#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Epistatic interactions between killer immunoglobulin-like receptors and human leukocyte antigen ligands are associated with ankylosing spondylitis


Autoři: Aimee L. Hanson aff001;  ;  Damjan Vukcevic aff002;  Stephen Leslie aff002;  Jessica Harris aff005;  Kim-Anh Lê Cao aff002;  Tony J. Kenna aff005;  Matthew A. Brown aff005
Působiště autorů: University of Queensland Diamantina Institute, University of Queensland, Brisbane, Queensland, Australia aff001;  Melbourne Integrative Genomics, School of Mathematics and Statistics, University of Melbourne, Parkville, Victoria, Australia aff002;  Data Science, Murdoch Children’s Research Institute, Parkville, Victoria, Australia aff003;  School of Biosciences, University of Melbourne, Parkville, Victoria Australia aff004;  Institute of Health and Biomedical Innovation, Queensland University of Technology, Brisbane, Queensland, Australia aff005;  Translational Research Institute, Princess Alexandra Hospital, Brisbane, Queensland, Australia aff006;  Translational Research Institute, Brisbane, Queensland, Australia aff006
Vyšlo v časopise: Epistatic interactions between killer immunoglobulin-like receptors and human leukocyte antigen ligands are associated with ankylosing spondylitis. PLoS Genet 16(8): e32767. doi:10.1371/journal.pgen.1008906
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1008906

Souhrn

The killer immunoglobulin-like receptors (KIRs), found predominantly on the surface of natural killer (NK) cells and some T-cells, are a collection of highly polymorphic activating and inhibitory receptors with variable specificity for class I human leukocyte antigen (HLA) ligands. Fifteen KIR genes are inherited in haplotypes of diverse gene content across the human population, and the repertoire of independently inherited KIR and HLA alleles is known to alter risk for immune-mediated and infectious disease by shifting the threshold of lymphocyte activation. We have conducted the largest disease-association study of KIR-HLA epistasis to date, enabled by the imputation of KIR gene and HLA allele dosages from genotype data for 12,214 healthy controls and 8,107 individuals with the HLA-B*27-associated immune-mediated arthritis, ankylosing spondylitis (AS). We identified epistatic interactions between KIR genes and their ligands (at both HLA subtype and allele resolution) that increase risk of disease, replicating analyses in a semi-independent cohort of 3,497 cases and 14,844 controls. We further confirmed that the strong AS-association with a pathogenic variant in the endoplasmic reticulum aminopeptidase gene ERAP1, known to alter the HLA-B*27 presented peptidome, is not modified by carriage of the canonical HLA-B receptor KIR3DL1/S1. Overall, our data suggests that AS risk is modified by the complement of KIRs and HLA ligands inherited, beyond the influence of HLA-B*27 alone, which collectively alter the proinflammatory capacity of KIR-expressing lymphocytes to contribute to disease immunopathogenesis.

Klíčová slova:

Alleles – Ankylosing spondylitis – Genetic loci – Haplotypes – Homozygosity – Medical risk factors – Single nucleotide polymorphisms – Variant genotypes


Zdroje

1. Brewerton DA, Cafrey M, Hart FD, James DCO, Nicholls A, Sturrock RD. Ankylosing Spondylitis and HL-A 27. Lancet. 1973: 904–7. doi: 10.1016/s0140-6736(73)91360-3 4123836

2. Schlosstein L, Terasaki PI, Bluestone R, Pearson CM. High association of an HL-A antigen, W27, with ankylosing spondylitis. N Engl J Med. 1973;288(14): 704–6. doi: 10.1056/NEJM197304052881403 4688372

3. Wellcome Trust Case Control Consortium, Australo-Anglo-American Spondylitis Consortium, Burton PR, Clayton DG, Cardon LR, Craddock N, et al. Association scan of 14,500 nonsynonymous SNPs in four diseases identifies autoimmunity variants. Nat Genet. 2007;39(11): 1329–37. doi: 10.1038/ng.2007.17 17952073

