Skip to main content

Adaptive features of natural killer cells, lymphocytes of innate immunity

Abstract

Natural killer cells (NK cells) are traditionally attributed to the innate immune system. It is considered that previously received stimuli have little effect on the functioning of these immune cells. Indeed, NK cells even without prior sensitization provide a rapid effector response against tumor, virus-infected, or otherwise damaged cells. They have a limited repertoire of receptors, the expression of which does not require somatic recombination. However, recent data indicate that NK cells may acquire the properties specific to adaptive immune cells. In particular, NK cells have been shown to possess the features of immunological memory, namely, the ability to more quickly and effectively respond to a repeated stimulus. The mechanisms of memory acquisition in NK cells differ from those implemented in T and B lymphocytes and are still rather vague. Presumably, some of these mechanisms underlie the significant phenotypic and functional NK cell diversity emerging during their differentiation. The recent data accumulated in this area considerably change the existing immunology paradigm, which postulates a clear delineation of the adaptive and innate immune cells. The published data on phenotypic and functional characteristics of NK cells and particular changes in these characteristics during NK cell differentiation and generation of memory-like NK cells are reviewed.

This is a preview of subscription content, access via your institution.

Abbreviations

ADCC:

antibody-dependent cell-mediated cytotoxicity

aKIRs:

activating KIRs

CLP:

common lymphoid progenitor

HCMV:

human cytomegalovirus

IFNγ:

interferon-γ

IL:

interleukin

IL-2(12,15,18)R:

IL-2(12,15,18) receptors

ILCs:

innate lymphoid cells

ITAM:

immunoreceptor tyrosinebased activation motif

ITIM:

immunoreceptor tyrosine-based inhibition motif

KIR:

killer-cell immunoglobulin-like receptor family

MHC:

major histocompatibility complex

NCRs:

natural cytotoxicity receptors

NK cells:

natural killer cells

PI3K:

phosphatidylinositol-3-kinase

PLC:

phospholipase C

RAGs:

recombination activating genes

SLAM:

signaling lymphocyte activation molecule.

References

  1. Hellstrom, I. and Hellstrom, K.E, Cancer, 1974, vol. 34, suppl. 4, pp. 1461–1468.

    Article  Google Scholar 

  2. Spits, H., Artis, D., Colonna, M., Diefenbach, A, Di Santo, J.P., Eberl, G., and Vivier, E, Nature Rev. Immunol., 2013, vol. 13, pp. 145–149.

    CAS  Article  Google Scholar 

  3. Eberl, G., Colonna, M, Di Santo, J.P., and McKenzie, A.N, Science, 2015, vol. 348, aaa6566.

  4. Yokoyama, W.M., Sojka, D.K., Peng, H., and Tian, Z, Cold Spring Harb. Symp. Quant. Biol., 2013, vol. 78, pp. 149–156.

    PubMed  Article  Google Scholar 

  5. Erick, T.K. and Brossay, L, Curr. Opin. Immunol., 2016, vol. 38, pp. 67–74.

    CAS  PubMed  Article  Google Scholar 

  6. Moretta, L., Biassoni, R., Bottino, C., Mingari, M.C., and Moretta, A, Scand. J. Immunol., 2002, vol. 55, pp. 229–232.

    CAS  PubMed  Article  Google Scholar 

  7. Sintsov, A.V., Kovalenko, E.I., and Khanin, M.A, Russ. J. Bioorg. Chem., 2008, vol. 34, pp. 647–654.

    CAS  Article  Google Scholar 

  8. Montaldo, E, Del Zotto, G, Della, Chiesa M., Mingari, M.C., Moretta, A., De Maria, A., and Moretta, L., Cytometry A, 2013, vol. 83, pp. 702–713.

    PubMed  Article  Google Scholar 

  9. Bryceson, Y.T., March, M.E., Ljunggren, H.G., and Long, E.O, Blood, 2006, vol. 107, pp. 159–166.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  10. Romee, R., Leong, J.W., and Fehniger, T.A, Scientifica (Cairo), 2014, vol. 205796. doi: 10.1155/2014/205796

  11. Dybkaer, K., Iqbal, J., Zhou, G., Geng, H., Xiao, L., Schmitz, A., d’Amore, F., and Chan, W.C., BMC Genomics, 2007, vol. 8, p. 230.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  12. Mishra, A., Sullivan, L., and Caligiuri, M.A, Clin. Cancer Res., 2014, vol. 20, pp. 2044–2050.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Nandagopal, N., Ali, A.K., Komal, A.K., and Lee, S.H, Front. Immunol., 2014, vol. 5, p. 187.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  14. Orange, J.S. and Biron, C.A., J. Immunol., 1996, vol. 156, pp. 1138–1142.

