Prenatal testosterone supplementation alters puberty onset, aggressive behavior, and partner preference in adult male rats

Journal of Physiological Sciences

Volumn 62, Issue 2, 2012, Pages 123-131

  Dela Cruz, Cynthia ^a   Pereira, Oduvaldo C M ^b  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

Aggressive behavior; Male rats; Prenatal testosterone; Puberty onset; Sexual behavior; Sexual differentiation

Indexed keywords

TESTOSTERONE; TESTOSTERONE PROPIONATE;

AGGRESSION; ANIMAL; ANIMAL MODEL; ARTICLE; BLOOD; DRUG EFFECT; FEMALE; GESTATIONAL AGE; MALE; PATHOPHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; PSYCHOLOGICAL ASPECT; RAT; SEX DIFFERENTIATION; SEXUAL BEHAVIOR; SEXUAL MATURATION; SOCIAL BEHAVIOR; WISTAR RAT;

AGGRESSION; ANIMALS; FEMALE; GESTATIONAL AGE; MALE; MODELS, ANIMAL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, WISTAR; SEX DIFFERENTIATION; SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION; SOCIAL BEHAVIOR; TESTOSTERONE; TESTOSTERONE PROPIONATE;

EID: 84860750190     PISSN: 18806546     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12576-011-0190-7     Document Type: Article

References (46)

