Immunotherapeutic targeting of membrane Hsp70-expressing tumors using recombinant human granzyme B

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Gehrmann, Mathias ^a   Stangl, Stefan ^a   Kirschner, Andreas ^a   Foulds, Gemma A ^a,b   Sievert, Wolfgang ^a   Doß, Brigitte T ^a   Walch, Axel ^c   Pockley, Alan G ^b   Multhoff, Gabriele ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; GRANZYME B; HEAT SHOCK PROTEIN 70; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 2; RAB PROTEIN; RAB11 PROTEIN; RAB7 PROTEIN; RAB9 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CANCER ADJUVANT THERAPY; CANCER IMMUNOTHERAPY; CANCER INHIBITION; CELL COUNT; COLON ADENOCARCINOMA; CONTROLLED STUDY; DRUG TOLERABILITY; ENDOSOME; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; INTERNALIZATION; LYSOSOME; MONOLAYER CULTURE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; TUMOR SPHEROID;

ANIMALS; APOPTOSIS; CAMPTOTHECIN; CELL LINE, TUMOR; CELLS, CULTURED; ENDOTHELIAL CELLS; FLOW CYTOMETRY; GRANZYMES; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; RECOMBINANT PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

MUS;

EID: 84864075586     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041341     Document Type: Article

References (41)

1. Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, et al. (2004) Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med 200: 425-435.
2. Schmitt E, Gehrmann M, Brunet M, Multhoff G, Garrido C, (2007) Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy. J Leukoc Biol 81: 15-27.
3. Rerole AL, Jego G, Garrido C, (2011) Hsp70: anti-apoptotic and tumorigenic protein. Methods Mol Biol 787: 205-230.
4. Multhoff G, Botzler C, Wiesnet M, Müller E, Meier T, et al. (1995) A stress-inducible 72-kDa heat-shock protein (HSP72) is expressed on the surface of human tumor cells, but not on normal cells. Int J Cancer 61: 272-279.
5. Botzler C, Issels R, Multhoff G, (1996) Heat-shock protein 72 cell-surface expression on human lung carcinoma cells in associated with an increased sensitivity to lysis mediated by adherent natural killer cells. Cancer Immunol Immunother 43: 226-230.
6. Botzler C, Li G, Issels RD, Multhoff G, (1998) Definition of extracellular localized epitopes of Hsp70 involved in an NK immune response. Cell Stress Chaperones 3: 6-11.
7. Gehrmann M, Brunner M, Pfister K, Reichle A, Kremmer E, et al. (2004) Differential up-regulation of cytosolic and membrane-bound heat shock protein 70 in tumor cells by anti-inflammatory drugs. Clin Cancer Res 10: 3354-3364.
8. Gehrmann M, Marienhagen J, Eichholtz-Wirth H, Fritz E, Ellwart J, et al. (2005) Dual function of membrane-bound heat shock protein 70 (Hsp70), Bag-4, and Hsp40: protection against radiation-induced effects and target structure for natural killer cells. Cell Death Differ 12: 38-51.
9. Gehrmann M, Liebisch G, Schmitz G, Anderson R, Steinem C, et al. (2008) Tumor-specific Hsp70 plasma membrane localization is enabled by the glycosphingolipid Gb3. PLos One 3: e1925.
10. Schilling D, Gehrmann M, Steinem C, DeMaio A, Pockley AG, et al. (2009) Binding of heat shock protein 70 to extracellular phosphatidylserine promotes killing of normoxic and hypoxic tumor cells. FASEB J 23: 2467-2477.
11. Stangl S, Gehrmann M, Riegger J, Kuhs I, Riederer I, et al. (2011) Targeting membrane heat-shock protein 70 (Hsp70) on tumors by cmHsp70.1 antibody. Proc Natl Acad Sci USA 108: 733-738.
12. Pfister K, Radons J, Busch R, Tidball JG, Pfeifer M, et al. (2007) Patient survival by Hsp70 membrane phenotype: association with different routes of metastasis. Cancer 110: 926-935.
13. Gehrmann M, Pfister K, Hutzler P, Gastpar R, Margulis B, et al. (2002) Effects of antineoplastic agents on cytoplasmic and membrane-bound heat shock protein 70 (Hsp70) levels. Biol Chem 383: 1715-1725.
14. Multhoff G, Botzler C, Jennen L, Schmidt J, Ellwart J, et al. (1997) Heat shock protein 72 on tumor cells: a recognition structure for natural killer cells. J Immunol 158: 4341-4350.
15. Krause SW, Gastpar R, Andreesen R, Gross C, Ullrich H, et al. (2004) Treatment of colon and lung cancer patients with ex vivo heat shock protein 70-peptide-activated, autologous natural killer cells: a clinical phase I trial. Clin Cancer Res 10: 3699-3707.
16. Milani V, Stangl S, Issels R, Gehrmann M, Wagner B, et al. (2009) Anti-tumor activity of patient-derived NK cells after cell-based immunotherapy- a case report. J Transl Med 7: 50.
17. Gross C, Koelch W, DeMaio A, Arispe N, Multhoff G, (2003) Cell surface-bound heat shock protein 70 (Hsp70) mediates perforin-independent apoptosis by specific binding and uptake of granzyme B. J Biol Chem 278: 41173-41181.
18. Gehrmann M, Doss BT, Wagner M, Zettlitz KA, Kontermann RE, et al. (2011) A novel expression and purification system for the production of enzymatic and biologically active human granzyme B. J. Immunol. Methods 371: 8-17.
19. Stangl S, Gehrmann M, Dressel R, Alves F, Dullin C, et al. (2011) In vivo imaging of CT26 mouse tumors by using cmHsp70.1 monoclonal antibody. J Cell Mol Med 15: 874-887.
20. Kurschus FC, Bruno R, Fellows E, Falk CS, Jenne DE, (2005) Membrane receptors are not required to deliver granzyme B during killer cell attack. Blood 105: 2049-2058.
21. Thiery J, Keefe D, Boulant S, Boucort E, Walch M, et al. (2011) Perforin pores in the endosomal membrane trigger the release of endocytosed granzyme B into the cytosol of target cells. Nat Immunol 12: 770-777.
22. Liu Y, Cheung LH, Hittelman WN, Rosenblum MG, (2003) Targeted delivery of human pro-apoptotic enzymes to tumor cells: In vitro studies describing a novel class of recombinant highly cytotoxic agents. Mol Cancer Ther 2: 1341-1350.
23. Liu Y, Zhang W, Niu T, Cheung LH, Munshi A, et al. (2006) Targeted apoptosis activation with GrB/scFvMEL modulates melanoma growth, metastatic spread, chemosensitivity, and radiosensitivity. Neoplasia 8: 125-135.
24. Sun J, Bird CH, Sutton V, McDonald L, Coughlin PB, et al. (1996) A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J Biol Chem 271: 27802-27809.
25. Xia Z, Kam CM, Huang C, Powers JC, Mandle RJ, et al. (1998) Expression and purification of enzymatically active recombinant granzyme B in a baculovirus system. Biochem Biophys Res Commun 243: 384-389.
26. Mahrus S, Kisiel W, Craik CS, (2004) Granzyme M is a regulatory protease that inactivates proteinase inhibitor 9, an endogenous inhibitor of granzyme B. J Biol Chem 279: 54275-54282.
27. Giesubel U, Dalken B, Mahmud H, Wels WS, (2006) Cell binding, internalization and cytotoxic activity of human granzyme B expressed in the yeast Pichia pastoris. Biochem J 394: 563-573.
28. Trapani JA, Browne KA, Smyth MJ, Jans DA, (1996) Localization of granzyme B in the nucleus. A putative role in the mechanism of cytotoxic lymphocyte-mediated apoptosis. J Biol Chem 271: 4127-4133.
29. Dertinger H, Hulser DF, (1984) Intercellular communication in spheroids. Recent Results Cancer Res 95: 67-83.
30. Friedrich J, Ebner R, Kunz-Schughart LA, (2007) Experimental anti-tumor therapy in 3-D: spheroids- old hat or new challenge? Int J Radiat Biol 83: 849-871.
31. Lin RZ, Chang HY, (2008) Recent advances in three-dimensional multicellular spheroid culture for biomedical research. Biotechnol J 3: 1172-1184.
32. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA, (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4: 309-324.
33. Ciocca DR, Calderwood SK, (2005) Heat shock proteins in cancer: diagnostic, prognostic, predictive, and treatment implications. Cell Stress Chaperones 10: 86-103.
34. MacDonald G, Shi L, Vande VC, Lieberman J, Greenberg AH, (1999) Mitochondria-dependent and-independent regulation of Granzyme B-induced apoptosis. J Exp Med 189: 131-144.
35. Kaiserman D, Bird CH, Sun J, Matthews A, Ung K, et al. (2006) The major human and mouse granzymes are structurally and functionally divergent. J Cell Biol 175: 619-630.
36. Boivin WA, Cooper DM, Hiebert PR, Granville DJ, (2009) Intracellular versus extracellular granzyme B in immunity and disease: challenging the dogma. Lab Invest 89: 1195-1220.
37. Chavez-Galan L, Renas-Del Angel MC, Zenteno E, Chavez R, Lascurain R, (2009) Cell death mechanisms induced by cytotoxic lymphocytes. Cell Mol. Immunol. 6: 15-25.
38. Cullen SP, Brunet M, Martin SJ, (2010) Granzymes in cancer and immunity. Cell Death Differ 17: 616-623.
39. Balkow S, Kersten A, Tran TT, Stehle T, Grosse P, et al. (2001) Concerted action of the FasL/Fas and perforin/granzyme A and B pathways is mandatory for the development of early viral hepatitis but not for recovery from viral infection. J Virol 75: 8781-8791.
40. Buzza MS, Bird PI, (2006) Extracellular granzymes: current perspectives. Biol Chem 387: 827-837.
41. Wang M, Bronte V, Chen PW, Gritz L, Panicali D, et al. (1995) Active immunotherapy of cancer with a nonreplicating recombinant fowlpox virus encoding a model tumor-associated antigen. J Immunol 154: 4685-4692.