Targeted Inhibition of Tumor Inflammation and Tumor-Platelet Crosstalk by Nanoparticle-Mediated Drug Delivery Mitigates Cancer Metastasis
Abstract
Sowing malignant cells (the "seeds" of metastasis) to engraft secondary sites requires a conducive premetastatic niche (PMN, the "soil" of metastasis). Inflammation and tumor associated platelet (TAP) has been hijacked by primary tumors to induce PMN "soil" in distant organs, as well as facilitate the dissemination of "seeds". This study reports a combinatory strategy with activated platelet-targeting nanoparticles to aim at the dynamic process of entire cancer metastasis, which exerts robust antimetastasis efficacy by simultaneously inhibiting tumor inflammation and tumor-platelet crosstalk. Our results reveals that the PSN peptide (a P-selectin-targeting peptide) modification enriched the accumulation of nanoparticles in primary tumor, pulmonary PMN, and metastases via capturing activated platelet. Such characteristics contribute to the efficient inhibition on almost every crucial and consecutive step of the metastasis cascade by retarding epithelial-mesenchymal transition (EMT) progression within tumors, specifically blocking the tumor-platelet crosstalk to remove the platelets "protective shield" around disseminated "seeds", and reversing the inflammatory microenvironment to interfere with the "soil" formation. Consisting of inflammation inhibiting and TAP impeding nanoparticles, this approach prominently reduces various metastasis in abscopal lung, including spontaneous metastasis, disseminated tumor cells metastasis, and post-operative metastasis. This work provides a generalizable nanoplatform of parallel inflammation disturbance and tumor-TAP crosstalk blockade to resist metastatic tumors.
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The magnetic response intelligent nano system has two treatment procedures: the first uses magnetic fields to assist drug targeting, and the second uses magnetic fields to cause hyperthermia.
“As a result, the magnetic response intelligent nano system has two treatment procedures. The first technique uses magnetic fields to assist drug targeting, whereas the second uses magnetic fields to cause hyperthermia.186–188”
From Smart nanoparticles for cancer therapy (2023) · cites this paper as [187]
Cites
Sung, H., Ferlay, J., Siegel, R. L., Laversanne, M., Soerjomataram, I., Jemal, A., & Bray, F. (2021) · CA: A Cancer Journal for Clinicians · doi:10.3322/caac.21660 · Cited by 108,699 · see citing works
Cancer Metastasis: Building a Framework
Gupta, G. P., & Massagué, J. (2006) · Cell · doi:10.1016/j.cell.2006.11.001 · Cited by 4,230 · see citing works
Metastatic colonization by circulating tumour cells
Massagué, J., & Obenauf, A. C. (2016) · Nature · doi:10.1038/nature17038 · Cited by 2,062 · see citing works
Pre-metastatic niches: organ-specific homes for metastases
Peinado, H., Zhang, H., Matei, I. R., Costa-Silva, B., Hoshino, A., Rodrigues, G., Psaila, B., Kaplan, R. N., Bromberg, J. F., Kang, Y., et al. (2017) · Nature Reviews Cancer · doi:10.1038/nrc.2017.6 · Cited by 1,889 · see citing works
20-Year Risks of Breast-Cancer Recurrence after Stopping Endocrine Therapy at 5 Years
Pan, H., Gray, R. G., Braybrooke, J. P., Davies, C., Taylor, C. W., McGale, P., Peto, R., Pritchard, K. I., Bergh, J. C. S., Dowsett, M., et al. (2017) · New England Journal of Medicine · doi:10.1056/nejmoa1701830 · Cited by 1,834 · see citing works
Labelle, M., Begum, S., & Hynes, R. O. (2011) · Cancer Cell · doi:10.1016/j.ccr.2011.09.009 · Cited by 1,833 · see citing works
Image-guided cancer surgery using near-infrared fluorescence
Vahrmeijer, A. L., Hutteman, M., van der Vorst, J. R., van de Velde, C. J. �., & Frangioni, J. V. (2013) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2013.123 · Cited by 1,470 · see citing works
Steeg, P. S. (2016) · Nature Reviews Cancer · doi:10.1038/nrc.2016.25 · Cited by 1,363 · see citing works
Loh, C.-Y., Chai, J., Tang, T. F., Wong, W. F., Sethi, G., Shanmugam, M. K., Chong, P. P., & Looi, C. Y. (2019) · Cells · doi:10.3390/cells8101118 · Cited by 1,323 · see citing works
The metastatic niche: adapting the foreign soil
Psaila, B., & Lyden, D. C. (2009) · Nature reviews. Cancer · doi:10.1038/nrc2621 · Cited by 1,302 · see citing works
Characteristics and Significance of the Pre-metastatic Niche
Liu, Y., & Cao, X. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.09.011 · Cited by 1,287 · see citing works
Borsig, L., Wong, R., Feramisco, J., Nadeau, D. R., Varki, N. M., & Varki, A. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.061615598 · Cited by 714 · see citing works
Cytokines and their relationship to the symptoms and outcome of cancer
