Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry

Science Translational Medicine

Volumn 5, Issue 208, 2013, Pages

  Horowitz, Amir ^a   Strauss Albee, Dara M ^a   Leipold, Michael ^a   Kubo, Jessica ^a   Nemat Gorgani, Neda ^a   Dogan, Ozge C ^a   Dekker, Cornelia L ^a   Mackey, Sally ^a   Maecker, Holden ^a   Swan, Gary E ^b   Davis, Mark M ^a   Norman, Paul J ^a   Guethlein, Lisbeth A ^a   Desai, Manisha ^a   Parham, Peter ^a   Blish, Catherine A ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SRI INTERNATIONAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD94 ANTIGEN; HLA ANTIGEN; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL1; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL5; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL KILLER CELL RECEPTOR NKG2D;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CYTOMETRY; ENVIRONMENTAL FACTOR; GENOTYPE; HEREDITY; HUMAN; HUMAN CELL; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MASS CYTOMETRY; MONOZYGOTIC TWINS; NATURAL KILLER CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADULT; CLUSTER ANALYSIS; ENVIRONMENT; FEMALE; GENE EXPRESSION REGULATION; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; MALE; MASS SPECTROMETRY; MIDDLE AGED; PHENOTYPE; RECEPTORS, NATURAL KILLER CELL; YOUNG ADULT;

EID: 84886419332     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3006702     Document Type: Article

References (56)

1. R. Kiessling, E. Klein, H. Wigzell, "Natural" killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur. J. Immunol. 5, 112-117 (1975).
2. R. R. Herberman, J. R. Ortaldo, G. D. Bonnard, Augmentation by interferon of human natural and antibody-dependent cell-mediated cytotoxicity. Nature 277, 221-223 (1979).
3. J. R. Ortaldo, G. D. Bonnard, P. D. Kind, R. B. Herberman, Cytotoxicity by cultured human lymphocytes: Characteristics of effector cells and specificity of cytotoxicity. J. Immunol. 122, 1489-1494 (1979).
4. C. A. Biron, R. M. Welsh, Activation and role of natural killer cells in virus infections. Med. Microbiol. Immunol. 170, 155-172 (1982).
5. J. P. Di Santo, Functionally distinct NK-cell subsets: Developmental origins and biological implications. Eur. J. Immunol. 38, 2948-2951 (2008).
6. M. Colonna, Specificity and function of immunoglobulin superfamily NK cell inhibitory and stimulatory receptors. Immunol. Rev. 155, 127-133 (1997).
7. D. H. Raulet, W. Held, I. Correa, J. R. Dorfman, M. F. Wu, L. Corral, Specificity, tolerance and developmental regulation of natural killer cells defined by expression of class I-specific Ly49 receptors. Immunol. Rev. 155, 41-52 (1997).
8. L. L. Lanier, Natural killer cells: From no receptors to too many. Immunity 6, 371-378 (1997).
9. H. G. H. Ljunggren, K. K. Kärre, In search of the "missing self": MHC molecules and NK cell recognition. Immunol. Today 11, 237-244 (1990).
10. E. Vivier, S. Ugolini, Natural killer cells: From basic research to treatments. Front. Immunol. 2, 18 (2011).
11. N. M. N. Valiante, M. M. Uhrberg, H. G. H. Shilling, K. K. Lienert-Weidenbach, K. L. K. Arnett, A. A. D'Andrea, J. H. J. Phillips, L. L. L. Lanier, P. P. Parham, Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7, 739-751 (1997).
12. N. N. Wagtmann, S. S. Rajagopalan, C. C. C. Winter, M. M. Peruzzi, E. O. E. Long, Killer cell inhibitory receptors specific for HLA-C and HLA-B identified by direct binding and by functional transfer. Immunity 3, 801-809 (1995).
13. M. Colonna, J. Samaridis, Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268, 405-408 (1995).
14. M. Sternberg-Simon, P. Brodin, Y. Pickman, B. Onfelt, K. Kärre, K. J. Malmberg, P. Höglund, R. Mehr, Natural killer cell inhibitory receptor expression in humans and mice: A closer look. Front. Immunol. 4, 1-12 (2013).
