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Nanoparticles predominantly enter solid tumors through blood vessel endothelial cells but then become trapped in the dense extracellular matrix layer. There are two known mechanisms that govern nanoparticle escape from this layer. Smaller nanoparticles slowly diffuse through the matrix into the tumor microenvironment. Larger nanoparticles trapped in the extracellular matrix are internalized and transported deeper into the tumor by macrophages. Here, we determined a third mechanism of nanoparticle penetration through the extracellular matrix. We show that neutrophil transendothelial migration through a remodeled extracellular matrix releases trapped nanoparticles into a less dense matrix microenvironment. We stimulated the transmigration process to increase the delivery of nanoparticles to cancer cells. We found that the three mechanisms are interrelated in allowing nanoparticles to escape the vascular extracellular matrix after entering the tumor. Our approach can lead to the development of strategies to increase the penetration of nanoparticles into the tumor microenvironment for efficient delivery to cancer cells.<\/jats:p>","DOI":"10.1021\/acsnano.5c21186","type":"journal-article","created":{"date-parts":[[2026,8,12]],"date-time":"2026-08-12T16:03:57Z","timestamp":1786550637000},"page":"23157-23174","source":"Crossref","is-referenced-by-count":0,"title":["Cellular Transmigration Increases Nanoparticle Penetration\nInto Solid Tumors"],"prefix":"10.1021","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-0446-9300","authenticated-orcid":true,"given":"Stefan M.","family":"Mladjenovic","sequence":"first","affiliation":[{"name":"University of Toronto , , Rosebrugh Building, 164 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3G9"]},{"name":"University of Toronto , , 160 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3E1"]},{"name":"University of Toronto , , , ,","place":["Toronto, Ontario, Canada, M5G 1L7"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Atta C. Y.","family":"Chang","sequence":"additional","affiliation":[{"name":"University of Toronto , , Rosebrugh Building, 164 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3G9"]},{"name":"University of Toronto , , 160 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3E1"]},{"name":"University of Toronto , , , ,","place":["Toronto, Ontario, Canada, M5G 1L7"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3847-3693","authenticated-orcid":true,"given":"Colin","family":"Blackadar","sequence":"additional","affiliation":[{"name":"University of Toronto , , Rosebrugh Building, 164 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3G9"]},{"name":"University of Toronto , , 160 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3E1"]},{"name":"University of Toronto , , , ,","place":["Toronto, Ontario, Canada, M5G 1L7"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qin","family":"Ji","sequence":"additional","affiliation":[{"name":"University of Toronto , , Rosebrugh Building, 164 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3G9"]},{"name":"University of Toronto , , 160 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3E1"]},{"name":"University of Toronto , , , ,","place":["Toronto, Ontario, Canada, M5G 1L7"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ayokunle A.","family":"Lekuti","sequence":"additional","affiliation":[{"name":"University of Toronto , , Rosebrugh Building, 164 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3G9"]},{"name":"University of Toronto , , 160 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3E1"]},{"name":"University of Toronto , , , ,","place":["Toronto, Ontario, Canada, M5G 1L7"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sara","family":"Ahmed","sequence":"additional","affiliation":[{"name":"University of Toronto , , Rosebrugh Building, 164 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3G9"]},{"name":"University of Toronto , , 160 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3E1"]},{"name":"University of Toronto , , , ,","place":["Toronto, Ontario, Canada, M5G 1L7"]},{"name":"University of Toronto , , Medical Science Building, Room 2256, 1 King\u2019s College Circle , , ,","place":["Toronto, Ontario, Canada, M5S 1A8"]},{"name":"University of Toronto , , 1 King\u2019s College Circle , , ,","place":["Toronto, Ontario, Canada, M5S 1A8"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5435-4785","authenticated-orcid":true,"given":"Warren