Conditional meta-analysis stratifying on detailed HLA genotypes identifies a novel type 1 diabetes locus around TCF19 in the MHC

Human Genetics

Volumn 129, Issue 2, 2011, Pages 161-176

  Cheung, Yee Him ^a   Watkinson, John ^a   Anastassiou, Dimitris ^a  

^a Columbia University ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HLA DQA1 ANTIGEN; HLA DQB1 ANTIGEN; HLA DR ANTIGEN; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR 19; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME 6; CONTROLLED STUDY; GENE LINKAGE DISEQUILIBRIUM; GENE REPLICATION; GENETIC SCREENING; HLA TYPING; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; MAJOR HISTOCOMPATIBILITY COMPLEX; NUCLEAR FAMILY; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM;

CASE-CONTROL STUDIES; DIABETES MELLITUS, TYPE 1; FEMALE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; OCTAMER TRANSCRIPTION FACTOR-3; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEINS; TRANSCRIPTION FACTORS;

EID: 78951485281     PISSN: 03406717     EISSN: 14321203     Source Type: Journal    
DOI: 10.1007/s00439-010-0908-2     Document Type: Article

References (56)

1. CA Alper CE Larsen DP Dubey ZL Awdeh DA Fici EJ Yunis 2006 The haplotype structure of the human major histocompatibility complex Hum Immunol 67 73 84 1:CAS:528:DC%2BD28Xks1eltrc%3D 16698428 10.1016/j.humimm.2005.11.006
2. TA Aly EE Baschal MM Jahromi MS Fernando SR Babu TE Fingerlin A Kretowski HA Erlich PR Fain MJ Rewers GS Eisenbarth 2008 Analysis of single nucleotide polymorphisms identifies major type 1A diabetes locus telomeric of the major histocompatibility complex Diabetes 57 770 776 1:CAS:528:DC%2BD1cXjt1Churk%3D 18065518 10.2337/db07-0900
3. P Armitage 1955 Tests for linear trends in proportions and frequencies Biometrics 11 375 386 10.2307/3001775
4. K Asumalahti C Veal T Laitinen S Suomela M Allen O Elomaa M Moser R de Cid S Ripatti I Vorechovsky JA Marcusson H Nakagawa C Lazaro X Estivill F Capon G Novelli U Saarialho-Kere J Barker R Trembath J Kere 2002 Coding haplotype analysis supports HCR as the putative susceptibility gene for psoriasis at the MHC PSORS1 locus Hum Mol Genet 11 589 597 1:CAS:528:DC%2BD38XitlWitro%3D 11875053 10.1093/hmg/11.5.589
5. JC Barrett B Fry J Maller MJ Daly 2005 Haploview: analysis and visualization of LD and haplotype maps Bioinformatics 21 263 265 1:CAS:528:DC%2BD2MXkt1WitQ%3D%3D 15297300 10.1093/bioinformatics/bth457
6. JC Barrett DG Clayton P Concannon B Akolkar JD Cooper HA Erlich C Julier G Morahan J Nerup C Nierras V Plagnol F Pociot H Schuilenburg DJ Smyth H Stevens JA Todd NM Walker SS Rich 2009 Genome-wide association study and meta-analysis find that over 40 loci affect risk of type 1 diabetes Nat Genet 41 703 707 1:CAS:528:DC%2BD1MXls1Cmt7c%3D 19430480 10.1038/ng.381
7. Y Benjamini Y Hochberg 1995 Controlling the false discovery rate-a practical and powerful approach to multiple testing J R Stat Soc Ser B Methodol 57 289 300
