Progesterone facilitates exploration, affective and social behaviors among wildtype, but not 5α-reductase Type 1 mutant, mice

Behavioural Brain Research

Volumn 253, Issue , 2013, Pages 232-239

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

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

^c Alaska IDeA Network of Biomedical Excellence (INBRE)   (United States)

Author keywords

3 ,5 THP; Hippocampus; Medroxyprogesterone acetate; Neurosteroid; Prefrontal cortex

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; MEDROXYPROGESTERONE ACETATE; PROGESTERONE; STEROID 5ALPHA REDUCTASE;

AFFECTIVE BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELEVATED PLUS MAZE; EXPLORATORY BEHAVIOR; FEMALE; HIPPOCAMPUS; KNOCKOUT MOUSE; MAZE TEST; MOUSE; MOUSE MUTANT; NONHUMAN; OPEN FIELD TEST; OVARIECTOMY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROGESTERONE METABOLISM; SOCIAL BEHAVIOR; SOCIAL INTERACTION; WILD TYPE;

3Α,5Α-THP; HIPPOCAMPUS; MEDROXYPROGESTERONE ACETATE; NEUROSTEROID; PREFRONTAL CORTEX;

3-OXO-5-ALPHA-STEROID 4-DEHYDROGENASE; AFFECT; ANIMALS; ANXIETY; DOSE-RESPONSE RELATIONSHIP, DRUG; EXPLORATORY BEHAVIOR; FEMALE; GENOTYPE; IMMUNOHISTOCHEMISTRY; INTERPERSONAL RELATIONS; MEDROXYPROGESTERONE; MICE; MICE, KNOCKOUT; MOTOR ACTIVITY; MUTATION; OVARIECTOMY; PREGNANOLONE; PROGESTERONE; SOCIAL BEHAVIOR; STEROIDS;

EID: 84882749697     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.07.025     Document Type: Article

References (78)

