Maternal malnutrition during lactation alters the folliculogenesis and gonadotropins and estrogen isoforms ovarian receptors in the offspring at puberty

Journal of Endocrinology

Volumn 198, Issue 3, 2008, Pages 625-634

  da Silva Faria, Tatiane ^a   de Bittencourt Brasil, Flávia ^a   Sampaio, Francisco J B ^a   de Fonte Ramos, Cristiane ^a  

^a STATE UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; ESTRADIOL; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR BETA 1; ESTROGEN RECEPTOR BETA 2; FOLLITROPIN RECEPTOR; GONADOTROPIN RECEPTOR; ISOPROTEIN; LUTEINIZING HORMONE RECEPTOR; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS LUTEUM; DIETARY INTAKE; ESTRADIOL BLOOD LEVEL; FEMALE; HUMAN; LACTATION; MALE; MALNUTRITION; NONHUMAN; OVARY FOLLICLE DEVELOPMENT; PERINATAL PERIOD; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; PROTEIN RESTRICTION; PUBERTY; RANDOMIZATION; TESTOSTERONE BLOOD LEVEL; WEANING;

ANIMALS; BODY WEIGHT; EATING; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; FEMALE; GONADOTROPINS; LACTATION; MALE; OVARIAN FOLLICLE; PREGNANCY; PROTEIN ISOFORMS; PROTEIN-ENERGY MALNUTRITION; PUBERTY; RATS; RATS, WISTAR; RECEPTORS, ESTROGEN; RECEPTORS, FSH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TESTOSTERONE; WEANING;

EID: 53349156847     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1677/JOE-08-0121     Document Type: Article

References (84)

1. Barker DJP 2000 In utero programming of cardiovascular disease. Theriogenology 53 555-574.
2. Bayne K 1996 Revised guide for the care and use of laboratory animals available. American physiological society. Physiologist 39 208-211.
3. Brasil FB, Faria TS, Costa WS, Sampaio FJB & Ramos CF 2005 The pups' endometrium morphology is affected by maternal malnutrition during suckling. Maturitas 51 405-412.
4. Britt KL, Drummond AE, Cox VA, Dyson M, Wreford NG, Jones MEE, Simpson ER & Findlay JK 2000 An age-related ovarian phenotype in mice with targeted disruption of the Cyp 19 (Aromatase) gene. Endocrinology 141 2614 2623.
5. Burns KH, Yan C, Kumar TR & Matzuk MM 2001 Analysis of ovarian gene expression in follicle-stimulating hormone beta knockout mice. Endocrinology 142 2742-2751.
6. Byers M, Kuiper GG, Gustafsson J-A & Park-Sarge O-K 1997 Oestrogen receptor-ß mRNA expression in rat ovary: down-regulation by gonadotropins. Molecular Endocrinology 11 172-182.
7. Cheng G, Weihua Z, Makinen S, Makela S, Saji S, Warner M, Gustafsson JA & Hovatta O 2002 A role for the androgen receptor infollicular atresia of estrogen receptor beta knockout mouse ovary. Biology of Reproduction 66 77-84.
8. Chu S & Fuller PJ 1997 Identification of a splice variant of the rat estrogen receptor beta gene. Molecular and Cellular Endocrinology 132 195-199.
9. Chun TY, Gregg D, Sarkar DK & Gorski J 1998 Differential regulation by estrogens of growth and prolactin synthesis in pituitary cells suggests that only a small pool of estrogen receptors is required for growth. PNAS 95 2325-2330.
10. Clark JH, Schrader WT & O'Malley BW 1992 Mechanisms of action of steroid hormones. In Textbook of Endocrinology, pp 35-90. Eds JD Wilson & DW Foster. New York: Saunders.
11. Conneely OM, Mulac-Jericevic B, Lydon JP & DeMayo FJ 2001 Reproductive functions of the progesterone receptor isoforms: lessons from knockout mice. Molecular and Cellular Endocrinology 179 97-103.