    CAS  PubMed  Google Scholar 

  15. Chaix, J., Tessmer, M.S., Hoebe, K., Fuseri, N., Ryffel, B., Dalod, M., Alexopoulou, L., Beutler, B., Brossay, L., Vivier, E., and Walzer, T., J. Immunol., 2008, vol. 181, pp. 1627–1631.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Nielsen, C.M., Wolf, A.S., Goodier, M.R., and Riley, E.M, Front. Immunol., 2016, vol. 7, p. 101.

    PubMed  PubMed Central  Article  Google Scholar 

  17. Ortaldo, J.R. and Young, H.A, Semin. Immunol., 2006, vol. 18, pp. 193–196.

    CAS  PubMed  Article  Google Scholar 

  18. de Rham, C., Ferrari-Lacraz, S., Jendly, S., Schneiter, G., Dayer, J.M., and Villard, J, Arthritis Res. Ther., 2007, vol. 9, p. R125.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  19. Kanevskiy, L.M., Telford, W.G., Sapozhnikov, A.M., and Kovalenko, E.I, Front. Immunol., 2013, vol. 4, p. 11.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  20. Dubois, S., Mariner, J., Waldmann, T.A., and Tagaya, Y, Immunity, 2002, vol. 17, pp. 537–547.

    CAS  PubMed  Article  Google Scholar 

  21. Kobayashi, H., Dubois, S., Sato, N., Sabzevari, H., Sakai, Y., Waldmann, T.A., and Tagaya, Y, Blood, 2005, vol. 105, pp. 721–727.

    CAS  PubMed  Article  Google Scholar 

  22. Long, E.O., Kim, H.S., Liu, D., Peterson, M.E., and Rajagopalan, S, Annu. Rev. Immunol., 2013, vol. 31, pp. 227–258.

    CAS  PubMed  Article  Google Scholar 

  23. Fauriat, C., Long, E.O., Ljunggren, H.G., and Bryceson, Y.T, Blood, 2010, vol. 115, pp. 2167–2176.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  24. Tassi, I., Presti, R., Kim, S., Yokoyama, W.M., Gilfillan, S., and Colonna, M., J. Immunol., 2005, vol. 175, pp. 749–754.

    CAS  PubMed  Article  Google Scholar 

  25. Cella, M., Fujikawa, K., Tassi, I., Kim, S., Latinis, K., Nishi, S., Yokoyama, W., Colonna, M., and Swat, W., J. Exp. Med., 2004, vol. 200, pp. 817–823.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  26. Glasner, A., Ghadially, H., Gur, C., Stanietsky, N., Tsukerman, P., Enk, J., and Mandelboim, O., J. Immunol., 2012, vol. 188, pp. 2509–2515.

    CAS  PubMed  Article  Google Scholar 

  27. Lakshmikanth, T., Burke, S., Ali, T.H., Kimpfler, S., Ursini, F., Ruggeri, L., Capanni, M., Umansky, V., Paschen, A., Sucker, A., Pende, D., Groh, V., Biassoni, R., Höglund, P., Kato, M., Shibuya, K., Schadendorf, D., Anichini, A., Ferrone, S., Velardi, A., Kärre, K., Shibuya, A., Carbone, E., and Colucci, F.J, Clin. Invest., 2009, vol. 119, pp. 1251–1263.

    CAS  Article  Google Scholar 

  28. Pogge von Strandmann, E., Simhadri, V.R., von Tresckow, B., Sasse, S., Reiners, K.S., Hansen, H.P., Rothe, A., Boll, B., Simhadri, V.L., Borchmann, P., McKinnon, P.J., Hallek, M., and Engert, A, Immunity, 2007, vol. 27, pp. 965–974.

