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Current Cancer Drug Targets

Editor-in-Chief

ISSN (Print): 1568-0096
ISSN (Online): 1873-5576

Review Article

Recent Progress in the Application of Exosome Analysis in Ovarian Cancer Management

Author(s): Vahideh Keyvani, Zari Naderi Ghale-Noie, Samaneh Mollazadeh, Reihaneh Alsadat Mahmoudian, Elnaz Ghorbani, Hamid Naderi, Majid Khazaei, Seyed Mahdi Hassanian, Gordon A. Ferns, Amir Avan* and Kazem Anvari*

Volume 24, Issue 9, 2024

Published on: 25 January, 2024

Page: [920 - 929] Pages: 10

DOI: 10.2174/0115680096281906231213055422

Price: $65

Open Access Journals Promotions 2
Abstract

Exosomes are very small (nano-sized) vesicles participating in tumor development by involvement in intercellular communication mediated by transferring biocomponents. Exosomes appear to play vital roles in various cancer development, such as ovarian cancer, a common malignancy in women. Several hallmarks of ovarian cancer are reported to be affected by the exosomemediated cellular cross-talk, including modulating peritoneal dissemination and chemoresistance. Since the expression of some biomolecules, such as miRNAs and mRNA, is changed in ovarian cancer, these exo-biomolecules can be applied as prognostic, diagnostic, and therapeutic biomarkers. Also, the selective loading of specific chemotherapeutic agents into exosomes highlights these biocarries as potential delivery devices. Exosomes could be artificially provided and engineered to better target the site of interest in ovarian cancer. In the present review, we summarize the notable achievement of exosome application in ovarian cancer management to gain applicable transitional insight against this cancer.

Keywords: Ovarian cancer, exosomes, bioactive molecules, biomarkers, delivery vehicles, extracellular vesicles.

Graphical Abstract
[1]
Feng, W.; Dean, D.C.; Hornicek, F.J.; Shi, H.; Duan, Z. Exosomes promote pre-metastatic niche formation in ovarian cancer. Mol. Cancer, 2019, 18(1), 124.
[http://dx.doi.org/10.1186/s12943-019-1049-4] [PMID: 31409361]
[2]
Cabasag, C.J.; Fagan, P.J.; Ferlay, J.; Vignat, J.; Laversanne, M.; Liu, L.; van der Aa, M.A.; Bray, F.; Soerjomataram, I. Ovarian cancer today and tomorrow: A global assessment by world region and human development index using GLOBOCAN 2020. Int. J. Cancer, 2022, 151(9), 1535-1541.
[http://dx.doi.org/10.1002/ijc.34002] [PMID: 35322413]
[3]
Xu, Z.; Zeng, S.; Gong, Z.; Yan, Y. Inmunoterapia basada en exosomas: un enfoque prometedor para el tratamiento del cáncer. Mol. Cancer, 2020, 19(1)
[4]
Soleimani, M.; Homayoun, M.; Sajedi, N. In vitro evaluation of the pogostone effects on the expression of PTEN and DACT1 tumor suppressor genes, cell cycle, and apoptosis in ovarian cancer cell line. Res. Pharm. Sci., 2022, 17(2), 164-175.
[http://dx.doi.org/10.4103/1735-5362.335175] [PMID: 35280836]
[5]
Lo Presti, E.; Pizzolato, G.; Corsale, A.M.; Caccamo, N.; Sireci, G.; Dieli, F.; Meraviglia, S. γδ T cells and tumor microenvironment: From immunosurveillance to tumor evasion. Front. Immunol., 2018, 9, 1395.
[http://dx.doi.org/10.3389/fimmu.2018.01395] [PMID: 29963061]
[6]
Becker, A.; Thakur, B.K.; Weiss, J.M.; Kim, H.S.; Peinado, H.; Lyden, D. Extracellular vesicles in cancer: Cell-to-cell mediators of metastasis. Cancer Cell, 2016, 30(6), 836-848.
[http://dx.doi.org/10.1016/j.ccell.2016.10.009] [PMID: 27960084]
[7]
Kowal, J.; Tkach, M.; Théry, C. Biogenesis and secretion of exosomes. Curr. Opin. Cell Biol., 2014, 29, 116-125.
[http://dx.doi.org/10.1016/j.ceb.2014.05.004] [PMID: 24959705]
[8]
Mousavi, S.; Moallem, R.; Hassanian, S.M.; Sadeghzade, M.; Mardani, R.; Ferns, G.A.; Khazaei, M.; Avan, A. Tumor-derived exosomes: Potential biomarkers and therapeutic target in the treatment of colorectal cancer. J. Cell. Physiol., 2019, 234(8), 12422-12432.
[http://dx.doi.org/10.1002/jcp.28080] [PMID: 30637729]
[9]
Cheng, L.; Wu, S.; Zhang, K.; Qing, Y.; Xu, T. A comprehensive overview of exosomes in ovarian cancer: Emerging biomarkers and therapeutic strategies. J. Ovarian Res., 2017, 10(1), 73.
