Studies in experimental autoimmune encephalomyelitis do not support developmental bisphenol a exposure as an environmental factor in increasing multiple sclerosis risk

Toxicological Sciences

Volumn 135, Issue 1, 2013, Pages 91-102

  Krementsov, Dimitry N ^a   Katchy, Anne ^b   Case, Laure K ^a   Carr, Frances E ^c   Davis, Barbara ^d   Williams, Cecilia ^b   Teuscher, Cory ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

^b University of Houston   (United States)

^c UNIVERSITY OF VERMONT   (Canada)

^d Nemucore Medical Innovations   (United States)

Author keywords

Autoimmunity; Bisphenol A; Central nervous system; Developmental; Endocrine disruption; Environmental exposure; Experimental autoimmune encephalomyelitis; Gestational; Multiple sclerosis; PDGF; T cell; Testes

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; COMPLEMENTARY DNA; DRINKING WATER; GAMMA INTERFERON; INTERLEUKIN 17; MESSENGER RNA; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR;

ALLERGIC ENCEPHALOMYELITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DISEASE COURSE; DISEASE SEVERITY; ENVIRONMENTAL FACTOR; FEMALE; GENE EXPRESSION; INCIDENCE; MALE; MOUSE; MULTIPLE SCLEROSIS; NONHUMAN; PRENATAL EXPOSURE; RECEPTOR DOWN REGULATION; SEX DIFFERENCE; T LYMPHOCYTE; TESTIS DEVELOPMENT; WEANING;

AUTOIMMUNITY; BISPHENOL A; CENTRAL NERVOUS SYSTEM; DEVELOPMENTAL; ENDOCRINE DISRUPTION; ENVIRONMENTAL EXPOSURE; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; GESTATIONAL; MULTIPLE SCLEROSIS; PDGF.; T CELL; TESTES;

ANIMALS; BENZHYDRYL COMPOUNDS; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; ENDOCRINE DISRUPTORS; FEMALE; FETUS; INTERFERON-GAMMA; INTERLEUKIN-17; MALE; MICE; MICE, INBRED C57BL; MULTIPLE SCLEROSIS; PHENOLS; PREGNANCY; RISK;

EID: 84883183897     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kft141     Document Type: Article

References (76)