Seruga, B., Zhang, H., Bernstein, L. J., & Tannock, I. F. (2008) · Nature Reviews Cancer · doi:10.1038/nrc2507 · Cited by 652 · see citing works
The Platelet Lifeline to Cancer: Challenges and Opportunities
Haemmerle, M., Stone, R. L., Menter, D. G., Afshar‐Kharghan, V., & Sood, A. K. (2018) · Cancer Cell · doi:10.1016/j.ccell.2018.03.002 · Cited by 638 · see citing works
Schumacher, D., Strilic, B., Sivaraj, K., Wettschureck, N., & Offermanns, S. (2013) · Cancer Cell · doi:10.1016/j.ccr.2013.05.008 · Cited by 614 · see citing works
TGF-β Tumor Suppression through a Lethal EMT
David, C. J., Huang, Y.-H., Chen, M., Su, J., Zou, Y., Bardeesy, N. M., Iacobuzio–Donahue, C. A., & Massagué, J. (2016) · Cell · doi:10.1016/j.cell.2016.01.009 · Cited by 597 · see citing works
Self-citationMurata, M. (2018) · Environmental Health and Preventive Medicine · doi:10.1186/s12199-018-0740-1 · Cited by 589 · see citing works
EMT and inflammation: inseparable actors of cancer progression
Suarez‐Carmona, M., Lesage, J., Cataldo, D. D., & Gilles, C. (2017) · Molecular Oncology · doi:10.1002/1878-0261.12095 · Cited by 573 · see citing works
Platelets guide the formation of early metastatic niches
Labelle, M., Begum, S., & Hynes, R. O. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411082111 · Cited by 555 · see citing works
Nanoparticles Coated with Neutrophil Membranes Can Effectively Treat Cancer Metastasis
Kang, T., Zhu, Q., Wei, D., Feng, J., Yao, J., Jiang, T., Song, Q., Wei, X., Chen, H., Gao, X., et al. (2017) · ACS Nano · doi:10.1021/acsnano.6b06477 · Cited by 554 · see citing works
EMT: Mechanisms and therapeutic implications
Singh, M., Yelle, N., Venugopal, C., & Singh, S. K. (2017) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2017.08.009 · Cited by 476 · see citing works
Selectins promote tumor metastasis
Laubli, H. P., & Borsig, L. (2010) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2010.04.005 · Cited by 464 · see citing works
The effects of surgery on tumor growth: a century of investigations
Demicheli, R., Retsky, M. W., Hrushesky, W. J. M., Baum, M., & Gukas, I. D. (2008) · Annals of Oncology · doi:10.1093/annonc/mdn386 · Cited by 400 · see citing works
A cancer vaccine-mediated postoperative immunotherapy for recurrent and metastatic tumors
Wang, T., Wang, D., Yu, H., Feng, B., Zhou, F., Zhang, H., Zhou, L., Jiao, S., & Li, Y. (2018) · Nature Communications · doi:10.1038/s41467-018-03915-4 · Cited by 394 · see citing works
Gil‐Bernabé, A. M., Ferjancic, S., Tlalka, M., Zhao, L., Allen, P. D., Im, J. H., Watson, K., Hill, S. A., Amirkhosravi, A., Francis, J. L., et al. (2012) · Blood · doi:10.1182/blood-2011-08-376426 · Cited by 353 · see citing works
Overcoming the Reticuloendothelial System Barrier to Drug Delivery with a “Don’t-Eat-Us” Strategy
Tang, Y., Wang, X., Li, J., Nie, Y., Liao, G., Yu, Y., & Li, C. (2019) · ACS Nano · doi:10.1021/acsnano.9b05679 · Cited by 341 · see citing works
Epigenetic therapy inhibits metastases by disrupting premetastatic niches
Lu, Z., Zou, J., Li, S., Topper, M. J., Tao, Y., Zhang, H., Jiao, X., Xie, W., Kong, X., Vaz, M., et al. (2020) · Nature · doi:10.1038/s41586-020-2054-x · Cited by 330 · see citing works
Self-citationFactors involved in cancer metastasis: a better understanding to “seed and soil” hypothesis
Liu, Q., Zhang, H., Jiang, X., Qian, C., Liu, Z., & Luo, D. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0742-4 · Cited by 328 · see citing works
Xu, X., Yousef, G. M., & Ni, H. (2018) · Blood · doi:10.1182/blood-2017-05-743187 · Cited by 324 · see citing works
Chiang, S., Cabrera, R. M., & Segall, J. E. (2016) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00238.2015 · Cited by 310 · see citing works
Inflammation-Induced Tumorigenesis and Metastasis
Hibino, S., Kawazoe, T., Kasahara, H., Itoh, S., Ishimoto, T., Sakata‐Yanagimoto, M., & Taniguchi, K. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115421 · Cited by 303 · see citing works
Gallo, O., Franchi, A., Magnelli, L., Sardi, I., Vannacci, A., Boddit, V., Chiarugi, V. P., & Masini, E. (2001) · Neoplasia · doi:10.1038/sj.neo.7900127 · Cited by 298 · see citing works
The evolving role of platelets in inflammation
Weyrich, A. S., Lindemann, S., & Zimmerman, G. A. (2003) · Journal of Thrombosis and Haemostasis · doi:10.1046/j.1538-7836.2003.00304.x · Cited by 293 · see citing works
Involvement of platelets in tumor cell metastasis
Tesfamariam, B. (2015) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2015.11.005 · Cited by 228 · see citing works
Paradoxical effects of chemotherapy on tumor relapse and metastasis promotion
D’Alterio, C., Scala, S., Sozzi, G., Roz, L., & Bertolini, G. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.08.019 · Cited by 224 · see citing works
