KIR Polymorphisms Modulate Peptide-Dependent Binding to an MHC Class I Ligand with a Bw6 Motif

English version České info

Molecular interactions between killer immunoglobulin-like receptors (KIRs) and their MHC class I ligands play a central role in the regulation of natural killer (NK) cell responses to viral pathogens and tumors. Here we identify Mamu-A1*00201 (Mamu-A*02), a common MHC class I molecule in the rhesus macaque with a canonical Bw6 motif, as a ligand for Mamu-KIR3DL05. Mamu-A1*00201 tetramers folded with certain SIV peptides, but not others, directly stained primary NK cells and Jurkat cells expressing multiple allotypes of Mamu-KIR3DL05. Differences in binding avidity were associated with polymorphisms in the D0 and D1 domains of Mamu-KIR3DL05, whereas differences in peptide-selectivity mapped to the D1 domain. The reciprocal exchange of the third predicted MHC class I-contact loop of the D1 domain switched the specificity of two Mamu-KIR3DL05 allotypes for different Mamu-A1*00201-peptide complexes. Consistent with the function of an inhibitory KIR, incubation of lymphocytes from Mamu-KIR3DL05⁺ macaques with target cells expressing Mamu-A1*00201 suppressed the degranulation of tetramer-positive NK cells. These observations reveal a previously unappreciated role for D1 polymorphisms in determining the selectivity of KIRs for MHC class I-bound peptides, and identify the first functional KIR-MHC class I interaction in the rhesus macaque. The modulation of KIR-MHC class I interactions by viral peptides has important implications to pathogenesis, since it suggests that the immunodeficiency viruses, and potentially other types of viruses and tumors, may acquire changes in epitopes that increase the affinity of certain MHC class I ligands for inhibitory KIRs to prevent the activation of specific NK cell subsets.

Vyšlo v časopise: KIR Polymorphisms Modulate Peptide-Dependent Binding to an MHC Class I Ligand with a Bw6 Motif. PLoS Pathog 7(3): e32767. doi:10.1371/journal.ppat.1001316
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1001316

Souhrn

Zdroje

1. LanierLL

2005 NK cell recognition. Annu Rev Immunol 23 225 274

2. ParhamP

2005 MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5 201 214

3. KimS

SunwooJB

YangL

ChoiT

SongY-J

2008 HLA alleles determine differences in human natural killer cell responsiveness and potency. Proc Natl Acad Sci U S A 105 3053 3058

4. ValianteNM

UhrbergM

ShillingHG

Lienert-WeidenbachK

ArnettKL

1997 Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7 739 751

5. SchwartzO

MarechalV

LeGallS

LemonnierF

HeardJ-M

1996 Endocytosis of major histocompatibility complex class I molecules is induced by the HIV-1 Nef protein. Nat Med 2 338 342

6. CohenGB

GandhiRT

DavisDM

MandelboimO

ChenBK

1999 The selective downregulation of class I major histocompatibility complex proteins by HIV-1 protects HIV-infected cells from NK cells. Immunity 10 661 671

7. FaddaL

BorhisG

AhmedP

CheentK

PageonSV

2010 Peptide antagonism as a mechanism for NK cell activation. Proc Natl Acad Sci U S A 107 10160 10165

8. AyersJ

CresswellP

1976 HLA-B specificities and w4, w6 specificities are on the same polypeptide. Eur J Immunol 6 794 799

9. GumperzJE

LitwinV

PhillipsJH

LanierLL

ParhamP

1995 The Bw4 public epitope of HLA-B molecules confers reactivity with natural killer cell clones that express NKB1, a putative HLA receptor. J Exp Med 181 1133 1144

10. MandelboimO

WilsonSB

Vales-GomezM

ReyburnHT

StromingerJL

1997 Self and viral peptides can initiate lysis by autologous natural killer cells. Proc Natl Acad Sci U S A 94 5604 4609

