The role of natural cytotoxicity receptors in various pathologies: Emphasis on Type I diabetes

Frontiers in Immunology

Volumn 5, Issue JAN, 2014, Pages

  Enk, Jonatan ^a   Mandelboim, Ofer ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

Beta cells; Diabetes; NCR; NK cells; NKp46

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR;

AUTOIMMUNE DISEASE; CYTOTOXICITY; GENE EXPRESSION; GLUCOSE HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; INFLAMMATION; INNATE IMMUNITY; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER CELL; NONHUMAN; SHORT SURVEY; SIGNAL TRANSDUCTION;

EID: 84897729389     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2014.00004     Document Type: Short Survey

References (79)

1. Herberman RB, Nunn ME, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic acid allogeneic tumors. I. Distribution of reactivity and specificity. Int J Cancer (1975) 16(2):216-29. doi:10.1002/ijc.2910160205.
2. Kiessling R, Klein E, Wigzell H. "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 (1975) 5(2):112-7. doi:10.1002/eji.1830050208.
3. Holmes KV, Welsh RM, Haspel MV. Natural cytotoxicity against mouse hepatitis virus-infected target cells. I. Correlation of cytotoxicity with virus binding to leukocytes. J Immunol (1986) 136(4):1446-53.
4. Vivier E, Raulet DH, Moretta A, Caligiuri MA, Zitvogel L, Lanier LL, et al. Innate or adaptive immunity? The example of natural killer cells. Science (2011) 331(6013):44-9. doi:10.1126/science.1198687.
5. Tian Z, Gershwin ME, Zhang C. Regulatory NK cells in autoimmune disease. J Autoimmun (2012) 39(3):206-15. doi:10.1016/j.jaut.2012.05.006.
6. Flodstrom M, Shi FD, Sarvetnick N, Ljunggren HG. The natural killer cell-friend or foe in autoimmune disease? Scand J Immunol (2002) 55(5):432-41. doi:10.1046/j.1365-3083.2002.01084.x.
7. Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol (2008) 9(5):503-10. doi:10.1038/ni1582.
8. Flodstrom-Tullberg M, Bryceson YT, Shi FD, Hoglund P, Ljunggren HG. Natural killer cells in human autoimmunity. Curr Opin Immunol (2009) 21(6):634-40. doi:10.1016/j.coi.2009.09.012.
9. Schleinitz N, Vely F, Harle JR, Vivier E. Natural killer cells in human autoimmune diseases. Immunology (2010) 131(4):451-8. doi:10.1111/j.1365-2567.2010.03360.x.
10. Johansson S, Berg L, Hall H, Hoglund P. NK cells: elusive players in autoimmunity. Trends Immunol (2005) 26(11):613-8. doi:10.1016/j.it.2005.08.008.
11. Fehniger TA, Cooper MA, Nuovo GJ, Cella M, Facchetti F, Colonna M, et al. CD56bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood (2003) 101(8):3052-7. doi:10.1182/blood-2002-09-2876.
12. Ebert LM, Meuter S, Moser B. Homing and function of human skin gammadelta T cells and NK cells: relevance for tumor surveillance. J Immunol (2006) 176(7):4331-6.
13. Robinson BW, Pinkston P, Crystal RG. Natural killer cells are present in the normal human lung but are functionally impotent. J Clin Invest (1984) 74(3):942-50. doi:10.1172/JCI111513.
14. Gregoire C, Chasson L, Luci C, Tomasello E, Geissmann F, Vivier E, et al. The trafficking of natural killer cells. Immunol Rev (2007) 220:169-82. doi:10.1111/j.1600-065X.2007.00563.x.
15. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, et al. Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med (2006) 12(9):1065-74. doi:10.1038/nm1452.
