Human-Specific Evolution and Adaptation Led to Major Qualitative Differences in the Variable Receptors of Human and Chimpanzee Natural Killer Cells
Natural killer (NK) cells serve essential functions in immunity and reproduction. Diversifying these functions within individuals and populations are rapidly-evolving interactions between highly polymorphic major histocompatibility complex (MHC) class I ligands and variable NK cell receptors. Specific to simian primates is the family of Killer cell Immunoglobulin-like Receptors (KIR), which recognize MHC class I and associate with a range of human diseases. Because KIR have considerable species-specificity and are lacking from common animal models, we performed extensive comparison of the systems of KIR and MHC class I interaction in humans and chimpanzees. Although of similar complexity, they differ in genomic organization, gene content, and diversification mechanisms, mainly because of human-specific specialization in the KIR that recognizes the C1 and C2 epitopes of MHC-B and -C. Humans uniquely focused KIR recognition on MHC-C, while losing C1-bearing MHC-B. Reversing this trend, C1-bearing HLA-B46 was recently driven to unprecedented high frequency in Southeast Asia. Chimpanzees have a variety of ancient, avid, and predominantly inhibitory receptors, whereas human receptors are fewer, recently evolved, and combine avid inhibitory receptors with attenuated activating receptors. These differences accompany human-specific evolution of the A and B haplotypes that are under balancing selection and differentially function in defense and reproduction. Our study shows how the qualitative differences that distinguish the human and chimpanzee systems of KIR and MHC class I predominantly derive from adaptations on the human line in response to selective pressures placed on human NK cells by the competing needs of defense and reproduction.
Vyšlo v časopise:
Human-Specific Evolution and Adaptation Led to Major Qualitative Differences in the Variable Receptors of Human and Chimpanzee Natural Killer Cells. PLoS Genet 6(11): e32767. doi:10.1371/journal.pgen.1001192
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1001192
Souhrn
Natural killer (NK) cells serve essential functions in immunity and reproduction. Diversifying these functions within individuals and populations are rapidly-evolving interactions between highly polymorphic major histocompatibility complex (MHC) class I ligands and variable NK cell receptors. Specific to simian primates is the family of Killer cell Immunoglobulin-like Receptors (KIR), which recognize MHC class I and associate with a range of human diseases. Because KIR have considerable species-specificity and are lacking from common animal models, we performed extensive comparison of the systems of KIR and MHC class I interaction in humans and chimpanzees. Although of similar complexity, they differ in genomic organization, gene content, and diversification mechanisms, mainly because of human-specific specialization in the KIR that recognizes the C1 and C2 epitopes of MHC-B and -C. Humans uniquely focused KIR recognition on MHC-C, while losing C1-bearing MHC-B. Reversing this trend, C1-bearing HLA-B46 was recently driven to unprecedented high frequency in Southeast Asia. Chimpanzees have a variety of ancient, avid, and predominantly inhibitory receptors, whereas human receptors are fewer, recently evolved, and combine avid inhibitory receptors with attenuated activating receptors. These differences accompany human-specific evolution of the A and B haplotypes that are under balancing selection and differentially function in defense and reproduction. Our study shows how the qualitative differences that distinguish the human and chimpanzee systems of KIR and MHC class I predominantly derive from adaptations on the human line in response to selective pressures placed on human NK cells by the competing needs of defense and reproduction.
