Hypoxic BMSC-derived exosomal miRNAs promote metastasis of lung cancer cells via STAT3-induced EMT
Open accessAbstract
BACKGROUND: Metastasis is the main cause of lung cancer mortality. Bone marrow-derived mesenchymal stem cells (BMSCs) are a component of the cancer microenvironment and contribute to cancer progression. Intratumoral hypoxia affects both cancer and stromal cells. Exosomes are recognized as mediators of intercellular communication. Here, we aim to further elucidate the communication between BMSC-derived exosomes and cancer cells in the hypoxic niche. METHODS: Exosomal miRNA profiling was performed using a microRNA array. Lung cancer cells and an in vivo mouse syngeneic tumor model were used to evaluate the effects of select exosomal microRNAs. Hypoxic BMSC-derived plasma exosomal miRNAs were assessed for their capacity to discriminate between cancer patients and non-cancerous controls and between cancer patients with or without metastasis. RESULTS: We demonstrate that exosomes derived from hypoxic BMSCs are taken by neighboring cancer cells and promote cancer cell invasion and EMT. Exosome-mediated transfer of select microRNAs, including miR-193a-3p, miR-210-3p and miR-5100, from BMSCs to epithelial cancer cells activates STAT3 signaling and increases the expression of mesenchymal related molecules. The diagnostic accuracy of individual microRNA showed that plasma exosomal miR-193a-3p can discriminate cancer patients from non-cancerous controls. A panel of these three plasma exosomal microRNAs showed a better diagnostic accuracy to discriminate lung cancer patients with or without metastasis than individual exosomal microRNA. CONCLUSIONS: Exosome-mediated transfer of miR-193a-3p, miR-210-3p and miR-5100, could promote invasion of lung cancer cells by activating STAT3 signalling-induced EMT. These exosomal miRNAs may be promising noninvasive biomarkers for cancer progression.
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Exosome microRNAs from hypoxic BMSCs have been identified as a new biomarker for lung cancer progression.
“which has been identified as a new biomarker for lung cancer progression [114].”
From The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System (2022) · cites this paper as [114]
Exosome microRNAs from hypoxic BMSCs were selectively taken up by lung cancer cells and could activate STAT3 signaling to induce epithelial-mesenchymal transition to promote invasion of lung cancer cells.
“Similarly, Zhang et al. showed that exosome microRNAs (such as miR-193a-3p, miR-210-3p, and miR-5100) from hypoxic BMSCs were selectively taken up by lung cancer cells and could activate STAT3 signaling to induce epithelial–mesenchymal transition (EMT) to promote the invasion of lung cancer cells, which has been identified as a new biomarker for lung cancer progression [114].”
From The Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System (2022) · cites this paper as [114]
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Cites
Arroyo, J. D., Chevillet, J. R., Kroh, E. M., Ruf, I. K., Pritchard, C. C., Gibson, D. F., Mitchell, P. S., Bennett, C. F., Pogosova-Agadjanyan, E. L., Stirewalt, D. L., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1019055108 · Cited by 3,294 · see citing works
Targeting hypoxia in cancer therapy
Wilson, W. R., & Hay, M. P. (2011) · Nature Reviews Cancer · doi:10.1038/nrc3064 · Cited by 3,172 · see citing works
Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer
Kamerkar, S., LeBleu, V. S., Sugimoto, H., Yang, S., Ruivo, C. F., Melo, S. A., Lee, J. J., & Kalluri, R. (2017) · Nature · doi:10.1038/nature22341 · Cited by 2,639 · see citing works
Exosome and Exosomal MicroRNA: Trafficking, Sorting, and Function
Zhang, J., Li, S., Li, L., Li, M., Guo, C., Yao, J., & Mi, S. (2015) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2015.02.001 · Cited by 2,189 · see citing works
Hypoxia signalling in cancer and approaches to enforce tumour regression
Pouysségur, J., Dayan, F., & Mazure, N. M. (2006) · Nature · doi:10.1038/nature04871 · Cited by 1,676 · see citing works
MicroRNAs in Stress Signaling and Human Disease
Mendell, J. T., & Olson, E. N. (2012) · Cell · doi:10.1016/j.cell.2012.02.005 · Cited by 1,673 · see citing works
Kroh, E. M., Parkin, R. K., Mitchell, P. S., & Tewari, M. (2010) · Methods · doi:10.1016/j.ymeth.2010.01.032 · Cited by 1,177 · see citing works
Hypoxic enhancement of exosome release by breast cancer cells
King, H. W., Michael, M. Z., & Gleadle, J. M. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-421 · Cited by 1,045 · see citing works
Sorting it out: Regulation of exosome loading
Villarroya‐Beltri, C., Baixauli, F., Gutiérrez‐Vázquez, C., Sánchez‐Madrid, F., & Mittelbrunn, M. (2014) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2014.04.009 · Cited by 745 · see citing works
Exosome-delivered microRNAs modulate the inflammatory response to endotoxin
Alexander, M., Hu, R., Runtsch, M. C., Kagele, D. A., Mosbruger, T. L., Tolmachova, T., Seabra, M. C., Round, J. L., Ward, D. M., & O’Connell, R. M. (2015) · Nature Communications · doi:10.1038/ncomms8321 · Cited by 707 · see citing works
Endogenous RNAs modulate microRNA sorting to exosomes and transfer to acceptor cells.