16. Ferlazzo G, Thomas D, Lin SL, Goodman K, Morandi B, Muller WA, et al. The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic. J Immunol (2004) 172(3):1455-62.
17. Cooper MA, Fehniger TA, Caligiuri MA. The biology of human natural killer-cell subsets. Trends Immunol (2001) 22(11):633-40. doi:10.1016/S1471-4906(01)02060-9.
18. Koopman LA, Kopcow HD, Rybalov B, Boyson JE, Orange JS, Schatz F, et al. Human decidual natural killer cells are a unique NK cell subset with immunomodulatory potential. J Exp Med (2003) 198(8):1201-12. doi:10.1084/jem.20030305.
19. Lopez-Verges S, Milush JM, Pandey S, York VA, Arakawa-Hoyt J, Pircher H, et al. CD57 defines a functionally distinct population of mature NK cells in the human CD56dimCD16+ NK-cell subset. Blood (2010) 116(19):3865-74. doi:10.1182/blood-2010-04-282301.
20. Romagnani C, Juelke K, Falco M, Morandi B, D'Agostino A, Costa R, et al. CD56brightCD16-killer Ig-like receptor NK cells display longer telomeres and acquire features of CD56dim NK cells upon activation. J Immunol (2007) 178(8):4947-55.
21. Juelke K, Killig M, Luetke-Eversloh M, Parente E, Gruen J, Morandi B, et al. CD62L expression identifies a unique subset of polyfunctional CD56dim NK cells. Blood (2010) 116(8):1299-307. doi:10.1182/blood-2009-11-253286.
22. Bjorkstrom NK, Riese P, Heuts F, Andersson S, Fauriat C, Ivarsson MA, et al. Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood (2010) 116(19):3853-64. doi:10.1182/blood-2010-04-281675.
23. De Maria A, Bozzano F, Cantoni C, Moretta L. Revisiting human natural killer cell subset function revealed cytolytic CD56(dim)CD16+ NK cells as rapid producers of abundant IFN-gamma on activation. Proc Natl Acad Sci U S A (2011) 108(2):728-32. doi:10.1073/pnas.1012356108.
24. Fauriat C, Long EO, Ljunggren HG, Bryceson YT. Regulation of human NK-cell cytokine and chemokine production by target cell recognition. Blood (2010) 115(11):2167-76. doi:10.1182/blood-2009-08-238469.
25. Paust S, von Andrian UH. Natural killer cell memory. Nat Immunol (2011) 12(6):500-8. doi:10.1038/ni.2032.
26. Campbell KS, Purdy AK. Structure/function of human killer cell immunoglobulin-like receptors: lessons from polymorphisms, evolution, crystal structures and mutations. Immunology (2011) 132(3):315-25. doi:10.1111/j.1365-2567.2010.03398.x.
27. Bryceson YT, Chiang SC, Darmanin S, Fauriat C, Schlums H, Theorell J, et al. Molecular mechanisms of natural killer cell activation. J Innate Immun (2011) 3(3):216-26. doi:10.1159/000325265.
28. Seidel E, Glasner A, Mandelboim O. Virus-mediated inhibition of natural cytotoxicity receptor recognition. Cell Mol Life Sci (2012) 69:3911-20. doi:10.1007/s00018-012-1001-x.
29. Shibuya A, Nakahashi-Oda C, Tahara-Hanaoka S. Regulation of immune responses by the activating and inhibitory myeloid-associate immunoglobulin-like receptors (MAIR) (CD300). Immune Netw (2009) 9(2):41-5. doi:10.4110/in.2009.9.2.41.
30. Stanietsky N, Simic H, Arapovic J, Toporik A, Levy O, Novik A, et al. The interaction of TIGIT with PVR and PVRL2 inhibits human NK cell cytotoxicity. Proc Natl Acad Sci U S A (2009) 106(42):17858-63. doi:10.1073/pnas.0903474106.
31. Orr MT, Lanier LL. Natural killer cell education and tolerance. Cell (2010) 142(6):847-56. doi:10.1016/j.cell.2010.08.031.
