Distinct roles for the NK cell-activating receptors in mediating interactions with dendritic cells and tumor cells

Journal of Immunology

Volumn 186, Issue 1, 2011, Pages 222-229

  Wai, Lu En ^a   Garcia, Jordan A ^a   Martinez, Olivia M ^a   Krams, Sheri M ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GAMMA INTERFERON; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2D; NATURAL KILLER CELL RECEPTOR NKP30; NATURAL KILLER CELL RECEPTOR NKP46; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL ACTIVATION; CELL CONTACT; CELL INTERACTION; COCULTURE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXICITY; DENDRITIC CELL; HEPATOMA CELL; IMMUNITY; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TUMOR CELL;

ADAPTIVE IMMUNITY; ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL COMMUNICATION; CELL LINE, TUMOR; CELLS, CULTURED; COCULTURE TECHNIQUES; CYTOTOXICITY TESTS, IMMUNOLOGIC; DENDRITIC CELLS; IMMUNITY, INNATE; INTERFERON-GAMMA; LECTINS, C-TYPE; LIVER NEOPLASMS, EXPERIMENTAL; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 1; NATURAL CYTOTOXICITY TRIGGERING RECEPTOR 3; NEOPLASM PROTEINS; RATS; RATS, INBRED LEW; RECEPTORS, IMMUNOLOGIC; TRANS-ACTIVATORS;

EID: 79251573522     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1002597     Document Type: Article

References (47)

