Shared target antigens on cancer cells and tissue stem cells: go or no-go for CAR T cells?

Expert Review of Clinical Immunology

Volumn 13, Issue 2, 2017, Pages 151-155

  Hombach, Andreas A ^a,b   Abken, Hinrich ^a,b  

^a UNIVERSITY OF COLOGNE   (Germany)

^b UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

Author keywords

Adoptive cell therapy; CAR; CD123; CD30; chimeric antigen receptor; hematopoietic stem and progenitor cell; HSPCs; SP6 PI9; stem cell; T cell

Indexed keywords

CD123 ANTIGEN; CD30 ANTIGEN; CELL ANTIGEN; CHIMERIC ANTIGEN RECEPTOR; FOLATE RECEPTOR 2; TUMOR ANTIGEN; AUTOANTIGEN; HYBRID PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; T LYMPHOCYTE RECEPTOR;

ACUTE MYELOBLASTIC LEUKEMIA; ANTIGEN EXPRESSION; CANCER CELL; CANCER CELL DESTRUCTION; CANCER STEM CELL; CANCER TISSUE; CELL LINE; CELL LINEAGE; CELL MATURATION; CELL THERAPY; CYTOLYSIS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; INDUCED PLURIPOTENT STEM CELL; LYMPHOMA CELL; NONHUMAN; PROGENITOR CELL LINE; REVIEW; STEM CELL TRANSPLANTATION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TARGET CELL; ADOPTIVE IMMUNOTHERAPY; ADULT STEM CELL; ANIMAL; AUTOIMMUNITY; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR MIMICRY; NEOPLASMS; PHYSIOLOGY; PROCEDURES; TRANSPLANTATION; TRENDS;

ADULT STEM CELLS; ANIMALS; ANTIGENS, NEOPLASM; AUTOANTIGENS; AUTOIMMUNITY; HUMANS; IMMUNOTHERAPY, ADOPTIVE; MOLECULAR MIMICRY; NEOPLASMS; RECEPTORS, ANTIGEN, T-CELL; RECOMBINANT FUSION PROTEINS; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES;

EID: 85008153195     PISSN: 1744666X     EISSN: 17448409     Source Type: Journal    
DOI: 10.1080/1744666X.2016.1221763     Document Type: Review

References (50)

