Chimeric antigen receptor T cell therapies for acute myeloid leukemia
Bin Gu, Jianhong Chu, Depei Wu
Chimeric antigen receptor T cell therapies for acute myeloid leukemia
Chimeric antigen receptor T cell (CAR T) therapies have achieved unprecedented efficacy in B-cell tumors, prompting scientists and doctors to exploit this strategy to treat other tumor types. Acute myeloid leukemia (AML) is a group of heterogeneous myeloid malignancies. Relapse remains the main cause of treatment failure, especially for patients with intermediate or high risk stratification. Allogeneic hematopoietic stem cell transplantation could be an effective therapy because of the graft-versus-leukemia effect, which unfortunately puts the patient at risk of serious complications, such as graft-versus-host disease. Although the identification of an ideal target antigen for AML is challenging, CAR T therapy remains a highly promising strategy for AML patients, particularly for those who are ineligible to receive a transplantation or have positive minimal residual disease. In this review, we focus on the most recent and promising advances in CAR T therapies for AML.
acute myeloid leukemia / CAR T / immunotherapy
[1] |
Döhner H, Weisdorf DJ, Bloomfield CD. Acute myeloid leukemia. N Engl J Med 2015; 373(12): 1136–1152
CrossRef
Pubmed
Google scholar
|
[2] |
Appelbaum FR, Gundacker H, Head DR, Slovak ML, Willman CL, Godwin JE, Anderson JE, Petersdorf SH. Age and acute myeloid leukemia. Blood 2006; 107(9): 3481–3485
CrossRef
Pubmed
Google scholar
|
[3] |
Mrózek K, Marcucci G, Nicolet D, Maharry KS, Becker H, Whitman SP, Metzeler KH, Schwind S, Wu YZ, Kohlschmidt J, Pettenati MJ, Heerema NA, Block AW, Patil SR, Baer MR, Kolitz JE, Moore JO, Carroll AJ, Stone RM, Larson RA, Bloomfield CD. Prognostic significance of the European LeukemiaNet standardized system for reporting cytogenetic and molecular alterations in adults with acute myeloid leukemia. J Clin Oncol 2012; 30(36): 4515–4523
CrossRef
Pubmed
Google scholar
|
[4] |
Röllig C, Bornhäuser M, Thiede C, Taube F, Kramer M, Mohr B, Aulitzky W, Bodenstein H, Tischler HJ, Stuhlmann R, Schuler U, Stölzel F, von Bonin M, Wandt H, Schäfer-Eckart K, Schaich M, Ehninger G. Long-term prognosis of acute myeloid leukemia according to the new genetic risk classification of the European LeukemiaNet recommendations: evaluation of the proposed reporting system. J Clin Oncol 2011; 29(20): 2758–2765
CrossRef
Pubmed
Google scholar
|
[5] |
Byrd JC, Mrózek K, Dodge RK, Carroll AJ, Edwards CG, Arthur DC, Pettenati MJ, Patil SR, Rao KW, Watson MS, Koduru PR, Moore JO, Stone RM, Mayer RJ, Feldman EJ, Davey FR, Schiffer CA, Larson RA, Bloomfield CD; Cancer and Leukemia Group B (CALGB 8461). Pretreatment cytogenetic abnormalities are predictive of induction success, cumulative incidence of relapse, and overall survival in adult patients with de novo acute myeloid leukemia: results from Cancer and Leukemia Group B (CALGB 8461). Blood 2002; 100(13): 4325–4336
CrossRef
Pubmed
Google scholar
|
[6] |
