Skip to main content
Top
Published in: Immunologic Research 3/2015

01-07-2015

Practical NK cell phenotyping and variability in healthy adults

Authors: Laura S. Angelo, Pinaki P. Banerjee, Linda Monaco-Shawver, Joshua B. Rosen, George Makedonas, Lisa R. Forbes, Emily M. Mace, Jordan S. Orange

Published in: Immunologic Research | Issue 3/2015

Login to get access

Abstract

Human natural killer (NK) cells display a wide array of surface and intracellular markers that indicate various states of differentiation and/or levels of effector function. These NK cell subsets exist simultaneously in peripheral blood and may vary among individuals. We examined variety among selected NK cell receptors expressed by NK cells from normal donors, as well as the distribution of select NK cell subsets and NK cell receptor expression over time in several individual donors. Peripheral blood mononuclear cells were evaluated using flow cytometry via fluorochrome-conjugated antibodies against a number of NK cell receptors. Results were analyzed for both mean fluorescence intensity (MFI) and the percent positive cells for each receptor. CD56bright and CD56dim NK cell subsets were also considered separately, as was variation in receptor expression in NK cell subsets over time in selected individuals. Through this effort, we provide ranges of NK cell surface receptor expression for a local adult population as well as provide insight into intra-individual variation.
Appendix
Available only for authorised users
Literature
1.
go back to reference Shearer WT, Rosenblatt HM, Gelman RS, Oyomopito R, Plaeger S, Stiehm ER, Wara DW, Douglas SD, Luzuriaga K, McFarland EJ, et al. Lymphocyte subsets in healthy children from birth through 18 years of age: the Pediatric AIDS Clinical Trials Group P1009 study. J Allergy Clin Immunol. 2003;112:973–80.CrossRefPubMed Shearer WT, Rosenblatt HM, Gelman RS, Oyomopito R, Plaeger S, Stiehm ER, Wara DW, Douglas SD, Luzuriaga K, McFarland EJ, et al. Lymphocyte subsets in healthy children from birth through 18 years of age: the Pediatric AIDS Clinical Trials Group P1009 study. J Allergy Clin Immunol. 2003;112:973–80.CrossRefPubMed
2.
go back to reference Al-Herz W, Bousfiha A, Casanova JL, Chatila T, Conley ME, Cunningham-Rundles C, Etzioni A, Franco JL, Gaspar HB, Holland SM, et al. Primary immunodeficiency diseases: an update on the classification from the international union of immunological societies expert committee for primary immunodeficiency. Front Immunol. 2014;5:162.PubMedCentralPubMed Al-Herz W, Bousfiha A, Casanova JL, Chatila T, Conley ME, Cunningham-Rundles C, Etzioni A, Franco JL, Gaspar HB, Holland SM, et al. Primary immunodeficiency diseases: an update on the classification from the international union of immunological societies expert committee for primary immunodeficiency. Front Immunol. 2014;5:162.PubMedCentralPubMed
4.
go back to reference Mace EM, Hsu AP, Monaco-Shawver L, Makedonas G, Rosen JB, Dropulic L, Cohen JI, Frenkel EP, Bagwell JC, Sullivan JL, et al. Mutations in GATA2 cause human NK cell deficiency with specific loss of the CD56(bright) subset. Blood. 2013;121:2669–77.PubMedCentralCrossRefPubMed Mace EM, Hsu AP, Monaco-Shawver L, Makedonas G, Rosen JB, Dropulic L, Cohen JI, Frenkel EP, Bagwell JC, Sullivan JL, et al. Mutations in GATA2 cause human NK cell deficiency with specific loss of the CD56(bright) subset. Blood. 2013;121:2669–77.PubMedCentralCrossRefPubMed
5.
6.
go back to reference Yu J, Freud AG, Caligiuri MA. Location and cellular stages of natural killer cell development. Trends Immunol. 2013;34:573–82.CrossRefPubMed Yu J, Freud AG, Caligiuri MA. Location and cellular stages of natural killer cell development. Trends Immunol. 2013;34:573–82.CrossRefPubMed
7.
go back to reference Thielens A, Vivier E, Romagne F. NK cell MHC class I specific receptors (KIR): from biology to clinical intervention. Curr Opin Immunol. 2012;24:239–45.CrossRefPubMed Thielens A, Vivier E, Romagne F. NK cell MHC class I specific receptors (KIR): from biology to clinical intervention. Curr Opin Immunol. 2012;24:239–45.CrossRefPubMed
9.
go back to reference Marras F, Bozzano F, Ascierto ML, De Maria A. Baseline and dynamic expression of activating NK cell receptors in the control of chronic viral infections: the paradigm of HIV-1 and HCV. Front Immunol. 2014;5:305.PubMedCentralCrossRefPubMed Marras F, Bozzano F, Ascierto ML, De Maria A. Baseline and dynamic expression of activating NK cell receptors in the control of chronic viral infections: the paradigm of HIV-1 and HCV. Front Immunol. 2014;5:305.PubMedCentralCrossRefPubMed
10.
go back to reference Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22:633–40.CrossRefPubMed Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol. 2001;22:633–40.CrossRefPubMed
11.
go back to reference Nagler A, Lanier LL, Cwirla S, Phillips JH. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol. 1989;143:3183–91.PubMed Nagler A, Lanier LL, Cwirla S, Phillips JH. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol. 1989;143:3183–91.PubMed
12.
go back to reference Morice WG. The immunophenotypic attributes of NK cells and NK-cell lineage lymphoproliferative disorders. Am J Clin Pathol. 2007;127:881–6.CrossRefPubMed Morice WG. The immunophenotypic attributes of NK cells and NK-cell lineage lymphoproliferative disorders. Am J Clin Pathol. 2007;127:881–6.CrossRefPubMed
13.
go back to reference Beziat V, Duffy D, Quoc SN, Le Garff-Tavernier M, Decocq J, Combadiere B, Debre P, Vieillard V. CD56bright, CD16+ NK cells: a functional intermediate stage of NK cell differentiation. J Immunol. 2011;186:6753–61.CrossRefPubMed Beziat V, Duffy D, Quoc SN, Le Garff-Tavernier M, Decocq J, Combadiere B, Debre P, Vieillard V. CD56bright, CD16+ NK cells: a functional intermediate stage of NK cell differentiation. J Immunol. 2011;186:6753–61.CrossRefPubMed
14.
