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The most advanced application is the use of CD19 chimeric antigen receptor (CAR)\u00adT (CAR-T) cells to B cell malignancies, but there are still side effects including potential carcinogenicity of lentiviral or retroviral insertion into the host cell genome. Here, we developed a nonviral aptamer-T cell targeted strategy for tumor therapy. Tumor cells surface-specific ssDNA aptamers were conjugated to CD3+T cells (aptamer-T cells) using N-azidomannosamine (ManNAz) sugar metabolic cell labeling and click chemistry. We found that the aptamer-T cells could specifically target and bind to tumor cells (such as SGC-7901 gastric cancer cell and CT26 colon carcinoma cell) in vitro and in mice after adoptively transfer in. Aptamer-T cells led to significant regression in tumor volume due to being enriched at tumor microenvironment and producing strong cytotoxicity activities of CD3+T cells with enhanced perforin, granzyme B, CD107a, CD69, and FasL expression. Moreover, aptamer-T displayed even stronger antitumor effects than an anti-PD1 immune-checkpoint monoclonal antibody (mAb) treatment in mice and combination with anti-PD1 yielded synergic antitumor effects. This study uncovers the strong potential of the adoptive nonviral aptamer-T cell strategy as a feasible and efficacious approach for tumor-targeted immunotherapy application.<\/jats:p>","DOI":"10.1021\/acschembio.0c00164","type":"journal-article","created":{"date-parts":[[2020,5,13]],"date-time":"2020-05-13T18:15:01Z","timestamp":1589393701000},"page":"1554-1565","source":"Crossref","is-referenced-by-count":54,"title":["Aptamer\u2011T Cell Targeted Therapy for Tumor Treatment\nUsing Sugar Metabolism and Click Chemistry"],"prefix":"10.1021","volume":"15","author":[{"given":"Chuan-Gang","family":"Liu","sequence":"first","affiliation":[{"name":"Wuhan University School of Medicine , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yong","family":"Wang","sequence":"additional","affiliation":[{"name":"Wuhan University School of Medicine , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peng","family":"Liu","sequence":"additional","affiliation":[{"name":"Wuhan University School of Medicine , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qi-Li","family":"Yao","sequence":"additional","affiliation":[{"name":"Wuhan University School of Medicine , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuan-Yuan","family":"Zhou","sequence":"additional","affiliation":[{"name":"Wuhan University School of Medicine , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chao-Fan","family":"Li","sequence":"additional","affiliation":[{"name":"Wuhan University School of Medicine , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qiu","family":"Zhao","sequence":"additional","affiliation":[{"name":"Wuhan University , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guang-Hui","family":"Liu","sequence":"additional","affiliation":[{"name":"Allergy Department of Zhongnan Hospital Wuhan University , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8283-9381","authenticated-orcid":true,"given":"Xiao-Lian","family":"Zhang","sequence":"additional","affiliation":[{"name":"Wuhan University School of Medicine , , ,","place":["Wuhan, China, 430071"]},{"name":"Allergy Department of Zhongnan Hospital Wuhan University , , ,","place":["Wuhan, China, 430071"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2020,5,13]]},"reference":[{"key":"2026081714174862300_cit1","doi-asserted-by":"publisher","first-page":"1112","DOI":"10.1200\/JCO.2015.64.5929","article-title":"Allogeneic T Cells That Express an\nAnti-CD19 Chimeric Antigen Receptor Induce Remissions of B-Cell Malignancies\nThat Progress After Allogeneic Hematopoietic Stem-Cell Transplantation\nWithout Causing Graft-Versus-Host Disease","volume":"34","author":"Brudno","year":"2016","journal-title":"J.\nClin. Oncol."