early life exposure to isoflavones adversely affects reproductive health in first but not second generation female CD-1 mice

Journal of Nutrition

Volumn 141, Issue 11, 2011, Pages 1996-2002

  Dinsdale, Elsa C ^a   Chen, Jianmin ^a   Ward, Wendy E ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b BROCK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CORN OIL; ISOFLAVONE;

ANIMAL EXPERIMENT; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; ESTRUS CYCLE; EXPOSURE; FEMALE; FERTILITY; HYPERPLASIA; LUTEAL CELL; MALE; MOUSE; NEWBORN; NONHUMAN; OVARY; PUBERTY; RANDOMIZED CONTROLLED TRIAL; REPRODUCTIVE HEALTH; SEXUAL DEVELOPMENT;

ANIMALS; BODY WEIGHT; ESTRUS; FEMALE; FERTILITY; ISOFLAVONES; MALE; MICE; REPRODUCTION; VAGINA;

MUS; ZEA MAYS;

EID: 81055124078     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.111.142281     Document Type: Article

References (41)

1. National Toxiciology Program. Final Center for the Evaluation of Risks to Human Reproduction Expert Panel Report on Soy Infant Formula. Bethesda, MD: National Institutes of Health, 2010.
2. Leclercq G, Heuson JC. Physiological and pharmacological effects of estrogens in breast cancer. Biochim Biophys Acta. 1979;560:427-55.
3. Strom BL, Schinnar R, Ziegler EE, Barnhart KT, Sammel MD, Macones GA, Stallings VA, Drulis JM, Nelson SE, Hanson SA. Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. JAMA. 2001;286:807-14.
4. Bernbaum JC, Umbach DM, Ragan NB, Ballard JL, Archer JI, Schmidt-Davis H, Rogan WJ. Pilot studies of estrogen-related physical findings in infants. Environ Health Perspect. 2008;116:416-20.
5. Zung A, Glaser T, Kerem Z, Zadik Z. Breast development in the first 2 years of life: an association with soy-based infant formulas. J Pediatr Gastroenterol Nutr. 2008;46:191-5.
6. Lamartiniere CA, Zhang JX, Cotroneo MS. Genistein studies in rats: potential for breast cancer prevention and reproductive and developmental toxicity. Am J Clin Nutr. 1998;68:S1400-5.
7. Newbold RR, Banks EP, Bullock B, Jefferson WN. Uterine adenocarcinoma in mice treated neonatally with genistein. Cancer Res. 2001; 61:4325-8.
8. Jefferson WN, Padilla-Banks E, Clark G, Newbold RR. Assessing estrogenic activity of phytochemicals using transcriptional activation and immature mouse uterotrophic responses. J Chromatogr B Analyt Technol Biomed Life Sci. 2002;777:179-89.
9. Lewis RW, Brooks N, Milburn GM, Soames A, Stone S, Hall M, Ashby J. The effects of the phytoestrogen genistein on the postnatal development of the rat. Toxicol Sci. 2003;71:74-83.
10. Kaludjerovic J, Ward WE. Neonatal administration of isoflavones attenuates deterioration of bone tissue in female but not male mice. J Nutr. 2010;140:766-72.
11. Kaludjerovic J, Ward WE. Neonatal exposure to daidzein, genistein, or the combination modulates bone development in female CD-1 mice. J Nutr. 2009;139:467-73.
12. Varayoud J, Ramos JG, Bosquiazzo VL, Munoz-de-Toro M, Luque EH. Developmental exposure to bisphenol a impairs the uterine response to ovarian steroids in the adult. Endocrinology. 2008;149: 5848-60.
13. Titus-Ernstoff L, Troisi R, Hatch EE, Palmer JR, Hyer M, Kaufman R, Adam E, Noller K, Hoover RN. Birth defects in the sons and daughters of women who were exposed in utero to diethylstilbestrol (DES). Int J Androl. 2010;33:377-84.
14. Dinsdale EC, Ward WE. Early exposure to soy isoflavones and effects on reproductive health: a review of human and animal studies. Nutrients. 2010;2:1156-87.
15. Klein MA, Nahin RL, Messina MJ, Rader JI, Thompson LU, Badger TM, Dwyer JT, Kim YS, Pontzer CH, Starke-Reed PE, et al. Guidance from an NIH workshop on designing, implementing, and reporting clinical studies of soy interventions. J Nutr. 2010;140:S1192-204.
16. Jefferson WN, Padilla-Banks E, Newbold RR. Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol Reprod. 2005;73:798-806.
17. Jefferson WN, Padilla-Banks E, Goulding EH, Lao SP, Newbold RR, Williams CJ. Neonatal exposure to genistein disrupts ability of female mouse reproductive tract to support preimplantation embryo development and implantation. Biol Reprod. 2009;80:425-31.
18. Jefferson WN, Doerge D, Padilla-Banks E, Woodling KA, Kissling GE, Newbold R. Oral exposure to genistin, the glycosylated form of genistein, during neonatal life adversely affects the female reproductive system. Environ Health Perspect. 2009;117:1883-9.
