Generic placeholder image

Current Medicinal Chemistry


ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Review Article

Exosomes and Lung Cancer: Roles in Pathophysiology, Diagnosis and Therapeutic Applications

Author(s): Atefeh Amiri, Mohammad Hossein Pourhanifeh, Hamid Reza Mirzaei, Javid Sadri Nahand, Mohsen Moghoofei, Roxana Sahebnasagh, Hamed Mirzaei* and Michael R. Hamblin*

Volume 28, Issue 2, 2021

Published on: 04 February, 2020

Page: [308 - 328] Pages: 21

DOI: 10.2174/0929867327666200204141952

Price: $65


Lung cancer is a malignancy with a high morbidity and mortality rate, and affected patients have low survival and poor prognosis. The therapeutic approaches for the treatment of this cancer, including radiotherapy and chemotherapy, are not particularly effective partly due to late diagnosis. Therefore, the search for new diagnostic and prognostic tools is a critical issue. Novel biomarkers, such as exosomes, could be considered as potential diagnostic tools for malignancies, particularly lung cancer. Exosomes are nanovesicles, which are associated with different physiological and pathological conditions. It has been shown that these particles are released from many cells, such as cancer cells, immune cells and to some degree normal cells. Exosomes could alter the behavior of target cells through intercellular transfer of their cargo (e.g. DNA, mRNA, long non-coding RNAs, microRNAs and proteins). Thus, these vehicles may play pivotal roles in various physiological and pathological conditions. The current insights into lung cancer pathogenesis suggest that exosomes are key players in the pathogenesis of this cancer. Hence, these nanovesicles and their cargos could be used as new diagnostic, prognostic and therapeutic biomarkers in the treatment of lung cancer. Besides the diagnostic roles of exosomes, their use as drug delivery systems and as cancer vaccines is under investigation. The present review summarizes the current information on the diagnostic and pathogenic functions of exosomes in lung cancer.

Keywords: Exosomes, lung cancer, diagnostic biomarkers, MicroRNAs, drug delivery vehicles, cancer vaccines.

Siegel, R.L.; Miller, K.D.; Jemal, A. Cancer Statistics, 2017. CA Cancer J. Clin., 2017, 67(1), 7-30.
[] [PMID: 28055103]
Sekido, Y.; Fong, K.M.; Minna, J.D. Progress in understanding the molecular pathogenesis of human lung cancer. Biochim. Biophys. Acta, 1998, 1378(1), F21-F59.
[] [PMID: 9739759]
Zochbauer-Muller, S.; Gazdar, A.F.; Minna, J.D. Molecular pathogenesis of lung cancer. Annu. Rev. Physiol., 2002, 64, 681-708.
[] [PMID: 11826285]
Zöchbauer-Müller, S.; Minna, J.D. The biology of lung cancer including potential clinical applications. Chest Surg. Clin. N. Am., 2000, 10(4), 691-708.
[PMID: 11091920]
Herbst, R.S.; Morgensztern, D.; Boshoff, C. The biology and management of non-small cell lung cancer. Nature, 2018, 553(7689), 446-454.
[] [PMID: 29364287]
Witwer, K.W.; Théry, C. Extracellular vesicles or exosomes? On primacy, precision, and popularity influencing a choice of nomenclature; Taylor & Francis, 2019.
van der Pol, E.; Böing, A.N.; Gool, E.L.; Nieuwland, R. Recent developments in the nomenclature, presence, isolation, detection and clinical impact of extracellular vesicles. J. Thromb. Haemost., 2016, 14(1), 48-56.
[] [PMID: 26564379]
Johnstone, R.M.; Adam, M.; Hammond, J.R.; Orr, L.; Turbide, C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem., 1987, 262(19), 9412-9420.
[PMID: 3597417]
Taverna, S.; Giallombardo, M.; Gil-Bazo, I.; Carreca, A.P.; Castiglia, M.; Chacártegui, J.; Araujo, A.; Alessandro, R.; Pauwels, P.; Peeters, M.; Rolfo, C. Exosomes isolation and characterization in serum is feasible in non-small cell lung cancer patients: critical analysis of evidence and potential role in clinical practice. Oncotarget, 2016, 7(19), 28748-28760.
[] [PMID: 26919248]
Bansal, S.; Sharma, M.R.R.; Mohanakumar, T. The role of exosomes in allograft immunity. Cell. Immunol., 2018, 331, 85-92.
[] [PMID: 29907298]
Meehan, B.; Rak, J.; Di Vizio, D. Oncosomes - large and small: what are they, where they came from? J. Extracell. Vesicles, 2016, 5, 33109.
[] [PMID: 27680302]
Cui, S.; Cheng, Z.; Qin, W.; Jiang, L. Exosomes as a liquid biopsy for lung cancer. Lung Cancer, 2018, 116, 46-54.
[] [PMID: 29413050]
Vlassov, A.V.; Magdaleno, S.; Setterquist, R.; Conrad, R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta, 2012, 1820(7), 940-948.
[] [PMID: 22503788]
Masaoutis, C.; Mihailidou, C.; Tsourouflis, G.; Theocharis, S. Exosomes in lung cancer diagnosis and treatment. From the translating research into future clinical practice. Biochimie, 2018, 151, 27-36.
[] [PMID: 29857182]
Lynch, T.J.; Bell, D.W.; Sordella, R.; Gurubhagavatula, S.; Okimoto, R.A.; Brannigan, B.W.; Harris, P.L.; Haserlat, S.M.; Supko, J.G.; Haluska, F.G.; Louis, D.N.; Christiani, D.C.; Settleman, J.; Haber, D.A. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N. Engl. J. Med., 2004, 350(21), 2129-2139.
[] [PMID: 15118073]
Imyanitov, E.N.; Kuligina, E.S.; Belogubova, E.V.; Togo, A.V.; Hanson, K.P. Mechanisms of lung cancer. Drug Discov. Today Dis. Mech., 2005, 2, 213-223.
Costa-Silva, B.; Aiello, N.M.; Ocean, A.J.; Singh, S.; Zhang, H.; Thakur, B.K.; Becker, A.; Hoshino, A.; Mark, M.T.; Molina, H.; Xiang, J.; Zhang, T.; Theilen, T.M.; García-Santos, G.; Williams, C.; Ararso, Y.; Huang, Y.; Rodrigues, G.; Shen, T.L.; Labori, K.J.; Lothe, I.M.; Kure, E.H.; Hernandez, J.; Doussot, A.; Ebbesen, S.H.; Grandgenett, P.M.; Hollingsworth, M.A.; Jain, M.; Mallya, K.; Batra, S.K.; Jarnagin, W.R.; Schwartz, R.E.; Matei, I.; Peinado, H.; Stanger, B.Z.; Bromberg, J.; Lyden, D. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat. Cell Biol., 2015, 17(6), 816-826.
