Genetics of the HLA region in the prediction of type 1 diabetes

Current Diabetes Reports

Volumn 11, Issue 6, 2011, Pages 533-542

  Noble, Janelle A ^a   Valdes, Ana M ^b  

^a CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Genetic risk; HLA class I; HLA class II; HLA class III; Risk prediction; Type 1 diabetes

Indexed keywords

AUTOANTIBODY; HLA ANTIGEN CLASS 2; HLA DPB1 ANTIGEN; HLA DQ ANTIGEN; HLA DQA1 ANTIGEN; HLA DR ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN;

ANTIBODY SCREENING; ARTICLE; CHROMOSOME MAP; DISEASE ASSOCIATION; DISEASE CONTROL; DISEASE COURSE; DISEASE PREDISPOSITION; DPB1 GENE; DQA1 GENE; DQB1 GENE; DRB1 GENE; FAMILIAL INCIDENCE; FAMILY HISTORY; GENE; GENE FREQUENCY; GENE FUNCTION; GENE LOCUS; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC MODEL; GENETIC POLYMORPHISM; GENETIC RISK; GENETIC SUSCEPTIBILITY; GENOTYPE; HAPLOTYPE; HETEROZYGOSITY; HIGH RISK INFANT; HLA SYSTEM; HOMOZYGOSITY; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; PATIENT SELECTION; PREDICTIVE VALUE; PROTEIN EXPRESSION; PROTEIN FUNCTION; RISK ASSESSMENT;

DIABETES MELLITUS, TYPE 1; GENETIC PREDISPOSITION TO DISEASE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HISTOCOMPATIBILITY ANTIGENS CLASS II; HUMANS;

EID: 80755135395     PISSN: 15344827     EISSN: 15390829     Source Type: Journal    
DOI: 10.1007/s11892-011-0223-x     Document Type: Article

References (75)

1. GS Eisenbarth Banting Lecture 2010 An unfinished journey: molecular pathogenesis to prevention of type 1A diabetes Diabetes 59 759 774 20350969 10.2337/db09-1855 1:CAS:528:DC%2BC3cXltFSmsbs%3D This lecture gives an excellent overview of T1D pathogenesis important to the understanding of the genetic susceptibility
2. DB Dunger MA Sperling CL Acerini DJ Bohn D Daneman TP Danne, et al. 2004 European Society for Paediatric Endocrinology/Lawson Wilkins Pediatric Endocrine Society consensus statement on diabetic ketoacidosis in children and adolescents Pediatrics 113 e133 e140 14754983 10.1542/peds.113.2.e133
3. DM Maahs NA West JM Lawrence EJ Mayer-Davis 2010 Epidemiology of type 1 diabetes Endocrinol Metab Clin North Am 39 481 497 20723815 10.1016/j.ecl.2010. 05.011
4. M Karvonen M Viik-Kajander E Moltchanova I Libman R LaPorte J Tuomilehto 2000 Incidence of childhood type 1 diabetes worldwide. Diabetes Mondiale (DiaMond) Project Group Diabetes Care 23 1516 1526 11023146 10.2337/diacare.23. 10.1516 1:STN:280:DC%2BD3cvmvVaqtA%3D%3D
5. D Dabelea RA Bell RB D'Agostino Jr G Imperatore JM Johansen B Linder, et al. 2007 Incidence of diabetes in youth in the United States Jama 297 2716 2724 17595272 10.1001/jama.297.24.2716 (Pubitemid 47001097)
6. P Concannon SS Rich GT Nepom 2009 Genetics of type 1A diabetes N Engl J Med 360 1646 1654 19369670 10.1056/NEJMra0808284 1:CAS:528:DC%2BD1MXkvVKltbs%3D
7. MJ Redondo J Jeffrey PR Fain GS Eisenbarth T Orban 2008 Concordance for islet autoimmunity among monozygotic twins N Engl J Med 359 2849 2850 19109586 10.1056/NEJMc0805398 1:CAS:528:DC%2BD1cXhsFCmtb%2FE
8. E Bonifacio AG Ziegler 2010 Advances in the prediction and natural history of type 1 diabetes Endocrinol Metab Clin North Am 39 513 525 20723817 10.1016/j.ecl.2010.05.007