1. Bäckström T., Andreen L., Birzniece V., Björn I., Johansson I.M., Nordenstam-Haghjo M., Nyberg S., Sundström-Poromaa I., Wahlström G., Wang M., Zhu D. The role of hormones and hormonal treatments in premenstrual syndrome. CNS Drugs 2003, 17:325-342.
2. Schmidt P.J., Rubinow D.R. Sex hormones and mood in the perimenopause. Annals of the New York Academy of Sciences 2009, 1179:70-85.
3. Joffe H., Cohen L.S. Estrogen, serotonin, and mood disturbance: where is the therapeutic bridge?. Biological Psychiatry 1998, 44:798-811.
4. Schmidt P.J., Nieman L., Danaceau M.A., Tobin M.B., Roca C.A., Murphy J.H., et al. Estrogen replacement in perimenopause-related depression: a preliminary report. American Journal of Obstetrics and Gynecology 2000, 183:414-420.
5. Marx C.E., Keefe R.S., Buchanan R.W., Hamer R.M., Kilts J.D., Bradford D.W., et al. Proof-of concept trial with the neurosteroid pregnenolone targeting cognitive and negative symptoms in schizophrenia. Neuropsychopharmacology 2009, 34:1885-1903.
6. Romeo E., Ströhle A., Spalletta G., di Michele F., Hermann B., Holsboer F., Pasini A., Rupprecht R. Effects of antidepressant treatment on neuroactive steroids in major depression. American Journal of Psychiatry 1998, 155:910-913.
7. Uzunova V., Sheline Y., Davis J.M., Rasmusson A., Uzunov D.P., Costa E., et al. Increase in the cerebrospinal fluid content of neurosteroids in patients with unipolar major depression who are receiving fluoxetine or fluvoxamine. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:3239-3244.
8. Wagner K.D. Major depression and anxiety disorders associated with Norplant. Journal of Clinical Psychiatry 1996, 57:152-157.
9. Bicikova M., Tallova J., Hill M., Krausova Z., Hampl R. Serum concentrations of some neuroactive steroids in women suffering from mixed anxiety-depressive disorder. Neurochemical Research 2000, 25:1623-1627.
10. Brambilla F., Biggio G., Pisu M.G., Bellodi L., Perna G., Bogdanovich-Djukic V., et al. Neurosteroid secretion in panic disorder. Psychiatry Research 2003, 118:107-116.
11. Eser D., Schule C., Romeo E., Baghai T.C., di Michele F., Pasini A., et al. Neuropsychopharmacological properties of neuroactive steroids in depression and anxiety disorders. Psychopharmacology 2006, 186:373-387.
12. Griffin L.D., Mellon S.H. Selective serotonin reuptake inhibitors directly alter activity of neurosteroidogenic enzymes. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:13512-13517.
13. Schüle C., Eser D., Baghai T.C., Nothdurfter C., Kessler J.S., Rupprecht R. Neuroactive steroids in affective disorders: target for novel antidepressant or anxiolytic drugs. Neuroscience 2011, 191:55-77.
14. Fu Y., Yu S., Guo X., Li X., Li T., Li H., Dong Y. Fluvoxamine increased glutamate release by activating both 5-HT(3) and sigma-1 receptors in prelimbic cortex of chronic restraint stress C57BL/6 mice. Biochimica et Biophysica Acta 2012, 1823:826-837.
15. Mellon S.H., Gong W., Schonemann M.D. Endogenous and synthetic neurosteroids in treatment of Niemann-Pick Type C disease. Brain Research Reviews 2008, 57:410-420.
16. Mellon S.H., Deschepper C.F. Neurosteroid biosynthesis: genes for adrenal steroidogenic enzymes are expressed in the brain. Brain Research 1993, 629:283-292.
17. Frye C.A. The role of neurosteroids and non-genomic effects of progestins and androgens in mediating sexual receptivity of rodents. Brain Research Reviews 2001, 37:201-222.
18. Frye C.A. Neurosteroids' effects and mechanisms for social, cognitive, emotional, and physical functions. Psychoneuroendocrinology 2009, 34:S143-S161.
19. Cheng Y.J., Karavolas H.J. 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 1973, 93:1157-1162.
20. Frye C.A., Vongher J.M. Progestins' rapid facilitation of lordosis when applied to the ventral tegmentum corresponds to efficacy at enhancing GABA(A)receptor activity. Journal of Neuroendocrinology 1999, 11:829-837.