[] [PMID: 25985394]
Melo, S.A.; Sugimoto, H.; O’Connell, J.T.; Kato, N.; Villanueva, A.; Vidal, A.; Qiu, L.; Vitkin, E.; Perelman, L.T.; Melo, C.A.; Lucci, A.; Ivan, C.; Calin, G.A.; Kalluri, R. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell, 2014, 26(5), 707-721.
[] [PMID: 25446899]
Peinado, H.; Alečković, M.; Lavotshkin, S.; Matei, I.; Costa-Silva, B.; Moreno-Bueno, G.; Hergueta-Redondo, M.; Williams, C.; García-Santos, G.; Ghajar, C.; Nitadori-Hoshino, A.; Hoffman, C.; Badal, K.; Garcia, B.A.; Callahan, M.K.; Yuan, J.; Martins, V.R.; Skog, J.; Kaplan, R.N.; Brady, M.S.; Wolchok, J.D.; Chapman, P.B.; Kang, Y.; Bromberg, J.; Lyden, D. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med., 2012, 18(6), 883-891.
[] [PMID: 22635005]
Kalluri, R. The biology and function of exosomes in cancer. J. Clin. Invest., 2016, 126(4), 1208-1215.
[] [PMID: 27035812]
Denzer, K.; Kleijmeer, M.J.; Heijnen, H.F.; Stoorvogel, W.; Geuze, H.J. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci., 2000, 113(Pt 19), 3365-3374.
[PMID: 10984428]
Reclusa, P.; Taverna, S.; Pucci, M.; Durendez, E.; Calabuig, S.; Manca, P.; Serrano, M.J.; Sober, L.; Pauwels, P.; Russo, A.; Rolfo, C. Exosomes as diagnostic and predictive biomarkers in lung cancer. J. Thorac. Dis., 2017, 9(Suppl. 13), S1373-S1382.
[] [PMID: 29184676]
Kowal, J.; Arras, G.; Colombo, M.; Jouve, M.; Morath, J.P.; Primdal-Bengtson, B.; Dingli, F.; Loew, D.; Tkach, M.; Théry, C. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Natl. Acad. Sci. USA, 2016, 113(8), E968-E977.
[] [PMID: 26858453]
Balaj, L.; Lessard, R.; Dai, L.; Cho, Y.J.; Pomeroy, S.L.; Breakefield, X.O.; Skog, J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun., 2011, 2, 180.
[] [PMID: 21285958]
Kahlert, C.; Melo, S.A.; Protopopov, A.; Tang, J.; Seth, S.; Koch, M.; Zhang, J.; Weitz, J.; Chin, L.; Futreal, A.; Kalluri, R. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J. Biol. Chem., 2014, 289(7), 3869-3875.
[] [PMID: 24398677]
Valadi, H.; Ekström, K.; Bossios, A.; Sjöstrand, M.; Lee, J.J.; Lötvall, J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol., 2007, 9(6), 654-659.
[] [PMID: 17486113]
Batrakova, E.V.; Kim, M.S. Using exosomes, naturally-equipped nanocarriers, for drug delivery. J. Control. Release, 2015, 219, 396-405.
[] [PMID: 26241750]
Wiklander, O.P.; Nordin, J.Z.; O’Loughlin, A.; Gustafsson, Y.; Corso, G.; Mäger, I.; Vader, P.; Lee, Y.; Sork, H.; Seow, Y.; Heldring, N.; Alvarez-Erviti, L.; Smith, C.I.; Le Blanc, K.; Macchiarini, P.; Jungebluth, P.; Wood, M.J.; Andaloussi, S.E. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J. Extracell. Vesicles, 2015, 4, 26316.
[] [PMID: 25899407]
Chow, A.; Zhou, W.; Liu, L.; Fong, M.Y.; Champer, J.; Van Haute, D.; Chin, A.R.; Ren, X.; Gugiu, B.G.; Meng, Z.; Huang, W.; Ngo, V.; Kortylewski, M.; Wang, S.E. Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB. Sci. Rep., 2014, 4, 5750.
[] [PMID: 25034888]
Raimondo, S.; Saieva, L.; Corrado, C.; Fontana, S.; Flugy, A.; Rizzo, A.; De Leo, G.; Alessandro, R. Chronic myeloid leukemia-derived exosomes promote tumor growth through an autocrine mechanism. Cell Commun. Signal., 2015, 13, 8.
[] [PMID: 25644060]
Hupfeld, T.; Chapuy, B.; Schrader, V.; Beutler, M.; Veltkamp, C.; Koch, R.; Cameron, S.; Aung, T.; Haase, D.; Larosee, P.; Truemper, L.; Wulf, G.G. Tyrosinekinase inhibition facilitates cooperation of transcription factor SALL4 and ABC transporter A3 towards intrinsic CML cell drug resistance. Br. J. Haematol., 2013, 161(2), 204-213.
[] [PMID: 23432194]
Safaei, R.; Larson, B.J.; Cheng, T.C.; Gibson, M.A.; Otani, S.; Naerdemann, W.; Howell, S.B. Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol. Cancer Ther., 2005, 4(10), 1595-1604.
[] [PMID: 16227410]
Qin, J.; Xu, Q. Functions and application of exosomes. Acta Pol. Pharm., 2014, 71(4), 537-543.
[PMID: 25272880]
Shi, R.; Wang, P-Y.; Li, X-Y.; Chen, J-X.; Li, Y.; Zhang, X-Z.; Zhang, C-G.; Jiang, T.; Li, W-B.; Ding, W.; Cheng, S.J. Exosomal levels of miRNA-21 from cerebrospinal fluids as-sociated with poor prognosis and tumor recurrence of glioma patients. Oncotarget, 2015, 6(29), 26971-26981.
[] [PMID: 26284486]
Logozzi, M.; De Milito, A.; Lugini, L.; Borghi, M.; Calabrò, L.; Spada, M.; Perdicchio, M.; Marino, M.L.; Federici, C.; Iessi, E.; Brambilla, D.; Venturi, G.; Lozupone, F.; Santinami, M.; Huber, V.; Maio, M.; Rivoltini, L.; Fais, S. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One, 2009, 4(4)e5219
[] [PMID: 19381331]
Edge, S.B.; Compton, C.C. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann. Surg Oncol , 2010; 17, pp. (6)1471-1474.
[] [PMID: 20180029]
Wood, S.L.; Pernemalm, M.; Crosbie, P.A.; Whetton, A.D. The role of the tumor-microenvironment in lung cancer-metastasis and its relationship to potential therapeutic targets. Cancer Treat. Rev., 2014, 40(4), 558-566.
[] [PMID: 24176790]
Azmi, A.S.; Bao, B.; Sarkar, F.H. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev., 2013, 32(3-4), 623-642.
[] [PMID: 23709120]
Rahman, M.A.; Barger, J.F.; Lovat, F.; Gao, M.; Otterson, G.A.; Nana-Sinkam, P. Lung cancer exosomes as drivers of epithelial mesenchymal transition. Oncotarget, 2016, 7(34), 54852-54866.