1. Alizadeh, M., Ota, F., Hosoi, K., Kato, M., Sakai, T., and Satter, M. A. (2006). Altered allergic cytokine and antibody response in mice treated with Bisphenol A. J. Med. Invest. 53, 70-80.
2. Balakrishnan, B., Henare, K., Thorstensen, E. B., Ponnampalam, A. P., and Mitchell, M. D. (2010). Transfer of bisphenol A across the human placenta. Am. J. Obstet. Gynecol. 202, 393.e1-393.e7.
3. Barnes, S. (2010). The biochemistry, chemistry and physiology of the isoflavones in soybeans and their food products. Lymphat. Res. Biol. 8, 89-98.
4. Basciani, S., Mariani, S., Spera, G., and Gnessi, L. (2010). Role of plateletderived growth factors in the testis. Endocr. Rev. 31, 916-939.
5. Bauer, S. M., Roy, A., Emo, J., Chapman, T. J., Georas, S. N., and Lawrence, B. P. (2012). The effects of maternal exposure to bisphenol A on allergic lung inflammation into adulthood. Toxicol. Sci. 130, 82-93.
6. Bryant, C. D. (2011). The blessings and curses of C57BL/6 substrains in mouse genetic studies. Ann. N.Y. Acad. Sci. 1245, 31-33.
7. Bushnik, T., Haines, D., Levallois, P., Levesque, J., Van Oostdam, J., and Viau, C. (2010). Lead and bisphenol A concentrations in the Canadian population. Health Rep. 21, 7-18.
8. Cerione, R. A. (2004). Cdc42: New roads to travel. Trends Cell Biol. 14, 127-132.
9. Chen, Y. T., Alpen, B., Ono, T., Gure, A. O., Scanlan, M. A., Biggs, W. H., III, Arden, K., Nakayama, E., and Old, L. J. (2003). Identification and characterization of mouse SSX genes: A multigene family on the X chromosome with restricted cancer/testis expression. Genomics 82, 628-636.
10. Courtney, A. M., Treadaway, K., Remington, G., and Frohman, E. (2009). Multiple sclerosis. Med. Clin. North Am. 93, 451-476, ix-x.
11. Dodds, E. C., and Lawson, W. (1938). Molecular structure in relation to oestrogenic activity. Compounds without a phenanthrene nucleus. Proc. R. Soc. Lond. B Biol. Sci., 125, 222-232.
12. Dolinoy, D. C., Huang, D., and Jirtle, R. L. (2007). Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc. Natl. Acad. Sci. U.S.A. 104, 13056-13061.
13. Donohue, K. M., Miller, R. L., Perzanowski, M. S., Just, A. C., Hoepner, L. A., Arunajadai, S., Canfield, S., Resnick, D., Calafat, A. M., Perera, F. P., et al. (2013). Prenatal and postnatal bisphenol A exposure and asthma development among inner-city children. J. Allergy Clin. Immunol. 131, 736-742.
14. Ebers, G. C., Sadovnick, A. D., Dyment, D. A., Yee, I. M., Willer, C. J., and Risch, N. (2004). Parent-of-origin effect in multiple sclerosis: Observations in half-siblings. Lancet 363, 1773-1774.
15. Erler, C., and Novak, J. (2010). Bisphenol a exposure: Human risk and health policy. J. Pediatr. Nurs. 25, 400-407.
16. Fagin, D. (2012). Toxicology: The learning curve. Nature 490, 462-465.
17. Fiedler, S. E., Dudiki, T., Vijayaraghavan, S., and Carr, D. W. (2013). Loss of R2D2 proteins ROPN1 and ROPN1L causes defects in murine sperm motility, phosphorylation, and fibrous sheath integrity. Biol. Reprod. 88, 41.
18. Griffith, J. S., Jensen, S. M., Lunceford, J. K., Kahn, M. W., Zheng, Y., Falase, E. A., Lyttle, C. R., and Teuscher, C. (1997). Evidence for the genetic control of estradiol-regulated responses. Implications for variation in normal and pathological hormone-dependent phenotypes. Am. J. Pathol. 150, 2223-2230.
19. Handunnetthi, L., Ramagopalan, S. V., and Ebers, G. C. (2010). Multiple sclerosis, vitamin D, and HLA-DRB1*15. Neurology 74, 1905-1910.
20. Haueter, S., Kawasumi, M., Asner, I., Brykczynska, U., Cinelli, P., Moisyadi, S., Bürki, K., Peters, A. H., and Pelczar, P. (2010). Genetic vasectomy-overexpression of Prm1-EGFP fusion protein in elongating spermatids causes dominant male sterility in mice. Genesis 48, 151-160.
21. Herrera, B. M., Ramagopalan, S. V., Lincoln, M. R., Orton, S. M., Chao, M. J., Sadovnick, A. D., and Ebers, G. C. (2008). Parent-of-origin effects in MS: Observations from avuncular pairs. Neurology 71, 799-803.
