European genome-wide association study identifies SLC14A1 as a new urinary bladder cancer susceptibility gene

Human Molecular Genetics

Volumn 20, Issue 21, 2011, Pages 4268-4281

  Rafnar, Thorunn ^a   Vermeulen, Sita H ^b   Sulem, Patrick ^a   Thorleifsson, Gudmar ^a   Aben, Katja K ^b,d   Witjes, J A ^b   Grotenhuis, Anne J ^b   Verhaegh, Gerald W ^b   van de Kaa, Christina A Hulsbergen ^c   Besenbacher, Soren ^e   Gudbjartsson, Daniel ^a   Stacey, Simon N ^a   Gudmundsson, Julius ^a   Johannsdottir, Hrefna ^a   Bjarnason, Hjordis ^a   Zanon, Carlo ^a   Helgadottir, Hafdis ^a   Jonasson, Jon Gunnlaugur ^f,g   Tryggvadottir, Laufey ^f,g   Jonsson, Eirikur ^h   Geirsson, Gudmundur ^h   Nikulasson, Sigfus ^h   Petursdottir, Vigdis ^h   Bishop, D Timothy ⁱ   Chung Sak, Sei ⁱ   Choudhury, Ananya ^j   Elliott, Faye ⁱ   Barrett, Jennifer H ⁱ   Knowles, Margaret A ⁱ   de Verdier, Petra J ^k   Ryk, Charlotta ^k   Lindblom, Annika ^k   Rudnai, Peter ^l   Gurzau, Eugene ^m   Koppova, Kvetoslava ⁿ   Vineis, Paolo ^o,p   Polidoro, Silvia ^o   Guarrera, Simonetta ^o   Sacerdote, Carlotta ^o,q   Panadero, Angeles ^r   Sanz Velez, José I ^s   Sanchez, Manuel ^t   Valdivia, Gabriel ^t   Garcia Prats, Maria D ^s   Hengstler, Jan G ^u   Selinski, Silvia ^u   Gerullis, Holger ^b   Ovsiannikov, Daniel ^v   Khezri, Abdolaziz ^w   Aminsharifi, Alireza ^x   Malekzadeh, Mahyar ^w   van den Berg, Leonard H ^y   Ophoff, Roel A ^y,z   Veldink, Jan H ^y   Zeegers, Maurice P ^aa,ac   Kellen, Eliane ^ad   Fostinelli, Jacopo ^ae   Andreoli, Daniele ^ae   Arici, Cecilia ^ae   Porru, Stefano ^ae   Buntinx, Frank ^ab,ad   Ghaderi, Abbas ^w   Golka, Klaus ^u   Mayordomo, José I ^t   Matullo, Giuseppe ^o,af   Kumar, Rajiv ^ag   Steineck, Gunnar ^ah   Kiltie, Anne E ^ai   Kong, Augustine ^a   Thorsteinsdottir, Unnur ^a,g   Stefansson, Kari ^a,g   Kiemeney, Lambertus A ^b,d   more..

^a DECODE GENETICS   (Iceland)

^b Biostatistics and HTA ^*  (Germany)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d Integraal Kankercentrum Nederland   (Netherlands)

^e AARHUS UNIVERSITY   (Denmark)

^f ICELANDIC CANCER REGISTRY   (Iceland)

^g UNIVERSITY OF ICELAND   (Iceland)

^h LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

ⁱ ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

^j CHRISTIE HOSPITAL   (United Kingdom)

^k KAROLINSKA INSTITUTE   (Sweden)

^l NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH   (Hungary)

^m Environmental Health Centre   (Romania)

ⁿ State Health Institute   (Slovakia)

^o Human Genetics Foundation   (Italy)

^p HOSPITAL SAN JORGE   (Spain)

^q Centre for Cancer Epidemiology and Prevention (CPO Piemonte)   (Italy)

^r Hospital Ciudad de Coria   (Spain)

^s San Jorge University Hospital   (Spain)

^t UNIVERSITY OF ZARAGOZA   (Spain)

^u LEIBNIZ RESEARCH CENTRE FOR WORKING ENVIRONMENT AND HUMAN FACTORS   (Germany)

^v St Josefs Hospital Dortmund Hörde   (Germany)

^w SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^x SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^y UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^z UNIVERSITY OF CALIFORNIA   (United States)

^aa MAASTRICHT UNIVERSITY   (Netherlands)

^ab MAASTRICHT UNIVERSITY   (Netherlands)

^ac UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^ad UNIVERSITY OF LEUVEN   (Belgium)

^ae UNIVERSITY OF BRESCIA   (Italy)

^af UNIVERSITY OF TURIN   (Italy)

