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In addition, the hypoxic environment of tumors severely limits the effectiveness of photodynamic therapy (PDT). In this study, a universal extracellular-intracellular \u2018on-demand\u2019 release nanomedicine DOX@PDA-ICG@MnO<jats:sub>2<\/jats:sub>@GN-CEL was developed for the combined fight against malignant tumors using a spatiotemporal controlled gelatin coated polydopamine (PDA@GN) as the carrier and loaded with the chemotherapeutic drug doxorubicin (DOX), the photosensitizer indocyanine green (ICG), the PDT enhancer MnO<jats:sub>2<\/jats:sub> and the anti-inflammatory drug celecoxib (CEL) individually. Our results showed that DOX@PDA-ICG@MnO<jats:sub>2<\/jats:sub>@GN-CEL could release CEL extracellularly by matrix metalloproteinase-2 response and inhibit the COX-2\/PGE-2 pathway, reduce chemotherapy resistance and attenuate the concurrent inflammation. After entering the tumor cells, the remaining DOX@PDA-ICG@MnO<jats:sub>2<\/jats:sub> released DOX, ICG and MnO<jats:sub>2<\/jats:sub> intracellularly through PDA acid response. MnO<jats:sub>2<\/jats:sub> promoted the degradation of endogenous H<jats:sub>2<\/jats:sub>O<jats:sub>2<\/jats:sub> to generate oxygen under acidic conditions to alleviate the tumor hypoxic environment, enhance PDT triggered by ICG. PDA and ICG exhibited photothermal therapy synergistically, and DOX exerted chemotherapy with reduced chemotherapy resistance. The dual responsive drug release switch enabled the chemotherapeutic, photothermal, photodynamic and anti-inflammatory drugs precisely acted on different sites of tumor tissues and realized a promising multimodal combination therapy.<\/jats:p>","DOI":"10.1088\/1758-5090\/ad22ef","type":"journal-article","created":{"date-parts":[[2024,1,26]],"date-time":"2024-01-26T22:24:12Z","timestamp":1706307852000},"page":"025012","update-policy":"https:\/\/doi.org\/10.1088\/crossmark-policy","source":"Crossref","is-referenced-by-count":16,"title":["Multilayer nanodrug delivery system with spatiotemporal drug release improves tumor microenvironment for synergistic anticancer therapy"],"prefix":"10.1088","volume":"16","author":[{"given":"Jiahui","family":"Cai","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yibo","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jia","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhimin","family":"Bai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xin","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kun","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ming","family":"Shi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhiwei","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liming","family":"Gao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7418-4795","authenticated-orcid":true,"given":"Jidong","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1539-1166","authenticated-orcid":true,"given":"Jian","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"266","published-online":{"date-parts":[[2024,2,7]]},"reference":[{"key":"bfad22efbib1","doi-asserted-by":"publisher","first-page":"128","DOI":"10.1016\/j.carbon.2020.02.029","article-title":"Potential applications of multifunctional mesoporous carbon nanoplatform for tumor microenvironment improving by combined chemo-\/phototherapy","volume":"163","author":"Zhang","year":"2020","journal-title":"Carbon"},{"key":"bfad22efbib2","doi-asserted-by":"publisher","first-page":"436","DOI":"10.1038\/nature07205","article-title":"Cancer-related inflammation","volume":"454","author":"Mantovani","year":"2008","journal-title":"Nature"},{"key":"bfad22efbib3","doi-asserted-by":"publisher","first-page":"1965","DOI":"10.1016\/j.celrep.2019.01.080","article-title":"Immune cell types and secreted factors contributing to inflammation-to-cancer transition and immune therapy response","volume":"26","author":"Chen","year":"2019","journal-title":"Cell Rep."},{"key":"bfad22efbib4","doi-asserted-by":"publisher","first-page":"10019","DOI":"10.1158\/0008-5472.CAN-07-2354","article-title":"Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression","volume":"67","author":"Bunt","year":"2007","journal-title":"Cancer Res."},{"key":"bfad22efbib5","doi-asserted-by":"publisher","first-page":"584","DOI":"10.1038\/nrclinonc.2015.105","article-title":"Inflammation and cancer: advances and new agents","volume":"12","author":"Crusz","year":"2015","journal-title":"Nat. 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