22. Holladay, S. D., Xiao, S., Diao, H., Barber, J., Nagy, T., Ye, X., and Gogal, R. M., Jr. (2010). Perinatal bisphenol A exposure in C57B6/129svj male mice: Potential altered cytokine/chemokine production in adulthood. Int. J. Environ. Res. Public Health 7, 2845-2852.
23. Honma, S., Suzuki, A., Buchanan, D. L., Katsu, Y., Watanabe, H., and Iguchi, T. (2002). Low dose effect of in utero exposure to bisphenol A and diethylstilbestrol on female mouse reproduction. Reprod. Toxicol. 16, 117-122.
24. Hoppenbrouwers, I. A., Liu, F., Aulchenko, Y. S., Ebers, G. C., Oostra, B. A., van Duijn, C. M., and Hintzen, R. Q. (2008). Maternal transmission of multiple sclerosis in a dutch population. Arch. Neurol. 65, 345-348.
25. Hoyer-Fender, S., Petersen, C., Brohmann, H., Rhee, K., and Wolgemuth, D. J. (1998). Mouse Odf2 cDNAs consist of evolutionary conserved as well as highly variable sequences and encode outer dense fiber proteins of the sperm tail. Mol. Reprod. Dev. 51, 167-175.
26. Kabuto, H., Amakawa, M., and Shishibori, T. (2004). Exposure to bisphenol A during embryonic/fetal life and infancy increases oxidative injury and causes underdevelopment of the brain and testis in mice. Life Sci. 74, 2931-2940.
27. Kang, T. H., and Kim, K. T. (2008). VRK3-mediated inactivation of ERK signaling in adult and embryonic rodent tissues. Biochim. Biophys. Acta 1783, 49-58.
28. Kuiper, G. G., Lemmen, J. G., Carlsson, B., Corton, J. C., Safe, S. H., van der Saag, P. T., van der Burg, B., and Gustafsson, J. A. (1998). Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139, 4252-4263.
29. LaRocca, J., Boyajian, A., Brown, C., Smith, S. D., and Hixon, M. (2011). Effects of in utero exposure to Bisphenol A or diethylstilbestrol on the adult male reproductive system. Birth Defects Res. B Dev. Reprod. Toxicol. 92, 526-533.
30. Lee, C. H., Jeon, Y. T., Kim, S. H., and Song, Y. S. (2007). NF-kappaB as a potential molecular target for cancer therapy. Biofactors 29, 19-35.
31. Liu, P., Lu, J., Cardoso, W. V., and Vaziri, C. (2008). The SPARC-related factor SMOC-2 promotes growth factor-induced cyclin D1 expression and DNA synthesis via integrin-linked kinase. Mol. Biol. Cell 19, 248-261.
32. Miao, M., Yuan, W., He, Y., Zhou, Z., Wang, J., Gao, E., Li, G., and Li, D. K. (2011). In utero exposure to bisphenol-A and anogenital distance of male offspring. Birth Defects Res. A Clin. Mol. Teratol. 91, 867-872.
33. Midoro-Horiuti, T., Tiwari, R., Watson, C. S., and Goldblum, R. M. (2010). Maternal bisphenol a exposure promotes the development of experimental asthma in mouse pups. Environ. Health Perspect. 118, 273-277.
34. Nakai, M., Uchida, K., and Teuscher, C. (1999). The development of male reproductive organ abnormalities after neonatal exposure to tamoxifen is genetically determined. J. Androl. 20, 626-634.
35. Nakajima, Y., Goldblum, R. M., and Midoro-Horiuti, T. (2012). Fetal exposure to bisphenol A as a risk factor for the development of childhood asthma: An animal model study. Environ. Health 11, 8.
36. Nishikawa, M., Iwano, H., Yanagisawa, R., Koike, N., Inoue, H., and Yokota, H. (2010). Placental transfer of conjugated bisphenol A and subsequent reactivation in the rat fetus. Environ. Health Perspect. 118, 1196-1203.
37. Noseworthy, J. H., Lucchinetti, C., Rodriguez, M., and Weinshenker, B. G. (2000). Multiple sclerosis. N. Engl. J. Med. 343, 938-952.
38. Noubade, R., Krementsov, D. N., Del Rio, R., Thornton, T., Nagaleekar, V., Saligrama, N., Spitzack, A., Spach, K., Sabio, G., Davis, R. J., et al. (2011). Activation of p38 MAPK in CD4 T cells controls IL-17 production and autoimmune encephalomyelitis. Blood 118, 3290-3300.
39. Ohshima, Y., Yamada, A., Tokuriki, S., Yasutomi, M., Omata, N., and Mayumi, M. (2007). Transmaternal exposure to bisphenol a modulates the development of oral tolerance. Pediatr. Res. 62, 60-64.
40. Orton, S. M., Herrera, B. M., Yee, I. M., Valdar, W., Ramagopalan, S. V., Sadovnick, A. D., and Ebers, G. C. (2006). Sex ratio of multiple sclerosis in Canada: A longitudinal study. Lancet Neurol. 5, 932-936.
41. Park, Y. J., and Luger, K. (2006). Structure and function of nucleosome assembly proteins. Biochem. Cell Biol. 84, 549-558.
