Female mice with deletion of Type One 5α-reductase have reduced reproductive responding during proestrus and after hormone-priming

Pharmacology Biochemistry and Behavior

Volumn 122, Issue , 2014, Pages 20-29

  Koonce, Carolyn J ^a,b   Frye, Cheryl A ^a,b  

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

Allopregnanolone; Lordosis; Medroxyprogesterone acetate; Midbrain; Sexual behavior

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; ESTRADIOL; GESTAGEN; MEDROXYPROGESTERONE ACETATE; PROGESTERONE; STEROID 5ALPHA REDUCTASE 1; CHOLESTENONE 5ALPHA REDUCTASE; MEMBRANE PROTEIN; SRD5A1 PROTEIN, MOUSE; STEROID 5ALPHA REDUCTASE;

ADULT; AGGRESSION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIESTRUS; ESTRUS; ESTRUS CYCLE; FEMALE; GENE DELETION; GENOTYPE; LORDOSIS; MALE; MESENCEPHALON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROESTRUS; REPRODUCTIVE BEHAVIOR; SEXUAL BEHAVIOR; ANIMAL; DEFICIENCY; DRUG EFFECTS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; REPRODUCTION;

3-OXO-5-ALPHA-STEROID 4-DEHYDROGENASE; ANIMALS; CHOLESTENONE 5 ALPHA-REDUCTASE; FEMALE; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; PROESTRUS; PROGESTERONE; REPRODUCTION; SEXUAL BEHAVIOR, ANIMAL;

EID: 84897521067     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2014.03.010     Document Type: Article

References (73)