21. Agis-Balboa R.C., et al. Down-regulation of neurosteroid biosynthesis in corticolimbic circuits mediates social isolation-induced behavior in mice. Proceedings of the National Academy of Science 2007, 1873:6-18741.
22. Pinna G., Agis-Balboa R.C., Pibiri F., Nelson M., Guidotti A., Costa E. Neurosteroid biosynthesis regulates sexually dimorphic fear and aggressive behavior in mice (Review). Neurochemical Research 2008, 33:1990-2007.
23. Iswari S., Colas A.E., Karavolas H.J. Binding of 5adihydroprogesterone and other progestins to female rat anterior pituitary nuclear extracts. Steroids 1986, 47:189-203.
24. Lambert J.J., Belelli D., Peden D.R., Vardy A.W., Peters J.A. Neurosteroid modulation of GABAA receptors. Progress in Neurobiology 2003, 71:67-80.
25. O'Malley B.W., McGuire W.L. Studies on the mechanism of estrogen-mediated tissue differentiation: regulation of nuclear transcription and induction of new RNA species. Proceedings of the National Academy of Sciences of the United States of America 1968, 60:1527-1534.
26. Pluchino N., Luisi M., Lenzi E., Centofanti M., Begliuomini S., Freschiet L., et al. Progesterone and progestins: effects on brain, allopregnanolone and β-endorphin. Journal of Steroid Biochemistry and Molecular Biology 2006, 102:205-213.
27. Rupprecht R., Zwanzger P. Significance of GABAA receptors for the pathophysiology and therapy of panic disorders. Nervenarzt 2003, 74:543-551.
28. Smith H.E., Smith R.G., Toft D.O., Neegard J.R., Burrows E.P., O'Malley B.W. Binding of steroids to progesterone receptor proteins in chick oviduct and human uterus. Journal of Biological Chemistry 1974, 249:5924-5932.
29. Corpéchot C., Collins B.E., Carey M.P., Tsouros A., Robel P., Fry J.P. Brain neurosteroids during the mouse oestrous cycle. Brain Research 1997, 766:276-280.
30. Gangitano D., Salas R., Teng Y., Perez E., De Biasi M. Progesterone modulation of α5 nAChR subunits influences anxiety-related behavior during estrus cycle. Genes, Brain and Behavior 2009, 8:398-406.
31. Gouveia A., dos Santos U.D., Felisbino F.E., de Afonseca T.L., Antunes G., Morato S. Influence of the estrous cycle on the behavior of rats in the elevated T-maze. Behavioural Processes 2004, 67:167-171.
32. Koonce C.J., Walf A.A., Frye C.A. Type 1 5α-reductase may be required for estrous cycle changes in affective behaviors of female mice. Behavioural Brain Research 2012, 226:376-380.
33. Lovick T.A. Estrous cycle and stress: influence of progesterone on the female brain. Brazilian Journal of Medical and Biological Research 2012, 45:314-320.
34. Mora S., Dussaubat N., Diaz-Veliz G. Effects of the estrous cycle and ovarian hormones on behavioral indices of anxiety in female rats. Psychoneuroendocrinology 1996, 21:609-620.
35. Reddy D.S., Kulkarni S.K. Sex and estrous cycle-dependent changes in neurosteroid and benzodiazepine effects on food consumption and plus-maze learning behaviors in rats. Pharmacology Biochemistry and Behavior 1999, 62:53-60.
36. Walf A.A., Koonce C., Manley K., Frye C.A. Proestrous compared to diestrous wildtype, but not estrogen receptor beta knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze. Behavioural Brain Research 2009, 196:254-260.
37. Frye C.A., Walf A.A. Estrogen and/or progesterone administered systemically or to the amygdala can have anxiety-, fear-, and pain-reducing effects in ovariectomized rats. Behavioral Neuroscience 2004, 118:306-313.
38. Frye C.A., Rhodes M.E. Estrogen-priming can enhance progesterone's anti-seizure effects in part by increasing hippocampal levels of allopregnanolone. Pharmacology Biochemistry and Behavior 2005, 81:907-916.
39. Chikahisa S., Sano A., Kitaoka K., Miyamoto K., Sei H. Anxiolytic effect of music depends on ovarian steroid in female mice. Behavioural Brain Research 2007, 179:50-59.
40. Frye C.A., Walf A.A. Changes in progesterone metabolites in the hippocampus can modulate open field and forced swim test behavior of proestrous rats. Hormones and Behavior 2002, 41(3):306-315.
41. Reddy D.S., O'Malley B.W., Rogawski M.A. Anxiolytic activity of progesterone in progesterone receptor knockout mice. Neuropharmacology 2005, 48:14-24.
