Accelerated ovarian failure: A novel, chemically induced animal model of menopause

Brain Research

Volumn 1379, Issue , 2011, Pages 176-187

  Van Kempen, Tracey A ^a   Milner, Teresa A ^a,b   Waters, Elizabeth M ^b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Estrogen; Hormone replacement therapy; Perimenopause

Indexed keywords

4 VINYLCYCLOHEXENE DIEPOXIDE; CARCINOGEN; EPOXIDE; ESTROGEN; FOLLITROPIN; GONADORELIN; UNCLASSIFIED DRUG;

AGING; BRAIN DAMAGE; CARDIOVASCULAR DISEASE; CELL DEATH; CELL POPULATION; CLIMACTERIUM; ENCEPHALITIS; FERTILITY; GENETICS; KIDNEY DISEASE; KNOCKOUT MOUSE; LIVER; MEMORY DISORDER; MENOPAUSE; METABOLIC SYNDROME X; MOOD DISORDER; NEUROPROTECTION; NONHUMAN; OSTEOLYSIS; OVARIECTOMY; OVARY; OVARY CANCER; OVARY FOLLICLE; OVARY INSUFFICIENCY; POSTMENOPAUSE; PRIORITY JOURNAL; REVIEW; RODENT; SPLEEN; TOXICOLOGY;

ANIMALS; CYCLOHEXENES; FEMALE; HUMANS; MENOPAUSE; MODELS, ANIMAL; OVARIECTOMY; POSTMENOPAUSE; PRIMARY OVARIAN INSUFFICIENCY; TIME FACTORS; VINYL COMPOUNDS;

ANIMALIA; MUS; RODENTIA;

EID: 79952316517     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2010.12.064     Document Type: Review

References (70)