Squadrito, M. L., Baer, C., Burdet, F., Maderna, C., Gilfillan, G. D., Lyle, R., Ibberson, M., & De Palma, M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.035 · Cited by 565 · see citing works
Guduric‐Fuchs, J., O’Connor, A., Camp, B., O’Neill, C. L., Medina, R. J., & Simpson, D. A. C. (2012) · BMC Genomics · doi:10.1186/1471-2164-13-357 · Cited by 554 · see citing works
Isolation and Characterization of RNA-Containing Exosomes
Lässer, C., Eldh, M., & Lötvall, J. (2012) · Journal of Visualized Experiments · doi:10.3791/3037 · Cited by 509 · see citing works
The hematopoietic stem cell niche: Low in oxygen but a nice place to be
Eliasson, P., & Jönsson, J. (2009) · Journal of Cellular Physiology · doi:10.1002/jcp.21908 · Cited by 473 · see citing works
Xu, W., Zhang, X., Qian, H., Zhu, W., Sun, X., Hu, J., Zhou, H., & Chen, Y. (2004) · Experimental Biology and Medicine · doi:10.1177/153537020422900706 · Cited by 371 · see citing works
Self-citationFang, J., Zhang, Z., Shang, L., Luo, Y., Lin, Y., Yuan, Y., & Zhuang, S. (2018) · Hepatology · doi:10.1002/hep.29920 · Cited by 335 · see citing works
Activity-associated miRNA are packaged in Map1b-enriched exosomes released from depolarized neurons
Goldie, B. J., Dun, M. D., Lin, M., Smith, N. D., Verrills, N. M., Dayas, C. V., & Cairns, M. J. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku594 · Cited by 294 · see citing works
Li, X. J., Ren, Z. J., Tang, J. H., & Yu, Q. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000485780 · Cited by 268 · see citing works
Self-citationZhu, J., Lü, K., Zhang, N., Zhao, Y. F., Ma, Q., Shen, J., Lin, Y., Xiang, P., Tang, Y., Hu, X., et al. (2017) · Artificial Cells Nanomedicine and Biotechnology · doi:10.1080/21691401.2017.1388249 · Cited by 264 · see citing works
Ren, D., Yang, Q., Dai, Y., Guo, W., Du, H., Song, L., & Peng, X. (2017) · Molecular Cancer · doi:10.1186/s12943-017-0688-6 · Cited by 234 · see citing works
Exosomes Packaging APOBEC3G Confer Human Immunodeficiency Virus Resistance to Recipient Cells
Khatua, A. K., Taylor, H. E., Hildreth, J. E. K., & Popik, W. (2008) · Journal of Virology · doi:10.1128/jvi.01658-08 · Cited by 177 · see citing works
Wu, H., Zhou, J., Mei, S., Wu, D., Mu, Z., Chen, B., Xie, Y., Ye, Y., & Liu, J. (2016) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.13056 · Cited by 173 · see citing works
Systemically Circulating Viral and Tumor-Derived MicroRNAs in KSHV-Associated Malignancies
Chugh, P., Sin, S., Özgür, S., Henry, D. H., Menezes, P., Griffith, J. D., Eron, J. J., Damania, B., & Dittmer, D. P. (2013) · PLoS Pathogens · doi:10.1371/journal.ppat.1003484 · Cited by 171 · see citing works
Vallabhajosyula, P., Korutla, L., Habertheuer, A., Yu, M., Rostami, S. Y., Yuan, C., Reddy, S., Liu, C., Korutla, V., Koeberlein, B., et al. (2017) · Journal of Clinical Investigation · doi:10.1172/jci87993 · Cited by 163 · see citing works
Qu, Z., Wu, J., Wu, J., Luo, D., Jiang, C., & Ding, Y. (2016) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-016-0430-z · Cited by 156 · see citing works
Cai, Q., Zhu, A., & Gong, L. (2018) · Bulletin du Cancer · doi:10.1016/j.bulcan.2018.05.003 · Cited by 116 · see citing works
Activation of neutral sphingomyelinase is involved in acute hypoxic pulmonary vasoconstriction
Cogolludo, A. L., Moreno, L., Frazziano, G., Moral‐Sanz, J., Menendez, C., Castaneda, J., González, C., Villamor, E., & Pérez‐Vizcaíno, F. (2008) · Cardiovascular Research · doi:10.1093/cvr/cvn349 · Cited by 111 · see citing works
Exosomes: a new horizon in lung cancer
Vanni, I., Alama, A., Grossi, F., Bello, M. G. D., & Coco, S. (2017) · Drug Discovery Today · doi:10.1016/j.drudis.2017.03.004 · Cited by 98 · see citing works
Wong, N. W., Khwaja, S. S., Baker, C. M., Gay, H. A., Thorstad, W. L., Daly, M. D., Lewis, J. S., & Wang, X. (2016) · Cancer Medicine · doi:10.1002/cam4.718 · Cited by 82 · see citing works
Hu, X., Wu, R., Shehadeh, L. A., Zhou, Q., Jiang, C., Huang, X., Zhang, L., Gao, F., Liu, X., Yu, H., et al. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-303 · Cited by 81 · see citing works
Bowler, E., Porazinski, S. R., Uzor, S., Thibault, P., Durand, M., Lapointe, E., Rouschop, K. M. A., Hancock, J. T., Wilson, I. D., & Ladomery, M. (2018) · BMC Cancer · doi:10.1186/s12885-018-4227-7 · Cited by 81 · see citing works
Urinary exosome miR-146a is a potential marker of albuminuria in essential hypertension
