Expression of intracellular progesterone receptors in rat brain during different reproductive states, and involvement in maternal behavior

Brain Research

Volumn 830, Issue 2, 1999, Pages 358-371

  Numan, Michael ^a   Roach, Jennifer K ^a   Del Cerro, M Cruz R ^b   Guillamón, Antonio ^b   Segovia, Santiago ^b   Sheehan, Teige P ^a   Numan, Marilyn J ^a  

^a BOSTON COLLEGE   (United States)

^b UNIVERSIDAD NACIONAL DE EDUCACIÓN A DISTANCIA   (Spain)

Author keywords

Lactation; Maternal behavior; Medial hypothalamus; Medial preoptic area; Pregnancy; Progesterone; RU 486

Indexed keywords

ANTIGESTAGEN; MEMBRANE RECEPTOR; MIFEPRISTONE; PROGESTERONE; PROGESTERONE RECEPTOR;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN; CELL DENSITY; FEMALE; FOREBRAIN; HORMONAL REGULATION; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IMMUNOCYTOCHEMISTRY; LACTATION; MATERNAL BEHAVIOR; MEDIAL PREOPTIC AREA; NERVE CELL MEMBRANE; NEUROMODULATION; NONHUMAN; PREGNANCY; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR INTRINSIC ACTIVITY; STRIA TERMINALIS; THALAMUS MIDLINE NUCLEUS; THALAMUS VENTRAL NUCLEUS;

ANALYSIS OF VARIANCE; ANIMALS; BRAIN CHEMISTRY; FEMALE; HORMONE ANTAGONISTS; IMMUNOHISTOCHEMISTRY; MATERNAL BEHAVIOR; MIFEPRISTONE; PREGNANCY; RATS; RECEPTORS, PROGESTERONE; REPRODUCTION;

EID: 0033526649     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(99)01424-9     Document Type: Article

References (79)

