Early life exposure to genistein and daidzein disrupts structural development of reproductive organs in female mice

Journal of Toxicology and Environmental Health - Part A: Current Issues

Volumn 75, Issue 11, 2012, Pages 649-660

  Kaludjerovic, Jovana ^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; DAIDZEIN; GENISTEIN; SOYBEAN PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; DRUG EXPOSURE; FEMALE; FEMALE GENITAL SYSTEM; HISTOPATHOLOGY; MOUSE; NONHUMAN; OOCYTE; ORGAN WEIGHT; OVARY CYST; OVARY DEVELOPMENT; OVARY FOLLICLE; PRIORITY JOURNAL; PUP (RODENT); SUCKLING; UTERUS;

ANIMALS; ANIMALS, SUCKLING; FEMALE; GENISTEIN; HUMANS; HYPERPLASIA; INFANT; INFANT FORMULA; ISOFLAVONES; LACTATION; MATERNAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; MICE; MICE, INBRED STRAINS; OVARY; OVIDUCTS; PHYTOESTROGENS; RANDOM ALLOCATION; SOY FOODS; UTERUS; WEIGHT GAIN;

MUS; ZEA MAYS;

EID: 84862856405     PISSN: 15287394     EISSN: 10872620     Source Type: Journal    
DOI: 10.1080/15287394.2012.688482     Document Type: Article

References (54)

