γδ T cell activation by bispecific antibodies

Cellular Immunology

Volumn 296, Issue 1, 2015, Pages 41-49

  Oberg, Hans Heinrich ^a   Kellner, Christian ^a   Gonnermann, Daniel ^a   Peipp, Matthias ^a   Peters, Christian ^a   Sebens, Susanne ^a   Kabelitz, Dieter ^a   Wesch, Daniela ^a  

^a UNIVERSITY OF KIEL   (Germany)

Author keywords

Bispecific antibodies; Cytotoxicity; Gammadelta T lymphocytes; Human; Pancreatic ductal adenocarcinoma

Indexed keywords

BISPECIFIC ANTIBODY; CD3 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GRANZYME; I KAPPA B; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; RAS PROTEIN; T LYMPHOCYTE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA; ZOLEDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; ERBB2 PROTEIN, HUMAN; LYMPHOCYTE ANTIGEN RECEPTOR; PYROPHOSPHORIC ACID DERIVATIVE; T-CELL RECEPTOR VGAMMA9, HUMAN;

ARTICLE; CELL CONTACT; CELL DEATH; CELL KILLING; COCULTURE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; ENHANCER REGION; GAMMA DELTA T LYMPHOCYTE; GLYCOSYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE PROLIFERATION; PANCREAS ADENOCARCINOMA; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TUMOR CELL; TUMOR GROWTH; BIOSYNTHESIS; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CYTOTOXICITY; GENETICS; IMMUNOLOGY; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; NEOPLASMS; TRANSPLANTATION; TUMOR CELL LINE;

ANTIBODIES, BISPECIFIC; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; CYTOTOXICITY, IMMUNOLOGIC; DIPHOSPHATES; DIPHOSPHONATES; HUMANS; IMMUNOTHERAPY; LYMPHOCYTE ACTIVATION; NEOPLASMS; RECEPTOR, ERBB-2; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA;

EID: 84930570731     PISSN: 00088749     EISSN: 10902163     Source Type: Journal    
DOI: 10.1016/j.cellimm.2015.04.009     Document Type: Article

References (50)