go back to reference Sabry M, Tsirogianni M, Bakhsh IA, North J, Sivakumaran J, Giannopoulos K, Anderson R, Mackinnon S, Lowdell MW. Leukemic priming of resting NK cells is killer Ig-like receptor independent but requires CD15-mediated CD2 ligation and natural cytotoxicity receptors. J Immunol. 2011;187:6227–34.CrossRefPubMed Sabry M, Tsirogianni M, Bakhsh IA, North J, Sivakumaran J, Giannopoulos K, Anderson R, Mackinnon S, Lowdell MW. Leukemic priming of resting NK cells is killer Ig-like receptor independent but requires CD15-mediated CD2 ligation and natural cytotoxicity receptors. J Immunol. 2011;187:6227–34.CrossRefPubMed
15.
go back to reference Nabekura T, Kanaya M, Shibuya A, Fu G, Gascoigne NR, Lanier LL. Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection. Immunity. 2014;40:225–34.PubMedCentralCrossRefPubMed Nabekura T, Kanaya M, Shibuya A, Fu G, Gascoigne NR, Lanier LL. Costimulatory molecule DNAM-1 is essential for optimal differentiation of memory natural killer cells during mouse cytomegalovirus infection. Immunity. 2014;40:225–34.PubMedCentralCrossRefPubMed
16.
go back to reference Yu J, Mao HC, Wei M, Hughes T, Zhang J, Park IK, Liu S, McClory S, Marcucci G, Trotta R, et al. CD94 surface density identifies a functional intermediary between the CD56bright and CD56dim human NK-cell subsets. Blood. 2010;115:274–81.PubMedCentralCrossRefPubMed Yu J, Mao HC, Wei M, Hughes T, Zhang J, Park IK, Liu S, McClory S, Marcucci G, Trotta R, et al. CD94 surface density identifies a functional intermediary between the CD56bright and CD56dim human NK-cell subsets. Blood. 2010;115:274–81.PubMedCentralCrossRefPubMed
17.
go back to reference Li Y, Mariuzza RA. Structural basis for recognition of cellular and viral ligands by NK cell receptors. Front Immunol. 2014;5:123.PubMedCentralPubMed Li Y, Mariuzza RA. Structural basis for recognition of cellular and viral ligands by NK cell receptors. Front Immunol. 2014;5:123.PubMedCentralPubMed
18.
go back to reference Henney CS, Kuribayashi K, Kern DE, Gillis S. Interleukin-2 augments natural killer cell activity. Nature. 1981;291:335–8.CrossRefPubMed Henney CS, Kuribayashi K, Kern DE, Gillis S. Interleukin-2 augments natural killer cell activity. Nature. 1981;291:335–8.CrossRefPubMed
19.
go back to reference van Montfrans JM, Hoepelman AI, Otto S, van Gijn M, van de Corput L, de Weger RA, Monaco-Shawver L, Banerjee PP, Sanders EA, Jol-van der Zijde CM, et al. CD27 deficiency is associated with combined immunodeficiency and persistent symptomatic EBV viremia. J Allergy Clin Immunol. 2012;129(787–93):e786. van Montfrans JM, Hoepelman AI, Otto S, van Gijn M, van de Corput L, de Weger RA, Monaco-Shawver L, Banerjee PP, Sanders EA, Jol-van der Zijde CM, et al. CD27 deficiency is associated with combined immunodeficiency and persistent symptomatic EBV viremia. J Allergy Clin Immunol. 2012;129(787–93):e786.
20.
go back to reference Pradier A, Tabone-Eglinger S, Huber V, Bosshard C, Rigal E, Wehrle-Haller B, Roosnek E. Peripheral blood CD56(bright) NK cells respond to stem cell factor and adhere to its membrane-bound form after upregulation of c-kit. Eur J Immunol. 2014;44:511–20.CrossRefPubMed Pradier A, Tabone-Eglinger S, Huber V, Bosshard C, Rigal E, Wehrle-Haller B, Roosnek E. Peripheral blood CD56(bright) NK cells respond to stem cell factor and adhere to its membrane-bound form after upregulation of c-kit. Eur J Immunol. 2014;44:511–20.CrossRefPubMed
21.
go back to reference Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, Norris PJ, Nixon DF, Lanier LL. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood. 2010;116:3865–74.PubMedCentralCrossRefPubMed Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, Norris PJ, Nixon DF, Lanier LL. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood. 2010;116:3865–74.PubMedCentralCrossRefPubMed
22.
go back to reference Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, York VA, Houchins JP, Miller S, Kang SM, Norris PJ, et al. Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA. 2011;108:14725–32.PubMedCentralCrossRefPubMed Lopez-Verges S, Milush JM, Schwartz BS, Pando MJ, Jarjoura J, York VA, Houchins JP, Miller S, Kang SM, Norris PJ, et al. Expansion of a unique CD57(+)NKG2Chi natural killer cell subset during acute human cytomegalovirus infection. Proc Natl Acad Sci USA. 2011;108:14725–32.PubMedCentralCrossRefPubMed
24.
go back to reference Millard AL, Valli PV, Stussi G, Mueller NJ, Yung GP, Seebach JD. Brief exercise increases peripheral blood NK Cell counts without immediate functional changes, but impairs their responses to ex vivo stimulation. Front Immunol. 2013;4:125.PubMedCentralCrossRefPubMed Millard AL, Valli PV, Stussi G, Mueller NJ, Yung GP, Seebach JD. Brief exercise increases peripheral blood NK Cell counts without immediate functional changes, but impairs their responses to ex vivo stimulation. Front Immunol. 2013;4:125.PubMedCentralCrossRefPubMed
25.
go back to reference Gineau L, Cognet C, Kara N, Lach FP, Dunne J, Veturi U, Picard C, Trouillet C, Eidenschenk C, Aoufouchi S, et al. Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J Clin Investig. 2012;122:821–32.PubMedCentralCrossRefPubMed Gineau L, Cognet C, Kara N, Lach FP, Dunne J, Veturi U, Picard C, Trouillet C, Eidenschenk C, Aoufouchi S, et al. Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J Clin Investig. 2012;122:821–32.PubMedCentralCrossRefPubMed
26.
