Sustained tumour eradication after induced caspase-3 activation and synchronous tumour apoptosis requires an intact host immune response

Cell Death and Differentiation

Volumn 20, Issue 5, 2013, Pages 765-773

  Melis, M H M ^a   Simpson, K L ^a   Dovedi, S J ^a   Welman, A ^a   MacFarlane, M ^b   Dive, C ^a   Honeychurch, J ^a   Illidge, T M ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

apoptosis; cancer; immunogenicity

Indexed keywords

CASPASE 3; HEAT SHOCK PROTEIN 90; HIGH MOBILITY GROUP B1 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CANCER CELL DESTRUCTION; CANCER RECURRENCE; CANCER REGRESSION; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DENDRITIC CELL; ENZYME ACTIVATION; FEMALE; FLOW CYTOMETRY; HOST RESISTANCE; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DEPLETION; MELANOMA B16; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; TUMOR IMMUNITY;

ANIMALS; ANTI-BACTERIAL AGENTS; APOPTOSIS; CASPASE 3; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; DOXYCYCLINE; ENZYME ACTIVATION; FEMALE; HMGB1 PROTEIN; HSP90 HEAT-SHOCK PROTEINS; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; PHAGOCYTOSIS;

MURINAE; MUS;

EID: 84877581869     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.8     Document Type: Article

References (41)

