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Cancer Causes & Control

, Volume 25, Issue 7, pp 869–879 | Cite as

Gene–environment interactions between JAZF1 and occupational and household lead exposure in prostate cancer among African American men

  • Christine Neslund-DudasEmail author
  • Albert M. Levin
  • Jennifer L. Beebe-Dimmer
  • Cathryn H. Bock
  • Nora L. Nock
  • Andrew Rundle
  • Michelle Jankowski
  • Richard Krajenta
  • Q. Ping Dou
  • Bharati Mitra
  • Deliang Tang
  • Timothy R. Rebbeck
  • Benjamin A. Rybicki
Original paper

Abstract

Purpose

A single nucleotide polymorphism, rs10486567, in JAZF1 has consistently been associated with increased risk of prostate cancer. The physical interaction of zinc finger proteins, such as JAZF1, with heavy metals may play a role in carcinogenesis. This study assessed potential gene–environment statistical interactions (G×E) between rs10486567 and heavy metals in prostate cancer.

Methods

In a case-only study of 228 African American prostate cancer cases, G×E between rs10486567 and sources of cadmium and lead (Pb) were assessed. Unconditional logistic regression was used to estimate interaction odds ratios (IORs), and generalized estimating equations were used for models containing nested data. Case–control validation of IORs was performed, using 82 controls frequency matched to cases on age–race.

Results

Among cases, a potential G×E interaction was observed between rs10486567 CC genotype and living in a Census tract with a high proportion of housing built before 1950, a proxy for household Pb exposure, when compared to CT or TT carriers (OR 1.81; 95 % CI 1.04–3.16; p = 0.036). A stronger G×E interaction was observed when both housing and occupational Pb exposure were taken into account (OR 2.62; 95 % CI 1.03–6.68; p = 0.04). Case–control stratified analyses showed the odds of being a CC carrier were higher in cases compared to controls among men living in areas with older housing (OR 2.03; CI 0.99–4.19; p = 0.05) or having high occupational Pb exposure (OR 2.50; CI 1.01–6.18; p = 0.05).

Conclusions

In African American men, the association between JAZF1 rs10486567 and prostate cancer may be modified by exposure to heavy metals such as Pb.

Keywords

Prostate cancer JAZF1 Lead Cadmium Housing Smoking African American 

Notes

Acknowledgments

NIEHS 5R01 ES011126, CDMRP W81XWH-07-1-0252, and CDMRP W81XWH-06-1-0181.

Conflict of interest

None.