4. Evans DM, Spencer CC, Pointon JJ, Su Z, Harvey D, Kochan G, et al. Interaction between ERAP1 and HLA-B27 in ankylosing spondylitis implicates peptide handling in the mechanism for HLA-B27 in disease susceptibility. Nat Genet. 2011;43(8): 761–7. doi: 10.1038/ng.873 21743469

5. International Genetics of Ankylosing Spondylitis Consortium, Cortes A, Hadler J, Pointon JP, Robinson PC, Karaderi T, et al. Identification of multiple risk variants for ankylosing spondylitis through high-density genotyping of immune-related loci. Nat Genet. 2013;45(7): 730–8. doi: 10.1038/ng.2667 23749187

6. Australo-Anglo-American Spondyloarthritis Consortium Reveille JD, Sims AM, Danoy P, Evans DM, Leo P, et al. Genome-wide association study of ankylosing spondylitis identifies non-MHC susceptibility loci. Nat Genet. 2010;42(2): 123–7. doi: 10.1038/ng.513 20062062

7. Cortes A, Pulit SL, Leo PJ, Pointon JJ, Robinson PC, Weisman MH, et al. Major histocompatibility complex associations of ankylosing spondylitis are complex and involve further epistasis with ERAP1. Nat Commun. 2015;6(7146).

8. Ellinghaus D, Jostins L, Spain SL, Cortes A, Bethune J, Han B, et al. Analysis of five chronic inflammatory diseases identifies 27 new associations and highlights disease-specific patterns at shared loci. Nat Genet. 2016;48: 510–8. doi: 10.1038/ng.3528 26974007

9. Li Z, Akar S, Yarkan H, Lee SK, Cetin P, Can G, et al. Genome-wide association study in Turkish and Iranian populations identify rare familial Mediterranean fever gene (MEFV) polymorphisms associated with ankylosing spondylitis. PLoS genetics. 2019;15(4): e1008038. doi: 10.1371/journal.pgen.1008038 30946743

10. Kuroki K, Furukawa A, Maenaka K. Molecular recognition of paired receptors in the immune system. Front Microbiol. 2012;3: 429. doi: 10.3389/fmicb.2012.00429 23293633

11. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9(5): 495–502. doi: 10.1038/ni1581 18425106

12. Saunders PM, Vivian JP, O’Connor GM, Sullivan LC, Pymm P, Rossjohn J, et al. A bird’s eye view of NK cell receptor interactions with their MHC class I ligands. Immunol Rev. 2015;267: 148–66. doi: 10.1111/imr.12319 26284476

13. Martin MP, Qi Y, Gao X, Yamada E, Martin JN, Pereyra F, et al. Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet. 2007;39(6): 733–40. doi: 10.1038/ng2035 17496894

14. Martin MP, Naranbhai V, Shea PR, Qi Y, Ramsuran V, Vince N, et al. Killer cell immunoglobulin-like receptor 3DL1 variation modifies HLA-B*57 protection against HIV-1. J Clin Invest. 2018;128(5): 1903–12. doi: 10.1172/JCI98463 29461980

15. Kazura JW, Hirayasu K, Ohashi J, Kashiwase K, Hananantachai H, Naka I, et al. Significant Association of KIR2DL3-HLA-C1 Combination with Cerebral Malaria and Implications for Co-evolution of KIR and HLA. PLoS Pathog. 2012;8(3): e1002565. doi: 10.1371/journal.ppat.1002565 22412373

16. Diaz-Pena R, Vidal-Castineira JR, Moro-Garcia MA, Alonso-Arias R, Castro-Santos P. Significant association of the KIR2DL3/HLA-C1 genotype with susceptibility to Crohn's disease. Hum Immunol. 2016;77(1): 104–9. doi: 10.1016/j.humimm.2015.10.020 26542067

17. Smigoc Schweiger D, Mendez A, Kunilo Jamnik S, Bratanic N, Bratina N, Battelino T, et al. Genetic risk for co-occurrence of type 1 diabetes and celiac disease is modified by HLA-C and killer immunoglobulin-like receptors. Tissue Antigens. 2014;84(5): 471–8. doi: 10.1111/tan.12450 25329633

