655
Views
3
CrossRef citations to date
0
Altmetric
Review

Treating hematological malignancies with cell therapy: where are we now?

&
Pages 65-75 | Received 27 Jun 2017, Accepted 22 Sep 2017, Published online: 05 Oct 2017

References

  • Horowitz MM, Gale RP, Sondel PM, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990 Feb 1;75(3):555–562.
  • Collins RH Jr, Shpilberg O, Drobyski WR, et al. Donor leukocyte infusions in 140 patients with relapsed malignancy after allogeneic bone marrow transplantation. J Clin Oncol. 1997 Feb;15(2):433–444.
  • Kolb HJ. Hematopoietic stem cell transplantation and cellular therapy. HLA. 2017 May;89(5):267–277.
  • Greco R, Oliveira G, Stanghellini MT, et al. Improving the safety of cell therapy with the TK-suicide gene. Front Pharmacol. 2015;6:95.
  • Diaconu I, Ballard B, Zhang M, et al. Inducible caspase-9 selectively modulates the toxicities of CD19-specific chimeric antigen receptor-modified T cells. Mol Ther. 2017 Mar 01;25(3):580–592.
  • Doubrovina E, Oflaz-Sozmen B, Prockop SE, et al. Adoptive immunotherapy with unselected or EBV-specific T cells for biopsy-proven EBV+ lymphomas after allogeneic hematopoietic cell transplantation. Blood. 2012 Mar 15;119(11):2644–2656.
  • Tashiro H, Brenner MK. Immunotherapy against cancer-related viruses. Cell Res. 2017 Jan;27(1):59–73.
  • Eshhar Z, Waks T, Gross G, et al. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci USA. 1993 Jan 15;90(2):720–724.
  • Maus MV, Haas AR, Beatty GL, et al. T cells expressing chimeric antigen receptors can cause anaphylaxis in humans. Cancer Immunol Res. 2013;1:26–31.
  • Turtle CJ, Hanafi LA, Berger C, et al. CD19 CAR-T cells of defined CD4+: CD8+composition in adult B cell ALL patients. J Clin Invest. 2016 Jun 1;126(6):2123–2138.
  • Hudecek M, Lupo-Stanghellini MT, 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 Jun 15;19(12):3153–3164.
  • Drent E, Themeli M, Poels R, et al. A rational strategy for reducing on-target off-tumor effects of CD38-chimeric antigen receptors by affinity optimization. Mol Ther. 2017 May 13;25(8):1946–1958.
  • Guest RD, Hawkins RE, Kirillova N, et al. The role of extracellular spacer regions in the optimal design of chimeric immune receptors: evaluation of four different scFvs and antigens. J Immunother. 2005 May-Jun;28(3):203–211.
  • Geldres C, Savoldo B, Dotti G. Chimeric antigen receptor-redirected T cells return to the bench. Semin Immunol. 2016 Feb;28(1):3–9.
  • Hudecek M, Sommermeyer D, Kosasih PL, et al. The nonsignaling extracellular spacer domain of chimeric antigen receptors is decisive for in vivo antitumor activity. Cancer Immunol Res. 2015 Feb;3(2):125–135.
  • Dotti G, Gottschalk S, Savoldo B, et al. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev. 2014 Jan;257(1):107–126.
  • Till BG, Jensen MC, Wang J, et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood. 2008 Sep 15;112(6):2261–2271.
  • Pule MA, Savoldo B, Myers GD, et al. Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma. Nat Med. 2008 Nov;14(11):1264–1270.
  • Brentjens RJ, Latouche JB, Santos E, et al. Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15. Nat Med. 2003 Mar;9(3):279–286.
  • Gajewski TF, Meng Y, Blank C, et al. Immune resistance orchestrated by the tumor microenvironment. Immunol Rev. 2006;213:131–145.
  • Milone MC, Fish JD, Carpenito C, et al. Chimeric receptors containing CD137 signal transduction domains mediate enhanced survival of T cells and increased antileukemic efficacy in vivo. Mol Ther. 2009 Aug;17(8):1453–1464.
  • Savoldo B, Ramos CA, Liu E, et al. CD28 costimulation improves expansion and persistence of chimeric antigen receptor-modified T cells in lymphoma patients. J Clin Invest. 2011 May;121(5):1822–1826.