Zdroje
1. LanierLL
2008 Evolutionary struggles between NK cells and viruses. Nat Rev Immunol 8 259 268
2. DiefenbachA
RauletDH
2002 The innate immune response to tumors and its role in the induction of T-cell immunity. Immunol Rev 188 9 21
3. MorettaL
FerlazzoG
BottinoC
VitaleM
PendeD
2006 Effector and regulatory events during natural killer-dendritic cell interactions. Immunol Rev 214 219 228
4. VivierE
TomaselloE
BaratinM
WalzerT
UgoliniS
2008 Functions of natural killer cells. Nat Immunol 9 503 510
5. Moffett-KingA
2002 Natural killer cells and pregnancy. Nat Rev Immunol 2 656 663
6. LanierLL
2008 Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9 495 502
7. ShumBP
FlodinLR
MuirDG
RajalingamR
KhakooSI
2002 Conservation and variation in human and common chimpanzee CD94 and NKG2 genes. J Immunol 168 240 252
8. VilchesC
ParhamP
2002 KIR: Diverse, Rapidly Evolving Receptors of Innate and Adaptive Immunity. Annu Rev Immunol 20 217 251
9. KulkarniS
MartinMP
CarringtonM
2008 The Yin and Yang of HLA and KIR in human disease. Semin Immunol 20 343 352
10. ParhamP
2005 MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5 201 214
11. RajagopalanS
LongEO
2005 Understanding how combinations of HLA and KIR genes influence disease. J Exp Med 201 1025 1029
12. BashirovaAA
MartinMP
McVicarDW
CarringtonM
2006 The killer immunoglobulin-like receptor gene cluster: tuning the genome for defense. Annu Rev Genomics Hum Genet 7 277 300
13. AverdamA
PetersenB
RosnerC
NeffJ
RoosC
2009 A novel system of polymorphic and diverse NK cell receptors in primates. PLoS Genet 5 e1000688 doi:10.1371/journal.pgen.1000688
14. WelchAY
KasaharaM
SpainLM
2003 Identification of the mouse killer immunoglobulin-like receptor-like (Kirl) gene family mapping to chromosome X. Immunogenetics 54 782 790
15. BartenR
TorkarM
HaudeA
TrowsdaleJ
WilsonMJ
2001 Divergent and convergent evolution of NK-cell receptors. Trends Immunol 22 52 57
16. GuethleinLA
Abi-RachedL
HammondJA
ParhamP
2007 The expanded cattle KIR genes are orthologous to the conserved single-copy KIR3DX1 gene of primates. Immunogenetics 59 517 522
17. GendzekhadzeK
NormanPJ
Abi-RachedL
GraefT
MoestaAK
2009 Co-evolution of KIR2DL3 with HLA-C in a human population retaining minimal essential diversity of KIR and HLA class I ligands. Proc Natl Acad Sci U S A 106 18692 18697
18. BettauerRH
2010 Chimpanzees in hepatitis C virus research: 1998-2007. J Med Primatol 39 9 23
19. OlsonMV
VarkiA
2003 Sequencing the chimpanzee genome: insights into human evolution and disease. Nat Rev Genet 4 20 28
20. AppsR
MurphySP
FernandoR
GardnerL
AhadT
2009 Human leucocyte antigen (HLA) expression of primary trophoblast cells and placental cell lines, determined using single antigen beads to characterize allotype specificities of anti-HLA antibodies. Immunology 127 26 39
21. TrowsdaleJ
MoffettA
2008 NK receptor interactions with MHC class I molecules in pregnancy. Semin Immunol 20 317 320
22. AdamsEJ
CooperS
ThomsonG
ParhamP
2000 Common chimpanzees have greater diversity than humans at two of the three highly polymorphic MHC class I genes. Immunogenetics 51 410 424
23. KhakooSI
RajalingamR
ShumBP
WeidenbachK
FlodinL
2000 Rapid evolution of NK cell receptor systems demonstrated by comparison of chimpanzees and humans. Immunity 12 687 698
24. 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
25. WilsonMJ
TorkarM
HaudeA
MilneS
JonesT
2000 Plasticity in the organization and sequences of human KIR/ILT gene families. Proc Natl Acad Sci U S A 97 4778 4783
26. YawataM
YawataN
Abi-RachedL
ParhamP
2002 Variation within the human killer cell immunoglobulin-like receptor (KIR) gene family. Crit Rev Immunol 22 463 482
27. MoestaAK
Abi-RachedL
NormanPJ
ParhamP
2009 Chimpanzees use more varied receptors and ligands than humans for inhibitory killer cell Ig-like receptor recognition of the MHC-C1 and MHC-C2 epitopes. J Immunol 182 3628 3637
28. MoestaAK
GraefT
Abi-RachedL
Older AguilarAM
GuetheinLA
2010 Humans differ from other hominids in lacking an activating NK cell receptor that recognizes the C1 epitope of MHC class I. J Immunol 185 4233 4237
29. BiassoniR