8. Brown WM, Pierce J, Hilner JE, Perdue LH, Lohman K, Li L, Venkatesh RB, Hunt S, Mychaleckyj JC, Deloukas P (2009) Overview of the MHC fine mapping data. Diabetes Obes Metab 11(Suppl 1):2-7
9. BL Browning SR Browning 2009 A unified approach to genotype imputation and haplotype-phase inference for large data sets of trios and unrelated individuals Am J Hum Genet 84 210 223 1:CAS:528:DC%2BD1MXisFCrtL8%3D 19200528 10.1016/j.ajhg.2009.01.005
10. TD Cruz AM Valdes A Santiago T Frazer de Llado LJ Raffel A Zeidler JI Rotter HA Erlich M Rewers T Bugawan JA Noble 2004 DPB1 alleles are associated with type 1 diabetes susceptibility in multiple ethnic groups Diabetes 53 2158 2163 1:CAS:528:DC%2BD2cXmtFGqt7Y%3D 15277401 10.2337/diabetes.53.8.2158
11. F Cucca F Dudbridge M Loddo AP Mulargia R Lampis E Angius S De Virgiliis BP Koeleman SC Bain AH Barnett F Gilchrist H Cordell K Welsh JA Todd 2001 The HLA-DPB1-associated component of the IDDM1 and its relationship to the major loci HLA-DQB1, -DQA1, and -DRB1 Diabetes 50 1200 1205 1:CAS:528: DC%2BD3MXkvFSnsrg%3D 11334427 10.2337/diabetes.50.5.1200
12. D Curtis 1997 Use of siblings as controls in case-control association studies Ann Hum Genet 61 319 333 1:STN:280:DyaK1c%2Fjt1Cruw%3D%3D 9365785 10.1017/S000348009700626X
13. PI de Bakker G McVean PC Sabeti MM Miretti T Green J Marchini X Ke AJ Monsuur P Whittaker M Delgado J Morrison A Richardson EC Walsh X Gao L Galver J Hart DA Hafler M Pericak-Vance JA Todd MJ Daly J Trowsdale C Wijmenga TJ Vyse S Beck SS Murray M Carrington S Gregory P Deloukas JD Rioux 2006 A high-resolution HLA and SNP haplotype map for disease association studies in the extended human MHC Nat Genet 38 1166 1172 16998491 10.1038/ng1885
14. P Duggal EM Gillanders TN Holmes JE Bailey-Wilson 2008 Establishing an adjusted p-value threshold to control the family-wide type 1 error in genome wide association studies BMC Genomics 9 516 18976480 10.1186/1471-2164-9-516
15. MC Eike T Becker K Humphreys M Olsson BA Lie 2009 Conditional analyses on the T1DGC MHC dataset: novel associations with type 1 diabetes around HLA-G and confirmation of HLA-B Genes Immun 10 56 67 1:CAS:528:DC%2BD1MXotVemtQ%3D%3D 18830248 10.1038/gene.2008.74
16. MC Eike M Olsson DE Undlien K Dahl-Jorgensen G Joner KS Ronningen E Thorsby BA Lie 2009 Genetic variants of the HLA-A, HLA-B and AIF1 loci show independent associations with type 1 diabetes in Norwegian families Genes Immun 10 141 150 1:CAS:528:DC%2BD1MXisFeltLo%3D 18987644 10.1038/gene.2008.88
17. EMBL-EBI (2010) The International Immunogenetics Information System (IMGT) HLA Database. http://www.ebi.ac.uk/imgt/hla/stats.html
18. H Erlich AM Valdes J Noble JA Carlson M Varney P Concannon JC Mychaleckyj JA Todd P Bonella AL Fear E Lavant A Louey P Moonsamy 2008 HLA DR-DQ haplotypes and genotypes and type 1 diabetes risk: analysis of the type 1 diabetes genetics consortium families Diabetes 57 1084 1092 1:CAS:528: DC%2BD1cXksVGrsr4%3D 18252895 10.2337/db07-1331
