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Published in: Journal of Translational Medicine 1/2021

Open Access 01-12-2021 | NSCLC | Review

The role of exosomes in lung cancer metastasis and clinical applications: an updated review

Authors: Lei Yin, Xiaotian Liu, Xuejun Shao, Tao Feng, Jun Xu, Qi Wang, Shenghao Hua

Published in: Journal of Translational Medicine | Issue 1/2021

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Abstract

Lung cancer is the leading cause of cancer-associated deaths accounting for 24% of all cancer deaths. As a crucial phase of tumor progression, lung cancer metastasis is linked to over 70% of these mortalities. In recent years, exosomes have received increasing research attention in their role in the induction of carcinogenesis and metastasis in the lung. In this review, recent studies on the contribution of exosomes to lung cancer metastasis are discussed, particularly highlighting the role of lung tumor-derived exosomes in immune system evasion, epithelial-mesenchymal transition, and angiogenesis, and their involvement at both the pre-metastatic and metastatic phases. The clinical application of exosomes as therapeutic drug carriers, their role in antitumor drug resistance, and their utility as predictive biomarkers in diagnosis and prognosis are also presented. The metastatic activity, a complex multistep process of cancer cell invasion, survival in blood vessels, attachment and subsequent colonization of the host's organs, is integrated with exosomal effects. Exosomes act as functional mediating factors in cell–cell communication, influencing various steps of the metastatic cascade. To this end, lung cancer cell-derived exosomes enhance cell proliferation, angiogenesis, and metastasis, regulate drug resistance, and antitumor immune activities during lung carcinogenesis, and are currently being explored as an important component in liquid biopsy assessment for diagnosing lung cancer. These nano-sized extracellular vesicles are also being explored as delivery vehicles for therapeutic molecules owing to their unique properties of biocompatibility, circulatory stability, decreased toxicity, and tumor specificity. The current knowledge of the role of exosomes highlights an array of exosome-dependent pathways and cargoes that are ripe for exploiting therapeutic targets to treat lung cancer metastasis, and for predictive value assessment in diagnosis, prognosis, and anti-tumor drug resistance.
Literature
2.
go back to reference Romaszko A, Doboszyńska A. Multiple primary lung cancer: a literature review. Adv Clin Exp Med. 2018;27:725–30.PubMedCrossRef Romaszko A, Doboszyńska A. Multiple primary lung cancer: a literature review. Adv Clin Exp Med. 2018;27:725–30.PubMedCrossRef
3.
go back to reference Li M-Y, Liu L-Z, Dong M. Progress on pivotal role and application of exosome in lung cancer carcinogenesis, diagnosis, therapy and prognosis. Mol Cancer. 2021;20:22.PubMedPubMedCentralCrossRef Li M-Y, Liu L-Z, Dong M. Progress on pivotal role and application of exosome in lung cancer carcinogenesis, diagnosis, therapy and prognosis. Mol Cancer. 2021;20:22.PubMedPubMedCentralCrossRef
4.
go back to reference Wood SL, Pernemalm M, Crosbie PA, Whetton AD. The role of the tumor-microenvironment in lung cancer-metastasis and its relationship to potential therapeutic targets. Cancer Treat Rev. 2014;40:558–66.PubMedCrossRef Wood SL, Pernemalm M, Crosbie PA, Whetton AD. The role of the tumor-microenvironment in lung cancer-metastasis and its relationship to potential therapeutic targets. Cancer Treat Rev. 2014;40:558–66.PubMedCrossRef
5.
go back to reference Fang T, Lv H, Lv G, Li T, Wang C, Han Q, et al. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun. 2018;9:191.PubMedPubMedCentralCrossRef Fang T, Lv H, Lv G, Li T, Wang C, Han Q, et al. Tumor-derived exosomal miR-1247-3p induces cancer-associated fibroblast activation to foster lung metastasis of liver cancer. Nat Commun. 2018;9:191.PubMedPubMedCentralCrossRef
7.
go back to reference Alipoor SD, Mortaz E, Varahram M, Movassaghi M, Kraneveld AD, Garssen J, et al. The potential biomarkers and immunological effects of tumor-derived exosomes in lung cancer. Front Immunol. 2018;9:819.PubMedPubMedCentralCrossRef Alipoor SD, Mortaz E, Varahram M, Movassaghi M, Kraneveld AD, Garssen J, et al. The potential biomarkers and immunological effects of tumor-derived exosomes in lung cancer. Front Immunol. 2018;9:819.PubMedPubMedCentralCrossRef
8.
go back to reference Fujita Y, Kosaka N, Araya J, Kuwano K, Ochiya T. Extracellular vesicles in lung microenvironment and pathogenesis. Trends Mol Med. 2015;21:533–42.PubMedCrossRef Fujita Y, Kosaka N, Araya J, Kuwano K, Ochiya T. Extracellular vesicles in lung microenvironment and pathogenesis. Trends Mol Med. 2015;21:533–42.PubMedCrossRef
9.
go back to reference Ocansey DKW, Zhang L, Wang Y, Yan Y, Qian H, Zhang X, et al. Exosome-mediated effects and applications in inflammatory bowel disease. Biol Rev Camb Philos Soc. 2020;95:1287–307.PubMedPubMedCentralCrossRef Ocansey DKW, Zhang L, Wang Y, Yan Y, Qian H, Zhang X, et al. Exosome-mediated effects and applications in inflammatory bowel disease. Biol Rev Camb Philos Soc. 2020;95:1287–307.PubMedPubMedCentralCrossRef
11.
go back to reference Mashouri L, Yousefi H, Aref AR, Ahadi AM, Molaei F, Alahari SK. Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol Cancer. 2019;18:75.PubMedPubMedCentralCrossRef Mashouri L, Yousefi H, Aref AR, Ahadi AM, Molaei F, Alahari SK. Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol Cancer. 2019;18:75.PubMedPubMedCentralCrossRef
12.
go back to reference Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–89.PubMedCrossRef Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–89.PubMedCrossRef
13.
go back to reference Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci. 2018;75:193–208.PubMedCrossRef Hessvik NP, Llorente A. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci. 2018;75:193–208.PubMedCrossRef
14.
15.
go back to reference Hu C, Meiners S, Lukas C, Stathopoulos GT, Chen J. Role of exosomal microRNAs in lung cancer biology and clinical applications. Cell Prolif. 2020;53: e12828.PubMedPubMedCentralCrossRef Hu C, Meiners S, Lukas C, Stathopoulos GT, Chen J. Role of exosomal microRNAs in lung cancer biology and clinical applications. Cell Prolif. 2020;53: e12828.PubMedPubMedCentralCrossRef
17.
go back to reference Reclusa P, Taverna S, Pucci M, Durendez E, Calabuig S, Manca P, et al. Exosomes as diagnostic and predictive biomarkers in lung cancer. J Thorac Dis. 2017;9:S1373-82.PubMedPubMedCentralCrossRef Reclusa P, Taverna S, Pucci M, Durendez E, Calabuig S, Manca P, et al. Exosomes as diagnostic and predictive biomarkers in lung cancer. J Thorac Dis. 2017;9:S1373-82.PubMedPubMedCentralCrossRef
18.
go back to reference Arrighetti N, Corbo C, Evangelopoulos M, Pastò A, Zuco V, Tasciotti E. Exosome-like nanovectors for drug delivery in cancer. Curr Med Chem. 2019;26:6132–48.PubMedPubMedCentralCrossRef Arrighetti N, Corbo C, Evangelopoulos M, Pastò A, Zuco V, Tasciotti E. Exosome-like nanovectors for drug delivery in cancer. Curr Med Chem. 2019;26:6132–48.PubMedPubMedCentralCrossRef
19.