9. JA Noble AM Valdes M Cook W Klitz G Thomson HA Erlich 1996 The role of HLA class II genes in insulin-dependent diabetes mellitus: molecular analysis of 180 Caucasian, multiplex families Am J Hum Genet 59 1134 1148 8900244 1:CAS:528:DyaK28XmvFyks7c%3D (Pubitemid 26346356)
10. AP Lambert KM Gillespie G Thomson HJ Cordell JA Todd EA Gale, et al. 2004 Absolute risk of childhood-onset type 1 diabetes defined by human leukocyte antigen class II genotype: a population-based study in the United Kingdom J Clin Endocrinol Metab 89 4037 4043 15292346 10.1210/jc.2003-032084 1:CAS:528:DC%2BD2cXmslKlsr4%3D (Pubitemid 39089121)
11. R Horton L Wilming V Rand RC Lovering EA Bruford VK Khodiyar, et al. 2004 Gene map of the extended human MHC Nat Rev Genet 5 889 899 15573121 10.1038/nrg1489 1:CAS:528:DC%2BD2cXhtVarsLbN (Pubitemid 39564252)
12. G Thomson AM Valdes JA Noble I Kockum MN Grote J Najman, et al. 2007 Relative predispositional effects of HLA class II DRB1-DQB1 haplotypes and genotypes on type 1 diabetes: a meta-analysis Tissue Antigens 70 110 127 17610416 10.1111/j.1399-0039.2007.00867.x 1:CAS:528:DC%2BD2sXpsVGiu7g%3D (Pubitemid 47024833)
13. ES Lander NJ Schork 1994 Genetic dissection of complex traits Science 265 2037 2048 8091226 10.1126/science.8091226 1:STN:280:DyaK2cznvVSjsg%3D%3D (Pubitemid 24325685)
14. DP Singal MA Blajchman 1973 Histocompatibility (HL-A) antigens, lymphocytotoxic antibodies and tissue antibodies in patients with diabetes mellitus Diabetes 22 429 432 4541338 1:STN:280:DyaE3s3gsV2ntQ%3D%3D
15. BD Tait 1990 Genetic susceptibility to type I diabetes: a review J Autoimmun 3 Suppl 1 3 11 2187458 10.1016/S0896-8411(09)90003-8 (Pubitemid 20326082)
16. H Payami G Thomson U Motro EJ Louis E Hudes 1985 The affected sib method. IV. Sib trios Ann Hum Genet 49 303 314 3865624 10.1111/j.1469-1809.1985. tb01706.x 1:STN:280:DyaL28%2FnsFyjsA%3D%3D (Pubitemid 16208770)
17. G Thomson WP Robinson MK Kuhner S Joe MJ MacDonald JL Gottschall, et al. 1988 Genetic heterogeneity, modes of inheritance, and risk estimates for a joint study of Caucasians with insulin-dependent diabetes mellitus Am J Hum Genet 43 799 816 3057885 1:STN:280:DyaL1M%2FmtVaktw%3D%3D (Pubitemid 19018982)
18. H Erlich AM Valdes J Noble JA Carlson M Varney P Concannon, et al. 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 18252895 10.2337/db07-1331 1:CAS:528:DC%2BD1cXksVGrsr4%3D This paper summarizes the analyses of HLA class II DR- and DQ-encoding genes on T1D risk in the T1DGC samples
19. 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 8224807 10.1002/gepi.1370100502 1:STN:280:DyaK2c%2FktVKktg%3D%3D (Pubitemid 23299714)
20. S Nejentsev JM Howson NM Walker J Szeszko SF Field HE Stevens, et al. 2007 Localization of type 1 diabetes susceptibility to the MHC class I genes HLA-B and HLA-A Nature 450 887 892 18004301 10.1038/nature06406 1:CAS:528:DC%2BD2sXhtl2nsrjF (Pubitemid 350231332)
21. G Thomson 1984 HLA DR antigens and susceptibility to insulin-dependent diabetes mellitus Am J Hum Genet 36 1309 1317 6334991 1:STN:280: DyaL2M%2FpsVamtw%3D%3D (Pubitemid 15156234)