11. ThananchaiH

GillespieG

MartinMP

BashirovaA

YawataN

2007 Allele-specific and peptide-dependent interactions between KIR3DL1 and HLA-A and HLA-B. J Immunol 178 33 37

12. HansasutaP

DongT

ThananchaiH

WeekesM

WillbergC

2004 Recognition of HLA-A3 and HLA-A11 by KIR3DL2 is peptide-specific. Eur J Immunol 34 1673 1679

13. RajagopalanS

LongEO

1997 The direct binding of a p58 killer cell inhibitory receptor to human histocompatibility leukocyte antigen (HLA)-Cw4 exhibits peptide selectivity. J Exp Med 185 1523 1528

14. ZappacostaF

BorregoF

BrooksAG

ParkerKC

ColiganJE

1997 Peptides isolated from HLA-Cw*0304 confer different degrees of protection from natural killer cell-mediated lysis. Proc Natl Acad Sci U S A 94 6313 6318

15. PeruzziM

ParkerKC

LongEO

MalnatiMS

1996 Peptide sequence requirements for the recognition of HLA-B*2705 by specific natural killer cells. J Immunol 157 3350 3356

16. MalnatiMS

PeruzziM

ParkerKC

BiddisonWE

CicconeE

1995 Peptide specificity in the recognition of MHC class I by natural killer cell clones. Science 267 1016 1018

17. FanQR

LongEO

WileyDC

2001 Crystal structure of the human natural killer cell inhibitory receptor KIR2DL1-HLA-Cw4 complex. Nat Immunol 2 452 460

18. BoyingtonJC

MotykaSA

SchuckP

BrooksAG

SunPD

2000 Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC. Nature 405 537 543

19. MartinMP

QiY

GaoX

YamadaE

MartinJN

2007 Innate partnership of HLA-B and KIR3DL1 subtypes against HIV-1. Nat Genet 39 733 740

20. MartinMP

GaoX

LeeJ-H

NelsonGW

DetelsR

2002 Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat Genet 31 429 434

21. KhakooSI

ThioCL

MartinMP

BrooksCR

GaoX

2004 HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305 872 874

22. CarringtonM

WangS

MartinMP

GaoX

SchiffmanM

2005 Hierarchy of resistance to cervical neoplasia mediated by combinations of killer immunoglobulin-like receptor and human leukocyte antigen loci. J Exp Med 201 1069 1075

23. ChenC

BussonM

RochaV

AppertM-L

LepageV

2006 Activating KIR genes are associated with CMV reactivation and survival after non-T-cell depleted HLA-identical sibling bone marrow transplantation for malignant disorders. Bone Marrow Transplant 38 437 444

24. AlterG

MartinMP

TeigenN

CarrWH

SuscovichTJ

2007 Differential natural killer cell-mediated inhibition of HIV-1 replication based on distinct KIR/HLA subtypes. J Exp Med 204 3027 3036

25. LetvinNL

DanielMD

SehgalPK

DesrosiersRC

HuntRD

1985 Induction of AIDS-like disease in macaque monkeys with T-cell tropic retrovirus STLV-III. Science 230 71 73

26. BoysonJE

SchufflebothamC

CadavidLF

UrvaterJA

KnappLA

1996 The MHC class I genes of the rhesus monkey: Different evolutionary histories of the MHC class I and II genes in primates. J Immunol 156 4656 4665

27. AdamsEJ

ParhamP

2001 Species-specific evolution of MHC class I genes in the higher primates. Immunol Rev 183 41 64

28. HershbergerKL

ShyamR

MiuraA

LetvinNL

2001 Diversity of the killer cell Ig-like receptors of rhesus monkeys. J Immunol 166 4380 4390

29. BimberBN

MorelandAJ

WisemanRW

HughesAL

O'ConnorDH

2008 Complete characterization of killer Ig-like receptor (KIR) haplotypes in Mauritian cynomolgus macaques: Novel insights into nonhuman primate KIR gene content and organization. J Immunol 181 6301 6308