Platelets in cancer metastasis: To help the “villain” to do evil
Li, N.-L. (2016) · International Journal of Cancer · doi:10.1002/ijc.29847 · Cited by 221 · see citing works
Lung inflammation promotes metastasis through neutrophil protease-mediated degradation of Tsp-1
Rayes, T. E., Catena, R., Lee, S. B., Stawowczyk, M., Joshi, N., Fischbach, C., Powell, C. A., Dannenberg, A. J., Altorki, N. K., Gao, D., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1507294112 · Cited by 209 · see citing works
Kim, Y. J., Borsig, L., Han, H., Varki, N. M., & Varki, A. P. (1999) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)65142-5 · Cited by 189 · see citing works
Intraoperative diagnostics and elimination of residual microtumours with plasmonic nanobubbles
Lukianova‐Hleb, E. Y., Kim, Y.-S., Belatsarkouski, I., Gillenwater, A. M., O’Neill, B. E., & Lapotko, D. O. (2016) · Nature Nanotechnology · doi:10.1038/nnano.2015.343 · Cited by 178 · see citing works
Epithelial-mesenchymal transition and inflammation at the site of the primary tumor
Dominguez, C. L., David, J. M., & Palena, C. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.08.002 · Cited by 160 · see citing works
Two-stage oxygen delivery for enhanced radiotherapy by perfluorocarbon nanoparticles
Zhou, Z., Zhang, B., Wang, H., Yuan, A., Hu, Y., & Wu, J. (2018) · Theranostics · doi:10.7150/thno.27598 · Cited by 139 · see citing works
The pro-inflammatory role of platelets in cancer
Olsson, A., & Cedervall, J. (2018) · Platelets · doi:10.1080/09537104.2018.1453059 · Cited by 126 · see citing works
Yamauchi, K., Yang, M., Hayashi, K., Jiang, P., Yamamoto, N., Tsuchiya, H., Tomita, K., Moossa, A. R., Bouvet, M., & Hoffman, R. M. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-3063 · Cited by 122 · see citing works
Dovizio, M., Maier, T. J., Alberti, S., Francesco, L. D., Marcantoni, E., Münch, G., John, C. M., Suess, B., Sgambato, A., Steinhilber, D., et al. (2013) · Molecular Pharmacology · doi:10.1124/mol.113.084988 · Cited by 120 · see citing works
Gingis‐Velitski, S., Loven, D., Benayoun, L., Munster, M., Bril, R., Voloshin, T., Alishekevitz, D., Bertolini, F., & Shaked, Y. (2011) · Cancer Research · doi:10.1158/0008-5472.can-11-0629 · Cited by 116 · see citing works
Ruiterkamp, J., Voogd, A. C., Bosscha, K. P., Tjan‐Heijnen, V. C. G., & Ernst, M. F. (2009) · Breast Cancer Research and Treatment · doi:10.1007/s10549-009-0670-0 · Cited by 112 · see citing works
Role of Platelet-Derived Tgfβ1 in the Progression of Ovarian Cancer
Hu, Q., Hisamatsu, T., Hämmerle, M., Cho, M. S., Pradeep, S., Rupaimoole, R., Rodriguez‐Aguayo, C., Lopez‐Berestein, G., Wong, S. T. C., Sood, A. K., et al. (2017) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-16-3272 · Cited by 102 · see citing works
Inflammation fires up cancer metastasis
Qian, B. (2017) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2017.08.006 · Cited by 98 · see citing works
Huang, Y., Yu, L., Ren, J., Gu, B., Longstaff, C., Hughes, A. D., Thom, S., Xu, X. Y., & Chen, R. (2019) · Journal of Controlled Release · doi:10.1016/j.jconrel.2019.02.033 · Cited by 95 · see citing works
Self-citationAssociation of cyclooxygenase-2 and matrix metalloproteinase-2 expression in human breast cancer
Sivula, A., Talvensaari‐Mattila, A., Lundin, J. E., Joensuu, H., Haglund, C. H., Ristim�ki, A., & Turpeenniemi-Hujanen, T. M. (2005) · Breast Cancer Research and Treatment · doi:10.1007/s10549-004-0714-4 · Cited by 92 · see citing works
Wang, T., Zhang, J., Hou, T., Yin, X., & Zhang, N. (2019) · Nanoscale · doi:10.1039/c9nr03374b · Cited by 91 · see citing works
Xu, Y., Liu, J., Liu, Z., Ren, H., Yong, J., Li, W., Wang, H., Yang, Z., Wang, Y., Chen, G., et al. (2020) · ACS Nano · doi:10.1021/acsnano.0c01687 · Cited by 91 · see citing works
Role of Platelets in Inflammation and Cancer: Novel Therapeutic Strategies
Dovizio, M., Alberti, S., Guillem‐Llobat, P., & Patrignani, P. (2013) · Basic & Clinical Pharmacology & Toxicology · doi:10.1111/bcpt.12156 · Cited by 89 · see citing works
Inhibition of platelet function using liposomal nanoparticles blocks tumor metastasis
Zhang, Y., Wei, J., Liu, S., Wang, J., Han, X., Qin, H., Lang, J., Cheng, K., Li, Y., Qi, Y., et al. (2017) · Theranostics · doi:10.7150/thno.17908 · Cited by 87 · see citing works
Self-citationTargeting self-assembly peptide for inhibiting breast tumor progression and metastasis
Luo, S., Feng, J., Xiao, L., Guo, L., Deng, L., Du, Z., Xue, Y., Song, X., Sun, X., Zhang, Z., et al. (2020) · Biomaterials · doi:10.1016/j.biomaterials.2020.120055 · Cited by 87 · see citing works