^ag GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^ah SAHLGRENSKA UNIVERSITY HOSPITAL   (Sweden)

^ai UNIVERSITY OF OXFORD   (United Kingdom)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; AGED; ARTICLE; BLADDER CANCER; CANCER SUSCEPTIBILITY; EUROPE; FEMALE; FOLLOW UP; GENE; GENE LOCUS; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; HUMAN; ICELAND; IRAN; KIDNEY CONCENTRATING CAPACITY; KIDNEY MEDULLA; MAJOR CLINICAL STUDY; MALE; NETHERLANDS; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SLC14A1 GENE;

ADULT; AGED; AGED, 80 AND OVER; CHROMOSOMES, HUMAN, PAIR 18; DISEASE PROGRESSION; EUROPEAN CONTINENTAL ANCESTRY GROUP; FEMALE; GENETIC LOCI; GENETIC PREDISPOSITION TO DISEASE; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; MEMBRANE TRANSPORT PROTEINS; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; REPRODUCIBILITY OF RESULTS; RISK FACTORS; URINARY BLADDER NEOPLASMS; YOUNG ADULT;

EID: 80053945781     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr303     Document Type: Article

References (55)

1. Ploeg, M., Aben, K.K. and Kiemeney, L.A. (2009) The present and future burden of urinary bladder cancer in the world. World J. Urol., 27, 289-293.
2. Ferlay, J., Shin, H.R., Bray, F., Forman, D., Mathers, C. and Parkin, D.M. (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008 Int. J. Cancer, 127, 2893-2917.
3. Sievert, K.D., Amend, B., Nagele, U., Schilling, D., Bedke, J., Horstmann, M., Hennenlotter, J., Kruck, S. and Stenzl, A. (2009) Economic aspects of bladder cancer: what are the benefits and costs? World J. Urol., 27, 295-300.
4. Mueller, C.M., Caporaso, N. and Greene, M.H. (2008) Familial and genetic risk of transitional cell carcinoma of the urinary tract. Urol. Oncol., 26, 451-464.
5. Aben, K.K., Witjes, J.A., Schoenberg, M.P., Hulsbergen-van de Kaa, C., Verbeek, A.L. and Kiemeney, L.A. (2002) Familial aggregation of urothelial cell carcinoma. Int. J. Cancer, 98, 274-278.
6. Aben, K.K., Baglietto, L., Baffoe-Bonnie, A., Coebergh, J.W., Bailey-Wilson, J.E., Trink, B., Verbeek, A.L., Schoenberg, M.P., Alfred, W.J. and Kiemeney, L.A. (2006) Segregation analysis of urothelial cell carcinoma. Eur. J. Cancer, 42, 1428-1433.
7. Murta-Nascimento, C., Silverman, D.T., Kogevinas, M., Garcia-Closas, M., Rothman, N., Tardon, A., Garcia-Closas, R., Serra, C., Carrato, A., Villanueva, C. et al. (2007) Risk of bladder cancer associated with family history of cancer: do low-penetrance polymorphisms account for the increase in risk? Cancer Epidemiol. Biomarkers Prev., 16, 1595-1600.
8. Amundadottir, L.T., Thorvaldsson, S., Gudbjartsson, D.F., Sulem, P., Kristjansson, K., Arnason, S., Gulcher, J.R., Bjornsson, J., Kong, A., Thorsteinsdottir, U. and Stefansson, K. (2004) Cancer as a complex phenotype: pattern of cancer distribution within and beyond the nuclear family. PLoS Med., 1, e65.
9. Garcia-Closas, M., Malats, N., Silverman, D., Dosemeci, M., Kogevinas, M., Hein, D.W., Tardon, A., Serra, C., Carrato, A., Garcia-Closas, R. et al. (2005) NAT2 slow acetylation, GSTM1 null genotype, and risk of bladder cancer: results from the Spanish Bladder Cancer Study and meta-analyses. Lancet, 366, 649-659.
10. Kiemeney, L.A., Thorlacius, S., Sulem, P., Geller, F., Aben, K.K., Stacey, S.N., Gudmundsson, J., Jakobsdottir, M., Bergthorsson, J.T., Sigurdsson, A. et al. (2008) Sequence variant on 8q24 confers susceptibility to urinary bladder cancer. Nat. Genet., 40, 1307-1312.
11. Kiemeney, L.A., Sulem, P., Besenbacher, S., Vermeulen, S.H., Sigurdsson, A., Thorleifsson, G., Gudbjartsson, D.F., Stacey, S.N., Gudmundsson, J., Zanon, C. et al. (2010) A sequence variant at 4p16.3 confers susceptibility to urinary bladder cancer. Nat. Genet., 42, 415-419.