1. Acosta, J.I., Mayer, L., Talboom, J.S., Tsang, C.W., Smith, C.J., Enders, C.K., Bimonte-Nelson, H.A., 2009. Transitional versus surgical menopause in a rodent model: etiology of ovarian hormone loss impacts memory and the acetylcholine system. Endocrinology 150, 4248-4259.
2. Acosta, J.I., Mayer, L.P., Braden, B.B., Nonnenmacher, S., Mennenga, S.E., Bimonte-Nelson, H.A., 2010. The cognitive effects of conjugated equine estrogens depend on whether menopause etiology is transitional or surgical. Endocrinology 151, 3795-3804.
3. Appt, S.E., Kaplan, J.R., Clarkson, T.B., Cline, J.M., Christian, P.J., Hoyer, P.B., 2006. Destruction of primordial ovarian follicles in adult cynomolgus macaques after exposure to 4-vinylcyclohexene diepoxide: a nonhuman primate model of the menopausal transition. Fertil. Steril. 86, 1210-1216.
4. Borman, S.M., Van De Pol, B.J., Kao, S., Thompson, K.E., Sipes, I.G., Hoyer, P.B., 1999. A single dose of the ovotoxicant 4 -vinylcyclohexene diepoxide is protective in rat primary ovarian follicles. Toxicol. Appl. Pharm. 158, 244-252.
5. Bulloch, K., Miller, M.M., Gal-Toth, J., Milner, T.A., Bottfried-Blackmore, A., Waters, E.M., Kaunzer, U.W., Liu, K., Lindquist, R., Nussenzweig, M.C., Steinman, R.M., McEwen, B.S., 2008. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult, and injured mouse brain. J. Comp. Neurol. 508, 687-710.
6. Cannady, E.A., Dyer, C.A., Christian, P.J., Sipes, I.G., Hoyer, P.B., 2003. Expression and activity of cytochromes P450 2E1, 2A, and 2B in the mouse ovary: the effect of 4-vinylcyclohexene and its diepoxide metabolite. Toxicol. Sci. 73, 423-430.
7. Chakraborty, T.R., Gore, A.C., 2004. Aging-related changes in ovarian hormones, their receptors, and neuroendocrine function. Exp. Biol. Med. 229, 977-987.
8. Chung, D.W., Yoo, K.-Y., Hwang, I.K., Kim, D.W., Chung, J.Y., Lee, C.H., Choi, J.H., Choi, S.Y., Youn, H.Y., Lee, I.S., Won, M.-H., 2010. Systemic administration of lipopolysaccharide induces cyclooxygenase-2 immunoreactivity in endothelium and increases microglia in the mouse hippocampus. Cell. Mol. Neurobiol. 30, 531-541.
9. Cohen, P.E., Milligan, S.R., 1993. Silastic implants for delivery of oestradiol to mice. J. Reprod. Fertil. 99, 219-223.
10. Craig, Z.R., Davis, J.R., Marion, S.L., Barton, J.K., Hoyer, P.B., 2010. 7,12-Dimethylbenz[a]anthracene induces Sertoli-Leydig-cell tumors in the follicle-depleted ovaries of mice treated with 4-vinylcyclohexene diepoxide. Comp. Med. 60, 10-17.
11. Danliovich, N., Ram, S.M., 2006. Recent female mouse models displaying advanced reproductive aging. Exp. Gerontol. 41, 117-122.
12. Davison, S.L., Bell, R., Donath, S., Montalto, J.G., Davis, S.R., 2005. Androgen levels in adult females: changes with age, menopause, and oophorectomy. J. Clin. Endocrinol. Metab. 90, 3847-3853.
13. Devine, P.J., Sipes, I.G., Hoyer, P.B., 2001. Effect of 4-vinylcyclohexene diepoxide dosing in rats on GSH levels in liver and ovaries. Toxicol. Sci. 62, 315-320.
14. Devine, P.J., Sipes, I.G., Skinner, M.K., Hoyer, P.B., 2002. Characterization of a rat in vitro ovarian culture system to study the ovarian toxicant 4-vinylcyclohexene diepoxide. Toxicol. Appl. Pharm. 184, 107-115.
15. Fogle, R.H., Stanczyk, F.Z., Zhang, X., Paulson, R.J., 2007. Ovarian androgen production in postmenopausal women. J. Clin. Endocrinol. Metab. 92, 3040-3043.
16. Frank, M.G., Baratta, M.V., Sprunger, D.B., Watkins, L.R., Maier, S.F., 2007. Microglia serve as a neuroimmune substrate for stress-induced potentiation of CNS pro-inflammatory cytokine responses. Brain Behav. Immun. 21, 47-59.
17. Frick, K.M., 2008. Estrogens and age-related memory decline in rodents: what have we learned and where do we go from here? Horm. Behav. 55, 2-23.
