The mammary gland is a sensitive pubertal target in CD-1 and C57Bl/6 mice following perinatal perfluorooctanoic acid (PFOA) exposure

Reproductive Toxicology

Volumn 54, Issue , 2015, Pages 26-36

  Tucker, Deirdre K ^a,b   Macon, Madisa B ^a,b   Strynar, Mark J ^c   Dagnino, Sonia ^c   Andersen, Erik ^c   Fenton, Suzanne E ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

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

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

C57Bl 6; CD 1; Estrous cycle; Mammary gland; Perfluorooctanoic acid; Puberty; Vaginal opening

Indexed keywords

HORMONE; PERFLUOROOCTANOIC ACID; FLUOROCARBON; OCTANOIC ACID DERIVATIVE; POLLUTANT;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BREAST DEVELOPMENT; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; ESTRUS; FEMALE; HEPATOMEGALY; HORMONE BLOOD LEVEL; MAMMARY GLAND; MOUSE; NONHUMAN; PRENATAL EXPOSURE; PROGENY; PUBERTY; ADVERSE EFFECTS; AGE; ANIMAL; BODY BURDEN; C57BL MOUSE; DOSE RESPONSE; DRUG EFFECTS; GESTATIONAL AGE; GROWTH, DEVELOPMENT AND AGING; LIVER; MATERNAL EXPOSURE; PATHOLOGY; POLLUTANT; PREGNANCY; RISK ASSESSMENT; RISK FACTOR; SEXUAL DEVELOPMENT; TOXICITY; UDDER;

AGE FACTORS; ANIMALS; BODY BURDEN; CAPRYLATES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; FEMALE; FLUOROCARBONS; GESTATIONAL AGE; LIVER; MAMMARY GLANDS, ANIMAL; MATERNAL EXPOSURE; MICE, INBRED C57BL; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK ASSESSMENT; RISK FACTORS; SEXUAL DEVELOPMENT;

EID: 84941268160     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2014.12.002     Document Type: Article

References (55)

