Unexpected effects of perinatal gonadal hormone manipulations on sexual differentiation of the extrahypothalamic arginine-vasopressin system in prairie voles

Endocrinology

Volumn 146, Issue 3, 2005, Pages 1559-1567

  Lonstein, Joseph S ^a   Rood, Benjamin D ^b   De Vries, Geert J ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROSTANOLONE; ARGININE; ARGIPRESSIN; DIETHYLSTILBESTROL; ESTROGEN; MESSENGER RNA; SEX HORMONE; TAMOXIFEN; TESTOSTERONE PROPIONATE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CASTRATION; CELL COUNT; CONTROLLED STUDY; FEMALE; HABENULA; HORMONAL REGULATION; HORMONE ACTION; INJECTION; MALE; MASCULINITY; NEWBORN; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; RECEPTOR BLOCKING; REPRODUCTION; SEX DIFFERENCE; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; STRIA TERMINALIS; VOLE;

ANIMALS; ARGININE VASOPRESSIN; ARVICOLINAE; BODY WEIGHT; DIETHYLSTILBESTROL; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; GONADAL HORMONES; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; RATS; RNA, MESSENGER; SEX DIFFERENTIATION; SEX FACTORS; TAMOXIFEN; TESTOSTERONE; TESTOSTERONE PROPIONATE;

EID: 14244250616     PISSN: 00137227     EISSN: None     Source Type: Journal    
DOI: 10.1210/en.2004-1315     Document Type: Article

References (68)

