Immunogenic cancer cell death: a key-lock paradigm

Current Opinion in Immunology

Volumn 20, Issue 5, 2008, Pages 504-511

  Tesniere, Antoine ^a,b,c   Apetoh, Lionel ^a,b,c   Ghiringhelli, Francois ^a,b,c   Joza, Nicholas ^a,b,c   Panaretakis, Theocharis ^a,b,c   Kepp, Oliver ^a,b,c   Schlemmer, Frederic ^a,b,c   Zitvogel, Laurence ^a,b,c   Kroemer, Guido ^a,b,c  

^a INSERM   (France)

^b INSTITUT GUSTAVE ROUSSY   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACYCLINE DERIVATIVE; B7 ANTIGEN; CALRETICULIN; CD4 ANTIGEN; CD40 ANTIGEN; CD40 LIGAND; CD8 ANTIGEN; CD83 ANTIGEN; CHAPERONE; COMPLEMENT COMPONENT C1Q; FAS LIGAND; GLYCOPROTEIN P 15095; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; HIGH MOBILITY GROUP B1 PROTEIN; INITIATION FACTOR 2ALPHA; INTERCELLULAR ADHESION MOLECULE 1; LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 3; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELOID DIFFERENTIATION FACTOR 88; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN P57; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNINDEXED DRUG;

ANTIGEN PRESENTATION; AUTOIMMUNITY; CANCER CELL; CANCER CHEMOTHERAPY; CANCER RADIOTHERAPY; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL MATURATION; CELL SURFACE; DENDRITIC CELL; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; ANTIGENS, NEOPLASM; APOPTOSIS; CALRETICULIN; DENDRITIC CELLS; HEAT-SHOCK PROTEINS; HMGB1 PROTEIN; HUMANS; LYMPHOCYTE ACTIVATION; MICE; NEOPLASMS; T-LYMPHOCYTES; TOLL-LIKE RECEPTOR 4;

EID: 50549102898     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2008.05.007     Document Type: Review

References (47)

