Functional genetic screen of human diversity reveals that a methionine salvage enzyme regulates inflammatory cell death

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 35, 2012, Pages

  Ko, Dennis C ^a,c   Gamazon, Eric R ^b   Shukla, Kajal P ^a   Pfuetzner, Richard A ^a   Whittington, Dale ^a   Holden, Tarah D ^a   Brittnacher, Mitchell J ^a   Fong, Christine ^a   Radey, Matthew ^a   Ogohara, Cassandra ^a   Stark, Amy L ^b   Akey, Joshua M ^a   Dolan, M Eileen ^b   Wurfel, Mark M ^a   Miller, Samuel I ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

HapMap; Lymphoblastoid; Polygenic adaptation; Pyroptosis; Quantitative trait

Indexed keywords

5' METHYLTHIOADENOSINE; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; APOPTOTIC PROTEASE ACTIVATING FACTOR 1 INTERACTING PROTEIN; BINDING PROTEIN; CARBOPLATIN; CASPASE 9; HYDROLYASE; INTERLEUKIN 1BETA CONVERTING ENZYME; METHIONINE; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ANIMAL CELL; APOPTOSIS; ARTICLE; BACTERIAL GROWTH; CELL DEATH; CHEMOSENSITIVITY; CULTURE MEDIUM; ENZYME SUBSTRATE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC SCREENING; GENETIC SUSCEPTIBILITY; GENETIC TRAIT; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATORY CELL; METHIONINE SALVAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SURVIVAL; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BONE MARROW CELLS; CASPASE 1; CASPASE 9; DEOXYADENOSINES; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; HAPMAP PROJECT; HEK293 CELLS; HUMANS; METHIONINE; MICE; MICE, INBRED C57BL; MIDDLE AGED; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; THIONUCLEOSIDES; YOUNG ADULT;

SALMONELLA;

EID: 84865552982     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1206701109     Document Type: Article

References (80)