1. Al-Khouri H., Greenstein B.D. Progesterone receptors in rat brain and uterus: dependence on the hormonal milieu. J. Endocrinol. 107:1985;159-162.
2. Alves S.E., Weiland N.G., Hayashi S., McEwen B.S. Immunocytochemical localization of nuclear estrogen receptors and progestin receptors within the rat dorsal raphe nucleus. J. Comp. Neurol. 391:1998;322-334.
3. Baulieu E.E., Schumacher M., Koenig H., Jung-Testas I., Akwa Y. Progesterone as a neurosteroid: actions within the nervous system. Cell. Mol. Neurobiol. 16:1996;143-153.
4. Beck C.A., Weigel N.L., Moyer M.L., Nordeen S.K., Edwards D.P. The progesterone antagonist RU486 acquires agonist activity upon stimulation of cAMP signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 90:1993;4441-4445.
5. Bethea C.L., Widmann A.A. Differential expression of progestin receptor isoforms in the hypothalamus, pituitary, and endometrium of rhesus macaques. Endocrinology. 139:1998;677-687.
6. Bitran D., Shiekh M., McLeod M. Anxiolytic effect of progesterone is mediated by the neurosteroid allopregnanolone at brain GABAA receptors. J. Neuroendocrinol. 7:1995;171-177.
7. Blaustein J.D., King J.C., Toft D.O., Turcotte J. Immunocytochemical localization of estrogen-induced progestin receptors in guinea pig brain. Brain Res. 474:1988;1-15.
8. Blaustein J.D., Olster D.H. Colchicine-induced accumulation of estrogen receptor and progestin receptor immunoreactivity in atypical areas in guinea-pig brain. J. Neuroendocrinol. 5:1993;63-70.
9. Blaustein J.D., Turcotte J.C. Down-regulation of progestin receptors in guinea pig brain: new findings using an immunocytochemical technique. J. Neurobiol. 21:1990;675-685.
10. Bridges R.S. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology. 114:1984;930-940.
11. R.S. Bridges, Biochemical basis of parental behavior in the rat, in: Advances in the Study of Behavior, Vol. 25, Academic Press, 1996, pp. 215-242.
12. Bridges R.S., Feder H.H. Inhibitory effects of various progestins and deoxycorticosterone on the rapid onset of maternal behavior induced by ovariectomy-hysterectomy during late pregnancy in rats. Horm. Behav. 10:1978;30-37.
13. Bridges R.S., Mann P.E. Prolactin-brain interactions in the induction of maternal behavior in rats. Psychoneuroendocrinology. 19:1994;611-622.
14. Bridges R.S., Numan M., Ronsheim P.M., Mann P.E., Lupini C.E. Central prolactin infusions stimulate maternal behavior in steroid-treated nulliparous rats. Proc. Natl. Acad. Sci. U.S.A. 87:1990;8003-8007.
15. Bridges R.S., Ronsheim P.M. Prolactin (PRL) regulation of maternal behavior in rats: bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology. 126:1990;837-848.
16. Brown T.J., MacLusky N.J. Progesterone modulation of estrogen receptors in microdissected regions of the rat hypothalamus. Mol. Cell. Neurosci. 5:1994;283-290.
17. Camacho-Arroyo I., Pasapera A.M., Cerbon M.A. Regulation of progesterone receptor gene expression by sex steroid hormones in the hypothalamus and the cerebral cortex of the rabbit. Neurosci. Lett. 214:1996;25-28.
18. Caron R.W., Salicioni A.M., Deis R.P. Mifepristone treatment demonstrates the participation of adrenal glucocorticoids in the regulation of oestrogen-induced prolactin secretion in ovariectomized rats. J. Steroid Biochem. Mol. Biol. 48:1994;385-389.
19. Clark A.S., Roy E.J. Behavioral insensitivity to progesterone during lactation in female rats. Physiol. Behav. 34:1985;677-682.
20. Crowley R.S., Insel T.R., O'Keefe J.A., Kim N.B., Amico J.A. Increased accumulation of oxytocin messenger ribonucleic acid in the hypothalamus of the female rat: induction by long term estradiol and progesterone administration and subsequent progesterone withdrawal. Endocrinology. 136:1995;224-231.
21. DeBold J.F., Frye C.A. Genomic and non-genomic actions of progesterone in the control of female hamster sexual behavior. Horm. Behav. 28:1994;445-453.
22. Del Cerro M.C.R. Role of the vomeronasal input in maternal behavior. Psychoneuroendocrinology. 23:1998;905-926.
23. Del Cerro M.C.R., Izquierdo M.A.P., Collado P., Segovia S., Guillamon A. Bilateral lesions of the bed nucleus of the accessory olfactory tract facilitate maternal behavior in virgin female rats. Physiol. Behav. 50:1991;67-71.
24. Doerr H.K., Siegel H.I., Rosenblatt J.S. Effects of progesterone withdrawal and estrogen on maternal behavior in nulliparous rats. Behav. Neural Biol. 32:1981;35-44.
25. DonCarlos L.L., Greene G.L., Morrell J.I. Estrogen plus progesterone increases progestin receptor immunoreactivity in the brain of ovariectomized guinea pigs. Neuroendocrinology. 50:1989;613-623.
26. Fahrbach S.E., Pfaff D.W. Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Horm. Behav. 20:1986;354-363.
27. Fang X., Wong S., Mitchell B.F. Effects of RU486 on estrogen, progesterone, oxytocin, and their receptors in the rat uterus during late gestation. Endocrinology. 138:1997;2763-2768.
