Superior Therapeutic Index in Lymphoma Therapy: CD30+ CD34+ Hematopoietic Stem Cells Resist a Chimeric Antigen Receptor T-cell Attack

Molecular Therapy

Volumn 24, Issue 8, 2016, Pages 1423-1434

  Hombach, Andreas A ^a   Görgens, André ^b   Chmielewski, Markus ^a   Murke, Florian ^b   Kimpel, Janine ^c   Giebel, Bernd ^b   Abken, Hinrich ^a  

^a UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^b UNIVERSITY HOSPITAL ESSEN   (Germany)

^c INNSBRUCK MEDICAL UNIVERSITY   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CD30 ANTIGEN; CD34 ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; GRANZYME B; SERINE PROTEASE PI9; SERINE PROTEASE SP6; SERINE PROTEINASE; SINGLE CHAIN FRAGMENT VARIABLE ANTIBODY; T LYMPHOCYTE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTICLE; BONE MARROW CELL; CANCER INHIBITION; CELL SUBPOPULATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; EMBRYO; ENZYME INACTIVATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOMA; LYMPHOMA CELL; LYMPHOPOIESIS; MOUSE; NEWBORN; NONHUMAN; T LYMPHOCYTE ACTIVATION; THERAPEUTIC INDEX;

EID: 84976385224     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2016.82     Document Type: Article

References (38)