go back to reference Yuan D, Zhao Y, Banks WA, Bullock KM, Haney M, Batrakova E, et al. Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials. 2017;142:1–12.PubMedPubMedCentralCrossRef Yuan D, Zhao Y, Banks WA, Bullock KM, Haney M, Batrakova E, et al. Macrophage exosomes as natural nanocarriers for protein delivery to inflamed brain. Biomaterials. 2017;142:1–12.PubMedPubMedCentralCrossRef
20.
go back to reference Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, et al. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 2015;207:18–30.PubMedPubMedCentralCrossRef Haney MJ, Klyachko NL, Zhao Y, Gupta R, Plotnikova EG, He Z, et al. Exosomes as drug delivery vehicles for Parkinson’s disease therapy. J Control Release. 2015;207:18–30.PubMedPubMedCentralCrossRef
21.
go back to reference Luan X, Sansanaphongpricha K, Myers I, Chen H, Yuan H, Sun D. Engineering exosomes as refined biological nanoplatforms for drug delivery. Acta Pharmacol Sin. 2017;38:754–63.PubMedPubMedCentralCrossRef Luan X, Sansanaphongpricha K, Myers I, Chen H, Yuan H, Sun D. Engineering exosomes as refined biological nanoplatforms for drug delivery. Acta Pharmacol Sin. 2017;38:754–63.PubMedPubMedCentralCrossRef
22.
go back to reference Ha D, Yang N, Nadithe V. Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: current perspectives and future challenges. Acta Pharm Sin B. 2016;6:287–96.PubMedPubMedCentralCrossRef Ha D, Yang N, Nadithe V. Exosomes as therapeutic drug carriers and delivery vehicles across biological membranes: current perspectives and future challenges. Acta Pharm Sin B. 2016;6:287–96.PubMedPubMedCentralCrossRef
23.
go back to reference Barile L, Vassalli G. Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol Ther. 2017;174:63–78.PubMedCrossRef Barile L, Vassalli G. Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol Ther. 2017;174:63–78.PubMedCrossRef
24.
go back to reference Amiri A, Pourhanifeh MH, Mirzaei HR, Nahand JS, Moghoofei M, Sahebnasagh R, et al. Exosomes and lung cancer: roles in pathophysiology, diagnosis and therapeutic applications. Curr Med Chem. 2020;28:308–28.CrossRef Amiri A, Pourhanifeh MH, Mirzaei HR, Nahand JS, Moghoofei M, Sahebnasagh R, et al. Exosomes and lung cancer: roles in pathophysiology, diagnosis and therapeutic applications. Curr Med Chem. 2020;28:308–28.CrossRef
25.
go back to reference Frydrychowicz M, Kolecka-Bednarczyk A, Madejczyk M, Yasar S, Dworacki G. Exosomes—structure, biogenesis and biological role in non-small-cell lung cancer. Scand J Immunol. 2015;81:2–10.PubMedCrossRef Frydrychowicz M, Kolecka-Bednarczyk A, Madejczyk M, Yasar S, Dworacki G. Exosomes—structure, biogenesis and biological role in non-small-cell lung cancer. Scand J Immunol. 2015;81:2–10.PubMedCrossRef
26.
go back to reference Chen R, Xu X, Qian Z, Zhang C, Niu Y, Wang Z, et al. The biological functions and clinical applications of exosomes in lung cancer. Cell Mol Life Sci. 2019;76:4613–33.PubMedCrossRef Chen R, Xu X, Qian Z, Zhang C, Niu Y, Wang Z, et al. The biological functions and clinical applications of exosomes in lung cancer. Cell Mol Life Sci. 2019;76:4613–33.PubMedCrossRef
27.
go back to reference Tian X, Shen H, Li Z, Wang T, Wang S. Tumor-derived exosomes, myeloid-derived suppressor cells, and tumor microenvironment. J Hematol Oncol. 2019;12:84.PubMedPubMedCentralCrossRef Tian X, Shen H, Li Z, Wang T, Wang S. Tumor-derived exosomes, myeloid-derived suppressor cells, and tumor microenvironment. J Hematol Oncol. 2019;12:84.PubMedPubMedCentralCrossRef
29.
go back to reference Chen G, Huang AC, Zhang W, Zhang G, Wu M, Xu W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 2018;560:382–6.PubMedPubMedCentralCrossRef Chen G, Huang AC, Zhang W, Zhang G, Wu M, Xu W, et al. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 2018;560:382–6.PubMedPubMedCentralCrossRef
30.
go back to reference Poggio M, Hu T, Pai C-C, Chu B, Belair CD, Chang A, et al. Suppression of exosomal PD-L1 induces systemic anti-tumor immunity and memory. Cell. 2019;177:414-27.e13.PubMedPubMedCentralCrossRef Poggio M, Hu T, Pai C-C, Chu B, Belair CD, Chang A, et al. Suppression of exosomal PD-L1 induces systemic anti-tumor immunity and memory. Cell. 2019;177:414-27.e13.PubMedPubMedCentralCrossRef
31.
go back to reference Kim DH, Kim H, Choi YJ, Kim SY, Lee J-E, Sung KJ, et al. Exosomal PD-L1 promotes tumor growth through immune escape in non-small cell lung cancer. Exp Mol Med. 2019;51:1–13.PubMedPubMedCentral Kim DH, Kim H, Choi YJ, Kim SY, Lee J-E, Sung KJ, et al. Exosomal PD-L1 promotes tumor growth through immune escape in non-small cell lung cancer. Exp Mol Med. 2019;51:1–13.PubMedPubMedCentral
32.
go back to reference Berchem G, Noman MZ, Bosseler M, Paggetti J, Baconnais S, Le cam E, et al. Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-β and miR23a transfer. Oncoimmunology. 2016;5: e1062968.PubMedCrossRef Berchem G, Noman MZ, Bosseler M, Paggetti J, Baconnais S, Le cam E, et al. Hypoxic tumor-derived microvesicles negatively regulate NK cell function by a mechanism involving TGF-β and miR23a transfer. Oncoimmunology. 2016;5: e1062968.PubMedCrossRef
33.
go back to reference Huang S, Li Y, Zhang J, Rong J, Ye S. Epidermal growth factor receptor-containing exosomes induce tumor-specific regulatory T cells. Cancer Invest. 2013;31:330–5.PubMedCrossRef Huang S, Li Y, Zhang J, Rong J, Ye S. Epidermal growth factor receptor-containing exosomes induce tumor-specific regulatory T cells. Cancer Invest. 2013;31:330–5.PubMedCrossRef
34.
go back to reference Greening D, Gopal S, Mathias R. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin Cell Dev Biol. 2015;40:60–71.PubMedCrossRef Greening D, Gopal S, Mathias R. Emerging roles of exosomes during epithelial-mesenchymal transition and cancer progression. Semin Cell Dev Biol. 2015;40:60–71.PubMedCrossRef
35.
go back to reference Blackwell R, Foreman K, Gupta G. The role of cancer-derived exosomes in tumorigenicity & epithelial-to-mesenchymal transition. Cancers. 2017;9:105.PubMedCentralCrossRef Blackwell R, Foreman K, Gupta G. The role of cancer-derived exosomes in tumorigenicity & epithelial-to-mesenchymal transition. Cancers. 2017;9:105.PubMedCentralCrossRef
36.
