Role of pregnane xenobiotic receptor in the midbrain ventral tegmental area for estradiol- and 3α,5α-THP-facilitated lordosis of female rats

Psychopharmacology

Volumn 231, Issue 17, 2014, Pages 3365-3374

  Frye, C A ^a,b   Koonce, C J ^a,b   Walf, A A ^a,b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

3 ,5 THP; Midbrain ventral tegmental area; Pregnane xenobiotic receptor (PXR)

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; ANTISENSE OLIGONUCLEOTIDE; CELL NUCLEUS RECEPTOR; ESTRADIOL; PREGNANE XENOBIOTIC RECEPTOR; UNCLASSIFIED DRUG; 20ALPHA DIHYDROPROGESTERONE; ELTANOLONE; PREGNANE X RECEPTOR; PROGESTERONE; STEROID RECEPTOR;

AFFECT; AGGRESSION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; ELEVATED PLUS MAZE TEST; EXPLORATORY BEHAVIOR; FEMALE; LORDOSIS; MALE; MATING; NONHUMAN; OPEN FIELD BEHAVIOR; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REPRODUCTIVE BEHAVIOR; SOCIAL INTERACTION; VENTRAL TEGMENTUM; ANIMAL; ANXIETY; DRUG EFFECTS; HUMAN RELATION; LONG EVANS RAT; METABOLISM; MOTOR ACTIVITY; PSYCHOLOGY; SEXUAL BEHAVIOR;

20-ALPHA-DIHYDROPROGESTERONE; ANIMALS; ANXIETY; ESTRADIOL; FEMALE; INTERPERSONAL RELATIONS; MOTOR ACTIVITY; PREGNANOLONE; PROGESTERONE; RATS; RATS, LONG-EVANS; RECEPTORS, STEROID; SEXUAL BEHAVIOR, ANIMAL; VENTRAL TEGMENTAL AREA;

EID: 84906940614     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-013-3406-0     Document Type: Article

References (55)

