Acute upregulation of an NKG2D ligand promotes rapid reorganization of a local immune compartment with pleiotropic effects on carcinogenesis

Nature Immunology

Volumn 9, Issue 2, 2008, Pages 146-154

  Strid, Jessica ^a   Roberts, Scott J ^b   Filler, Renata B ^b   Lewis, Julia M ^b   Kwong, Bernice Y ^b   Schpero, William ^b   Kaplan, Daniel H ^c   Hayday, Adrian C ^a   Girardi, Michael ^a  

^a GUY S HOSPITAL   (United Kingdom)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL RECEPTOR NKG2D; PROTEIN; RETINOIC ACID EARLY INDUCIBLE 1 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; EPITHELIUM; GRAFT REJECTION; IMMUNOREGULATION; IMMUNOSURVEILLANCE; IN VIVO STUDY; INFLAMMATION; LANGERHANS CELL; LYMPHOCYTIC INFILTRATION; MOUSE; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; UPREGULATION;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; EPIDERMIS; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNOLOGIC SURVEILLANCE; LANGERHANS CELLS; LIGANDS; MICE; MICE, INBRED STRAINS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, IMMUNOLOGIC; SKIN NEOPLASMS; T-LYMPHOCYTES; UP-REGULATION;

EID: 38349191091     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni1556     Document Type: Article

References (50)