},{"key":"2026081714174862300_cit2","first-page":"403","article-title":"CD19 chimeric\nantigen receptor (CD19 CAR)-redirected\nadoptive T-cell immunotherapy for the treatment of relapsed or refractory\nB-cell Non-Hodgkin\u2019s Lymphomas","volume":"6","author":"Onea","year":"2016","journal-title":"Am. J.\nCancer Res."},{"key":"2026081714174862300_cit3","doi-asserted-by":"publisher","first-page":"2545","DOI":"10.1056\/NEJMoa1708566","article-title":"Chimeric\nAntigen Receptor T Cells in Refractory B-Cell Lymphomas","volume":"377","author":"Schuster","year":"2017","journal-title":"N. Engl. J. Med."},{"key":"2026081714174862300_cit4","doi-asserted-by":"publisher","first-page":"370","DOI":"10.1038\/nrclinonc.2016.36","article-title":"Driving CAR T-cells forward","volume":"13","author":"Jackson","year":"2016","journal-title":"Nat. Rev. Clin. Oncol."},{"key":"2026081714174862300_cit5","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1038\/nrclinonc.2016.25","article-title":"The future of cancer\ntreatment: immunomodulation, CARs and combination immunotherapy","volume":"13","author":"Khalil","year":"2016","journal-title":"Nat. Rev. Clin. Oncol."},{"key":"2026081714174862300_cit6","doi-asserted-by":"publisher","first-page":"56","DOI":"10.1186\/s40425-018-0343-9","article-title":"Cytokine\nrelease syndrome","volume":"6","author":"Shimabukuro-Vornhagen","year":"2018","journal-title":"J. Immunother Cancer"},{"key":"2026081714174862300_cit7","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1007\/s13238-017-0411-9","article-title":"Increasing the safety\nand efficacy of chimeric antigen receptor T\ncell therapy","volume":"8","author":"Li","year":"2017","journal-title":"Protein Cell"},{"key":"2026081714174862300_cit8","doi-asserted-by":"publisher","first-page":"459","DOI":"10.2174\/156652309790031120","article-title":"State-of-the-art\nlentiviral vectors for research use: risk assessment and biosafety\nrecommendations","volume":"9","author":"Pauwels","year":"2009","journal-title":"Curr. Gene Ther."},{"key":"2026081714174862300_cit9","doi-asserted-by":"publisher","first-page":"41","DOI":"10.1016\/j.addr.2019.04.006","article-title":"CAR T-cell bioengineering: Single\nvariable domain of heavy chain antibody targeted CARs","volume":"141","author":"Rahbarizadeh","year":"2019","journal-title":"Adv. Drug Delivery Rev."},{"key":"2026081714174862300_cit10","doi-asserted-by":"publisher","first-page":"E2511","DOI":"10.3390\/ijms20102511","article-title":"Updates on Aptamer\nResearch","volume":"20","author":"Ali","year":"2019","journal-title":"Int. J. Mol. Sci."},{"key":"2026081714174862300_cit11","doi-asserted-by":"publisher","first-page":"E80","DOI":"10.3390\/cancers10030080","article-title":"Aptamer Therapeutics\nin Cancer: Current and Future","volume":"10","author":"Morita","year":"2018","journal-title":"Cancers"},{"key":"2026081714174862300_cit12","doi-asserted-by":"publisher","first-page":"11836","DOI":"10.1002\/anie.201206703","article-title":"Bioorthogonal copper-free\nclick chemistry in vivo for tumor-targeted delivery of nanoparticles","volume":"51","author":"Koo","year":"2012","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026081714174862300_cit13","doi-asserted-by":"publisher","first-page":"742","DOI":"10.1021\/ar200067r","article-title":"Introducing bioorthogonal\nfunctionalities into proteins in living cells","volume":"44","author":"Hao","year":"2011","journal-title":"Acc. Chem. Res."},{"key":"2026081714174862300_cit14","doi-asserted-by":"publisher","first-page":"1765","DOI":"10.1002\/anie.201407976","article-title":"Tracking surface\nglycans on live cancer cells with single-molecule sensitivity","volume":"54","author":"Jiang","year":"2015","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026081714174862300_cit15","doi-asserted-by":"publisher","first-page":"17468","DOI":"10.1021\/ja508484c","article-title":"Glycan imaging in intact rat hearts and glycoproteomic analysis reveal\nthe upregulation of sialylation during cardiac hypertrophy","volume":"136","author":"Rong","year":"2014","journal-title":"J. Am. Chem. Soc."