12. Couse JE Curtis-Hewitt S, Bunch DO, Sar M, Walker VR, Davis Bj & Korach KS 1999 Postnatal sex reversal of the ovaries in mice lacking estrogen receptors alpha and beta. Science 286 2328-2331.
13. Couse JF, Yates MM, Deroo BJ & Korach KS 2005 Estrogen receptor-ß is critical to granulose cell differentiation and the ovulatory response to gonadotripins. Endocrinology 146 3247-3262.
14. Danilovich N, Roy I & Sairam MR 2001 Ovarian pathology and high incidence of sex cord tumors in follitropin receptor knockout (FORKO) mice. Endocrinology 142 3673-3684.
15. Davis BJ, Lennard DE, Lee CA, Tiano HF, Morham SG, Wetsel WC & Langenbach R 1999 Anovulation in cyclo-oxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1b. Endocrinology 140 2685-2696.
16. Dierich A, Sairam MR, Monaco L, Fimia GM, Gansmuller A, LeMeur M & Sassone-Corsi P 1998 Impairing follicle-stimulating hormone (FSH) signaling in vivo: targeted disruption of the FSH receptor leads to aberrant gametogenesis and hormonal imbalance. PNAS 95 13612-13617.
17. Drummond AE & Findlay JK 1999 The role of estrogen in folliculogenesis. Molecular and Cellular Endocrinology 151 57-64.
18. Drummond AE, Baillie AJ & Findlay JK 1999 Ovarian oestrogen receptor α and β mRNA expression: impact of development and oestrogen. Molecular and Cellular Endocrinology 149 153-161.
19. Dupont S, Krust A, Gansmuller A, Dierich A, Chambon P & Mark M 2000 Effect of single and compound knockouts of estrogen receptors alpha (ERα) and beta (ERß) on mouse reproductive phenotypes. Development 127 4277-4291.
20. Emmen JMA, Couse JF, Elmore SA, Yates MM, Kissling GE & Korach KS 2005 In vitro growth and ovulation of follicles from ovaries of estrogen receptor (ER)α and ERβ null mice indicate a role for ERβ in follicular maturation. Endocrinology 146 2817-2826.
21. Engelbregt MJT, Houdjik MECAM, Popp-Snijders C & Delemarre-Van de Wall HA 2000 The effects of intra-uterine growth retardation and postnatal undernutrition on onset of puberty in male and female rats. Pediatric Research 48 803-807.
22. Faria TS, Ramos CF & Sampaio FJB 2004 Puberty onset in the female offspring of rats submitted to protein or energy restricted diet during lactation. Journal of Nutritional Biochemistry 5 123-127.
23. Fishbeck KL & Rasmussen KM 1987 Effect of repeated cycles on maternal nutritional status, lactational performance and litter growth in ad libitum-fed and chronically food-restricted rats. Journal of Nutrition 117 1967-1975.
24. Fisher CR, Graves KH, Parlow AF & Simpson ER 1998 Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. PNAS 95 6965-6970.
25. Fortune JE 1994 Ovarian follicular growth and development in mammals. Biology of Reproduction 50 225-232.
26. Gelety TJ & Magoffin DA 1997 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. Biology of Reproduction 56 938-945.
27. Goldenberg RL, Vaitukaitis JL & Ross GT 1972 Estrogen and follicle stimulation hormone interactions on follicle growth in rats. Endocrinology 90 1492-1498.
28. Gore-Langton RE & Daniel SAJ 1990 Follicle-stimulating hormone and estradiol regulate antrum-like reorganization of granulosa cells in rat preantral follicle cultures. Biology of Reproduction 43 65-72.
29. Gougeon A 1996 Regulation of ovarian follicular development in primates: facts and hypotheses. Endocrine Reviews 17 121-155.
30. Guzmán C, Cabrera R, Cárdenas M, Larrea F, Nathanielsz PW & Zambrano E 2006 Protein restriction during fetal and neonatal development in the rat alters reproductive function and accelerates reproductive ageing in female progeny. Journal of Physiology 572 97-108.
31. Hirshfield AN 1991 Development of follicles in the mammalian ovary. International Review of Cytology 124 43-101.
32. Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, Matsuoka T, Noda Y, Tanaka T, Yoshida N et al. 1999 Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). PNAS 96 10501-10506.