15. M. Yawata, N. Yawata, M. Draghi, F. Partheniou, A. M. Little, P. Parham, 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 (2008).
16. H. G. Shilling, K. L. McQueen, N. W. Cheng, J. A. Shizuru, R. S. Negrin, P. Parham, Reconstitution of NK cell receptor repertoire following HLA-matched hematopoietic cell transplantation. Blood 101, 3730-3740 (2003).
17. V. Béziat, L. Liu, J. A. Malmberg, M. A. Ivarsson, E. Sohlberg, A. T. Björklund, C. Retière, E. Sverremark-Ekström, J. Traherne, P. Ljungman, M. Schaffer, D. A. Price, J. Trowsdale, J. Michaëlsson, H. G. Ljunggren, K. J. Malmberg, NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 121, 2678-2688 (2013).
18. K. Schönberg, M. Sribar, J. Enczmann, J. C. Fischer, M. Uhrberg, Analyses of HLA-C-specific KIR repertoires in donors with group A and B haplotypes suggest a ligand-instructed model of NK cell receptor acquisition. Blood 117, 98-107 (2011).
19. K. Schönberg, J. C. Fischer, G. Kögler, M. Uhrberg, Neonatal NK-cell repertoires are functionally, but not structurally, biased toward recognition of self HLA class I. Blood 117, 5152-5156 (2011).
20. F. Cichocki, J. S. Miller, S. K. Anderson, Y. T. Bryceson, Epigenetic regulation of NK cell differentiation and effector functions. Front. Immunol. 4, 55 (2013).
21. N. K. Bjorkström, T. Lindgren, M. Stoltz, C. Fauriat, M. Braun, M. Evander, J. Michaëlsson, K. J. Malmberg, J. Klingström, C. Ahlm, H. G. Ljunggren, Rapid expansion and long-term persistence of elevated NK cell numbers in humans infected with hantavirus. J. Exp. Med. 208, 13-21 (2011).
22. C. Petitdemange, P. Becquart, N. Wauquier, V. Béziat, P. Debré, E. M. Leroy, V. Vieillard, W. M. Yokoyama, Unconventional repertoire profile is imprinted during acute chikungunya infection for natural killer cells polarization toward cytotoxicity. PLoS Pathog. 7, e1002268 (2011).
23. S. Lopez-Vergès, J. M. Milush, B. S. Schwartz, M. J. Pando, J. Jarjoura, V. A. York, J. P. Houchins, S. Miller, S. M. Kang, P. J. Norris, D. F. Nixon, L. L. Lanier, Expansion of a unique CD57+NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc. Natl. Acad. Sci. U.S.A. 108, 14725-14732 (2011).
24. + natural killer cells with potent function. Blood 119, 2665 -2674 (2012).
25. S. C. Bendall, E. F. Simonds, P. Qiu, E. A. D. Amir, P. O. Krutzik, R. Finck, R. V. Bruggner, R. Melamed, A. Trejo, O. I. Ornatsky, R. S. Balderas, S. K. Plevritis, K. Sachs, D. Pe'er, S. D. Tanner, G. P. Nolan, Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science 332, 687-696 (2011).
26. + T cell phenotypes. Immunity 36, 142-152 (2012).
27. S. S. Bauer, V. V. Groh, J. J. Wu, A. A. Steinle, J. H. J. Phillips, L. L. L. Lanier, T. T. Spies, Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285, 727-729 (1999).
28. S. Sivori, M. Falco, L. Moretta, A. Moretta, Extending killer Ig-like receptor function: From HLA class I recognition to sensors of microbial products. Trends Immunol. 31, 289-294 (2010).
29. A. Silva, D. M. Andrews, A. G. Brooks, M. J. Smyth, Y. Hayakawa, Application of CD27 as a marker for distinguishing human NK cell subsets. Int. Immunol. 20, 625-630 (2008).
30. M. Della Chiesa, M. Falco, M. Podestà, F. Locatelli, L. Moretta, F. Frassoni, A. Moretta, Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: A role for human cytomegalovirus? Blood 119, 399-410 (2012).
