Cytomegalovirus and tumor stress surveillance by binding of a human γδ T cell antigen receptor to endothelial protein C receptor

Nature Immunology

Volumn 13, Issue 9, 2012, Pages 872-879

  Willcox, Carrie R ^a   Pitard, Vincent ^b,c   Netzer, Sonia ^b,c   Couzi, Lionel ^b,c,d   Salim, Mahboob ^a   Silberzahn, Tobias ^e,f   Moreau, Jean François ^b,c,d   Hayday, Adrian C ^e,f   Willcox, Benjamin E ^a   Déchanet Merville, Julie ^b,c  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b CNRS Bordeaux Segalen University   (France)

^c CNRS   (France)

^d BORDEAUX UNIVERSITY HOSPITAL   (France)

^e GUY S HOSPITAL   (United Kingdom)

^f IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; ENDOTHELIAL PROTEIN C RECEPTOR; LIPID; T LYMPHOCYTE RECEPTOR;

ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; ARTICLE; CELL STRESS; CONTROLLED STUDY; CYTOMEGALOVIRUS; ENDOTHELIUM CELL; EPITHELIUM TUMOR; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; TARGET CELL; TUMOR STRESS;

ANTIGENS, CD; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; HUMANS; IMMUNOBLOTTING; IMMUNOLOGIC SURVEILLANCE; IMMUNOPRECIPITATION; NEOPLASMS, GLANDULAR AND EPITHELIAL; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RECEPTORS, CELL SURFACE; STRESS, PHYSIOLOGICAL; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES;

EID: 84865419573     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2394     Document Type: Article

References (47)

