Postnatal androgenization induces premature aging of rat ovaries

Steroids

Volumn 65, Issue 4, 2000, Pages 190-205

  Bukovskya, Antonin ^a   Ayala, Maria E ^b   Dominguez, Roberto ^b   Keenan, Jeffrey A ^a   Wimalasena, Jay ^a   McKenzie, Pamela P ^c   Caudle, Michael R ^a  

^a UNIVERSITY OF TENNESSEE MEDICAL CENTER   (United States)

^b Fac Estud Profesionales Z   (Mexico)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Androgens; Cellular aging; Immune adaptation; Mesenchymal cells; Ontogeny; Ovarian steroidogenic cells

Indexed keywords

LUTEINIZING HORMONE RECEPTOR; TESTOSTERONE PROPIONATE;

ADAPTATION; AGING; ANDROGEN THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOVULATION; CELL AGING; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; IMMUNOHISTOCHEMISTRY; MESENCHYME; NONHUMAN; ONTOGENY; OVARY; OVARY INSUFFICIENCY; PERINATAL PERIOD; PREMATURE AGING; RAT; REVIEW; STEROIDOGENESIS;

EID: 0034010551     PISSN: 0039128X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0039-128X(99)00101-4     Document Type: Article

References (106)

1. Barraclough C.A. Production of anovulatory, sterile rats by single injections of testosterone propionate. Endocrinology. 68:1961;62-67.
2. Mennin S.P., Kubo K., Gorski R.A. Pituitary responsiveness to luteinizing hormone-releasing factor in normal and androgenized female rats. Endocrinology. 95:1974;412-416.
3. Kubo K., Mennin S.P., Gorski R.A. Similarity of plasma LH release in androgenized and normal rats following electrochemical stimulation of the basal forebrain. Endocrinology. 96:1975;492-500.
4. Jones H.M., Vernon M.W., Rush M.E. Systematic studies invalidate the neonatally androgenized rat as a model for polycystic ovary disease. Biol Reprod. 36:1987;1253-1265.
5. Danguy A., Pasteels J.L., Ectors F. Sensitivity of anterior hypothalamic areas to gonadal steroid implantation in androgenized female rats. J Endocrinol. 74:1977;315-322.
6. Sarkar D.K., Fink G. Mechanism of the first spontaneous gonadotrophin surge and that induced by pregnant mare serum and effects of neonatal androgen in rats. J Endocrinol. 83:1979;339-354.
7. Zachow R.J., Magoffin D.A. Granulosa cell modulation of luteinizing hormone-dependent androgen production by ovarian theca-interstitial cells a temporal switch from suppression to augmentation stimulated by follicle-stimulating hormone in vitro . Biol Reprod. 53:1995;758-765.
8. Abhilasha, Krishna A. High androgen production by ovarian thecal interstitial cells: a mechanism for delayed ovulation in a tropical vespertillionid bat, Scotophilus heathi. J Reprod Fertil 1996;106:207-11.
9. Spinedi E., Mariani V., Bulfon M., Colombani-Vidal M., Scaglia H. Analysis of the hypothalamic-pituitary-ovary axis in the neonatally-androgenized female rat. J Endocrinol Invest. 13:1990;481-488.
10. Guraya S.S. Interstitial gland tissue of mammalian ovary. Acta Endocrinol Suppl(Copenh). 171:1973;5-27.
11. Guraya S.S. Histochemical observations on the lipid changes in the ovarian interstitial gland tissue of rats. J Reprod Fertil. 45:1975;141-145.
12. Louvet J.P., Harman S.M., Schrieber J.R., Ross G.T. Evidence of a role of androgens in follicular maturation. Endocrinology. 97:1975;366-372.
13. Guraya S.S., Gupta S.K. Morphology and histochemistry of ovarian changes in the field rat, Millardia meltada. Z Mikrosk Anat Forsch. 93:1979;959-973.
14. Hillier S.G., Zeleznik A.J., Knazek R.A., Ross G.T. Hormonal regulation of preovulatory follicle maturation in the rat. J Reprod Fertil. 60:1980;219-229.