1. Almåsbak H, Aarvak T, Vemuri MC., CAR T cell therapy:a game changer in cancer treatment. J Immunol Res. 2016. doi:10.1155/2016/5474602. Epub 2016 May 19.
2. Maus MV, June CH. Making better chimeric antigen receptors for adoptive T-cell THERAPY. Clin Cancer Res. 2016;22(8):1875–1884.
3. Weijtens ME, Willemsen RA, Valerio D, et al. Single chain Ig/gamma gene-redirected human T lymphocytes produce cytokines, specifically lyse tumor cells, and recycle lytic capacity. J Immunol. 1996;157(2):836–843.
4. Nolan KF, Yun CO, Akamatsu Y, et al. Bypassing immunization:optimized design of “designer T cells” against carcinoembryonic antigen (CEA)-expressing tumors, and lack of suppression by soluble CEA. Clin Cancer Res. 1999;5(12):3928–3941.
5. Hombach A, Muche JM, Gerken M, et al. T cells engrafted with a recombinant anti-CD30 receptor target autologous CD30(+) cutaneous lymphoma cells. Gene Ther. 2001;8(11):891–895.
6. Maude S, Barrett DM. Current status of chimeric antigen receptor therapy for haematological malignancies. Br J Haematol. 2016;172(1):11–22.
7. Hombach AA, Görgens A, Chmielewski M, et al. Superior therapeutic index in lymphoma therapy:CD30(+) CD34(+) hematopoietic stem cells resist a chimeric antigen receptor (CAR) T cell attack. Mol Ther. 2016. doi:10.1038/mt.2016.82. [Epub ahead of print]• First report that an antigen on hematopoietic stem cells can be used as target for cancer cells without killing the healthy stem cells.
8. Lynn RC, Poussin M, Kalota A, et al. Targeting of folate receptor β on acute myeloid leukemia blasts with chimeric antigen receptor-expressing T cells. Blood. 2015;125(22):3466–3476.
9. Lynn RC, Feng Y, Schutsky K, et al. High-affinity FRβ-specific CAR T cells eradicate AML and normal myeloid lineage without HSC toxicity. Leukemia. 2016. doi:10.1038/leu.2016.35. Epub 2016 Feb 22.• Report on differential sensitivity of hematopoietic stem cells and leukemia cells toward a CAR T-cell attack.
10. Stein H, Mason DY, Gerdes J, et al. The expression of the Hodgkin’s disease associated antigen Ki-1 in reactive and neoplastic lymphoid tissue:evidence that reed-sternberg cells and histiocytic malignancies are derived from activated lymphoid cells. Blood. 1985;66(4):848–858.
11. Agrawal B, Reddish M, Longenecker BM. CD30 expression on human CD8+ T cells isolated from peripheral blood lymphocytes of normal donors. J Immunol. 1996;157(8):3229–3234.
12. von Wasielewski R, Mengel M, Fischer R, et al. Classical Hodgkin’s disease. Clinical impact of the immunophenotype. Am J Pathol. 1997;151(4):1123–1130.
13. von Wasielewski R, Werner M, Fischer R, et al. Lymphocyte-predominant Hodgkin’s disease. An immunohistochemical analysis of 208 reviewed Hodgkin’s disease cases from the German Hodgkin study group. Am J Pathol. 1997;150(6):1925–1932.
14. de Bruin PC, Gruss HJ, van der Valk P, et al. CD30 expression in normal and neoplastic lymphoid tissue:biological aspects and clinical implications. Leukemia. 1995;9(10):1620–1627.
15. Chiarle R, Podda A, Prolla G, et al. CD30 in normal and neoplastic cells. Clin Immunol. 1999;90(2):157–164.
16. Latza U, Foss HD, Dürkop H, et al. CD30 antigen in embryonal carcinoma and embryogenesis and release of the soluble molecule. Am J Pathol. 1995;146(2):463–471.
17. Dürkop H, Foss HD, Eitelbach F, et al. Expression of the CD30 antigen in non-lymphoid tissues and cells. J Pathol. 2000;190(5):613–618.
18. Mechtersheimer G, Möller P. Expression of Ki-1 antigen (CD30) in mesenchymal tumors. Cancer. 1990;66(8):1732–1737.
19. Aggerholm-Pedersen N, Bærentzen S, Holmberg Jørgensen JP, et al. A rare case of CD30(+), radiation-induced cutaneous angiosarcoma misdiagnosed as T-cell lymphoma. J Clin Oncol. 2011;29(13):e362–364.
20. Schwarting R, Gerdes J, Dürkop H, et al. BER-H2:a new anti-Ki-1 (CD30) monoclonal antibody directed at a formol-resistant epitope. Blood. 1989;74(5):1678–1689.
21. Muta H, Podack ER. CD30:from basic research to cancer therapy. Immunol Res. 2013;57(1–3):151–158.
22. Abujarour R, Valamehr B, Robinson M, et al. Optimized surface markers for the prospective isolation of high-quality hiPSCs using flow cytometry selection. Sci Rep. 2013;3:1179.
23. Chung T-L, Turner JP, Thaker NY, et al. Ascorbate promotes epigenetic activation of CD30 in human embryonic stem cells. Stem Cells. 2010;28(10):1782–1793.
24. Mateizel I, Spits C, Verloes A, et al. Characterization of CD30 expression in human embryonic stem cell lines cultured in serum-free media and passaged mechanically. Hum Reprod. 2009;24(10):2477–2489.
25. Beckmann J, Scheitza S, Wernet P, et al. Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment:identification of asymmetrically segregating proteins. Blood. 2007;109(6):5494–5501.
26. Dotti G, Gottschalk S, Savoldo B, et al. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev. 2014;257(1):107–126.
