A sexually dimorphic area of the dorsal hypothalamus in mice and common marmosets

Endocrinology

Volumn 157, Issue 12, 2016, Pages 4817-4828

  Moe, Yadanar ^a   Kyi Tha Thu, Chaw ^a   Tanaka, Tomoko ^a   Ito, Hiroto ^a   Yahashi, Satowa ^b   Matsuda, Ken Ichi ^c   Kawata, Mitsuhiro ^c   Katsuura, Goro ^d   Iwashige, Fumihiro ^b   Sakata, Ichiro ^a   Akune, Atsushi ^b   Inui, Akio ^d   Sakai, Takafumi ^a   Ogawa, Sonoko ^e   Tsukahara, Shinji ^a  

^a SAITAMA UNIVERSITY   (Japan)

^b SHIN NIPPON BIOMEDICAL LABORATORIES LTD   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^d KAGOSHIMA UNIVERSITY   (Japan)

^e UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROSTANOLONE; CALBINDIN; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; GREEN FLUORESCENT PROTEIN; PROTEIN C FOS; TESTOSTERONE; ANDROGEN; ANDROGEN RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN NERVE CELL; CALLITHRIX JACCHUS; CELL DENSITY; CONTROLLED STUDY; DORSAL HYPOTHALAMUS; FEMALE; HYPOTHALAMUS; MALE; MATERNAL BEHAVIOR; MOUSE; NONHUMAN; ORCHIECTOMY; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECEPTOR BINDING; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; STRIA TERMINALIS; ANIMAL; CALLITHRIX; CELL COUNT; CYTOLOGY; DRUG EFFECTS; METABOLISM; NERVE CELL; PHYSIOLOGY; SEXUAL DEVELOPMENT;

ANDROGENS; ANIMALS; CALLITHRIX; CELL COUNT; DIHYDROTESTOSTERONE; FEMALE; HYPOTHALAMUS; MALE; MICE; NEURONS; ORCHIECTOMY; PROTO-ONCOGENE PROTEINS C-FOS; RECEPTORS, ANDROGEN; SEX CHARACTERISTICS; SEXUAL BEHAVIOR, ANIMAL; TESTOSTERONE;

EID: 85001907816     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2016-1428     Document Type: Article

References (57)