go back to reference Horowitz A, Strauss-Albee DM, Leipold M, Kubo J, Nemat-Gorgani N, Dogan OC, Dekker CL, Mackey S, Maecker H, Swan GE, et al. Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci Transl Med. 2013;5:208ra145.PubMedCentralCrossRefPubMed Horowitz A, Strauss-Albee DM, Leipold M, Kubo J, Nemat-Gorgani N, Dogan OC, Dekker CL, Mackey S, Maecker H, Swan GE, et al. Genetic and environmental determinants of human NK cell diversity revealed by mass cytometry. Sci Transl Med. 2013;5:208ra145.PubMedCentralCrossRefPubMed
27.
go back to reference Shaw RK, Issekutz AC, Fraser R, Schmit P, Morash B, Monaco-Shawver L, Orange JS, Fernandez CV. Bilateral adrenal EBV-associated smooth muscle tumors in a child with a natural killer cell deficiency. Blood. 2012;119:4009–12.PubMedCentralCrossRefPubMed Shaw RK, Issekutz AC, Fraser R, Schmit P, Morash B, Monaco-Shawver L, Orange JS, Fernandez CV. Bilateral adrenal EBV-associated smooth muscle tumors in a child with a natural killer cell deficiency. Blood. 2012;119:4009–12.PubMedCentralCrossRefPubMed
28.
go back to reference Grier JT, Forbes LR, Monaco-Shawver L, Oshinsky J, Atkinson TP, Moody C, Pandey R, Campbell KS, Orange JS. Human immunodeficiency-causing mutation defines CD16 in spontaneous NK cell cytotoxicity. J Clin Investig. 2012;122:3769–80.PubMedCentralCrossRefPubMed Grier JT, Forbes LR, Monaco-Shawver L, Oshinsky J, Atkinson TP, Moody C, Pandey R, Campbell KS, Orange JS. Human immunodeficiency-causing mutation defines CD16 in spontaneous NK cell cytotoxicity. J Clin Investig. 2012;122:3769–80.PubMedCentralCrossRefPubMed
29.
go back to reference Risma KA, Frayer RW, Filipovich AH, Sumegi J. Aberrant maturation of mutant perforin underlies the clinical diversity of hemophagocytic lymphohistiocytosis. J Clin Investig. 2006;116:182–92.PubMedCentralCrossRefPubMed Risma KA, Frayer RW, Filipovich AH, Sumegi J. Aberrant maturation of mutant perforin underlies the clinical diversity of hemophagocytic lymphohistiocytosis. J Clin Investig. 2006;116:182–92.PubMedCentralCrossRefPubMed
30.
go back to reference Seed B, Aruffo A. Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc Natl Acad Sci USA. 1987;84:3365–9.PubMedCentralCrossRefPubMed Seed B, Aruffo A. Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc Natl Acad Sci USA. 1987;84:3365–9.PubMedCentralCrossRefPubMed
31.
go back to reference Sewell WA, Brown MH, Dunne J, Owen MJ, Crumpton MJ. Molecular cloning of the human T-lymphocyte surface CD2 (T11) antigen. Proc Natl Acad Sci USA. 1986;83:8718–22.PubMedCentralCrossRefPubMed Sewell WA, Brown MH, Dunne J, Owen MJ, Crumpton MJ. Molecular cloning of the human T-lymphocyte surface CD2 (T11) antigen. Proc Natl Acad Sci USA. 1986;83:8718–22.PubMedCentralCrossRefPubMed
33.
go back to reference Zheng X, Wang Y, Wei H, Sun R, Tian Z. LFA-1 and CD2 synergize for the Erk1/2 activation in the natural killer (NK) cell immunological synapse. J Biol Chem. 2009;284:21280–7.PubMedCentralCrossRefPubMed Zheng X, Wang Y, Wei H, Sun R, Tian Z. LFA-1 and CD2 synergize for the Erk1/2 activation in the natural killer (NK) cell immunological synapse. J Biol Chem. 2009;284:21280–7.PubMedCentralCrossRefPubMed
34.
go back to reference Nakayama K, Kawachi Y, Tokito S, Minami N, Yamamoto R, Imai T, Gachelin G, Nakauchi H. Recent duplication of the two human CD8 beta-chain genes. J Immunol. 1992;148:1919–27.PubMed Nakayama K, Kawachi Y, Tokito S, Minami N, Yamamoto R, Imai T, Gachelin G, Nakauchi H. Recent duplication of the two human CD8 beta-chain genes. J Immunol. 1992;148:1919–27.PubMed
35.
go back to reference Addison EG, North J, Bakhsh I, Marden C, Haq S, Al-Sarraj S, Malayeri R, Wickremasinghe RG, Davies JK, Lowdell MW. Ligation of CD8alpha on human natural killer cells prevents activation-induced apoptosis and enhances cytolytic activity. Immunology. 2005;116:354–61.PubMedCentralCrossRefPubMed Addison EG, North J, Bakhsh I, Marden C, Haq S, Al-Sarraj S, Malayeri R, Wickremasinghe RG, Davies JK, Lowdell MW. Ligation of CD8alpha on human natural killer cells prevents activation-induced apoptosis and enhances cytolytic activity. Immunology. 2005;116:354–61.PubMedCentralCrossRefPubMed
36.
go back to reference Rodriguez AR, Arulanandam BP, Hodara VL, McClure HM, Cobb EK, Salas MT, White R, Murthy KK. Influence of interleukin-15 on CD8+ natural killer cells in human immunodeficiency virus type 1-infected chimpanzees. J Gen Virol. 2007;88(Pt 2):641–51.CrossRefPubMed Rodriguez AR, Arulanandam BP, Hodara VL, McClure HM, Cobb EK, Salas MT, White R, Murthy KK. Influence of interleukin-15 on CD8+ natural killer cells in human immunodeficiency virus type 1-infected chimpanzees. J Gen Virol. 2007;88(Pt 2):641–51.CrossRefPubMed
37.