  • Pule MA, Straathof KC, Dotti G, et al. A chimeric T cell antigen receptor that augments cytokine release and supports clonal expansion of primary human T cells. Mol Ther. 2005 Nov;12(5):933–941.
  • Zhong XS, Matsushita M, Plotkin J, et al. Chimeric antigen receptors combining 4-1BB and CD28 signaling domains augment PI3kinase/AKT/Bcl-XL activation and CD8+ T cell-mediated tumor eradication. Mol Ther. 2010 Feb;18(2):413–420.
  • Park JH, Geyer MB, Brentjens RJ. CD19-targeted CAR T-cell therapeutics for hematologic malignancies: interpreting clinical outcomes to date. Blood. 2016 Jun 30;127(26):3312–3320.
  • Fesnak AD, June CH, Levine BL. Engineered T cells: the promise and challenges of cancer immunotherapy. Nat Rev Cancer. 2016 Aug 23;16(9):566–581.
  • Scheuermann RH, Racila E. CD19 antigen in leukemia and lymphoma diagnosis and immunotherapy. Leuk Lymphoma. 1995 Aug;18(5–6):385–397.
  • Fujiwara H. Adoptive immunotherapy for hematological malignancies using T cells gene-modified to express tumor antigen-specific receptors. Pharmaceuticals (Basel). 2014 Dec 15;7(12):1049–1068.
  • Till BG, Jensen MC, Wang J, et al. CD20-specific adoptive immunotherapy for lymphoma using a chimeric antigen receptor with both CD28 and 4-1BB domains: pilot clinical trial results. Blood. 2012 Apr 26;119(17):3940–3950.
  • Vera J, Savoldo B, Vigouroux S, et al. T lymphocytes redirected against the kappa light chain of human immunoglobulin efficiently kill mature B lymphocyte-derived malignant cells. Blood. 2006 Dec 01;108(12):3890–3897.
  • Ramos CA, Savoldo B, Torrano V, et al. Clinical responses with T lymphocytes targeting malignancy-associated kappa light chains. J Clin Invest. 2016 Jul 01;126(7):2588–2596.
  • Zhang S, Chen L, Wang-Rodriguez J, et al. The onco-embryonic antigen ROR1 is expressed by a variety of human cancers. Am J Pathol. 2012 Dec;181(6):1903–1910.
  • Bicocca VT, Chang BH, Masouleh BK, et al. Crosstalk between ROR1 and the Pre-B cell receptor promotes survival of t(1;19) acute lymphoblastic leukemia. Cancer Cell. 2012 Nov 13;22(5):656–667.
  • Aghebati-Maleki L, Shabani M, Baradaran B, et al. Receptor tyrosine kinase-like orphan receptor 1 (ROR-1): an emerging target for diagnosis and therapy of chronic lymphocytic leukemia. Biomed Pharmacother. 2017;88:814–822.
  • Deniger DC, Yu J, Huls MH, et al. Sleeping beauty transposition of chimeric antigen receptors targeting receptor tyrosine kinase-like orphan receptor-1 (ROR1) into diverse memory T-cell populations. PLoS One. 2015;10(6):e0128151.
  • Berger C, Sommermeyer D, Hudecek M, et al. Safety of targeting ROR1 in primates with chimeric antigen receptor-modified T cells. Cancer Immunol Res. 2015 Feb;3(2):206–216.
  • Gohil S, Della Peruta M, Paredes-Moscosso S, et al. Novel humanised ROR1 chimeric antigen receptors for the treatment of haematological malignancies [abstract]. Blood. 2016;128(22):3361.
  • Wang CM, Wu ZQ, Wang Y, et al. Autologous T cells expressing CD30 chimeric antigen receptors for relapsed or refractory Hodgkin lymphoma: an open-label phase I trial. Clin Cancer Res. 2017 Mar 1;23(5):1156–1166.
  • Ramos CA, Ballard B, Zhang H, et al. Clinical and immunological responses after CD30-specific chimeric antigen receptor-redirected lymphocytes. J Clin Invest. 2017 Aug 14.
