Trogocytosis in CAR immune cell therapy: a key mechanism of tumor immune escape.
CAR-NK
CAR-T
Fratricide
Immune escape
Trogocytosis
Journal
Cell communication and signaling : CCS
ISSN: 1478-811X
Titre abrégé: Cell Commun Signal
Pays: England
ID NLM: 101170464
Informations de publication
Date de publication:
28 Oct 2024
28 Oct 2024
Historique:
received:
10
09
2024
accepted:
15
10
2024
medline:
29
10
2024
pubmed:
29
10
2024
entrez:
29
10
2024
Statut:
epublish
Résumé
Immune cell therapy based on chimeric antigen receptor (CAR) technology platform has been greatly developed. The types of CAR immune cell therapy have expanded from T cells to innate immune cells such as NK cells and macrophages, and the diseases treated have expanded from hematological malignancies to non-tumor fields such as infectious diseases and autoimmune diseases. Among them, CAR-T and CAR-NK therapy have observed examples of rapid remission in approved clinical trials, but the efficacy is unstable and plagued by tumor resistance. Trogocytosis is a special phenomenon of intercellular molecular transfer that is common in the immune system and is achieved by recipient cells through acquisition and internalization of donor cell-derived molecules and mediates immune effects. Recently, a novel short-term drug resistance mechanism based on trogocytosis has been proposed, and the bidirectional molecular exchange between CAR immune cells and tumor cells triggered by trogocytosis partially explains the long-term relapse phenomenon after treatment with CAR immune cells. In this review, we summarize the research progress of trogocytosis in CAR immunotherapy, discuss the influencing factors of trogocytosis and its direct and indirect interference with CAR immune cells and emphasize that the interference of trogocytosis can further release the potential of CAR immune cell therapy.
Identifiants
pubmed: 39468646
doi: 10.1186/s12964-024-01894-2
pii: 10.1186/s12964-024-01894-2
doi:
Substances chimiques
Receptors, Chimeric Antigen
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
521Subventions
Organisme : Basic and Clinical Cooperative Research Program of Anhui Medical University Incubation Project for The Third Affiliated Hospital
ID : 2022sfy017
Informations de copyright
© 2024. The Author(s).
Références
DeVita VT Jr., Chu E. A history of cancer chemotherapy. Cancer Res. 2008;68:8643–53.
pubmed: 18974103
doi: 10.1158/0008-5472.CAN-07-6611
Kang E, Kang JH, Koh SJ, Kim YJ, Seo S, Kim JH, Cheon J, Kang EJ, Song EK, Nam EM, et al. Early Integrated Palliative Care in patients with Advanced Cancer: a Randomized Clinical Trial. JAMA Netw Open. 2024;7:e2426304.
pubmed: 39115845
pmcid: 11310828
doi: 10.1001/jamanetworkopen.2024.26304
Greer JA, Applebaum AJ, Jacobsen JC, Temel JS, Jackson VA. Understanding and addressing the role of coping in Palliative Care for patients with Advanced Cancer. J Clin Oncol. 2020;38:915–25.
pubmed: 32023161
pmcid: 7082158
doi: 10.1200/JCO.19.00013
Liu B, Zhou H, Tan L, Siu KTH, Guan XY. Exploring treatment options in cancer: tumor treatment strategies. Signal Transduct Target Ther. 2024;9:175.
pubmed: 39013849
pmcid: 11252281
doi: 10.1038/s41392-024-01856-7
André F, Rassy E, Marabelle A, Michiels S, Besse B. Forget lung, breast or prostate cancer: why tumour naming needs to change. Nature. 2024;626:26–9.
pubmed: 38347121
doi: 10.1038/d41586-024-00216-3
Zhang Y, Zhang Z. The history and advances in cancer immunotherapy: understanding the characteristics of tumor-infiltrating immune cells and their therapeutic implications. Cell Mol Immunol. 2020;17:807–21.
pubmed: 32612154
pmcid: 7395159
doi: 10.1038/s41423-020-0488-6
Ledford H. Melanoma drug wins US approval. Nature. 2011;471:561.
pubmed: 21455150
doi: 10.1038/471561a
Buonerba C, Ferro M, Di Lorenzo G. Sipuleucel-T for prostate cancer: the immunotherapy era has commenced. Expert Rev Anticancer Ther. 2011;11:25–8.
