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Mater."],"published-print":{"date-parts":[[2026,10,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    Multidrug resistance (MDR) remains a severe challenge in the field of cancer treatment. Herein, two types of drug delivery system based on heparin named as H\u2013F-DOX NPs (NPs-1) and H\u2013F-Tat-DOX NPs (NPs-2) are demonstrated for efficiently reversing MDR. NPs-1 and NPs-2 were developed by nanoprecipitation method to use succinylated-heparin as backbone and decorated with folate-targeting ligand or dual-targeting ligands of folate combined with cell-penetrating peptide Tat to release doxorubicin (DOX) for reversing MDR in A2780\/R (ovarian doxorubicin-resistant cell line) and HCT-8\/R (colorectal doxorubicin-resistant cell line). Cellular uptake assay, colocalization study, rhodamine 123 accumulation and cellular uptake mechanism were detected by flow cytometry and laser confocal microscope. The expression of P-gp was estimated by western blotting. Detection of intracellular adenosine triphosphate (ATP) level and reactive oxygen species (ROS) level were evaluated by luminescence assay and flow cytometry. The results of cytotoxicity, cellular uptake, colocalization, and detection of intracellular level of ATP and ROS level elucidated that NPs-2 could efficiently enter A2780\/R and HCT-8\/R cells through dual-targeting of cell penetrating peptide and folate, release more DOX into nucleus by the inhibition of drug efflux, significantly increase ROS level and reduce production of ATP level for inhibiting the proliferation of A2780\/R and HCT-8\/R cells. It is worth noting that the reversal coefficients of NPs-2 in A2780\/R and HCT-8\/R were 7.47 and 9.86. The endocytosis of NPs-2 in A2780\/R and HCT-8\/R depend on energy-dependent endocytosis, lipid raft and caveolae for efficient uptake and ATP production reduction. It demonstrates that NPs-2 could efficiently reverse MDR of ovarian and colorectal cancer\n                    <jats:italic>in vitro<\/jats:italic>\n                    . This strategy provides a novel approach by increasing endocytosis-mediated efficient cellular uptake and reducing energy production to construct smart drug delivery systems for reversing MDR.\n                  <\/jats:p>","DOI":"10.1088\/1748-605x\/aea048","type":"journal-article","created":{"date-parts":[[2026,8,28]],"date-time":"2026-08-28T22:53:56Z","timestamp":1787957636000},"page":"055012","update-policy":"https:\/\/doi.org\/10.1088\/crossmark-policy","source":"Crossref","is-referenced-by-count":0,"title":["Drug delivery systems modified with cell-penetrating peptide tat and folate reverse multidrug resistance in ovarian and colorectal cancer by endocytosis-mediated efficient uptake and energy production reduction"],"prefix":"10.1088","volume":"21","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8217-4044","authenticated-orcid":true,"given":"Junqiao","family":"Zhu","sequence":"first","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hanhan","family":"Zhu","sequence":"additional","affiliation":[{"name":"Jinan University"},{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiting","family":"Sun","sequence":"additional","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xinhai","family":"Zhu","sequence":"additional","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yanfang","family":"Chen","sequence":"additional","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Min","family":"Wang","sequence":"additional","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuqin","family":"Tang","sequence":"additional","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Zhang","sequence":"additional","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guichao","family":"Liu","sequence":"additional","affiliation":[{"name":"Southern University of Science and Technology"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhigang","family":"Zhou","sequence":"additional","affiliation":[{"name":"Central South University (The first people\u2019s hospital of Changde city)"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6130-7266","authenticated-orcid":true,"given":"Jianfu","family":"Zhao","sequence":"additional","affiliation":[{"name":"Jinan University"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"266","published-online":{"date-parts":[[2026,9,25]]},"reference":[{"key":"bmmaea048bib1","doi-asserted-by":"publisher","first-page":"760","DOI":"10.1038\/s41571-025-01059-1","type":"journal-article","article-title":"Understanding and overcoming multidrug resistance in cancer","volume":"22","author":"Ge","year":"2025","journal-title":"Nat. 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