1. Caligiuri, M. A. 2008. Human natural killer cells. Blood 112: 461-469.
2. Parham, P. 2005. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 5: 201-214.
3. Bauer, S., V. Groh, J. Wu, A. Steinle, J. H. Phillips, L. L. Lanier, and T. Spies. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stressinducible MICA. Science 285: 727-729.
4. Cosman, D., J. Müllberg, C. L. Sutherland, W. Chin, R. Armitage, W. Fanslow, M. Kubin, and N. J. Chalupny. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14: 123-133.
5. Diefenbach, A., A. M. Jamieson, S. D. Liu, N. Shastri, and D. H. Raulet. 2000. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1: 119-126.
6. Savithri, B., and A. Khar. 2006. A transmembrane-anchored rat RAE-1-like transcript as a ligand for NKR-P2, the rat ortholog of human and mouse NKG2D. Eur. J. Immunol. 36: 107-117.
7. Moretta, L., and A. Moretta. 2004. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J. 23: 255-259. (Pubitemid 38294490)
8. Moretta, A., R. Biassoni, C. Bottino, M. C. Mingari, and L. Moretta. 2000. Natural cytotoxicity receptors that trigger human NK-cell-mediated cytolysis. Immunol. Today 21: 228-234. (Pubitemid 30259028)
9. Mandelboim, O., N. Lieberman, M. Lev, L. Paul, T. I. Arnon, Y. Bushkin, D. M. Davis, J. L. Strominger, J. W. Yewdell, and A. Porgador. 2001. Recognition of haemagglutinins on virus-infected cells by NKp46 activates lysis by human NK cells. Nature 409: 1055-1060.
10. Arnon, T. I., M. Lev, G. Katz, Y. Chernobrov, A. Porgador, and O. Mandelboim. 2001. Recognition of viral hemagglutinins by NKp44 but not by NKp30. Eur. J. Immunol. 31: 2680-2689.
11. Draghi, M., A. Pashine, B. Sanjanwala, K. Gendzekhadze, C. Cantoni, D. Cosman, A. Moretta, N. M. Valiante, and P. Parham. 2007. NKp46 and NKG2D recognition of infected dendritic cells is necessary for NK cell activation in the human response to influenza infection. J. Immunol. 178: 2688-2698.
12. Arnon, T. I., H. Achdout, O. Levi, G. Markel, N. Saleh, G. Katz, R. Gazit, T. Gonen-Gross, J. Hanna, E. Nahari, et al. 2005. Inhibition of the NKp30 activating receptor by pp65 of human cytomegalovirus. Nat. Immunol. 6: 515-523.
13. Pogge von Strandmann, E., V. R. Simhadri, B. von Tresckow, S. Sasse, K. S. Reiners, H. P. Hansen, A. Rothe, B. Böll, V. L. Simhadri, P. Borchmann, et al. 2007. Human leukocyte antigen-B-associated transcript 3 is released from tumor cells and engages the NKp30 receptor on natural killer cells. Immunity 27: 965-974.
14. Brandt, C. S., M. Baratin, E. C. Yi, J. Kennedy, Z. Gao, B. Fox, B. Haldeman, C. D. Ostrander, T. Kaifu, C. Chabannon, et al. 2009. The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J. Exp. Med. 206: 1495-1503.
15. Bloushtain, N., U. Qimron, A. Bar-Ilan, O. Hershkovitz, R. Gazit, E. Fima, M. Korc, I. Vlodavsky, N. V. Bovin, and A. Porgador. 2004. Membrane-associated heparan sulfate proteoglycans are involved in the recognition of cellular targets by NKp30 and NKp46. J. Immunol. 173: 2392-2401.
16. Warren, H. S., A. L. Jones, C. Freeman, J. Bettadapura, and C. R. Parish. 2005. Evidence that the cellular ligand for the human NK cell activation receptor NKp30 is not a heparan sulfate glycosaminoglycan. J. Immunol. 175: 207-212.
17. Pende, D., C. Cantoni, P. Rivera, M. Vitale, R. Castriconi, S. Marcenaro, M. Nanni, R. Biassoni, C. Bottino, A. Moretta, and L. Moretta. 2001. Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxicity receptors and capability of recognizing tumors of non-epithelial origin. Eur. J. Immunol. 31: 1076-1086.
18. Ferlazzo, G., M. L. Tsang, L. Moretta, G. Melioli, R. M. Steinman, and C. Münz. 2002. Human dendritic cells activate resting natural killer (NK) cells and are recognized via the NKp30 receptor by activated NK cells. J. Exp. Med. 195: 343-351.
19. Spaggiari, G. M., R. Carosio, D. Pende, S. Marcenaro, P. Rivera, M. R. Zocchi, L. Moretta, and A. Poggi. 2001. NK cell-mediated lysis of autologous antigen-presenting cells is triggered by the engagement of the phosphatidylinositol 3-kinase upon ligation of the natural cytotoxicity receptors NKp30 and NKp46. Eur. J. Immunol. 31: 1656-1665.
20. Vitale, M., M. Della Chiesa, S. Carlomagno, D. Pende, M. Aricò, L. Moretta, and A. Moretta. 2005. NK-dependent DC maturation is mediated by TNFalpha and IFNgamma released upon engagement of the NKp30 triggering receptor. Blood 106: 566-571.
21. Piccioli, D., S. Sbrana, E. Melandri, and N. M. Valiante. 2002. Contact-dependent stimulation and inhibition of dendritic cells by natural killer cells. J. Exp. Med. 195: 335-341.
22. Gerosa, F., B. Baldani-Guerra, C. Nisii, V. Marchesini, G. Carra, and G. Trinchieri. 2002. Reciprocal activating interaction between natural killer cells and dendritic cells. J. Exp. Med. 195: 327-333.
23. Gerosa, F., A. Gobbi, P. Zorzi, S. Burg, F. Briere, G. Carra, and G. Trinchieri. 2005. The reciprocal interaction of NK cells with plasmacytoid or myeloid dendritic cells profoundly affects innate resistance functions. J. Immunol. 174: 727-734. (Pubitemid 40094266)
24. Jinushi, M., T. Takehara, T. Kanto, T. Tatsumi, V. Groh, T. Spies, T. Miyagi, T. Suzuki, Y. Sasaki, and N. Hayashi. 2003. Critical role of MHC class I-related chain A and B expression on IFN-α-stimulated dendritic cells in NK cell activation: impairment in chronic hepatitis C virus infection. J. Immunol. 170: 1249-1256. (Pubitemid 36139490)
