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

Neuroscience Letters

Volumn 551, Issue , 2013, Pages 53-57

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

^a STATE UNIVERSITY OF NEW YORK   (United States)

^b UNIVERSITY OF ALASKA FAIRBANKS   (United States)

Author keywords

Brain derived neurotrophic factor (BDNF); Cognition; Hormone replacement therapy; Learning; Memory; Neurosteroids

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; BRAIN DERIVED NEUROTROPHIC FACTOR; MEDROXYPROGESTERONE ACETATE; NEUROSTEROID; PROGESTERONE; STEROID 5ALPHA REDUCTASE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEMALE; GENE INACTIVATION; GENOTYPE; HIPPOCAMPUS; HORMONE SUBSTITUTION; MEMORY; MENTAL PERFORMANCE; MOUSE; NERVE CELL GROWTH; NONHUMAN; OVARIECTOMY; PLACEMENT MEMORY; PREFRONTAL CORTEX; PRIORITY JOURNAL; RECOGNITION;

BRAIN DERIVED NEUROTROPHIC FACTOR (BDNF); COGNITION; HORMONE REPLACEMENT THERAPY; LEARNING; MEMORY; NEUROSTEROIDS;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; CHOLESTENONE 5 ALPHA-REDUCTASE; FEMALE; HIPPOCAMPUS; MEDROXYPROGESTERONE ACETATE; MEMORY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OVARIECTOMY; PREGNANOLONE; PROGESTERONE; RECOGNITION (PSYCHOLOGY);

EID: 84882236795     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2013.07.002     Document Type: Article

References (37)