Perez-Hernandez, J., Olivares, D. A., Forner, M. J., Ortega, A., Solaz, E., Martínez, F., Chaves, F. J., Redón, J., & Cortés, R. (2018) · Journal of Translational Medicine · doi:10.1186/s12967-018-1604-6 · Cited by 79 · see citing works
Betulinic acid impairs metastasis and reduces immunosuppressive cells in breast cancer models
Zeng, A., Yu, Y., Yao, Y.-Q., Yang, F.-F., Liao, M., Song, L.-J., Li, Y.-L., Yu, Y., Li, Y., Zeng, C., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.23376 · Cited by 72 · see citing works
Chen, J., Sun, J., Dai, Y., Cao, P., Zhang, L., Peng, S., Zhou, Y., Li, G., Tang, J., & Xiang, J. (2015) · Stem Cell Research & Therapy · doi:10.1186/s13287-015-0014-4 · Cited by 70 · see citing works
Self-citationKim, J. E., Eom, J. S., Kim, W., Jo, E. J., Mok, J., Lee, K., Kim, K. U., Park, H., Lee, M. K., & Kim, M. (2018) · Thoracic Cancer · doi:10.1111/1759-7714.12756 · Cited by 69 · see citing works
MiR-193a-3p is an Important Tumour Suppressor in Lung Cancer and Directly Targets KRAS
Fan, Q., Hu, X., Zhang, H., Wang, S., Zhang, H., You, C., Zhang, C.-Y., Liang, H., Chen, X., & Ba, Y. (2017) · Cellular Physiology and Biochemistry · doi:10.1159/000485491 · Cited by 63 · see citing works
Secreted miR-210-3p as non-invasive biomarker in clear cell renal cell carcinoma
Petrozza, V., Pastore, A. L., Palleschi, G., Tito, C., Porta, N., Ricci, S., Marigliano, C., Costantini, M., Simone, G., Carlo, A. D., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.18449 · Cited by 56 · see citing works
Pan, Y., Hu, J., Ma, J., Qi, X., Zhou, H., Miao, X., Zheng, W., & Li, J. (2018) · Molecular Carcinogenesis · doi:10.1002/mc.22826 · Cited by 54 · see citing works
Zhang, Z., Xu, J., Fu, Y., Liu, J., Jiang, Y., Cui, H., Zhao, B., Sun, H., He, Y.-W., Li, Q.-J., et al. (2013) · Clinical Chemistry · doi:10.1373/clinchem.2012.197335 · Cited by 51 · see citing works
Identification and analysis of exosomes secreted from macrophages extracted by different methods.
Wang, J., Yao, Y., Wu, J., & Li, G. (2015) · Europe PMC (PubMed Central) · Cited by 50 · see citing works
Self-citationYang, X., Shi, L., Yi, C., Yang, Y., Chang, L., & Song, D. (2017) · PubMed Central · Cited by 48 · see citing works
The relationship between microRNAs and the STAT3-related signaling pathway in cancer
Zhang, L., Li, J., Wang, Q., Meng, G., Lv, X., Zhou, H., Li, W., & Zhang, J. (2017) · Tumor Biology · doi:10.1177/1010428317719869 · Cited by 46 · see citing works
Purification and microRNA Profiling of Exosomes Derived from Blood and Culture Media
McDonald, M. K., Capasso, K. E., & Ajit, S. K. (2013) · Journal of Visualized Experiments · doi:10.3791/50294 · Cited by 45 · see citing works
Liu, L., Li, Y., Liu, S., Duan, Q., Chen, L., Wu, T., Qian, H., Yang, S., & Xin, D. (2017) · Tumor Biology · doi:10.1177/1010428317711951 · Cited by 44 · see citing works
Zhang, X., Xin, G., & Sun, D. (2018) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2018.6458 · Cited by 39 · see citing works
Self-citationElevation of Circulating miR-210-3p in High-Altitude Hypoxic Environment
Yan, Y., Wang, C., Zhou, W., Shi, Y., Guo, P.-T., Liu, Y., Wang, J., Zhang, C., & Zhang, C. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00084 · Cited by 36 · see citing works
Clinical and biological significance of miR-193a-3p targeted KRAS in colorectal cancer pathogenesis
Mamoori, A., Wahab, R., Islam, F., Lee, K. T., Vider, J., Lu, C., Gopalan, V., & Lam, A. K.-Y. (2017) · Human Pathology · doi:10.1016/j.humpath.2017.10.024 · Cited by 31 · see citing works
Block, I., Burton, M., Sørensen, K. P., Andersen, L. I., Larsen, M. J., Bak, M., Cold, S., Thomassen, M., Tan, Q., & Kruse, T. A. (2018) · Oncotarget · doi:10.18632/oncotarget.24088 · Cited by 29 · see citing works
Jorge, K. T. D. O. S., de Souza, R. P., Assis, M. T. A., Araújo, M. G., Locati, M., de Jesus, A. R., Baptista, I. M. F. D., Lima, C. X., Teixeira, A. L., Teixeira, M. M., et al. (2017) · Journal of Clinical Microbiology · doi:10.1128/jcm.02408-16 · Cited by 26 · see citing works
Decreased expression of miR-193a-3p is associated with poor prognosis in colorectal cancer
Lin, M., Duan, B., Hu, J., Yu, H., Sheng, H., Gao, H., & Huang, J. (2017) · Oncology Letters · doi:10.3892/ol.2017.6266 · Cited by 26 · see citing works