28. Fleming A.S., Vaccarino F., Luebke C. Amygdaloid inhibition of maternal behavior in the nulliparous female rat. Physiol. Behav. 25:1980;731-743.
29. M.E. Freeman, The ovarian cycle of the rat, in: E. Knobil, J.D. Neill (Eds.), The Physiology of Reproduction, Vol. 2, Raven Press, New York, 1988, pp. 1893-2021.
30. Gass E.K., Leonhardt S.A., Nordeen S.K., Edwards D.P. The antagonists RU486 and ZK98299 stimulate progesterone receptor binding to deoxyribonucleic acid in vitro and in vivo, but have distinct effects on receptor conformation. Endocrinology. 139:1998;1905-1919.
31. Grazzini E., Guillon G., Mouillac B., Zingg H.H. Inhibition of oxytocin receptor function by direct binding of progesterone. Nature. 392:1998;509-512.
32. Gronemeyer H. Transcription activation by estrogen and progesterone receptors. Annu. Rev. Genet. 25:1991;89-123.
33. Hagihara K., Hirata S., Osada T., Hirai M., Kato J. Distribution of cells containing progesterone receptor mRNA in the female rat di- and telencephalon: an in situ hybridization study. Mol. Brain Res. 14:1992;239-249.
34. Insel T.R. Oxytocin-a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies. Psychoneuroendocrinology. 17:1992;3-35.
35. Insel T.R., Harbaugh C.R. Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol. Behav. 45:1989;1033-1041.
36. Jahn G.A., Edery M., Belair L., Kelly P.A., Djiane J. Prolactin receptor gene expression in rat mammary gland and liver during pregnancy and lactation. Endocrinology. 128:1991;2976-2984.
37. Joels M., deKloet E.R. Mineralocorticoid and glucocorticoid receptors in the brain. Implications for ion permeability and transmitter systems. Prog. Neurobiol. 43:1994;1-36.
38. Kastrup Y., Amandasson A., Hallbeck M., Hirato S., Hermanson O., Blomqvist A. Localization of progesterone receptor mRNA and progesterone receptor-like immunoreactovity in the rat brain stem. Soc. Neurosci. Abstr. 24:1998;1853.
39. Kato J., Hirata S., Nozawa A., Yamada-Mouri N. Gene expression of progesterone receptor isoforms in the rat brain. Horm. Behav. 28:1994;454-463.
40. Kirkland J.L., Murthy L., Stancel G.M. Progesterone inhibits the estrogen-induced expression of c-fos messenger ribonucleic acid in the uterus. Endocrinology. 130:1992;3223-3230.
41. Majewska M.D. Neurosteroids: endogenous bimodal modulators of the GABA-A receptor. Mechanism of action and physiological significance. Prog. Neurobiol. 38:1992;379-395.
42. Mani S.K., Blaustein J.D., Allen J.M.C., Law S.W., O'Malley B.W., Clark J.H. Inhibition of rat sexual behavior by antisense oligonucleotides to the progesterone receptor. Endocrinology. 135:1994;1409-1414.
43. McGinnis M.Y., Krey L.C., MacLusky N.J., McEwen B.S. Steroid receptor levels in intact and ovariectomized estrogen-treated rats: an examination of quantitative, temporal and endocrine factors influencing the efficacy of an estradiol stimulus. Neuroendocrinology. 33:1981;158-165.
44. Moltz H., Levin R., Leon M. Differential effects of progesterone on the maternal behavior of primiparous and multiparous rats. J. Comp. Physiol. Psych. 67:1969;36-40.
45. Moltz H., Lubin M., Leon M., Numan M. Hormonal induction of maternal behavior in the ovariectomized nulliparous rat. Physiol. Behav. 5:1970;1373-1377.
46. Numan M. Progesterone inhibition of maternal behavior in the rat. Horm. Behav. 11:1978;209-231.
47. M. Numan, Maternal Behavior, in: E. Knobil, J.D. Neill (Eds.), The Physiology of Reproduction, Vol. 2, 2nd Edn., Raven Press, New York, 1994, pp. 221-302.
48. Numan M., Numan M.J. Expression of Fos-like immunoreactivity in the preoptic area of maternally behaving virgin and postpartum rats. Behav. Neurosci. 108:1994;379-394.
49. Numan M., Numan M.J. Importance of pup-related sensory inputs and maternal performance for the expression of Fos-like immunoreactivity in the preoptic area and ventral bed nucleus of the stria terminalis of postpartum rats. Behav. Neurosci. 109:1995;135-149.
50. Numan M., Numan M.J. Projection sites of medical preoptic area and ventral bed nucleus of the stria terminalis neurons that express Fos during maternal behavior in female rats. J. Neuroendocrinol. 9:1997;369-384.
51. Numan M., Numan M.J., English J.B. Excitotoxic amino acid injections into the medial amygdala facilitate maternal behavior in virgin female rats. Horm. Behav. 27:1993;56-81.
52. Numan M., Rosenblatt J.S., Komisaruk B.R. Medial preoptic area and onset of maternal behavior in the rat. J. Comp. Physiol. Psych. 91:1977;146-164.
53. Numan M., Smith H.G. Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav. Neurosci. 98:1984;712-727.
54. Parsons B., Rainbow T.C., MacLusky N.J., McEwen B.S. Progestin receptor levels in rat hypothalamus and limbic nuclei. J. Neurosci. 2:1982;1446-1452.
