Human immunology: An NKG2D-mediated human lymphoid stress surveillance response with high interindividual variation

Science Translational Medicine

Volumn 3, Issue 113, 2011, Pages

  Shafi, Seema ^a   Vantourout, Pierre ^a,b   Wallace, Graham ^c   Antoun, Ayman ^c   Vaughan, Robert ^d,e   Stanford, Miles ^f   Hayday, Adrian ^a,b,e,f  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d GUY S HOSPITAL   (United Kingdom)

^e MEDICAL RESEARCH COUNCIL   (United Kingdom)

^f ST THOMAS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN MICA; UNCLASSIFIED DRUG; HLA ANTIGEN CLASS 1; KLRK1 PROTEIN, HUMAN; MHC CLASS I RELATED CHAIN A; MHC CLASS I-RELATED CHAIN A; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY K;

ALLELE; ARTICLE; CELL KILLING; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; GENETIC POLYMORPHISM; HUMAN; HUMAN CELL; IMMUNOSURVEILLANCE; LYMPHOID TISSUE; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; T LYMPHOCYTE; ANIMAL; CHO CELL; CRICETULUS; CYTOLOGY; GENETICS; HAMSTER; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; PHYSIOLOGICAL STRESS;

ANIMALS; CHO CELLS; CRICETINAE; CRICETULUS; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNOLOGIC SURVEILLANCE; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY K; POLYMORPHISM, GENETIC; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTES;

EID: 83655193395     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3002922     Document Type: Article

References (34)