32. Watzl C, Long EO. Signal transduction during activation and inhibition of natural killer cells. Curr Protoc Immunol (2010) 11:119B. doi:10.1002/0471142735.im1109bs90.
33. Elliott JM, Yokoyama WM. Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol (2011) 32(8):364-72. doi:10.1016/j.it.2011.06.001.
34. Pende D, Parolini S, Pessino A, Sivori S, Augugliaro R, Morelli L, et al. Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J Exp Med (1999) 190(10):1505-16. doi:10.1084/jem.190.10.1505.
35. Vitale M, Bottino C, Sivori S, Sanseverino L, Castriconi R, Marcenaro E, et al. NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells, is involved in non-major histocompatibility complex-restricted tumor cell lysis. J Exp Med (1998) 187(12):2065-72. doi:10.1084/jem.187.12.2065.
36. Sivori S, Vitale M, Morelli L, Sanseverino L, Augugliaro R, Bottino C, et al. p46, a novel natural killer cell-specific surface molecule that mediates cell activation. J Exp Med (1997) 186(7):1129-36. doi:10.1084/jem.186.7.1129.
37. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol (2001) 19:197-223. doi:10.1146/annurev.immunol.19.1.197.
38. Brusilovsky M, Rosental B, Shemesh A, Appel MY, Porgador A. Human NK cell recognition of target cells in the prism of natural cytotoxicity receptors and their ligands. J Immunotoxicol (2012) 9(3):267-74. doi:10.3109/1547691X.2012.675366.
39. Joyce MG, Sun PD. The structural basis of ligand recognition by natural killer cell receptors. J Biomed Biotechnol (2011) 2011:203628. doi:10.1155/2011/203628.
40. Mandelboim O, Lieberman N, Lev M, Paul L, Arnon TI, Bushkin Y, et al. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature (2001) 409(6823):1055-60. doi:10.1038/35059110.
41. Chaushu S, Wilensky A, Gur C, Shapira L, Elboim M, Halftek G, et al. Direct recognition of Fusobacterium nucleatum by the NK cell natural cytotoxicity receptor NKp46 aggravates periodontal disease. PLoS Pathog (2012) 8(3):e1002601. doi:10.1371/journal.ppat.1002601.
42. Esin S, Batoni G, Counoupas C, Stringaro A, Brancatisano FL, Colone M, et al. Direct binding of human NK cell natural cytotoxicity receptor NKp44 to the surfaces of mycobacteria and other bacteria. Infect Immun (2008) 76(4):1719-27. doi:10.1128/IAI.00870-07.
43. Mavoungou E, Held J, Mewono L, Kremsner PGA. Duffy binding-like domain is involved in the NKp30-mediated recognition of Plasmodium falciparum-parasitized erythrocytes by natural killer cells. J Infect Dis (2007) 195(10):1521-31. doi:10.1086/515579.
44. Li SS, Kyei SK, Timm-McCann M, Ogbomo H, Jones GJ, Shi M, et al. The NK receptor NKp30 mediates direct fungal recognition and killing and is diminished in NK cells from HIV-infected patients. Cell Host Microbe (2013) 14(4):387-97. doi:10.1016/j.chom.2013.09.007.
45. Jarahian M, Fiedler M, Cohnen A, Djandji D, Hammerling GJ, Gati C, et al. Modulation of NKp30-and NKp46-mediated natural killer cell responses by poxviral hemagglutinin. PLoS Pathog (2011) 7(8):e1002195. doi:10.1371/journal.ppat.1002195.
46. Arnon TI, Achdout H, Levi O, Markel G, Saleh N, Katz G, et al. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat Immunol (2005) 6(5):515-23. doi:10.1038/ni1190.