  • Garfall AL, Maus MV, Hwang WT, et al. Chimeric antigen receptor T cells against CD19 for multiple myeloma. N Engl J Med. 2015 Sep 10;373(11):1040–1047.
  • Carpenter RO, Evbuomwan MO, Pittaluga S, et al. B-cell maturation antigen is a promising target for adoptive T-cell therapy of multiple myeloma. Clin Cancer Res. 2013 Apr 15;19(8):2048–2060.
  • Ali SA, Shi V, Maric I, et al. T cells expressing an anti-B-cell maturation antigen chimeric antigen receptor cause remissions of multiple myeloma. Blood. 2016 Sep 29;128(13):1688–1700.
  • Garrett T, Chekmasova A, Evans J, et al. A BCMA-specific CAR T cell produced with clinically scalable lentiviral and T cell manufacturing processes has potent anti-multiple myeloma activity. J ImmunoTherapy Cancer. 2015;3(Suppl 2): P124.
  • Guo B, Chen M, Han Q, et al. CD138-directed adoptive immunotherapy of chimeric antigen receptor (CAR)-modified T cells for multiple myeloma. Journal of Cellular Immunotherapy. 2016;2(1):28–35.
  • Volk R, Schwartz JJ, Li J, et al. The role of syndecan cytoplasmic domain in basic fibroblast growth factor-dependent signal transduction. J Biol Chem. 1999 Aug 20;274(34):24417–24424.
  • Tian C, Yang H, Zhu L, et al. Anti-CD138 chimeric antigen receptor-modified T cell therapy for multiple myeloma with extensive extramedullary involvement. Ann Hematol. 2017 Jun 2.
  • Wang QS, Wang Y, Lv HY, et al. Treatment of CD33-directed chimeric antigen receptor-modified T cells in one patient with relapsed and refractory acute myeloid leukemia. Mol Ther. 2015 Jan;23(1):184–191.
  • Luo Y, Chang L, Hu Y, et al. First-in-man CD123-specific chimeric antigen receptor-modified T cells for the treatment of refractory acute myeloid leukemia [abstract]. Blood. 2015;126(23):3778.
  • Tasian S, Kenderian S, Li Y, et al. Efficient termination of CD123-redirected chimeric antigen receptor T cells for acute myeloid leukemia to mitigate toxicity [abstract]. Blood. 2015;126(23):565.
  • Lynn RC, Feng Y, Schutsky K, et al. High-affinity FRbeta-specific CAR T cells eradicate AML and normal myeloid lineage without HSC toxicity. Leukemia. 2016 Jun;30(6):1355–1364.
  • Casucci M, Nicolis di Robilant B, Falcone L, et al. CD44v6-targeted T cells mediate potent antitumor effects against acute myeloid leukemia and multiple myeloma. Blood. 2013 Nov 14;122(20):3461–3472.
  • Zhang S, Zhang HS, Cordon-Cardo C, et al. Selection of tumor antigens as targets for immune attack using immunohistochemistry: II. Blood group-related antigensInt J Cancer. 1997 Sep 26;73(1):50–56.
  • Ritchie DS, Neeson PJ, Khot A, et al. Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol Ther. 2013 Nov;21(11):2122–2129.
  • Marino J, Paster J, Benichou G. Allorecognition by T lymphocytes and allograft rejection. Front Immunol. 2016;7:582.
  • Qasim W, Zhan H, Samarasinghe S, et al. Molecular remission of infant B-ALL after infusion of universal TALEN gene-edited CAR T cells. Sci Transl Med. 2017 Jan 25;9(374).
  • MacLeod DT, Antony J, Martin AJ, et al. Integration of a CD19 CAR into the TCR alpha chain locus streamlines production of allogeneic gene-edited CAR T cells. Mol Ther. 2017 Apr 05;25(4):949–961.
  • Yang W, Agrawal N, Patel J, et al. Diminished expression of CD19 in B-cell lymphomas. Cytometry B Clin Cytom. 2005 Jan;63(1):28–35.
  • Sotillo E, Barrett DM, Black KL, et al. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov. 2015 Dec;5(12):1282–1295.