18. Golub, M.S., Germann, S.L., Mercer, M., Gordon, M.N., Morgan, D.G., Mayer, L.P., Hoyer, P.B., 2008. Behavioral consequences of ovarian atrophy and estrogen replacement in the APPswe mouse. Neurobiol. Aging 29, 1512-1523.
19. Gore, A.C., Oung, T., Woller, M.J., 2002. Age-related changes in hypothalamic gonadotropin-releasing hormone and N-methyl-D-aspartate receptor gene expression, and their regulation by oestrogen, in the female rat. J. Neuroendocrinol. 14, 300-309. (Pubitemid 34285299)
20. Greendale, G.A., Huang, M.-H., Wight, R.G., Seeman, T., Luetters, C., Avis, N.E., Johnston, J., Karlamangla, A.S., 2009. Effects of the menopause transition and hormone use on cognitive performance in midlife women. Neurology 72, 1850-1857.
21. Haas, J.R., Christian, P.J., Hoyer, P.B., 2007. Effects of impending ovarian failure induced by 4-vinylcyclohexene diepoxide on fertility in C57BL/6 female mice. Comp. Med. 57, 443-449.
22. Harsh, V., Meltzer-Brody, S., Rubinow, D.R., Schmidt, P.J., 2009. Reproductive aging, sex steroids, and mood disorders. Harv. Rev. Psychiat. 17, 87-102.
23. Havelock, J.C., Rainey, W.E., Bradshaw, K.D., Carr, B.R., 2006. The post-menopausal ovary displays a unique pattern of steroidogenic enzyme expression. Hum. Reprod. 21, 309-317.
24. Henderson, V.W., Benke, K.S., Green, R.C., Cuppes, L.A., Farrer, L.A., 2005. Postmenopausal hormone therapy and Azheimer's disease risk: interaction with age. J. Neurol. Neurosur. Ps. 76, 103-105.
25. Hoyer, P.B., Sipes, I.G., 1996. Assessment of follicle destruction in chemical-induced ovarian toxicity. Annu. Rev. Pharmacol. Toxicol. 36, 307-331.
26. Hoyer, P.B., Devine, P.J., Hu, X., Thompson, K.E., Sipes, I.G., 2001. Ovarian toxicity of 4-vinylcyclohexene diepoxide: a mechanistic model. Toxicol. Pathol. 29, 91-99.
27. Hoyer, P.B., Sipes, I.G., 2007. Development of an animal model for ovotoxicity using 4-vinylcyclohexene: a case study. Birth Defects Res. B 80, 113-125. (Pubitemid 46762320)
28. Hoyer, P.B., Davis, J.R., Bedrnicek, J.B., Marion, S.L., Christian, P.J., Barton, J.K., Brewer, M.A., 2009. Ovarian neoplasm development by 7,12-dimethylbenz[a]anthracene (DMBA) in a chemically-induced rat model of ovarian failure. Gynecol. Oncol. 112, 610-615.
29. Hu, X., Christian, P., Sipes, I.G., Hoyer, P.B., 2001a. Expression and redistribution of cellular Bad, Bax, and Bcl-X(L) protein is associated with VCD-induced ovotoxicity in rats. Biol. Reprod. 65, 1489-1495.
30. Hu, X., Christian, P.J., Thompson, K.E., Sipes, I.G., Hoyer, P.B., 2001b. Apoptosis induced in rats by 4-vinylcyclohexene diepoxide is associated with activation of the caspase cascades. Biol. Reprod. 65, 87-93.
31. Hu, X., Flaws, J.A., Sipes, I.G., Hoyer, P.B., 2002. Activation of mitogen-activated protein kinases and AP-1 transcription factor in ovotoxicity induced by 4-vinylcyclohexene diepoxide in rats. Biol. Reprod. 67, 718-724.
32. IARC, 1982. 4-Vinylcyclohexene and 4-Vinylcyclohexene diepoxide. IARC Monogr. Eval. Carcinog. Risks Hum. 60, 347-359.
33. Joffe, H., Hall, J.E., Gruber, S., Sarmiento, I.A., Cohen, L.S., Yurgelun-Todd, D., Martin, K.A., 2006. Estrogen therapy selectively enhances prefrontal cognitive processes: a randomized, double-blind, placebo-controlled study with functional magnetic resonance imaging in perimenopausal and recently postmenopausal women. Menopause 13, 411-422.
34. Keating, A.F., Mark, J., Sen, N., Sipes, I.G., Hoyer, P.B., 2009. Effect of phosphatidylinositol-3 kinase inhibition on ovotoxicity caused by 4-vinylcyclohexene diepoxide and 7,12-dimethylbenz[a] anthracene in neonatal rat ovaries. Toxicol. Appl. Pharmacol. 241, 127-134.
