Indole-3-carbinol attenuates the deleterious gestational effects of bisphenol A exposure on the prostate gland of male F1 rats

Reproductive Toxicology

Volumn 43, Issue , 2014, Pages 56-66

  Brandt, Joyce Zalotti ^a   Silveira, Lívia Teresa R ^a   Grassi, Tony Fernando ^a   Anselmo Franci, Janete A ^b   Fávaro, Wagner José ^c   Felisbino, Sérgio Luis ^a   Barbisan, Luis Fernando ^a   Scarano, Wellerson Rodrigo ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF CAMPINAS   (Brazil)

Author keywords

Bisphenol A; Chemoprevention; Indole 3 carbinol; Inflammation; Prostate; Reproductive toxicology

Indexed keywords

3 INDOLEMETHANOL; 4,4' ISOPROPYLIDENEDIPHENOL; ANDROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BASEMENT MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG ACTIVITY; DRUG EFFICACY; ENVIRONMENTAL EXPOSURE; FEMALE; GESTATIONAL AGE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MORPHOGENESIS; NONHUMAN; OPTICAL DENSITY; PERINATAL PERIOD; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROSTATE DISEASE; PROTEIN EXPRESSION; RAT; TREATMENT RESPONSE;

RATTUS;

BISPHENOL A; CHEMOPREVENTION; INDOLE-3-CARBINOL; INFLAMMATION; PROSTATE; REPRODUCTIVE TOXICOLOGY;

ANIMALS; APOPTOSIS; BENZHYDRYL COMPOUNDS; CELL PROLIFERATION; ENDOCRINE DISRUPTORS; EPITHELIAL CELLS; ESTROGEN RECEPTOR ALPHA; FEMALE; INDOLES; MALE; MATERNAL-FETAL EXCHANGE; PHENOLS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROSTATE; PROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANDROGEN; RECEPTORS, THROMBIN;

EID: 84888797197     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2013.11.001     Document Type: Article

References (71)

