Radiation modulates the peptide repertoire, enhances MHC class I expression, and induces successful antitumor immunotherapy

Journal of Experimental Medicine

Volumn 203, Issue 5, 2006, Pages 1259-1271

  Reits, Eric A ^a,d   Hodge, James W ^b   Herberts, Carla A ^a   Groothuis, Tom A ^a   Chakraborty, Mala ^b   Wansley, Elizabeth K ^b   Camphausen, Kevin ^b   Luiten, Rosalie M ^a   De Ru, Arnold H ^c   Neijssen, Joost ^a   Griekspoor, Alexander ^a   Mesman, Elly ^a   Verreck, Frank A ^c   Spits, Hergen ^a,d   Schlom, Jeffrey ^b   Van Veelen, Peter ^c   Neefjes, Jacques J ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b NATIONAL CANCER INSTITUTE   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAMMALIAN TARGET OF RAPAMYCIN;

ANIMAL CELL; ANTIGEN PRESENTATION; ARTICLE; CANCER IMMUNOTHERAPY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; GAMMA IRRADIATION; IONIZING RADIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN SYNTHESIS;

ADENOCARCINOMA; ANIMALS; ANTIGEN PRESENTATION; COLONIC NEOPLASMS; DOSE-RESPONSE RELATIONSHIP, RADIATION; GAMMA RAYS; GENE EXPRESSION REGULATION, NEOPLASTIC; HLA-A2 ANTIGEN; HUMANS; IMMUNOTHERAPY; MICE; MICE, TRANSGENIC; PEPTIDES; PROTEIN BIOSYNTHESIS; PROTEIN KINASES; RADIOTHERAPY; T-LYMPHOCYTES, CYTOTOXIC;

EID: 33646704729     PISSN: 00221007     EISSN: 00221007     Source Type: Journal    
DOI: 10.1084/jem.20052494     Document Type: Article

References (51)