The brain tissue response to surgical injury and its possible contribution to glioma recurrence
Hamard, L., Ratel, D., Selek, L., Berger, F. R., van der Sanden, B. P. J., & Wion, D. (2016) · Journal of Neuro-Oncology · doi:10.1007/s11060-016-2096-y · Cited by 83 · see citing works
The gate to metastasis: key players in cancer cell intravasation
Sznurkowska, M. K., & Aceto, N. (2021) · FEBS Journal · doi:10.1111/febs.16046 · Cited by 81 · see citing works
Han, Z., Lv, W., Li, Y., Chang, J., Zhang, W., Liu, C., & Sun, J. (2020) · ACS Applied Bio Materials · doi:10.1021/acsabm.0c00181 · Cited by 78 · see citing works
Gómez‐Vallejo, V., Puigivila, M., Plaza‐García, S., Szczupak, B., Piñol, R., Murillo, J. L., Sorribas, V., Lou, G., Veintemillas-Verdaguer, S., Ramos‐Cabrer, P., et al. (2018) · Nanoscale · doi:10.1039/c8nr03084g · Cited by 74 · see citing works
Guo, R., Deng, M., He, X., Li, M., Li, J., He, P., Liu, H., Li, M., Zhang, Z., & He, Q. S. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.05.012 · Cited by 74 · see citing works
Jiang, T., Chen, L., Huang, Y., Wang, J., Xu, M., Zhou, S., Gu, X. Q., Chen, Y., Liang, K., Pei, Y., et al. (2019) · Nano Letters · doi:10.1021/acs.nanolett.9b00495 · Cited by 70 · see citing works
Self-citationZhang, Y., Zhu, X., Chen, X., Chen, Q., Zhou, W., Guo, Q., Lü, Y., Li, C., Zhang, Y. X., Liang, D., et al. (2019) · Advanced Functional Materials · doi:10.1002/adfm.201806620 · Cited by 69 · see citing works
Wang, J., Su, X., Liu, Y., Qiao, F., Yu, F., Yu, L., Yang, Q., Wang, Y., Yin, Y., Chen, R., et al. (2016) · International Journal of Cancer · doi:10.1002/ijc.29998 · Cited by 67 · see citing works
Modery, C. L., Ravikumar, M., Wong, T. L., Dzuricky, M. J., Durongkaveroj, N., & Gupta, A. S. (2011) · Biomaterials · doi:10.1016/j.biomaterials.2011.08.067 · Cited by 65 · see citing works
Liu, S., Zhang, Y., Zhao, X., Wang, J., Di, C., Zhao, Y., Ji, T., Cheng, K., Wang, Y., Chen, L., et al. (2019) · Nano Letters · doi:10.1021/acs.nanolett.9b01785 · Cited by 62 · see citing works
Self-citationNie, L., Li, F., Huang, X., Aguilar, Z. P., Wang, Y. A., Xiong, Y., Fu, F., & Xu, H. (2018) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.8b02583 · Cited by 61 · see citing works
Prognosis and targeting of pre-metastatic niche
Zhou, Y., Han, M. Y., & Gao, J. (2020) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.06.037 · Cited by 60 · see citing works
Dymicka-Piekarska, V., Koper‐Lenkiewicz, O. M., Dorf, J., Kratz, E. M., & Kamińska, J. (2020) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-020-02758-7 · Cited by 59 · see citing works
Yap, M. L., McFadyen, J. D., Wang, X., Ziegler, M., Chen, Y., Willcox, A., Nowell, C. J., Scott, A. M., Sloan, E. K., Hogarth, P. M., et al. (2019) · Theranostics · doi:10.7150/thno.29146 · Cited by 56 · see citing works
Qian, X., Ge, L., Yuan, K., Li, C., Xu, Z. C., Cai, W., Cheng, R., & Jiang, X. (2019) · Theranostics · doi:10.7150/thno.33470 · Cited by 51 · see citing works
Multifaceted role of cancer educated platelets in survival of cancer cells
Asghar, S., Parvaiz, F., & Manzoor, S. (2019) · Thrombosis Research · doi:10.1016/j.thromres.2019.02.026 · Cited by 43 · see citing works
Ghouse, S. M., Vadrevu, S. K., Manne, S., Reese, B., Patel, J., Patel, B. B., Silwal, A., Lodhi, N., Paterson, Y. Y. W., Srivastava, S., et al. (2020) · The Journal of Immunology · doi:10.4049/jimmunol.1901208 · Cited by 41 · see citing works
Redox-responsive amphiphilic camptothecin prodrug nanoparticles for targeted liver tumor therapy
Lu, L., Li, B., Lin, C., Li, K., Liu, G., Xia, Z., Luo, Z. Y., & Cai, K. (2020) · Journal of Materials Chemistry B · doi:10.1039/d0tb00285b · Cited by 41 · see citing works
Double-sided effect of tumor microenvironment on platelets targeting nanoparticles
Chen, X., Wang, Q., Liu, L., Sun, T., Zhou, W., Chen, Q., Lü, Y., He, X., Zhang, Y., Zhang, Y., et al. (2018) · Biomaterials · doi:10.1016/j.biomaterials.2018.07.005 · Cited by 40 · see citing works
Targeting tumor metastases: Drug delivery mechanisms and technologies
Ganapathy, V., Moghe, P. V., & Roth, C. M. (2015) · Journal of Controlled Release · doi:10.1016/j.jconrel.2015.09.042 · Cited by 39 · see citing works
Postoperative cancer treatments: In-situ delivery system designed on demand
Zhang, Y., & Jiang, C. (2021) · Journal of Controlled Release · doi:10.1016/j.jconrel.2020.12.038 · Cited by 35 · see citing works
A novel nanomissile targeting two biomarkers and accurately bombing CTCs with doxorubicin
Gao, Y., Xie, X., Li, F., Lu, Y., Li, T., Lian, S., Zhang, Y., Zhang, H., Mei, H., & Jia, L. (2017) · Nanoscale · doi:10.1039/c7nr00273d · Cited by 34 · see citing works