[] [PMID: 27363026]
Munagala, R.; Aqil, F.; Gupta, R.C. Exosomal miRNAs as biomarkers of recurrent lung cancer. Tumour Biol., 2016, 37(8), 10703-10714.
[] [PMID: 26867772]
D’Amico, T.A.; Massey, M.; Herndon, J.E. II.; Moore, M.B.; Harpole, D.H.Jr. A biologic risk model for stage I lung cancer: immunohistochemical analysis of 408 patients with the use of ten molecular markers. J. Thorac. Cardiovasc. Surg., 1999, 117(4), 736-743.
[] [PMID: 10096969]
Liang, Y.; Guo, S.; Zhou, Q. Prognostic value of matrix metalloproteinase-7 expression in patients with non-small cell lung cancer. Tumour Biol., 2014, 35(4), 3717-3724.
[] [PMID: 24338766]
Passlick, B.; Sienel, W.; Seen-Hibler, R.; Wöckel, W.; Thetter, O.; Mutschler, W.; Pantel, K. Overexpression of matrix metalloproteinase 2 predicts unfavorable outcome in early-stage non-small cell lung cancer. Clin. Cancer Res., 2000, 6(10), 3944-3948.
[PMID: 11051242]
Qian, Q.; Wang, Q.; Zhan, P.; Peng, L.; Wei, S.Z.; Shi, Y.; Song, Y. The role of matrix metalloproteinase 2 on the survival of patients with non-small cell lung cancer: a systematic review with meta-analysis. Cancer Invest., 2010, 28(6), 661-669.
[] [PMID: 20394501]
Larsen, J.E.; Minna, J.D. Molecular biology of lung cancer: clinical implications. Clin. Chest Med., 2011, 32(4), 703-740.
[] [PMID: 22054881]
Ribeiro, M.F.; Zhu, H.; Millard, R.W.; Fan, G-C. Exosomes function in pro- and anti-angiogenesis. Curr. Angiogenes., 2013, 2(1), 54-59.
[] [PMID: 25374792]
Ferrara, N. Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev., 2004, 25(4), 581-611.
[] [PMID: 15294883]
Zheng, C-L.; Qiu, C.; Shen, M-X.; Qu, X.; Zhang, T-H.; Zhang, J-H.; Du, J-J. Prognostic impact of elevation of vascular endothelial growth factor family expression in patients with non-small cell lung cancer: an updated meta-analysis. Asian Pac. J. Cancer Prev., 2015, 16(5), 1881-1895.
[] [PMID: 25773840]
Liu, Y.; Luo, F.; Wang, B.; Li, H.; Xu, Y.; Liu, X.; Shi, L.; Lu, X.; Xu, W.; Lu, L.; Qin, Y.; Xiang, Q.; Liu, Q. STAT3-regulated exosomal miR-21 promotes angiogenesis and is involved in neoplastic processes of transformed human bronchial epithelial cells. Cancer Lett., 2016, 370(1), 125-135.
[] [PMID: 26525579]
Hsu, Y-L.; Hung, J-Y.; Chang, W-A.; Lin, Y-S.; Pan, Y-C.; Tsai, P-H.; Wu, C-Y.; Kuo, P-L. Hypoxic lung cancer-secreted exosomal miR-23a increased angiogenesis and vascular permeability by targeting prolyl hydroxylase and tight junction protein ZO-1. Oncogene, 2017, 36(34), 4929-4942.
[] [PMID: 28436951]
Clark, D.J.; Fondrie, W.E.; 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, 161-169.
[] [PMID: 26739763]
Yamashita, T.; Kamada, H.; Kanasaki, S.; Maeda, Y.; Nagano, K.; Abe, Y.; Inoue, M.; Yoshioka, Y.; Tsutsumi, Y.; Katayama, S.; Inoue, M.; Tsunoda, S. Epidermal growth factor receptor localized to exosome membranes as a possible biomarker for lung cancer diagnosis. Pharmazie, 2013, 68(12), 969-973.
[PMID: 24400444]
Abou-Seri, S.M. Synthesis and biological evaluation of novel 2,4′-bis substituted diphenylamines as anticancer agents and potential epidermal growth factor receptor tyrosine kinase inhibitors. Eur. J. Med. Chem., 2010, 45(9), 4113-4121.
[] [PMID: 20580136]
Gullick, W.J. Prevalence of aberrant expression of the epidermal growth factor receptor in human cancers. Br. Med. Bull., 1991, 47(1), 87-98.
[] [PMID: 1863851]
Cui, H.; Seubert, B.; Stahl, E.; Dietz, H.; Reuning, U.; Moreno-Leon, L.; Ilie, M.; Hofman, P.; Nagase, H.; Mari, B.; Krüger, A. Tissue inhibitor of metalloproteinases-1 induces a pro-tumourigenic increase of miR-210 in lung adenocarcinoma cells and their exosomes. Oncogene, 2015, 34(28), 3640-3650.
[] [PMID: 25263437]
Wu, H.; Zhou, J.; Mei, S.; Wu, D.; Mu, Z.; Chen, B.; Xie, Y.; Ye, Y.; Liu, J. Circulating exosomal microRNA-96 promotes cell proliferation, migration and drug resistance by targeting LMO7. J. Cell. Mol. Med., 2017, 21(6), 1228-1236.
[] [PMID: 28026121]
Lobb, R.J.; van Amerongen, R.; Wiegmans, A.; Ham, S.; Larsen, J.E.; Möller, A. Exosomes derived from mesenchymal non-small cell lung cancer cells promote chemoresistance. Int. J. Cancer, 2017, 141(3), 614-620.
[] [PMID: 28445609]
Vanni, I.; Alama, A.; Grossi, F.; Dal Bello, M.G.; Coco, S. Exosomes: a new horizon in lung cancer. Drug Discov. Today, 2017, 22(6), 927-936.
[] [PMID: 28288782]
Alipoor, S.D.; Mortaz, E.; Garssen, J.; Movassaghi, M.; Mirsaeidi, M.; Adcock, I.M. Exosomes and exosomal miRNA in respiratory diseases. Mediators Inflamm., 2016, 20165628404
[] [PMID: 27738390]
Silva, J.; García, V.; Zaballos, Á.; Provencio, M.; Lombardía, L.; Almonacid, L.; García, J.M.; Domínguez, G.; Peña, C.; Diaz, R.; Herrera, M.; Varela, A.; Bonilla, F. Vesicle-related microRNAs in plasma of nonsmall cell lung cancer patients and correlation with survival. Eur. Respir. J., 2011, 37(3), 617-623.
[] [PMID: 20595154]
Cazzoli, R.; Buttitta, F.; Di Nicola, M.; Malatesta, S.; Marchetti, A.; Rom, W.N.; Pass, H.I. microRNAs derived from circulating exosomes as noninvasive biomarkers for screening and diagnosing lung cancer. J. Thorac. Oncol., 2013, 8(9), 1156-1162.
