Journal Article
. 2011 May; 71(13):4617-27.
doi: 10.1158/0008-5472.CAN-11-0422.

In vivo persistence, tumor localization, and antitumor activity of CAR-engineered T cells is enhanced by costimulatory signaling through CD137 (4-1BB)

De-Gang Song 1 Qunrui Ye  Carmine Carpenito  Mathilde Poussin  Li-Ping Wang  Chunyan Ji  Mariangela Figini  Carl H June  George Coukos  Daniel J Powell  
Affiliations
  • PMID: 21546571
  •     50 References
  •     127 citations

Abstract

Human T cells engineered to express a chimeric antigen receptor (CAR) specific for folate receptor-α (FRα) have shown robust antitumor activity against epithelial cancers in vitro but not in the clinic because of their inability to persist and home to tumor in vivo. In this study, CARs were constructed containing a FRα-specific scFv (MOv19) coupled to the T-cell receptor CD3ζ chain signaling module alone (MOv19-ζ) or in combination with the CD137 (4-1BB) costimulatory motif in tandem (MOv19-BBζ). Primary human T cells transduced to express conventional MOv19-ζ or costimulated MOv19-BBζ CARs secreted various proinflammatory cytokines, and exerted cytotoxic function when cocultured with FRα(+) tumor cells in vitro. However, only transfer of human T cells expressing the costimulated MOv19-BBζ CAR mediated tumor regression in immunodeficient mice bearing large, established FRα(+) human cancer. MOv19-BBζ CAR T-cell infusion mediated tumor regression in models of metastatic intraperitoneal, subcutaneous, and lung-involved human ovarian cancer. Importantly, tumor response was associated with the selective survival and tumor localization of human T cells in vivo and was only observed in mice receiving costimulated MOv19-BBζ CAR T cells. T-cell persistence and antitumor activity were primarily antigen-driven; however, antigen-independent CD137 signaling by CAR improved T-cell persistence but not antitumor activity in vivo. Our results show that anti-FRα CAR outfitted with CD137 costimulatory signaling in tandem overcome issues of T-cell persistence and tumor localization that limit the conventional FRα T-cell targeting strategy to provide potent antitumor activity in vivo.

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J Hematol Oncol, 2016 Jul 22; 9(1). PMID: 27439908    Free PMC article.
Enhancement of the in vivo persistence and antitumor efficacy of CD19 chimeric antigen receptor T cells through the delivery of modified TERT mRNA.
Yun Bai, Shifeng Kan, +5 authors, Hongkui Deng.
Cell Discov, 2015 Jan 01; 1. PMID: 27462436    Free PMC article.
Summary of emerging targets in anal cancer: the case for an immunotherapy based-approach.
Van Morris, Cathy Eng.
J Gastrointest Oncol, 2016 Oct 18; 7(5). PMID: 27747086    Free PMC article.
Review.
Preclinical Evaluation of Chimeric Antigen Receptors Targeting CD70-Expressing Cancers.
Qiong J Wang, Zhiya Yu, +4 authors, James C Yang.
Clin Cancer Res, 2016 Nov 03; 23(9). PMID: 27803044    Free PMC article.
Improving Chimeric Antigen Receptor-Modified T Cell Function by Reversing the Immunosuppressive Tumor Microenvironment of Pancreatic Cancer.
Somala Mohammed, Sujita Sukumaran, +7 authors, Juan F Vera.
Mol Ther, 2017 Jan 28; 25(1). PMID: 28129119    Free PMC article.
Highly Cited.
Chimeric antigen receptor T cells: a novel therapy for solid tumors.
Shengnan Yu, Anping Li, +4 authors, Kongming Wu.
J Hematol Oncol, 2017 Mar 31; 10(1). PMID: 28356156    Free PMC article.
Highly Cited. Review.
Emerging therapies for breast cancer.
Xichun Hu, Wei Huang, Minhao Fan.