1. Rubin B.S. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 2011, 127:27-34.
2. Howdeshell K.L., Peterman P.H., Judy B.M., Taylor J.A., Orazio C.E., Ruhlen R.L., et al. Bisphenol A is released from used polycarbonate animal cages into water at room temperature. Environ Health Perspect 2003, 111:1180-1187.
3. Diamanti-Kandarakis E., Bourguignon J.P., Giudice L.C., Hauser R., Prins G.S., Soto A.M., et al. Endocrine-disrupting chemicals: an endocrine society scientific statement. Endocr Rev 2009, 30:293-342.
4. Kang J.H., Kondo F., Katayama Y. Human exposure to bisphenol A. Toxicology 2006, 226:79-89.
5. Krishnan A.V., Stathis P., Permuth S.F., Tokes L., Feldman D. Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 1993, 132:2279-2286.
6. Vogel S.A. The politics of plastics: the making and unmaking of bisphenol a safety. Am J Public Health 2009, 559-566.
7. Durando M., Kass L., Piva J., Sonnenschein C., Soto A.M., Luque E.H., et al. Prenatal bisphenol A exposure induces preneoplastic lesions in the mammary gland in Wistar rats. Environ Health Perspect 2007, 115:80-86.
8. Welshons W.V., Nagel S.C., vomSaal F.S. Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 2006, 147:56-69.
9. Sun Y., Irie M., Kishikawa N., Wada M., Kuroda N., Nakashima K. Determination of bisphenol A in human breast milk by HPLC with column-switching and fluorescence detection. Biomed Chromatogr 2004, 18:501-507.
10. Kuruto-Niwa R., Tateoka Y., Usuki Y., Nozawa R. Measurement of bisphenol A concentrations in human colostrum. Chemosphere 2007, 66:1160-1164.
11. Ikezuki Y., Tsutsumi O., Takai Y., Kamei Y., Taketani Y. Determination of bisphenol A concentrations in human biological fluids reveals significant early prenatal exposure. Hum Reprod 2002, 17:2839-2841.
12. Yamada H., Furuta I., Kato E.H., Kataoka S., Usuki Y., Kobashi G., et al. Maternal serum and amniotic fluid bisphenol A concentrations in the early second trimester. Reprod Toxicol 2002, 16:735-739.
13. Engel S.M., Levy B., Liu Z., Kaplan D., Wolff M.S. Xenobiotic phenols in early pregnancy amniotic fluid. Reprod Toxicol 2006, 21:110-112.
14. Doerge D.R., Twaddle N.C., Vanlandingham M., Brown R.P., Fisher J.W. Distribution of bisphenol A into tissues of adult, neonatal, and fetal Sprague-Dawley rats. Toxicol Appl Pharmacol 2011, 255:261-270.
15. Doerge D.R., Vanlandingham M., Twaddle N.C., Delclos K.B. Lactational transfer of bisphenol A in Sprague-Dawley rats. Toxicol Lett 2010, 199:372-376.
16. Zalko D., Soto A.M., Dolo L., Dorio C., Rathahao E., Debrauwer L., et al. Biotransformations of bisphenol A in a mammalian model: answers and new questions raised by low-dose metabolic fate studies in pregnant CD1 mice. Environ Health Perspect 2003, 111:309-319.
17. Yoo S.D., Shin B.S., Lee B.M., Lee K.C., Han S.Y., Kim H.S., et al. Bioavailability and mammary excretion of bisphenol A in Sprague-Dawley rats. J Toxicol Environ Health 2001, 64:417-426.
18. Markey C.M., Michaelson C.L., Sonnenschein C., Soto A.M. Alkylphenols and bisphenol A as environmental estrogens. The Handbook of Environmental Chemistry 2001, 129-153. Springer-Verlag, Berlin/Heidelberg. M. Metzler (Ed.).
19. Colerangle J.B., Roy D. Profound effects of the weak environmental estrogen-like chemical bisphenol A on the growth of the mammary gland of Noble rats. J Steroid Biochem Mol Biol 1997, 60:153-160.
20. Steinmetz R., Brown N.G., Allen D.L., Bigsby R.M., Ben-Jonathan N. The environmental estrogen bisphenol A stimulates prolactin release in vitro and in vivo. Endocrinology 1997, 138:1780-1786.
21. Prins G.S., Ye S.H., Birch L., Ho S.M., Kannan K. Serum bisphenol A pharmacokinetics and prostate neoplastic responses following oral and subcutaneous exposures in neonatal Sprague-Dawley rats. Reprod Toxicol 2011, 31:1-9.
22. Tang W.Y., Morey L.M., Cheung Y.Y., Birch L., Prins G.S., Ho S.M. Neonatal Exposure to Estradiol/Bisphenol A alters promoter methylation and expression of Nsbp1 and Hpcal1 genes and transcriptional programs of Dnmt3a/b and Mbd2/4 in the rat prostate gland throughout life. Endocrinology 2012, 153:42-55.
23. Dave B., Eason R.R., Till S.R., Geng Y., Velarde M.C., Badger T.M., et al. The soy isoflavone genistein promotes apoptosis in mammary epithelial cells by inducing the tumor suppressor PTEN. Carcinogenesis 2005, 26:1793-1803.
24. Li Y., Ahmed F., Ali S., Philip P.A., Kucuk O., Sarkar F.H. Inactivation of nuclear factor kappaB by soy isoflavone genistein contributes to increased apoptosis induced by chemotherapeutic agents in human cancer cells. Cancer Res 2005, 65:6934-6942.