go back to reference Corbi AL, Larson RS, Kishimoto TK, Springer TA, Morton CC. Chromosomal location of the genes encoding the leukocyte adhesion receptors LFA-1, Mac-1 and p150,95. Identification of a gene cluster involved in cell adhesion. J Exp Med. 1988;167:1597–607.CrossRefPubMed Corbi AL, Larson RS, Kishimoto TK, Springer TA, Morton CC. Chromosomal location of the genes encoding the leukocyte adhesion receptors LFA-1, Mac-1 and p150,95. Identification of a gene cluster involved in cell adhesion. J Exp Med. 1988;167:1597–607.CrossRefPubMed
38.
go back to reference Wang H, Zheng X, Wei H, Tian Z, Sun R. Important role for NKp30 in synapse formation and activation of NK cells. Immunol Invest. 2012;41:367–81.CrossRefPubMed Wang H, Zheng X, Wei H, Tian Z, Sun R. Important role for NKp30 in synapse formation and activation of NK cells. Immunol Invest. 2012;41:367–81.CrossRefPubMed
39.
go back to reference Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med. 2005;202:1001–12.PubMedCentralCrossRefPubMed Bryceson YT, March ME, Barber DF, Ljunggren HG, Long EO. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J Exp Med. 2005;202:1001–12.PubMedCentralCrossRefPubMed
40.
go back to reference Sadhu C, Harris EA, Staunton DE. Enhancement of natural killer cell cytotoxicity by a CD18 integrin-activating antibody. Biochemi Biophys Res Commun. 2007;358:938–41.CrossRef Sadhu C, Harris EA, Staunton DE. Enhancement of natural killer cell cytotoxicity by a CD18 integrin-activating antibody. Biochemi Biophys Res Commun. 2007;358:938–41.CrossRef
41.
go back to reference Corbi AL, Kishimoto TK, Miller LJ, Springer TA. The human leukocyte adhesion glycoprotein Mac-1 (complement receptor type 3, CD11b) alpha subunit. Cloning, primary structure, and relation to the integrins, von Willebrand factor and factor B. J Biol Chem. 1988;263:12403–11.PubMed Corbi AL, Kishimoto TK, Miller LJ, Springer TA. The human leukocyte adhesion glycoprotein Mac-1 (complement receptor type 3, CD11b) alpha subunit. Cloning, primary structure, and relation to the integrins, von Willebrand factor and factor B. J Biol Chem. 1988;263:12403–11.PubMed
42.
go back to reference Arnaout MA, Remold-O’Donnell E, Pierce MW, Harris P, Tenen DG. Molecular cloning of the alpha subunit of human and guinea pig leukocyte adhesion glycoprotein Mo1: chromosomal localization and homology to the alpha subunits of integrins. Proc Natl Acad Sci USA. 1988;85:2776–80.PubMedCentralCrossRefPubMed Arnaout MA, Remold-O’Donnell E, Pierce MW, Harris P, Tenen DG. Molecular cloning of the alpha subunit of human and guinea pig leukocyte adhesion glycoprotein Mo1: chromosomal localization and homology to the alpha subunits of integrins. Proc Natl Acad Sci USA. 1988;85:2776–80.PubMedCentralCrossRefPubMed
43.
go back to reference Orange JS, Chehimi J, Ghavimi D, Campbell D, Sullivan KE. Decreased natural killer (NK) cell function in chronic NK cell lymphocytosis associated with decreased surface expression of CD11b. Clin Immunol. 2001;99:53–64.CrossRefPubMed Orange JS, Chehimi J, Ghavimi D, Campbell D, Sullivan KE. Decreased natural killer (NK) cell function in chronic NK cell lymphocytosis associated with decreased surface expression of CD11b. Clin Immunol. 2001;99:53–64.CrossRefPubMed
44.
go back to reference Arnaout MA, Gupta SK, Pierce MW, Tenen DG. Amino acid sequence of the alpha subunit of human leukocyte adhesion receptor Mo1 (complement receptor type 3). J Cell Biol. 1988;106:2153–8.CrossRefPubMed Arnaout MA, Gupta SK, Pierce MW, Tenen DG. Amino acid sequence of the alpha subunit of human leukocyte adhesion receptor Mo1 (complement receptor type 3). J Cell Biol. 1988;106:2153–8.CrossRefPubMed
45.
go back to reference Ornstein BW, Hill EB, Geurs TL, French AR. Natural killer cell functional defects in pediatric patients with severe and recurrent herpesvirus infections. J Infect Dis. 2013;207:458–68.PubMedCentralCrossRefPubMed Ornstein BW, Hill EB, Geurs TL, French AR. Natural killer cell functional defects in pediatric patients with severe and recurrent herpesvirus infections. J Infect Dis. 2013;207:458–68.PubMedCentralCrossRefPubMed
46.
go back to reference Ravetch JV, Perussia B. Alternative membrane forms of Fc gamma RIII(CD16) on human natural killer cells and neutrophils. Cell type-specific expression of two genes that differ in single nucleotide substitutions. J Exp Med. 1989;170:481–97.CrossRefPubMed Ravetch JV, Perussia B. Alternative membrane forms of Fc gamma RIII(CD16) on human natural killer cells and neutrophils. Cell type-specific expression of two genes that differ in single nucleotide substitutions. J Exp Med. 1989;170:481–97.CrossRefPubMed
47.
go back to reference Qiu WQ, de Bruin D, Brownstein BH, Pearse R, Ravetch JV. Organization of the human and mouse low-affinity Fc gamma R genes: duplication and recombination. Science. 1990;248:732–5.CrossRefPubMed Qiu WQ, de Bruin D, Brownstein BH, Pearse R, Ravetch JV. Organization of the human and mouse low-affinity Fc gamma R genes: duplication and recombination. Science. 1990;248:732–5.CrossRefPubMed
48.
go back to reference Jawahar S, Moody C, Chan M, Finberg R, Geha R, Chatila T. Natural killer (NK) cell deficiency associated with an epitope-deficient Fc receptor type IIIA (CD16-II). Clin Exp Immunol. 1996;103:408–13.PubMedCentralCrossRefPubMed Jawahar S, Moody C, Chan M, Finberg R, Geha R, Chatila T. Natural killer (NK) cell deficiency associated with an epitope-deficient Fc receptor type IIIA (CD16-II). Clin Exp Immunol. 1996;103:408–13.PubMedCentralCrossRefPubMed
49.
