KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C

Graef, Thorsten; Moesta, Achim K.; Norman, Paul J.; Abi-Rached, Laurent; Vago, Luca; Older Aguilar, Anastazia M.; Gleimer, Michael; Hammond, John A.; Guethlein, Lisbeth A.; Bushnell, David A.; Robinson, Philip J.; Parham, Peter

doi:10.1084/jem.20091010

Title: KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C

Journal Article · 25 October 2009 · Journal of Experimental Medicine

DOI: https://doi.org/10.1084/jem.20091010 · OSTI ID:1625195

Graef, Thorsten ^[1]; Moesta, Achim K. ^[2]; Norman, Paul J. ^[2]; Abi-Rached, Laurent ^[2]; Vago, Luca ^[2]; Older Aguilar, Anastazia M. ^[2]; Gleimer, Michael ^[2]; Hammond, John A. ^[2]; Guethlein, Lisbeth A. ^[2]; Bushnell, David A. ^[2]; Robinson, Philip J. ^[2]; Parham, Peter ^[2]

Stanford Univ., CA (United States). School of Medicine, Dept. of Structural Biology; DOE/OSTI
Stanford Univ., CA (United States). School of Medicine, Dept. of Structural Biology

Human killer cell immunoglobulin-like receptors (KIRs) are distinguished by expansion of activating KIR2DS, whose ligands and functions remain poorly understood. The oldest, most prevalent KIR2DS is KIR2DS4, which is represented by a variable balance between “full-length” and “deleted” forms. We find that full-length 2DS4 is a human histocompatibility leukocyte antigen (HLA) class I receptor that binds specifically to subsets of C1+ and C2+ HLA-C and to HLA-A*11, whereas deleted 2DS4 is nonfunctional. Activation of 2DS4+ NKL cells was achieved with A*1102 as ligand, which differs from A*1101 by unique substitution of lysine 19 for glutamate, but not with A*1101 or HLA-C. Distinguishing KIR2DS4 from other KIR2DS is the proline–valine motif at positions 71–72, which is shared with KIR3DL2 and was introduced by gene conversion before separation of the human and chimpanzee lineages. Site-directed swap mutagenesis shows that these two residues are largely responsible for the unique HLA class I specificity of KIR2DS4. Determination of the crystallographic structure of KIR2DS4 shows two major differences from KIR2DL: displacement of contact loop L2 and altered bonding potential because of the substitutions at positions 71 and 72. Correlation between the worldwide distributions of functional KIR2DS4 and HLA-A*11 points to the physiological importance of their mutual interaction.

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Research Organization:: SLAC National Accelerator Laboratory, Menlo Park, CA (United States). Stanford Synchrotron Radiation Lightsource (SSRL)

Sponsoring Organization:: Dr. Mildred Scheel Foundation for Cancer Research; National Center for Research Resources (NCRR); National Institute of General Medical Sciences (NIGMS); National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER); USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-76SF00515

OSTI ID:: 1625195

Journal Information:: Journal of Experimental Medicine, Journal Name: Journal of Experimental Medicine Journal Issue: 11 Vol. 206; ISSN 0022-1007