1. Savill J, Fadok V. Corpse clearance defines the meaning of cell death. Nature 2000; 407: 784-788.
2. Matzinger P. Tolerance, danger, and the extended family. Annu Rev Immunol 1994; 12: 991-1045.
3. Rock KL, Lai JJ, Kono H. Innate and adaptive immune responses to cell death. Immunol Rev 2011; 243: 191-205.
4. Shi Y, Evans JE, Rock KL. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003; 425: 516-521.
5. Quintana FJ, Cohen IR. Heat shock proteins as endogenous adjuvants in sterile and septic inflammation. J Immunol 2005; 175: 2777-2782.
6. Zhang Q, Raoof M, Chen Y, Sumi Y, Sursal T, Junger W et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature 2010; 464: 104-107.
7. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012; 19: 107-120.
8. Okada H, Mak TW. Pathways of apoptotic and non-apoptotic death in tumour cells. Nat Rev Cancer 2004; 4: 592-603.
9. Michaud M, Martins I, Sukkurwala AQ, Adjemian S, Ma Y, Pellegatti P et al. Autophagydependent anticancer immune responses induced by chemotherapeutic agents in mice. Science 2011; 334: 1573-1577.
10. Ghiringhelli F, Apetoh L, Tesniere A, Aymeric L, Ma Y, Ortiz C et al. Activation of the NLRP3 inflammasome in dendritic cells induces IL-1beta-dependent adaptive immunity against tumors. Nat Med 2009; 15: 1170-1178.
11. Kepp O, Tesniere A, Schlemmer F, Michaud M, Senovilla L, Zitvogel L et al. Immunogenic cell death modalities and their impact on cancer treatment. Apoptosis 2009; 14: 364-375.
12. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13: 54-61.
13. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13: 1050-1059.
14. Obeid M, Panaretakis T, Joza N, Tufi R, Tesniere A, van Endert P et al. Calreticulin exposure is required for the immunogenicity of gamma-irradiation and UVC light-induced apoptosis. Cell Death Differ 2007; 14:1848-1850.
15. Casares N, Pequignot MO, Tesniere A, Ghiringhelli F, Roux S, Chaput N et al. Caspasedependent immunogenicity of doxorubicin-induced tumor cell death. J Exp Med 2005; 202: 1691-1701.
16. Welman A, Barraclough J, Dive C. Generation of cells expressing improved doxycyclineregulated reverse transcriptional transactivator rtTA2S-M2. Nat Protoc 2006; 1: 803-811.
17. Srinivasula SM, Ahmad M, MacFarlane M, Luo Z, Huang Z, Fernandes-Alnemri T et al. Generation of constitutively active recombinant caspases-3 and-6 by rearrangement of their subunits. J Biol Chem 1998; 273: 10107-10111.
18. Panaretakis T, Kepp O, Brockmeier U, Tesniere A, Bjorklund AC, Chapman DC et al. Mechanisms of pre-apoptotic calreticulin exposure in immunogenic cell death. EMBO J 2009; 28: 578-590.
19. Earnshaw WC, Martins LM, Kaufmann SH. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu Rev Biochem 1999; 68: 383-424.
20. MacCorkle RA, Freeman KW, Spencer DM. Synthetic activation of caspases: artificial death switches. Proc Natl Acad Sci USA 1998; 95: 3655-3660.
21. Scaffidi P, Misteli T, Bianchi ME. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002; 418: 191-195.
22. Basu S, Binder RJ, Suto R, Anderson KM, Srivastava PK. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-kappa B pathway. Int Immunol 2000; 12: 1539-1546.
23. Bell CW, Jiang W, Reich CF 3rd, Pisetsky DS. The extracellular release of HMGB1 during apoptotic cell death. Am J Physiol Cell Physiol 2006; 291: C1318-C1325.
24. Martins I, Tesniere A, Kepp O, Michaud M, Schlemmer F, Senovilla L et al. Chemotherapy induces ATP release from tumor cells. Cell Cycle 2009; 8: 3723-3728.
25. Choi JJ, Reich CF 3rd, Pisetsky DS. Release of DNA from dead and dying lymphocyte and monocyte cell lines in vitro. Scand J Immunol 2004; 60: 159-166.
26. Kazama H, Ricci JE, Herndon JM, Hoppe G, Green DR, Ferguson TA. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 2008; 29: 21-32.
27. Hoppe G, Talcott KE, Bhattacharya SK, Crabb JW, Sears JE. Molecular basis for the redox control of nuclear transport of the structural chromatin protein Hmgb1. Exp Cell Res 2006; 312: 3526-3538.
28. Bonaldi T, Talamo F, Scaffidi P, Ferrera D, Porto A, Bachi A et al. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J 2003; 22: 5551-5560.
29. Thorburn J, Horita H, Redzic J, Hansen K, Frankel AE, Thorburn A. Autophagy regulates selective HMGB1 release in tumor cells that are destined to die. Cell Death Differ 2009; 16: 175-183.
30. Scheffer SR, Nave H, Korangy F, Schlote K, Pabst R, Jaffee EM et al. Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo. Int J Cancer 2003; 103: 205-211.
31. Ronchetti A, Rovere P, Iezzi G, Galati G, Heltai S, Protti MP et al. Immunogenicity of apoptotic cells in vivo: role of antigen load, antigen-presenting cells, and cytokines. J Immunol 1999; 163: 130-136.
32. Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med 2000; 191: 423-434.
33. Zou W. Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer 2005; 5: 263-274.
34. Gregory CD, Devitt A. The macrophage and the apoptotic cell: an innate immune interaction viewed simplistically? Immunology 2004; 113: 1-14.
35. Rovere P, Sabbadini MG, Vallinoto C, Fascio U, Zimmermann VS, Bondanza A et al. Delayed clearance of apoptotic lymphoma cells allows cross-presentation of intracellular antigens by mature dendritic cells. J Leukoc Biol 1999; 66: 345-349.
36. Patel VA, Longacre A, Hsiao K, Fan H, Meng F, Mitchell JE et al. Apoptotic cells, at all stages of the death process, trigger characteristic signaling events that are divergent from and dominant over those triggered by necrotic cells: implications for the delayed clearance model of autoimmunity. J Biol Chem 2006; 281: 4663-4670.
37. van Rooijen N, van Kesteren-Hendrikx E. "In vivo depletion of macrophages by liposomemediated "suicide". Methods Enzymol 2003; 373: 3-16.
38. Jung S, Unutmaz D, Wong P, Sano G, De los Santos K, Sparwasser T et al. In vivo depletion of CD11c\+ dendritic cells abrogates priming of CD8\+ T cells by exogenous cell-associated antigens. Immunity 2002; 17: 211-220.
39. Vile RG, Castleden S, Marshall J, Camplejohn R, Upton C, Chong H. Generation of an anti-tumour immune response in a non-immunogenic tumour: HSVtk killing in vivo stimulates a mononuclear cell infiltrate and a Th1-like profile of intratumoural cytokine expression. Int J Cancer 1997; 71: 267-274.
40. Lohmann C, Muschaweckh A, Kirschnek S, Jennen L, Wagner H, Hacker G. Induction of tumor cell apoptosis or necrosis by conditional expression of cell death proteins: analysis of cell death pathways and in vitro immune stimulatory potential. J Immunol 2009; 182: 4538-4546.
41. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, Romani N et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 1999; 223: 77-92.