DNA alkylating therapy induces tumor regression through an HMGB1-mediated activation of innate immunity

Journal of Immunology

Volumn 186, Issue 6, 2011, Pages 3517-3526

  Guerriero, Jennifer L ^a,c   Ditsworth, Dara ^b,d   Catanzaro, Joseph M ^a   Sabino, Gregory ^a   Furie, Martha B ^a   Kew, Richard R ^a   Crawford, Howard C ^a   Zong, Wei Xing ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATING AGENT; C 0768; CYCLOPHOSPHAMIDE; HIGH MOBILITY GROUP B1 PROTEIN; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CONTROLLED STUDY; IMMUNOCOMPETENT CELL; IMMUNOSTIMULATION; IMMUNOSUPPRESSIVE TREATMENT; INNATE IMMUNITY; MACROPHAGE; MALE; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; TUMOR; TUMOR REGRESSION;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; CELL LINE, TRANSFORMED; CELL LINE, TUMOR; CELLS, CULTURED; DRUG RESISTANCE, NEOPLASM; HEK293 CELLS; HMGB1 PROTEIN; HUMANS; IMMUNITY, INNATE; MALE; MICE; MICE, NUDE; NECROSIS; NEOPLASMS, EXPERIMENTAL; RANDOM ALLOCATION;

EID: 79953188695     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1003267     Document Type: Article

References (56)