go back to reference Kim J, Kim TY, Lee MS, Mun JY, Ihm C, Kim SA. Exosome cargo reflects TGF-β1-mediated epithelial-to-mesenchymal transition (EMT) status in A549 human lung adenocarcinoma cells. Biochem Biophys Res Commun. 2016;478:643–8.PubMedCrossRef Kim J, Kim TY, Lee MS, Mun JY, Ihm C, Kim SA. Exosome cargo reflects TGF-β1-mediated epithelial-to-mesenchymal transition (EMT) status in A549 human lung adenocarcinoma cells. Biochem Biophys Res Commun. 2016;478:643–8.PubMedCrossRef
37.
go back to reference Tang Y-T, Huang Y-Y, Li J-H, Qin S-H, Xu Y, An T-X, et al. Alterations in exosomal miRNA profile upon epithelial-mesenchymal transition in human lung cancer cell lines. BMC Genomics. 2018;19:802.PubMedPubMedCentralCrossRef Tang Y-T, Huang Y-Y, Li J-H, Qin S-H, Xu Y, An T-X, et al. Alterations in exosomal miRNA profile upon epithelial-mesenchymal transition in human lung cancer cell lines. BMC Genomics. 2018;19:802.PubMedPubMedCentralCrossRef
38.
go back to reference Rahman MA, Barger JF, Lovat F, Gao M, Otterson GA, Nana-Sinkam P. Lung cancer exosomes as drivers of epithelial mesenchymal transition. Oncotarget. 2016;7:54852–66.PubMedPubMedCentralCrossRef Rahman MA, Barger JF, Lovat F, Gao M, Otterson GA, Nana-Sinkam P. Lung cancer exosomes as drivers of epithelial mesenchymal transition. Oncotarget. 2016;7:54852–66.PubMedPubMedCentralCrossRef
39.
go back to reference Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer. 2017;17:302–17.PubMedCrossRef Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer. 2017;17:302–17.PubMedCrossRef
41.
go back to reference Cheng Y, Dai X, Yang T, Zhang N, Liu Z, Jiang Y. Low long noncoding RNA growth arrest-specific transcript 5 expression in the exosomes of lung cancer cells promotes tumor angiogenesis. J Oncol. 2019;2019:1–13.CrossRef Cheng Y, Dai X, Yang T, Zhang N, Liu Z, Jiang Y. Low long noncoding RNA growth arrest-specific transcript 5 expression in the exosomes of lung cancer cells promotes tumor angiogenesis. J Oncol. 2019;2019:1–13.CrossRef
42.
go back to reference Mao S, Lu Z, Zheng S, Zhang H, Zhang G, Wang F, et al. Exosomal miR-141 promotes tumor angiogenesis via KLF12 in small cell lung cancer. J Exp Clin Cancer Res. 2020;39:193.PubMedPubMedCentralCrossRef Mao S, Lu Z, Zheng S, Zhang H, Zhang G, Wang F, et al. Exosomal miR-141 promotes tumor angiogenesis via KLF12 in small cell lung cancer. J Exp Clin Cancer Res. 2020;39:193.PubMedPubMedCentralCrossRef
43.
go back to reference Fan J, Xu G, Chang Z, Zhu L, Yao J. miR-210 transferred by lung cancer cell-derived exosomes may act as proangiogenic factor in cancer-associated fibroblasts by modulating JAK2/STAT3 pathway. Clin Sci. 2020;134:807–25.CrossRef Fan J, Xu G, Chang Z, Zhu L, Yao J. miR-210 transferred by lung cancer cell-derived exosomes may act as proangiogenic factor in cancer-associated fibroblasts by modulating JAK2/STAT3 pathway. Clin Sci. 2020;134:807–25.CrossRef
44.
go back to reference Liu M, Sun X, Shi S. MORC2 enhances tumor growth by promoting angiogenesis and tumor-associated macrophage recruitment via Wnt/β-catenin in lung cancer. Cell Physiol Biochem. 2018;51:1679–94.PubMedCrossRef Liu M, Sun X, Shi S. MORC2 enhances tumor growth by promoting angiogenesis and tumor-associated macrophage recruitment via Wnt/β-catenin in lung cancer. Cell Physiol Biochem. 2018;51:1679–94.PubMedCrossRef
45.
go back to reference Zhou L, Lv T, Zhang Q, Zhu Q, Zhan P, Zhu S, et al. The biology, function and clinical implications of exosomes in lung cancer. Cancer Lett. 2017;407:84–92.PubMedCrossRef Zhou L, Lv T, Zhang Q, Zhu Q, Zhan P, Zhu S, et al. The biology, function and clinical implications of exosomes in lung cancer. Cancer Lett. 2017;407:84–92.PubMedCrossRef
46.
go back to reference Iqbal MA, Arora S, Prakasam G, Calin GA, Syed MA. MicroRNA in lung cancer: role, mechanisms, pathways and therapeutic relevance. Mol Aspects Med. 2019;70:3–20.PubMedCrossRef Iqbal MA, Arora S, Prakasam G, Calin GA, Syed MA. MicroRNA in lung cancer: role, mechanisms, pathways and therapeutic relevance. Mol Aspects Med. 2019;70:3–20.PubMedCrossRef
47.
go back to reference Wang Y, Yi J, Chen X, Zhang Y, Xu M, Yang Z. The regulation of cancer cell migration by lung cancer cell-derived exosomes through TGF-β and IL-10. Oncol Lett. 2016;11:1527–30.PubMedCrossRef Wang Y, Yi J, Chen X, Zhang Y, Xu M, Yang Z. The regulation of cancer cell migration by lung cancer cell-derived exosomes through TGF-β and IL-10. Oncol Lett. 2016;11:1527–30.PubMedCrossRef
48.
go back to reference Wu C-F, Andzinski L, Kasnitz N, Kröger A, Klawonn F, Lienenklaus S, et al. The lack of type I interferon induces neutrophil-mediated pre-metastatic niche formation in the mouse lung. Int J Cancer. 2015;137:837–47.PubMedCrossRef Wu C-F, Andzinski L, Kasnitz N, Kröger A, Klawonn F, Lienenklaus S, et al. The lack of type I interferon induces neutrophil-mediated pre-metastatic niche formation in the mouse lung. Int J Cancer. 2015;137:837–47.PubMedCrossRef
49.
go back to reference Liu Y, Gu Y, Han Y, Zhang Q, Jiang Z, Zhang X, et al. Tumor exosomal RNAs promote lung pre-metastatic niche formation by activating alveolar epithelial TLR3 to recruit neutrophils. Cancer Cell. 2016;30:243–56.PubMedCrossRef Liu Y, Gu Y, Han Y, Zhang Q, Jiang Z, Zhang X, et al. Tumor exosomal RNAs promote lung pre-metastatic niche formation by activating alveolar epithelial TLR3 to recruit neutrophils. Cancer Cell. 2016;30:243–56.PubMedCrossRef
50.
go back to reference Hoshino A, Costa-Silva B, Shen T-L, Rodrigues G, Hashimoto A, Mark MT, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527:329–35.PubMedPubMedCentralCrossRef Hoshino A, Costa-Silva B, Shen T-L, Rodrigues G, Hashimoto A, Mark MT, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527:329–35.PubMedPubMedCentralCrossRef
51.
go back to reference Hood JL, San RS, Wickline SA. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 2011;71:3792–801.PubMedCrossRef Hood JL, San RS, Wickline SA. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 2011;71:3792–801.PubMedCrossRef
52.
go back to reference Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–7.PubMedPubMedCentralCrossRef Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438:820–7.PubMedPubMedCentralCrossRef
53.
go back to reference Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012;18:883–91.PubMedPubMedCentralCrossRef Peinado H, Alečković M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012;18:883–91.PubMedPubMedCentralCrossRef
54.