References

  1. 1.
    American Cancer S (2012) Cancer facts and figures for African Americans 2011–2012. American Cancer Society, AtlantaGoogle Scholar
  2. 2.
    Eeles RA, Kote-Jarai Z, Giles GG, Olama AA, Guy M, Jugurnauth SK, Mulholland S, Leongamornlert DA, Edwards SM, Morrison J, Field HI, Southey MC, Severi G, Donovan JL, Hamdy FC, Dearnaley DP, Muir KR, Smith C, Bagnato M, Ardern-Jones AT, Hall AL, O’Brien LT, Gehr-Swain BN, Wilkinson RA, Cox A, Lewis S, Brown PM, Jhavar SG, Tymrakiewicz M, Lophatananon A, Bryant SL, Horwich A, Huddart RA, Khoo VS, Parker CC, Woodhouse CJ, Thompson A, Christmas T, Ogden C, Fisher C, Jamieson C, Cooper CS, English DR, Hopper JL, Neal DE, Easton DF (2008) Multiple newly identified loci associated with prostate cancer susceptibility. Nat Genet 40(3):316–321PubMedCrossRefGoogle Scholar
  3. 3.
    Haiman CA, Chen GK, Blot WJ, Strom SS, Berndt SI, Kittles RA, Rybicki BA, Isaacs WB, Ingles SA, Stanford JL, Diver WR, Witte JS, Hsing AW, Nemesure B, Rebbeck TR, Cooney KA, Xu J, Kibel AS, Hu JJ, John EM, Gueye SM, Watya S, Signorello LB, Hayes RB, Wang Z, Yeboah E, Tettey Y, Cai Q, Kolb S, Ostrander EA, Zeigler-Johnson C, Yamamura Y, Neslund-Dudas C, Haslag-Minoff J, Wu W, Thomas V, Allen GO, Murphy A, Chang BL, Zheng SL, Leske MC, Wu SY, Ray AM, Hennis AJ, Thun MJ, Carpten J, Casey G, Carter EN, Duarte ER, Xia LY, Sheng X, Wan P, Pooler LC, Cheng I, Monroe KR, Schumacher F, Le ML, Kolonel LN, Chanock SJ, Berg DV, Stram DO, Henderson BE (2011) Genome-wide association study of prostate cancer in men of African ancestry identifies a susceptibility locus at 17q21. Nat Genet 43(6):570–573PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Waters KM, Le ML, Kolonel LN, Monroe KR, Stram DO, Henderson BE, Haiman CA (2009) Generalizability of associations from prostate cancer genome-wide association studies in multiple populations. Cancer Epidemiol Biomarkers Prev 18(4):1285–1289PubMedCentralPubMedCrossRefGoogle Scholar
  5. 5.
    Liu H, Wang B, Han C (2011) Meta-analysis of genome-wide and replication association studies on prostate cancer. Prostate 71(2):209–224 PubMedCrossRefGoogle Scholar
  6. 6.
    Prokunina-Olsson L, Fu YP, Tang W, Jacobs KB, Hayes RB, Kraft P, Berndt SI, Wacholder S, Yu K, Hutchinson A, Spencer FH, Thun MJ, Diver WR, Albanes D, Virtamo J, Weinstein S, Schumacher FR, Cancel-Tassin G, Cussenot O, Valeri A, Andriole GL, Crawford ED, Haiman CA, Henderson BE, Kolonel L, Le ML, Siddiq A, Riboli E, Travis R, Kaaks R, Isaacs WB, Isaacs SD, Gronberg H, Wiklund F, Xu J, Vatten LJ, Hveem K, Kumle M, Tucker M, Hoover RN, Fraumeni JF Jr, Hunter DJ, Thomas G, Chatterjee N, Chanock SJ, Yeager M (2010) Refining the prostate cancer genetic association within the JAZF1 gene on chromosome 7p15.2. Cancer Epidemiol Biomarkers Prev 19(5):1349–1355PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Hanas JS, Gunn CG (1996) Inhibition of transcription factor IIIA-DNA interactions by xenobiotic metal ions. Nucleic Acids Res 24(5):924–930PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Hanas JS, Rodgers JS, Bantle JA, Cheng YG (1999) Lead inhibition of DNA-binding mechanism of Cys(2)His(2) zinc finger proteins. Mol Pharmacol 56(5):982–988PubMedGoogle Scholar
  9. 9.
    Asmuss M, Mullenders LH, Hartwig A (2000) Interference by toxic metal compounds with isolated zinc finger DNA repair proteins. Toxicol Lett 112–113:227–231PubMedCrossRefGoogle Scholar