1. Adewale, H. B., Jefferson, W. N., Newbold, R. R., and Patisaul, H. B. 2009. Neonatal bisphenol-a exposure alters rat reproductive development and ovarian morphology without impairing activation of gonadotropin-releasing hormone neurons. Biol. Reprod. 81: 690-99.
2. Agostoni, C., Axelsson, I., Goulet, O., Koletzko, B., Michaelsen, K. F., Puntis, J., Rieu, D., Rigo, J., Shamir, R., Szajewska, H., and Turck, D. 2006. Soy protein infant formulae and follow-on formulae: A commentary by the ESPGHAN Committee on Nutrition. J. Pediatr. Gastroenterol. Nutr. 42: 352-61. (Pubitemid 43841016)
3. Amleh, A., and Dean, J. 2002. Mouse genetics provides insight into folliculogenesis, fertilization and early embryonic development. Human Reprod. Update 8: 395-403. (Pubitemid 35175201)
4. Arango, N. A., and Donahoe, P. K. 2008. Sex differentiation in mouse and man and subsequent development of the female reproductive organs. StemBook. Cambridge, MA: Harvard Stem Cell Institute.
5. Barker, D. J. 2002. Fetal programming of coronary heart disease. Trends Endocrinol. Metab. 13: 364-68. (Pubitemid 36723587)
6. Bern, H. 1992. The fragile fetus. In Chemically-induced alterations in sexual and funcational development: The wildlife/human connection, eds. T. Colborn and C. Clement, Princeton, NJ: Princeton Scientific. pg. 9-15
7. Bernbaum, J. C., Umbach, D. M., Ragan, N. B., Ballard, J. L., Archer, J. I., Schmidt-Davis, H., and Rogan, W. J. 2008. Pilot studies of estrogen-related physical findings in infants. Environ. Health. Perspect. 116: 416-20. (Pubitemid 351409147)
8. Canadian Council on Animal Care. 1993. Guide to the care and use of experimental animals. Ottawa, ON: Canadian Council on Animal Care.
9. Cimafranca, M. A., Davila, J., Ekman, G. C., Andrews, R. N., Neese, S. L., Peretz, J., Woodling, K. A., Helferich, W. G., Sarkar, J., Flaws, J. A., Schantz, S. L., Doerge, D. R., and Cooke, P. S. 2010. Acute and chronic effects of oral genistein administration in neonatal mice. Biol. Reprod. 83: 114-21.
10. Couse, J. F., Lindzey, J., Grandien, K., Gustafsson, J. A., and Korach, K. S. 1997. Tissue distribution and quantitative analysis of estrogen receptor-alpha (ERalpha) and estrogen receptor-beta (ERbeta) messenger ribonucleic acid in the wild-type and ERalpha-knockout mouse. Endocrinol. 138: 4613-21. (Pubitemid 27460895)
11. Currie, A. J., Curtis, S., Strunk, T., Riley, K., Liyanage, K., Prescott, S., Doherty, D., Simmer, K., Richmond, P., and Burgner, D. 2011. Preterm infants have deficientmonocyte and lymphocyte cytokine responses to group B streptococcus. Infect Immun. 79: 1588-96.
12. Day, J. K., Bauer, A. M., DesBordes, C., Zhuang, Y., Kim, B. E., Newton, L. G., Nehra, V., Forsee, K. M., MacDonald, R. S., Besch-Williford, C., Huang, T. H., and Lubahn, D. B. 2002. Genistein alters methylation patterns in mice. J. Nutr. 132: S2419-23.
13. Dinsdale, E. C., Chen, J., and Ward, W. E. 2011. Early life exposure to isoflavones adversely affects reproductive health in first but not second generation female CD-1 mice. J. Nutr. 141: 1-7.
14. Dinsdale, E. C., and Ward, W. E. 2010. Early exposure to soy isoflavones and effects on reproductive health: A review of human and animal studies. Nutri. 2: 1156-87.
15. Dolinoy, D. C., Weidman, J. R., Waterland, R. A., and Jirtle, R. L. 2006. Maternal genistein alters coat color and protects Avy mouse offspring from obesity by modifying the fetal epigenome. Environ. Health Perspect. 114: 567-72.
16. Gilchrist, J. M., Moore, M. B., Andres, A., Estroff, J. A., and Badger, T. M. 2010. Ultrasonographic patterns of reproductive organs in infants fed soy formula: Comparisons to infants fed breast milk and milk formula. J. Pediatr. 156: 215-20.
17. Gilchrist, J. M., Wiggins, P., Brackenbury, J., Worthen, A., Crook, T., Brodie, M., and Badger, T. M. 2004. Body composition among infants fed breast milk, milk-based formula or soy based formula: Preliminary data from the Beginnings Study. FASEB. J. 18: A1112 (abstr.).