go back to reference Weidle UH, Birzele F, Kollmorgen G, Rüger R. The multiple roles of exosomes in metastasis. Cancer Genomics Proteomics. 2017;14:1–16.PubMedCrossRef Weidle UH, Birzele F, Kollmorgen G, Rüger R. The multiple roles of exosomes in metastasis. Cancer Genomics Proteomics. 2017;14:1–16.PubMedCrossRef
55.
go back to reference Zeng Z, Li Y, Pan Y, Lan X, Song F, Sun J, et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun. 2018;9:5395.PubMedPubMedCentralCrossRef Zeng Z, Li Y, Pan Y, Lan X, Song F, Sun J, et al. Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis. Nat Commun. 2018;9:5395.PubMedPubMedCentralCrossRef
56.
go back to reference Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M, et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci. 2013;110:7312–7.PubMedPubMedCentralCrossRef Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M, et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci. 2013;110:7312–7.PubMedPubMedCentralCrossRef
58.
go back to reference Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin J-P, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest. 2010;120:457–71.PubMedPubMedCentral Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin J-P, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest. 2010;120:457–71.PubMedPubMedCentral
59.
go back to reference Benito-Martin A, Di Giannatale A, Ceder S, Peinado H. The new deal: a potential role for secreted vesicles in innate immunity and tumor progression. Front Immunol. 2015;6:66.PubMedPubMedCentralCrossRef Benito-Martin A, Di Giannatale A, Ceder S, Peinado H. The new deal: a potential role for secreted vesicles in innate immunity and tumor progression. Front Immunol. 2015;6:66.PubMedPubMedCentralCrossRef
60.
go back to reference Bobrie A, Krumeich S, Reyal F, Recchi C, Moita LF, Seabra MC, et al. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res. 2012;72:4920–30.PubMedCrossRef Bobrie A, Krumeich S, Reyal F, Recchi C, Moita LF, Seabra MC, et al. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res. 2012;72:4920–30.PubMedCrossRef
61.
go back to reference Ludwig S, Floros T, Theodoraki M-N, Hong C-S, Jackson EK, Lang S, et al. Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer. Clin Cancer Res. 2017;23:4843–54.PubMedPubMedCentralCrossRef Ludwig S, Floros T, Theodoraki M-N, Hong C-S, Jackson EK, Lang S, et al. Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer. Clin Cancer Res. 2017;23:4843–54.PubMedPubMedCentralCrossRef
62.
go back to reference Czernek L, Düchler M. Functions of cancer-derived extracellular vesicles in immunosuppression. Arch Immunol Ther Exp. 2017;65:311–23.CrossRef Czernek L, Düchler M. Functions of cancer-derived extracellular vesicles in immunosuppression. Arch Immunol Ther Exp. 2017;65:311–23.CrossRef
63.
go back to reference Plebanek MP, Angeloni NL, Vinokour E, Li J, Henkin A, Martinez-Marin D, et al. Pre-metastatic cancer exosomes induce immune surveillance by patrolling monocytes at the metastatic niche. Nat Commun. 2017;8:1319.PubMedPubMedCentralCrossRef Plebanek MP, Angeloni NL, Vinokour E, Li J, Henkin A, Martinez-Marin D, et al. Pre-metastatic cancer exosomes induce immune surveillance by patrolling monocytes at the metastatic niche. Nat Commun. 2017;8:1319.PubMedPubMedCentralCrossRef
64.
go back to reference Pritchard A, Tousif S, Wang Y, Hough K, Khan S, Strenkowski J, et al. Lung tumor cell-derived exosomes promote M2 macrophage polarization. Cells. 2020;9:1303.PubMedCentralCrossRef Pritchard A, Tousif S, Wang Y, Hough K, Khan S, Strenkowski J, et al. Lung tumor cell-derived exosomes promote M2 macrophage polarization. Cells. 2020;9:1303.PubMedCentralCrossRef
65.
go back to reference Clark DJ, Fondrie WE, Yang A, Mao L. Triple SILAC quantitative proteomic analysis reveals differential abundance of cell signaling proteins between normal and lung cancer-derived exosomes. J Proteomics. 2016;133:161–9.PubMedCrossRef Clark DJ, Fondrie WE, Yang A, Mao L. Triple SILAC quantitative proteomic analysis reveals differential abundance of cell signaling proteins between normal and lung cancer-derived exosomes. J Proteomics. 2016;133:161–9.PubMedCrossRef
66.
go back to reference Zhang N, Nan A, Chen L, Li X, Jia Y, Qiu M, et al. Circular RNA circSATB2 promotes progression of non-small cell lung cancer cells. Mol Cancer. 2020;19:101.PubMedPubMedCentralCrossRef Zhang N, Nan A, Chen L, Li X, Jia Y, Qiu M, et al. Circular RNA circSATB2 promotes progression of non-small cell lung cancer cells. Mol Cancer. 2020;19:101.PubMedPubMedCentralCrossRef
67.
go back to reference Qi Y, Zha W, Zhang W. Exosomal miR-660-5p promotes tumor growth and metastasis in non-small cell lung cancer. J BUON. 2019;24:599–607.PubMed Qi Y, Zha W, Zhang W. Exosomal miR-660-5p promotes tumor growth and metastasis in non-small cell lung cancer. J BUON. 2019;24:599–607.PubMed
68.
go back to reference Hong W, Xue M, Jiang J, Zhang Y, Gao X. Circular RNA circ-CPA4/ let-7 miRNA/PD-L1 axis regulates cell growth, stemness, drug resistance and immune evasion in non-small cell lung cancer (NSCLC). J Exp Clin Cancer Res. 2020;39:149.PubMedPubMedCentralCrossRef Hong W, Xue M, Jiang J, Zhang Y, Gao X. Circular RNA circ-CPA4/ let-7 miRNA/PD-L1 axis regulates cell growth, stemness, drug resistance and immune evasion in non-small cell lung cancer (NSCLC). J Exp Clin Cancer Res. 2020;39:149.PubMedPubMedCentralCrossRef
69.
go back to reference Wu D, Deng S, Liu T, Han R, Zhang T, Xu Y. TGF-β-mediated exosomal lnc-MMP2-2 regulates migration and invasion of lung cancer cells to the vasculature by promoting MMP2 expression. Cancer Med. 2018;7:5118–29.PubMedPubMedCentralCrossRef Wu D, Deng S, Liu T, Han R, Zhang T, Xu Y. TGF-β-mediated exosomal lnc-MMP2-2 regulates migration and invasion of lung cancer cells to the vasculature by promoting MMP2 expression. Cancer Med. 2018;7:5118–29.PubMedPubMedCentralCrossRef
70.
go back to reference Yao J, Lu X, Wang Y, Li J, Ni B. Long noncoding RNAs AC026904.1 is essential for TGF-β-induced migration and epithelial-mesenchymal transition through functioning as an enhancer of slug in lung cancer cells. Environ Toxicol. 2020;35:942–51.PubMedCrossRef Yao J, Lu X, Wang Y, Li J, Ni B. Long noncoding RNAs AC026904.1 is essential for TGF-β-induced migration and epithelial-mesenchymal transition through functioning as an enhancer of slug in lung cancer cells. Environ Toxicol. 2020;35:942–51.PubMedCrossRef
71.
go back to reference Li C, Wan L, Liu Z, Xu G, Wang S, Su Z, et al. Long non-coding RNA XIST promotes TGF-β-induced epithelial-mesenchymal transition by regulating miR-367/141-ZEB2 axis in non-small-cell lung cancer. Cancer Lett. 2018;418:185–95.PubMedCrossRef Li C, Wan L, Liu Z, Xu G, Wang S, Su Z, et al. Long non-coding RNA XIST promotes TGF-β-induced epithelial-mesenchymal transition by regulating miR-367/141-ZEB2 axis in non-small-cell lung cancer. Cancer Lett. 2018;418:185–95.PubMedCrossRef
72.