1. CDC fourth national report on human exposure to environmental chemicals: updated tables 2013, http://www.cdc.gov/exposurereport/pdf/FourthReport_UpdatedTables_Mar2013.pdf [accessed 20.02.14].
2. Emmett E., Zhang H., Shofer F., Freeman D., Rodway N., Desai C., et al. Community exposure to perfluorooctanoate: relationships between serum levels and certain health parameters. J Occup Environ Med 2006, 48(8):771-779.
3. Frisbee S., Brooks A., Maher A., Flensborg P., Arnold S., Flethcher T., et al. The C8 health project: design, methods, and participants. Environ Health Perspect 2009, 117(12):1873-1882.
4. Apelberg B., Witter F., Herbstman J., Calafat A., Halden R., Needham L., et al. Cord serum concentrations of perfluorooctane sulfonate (PFOS) and perfluorooctanoate (PFOA) in relation to weight and size at birth. Environ Health Perspect 2007, 115(11):1670-1676.
5. Fenton S., Reiner J., Nakayama S., Delinsky A., Stanko J., Hines E., 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(3-4):365-372.
6. Fromme H., Midasch O., Twardella D., Angerer J., Boehmer S., Liebl B. Occurrence of perfluorinated substances in an adult German population in southern Bavaria. Int Arch Occup Environ Health 2007, 80(4):313-319.
7. Olsen G. Evaluation of the half-life (t1/2) of elimination of perfluorooctanesulfonate (PFOS), perfluorohexanesulfonate (PFHS), and perfluorooctanoate (PFOA) from human serum. FLUOROS: international symposium on fluorinated alkyl organics in the environment, TOX017 2005.
8. Mondal D., Weldon R., Armstrong B., Gibson L., Lopez-Espinosa M., Shin H., et al. Breastfeeding: a potential excretion route for mothers and implications for infant exposure to perfluoroalkyl acids. Environ Health Perspect 2014, 122(2):187-192.
9. Guerrero-Preston R., Goldman L., Brebi-Mieville P., Ili-Gangas C., Lebron C., Witter F., et al. Global DNA hypomethylation is associated with in utero exposure to cotinine and perfluorinated alkyl compounds. Epigenetics 2010, 5(6):539-546.
10. Knower K., To S., Leung Y., Ho S., Clyne C. Endocrine disruption of the epigenome: a breast cancer link. Endocr Relat Cancer 2014, 21(2):T33-T55.
11. Biegel L., Hurtt M., Frame S., O'Connor J., Cook J. Mechanisms of extrahepatic tumor induction by peroxisomes proliferators in male CD rats. Toxicol Sci 2001, 60(1):44-55.
12. Kennedy G., Butenhoff J., Olsen G., O'Connor J., Seacat A., Perkins R., et al. The toxicology of perfluorooctanoate. Crit Rev Toxicol 2004, 34(4):351-384.
13. Lau C., Thibodeaux J., Hanson R., Narotsky M., Rogers J., Lindstrom A., et al. Effects of perfluorooctanoic acid exposure during pregnancy in the mouse. Toxicol Sci 2006, 90(2):510-518.
14. Onishchenko N., Fischer C., Wan Ibrahim W., Negri S., Spulber S., Cottica D., et al. Prenatal exposure to PFOS or PFOA alters motor function in mice in a sex-related manner. Neurotox Res 2011, 19(3):452-461.
15. Macon M., Villanueva L., Tatum-Gibbs K., Zehr R., Strynar M., Stanko J., et al. Prenatal perfluorooctanoic acid exposure in CD-1 mice: low-dose developmental effects and internal dosimetry. Toxicol Sci 2011, 122(1):134-145.
16. Gilberstein G. Postnatal mammary gland morphogenesis. Microsc Res Tech 2001, 52:155-162.
17. Gjorevski N., Nelson C. Integrated morphodynamic signaling of the mammary gland. Nat Rev Mol Cell Biol 2011, 12:581-593.
18. Tiede B., Kang Y. From milk to malignancy; the role of mammary stem cells in development, pregnancy and breast cancer. Cell Res 2011, 21:245-257.
19. US EPA Office of Science and Coordination and Policy. Endocrine disruptors: basic information, [accessed 1.07.14]. http://www.epa.gov/endo/pubs/edspoverview/whatare.htm.
20. Zhao Y., Tan Y., Haslam S., 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(1):214-224.
21. Fenton S. Endocrine-disrupting compounds and mammary gland development: early exposure and later life consequences. Endocrinology 2006, 147(6 Suppl):S18-S24.
22. Macon M., Fenton S. Endocrine disruptors and the breast: early life effects and later life disease. J Mammary Gland Biol Neoplasia 2013, 18(1):43-61.
23. White S., Fenton S., Hines E. Endocrine disrupting properties of perfluorooctanoic acid. J Steroid Biochem Mol Biol 2011, 127(1-2):16-26.
24. Yang C., Tan Y., Harkema J., Haslam S. Differential effects of peripubertal exposure to perfluorooctanoic acid on mammary gland development in C57Bl/6 and Balb/c mouse strains. Reprod Toxicol 2009, 27(3-4):299-306.
25. Lopez-Espinosa 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, 45(19):8160-8166.
26. Vandenberg L., Colborn T., Hayes T., Heindel J., Jacobs D., Lee D., et al. Hormones and endocrine disrupting chemicals: low dose effects and nonmonotonic dose responses. Endocr Rev 2012, 33(3):378-455.
27. Whitten W. Modification of the oestrous cycle of the mouse by external stimuli associated with the male. J Endocrinol 1956, 13(4):399-404.
28. Whitten W., Bronson F., Greenstein J. Estrus-inducing pheromone of male mice: transport by movement of air. Science 1968, 161(3841):584-585.
29. Silver L, Mouse genetics: concepts and applications, [accessed 13.09.14]. http://www.informatics.jax.org/silver/chapters/4-3.shtml.