31. P. André, R. Castriconi, M. Espéli, N. Anfossi, T. Juarez, S. Huë, H. Conway, F. Romagné, A. Dondero, M. Nanni, S. Caillat-Zucman, D. H. Raulet, C. Bottino, E. Vivier, A. Moretta, P. Paul, Comparative analysis of human NK cell activation induced by NKG2D and natural cytotoxicity receptors. Eur. J. Immunol. 34, 961-971 (2004).
32. J. M. Milush, B. R. Long, J. E. Snyder-Cappione, A. J. Cappione, V. A. York, L. C. Ndhlovu, L. L. Lanier, J. Michaëlsson, D. F. Nixon, Functionally distinct subsets of human NK cells and monocyte/DC-like cells identified by coexpression of CD56, CD7, and CD4. Blood 114, 4823 - 4831 (2009).
33. dim NK-cell differentiation uncoupled from NK-cell education. Blood 116, 3853-3864 (2010).
34. M. Yawata, N. Yawata, M. Draghi, A. M. Little, F. Partheniou, P. Parham, Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J. Exp. Med. 203, 633-645 (2006).
35. P. P. Qiu, E. F. E. Simonds, S. C. S. Bendall, K. D. K. Gibbs, R. V. R. Bruggner, M. D. M. Linderman, K. K. Sachs, G. P. G. Nolan, S. K. S. Plevritis, Extracting a cellular hierarchy from high-dimensional cytometry data with SPADE. Nat. Biotechnol. 29, 886-891 (2011).
36. M. Gumá, A. Angulo, C. Vilches, N. Gómez-Lozano, N. Malats, M. López-Botet, Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104, 3664-3671 (2004).
37. M. Gumá, M. Budt, A. Sáez, T. Brckalo, H. Hengel, A. Angulo, M. López-Botet, Expansion of CD94/NKG2C+ NK cells in response to human cytomegalovirus-infected fibroblasts. Blood 107, 3624 -3631 (2006).
38. N. J. Gotelli, R. K. Colwell, Estimating species richness, in Biological Diversity: Frontiers in Measurement and Assessment, A. E. Magurran, B. J. McGill, Eds. (Oxford Univ. Press, Oxford, 2010), pp. 39-54.
39. N. J. Gotelli, R. K. Colwell, Quantifying biodiversity: Procedures and pitfalls in the measurement and comparison of species richness. Ecol. Lett. 4, 379-391 (2001).
40. R. K. Colwell, Biodiversity: Concepts, patterns, and measurement, in The Princeton Guide to Ecology (Princeton Univ. Press, Princeton, 2009), pp. 257-263.
41. B. P. Shum, L. R. Flodin, D. G. Muir, R. Rajalingam, S. I. Khakoo, S. Cleland, L. A. Guethlein, M. Uhrberg, P. Parham, Conservation and variation in human and common chimpanzee CD94 and NKG2 genes. J. Immunol. 168, 240-252 (2002).
42. J. H. Evans, A. Horowitz, M. Mehrabi, E. L. Wise, J. E. Pease, E. M. Riley, D. M. Davis, A distinct subset of human NK cells expressing HLA-DR expand in response to IL-2 and can aid immune responses to BCG. Eur. J. Immunol. 41, 1924-1933 (2011).
43. B. Grzywacz, N. Kataria, M. Sikora, R. A. Oostendorp, E. A. Dzierzak, B. R. Blazar, J. S. Miller, M. R. Verneris, Coordinated acquisition of inhibitory and activating receptors and functional properties by developing human natural killer cells. Blood 108, 3824-3833 (2006).
44. + natural killer (NK) cells and decrease in NKp46+ NK cells in response to influenza. Immunology 132, 516-526 (2011).
45. R. Marlin, M. Duriez, N. Berkane, C. De Truchis, Y. Madec, M. A. Rey-Cuille, J. S. Cummings, C. Cannou, H. Quillay, F. Barré-Sinoussi, M. T. Nugeyre, E. Menu, Dynamic shift from CD85j/ILT-2 to NKG2D NK receptor expression pattern on human decidual NK during the first trimester of pregnancy. PLoS One 7, e30017 (2012).