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- [23]Fang JH Zhang ZJ Shang LR Luo YW Lin YF Yuan Y Hepatoma cell-secreted exosomal microRNA-103 increases vascular permeability and promotes metastasis by targeting junction proteins Hepatology 2018 68 4 1459 1475 10.1002/hep.29920 29637568 · DOI
Cited by
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Exosomes: key players in cancer and potential therapeutic strategy
Dai, J., Su, Y., Zhong, S., Cong, L., Liu, B., Yang, J., Tao, Y., He, Z., Chen, C., & Jiang, Y. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00261-0 · Cited by 1,186 · see citing works
Targeting STAT3 in Cancer Immunotherapy
Zou, S., Tong, Q., Liu, B., Huang, W., Tian, Y., & Fu, X. (2020) · Molecular Cancer · doi:10.1186/s12943-020-01258-7 · Cited by 1,075 · see citing works
miRNA-based biomarkers, therapies, and resistance in Cancer
He, B., Zhao, Z., Cai, Q., Zhang, Y., Zhang, P., Shi, S., Xie, H., Peng, X., Yin, W., Tao, Y., et al. (2020) · International Journal of Biological Sciences · doi:10.7150/ijbs.47203 · Cited by 632 · see citing works
The biology, function, and applications of exosomes in cancer
Liu, J., Ren, L., Li, S., Li, W., Zheng, X., Yang, Y., Fu, W., Yi, J., Wang, J., & Du, G. (2021) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2021.01.001 · Cited by 564 · see citing works
Liu, W., Li, L., Rong, Y., Qian, D., Chen, J., Zhou, Z. Y., Luo, Y., Jiang, D., Cheng, L., Zhao, S., et al. (2019) · Acta Biomaterialia · doi:10.1016/j.actbio.2019.12.020 · Cited by 473 · see citing works
Self-citationRoles and mechanisms of exosomal non-coding RNAs in human health and diseases
Li, C., Ni, Y., Xu, H., Xiang, Q., Zhao, Y. Q., Zhan, J., He, J., Li, S., & Liu, Y. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00779-x · Cited by 407 · see citing works
Unraveling the complexity of STAT3 in cancer: molecular understanding and drug discovery
Hu, Y., Dong, Z., & Liu, K. (2024) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-024-02949-5 · Cited by 288 · see citing works
Emerging role of tumor cell plasticity in modifying therapeutic response
Qin, S., Jiang, J., Lü, Y., Nice, E. C., Huang, C., Zhang, J., & He, W. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-00313-5 · Cited by 274 · see citing works
Kong, J., Tian, H., Zhang, F., Zhang, Z., Li, J., Liu, X., Li, X., Liu, J., Li, X., Jin, D., et al. (2019) · Molecular Cancer · doi:10.1186/s12943-019-1101-4 · Cited by 239 · see citing works
Chu, D., Nguyen, T. T. P., Tien, N. L. B., Khoa, T. D., Thanh, V. V., Quang, T. L., Truong, D. T., Pham, V.-H., Ngọc, V. T. N., Chu-Dinh, T., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21030708 · Cited by 239 · see citing works
Emerging roles of exosomal miRNAs in diabetes mellitus
He, X., Kuang, G., Wu, Y., & Ou, C. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.468 · Cited by 232 · see citing works
Wang, D., Zhao, C., Xu, F., Zhang, A., Jin, M., Zhang, K., Liu, L., Hua, Q., Zhao, J., Liu, J., et al. (2021) · Theranostics · doi:10.7150/thno.51797 · Cited by 228 · see citing works
Exosomes: Small vesicles with big roles in cancer, vaccine development, and therapeutics
Thakur, A., Parra, D. C., Motallebnejad, P., Brocchi, M., & Chen, H. J. (2021) · Bioactive Materials · doi:10.1016/j.bioactmat.2021.08.029 · Cited by 223 · see citing works
Hypoxia and extracellular vesicles: A review on methods, vesicular cargo and functions
Korvenlaita, N., Pistono, C., Huremagic, B., Jolkkonen, J., Giugno, R., & Malm, T. (2020) · Journal of Extracellular Vesicles · doi:10.1002/jev2.12002 · Cited by 219 · see citing works
Hu, W., Liu, C., Bi, Z., Zhou, Q. Y., Zhang, H., Li, L., Zhang, J., Zhu, W., Song, Y., Zhang, F., et al. (2020) · Molecular Cancer · doi:10.1186/s12943-020-01199-1 · Cited by 215 · see citing works
Treatment of inflammatory bone loss in periodontitis by stem cell-derived exosomes
Lei, F., Li, M., Lin, T., Zhou, H., Wang, F., & Su, X. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.12.035 · Cited by 213 · see citing works
Self-citationTumor-associated exosomes promote lung cancer metastasis through multiple mechanisms
Jiang, C., Zhang, N., Hu, X., & Wang, H. (2021) · Molecular Cancer · doi:10.1186/s12943-021-01411-w · Cited by 210 · see citing works
The metastasizing mechanisms of lung cancer: Recent advances and therapeutic challenges
Xie, S., Wu, Z., Qi, Y., Wu, B., & Zhu, X. M. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111450 · Cited by 202 · see citing works
Exosomes in the hypoxic TME: from release, uptake and biofunctions to clinical applications
