Exposure of human fetal penile cells to different PCB mixtures: Transcriptome analysis points to diverse modes of interference on external genitalia programming

Reproductive Toxicology

Volumn 32, Issue 1, 2011, Pages 1-14

  Tait, Sabrina ^a   La Rocca, Cinzia ^a   Mantovani, Alberto ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Contaminants; Endocrine disrupters; Genitourinary development; Malformations; Reproductive system; Toxicogenomics

Indexed keywords

POLYCHLORINATED BIPHENYL;

ARTICLE; CELL GROWTH; CELL METABOLISM; FETUS; FETUS CELL; GENE EXPRESSION PROFILING; GENE FUNCTION; GENETIC REGULATION; GENITOURINARY DEVELOPMENT; HUMAN; HUMAN CELL; MALE; MORPHOGENESIS; NUCLEOTIDE SEQUENCE; ORGANOGENESIS; PENIS; PRENATAL EXPOSURE; SMOOTH MUSCLE; TOXICOGENETICS; TRANSCRIPTOMICS; UROGENITAL SYSTEM;

CELL SURVIVAL; CELLS, CULTURED; ENVIRONMENTAL POLLUTANTS; FETAL DEVELOPMENT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENITALIA, MALE; GESTATIONAL AGE; HUMANS; MALE; MYOCYTES, SMOOTH MUSCLE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PENIS; POLYCHLORINATED BIPHENYLS;

EID: 79960466934     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2011.02.001     Document Type: Article

References (67)