  10. 10.
    Beyersmann D, Hartwig A (2008) Carcinogenic metal compounds: recent insight into molecular and cellular mechanisms. Arch Toxicol 82(8):493–512PubMedCrossRefGoogle Scholar
  11. 11.
    Koedrith P, Seo YR (2011) Advances in carcinogenic metal toxicity and potential molecular markers. Int J Mol Sci 12(12):9576–9595PubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Meplan C, Mann K, Hainaut P (1999) Cadmium induces conformational modifications of wild-type p53 and suppresses p53 response to DNA damage in cultured cells. J Biol Chem 274(44):31663–31670PubMedCrossRefGoogle Scholar
  13. 13.
    Hartwig A, Asmuss M, Ehleben I, Herzer U, Kostelac D, Pelzer A, Schwerdtle T, Burkle A (2002) Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Environ Health Perspect 110(Suppl 5):797–799PubMedCentralPubMedCrossRefGoogle Scholar
  14. 14.
    Wirth JJ, Mijal RS (2010) Adverse effects of low level heavy metal exposure on male reproductive function. Syst Biol Reprod Med 56(2):147–167PubMedCrossRefGoogle Scholar
  15. 15.
    Sahmoun AE, Case LD, Jackson SA, Schwartz GG (2005) Cadmium and prostate cancer: a critical epidemiologic analysis. Cancer Invest 23(3):256–263PubMedCrossRefGoogle Scholar
  16. 16.
    Thun MJ, Schnorr TM, Smith AB, Halperin WE, Lemen RA (1985) Mortality among a cohort of U.S. cadmium production workers—an update. J Natl Cancer Inst 74(2):325–333PubMedGoogle Scholar
  17. 17.
    International Agency for Research on Cancer (1987) Overall evaluation of carcinogenicity:updating of IARC Monographs Vols. 1–42. IARC Monogr 1–42:230–232Google Scholar
  18. 18.
    International Agency For Research On Cancer (2006) Inorganic and Organic Lead Compounds: Summary of Data Reported and Evaluation. Vol. 87: IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. (2004: Lyon, France). 87Google Scholar
  19. 19.
    Telisman S, Colak B, Pizent A, Jurasovic J, Cvitkovic P (2007) Reproductive toxicity of low-level lead exposure in men. Environ Res 105(2):256–266PubMedCrossRefGoogle Scholar
  20. 20.
    Zaichick VY, Sviridova TV, Zaichick SV (1996) Zinc concentration in human prostatic fluid: normal, chronic prostatitis, adenoma and cancer. Int Urol Nephrol 28(5):687–694PubMedCrossRefGoogle Scholar
  21. 21.
    Zaichick VY, Sviridova TV, Zaichick SV (1997) Zinc in the human prostate gland: normal, hyperplastic and cancerous. Int Urol Nephrol 29(5):565–574PubMedCrossRefGoogle Scholar
  22. 22.
    Costello LC, Franklin RB (2011) Zinc is decreased in prostate cancer: an established relationship of prostate cancer! J Biol Inorg Chem 16(1):3–8PubMedCentralPubMedCrossRefGoogle Scholar
  23. 23.
    Hogervorst J, Plusquin M, Vangronsveld J, Nawrot T, Cuypers A, Van HE, Roels HA, Carleer R, Staessen JA (2007) House dust as possible route of environmental exposure to cadmium and lead in the adult general population. Environ Res 103(1):30–37PubMedCrossRefGoogle Scholar
  24. 24.
    Nriagu J, Burt B, Linder A, Ismail A, Sohn W (2006) Lead levels in blood and saliva in a low-income population of Detroit, Michigan. Int J Hyg Environ Health 209(2):109–121PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Dye BA, Hirsch R, Brody DJ (2002) The relationship between blood lead levels and periodontal bone loss in the United States, 1988–1994. Environ Health Perspect 110(10):997–1002PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Muntner P, Menke A, DeSalvo KB, Rabito FA, Batuman V (2005) Continued decline in blood lead levels among adults in the United States: the National Health and Nutrition Examination Surveys. Arch Intern Med 165(18):2155–2161PubMedCrossRefGoogle Scholar