go back to reference Chen L, Xu S, Xu H, Zhang J, Ning J, Wang S. MicroRNA-378 is associated with non-small cell lung cancer brain metastasis by promoting cell migration, invasion and tumor angiogenesis. Med Oncol. 2012;29:1673–80.PubMedCrossRef Chen L, Xu S, Xu H, Zhang J, Ning J, Wang S. MicroRNA-378 is associated with non-small cell lung cancer brain metastasis by promoting cell migration, invasion and tumor angiogenesis. Med Oncol. 2012;29:1673–80.PubMedCrossRef
73.
go back to reference Kim DH, Park S, Kim H, Choi YJ, Kim SY, Sung KJ, et al. Tumor-derived exosomal miR-619-5p promotes tumor angiogenesis and metastasis through the inhibition of RCAN1.4. Cancer Lett. 2020;475:2–13.PubMedCrossRef Kim DH, Park S, Kim H, Choi YJ, Kim SY, Sung KJ, et al. Tumor-derived exosomal miR-619-5p promotes tumor angiogenesis and metastasis through the inhibition of RCAN1.4. Cancer Lett. 2020;475:2–13.PubMedCrossRef
74.
go back to reference Taverna S, Pucci M, Giallombardo M, Di Bella MA, Santarpia M, Reclusa P, et al. Amphiregulin contained in NSCLC-exosomes induces osteoclast differentiation through the activation of EGFR pathway. Sci Rep. 2017;7:3170.PubMedPubMedCentralCrossRef Taverna S, Pucci M, Giallombardo M, Di Bella MA, Santarpia M, Reclusa P, et al. Amphiregulin contained in NSCLC-exosomes induces osteoclast differentiation through the activation of EGFR pathway. Sci Rep. 2017;7:3170.PubMedPubMedCentralCrossRef
75.
go back to reference Liao T, Chen W, Sun J, Zhang Y, Hu X, Yang S, et al. CXCR4 accelerates osteoclastogenesis induced by non-small cell lung carcinoma cells through self-potentiation and VCAM1 secretion. Cell Physiol Biochem. 2018;50:1084–99.PubMedCrossRef Liao T, Chen W, Sun J, Zhang Y, Hu X, Yang S, et al. CXCR4 accelerates osteoclastogenesis induced by non-small cell lung carcinoma cells through self-potentiation and VCAM1 secretion. Cell Physiol Biochem. 2018;50:1084–99.PubMedCrossRef
76.
go back to reference Peng X, Guo W, Ren T, Lou Z, Lu X, Zhang S, et al. Differential expression of the RANKL/RANK/OPG System is associated with bone metastasis in human non-small cell lung cancer. PLoS ONE. 2013;8: e58361.PubMedPubMedCentralCrossRef Peng X, Guo W, Ren T, Lou Z, Lu X, Zhang S, et al. Differential expression of the RANKL/RANK/OPG System is associated with bone metastasis in human non-small cell lung cancer. PLoS ONE. 2013;8: e58361.PubMedPubMedCentralCrossRef
77.
go back to reference Raimondo S, Saieva L, Vicario E, Pucci M, Toscani D, Manno M, et al. Multiple myeloma-derived exosomes are enriched of amphiregulin (AREG) and activate the epidermal growth factor pathway in the bone microenvironment leading to osteoclastogenesis. J Hematol Oncol. 2019;12:2.PubMedPubMedCentralCrossRef Raimondo S, Saieva L, Vicario E, Pucci M, Toscani D, Manno M, et al. Multiple myeloma-derived exosomes are enriched of amphiregulin (AREG) and activate the epidermal growth factor pathway in the bone microenvironment leading to osteoclastogenesis. J Hematol Oncol. 2019;12:2.PubMedPubMedCentralCrossRef
78.
go back to reference Yang X-R, Pi C, Yu R, Fan X-J, Peng X-X, Zhang X-C, et al. Correlation of exosomal microRNA clusters with bone metastasis in non-small cell lung cancer. Clin Exp Metastasis. 2020;38:109–17.PubMedPubMedCentralCrossRef Yang X-R, Pi C, Yu R, Fan X-J, Peng X-X, Zhang X-C, et al. Correlation of exosomal microRNA clusters with bone metastasis in non-small cell lung cancer. Clin Exp Metastasis. 2020;38:109–17.PubMedPubMedCentralCrossRef
79.
go back to reference Xu Z-H, Miao Z-W, Jiang Q-Z, Gan D-X, Wei X-G, Xue X-Z, et al. Brain microvascular endothelial cell exosome-mediated S100A16 up-regulation confers small-cell lung cancer cell survival in brain. FASEB J. 2019;33:1742–57.PubMedCrossRef Xu Z-H, Miao Z-W, Jiang Q-Z, Gan D-X, Wei X-G, Xue X-Z, et al. Brain microvascular endothelial cell exosome-mediated S100A16 up-regulation confers small-cell lung cancer cell survival in brain. FASEB J. 2019;33:1742–57.PubMedCrossRef
80.
go back to reference Wei C, Zhang R, Cai Q, Gao X, Tong F, Dong J, et al. MicroRNA-330-3p promotes brain metastasis and epithelial-mesenchymal transition via GRIA3 in non-small cell lung cancer. Aging. 2019;11:6734–61.PubMedPubMedCentralCrossRef Wei C, Zhang R, Cai Q, Gao X, Tong F, Dong J, et al. MicroRNA-330-3p promotes brain metastasis and epithelial-mesenchymal transition via GRIA3 in non-small cell lung cancer. Aging. 2019;11:6734–61.PubMedPubMedCentralCrossRef
81.
go back to reference Leong HS, Robertson AE, Stoletov K, Leith SJ, Chin CA, Chien AE, et al. Invadopodia are required for cancer cell extravasation and are a therapeutic target for metastasis. Cell Rep. 2014;8:1558–70.PubMedCrossRef Leong HS, Robertson AE, Stoletov K, Leith SJ, Chin CA, Chien AE, et al. Invadopodia are required for cancer cell extravasation and are a therapeutic target for metastasis. Cell Rep. 2014;8:1558–70.PubMedCrossRef
82.
go back to reference Wang L, Tong X, Zhou Z, Wang S, Lei Z, Zhang T, et al. Circular RNA hsa_circ_0008305 (circPTK2) inhibits TGF-β-induced epithelial-mesenchymal transition and metastasis by controlling TIF1γ in non-small cell lung cancer. Mol Cancer. 2018;17:140.PubMedPubMedCentralCrossRef Wang L, Tong X, Zhou Z, Wang S, Lei Z, Zhang T, et al. Circular RNA hsa_circ_0008305 (circPTK2) inhibits TGF-β-induced epithelial-mesenchymal transition and metastasis by controlling TIF1γ in non-small cell lung cancer. Mol Cancer. 2018;17:140.PubMedPubMedCentralCrossRef
83.
go back to reference You J, Li M, Cao LM, Gu QH, Deng PB, Tan Y, et al. Snail1-dependent cancer-associated fibroblasts induce epithelial-mesenchymal transition in lung cancer cells via exosomes. QJM An Int J Med. 2019;112:581–90.CrossRef You J, Li M, Cao LM, Gu QH, Deng PB, Tan Y, et al. Snail1-dependent cancer-associated fibroblasts induce epithelial-mesenchymal transition in lung cancer cells via exosomes. QJM An Int J Med. 2019;112:581–90.CrossRef
84.