1. R.C. Agís-Balboa, G. Pinna, F. Pibiri, B. Kadriu, E. Costa, and A. Guidotti Down-regulation of neurosteroid biosynthesis in corticolimbic circuits mediates social isolation-induced behavior in mice Proc Natl Acad Sci U S A 104 2007 18736 18741 (Pubitemid 350210766)
2. E. Allen The oestrous cycle in the mouse Am J Anat 30 1922 297 371
3. J.D. Blaustein Steroid hormone receptors: long- and short-term integrators of the internal milieu and the external environment Horm Metab Res 44 2012 563 568
4. B.B. Braden, J.S. Talboom, I.D. Crain, A.R. Simard, and R.J. Lukas et al. Medroxyprogesterone acetate impairs memory and alters the GABAergic system in aged surgically menopausal rats Neurobiol Learn Mem 93 2010 444 453
5. B.B. Braden, A.N. Garcia, S.E. Mennenga, L. Prokai, and S.R. Villa et al. Cognitive-impairing effects of medroxyprogesterone acetate in the rat: independent and interactive effects across time Psychopharmacology (Berl) 218 2011 405 418
6. Y. Caldwell A sexual arousability model involving steroid effects at the plasma membrane Neurosci Biobehav Rev 26 2002 13 30
7. F. Celotti, R.C. Melcangi, and L. Martini The 5α-reductase in the brain: molecular aspects and relation to brain function Front Neuroendocrinol 13 1992 163 215
8. Y.J. Cheng, and H.J. Karavolas Conversion of progesterone to 5α-pregnane-3,20-dione and 3α-hydroxy-5α-pregnan-20-one by rat medical basal hypothalami and the effects of estradiol and stage of estrous cycle on the conversion Endocrinology 93 1973 1157 1162
9. J.I. Christian Effect of chronic ACTH treatment on maturation of intact female mice Endocrinology 74 1964 669 679
10. I. Ciriza, P. Carrero, C.A. Frye, and L.M. Garcia-Segura Reduced metabolites mediate neuroprotective effects of progesterone in the adult rat hippocampus. The synthetic progestin medroxyprogesterone acetate (Provera) is not neuroprotective J Neurobiol 66 2006 916 928 (Pubitemid 44222653)
11. C. Corpechot, B.E. Collins, M.P. Carey, A. Tsouros, P. Robel, and J.P. Fry Brain neurosteroids during the mouse oestrous cycle Brain Res 766 1997 276 280 (Pubitemid 27431463)
12. E.S. Davis, and C.A. Marler The progesterone challenge: steroid hormone changes following a simulated territorial intrusion in female Peromyscus californicus Horm Behav 44 2003 185 198 (Pubitemid 37371974)
13. E.S. Davis, and C.A. Marler C-fos changes following an aggressive encounter in female California mice: a synthesis of behavior, hormone changes and neural activity Neuroscience 127 2004 611 624 (Pubitemid 38993165)
14. Y. Delville Progesterone-facilitated sexual receptivity: a review of arguments supporting a nongenomic mechanism Neurosci Biobehav Rev 15 1991 407 414
15. E. Dominguez-Salazar, H.L. Bateman, and E.F. Rissman Background matters: the effects of estrogen receptor α gene disruption on male sexual behavior are modified by background strain Horm Behav 46 2004 482 490 (Pubitemid 39311917)
16. D.A. Edwards Induction of estrus in female mice: estrogen progesterone interactions Horm Behav 1 1970 299 304
17. B.G. England, G.D. Niswender, and A.R. Midgley Jr. Radioimmunoassay of estradiol-17beta without chromatography J Clin Endocrinol Metab 38 1974 42 50
18. L. Kappeler, and M.J. Meaney Epigenetics and parental effects Bioessays 32 2010 818 827
19. D.A. Finn, and K.W. Gee The estrus cycle, sensitivity to convulsants and the anticonvulsant effect of a neuroactive steroid J Pharmacol Exp Ther 271 1994 164 170 (Pubitemid 24333126)
20. C.A. Frye The role of neurosteroids and nongenomic effects of progestins in the ventral tegmental area in mediating sexual receptivity of rodents Horm Behav 40 2001 226 233 (Pubitemid 32846357)
21. C.A. Frye Progestins influence motivation, reward, conditioning, stress, and/or response to drugs of abuse Pharmacol Biochem Behav 86 2007 209 219 (Pubitemid 46282047)
22. C.A. Frye, and L.E. Bayon Mating stimuli influence endogenous variations in the neurosteroids 3alpha,5alpha-THP and 3alpha-Diol J Neuroendocrinol 11 1999 839 847 (Pubitemid 29494889)
23. C.A. Frye, and J.F. DeBold P-3-BSA, but not P-11-BSA, implants in the VTA rapidly facilitate receptivity in hamsters after progesterone priming to the VMH Behav Brain Res 53 1993 167 175 (Pubitemid 23074040)
24. C.A. Frye, and J.M. Vongher Progesterone has rapid and membrane effects in the facilitation of female mouse sexual behavior Brain Res 815 1999 259 269 (Pubitemid 29225273)
25. C.A. Frye, and J.M. Vongher Progesterone and 3α,5α-THP enhance sexual receptivity in mice Behav Neurosci 115 2001 1118 1128 (Pubitemid 32906650)
26. C.A. Frye, and J.M. Vongher Ventral tegmental area infusions of inhibitors of the biosynthesis and metabolism of 3α,5α-THP attenuate lordosis of hormone-primed and behavioural oestrous rats and hamsters J Neuroendocrinol 13 2001 1076 1086 (Pubitemid 33100225)