go back to reference Mandelboim O, Malik P, Davis DM, Jo CH, Boyson JE, Strominger JL. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc Natl Acad Sci USA. 1999;96:5640–4.PubMedCentralCrossRefPubMed Mandelboim O, Malik P, Davis DM, Jo CH, Boyson JE, Strominger JL. Human CD16 as a lysis receptor mediating direct natural killer cell cytotoxicity. Proc Natl Acad Sci USA. 1999;96:5640–4.PubMedCentralCrossRefPubMed
50.
go back to reference Axberg I, Ramstedt U, Patarroyo M, Beatty P, Wigzell H. Inhibition of natural killer cell cytotoxicity by a monoclonal antibody directed against adhesion-mediating protein gp 90 (CD18). Scand J Immunol. 1987;26:547–54.CrossRefPubMed Axberg I, Ramstedt U, Patarroyo M, Beatty P, Wigzell H. Inhibition of natural killer cell cytotoxicity by a monoclonal antibody directed against adhesion-mediating protein gp 90 (CD18). Scand J Immunol. 1987;26:547–54.CrossRefPubMed
51.
go back to reference Liu JH, Wei S, Blanchard DK, Djeu JY. Restoration of lytic function in a human natural killer cell line by gene transfection. Cell Immunol. 1994;156:24–35.CrossRefPubMed Liu JH, Wei S, Blanchard DK, Djeu JY. Restoration of lytic function in a human natural killer cell line by gene transfection. Cell Immunol. 1994;156:24–35.CrossRefPubMed
52.
go back to reference Timonen T, Patarroyo M, Gahmberg CG. CD11a-c/CD18 and GP84 (LB-2) adhesion molecules on human large granular lymphocytes and their participation in natural killing. J Immunol. 1988;141:1041–6.PubMed Timonen T, Patarroyo M, Gahmberg CG. CD11a-c/CD18 and GP84 (LB-2) adhesion molecules on human large granular lymphocytes and their participation in natural killing. J Immunol. 1988;141:1041–6.PubMed
53.
go back to reference Bigler RD, Bushkin Y, Chiorazzi N. S152 (CD27). A modulating disulfide-linked T cell activation antigen. J Immunol. 1988;141:21–8.PubMed Bigler RD, Bushkin Y, Chiorazzi N. S152 (CD27). A modulating disulfide-linked T cell activation antigen. J Immunol. 1988;141:21–8.PubMed
54.
go back to reference Vossen MT, Matmati M, Hertoghs KM, Baars PA, Gent MR, Leclercq G, Hamann J, Kuijpers TW, van Lier RA. CD27 defines phenotypically and functionally different human NK cell subsets. J Immunol. 2008;180:3739–45.CrossRefPubMed Vossen MT, Matmati M, Hertoghs KM, Baars PA, Gent MR, Leclercq G, Hamann J, Kuijpers TW, van Lier RA. CD27 defines phenotypically and functionally different human NK cell subsets. J Immunol. 2008;180:3739–45.CrossRefPubMed
56.
go back to reference Mitsumoto Y, Oka S, Sakuma H, Inazawa J, Kawasaki T. Cloning and chromosomal mapping of human glucuronyltransferase involved in biosynthesis of the HNK-1 carbohydrate epitope. Genomics. 2000;65:166–73.CrossRefPubMed Mitsumoto Y, Oka S, Sakuma H, Inazawa J, Kawasaki T. Cloning and chromosomal mapping of human glucuronyltransferase involved in biosynthesis of the HNK-1 carbohydrate epitope. Genomics. 2000;65:166–73.CrossRefPubMed
57.
go back to reference Yamamoto S, Oka S, Inoue M, Shimuta M, Manabe T, Takahashi H, Miyamoto M, Asano M, Sakagami J, Sudo K, et al. Mice deficient in nervous system-specific carbohydrate epitope HNK-1 exhibit impaired synaptic plasticity and spatial learning. J Biol Chem. 2002;277:27227–31.CrossRefPubMed Yamamoto S, Oka S, Inoue M, Shimuta M, Manabe T, Takahashi H, Miyamoto M, Asano M, Sakagami J, Sudo K, et al. Mice deficient in nervous system-specific carbohydrate epitope HNK-1 exhibit impaired synaptic plasticity and spatial learning. J Biol Chem. 2002;277:27227–31.CrossRefPubMed
58.
go back to reference Chang C, Rodriguez A, Carretero M, Lopez-Botet M, Phillips JH, Lanier LL. Molecular characterization of human CD94: a type II membrane glycoprotein related to the C-type lectin superfamily. Eur J Immunol. 1995;25:2433–7.CrossRefPubMed Chang C, Rodriguez A, Carretero M, Lopez-Botet M, Phillips JH, Lanier LL. Molecular characterization of human CD94: a type II membrane glycoprotein related to the C-type lectin superfamily. Eur J Immunol. 1995;25:2433–7.CrossRefPubMed
59.
go back to reference Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J Exp Med. 1998;187:813–8.PubMedCentralCrossRefPubMed Borrego F, Ulbrecht M, Weiss EH, Coligan JE, Brooks AG. Recognition of human histocompatibility leukocyte antigen (HLA)-E complexed with HLA class I signal sequence-derived peptides by CD94/NKG2 confers protection from natural killer cell-mediated lysis. J Exp Med. 1998;187:813–8.PubMedCentralCrossRefPubMed
60.
go back to reference Braud VM, Allan DS, O’Callaghan CA, Soderstrom K, D’Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998;391:795–9.CrossRefPubMed Braud VM, Allan DS, O’Callaghan CA, Soderstrom K, D’Andrea A, Ogg GS, Lazetic S, Young NT, Bell JI, Phillips JH, et al. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature. 1998;391:795–9.CrossRefPubMed
61.
go back to reference Lee N, Llano M, Carretero M, Ishitani A, Navarro F, Lopez-Botet M, Geraghty DE. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci USA. 1998;95:5199–204.PubMedCentralCrossRefPubMed Lee N, Llano M, Carretero M, Ishitani A, Navarro F, Lopez-Botet M, Geraghty DE. HLA-E is a major ligand for the natural killer inhibitory receptor CD94/NKG2A. Proc Natl Acad Sci USA. 1998;95:5199–204.PubMedCentralCrossRefPubMed
62.