15. Magoffin D.A., Reynolds D.S., Erickson G.F. Direct inhibitory effect of GnRH on androgen secretion by ovarian interstitial cells. Endocrinology. 109:1981;661-663.
16. Magoffin D.A., Erickson G.F. Direct inhibitory effect of estrogen on LH-stimulated androgen synthesis by ovarian cells cultured in defined medium. Mol Cell Endocrinol. 28:1982;81-89.
17. Magoffin D.A., Erickson G.F. Mechanism by which GnRH inhibits androgen synthesis directly in ovarian interstitial cells. Mol Cell Endocrinol. 27:1982;191-198.
18. Magoffin D.A., Erickson G.F. Prolactin inhibition of luteinizing hormone-stimulated androgen synthesis in ovarian interstitial cells cultured in defined medium mechanism of action . Endocrinology. 111:1982;2001-2007.
19. Erickson G.F., Magoffin D.A., Jones K.L. Theca function in polycystic ovaries of a patient with virilizing congenital adrenal hyperplasia. Fertil Steril. 51:1989;173-176.
20. Magoffin D.A. Evidence that luteinizing hormone-stimulated differentiation of purified ovarian thecal-interstitial cells is mediated by both type I and type II adenosine 3′,5′-monophosphate-dependent protein kinases. Endocrinology. 125:1989;1464-1473.
21. Nicosia M., Moger W.H., Dyer C.A., Prack M.M., Williams D.L. Apolipoprotein-E messenger RNA in rat ovary is expressed in theca and interstitial cells and presumptive macrophage, but not in granulosa cells. Mol Endocrinol. 6:1992;978-988.
22. Magoffin D.A., Weitsman S.R. Differentiation of ovarian theca-interstitial cells in vitro regulation of 17 alpha-hydroxylase messenger ribonucleic acid expression by luteinizing hormone and insulin-like growth factor-I . Endocrinology. 132:1993;1945-1951.
23. Magarelli P.C., Zachow R.J., Magoffin D.A. Developmental and hormonal regulation of rat theca-cell differentiation factor secretion in ovarian follicles. Biol Reprod. 55:1996;416-420.
24. Sridaran R., Gibori G. Intraovarian localization of luteinizing hormone/human chorionic gonadotropin stimulation of testosterone and estradiol synthesis in the pregnant rat. Endocrinology. 112:1983;1770-1776.
25. Dyer C.A., Erickson G.F. Norepinephrine amplifies human chorionic gonadotropin-stimulated androgen biosynthesis by ovarian theca-interstitial cells. Endocrinology. 116:1985;1645-1652.
26. Magoffin D.A., Erickson G.F. An improved method for primary culture of ovarian androgen-producing cells in serum-free medium effect of lipoproteins, insulin, and insulinlike growth factor-I . In Vitro Cell Dev Biol. 24:1988;862-870.
27. Magoffin D.A., Gancedo B., Erickson G.F. Transforming growth factor-beta promotes differentiation of ovarian thecal-interstitial cells but inhibits androgen production. Endocrinology. 125:1989;1951-1958.
28. Zachow R.J., Magoffin D.A. Granulosa cell modulation of luteinizing hormone-dependent androgen production by ovarian theca-interstitial cells a temporal switch from suppression to augmentation stimulated by follicle-stimulating hormone in vitro . Biol Reprod. 53:1995;758-765.
29. Gelety T.J., Magoffin D.A. Ontogeny of steroidogenic enzyme gene expression in ovarian theca- interstitial cells in the rat regulation by a paracrine theca-differentiating factor prior to achieving luteinizing hormone responsiveness . Biol Reprod. 56:1997;938-945.
30. Zachow R.J., Weitsman S.R., Magoffin D.A. Hepatocyte growth factor regulates ovarian theca-interstitial cell differentiation and androgen production. Endocrinology. 138:1997;691-697.