1. Ahdieh HB, Brown TJ, Wade GN, Blaustein JD (1986) Hypothalamic nuclear progestin receptors and the duration of sexual receptivity in ovariectomized and ovariectomized-hysterectomized rats. Physiol Behav 36:211-215 (Pubitemid 16188259)
2. Balasubramanian B, Portillo W, Reyna A, Chen JZ, Moore AN, Dash PK, Mani SK (2008a) Nonclassical mechanisms of progesterone action in the brain: I. Protein kinase C activation in the hypothalamus of female rats. Endocrinology 149:5509-5517
3. Balasubramanian B, Portillo W, Reyna A, Chen JZ, Moore AN, Dash PK, Mani SK (2008b) Nonclassical mechanisms of progesterone action in the brain: II. Role of calmodulin-dependent protein kinase II in progesterone-mediated signaling in the hypothalamus of female rats. Endocrinology 149:5518-5526
4. Barbaccia ML, Roscetti G, Trabucchi M, Mostallino MC, Concas A, Purdy RH, Biggio G (1996) Time-dependent changes in rat brain neuroactive steroid concentrations and GABAA receptor function after acute stress. Neuroendocrinology 63:166-172
5. Bauer B, Hartz AM, Fricker G, Miller DS (2004) Pregnane X receptor upregulation of P-glycoprotein expression and transport function at the blood-brain barrier. Mol Pharmacol 66:413-419 (Pubitemid 39329239)
6. Baulieu EE (1991) Neurosteroids: a new function in the brain. Biol Cell 71:3-10
7. Beyer C, González-Flores O, Ramírez-Orduña JM, González-Mariscal G (1999) Indomethacin inhibits lordosis induced by ring A-reduced progestins: possible role of 3α-oxoreduction in progestin-facilitated lordosis. Horm Behav 35:1-8 (Pubitemid 29100803)
8. Cheng YJ, Karavolas HJ (1975) Subcellular distribution and properties of progesterone (delta4-steroid) 5α-reductase in rat medial basal hypothalamus. J Biol Chem 250:7997-8003
9. Christensen A, Dewing P, Micevych P (2011) Membrane-initiated estradiol signaling induces spinogenesis required for female sexual receptivity. J Neurosci 31:17583-17589
10. DeBold JF, Malsbury CW (1989) Facilitation of sexual receptivity by hypothalamic and midbrain implants of progesterone in female hamsters. Physiol Behav 46:655-660 (Pubitemid 19268836)
11. DeBold JF, Malsbury CW, Harris VS, Malenka R (1982) Sexual receptivity: brain sites of estrogen action in female hamsters. Physiol Behav 29:589-593 (Pubitemid 13220501)
12. Dussault I, Forman BM (2002) The nuclear receptor PXR: a master regulator of "homeland" defense. Crit Rev Eukaryot Gene Expr 12:53-64 (Pubitemid 35239413)
13. Erskine MS (1985) Effects of paced coital stimulation on estrus duration in intact cycling rats and ovariectomized and ovariectomized/adrenalectomized hormone-primed rats. J Comp Physiol Psychol 99:151-161
14. Etgen AM, González-Flores O, Todd BJ (2006) The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors. Front Neuroendocrinol 27:363-375 (Pubitemid 44738013)
15. File SE, Hyde JR (1978) Can social interaction be used to measure anxiety? Br J Pharmacol 62:19-24 (Pubitemid 8251893)
16. Francis GA, Fayard E, Picard F, Auwerx J (2003) Nuclear receptors and the control of metabolism. Annu Rev Physiol 65:261-311 (Pubitemid 38249155)
17. Frye CA (2011) Novel substrates for, and sources of, progestogens for reproduction. J Neuroendocrinol 23:961-973
18. Frye CA, Rhodes ME (2006) Infusions of 5α-pregnan-3α-ol-20- one (3α, 5α-THP) to the ventral tegmental area, but not the substantia nigra, enhance exploratory, anti-anxiety, social and sexual behaviours and concomitantly increase 3α,5α-THP concentrations in the hippocampus, diencephalon and cortex of ovariectomised oestrogen-primed rats. J Neuroendocrinol 18:960-975 (Pubitemid 44660629)
19. Frye CA, Paris JJ, Rhodes ME (2008) Exploratory, anti-anxiety, social, and sexual behaviors of rats in behavioral estrus is attenuated with inhibition of 3α,5α-THP formation in the midbrain ventral tegmental area. Behav Brain Res 193:269-276
20. Frye CA, Paris JJ, Walf AA, Rusconi JC (2011) Effects and mechanisms of 3α, 5α,-THP on emotion, motivation, and reward functions involving pregnane xenobiotic receptor. Front Neurosci 5:136
21. Frye CA, Koonce CJ, Walf AA, Rusconi JC (2013) Motivated behaviors and levels of 3α,5α-THP in themidbrain are attenuated by knocking down expression of pregnane xenobiotic receptor in the midbrain ventral tegmental area of proestrous rats. J Med Sex 10:1692-1706
22. García-Juárez M, Beyer C, Soto-Sánchez A, Domínguez-Ordoñez R, Gómora-Arrati P, Lima-Hernández FJ, Eguibar JR, Etgen AM, González-Flores O (2011) Leptin facilitates lordosis behavior through GnRH-1 and progestin receptors in estrogen-primed rats. Neuropeptides 45(1):63-67
23. Geick A, Eichelbaum M, Burk O (2001) Nuclear receptor response elements mediate induction of intestinal MDR1 by rifampin. J Biol Chem 276:14581-14587
24. González-Mariscal G, González-Flores O, Beyer C (1989) Intrahypothalamic injection of RU486 antagonizes the lordosis induced by ring A-reduced progestins. Physiol Behav 46:435-438 (Pubitemid 19253855)
25. Hall CS, Ballachey EL (1932) A study of the rat's behavior in a field: a contribution to method in comparative psychology. Univ Calif Publ Psychol 6:1-12
26. Handley SL, Mithani S (1984) Effects of α-adrenoreceptor agonists and antagonists in a maze-exploration model of 'fear'-motivated behaviour. Naunyn-Schmeideberg's Arch Pharmacol 327:1-5 (Pubitemid 14061582)
27. Harmsen S, Meijerman I, Beijnen JH, Schellens JH (2007) The role of nuclear receptors in pharmacokinetic drug-drug interactions in oncology. Cancer Treat Rev 33:369-380 (Pubitemid 46760528)