1. Reits, E.A., J.C. Vos, M. Gromme, and J. Neefjes. 2000. The major substrates for TAP in vivo are derived from newly synthesized proteins. Nature. 404:774-778.
2. Schubert, U., L.C. Anton, J. Gibbs, C.C. Norbury, J.W. Yewdell, and J.R. Bennink. 2000. Rapid degradation of a large fraction of newly synthesized proteins by proteasomes. Nature. 404:770-774.
3. Reits, E., J. Neijssen, C. Herberts, W. Benckhuijsen, L. Janssen, J.W. Drijfhout, and J. Neefjes. 2004. A major role for TPPII in trimming proteasomal degradation products for MHC class I antigen presentation. Immunity. 20:495-506.
4. Reits, E., A. Griekspoor, J. Neijssen, T. Groothuis, K. Jalink, P. van Veelen, H. Janssen, J. Calafat, J.W. Drijfhout, and J. Neefjes. 2003. Peptide diffusion, protection, and degradation in nuclear and cytoplasmic compartments before antigen presentation by MHC class I. Immunity. 18:97-108.
5. Yewdell, J.W. 2001. Not such a dismal science: the economics of protein synthesis, folding, degradation and antigen processing. Trends Cell Biol. 11:294-297.
6. Princiotta, M.F., D. Finzi, S.B. Qian, J. Gibbs, S. Schuchmann, F. Buttgereit, J.R. Bennink, and J.W. Yewdell. 2003. Quantitating protein synthesis, degradation, and endogenous antigen processing. Immunity. 18:343-354.
7. Yewdell, J.W., E. Reits, and J. Neefjes. 2003. Making sense of mass destruction: quantitating MHC class I antigen presentation. Nat. Rev. Immunol. 3:952-961.
8. Khanna, K.K., and S.P. Jackson. 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 27:247-254.
9. Rosen, E.M., S. Fan, I.D. Goldberg, and S. Rockwell. 2000. Biological basis of radiation sensitivity. Part 2: cellular and molecular determinants of radiosensitivity. Oncology (Huntingt) 14:741-757.
10. Bartek, J., and J. Lukas. 2001. Cell cycle. Order from destruction. Science. 294:66-67.
11. Tusher, V.G., R. Tibshirani, and G. Chu. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. USA. 98:5116-5121.
12. Schaich, K.M. 1980. Free radical initiation in proteins and amino acids by ionizing and ultraviolet radiations and lipid oxidation-part I: ionizing radiation. Crit. Rev. Food Sci. Nutr. 13:89-129.
13. Neefjes, J.J., and H.L. Ploegh. 1988. Allele and locus-specific differences in cell surface expression and the association of HLA class I heavy chain with beta 2-microglobulin: differential effects of inhibition of glycosylation on class I subunit association. Eur. J. Immunol. 18:801-810.
14. Santin, A.D., P.L. Hermonat, J.C. Hiserodt, M. Chiriva-Internati, J. Woodliff, J.W. Theus, D. Barclay, S. Pecorelli, and G.P. Parham. 1997. Effects of irradiation on the expression of major histocompatibility complex class I antigen and adhesion costimulation molecules ICAM-1 in human cervical cancer. Int J Radiat Oncol Biol Phys. 39:737-742.
15. Chakraborty, M., S.I. Abrams, K. Camphausen, K. Liu, T. Scott, C.N. Coleman, and J.W. Hodge. 2003. Irradiation of tumor cells up-regulates Fas and enhances CTL lytic activity and CTL adoptive immunotherapy. J. Immunol. 170:6338-6347.
16. Garnett, C.T., C. Palena, M. Chakraborty, K.Y. Tsang, J. Schlom, and J.W. Hodge. 2004. Sublethal irradiation of human tumor cells modulates phenotype resulting in enhanced killing by cytotoxic T lymphocytes. Cancer Res. 64:7985-7994.
17. Firat, H., F. Garcia-Pons, S. Tourdot, S. Pascolo, A. Scardino, Z. Garcia, M.L. Michel, R.W. Jack, G. Jung, K. Kosmatopoulos, et al. 1999. H-2 class I knockout, HLA-A 2.1-transgenic mice: a versatile animal model for preclinical evaluation of antitumor immunotherapeutic strategies. Eur. J. Immunol. 29:3112-3121.
18. Ahn, K., A. Gruhler, B. Galocha, T.R. Jones, E.J. Wiertz, H.L. Ploegh, P.A. Peterson, Y. Yang, and K. Fruh. 1997. The ER-luminal domain of the HCMV glycoprotein US6 inhibits peptide translocation by TAP. Immunity. 6:613-621.