27. C.A. Frye, M.E. Rhodes, A. Walf, and J.P. Harney Testosterone enhances aggression of wild-type mice but not those deficient in type I 5alpha-reductase Brain Res 948 2002 165 170 (Pubitemid 35283776)
28. C.A. Frye, A.A. Walf, M.E. Rhodes, and J.P. Harney Progesterone enhances motor, anxiolytic, analgesic, and antidepressive behavior of wild-type mice, but not those deficient in type 1 5α-reductase Brain Res 1004 2004 116 124 (Pubitemid 38368067)
29. C.A. Frye, J.J. Paris, and M.E. Rhodes 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 2008 269 276
30. C.A. Frye, J.J. Paris, and M.E. Rhodes Engaging in paced mating, but neither exploratory, anti-anxiety, nor social behavior, increases 5alpha-reduced progestin concentrations in midbrain, hippocampus, striatum, and cortex Reproduction 133 2007 663 674 (Pubitemid 46671870)
31. C.A. Frye, and S.G. Gardiner Progestins can have a membrane-mediated action in rat midbrain for facilitation of sexual receptivity Horm Behav 30 1996 682 691 (Pubitemid 27148198)
32. C.A. Frye, C.J. Koonce, and A.A. Walf Mnemonic effects of progesterone to mice require formation of 3α,5α-THP Neuroreport 21 2010 590 595
33. C.A. Frye, C.J. Koonce, and A.A. Walf Progesterone, compared to medroxyprogesterone acetate, to C57BL/6, but not 5α-reductase mutant, mice enhances object recognition and placement memory and is associated with higher BDNF levels in the hippocampus and cortex Neurosci Lett 551 2013 53 57
34. C.A. Frye Novel substrates for, and sources of, progestogens for reproduction J Neuroendocrinol 23 2011 961 973
35. C.A. Frye, J.J. Paris, A.A. Walf, and J.C. Rusconi Effects and Mechanisms of 3α,5α,-THP on emotion, motivation, and reward functions involving pregnane xenobiotic receptor Front Neurosci 5 2012 136 153
36. B.B. Gorzalka, and R.E. Whalen Genetic regulation of hormone action: selective effects of progesterone and dihydroprogesterone (5α-pregnane-3, 20-dione) on sexual receptivity in mice Steroids 23 1974 499 505
37. I. Guttenberg Plasma levels of "free" progestin during the estrous cycle in the mouse Endocrinology 68 1961 1006 1009
38. D.H. Ho, and W.W. Burggren Epigenetics and transgenerational transfer: a physiological perspective J Exp Biol 213 2010 3 16
39. J. Jarrell Studies on the developmental pattern of rat ovarian 3 alpha-hydroxysteroid dehydrogenase: inhibition of the postpubertal activity with medroxyprogesterone acetate in vivo J Steroid Biochem 21 1984 151 156 (Pubitemid 14075011)
40. M. Karolczak, E. Küppers, and C. Beyer Developmental expression and regulation of aromatase- and 5α-reductase type 1 mRNA in the male and female mouse hypothalamus J Neuroendocrinol 10 1998 267 274 (Pubitemid 28177347)
41. S.R. King, P.R. Manna, T. Ishii, P.J. Syapin, and S.D. Ginsberg et al. An essential component in steroid synthesis, the steroidogenic acute regulatory protein, is expressed in discrete regions of the brain J Neurosci 22 2002 10613 10620 (Pubitemid 36005134)
42. S.R. King, S.D. Ginsberg, T. Ishii, R.G. Smith, K.L. Parker, and D.J. Lamb The steroidogenic acute regulatory protein is expressed in steroidogenic cells of the day-old brain Endocrinology 145 2004 4775 4780 (Pubitemid 39281472)
43. C.J. Koonce, and C.A. Frye Progesterone facilitates exploration, affective and social behaviors among wildtype, but not 5α-reductase Type 1 mutant, mice Behav Brain Res 253 2013 232 239
44. C.J. Koonce, A.A. Walf, and C.A. Frye Type 1 5α-reductase may be required for estrous cycle changes in affective behaviors of female mice Behav Brain Res 226 2012 376 380
45. X. Li, P.J. Bertics, and H.J. Karavolas Regional distribution of cytosolic and particulate 5α-dihydroprogesterone 3α-hydroxysteroid oxidoreductase in female rat brain J Steroid Biochem Mol Biol 60 1997 311 318 (Pubitemid 27278063)
46. J. Maguire, and I. Mody Neurosteroid synthesis-mediated regulation of GABA(A) receptors: relevance to the ovarian cycle and stress J Neurosci 27 2007 2155 2162 (Pubitemid 46340948)
47. M.S. Mahendroo, K.M. Cala, and D.W. Russell 5α-Reduced androgens play a key role in murine parturition Mol Endocrinol 10 1996 380 392 (Pubitemid 26112402)
48. M.S. Mahendroo, K.M. Cala, D.P. Landrum, and D.W. Russell Fetal death in mice lacking 5α-reductase type 1 caused by estrogen excess Mol Endocrinol 11 1997 917 927 (Pubitemid 27241784)
49. D. Matsui, M. Sakari, T. Sato, A. Murayama, I. Takada, and M. Kim et al. Transcriptional regulation of the mouse steroid 5α-reductase type II gene by progesterone in brain Nucleic Acids Res 30 2002 1387 1393 (Pubitemid 34679717)
