Human NK cells licensed by killer Ig receptor genes have an altered cytokine program that modifies CD4+ T cell function

Journal of Immunology

Volumn 193, Issue 2, 2014, Pages 940-949

  Lin, Lin ^a   Ma, Chao ^b   Wei, Bo ^a   Aziz, Najib ^a   Rajalingam, Raja ^a   Yusung, Susy ^c   Erlich, Henry A ^d   Trachtenberg, Elizabeth A ^e   Targan, Stephan R ^f   McGovern, Dermot P B ^f,g   Heath, James R ^a,b,h   Braun, Jonathan ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c MATTEL CHILDREN S HOSPITAL   (United States)

^d CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

^e STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f F Widjaja Foundation Inflammatory Bowel and Immunobiology Research Institute   (United States)

^g CEDARS SINAI MEDICAL CENTER   (United States)

^h California Institute of Technology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; HLA C ANTIGEN; HLA C1 ANTIGEN; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 6; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; RANTES; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADULT; ARTICLE; CD4+ T LYMPHOCYTE; CHILD; CLINICAL ARTICLE; CYTOKINE PRODUCTION; EX VIVO STUDY; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MALE; MICROFLUIDIC ANALYSIS; MIDDLE AGED; NATURAL KILLER CELL; PRIORITY JOURNAL; SCHOOL CHILD; T LYMPHOCYTE ACTIVATION; TH17 CELL;

CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CLUSTER ANALYSIS; COCULTURE TECHNIQUES; CROHN DISEASE; CYTOKINES; FLOW CYTOMETRY; HLA-C ANTIGENS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-17; INTERLEUKIN-6; INTERLEUKINS; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; RECEPTORS, KIR; RECEPTORS, KIR2DL3; TH17 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84904250327     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400093     Document Type: Article

References (50)