35. Keating, A.F., Sen, N., Sipes, I.G., Hoyer, P.B., 2010. Dual protective role for glutathione S-transferase class pi against VCD-induced ovotoxicity in the rat ovary. Toxicol. Appl. Pharm. 247, 71-75.
36. Keating, A.F., Fernandez, S.M., Mark-Kappeler, C.J., Sen, N., Sipes, I.G., Hoyer, P.B., 2010. Inhibition of PIK3 signaling pathway members by the ovotoxicant 4-vinylcyclohexene diepoxide in rats. Biol. Reprod.
37. Keck, M., Romero-Aleshire, M.J., Cai, Q., Hoyer, P.B., Brooks, H.L., 2007. Hormonal status affects the progression of STZ-induced diabetes and diabetic renal damage in the VCD mouse model of menopause. Am. J. Physiol Ren. 293, 193-199.
38. Laughlin, G.A., Barrett-Connor, E., Kritz-Silverstein, D., von Mühlen, D., 2000. Hysterectomy, oophorectomy, and endogenous sex hormone levels in older women: the Rancho Bernardo Study. J. Clin. Endocrinol. Metab. 85, 645-651.
39. Lekontseva, O.N., Rueda-Clausen, C.F., Morton, J.S., Davidge, S.T., 2010. Ovariectomy in aged versus young rats augments matrix metalloproteinase- mediated vasoconstriction in mesenteric arteries. Menopause 17, 516-523.
40. Lohff, J.C., Christian, P.J., Marion, S.L., Arrandale, A., Hoyer, P.B., 2005. Characterization of cyclicity and hormonal profile with impending ovarian failure in a novel chemical-induced mouse model of perimenopause. Comp. Med. 55, 523-527.
41. Lohff, J.C., Christian, P.J., Marion, S.L., Hoyer, P.B., 2006. Effect of duration of dosing on onset of ovarian failure in a chemical-induced mouse model of perimenopause. Menopause 13, 482-488.
42. Maffucci, J.A., Gore, A.C., 2006. Age-related changes in hormones and their receptors in animal models of female reproductive senescence. In: Conn, M.P. (Ed.), Handbook of Models for Human Aging. Academic Press and Elsevier, San Diego, pp. 533-552.
43. Maki, P.M., 2006. Hormone therapy and cognitive function: is there a critical period for benefit? Neuroscience 138, 1027-1030.
44. Mark-Kappeler, C.J., Sen, N., Keating, A.F., Sipes, I.G., Hoyer, P.B., 2010. Distribution and responsiveness of rat anti-Müllerian hormone during ovarian development and VCD-induced ovotoxicity. Toxicol. Appl. Pharm. 249, 1-7.
45. Mayer, L.P., Devine, P.J., Dyer, C.A., Hoyer, P.B., 2004. The follicle-deplete mouse ovary produces androgen. Biol. Reprod. 71, 130-138.
46. Mayer, L.P., Dyer, C.A., Eastgard, R.L., Hoyer, P.B., Banka, C.L., 2005. Atherosclerotic lesion development in a novel ovary-intact mouse model of perimenopause. Arterioscler. Thromb. Vasc. Biol. 25, 1910-1916.
47. Morrison, J.H., Brinton, R.D., Schmidt, P.J., Gore, A.C., 2006. Estrogen, menopause, and the aging brain: how basic neuroscience can inform hormone therapy in women. J. Neurosci. 26, 10332-10348. (Pubitemid 44564581)
48. 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., 2009. Effects of 4-vinylcyclohexene diepoxide on peripubertal and adult Sprague-Dawley rats: ovarian, clinical, and pathologic outcomes. Comp. Med. 59, 46-59.
49. National Toxicology Program, 1986. Toxicology and carcinogenesis studies of 4-vinylcyclohexene (CAS No. 100-40-3) in F344/N rats and B6C3F1 mice (gavage studies). Natl Toxicol. Program Tech. Rep. Ser. 303, 1-190.
50. National Toxicology Program, 1989. Toxicology and carcinogenesis studies of 4-vinyl-1-cyclohexene diepoxide (CAS No. 106-87-6) in F344/N rats and B6C3F1 mice (dermal studies). Natl Toxicol. Program Tech. Rep. Ser. 362, 1-249.
51. Nejat, E.J., Chervenak, J.L., 2010. The continuum of ovarian aging and clinicopathologies associated with the menopausal transition. Maturitas 66, 187-190.
52. Rivera, Z., Christian, P.J., Marion, S.L., Brooks, H.L., Hoyer, P.B., 2009. Steroidogenic capacity of residual ovarian tissue in 4-vinylcyclohexene diepoxide-treated mice. Biol. Reprod. 80, 328-336.
