Variation in Maternal Care Influences Ventromedial Hypothalamus Activation in the Rat

Journal of Neuroendocrinology

Volumn 23, Issue 5, 2011, Pages 393-400

  Cameron, N M ^a   Soehngen, E ^a   Meaney, M J ^b  

^a BINGHAMTON UNIVERSITY   (United States)

^b DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

C Fos; Female; Oestrogen receptor ; Progesterone receptor; Sexual behaviour

Indexed keywords

ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; PROTEIN C FOS; STEROID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONTROLLED STUDY; DIESTRUS; FEMALE; GROOMING; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; LICKING; LORDOSIS; MALE; MATERNAL CARE; MATING; NEUROENDOCRINE SYSTEM; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROESTRUS; PROGENY; PROTEIN EXPRESSION; PSEUDOPREGNANCY; RAT; SEXUAL BEHAVIOR; ZONA INCERTA;

ANIMALS; BEHAVIOR, ANIMAL; ESTROGEN RECEPTOR ALPHA; ESTROUS CYCLE; FEMALE; HYPOTHALAMUS; MALE; MATERNAL BEHAVIOR; NEUROSECRETORY SYSTEMS; OVARIECTOMY; PREGNANCY; PROTO-ONCOGENE PROTEINS C-FOS; PSEUDOPREGNANCY; RATS; RATS, LONG-EVANS; RECEPTORS, PROGESTERONE; SEXUAL BEHAVIOR, ANIMAL;

EID: 79954547496     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02124.x     Document Type: Article

References (47)