47. Hecht ML, Rosental B, Horlacher T, Hershkovitz O, De Paz JL, Noti C, et al. Natural cytotoxicity receptors NKp30, NKp44 and NKp46 bind to different heparan sulfate/heparin sequences. J Proteome Res (2009) 8(2):712-20. doi:10.1021/pr800747c.
48. Brandt CS, Baratin M, Yi EC, Kennedy J, Gao Z, Fox B, et al. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J Exp Med (2009) 206(7):1495-503. doi:10.1084/jem.20090681.
49. Pogge von Strandmann E, Simhadri VR, von Tresckow B, Sasse S, Reiners KS, Hansen HP, et al. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity (2007) 27(6):965-74. doi:10.1016/j.immuni.2007.10.010.
50. Wehner R, Dietze K, Bachmann M, Schmitz M. The bidirectional crosstalk between human dendritic cells and natural killer cells. J Innate Immun (2011) 3(3):258-63. doi:10.1159/000323923.
51. Piccioli D, Sbrana S, Melandri E, Valiante NM. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J Exp Med (2002) 195(3):335-41. doi:10.1084/jem.20010934.
52. Walzer T, Dalod M, Vivier E, Zitvogel L. Natural killer cell-dendritic cell crosstalk in the initiation of immune responses. Expert Opin Biol Ther (2005) 5(Suppl 1):S49-59. doi:10.1517/14712598.5.1.S49.
53. Hayakawa Y, Screpanti V, Yagita H, Grandien A, Ljunggren HG, Smyth MJ, et al. NK cell TRAIL eliminates immature dendritic cells in vivo and limits dendritic cell vaccination efficacy. J Immunol (2004) 172(1):123-9.
54. Gazit R, Gruda R, Elboim M, Arnon TI, Katz G, Achdout H, et al. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat Immunol (2006) 7(5):517-23. doi:10.1038/ni1322.
55. Satoh-Takayama N, Dumoutier L, Lesjean-Pottier S, Ribeiro VS, Mandelboim O, Renauld JC, et al. The natural cytotoxicity receptor NKp46 is dispensable for IL-22-mediated innate intestinal immune defense against Citrobacter rodentium. J Immunol (2009) 183(10):6579-87. doi:10.4049/jimmunol.0901935.
56. Moretta L. Lymphocyte effector mechanisms in innate and adaptive immunity. Curr Opin Immunol (2005) 17(3):303-5. doi:10.1016/j.coi.2005.04.011.
57. Gur C, Porgador A, Elboim M, Gazit R, Mizrahi S, Stern-Ginossar N, et al. The activating receptor NKp46 is essential for the development of type 1 diabetes. Nat Immunol (2010) 11(2):121-8. doi:10.1038/ni.1834.
58. Gur C, Enk J, Kassem SA, Suissa Y, Magenheim J, Stolovich-Rain M, et al. Recognition and killing of human and murine pancreatic beta cells by the NK receptor NKp46. J Immunol (2011) 187(6):3096-103. doi:10.4049/jimmunol.1101269.
59. Gur C, Doron S, Kfir-Erenfeld S, Horwitz E, Abu-Tair L, Safadi R, et al. NKp46-mediated killing of human and mouse hepatic stellate cells attenuates liver fibrosis. Gut (2012) 61(6):885-93. doi:10.1136/gutjnl-2011-301400.
60. Abeyweera TP, Merino E, Huse M. Inhibitory signaling blocks activating receptor clustering and induces cytoskeletal retraction in natural killer cells. J Cell Biol (2011) 192(4):675-90. doi:10.1083/jcb.201009135.
61. Paik SG, Fleischer N, Shin SI. Insulin-dependent diabetes mellitus induced by subdiabetogenic doses of streptozotocin: obligatory role of cell-mediated autoimmune processes. Proc Natl Acad Sci U S A (1980) 77(10):6129-33. doi:10.1073/pnas.77.10.6129.
62. Seydel HG, Loomus MG, Krohmer JS, MacLean CJ. The effect of irradiation in the therapeutic dose range on vascular-graft material. Radiology (1983) 146(3):815-6.