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Revealing complete complex KIR haplotypes phased by long-read sequencing technology Roe, D.; Vierra-Green, C.; Pyo, C-W Genes & Immunity, Vol. 18, Issue 3 https://doi.org/10.1038/gene.2017.10	journal	June 2017
Correction: High resolution HLA analysis reveals independent class I haplotypes and amino-acid motifs protective for multiple sclerosis Mack, Steven J.; Udell, Julia; Cohen, Franziska Genes & Immunity, Vol. 20, Issue 4 https://doi.org/10.1038/s41435-018-0037-9	journal	June 2018
Distribution of killer cell immunoglobulin-like receptor genes in the mestizo population from Venezuela Conesa, A.; Fernández-Mestre, M.; Padrón, D. Tissue Antigens, Vol. 75, Issue 6 https://doi.org/10.1111/j.1399-0039.2010.01446.x	journal	February 2010
Genome hyperevolution and the success of a parasite Barry, J. David; Hall, James P. J.; Plenderleith, Lindsey Annals of the New York Academy of Sciences, Vol. 1267, Issue 1 https://doi.org/10.1111/j.1749-6632.2012.06654.x	journal	September 2012
Natural killer cells: From surface receptors to the cure of high‐risk leukemia (Ceppellini Lecture) Falco, Michela; Pende, Daniela; Munari, Enrico HLA, Vol. 93, Issue 4 https://doi.org/10.1111/tan.13509	journal	March 2019
The Structural Basis of Ligand Recognition by Natural Killer Cell Receptors Joyce, M. Gordon; Sun, Peter D. Journal of Biomedicine and Biotechnology, Vol. 2011 https://doi.org/10.1155/2011/203628	journal	January 2011
Expression of ligands for activating natural killer cell receptors on cell lines commonly used to assess natural killer cell function Tremblay-McLean, Alexandra; Coenraads, Sita; Kiani, Zahra BMC Immunology, Vol. 20, Issue 1 https://doi.org/10.1186/s12865-018-0272-x	journal	January 2019
Self-Association of an Activating Natural Killer Cell Receptor, KIR2DS1 Hayley, Michael; Bourbigot, Sarah; Booth, Valerie PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0023052	journal	August 2011
Killer Immunoglobulin-like Receptor (KIR) and HLA Genotypes Affect the Outcome of Allogeneic Kidney Transplantation Nowak, Izabela; Magott-Procelewska, Maria; Kowal, Agnieszka PLoS ONE, Vol. 7, Issue 9 https://doi.org/10.1371/journal.pone.0044718	journal	September 2012
KIR2DS4 Promotes HIV-1 Pathogenesis: New Evidence from Analyses of Immunogenetic Data and Natural Killer Cell Function Merino, Aimee M.; Dugast, Anne-Sophie; Wilson, Craig M. PLoS ONE, Vol. 9, Issue 6 https://doi.org/10.1371/journal.pone.0099353	journal	June 2014
Significant Association of KIR2DL3-HLA-C1 Combination with Cerebral Malaria and Implications for Co-evolution of KIR and HLA Hirayasu, Kouyuki; Ohashi, Jun; Kashiwase, Koichi PLoS Pathogens, Vol. 8, Issue 3 https://doi.org/10.1371/journal.ppat.1002565	journal	March 2012
Diverse functionality among human NK cell receptors for the C1 epitope of HLA-C: KIR2DS2, KIR2DL2, and KIR2DL3 Moesta, Achim K.; Parham, Peter Frontiers in Immunology, Vol. 3 https://doi.org/10.3389/fimmu.2012.00336	journal	January 2012
Killer Cell Immunoglobulin-Like Receptor Gene Associations with Autoimmune and Allergic Diseases, Recurrent Spontaneous Abortion, and Neoplasms Kuśnierczyk, Piotr Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00008	journal	January 2013
The role of KIR genes and ligands in leukemia surveillance Babor, Florian; Fischer, Johannes C.; Uhrberg, Markus Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00027	journal	January 2013
Donor killer immunoglobulin-like receptor genes and reactivation of cytomegalovirus after HLA-matched hematopoietic stem-cell transplantation: HLA-C allotype is an essential cofactor Behrendt, Carolyn E.; Nakamura, Ryotaro; Forman, Stephen J. Frontiers in Immunology, Vol. 4 https://doi.org/10.3389/fimmu.2013.00036	journal	January 2013
