Hormonal changes and increased anxiety-like behavior in a perimenopause-animal model induced by 4-vinylcyclohexene diepoxide (VCD) in female rats

Psychoneuroendocrinology

Volumn 49, Issue 1, 2014, Pages 130-140

  Reis, FMCV ^a,c   Pestana Oliveira, N ^a   Leite, C M ^a   Lima, F B ^b   Brandao M L ^a,c   Graeff, F G ^a,c   Del Ben, C M ^a   Anselmo Franci, J A ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b FEDERAL UNIVERSITY OF SANTA CATARINA   (Brazil)

^c Campus USP   (Brazil)

Author keywords

Anxiety; DHT; Estradiol; Follicular depletion; FSH; Glucocorticoids; Perimenopause; Progesterone; Testosterone

Indexed keywords

4 VINYLCYCLOHEXENE DIEPOXIDE; ANDROSTANOLONE; CORTICOSTERONE; ESTRADIOL; FOLLITROPIN; INDUSTRIAL CHEMICAL; PROGESTERONE; TESTOSTERONE; UNCLASSIFIED DRUG; 4-VINYL-1-CYCLOHEXENE DIOXIDE; CYCLOHEXENE DERIVATIVE; VINYL DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY DISORDER; ARTICLE; CLIMACTERIUM; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DIESTRUS; ELEVATED PLUS MAZE TEST; ESTRADIOL BLOOD LEVEL; EXPLORATORY BEHAVIOR; FEMALE; FOLLITROPIN BLOOD LEVEL; NONHUMAN; OVARY FOLLICLE ATRESIA; OVARY INSUFFICIENCY; PROESTRUS; PROGESTERONE BLOOD LEVEL; RAT; TESTOSTERONE BLOOD LEVEL; ANIMAL; ANXIETY; BLOOD; CHEMICALLY INDUCED; DISEASE MODEL; DRUG EFFECTS; ESTRUS CYCLE; MAZE TEST; OVARY FOLLICLE; PREMATURE OVARIAN FAILURE; PSYCHOLOGY;

ANIMALS; ANXIETY; CORTICOSTERONE; CYCLOHEXENES; DIHYDROTESTOSTERONE; DISEASE MODELS, ANIMAL; ESTRADIOL; ESTROUS CYCLE; FEMALE; FOLLICLE STIMULATING HORMONE; MAZE LEARNING; OVARIAN FOLLICLE; PERIMENOPAUSE; PRIMARY OVARIAN INSUFFICIENCY; PROGESTERONE; RATS; TESTOSTERONE; VINYL COMPOUNDS;

EID: 84922433434     PISSN: 03064530     EISSN: 18733360     Source Type: Journal    
DOI: 10.1016/j.psyneuen.2014.06.019     Document Type: Article

References (66)

