Increased serotonin-1A (5-HT1A) autoreceptor expression and reduced raphe serotonin levels in deformed epidermal autoregulatory factor-1 (Deaf-1) gene knock-out mice

Journal of Biological Chemistry

Volumn 287, Issue 9, 2012, Pages 6615-6627

  Czesak, Margaret ^a   Le François, Brice ^a   Millar, Anne M ^a   Deria, Mariam ^a   Daigle, Mireille ^a   Visvader, Jane E ^b   Anisman, Hymie ^c   Albert, Paul R ^a  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c CARLETON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL COUNT; CELL MODEL; DE-REPRESSION; FRONTAL CORTEX; GENE TRANSCRIPTIONS; HYDROXYLASES; IN-SITU HYBRIDIZATION; IN-VITRO; IN-VIVO; KNOCK OUTS; KNOCKOUT MICE; MOOD DISORDERS; QUANTITATIVE RT-PCR; RECEPTOR GENES; WILD TYPES;

AMINO ACIDS; BRAIN; CELLS; CYTOLOGY; MAMMALS; POLYMERASE CHAIN REACTION; PROTEINS; RNA; TRANSCRIPTION;

GENE EXPRESSION REGULATION;

AUTORECEPTOR; DEFORMED EPIDERMAL AUTOREGULATORY FACTOR 1; MESSENGER RNA; REGULATOR PROTEIN; SEROTONIN; SEROTONIN 1A RECEPTOR; TRYPTOPHAN HYDROXYLASE 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; DEFORMED EPIDERMAL AUTOREGULATORY FACTOR 1 GENE; DNA POLYMORPHISM; DORSAL RAPHE NUCLEUS; FRONTAL CORTEX; GENE; GENE EXPRESSION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE TEST; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ANALYSIS; SIBLING; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; AUTORECEPTORS; DEPRESSIVE DISORDER; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; POLYMORPHISM, GENETIC; PROMOTER REGIONS, GENETIC; RAPHE NUCLEI; RECEPTOR, SEROTONIN, 5-HT1A; RNA, MESSENGER; SEROTONIN; TRANSCRIPTION FACTORS; TRYPTOPHAN HYDROXYLASE;

MUS;

EID: 84857470871     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.293027     Document Type: Article

References (65)