42. Walf A.A., Sumida K., Frye C.A. Inhibiting 5α-reductase in the amygdala attenuates antianxiety and antidepressive behavior of naturally receptive and hormone-primed ovariectomized rats. Psychopharmacology (Berl). 2006, 186:302-311.
43. Mahendroo M.S., Cala K.M., Russell D.W. 5α-reduced androgens play a key role in murine parturition. Molecular Endocrinology 1996, 10:380-392.
44. Mahendroo M.S., Cala K.M., Landrum D.P., Russell D.W. Fetal death in mice lacking 5α-reductase type 1 caused by estrogen excess. Molecular Endocrinology 1997, 11:917-927.
45. Frye C.A., Walf A.A., Rhodes M.E., Harney J.P. Progesterone enhances motor, anxiolytic, analgesic, and antidepressive behavior of wild-type mice, but not those deficient in type 1 5α-reductase. Brain Research 2004, 1004:116-124.
46. Frye C.A., Koonce C.J., Walf A.A. Unlike medroxyprogesterone acetate, progesterone to C57BL/6, but not 5α-reductase mutant, mice enhances object recognition and placement memory and does not decrease BDNF levels in the hippocampus and cortex. Neuroscience Letters 2013, 10.1016/j.neulet.2013.07.002.
47. Walf A.A., Koonce C.J., Frye C.A. Estradiol or diarylpropionitrile decrease anxiety-like behavior of wildtype, but not estrogen receptor beta knockout, mice. Behavioral Neuroscience 2008, 122:974-981.
48. Walf A.A., Frye C.A. A review and update of mechanisms of estrogen in the hippocampus and amygdala for anxiety and depression behavior. Neuropsychopharmacology 2006, 31:1097-1111. (Review).
49. Frye C.A. Ichiro Sora Progesterone reduces hyperactivity of female and male dopamine transporter knockout mice. Behavioural Brain Research 2010, 209:59-65.
50. Llaneza D.C., Frye C.A. Progestogens and estrogen influence impulsive burying and avoidant freezing behavior of naturally cycling and ovariectomized rats. Pharmacology Biochemistry and Behavior 2009, 93:337-342.
51. Ciriza I., Carrero P., Frye C.A., Garcia-Segura L.M. Reduced metabolites mediate neuroprotective effects of progesterone in the adult rat hippocampus. The synthetic progestin medroxyprogesterone acetate (Provera) is not neuroprotective. Journal of Neurobiology 2006, 66:916-928.
52. Braden B.B., Talboom J.S., Crain I.D., Simard A.R., Lukas R.J., Prokai L., Scheldrup M.R., Bowman B.L., Bimonte-Nelson H.A. Medroxyprogesterone acetate impairs memory and alters the GABAergic system in aged surgically menopausal rats. Neurobiology of Learning and Memory 2010, 93:444-453.
53. Frye C.A., Walf A.A., Paris J.J. Conjugated equine estrogen, with medroxyprogesterone acetate, enhances formation of 5α-reduced progestogens and reduces anxiety-like behavior of middle-aged rats. Behavioural Pharmacology 2010, 21:530-539.
54. Reddy D.S., Kulkarni S.K. Differential anxiolytic effects of neurosteroids in the mirrored chamber behavior test in mice. Brain Research 1997, 752:61-71.
55. Rodgers R.J., Johnson N.J. Behaviorally selective effects of neuroactive steroids on plus-maze anxiety in mice. Pharmacology Biochemistry and Behavior 1998, 59:221-232.
56. Wieland S., Lan N.C., Mirasedeghi S., Gee K.W. Anxiolytic activity of the progesterone metabolite 5α-pregnan-3α-o1-20-one. Brain Research 1991, 565:263-268.
57. Finn D.A., Roberts A.J., Long S., Tanchuck M., Phillips T.J. Neurosteroid consumption has anxiolytic effects in mice. Pharmacology Biochemistry and Behavior 2003, 76:451-462.
58. Mòdol L., Darbra S., Pallarès M. Neurosteroids infusion into the CA1 hippocampal region on exploration, anxiety-like behaviour and aversive learning. Behavioural Brain Research 2011, 222:223-229.
59. Rhodes M.E. Frye CA Inhibiting progesterone metabolism in the hippocampus of rats in behavioral estrus decreases anxiolytic behaviors and enhances exploratory and antinociceptive behaviors. Cognitive, Affective, & Behavioral Neuroscience 2001, 1:287-296.
60. Jensen E.V., Jacobson H.I., Walf A.A. Frye CA Review Estrogen action: a historic perspective on the implications of considering alternative approaches. Physiology & Behavior 2010, 99:151-162.