25. Andoniou, C. E., S. L. H. van Dommelen, V. Voigt, D. M. Andrews, G. Brizard, C. Asselin-Paturel, T. Delale, K. J. Stacey, G. Trinchieri, and M. A. Degli-Esposti. 2005. Interaction between conventional dendritic cells and natural killer cells is integral to the activation of effective antiviral immunity. Nat. Immunol. 6: 1011-1019.
26. Gazit, R., R. Gruda, M. Elboim, T. I. Arnon, G. Katz, H. Achdout, J. Hanna, U. Qimron, G. Landau, E. Greenbaum, et al. 2006. Lethal influenza infection in the absence of the natural killer cell receptor gene Ncr1. Nat. Immunol. 7: 517-523.
27. Halfteck, G. G., M. Elboim, C. Gur, H. Achdout, H. Ghadially, and O. Mandelboim. 2009. Enhanced in vivo growth of lymphoma tumors in the absence of the NK-activating receptor NKp46/NCR1. J. Immunol. 182: 2221-2230.
28. Satoh-Takayama, N., C. A. J. Vosshenrich, S. Lesjean-Pottier, S. Sawa, M. Lochner, F. Rattis, J.-J. Mention, K. Thiam, N. Cerf-Bensussan, O. Mandelboim, et al. 2008. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 29: 958-970.
29. Luci, C., A. Reynders, I. I. Ivanov, C. Cognet, L. Chiche, L. Chasson, J. Hardwigsen, E. Anguiano, J. Banchereau, D. Chaussabel, et al. 2009. Influence of the transcription factor RORγt on the development of NKp46+ cell populations in gut and skin. Nat. Immunol. 10: 75-82.
30. Sanos, S. L., V. L. Bui, A. Mortha, K. Oberle, C. Heners, C. Johner, and A. Diefenbach. 2009. RORγt and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat. Immunol. 10: 83-91.
31. Pende, D., R. Castriconi, P. Romagnani, G.M. Spaggiari, S. Marcenaro, A. Dondero, E. Lazzeri, L. Lasagni, S. Martini, P. Rivera, et al. 2006. Expression of the DNAM-1 ligands, Nectin-2 (CD112) and poliovirus receptor (CD155), on dendritic cells: relevance for natural killer-dendritic cell interaction. Blood 107: 2030-2036.
32. Hollyoake, M., R. D. Campbell, and B. Aguado. 2005. NKp30 (NCR3) is a pseudogene in 12 inbred and wild mouse strains, but an expressed gene in Mus caroli. Mol. Biol. Evol. 22: 1661-1672.
33. Hsieh, C. L., Y. Ogura, H. Obara,U. A. Ali,G. M. Rodriguez, R. R. Nepomuceno, O. M. Martinez, and S. M. Krams. 2004. Identification, cloning, and characterization of a novel rat natural killer receptor, RNKP30: a molecule expressed in liver allografts. Transplantation 77: 121-128.
34. Hsieh, C. L., K. Nagasaki, O. M. Martinez, and S. M. Krams. 2006. NKp30 is a functional activation receptor on a subset of rat natural killer cells. Eur. J. Immunol. 36: 2170-2180.
35. Westgaard, I. H., S. F. Berg, J. T. Vaage, L. L. Wang, W. M. Yokoyama, E. Dissen, and S. Fossum. 2004. Rat NKp46 activates natural killer cell cytotoxicity and is associated with FcepsilonRIgamma and CD3z. J. Leukoc. Biol. 76: 1200-1206.
36. Zhuo, M., M. Fujiki, M. Wang, K. Piard-Ruster, L.-E. Wai, L. Wei, O. M. Martinez, and S. M. Krams. 2010. Identification of the rat NKG2D ligands, RAE1L and RRLT, and their role in allograft rejection. Eur. J. Immunol. 40: 1748-1757.
37. Matzinger, P. 1991. The JAM test: a simple assay for DNA fragmentation and cell death. J. Immunol. Methods 145: 185-192.
38. Ferlazzo, G., M. Pack, D. Thomas, C. Paludan, D. Schmid, T. Strowig, G. Bougras, W. A. Muller, L. Moretta, and C. Münz. 2004. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc. Natl. Acad. Sci. USA 101: 16606-16611.
39. Poggi, A., C. Prevosto, M. Zancolli, P. Canevali, A. Musso, and M. R. Zocchi. 2007. NKG2D and natural cytotoxicity receptors are involved in natural killer cell interaction with self-antigen presenting cells and stromal cells. Ann. N. Y. Acad. Sci. 1109: 47-57.
40. Lucas, M., W. Schachterle, K. Oberle, P. Aichele, and A. Diefenbach. 2007. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26: 503-517.
41. Fernandez, N. C., A. Lozier, C. Flament, P. Ricciardi-Castagnoli, D. Bellet, M. Suter, M. Perricaudet, T. Tursz, E. Maraskovsky, and L. Zitvogel. 1999. Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat. Med. 5: 405-411.
42. Seth, S., A.-M. Georgoudaki, B. J. Chambers, Q. Qiu, E. Kremmer, M. K. Maier, N. Czeloth, I. Ravens, R. Foerster, and G. Bernhardt. 2009. Heterogeneous expression of the adhesion receptor CD226 on murine NK and T cells and its function in NK-mediated killing of immature dendritic cells. J. Leukoc. Biol. 86: 91-101.
43. Lanier, L. L. 2003. Natural killer cell receptor signaling. Curr. Opin. Immunol. 15: 308-314.
44. Jinushi, M., T. Takehara, T. Tatsumi, T. Kanto, V. Groh, T. Spies, R. Kimura, T. Miyagi, K. Mochizuki, Y. Sasaki, and N. Hayashi. 2003. Expression and role of MICA and MICB in human hepatocellular carcinomas and their regulation by retinoic acid. Int. J. Cancer 104: 354-361.
45. Jinushi, M., T. Takehara, T. Tatsumi, N. Hiramatsu, R. Sakamori, S. Yamaguchi, and N. Hayashi. 2005. Impairment of natural killer cell and dendritic cell functions by the soluble form of MHC class I-related chain A in advanced human hepatocellular carcinomas. J. Hepatol. 43: 1013-1020. (Pubitemid 41627987)
46. Chew, V., C. Tow, M. Teo, H. L. Wong, J. Chan, A. Gehring, M. Loh, A. Bolze, R. Quek, V. K. M. Lee, et al. 2010. Inflammatory tumour microenvironment is associated with superior survival in hepatocellular carcinoma patients. J. Hepatol. 52: 370-379.
47. Byrd, A., S. C. Hoffmann, M. Jarahian, F. Momburg, and C. Watzl. 2007. Expression analysis of the ligands for the natural killer cell receptors NKp30 and NKp44. PLoS One 2: e1339.