Natural selection in a bangladeshi population from the cholera-endemic ganges river delta

Science Translational Medicine

Volumn 5, Issue 192, 2013, Pages

  Karlsson, Elinor K ^a,b   Harris, Jason B ^c,d   Tabrizi, Shervin ^a,b   Rahman, Atiqur ^c,e,g   Shlyakhter, Ilya ^a,b   Patterson, Nick ^b   O'Dushlaine, Colm ^b   Schaffner, Stephen F ^b,f   Gupta, Sameer ^d   Chowdhury, Fahima ^e   Sheikh, Alaullah ^e,h   Shin, Ok Sarah ^c,i   Ellis, Crystal ^c   Becker, Christine E ^c   Stuart, Lynda M ^b,c   Calderwood, Stephen B ^c,d   Ryan, Edward T ^c,d,f   Qadri, Firdausi ^e   Sabeti, Pardis C ^a,b,f   LaRocque, Regina C ^c,d  

^a HARVARD UNIVERSITY   (United States)

^b BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e INTERNATIONAL CENTRE FOR DIARRHOEAL DISEASE RESEARCH   (Bangladesh)

^f HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^g UNIVERSITY OF DHAKA   (Bangladesh)

^h WASHINGTON UNIVERSITY   (United States)

ⁱ Korea University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ACTIVATED POTASSIUM CHANNEL; CHLORIDE; CYCLIC AMP; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; POTASSIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL;

ADULT; ANIMAL CELL; ARTICLE; BANGLADESH; BANGLADESHI; CHILD; CHOLERA; CONTROLLED STUDY; ENDEMIC DISEASE; ETHNIC GROUP; FEMALE; GENE; GENETIC ANALYSIS; GENETIC DISTANCE; GENETIC SELECTION; HEREDITY; HUMAN; IN VITRO STUDY; INFECTION RESISTANCE; INFECTION SENSITIVITY; INNATE IMMUNITY; MAJOR CLINICAL STUDY; MALE; MOUSE; NATURAL SELECTION; NONHUMAN; POPULATION GENETICS; POTASSIUM CHANNEL GENE; PRIORITY JOURNAL; RIVER; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; VIBRIO CHOLERAE;

CHOLERA; GENETIC PREDISPOSITION TO DISEASE; HUMANS; INFLAMMASOMES; NF-KAPPA B; RIVERS; SELECTION, GENETIC; VIBRIO CHOLERAE;

EID: 84880540798     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006338     Document Type: Article

References (88)

1. K. Lee, The global dimensions of cholera. Global Change Hum. Health 2, 6-17 (2001).
2. F. Chowdhury, M. A. Rahman, Y. A. Begum, A. I. Khan, A. S. Faruque, N. C. Saha, N. I. Baby, M. A. Malek, A. R. Kumar, A. M. Svennerholm, M. Pietroni, A. Cravioto, F. Qadri, Impact of rapid urbanization on the rates of infection by Vibrio cholerae O1 and enterotoxigenic Escherichia coli in Dhaka, Bangladesh. PLoS Negl. Trop. Dis. 5, e999 (2011).
3. W. H. Mosley, W. M. McCormack, A. Ahmed, A. K. Chowdhury, R. K. Barui, Report of the 1966-67 cholera vaccine field trial in rural East Pakistan. 2. Results of the serological surveys in the study population - The relationship of case rate to antibody titre and an estimate of the inapparent infection rate with Vibrio cholerae. Bull. World Health Organ. 40, 187-197 (1969).
4. R. I. Glass, A. M. Svennerholm, M. R. Khan, S. Huda, M. I. Huq, J. Holmgren, Seroepidemiological studies of El Tor cholera in Bangladesh: Association of serum antibody levels with protection. J. Infect. Dis. 151, 236-242 (1985).
5. J. B. Harris, R. C. Larocque, R. C. Charles, R. N. Mazumder, A. I. Khan, P. K. Bardhan, Cholera's western front. Lancet 376, 1961-1965 (2010).
6. D. A. Sack, R. B. Sack, G. B. Nair, A. K. Siddique, Cholera. Lancet 363, 223-233 (2004).
7. J. B. Harris, R. C. LaRocque, F. Qadri, E. T. Ryan, S. B. Calderwood, Cholera. Lancet 379, 2466-2476 (2012).
8. J. B. Harris, R. C. LaRocque, F. Chowdhury, A. I. Khan, T. Logvinenko, A. S. Faruque, E. T. Ryan, F. Qadri, S. B. Calderwood, Susceptibility to Vibrio cholerae infection in a cohort of household contacts of patients with cholera in Bangladesh. PLoS Negl. Trop. Dis. 2, e221 (2008).
9. D. Barua, A. S. Paguio, ABO blood groups and cholera. Ann. Hum. Biol. 4, 489-492 (1977).
10. J. Fellay, K. V. Shianna, D. Ge, S. Colombo, B. Ledergerber, M. Weale, K. Zhang, C. Gumbs, A. Castagna, A. Cossarizza, A. Cozzi-Lepri, A. De Luca, P. Easterbrook, P. Francioli, S. Mallal, J. Martinez-Picado, J. M. Miro, N. Obel, J. P. Smith, J. Wyniger, P. Descombes, S. E. Antonarakis, N. L. Letvin, A. J. McMichael, B. F. Haynes, A. Telenti, D. B. Goldstein, A whole-genome association study of major determinants for host control of HIV-1. Science 317, 944-947 (2007).