1. Crenshaw BJ, De Vries GJ, Yahr P 1992 Vasopressin innervation of sexually dimorphic structures of the gerbil forebrain under various hormonal conditions. J Comp Neurol 322:589-598
2. De Vries GJ, Buijs RM, Swaab, DF 1981 Ontogeny of the vasopressinergic neurons of the suprachiasmatic nucleus and their extrahypothalamic projections in the rat brain-presence of a sex differences in the lateral septum. Brain Res 218:67-78
3. Boyd SK, Tyler CJ, De Vries GJ 1992 Sexual dimorphism in the vasotocin system of the bullfrog (Rana catesbeiana). J Comp Neurol 352:313-325
4. Panzica GC, Castagana C, Viglietti-Panzica C, Russo C, Tlemcani O, Balthazart J 1998 Organizational effects of estrogens on brain vasotocin and sexual behavior in quail. J Neurobiol 37:684-699
5. Foran CM, Bass AH 1999 Preoptic GnRH and AVP: axes for sexual plasticity in teleost fish. Gen Comp Endocrinol 116:141-152
6. Moore RL, Richardson C, Lowry CA 2000 Sexual dimorphism in numbers of vasotocin-immunoreactive neurons in brain areas associated with reproductive behaviors in the roughskin newt. Gen Comp Endocrinol 117:281-298
7. Miller M, De Vries GJ 1998 Anatomy and function of extrahypothalamic vasopressin systems in the brain. Prog Brain Res 119:3-20
8. De Vries GJ 1990 Sex differences in neurotransmitter systems. J Neuroendocrinol 2:1-13
9. Yahr P 1988 Sexual differentiation of behavior in the context of developmental psychobiology. In: Blass EM, ed. Handbook of behavioral neurobiology. Vol 9. New York: Plenum; 197-243
10. Cooke BM, Hegstrom CD, Villeneuve LS, Breedlove MS 1998 Sexual differentiation of the vertebrate brain: principles and mechanisms. Front Neuroendocrinol 19:323-362
11. Forger NG 2001 The development of sex differences in the nervous system. In: Blass EM, ed. Handbook of behavioral neurobiology. Vol 12. New York: Plenum; 153-208
12. Wang Z, Bullock NA, De Vries GJ 1993 Sexual differentiation of vasopressin projection of the bed nucleus of the stria terminalis and medial amygdaloid nucleus in rats. Endocrinology 132:2299-2306
13. Wang Z 1994 Testosterone effects on development of vasopressin messenger RNA expression in the bed nucleus of the stria terminalis and medial amygdaloid nucleus in male rats. Brain Res Dev Brain Res 79:147-150
14. Han T, De Vries GJ 2003 Organizational effects of testosterone, estradiol, and dihydrotestosterone on vasopressin mRNA expression in the bed nucleus of the stria terminalis. J Neurobiol 54:502-510
15. Buijs RM, Pevet P, Masson-Pevet M, Pool CW, De Vries GJ, Canguilhem B, Vivien-Roels B 1986 Seasonal variation in vasopressin innervation in the brain of the European hamster (Cricetus cricetus). Brain Res 371:193-196
16. Hermes ML, Buijs RM, Masson-Pevet M, Pevet P 1990 Seasonal changes in vasopressin in the brain of the garden dormouse (Eliomys quercinus L.). J Comp Neurol 293:340-346
17. Bamshad M, Novak MA, De Vries GJ 1993 Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus. J Neuroendocrinol 5:247-255
18. Wang Z, Smith W, Major DE, De Vries GJ 1994 Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Brain Res 650:212-218
19. 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 sexual dimorphic neural and behavioral traits. J Neurosci 22:9005-9014
20. Baum MJ 1979 Differentiation of coital behavior in mammals: a comparative analysis. Neurosci Biobehav Rev 3:265-284
21. Carter CS, De Vries AC, Getz LL 1995 Physiological substrates of mammalian monogamy: the prairie vole model. Neurosci Biobehav Rev 19:303-314
22. Pfaff DW, Zigmond RE 1971 Neonatal androgen effects on sexual and nonsexual behavior of adult rats tested under various hormone regimes. Neuroendocrinology 7:129-145
23. Roberts RL, Zullo AS, Carter CS 1997 Sexual differentiation in prairie voles: the effects of corticosterone and testosterone. Physiol Behav 62:1379-1383
24. Smale L, Nelson RJ, Zucker I 1985 Neuroendocrine responsiveness to oestradiol and male urine in neonatally androgenized prairie voles (Microtus ochrogaster). J Reprod Fertil 74:491-496
25. Lonstein JS, De Vries GJ 2000 Influence of gonadal hormones in the development of parental behavior in adult virgin prairie voles (Microtus ochrogaster). Behav Brain Res 114:79-87
26. Lonstein JS, Rood BD, De Vries GJ 2002 Parental responsiveness is feminized after neonatal castration in virgin male prairie voles, but is not masculinized by perinatal testosterone in virgin females. Horm Behav 41:80-87
27. Wang Z, De Vries GJ 1993 Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res 631:156-160
28. Lonstein JS, De Vries GJ 2000 Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 24:669-686
29. Lonstein JS, De Vries GJ 1999 Sex differences in the parental behaviour of adult virgin prairie voles: independence from gonadal hormones and vasopressin. J Neuroendocrinol 11:441-449
30. Paxinos G, Watson 1998 The rat brain in stereotaxic coordinates. 4th ed. New York: Academic Press
31. Simerly RB 1990 Hormonal control of neuropeptide gene expression in sexually dimorphic olfactory pathways. Trends Neurosci 13:104-110
32. Breedlove SM, Cooke BM, Jordan CL 1999 The orthodox view of brain sexual differentiation. Brain Behav Evol 54:8-14
33. Cooke BM, Chowanadisai W, Breedlove SM 2000 Post-weaning social isolation of male rats reduces the volume of the medial amygdala and leads to deficits in adult sexual behavior. Behav Brain Res 117:107-113
34. Cooke BM, Tabibnia G, Breedlove SM 1999 A brain sexual dimorphism controlled by adult circulating androgens. Proc Natl Acad Sci USA 96:7538-7540
35. Becu-Villalobos D, Gonzalez Iglesias A, Diaz-Torga G, Hockl P, Libertun C 1997 Brain sexual differentiation and gonadotropins secretion in the rat. Cell Mol Neurobiol 17:699-715
36. Jacobson CD, Csernus VJ, Shryne JE, Gorski RA 1981 The influence of gonadectomy, androgen exposure, or a gonadal graft in the neonatal rat on the volume of the sexually dimorphic nucleus of the preoptic area. J Neurosci 1:1142-1147
37. Del Abril A, Segovia S, Guillamon A 1987 The bed nucleus of the stria terminalis in the rat: regional sex differences controlled by gonadal steroids early after birth. Brain Res 429:295-300