2009 Human natural killer receptors, co-receptors, and their ligands. Curr Protoc Immunol Chapter 14 Unit 14 10
30. GuethleinLA
Older AguilarAM
Abi-RachedL
ParhamP
2007 Evolution of killer cell Ig-like receptor (KIR) genes: definition of an orangutan KIR haplotype reveals expansion of lineage III KIR associated with the emergence of MHC-C. J Immunol 179 491 504
31. Abi-RachedL
ParhamP
2005 Natural selection drives recurrent formation of activating killer cell immunoglobulin-like receptor and Ly49 from inhibitory homologues. J Exp Med 201 1319 1332
32. RobinsonJ
WallerMJ
StoehrP
MarshSG
2005 IPD—the Immuno Polymorphism Database. Nucleic Acids Res 33 D523 526
33. FanQR
LongEO
WileyDC
2001 Crystal structure of the human natural killer cell inhibitory receptor KIR2DL1-HLA-Cw4 complex. Nat Immunol 2 452 460
34. BoyingtonJC
MotykaSA
SchuckP
BrooksAG
SunPD
2000 Crystal structure of an NK cell immunoglobulin-like receptor in complex with its class I MHC ligand. Nature 405 537 543
35. DavisDM
ChiuI
FassettM
CohenGB
MandelboimO
1999 The human natural killer cell immune synapse. Proc Natl Acad Sci U S A 96 15062 15067
36. YusaS
CampbellKS
2003 Src homology region 2-containing protein tyrosine phosphatase-2 (SHP-2) can play a direct role in the inhibitory function of killer cell Ig-like receptors in human NK cells. J Immunol 170 4539 4547
37. SweeneyMC
WavreilleAS
ParkJ
ButcharJP
TridandapaniS
2005 Decoding protein-protein interactions through combinatorial chemistry: sequence specificity of SHP-1, SHP-2, and SHIP SH2 domains. Biochemistry 44 14932 14947
38. Alvarez-AriasDA
CampbellKS
2007 Protein kinase C regulates expression and function of inhibitory killer cell Ig-like receptors in NK cells. J Immunol 179 5281 5290
39. FujiiK
ZhuG
LiuY
HallamJ
ChenL
2004 Kinase peptide specificity: improved determination and relevance to protein phosphorylation. Proc Natl Acad Sci U S A 101 13744 13749
40. NishikawaK
TokerA
JohannesFJ
SongyangZ
CantleyLC
1997 Determination of the specific substrate sequence motifs of protein kinase C isozymes. J Biol Chem 272 952 960
41. ParhamP
ArnettKL
AdamsEJ
BarberLD
DomenaJD
1994 The HLA-B73 antigen has a most unusual structure that defines a second lineage of HLA-B alleles. Tissue Antigens 43 302 313
42. CellaM
LongoA
FerraraGB
StromingerJL
ColonnaM
1994 NK3-specific natural killer cells are selectively inhibited by Bw4-positive HLA alleles with isoleucine 80. J Exp Med 180 1235 1242
43. 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
44. BarberLD
PercivalL
ValianteNM
ChenL
LeeC
1996 The inter-locus recombinant HLA-B*4601 has high selectivity in peptide binding and functions characteristic of HLA-C. J Exp Med 184 735 740
45. MellarsP
2006 Going east: new genetic and archaeological perspectives on the modern human colonization of Eurasia. Science 313 796 800
46. MoestaAK
NormanPJ
YawataM
YawataN
GleimerM
2008 Synergistic polymorphism at two positions distal to the ligand-binding site makes KIR2DL2 a stronger receptor for HLA-C than KIR2DL3. J Immunol 180 3969 3979
47. BiassoniR
FalcoM
CambiaggiA
CostaP
VerdianiS
1995 Amino acid substitutions can influence the natural killer (NK)-mediated recognition of HLA-C molecules. Role of serine-77 and lysine-80 in the target cell protection from lysis mediated by “group 2” or “group 1” NK clones. J Exp Med 182 605 609
48. YawataM
YawataN
DraghiM
PartheniouF
LittleAM
2008 MHC class I-specific inhibitory receptors and their ligands structure diverse human NK-cell repertoires toward a balance of missing self-response. Blood 112 2369 2380
49. ZemmourJ
ParhamP
1992 Distinctive polymorphism at the HLA-C locus: implications for the expression of HLA-C. J Exp Med 176 937 950
50. ParhamP
LawlorDA
LomenCE
EnnisPD
1989 Diversity and diversification of HLA-A,B,C alleles. J Immunol 142 3937 3950
51. SibilioL
MartayanA
SetiniA
Lo MonacoE
TremanteE
2008 A single bottleneck in HLA-C assembly. J Biol Chem 283 1267 1274
52. ShillingHG
GuethleinLA
ChengNW
GardinerCM
RodriguezR
2002 Allelic polymorphism synergizes with variable gene content to individualize human KIR genotype. J Immunol 168 2307 2315
53. DeSilvaJM
LesnikJJ
