Role of testosterone in mediating prenatal ethanol effects on hypothalamic-pituitary-adrenal activity in male rats

Psychoneuroendocrinology

Volumn 34, Issue 9, 2009, Pages 1314-1328

  Lan, Ni ^a,b   Hellemans, Kim G C ^a   Ellis, Linda ^a   Viau, Victor ^a   Weinberg, Joanne ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b CHINA MEDICAL UNIVERSITY   (China)

Author keywords

Pituitary adrenal; Pituitary gonadal; Prenatal ethanol; Stress; Testosterone

Indexed keywords

ALCOHOL; ANDROGEN RECEPTOR; ARGIPRESSIN; CORTICOSTERONE; CORTICOTROPIN RELEASING FACTOR; LUTEINIZING HORMONE; TESTOSTERONE;

ALCOHOL CONSUMPTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DIETARY INTAKE; FEMALE; GENE EXPRESSION; GONADECTOMY; HIPPOCAMPUS; HORMONAL REGULATION; HORMONE SUBSTITUTION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; MALE; NEWBORN; NONHUMAN; ORGAN WEIGHT; PRENATAL EXPOSURE; PREOPTIC NUCLEUS; PRIORITY JOURNAL; RAT; STRIA TERMINALIS; TESTOSTERONE BLOOD LEVEL;

ANIMALS; ARGININE VASOPRESSIN; BODY WEIGHT; CORTICOSTERONE; CORTICOTROPIN-RELEASING HORMONE; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHANOL; FEMALE; GONADS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; LUTEINIZING HORMONE; MALE; ORGAN SIZE; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PHYSIOLOGICAL; TESTOSTERONE;

EID: 69849094464     PISSN: 03064530     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2009.04.001     Document Type: Article

References (71)