53. Rocca, W.A., Grossardt, B.R., Shuster, L.T., 2011. Oophorectomy, menopause, estrogen treatment, and cognitive aging: clinical evidence for a window of opportunity. Brain Res. 1379, 188-198.
54. Romero-Aleshire, M.J., Diamond-Stanic, M.K., Hasty, A.H., Hoyer, P.B., Brooks, H.L., 2009. Loss of ovarian function in the VCD mouse-model of menopause leads to insulin resistance and a rapid progression into the metabolic syndrome. Am. J. Physiol. Regul. Integr. Comp. Physiol. 297, 587-592.
55. Rousseau, M.E., 2006. Managing menopausal symptoms. In: Conn, M.P. (Ed.), Handbook for Models for Human Aging. Elsevier Academic Press, Amsterdam.
56. Rubin, B.S., 2000. Hypothalamic alterations and reproductive aging in female rats: evidence of altered luteinizing hormone-releasing hormone neuronal function. Biol. Reprod. 63, 968-976.
57. Sahambi, S.K., Visser, J.A., Themmen, A.P., Mayer, L.P., Devine, P.J., 2008. Correlation of serum anti-Mullerian hormone with accelerated follicle loss following 4-vinylcyclohexene diepoxide-induced follicle loss in mice. Reprod. Toxicol. 26, 116-122.
58. Schauwecker, P.E., Wood, R.I., Lorenzana, A., 2009. Neuroprotection against excitotoxic brain injury in mice after ovarian steroid depletion. Brain Res. 1265, 37-46.
59. Schmidt, P.J., Rubinow, D.R., 2009. Sex hormones and mood in the perimenopause. Ann. NY Acad. Sci. 1179, 70-85.
60. Sherwin, B.B., 2003. Estrogen and cognitive functioning in women. Endocr. Rev. 24, 133-151.
61. Shuster, L.T., Rhodes, D.J., Gostout, B.S., Grossardt, B.R., Rocca, W.A., 2010. Premature menopause or early menopause: long-term health consequences. Maturitas 65, 161-166.
62. Smith, B.J., Mattison, D.R., Sipes, I.G., 1990. The role of epoxidation in 4-vinylcyclohexene-induced ovarian toxicity. Toxicol. Appl. Pharm. 105, 372-381.
63. Smith, C.C., Vedder, L.C., Nelson, A.R., Bredemann, T.M., McMahon, L.L., 2010. Duration of estrogen deprivation, not chronological age, prevents estrogen's ability to enhance hippocampal synaptic physiology. Proc. Natl Acad. Sci. USA 107, 19543-19548.
64. Sobinoff, A.P., Pye, V., Nixon, B., Roman, S.D., McLaughlin, E.A., 2010. Adding insult to injury: effects of xenobiotic-induced preantral ovotoxicity on ovarian development and oocyte fusibility. Toxicol. Sci. 118, 653-666.
65. Spencer, J.L., Waters, E.M., Milner, T.A., McEwen, B.S., 2008. Estrous cycle regulates activation of hippocampal Akt, LIM kinase, and neurotrophin receptors in C57BL/6 mice. Neuroscience 155, 1106-1119.
66. Thompson, K.E., Sipes, I.G., Greenstein, B.D., Hoyer, P.B., 2002. 17beta-estradiol affords protection against 4-vinylcyclohexene diepoxide-induced ovarian follicle loss in Fischer-344 rats. Endocrinology 143, 1058-1065. (Pubitemid 34164054)
67. Williams, J.K., 2005. A mouse model of the perimenopausal transition: importance for cardiovascular research. Arterioscler. Thromb. Vasc. Biol. 25, 1765-1766.
68. Wise, P.M., Smith, M.J., Dubal, D.B., Wilson, M.E., Rau, S.W., Cashion, A.B., Böttner, M., Rosewell, K.L., 2002. Neuroendocrine modulation and repercussions of female reproductive aging. Recent Prog. Horm. Res. 57, 235-256.
69. Wright, L.E., Christian, P.J., Rivera, Z., Van Alstine, W.G., Funk, J.L., Bouxsein, M.L., Hoyer, P.B., 2008. Comparison of skeletal effects of ovariectomy versus chemically induced ovarian failure in mice. J. Bone Miner. Res. 23, 1296-1303.
70. Zandi, P.P., Carlson, M.C., Plassman, B.L., Welsh-Bohmer, K.A., Mayer, S.L., Steffens, D.C., Breitner, J.C., 2002. Hormone replacement therapy and incidence of Alzheimer disease in older women: the Cache County Study. JAMA 288, 2123-2129. (Pubitemid 35265379)