Anti-human CD117 CAR T-cells efficiently eliminate healthy and malignant CD117-expressing hematopoietic cells (original) (raw)

References

  1. Tyner JW, Tognon CE, Bottomly D, Wilmot B, Kurtz SE, Savage SL, et al. Functional genomic landscape of acute myeloid leukaemia. Nature. 2018;562:526–31.
    CAS PubMed PubMed Central Google Scholar
  2. Dohner H, Weisdorf DJ, Bloomfield CD. Acute myeloid leukemia. N Engl J Med. 2015;373:1136–52.
    PubMed Google Scholar
  3. Short NJ, Rytting ME, Cortes JE. Acute myeloid leukaemia. Lancet. 2018;392:593–606.
    PubMed Google Scholar
  4. June CH, O’Connor RS, Kawalekar OU, Ghassemi S, Milone MC. CAR T cell immunotherapy for human cancer. Science. 2018;359:1361–5.
    CAS PubMed Google Scholar
  5. June CH, Sadelain M. Chimeric antigen receptor therapy. N Engl J Med. 2018;379:64–73.
    CAS PubMed PubMed Central Google Scholar
  6. van der Stegen SJ, Hamieh M, Sadelain M. The pharmacology of second-generation chimeric antigen receptors. Nat Rev Drug Discov. 2015;14:499–509.
    PubMed PubMed Central Google Scholar
  7. Park JH, Riviere I, Gonen M, Wang X, Senechal B, Curran KJ, et al. Long-term follow-up of CD19 CAR therapy in acute lymphoblastic leukemia. N Engl J Med. 2018;378:449–59.
    CAS PubMed PubMed Central Google Scholar
  8. Neelapu SS, Locke FL, Bartlett NL, Lekakis LJ, Miklos DB, Jacobson CA, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377:2531–44.
    CAS PubMed PubMed Central Google Scholar
  9. Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H, et al. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med. 2018;378:439–48.
    CAS PubMed PubMed Central Google Scholar
  10. Raje N, Berdeja J, Lin Y, Siegel D, Jagannath S, Madduri D, et al. Anti-BCMA CAR T-cell therapy bb2121 in relapsed or refractory multiple myeloma. N Engl J Med. 2019;380:1726–37.
    CAS PubMed PubMed Central Google Scholar
  11. Kochenderfer JN, Dudley ME, Feldman SA, Wilson WH, Spaner DE, Maric I, et al. B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. Blood. 2012;119:2709–20.
    CAS PubMed PubMed Central Google Scholar
  12. Brudno JN, Kochenderfer JN. Recent advances in CAR T-cell toxicity: Mechanisms, manifestations and management. Blood Rev. 2019;34:45–55.
    CAS PubMed Google Scholar
  13. Finney OC, Brakke HM, Rawlings-Rhea S, Hicks R, Doolittle D, Lopez M, et al. CD19 CAR T cell product and disease attributes predict leukemia remission durability. J Clin Invest. 2019; 129:2123–32.
    PubMed PubMed Central Google Scholar
  14. Haubner S, Perna F, Kohnke T, Schmidt C, Berman S, Augsberger C, et al. Coexpression profile of leukemic stem cell markers for combinatorial targeted therapy in AML. Leukemia. 2019; 33:64–74.
    CAS PubMed Google Scholar
  15. Perna F, Berman SH, Soni RK, Mansilla-Soto J, Eyquem J, Hamieh M, et al. Integrating proteomics and transcriptomics for systematic combinatorial chimeric antigen receptor therapy of AML. Cancer Cell. 2017;32:506–19.e505.
    CAS PubMed PubMed Central Google Scholar
  16. Lennartsson J, Ronnstrand L. Stem cell factor receptor/c-Kit: from basic science to clinical implications. Physiol Rev. 2012;92:1619–49.
    CAS PubMed Google Scholar
  17. Tsao AS, Kantarjian H, Thomas D, Giles F, Cortes J, Garcia-Manero G, et al. C-Kit receptor expression in acute leukemias-association with patient and disease characteristics and with outcome. Leuk Res. 2004;28:373–8.
    CAS PubMed Google Scholar
  18. Valverde LR, Matutes E, Farahat N, Heffernan A, Owusu-Ankomah K, Morilla R, et al. C-Kit receptor (CD117) expression in acute leukemia. Ann Hematol. 1996;72:11–15.
    CAS PubMed Google Scholar
  19. Wells SJ, Bray RA, Stempora LL, Farhi DC. CD117/CD34 expression in leukemic blasts. Am J Clin Pathol. 1996;106:192–5.
    CAS PubMed Google Scholar
  20. Cascavilla N, Musto P, D’Arena G, Melillo L, Carella AM, Petrilli MP, et al. CD117 (c-Kit) is a restricted antigen of acute myeloid leukemia and characterizes early differentiative levels of M5 FAB subtype. Haematologica. 1998;83:392–7.