    CAS  PubMed  Article  Google Scholar 

  29. Brandt, C.S., Baratin, M., Yi, E.C., Kennedy, J., Gao, Z., Fox, B., Haldeman, B., Ostrander, C.D., Kaifu, T., Chabannon, C., Moretta, A., West, R., Xu, W., Vivier, E., and Levin, S.D., J. Exp. Med., 2009, vol. 206, pp. 1495–1503.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. Hartmann, J., Tran, T.V., Kaudeer, J., Oberle, K., Herrmann, J., Quagliano, I., Abel, T., Cohnen, A., Gatterdam, V., Jacobs, A., Wollscheid, B., Watzl, C., Diefenbach, A., and Koch, J., J. Biol. Chem., 2012, vol. 287, pp. 31527–31539.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  31. Byrd, A., Hoffmann, S.C., Jarahian, M., Momburg, F., and Watzl, C., PLoS ONE, 2007, vol. 2, p. e1339.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  32. Arnon, T.I., Achdout, H., Levi, O., Markel, G., Saleh, N., Katz, G., Gazit, R., Gonen-Gross, T., Hanna, J., Nahari, E., Porgador, A., Honigman, A., Plachter, B., Mevorach, D., Wolf, D.G., and Mandelboim, O, Nat. Immunol., 2005, vol. 6, pp. 515–523.

    CAS  PubMed  Article  Google Scholar 

  33. Wang, W., Guo, H., Geng, J., Zheng, X., Wei, H., Sun, R., and Tian, Z., J. Biol. Chem., 2014, vol. 289, pp. 33311–33319.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. Rosental, B., Brusilovsky, M., Hadad, U., Oz, D., Appel, M.Y., Afergan, F., Yossef, R., Rosenberg, L.A., Aharoni, A., Cerwenka, A., Campbell, K.S., Braiman, A., and Porgador, A., J. Immunol.,2011, vol. 187, pp. 5693–5702.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Horton, N.C. and Mathew, P.A, Front. Immunol., 2015, vol. 6, p. 31.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  36. Colucci, F., Schweighoffer, E., Tomasello, E., Turner, M., Ortaldo, J.R., Vivier, E., Tybulewicz, V.L., and Di Santo, J.P, Nat. Immunol., 2002, vol. 3, pp. 288–294.

    CAS  PubMed  Article  Google Scholar 

  37. Billadeau, D.D., Upshaw, J.L., Schoon, R.A., Dick, C.J., and Leibson, P.J, Nat. Immunol., 2003, vol. 4, pp. 557–564.

    CAS  PubMed  Article  Google Scholar 

  38. Eagle, R.A, Nat. Rev. Immunol., 2007, vol. 7, pp. 737–744.

    CAS  PubMed  Article  Google Scholar 

  39. Champsaur, M. and Lanier, L.L, Immunol. Rev., 2010, vol. 235, pp. 267–285.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  40. Klinkova, A.V., Kuz’mina, E.G., Abakushina, E.V., Kanevskii, L.M., Neprina, G.S., Pavlov, V.V., and Kovalenko, E.I, Med. Immunol., 2016, vol. 18, pp. 151–162.

    Article  Google Scholar 

  41. Veillette, A, Cold Spring Harb. Perspect. Biol., 2010, vol. 2, p. a002469.

    PubMed  PubMed Central  Article  Google Scholar 

  42. Latour, S., Roncagalli, R., Chen, R., Bakinowski, M., Shi, X., Schwartzberg, P.L., Davidson, D., and Veillette, A, Nat. Cell Biol., 2003, vol. 5, pp. 149–154.

    CAS  PubMed  Article  Google Scholar 

  43. Nichols, K.E., Harkin, D.P., Levitz, S., Krainer, M., Kolquist, K.A., Genovese, C., Bernard, A., Ferguson, M., Zuo, L., Snyder, E., Buckler, A.J., Wise, C., Ashley, J., Lovett, M., Valentine, M.B., Look, A.T., Gerald, W., Housman, D.E., and Haber, D.A, Proc. Natl. Acad. Sci. U. S. A., 1998, vol. 95, pp. 13765–13770.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  44. Eissmann, P., Beauchamp, L., Wooters, J., Tilton, J.C., Long, E.O., and Watzl, C, Blood, 2005, vol. 105, pp. 4722–4729.

    CAS  PubMed  Article  Google Scholar 

  45. Welte, S., Kuttruff, S., Waldhauer, I., and Steinle, A, Nat. Immunol., 2006, vol. 7, pp. 1334–1342.

    CAS  PubMed  Article  Google Scholar 

  46. Dennehy, K.M., Klimosch, S.N., and Steinle, A., J. Immunol.,2011, vol. 186, pp. 657–661.

    CAS  PubMed  Article  Google Scholar 

  47. Carlsten, M., Bjorkstrom, N.K., Norell, H., Bryceson, Y., van Hall, T., Baumann, B.C., Hanson, M., Schedvins, K., Kiessling, R., Ljunggren, H.G., and Malmberg, K.J, Cancer Res., 2007, vol. 67, pp. 1317–1325.