},{"key":"2026081714174862300_cit16","doi-asserted-by":"publisher","first-page":"11473","DOI":"10.1021\/jacs.6b07132","article-title":"Two-Step\nChemoenzymatic Detection of N-Acetylneuraminic Acid-alpha(2\u20133)-Galactose\nGlycans","volume":"138","author":"Wen","year":"2016","journal-title":"J. Am. Chem. Soc."},{"key":"2026081714174862300_cit17","doi-asserted-by":"publisher","first-page":"6457","DOI":"10.1002\/anie.201601744","article-title":"Bioorthogonal Turn-On\nProbe Based on Aggregation-Induced Emission Characteristics for Cancer\nCell Imaging and Ablation","volume":"55","author":"Yuan","year":"2016","journal-title":"Angew. Chem., Int.\nEd."},{"key":"2026081714174862300_cit18","doi-asserted-by":"publisher","first-page":"30","DOI":"10.1016\/j.talanta.2014.09.036","article-title":"Diagnostic applications\nof gastric carcinoma cell aptamers in vitro and in vivo","volume":"134","author":"Ding","year":"2015","journal-title":"Talanta"},{"key":"2026081714174862300_cit19","doi-asserted-by":"publisher","DOI":"10.1038\/mtna.2016.102","article-title":"A Novel\nPD-L1-targeting Antagonistic DNA Aptamer With Antitumor Effects","volume":"5","author":"Lai","year":"2016","journal-title":"Mol. Ther.--Nucleic Acids"},{"key":"2026081714174862300_cit20","doi-asserted-by":"publisher","first-page":"11680","DOI":"10.1021\/jacs.6b05357","article-title":"A Single ssDNA Aptamer Binding to\nMannose-Capped Lipoarabinomannan of Bacillus Calmette-Guerin Enhances\nImmunoprotective Effect against Tuberculosis","volume":"138","author":"Sun","year":"2016","journal-title":"J. Am. Chem. Soc."},{"key":"2026081714174862300_cit21","doi-asserted-by":"publisher","first-page":"1143","DOI":"10.1111\/j.1600-0854.2006.00464.x","article-title":"T-cell antigen receptor-induced signaling\ncomplexes: internalization via a cholesterol-dependent endocytic pathway","volume":"7","author":"Barr","year":"2006","journal-title":"Traffic"},{"key":"2026081714174862300_cit22","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1002\/cbic.201500344","article-title":"Metabolic Remodeling of Cell-Surface\nSialic Acids: Principles, Applications, and Recent Advances","volume":"17","author":"Cheng","year":"2016","journal-title":"ChemBioChem"},{"key":"2026081714174862300_cit23","doi-asserted-by":"publisher","first-page":"4065","DOI":"10.1038\/s41467-019-11942-y","article-title":"Next-generation unnatural monosaccharides\nreveal that ESRRB O-GlcNAcylation regulates pluripotency of mouse\nembryonic stem cells","volume":"10","author":"Hao","year":"2019","journal-title":"Nat. Commun."},{"key":"2026081714174862300_cit24","doi-asserted-by":"publisher","first-page":"1817","DOI":"10.1002\/anie.201711710","article-title":"Artificial Cysteine\nS-Glycosylation Induced by Per-O-Acetylated Unnatural Monosaccharides\nduring Metabolic Glycan Labeling","volume":"57","author":"Qin","year":"2018","journal-title":"Angew. Chem.,\nInt. Ed."},{"key":"2026081714174862300_cit25","doi-asserted-by":"publisher","DOI":"10.4161\/2162402X.2014.994446","article-title":"IL-12 secreting\ntumor-targeted chimeric antigen receptor T cells eradicate ovarian\ntumors in vivo","volume":"4","author":"Koneru","year":"2015","journal-title":"Oncoimmunology"},{"key":"2026081714174862300_cit26","doi-asserted-by":"publisher","first-page":"847","DOI":"10.1038\/nbt.4195","article-title":"Targeted\ndelivery of a PD-1-blocking scFv by CAR-T cells enhances anti-tumor\nefficacy in vivo","volume":"36","author":"Rafiq","year":"2018","journal-title":"Nat. Biotechnol."},{"key":"2026081714174862300_cit27","doi-asserted-by":"publisher","first-page":"3130","DOI":"10.1172\/JCI83092","article-title":"Human CAR\nT cells with cell-intrinsic PD-1 checkpoint blockade resist tumor-mediated\ninhibition","volume":"126","author":"Cherkassky","year":"2016","journal-title":"J. Clin. Invest."},{"key":"2026081714174862300_cit28","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1016\/j.omtn.2019.04.016","article-title":"Targeting Lymph Node\nSinus Macrophages to Inhibit Lymph Node Metastasis","volume":"16","author":"Hu","year":"2019","journal-title":"Mol. Ther.