    CAS PubMed Google Scholar
  21. Lauria F, Bagnara GP, Rondelli D, Raspadori D, Strippoli P, Bonsi L, et al. Cytofluorimetric and functional analysis of c-Kit receptor in acute leukemia. Leuk Lymphoma. 1995;18:451–5.
    CAS PubMed Google Scholar
  22. Bene MC, Bernier M, Casasnovas RO, Castoldi G, Knapp W, Lanza F, et al. The reliability and specificity of c-Kit for the diagnosis of acute myeloid leukemias and undifferentiated leukemias. The European Group for the Immunological Classification of Leukemias (EGIL). Blood. 1998;92:596–9.
    CAS PubMed Google Scholar
  23. Hans CP, Finn WG, Singleton TP, Schnitzer B, Ross CW. Usefulness of anti-CD117 in the flow cytometric analysis of acute leukemia. Am J Clin Pathol. 2002;117:301–5.
    CAS PubMed Google Scholar
  24. Schwartz S, Heinecke A, Zimmermann M, Creutzig U, Schoch C, Harbott J, et al. Expression of the c-Kit receptor (CD117) is a feature of almost all subtypes of de novo acute myeloblastic leukemia (AML), including cytogenetically good-risk AML, and lacks prognostic significance. Leuk Lymphoma. 1999;34:85–94.
    CAS PubMed Google Scholar
  25. Sperling C, Schwartz S, Buchner T, Thiel E, Ludwig WD. Expression of the stem cell factor receptor c-Kit (CD117) in acute leukemias. Haematologica. 1997;82:617–21.
    CAS PubMed Google Scholar
  26. Di Noto R, Lo Pardo C, Schiavone EM, Manzo C, Vacca C, Ferrara F, et al. Stem cell factor receptor (c-Kit, CD117) is expressed on blast cells from most immature types of acute myeloid mallignancies but is also a characteristic of a subset of acute promyelocytic leukaemia. Br J Haematol. 1996;92:562–4.
    PubMed Google Scholar
  27. Czechowicz A, Kraft D, Weissman IL, Bhattacharya D. Efficient transplantation via antibody-based clearance of hematopoietic stem cell niches. Science. 2007;318:1296–9.
    CAS PubMed PubMed Central Google Scholar
  28. Chhabra A, Ring AM, Weiskopf K, Schnorr PJ, Gordon S, Le AC, et al. Hematopoietic stem cell transplantation in immunocompetent hosts without radiation or chemotherapy. Sci Transl Med. 2016;8:351ra105.
    PubMed PubMed Central Google Scholar
  29. Czechowicz A, Palchaudhuri R, Scheck A, Hu Y, Hoggatt J, Saez B, et al. Selective hematopoietic stem cell ablation using CD117-antibody-drug-conjugates enables safe and effective transplantation with immunity preservation. Nat Commun. 2019;10:617.
    CAS PubMed PubMed Central Google Scholar
  30. Xue X, Pech NK, Shelley WC, Srour EF, Yoder MC, Dinauer MC. Antibody targeting KIT as pretransplantation conditioning in immunocompetent mice. Blood. 2010;116:5419–22.
    CAS PubMed PubMed Central Google Scholar
  31. Kwon HS, Logan AC, Chhabra A, Pang WW, Czechowicz A, Tate K, et al. Anti-human CD117 antibody-mediated bone marrow niche clearance in nonhuman primates and humanized NSG mice. Blood. 2019;133:2104–8.
    CAS PubMed PubMed Central Google Scholar
  32. Pearse BR, McDonough SM, Proctor JL, Panwar R, Sarma G, McShea MA, et al. CD117-amanitin antibody drug conjugates effectively deplete human and non-human primate HSCs: proof of concept as a targeted strategy for conditioning patients for bone marrow transplant. Blood. 2018;132:3314.
    Google Scholar
  33. Pang WW, Czechowicz A, Logan AC, Bhardwaj R, Poyser J, Park CY, et al. Anti-CD117 antibody depletes normal and myelodysplastic syndrome human hematopoietic stem cells in xenografted mice. Blood. 2019;133:2069–78.
    CAS PubMed PubMed Central Google Scholar
  34. Arai Y, Choi U, Corsino CI, Koontz SM, Tajima M, Sweeney CL, et al. Myeloid conditioning with c-Kit-targeted CAR-T cells enables donor stem cell engraftment. Mol Ther. 2018;26:1181–97.
    CAS PubMed PubMed Central Google Scholar
  35. Reshetnyak AV, Nelson B, Shi X, Boggon TJ, Pavlenco A, Mandel-Bausch EM, et al. Structural basis for KIT receptor tyrosine kinase inhibition by antibodies targeting the D4 membrane-proximal region. Proc Natl Acad Sci USA. 2013;110:17832–7.
    CAS PubMed PubMed Central Google Scholar
  36. Philip B, Kokalaki E, Mekkaoui L, Thomas S, Straathof K, Flutter B, et al. A highly compact epitope-based marker/suicide gene for easier and safer T-cell therapy. Blood. 2014;124:1277–87.
