Trifunctional bispecific antibodies induce tumor-specific T cells and elicit a vaccination effect

Cancer Research

Volumn 72, Issue 16, 2012, Pages 3958-3966

  Eissler, Nina ^a   Ruf, Peter ^b   Mysliwietz, Josef ^a   Lindhofer, Horst ^b,c   Mocikat, Ralph ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b Trion Research GmbH   (Germany)

^c TRION Pharma GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BISPECIFIC ANTIBODY; CD3 ANTIGEN; GAMMA INTERFERON; GANGLIOSIDE GD2; IMMUNOGLOBULIN F(AB')2 FRAGMENT; IMMUNOGLOBULIN FC FRAGMENT; MELANOMA ANTIGEN; PEPTIDE; SUREK; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CANCER IMMUNIZATION; CANCER INHIBITION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; FEMALE; IMMUNE RESPONSE; IN VITRO STUDY; LYMPH NODE CELL; MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, BISPECIFIC; ANTIGENS, CD3; CANCER VACCINES; EPITOPES, T-LYMPHOCYTE; FEMALE; GANGLIOSIDES; LYMPHOCYTE ACTIVATION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; T-LYMPHOCYTES;

EID: 84865115651     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0146     Document Type: Article

References (48)

1. Beck A, Wurch T, Corvaia N. Therapeutic antibodies and derivatives: from the bench to the clinic. Curr Pharm Biotechnol 2008;9:421-2.
2. Beck A, Wurch T, Bailly C, Corvaia N. Strategies and challenges for the next generation of therapeutic antibodies. Nat Rev Immunol 2010;10:345-52.
3. Peipp M, Valerius T. Bispecific antibodies targeting cancer cells. Biochem Soc Trans 2002;30:507-11. (Pubitemid 35001586)
4. Jäger M, Schoberth A, Ruf P, Hess J, Lindhofer H. The trifunctional antibody ertumaxomab destroys tumor cells that express low levels of humanepidermal growthfactor receptor 2.CancerRes2009;69:4270-6.
5. Fanger MW, Guyre PM. Bispecific antibodies for targeted cellular cytotoxicity. Trends Biotechnol 1991;9:375-80. (Pubitemid 121003140)
6. Fanger MW, Segal DM, Wunderlich JR. Going both ways: bispecific antibodies and targeted cellular cytotoxicity. FASEB J 1990;4:2846-9.
7. Weiner LM, Clark JI, Ring DB, Alpaugh RK. Clinical development of 2B1, a bispecific murine monoclonal antibody targeting c-erbB-2 and Fc gamma RIII. J Hematother 1995;4:453-6.
8. Heijnen IA, Rijks LJ, Schiel A, Stockmeyer B, van Ojik HH, Dechant M, et al. Generation of HER-2/neu-specific cytotoxic neutrophils in vivo: efficient arming of neutrophils by combined administration of granulocyte colony-stimulating factor and Fcgamma receptor I bispecific antibodies. J Immunol 1997;159:5629-39. (Pubitemid 127470094)
9. Michon J, Moutel S, Barbet J, Romet-Lemonne JL, Deo YM, Fridman WH, et al. In vitro killing of neuroblastoma cells by neutrophils derived from granulocyte colony-stimulating factor-treated cancer patients using an anti-disialoganglioside/anti-Fc gamma RI bispecific antibody. Blood 1995;86:1124-30.
10. Boussiotis VA, Barber DL, Nakarai T, Freeman GJ, Gribben JG, Bernstein GM, et al. Prevention of T cell anergy by signaling through the gamma c chain of the IL-2 receptor. Science 1994;266:1039-42.
11. Linsley PS, Ledbetter JA. The role of the CD28 receptor during T cell responses to antigen. Annu Rev Immunol 1993;11:191-212. (Pubitemid 23115006)
12. Zeidler R, Reisbach G, Wollenberg B, Lang S, Chaubal S, Schmitt B, et al. Simultaneous activation of T cells and accessory cells by a new class of intact bispecific antibody results in efficient tumor cell killing. J Immunol 1999;163:1246-52. (Pubitemid 29352740)
13. Zeidler R, Mysliwietz J, Csanady M, Walz A, Ziegler I, Schmitt B, et al. The Fc-region of a new class of intact bispecific antibody mediates activation of accessory cells and NK cells and induces direct phagocytosis of tumour cells. Br J Cancer 2000;83:261-6. (Pubitemid 30411727)