27. Savoldo B, Rooney CM, Di Stasi A, et al. Epstein Barr virus specific cytotoxic T lymphocytes expressing the anti-CD30zeta artificial chimeric T-cell receptor for immunotherapy of Hodgkin disease. Blood. 2007;110(7):2620–2630.• Successful eradication of Hodgkin’s lymphoma cells by EBV-specific anti-CD30 CAR T cells in a mouse model.
28. Taussig DC, Pearce DJ, Simpson C, et al. Hematopoietic stem cells express multiple myeloid markers:implications for the origin and targeted therapy of acute myeloid leukemia. Blood. 2005;106(13):4086–4092.
29. Mardiros A, Dos Santos C, McDonald T, et al. T cells expressing CD123-specific chimeric antigen receptors exhibit specific cytolytic effector functions and antitumor effects against human acute myeloid leukemia. Blood. 2013;122(18):3138–3148.
30. Tettamanti S, Marin V, Pizzitola I, et al. Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br J Haematol. 2013;161(3):389–401.
31. Pizzitola I, Anjos-Afonso F, Rouault-Pierre K, et al. Chimeric antigen receptors against CD33/CD123 antigens efficiently target primary acute myeloid leukemia cells in vivo. Leukemia. 2014;28(8):1596–1605.
32. Gill S, Tasian SK, Ruella M, et al. Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood. 2014;123(15):2343–2354.
33. Liu X, Jiang S, Fang C, et al. Affinity-tuned ErbB2 or EGFR chimeric antigen receptor T cells exhibit an increased therapeutic index against tumors in mice. Cancer Res. 2015;75(17):3596–3607.
34. Zhao Y, Wang QJ, Yang S, et al. A herceptin-based chimeric antigen receptor with modified signaling domains leads to enhanced survival of transduced T lymphocytes and antitumor activity. J Immunol. 2009;183(9):5563–5574.
35. Chmielewski M, Hombach A, Heuser C, et al. T cell activation by antibody-like immunoreceptors:increase in affinity of the single-chain fragment domain above threshold does not increase T cell activation against antigen-positive target cells but decreases selectivity. J Immunol. 2004;173(12):7647–7653.
36. Chen H-F, Yu C-Y, Chen M-J, et al. Characteristic expression of major histocompatibility complex and immune privilege genes in human pluripotent stem cells and their derivatives. Cell Transplant. 2015;24(5):845–864.
37. Zheng J, Umikawa M, Zhang S, et al. Ex vivo expanded hematopoietic stem cells overcome the MHC barrier in allogeneic transplantation. Cell Stem Cell. 2011;9(2):119–130.
38. El Haddad N, Moore R, Heathcote D, et al. The novel role of SERPINB9 in cytotoxic protection of human mesenchymal stem cells. J Immunol. 2011;187(5):2252–2260.
39. El Haddad N, Heathcote D, Moore R, et al. Mesenchymal stem cells express serine protease inhibitor to evade the host immune response. Blood. 2011;117(4):1176–1183.• Identification of SP6/IP9 as a key factor mediating protection against a cytolytic T-cell attack.
40. Utermöhlen O, Krönke M. Survival of priceless cells:active and passive protection of embryonic stem cells against immune destruction. Arch Biochem Biophys. 2007;462(2):273–277.
41. Abdullah Z, Saric T, Kashkar H, et al. Serpin-6 expression protects embryonic stem cells from lysis by antigen-specific CTL. J Immunol. 2007;178(6):3390–3399.
42. Sun J, Bird CH, Sutton V, et al. A cytosolic granzyme B inhibitor related to the viral apoptotic regulator cytokine response modifier A is present in cytotoxic lymphocytes. J Biol Chem. 1996;271(44):27802–27809.
43. Watanabe K, Terakura S, Martens AC, et al. Target antigen density governs the efficacy of anti-CD20-CD28-CD3 ζ chimeric antigen receptor-modified effector CD8+ T cells. J Immunol. 2015;194(3):911–920.• Demonstrates antigen density-dependent CAR T-cell activation.
44. Valitutti S, Müller S, Cella M, et al. Serial triggering of many T-cell receptors by a few peptide-MHC complexes. Nature. 1995;375(6527):148–151.
45. Huang J, Brameshuber M, Zeng X, et al. A single peptide-major histocompatibility complex ligand triggers digital cytokine secretion in CD4(+) T cells. Immunity. 2013;39(5):846–857.
46. Sykulev Y, Joo M, Vturina I, et al. Evidence that a single peptide-MHC complex on a target cell can elicit a cytolytic T cell response. Immunity. 1996;4(6):565–571.
47. Hudecek M, Lupo-Stanghellini M-T, Kosasih PL, et al. Receptor affinity and extracellular domain modifications affect tumor recognition by ROR1-specific chimeric antigen receptor T cells. Clin Cancer Res. 2013;19(12):3153–3164.
48. James SE, Greenberg PD, Jensen MC, et al. Antigen sensitivity of CD22-specific chimeric TCR is modulated by target epitope distance from the cell membrane. J Immunol. 2008;180(10):7028–7038.
49. Hombach A, Heuser C, Gerken M, et al. 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. 2000;7(12):1067–1075.
50. Caruso HG, Hurton LV, Najjar A, et al. Tuning sensitivity of CAR to EGFR density limits recognition of normal tissue while maintaining potent antitumor activity. Cancer Res. 2015;75(17):3505–3518.