1. Vannberg FO, Chapman SJ, Hill AV (2011) Human genetic susceptibility to intracellular pathogens. Immunol Rev 240:105-116.
2. Wong SH, et al. (2010) Leprosy and the adaptation of human toll-like receptor 1. PLoS Pathog 6:e1000979.
3. Wong SH, Hill AV, Vannberg FO; India-Africa-United Kingdom Leprosy Genetics Consortium (2010) Genomewide association study of leprosy. N Engl J Med 362:1446-1447.
4. Zhang FR, et al. (2009) Genomewide association study of leprosy. N Engl J Med 361:2609-2618.
5. Fellay J, et al. (2007) A whole-genome association study of major determinants for host control of HIV-1. Science 317:944-947. (Pubitemid 47301321)
6. Shrestha S, et al. (2009) Host genetics and HIV-1 viral load set-point in African-Americans. AIDS 23:673-677.
7. Thye T, et al.; African TB Genetics Consortium; Wellcome Trust Case Control Consortium (2010) Genome-wide association analyses identifies a susceptibility locus for tuberculosis on chromosome 18q11.2. Nat Genet 42:739-741.
8. Davila S, et al.; International Meningococcal Genetics Consortium (2010) Genomewide association study identifies variants in the CFH region associated with host susceptibility to meningococcal disease. Nat Genet 42:772-776.
9. Bergsbaken T, Fink SL, Cookson BT (2009) Pyroptosis: Host cell death and inflammation. Nat Rev Microbiol 7:99-109.
10. Kuida K, et al. (1995) Altered cytokine export and apoptosis in mice deficient in interleukin-1 beta converting enzyme. Science 267:2000-2003.
11. Li P, et al. (1995) Mice deficient in IL-1 beta-converting enzyme are defective in production of mature IL-1 beta and resistant to endotoxic shock. Cell 80:401-411.
12. Villani AC, et al. (2009) Common variants in the NLRP3 region contribute to Crohn's disease susceptibility. Nat Genet 41:71-76.
13. Martinon F, Pétrilli V, Mayor A, Tardivel A, Tschopp J (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440:237-241.
14. Savic S, Dickie LJ, Battellino M, McDermott MF (2012) Familial Mediterranean fever and related periodic fever syndromes/autoinflammatory diseases. Curr Opin Rheumatol 24:103-112.
15. Lara-Tejero M, et al. (2006) Role of the caspase-1 inflammasome in Salmonella typhimurium pathogenesis. J Exp Med 203:1407-1412. (Pubitemid 43877602)
16. Mariathasan S, Weiss DS, Dixit VM, Monack DM (2005) Innate immunity against Francisella tularensis is dependent on the ASC/caspase-1 axis. J Exp Med 202:1043-1049. (Pubitemid 41464498)
17. Miao EA, et al. (2010) Caspase-1-induced pyroptosis is an innate immune effector mechanism against intracellular bacteria. Nat Immunol 11:1136-1142.
18. Ko DC, et al. (2009) A genome-wide in vitro bacterial-infection screen reveals human variation in the host response associated with inflammatory disease. Am J Hum Genet 85:214-227.
19. Huang RS, et al. (2007) A genome-wide approach to identify genetic variants that contribute to etoposide-induced cytotoxicity. Proc Natl Acad Sci USA 104:9758-9763. (Pubitemid 47175340)
20. Huang RS, Duan S, Kistner EO, Hartford CM, Dolan ME (2008) Genetic variants associated with carboplatin-induced cytotoxicity in cell lines derived from Africans. Mol Cancer Ther 7:3038-3046.
21. Loeuillet C, et al. (2008) In vitro whole-genome analysis identifies a susceptibility locus for HIV-1. PLoS Biol 6:e32.
22. Martchenko M, Candille SI, Tang H, Cohen SN (2012) Human genetic variation altering anthrax toxin sensitivity. Proc Natl Acad Sci USA 109:2972-2977.
23. Frazer KA, et al.; International HapMap Consortium (2007) A second generation human haplotype map of over 3.1 million SNPs. Nature 449:851-861.
24. Razmara M, et al. (2002) CARD-8 protein, a new CARD family member that regulates caspase-1 activation and apoptosis. J Biol Chem 277:13952-13958. (Pubitemid 34968002)
25. Fontalba A, et al. (2007) Deficiency of the NF-kappaB inhibitor caspase activating and recruitment domain 8 in patients with rheumatoid arthritis is associated with disease severity. J Immunol 179:4867-4873.
26. Gamazon ER, Huang RS, Cox NJ, Dolan ME (2010) Chemotherapeutic drug susceptibility associated SNPs are enriched in expression quantitative trait loci. Proc Natl Acad Sci USA 107:9287-9292.