22. 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 12121673 10.1016/S0198-8859(02)00421-4 1:CAS:528:DC%2BD38Xlt12nu78%3D (Pubitemid 34816108)
23. A Svejgaard LP Ryder 1989 HLA and insulin-dependent diabetes: an overview Genet Epidemiol 6 1 14 2659426 10.1002/gepi.1370060104 1:STN:280: DyaL1M3ns1ygtg%3D%3D (Pubitemid 19081905)
24. KS Ronningen G Markussen T Iwe E Thorsby 1989 An increased risk of insulin-dependent diabetes mellitus (IDDM) among HLA-DR4, DQw8/DRw8, DQw4 heterozygotes Hum Immunol 24 165 173 2564383 10.1016/0198-8859(89)90057-8 1:STN:280:DyaL1M7nsVSltg%3D%3D (Pubitemid 19072834)
25. AM Valdes G Thomson J Graham M Zarghami B McNeney I Kockum, et al. 2005 D6S265*15 marks a DRB1*15, DQB1*0602 haplotype associated with attenuated protection from type 1 diabetes mellitus Diabetologia 48 2540 2543 16320082 10.1007/s00125-005-0011-8 1:CAS:528:DC%2BD2MXht1Omu7zP (Pubitemid 41738220)
26. G Pawelec HJ Buhring 1990 Expression of MHC class II epitopes on human T lymphocyte clones Cell Immunol 127 520 526 1970281 10.1016/0008-8749(90)90152-H 1:STN:280:DyaK3c3islOnsQ%3D%3D (Pubitemid 20147808)
27. A Cesbron P Moreau N Milpied JL Harousseau JY Muller JD Bignon 1992 Crucial role of the third and fourth hypervariable regions of HLA-DPB1 allelic sequences in the mixed lymphocyte reaction Hum Immunol 33 202 207 1535619 10.1016/0198-8859(92)90072-U 1:CAS:528:DyaK38XlsVyrtLw%3D
28. I Nicholson M Varney C Kanaan A Grigg J Szer K Tiedemann, et al. 1997 Alloresponses to HLA-DP detected in the primary MLR: correlation with a single amino acid difference Hum Immunol 55 163 169 9361968 10.1016/S0198-8859(97) 00091-8 1:CAS:528:DyaK2sXnsVeisrc%3D (Pubitemid 27467988)
29. AB Begovich TL Bugawan BS Nepom W Klitz GT Nepom HA Erlich 1989 A specific HLA-DP beta allele is associated with pauciarticular juvenile rheumatoid arthritis but not adult rheumatoid arthritis Proc Natl Acad Sci U S A 86 9489 9493 2512583 10.1073/pnas.86.23.9489 1:CAS:528:DyaK3cXnsFSqtA%3D%3D (Pubitemid 20010452)
30. KD Rosenman M Rossman V Hertzberg MJ Reilly C Rice E Kanterakis, et al. 2011 HLA class II DPB1 and DRB1 polymorphisms associated with genetic susceptibility to beryllium toxicity Occup Environ Med 68 487 493 21186201 10.1136/oem.2010.055046 1:CAS:528:DC%2BC3MXps1OgtLk%3D
31. TD Cruz AM Valdes A Santiago T Frazer De Llado LJ Raffel A Zeidler 2004 DPB1 alleles are associated with type 1 diabetes susceptibility in multiple ethnic groups Diabetes 53 2158 2163 15277401 10.2337/diabetes.53.8.2158 1:CAS:528:DC%2BD2cXmtFGqt7Y%3D (Pubitemid 38970770)
32. KA Al-Hussein NR Rama M Ahmad E Rozemuller MG Tilanus 2003 HLA-DPB1*0401 is associated with dominant protection against type 1 diabetes in the general Saudi population and in subjects with a high-risk DR/DQ haplotype Eur J Immunogenet 30 115 119 12648278 10.1046/j.1365-2370.2003.00369.x 1:CAS:528:DC%2BD3sXjtlKgsLk%3D (Pubitemid 36408299)
33. F Cucca F Dudbridge M Loddo AP Mulargia R Lampis E Angius, et al. 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 11334427 10.2337/diabetes.50.5.1200 1:CAS:528:DC%2BD3MXkvFSnsrg%3D (Pubitemid 32374554)