12. Rothman, N., Garcia-Closas, M., Chatterjee, N., Malats, N., Wu, X., Figueroa, J.D., Real, F.X., Van Den, B.D., Matullo, G., Baris, D. et al. (2010) A multi-stage genome-wide association study of bladder cancer identifies multiple susceptibility loci. Nat. Genet., 42, 978-984.
13. Wu, X., Ye, Y., Kiemeney, L.A., Sulem, P., Rafnar, T., Matullo, G., Seminara, D., Yoshida, T., Saeki, N., Andrew, A.S. et al. (2009) Genetic variation in the prostate stem cell antigen gene PSCA confers susceptibility to urinary bladder cancer. Nat. Genet., 41, 991-995.
14. Stewart, G. (2011) The emerging physiological roles of the SLC14A family of urea transporters. Br. J. Pharmacol., 41, 991-995.
15. Olives, B., Merriman, M., Bailly, P., Bain, S., Barnett, A., Todd, J., Cartron, J.P. and Merriman, T. (1997) The molecular basis of the Kidd blood group polymorphism and its lack of association with type 1 diabetes susceptibility. Hum. Mol. Genet., 6, 1017-1020.
16. Thorgeirsson, T.E., Geller, F., Sulem, P., Rafnar, T., Wiste, A., Magnusson, K.P., Manolescu, A., Thorleifsson, G., Stefansson, H., Ingason, A. et al. (2008) A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature, 452, 638-642.
17. Gudbjartsson, D.F., Holm, H., Indridason, O.S., Thorleifsson, G., Edvardsson, V., Sulem, P., de Vegt, F., d'Ancona, F.C., den Heijer, M., Wetzels, J.F. et al. (2010) Association of variants at UMOD with chronic kidney disease and kidney stones-role of age and comorbid diseases. PLoS Genet., 6, e1001039.
18. Smith, C.P. (2009) Mammalian urea transporters. Exp. Physiol., 94, 180-185.
19. Fenton, R.A., Hewitt, J.E., Howorth, A., Cottingham, C.A. and Smith, C.P. (1999) The murine urea transporter genes Slc14a1 and Slc14a2 occur in tandem on chromosome 18. Cytogenet. Cell Genet., 87, 95-96.
20. Sands, J.M., Gargus, J.J., Frohlich, O., Gunn, R.B. and Kokko, J.P. (1992) Urinary concentrating ability in patients with Jk(a-b-) blood type who lack carrier-mediated urea transport. J. Am. Soc. Nephrol., 2, 1689-1696.
21. Yang, B., Bankir, L., Gillespie, A., Epstein, C.J. and Verkman, A.S. (2002) Urea-selective concentrating defect in transgenic mice lacking urea transporter UT-B. J. Biol. Chem., 277, 10633-10637.
22. Kamatani, Y., Matsuda, K., Okada, Y., Kubo, M., Hosono, N., Daigo, Y., Nakamura, Y. and Kamatani, N. (2010) Genome-wide association study of hematological and biochemical traits in a Japanese population. Nat. Genet., 42, 210-215.
23. Dyrskjot, L., Thykjaer, T., Kruhoffer, M., Jensen, J.L., Marcussen, N., Hamilton-Dutoit, S., Wolf, H. and Orntoft, T.F. (2003) Identifying distinct classes of bladder carcinoma using microarrays. Nat. Genet., 33, 90-96.
24. Dyrskjot, L., Kruhoffer, M., Thykjaer, T., Marcussen, N., Jensen, J.L., Moller, K. and Orntoft, T.F. (2004) Gene expression in the urinary bladder: a common carcinoma in situ gene expression signature exists disregarding histopathological classification. Cancer Res., 64, 4040-4048.
25. Braver, D.J., Modan, M., Chetrit, A., Lusky, A. and Braf, Z. (1987) Drinking, micturition habits, and urine concentration as potential risk factors in urinary bladder cancer. J. Natl Cancer Inst., 78, 437-440.
26. Michaud, D.S., Spiegelman, D., Clinton, S.K., Rimm, E.B., Curhan, G.C., Willett, W.C. and Giovannucci, E.L. (1999) Fluid intake and the risk of bladder cancer in men. N. Engl. J. Med., 340, 1390-1397.
