Acute and chronic effects of oral genistein administration in neonatal mice

Biology of Reproduction

Volumn 83, Issue 1, 2010, Pages 114-121

  Cimafranca, Melissa A ^a   Davila, Juanmahel ^a   Ekman, Gail C ^a   Andrews, Rachel N ^a   Neese, Steven L ^a   Peretz, Jackye ^a   Woodling, Kellie A ^b   Helferich, William G ^a   Sarkar, Jhimly ^a   Flaws, Jodi A ^a   Schantz, Susan L ^a   Doerge, Daniel R ^b   Cooke, Paul S ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Female reproductive tract; Genistein; Infant; Soy formula; Toxicology

Indexed keywords

CORN OIL; ESTROGEN; GENISTEIN; PROGESTERONE RECEPTOR; PHYTOESTROGEN;

ACUTE TOXICITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL MILK; BLOOD LEVEL; BODY WEIGHT; CHRONIC TOXICITY; CONTROLLED STUDY; DOWN REGULATION; DRUG EXPOSURE; EMULSION; ENDOMETRIUM; ESTRUS CYCLE; FEMALE; FEMALE GENITAL SYSTEM; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NEWBORN; NONHUMAN; OVARY; OVARY FOLLICLE; PERINATAL PERIOD; PRIORITY JOURNAL; REPRODUCTION; REPRODUCTIVE TOXICITY; THYMUS; UTERUS WEIGHT; ANIMAL; BLOOD; C57BL MOUSE; DRUG EFFECTS; HUMAN; INFANT; ORAL DRUG ADMINISTRATION;

ANIMALIA; MUS; RODENTIA; ZEA MAYS;

ADMINISTRATION, ORAL; ANIMALS; ANIMALS, NEWBORN; CORN OIL; FEMALE; GENISTEIN; GENITALIA, FEMALE; HUMANS; INFANT; INFANT FORMULA; MICE; MICE, INBRED C57BL; PHYTOESTROGENS;

EID: 77954196531     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.080549     Document Type: Article

References (53)