34. JA Noble AM Valdes G Thomson HA Erlich 2000 The HLA class II locus DPB1 can influence susceptibility to type 1 diabetes Diabetes 49 121 125 10615959 10.2337/diabetes.49.1.121 1:CAS:528:DC%2BD3cXkt1ygtw%3D%3D (Pubitemid 30022933)
35. K Nishimaki T Kawamura H Inada K Yagawa Y Nose N Nabeya, et al. 2000 HLA DPB1*0201 gene confers disease susceptibility in Japanese with childhood onset Type I diabetes, independent of HLA-DR and DQ genotypes Diabetes Res Clin Pract 47 49 55 10660221 10.1016/S0168-8227(99)00103-5 1:CAS:528: DyaK1MXnslyhu7w%3D
36. HA Erlich JI Rotter JD Chang SD Shaw LJ Raffel W Klitz, et al. 1996 Association of HLA-DPB1*0301 with insulin dependent diabetes mellitus in Mexican-Americans Diabetes 45 610 614 8621011 10.2337/diabetes.45.5.610 1:CAS:528:DyaK28Xjs1ylsLo%3D (Pubitemid 26140544)
37. PL Balducci-Silano ZE Layrisse 1995 HLA-DP and susceptibility to insulin-dependent diabetes mellitus in an ethnically mixed population. Associations with other HLA-alleles J Autoimmun 8 425 437 7576003 10.1006/jaut.1995.0034 1:STN:280:DyaK28%2Fot1ejsA%3D%3D
38. JM Baisch JD Capra 1992 Analysis of HLA genotypes and susceptibility to insulin-dependent diabetes mellitus: association maps telomeric to HLA-DP Scand J Immunol 36 331 340 1502500 10.1111/j.1365-3083.1992.tb03106.x 1:CAS:528:DyaK3sXjsleluw%3D%3D
39. S Johansson BA Lie F Pociot J Nerup A Cambon-Thomsen I Kockum, et al. 2003 HLA associations in type 1 diabetes: DPB1 alleles may act as markers of other HLA-complex susceptibility genes Tissue Antigens 61 344 351 12753653 10.1034/j.1399-0039.2003.00055.x 1:CAS:528:DC%2BD3sXkslemtb0%3D (Pubitemid 36605667)
40. BA Lie HE Akselsen G Joner K Dahl-Jorgensen KS Ronningen E Thorsby, et al. 1997 HLA associations in insulin-dependent diabetes mellitus: no independent association to particular DP genes Hum Immunol 55 170 175 9361969 10.1016/S0198-8859(97)00095-5 1:CAS:528:DyaK2sXnsVeis74%3D (Pubitemid 27467989)
41. JC Mbanya E Sobngwi DN Mbanya 2001 HLA-DRB1, -DQA1, -DQB1 and DPB1 susceptibility alleles in Cameroonian type 1 diabetes patients and controls Eur J Immunogenet 28 459 462 11532022 10.1046/j.0960-7420.2001.00247.x 1:CAS:528:DC%2BD3MXnvVGitL8%3D (Pubitemid 32758422)
42. MD Varney AM Valdes JA Carlson JA Noble BD Tait P Bonella, et al. 2010 HLA DPA1, DPB1 alleles and haplotypes contribute to the risk associated with type 1 diabetes: analysis of the type 1 diabetes genetics consortium families Diabetes 59 2055 2062 20424227 10.2337/db09-0680 1:CAS:528:DC%2BC3cXhtVOlsbjK This paper summarizes the results of T1D association analyses of the HLA class II genes encoding the DP molecule in the T1DGC samples
43. DV Serreze TM Holl MP Marron RT Graser EA Johnson C Choisy-Rossi, et al. 2004 MHC class II molecules play a role in the selection of autoreactive class I-restricted CD8 T cells that are essential contributors to type 1 diabetes development in nonobese diabetic mice J Immunol 172 871 879 14707058 1:CAS:528:DC%2BD2cXnvVCh (Pubitemid 38113744)
44. K Inoue H Ikegami T Fujisawa S Noso K Nojima N Babaya, et al. 2004 Allelic variation in class I K gene as candidate for a second component of MHC-linked susceptibility to type 1 diabetes in non-obese diabetic mice Diabetologia 47 739 747 15298352 10.1007/s00125-004-1370-2 1:CAS:528: DC%2BD2cXjtlOqsb0%3D (Pubitemid 38658377)