25. Aggarwal B.B., Ichikawa H. Molecular targets and anti-cancer potential of indole-3-carbinol and its derivatives. Cell Cycle 2005, 4:1201-1215.
26. Kim Y.S., Milner J.A. Targets for indole-3-carbinol in cancer prevention. J Nutr Biochem 2005, 16:65-73.
27. Weng J.R., Tsai C.H., Kulp S.K., Chen C.S. Indole-3-carbinol as a chemopreventive and anti-cancer agent. Cancer Lett 2008, 262:153-163.
28. Wu T.Y., Saw C.L., Khor T.O., Pung D., Boyanapalli S.S.S., Kong A.T. In vivo pharmacodynamics of indole-3-carbinol in the inhibition of prostate cancer in transgenic adenocarcinoma of mouse prostate (TRAMP) mice: involvement of Nrf2 and cell cycle/apoptosis signaling pathways. Mol Carcinog 2011, 51:761-770.
29. Cho H.J., Park S.Y., Kim E.J., Kim J.K., Park J.H. 3,3'-Diindolylmethane inhibits prostate cancer development in the transgenic adenocarcinoma mouse prostate model. Mol Carcinog 2011, 50:100-112.
30. Souli E., Machluf M., Morgenstern A., Sabo E., Yannai S. Indole-3-carbinol (I3C) exhibits inhibitory and preventive effects on prostate tumors in mice. Food Chem Toxicol 2008, 46:863-870.
31. Kassie F., Matise I., Negia M., Upadhhyaya P., Hecht S.S. Dose-dependent inhibition of tobacco smoke carcinogen-induced lung tumorigenesis in A/J mice by indole-3-carbinol. Cancer Prev Res 2008, 1:568-576.
32. Broadbent T.A., Broadbent H.S. The chemistry and pharmacology of indole-3-carbinol(indole-3-methanol) and 3-(methoximethyl)indole. Curr Med Chem 1998, 5:469-491.
33. Hecht S.S., Carmella S.G., Kenny P.M.J., Low S.H., Arakawa K., Yu M.C. Effects of cruciferous vegetable consumption on urinary metabolites of the tobacco-specific lung carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone in Singapore Chinese. Cancer Epidemiol Biomarkers Prev 2004, 13:997-1004.
34. Sundar S.N., Kerekatte V., Equinozio C.N., Doan V.B., Bjeldanes L.F., Firestone G.L. Indole-3-carbinol selectively uncouples expression and activity of estrogen receptor subtypes in human breast cancer cells. Mol Endocrinol 2006, 20:3070-3082.
35. Wang T.T., Milner M.J., Milner J.A., Kim Y.S. Estrogen receptor alpha as a target for indole-3-carbinol. J Nutr Biochem 2006, 17:659-664.
36. Reed G.A., Peterson K.S., Smith H.J., Gray J.C., Sullivan D.K., Mayo M.S., et al. A phase I study of indole-3-carbinol in women: tolerability and effects. Cancer Epidemiol Biomark Prev 2005, 14:1953-1960.
37. Yu Z., Mahadevan B., Löhr C.V., Fischer K.A., Louderback M.A., Krueger S.K., et al. Indole-3-carbinol in the maternal diet provides chemoprotection for the fetus against transplacental carcinogenesis by the polycyclic aromatic hydrocarbon dibenzo[a,l]pyrene. Carcinogenesis 2006, 27:2116-2123.
38. Marker P.C., Donjacour A.A., Dahiya R., Cunha G.R. Hormonal, cellular and molecular control of prostatic development. Developmental Biol 2003, 253:165-174.
39. Prins G.S., Birch L., Tang W.Y., Ho S.M. Developmental estrogen exposures predispose to prostate carcinogenesis with aging. Reprod Toxicol 2007, 23:374-382.
40. Vilamaior P.S.L., Taboga S.R., Carvalho H.F. Postnatal growth of the ventral prostate in Wistar rats: a stereological and morphometrical study. Anat Rec A Discov Mol Cell Evol Biol 2006, 288A:885-892.
41. Puchtler H., Waldrop F.S., Meloan S.N., Terry M.S., Conner H.M. Methacarn (Methanol-Carnoy) Fixation: Practical and Theoretical Considerations. Histochem Cell Biol 1970, 21:97-116.
42. Weibel E.R. Principles and methods for the morphometric study of the lung and other organs. Lab Invest 1963, 12:131-155.
43. Barker D.J. The developmental origins of adult disease. J Am Coll Nutr 2004, 23:88-95.
44. Fowden A.L., Forhead A.J. Endocrine mechanisms of intrauterine programming. Reproduction 2004, 127:15-26.
45. Ismail-Beigi F., Catalano P.M., Hanson R.W. Metabolic programming: fetal origins of obesity and metabolic syndrome in the adult. Am J Physiol Endocrinol Metab 2006, 291:439-440.
46. Keri R.A., Ho S.M., Hunt P.A., Knudsen K.E., Soto A.M., Prins G.S. An evaluation of evidence for the carcinogenic activity of bisphenol A. Reprod Toxicol 2007, 24:240-252.
47. Ho S.M., Tang W.Y., Belmonte de Frausto J., Prins G. Developmental exposure to estradiol and bisphenol A increases susceptibility to prostate carcinogenesis and epigenetically regulates phosphodiesterase type 4 variant 4. Cancer Res 2006, 66:5624-5632.
48. Della Seta D., Minder I., Belloni V., Aloisi A.M., Dessi-Fulgheri F., Farabollini F. Pubertal exposure to estrogenic chemicals affects behavior in juvenile and adult male rats. Horm Behav 2006, 50:301-307.