J Hematol Oncol, 2017 Apr 30; 10(1). PMID: 28454587    Free PMC article.
Review.
FCγ Chimeric Receptor-Engineered T Cells: Methodology, Advantages, Limitations, and Clinical Relevance.
Sara Caratelli, Tommaso Sconocchia, +9 authors, Giuseppe Sconocchia.
Front Immunol, 2017 May 13; 8. PMID: 28496440    Free PMC article.
Review.
TNF-receptor superfamily agonists as molecular adjuvants for cancer vaccines.
Timothy Nj Bullock.
Curr Opin Immunol, 2017 Jul 28; 47. PMID: 28750279    Free PMC article.
Review.
Chimeric antigen receptors for adoptive T cell therapy in acute myeloid leukemia.
Mingxue Fan, Minghao Li, +5 authors, Lei Yu.
J Hematol Oncol, 2017 Aug 31; 10(1). PMID: 28851445    Free PMC article.
Highly Cited. Review.
CAR-T cell therapy in ovarian cancer: from the bench to the bedside.
Xinxin Zhu, Han Cai, +2 authors, Jinghe Lang.
Oncotarget, 2017 Oct 04; 8(38). PMID: 28969098    Free PMC article.
Review.
Supraphysiologic control over HIV-1 replication mediated by CD8 T cells expressing a re-engineered CD4-based chimeric antigen receptor.
Rachel S Leibman, Max W Richardson, +14 authors, James L Riley.
PLoS Pathog, 2017 Oct 13; 13(10). PMID: 29023549    Free PMC article.
Anti-GD2/4-1BB chimeric antigen receptor T cell therapy for the treatment of Chinese melanoma patients.
Jiayi Yu, Xiaowen Wu, +11 authors, Jun Guo.
J Hematol Oncol, 2018 Jan 05; 11(1). PMID: 29298689    Free PMC article.
Antitumor effects and persistence of a novel HER2 CAR T cells directed to gastric cancer in preclinical models.
Yali Han, Chuanyong Liu, +9 authors, Meili Sun.
Am J Cancer Res, 2018 Feb 09; 8(1). PMID: 29416924    Free PMC article.
Prospects of chimeric antigen receptor T cell therapy in ovarian cancer.
Vishal Jindal, Ena Arora, +3 authors, Rashmika Potdar.
Med Oncol, 2018 Apr 14; 35(5). PMID: 29651744
Review.
Nature of tumour rejection antigens in ovarian cancer.
Muzamil Y Want, Amit A Lugade, Sebastiano Battaglia, Kunle Odunsi.
Immunology, 2018 May 18; 155(2). PMID: 29772069    Free PMC article.
Review.
Choice of costimulatory domains and of cytokines determines CAR T-cell activity in neuroblastoma.
Concetta Quintarelli, Domenico Orlando, +14 authors, Ignazio Caruana.
Oncoimmunology, 2018 Jun 07; 7(6). PMID: 29872565    Free PMC article.
Development of third generation anti-EGFRvIII chimeric T cells and EGFRvIII-expressing artificial antigen presenting cells for adoptive cell therapy for glioma.
Ayguen Sahin, Carlos Sanchez, +3 authors, Bob S Carter.
PLoS One, 2018 Jul 06; 13(7). PMID: 29975720    Free PMC article.
Control of triple-negative breast cancer using ex vivo self-enriched, costimulated NKG2D CAR T cells.
Yali Han, Wei Xie, De-Gang Song, Daniel J Powell.
J Hematol Oncol, 2018 Jul 08; 11(1). PMID: 29980239    Free PMC article.
Human iPSC-Derived Natural Killer Cells Engineered with Chimeric Antigen Receptors Enhance Anti-tumor Activity.
Ye Li, David L Hermanson, Branden S Moriarity, Dan S Kaufman.
Cell Stem Cell, 2018 Aug 08; 23(2). PMID: 30082067    Free PMC article.
Highly Cited.