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qKAT: Quantitative Semi-automated Typing of Killer-cell Immunoglobulin-like Receptor Genes Jayaraman, Jyothi; Kirgizova, Vitalina; Di, Da Journal of Visualized Experiments, Issue 145 https://doi.org/10.3791/58646	journal	March 2019
Bonobos Maintain Immune System Diversity with Three Functional Types of MHC-B Wroblewski, Emily E.; Guethlein, Lisbeth A.; Norman, Paul J. The Journal of Immunology, Vol. 198, Issue 9 https://doi.org/10.4049/jimmunol.1601955	journal	May 2017
Killer Immunoglobulin-Like Receptors and Their Ligands Biassoni, Roberto; Vanni, Irene; Ugolotti, Elisabetta Histocompatibility https://doi.org/10.5772/35396	book	May 2012
Human Natural Killer Receptors, Co‐Receptors, and Their Ligands Biassoni, Roberto; Malnati, Mauro S. Current Protocols in Immunology, Vol. 121, Issue 1 https://doi.org/10.1002/cpim.47	journal	April 2018
Overview of the Killer Cell Immunoglobulin-Like Receptor System Rajalingam, Raja Methods in Molecular Biology https://doi.org/10.1007/978-1-61779-842-9_23	book	January 2012
Signatures of historical demography and pathogen richness on MHC class I genes Qutob, Nouar; Balloux, Francois; Raj, Towfique Immunogenetics, Vol. 64, Issue 3 https://doi.org/10.1007/s00251-011-0576-y	journal	September 2011
KIR diversity in Māori and Polynesians: populations in which HLA-B is not a significant KIR ligand Nemat-Gorgani, Neda; Edinur, Hisham A.; Hollenbach, Jill A. Immunogenetics, Vol. 66, Issue 11 https://doi.org/10.1007/s00251-014-0794-1	journal	August 2014
KIR2DS5 in the presence of HLA-C C2 protects against endometriosis Nowak, Izabela; Płoski, Rafał; Barcz, Ewa Immunogenetics, Vol. 67, Issue 4 https://doi.org/10.1007/s00251-015-0828-3	journal	March 2015
Missing or altered self: human NK cell receptors that recognize HLA-C Hilton, Hugo G.; Parham, Peter Immunogenetics, Vol. 69, Issue 8-9 https://doi.org/10.1007/s00251-017-1001-y	journal	July 2017
Conserved KIR allele-level haplotypes are altered by microvariation in individuals with European ancestry Hou, L.; Chen, M.; Ng, J. Genes & Immunity, Vol. 13, Issue 1 https://doi.org/10.1038/gene.2011.52	journal	July 2011
Genetic epistasis between killer immunoglobulin-like receptors and human leukocyte antigens in Kawasaki disease susceptibility Bossi, G.; Mannarino, S.; Pietrogrande, M. C. Genes & Immunity, Vol. 16, Issue 7 https://doi.org/10.1038/gene.2015.34	journal	September 2015
The early onset of type 1 autoimmune hepatitis has a strong genetic influence: role of HLA and KIR genes Podhorzer, A.; Paladino, N.; Cuarterolo, M. L. Genes & Immunity, Vol. 17, Issue 3 https://doi.org/10.1038/gene.2016.7	journal	February 2016
Revealing complete complex KIR haplotypes phased by long-read sequencing technology Roe, D.; Vierra-Green, C.; Pyo, C-W Genes & Immunity, Vol. 18, Issue 3 https://doi.org/10.1038/gene.2017.10	journal	June 2017
Variable NK cell receptors and their MHC class I ligands in immunity, reproduction and human evolution Parham, Peter; Moffett, Ashley Nature Reviews Immunology, Vol. 13, Issue 2 https://doi.org/10.1038/nri3370	journal	January 2013
Balancing natural killer cell activation through paired receptors Martinet, Ludovic; Smyth, Mark J. Nature Reviews Immunology, Vol. 15, Issue 4 https://doi.org/10.1038/nri3799	journal	March 2015
Human NK cells: surface receptors, inhibitory checkpoints, and translational applications Sivori, Simona; Vacca, Paola; Del Zotto, Genny Cellular & Molecular Immunology, Vol. 16, Issue 5 https://doi.org/10.1038/s41423-019-0206-4	journal	February 2019
High resolution HLA analysis reveals independent class I haplotypes and amino-acid motifs protective for multiple sclerosis Mack, Steven J.; Udell, Julia; Cohen, Franziska Genes & Immunity, Vol. 20, Issue 4 https://doi.org/10.1038/s41435-017-0006-8	journal	January 2018