  27. 27.
    Krieger N, Chen JT, Waterman PD, Soobader MJ, Subramanian SV, Carson R (2003) Choosing area based socioeconomic measures to monitor social inequalities in low birth weight and childhood lead poisoning: the public health disparities geocoding project (US). J Epidemiol Community Health 57(3):186–199PubMedCentralPubMedCrossRefGoogle Scholar
  28. 28.
    Krieger N, Chen JT, Waterman PD, Rehkopf DH, Subramanian SV (2003) Race/ethnicity, gender, and monitoring socioeconomic gradients in health: a comparison of area-based socioeconomic measures—the public health disparities geocoding project. Am J Public Health 93(10):1655–1671PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Sargent JD, Bailey A, Simon P, Blake M, Dalton MA (1997) Census tract analysis of lead exposure in Rhode Island children. Environ Res 74(2):159–168PubMedCrossRefGoogle Scholar
  30. 30.
    Update: blood lead levels–United States, 1991–1994 (1997). MMWR Morb Mortal Wkly Rep 46 (7):141–146Google Scholar
  31. 31.
    Bako G, Smith ES, Hanson J, Dewar R (1982) The geographical distribution of high cadmium concentrations in the environment and prostate cancer in Alberta. Can J Public Health 73(2):92–94PubMedGoogle Scholar
  32. 32.
    Platz EA, Helzlsouer KJ, Hoffman SC, Morris JS, Baskett CK, Comstock GW (2002) Prediagnostic toenail cadmium and zinc and subsequent prostate cancer risk. Prostate 52(4):288–296PubMedCrossRefGoogle Scholar
  33. 33.
    Vinceti M, Venturelli M, Sighinolfi C, Trerotoli P, Bonvicini F, Ferrari A, Bianchi G, Serio G, Bergomi M, Vivoli G (2007) Case–control study of toenail cadmium and prostate cancer risk in Italy. Sci Total Environ 373(1):77–81PubMedCrossRefGoogle Scholar
  34. 34.
    Chen YC, Pu YS, Wu HC, Wu TT, Lai MK, Yang CY, Sung FC (2009) Cadmium burden and the risk and phenotype of prostate cancer. BMC Cancer 9:429PubMedCentralPubMedCrossRefGoogle Scholar
  35. 35.
    Lam TV, Agovino P, Niu X, Roche L (2007) Linkage study of cancer risk among lead-exposed workers in New Jersey. Sci Total Environ 372(2–3):455–462PubMedCrossRefGoogle Scholar
  36. 36.
    Rousseau MC, Parent ME, Nadon L, Latreille B, Siemiatycki J (2007) Occupational exposure to lead compounds and risk of cancer among men: a population-based case–control study. Am J Epidemiol 166(9):1005–1014PubMedCrossRefGoogle Scholar
  37. 37.
    Rybicki BA, Neslund-Dudas C, Nock NL, Schultz LR, Eklund L, Rosbolt J, Bock CH, Monaghan KG (2006) Prostate cancer risk from occupational exposure to polycyclic aromatic hydrocarbons interacting with the GSTP1 Ile105Val polymorphism. Cancer Detect Prev 30(5):412–422PubMedCentralPubMedCrossRefGoogle Scholar
  38. 38.
    Tang D, Liu JJ, Rundle A, Neslund-Dudas C, Savera AT, Bock CH, Nock NL, Yang JJ, Rybicki BA (2007) Grilled meat consumption and PhIP-DNA adducts in prostate carcinogenesis. Cancer Epidemiol Biomarkers Prev 16(4):803–808PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Umbach DM, Weinberg CR (1997) Designing and analysing case–control studies to exploit independence of genotype and exposure. Stat Med 16(15):1731–1743PubMedCrossRefGoogle Scholar
