Histopathologic changes in the uterus, cervix and vagina of immature CD-1 mice exposed to low doses of perfluorooctanoic acid (PFOA) in a uterotrophic assay

Reproductive Toxicology

Volumn 33, Issue 4, 2012, Pages 506-512

  Dixon, Darlene ^a   Reed, Casey E ^a   Moore, Alicia B ^a   Gibbs Flournoy, Eugene A ^b   Hines, Erin P ^c   Wallace, Elizabeth A ^a   Stanko, Jason P ^a   Lu, Yi ^d   Jefferson, Wendy N ^a   Newbold, Retha R ^a   Fenton, Suzanne E ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^d SOCIAL AND SCIENTIFIC SYSTEMS INC   (United States)

Author keywords

Cervix; Estradiol; Immature mice; Pathology; PFOA; Uterotrophic assay; Uterus; Vagina

Indexed keywords

ESTRADIOL; PERFLUOROOCTANOIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOASSAY; DISEASE SEVERITY; ENDOMETRIUM HYPERPLASIA; ENVIRONMENTAL EXPOSURE; FEMALE; GENITAL SYSTEM EXAMINATION; HISTOPATHOLOGY; MOUSE; NONHUMAN; ORGAN WEIGHT; REPRODUCTIVE TOXICITY; TOXICITY TESTING; UTERINE CERVIX; VAGINA;

ADMINISTRATION, ORAL; ANIMALS; BIOLOGICAL ASSAY; CERVIX UTERI; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; ESTRADIOL; FEMALE; FLUOROCARBONS; MICE; MICE, INBRED STRAINS; OCTANOIC ACIDS; ORGAN SIZE; UTERUS; VAGINA;

MUS;

EID: 84861531551     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2011.10.011     Document Type: Article

References (42)