1. M. Gleimer, P. Parham, Stress management: MHC class I and class I-like molecules as reporters of cellular stress. Immunity 19, 469-477 (2003).
2. A. C. Hayday, gd T cells and the lymphoid stress-surveillance response. Immunity 31, 184-196 (2009).
3. J. Strid, S. J. Roberts, R. B. Filler, J. M. Lewis, B. Y. Kwong, W. Schpero, D. H. Kaplan, A. C. Hayday, M. Girardi, Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis. Nat. Immunol. 9, 146-154 (2008).
4. L. Fernández-Messina, O. Ashiru, P. Boutet, S. Agüera-González, J. N. Skepper, H. T. Reyburn, M. Valés-Gómez, Differential mechanisms of shedding of the glycosylphosphatidylinositol (GPI)-anchored NKG2D ligands. J. Biol. Chem. 285, 8543-8551 (2010).
5. I. Waldhauer, D. Goehlsdorf, F. Gieseke, T. Weinschenk, M. Wittenbrink, A. Ludwig, S. Stevanovic, H. G. Rammensee, A. Steinle, Tumor-associated MICA is shed by ADAM proteases. Cancer Res. 68, 6368-6376 (2008).
6. G. W. Wilkinson, P. Tomasec, R. J. Stanton, M. Armstrong, V. Prod'homme, R. Aicheler, B. P. McSharry, C. R. Rickards, D. Cochrane, S. Llewellyn-Lacey, E. C. Wang, C. A. Griffin, A. J. Davison, Modulation of natural killer cells by human cytomegalovirus. J. Clin. Virol. 41, 206-212 (2008).
7. W. A. Flegel, Will MICA glitter for recipients of kidney transplants? N. Engl. J. Med. 357, 1337-1339 (2007).
8. Y. T. Bryceson, H. G. Ljunggren, E. O. Long, Minimal requirement for induction of natural cytotoxicity and intersection of activation signals by inhibitory receptors. Blood 114, 2657-2666 (2009).
9. Y. T. Bryceson, M. E. March, H. G. Ljunggren, E. O. Long, Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107, 159-166 (2006).
10. H. Das, V. Groh, C. Kuijl, M. Sugita, C. T. Morita, T. Spies, J. F. Bukowski, MICA engagement by human Vg2Vd2 T cells enhances their antigen-dependent effector function. Immunity 15, 83-93 (2001).
11. S. Nedellec, C. Sabourin, M. Bonneville, E. Scotet, NKG2D costimulates human Vγ9Vδ2 T cell antitumor cytotoxicity through protein kinase Cθ-dependent modulation of early TCR-induced calcium and transduction signals. J. Immunol. 185, 55-63 (2010).
12. B. Rincon-Orozco, V. Kunzmann, P. Wrobel, D. Kabelitz, A. Steinle, T. Herrmann, Activation of Vγ9Vδ2 T cells by NKG2D. J. Immunol. 175, 2144-2151 (2005).
13. R. A. Eagle, J. Trowsdale, Promiscuity and the single receptor: NKG2D. Nat. Rev. Immunol. 7, 737-744 (2007).
14. K. Eleme, S. B. Taner, B. Onfelt, L. M. Collinson, F. E. McCann, N. J. Chalupny, D. Cosman, C. Hopkins, A. I. Magee, D. M. Davis, Cell surface organization of stress-inducible proteins ULBP and MICA that stimulate human NK cells and T cells via NKG2D. J. Exp. Med. 199, 1005-1010 (2004).
15. H. Suemizu, M. Radosavljevic, M. Kimura, S. Sadahiro, S. Yoshimura, S. Bahram, H. Inoko, A basolateral sorting motif in the MICA cytoplasmic tail. Proc. Natl. Acad. Sci. U.S.A. 99, 2971-2976 (2002).
16. N. Fodil, L. Laloux, V. Wanner, P. Pellet, G. Hauptmann, N. Mizuki, H. Inoko, T. Spies, I. Theodorou, S. Bahram, Allelic repertoire of the human MHC class I MICA gene. Immunogenetics 44, 351-357 (1996).
17. M. T. Borchers, N. L. Harris, S. C. Wesselkamper, M. Vitucci, D. Cosman, NKG2D ligands are expressed on stressed human airway epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L222-L231 (2006).
18. R. A. Eagle, G. Flack, A. Warford, J. Martínez-Borra, I. Jafferji, J. A. Traherne, M. Ohashi, L. H. Boyle, A. D. Barrow, S. Caillat-Zucman, N. T. Young, J. Trowsdale, Cellular expression, trafficking, and function of two isoforms of human ULBP5/RAET1G. PLoS One 4, e4503 (2009).
19. L. L. Molinero, M. B. Fuertes, G. A. Rabinovich, L. Fainboim, N. W. Zwirner, Activation-induced expression of MICA on T lymphocytes involves engagement of CD3 and CD28. J. Leukoc. Biol. 71, 791-797 (2002).
20. M. R. Betts, J. M. Brenchley, D. A. Price, S. C. De Rosa, D. C. Douek, M. Roederer, R. A. Koup, Sensitive and viable identification of antigen-specific CD8+ T cells by a flow cytometric assay for degranulation. J. Immunol. Methods 281, 65-78 (2003).
21. J. Deguine, B. Breart, F. Lemaître, J. P. Di Santo, P. Bousso, Intravital imaging reveals distinct dynamics for natural killer and CD8+ T cells during tumor regression. Immunity 33, 632-644 (2010).
22. O. Ashiru, P. Boutet, L. Fernández-Messina, S. Agüera-González, J. N. Skepper, M. Valés-Gómez, H. T. Reyburn, Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res. 70, 481-489 (2010).
23. + cells. Nat. Immunol. 4, 991-998 (2003).
24. G. de Saint Basile, G. Ménasché, A. Fischer, Molecular mechanisms of biogenesis and exocytosis of cytotoxic granules. Nat. Rev. Immunol. 10, 568-579 (2010).
25. P. Brodin, K. Kärre, P. Höglund, NK cell education: Not an on-off switch but a tunable rheostat. Trends Immunol. 30, 143-149 (2009).
26. N. T. Joncker, N. C. Fernandez, E. Treiner, E. Vivier, D. H. Raulet, NK cell responsiveness is tuned commensurate with the number of inhibitory receptors for self-MHC class I: The rheostat model. J. Immunol. 182, 4572-4580 (2009).
27. Z. Grossman, W. E. Paul, Adaptive cellular interactions in the immune system: The tunable activation threshold and the significance of subthreshold responses. Proc. Natl. Acad. Sci. U.S.A. 89, 10365-10369 (1992).
28. W. Cookson, L. Liang, G. Abecasis, M. Moffatt, M. Lathrop, Mapping complex disease traits with global gene expression. Nat. Rev. Genet. 10, 184-194 (2009).
29. V. A. Boussiotis, G. J. Freeman, A. Berezovskaya, D. L. Barber, L. M. Nadler, Maintenance of human T cell anergy: Blocking of IL-2 gene transcription by activated Rap1. Science 278, 124-128 (1997).
30. H. Wang, M. L. Madariaga, S. Wang, N. Van Rooijen, P. A. Oldenborg, Y. G. Yang, Lack of CD47 on nonhematopoietic cells induces split macrophage tolerance to CD47null cells. Proc. Natl. Acad. Sci. U.S.A. 104, 13744-13749 (2007).
31. G. R. Wallace, D. H. Verity, L. J. Delamaine, S. Ohno, H. Inoko, M. Ota, N. Mizuki, K. Yabuki, E. Kondiatis, H. A. Stephens, W. Madanat, C. A. Kanawati, M. R. Stanford, R. W. Vaughan, MIC-A allele profiles and HLA class I associations in Behçet's disease. Immunogenetics 49, 613-617 (1999).
32. M. Jinushi, F. S. Hodi, G. Dranoff, Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc. Natl. Acad. Sci. U.S.A. 103, 9190-9195 (2006).
33. T. Lança, D. V. Correia, C. F. Moita, H. Raquel, A. Neves-Costa, C. Ferreira, J. S. Ramalho, J. T. Barata, L. F. Moita, A. Q. Gomes, B. Silva-Santos, The MHC class Ib protein ULBP1 is a nonredundant determinant of leukemia/lymphoma susceptibility to gd T-cell cytotoxicity. Blood 115, 2407-2411 (2010).
34. D. E. Oppenheim, S. J. Roberts, S. L. Clarke, R. Filler, J. M. Lewis, R. E. Tigelaar, M. Girardi, A. C. Hayday, Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immunosurveillance. Nat. Immunol. 6, 928-937 (2005).