1. Charney, D. S., Krystal, J. H., Delgado, P. L., and Heninger, G. R. (1990) Serotonin-specific drugs for anxiety and depressive disorders. Annu. Rev. Med. 41, 437-446 (Pubitemid 20121749)
2. Mann, J. J. (1999) Role of the serotonergic system in the pathogenesis of major depression and suicidal behavior. Neuropsychopharmacology 21, 99S-105S
3. Jans, L. A., Riedel, W. J., Markus, C. R., and Blokland, A. (2007) Serotonergic vulnerability and depression: assumptions, experimental evidence and implications. Mol. Psychiatry 12, 522-543 (Pubitemid 46816766)
4. Piñeyro, G., and Blier, P. (1999) Autoregulation of serotonin neurons: role in antidepressant drug action. Pharmacol. Rev. 51, 533-591 (Pubitemid 29420214)
5. Blier, P. (2003) The pharmacology of putative early-onset antidepressant strategies. Eur. Neuropsychopharmacol. 13, 57-66
6. Chalmers, D. T., and Watson, S. J. (1991) Comparative anatomical distribution of 5-HT1A receptor mRNA and 5-HT1A binding in rat brain: a combined in situ hybridization/in vitro receptor autoradiographic study. Brain Res. 561, 51-60
7. Pompeiano, M., Palacios, J. M., and Mengod, G. (1992) Distribution and cellular localization of mRNA coding for 5-HT1A receptor in the rat brain: correlation with receptor binding. J. Neurosci. 12, 440-453
8. Ramboz, S., Oosting, R., Amara, D. A., Kung, H. F., Blier, P., Mendelsohn, M., Mann, J. J., Brunner, D., and Hen, R. (1998) Serotonin receptor 1A knock-out: an animal model of anxiety-related disorder. Proc. Natl. Acad. Sci. U.S.A. 95, 14476-14481 (Pubitemid 28549392)
9. Parks, C. L., Robinson, P. S., Sibille, E., Shenk, T., and Toth, M. (1998) Increased anxiety of mice lacking the serotonin 1A receptor. Proc. Natl. Acad. Sci. U.S.A. 95, 10734-10739
10. Heisler, L. K., Chu, H. M., Brennan, T. J., Danao, J. A., Bajwa, P., Parsons, L. H., and Tecott, L. H. (1998) Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice. Proc. Natl. Acad. Sci. U.S.A. 95, 15049-15054 (Pubitemid 29003754)
11. Santarelli, L., Saxe, M., Gross, C., Surget, A., Battaglia, F., Dulawa, S., Weisstaub, N., Lee, J., Duman, R., Arancio, O., Belzung, C., and Hen, R. (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805-809 (Pubitemid 36962615)
12. Kusserow, H., Davies, B., Hörtnagl, H., Voigt, I., Stroh, T., Bert, B., Deng, D. R., Fink, H., Veh, R. W., and Theuring, F. (2004) Reduced anxietyrelated behavior in transgenic mice overexpressing serotonin 1A receptors. Brain Res. Mol. Brain Res. 129, 104-116 (Pubitemid 39304254)
13. Gross, C., Zhuang, X., Stark, K., Ramboz, S., Oosting, R., Kirby, L., Santarelli, L., Beck, S., and Hen, R. (2002) Serotonin 1A receptor acts during development to establish normal anxiety-like behavior in the adult. Nature 416, 396-400 (Pubitemid 34272867)
14. Lemonde, S., Rogaeva, A., and Albert, P. R. (2004) Cell type-dependent recruitment of trichostatin A-sensitive repression of the human 5-HT1A receptor gene. J. Neurochem 88, 857-868 (Pubitemid 38199306)
15. Ou, X. M., Jafar-Nejad, H., Storring, J. M., Meng, J. H., Lemonde, S., and Albert, P. R. (2000) Novel dual repressor elements for neuronal cell-specific transcription of the rat 5-HT1A receptor gene. J. Biol. Chem. 275, 8161-8168 (Pubitemid 30159731)
16. Le François, B., Czesak, M., Steubl, D., and Albert, P. R. (2008) Transcriptional regulation at a HTR1A polymorphism associated with mental illness. Neuropharmacology 55, 977-985
17. Kishi, T., Tsunoka, T., Ikeda, M., Kawashima, K., Okochi, T., Kitajima, T., Kinoshita, Y., Okumura, T., Yamanouchi, Y., Inada, T., Ozaki, N., and Iwata, N. (2009) Serotonin 1A receptor gene and major depressive disorder: an association study and meta-analysis. J. Hum. Genet. 54, 629-633
