Novel humanized and highly efficient bispecific antibodies mediate killing of prostate stem cell antigen-expressing tumor cells by CD8+and CD4+ T cells

Journal of Immunology

Volumn 189, Issue 6, 2012, Pages 3249-3259

  Feldmann, Anja ^a   Arndt, Claudia ^a   Töpfer, Katrin ^b   Stamova, Slava ^a   Krone, Franziska ^a   Cartellieri, Marc ^a   Koristka, Stefanie ^a   Michalk, Irene ^a   Lindemann, Dirk ^b,c   Schmitz, Marc ^a,c   Temme, Achim ^b   Bornhaüser, Martin ^b,c   Ehninger, Gerhard ^b   Bachmann, Michael ^a,c  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^c CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BISPECIFIC ANTIBODY; GAMMA INTERFERON; PROSTATE STEM CELL ANTIGEN; SINGLE CHAIN BISPECIFIC CD3 PSCA ANTIBODY; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER INHIBITION; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE RELEASE; DEGRANULATION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CROSS LINKING; T LYMPHOCYTE ACTIVATION; TUMOR; TUMOR CELL; TUMOR CELL DESTRUCTION; TUMOR XENOGRAFT;

ANTIBODIES, BISPECIFIC; ANTIBODIES, MONOCLONAL, HUMANIZED; ANTIGENS, NEOPLASM; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DEATH; EPITOPES, T-LYMPHOCYTE; GPI-LINKED PROTEINS; HUMANS; MALE; NEOPLASM PROTEINS; PROSTATIC NEOPLASMS; STEM CELLS; TUMOR STEM CELL ASSAY;

EID: 84866159579     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200341     Document Type: Article

References (49)