18. Nelson GW, Martin MP, Gladman D, Wade J, Trowsdale J, Carrington M. Cutting Edge: Heterozygote Advantage in Autoimmune Disease: Hierarchy of Protection/Susceptibility Conferred by HLA and Killer Ig-Like Receptor Combinations in Psoriatic Arthritis. J Immunol. 2004;173(7): 4273–6. doi: 10.4049/jimmunol.173.7.4273 15383555

19. Bao X, Hanson AL, Madeleine MM, Wang SS, Schwartz SM, Newell F, et al. HLA and KIR Associations of Cervical Neoplasia. J Infect Dis. 2018;218(12): 2006–15. doi: 10.1093/infdis/jiy483 30099516

20. Hernandez EG, Partida-Rodriguez O, Camorlinga-Ponce M, Nieves-Ramirez M, Ramos-Vega I, Torres J, et al. Genotype B of Killer Cell Immunoglobulin-Like Receptor is Related with Gastric Cancer Lesions. Sci Rep. 2018;8(1): 6104. doi: 10.1038/s41598-018-24464-2 29666399

21. Martin AM, Freitas EM, Witt CS, Christiansen FT. The genomic organization and evolution of the natural killer immunoglobulin-like receptor (KIR) gene cluster. Immunogenetics. 2000;51: 268–80. doi: 10.1007/s002510050620 10803839

22. Pyo C-W, Wang R, Vu Q, Cereb N, Yang SY, Duh F-M, et al. Recombinant structures expand and contract inter and intragenic diversification at the KIR locus. BMC Genomics. 2013;14(89).

23. Jiang W, Johnson C, Jayaraman J, Simecek N, Noble J, Moffatt MF, et al. Copy number variation leads to considerable diversity for B but not A haplotypes of the human KIR genes encoding NK cell receptors. Genome Res. 2012;22(10): 1845–54. doi: 10.1101/gr.137976.112 22948769

24. Pyo CW, Guethlein LA, Vu Q, Wang R, Abi-Rached L, Norman PJ, et al. Different patterns of evolution in the centromeric and telomeric regions of group A and B haplotypes of the human killer cell Ig-like receptor locus. PLoS One. 2010;5(12): e15115. doi: 10.1371/journal.pone.0015115 21206914

25. Santourlidis S, Trompeter HI, Weinhold S, Eisermann B, Meyer KL, Wernet P, et al. Crucial Role of DNA Methylation in Determination of Clonally Distributed Killer Cell Ig-like Receptor Expression Patterns in NK Cells. J Immunol. 2002;169(8): 4253–61. doi: 10.4049/jimmunol.169.8.4253 12370356

26. Chan H-W, Kurago ZB, Stewart CA, Wilson MJ, Martin MP, Mace BE, et al. DNA Methylation Maintains Allele-specific KIR Gene Expression in Human Natural Killer Cells. The Journal of Experimental Medicine. 2003;197(2): 245–55. doi: 10.1084/jem.20021127 12538663

27. Boudreau JE, Mulrooney TJ, Le Luduec JB, Barker E, Hsu KC. KIR3DL1 and HLA-B Density and Binding Calibrate NK Education and Response to HIV. J Immunol. 2016.

28. Saunders PM, Pymm P, Pietra G, Hughes VA, Hitchen C, O'Connor GM, et al. Killer cell immunoglobulin-like receptor 3DL1 polymorphism defines distinct hierarchies of HLA class I recognition. J Exp Med. 2016;213(5): 791–807. doi: 10.1084/jem.20152023 27045007

29. Carr WH, Pando MJ, Parham P. KIR3DL1 Polymorphisms That Affect NK Cell Inhibition by HLA-Bw4 Ligand. J Immunol. 2005;175(8): 5222–9. doi: 10.4049/jimmunol.175.8.5222 16210627

30. Frazier WR, Steiner N, Hou L, Dakshanamurthy S, Hurley CK. Allelic variation in KIR2DL3 generates a KIR2DL2-like receptor with increased binding to its HLA-C ligand. J Immunol. 2013;190(12): 6198–208. doi: 10.4049/jimmunol.1300464 23686481

31. Vilches C, Gardiner CM, Parham P. Gene Structure and Promoter Variation of Expressed and Nonexpressed Variants of the KIR2DL5 Gene. J Immunol. 2000;165(11): 6416–21. doi: 10.4049/jimmunol.165.11.6416 11086080