Early Investigations and Recent Advances in Intraperitoneal Immunotherapy for Peritoneal Metastasis.
Anusha Thadi, Marian Khalili, +3 authors, Wilbur B Bowne.
Vaccines (Basel), 2018 Aug 15; 6(3). PMID: 30103457    Free PMC article.
Review.
CAR T Cells in Solid Tumors: Blueprints for Building Effective Therapies.
Hannah M Knochelmann, Aubrey S Smith, +3 authors, Chrystal M Paulos.
Front Immunol, 2018 Aug 25; 9. PMID: 30140266    Free PMC article.
Highly Cited. Review.
Strategies to Address Chimeric Antigen Receptor Tonic Signaling.
Adam Ajina, John Maher.
Mol Cancer Ther, 2018 Sep 06; 17(9). PMID: 30181329    Free PMC article.
Review.
The efficacy and safety of anti-CD19/CD20 chimeric antigen receptor- T cells immunotherapy in relapsed or refractory B-cell malignancies:a meta-analysis.
Hui Zhou, Yuling Luo, +5 authors, Xuelei Ma.
BMC Cancer, 2018 Sep 28; 18(1). PMID: 30257649    Free PMC article.
Synthetic immunology: T-cell engineering and adoptive immunotherapy.
Wen Si, Cheng Li, Ping Wei.
Synth Syst Biotechnol, 2018 Oct 23; 3(3). PMID: 30345403    Free PMC article.
Review.
CD137 (4-1BB) Signalosome: Complexity Is a Matter of TRAFs.
Juan M Zapata, Gema Perez-Chacon, +4 authors, Ignacio Melero.
Front Immunol, 2018 Dec 14; 9. PMID: 30524423    Free PMC article.
Review.
DNAX-activating protein 10 co-stimulation enhances the anti-tumor efficacy of chimeric antigen receptor T cells.
Ruocong Zhao, Lin Cheng, +15 authors, Peng Li.
Oncoimmunology, 2018 Dec 14; 8(1). PMID: 30546945    Free PMC article.
Application Of Adoptive Immunotherapy In Ovarian Cancer.
Siyu Yang, Xiaojiao Yin, Ying Yue, Siqing Wang.
Onco Targets Ther, 2019 Oct 22; 12. PMID: 31632055    Free PMC article.
Genetically engineered T cells for cancer immunotherapy.
Dan Li, Xue Li, +8 authors, Wei Wang.
Signal Transduct Target Ther, 2019 Oct 23; 4. PMID: 31637014    Free PMC article.
Review.
Advances Of Chimeric Antigen Receptor T Cell Therapy In Ovarian Cancer.
Wenying Yan, Hongmei Hu, Biao Tang.
Onco Targets Ther, 2019 Nov 07; 12. PMID: 31686857    Free PMC article.
CD137 deficiency causes immune dysregulation with predisposition to lymphomagenesis.
Ido Somekh, Marini Thian, +33 authors, Kaan Boztug.
Blood, 2019 Sep 11; 134(18). PMID: 31501153    Free PMC article.
Folate receptor alpha expression associates with improved disease-free survival in triple negative breast cancer patients.
Nadine Norton, Bahaaeldin Youssef, +18 authors, Keith L Knutson.
NPJ Breast Cancer, 2020 Feb 13; 6. PMID: 32047850    Free PMC article.
Potential of Glioblastoma-Targeted Chimeric Antigen Receptor (CAR) T-Cell Therapy.
Ryan D Salinas, Joseph S Durgin, Donald M O'Rourke.
CNS Drugs, 2020 Jan 10; 34(2). PMID: 31916100
Review.
IL15 Enhances CAR-T Cell Antitumor Activity by Reducing mTORC1 Activity and Preserving Their Stem Cell Memory Phenotype.
Darya Alizadeh, Robyn A Wong, +11 authors, Christine E Brown.