[http://dx.doi.org/10.1186/s13048-017-0368-6] [PMID: 29100532]
[10]
Gopikrishnan, M.; R, H.C.; R, G.; Ashour, H.M.; Pintus, G.; Hammad, M.; Kashyap, M.K.; C, G.P.D.; Zayed, H. Therapeutic and diagnostic applications of exosomal circRNAs in breast cancer. Funct. Integr. Genomics, 2023, 23(2), 184.
[http://dx.doi.org/10.1007/s10142-023-01083-3] [PMID: 37243750]
[11]
Sharma, J.; Balakrishnan, L.; Kaushik, S.; Kashyap, M.K. multi- omics approaches to study signaling pathways In: Frontiers Media SA; , 2020; p. 829.
[12]
Hashemi, Z.S.; Ghavami, M.; Kashyap, M.K. Editorial: Exosomes, miRNAs, and lncRNAs in breast cancer: Therapeutic and diagnostic applications. Front. Genet., 2023, 14, 1192866.
[http://dx.doi.org/10.3389/fgene.2023.1192866] [PMID: 37229186]
[13]
Conigliaro, A.; Cicchini, C. Exosome-mediated signaling in epithelial to mesenchymal transition and tumor progression. J. Clin. Med., 2018, 8(1), 26.
[http://dx.doi.org/10.3390/jcm8010026] [PMID: 30591649]
[14]
Li, K.; Chen, Y.; Li, A.; Tan, C.; Liu, X. Exosomes play roles in sequential processes of tumor metastasis. Int. J. Cancer, 2019, 144(7), 1486-1495.
[http://dx.doi.org/10.1002/ijc.31774] [PMID: 30155891]
[15]
Nakamura, K.; Sawada, K.; Kinose, Y.; Yoshimura, A.; Toda, A.; Nakatsuka, E.; Hashimoto, K.; Mabuchi, S.; Morishige, K.; Kurachi, H.; Lengyel, E.; Kimura, T. Exosomes promote ovarian cancer cell invasion through transfer of CD44 to peritoneal mesothelial cells. Mol. Cancer Res., 2017, 15(1), 78-92.
[http://dx.doi.org/10.1158/1541-7786.MCR-16-0191] [PMID: 27758876]
[16]
Yoshimura, A.; Sawada, K.; Nakamura, K.; Kinose, Y.; Nakatsuka, E.; Kobayashi, M.; Miyamoto, M.; Ishida, K.; Matsumoto, Y.; Kodama, M.; Hashimoto, K.; Mabuchi, S.; Kimura, T. Exosomal miR-99a-5p is elevated in sera of ovarian cancer patients and promotes cancer cell invasion by increasing fibronectin and vitronectin expression in neighboring peritoneal mesothelial cells. BMC Cancer, 2018, 18(1), 1065.
[http://dx.doi.org/10.1186/s12885-018-4974-5] [PMID: 30396333]
[17]
Théry, C.; Zitvogel, L.; Amigorena, S. Exosomes: Composition, biogenesis and function. Nat. Rev. Immunol., 2002, 2(8), 569-579.
[http://dx.doi.org/10.1038/nri855] [PMID: 12154376]
[18]
Ibrahim, A.; Marbán, E. Exosomes: Fundamental biology and roles in cardiovascular physiology. Annu. Rev. Physiol., 2016, 78(1), 67-83.
[http://dx.doi.org/10.1146/annurev-physiol-021115-104929] [PMID: 26667071]
[19]
Maia, J.; Caja, S.; Strano Moraes, M.C.; Couto, N.; Costa-Silva, B. Exosome-based cell-cell communication in the tumor microenvironment. Front. Cell Dev. Biol., 2018, 6(6), 18.
[http://dx.doi.org/10.3389/fcell.2018.00018] [PMID: 29515996]
[20]
Li, N.; Zhao, L.; Wei, Y.; Ea, V.L.; Nian, H.; Wei, R. Recent advances of exosomes in immune-mediated eye diseases. Stem Cell Res. Ther., 2019, 10(1), 278.
[http://dx.doi.org/10.1186/s13287-019-1372-0] [PMID: 31470892]
[21]
Kenny, H.A.; Chiang, C.Y.; White, E.A.; Schryver, E.M.; Habis, M.; Romero, I.L.; Ladanyi, A.; Penicka, C.V.; George, J.; Matlin, K.; Montag, A.; Wroblewski, K.; Yamada, S.D.; Mazar, A.P.; Bowtell, D.; Lengyel, E. Mesothelial cells promote early ovarian cancer metastasis through fibronectin secretion. J. Clin. Invest., 2014, 124(10), 4614-4628.