--Nucleic Acids"},{"key":"2026081714174862300_cit29","doi-asserted-by":"publisher","first-page":"14327","DOI":"10.1002\/anie.201907410","article-title":"Direct Visualization\nof Live Zebrafish Glycans via Single-Step Metabolic\nLabeling with Fluorophore-Tagged Nucleotide Sugars","volume":"58","author":"Hong","year":"2019","journal-title":"Angew. Chem., Int. Ed."},{"key":"2026081714174862300_cit30","doi-asserted-by":"publisher","first-page":"16589","DOI":"10.1021\/jacs.8b08442","article-title":"Amplified Visualization of Protein-Specific Glycosylation\nin Zebrafish via Proximity-Induced Hybridization Chain Reaction","volume":"140","author":"Li","year":"2018","journal-title":"J. Am. Chem. Soc."},{"key":"2026081714174862300_cit31","doi-asserted-by":"publisher","first-page":"3482","DOI":"10.1039\/C5CC10625G","article-title":"Bioorthogonal chemistry for selective recognition, separation and\nkilling bacteria over mammalian cells","volume":"52","author":"Li","year":"2016","journal-title":"Chem.\nCommun. (Cambridge, U. K.)"},{"key":"2026081714174862300_cit32","doi-asserted-by":"publisher","first-page":"2946730","DOI":"10.1155\/2018\/2946730","article-title":"Applications of Click Chemistry in\nthe Development of HIV Protease Inhibitors","volume":"2018","author":"Mudgal","year":"2018","journal-title":"Int. J. Med. Chem."},{"key":"2026081714174862300_cit33","doi-asserted-by":"publisher","first-page":"E481","DOI":"10.3390\/molecules24030481","article-title":"A Spotlight on Viruses-Application\nof Click Chemistry to Visualize Virus-Cell Interactions","volume":"24","author":"Muller","year":"2019","journal-title":"Molecules"},{"key":"2026081714174862300_cit34","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1016\/j.virusres.2018.08.003","article-title":"Recent trends in click chemistry\nas a promising technology for virus-related research","volume":"256","author":"Ouyang","year":"2018","journal-title":"Virus Res."},{"key":"2026081714174862300_cit35","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1021\/acscentsci.9b00956","article-title":"Glycoengineering of\nNatural Killer Cells with CD22 Ligands for Enhanced Anticancer Immunotherapy","volume":"6","author":"Wang","year":"2020","journal-title":"ACS Cent. Sci."},{"key":"2026081714174862300_cit36","doi-asserted-by":"publisher","first-page":"918","DOI":"10.1002\/ijc.29826","article-title":"An aptamer targeting\nshared tumor-specific\npeptide antigen of MAGE-A3 in multiple cancers","volume":"138","author":"Wang","year":"2016","journal-title":"Int. J. Cancer"},{"key":"2026081714174862300_cit37","doi-asserted-by":"publisher","first-page":"5779","DOI":"10.1007\/s00216-019-01958-0","article-title":"A label-free fluorescence method\nbased on terminal deoxynucleotidyl transferase and thioflavin T for\ndetecting prostate-specific antigen","volume":"411","author":"Chen","year":"2019","journal-title":"Anal. Bioanal.\nChem."},{"key":"2026081714174862300_cit38","doi-asserted-by":"publisher","first-page":"111484","DOI":"10.1016\/j.bios.2019.111484","article-title":"Application of various optical and electrochemical\naptasensors for detection of human prostate specific antigen: A review","volume":"142","author":"Ghorbani","year":"2019","journal-title":"Biosens. Bioelectron."},{"key":"2026081714174862300_cit39","doi-asserted-by":"publisher","first-page":"8471","DOI":"10.1021\/acsomega.8b00990","article-title":"Top-Down Fabricated\nSilicon Nanowire Arrays for Field-Effect Detection of Prostate-Specific\nAntigen","volume":"3","author":"Rani","year":"2018","journal-title":"ACS Omega"},{"key":"2026081714174862300_cit40","doi-asserted-by":"publisher","first-page":"21","DOI":"10.29252\/ibj.23.1.21","article-title":"Anti-Mucin1 Aptamer-Conjugated Chitosan\nNanoparticles for Targeted Co-Delivery of Docetaxel and IGF-1R siRNA\nto SKBR3Metastatic Breast Cancer Cells","volume":"23","author":"Jafari","year":"2019","journal-title":"Iran.\nBiomed. J."