1. Bhatia J, Greer F. Use of soy protein-based formulas in infant feeding. Pediatrics 2008; 121:1062-1068.
2. 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; 286:807-814. (Pubitemid 33015574)
3. Berger-Achituv S, Shohat T, Romano-Zelekha O, Ophir E, Rachmani S, Malovizky D, Garty BZ. Widespread use of soy-based formula without clinical indications. J Pediatr Gastroenterol Nutr 2005; 41:660-666. (Pubitemid 41579680)
4. Agostoni C, Axelsson I, Goulet O, Koletzko B, Michaelsen KF, Puntis J, Rieu D, Rigo J, Shamir R, Szajewska H, Turck D. Soy protein infant formulae and follow-on formulae: a commentary by the ESPGHAN Committee on Nutrition. J Pediatr Gastroenterol Nutr 2006; 42:352-361. (Pubitemid 43841016)
5. Badger TM, Gilchrist JM, Pivik RT, Andres A, Shankar K, Chen JR, Ronis MJ. The health implications of soy infant formula. Am J Clin Nutr 2009; 89:1668S-1672S.
6. Lasekan JB, Ostrom KM, Jacobs JR, Blatter MM, Ndife LI, Gooch WM III, Cho S. Growth of newborn, term infants fed soy formulas for 1 year. Clin Pediatr (Phila) 1999; 38:563-571. (Pubitemid 29483200)
7. Mendez MA, Anthony MS, Arab L. Soy-based formulae and infant growth and development: a review. J Nutr 2002; 132:2127-2130. (Pubitemid 34851638)
8. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 1998; 139:4252-4263. (Pubitemid 28513713)
9. Setchell KD, Zimmer-Nechemias L, Cai J, Heubi JE. Exposure of infants to phyto-oestrogens from soy-based infant formula. Lancet 1997; 350:23-27. (Pubitemid 27279766)
10. Setchell KD. Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am J Clin Nutr 1998; 68:1333S-1346S.
11. Adlercreutz H, Markkanen H, Watanabe S. Plasma concentrations of phyto-oestrogens in Japanese men. Lancet 1993; 342:1209-1210. (Pubitemid 23331713)
12. Cassidy A, Bingham S, Setchell KD. Biological effects of a diet of soy protein rich in isoflavones on the menstrual cycle of premenopausal women. Am J Clin Nutr 1994; 60:333-340. (Pubitemid 24278733)
13. Freni-Titulaer LW, Cordero JF, Haddock L, Lebron G, Martinez R, Mills JL. Premature thelarche in Puerto Rico. A search for environmental factors. Am J Dis Child 1986; 140:1263-1267. (Pubitemid 17195073)
14. Zoppi G, Mantovanelli F, Pittschieler K, Delem A, Teuwen DE. Response to RIT 4237 oral rotavirus vaccine in human milk, adapted-and soy-formula fed infants. Acta Paediatr Scand 1989; 78:759-762. (Pubitemid 19232313)
15. Cordle CT, Winship TR, Schaller JP, Thomas DJ, Buck RH, Ostrom KM, Jacobs JR, Blatter MM, Cho S, Gooch WM III, Pickering LK. Immune status of infants fed soy-based formulas with or without added nucleotides for 1 year: part 2: immune cell populations. J Pediatr Gastroenterol Nutr 2002; 34:145-153. (Pubitemid 34259633)
16. Ostrom KM, Cordle CT, Schaller JP, Winship TR, Thomas DJ, Jacobs JR, Blatter MM, Cho S, Gooch WM III, Granoff DM, Faden H, Pickering LK. Immune status of infants fed soy-based formulas with or without added nucleotides for 1 year: part 1: vaccine responses, and morbidity. J Pediatr Gastroenterol Nutr 2002; 34:137-144. (Pubitemid 34259632)
17. 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; 116:416-420.
18. Cao Y, Calafat AM, Doerge DR, Umbach DM, Bernbaum JC, Twaddle NC, Ye X, Rogan WJ. Isoflavones in urine, saliva, and blood of infants: data from a pilot study on the estrogenic activity of soy formula. J Expo Sci Environ Epidemiol 2009; 19:223-234.
19. Jing H, Pivik RT, Gilchrist JM, Badger TM. No difference indicated in electroencephalographic power spectral analysis in 3- and 6-mo-old infants fed soy- or milk-based formula. Matern Child Nutr 2008; 4:136-145. (Pubitemid 351411152)
20. Doerge DR, Twaddle NC, Churchwell MI, Newbold RR, Delclos KB. Lactational transfer of the soy isoflavone, genistein, in Sprague-Dawley rats consuming dietary genistein. Reprod Toxicol 2006; 21:307-312.
21. Iguchi T, Fukazawa Y, Uesugi Y, Takasugi N. Polyovular follicles in mouse ovaries exposed neonatally to diethylstilbestrol in vivo and in vitro. Biol Reprod 1990; 43:478-484. (Pubitemid 20289497)
22. 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; 51:832-844. (Pubitemid 47173693)
23. Ashby J, Odum J, Tinwell H. Predictive value of the uterotrophic assay for genistein carcinogenicity in the neonatal mouse: relevance to infants consuming soy-based formula. Environ Health Perspect 2001; 109:A568-A570.
24. Rozman KK, Bhatia J, Calafat AM, Chambers C, Culty M, Etzel RA, Flaws JA, Hansen DK, Hoyer PB, Jeffery EH, Kesner JS, Marty S, et al. NTP-CERHR expert panel report on the reproductive and developmental toxicity of soy formula. Birth Defects Res B Dev Reprod Toxicol 2006; 77:280-397. (Pubitemid 44484021)
25. Rozman KK, Bhatia J, Calafat AM, Chambers C, Culty M, Etzel RA, Flaws JA, Hansen DK, Hoyer PB, Jeffery EH, Kesner JS, Marty S, et al. NTP-CERHR expert panel report on the reproductive and developmental toxicity of genistein. Birth Defects Res B Dev Reprod Toxicol 2006; 77:485-638. (Pubitemid 46025633)
26. Twaddle NC, Churchwell MI, Doerge DR. High-throughput quantification of soy isoflavones in human and rodent blood using liquid chromatography with electrospray mass spectrometry and tandem mass spectrometry detection. J Chromatogr B Analyt Technol Biomed Life Sci 2002; 777:139-145. (Pubitemid 35257868)