Cornelissen JJ, Gratwohl A, Schlenk RF, Sierra J, Bornhäuser M, Juliusson G, Råcil Z, Rowe JM, Russell N, Mohty M, Löwenberg B, Socié G, Niederwieser D, Ossenkoppele GJ. The European LeukemiaNet AML Working Party consensus statement on allogeneic HSCT for patients with AML in remission: an integrated-risk adapted approach. Nat Rev Clin Oncol 2012; 9(10): 579–590
CrossRef
Pubmed
Google scholar
|
[7] |
Maus MV, Grupp SA, Porter DL, June CH. Antibody-modified T cells: CARs take the front seat for hematologic malignancies. Blood 2014; 123(17): 2625–2635
CrossRef
Pubmed
Google scholar
|
[8] |
Wei J, Han X, Bo J, Han W. Target selection for CAR-T therapy. J Hematol Oncol 2019; 12(1): 62
CrossRef
Pubmed
Google scholar
|
[9] |
Drent E, Themeli M, Poels R, de Jong-Korlaar R, Yuan H, de Bruijn J, Martens ACM, Zweegman S, van de Donk N, Groen RWJ, Lokhorst HM, Mutis T. A rational strategy for reducing on-target off-tumor effects of CD38-chimeric antigen receptors by affinity optimization. Mol Ther 2017; 25(8): 1946–1958
CrossRef
Pubmed
Google scholar
|
[10] |
Walker AJ, Majzner RG, Zhang L, Wanhainen K, Long AH, Nguyen SM, Lopomo P, Vigny M, Fry TJ, Orentas RJ, Mackall CL. Tumor antigen and receptor densities regulate efficacy of a chimeric antigen receptor targeting anaplastic lymphoma kinase. Mol Ther 2017; 25(9): 2189–2201
CrossRef
Pubmed
Google scholar
|
[11] |
Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N Engl J Med 2011; 365(8): 725–733
CrossRef
Pubmed
Google scholar
|
[12] |
Grupp SA, Kalos M, Barrett D, Aplenc R, Porter DL, Rheingold SR, Teachey DT, Chew A, Hauck B, Wright JF, Milone MC, Levine BL, June CH. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N Engl J Med 2013; 368(16): 1509–1518
CrossRef
Pubmed
Google scholar
|
[13] |
Ceppi F, Gardner RA. Chimeric antigen receptor T cells for B-cell acute lymphoblastic leukemia. Cancer J 2019; 25(3): 191–198
CrossRef
Pubmed
Google scholar
|
[14] |
Papaemmanuil E, Gerstung M, Bullinger L, Gaidzik VI, Paschka P, Roberts ND, Potter NE, Heuser M, Thol F, Bolli N, Gundem G, Van Loo P, Martincorena I, Ganly P, Mudie L, McLaren S, O’Meara S, Raine K, Jones DR, Teague JW, Butler AP, Greaves MF, Ganser A, Döhner K, Schlenk RF, Döhner H, Campbell PJ. Genomic classification and prognosis in acute myeloid leukemia. N Engl J Med 2016; 374(23): 2209–2221
CrossRef
Pubmed
Google scholar
|
[15] |
Sotillo E, Barrett DM, Black KL, Bagashev A, Oldridge D, Wu G, Sussman R, Lanauze C, Ruella M, Gazzara MR, Martinez NM, Harrington CT, Chung EY, Perazzelli J, Hofmann TJ, Maude SL, Raman P, Barrera A, Gill S, Lacey SF, Melenhorst JJ, Allman D, Jacoby E, Fry T, Mackall C, Barash Y, Lynch KW, Maris JM, Grupp SA, Thomas-Tikhonenko A. Convergence of acquired mutations and alternative splicing of CD19 enables resistance to CART-19 immunotherapy. Cancer Discov 2015; 5(12): 1282–1295
CrossRef
Pubmed
Google scholar
|
[16] |
Gardner R, Wu D, Cherian S, Fang M, Hanafi LA, Finney O, Smithers H, Jensen MC, Riddell SR, Maloney DG, Turtle CJ. Acquisition of a CD19-negative myeloid phenotype allows immune escape of MLL-rearranged B-ALL from CD19 CAR-T-cell therapy. Blood 2016; 127(20): 2406–2410
CrossRef
Pubmed
Google scholar
|
[17] |