go back to reference Zhao X, Wu X, Qian M, Song Y, Wu D, Zhang W. Knockdown of TGF-β1 expression in human umbilical cord mesenchymal stem cells reverts their exosome-mediated EMT promoting effect on lung cancer cells. Cancer Lett. 2018;428:34–44.PubMedCrossRef Zhao X, Wu X, Qian M, Song Y, Wu D, Zhang W. Knockdown of TGF-β1 expression in human umbilical cord mesenchymal stem cells reverts their exosome-mediated EMT promoting effect on lung cancer cells. Cancer Lett. 2018;428:34–44.PubMedCrossRef
85.
go back to reference Wang J, Wu Y, Guo J, Fei X, Yu L, Ma S. Adipocyte-derived exosomes promote lung cancer metastasis by increasing MMP9 activity via transferring MMP3 to lung cancer cells. Oncotarget. 2017;8:81880–91.PubMedPubMedCentralCrossRef Wang J, Wu Y, Guo J, Fei X, Yu L, Ma S. Adipocyte-derived exosomes promote lung cancer metastasis by increasing MMP9 activity via transferring MMP3 to lung cancer cells. Oncotarget. 2017;8:81880–91.PubMedPubMedCentralCrossRef
86.
go back to reference Zhang X, Sai B, Wang F, Wang L, Wang Y, Zheng L, et al. Hypoxic BMSC-derived exosomal miRNAs promote metastasis of lung cancer cells via STAT3-induced EMT. Mol Cancer. 2019;18:40.PubMedPubMedCentralCrossRef Zhang X, Sai B, Wang F, Wang L, Wang Y, Zheng L, et al. Hypoxic BMSC-derived exosomal miRNAs promote metastasis of lung cancer cells via STAT3-induced EMT. Mol Cancer. 2019;18:40.PubMedPubMedCentralCrossRef
87.
go back to reference Wang Q, Li Z, Sun L, Chen B, Zhao Y, Shen B, et al. Platelets enhance the ability of bone-marrow mesenchymal stem cells to promote cancer metastasis. Onco Targets Ther. 2018;11:8251–63.PubMedPubMedCentralCrossRef Wang Q, Li Z, Sun L, Chen B, Zhao Y, Shen B, et al. Platelets enhance the ability of bone-marrow mesenchymal stem cells to promote cancer metastasis. Onco Targets Ther. 2018;11:8251–63.PubMedPubMedCentralCrossRef
89.
go back to reference Milman N, Ginini L, Gil Z. Exosomes and their role in tumorigenesis and anticancer drug resistance. Drug Resist Updat. 2019;45:1–12.PubMedCrossRef Milman N, Ginini L, Gil Z. Exosomes and their role in tumorigenesis and anticancer drug resistance. Drug Resist Updat. 2019;45:1–12.PubMedCrossRef
90.
go back to reference Bach D-H, Hong J-Y, Park HJ, Lee SK. The role of exosomes and miRNAs in drug-resistance of cancer cells. Int J Cancer. 2017;141:220–30.PubMedCrossRef Bach D-H, Hong J-Y, Park HJ, Lee SK. The role of exosomes and miRNAs in drug-resistance of cancer cells. Int J Cancer. 2017;141:220–30.PubMedCrossRef
91.
go back to reference Li S, Yi M, Dong B, Jiao Y, Luo S, Wu K. The roles of exosomes in cancer drug resistance and its therapeutic application. Clin Transl Med. 2020;10: e257.PubMedPubMedCentralCrossRef Li S, Yi M, Dong B, Jiao Y, Luo S, Wu K. The roles of exosomes in cancer drug resistance and its therapeutic application. Clin Transl Med. 2020;10: e257.PubMedPubMedCentralCrossRef
92.
go back to reference Pasquier J, Galas L, Boulangé-Lecomte C, Rioult D, Bultelle F, Magal P, et al. Different modalities of intercellular membrane exchanges mediate cell-to-cell p-glycoprotein transfers in MCF-7 breast cancer cells. J Biol Chem. 2012;287:7374–87.PubMedPubMedCentralCrossRef Pasquier J, Galas L, Boulangé-Lecomte C, Rioult D, Bultelle F, Magal P, et al. Different modalities of intercellular membrane exchanges mediate cell-to-cell p-glycoprotein transfers in MCF-7 breast cancer cells. J Biol Chem. 2012;287:7374–87.PubMedPubMedCentralCrossRef
93.
go back to reference Wang D, Zhao C, Xu F, Zhang A, Jin M, Zhang K, et al. Cisplatin-resistant NSCLC cells induced by hypoxia transmit resistance to sensitive cells through exosomal PKM2. Theranostics. 2021;11:2860–75.PubMedPubMedCentralCrossRef Wang D, Zhao C, Xu F, Zhang A, Jin M, Zhang K, et al. Cisplatin-resistant NSCLC cells induced by hypoxia transmit resistance to sensitive cells through exosomal PKM2. Theranostics. 2021;11:2860–75.PubMedPubMedCentralCrossRef
94.
go back to reference Qin X, Yu S, Zhou L, Shi M, Hu Y, Xu X, et al. Cisplatin-resistant lung cancer cell-derived exosomes increase cisplatin resistance of recipient cells in exosomal miR-100-5p-dependent manner. Int J Nanomed. 2017;12:3721–33.CrossRef Qin X, Yu S, Zhou L, Shi M, Hu Y, Xu X, et al. Cisplatin-resistant lung cancer cell-derived exosomes increase cisplatin resistance of recipient cells in exosomal miR-100-5p-dependent manner. Int J Nanomed. 2017;12:3721–33.CrossRef
95.
go back to reference Chen Q, Jiao D, Wang J, Hu H, Tang X, Chen J, et al. miR-206 regulates cisplatin resistance and EMT in human lung adenocarcinoma cells partly by targeting MET. Oncotarget. 2016;7:24510–26.PubMedPubMedCentralCrossRef Chen Q, Jiao D, Wang J, Hu H, Tang X, Chen J, et al. miR-206 regulates cisplatin resistance and EMT in human lung adenocarcinoma cells partly by targeting MET. Oncotarget. 2016;7:24510–26.PubMedPubMedCentralCrossRef
96.
go back to reference Yuwen D-L, Sheng B-B, Liu J, Wenyu W, Shu Y-Q. MiR-146a-5p level in serum exosomes predicts therapeutic effect of cisplatin in non-small cell lung cancer. Eur Rev Med Pharmacol Sci. 2017;21:2650–8.PubMed Yuwen D-L, Sheng B-B, Liu J, Wenyu W, Shu Y-Q. MiR-146a-5p level in serum exosomes predicts therapeutic effect of cisplatin in non-small cell lung cancer. Eur Rev Med Pharmacol Sci. 2017;21:2650–8.PubMed
97.
go back to reference Lei Y, Guo W, Chen B, Chen L, Gong J, Li W. Tumor-released lncRNA H19 promotes gefitinib resistance via packaging into exosomes in non-small cell lung cancer. Oncol Rep. 2018;40:3438–46.PubMedPubMedCentral Lei Y, Guo W, Chen B, Chen L, Gong J, Li W. Tumor-released lncRNA H19 promotes gefitinib resistance via packaging into exosomes in non-small cell lung cancer. Oncol Rep. 2018;40:3438–46.PubMedPubMedCentral
98.
go back to reference Zhang W, Cai X, Yu J, Lu X, Qian Q, Qian W. Exosome-mediated transfer of lncRNA RP11-838N2.4 promotes erlotinib resistance in non-small cell lung cancer. Int J Oncol. 2018;53:527–38.PubMedPubMedCentral Zhang W, Cai X, Yu J, Lu X, Qian Q, Qian W. Exosome-mediated transfer of lncRNA RP11-838N2.4 promotes erlotinib resistance in non-small cell lung cancer. Int J Oncol. 2018;53:527–38.PubMedPubMedCentral
99.