  40. 40.
    Chang BL, Spangler E, Gallagher S, Haiman CA, Henderson BE, Isaacs WB, Benford ML, Kidd LR, Cooney K, Strom SS, Ingles SA, Stern MC, Corral R, Joshi AD, Xu J, Giri VN, Rybicki BA, Neslund-Dudas C, Kibel AS, Thompson IM Jr, Leach RJ, Ostrander EA, Stanford J, Witte JS, Casey G, Eeles R, Hsing AW, Chanock SJ, Hu JJ, John EM, Park JY, Stefflova K, Zeigler-Johnson C, Rebbeck TR (2011) Validation of genome-wide prostate cancer associations in men of African descent. Cancer Epidemiol Biomarkers Prev 20(1):23–32PubMedCentralPubMedCrossRefGoogle Scholar
  41. 41.
    Bock CH, Schwartz AG, Ruterbusch JJ, Levin AM, Neslund-Dudas C, Land SJ, Wenzlaff AS, Reich D, McKeigue P, Chen W, Heath EI, Powell IJ, Kittles RA, Rybicki BA (2009) Results from a prostate cancer admixture mapping study in African-American men. Hum Genet 126(5):637–642PubMedCentralPubMedCrossRefGoogle Scholar
  42. 42.
    Bress WC, Bidanset JH (1991) Percutaneous in vivo and in vitro absorption of lead. Vet Hum Toxicol 33(3):212–214PubMedGoogle Scholar
  43. 43.
    Stauber JL, Florence TM, Gulson BL, Dale LS (1994) Percutaneous absorption of inorganic lead compounds. Sci Total Environ 145(1–2):55–70PubMedCrossRefGoogle Scholar
  44. 44.
    Sun CC, Wong TT, Hwang YH, Chao KY, Jee SH, Wang JD (2002) Percutaneous absorption of inorganic lead compounds. AIHA J (Fairfax, Va) 63(5):641–646CrossRefGoogle Scholar
  45. 45.
    Filon FL, Boeniger M, Maina G, Adami G, Spinelli P, Damian A (2006) Skin absorption of inorganic lead (PbO) and the effect of skin cleansers. J Occup Environ Med 48(7):692–699PubMedCrossRefGoogle Scholar
  46. 46.
    Pan J, Plant JA, Voulvoulis N, Oates CJ, Ihlenfeld C (2010) Cadmium levels in Europe: implications for human health. Environ Geochem Health 32(1):1–12PubMedCrossRefGoogle Scholar
  47. 47.
    Khoury MJ, Flanders WD (1996) Nontraditional epidemiologic approaches in the analysis of gene–environment interaction: case–control studies with no controls! Am J Epidemiol 144(3):207–213PubMedCrossRefGoogle Scholar
  48. 48.
    Frazer KA, Ballinger DG, Cox DR, Hinds DA, Stuve LL, Gibbs RA, Belmont JW, Boudreau A, Hardenbol P, Leal SM, Pasternak S, Wheeler DA, Willis TD, Yu F, Yang H, Zeng C, Gao Y, Hu H, Hu W, Li C, Lin W, Liu S, Pan H, Tang X, Wang J, Wang W, Yu J, Zhang B, Zhang Q, Zhao H, Zhou J, Gabriel SB, Barry R, Blumenstiel B, Camargo A, Defelice M, Faggart M, Goyette M, Gupta S, Moore J, Nguyen H, Onofrio RC, Parkin M, Roy J, Stahl E, Winchester E, Ziaugra L, Altshuler D, Shen Y, Yao Z, Huang W, Chu X, He Y, Jin L, Liu Y, Sun W, Wang H, Wang Y, Xiong X, Xu L, Waye MM, Tsui SK, Xue H, Wong JT, Galver LM, Fan JB, Gunderson K, Murray SS, Oliphant AR, Chee MS, Montpetit A, Chagnon F, Ferretti V, Leboeuf M, Olivier JF, Phillips MS, Roumy S, Sallee C, Verner A, Hudson TJ, Kwok PY, Cai D, Koboldt DC, Miller RD, Pawlikowska L, Taillon-Miller P, Xiao M, Tsui LC, Mak W, Song YQ, Tam PK, Nakamura Y, Kawaguchi T, Kitamoto T, Morizono T, Nagashima A, Ohnishi Y, Sekine A, Tanaka T, Tsunoda T, Deloukas P, Bird CP, Delgado M, Dermitzakis ET, Gwilliam R, Hunt S, Morrison J, Powell D, Stranger BE, Whittaker P, Bentley DR, Daly MJ, de Bakker PI, Barrett J, Chretien YR, Maller J, McCarroll S, Patterson N, Pe’er I, Price A, Purcell S, Richter