1. Ahima R.S., Lawson A.N., Osei S.Y., and Harlan R.E. Sexual dimorphism in regulation of type II corticosteroid receptor immunoreactivity in the rat hippocampus. Endocrinology 131 (1992) 1409-1416
2. Attademo A.M., Sanchez-Borzone M., Lasaga M., and Celis M.E. Intracerebroventricular injection of neuropeptide EI increases serum LH in male and female rats. Peptides 25 (2004) 1995-1999
3. Barron S., and Gilbertson R. Neonatal ethanol exposure but not neonatal cocaine selectively reduces specific isolation-induced vocalization waveforms in rats. Behav. Genet. 35 (2005) 93-102
4. Bingaman E.W., Magnuson D.J., Gray T.S., and Handa R.J. Androgen inhibits the increases in hypothalamic corticotropin-releasing hormone (CRH) and CRH-immunoreactivity following gonadectomy. Neuroendocrinology 59 (1994) 228-234
5. Bingham B., Williamson M., and Viau V. Androgen and estrogen receptor-beta distribution within spinal-projecting and neurosecretory neurons in the paraventricular nucleus of the male rat. J. Comp. Neurol. 499 (2006) 911-923
6. Bohn M.C., Dean D., Hussain S., and Giuliano R. Development of mRNAs for glucocorticoid and mineralocorticoid receptors in rat hippocampus. Brain Res. Dev. Brain Res. 77 (1994) 157-162
7. Briski K.P., and Sylvester P.W. Effects of repetitive daily acute stress on pituitary LH and prolactin release during exposure to the same stressor or a second novel stress. Psychoneuroendocrinology 12 (1987) 429-437
8. Briski K.P., and Sylvester P.W. Effects of sequential acute stress exposure on stress-induced pituitary luteinizing hormone and prolactin secretion. Life Sci. 41 (1987) 1249-1255
9. Burgess L.H., and Handa R.J. Hormonal regulation of androgen receptor mRNA in the brain and anterior pituitary gland of the male rat. Brain Res. Mol. Brain Res. 19 (1993) 31-38
10. Cardinal R.N., and Aitken a.M.R.F. ANOVA for the Behavioural Sciences Researcher (2006), Lawrence Erbaum Associates, London, UK
11. Champagne D., Beaulieu J., and Drolet G. CRFergic innervation of the paraventricular nucleus of the rat hypothalamus: a tract-tracing study. J. Neuroendocrinol. 10 (1998) 119-131
12. Chang C., and Kokontis J. Identification of a new member of the steroid receptor super-family by cloning and sequence analysis. Biochem. Biophys. Res. Commun. 155 (1988) 971-977
13. Cullinan W.E., Herman J.P., Battaglia D.F., Akil H., and Watson S.J. Pattern and time course of immediate early gene expression in rat brain following acute stress. Neuroscience 64 (1995) 477-505
14. Dallman M.F., Viau V., Bhatnagar S., Gomez F., Laugero K., and Bell M.E. Corticotropin-releasing factor, corticosteroids, stress, and sugar: energy balance, the brain, and behavior. hormones. In: Pfaff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Brain and Behavior vol. 1 (2002), Academic Press, New York 571-631
15. Davis M. The role of the amygdala in fear and anxiety. Annu. Rev. Neurosci. 15 (1992) 353-375
16. De Kloet E.R., Vreugdenhil E., Oitzl M.S., and Joels M. Brain corticosteroid receptor balance in health and disease. Endocr. Rev. 19 (1998) 269-301
17. De Vries G.J., Wang Z., Bullock N.A., and Numan S. Sex differences in the effects of testosterone and its metabolites on vasopressin messenger RNA levels in the bed nucleus of the stria terminalis of rats. J. Neurosci. 14 (1994) 1789-1794
18. Dong H.W., Petrovich G.D., and Swanson L.W. Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev. 38 (2001) 192-246
19. Dong H.W., Petrovich G.D., Watts A.G., and Swanson L.W. Basic organization of projections from the oval and fusiform nuclei of the bed nuclei of the stria terminalis in adult rat brain. J. Comp. Neurol. 436 (2001) 430-455
20. Faul F., Erdfelder E., Lang A.G., and Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39 (2007) 175-191
21. Gentry R.T., and Wade G.N. Androgenic control of food intake and body weight in male rats. J. Comp. Physiol. Psychol. 90 (1976) 18-25
22. Glavas M.M., Ellis L., Yu W.K., and Weinberg J. Effects of prenatal ethanol exposure on basal limbic-hypothalamic-pituitary-adrenal regulation: role of corticosterone. Alcohol. Clin. Exp. Res. 31 (2007) 1598-1610
23. Greenstein B.D., Fitzpatrick F.T., Adcock I.M., Kendall M.D., and Wheeler M.J. Reappearance of the thymus in old rats after orchidectomy: inhibition of regeneration by testosterone. J. Endocrinol. 110 (1986) 417-422
