Brain serotonin signaling does not determine sexual preference in male mice

PLoS ONE

Volumn 10, Issue 2, 2015, Pages

  Angoa Pérez, Mariana ^a,b   Herrera Mundo, Nieves ^a,b   Kane, Michael J ^a,b   Sykes, Catherine E ^a,b   Anneken, John H ^a,b   Francescutti, Dina M ^a,b   Kuhn, Donald M ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC NUCLEOTIDE GATED CHANNEL; CYCLIC NUCLEOTIDE GATED CHANNEL ALPHA 2; PHEROMONE; SEROTONIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL 2; TRYPTOPHAN HYDROXYLASE 2; UNCLASSIFIED DRUG; TPH2 PROTEIN, HUMAN; TRYPTOPHAN HYDROXYLASE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DECISION MAKING; EXPERIMENTAL BEHAVIORAL TEST; FEMALE; MALE; MATE CHOICE; MOUSE; NONHUMAN; ODOR; OLFACTORY EPITHELIUM; PROTEIN EXPRESSION; SEROTONIN RELEASE; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; VOMERONASAL ORGAN; ANIMAL; BRAIN; C57BL MOUSE; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY;

MUS;

ANIMALS; BRAIN; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SEROTONIN; SEXUAL BEHAVIOR, ANIMAL; SIGNAL TRANSDUCTION; TRYPTOPHAN HYDROXYLASE;

EID: 84923352641     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0118603     Document Type: Article

References (64)