DJ, Sabeti P, Saxena R, Schaffner SF, Sham PC, Varilly P, Stein LD, Krishnan L, Smith AV, Tello-Ruiz MK, Thorisson GA, Chakravarti A, Chen PE, Cutler DJ, Kashuk CS, Lin S, Abecasis GR, Guan W, Li Y, Munro HM, Qin ZS, Thomas DJ, McVean G, Auton A, Bottolo L, Cardin N, Eyheramendy S, Freeman C, Marchini J, Myers S, Spencer C, Stephens M, Donnelly P, Cardon LR, Clarke G, Evans DM, Morris AP, Weir BS, Mullikin JC, Sherry ST, Feolo M, Skol A, Zhang H, Matsuda I, Fukushima Y, Macer DR, Suda E, Rotimi CN, Adebamowo CA, Ajayi I, Aniagwu T, Marshall PA, Nkwodimmah C, Royal CD, Leppert MF, Dixon M, Peiffer A, Qiu R, Kent A, Kato K, Niikawa N, Adewole IF, Knoppers BM, Foster MW, Clayton EW, Watkin J, Muzny D, Nazareth L, Sodergren E, Weinstock GM, Yakub I, Birren BW, Wilson RK, Fulton LL, Rogers J, Burton J, Carter NP, Clee CM, Griffiths M, Jones MC, McLay K, Plumb RW, Ross MT, Sims SK, Willey DL, Chen Z, Han H, Kang L, Godbout M, Wallenburg JC, L’Archeveque P, Bellemare G, Saeki K, An D, Fu H, Li Q, Wang Z, Wang R, Holden AL, Brooks LD, McEwen JE, Guyer MS, Wang VO, Peterson JL, Shi M, Spiegel J, Sung LM, Zacharia LF, Collins FS, Kennedy K, Jamieson R, Stewart J (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449(7164):851–861PubMedCrossRefGoogle Scholar
  49. 49.
    Muntner P, He J, Vupputuri S, Coresh J, Batuman V (2003) Blood lead and chronic kidney disease in the general United States population: results from NHANES III. Kidney Int 63(3):1044–1050PubMedCrossRefGoogle Scholar
  50. 50.
    Richter PA, Bishop EE, Wang J, Swahn MH (2009) Tobacco smoke exposure and levels of urinary metals in the U.S. youth and adult population: the National Health and Nutrition Examination Survey (NHANES) 1999–2004. Int J Environ Res Public Health 6(7):1930–1946PubMedCentralPubMedCrossRefGoogle Scholar
  51. 51.
    O’Leary ES, Schoenfeld ER, Henderson K, Grimson R, Kabat GC, Kaune WT, Gammon MD, Leske MC (2003) Wire coding in the EMF and Breast Cancer on Long Island Study: relationship to magnetic fields. J Expo Anal Environ Epidemiol 13(4):283–293PubMedCrossRefGoogle Scholar
  52. 52.
    Charles LE, Loomis D, Shy CM, Newman B, Millikan R, Nylander-French LA, Couper D (2003) Electromagnetic fields, polychlorinated biphenyls, and prostate cancer mortality in electric utility workers. Am J Epidemiol 157(8):683–691PubMedCrossRefGoogle Scholar
  53. 53.
    Haddow AD, Bixler D, Schuh AJ (2011) The demographic and socioeconomic factors predictive for populations at high-risk for la crosse virus infection in West Virginia. PLoS One 6(9):e25739PubMedCentralPubMedCrossRefGoogle Scholar
  54. 54.
    Schootman M, Andresen EM, Wolinsky FD, Malmstrom TK, Morley JE, Miller DK (2010) Adverse housing and neighborhood conditions and inflammatory markers among middle-aged African Americans. J Urban Health 87(2):199–210PubMedCentralPubMedCrossRefGoogle Scholar
  55. 55.
    Nakajima T, Fujino S, Nakanishi G, Kim YS, Jetten AM (2004) TIP27: a novel repressor of the nuclear orphan receptor TAK1/TR4. Nucleic Acids Res 32(14):4194–4204PubMedCentralPubMedCrossRefGoogle Scholar
  56. 56.
    Lapointe J, Li C, Higgins JP, van de Rijn M, Bair E, Montgomery K, Ferrari M, Egevad L, Rayford W, Bergerheim U, Ekman P, DeMarzo AM, Tibshirani R, Botstein D, Brown PO, Brooks JD, Pollack JR (2004) Gene expression profiling identifies clinically relevant subtypes of prostate cancer. Proc Natl Acad Sci USA 101(3):811–816PubMedCentralPubMedCrossRefGoogle Scholar