Activating killer cell immunoglobulin-like receptor 2DS2 binds to HLA-A*11 Liu, J.; Xiao, Z.; Ko, H. L. Proceedings of the National Academy of Sciences, Vol. 111, Issue 7 https://doi.org/10.1073/pnas.1322052111	journal	February 2014
Human NK cell receptor KIR2DS4 detects a conserved bacterial epitope presented by HLA-C Sim, Malcolm J. W.; Rajagopalan, Sumati; Altmann, Daniel M. Proceedings of the National Academy of Sciences, Vol. 116, Issue 26 https://doi.org/10.1073/pnas.1903781116	journal	May 2019
Structure and flexibility of the extracellular region of the PirB receptor Vlieg, Hedwich C.; Huizinga, Eric G.; Janssen, Bert J. C. Journal of Biological Chemistry, Vol. 294, Issue 12 https://doi.org/10.1074/jbc.RA118.004396	journal	March 2019
Natural killer cells and their receptors in multiple sclerosis Kaur, Gurman; Trowsdale, John; Fugger, Lars Brain, Vol. 136, Issue 9 https://doi.org/10.1093/brain/aws159	journal	June 2012
Revealing Mammalian Evolutionary Relationships by Comparative Analysis of Gene Clusters Song, Giltae; Riemer, Cathy; Dickins, Benjamin Genome Biology and Evolution, Vol. 4, Issue 4 https://doi.org/10.1093/gbe/evs032	journal	January 2012
Human-specific evolution of killer cell immunoglobulin-like receptor recognition of major histocompatibility complex class I molecules Parham, Peter; Norman, Paul J.; Abi-Rached, Laurent Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 367, Issue 1590 https://doi.org/10.1098/rstb.2011.0266	journal	March 2012
HLA-C-restricted presentation of a conserved bacterial epitope to an innate NK cell receptor Sim, Malcolm J. W.; Rajagopalan, Sumati; Altmann, Daniel M. Proceedings of the National Academy of Sciences https://doi.org/10.1101/550889	posted_content	February 2019
Activating killer cell immunoglobulin‐like receptors: Detection, function and therapeutic use Blunt, Matthew D.; Khakoo, Salim I. International Journal of Immunogenetics, Vol. 47, Issue 1 https://doi.org/10.1111/iji.12461	journal	November 2019
Deciphering the killer-cell immunoglobulin-like receptor system at super-resolution for natural killer and T-cell biology Béziat, Vivien; Hilton, Hugo G.; Norman, Paul J. Immunology, Vol. 150, Issue 3 https://doi.org/10.1111/imm.12684	journal	December 2016
Immunogenetics of HIV disease Martin, Maureen P.; Carrington, Mary Immunological Reviews, Vol. 254, Issue 1 https://doi.org/10.1111/imr.12071	journal	June 2013
Human KIR repertoires: shaped by genetic diversity and evolution Manser, Angela R.; Weinhold, Sandra; Uhrberg, Markus Immunological Reviews, Vol. 267, Issue 1 https://doi.org/10.1111/imr.12316	journal	August 2015
A bird's eye view of NK cell receptor interactions with their MHC class I ligands Saunders, Philippa M.; Vivian, Julian P.; O'Connor, Geraldine M. Immunological Reviews, Vol. 267, Issue 1 https://doi.org/10.1111/imr.12319	journal	August 2015
Co-evolution of MHC class I and variable NK cell receptors in placental mammals Guethlein, Lisbeth A.; Norman, Paul J.; Hilton, Hugo G. Immunological Reviews, Vol. 267, Issue 1 https://doi.org/10.1111/imr.12326	journal	August 2015
The killer-cell immunoglobulin-like receptors of macaques Bimber, Benjamin N.; Evans, David T. Immunological Reviews, Vol. 267, Issue 1 https://doi.org/10.1111/imr.12329	journal	August 2015
Structure/function of human killer cell immunoglobulin-like receptors: lessons from polymorphisms, evolution, crystal structures and mutations: Structure/function of human KIR Campbell, Kerry S.; Purdy, Amanda K. Immunology, Vol. 132, Issue 3 https://doi.org/10.1111/j.1365-2567.2010.03398.x	journal	January 2011
Structural insights into activation of antiviral NK cell responses Finton, Kathryn A.; Strong, Roland K. Immunological Reviews, Vol. 250, Issue 1 https://doi.org/10.1111/j.1600-065x.2012.01168.x	journal	October 2012
