Adaptive changes in serotonin metabolism preserve normal behavior in mice with reduced TPH2 activity

Neuropharmacology

Volumn 85, Issue , 2014, Pages 73-80

  Mosienko, Valentina ^a   Matthes, Susann ^a,b   Hirth, Natalie ^c   Beis, Daniel ^a,b   Flinders, Michael ^a   Bader, Michael ^a   Hansson, Anita C ^c   Alenina, Natalia ^a  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c CENTRAL INSTITUTE OF MENTAL HEALTH   (Germany)

Author keywords

Anxiety; Depression like behavior; Gene polymorphism; Serotonin; TPH2

Indexed keywords

8 HYDROXY 2 PROPYLAMINOTETRALIN; AUTORECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; SEROTONIN 1A RECEPTOR; 2 DIPROPYLAMINO 8 HYDROXYTETRALIN; SEROTONIN; SEROTONIN 1 AGONIST; TPH2 PROTEIN, MOUSE; TRYPTOPHAN HYDROXYLASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; AUTORADIOGRAPHY; BIODEGRADATION; CONGENIC STRAIN; CONTROLLED STUDY; DEPRESSION; DOWN REGULATION; EVOLUTIONARY ADAPTATION; GENE; GENE DELETION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; HETEROZYGOSITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOMOZYGOSITY; HYPOTHERMIA; MALE; MOUSE; MOUSE MODEL; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; SEROTONIN BRAIN LEVEL; SEROTONIN METABOLISM; SIGNAL TRANSDUCTION; TPH2 GENE; TRANSGENIC MOUSE; ANIMAL; ANXIETY; BRAIN; C57BL MOUSE; CHEMICALLY INDUCED; DEFICIENCY; FEMALE; GENETICS; METABOLISM; NERVE CELL PLASTICITY; NEUROPSYCHOLOGICAL TEST; PATHOPHYSIOLOGY; PHYSIOLOGY;

8-HYDROXY-2-(DI-N-PROPYLAMINO)TETRALIN; ANIMALS; ANXIETY; BRAIN; DEPRESSION; FEMALE; HYPOTHERMIA; MALE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONAL PLASTICITY; NEUROPSYCHOLOGICAL TESTS; RECEPTOR, SEROTONIN, 5-HT1A; SEROTONIN; SEROTONIN 5-HT1 RECEPTOR AGONISTS; TRYPTOPHAN HYDROXYLASE;

EID: 84902123522     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2014.05.015     Document Type: Article

References (51)