33. Horie K, Takakura K, Fujiwara H, Suginami H, Liao S & Mori T 1992 Immunohistochemical localization of androgen receptor in the human ovary throughout the menstrual cycle in relation to estrogen and progesterone receptor expression. Human Reproduction 7 184-190.
34. Hu YC, Wang PH, Yeh S, Wang RS, Xie C, Xu Q, Zhou X, Chao HT, Tsai MY & Chang C 2004 Subfertility and defective folliculogenesis in female mice lacking androgen receptor. PNAS 101 11209-11214.
35. Hulshof SCJ, Figueiredo JR, Beckers JF, Beyers MM, van der Donk JA & Van Den Hurk R 1995 Effects of fetal bovine serum, FSH, and 17β-estradiol on the culture of bovine preantral follicles. Theriogenology 44 217-226.
36. Joyce IM, Pendola FL, O'Brien M & Eppig JJ 2001 Regulation of prostaglandin-endoperoxide synthase 2 messenger ribonucleic acid expression in mouse granulosa cells during ovulation. Endocrinology 142 3187-3197.
37. Kimura S, Matsumoto T, Matsuyama R, Shima H, Sato T, Takeyama K & Kato S 2007 Androgen receptor function in folliculogenesis and its clinical implication in premature ovarian failure. Trends in Endocrinology and Metabolism 18 183-189.
38. Knecht M, Darbon JM, Ranta T, Baukal AJ & Catt KJ 1984 Estrogens enhance the adenosine 3′,5′-monophosphate-mediated induction of follicle-stimulating hormone and luteinizing hormone receptors in rat granulosa cells. Endocrinology 115 41-49.
39. Knecht M, Brodie AM & Catt KJ 1985a Aromatase inhibitors prevent granulose cell differentiation: an obligatory role for estrogens in luteinizing hormone receptor expression. Endocrinology 117 1156-1161.
40. Knecht M, Tsai-Morris CH & Catt KJ 1985b Estrogen dependence of luteinizing hormone receptor expression in cultured rat granulosa cells. Inhibition of granulosa cell development by the antiestrogens tamoxifen and keoxifene. Endocrinology 116 1771-1777.
41. Korach KS, Migliaccio S & Davis VL 1995 Estrogens. In Principles of Pharmacology: Basic Concepts and Clinical Applications, pp 827-836. Ed. PL Munson. New York: Chapman & Hall.
42. Krege JH, Hodgin JB, Couse JF, Enmark E, Warner M, Mahler JF, Sar M, Korach KS, Gustafsson J-A & Smithies O 1998 Generation and reproductive phenotypes of mice lacking estrogen receptor β. PNAS 95 15677-15682.
43. Kumar TR, Wang Y, Lu N & Matzuk MM 1997 Follicle stimulating hormone is required for ovarian follicle maturation but not male fertility. Nature Genetics 15 201-204.
44. Lapolt PS, Tilly JL, Aihara T, Nishimori K & Hsueh AJ 1992 Gonadotropin-induced up- and down-regulation of ovarian follicle-stimulating hormone (FSH) receptor gene expression in immature rats: effects of pregnant mare's serum gonadotropin, human chorionic gonadotropin, and recombinant FSH. Endocrinology 130 1289-1295.
45. Leonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beuvillain JC & Dupouy JP 2003 Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biology of Reproduction 68 390-400.
46. Lindberg MK, Movérare S, Skrtic S, Gao H, Dahlman-Wright K, Gustafsson JA & Ohlsson C 2003 Estrogen receptor (ER)-β reduces ERα-regulated gene transcription, supporting a 'ying yang' relationship between ERα and ERβ in mice. Molecular Endocrinology 17 203-208.
47. Liu MM, Albanese C, Anderson CM, Hilty K, Webb P, Uht RM, Price RH Jr, Pestell RG & Kushner PJ 2002 Opposing action of estrogen receptors α and β on cyclin D1 gene expression. Journal of Biological Chemistry 277 24353-24360.