1. Gorski RA, Gordon JH, Shryne JE, Southam AM. Evidence for a morphological sex difference within the medial preoptic area of the rat brain. Brain Res. 1978;148(2):333-346.
2. Roselli CE, Larkin K, Resko JA, Stellflug JN, Stormshak F. The volume of a sexually dimorphic nucleus in the ovine medial preoptic area/anterior hypothalamus varies with sexual partner preference. Endocrinology. 2004;145(2):478-483.
3. Byne W. The medial preoptic and anterior hypothalamic regions of the rhesus monkey: cytoarchitectonic comparison with the human and evidence for sexual dimorphism. Brain Res. 1998;793(1-2): 346-350.
4. Allen LS, Hines M, Shryne JE, Gorski RA. Two sexually dimorphic cell groups in the human brain. J Neurosci. 19(2)89;9:497-506.
5. Swaab DF, Fliers E. A sexually dimorphic nucleus in the human brain. Science. 1985;228(4703):1112-1115.
6. Dominguez JM, Hull EM. Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav. 2005;86(3):356-368.
7. Stolzenberg DS, Numan M. Hypothalamic interaction with the mesolimbic DA system in the control of the maternal and sexual behaviors in rats. Neurosci Biobehav Rev. 2011;35(3):826-847.
8. Numan M, Stolzenberg DS. Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol. 2009;30(1): 46-64.
9. DeJonge FH, Louwerse AL,OomsMP,Evers P, Endert E, van de Poll NE. Lesions of the SDN-POA inhibit sexual behavior of male Wistar rats. Brain Res Bull. 1989;23(6):483-492.
10. Houtsmuller EJ, Brand T, de Jonge FH, Joosten RN, van de Poll NE, Slob AK. SDN-POA volume, sexual behavior, and partner preference of male rats affected by perinatal treatment with ATD. Physiol Behav. 1994;56(3):535-541.
11. Garcia-Falgueras A, Swaab DF. Asex difference in the hypothalamic uncinate nucleus: relationship to gender identity. Brain. 2008; 131(Pt 12):3132-3146.
12. LeVay S. A difference in hypothalamic structure between heterosexual and homosexual men. Science. 1991;253(5023):1034-1037.
13. Woodson JC, Gorski RA. Structural sex difference in the mammalian brain: reconsidering the male/female dichotomy. In: Matsumoto A, ed. Sexual Differentiation of the Brain. Boca Raton, FL: CRC Press LLC; 1999:229-255.
14. Sickel MJ, McCarthy MM. Calbindin-D28k immunoreactivity is a marker for a subdivision of the sexually dimorphic nucleus of the preoptic area of the rat: developmental profile and gonadal steroid modulation. J Neuroendocrinol. 2000;12(5):397-402.
15. Orikasa C,SakumaY. Estrogen configures sexual dimorphism in the preoptic area of C57BL/6J and ddN strains of mice. J Comp Neurol. 2010;518(17):3618-3629.
16. Edelmann M, Wolfe C, Scordalakes EM, Rissman EF, Tobet S. Neuronal nitric oxide synthase and calbindin delineate sex differences in the developing hypothalamus and preoptic area. Dev Neurobiol. 2007;67(10):1371-1381.
17. Gilmore RF, Varnum MM, Forger NG. Effects of blocking developmental cell death on sexually dimorphic calbindin cell groups in the preoptic area and bed nucleus of the stria terminalis. Biol Sex Differ. 2012;3:5.
18. Wittmann W, McLennan IS. Anti-Müllerian hormone may regulate the number of calbindin-positive neurons in the sexually dimorphic nucleus of the preoptic area of male mice. Biol Sex Differ. 2013; 4(1):18.
19. Maejima S, Ohishi N, Yamaguchi S, Tsukahara S. A neural connection between the central part of the medial preoptic nucleus and the bed nucleus of the stria terminalis to regulate sexual behavior in male rats. Neurosci Lett. 2015;606:66-71.
20. Wittmann W, McLennan IS. The bed nucleus of the stria terminalis has developmental and adult forms in mice, with the male bias in the developmental form being dependent on testicular AMH. Horm Behav. 2013;64(4):605-610.
21. Zhou JN, Hofman MA, Gooren LJ, Swaab DF. A sex difference in the human brain and its relation to transsexuality. Nature. 1995; 378(6552):68-70.
22. Kruijver FP, Zhou JN, Pool CW, Hofman MA, Gooren LJ, Swaab DF. Male-to-female transsexuals have female neuron numbers in a limbic nucleus. J Clin Endocrinol Metab. 2000;85(5):2034-2041.
23. Claro F, Segovia S, Guilamón A, Del Abril A. Lesions in the medial posterior region of the BST impair sexual behavior in sexually experienced and inexperienced male rats. Brain Res Bull. 1995;36(1): 1-10.
24. Numan M, Numan M. A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev Psychobiol. 1996;29(1):23-51.
25. McEwen BS, Lieberburg I, Chaptal C, Krey LC. Aromatization: important for sexual differentiation of the neonatal rat brain. Horm Behav. 19(3)77;9:249-263.
26. MacLusky NJ, Naftolin F. Sexual differentiation of the central nervous system. Science. 1981;211(4488):1294-1302.
27. Hisasue S, Seney ML, Immerman E, Forger NG. Control of cell number in the bed nucleus of the stria terminalis of mice: role of testosterone metabolites and estrogen receptor subtypes. J Sex Med. 2010;7(4 Pt 1):1401-1409.
28. Durazzo A, Morris JA, Breedlove SM, Jordan CL. Effects of the testicular feminization mutation (tfm) of the androgen receptor gene on BSTMPM volume and morphology in rats. Neurosci Lett. 2007; 419(2):168-171.
29. Allieri F, Spigolon G, Melcangi RC, et al. Androgen receptor deficiency alters the arginine-vasopressin sexually dimorphic system in Tfm rats. Neuroscience. 2013;253:67-77.