27. Nica AC, et al. (2010) Candidate causal regulatory effects by integration of expression QTLs with complex trait genetic associations. PLoS Genet 6:e1000895.
28. Nicolae DL, et al. (2010) Trait-associated SNPs are more likely to be eQTLs: Annotation to enhance discovery from GWAS. PLoS Genet 6:e1000888.
29. Stranger BE, et al. (2007) Population genomics of human gene expression. Nat Genet 39:1217-1224. (Pubitemid 47482691)
30. Zeller T, et al. (2010) Genetics and beyond - the transcriptome of human monocytes and disease susceptibility. PLoS One 5:e10693.
31. Cho DH, et al. (2004) Induced inhibition of ischemic/hypoxic injury by APIP, a novel Apaf-1-interacting protein. J Biol Chem 279:39942-39950.
32. Huang RS, et al. (2011) Platinum sensitivity-related germline polymorphism discovered via a cell-based approach and analysis of its association with outcome in ovarian cancer patients. Clin Cancer Res 17:5490-5500.
33. Singh S, Chhipa RR, Vijayakumar MV, Bhat MK (2006) DNA damaging drugs-induced down-regulation of Bcl-2 is essential for induction of apoptosis in high-risk HPVpositive HEp-2 and KB cells. Cancer Lett 236:213-221. (Pubitemid 43732548)
34. Itoh M, Chiba H, Noutomi T, Takada E, Mizuguchi J (2000) Cleavage of Bax-alpha and Bcl-x(L) during carboplatin-mediated apoptosis in squamous cell carcinoma cell line. Oral Oncol 36:277- 285.
35. Voth DE, Howe D, Heinzen RA (2007) Coxiella burnetii inhibits apoptosis in human THP-1 cells and monkey primary alveolar macrophages. Infect Immun 75:4263-4271. (Pubitemid 47378082)
36. Cho DH, et al. (2007) Suppression of hypoxic cell death by APIP-induced sustained activation of AKT and ERK1/2. Oncogene 26:2809-2814.
37. Agostini L, et al. (2004) NALP3 forms an IL-1beta-processing inflammasome with increased activity in Muckle-Wells autoinflammatory disorder. Immunity 20:319-325. (Pubitemid 38388233)
38. Bergsbaken T, Cookson BT (2007) Macrophage activation redirects yersinia-infected host cell death from apoptosis to caspase-1-dependent pyroptosis. PLoS Pathog 3:e161.
39. Broz P, et al. (2010) Redundant roles for inflammasome receptors NLRP3 and NLRC4 in host defense against Salmonella. J Exp Med 207:1745-1755.
40. Albers E (2009) Metabolic characteristics and importance of the universal methionine salvage pathway recycling methionine from 5′- methylthioadenosine. IUBMB Life 61:1132-1142.
41. Ashida H, Saito Y, Kojima C, Yokota A (2008) Enzymatic characterization of 5-methylthioribulose-1-phosphate dehydratase of the methionine salvage pathway in Bacillus subtilis. Biosci Biotechnol Biochem 72:959-967. (Pubitemid 351679353)
42. De Montigny C, Sygusch J (1996) Functional characterization of an extreme thermophilic class II fructose-1,6-bisphosphate aldolase. Eur J Biochem 241:243-248. (Pubitemid 26342995)
43. Sauvé V, Sygusch J (2001)Molecular cloning, expression, purification, and characterization of fructose-1,6-bisphosphate aldolase from Thermus aquaticus. Protein Expr Purif 21:293-302.
44. Pirkov I, Norbeck J, Gustafsson L, Albers E (2008) A complete inventory of all enzymes in the eukaryotic methionine salvage pathway. FEBS J 275:4111-4120.
45. Pegg AE (2009) Mammalian polyamine metabolism and function. IUBMB Life 61:880-894.
46. Fernandes-Alnemri T, et al. (2010) The AIM2 infl ammasome is critical for innate immunity to Francisella tularensis. Nat Immunol 11:385-393.
47. Jones JW, et al. (2010) Absent in melanoma 2 is required for innate immune recognition of Francisella tularensis. Proc Natl Acad Sci USA 107:9771-9776.
48. Thornberry NA, et al. (1992) A novel heterodimeric cysteine protease is required for interleukin-1 beta processing in monocytes. Nature 356:768-774.
49. Hall DR, et al. (1999) The crystal structure of Escherichia coli class II fructose-1, 6-bisphosphate aldolase in complex with phosphoglycolohydroxamate reveals details of mechanism and specificity. J Mol Biol 287:383-394. (Pubitemid 29141294)
50. Li TW, et al. (2009) S-Adenosylmethionine and methylthioadenosine inhibit cellular FLICE inhibitory protein expression and induce apoptosis in colon cancer cells. Mol Pharmacol 76:192-200.
51. Ansorena E, et al. (2002) S-adenosylmethionine and methylthioadenosine are antiapoptotic in cultured rat hepatocytes but proapoptotic in human hepatoma cells. Hepatology 35:274-280. (Pubitemid 34106365)