1. Brown, J. M., and L. D. Attardi. 2005. The role of apoptosis in cancer development and treatment response. Nat. Rev. Cancer 5: 231-237.
2. Havelka, A. M., M. Berndtsson, M. H. Olofsson, M. C. Shoshan, and S. Linder. 2007. Mechanisms of action of DNA-damaging anticancer drugs in treatment of carcinomas: is acute apoptosis an "off-target" effect? Mini Rev. Med. Chem. 7: 1035-1039.
3. Melino, G., R. A. Knight, and P. Nicotera. 2005. How many ways to die? How many different models of cell death? Cell Death Differ. 12(Suppl. 2): 1457-1462.
4. Okada, H., and T. W. Mak. 2004. Pathways of apoptotic and non-apoptotic death in tumour cells. Nat. Rev. Cancer 4: 592-603.
5. Bacci, G., M. Mercuri, A. Longhi, S. Ferrari, F. Bertoni, M. Versari, and P. Picci. 2005. Grade of chemotherapy-induced necrosis as a predictor of local and systemic control in 881 patients with non-metastatic osteosarcoma of the extremities treated with neoadjuvant chemotherapy in a single institution. Eur. J. Cancer 41: 2079-2085. (Pubitemid 41337949)
6. Delanian, S., and J. L. Lefaix. 2007. Current management for late normal tissue injury: radiation-induced fibrosis and necrosis. Semin. Radiat. Oncol. 17: 99-107.
7. Linder, S., A. M. Havelka, T. Ueno, and M. C. Shoshan. 2004. Determining tumor apoptosis and necrosis in patient serum using cytokeratin 18 as a biomarker. Cancer Lett. 214: 1-9.
8. Raymond, A. K., S. P. Chawla, C. H. Carrasco, A. G. Ayala, C. V. Fanning, B. Grice, T. Armen, C. Plager, N. E. Papadopoulos, J. Edeiken, et al. 1987. Osteosarcoma chemotherapy effect: a prognostic factor. Semin. Diagn. Pathol. 4: 212-236.
9. Guerriero, J. L., D. Ditsworth, Y. Fan, F. Zhao, H. C. Crawford, and W. X. Zong. 2008. Chemotherapy induces tumor clearance independent of apoptosis. Cancer Res. 68: 9595-9600.
10. Zong, W. X., D. Ditsworth, D. E. Bauer, Z. Q. Wang, and C. B. Thompson. 2004. Alkylating DNA damage stimulates a regulated form of necrotic cell death. Genes Dev. 18: 1272-1282.
11. Lauber, K., S. G. Blumenthal, M. Waibel, and S. Wesselborg. 2004. Clearance of apoptotic cells: getting rid of the corpses. Mol. Cell 14: 277-287. (Pubitemid 38607340)
12. Nagata, S., R. Hanayama, and K. Kawane. 2010. Autoimmunity and the clearance of dead cells. Cell 140: 619-630.
13. Fadok, V. A., D. L. Bratton, D. M. Rose, A. Pearson, R. A. Ezekewitz, and P. M. Henson. 2000. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405: 85-90.
14. Golstein, P., and G. Kroemer. 2007. Cell death by necrosis: towards a molecular definition. Trends Biochem. Sci. 32: 37-43.
15. Zong, W. X., and C. B. Thompson. 2006. Necrotic death as a cell fate. Genes Dev. 20: 1-15.
16. Bianchi, M. E., and A. A. Manfredi. 2007. High-mobility group box 1 (HMGB1) protein at the crossroads between innate and adaptive immunity. Immunol. Rev. 220: 35-46.
17. Ellerman, J. E., C. K. Brown, M. de Vera, H. J. Zeh, T. Billiar, A. Rubartelli, and M. T. Lotze. 2007. Masquerader: high mobility group box-1 and cancer. Clin. Cancer Res. 13: 2836-2848.
18. Scaffidi, P., T. Misteli, and M. E. Bianchi. 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418: 191-195.
19. Andersson, U. G., and K. J. Tracey. 2004. HMGB1, a pro-inflammatory cytokine of clinical interest: introduction. J. Intern. Med. 255: 318-319.
20. Palumbo, R., and M. E. Bianchi. 2004. High mobility group box 1 protein, a cue for stem cell recruitment. Biochem. Pharmacol. 68: 1165-1170.
21. Sims, G. P., D. C. Rowe, S. T. Rietdijk, R. Herbst, and A. J. Coyle. 2010. HMGB1 and RAGE in inflammation and cancer. Annu. Rev. Immunol. 28: 367-388.
22. Tang, D., R. Kang, H. J. Zeh, III, and M. T. Lotze. 2010. High-mobility group box 1 and cancer. Biochim. Biophys. Acta 1799: 131-140.
23. Taguchi, A., D. C. Blood, G. del Toro, A. Canet, D. C. Lee, W. Qu, N. Tanji, Y. Lu, E. Lalla, C. Fu, et al. 2000. Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 405: 354-360. (Pubitemid 30337069)
24. Tang, D., R. Kang, K. M. Livesey, C. W. Cheh, A. Farkas, P. Loughran, G. Hoppe, M. E. Bianchi, K. J. Tracey, H. J. Zeh, III, and M. T. Lotze. 2010. Endogenous HMGB1 regulates autophagy. J. Cell Biol. 190: 881-892.
25. Liu, L., M. Yang, R. Kang, Z. Wang, Y. Zhao, Y. Yu, M. Xie, X. Yin, K. M. Livesey, M. T. Lotze, et al 2011. HMGB1-induced autophagy promotes chemotherapy resistance in leukemia cells. Leukemia 25: 23-31.
26. Apetoh, L., F. Ghiringhelli, A. Tesniere, M. Obeid, C. Ortiz, A. Criollo, G. Mignot, M. C. Maiuri, E. Ullrich, P. Saulnier, et al. 2007. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat. Med. 13: 1050-1059.
27. Rovere-Querini, P., A. Capobianco, P. Scaffidi, B. Valentinis, F. Catalanotti, M. Giazzon, I. E. Dumitriu, S. Müller, M. Iannacone, C. Traversari, et al. 2004. HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 5: 825-830. (Pubitemid 39199174)
28. Curtin, J. F., N. Liu, M. Candolfi, W. Xiong, H. Assi, K. Yagiz, M. R. Edwards, K. S. Michelsen, K. M. Kroeger, C. Liu, et al. 2009. HMGB1 mediates endogenous TLR2 activation and brain tumor regression. PLoS Med. 6: e10.
29. Kazama, H., J. E. Ricci, J. M. Herndon, G. Hoppe, D. R. Green, and T. A. Ferguson. 2008. Induction of immunological tolerance by apoptotic cells requires caspase-dependent oxidation of high-mobility group box-1 protein. Immunity 29: 21-32.