},{"key":"2026081714174862300_cit41","doi-asserted-by":"publisher","first-page":"E478","DOI":"10.3390\/molecules24030478","article-title":"Novel Bispecific\nAptamer Enhances Immune Cytotoxicity Against MUC1-Positive Tumor Cells\nby MUC1-CD16 Dual Targeting","volume":"24","author":"Li","year":"2019","journal-title":"Molecules"},{"key":"2026081714174862300_cit42","doi-asserted-by":"publisher","first-page":"4066","DOI":"10.7150\/thno.33383","article-title":"Enhanced cytotoxic\nT lymphocytes recruitment targeting tumor vasculatures by endoglin\naptamer and IP-10 plasmid presenting liposome-based nanocarriers","volume":"9","author":"Yang","year":"2019","journal-title":"Theranostics"},{"key":"2026081714174862300_cit43","doi-asserted-by":"publisher","DOI":"10.1038\/mtna.2015.11","article-title":"Targeting the PD-1\/PD-L1 Immune Evasion Axis With DNA\nAptamers as a Novel Therapeutic Strategy for the Treatment of Disseminated\nCancers","volume":"4","author":"Prodeus","year":"2015","journal-title":"Mol. Ther.--Nucleic Acids"},{"key":"2026081714174862300_cit44","doi-asserted-by":"publisher","first-page":"2977","DOI":"10.1172\/JCI73174","article-title":"CTLA4 aptamer delivers\nSTAT3 siRNA to tumor-associated and malignant T cells","volume":"124","author":"Herrmann","year":"2014","journal-title":"J. Clin. Invest."},{"key":"2026081714174862300_cit45","doi-asserted-by":"publisher","first-page":"417","DOI":"10.1038\/nature19330","article-title":"Defining CD8+ T cells\nthat provide the proliferative burst after PD-1 therapy","volume":"537","author":"Im","year":"2016","journal-title":"Nature"},{"key":"2026081714174862300_cit46","doi-asserted-by":"publisher","first-page":"11959","DOI":"10.3390\/molecules200711959","article-title":"A Highlight of Recent Advances in Aptamer Technology and Its Application","volume":"20","author":"Sun","year":"2015","journal-title":"Molecules"},{"key":"2026081714174862300_cit47","doi-asserted-by":"publisher","first-page":"3359","DOI":"10.3748\/wjg.v25.i26.3359","article-title":"Screening\nof aptamers\nand their potential application in targeted diagnosis and therapy\nof liver cancer","volume":"25","author":"Zhang","year":"2019","journal-title":"World J. Gastroenterol"},{"key":"2026081714174862300_cit48","doi-asserted-by":"publisher","first-page":"1462","DOI":"10.3389\/fmicb.2019.01462","article-title":"Application of Aptamers\nin Virus Detection and Antiviral Therapy","volume":"10","author":"Zou","year":"2019","journal-title":"Front.\nMicrobiol."},{"key":"2026081714174862300_cit49","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1016\/j.smim.2017.07.011","article-title":"Natural killer cells\nunleashed: Checkpoint receptor blockade and BiKE\/TriKE utilization\nin NK-mediated anti-tumor immunotherapy","volume":"31","author":"Davis","year":"2017","journal-title":"Semin.\nImmunol."},{"key":"2026081714174862300_cit50","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1111\/imm.12976","article-title":"Macrophage targeting: opening new possibilities for\ncancer immunotherapy","volume":"155","author":"Cassetta","year":"2018","journal-title":"Immunology"}],"container-title":["ACS Chemical Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pubs.acs.org\/doi\/pdf\/10.1021\/acschembio.0c00164","content-type":"application\/pdf","content-version":"vor","intended-application":"unspecified"},{"URL":"https:\/\/pubs.acs.org\/acbcct\/article-pdf\/15\/6\/1554\/5890476\/cb0c00164.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/pubs.acs.org\/acbcct\/article-pdf\/15\/6\/1554\/5890476\/cb0c00164.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,8,17]],"date-time":"2026-08-17T18:23:50Z","timestamp":1786991030000},"score":1,"resource":{"primary":{"URL":"https:\/\/pubs.acs.org\/acbcct\/article\/15\/6\/1554\/588786\/Aptamer-T-Cell-Targeted-Therapy-for-Tumor"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,13]]},"references-count":50,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,5,13]]},"published-print":{"date-parts":[[2020,6,19]]}},"URL":"https:\/\/doi.org\/10.1021\/acschembio.0c00164","relation":{},"ISSN":["1554-8929","1554-8937"],"issn-type":[{"value":"1554-8929","type":"print"},{"value":"1554-8937","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,5,13]]}}}