1. Porter, DL, Levine, BL, Kalos, M, Bagg, A and June, CH (2011). Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 365: 725-733.
2. Grupp, SA, Kalos, M, Barrett, D, Aplenc, R, Porter, DL, Rheingold, SR et al. (2013). Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368: 1509-1518.
3. Nakamura, T, Lee, RK, Nam, SY, Al-Ramadi, BK, Koni, PA, Bottomly, K et al. (1997). Reciprocal regulation of CD30 expression on CD4+ T cells by IL-4 and IFN-gamma. J Immunol 158: 2090-2098.
4. Muta, H and Podack, ER (2013). CD30: from basic research to cancer therapy. Immunol Res 57: 151-158.
5. Kumar, A and Younes, A (2014). Role of CD30 targeting in malignant lymphoma. Curr Treat Options Oncol 15: 210-225.
6. Hombach, A, Heuser, C, Sircar, R, Tillmann, T, Diehl, V, Pohl, C et al. (1998). An anti-CD30 chimeric receptor that mediates CD3-zeta-independent T-cell activation against Hodgkin's lymphoma cells in the presence of soluble CD30. Cancer Res 58: 1116-1119.
7. Savoldo, B, Rooney, CM, Di Stasi, A, Abken, H, Hombach, A, Foster, AE et al. (2007). Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood 110: 2620-2630.
8. Hombach, A, Muche, JM, Gerken, M, Gellrich, S, Heuser, C, Pohl, C et al. (2001). T cells engrafted with a recombinant anti-CD30 receptor target autologous CD30(+) cutaneous lymphoma cells. Gene Ther 8: 891-895.
9. Beckmann, J, Scheitza, S, Wernet, P, Fischer, JC and Giebel, B (2007). Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins. Blood 109: 5494-5501.
10. Hombach, A, Hombach, AA and Abken, H (2010). Adoptive immunotherapy with genetically engineered T cells: modification of the IgG1 Fc 'spacer' domain in the extracellular moiety of chimeric antigen receptors avoids 'off-target' activation and unintended initiation of an innate immune response. Gene Ther 17: 1206-1213.
11. Kofler, DM, Chmielewski, M, Rappl, G, Hombach, A, Riet, T, Schmidt, A et al. (2011). CD28 costimulation Impairs the efficacy of a redirected t-cell antitumor attack in the presence of regulatory T cells which can be overcome by preventing Lck activation. Mol Ther 19: 760-767.
12. Zanotti, R, Trolese, A, Ambrosetti, A, Nadali, G, Visco, C, Ricetti, MM et al. (2002). Serum levels of soluble CD30 improve International Prognostic Score in predicting the outcome of advanced Hodgkin's lymphoma. Ann Oncol 13: 1908-1914.
13. Horie, R and Watanabe, T (1998). CD30: expression and function in health and disease. Semin Immunol 10: 457-470.
14. Görgens, A, Radtke, S, Möllmann, M, Cross, M, Dürig, J, Horn, PA et al. (2013). Revision of the human hematopoietic tree: granulocyte subtypes derive from distinct hematopoietic lineages. Cell Rep 3: 1539-1552.
15. Radtke, S, Görgens, A, Kordelas, L, Schmidt, M, Kimmig, KR, Köninger, A et al. (2015). CD133 allows elaborated discrimination and quantification of haematopoietic progenitor subsets in human haematopoietic stem cell transplants. Br J Haematol 169: 868-878.
16. de Bruin, PC, Gruss, HJ, van der Valk, P, Willemze, R and Meijer, CJ (1995). CD30 expression in normal and neoplastic lymphoid tissue: biological aspects and clinical implications. Leukemia 9: 1620-1627.
17. Sun, J, Bird, CH, Sutton, V, McDonald, L, Coughlin, PB, De Jong, TA 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.
18. El Haddad, N, Moore, R, Heathcote, D, Mounayar, M, Azzi, J, Mfarrej, B et al. (2011). The novel role of SERPINB9 in cytotoxic protection of human mesenchymal stem cells. J Immunol 187: 2252-2260.
19. El Haddad, N, Heathcote, D, Moore, R, Yang, S, Azzi, J, Mfarrej, B et al. (2011). Mesenchymal stem cells express serine protease inhibitor to evade the host immune response. Blood 117: 1176-1183.
20. Utermöhlen, O and Krönke, M (2007). Survival of priceless cells: active and passive protection of embryonic stem cells against immune destruction. Arch Biochem Biophys 462: 273-277.
21. Dotti, G, Gottschalk, S, Savoldo, B and Brenner, MK (2014). Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev 257: 107-126.
22. Grupp, SA, Kalos, M, Barrett, D, Aplenc, R, Porter, DL, Rheingold, SR et al. (2013). Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 368: 1509-1518.
23. Lee, DW, Kochenderfer, JN, Stetler-Stevenson, M, Cui, YK, Delbrook, C, Feldman, SA et al. (2015). T cells expressing CD19 chimeric antigen receptors for acute lymphoblastic leukaemia in children and young adults: a phase 1 dose-escalation trial. Lancet 385: 517-528.
24. Rappl, G, Riet, T, Awerkiew, S, Schmidt, A, Hombach, AA, Pfister, H et al. (2012). The CD3-zeta chimeric antigen receptor overcomes TCR Hypo-responsiveness of human terminal late-stage T cells. PLoS One 7: e30713.
25. Hombach, A, Köhler, H, Rappl, G and Abken, H (2006). Human CD4+ T cells lyse targeT cells via granzyme/perforin upon circumvention of MHC class II restriction by an antibody-like immunoreceptor. J Immunol 177: 5668-5675.
26. Kaiserman, D and Bird, PI (2010). Control of granzymes by serpins. Cell Death Differ 17: 586-595.
27. Graham, FL, Smiley, J, Russell, WC and Nairn, R (1977). Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36: 59-74.
28. Wolf, J, Kapp, U, Bohlen, H, Kornacker, M, Schoch, C, Stahl, B et al. (1996). Peripheral blood mononuclear cells of a patient with advanced Hodgkin's lymphoma give rise to permanently growing Hodgkin-Reed Sternberg cells. Blood 87: 3418-3428.
29. Schwegler, C, Dorn-Beineke, A, Nittka, S, Stocking, C and Neumaier, M (2005). Monoclonal anti-idiotype antibody 6G6.C4 fused to GM-CSF is capable of breaking tolerance to carcinoembryonic antigen (CEA) in CEA-transgenic mice. Cancer Res 65: 1925-1933.
30. Pohl, C, Renner, C, Schwonzen, M, Schobert, I, Liebenberg, V, Jung, W et al. (1993). CD30-specific AB1-AB2-AB3 internal image antibody network: potential use as antiidiotype vaccine against Hodgkin's lymphoma. Int J Cancer 54: 418-425.
31. Renner, C, Jung, W, Sahin, U, van Lier, R and Pfreundschuh, M (1995). The role of lymphocyte subsets and adhesion molecules in T cell-dependent cytotoxicity mediated by CD3 and CD28 bispecific monoclonal antibodies. Eur J Immunol 25: 2027-2033.
32. Weijtens, ME, Willemsen, RA, Hart, EH and Bolhuis, RL (1998). A retroviral vector system 'STITCH' in combination with an optimized single chain antibody chimeric receptor gene structure allows efficient gene transduction and expression in human T lymphocytes. Gene Ther 5: 1195-1203.
33. Hombach, A, Wieczarkowiecz, A, Marquardt, T, Heuser, C, Usai, L, Pohl, C et al. (2001). Tumor-specific T cell activation by recombinant immunoreceptors: CD3 zeta signaling and CD28 costimulation are simultaneously required for efficient IL-2 secretion and can be integrated into one combined CD28/CD3 zeta signaling receptor molecule. J Immunol 167: 6123-6131.
34. Hombach, A, Heuser, C, Gerken, M, Fischer, B, Lewalter, K, Diehl, V et al. (2000). T cell activation by recombinant FcepsilonRI gamma-chain immune receptors: an extracellular spacer domain impairs antigen-dependent T cell activation but not antigen recognition. Gene Ther 7: 1067-1075.
35. Giebel, B, Corbeil, D, Beckmann, J, Höhn, J, Freund, D, Giesen, K et al. (2004). Segregation of lipid raft markers including CD133 in polarized human hematopoietic stem and progenitor cells. Blood 104: 2332-2338.
36. Görgens, A, Ludwig, AK, Möllmann, M, Krawczyk, A, Dürig, J, Hanenberg, H et al. (2014). Multipotent hematopoietic progenitors divide asymmetrically to create progenitors of the lymphomyeloid and erythromyeloid lineages. Stem Cell Reports 3: 1058-1072.
37. Jost, LM, Kirkwood, JM and Whiteside, TL (1992). Improved short-and long-term XTT-based colorimetric cellular cytotoxicity assay for melanoma and other tumor cells. J Immunol Methods 147: 153-165.
38. Duan, F, Simeone, S, Wu, R, Grady, J, Mandoiu, I and Srivastava, PK (2012). Area under the curve as a tool to measure kinetics of tumor growth in experimental animals. J Immunol Methods 382: 224-228.