1. Liu Y, Jiang Y, Si Y, Kim JY, Chen ZF, Rao Y (2011) Molecular regulation of sexual preference revealed by genetic studies of 5-HT in the brains of male mice. Nature 472: 95-100. doi: 10.1038/nature09822 PMID: 21441904
2. Steinbusch HW (1981) Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 6: 557-618. PMID: 7017455
3. Monti JM (2011) Serotonin control of sleep-wake behavior. Sleep Med Rev 15: 269-281. doi: 10.1016/j.smrv.2010.11.003 PMID: 21459634
4. Murillo-Rodriguez E, Arias-Carrion O, Zavala-Garcia A, Sarro-Ramirez A, Huitron-Resendiz S, Arankowsky-Sandoval G (2012) Basic sleep mechanisms: an integrative review. Cent Nerv Sys Agents Med Chem 12: 38-54. PMID: 22524274
5. Bortolato M, Pivac N, Muck Seler D, Nikolac Perkovic M, Pessia M, Di Giovanni G (2013) The role of the serotonergic system at the interface of aggression and suicide. Neuroscience 236: 160-185. doi: 10.1016/j.neuroscience.2013.01.015 PMID: 23333677
6. Lesch KP, Araragi N, Waider J, van den Hove D, Gutknecht L (2012) 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: 2426-2443. doi: 10.1098/rstb.2012.0039 PMID: 22826343
7. Fidalgo S, Ivanov DK, Wood SH (2013) Serotonin: from top to bottom. Biogerontology 14: 21-45. doi: 10.1007/s10522-012-9406-3 PMID: 23100172
8. Lam DD, Garfield AS, Marston OJ, Shaw J, Heisler LK (2010) Brain serotonin system in the coordination of food intake and body weight. Pharmacol Biochem Behav 97: 84-91. doi: 10.1016/j.pbb.2010.09.003 PMID: 20837046
9. Blier P (2013) Neurotransmitter targeting in the treatment of depression. J Clin Psychiatry 74 Suppl 2: 19-24. doi: 10.4088/JCP.12084su1c.04 PMID: 24191974
10. Griebel G, Holmes A (2013) 50 years of hurdles and hope in anxiolytic drug discovery. Nat Rev Drug Discov 12: 667-687. doi: 10.1038/nrd4075 PMID: 23989795
11. Fineberg NA, Brown A, Reghunandanan S, Pampaloni I (2012) Evidence-based pharmacotherapy of obsessive-compulsive disorder. Int J Neuropsychopharmacol 15: 1173-1191. doi: 10.1017/S1461145711001829 PMID: 22226028
12. Salis PJ, Dewsbury DA (1971) p-chlorophenylalanine facilitates copulatory behaviour in male rats. Nature 232: 400-401. PMID: 4255664
13. Malmnas CO, Meyerson BJ (1971) p-chlorophenylalanine and copulatory behaviour in the male rat. Nature 232: 398-400. PMID: 4255663
14. Ferguson J, Henriksen S, Cohen H, Mitchell G, Barchas J, Dement W (1970) "Hypersexuality" and behavioral changes in cats caused by administration of p-chlorophenylalanine. Science 168: 499-501. PMID: 5461688
15. Tagliamonte A, Tagliamonte P, Gessa GL, Brodie BB (1969) Compulsive sexual activity induced by p-chlorophenylalanine in normal and pinealectomized male rats. Science 166: 1433-1435. PMID: 5307630
16. Whalen RE, Luttge WG (1970) P-chlorophenylalanine methyl ester: an aphrodisiac? Science 169: 1000-1001. PMID: 5432696
17. Fratta W, Biggio G, Gessa GL (1977) Homosexual mounting behavior induced in male rats and rabbits by a tryptophan-free diet. Life Sci 21: 379-383. PMID: 302380
18. van de Poll NE, van Dis H, Bermond B (1977) The induction of mounting behavior in female rats by p-chlorophenylalanine. Eur J Pharmacol 41: 225-229. PMID: 137815
19. Zhang S, Liu Y, Rao Y (2013) Serotonin signaling in the brain of adult female mice is required for sexual preference. Proc Natl Acad Sci U S A 110: 9968-9973. doi: 10.1073/pnas.1220712110 PMID: 23716677
20. Walther DJ, Peter JU, Bashammakh S, Hortnagl H, Voits M, Fink H, et al. (2003) Synthesis of serotonin by a second tryptophan hydroxylase isoform. Science 299: 76. PMID: 12511643
21. Kim KS, Wessel TC, Stone DM, Carver CH, Joh TH, Park DH (1991) Molecular cloning and characterization of cDNA encoding tryptophan hydroxylase from rat central serotonergic neurons. Brain Res Mol Brain Res 9: 277-283. PMID: 1645430
22. Walther DJ, Bader M (2003) A unique central tryptophan hydroxylase isoform. Biochem Pharmacol 66: 1673-1680. PMID: 14563478
23. Gutknecht L, Waider J, Kraft S, Kriegebaum C, Holtmann B, Reif A, et al. (2008) Deficiency of brain 5-HT synthesis but serotonergic neuron formation in Tph2 knockout mice. J Neural Transm 115: 1127-1132. doi: 10.1007/s00702-008-0096-6 PMID: 18665319
24. Savelieva KV, Zhao S, Pogorelov VM, Rajan I, Yang Q, Cullinan E, et al. (2008) Genetic disruption of both tryptophan hydroxylase genes dramatically reduces serotonin and affects behavior in models sensitive to antidepressants. PLoS ONE 3: e3301. doi: 10.1371/journal.pone.0003301 PMID: 18923670