1. Acosta J.I., Mayer L., Talboom J.S., Tsang C.W., Smith C.J., Enders C.K., Bimonte-Nelson H.A. Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology 2009, 150:4248-4259.
2. Albrechet-Souza L., Cristina de Carvalho M., Rodrigues Franci C., Brandão M.L. Increases in plasma corticosterone and stretched-attend postures in rats naive and previously exposed to the elevated plus-maze are sensitive to the anxiolytic-like effects of midazolam. Horm. Behav. 2007, 52:267-273.
3. Anseloni V.Z., Brandão M.L. Ethopharmacological analysis of behaviour of rats using variations of the elevated plus-maze. Behav. Pharmacol. 1997, 8:533-540.
4. Bethea C.L., Lu N.Z., Gundlah C., Streicher J.M. Diverse actions of ovarian steroids in the serotonin neural system. Front. Neuroendocrinol. 2002, 23:41-100.
5. Bethea C.L., Pecins-Thompson M., Schutzer W.E., Gundlah C., Lu Z.N. Ovarian steroids and serotonin neural function. Mol. Neurobiol. 1998, 18:87-123.
6. Blanchard D.C., Griebel G., Blanchard R.J. Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic. Neurosci. Biobehav. Rev. 2001, 25:205-218.
7. Blanchard D.C., Hynd A.L., Minke K.A., Minemoto T., Blanchard R.J. Human defensive behaviors to threat scenarios show parallels to fear- and anxiety-related defense patterns of non-human mammals. Neurosci. Biobehav. Rev. 2001, 25:761-770.
8. Bromberger J.T., Meyer P.M., Kravitz H.M., Sommer B., Cordal A., Powell L., Ganz P.A., Sutton-Tyrrell K. Psychologic distress and natural menopause: a multiethnic community study. Am. J. Public Health 2001, 91:1435-1442.
9. Bryant C., Judd F.K., Hickey M. Anxiety during the menopausal transition: a systematic review. J. Affect Disord. 2012, 139:141-148.
10. Buddenberg T.E., Komorowski M., Ruocco L.A., Silva M.A., Topic B. Attenuating effects of testosterone on depressive-like behavior in the forced swim test in healthy male rats. Brain Res. Bull. 2009, 79:182-186.
11. Burger H.G., Cahir N., Robertson D.M., Groome N.P., Dudley E., Green A., Dennerstein L. Serum inhibins A and B fall differentially as FSH rises in perimenopausal women. Clin. Endocrinol. (Oxf) 1998, 48:809-813.
12. Burger H.G., Dudley E.C., Hopper J.L., Shelley J.M., Green A., Smith A., Dennerstein L., Morse C. The endocrinology of the menopausal transition: a cross-sectional study of a population-based sample. J. Clin. Endocrinol. Metab. 1995, 80:3537-3545.
13. Chen J., Sowers M.R., Moran F.M., McConnell D.S., Gee N.A., Greendale G.A., Whitehead C., Kasim-Karakas S.E., Lasley B.L. Circulating bioactive androgens in midlife women. J. Clin. Endocrinol. Metab. 2006, 91:4387-4394.
14. Cui J., Shen Y., Li R. Estrogen synthesis and signaling pathways during aging: from periphery to brain. Trends Mol. Med. 2013, 19:197-209.
15. Deecher D., Andree T.H., Sloan D., Schechter L.E. From menarche to menopause: exploring the underlying biology of depression in women experiencing hormonal changes. Psychoneuroendocrinology 2008, 33:3-17.
16. Dupon C., Kim M.H. Peripheral plasma levels of testosterone, androstenedione, and oestradiol during the rat oestrous cycle. J. Endocrinol. 1973, 59:653-654.
17. Figueiredo H.F., Dolgas C.M., Herman J.P. Stress activation of cortex and hippocampus is modulated by sex and stage of estrus. Endocrinology 2002, 143:2534-2540.
18. Freeman E.W., Sammel M.D., Gracia C.R., Kapoor S., Lin H., Liu L., Nelson D.B. Follicular phase hormone levels and menstrual bleeding status in the approach to menopause. Fertil. Steril. 2005, 83:383-392.
19. Freeman E.W., Sammel M.D., Lin H., Gracia C.R., Kapoor S., Ferdousi T. The role of anxiety and hormonal changes in menopausal hot flashes. Menopause 2005, 12:258-266.
20. Freeman E.W., Sammel M.D., Lin H., Gracia C.R., Kapoor S. Symptoms in the menopausal transition: hormone and behavioral correlates. Obstet. Gynecol. 2008, 111:127-136.
21. Frye C.A., Seliga A.M. Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn. Affect. Behav. Neurosci. 2001, 1:371-381.
22. Gee K.W. Steroid modulation of the GABA/benzodiazepine receptor-linked chloride ionophore. Mol. Neurobiol. 1988, 2:291-317.
23. Hale G.E., Hughes C.L., Burger H.G., Robertson D.M., Fraser I.S. Atypical estradiol secretion and ovulation patterns caused by luteal out-of-phase (LOOP) events underlying irregular ovulatory menstrual cycles in the menopausal transition. Menopause 2009, 16:50-59.