1. Galluzzi L., Maiuri M.C., Vitale I., Zischka H., Castedo M., Zitvogel L., and Kroemer G. Cell death modalities: classification and pathophysiological implications. Cell Death Differ 14 (2007) 1237-1243
2. Kroemer G., El-Deiry W.S., Golstein P., Peter M.E., Vaux D., Vandenabeele P., Zhivotovsky B., Blagosklonny M.V., Malorni W., Knight R.A., et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death. Cell Death Differ 12 Suppl. 2 (2005) 1463-1467
3. Savill J., Dransfield I., Gregory C., and Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2 (2002) 965-975
4. Hengartner M.O. The biochemistry of apoptosis. Nature 407 (2000) 770-776
5. Zitvogel L., Casares N., Pequignot M.O., Chaput N., Albert M.L., and Kroemer G. Immune response against dying tumor cells. Adv Immunol 84 (2004) 131-179
6. Kroemer G., and Martin S.J. Caspase-independent cell death. Nat Med 11 (2005) 725-730
7. Casares N., Pequignot M.O., Tesniere A., Ghiringhelli F., Roux S., Chaput N., Schmitt E., Hamai A., Hervas-Stubbs S., Obeid M., et al. Caspase-dependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 202 (2005) 1691-1701
8. Obeid M., Tesniere A., Ghiringhelli F., Fimia G.M., Apetoh L., Perfettini J.L., Castedo M., Mignot G., Panaretakis T., Casares N., et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 13 (2007) 54-61
9. Obeid M., Panaretakis T., Joza N., Tufi R., Tesniere A., van Endert P., Zitvogel L., and Kroemer G. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ 14 (2007) 1848-1850
10. Obeid M., Tesniere A., Panaretakis T., Tufi R., Joza N., van Endert P., Ghiringhelli F., Apetoh L., Chaput N., Flament C., et al. Ecto-calreticulin in immunogenic chemotherapy. Immunol Rev 220 (2007) 22-34
11. Panaretakis T., Joza N., Modjtahedi N., Tesniere A., Vitale I., Durchschlag M., Fimia G.M., Kepp O., Piacentini M., Froehlich K.U., van Endert P., Zitvogel L., Madeo F., and Kroemer G. The co-translocation of ERp57 and calreticulin determines the immunogenicity of cell death. Cell Death Differ (2008)
12. Gardai S.J., McPhillips K.A., Frasch S.C., Janssen W.J., Starefeldt A., Murphy-Ullrich J.E., Bratton D.L., Oldenborg P.A., Michalak M., and Henson P.M. Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123 (2005) 321-334
13. Franz S., Herrmann K., Fuhrnrohr B., Sheriff A., Frey B., Gaipl U.S., Voll R.E., Kalden J.R., Jack H.M., and Herrmann M. After shrinkage apoptotic cells expose internal membrane-derived epitopes on their plasma membranes. Cell Death Differ 14 (2007) 733-742
14. Tufi R., Panaretakis T., Bianchi K., Criollo A., Fazi B., Di Sano F., Tesniere A., Kepp O., Paterlini-Brechot P., Zitvogel L., et al. Reduction of endoplasmic reticulum Ca(2+) levels favors plasma membrane surface exposure of calreticulin. Cell Death Differ 15 (2008) 274-282
15. Hayashi E., Matsuzaki Y., Hasegawa G., Yaguchi T., Kurihara S., Fujita T., Kageshita T., Sano M., and Kawakami Y. Identification of a novel cancer-testis antigen CRT2 frequently expressed in various cancers using representational differential analysis. Clin Cancer Res 13 (2007) 6267-6274
16. Saito K., Dai Y., and Ohtsuka K. Enhanced expression of heat shock proteins in gradually dying cells and their release from necrotically dead cells. Exp Cell Res 310 (2005) 229-236
17. Spisek R., Charalambous A., Mazumder A., Vesole D.H., Jagannath S., and Dhodapkar M.V. Bortezomib enhances dendritic cell (DC)-mediated induction of immunity to human myeloma via exposure of cell surface heat shock protein 90 on dying tumor cells: therapeutic implications. Blood 109 (2007) 4839-4845
18. Mukhopadhaya A., Mendecki J., Dong X., Liu L., Kalnicki S., Garg M., Alfieri A., and Guha C. Localized hyperthermia combined with intratumoral dendritic cells induces systemic antitumor immunity. Cancer Res 67 (2007) 7798-7806
19. Chan T., Chen Z., Hao S., Xu S., Yuan J., Saxena A., Qureshi M., Zheng C., and Xiang J. Enhanced T-cell immunity induced by dendritic cells with phagocytosis of heat shock protein 70 gene-transfected tumor cells in early phase of apoptosis. Cancer Gene Ther 14 (2007) 409-420
20. Wang X.Y., Arnouk H., Chen X., Kazim L., Repasky E.A., and Subjeck J.R. Extracellular targeting of endoplasmic reticulum chaperone glucose-regulated protein 170 enhances tumor immunity to a poorly immunogenic melanoma. J Immunol 177 (2006) 1543-1551
21. Srivastava P.K. Immunotherapy for human cancer using heat shock protein-peptide complexes. Curr Oncol Rep 7 (2005) 104-108
22. Scaffidi P., Misteli T., and Bianchi M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418 (2002) 191-195
23. Bell C.W., Jiang W., Reich III C.F., and Pisetsky D.S. The extracellular release of HMGB1 during apoptotic cell death. Am J Physiol Cell Physiol 291 (2006) C1318-C1325