19. MA Ferreira JJ Hottenga NM Warrington SE Medland G Willemsen RW Lawrence S Gordon EJ de Geus AK Henders JH Smit MJ Campbell L Wallace DM Evans MJ Wright DR Nyholt AL James JP Beilby BW Penninx LJ Palmer IH Frazer GW Montgomery NG Martin DI Boomsma 2009 Sequence variants in three loci influence monocyte counts and erythrocyte volume Am J Hum Genet 85 745 749 1:CAS:528: DC%2BC3cXksFajsA%3D%3D 19853236 10.1016/j.ajhg.2009.10.005
20. B Freidlin G Zheng Z Li JL Gastwirth 2002 Trend tests for case-control studies of genetic markers: power, sample size and robustness Hum Hered 53 146 152 1:STN:280:DC%2BD38zps1amtA%3D%3D 12145550 10.1159/000064976
21. SB Gabriel SF Schaffner H Nguyen JM Moore J Roy B Blumenstiel J Higgins M DeFelice A Lochner M Faggart SN Liu-Cordero C Rotimi A Adeyemo R Cooper R Ward ES Lander MJ Daly D Altshuler 2002 The structure of haplotype blocks in the human genome Science 296 2225 2229 1:CAS:528:DC%2BD38XkvFGhtrc%3D 12029063 10.1126/science.1069424
22. CJ Greenbaum 2002 Insulin resistance in type 1 diabetes Diabetes Metab Res Rev 18 192 200 1:CAS:528:DC%2BD38XmtVWjs7Y%3D 12112937 10.1002/dmrr.291
23. P Hanifi Moghaddam P de Knijf BO Roep B Van der Auwera A Naipal F Gorus F Schuit MJ Giphart 1998 Genetic structure of IDDM1: two separate regions in the major histocompatibility complex contribute to susceptibility or protection. Belgian Diabetes Registry Diabetes 47 263 269 1:STN:280:DyaK1c7nvVGgug%3D%3D 9519723 10.2337/diabetes.47.2.263
24. SJ Holm LM Carlen L Mallbris M Stahle-Backdahl KP O'Brien 2003 Polymorphisms in the SEEK1 and SPR1 genes on 6p21.3 associate with psoriasis in the Swedish population Exp Dermatol 12 435 444 1:CAS:528:DC%2BD3sXmvFymtrw%3D 12930300 10.1034/j.1600-0625.2003.00048.x
25. R Horton L Wilming V Rand RC Lovering EA Bruford VK Khodiyar MJ Lush S Povey CC Talbot Jr MW Wright HM Wain J Trowsdale A Ziegler S Beck 2004 Gene map of the extended human MHC Nat Rev Genet 5 889 899 1:CAS:528:DC%2BD2cXhtVarsLbN 15573121 10.1038/nrg1489
26. T Hothorn K Hornik MAV van de Wiel A Zeileis 2008 Implementing a class of permutation tests: the coin package J Stat Softw 28 1 23
27. BN Howie P Donnelly J Marchini 2009 A flexible and accurate genotype imputation method for the next generation of genome-wide association studies PLoS Genet 5 e1000529 19543373 10.1371/journal.pgen.1000529
28. JMM Howson NM Walker D Clayton JA Todd TDG Consortium 2009 Confirmation of HLA class II independent type 1 diabetes associations in the major histocompatibility complex including HLA-B and HLA-A Diabetes Obes Metab 11 31 45 19143813 10.1111/j.1463-1326.2008.01001.x
29. Huang C-Y (1999) Factors influencing the reliability of DIF detection methods. Dissertation Abstracts International 59:2944
30. ME Hystad JH Myklebust TH Bo EA Sivertsen E Rian L Forfang E Munthe A Rosenwald M Chiorazzi I Jonassen LM Staudt EB Smeland 2007 Characterization of early stages of human B cell development by gene expression profiling J Immunol 179 3662 3671 1:CAS:528:DC%2BD2sXpvFKls7c%3D 17785802
31. S Johansson BA Lie JA Todd F Pociot J Nerup A Cambon-Thomsen I Kockum HE Akselsen E Thorsby DE Undlien 2003 Evidence of at least two type 1 diabetes susceptibility genes in the HLA complex distinct from HLA-DQB1,-DQA1 and-DRB1 Genes Immun 4 46 53 1:CAS:528:DC%2BD3sXhsVCmur4%3D 12595901 10.1038/sj.gene. 6363917
