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Conventional direct bactericidal strategies often inflict collateral damage on host cells and fail to counteract this effector-mediated immune evasion, ultimately leading to treatment failure and infection relapse. Here, we developed a targeted and enzyme-activated peptide self-assembling nanofiber system (TESAN) to address these challenges. We used orthogonal design to screen functional modules, balancing safety with efficacy to identify an optimal formulation. TESAN maintains charge masking during delivery to minimize host toxicity. Upon targeting bacteria within the cytoplasm, bacteria-secreted enzymes selectively activate the peptides, simultaneously releasing antimicrobial moiety for bacterial killing and inducing self-assembly into a dense nanofiber network on the bacterial surface. The assembled nanofibers restrict secretion of immunosuppressive effector proteins, which reverses local immune suppression and restores macrophage clearance function. TESAN eliminated 99.98% of intracellular persisters without compromising host cell viability. In a murine pulmonary infection model, TESAN achieved a 4.64\u202flog10 reduction in bacterial burden and increased seven-day survival from 10% to 70%. Studies using alveolar macrophages from patient bronchoalveolar lavage fluid confirmed intracellular targeting and achieved up to 99.91% bacterial elimination. These results establish enzyme-responsive in situ self-assembly as an effective strategy for treating persistent intracellular infections.<\/jats:p>","DOI":"10.1021\/jacs.6c08625","type":"journal-article","created":{"date-parts":[[2026,8,4]],"date-time":"2026-08-04T14:32:48Z","timestamp":1785853968000},"page":"33496-33507","source":"Crossref","is-referenced-by-count":0,"title":["Targeted\nand Enzyme-Activated Self-Assembling Peptide\nNanofibers for Intracellular Bacterial Clearance and Immune Restoration"],"prefix":"10.1021","volume":"148","author":[{"given":"Jieling","family":"Chen","sequence":"first","affiliation":[{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]},{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lixue","family":"Feng","sequence":"additional","affiliation":[{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]},{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yao","family":"Xiao","sequence":"additional","affiliation":[{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]},{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2139-4750","authenticated-orcid":true,"given":"Yanbin","family":"Cai","sequence":"additional","affiliation":[{"name":"Zhujiang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510282"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2576-8780","authenticated-orcid":true,"given":"Lei","family":"Zheng","sequence":"additional","affiliation":[{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]},{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]},{"name":"Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7190-5307","authenticated-orcid":true,"given":"Jie","family":"Zhan","sequence":"additional","affiliation":[{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]},{"name":"Nanfang Hospital, Southern Medical University , , ,","place":["Guangzhou, P. R. China, 510515"]},{"name":"Southern Medical University , , ,","place":["Guangzhou, P. 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Adv."},{"issue":"4","key":"2026081210094538900_cit32","doi-asserted-by":"publisher","DOI":"10.1002\/INMD.20240125","article-title":"Harnessing the therapeutic\npotential of bacterial extracellular vesicles via functional peptides","volume":"3","author":"Shi","year":"2025","journal-title":"Interdiscip. Med."},{"issue":"1","key":"2026081210094538900_cit33","doi-asserted-by":"publisher","DOI":"10.1002\/inmd.20240053","article-title":"NIR-II emissive biohybrid nanovesicles\nas mild-temperature photothermal antibiofilm agents against acute\nbacterial skin and skin-structure infections","volume":"3","author":"Wang","year":"2024","journal-title":"Interdiscip. Med."},{"issue":"8","key":"2026081210094538900_cit34","doi-asserted-by":"publisher","first-page":"1295","DOI":"10.1038\/s41563-025-02164-3","article-title":"De novo design of self-assembling\npeptides with antimicrobial activity guided by deep learning","volume":"24","author":"Liu","year":"2025","journal-title":"Nat. Mater."