    CAS  PubMed  Article  Google Scholar 

  48. Bottino, C., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., Cantoni, C., Grassi, J., Marcenaro, S., Reymond, N., Vitale, M., Moretta, L., Lopez, M., and Moretta, A., J. Exp. Med., 2003, vol. 198, pp. 557–567.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  49. Shibuya, A., Lanier, L.L., and Phillips, J.H., J. Immunol.,1998, vol. 161, pp. 1671–1676.

    CAS  PubMed  Google Scholar 

  50. Bell, G.M., Fargnoli, J., Bolen, J.B., Kish, L., and Imboden, J.B., J. Exp. Med., 1996, vol. 183, pp. 169–178.

    CAS  PubMed  Article  Google Scholar 

  51. Le Bouteiller, P., Tabiasco, J., Polgar, B., Kozma, N., Giustiniani, J., Siewiera, J., Berrebi, A., Aguerre-Girr, M., Bensussan, A., and Jabrane-Ferrat, N, Immunol. Lett., 2011, vol. 138, pp. 93–96.

    PubMed  Article  CAS  Google Scholar 

  52. Dharmadhikari, B., Wu, M., Abdullah, N.S., Rajendran, S., Ishak, N.D., Nickles, E., Harfuddin, Z., and Schwarz, H, Oncoimmunology, 2015, vol. 5, p. e1113367.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  53. Nolte, M.A., van Olffen, R.W., van Gisbergen, K.P., and van Lier, R.A, Immunol. Rev., 2009, vol. 229, pp. 216–231.

    CAS  PubMed  Article  Google Scholar 

  54. Kim, H.S. and Long, E.O, Sci. Signal, 2012, vol. 5, p. ra49.

    PubMed  Google Scholar 

  55. IPD-KIR. http://www.ebi.ac.uk/ipd/kir. Release 2.6.1, February 17, 2015.

  56. Varbanova, V., Naumova, E., and Mihaylova, A, Cancer Immunol. Immunother., 2016, vol. 65, pp. 427–440.

    CAS  PubMed  Article  Google Scholar 

  57. Stebbins, C.C., Watzl, C., Billadeau, D.D., Leibson, P.J., Burshtyn, D.N., and Long, E.O, Mol. Cell Biol., 2003, vol. 23, pp. 6291–6299.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. Long, E.O, Immunol. Rev., 2008, vol. 224, pp. 70–84.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  59. Kikuchi-Maki, A., Catina, T., and Cambpbell, K., J. Immunol.,2005, vol. 174, pp. 3859–3863.

    CAS  PubMed  Article  Google Scholar 

  60. Rajagopalan, S., Bryceson, Y.T., Kuppusamy, S.P., Geraghty, D.E., van der Meer, A., Joosten, I., and Long, E.O., PLoS Biol., 2006, vol. 4, p. e9.

  61. Kim, S., Poursine-Laurent, J., Truscott, S.M., Lybarger, L., Song, Y.J., Yang, L., French, A.R., Sunwoo, J.B., Lemieux, S., Hansen, T.H., and Yokoyama, W.M, Nature, 2005, vol. 436, pp. 709–713.

    CAS  PubMed  Article  Google Scholar 

  62. Kaiser, B.K., Barahmand-Pour, F., Paulsene, W., Medley, S., Geraghty, D.E., and Strong, R.K., J. Immunol.,2005, vol. 174, pp. 2878–2884.

    CAS  PubMed  Article  Google Scholar 

  63. Peterson, M.E. and Long, E.O, Immunity, 2008, vol. 29, pp. 578–588.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  64. Orbelyan, G.A., Tang, F., Sally, B., Solus, J., Meresse, B., Ciszewski, C., Grenier, J.C., Barreiro, L.B., Lanier, L.L., and Jabri, B., J. Immunol.,2014, vol. 193, pp. 610–616.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  65. Beziat, V., Hervier, B., Achour, A., Boutolleau, D., Marfain-Koka, A., and Vieillard, V, Blood, 2011, vol. 117, pp. 4394–4396.

    CAS  PubMed  Article  Google Scholar 

  66. Prod’homme, V., Griffin, C., Aicheler, R.J., Wang, E.C., McSharry, B.P., Rickards, C.R., Stanton, R.J., Borysiewicz, L.K., Lopez-Botet, M., Wilkinson, G.W., and Tomasec, P., J. Immunol.,2007, vol. 178, pp. 4473–4481.