1. Greene RR, Burrill MW, Ivy AC (1938) Experimental intersexuality: the production of feminized male rats by antenatal treatment with estrogens. Science 88(2275):130-131
2. Huffman L, Hendricks SE (1981) Prenatally injected testosterone propionate and sexual behavior of female rats. Physiol Behav 26(5):773-778 (Pubitemid 11048805)
3. Slob AK, den Hamer R, Woutersen PJA, van der Werff JJ (1983) Prenatal testosterone propionate and postnatal ovarian activity in the rat. Acta Endocrinol 103:420-427 (Pubitemid 13060447)
4. Rhees RW, Kirk BA, Sephton S, Lephart ED (1997) Effects of prenatal testosterone on sexual behavior, reproductive morphology and LH secretion in the female rat. Dev Neurosci 19(5): 430-437 (Pubitemid 27389058)
5. Wolf CJ, Hotchkiss A, Ostby JS, LeBlanc GA, Earl Gray Jr L (2002) Effects of prenatal testosterone propionate on the sexual development of male and female rats: a dose-response study. Toxicol Sci 65(1):71-86 (Pubitemid 34092692)
6. Blank SK, McCartney CR, Marshall JC (2006) The origins and sequelae of abnormal neuroendocrine function in polycystic ovary syndrome. Hum Reprod Update 12(4):351-361 (Pubitemid 43923410)
7. Sir-Petermann T, Maliqueo M, Angel B, Lara HE, Perez-Bravo F, Recabarren SE (2002) Maternal serum androgens in pregnant women with polycystic ovarian syndrome: possible implications in prenatal androgenization. Hum Reprod 17(10):2573-2579 (Pubitemid 35174106)
8. Otten BJ, Stikkelbroeck MM, Claahsen-van der Grinten HL, Hermes AR (2005) Puberty and fertility in congenital adrenal hyperplasia. Endocr Dev 8:54-66
9. Morris JA, Jordan CL, Breedlove SM (2004) Sexual differentiation of the vertebrate nervous system. Nat Neurosci 7(10):1034-1039 (Pubitemid 41184441)
10. Naftolin F, Ryan KJ, Davies IJ, Petro Z, Kuhn M (1975) The formation and metabolism of estrogens in brain tissues. Adv Biosci 15:105-121
11. Zuloaga DG, Puts DA, Jordan CL, Breedlove SM (2008) The role of androgen receptors in the masculinization of brain and behavior: what we've learned from the testicular feminization mutation. Horm Behav 53(5):613-626
12. Trainor BC, Kyomen HH, Marler CA (2006) Estrogenic encounters: how interactions between aromatase and the environment modulate aggression. Front Neuroendocrinol 27(2):170-179 (Pubitemid 43947165)
13. Corbier P, Edwards DA, Roffi J (1992) The neonatal testosterone surge: a comparative study. Arch Int Physiol Biochim Biophys 100(2):127-131
14. Hoepfner BA, Ward IL (1988) Prenatal and neonatal androgen exposure interact to affect sexual differentiation in female rats. Behav Neurosci 102(1):61-65
15. Piacsek BE, Hostetter MW (1984) Neonatal androgenization in the male rat: evidence for central and peripheral defects. Biol Reprod 30(2):344-351 (Pubitemid 14144459)
16. Book AS, Starzyk KB, Quinsey VL (2001) The relationship between testosterone and aggression: a meta-analysis. Aggress Viol Behav 6(6):579-599 (Pubitemid 33108977)
17. Giammanco M, Tabacchi G, Giammanco S, Di Majo D, La Guardia M (2005) Testosterone and aggressiveness. Med Sci Monit 11(4):RA 136-RA 145 (Pubitemid 40546961)
18. Weisz J, Ward IL (1980) Plasma testosterone and progesterone titers of pregnant rats, their male and female fetuses, and neonatal offspring. Endocrinology 106(1):306-316 (Pubitemid 10212501)
19. McCoy SJ, Shirley BA (1992) Effects of prenatal administration of testosterone and cortisone on the reproductive system of the female rat. Life Sci 50(9):621-628
20. Lee SM, Hutson JM (1999) Effect of androgens on the cranial suspensory ligament and ovarian position. Anat Rec 255(3): 306-315 (Pubitemid 29294016)
21. Piffer RC, Garcia PC, Gerardin DCC, Kempinas WG, Pereira OCM (2009) Semen parameters, fertility and testosterone levels in male rats exposed prenatally to betamethasone. Reprod Fertil Dev 21(5):634-639
22. Vandenbergh JG, Huggett CL (1995) The anogenital distance index, a predictor of the intrauterine position effects on reproduction in female house mice. Lab Anim Sci 45(5):567-573
23. Long SF, Wilson MC, Sufka KJ, Davis WM (1996) The effects of cocaine and nandrolone co-administration on aggression in male rats. Prog Neuropsychopharmacol Biol Psychiatry 20(5): 839-856 (Pubitemid 26261914)
24. Albert DJ, Dyson EM, Walsh ML, Petrovic DM (1988) Cohabitation with a female activates testosterone-dependent social aggression in male rats independently of changes in serum testosterone concentration. Physiol Behav 44(6):735-740 (Pubitemid 19037736)