28. King SR, Manna PR, Ishii T, Syapin PJ, Ginsberg SD, Wilson K, Walsh LP, Parker KL, Stocco DM, Smith RG, Lamb DJ (2002) An essential component in steroid synthesis, the steroidogenic acute regulatory protein, is expressed in discrete regions of the brain. J Neurosci 22:10613-10620 (Pubitemid 36005134)
29. Kliewer SA, Goodwin B, Willson TM (2002) The nuclear pregnane X receptor: a key regulator of xenobiotic metabolism. Endocr Rev 23:687-702 (Pubitemid 35191629)
30. Lamba V, Yasuda K, Lamba JK, Assem M, Davila J, Strom S, Schuetz EG (2004) PXR (NR1I2): splice variants in human tissues, including brain, and identification of neurosteroids and nicotine asPXR activators. Toxicol Appl Pharmacol 199:251-265 (Pubitemid 39208725)
31. Lisciotto CA, DeBold JF (1991) Ventral tegmental lesions impair sexual receptivity in female hamsters. Brain Res Bull 26:877-883
32. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)). Methods 25:402-408 (Pubitemid 34164012)
33. Ma X, Idle JR, Gonzalez FJ (2008) The pregnane X receptor: from bench to bedside. Expert Opin Drug Metab Toxicol 4:895-908
34. Mani SK, Blaustein JD (2012) Neural progestin receptors and female sexual behavior. Neuroendocrinology 96:152-161
35. Marini S, Nannelli A, Sodini D, Dragoni S, Valoti M, Longo V, Gervasi PG (2007) Expression, microsomal and mitochondrial activities of cytochrome P450 enzymes in brain regions from control and phenobarbital-treated rabbits. Life Sci 80(10):910-917 (Pubitemid 46186419)
36. Mellon SH, Deschepper CF (1993) Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Res 629:283-292 (Pubitemid 23337803)
37. Mellon SH, Gong W, Schonemann MD (2008) Endogenous and synthetic neurosteroids in treatment of Niemann-Pick Type C disease. Brain Res Rev 57:410-420 (Pubitemid 351381765)
38. Micevych P, Christensen A (2012) Membrane-initiated estradiol actions mediate structural plasticity and reproduction. Front Neuroendocrinol 33:331-341
39. Miryala CS, Hassell J, Adams S, Hiegel C, Uzor N, Uphouse L (2011) Mechanisms responsible for progesterone's protection against lordosis-inhibiting effects of restraint II. Role of progesterone metabolites. Horm Behav 60:226-232
40. Mòdol L, Darbra S, Pallarès M (2011) Neurosteroids infusion into the CA1 hippocampal region on exploration, anxiety-like behaviour and aversive learning. Behav Brain Res 222:223-229
41. Moore LB, Parks DJ, Jones SA, Bledsoe RK, Consler TG, Stimmel JB, Goodwin B, Liddle C, Blanchard SG, Willson TM, Collins JL (2000) Kliewer SA (2000) Orphan nuclear receptors constitutive androstane receptor and pregnane X receptor share xenobiotic and steroid ligands. J Biol Chem 275:15122-15127 (Pubitemid 30337234)
42. National Research Council (US) Committee on Guidelines for the Use of Animals in Neuroscience and Behavioral Research (2003) Guidelines for the Care and Use of Mammals in Neuroscience and Behavioral Research. National Academies Press (US), Washington (DC)
43. Papadopoulos V, Baraldi M, Guilarte TR, Knudsen TB, Lacapère JJ, Lindemann P, Norenberg MD, Nutt D, Weizman A, Zhang MR, Gavish M (2006) Translocator protein (18 kDa): new nomenclature for the peripheral-type benzodiazepine receptor based on its structure and molecular function. Trends Pharmacol Sci 27:402-409 (Pubitemid 44069585)
44. Paxinos G, Watson C (1986) The rat brain. Academic Press, NY
45. Pleim ET, Brown TJ, MacLusky NJ, Etgen AM, Barfield RJ (1989) Dilute estradiol implants and progestin receptor induction in the ventromedial nucleus of the hypothalamus: correlation with receptive behavior in female rats. Endocrinology 124:1807-1812 (Pubitemid 19105450)
46. Pleim ET, Lisciotto CA, DeBold JF (1990) Facilitation of sexual receptivity in hamsters by simultaneous progesterone implants into the VMH and ventral mesencephalon. Horm Behav 24:139-151 (Pubitemid 20184129)
47. Pleim ET, Baumann J, Barfield RJ (1991) A contributory role for midbrain progesterone in the facilitation of female sexual behavior in rats. Horm Behav 25:19-28
48. Purdy RH, Morrow AL, Moore PH Jr, Paul SM (1991) Stress-induced elevations of gamma-aminobutyric acid type A receptor-active steroids in the rat brain. Proc Natl Acad Sci U S A 88:4553-4557 (Pubitemid 21914579)
49. Rubin BS, Barfield RJ (1983a) Induction of estrous behavior in ovariectomized rats by sequential replacement of estrogen and progesterone to the ventromedial hypothalamus. Neuroendocrinology 37:218-224
50. Rubin BS, Barfield RJ (1983b) Progesterone in the ventromedial hypothalamus facilitates estrous behavior in ovariectomized, estrogen-primed rats. Endocrinology 113:797-804 (Pubitemid 13048979)
51. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108 (Pubitemid 351818697)
52. Vallée M, Rivera JD, Koob GF, Purdy RH, Fitzgerald RL (2000) Quantification of neurosteroids in rat plasma and brain following swim stress and allopregnanolone administration using negative chemical ionization gas chromatography/mass spectrometry. Anal Biochem 287:153-166
53. Watkins RE, Wisely GB, Moore LB, Collins JL, Lambert MH, Williams SP, Willson TM, Kliewer SA, Redinbo MR (2001) The human nuclear xenobiotic receptor PXR: structural determinants of directed promiscuity. Science 292:2329-2333 (Pubitemid 32568055)
54. Xu DX, Chen YH, Wang JP, Sun MF, Wang H, Wei LZ, Wei W (2005) Perinatal lipopolysaccharide exposure downregulates pregnane X receptor and Cyp3a11 expression in fetal mouse liver. Toxicol Sci 87:38-45 (Pubitemid 41222656)
55. Zhang B, Xie W, Krasowski MD (2008) PXR: a xenobiotic receptor of diverse function implicated in pharmacogenetics. Pharmacogenomics 9:1695-1709