He, G., Peng, X., Wei, S., Yang, S., Li, X., Huang, M., Tang, S., Jin, H., Liu, J., Zhang, S., et al. (2022) · Molecular Cancer · doi:10.1186/s12943-021-01440-5 · Cited by 201 · see citing works
The roles of exosomal miRNAs and lncRNAs in lung diseases
Yang, L., Yin, Z., Fan, J., Zhang, S., & Yang, W.-B. (2019) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-019-0080-7 · Cited by 189 · see citing works
Kumar, A., & Deep, G. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.03.017 · Cited by 186 · see citing works
STAT3-EMT axis in tumors: Modulation of cancer metastasis, stemness and therapy response
Sadrkhanloo, M., Entezari, M., Orouei, S., Ghollasi, M., Fathi, N., Rezaei, S., Hejazi, E. S., Kakavand, A., Saebfar, H., Hashemi, M., et al. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106311 · Cited by 188 · see citing works
The role of exosomes in liquid biopsy for cancer diagnosis and prognosis prediction
Li, S., Yi, M., Dong, B., Tan, X., Luo, S., & Wu, K. (2020) · International Journal of Cancer · doi:10.1002/ijc.33386 · Cited by 181 · see citing works
Progress of exosomes in the diagnosis and treatment of lung cancer
Xu, K., Zhang, C., Du, T., Gabriel, A. N. A., Wang, X., Li, X., Sun, L. J., Wang, N., Jiang, X., & Zhang, Y. (2020) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2020.111111 · Cited by 180 · see citing works
Ding, J., Zhang, Y., Cai, X., Zhang, Y., Yan, S., Wang, J., Zhang, S., Yin, T., Yang, C., & Yang, J. (2021) · Theranostics · doi:10.7150/thno.58731 · Cited by 170 · see citing works
Xiong, Y., Chen, L., Yan, C., Zhou, W., Tao, Y., Sun, Y. T., Cao, F., Xue, H., Hu, Y., Chen, D., et al. (2020) · Journal of Nanobiotechnology · doi:10.1186/s12951-020-00622-5 · Cited by 164 · see citing works
RetractedRole of exosomal microRNAs in lung cancer biology and clinical applications
Hu, C., Meiners, S., Lukas, C., Stathopoulos, G. T., & Chen, J. (2020) · Cell Proliferation · doi:10.1111/cpr.12828 · Cited by 153 · see citing works
Wu, X., Zhou, Z., Xu, S., Liao, C., Chen, X., Li, B., Peng, J., Li, D., & Yang, L. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.03.004 · Cited by 145 · see citing works
Wu, H., Mu, X., Liu, L., Hu, X., Hu, X., Chen, L., Liu, J., Mu, Y., Yuan, F., Liu, W., et al. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-02962-4 · Cited by 145 · see citing works
The epithelial–mesenchymal plasticity landscape: principles of design and mechanisms of regulation
Haerinck, J., Goossens, S., & Berx, G. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00601-0 · Cited by 138 · see citing works
Extracellular Vesicles in Cancer Drug Resistance: Roles, Mechanisms, and Implications
Yang, Q., Xu, J. B., Gu, J., Shi, H., Zhang, J., Zhang, J., Chen, Z., Fang, X., Zhu, T., & Zhang, X. (2022) · Advanced Science · doi:10.1002/advs.202201609 · Cited by 142 · see citing works
Self-citationZhang, H., Wang, J., Ren, T., Huang, Y., Liang, X., Yu, Y., Wang, W., Niu, J., & Guo, W. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.07.008 · Cited by 136 · see citing works
Extracellular vesicles and particles impact the systemic landscape of cancer
Lucotti, S., Kenific, C. M., Zhang, H., & Lyden, D. C. (2022) · The EMBO Journal · doi:10.15252/embj.2021109288 · Cited by 134 · see citing works
Mesenchymal stem cell-derived exosome: A tumor regulator and carrier for targeted tumor therapy
Zhang, F., Guo, J. J., Zhang, Z., Qian, Y., Wang, G., Duan, M., Zhao, H., Yang, Z., & Jiang, X. (2021) · Cancer Letters · doi:10.1016/j.canlet.2021.11.015 · Cited by 133 · see citing works
CircOGDH Is a Penumbra Biomarker and Therapeutic Target in Acute Ischemic Stroke
Liu, Y., Li, Y., Zhang, T., Zhang, T., Li, Y., Tan, Z., Ma, D., Zhang, Y., Wang, S., Zhang, Y., et al. (2022) · Circulation Research · doi:10.1161/circresaha.121.319412 · Cited by 131 · see citing works
Hypoxia Induced Changes of Exosome Cargo and Subsequent Biological Effects
Jiang, H., Zhao, H., Zhang, M., He, Y., Li, X., Xu, Y., & Liu, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.824188 · Cited by 128 · see citing works
Dou, R., Liu, K., Yang, C., Zheng, J., Shi, D., Lin, X., Chen, W., Zhang, C., Fang, Y., Huang, S., et al. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.595 · Cited by 124 · see citing works
Du, Y., Wei, N., Ma, R., Jiang, S., & Song, D. (2020) · Cell Death and Disease · doi:10.1038/s41419-020-02952-6 · Cited by 121 · see citing works