},{"issue":"11","key":"2026081210094538900_cit35","doi-asserted-by":"publisher","first-page":"9122","DOI":"10.1021\/acsnano.5c17134","article-title":"Engineered Peptide\nCoassembly Enables Precision Delivery of As(III)-Peptide Complexes\nand Counteracts Inflammation-Dependent Therapeutic Resistance in High-Risk\nNeuroblastoma","volume":"20","author":"Zeng","year":"2026","journal-title":"ACS Nano"},{"issue":"7","key":"2026081210094538900_cit36","doi-asserted-by":"publisher","DOI":"10.1002\/adma.202516767","article-title":"Tumor-Targeting\nCo-Delivery of T-Cell Antigen and Camptothecin Guided\nby Cascade-Responsive Peptide Self-Assembly to Reshape Tumor Antigenicity\nfor Cancer Immunotherapy","volume":"38","author":"Ding","year":"2026","journal-title":"Adv. Mater."},{"issue":"29","key":"2026081210094538900_cit37","doi-asserted-by":"publisher","DOI":"10.1002\/adma.202210766","article-title":"pH-Triggered\nSize-Transformable and Bioactivity-Switchable Self-Assembling\nChimeric Peptide Nanoassemblies for Combating Drug-Resistant Bacteria\nand Biofilms","volume":"35","author":"Tan","year":"2023","journal-title":"Adv. Mater."},{"issue":"2","key":"2026081210094538900_cit38","doi-asserted-by":"publisher","first-page":"2148","DOI":"10.1021\/jacs.5c09790","article-title":"A Tumor-Selective\nSelf-Assembling\nNetwork of Poly(amino acid) Induces Cascading Bystander Cytotoxicity\nthrough Microvesicle Fission Amplification","volume":"148","author":"Sun","year":"2026","journal-title":"J. Am. Chem. 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Ed."},{"issue":"42","key":"2026081210094538900_cit42","doi-asserted-by":"publisher","DOI":"10.1002\/smll.202504647","article-title":"Dual-Targeting Peptide Assembly Probe\nfor Precise Detection of Biomarkers of Circulating Tumor Cells in\nHepatocellular Carcinoma","volume":"21","author":"Wang","year":"2025","journal-title":"Small"},{"issue":"28","key":"2026081210094538900_cit43","doi-asserted-by":"publisher","first-page":"18160","DOI":"10.1021\/acsnano.3c09642","article-title":"Microarray Chip-Based\nHigh-Throughput Screening of Neurofilament\nLight Chain Self-Assembling Peptide for Noninvasive Monitoring of\nAlzheimer\u2019s Disease","volume":"18","author":"Zhou","year":"2024","journal-title":"ACS Nano"},{"issue":"6","key":"2026081210094538900_cit44","doi-asserted-by":"publisher","DOI":"10.1002\/anie.202517035","article-title":"Apoptosis-Amplified Intracellular\nPaclitaxel Nanoparticle Formation Enhances Microtubule Aggregation\nand PANoptosis","volume":"65","author":"Liu","year":"2026","journal-title":"Angew. Chem., Int. Ed."},{"issue":"7","key":"2026081210094538900_cit45","doi-asserted-by":"publisher","DOI":"10.1002\/anie.202521145","article-title":"Ruthenium-Based Sonoafterglow\nProbes for Tumor-Specific Theranostics","volume":"65","author":"Wang","year":"2026","journal-title":"Angew.\nChem., Int. Ed."},{"issue":"42","key":"2026081210094538900_cit46","doi-asserted-by":"publisher","first-page":"28669","DOI":"10.1021\/jacs.4c03420","article-title":"Homologous Peptide Foldamer Promotes FUS Aggregation\nand Triggers Cancer Cell Death","volume":"146","author":"Wang","year":"2024","journal-title":"J. Am. Chem.\nSoc."},{"issue":"21","key":"2026081210094538900_cit47","doi-asserted-by":"publisher","DOI":"10.1002\/smll.202307390","article-title":"Supramolecular\nPeptide Amphiphile Nanospheres Reprogram Tumor-associated Macrophage\nto Reshape the Immune Microenvironment for Enhanced Breast Cancer\nImmunotherapy","volume":"20","author":"Xiao","year":"2023","journal-title":"Small"},{"key":"2026081210094538900_cit48","doi-asserted-by":"publisher","first-page":"391","DOI":"10.1016\/j.jcis.2020.10.103","article-title":"pH-dependent\nreversibly activatable cell-penetrating peptides improve the antitumor\neffect of artemisinin-loaded liposomes","volume":"586","author":"Yu","year":"2021","journal-title":"J. Colloid\nInterface Sci."},{"key":"2026081210094538900_cit49","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1016\/j.jconrel.2018.04.016","article-title":"Acid-sensitive\nhybrid polymeric micelles containing a reversibly activatable cell-penetrating\npeptide for tumor-specific cytoplasm targeting","volume":"279","author":"Tang","year":"2018","journal-title":"J. Controlled Release"},{"issue":"1","key":"2026081210094538900_cit50","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-024-49825-6","article-title":"An in-situ peptide-antibody self-assembly to block CD47 and CD24\nsignaling enhances macrophage-mediated phagocytosis and anti-tumor\nimmune responses","volume":"15","author":"Zhang","year":"2024","journal-title":"Nat. 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