[http://dx.doi.org/10.1172/JCI74778] [PMID: 25202979]
[22]
Mutsaers, S.E. The mesothelial cell. Int. J. Biochem. Cell Biol., 2004, 36(1), 9-16.
[http://dx.doi.org/10.1016/S1357-2725(03)00242-5] [PMID: 14592528]
[23]
Peinado, H.; Alečković, M.; Lavotshkin, S.; Matei, I.; Costa-Silva, B.; Moreno-Bueno, G.; Hergueta-Redondo, M.; Williams, C.; García-Santos, G.; Ghajar, C.M.; 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.
[http://dx.doi.org/10.1038/nm.2753] [PMID: 22635005]
[24]
Yokoi, A.; Yoshioka, Y.; Yamamoto, Y.; Ishikawa, M.; Ikeda, S.; Kato, T.; Kiyono, T.; Takeshita, F.; Kajiyama, H.; Kikkawa, F.; Ochiya, T. Malignant extracellular vesicles carrying MMP1 mRNA facilitate peritoneal dissemination in ovarian cancer. Nat. Commun., 2017, 8(1), 14470.
[http://dx.doi.org/10.1038/ncomms14470] [PMID: 28262727]
[25]
Yi, H.; Ye, J.; Yang, X-M.; Zhang, L-W.; Zhang, Z-G.; Chen, Y-P. High-grade ovarian cancer secreting effective exosomes in tumor angiogenesis. Int. J. Clin. Exp. Pathol., 2015, 8(5), 5062-5070.
[PMID: 26191200]
[26]
Qiu, J.J.; Lin, X.J.; Tang, X.Y.; Zheng, T.T.; Lin, Y.Y.; Hua, K.Q. Exosomal metastasis-associated lung adenocarcinoma transcript 1 promotes angiogenesis and predicts poor prognosis in epithelial ovarian cancer. Int. J. Biol. Sci., 2018, 14(14), 1960-1973.
[http://dx.doi.org/10.7150/ijbs.28048] [PMID: 30585260]
[27]
Czystowska-Kuzmicz, M.; Sosnowska, A.; Nowis, D.; Ramji, K.; Szajnik, M.; Chlebowska-Tuz, J.; Wolinska, E.; Gaj, P.; Grazul, M.; Pilch, Z.; Zerrouqi, A.; Graczyk-Jarzynka, A.; Soroczynska, K.; Cierniak, S.; Koktysz, R.; Elishaev, E.; Gruca, S.; Stefanowicz, A.; Blaszczyk, R.; Borek, B.; Gzik, A.; Whiteside, T.; Golab, J. Small extracellular vesicles containing arginase-1 suppress T-cell responses and promote tumor growth in ovarian carcinoma. Nat. Commun., 2019, 10(1), 3000.
[http://dx.doi.org/10.1038/s41467-019-10979-3] [PMID: 31278254]
[28]
Meng, Y.; Kang, S.; Fishman, D.A. Lysophosphatidic acid stimulates fas ligand microvesicle release from ovarian cancer cells. Cancer Immunol. Immunother., 2005, 54(8), 807-814.
[http://dx.doi.org/10.1007/s00262-004-0642-5] [PMID: 15662527]
[29]
Sawada, K.; Mitra, A.K.; Radjabi, A.R.; Bhaskar, V.; Kistner, E.O.; Tretiakova, M.; Jagadeeswaran, S.; Montag, A.; Becker, A.; Kenny, H.A.; Peter, M.E.; Ramakrishnan, V.; Yamada, S.D.; Lengyel, E. Loss of E-cadherin promotes ovarian cancer metastasis via α 5-integrin, which is a therapeutic target. Cancer Res., 2008, 68(7), 2329-2339.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-5167] [PMID: 18381440]
[30]
Vella, L.J. The emerging role of exosomes in epithelial-mesenchymal-transition in cancer. Front. Oncol., 2014, 4, 361.
[http://dx.doi.org/10.3389/fonc.2014.00361] [PMID: 25566500]
[31]
Li, W.; Zhang, X.; Wang, J.; Li, M.; Cao, C.; Tan, J.; Ma, D.; Gao, Q. TGFβ1 in fibroblasts-derived exosomes promotes epithelial-mesenchymal transition of ovarian cancer cells. Oncotarget, 2017, 8(56), 96035-96047.
[http://dx.doi.org/10.18632/oncotarget.21635] [PMID: 29221185]
[32]
Li, P.; Kaslan, M.; Lee, S.H.; Yao, J.; Gao, Z. Progress in exosome isolation techniques. Theranostics, 2017, 7(3), 789-804.
[http://dx.doi.org/10.7150/thno.18133] [PMID: 28255367]
[33]
Zhu, L.; Sun, H.T.; Wang, S.; Huang, S.L.; Zheng, Y.; Wang, C.Q.; Hu, B.Y.; Qin, W.; Zou, T.T.; Fu, Y.; Shen, X.T.; Zhu, W.W.; Geng, Y.; Lu, L.; Jia, H.; Qin, L.X.; Dong, Q.Z. Isolation and characterization of exosomes for cancer research. J. Hematol. Oncol., 2020, 13(1), 152.