32. Burshtyn DN, Scharenberg AM, Wagtmann N, Rajagopalan S, Berrada K, Yi T, et al. Recruitment of Tyrosine Phosphatase HCP (SHP-1) by the Killer Cell Inhibitory Receptor. Immunity. 1996;4(1): 77–85. doi: 10.1016/s1074-7613(00)80300-3 8574854

33. Ljunggren H-G, Karre K. In search of the 'missing self': MHC molecules and NK cell recognition. Immunol Today. 1990;11(7).

34. Peruzzi M, Parker KC, Malnati EOLaMS. Peptide sequence requirements for the recognition of HLA-B*2705 by specific natural killer cells. J Immunol. 1996;157: 3350–6. 8871631

35. Rajagopalan S, Long EO. The direct binding of a p58 killer cell inhibitory receptor to human histocompatibility leukocyte antigen (HLA)-Cw4 exhibits peptide selectivity. The Journal of Experimental Medicine. 1997;185(8): 1523–8. doi: 10.1084/jem.185.8.1523 9126935

36. Hansasuta P, Dong T, Thananchai H, Weekes M, Willberg C, Aldemir H, et al. Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific. Eur J Immunol. 2004;34: 1673–6. doi: 10.1002/eji.200425089 15162437

37. Stewart CA, Laugier-Anfossi F, Vely F, Saulquin X, Riedmuller J, Tisserant A, et al. Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc Natl Acad Sci U S A. 2005;102(37): 13224–9. doi: 10.1073/pnas.0503594102 16141329

38. Sanjanwala B, Draghi M, Norman PJ, Guethlein LA, Parham P. Polymorphic Sites Away from the Bw4 Epitope That Affect Interaction of Bw4+ HLA-B with KIR3DL1. J Immunol. 2008;181(9): 6293–300. doi: 10.4049/jimmunol.181.9.6293 18941220

39. Gumperz JE, Barber LD, Valiante NM, Percival L, Phillips JH, Lanier LL, et al. Conserved and variable residues within the Bw4 motif of HLA-B make separable contributions to recognition by the NKB1 killer cell-inhibitory receptor. J Immunol. 1997;158: 5237–41. 9164941

40. Cella M, Longo A, Ferrara GB, Strominger JL, Colonna M. NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80. J Exp Med. 1994;180: 1235–42. doi: 10.1084/jem.180.4.1235 7931060

41. Moesta AK, Norman PJ, Yawata M, Yawata N, Gleimer M, Parham P. Synergistic Polymorphism at Two Positions Distal to the Ligand-Binding Site Makes KIR2DL2 a Stronger Receptor for HLA-C Than KIR2DL3. J Immunol. 2008;180(6): 3969–79. doi: 10.4049/jimmunol.180.6.3969 18322206

42. Biassoni R, Pessino A, Malaspina A, Cantoni C, Bottino C, Sivori S, et al. Role of amino acid position 70 in the binding affinity of p50.1 and p58.1 receptors for HLA-Cw4 molecules. Eur J Immunol. 1997;27: 3095–9. doi: 10.1002/eji.1830271203 9464792

43. Gomez MV, Reyburn HT, Erskine RA, Strominger J. Differential binding to HLA-C of p50-activating and p58-inhibitory natural killer cell receptors. Proceedings of the National Academy of Sciences. 1998;95: 14326–31.

44. Thiruchelvam-Kyle L, Hoelsbrekken SE, Saether PC, Gyllensten Bjørnsen E, Pende D, Fossum S, et al. The Activating Human NK Cell Receptor KIR2DS2 Recognizes a β2-Microglobulin–Independent Ligand on Cancer Cells. J Immunol. 2017: 1600930.