Cancer Immunol Res, 2019 Mar 21; 7(5). PMID: 30890531    Free PMC article.
Highly Cited.
Mesothelin is a target of chimeric antigen receptor T cells for treating gastric cancer.
Jiang Lv, Ruocong Zhao, +24 authors, Peng Li.
J Hematol Oncol, 2019 Feb 20; 12(1). PMID: 30777106    Free PMC article.
Pilot Trial of Adoptive Transfer of Chimeric Antigen Receptor-transduced T Cells Targeting EGFRvIII in Patients With Glioblastoma.
Stephanie L Goff, Richard A Morgan, +14 authors, Steven A Rosenberg.
J Immunother, 2019 Mar 19; 42(4). PMID: 30882547    Free PMC article.
Highly Cited.
Limitations in the Design of Chimeric Antigen Receptors for Cancer Therapy.
Stefan Stoiber, Bruno L Cadilha, +3 authors, Sebastian Kobold.
Cells, 2019 May 22; 8(5). PMID: 31108883    Free PMC article.
Review.
Modified CAR T cells targeting membrane-proximal epitope of mesothelin enhances the antitumor function against large solid tumor.
Zhiwei Zhang, Duqing Jiang, +10 authors, Qijun Qian.
Cell Death Dis, 2019 Jun 19; 10(7). PMID: 31209210    Free PMC article.
CD137 Co-Stimulation Improves The Antitumor Effect Of LMP1-Specific Chimeric Antigen Receptor T Cells In Vitro And In Vivo.
Xiaojun Tang, Qi Tang, +4 authors, Zhenqing Feng.
Onco Targets Ther, 2019 Dec 07; 12. PMID: 31807014    Free PMC article.
From single gene analysis to single cell profiling: a new era for precision medicine.
Maria Teresa Di Martino, Stefania Meschini, +6 authors, Michele Caraglia.
J Exp Clin Cancer Res, 2020 Mar 07; 39(1). PMID: 32138788    Free PMC article.
Building a CAR Garage: Preparing for the Delivery of Commercial CAR T Cell Products at Memorial Sloan Kettering Cancer Center.
Karlo Perica, Kevin J Curran, Renier J Brentjens, Sergio A Giralt.
Biol Blood Marrow Transplant, 2018 Mar 03; 24(6). PMID: 29499327    Free PMC article.
Review.
Immunotherapy For Ovarian Cancer: Recent Advances And Combination Therapeutic Approaches.
Innocenza Palaia, Federica Tomao, +2 authors, Pierluigi Benedetti Panici.
Onco Targets Ther, 2020 Jul 04; 13. PMID: 32617007    Free PMC article.
Review.
CAR-T design: Elements and their synergistic function.
Jayapriya Jayaraman, Michael P Mellody, +5 authors, Weian Zhao.
EBioMedicine, 2020 Aug 03; 58. PMID: 32739874    Free PMC article.
Review.
Chemically Programmable and Switchable CAR-T Therapy.
Junpeng Qi, Kohei Tsuji, +4 authors, Haiyong Peng.
Angew Chem Int Ed Engl, 2020 Apr 25; 59(29). PMID: 32329959    Free PMC article.
The Future of Regulatory T Cell Therapy: Promises and Challenges of Implementing CAR Technology.
Yasmin R Mohseni, Sim L Tung, +3 authors, Giovanna Lombardi.
Front Immunol, 2020 Aug 15; 11. PMID: 32793236    Free PMC article.
Review.
Preclinical and Clinical Immunotherapeutic Strategies in Epithelial Ovarian Cancer.
Alejandra Martinez, Jean-Pierre Delord, Maha Ayyoub, Christel Devaud.
Cancers (Basel), 2020 Jul 08; 12(7). PMID: 32630708    Free PMC article.
Review.
FGG promotes migration and invasion in hepatocellular carcinoma cells through activating epithelial to mesenchymal transition.
Xiang Zhang, Fei Wang, +9 authors, Jingfeng Liu.