[http://dx.doi.org/10.1186/s13045-020-00987-y] [PMID: 33168028]
[34]
Iwai, K.; Minamisawa, T.; Suga, K.; Yajima, Y.; Shiba, K. Isolation of human salivary extracellular vesicles by iodixanol density gradient ultracentrifugation and their characterizations. J. Extracell. Vesicles, 2016, 5(1), 30829.
[http://dx.doi.org/10.3402/jev.v5.30829] [PMID: 27193612]
[35]
Helwa, I.; Cai, J.; Drewry, M.D.; Zimmerman, A.; Dinkins, M.B.; Khaled, M.L.; Seremwe, M.; Dismuke, W.M.; Bieberich, E.; Stamer, W.D.; Hamrick, M.W.; Liu, Y. A comparative study of serum exosome isolation using differential ultracentrifugation and three commercial reagents. PLoS One, 2017, 12(1), e0170628.
[http://dx.doi.org/10.1371/journal.pone.0170628] [PMID: 28114422]
[36]
Liang, B.; Peng, P.; Chen, S.; Li, L.; Zhang, M.; Cao, D.; Yang, J.; Li, H.; Gui, T.; Li, X.; Shen, K. Characterization and proteomic analysis of ovarian cancer-derived exosomes. J. Proteomics, 2013, 80, 171-182.
[http://dx.doi.org/10.1016/j.jprot.2012.12.029] [PMID: 23333927]
[37]
Dorayappan, K.D.P.; Gardner, M.L.; Hisey, C.L.; Zingarelli, R.A.; Smith, B.Q.; Lightfoot, M.D.S.; Gogna, R.; Flannery, M.M.; Hays, J.; Hansford, D.J.; Freitas, M.A.; Yu, L.; Cohn, D.E.; Selvendiran, K. A microfluidic chip enables isolation of exosomes and establishment of their protein profiles and associated signaling pathways in ovarian cancer. Cancer Res., 2019, 79(13), 3503-3513.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-3538] [PMID: 31097475]
[38]
Zhao, Z.; Yang, Y.; Zeng, Y.; He, M. A microfluidic exosearch chip for multiplexed exosome detection towards blood-based ovarian cancer diagnosis. Lab Chip, 2016, 16(3), 489-496.
[http://dx.doi.org/10.1039/C5LC01117E] [PMID: 26645590]
[39]
Ye, D.; Gong, M.; Deng, Y.; Fang, S.; Cao, Y.; Xiang, Y.; Shen, Z. Roles and clinical application of exosomal circRNAs in the diagnosis and treatment of malignant tumors. J. Transl. Med., 2022, 20(1), 161.
[http://dx.doi.org/10.1186/s12967-022-03367-x] [PMID: 35382838]
[40]
Hu, C.; Jiang, W.; Lv, M.; Fan, S.; Lu, Y.; Wu, Q.; Pi, J. Potentiality of exosomal proteins as novel cancer biomarkers for liquid biopsy. Front. Immunol., 2022, 13, 792046.
[http://dx.doi.org/10.3389/fimmu.2022.792046] [PMID: 35757760]
[41]
Yang, S.; Wang, J.; Wang, S.; Zhou, A.; Zhao, G.; Li, P. Roles of small extracellular vesicles in the development, diagnosis and possible treatment strategies for hepatocellular carcinoma (Review). Int. J. Oncol., 2022, 61(2), 91.
[http://dx.doi.org/10.3892/ijo.2022.5381] [PMID: 35674180]
[42]
Zhang, M.; He, Y.; Sun, X.; Li, Q.; Wang, W.; Zhao, A.; Di, W. A high M1/M2 ratio of tumor-associated macrophages is associated with extended survival in ovarian cancer patients. J. Ovarian Res., 2014, 7(1), 19.
[http://dx.doi.org/10.1186/1757-2215-7-19] [PMID: 24507759]
[43]
Li, W.; Li, C.; Zhou, T.; Liu, X.; Liu, X.; Li, X.; Chen, D. Role of exosomal proteins in cancer diagnosis. Mol. Cancer, 2017, 16(1), 145.
[http://dx.doi.org/10.1186/s12943-017-0706-8] [PMID: 28851367]
[44]
Zhang, B.; Chen, F.; Xu, Q.; Han, L.; Xu, J.; Gao, L.; Sun, X.; Li, Y.; Li, Y.; Qian, M.; Sun, Y. Revisiting ovarian cancer microenvironment: A friend or a foe? Protein Cell, 2018, 9(8), 674-692.
[http://dx.doi.org/10.1007/s13238-017-0466-7] [PMID: 28929459]
[45]
Wang, X.; Yao, Y.; Jin, M. Circ-0001068 is a novel biomarker for ovarian cancer and inducer of PD1 expression in T cells. Aging (Albany NY), 2020, 12(19), 19095-19106.