1. N. Alenina, D. Kikic, M. Todiras, V. Mosienko, F. Qadri, and R. Plehm et al. Growth retardation and altered autonomic control in mice lacking brain serotonin Proc. Natl. Acad. Sci. U. S. A. 106 25 2009 10332 10337
2. J.C. Alvarez, M. Sanceaume, C. Advenier, and O. Spreux-Varoquaux Differential changes in brain and platelet 5-HT concentrations after steady-state achievement and repeated administration of antidepressant drugs in mice Eur. Neuropsychopharmacol. 10 1 1999 31 36
3. M. Angoa-Perez, M.J. Kane, D.I. Briggs, C.E. Sykes, M.M. Shah, and D.M. Francescutti et al. Genetic depletion of brain 5HT reveals a common molecular pathway mediating compulsivity and impulsivity J. Neurochem. 121 6 2012 974 984
4. J.M. Beaulieu, X. Zhang, R.M. Rodriguiz, T.D. Sotnikova, M.J. Cools, and W.C. Wetsel et al. Role of GSK3 beta in behavioral abnormalities induced by serotonin deficiency Proc. Natl. Acad. Sci. U. S. A. 105 4 2008 1333 1338 (Pubitemid 351397053)
5. S.M. Berger, T. Weber, S. Perreau-Lenz, M.A. Vogt, S.E. Gartside, and C. Maser-Gluth et al. A functional Tph2 C1473G polymorphism causes an anxiety phenotype via compensatory changes in the serotonergic system Neuropsychopharmacology 37 9 2012 1986 1998
6. I. Brunk, M. Holtje, B. von Jagow, S. Winter, J. Sternberg, and C. Blex et al. Regulation of vesicular monoamine and glutamate transporters by vesicle-associated trimeric G proteins: new jobs for long-known signal transduction molecules Handb. Exp. Pharmacol. 175 2006 305 325
7. P.J. Cowen Psychopharmacology of 5-HT(1A) receptors Nucl. Med. Biol. 27 5 2000 437 439 (Pubitemid 30658143)
8. R.M. De Almeida, M. Giovenardi, H. Charchat, and A.B. Lucion 8-OH-DPAT in the median raphe nucleus decreases while in the medial septal area it may increase anxiety in female rats Neurosci. Biobehav. Rev. 23 2 1998 259 264 (Pubitemid 29011627)
9. L. Descarries, and M. Riad Effects of the antidepressant fluoxetine on the subcellular localization of 5-HT1A receptors and SERT Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 1601 2012 2416 2425
10. S.P. Fernandez, and P. Gaspar Investigating anxiety and depressive-like phenotypes in genetic mouse models of serotonin depletion Neuropharmacology 62 1 2012 144 154
11. J.D. Fernstrom, and R.J. Wurtman Brain serotonin content: physiological dependence on plasma tryptophan levels Science N. Y. 173 3992 1971 149 152
12. M.D. Gershon, and J. Tack The serotonin signaling system: from basic understanding to drug development for functional GI disorders Gastroenterology 132 1 2007 397 414 (Pubitemid 46127672)
13. C. Gross, L. Santarelli, D. Brunner, X. Zhuang, and R. Hen Altered fear circuits in 5-HT(1A) receptor KO mice Biol. Psychiatry 48 12 2000 1157 1163 (Pubitemid 32008441)
14. L. Gutknecht, N. Araragi, S. Merker, J. Waider, F.M. Sommerlandt, and B. Mlinar et al. Impacts of brain serotonin deficiency following Tph2 inactivation on development and raphe neuron serotonergic specification PLoS One 7 8 2012 e43157
15. L. Gutknecht, C. Kriegebaum, J. Waider, A. Schmitt, and K.P. Lesch Spatio-temporal expression of tryptophan hydroxylase isoforms in murine and human brain: convergent data from Tph2 knockout mice Eur. Neuropsychopharmacol. 19 4 2009 266 282
16. L. Gutknecht, J. Waider, S. Kraft, C. Kriegebaum, B. Holtmann, and A. Reif et al. Deficiency of brain 5-HT synthesis but serotonergic neuron formation in Tph2 knockout mice J. Neural Transm. 115 8 2008 1127 1132