52. Hevia H, et al. (2004) 5?-methylthioadenosine modulates the inflammatory response to endotoxin in mice and in rat hepatocytes. Hepatology 39:1088-1098. (Pubitemid 38428948)
53. Kayagaki N, et al. (2011) Non-canonical inflammasome activation targets caspase-11. Nature 479:117-121.
54. Grimble RF, Grimble GK (1998) Immunonutrition: Role of sulfur amino acids, related amino acids, and polyamines. Nutrition 14:605-610. (Pubitemid 28346854)
55. Wright FA, et al. (2011) Genome-wide association and linkage identify modifier loci of lung disease severity in cystic fibrosis at 11p13 and 20q13.2. Nat Genet 43:539-546.
56. Wolfe ND, Dunavan CP, Diamond J (2007) Origins of major human infectious diseases. Nature 447:279-283. (Pubitemid 46788835)
57. Lamkanfi M, Dixit VM (2011) Modulation of inflammasome pathways by bacterial and viral pathogens. J Immunol 187:597-602.
58. Jobling MA, Hurles ME, Tyler-Smith C (2004) Human Evolutionary Genetics: Origins (Garland, New York).
59. Coop G, Witonsky D, Di Rienzo A, Pritchard JK (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics 185:1411-1423.
60. Saleh M, et al. (2004) Differential modulation of endotoxin responsiveness by human caspase-12 polymorphisms. Nature 429:75-79. (Pubitemid 38620553)
61. Xue Y, et al. (2006) Spread of an inactive form of caspase-12 in humans is due to recent positive selection. Am J Hum Genet 78:659-670.
62. Olson MV (1999) When less is more: Gene loss as an engine of evolutionary change. Am J Hum Genet 64:18-23.
63. Purcell S, et al. (2007) PLINK: A tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet 81:559-575. (Pubitemid 47330214)
64. Saxena R, et al. (2007) Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316:1331-1336. (Pubitemid 46871653)
65. Fong C, et al. (2010) GWAS analyzer: Integrating genotype, phenotype and public annotation data for genome-wide association study analysis. Bioinformatics 26:560-564.
66. Barrett JC, Fry B, Maller J, Daly MJ (2005) Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics 21:263-265. (Pubitemid 40202029)
67. Abecasis GR, Cardon LR, Cookson WO (2000) A general test of association for quantitative traits in nuclear families. Am J Hum Genet 66:279-292. (Pubitemid 30481489)
68. Stark AL, et al. (2010) Population differences in the rate of proliferation of international HapMap cell lines. Am J Hum Genet 87:829-833.
69. Garcia-Calvo M, et al. (1998) Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 273:32608-32613. (Pubitemid 28557641)
70. Stennicke HR, Salvesen GS (1997) Biochemical characteristics of caspases-3, -6, -7, and -8. J Biol Chem 272:25719-25723. (Pubitemid 27438890)
71. Kahlenberg JM, Dubyak GR (2004) Differing caspase-1 activation states in monocyte versus macrophage models of IL-1beta processing and release. J Leukoc Biol 76:676-684. (Pubitemid 39129101)
72. Stevens AP, Dettmer K,Wallner S, Bosserhoff AK, Oefner PJ (2008) Quantitative analysis of 5′-deoxy-5′-methylthioadenosine in melanoma cells by liquid chromatography-stable isotope ratio tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 876:123-128.
73. Levy MM, et al.; International Sepsis Definitions Conference (2003) 2001 SCCM/ESICM/ACCP/ATS/SIS International Sepsis Definitions Conference. Intensive Care Med 29:530-538. (Pubitemid 36523666)
74. Coop G, et al. (2009) The role of geography in human adaptation. PLoS Genet 5:e1000500.
75. Pickrell JK, et al. (2009) Signals of recent positive selection in a worldwide sample of human populations. Genome Res 19:826-837.
76. Pritchard JK, Pickrell JK, Coop G (2010) The genetics of human adaptation: Hard sweeps, soft sweeps, and polygenic adaptation. Curr Biol 20:R208-R215.
77. Conrad DF, et al. (2006) A worldwide survey of haplotype variation and linkage disequilibrium in the human genome. Nat Genet 38:1251-1260. (Pubitemid 44646287)
78. Altshuler DM, et al. (2010) Integrating common and rare genetic variation in diverse human populations. Nature 467:52-58.
79. Pickrell JK, et al. (2010) Understanding mechanisms underlying human gene expression variation with RNA sequencing. Nature 464:768-772.
80. Gamazon ER, et al. (2010) SCAN: SNP and copy number annotation. Bioinformatics 26:259-262.