45. Goodridge JP, Burian A, Lee N, Geraghty DE. HLA-F and MHC class I open conformers are ligands for NK cell Ig-like receptors. J Immunol. 2013;191(7): 3553–62. doi: 10.4049/jimmunol.1300081 24018270

46. Burian A, Wang KL, Finton KA, Lee N, Ishitani A, Strong RK, et al. HLA-F and MHC-I Open Conformers Bind Natural Killer Cell Ig-Like Receptor KIR3DS1. PLoS One. 2016;11(9): e0163297. doi: 10.1371/journal.pone.0163297 27649529

47. O'Connor GM, Vivian JP, Gostick E, Pymm P, Lafont BA, Price DA, et al. Peptide-Dependent Recognition of HLA-B*57:01 by KIR3DS1. J Virol. 2015;89(10): 5213–21. doi: 10.1128/JVI.03586-14 25740999

48. Winter CC, Long E. A Single Amino Acid in the p58 Killer Cell Inhibitory Receptor Controls the Ability of Natural Killer Cells to Discriminate Between the Two Groups of HLA-C Allotypes. J Immunol. 1997;158: 4026–8. 9126959

49. Rajagopalan S, Long EO. A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. The Journal of Experimental Medicine. 1999;189(7): 1093–9. doi: 10.1084/jem.189.7.1093 10190900

50. Döhring C, Scheidegger D, Samaridis J, Cella M, Colonna M. A Human Killer Inhibitory Receptor Specific for HLA-A. J Immunol. 1996;156: 3098–101. 8617928

51. Pende D, Biassoni R, Cantoni C, Verdiani S, Falco M, Donato CD, et al. The Natural Killer Cell Receptor Specific for HLA-A Ailotypes- A Novel Member of the p58:p70 Family of Inhibitory Receptors That Is Characterized by Three Immunoglobulin-like Domains and Is Expressed as a 140-kD Disulphide-linked Dimer>. J Exp Med. 1996;184: 505–18. doi: 10.1084/jem.184.2.505 8760804

52. Wong-Baeza I, Ridley A, Shaw J, Hatano H, Rysnik O, McHugh K, et al. KIR3DL2 binds to HLA-B27 dimers and free H chains more strongly than other HLA class I and promotes the expansion of T cells in ankylosing spondylitis. J Immunol. 2013;190(7): 3216–24. doi: 10.4049/jimmunol.1202926 23440420

53. Liu J, Xiao Z, Ko HL, Shen M, Ren EC. Activating killer cell immunoglobulin-like receptor 2DS2 binds to HLA-A*11. Proc Natl Acad Sci U S A. 2014;111(7): 2662–7. doi: 10.1073/pnas.1322052111 24550293

54. David G, Djaoud Z, Willem C, Legrand N, Rettman P, Gagne K, et al. Large Spectrum of HLA-C Recognition by Killer Ig-like Receptor (KIR)2DL2 and KIR2DL3 and Restricted C1 Specificity of KIR2DS2: Dominant Impact of KIR2DL2/KIR2DS2 on KIR2D NK Cell Repertoire Formation. J Immunol. 2013;191(9): 4778–88. doi: 10.4049/jimmunol.1301580 24078689

55. Graef T, Moesta AK, Norman PJ, Abi-Rached L, Vago L, Older Aguilar AM, et al. KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. The Journal of Experimental Medicine. 2009;206(11): 2557–72. doi: 10.1084/jem.20091010 19858347

56. Mulrooney TJ, Zhang AC, Goldgur Y, Boudreau JE, Hsu KC. KIR3DS1-Specific D0 Domain Polymorphisms Disrupt KIR3DL1 Surface Expression and HLA Binding. J Immunol. 2015;195(3): 1242–50. doi: 10.4049/jimmunol.1500243 26109640

57. Lopez-Larrea C, Blanco-Gelaz MA, Torre-Alonso JC, Bruges Armas J, Suarez-Alvarez B, Pruneda L, et al. Contribution of KIR3DL1/3DS1 to ankylosing spondylitis in human leukocyte antigen-B27 Caucasian populations. Arthritis Res Ther. 2006;8(4): R101. doi: 10.1186/ar1988 16805919

58. Diaz-Pena R, Blanco-Gelaz MA, Suarez-Alvarez B, Martinez-Borra J, Lopez-Vazquez A, Alonso-Arias R, et al. Activating KIR genes are associated with ankylosing spondylitis in Asian populations. Hum Immunol. 2008;69(7): 437–42. doi: 10.1016/j.humimm.2008.04.012 18638658