Zhuang, Y., Cheng, M., Li, M., Cui, J., Huang, J., Zhang, C., Si, J., Lin, K., & Yu, H. (2022) · Acta Biomaterialia · doi:10.1016/j.actbio.2022.07.015 · Cited by 118 · see citing works
Zhao, W., Qin, P., Zhang, D., Cui, X., Gao, J., Yu, Z., Chai, Y., Wang, J., & Li, J. (2019) · Aging · doi:10.18632/aging.102406 · Cited by 115 · see citing works
Role of Exosomal miRNAs and the Tumor Microenvironment in Drug Resistance
dos Santos, P. W. D. S., & Almeida, F. B. D. R. (2020) · Cells · doi:10.3390/cells9061450 · Cited by 112 · see citing works
Yang, F., Yan, Y., Yang, Y., Hong, X., Wang, M., Yang, Z., Liu, B., & Ye, L. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2020.109675 · Cited by 110 · see citing works
RetractedThe Therapeutic Potential and Clinical Significance of Exosomes as Carriers of Drug Delivery System
Li, T., Li, X., Han, G., Liang, M., Yang, Z., Zhang, C., Huang, S., Tai, S., & Yu, S. (2022) · Pharmaceutics · doi:10.3390/pharmaceutics15010021 · Cited by 110 · see citing works
Entezari, M., Ghanbarirad, M., Taheriazam, A., Sadrkhanloo, M., Zabolian, A., Goharrizi, M. A. S. B., Hushmandi, K., Aref, A. R., Ashrafizadeh, M., Zarrabi, A., et al. (2022) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2022.112963 · Cited by 107 · see citing works
Li, P., Liu, S., Du, L., Mohseni, G., Zhang, Y., & Wang, C. (2022) · Clinical Epigenetics · doi:10.1186/s13148-022-01337-0 · Cited by 106 · see citing works
Wang, L., He, J., Hu, H., Tu, L., Sun, Z., Liu, Y., & Luo, F. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15274 · Cited by 100 · see citing works
Self-citationRole and Function of O-GlcNAcylation in Cancer
Lee, J. B., Pyo, K., & Kim, H. R. (2021) · Cancers · doi:10.3390/cancers13215365 · Cited by 100 · see citing works
Liu, H., Liu, Y., Sun, P., Leng, K., Xu, Y., Mei, L., Han, P., Zhang, B., Yao, K., Li, C., et al. (2020) · Clinical Science · doi:10.1042/cs20191087 · Cited by 99 · see citing works
Xiong, Y., Chen, L., Yan, C., Zhou, W., Yu, T., Sun, Y. T., Cao, F., Xue, H., Hu, Y., Dong, C., et al. (2021) · Journal of Nanobiotechnology · doi:10.1186/s12951-021-00828-1 · Cited by 99 · see citing works
Pulido-Escribano, V., Torrecillas-Baena, B., Camacho-Cardeñosa, M., Dorado, G., Gálvez-Moreno, M. Á., & Casado‐Díaz, A. (2022) · World Journal of Stem Cells · doi:10.4252/wjsc.v14.i7.453 · Cited by 100 · see citing works
Current progress and mechanisms of bone metastasis in lung cancer: a narrative review
Wu, S., Pan, Y., Mao, Y., Chen, Y., & He, Y. (2021) · Translational Lung Cancer Research · doi:10.21037/tlcr-20-835 · Cited by 92 · see citing works
Targeted extracellular vesicle delivery systems employing superparamagnetic iron oxide nanoparticles
Zhuo, Z., Wang, J., Luo, Y., Zeng, R., Zhang, C., Zhou, W., Guo, K., Wu, H., Sha, W., & Chen, H. H. (2021) · Acta Biomaterialia · doi:10.1016/j.actbio.2021.07.027 · Cited by 93 · see citing works
Jiang, D., Wu, X., Sun, X., Tan, W., Dai, X. J., Xie, Y., Du, A., & Zhao, Q. (2022) · Journal of Nanobiotechnology · doi:10.1186/s12951-021-01206-7 · Cited by 90 · see citing works
RetractedExosomes in hypoxia-induced remodeling of the tumor microenvironment
Kumar, A., & Deep, G. (2020) · Cancer Letters · doi:10.1016/j.canlet.2020.05.018 · Cited by 89 · see citing works
Wang, K., Ru, J., Zhang, H., Chen, J., Lin, X., Lin, Z., Wen, M., Huang, L., Ni, H., Zhuge, Q., et al. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.00848 · Cited by 87 · see citing works
The role of exosomes in lung cancer metastasis and clinical applications: an updated review
Yin, L., Liu, X., Shao, X., Feng, T., Xu, J., Wang, Q., & Hua, S. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-02985-1 · Cited by 87 · see citing works
Lei, B., Wang, D., Zhang, M., Deng, Y., Jiang, H., & Li, Y. (2020) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-020-01571-5 · Cited by 85 · see citing works
Zhan, Y., Du, J.-X., Min, Z., Ma, L., Zhang, W., Zhu, W., & Liu, Y. (2021) · Cell Death Discovery · doi:10.1038/s41420-021-00506-z · Cited by 84 · see citing works
Targeting STAT3 inhibition to reverse cisplatin resistance
Sun, C., Nie, J., Huang, J.-P., Zheng, G., & Feng, B. (2019) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2019.109135 · Cited by 83 · see citing works
Extracellular vesicles in cancer´s communication: messages we can read and how to answer
Semerádtová, A., Liegertová, M., Herma, R., Čapková, M., Brignole, C., & Zotto, G. D. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02282-1 · Cited by 89 · see citing works