Cancer Manag Res, 2019 Mar 14; 11. PMID: 30863175    Free PMC article.
Selecting costimulatory domains for chimeric antigen receptors: functional and clinical considerations.
Robert Weinkove, Philip George, Nathaniel Dasyam, Alexander D McLellan.
Clin Transl Immunology, 2019 May 22; 8(5). PMID: 31110702    Free PMC article.
Highly Cited. Review.
Survival outcomes and efficacy of autologous CD19 chimeric antigen receptor-T cell therapy in the patient with diagnosed hematological malignancies: a systematic review and meta-analysis.
Emmanuel Kwateng Drokow, Hafiz Abdul Waqas Ahmed, +4 authors, Kai Sun.
Ther Clin Risk Manag, 2019 Jun 14; 15. PMID: 31190844    Free PMC article.
An Antibody Fab Fragment-based Chimeric Antigen Receptor Could Efficiently Eliminate Human Thyroid Cancer Cells.
Honghong Duan, Huibin Huang, Guangjun Jing.
J Cancer, 2019 Jun 18; 10(8). PMID: 31205546    Free PMC article.
Dawn of Chimeric Antigen Receptor T Cell Therapy in Non-Hodgkin Lymphoma.
Karlo Perica, Lia Palomba, Renier J Brentjens.
Adv Cell Gene Ther, 2018 Nov 01; 1(3). PMID: 33043278    Free PMC article.
Rictor promotes cell migration and actin polymerization through regulating ABLIM1 phosphorylation in Hepatocellular Carcinoma.
Xin Dong, Mei Feng, +8 authors, Ruirui Kong.
Int J Biol Sci, 2020 Oct 17; 16(15). PMID: 33061800    Free PMC article.
Adoptive cell transfer as personalized immunotherapy for human cancer.
Steven A Rosenberg, Nicholas P Restifo.
Science, 2015 Apr 04; 348(6230). PMID: 25838374    Free PMC article.
Highly Cited. Review.
A Novel Approach for the Treatment of T Cell Malignancies: Targeting T Cell Receptor Vβ Families.
Jie Wang, Katarzyna Urbanska, +5 authors, Daniel J Powell Jr.
Vaccines (Basel), 2020 Nov 05; 8(4). PMID: 33142718    Free PMC article.
GD2-specific chimeric antigen receptor-modified T cells targeting retinoblastoma - assessing tumor and T cell interaction.
Jatuporn Sujjitjoon, Elias Sayour, +6 authors, Lung-Ji Chang.
Transl Oncol, 2020 Dec 16; 14(2). PMID: 33321428    Free PMC article.
Driving Immune Responses in the Ovarian Tumor Microenvironment.
Franklin Ning, Christopher B Cole, Christina M Annunziata.
Front Oncol, 2021 Feb 02; 10. PMID: 33520713    Free PMC article.
Review.
4-1BB costimulation promotes CAR T cell survival through noncanonical NF-κB signaling.
Benjamin I Philipson, Roddy S O'Connor, +3 authors, Michael C Milone.
Sci Signal, 2020 Apr 03; 13(625). PMID: 32234960    Free PMC article.
Exploiting the folate receptor α in oncology.
Mariana Scaranti, Elena Cojocaru, Susana Banerjee, Udai Banerji.
Nat Rev Clin Oncol, 2020 Mar 11; 17(6). PMID: 32152484
Review.
Chimeric Antigen Receptor Design and Efficacy in Ovarian Cancer Treatment.
Katarzyna M Terlikowska, Bożena Dobrzycka, Sławomir J Terlikowski.
Int J Mol Sci, 2021 Apr 04; 22(7). PMID: 33800608    Free PMC article.
Review.
Cellular networks controlling T cell persistence in adoptive cell therapy.
Jack D Chan, Junyun Lai, +3 authors, Phillip K Darcy.
Nat Rev Immunol, 2021 Apr 22; 21(12). PMID: 33879873
Review.