1. Garber K. Bispecific antibodies rise again. Nat. Rev. Drug Discov. 2014, 13:799-801.
2. Weidle U.H., Kontermann R.E., Brinkmann U. Tumor-antigen-binding bispecific antibodies for cancer treatment. Semin. Oncol. 2014, 41:653-660.
3. Staerz U.D., Kanagawa O., Bevan M.J. Hybrid antibodies can target sites for attack by T cells. Nature 1985, 314:628-631.
4. Bargou R., Leo E., Zugmaier G., Klinger M., Goebeler M., Knop S., Noppeney R., Viardot A., Hess G., Schuler M., Einsele H., Brandl C., Wolf A., Kirchinger P., Klappers P., Schmidt M., Riethmuller G., Reinhardt C., Baeuerle P.A., Kufer P. Tumor regression in cancer patients by very low doses of a T cell-engaging antibody. Science 2008, 321:974-977.
5. Sanford M. Blinatumomab: first global approval. Drugs 2015, 75:321-327.
6. Kellner C., Bruenke J., Stieglmaier J., Schwemmlein M., Schwenkert M., Singer H., Mentz K., Peipp M., Lang P., Oduncu F., Stockmeyer B., Fey G.H. A novel CD19-directed recombinant bispecific antibody derivative with enhanced immune effector functions for human leukemic cells. J. Immunother. 2008, 31:871-884.
7. Kugler M., Stein C., Kellner C., Mentz K., Saul D., Schwenkert M., Schubert I., Singer H., Oduncu F., Stockmeyer B., Mackensen A., Fey G.H. A recombinant trispecific single-chain Fv derivative directed against CD123 and CD33 mediates effective elimination of acute myeloid leukaemia cells by dual targeting. Br. J. Haematol. 2010, 150:574-586.
8. Shahied L.S., Tang Y., Alpaugh R.K., Somer R., Greenspon D., Weiner L.M. Bispecific minibodies targeting HER2/neu and CD16 exhibit improved tumor lysis when placed in a divalent tumor antigen binding format. J. Biol. Chem. 2004, 279:53907-53914.
9. Glorius P., Baerenwaldt A., Kellner C., Staudinger M., Dechant M., Stauch M., Beurskens F.J., Parren P.W., Winkel J.G., Valerius T., Humpe A., Repp R., Gramatzki M., Nimmerjahn F., Peipp M. The novel tribody [(CD20)(2)×CD16] efficiently triggers effector cell-mediated lysis of malignant B cells. Leukemia 2013, 27:190-201.
10. Kellner C., Bruenke J., Horner H., Schubert J., Schwenkert M., Mentz K., Barbin K., Stein C., Peipp M., Stockmeyer B., Fey G.H. Heterodimeric bispecific antibody-derivatives against CD19 and CD16 induce effective antibody-dependent cellular cytotoxicity against B-lymphoid tumor cells. Cancer Lett. 2011, 303:128-139.
11. Schoonjans R., Willems A., Schoonooghe S., Fiers W., Grooten J., Mertens N. Fab chains as an efficient heterodimerization scaffold for the production of recombinant bispecific and trispecific antibody derivatives. J. Immunol. 2000, 165:7050-7057.
12. Helm O., Mennrich R., Petrick D., Goebel L., Freitag-Wolf S., Roder C., Kalthoff H., Röcken C., Sipos B., Kabelitz D., Schafer H., Oberg H.H., Wesch D., Sebens S. Comparative characterization of stroma cells and ductal epithelium in chronic pancreatitis and pancreatic ductal adenocarcinoma. PLoS One 2014, 9:e94357.
13. Lunardi S., Muschel R.J., Brunner T.B. The stromal compartments in pancreatic cancer: are there any therapeutic targets?. Cancer Lett. 2014, 343:147-155.
14. Siegel R., Ma J., Zou Z., Jemal A. Cancer statistics, 2014. CA Cancer J. Clin. 2014, 64(2014):9-29.
15. Harder J., Ihorst G., Heinemann V., Hofheinz R., Moehler M., Buechler P., Kloeppel G., Röcken C., Bitzer M., Boeck S., Endlicher E., Reinacher-Schick A., Schmoor C., Geissler M. Multicentre phase II trial of trastuzumab and capecitabine in patients with HER2 overexpressing metastatic pancreatic cancer. Br. J. Cancer 2012, 106:1033-1038.
16. Tsiambas E., Karameris A., Dervenis C., Lazaris A.C., Giannakou N., Gerontopoulos K., Patsouris E. HER2/neu expression and gene alterations in pancreatic ductal adenocarcinoma: a comparative immunohistochemistry and chromogenic in situ hybridization study based on tissue microarrays and computerized image analysis. JOP 2006, 7:283-294.
17. Benzaid I., Monkkonen H., Stresing V., Bonnelye E., Green J., Monkkonen J., Touraine J.L., Clezardin P. High phosphoantigen levels in bisphosphonate-treated human breast tumors promote Vγ9Vδ2 T-cell chemotaxis and cytotoxicity in vivo. Cancer Res. 2011, 71:4562-4572.