30. Tang, D., R. Kang, C. W. Cheh, K. M. Livesey, X. Liang, N. E. Schapiro, R. Benschop, L. J. Sparvero, A. A. Amoscato, K. J. Tracey, et al. 2010. HMGB1 release and redox regulates autophagy and apoptosis in cancer cells. Oncogene 29: 5299-5310.
31. Coussens, L. M., and Z. Werb. 2002. Inflammation and cancer. Nature 420: 860-867. (Pubitemid 36019639)
32. Zitvogel, L., L. Apetoh, F. Ghiringhelli, and G. Kroemer. 2008. Immunological aspects of cancer chemotherapy. Nat. Rev. Immunol. 8: 59-73.
33. Vakkila, J., and M. T. Lotze. 2004. Inflammation and necrosis promote tumour growth. Nat. Rev. Immunol. 4: 641-648.
34. Degenhardt, K., R. Mathew, B. Beaudoin, K. Bray, D. Anderson, G. Chen, C. Mukherjee, Y. Shi, C. Gélinas, Y. Fan, et al. 2006. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64.
35. Xue, W., L. Zender, C. Miething, R. A. Dickins, E. Hernando, V. Krizhanovsky, C. Cordon-Cardo, and S. W. Lowe. 2007. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445: 656-660.
36. Zong, W. X., T. Lindsten, A. J. Ross, G. R. MacGregor, and C. B. Thompson. 2001. BH3-only proteins that bind pro-survival Bcl-2 family members fail to induce apoptosis in the absence of Bax and Bak. Genes Dev. 15: 1481-1486.
37. Ditsworth, D., W. X. Zong, and C. B. Thompson. 2007. Activation of poly (ADP)-ribose polymerase (PARP-1) induces release of the pro-inflammatory mediator HMGB1 from the nucleus. J. Biol. Chem. 282: 17845-17854.
38. Wang, H., O. Bloom, M. Zhang, J. M. Vishnubhakat, M. Ombrellino, J. Che, A. Frazier, H. Yang, S. Ivanova, L. Borovikova, et al. 1999. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285: 248-251. (Pubitemid 29329996)
39. Yang, H., M. Ochani, J. Li, X. Qiang, M. Tanovic, H. E. Harris, S. M. Susarla, L. Ulloa, H. Wang, R. DiRaimo, et al. 2004. Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl. Acad. Sci. USA 101: 296-301.
40. Calogero, S., F. Grassi, A. Aguzzi, T. Voigtländer, P. Ferrier, S. Ferrari, and M. E. Bianchi. 1999. The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat. Genet. 22: 276-280.
41. Lotze, M. T., and K. J. Tracey. 2005. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 5: 331-342.
42. Völp, K., M. L. Brezniceanu, S. Bösser, T. Brabletz, T. Kirchner, D. Göttel, S. Joos, and M. Zörnig. 2006. Increased expression of high mobility group box 1 (HMGB1) is associated with an elevated level of the antiapoptotic c-IAP2 protein in human colon carcinomas. Gut 55: 234-242. (Pubitemid 43117284)
43. Hattori, K., K. Shimizu, M. Takahashi, M. Tamura, M. Oheda, N. Ohsawa, and M. Ono. 1990. Quantitative in vivo assay of human granulocyte colony-stimulating factor using cyclophosphamide-induced neutropenic mice. Blood 75: 1228-1233. (Pubitemid 20107287)
44. Chowdhury, D., and J. Lieberman. 2008. Death by a thousand cuts: granzyme pathways of programmed cell death. Annu. Rev. Immunol. 26: 389-420.
45. MacDonald, G., L. Shi, C. Vande Velde, J. Lieberman, and A. H. Greenberg. 1999. Mitochondria-dependent and -independent regulation of granzyme B-induced apoptosis. J. Exp. Med. 189: 131-144.
46. Thomas, D. A., C. Du, M. Xu, X. Wang, and T. J. Ley. 2000. DFF45/ICAD can be directly processed by granzyme B during the induction of apoptosis. Immunity 12: 621-632.
47. Enari, M., H. Sakahira, H. Yokoyama, K. Okawa, A. Iwamatsu, and S. Nagata. 1998. A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391: 43-50. (Pubitemid 28079208)
48. Lamagna, C., M. Aurrand-Lions, and B. A. Imhof. 2006. Dual role of macrophages in tumor growth and angiogenesis. J. Leukoc. Biol. 80: 705-713.
49. Mantovani, A., and A. Sica. 2010. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr. Opin. Immunol. 22: 231-237.
50. Qian, B. Z., and J. W. Pollard. 2010. Macrophage diversity enhances tumor progression and metastasis. Cell 141: 39-51.
51. Fleetwood, A. J., T. Lawrence, J. A. Hamilton, and A. D. Cook. 2007. Granulocyte-macrophage colony-stimulating factor (CSF) and macrophage CSF-dependent macrophage phenotypes display differences in cytokine profiles and transcription factor activities: implications for CSF blockade in inflammation. J. Immunol. 178: 5245-5252.
52. Andersson, U., H. Wang, K. Palmblad, A. C. Aveberger, O. Bloom, H. Erlandsson-Harris, A. Janson, R. Kokkola, M. Zhang, H. Yang, and K. J. Tracey. 2000. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 192: 565-570.
53. Rao, D. A., K. J. Tracey, and J. S. Pober. 2007. IL-1alpha and IL-1beta are endogenous mediators linking cell injury to the adaptive alloimmune response. J. Immunol. 179: 6536-6546.
54. Thorburn, J., H. Horita, J. Redzic, K. Hansen, A. E. Frankel, and A. Thorburn. 2009. Autophagy regulates selective HMGB1 release in tumor cells that are destined to die. Cell Death Differ. 16: 175-183.
55. Lerman, S. P., and W. P. Weidanz. 1970. The effect of cyclophosphamide on the ontogeny of the humoral immune response in chickens. J. Immunol. 105: 614-619.
56. Stockman, G. D., L. R. Heim, M. A. South, and J. J. Trentin. 1973. Differential effects of cyclophosphamide on the B and T cell compartments of adult mice. J. Immunol. 110: 277-282.