11. D. L. Thomas, C. L. Thio, M. P. Martin, Y. Qi, D. Ge, C. O'Huigin, J. Kidd, K. Kidd, S. I. Khakoo, G. Alexander, J. J. Goedert, G. D. Kirk, S. M. Donfield, H. R. Rosen, L. H. Tobler, M. P. Busch, J. G. McHutchison, D. B. Goldstein, M. Carrington, Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461, 798-801 (2009).
12. Y. Tanaka, N. Nishida, M. Sugiyama, M. Kurosaki, K. Matsuura, N. Sakamoto, M. Nakagawa, M. Korenaga, K. Hino, S. Hige, Y. Ito, E. Mita, E. Tanaka, S. Mochida, Y. Murawaki, M. Honda, A. Sakai, Y. Hiasa, S. Nishiguchi, A. Koike, I. Sakaida, M. Imamura, K. Ito, K. Yano, N. Masaki, F. Sugauchi, N. Izumi, K. Tokunaga, M. Mizokami, Genome-wide association of IL28B with response to pegylated interferon-a and ribavirin therapy for chronic hepatitis C. Nat. Genet. 41, 1105-1109 (2009).
13. P. C. Sabeti, P. Varilly, B. Fry, J. Lohmueller, E. Hostetter, C. Cotsapas, X. Xie, E. H. Byrne, S. A. McCarroll, R. Gaudet, S. F. Schaffner, E. S. Lander; International HapMap Consortium; K. A. Frazer, D. G. Ballinger, D. R. Cox, D. A. Hinds, L. L. Stuve, R. A. Gibbs, J. W. Belmont, A. Boudreau, P. Hardenbol, S. M. Leal, S. Pasternak, D. A. Wheeler, T. D. Willis, F. Yu, H. Yang, C. Zeng, Y. Gao, H. Hu, W. Hu, C. Li, W. Lin, S. Liu, H. Pan, X. Tang, J. Wang, W. Wang, J. Yu, B. Zhang, Q. Zhang, H. Zhao, H. Zhao, J. Zhou, S. B. Gabriel, R. Barry, B. Blumenstiel, A. Camargo, M. Defelice, M. Faggart,M. Goyette, S. Gupta, J. Moore, H. Nguyen, R. C. Onofrio,M. Parkin, J. Roy, E. Stahl, E. Winchester, L. Ziaugra, D. Altshuler, Y. Shen, Z. Yao, W. Huang, X. Chu, Y. He, L. Jin, Y. Liu, Y. Shen, W. Sun, H. Wang, Y. Wang, Y.Wang, X. Xiong, L. Xu, M. M. Waye, S. K. Tsui, H. Xue, J. T. Wong, L. M. Galver, J. B. Fan, K. Gunderson, S. S. Murray, A. R.Oliphant, M. S. Chee, A. Montpetit, F. Chagnon, V. Ferretti, M. Leboeuf, J. F. Olivier, M. S. Phillips, S. Roumy, C. Sallée, A. Verner, T. J.Hudson, P. Y. Kwok, D. Cai,D. C. Koboldt, R.D. Miller, L. Pawlikowska, P. Taillon-Miller, M. Xiao, L. C. Tsui, W. Mak, Y. Q. Song, P. K. Tam, Y. Nakamura, T. Kawaguchi, T. Kitamoto, T. Morizono, A. Nagashima, Y. Ohnishi, A. Sekine, T. Tanaka, T. Tsunoda, P. Deloukas, C. P. Bird, M.Delgado, E. T. Dermitzakis, R. Gwilliam, S. Hunt, J. Morrison, D. Powell, B. E. Stranger, P. Whittaker, D. R. Bentley, M. J. Daly, P. I. de Bakker, J. Barrett, Y. R. Chretien, J. Maller, S. McCarroll, N. Patterson, I. Pe'er, A. Price, S. Purcell, D. J. Richter, P. Sabeti, R. Saxena, S. F. Schaffner, P. C. Sham, P. Varilly, D. Altshuler, L. D. Stein, L. Krishnan, A. V. Smith, M. K. Tello-Ruiz, G. A. Thorisson, A. Chakravarti, P. E. Chen, D. J. Cutler, C. S. Kashuk, S. Lin, G. R. Abecasis, W.Guan, Y. Li, H.M.Munro, Z. S. Qin, D. J. Thomas, G. McVean, A. Auton, L. Bottolo, N. Cardin, S. Eyheramendy, C. Freeman, J. Marchini, S. Myers, C. Spencer, M. Stephens, P. Donnelly, L. R. Cardon, G. Clarke, D. M. Evans, A. P. Morris, B. S. Weir, T. Tsunoda, T. A. Johnson, J. C. Mullikin, S. T. Sherry, M. Feolo, A. Skol, H. Zhang, C. Zeng, H. Zhao, I. Matsuda, Y. Fukushima, D. R. Macer, E. Suda, C. N. Rotimi, C. A. Adebamowo, I. Ajayi, T. Aniagwu, P. A. Marshall, C. Nkwodimmah, C. D. Royal, M. F. Leppert, M. Dixon, A. Peiffer, R. Qiu, A. Kent, K. Kato, N. Niikawa, I. F. Adewole, B. M. Knoppers, M. W. Foster, E.W. Clayton, J. Watkin, R. A. Gibbs, J. W. Belmont, D. Muzny, L. Nazareth, E. Sodergren, G. M. Weinstock, D. A. Wheeler, I. Yakub, S. B. Gabriel, R. C. Onofrio, D. J. Richter, L. Ziaugra, B. W. Birren, M. J. Daly, D. Altshuler, R. K. Wilson, L. L. Fulton, J. Rogers, J. Burton, N. P. Carter, C. M. Clee, M. Griffiths, M. C. Jones, K. McLay, R. W. Plumb, M. T. Ross, S. K. Sims, D. L. Willey, Z. Chen, H. Han, L. Kang, M. Godbout, J. C. Wallenburg, P. L'Archevêque, G. Bellemare, K. Saeki, H.Wang,D.An, H. Fu, Q. Li, Z.Wang, R. Wang, A. L. Holden, L. D. Brooks, J. E. McEwen, M. S. Guyer, V. O. Wang, J. L. Peterson, M. Shi, J. Spiegel, L. M. Sung, L. F. Zacharia, F. S. Collins, K. Kennedy, R. Jamieson, J. Stewart, Genome-wide detection and characterization of positive selection in human populations. Nature 449, 913-918 (2007).