24. Handa R.J., Kerr J.E., DonCarlos L.L., McGivern R.F., and Hejna G. Hormonal regulation of androgen receptor messenger RNA in the medial preoptic area of the male rat. Brain Res. Mol. Brain Res. 39 (1996) 57-67
25. Handa R.J., Nunley K.M., Lorens S.A., Louie J.P., McGivern R.F., and Bollnow M.R. Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol. Behav. 55 (1994) 117-124
26. Herman J.P., Patel P.D., Akil H., and Watson S.J. Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Mol. Endocrinol. 3 (1989) 1886-1894
27. Hoyme H.E., May P.A., Kalberg W.O., Kodituwakku P., Gossage J.P., Trujillo P.M., Buckley D.G., Miller J.H., Aragon A.S., Khaole N., Viljoen D.L., Jones K.L., and Robinson L.K. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics 115 (2005) 39-47
28. Jacobson J.L., and Jacobson S.W. Drinking moderately and pregnancy. Effects on child development. Alcohol Res. Health 23 (1999) 25-30
29. Kehoe P., and Shoemaker W. Opioid-dependent behaviors in infant rats: effects of prenatal exposure to ethanol. Pharmacol. Biochem. Behav. 39 (1991) 389-394
30. Kerr J.E., Allore R.J., Beck S.G., and Handa R.J. Distribution and hormonal regulation of androgen receptor (AR) and AR messenger ribonucleic acid in the rat hippocampus. Endocrinology 136 (1995) 3213-3221
31. Kerr J.E., Beck S.G., and Handa R.J. Androgens modulate glucocorticoid receptor mRNA, but not mineralocorticoid receptor mRNA levels, in the rat hippocampus. J. Neuroendocrinol. 8 (1996) 439-447
32. Koehl M., Darnaudery M., Dulluc J., Van Reeth O., Le Moal M., and Maccari S. Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J. Neurobiol. 40 (1999) 302-315
33. Kofman O. The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci. Biobehav. Rev. 26 (2002) 457-470
34. Krulich L., Hefco E., Illner P., and Read C.B. The effects of acute stress on the secretion of LH, FSH, prolactin and GH in the normal male rat, with comments on their statistical evaluation. Neuroendocrinology 16 (1974) 293-311
35. Lan N., Yamashita F., Halpert A.G., Ellis L., Yu W.K., Viau V., and Weinberg J. Prenatal ethanol exposure alters the effects of gonadectomy on hypothalamic-pituitary-adrenal activity in male rats. J. Neuroendocrinol. 18 (2006) 672-684
36. Lee S., and Rivier C. Gender differences in the effect of prenatal alcohol exposure on the hypothalamic-pituitary-adrenal axis response to immune signals. Psychoneuroendocrinology 21 (1996) 145-155
37. Lee S., Schmidt D., Tilders F., and Rivier C. Increased activity of the hypothalamic-pituitary-adrenal axis of rats exposed to alcohol in utero: role of altered pituitary and hypothalamic function. Mol. Cell. Neurosci. 16 (2000) 515-528
38. Lesage J., Blondeau B., Grino M., Breant B., and Dupouy J.P. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo-pituitary adrenal axis in the newborn rat. Endocrinology 142 (2001) 1692-1702
39. Marino M.D., Cronise K., Lugo Jr. J.N., and Kelly S.J. Ultrasonic vocalizations and maternal-infant interactions in a rat model of fetal alcohol syndrome. Dev. Psychobiol. 41 (2002) 341-351
40. Matthews S.G. Early programming of the hypothalamo-pituitary-adrenal axis. Trends Endocrinol. Metab. 13 (2002) 373-380
41. Miller M.A., DeVries G.J., al-Shamma H.A., and Dorsa D.M. Decline of vasopressin immunoreactivity and mRNA levels in the bed nucleus of the stria terminalis following castration. J. Neurosci. 12 (1992) 2881-2887
42. Moga M.M., and Saper C.B. Neuropeptide-immunoreactive neurons projecting to the paraventricular hypothalamic nucleus in the rat. J. Comp. Neurol. 346 (1994) 137-150
43. Myers J.L., and Well A.D. Research Design and Statistical Analysis (2003), Lawrence Erlbaum Associates, Mahwah, NJ
44. Ness J.W., and Franchina J.J. Effects of prenatal alcohol exposure on rat pups' ability to elicit retrieval behavior from dams. Dev. Psychobiol. 23 (1990) 85-99
45. Oner H., and Ozan E. Effects of gonadal hormones on thymus gland after bilateral ovariectomy and orchidectomy in rats. Arch. Androl. 48 (2002) 115-126
46. Pace T.W., and Spencer R.L. Disruption of mineralocorticoid receptor function increases corticosterone responding to a mild, but not moderate, psychological stressor. Am. J. Physiol. Endocrinol. Metab. 288 (2005) E1082-1088
47. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (2005), Elsevier, Burlington, MA, USA