30. SambrookJG

BashirovaA

PalmerS

SimsS

TrowsdaleJ

2005 Single haplotype analysis demonstrates rapid evolution of the killer immunoglobulin-like receptor (KIR) loci in primates. Genome Res 15 25 35

31. BlokhuisJH

van der WielMK

DoxiadisGG

BontropRE

2010 The mosaic of KIR haplotypes in rhesus macaques. Immunogenetics 62 295 306

32. KrusePH

RosnerC

WalterL

2010 Characterization of rhesus macaque KIR genotypes and haplotypes. Immunogenetics 62 281 293

33. ReevesRK

GillisJ

WongFE

YuY

ConnoleM

2010 CD16- natural killer cells: enrichment in mucosal and secondary lymphoid tissues and altered function during chronic SIV infection. Blood 115 4439 4446

34. LoffredoJT

SidneyJ

WojewodaC

DoddsE

ReynoldsMR

2004 Idenification of seventeen new simian immunodeficiency virus-derived CD8+ T cell epitopes restricted by the high frequency molecule, Mamu-A*02, and potential escape from CTL recognition. J Immunol 173 5064 5076

35. MingariMC

SchiavettiF

PonteM

VitaleC

MaggiE

1996 Human CD8+ T lymphocyte subsets that express HLA class I-specific inhibitory receptors represent oligoclonally or monoclonally expanded cell populations. Proc Natl Acad Sci U S A 93 12433 12438

36. AnfossiN

PasccalV

VivierE

UgoliniS

2001 Biology of T memory type 1 cells. Immunol Rev 181 269 278

37. SharmaD

BastardK

GuethleinLA

NormanPJ

YawataN

2009 Dimorphic motifs in D0 and D1 + D2 domains of killer cell Ig-like receptor 3DL1 combine to form receptors with high, moderate, and no avidity for the complex of a peptide derived from HIV and HLA-A*2402. J Immunol 183 4569 4582

38. CarrWH

RosenDB

AraseH

NixonDF

MichaelssonJ

2007 Cutting edge: KIR3DS1, a gene implicated in resistance to progression to AIDS, encodes a DAP12-associated receptor expressed on NK cells that triggers NK cell activation. J Immunol 178 647 651

39. KhakooSI

GellerR

ShinS

JenkinsJA

ParhamP

2002 The D0 domain of KIR3D acts as a major histocompatibility complex class I binding enhancer. J Exp Med 196 911 921

40. ParhamP

2006 Taking license with natural killer cell maturation and repertoire development. Immunol Rev 214 155 160

41. GardinerCM

GuethleinLA

ShillingHG

PandoM

CarrWH

2001 Different NK cell surface phenotypes defined by the DX9 antibody are due to KIR3DL1 gene polymorphism. J Immunol 166 2992 3001

42. ShillingHG

YoungN

GuethleinLA

ChengNW

GardinerCM

2002 Genetic control of human NK cell repertoire. J Immunol 169 239 247

43. YawataM

YawataN

DraghiM

LittleA-M

ParheniouF

2006 Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J Exp Med 203 633 645

44. AlterG

RihnS

StreeckH

TeigenN

Piechocka-TrochaA

2008 Ligand-independent exhaustion of killer immunoglobulin-like receptor-positive CD8+ T cells in human immunodefieciency virus type 1 infection. J Virol 82 9668 9677

45. BonorinoP

LeroyV

Dufeu-DuchesneT

Tongiani-DashanS

SturmN

2007 Features and distribution of CD8 T cells with human leukocyte antigen class I-specific receptor expression in chronic hepatitis C. Hepatology 46 1375 1386

46. GumperzJE

ValianteNM

ParhamP

LanierLL

TyanD

1996 Heterogeneous phenotypes of expression of the NKB1 natural killer cell class I receptor among individuals of different human histocompatibility leukocyte antigens types appear genetically regulated, but not linked to major histocompatibility complex haplotype. J Exp Med 183 1817 1827