31. Zhang G., Curtiss L.K., Wade R.L., Dyer C.A. An apolipoprotein E synthetic peptide selectively modulates the transcription of the gene for rat ovarian theca and interstitial cell P450 17alpha-hydroxylase, C17-20 lyase. J Lipid Res. 39:1998;2406-2414.
32. Magoffin D.A., Erickson G.F. Purification of ovarian theca-interstitial cells by density gradient centrifugation. Endocrinology. 122:1988;2345-2347.
33. Billig H., Furuta I., Hsueh A.J. Estrogens inhibit and androgens enhance ovarian granulosa cell apoptosis. Endocrinology. 133:1993;2204-2212.
34. Rosen E.M., Grant D.S., Kleinman H.K., Goldberg I.D., Bhargava M.M., Nickoloff B.J., Kinsella J.L., Polverini P. Scatter factor (hepatocyte growth factor) is a potent angiogenesis factor in vivo. Symp Soc Exp Biol. 47:1993;227-234.
35. Diaz-Flores L., Gutierrez R., Varela H. Behavior of postcapillary venule pericytes during postnatal angiogenesis. J Morphol. 213:1992;33-45.
36. Zachow R.J., Tash J.S., Terranova P.F. Tumor necrosis factor-alpha induces clustering in ovarian theca-interstitial cells in vitro. Endocrinology. 131:1992;2503-2513.
37. Wang Y., Walsh S.W. TNF alpha concentrations and mRNA expression are increased in preeclamptic placentas. J Reprod Immunol. 32:1996;157-169.
38. Foghi A., Teerds K.J., Van der Donk H., Dorrington J. Induction of apoptosis in rat thecal/interstitial cells by transforming growth factor alpha plus transforming growth factor beta in vitro. J Endocrinol. 153:1997;169-178.
39. Guilbert L., Robertson S.A., Wegmann T.G. The trophoblast as an integral component of a macrophage-cytokine network. Immunol Cell Biol. 71:1993;49-57.
40. Kearsey J.A., Stadnyk A.W. Isolation and characterization of highly purified rat intestinal intraepithelial lymphocytes. J Immunol Methods. 194:1996;35-48.
41. Stanulis-Praeger B.M. Cellular senescence revisited a review . Mech Ageing Dev. 38:1987;1-48.
42. Eiben R., Liebich H.G. Detection and evaluation of lesions in the retina, optic nerve, and ciliary muscle of old rats using a electron microscope. Lens Eye Toxic Res. 6:1989;269-287.
43. Bukovsky A., Caudle M.R., Keenan J.A., Wimalasena J., Upadhyaya N.B., Van Meter S.E. Is irregular regression of corpora lutea in climacteric women caused by age-induced alterations in the "tissue control system"? Am J Reprod Immunol. 36:1996;327-341.
44. Sell D.R., Primc M., Schafer I.A., Kovach M., Weiss M.A., Monnier V.M. Cell-associated pentosidine as a marker of aging in human diploid cells in vitro and in vivo. Mech Ageing Dev. 105:1998;221-240.
45. Sloviter R.S., Dean E., Sollas A.L., Goodman J.H. Apoptosis and necrosis induced in different hippocampal neuron populations by repetitive perforant path stimulation in the rat. J Comp Neurol. 366:1996;516-533.
46. Gomez-Cuetara C., Flores J.M., Sanchez J., Rodriguez A., Sanchez M.A. Histological changes in the uterus during postpartum in the mare. Anat Histol Embryol. 24:1995;19-23.
47. Bukovsky A., Chen T.T., Wimalasena J., Caudle M.R. Cellular localization of luteinizing hormone receptor immunoreactivity in the ovaries of immature, gonadotropin-primed and normal cycling rats. Biol Reprod. 48:1993;1367-1382.
48. Indrapichate K., Meehan D., Lane T.A., Chu S.-Y., Rao C.V., Johnson D., Chen T.T., Wimalasena J. Biological actions of monoclonal luteinizing hormone/human chorionic gonadotropin receptor antibodies. Biol Reprod. 46:1992;265-278.
49. Teerds K.J., Dorrington J.H. Immunolocalization of transforming growth factor alpha and luteinizing hormone receptor in healthy and atretic follicles of the adult rat ovary. Biol Reprod. 52:1995;500-508.
