دورية أكاديمية

Current perspectives on resistance to chimeric antigen receptor T-cell therapy and strategies to improve efficacy in B-cell lymphoma.

التفاصيل البيبلوغرافية
العنوان: Current perspectives on resistance to chimeric antigen receptor T-cell therapy and strategies to improve efficacy in B-cell lymphoma.
المؤلفون: Ong SY; Department of Haematology, Singapore General Hospital, Singapore, Singapore., Chen Y; Department of Haematology, Singapore General Hospital, Singapore, Singapore., Tan MSY; Department of Haematology, Singapore General Hospital, Singapore, Singapore., Ho AYL; Department of Haematology, Singapore General Hospital, Singapore, Singapore., Hwang WYK; Department of Haematology, Singapore General Hospital, Singapore, Singapore.; Division of Medical Oncology, National Cancer Centre, Singapore, Singapore., Lim FLWI; Department of Haematology, Singapore General Hospital, Singapore, Singapore.
المصدر: European journal of haematology [Eur J Haematol] 2024 Feb; Vol. 112 (2), pp. 144-152. Date of Electronic Publication: 2023 Apr 03.
نوع المنشور: Journal Article; Review
اللغة: English
بيانات الدورية: Publisher: Blackwell Country of Publication: England NLM ID: 8703985 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1600-0609 (Electronic) Linking ISSN: 09024441 NLM ISO Abbreviation: Eur J Haematol Subsets: MEDLINE
أسماء مطبوعة: Publication: <2005->: Oxford : Blackwell
Original Publication: Copenhagen : Munksgaard, c1987-
مواضيع طبية MeSH: Receptors, Chimeric Antigen*/genetics , Lymphoma, B-Cell*/therapy, Humans ; Immunotherapy, Adoptive/adverse effects ; Receptors, Antigen, T-Cell/genetics ; Antigens, CD19 ; Recurrence ; Cell- and Tissue-Based Therapy ; Tumor Microenvironment
مستخلص: Although chimeric antigen receptor (CAR) T-cell therapy has demonstrated remarkable efficacy in patients with chemo-refractory B-cell lymphoma, a significant portion is refractory or relapse. Resistance is a major barrier to improving treatment efficacy and long-term survival in CAR T-cell therapy, and clinicians have very limited tools to discriminate a priori patients who will or will not respond to treatment. While CD19-negative relapses due to loss of target antigen is well described, it accounts for only about 30% of cases with treatment failure. Recent efforts have shed light on mechanisms of CD19-positive relapse due to tumor intrinsic resistance, T-cell quality/manufacturing, or CAR T-cell exhaustion mediated by hostile tumor microenvironment. Here, we review the latest updates of preclinical and clinical trials to investigate the mechanisms of resistance and relapse post CAR T-cell therapy in B cell lymphoma and discuss novel treatment strategies to overcome resistance as well as advances that are useful for a CAR T therapist to optimize and personalize CAR T-cell therapy.
(© 2023 The Authors. European Journal of Haematology published by John Wiley & Sons Ltd.)
References: Dotti G, Gottschalk S, Savoldo B, Brenner MK. Design and development of therapies using chimeric antigen receptor-expressing T cells. Immunol Rev. 2014;257:107-126.
Schuster SJ, Bishop MR, Tam CS, et al. Tisagenlecleucel in adult relapsed or refractory diffuse large B-cell lymphoma. N Engl J Med. 2019;380:45-56.
Abramson JS, Palomba ML, Gordon LI, et al. Lisocabtagene maraleucel for patients with relapsed or refractory large B-cell lymphomas (TRANSCEND NHL 001): a multicentre seamless design study. Lancet. 2020;396:839-852.
Neelapu SS, Locke FL, Bartlett NL, et al. Axicabtagene ciloleucel CAR T-cell therapy in refractory large B-cell lymphoma. N Engl J Med. 2017;377:2531-2544.
Jacobson CA, Hunter BD, Redd R, et al. Axicabtagene ciloleucel in the non-trial setting: outcomes and correlates of response, resistance, and toxicity. J Clin Oncol. 2020;38:3095-3106.
Dean EA, Mhaskar RS, Lu H, et al. High metabolic tumor volume is associated with decreased efficacy of axicabtagene ciloleucel in large B-cell lymphoma. Blood Adv. 2020;4:3268-3276.