pubmed: 21166508
doi: 10.1586/era.10.180
Foy SP, Jacoby K, Bota DA, Hunter T, Pan Z, Stawiski E, Ma Y, Lu W, Peng S, Wang CL, et al. Non-viral precision T cell receptor replacement for personalized cell therapy. Nature. 2023;615:687–96.
pubmed: 36356599
doi: 10.1038/s41586-022-05531-1
Melenhorst JJ, Chen GM, Wang M, Porter DL, Chen C, Collins MA, Gao P, Bandyopadhyay S, Sun H, Zhao Z, et al. Decade-long leukaemia remissions with persistence of CD4(+) CAR T cells. Nature. 2022;602:503–9.
pubmed: 35110735
pmcid: 9166916
doi: 10.1038/s41586-021-04390-6
Ramamurthy A, Tommasi A, Saha K. Advances in manufacturing chimeric antigen receptor immune cell therapies. Semin Immunopathol. 2024;46:12.
pubmed: 39150566
doi: 10.1007/s00281-024-01019-4
Wu J, Wu W, Zhou B, Li B. Chimeric antigen receptor therapy meets mRNA technology. Trends Biotechnol. 2024;42:228–40.
pubmed: 37741706
doi: 10.1016/j.tibtech.2023.08.005
Keshavarz A, Salehi A, Khosravi S, Shariati Y, Nasrabadi N, Kahrizi MS, Maghsoodi S, Mardi A, Azizi R, Jamali S, Fotovat F. Recent findings on chimeric antigen receptor (CAR)-engineered immune cell therapy in solid tumors and hematological malignancies. Stem Cell Res Ther. 2022;13:482.
pubmed: 36153626
pmcid: 9509604
doi: 10.1186/s13287-022-03163-w
Kittai AS, Bond D, Huang Y, Bhat SA, Blyth E, Byrd JC, Chavez JC, Davids MS, Dela Cruz JP, Dowling MR, et al. Anti-CD19 chimeric Antigen receptor T-Cell therapy for Richter Transformation: An International, Multicenter, Retrospective Study. J Clin Oncol. 2024;42:2071–9.
pubmed: 38552193
doi: 10.1200/JCO.24.00033
Parikh RH, Lonial S. Chimeric antigen receptor T-cell therapy in multiple myeloma: a comprehensive review of current data and implications for clinical practice. CA Cancer J Clin. 2023;73:275–85.
pubmed: 36627265
doi: 10.3322/caac.21771
Tsiverioti CA, Gottschlich A, Trefny M, Theurich S, Anders HJ, Kroiss M, Kobold S. Beyond CAR T cells: exploring alternative cell sources for CAR-like cellular therapies. Biol Chem. 2024;405:485–515.
pubmed: 38766710
doi: 10.1515/hsz-2023-0317
Yang R, Yang Y, Liu R, Wang Y, Yang R, He A. Advances in CAR-NK cell therapy for hematological malignancies. Front Immunol. 2024;15:1414264.
pubmed: 39007146
pmcid: 11239349
doi: 10.3389/fimmu.2024.1414264
Uslu U, Castelli S, June CH. CAR T cell combination therapies to treat cancer. Cancer Cell. 2024;42:1319–25.
pubmed: 39059390
doi: 10.1016/j.ccell.2024.07.002
Ebrahimiyan H, Tamimi A, Shokoohian B, Minaei N, Memarnejadian A, Hossein-Khannazer N, Hassan M, Vosough M. Novel insights in CAR-NK cells beyond CAR-T cell technology; promising advantages. Int Immunopharmacol. 2022;106:108587.
pubmed: 35149294
doi: 10.1016/j.intimp.2022.108587
Chen Y, Yu Z, Tan X, Jiang H, Xu Z, Fang Y, Han D, Hong W, Wei W, Tu J. CAR-macrophage: a new immunotherapy candidate against solid tumors. Biomed Pharmacother. 2021;139:111605.
pubmed: 33901872
doi: 10.1016/j.biopha.2021.111605
Klichinsky M, Ruella M, Shestova O, Lu XM, Best A, Zeeman M, Schmierer M, Gabrusiewicz K, Anderson NR, Petty NE, et al. Human chimeric antigen receptor macrophages for cancer immunotherapy. Nat Biotechnol. 2020;38:947–53.