go back to reference Kumar S, Sharawat SK, Ali A, Gaur V, Malik PS, Kumar S, et al. Identification of differentially expressed circulating serum microRNA for the diagnosis and prognosis of Indian non-small cell lung cancer patients. Curr Probl Cancer. 2020;44: 100540.PubMedCrossRef Kumar S, Sharawat SK, Ali A, Gaur V, Malik PS, Kumar S, et al. Identification of differentially expressed circulating serum microRNA for the diagnosis and prognosis of Indian non-small cell lung cancer patients. Curr Probl Cancer. 2020;44: 100540.PubMedCrossRef
100.
go back to reference Sun S, Chen H, Xu C, Zhang Y, Zhang Q, Chen L, et al. Exosomal miR-106b serves as a novel marker for lung cancer and promotes cancer metastasis via targeting PTEN. Life Sci. 2020;244: 117297.PubMedCrossRef Sun S, Chen H, Xu C, Zhang Y, Zhang Q, Chen L, et al. Exosomal miR-106b serves as a novel marker for lung cancer and promotes cancer metastasis via targeting PTEN. Life Sci. 2020;244: 117297.PubMedCrossRef
101.
go back to reference Jakobsen KR, Paulsen BS, Bæk R, Varming K, Sorensen BS, Jørgensen MM. Exosomal proteins as potential diagnostic markers in advanced non-small cell lung carcinoma. J Extracell Vesicles. 2015;4: 26659.PubMedCrossRef Jakobsen KR, Paulsen BS, Bæk R, Varming K, Sorensen BS, Jørgensen MM. Exosomal proteins as potential diagnostic markers in advanced non-small cell lung carcinoma. J Extracell Vesicles. 2015;4: 26659.PubMedCrossRef
102.
go back to reference Li Y, Zhang Y, Qiu F, Qiu Z. Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC. Electrophoresis. 2011;32:1976–83.PubMedCrossRef Li Y, Zhang Y, Qiu F, Qiu Z. Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC. Electrophoresis. 2011;32:1976–83.PubMedCrossRef
103.
go back to reference Sandfeld-Paulsen B, Jakobsen KR, Bæk R, Folkersen BH, Rasmussen TR, Meldgaard P, et al. Exosomal proteins as diagnostic biomarkers in lung cancer. J Thorac Oncol. 2016;11:1701–10.PubMedCrossRef Sandfeld-Paulsen B, Jakobsen KR, Bæk R, Folkersen BH, Rasmussen TR, Meldgaard P, et al. Exosomal proteins as diagnostic biomarkers in lung cancer. J Thorac Oncol. 2016;11:1701–10.PubMedCrossRef
104.
go back to reference Li L, Li W, Chen N, Zhao H, Xu G, Zhao Y, et al. FLI1 exonic circular RNAs as a novel oncogenic driver to promote tumor metastasis in small cell lung cancer. Clin Cancer Res. 2019;25:1302–17.PubMedCrossRef Li L, Li W, Chen N, Zhao H, Xu G, Zhao Y, et al. FLI1 exonic circular RNAs as a novel oncogenic driver to promote tumor metastasis in small cell lung cancer. Clin Cancer Res. 2019;25:1302–17.PubMedCrossRef
105.
go back to reference Li L, Song W, Yan X, Li A, Zhang X, Li W, et al. Friend leukemia virus integration 1 promotes tumorigenesis of small cell lung cancer cells by activating the miR-17-92 pathway. Oncotarget. 2017;8:41975–87.PubMedPubMedCentralCrossRef Li L, Song W, Yan X, Li A, Zhang X, Li W, et al. Friend leukemia virus integration 1 promotes tumorigenesis of small cell lung cancer cells by activating the miR-17-92 pathway. Oncotarget. 2017;8:41975–87.PubMedPubMedCentralCrossRef
106.
go back to reference Wang H, Feng L, Zheng Y, Li W, Liu L, Xie S, et al. LINC00680 promotes the progression of non-small cell lung cancer and functions as a sponge of miR-410-3p to enhance HMGB1 expression. Onco Targets Ther. 2020;13:8183–96.PubMedPubMedCentralCrossRef Wang H, Feng L, Zheng Y, Li W, Liu L, Xie S, et al. LINC00680 promotes the progression of non-small cell lung cancer and functions as a sponge of miR-410-3p to enhance HMGB1 expression. Onco Targets Ther. 2020;13:8183–96.PubMedPubMedCentralCrossRef
107.
go back to reference Hall RD, Le TM, Haggstrom DE, Gentzler RD. Angiogenesis inhibition as a therapeutic strategy in non-small cell lung cancer (NSCLC). Transl Lung Cancer Res. 2015;4:515–23.PubMedPubMedCentral Hall RD, Le TM, Haggstrom DE, Gentzler RD. Angiogenesis inhibition as a therapeutic strategy in non-small cell lung cancer (NSCLC). Transl Lung Cancer Res. 2015;4:515–23.PubMedPubMedCentral
108.
go back to reference Lammers PE, Horn L. Targeting angiogenesis in advanced non-small cell lung cancer. J Natl Compr Cancer Netw. 2013;11:1235–47.CrossRef Lammers PE, Horn L. Targeting angiogenesis in advanced non-small cell lung cancer. J Natl Compr Cancer Netw. 2013;11:1235–47.CrossRef
109.
go back to reference Xu X, Zhu S, Tao Z, Ye S. High circulating miR-18a, miR-20a, and miR-92a expression correlates with poor prognosis in patients with non-small cell lung cancer. Cancer Med. 2018;7:21–31.PubMedCrossRef Xu X, Zhu S, Tao Z, Ye S. High circulating miR-18a, miR-20a, and miR-92a expression correlates with poor prognosis in patients with non-small cell lung cancer. Cancer Med. 2018;7:21–31.PubMedCrossRef
110.
go back to reference Coelho AL, Araújo A, Gomes M, Catarino R, Marques A, Medeiros R. Circulating Ang-2 mRNA expression levels: looking ahead to a new prognostic factor for NSCLC. PLoS ONE. 2014;9: e90009.PubMedPubMedCentralCrossRef Coelho AL, Araújo A, Gomes M, Catarino R, Marques A, Medeiros R. Circulating Ang-2 mRNA expression levels: looking ahead to a new prognostic factor for NSCLC. PLoS ONE. 2014;9: e90009.PubMedPubMedCentralCrossRef
111.
go back to reference Dong Q, Dong L, Liu S, Kong Y, Zhang M, Wang X. Tumor-derived exosomal eIF4E as a biomarker for survival prediction in patients with non-small cell lung cancer. Med Sci Monit. 2020;26: e923210.PubMedPubMedCentralCrossRef Dong Q, Dong L, Liu S, Kong Y, Zhang M, Wang X. Tumor-derived exosomal eIF4E as a biomarker for survival prediction in patients with non-small cell lung cancer. Med Sci Monit. 2020;26: e923210.PubMedPubMedCentralCrossRef
112.
go back to reference Li J, Yu J, Zhang H, Wang B, Guo H, Bai J, et al. Exosomes-derived MiR-302b suppresses lung cancer cell proliferation and migration via TGFβRII inhibition. Cell Physiol Biochem. 2016;38:1715–26.PubMedCrossRef Li J, Yu J, Zhang H, Wang B, Guo H, Bai J, et al. Exosomes-derived MiR-302b suppresses lung cancer cell proliferation and migration via TGFβRII inhibition. Cell Physiol Biochem. 2016;38:1715–26.PubMedCrossRef
113.