    PubMed  PubMed Central  Article  Google Scholar 

  67. Nicoll, G., Avril, T., Lock, K., Furukawa, K., Bovin, N., and Crocker, P.R, Eur. J. Immunol., 2003, vol. 33, pp. 1642–1648.

    CAS  PubMed  Article  Google Scholar 

  68. Belisle, J.A., Horibata, S., Jennifer, G.A., Petrie, S., Kapur, A., Andre, S., Gabius, H.J., Rancourt, C., Connor, J., Paulson, J.C., and Patankar, M.S, Mol. Cancer, 2010, vol. 9, p. 118.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  69. Jandus, C., Boligan, K.F., Chijioke, O., Liu, H., Dahlhaus, M., Demoulins, T., Schneider, C., Wehrli, M., Hunger, R.E., Baerlocher, G.M., Simon, H.U., Romero, P., Munz, C., and von Gunten, S., J. Clin. Invest., 2014, vol. 124, pp. 1810–1820.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  70. http://www.functionalglycomics.org.

  71. Rapoport, E.M., Pazynina, G.V., Sablina, M.A., Croker, P.R., and Bovin, N.V, Biochemistry (Moscow), 2006, vol. 71, pp. 496–504.

    CAS  Article  Google Scholar 

  72. Brunetta, E., Fogli, M., Varchetta, S., Bozzo, L., Hudspeth, K.L., Marcenaro, E., Moretta, A., and Mavilio, D, Blood, 2009, vol. 114, pp. 3822–3830.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  73. Della, Chiesa M., Falco, M., Bertaina, A., Muccio, L., Alicata, C., Frassoni, F., Locatelli, F., Moretta, L., and Moretta, A., J. Immunol.,2014, vol. 192, pp. 1471–1479.

    Article  CAS  Google Scholar 

  74. Verbrugge, A., Rijkers, E.S., de Ruiter, T., and Meyaard, L, Eur. J. Immunol., 2006, vol. 36, pp. 190–198.

    CAS  PubMed  Article  Google Scholar 

  75. Geiger, T.L. and Sun, J.C, Curr. Opin. Immunol., 2016, vol. 39, pp. 82–89.

    CAS  PubMed  Article  Google Scholar 

  76. Kamizono, S., Duncan, G.S., Seidel, M.G., Morimoto, A., Hamada, K., Grosveld, G., Akashi, K., Lind, E.F., Haight, J.P., Ohashi, P.S., Look, A.T., and Mak, T.W., J. Exp. Med., 2009, vol. 206, pp. 2977–2986.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  77. Freud, A.G., Yokohama, A., Becknell, B., Lee, M.T., Mao, H.C., Ferketich, A.K., and Caligiuri, M.A., J. Exp. Med., 2006, vol. 203, pp. 1033–1043.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  78. Diefenbach, A., Colonna, M., and Koyasu, S, Immunity, 2014, vol. 41, pp. 354–365.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  79. Abakushina, E.V., Kuz’mina, E.G., and Kovalenko, E.I, Immunologiya, 2012, vol. 4, pp. 220–225.

    Google Scholar 

  80. Romagnani, C., Juelke, K., Falco, M., Morandi, B., D’Agostino, A., Costa, R., and Ferlazzo, G., J. Immunol.,2007, vol. 178, pp. 4947–4955.

    CAS  PubMed  Article  Google Scholar 

  81. Cooper, M.A., Fehniger, T.A., Turner, S.C., Chen, K.S., Ghaheri, B.A., Ghayur, T., Carson, W.E., and Caligiuri, M.A, Blood, 2001, vol. 97, pp. 3146–3151.

    CAS  PubMed  Article  Google Scholar 

  82. Milush, J.M., Lopez-Verges, S., York, V.A., Deeks, S.G., Martin, J.N., Hecht, F.M., Lanier, L.L., and Nixon, D.F, Retrovirology, 2013, vol. 10, p. 158.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  83. Mitsumoto, Y., Oka, S., Sakuma, H., Inazawa, J., and Kawasaki, T, Genomics, 2000, vol. 65, pp. 166–173.

    CAS  PubMed  Article  Google Scholar 

  84. Kanevskiy, L.M., Erokhina, S.A., Streltsova, M.A., Telford, W.G., Sapozhnikov, A.M., and Kovalenko, E.I, Biochemistry (Moscow), 2014, vol. 79, pp. 1339–1348.