50. Takao Y., Honda T., Ueda M., Hattori N., Yamada S., Maeda M., Fujiwara H., Mori T., Wimalasena J. Immunohistochemical localization of the LH/HCG receptor in human ovary HCG enhances cell surface expression of LH/HCG receptor on luteinizing granulosa cells in vitro . Mol Hum Reprod. 3:1997;569-578.
51. Gelety T.J., Magoffin D.A. Ontogeny of steroidogenic enzyme gene expression in ovarian theca-interstitial cells in the rat regulation by a paracrine theca-differentiating factor prior to achieving luteinizing hormone responsiveness . Biol Reprod. 56:1997;938-945.
52. Peters H, McNatty KP. The Ovary. A Correlation of Structure and Function in Mammals. Los Angeles: University of California Press, 1980.
53. Gaytan F., Morales C., Bellido C., Aguilar E., Sanchez-Criado J.E. Ovarian follicle macrophages is follicular atresia in the immature rat a macrophage-mediated event? Biol Reprod. 58:1998;52-59.
54. Bukovsky A., Trebichavsky I., Presl J., Zidovsky J. Submicroscopic evidence of lymphoid cells within the granulosa of the rat atretic follicle. IRCS Med Sci. 6:1978;80.
55. Bukovsky A., Presl J., Holub M. The ovarian follicle as a model for the cell-mediated control of tissue growth. Cell Tissue Res. 236:1984;717-724.
56. Greenwald GS, Terranova PF. Follicular selection and its control. In: Knobil E, Neill JD, editors. Physiology of Reproduction, Vol. 1. New York: Raven Press, 387-445.
57. Bukovsky A., Caudle M.R., Keenan J.A., Wimalasena J., Upadhyaya N.B., Van Meter S.E. Is corpus luteum regression an immune-mediated event? Localization of immune system components, and luteinizing hormone receptor in human corpora lutea. Biol Reprod. 53:1995;1373-1384.
58. Bukovsky A., Caudle M.R., Keenan J.A., Wimalasena J., Foster J.S., Van Meter S.E. Quantitative evaluation of the cell cycle-related retinoblastoma protein and localization of Thy-1 differentiation protein and macrophages during follicular development and atresia, and in human corpora lutea. Biol Reprod. 52:1995;776-792.
59. Bukovsky A., Caudle M.R., Keenan J.A. Regulation of ovarian function by immune system components the tissue control system (TCS) . Motta P.M. Microscopy of Reproduction and Development A Dynamic Approach . 1997;79-89 Antonio Delfino Editore, Rome.
60. Bukovsky A., Caudle M.R., Keenan J.A., Wimalasena J., McKenzie P.P. Thy-1 differentiation protein and monocyte-derived cells during regeneration and aging of human placental villi. Am J Reprod Immunol. 42:1999;135-152.
61. Ahmed C.E., Dees W.L., Ojeda S.R. The immature rat ovary is innervated by vasoactive intestinal peptide (VIP)-containing fibers and responds to VIP with steroid secretion. Endocrinology. 118:1986;1682-1689.
62. Lawrence I.E.J., Burden H.W. The autonomic innervation of the interstitial gland of the rat ovary during pregnancy. Am J Anat. 147:1976;81-94.
63. Svensson K.G. , Owman Ch, Sjoberg NO, Sporring B, Walls B. Ultrastructural evidence for adrenergic innervation of the interstitial gland in the guinea pig ovary. Neuroendocrinology. 17:1975;40-47.
64. Gorski R.A. Sexual differentiation of the hypothalamus. Mack H.C., Sherman A.I. , The Neuroendocrinology of Human Reproduction. 1971;60-90 CC Thomas Publ, Springfield.
65. Wise P.M., Krajnak K.M., Kashon M.L. Menopause the aging of multiple pacemakers . Science. 273:1996;67-70.
66. Knobil E., Yen S.S. The advent of menopause. Science. 274:1996;18-20.