24. Harlow S.D., Gass M., Hall J.E., Lobo R., Maki P., Rebar R.W., Sherman S., Sluss P.M., de Villiers T.J. Executive summary of the Stages of Reproductive Aging Workshop +10: addressing the unfinished agenda of staging reproductive aging. Menopause 2012, 19:387-395.
25. Hoyer P.B., Devine P.J., Hu X., Thompson K.E., Sipes I.G. Ovarian toxicity of 4-vinylcyclohexene diepoxide: a mechanistic model. Toxicol. Pathol. 2001, 29:91-99.
26. Imhof J.T., Coelho Z.M., Schmitt M.L., Morato G.S., Carobrez A.P. Influence of gender and age on performance of rats in the elevated plus maze apparatus. Behav. Brain Res. 1993, 56:177-180.
27. Kalil B., Leite C.M., Carvalho-Lima M., Anselmo-Franci J.A. Role of sex steroids in progesterone and corticosterone response to acute restraint stress in rats: sex differences. Stress 2013, 16:452-460.
28. Kermath B.A., Gore A.C. Neuroendocrine control of the transition to reproductive senescence: lessons learned from the female rodent model. Neuroendocrinology 2012, 96:1-12.
29. Kontogianni M.D., Dafni U.G., Routsias J.G., Skopouli F.N. Blood leptin and adiponectin as possible mediators of the relation between fat mass and BMD in perimenopausal women. J. Bone Miner. Res. 2004, 19:546-551.
30. Lohff J.C., Christian P.J., Marion S.L., Arrandale A., Hoyer P.B. Characterization of cyclicity and hormonal profile with impending ovarian failure in a novel chemical-induced mouse model of perimenopause. Comp. Med. 2005, 55:523-527.
31. Lukefahr A.L., Frye J.B., Wright L.E., Marion S.L., Hoyer P.B., Funk J.L. Decreased bone mineral density in rats rendered follicle-deplete by an ovotoxic chemical correlates with changes in follicle-stimulating hormone and inhibin A. Calcif. Tissue Int. 2012, 90:239-249.
32. Marcondes F.K., Miguel K.J., Melo L.L., Spadari-Bratfisch R.C. Estrous cycle influences the response of female rats in the elevated plus-maze test. Physiol. Behav. 2001, 74:435-440.
33. Mayer L.P., Devine P.J., Dyer C.A., Hoyer P.B. The follicle-deplete mouse ovary produces androgen. Biol. Reprod. 2004, 71:130-138.
34. Mayer L.P., Pearsall N.A., Christian P.J., Devine P.J., Payne C.M., McCuskey M.K., Marion S.L., Sipes I.G., Hoyer P.B. Long-term effects of ovarian follicular depletion in rats by 4-vinylcyclohexene diepoxide. Reprod. Toxicol. 2002, 16:775-781.
35. 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.
36. Morgan M.A., Pfaff D.W. Estrogen's effects on activity, anxiety, and fear in two mouse strains. Behav. Brain Res. 2002, 132:85-93.
37. Muhammad F.S., Goode A.K., Kock N.D., Arifin E.A., Cline J.M., Adams M.R., Hoyer P.B., Christian P.J., Isom S., Kaplan J.R., Appt S.E. Effects of 4-vinylcyclohexene diepoxide on peripubertal and adult Sprague-Dawley rats: ovarian, clinical, and pathologic outcomes. Comp. Med. 2009, 59:46-59.
38. Munday M.R., Brush M.G., Taylor R.W. Correlations between progesterone oestradiol and aldosterone levels in the premenstrual syndrome. Clin. Endocrinol. (Oxf.) 1981, 14:1-9.
39. Nomikos G.G., Spyraki C. Influence of oestrogen on spontaneous and diazepam-induced exploration of rats in an elevated plus maze. Neuropharmacology 1988, 27:691-696.
40. O'Connor K.A., Ferrell R., Brindle E., Trumble B., Shofer J., Holman D.J., Weinstein M. Progesterone and ovulation across stages of the transition to menopause. Menopause 2009, 16:1178-1187.
41. Osborne D.M., Edinger K., Frye C.A. Chronic administration of androgens with actions at estrogen receptor beta have anti-anxiety and cognitive-enhancing effects in male rats. Age (Dordr) 2009, 31:191-198.
42. Pellow S., Chopin P., File S.E., Briley M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J. Neurosci. Methods 1985, 14:149-167.
43. Perkins A.M., Ettinger U., Davis R., Foster R., Williams S.C., Corr P.J. Effects of Lorazepam and citalopram on human defensive reactions: ethopharmacological differentiation of fear and anxiety. J. Neurosci. 2009, 29:12617-12624.
44. Piva F., Limonta P., Dondi D., Pimpinelli F., Martini L., Maggi R. Effects of steroids on the brain opioid system. J. Steroid Biochem. Mol. Biol. 1995, 53:343-348.
45. Prior J.C., Hitchcock C.L. The endocrinology of perimenopause: need for a paradigm shift. Front. Biosci. (Schol. Ed.) 2011, 3:474-486.
46. Reis F.M., Albrechet-Souza L., Franci C.R., Brandao M.L. Risk assessment behaviors associated with corticosterone trigger the defense reaction to social isolation in rats: role of the anterior cingulate cortex. Stress 2012, 15:318-328.