50. C.M. McCormick, D. Robarts, K. Kopeikina, and J.E. Kelsey Long-lasting, sex- and age-specific effects of social stressors on corticosterone responses to restraint and on locomotor responses to psychostimulants in rats Horm Behav 48 2005 64 74 (Pubitemid 40779291)
51. R.C. Melcangi, A. Poletti, I. Cavarretta, F. Celotti, A. Colciago, and V. Magnaghi et al. The 5α-reductase in the central nervous system: expression and modes of control J Steroid Biochem Mol Biol 65 1998 295 299 (Pubitemid 28335616)
52. P. Micevych, and K. Sinchak Estradiol regulation of progesterone synthesis in the brain Mol Cell Endocrinol 290 2008 44 50
53. L. Milewich, B.B. Mendonca, I. Arnhold, A.M. Wallace, M.D. Donaldson, and J.D. Wilson et al. Women with steroid 5α-reductase 2 deficiency have normal concentrations of plasma 5α-dihydroprogesterone during the luteal phase J Clin Endocrinol Metab 80 1995 3136 3139 (Pubitemid 3010543)
54. G.D. Niswender Influence of the site of conjugation on the specificity of antibodies to progesterone Steroids 22 1973 413 424
55. K. Normington, and D.W. Russell Tissue distribution and kinetic characteristics of rat steroid 5α reductase isozymes. Evidence for distinct physiological functions J Biol Chem 267 1992 19548 19554
56. K. Pazol, K.V. Northcutt, M.E. Wilson, and K. Wallen Medroxyprogesterone acetate acutely facilitates and sequentially inhibits sexual behavior in female rats Horm Behav 49 2006 105 113 (Pubitemid 41821875)
57. T.M. Penning, R.B. Sharp, and N.R. Krieger Purification and properties of 3 alpha-hydroxysteroid dehydrogenase from rat brain cytosol. Inhibition by nonsteroidal anti-inflammatory drugs and progestins J Biol Chem 260 1985 15266 15272 (Pubitemid 16147972)
58. S.M. Petralia, V. Jahagirdar, and C.A. Frye Inhibiting biosynthesis and/or metabolism of progestins in the ventral tegmental area attenuates lordosis of rats in behavioural oestrus J Neuroendocrinol 17 2005 545 552 (Pubitemid 41195407)
59. A. Poletti, and L. Martini Androgen-activating enzymes in the central nervous system J Steroid Biochem Mol Biol 69 1999 117 122 (Pubitemid 29305529)
60. A. Poletti, P. Negri-Cesi, M. Rabufetti, A. Colciago, F. Celotti, and L. Martini Transient expression of the 5α-reductase type 2 isozyme in the rat brain in late fetal and early postnatal life Endocrinology 139 1998 2171 2178 (Pubitemid 28513882)
61. R.H. Purdy, P.H. Moore Jr., P.N. Rao, N. Hagino, T. Yamaguchi, and P. Schmidt et al. Radioimmunoassay of 3α-hydroxy-5α-pregnan-20-one in rat and human plasma Steroids 55 1990 290 296 (Pubitemid 20246184)
62. J.R. Ring The estrogen-progesterone induction of sexual receptivity in the spayed female mouse Endocrinology 34 1944 269 275
63. E.F. Rissman, S.R. Wersinger, H.N. Fugger, and T.C. Foster Sex with knockout models: behavioral studies of estrogen receptor α Brain Res 835 1999 80 90 (Pubitemid 29336553)
64. D. Rodbard, and D.M. Hutt Int atomic energy agency: symposium on RIA and related procedures in medicine Statistical analysis of radioimmunoassay and immunoradiometric (labeled antibody) assays: a generalized, weighted, iterative, least-squares method for logistic curve fitting 1974 Uni-pub New York 165
65. C.E. Roselli, and C.A. Snipes Progesterone 5α-reductase in mouse brain Brain Res 305 1984 197 202
66. D.W. Russell, and J.D. Wilson Steroid 5α-reductase: two genes/two enzymes Annu Rev Biochem 63 1994 25 61
67. J. Sambrook, E.F. Fritsch, and T. Maniatis Molecular cloning: a laboratory manual 1989 Cold Spring Harbor Laboratory Press New York
68. P. Sanchez, J.M. Torres, A. Olmo, F. O'Valle, and E. Ortega Effects of environmental stress on mRNA and protein expression levels of steroid 5α-reductase isozymes in adult rat brain Horm Behav 56 2009 348 353
69. J. Sarkar, S. Wakefield, G. MacKenzie, S.J. Moss, and J. Maguire Neurosteroidogenesis is required for the physiological response to stress: role of neurosteroid-sensitive GABAA receptors J Neurosci 31 2011 18198 18210
70. M. Thompson, and D.A. Edwards Experiential and strain determinants of the estrogen-progesterone induction of sexual receptivity in spayed female mice Horm Behav 2 1971 299 305
71. J.M. Torres, and E. Ortega Differential regulation of steroid 5α-reductase isozymes expression by androgens in the adult rat brain FASEB J 63 2003 246 251
72. A.A. Walf, and C.A. Frye Using the elevated plus maze as a bioassay to assess the effects of naturally-occurring, and exogenously-administered compounds, to influence anxiety-related behaviors of mice Todd Gould, Mood & Anxiety Related Phenotypes in Mice: Characterization Using Behavioral Tests 2009 Springer Protocols New York 225 246
73. J.D. Wilson, J.E. Griffin, and D.W. Russell Steroid 5α-reductase 2 deficiency Endocr Rev 14 1993 577 593