Jacoby E, Nguyen SM, Fountaine TJ, Welp K, Gryder B, Qin H, Yang Y, Chien CD, Seif AE, Lei H, Song YK, Khan J, Lee DW, Mackall CL, Gardner RA, Jensen MC, Shern JF, Fry TJ. CD19 CAR immune pressure induces B-precursor acute lymphoblastic leukaemia lineage switch exposing inherent leukaemic plasticity. Nat Commun 2016; 7(12320): 12320
CrossRef
Pubmed
Google scholar
|
[18] |
Sadelain M. Chimeric antigen receptors: driving immunology towards synthetic biology. Curr Opin Immunol 2016; 41: 68–76
CrossRef
Pubmed
Google scholar
|
[19] |
Yu H, Sotillo E, Harrington C, Wertheim G, Paessler M, Maude SL, Rheingold SR, Grupp SA, Thomas-Tikhonenko A, Pillai V. Repeated loss of target surface antigen after immunotherapy in primary mediastinal large B cell lymphoma. Am J Hematol 2017; 92(1): E11–E13
CrossRef
Pubmed
Google scholar
|
[20] |
Ritchie DS, Neeson PJ, Khot A, Peinert S, Tai T, Tainton K, Chen K, Shin M, Wall DM, Honemann D, Gambell P, Westerman DA, Haurat J, Westwood JA, Scott AM, Kravets L, Dickinson M, Trapani JA, Smyth MJ, Darcy PK, Kershaw MH, Prince HM. Persistence and efficacy of second generation CAR T cell against the LeY antigen in acute myeloid leukemia. Mol Ther 2013; 21(11): 2122–2129
CrossRef
Pubmed
Google scholar
|
[21] |
Perna F, Berman SH, Soni RK, Mansilla-Soto J, Eyquem J, Hamieh M, Hendrickson RC, Brennan CW, Sadelain M. Integrating proteomics and transcriptomics for systematic combinatorial chimeric antigen receptor therapy of AML. Cancer Cell 2017; 32(4): 506–519.e5
CrossRef
Pubmed
Google scholar
|
[22] |
Giles FJ, Kantarjian HM, Kornblau SM, Thomas DA, Garcia-Manero G, Waddelow TA, David CL, Phan AT, Colburn DE, Rashid A, Estey EH. Mylotarg (gemtuzumab ozogamicin) therapy is associated with hepatic venoocclusive disease in patients who have not received stem cell transplantation. Cancer 2001; 92(2): 406–413
CrossRef
Pubmed
Google scholar
|
[23] |
Kenderian SS, Ruella M, Shestova O, Klichinsky M, Aikawa V, Morrissette JJ, Scholler J, Song D, Porter DL, Carroll M, June CH, Gill S. CD33-specific chimeric antigen receptor T cells exhibit potent preclinical activity against human acute myeloid leukemia. Leukemia 2015; 29(8): 1637–1647
CrossRef
Pubmed
Google scholar
|
[24] |
O’Hear C, Heiber JF, Schubert I, Fey G, Geiger TL. Anti-CD33 chimeric antigen receptor targeting of acute myeloid leukemia. Haematologica 2015; 100(3): 336–344
CrossRef
Pubmed
Google scholar
|
[25] |
Rafiq S, Purdon TJ, Schultz LM, Brentjens RJ. CD33-directed chimeric antigen receptor (CAR) T cells for the treatment of acute myeloid leukemia (AML). Blood 2016; 128(22): 2825
CrossRef
Google scholar
|
[26] |
Wang QS, Wang Y, Lv HY, Han QW, Fan H, Guo B, Wang LL, Han WD. Treatment of CD33-directed chimeric antigen receptor-modified T cells in one patient with relapsed and refractory acute myeloid leukemia. Mol Ther 2015; 23(1): 184–191
CrossRef
Pubmed
Google scholar
|
[27] |
Kim MY, Yu KR, Kenderian SS, Ruella M, Chen S, Shin TH, Aljanahi AA, Schreeder D, Klichinsky M, Shestova O, Kozlowski MS, Cummins KD, Shan X, Shestov M, Bagg A, Morrissette JJD, Sekhri P, Lazzarotto CR, Calvo KR, Kuhns DB, Donahue RE, Behbehani GK, Tsai SQ, Dunbar CE, Gill S. Genetic inactivation of CD33 in hematopoietic stem cells to enable CAR T cell immunotherapy for acute myeloid leukemia. Cell 2018; 173(6): 1439–1453.e19