59. Jiao YL, Ma CY, Wang LC, Cui B, Zhang J, You L, et al. Polymorphisms of KIRs gene and HLA-C alleles in patients with ankylosing spondylitis: possible association with susceptibility to the disease. J Clin Immunol. 2008;28(4): 343–9. doi: 10.1007/s10875-008-9183-6 18297378

60. Harvey D, Pointon JJ, Sleator C, Meenagh A, Farrar C, Sun JY, et al. Analysis of killer immunoglobulin-like receptor genes in ankylosing spondylitis. Ann Rheum Dis. 2009;68(4): 595–8. doi: 10.1136/ard.2008.095927 19019897

61. Diaz-Pena R, Vidal-Castineira JR, Alonso-Arias R, Suarez-Alvarez B, Vicario JL, Solana R, et al. Association of the KIR3DS1*013 and KIR3DL1*004 alleles with susceptibility to ankylosing spondylitis. Arthritis Rheum. 2010;62(4): 1000–6. doi: 10.1002/art.27332 20131260

62. Jiao YL, Zhang BC, You L, Li JF, Zhang J, Ma CY, et al. Polymorphisms of KIR gene and HLA-C alleles: possible association with susceptibility to HLA-B27-positive patients with ankylosing spondylitis. J Clin Immunol. 2010;30(6): 840–4. doi: 10.1007/s10875-010-9444-z 20652381

63. Nowak I, Majorczyk E, Wisniewski A, Pawlik A, Magott-Procelewska M, Passowicz-Muszynska E, et al. Does the KIR2DS5 gene protect from some human diseases? PLoS One. 2010;5(8): e12381. doi: 10.1371/journal.pone.0012381 20865034

64. Zvyagin IV, Mamedov IZ, Britanova OV, Staroverov DB, Nasonov EL, Bochkova AG, et al. Contribution of functional KIR3DL1 to ankylosing spondylitis. Cell Mol Immunol. 2010;7(6): 471–6. doi: 10.1038/cmi.2010.42 20818412

65. Tajik N, Shahsavar F, Poormoghim H, Radjabzadeh MF, Mousavi T, Jalali A. KIR3DL1+HLA-B Bw4Ile80 and KIR2DS1+HLA-C2 combinations are both associated with ankylosing spondylitis in the Iranian population. Int J Immunogenet. 2011;38(5): 403–9. doi: 10.1111/j.1744-313X.2011.01024.x 21797986

66. Wang CM, Wang SH, Jan Wu YJ, Lin JC, Wu J, Chen JY. Human Leukocyte Antigen C*12:02:02 and Killer Immunoglobulin-Like Receptor 2DL5 are Distinctly Associated with Ankylosing Spondylitis in the Taiwanese. Int J Mol Sci. 2017;18(8).

67. Robinson J, Halliwell JA, McWilliam H, Lopez R, Marsh SG. IPD—the Immuno Polymorphism Database. Nucleic Acids Res. 2013;41(Database issue): D1234–40. doi: 10.1093/nar/gks1140 23180793

68. Gardiner CM, Guethlein LA, Shilling HG, Pando M, Carr WH, Rajalingam R, et al. Different NK Cell Surface Phenotypes Defined by the DX9 Antibody Are Due to KIR3DL1 Gene Polymorphism. J Immunol. 2001;166(5): 2992–3001. doi: 10.4049/jimmunol.166.5.2992 11207248

69. Kollnberger S, Bird L, Sun MY, Retiere C, Braud VM, McMichael A, et al. Cell-surface expression and immune receptor recognition of HLA-B27 homodimers. Arthritis Rheum. 2002;46(11): 2972–82. doi: 10.1002/art.10605 12428240

70. Kollnberger S, Chan A, Sun M-Y, Ye Chen L, Wright C, di Gleria K, et al. Interaction of HLA-B27 homodimers with KIR3DL1 and KIR3DL2, unlike HLA-B27 heterotrimers, is independent of the sequence of bound peptide. Eur J Immunol. 2007;37(5): 1313–22. doi: 10.1002/eji.200635997 17407096