14. D. J. Park, A. K. Lukens, D. E. Neafsey, S. F. Schaffner, H. H. Chang, C. Valim, U. Ribacke, D. Van Tyne, K. Galinsky, M. Galligan, J. S. Becker, D. Ndiaye, S. Mboup, R. C. Wiegand, D. L. Hartl, P. C. Sabeti, D. F.Wirth, S. K. Volkman, Sequence-based association and selection scans identify drug resistance loci in the Plasmodium falciparum malaria parasite. Proc. Natl. Acad. Sci. U.S.A. 109, 13052-13057 (2012).
15. H. Schwarzenbacher, M. Dolezal, K. Flisikowski, F. Seefried, C. Wurmser, C. Schlötterer, R. Fries, Combining evidence of selection with association analysis increases power to detect regions influencing complex traits in dairy cattle. BMC Genomics 13, 48 (2012).
16. J. S. Matson, J. H. Withey, V. J. DiRita, Regulatory networks controlling Vibrio cholerae virulence gene expression. Infect. Immun. 75, 5542-5549 (2007).
17. J. F. Heidelberg, J. A. Eisen, W. C. Nelson, R. A. Clayton, M. L. Gwinn, R. J. Dodson, D. H. Haft, E. K. Hickey, J. D. Peterson, L. Umayam, S. R. Gill, K. E. Nelson, T. D. Read, H. Tettelin, D. Richardson, M. D. Ermolaeva, J. Vamathevan, S. Bass, H. Qin, I. Dragoi, P. Sellers, L. McDonald, T. Utterback, R. D. Fleishmann, W. C. Nierman, O. White, S. L. Salzberg, H. O. Smith, R. R. Colwell, J. J. Mekalanos, J. C. Venter, C. M. Fraser, DNA sequence of both chromosomes of the cholera pathogen Vibrio cholerae. Nature 406, 477-483 (2000).
18. S. M. Faruque, J. J. Mekalanos, Pathogenicity islands and phages in Vibrio cholerae evolution. Trends Microbiol. 11, 505-510 (2003).
19. J. J. Mekalanos, E. J. Rubin, M. K. Waldor, Cholera: Molecular basis for emergence and pathogenesis. FEMS Immunol. Med. Microbiol. 18, 241-248 (1997).
20. E. J. Nelson, J. B. Harris, J. G. Morris Jr., S. B. Calderwood, A. Camilli, Cholera transmission: The host, pathogen and bacteriophage dynamic. Nat. Rev. Microbiol. 7, 693-702 (2009).
21. D. Cassel, T. Pfeuffer, Mechanism of cholera toxin action: Covalent modification of the guanyl nucleotide-binding protein of the adenylate cyclase system. Proc. Natl. Acad. Sci. U.S.A. 75, 2669-2673 (1978).
22. D. M. Gill, R. Meren, ADP-ribosylation of membrane proteins catalyzed by cholera toxin: Basis of the activation of adenylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 75, 3050-3054 (1978).
23. S. R. Grossman, I. Shlyakhter, E. K. Karlsson, E. H. Byrne, S. Morales, G. Frieden, E. Hostetter, E. Angelino, M.Garber,O. Zuk, E. S. Lander, S. F. Schaffner, P. C. Sabeti, A composite ofmultiple signals distinguishes causal variants in regions of positive selection. Science 327, 883-886 (2010).
24. S. R. Grossman, K. G. Andersen, I. Shlyakhter, S. Tabrizi, S. Winnicki, A. Yen, D. J. Park, D. Griesemer, E. K. Karlsson, S. H. Wong, M. Cabili, R. A. Adegbola, R. N. Bamezai, A. V. Hill, F. O. Vannberg, J. L. Rinn; 1000 Genomes Project, E. S. Lander, S. F. Schaffner, P. C. Sabeti, Identifying recent adaptations in large-scale genomic data. Cell 152, 703-713 (2013).