27. Tomic D, Frech MS, Babus JK, Symonds D, Furth PA, Koos RD, Flaws JA. Effects of ERalpha overexpression on female reproduction in mice. Reprod Toxicol 2007; 23:317-325. (Pubitemid 46602922)
28. Goldman JM, Murr AS, Cooper RL. The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res B Dev Reprod Toxicol 2007; 80:84-97.
29. Forsberg JG. The different responses of the female mouse thymus to estrogen after treatment of neonatal, prepubertal, and adult animals. Acta Anat (Basel) 1996; 157:275-290.
30. Yellayi S, Naaz A, Szewczykowski MA, Sato T, Woods JA, Chang J, Segre M, Allred CD, Helferich WG, Cooke PS. The phytoestrogen genistein induces thymic and immune changes: a human health concern? Proc Natl Acad Sci U S A 2002; 99:7616-7621.
31. Bern HA, Edery M, Mills KT, Kohrman AF, Mori T, Larson L. Long-term alterations in histology and steroid receptor levels of the genital tract and mammary gland following neonatal exposure of female BALB/cCrgl mice to various doses of diethylstilbestrol. Cancer Res 1987; 47:4165-4172. (Pubitemid 17108488)
32. Thigpen JE, Haseman JK, Saunders HE, Setchell KD, Grant MG, Forsythe DB. Dietary phytoestrogens accelerate the time of vaginal opening in immature CD-1 mice. Comp Med 2003; 53:607-615.
33. 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. (Pubitemid 41356140)
34. 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: estrous cycle and lordosis. Horm Behav 2003; 44:140-145. (Pubitemid 37108636)
35. Yellayi S, Teuscher C, Woods JA, Welsh TH Jr, Tung KS, Nakai M, Rosenfeld CS, Lubahn DB, Cooke PS. Normal development of thymus in male and female mice requires estrogen/estrogen receptor-alpha signaling pathway. Endocrine 2000; 12:207-213. (Pubitemid 30432235)
36. Doerge DR, Twaddle NC, Banks EP, Jefferson WN, Newbold RR. Pharmacokinetic analysis in serum of genistein administered subcutaneously to neonatal mice. Cancer Lett 2002; 184:21-27.
37. Jefferson WN, Padilla-Banks E, Newbold RR. Disruption of the female reproductive system by the phytoestrogen genistein. Reprod Toxicol 2007; 23:308-316. (Pubitemid 46628872)
38. 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. (Pubitemid 32758394)
39. 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; 117:1883-1889.
40. Nagel SC, vom Saal FS, Welshons WV. Developmental effects of estrogenic chemicals are predicted by an in vitro assay incorporating modification of cell uptake by serum. J Steroid Biochem Mol Biol 1999; 69:343-357.
41. Milligan SR, Khan O, Nash M. Competitive binding of xenobiotic oestrogens to rat alpha-fetoprotein and to sex steroid binding proteins in human and rainbow trout (Oncorhynchus mykiss) plasma. Gen Comp Endocrinol 1998; 112:89-95. (Pubitemid 28456072)
42. Kurita T, Lee KJ, Cooke PS, Taylor JA, Lubahn DB, Cunha GR. Paracrine regulation of epithelial progesterone receptor by estradiol in the mouse female reproductive tract. Biol Reprod 2000; 62:821-830. (Pubitemid 30173793)
43. Ohta Y, Fukazawa Y, Sato T, Suzuki A, Nishimura N, Iguchi T. Effect of estrogen on ontogenic expression of progesterone and estrogen receptors in rat uterus. Zoolog Sci 1996; 13:143-149. (Pubitemid 126409789)
44. 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; 46:191-195. (Pubitemid 351161126)
45. Manivel JC, Dehner LP, Burke B. Ovarian tumorlike structures, biovular follicles, and binucleated oocytes in children: their frequency and possible pathologic significance. Pediatr Pathol 1988; 8:283-292.
46. Gougeon A. Frequent occurrence of multiovular follicles and multinuclear oocytes in the adult human ovary. Fertil Steril 1981; 35:417-422. (Pubitemid 11113217)
47. Chen Y, Jefferson WN, Newbold RR, Padilla-Banks E, Pepling ME. Estradiol, progesterone, and genistein inhibit oocyte nest breakdown and primordial follicle assembly in the neonatal mouse ovary in vitro and in vivo. Endocrinology 2007; 148:3580-3590. (Pubitemid 47105867)
48. Kipp JL, Kilen SM, Bristol-Gould S, Woodruff TK, Mayo KE. Neonatal exposure to estrogens suppresses activin expression and signaling in the mouse ovary. Endocrinology 2007; 148:1968-1976. (Pubitemid 46997073)
49. Guillette LJ Jr, Moore BC. Environmental contaminants, fertility, and multioocytic follicles: a lesson from wildlife? Semin Reprod Med 2006; 24:134-141.
50. Delclos KB, Newbold R. NTP toxicity report of reproductive dose range-finding study of genistein (CAS No. 446-72-0) administered in feed to Sprague-Dawley rats. Toxic Rep Ser 2007; 79:1-C2.
51. Hoey L, Rowland IR, Lloyd AS, Clarke DB, Wiseman H. Influence of soya-based infant formula consumption on isoflavone and gut microflora metabolite concentrations in urine and on faecal microflora composition and metabolic activity in infants and children. Br J Nutr 2004; 91:607-616. (Pubitemid 38584785)
52. Allred CD, Ju YH, Allred KF, Chang J, Helferich WG. Dietary genistin stimulates growth of estrogen-dependent breast cancer tumors similar to that observed with genistein. Carcinogenesis 2001; 22:1667-1673. (Pubitemid 32952145)
53. Whitten PL, Patisaul HB. Cross-species and interassay comparisons of phytoestrogen action. Environ Health Perspect 2001; 109(suppl 1):520.