NKG2D ligands: Unconventional MHC class I-like molecules exploited by viruses and cancer

Tissue Antigens

Volumn 61, Issue 5, 2003, Pages 335-343

  Cerwenka, A ^a   Lanier, L L ^b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Innate immunity; NK cells; NKG2D; RAE 1

Indexed keywords

CD8 ANTIGEN; CYTOKINE; INTERLEUKIN 10; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MINOR HISTOCOMPATIBILITY ANTIGEN; NKG2D LIGAND; RECOMBINANT PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ANIMAL MODEL; BONE MARROW CELL; CANCER IMMUNOLOGY; CHROMOSOME 10; CHROMOSOME 6; CYTOMEGALOVIRUS INFECTION; GENE; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; RETINOIC ACID INDUCIBLE GENE 1; REVIEW; TUMOR CELL; VIRUS CELL INTERACTION; VIRUS INFECTION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; KILLER CELLS, NATURAL; LIGANDS; MACROPHAGES; MICE; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; VIRAL PROTEINS; VIRUSES;

ANIMALIA; CYTOMEGALOVIRUS;

EID: 0037515740     PISSN: 00012815     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1399-0039.2003.00070.x     Document Type: Review

References (55)

1. Long EO, Colonna M, Lanier LL. Inhibitory MHC class I receptors on NK and T cells: a standard nomenclature. Immunol Today 1996: 17: 100.
2. Lanier LL. NK cell receptors. Annu Rev Immunol 1998: 16: 359-93.
3. Yokoyama WM, Seaman WE. The Ly-49 and NKR-P1 gene families encoding lectin-like receptors on natural killer cells: the NK gene complex. Annu Rev Immunol 1993: 11: 613-35.
4. Hofer E, Sobanov Y, Brostjan C, Lehrach H, Duchler M. The centromeric part of the human natural killer (NK) receptor complex: lectin-like receptor genes expressed in NK, dendritic and endothelial cells. Immunol Rev 2001: 181: 5-19.
5. Houchins JP, Yabe T, McSherry C et al. 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.
6. Wu J, Song Y, Bakker ABH et al. An activating receptor complex on natural killer and T cells formed by NKG2D and DAP10. Science 1999: 285: 730-2.
7. Chang C, Dietrich J, Harpur AG, et al. Cutting edge: KAP10, a novel transmembrane adapter protein genetically linked to DAP12 but with unique signaling properties. J Immunol 1999: 163: 4651-4.
8. Sutherland CL, Chalupny NJ, Schooley K, VandenBos T, Kubin M, Cosman D. UL16-binding proteins, novel MHC class I-related proteins, bind to NKG2D and activate multiple signaling pathways in primary NK cells. J Immunol 2002: 168: 671-9.
9. Wu J, Cherwinski H, Spies T, Phillips JH, Lanier LL. DAP10 and DAP12 form distinct, but functionally cooperative, receptor complexes in natural killer cells. J Exp Med 2000: 192: 1059-68.
10. Diefenbach A, Tomasello E, Lucas M, et al.: Selective associations with signaling proteins determine stimulatory versus costimulatory activity of NKG2D. Nat Immunol 2002: 3: 1142-9.
11. Gilfillan S, Ho EL, Cella M, Yokoyama WM, Colonna M. NKG2D recruits two distinct adapters to trigger NK cell activation and costimulation. Nat Immunol 2002: 3: 1150-5.
12. Lanier LL, Corliss BC, Wu J, Leong C, Phillips JH. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 1998: 391: 703-7.
13. Paloneva J, Kestila M, Wu J, et al.: Loss-of-function mutations in TYROBP (DAP12) result in a presenile dementia with bone cysts. Nat Genet 2000: 25: 357-61.
14. Pende D, Cantoni C, Rivera P et al. Role of NKG2D in tumor cell lysis mediated by human NK cells: cooperation with natural cytotoxidty receptors and capability of recognizing tumors of nonepithelial origin. Eur J Immunol 2001: 31: 1076-86.
15. Menier C, Riteau B, Carosella ED, Rouas-Freiss N. MICA triggering signal for NK cell tumor lysis is counteracted by HLA-G1-mediated inhibitory signal. Int J Cancer 2002: 100: 63-70.
16. Long EO. Regulation of immune responses through inhibitory receptors. Annu Rev Immunol 1999: 17: 875-904.
17. Bahram S. MIC genes: from genetics to biology. Adv Immunol 2000: 76: 1-60.
18. Cosman D, Mullberg J, Fanslow W et al. The human cytomegalovirus (HCMV) glycoprotein, UL16, binds to the MHC class I-related protein, MICB/PERB11, and to two novel, MHC class I-related molecules, ULBP1 and ULBP2. FASEB J 2000: 14: A1018.
19. Radosavljevic M, Cuillerier B, Wilson MJ et al. A cluster of ten novel MHC class I related genes on human chromosome 6q24.2-q25.3. Genomics 2002: 79: 114-23.
20. Strong RK. Asymmetric ligand recognition by the activating natural killer cell receptor NKG2D, a symmetric homodimer. Mol Immunol 2002: 38: 1029-37.
21. Cerwenka A, Bakker AB, McClanahan T et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 2000: 12: 721-7.
22. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nature Immunol 2000: 1: 119-26.
23. Kasahara M, Watanabe Y, Surnasu M, Nagata T. A family of MHC class I-like genes located in the vicinity of the mouse leukocyte receptor complex. Proc Natl Acad Sci U S A 2002: 99: 13687-92.
