Sex chromosome complement and gonadal sex influence aggressive and parental behaviors in mice

Journal of Neuroscience

Volumn 26, Issue 8, 2006, Pages 2335-2342

  Gatewood, Jessica D ^a   Wills, Aileen ^a   Shetty, Savera ^b   Xu, Jun ^b   Arnold, Arthur P ^b   Burgoyne, Paul S ^c   Rissman, Emilie F ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

Aggression; Autism; Klinefelter syndrome; Parental behavior; Sex chromosomes; Vasopressin

Indexed keywords

AGGRESSIVENESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GONAD DEVELOPMENT; IMMUNOREACTIVITY; KARYOTYPE 46,XX; MALE; MOUSE; NONHUMAN; PARENTAL BEHAVIOR; PRIORITY JOURNAL; SEX CHROMOSOME; SEX DIFFERENCE; SOCIAL BEHAVIOR; SRY GENE; TRANSGENIC ANIMAL; AGGRESSION; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; EXPLORATORY BEHAVIOR; GENDER AND SEX; PARENT; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; REPRODUCTION; SEXUAL DEVELOPMENT; TRANSGENIC MOUSE;

AGGRESSION; ANIMALS; BEHAVIOR, ANIMAL; EXPLORATORY BEHAVIOR; GENES, SRY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PARENTS; SEX CHARACTERISTICS; SEX CHROMOSOMES; SEX DETERMINATION (GENETICS); SEX REVERSAL, GONADAL; SOCIAL BEHAVIOR;

EID: 33645634696     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3743-05.2006     Document Type: Article

References (62)