67. Morley P., Armstrong D.T., Calaresu F.R. Ovarian nerve extracts influence androgen production by cultured ovarian thecal cells. Neuroendocrinology. 50:1989;93-99.
68. Rosa, Prajiante TM, Almeida FH, Guimaraes MA, Lunardi LO. Ovarian granulosa and theca interstitial cells: a morphological and physiological analysis in guanethidine denervated rats at pre-puberty. Cell Mol Biol (Noisy-le-grand) 1997;43:409-16.
69. Dominguez R. Differential ovulatory responses of the right and left ovaries of the adult rat to unilateral lesion and anaesthesia of the cervico-vaginal plexus. J Endocrinol. 124:1990;43-45.
70. Nakamura Y., Kato H., Terranova P.F. Abdominal vagotomy decreased the number of ova shed and serum progesterone levels on estrus in the cyclic hamster. Endocrinol Jpn. 39:1992;141-145.
71. Chavez R., Dominguez R. Participation of the superior ovarian nerve in the regulation of compensatory ovarian hypertrophy the effects of its section performed on each day of the oestrous cycle . J Endocrinol. 140:1994;197-201.
72. Tamura K., Tamura H., Kumasaka K., Miyajima A., Suga T., Kogo H. Ovarian immune cells express granulocyte-macrophage colony-stimulating factor (GM-CSF) during follicular growth and luteinization in gonadotropin-primed immature rodents. Mol Cell Endocrinol. 142:1998;153-163.
73. Vigano P., Gaffuri B., Ragni G. , Di BA, Vignali M. Intercellular adhesion molecule-1 is expressed on human granulosa cells and mediates their binding to lymphoid cells. J Clin Endocrinol Metab. 82:1997;101-105.
74. Best C.L., Pudney J., Anderson D.J., Hill J.A. Modulation of human granulosa cell steroid production in vitro by tumor necrosis factor alpha implications of white blood cells in culture . Obstet Gynecol. 84:1994;121-127.
75. Emi N., Kanzaki H., Yoshida M., Takakura K., Kariya M., Okamoto N., Imai K., Mori T. Lymphocytes stimulate progesterone production by cultured human granulosa luteal cells. Am J Obstet Gynecol. 165:1991;1469-1474.
76. Hoek A., van Kasteren Y., de Haan-Meulman M., Schoemaker J., Drexhage H.A. Dysfunction of monocytes and dendritic cells in patients with premature ovarian failure. Am J Reprod Immunol. 30:1993;207-217.
77. Chryssikopoulos A. The relationship between the immune and endocrine systems. Ann N Y Acad Sci. 816:1997;83-93.
78. Spanel-Borowski K., Ricken A.M. Evidence for the maintenance of macrophage-like cells in long-term bovine granulosa cell cultures. Cell Tissue Res. 288:1997;529-538.
79. Vinatier D., Dufour P., Tordjeman-Rizzi N., Prolongeau J.F., Depret-Moser S., Monnier J.C. Immunological aspects of ovarian function role of the cytokines . Eur J Obstet Gynecol Reprod Biol. 63:1995;155-168.
80. Harris H. Unfinished business. Gordon S. , The Legacy of Cell Fusion. 1994;286-295 Oxford University Press, Oxford.
81. Hughes F.M. Jr, Lane T.A., Chen T.T., Gorospe W.C. Effects of cytokines on porcine granulosa cell steroidogenesis in vitro. Biol Reprod. 43:1990;812-817.
82. Garcia-Lloret M.I., Morrish D.W., Wegmann T.G., Honore L., Turner A.R., Guilbert L.J. Demonstration of functional cytokine-placental interactions CSF-1 and GM-CSF stimulate human cytotrophoblast differentiation and peptide hormone secretion . Exp Cell Res. 214:1994;46-54.
83. Bukovsky A., Michael S.D., Presl J. Cell-mediated and neural control of morphostasis. Med Hypotheses. 36:1991;261-268.
84. Pennisi E. Teetering on the brink of danger. Science. 271:1996;1665-1667.
85. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature. 392:1998;245-252.