30. Nelson J., Karelus K., Felicio L., Johnson T. Genetic influences on the timing of puberty in mice. Biol Reprod 1990, 42:649-655.
31. Caligioni C. Assessing reproductive status/stages in mice. Curr Protoc Neurosci 2009, 48. A.4I.1-A.4I.8.
32. Davis B., Fenton S. The mammary gland. Haschek and Rousseaux's handbook of toxicologic pathology 2013, 2665-2694. Elsevier, Inc., Academic Press (USA), [Chapter 61]. 3rd ed. W.M. Haschek, C.G. Rousseaux, M.A. Wallig (Eds.).
33. Reiner J., Nakayam S., Delinsky A., Stanko J., Fenton S., Lindstrom A., et al. Analysis of PFOA in dosed CD1 mice. Part 1. Methods development for the analysis of tissues and fluids from pregnant and lactating mice and their pups. Reprod Toxicol 2009, 27(3-4):360-364.
34. Lou I., Wambaugh J., Lau C., Hanson R., Lindstrom A., Strynar M., et al. Modeling single and repeated dose pharmacokinetics of PFOA in mice. Toxicol Sci 2009, 107:331-341.
35. Brisken C., O'Malley B. Hormone action in the mammary gland. Cold Spring Harbor Perspect Biol 2010, 2:a003178.
36. Bordini B., Rosenfield R. Normal pubertal development: Part I: The endocrine basis of puberty. Pediatr Rev 2011, 32(6):223-229.
37. Zhao Y., Tan Y., Strynar M., Perez G., Haslam S., Yang C. Perfluorooctanoic acid effects on ovaries mediate its inhibition of peripubertal mammary gland development in Balb/c and C57Bl/6 mice. Reprod Toxicol 2012, 33(4):563-576.
38. Yoon C. Homeostasis associated with heterozygosity in the genetics of timing of vaginal opening in the house mouse. Genetics 1955, 40(3):297-309.
39. CDC Fourth national report on human exposure to environmental chemicals: updated tables 2014, http://www.cdc.gov/exposurereport/pdf/FourthReport_UpdatedTables_Jul2014.pdf [accessed 21.07.14].
40. Biro F., Greenspan L., Galvez M., Pinney S., Teitelbaum S., Windham G., et al. Onset of breast development in a longitudinal cohort. Pediatrics 2013, 10.1542/peds.2012-3773.
41. Pinney S., Biro F., Windham G., Herrick R., Yaghjyan L., Calafat A., et al. Serum biomarkers of polyfluoroalkyl compound exposure in young girls in Greater Cincinnati and the San Francisco Bay Area, USA. Environ Pollut 2014, 184:327-334.
42. Kale A., Deardorff J., Lahiff M., Laurent C., Greenspan L., Hiatt R., et al. Breastfeeding versus formula-feeding and girls' pubertal development. Matern Child Health J 2014, 10.1007/s10995-014-1533-9.
43. Buck G., Gray L., Marcus M., Ojeda S., Pescovitz O., Witchel S., et al. Environmental factors and puberty timing: expert panel research needs. Pediatrics 2008, 121(Sup 3):S192-S207.
44. Fenton S., Hamm J., Birnbaum L., Youngblood G. Persistent abnormalities in the rat mammary gland following gestational and lactational exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Toxicol Sci 2002, 67(1):63-74.
45. Markey C., Luqui E., Munoz-de Toro M., Sonnenschein C., Soto A. In utero exposure to bisphenol A alters the development and tissue organization of the mouse mammary gland. Biol Reprod 2001, 65(4):12515-21223.
46. Munoz-de Toro M., Markey C., Wadia P., Luque E., Rubin B., Sonnenschein C., et al. Perinatal exposure to bisphenol A alters peripubertal mammary gland development in mice. Endocrinology 2005, 146(9):4138-4147.
47. Wadia P., Vandenberg L., Schaeberle C., Rubin B., Sonnenschein C., Soto A. Perinatal bisphenol A exposure increases estrogen sensitivity of the mammary gland in diverse mouse strains. Environ Health Perspect 2007, 115(4):592-598.
48. White S., Calafat A., Kuklenyik Z., Villanueva L., Zehr R., Helfant L., et al. Gestational PFOA exposure of mice is associated with altered mammary gland development in dams and female offspring. Toxicol Sci 2007, 96(1):133-144.
49. White S., Kato K., Jia L., Basden B., Calafat A., Hines E., et al. Effects of perfluorooctanoic acid on mouse mammary gland development and differentiation resulting from cross foster and restricted gestational exposure. Reprod Toxicol 2007, 27:289-298.
50. Macon M.B., Ren H., Fenton S.E. Prenatal PFOA exposure alters gene expression pathways in murine mammary gland. Toxicol Sci 2014, (in press). 10.1093/toxsci/kfu253.
51. Bonefeld-Jorgensen C., Long M., Bossi R., Ayotte P., Asmund G., Kruger T., et al. Perfluorinated compounds are related to breast cancer risk in Greenlandic Inuit: a case control study. Environ Health 2011, 10:88.
52. Bonefeld-Jørgensen E., Long M., Fredslund S., Bossi R., Olsen J. Breast cancer risk after exposure to perfluorinated compounds in Danish women: a case-control study nested in the Danish National Birth Cohort. Cancer Causes Control 2014, PMID: 25148915.
53. IBCERCC, Interagency Breast Cancer and the Environment Research Coordinating Committee.Department of Health and Human Services Breast cancer and the environment: prioritizing prevention 2013, Available at: http://www.niehs.nih.gov/about/assets/docs/ibcercc_full_508.pdf.
54. Osborne G., Rudel R., Schwarzmann M. Evaluating chemical effects on mammary gland development: a critical need in disease prevention. Reprod Toxicol 2014, 10.1016/j.reprotox.07.077.
55. US EPA Chemical Safety and Pollution Prevention. Pollution prevention and toxics: perfluorooctanoic acid (PFOA) and fluorinated telomers, [accessed 21.07.14]. http://www.epa.gov/oppt/pfoa/.