Identification of novel low-dose bisphenol A targets in human foreskin fibroblast cells derived from hypospadias patients

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Qin, Xian Yang ^a,b   Kojima, Yoshiyuki ^c   Mizuno, Kentaro ^c   Ueoka, Katsuhiko ^d   Muroya, Koji ^e   Miyado, Mami ^f   Zaha, Hiroko ^a   Akanuma, Hiromi ^a   Zeng, Qin ^a   Fukuda, Tomokazu ^g   Yoshinaga, Jun ^b   Yonemoto, Junzo ^a   Kohri, Kenjiro ^c   Hayashi, Yutaro ^c   Fukami, Maki ^f   Ogata, Tsutomu ^f,h   Sone, Hideko ^a  

^a NATIONAL INSTITUTE FOR ENVIRONMENTAL STUDIES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NAGOYA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICAL SCIENCES   (Japan)

^d National Center for Child Health and Development   (Japan)

^e KANAGAWA CHILDREN'S MEDICAL CENTER   (Japan)

^f NATIONAL RESEARCH INSTITUTE FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^g TOHOKU UNIVERSITY   (Japan)

^h HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 4,4' ISOPROPYLIDENEDIPHENOL; ESTRADIOL; STROMELYSIN 3; AROMATIC HYDROCARBON RECEPTOR; ESTROGEN RECEPTOR; PHENOL DERIVATIVE; TRANSCRIPTOME;

ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CRYPTORCHISM; DRUG EXPOSURE; ENZYME INHIBITION; FIBROBLAST; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC SCREENING; GENETIC VARIABILITY; HUMAN; HUMAN CELL; HYPOSPADIAS; MOLECULAR PATHOLOGY; NUCLEOTIDE SEQUENCE; PREPUCE; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTIVE HEALTH; DOSE RESPONSE; DRUG EFFECT; GENETICS; GENOMICS; MALE; METABOLISM; PATHOLOGY; POLLUTANT; PRESCHOOL CHILD; REPRODUCIBILITY; REPRODUCTION; SIGNAL TRANSDUCTION;

CHILD, PRESCHOOL; DOSE-RESPONSE RELATIONSHIP, DRUG; ENVIRONMENTAL POLLUTANTS; ESTRADIOL; FIBROBLASTS; FORESKIN; GENOMICS; HUMANS; HYPOSPADIAS; MALE; MATRIX METALLOPROTEINASE 11; PHENOLS; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, ESTROGEN; REPRODUCIBILITY OF RESULTS; REPRODUCTION; SIGNAL TRANSDUCTION; TETRACHLORODIBENZODIOXIN; TRANSCRIPTOME;

EID: 84860534831     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036711     Document Type: Article

References (44)

