnie D.G. Serotonergic modulation of neurotransmission in the rat basolateral amygdala. J Neurophysiol 1999, 82:69-85.
47. Fisher P.M., Meltzer C.C., Ziolko S.K., Price J.C., Hariri A.R. Capacity for 5-HT1A-mediated autoregulation predicts amygdala reactivity. Nat Neurosci 2006, 9:1362-1363.
48. Fisher P.M., Price J.C., Meltzer C.C., Moses-Kolko E.L., Becker C., Berga S.L., Hariri A.R. Medial prefrontal cortex serotonin 1A and 2A receptor binding interacts to predict threat-related amygdala reactivity. Biol Mood Anxiety Disord 2011, 1:2.
49. McHugh T.J., Jones M.W., Quinn J.J., Balthasar N., Coppari R., Elmquist J.K., Lowell B.B., Fanselow M.S., Wilson M.A., Tonegawa S. Dentate gyrus NMDA receptors mediate rapid pattern separation in the hippocampal network. Science 2007, 317:94-99.
50. Maren S., Quirk G.J. Neuronal signalling of fear memory. Nat Rev Neurosci 2004, 5:844-852.
51. Gray J.A., McNaughton N. The neuropsychology of anxiety: reprise. Nebr Symp Motiv 1996, 43:61-134.
52. Herman J.P., Ostrander M.M., Mueller N.K., Figueiredo H. Limbic system mechanisms of stress regulation: hypothalamo-pituitary-adrenocortical axis. Prog Neuropsychopharmacol Biol Psychiatry 2005, 29:1201-1213.
53. Santarelli L., Saxe M., Gross C., Surget A., Battaglia F., Dulawa S., Weisstaub N., Lee J., Duman R., Arancio O., et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 2003, 301:805-809.
54. Wang S.H., Zhang Z.J., Guo Y.J., Teng G.J., Chen B.A. Decreased expression of serotonin 1A receptor in the dentate gyrus in association with chronic mild stress: a rat model of post-stroke depression. Psychiatry Res 2009, 170:245-251.
55. Spinelli S., Chefer S., Carson R.E., Jagoda E., Lang L., Heilig M., Barr C.S., Suomi S.J., Higley J.D., Stein E.A. Effects of early-life stress on serotonin1A receptors in juvenile rhesus monkeys measured by positron emission tomography. Biol Psychiatry 2010, 67:1146-1153.
56. Iyo A.H., Kieran N., Chandran A., Albert P.R., Wicks I., Bissette G., Austin M.C. Differential regulation of the serotonin 1A transcriptional modulators five prime repressor element under dual repression-1 and nuclear-deformed epidermal autoregulatory factor by chronic stress. Neuroscience 2009, 163:1119-1127.
57. Lanfumey L., Pardon M.C., Laaris N., Joubert C., Hanoun N., Hamon M., Cohen-Salmon C. 5-HT(1A) autoreceptor desensitization by chronic ultramild stress in mice. Neuroreport 1999, 10:3369-3374.
58. Laaris N., Haj-Dahmane S., Hamon M., Lanfumey L. Glucocorticoid receptor-mediated inhibition by corticosterone of 5-HT(1A) autoreceptor functioning in the rat dorsal raphe nucleus. Neuropharmacology 1995, 34:1201-1210.
59. Laaris N., Le Poul E., Hamon M., Lanfumey L. Stress-induced alterations of somatodendritic 5-HT(1A) autoreceptor sensitivity in the rat dorsal raphe nucleus-in vitro electrophysiological evidence. Fundam Clin Pharmacol 1997, 11:206-214.
60. Gartside S.E., Johnson D.A., Leitch M.M., Troakes C., Ingram C.D. Early life adversity programs changes in central 5-HT neuronal function in adulthood. Eur J Neurosci 2003, 17:2401-2408.
61. Blier P. Altered function of the serotonin 1A autoreceptor and the antidepressant response. Neuron 2010, 65:1-2.
62. Lucki I. The spectrum of behaviors influenced by serotonin. Biol Psychiatry 1998, 44:151-162.
63. Tanaka K.F., Ahmari S.E., Leonardo E.D., Richardson-Jones J.W., Budreck E.C., Scheiffele P., Sugio S., Inamura N., Ikenaka K., Hen R. Flexible accelerated STOP tetracycline operator-knockin (FAST): a versatile and efficient new gene modulating system. Biol Psychiatry 2010, 67:770-773.
64. Ahlenius S., Larsson K., Arvidsson L.E. Effects of stereoselective 5-HT1A agonists on male rat sexual behavior. Pharmacol Biochem Behav 1989, 33:691-695.
65. Guptarak J., Sarkar J., Hiegel C., Uphouse L. Role of 5-HT(1A) receptors in fluoxetine-induced lordosis inhibition. Horm Behav 2010, 58:290-296.
66. Saudou F., Amara D.A., Dierich A., LeMeur M., Ramboz S., Segu L., Buhot M.C., Hen R. Enhanced aggressive behavior in mice lacking 5-HT(1B) receptor. Science 1994, 265:1875-1878.