Gkolfinopoulos, S., Jones, R. L., & Constantinidou, A. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.00374 · Cited by 34 · see citing works
Chemotherapy can promote liver metastasis by enhancing metastatic niche formation in mice
Zenitani, M., Nojiri, T., Hosoda, H., Kimura, T., Uehara, S., Miyazato, M., Okuyama, H., & Kangawa, K. (2017) · Journal of Surgical Research · doi:10.1016/j.jss.2017.11.050 · Cited by 29 · see citing works
Ye, Y., Liu, S., Wu, C., & Sun, Z. (2015) · Journal of Molecular Histology · doi:10.1007/s10735-015-9633-4 · Cited by 27 · see citing works
Targeting Delivery of Platelets Inhibitor to Prevent Tumor Metastasis
Geranpayehvaghei, M., Shi, Q., Zhao, B., Li, S., Xu, J., Taleb, M., Qin, H., Zhang, Y., Khajeh, K., & Nie, G. (2019) · Bioconjugate Chemistry · doi:10.1021/acs.bioconjchem.9b00457 · Cited by 24 · see citing works
Self-citationGuo, W., Gao, X., Zhan, R., Zhao, Z., Xu, K., & Tang, B. (2020) · Talanta · doi:10.1016/j.talanta.2020.121525 · Cited by 24 · see citing works
Cancer metastasis versus stem cell homing: Role of platelets
Naderi‐Meshkin, H., & Ahmadiankia, N. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.26937 · Cited by 20 · see citing works
Ye, Y., Pei, L., Wu, C., & Liu, S. (2019) · Integrative Cancer Therapies · doi:10.1177/1534735419876341 · Cited by 20 · see citing works
P2Y12 antibody inhibits platelet activity and protects against thrombogenesis
Hensch, N. R., Karim, Z. A., Pineda, J., Mercado, N., Alshbool, F. Z., & Khasawneh, F. T. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.09.083 · Cited by 16 · see citing works
Pre-Metastatic Niche Formation Has Taken Its TOLL
Kenific, C. M., Nogués, L., & Lyden, D. C. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.07.012 · Cited by 12 · see citing works
Li, J., Zheng, L., Wang, R., Sun, D., Liang, S., Wu, J., Liu, Y., Tian, X., Li, T., Yang, Y., et al. (2020) · International Journal of Nanomedicine · doi:10.2147/ijn.s259432 · Cited by 12 · see citing works
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Sun, L., Liu, H., Ye, Y., Lei, Y., Islam, R., Tan, S., Tong, R., Miao, Y.-B., & Cai, L. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01642-x · Cited by 1,073 · see citing works
The dynamic role of platelets in cancer progression and their therapeutic implications
Li, S., Lu, Z., Wu, S., Chu, T., Li, B., Qi, F., Zhao, Y., & Nie, G. (2023) · Nature reviews. Cancer · doi:10.1038/s41568-023-00639-6 · Cited by 218 · see citing works
Self-citationBiomimetic Nano-Drug Delivery System: An Emerging Platform for Promoting Tumor Treatment
Han, X., Gong, C., Yang, Q., Zheng, K., Wang, Z., & Zhang, W. (2024) · International Journal of Nanomedicine · doi:10.2147/ijn.s442877 · Cited by 109 · see citing works
Liao, K., Zhang, X., Liu, J., Teng, F., He, Y., Cheng, J., Yang, Q., Zhang, W., Xie, Y., Guo, D., et al. (2023) · MedComm · doi:10.1002/mco2.350 · Cited by 100 · see citing works
Zhang, Z., Yan, H., Cao, W., Xie, S., Ran, P., Wei, K., & Li, X. (2023) · ACS Nano · doi:10.1021/acsnano.3c04906 · Cited by 67 · see citing works
Chao, C.-J., Zhang, E., & Zhao, Z. (2023) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2023.114840 · Cited by 59 · see citing works
Zhang, Z., Xia, T., Ran, P., Wei, J., Meng, J., Zhang, G., & Li, X. (2022) · Chemical Engineering Journal · doi:10.1016/j.cej.2022.141226 · Cited by 54 · see citing works
Gou, S., Wang, G., Zou, Y., Geng, W., He, T., Qin, Z., Che, L., Feng, Q., & Cai, K. (2023) · Advanced Materials · doi:10.1002/adma.202303718 · Cited by 54 · see citing works
EMT and cancer stem cells: Drivers of therapy resistance and promising therapeutic targets
Jiang, M., Wang, J., Li, Y., Zhang, K., Wang, T., Bo, Z., Lu, S., Alarcón, R., Wei, R., Zhu, M., et al. (2025) · Drug Resistance Updates · doi:10.1016/j.drup.2025.101276 · Cited by 56 · see citing works
Endothelial Cell Adhesion Molecules- (un)Attainable Targets for Nanomedicines
Milošević, N., Rütter, M., & David, A. (2022) · Frontiers in Medical Technology · doi:10.3389/fmedt.2022.846065 · Cited by 38 · see citing works
Ilieş, B. D., Yıldız, İ., & Abbas, M. (2024) · ChemBioChem · doi:10.1002/cbic.202300867 · Cited by 37 · see citing works
Boosting Theranostic Performance of AIEgens Using Nanocatalyzer for Robust Cancer Immunotherapy
Li, Y., Du, Z., Zhang, Y., Kang, X., Song, J., Chen, X., Hu, Y., Yang, Z., Qi, J., & Shen, X. (2024) · Advanced Functional Materials · doi:10.1002/adfm.202315127 · Cited by 34 · see citing works
Platelets in the tumor microenvironment and their biological effects on cancer hallmarks
Chen, L., Zhu, C., Pan, F., Chen, Y., Xiong, L., Li, Y., Chu, X., & Huang, G. (2023) · Frontiers in Oncology · doi:10.3389/fonc.2023.1121401 · Cited by 31 · see citing works