1. Jemal, A., R. Siegel, J. Xu, and E. Ward. 2010. Cancer statistics, 2010. CA Cancer J. Clin. 60: 277-300.
2. Coen, J. J., A. L. Zietman, H. Thakral, and W. U. Shipley. 2002. Radical radiation for localized prostate cancer: local persistence of disease results in a late wave of metastases. J. Clin. Oncol. 20: 3199-3205. (Pubitemid 34831515)
3. Roehl, K. A., M. Han, C. G. Ramos, J. A. Antenor, and W. J. Catalona. 2004. Cancer progression and survival rates following anatomical radical retropubic prostatectomy in 3,478 consecutive patients: long-term results. J. Urol. 172: 910-914. (Pubitemid 39096421)
4. Miyamoto, H., E. M. Messing, and C. Chang. 2004. Androgen deprivation therapy for prostate cancer: current status and future prospects. Prostate 61: 332-353. (Pubitemid 39571710)
5. Feldman, B. J., and D. Feldman. 2001. The development of androgen-independent prostate cancer. Nat. Rev. Cancer 1: 34-45. (Pubitemid 33741879)
6. Tannock, I. F., R. de Wit, W. R. Berry, J. Horti, A. Pluzanska, K. N. Chi, S. Oudard, C. Théodore, N. D. James, I. Turesson, et al TAX 327 Investigators. 2004. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N. Engl. J. Med. 351: 1502-1512. (Pubitemid 39315317)
7. Raff, A. B., A. Gray, and W. M. Kast. 2009. Prostate stem cell antigen: a prospective therapeutic and diagnostic target. Cancer Lett. 277: 126-132.
8. Reiter, R. E., Z. Gu, T. Watabe, G. Thomas, K. Szigeti, E. Davis, M. Wahl, S. Nisitani, J. Yamashiro, M. M. Le Beau, et al. 1998. Prostate stem cell antigen: a cell surface marker overexpressed in prostate cancer. Proc. Natl. Acad. Sci. USA 95: 1735-1740. (Pubitemid 28103463)
9. Gu, Z., G. Thomas, J. Yamashiro, I. P. Shintaku, F. Dorey, A. Raitano, O. N. Witte, J. W. Said, M. Loda, and R. E. Reiter. 2000. Prostate stem cell antigen (PSCA) expression increases with high gleason score, advanced stage and bone metastasis in prostate cancer. Oncogene 19: 1288-1296. (Pubitemid 30160621)
10. Lam, J. S., J. Yamashiro, I. P. Shintaku, R. L. Vessella, R. B. Jenkins, S. Horvath, J. W. Said, and R. E. Reiter. 2005. Prostate stem cell antigen is overexpressed in prostate cancer metastases. Clin. Cancer Res. 11: 2591-2596. (Pubitemid 40569458)
11. Han, K. R., D. B. Seligson, X. Liu, S. Horvath, P. I. Shintaku, G. V. Thomas, J. W. Said, and R. E. Reiter. 2004. Prostate stem cell antigen expression is associated with gleason score, seminal vesicle invasion and capsular invasion in prostate cancer. J. Urol. 171: 1117-1121. (Pubitemid 38327539)
12. Argani, P., C. Rosty, R. E. Reiter, R. E. Wilentz, S. R. Murugesan, S. D. Leach, B. Ryu, H. G. Skinner, M. Goggins, E. M. Jaffee, et al. 2001. Discovery of new markers of cancer through serial analysis of gene expression: prostate stem cell antigen is overexpressed in pancreatic adenocarcinoma. Cancer Res. 61: 4320-4324. (Pubitemid 32685751)
13. Elsamman, E., T. Fukumori, T. Kasai, H. Nakatsuji, M. A. Nishitani, K. Toida, N. Ali, and H. O. Kanayama. 2006. Prostate stem cell antigen predicts tumour recurrence in superficial transitional cell carcinoma of the urinary bladder. BJU Int. 97: 1202-1207. (Pubitemid 43907322)
14. Müller, D., and R. E. Kontermann. 2010. Bispecific antibodies for cancer immunotherapy: Current perspectives. BioDrugs 24: 89-98.
15. Hoffmann, P., R. Hofmeister, K. Brischwein, C. Brandl, S. Crommer, R. Bargou, C. Itin, N. Prang, and P. A. Baeuerle. 2005. Serial killing of tumor cells by cytotoxic T cells redirected with a CD19-/CD3-bispecific single-chain antibody construct. Int. J. Cancer 115: 98-104. (Pubitemid 40559673)
16. Offner, S., R. Hofmeister, A. Romaniuk, P. Kufer, and P. A. Baeuerle. 2006. Induction of regular cytolytic T cell synapses by bispecific single-chain antibody constructs on MHC class I-negative tumor cells. Mol. Immunol. 43: 763-771. (Pubitemid 41785405)
17. Wolf, E., R. Hofmeister, P. Kufer, B. Schlereth, and P. A. Baeuerle. 2005. BiTEs: bispecific antibody constructs with unique anti-tumor activity. Drug Discov. Today 10: 1237-1244. (Pubitemid 41411434)