32. BP Koeleman F Dudbridge HJ Cordell JA Todd 2000 Adaptation of the extended transmission/disequilibrium test to distinguish disease associations of multiple loci: the conditional extended transmission/disequilibrium test Ann Hum Genet 64 207 213 1:STN:280:DC%2BD3MvitlKksA%3D%3D 11246472 10.1046/j.1469-1809.2000.6430207.x
33. BP Koeleman MH Herr P Zavattari F Dudbridge R March D Campbell AH Barnett SC Bain AP Mulargia M Loddo W Amos F Cucca JA Todd 2000 Conditional ETDT analysis of the human leukocyte antigen region in type 1 diabetes Ann Hum Genet 64 215 221 1:STN:280:DC%2BD3MvitlKksQ%3D%3D 11246473 10.1046/j.1469-1809.2000. 6430215.x
34. BP Koeleman BA Lie DE Undlien F Dudbridge E Thorsby RR de Vries F Cucca BO Roep MJ Giphart JA Todd 2004 Genotype effects and epistasis in type 1 diabetes and HLA-DQ trans dimer associations with disease Genes Immun 5 381 388 1:CAS:528:DC%2BD2cXlvValsLs%3D 15164102 10.1038/sj.gene.6364106
35. DH Ku CD Chang J Koniecki LA Cannizzaro L Boghosian-Sell H Alder R Baserga 1991 A new growth-regulated complementary DNA with the sequence of a putative trans-activating factor Cell Growth Differ 2 179 186 1:CAS:528:DyaK38XmsVKgtr4%3D 1868030
36. BA Lie JA Todd F Pociot J Nerup HE Akselsen G Joner K Dahl-Jorgensen KS Ronningen E Thorsby DE Undlien 1999 The predisposition to type 1 diabetes linked to the human leukocyte antigen complex includes at least one non-class II gene Am J Hum Genet 64 793 800 1:CAS:528:DyaK1MXitFCht7c%3D 10053014 10.1086/302283
37. K Lunde HG Belting W Driever 2004 Zebrafish pou5f1/pou2, homolog of mammalian Oct4, functions in the endoderm specification cascade Curr Biol 14 48 55 1:CAS:528:DC%2BD2cXjsFemsQ%3D%3D 14711414 10.1016/j.cub.2003.11.022
38. N Mantel W Haenszel 1959 Statistical aspects of the analysis of data from retrospective studies of disease J Natl Cancer Inst 22 719 748 1:STN:280:DyaG1M%2FosVOhtQ%3D%3D 13655060
39. S Nejentsev Z Gombos AP Laine R Veijola M Knip O Simell O Vaarala HK Akerblom J Ilonen 2000 Non-class II HLA gene associated with type 1 diabetes maps to the 240-kb region near HLA-B Diabetes 49 2217 2221 1:CAS:528: DC%2BD3cXos1ejsbs%3D 11118029 10.2337/diabetes.49.12.2217
40. S Nejentsev JM Howson NM Walker J Szeszko SF Field HE Stevens P Reynolds M Hardy E King J Masters J Hulme LM Maier D Smyth R Bailey JD Cooper G Ribas RD Campbell DG Clayton JA Todd 2007 Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A Nature 450 887 892 1:CAS:528: DC%2BD2sXhtl2nsrjF 18004301 10.1038/nature06406
41. JA Noble AM Valdes TL Bugawan RJ Apple G Thomson HA Erlich 2002 The HLA class I A locus affects susceptibility to type 1 diabetes Hum Immunol 63 657 664 1:CAS:528:DC%2BD38Xlt12nu78%3D 12121673 10.1016/S0198-8859(02)00421-4
42. S Purcell B Neale K Todd-Brown L Thomas MA Ferreira D Bender J Maller P Sklar PI de Bakker MJ Daly PC Sham 2007 PLINK: a tool set for whole-genome association and population-based linkage analyses Am J Hum Genet 81 559 575 1:CAS:528:DC%2BD2sXhtVSqurrL 17701901 10.1086/519795