18. Lemonde, S., Turecki, G., Bakish, D., Du, L., Hrdina, P. D., Bown, C. D., Sequeira, A., Kushwaha, N., Morris, S. J., Basak, A., Ou, X. M., and Albert, P. R. (2003) Impaired repression at a 5-hydroxytryptamine 1A receptor gene polymorphism associated with major depression and suicide. J. Neurosci. 23, 8788-8799 (Pubitemid 37176660)
19. Czesak, M., Lemonde, S., Peterson, E. A., Rogaeva, A., and Albert, P. R. (2006) Cell-specific repressor or enhancer activities of Deaf-1 at a serotonin 1A receptor gene polymorphism. J. Neurosci. 26, 1864-1871 (Pubitemid 43236999)
20. Parsey, R. V., Oquendo, M. A., Ogden, R. T., Olvet, D. M., Simpson, N., Huang, Y. Y., Van Heertum, R. L., Arango, V., and Mann, J. J. (2006) Altered serotonin 1A binding in major depression: a [carbonyl-C-11]WAY100635 positron emission tomography study. Biol. Psychiatry 59, 106-113 (Pubitemid 43117499)
21. Sullivan, G. M., Ogden, R. T., Oquendo, M. A., Kumar, J. S., Simpson, N., Huang, Y. Y., Mann, J. J., and Parsey, R. V. (2009) Positron emission tomography quantification of serotonin-1A receptor binding in medicationfree bipolar depression. Biol. Psychiatry 66, 223-230
22. Parsey, R. V., Ogden, R. T., Miller, J. M., Tin, A., Hesselgrave, N., Goldstein, E., Mikhno, A., Milak, M., Zanderigo, F., Sullivan, G. M., Oquendo, M. A., and Mann, J. J. (2010) Higher serotonin 1A binding in a second major depression cohort: modeling and reference region considerations. Biol. Psychiatry 68, 170-178
23. Boldrini, M., Underwood, M. D., Mann, J. J., and Arango, V. (2008) Serotonin-1A autoreceptor binding in the dorsal raphe nucleus of depressed suicides. J. Psychiatr. Res. 42, 433-442 (Pubitemid 351240919)
24. Stockmeier, C. A., Shapiro, L. A., Dilley, G. E., Kolli, T. N., Friedman, L., and Rajkowska, G. (1998) Increase in serotonin-1A autoreceptors in the midbrain of suicide victims with major depression-postmortem evidence for decreased serotonin activity. J. Neurosci. 18, 7394-7401 (Pubitemid 28425823)
25. Hahm, K., Sum, E. Y., Fujiwara, Y., Lindeman, G. J., Visvader, J. E., and Orkin, S. H. (2004) Defective neural tube closure and anteroposterior patterning in mice lacking the LIM protein LMO4 or its interacting partner Deaf-1. Mol. Cell. Biol. 24, 2074-2082 (Pubitemid 38248946)
26. Paxinos, G., and Franklin, K. (2001) The Mouse Brain, 2nd Ed., Academic Press, New York
27. Bonnin, A., Peng, W., Hewlett, W., and Levitt, P. (2006) Expression mapping of 5-HT1 serotonin receptor subtypes during fetal and early postnatal mouse forebrain development. Neuroscience 141, 781-794 (Pubitemid 44066651)
28. Ferguson, K. L., McClellan, K. A., Vanderluit, J. L., McIntosh, W. C., Schuurmans, C., Polleux, F., and Slack, R. S. (2005) A cell-autonomous requirement for the cell cycle regulatory protein, Rb, in neuronal migration. EMBO J. 24, 4381-4391 (Pubitemid 41828912)
29. Czesak, M., Burns, A. M., Lenicov, F. R., and Albert, P. R. (2007) Characterization of rat rostral raphe primary cultures: multiplex quantification of serotonergic markers. J. Neurosci. Methods 164, 59-67 (Pubitemid 46935970)
30. Livak, K. J., and Schmittgen, T. D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25, 402-408 (Pubitemid 34164012)
31. Huggenvik, J. I., Michelson, R. J., Collard, M. W., Ziemba, A. J., Gurley, P., and Mowen, K. A. (1998) Characterization of a nuclear deformed epidermal autoregulatory factor-1 (DEAF-1)-related (NUDR) transcriptional regulator protein. Mol. Endocrinol. 12, 1619-1639 (Pubitemid 30663442)
32. Jensen, P., Farago, A. F., Awatramani, R. B., Scott, M. M., Deneris, E. S., and Dymecki, S. M. (2008) Redefining the serotonergic system by genetic lineage. Nat. Neurosci. 11, 417-419 (Pubitemid 351441875)
33. Kim, J. Y., Duan, X., Liu, C. Y., Jang, M. H., Guo, J. U., Pow-anpongkul, N., Kang, E., Song, H., and Ming, G. L. (2009) DISC1 regulates new neuron development in the adult brain via modulation of AKT-mTOR signaling through KIAA1212. Neuron 63, 761-773