2008 Brain size at birth throughout human evolution: a new method for estimating neonatal brain size in hominins. J Hum Evol 55 1064 1074
54. Fukami-KobayashiK
ShiinaT
AnzaiT
SanoK
YamazakiM
2005 Genomic evolution of MHC class I region in primates. Proc Natl Acad Sci U S A 102 9230 9234
55. KhakooSI
ThioCL
MartinMP
BrooksCR
GaoX
2004 HLA and NK cell inhibitory receptor genes in resolving hepatitis C virus infection. Science 305 872 874
56. MarshSG
ParhamP
DupontB
GeraghtyDE
TrowsdaleJ
2003 Killer-cell immunoglobulin-like receptor (KIR) nomenclature report, 2002. Immunogenetics 55 220 226
57. YooYJ
TangJ
KaslowRA
ZhangK
2007 Haplotype inference for present-absent genotype data using previously identified haplotypes and haplotype patterns. Bioinformatics 23 2399 2406
58. NormanPJ
CarringtonCV
ByngM
MaxwellLD
CurranMD
2002 Natural killer cell immunoglobulin-like receptor (KIR) locus profiles in African and South Asian populations. Genes Immun 3 86 95
59. UhrbergM
ParhamP
WernetP
2002 Definition of gene content for nine common group B haplotypes of the Caucasoid population: KIR haplotypes contain between seven and eleven KIR genes. Immunogenetics 54 221 229
60. YawataM
YawataN
McQueenKL
ChengNW
GuethleinLA
2002 Predominance of group A KIR haplotypes in Japanese associated with diverse NK cell repertoires of KIR expression. Immunogenetics 54 543 550
61. KumarS
TamuraK
NeiM
2004 MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 5 150 163
62. GendzekhadzeK
NormanPJ
Abi-RachedL
LayrisseZ
ParhamP
2006 High KIR diversity in Amerindians is maintained using few gene-content haplotypes. Immunogenetics 58 474 480
63. LibradoP
RozasJ
2009 DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25 1451 1452
64. DuZ
SharmaSK
SpellmanS
ReedEF
RajalingamR
2008 KIR2DL5 alleles mark certain combination of activating KIR genes. Genes Immun 9 470 480
65. OrdonezD
MeenaghA
Gomez-LozanoN
CastanoJ
MiddletonD
2008 Duplication, mutation and recombination of the human orphan gene KIR2DS3 contribute to the diversity of KIR haplotypes. Genes Immun 9 431 437
66. NormanPJ
CookMA
CareyBS
CarringtonCV
VerityDH
2004 SNP haplotypes and allele frequencies show evidence for disruptive and balancing selection in the human leukocyte receptor complex. Immunogenetics 56 225 237
67. YangZ
1997 PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13 555 556
68. RobinsonJ
WallerMJ
ParhamP
de GrootN
BontropR
2003 IMGT/HLA and IMGT/MHC: sequence databases for the study of the major histocompatibility complex. Nucleic Acids Res 31 311 314
69. MiddletonD
MenchacaL
RoodH
KomerofskyR
2003 61 403 407 New allele frequency database: http://www.allelefrequencies.net. Tissue Antigens
70. WesselP
SmithWHF
1998 New, improved version of generic mapping tools released. Eos, Transactions, American Geophysical Union 79 579
71. SolbergOD
MackSJ
LancasterAK
SingleRM
TsaiY
2008 Balancing selection and heterogeneity across the classical human leukocyte antigen loci: a meta-analytic review of 497 population studies. Hum Immunol 69 443 464
72. GuX
Vander VeldenK
2002 DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. Bioinformatics 18 500 501
73. ChelvanayagamG
1996 A roadmap for HLA-A, HLA-B, and HLA-C peptide binding specificities. Immunogenetics 45 15 26
74. MarrackP
Scott-BrowneJP
DaiS
GapinL
KapplerJW
2008 Evolutionarily conserved amino acids that control TCR-MHC interaction. Annu Rev Immunol 26 171 203
Štítky
Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
2010 Číslo 11
- Je „freeze-all“ pro všechny? Odborníci na fertilitu diskutovali na virtuálním summitu
- Gynekologové a odborníci na reprodukční medicínu se sejdou na prvním virtuálním summitu
Najčítanejšie v tomto čísle
- Genome-Wide Association Study Identifies Two Novel Regions at 11p15.5-p13 and 1p31 with Major Impact on Acute-Phase Serum Amyloid A
- Analysis of the 10q11 Cancer Risk Locus Implicates and in Human Prostate Tumorigenesis
- The Parental Non-Equivalence of Imprinting Control Regions during Mammalian Development and Evolution
- A Functional Genomics Approach Identifies Candidate Effectors from the Aphid Species (Green Peach Aphid)