1. Skakkebaek N.E., Rajpert-De Meyts E., Main K.M. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum Reprod 2001, 16(May (5)):972-978.
2. Fisher J.S., Macpherson S., Marchetti N., Sharpe R.M. Human 'testicular dysgenesis syndrome': a possible model using in-utero exposure of the rat to dibutyl phthalate. Hum Reprod 2003, 18(July (7)):1383-1394.
3. Ebert A.K., Reutter H., Ludwig M., Rosch W.H. The exstrophy-epispadias complex. Orphanet J Rare Dis 2009, 4(October):23.
4. Foster P.M., Harris M.W. Changes in androgen-mediated reproductive development in male rat offspring following exposure to a single oral dose of flutamide at different gestational ages. Toxicol Sci 2005, 85(June (2)):1024-1032.
5. Wohlfahrt-Veje C., Main K.M., Skakkebaek N.E. Testicular dysgenesis syndrome: foetal origin of adult reproductive problems. Clin Endocrinol (Oxf) 2009, 71(October (4)):459-465.
6. Kojima Y., Kohri K., Hayashi Y. Genetic pathway of external genitalia formation and molecular etiology of hypospadias. J Pediatr Urol 2010, 6(August (4)):346-354.
7. Haraguchi R., Motoyama J., Sasaki H., Satoh Y., Miyagawa S., Nakagata N., et al. Molecular analysis of coordinated bladder and urogenital organ formation by Hedgehog signaling. Development 2007, 134(February (3)):525-533.
8. Yamada G., Suzuki K., Haraguchi R., Miyagawa S., Satoh Y., Kamimura M., et al. Molecular genetic cascades for external genitalia formation: an emerging organogenesis program. Dev Dyn 2006, 235(July (7)):1738-1752.
9. Wang Z., Liu B.C., Lin G.T., Lin C.S., Lue T.F., Willingham E., et al. Up-regulation of estrogen responsive genes in hypospadias: microarray analysis. J Urol 2007, 177(May (5)):1939-1946.
10. Draaken M., Proske J., Schramm C., Wittler L., Bartels E., Nothen M.M., et al. Embryonic expression of the cysteine rich protein 61 (CYR61) gene: a candidate for the development of human epispadias. Birth Defects Res A Clin Mol Teratol 2010, 88(July (7)):546-550.
11. European Food Safety Authority Results of the monitoring of dioxin levels in food and feed. EFSA J 2010, 8(3):1385.
12. European Food Safety Authority Results of the monitoring of non dioxin-like PCBs in food and feed. EFSA J 2010, 8(7):1701.
13. Meijer L., Weiss J., Van Velzen M., Brouwer A., Bergman A., Sauer P.J. Serum concentrations of neutral and phenolic organohalogens in pregnant women and some of their infants in The Netherlands. Environ Sci Technol 2008, 42(May (9)):3428-3433.
14. Brucker-Davis F., Wagner-Mahler K., Delattre I., Ducot B., Ferrari P., Bongain A., et al. Cryptorchidism at birth in Nice area (France) is associated with higher prenatal exposure to PCBs and DDE, as assessed by colostrum concentrations. Hum Reprod 2008, 23(August (8)):1708-1718.
15. Hosie S., Loff S., Witt K., Niessen K., Waag K.L. Is there a correlation between organochlorine compounds and undescended testes?. Eur J Pediatr Surg 2000, 10(October (5)):304-309.
16. McGlynn K.A., Guo X., Graubard B.I., Brock J.W., Klebanoff M.A., Longnecker M.P. Maternal pregnancy levels of polychlorinated biphenyls and risk of hypospadias and cryptorchidism in male offspring. Environ Health Perspect 2009, 117(September (9)):1472-1476.
17. Hardell L., van Bavel B., Lindstrom G., Carlberg M., Dreifaldt A.C., Wijkstrom H., et al. Increased concentrations of polychlorinated biphenyls, hexachlorobenzene, and chlordanes in mothers of men with testicular cancer. Environ Health Perspect 2003, 111(June (7)):930-934.
18. Hardell L., Van Bavel B., Lindstrom G., Carlberg M., Eriksson M., Dreifaldt A.C., et al. Concentrations of polychlorinated biphenyls in blood and the risk for testicular cancer. Int J Androl 2004, 27(October (5)):282-290.
19. Toppari J., Larsen J.C., Christiansen P., Giwercman A., Grandjean P., Guillette L.J., et al. Male reproductive health and environmental xenoestrogens. Environ Health Perspect 1996, 104(August (Suppl. 4)):741-803.
20. Letcher R.J., Lemmen J.G., van der Burg B., Brouwer A., Bergman A., Giesy J.P., et al. In vitro antiestrogenic effects of aryl methyl sulfone metabolites of polychlorinated biphenyls and 2,2-bis(4-chlorophenyl)-1,1-dichloroethene on 17beta-estradiol-induced gene expression in several bioassay systems. Toxicol Sci 2002, 69(October (2)):362-372.
21. Pliskova M., Vondracek J., Canton R.F., Nera J., Kocan A., Petrik J., et al. Impact of polychlorinated biphenyls contamination on estrogenic activity in human male serum. Environ Health Perspect 2005, 113(October (10)):1277-1284.