18. Jefferson, W. N., Couse, J. F., Padilla-Banks, E., Korach, K. S., and Newbold, R. R. 2000. Expression of estrogen receptor {beta} is developmentally regulated in reproductive tissues of male and female mice. Biol. Reprod. 62: 310-17. (Pubitemid 30067330)
19. Jefferson, W. N., Couse, J. F., Padilla-Banks, E., Korach, K. S., and Newbold, R. R. 2002. Neonatal exposure to genistein induces estrogen receptor (ER){alpha} expression and multioocyte follicles in the maturing mouse ovary: Evidence for ER{beta}-mediated and nonestrogenic actions. Biol. Reprod. 67: 1285-96.
20. Jefferson, W. N., Padilla-Banks, E., and Newbold, R. R. 2005. Adverse effects on female development and reproduction in CD-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol. Reprod. 73: 798-806. (Pubitemid 41356140)
21. Jefferson, W. N., Newbold, R., Padilla-Banks, E., and Pepling, M. 2006a. Neonatal genistein treatment alters ovarian differentiation in the mouse: Inhibition of oocyte nest breakdown and increased oocyte survival. Biol. Reprod. 74: 161-68. (Pubitemid 43068804)
22. Jefferson, W. N., Padilla-Banks, E., and Newbold, R. R. 2006b. Studies of the effects of neonatal exposure to genistein on the developing female reproductive system. J. AOAC Int. 89: 1189-96. (Pubitemid 44972071)
23. Jefferson, W. N., Padilla-Banks, E., and Newbold, R. R. 2007a. Disruption of the female reproductive system by the phytoestrogen genistein. Reprod. Toxicol. 23: 308-16. (Pubitemid 46628872)
24. Jefferson, W. N., Padilla-Banks, E., and Newbold, R. R. 2007b. Disruption of the developing female reproductive system by phytoestrogens: Genistein as an example. Mol. Nutr. Food Res. 51: 832-44. (Pubitemid 47173693)
25. Jefferson, W. N., Doerge, D., Padilla-Banks, E., Woodling, K. A., Kissling, G. E., and Newbold, R. 2009. Oral exposure to genistin, the glycosylated form of genistein, during neonatal life adversely affects the female reproductive system. Environ. Health Perspect. 117: 1883-89.
26. Kaludjerovic, J., Franke, A. A., and Ward, W. E. 2012. Circulating isoflavonoid levels in CD-1 mice: Effect of oral versus subcutaneous delivery and frequency of administration. J. Nutr. Biochem. 23:437-42.
27. Kaludjerovic, J., and Ward, W. E. 2008. Diethylstilbesterol has gender-specific effects on weight gain and bone development in mice. J. Toxicol. Environ. Health A. 71: 1032-42.
28. Kaludjerovic, J., and Ward, W. E. 2009. Neonatal exposure to daidzein, genistein, or the combination modulates bone development in female CD-1 mice. J. Nutr. 139: 467-73.
29. Kaludjerovic, J., and Ward, W. E. 2010. Neonatal administration of isoflavones attenuates deterioration of bone tissue in female but not male mice. J. Nutr. 140: 766-72.
30. Klein, M. A., Nahin, R. L., Messina,M. J., Rader, J. I., Thompson, L. U., Badger, T. M., Dwyer, J. T., Kim, Y. S., Pontzer, C. H., Starke-Reed, P. E., and Weaver, C. M. 2010. Guidance from an NIH workshop on designing, implementing, and reporting clinical studies of soy interventions. J. Nutr. 140: S1192-204.
31. Kouki, T., Kishitake, M., Okamoto, M., Oosuka, I., Takebe, M., and Yamanouchi, K. 2003. Effects of neonatal treatment with phytoestrogens, genistein and daidzein, on sex difference in female rat brain function: Estrous cycle and lordosis. Horm. Behav. 44: 140-45. (Pubitemid 37108636)
32. Lee, J. S., Ward, W. O., Knapp, G., Ren, H., Vallanat, B., Abbott, B., Ho, K., Karp, S. J., and Corton, J. C. 2012. Transcriptional ontogeny of the developing liver. BMC Genomics 13: 33. [Epub ahead of print]
33. Liu, Z., Zhang, X., Li, L., Zhang, W., Cui, W., Song, Y., Wang, W., Jia, X., Li, N., and Yan, W. 2008. Effects of lactational exposure to soy isoflavones on reproductive system in neonatal female rats. Basic Clin. Pharmacol. Toxicol. 102: 317-24. (Pubitemid 351287565)
34. Magos, L. 2003. Neurotoxic character of thimerosal and the allometric extrapolation of adult clearance half-time to infants. J. Appl. Toxicol. 23: 263-69. (Pubitemid 36950296)
35. McCarver, G., Bhatia, J., Chambers, C., Clarke, R., Etzel, R., Foster, W., Hoyer, P., Leeder, J. S., Peters, J. M., Rissman, E., Rybak, M., Sherman, C., Toppari, J., and Turner, K. 2011. NTP-CERHR expert panel report on the developmental toxicity of soy infant formula. Birth Defects Res. B Dev. Reprod. Toxicol. 92: 421-68.