1. Agate RJ, Grisham W, Wade J, Mann S, Wingfield J, Schanen C, Palotie A, Arnold AP (2003) Neural, not gonadal, origin of brain sex differences in a gynandromorphic finch. Proc Natl Acad Sci USA 100:4873-4878.
2. Arnold AP (2004) Sex chromosomes and brain gender. Nat Rev Neurosci 5:701-708.
3. Arnold AP, Gorski RA (1984) Gonadal steroid induction of structural sex differences in the central nervous system. Annu Rev Neurosci 7:413-442.
4. Arnold AP, Rissman EF, De Vries GJ (2003) Two perspectives on the origin of sex differences in the brain. Ann NY Acad Sci 1007:176-188.
5. Bester-Meredith JK, Young LJ, Marler CA (1999) Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm Behav 36:25-38.
6. Burgoyne PS (1989) Genetics of XX and XO sex reversal in the mouse. In: Evolutionary mechamisms of sex determination. (Wachtel S, ed), pp 161-169. Boca Raton, FL: CRC.
7. Carlier M, Roubertoux PL, Kottler ML, Degrelle H (1990) Y chromosome and aggression in strains of laboratory mice. Behav Genet 20:137-156.
8. Carruth LL, Reisert I, Arnold AP (2002) Sex chromosome genes directly affect brain sexual differentiation. Nat Neurosci 5:933-934.
9. Compaan JC, Buijs RM, Pool CW, De Ruiter AJ, Koolhaas JM (1993) Differential lateral septal vasopressin innervation in aggressive and nonaggressive male mice. Brain Res Bull 30:1-6.
10. Davies W, Isles A, Smith R, Karunadasa D, Burrmann D, Humby T, Ojarikre O, Biggin C, Skuse D, Burgoyne P, Wilkinson L (2005) Xlr3b is a new imprinted candidate for X-linked parent-of-origin effects on cognitive function in mice. Nat Genet 37:625-629.
11. De Vries GJ, Rissman EF, Simerly RB, Yang LY, Scordalakes EM, Auger CJ, Swain A, Lovell-Badge R, Burgoyne PS, Arnold AP (2002) A model system for study of sex chromosome effects on sexually dimorphic neural and behavioral traits. J Neurosci 22:9005-9014.
12. Dewing P, Shi T, Horvath S, Vilain E (2003) Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res Mol Brain Res 118:82-90.
13. Dominguez-Salazar E, Bateman HL, Rissman EF (2004) Background matters: the effects of estrogen receptor alpha gene disruption on male sexual behavior are modified by background strain. Horm Behav 46:482-490.
14. Franklin KBL, Paxinos G (1997) The mouse brain in stereotaxic coordinates. New York: Academic.
15. Gandelman R, Vom Saal FS (1975) Pup-killing in mice: the effects of gonadectomy and testosterone administration. Physiol Behav 15:647-651.
16. Gubbay J, Vivian N, Economou A, Jackson D, Goodfellow P, Lovell-Badge R (1992) Inverted repeat structure of the Sry locus in mice. Proc Natl Acad Sci USA 89:7953-7957.
17. Guillot PV, Carlier M, Maxson SC, Roubertoux PL (1995) Intermale aggression tested in two procedures, using four inbred strains of mice and their reciprocal congenics: Y chromosomal implications. Behav Genet 25:357-360.
18. Imwalle DB, Scordalakes EM, Rissman EF (2002) Estrogen receptor alpha influences socially motivated behaviors. Horm Behav 42:484-491.
19. Isles AR, Davies W, Burrmann D, Burgoyne PS, Wilkinson LS (2004) 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 13:1849-1855.
20. Jamain S, Quach H, Betancur C, Rastam M, Colineaux C, Gillberg IC, Soderstrom H, Giros B, Leboyer M, Gillberg C, Bourgeron T (2003) Mutations of the X-linked genes encoding neuroligins NLGN3 and NLGN4 are associated with autism. Nat Genet 34:27-29.
21. Kau AS, Tierney E, Bukelis I, Stump MH, Kates WR, Trescher WH, Kaufmann WE (2004) Social behavior profile in young males with fragile X syndrome: characteristics and specificity. Am J Med Genet A 126:9-17.
22. Kaufmann WE, Cortell R, Kau AS, Bukelis I, Tierney E, Gray RM, Cox C, Capone GT, Stanard P (2004) Autism spectrum disorder in fragile X syndrome: communication, social interaction, and specific behaviors. Am J Med Genet A 129:225-234.
23. Lahr G, Maxson SC, Mayer A, Just W, Pilgrim C, Reisert I (1995) Transcription of the Y chromosomal gene, Sry, in adult mouse brain. Brain Res Mol Brain Res 33:179-182.
24. Le Roy I, Mortaud S, Tordjman S, Donsez-Darcel E, Carlier M, Degrelle H, Roubertoux PL (1999) Genetic correlation between steroid sulfatase concentration and initiation of attack behavior in mice. Behav Genet 29:131-136.
25. Lovell-Badge R, Robertson E (1990) XY female mice resulting from a heritable mutation in the primary testis-determining gene, Tdy. Development 109:635-646.
26. Lue Y, Jentsch JD, Wang C, Rao PN, Sinha Hikim AP, Salameh W, Swerdloff RS (2005) XXY mice exhibit gonadal and behavioral phenotypes similar to Klinefelter syndrome. Endocrinology 146:4148-4154.
27. Mahadevaiah SK, Lovell-Badge R, Burgoyne PS (1993) Tdy-negative XY, XXY and XYY female mice: breeding data and synaptonemal complex analysis. J Reprod Fertil 97:151-160.
28. Mahadevaiah SK, Odorisio T, Elliott DJ, Rattigan A, Szot M, Laval SH, Washburn LL, McCarrey JR, Cattanach BM, Lovell-Badge R, Burgoyne PS (1998) Mouse homologues of the human AZF candidate gene RBM are expressed in spermatogonia and spermatids, and map to a Y chromosome deletion interval associated with a high incidence of sperm abnormalities. Hum Mol Genet 7:715-727.
29. Markham JA, Jurgens HA, Auger CJ, De Vries GJ, Arnold AP, Juraska JM (2003) Sex differences in mouse cortical thickness are independent of the complement of sex chromosomes. Neuroscience 116:71-75.
30. Maxson SC (1996) Issues in the search for candidate genes in mice as potential animal models of human aggression. Ciba Found Symp 194:21-30; discussion 30-35.
31. Mayer A, Mosler G, Just W, Pilgrim C, Reisert I (2000) Developmental profile of Sry transcripts in mouse brain. Neurogenetics 3:25-30.