43. WP Robinson J Barbosa SS Rich G Thomson 1993 Homozygous parent affected sib pair method for detecting disease predisposing variants: application to insulin dependent diabetes mellitus Genet Epidemiol 10 273 288 1:STN:280:DyaK2c%2FktVKktg%3D%3D 8224807 10.1002/gepi.1370100502
44. I Santin A Castellanos-Rubio AM Aransay G Gutierrez S Gaztambide I Rica JL Vicario JA Noble L Castano JR Bilbao 2009 Exploring the diabetogenicity of the HLA-B18-DR3 CEH: independent association with T1D genetic risk close to HLA-DOA Genes Immun 10 596 600 1:CAS:528:DC%2BD1MXhtVKrs73N 19458622 10.1038/gene.2009.41
45. T Sugawara H Shimizu N Hoshi A Nakajima S Fujimoto 2003 Steroidogenic acute regulatory protein-binding protein cloned by a yeast two-hybrid system J Biol Chem 278 42487 42494 1:CAS:528:DC%2BD3sXot1alsrc%3D 12909641 10.1074/jbc.M302291200
46. The International HapMap Consortium (2005) A haplotype map of the human genome. Nature 437:1299-1320
47. G Thomson 1984 HLA DR antigens and susceptibility to insulin-dependent diabetes mellitus Am J Hum Genet 36 1309 1317 1:STN:280:DyaL2M%2FpsVamtw%3D%3D 6334991
48. G Thomson 1995 Mapping disease genes: family-based association studies Am J Hum Genet 57 487 498 1:STN:280:DyaK2MzpslygsA%3D%3D 7668275
49. G Thomson LF Barcellos AM Valdes 2008 Searching for additional disease loci in a genomic region Adv Genet 60 253 292 1:CAS:528:DC%2BD1cXmtFSltbs%3D 18358324 10.1016/S0065-2660(07)00411-7
50. AM Valdes HA Erlich JA Noble 2005 Human leukocyte antigen class I B and C loci contribute to type 1 diabetes (T1D) susceptibility and age at T1D onset Hum Immunol 66 301 313 1:CAS:528:DC%2BD2MXisVWqtrs%3D 15784469 10.1016/j.humimm.2004.12.001
51. AM Valdes G Thomson TDG Consortium 2009 Several loci in the HLA class III region are associated with T1D risk after adjusting for DRB1-DQB1 Diabetes Obes Metab 11 46 52 19143814 10.1111/j.1463-1326.2008.01002.x
52. AM Valdes G Thomson LF Barcellos 2010 Genetic variation within the HLA class III influences T1D susceptibility conferred by high-risk HLA haplotypes Genes Immun 11 209 218 1:CAS:528:DC%2BC3cXkvFCqsrk%3D 20054343 10.1038/gene.2009.104
53. MK Viken A Blomhoff M Olsson HE Akselsen F Pociot J Nerup I Kockum A Cambon-Thomsen E Thorsby DE Undlien BA Lie 2009 Reproducible association with type 1 diabetes in the extended class I region of the major histocompatibility complex Genes Immun 10 323 333 1:CAS:528:DC%2BD1MXms12htb8%3D 19295542 10.1038/gene.2009.13
54. C Wallace DJ Smyth M Maisuria-Armer NM Walker JA Todd DG Clayton 2009 The imprinted DLK1-MEG3 gene region on chromosome 14q32.2 alters susceptibility to type 1 diabetes Nat Genet 42 68 71 19966805 10.1038/ng.493
55. WTCCC 2007 Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls Nature 447 661 678 10.1038/nature05911
56. Z Yu DJ Schaid 2007 Sequential haplotype scan methods for association analysis Genet Epidemiol 31 553 564 17487883 10.1002/gepi.20228