    CAS  Article  Google Scholar 

  85. Lopez-Verges, S., Milush, J.M., Pandey, S., York, V.A., Arakawa-Hoyt, J., Pircher, H., Norris, P.J., Nixon, D.F., and Lanier, L.L, Blood, 2010, vol. 116, pp. 3865–3874.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  86. Yu, J., Mao, H.C., Wei, M., Hughes, T., Zhang, J., Park, I., Liu, S., McClory, S., Marcucci, G., Trotta, R., and Caligiuri, M.A, Blood, 2010, vol. 115, pp. 274–281.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  87. Juelke, K., Killig, M., Luetke-Eversloh, M., Parente, E., Gruen, J., Morandi, B., Ferlazzo, G., Thiel, A., Schmitt-Knosalla, I., and Romagnani, C, Blood, 2010, vol. 116, pp. 1299–1307.

    CAS  PubMed  Article  Google Scholar 

  88. Beziat, V., Descours, B., Parizot, C., Debré, P., and Veillard, V., PLoS ONE, 2010, vol. 5, p. e11966.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  89. Beziat, V., Liu, L.L., Malmberg, J.A., Ivarsson, M.A., Sohlberg, E., Bjorklund, A.T., Retiere, C., Sverremark-Ekstrom, E., Traherne, J., Ljungman, P., Schaffer, M., Price, D.A., Trowsdale, J., Michaelsson, J., Ljunggren, H.G., and Malmberg, K.J, Blood, 2013, vol. 121, pp. 2678–2688.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  90. Bjorkstrom, N.K., Riese, P., Heuts, F., Andersson, S., Fauriat, C., Ivarsson, M.A., Bjorklund, A.T., Flodstrom-Tullberg, M., Michaelsson, J., Rottenberg, M.E., Guzman, C.A., Ljunggren, H.G., and Malmberg, K.J, Blood, 2010, vol. 116, pp. 3853–3864.

    PubMed  Article  CAS  Google Scholar 

  91. Luetke-Eversloh, M., Killig, M., and Romagnani, C, Front. Immunol., 2013, vol. 4, p. 499.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  92. Huntington, N.D., Legrand, N., Alves, N.L., Jaron, B., Weijer, K., Plet, A., Corcuff, E., Mortier, E., Jacques, Y., Spits, H., and Di Santo James P., J. Exp. Med., 2009, vol. 206, pp. 25–34.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  93. Chan, A., Hong, D., Atzberger, A., Kollnberger, S., Filer, A.D., Buckley, C.D., McMichael, A., Enver, T., and Bowness, P., J. Immunol.,2007, vol. 179, pp. 89–94.

    CAS  PubMed  Article  Google Scholar 

  94. Guma, M., Angulo, A., Vilches, C., Gomez-Lozano, N., Malats, N., and Lopez-Botet, M, Blood, 2004, vol. 104, pp. 3664–3671.

    CAS  PubMed  Article  Google Scholar 

  95. Horowitz, A., Strauss-Albee, D.M., Leipold, M., Kubo, J., Nemat-Gorgani, N., Dogan, O.C., Dekker, C.L., Mackey, S., Maecker, H., Swan, G.E., Davis, M.M., Norman, P.J., Guethlein, L.A., Desai, M., Parham, P., and Blish, C.A, Sci. Transl. Med., 2013, vol. 5, p. 208.

    Article  CAS  Google Scholar 

  96. O’Leary, J.G., Goodarzi, M., Drayton, D.L., and von Andrian Ulrich, H, Nat. Immunol., 2006, vol. 7, pp. 507–516.

    PubMed  Article  CAS  Google Scholar 

  97. Paust, S., Gill, H.S., Wang, B., Flynn, M.P., Moseman, E.A., Senman, B., Szczepanik, M., Telenti, A., Askenase, P.W., Compans, R.W., and von Andrian Ulrich, H, Nat. Immunol., 2010, vol. 11, pp. 1127–1135.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. Sun, J.C., Beilke, J.N., and Lanier, L.L, Nature, 2009, vol. 457, pp. 557–561.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  99. Lopez-Verges, S., Milush, J.M., Schwartz, B.S., Pando, M.J., Jarjoura, J., York, V.A., Houchins, J.P., Miller, S., Kang, S., Norris, P.J., Nixon, D.F., and Lanier, L.L, Proc. Natl. Acad. Sci. U. S. A., 2011, vol. 108, pp. 14725–14732.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  100. Guma, M., Budt, M., Saez, A., Brckalo, T., Hengel, H., Angulo, A., and Lopez-Botet, M, Blood, 2006, vol. 107, pp. 3624–3631.

    CAS  PubMed  Article  Google Scholar 

  101. Della, Chiesa M., Falco, M., Podesta, M., Locatelli, F., Moretta, L., Frassoni, F., and Moretta, A, Blood, 2012, vol. 119, pp. 399–410.