45. K Nakanishi T Kobayashi T Murase T Naruse Y Nose H Inoko 1999 Human leukocyte antigen-A24 and -DQA1*0301 in Japanese insulin-dependent diabetes mellitus: independent contributions to susceptibility to the disease and additive contributions to acceleration of beta-cell destruction J Clin Endocrinol Metab 84 3721 3725 10523020 10.1210/jc.84.10.3721 1:CAS:528:DyaK1MXms1Ohur0%3D (Pubitemid 30645231)
46. JA Noble AM Valdes MD Varney JA Carlson P Moonsamy AL Fear, et al. 2010 HLA class I and genetic susceptibility to type 1 diabetes: results from the Type 1 Diabetes Genetics Consortium Diabetes 59 2972 2979 20798335 10.2337/db10-0699 1:CAS:528:DC%2BC3cXhsV2nsb3P This paper describes the results of T1D association for HLA class I A, B, and C genes from the T1DGC samples
47. 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 15784469 10.1016/j.humimm.2004.12.001 1:CAS:528:DC%2BD2MXisVWqtrs%3D (Pubitemid 40395251)
48. EE Baschal PR Baker KR Eyring JC Siebert JM Jasinski GS Eisenbarth 2011 The HLA-B*3906 allele imparts a high risk of diabetes only on specific HLA-DR/DQ haplotypes Diabetologia 54 1702 1709 21533899 10.1007/s00125-011-2161- 1 1:STN:280:DC%2BC3MrosFSrtg%3D%3D
49. F Cucca R Lampis F Frau D Macis E Angius P Masile, et al. 1995 The distribution of DR4 haplotypes in Sardinia suggests a primary association of type I diabetes with DRB1 and DQB1 loci Hum Immunol 43 301 308 7499178 10.1016/0198-8859(95)00042-3 1:CAS:528:DyaK2MXotVajsrs%3D
50. F Cucca F Muntoni R Lampis F Frau L Argiolas M Silvetti, et al. 1993 Combinations of specific DRB1, DQA1, DQB1 haplotypes are associated with insulin-dependent diabetes mellitus in Sardinia Hum Immunol 37 85 94 8226139 10.1016/0198-8859(93)90146-R 1:CAS:528:DyaK2cXhtVCku7g%3D (Pubitemid 23259993)
51. G Hauptmann S Bahram 2004 Genetics of the central MHC Curr Opin Immunol 16 668 672 15342015 10.1016/j.coi.2004.07.001 1:CAS:528:DC%2BD2cXntleksbc%3D (Pubitemid 39165896)
52. S Johansson BA Lie JA Todd F Pociot J Nerup A Cambon-Thomsen, et al. 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 12595901 10.1038/sj.gene.6363917 1:CAS:528:DC%2BD3sXhsVCmur4%3D (Pubitemid 38967574)
53. JA Noble AM Valdes JA Lane AE Green HA Erlich 2006 Linkage disequilibrium with predisposing DR3 haplotypes accounts for apparent effects of tumor necrosis factor and lymphotoxin-alpha polymorphisms on type 1 diabetes susceptibility Hum Immunol 67 999 1004 17174749 10.1016/j.humimm.2006.10.002 1:CAS:528:DC%2BD28XhtlaktLrN (Pubitemid 44894643)
54. MC Eike M Olsson DE Undlien K Dahl-Jorgensen G Joner KS Ronningen, et al. 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 18987644 10.1038/gene.2008.88 1:CAS:528:DC%2BD1MXisFeltLo%3D
55. AM Valdes NK Arden A Tamm K Kisand S Doherty E Pola, et al. 2010 A meta-analysis of interleukin-6 promoter polymorphisms on risk of hip and knee osteoarthritis Osteoarthritis Cartilage 18 699 704 20175976 10.1016/j.joca.2009. 12.012 1:STN:280:DC%2BC3czgt1SgtQ%3D%3D