30. Kanaya M, Tsuda MC, Sagoshi S, et al. Regional difference in sex steroid action on formation of morphological sex differences in the anteroventral periventricular nucleus and principal nucleus of the bed nucleus of the stria terminalis. PLoS One. 2014;9(11):e112616.
31. Tsukahara S, Tsuda MC, Kurihara R, et al. Effects of aromatase or estrogen receptor gene deletion on masculinization of the principal nucleus of the bed nucleus of the stria terminalis of mice. Neuroendocrinology. 2011;94(2):137-147.
32. Simerly RB, Zee MC, Pendleton JW, Lubahn DB, Korach KS. Estrogen receptor-dependent sexual differentiation of dopaminergic neurons in the preoptic region of the mouse. Proc Natl Acad Sci USA. 1997;94(25):14077-14082.
33. Bodo C, Kudwa AE, Rissman EF. Both estrogen receptor and are required for sexual differentiation of the anteroventral periventricular area in mice. Endocrinology. 2006;147(1):415-420.
34. Matsuda KI, Yanagisawa M, Sano K, et al. Visualisation and characterisation of oestrogen receptor positive neurons expressing green fluorescent protein under the control of the oestrogen receptor promoter. Eur J Neurosci. 2013;38(2):2242-2249.
35. Kyi-Tha-Thu C, Okoshi K, Ito H, Matsuda K, Kawata M, Tsukahara S. Sex differences in cells expressing green fluorescent protein under the control of the estrogen receptor promoter in the hypothalamus of mice. Neurosci Res. 2015;101:44-52.
36. Franklin KBJ, Paxinos G. The Mouse Brain in Stereotaxic Coordinates. 3rd ed. Cambridge, MA: Academic Press; 2008.
37. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates. 2nd ed. Cambridge, MA: Academic Press; 2003.
38. Ogawa S, Washburn TF, Taylor J, Lubahn DB, Korach KS, Pfaff DW. Modifications of testosterone-dependent behaviors by estrogen receptor gene disruption in male mice. Endocrinology. 1998; 139(12):5058-5069.
39. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW. Roles of estrogen receptor gene expression in reproduction-related behaviors in female mice. Endocrinology. 1998;139(12):5070-5081.
40. Ogawa S, Lubahn DB, Korach KS, Pfaff DW. Behavioral effects of estrogen receptor gene disruption in male mice. Proc Natl Acad Sci USA. 1997;94(4):1476-1481.
41. Ogawa S, Taylor JA, Lubahn DB, Korach KS, Pfaff DW. Reversal of sex roles in genetic female mice by disruption of estrogen receptor gene. Neuroendocrinology. 1996;64(6):467-470.
42. Terasawa E, Wiegand SJ, Bridson WE. A role for medial preoptic nucleus on afternoon of proestrus in female rats. Am J Physiol. 1980;238(6):E533-E539.
43. Wiegand SJ, Terasawa E, Bridson WE. Persistent estrus and blockade of progesterone-inducedLHrelease follows lesions which do not damage the suprachiasmatic nucleus. Endocrinology. 1978;102(5): 1645-1648.
44. Ogawa S, Chan J, Chester AE, Gustafsson JA, Korach KS, PfaffDW. Survival of reproductive behaviors in estrogen receptor gene-deficient (-ERKO) male and female mice. Proc Natl Acad Sci USA. 1999;96(22):12887-12892.
45. Krege JH, Hodgin JB, Couse JF, et al. Generation and reproductive phenotypes of mice lacking estrogen receptor. Proc Natl Acad Sci USA. 1998;95(26):15677-15682.
46. Schulz KM, Molenda-Figueira HA, Sisk CL. Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav. 2009;55(5):597-604.
47. Juraska JM, Sisk CL, DonCarlos LL. Sexual differentiation of the adolescent rodent brain: hormonal influences and developmental mechanisms. Horm Behav. 2013;64(2):203-210.
48. Coolen LM, Peters HJ, Veening JG. Fos immunoreactivity in the rat brain following consummatory elements of sexual behavior: a sex comparison. Brain Res. 1996;738(1):67-82.
49. Pfaus JG, Marcangione C, Smith WJ, Manitt C, Abillamaa H. Differential induction of Fos in the female rat brain following different amounts of vaginocervical stimulation: modulation by steroid hormones. Brain Res. 1996;741(1-2):314-330.
50. Numan M, Corodimas KP, Numan MJ, Factor EM, Piers WD. Axon-sparing lesions of the preoptic region and substantia innominata disrupt maternal behavior in rats. Behav Neurosci. 1988;102(3): 381-396.
51. Tsuneoka Y,MaruyamaT, Yoshida S, et al. Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. J Comp Neurol. 2013;521(7):1633-1663.
52. Pfaff D, Waters E, Khan Q, Zhang X, Numan M. Minireview: estrogen receptor-initiated mechanisms causal to mammalian reproductive behaviors. Endocrinology. 2011;152(4):1209-1217.
53. Bridges RS. Neuroendocrine regulation of maternal behavior. Front Neuroendocrinol. 2015;36:178-196.
54. Numan M, Rosenblatt JS, Komisaruk BR. Medial preoptic area and onset of maternal behavior in the rat. JCompPhysiol Psychol. 1977; 91(1):146-164.
55. Ribeiro AC, Musatov S, Shteyler A, et al. siRNA silencing of estrogen receptor expression specifically in medial preoptic area neurons abolishes maternal care in female mice. Proc Natl Acad Sci USA. 2012;109(40):16324-16329.
56. Marmoset Genome Sequencing and Analysis Consortium. The common marmoset genome provides insight into primate biology and evolution. Nat Genet. 2014;46(8):850-857.
57. Kishi N, Sato K, Sasaki E, Okano H. Common marmoset as a new model animal for neuroscience research and genome editing technology. Dev Growth Differ. 2014;56(1):53-62.