38. Fitch RH, Cowell PE, Schrott LM, Denenberg VH 1991 Corpus callosum: demasculinization via perinatal anti-androgen. Int J Dev Neurosci 9:35-38
39. Nunez JL, Jurgens HA, Juraska JM 2000 Androgens reduce cell death in the developing rat visual cortex. Dev Brain Res 125:83-88
40. Vinader-Caerols C, Callado P, Segovia S, Guillamon A 2000 Estradiol masculinizes the posteromedial cortical nucleus of the amygdala in the rat. Brain Res Bull 53:269-273
41. Bakker J, Pool CW, Sonnemans M, Van Leeuwen FW, Slob AK 1997 Quantitative estimation of estrogen and androgen receptor-immunoreactive cells in the forebrain of neonatally estrogen-deprived male rats. Neuroscience 77:911-919
42. McAbee MD, DonCarlos LL 1999 Estrogen, but not androgens, regulates androgen receptor messenger ribonucleic acid expression in the developing male rat forebrain. Endocrinology 140:3674-3681
43. Quadros PS, Goldstein AY, De Vries GJ, Wagner CK 2002 Regulation of sex differences in progesterone receptor expression in the medial preoptic nucleus of postnatal rats. J Neuroendocrinol 14:761-767
44. Simerly RB, Swanson LW, Gorski RA 1985 Reversal of the sexually dimorphic distribution of serotonin-immunoreactive fibers in the medial preoptic nucleus by treatment with perinatal androgen. Brain Res 340:91-98
45. Simerly RB 1989 Hormonal control of the development and regulation of tyrosine hydroxylase expression within a sexually dimorphic population of dopaminergic cells in the hypothalamus. Brain Res Mol Brain Res 6:297-310
46. Siddiqui A, Shah BH 1997 Neonatal androgen manipulation differentially affects the development of monoamine systems in rat cerebral cortex, amygdala and hypothalamus. Dev Brain Res 98:247-252
47. Davis AM, Ward SC, Selmanoff M, Herbison AE, McCarthy MM 1999 Developmental sex differences in amino acid neurotransmitter levels in hypothalamic and limbic areas of rat brain. Neuroscience 90:1471-1482
48. De Vries GJ, Best W, Sluiter AA 1983 The influence of androgens on the development of a sex differences in the vasopressinergic innervation of the rat lateral septum. Brain Res 284:377-380
49. Petersen SL 1986 Perinatal androgen manipulations do not affect feminine behavioral potentials in voles. Physiol Behav 36:527-531
50. Wekesa KS, Vandenbergh JG 1996 Androgen exposure and reproductive behavior in an induced ovulator, the pine vole (Microtus pinetorum). Horm Behav 30:416-423
51. Wallin K, Baum MJ 2002 Masculinization and defeminization in altricial and precocial mammals: comparative aspects of steroid hormone action. In: Pfaff DW, Arnold AP, Etgen AM, Fahrbach SE, Rubin RT, eds. Hormones, brain, and behavior. Vol 4. New York: Academic Press; 385-424
52. Szot P, Dorsa DM 1993 Differential timing and sexual dimorphism in the expression of vasopressin gene in the developing rat brain. Dev Brain Res 73:177-183
53. Krukenberg SM, Gier HT, Dennis SM 1973 Postnatal development of the prairie vole, Microtus ochrogaster. Lab Arum Sci 23:53-55
54. Salo AL, Shapiro LE, Dewsbury DA 1994 Comparisons of nipple attachment and incisor growth among four species of voles (Microtus). Dev Psychobiol 27:317-330
55. Wang Z, Novak MA 1994 Alloparental care and the influence of father presence on juvenile prairie voles, Microtus ochrogaster. Anim Behav 47:281-288
56. DonCarlos LL, McAbee M, Ramer-Quinn DS, Stancik DM 1995 Estrogen receptor mRNA levels in the preoptic area of neonatal rats are responsive to hormone manipulation. Dev Brain Res 84:253-260
57. Lisciotto CA, Morrell JI 1993 Circulating gonadal steroid hormones regulate estrogen receptor mRNA in the male rat forebrain. Brain Res Mol Brain Res 20:79-90
58. Faber KA, Ayyash L, Dixon S, Hughes CL 1993 Effect of neonatal diethylstilbestrol exposure on volume of the sexually dimorphic nucleus of the preoptic area and pituitary responsiveness to gonadotropin-releasing hormone in female rats of known anogenital distance at birth. Biol Reprod 48:947-951
59. Morgan LR, Hite RF, Cushing BS 1997 Exposure to male siblings facilitates the response to estradiol in sexually naive female prairie voles. Physiol Behav 61:955-956
60. Wang Z, De Vries GJ 1995 Androgen and estrogen effects on vasopressin messenger RNA expression in the medial amygdaloid nucleus in male and female rats. J Neuroendocrinology 7:827-831
61. Al-Shamma HA, De Vries GJ 1996 Neurogenesis of the sexually dimorphic vasopressin cells of the bed nucleus of the stria terminalis and amygdala of rats. J Neurobiol 29:91-98
62. De Vries GJ, Al-Shamma HA 1990 Sex differences in hormonal responses of vasopressin pathways in the rat brain. J Neurobiol 21:686-693
63. Brown NM, Setchell KD 2001 Animal models impacted by phytoestrogens in commercial chow: implications for pathways influenced by hormones. Lab Invest 81:735-747
64. Masutomi N, Shibutani M, Takagi H, Uneyama C, Takahashi N, Hirose M 2003 Impact of dietary exposure to methoxychlor, genistein, or diisononyl phthalate during the perinatal period on the development of the rat endocrine/reproductive systems in later life. Toxicology 192:149-170
65. Thigpen JE, Haseman JK, Saunders HE, Setchell KD, Grant MG, Forsythe DB 2003 Dietary phytoestrogens accelerate the time of vaginal opening in immature CD-1 mice. Comp Med 53:607-615
66. Faber KA, Hughes CL 1993 Dose-response characteristics of neonatal exposure to genistein on pituitary responsiveness to gonadotropin releasing hormone and volume of the sexually dimorphic nucleus of the preoptic area (SDN-POA) in postpubertal castrated female rats. Reprod Toxicol 7:35-39
67. Weber KS, Setchell KD, Lephart ED 2001 Maternal and perinatal brain aromatase: effects of dietary soy phytoestrogens. Brain Res Dev Brain Res 126:217-221
68. Bilinska B, Schmalz-Fraczek B, Kotula M, Carreau S 2001 Photoperiod-dependent capability of androgen aromatization and the role of estrogen in the bank vole testis visualized by means of immunohistochemistry. Mol Cell Endocrinol 178:189-198