  57. 57.
    Wallace TA, Prueitt RL, Yi M, Howe TM, Gillespie JW, Yfantis HG, Stephens RM, Caporaso NE, Loffredo CA, Ambs S (2008) Tumor immuno biological differences in prostate cancer between African-American and European-American men. Cancer Res 68(3):927–936PubMedCrossRefGoogle Scholar
  58. 58.
    Chang C, Da Silva SL, Ideta R, Lee Y, Yeh S, Burbach JP (1994) Human and rat TR4 orphan receptors specify a subclass of the steroid receptor superfamily. Proc Natl Acad Sci USA 91(13):6040–6044PubMedCentralPubMedCrossRefGoogle Scholar
  59. 59.
    Lee YF, Shyr CR, Thin TH, Lin WJ, Chang C (1999) Convergence of two repressors through heterodimer formation of androgen receptor and testicular orphan receptor-4: a unique signaling pathway in the steroid receptor superfamily. Proc Natl Acad Sci USA 96(26):14724–14729PubMedCentralPubMedCrossRefGoogle Scholar
  60. 60.
    Liu NC, Lin WJ, Kim E, Collins LL, Lin HY, Yu IC, Sparks JD, Chen LM, Lee YF, Chang C (2007) Loss of TR4 orphan nuclear receptor reduces phosphoenolpyruvate carboxykinase-mediated gluconeogenesis. Diabetes 56(12):2901–2909PubMedCrossRefGoogle Scholar
  61. 61.
    Soraham T, Waterhouse JA (1985) Cancer of prostate among nickel-cadmium battery workers. Lancet 1(8426):459PubMedCrossRefGoogle Scholar
  62. 62.
    Enterline PE, Marsh GM (1980) Mortality studies of smelter workers. Am J Ind Med 1(3–4):251–259PubMedCrossRefGoogle Scholar
  63. 63.
    McMichael AJ, Johnson HM (1982) Long-term mortality profile of heavily-exposed lead smelter workers. J Occup Med 24(5):375–378PubMedCrossRefGoogle Scholar
  64. 64.
    Selevan SG, Landrigan PJ, Stern FB, Jones JH (1985) Mortality of lead smelter workers. Am J Epidemiol 122(4):673–683PubMedGoogle Scholar
  65. 65.
    Gerhardsson L, Lundstrom NG, Nordberg G, Wall S (1986) Mortality and lead exposure: a retrospective cohort study of Swedish smelter workers. Br J Ind Med 43(10):707–712PubMedCentralPubMedGoogle Scholar
  66. 66.
    Fu H, Boffetta P (1995) Cancer and occupational exposure to inorganic lead compounds: a meta-analysis of published data. Occup Environ Med 52(2):73–81PubMedCentralPubMedCrossRefGoogle Scholar
  67. 67.
    Apostoli P, Kiss P, Porru S, Bonde JP, Vanhoorne M (1998) Male reproductive toxicity of lead in animals and humans. ASCLEPIOS Study Group. Occup Environ Med 55(6):364–374PubMedCentralPubMedCrossRefGoogle Scholar
  68. 68.
    Woodruff TJ, Carlson A, Schwartz JM, Giudice LC (2008) Proceedings of the summit on environmental challenges to reproductive health and fertility: executive summary. Fertil Steril 89(2):281–300PubMedCentralPubMedCrossRefGoogle Scholar
  69. 69.
    Mendiola J, Moreno JM, Roca M, Vergara-Juarez N, Martinez-Garcia MJ, Garcia-Sanchez A, Elvira-Rendueles B, Moreno-Grau S, Lopez-Espin JJ, Ten J, Bernabeu R, Torres-Cantero AM (2011) Relationships between heavy metal concentrations in three different body fluids and male reproductive parameters: a pilot study. Environ Health 10(1):6PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Anis TH, ElKaraksy A, Mostafa T, Gadalla A, Imam H, Hamdy L, Abu el-Alla O (2007) Chronic lead exposure may be associated with erectile dysfunction. J Sex Med 4(5):1428–1434PubMedCrossRefGoogle Scholar
  71. 71.