C. W.","family":"Chan","sequence":"additional","affiliation":[{"name":"University of Toronto , , Rosebrugh Building, 164 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3G9"]},{"name":"University of Toronto , , 160 College Street , , ,","place":["Toronto, Ontario, Canada, M5S 3E1"]},{"name":"University of Toronto , , 80 St. George Street , , ,","place":["Toronto, Ontario, Canada, M5S 3H6"]},{"name":"Nanyang Technological University , ,","place":["Singapore, 637371"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"316","published-online":{"date-parts":[[2026,8,12]]},"reference":[{"key":"2026090202472590000_cit1","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1038\/s41563-019-0566-2","article-title":"The entry of nanoparticles\ninto solid tumours","volume":"19","author":"Sindhwani","year":"2020","journal-title":"Nat. Mater."},{"key":"2026090202472590000_cit2","doi-asserted-by":"publisher","first-page":"672","DOI":"10.1038\/s41565-025-01877-5","article-title":"The pathways for nanoparticle\ntransport across tumour endothelium","volume":"20","author":"Wu","year":"2025","journal-title":"Nat. Nanotechnol."},{"key":"2026090202472590000_cit3","doi-asserted-by":"publisher","first-page":"95","DOI":"10.1038\/s41565-023-01498-w","article-title":"Breaking through the\nbasement membrane barrier to improve nanotherapeutic delivery to tumours","volume":"19","author":"Wang","year":"2024","journal-title":"Nat. Nanotechnol."},{"key":"2026090202472590000_cit4","doi-asserted-by":"publisher","first-page":"395","DOI":"10.1083\/jcb.201102147","article-title":"The extracellular matrix: A dynamic\nniche in cancer progression","volume":"196","author":"Lu","year":"2012","journal-title":"J. Cell Biol."},{"key":"2026090202472590000_cit5","doi-asserted-by":"publisher","first-page":"217","DOI":"10.1038\/s41568-020-00329-7","article-title":"The matrix\nin cancer","volume":"21","author":"Cox","year":"2021","journal-title":"Nat. Rev. Cancer"},{"key":"2026090202472590000_cit6","doi-asserted-by":"publisher","first-page":"11008","DOI":"10.1021\/acsnano.9b02395","article-title":"Collagenase Nanoparticles\nEnhance the Penetration of Drugs into Pancreatic Tumors","volume":"13","author":"Zinger","year":"2019","journal-title":"ACS Nano"},{"key":"2026090202472590000_cit7","doi-asserted-by":"publisher","first-page":"E1142","DOI":"10.1073\/pnas.1521265113","article-title":"Tailoring nanoparticle designs to target\ncancer based on tumor pathophysiology","volume":"113","author":"Sykes","year":"2016","journal-title":"Proc.\nNatl. Acad. Sci. U.S.A."},{"key":"2026090202472590000_cit8","doi-asserted-by":"publisher","first-page":"8423","DOI":"10.1021\/acsnano.8b03900","article-title":"Quantifying the Ligand-Coated\nNanoparticle Delivery to Cancer Cells in Solid Tumors","volume":"12","author":"Dai","year":"2018","journal-title":"ACS Nano"},{"key":"2026090202472590000_cit9","doi-asserted-by":"publisher","first-page":"6080","DOI":"10.1021\/acsnano.1c11578","article-title":"Macrophages Actively\nTransport Nanoparticles in Tumors After Extravasation","volume":"16","author":"Lin","year":"2022","journal-title":"ACS Nano"},{"key":"2026090202472590000_cit10","doi-asserted-by":"publisher","first-page":"14080","DOI":"10.1021\/acsnano.1c04510","article-title":"Specific Endothelial\nCells Govern Nanoparticle Entry into Solid Tumors","volume":"15","author":"Kingston","year":"2021","journal-title":"ACS Nano"},{"key":"2026090202472590000_cit11","doi-asserted-by":"publisher","first-page":"1261","DOI":"10.1038\/s41563-023-01630-0","article-title":"The exit of nanoparticles\nfrom solid tumours","volume":"22","author":"Nguyen","year":"2023","journal-title":"Nat. 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Exp.\nMed."},{"key":"2026090202472590000_cit16","doi-asserted-by":"publisher","first-page":"2315","DOI":"10.1084\/jem.20151193","article-title":"Tumor macrophages are\npivotal constructors of tumor collagenous matrix","volume":"213","author":"Afik","year":"2016","journal-title":"J. Exp. Med."},{"key":"2026090202472590000_cit17","doi-asserted-by":"publisher","first-page":"1455","DOI":"10.1016\/j.ajpath.2011.05.031","article-title":"Tumor-Recruited Neutrophils\nand Neutrophil TIMP-Free MMP-9 Regulate Coordinately the Levels of\nTumor Angiogenesis and Efficiency of Malignant Cell Intravasation","volume":"179","author":"Bekes","year":"2011","journal-title":"Am. J. 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Lipid Res."