    CAS PubMed Google Scholar
  37. Ellegast JM, Rauch PJ, Kovtonyuk LV, Muller R, Wagner U, Saito Y, et al. inv(16) and NPM1mut AMLs engraft human cytokine knock-in mice. Blood. 2016;128:2130–4.
    CAS PubMed PubMed Central Google Scholar
  38. Theocharides AP, Rongvaux A, Fritsch K, Flavell RA, Manz MG. Humanized hemato-lymphoid system mice. Haematologica. 2016;101:5–19.
    CAS PubMed PubMed Central Google Scholar
  39. Nischang M, Sutmuller R, Gers-Huber G, Audigé A, Li D, Rochat M-A, et al. Humanized mice recapitulate key features of HIV-1 infection: a novel concept using long-acting anti-retroviral drugs for treating HIV-1. PLoS One. 2012;7:e38853.
    CAS PubMed PubMed Central Google Scholar
  40. Song Y, Rongvaux A, Taylor A, Jiang T, Tebaldi T, Balasubramanian K, et al. A highly efficient and faithful MDS patient-derived xenotransplantation model for pre-clinical studies. Nat Commun. 2019;10:366.
    CAS PubMed PubMed Central Google Scholar
  41. Rongvaux A, Willinger T, Martinek J, Strowig T, Gearty SV, Teichmann LL, et al. Development and function of human innate immune cells in a humanized mouse model. Nat Biotechnol. 2014;32:364–72.
    CAS PubMed PubMed Central Google Scholar
  42. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, et al. Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol. 2005;174:6477–89.
    CAS PubMed Google Scholar
  43. Tsuura Y, Hiraki H, Watanabe K, Igarashi S, Shimamura K, Fukuda T, et al. Preferential localization of c-kit product in tissue mast cells, basal cells of skin, epithelial cells of breast, small cell lung carcinoma and seminoma/dysgerminoma in human: immunohistochemical study on formalin-fixed, paraffin-embedded tissues. Virchows Arch. 1994;424:135–41.
    CAS PubMed Google Scholar
  44. Miettinen M, Lasota J. KIT (CD117): a review on expression in normal and neoplastic tissues, and mutations and their clinicopathologic correlation. Appl Immunohistochem Mol Morphol. 2005;13:205–20.
    CAS PubMed Google Scholar
  45. Strobl H, Takimoto M, Majdic O, Hocker P, Knapp W. Antigenic analysis of human haemopoietic progenitor cells expressing the growth factor receptor c-Kit. Br J Haematol. 1992;82:287–94.
    CAS PubMed Google Scholar
  46. Lerner NB, Nocka KH, Cole SR, Qiu FH, Strife A, Ashman LK, et al. Monoclonal antibody YB5.B8 identifies the human c-Kit protein product. Blood. 1991;77:1876–83.
    CAS PubMed Google Scholar
  47. Nombela-Arrieta C, Manz MG. Quantification and three-dimensional microanatomical organization of the bone marrow. Blood Adv. 2017;1:407–16.
    CAS PubMed PubMed Central Google Scholar
  48. Manz MG, Russkamp NF. Selective CD117(+) HSC exchange therapy. Blood. 2019;133:2007–9.
    CAS PubMed Google Scholar
  49. Agarwal R, Dvorak CC, Prohaska S, Long-Boyle J, Kwon H-S, Brown JM, et al. Toxicity-Free Hematopoietic Stem Cell Engraftment Achieved with Anti-CD117 Monoclonal Antibody Conditioning. Biol Blood Marrow Transplant. 2019;25(Suppl 3):S92.
    Google Scholar
  50. Beyar-Katz O, Gill S. Novel Approaches to Acute Myeloid Leukemia Immunotherapy. Clin Cancer Res. 2018;24:5502–15.
    CAS PubMed Google Scholar
  51. Kim MY, Yu KR, Kenderian SS, Ruella M, Chen S, Shin TH, et al. Genetic inactivation of CD33 in hematopoietic stem cells to enable CAR T cell immunotherapy for acute myeloid leukemia. Cell. 2018;173:1439–53.e1419.
    CAS PubMed PubMed Central Google Scholar
  52. Straathof KC, Pule MA, Yotnda P, Dotti G, Vanin EF, Brenner MK, et al. An inducible caspase 9 safety switch for T-cell therapy. Blood. 2005;105:4247–54.
    CAS PubMed PubMed Central Google Scholar
  53. Holzinger A, Abken H. CAR T-cells: a snapshot on the growing options to design a CAR. HemaSphere. 2019;3:e172.
    PubMed PubMed Central Google Scholar
  54. Roybal KT, Rupp LJ, Morsut L, Walker WJ, McNally KA, Park JS, et al. Precision tumor recognition by T cells with combinatorial antigen-sensing circuits. Cell. 2016;164:770–9.
    CAS PubMed PubMed Central Google Scholar

Download references