14. Ruf P, Lindhofer H. Induction of a long-lasting antitumor immunity by a trifunctional bispecific antibody. Blood 2001;98:2526-34.
15. Haraguchi M, Yamashiro S, Yamamoto A, Furukawa K, Takamiya K, Lloyd KO, et al. Isolation of GD3 synthase gene by expression cloning of GM3 alpha-2,8-sialyltransferase cDNA using anti-GD2 monoclonal antibody. Proc Natl Acad Sci USA 1994;91:10455-9.
16. Ragupathi G, Livingston PO, Hood C, Gathuru J, Krown SE, Chapman PB, et al. Consistent antibody response against ganglioside GD2 induced in patients with melanoma by a GD2 lactone-keyhole limpet hemocyanin conjugate vaccine plus immunological adjuvant QS-21. Clin Cancer Res 2003;9:5214-20. (Pubitemid 37413571)
17. Navid F, Santana VM, Barfield RC. Anti-GD2 antibody therapy for GD2-expressing tumors. Curr Cancer Drug Targets 2010;10:200-9.
18. Ruf P, Jäger M, Ellwart J, Wosch S, Kusterer E, Lindhofer H. Two new trifunctional antibodies for the therapy of human malignant melanoma. Int J Cancer 2004;108:725-32. (Pubitemid 38076404)
19. Fidler IJ. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 1975;35:218-24.
20. Nicolson GL, Brunson KW, Fidler IJ. Specificity of arrest, survival, and growth of selected metastatic variant cell lines. Cancer Res 1978;38:4105-11. (Pubitemid 9060148)
21. Becker JC, Varki N, Gillies SD, Furukawa K, Reisfeld RA. Long-lived and transferable tumor immunity in mice after targeted interleukin-2 therapy. J Clin Invest 1996;98:2801-4. (Pubitemid 26427408)
22. Lindhofer H, Mocikat R, Steipe B, Thierfelder S. Preferential species-restricted heavy/light chain pairing in rat/mouse quadromas. Implications for a single-step purification of bispecific antibodies. J Immunol 1995;155:219-25.
23. Eggert AO, Andersen MH, Voigt H, Schrama D, Kampgen E, Straten PT, et al. Characterization of mouse MAGE-derived H-2Kb-restricted CTL epitopes. Eur J Immunol 2004;34:3285-90. (Pubitemid 39549407)
24. Mansour M, Pohajdak B, KastWM,Fuentes-Ortega A, Korets-Smith E, Weir GM, et al. Therapy of established B16-F10 melanomatumors by a single vaccination of CTL/T helper peptides in VacciMax. J Transl Med 2007;5:20.
25. Overwijk WW, Tsung A, Irvine KR, Parkhurst MR, Goletz TJ, Tsung K, et al. gp100/pmel 17 is a murine tumor rejection antigen: induction of "self"-reactive, tumoricidal T cells using high-affinity, altered peptide ligand. J Exp Med 1998;188:277-86. (Pubitemid 28357756)
26. Sebastian M, Passlick B, Friccius-Quecke H, Jäger M, Lindhofer H, Kanniess F, et al. Treatment of non-small cell lung cancer patients with the trifunctionalmonoclonal antibodycatumaxomab(anti-EpCAMx anti-CD3): a phase I study. Cancer Immunol Immunother 2007;56:1637-44. (Pubitemid 47094393)
27. Ruf P, Schäfer B, Eißler N, Mocikat R, Hess J, Wosch S, et al. Ganglioside GD2-specific trifunctional surrogate antibody Surek demonstrates therapeutic activity against experimental melanoma. Manuscript submitted.
28. Bloom MB, Perry-Lalley D, Robbins PF, Li Y, el-Gamil M, Rosenberg SA, et al. Identification of tyrosinase-related protein 2 as a tumor rejection antigen for the B16 melanoma. J Exp Med 1997;185:453-9. (Pubitemid 27078363)
29. Lindhofer H, Menzel H, Günther W, Hültner L, Thierfelder S. Bispecific antibodies target operationally tumor-specific antigens in two leukemia relapse models. Blood 1996;88:4651-8. (Pubitemid 26419149)
30. Heiss MM, Ströhlein MA, Jäger M, Kimmig R, Burges A, Schoberth A, et al. Immunotherapy of malignant ascites with trifunctional antibodies. Int J Cancer 2005;117:435-43. (Pubitemid 41429567)
31. Heiss MM, Murawa P, Koralewski P, Kutarska E, Kolesnik OO, Ivanchenko VV, et al. The trifunctional antibody catumaxomab for the treatment of malignant ascites due to epithelial cancer: results of a prospective randomized phase II/III trial. Int J Cancer 2010;127:2209-21.