CrossRef
Pubmed
Google scholar
|
[28] |
Humbert O, Laszlo GS, Sichel S, Ironside C, Haworth KG, Bates OM, Beddoe ME, Carrillo RR, Kiem HP, Walter RB. Engineering resistance to CD33-targeted immunotherapy in normal hematopoiesis by CRISPR/Cas9-deletion of CD33 exon 2. Leukemia 2019; 33(3): 762–808
CrossRef
Pubmed
Google scholar
|
[29] |
Borot F, Wang H, Ma Y, Jafarov T, Raza A, Ali AM, Mukherjee S. Gene-edited stem cells enable CD33-directed immune therapy for myeloid malignancies. Proc Natl Acad Sci USA 2019; 116(24): 11978–11987
CrossRef
Pubmed
Google scholar
|
[30] |
Testa U, Riccioni R, Diverio D, Rossini A, Lo Coco F, Peschle C. Interleukin-3 receptor in acute leukemia. Leukemia 2004; 18(2): 219–226
CrossRef
Pubmed
Google scholar
|
[31] |
Jin L, Lee EM, Ramshaw HS, Busfield SJ, Peoppl AG, Wilkinson L, Guthridge MA, Thomas D, Barry EF, Boyd A, Gearing DP, Vairo G, Lopez AF, Dick JE, Lock RB. Monoclonal antibody-mediated targeting of CD123, IL-3 receptor alpha chain, eliminates human acute myeloid leukemic stem cells. Cell Stem Cell 2009; 5(1): 31–42
CrossRef
Pubmed
Google scholar
|
[32] |
Du X, Ho M, Pastan I. New immunotoxins targeting CD123, a stem cell antigen on acute myeloid leukemia cells. J Immunother 2007; 30(6): 607–613
CrossRef
Pubmed
Google scholar
|
[33] |
Mardiros A, Dos Santos C, McDonald T, Brown CE, Wang X, Budde LE, Hoffman L, Aguilar B, Chang WC, Bretzlaff W, Chang B, Jonnalagadda M, Starr R, Ostberg JR, Jensen MC, Bhatia R, Forman SJ. 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
CrossRef
Pubmed
Google scholar
|
[34] |
Gill S, Tasian SK, Ruella M, Shestova O, Li Y, Porter DL, Carroll M, Danet-Desnoyers G, Scholler J, Grupp SA, June CH, Kalos M. Preclinical targeting of human acute myeloid leukemia and myeloablation using chimeric antigen receptor-modified T cells. Blood 2014; 123(15): 2343–2354
CrossRef
Pubmed
Google scholar
|
[35] |
Ruella M, Barrett DM, Kenderian SS, Shestova O, Hofmann TJ, Perazzelli J, Klichinsky M, Aikawa V, Nazimuddin F, Kozlowski M, Scholler J, Lacey SF, Melenhorst JJ, Morrissette JJ, Christian DA, Hunter CA, Kalos M, Porter DL, June CH, Grupp SA, Gill S. Dual CD19 and CD123 targeting prevents antigen-loss relapses after CD19-directed immunotherapies. J Clin Invest 2016; 126(10): 3814–3826
CrossRef
Pubmed
Google scholar
|
[36] |
Rebmann V, Schütt P, Brandhorst D, Opalka B, Moritz T, Nowrousian MR, Grosse-Wilde H. Soluble MICA as an independent prognostic factor for the overall survival and progression-free survival of multiple myeloma patients. Clin Immunol 2007; 123(1): 114–120
CrossRef
Pubmed
Google scholar
|
[37] |
Taussig DC, Pearce DJ, Simpson C, Rohatiner AZ, Lister TA, Kelly G, Luongo JL, Danet-Desnoyers GA, Bonnet D. Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood 2005; 106(13): 4086–4092
CrossRef
Pubmed
Google scholar
|
[38] |
Wang X, Chang WC, Wong CW, Colcher D, Sherman M, Ostberg JR, Forman SJ, Riddell SR, Jensen MC. A transgene-encoded cell surface polypeptide for selection, in vivo tracking, and ablation of engineered cells. Blood 2011; 118(5): 1255–1263
CrossRef
Pubmed
Google scholar
|
[39] |