[] [PMID: 23945385]
Zhou, X.; Wen, W.; Shan, X.; Zhu, W.; Xu, J.; Guo, R.; Cheng, W.; Wang, F.; Qi, L.W.; Chen, Y.; Huang, Z.; Wang, T.; Zhu, D.; Liu, P.; Shu, Y. A six-microRNA panel in plasma was identified as a potential biomarker for lung adenocarcinoma diagnosis. Oncotarget, 2017, 8(4), 6513-6525.
[] [PMID: 28036284]
Rolfo, C.; Chacartegui, J.; Giallombardo, M.; Alessandro, R.; Peeters, M. 71P Exosomes isolated in plasma of non-small cell lung cancer patients contain microRNA related to the EGFR pathway: proof of concept. J. Thorac. Oncol., 2016, 11, S85.
Jin, X.; Chen, Y.; Chen, H.; Fei, S.; Chen, D.; Cai, X.; Liu, L.; Lin, B.; Su, H.; Zhao, L.; Su, M.; Pan, H.; Shen, L.; Xie, D.; Xie, C. Evaluation of tumor-derived exosomal mirna as potential diagnostic biomarkers for early-stage non-small cell lung cancer using next-generation sequencing. Clin. Cancer Res., 2017, 23(17), 5311-5319.
[] [PMID: 28606918]
Wang, Z.; Chen, J.Q.; Liu, J.L.; Tian, L. Exosomes in tumor microenvironment: novel transporters and biomarkers. J. Transl. Med., 2016, 14(1), 297.
[] [PMID: 27756426]
Liu, Q.; Yu, Z.; Yuan, S.; Xie, W.; Li, C.; Hu, Z.; Xiang, Y.; Wu, N.; Wu, L.; Bai, L.; Li, Y. Circulating exosomal microRNAs as prognostic biomarkers for non-small-cell lung cancer. Oncotarget, 2017, 8(8), 13048-13058.
[] [PMID: 28055956]
Zhang, J.; Li, S.; Li, L.; Li, M.; Guo, C.; Yao, J.; Mi, S. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics, 2015, 13(1), 17-24.
[] [PMID: 25724326]
Lin, J.; Li, J.; Huang, B.; Liu, J.; Chen, X.; Chen, X-M.; Xu, Y-M.; Huang, L-F.; Wang, X-Z. Exosomes: novel biomarkers for clinical diagnosis. Sci World J., 2015, 2015657086
[] [PMID: 25695100]
van Dommelen, S.M.; Vader, P.; Lakhal, S.; Kooijmans, S.A.; van Solinge, W.W.; Wood, M.J.; Schiffelers, R.M. Microvesicles and exosomes: opportunities for cell-derived membrane vesicles in drug delivery. J. Control. Release, 2012, 161(2), 635-644.
[] [PMID: 22138068]
Schey, K.L.; Luther, J.M.; Rose, K.L. Proteomics characterization of exosome cargo. Methods, 2015, 87, 75-82.
[] [PMID: 25837312]
Sandfeld-Paulsen, B.; Jakobsen, K.R.; Bæk, R.; Folkersen, B.H.; Rasmussen, T.R.; Meldgaard, P.; Varming, K.; Jørgensen, M.M.; Sorensen, B.S. Exosomal proteins as diagnostic biomarkers in lung cancer. J. Thorac. Oncol., 2016, 11(10), 1701-1710.
[] [PMID: 27343445]
Jakobsen, K.R.; Paulsen, B.S.; Bæk, R.; Varming, K.; Sorensen, B.S.; Jørgensen, M.M. Exosomal proteins as potential diagnostic markers in advanced non-small cell lung carcinoma. J. Extracell. Vesicles, 2015, 4, 26659.
[] [PMID: 25735706]
Rabinowits, G.; Gerçel-Taylor, C.; Day, J.M.; Taylor, D.D.; Kloecker, G.H. Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer, 2009, 10(1), 42-46.
[] [PMID: 19289371]
Dejima, H.; Iinuma, H.; Kanaoka, R.; Matsutani, N.; Kawamura, M. Exosomal microRNA in plasma as a non-invasive biomarker for the recurrence of non-small cell lung cancer. Oncol. Lett., 2017, 13(3), 1256-1263.
[] [PMID: 28454243]
Rodríguez, M.; Silva, J.; López-Alfonso, A.; López-Muñiz, M.B.; Peña, C.; Domínguez, G.; García, J.M.; López-Gónzalez, A.; Méndez, M.; Provencio, M.; García, V.; Bonilla, F. Different exosome cargo from plasma/bronchoalveolar lavage in non-small-cell lung cancer. Genes Chromos Cancer, 2014, 53(9), 713-724.
[] [PMID: 24764226]
Giallombardo, M.; Chacártegui Borrás, J.; Castiglia, M.; Van Der Steen, N.; Mertens, I.; Pauwels, P.; Peeters, M.; Rolfo, C. Exosomal miRNA analysis in non-small cell lung cancer (NSCLC) patients’ plasma through qPCR: a feasible liquid biopsy tool. J. Vis. Exp., 2016, (111), 53900.
[] [PMID: 27285610]
Wang, Y.; Xu, Y.M.; Zou, Y.Q.; Lin, J.; Huang, B.; Liu, J.; Li, J.; Zhang, J.; Yang, W.M.; Min, Q.H.; Li, S.Q.; Gao, Q.F.; Sun, F.; Chen, Q.G.; Zhang, L.; Jiang, Y.H.; Deng, L.B.; Wang, X.Z. Identification of differential expressed PE exosomal miRNA in lung adenocarcinoma, tuberculosis, and other benign lesions. Medicine (Baltimore), 2017, 96(44)e8361
[] [PMID: 29095265]
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(11), 2650-2658.
[PMID: 28678319]
Qin, X.; Yu, S.; Xu, X.; Shen, B.; Feng, J. Comparative analysis of microRNA expression profiles between A549, A549/DDP and their respective exosomes. Oncotarget, 2017, 8(26), 42125-42135.
[] [PMID: 28178672]
Dinh, T.K.; Fendler, W.; Chałubińska-Fendler, J.; Acharya, S.S.; O’Leary, C.; Deraska, P.V.; D’Andrea, A.D.; Chowdhury, D.; Kozono, D. Circulating miR-29a and miR-150 correlate with delivered dose during thoracic radiation therapy for non-small cell lung cancer. Radiat. Oncol., 2016, 11, 61.
[] [PMID: 27117590]
Aushev, V.N.; Zborovskaya, I.B.; Laktionov, K.K.; Girard, N.; Cros, M.P.; Herceg, Z.; Krutovskikh, V. Comparisons of microRNA patterns in plasma before and after tumor removal reveal new biomarkers of lung squamous cell carcinoma. PLoS One, 2013, 8(10)e78649
[] [PMID: 24130905]
Rolfo, C.; Laes, J.F.; Reclusa, P.; Valentino, A.; Lienard, M.; Gil-Bazo, I.; Malapelle, U.; Sirera, R.; Rocco, D.; Van Meerbeeck, J. P2. 01-093 Exo-ALK proof of concept: exosomal analysis of ALK alterations in advanced NSCLC patients: topic: targets for treatment prediction. J. Thorac. Oncol., 2017, 12, S844-S845.