32. Ruf P, Kluge M, Jäger M, Burges A, Volovat C, Heiss MM, et al. Pharmacokinetics, immunogenicity and bioactivity of the therapeutic antibody catumaxomab intraperitoneally administered to cancer patients. Br J Clin Pharmacol 2010;69:617-25.
33. Lindhofer H, Hess J, Ruf P. Triomab antibodies for cancer therapy. In: Kontermann R, editor. Bispecific antibodies. Berlin: Springer; 2011. p. 289-312.
34. Cheresh DA, Honsik CJ, Staffileno LK, Jung G, Reisfeld RA. Disialoganglioside GD3 on human melanoma serves as a relevant target antigen for monoclonal antibody-mediated tumor cytolysis. Proc Natl Acad Sci USA 1985;82:5155-9. (Pubitemid 16242819)
35. Hellström I, Brankovan V, Hellström KE. Strong antitumor activities of IgG3 antibodies to a human melanoma-associated ganglioside. Proc Natl Acad Sci USA 1985;82:1499-502. (Pubitemid 15120570)
36. Mueller BM, Romerdahl CA, Gillies SD, Reisfeld RA. Enhancement of antibody-dependent cytotoxicity with a chimeric anti-GD2 antibody. J Immunol 1990;144:1382-6. (Pubitemid 20072910)
37. Becker JC, Pancook JD, Gillies SD, Mendelsohn J, Reisfeld RA. Eradication of human hepatic and pulmonary melanoma metastases in SCID mice by antibody-interleukin 2 fusion proteins. Proc Natl Acad Sci USA 1996;93:2702-7. (Pubitemid 26114312)
38. Hank JA, Surfus JE, Gan J, Jaeger P, Gillies SD, Reisfeld RA, et al. Activation of human effector cells by a tumor reactive recombinant anti-ganglioside GD2 interleukin-2 fusion protein (ch14.18-IL2). Clin Cancer Res 1996;2:1951-9. (Pubitemid 27006627)
39. Becker JC, Pancook JD, Gillies SD, Furukawa K, Reisfeld RA. T cell-mediated eradication of murine metastatic melanoma induced by targeted interleukin 2 therapy. J Exp Med 1996;183:2361-6. (Pubitemid 26158928)
40. Ruf P, Jäger M, Foerster B, Martinius D, Seimetz D, Lindhofer H. Humoral tumor-associated immune responses induced by catumaxomab in patients with malignant ascites. J Clin Oncol 2011;29: Suppl abstr 2575.
41. Egeter O, Mocikat R, Ghoreschi K, Dieckmann A, Röcken M. Eradication of disseminated lymphomas with CpG-DNA activated T helper type 1 cells from nontransgenic mice. Cancer Res 2000;60:1515-20. (Pubitemid 30183417)
42. Lüking C, Kronenberger K, Frankenberger B, Nöbner E, Röcken M, Mocikat R. Antitumor effector functions of T cells are dependent on in vivo priming and restricted T-cell receptor expression. Int J Cancer 2008;122:2280-5. (Pubitemid 351542332)
43. Schüler T, Qin Z, Ibe S, Noben-Trauth N, Blankenstein T. T helper cell type 1-associated and cytotoxic T lymphocyte-mediated tumor immunity is impaired in interleukin 4-deficient mice. J Exp Med 1999;189:803-10. (Pubitemid 29189685)
44. O'Garra A, Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat Rev Immunol 2007;7:425-8. (Pubitemid 46834852)
45. Kronenberger K, Dieckmann A, Selmayr M, Strehl J, Wahl U, Lindhofer H, et al. Impact of the lymphoma idiotype on in vivo tumor protection in a vaccination model based on targeting antigens to antigen-presenting cells. Blood 2002;99:1327-31. (Pubitemid 34547088)
46. Kronenberger K, Nößner E, Frankenberger B, Wahl U, Dreyling M, Hallek M, et al. A polyvalent cellular vaccine induces T-cell responses against specific self-antigens overexpressed in chronic lymphocytic B-cell leukemia. J Immunother 2008;31:723-30.
47. Hilchey SP, Hyrien O, Mosmann TR, Livingstone AM, Friedberg JW, Young F, et al. Rituximab immunotherapy results in the induction of a lymphoma idiotype-specific T-cell response in patients with follicular lymphoma: support for a "vaccinal effect" of rituximab. Blood 2009;113:3809-12.
48. Abès R, Gélizé E, Fridman WH, Teillaud JL. Long-lasting antitumor protection by anti-CD20 antibody through cellular immune response. Blood 2010;116:926-34.