24. Ditsworth D., Zong W.X., and Thompson C.B. Activation of poly(ADP)-ribose polymerase (PARP-1) induces release of the pro-inflammatory mediator HMGB1 from the nucleus. J Biol Chem 282 (2007) 17845-17854
25. Apetoh L., Ghiringhelli F., Tesniere A., Obeid M., Ortiz C., Criollo A., Mignot G., Maiuri M.C., Ullrich E., Saulnier P., et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 13 (2007) 1050-1059
26. Savill J., and Fadok V. Corpse clearance defines the meaning of cell death. Nature 407 (2000) 784-788
27. Ogden C.A., deCathelineau A., Hoffmann P.R., Bratton D., Ghebrehiwet B., Fadok V.A., and Henson P.M. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 194 (2001) 781-795
28. Berwin B., Delneste Y., Lovingood R.V., Post S.R., and Pizzo S.V. SREC-I, a type F scavenger receptor, is an endocytic receptor for calreticulin. J Biol Chem 279 (2004) 51250-51257
29. Duus K., Pagh R.T., Holmskov U., Hojrup P., Skov S., and Houen G. Interaction of calreticulin with CD40 ligand, TRAIL and Fas ligand. Scand J Immunol 66 (2007) 501-507
30. Wang X.Y., Facciponte J., Chen X., Subjeck J.R., and Repasky E.A. Scavenger receptor-A negatively regulates antitumor immunity. Cancer Res 67 (2007) 4996-5002
31. Dumitriu I.E., Baruah P., Bianchi M.E., Manfredi A.A., and Rovere-Querini P. Requirement of HMGB1 and RAGE for the maturation of human plasmacytoid dendritic cells. Eur J Immunol 35 (2005) 2184-2190
32. Kokkola R., Andersson A., Mullins G., Ostberg T., Treutiger C.J., Arnold B., Nawroth P., Andersson U., Harris R.A., and Harris H.E. RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand J Immunol 61 (2005) 1-9
33. Chen C.J., Kono H., Golenbock D., Reed G., Akira S., and Rock K.L. Identification of a key pathway required for the sterile inflammatory response triggered by dying cells. Nat Med 13 (2007) 851-856
34. Park J.S., Gamboni-Robertson F., He Q., Svetkauskaite D., Kim J.Y., Strassheim D., Sohn J.W., Yamada S., Maruyama I., Banerjee A., et al. High mobility group box 1 protein interacts with multiple Toll-like receptors. Am J Physiol Cell Physiol 290 (2006) C917-C924
35. Apetoh L., Ghiringhelli F., Tesniere A., Criollo A., Ortiz C., Lidereau R., Mariette C., Chaput N., Mira J.P., Delaloge S., et al. The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy. Immunol Rev 220 (2007) 47-59
36. Shiratsuchi A., Watanabe I., Takeuchi O., Akira S., and Nakanishi Y. Inhibitory effect of Toll-like receptor 4 on fusion between phagosomes and endosomes/lysosomes in macrophages. J Immunol 172 (2004) 2039-2047
37. Bak S.P., Amiel E., Walters J.J., and Berwin B. Calreticulin requires an ancillary adjuvant for the induction of efficient cytotoxic T cell responses. Mol Immunol 45 (2008) 1414-1423
38. Messmer D., Yang H., Telusma G., Knoll F., Li J., Messmer B., Tracey K.J., and Chiorazzi N. High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J Immunol 173 (2004) 307-313
39. Tian J., Avalos A.M., Mao S.Y., Chen B., Senthil K., Wu H., Parroche P., Drabic S., Golenbock D., Sirois C., et al. Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8 (2007) 487-496
40. Dumitriu I.E., Baruah P., Valentinis B., Voll R.E., Herrmann M., Nawroth P.P., Arnold B., Bianchi M.E., Manfredi A.A., and Rovere-Querini P. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J Immunol 174 (2005) 7506-7515
41. Massa C., Melani C., and Colombo M.P. Chaperon and adjuvant activity of hsp70: different natural killer requirement for cross-priming of chaperoned and bystander antigens. Cancer Res 65 (2005) 7942-7949
42. Baker-LePain J.C., Sarzotti M., and Nicchitta C.V. Glucose-regulated protein 94/glycoprotein 96 elicits bystander activation of CD4+ T cell Th1 cytokine production in vivo. J Immunol 172 (2004) 4195-4203
43. Endo Y., Sakai R., Ouchi M., Onimatsu H., Hioki M., Kagawa S., Uno F., Watanabe Y., Urata Y., Tanaka N., et al. Virus-mediated oncolysis induces danger signal and stimulates cytotoxic T-lymphocyte activity via proteasome activator upregulation. Oncogene (2007)
44. Gasser S., Orsulic S., Brown E.J., and Raulet D.H. The DNA damage pathway regulates innate immune system ligands of the NKG2D receptor. Nature 436 (2005) 1186-1190
45. Unni A.M., Bondar T., and Medzhitov R. Intrinsic sensor of oncogenic transformation induces a signal for innate immunosurveillance. Proc Natl Acad Sci U S A 105 (2008) 1686-1691
46. Xue W., Zender L., Miething C., Dickins R.A., Hernando E., Krizhanovsky V., Cordon-Cardo C., and Lowe S.W. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445 (2007) 656-660
47. Zitvogel L., Apetoh L., Ghiringhelli F., André F., Tesniere A., and Kroemer G. The anticancer immune response: indispensable for therapeutic success?. J Clin Invest 118 6 (2008) 1991-2001