Finding new lanes: Chimeric antigen receptor (CAR) T-cells for myeloid leukemia.
Suraj Pratap, Zhizhuang J Zhao.
Cancer Rep (Hoboken), 2020 Jul 17; 3(2). PMID: 32671999    Free PMC article.
Review.
Dual CD4-based CAR T cells with distinct costimulatory domains mitigate HIV pathogenesis in vivo.
Colby R Maldini, Daniel T Claiborne, +15 authors, Todd M Allen.
Nat Med, 2020 Sep 02; 26(11). PMID: 32868878
CAR-T cells: Early successes in blood cancer and challenges in solid tumors.
Hassan Dana, Ghanbar Mahmoodi Chalbatani, +5 authors, Thomas J Webster.
Acta Pharm Sin B, 2021 Jun 08; 11(5). PMID: 34094824    Free PMC article.
Review.
Mathematical Modelling Based on In Vivo Imaging Suggests CD137-Stimulated Cytotoxic T Lymphocytes Exert Superior Tumour Control Due to an Enhanced Antimitotic Effect on Tumour Cells.
Richard J Beck, Bettina Weigelin, Joost B Beltman.
Cancers (Basel), 2021 Jun 03; 13(11). PMID: 34073822    Free PMC article.
Making Potent CAR T Cells Using Genetic Engineering and Synergistic Agents.
Chi Hoon Park.
Cancers (Basel), 2021 Jul 03; 13(13). PMID: 34209505    Free PMC article.
Review.
Engineering enhanced CAR T-cells for improved cancer therapy.
Michael C Milone, Jie Xu, +4 authors, J Joseph Melenhorst.
Nat Cancer, 2021 Sep 07; 2(8). PMID: 34485921    Free PMC article.
Review.
Chimeric antigen receptor (CAR) immunotherapy: basic principles, current advances, and future prospects in neuro-oncology.
Hyeon Joo Yoo, Biyan Nathanael Harapan.
Immunol Res, 2021 Sep 24; 69(6). PMID: 34554405    Free PMC article.
Review.
NK Cell-Mediated Eradication of Ovarian Cancer Cells with a Novel Chimeric Antigen Receptor Directed against CD44.
Rüdiger Klapdor, Shuo Wang, +6 authors, Axel Schambach.
Biomedicines, 2021 Oct 24; 9(10). PMID: 34680456    Free PMC article.
Barriers to Immunotherapy in Ovarian Cancer: Metabolic, Genomic, and Immune Perturbations in the Tumour Microenvironment.
Racheal Louise Johnson, Michele Cummings, +3 authors, Nicolas Michel Orsi.
Cancers (Basel), 2021 Dec 25; 13(24). PMID: 34944851    Free PMC article.
Review.
Emerging CAR T Cell Strategies for the Treatment of AML.
Paresh Vishwasrao, Gongbo Li, +2 authors, Susanta K Hui.
Cancers (Basel), 2022 Mar 11; 14(5). PMID: 35267549    Free PMC article.
Review.
A novel PD-L1-targeted shark VNAR single-domain-based CAR-T cell strategy for treating breast cancer and liver cancer.
Dan Li, Hejiao English, +4 authors, Mitchell Ho.
Mol Ther Oncolytics, 2022 Mar 24; 24. PMID: 35317524    Free PMC article.
Visualizing CAR-T cell Immunotherapy Using 3 Tesla Fluorine-19 MRI.
Veronica P Dubois, Olivia C Sehl, Paula J Foster, John A Ronald.
Mol Imaging Biol, 2021 Nov 18; 24(2). PMID: 34786668    Free PMC article.
Emerging Strategies in TCR-Engineered T Cells.
Fang Wei, Xiao-Xia Cheng, John Zhao Xue, Shao-An Xue.
Front Immunol, 2022 Apr 19; 13. PMID: 35432319    Free PMC article.
Review.