34. Holick, K. A., Lee, D. C., Hen, R., and Dulawa, S. C. (2008) Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33, 406-417 (Pubitemid 350243341)
35. Zhang, X., Beaulieu, J. M., Sotnikova, T. D., Gainetdinov, R. R., and Caron, M. G. (2004) Tryptophan hydroxylase-2 controls brain serotonin synthesis. Science 305, 217 (Pubitemid 38886729)
36. Carneiro, A. M., Airey, D. C., Thompson, B., Zhu, C. B., Lu, L., Chesler, E. J., Erikson, K. M., and Blakely, R. D. (2009) Functional coding variation in recombinant inbred mouse lines reveals multiple serotonin transporter- associated phenotypes. Proc. Natl. Acad. Sci. U.S.A. 106, 2047-2052
37. Jacobsen, K. X., Czesak, M., Deria, M., Le François, B., and Albert, P. R. (2011) Region-specific regulation of 5-HT1A receptor expression by Pet-1-dependent mechanisms in vivo. J. Neurochem. 116, 1066-1076
38. Liu, C., Maejima, T., Wyler, S. C., Casadesus, G., Herlitze, S., and Deneris, E. S. (2010) Pet-1 is required across different stages of life to regulate serotonergic function. Nat. Neurosci. 13, 1190-1198
39. He, M., Sibille, E., Benjamin, D., Toth, M., and Shippenberg, T. (2001) Differential effects of 5-HT1A receptor deletion upon basal and fluoxetine- evoked 5-HT concentrations as revealed by in vivo microdialysis. Brain Res. 902, 11-17 (Pubitemid 32499270)
40. Richer, M., Hen, R., and Blier, P. (2002) Modification of serotonin neuron properties in mice lacking 5-HT1A receptors. Eur. J. Pharmacol. 435, 195-203 (Pubitemid 34131700)
41. Bortolozzi, A., Amargós-Bosch, M., Toth, M., Artigas, F., and Adell, A. (2004) In vivo efflux of serotonin in the dorsal raphe nucleus of 5-HT1A receptor knock-out mice. J. Neurochem. 88, 1373-1379 (Pubitemid 38366912)
42. 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., Hen, R., and Leonardo, E. D. (2010) 5-HT1A autoreceptor levels determine vulnerability to stress and response to antidepressants. Neuron 65, 40-52
43. 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., and 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
44. Bortolozzi, A., Castane, A., Semakova, J., Santana, N., Alvarado, G., Cortes, R., Ferres-Coy, A., Fernandez, G., Carmona, M. C., Toth, M., Perales, J. C., Montefeltro, A., and Artigas, F. (August 2, 2011) Mol. Psychiatry 10.1038/mp.2011.92
45. Jacobsen, K. X., Vanderluit, J. L., Slack, R. S., and Albert, P. R. (2008) HES1 regulates 5-HT1A receptor gene transcription at a functional polymorphism: essential role in developmental expression. Mol. Cell. Neurosci. 38, 349-358
46. Rueter, L. E., De Montigny, C., and Blier, P. (1998) Electrophysiological characterization of the effect of long term duloxetine administration on the rat serotonergic and noradrenergic systems. J. Pharmacol. Exp. Ther. 285, 404-412 (Pubitemid 28237412)
47. Le Poul, E., Boni, C., Hanoun, N., Laporte, A. M., Laaris, N., Chauveau, J., Hamon, M., and Lanfumey, L. (2000) Differential adaptation of brain 5-HT1A and 5-HT1B receptors and 5-HT transporter in rats treated chronically with fluoxetine. Neuropharmacology 39, 110-122
48. Hensler, J. G. (2002) Differential regulation of 5-HT1A receptor-G protein interactions in brain following chronic antidepressant administration. Neuropsychopharmacology 26, 565-573
49. Castro, M. E., Diaz, A., del Olmo, E., and Pazos, A. (2003) Chronic fluoxetine induces opposite changes in G protein coupling at pre- and postsynaptic 5-HT1A receptors in rat brain. Neuropharmacology 44, 93-101 (Pubitemid 36135846)
50. Parsey, R. V., Olvet, D. M., Oquendo, M. A., Huang, Y. Y., Ogden, R. T., and Mann, J. J. (2006) Higher 5-HT1A receptor binding potential during a major depressive episode predicts poor treatment response: preliminary data from a naturalistic study. Neuropsychopharmacology 31, 1745-1749 (Pubitemid 44106705)