1. Hesslein, D. G., and L. L. Lanier. 2011. Transcriptional control of natural killer cell development and function. Adv. Immunol. 109: 45-85.
2. Elliott, J. M., and W. M. Yokoyama. 2011. Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol. 32: 364-372.
3. Vivier, E., E. Tomasello, M. Baratin, T. Walzer, and S. Ugolini. 2008. Functions of natural killer cells. Nat. Immunol. 9: 503-510. (Pubitemid 351560519)
4. Vivier, E., D. H. Raulet, A. Moretta, M. A. Caligiuri, L. Zitvogel, L. L. Lanier, W. M. Yokoyama, and S. Ugolini. 2011. Innate or adaptive immunity? The example of natural killer cells. Science 331: 44-49.
5. Bashirova, A. A., R. Thomas, and M. Carrington. 2011. HLA/KIR restraint of HIV: surviving the fittest. Annu. Rev. Immunol. 29: 295-317.
6. Khakoo, S. I., and M. Carrington. 2006. KIR and disease: a model system or system of models? Immunol. Rev. 214: 186-201. (Pubitemid 44707911)
7. Jostins, L., S. Ripke, R. K. Weersma, R. H. Duerr, D. P. McGovern, K. Y. Hui, J. C. Lee, L. P. Schumm, Y. Sharma, C. A. Anderson, et al. 2012. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491: 119-124.
8. Hall, L. J., C. T. Murphy, A. Quinlan, G. Hurley, F. Shanahan, K. Nally, and S. Melgar. 2013. Natural killer cells protect mice from DSS-induced colitis by regulating neutrophil function via the NKG2A receptor. Mucosal Immunol. 6: 1016-1026.
9. Saha, S., X. Jing, S. Y. Park, S. Wang, X. Li, D. Gupta, and R. Dziarski. 2010. Peptidoglycan recognition proteins protect mice from experimental colitis by promoting normal gut flora and preventing induction of interferon-gamma. Cell Host Microbe 8: 147-162.
10. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274. (Pubitemid 40563170)
11. Fauriat, C., M. A. Ivarsson, H. G. Ljunggren, K. J. Malmberg, and J. Michaëlsson. 2010. Education of human natural killer cells by activating killer cell immunoglobulin-like receptors. Blood 115: 1166-1174.
12. Du, Z., D. W. Gjertson, E. F. Reed, and R. Rajalingam. 2007. Receptor-ligand analyses define minimal killer cell Ig-like receptor (KIR) in humans. Immunogenetics 59: 1-15. (Pubitemid 46011187)
13. Hollenbach, J. A., M. B. Ladner, K. Saeteurn, K. D. Taylor, L. Mei, T. Haritunians, D. P. McGovern, H. A. Erlich, J. I. Rotter, and E. A. Trachtenberg. 2009. Susceptibility to Crohn's disease is mediated by KIR2DL2/KIR2DL3 heterozygosity and the HLA-C ligand. Immunogenetics 61: 663-671.
14. Wilson, T. J., M. Jobim, L. F. Jobim, P. Portela, P. H. Salim, M. A. Rosito, D. C. Damin, C. Flores, A. Peres, M. B. Machado, et al. 2010. Study of killer immunoglobulin-like receptor genes and human leukocyte antigens class I ligands in a Caucasian Brazilian population with Crohn's disease and ulcerative colitis. Hum. Immunol. 71: 293-297.
15. Jones, D. C., R. S. Edgar, T. Ahmad, J. R. Cummings, D. P. Jewell, J. Trowsdale, and N. T. Young. 2006. Killer Ig-like receptor (KIR) genotype and HLA ligand combinations in ulcerative colitis susceptibility. Genes Immun. 7: 576-582. (Pubitemid 44614872)
16. Yokoyama, W. M., and S. Kim. 2006. How do natural killer cells find self to achieve tolerance? Immunity 24: 249-257.
17. Anfossi, N., P. André, S. Guia, C. S. Falk, S. Roetynck, C. A. Stewart, V. Breso, C. Frassati, D. Reviron, D. Middleton, et al. 2006. Human NK cell education by inhibitory receptors for MHC class I. Immunity 25: 331-342. (Pubitemid 44224147)
18. Fauriat, C., E. O. Long, H. G. Ljunggren, and Y. T. Bryceson. 2010. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood 115: 2167-2176.
19. Hollenbach, J. A., I. Nocedal, M. B. Ladner, R. M. Single, and E. A. Trachtenberg. 2012. Killer cell immunoglobulin-like receptor (KIR) gene content variation in the HGDP-CEPH populations. Immunogenetics 64: 719-737.
20. Yawata, M., N. Yawata, M. Draghi, F. Partheniou, A. M. Little, and P. Parham. 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.
21. Neurath, M. F., S. Finotto, and L. H. Glimcher. 2002. The role of Th1/Th2 polarization in mucosal immunity. Nat. Med. 8: 567-573. (Pubitemid 34633433)
22. Bouma, G., and W. Strober. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3: 521-533. (Pubitemid 37328672)
23. Kim, S., J. B. Sunwoo, L. Yang, T. Choi, Y. J. Song, A. R. French, A. Vlahiotis, J. F. Piccirillo, M. Cella, M. Colonna, et al. 2008. HLA alleles determine differences in human natural killer cell responsiveness and potency. Proc. Natl. Acad. Sci. USA 105: 3053-3058. (Pubitemid 351723666)
24. Shi, F. D., and L. Van Kaer. 2006. Reciprocal regulation between natural killer cells and autoreactive T cells. Nat. Rev. Immunol. 6: 751-760. (Pubitemid 44453461)
25. Narni-Mancinelli, E., B. N. Jaeger, C. Bernat, A. Fenis, S. Kung, A. De Gassart, S. Mahmood, M. Gut, S. C. Heath, J. Estellé, et al. 2012. Tuning of natural killer cell reactivity by NKp46 and Helios calibrates T cell responses. Science 335: 344-348.
26. Martín-Fontecha, A., L. L. Thomsen, S. Brett, C. Gerard, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2004. Induced recruitment of NK cells to lymph nodes provides IFN-γ for T(H)1 priming. Nat. Immunol. 5: 1260-1265. (Pubitemid 41057741)
27. Assarsson, E., T. Kambayashi, J. D. Schatzle, S. O. Cramer, A. von Bonin, P. E. Jensen, H. G. Ljunggren, and B. J. Chambers. 2004. NK cells stimulate proliferation of T and NK cells through 2B4/CD48 interactions. J. Immunol. 173: 174-180. (Pubitemid 38797339)