    Article  CAS  Google Scholar 

  102. Foley, B., Cooley, S., Verneris, M.R., Pitt, M., Curtsinger, J., Luo, X., Lopez-Vergés, S., Lanier, L.L., Weisdorf, D., and Miller, J.S, Blood, 2012, vol. 119, pp. 2665–2674.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  103. Muccio, L., Bertaina, A., Falco, M., Pende, D., Meazza, R., Lopez-Botet, M., Moretta, L., Locatelli, F., Moretta, A., and Chiesa, M.D, Haematologica, 2016, vol. 101, pp. 371–381.

    PubMed  PubMed Central  Article  Google Scholar 

  104. Rolle, A., Pollmann, J., Ewen, E.M., Le, V.T., Halenius, A., Hengel, H., and Cerwenka, A., J. Clin. Invest., 2014, vol. 124, pp. 5305–5316.

    PubMed  PubMed Central  Article  Google Scholar 

  105. Goodier, M.R., White, M.J., Darboe, A., Nielsen, C.M., Goncalves, A., Bottomley, C., Moore, S.E., and Riley, E.M, Blood, 2014, vol. 124, pp. 2213–2222.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  106. Muntasell, A., Lopez-Montanes, M., Vera, A., Heredia, G., Romo, N., Penafiel, J., Moraru, M., Vila, J., Vilches, C., and Lopez-Botet, M, Eur. J. Immunol., 2013, vol. 43, pp. 3268–3278.

    CAS  PubMed  Article  Google Scholar 

  107. Muntasell, A., Pupuleku, A., Cisneros, E., Vera, A., Moraru, M., Vilches, C., and Lopez-Botet, M., J. Immunol.,2016, vol. 196, pp. 3818–3827.

    CAS  PubMed  Article  Google Scholar 

  108. Bjorkstrom, N.K., Lindgren, T., Stoltz, M., Fauriat, C., Braun, M., Evander, M., Michaelsson, J., Malmberg, K., Klingstrom, J., Ahlm, C., and Ljunggren, H., J. Exp. Med., 2011, vol. 208, pp. 13–21.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  109. Brunetta, E., Fogli, M., Varchetta, S., Bozzo, L., Hudspeth, K.L., Marcenaro, E., Moretta, A., and Mavilio, D., AIDS, 2010, vol. 24, pp. 27–34.

    PubMed  Article  Google Scholar 

  110. Cooper, M.A., Elliott, J.M., Keyel, P.A., Yang, L., Carrero, J.A., and Yokoyama, W.M, Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 1915–1919.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  111. Romee, R., Schneider, S.E., Leong, J.W., Chase, J.M., Keppel, C.R., Sullivan, R.P., Cooper, M.A., and Fehniger, T.A, Blood, 2012, vol. 120, pp. 4751–4760.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  112. Leong, J.W., Chase, J.M., Romee, R., Schneider, S.E., Sullivan, R.P., Cooper, M.A., and Fehniger, T.A, Biol. Blood Marrow Transplant., 2014, vol. 20, pp. 463–473.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  113. Berrien-Elliott, M.M., Wagner, J.A., and Fehniger, T.A., J. Innate Immun., 2015, vol. 7, pp. 563–571.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  114. Sun, J.C., Beilke, J.N., Bezman, N.A., and Lanier, L.L., J. Exp. Med., 2011, vol. 208, pp. 357–368.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  115. Beziat, V., Traherne, J., Malmberg, J.A., Ivarsson, M.A., Bjorkstrom, N.K., Retiere, C., Ljunggren, H.G., Michaelsson, J., Trowsdale, J., and Malmberg, K.J, Eur. J. Immunol., 2014, vol. 7, pp. 2192–2196.