Krug, A.K.; Karlovich, C.; Koestler, T.; Brinkmann, K.; Spiel, A.; Emenegger, J.; Noerholm, M.; O’Neill, V.; Sequist, L.V.; Soria, J-C. Abstract B136: Plasma EGFR mutation detection using a combined exosomal RNA and circulating tumor DNA approach in patients with acquired resistance to first-generation EGFR-TKIs. Mol. Cancer Ther., 2015, 14(12)(Suppl. 2), B136-B136.
Zhang, R.; Xia, Y.; Wang, Z.; Zheng, J.; Chen, Y.; Li, X.; Wang, Y.; Ming, H. Serum long non coding RNA MALAT-1 protected by exosomes is up-regulated and promotes cell proliferation and migration in non-small cell lung cancer. Biochem. Biophys. Res. Commun., 2017, 490(2), 406-414.
[] [PMID: 28623135]
Thakur, B.K.; Zhang, H.; Becker, A.; Matei, I.; Huang, Y.; Costa-Silva, B.; Zheng, Y.; Hoshino, A.; Brazier, H.; Xiang, J.; Williams, C.; Rodriguez-Barrueco, R.; Silva, J.M.; Zhang, W.; Hearn, S.; Elemento, O.; Paknejad, N.; Manova-Todorova, K.; Welte, K.; Bromberg, J.; Peinado, H.; Lyden, D. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res., 2014, 24(6), 766-769.
[] [PMID: 24710597]
Al-Nedawi, K.; Meehan, B.; Kerbel, R.S.; Allison, A.C.; Rak, J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc. Natl. Acad. Sci. USA, 2009, 106(10), 3794-3799.
[] [PMID: 19234131]
Sandfeld-Paulsen, B.; Aggerholm-Pedersen, N.; Bæk, R.; Jakobsen, K.R.; Meldgaard, P.; Folkersen, B.H.; Rasmussen, T.R.; Varming, K.; Jørgensen, M.M.; Sorensen, B.S. Exosomal proteins as prognostic biomarkers in non-small cell lung cancer. Mol. Oncol., 2016, 10(10), 1595-1602.
[] [PMID: 27856179]
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(2), 1527-1530.
[] [PMID: 26893774]
Li, X.; Wang, S.; Zhu, R.; Li, H.; Han, Q.; Zhao, R.C. Lung tumor exosomes induce a pro-inflammatory phenotype in mesenchymal stem cells via NFκB-TLR signaling pathway. J. Hematol. Oncol., 2016, 9, 42.
[] [PMID: 27090786]
Xiao, H.; Lässer, C.; Shelke, G.V.; Wang, J.; Rådinger, M.; Lunavat, T.R.; Malmhäll, C.; Lin, L.H.; Li, J.; Li, L.; Lötvall, J. Mast cell exosomes promote lung adenocarcinoma cell proliferation - role of KIT-stem cell factor signaling. Cell Commun. Signal., 2014, 12, 64.
[] [PMID: 25311367]
Taverna, S.; Pucci, M.; Giallombardo, M.; Di Bella, M.A.; Santarpia, M.; Reclusa, P.; Gil-Bazo, I.; Rolfo, C.; Alessandro, R. Amphiregulin contained in NSCLC-exosomes induces osteoclast differentiation through the activation of EGFR pathway. Sci. Rep., 2017, 7(1), 3170.
[] [PMID: 28600504]
Ishida, T.; Kiwada, H. Accelerated blood clearance (ABC) phenomenon upon repeated injection of PEGylated liposomes. Int. J. Pharm., 2008, 354(1-2), 56-62.
[] [PMID: 18083313]
Xu, X.; Ho, W.; Zhang, X.; Bertrand, N.; Farokhzad, O. Cancer nanomedicine: from targeted delivery to combination therapy. Trends Mol. Med., 2015, 21(4), 223-232.
[] [PMID: 25656384]
Johnsen, K.B.; Gudbergsson, J.M.; Skov, M.N.; Pilgaard, L.; Moos, T.; Duroux, M. A comprehensive overview of exosomes as drug delivery vehicles - endogenous nanocarriers for targeted cancer therapy. Biochim. Biophys. Acta, 2014, 1846(1), 75-87.
[PMID: 24747178]
Manoochehri, H.; Sheykhhasan, M.; Pourjafar, M.; Saidijam, M. Exosomes and their role in cancer development, diagnosis and therapy. Research in molecular medicine; RMM, 2018, pp. 1-4.
Katakowski, M.; Buller, B.; Zheng, X.; Lu, Y.; Rogers, T.; Osobamiro, O.; Shu, W.; Jiang, F.; Chopp, M. Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett., 2013, 335(1), 201-204.
[] [PMID: 23419525]
Ohno, S.; Takanashi, M.; Sudo, K.; Ueda, S.; Ishikawa, A.; Matsuyama, N.; Fujita, K.; Mizutani, T.; Ohgi, T.; Ochiya, T.; Gotoh, N.; Kuroda, M. Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol. Ther., 2013, 21(1), 185-191.
[] [PMID: 23032975]
Munoz, J.L.; Bliss, S.A.; Greco, S.J.; Ramkissoon, S.H.; Ligon, K.L.; Rameshwar, P. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol. Ther. Nucleic Acids, 2013, 2(10)e126
[] [PMID: 24084846]
Marleau, A.M.; Chen, C.S.; Joyce, J.A.; Tullis, R.H. Exosome removal as a therapeutic adjuvant in cancer. J. Transl. Med., 2012, 10, 134.
[] [PMID: 22738135]
Ichim, T.E.; Zhong, Z.; Kaushal, S.; Zheng, X.; Ren, X.; Hao, X.; Joyce, J.A.; Hanley, H.H.; Riordan, N.H.; Koropatnick, J.; Bogin, V.; Minev, B.R.; Min, W.P.; Tullis, R.H. Exosomes as a tumor immune escape mechanism: possible therapeutic implications. J. Transl. Med., 2008, 6, 37.
[] [PMID: 18644158]
Federici, C.; Petrucci, F.; Caimi, S.; Cesolini, A.; Logozzi, M.; Borghi, M.; D’Ilio, S.; Lugini, L.; Violante, N.; Azzarito, T.; Majorani, C.; Brambilla, D.; Fais, S. Exosome release and low pH belong to a framework of resistance of human melanoma cells to cisplatin. PLoS One, 2014, 9(2)e88193
[] [PMID: 24516610]
Fabbri, M.; Paone, A.; Calore, F.; Galli, R.; Gaudio, E.; Santhanam, R.; Lovat, F.; Fadda, P.; Mao, C.; Nuovo, G.J.; Zanesi, N.; Crawford, M.; Ozer, G.H.; Wernicke, D.; Alder, H.; Caligiuri, M.A.; Nana-Sinkam, P.; Perrotti, D.; Croce, C.M. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA, 2012, 109(31), E2110-E2116.