25. International HapMap Consortium; K. A. Frazer, D. G. Ballinger, D. R. Cox, D. A. Hinds, L. L. Stuve, R. A. Gibbs, J. W. Belmont, A. Boudreau, P. Hardenbol, S. M. Leal, S. Pasternak, D. A. Wheeler, T. D. Willis, F. Yu, H. Yang, C. Zeng, Y. Gao, H. Hu, W. Hu, C. Li, W. Lin, S. Liu, H. Pan, X. Tang, J. Wang, W. Wang, J. Yu, B. Zhang, Q. Zhang, H. Zhao, H. Zhao, J. Zhou, S. B. Gabriel, R. Barry, B. Blumenstiel, A. Camargo, M. Defelice, M. Faggart, M. Goyette, S. Gupta, J. Moore, H. Nguyen, R. C. Onofrio, M. Parkin, J. Roy, E. Stahl, E. Winchester, L. Ziaugra, D. Altshuler, Y. Shen, Z. Yao, W. Huang, X. Chu, Y. He, L. Jin, Y. Liu, Y. Shen, W. Sun, H. Wang, Y. Wang, Y. Wang, X. Xiong, L. Xu, M. M. Waye, S. K. Tsui, H. Xue, J. T. Wong, L. M. Galver, J. B. Fan, K. Gunderson, S. S.Murray, A. R. Oliphant, M. S. Chee, A. Montpetit, F. Chagnon, V. Ferretti, M. Leboeuf, J. F. Olivier, M. S. Phillips, S. Roumy, C. Sallée, A. Verner, T. J. Hudson, P. Y. Kwok, D. Cai, D. C. Koboldt, R. D. Miller, L. Pawlikowska, P. Taillon-Miller, M. Xiao, L. C. Tsui, W. Mak, Y. Q. Song, P. K. Tam, Y. Nakamura, T. Kawaguchi, T. Kitamoto, T. Morizono, A. Nagashima, Y. Ohnishi, A. Sekine, T. Tanaka, T. Tsunoda, P. Deloukas, C. P. Bird, M. Delgado, E. T. Dermitzakis, R. Gwilliam, S. Hunt, J. Morrison,D. Powell, B. E. Stranger, P.Whittaker,D. R. Bentley,M. J.Daly, P. I. de Bakker, J. Barrett, Y. R. Chretien, J. Maller, S. McCarroll, N. Patterson, I. Pe'er, A. Price, S. Purcell, D. J. Richter, P. Sabeti, R. Saxena, S. F. Schaffner, P. C. Sham, P. Varilly, D. Altshuler, L. D. Stein, L. Krishnan, A. V. Smith, M. K. Tello-Ruiz, G. A. Thorisson, A. Chakravarti, P. E. Chen, D. J. Cutler, C. S. Kashuk, S. Lin, G. R. Abecasis,W. Guan, Y. Li, H.M.Munro, Z. S. Qin, D. J. Thomas, G. McVean, A. Auton, L. Bottolo, N. Cardin, S. Eyheramendy, C. Freeman, J. Marchini, S. Myers, C. Spencer, M. Stephens, P. Donnelly, L. R. Cardon, G. Clarke, D. M. Evans, A. P. Morris, B. S. Weir, T. Tsunoda, J. C. Mullikin, S. T. Sherry, M. Feolo, A. Skol, H. Zhang, C. Zeng, H. Zhao, I. Matsuda, Y. Fukushima, D. R. Macer, E. Suda, C. N. Rotimi, C. A. Adebamowo, I. Ajayi, T. Aniagwu, P. A. Marshall, C. Nkwodimmah, C. D. Royal, M. F. Leppert, M. Dixon, A. Peiffer, R. Qiu, A. Kent, K. Kato, N. Niikawa, I. F. Adewole, B. M. Knoppers, M. W. Foster, E. W. Clayton, J. Watkin, R. A. Gibbs, J. W. Belmont, D. Muzny, L. Nazareth, E. Sodergren, G. M.Weinstock, D. A.Wheeler, I. Yakub, S. B. Gabriel, R. C. Onofrio, D. J. Richter, L. Ziaugra, B. W. Birren, M. J. Daly, D. Altshuler, R. K. Wilson, L. L. Fulton, J. Rogers, J. Burton, N. P. Carter, C. M. Clee, M. Griffiths, M. C. Jones, K. McLay, R. W. Plumb, M. T. Ross, S. K. Sims, D. L. Willey, Z. Chen, H. Han, L. Kang,M. Godbout, J. C.Wallenburg, P. L'Archevêque, G. Bellemare, K. Saeki, H.Wang, D. An, H. Fu, Q. Li, Z. Wang, R.Wang, A. L. Holden, L. D. Brooks, J. E.McEwen, M. S. Guyer, V. O.Wang, J. L. Peterson, M. Shi, J. Spiegel, L. M. Sung, L. F. Zacharia, F. S. Collins, K. Kennedy, R. Jamieson, J. Stewart, A second generation human haplotype map of over 3.1 million SNPs. Nature 449, 851-861 (2007).