1. Toppari J, Virtanen HE, Main KM, Skakkebaek NE, (2010) Cryptorchidism and hypospadias as a sign of testicular dysgenesis syndrome (TDS): environmental connection. Birth Defects Res A Clin Mol Teratol 88: 910-919.
2. Skakkebaek NE, Rajpert-De Meyts E, Main KM, (2001) Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 16: 972-978.
3. Jorgensen N, Meyts ER, Main KM, Skakkebaek NE, (2010) Testicular dysgenesis syndrome comprises some but not all cases of hypospadias and impaired spermatogenesis. Int J Androl 33: 298-303.
4. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV, (2007) Human exposure to bisphenol A (BPA). Reprod Toxicol 24: 139-177.
5. Krishnan AV, Stathis P, Permuth SF, Tokes L, Feldman D, (1993) Bisphenol-A: an estrogenic substance is released from polycarbonate flasks during autoclaving. Endocrinology 132: 2279-2286.
6. Calafat AM, Kuklenyik Z, Reidy JA, Caudill SP, Ekong J, et al. (2005) Urinary concentrations of bisphenol A and 4-nonylphenol in a human reference population. Environ Health Perspect 113: 391-395.
7. Wetherill YB, Akingbemi BT, Kanno J, McLachlan JA, Nadal A, et al. (2007) In vitro molecular mechanisms of bisphenol A action. Reprod Toxicol 24: 178-198.
8. Allard P, Colaiacovo MP, (2010) Bisphenol A impairs the double-strand break repair machinery in the germline and causes chromosome abnormalities. Proc Natl Acad Sci U S A 107: 20405-20410.
9. Leranth C, Hajszan T, Szigeti-Buck K, Bober J, MacLusky NJ, (2008) Bisphenol A prevents the synaptogenic response to estradiol in hippocampus and prefrontal cortex of ovariectomized nonhuman primates. Proc Natl Acad Sci U S A 105: 14187-14191.
10. Lang IA, Galloway TS, Scarlett A, Henley WE, Depledge M, et al. (2008) Association of urinary bisphenol A concentration with medical disorders and laboratory abnormalities in adults. JAMA 300: 1303-1310.
11. Wei J, Lin Y, Li Y, Ying C, Chen J, et al. (2011) Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology 152: 3049-3061.
12. Qin XY, Fukuda T, Yang L, Zaha H, Akanuma H, et al. (2012) Effects of bisphenol A exposure on the proliferation and senescence of normal human mammary epithelial cells. Cancer Biol Ther 13.
13. Sharpe RM, (2010) Is it time to end concerns over the estrogenic effects of bisphenol A? Toxicol Sci 114: 1-4.
14. Welshons WV, Nagel SC, vom Saal FS, (2006) Large effects from small exposures. III. Endocrine mechanisms mediating effects of bisphenol A at levels of human exposure. Endocrinology 147: S56-69.
15. Li D, Zhou Z, Qing D, He Y, Wu T, et al. (2010) Occupational exposure to bisphenol-A (BPA) and the risk of self-reported male sexual dysfunction. Hum Reprod 25: 519-527.
16. Jasarevic E, Sieli PT, Twellman EE, Welsh TH Jr, Schachtman TR, et al. (2011) Disruption of adult expression of sexually selected traits by developmental exposure to bisphenol A. Proc Natl Acad Sci U S A 108: 11715-11720.
17. Zhang X, Chang H, Wiseman S, He Y, Higley E, et al. (2011) Bisphenol A disrupts steroidogenesis in human H295R cells. Toxicol Sci 121: 320-327.
18. Calvano SE, Xiao W, Richards DR, Felciano RM, Baker HV, et al. (2005) A network-based analysis of systemic inflammation in humans. Nature 437: 1032-1037.
19. Bronner IF, Bochdanovits Z, Rizzu P, Kamphorst W, Ravid R, et al. (2009) Comprehensive mRNA expression profiling distinguishes tauopathies and identifies shared molecular pathways. PLoS One 4: e6826.
20. Qiao L, Tasian GE, Zhang H, Cunha GR, Baskin L, (2011) ZEB1 is estrogen responsive in vitro in human foreskin cells and is over expressed in penile skin in patients with severe hypospadias. J Urol 185: 1888-1893.
21. Vottero A, Minari R, Viani I, Tassi F, Bonatti F, et al. (2011) Evidence for epigenetic abnormalities of the androgen receptor gene in foreskin from children with hypospadias. J Clin Endocrinol Metab 96: E1953-1962.
22. Wang Z, Liu BC, Lin GT, Lin CS, Lue TF, et al. (2007) Up-regulation of estrogen responsive genes in hypospadias: microarray analysis. J Urol 177: 1939-1946.