18. Dreier, T., P. A. Baeuerle, I. Fichtner, M. Grün, B. Schlereth, G. Lorenczewski, P. Kufer, R. Lutterbüse, G. Riethmüller, P. Gjorstrup, and R. C. Bargou. 2003. T cell costimulus-independent and very efficacious inhibition of tumor growth in mice bearing subcutaneous or leukemic human B cell lymphoma xenografts by a CD19-/CD3- bispecific single-chain antibody construct. J. Immunol. 170: 4397-4402. (Pubitemid 36428210)
19. Lutterbuese, R., T. Raum, R. Kischel, P. Lutterbuese, B. Schlereth, E. Schaller, S. Mangold, D. Rau, P. Meier, P. A. Kiener, et al. 2009. Potent control of tumor growth by CEA/CD3-bispecific single-chain antibody constructs that are not competitively inhibited by soluble CEA. J. Immunother. 32: 341-352.
20. Amann, M., S. D'Argouges, G. Lorenczewski, K. Brischwein, R. Kischel, R. Lutterbuese, S. Mangold, D. Rau, J. Volkland, S. Pflanz, et al. 2009. Anti-tumor activity of an EpCAM/CD3-bispecific BiTE antibody during long-term treatment of mice in the absence of T-cell anergy and sustained cytokine release. J. Immunother. 32: 452-464.
21. Fortmüller, K., K. Alt, D. Gierschner, P. Wolf, V. Baum, N. Freudenberg, U. Wetterauer, U. Elsässer-Beile, and P. Bühler. 2011. Effective targeting of prostate cancer by lymphocytes redirected by a PSMA X CD3 bispecific single-chain diabody. Prostate 71: 588-596.
22. Schlereth, B., C. Quadt, T. Dreier, P. Kufer, G. Lorenczewski, N. Prang, C. Brandl, S. Lippold, K. Cobb, K. Brasky, et al. 2006. T-cell activation and B-cell depletion in chimpanzees treated with a bispecific anti-CD19/anti-CD3 single-chain antibody construct. Cancer Immunol. Immunother. 55: 503-514.
23. Bargou, R., E. Leo, G. Zugmaier, M. Klinger, M. Goebeler, S. Knop, R. Noppeney, A. Viardot, G. Hess, M. Schuler, et al. 2008. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 321: 974-977.
24. Topp, M. S., P. Kufer, N. Gökbuget, M. Goebeler, M. Klinger, S. Neumann, H. A. Horst, T. Raff, A. Viardot, M. Schmid, et al. 2011. Targeted therapy with the T-cell-engaging antibody blinatumomab of chemotherapy- refractory minimal residual disease in B-lineage acute lymphoblastic leukemia patients results in high response rate and prolonged leukemia-free survival. J. Clin. Oncol. 29: 2493-2498.
25. Wu, A. M., W. Chen, A. Raubitschek, L. E. Williams, M. Neumaier, R. Fischer, S. Z. Hu, T. Odom-Maryon, J. Y. Wong, and J. E. Shively. 1996. Tumor localization of anti-CEA single-chain Fvs: improved targeting by non-covalent dimers. Immunotechnology 2: 21-36. (Pubitemid 26096269)
26. Divgi, C. R., A. M. Scott, S. Gulec, E. K. Broussard, N. Levy, C. Young, P. Capitelli, F. Daghighian, J. M. Williams, R. D. Finn, et al. 1995. Pilot radioimmunotherapy trial with 131I-labeled murine monoclonal antibody CC49 and deoxyspergualin in metastatic colon carcinoma. Clin. Cancer Res. 1: 1503-1510.
27. Saleh, M. N., A. F. LoBuglio, R. H. Wheeler, K. J. Rogers, A. Haynes, J. Y. Lee, and M. B. Khazaeli. 1990. A phase II trial of murine monoclonal antibody 17-1A and interferon-gamma: clinical and immunological data. Cancer Immunol. Immunother. 32: 185-190.
28. Jolliffe, L. K. 1993. Humanized antibodies: enhancing therapeutic utility through antibody engineering. Int. Rev. Immunol. 10: 241-250.
29. Pavlinkova, G., D. Colcher, B. J. Booth, A. Goel, U. A. Wittel, and S. K. Batra. 2001. Effects of humanization and gene shuffling on immunogenicity and antigen binding of anti-TAG-72 single-chain Fvs. Int. J. Cancer 94: 717-726. (Pubitemid 33035693)
30. Feldmann, A., S. Stamova, C. C. Bippes, H. Bartsch, R. Wehner, M. Schmitz, A. Temme, M. Cartellieri, and M. Bachmann. 2011. Retargeting of T cells to prostate stem cell antigen expressing tumor cells: comparison of different antibody formats. Prostate 71: 998-1011.
31. Stamova, S., M. Cartellieri, A. Feldmann, C. C. Bippes, H. Bartsch, R. Wehner, M. Schmitz, M. von Bonin, M. Bornhäuser, G. Ehninger, et al. 2011. Simultaneous engagement of the activatory receptors NKG2D and CD3 for retargeting of effector cells to CD33-positive malignant cells. Leukemia 25: 1053-1056.
32. Stamova, S., M. Cartellieri, A. Feldmann, C. Arndt, S. Koristka, H. Bartsch, C. C. Bippes, R. Wehner, M. Schmitz, M. von Bonin, et al. 2011. Unexpected recombinations in single chain bispecific anti-CD3-anti-CD33 antibodies can be avoided by a novel linker module. Mol. Immunol. 49: 474-482.