18. Gober H.J., Kistowska M., Angman L., Jeno P., Mori L., De L.G. Human T cell receptor γδ cells recognize endogenous mevalonate metabolites in tumor cells. J. Exp. Med. 2003, 197:163-168.
19. Bennouna J., Bompas E., Neidhardt E.M., Rolland F., Philip I., Galea C., Salot S., Saiagh S., Audrain M., Rimbert M., Lafaye-de M.S., Tiollier J., Negrier S. Phase-I study of Innacell γδ, an autologous cell-therapy product highly enriched in γ9δ2 T lymphocytes, in combination with IL-2, in patients with metastatic renal cell carcinoma. Cancer Immunol. Immunother. 2008, 57:1599-1609.
20. Bouet-Toussaint F., Cabillic F., Toutirais O., Le G.M., Thomas d.L.P., Daniel P., Genetet N., Meunier B., Dupont-Bierre E., Boudjema K., Catros V. Vγ9Vδ2 T cell-mediated recognition of human solid tumors potential for immunotherapy of hepatocellular and colorectal carcinomas. Cancer Immunol. Immunother. 2008, 57:531-539.
21. Dieli F., Vermijlen D., Fulfaro F., Caccamo N., Meraviglia S., Cicero G., Roberts A., Buccheri S., D'Asaro M., Gebbia N., Salerno A., Eberl M., Hayday A.C. Targeting human γδ T cells with zoledronate and interleukin-2 for immunotherapy of hormone-refractory prostate cancer. Cancer Res. 2007, 67:7450-7457.
22. Meraviglia S., Eberl M., Vermijlen D., Todaro M., Buccheri S., Cicero G., La M.C., Guggino G., D'Asaro M., Orlando V., Scarpa F., Roberts A., Caccamo N., Stassi G., Dieli F., Hayday A.C. In vivo manipulation of Vγ9Vδ2 T cells with zoledronate and low-dose interleukin-2 for immunotherapy of advanced breast cancer patients. Clin. Exp. Immunol. 2010, 161:290-297.
23. Wilhelm M., Smetak M., Schaefer-Eckart K., Kimmel B., Birkmann J., Einsele H., Kunzmann V. Successful adoptive transfer and in vivo expansion of haploidentical γδ T cells. J. Transl. Med. 2014, 12. 10.1186/1479-5876-12-45.
24. Hintz M., Reichenberg A., Altincicek B., Bahr U., Gschwind R.M., Kollas A.K., Beck E., Wiesner J., Eberl M., Jomaa H. Identification of (E)-4-hydroxy-3-methyl-but-2-enyl pyrophosphate as a major activator for human γδ T cells in Escherichia coli. FEBS Lett. 2001, 509:317-322.
25. Oberg H.H., Peipp M., Kellner C., Sebens S., Krause S., Petrick D., Adam-Klages S., Röcken C., Becker T., Vogel I., Weisner D., Freitag-Wolf S., Gramatzki M., Kabelitz D., Wesch D. Novel bispecific antibodies increase γδ T-cell cytotoxicity against pancreatic cancer cells. Cancer Res. 2014, 74:1349-1360.
26. Peters C., Oberg H.H., Kabelitz D., Wesch D. Phenotype and regulation of immunosuppressive Vδ2-expressing γδ T cells. Cell. Mol. Life Sci. 2013, 71:1943-1960.
27. Kellner C., Maurer T., Hallack D., Repp R., van de Winkel J.G., Parren P.W., Valerius T., Humpe A., Gramatzki M., Peipp M. Mimicking an induced self phenotype by coating lymphomas with the NKp30 ligand B7-H6 promotes NK cell cytotoxicity. J. Immunol. 2012, 189:5037-5046.
28. Gonnermann D., Oberg H.H., Kellner C., Peipp M., Sebens S., Kabelitz D., Wesch D. Resistance of cyclooxygenase-2 expressing pancreatic ductal adenocarcinoma cells against γδ T cell cytotoxicity. Oncoimmunology 2014, 10.4161/2162402X.2014.988460.
29. Oberg H.H., Kellner C., Peipp M., Sebens S., Adam-Klages S., Gramatzki M., Kabelitz D., Wesch D. Monitoring circulating γδ T cells in cancer patients to optimize γδ T cell-based immunotherapy. Front. Immunol. 2014, 5. 10.3389/fimmu.2014.00643.
30. Pechhold K., Pohl T., Kabelitz D. Rapid quantification of lymphocyte subsets in heterogeneous cell populations by flow cytometry. Cytometry 1994, 16:152-159.
31. Kobayashi H., Tanaka Y., Yagi J., Minato N., Tanabe K. Phase I/II study of adoptive transfer of γδ T cells in combination with zoledronic acid and IL-2 to patients with advanced renal cell carcinoma. Cancer Immunol. Immunother. 2011, 60:1075-1084.
32. Wesch D., Marx S., Kabelitz D. Comparative analysis of αβ and γδ T cell activation by Mycobacterium tuberculosis and isopentenyl pyrophosphate. Eur. J. Immunol. 1997, 27:952-956.
33. Chen H.C., Dieli F., Eberl M. An unconventional TRAIL to cancer therapy. Eur. J. Immunol. 2013, 43:3159-3162.