Genome hyperevolution and the success of a parasite Barry, J. David; Hall, James P. J.; Plenderleith, Lindsey Annals of the New York Academy of Sciences, Vol. 1267, Issue 1 https://doi.org/10.1111/j.1749-6632.2012.06654.x	journal	September 2012
KIR and KIR ligand polymorphism: a new area for clinical applications?: Relevance of KIR and KIR-L polymorphism Falco, M.; Moretta, L.; Moretta, A. Tissue Antigens, Vol. 82, Issue 6 https://doi.org/10.1111/tan.12262	journal	November 2013
Natural killer cells: From surface receptors to the cure of high‐risk leukemia (Ceppellini Lecture) Falco, Michela; Pende, Daniela; Munari, Enrico HLA, Vol. 93, Issue 4 https://doi.org/10.1111/tan.13509	journal	March 2019
The Shaping of Modern Human Immune Systems by Multiregional Admixture with Archaic Humans Abi-Rached, L.; Jobin, M. J.; Kulkarni, S. Science, Vol. 334, Issue 6052 https://doi.org/10.1126/science.1209202	journal	August 2011
KIR2DS2 recognizes conserved peptides derived from viral helicases in the context of HLA-C Naiyer, Mohammed M.; Cassidy, Sorcha A.; Magri, Andrea Science Immunology, Vol. 2, Issue 15 https://doi.org/10.1126/sciimmunol.aal5296	journal	September 2017
Genetic and Environmental Determinants of Human NK Cell Diversity Revealed by Mass Cytometry Horowitz, A.; Strauss-Albee, D. M.; Leipold, M. Science Translational Medicine, Vol. 5, Issue 208 https://doi.org/10.1126/scitranslmed.3006702	journal	October 2013
The Structural Basis of Ligand Recognition by Natural Killer Cell Receptors Joyce, M. Gordon; Sun, Peter D. Journal of Biomedicine and Biotechnology, Vol. 2011 https://doi.org/10.1155/2011/203628	journal	January 2011
Uptake of CCR7 by KIR2DS4 ⁺ NK Cells Is Induced upon Recognition of Certain HLA-C Alleles Pesce, Silvia; Carlomagno, Simona; Moretta, Alessandro Journal of Immunology Research, Vol. 2015 https://doi.org/10.1155/2015/754373	journal	January 2015
Maternal activating KIRs protect against human reproductive failure mediated by fetal HLA-C2 Hiby, Susan E.; Apps, Richard; Sharkey, Andrew M. Journal of Clinical Investigation, Vol. 120, Issue 11 https://doi.org/10.1172/jci43998	journal	November 2010
NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs Béziat, Vivien; Liu, Lisa L.; Malmberg, Jenny-Ann Blood, Vol. 121, Issue 14 https://doi.org/10.1182/blood-2012-10-459545	journal	April 2013
Expression of ligands for activating natural killer cell receptors on cell lines commonly used to assess natural killer cell function Tremblay-McLean, Alexandra; Coenraads, Sita; Kiani, Zahra BMC Immunology, Vol. 20, Issue 1 https://doi.org/10.1186/s12865-018-0272-x	journal	January 2019
DAP12 impacts trafficking and surface stability of killer immunoglobulin-like receptors on natural killer cells Mulrooney, Tiernan J.; Posch, Phillip E.; Hurley, Carolyn Katovich Journal of Leukocyte Biology, Vol. 94, Issue 2 https://doi.org/10.1189/jlb.0213093	journal	May 2013
Role of alloreactive KIR2DS1 ⁺ NK cells in haploidentical hematopoietic stem cell transplantation Marcenaro, Emanuela; Carlomagno, Simona; Pesce, Silvia Journal of Leukocyte Biology, Vol. 90, Issue 4 https://doi.org/10.1189/jlb.0311137	journal	July 2011
Co-evolution of Human Leukocyte Antigen (HLA) Class I Ligands with Killer-Cell Immunoglobulin-Like Receptors (KIR) in a Genetically Diverse Population of Sub-Saharan Africans Norman, Paul J.; Hollenbach, Jill A.; Nemat-Gorgani, Neda PLoS Genetics, Vol. 9, Issue 10 https://doi.org/10.1371/journal.pgen.1003938	journal	October 2013
Self-Association of an Activating Natural Killer Cell Receptor, KIR2DS1 Hayley, Michael; Bourbigot, Sarah; Booth, Valerie PLoS ONE, Vol. 6, Issue 8 https://doi.org/10.1371/journal.pone.0023052	journal	August 2011
Uterine Natural Killer Cells: Functional Distinctions and Influence on Pregnancy in Humans and Mice Gaynor, Louise; Colucci, Francesco Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.11564	text	January 2017