[http://dx.doi.org/10.18632/aging.103706] [PMID: 33028742]
[46]
Wu, Y.; Yuan, W.; Ding, H.; Wu, X. Serum exosomal miRNA from endometriosis patients correlates with disease severity. Arch. Gynecol. Obstet., 2022, 305(1), 117-127.
[http://dx.doi.org/10.1007/s00404-021-06227-z] [PMID: 34542679]
[47]
Lin, J; Li, J; Huang, B; Liu, J; Chen, X; Chen, X-M Exosomes: novel biomarkers for clinical diagnosis. The scientific world journal. , 2015, 657086.
[http://dx.doi.org/10.1155/2015/657086]
[48]
Runz, S.; Keller, S.; Rupp, C.; Stoeck, A.; Issa, Y.; Koensgen, D.; Mustea, A.; Sehouli, J.; Kristiansen, G.; Altevogt, P. Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol. Oncol., 2007, 107(3), 563-571.
[http://dx.doi.org/10.1016/j.ygyno.2007.08.064] [PMID: 17900673]
[49]
Jiang, H.; Zhao, H.; Zhang, M.; He, Y.; Li, X.; Xu, Y.; Liu, X. Hypoxia induced changes of exosome cargo and subsequent biological effects. Front. Immunol., 2022, 13, 824188.
[http://dx.doi.org/10.3389/fimmu.2022.824188] [PMID: 35444652]
[50]
Kim, Y.S.; Ahn, J.S.; Kim, S.; Kim, H.J.; Kim, S.H.; Kang, J.S. The potential theragnostic (diagnostic+therapeutic) application of exosomes in diverse biomedical fields. Korean J. Physiol. Pharmacol., 2018, 22(2), 113-125.
[http://dx.doi.org/10.4196/kjpp.2018.22.2.113] [PMID: 29520164]
[51]
Grass, G.D.; Toole, B.P. How, with whom and when: an overview of CD147-mediated regulatory networks influencing matrix metalloproteinase activity. Biosci. Rep., 2016, 36(1), e00283.
[http://dx.doi.org/10.1042/BSR20150256] [PMID: 26604323]
[52]
Shimizu, A.; Sawada, K.; Kimura, T. Pathophysiological role and potential therapeutic exploitation of exosomes in ovarian cancer. Cells, 2020, 9(4), 814.
[http://dx.doi.org/10.3390/cells9040814] [PMID: 32230983]
[53]
Nakamura, K.; Sawada, K.; Kobayashi, M.; Miyamoto, M.; Shimizu, A.; Yamamoto, M.; Kinose, Y.; Kimura, T. Role of the exosome in ovarian cancer progression and its potential as a therapeutic target. Cancers (Basel), 2019, 11(8), 1147.
[http://dx.doi.org/10.3390/cancers11081147] [PMID: 31405096]
[54]
Tang, M.K.S.; Wong, A.S.T. Exosomes: Emerging biomarkers and targets for ovarian cancer. Cancer Lett., 2015, 367(1), 26-33.
[http://dx.doi.org/10.1016/j.canlet.2015.07.014] [PMID: 26189430]
[55]
Datta, A.; Kim, H.; McGee, L.; Johnson, A.E.; Talwar, S.; Marugan, J.; Southall, N.; Hu, X.; Lal, M.; Mondal, D.; Ferrer, M.; Abdel-Mageed, A.B. High-throughput screening identified selective inhibitors of exosome biogenesis and secretion: A drug repurposing strategy for advanced cancer. Sci. Rep., 2018, 8(1), 8161.
[http://dx.doi.org/10.1038/s41598-018-26411-7] [PMID: 29802284]
[56]
Doyle, L.; Wang, M. Overview of extracellular vesicles, their origin, composition, purpose, and methods for exosome isolation and analysis. Cells, 2019, 8(7), 727.
[http://dx.doi.org/10.3390/cells8070727] [PMID: 31311206]
[57]
Zhang, Y.; Li, J.; Gao, W.; Xie, N. Exosomes as anticancer drug delivery vehicles: prospects and challenges. Frontiers in Bioscience-Landmark, 2022, 27(10), 293.
[http://dx.doi.org/10.31083/j.fbl2710293] [PMID: 36336863]
[58]
Raguraman, R.; Bhavsar, D.; Kim, D.; Ren, X.; Sikavitsas, V.; Munshi, A.; Ramesh, R. Tumor-targeted exosomes for delivery of anticancer drugs. Cancer Lett., 2023, 558, 216093.
[http://dx.doi.org/10.1016/j.canlet.2023.216093] [PMID: 36822543]
[59]
Herrmann, I.K.; Wood, M.J.A.; Fuhrmann, G. Extracellular vesicles as a next-generation drug delivery platform. Nat. Nanotechnol., 2021, 16(7), 748-759.