48. Lucas A 1994 Role of nutritional programming in determining adult morbidity. Archives of Disease in Childhood 71 288-290.
49. Lucas A 1998 Programming by early nutrition: an experimental approach. Journal of Nutrition 128 401S-406S.
50. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery CA Jr, Shyamala G, Conneely OM & O'Malley BW 1995 Mice lacking progesterone receptor exhibit reproductive abnormalities. Genes and Development 9 2266-2278.
51. Maruyama K, Endoh H, Sasaki-Iwaoka H, Kanou H, Shimaya E, Hashimoto S, Kato S & Kawashima H 1998 A novel isoform of rat estrogen receptor beta with 18 amino acid insertion in the ligand binding domain as a putative dominant negative regulator of estrogen action. Biochemical and Biophysical Research Communications 246 142-147.
52. McFarland KC, Sprengel R, Phillips HS, Kohler M, Rosemblit N, Nikolics K, Segaloff DL & Seeburg PH 1989 Lutropin-choriogonadotropin receptor: an unusual member of the G protein-coupled receptor family. Science 245 494-499.
53. McGee EA, Perlas E, LaPolt PS, Tsafriri A & Hsueh AJW 1997 Follicle-stimulating hormone enhances the development of preantral follicles in juvenile rats. Biology of Reproduction 57 990-998.
54. Moura AS, Caldeira Filho JS, Mathias PC & Franco de Sá CCN 1997 Insulin secretion impairment and insulin sensitivity improvement in adults rats undernourished during early lactation. Research Communications in Molelcular Pathology and Pharmacology 96 180-192.
55. Moura AS, Franco de Sá CC, Cruz HG & Costa CL 2002 Malnutrition during lactation as a metabolic imprinting factor inducing the feeding pattern of offspring rats when adults. The role of insulin and leptin. Brazilian Journal of Medical and Biological Research 35 617-622.
56. Nakano R, Nakayama T & Iwao M 1982 Inhibition of ovarian follicle growth by a chemical antiestrogen. Hormone Research 16 230-236.
57. Nakayama T, Nakano R & Iwao M 1981 Evidence for a role of endogenous estrogen on follicular growth in immature female rats. Endocrinologia Japonica 28 715-723.
58. Nayudu PL & Osborn SM 1992 Factors influencing the rate of preantral and antral growth of mouse ovarian follicles in vitro. Journal of Reproduction and Fertility 95 349-362.
59. Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson J, Kushner PJ & Scanlan TS 1997 Differential ligand activation of estrogen receptors ERα and ERβ at AP1 sites. Science 277 1508-1510.
60. Passos MCF, Ramos CF & Moura EG 2000 Short and long term effects of malnutrition in rats during lactation on the body weight of offspring. Nutrition Research 20 1603-1612.
61. Passos MCF, Ramos CF, Dutra SCP & Moura EG 2001 Transfer of iodine through the milk in protein-restricted lactating rats. Journal of Nutritional Biochemistry 2 300-303.
62. Peng B, Lu B, Leygue E & Murphy LC 2003 Putative functional characteristics of human estrogen receptor-beta isoforms. Journal of Molecular Endocrinology 30 13-29.
63. Petersen DN, Tkalcevic GT, Koza-Taylor PH, Turi TG & Brown TA 1998 Identification of estrogen receptor β2, a functional variant of estrogen receptor beta expressed in normal rat tissues. Endocrinology 139 1082-1092.
64. Price RH Jr & Handa RJ 2000 Expression of estrogen receptor-beta protein and mRNA in the cerebellum of the rat. Neuroscience Letters 288 115-118.
65. Rajah R, Glaser EM & Hirshfield NA 1992 The changing architecture of the neonatal rat ovary during histogenesis. Developmental Dynamics 194 177-192.
66. Ramos CF, Teixeira CV, Passos MCF, Pazos-Moura CC, Lisboa PC, Curry FH & Moura EG 2000 Low-protein diet changes thyroid function in lactating rats. Proceedings of the Society for Experimental Biology and Medicine 224 256-263.