1. Andreano J.M., Cahill L. Menstrual cycle modulation of medial temporal activity evoked by negative emotion. NeuroImage 2010, 53:1286-1293.
2. Belelli D., Herd M.B. The contraceptive agent Provera enhances GABA(A) receptor-mediated inhibitory neurotransmission in the rat hippocampus: evidence for endogenous neurosteroids?. J. Neurosci. 2003, 23:10013-10020.
3. Bimonte-Nelson H.A., Nelson M.E., Granholm A.C. Progesterone counteracts estrogen-induced increases in neurotrophins in the aged female rat brain. Neuroreport 2004, 15:2659-2663.
4. Brinton R.D., Thompson R.F., Foy M.R., Baudry M., Wang J., Finch C.E., Morgan T.E., Pike C.J., Mack W.J., Stanczyk F.Z., Nilsen J. Progesterone receptors: form and function in brain. Front. Neuroendocrinol. 2008, 29:313-339.
5. Christensen H., Leach L.S., Mackinnon A. Cognition in pregnancy and motherhood: prospective cohort study. Br. J. Psychiatry 2010, 196:126-132.
6. 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. J. Neurobiol. 2006, 66:916-928.
7. Franklin T.B., Perrot-Sinal.T.S. Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology 2006 Jan, 31(1):38-48.
8. Freeman E.W., Weinstock L., Rickels K., Sondheimer S.J., Coutifaris C. A placebo-controlled study of effects of oral progesterone on performance and mood. Br. J. Clin. Pharmacol. 1992, 33:293-298.
9. 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 5 alpha-reductase. Brain Res. 2004, 1004:116-124.
10. Frye C.A. Progestins influence motivation, reward, conditioning, stress, and/or response to drugs of abuse. Pharmacol. Biochem. Behav. 2007, 86:209-219.
11. Frye C.A., Koonce C.J., Walf A.A. Mnemonic effects of progesterone to mice require formation of 3α,5α-THP. Neuroreport 2010, 21:590-595.
12. Frye C.A., Walf A.A., Paris J.J. Conjugated equine estrogen, with medroxyprogesterone acetate, enhances formation of 5alpha-reduced progestogens and reduces anxiety-like behavior of middle-aged rats. Behav. Pharmacol. 2010, 21:530-539.
13. Gibbs R.B. Treatment with estrogen and progesterone affects relative levels of brain-derived neurotrophic factor mRNA and protein in different regions of the adult rat brain. Brain Res. 1999, 844:20-27.
14. Henry J.D., Rendell P.G. A review of the impact of pregnancy on memory function. J. Clin. Exp. Neuropsychol. 2007, 29:793-803.
15. Hogervorst E., Yaffe K., Richards M., Huppert F. Hormone replacement therapy to maintain cognitive function in women with dementia. Cochrane Database Syst. Rev. 2002, 3:CD003799.
16. Jodhka P.K., Kaur P., Underwood W., Lydon J.P., Singh M. The differences in neuroprotective efflcacy of progesterone and medroxyprogesterone acetate correlate with their effects on bdnf expression. Endocrinology 2009, 150:3162-3168.
17. 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. Behav. Brain Res. 2012, 226:376-380.
18. 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. Mol. Endocrinol. 1997, 11:917-927.
19. Mahendroo M.S., Cala K.M., Russell D.W. 5α-reduced androgens play a key role in murine parturition. Mol. Endocrinol. 1996, 10:380-392.
20. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 1986, 232:1004-1007.
21. Maki P.M. A systematic review of clinical trials of hormone therapy on cognitive function: effects of age at initiation and progestin use. Ann. N.Y. Acad. Sci. 2005, 1052:182-197.
22. Paris J.J., Walf A.A., Frye C.A. Cognitive performance of middle-aged female rats is influenced by capacity to metabolize progesterone in the prefrontal cortex and hippocampus. Brain Res. 2011, 1379:149-163.
23. Pazol K., Northcutt K.V., Patisaul H.B., Wallen K., Wilson M.E. Progesterone and medroxyprogesterone acetate differentially regulate α4 subunit expression of gaba(a) receptors in the ca1 hippocampus of female rats. Physiol. Behav. 2009, 97:58-61.
24. Pearson B.E., Allison C.M. Determination of progesterone and some of its neuroactive ring a-reduced metabolites in human serum. J. Steroid Biochem. Mol. Biol. 2000, 74:137-142.
25. Phillips S.M., Sherwin B.B. Variations in memory function and sex steroid hormones across the menstrual cycle. Psychoneuroendocrinology 1992, 17:497-506.
26. Rapp S.R., Espeland M.A., Shumaker S.A., Henderson V.W., Brunner R.L., Manson J.E., Gass M.L., Stefanick M.L., Lane D.S., Hays J., Johnson K.C., Coker L.H., Dailey M., Bowen D., WHIMS Investigators Effect of estrogen plus progestin on global cognitive function in postmenopausal women: the women's health initiative memory study: a randomized controlled trial. JAMA 2003, 289:2663-2672.
27. Schüssler P., Kluge M., Yassouridis A., Dresler M., Held K., Zihl J., Steiger A. Progesterone reduces wakefulness in sleep eeg and has no effect on cognition in healthy postmenopausal women. Psychoneuroendocrinology 2008, 33:1124-1131.
28. Singh M., Meyer E.M., Simpkins J.W. The effect of ovariectomy and estradiol replacement on brain-derived neurotrophic factor messenger ribonucleic acid expression in cortical and hippocampal brain regions of female Sprague-Dawley rats. Endocrinology 1995, 136:2320-2324.
29. Singh M., Su C. Progesterone, brain-derived neurotrophic factor and neuroprotection. Neuroscience 2013, 239:84-91.
30. Söderpalm A.H., Lindsey S., Purdy R.H., Hauger R., deWit H. Administration of progesterone produces mild sedative-like effects in men and women. Psychoneuroendocrinology 2004, 29:339-354.
31. Sofuoglu M., Mouratidis M., Mooney M. Progesterone improves cognitive performance and attenuates smoking urges in abstinent smokers. Psychoneuroendocrinology 2010, 36:123-132.
32. Solis-Ortiz S., Corsi-Cabrera M. Sustained attention is favored by progesterone during early luteal phase and visuo-spatial memory by estrogens during ovulatory phase in young women. Psychoneuroendocrinology 2008, 33:989-998.
33. Stein D.G. Progesterone in the treatment of acute traumatic brain injury: a clinical perspective and update. Neuroscience 2011, 191:101-106.
34. 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. Behav. Brain Res. 2009, 196:254-260.
35. Walf A.A., Koonce C.J., Frye C.A. Estradiol or diarylpropionitrile administration to wild type, but not estrogen receptor beta knockout, mice enhances performance in the object recognition and object placement tasks. Neurobiol. Learn. Membr. 2008, 89:513-521.
36. van Wingen, van Broekhoven Verkes R.J., Petersson K.M., Backstrom T., Buitelaar J.K., Fernandez G. Progesterone selectively increases amygdala reactivity in women. Mol. Psychiatry 2008, 13:325-333.
37. van Wingen G., van Broekhoven F., Verkes R.J., Petersson K.M., Bäckström T., Buitelaar J., Fernández G. How progesterone impairs memory for biologically salient stimuli in healthy young women. J. Neurosci. 2007, 27:11416-11423.