pubmed: 32361713
pmcid: 7883632
doi: 10.1038/s41587-020-0462-y
Xin Q, Chen Y, Sun X, Li R, Wu Y, Huang X. CAR-T therapy for ovarian cancer: recent advances and future directions. Biochem Pharmacol. 2024;226:116349.
pubmed: 38852648
doi: 10.1016/j.bcp.2024.116349
Rosado-Sánchez I, Levings MK. Building a CAR-Treg: going from the basic to the luxury model. Cell Immunol. 2020;358:104220.
pubmed: 33096321
doi: 10.1016/j.cellimm.2020.104220
Chang Y, Cai X, Syahirah R, Yao Y, Xu Y, Jin G, Bhute VJ, Torregrosa-Allen S, Elzey BD, Won YY, et al. CAR-neutrophil mediated delivery of tumor-microenvironment responsive nanodrugs for glioblastoma chemo-immunotherapy. Nat Commun. 2023;14:2266.
pubmed: 37080958
pmcid: 10119091
doi: 10.1038/s41467-023-37872-4
Mackensen A, Müller F, Mougiakakos D, Böltz S, Wilhelm A, Aigner M, Völkl S, Simon D, Kleyer A, Munoz L, et al. Anti-CD19 CAR T cell therapy for refractory systemic lupus erythematosus. Nat Med. 2022;28:2124–32.
pubmed: 36109639
doi: 10.1038/s41591-022-02017-5
Dai H, Zhu C, Huai Q, Xu W, Zhu J, Zhang X, Zhang X, Sun B, Xu H, Zheng M, et al. Chimeric antigen receptor-modified macrophages ameliorate liver fibrosis in preclinical models. J Hepatol. 2024;80:913–27.
pubmed: 38340812
doi: 10.1016/j.jhep.2024.01.034
Rurik JG, Tombácz I, Yadegari A, Méndez Fernández PO, Shewale SV, Li L, Kimura T, Soliman OY, Papp TE, Tam YK, et al. CAR T cells produced in vivo to treat cardiac injury. Science. 2022;375:91–6.
pubmed: 34990237
pmcid: 9983611
doi: 10.1126/science.abm0594
Lu J, Jiang G. The journey of CAR-T therapy in hematological malignancies. Mol Cancer. 2022;21:194.
pubmed: 36209106
pmcid: 9547409
doi: 10.1186/s12943-022-01663-0
Zhang J, Hu Y, Yang J, Li W, Zhang M, Wang Q, Zhang L, Wei G, Tian Y, Zhao K, et al. Non-viral, specifically targeted CAR-T cells achieve high safety and efficacy in B-NHL. Nature. 2022;609:369–74.
pubmed: 36045296
pmcid: 9452296
doi: 10.1038/s41586-022-05140-y
Majzner RG, Mackall CL. Tumor Antigen escape from CAR T-cell therapy. Cancer Discov. 2018;8:1219–26.
pubmed: 30135176
doi: 10.1158/2159-8290.CD-18-0442
Kaczanowska S, Murty T, Alimadadi A, Contreras CF, Duault C, Subrahmanyam PB, Reynolds W, Gutierrez NA, Baskar R, Wu CJ, et al. Immune determinants of CAR-T cell expansion in solid tumor patients receiving GD2 CAR-T cell therapy. Cancer Cell. 2024;42:35–e5138.
pubmed: 38134936
doi: 10.1016/j.ccell.2023.11.011
Zeng W, Zhang P. Resistance and recurrence of malignancies after CAR-T cell therapy. Exp Cell Res. 2022;410:112971.
pubmed: 34906583
doi: 10.1016/j.yexcr.2021.112971
Rejeski K, Jain MD, Smith EL. Mechanisms of resistance and treatment of Relapse after CAR T-cell therapy for large B-cell lymphoma and multiple myeloma. Transpl Cell Ther. 2023;29:418–28.
doi: 10.1016/j.jtct.2023.04.007
Joly E, Hudrisier D. What is trogocytosis and what is its purpose? Nat Immunol. 2003;4:815.
pubmed: 12942076
doi: 10.1038/ni0903-815
Matlung HL, Babes L, Zhao XW, van Houdt M, Treffers LW, van Rees DJ, Franke K, Schornagel K, Verkuijlen P, Janssen H, et al. Neutrophils kill antibody-opsonized Cancer cells by Trogoptosis. Cell Rep. 2018;23:3946–e39593946.