24. Nomura M, Takihara Y, Shimada K. Isolation and characterization of retinoic acid-inducible cDNA clones in F9 calls: one of the early inducible clones encodes a novel protein sharing several highly homologous regions with a Drosophila polyhomeotic protein. Differentiation 1994: 57: 39-50.
25. Girardi M, Oppenheim DE, Steele CR et al. Regulation of cutaneous malignancy by gammadelta T cells. Science 2001: 294: 605-9.
26. Carayannopoulos LN, Naidenko OV, Fremont DH, Yokoyama WM. Cutting edge: murine UL16-binding protein-like transcript 1: a newly described transcript encoding a high-affinity ligand for murine NKG2D. J Immunol 2002: 169: 4079-83.
27. Malarkannan SPP et al. The molecular and functional characterization of a dominant minor H antigen, H60. J Immunol 1998: 161: 3501-9.
28. Cerwenka A, O'Callaghan CA, Hamerman JA et al. Cutting edge: the minor histocompatibility antigen H60 peptide interacts with both H-2Kb and NKG2D. J Immunol 2002: 168: 3131-4.
29. O'Callaghan CA, Cerwenka A, Willcox BE, Lanier LL, Bjorkman PJ. Molecular competition for NKG2D: H60 and RAE1 compete unequally for NKG2D with dominance of H60. Immunity 2001: 15: 201-11.
30. Carayannopoulos LN, Naidenko OV, Kinder J, Ho EL, Fremont DH, Yokoyama WM. Ligands for murine NKG2D display heterogeneous binding behavior. Eur J Immunol 2002: 32: 597-605.
31. Cerwenka A, Lanier L. Ligands for natural killer cell receptors: redundancy or specificity. Immunol Rev 2001: 181: 158-69.
32. Malarkannan ST, Horng P, Eden F et al. Differences that matter: major cytotoxic T cell-stimulating minor histocompatibility antigens. Immunity 2000: 13: 333-44.
33. Choi EY, Christianson GJ, Yoshimura Y, et al. Immunodominance of H60 is caused by an abnormally high precursor T cell pool directed against its unique minor histocompatibility antigen peptide. Immunity 2002: 17: 593-603.
34. Groh V, Bahram S, Bauer S, Herman A, Beauchamp M, Spies T. Cell stress-regulated human major histocompatibility complex class I gene expressed in gastrointestinal epithelium. Proc Natl Acad Sci U S A 1996: 93: 12445-50.
35. Salih HR, Rammensee HG, Steinle A. Cutting edge: down-regulation of MICA on human tumors by proteolytic shedding. J Immunol 2002: 169: 4098-102.
36. 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.
37. Steinle A, Li P, Morris DL et al. Interactions of human NKG2D with its ligands MICA, MICB, and homologs of the mouse RAE-1 protein family. Immunogenetics 2001: 53: 279-87.
38. Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci U S A 1999: 96: 6879-84.
39. Cerwenka A, Lanier LL. Natural killer cells, viruses and cancer. Nat Rev Immunol 2001: 1: 41-9.
40. Masuda H, Saeki Y, Nomura M et al. High levels of RAE-1 isoforms on mouse tumor cell lines assessed by anti-'pan' RAE-1 antibody confer tumor susceptibility to NK cells. Biochem Biophys Res Commun 2002: 290: 140-5.
41. Ogasawara K, Hamerman JA, Hsin H et al. Impairment of NK cell function by NKG2D modulation in NOD mice. Immunity 2003: 18: 41-51.
42. 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.
43. 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 U S A 2001: 98: 11521-6.
44. Diefenbach A, Jensen ER, Jamieson AM, Raulet DH. Rael and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 2001: 413: 165-71.
45. Hayakawa Y, Kelly JM, Westwood JA et al. Cutting edge: tumor rejection mediated by NKG2D receptor-ligand interaction is dependent upon perforin. J Immunol 2002: 169: 5377-81.
46. Onda H, Ohkubo S, Shintani Y et al. A novel secreted tumor antigen with a glycosylphosphatidylinositol-anchored structure ubiquitously expressed in human cancers. Biochem Biophys Res Commun 2001: 285: 235-43.
47. Spriggs ME. One step ahead of the game: viral immunomodulatory molecules. Annu Rev Immunol 1996: 14: 101-30.
48. Biron CA, Byron KS, Sullivan JL. Severe herpesvirus infections in an adolescent without natural killer calls. N Eng J Med 1989: 320: 1731-5.
49. Groh V, Rhinehart R, Randolph-Habecker J, Topp MS, Riddell SR, Spies T. Costimulation of CD8alphabeta T cells by NKG2D via engagement by MIC induced on virus-infected cells. Nat Immunol 2001: 2: 255-60.
50. Dunn C, Chalupny NJ, Sutherland CL et al. Human cytomegalovirus glycoprotein UL16 causes intracellular sequestration of NKG2D ligands, protecting against NK cell cytotoxicity. J Exp Med 2003: in press.
51. Komatsu-Wakui ME, Tokunaga Y, Ishikawa K et al. MIC-A polymorphism in Japanese and a MIC-A-MIC-B null haplotype. Immunogenetics 1999: 49: 620-8.
52. Tay CH, Welsh RM. Distinct organ-dependent mechanisms for the control of murine cytomegalovirus infection by natural killer cells. J Virol 1997: 71: 267-75.
53. Krmpotic A, Busch DH, Bubic I et al. MCMV glycoprotein gp40 confers virus resistance to CD8+ T cells and NK cells in vivo. Nat Immunol 2002: 3: 529-35.
54. Lodoen M, Ogasawara K, Hamerman JA et al. NKG2D-mediated NK cell protection against cytomegalovirus is impaired by viral gp40 modulation of RAE-1 molecules. J Exp Med 2003: in press.
55. Igney FH, Krammer PH. Immune escape of tumors: apoptosis resistance and tumor counterattack. J Leukoc Biol 2002: 71: 907-20.