33. Morgenroth, A., M. Cartellieri, M. Schmitz, S. Günes, B. Weigle, M. Bachmann, H. Abken, E. P. Rieber, and A. Temme. 2007. Targeting of tumor cells expressing the prostate stem cell antigen (PSCA) using genetically engineered T-cells. Prostate 67: 1121-1131. (Pubitemid 46983341)
34. Carmo-Fonseca, M., K. Pfeifer, H. C. Schröder, M. F. Vaz, J. E. Fonseca, W. E. Müller, and M. Bachmann. 1989. Identification of La ribonucleoproteins as a component of interchromatin granules. Exp. Cell Res. 185: 73-85. (Pubitemid 19284956)
35. Crawford, E. D., M. Rosenblum, A. M. Ziada, and P. H. Lange. 1999. Hormone refractory prostate cancer. Urology 54(6A Suppl.): 1-7.
36. Kiessling, A., S. Füssel, R. Wehner, M. Bachmann, M. P. Wirth, E. P. Rieber, and M. Schmitz. 2008. Advances in specific immunotherapy for prostate cancer. Eur. Urol. 53: 694-708.
37. Brischwein, K., B. Schlereth, B. Guller, C. Steiger, A. Wolf, R. Lutterbuese, S. Offner, M. Locher, T. Urbig, T. Raum, et al. 2006. MT110: a novel bispecific single-chain antibody construct with high efficacy in eradicating established tumors. Mol. Immunol. 43: 1129-1143. (Pubitemid 43063166)
38. Löffler, A., P. Kufer, R. Lutterbüse, F. Zettl, P. T. Daniel, J. M. Schwenkenbecher, G. Riethmüller, B. Dörken, and R. C. Bargou. 2000. A recombinant bispecific single-chain antibody, CD19 X CD3, induces rapid and high lymphoma-directed cytotoxicity by unstimulated T lymphocytes. Blood 95: 2098-2103. (Pubitemid 30151651)
39. Dreier, T., G. Lorenczewski, C. Brandl, P. Hoffmann, U. Syring, F. Hanakam, P. Kufer, G. Riethmuller, R. Bargou, and P. A. Baeuerle. 2002. Extremely potent, rapid and costimulation-independent cytotoxic T-cell response against lymphoma cells catalyzed by a single-chain bispecific antibody. Int. J. Cancer 100: 690-697. (Pubitemid 34832980)
40. Haas, C., E. Krinner, K. Brischwein, P. Hoffmann, R. Lutterbüse, B. Schlereth, P. Kufer, and P. A. Baeuerle. 2009. Mode of cytotoxic action of T cell-engaging BiTE antibody MT110. Immunobiology 214: 441-453.
41. Gruen, M., K. Bommert, and R. C. Bargou. 2004. T-cell-mediated lysis of B cells induced by a CD19xCD3 bispecific single-chain antibody is perforin dependent and death receptor independent. Cancer Immunol. Immunother. 53: 625-632. (Pubitemid 38858336)
42. Stamova, S., A. Feldmann, M. Cartellieri, C. Arndt, S. Koristka, F. Apel, R. Wehner, M. Schmitz, M. Bornhäuser, M. von Bonin, et al. 2012. Generation of single-chain bispecific green fluorescent protein fusion antibodies for imaging of antibody-induced T cell synapses. Anal. Biochem. 423: 261-268.
43. Brischwein, K., L. Parr, S. Pflanz, J. Volkland, J. Lumsden, M. Klinger, M. Locher, S. A. Hammond, P. Kiener, P. Kufer, et al. 2007. Strictly target cell-dependent activation of T cells by bispecific single-chain antibody constructs of the BiTE class. J. Immunother. 30: 798-807. (Pubitemid 350295358)
44. Zou, W. 2006. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol. 6: 295-307.
45. Nishikawa, H., and S. Sakaguchi. 2010. Regulatory T cells in tumor immunity. Int. J. Cancer 127: 759-767.
46. Bates, G. J., S. B. Fox, C. Han, R. D. Leek, J. F. Garcia, A. L. Harris, and A. H. Banham. 2006. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J. Clin. Oncol. 24: 5373-5380. (Pubitemid 46623168)
47. Ling, K. L., S. E. Pratap, G. J. Bates, B. Singh, N. J. Mortensen, B. D. George, B. F. Warren, J. Piris, G. Roncador, S. B. Fox, et al. 2007. Increased frequency of regulatory T cells in peripheral blood and tumour infiltrating lymphocytes in colorectal cancer patients. Cancer Immun. 7: 7.
48. Szczepanski, M. J., M. Szajnik, M. Czystowska, M. Mandapathil, L. Strauss, A. Welsh, K. A. Foon, T. L. Whiteside, and M. Boyiadzis. 2009. Increased frequency and suppression by regulatory T cells in patients with acute myelogenous leukemia. Clin. Cancer Res. 15: 3325-3332.
49. Koristka, S., M. Cartellieri, A. Theil, A. Feldmann, C. Arndt, S. Stamova, I. Michalk, K. Töpfer, A. Temme, K. Kretschmer, et al. 2012. Retargeting of human regulatory T cells by single-chain bispecific antibodies. J. Immunol. 188: 1551-1558.