pubmed: 29949776
doi: 10.1016/j.celrep.2018.05.082
Agbakwuru D, Wetzel SA. The Biological significance of trogocytosis. Results Probl Cell Differ. 2024;73:87–129.
pubmed: 39242376
doi: 10.1007/978-3-031-62036-2_5
Dance A. Core Concept: cells nibble one another via the under-appreciated process of trogocytosis. Proc Natl Acad Sci U S A. 2019;116:17608–10.
pubmed: 31481628
pmcid: 6731757
doi: 10.1073/pnas.1912252116
Li KJ, Wu CH, Lu CH, Shen CY, Kuo YM, Tsai CY, et al. Trogocytosis between Non-immune cells for cell clearance, and among Immune-related cells for modulating Immune responses and autoimmunity. Int J Mol Sci. 2021;22(5).
Daubeuf S, Lindorfer MA, Taylor RP, Joly E, Hudrisier D. The direction of plasma membrane exchange between lymphocytes and accessory cells by trogocytosis is influenced by the nature of the accessory cell. J Immunol. 2010;184:1897–908.
pubmed: 20089699
doi: 10.4049/jimmunol.0901570
Zhao S, Zhang L, Xiang S, Hu Y, Wu Z, Shen J. Gnawing between cells and cells in the Immune System: friend or foe? A review of trogocytosis. Front Immunol. 2022;13:791006.
pubmed: 35185886
pmcid: 8850298
doi: 10.3389/fimmu.2022.791006
Caumartin J, Favier B, Daouya M, Guillard C, Moreau P, Carosella ED, LeMaoult J. Trogocytosis-based generation of suppressive NK cells. Embo j. 2007;26:1423–33.
pubmed: 17318190
pmcid: 1817622
doi: 10.1038/sj.emboj.7601570
Alegre E, Howangyin KY, Favier B, Baudhuin J, Lesport E, Daouya M, Gonzalez A, Carosella ED, Lemaoult J. Membrane redistributions through multi-intercellular exchanges and serial trogocytosis. Cell Res. 2010;20:1239–51.
pubmed: 20877312
doi: 10.1038/cr.2010.136
Miyake K, Karasuyama H. The role of trogocytosis in the modulation of Immune Cell functions. Cells. 2021;10(5).
Martinez-Martin N, Alarcon B. Physiological and therapeutic relevance of T cell receptor-mediated antigen trogocytosis. Biomed J. 2023;47(5):100630.
Campos-Mora M, Jacot W, Garcin G, Depondt ML, Constantinides M, Alexia C, Villalba M. NK cells in peripheral blood carry trogocytosed tumor antigens from solid cancer cells. Front Immunol. 2023;14:1199594.
pubmed: 37593736
pmcid: 10427869
doi: 10.3389/fimmu.2023.1199594
Singhal S, Rao AS, Stadanlick J, Bruns K, Sullivan NT, Bermudez A, Honig-Frand A, Krouse R, Arambepola S, Guo E, et al. Human Tumor-Associated macrophages and neutrophils regulate antitumor antibody efficacy through Lethal and Sublethal Trogocytosis. Cancer Res. 2024;84:1029–47.
pubmed: 38270915
pmcid: 10982649
doi: 10.1158/0008-5472.CAN-23-2135
Hamieh M, Dobrin A, Cabriolu A, van der Stegen SJC, Giavridis T, Mansilla-Soto J, Eyquem J, Zhao Z, Whitlock BM, Miele MM, et al. CAR T cell trogocytosis and cooperative killing regulate tumour antigen escape. Nature. 2019;568:112–6.
pubmed: 30918399
pmcid: 6707377
doi: 10.1038/s41586-019-1054-1
Li Y, Basar R, Wang G, Liu E, Moyes JS, Li L, Kerbauy LN, Uprety N, Fathi M, Rezvan A, et al. KIR-based inhibitory CARs overcome CAR-NK cell trogocytosis-mediated fratricide and tumor escape. Nat Med. 2022;28:2133–44.
pubmed: 36175679
pmcid: 9942695
doi: 10.1038/s41591-022-02003-x
Zhai Y, Du Y, Li G, Yu M, Hu H, Pan C, Wang D, Shi Z, Yan X, Li X, et al. Trogocytosis of CAR molecule regulates CAR-T cell dysfunction and tumor antigen escape. Signal Transduct Target Ther. 2023;8:457.