Theoretical basis, state and challenges of living cell-based drug delivery systems
Liu, W., Cheng, G., Cui, H., Tian, Z., Li, B., Han, Y., Wu, J., Sun, J., Zhao, Y., Chen, T., et al. (2024) · Theranostics · doi:10.7150/thno.99257 · Cited by 30 · see citing works
Study on the mechanism of MDSC-platelets and their role in the breast cancer microenvironment
Han, X., Song, X., Xiao, Z., Zhu, G., Gao, R., Ni, B., & Li, J. (2024) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2024.1310442 · Cited by 29 · see citing works
Kong, J., Deng, Y., Xu, Y., Zhang, P., Li, L., & Huang, Y. (2024) · ACS Nano · doi:10.1021/acsnano.3c09165 · Cited by 29 · see citing works
Self-citationHe, J., Wang, Y., Ren, Y., Yuan, Q., Zhang, Z., Li, L., Bao, B., Jia, W., Zhang, X., Li, M., et al. (2024) · ACS Nano · doi:10.1021/acsnano.4c05771 · Cited by 29 · see citing works
Self-citationThe role of tumor-platelet interplay and micro tumor thrombi during hematogenous tumor metastasis
Shi, Q., Ji, T., Tang, X., & Guo, W. (2023) · Cellular Oncology · doi:10.1007/s13402-023-00773-1 · Cited by 28 · see citing works
He, M., Yu, H., Zhao, Y., Liu, J., Dong, Q., Xu, Z., Kang, Y., & Xue, P. (2023) · Small · doi:10.1002/smll.202300244 · Cited by 24 · see citing works
Gao, J.-H., He, A., Liu, L.-M., Zhou, Y.-J., Guo, Y.-W., Meng, L., Zeng, X., Gong, X., Lu, Y., Liang, H., et al. (2024) · Cancer Letters · doi:10.1016/j.canlet.2024.216674 · Cited by 23 · see citing works
Garofano, K., Rashid, K., Smith, M., Brantner, C. A., Suwunnakorn, S., Diemert, D. J., Gordon, O. F., Horvath, A., Khan, S., Popratiloff, A. S., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-29450-x · Cited by 21 · see citing works
Chen, S., Wu, A., Shen, X., Kong, J., & Huang, Y. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.01.053 · Cited by 21 · see citing works
Self-citationFeng, Y., Liu, C., Cui, W., Yang, L., Wu, D., Zhang, H., Wang, X., Sun, Y., He, B., Dai, W., et al. (2024) · Science Advances · doi:10.1126/sciadv.adq2072 · Cited by 20 · see citing works
Peritumoral scaffold neutralizes tumor pH for chemotherapy sensitization and metastasis inhibition
Yan, Y., Li, J., Yi, X., Liu, C., Zhou, Z., Huang, Y., & Li, L. (2022) · Journal of Controlled Release · doi:10.1016/j.jconrel.2022.11.006 · Cited by 20 · see citing works
Self-citationPlatelets in cancer and immunotherapy: functional dynamics and therapeutic opportunities
Cai, C., Liu, Y., Lu, R., Fan, X., Zeng, S., & Gan, P. (2025) · Experimental Hematology and Oncology · doi:10.1186/s40164-025-00676-x · Cited by 23 · see citing works
Gui, J., Zhu, Y., Chen, X., Gong, T., Zhang, Z., Yu, R., & Fu, Y. S. (2024) · Acta Biomaterialia · doi:10.1016/j.actbio.2024.01.037 · Cited by 18 · see citing works
Platelets for advanced drug delivery in cancer
Cacic, D. L., Hervig, T. A., & Reikvam, H. (2023) · Expert Opinion on Drug Delivery · doi:10.1080/17425247.2023.2217378 · Cited by 17 · see citing works
Ciummo, S. L., Sorrentino, C., Fieni, C., & Carlo, E. D. (2023) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-023-02902-y · Cited by 16 · see citing works
Liu, H., Huang, M., Lyu, J., Tao, J., Li, Y., Li, L., Huang, Y., & Zhou, Z. (2025) · ACS Nano · doi:10.1021/acsnano.4c13533 · Cited by 15 · see citing works
Self-citationHeating Induced Nanoparticle Migration and Enhanced Delivery in Tumor Treatment Using Nanotechnology
Gu, Q., & Zhu, L. K. (2024) · Bioengineering · doi:10.3390/bioengineering11090900 · Cited by 11 · see citing works
Li, Q., Sun, Y., Zhai, K., Geng, B., Dong, Z., Ji, L., Chen, H., & Cui, Y. (2024) · Physiological Genomics · doi:10.1152/physiolgenomics.00032.2024 · Cited by 11 · see citing works
Gong, T., Ullah, Z., Roy, S., Cheng, C., Li, M., Cheng, J., Zhang, Y., Guo, B., & Qiu, Y. (2025) · International Journal of Nanomedicine · doi:10.2147/ijn.s524454 · Cited by 10 · see citing works
Designing highly UV-emitting lanthanide nanoscintillators for in vivo X-ray-activated tumor therapy
Yang, K., Yang, Y., Sun, D., Li, S., Song, X., & Yang, H. (2023) · Science China Materials · doi:10.1007/s40843-023-2548-8 · Cited by 10 · see citing works
Self-citationWu, Z., Li, B., Qie, Y., Wu, S., Qi, F., Chu, T., Nie, G., & Hu, H. (2024) · Nano Letters · doi:10.1021/acs.nanolett.4c02485 · Cited by 9 · see citing works
Bio-inspired hierarchical particles for bioassays
Li, N., Chen, H., Xu, D., & Zhao, Y. (2023) · Biomedical Technology · doi:10.1016/j.bmt.2023.09.003 · Cited by 9 · see citing works
Yang, W., Wang, L., Lü, F., Li, W., Zhao, Y., Shang, L., & Jiang, M. (2023) · Small Methods · doi:10.1002/smtd.202301002 · Cited by 9 · see citing works
Zhang, W., Yu, B., Chen, X., Yan, M., Liu, Q., Liu, Y., Ni, Y., Cai, H., Yan, N., Kong, R., et al. (2024) · Small · doi:10.1002/smll.202309882 · Cited by 9 · see citing works