Non-coding RNAs shuttled via exosomes reshape the hypoxic tumor microenvironment
Wang, W., Han, Y., Jo, H. A., Lee, J., & Song, Y. S. (2020) · Journal of Hematology & Oncology · doi:10.1186/s13045-020-00893-3 · Cited by 80 · see citing works
Luo, Z., Sun, Y., Qi, B., Lin, J., Chen, Y., Xu, Y., & Chen, J. (2022) · Bioactive Materials · doi:10.1016/j.bioactmat.2022.01.016 · Cited by 81 · see citing works
Exosomes and organ-specific metastasis
Zhao, L., Ma, X., & Yu, J. (2021) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2021.05.016 · Cited by 81 · see citing works
Potential therapeutic effects of milk-derived exosomes on intestinal diseases
Cui, Z., Amevor, F. K., Zhao, X., Mou, C., Pang, J., Peng, X., Liu, A., Lan, X., & Liu, L. (2023) · Journal of Nanobiotechnology · doi:10.1186/s12951-023-02176-8 · Cited by 80 · see citing works
Wang, Y., Zhao, R., Shen, C., Liu, W., Yuan, J., Li, C., Deng, W., Wang, Z., Zhang, W., Ge, J., et al. (2020) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2020/8418407 · Cited by 79 · see citing works
Self-citationHuang, Y., Kanada, M., Ye, J.-X., Deng, Y., He, Q., Lei, Z., Chen, Y., Li, Y., Qin, P.-W., Zhang, J., et al. (2022) · Cancer Letters · doi:10.1016/j.canlet.2022.215796 · Cited by 77 · see citing works
Extracellular vesicles set the stage for brain plasticity and recovery by multimodal signalling
Hermann, D. M., Peruzzotti‐Jametti, L., Giebel, B., & Pluchino, S. (2023) · Brain · doi:10.1093/brain/awad332 · Cited by 75 · see citing works
The Long and Short of It: The Emerging Roles of Non-Coding RNA in Small Extracellular Vesicles
Abramowicz, A., & Story, M. D. (2020) · Cancers · doi:10.3390/cancers12061445 · Cited by 76 · see citing works
Exosomal miRNAs: the tumor's trojan horse in selective metastasis
Bayat, M., & Nahand, J. S. (2024) · Molecular Cancer · doi:10.1186/s12943-024-02081-0 · Cited by 77 · see citing works
Exosome-Mediated Crosstalk Between Tumor and Tumor-Associated Macrophages
Chen, Q., Li, Y., Gao, W., Chen, L., Xu, W., & Zhu, X. (2021) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.764222 · Cited by 76 · see citing works
Shi, Y., Wang, S., Wang, K., Yang, R., Liu, D., Liao, H., Qi, Y., Qiu, K., Hu, Y., Wen, H., et al. (2024) · Small · doi:10.1002/smll.202309276 · Cited by 76 · see citing works
Mesenchymal stromal cells as cancer promoters
Antoon, R., Overdevest, N., Saleh, A. H., & Keating, A. (2024) · Oncogene · doi:10.1038/s41388-024-03183-1 · Cited by 75 · see citing works
Hermann, D. M., Xin, W., Bähr, M., Giebel, B., & Doeppner, T. R. (2022) · Theranostics · doi:10.7150/thno.73931 · Cited by 74 · see citing works
Li, C., & Xu, X. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03215-0 · Cited by 70 · see citing works
Li, C., Qin, F., Wang, W., Ni, Y., Gao, M., Guo, M., & Sun, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312866 · Cited by 69 · see citing works
BMSC-derived exosomes promote osteoporosis alleviation via M2 macrophage polarization
Zhang, Y., Bai, J., Xiao, B., & Li, C. (2024) · Molecular Medicine · doi:10.1186/s10020-024-00904-w · Cited by 68 · see citing works
Peppicelli, S., Calorini, L., Bianchini, F., Papucci, L., Magnelli, L., & Andreucci, E. (2024) · Cellular Oncology · doi:10.1007/s13402-024-00969-z · Cited by 70 · see citing works
Exosomal Non-coding RNAs-Mediated Crosstalk in the Tumor Microenvironment
Chen, Q., Li, Y.-F., Liu, Y.-Q., Xu, W.-L., & Zhu, X.-L. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.646864 · Cited by 55 · see citing works
Ge, X., Liu, W., Zhao, W., Feng, S., Duan, A., Ji, C., Shen, K., Liu, W., Zhou, J., Jiang, D., et al. (2020) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2020.07.025 · Cited by 63 · see citing works
Wang, L., Wang, Y., & Quan, J. (2020) · Molecular Medicine · doi:10.1186/s10020-020-00207-w · Cited by 63 · see citing works
Self-citationThe role of exosomes from BALF in lung disease
Liu, Z., Yan, J., Tong, L., Liu, S., & Zhang, Y. (2021) · Journal of Cellular Physiology · doi:10.1002/jcp.30553 · Cited by 63 · see citing works
Current Landscape of Epigenetics in Lung Cancer: Focus on the Mechanism and Application
Shi, Y.-X., Sheng, D., Cheng, L. Z., & Song, X.-Y. (2019) · Journal of Oncology · doi:10.1155/2019/8107318 · Cited by 63 · see citing works
How hypoxia regulate exosomes in ischemic diseases and cancer microenvironment?