1. EPA US. Perfluoroctanoic Acid (PFOA) and Fluorinated Telomers. http://epa.gov/oppt/pfoa/.
2. Hekster F.M., Laane R.W., de Voogt P. Environmental and toxicity effects of perfluoroalkylated substances. Rev Environ Contam Toxicol 2003, 179:99-121.
3. Houde M., Martin J.W., Letcher R.J., Solomon K.R., Muir D.C. Biological monitoring of polyfluoroalkyl substances: a review. Environ Sci Technol 2006, 40:3463-3473.
4. Letcher R.J., Bustnes J.O., Dietz R., Jenssen B.M., Jorgensen E.H., Sonne C., et al. Exposure and effects assessment of persistent organohalogen contaminants in arctic wildlife and fish. Sci Total Environ 2010, 408:2995-3043.
5. Keller J.M., Calafat A.M., Kato K., Ellefson M.E., Reagen W.K., Strynar M., et al. Determination of perfluorinated alkyl acid concentrations in human serum and milk standard reference materials. Anal Bioanal Chem 2010, 397:439-451.
6. Vestergren R., Cousins I.T. Tracking the pathways of human exposure to perfluorocarboxylates. Environ Sci Technol 2009, 43:5565-5575.
7. Betts K.S. Perfluoroalkyl acids: what is the evidence telling us?. Environ Health Perspect 2007, 115:A250-A256.
8. Skutlarek D., Exner M., Farber H. Perfluorinated surfactants in surface and drinking waters. Environ Sci Pollut Res Int 2006, 13:299-307.
9. Liu J., Li J., Zhao Y., Wang Y., Zhang L., Wu Y. The occurrence of perfluorinated alkyl compounds in human milk from different regions of China. Environ Int 2010, 36:433-438.
10. Haug L.S., Huber S., Becher G., Thomsen C. Characterisation of human exposure pathways to perfluorinated compounds - comparing exposure estimates with biomarkers of exposure. Environ Int 2011.
11. Kim S.K., Lee K.T., Kang C.S., Tao L., Kannan K., Kim K.R., et al. Distribution of perfluorochemicals between sera and milk from the same mothers and implications for prenatal and postnatal exposures. Environ Pollut 2011, 159:169-174.
12. Lau C., Thibodeaux J.R., Hanson R.G., Narotsky M.G., Rogers J.M., Lindstrom A.B., et al. Effects of perfluorooctanoic acid exposure during pregnancy in the mouse. Toxicol Sci 2006, 90:510-518.
13. Fenton S.E., Reiner J.L., Nakayama S.F., Delinsky A.D., Stanko J.P., Hines E.P., et al. Analysis of PFOA in dosed CD-1 mice. Part 2. Disposition of PFOA in tissues and fluids from pregnant and lactating mice and their pups. Reprod Toxicol 2009, 27:365-372.
14. Zhao Y., Tan Y.S., Haslam S.Z., Yang C. Perfluorooctanoic acid effects on steroid hormone and growth factor levels mediate stimulation of peripubertal mammary gland development in C57BL/6 mice. Toxicol Sci 2010, 115:214-224.
15. White S.S., Calafat A.M., Kuklenyik Z., Villanueva L., Zehr R.D., Helfant L., et al. exposure of mice is associated with altered mammary gland development in dams and female offspring. Toxicol Sci 2007, 96:133-144.
16. Elcombe C.R., Elcombe B.M., Foster J.R., Farrar D.G., Jung R., Chang S.C., et al. Hepatocellular hypertrophy and cell proliferation in Sprague-Dawley rats following dietary exposure to ammonium perfluorooctanoate occurs through increased activation of the xenosensor nuclear receptors PPARalpha and CAR/PXR. Arch Toxicol. 2010, 84:787-798.
17. Knox S.S., Jackson T., Javins B., Frisbee S.J., Shankar A., Ducatman A.M. Implications of early menopause in women exposed to perfluorocarbons. J Clin Endocrinol Metab 2011.
18. Shi Z., Zhang H., Liu Y., Xu M., Dai J. Alterations in gene expression and testosterone synthesis in the testes of male rats exposed to perfluorododecanoic acid. Toxicol Sci 2007, 98:206-215.
19. Shi Z., Zhang H., Ding L., Feng Y., Xu M., Dai J. The effect of perfluorododecanonic acid on endocrine status, sex hormones and expression of steroidogenic genes in pubertal female rats. Reprod Toxicol 2009, 27:352-359.
20. Yang C., Tan Y.S., Harkema J.R., Haslam S.Z. Differential effects of peripubertal exposure to perfluorooctanoic acid on mammary gland development in C57Bl/6 and Balb/c mouse strains. Reprod Toxicol 2009, 27:299-306.
21. Lopez-Espinosa M.J., Fletcher T., Armstrong B., Genser B., Dhatariya K., Mondal D., et al. Association of perfluorooctanoic acid (PFOA) and perfluorooctane sulfonate (PFOS) with age of puberty among children living near a chemical plant. Environ Sci Technol 2011.
22. Christensen K.Y., Maisonet M., Rubin C., Holmes A., Flanders W.D., Heron J., et al. Progression through puberty in girls enrolled in a contemporary British cohort. J Adolesc Health 2010, 47:282-289.