47. Reyes F.I., Winter J.S., Faiman C. Pituitary-ovarian relationships preceding the menopause. I. A cross-sectional study of serum follice-stimulating hormone, luteinizing hormone, prolactin, estradiol, and progesterone levels. Am. J. Obstet. Gynecol. 1977, 129:557-564.
48. Robichaud M., Debonnel G. Oestrogen and testosterone modulate the firing activity of dorsal raphe nucleus serotonergic neurones in both male and female rats. J. Neuroendocrinol. 2005, 17:179-185.
49. Rodgers R.J., Johnson N.J. Factor analysis of spatiotemporal and ethological measures in the murine elevated plus-maze test of anxiety. Pharmacol. Biochem. Behav. 1995, 52:297-303.
50. Rubin B.S. Hypothalamic alterations and reproductive aging in female rats: evidence of altered luteinizing hormone-releasing hormone neuronal function. Biol. Reprod. 2000, 63:968-976.
51. Rupprecht R. Neuroactive steroids: mechanisms of action and neuropsychopharmacological properties. Psychoneuroendocrinology 2003, 28:139-168.
52. Salonia A., Pontillo M., Nappi R.E., Zanni G., Fabbri F., Scavini M., Daverio R., Gallina A., Rigatti P., Bosi E., Bonini P.A., Montorsi F. Menstrual cycle-related changes in circulating androgens in healthy women with self-reported normal sexual function. J. Sex. Med. 2008, 5:854-863.
53. Santoro N., Brown J.R., Adel T., Skurnick J.H. Characterization of reproductive hormonal dynamics in the perimenopause. J. Clin. Endocrinol. Metab. 1996, 81:1495-1501.
54. Santoro N., Crawford S.L., Lasley W.L., Luborsky J.L., Matthews K.A., McConnell D., Randolph J.F., Gold E.B., Greendale G.A., Korenman S.G., Powell L., Sowers M.F., Weiss G. Factors related to declining luteal function in women during the menopausal transition. J. Clin. Endocrinol. Metab. 2008, 93:1711-1721.
55. Schmidt P.J., Rubinow D.R. Sex hormones and mood in the perimenopause. Ann. N.Y. Acad. Sci. 2009, 1179:70-85.
56. Seritan A.L., Iosif A.M., Park J.H., DeatherageHand D., Sweet R.L., Gold E.B. Self-reported anxiety, depressive, and vasomotor symptoms: a study of perimenopausal women presenting to a specialized midlife assessment center. Menopause 2010, 17:410-415.
57. Smith M.S., Freeman M.E., Neill J.D. The control of progesterone secretion during the estrous cycle and early pseudopregnancy in the rat: prolactin, gonadotropin and steroid levels associated with rescue of the corpus luteum of pseudopregnancy. Endocrinology 1975, 96:219-226.
58. Sowers M.R., Eyvazzadeh A.D., McConnell D., Yosef M., Jannausch M.L., Zhang D., Harlow S., Randolph J.F. Anti-mullerian hormone and inhibin B in the definition of ovarian aging and the menopause transition. J. Clin. Endocrinol. Metab. 2008, 93:3478-3483.
59. Szawka R.E., Poletini M.O., Leite C.M., Bernuci M.P., Kalil B., Mendonca L.B., Carolino R.O., Helena C.V., Bertram R., Franci C.R., Anselmo-Franci J.A. Release of norepinephrine in the preoptic area activates anteroventral periventricular nucleus neurons and stimulates the surge of luteinizing hormone. Endocrinology 2013, 154:363-374.
60. Toufexis D.J., Myers K.M., Davis M. The effect of gonadal hormones and gender on anxiety and emotional learning. Horm. Behav. 2006, 50:539-549.
61. van Weerden W.M., Bierings H.G., van Steenbrugge G.J., de Jong F.H., Schroder F.H. Adrenal glands of mouse and rat do not synthesize androgens. Life Sci. 1992, 50:857-861.
62. Welt C.K., McNicholl D.J., Taylor A.E., Hall J.E. Female reproductive aging is marked by decreased secretion of dimeric inhibin. J. Clin. Endocrinol. Metab. 1999, 84:105-111.
63. Wise P.M. Norepinephrine and dopamine activity in microdissected brain areas of the middle-aged and young rat on proestrus. Biol. Reprod. 1982, 27:562-574.
64. Woods N.F., Carr M.C., Tao E.Y., Taylor H.J., Mitchell E.S. Increased urinary cortisol levels during the menopausal transition. Menopause 2006, 13:212-221.
65. Woods N.F., Smith-Dijulio K., Percival D.B., Tao E.Y., Taylor H.J., Mitchell E.S. Symptoms during the menopausal transition and early postmenopause and their relation to endocrine levels over time: observations from the Seattle Midlife Women's Health Study. J. Womens Health (Larchmt) 2007, 16:667-677.
66. Zumoff B., Strain G.W., Miller L.K., Rosner W. Twenty-four-hour mean plasma testosterone concentration declines with age in normal premenopausal women. J. Clin. Endocrinol. Metab. 1995, 80:1429-1430.