17. L.K. Heisler, H.M. Chu, T.J. Brennan, J.A. Danao, P. Bajwa, and L.H. Parsons et al. Elevated anxiety and antidepressant-like responses in serotonin 5-HT1A receptor mutant mice Proc. Natl. Acad. Sci. U. S. A. 95 25 1998 15049 15054 (Pubitemid 29003754)
18. M. Holtje, B. von Jagow, I. Pahner, M. Lautenschlager, H. Hortnagl, and B. Nurnberg et al. The neuronal monoamine transporter VMAT2 is regulated by the trimeric GTPase Go(2) J. Neurosci. 20 6 2000 2131 2141 (Pubitemid 30230065)
19. M. Holtje, S. Winter, D. Walther, I. Pahner, H. Hortnagl, and O.P. Ottersen et al. The vesicular monoamine content regulates VMAT2 activity through Galphaq in mouse platelets. Evidence for autoregulation of vesicular transmitter uptake J. Biol. Chem. 278 18 2003 15850 15858 (Pubitemid 36799700)
20. R.W. Invernizzi Role of TPH-2 in brain function: news from behavioral and pharmacologic studies J. Neurosci. Res. 85 14 2007 3030 3035 (Pubitemid 350057357)
21. J.P. Jacobsen, W.B. Siesser, B.D. Sachs, S. Peterson, M.J. Cools, and V. Setola et al. Deficient serotonin neurotransmission and depression-like serotonin biomarker alterations in tryptophan hydroxylase 2 (Tph2) loss-of-function mice Mol. Psychiatry 17 7 2012 694 704
22. R.J. Katz Animal models and human depressive disorders Neurosci. Biobehav. Rev. 5 2 1981 231 246 (Pubitemid 11074537)
23. R.J. Katz Animal model of depression: pharmacological sensitivity of a hedonic deficit Pharmacol. Biochem. Behav 16 6 1982 965 968 (Pubitemid 12081655)
24. K. Kobayashi, S. Morita, H. Sawada, T. Mizuguchi, K. Yamada, and I. Nagatsu et al. Targeted disruption of the tyrosine hydroxylase locus results in severe catecholamine depletion and perinatal lethality in mice J. Biol. Chem. 270 45 1995 27235 27243
25. N. Koen, and D.J. Stein Pharmacotherapy of anxiety disorders: a critical review Dialogues Clin. Neurosci. 13 4 2011 423 437
26. K.P. Lesch, N. Araragi, J. Waider, D. van den Hove, and L. Gutknecht Targeting brain serotonin synthesis: insights into neurodevelopmental disorders with long-term outcomes related to negative emotionality, aggression and antisocial behaviour Philos. Trans. R. Soc. Lond. B Biol. Sci. 367 1601 2012 2426 2443
27. K.P. Lesch, and J. Waider Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders Neuron 76 1 2012 175 191
28. M. Lesurtel, and P.A. Clavien Serotonin: a key molecule in acute and chronic liver injury Clin. Res. Hepatol. Gastroenterol. 36 4 2012 319 322
29. Y. Liu, Y. Jiang, Y. Si, J.Y. Kim, Z.F. Chen, and Y. Rao Molecular regulation of sexual preference revealed by genetic studies of 5-HT in the brains of male mice Nature 472 7341 2011 95 99
30. I. Lucki The spectrum of behaviors influenced by serotonin Biol. Psychiatry 44 3 1998 151 162 (Pubitemid 28378297)
31. S. Matthes, V. Mosienko, S. Bashammakh, N. Alenina, and M. Bader Tryptophan hydroxylase as novel target for the treatment of depressive disorders Pharmacology 85 2 2010 95 109
32. S. Migliarini, G. Pacini, B. Pelosi, G. Lunardi, and M. Pasqualetti Lack of brain serotonin affects postnatal development and serotonergic neuronal circuitry formation Mol. Psychiatry 18 10 2013 1106 1118
33. V. Mosienko, B. Bert, D. Beis, S. Matthes, H. Fink, and M. Bader et al. Exaggerated aggression and decreased anxiety in mice deficient in brain serotonin Transl. Psychiatry 2 2012 e122
34. K.B. Neal, L.J. Parry, and J.C. Bornstein Strain-specific genetics, anatomy and function of enteric neural serotonergic pathways in inbred mice J. Physiol. 587 Pt 3 2009 567 586