42. Pazin, D. E., and Albrecht, K. H. (2009). Developmental expression of Smoc1 and Smoc2 suggests potential roles in fetal gonad and reproductive tract differentiation. Dev. Dyn. 238, 2877-2890.
43. Polanczyk, M., Yellayi, S., Zamora, A., Subramanian, S., Tovey, M., Vandenbark, A. A., Offner, H., Zachary, J. F., Fillmore, P. D., Blankenhorn, E. P., et al. (2004). Estrogen receptor-1 (Esr1) and -2 (Esr2) regulate the severity of clinical experimental allergic encephalomyelitis in male mice. Am. J. Pathol. 164, 1915-1924.
44. Polanczyk, M., Zamora, A., Subramanian, S., Matejuk, A., Hess, D. L., Blankenhorn, E. P., Teuscher, C., Vandenbark, A. A., and Offner, H. (2003). The protective effect of 17beta-estradiol on experimental autoimmune encephalomyelitis is mediated through estrogen receptor-alpha. Am. J. Pathol. 163, 1599-1605.
45. Ramagopalan, S. V., Byrnes, J. K., Orton, S. M., Dyment, D. A., Guimond, C., Yee, I. M., Ebers, G. C., and Sadovnick, A. D. (2010). Sex ratio of multiple sclerosis and clinical phenotype. Eur. J. Neurol. 17, 634-637.
46. Ramagopalan, S. V., Yee, I. M., Dyment, D. A., Orton, S. M., Marrie, R. A., Sadovnick, A. D., and Ebers, G. C. (2009). Parent-of-origin effect in multiple sclerosis: Observations from interracial matings. Neurology 73, 602-605.
47. Richter, C. A., Birnbaum, L. S., Farabollini, F., Newbold, R. R., Rubin, B. S., Talsness, C. E., Vandenbergh, J. G., Walser-Kuntz, D. R., and vom Saal, F. S. (2007). In vivo effects of bisphenol A in laboratory rodent studies. Reprod. Toxicol. 24, 199-224.
48. Richter K., Wirta V., Dahl L., Bruce S., Lundeberg J., Carlsson L., and Williams C. (2006). Global gene expression analyses of hematopoietic stem cell-like cell lines with inducible Lhx2 expression. BMC Genomics. 7, 75.
49. Ricklin, D., Hajishengallis, G., Yang, K., and Lambris, J. D. (2010). Complement: A key system for immune surveillance and homeostasis. Nat. Immunol. 11, 785-797.
50. Rogers, J. A., Metz, L., and Yong, V. W. (2013). Review: Endocrine disrupting chemicals and immune responses: A focus on bisphenol-A and its potential mechanisms. Mol. Immunol. 53, 421-430.
51. Roper, R. J., Griffith, J. S., Lyttle, C. R., Doerge, R. W., McNabb, A. W., Broadbent, R. E., and Teuscher, C. (1999). Interacting quantitative trait loci control phenotypic variation in murine estradiol-regulated responses. Endocrinology 140, 556-561.
52. Roy, A., Bauer, S. M., and Lawrence, B. P. (2012). Developmental exposure to bisphenol A modulates innate but not adaptive immune responses to influenza A virus infection. PLoS One 7, e38448.
53. Roy, A., Gaylo, A., Cao, W., Saubermann, L. J., and Lawrence, B. P. (2013). Neither direct nor developmental exposure to bisphenol A alters the severity of experimental inflammatory colitis in mice [Epub ahead of print]. J. Immunotoxicol.
54. Sawai, C., Anderson, K., and Walser-Kuntz, D. (2003). Effect of bisphenol A on murine immune function: Modulation of interferon-gamma, IgG2a, and disease symptoms in NZB X NZW F1 mice. Environ. Health Perspect. 111, 1883-1887.
55. Shor, D., Sathyapalan, T., Atkin, S. L., and Thatcher, N. J. (2012). Does equol production determine soy endocrine effects? Eur. J. Nutr. 51, 389-398.
56. Soto, A. M., and Sonnenschein, C. (2010). Environmental causes of cancer: Endocrine disruptors as carcinogens. Nat. Rev. Endocrinol. 6, 363-370.
57. Spanier, A. J., Kahn, R. S., Kunselman, A. R., Hornung, R., Xu, Y., Calafat, A. M., and Lanphear, B. P. (2012). Prenatal exposure to bisphenol A and child wheeze from birth to 3 years of age. Environ. Health Perspect. 120, 916-920.
58. Spearow, J. L., Doemeny, P., Sera, R., Leffler, R., and Barkley, M. (1999). Genetic variation in susceptibility to endocrine disruption by estrogen in mice. Science 285, 1259-1261.
59. Spearow, J. L., O'Henley, P., Doemeny, P., Sera, R., Leffler, R., Sofos, T., and Barkley, M. (2001). Genetic variation in physiological sensitivity to estrogen in mice. APMIS 109, 356-364.