55. Pedersen C.A. Oxytocin control of maternal behavior. Ann. NY Acad. Sci. 807:1997;126-145.
56. Pepe G.J., Rothchild I. Serum progesterone levels in ovariectomized rats injected with progesterone and estrone: relation to pregnancy maintenance and growth of decidual tissue. Endocrinology. 93:1973;1193-1199.
57. Ramirez V.D., Zheng J. Membrane sex-steroid receptors in the brain. Frontiers Neuroendocrinol. 17:1996;402-439.
58. Romano G.J., Krust A., Pfaff D.W. Expression and estrogen regulation of progesterone receptor mRNA in neurons of the mediobasal hypothalamus: an in situ hybridization study. Mol. Endocrinol. 3:1989;1295-1300.
59. Rosenblatt J.S., Olufowobi A., Siegel H.I. Effects of pregnancy hormones on maternal responsiveness, responsiveness to estrogen stimulation of maternal behavior, and the lordosis response to estrogen stimulation. Horm. Behav. 33:1998;104-114.
60. Sheehan T.P., Numan M. Microinjection of the tachykinin neuropeptide K into the ventromedial hypothalamus disrupts the hormonal onset of maternal behavior in female rats. J. Neuroendocrinol. 9:1997;677-687.
61. Shughrue P.J., Lane M.V., Merchenthaler I. Regulation of progesterone receptor messenger ribonucleic acid in the rat medial preoptic nucleus by estrogenic and antiestrogenic compounds: an in situ hybridization study. Endocrinology. 138:1997;5476-5484.
62. Siegel H.I., Rosenblatt J.S. Hormonal basis of hysterectomy-induced maternal behavior during pregnancy in the rat. Horm. Behav. 6:1975;211-222.
63. Siegel H.I., Rosenblatt J.S. Progesterone inhibition of estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats. Horm. Behav. 6:1975;223-230.
64. Siegel H.I., Rosenblatt J.S. Duration of estrogen stimulation and progesterone inhibition of maternal behavior in pregnancy-terminated rats. Horm. Behav. 11:1978;12-19.
65. Siegel H.I., Senatore A., Rogers S., Ahdieh H.B. Sexual receptivity in hamsters: brain nuclear estrogen and cytosolic progestin receptors after single and multiple steroid treatments and during the estrous cycle. Horm. Behav. 23:1989;173-184.
66. Simerly R.B., Carr A.M., Zee M.C., Lorang D. Ovarian steroid regulation of estrogen and progesterone receptor messenger ribonucleic acid in the anteroventral periventricular nucleus of the rat. J. Neuroendocrinol. 8:1996;45-56.
67. Smith S.S. Female sex steroid hormones: from receptors to networks to performance-actions on the sensorimotor system. Prog. Neurobiol. 44:1994;55-86.
68. Smith S.S., Gong Q.H., Hsu F.-C., Markowitz R.S., ffrench-Mullen J.M.H., Li X. GABAA receptor alpha4 subunit suppression prevents withdrawal properties of an endogenous steroid. Nature. 392:1998;926-930.
69. Smith S.S., Gong Q.H., Li X., Moran M.H., Bitran D., Frye C.A., Hsu F.-C. Withdrawal from 3alpha-OH-5alpha-pregnan-20-one using a pseudopregnancy model alters the kinetics of hippocampal GABA-A-gated current and increases the GABA-A receptor alpha 4 subunit in association with increased anxiety. J. Neurosci. 18:1998;5275-5284.
70. Spitz I.M., Croxatto H.B., Robbins A. Antiprogestins: mechanism of action and contraceptive potential. Annu. Rev. Pharmacol. Toxicol. 36:1996;47-81.
71. Sugino N., Telleria C.M., Gibori G. Progesterone inhibits 20alpha-hydroxysteroid dehydrogenase expression in the rat corpus luteum through the glucocorticoid receptor. Endocrinology. 138:1997;4497-4500.
72. L.W. Swanson, Brain maps: Structure of the Rat Brain, Elsevier, Amsterdam, 1992.
73. Traish A.M., Wotiz H.H. Monoclonal and polyclonal antibodies to human progesterone receptor peptide-(533-547) recognize a specific site in unactivated (8S) and activated (4S) progesterone receptor and distinguish between intact and proteolyzed receptors. Endocrinology. 127:1990;1167-1175.
74. Tsai M.-J., O'Malley B.W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63:1994;451-486.
75. Turcotte J.C., Blaustein J.D. Immunocytochemical localization of midbrain estrogen receptor- and progestin receptor-containing cells in female guinea pigs. J. Comp. Neurol. 328:1993;76-87.
76. Uht R.M., Anderson C.M., Webb P., Kushner P.J. Transcriptional activities of estrogen and glucocorticoid receptors are functionally integrated at the AP-1 response element. Endocrinology. 138:1997;2900-2908.
77. Wang M.-W., Crombie D.L., Hayes J.S., Heap R.B. Aberrant maternal behaviour in mice treated with a progesterone receptor antagonist during pregnancy. J. Endocrinol. 145:1995;371-377.
78. Wen D.X., Xu Y.-F., Mais D.E., Goldman M.E., McDonnell D.P. The A and B isoforms of the human progesterone receptor operate through distinct signaling pathways within target cells. Mol. Cell. Biol. 14:1994;8356-8364.
79. Yuan H., Bowlby D.A., Brown T.J., Hochberg R.B., MacLusky N.J. Distribution of occupied and unoccupied estrogen receptors in the rat brain: effects of physiological gonadal steroid exposure. Endocrinology. 136:1995;96-105.