[http://dx.doi.org/10.1038/s41565-021-00931-2] [PMID: 34211166]
[60]
Melzer, C.; Rehn, V.; Yang, Y.; Bähre, H.; von der Ohe, J.; Hass, R. Taxol-loaded MSC-derived exosomes provide a therapeutic vehicle to target metastatic breast cancer and other carcinoma cells. Cancers (Basel), 2019, 11(6), 798.
[http://dx.doi.org/10.3390/cancers11060798] [PMID: 31181850]
[61]
Brown, A.; Kumar, S.; Tchounwou, P.B. Cisplatin-based chemotherapy of human cancers. J. Cancer Sci. Ther., 2019, 11(4), 97.
[PMID: 32148661]
[62]
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(1), 88.
[http://dx.doi.org/10.1186/1478-811X-11-88] [PMID: 24245560]
[63]
Liang, X.; Ye, X.; Wang, C.; Xing, C.; Miao, Q.; Xie, Z.; Chen, X.; Zhang, X.; Zhang, H.; Mei, L. Photothermal cancer immunotherapy by erythrocyte membrane-coated black phosphorus formulation. J. Control. Release, 2019, 296, 150-161.
[http://dx.doi.org/10.1016/j.jconrel.2019.01.027] [PMID: 30682441]
[64]
Zheng, Z.; Li, Z.; Xu, C.; Guo, B.; Guo, P. Folate-displaying exosome mediated cytosolic delivery of siRNA avoiding endosome trapping. J. Control. Release, 2019, 311-312, 43-49.
[http://dx.doi.org/10.1016/j.jconrel.2019.08.021] [PMID: 31446085]
[65]
Zeh, N.; Schneider, H.; Mathias, S.; Raab, N.; Kleemann, M.; Schmidt-Hertel, S.; Weis, B.; Wissing, S.; Strempel, N.; Handrick, R.; Otte, K. Human CAP cells represent a novel source for functional, miRNA-loaded exosome production. PLoS One, 2019, 14(8), e0221679.
[http://dx.doi.org/10.1371/journal.pone.0221679] [PMID: 31461486]
[66]
Hu, Y.; Li, D.; Wu, A.; Qiu, X.; Di, W.; Huang, L.; Qiu, L. TWEAK-stimulated macrophages inhibit metastasis of epithelial ovarian cancer via exosomal shuttling of microRNA. Cancer Lett., 2017, 393, 60-67.
[http://dx.doi.org/10.1016/j.canlet.2017.02.009] [PMID: 28216373]
[67]
Wei, L.; He, Y.; Bi, S.; Li, X.; Zhang, J.; Zhang, S. miRNA-199b-3p suppresses growth and progression of ovarian cancer via the CHK1/E-cadherin/EMT signaling pathway by targeting ZEB1. Oncol. Rep., 2020, 45(2), 569-581.
[http://dx.doi.org/10.3892/or.2020.7895] [PMID: 33416170]
[68]
Hussain, M.W.A.; Jahangir, S.; Ghosh, B.; Yesmin, F.; Anis, A.; Satil, S.N.; Anwar, F.; Rashid, M.H. Exosomes for regulation of immune responses and immunotherapy. Journal of Nanotheranostics, 2022, 3(1), 55-85.
[http://dx.doi.org/10.3390/jnt3010005]
[69]
Bhatnagar, S.; Schorey, J.S. Exosomes released from infected macrophages contain Mycobacterium avium glycopeptidolipids and are proinflammatory. J. Biol. Chem., 2007, 282(35), 25779-25789.
[http://dx.doi.org/10.1074/jbc.M702277200] [PMID: 17591775]
[70]
Vega, V.L.; Rodríguez-Silva, M.; Frey, T.; Gehrmann, M.; Diaz, J.C.; Steinem, C.; Multhoff, G.; Arispe, N.; De Maio, A. Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J. Immunol., 2008, 180(6), 4299-4307.
[http://dx.doi.org/10.4049/jimmunol.180.6.4299] [PMID: 18322243]
[71]
Gastpar, R.; Gehrmann, M.; Bausero, M.A.; Asea, A.; Gross, C.; Schroeder, J.A.; Multhoff, G. Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res., 2005, 65(12), 5238-5247.
[http://dx.doi.org/10.1158/0008-5472.CAN-04-3804] [PMID: 15958569]
[72]
Skokos, D.; Botros, H.G.; Demeure, C.; Morin, J.; Peronet, R.; Birkenmeier, G.; Boudaly, S.; Mécheri, S. Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J. Immunol., 2003, 170(6), 3037-3045.
[http://dx.doi.org/10.4049/jimmunol.170.6.3037] [PMID: 12626558]
[73]
Segura, E.; Amigorena, S.; Théry, C. Mature dendritic cells secrete exosomes with strong ability to induce antigen-specific effector immune responses. Blood Cells Mol. Dis., 2005, 35(2), 89-93.