[] [PMID: 22753494]
Savina, A.; Furlán, M.; Vidal, M.; Colombo, M.I. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem., 2003, 278(22), 20083-20090.
[] [PMID: 12639953]
Combes, V.; Latham, S.L.; Wen, B.; Allison, A.C.; Grau, G.E. Diannexin down-modulates TNF-induced endothelial microparticle release by blocking membrane budding process. Int. J. Innov. Med. Health Sci., 2016, 7, 1-11.
[] [PMID: 28149531]
Ostrowski, M.; Carmo, N.B.; Krumeich, S.; Fanget, I.; Raposo, G.; Savina, A.; Moita, C.F.; Schauer, K.; Hume, A.N.; Freitas, R.P.; Goud, B.; Benaroch, P.; Hacohen, N.; Fukuda, M.; Desnos, C.; Seabra, M.C.; Darchen, F.; Amigorena, S.; Moita, L.F.; Thery, C. Rab27a and Rab27b control different steps of the exosome secretion pathway.Nat. Cell Biol., 2010, 12(1)19-30, 1-13.
[] [PMID: 19966785]
Villarroya-Beltri, C.; Baixauli, F.; Mittelbrunn, M.; Fernandez-Delgado, I.; Torralba, D. ISGylation controls exosome secretion by promoting lysosomal degradation of MVB proteins. Nat. Commun., 2016, 24(7), 13588.
[] [PMID: 27882925]
Villarroya-Beltri, C.; Guerra, S.; Sánchez-Madrid, F. ISGylation - a key to lock the cell gates for preventing the spread of threats. J. Cell Sci., 2017, 130(18), 2961-2969.
[] [PMID: 28842471]
Baietti, M.F.; Zhang, Z.; Mortier, E.; Melchior, A.; Degeest, G.; Geeraerts, A.; Ivarsson, Y.; Depoortere, F.; Coomans, C.; Vermeiren, E.; Zimmermann, P.; David, G. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat. Cell Biol., 2012, 14(7), 677-685.
[] [PMID: 22660413]
Yang, G.; Zhang, W.; Yu, C.; Ren, J.; An, Z. MicroRNA let-7: Regulation, single nucleotide polymorphism, and therapy in lung cancer. J. Cancer Res. Ther., 2015, 11(Suppl. 1), C1-C6.
[] [PMID: 26323902]
Nishida-Aoki, N.; Tominaga, N.; Takeshita, F.; Sonoda, H.; Yoshioka, Y.; Ochiya, T. Disruption of circulating extracellular vesicles as a novel therapeutic strategy against cancer metastasis. Mol. Ther., 2017, 25(1), 181-191.
[] [PMID: 28129113]
Zhu, D.E.; Höti, N.; Song, Z.; Jin, L.; Wu, Z.; Wu, Q.; Wu, M. Suppression of tumor growth using a recombinant adenoviral vector carrying the dominant-negative mutant gene Survivin-D53A in a nude mice model. Cancer Gene Ther., 2006, 13(8), 762-770.
[] [PMID: 16543917]
Tian, H.; Liu, S.; Zhang, J.; Zhang, S.; Cheng, L.; Li, C.; Zhang, X.; Dail, L.; Fan, P.; Dai, L.; Yan, N.; Wang, R.; Wei, Y.; Deng, H. Enhancement of cisplatin sensitivity in lung cancer xenografts by liposome-mediated delivery of the plasmid expressing small hairpin RNA targeting Survivin. J. Biomed. Nanotechnol., 2012, 8(4), 633-641.
[] [PMID: 22852473]
Li, J.; Yu, J.; Zhang, H.; Wang, B.; Guo, H.; Bai, J.; Wang, J.; Dong, Y.; Zhao, Y.; Wang, Y. Exosomes-derived MiR-302b suppresses lung cancer cell proliferation and migration via TGFβRII inhibition. Cell. Physiol. Biochem., 2016, 38(5), 1715-1726.
[] [PMID: 27160836]
Alvarez-Erviti, L.; Seow, Y.; Yin, H.; Betts, C.; Lakhal, S.; Wood, M.J. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol., 2011, 29(4), 341-345.
[] [PMID: 21423189]
Chen, L.; Charrier, A.; Zhou, Y.; Chen, R.; Yu, B.; Agarwal, K.; Tsukamoto, H.; Lee, L.J.; Paulaitis, M.E.; Brigstock, D.R. Epigenetic regulation of connective tissue growth factor by MicroRNA-214 delivery in exosomes from mouse or human hepatic stellate cells. Hepatology, 2014, 59(3), 1118-1129.
[] [PMID: 24122827]
Bryniarski, K.; Ptak, W.; Jayakumar, A.; Püllmann, K.; Caplan, M.J.; Chairoungdua, A.; Lu, J.; Adams, B.D.; Sikora, E.; Nazimek, K.; Marquez, S.; Kleinstein, S.H.; Sangwung, P.; Iwakiri, Y.; Delgato, E.; Redegeld, F.; Blokhuis, B.R.; Wojcikowski, J.; Daniel, A.W.; Groot Kormelink, T.; Askenase, P.W. Antigen-specific, antibody-coated, exosome-like nanovesicles deliver suppressor T-cell microRNA-150 to effector T cells to inhibit contact sensitivity. J. Allergy Clin. Immunol., 2013, 132(1), 170-181.
[] [PMID: 23727037]
Zhang, Y.; Liu, D.; Chen, X.; Li, J.; Li, L.; Bian, Z.; Sun, F.; Lu, J.; Yin, Y.; Cai, X.; Sun, Q.; Wang, K.; Ba, Y.; Wang, Q.; Wang, D.; Yang, J.; Liu, P.; Xu, T.; Yan, Q.; Zhang, J.; Zen, K.; Zhang, C.Y. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol. Cell, 2010, 39(1), 133-144.
[] [PMID: 20603081]
Kosaka, N.; Iguchi, H.; Yoshioka, Y.; Hagiwara, K.; Takeshita, F.; Ochiya, T. Competitive interactions of cancer cells and normal cells via secretory microRNAs. J. Biol. Chem., 2012, 287(2), 1397-1405.
[] [PMID: 22123823]
Pan, Q.; Ramakrishnaiah, V.; Henry, S.; Fouraschen, S.; de Ruiter, P.E.; Kwekkeboom, J.; Tilanus, H.W.; Janssen, H.L.; van der Laan, L.J. Hepatic cell-to-cell transmission of small silencing RNA can extend the therapeutic reach of RNA interference (RNAi). Gut, 2012, 61(9), 1330-1339.