23. White S.S., Stanko J.P., Kato K., Calafat A.M., Hines E.P., Fenton S.E., et al. Gestational and chronic low-dose PFOA exposures and mammary gland growth and differentiation in three generations of CD-1 mice. Environ Health Perspect 2011, 119:1070-1076.
24. Macon M.B., Villanueva L.R., Tatum-Gibbs K., Zehr R.D., Strynar M.J., Stanko J.P., et al. Prenatal perfluorooctanoic acid exposure in CD-1 mice: low-dose developmental effects and internal dosimetry. Toxicol Sci 2011, 122:134-145.
25. Wei Y., Liu Y., Wang J., Tao Y., Dai J. Toxicogenomic analysis of the hepatic effects of perfluorooctanoic acid on rare minnows (Gobiocypris rarus). Toxicol Appl Pharmacol 2008, 226:285-297.
26. White S.S., Fenton S.E., Hines E.P. Endocrine disrupting properties of perfluorooctanoic acid. J Steroid Biochem Mol Biol 2011.
27. Newbold R.R., Jefferson W.N., Padilla-Banks E. The mouse uterotrophic assay: other end points. Environ Health Perspect 2001, 109:A569-A570.
28. Padilla-Banks E., Jefferson W.N., Newbold R.R. The immature mouse is a suitable model for detection of estrogenicity in the uterotropic bioassay. Environ Health Perspect 2001, 109:821-826.
29. Sibinski L. Two-Year oral (diet) toxicity/carcinogenicity study of fluorochemical FC-143 (perfluorooctane ammonium carboxylate) in rats. 1987, pp. 226-1137.
30. Hardisty J.F., Willson G.A., Brown W.R., McConnell E.E., Frame S.R., Gaylor D.W., et al. Pathology Working Group review and evaluation of proliferative lesions of mammary gland tissues in female rats fed ammonium perfluorooctanoate (APFO) in the diet for 2 years. Drug Chem Toxicol 2010, 33:131-137.
31. Benninghoff A.D., Bisson W.H., Koch D.C., Ehresman D.J., Kolluri S.K., Williams D.E. Estrogen-like activity of perfluoroalkyl acids in vivo and interaction with human and rainbow trout estrogen receptors in vitro. Toxicol Sci 2011, 120:42-58.
32. Tilton S.C., Orner G.A., Benninghoff A.D., Carpenter H.M., Hendricks J.D., Pereira C.B., et al. Genomic profiling reveals an alternate mechanism for hepatic tumor promotion by perfluorooctanoic acid in rainbow trout. Environ Health Perspect 2008, 116:1047-1055.
33. Wei Y., Dai J., Liu M., Wang J., Xu M., Zha J., et al. Estrogen-like properties of perfluorooctanoic acid as revealed by expressing hepatic estrogen-responsive genes in rare minnows (Gobiocypris rarus). Environ Toxicol Chem 2007, 26:2440-2447.
34. Aoyama H., Couse J.F., Hewitt S.C., Haseman J.K., He H., Zheng X., et al. Upregulation of estrogen receptor expression in the uterus of ovariectomized B6C3F1 mice and Ishikawa cells treated with bromoethane. Toxicol Appl Pharmacol 2005, 209:226-235.
35. Newbold R.R., McLachlan J.A. Vaginal adenosis and adenocarcinoma in mice exposed prenatally or neonatally to diethylstilbestrol. Cancer Res 1982, 42:2003-2011.
36. Eroschenko V.P., Osman F. Scanning electron microscopic changes in vaginal epithelium of suckling neonatal mice in response to estradiol or insecticide chlordecone (Kepone) passage in milk. Toxicology 1986, 38:175-185.
37. Holderegger C. Ultrastructural study of the mucification of the stratified epithelium of the mouse vagina. Cell Tissue Res 1980, 213:475-482.
38. McClain R., Wolz E., Davidovich A., Pfannkuch F., Edwards J., Bausch J. Acute, subchronic and chronic safety studies with genistein in rats. Food Chem Toxicol 2006, 44:56-80.
39. Mori T., Mills K.T., Bern H.A. Sensitivity of the vagina and uterus of mice neonatally exposed to estrogen or androgen to postnatal treatment with estrogen or androgen. Proc Soc Exp Biol Med 1992, 199:466-469.
40. DeManno D., Elger W., Garg R., Lee R., Schneider B., Hess-Stumpp H., et al. Asoprisnil (J867): a selective progesterone receptor modulator for gynecological therapy. Steroids 2003, 68:1019-1032.
41. Hayashi K., Hayashi M., Boutin E., Cunha G.R., Bernfield M., Trelstad R.L. Hormonal modification of epithelial differentiation and expression of cell surface heparan sulfate proteoglycan in the mouse vaginal epithelium. An immunohistochemical and electron microscopic study. Lab Invest 1988, 58:68-76.
42. Liu C., Du Y., Zhou B. Evaluation of estrogenic activities and mechanism of action of perfluorinated chemicals determined by vitellogenin induction in primary cultured tilapia hepatocytes. Aquat Toxicol 2007, 85:267-277.