27. Ros, M.M., Bas Bueno-de-Mesquita, H.B., Buchner, F.L., Aben, K.K., Kampman, E., Egevad, L., Overvad, K., Tjonneland, A., Roswall, N., Clavel-Chapelon, F. et al. (2011) Fluid intake and the risk of urothelial cell carcinomas in the European Prospective Investigation into Cancer and Nutrition (EPIC). Int. J. Cancer, 128, 2695-2708.
28. Kadlubar, F.F., Dooley, K.L., Teitel, C.H., Roberts, D.W., Benson, R.W., Butler, M.A., Bailey, J.R., Young, J.F., Skipper, P.W. and Tannenbaum, S.R. (1991) Frequency of urination and its effects on metabolism, pharmacokinetics, blood hemoglobin adduct formation, and liver and urinary bladder DNA adduct levels in beagle dogs given the carcinogen 4-aminobiphenyl. Cancer Res., 51, 4371-4377.
29. Wetzels, J.F., Kiemeney, L.A., Swinkels, D.W., Willems, H.L. and den Heijer, M. (2007) Age- and gender-specific reference values of estimated GFR in Caucasians: the Nijmegen Biomedical Study. Kidney Int., 72, 632-637.
30. van Es, M.A., Veldink, J.H., Saris, C.G., Blauw, H.M., van Vught, P.W., Birve, A., Lemmens, R., Schelhaas, H.J., Groen, E.J., Huisman, M.H. et al. (2009) Genome-wide association study identifies 19p13.3 (UNC13A) and 9p21.2 as susceptibility loci for sporadic amyotrophic lateral sclerosis. Nat. Genet., 41, 1083-1087.
31. Sak, S.C., Barrett, J.H., Paul, A.B., Bishop, D.T. and Kiltie, A.E. (2005) The polyAT, intronic IVS11-6 and Lys939Gln XPC polymorphisms are not associated with transitional cell carcinoma of the bladder. Br. J. Cancer, 92, 2262-2265.
32. Matullo, G., Guarrera, S., Sacerdote, C., Polidoro, S., Davico, L., Gamberini, S., Karagas, M., Casetta, G., Rolle, L., Piazza, A. and Vineis, P. (2005) Polymorphisms/haplotypes in DNA repair genes and smoking: a bladder cancer case-control study. Cancer Epidemiol. Biomarkers Prev., 14, 2569-2578.
33. Shen, M., Hung, R.J., Brennan, P., Malaveille, C., Donato, F., Placidi, D., Carta, A., Hautefeuille, A., Boffetta, P. and Porru, S. (2003) Polymorphisms of the DNA repair genes XRCC1, XRCC3, XPD, interaction with environmental exposures, and bladder cancer risk in a case-control study in northern Italy. Cancer Epidemiol. Biomarkers Prev., 12, 1234-1240.
34. Kellen, E., Zeegers, M., Paulussen, A., Van Dongen, M. and Buntinx, F. (2006) Fruit consumption reduces the effect of smoking on bladder cancer risk. The Belgian case control study on bladder cancer. Int. J. Cancer, 118, 2572-2578.
35. Thirumaran, R.K., Bermejo, J.L., Rudnai, P., Gurzau, E., Koppova, K., Goessler, W., Vahter, M., Leonardi, G.S., Clemens, F., Fletcher, T. et al. (2006) Single nucleotide polymorphisms in DNA repair genes and basal cell carcinoma of skin. Carcinogenesis, 27, 1676-1681.
36. Larsson, P., Wijkstrom, H., Thorstenson, A., Adolfsson, J., Norming, U., Wiklund, P., Onelov, E. and Steineck, G. (2003) A population-based study of 538 patients with newly detected urinary bladder neoplasms followed during 5 years. Scand. J. Urol. Nephrol., 37, 195-201.
37. Lehmann, M.L., Selinski, S., Blaszkewicz, M., Orlich, M., Ovsiannikov, D., Moormann, O., Guballa, C., Kress, A., Truss, M.C., Gerullis, H. et al. (2010) Rs710521[A] on chromosome 3q28 close to TP63 is associated with increased urinary bladder cancer risk. Arch. Toxicol., 84, 967-978.
38. Golka, K., Schmidt, T., Seidel, T., Dietrich, H., Roemer, H.C., Lohlein, D., Reckwitz, T., Sokeland, J., Weistenhofer, W., Blaszkewicz, M. and Selinski, S. (2008) The influence of polymorphisms of glutathione S-transferases M1 and M3 on the development of human urothelial cancer. J. Toxicol. Environ. Health A, 71, 881-886.
39. Golka, K., Hermes, M., Selinski, S., Blaszkewicz, M., Bolt, H.M., Roth, G., Dietrich, H., Prager, H.M., Ickstadt, K. and Hengstler, J.G. (2009) Susceptibility to urinary bladder cancer: relevance of rs9642880[T], GSTM1 0/0 and occupational exposure. Pharmacogenet. Genomics, 19, 903-906.