67. Reeves PG, Nielsen FH & Fahey GC 1993 AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition Ad Hoc Writing Committee on the reformulation of the AIN-76 rodent diet. Journal of Nutrition 123 1939-1951.
68. Ricci AG, Di Yorio MP & Faletti AG 2006 Inhibitory effect of leptin on the rat ovary during the ovulatory process. Reproduction 132 771-780.
69. Richards JS 1994 Hormonal control of gene expression in the ovary. Endocrine Reviews 15 725-751.
70. Richards JS, Russell DL, Ochsner S & Espey LL 2002 Ovulation: new dimensions and new regulators of the inflammatory-like response. Annual Review of Physiology 64 69-92.
71. Robker RL, Russell DL, Espey LL, Lydon JP, O'Malley BW & Richards JS 2000 Progesterone-regulated genes in the ovulation process: ADAMTS-1 and cathepsin L proteases. PNAS 97 4689-4694.
72. Rosenfeld CS, Murray AA, Simmer G, Hufford MG, Smith MF, Spears N & Lubahn DB 2000 Gonadotropin induction of ovulation and corpus luteum formation in young estrogen receptor-α knockout mice. Biology of Reproduction 62 599-605.
73. Ryan NK, Van Der Hoek KH, Robertson SA & Norman RJ 2003 Leptin and leptin receptor expression in the rat ovary. Endocrinology 144 5006-5013.
74. Shimada M, Gonzalez-Robayna I, Hernandez-Gonzalez I & Richards JS 2006 Paracrine and autocrine regulation of EGF-like factors in cumulus oocyte complexes and granulosa cells: key role for prostaglandin synthase 2 (Ptgs2) and progesterone receptor (Pgr). Molecular Endocrinology 20 1352-1365.
75. Sirois J, Simmons DL & Richards JS 1992 Hormonal regulation of messenger ribonucleic acid encoding a novel isoform of prostaglandin endoperoxide H synthase in rat preovulatory follicles. Journal of Biological Chemistry 267 11586-11592.
76. Sprengel R, Braun T, Nikolics K, Segaloff DL & Seeburg PH 1990 The testicular receptor for follicle stimulating hormone: structure and functional expression of cloned cDNA. Molecular Endocrinology 4 525-530.
77. Tamura K, Matsushita M, Endo A, Kutsukake M & Kogo H 2007 Effect of insulin-like growth factor-binding protein 7 on steroidogenesis in granulosa cells derived from equine chorionic gonadotropin-primed immature rat ovaries. Biology of Reproduction 77 485-491.
78. Tano M, Minegishi T, Kishi H, Kameda T, Abe Y & Miyamoto K 1999 The effect of follicle-stimulating hormone (FSH) on the expression of Fsh receptor in cultured rat granulosa cells. Life Sciences 64 1063-1069.
79. Teixeira C, Passos M, Ramos C, Dutra S & Moura E 2002 Leptin serum concentration, food intake and body weight in rats whose mothers were exposed to malnutrition during lactation. Journal of Nutritional Biochemistry 13 493-498.
80. Teixeira C, Silandre D, Santos AMS, Delalande C, Sampaio FJB, Carreau S & Ramos CF 2007 Effects of maternal undernutrition during lactation on aromatase, estrogen, and androgen receptors expression in rat testis at weaning. Journal of Endocrinology 192 301-311.
81. Themmen APN & Huhtaniemi IT 2000 Mutations of gonadotropins and gonadotropin receptors: elucidating the physiology and pathophysiology of pituitary-gonadal function. Endocrine Reviews 21 551-583.
82. Vitt UA, Hayashi M, Klein C & Hsueh AJW 2000 Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biology of Reproduction 62 370-377.
83. Wang H, Andoh K, Hagiwara H, Xiaowei L, Kikuchi N, Abe Y, Yamada K, Fatima R & Mizunuma H 2001 Effect of adrenal and ovarian androgens on type 4 follicles unresponsive to FSH in immature mice. Endocrinology 142 4930-4936.
84. Wong WYW & Richards JS 1991 Evidence for two antigenically distinct molecular weight variants of prostaglandin H synthase in the rat ovary. Molecular Endocrinology 5 1269-1279.