    van Wijngaarden E, Singer EA, Palapattu GS (2008) Prostate-specific antigen levels in relation to cadmium exposure and zinc intake: results from the 2001–2002 National Health and Nutrition Examination Survey. Prostate 68(2):122–128PubMedCrossRefGoogle Scholar
  72. 72.
    Pizent A, Colak B, Kljakovic Z, Telisman S (2009) Prostate-specific antigen (PSA) in serum in relation to blood lead concentration and alcohol consumption in men. Arh Hig Rada Toksikol 60(1):69–78PubMedCrossRefGoogle Scholar
  73. 73.
    Clayton D, McKeigue PM (2001) Epidemiological methods for studying genes and environmental factors in complex diseases. Lancet 358(9290):1356–1360PubMedCrossRefGoogle Scholar
  74. 74.
    Bookman EB, McAllister K, Gillanders E, Wanke K, Balshaw D, Rutter J, Reedy J, Shaughnessy D, gurs-Collins T, Paltoo D, Atienza A, Bierut L, Kraft P, Fallin MD, Perera F, Turkheimer E, Boardman J, Marazita ML, Rappaport SM, Boerwinkle E, Suomi SJ, Caporaso NE, Hertz-Picciotto I, Jacobson KC, Lowe WL, Goldman LR, Duggal P, Gunnar MR, Manolio TA, Green ED, Olster DH, Birnbaum LS (2011) Gene–environment interplay in common complex diseases: forging an integrative model-recommendations from an NIH workshop. Genet Epidemiol 35:217–225Google Scholar
  75. 75.
    Bhatti P, Stewart PA, Linet MS, Blair A, Inskip PD, Rajaraman P (2011) Comparison of occupational exposure assessment methods in a case-control study of lead, genetic susceptibility and risk of adult brain tumours. Occup Environ Med 68:4–9PubMedCrossRefGoogle Scholar
  76. 76.
    Mielke HW, Powell ET, Shah A, Gonzales CR, Mielke PW (2001) Multiple metal contamination from house paints: consequences of power sanding and paint scraping in New Orleans. Environ Health Perspect 109(9):973–978PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  • Christine Neslund-Dudas
    • 1
    • 2
    Email author
  • Albert M. Levin
    • 1
    • 2
  • Jennifer L. Beebe-Dimmer
    • 2
    • 3
  • Cathryn H. Bock
    • 2
    • 3
  • Nora L. Nock
    • 4
  • Andrew Rundle
    • 5
  • Michelle Jankowski
    • 1
  • Richard Krajenta
    • 1
  • Q. Ping Dou
    • 3
    • 6
    • 7
  • Bharati Mitra
    • 8
  • Deliang Tang
    • 9
  • Timothy R. Rebbeck
    • 10
    • 11
  • Benjamin A. Rybicki
    • 1
    • 2
  1. 1.Department of Public Health SciencesHenry Ford Health SystemDetroitUSA
  2. 2.Population Studies and Disparities ResearchBarbara Ann Karmanos Cancer InstituteDetroitUSA
  3. 3.Department of OncologyWayne State University School of MedicineDetroitUSA
  4. 4.Department of Epidemiology and BiostatisticsCase Western Reserve UniversityClevelandUSA
  5. 5.Departments of Epidemiology, Mailman School of Public HealthColumbia UniversityNew YorkUSA
  6. 6.Developmental Therapeutics ProgramsBarbara Ann Karmanos Cancer InstituteDetroitUSA
  7. 7.Department of Pharmacology and PathologyWayne State University School of MedicineDetroitUSA
  8. 8.Department of Biochemistry and Molecular BiologyWayne State University School of MedicineDetroitUSA
  9. 9.Department of Environmental Health Sciences, Mailman School of Public HealthColumbia UniversityNew YorkUSA
  10. 10.Department of Biostatistics and Epidemiology, Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA
  11. 11.Abramson Cancer Center, Perelman School of MedicineUniversity of PennsylvaniaPhiladelphiaUSA

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