  • Grupp SA, Maude SL, Shaw PA, et al. Durable remissions in children with relapsed/refractory all treated with T cells engineered with a CD19-targeted chimeric antigen receptor (CTL019) [abstract]. Blood. 2015;126(23): Abstract 681;126:681.
  • Lee III D, Stetler-Stevenson M, Yuan C, et al. Safety and response of incorporating CD19 chimeric antigen receptor T cell therapy in typical salvage regimens for children and young adults with acute lymphoblastic leukemia [abstract]. Blood. 2015;126(23):684.
  • Maude S, Barrett D, Ambrose D, et al. Efficacy and safety of humanized Chimeric Antigen Receptor (CAR)-modified T cells targeting CD19 in children with relapsed/refractory ALL [abstract]. Blood. 2015;126(23):683.
  • Hegde M, Corder A, Chow KK, et al. Combinational targeting offsets antigen escape and enhances effector functions of adoptively transferred T cells in glioblastoma. Mol Ther. 2013 Nov;21(11):2087–2101.
  • Anurathapan U, Chan RC, Hindi HF, et al. Kinetics of tumor destruction by chimeric antigen receptor-modified T cells. Mol Ther. 2014 Mar;22(3):623–633.
  • Zah E, Lin MY, Silva-Benedict A, et al. T cells expressing CD19/CD20 bispecific chimeric antigen receptors prevent antigen escape by malignant B cells. Cancer Immunol Res. 2016 Jun;4(6):498–508.
  • Grada Z, Hegde M, Byrd T, et al. TanCAR: a novel bispecific chimeric antigen receptor for cancer immunotherapy. Mol Ther Nucleic Acids. 2013 Jul;09(2):e105.
  • Zhao Q, Ahmed M, Tassev DV, et al. Affinity maturation of T-cell receptor-like antibodies for Wilms tumor 1 peptide greatly enhances therapeutic potential. Leukemia. 2015 Nov;29(11):2238–2247.
  • Ma Q, Garber HR, Lu S, et al. A novel TCR-like CAR with specificity for PR1/HLA-A2 effectively targets myeloid leukemia in vitro when expressed in human adult peripheral blood and cord blood T cells. Cytotherapy. 2016 Aug;18(8):985–994.
  • Morris EC, Stauss HJ. Optimizing T-cell receptor gene therapy for hematologic malignancies. Blood. 2016 Jun 30;127(26):3305–3311.
  • Dembic Z, Haas W, Weiss S, et al. Transfer of specificity by murine alpha and beta T-cell receptor genes. Nature. 1986 Mar 20-26;320(6059):232–238.
  • Perry JS, Hsieh CS. Development of T-cell tolerance utilizes both cell-autonomous and cooperative presentation of self-antigen. Immunol Rev. 2016 May;271(1):141–155.
  • Linette GP, Stadtmauer EA, Maus MV, et al. Cardiovascular toxicity and titin cross-reactivity of affinity-enhanced T cells in myeloma and melanoma. Blood. 2013 Aug 8;122(6):863–871.
  • Hossain NM, Chapuis AG, Walter RB. T-cell receptor-engineered cells for the treatment of hematologic malignancies. Curr Hematol Malig Rep. 2016 Aug;11(4):311–317.
  • Szymczak AL, Workman CJ, Wang Y, et al. Correction of multi-gene deficiency in vivo using a single ‘self-cleaving’ 2A peptide-based retroviral vector. Nat Biotechnol. 2004 May;22(5):589–594.
  • Cohen CJ, Zhao Y, Zheng Z, et al. Enhanced antitumor activity of murine-human hybrid T-cell receptor (TCR) in human lymphocytes is associated with improved pairing and TCR/CD3 stability. Cancer Res. 2006 Sep 01;66(17):8878–8886.
  • Cohen CJ, Li YF, El-Gamil M, et al. Enhanced antitumor activity of T cells engineered to express T-cell receptors with a second disulfide bond. Cancer Res. 2007 Apr 15;67(8):3898–3903.
  • Ahmadi M, King JW, Xue SA, et al. CD3 limits the efficacy of TCR gene therapy in vivo. Blood. 2011 Sep 29;118(13):3528–3537.