Straathof KC, Pulè MA, Yotnda P, Dotti G, Vanin EF, Brenner MK, Heslop HE, Spencer DM, Rooney CM. An inducible caspase 9 safety switch for T-cell therapy. Blood 2005; 105(11): 4247–4254
CrossRef
Pubmed
Google scholar
|
[40] |
Spear P, Wu MR, Sentman ML, Sentman CL. NKG2D ligands as therapeutic targets. Cancer Immun 2013; 13(8): 8
Pubmed
|
[41] |
Hilpert J, Grosse-Hovest L, Grünebach F, Buechele C, Nuebling T, Raum T, Steinle A, Salih HR. Comprehensive analysis of NKG2D ligand expression and release in leukemia: implications for NKG2D-mediated NK cell responses. J Immunol 2012; 189(3): 1360–1371
CrossRef
Pubmed
Google scholar
|
[42] |
Baumeister SH, Murad J, Werner L, Daley H, Trebeden-Negre H, Gicobi JK, Schmucker A, Reder J, Sentman CL, Gilham DE, Lehmann FF, Galinsky I, DiPietro H, Cummings K, Munshi NC, Stone RM, Neuberg DS, Soiffer R, Dranoff G, Ritz J, Nikiforow S. Phase I trial of autologous CAR T cells targeting NKG2D ligands in patients with AML/MDS and multiple myeloma. Cancer Immunol Res 2019; 7(1): 100–112
CrossRef
Pubmed
Google scholar
|
[43] |
Sakamoto J, Furukawa K, Cordon-Cardo C, Yin BW, Rettig WJ, Oettgen HF, Old LJ, Lloyd KO. Expression of Lewisa, Lewisb, X, and Y blood group antigens in human colonic tumors and normal tissue and in human tumor-derived cell lines. Cancer Res 1986; 46(3): 1553–1561
Pubmed
|
[44] |
Westwood JA, Murray WK, Trivett M, Haynes NM, Solomon B, Mileshkin L, Ball D, Michael M, Burman A, Mayura-Guru P, Trapani JA, Peinert S, Hönemann D, Miles Prince H, Scott AM, Smyth MJ, Darcy PK, Kershaw MH. The Lewis-Y carbohydrate antigen is expressed by many human tumors and can serve as a target for genetically redirected T cells despite the presence of soluble antigen in serum. J Immunother 2009; 32(3): 292–301
CrossRef
Pubmed
Google scholar
|
[45] |
Peinert S, Prince HM, Guru PM, Kershaw MH, Smyth MJ, Trapani JA, Gambell P, Harrison S, Scott AM, Smyth FE, Darcy PK, Tainton K, Neeson P, Ritchie DS, Hönemann D. Gene-modified T cells as immunotherapy for multiple myeloma and acute myeloid leukemia expressing the Lewis Y antigen. Gene Ther 2010; 17(5): 678–686
CrossRef
Pubmed
Google scholar
|
[46] |
Ma G, Wang Y, Ahmed T, Zaslav AL, Hogan L, Avila C, Wada M, Salman H. Anti-CD19 chimeric antigen receptor targeting of CD19+ acute myeloid leukemia. Leuk Res Rep 2018; 9(42–44): 42–44
CrossRef
Pubmed
Google scholar
|
[47] |
Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Le Beau MM, Bloomfield CD, Cazzola M, Vardiman JW. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood 2016; 127(20): 2391–2405
CrossRef
Pubmed
Google scholar
|
[48] |
Jetani H, Garcia-Cadenas I, Nerreter T, Thomas S, Rydzek J, Meijide JB, Bonig H, Herr W, Sierra J, Einsele H, Hudecek M. CAR T-cells targeting FLT3 have potent activity against FLT3−ITD+ AML and act synergistically with the FLT3-inhibitor crenolanib. Leukemia 2018; 32(5): 1168–1179
CrossRef
Pubmed
Google scholar
|
[49] |
Chien CD, Sauter C, Ishii K, Nguyen SM, Shen F, Tasian SK, Chen W, Dimitrov DS, Fry TJ. Preclinical development of flt3-redirected chimeric antigen receptor T cell immunotherapy for acute myeloid leukemia. Blood 2016; 128(22): 1072
CrossRef
Google scholar
|
[50] |
Wang Y, Xu Y, Li S, Liu J, Xing Y, Xing H, Tian Z, Tang K, Rao Q, Wang M, Wang J. Targeting FLT3 in acute myeloid leukemia using ligand-based chimeric antigen receptor-engineered T cells. J Hematol Oncol 2018; 11(1): 60
CrossRef
Pubmed
Google scholar
|
[51] |
Campana D, van Dongen JJ, Mehta A, Coustan-Smith E, Wolvers-Tettero IL, Ganeshaguru K, Janossy G. Stages of T-cell receptor protein expression in T-cell acute lymphoblastic leukemia. Blood 1991; 77(7): 1546–1554
CrossRef
Pubmed
Google scholar
|
[52] |
Campana D, Behm FG. Immunophenotyping of leukemia. J Immunol Methods 2000; 243(1-2): 59–75
CrossRef
Pubmed
Google scholar
|
[53] |
Tiftik N, Bolaman Z, Batun S, Ayyildiz O, Isikdogan A, Kadikoylu G, Muftuoglu E. The importance of CD7 and CD56 antigens in acute leukaemias. Int J Clin Pract 2004; 58(2): 149–152
CrossRef
Pubmed
Google scholar
|
[54] |
Miwa H, Nakase K, Kita K. Biological characteristics of CD7+ acute leukemia. Leuk Lymphoma 1996; 21(3-4): 239–244
Pubmed
|
[55] |
Gomes-Silva D, Atilla E, Atilla PA, Mo F, Tashiro H, Srinivasan M, Lulla P, Rouce RH, Cabral JMS, Ramos CA, Brenner MK, Mamonkin M. CD7 CAR T cells for the therapy of acute myeloid leukemia. Mol Ther 2019; 27(1): 272–280
CrossRef
Pubmed
Google scholar
|
[56] |
Bakker AB, van den Oudenrijn S, Bakker AQ, Feller N, van Meijer M, Bia JA, Jongeneelen MA, Visser TJ, Bijl N, Geuijen CA, Marissen WE, Radosevic K, Throsby M, Schuurhuis GJ, Ossenkoppele GJ, de Kruif J, Goudsmit J, Kruisbeek AM. C-type lectin-like molecule-1: a novel myeloid cell surface marker associated with acute myeloid leukemia. Cancer Res 2004; 64(22): 8443–8450
CrossRef
Pubmed
Google scholar
|
[57] |
Wang J, Chen S, Xiao W, Li W, Wang L, Yang S, Wang W, Xu L, Liao S, Liu W, Wang Y, Liu N, Zhang J, Xia X, Kang T, Chen G, Cai X, Yang H, Zhang X, Lu Y, Zhou P. CAR-T cells targeting CLL-1 as an approach to treat acute myeloid leukemia. J Hematol Oncol 2018; 11(1): 7
CrossRef
Pubmed
Google scholar
|
[58] |
Laborda E, Mazagova M, Shao S, Wang X, Quirino H, Woods AK, Hampton EN, Rodgers DT, Kim CH, Schultz PG, Young TS. Development of a chimeric antigen receptor targeting C-type lectin-like molecule-1 for human acute myeloid leukemia. Int J Mol Sci 2017; 18(11): E2259
CrossRef
Pubmed
Google scholar
|
[59] |
Kenderian SS, Habermann TM, Macon WR, Ristow KM, Ansell SM, Colgan JP, Johnston PB, Inwards DJ, Markovic SN, Micallef IN, Thompson CA, Porrata LF, Martenson JA, Witzig TE, Nowakowski GS. Large B-cell transformation in nodular lymphocyte-predominant Hodgkin lymphoma: 40-year experience from a single institution. Blood 2016; 127(16): 1960–1966
CrossRef
Pubmed
Google scholar
|
[60] |
Tashiro H, Sauer T, Shum T, Parikh K, Mamonkin M, Omer B, Rouce RH, Lulla P, Rooney CM, Gottschalk S, Brenner MK. Treatment of acute myeloid leukemia with T cells expressing chimeric antigen receptors directed to C-type lectin-like molecule 1. Mol Ther 2017; 25(9): 2202–2213
CrossRef
Pubmed
Google scholar
|
[61] |
Legras S, Günthert U, Stauder R, Curt F, Oliferenko S, Kluin-Nelemans HC, Marie JP, Proctor S, Jasmin C, Smadja-Joffe F. A strong expression of CD44-6v correlates with shorter survival of patients with acute myeloid leukemia. Blood 1998; 91(9): 3401–3413
CrossRef
Pubmed
Google scholar
|
[62] |
Casucci M, Nicolis di Robilant B, Falcone L, Camisa B, Norelli M, Genovese P, Gentner B, Gullotta F, Ponzoni M, Bernardi M, Marcatti M, Saudemont A, Bordignon C, Savoldo B, Ciceri F, Naldini L, Dotti G, Bonini C, Bondanza A. CD44v6-targeted T cells mediate potent antitumor effects against acute myeloid leukemia and multiple myeloma. Blood 2013; 122(20): 3461–3472
CrossRef
Pubmed
Google scholar
|
[63] |
Ross JF, Wang H, Behm FG, Mathew P, Wu M, Booth R, Ratnam M. Folate receptor type β is a neutrophilic lineage marker and is differentially expressed in myeloid leukemia. Cancer 1999; 85(2): 348–357
CrossRef
Pubmed
Google scholar
|
[64] |
Pan XQ, Zheng X, Shi G, Wang H, Ratnam M, Lee RJ. Strategy for the treatment of acute myelogenous leukemia based on folate receptor β-targeted liposomal doxorubicin combined with receptor induction using all-trans retinoic acid. Blood 2002; 100(2): 594–602
CrossRef
Pubmed
Google scholar
|
[65] |
Lynn RC, Poussin M, Kalota A, Feng Y, Low PS, Dimitrov DS, Powell DJ Jr. Targeting of folate receptor b on acute myeloid leukemia blasts with chimeric antigen receptor-expressing T cells. Blood 2015; 125(22): 3466–3476
CrossRef
Pubmed
Google scholar
|
[66] |
Lynn RC, Feng Y, Schutsky K, Poussin M, Kalota A, Dimitrov DS, Powell DJ Jr. High-affinity FRb-specific CAR T cells eradicate AML and normal myeloid lineage without HSC toxicity. Leukemia 2016; 30(6): 1355–1364
CrossRef
Pubmed
Google scholar
|
[67] |
Jiang H, Li C, Yin P, Guo T, Liu L, Xia L, Wu Y, Zhou F, Ai L, Shi W, Lu X, Wang H, Tang L, Wei Q, Deng J, Jin R, Xiong W, Dong J, Mei H, Hu Y. Anti-CD19 chimeric antigen receptor-modified T-cell therapy bridging to allogeneic hematopoietic stem cell transplantation for relapsed/refractory B-cell acute lymphoblastic leukemia: an open-label pragmatic clinical trial. Am J Hematol 2019; 94(10): 1113–1122
CrossRef
Pubmed
Google scholar
|
[68] |
Park JH, Rivière I, Gonen M, Wang X, Sénéchal B, Curran KJ, Sauter C, Wang Y, Santomasso B, Mead E, Roshal M, Maslak P, Davila M, Brentjens RJ, Sadelain M. Long-term follow-up of CD19 CAR therapy in acute lymphoblastic leukemia. N Engl J Med 2018; 378(5): 449–459
CrossRef
Pubmed
Google scholar
|
[69] |
Zhu YM, Wu Z, Tan YP, Du YY, Liu Z, Ou RM, Liu S, Pu CF, Jiang J, Wang JP, Xiao L, Zhang Q. Anti-CD19 chimeric antigen receptor T-cell therapy for adult Philadelphia chromosome-positive acute lymphoblastic leukemia: two case reports. Medicine (Baltimore) 2016; 95(51): e5676
CrossRef
Pubmed
Google scholar
|
[70] |
Maude SL, Laetsch TW, Buechner J, Rives S, Boyer M, Bittencourt H, Bader P, Verneris MR, Stefanski HE, Myers GD, Qayed M, De Moerloose B, Hiramatsu H, Schlis K, Davis KL, Martin PL, Nemecek ER, Yanik GA, Peters C, Baruchel A, Boissel N, Mechinaud F, Balduzzi A, Krueger J, June CH, Levine BL, Wood P, Taran T, Leung M, Mueller KT, Zhang Y, Sen K, Lebwohl D, Pulsipher MA, Grupp SA. Tisagenlecleucel in children and young adults with B-cell lymphoblastic leukemia. N Engl J Med 2018; 378(5): 439–448
CrossRef
Pubmed
Google scholar
|
/
〈 | 〉 |