51. David, S. P., Murthy, N. V., Rabiner, E. A., Munafó, M. R., Johnstone, E. C., Jacob, R., Walton, R. T., and Grasby, P. M. (2005) A functional genetic variation of the serotonin (5-HT) transporter affects 5-HT1A receptor binding in humans. J. Neurosci. 25, 2586-2590 (Pubitemid 40365170)
52. Abbas, S. Y., Nogueira, M. I., and Azmitia, E. C. (2007) Antagonist-induced increase in 5-HT1A-receptor expression in adult rat hippocampus and cortex. Synapse 61, 531-539 (Pubitemid 46753972)
53. Szewczyk, B., Albert, P. R., Burns, A. M., Czesak, M., Overholser, J. C., Jurjus, G. J., Meltzer, H. Y., Konick, L. C., Dieter, L., Herbst, N., May, W., Rajkowska, G., Stockmeier, C. A., and Austin, M. C. (2009) Gender-specific decrease in NUDR and 5-HT1A receptor proteins in the prefrontal cortex of subjects with major depressive disorder. Int. J. Neuropsychopharmacol. 12, 155-168
54. López, J. F., Chalmers, D. T., Little, K. Y., and Watson, S. J. (1998) A.E. Bennett Research Award. Regulation of serotonin 1A, glucocorticoid, and mineralocorticoid receptor in rat and human hippocampus: implications for the neurobiology of depression. Biol. Psychiatry 43, 547-573 (Pubitemid 28198224)
55. Drevets, W. C., Thase, M. E., Moses-Kolko, E. L., Price, J., Frank, E., Kupfer, D. J., and Mathis, C. (2007) Serotonin-1A receptor imaging in recurrent depression: replication and literature review. Nucl. Med. Biol. 34, 865-877 (Pubitemid 47505401)
56. 11C]WAY-100635: effects of depression and antidepressant treatment. Arch. Gen. Psychiatry 57, 174-180
57. Shively, C. A., Friedman, D. P., Gage, H. D., Bounds, M. C., Brown-Proctor, C., Blair, J. B., Henderson, J. A., Smith, M. A., and Buchheimer, N. (2006) Behavioral depression and positron emission tomography-determined serotonin 1A receptor binding potential in cynomolgus monkeys. Arch. Gen. Psychiatry 63, 396-403
58. Arias, B., Catalán, R., Gastó, C., Gutiérrez, B., and Fañanás, L. (2005) Evidence for a combined genetic effect of the 5-HT(1A) receptor and serotonin transporter genes in the clinical outcome of major depressive patients treated with citalopram. J. Psychopharmacol. 19, 166-172 (Pubitemid 40577221)
59. Baune, B. T., Hohoff, C., Roehrs, T., Deckert, J., Arolt, V., and Domschke, K. (2008) Serotonin receptor 1A-1019C/G variant: impact on antidepressant pharmacoresponse in melancholic depression? Neurosci. Lett. 436, 111-115
60. Hong, C. J., Chen, T. J., Yu, Y. W., and Tsai, S. J. (2006) Response to fluoxetine and serotonin 1A receptor (C-1019G) polymorphism in Taiwan Chinese major depressive disorder. Pharmacogenomics J. 6, 27-33 (Pubitemid 43118308)
61. Serretti, A., Artioli, P., Lorenzi, C., Pirovano, A., Tubazio, V., and Zanardi, R. (2004) The C(-1019)G polymorphism of the 5-HT1A gene promoter and antidepressant response in mood disorders: preliminary findings. Int. J. Neuropsychopharmacol. 7, 453-460 (Pubitemid 39648075)
62. Wang, L., Fang, C., Zhang, A., Du, J., Yu, L., Ma, J., Feng, G., Xing, Q., and He, L. (2008) The -1019 C/G polymorphism of the 5-HT(1)A receptor gene is associated with negative symptom response to risperidone treatment in schizophrenia patients. J. Psychopharmacol. 22, 904-909
63. Yu, Y. W., Tsai, S. J., Liou, Y. J., Hong, C. J., and Chen, T. J. (2006) Association study of two serotonin 1A receptor gene polymorphisms and fluoxetine treatment response in Chinese major depressive disorders. Eur. Neuropsychopharmacol. 16, 498-503 (Pubitemid 44376554)
64. Yevtushenko, O. O., Oros, M. M., and Reynolds, G. P. (2010) Early response to selective serotonin reuptake inhibitors in panic disorder is associated with a functional 5-HT1A receptor gene polymorphism. J. Affect. Disord. 123, 308-311
65. Greene, J., Banasr, M., Lee, B., Warner-Schmidt, J., and Duman, R. S. (2009) Vascular endothelial growth factor signaling is required for the behavioral actions of antidepressant treatment: pharmacological and cellular characterization. Neuropsychopharmacology 34, 2459-2468