  • Knipping F, Osborn MJ, Petri K, et al. Genome-wide specificity of highly efficient TALENs and CRISPR/Cas9 for T cell receptor modification. Mol Ther Methods Clin Dev. 2017 Mar 17;4:213–224.
  • Mastaglio S, Genovese P, Magnani Z, et al. NY-ESO-1 TCR single edited central memory and memory stem T cells to treat multiple myeloma without inducing GvHD. Blood. 2017 Jun 21.
  • Robbins PF, Morgan RA, Feldman SA, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol. 2011 Mar 1;29(7):917–924.
  • Robbins PF, Kassim SH, Tran TL, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res. 2015 Mar 1;21(5):1019–1027.
  • Rapoport AP, Stadtmauer EA, Binder-Scholl GK, et al. NY-ESO-1-specific TCR-engineered T cells mediate sustained antigen-specific antitumor effects in myeloma. Nature Medicine. 2015 Aug;21(8):914–921.
  • Inoue K, Ogawa H, Sonoda Y, et al. Aberrant overexpression of the Wilms tumor gene (WT1) in human leukemia. Blood. 1997 Feb 15;89(4):1405–1412.
  • Bar M, Chapuis A, Schmitt T, et al. Transferred donor-derived virus specific CD8+ T cells that have been transduced to express a WT1-Specific T cell receptor can persist and provide anti-leukemic activity in AML patients post- transplant [abstract]. Blood. 2014;124(21):3939.
  • Cheever MA, Allison JP, Ferris AS, et al. The prioritization of cancer antigens: a national cancer institute pilot project for the acceleration of translational research. Clin Cancer Res. 2009 Sep 01;15(17):5323–5337.
  • Leisegang M, Wilde S, Spranger S, et al. MHC-restricted fratricide of human lymphocytes expressing survivin-specific transgenic T cell receptors. J Clin Invest. 2010 Nov;120(11):3869–3877.
  • Arber C, Feng X, Abhyankar H, et al. Survivin-specific T cell receptor targets tumor but not T cells. J Clin Invest. 2015 Jan;125(1):157–168.
  • Jahn L, Hagedoorn RS, van der Steen DM, et al. A CD22-reactive TCR from the T-cell allorepertoire for the treatment of acute lymphoblastic leukemia by TCR gene transfer. Oncotarget. 2016 Nov 01;7(44):71536–71547.
  • Jahn L, Hombrink P, Hagedoorn RS, et al. TCR-based therapy for multiple myeloma and other B-cell malignancies targeting intracellular transcription factor BOB1. Blood. 2017 Mar 09;129(10):1284–1295.
  • Yarchoan M, Johnson BA 3rd, Lutz ER, et al. Targeting neoantigens to augment antitumour immunity. Nat Rev Cancer. 2017 Apr;17(4):209–222.
  • Ward JP, Gubin MM, Schreiber RD. The role of neoantigens in naturally occurring and therapeutically induced immune responses to cancer. Adv Immunol. 2016;130:25–74.
  • Schumacher TN, Schreiber RD. Neoantigens in cancer immunotherapy. Science. 2015 Apr 3;348(6230):69–74.
  • Alexandrov LB, Nik-Zainal S, Wedge DC, et al. Signatures of mutational processes in human cancer. Nature. 2013 Aug 22;500(7463):415–421.
  • Sun C, Dotti G, Savoldo B. Utilizing cell-based therapeutics to overcome immune evasion in hematologic malignancies. Blood. 2016 Jun 30;127(26):3350–3359.
  • Armand P. Immune checkpoint blockade in hematologic malignancies. Blood. 2015 May 28;125(22):3393–3400.
  • Cherkassky L, Morello A, Villena-Vargas J, et al. Human CAR T cells with cell-intrinsic PD-1 checkpoint blockade resist tumor-mediated inhibition. J Clin Invest. 2016 Aug 01;126(8):3130–3144.
  • McGranahan N, Furness AJ, Rosenthal R, et al. Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 2016 Mar 25;351(6280):1463–1469.
  • Paszkiewicz PJ, Frassle SP, Srivastava S, et al. Targeted antibody-mediated depletion of murine CD19 CAR T cells permanently reverses B cell aplasia. J Clin Invest. 2016 Nov 01;126(11):4262–4272.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.