26. J. Z. Li, D. M. Absher, H. Tang, A. M. Southwick, A. M. Casto, S. Ramachandran, H. M. Cann, G. S. Barsh, M. Feldman, L. L. Cavalli-Sforza, R. M. Myers, Worldwide human relationships inferred from genome-wide patterns of variation. Science 319, 1100-1104 (2008).
27. Y. Y. Teo, X. Sim, R. T. Ong, A. K. Tan, J. Chen, E. Tantoso, K. S. Small, C. S. Ku, E. J. Lee,M. Seielstad, K. S. Chia, Singapore Genome Variation Project: A haplotype map of three Southeast Asian populations. Genome Res. 19, 2154-2162 (2009).
28. D. Reich, K. Thangaraj, N. Patterson, A. L. Price, L. Singh, Reconstructing Indian population history. Nature 461, 489-494 (2009).
29. J. N. Fenner, Cross-cultural estimation of the human generation interval for use in geneticsbased population divergence studies. Am. J. Phys. Anthropol. 128, 415-423 (2005).
30. P. Moorjani, N. Patterson, J. N. Hirschhorn, A. Keinan, L. Hao, G. Atzmon, E. Burns, H. Ostrer, A. L. Price, D. Reich, The history of African gene flow into Southern Europeans, Levantines, and Jews. PLoS Genet. 7, e1001373 (2011).
31. N. Patterson, P. Moorjani, Y. Luo, S. Mallick, N. Rohland, Y. Zhan, T. Genschoreck, T. Webster, D. Reich, Ancient admixture in human history. Genetics 192, 1065-1093 (2012).
32. D. H. Alexander, J. Novembre, K. Lange, Fast model-based estimation of ancestry in unrelated individuals. Genome Res. 19, 1655-1664 (2009).
33. -1000 Genomes Project Consortium; G. R. Abecasis, D. Altshuler, A. Auton, L. D. Brooks, R.M. Durbin, R. A. Gibbs, M. E. Hurles, G. A.McVean, Amap of human genome variation from population-scale sequencing. Nature 467, 1061-1073 (2010).
34. Psychiatric GWAS Consortium Bipolar Disorder Working Group, Large-scale genome-wide association analysis of bipolar disorder identifies a new susceptibility locus near ODZ4. Nat. Genet. 43, 977-983 (2011).
35. P. H. Lee, C. O'Dushlaine, B. Thomas, S. M. Purcell, INRICH: Interval-based enrichment analysis for genome-wide association studies. Bioinformatics 28, 1797-1799 (2012).
36. A. Subramanian, P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R. Golub, E. S. Lander, J. P. Mesirov, Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550 (2005).
37. M. A. Harris, J. Clark, A. Ireland, J. Lomax, M. Ashburner, R. Foulger, K. Eilbeck, S. Lewis, B. Marshall, C. Mungall, J. Richter, G. M. Rubin, J. A. Blake, C. Bult, M. Dolan, H. Drabkin, J. T. Eppig, D. P. Hill, L. Ni, M. Ringwald, R. Balakrishnan, J. M. Cherry, K. R. Christie, M. C. Costanzo, S. S. Dwight, S. Engel, D. G. Fisk, J. E. Hirschman, E. L. Hong, R. S. Nash, A. Sethuraman, C. L. Theesfeld, D. Botstein, K. Dolinski, B. Feierbach, T. Berardini, S. Mundodi, S. Y. Rhee, R. Apweiler, D. Barrell, E. Camon, E. Dimmer, V. Lee, R. Chisholm, P. Gaudet, W. Kibbe, R. Kishore, E. M. Schwarz, P. Sternberg, M. Gwinn, L. Hannick, J. Wortman, M. Berriman, V. Wood, N. de la Cruz, P. Tonellato, P. Jaiswal, T. Seigfried, R. White; Gene Ontology Consortium, The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res. 32, D258-D261 (2004).
38. D. Heitzmann, R. Warth, Physiology and pathophysiology of potassium channels in gastrointestinal epithelia. Physiol. Rev. 88, 1119-1182 (2008).
39. D. Saha, R. C. LaRocque, A. I. Khan, J. B. Harris, Y. A. Begum, S. M. Akramuzzaman, A. S. Faruque, E. T. Ryan, F. Qadri, S. B. Calderwood, Incomplete correlation of serum vibriocidal antibody titer with protection from Vibrio cholerae infection in urban Bangladesh. J. Infect. Dis. 189, 2318-2322 (2004).
40. S. Purcell, B. Neale, K. Todd-Brown, L. Thomas, M. A. Ferreira, D. Bender, J. Maller, P. Sklar, P. I. de Bakker, M. J. Daly, P. C. Sham, PLINK: A tool set for whole-genome association and population-based linkage analyses. Am. J. Hum. Genet. 81, 559-575 (2007).
41. R. S. Spielman, R. E. McGinnis, W. J. Ewens, Transmission test for linkage disequilibrium: The insulin gene region and insulin-dependent diabetes mellitus (IDDM). Am. J. Hum. Genet. 52, 506-516 (1993).
42. J. C. Barrett, B. Fry, J. Maller, M. J. Daly, Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21, 263-265 (2005).