19. Hengel, H., J.O. Koopmann, T. Flohr, W. Muranyi, E. Goulmy, G.J. Hammerling, U.H. Koszinowski, and F. Momburg. 1997. A viral ER-resident glycoprotein inactivates the MHC-encoded peptide transporter. Immunity. 6:623-632.
20. Sunavala-Dossabhoy, G., M. Fowler, and A. De Benedetti. 2004. Translation of the radioresistance kinase TLK1B is induced by gamma-irradiation through activation of mTOR and phosphorylation of 4E-BP 1. BMC Mol. Biol. 5:1.
21. Fingar, D.C., and J. Blenis. 2004. Target of rapamycin (TOR): an integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene. 23:3151-3171.
22. Falk, K., O. Rotzschke, M. Takiguchi, B. Grahovac, V. Gnau, S. Stevanovic, G. Jung, and H.G. Rammensee. 1994. Peptide motifs of HLA-A1, -A11, -A31, and -A33 molecules. Immunogenetics. 40:238-241.
23. Gu, L., Y. Hong, S. McCulloch, H. Watanabe, and G.M. Li. 1998. ATP-dependent interaction of human mismatch repair proteins and dual role of PCNA in mismatch repair. Nucleic Acids Res. 26:1173-1178.
24. Kozjak, V., N. Wiedemann, D. Milenkovic, C. Lohaus, H.E. Meyer, B. Guiard, C. Meisinger, and N. Pfanner. 2003. An essential role of Sam50 in the protein sorting and assembly machinery of the mitochondrial outer membrane. J. Biol. Chem. 278:48520-48523.
25. Traversari, C., P. van der Bruggen, I.F. Luescher, C. Lurquin, P. Chomez, A. Van Pel, E. De Plaen, A. Amar-Costesec, and T. Boon. 1992. A nonapeptide encoded by human gene MAGE-1 is recognized on HLA-A1 by cytolytic T lymphocytes directed against tumor antigen MZ2-E. J. Exp. Med. 176:1453-1457.
26. Yee, C., P.A. Savage, P.P. Lee, M.M. Davis, and P.D. Greenberg. 1999. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide-MHC tetramers. J. Immunol. 162:2227-2234.
27. Lee, P.P., C. Yee, P.A. Savage, L. Fong, D. Brockstedt, J.S. Weber, D. Johnson, S. Swetter, J. Thompson, P.D. Greenberg, et al. 1999. Characterization of circulating T cells specific for tumor-associated antigens in melanoma patients. Nat. Med. 5:677-685.
28. Germeau, C., W. Ma, F. Schiavetti, C. Lurquin, E. Henry, N. Vigneron, F. Brasseur, B. Lethe, E. De Plaen, T. Velu, et al. 2005. High frequency of antitumor T cells in the blood of melanoma patients before and after vaccination with tumor antigens. J. Exp. Med. 201:241-248.
29. Hareyama, M., K. Imai, T. Ban, H. Koshiba, K. Kubo, M. Shidou, A. Oouchi, and K. Morita. 1988. Effect of radiation on the expression of carcinoembryonic antigen on the membranes of human gastric adenocarcinoma cells-immunological study using monoclonal antibodies. Nippon Igaku Hoshasen Gakkai Zasshi. 48:1572-1574.
30. Ciernik, I.F., P. Romero, J.A. Berzofsky, and D.P. Carbone. 1999. Ionizing radiation enhances immunogenicity of cells expressing a tumor-specific T-cell epitope. Int J Radiat Oncol Biol Phys. 45:735-741.
31. Gaugler, M.H., C. Squiban, A. van der Meeren, J.M. Bertho, M. Vandamme, and M.A. Mouthon. 1997. Late and persistent up-regulation of intercellular adhesion molecule-1 (ICAM-1) expression by ionizing radiation in human endothelial cells in vitro. Int. J. Radiat. Biol. 72:201-209.
32. Quarmby, S., R.D. Hunter, and S. Kumar. 2000. Irradiation induced expression of CD31, ICAM-1 and VCAM-1 in human microvascular endothelial cells. Anticancer Res. 20:3375-3381.
33. Lugade, A.A., J.P. Moran, S.A. Gerber, R.C. Rose, J.G. Frelinger, and E.M. Lord. 2005. Local radiation therapy of B16 melanoma tumors increases the generation of tumor antigen-specific effector cells that traffic to the tumor. J. Immunol. 174:7516-7523.
34. Ganss, R., E. Ryschich, E. Klar, B. Arnold, and G.J. Hammerling. 2002. Combination of T-cell therapy and trigger of inflammation induces remodeling of the vasculature and tumor eradication. Cancer Res. 62:1462-1470.