25. Piffer RC, Garcia PC, Pereira OC (2009) Adult partner preference and sexual behavior of male rats exposed prenatally to betamethasone. Physiol Behav 98(1-2):163-167
26. Gerardin DC, Pereira OC (2002) Reproductive changes in male rats treated perinatally with an aromatase inhibitor. Pharmacol Biochem Behav 71(1-2):301-305
27. Leonelli C, Garcia PC, Pereira OC (2011) Copulatory efficiency and fertility in male rats exposed perinatally to flutamide. Reprod Toxicol 31(1):10-16
28. Gerardin DCC, Pereira OCM, Kempinas WG, Florio JC, Moreira EG, Bernardi MM (2005) Sexual behavior, neuroendocrine, and neurochemical aspects in male rats exposed prenatally to stress. Physiol Behav 84(1):97-104 (Pubitemid 40092070)
29. Pereira OC, Bernardi MM, Gerardin DC (2006) Could neonatal testosterone replacement prevent alterations induced by prenatal stress in male rats? Life Sciences 8(78):2767-2771
30. Cummings J, Clemens LG, Nunez AA (2008) Exposure to PCB 77 affects partner preference but not sexual behavior in the female rat. Physiol Behav 95(3):471-475
31. Henley CL, Nunez AA, Clemens LG (2009) Estrogen treatment during development alters adult partner preference and reproductive behavior in female laboratory rats. Horm Behav 55(1):68-75
32. Vega Matuszczyk JV, Larsson K (1995) Sexual preference and feminine and masculine sexual behavior of male rats prenatally exposed to antiandrogen or antiestrogen. Horm Behav 29(2): 191-206
33. Negri-Cesi P, Colciago A, Pravettoni A, Casati L, Conti L, Celotti F (2008) Sexual differentiation of the rodent hypothalamus: hormonal and environmental influences. J Steroid Biochem Mol Biol 109(3-5):294-299
34. Gray LE Jr, Wolf C, Lambright C, Mann P, Price M, Cooper RL, Ostby J (1999) Administration of potentially antiandrogenic pesticides (procymidone, linuron, iprodione, chlozolinate, p, p'-DDE, and ketoconazole) and toxic substances (dibutyl- and diethylhexyl phthalate, PCB 169, and ethane dimethane sulphonate)during sexual differentiation produces diverse profiles of reproductive malformations in the male rat. Toxicol Ind Health 15(1-2):94-118 (Pubitemid 30484120)
35. Schulz KM, Molenda-Figueira HA, Sisk CL (2009) Back to the future: the organizational-activational hypothesis adapted to puberty and adolescence. Horm Behav 55(5):597-604
36. Henley CL, Nunez AA, Clemens LG (2010) Exogenous androgen during development alters adult partner preference and mating behavior in gonadally intact male rats. Horm Behav 57(4-5): 488-495
37. Matsumoto A (1991) Synaptogenic action of sex steroids in developing and adult neuroendocrine brain. Psychoneuroendocrinology 16(1-3):25-40
38. Cologer-Clifford A, Simon NG, Lu SF, Smoluk SA (1997) Serotonin agonist-induced decreases in intermale aggression are dependent on brain region and receptor subtype. Pharmacol Biochem Behav 58(2):425-430 (Pubitemid 27394295)
39. Baum MJ (1979) Differentiation of coital behavior in mammals: a comparative analysis. Neurosci Biobehav Rev 3(4):265-284 (Pubitemid 10103187)
40. Balthazart J, Baillien M, Cornil CA, Ball GF (2004) Preoptic aromatase modulates male sexual behavior: slow and fast mechanisms of action. Physiol Behav 83(2):247-270 (Pubitemid 39361569)
41. Toda K, Saibara T, Okada T, Onishi S, Shizuta Y (2001) A loss of aggressive behaviour and its reinstatement by oestrogen in mice lacking the aromatase gene (Cyp19). J Endocrinol 168(2):217-220 (Pubitemid 32184284)
42. Matsumoto T, Honda S, Harada N (2003) Alteration in sexspecific behaviors in male mice lacking the aromatase gene. Neuroendocrinol 77(6):416-424 (Pubitemid 36831205)
43. Lumia AR, Thorner KM, McGinnis MY (1994) Effects of chronically high doses of the anabolic androgenic steroid, testosterone, on intermale aggression and sexual behavior in male rats. Physiol Behav 55(2):331-335 (Pubitemid 24065243)
44. Henley CL, Nunez AA, Clemens LG (2011) Hormones of choice: the neuroendocrinology of partner preference in animals. Front Neuroendocrinol 32(2):146-154
45. Nordenstrom A, Servin A, Bohlin G, Larsson A, Wedell A (2002) Sex-typed toy play behavior correlates with the degree of prenatal androgen exposure assessed by CYP21 genotype in girls with congenital adrenal hyperplasia. J Clin Endocrinol Metab 87(11):5119-5124 (Pubitemid 35316354)
46. Mathews GA, Fane BA, Conway GS, Brook CG, Hines M (2009) Personality and congenital adrenal hyperplasia: possible effects of prenatal androgen exposure. Horm Behav 55(2):285-291