},{"key":"2026090202472590000_cit25","doi-asserted-by":"publisher","first-page":"950","DOI":"10.1158\/0008-5472.CAN-14-0992","article-title":"CSF1 Receptor Targeting\nin Prostate Cancer Reverses Macrophage-Mediated Resistance to Androgen\nBlockade Therapy","volume":"75","author":"Escamilla","year":"2015","journal-title":"Cancer Res."},{"key":"2026090202472590000_cit26","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/djv017","article-title":"Blockade of MMP14 Activity\nin Murine Breast Carcinomas: Implications for Macrophages, Vessels,\nand Radiotherapy","volume":"107","author":"Ager","year":"2015","journal-title":"JNCI: J. Natl. Cancer Inst."},{"key":"2026090202472590000_cit27","doi-asserted-by":"publisher","first-page":"2830","DOI":"10.7150\/thno.23209","article-title":"Targeting intracellular\nMMPs efficiently inhibits tumor metastasis and angiogenesis","volume":"8","author":"Lv","year":"2018","journal-title":"Theranostics"},{"key":"2026090202472590000_cit28","doi-asserted-by":"publisher","first-page":"9825","DOI":"10.1021\/acsnano.7b03150","article-title":"In Situ Imaging of Tissue\nRemodeling with Collagen Hybridizing Peptides","volume":"11","author":"Hwang","year":"2017","journal-title":"ACS Nano"},{"key":"2026090202472590000_cit29","doi-asserted-by":"publisher","first-page":"10901","DOI":"10.1021\/jacs.3c00713","article-title":"The Chemistry and Biology\nof Collagen Hybridization","volume":"145","author":"Li","year":"2023","journal-title":"J. Am. Chem. 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Leukocyte Biol."},{"key":"2026090202472590000_cit34","doi-asserted-by":"publisher","first-page":"3832","DOI":"10.1182\/blood-2012-12-473835","article-title":"Elevated CXCL1 expression\nin gp130-deficient endothelial cells impairs neutrophil migration\nin mice","volume":"122","author":"Yao","year":"2013","journal-title":"Blood"},{"issue":"5","key":"2026090202472590000_cit35","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1182\/blood-2012-12-472944","article-title":"Matrix\nmetalloproteinases modulate ameboid-like migration of neutrophils\nthrough inflamed interstitial tissue","volume":"122","author":"Lerchenberger","year":"2013","journal-title":"Blood"},{"key":"2026090202472590000_cit36","doi-asserted-by":"publisher","first-page":"533","DOI":"10.1038\/nnano.2015.342","article-title":"Vascular bursts enhance\npermeability of tumour blood vessels and improve nanoparticle delivery","volume":"11","author":"Matsumoto","year":"2016","journal-title":"Nat. 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Interfaces"},{"key":"2026090202472590000_cit43","doi-asserted-by":"publisher","first-page":"1200","DOI":"10.1080\/10717544.2018.1474973","article-title":"Neutrophil-mediated delivery of pixantrone-loaded\nliposomes decorated with poly(sialic acid)\u2013octadecylamine conjugate\nfor lung cancer treatment","volume":"25","author":"Luo","year":"2018","journal-title":"Drug Delivery"},{"key":"2026090202472590000_cit44","doi-asserted-by":"publisher","first-page":"176","DOI":"10.1016\/j.actbio.2020.01.011","article-title":"Neutrophil-mediated\ntransport is crucial for delivery of short-circulating magnetic nanoparticles\nto tumors","volume":"104","author":"Naumenko","year":"2020","journal-title":"Acta Biomater."},{"key":"2026090202472590000_cit45","doi-asserted-by":"publisher","DOI":"10.1002\/adma.201701021","article-title":"Photosensitization\nPriming of Tumor Microenvironments Improves Delivery of Nanotherapeutics\nvia Neutrophil Infiltration","volume":"29","author":"Chu","year":"2017","journal-title":"Adv. Mater."},{"key":"2026090202472590000_cit46","doi-asserted-by":"publisher","first-page":"42402","DOI":"10.1021\/acsnano.5c14907","article-title":"Transporting via Neutrophil\nas a Key Mechanism for Nanoparticle Redistribution to Tumor and Spleen","volume":"19","author":"Wang","year":"2025","journal-title":"ACS Nano"},{"key":"2026090202472590000_cit47","doi-asserted-by":"publisher","first-page":"15542","DOI":"10.1021\/acsnano.3c02013","article-title":"Neutrophil-Mediated\nDelivery of Nanocrystal Drugs via Photoinduced Inflammation Enhances\nCancer Therapy","volume":"17","author":"Su","year":"2023","journal-title":"ACS Nano"},{"key":"2026090202472590000_cit48","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s44222-024-00154-9","article-title":"The mechanisms of nanoparticle\ndelivery to solid tumours","volume":"2","author":"Nguyen","year":"2024","journal-title":"Nat. Rev. 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