46. H. G. Hilton, L. Vago, A. M. Older Aguilar, A. K. Moesta, T. Graef, L. Abi-Rached, P. J. Norman, L. A. Guethlein, K. Fleischhauer, P. Parham, 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. J. Immunol. 189, 1418-1430 (2012).
47. P. J. Norman, L. Abi-Rached, K. Gendzekhadze, D. Korbel, M. Gleimer, D. Rowley, D. Bruno, C. V. F. Carrington, D. Chandanayingyong, Y. H. Chang, C. Crespí, G. Saruhan-Direskeneli, P. A. Fraser, K. Hameed, G. Kamkamidze, K. A. Koram, Z. Layrisse, N. Matamoros, J. Milà, M. H. Park, R. M. Pitchappan, D. D. Ramdath, M. Y. Shiau, H. A. F. Stephens, S. Struik, D. H. Verity, R. W. Vaughan, D. Tyan, R. W. Davis, E. M. Riley, M. Ronaghi, P. Parham, Unusual selection on the KIR3DL1/S1 natural killer cell receptor in Africans. Nat. Genet. 39, 1092-1099 (2007).
48. T. Graef, A. K. Moesta, P. J. Norman, L. Abi-Rached, L. Vago, A. M. Older Aguilar, M. Gleimer, J. A. Hammond, L. A. Guethlein, D. A. Bushnell, P. J. Robinson, P. Parham, KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. J. Exp. Med. 206, 2557-2572 (2009).
49. K.-J. Malmberg, J. Michaëlsson, P. Parham, H.-G. Ljunggren, Killer cell immunoglobulin-like receptor workshop: Insights into evolution, genetics, function, and translation. Immunity 35, 653-657 (2011).
50. Y. T. Bryceson, M. E. March, H. G. Ljunggren, E. O. Long, Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107, 159-166 (2006).
51. H. G. H. Shilling, N. N. Young, L. A. L. Guethlein, N. W. N. Cheng, C. M. C. Gardiner, D. D. Tyan, P. P. Parham, Genetic control of human NK cell repertoire. J. Immunol. 169, 239-247 (2002).
52. N. Anfossi, P. André, S. Guia, C. S. Falk, S. Roetynck, C. A. Stewart, V. Breso, C. Frassati, D. Reviron, D. Middleton, F. Romagné, S. Ugolini, E. Vivier, Human NK cell education by inhibitory receptors for MHC class I. Immunity 25, 331-342 (2006).
53. N. Tarek, J. B. Le Luduec, M. M. Gallagher, J. Zheng, J. M. Venstrom, E. Chamberlain, S. Modak, G. Heller, B. Dupont, N. K. V. Cheung, K. C. Hsu, Unlicensed NK cells target neuroblastoma following anti-GD2 antibody treatment. J. Clin. Invest. 122, 3260-3270 (2012).
54. + NK cells are enriched in AIDS patients with advanced-stage Kaposi's sarcoma. J. Virol. 81, 430-433 (2006).
55. R. E. Krasnow, L. M. Jack, C. N. Lessov-Schlaggar, A. W. Bergen, G. E. Swan, The Twin Research Registry at SRI International. Twin Res. Hum. Genet. 16, 463-470 (2013).
56. P. J. Norman, L. Abi-Rached, K. Gendzekhadze, J. A. Hammond, A. K. Moesta, D. Sharma, T. Graef, K. L. McQueen, L. A. Guethlein, C. V. F. Carrington, D. Chandanayingyong, Y. H. Chang, C. Crespí, G. Saruhan-Direskeneli, K. Hameed, G. Kamkamidze, K. A. Koram, Z. Layrisse, N. Matamoros, J. Milà, M. H. Park, R. M. Pitchappan, D. D. Ramdath, M. Y. Shiau, H. A. F. Stephens, S. Struik, D. Tyan, D. H. Verity, R. W. Vaughan, R. W. Davis, P. A. Fraser, E. M. Riley, M. Ronaghi, P. Parham, Meiotic recombination generates rich diversity in NK cell receptor genes, alleles, and haplotypes. Genome Res. 19, 757-769 (2009).