56. JC Roach K Deutsch S Li AF Siegel LM Bekris DC Einhaus, et al. 2006 Genetic mapping at 3-kilobase resolution reveals inositol 1,4,5-triphosphate receptor 3 as a risk factor for type 1 diabetes in Sweden Am J Hum Genet 79 614 627 16960798 10.1086/507876 1:CAS:528:DC%2BD28XhtVChur3L (Pubitemid 44452739)
57. HQ Qu L Marchand A Szymborski R Grabs C Polychronakos 2008 The association between type 1 diabetes and the ITPR3 gene polymorphism due to linkage disequilibrium with HLA class II Genes Immun 9 264 266 18340361 10.1038/gene.2008.12 1:CAS:528:DC%2BD1cXkvFylu7g%3D (Pubitemid 351584193)
58. TA Aly EE Baschal MM Jahromi MS Fernando SR Babu TE Fingerlin, et al. 2008 Analysis of single nucleotide polymorphisms identifies major type 1A diabetes locus telomeric of the major histocompatibility complex Diabetes 57 770 776 18065518 10.2337/db07-0900 1:CAS:528:DC%2BD1cXjt1Churk%3D
59. MK Viken A Blomhoff M Olsson HE Akselsen F Pociot J Nerup, et al. 2009 Reproducible association with type 1 diabetes in the extended class I region of the major histocompatibility complex Genes Immun 10 323 333 19295542 10.1038/gene.2009.13 1:CAS:528:DC%2BD1MXms12htb8%3D
60. Bossuyt P. In Evidence-based laboratory medicine: principles, practice, and outcomes Washington, DC, USA, AACC Press, 2007, p. 67-81.
61. DG Clayton 2009 Prediction and interaction in complex disease genetics: experience in type 1 diabetes PLoS Genet 5 e1000540 19584936 10.1371/journal.pgen.1000540
62. Aly TA, Ide A, Humphrey K, Barker JM, Steck A, Erlich HA, Yu L, Miao D, Redondo MJ, McFann K, Roberts CM, Babu SR, Norris JM, Eisenbarth GS, Rewers MJ: Genetic prediction of autoimmunity: initial oligogenic prediction of anti-islet autoimmunity amongst DR3/DR4-DQ8 relatives of patients with type 1A diabetes. J Autoimmun 25 2005, Suppl:40-45. (Pubitemid 41728043)
63. TA Aly A Ide MM Jahromi JM Barker MS Fernando SR Babu, et al. 2006 Extreme genetic risk for type 1A diabetes Proc Natl Acad Sci U S A 103 14074 14079 16966600 10.1073/pnas.0606349103 1:CAS:528:DC%2BD28XhtVCqs7jN (Pubitemid 44452982)
64. B Keymeulen E Vandemeulebroucke AG Ziegler C Mathieu L Kaufman G Hale, et al. 2005 Insulin needs after CD3-antibody therapy in new-onset type 1 diabetes N Engl J Med 352 2598 2608 15972866 10.1056/NEJMoa043980 1:CAS:528: DC%2BD2MXls1Wqu7k%3D (Pubitemid 41007846)
65. F Cucca R Lampis M Congia E Angius S Nutland SC Bain, et al. 2001 A correlation between the relative predisposition of MHC class II alleles to type 1 diabetes and the structure of their proteins Hum Mol Genet 10 2025 2037 11590120 10.1093/hmg/10.19.2025 1:CAS:528:DC%2BD3MXnsl2ktL0%3D (Pubitemid 32998815)
66. A Petrone TL Bugawan CA Mesturino L Nistico A Galgani G Giorgi, et al. 2001 The distribution of HLA class II susceptible/protective haplotypes could partially explain the low incidence of type 1 diabetes in continental Italy (Lazio region) Tissue Antigens 58 385 394 11929589 10.1034/j.1399-0039.2001. 580607.x 1:CAS:528:DC%2BD38XislCls7Y%3D (Pubitemid 34203100)
67. Pugliese A, Dorman JS, Steenkiste A. The 13th International Histocompatibility Working Group for Type 1 Diabetes (T1D) Joint Report. In: Hanson JA, editor. 13th International Histocompatibility Workshop and Conference. Seattle: IHWG Press; 2007. p. 788-96.