43. O. S. Shin, T. Uddin, R. Citorik, J. P. Wang, P. Della Pelle, R. L. Kradin, C. D. Bingle, L. Bingle, A. Camilli, T. R. Bhuiyan, T. Shirin, E. T. Ryan, S. B. Calderwood, R. W. Finberg, F. Qadri, R. C. Larocque, J. B. Harris, LPLUNC1 modulates innate immune responses to Vibrio cholerae. J. Infect. Dis. 204, 1349-1357 (2011).
44. A. Thanawastien, W. R. Montor, J. Labaer, J. J. Mekalanos, S. S. Yoon, Vibrio cholerae proteomewide screen for immunostimulatory proteins identifies phosphatidylserine decarboxylase as a novel Toll-like receptor 4 agonist. PLoS Pathog. 5, e1000556 (2009).
45. Ingenuity Systems, IPA; http://www.ingenuity.com.
46. V. A. Rathinam, S. K. Vanaja, L. Waggoner, A. Sokolovska, C. Becker, L. M. Stuart, J. M. Leong, K. A. Fitzgerald, TRIF licenses caspase-11-dependent NLRP3 inflammasome activation by Gram-negative bacteria. Cell 150, 606-619 (2012).
47. N. Kayagaki, S. Warming, M. Lamkanfi, L. Vande Walle, S. Louie, J. Dong, K. Newton, Y. Qu, J. Liu, S. Heldens, J. Zhang, W. P. Lee, M. Roose-Girma, V. M. Dixit, Non-canonical inflammasome activation targets caspase-11. Nature 479, 117-121 (2011).
48. M. S. Hayden, S. Ghosh, NF-kB, the first quarter-century: Remarkable progress and outstanding questions. Genes Dev. 26, 203-234 (2012).
49. S. Xu, H. Bayat, X. Hou, B. Jiang, Ribosomal S6 kinase-1 modulates interleukin-1b-induced persistent activation of NF-kB through phosphorylation of IkBb. Am. J. Physiol. Cell Physiol. 291, C1336-C1345 (2006).
50. R. M. Ewing, P. Chu, F. Elisma, H. Li, P. Taylor, S. Climie, L. McBroom-Cerajewski, M. D. Robinson, L. O'Connor, M. Li, R. Taylor, M. Dharsee, Y. Ho, A. Heilbut, L. Moore, S. Zhang, O. Ornatsky, Y. V. Bukhman, M. Ethier, Y. Sheng, J. Vasilescu, M. Abu-Farha, J. P. Lambert, H. S. Duewel, I. I. Stewart, B. Kuehl, K. Hogue, K. Colwill, K. Gladwish, B. Muskat, R. Kinach, S. L. Adams, M. F. Moran, G. B. Morin, T. Topaloglou, D. Figeys, Large-scale mapping of human protein- protein interactions by mass spectrometry. Mol. Syst. Biol. 3, 89 (2007).
51. C. F. Flach, F. Qadri, T. R. Bhuiyan, N. H. Alam, E. Jennische, I. Lönnroth, J. Holmgren, Broad up-regulation of innate defense factors during acute cholera. Infect. Immun. 75, 2343-2350 (2007).
52. C. D. Berkey, N. Blow, P. I. Watnick, Genetic analysis of Drosophila melanogaster susceptibility to intestinal Vibrio cholerae infection. Cell. Microbiol. 11, 461-474 (2009).
53. Z. Wang, C. D. Berkey, P. I. Watnick, The Drosophila protein mustard tailors the innate immune response activated by the immune deficiency pathway. J. Immunol. 188, 3993-4000 (2012).
54. M. M. Rahman, G. McFadden, Modulation of NF-kB signalling by microbial pathogens. Nat. Rev. Microbiol. 9, 291-306 (2011).
55. S. J. Chapman, C. C. Khor, F. O. Vannberg, A. Rautanen, S. Segal, C. E. Moore, R. J. Davies, N. P. Day, N. Peshu, D. W. Crook, J. A. Berkley, T. N. Williams, J. A. Scott, A. V. Hill, NFKBIZ polymorphisms and susceptibility to pneumococcal disease in European and African populations. Genes Immun. 11, 319-325 (2010).
56. S. J. Chapman, C. C. Khor, F. O. Vannberg, A. Rautanen, A. Walley, S. Segal, C. E. Moore, R. J. Davies, N. P. Day, N. Peshu, D. W. Crook, J. A. Berkley, T. N. Williams, J. A. Scott, A. V. Hill, Common NFKBIL2 polymorphisms and susceptibility to pneumococcal disease: A genetic association study. Crit. Care 14, R227 (2010).
57. S. J. Chapman, C. C. Khor, F. O. Vannberg, A. Frodsham, A. Walley, N. A. Maskell, C. W. Davies, S. Segal, C. E. Moore, S. H. Gillespie, P. Denny, N. P. Day, D. W. Crook, R. J. Davies, A. V. Hill, IkB genetic polymorphisms and invasive pneumococcal disease. Am. J. Respir. Crit. Care Med. 176, 181-187 (2007).
58. P. D. Smith, L. E. Smythies, R. Shen, T. Greenwell-Wild, M. Gliozzi, S. M. Wahl, Intestinal macrophages and response to microbial encroachment. Mucosal Immunol. 4, 31-42 (2011).