pubmed: 38143263
pmcid: 10749292
doi: 10.1038/s41392-023-01708-w
Schoutrop E, Renken S, Micallef Nilsson I, Hahn P, Poiret T, Kiessling R, Wickström SL, Mattsson J, Magalhaes I. Trogocytosis and fratricide killing impede MSLN-directed CAR T cell functionality. Oncoimmunology. 2022;11:2093426.
pubmed: 35898704
pmcid: 9313125
doi: 10.1080/2162402X.2022.2093426
Lei A, Yu H, Lu S, Lu H, Ding X, Tan T, Zhang H, Zhu M, Tian L, Wang X, et al. A second-generation M1-polarized CAR macrophage with antitumor efficacy. Nat Immunol. 2024;25:102–16.
pubmed: 38012418
doi: 10.1038/s41590-023-01687-8
Unver N. Sophisticated genetically engineered macrophages, CAR-Macs, in hitting the bull’s eye for solid cancer immunotherapy approaches. Clin Exp Med. 2023;23:3171–7.
pubmed: 37278931
doi: 10.1007/s10238-023-01106-0
Chen Y, Zhu X, Liu H, Wang C, Chen Y, Wang H, Fang Y, Wu X, Xu Y, Li C, et al. The application of HER2 and CD47 CAR-macrophage in ovarian cancer. J Transl Med. 2023;21:654.
pubmed: 37740183
pmcid: 10517545
doi: 10.1186/s12967-023-04479-8
Weinhard L, di Bartolomei G, Bolasco G, Machado P, Schieber NL, Neniskyte U, Exiga M, Vadisiute A, Raggioli A, Schertel A, et al. Microglia remodel synapses by presynaptic trogocytosis and spine head filopodia induction. Nat Commun. 2018;9:1228.
pubmed: 29581545
pmcid: 5964317
doi: 10.1038/s41467-018-03566-5
Morrissey MA, Williamson AP, Steinbach AM, Roberts EW, Kern N, Headley MB, et al. Chimeric antigen receptors that trigger phagocytosis. Elife. 2018;7.
Mishra AK, Rodriguez M, Torres AY, Smith M, Rodriguez A, Bond A, Morrissey MA, Montell DJ. Hyperactive rac stimulates cannibalism of living target cells and enhances CAR-M-mediated cancer cell killing. Proc Natl Acad Sci U S A. 2023;120:e2310221120.
pubmed: 38109551
pmcid: 10756302
doi: 10.1073/pnas.2310221120
Gao X, Carpenter RS, Boulais PE, Zhang D, Marlein CR, Li H, Smith M, Chung DJ, Maryanovich M, Will B, et al. Regulation of the hematopoietic stem cell pool by C-Kit-associated trogocytosis. Science. 2024;385:eadp2065.
pubmed: 39116219
doi: 10.1126/science.adp2065
Ma R, Woods M, Burkhardt P, Crooks N, van Leeuwen DG, Shmidt D, Couturier J, Chaumette A, Popat D, Hill LC, et al. Chimeric antigen receptor-induced antigen loss protects CD5.CART cells from fratricide without compromising on-target cytotoxicity. Cell Rep Med. 2024;5:101628.
pubmed: 38986621
pmcid: 11293353
doi: 10.1016/j.xcrm.2024.101628
Franzén AS, Boulifa A, Radecke C, Stintzing S, Raftery MJ, Pecher G. Next-generation CEA-CAR-NK-92 cells against solid tumors: overcoming Tumor Microenvironment challenges in Colorectal Cancer. Cancers (Basel). 2024;16(2).
Seigner J, Zajc CU, Dötsch S, Eigner C, Laurent E, Busch DH, Lehner M, Traxlmayr MW. Solving the mystery of the FMC63-CD19 affinity. Sci Rep. 2023;13:23024.
pubmed: 38155191
pmcid: 10754921
doi: 10.1038/s41598-023-48528-0
He C, Mansilla-Soto J, Khanra N, Hamieh M, Bustos V, Paquette AJ, Garcia Angus A, Shore DM, Rice WJ, Khelashvili G, et al. CD19 CAR antigen engagement mechanisms and affinity tuning. Sci Immunol. 2023;8:eadf1426.
pubmed: 36867678
pmcid: 10228544
doi: 10.1126/sciimmunol.adf1426
Harrer DC, Li SS, Kaljanac M, Barden M, Pan H, Abken H. Fine-tuning the antigen sensitivity of CAR T cells: emerging strategies and current challenges. Front Immunol. 2023;14:1321596.