40. Howie, B.N., Donnelly, P. and Marchini, J. (2009) A flexible and accurate genotype imputation method for the next generation of genome-wide association studies. PLoS Genet., 5, e1000529.
41. Marchini, J., Howie, B., Myers, S., McVean, G. and Donnelly, P. (2007) A new multipoint method for genome-wide association studies by imputation of genotypes. Nat. Genet., 39, 906-913.
42. Kong, A., Steinthorsdottir, V., Masson, G., Thorleifsson, G., Sulem, P., Besenbacher, S., Jonasdottir, A., Sigurdsson, A., Kristinsson, K.T., Jonasdottir, A. et al. (2009) Parental origin of sequence variants associated with complex diseases. Nature, 462, 868-874.
43. Kutyavin, I.V., Milesi, D., Belousov, Y., Podyminogin, M., Vorobiev, A., Gorn, V., Lukhtanov, E.A., Vermeulen, N.M. and Mahoney, W. (2006) A novel endonuclease IV post-PCR genotyping system. Nucleic Acids Res., 34, e128.
44. International Hapmap Consortium (2005) A haplotype map of the human genome. Nature, 437, 1299-1320.
45. Kruglyak, L. and Lander, E.S. (1998) Faster multipoint linkage analysis using Fourier transforms. J. Comput. Biol., 5, 1-7.
46. Lander, E.S. and Green, P. (1987) Construction of multilocus genetic linkage maps in humans. Proc. Natl Acad. Sci. USA, 84, 2363-2367.
47. Kong, A., Thorleifsson, G., Gudbjartsson, D.F., Masson, G., Sigurdsson, A., Jonasdottir, A., Walters, G.B., Jonasdottir, A., Gylfason, A., Kristinsson, K.T. et al. (2010) Fine-scale recombination rate differences between sexes, populations and individuals. Nature, 467, 1099-1103.
48. Gretarsdottir, S., Thorleifsson, G., Reynisdottir, S.T., Manolescu, A., Jonsdottir, S., Jonsdottir, T., Gudmundsdottir, T., Bjarnadottir, S.M., Einarsson, O.B., Gudjonsdottir, H.M. et al. (2003) The gene encoding phosphodiesterase 4D confers risk of ischemic stroke. Nat. Genet., 35, 131-138.
49. Higgins, J.P. and Thompson, S.G. (2002) Quantifying heterogeneity in a meta-analysis. Stat. Med., 21, 1539-1558.
50. Cortessis, V.K., Yuan, J.M., Van Den, B.D., Jiang, X., Gago-Dominguez, M., Stern, M.C., Castelao, J.E., Xiang, Y.B., Gao, Y.T., Pike, M.C. and Conti, D.V. (2010) Risk of urinary bladder cancer is associated with 8q24 variant rs9642880[T] in multiple racial/ethnic groups: results from the Los Angeles-Shanghai case-control study. Cancer Epidemiol. Biomarkers Prev., 19, 3150-3156.
51. Wang, M., Wang, M., Zhang, W., Yuan, L., Fu, G., Wei, Q. and Zhang, Z. (2009) Common genetic variants on 8q24 contribute to susceptibility to bladder cancer in a Chinese population. Carcinogenesis, 30, 991-996.
52. Rafnar, T., Sulem, P., Stacey, S.N., Geller, F., Gudmundsson, J., Sigurdsson, A., Jakobsdottir, M., Helgadottir, H., Thorlacius, S., Aben, K.K. et al. (2009) Sequence variants at the TERT-CLPTM1L locus associate with many cancer types. Nat. Genet., 41, 221-227.
53. Gago-Dominguez, M., Jiang, X., Conti, D.V., Castelao, J.E., Stern, M.C., Cortessis, V.K., Pike, M.C., Xiang, Y.B., Gao, Y.T., Yuan, J.M. and Van Den Berg, D.J. (2011) Genetic variations on chromosomes 5p15 and 15q25 and bladder cancer risk: findings from the Los Angeles-Shanghai bladder case-control study. Carcinogenesis, 32, 197-202.
54. Wang, S., Tang, J., Wang, M., Yuan, L. and Zhang, Z. (2010) Genetic variation in PSCA and bladder cancer susceptibility in a Chinese population. Carcinogenesis, 31, 621-624.
55. Wang, M., Chu, H., Yan, F., Qin, C., Li, P., Yuan, L., Yin, C., Xu, J. and Zhang, Z. (2011) Chromosome 4p16.3 variant modify bladder cancer risk in a Chinese population. Carcinogenesis, 32, 872-875.