59. A. Nenci, C. Becker, A. Wullaert, R. Gareus, G. van Loo, S. Danese, M. Huth, A. Nikolaev, C. Neufert, B. Madison, D. Gumucio, M. F. Neurath, M. Pasparakis, Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 446, 557-561 (2007).
60. C. A. Anderson, G. Boucher, C. W. Lees, A. Franke, M. D'Amato, K. D. Taylor, J. C. Lee, P. Goyette, M. Imielinski, A. Latiano, C. Lagacé, R. Scott, L. Amininejad, S. Bumpstead, L. Baidoo, R. N. Baldassano, M. Barclay, T. M. Bayless, S. Brand, C. Büning, J. F. Colombel, L. A. Denson, M. De Vos, M. Dubinsky, C. Edwards, D. Ellinghaus, R. S. Fehrmann, J. A. Floyd, T. Florin, D. Franchimont, L. Franke, M. Georges, J. Glas, N. L. Glazer, S. L. Guthery, T. Haritunians, N. K. Hayward, J. P. Hugot, G. Jobin, D. Laukens, I. Lawrance, M. Lémann, A. Levine, C. Libioulle, E. Louis, D. P.McGovern, M. Milla, G. W. Montgomery, K. I. Morley, C. Mowat, A. Ng, W. Newman, R. A. Ophoff, L. Papi, O. Palmieri, L. Peyrin-Biroulet, J. Panés, A. Phillips, N. J. Prescott, D. D. Proctor, R. Roberts, R. Russell, P. Rutgeerts, J. Sanderson, M. Sans, P. Schumm, F. Seibold, Y. Sharma, L. A. Simms, M. Seielstad, A. H. Steinhart, S. R. Targan, L. H. van den Berg, M. Vatn, H. Verspaget, T. Walters, C. Wijmenga, D. C. Wilson, H. J. Westra, R. J. Xavier, Z. Z. Zhao, C. Y. Ponsioen, V. Andersen, L. Torkvist, M. Gazouli, N. P. Anagnou, T. H. Karlsen, L. Kupcinskas, J. Sventoraityte, J. C. Mansfield, S. Kugathasan, M. S. Silverberg, J. Halfvarson, J. I. Rotter, C. G. Mathew, A. M. Griffiths, R. Gearry, T. Ahmad, S. R. Brant, M. Chamaillard, J. Satsangi, J. H. Cho, S. Schreiber, M. J. Daly, J. C. Barrett, M. Parkes, V. Annese, H. Hakonarson, G. Radford-Smith, R. H. Duerr, S. Vermeire, R. K. Weersma, J. D. Rioux, Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat. Genet. 43, 246-252 (2011).
61. V. Pinsk, D. A. Lemberg, K. Grewal, C. C. Barker, R. A. Schreiber, K. Jacobson, Inflammatory bowel disease in the South Asian pediatric population of British Columbia. Am. J. Gastroenterol. 102, 1077-1083 (2007).
62. I. Carr, J. F. Mayberry, The effects of migration on ulcerative colitis: A three-year prospective study among Europeans and first- and second-generation South Asians in Leicester (1991-1994). Am. J. Gastroenterol. 94, 2918-2922 (1999).
63. P. S. Baxter, J. Goldhill, J. Hardcastle, P. T. Hardcastle, C. J. Taylor, Accounting for cystic fibrosis. Nature 335, 211 (1988).
64. D. M. Rodman, S. Zamudio, The cystic fibrosis heterozygote - Advantage in surviving cholera? Med. Hypotheses 36, 253-258 (1991).
65. S. M. O'Grady, S. Y. Lee, Molecular diversity and function of voltage-gated (Kv) potassium channels in epithelial cells. Int. J. Biochem. Cell Biol. 37, 1578-1594 (2005).
66. K. Kunzelmann, M. Bleich, R. Warth, R. Levy-Holzman, H. Garty, R. Schreiber, Expression and function of colonic epithelial KVLQT1 K+ channels. Clin. Exp. Pharmacol. Physiol. 28, 79-83 (2001).
67. E. Lohrmann, I. Burhoff, R. B. Nitschke, H. J. Lang, D. Mania, H. C. Englert, M. Hropot, R. Warth, W. Rohm, M. Bleich, R. Greger, A new class of inhibitors of cAMP-mediated Cl - secretion in rabbit colon, acting by the reduction of cAMP-activated K+ conductance. Pflugers Arch. 429, 517-530 (1995).
68. V. Vallon, F. Grahammer, H. Volkl, C. D. Sandu, K. Richter, R. Rexhepaj, U. Gerlach, Q. Rong, K. Pfeifer, F. Lang, KCNQ1-dependent transport in renal and gastrointestinal epithelia. Proc. Natl. Acad. Sci. U.S.A. 102, 17864-17869 (2005).
69. L. J. MacVinish, M. E. Hickman, D. A. Mufti, H. J. Durrington, A. W. Cuthbert, Importance of basolateral K+ conductance in maintaining Cl- secretion in murine nasal and colonic epithelia. J. Physiol. 510 (Pt. 1), 237-247 (1998).
70. M. Mall, M. Bleich, M. Schürlein, J. Kühr, H. H. Seydewitz, M. Brandis, R. Greger, K. Kunzelmann, Cholinergic ion secretion in human colon requires coactivation by cAMP. Am. J. Physiol. 275, G1274-G1281 (1998).