1. Meaney M. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001; 24: 1161-1192.
2. Cameron NM, Champagne FA, Parent C, Fish EW, Ozaki-Kuroda K, Meaney MJ. The programming of individual differences in defensive responses and reproductive strategies in the rat through variations in maternal care. Neurosci Biobehav Rev 2005; 29: 843-865.
3. Cameron NM, del Corpo A, Diorio J, McAllister K, Sharma S, Meaney MJ. Maternal programming of sexual behaviour and hypothalamic-pituitary-gonadal function in the female. PLoS ONE 2008; 3: e2210.
4. Champagne F, Francis D, Mar A, Meaney M. Oestrogen receptor alpha is essential for induction of oxytocin receptor by oestrogen. Neuroreport 2003; 29: 33-36.
5. Champagne FA, Weaver ICG, Diorio J, Dymov S, Szyf M, Meaney JM. Maternal care associated with methylation of the oestrogen receptor-alpha1b promoter and oestrogen receptor-alpha expression in the medial preoptic area of female offspring. Endocrinology 2006; 147: 2909-2915.
6. Cameron NM, Dhir SK, Meaney MJ. Effect of variation in maternal care and gonadal hormones on sexual behaviours. The Endocrine Society's 88th Annual Meeting, Boston, MA, 2006.
7. Simerly RB. Organization and regulation of sexually dimorphic neuroendocrine pathways. Behav Brain Res 1998; 92: 195-203.
8. Chateau D, Chabli A, Aron C. Effects of ventromedial nucleus lesions on the display of lordosis behaviour in the male rat. Interactions with facilitory effects of male urine. Physiol Behav 1987; 39: 341-345.
9. Pfaff DW, Sakuma Y. Deficit in the lordosis reflex of female rats caused by lesions in the ventromedial nucleus of the hypothalamus. J Physiol 1979; 288: 203-210.
10. La Vaque TJ, Rodgers CH. Recovery of mating behaviour in the female rat following VMH lesions. Physiol Behav 1975; 14: 59-63.
11. Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW. Roles of oestrogen receptor-{alpha} gene expression in reproduction-related behaviours in female mice. Endocrinology 1998; 139: 5070-5081.
12. Rubin BS, Barfield RJ. Priming of estrous responsiveness by implants of 17{beta}-estradiol in the ventromedial hypothalamic nucleus of female rats. Endocrinology 1980; 106: 504-509.
13. Frye CA. The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain Res Rev 2001; 37: 201-222.
14. Rønnekleiv OK, Kelly MJ. Diversity of ovarian steroid signaling in the hypothalamus. Front Neuroendocrinol 2005; 26: 65-84.
15. Tsai M, O'Malley BW. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem 1994; 63: 451-486.
16. Joel PB, Traish AM, Lannigan DA. Estradiol and phorbol ester cause phosphorylation of serine 118 in the human oestrogen receptor. Mol Endocrinol 1995; 9: 1041-1052.
17. Hardy DF, DeBold JF. Effects of coital stimulation upon behaviour of the female rat. J Comp Physiol Psychol 1972; 78: 400-408.
18. Lehmann ML, Erskine MS. Induction of pseudopregnancy using artificial VCS: importance of lordosis intensity and prestimulus estrous cycle length. Horm Behav 2004; 45: 75-83.
19. Champagne FA, Francis DD, Mar A, Meaney MJ. Variation in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003; 79: 359-371.
20. Myers M, Brunelli S, Snair H. Relationships between maternal behaviour of SHR and WKY dams and adult blood pressures of croos-fostered F1 pups. Dev Psychobiol 1989; 22: 55-67.
21. Lannigan DA. Oestrogen receptor phosphorylation. Steroids 2003; 68: 1-9.
22. Blaustein JD, Erskine MS. Feminine sexual behaviour: cellular integration of hormonal and afferent information in the rodent forebrain. In: Pfaff DW, et al., ed. Hormones, Brain and Behaviour. San Diego, CA: Elsivier, 2002: 139-214.
23. Menard JL, Champagne DL, Meaney MJP. Variation of maternal care differentially influence 'fear' reactivity and regional pattern of cfos immunoreactivity in response to the shock-probe burying test. Neuroscience 2004; 129: 297-308.
24. Greco B, Allegretto EA, Tetel MJ, Blaustein JD. Coexpression of ERβ with ERα and progestin receptor proteins in the female rat forebrain: effects of estradiol treatment. Endocrinology 2001; 142: 5172-5181.
25. Kobelt P, Tebbe JJ, Tjandra I, Bae H-G, Ruter J, Klapp BF, Wiedenmann B, Monnikes H. Two immunocytochemical protocols for immunoflurescent detection of c-Fos positive neurons in the rat brain. Brain Res Brain Res Protoc 2004; 13: 45-52.
26. Naef L, Woodside B. Prolactin/leptin interactions in the control of food intake in rats. Endocrinology 2007; 148: 5977-5983.
27. Swanson LW. Brain Maps: Structure of the Rat Brain. San Diego, CA: Academic Press, 2004.
28. Cameron NM, Fish EW, Meaney MJ. Maternal influences on the sexual behaviour and reproductive success of the female rat. Horm Behav 2008; 54: 178-184.
29. Champagne F, Diorio J, Sharma S, Meaney MJ. Naturally occurring variations in maternal behaviour in the rat are associated with differences in oestrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 2001; 98: 12736-12741.
30. Chen D, Riedl T, Washbrook E, Pace PE, Coombes RC, Egly J-M, Ali S. Activation of oestrogen receptor [alpha] by S118 phosphorylation involves a ligand-dependent interaction with TFIIH and participation of CDK7. Mol Cell 2000; 6: 127-137.
31. Kato S, Endoh H, Masuhiro Y, Kitamoto T, Uchiyama S, Sasaki H, Masushige S, Gotoh Y, Nishida E, Kawashima H, Metzger D, Chambon P. Activation of the oestrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 1995; 27: 1491-1494.
32. Cameron NM, Shahrokh D, Del Corpo A, Dhir SK, Szyf M, Champagne FA, Meaney MJ. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinol 2008; 20: 795-801.
33. Schibler U, Sierra F. Alternative promoters in developmental gene expression. Annu Rev Genet 1987; 21: 237-257.
34. Bird AP. DNA methylation patterns and epigenetic memory. Genes Dev 2002; 16: 6-21.
35. Frasor J, Gibori G. Prolactin regulation of oestrogen receptor expression. Trends Endocrinol Metab 2003; 14: 118-123.
36. Simerly RB, Young BJ. Regulation of oestrogen receptor messenger ribonucleic acid in rat hypothalamus by sex steroid hormones. Mol Endocrinol 1991; 5: 424-432.
37. Blaustein JD, Brown TJ. Progesterone decreases the concentration of hypothalamic and anterior pituitary oestrogen receptors in ovariectomized rats. Brain Res 1984; 304: 225-236.
38. Blaustein JD, Turcotte JC. Estradiol-induced progestin receptor immunoreactivity is found only in oestrogen receptor-immunoreactive cells in guinea pig brain. Neuroendocrinology 1989; 49: 454-461.
39. Quadros PS, Wagner CK. Regulation of progesterone receptor expression by estradiol is dependent on age, sex and region in the rat brain. Endocrinology 2008; 149: 3054-3061.
40. Lauber AH, Romano GJ, Pfaff DW. Sex difference in estradiol regulation of progestin receptor mRNA in rat mediobasal hypothalamus as demonstrated by in situ hybridization. Neuroendocrinology 1991; 53: 608-613.
41. Romano GJ, Krust A, Pfaff DW. Expression and estrogen regulation of progesterone receptor mRNA in neurons of the mediobasal hypothalamus: an in situ hybridization study. Mol Endocrinol 1989; 3: 1295-1300.
42. Shughrue PJ, Bushnell CD, Dorsa DM. Oestrogen receptor messenger ribonucleic acid in female rat brain during the estrous cycle: a comparison with ovariectomized females and intact males. Endocrinology 1992; 131: 381-388.
43. Byrnes EM, Babb JA, Bridges RS. Differential expression of ooestrogen receptor alpha following reproductive experience in young and middle-aged female rats. J Neuroendocrinol 2009; 21: 550-557.
44. Calizo LH, Flanagan-Cato LM. Hormonal-neural integration in the female rat ventromedial hypothalamus: triple labeling for oestrogen receptor-{alpha}, retrograde tract tracing from the periaqueductal gray, and mating-induced Fos expression. Endocrinology 2003; 144: 5430-5440.
45. Tetel MJ, Celentano DC, Blaustein JD. Intraneuronal convergence of tactile and hormonal stimuli associated with female reproduction in rats. J Neuroendocrinol 1994; 6: 211-216.
46. Georgescu M, Sabongui C, Del Corpo A, Marsan L, Pfaus JG. Vaginocervical stimulation induces Fos in glutamate neurons in the ventromedial hypothalamus: attenuation by oestrogen and progesterone. Horm Behav 2009; 56: 450-466.
47. Edmonds S, Zoloth SR, Adler NT. Storage of copulatory stimulation in the female rat. Physiol Behav 1972; 8: 161-164.