go back to reference Vandenbark GR, deCastro CM, Taylor H, Dew-Knight S, Kaufman RE. Cloning and structural analysis of the human c-kit gene. Oncogene. 1992;7:1259–66.PubMed Vandenbark GR, deCastro CM, Taylor H, Dew-Knight S, Kaufman RE. Cloning and structural analysis of the human c-kit gene. Oncogene. 1992;7:1259–66.PubMed
63.
go back to reference Matos ME, Schnier GS, Beecher MS, Ashman LK, William DE, Caligiuri MA. Expression of a functional c-kit receptor on a subset of natural killer cells. J Exp Med. 1993;178:1079–84.CrossRefPubMed Matos ME, Schnier GS, Beecher MS, Ashman LK, William DE, Caligiuri MA. Expression of a functional c-kit receptor on a subset of natural killer cells. J Exp Med. 1993;178:1079–84.CrossRefPubMed
64.
go back to reference Carson WE, Haldar S, Baiocchi RA, Croce CM, Caligiuri MA. The c-kit ligand suppresses apoptosis of human natural killer cells through the upregulation of bcl-2. Proc Natl Acad Sci USA. 1994;91:7553–7.PubMedCentralCrossRefPubMed Carson WE, Haldar S, Baiocchi RA, Croce CM, Caligiuri MA. The c-kit ligand suppresses apoptosis of human natural killer cells through the upregulation of bcl-2. Proc Natl Acad Sci USA. 1994;91:7553–7.PubMedCentralCrossRefPubMed
65.
go back to reference Carson WE, Fehniger TA, Caligiuri MA. CD56bright natural killer cell subsets: characterization of distinct functional responses to interleukin-2 and the c-kit ligand. Eur J Immunol. 1997;27:354–60.CrossRefPubMed Carson WE, Fehniger TA, Caligiuri MA. CD56bright natural killer cell subsets: characterization of distinct functional responses to interleukin-2 and the c-kit ligand. Eur J Immunol. 1997;27:354–60.CrossRefPubMed
66.
go back to reference Benson DM Jr, Yu J, Becknell B, Wei M, Freud AG, Ferketich AK, Trotta R, Perrotti D, Briesewitz R, Caligiuri MA. Stem cell factor and interleukin-2/15 combine to enhance MAPK-mediated proliferation of human natural killer cells. Blood. 2009;113:2706–14.PubMedCentralCrossRefPubMed Benson DM Jr, Yu J, Becknell B, Wei M, Freud AG, Ferketich AK, Trotta R, Perrotti D, Briesewitz R, Caligiuri MA. Stem cell factor and interleukin-2/15 combine to enhance MAPK-mediated proliferation of human natural killer cells. Blood. 2009;113:2706–14.PubMedCentralCrossRefPubMed
67.
go back to reference Fehniger TA, Carson WE, Mrozek E, Caligiuri MA. Stem cell factor enhances interleukin-2-mediated expansion of murine natural killer cells in vivo. Blood. 1997;90:3647–53.PubMed Fehniger TA, Carson WE, Mrozek E, Caligiuri MA. Stem cell factor enhances interleukin-2-mediated expansion of murine natural killer cells in vivo. Blood. 1997;90:3647–53.PubMed
68.
go back to reference Di Santo JP, Rodewald HR. In vivo roles of receptor tyrosine kinases and cytokine receptors in early thymocyte development. Curr Opin Immunol. 1998;10:196–207.CrossRefPubMed Di Santo JP, Rodewald HR. In vivo roles of receptor tyrosine kinases and cytokine receptors in early thymocyte development. Curr Opin Immunol. 1998;10:196–207.CrossRefPubMed
69.
go back to reference Tsudo M, Kitamura F, Miyasaka M. Characterization of the interleukin 2 receptor beta chain using three distinct monoclonal antibodies. Proc Natl Acad Sci USA. 1989;86:1982–6.PubMedCentralCrossRefPubMed Tsudo M, Kitamura F, Miyasaka M. Characterization of the interleukin 2 receptor beta chain using three distinct monoclonal antibodies. Proc Natl Acad Sci USA. 1989;86:1982–6.PubMedCentralCrossRefPubMed
70.
go back to reference Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol. 2006;6:595–601.CrossRefPubMed Waldmann TA. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat Rev Immunol. 2006;6:595–601.CrossRefPubMed
71.
go back to reference Carson WE, Fehniger TA, Haldar S, Eckhert K, Lindemann MJ, Lai CF, Croce CM, Baumann H, Caligiuri MA. A potential role for interleukin-15 in the regulation of human natural killer cell survival. J Clin Investig. 1997;99:937–43.PubMedCentralCrossRefPubMed Carson WE, Fehniger TA, Haldar S, Eckhert K, Lindemann MJ, Lai CF, Croce CM, Baumann H, Caligiuri MA. A potential role for interleukin-15 in the regulation of human natural killer cell survival. J Clin Investig. 1997;99:937–43.PubMedCentralCrossRefPubMed
72.
go back to reference Colonna M, Samaridis J. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science. 1995;268:405–8.CrossRefPubMed Colonna M, Samaridis J. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science. 1995;268:405–8.CrossRefPubMed
73.
go back to reference Wagtmann N, Biassoni R, Cantoni C, Verdiani S, Malnati MS, Vitale M, Bottino C, Moretta L, Moretta A, Long EO. Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. Immunity. 1995;2:439–49.CrossRefPubMed Wagtmann N, Biassoni R, Cantoni C, Verdiani S, Malnati MS, Vitale M, Bottino C, Moretta L, Moretta A, Long EO. Molecular clones of the p58 NK cell receptor reveal immunoglobulin-related molecules with diversity in both the extra- and intracellular domains. Immunity. 1995;2:439–49.CrossRefPubMed
74.