71. Ridley A, Hatano H, Wong-Baeza I, Shaw J, Matthews KK, Al-Mossawi H, et al. Activation-Induced Killer Cell Immunoglobulin-like Receptor 3DL2 Binding to HLA–B27 Licenses Pathogenic T Cell Differentiation in Spondyloarthritis. Arthritis Rheumatol. 2016;68(4): 901–14. doi: 10.1002/art.39515 26841353

72. Vukcevic D, Traherne JA, Naess S, Ellinghaus E, Kamatani Y, Dilthey A, et al. Imputation of KIR Types from SNP Variation Data. Am J Hum Genet. 2015;97(4): 593–607. doi: 10.1016/j.ajhg.2015.09.005 26430804

73. Boudreau JE, Le Luduec JB, Hsu KC. Development of a novel multiplex PCR assay to detect functional subtypes of KIR3DL1 alleles. PLoS One. 2014;9(6): e99543. doi: 10.1371/journal.pone.0099543 24919192

74. van der Linden S, Valkenberg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. Arthritis Rheum. 1984;27(4): 361–8. doi: 10.1002/art.1780270401 6231933

75. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, et al. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81(3): 559–75. doi: 10.1086/519795 17701901

76. Price AL, Weale ME, Patterson N, Myers SR, Need AC, Shianna KV, et al. Long-range LD can confound genome scans in admixed populations. Am J Hum Genet. 2008;83(1): 132–5; author reply 5–9. doi: 10.1016/j.ajhg.2008.06.005 18606306

77. Delaneau O, Marchini J, Zagury JF. A linear complexity phasing method for thousands of genomes. Nature methods. 2012;9(2): 179–81.

78. McCarthy S, Das S, Kretzschmar W, Delaneau O, Wood AR, Teumer A, et al. A reference panel of 64,976 haplotypes for genotype imputation. Nat Genet. 2016;48(10): 1279–83. doi: 10.1038/ng.3643 27548312

79. Gonzalez-Galarza FF, Takeshita LY, Santos EJ, Kempson F, Maia MH, da Silva AL, et al. Allele frequency net 2015 update: new features for HLA epitopes, KIR and disease and HLA adverse drug reaction associations. Nucleic Acids Res. 2015;43(Database issue): D784–8. doi: 10.1093/nar/gku1166 25414323

80. Motyer A, Vukcevic D, Dilthey A, Donnelly P, McVean G, Leslie S. Practical Use of Methods for Imputation of HLA Alleles from SNP Genotype Data. bioRxive. 2016.

81. Das S, Forer L, Schonherr S, Sidore C, Locke AE, Kwong A, et al. Next-generation genotype imputation service and methods. Nat Genet. 2016;48(10): 1284–7. doi: 10.1038/ng.3656 27571263

82. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2015.

83. Warnes G, Gorjanc G, Leisch F, Man M. genetics: Population Genetics. R package version 1381. 2013.

84. Pando MJ, Gardiner CM, Gleimer M, McQueen KL, Parham P. The Protein Made from a Common Allele of KIR3DL1 (3DL1*004) Is Poorly Expressed at Cell Surfaces due to Substitution at Positions 86 in Ig Domain 0 and 182 in Ig Domain 1. J Immunol. 2003;171(12): 6640–9. doi: 10.4049/jimmunol.171.12.6640 14662867

85. Luque I, Solana R, Galiani MD, Gonzalez R, Garcia F, Castro JALd, et al. Threonine 80 on HLA-B27 confers protection against lysis by a group of natural killer clones. Eur J Immunol. 1996;26: 1974–7. doi: 10.1002/eji.1830260845 8765048

86. Sanz-Bravo A, Campos J, Mazariegos MS, Lopez de Castro JA. Dominant role of the ERAP1 polymorphism R528K in shaping the HLA-B27 peptidome through differential processing determined by multiple peptide residues. Arthritis & rheumatology. 2015;67(3): 692–701.

87. Martin-Esteban A, Sanz-Bravo A, Guasp P, Barnea E, Admon A, Lopez de Castro JA. Separate effects of the ankylosing spondylitis associated ERAP1 and ERAP2 aminopeptidases determine the influence of their combined phenotype on the HLA-B*27 peptidome. J Autoimmun. 2017.