pubmed: 38090558
pmcid: 10711209
doi: 10.3389/fimmu.2023.1321596
Ghorashian S, Kramer AM, Onuoha S, Wright G, Bartram J, Richardson R, Albon SJ, Casanovas-Company J, Castro F, Popova B, et al. Enhanced CAR T cell expansion and prolonged persistence in pediatric patients with ALL treated with a low-affinity CD19 CAR. Nat Med. 2019;25:1408–14.
pubmed: 31477906
doi: 10.1038/s41591-019-0549-5
Zhao J, Chen J, Li M, Chen M, Sun C. Multifaceted functions of CH25H and 25HC to modulate the lipid metabolism, Immune responses, and broadly antiviral activities. Viruses. 2020;12(7).
Lu Z, McBrearty N, Chen J, Tomar VS, Zhang H, De Rosa G, Tan A, Weljie AM, Beiting DP, Miao Z, et al. ATF3 and CH25H regulate effector trogocytosis and anti-tumor activities of endogenous and immunotherapeutic cytotoxic T lymphocytes. Cell Metab. 2022;34:1342–e13581347.
pubmed: 36070682
pmcid: 10496461
doi: 10.1016/j.cmet.2022.08.007
Schriek P, Villadangos JA. Trogocytosis and cross-dressing in antigen presentation. Curr Opin Immunol. 2023;83:102331.
pubmed: 37148582
doi: 10.1016/j.coi.2023.102331
Hasim MS, Marotel M, Hodgins JJ, Vulpis E, Makinson OJ, Asif S, Shih HY, Scheer AK, MacMillan O, Alonso FG, et al. When killers become thieves: trogocytosed PD-1 inhibits NK cells in cancer. Sci Adv. 2022;8:eabj3286.
pubmed: 35417234
pmcid: 9007500
doi: 10.1126/sciadv.abj3286
Lu T, Ma R, Li Z, Mansour AG, Teng KY, Chen L, Zhang J, Barr T, Caligiuri MA, Yu J. Hijacking TYRO3 from Tumor cells via trogocytosis enhances NK-cell effector functions and proliferation. Cancer Immunol Res. 2021;9:1229–41.
pubmed: 34326137
pmcid: 8562593
doi: 10.1158/2326-6066.CIR-20-1014
Ramezani F, Panahi Meymandi AR, Akbari B, Tamtaji OR, Mirzaei H, Brown CE, Mirzaei HR. Outsmarting trogocytosis to boost CAR NK/T cell therapy. Mol Cancer. 2023;22:183.
pubmed: 37974170
pmcid: 10652537
doi: 10.1186/s12943-023-01894-9
Hu H, Tang L, Zhao Y, Cheng J, Huang M, You Y, Zou P, Lei Q, Zhu X, Guo AY. Single-cell analysis of the survival mechanisms of fratricidal CAR-T targeting of T cell malignancies. Mol Ther Nucleic Acids. 2024;35:102225.
pubmed: 38948332
pmcid: 11214519
doi: 10.1016/j.omtn.2024.102225
Ruella M, Xu J, Barrett DM, Fraietta JA, Reich TJ, Ambrose DE, Klichinsky M, Shestova O, Patel PR, Kulikovskaya I, et al. Induction of resistance to chimeric antigen receptor T cell therapy by transduction of a single leukemic B cell. Nat Med. 2018;24:1499–503.
pubmed: 30275568
pmcid: 6511988
doi: 10.1038/s41591-018-0201-9
Labanieh L, Mackall CL. CAR immune cells: design principles, resistance and the next generation. Nature. 2023;614:635–48.
pubmed: 36813894
doi: 10.1038/s41586-023-05707-3
Vander Mause ER, Atanackovic D, Lim CS, Luetkens T. Roadmap to affinity-tuned antibodies for enhanced chimeric antigen receptor T cell function and selectivity. Trends Biotechnol. 2022;40:875–90.
pubmed: 35078657
doi: 10.1016/j.tibtech.2021.12.009
Abreu TR, Fonseca NA, Gonçalves N, Moreira JN. Current challenges and emerging opportunities of CAR-T cell therapies. J Control Release. 2020;319:246–61.