1. Smyth, M.J., Dunn, G.P. & Schreiber, R.D. Cancer immunosurveilance and immuno-editing: The roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv. Immunol. 90, 1-50 (2006).
2. Qin, Z. & Blankenstein, T. A cancer immunosurveillance controversy. Nat Immunol 5, 3-4 (2004).
3. α14 NKT cells in IL-12-mediated rejection of tumors. Science 278, 1623-1626 (1997).
4. α14 NKT cells by glycosylceramides. Science 278, 1626-1629 (1997).
5. Girardi, M. et al. Regulation of cutaneous malignancy by γδ T cells. Science 294, 605-609 (2001).
6. + T cells to different stages of chemically induced skin cancer. J. Exp. Med. 198, 747-755 (2003).
7. Wilhelm, M. et al. γδ T cells for immune therapy of patients with lymphoid malignancies. Blood 102, 200-206 (2003).
8. Dieli, F. et al. Targeting human γδ Tcells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 67, 7450-7457 (2007).
9. Bauer, S. et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285, 727-729 (1999).
10. Diefenbach, A., Jamieson, A.M., Liu, S.D., Shastri, N. & Raulet, D.H. Ligands for the murine NKG2D receptor: Expression by tumor cells and activation of NK cells and macrophages. Nat. Immunol. 1, 119-126 (2000).
11. Cerwenka, A. et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12, 721-727 (2000).
12. Carayannopoulos, L.N., Naidenko, O.V., Fremont, D.H. & Yokoyama, W.M. Cutting edge: Murine UL16-binding proteinAlike transcript 1: a newly described transcript encoding a high-affinity ligand for murine NKG2D. J. Immunol. 169, 4079-4083 (2002).
13. Groh, V. et al. Broad tumor-associated expression and recognition by tumor-derived γδ T cells of MICA and MICB. Proc. Natl. Acad. Sci. USA 96, 6879-6884 (1999).
14. Gasser, S., Orsulic, S., Brown, E.J. & Raulet, D.H. The DNA damage pathway regulates innate immune system ligands at the NKG2D receptor. Nature 436, 1186-1190 (2005).
15. Rolle, A. et al. Effects of human cytomegalovirus infection on ligands for the activating NKG2D receptor of NK cells: Up-regulation of UL16-binding protein (ULBP)1 and ULBP2 is counteracted by the viral UL16 protein. J. Immunol. 171, 902-908 (2003).
16. Zou, Y., Stastny, P., Susal, C., Dohler, B. & Opelz, G. Antibodies against MICA antigens and kidney-transplant rejection. N. Engl. J. Med. 357, 1293-1300 (2007).
17. Ogasawara, K. et al. NKG2D blockade prevents autoimmune diabetes in NOD mice. Immunity 20, 757-767 (2004).
18. Groh, V., Bruhl, A., El-Gabalawy, H., Nelson, J.L. & Spies, T. Stimulation of T cell autoreactivity by anomalous expression of NKG2D and its MIC ligands in rheumatoid arthritis. Proc. Natl. Acad. Sci. USA 100, 9452-9457 (2003).
19. Smyth, M.J. et al. NKG2D function protects the host from tumor initiation. J. Exp. Med. 202, 583-588 (2005).
20. Groh, V., Wu, J., Yee, C. & Spies, T. Tumour-derived soluble MIC ligands impair expression of NKG2D and T-cell activation. Nature 419 734-738 (2002).
21. Dunn, G.P., Old, L.J. & Schreiber, R.D. The three Es of cancer immunoediting. Annu. Rev. Immunol. 22, 329-360 (2004).
22. Wiemann, K. et al. Systemic NKG2D down-regulation impairs NK and CD8 T cell responses in vivo. J. Immunol. 175, 720-729 (2005).
23. Oppenheim, D.E. et al. Sustained localized expression of ligand for the activating NKG2D receptor impairs natural cytotoxicity in vivo and reduces tumor immuno-surveillance. Nat. Immunol. 6 928-937 (2005).
24. + T cell populations lacking helper function. Nat. Immunol. 6, 163-170 (2005).
25. Mantovani, A., Bottazzi, B., Colotta, F., Sozzani, S. & Ruco, L. The origin and function of tumor-associated macrophages. Immunol. Today 13, 265-270 (1992).
26. Roberts, S.J. et al. Characterizing tumor-promoting T cells in chemically induced cutaneous carcinogenesis. Proc. Natl. Acad. Sci. USA 104, 6770-6775 (2007).
27. Banchereau, J. & Steinman, R.M. Dendritic cells and the control of immunity. Nature 392, 245-252 (1998).
28. Born, W. et al. Immunoregulatory functions of γδ T cells. Adv. Immunol. 71, 77-144 (1999).
29. Girardi, M. et al. Resident skin-specific γδ T cells provide local, nonredundant regulation of cutaneous inflammation. J. Exp. Med. 195, 855-867 (2002).
30. Kaplan, D.H., Jenison, M.C., Saeland, S., Shlomchik, W.D. & Shlomchik, M.J. Epidermal langerhans cell-deficient mice develop enhanced contact hypersensitivity. Immunity 23, 611-620 (2005).
31. Medzhitov, R., Preston-Hurlburt, P. & Janeway, C.A., Jr. A human homologue of the Drosophila Toll protein signals activation of adaptive immunity. Nature 398, 394-397 (1997).
32. Graham, D.B. et al. Vav1 controls DAP10-mediated natural cytotoxicity by regulating actin and microtubule dynamics. J. Immunol. 177, 2349-2355 (2006).
33. Nishibu, A. et al Behavioral responses of epidermal Langerhans cells in situ to local pathological stimuli. J. Invest. Dermatol. 126, 787-796 (2006).
34. Jameson, J.M., Cauvi, G., Witherden, D.A. & Havran, W.L. A keratinocyte-responsive γδ TCR is necessary for dendritic epidermal T cell activation by damaged keratinocytes and maintenance in the epidermis. J. Immunol. 172, 3573-3579 (2004).
35. Bendelac, A., Savage, P.B. & Teyton, L. The biology of NKT cells. Annu. Rev Immunol. 25, 297-336 (2007).
36. Godfrey, D.I., MacDonald, H.R., Kronenberg, M., Smyth, M.J. & Van Kaer, L. NKT cells: What's in a name? Nat. Rev. Immunol. 4, 231-237 (2004).
37. Miller, S.J. et al. Mouse skin is particularly susceptible to tumor initiation during early anagen of the hair cycle: Possible involvement of hair follicle stem cells. J. Invest. Dermatol. 101, 591-594 (1993).
38. Trempus, C.S. et al. CD34 expression by hair follicle stem cells is required for skin tumor development in mice. Cancer Res. 67 4173-4181 (2007).
39. γ gene usage. Science 279, 1729-1733 (1998).
40. Willimsky, G. & Blankenstein, T. Sporadic immunogenic tumours avoid destruction by inducing T-cell tolerance. Nature 437, 141-146 (2005).
41. Schreiber, R.D., Did, L.J., Hayday, A.C. & Smyth, M.J. Response to 'A cancer immunosurveillance controversy'. Nat. Immunol. 5, 4-5 (2004).
42. Bonish, B. et al. Overexpression of CD1d by keratinocytes in psoriasis and CD1d-dependent IFN-γ production by NK-T cells. J. Immunol. 165, 4076-4085 (2000).
43. Cameron, A.L., Kirby, B., Fei, W. & Griffiths, C.E. Natural killer and natural killer-T cells in psoriasis. Arch. Dermatol. Res. 294 363-369 (2002).
44. Moodycliffe, A.M., Nghiem, D., Clydesdale, G. & Ullrich, S.E. Immune suppression and skin cancer development: Regulation ty NKT cells. Nat. Immunol. 1, 521-525 (2000).
45. Ambrosino, E. et al. Cross-regulation between type I and type II NRT cells in regulating tumor immunity: A new immunoregulatory axis. J. Immunol. 179, 5126-5136 (2007).
46. α18 CD1d-restricted (type II) NKT cell is sufficient for down-regulation of tumor immunosurveillance. J. Exp. Med. 202, 1627-1633 (2005).
47. Stephens, H.A. MICA and MICB genes: Can the enigma of their polymorphism be resolved? Trends Immunol 22, 378-385 (2001).
48. Jinushi, M., Hodi, F.S. & Dranoff, G. Therapy-induced antibodies to MHC class I chain-related protein A antagonize immune suppression and stimulate antitumor cytotoxicity. Proc. Natl. Acad. Sci. USA 103, 9190-9195 (2006).
49. Grossman, Z. & Paul, W.E. Adaptive cellular interactions in the immune system: The tunable activation threshold and the significance of subthreshold responses. Proc. Natl. Acad. Sci. USA 89, 10365-10369 (1992).
50. + T cell repertoire by a thymic stromal determinant. Nat. Immunol. 7, 843-850 (2006).