1. Girardi, M. et al. Regulation of cutaneous malignancy by γδ T cells. Science 294, 605-609 (2001).
2. Born, W. et al. Immunoregulatory functions of γδ T cells. Adv. Immunol. 71, 77-144 (1999).
3. Ma, Y. et al. Contribution of IL-17a producing γδ T cells to the effcacy of anticancer chemotherapy. J. Exp. Med. 208, 491-503 (2011).
4. Wilhelm, M. γδ T cells for immune therapy of patients with lymphoid malignancies. Blood 102, 200-206 (2003). (Pubitemid 36759655)
5. Costa, G. et al. Control of Plasmodium falciparum erythrocytic cycle: γδ T cells target the red blood cell-invasive merozoites. Blood 118, 6952-6962 (2011).
6. Peng, G. et al. Tumor-infltrating γδ T cells suppress T and dendritic cell function via mechanisms controlled by a unique toll-like receptor signaling pathway. Immunity 27, 334-348 (2007). (Pubitemid 47284914)
7. Brandes, M., Willimann, K. & Moser, B. Professional antigen-presentation function by human γδ T Cells. Science 309, 264-268 (2005). (Pubitemid 40967855)
8. Toulon, A. et al. A role for human skin-resident T cells in wound healing. J. Exp. Med. 206, 743-750 (2009).
9. Dieli, F. et al. Targeting human γδ T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 67, 7450-7457 (2007). (Pubitemid 47206575)
10. Zarski, J. et al. Repeated administrations of IPH1101 in monotherapy or combined with low dose IL2 (2 M IU) in patients chronically infected with hepatitis C virus: effcacy, safety and immunomonitoring results from a phase 2 study. Hepatology 50, 1031A (2009).
11. Bonneville, M., O'Brien, R.L. & Born, W.K. γδ T cell effector functions: a blend of innate programming and acquired plasticity. Nat. Rev. Immunol. 10, 467-478 (2010).
12. Hayday, A.C. γδ T cells and the lymphoid stress-surveillance response. Immunity 31, 184-196 (2009).
13. Strid, J. et al. 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).
14. Adams, E.J., Chien, Y.H. & Garcia, K.C. Structure of a γδ T cell receptor in complex with the nonclassical MHC T22. Science 308, 227-231 (2005). (Pubitemid 40558852)
15. δ2 T cell receptor interactions with a surface F1-ATPase-related structure and apolipoprotein A-I. Immunity 22, 71-80 (2005). (Pubitemid 40143452)
16. Bukowski, J.F., Morita, C.T. & Brenner, M.B. Recognition and destruction of virus-infected cells by human γδ CTL. J. Immunol. 153, 5133-5140 (1994). (Pubitemid 24356144)
17. Constant, P. et al. Stimulation of human γδ T cells by nonpeptidic mycobacterial ligands. Science 264, 267-270 (1994).
18. Gober, H.J. et al. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 197, 163-168 (2003).
19. Halary, F. et al. Shared reactivity of Vdelta2-neg γδ T cells against cytomegalovirus-infected cells and tumor intestinal epithelial cells. J. Exp. Med. 201, 1567-1578 (2005). (Pubitemid 40721002)
20. + T cells obtained from patients with colon cancer respond exclusively to SEB but not to SEA. Natural Immunity 14, 188-197 (1995). (Pubitemid 26146446)
21. Spada, F.M. et al. Self-Recognition of CD1 by γδ T cells: implications for innate immunity. J. Exp. Med. 191, 937-948 (2000).
22. Groh, V., Steinle, A., Bauer, S. & Spies, T. Recognition of stress-induced MHC molecules by intestinal epithelial γδ T cells. Science 279, 1737-1740 (1998). (Pubitemid 28164472)
23. Déchanet, J. et al. Implication of γδ T cells in the human immune response to cytomegalovirus. J. Clin. Invest. 103, 1437-1449 (1999). (Pubitemid 29535500)
24. Pitard, V. et al. Long-term expansion of effector-memory Vδ2-γδ T cells is a specifc blood signature of CMV infection. Blood 112, 1317-1324 (2008).
25. Ehl, S. et al. A variant of SCID with specifc immune responses and predominance of γδ T cells. J. Clin. Invest. 115, 3140-3148 (2005). (Pubitemid 41567578)
26. Vermijlen, D. et al. Human cytomegalovirus elicits fetal γδ T cell responses in utero. J. Exp. Med. 207, 807-821 (2010).
27. δ2-negative γδ T cells during cytomegalovirus reactivation in recipients of allogeneic stem cell transplantation. Blood 116, 2164-2172 (2010).
28. Couzi, L. et al. Cytomegalovirus-induced γδ T cells associate with reduced cancer risk after kidney transplantation. J. Am. Soc. Nephrol. 21, 181-188 (2010).
29. Devaud, C. et al. Antitumor activity of γδ T cells reactive against cytomegalovirus-infected cells in a mouse xenograft tumor model. Cancer Res. 69, 3971-3978 (2009).
30. + αβ T cells responding to human cytomegalovirus infection in kidney transplant recipients. J. Infect. Dis. 200, 1415-1424 (2009).
31. Lafarge, X. et al. Expression of MHC class I receptors confers functional intraclonal heterogeneity to a reactive expansion of γδ T cells. Eur. J. Immunol. 35, 1896-1905 (2005). (Pubitemid 40862338)
32. Oganesyan, V. et al. The crystal structure of the endothelial protein C receptor and a bound phospholipid. J. Biol. Chem. 277, 24851-24854 (2002). (Pubitemid 34951783)
33. Esmon, C.T. Structure and functions of the endothelial cell protein C receptor. Crit. Care Med. 32, S298-S301 (2004).
34. Scheffer, G.L. et al. Expression of the vascular endothelial cell protein C receptor in epithelial tumor cells. Eur. J. Cancer 38, 1535-1542 (2002). (Pubitemid 34756407)
35. Tsuneyoshi, N. et al. Expression and anticoagulant function of the endothelial cell protein C receptor (EPCR) in cancer cell lines. Thromb. Haemost. 85, 356-361 (2001). (Pubitemid 32140584)
36. Cheng, T. et al. Activated protein C blocks p53-mediated apoptosis in ischemic human brain endothelium and is neuroprotective. Nat. Med. 9, 338-342 (2003). (Pubitemid 36362790)
37. Schild, H. et al. The nature of MHC recognition by γδ T cells. Cell 76, 29-37 (1994).
38. Tikhonova, A.N. et al. αβ T cell receptors that do not undergo major histocompatibility complex-specifc thymic selection possess antibody-like recognition specifcities. Immunity 36, 79-91 (2012).
39. Noriega, V., Redmann, V., Gardner, T. & Tortorella, D. Diverse immune evasion strategies by human cytomegalovirus. Immunologic Res 1-12 (2012).
40. Garrido, F., Cabrera, T. & Aptsiauri, N. "Hard" and "soft" lesions underlying the HLA class I alterations in cancer cells: Implications for immunotherapy. Int. J. Cancer 127, 249-256 (2010).
41. Chodaczek, G., Papanna, V., Zal, M.A. & Zal, T. Body-barrier surveillance by epidermal γδ TCRs. Nat. Immunol. 13, 272-282 (2012).
42. Squizzato, A., Gerdes, V.E. & Buller, H.R. Effects of human cytomegalovirus infection on the coagulation system. Thromb. Haemost. 93, 403-410 (2005). (Pubitemid 40392525)
43. Couzi, L. et al. Antibody-dependent anti-cytomegalovirus activity of human γδ T cells expressing CD16 (FcγRIIIa). Blood 119, 1418-1427 (2012).
44. - cells from mobilized peripheral blood after cytokine prestimulation. Stem Cells 21, 472-480 (2003). (Pubitemid 36793489)
45. Peterman, S.M., Dufresne, C.P. & Horning, S. The use of a hybrid linear trap-FT-ICR mass spectrometer for on-line high resolution-high mass accuracy bottom-up sequencing. J. Biomol. Tech. 16, 112-124 (2005).
46. Eng, J.K., McCormack, A.L. & Yates Iii, J.R. An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989 (1994).
47. Willcox, B.E. et al. TCR binding to peptide-MHC stabilizes a fexible recognition interface. Immunity 10, 357-365 (1999). (Pubitemid 29165290)