Yaghoubi, S., Najminejad, H., Dabaghian, M., Karimi, M. H., Abdollahpour‐Alitappeh, M., Rad, F., Mahi‐Birjand, M., Mohammadi, S., Mohseni, F., Lari, M. S., et al. (2020) · IUBMB Life · doi:10.1002/iub.2275 · Cited by 61 · see citing works
Zang, J., Wu, Y., Su, X., Zhang, T., Tang, X., Ma, D., Li, Y., Liu, Y., Weng, Z., Liu, X., et al. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.616590 · Cited by 60 · see citing works
Extracellular Vesicles for Drug Delivery in Cancer Treatment
Wang, L., Yu, X., Zhou, J., & Su, C. (2023) · Biological Procedures Online · doi:10.1186/s12575-023-00220-3 · Cited by 60 · see citing works
Self-citationZhang, X., Wang, T., Wang, Z., Huang, K., Zhang, Y., Wang, G., Zhang, H., Chen, Z.-H., Wang, C., Zhang, J., et al. (2021) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2021.07.014 · Cited by 59 · see citing works
Self-citationNie, H., Liao, Z., Wang, Y., Zhou, J., He, X., & Ou, C. (2020) · Genes & Diseases · doi:10.1016/j.gendis.2020.12.004 · Cited by 57 · see citing works
Self-citationLyu, Z., Xin, M., Oyston, D. R., Xue, T., Kang, H., Wang, X., Wang, Z., & Wang, Z. (2024) · Pathology - Research and Practice · doi:10.1016/j.prp.2024.155354 · Cited by 58 · see citing works
Chen, H., Li, J.-J., Jiang, F., Shi, W., & Chang, G. (2019) · Bioscience Biotechnology and Biochemistry · doi:10.1080/09168451.2019.1677452 · Cited by 57 · see citing works
Liu, J., Feng, Y., Zeng, X., He, M., Gong, Y., & Liu, Y. (2020) · Journal of Cellular and Molecular Medicine · doi:10.1111/jcmm.15866 · Cited by 56 · see citing works
Hypoxia-Regulated Tumor-Derived Exosomes and Tumor Progression: A Focus on Immune Evasion
Shao, X., Hua, S., Feng, T., Ocansey, D. K. W., & Yin, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231911789 · Cited by 57 · see citing works
Huang, Y., Liu, W., He, B., Wang, L., Zhang, F., Shu, H., & Sun, L. (2020) · Journal of Bone Oncology · doi:10.1016/j.jbo.2020.100280 · Cited by 55 · see citing works
Self-citationTherapeutic Potential of Exosomes in Pulmonary Fibrosis
Xie, L., & Zeng, Y. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.590972 · Cited by 54 · see citing works
Zhang, Z., Hu, J., Ishihara, M., Sharrow, A. C., Flora, K., He, Y., & Wu, L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23063005 · Cited by 54 · see citing works
Zhou, S., Yu, L., Li, Y., Li, Z., Pu, J., & Wei, L. (2022) · Cell Transplantation · doi:10.1177/09636897221106998 · Cited by 54 · see citing works
Hypoxia‐Induced FUS–circTBC1D14 Stress Granules Promote Autophagy in TNBC
Liu, Y., Liu, Y., He, Y., Zhang, N., Zhang, S., Li, Y., Wang, X., Liang, Y., Chen, X., Zhao, W., et al. (2023) · Advanced Science · doi:10.1002/advs.202204988 · Cited by 54 · see citing works
Self-citationTumor-derived nanoseeds condition the soil for metastatic organotropism
Hu, M., Kenific, C. M., Boudreau, N. J., & Lyden, D. C. (2023) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2023.05.003 · Cited by 52 · see citing works
Underlying mechanisms and drug intervention strategies for the tumour microenvironment
Li, H., Zhou, L., Zhou, J., Li, Q., & Ji, Q. (2021) · Journal of Experimental & Clinical Cancer Research · doi:10.1186/s13046-021-01893-y · Cited by 51 · see citing works
The Role and Therapeutic Potential of Macropinocytosis in Cancer
Qiu, Z., Liu, W., Zhu, Q., Ke, K., Zhu, Q., Jin, W., Yu, S., Yang, Z., Li, L., Sun, X., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.919819 · Cited by 52 · see citing works
Hisakane, K., Seike, M., Sugano, T., Yoshikawa, A., Matsuda, K., Takano, N., Takahashi, S., Noro, R., & Gemma, A. (2021) · Thoracic Cancer · doi:10.1111/1759-7714.13943 · Cited by 50 · see citing works
- Authors
- Zhang, X., Sai, B., Wang, F., Wang, L., Wang, Y., Zheng, L., Li, G., Tang, J., & Xiang, J.
- Affiliations
- Central South University (CN)
- Corresponding author
- Tang, Jingqun
- Xiang, Juanjuan
- Venue
- Molecular Cancer
- Published
- 2019-03-13
- Volume
- 18
- Issue
- 1
- Pages
- 40-40
- ISSN
- 1476-4598 (ISSN-L)
- PMC
- PMC6417285
- OpenAlex
- W2938403043
- Cited by
- 560
- References
- 50
- Citations by year
- 2026: 34 · 2025: 61 · 2024: 96 · 2023: 94 · 2022: 114 · 2021: 81 · 2020: 63 · 2019: 16
- FWCI
- 23.01
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Molecular Cancer (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Natural Science Foundation of China (81472695, 81773147)
- Strategic Priority Research Program of Central South University (ZLXD2017004)
- National Training and Research Base for Talents of principles of carcinogenesis foundation (111 project: 111-2-12)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Keywords
- lung cancer metastasis, bone marrow-derived mesenchymal stem cells, exosomes, exosomal microRNAs, hypoxia, STAT3 signaling, epithelial-mesenchymal transition, tumor invasion, miR-193a-3p, miR-210-3p, tumor microenvironment, exosome-mediated intercellular communication
- MeSH terms
- Animals, Hypoxia, Cell Movement, Female, Follow-Up Studies, Humans, Lung Neoplasms, Male, Mice, Inbred C57BL, Mice, Nude, Middle Aged, Prognosis, Tumor Cells, Cultured, Biomarkers, Tumor, Signal Transduction, Gene Expression Regulation, Neoplastic, Survival Rate, Case-Control Studies, Apoptosis, Xenograft Model Antitumor Assays, MicroRNAs, Cell Proliferation, STAT3 Transcription Factor, Mice, Exosomes, Epithelial-Mesenchymal Transition, Mesenchymal Stem Cells
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