Self-citationSong, Z., Sun, Q., Yang, W., Li, Y., Hu, C., Chen, C., Liu, K., Shen, W. H., Yang, Y., & Yin, D. (2025) · Journal of Nanobiotechnology · doi:10.1186/s12951-025-03332-y · Cited by 8 · see citing works
Self-citationAdvanced biomaterials and delivery modalities to alleviate cancer therapy-induced inflammation
Huang, H., Ke, Q., Li, T., Yang, Z., Shen, J., Li, Z., Zeng, Q., Wei, X., Yang, H., Wang, D., et al. (2025) · Biomaterials · doi:10.1016/j.biomaterials.2025.123419 · Cited by 8 · see citing works
Wu, X., Li, B., Liao, H., Chen, X., Yu, X., Hu, J., Lin, Q., Cao, T., Xu, K., Zhou, Q., et al. (2025) · ACS Nano · doi:10.1021/acsnano.5c05274 · Cited by 8 · see citing works
TEP RNA: a new frontier for early diagnosis of NSCLC
Wang, Y., Dong, A., Jin, M., Li, S., & Duan, Y. (2024) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-024-05620-w · Cited by 7 · see citing works
Self-citationXing, Y., Zhang, Y., Li, J., Tang, Y., Zhang, J., Yang, R., Tang, H., Qian, H., Huang, D., Chen, W., et al. (2024) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.4c11686 · Cited by 7 · see citing works
Cai, Q., He, Y., Zhou, Y., Zheng, J., & Deng, J. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202303543 · Cited by 6 · see citing works
Engineered Platelets for Cancer Therapy
Zhang, K., Li, H., Ma, Z., Zhong, W., Yu, Y., & Zhao, Y. (2024) · Aggregate · doi:10.1002/agt2.704 · Cited by 6 · see citing works
Liu, X., Mao, Z., Yang, J., Zhu, Q., Dong, X., Huang, G., Shen, X., Zhang, L., & Yang, H. (2025) · Journal of Translational Medicine · doi:10.1186/s12967-025-07318-0 · Cited by 5 · see citing works
Hu, B., Lin, H., Quan, X., Sun, F., Zhang, F., Zhang, F., Wang, Y., Chang, Y., Wang, J., Duan, X., et al. (2025) · Biomaterials · doi:10.1016/j.biomaterials.2025.123380 · Cited by 5 · see citing works
Targeted nanostrategies eliminate pre-metastatic niche of cancer
Wang, J., Zhang, N., Ding, X., Fu, C., Li, X., Li, B., Ding, J., & Sun, T. (2024) · Nano Research · doi:10.1007/s12274-024-6412-0 · Cited by 5 · see citing works
Platelet-based bioactive systems guided precision targeting and immune regulation for cancer therapy
Cai, X., Qiu, L., Diao, Z., Cai, L., Yin, T., & Pan, H. (2024) · Nano Research · doi:10.1007/s12274-024-6777-0 · Cited by 5 · see citing works
Tumor-associated inflammation: The role and research progress in tumor therapy
Xu, J., Xu, X., Zhang, H., Wu, J., Pan, R., & Zhang, B. (2024) · Journal of Drug Delivery Science and Technology · doi:10.1016/j.jddst.2024.106376 · Cited by 4 · see citing works
Cheng, G., Yuan, S., Wang, J., Deng, S., Wu, Y., Wang, Y., Shen, Y., & Li, L. (2024) · Clinical & Translational Oncology · doi:10.1007/s12094-024-03781-1 · Cited by 4 · see citing works
Self-citationElectro-promoted radical-radical cross-coupling reaction to synthesize sulfonamides
Gong, H., Fu, H., Lu, C. T., & Cai, C. (2024) · Tetrahedron · doi:10.1016/j.tet.2024.134315 · Cited by 3 · see citing works
Ji, K., Jiang, X., Zhang, Z., Li, M., Zhu, P., Wang, Y., & Gao, J. (2025) · Biomaterials Research · doi:10.34133/bmr.0165 · Cited by 3 · see citing works
Emerging Strategies for Platelet‐Modified Nanoparticles in Targeted Tumor Therapy
Bai, C., Sun, L., Cui, Y., Meng, H., Li, J., & Xiang, Q. (2025) · Advanced NanoBiomed Research · doi:10.1002/anbr.202500082 · Cited by 3 · see citing works
Hu, Y., Hou, D., Wang, S., Wang, N., Wang, Q., Zhang, C., Chen, J., Su, X., & Yang, G. (2025) · Cell Death Discovery · doi:10.1038/s41420-025-02738-9 · Cited by 3 · see citing works
Zhang, Y., Sun, W., Xing, G., Zhu, D., Mei, L., Dong, X., & Lv, F. (2024) · Chemical Engineering Journal · doi:10.1016/j.cej.2024.157868 · Cited by 3 · see citing works
Inflamed lung-targeting nanoparticles hijack activated platelets to alleviate lung injury in sepsis
Yan, Y., Li, S., Chen, S., Zhou, Z., Li, L., & Huang, Y. (2024) · Nano Research · doi:10.26599/nr.2025.94907502 · Cited by 3 · see citing works
Self-citationLi, H., Liu, J., Yan, S., Rao, C., & Wang, L. (2023) · Cancer Management and Research · doi:10.2147/cmar.s408548 · Cited by 3 · see citing works
Inhalable Chemotactic Liposome for Targeted Modulation of Pulmonary Pre‐Metastatic Niche
Wang, Z., Liao, L., Wang, F., Shi, J., Liu, J., Zhou, R., Liu, M., Huang, Y., & Li, L. (2025) · Advanced Functional Materials · doi:10.1002/adfm.202419583 · Cited by 3 · see citing works
Self-citationNatural carrier systems in cancer vaccines and immunotherapy
Owliaee, I., Shoushtari, M. M., Karimi, Z., & Shojaeian, A. (2025) · Human Vaccines & Immunotherapeutics · doi:10.1080/21645515.2025.2535787 · Cited by 3 · see citing works
Redox-Responsive π-Conjugated Prodrug Nanoassemblies for Cancer Chemotherapy