25. Yadav VK, Oury F, Suda N, Liu ZW, Gao XB, Confavreux C, et al. (2009) A serotonin-dependent mechanism explains the leptin regulation of bonemass, appetite, and energy expenditure. Cell 138: 976-989. doi: 10.1016/j.cell.2009.06.051 PMID: 19737523
26. Thomas DM, Angoa Perez M, Francescutti-Verbeem DM, Shah MM, Kuhn DM (2010) The role of endogenous serotonin in methamphetamine-induced neurotoxicity to dopamine nerve endings of the striatum. J Neurochem 115: 595-605. doi: 10.1111/j.1471-4159.2010.06950.x PMID: 20722968
27. Alenina N, Kikic D, Todiras M, Mosienko V, Qadri F, Plehm R, et al. (2009) Growth retardation and altered autonomic control in mice lacking brain serotonin. Proc Natl Acad Sci USA 106: 10332-10337. doi: 10.1073/pnas.0810793106 PMID: 19520831
28. Narboux-Neme N, Angenard G, Mosienko V, Klempin F, Pitychoutis PM, Deneris E, et al. (2013) Post-natal growth defects in mice with constitutive depletion of central serotonin. ACS Chem Neurosci 4: 171-181. doi: 10.1021/cn300165x PMID: 23336056
29. Klempin F, Beis D, Mosienko V, Kempermann G, Bader M, Alenina N (2013) Serotonin is required for exercise-induced adult hippocampal neurogenesis. J Neurosci 33: 8270-8275. doi: 10.1523/JNEUROSCI.5855-12.2013 PMID: 23658167
30. Hickner S, Hussain N, Angoa-Perez M, Francescutti DM, Kuhn DM, Mateika JH (2014) Ventilatory long-term facilitation is evident after initial and repeated exposure to intermittent hypoxia in mice genetically depleted of brain serotonin. J Appl Physiol 116: 240-250. doi: 10.1152/japplphysiol.01197.2013 PMID: 24336886
31. Gaspar P, Lillesaar C (2012) Probing the diversity of serotonin neurons. Philos Trans R Soc Lond B Biol Sci 367: 2382-2394. doi: 10.1098/rstb.2011.0378 PMID: 22826339
32. Gaspar P, Cases O, Maroteaux L (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4: 1002-1012. PMID: 14618156
33. Levitt P, Harvey JA, Friedman E, Simansky K, Murphy EH (1997) New evidence for neurotransmitter influences on brain development. Trends Neurosci 20: 269-274. PMID: 9185309
34. Lauder JM (1990) Ontogeny of the serotonergic system in the rat: serotonin as a developmental signal. Ann N Y Acad Sci 600: 297-313. PMID: 2252317
35. Trowbridge S, Narboux-Neme N, Gaspar P (2011) Genetic Models of Serotonin (5-HT) Depletion: What do They Tell Us About the Developmental Role of 5-HT? Anat Rec 294: 1615-1623. doi: 10.1002/ar.21248 PMID: 20818612
36. Waider J, Proft F, Langlhofer G, Asan E, Lesch KP, Gutknecht L (2013) GABA concentration and GABAergic neuron populations in limbic areas are differentially altered by brain serotonin deficiency in Tph2 knockout mice. Histochem Cell Biol 139: 267-281. doi: 10.1007/s00418-012-1029-x PMID: 23052836
37. Gutknecht L, Araragi N, Merker S, Waider J, Sommerlandt FM, Mlinar B, et al. (2012) Impacts of brain serotonin deficiency following Tph2 inactivation on development and raphe neuron serotonergic specification. PLoS One 7: e43157. doi: 10.1371/journal.pone.0043157 PMID: 22912815
38. Kriegebaum C, Song NN, Gutknecht L, Huang Y, Schmitt A, Reif A, et al. (2010) Brain-specific conditional and time-specific inducible Tph2 knockout mice possess normal serotonergic gene expression in the absence of serotonin during adult life. Neurochem Int 57: 512-517. doi: 10.1016/j.neuint.2010.06.015 PMID: 20599453
39. Angoa-Perez M, Kane MJ, Briggs DI, Sykes CE, Shah MM, Francescutti DM, et al. (2012) Genetic depletion of brain 5HT reveals a common molecular pathway mediating compulsivity and impulsivity. J Neurochem 121: 974-984. doi: 10.1111/j.1471-4159.2012.07739.x PMID: 22443164
40. Kane MJ, Angoa-Perez M, Briggs DI, Sykes CE, Francescutti DM, Rosenberg DR, et al. (2012) Mice genetically depleted of brain serotonin display social impairments, communication deficits and repetitive behaviors: possible relevance to autism. PLoS One 7: e48975. doi: 10.1371/journal.pone.0048975 PMID: 23139830
41. Mosienko V, Bert B, Beis D, Matthes S, Fink H, Bader M, et al. (2012) Exaggerated aggression and decreased anxiety in mice deficient in brain serotonin. Transl Psychiatry 2: e122. doi: 10.1038/tp.2012.44 PMID: 22832966
42. Thomas DM, Angoa Perez M, Francescutti-Verbeem DM, Shah MM, Kuhn DM (2010) The role of endogenous serotonin in methamphetamine-induced neurotoxicity to dopamine nerve endings of the striatum. J Neurochem 115: 595-605. doi: 10.1111/j.1471-4159.2010.06950.x PMID: 20722968
43. Caligioni CS (2009) Assessing reproductive status/stages in mice. Current protocols in neuroscience Appendix 4: Appendix 4I.
44. Moy SS, Nadler JJ, Perez A, Barbaro RP, Johns JM, Magnuson TR, et al. (2004) Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav 3: 287-302. PMID: 15344922
45. Crawley JN (2007) Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol 17: 448-459. PMID: 17919130
46. Stowers L, Holy TE, Meister M, Dulac C, Koentges G (2002) Loss of sex discrimination and male-male aggression in mice deficient for TRP2. Science 295: 1493-1500. PMID: 11823606
47. Pankevich DE, Baum MJ, Cherry JA (2004) Olfactory sex discrimination persists, whereas the preference for urinary odorants from estrous females disappears in male mice after vomeronasal organ removal. J Neurosci 24: 9451-9457. PMID: 15496681
48. Leypold BG, Yu CR, Leinders-Zufall T, Kim MM, Zufall F, Axel R (2002) Altered sexual and social behaviors in trp2 mutant mice. Proc Natl Acad Sci U S A 99: 6376-6381. PMID: 11972034
49. Mandiyan VS, Coats JK, Shah NM (2005) Deficits in sexual and aggressive behaviors in Cnga2 mutant mice. Nat Neurosci 8: 1660-1662. PMID: 16261133
50. Dailly E, Chenu F, Petit-Demouliere B, Bourin M (2006) Specificity and efficacy of noradrenaline, serotonin depletion in discrete brain areas of Swiss mice by neurotoxins. J NeurosciMethods 150: 111-115. PMID: 16098600
51. Simon KR, Dos Santos RM, Scaini G, Leffa DD, Damiani AP, Furlanetto CB, et al. (2013) DNA damage induced by phenylalanine and its analogue p-chlorophenylalanine in blood and brain of rats subjected to a model of hyperphenylalaninemia. Biochem Cell Biol 91: 319-324. doi: 10.1139/bcb-2013-0023 PMID: 24032682
52. Hull EM, Dominguez JM (2007) Sexual behavior in male rodents. Horm Behav 52: 45-55. PMID: 17499249
53. Lichtensteiger W, Mutzner U, Langemann H (1967) Uptake of 5-hydroxytryptamine and 5-hydroxytryptophan by neurons of the central nervous system normally containing catecholamines. J Neurochem 14: 489-497. PMID: 5297947
54. Sanger GJ, Yoshida M, Yahyah M, Kitazumi K (2000) Increased defecation during stress or after 5-hydroxytryptophan: selective inhibition by the 5-HT(4) receptor antagonist, SB-207266. Br J Pharmacol 130: 706-712. PMID: 10821802
55. Bourin M, Hascoet M, Deguiral P (1996) 5-HTP induced diarrhea as a carcinoid syndrome model in mice? Fundam Clin Pharmacol 10: 450-457. PMID: 8902548
56. Hedge SS, Moy TM, Perry MR, Loeb M, Eglen RM (1994) Evidence for the involvement of 5-hydroxytryptamine 4 receptors in 5-hydroxytryptophan-induced diarrhea in mice. J Pharmacol Exp Ther 271: 741-747. PMID: 7965791
57. Angoa Perez M, Verbeem DM, Kane MJ, Sykes CE, Thomas DM, Kuhn DM (2010) Hypersensitive response to serotonin agonists and releasing drugs in TPH2 knockout mice. Neuroscience 2010 (SFN): 884.814.
58. Sloviter RS, Drust EG, Connor JD (1978) Specificity of a rat behavioral model for serotonin receptor activation. J Pharmacol Exp Ther 206: 339-347. PMID: 682117
59. Migliarini S, Pacini G, Pelosi B, Lunardi G, Pasqualetti M (2012) Lack of brain serotonin affects postnatal development and serotonergic neuronal circuitry formation. Mol Psychiatry. doi: 10.1038/mp.2012.176 PMID: 23247078
60. Waider J, Araragi N, Gutknecht L, Lesch KP (2011) Tryptophan hydroxylase-2 (TPH2) in disorders of cognitive control and emotion regulation: A perspective. Psychoneuroendocrinology 36: 393-405. doi: 10.1016/j.psyneuen.2010.12.012 PMID: 21257271
61. Jimenez-Trejo F, Tapia-Rodriguez M, Cerbon M, Kuhn DM, Manjarrez-Gutierrez G, Mendoza-Rodriguez CA, et al. (2012) Evidence of 5-HT components in human sperm: implications for protein tyrosine phosphorylation and the physiology of motility. Reproduction 144: 677-685. doi: 10.1530/REP-12-0145 PMID: 23028123
62. Fligny C, Hatia S, Amireault P, Mallet J, Cote F (2009) Mammalian prenatal development: the influence of maternally derived molecules. Bioessays 31: 935-943. doi: 10.1002/bies.200800217 PMID: 19644917
63. Amireault P, Dube F (2005) Serotonin and its antidepressant-sensitive transport in mouse cumulus-oocyte complexes and early embryos. Biol Reprod 73: 358-365. PMID: 15858217
64. Basu B, Desai R, Balaji J, Chaerkady R, Sriram V, Maiti S, et al. (2008) Serotonin in pre-implantation mouse embryos is localized to the mitochondria and can modulate mitochondrial potential. Reproduction 135: 657-669. doi: 10.1530/REP-07-0577 PMID: 18304982