[] [PMID: 22198713]
Xin, H.; Li, Y.; Buller, B.; Katakowski, M.; Zhang, Y.; Wang, X.; Shang, X.; Zhang, Z.G.; Chopp, M. Exosome-mediated transfer of miR-133b from multipotent mesenchymal stromal cells to neural cells contributes to neurite outgrowth. Stem Cells, 2012, 30(7), 1556-1564.
[] [PMID: 22605481]
Wahlgren, J.; De, L. Karlson, T.; Brisslert, M.; Vaziri Sani, F.; Telemo, E.; Sunnerhagen, P.; Valadi, H. Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes. Nucleic Acids Res., 2012, 40(17)e130
[] [PMID: 22618874]
Shtam, T.A.; Kovalev, R.A.; Varfolomeeva, E.Y.; Makarov, E.M.; Kil, Y.V.; Filatov, M.V. Exosomes are natural carriers of exogenous siRNA to human cells in vitro. Cell Commun. Signal., 2013, 11, 88.
[] [PMID: 24245560]
Zhuang, X.; Xiang, X.; Grizzle, W.; Sun, D.; Zhang, S.; Axtell, R.C.; Ju, S.; Mu, J.; Zhang, L.; Steinman, L.; Miller, D.; Zhang, H.G. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol. Ther., 2011, 19(10), 1769-1779.
[] [PMID: 21915101]
Sun, D.; Zhuang, X.; Xiang, X.; Liu, Y.; Zhang, S.; Liu, C.; Barnes, S.; Grizzle, W.; Miller, D.; Zhang, H-G. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol. Ther., 2010, 18(9), 1606-1614.
[] [PMID: 20571541]
Mizrak, A.; Bolukbasi, M.F.; Ozdener, G.B.; Brenner, G.J.; Madlener, S.; Erkan, E.P.; Ströbel, T.; Breakefield, X.O.; Saydam, O. Genetically engineered microvesicles carrying suicide mRNA/protein inhibit schwannoma tumor growth. Mol. Ther., 2013, 21(1), 101-108.
[] [PMID: 22910294]
Maguire, C.A.; Balaj, L.; Sivaraman, S.; Crommentuijn, M.H.; Ericsson, M.; Mincheva-Nilsson, L.; Baranov, V.; Gianni, D.; Tannous, B.A.; Sena-Esteves, M.; Breakefield, X.O.; Skog, J. Microvesicle-associated AAV vector as a novel gene delivery system. Mol. Ther., 2012, 20(5), 960-971.
[] [PMID: 22314290]
Tian, Y.; Li, S.; Song, J.; Ji, T.; Zhu, M.; Anderson, G.J.; Wei, J.; Nie, G. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials, 2014, 35(7), 2383-2390.
[] [PMID: 24345736]
Jang, S.C.; Kim, O.Y.; Yoon, C.M.; Choi, D-S.; Roh, T-Y.; Park, J.; Nilsson, J.; Lötvall, J.; Kim, Y-K.; Gho, Y.S. Bioinspired exosome-mimetic nanovesicles for targeted delivery of chemotherapeutics to malignant tumors. ACS Nano, 2013, 7(9), 7698-7710.
[] [PMID: 24004438]
Koos, D.; Josephs, S.F.; Alexandrescu, D.T.; Chan, R.C.; Ramos, F.; Bogin, V.; Gammill, V.; Dasanu, C.A.; De Necochea-Campion, R.; Riordan, N.H.; Carrier, E. Tumor vaccines in 2010: need for integration. Cell. Immunol., 2010, 263(2), 138-147.
[] [PMID: 20434139]
Sasada, T.; Komatsu, N.; Suekane, S.; Yamada, A.; Noguchi, M.; Itoh, K. Overcoming the hurdles of randomised clinical trials of therapeutic cancer vaccines. Eur. J. Cancer, 2010, 46(9), 1514-1519.
[] [PMID: 20413296]
Tanne, J.H. FDA approves prostate cancer “vaccine”. BMJ, 2010, 340, c2431.
[] [PMID: 20442242]
Théry, C.; Ostrowski, M.; Segura, E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol., 2009, 9(8), 581-593.
[] [PMID: 19498381]
Bu, N.; Li, Q.L.; Feng, Q.; Sun, B.Z. Immune protection effect of exosomes against attack of L1210 tumor cells. Leuk. Lymphoma, 2006, 47(5), 913-918.
[] [PMID: 16753878]
Andre, F.; Schartz, N.E.; Movassagh, M.; Flament, C.; Pautier, P.; Morice, P.; Pomel, C.; Lhomme, C.; Escudier, B.; Le Chevalier, T.; Tursz, T.; Amigorena, S.; Raposo, G.; Angevin, E.; Zitvogel, L. Malignant effusions and immunogenic tumour-derived exosomes. Lancet, 2002, 360(9329), 295-305.
[] [PMID: 12147373]
Cho, J.A.; Yeo, D.J.; Son, H.Y.; Kim, H.W.; Jung, D.S.; Ko, J.K.; Koh, J.S.; Kim, Y.N.; Kim, C.W. Exosomes: a new delivery system for tumor antigens in cancer immunotherapy. Int. J. Cancer, 2005, 114(4), 613-622.
[] [PMID: 15609328]
Cho, J.A.; Lee, Y.S.; Kim, S.H.; Ko, J.K.; Kim, C.W. MHC independent anti-tumor immune responses induced by Hsp70-enriched exosomes generate tumor regression in murine models. Cancer Lett., 2009, 275(2), 256-265.
[] [PMID: 19036499]
Xie, Y.; Bai, O.; Zhang, H.; Yuan, J.; Zong, S.; Chibbar, R.; Slattery, K.; Qureshi, M.; Wei, Y.; Deng, Y.; Xiang, J. Membrane-bound HSP70-engineered myeloma cell-derived exosomes stimulate more efficient CD8(+) CTL- and NK-mediated antitumour immunity than exosomes released from heat-shocked tumour cells expressing cytoplasmic HSP70. J. Cell. Mol. Med., 2010, 14(11), 2655-2666.
[] [PMID: 19627400]
Zeelenberg, I.S.; Ostrowski, M.; Krumeich, S.; Bobrie, A.; Jancic, C.; Boissonnas, A.; Delcayre, A.; Le Pecq, J.B.; Combadière, B.; Amigorena, S.; Théry, C. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res., 2008, 68(4), 1228-1235.
[] [PMID: 18281500]
Ristorcelli, E.; Beraud, E.; Mathieu, S.; Lombardo, D.; Verine, A. Essential role of Notch signaling in apoptosis of human pancreatic tumoral cells mediated by exosomal nanoparticles. Int. J. Cancer, 2009, 125(5), 1016-1026.
[] [PMID: 19405120]
Ristorcelli, E.; Beraud, E.; Verrando, P.; Villard, C.; Lafitte, D.; Sbarra, V.; Lombardo, D.; Verine, A. Human tumor nanoparticles induce apoptosis of pancreatic cancer cells. FASEB J., 2008, 22(9), 3358-3369.