35. Nobler, M.P. 1969. The abscopal effect in malignant lymphoma and its relationship to lymphocyte circulation. Radiology. 93:410-412.
36. Demaria, S., B. Ng, M.L. Devitt, J.S. Babb, N. Kawashima, L. Liebes, and S.C. Formenti. 2004. Ionizing radiation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Int J Radiat Oncol Biol Phys. 58:862-870.
37. Neefjes, J.J., G.J. Hammerling, and F. Momburg. 1993. Folding and assembly of major histocompatibility complex class I heterodimers in the endoplasmic reticulum of intact cells precedes the binding of peptide. J. Exp. Med. 178:1971-1980.
38. Chakraborty, M., S.I. Abrams, C.N. Coleman, K. Camphausen, J. Schlom, and J.W. Hodge. 2004. External beam radiation of tumors alters phenotype of tumor cells to render them susceptible to vaccine-mediated T-cell killing. Cancer Res. 64:4328-4337.
39. Gromme, M., F.G. Uytdehaag, H. Janssen, J. Calafat, R.S. van Binnendijk, M.J. Kenter, A. Tulp, D. Verwoerd, and J. Neefjes. 1999. Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. USA. 96:10326-10331.
40. van Ham, M., M. van Lith, B. Lillemeier, E. Tjin, U. Gruneberg, D. Rahman, L. Pastoors, K. van Meijgaarden, C. Roucard, J. Trowsdale, et al. 2000. Modulation of the major histocompatibility complex class II-associated peptide repertoire by human histocompatibility leukocyte antigen (HLA)-DO. J. Exp. Med. 191:1127-1136.
41. Robbins, P.F., J.A. Kantor, M. Salgaller, P.H. Hand, P.D. Fernsten, and J. Schlom. 1991. Transduction and expression of the human carcinoembryonic antigen gene in a murine colon carcinoma cell line. Cancer Res. 51:3657-3662.
42. Kudo-Saito, C., J. Schlom, and J.W. Hodge. 2005. Induction of an antigen cascade by diversified subcutaneous/intratumoral vaccination is associated with antitumor responses. Clin. Cancer Res. 11:2416-2426.
43. Yang, J.C., and D. Perry-Lalley. 2000. The envelope protein of an endogenous murine retrovirus is a tumor-associated T-cell antigen for multiple murine tumors. J. Immunother. 23:177-183.
44. van de Rijn, M., A.H. Geurts van Kessel, V. Kroezen, A.J. van Agthoven, K. Verstijnen, C. Terhorst, and J. Hilgers. 1983. Localization of a gene controlling the expression of the human transferrin receptor to the region q12 leads to qter of chromosome 3. Cytogenet. Cell Genet. 36:525-531.
45. Parham, P., C.J. Barnstable, and W.F. Bodmer. 1979. Use of a monoclonal antibody (W6/32) in structural studies of HLA-A,B,C, antigens. J. Immunol. 123:342-349.
46. Neefjes, J.J., V. Stollorz, P.J. Peters, H.J. Geuze, and H.L. Ploegh. 1990. The biosynthetic pathway of MHC class II but not class I molecules intersects the endocytic route. Cell. 61:171-183.
47. Kruse, J.J., J.A. te Poele, A. Velds, R.M. Kerkhoven, L.J. Boersma, N.S. Russell, and F.A. Stewart. 2004. Identification of differentially expressed genes in mouse kidney after irradiation using microarray analysis. Radiat. Res. 161:28-38.
48. de Bueger, M., F. Verreck, E. Blokland, J.W. Drijfhout, R. Amons, F. Koning, and E. Goulmy. 1993. Isolation of an HLA-A 2.1 extracted human minor histocompatibility peptide. Eur. J. Immunol. 23:614-618.
49. Beekman, N.J., P.A. van Veelen, T. van Hall, A. Neisig, A. Sijts, M. Camps, P.M. Kloetzel, J.J. Neefjes, C.J. Melief, and F. Ossendorp. 2000. Abrogation of CTL epitope processing by single amino acid substitution flanking the C-terminal proteasome cleavage site. J. Immunol. 164:1898-1905.
50. Mann, M., and M. Wilm. 1994. Error-tolerant identification of peptides in sequence databases by peptide sequence tags. Anal. Chem. 66:4390-4399.
51. Altman, J.D., P.A. Moss, P.J. Goulder, D.H. Barouch, M.G. McHeyzer-Williams, J.I. Bell, A.J. McMichael, and M.M. Davis. 1996. Phenotypic analysis of antigen-specific T lymphocytes. Science. 274:94-96.