go back to reference Huang W-T, Chong I-W, Chen H-L, Li C-Y, Hsieh C-C, Kuo H-F, et al. Pigment epithelium-derived factor inhibits lung cancer migration and invasion by upregulating exosomal thrombospondin 1. Cancer Lett. 2019;442:287–98.PubMedCrossRef Huang W-T, Chong I-W, Chen H-L, Li C-Y, Hsieh C-C, Kuo H-F, et al. Pigment epithelium-derived factor inhibits lung cancer migration and invasion by upregulating exosomal thrombospondin 1. Cancer Lett. 2019;442:287–98.PubMedCrossRef
114.
go back to reference Broadhead ML, Dass CR, Choong PFM. Cancer cell apoptotic pathways mediated by PEDF: prospects for therapy. Trends Mol Med. 2009;15:461–7.PubMedCrossRef Broadhead ML, Dass CR, Choong PFM. Cancer cell apoptotic pathways mediated by PEDF: prospects for therapy. Trends Mol Med. 2009;15:461–7.PubMedCrossRef
115.
go back to reference Huang X, Ding J, Li Y, Liu W, Ji J, Wang H, et al. Exosomes derived from PEDF modified adipose-derived mesenchymal stem cells ameliorate cerebral ischemia-reperfusion injury by regulation of autophagy and apoptosis. Exp Cell Res. 2018;371:269–77.PubMedCrossRef Huang X, Ding J, Li Y, Liu W, Ji J, Wang H, et al. Exosomes derived from PEDF modified adipose-derived mesenchymal stem cells ameliorate cerebral ischemia-reperfusion injury by regulation of autophagy and apoptosis. Exp Cell Res. 2018;371:269–77.PubMedCrossRef
116.
go back to reference Huang W, Yan Y, Liu Y, Lin M, Ma J, Zhang W, et al. Exosomes with low miR-34c-3p expression promote invasion and migration of non-small cell lung cancer by upregulating integrin α2β1. Signal Transduct Target Ther. 2020;5:39.PubMedPubMedCentralCrossRef Huang W, Yan Y, Liu Y, Lin M, Ma J, Zhang W, et al. Exosomes with low miR-34c-3p expression promote invasion and migration of non-small cell lung cancer by upregulating integrin α2β1. Signal Transduct Target Ther. 2020;5:39.PubMedPubMedCentralCrossRef
117.
go back to reference Liang M, Chen X, Wang L, Qin L, Wang H, Sun Z, et al. Cancer-derived exosomal TRIM59 regulates macrophage NLRP3 inflammasome activation to promote lung cancer progression. J Exp Clin Cancer Res. 2020;39:176.PubMedPubMedCentralCrossRef Liang M, Chen X, Wang L, Qin L, Wang H, Sun Z, et al. Cancer-derived exosomal TRIM59 regulates macrophage NLRP3 inflammasome activation to promote lung cancer progression. J Exp Clin Cancer Res. 2020;39:176.PubMedPubMedCentralCrossRef
118.
go back to reference Xu K, Zhang C, Du T, Gabriel ANA, Wang X, Li X, et al. Progress of exosomes in the diagnosis and treatment of lung cancer. Biomed Pharmacother. 2021;134: 111111.PubMedCrossRef Xu K, Zhang C, Du T, Gabriel ANA, Wang X, Li X, et al. Progress of exosomes in the diagnosis and treatment of lung cancer. Biomed Pharmacother. 2021;134: 111111.PubMedCrossRef
120.
go back to reference Nie H, Xie X, Zhang D, Zhou Y, Li B, Li F, et al. Use of lung-specific exosomes for miRNA-126 delivery in non-small cell lung cancer. Nanoscale. 2020;12:877–87.PubMedCrossRef Nie H, Xie X, Zhang D, Zhou Y, Li B, Li F, et al. Use of lung-specific exosomes for miRNA-126 delivery in non-small cell lung cancer. Nanoscale. 2020;12:877–87.PubMedCrossRef
121.
go back to reference Hao D, Li Y, Zhao G, Zhang M. Soluble fms-like tyrosine kinase-1-enriched exosomes suppress the growth of small cell lung cancer by inhibiting endothelial cell migration. Thorac Cancer. 2019;10:1962–72.PubMedPubMedCentralCrossRef Hao D, Li Y, Zhao G, Zhang M. Soluble fms-like tyrosine kinase-1-enriched exosomes suppress the growth of small cell lung cancer by inhibiting endothelial cell migration. Thorac Cancer. 2019;10:1962–72.PubMedPubMedCentralCrossRef
122.
go back to reference Srivastava A, Amreddy N, Babu A, Panneerselvam J, Mehta M, Muralidharan R, et al. Nanosomes carrying doxorubicin exhibit potent anticancer activity against human lung cancer cells. Sci Rep. 2016;6: 38541.PubMedPubMedCentralCrossRef Srivastava A, Amreddy N, Babu A, Panneerselvam J, Mehta M, Muralidharan R, et al. Nanosomes carrying doxorubicin exhibit potent anticancer activity against human lung cancer cells. Sci Rep. 2016;6: 38541.PubMedPubMedCentralCrossRef
123.
go back to reference Munagala R, Aqil F, Jeyabalan J, Agrawal AK, Mudd AM, Kyakulaga AH, et al. Exosomal formulation of anthocyanidins against multiple cancer types. Cancer Lett. 2017;393:94–102.PubMedPubMedCentralCrossRef Munagala R, Aqil F, Jeyabalan J, Agrawal AK, Mudd AM, Kyakulaga AH, et al. Exosomal formulation of anthocyanidins against multiple cancer types. Cancer Lett. 2017;393:94–102.PubMedPubMedCentralCrossRef
124.
go back to reference Kim MS, Haney MJ, Zhao Y, Yuan D, Deygen I, Klyachko NL, et al. Engineering macrophage-derived exosomes for targeted paclitaxel delivery to pulmonary metastases: in vitro and in vivo evaluations. Nanomedicine. 2018;14:195–204.PubMedCrossRef Kim MS, Haney MJ, Zhao Y, Yuan D, Deygen I, Klyachko NL, et al. Engineering macrophage-derived exosomes for targeted paclitaxel delivery to pulmonary metastases: in vitro and in vivo evaluations. Nanomedicine. 2018;14:195–204.PubMedCrossRef
125.
go back to reference Yu Y, Luo Y, Fang Z, Teng W, Yu Y, Tian J, et al. Mechanism of sanguinarine in inhibiting macrophages to promote metastasis and proliferation of lung cancer via modulating the exosomes in A549 cells. Onco Targets Ther. 2020;13:8989–9003.PubMedPubMedCentralCrossRef Yu Y, Luo Y, Fang Z, Teng W, Yu Y, Tian J, et al. Mechanism of sanguinarine in inhibiting macrophages to promote metastasis and proliferation of lung cancer via modulating the exosomes in A549 cells. Onco Targets Ther. 2020;13:8989–9003.PubMedPubMedCentralCrossRef
126.
go back to reference Sceneay J, Smyth MJ, Möller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 2013;32:449–64.PubMedCrossRef Sceneay J, Smyth MJ, Möller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 2013;32:449–64.PubMedCrossRef
Metadata
Title
The role of exosomes in lung cancer metastasis and clinical applications: an updated review
Authors
Lei Yin
Xiaotian Liu
Xuejun Shao
Tao Feng
Jun Xu
Qi Wang
Shenghao Hua
Publication date
01-12-2021
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2021
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-021-02985-1

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Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.