[http://dx.doi.org/10.1016/j.bcmd.2005.05.003] [PMID: 15990342]
[74]
Abusamra, A.J.; Zhong, Z.; Zheng, X.; Li, M.; Ichim, T.E.; Chin, J.L.; Min, W.P. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol. Dis., 2005, 35(2), 169-173.
[http://dx.doi.org/10.1016/j.bcmd.2005.07.001] [PMID: 16081306]
[75]
Theodoraki, M.N.; Yerneni, S.S.; Hoffmann, T.K.; Gooding, W.E.; Whiteside, T.L. Clinical significance of PD-L1+ exosomes in plasma of head and neck cancer patients. Clin. Cancer Res., 2018, 24(4), 896-905.
[http://dx.doi.org/10.1158/1078-0432.CCR-17-2664] [PMID: 29233903]
[76]
Chen, G.; Huang, A.C.; Zhang, W.; Zhang, G.; Wu, M.; Xu, W.; Yu, Z.; Yang, J.; Wang, B.; Sun, H.; Xia, H.; Man, Q.; Zhong, W.; Antelo, L.F.; Wu, B.; Xiong, X.; Liu, X.; Guan, L.; Li, T.; Liu, S.; Yang, R.; Lu, Y.; Dong, L.; McGettigan, S.; Somasundaram, R.; Radhakrishnan, R.; Mills, G.; Lu, Y.; Kim, J.; Chen, Y.H.; Dong, H.; Zhao, Y.; Karakousis, G.C.; Mitchell, T.C.; Schuchter, L.M.; Herlyn, M.; Wherry, E.J.; Xu, X.; Guo, W. Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature, 2018, 560(7718), 382-386.
[http://dx.doi.org/10.1038/s41586-018-0392-8] [PMID: 30089911]
[77]
Chen, J.; Song, Y.; Miao, F.; Chen, G.; Zhu, Y.; Wu, N.; Pang, L.; Chen, Z.; Chen, X. PDL1-positive exosomes suppress antitumor immunity by inducing tumor-specific CD8 + T cell exhaustion during metastasis. Cancer Sci., 2021, 112(9), 3437-3454.
[http://dx.doi.org/10.1111/cas.15033] [PMID: 34152672]
[78]
Taylor, D.D.; Gerçel-Taylor, C.; Lyons, K.S.; Stanson, J.; Whiteside, T.L. T-cell apoptosis and suppression of T-cell receptor/CD3-ζ by Fas ligand-containing membrane vesicles shed from ovarian tumors. Clin. Cancer Res., 2003, 9(14), 5113-5119.
[PMID: 14613988]
[79]
Klinker, M.W.; Lizzio, V.; Reed, T.J.; Fox, D.A.; Lundy, S.K. Human B cell-derived lymphoblastoid cell lines constitutively produce Fas ligand and secrete MHCII+ FasL+ killer exosomes. Front. Immunol., 2014, 5, 144.
[http://dx.doi.org/10.3389/fimmu.2014.00144] [PMID: 24765093]
[80]
Clayton, A.; Mitchell, J.P.; Court, J.; Linnane, S.; Mason, M.D.; Tabi, Z. Human tumor-derived exosomes down-modulate NKG2D expression. J. Immunol., 2008, 180(11), 7249-7258.
[http://dx.doi.org/10.4049/jimmunol.180.11.7249] [PMID: 18490724]
[81]
Vulpis, E.; Cecere, F.; Molfetta, R.; Soriani, A.; Fionda, C.; Peruzzi, G.; Caracciolo, G.; Palchetti, S.; Masuelli, L.; Simonelli, L.; D’Oro, U.; Abruzzese, M.P.; Petrucci, M.T.; Ricciardi, M.R.; Paolini, R.; Cippitelli, M.; Santoni, A.; Zingoni, A. Genotoxic stress modulates the release of exosomes from multiple myeloma cells capable of activating NK cell cytokine production: Role of HSP70/TLR2/NF-kB axis. OncoImmunology, 2017, 6(3), e1279372.
[http://dx.doi.org/10.1080/2162402X.2017.1279372] [PMID: 28405503]
[82]
Bald, T.; Krummel, M.F.; Smyth, M.J.; Barry, K.C. The NK cell-cancer cycle: Advances and new challenges in NK cell–based immunotherapies. Nat. Immunol., 2020, 21(8), 835-847.
[http://dx.doi.org/10.1038/s41590-020-0728-z] [PMID: 32690952]
[83]
Elsner, L.; Muppala, V.; Gehrmann, M.; Lozano, J.; Malzahn, D.; Bickeböller, H.; Brunner, E.; Zientkowska, M.; Herrmann, T.; Walter, L.; Alves, F.; Multhoff, G.; Dressel, R. The heat shock protein HSP70 promotes mouse NK cell activity against tumors that express inducible NKG2D ligands. J. Immunol., 2007, 179(8), 5523-5533.