Plaks V, Rossi JM, Chou J, et al. CD19 target evasion as a mechanism of relapse in large B-cell lymphoma treated with axicabtagene ciloleucel. Blood. 2021;138:1081-1085.
Orlando EJ, Han X, Tribouley C, et al. Genetic mechanisms of target antigen loss in CAR19 therapy of acute lymphoblastic leukemia. Nat Med. 2018;24:1504-1506.
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;5:1282-1295.
Zhang Z, Chen X, Tian Y, et al. Point mutation in CD19 facilitates immune escape of B cell lymphoma from CAR-T cell therapy. J Immunother Cancer. 2020;8:e001150.
Ledererova A, Dostalova L, Kozlova V, et al. Hypermethylation of CD19 promoter enables antigen-negative escape to CART-19 in vivo and in vitro. J Immunother Cancer. 2021;9:e002352.
Fitzgerald KN, Quesada AE, von Keudell G, et al. CD19 epitope masking by tafasitamab leads to delays in subsequent use of CD19 CAR T-cell therapy in two patients with aggressive mature B-cell lymphomas. Leuk Lymphoma. 2022;63:751-754.
Zhang Q, Orlando EJ, Wang HY, et al. Transdifferentiation of lymphoma into sarcoma associated with profound reprogramming of the epigenome. Blood. 2020;136:1980-1983.
Hamieh M, Dobrin A, Cabriolu A, et al. CAR T cell trogocytosis and cooperative killing regulate tumour antigen escape. Nature. 2019;568:112-116.
Challa-Malladi M, Lieu YK, Califano O, et al. Combined genetic inactivation of β2-microglobulin and CD58 reveals frequent escape from immune recognition in diffuse large B cell lymphoma. Cancer Cell. 2011;20(6):728-740.
Majzner RG, Frank MJ, Mount C, et al. CD58 aberrations limit durable responses to CD19 CAR in large B cell lymphoma patients treated with axicabtagene ciloleucel but can be overcome through novel CAR engineering. Blood. 2020;136(1):53-54.
Yan X, Chen D, Ma X, et al. CD58 loss in tumor cells confers functional impairment of CAR T cells. Blood Adv. 2022;6(22):5844-5856.
Romain G, Strati P, Rezvan A, et al. Multidimensional single-cell analysis identifies a role for CD2-CD58 interactions in clinical antitumor T cell responses. J Clin Invest. 2022;132(17):e159402.
Spiegel JY, Patel S, Muffly L, et al. CAR T cells with dual targeting of CD19 and CD22 in adult patients with recurrent or refractory B cell malignancies: a phase 1 trial. Nat Med. 2021;27:1419-1431.
Majzner RG, Rietberg SP, Sotillo E, et al. Tuning the antigen density requirement for CAR T-cell activity. Cancer Discov. 2020;10:702-723.
Watanabe K, Terakura S, Martens AC, et al. Target antigen density governs the efficacy of anti-CD20-CD28-CD3 zeta chimeric antigen receptor-modified effector CD8 + T cells. J Immunol. 2015;194(3):911-920.
Shah NN, Johnson BD, Schneider D, et al. Bispecific anti-CD20, anti-CD19 CAR T cells for relapsed B cell malignancies: a phase 1 dose escalation and expansion trial. Nat Med. 2020;26:1569-1575.
Zhang Y, Wang Y, Liu Y, et al. Long-term activity of tandem CD19/CD20 CAR therapy in refractory/relapsed B-cell lymphoma: a single-arm, phase 1-2 trial. Leukemia. 2022;36:189-196.
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;75:3596-3607.
Kueberuwa G, Kalaitsidou M, Cheadle E, Hawkins RE, Gilham DE. CD19 CAR T cells expressing IL-12 eradicate lymphoma in fully lymphoreplete mice through induction of host immunity. Mol Ther Oncolytics. 2017;19(8):41-51.
Gaidarova S, Corral LG, Gleizer E, et al. Lenalidomide enhances anti-tumor effect of gamma delta T cells against mantle cell lymphoma. Blood. 2008;112:2616.
Otsuka Y, Nishikori M, Arima H, et al. EZH2 inhibitors restore epigenetically silenced CD58 expression in B-cell lymphomas. Mol Immunol. 2020;119:35-45.
Singh N, Lee YG, Shestova O, et al. Impaired death receptor signaling in leukemia causes antigen-independent resistance by inducing CAR T-cell dysfunction. Cancer Discov. 2020;10:552-567.
Cherng HJ, Sun R, Sugg B, et al. Risk assessment with low-pass whole-genome sequencing of cell-free DNA before CD19 CAR T-cell therapy for large B-cell lymphoma. Blood. 2022;140:504-515.
Shouval R, Alarcon Tomas A, Fein JA, et al. Impact of TP53 genomic alterations in large B-cell lymphoma treated with CD19-chimeric antigen receptor T-cell therapy. J Clin Oncol. 2022;40:369-381.
Jain MD, Ziccheddu B, Coughlin CA, et al. Whole-genome sequencing reveals complex genomic features underlying anti-CD19 CAR T-cell treatment failures in lymphoma. Blood. 2022;140:491-503.
Torres-Collado AX, Jazirehi AR. Overcoming resistance of human non-Hodgkin's lymphoma to CD19-CAR CTL therapy by celecoxib and histone deacetylase inhibitors. Cancers (Basel). 2018;10:200.
Dufva O, Koski J, Maliniemi P, et al. Integrated drug profiling and CRISPR screening identify essential pathways for CAR T-cell cytotoxicity. Blood. 2020;135:597-609.
Yang M, Wang L, Ni M, et al. Pre-sensitization of malignant B cells through Venetoclax significantly improves the cytotoxic efficacy of CD19 CAR-T cells. Front Immunol. 2020;11:608167.
Ramsay AG, Johnson AJ, Lee AM, et al. Chronic lymphocytic leukemia T cells show impaired immunological synapse formation that can be reversed with an immunomodulating drug. J Clin Invest. 2008;118:427-2437.
Singh N, Perazzelli J, Grupp SA, Barrett DM. Early memory phenotypes drive T cell proliferation in patients with pediatric malignancies. Sci Transl Med. 2016 Jan;6(8):3203.
Duell J, Lukic DS, Karg M, et al. Functionally defective T cells after chemotherapy of B-cell malignancies can be activated by the tetravalent bispecific CD19/CD3 antibody AFM11. J Immunother. 2019;42:180.
Locke FL, Rossi JM, Neelapu SS, et al. Tumor burden, inflammation, and product attributes determine outcomes of axicabtagene ciloleucel in large B-cell lymphoma. Blood Adv. 2020;4:4898-4911.
Deng Q, Han G, Puebla-Osorio N, et al. Characteristics of anti-CD19 CAR T cell infusion products associated with efficacy and toxicity in patients with large B cell lymphomas. Nat Med. 2020;26:1878-1887.
Rossi J, Paczkowski P, Shen YW, et al. Preinfusion polyfunctional anti-CD19 chimeric antigen receptor T cells are associated with clinical outcomes in NHL. Blood. 2018;132:804-814.
van Bruggen JAC, Martens AWJ, Fraietta JA, et al. Chronic lymphocytic leukemia cells impair mitochondrial fitness in CD8+ T cells and impede CAR T-cell efficacy. Blood. 2019;134:44-58.
Chen GM, Chen C, Das RK, et al. Integrative bulk and single-cell profiling of premanufacture T-cell populations reveals factors mediating Long-term persistence of CAR T-cell therapy. Cancer Discov. 2021;11:2186-2199.
Lee JC, Hayman E, Pegram HJ, et al. In vivo inhibition of human CD19-targeted effector T cells by natural T regulatory cells in a xenotransplant murine model of B cell malignancy. Cancer Res. 2011;71:2871-2881.
Haradhvala NJ, Leick MB, Maurer K, et al. Distinct cellular dynamics associated with response to CAR-T therapy for refractory B cell lymphoma. Nat Med. 2022;28:1848-1859.
Good Z, Spiegel JY, Sahaf B, et al. Post-infusion CAR TReg cells identify patients resistant to CD19-CAR therapy. Nat Med. 2022;28:1860-1871.
Neelapu SS, Dickinson M, Munoz J, et al. Axicabtagene ciloleucel as first-line therapy in high-risk large B-cell lymphoma: the phase 2 ZUMA-12 trial. Nat Med. 2022;28:735-742.
Gauthier J, Hirayama AV, Purushe J, et al. Feasibility and efficacy of CD19-targeted CAR T cells with concurrent ibrutinib for CLL after ibrutinib failure. Blood. 2020;135:1650-1660.
Cieri N, Camisa B, Cocchiarella F, et al. IL-7 and IL-15 instruct the generation of human memory stem T cells from naive precursors. Blood. 2013;121:573-584.
Gargett T, Truong N, Ebert LM, Yu W, Brown MP. Optimization of manufacturing conditions for chimeric antigen receptor T cells to favor cells with a central memory phenotype. Cytotherapy. 2019;21:593-602.
Klebanoff CA, Crompton JG, Leonardi AJ, et al. Inhibition of AKT signaling uncouples T cell differentiation from expansion for receptor-engineered adoptive immunotherapy. JCI Insight. 2017;2:e95103.
Kong W, Dimitri A, Wang W, et al. BET bromodomain protein inhibition reverses chimeric antigen receptor extinction and reinvigorates exhausted T cells in chronic lymphocytic leukemia. J Clin Invest. 2021;131:e145459.
Arcangeli S, Bove C, Mezzanotte C, et al. CAR T cell manufacturing from naive/stem memory T lymphocytes enhances antitumor responses while curtailing cytokine release syndrome. J Clin Invest. 2022;132:e150807.
Wang X, Borquez-Ojeda O, Stefanski J, et al. Depletion of high-content CD14+ cells from apheresis products is critical for successful transduction and expansion of CAR T cells during large-scale cGMP manufacturing. Mol Ther Methods Clin Dev. 2021;22:377-387.
Derman BA, Zha Y, Zimmerman TM, et al. Regulatory T-cell depletion in the setting of autologous stem cell transplantation for multiple myeloma: pilot study. J Immunother Cancer. 2020;8:e000286.
Depil S, Duchateau P, Grupp SA, Mufti G, Poirot L. 'Off-the-shelf' allogeneic CAR T cells: development and challenges. Nat Rev Drug Discov. 2020;19:185-199.
Jain MD, Zhao H, Wang X, et al. Tumor interferon signaling and suppressive myeloid cells are associated with CAR T-cell failure in large B-cell lymphoma. Blood. 2021;137:2621-2633.
Scholler N, Perbost R, Locke FL, et al. Tumor immune contexture is a determinant of anti-CD19 CAR T cell efficacy in large B cell lymphoma. Nat Med. 2022;28:1872-1882.
Long AH, Highfill SL, Cui Y, et al. Reduction of MDSCs with all-trans retinoic acid improves CAR therapy efficacy for sarcomas. Cancer Immunol Res. 2016;4:869-880.
Chen J, López-Moyado IF, Seo H, et al. NR4A transcription factors limit CAR T cell function in solid tumours. Nature. 2019;567:530-534.
Fraietta JA, Lacey SF, Orlando EJ, et al. Determinants of response and resistance to CD19 chimeric antigen receptor (CAR) T cell therapy of chronic lymphocytic leukemia. Nat Med. 2018;24:563-571.
Guedan S, Madar A, Casado-Medrano V, et al. Single residue in CD28-costimulated CAR-T cells limits long-term persistence and antitumor durability. J Clin Invest. 2020;130:3087-3097.
Riedell PA, Hwang WT, Nastoupil LJ, et al. Patterns of use, outcomes, and resource utilization among recipients of commercial axicabtagene ciloleucel and tisagenlecleucel for relapsed/refractory aggressive B cell lymphomas. Transplant Cell Ther. 2022;28:669-676.
Bachy E, Le Gouill S, Di Blasi R, et al. A real-world comparison of tisagenlecleucel and axicabtagene ciloleucel CAR T cells in relapsed or refractory diffuse large B cell lymphoma. Nat Med. 2022;28:2145-2154.
Maloney DG, Kuruvilla J, Liu FF, et al. Matching-adjusted indirect treatment comparison of liso-cel versus axi-cel in relapsed or refractory large B cell lymphoma. J Hematol Oncol. 2021;14:140.
Barba P, Kwon M, Btiones J, et al. YTB323 (rapcabtagene autoleucel) demonstrates durable efficacy and a manageable safety profiles in patients with relapsed/ refractory DLBCL: phase I study update. Presented at ASH. 2022;140:1056-1059.
Razeghian E, Nasution MKM, Rahman HS, et al. A deep insight into CRISPR/Cas9 application in CAR-T cell-based tumor immunotherapies. Stem Cell Res Ther. 2021;12:428.
Xie G, Dong H, Liang Y, Ham JD, Rizwan R, Chen J. CAR-NK cells: a promising cellular immunotherapy for cancer. EBioMedicine. 2020;59:102975.
Liu E, Marin D, Banerjee P, et al. Use of CAR-transduced natural killer cells in CD19-positive lymphoid tumors. N Engl J Med. 2020;382:545-553.
Reinhard K, Rengstl B, Oehm P, et al. An RNA vaccine drives expansion and efficacy of claudin-CAR-T cells against solid tumors. Science. 2020;367:446-453.
Ghassemi S, Nunez-Cruz S, O'Connor RS, et al. Reducing ex vivo culture improves the antileukemic activity of chimeric antigen receptor (CAR) T cells. Cancer Immunol Res. 2018;6:1100-1109.
Alizadeh D, Wong RA, Yang X, et al. IL15 enhances CAR-T cell antitumor activity by reducing mTORC1 activity and preserving their stem cell memory phenotype. Cancer Immunol Res. 2019;7:759-772.
Funk CR, Wang S, Chen KZ, et al. PI3Kδ/γ inhibition promotes human CART cell epigenetic and metabolic reprogramming to enhance antitumor cytotoxicity. Blood. 2022;139:523-537.
Mestermann K, Giavridis T, Weber J, et al. The tyrosine kinase inhibitor dasatinib acts as a pharmacologic on/off switch for CAR T cells. Sci Transl Med. 2019;11:907.
Feucht J, Sun J, Eyquem J, et al. Calibration of CAR activation potential directs alternative T cell fates and therapeutic potency. Nat Med. 2019;25:82-88.
Lynn RC, Weber EW, Sotillo E, et al. c-Jun overexpression in CAR T cells induces exhaustion resistance. Nature. 2019;576:293-300.
Eyquem J, Mansilla-Soto J, Giavridis T, et al. Targeting a CAR to the TRAC locus with CRISPR/Cas9 enhances tumour rejection. Nature. 2017;543:113-117.
Jacobson CA, Westin JR, Miklos DB, et al. Abstract CT055: phase 1/2 primary analysis of ZUMA-6: axicabtagene ciloleucel (Axi-Cel) in combination with atezolizumab (Atezo) for the treatment of patients (pts) with refractory diffuse large B cell lymphoma (DLBCL). Cancer Res. 2020;80:CT055.
Rafiq S, Yeku OO, Jackson HJ, et al. Targeted delivery of a PD-1-blocking scFv by CAR-T cells enhances anti-tumor efficacy in vivo. Nat Biotechnol. 2018;36:847-856.
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;126:3130-3144.
Ren J, Liu X, Fang C, Jiang S, June CH, Zhao Y. Multiplex genome editing to generate universal CAR T cells resistant to PD1 inhibition. Clin Cancer Res. 2017;23:2255-2266.
Seo H, Chen J, González-Avalos E, et al. TOX and TOX2 transcription factors cooperate with NR4A transcription factors to impose CD8+ T cell exhaustion. Proc Natl Acad Sci U S A. 2019;116:12410-12415.
Seo H, González-Avalos E, Zhang W, et al. BATF and IRF4 cooperate to counter exhaustion in tumor-infiltrating CAR T cells. Nat Immunol. 2021;22:983-995.
Good CR, Aznar MA, Kuramitsu S, et al. An NK-like CAR T cell transition in CAR T cell dysfunction. Cell. 2021;184:6081-6100.e26.
Pace L, Goudot C, Zueva E, et al. The epigenetic control of stemness in CD8+ T cell fate commitment. Science. 2018;359:177-186.
Dumauthioz N, Tschumi B, Wenes M, et al. Enforced PGC-1α expression promotes CD8 T cell fitness, memory formation and antitumor immunity. Cell Mol Immunol. 2021;18:1761-1771.
فهرسة مساهمة: Keywords: B-cell lymphoma; CD19; T cell exhaustion; antigen escape; chimeric antigen receptor
المشرفين على المادة: 0 (Receptors, Chimeric Antigen)
0 (Receptors, Antigen, T-Cell)
0 (Antigens, CD19)
تواريخ الأحداث: Date Created: 20230329 Date Completed: 20240117 Latest Revision: 20240117
رمز التحديث: 20240117
DOI: 10.1111/ejh.13964
PMID: 36987995
قاعدة البيانات: MEDLINE
الوصف
تدمد:1600-0609
DOI:10.1111/ejh.13964