28. + T cells via OX40- OX40 ligand interactions. J. Immunol. 173: 3716-3724.
29. Hanna, J., T. Gonen-Gross, J. Fitchett, T. Rowe, M. Daniels, T. I. Arnon, R. Gazit, A. Joseph, K. W. Schjetne, A. Steinle, et al. 2004. Novel APC-like properties of human NK cells directly regulate T cell activation. J. Clin. Invest. 114: 1612-1623. (Pubitemid 40385552)
30. Ma, C., R. Fan, H. Ahmad, Q. Shi, B. Comin-Anduix, T. Chodon, R. C. Koya, C. C. Liu, G. A. Kwong, C. G. Radu, et al. 2011. A clinical microchip for evaluation of single immune cells reveals high functional heterogeneity in phenotypically similar T cells. Nat. Med. 17: 738-743.
31. Fan, R., O. Vermesh, A. Srivastava, B. K. Yen, L. Qin, H. Ahmad, G. A. Kwong, C. C. Liu, J. Gould, L. Hood, and J. R. Heath. 2008. Integrated barcode chips for rapid, multiplexed analysis of proteins in microliter quantities of blood. Nat. Biotechnol. 26: 1373-1378.
32. Valiante, N. M., M. Uhrberg, H. G. Shilling, K. Lienert-Weidenbach, K. L. Arnett, A. D'Andrea, J. H. Phillips, L. L. Lanier, and P. Parham. 1997. Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7: 739-751. (Pubitemid 28064888)
33. McGeachy, M. J., and D. J. Cua. 2008. Th17 cell differentiation: the long and winding road. Immunity 28: 445-453. (Pubitemid 351467042)
34. Franke, A., D. P. McGovern, J. C. Barrett, K. Wang, G. L. Radford-Smith, T. Ahmad, C. W. Lees, T. Balschun, J. Lee, R. Roberts, et al. 2010. Genomewide meta-analysis increases to 71 the number of confirmed Crohn's disease susceptibility loci. Nat. Genet. 42: 1118-1125.
35. Acosta-Rodriguez, E. V., G. Napolitani, A. Lanzavecchia, and F. Sallusto. 2007. Interleukins 1β and 6 but not transforming growth factor-β are essential for the differentiation of interleukin 17-producing human T helper cells. Nat. Immunol. 8: 942-949. (Pubitemid 47300008)
36. Wilson, N. J., K. Boniface, J. R. Chan, B. S. McKenzie, W. M. Blumenschein, J. D. Mattson, B. Basham, K. Smith, T. Chen, F. Morel, et al. 2007. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat. Immunol. 8: 950-957.
37. Anderson, C. A., G. Boucher, C. W. Lees, A. Franke, M. D'Amato, K. D. Taylor, J. C. Lee, P. Goyette, M. Imielinski, A. Latiano, et al. 2011. Meta-analysis identifies 29 additional ulcerative colitis risk loci, increasing the number of confirmed associations to 47. Nat. Genet. 43: 246-252.
38. McGovern, D. P., A. Gardet, L. Törkvist, P. Goyette, J. Essers, K. D. Taylor, B. M. Neale, R. T. Ong, C. Lagacé, C. Li, et al. 2010. Genome-wide association identifies multiple ulcerative colitis susceptibility loci. Nat. Genet. 42: 332-337.
39. Martin, M. P., G. Nelson, J. H. Lee, F. Pellett, X. Gao, J. Wade, M. J. Wilson, J. Trowsdale, D. Gladman, and M. Carrington. 2002. Cutting edge: susceptibility to psoriatic arthritis: influence of activating killer Ig-like receptor genes in the absence of specific HLA-C alleles. J. Immunol. 169: 2818-2822. (Pubitemid 35013118)
40. Moodie, S. J., P. J. Norman, A. L. King, J. S. Fraser, D. Curtis, H. J. Ellis, R. W. Vaughan, and P. J. Ciclitira. 2002. Analysis of candidate genes on chromosome 19 in coeliac disease: an association study of the KIR and LILR gene clusters. Eur. J. Immunogenet. 29: 287-291.
41. Chan, A. T., S. D. Kollnberger, L. R. Wedderburn, and P. Bowness. 2005. Expansion and enhanced survival of natural killer cells expressing the killer immunoglobulin-like receptor KIR3DL2 in spondylarthritis. Arthritis Rheum. 52: 3586-3595. (Pubitemid 41612228)
42. Brodin, P., T. Lakshmikanth, K. Kärre, and P. Höglund. 2012. Skewing of the NK cell repertoire by MHC class I via quantitatively controlled enrichment and contraction of specific Ly49 subsets. J. Immunol. 188: 2218-2226.
43. Zhi, D., C. Sun, S. K. Sedimbi, F. Luo, S. Shen, and C. B. Sanjeevi. 2011. Killer cell immunoglobulin-like receptor along with HLA-C ligand genes are associated with type 1 diabetes in Chinese Han population. Diabetes Metab. Res. Rev. 27: 872-877.
44. Mehers, K. L., A. E. Long, A. R. van der Slik, R. J. Aitken, V. Nathwani, F. S. Wong, S. Bain, G. Gill, B. O. Roep, P. J. Bingley, and K. M. Gillespie. 2011. An increased frequency of NK cell receptor and HLA-C group 1 combinations in early-onset type 1 diabetes. Diabetologia 54: 3062-3070.
45. Shastry, A., S. K. Sedimbi, R. Rajalingam, L. Nikitina-Zake, I. Rumba, H. Wigzell, and C. B. Sanjeevi. 2008. Combination of KIR 2DL2 and HLA-C1 (Asn 80) confers susceptibility to type 1 diabetes in Latvians. Int. J. Immunogenet. 35: 439-446.
46. + memory T cells. Immunity 38: 131-139.
47. + T cells by enhancing T cell receptor signaling. Immunity 38: 140-152.
48. + subset expressing natural killer markers and a singular pattern of adhesion molecules. Scand. J. Immunol. 52: 1-6.
49. Sips, M., G. Sciaranghella, T. Diefenbach, A. S. Dugast, C. T. Berger, Q. Liu, D. Kwon, M. Ghebremichael, J. D. Estes, M. Carrington, et al. 2012. Altered distribution of mucosal NK cells during HIV infection. Mucosal Immunol. 5: 30-40.
50. León, F., E. Roldán, L. Sanchez, C. Camarero, A. Bootello, and G. Roy. 2003. Human small-intestinal epithelium contains functional natural killer lymphocytes. Gastroenterology 125: 345-356. (Pubitemid 36929414)