pubmed: 31899268
doi: 10.1016/j.jconrel.2019.12.047
Olson ML, Mause ERV, Radhakrishnan SV, Brody JD, Rapoport AP, Welm AL, Atanackovic D, Luetkens T. Low-affinity CAR T cells exhibit reduced trogocytosis, preventing rapid antigen loss, and increasing CAR T cell expansion. Leukemia. 2022;36:1943–6.
pubmed: 35490197
pmcid: 9252916
doi: 10.1038/s41375-022-01585-2
Pan J, Tang K, Luo Y, Seery S, Tan Y, Deng B, Liu F, Xu X, Ling Z, Song W, et al. Sequential CD19 and CD22 chimeric antigen receptor T-cell therapy for childhood refractory or relapsed B-cell acute lymphocytic leukaemia: a single-arm, phase 2 study. Lancet Oncol. 2023;24:1229–41.
pubmed: 37863088
doi: 10.1016/S1470-2045(23)00436-9
Wang T, Tang Y, Cai J, Wan X, Hu S, Lu X, Xie Z, Qiao X, Jiang H, Shao J, et al. Coadministration of CD19- and CD22-Directed chimeric Antigen receptor T-Cell therapy in Childhood B-Cell Acute Lymphoblastic Leukemia: a Single-Arm, Multicenter, Phase II Trial. J Clin Oncol. 2023;41:1670–83.
pubmed: 36346962
doi: 10.1200/JCO.22.01214
Liu S, Deng B, Yin Z, Lin Y, An L, Liu D, Pan J, Yu X, Chen B, Wu T, et al. Combination of CD19 and CD22 CAR-T cell therapy in relapsed B-cell acute lymphoblastic leukemia after allogeneic transplantation. Am J Hematol. 2021;96:671–9.
pubmed: 33725422
doi: 10.1002/ajh.26160
Kumar S. Natural killer cell cytotoxicity and its regulation by inhibitory receptors. Immunology. 2018;154:383–93.
pubmed: 29512837
pmcid: 6002213
doi: 10.1111/imm.12921
Liu D, Hu X, Chen Z, Wei W, Wu Y. Key links in the physiological regulation of the immune system and disease induction: T cell receptor -CD3 complex. Biochem Pharmacol. 2024;227:116441.
pubmed: 39029632
doi: 10.1016/j.bcp.2024.116441
Burr ML, Sparbier CE, Chan KL, Chan YC, Kersbergen A, Lam EYN, Azidis-Yates E, Vassiliadis D, Bell CC, Gilan O, et al. An evolutionarily conserved function of polycomb silences the MHC Class I Antigen Presentation Pathway and enables Immune Evasion in Cancer. Cancer Cell. 2019;36:385–e401388.
pubmed: 31564637
pmcid: 6876280
doi: 10.1016/j.ccell.2019.08.008
Zhao H, Zhao P, Huang C. Targeted inhibition of SUMOylation: treatment of tumors. Hum Cell. 2024;37:1347–54.
pubmed: 38856883
doi: 10.1007/s13577-024-01092-9
Zhou X, Cao H, Fang SY, Chow RD, Tang K, Majety M, Bai M, Dong MB, Renauer PA, Shang X, et al. CTLA-4 tail fusion enhances CAR-T antitumor immunity. Nat Immunol. 2023;24:1499–510.
pubmed: 37500885
pmcid: 11344484
doi: 10.1038/s41590-023-01571-5
Walker LS, Sansom DM. The emerging role of CTLA4 as a cell-extrinsic regulator of T cell responses. Nat Rev Immunol. 2011;11:852–63.
pubmed: 22116087
doi: 10.1038/nri3108
Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, Schmidt EM, Baker J, Jeffery LE, Kaur S, Briggs Z, et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science. 2011;332:600–3.
pubmed: 21474713
pmcid: 3198051
doi: 10.1126/science.1202947
Weber EW, Parker KR, Sotillo E, Lynn RC, Anbunathan H, Lattin J, et al. Transient rest restores functionality in exhausted CAR-T cells through epigenetic remodeling. Science. 2021;372.
Richman SA, Wang LC, Moon EK, Khire UR, Albelda SM, Milone MC. Ligand-Induced Degradation of a CAR permits reversible remote control of CAR T cell activity in Vitro and in vivo. Mol Ther. 2020;28:1600–13.
pubmed: 32559430
pmcid: 7335755
doi: 10.1016/j.ymthe.2020.06.004