[] [PMID: 18511551]
Wolfers, J.; Lozier, A.; Raposo, G.; Regnault, A.; Théry, C.; Masurier, C.; Flament, C.; Pouzieux, S.; Faure, F.; Tursz, T.; Angevin, E.; Amigorena, S.; Zitvogel, L. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat. Med., 2001, 7(3), 297-303.
[] [PMID: 11231627]
Temchura, V.V.; Tenbusch, M.; Nchinda, G.; Nabi, G.; Tippler, B.; Zelenyuk, M.; Wildner, O.; Uberla, K.; Kuate, S. Enhancement of immunostimulatory properties of exosomal vaccines by incorporation of fusion-competent G protein of vesicular stomatitis virus. Vaccine, 2008, 26(29-30), 3662-3672.
[] [PMID: 18538453]
Zitvogel, L.; Regnault, A.; Lozier, A.; Wolfers, J.; Flament, C.; Tenza, D.; Ricciardi-Castagnoli, P.; Raposo, G.; Amigorena, S. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat. Med., 1998, 4(5), 594-600.
[] [PMID: 9585234]
Beauvillain, C.; Ruiz, S.; Guiton, R.; Bout, D.; Dimier-Poisson, I. A vaccine based on exosomes secreted by a dendritic cell line confers protection against T. gondii infection in syngeneic and allogeneic mice. Microbes Infect., 2007, 9(14-15), 1614-1622.
[] [PMID: 17905628]
Hegmans, J.P.; Hemmes, A.; Aerts, J.G.; Hoogsteden, H.C.; Lambrecht, B.N. Immunotherapy of murine malignant mesothelioma using tumor lysate-pulsed dendritic cells. Am. J. Respir. Crit. Care Med., 2005, 171(10), 1168-1177.
[] [PMID: 15764728]
Viaud, S.; Terme, M.; Flament, C.; Taieb, J.; André, F.; Novault, S.; Escudier, B.; Robert, C.; Caillat-Zucman, S.; Tursz, T.; Zitvogel, L.; Chaput, N. Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: a role for NKG2D ligands and IL-15Ralpha. PLoS One, 2009, 4(3)e4942
[] [PMID: 19319200]
Dai, S.; Wei, D.; Wu, Z.; Zhou, X.; Wei, X.; Huang, H.; Li, G. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol. Ther., 2008, 16(4), 782-790.
[] [PMID: 18362931]
Escudier, B.; Dorval, T.; Chaput, N.; André, F.; Caby, M-P.; Novault, S.; Flament, C.; Leboulaire, C.; Borg, C.; Amigorena, S.; Boccaccio, C.; Bonnerot, C.; Dhellin, O.; Movassagh, M.; Piperno, S.; Robert, C.; Serra, V.; Valente, N.; Le Pecq, J.B.; Spatz, A.; Lantz, O.; Tursz, T.; Angevin, E.; Zitvogel, L. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J. Transl. Med., 2005, 3(1), 10.
[] [PMID: 15740633]
Morse, M.A.; Garst, J.; Osada, T.; Khan, S.; Hobeika, A.; Clay, T.M.; Valente, N.; Shreeniwas, R.; Sutton, M.A.; Delcayre, A.; Hsu, D.H.; Le Pecq, J.B.; Lyerly, H.K. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J. Transl. Med., 2005, 3(1), 9.
[] [PMID: 15723705]
Tan, A.; De La Peña, H.; Seifalian, A.M. The application of exosomes as a nanoscale cancer vaccine. Int. J. Nanomedicine, 2010, 5, 889-900.
[] [PMID: 21116329]
Dyck, L.; Mills, K.H.G. Immune checkpoints and their inhibition in cancer and infectious diseases. Eur. J. Immunol., 2017, 47(5), 765-779.
[] [PMID: 28393361]
Xiu, F.; Cai, Z.; Yang, Y.; Wang, X.; Wang, J.; Cao, X. Surface anchorage of superantigen SEA promotes induction of specific antitumor immune response by tumor-derived exosomes. J. Mol. Med. (Berl.), 2007, 85(5), 511-521.
[] [PMID: 17219095]
Chen, W.; Wang, J.; Shao, C.; Liu, S.; Yu, Y.; Wang, Q.; Cao, X. Efficient induction of antitumor T cell immunity by exosomes derived from heat-shocked lymphoma cells. Eur. J. Immunol., 2006, 36(6), 1598-1607.
[] [PMID: 16708399]
Dai, S.; Wan, T.; Wang, B.; Zhou, X.; Xiu, F.; Chen, T.; Wu, Y.; Cao, X. More efficient induction of HLA-A*0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin. Cancer Res., 2005, 11(20), 7554-7563.
[] [PMID: 16243831]
Chaput, N.; Schartz, N.E.; André, F.; Taïeb, J.; Novault, S.; Bonnaventure, P.; Aubert, N.; Bernard, J.; Lemonnier, F.; Merad, M.; Adema, G.; Adams, M.; Ferrantini, M.; Carpentier, A.F.; Escudier, B.; Tursz, T.; Angevin, E.; Zitvogel, L. Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CpG adjuvants efficiently prime naive Tc1 lymphocytes leading to tumor rejection. J. Immunol., 2004, 172(4), 2137-2146.
[] [PMID: 14764679]
Hao, S.; Bai, O.; Yuan, J.; Qureshi, M.; Xiang, J. Dendritic cell-derived exosomes stimulate stronger CD8+ CTL responses and antitumor immunity than tumor cell-derived exosomes. Cell. Mol. Immunol., 2006, 3(3), 205-211.
[PMID: 16893501]
Hao, S.; Bai, O.; Li, F.; Yuan, J.; Laferte, S.; Xiang, J. Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T-lymphocyte responses and antitumour immunity. Immunology, 2007, 120(1), 90-102.
[] [PMID: 17073943]
Hao, S.; Ye, Z.; Yang, J.; Bai, O.; Xiang, J. Intradermal vaccination of dendritic cell-derived exosomes is superior to a subcutaneous one in the induction of antitumor immunity. Cancer Biother. Radiopharm., 2006, 21(2), 146-154.
[] [PMID: 16706635]
Besse, B.; Charrier, M.; Lapierre, V.; Dansin, E.; Lantz, O.; Planchard, D.; Le Chevalier, T.; Livartoski, A.; Barlesi, F.; Laplanche, A.; Ploix, S.; Vimond, N.; Peguillet, I.; Théry, C.; Lacroix, L.; Zoernig, I.; Dhodapkar, K.; Dhodapkar, M.; Viaud, S.; Soria, J.C.; Reiners, K.S.; Pogge von Strandmann, E.; Vély, F.; Rusakiewicz, S.; Eggermont, A.; Pitt, J.M.; Zitvogel, L.; Chaput, N. Dendritic cell-derived exosomes as maintenance immunotherapy after first line chemotherapy in NSCLC. OncoImmunology, 2015, 5(4)e1071008
[] [PMID: 27141373]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy