Number of X-chromosome genes influences social behavior and vasopressin gene expression in mice

Psychoneuroendocrinology

Volumn 51, Issue , 2015, Pages 271-281

  Cox, Kimberly H ^a,c   Quinnies, Kayla M ^a   Eschendroeder, Alex ^a   Didrick, Paula M ^b   Eugster, Erica A ^b   Rissman, Emilie F ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Anxiety; Klinefelter syndrome; Sex differences; Sexual differentiation; Social anxiety; Social behavior; Turner syndrome

Indexed keywords

VASOPRESSIN; VASOPRESSIN DERIVATIVE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; CHILD; CLINICAL ARTICLE; CONDITIONED PLACE PREFERENCE TEST; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; FEMALE; GENE; GENE EXPRESSION; HUMAN; JUVENILE ANIMAL; KARYOTYPE 45,X; KARYOTYPE 47,XXY; MALE; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEX DIFFERENCE; SOCIAL BEHAVIOR; SOCIAL COGNITION; TURNER SYNDROME; VASOPRESSIN BLOOD LEVEL; X CHROMOSOME; ANIMAL; ANIMAL BEHAVIOR; BLOOD; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; X CHROMOSOMAL INHERITANCE;

AMYGDALA; ANIMALS; BEHAVIOR, ANIMAL; CHILD; FEMALE; GENE DOSAGE; GENE EXPRESSION REGULATION; GENES, X-LINKED; HUMANS; MALE; MICE; SOCIAL BEHAVIOR; TURNER SYNDROME; VASOPRESSINS; X CHROMOSOME;

EID: 84920576028     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.10.010     Document Type: Article

References (50)

1. Adolphs R. What does the amygdala contribute to social cognition?. Ann. N.Y. Acad. Sci. 2010, 1191:42-61.
2. Arnold A.P. The organizational-activational hypothesis as the foundation for a unified theory of sexual differentiation of all mammalian tissues. Horm. Behav. 2009, 55:570-578.
3. Auger C.J., Coss D., Auger A.P., Forbes-Lorman R.M. Epigenetic control of vasopressin expression is maintained by steroid hormones in the adult male rat brain. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4242-4247.
4. Berletch J.B., Yang F., Xu J., Carrel L., Disteche C.M. Genes that escape from X inactivation. Hum. Genet. 2011, 130:237-245.
5. Bielsky I.F., Hu S.B., Szegda K.L., Westphal H., Young L.J. Profound impairment in social recognition and reduction in anxiety-like behavior in vasopressin V1a receptor knockout mice. Neuropsychopharmacology 2004, 29:483-493.
6. Bonthuis P.J., Rissman E.F. Neural growth hormone implicated in body weight sex differences. Endocrinology 2013, 154(10):3826-3835.
7. Bowen M.T., McGregor I.S. Oxytocin and vasopressin modulate the social response to threat: a preclinical study. Int. J. Neuropsychopharmacol. 2014, 17(10):1621-1633.
8. Burgoyne P.S., Mahadevaiah S.K., Perry J., Palmer S.J., Ashworth A. The Y* rearrangement in mice: new insights into a perplexing PAR. Cytogenet. Cell Genet. 1998, 80:37-40.
9. Caldwell H.K., Lee H.J., Macbeth A.H., Young W.S. Vasopressin: behavioral roles of an "original" neuropeptide. Prog. Neurobiol. 2008, 84:1-24.
10. Chahrour M., Jung S.Y., Shaw C., Zhou X., Wong S.T., Qin J., Zoghbi H.Y. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science 2008, 320:1224-1229.
11. Cox K.H., Gatewood J.D., Howeth C., Rissman E.F. Gestational exposure to bisphenol A and cross-fostering affect behaviors in juvenile mice. Horm. Behav. 2010, 58:754-761.
12. Cox K.H., Rissman E.F. Sex differences in juvenile mouse social behavior are influenced by sex chromosomes and social context. Genes Brain Behav. 2011, 10:465-472.
13. Cox K.H., Bonthuis P.J., Rissman E.F. Mouse model systems to study sex chromosome genes and behavior: relevance to humans. Front. Neuroendocrinol. 2014, 35(4):405-419.
14. Egashira N., Tanoue A., Matsuda T., Koushi E., Harada S., Takano Y., Tsujimoto G., Mishima K., Iwasaki K., Fujiwara M. Impaired social interaction and reduced anxiety-related behavior in vasopressin V1a receptor knockout mice. Behav. Brain Res. 2007, 178:123-127.
15. Eicher E.M., Hale D.W., Hunt P.A., Lee B.K., Tucker P.K., King T.R., Eppig J.T., Washburn L.L. The mouse Y* chromosome involves a complex rearrangement, including interstitial positioning of the pseudoautosomal region. Cytogenet. Cell Genet. 1991, 57:221-230.
16. Forbes-Lorman R.M., Rautio J.J., Kurian J.R., Auger A.P., Auger C.J. Neonatal MeCP2 is important for the organization of sex differences in vasopressin expression. Epigenetics 2012, 7:230-238.
17. Gatewood J.D., Wills A., Shetty S., Xu J., Arnold A.P., Burgoyne P.S., Rissman E.F. Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice. J. Neurosci. 2006, 26:2335-2342.
18. Giarelli E., Wiggins L.D., Rice C.E., Levy S.E., Kirby R.S., Pinto-Martin J., Mandell D. Sex differences in the evaluation and diagnosis of autism spectrum disorders among children. Disabil. Health J. 2010, 3:107-116.
19. Isles A.R., Davies W., Burrmann D., Burgoyne P.S., Wilkinson L.S. Effects on fear reactivity in XO mice are due to haploinsufficiency of a non-PAR X gene: implications for emotional function in Turner's syndrome. Hum. Mol. Genet. 2004, 13:1849-1855.
20. Jessen H.M., Kolodkin M.H., Bychowski M.E., Auger C.J., Auger A.P. The nuclear receptor corepressor has organizational effects within the developing amygdala on juvenile social play and anxiety-like behavior. Endocrinology 2010, 151:1212-1220.
21. Kudwa A.E., Dominguez-Salazar E., Cabrera D.M., Sibley D.R., Rissman E.F. Dopamine D5 receptor modulates male and female sexual behavior in mice. Psychopharmacology (Berl) 2005, 180:206-214.
22. Kurian J.R., Forbes-Lorman R.M., Auger A.P. Sex difference in mecp2 expression during a critical period of rat brain development. Epigenetics 2007, 2:173-178.
23. Kurian J.R., Bychowski M.E., Forbes-Lorman R.M., Auger C.J., Auger A.P. Mecp2 organizes juvenile social behavior in a sex-specific manner. J. Neurosci. 2008, 28:7137-7142.
24. Lesniak-Karpiak K., Mazzocco M.M., Ross J.L. Behavioral assessment of social anxiety in females with Turner or fragile X syndrome. J. Autism Dev. Disord. 2003, 33:55-67.
25. Liu P.Y., Erkkila K., Lue Y., Jentsch J.D., Schwarcz M.D., Abuyounes D., Hikim A.S., Wang C., Lee P.W., Swerdloff R.S. Genetic, hormonal, and metabolomic influences on social behavior and sex preference of XXY mice. Am. J. Physiol. Endocrinol. Metab. 2010, 299:E446-E455.
26. Mann K.M., Ward J.M., Yew C.C., Kovochich A., Dawson D.W., Black M.A., Brett B.T., Sheetz T.E., Dupuy A.J., Chang D.K., Biankin A.V., Waddell N., Kassahn K.S., Grimmond S.M., Rust A.G., Adams D.J., Jenkins N.A., Copeland N.G. Sleeping Beauty mutagenesis reveals cooperating mutations and pathways in pancreatic adenocarcinoma. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:5934-5941.
27. Maxson S.C., Ginsburg B.E., Trattner A. Interaction of Y-chromosomal and autosomal gene(s) in the development of intermale aggression in mice. Behav. Genet. 1979, 9:219-226.
28. McFarlane H.G., Kusek G.K., Yang M., Phoenix J.L., Bolivar V.J., Crawley J.N. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 2008, 7:152-163.
29. Mortensen K.H., Andersen N.H., Gravholt C.H. Cardiovascular phenotype in Turner syndrome-integrating cardiology, genetics, and endocrinology. Endocr. Rev. 2012, 33:677-714.
30. Mosammaparast N., Shi Y. Reversal of histone methylation: biochemical and molecular mechanisms of histone demethylases. Annu. Rev. Biochem. 2010, 79:155-179.
31. Moy S.S., Nadler J.J., Perez A., Barbaro R.P., Johns J.M., Magnuson T.R., Piven J., Crawley J.N. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 2004, 3:287-302.
32. Murgatroyd C., Patchev A.V., Wu Y., Micale V., Bockmuhl Y., Fischer D., Holsboer F., Wotjak C.T., Almeida O.F., Spengler D. Dynamic DNA methylation programs persistent adverse effects of early-life stress. Nat. Neurosci. 2009, 12:1559-1566.
33. Nelson V.R., Spiezio S.H., Nadeau J.H. Transgenerational genetic effects of the paternal Y chromosome on daughters' phenotypes. Epigenomics 2010, 2:513-521.
34. Panksepp J.B., Lahvis G.P. Social reward among juvenile mice. Genes Brain Behav. 2007, 6:661-671.
35. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2004, Academic Press, San Diego, CA.
36. Raymond F.L. X linked mental retardation: a clinical guide. J. Med. Genet. 2006, 43:193-200.
37. Rood B.D., Stott R.T., You S., Smith C.J., Woodbury M.E., De Vries G.J. Site of origin of and sex differences in the vasopressin innervation of the mouse (Mus musculus) brain. J. Comp. Neurol. 2013, 521:2321-2358.
38. Russell H.F., Wallis D., Mazzocco M.M., Moshang T., Zackai E., Zinn A.R., Ross J.L., Muenke M. Increased prevalence of ADHD in Turner syndrome with no evidence of imprinting effects. J. Pediatr. Psychol. 2006, 31:945-955.
39. Seney M.L., Chang L.C., Oh H., Wang X., Tseng G.C., Lewis D.A., Sibille E. The role of genetic sex in affect regulation and expression of GABA-related genes across species. Front. Psychiatry 2013, 4:104.
40. Szot P., Dorsa D.M. Expression of vasopressin mRNA in extrahypothalamic nuclei of the homozygous Brattleboro rat is not modulated by testosterone. Neuroendocrinology 1993, 58:381-387.
41. Tejada L.D., Rissman E.F. Sex differences in social investigation: effects of androgen receptors, hormones and test partner. J. Neuroendocrinol. 2012.
42. Trolle C., Mortensen K.H., Hjerrild B.E., Cleemann L., Gravholt C.H. Clinical care of adult Turner syndrome-new aspects. Pediatr. Endocrinol. Rev. 2012, 9(Suppl. 2):739-749.
43. Tsai H.W., Grant P.A., Rissman E.F. Sex differences in histone modifications in the neonatal mouse brain. Epigenetics 2009, 4:47-53.
44. van Rijn S., Aleman A., Swaab H., Kahn R. Klinefelter's syndrome (karyotype 47,XXY) and schizophrenia-spectrum pathology. Br. J. Psychiatry 2006, 189:459-460.
45. Veenema A.H., Neumann I.D. Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog. Brain Res. 2008, 170:261-276.
46. Wolstenholme J.T., Goldsby J.A., Rissman E.F. Transgenerational effects of prenatal bisphenol A on social recognition. Horm. Behav. 2013, 64:833-839.
47. Wolstenholme J.T., Rissman E.F., Bekiranov S. Sexual differentiation in the developing mouse brain: contributions of sex chromosome genes. Genes Brain Behav. 2013, 12:166-180.
48. Xu J., Deng X., Disteche C.M. Sex-specific expression of the X-linked histone demethylase gene Jarid1c in brain. PLoS One 2008, 3:e2553.
49. Xu J., Deng X., Watkins R., Disteche C.M. Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons. J. Neurosci. 2008, 28:4521-4527.
50. Yang M., Perry K., Weber M.D., Katz A.M., Crawley J.N. Social peers rescue autism-relevant sociability deficits in adolescent mice. Autism Res. 2011, 4:17-27.