35. D.V. Osipova, A.V. Kulikov, and N.K. Popova C1473G polymorphism in mouse tph2 gene is linked to tryptophan hydroxylase-2 activity in the brain, intermale aggression, and depressive-like behavior in the forced swim test J. Neurosci. Res. 87 5 2009 1168 1174
36. C.L. Parks, P.S. Robinson, E. Sibille, T. Shenk, and M. Toth Increased anxiety of mice lacking the serotonin1A receptor Proc. Natl. Acad. Sci. U. S. A. 95 18 1998 10734 10739
37. J.W. Richardson-Jones, C.P. Craige, T.H. Nguyen, H.F. Kung, A.M. Gardier, and A. Dranovsky et al. Serotonin-1A autoreceptors are necessary and sufficient for the normal formation of circuits underlying innate anxiety J. Neurosci. 31 16 2011 6008 6018
38. A. Romaniuk, M. Koprowska, M. Krotewicz, M. Strzelczuk, and M. Wieczorek Effects of 8-OHDPAT administration into the dorsal raphe nucleus and dorsal hippocampus on fear behavior and regional brain monoamines distribution in rats Behav. Brain Res. 120 1 2001 47 57 (Pubitemid 32118147)
39. B.D. Sachs, J.P. Jacobsen, T.L. Thomas, W.B. Siesser, W.L. Roberts, and M.G. Caron The effects of congenital brain serotonin deficiency on responses to chronic fluoxetine Transl. Psychiatry 3 2013 e291
40. B.D. Sachs, R.M. Rodriguiz, W.B. Siesser, A. Kenan, E.L. Royer, and J.P. Jacobsen et al. The effects of brain serotonin deficiency on behavioural disinhibition and anxiety-like behaviour following mild early life stress Int. J. Neuropsychopharmacol. 16 9 2013 2081 2094
41. S.A. Sakowski, T.J. Geddes, and D.M. Kuhn Mouse tryptophan hydroxylase isoform 2 and the role of proline 447 in enzyme function J. Neurochem. 96 3 2006 758 765
42. W.B. Siesser, B.D. Sachs, A.J. Ramsey, T.D. Sotnikova, J.M. Beaulieu, and X. Zhang et al. Chronic SSRI treatment exacerbates serotonin deficiency in humanized Tph2 mutant mice ACS Chem. Neurosci. 4 1 2013 84 88
43. W.B. Siesser, X. Zhang, J.P. Jacobsen, T.D. Sotnikova, R.R. Gainetdinov, and M.G. Caron Tryptophan hydroxylase 2 genotype determines brain serotonin synthesis but not tissue content in C57Bl/6 and BALB/c congenic mice Neurosci. Lett. 481 1 2010 6 11
44. K. Tenner, F. Qadri, B. Bert, J.P. Voigt, and M. Bader The mTPH2 C1473G single nucleotide polymorphism is not responsible for behavioural differences between mouse strains Neurosci. Lett. 431 1 2008 21 25
45. D.M. Thomas, M. Angoa Perez, D.M. Francescutti-Verbeem, M.M. Shah, and D.M. Kuhn The role of endogenous serotonin in methamphetamine-induced neurotoxicity to dopamine nerve endings of the striatum J. Neurochem. 115 3 2010 595 605
46. D.J. Walther, and M. Bader A unique central tryptophan hydroxylase isoform Biochem. Pharmacol. 66 9 2003 1673 1680 (Pubitemid 37249312)
47. D.J. Walther, J.U. Peter, S. Bashammakh, H. Hortnagl, M. Voits, and H. Fink et al. Synthesis of serotonin by a second tryptophan hydroxylase isoform Science N. Y. 299 5603 2003 76 (Pubitemid 36042402)
48. V.K. Yadav, F. Oury, N. Suda, Z.W. Liu, X.B. Gao, and C. Confavreux et al. A serotonin-dependent mechanism explains the leptin regulation of bone mass, appetite, and energy expenditure Cell 138 5 2009 976 989
49. X. Zhang, J.M. Beaulieu, T.D. Sotnikova, R.R. Gainetdinov, and M.G. Caron Tryptophan hydroxylase-2 controls brain serotonin synthesis Science N. Y. 305 5681 2004 217 (Pubitemid 38886729)
50. Q.Y. Zhou, and R.D. Palmiter Dopamine-deficient mice are severely hypoactive, adipsic, and aphagic Cell 83 7 1995 1197 1209 (Pubitemid 26007810)
51. Q.Y. Zhou, C.J. Quaife, and R.D. Palmiter Targeted disruption of the tyrosine hydroxylase gene reveals that catecholamines are required for mouse fetal development Nature 374 6523 1995 640 643