go back to reference D’Andrea A, Chang C, Franz-Bacon K, McClanahan T, Phillips JH, Lanier LL. Molecular cloning of NKB1. A natural killer cell receptor for HLA-B allotypes. J Immunol. 1995;155:2306–10.PubMed D’Andrea A, Chang C, Franz-Bacon K, McClanahan T, Phillips JH, Lanier LL. Molecular cloning of NKB1. A natural killer cell receptor for HLA-B allotypes. J Immunol. 1995;155:2306–10.PubMed
75.
go back to reference Pende D, Biassoni R, Cantoni C, Verdiani S, Falco M, di Donato C, Accame L, Bottino C, Moretta A, Moretta L. The natural killer cell receptor specific for HLA-A allotypes: a novel member of the p58/p70 family of inhibitory receptors that is characterized by three immunoglobulin-like domains and is expressed as a 140-kD disulphide-linked dimer. J Exp Med. 1996;184:505–18.CrossRefPubMed Pende D, Biassoni R, Cantoni C, Verdiani S, Falco M, di Donato C, Accame L, Bottino C, Moretta A, Moretta L. The natural killer cell receptor specific for HLA-A allotypes: a novel member of the p58/p70 family of inhibitory receptors that is characterized by three immunoglobulin-like domains and is expressed as a 140-kD disulphide-linked dimer. J Exp Med. 1996;184:505–18.CrossRefPubMed
76.
go back to reference Shibuya A, Campbell D, Hannum C, Yssel H, Franz-Bacon K, McClanahan T, Kitamura T, Nicholl J, Sutherland GR, Lanier LL, et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity. 1996;4:573–81.CrossRefPubMed Shibuya A, Campbell D, Hannum C, Yssel H, Franz-Bacon K, McClanahan T, Kitamura T, Nicholl J, Sutherland GR, Lanier LL, et al. DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity. 1996;4:573–81.CrossRefPubMed
77.
go back to reference Shibuya K, Lanier LL, Phillips JH, Ochs HD, Shimizu K, Nakayama E, Nakauchi H, Shibuya A. Physical and functional association of LFA-1 with DNAM-1 adhesion molecule. Immunity. 1999;11:615–23.CrossRefPubMed Shibuya K, Lanier LL, Phillips JH, Ochs HD, Shimizu K, Nakayama E, Nakauchi H, Shibuya A. Physical and functional association of LFA-1 with DNAM-1 adhesion molecule. Immunity. 1999;11:615–23.CrossRefPubMed
78.
go back to reference Bottino C, Castriconi R, Pende D, Rivera P, Nanni M, Carnemolla B, Cantoni C, Grassi J, Marcenaro S, Reymond N, et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med. 2003;198:557–67.PubMedCentralCrossRefPubMed Bottino C, Castriconi R, Pende D, Rivera P, Nanni M, Carnemolla B, Cantoni C, Grassi J, Marcenaro S, Reymond N, et al. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J Exp Med. 2003;198:557–67.PubMedCentralCrossRefPubMed
79.
go back to reference Iguchi-Manaka A, Kai H, Yamashita Y, Shibata K, Tahara-Hanaoka S, Honda S, Yasui T, Kikutani H, Shibuya K, Shibuya A. Accelerated tumor growth in mice deficient in DNAM-1 receptor. J Exp Med. 2008;205:2959–64.PubMedCentralCrossRefPubMed Iguchi-Manaka A, Kai H, Yamashita Y, Shibata K, Tahara-Hanaoka S, Honda S, Yasui T, Kikutani H, Shibuya K, Shibuya A. Accelerated tumor growth in mice deficient in DNAM-1 receptor. J Exp Med. 2008;205:2959–64.PubMedCentralCrossRefPubMed
80.
go back to reference Chan CJ, Andrews DM, McLaughlin NM, Yagita H, Gilfillan S, Colonna M, Smyth MJ. DNAM-1/CD155 interactions promote cytokine and NK cell-mediated suppression of poorly immunogenic melanoma metastases. J Immunol. 2010;184:902–11.CrossRefPubMed Chan CJ, Andrews DM, McLaughlin NM, Yagita H, Gilfillan S, Colonna M, Smyth MJ. DNAM-1/CD155 interactions promote cytokine and NK cell-mediated suppression of poorly immunogenic melanoma metastases. J Immunol. 2010;184:902–11.CrossRefPubMed
81.
go back to reference Pende D, Castriconi R, Romagnani P, Spaggiari GM, Marcenaro S, Dondero A, Lazzeri E, Lasagni L, Martini S, Rivera P, et al. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood. 2006;107:2030–6.CrossRefPubMed Pende D, Castriconi R, Romagnani P, Spaggiari GM, Marcenaro S, Dondero A, Lazzeri E, Lasagni L, Martini S, Rivera P, et al. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood. 2006;107:2030–6.CrossRefPubMed
82.
go back to reference Hou S, Ge K, Zheng X, Wei H, Sun R, Tian Z. CD226 protein is involved in immune synapse formation and triggers natural killer (NK) cell activation via its first extracellular domain. J Biol Chem. 2014;289:6969–77.PubMedCentralCrossRefPubMed Hou S, Ge K, Zheng X, Wei H, Sun R, Tian Z. CD226 protein is involved in immune synapse formation and triggers natural killer (NK) cell activation via its first extracellular domain. J Biol Chem. 2014;289:6969–77.PubMedCentralCrossRefPubMed
83.
go back to reference Hou S, Zheng X, Wei H, Tian Z, Sun R. Recombinant soluble CD226 protein directly inhibits cancer cell proliferation in vitro. Int Immunopharmacol. 2014;19:119–26.CrossRefPubMed Hou S, Zheng X, Wei H, Tian Z, Sun R. Recombinant soluble CD226 protein directly inhibits cancer cell proliferation in vitro. Int Immunopharmacol. 2014;19:119–26.CrossRefPubMed
84.
go back to reference Boles KS, Nakajima H, Colonna M, Chuang SS, Stepp SE, Bennett M, Kumar V, Mathew PA. Molecular characterization of a novel human natural killer cell receptor homologous to mouse 2B4. Tissue Antigens. 1999;54:27–34.CrossRefPubMed Boles KS, Nakajima H, Colonna M, Chuang SS, Stepp SE, Bennett M, Kumar V, Mathew PA. Molecular characterization of a novel human natural killer cell receptor homologous to mouse 2B4. Tissue Antigens. 1999;54:27–34.CrossRefPubMed
85.