32. Meek LR, Dittel PL, Sheehan MC, Chan JY, Kjolhaug SR (2001) Effects of stress during pregnancy on maternal behavior in mice. Physiol Behav 72:473-479.
33. Miczek KA, Maxson SC, Fish EW, Faccidomo S (2001) Aggressive behavioral phenotypes in mice. Behav Brain Res 125:167-181.
34. Mortaud S, Donsez-Darcel E, Roubertoux PL, Degrelle H (1996) Murine steroid sulfatase gene expression in the brain during postnatal development and adulthood. Neurosci Lett 215:145-148.
35. Palaszynski KM, Smith DL, Kamrava S, Burgoyne PS, Arnold AP, Voskuhl RR (2005) A yin-yang effect between sex chromosome complement and sex hormones on the immune response. Endocrinology146:3280-3285.
36. Petit E, Herault J, Raynaud M, Cherpi C, Perrot A, Barthelemy C, Lelord G, Muh JP (1996) X chromosome and infantile autism. Biol Psychiatry 40:457-464.
37. Pilgrim C, Beyer C, Reisert I (1999) The effects of sex and sex hormones on the development of dopaminergic neurons. In: Development of dopaminergic neurons (Di Porzio U, Pernas-Alonso R, Perrone-Capano C, eds), pp 75-86. Austin, TX: R.G. Landes.
38. Raefski AS, O'Neill MJ (2005) Identification of a cluster of X-linked imprinted genes in mice. Nat Genet 37:620-624.
39. Reisert I, Karolczak M, Beyer C, Just W, Maxson SC, Ehret G (2002) Sry does not fully sex-reverse female into male behavior towards pups. Behav Genet 32:103-111.
40. Roubertoux PL, Carlier M (1988) Differences between CBA/H and NZB mice on intermale aggression. II. Maternal effects. Behav Genet 18:175-184.
41. Roubertoux PL, Carlier M, Degrelle H, Haas-Dupertuis MC, Phillips J, Moutier R (1994) Co-segregation of intermale aggression with the pseudoautosomal region of the Y chromosome in mice. Genetics 136:225-230.
42. Rowe FA, Edwards DA (1971) Olfactory bulb removal: influences on the aggressive behaviors of male mice. Physiol Behav 7:889-892.
43. Scordalakes EM, Rissman EF (2003) Aggression in male mice lacking functional estrogen receptor alpha. Behav Neurosci 117:38-45.
44. Scordalakes EM, Rissman EF (2004) Aggression and arginine vasopressin immunoreactivity regulation by androgen receptor and estrogen receptor alpha. Genes Brain Behav 3:20-26.
45. Selmanoff MK, Jumonville JE, Maxson SC, Ginsburg BE (1975) Evidence for a Y chromosomal contribution to an aggressive phenotype in inbred mice. Nature 253:529-530.
46. Selmanoff MK, Maxson SC, Ginsburg BE (1976) Chromosomal determinants of intermale aggressive behavior in inbred mice. Behav Genet 6:53-69.
47. Shrenker P, Maxson SC (1982) The Y chromosomes of DBA/1Bg and DBA/2Bg compared for effects on intermale aggression. Behav Genet 12:429-434.
48. Simpson EM, Linder CC, Sargent EE, Davisson MT, Mobraaten LE, Sharp JJ (1997) Genetic variation among 129 substrains and its importance for targeted mutagenesis in mice. Nat Genet 16:19-27.
49. Skuse DH, James RS, Bishop DV, Coppin B, Dalton P, Aamodt-Leeper G, Bacarese-Hamilton M, Creswell C, McGurk R, Jacobs PA (1997) Evidence from Turner's syndrome of an imprinted X-linked locus affecting cognitive function. Nature 387:705-708.
50. Sluyter F, van Oortmerssen GA, de Ruiter AJ, Koolhaas JM (1996) Aggression in wild house mice: current state of affairs. Behav Genet 26:489-496.
51. Stavnezer AJ, McDowell CS, Hyde LA, Bimonte HA, Balogh SA, Hoplight BJ, Denenberg VH (2000) Spatial ability of XY sex-reversed female mice. Behav Brain Res 112:135-143.
52. Svare B, Mann M (1981) Infanticide: genetic, developmental and hormonal influences in mice. Physiol Behav 27:921-927.
53. Svare B, Bartke A, Gandelman R (1977) Individual differences in the maternal behavior of male mice: no evidence for a relationship to circulating testosterone levels. Horm Behav 8:372-376.
54. Taketo T, Saeed J, Nishioka Y, Donahoe PK (1991) Delay of testicular differentiation in the B6.YDOM ovotestis demonstrated by immunocytochemical staining for mullerian inhibiting substance. Dev Biol 146:386-395.
55. Thomas NS, Sharp AJ, Browne CE, Skuse D, Hardie C, Dennis NR (1999) Xp deletions associated with autism in three females. Hum Genet 104:43-48.
56. Turner JM, Mahadevaiah SK, Benavente R, Offenberg HH, Heyting C, Burgoyne PS (2000) Analysis of male meiotic "sex body" proteins during XY female meiosis provides new insights into their functions. Chromosoma 109:426-432.
57. Van Oortmerssen GA, Sluyter F (1994) Studies on wild house mice. V. Aggression in lines selected for attack latency and their Y-chromosomal congenics. Behav Genet 24:73-78.
58. Vawter MP, Evans S, Choudary P, Tomita H, Meador-Woodruff J, Molnar M, Li J, Lopez JF, Myers R, Cox D, Watson SJ, Akil H, Jones EG, Bunney WE (2004) Gender-specific gene expression in post-mortem human brain: localization to sex chromosomes. Neuropsychopharmacology 29:373-384.
59. Wagner CK, Xu J, Pfau JL, Quadros PS, De Vries GJ, Arnold AP (2004) Neonatal mice possessing an Sry transgene show a masculinized pattern of progesterone receptor expression in the brain independent of sex chromosome status. Endocrinology 145:1046-1049.
60. Wang Z, Young LJ, De Vries GJ, Insel TR (1998) Voles and vasopressin: a review of molecular, cellular, and behavioral studies of pair bonding and paternal behaviors. Prog Brain Res 119:483-499.
61. Wersinger SR, Ginns EI, O'Carroll AM, Lolait SJ, Young III WS (2002) Vasopressin V1b receptor knockout reduces aggressive behavior in male mice. Mol Psychiatry 7:975-984.
62. Xu J, Burgoyne PS, Arnold AP (2002) Sex differences in sex chromosome gene expression in mouse brain. Hum Mol Genet 11:1409-1419.