Liu, S., Chen, L., Zhang, H., Wang, Y., & Luo, C. (2025) · Pharmaceutics · doi:10.3390/pharmaceutics17091162 · Cited by 2 · see citing works
Self-citationMo, Z., He, J., Li, M., Guo, R., & He, Q. (2024) · Pharmaceutical Fronts · doi:10.1055/s-0044-1786681 · Cited by 2 · see citing works
Potassium Ferric Oxalate Nanoparticles Prevent Human Blood Clotting and Thrombosis in a Mouse Model
Yenurkar, D., Choudhary, A., Shrivastava, A., Pragya, P., Mandal, S., Soni, P., Pradhan, L., Singh, A., Sarkar, A., & Mukherjee, S. (2025) · ACS Applied Materials & Interfaces · doi:10.1021/acsami.5c04112 · Cited by 2 · see citing works
Key processes in tumor metastasis and therapeutic strategies with nanocarriers: a review
Li, H., Huang, H., Tan, H., Jia, Q., Song, W., Zhang, Q., Zhou, B., & Bai, J. (2024) · Molecular Biology Reports · doi:10.1007/s11033-023-08910-7 · Cited by 2 · see citing works
Chen, W., Cai, C., Bing-zhong, G., Hong, W.-S., Xu, Y.-Z., & Cai, W.-J. (2025) · World Journal of Gastrointestinal Surgery · doi:10.4240/wjgs.v17.i12.110617 · Cited by 1 · see citing works
The unseen architects of metastasis: coagulation factors in pre-metastatic niche development
Huang, H., Lu, X., Liu, Y., Zhang, Y., Zhan, J., Zeng, W., Sun, C., Li, B., Zhang, Y., Wang, Q., et al. (2026) · Cell Communication and Signaling · doi:10.1186/s12964-026-02727-0 · Cited by 1 · see citing works
Liu, X., Zhao, Y., Cai, Y., Zhang, Y., Wang, X., Chen, Q., & Luo, L. (2026) · Advanced Healthcare Materials · doi:10.1002/adhm.70968 · Cited by 1 · see citing works
“Targeting platelets in breast cancer: Insights into pathophysiology and therapeutic strategies”
Moghaddasnejad, M. R., & Saki, N. (2026) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2026.105266 · Cited by 1 · see citing works
Gui, J., Zhu, Y., Chen, X., Gong, T., Zhang, Z., Yu, R., & Fu, Y. S. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4652646
Singh, C., & Gurudiwan, P. (2025) · Journal of cancer research updates · doi:10.30683/1929-2279.2025.14.12
Meng, C., Qiao, C., Hao, Q., Shi, J., Lou, C., Song, J., Wang, L., Yang, J., Ma, X., Kang, H., et al. (2025) · Advanced Functional Materials · doi:10.1002/adfm.202516391
Self-citationZhang, C., Chen, Q., Zhang, S., Sun, Y., Li, J., Chen, Y., Zhang, L., Pan, Y., & Fan, W. (2025) · Materials Today · doi:10.1016/j.mattod.2025.11.013
Zhang, B., Hua, Y., Wen, X. R., Liao, Z., Ren, J., Weng, Y., & Wang, Q. (2025) · Advanced Science · doi:10.1002/advs.202518005
Ciummo, S. L., Sorrentino, C., Fieni, C., & Carlo, E. D. (2023) · Figshare · doi:10.6084/m9.figshare.24797842
Stimuli-Responsive Lipid Nanoparticles for Cancer Therapy
Umeyor, C. E., Negi, P., Andrew, E. C., Bairagi, G., & Patravale, V. B. (2026) · Springer eBooks · doi:10.1007/978-981-95-2744-1_7
Li, J., Wen, X. R., Zhang, B., Ren, J., Liao, Z. J., Hua, Y., Li, X., & Wang, Q. (2026) · Advanced Functional Materials · doi:10.1002/adfm.202516787
Cancer cell-platelet interactions: Harnessing therapeutic opportunities in cancer treatment
Jain, S., & Rao, G. S. N. K. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-27731-3.00013-9
Huang, J., Chen, W., Huang, Z., Huang, W., Lu, Y., Jiang, H., Chen, X., Wang, S., & Zhu, Y. (2026) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2026.101776
Pan, H., Yang, J., Fu, J., Yan, S., Yan, Y., Xu, Y., Zhou, M., Li, L., & Xiang, Y. (2026) · Pharmaceutics · doi:10.3390/pharmaceutics18091070
Self-citation
- Authors
- Li, S., Li, L., Lin, X., Chen, C., Luo, C., & Huang, Y.
- Affiliations
- Sichuan University (CN)
- Corresponding author
- Huang, Yuan
- Venue
- ACS Nano
- Publisher
- American Chemical Society (ACS)
- Published
- 2021-12-07
- Volume
- 16
- Issue
- 1
- Pages
- 50-67
- ISSN
- 1936-0851 (ISSN-L)
- 1936-086X
- OpenAlex
- W4200265423
- Cited by
- 78
- References
- 87
- Citations by year
- 2026: 8 · 2025: 22 · 2024: 27 · 2023: 18 · 2022: 3
- FWCI
- 3.13
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- Locations
- ACS Nano (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Natural Science Foundation of China (81625023)
- Topics
- Physical Sciences › Materials Science › Biomaterials › Nanoparticle-Based Drug Delivery
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Engineering › Biomedical Engineering › Nanoplatforms for cancer theranostics
- Keywords
- metastasis, pre-metastatic niche, tumor inflammation, epithelial-mesenchymal transition, lung metastasis, abscopal effect, disseminated tumor cells, nanoparticle drug delivery
- MeSH terms
- Blood Platelets, Humans, Inflammation, Neoplasm Metastasis, Neoplasms, Nanoparticles, Epithelial-Mesenchymal Transition, Tumor Microenvironment
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