88. Stern M, Ruggeri L, Capanni M, Mancusi A, Velardi A. Human leukocyte antigens A23, A24, and A32 but not A25 are ligands for KIR3DL1. Blood. 2008;112(3): 708–10. doi: 10.1182/blood-2008-02-137521 18502829

89. Kaser A, Lee AH, Franke A, Glickman JN, Zeissig S, Tilg H, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell. 2008;134(5): 743–56. doi: 10.1016/j.cell.2008.07.021 18775308

90. Ulianich L, Terrazzano G, Annunziatella M, Ruggiero G, Beguinot F, Di Jeso B. ER stress impairs MHC Class I surface expression and increases susceptibility of thyroid cells to NK-mediated cytotoxicity. Biochim Biophys Acta. 2011;1812(4): 431–8. doi: 10.1016/j.bbadis.2010.12.013 21199669

91. Chewning JH, Gudme CN, Hsu KC, Selvakumar A, Dupont B. KIR2DS1-Positive NK Cells Mediate Alloresponse against the C2 HLA-KIR Ligand Group In Vitro. J Immunol. 2007;179(2): 854–68. doi: 10.4049/jimmunol.179.2.854 17617576

92. Chapel A, Garcia-Beltran WF, Holzemer A, Ziegler M, Lunemann S, Martrus G, et al. Peptide-specific engagement of the activating NK cell receptor KIR2DS1. Sci Rep. 2017;7(1): 2414. doi: 10.1038/s41598-017-02449-x 28546555

93. Luszczek W, Manczak M, Cislo M, Nockowski P, Wisniewski A, Jasek M, et al. Gene for the activating natural killer cell receptor, KIR2DS1, is associated with susceptibility to psoriasis vulgaris. Hum Immunol. 2004;65(7): 758–66. doi: 10.1016/j.humimm.2004.05.008 15310528

94. Jobim M, Jobim LF, Salim PH, Cestari TF, Toresan R, Gil BC, et al. A study of the killer cell immunoglobulin-like receptor gene KIR2DS1 in a Caucasoid Brazilian population with psoriasis vulgaris. Tissue Antigens. 2008;72(4): 392–6. doi: 10.1111/j.1399-0039.2008.01096.x 18643961

95. Papavasiliou N, Besson C, Roetynck S, Williams F, Orsi L, Amiel C, et al. Association of Killer Cell Immunoglobulin-Like Receptor Genes with Hodgkin's Lymphoma in a Familial Study. PLoS One. 2007;2(5).

96. Pende D, Marcenaro S, Falco M, Martini S, Bernardo ME, Montagna D, et al. Anti-leukemia activity of alloreactive NK cells in KIR ligand-mismatched haploidentical HSCT for pediatric patients- evaluation of the functional role of activating KIR and redefinition of inhibitory KIR specificity. Blood. 2009;113(13): 3119–29. doi: 10.1182/blood-2008-06-164103 18945967


Článek vyšel v časopise

PLOS Genetics


2020 Číslo 8
Nejčtenější tento týden
Nejčtenější v tomto čísle
Kurzy

Zvyšte si kvalifikaci online z pohodlí domova

Důležitost adherence při depresivním onemocnění
nový kurz
Autoři: MUDr. Eliška Bartečková, Ph.D.

Koncepce osteologické péče pro gynekology a praktické lékaře
Autoři: MUDr. František Šenk

Sekvenční léčba schizofrenie
Autoři: MUDr. Jana Hořínková, Ph.D.

Hypertenze a hypercholesterolémie – synergický efekt léčby
Autoři: prof. MUDr. Hana Rosolová, DrSc.

Multidisciplinární zkušenosti u pacientů s diabetem
Autoři: Prof. MUDr. Martin Haluzík, DrSc., prof. MUDr. Vojtěch Melenovský, CSc., prof. MUDr. Vladimír Tesař, DrSc.

Všechny kurzy
Přihlášení
Zapomenuté heslo

Zadejte e-mailovou adresu, se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

#ADS_BOTTOM_SCRIPTS#