19. Jefferson WN, Couse JF, Padilla-Banks E, Korach KS, Newbold RR. Neonatal exposure to genistein induces estrogen receptor (ER)alpha expression and multioocyte follicles in the maturing mouse ovary: evidence for ERbeta-mediated and nonestrogenic actions. Biol Reprod. 2002;67:1285-96.
20. Jefferson W, Newbold R, Padilla-Banks E, Pepling M. Neonatal genistein treatment alters ovarian differentiation in the mouse: inhibition of oocyte nest breakdown and increased oocyte survival. Biol Reprod. 2006;74:161-8.
21. Doerge DR, Twaddle NC, Banks EP, Jefferson WN, Newbold RR. Pharmacokinetic analysis in serum of genistein administered subcutaneously to neonatal mice. Cancer Lett. 2002;184:21-7.
22. Newbold RR, Padilla-Banks E, Jefferson WN. Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology. 2006;147:S11-7.
23. Titus-Ernstoff L, Troisi R, Hatch EE, Wise LA, Palmer J, Hyer M, Kaufman R, Adam E, Strohsnitter W, Noller K, et al. Menstrual and reproductive characteristics of women whose mothers were exposed in utero to diethylstilbestrol (DES). Int J Epidemiol. 2006; 35:862-8.
24. National Toxicology Program. Toxicology and carcinogenesis studies of genistein (CAS no. 446-72-0) in Sprague-Dawley Rats (feed study). Natl Toxicol Program Tech Rep Ser. 2008:1-240.
25. Canadian Council on Animal Care. Guide to the care and use of experimental animals. Ottawa: Canadian Council on Animal Care; 1993. p. 1-212.
26. Reeves PG. Components of the AIN-93 diets as improvements in the AIN-76A diet. J Nutr. 1997;127:S838-41.
27. Hotchkiss AK, Vandenbergh JG. The anogenital distance index of mice (Mus musculus domesticus): an analysis. Contemp Top Lab Anim Sci. 2005;44:46-8.
28. McClintock MK. Estrus synchrony: modulation of ovarian cycle length by female pheromones. Physiol Behav. 1984;32:701-5.
29. Kim HK, Nelson-Dooley C, Della-Fera MA, Yang JY, Zhang W, Duan J, Hartzell DL, Hamrick MW, Baile CA. Genistein decreases food intake, body weight, and fat pad weight and causes adipose tissue apoptosis in ovariectomized female mice. J Nutr. 2006;136: 409-14.
30. Charles River. CD-1 mice. 2005 [cited 2011 Jan 10]. Available from: http://www.criver.com/sitecollectiondocuments/cd1-mice.pdf.
31. Shields M. Overweight and obesity among children and youth. Health Rep. 2006;17:27-42.
32. Wright C. US epidemic: childhood obesity. J Physician Assist Educ. 2010;21:39-41.
33. Jefferson WN, Padilla-Banks E, Newbold RR. Disruption of the developing female reproductive system by phytoestrogens: genistein as an example. Mol Nutr Food Res. 2007;51:832-44.
34. Nagao T, Yoshimura S, Saito Y, Nakagomi M, Usumi K, Ono H. Reproductive effects in male and female rats of neonatal exposure to genistein. Reprod Toxicol. 2001;15:399-411.
35. Kouki T, Kishitake M, Okamoto M, Oosuka I, Takebe M, Yamanouchi K. Effects of neonatal treatment with phytoestrogens, genistein and daidzein, on sex difference in female rat brain function: estrus cycle and lordosis. Horm Behav. 2003;44:140-5.
36. Faber KA, Hughes CL Jr. Dose-response characteristics of neonatal exposure to genistein on pituitary responsiveness to gonadotropin releasing hormone and volume of the sexually dimorphic nucleus of the preoptic area (SDN-POA) in postpubertal castrated female rats. Reprod Toxicol. 1993;7:35-9.
37. Weinberg RW, editor. Clinical gynecologic and endocrinologic infertility. Philadelphia: Lippincott Williams and Wilkins; 2005.
38. Iguchi T, Kamiya K, Uesugi Y, Sayama K, Takasugi N. In vitro fertilization of oocytes from polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol. In Vivo. 1991;5:359-63.
39. Jefferson WN, Williams CJ. Circulating levels of genistein in the neonate, apart from dose and route, predict future adverse female reproductive outcomes. Reprod Toxicol. 2011;31:272-9.
40. Amstislavsky SY, Kizilova EA, Golubitsa AN, Vasilkova AA, Eroschenko VP. Preimplantation exposures of murine embryos to estradiol or methoxychlor change postnatal development. Reprod Toxicol. 2004;18:103-8.
41. Setchell KD, Zimmer-Nechemias L, Cai J, Heubi JE. Isoflavone content of infant formulas and the metabolic fate of these phytoestrogens in early life. Am J Clin Nutr. 1998;68:S1453-61.