Induction of hsp70-mediated Th17 autoimmunity can be exploited as immunotherapy for metastatic prostate cancer

Cancer Research

Volumn 67, Issue 24, 2007, Pages 11970-11979

  Kottke, Timothy ^a   Sanchez Perez, Luis ^a,b,g   Diaz, Rosa Maria ^a   Thompson, Jill ^a   Chong, Heung ^c   Harrington, Kevin ^d   Calderwood, Stuart K ^e   Pulido, Jose ^a   Georgopoulos, Nick ^f   Selby, Peter ^f   Melcher, Alan ^f   Vile, Richard ^a,b,f  

^a MAYO CLINIC   (United States)

^b MAYO GRADUATE SCHOOL   (United States)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^d INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^e BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^f UNIVERSITY OF LEEDS   (United Kingdom)

^g NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; GREEN FLUORESCENT PROTEIN; HEAT SHOCK PROTEIN 70; INTERLEUKIN 17; INTERLEUKIN 6; MEMBRANE PROTEIN; THROMBOSPONDIN; TUMOR ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CANCER IMMUNOTHERAPY; CELL TYPE; CONTROLLED STUDY; IMMUNE RESPONSE; MALE; MELANOMA; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN INDUCTION; T LYMPHOCYTE; TH17 CELL; TREATMENT RESPONSE; TUMOR REJECTION;

ANIMALS; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; HSP70 HEAT-SHOCK PROTEINS; IMMUNOTHERAPY; INFLAMMATION; INTERLEUKIN-17; INTERLEUKIN-6; LYMPH NODES; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; NEOPLASM METASTASIS; PROSTATIC NEOPLASMS; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 37549008775     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-2259     Document Type: Article

References (50)