36. Migliaccio, S., Newbold, R. R., Bullock, B. C., Jefferson, W. J., Sutton, F. G., Jr., McLachlan, J. A., Korach, K. S. 1996. Alterations of maternal estrogen levels during gestation affect the skeleton of female offspring. Endocrinology 137: 2118-25. (Pubitemid 26133984)
37. Moller, F. J., Zierau, O., Hertrampf, T., Bliedtner, A., Diel, P., and Vollmer, G. 2009. Long-term effects of dietary isoflavones on uterine gene expression profiles. J. Steroid Biochem. Mol. Biol. 113: 296-303.
38. Newbold, R. R., Padilla-Banks, E., Bullock, B., and Jefferson, W. N. 2001. Uterine adenocarcinoma in mice treated neonatally with genistein. Cancer Res. 61: 4325-28. (Pubitemid 32685752)
39. Newbold, R. R., Padilla-Banks, E., Snyder, R. J., and Jefferson, W.N. 2005. Developmental exposure to estrogenic compounds and obesity. Birth Defects Res. A Clin. Mol. Teratol. 73: 478-80. (Pubitemid 41045293)
40. Newbold, R. R., Padilla-Banks, E., and Jefferson, W. N. 2006. Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147: S11-17. (Pubitemid 43764585)
41. Newbold, R. R., Jefferson, W. N., and Padilla-Banks, E. 2007. Long-term adverse effects of neonatal exposure to bisphenol A on the murine female reproductive tract. Reprod. Toxicol. 24: 253-58. (Pubitemid 47393609)
42. Newbold, R. R., Jefferson, W. N., and Padilla-Banks, E. 2009. Prenatal exposure to bisphenol a at environmentally relevant doses adversely affects the murine female reproductive tract later in life. Environ. Health Perspect. 117: 879-885.
43. Piekarz, A. V., and Ward, W. E. 2007. Effect of neonatal exposure to genistein on bone metabolism in mice at adulthood. Pediatr. Res. 61: 48-53. (Pubitemid 46352315)
44. Prescott, S. L., Taylor, A., King, B., Dunstan, J., Upham, J. W., Thornton, C. A., and Holt, P. G. 2003. Neonatal interleukin-12 capacity is associated with variations in allergen-specific immune responses in the neonatal and postnatal periods. Clin. Exp. Allergy. 33: 566-72. (Pubitemid 36629679)
45. Reinwald, S., and Weaver, C. M. 2006. Soy isoflavones and bone health: A double-edged sword? J. Nat. Prod. 69: 450-59.
46. Riggs, B. L., and Hartmann, L. C. 2003. Selective estrogen-receptor modulators - Mechanisms of action and application to clinical practice. N. Engl. J. Med. 348: 618-29.
47. Sar, M., and Welsch, F. 1999. Differential expression of estrogen receptor-beta and estrogen receptor-alpha in the rat ovary. Endocrinology 140: 963-71. (Pubitemid 29058237)
48. Sato, K., Fukata, H., Kogo, Y., Ohgane, J., Shiota, K., and Mori, C. 2009. Neonatal exposure to diethylstilbestrol alters expression of DNA methyltransferases and methylation of genomic DNA in the mouse uterus. Endocr. J. 56: 131-39.
49. Strom, B. L., Schinnar, R., Ziegler, E. E., Barnhart, K. T., Sammel, M. D., Macones, G. A., Stallings, V. A., Drulis, J. M., Nelson, S. E., and Hanson, S. A. 2001. Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. J. Am. Med. Assoc. 286: 807-14. (Pubitemid 33015574)
50. Vieau, D. 2011. Perinatal nutritional programming of health and metabolic adult disease. World J. Diabetes 2: 133-36.
51. Ward, W. E., Piekarz, A. V., and Fonseca, D. 2007. Bone mass, bone strength, and their relationship in developing CD-1 mice. Can. J. Physiol. Pharmacol. 85: 274-79. (Pubitemid 46846439)
52. Yamashita, S., Newbold, R. R., McLachlan, J. A., and Korach, K. S. 1990. The role of the estrogen receptor in uterine epithelial proliferation and cytodifferentiation in neonatal mice. Endocrinology 127: 2456-63. (Pubitemid 20381782)
53. Yu, C., Tai, F., Wu, R., Song, Z., Zhang, X., and An, X. 2010. Maternal exposure to daidzein alters behaviour and oestrogen receptor alpha expression in adult female offspring. Behav. Pharmacol. 21: 283-91.
54. Zung, A., Glaser, T., Kerem, Z., and Zadik, Z. 2008. Breast development in the first 2 years of life: An association with soy-based infant formulas. J. Pediatr. Gastroenterol. Nutr. 46: 191-95. (Pubitemid 351161126)