60. Stromnes, I. M., and Goverman, J. M. (2006). Active induction of experimental allergic encephalomyelitis. Nat. Protoc. 1, 1810-1819.
61. Thuillier, R., Mazer, M., Manku, G., Boisvert, A., Wang, Y., and Culty, M. (2010). Interdependence of platelet-derived growth factor and estrogensignaling pathways in inducing neonatal rat testicular gonocytes proliferation. Biol. Reprod. 82, 825-836.
62. Thuillier, R., Wang, Y., and Culty, M. (2003). Prenatal exposure to estrogenic compounds alters the expression pattern of platelet-derived growth factor receptors alpha and beta in neonatal rat testis: Identification of gonocytes as targets of estrogen exposure. Biol. Reprod. 68, 867-880.
63. Vaidya, S. V., and Kulkarni, H. (2012). Association of urinary bisphenol A concentration with allergic asthma: Results from the National Health and Nutrition Examination Survey 2005-2006. J. Asthma 49, 800-806.
64. vom Saal, F. S., Cooke, P. S., Buchanan, D. L., Palanza, P., Thayer, K. A., Nagel, S. C., Parmigiani, S., and Welshons, W. V. (1998). A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol. Ind. Health 14, 239-260.
65. Wall, E. H., Hewitt, S. C., Liu, L., del Rio, R., Case, L. K., Lin, C. Y., Korach, K. S., and Teuscher, C. (2013). Genetic control of estrogen-regulated transcriptional and cellular responses in mouse uterus. FASEB J. 27, 1874-1886.
66. Weinstock-Guttman, B., Jacobs, L. D., Brownscheidle, C. M., Baier, M., Rea, D. F., Apatoff, B. R., Blitz, K. M., Coyle, P. K., Frontera, A. T., Goodman, A. D., et al. (2003). Multiple sclerosis characteristics in African American patients in the New York State Multiple Sclerosis Consortium. Mult. Scler. 9, 293-298.
67. Willer, C. J., Dyment, D. A., Risch, N. J., Sadovnick, A. D., and Ebers, G. C. (2003). Twin concordance and sibling recurrence rates in multiple sclerosis. Proc. Natl. Acad. Sci. U.S.A. 100, 12877-12882.
68. Williams C. Edvardsson K., Lewandowski, S. A., Ström, A., and Gustafsson, J. A. (2008). A genome-wide study of the repressive effects of estrogen receptor beta on estrogen receptor alpha signaling in breast cancer cells. Oncogene 27, 1019-1032.
69. Xi, W., Wan, H. T., Zhao, Y. G., Wong, M. H., Giesy, J. P., and Wong, C. K. (2011). Effects of perinatal exposure to bisphenol A and di(2-ethylhexyl)-phthalate on gonadal development of male mice. Environ. Sci. Pollut. Res. Int. 19, 2515-2527.
70. Yan, H., Takamoto, M., and Sugane, K. (2008). Exposure to Bisphenol A prenatally or in adulthood promotes T(H)2 cytokine production associated with reduction of CD4CD25 regulatory T cells. Environ. Health Perspect. 116, 514-519.
71. Yoshino, S., Yamaki, K., Li, X., Sai, T., Yanagisawa, R., Takano, H., Taneda, S., Hayashi, H., and Mori, Y. (2004). Prenatal exposure to bisphenol A upregulates immune responses, including T helper 1 and T helper 2 responses, in mice. Immunology 112, 489-495.
72. Youn, J. Y., Park, H. Y., Lee, J. W., Jung, I. O., Choi, K. H., Kim, K., and Cho, K. H. (2002). Evaluation of the immune response following exposure of mice to bisphenol A: Induction of Th1 cytokine and prolactin by BPA exposure in the mouse spleen cells. Arch. Pharm. Res. 25, 946-953.
73. Yurino, H., Ishikawa, S., Sato, T., Akadegawa, K., Ito, T., Ueha, S., Inadera, H., and Matsushima, K. (2004). Endocrine disruptors (environmental estrogens) enhance autoantibody production by B1 cells. Toxicol. Sci. 81, 139-147.
74. Zariwala, M., O'Neal, W. K., Noone, P. G., Leigh, M. W., Knowles, M. R., and Ostrowski, L. E. (2004). Investigation of the possible role of a novel gene, DPCD, in primary ciliary dyskinesia. Am. J. Respir. Cell Mol. Biol. 30, 428-434.
75. Zhao, M., Shirley, C. R., Mounsey, S., and Meistrich, M. L. (2004). Nucleoprotein transitions during spermiogenesis in mice with transition nuclear protein Tnp1 and Tnp2 mutations. Biol. Reprod. 71, 1016-1025.
76. Zheng, Y., Sundstrom, S. A., Lyttle, C. R., and Teuscher, C. (1989). Differential expression of estrogen-regulated CD4 and Ia positive cells in the immature rat uterus. J. Leukoc. Biol. 46, 493-496.