1. Pardoll DM. Spinning molecular immunology into successful immunotherapy. Nat Rev Immunol 2002;2:227-38.
2. Houghton AN. Cancer antigens: immune recognition of self and altered self. J Exp Med 1994;180:1-4.
3. Parmiani G. Tumor immunity as autoimmunity: tumor antigens include normal self proteins which stimulate anergic peripheral T cells. Immunol. Today 1993;14:536-8.
4. Bronte V, Apolloni E, Ronca R, et al. Genetic vaccination with "self" tyrosinase-related protein 2 causes melanoma eradication but not vitiligo. Cancer Res 2000;60:253-8.
5. Hodi FS, Mihm MC, Soiffer RJ, et al. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci U S A 2003;100:4712-7.
6. Dudley ME, Wunderlich JR, Robbins PF, et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 2002;298:850-4.
7. Overwijk W, Theoret M, Finkelstein S, et al. Tumor regression and autoimmunity after reversal of a functionally tolerant state of self-reactive CD8+ T cells. J Exp Med 2003;198:569-80.
8. Gogas H, Ioannovich J, Dafni U, et al. Prognostic significance of autoimmunity during treatment of melanoma with interferon. N Engl J Med 2006;354:758-60.
9. Ferrone S. Immunotherapy dispenses with tumor antigens. Nat Biotechnol 2004;22:1096-8.
10. Melcher AA, Todryk S, Hardwick N, Ford M, Jacobson M, Vile RG. Tumor immunogenicity is determined by the mechanism of cell death via induction of heat shock protein expression. Nat Med 1998;4:581-7.
11. Todryk S, Melcher AA, Hardwick N, et al. Heat shock protein 70 induced during tumor cell killing induces Th1 cytokines and targets immature dendritic cell precursors to enhance antigen uptake. J Immunol 1999;163:1398-408.
12. Gough MJ, Melcher AA, Ahmed A, et al. Macrophages orchestrate the immune response to tumor cell death. Cancer Res 2001;61:7240-7.
13. Singh-Jasuja H, Toes RE, Spee P, et al. Cross-presentation of glycoprotein 96-associated antigens on major histocompatibility complex class I molecules requires receptor-mediated endocytosis. J Exp Med 2000;191:1965-74.
14. Castellino F, Boucher PE, Eichelberg K, et al. Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J Exp Med 2000;191:1957-64.
15. Srivastava PK, Menoret A, Basu S, Binder RJ, McQuade KL. Heat shock proteins come of age: primitive functions acquire new roles in an adaptive world. Immunity 1998;8:657-65.
16. Suzue K, Zhou X, Eisen HN, Young RA. Heat shock fusion proteins as vehicles for antigen delivery into the major histocompatibility complex class I presentation pathway. Proc Natl Acad Sci U S A 1997;94:13146-51.
17. MacAry PA, Javid B, Floto RA, et al. HSP70 peptide binding mutants separate antigen delivery from dendritic cell stimulation. Immunity 2004;20:95-106.
18. Asea A, Rehli M, Kabingu E, et al. Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem 2002;277:15028-34.
19. Millar DG, Garza KM, Odermatt B, et al. Hsp70 promotes antigen-presenting cell function and converts T-cell tolerance to autoimmunity in vivo. Nat Med 2003;9:1469-76.
20. Lukacs KV, Nakakes A, Atkins CJ, Lowrie DB, Colston MJ. In vivo gene therapy of malignant tumours with heat shock protein-65 gene. Gene Ther 1997;4:346-50.
21. Sanchez-Perez L, Kottke T, Daniels G, et al. Killing of normal melanocytes, combined with hsp70 and CD40L expression, cures large established melanomas. J Immunol 2006;177:4168-77.
22. Melcher AA, Gough MJ, Todryk S, Vile RG. Apoptosis or necrosis for tumour immunotherapy - what's in a name? J Mol Med 1999;77:824-33.
23. Srivastava PK. Hypothesis: controlled necrosis as a tool for immunotherapy of human cancer. Can Immunol 2003;3:4.
24. Daniels G, Sanchez-Perez L, Kottke T, et al. A simple method to cure established tumors by inflammatory killing of normal cells. Nat Biotechnol 2004;22:1125-32.
25. Sanchez-Perez L, Kottke T, Diaz RM, et al. Potent selection of antigen loss variants of B16 melanoma following inflammatory killing of melanocytes in vivo. Cancer Res 2005;65:2009-17.
26. von Herrath MG, Harrison LC. Antigen-induced regulatory T cells in autoimmunity. Nat Rev Immunol 2003;3:223-32.
27. Linardakis E, Bateman A, Phan V, et al. Enhancing the efficacy of a weak allogeneic melanoma vaccine by viral fusogenic membrane glycoprotein-mediated tumor cell-tumor cell fusion. Can Res 2002;62:5495-504.
28. Bateman A, Harrington K, Kottke T, et al. Viral fusogenic membrane glycoproteins kill solid tumor cells by non-apoptotic mechanisms which promote cross presentation of tumor antigens by dendritic cells. Cancer Res 2002;62:5466-6578.
29. Higuchi H, Bronk S, Bateman A, Harrington KJ, Vile RG, Gores GJ. Viral fusogenic membrane glycoprotein expression causes syncytia formation with bioenergetic cell death: implications for gene therapy. Cancer Res 2000;60:6396-402.
30. Melcher A, Murphy S, Vile RG. Heat shock protein expression in target cells infected by poorly detectable levels of replication competent virus contributes to the immunogenicity of adenoviral vectors. Hum Gene Ther 1999;10:1431-42.
31. Ahmed A, Thompson J, Emiliusen L, et al. A conditionally replicating adenovirus targeted to tumor cells through activated RAS/MAPK-selective mRNA stabilisation. Nat Biotechnol 2003;21:771-7.
32. Vile RG, Castleden SC, 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;71:267-74.
33. Hogquist KA, Jameson SC, Health WR, Howard JL, Bevan MJ, Carbone FR. T cell receptor antagonistic peptides induce positive selection. Cell 1994;76:17.
34. Dyall R, Bowne WB, Weber LW, et al. Heteroclitic immunization induces tumor immunity. J Exp Med 1998;188:1553-61.
35. Thomas DA, Massague J. TGF-β directly targets cytotoxic T cell functions during tumor evasion of immune surveillance. Cancer Cell 2005;8:369-80.
36. Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W. Current Protocols in Immunology. Wiley and Sons, Inc.; 1998.
37. Altman DG. Analysis of survival times. In: Practical Statistics for Medical Research 1991;365-95.
38. Veldhoen M, Hocking R, Atkins C, Locksley R, Stockinger B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiaton of IL-17-producing T cells. Immunity 2006;24:179-89.
39. Mangan P, Harrington L, O'Quinn D, et al. Transforming growth factor-β induces development of the TH17 lineage. Nature 2006;441:231-4.
40. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235-8.
41. Theriault JR, Adachi H, Calderwood SK. Role of scavenger receptors in the binding and internalization of heat shock protein 70. J Immunol 2006;177:8604-11.
42. Becker T, Hartl FU, Wieland F. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J Cell Biol 2002;158:1227-85.
43. Gross C, Schmidt-Wolf IG, Nagaraj S, et al. Heat shock protein 70-reactivity is associated with increased cell surface density of CD94-56 on primary natural killer cells. Cell Stress Chaperones 2003;8:348-60.
44. Jiang S, Lechler RI. CD4+CD25+ regulatory T-cell therapy for allergy, autoimmune disease and transplant rejection. Inflamm Allergy Drug Targets 2006;5:239-42.
45. Tarbell KV, Petit L, Zuo X, et al. Dendritic cell-expanded, islet-specific CD4+ CD25+ CD62L+ regulatory T cells restore normoglycemia in diabetic NOD mice. J Exp Med 2007;204:191-201.
46. Bateman A, Bullough F, Murphy S, et al. Fusogenic membrane glycoproteins as a novel class of genes for the local and immune-mediated control of tumor growth. Cancer Res 2000;60:1492-7.
47. Diaz RM, Bateman A, Emiliusen L, et al. A lentiviral vector expressing a fusogenic glycoprotein for cancer gene therapy. Gene Therapy 2000;7:1656-63.
48. Fu X, Tao L, Jin A, Vile R, Brenner MK, Zhang X. Expression of a fusogenic membrane glycoprotein by an oncolytic herpes simplex virus provides potent synergistic anti-tumor effect. Molecular Therapy 2003;7:748-54.
49. Emiliusen L, Gough M, Bateman A, et al. A transcriptional feedback loop for tissue-specific expression of highly cytotoxic genes which incorporates an immunostimulatory component. Gene Ther 2001;8:987-98.
50. Bateman A, Phan V, Melcher A, Linardakis E, Harrington H, Vile R. Fusogenic membrane proteins for cancer gene therapy: a better class of killer. In: Curiel D, Douglas JT, editors. Contemporary cancer research: cancer gene therapy. Totowa (NJ): Humana Press Inc; 2005.