48. Prewitt C.M., and Herman J.P. Anatomical interactions between the central amygdaloid nucleus and the hypothalamic paraventricular nucleus of the rat: a dual tract-tracing analysis. J. Chem. Neuroanat. 15 (1998) 173-185
49. Ramsay D.S., Bendersky M.I., and Lewis M. Effect of prenatal alcohol and cigarette exposure on two- and six-month-old infants' adrenocortical reactivity to stress. J. Pediatr. Psychol. 21 (1996) 833-840
50. Sapolsky R.M., Romero L.M., and Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21 (2000) 55-89
51. Seckl J.R. Prenatal glucocorticoids and long-term programming. Eur. J. Endocrinol. 151 Suppl 3 (2004) U49-62
52. Shughrue P.J., Lane M.V., and Merchenthaler I. Comparative distribution of estrogen receptor-alpha and -beta mRNA in the rat central nervous system. J. Comp. Neurol. 388 (1997) 507-525
53. Simerly R.B., Chang C., Muramatsu M., and Swanson L.W. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J. Comp. Neurol. 294 (1990) 76-95
54. Taylor A.N., Branch B.J., Kokka N., and Poland R.E. Neonatal and long-term neuroendocrine effects of fetal alcohol exposure. Monogr. Neural Sci. 9 (1983) 140-152
55. Taylor A.N., Branch B.J., Van Zuylen J.E., and Redei E. Maternal alcohol consumption and stress responsiveness in offspring. Adv. Exp. Med. Biol. 245 (1988) 311-317
56. Taylor A.N., Nelson L.R., Branch B.J., Kokka N., and Poland R.E. Altered stress responsiveness in adult rats exposed to ethanol in utero: neuroendocrine mechanisms. Ciba Found. Symp. 105 (1984) 47-65
57. Turner B.B. Influence of gonadal steroids on brain corticosteroid receptors: a minireview. Neurochem. Res. 22 (1997) 1375-1385
58. Turner B.B., and Weaver D.A. Sexual dimorphism of glucocorticoid binding in rat brain. Brain Res. 343 (1985) 16-23
59. Viau V., Chu A., Soriano L., and Dallman M.F. Independent and overlapping effects of corticosterone and testosterone on corticotropin-releasing hormone and arginine vasopressin mRNA expression in the paraventricular nucleus of the hypothalamus and stress-induced adrenocorticotropic hormone release. J. Neurosci. 19 (1999) 6684-6693
60. Viau V., Lee P., Sampson J., and Wu J. A testicular influence on restraint-induced activation of medial parvocellular neurons in the paraventricular nucleus in the male rat. Endocrinology 144 (2003) 3067-3075
61. Viau V., Soriano L., and Dallman M.F. Androgens alter corticotropin releasing hormone and arginine vasopressin mRNA within forebrain sites known to regulate activity in the hypothalamic-pituitary-adrenal axis. J. Neuroendocrinol. 13 (2001) 442-452
62. Vorhees C.V. A fostering/crossfostering analysis of the effects of prenatal ethanol exposure in a liquid diet on offspring development and behavior in rats. Neurotoxicol. Teratol. 11 (1989) 115-120
63. Wade G.N. Sex hormone, regulatory behaviors, and body weight. In: Rosenblatt J.S., Hinde R.A., Shaw E., and Beer C.G. (Eds). Advances in the Study of Behavior (1976), Academic Press, New York 201-279
64. Weinberg J. Hyperresponsiveness to stress: differential effects of prenatal ethanol on males and females. Alcohol. Clin. Exp. Res. 12 (1988) 647-652
65. Weinberg J. Prenatal ethanol exposure alters adrenocortical development of offspring. Alcohol. Clin. Exp. Res. 13 (1989) 73-83
66. Weinberg J. Prenatal ethanol effects: sex differences in offspring stress responsiveness. Alcohol 9 (1992) 219-223
67. Weinberg J., Sliwowska J.H., Lan N., and Hellemans K.G. Prenatal alcohol exposure: foetal programming, the hypothalamic-pituitary-adrenal axis and sex differences in outcome. J. Neuroendocrinol. 20 (2008) 470-488
68. Williamson M., Bingham B., and Viau V. Central organization of androgen-sensitive pathways to the hypothalamic-pituitary-adrenal axis: implications for individual differences in responses to homeostatic threat and predisposition to disease. Prog. Neuropsychopharmacol. Biol. Psychiatry 29 (2005) 1239-1248
69. Williamson M., and Viau V. Androgen receptor expressing neurons that project to the paraventricular nucleus of the hypothalamus in the male rat. J. Comp. Neurol. 503 (2007) 717-740
70. Yukhananov R.Y., and Handa R.J. Estrogen alters proenkephalin RNAs in the paraventricular nucleus of the hypothalamus following stress. Brain Res. 764 (1997) 109-116
71. Zhou L., Blaustein J.D., and De Vries G.J. Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 134 (1994) 2622-2627