49. Gray L.E., Ostby J., Furr J., Price M., Veeramachaneni D.N.R., Parks L. Perinatal exposure to the phthalates DEHP, BBP, and DINP, but not DEP, DMP, or DOTP, alters sexual differentiation of the male rat. Toxicol Sci 2000, 58:350-365.
50. Scarano W.R., Toledo F.C., Guerra M.T., Campos S.G.P., Júnior L.A.J., Felisbino S.L., et al. Long-term effects of developmental exposure to di-n-butyl-phthalate (DBP) on rat prostate: proliferative and inflammatory disorders and a possible role of androgens. Toxicology 2009, 262:215-223.
51. Putz O., Schwartz C.B., LeBlanc G.A., Cooper R.L., Prins G.S. Neonatal low- and high-dose exposure to estradiol benzoate in the male rat: II Effects on male puberty and the reproductive tract. Biol Reprod 2001, 65:1506-1517.
52. Scarano W.R., Cordeiro R.S., Góes R.M., Carvalho H.F., Taboga S.R. Tissue remodeling in Guinea pig lateral prostate at different ages after estradiol treatment. Cell Biol Int 2005, 29:778-784.
53. Scarano W.R., Sousa D.E., Campos S.G., Corradi L.S., Vilamaior P.S.L., Taboga S.R. Oestrogen supplementation following castration promotes stromal remodelling and histopathological alterations in the Mongolian gerbil ventral prostate. Intern J Exp Pathol 2008, 89:25-37.
54. Tilley W.D., Horsfall D.J., Skinner J.M., Henderson D.W., Marshall V.R. Effect of pubertal development on estrogen receptor levels and stromal morphology in the Guinea pig prostate. Prostate 1989, 15:195-210.
55. Wilson M.J., Woodson M., Wiehr C., Reddy A., Sinha A.A. Matrix metalloproteinases in the pathogenesis of estradiol-induced nonbacterial prostatitis in the lateral prostate lobe of the Wistar rat. Exp Mol Pathol 2004, 77:7-17.
56. DeMarzo A.M., Marchi V.L., Epstein J.I., Nelson W.G. Proliferative inflammatory atrophy of the prostate implications for prostatic carcinogenesis. Am J Pathol 1999, 155:1985-1992.
57. Bernoulli J., Yatkin E., Laakso A., Anttinen M., Bosland M., Vega K., et al. Histopathological evidence for an association of inflammation with ductal pin-like lesions but not with ductal adenocarcinoma in the prostate of the Noble rat. Prostate 2008, 68:728-739.
58. Reznik G., Hamlim M.H., Ward J.M., Stinson S.F. Prostatic hyperplasia and neoplasia in aging F344 rats. Prostate 1981, 2:261-268.
59. Prins G.S. Differential regulation of androgen receptors in the separate rat prostate lobes: androgen independent expression in the lateral lobe. J Steroid Biochem 1989, 33:319-326.
60. Banerjee P.P., Banerjee S., Lay J.M., Strandberg J.D., Zirkin B.R. Age-dependent and lobe-specific spontaneous hyperplasia in the brown Norway rat prostate. Biol Reprod 1998, 59:1163-1170.
61. Vilamaior P.S.L., Felisbino S.L., Taboga S.R., Carvalho H.F. Collagen fiber reorganization in the rat ventral prostate following androgen deprivation: a possible role for smooth muscle cells. Prostate 2000, 45:253-258.
62. Shappell S.B., Thomas G.V., Roberts R.L., Herbert R., Ittmann M.M., Rubin M.A., et al. Prostate pathology of genetically engineered mice: definitions and classification. The consensus report from the Bar Harbor Meeting of the mouse models of human cancer consortium prostate pathology committee. Cancer Res 2004, 64:2270-2305.
63. Bosland M.C. Use of animal models in defining efficacy of chemoprevention agents against prostate cancer. Eur Urol 1999, 35:459-463.
64. Lucia M.S., Bostwick D.G., Bosland M., Cockett A.T., Knapp D.W., Leav I., et al. Workgroup I: rodent models of prostate cancer. Prostate 1998, 36:49-55.
65. Ellem S.J., Risbridger G.P. The dual, opposing roles of estrogen in the prostate. Ann N Y Acad Sci 2009, 1155:174-186.
66. Li Y., Li X., Sarkar F.H. Gene expression profiles of I3C- and DIM-treated PC3 human prostate cancer cells determined by cDNA microarray analysis. J Nutr 2003, 133:1011-1019.
67. Nagel S.C., vom Saal F.S., Thayer K.A., Dhar M.G., Boechler M., Welshons W.V. Relative binding affinity-serum modified access (RBA-SMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol. Environ Health Perspect 1997, 105:70-76.
68. Gupta C. Reproductive malformation of the male offspring following maternal exposure to estrogenic chemicals. Proc Soc Exp Biol Med 2000, 224:61-68.
69. García-Cao I., Duran A., Collado M., Carrascosa M.J., Martín-Caballero J., Flores J.M., et al. Tumour-suppression activity of the proapoptotic regulator Par4. EMBO Rep 2005, 6:577-583.
70. Higdon J.V., Delage B., Williams D.E., Dashwood R.H. Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol Res 2007, 55:224-236.
71. Sarkar F.H., Li Y. Indole-3-carbinol and prostate cancer. J Nutr 2004, 134:3493S-3498S.