47. ShimizuY

KollerB

GeraghtyD

OrrH

ShawS

1986 Transfer of cloned human class I major histocompatibility complex genes into HLA mutant human lymphoblastoid cells. Mol Cell Biol 6 1074 1087

48. KaizuM

BorchardtGJ

GliddenCE

FiskDL

LoffredoJT

2007 Molecular typing of major histocompatibility complex class I alleles in the Indian rhesus macaque which restrict SIV CD8+ T cell epitopes. Immunogenetics 59 693 703

49. RauletDH

VanceRE

McMahonCW

2001 Regulation of the natural killer cell receptor repertoire. Annu Rev Immunol 19 291 330

50. PascalV

StulbergMJ

AndersonSK

2006 Regulation of class I major histocompatibility complex receptor expression in natural killer cells: one promoter is not enough! Immunol Rev 214 9 21

51. DaviesGE

LockeSM

WrightPW

LiH

HansonRJ

2007 Identification of bidirectional promoters in the human KIR genes. Genes Immun 8 245 253

52. HoglundP

BrodinP

2010 Current perspectives of natural killer cell education by MHC class I molecules. Nat Rev Immunol 10 724 734

53. KimS

Poursine-LaurentJ

TruscottSM

LybargerL

SongY-J

2005 Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436 709 713

54. AnfossiN

AndreP

GuiaS

FalkCS

RoetynckS

2006 Human NK cell education by inhibitory receptors for MHC class I. Immunity 25 331 342

55. WisemanRW

KarlJA

BimberBN

O'LearyCE

LankSM

2009 Major histocompatibility complex genotyping with massively parallel pyrosequencing. Nat Med 15 1322 1327

56. OttingN

HeijmansCMC

NoortRC

de GrootNG

DoxiadisGG

2005 Unparalleled complexity of the MHC class I region in rhesus macaques. Proc Natl Acad Sci U S A 102 1626 1631

57. MandelboimO

ReyburnHT

Valez-GomezM

PazmanyL

ColonnaM

1996 Protection from lysis by natural killer cells of group 1 and 2 specificity is mediated by residue 80 in human histocompatibility leukocyte antigen C alleles and also occurs with empty major histocompatibility complex molecules. J Exp Med 184 913 922

58. RajalingamR

ParhamP

Abi-RachedL

2004 Domain shuffling has been the main mechanism forming new hominoid killer cell Ig-like receptors. J Immunol 172 356 369

59. DeGottardiMQ

SpechtA

MetcalfB

KaurA

KirchhoffF

2008 Selective downregulation of rhesus macaque and sooty mangabey major histocompatibility complex class I molecules by nef alleles of simian immunodeficiency virus and human immunodeficiency virus type 2. J Virol 82 3139 3146

60. MariaAD

FerrarisA

GuastellaM

PiliaS

CantoniC

1997 Expression of HLA class I-specific inhibitory natural killer cell receptors in HIV-specific cytolytic T lymphocytes: Impairment of specific cytolytic functions. Proc Natl Acad Sci U S A 94 10285 10288

61. BostikP

KobkitjaroenJ

TangW

VillingerF

PereiraLE

2009 Decreased NK cell frequency and function is associated with increased risk of KIR3DL allele polymorphism in simian immunodeficiency virus-infected rhesus macaques with high viral loads. J Immunol 182 3638 3649

62. Anonymous

1996 The Institute of Laboratory Animal Resources, National Research Council: Guide for the Care and Use of Laboratory Animals. Washington, D.C. National Academy Press 86 123

63. RobinsonJ

MistryK

McWilliamH

LopezR

MarshSGE

2010 IPD-the immuo polymorphism database. Nucleic Acids Res 38 D863 D869

64. PendeD

BiassoniR

CantoniC

VerdianiS

FalcoM

1996 The natural killer cell receptor specific for HLA-A allotypes: 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 184 505 518