63. Lehuen A, Diana J, Zaccone P, Cooke A. Immune cell crosstalk in type 1 diabetes. Nat Rev Immunol (2010) 10(7):501-13. doi:10.1038/nri2787.
64. Flodstrom M, Maday A, Balakrishna D, Cleary MM, Yoshimura A, Sarvetnick N. Target cell defense prevents the development of diabetes after viral infection. Nat Immunol (2002) 3(4):373-82. doi:10.1038/ni771.
65. MacKay P, Jacobson J, Rabinovitch A. Spontaneous diabetes mellitus in the Bio-Breeding/Worcester rat. Evidence in vitro for natural killer cell lysis of islet cells. J Clin Invest (1986) 77(3):916-24. doi:10.1172/JCI112390.
66. Koevary SB. In vitro natural killer cell activity in the spontaneously diabetic BB/Wor rat: effects of serum on lysis of insulinoma cells. Diabetes Res (1988) 8(2):77-84.
67. Nakamura N, Woda BA, Tafuri A, Greiner DL, Reynolds CW, Ortaldo J, et al. Intrinsic cytotoxicity of natural killer cells to pancreatic islets in vitro. Diabetes (1990) 39(7):836-43. doi:10.2337/diab.39.7.836.
68. Nishikado H, Mukai K, Kawano Y, Minegishi Y, Karasuyama H. NK cell-depleting anti-asialo GM1 antibody exhibits a lethal off-target effect on basophils in vivo. J Immunol (2011) 186(10):5766-71. doi:10.4049/jimmunol.1100370.
69. Maruyama T, Watanabe K, Yanagawa T, Kasatani T, Kasuga A, Shimada A, et al. The suppressive effect of anti-asialo GM1 antibody on low-dose streptozotocin-induced diabetes in CD-1 mice. Diabetes Res (1991) 16(4):171-5.
70. Maruyama T, Watanabe K, Takei I, Kasuga A, Shimada A, Yanagawa T, et al. Anti-asialo GM1 antibody suppression of cyclophosphamide-induced diabetes in NOD mice. Diabetes Res (1991) 17(1):37-41.
71. Poirot L, Benoist C, Mathis D. Natural killer cells distinguish innocuous and destructive forms of pancreatic islet autoimmunity. Proc Natl Acad Sci U S A (2004) 101(21):8102-7. doi:10.1073/pnas.0402065101.
72. Rodacki M, Milech A, de Oliveira JE. NK cells and type 1 diabetes. Clin Dev Immunol (2006) 13(2-4):101-7. doi:10.1080/17402520600877182.
73. Rodacki M, Svoren B, Butty V, Besse W, Laffel L, Benoist C, et al. Altered natural killer cells in type 1 diabetic patients. Diabetes (2007) 56(1):177-85. doi:10.2337/db06-0493.
74. van der Slik AR, Koeleman BP, Verduijn W, Bruining GJ, Roep BO, Giphart MJ. KIR in type 1 diabetes: disparate distribution of activating and inhibitory natural killer cell receptors in patients versus HLA-matched control subjects. Diabetes (2003) 52(10):2639-42. doi:10.2337/diabetes.52.10.2639.
75. Nair MP, Lewis EW, Schwartz SA. Immunoregulatory dysfunctions in type I diabetes: natural and antibody-dependent cellular cytotoxic activities. J Clin Immunol (1986) 6(5):363-72. doi:10.1007/BF00915375.
76. Gur C, Enk J, Weitman E, Bachar E, Suissa Y, Cohen G, et al. The expression of the beta cell-derived autoimmune ligand for the killer receptor nkp46 is attenuated in type 2 diabetes. PLoS One (2013) 8(8):e74033. doi:10.1371/journal.pone.0074033.
77. Nir T, Melton DA, Dor Y. Recovery from diabetes in mice by beta cell regeneration. J Clin Invest (2007) 117(9):2553-61. doi:10.1172/JCI32959.
78. Suni MA, Maino VC, Maecker HT. Ex vivo analysis of T-cell function. Curr Opin Immunol (2005) 17(4):434-40. doi:10.1016/j.coi.2005.05.002.
79. Janeway CA. Natural killer cells: a primitive immune system. Nature (1989) 341(6238):108. doi:10.1038/341108a0.