68. R Hermann H Turpeinen AP Laine R Veijola M Knip O Simell, et al. 2003 HLA DR-DQ-encoded genetic determinants of childhood-onset type 1 diabetes in Finland: an analysis of 622 nuclear families Tissue Antigens 62 162 169 12889996 10.1034/j.1399-0039.2003.00071.x 1:CAS:528:DC%2BD3sXntlajsbY%3D (Pubitemid 36981422)
69. R Hermann CH Mijovic M Rayner N Croft MA Kelly D Jenkins, et al. 2001 HLA alleles and IDDM in children in Hungary: a comparison with Finland Hum Immunol 62 391 398 11295472 10.1016/S0198-8859(01)00224-5 1:CAS:528:DC%2BD3MXisF2lu7c%3D (Pubitemid 32298982)
70. A Petrone T Battelino C Krzisnik T Bugawan H Erlich U Di Mario, et al. 2002 Similar incidence of type 1 diabetes in two ethnically different populations (Italy and Slovenia) is sustained by similar HLA susceptible/protective haplotype frequencies Tissue Antigens 60 244 253 12445307 10.1034/j.1399-0039.2002.600306.x 1:CAS:528:DC%2BD38Xps1Kltbo%3D (Pubitemid 35398827)
71. G Saruhan-Direskeneli FA Uyar F Bas H Gunoz R Bundak N Saka, et al. 2000 HLA-DR and -DQ associations with insulin-dependent diabetes mellitus in a population of Turkey Hum Immunol 61 296 302 10689119 10.1016/S0198-8859(99) 00182-2 1:CAS:528:DC%2BD3cXht1Kqt78%3D (Pubitemid 30117797)
72. YW Chang KS Lam BR Hawkins 1998 Strong association between DQA1/DQB1 genotype and early-onset IDDM in Chinese: the association is with alleles rather than specific residues Eur J Immunogenet 25 273 280 9777326 10.1046/j.1365-2370.1998.00109.x 1:STN:280:DyaK1cvltVGjsw%3D%3D (Pubitemid 28408289)
73. SH Chan AC Thai YN Lin KF Liu GB Wee 1995 Influence of gender and age at onset on the HLA associations in Chinese with insulin-dependent diabetes mellitus Hum Immunol 44 175 180 8666554 10.1016/0198-8859(95)00085-2 1:STN:280:DyaK283ksFKjsA%3D%3D (Pubitemid 26006726)
74. TL Bugawan W Klitz M Alejandrino J Ching A Panelo CM Solfelix, et al. 2002 The association of specific HLA class I and II alleles with type 1 diabetes among Filipinos Tissue Antigens 59 452 469 12445315 10.1034/j.1399-0039.2002. 590602.x 1:CAS:528:DC%2BD38XnvVynt78%3D (Pubitemid 35034465)
75. HA Erlich A Zeidler J Chang S Shaw LJ Raffel W Klitz, et al. 1993 HLA class II alleles and susceptibility and resistance to insulin dependent diabetes mellitus in Mexican-American families Nat Genet 3 358 364 7981758 10.1038/ng0493-358 1:CAS:528:DyaK3sXisFamsL0%3D (Pubitemid 23112964)