61. Genazzani A.R., Petraglia F., Bernardi F., Casarosa E., Salvestroni C., Tonetti A., Nappi R.E., Luisi S., Palumbo M., Purdy R.H., Luisi M. Circulating levels of allopregnanolone in humans: gender, age, and endocrine influences. Journal of Clinical Endocrinology and Metabolism 1998, 83:2099-2103.
62. Sundström I., Bäckström T. Citalopram increases pregnanolone sensitivity in patients with premenstrual syndrome: an open trial. Psychoneuroendocrinology 1998, 23:73-88.
63. Wang M., Seippel L., Purdy R.H., Bãckström T. Relationship between symptom severity and steroid variation in women with premenstrual syndrome: study on serum pregnenolone, pregnenolone sulfate, 5α-pregnane-3,20-dione and 3α-hydroxy-5α-pregnan-20-one. Journal of Clinical Endocrinology and Metabolism 1996, 81:1076-1082.
64. Markou A., Duka T., Prelevic G.M. Estrogens and brain function. Hormones (Athens) 2005, 4:9-17.
65. Pearlstein T., Yonkers K.A., Fayyad R., Gillespie J.A. Pretreatment pattern of symptom expression in premenstrual dysphoric disorder. Journal of Affective Disorders 2005, 85:275-282.
66. Rapkin A.J., Mikacich J.A., Moatakef-Imani B., Rasgon N. The clinical nature and formal diagnosis of premenstrual, postpartum, and perimenopausal affective disorders. Current Psychiatry Reports 2002, 4:419-428.
67. Ströhle A., Romeo E., di Michele F., Pasini A., Hermann B., Gajewsky G., Holsboer F., Rupprecht R. Induced panic attacks shift gamma-aminobutyric acid type A receptor modulatory neuroactive steroid composition in patients with panic disorder: preliminary results. Archives of General Psychiatry 2003, 60:161-168.
68. Eser D., di Michele F., Zwanzger P., Pasini A., Baghai T.C., Schüle C., Rupprecht R., Romeo E. Panic induction with cholecystokinin-tetrapeptide (CCK-4) Increases plasma concentrations of the neuroactive steroid 3α,5α tetrahydrodeoxycorticosterone (3α,5α-THDOC) in healthy volunteers. Neuropsychopharmacology 2005, 30:192-195.
69. Tait G.R., McManus K., Bellavance F., Lara N., Chrapko W., Le Mellédo J.M. Neuroactive steroid changes in response to challenge with the panicogenic agent pentagastrin. Psychoneuroendocrinology 2002, 27:417-429.
70. Zwanzger P., Eser D., Padberg F., Baghai T.C., Schüle C., Rupprecht R., di Michele F., Romeo E., Pasini A., Ströhle A. Neuroactive steroids are not affected by panic induction with 50 microg cholecystokinin-tetrapeptide (CCK-4) in healthy volunteers. Journal of Psychiatric Research 2004, 38:215-217.
71. Girdler S.S., Straneva P.A., Light K.C., Pedersen C.A., Morrow A.L. Allopregnanolone levels and reactivity to mental stress in premenstrual dysphoric disorder. Biological Psychiatry 2001, 49:788-797.
72. Pearlstein T.B. Hormones and depression: what are the facts about premenstrual syndrome, menopause, and hormone replacement therapy. American Journal of Obstetrics and Gynecology 1995, 173:646-653.
73. Sitruk-Ware R. Progestins in hormonal replacement therapy and prevention of endometrial disease. Progestins and Antiprogestins in Clincial Practice 2000, 269-277. Marcel Dekker Inc., New York. R. Sitruk-Ware, D.R. Mischell (Eds.).
74. Beresford S.A., Weiss N.S., Voigt L.F., McKnight B. Risk of endometrial cancer in relation to use of oestrogen combined with cyclic progestagen therapy in postmenopausal women. Lancet 1997, 349:458-461.
75. Nilsen J., Brinton R.D. Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase signaling. Proceedings of the National Academy of Sciences of the United States of America 2003, 100:10506-10511.
76. Singh M., Su C. Progesterone, brain-derived neurotrophic factor and neuroprotection. Neuroscience 2013, 239:84-91. 2013.
77. Bernardi F., Pluchino N., Pieri M., Begliuomini S., Lenzi E., Puccetti S., Casarosa E., Luisi M., Genazzani A.R. Progesterone and medroxyprogesterone acetate effects on central and peripheral allopregnanolone and beta-endorphin levels. Neuroendocrinology 2006, 83:348-359.
78. A receptors. Journal of Neuroendocrinology 1995, 7:171-177.