go back to reference Brown MH, Boles K, van der Merwe PA, Kumar V, Mathew PA, Barclay AN. 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J Exp Med. 1998;188:2083–90.PubMedCentralCrossRefPubMed Brown MH, Boles K, van der Merwe PA, Kumar V, Mathew PA, Barclay AN. 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J Exp Med. 1998;188:2083–90.PubMedCentralCrossRefPubMed
86.
go back to reference Bryceson YT, March ME, Ljunggren HG, Long EO. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood. 2006;107:159–66.PubMedCentralCrossRefPubMed Bryceson YT, March ME, Ljunggren HG, Long EO. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood. 2006;107:159–66.PubMedCentralCrossRefPubMed
87.
go back to reference Houchins JP, Yabe T, McSherry C, Bach FH. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. J Exp Med. 1991;173:1017–20.CrossRefPubMed Houchins JP, Yabe T, McSherry C, Bach FH. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. J Exp Med. 1991;173:1017–20.CrossRefPubMed
88.
go back to reference Yabe T, McSherry C, Bach FH, Fisch P, Schall RP, Sondel PM, Houchins JP. A multigene family on human chromosome 12 encodes natural killer-cell lectins. Immunogenetics. 1993;37:455–60.CrossRefPubMed Yabe T, McSherry C, Bach FH, Fisch P, Schall RP, Sondel PM, Houchins JP. A multigene family on human chromosome 12 encodes natural killer-cell lectins. Immunogenetics. 1993;37:455–60.CrossRefPubMed
89.
go back to reference Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285:727–9.CrossRefPubMed Bauer S, Groh V, Wu J, Steinle A, Phillips JH, Lanier LL, Spies T. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science. 1999;285:727–9.CrossRefPubMed
90.
92.
go back to reference Lopez-Soto A, Huergo-Zapico L, Acebes-Huerta A, Villa-Alvarez M, Gonzalez S. NKG2D signaling in cancer immunosurveillance. Int J Cancer. 2015;136:1741–50.CrossRefPubMed Lopez-Soto A, Huergo-Zapico L, Acebes-Huerta A, Villa-Alvarez M, Gonzalez S. NKG2D signaling in cancer immunosurveillance. Int J Cancer. 2015;136:1741–50.CrossRefPubMed
93.
go back to reference Pessino A, Sivori S, Bottino C, Malaspina A, Morelli L, Moretta L, Biassoni R, Moretta A. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med. 1998;188:953–60.PubMedCentralCrossRefPubMed Pessino A, Sivori S, Bottino C, Malaspina A, Morelli L, Moretta L, Biassoni R, Moretta A. Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J Exp Med. 1998;188:953–60.PubMedCentralCrossRefPubMed
94.
go back to reference Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, Hanna J, Qimron U, Landau G, Greenbaum E, et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol. 2006;7:517–23.CrossRefPubMed Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, Hanna J, Qimron U, Landau G, Greenbaum E, et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol. 2006;7:517–23.CrossRefPubMed
95.
go back to reference Hudspeth K, Silva-Santos B, Mavilio D. Natural cytotoxicity receptors: broader expression patterns and functions in innate and adaptive immune cells. Front Immunol. 2013;4:69.PubMedCentralCrossRefPubMed Hudspeth K, Silva-Santos B, Mavilio D. Natural cytotoxicity receptors: broader expression patterns and functions in innate and adaptive immune cells. Front Immunol. 2013;4:69.PubMedCentralCrossRefPubMed
96.
go back to reference Thoren FB, Riise RE, Ousback J, Della Chiesa M, Alsterholm M, Marcenaro E, Pesce S, Prato C, Cantoni C, Bylund J, et al. Human NK Cells induce neutrophil apoptosis via an NKp46- and Fas-dependent mechanism. J Immunol. 2012;188:1668–74.CrossRefPubMed Thoren FB, Riise RE, Ousback J, Della Chiesa M, Alsterholm M, Marcenaro E, Pesce S, Prato C, Cantoni C, Bylund J, et al. Human NK Cells induce neutrophil apoptosis via an NKp46- and Fas-dependent mechanism. J Immunol. 2012;188:1668–74.CrossRefPubMed
97.
go back to reference Podack ER, Lowrey DM, Lichtenheld M, Olsen KJ, Aebischer T, Binder D, Rupp F, Hengartner H. Structure, function and expression of murine and human perforin 1 (P1). Immunol Rev. 1988;103:203–11.CrossRefPubMed Podack ER, Lowrey DM, Lichtenheld M, Olsen KJ, Aebischer T, Binder D, Rupp F, Hengartner H. Structure, function and expression of murine and human perforin 1 (P1). Immunol Rev. 1988;103:203–11.CrossRefPubMed
98.
go back to reference Shinkai Y, Takio K, Okumura K. Homology of perforin to the ninth component of complement (C9). Nature. 1988;334:525–7.CrossRefPubMed Shinkai Y, Takio K, Okumura K. Homology of perforin to the ninth component of complement (C9). Nature. 1988;334:525–7.CrossRefPubMed
99.
go back to reference Voskoboinik I, Trapani JA. Perforinopathy: a spectrum of human immune disease caused by defective perforin delivery or function. Front Immunol. 2013;4:441.PubMedCentralCrossRefPubMed Voskoboinik I, Trapani JA. Perforinopathy: a spectrum of human immune disease caused by defective perforin delivery or function. Front Immunol. 2013;4:441.PubMedCentralCrossRefPubMed
Metadata
Title
Practical NK cell phenotyping and variability in healthy adults
Authors
Laura S. Angelo
Pinaki P. Banerjee
Linda Monaco-Shawver
Joshua B. Rosen
George Makedonas
Lisa R. Forbes
Emily M. Mace
Jordan S. Orange
Publication date
01-07-2015
Publisher
Springer US
Published in
Immunologic Research / Issue 3/2015
Print ISSN: 0257-277X
Electronic ISSN: 1559-0755
DOI
https://doi.org/10.1007/s12026-015-8664-y

Other articles of this Issue 3/2015

Immunologic Research 3/2015 Go to the issue