22. Negri E., Bosetti C., Fattore E., La Vecchia C. Environmental exposure to polychlorinated biphenyls (PCBs) and breast cancer: a systematic review of the epidemiological evidence. Eur J Cancer Prev 2003, 12(December (6)):509-516.
23. Wolff M.S., Camann D., Gammon M., Stellman S.D. Proposed PCB congener groupings for epidemiological studies. Environ Health Perspect 1997, 105(January (1)):13-14.
24. La Rocca C., Alivernini S., Badiali M., Cornoldi A., Iacovella N., Silvestroni L., et al. TEQ(S) and body burden for PCDDs, PCDFs, and dioxin-like PCBs in human adipose tissue. Chemosphere 2008, 73(August (1)):92-96.
25. Turrio Baldassarri L., La Rocca C., Alivernini S., Iacovella N., Badiali M., Spera G., et al. Levels and profiles of organohalogen compounds (PCDDs, PCDFs, PCBs, DDE, DDT, DDD, HCB) in adipose tissues of Italian obese patients. Organohalogen Compd 2002, 58:253-256.
26. Brokken L.J., Adamsson A., Paranko J., Toppari J. Antiandrogen exposure in utero disrupts expression of desert hedgehog and insulin-like factor 3 in the developing fetal rat testis. Endocrinology 2009, 150(January (1)):445-451.
27. Adamsson A., Simanainen U., Viluksela M., Paranko J., Toppari J. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on foetal male rat steroidogenesis. Int J Androl 2009, 32(October (5)):575-585.
28. Murugesan P., Muthusamy T., Balasubramanian K., Arunakaran J. Polychlorinated biphenyl (Aroclor 1254) inhibits testosterone biosynthesis and antioxidant enzymes in cultured rat Leydig cells. Reprod Toxicol 2008, 25(August (4)):447-454.
29. Hipp J., Andersson K.E., Kwon T.G., Kwak E.K., Yoo J., Atala A. Microarray analysis of exstrophic human bladder smooth muscle. BJU Int 2008, 101(January (1)):100-105.
30. Goyal H.O., Braden T.D., Williams C.S., Williams J.W. Role of estrogen in induction of penile dysmorphogenesis: a review. Reproduction 2007, 134(August (2)):199-208.
31. Huang Y., Pan L., Xia X., Feng Y., Jiang C., Cui Y. Long-term effects of phytoestrogen daidzein on penile cavernosal structures in adult rats. Urology 2008, 72(July (1)):220-224.
32. Bond C., Tang Y., Podlasek C.A. Neural influences on sonic hedgehog and apoptosis in the rat penis. Biol Reprod 2008, 78(May (5)):947-956.
33. Wang M.H., Baskin L.S. Endocrine disruptors, genital development, and hypospadias. J Androl 2008, 29(September-October (5)):499-505.
34. Crescioli C., Maggi M., Vannelli G.B., Ferruzzi P., Granchi S., Mancina R., et al. Expression of functional estrogen receptors in human fetal male external genitalia. J Clin Endocrinol Metab 2003, 88(April (4)):1815-1824.
35. Liu K., Lehmann K.P., Sar M., Young S.S., Gaido K.W. Gene expression profiling following in utero exposure to phthalate esters reveals new gene targets in the etiology of testicular dysgenesis. Biol Reprod 2005, 73(July (1)):180-192.
36. Vo T.T., Jung E.M., Dang V.H., Yoo Y.M., Choi K.C., Yu F.H., et al. Di-(2 ethylhexyl) phthalate and flutamide alter gene expression in the testis of immature male rats. Reprod Biol Endocrinol 2009, 7(September):104.
37. Eustache F., Mondon F., Canivenc-Lavier M.C., Lesaffre C., Fulla Y., Berges R., et al. Chronic dietary exposure to a low-dose mixture of genistein and vinclozolin modifies the reproductive axis, testis transcriptome, and fertility. Environ Health Perspect 2009, 117(August (8)):1272-1279.
38. National Institutes of Health. Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). NIH Publicaton; 2002, 02-5215:2002.
39. Smyth G.K. Limma: linear models for microarray data. Bioinformatics and computational biology solutions using R and bioconductor 2005, Springer, New York, p. 397-398-420. R. Gentleman, V. Carey, S. Dudoit, R. Irizarry, W. Huber (Eds.).
40. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5(10):R80.
41. R Development Core Team R: a language and environment for statistical computing 2009, R Foundation for Statistical Computing, Vienna, Austria.
42. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B 1995, 57:289-300.
43. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003, 4(5):P3.
44. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M., et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25(May (1)):25-29.
45. Thomas P.D., Campbell M.J., Kejariwal A., Mi H., Karlak B., Daverman R., et al. PANTHER: a library of protein families and subfamilies indexed by function. Genome Res 2003, 13(September (9)):2129-2141.
46. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 2001, 29(May (9)):e45.
47. Han J., Lee Y., Yeom K.H., Nam J.W., Heo I., Rhee J.K., et al. Molecular basis for the recognition of primary microRNAs by the Drosha-DGCR8 complex. Cell 2006, 125(June (5)):887-901.
48. Takenawa T., Miki H. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 2001, 114(May (Pt 10)):1801-1809.
49. Yan C., Martinez-Quiles N., Eden S., Shibata T., Takeshima F., Shinkura R., et al. WAVE2 deficiency reveals distinct roles in embryogenesis and Rac-mediated actin-based motility. EMBO J 2003, 22(July (14)):3602-3612.
50. Valcourt U., Kowanetz M., Niimi H., Heldin C.H., Moustakas A. TGF-beta and the Smad signaling pathway support transcriptomic reprogramming during epithelial-mesenchymal cell transition. Mol Biol Cell 2005, 16(April (4)):1987-2002.
51. Andersson K.E. Erectile physiological and pathophysiological pathways involved in erectile dysfunction. J Urol 2003, 170(August (2 Pt 2)):S6,13. discussion S13-4.
52. Douglas S.A., Ohlstein E.H. Signal transduction mechanisms mediating the vascular actions of endothelin. J Vasc Res 1997, 34(May-June (3)):152-164.
53. Deacon K., Knox A.J. Endothelin-1 (ET-1) increases the expression of remodeling genes in vascular smooth muscle through linked calcium and cAMP pathways: role of a phospholipase A(2)(cPLA(2))/cyclooxygenase-2 (COX-2)/prostacyclin receptor-dependent autocrine loop. J Biol Chem 2010, 285(August (34)):25913-25927.
54. Wang J., Gebre A.K., Anderson R.A., Parks J.S. Amino acid residue 149 of lecithin:cholesterol acyltransferase determines phospholipase A2 and transacylase fatty acyl specificity. J Biol Chem 1997, 272(January (1)):280-286.
55. Bae J., Mousa M.A., Quensen J.F., Boyd S.A., Loch-Caruso R. Stimulation of contraction of pregnant rat uterus in vitro by non-dechlorinated and microbially dechlorinated mixtures of polychlorinated biphenyls. Environ Health Perspect 2001, 109(March (3)):275-282.
56. Tsai M.L., Webb R.C., Loch-Caruso R. Congener-specific effects of PCBs on contractions of pregnant rat uteri. Reprod Toxicol 1996, 10(January-February (1)):21-28.
57. Brant K., Caruso R.L. Late-gestation rat myometrial cells express multiple isoforms of phospholipase A2 that mediate PCB 50-induced release of arachidonic acid with coincident prostaglandin production. Toxicol Sci 2005, 88(November (1)):222-230.
58. Kasahara K., Sanai Y. Functional roles of glycosphingolipids in signal transduction via lipid rafts. Glycoconj J 2000, 17(March-April (3-4)):153-162.
59. Connelly M.A., Williams D.L. SR-BI and HDL cholesteryl ester metabolism. Endocr Res 2004, 30(November (4)):697-703.
60. Franchimont P. Regulation of gonadal androgen secretion. Horm Res 1983, 18(1-3):7-17.
61. Grover A., Smith C.E., Gregory M., Cyr D.G., Sairam M.R., Hermo L. Effects of FSH receptor deletion on epididymal tubules and sperm morphology, numbers, and motility. Mol Reprod Dev 2005, 72(October (2)):135-144.
62. Ma X., Dong Y., Matzuk M.M., Kumar T.R. Targeted disruption of luteinizing hormone beta-subunit leads to hypogonadism, defects in gonadal steroidogenesis, and infertility. Proc Natl Acad Sci USA 2004, 101(December (49)):17294-17299.
63. Lin S.X., Shi R., Qiu W., Azzi A., Zhu D.W., Dabbagh H.A., et al. Structural basis of the multispecificity demonstrated by 17beta-hydroxysteroid dehydrogenase types 1 and 5. Mol Cell Endocrinol 2006, 248(March (1-2)):38-46.
64. Oishi I., Suzuki H., Onishi N., Takada R., Kani S., Ohkawara B., et al. The receptor tyrosine kinase Ror2 is involved in non-canonical Wnt5a/JNK signalling pathway. Genes Cells 2003, 8(July (7)):645-654.
65. Draaken M., Reutter H., Schramm C., Bartels E., Boemers T.M., Ebert A.K., et al. Microduplications at 22q11.21 are associated with non-syndromic classic bladder exstrophy. Eur J Med Genet 2010, 53(March-April (2)):55-60.
66. Yeom K.H., Lee Y., Han J., Suh M.R., Kim V.N. Characterization of DGCR8/Pasha, the essential cofactor for Drosha in primary miRNA processing. Nucleic Acids Res 2006, 34(16):4622-4629.
67. Li Y., Millikan R.C., Bell D.A., Cui L., Tse C.K., Newman B., et al. Polychlorinated biphenyls, cytochrome P450 1A1 (CYP1A1) polymorphisms, and breast cancer risk among African American women and white women in North Carolina: a population-based case-control study. Breast Cancer Res 2005, 7(1):R12-R18.