34. Dokouhaki P., Schuh N.W., Joe B., Allen C.A., Der S.D., Tsao M.S., Zhang L. NKG2D regulates production of soluble TRAIL by ex vivo expanded human γδ T cells. Eur. J. Immunol. 2013, 43:3175-3182.
35. Kabelitz D., Wesch D., Pitters E., Zoller M. Characterization of tumor reactivity of human Vγ9Vδ2 γδ T cells in vitro and in SCID mice in vivo. J. Immunol. 2004, 173:6767-6776.
36. Ungefroren H., Voss M., Jansen M., Roeder C., Henne-Bruns D., Kremer B., Kalthoff H. Human pancreatic adenocarcinomas express Fas and Fas ligand yet are resistant to Fas-mediated apoptosis. Cancer Res. 1998, 58:1741-1749.
37. Capietto A.H., Martinet L., Fournie J.J. How tumors might withstand γδ T-cell attack. Cell. Mol. Life Sci. 2011, 68:2433-2442.
38. Hinz S., Pagerols-Raluy L., Oberg H.H., Ammerpohl O., Grussel S., Sipos B., Grutzmann R., Pilarsky C., Ungefroren H., Saeger H.D., Klöppel G., Kabelitz D., Kalthoff H. Foxp3 expression in pancreatic carcinoma cells as a novel mechanism of immune evasion in cancer. Cancer Res. 2007, 67:8344-8350.
39. Alarcon B., De V.J., Pettey C., Boylston A., Yssel H., Terhorst C., Spits H. The T-cell receptor gamma chain-CD3 complex: implication in the cytotoxic activity of a CD3+ CD4- CD8- human natural killer clone. Proc. Natl. Acad. Sci. U.S.A. 1987, 84:3861-3865.
40. Dopfer E.P., Hartl F.A., Oberg H.H., Siegers G.M., Yousefi O.S., Kock S., Fiala G.J., Garcillan B., Sandstrom A., Alarcon B., Regueiro J.R., Kabelitz D., Adams E.J., Minguet S., Wesch D., Fisch P., Schamel W.W. The CD3 conformational change in the γδ T cell receptor is not triggered by antigens but can be enforced to enhance tumor killing. Cell Rep. 2014, 7:1704-1715.
41. Siegers G.M., Swamy M., Fernandez-Malave E., Minguet S., Rathmann S., Guardo A.C., Perez-Flores V., Regueiro J.R., Alarcon B., Fisch P., Schamel W.W. Different composition of the human and the mouse γδ T cell receptor explains different phenotypes of CD3γ and CD3δ immunodeficiencies. J. Exp. Med. 2007, 204:2537-2544.
42. Martinez-Martin N., Risueno R.M., Morreale A., Zaldivar I., Fernandez-Arenas E., Herranz F., Ortiz A.R., Alarcon B. Cooperativity between T cell receptor complexes revealed by conformational mutants of CD3ε. Sci. Signal. 2009, 2. 10.1126/scisignal.2000402.
43. Minguet S., Schamel W.W. A permissive geometry model for TCR-CD3 activation. Trends Biochem. Sci. 2008, 33:51-57.
44. Arnett K.L., Harrison S.C., Wiley D.C. Crystal structure of a human CD3-ε/δ dimer in complex with a UCHT1 single-chain antibody fragment. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:16268-16273.
45. R. Hofmeister, B. Kohleisen, U. Lenkeri-Schuetz, C. Itin, P.A. Baeuerle, F.J. Carr, A.A. Hamilton, S. Williams. Multispecific deimmunized CD3 binders. [WO2005/040220], 2005.
46. Kjer-Nielsen L., Dunstone M.A., Kostenko L., Ely L.K., Beddoe T., Mifsud N.A., Purcell A.W., Brooks A.G., McCluskey J., Rossjohn J. Crystal structure of the human T cell receptor CD3 ε γ heterodimer complexed to the therapeutic mAb OKT3. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:7675-7680.
47. Coscia M., Vitale C., Peola S., Foglietta M., Rigoni M., Griggio V., Castella B., Angelini D., Chiaretti S., Riganti C., Guarini A., Drandi D., Ladetto M., Bosia A., Foa R., Battistini L., Boccadoro M., Fournie J.J., Massaia M. Dysfunctional Vγ9Vδ2 T cells are negative prognosticators and markers of dysregulated mevalonate pathway activity in chronic lymphocytic leukemia cells. Blood 2012, 120:3271-3279.
48. Mariani S., Muraro M., Pantaleoni F., Fiore F., Nuschak B., Peola S., Foglietta M., Palumbo A., Coscia M., Castella B., Bruno B., Bertieri R., Boano L., Boccadoro M., Massaia M. Effector γδ T cells and tumor cells as immune targets of zoledronic acid in multiple myeloma. Leukemia 2005, 19:664-670.
49. Sicard H., Ingoure S., Luciani B., Serraz C., Fournie J.J., Bonneville M., Tiollier J., Romagne F. In vivo immunomanipulation of Vγ9Vd2 T cells with a synthetic phosphoantigen in a preclinical nonhuman primate model. J. Immunol. 2005, 175:5471-5480.
50. Wilhelm M., Kunzmann V., Eckstein S., Reimer P., Weissinger F., Ruediger T., Tony H.P. γδ T cells for immune therapy of patients with lymphoid malignancies. Blood 2003, 102:200-206.