    Article  CAS  Google Scholar 

  116. Liu, L.L., Landskron, J., Ask, E.H., Enqvist, M., Sohlberg, E., Traherne, J.A., Hammer, Q., Goodridge, J.P., Larsson, S., Jayaraman, J., Oei, V.Y., Schaffer, M., Tasken, K., Ljunggren, H.G., Romagnani, C., Trowsdale, J., Malmberg, K.J., and Beziat, V, Cell. Rep., 2016, vol. 15, pp. 1088–1099.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  117. Zhang, T., Scott, J.M., Hwang, I., and Kim, S., J. Immunol.,2013, vol. 190, pp. 1402–1406.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  118. Hwang, I., Zhang, T., Scott, J.M., Kim, A.R., Lee, T., Kakarla, T., Kim, A., Sunwoo, J.B., and Kim, S, Int. Immunol., 2012, vol. 24, pp. 793–802.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  119. Lee, J., Zhang, T., Hwang, I., Kim, A., Nitschke, L., Kim, M., Scott, J.M., Kamimura, Y., Lanier, L.L., and Kim, S, Immunity, 2015, vol. 42, pp. 431–442.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  120. Schlums, H., Cichocki, F., Tesi, B., Theorell, J., Beziat, V., Holmes, T.D., Han, H., Chiang, S.C., Foley, B., Mattsson, K., Larsson, S., Schaffer, M., Malmberg, K.J., Ljunggren, H.G., Miller, J.S., and Bryceson, Y.T, Immunity, 2015, vol. 42, pp. 443–456.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  121. Bezman, N.A., Kim, C.C., Sun, J.C., Min-Oo, G., Hendricks, D.W., Kamimura, Y., Best, J.A., Goldrath, A.W., and Lanier, L.L, Nat. Immunol., 2012, vol. 13, pp. 1000–1009.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. Luetke-Eversloh, M., Hammer, Q., Durek, P., Nordström, K., Gasparoni, G., Pink, M., Hamann, A., Walter, J., Chang, H.D., Dong, J., and Romagnani, C., PLoS Pathog., 2014, vol. 10, p. e1004441.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  123. Tesi, B., Schlums, H., Cichocki, F., and Bryceson, Y.T, Trends Immunol., 2016. pii S1471-4906(16)30027-8 [Epub ahead of print]. doi 10.1016/j.it.2016.04.006

    Google Scholar 

  124. Trotta, R., Chen, L., Ciarlariello, D., Josyula, S., Mao, C., Costinean, S., Yu, L., Butchar, J.P., Tridandapani, S., Croce, C.M., and Caligiuri, M.A, Blood, 2012, vol. 119, pp. 3478–3485.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  125. Childs, R.W. and Berg, M, Hematology Am. Soc. Hematol. Educ. Program., 2013, vol. 2013, pp. 234–246.

    PubMed  Google Scholar 

  126. Dudley, M.E. and Rosenberg, S.A, Semin. Oncol., 2007, vol. 34, pp. 524–531.

    PubMed  PubMed Central  Article  Google Scholar 

  127. Pende, D., Marcenaro, S., Falco, M., Martini, S., Bernardo, M.E., Montagna, D., Romeo, E., Cognet, C., Martinetti, M., Maccario, R., Mingari, M.C., Vivier, E., Moretta, L., Locatelli, F., and Moretta, A, Blood, 2009, vol. 113, pp. 3119–3129.

    CAS  PubMed  Article  Google Scholar 

  128. Lonnqvist, B., Ringden, O., Ljungman, P., Wahren, B., and Gahrton, G, Br. J. Haematol., 1986, vol. 63, pp. 671–679.

    CAS  PubMed  Article  Google Scholar 

  129. Cichocki, F., Cooley, S., Davis, Z., DeFor, T.E., Schlums, H., Zhang, B., Brunstein, C.G., Blazar, B.R., Wagner, J., Diamond, D.J., Verneris, M.R., Bryceson, Y.T., Weisdorf, D.J., and Miller, J.S, Leukemia, 2016, vol. 30, pp. 456–463.

    CAS  PubMed  Google Scholar 

  130. Bjorklund, A.T., Clancy, T., Goodridge, J.P., Beziat, V., Schaffer, M., Hovig, E., Ljunggren, H.G., Ljungman, P.T., and Malmberg, K.J., J. Immunol.,2016, vol. 196, pp. 1400–1411.

    PubMed  Article  CAS  Google Scholar 

  131. Rosario, M., Romee, R., Schneider, S., Wagner, J., Sullivan, R.P., and Fehniger, T.A, Blood, 2014, vol. 124, pp. 1117.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. I. Kovalenko.

Additional information

Original Russian Text © E.I. Kovalenko, M.A. Streltsova, 2016, published in Bioorganicheskaya Khimiya, 2016, Vol. 42, No. 6, pp. 649–667.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kovalenko, E.I., Streltsova, M.A. Adaptive features of natural killer cells, lymphocytes of innate immunity. Russ J Bioorg Chem 42, 590–605 (2016). https://doi.org/10.1134/S1068162016060066

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162016060066

Keywords

  • natural killer cells
  • adaptive NK cells
  • immunological memory
  • NK cell differentiation
  • NK cell activation