71. L. H. Yih, K. Peck, T. C. Lee, Changes in gene expression profiles of human fibroblasts in response to sodium arsenite treatment. Carcinogenesis 23, 867-876 (2002).
72. A. Mukherjee, M. K. Sengupta, M. A. Hossain, S. Ahamed, B. Das, B. Nayak, D. Lodh, M.M. Rahman, D. Chakraborti, Arsenic contamination in groundwater: A global perspective with emphasis on the Asian scenario. J. Health Popul. Nutr. 24, 142-163 (2006).
73. Human Microbiome Project Consortium, Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214 (2012).
74. B. L. Browning, S. R. Browning, A unified approach to genotype imputation and haplotypephase inference for large data sets of trios and unrelated individuals. Am. J. Hum. Genet. 84, 210-223 (2009).
75. J. Yang, S. H. Lee, M. E. Goddard, P. M. Visscher, GCTA: A tool for genome-wide complex trait analysis. Am. J. Hum. Genet. 88, 76-82 (2011).
76. M. N. Cabili, C. Trapnell, L. Goff, M. Koziol, B. Tazon-Vega, A. Regev, J. L. Rinn, Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev. 25, 1915-1927 (2011).
77. D. Karolchik, A. S. Hinrichs, T. S. Furey, K. M. Roskin, C. W. Sugnet, D. Haussler, W. J. Kent, The UCSC Table Browser data retrieval tool. Nucleic Acids Res. 32, D493-D496 (2004).
78. K. D. Pruitt, T. Tatusova, G. R. Brown, D. R. Maglott, NCBI Reference Sequences (RefSeq): Current status, new features and genome annotation policy. Nucleic Acids Res. 40, D130-D135 (2012).
79. A. George-Chandy, K. Eriksson, M. Lebens, I. Nordström, E. Schön, J. Holmgren, Cholera toxin B subunit as a carrier molecule promotes antigen presentation and increases CD40 and CD86 expression on antigen-presenting cells. Infect. Immun. 69, 5716-5725 (2001).
80. M. C. Bourgeois-Daigneault, J. Thibodeau, Autoregulation of MARCH1 expression by dimerization and autoubiquitination. J. Immunol. 188, 4959-4970 (2012).
81. E. Goto, S. Ishido, Y. Sato, S. Ohgimoto, K. Ohgimoto, M. Nagano-Fujii, H. Hotta, c-MIR, a human E3 ubiquitin ligase, is a functional homolog of herpesvirus proteins MIR1 and MIR2 and has similar activity. J. Biol. Chem. 278, 14657-14668 (2003).
82. L. D. Roy, M. Sahraei, D. B. Subramani, D. Besmer, S. Nath, T. L. Tinder, E. Bajaj, K. Shanmugam, Y. Y. Lee, S. I. Hwang, S. J. Gendler, P. Mukherjee, MUC1 enhances invasiveness of pancreatic cancer cells by inducing epithelial to mesenchymal transition. Oncogene 30, 1449-1459 (2011).
83. B. J. Fenner, M. Scannell, J. H. Prehn, Expanding the substantial interactome of NEMO using protein microarrays. PLoS One 5, e8799 (2010).
84. T. Bouwmeester, A. Bauch, H. Ruffner, P. O. Angrand, G. Bergamini, K. Croughton, C. Cruciat, D. Eberhard, J. Gagneur, S. Ghidelli, C. Hopf, B. Huhse, R. Mangano, A. M. Michon, M. Schirle, J. Schlegl, M. Schwab, M. A. Stein, A. Bauer, G. Casari, G. Drewes, A. C. Gavin, D. B. Jackson, G. Joberty, G. Neubauer, J. Rick, B. Kuster, G. Superti-Furga, A physical and functional map of the human TNF-a/NF-kB signal transduction pathway. Nat. Cell Biol. 6, 97-105 (2004).
85. I. García-Arnandis, M. I. Guillén, F. Gomar, J. P. Pelletier, J. Martel-Pelletier, M. J. Alcaraz, High mobility group box 1 potentiates the pro-inflammatory effects of interleukin-1b in osteoarthritic synoviocytes. Arthritis Res. Ther. 12, R165 (2010).
86. M. Stefanidakis, M. Bjorklund, E. Ihanus, C. G. Gahmberg, E. Koivunen, Identification of a negatively charged peptide motif within the catalytic domain of progelatinases that mediates binding to leukocyte b2 integrins. J. Biol. Chem. 278, 34674-34684 (2003).
87. I. E. Dumitriu, P. Baruah, B. Valentinis, R. E. Voll, M. Herrmann, P. P. Nawroth, B. Arnold, M. E. Bianchi, A. A. Manfredi, P. Rovere-Querini, Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J. Immunol. 174, 7506-7515 (2005).
88. P. J. Popovic, R. DeMarco, M. T. Lotze, S. E. Winikoff, D. L. Bartlett, A. M. Krieg, Z. S. Guo, C. K. Brown, K. J. Tracey, H. J. Zeh III, High mobility group B1 protein suppresses the human plasmacytoid dendritic cell response to TLR9 agonists. J. Immunol. 177, 8701-8707 (2006).