Impaired tumor rejection by memory CD8 T cells in mice with NKG2D dysfunction

International Journal of Cancer

Volumn 131, Issue 7, 2012, Pages 1601-1610

  André, Maya Caroline ^a,b   Sigurdardottir, Dagmar ^b,d   Kuttruff, Sabrina ^b   Pömmerl, Beate ^b   Handgretinger, Rupert ^a   Rammensee, Hans Georg ^b   Steinle, Alexander ^b,c  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c GOETHE UNIVERSITY   (Germany)

^d MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

Author keywords

memory CD8 T cells; MICA; NKG2D; tumor immunosurveillance

Indexed keywords

NATURAL KILLER CELL RECEPTOR NKG2D;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CELL; CANCER GROWTH; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOLYSIS; DISEASE SEVERITY; GENE EXPRESSION; IN VIVO STUDY; LYMPHOMA; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC MOUSE; TUMOR REJECTION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, NEOPLASM; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; HUMANS; IMMUNOLOGIC MEMORY; MICE; MICE, TRANSGENIC; NEOPLASMS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K;

EID: 84864488308     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.26191     Document Type: Article

References (41)

1. 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.
2. Das H, Groh V, Kuijl C, Sugita M, Morita CT, Spies T, Bukowski JF,. MICA engagement by human Vγ2Vδ2 T cells enhances their antigen-dependent effector function. Immunity 2001; 15: 83-93.
3. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T,. Costimulation of CD8αβ T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2001; 2: 255-60.
4. Rincon-Orozco B, Kunzmann V, Wrobel P, Kabelitz D, Steinle A, Herrmann T,. Activation of Vγ9Vδ2 T cells by NKG2D. J Immunol 2005; 175: 2144-51.
5. Jamieson AM, Diefenbach A, McMahon CW, Xiong N, Carlyle JR, Raulet DH,. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 2002; 17: 19-29.
6. Eagle RA, Trowsdale J,. Promiscuity and the single receptor: NKG2D. Nat Rev Immunol 2007; 7: 737-44.
7. Gonzalez S, Groh V, Spies T,. Immunobiology of human NKG2D and its ligands. Curr Top Microbiol Immunol 2006; 298: 121-38.
8. Nausch N, Cerwenka A,. NKG2D ligands in tumor immunity. Oncogene 2008; 27: 5944-58.
9. Steinle A, Li P, Morris DL, Groh V, Lanier LL, Strong RK, Spies T,. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics 2001; 53: 279-87.
10. Takada A, Yoshida S, Kajikawa M, Miyatake Y, Tomaru U, Sakai M, Chiba H, Maenaka K, Kohda D, Fugo K, Kasahara M,. Two novel NKG2D ligands of the mouse H60 family with differential expression patterns and binding affinities to NKG2D. J Immunol 2008; 180: 1678-85.
11. Waldhauer I, Steinle A,. NK cells and cancer immunosurveillance. Oncogene 2008; 27: 5932-43.
12. Gasser S, Raulet DH,. The DNA damage response arouses the immune system. Cancer Res 2006; 66: 3959-62.
13. Welte SA, Sinzger C, Lutz SZ, Singh-Jasuja H, Sampaio KL, Eknigk U, Rammensee HG, Steinle A,. Selective intracellular retention of virally induced NKG2D ligands by the human cytomegalovirus UL16 glycoprotein. Eur J Immunol 2003; 33: 194-203.
14. Guerra N, Tan YX, Joncker NT, Choy A, Gallardo F, Xiong N, Knoblaugh S, Cado D, Greenberg NM, Raulet DH,. NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 2008; 28: 571-80.
15. Hayakawa Y, Smyth MJ,. Innate immune recognition and suppression of tumors. Adv Cancer Res 2006; 95: 293-322.
16. Oppenheim DE, Roberts SJ, Clarke SL, Filler R, Lewis JM, Tigelaar RE, Girardi M, Hayday AC,. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat Immunol 2005; 6: 928-37.
17. Smyth MJ, Swann J, Cretney E, Zerafa N, Yokoyama WM, Hayakawa Y,. NKG2D function protects the host from tumor initiation. J Exp Med 2005; 202: 583-8.
18. Zafirova B, Mandaric S, Antulov R, Krmpotic A, Jonsson H, Yokoyama WM, Jonjic S, Polic B,. Altered NK cell development and enhanced NK cell-mediated resistance to mouse cytomegalovirus in NKG2D-deficient mice. Immunity 2009; 31: 270-82.
19. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH,. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001; 413: 165-71.
20. Salih HR, Rammensee HG, Steinle A,. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 2002; 169: 4098-102.
21. Groh V, Wu J, Yee C, Spies T,. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 2002; 419: 734-8.
22. Groh V, Smythe K, Dai Z, Spies T,. Fas-ligand-mediated paracrine T cell regulation by the receptor NKG2D in tumor immunity. Nat Immunol 2006; 7: 755-62.
23. Salih HR, Holdenrieder S, Steinle A,. Soluble NKG2D ligands: prevalence, release, and functional impact. Front Biosci 2008; 13: 3448-56.
24. Wu JD, Atteridge CL, Wang X, Seya T, Plymate SR,. Obstructing shedding of the immunostimulatory MHC class I chain-related gene B prevents tumor formation. Clin Cancer Res 2009; 15: 632-40.
25. Champsaur M, Lanier LL,. Effect of NKG2D ligand expression on host immune responses. Immunol Rev 2010; 235: 267-85.
26. Wiemann K, Mittrucker HW, Feger U, Welte SA, Yokoyama WM, Spies T, Rammensee HG, Steinle A,. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J Immunol 2005; 175: 720-9.
27. Maasho K, Opoku-Anane J, Marusina AI, Coligan JE, Borrego F,. NKG2D is a costimulatory receptor for human naive CD8+ T cells. J Immunol 2005; 174: 4480-4.
28. Markiewicz MA, Carayannopoulos LN, Naidenko OV, Matsui K, Burack WR, Wise EL, Fremont DH, Allen PM, Yokoyama WM, Colonna M, Shaw AS,. Costimulation through NKG2D enhances murine CD8+ CTL function: similarities and differences between NKG2D and CD28 costimulation. J Immunol 2005; 175: 2825-33.
29. Rotzschke O, Falk K, Stevanovic S, Jung G, Walden P, Rammensee HG,. Exact prediction of a natural T cell epitope. Eur J Immunol 1991; 21: 2891-4.
30. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR,. T cell receptor antagonist peptides induce positive selection. Cell 1994; 76: 17-27.
31. Moore MW, Carbone FR, Bevan MJ,. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 1988; 54: 777-85.
32. Mittrucker HW, Kursar M, Kohler A, Hurwitz R, Kaufmann SH,. Role of CD28 for the generation and expansion of antigen-specific CD8(+) T lymphocytes during infection with Listeria monocytogenes. J Immunol 2001; 167: 5620-7.
33. Huster KM, Busch V, Schiemann M, Linkemann K, Kerksiek KM, Wagner H, Busch DH,. Selective expression of IL-7 receptor on memory T cells identifies early CD40L-dependent generation of distinct CD8+ memory T cell subsets. Proc Natl Acad Sci USA 2004; 101: 5610-5.
34. Kaech SM, Tan JT, Wherry EJ, Konieczny BT, Surh CD, Ahmed R,. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat Immunol 2003; 4: 1191-8.
35. Raulet DH, Guerra N,. Oncogenic stress sensed by the immune system: role of natural killer cell receptors. Nat Rev Immunol 2009; 9: 568-80.
36. Cerwenka A, Baron JL, Lanier LL,. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc Natl Acad Sci USA 2001; 98: 11521-6.
37. Wolkers MC, Stoetter G, Vyth-Dreese FA, Schumacher TN,. Redundancy of direct priming and cross-priming in tumor-specific CD8+ T cell responses. J Immunol 2001; 167: 3577-84.
38. Champsaur M, Beilke JN, Ogasawara K, Koszinowski UH, Jonjic S, Lanier LL,. Intact NKG2D-independent function of NK cells chronically stimulated with the NKG2D ligand Rae-1. J Immunol 2010; 185: 157-65.
39. Hamerman JA, Ogasawara K, Lanier LL,. Cutting edge: Toll-like receptor signaling in macrophages induces ligands for the NKG2D receptor. J Immunol 2004; 172: 2001-5.
40. Kloss M, Decker P, Baltz KM, Baessler T, Jung G, Rammensee HG, Steinle A, Krusch M, Salih HR,. Interaction of monocytes with NK cells upon Toll-like receptor-induced expression of the NKG2D ligand MICA. J Immunol 2008; 181: 6711-9.
41. Bertram EM, Dawicki W, Sedgmen B, Bramson JL, Lynch DH, Watts TH,. A switch in costimulation from CD28 to 4-1BB during primary versus secondary CD8 T cell response to influenza in vivo. J Immunol 2004; 172: 981-8.