23. Qin XY, Zaha H, Nagano R, Yoshinaga J, Yonemoto J, et al. (2011) Xenoestrogens down-regulate aryl-hydrocarbon receptor nuclear translocator 2 mRNA expression in human breast cancer cells via an estrogen receptor alpha-dependent mechanism. Toxicol Lett 206: 152-157.
24. Singleton DW, Feng Y, Yang J, Puga A, Lee AV, et al. (2006) Gene expression profiling reveals novel regulation by bisphenol-A in estrogen receptor-alpha-positive human cells. Environ Res 100: 86-92.
25. Gibert Y, Sassi-Messai S, Fini JB, Bernard L, Zalko D, et al. (2011) Bisphenol A induces otolith malformations during vertebrate embryogenesis. BMC Dev Biol 11: 4.
26. Laity JH, Lee BM, Wright PE, (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr Opin Struct Biol 11: 39-46.
27. Lupo A, Cesaro E, Montano G, Izzo P, Costanzo P, (2011) ZNF224: Structure and role of a multifunctional KRAB-ZFP protein. Int J Biochem Cell Biol 43: 470-473.
28. Harada Y, Kanehira M, Fujisawa Y, Takata R, Shuin T, et al. (2010) Cell-permeable peptide DEPDC1-ZNF224 interferes with transcriptional repression and oncogenicity in bladder cancer cells. Cancer Res 70: 5829-5839.
29. Garavelli L, Cerruti-Mainardi P, Virdis R, Pedori S, Pastore G, et al. (2005) Genitourinary anomalies in Mowat-Wilson syndrome with deletion/mutation in the zinc finger homeo box 1B gene (ZFHX1B). Report of three Italian cases with hypospadias and review. Horm Res 63: 187-192.
30. Peruzzi D, Mori F, Conforti A, Lazzaro D, De Rinaldis E, et al. (2009) MMP11: a novel target antigen for cancer immunotherapy. Clin Cancer Res 15: 4104-4113.
31. Vu TH, Werb Z, (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev 14: 2123-2133.
32. Valdivia A, Peralta R, Matute-Gonzalez M, Garcia Cebada JM, Casasola I, et al. (2011) Co-expression of metalloproteinases 11 and 12 in cervical scrapes cells from cervical precursor lesions. Int J Clin Exp Pathol 4: 674-682.
33. McCord LA, Li F, Rosewell KL, Brannstrom M, Curry TE Jr, (2011) Ovarian Expression and Regulation of the Stromelysins During the Periovulatory Period in the Human and the Rat. Biol Reprod.
34. Desmedt C, Majjaj S, Kheddoumi N, Singhal SK, Haibe-Kains B, et al. (2012) Characterization and Clinical Evaluation of CD10+ Stroma Cells in the Breast Cancer Microenvironment. Clin Cancer Res 18: 1004-1014.
35. Roy R, Yang J, Moses MA, (2009) Matrix metalloproteinases as novel biomarkers and potential therapeutic targets in human cancer. J Clin Oncol 27: 5287-5297.
36. Wei L, Shi YB, (2005) Matrix metalloproteinase stromelysin-3 in development and pathogenesis. Histol Histopathol 20: 177-185.
37. Ishizuya-Oka A, Li Q, Amano T, Damjanovski S, Ueda S, et al. (2000) Requirement for matrix metalloproteinase stromelysin-3 in cell migration and apoptosis during tissue remodeling in Xenopus laevis. J Cell Biol 150: 1177-1188.
38. Simian M, Hirai Y, Navre M, Werb Z, Lochter A, et al. (2001) The interplay of matrix metalloproteinases, morphogens and growth factors is necessary for branching of mammary epithelial cells. Development 128: 3117-3131.
39. Knorr E, Schmidtberg H, Vilcinskas A, Altincicek B, (2009) MMPs regulate both development and immunity in the tribolium model insect. PLoS One 4: e4751.
40. Baskin LS, Erol A, Jegatheesan P, Li Y, Liu W, et al. (2001) Urethral seam formation and hypospadias. Cell Tissue Res 305: 379-387.
41. Virtanen HE, Bjerknes R, Cortes D, Jorgensen N, Rajpert-De Meyts E, et al. (2007) Cryptorchidism: classification, prevalence and long-term consequences. Acta Paediatr 96: 611-616.
42. Kojima Y, Mizuno K, Kohri K, Hayashi Y, (2009) Advances in molecular genetics of cryptorchidism. Urology 74: 571-578.
43. Kojima Y, Kohri K, Hayashi Y, (2010) Genetic pathway of external genitalia formation and molecular etiology of hypospadias. J Pediatr Urol 6: 346-354.
44. Rey RA, Codner E, Iniguez G, Bedecarras P, Trigo R, et al. (2005) Low risk of impaired testicular Sertoli and Leydig cell functions in boys with isolated hypospadias. J Clin Endocrinol Metab 90: 6035-6040.