TLR/NCR/KIR: Which One to Use and When? Sivori, Simona; Carlomagno, Simona; Pesce, Silvia Frontiers in Immunology, Vol. 5 https://doi.org/10.3389/fimmu.2014.00105	journal	March 2014
Activating Killer Cell Ig-Like Receptors in Health and Disease Ivarsson, Martin A.; MichaÃ«lsson, Jakob; Fauriat, Cyril Frontiers in Immunology, Vol. 5 https://doi.org/10.3389/fimmu.2014.00184	journal	April 2014
Uterine Natural Killer Cells: Functional Distinctions and Influence on Pregnancy in Humans and Mice Gaynor, Louise M.; Colucci, Francesco Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.00467	journal	April 2017
Conservation, Extensive Heterozygosity, and Convergence of Signaling Potential All Indicate a Critical Role for KIR3DL3 in Higher Primates Leaton, Laura A.; Shortt, Jonathan; Kichula, Katherine M. Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.00024	journal	January 2019
Two to Tango: Co-evolution of Hominid Natural Killer Cell Receptors and MHC Wroblewski, Emily E.; Parham, Peter; Guethlein, Lisbeth A. Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.00177	journal	February 2019
Killer Ig-Like Receptors (KIRs): Their Role in NK Cell Modulation and Developments Leading to Their Clinical Exploitation Pende, Daniela; Falco, Michela; Vitale, Massimo Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.01179	journal	May 2019
Distribution of Killer-Cell Immunoglobulin-Like Receptor Genes and Combinations of Their Human Leucocyte Antigen Ligands in 11 Ethnic Populations in China Yao, Yufeng; Shi, Lei; Yu, Jiankun Cells, Vol. 8, Issue 7 https://doi.org/10.3390/cells8070711	journal	July 2019
Mutation at Positively Selected Positions in the Binding Site for HLA-C Shows That KIR2DL1 Is a More Refined but Less Adaptable NK Cell Receptor Than KIR2DL3 Hilton, Hugo G.; Vago, Luca; Older Aguilar, Anastazia M. The Journal of Immunology, Vol. 189, Issue 3 https://doi.org/10.4049/jimmunol.1100431	journal	July 2012
Host Genetic Factors in Susceptibility to Herpes Simplex Type 1 Virus Infection: Contribution of Polymorphic Genes at the Interface of Innate and Adaptive Immunity Moraru, Manuela; Cisneros, Elisa; Gómez-Lozano, Natalia The Journal of Immunology, Vol. 188, Issue 9 https://doi.org/10.4049/jimmunol.1103434	journal	April 2012
HLA-F and MHC Class I Open Conformers Are Ligands for NK Cell Ig-like Receptors Goodridge, Jodie P.; Burian, Aura; Lee, Ni The Journal of Immunology, Vol. 191, Issue 7 https://doi.org/10.4049/jimmunol.1300081	journal	September 2013
Allelic Variation in KIR2DL3 Generates a KIR2DL2-like Receptor with Increased Binding to its HLA-C Ligand Frazier, William R.; Steiner, Noriko; Hou, Lihua The Journal of Immunology, Vol. 190, Issue 12 https://doi.org/10.4049/jimmunol.1300464	journal	May 2013
Human Cytomegalovirus Infection Promotes Rapid Maturation of NK Cells Expressing Activating Killer Ig–like Receptor in Patients Transplanted with NKG2C ^−/− Umbilical Cord Blood Della Chiesa, Mariella; Falco, Michela; Bertaina, Alice The Journal of Immunology, Vol. 192, Issue 4 https://doi.org/10.4049/jimmunol.1302053	journal	January 2014
Different Selected Mechanisms Attenuated the Inhibitory Interaction of KIR2DL1 with C2 ⁺ HLA-C in Two Indigenous Human Populations in Southern Africa Nemat-Gorgani, Neda; Hilton, Hugo G.; Henn, Brenna M. The Journal of Immunology, Vol. 200, Issue 8 https://doi.org/10.4049/jimmunol.1701780	journal	March 2018
Diversity of KIR, HLA Class I, and Their Interactions in Seven Populations of Sub-Saharan Africans Nemat-Gorgani, Neda; Guethlein, Lisbeth A.; Henn, Brenna M. The Journal of Immunology, Vol. 202, Issue 9 https://doi.org/10.4049/jimmunol.1801586	journal	March 2019

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