86. Klein J. Immunology: the science of self-nonself discrimination. New York: John Wiley and Sons, Inc., 1982.
87. Nagasawa H., Yanai R., Kikuyama S., Mori J. Pituitary secretion of prolactin, luteinizing hormone and follicle-stimulating hormone in adult female rats treated neonatally with oestrogen. J Endocrinol. 59:1973;599-604.
88. Matsumoto A., Asai T., Wakabayashi K. Effects of x-ray irradiation on the subsequent gonadotropin secretion in normal and neonatally estrogenized female rats. Endocrinol Jpn. 22:1975;233-241.
89. Kincl FA. Permanent Atrophy of Gonadal Glands Induced by Steroid Hormones. Charles University, Prague. Ph.D. Thesis. 1965.
90. Kincl F.A., Oriol A., Folch Pi A., Maqueo M. Prevention of steroid-induced sterility in neonatal rats with thymic cell suspension. Proc Soc Exp Biol Med. 120:1965;252-255.
91. Gaytan F., Bellido C., Morales C., Reymundo C., Aguilar E., van Rooijen N. Selective depletion of testicular macrophages and prevention of Leydig cell repopulation after treatment with ethylene dimethane sulfonate in rats. J Reprod Fertil. 101:1994;175-182.
92. Beagley K.W., Husband A.J. Intraepithelial lymphocytes origins, distribution, and function . Crit Rev Immunol. 18:1998;237-254.
93. Kroemer G., Cuende E., Martinez C. Compartmentalization of the peripheral immune system. Adv Immunol. 53:1993;157-216.
94. Avrameas S. Natural autoantibodies from 'horror autotoxicus' to 'gnothi seauton' . Immunol Today. 12:1991;154-159.
95. Huston D.P. The biology of the immune system. J Am Med Assoc. 278:1997;1804-1814.
96. Silverstein A.M., Rose N.R. On the mystique of the immunological self. Immunol Rev. 159:1997;197-206.
97. Owen R.D. Immunogenetic consequences of vascular anastomosis between bovine twins. Science. 102:1945;400-401.
98. Hasek M. Parabiosis of birds during embryonic development. Cesk Biol. 2:1953;265-270.
99. Billingham R.E., Brent L., Medawar P.B. Actively acquired tolerance of foreign cells. Nature. 172:1953;603-606.
100. Holbrook K.A., Odland G.F. Regional development of the human epidermis in the first trimester embryo and the second trimester fetus. J Invest Dermatol. 74:1980;161-168.
101. Sharpe R.M., Atanassova N., McKinnell C., Parte P., Turner K.J., Fisher J.S., Kerr J.B., Groome N.P., Macpherson S., Millar M.R., Saunders P.T. Abnormalities in functional development of the Sertoli cells in rats treated neonatally with diethylstilbestrol a possible role for estrogens in Sertoli cell development . Biol Reprod. 59:1998;1084-1094.
102. Takasugi N. Development of permanently proliferated and cornified vaginal epithelium in mice treated neonatally with steroid hormones and the implication in tumorigenesis. Natl Cancer Inst Monogr. 51:1979;57-66.
103. Vingerhoets A.J., Assies J., Goodkin K. , Van HG, Bekker MH. Prenatal diethylstilbestrol exposure and self-reported immune-related diseases. Eur J Obstet Gynecol Reprod Biol. 77:1998;205-209.
104. Swanson H.E., van Werff ten Bosch J.J. The "early-androgen" syndrome; differences in response to prenatal and postnatal administration of various doses of testosterone propionate in female and male rats. Acta Endocrinol (Copenh). 47:1964;37-50.
105. Farkas-Bargeton E., Barbet J.P., Dancea S., Wehrle R., Checouri A., Dulac O. Immaturity of muscle fibers in the congenital form of myotonic dystrophy its consequences and its origin . J Neurol Sci. 83:1988;145-159.
106. Weksler M.E. Immune senescence. Ann Neurol. 35:(suppl):1994;S35-S37.