[http://dx.doi.org/10.4049/jimmunol.179.8.5523] [PMID: 17911639]
[84]
Liu, C.; Yu, S.; Zinn, K.; Wang, J.; Zhang, L.; Jia, Y.; Kappes, J.C.; Barnes, S.; Kimberly, R.P.; Grizzle, W.E.; Zhang, H.G. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J. Immunol., 2006, 176(3), 1375-1385.
[http://dx.doi.org/10.4049/jimmunol.176.3.1375] [PMID: 16424164]
[85]
Ashiru, O.; Boutet, P.; Fernández-Messina, L.; Agüera-González, S.; Skepper, J.N.; Valés-Gómez, M.; Reyburn, H.T. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res., 2010, 70(2), 481-489.
[http://dx.doi.org/10.1158/0008-5472.CAN-09-1688] [PMID: 20068167]
[86]
Pritchard, A.; Tousif, S.; Wang, Y.; Hough, K.; Khan, S.; Strenkowski, J.; Chacko, B.K.; Darley-Usmar, V.M.; Deshane, J.S. Lung tumor cell-derived exosomes promote M2 macrophage polarization. Cells, 2020, 9(5), 1303.
[http://dx.doi.org/10.3390/cells9051303] [PMID: 32456301]
[87]
Jiang, H.; Zhou, L.; Shen, N.; Ning, X.; Wu, D.; Jiang, K.; Huang, X. M1 macrophage-derived exosomes and their key molecule lncRNA HOTTIP suppress head and neck squamous cell carcinoma progression by upregulating the TLR5/NF-κB pathway. Cell Death Dis., 2022, 13(2), 183.
[http://dx.doi.org/10.1038/s41419-022-04640-z] [PMID: 35210436]
[88]
Khare, D.; Or, R.; Resnick, I.; Barkatz, C.; Almogi-Hazan, O.; Avni, B. Mesenchymal stromal cell-derived exosomes affect mRNA expression and function of B-lymphocytes. Front. Immunol., 2018, 9, 3053.
[http://dx.doi.org/10.3389/fimmu.2018.03053] [PMID: 30622539]
[89]
Ye, L.; Zhang, Q.; Cheng, Y.; Chen, X.; Wang, G.; Shi, M.; Zhang, T.; Cao, Y.; Pan, H.; Zhang, L.; Wang, G.; Deng, Y.; Yang, Y.; Chen, G. Tumor-derived exosomal HMGB1 fosters hepatocellular carcinoma immune evasion by promoting TIM-1+ regulatory B cell expansion. J. Immunother. Cancer, 2018, 6(1), 145.
[http://dx.doi.org/10.1186/s40425-018-0451-6] [PMID: 30526680]
[90]
Yu, S.; Liu, C.; Su, K.; Wang, J.; Liu, Y.; Zhang, L.; Li, C.; Cong, Y.; Kimberly, R.; Grizzle, W.E.; Falkson, C.; Zhang, H.G. Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J. Immunol., 2007, 178(11), 6867-6875.
[http://dx.doi.org/10.4049/jimmunol.178.11.6867] [PMID: 17513735]
[91]
Hinata, M.; Kunita, A.; Abe, H.; Morishita, Y.; Sakuma, K.; Yamashita, H.; Seto, Y.; Ushiku, T.; Fukayama, M. Exosomes of Epstein-Barr virus-associated gastric carcinoma suppress dendritic cell maturation. Microorganisms, 2020, 8(11), 1776.
[http://dx.doi.org/10.3390/microorganisms8111776] [PMID: 33198173]
[92]
Ren, W.; Zhang, X.; Li, W.; Feng, Q.; Feng, H.; Tong, Y.; Rong, H.; Wang, W.; Zhang, D.; Zhang, Z.; Tu, S.; Zhu, X.; Zhang, Q. Exosomal miRNA-107 induces myeloid-derived suppressor cell expansion in gastric cancer. Cancer Manag. Res., 2019, 11, 4023-4040.
[http://dx.doi.org/10.2147/CMAR.S198886] [PMID: 31190980]
[93]
Guo, X.; Qiu, W.; Liu, Q.; Qian, M.; Wang, S.; Zhang, Z.; Gao, X.; Chen, Z.; Xue, H.; Li, G. Immunosuppressive effects of hypoxia-induced glioma exosomes through myeloid-derived suppressor cells via the miR-10a/Rora and miR-21/Pten Pathways. Oncogene, 2018, 37(31), 4239-4259.
[http://dx.doi.org/10.1038/s41388-018-0261-9] [PMID: 29713056]
[94]
Gong, X.; Chi, H.; Strohmer, D.F.; Teichmann, A.T.; Xia, Z.; Wang, Q. Exosomes: A potential tool for immunotherapy of ovarian cancer. Front. Immunol., 2023, 13, 1089410.
[http://dx.doi.org/10.3389/fimmu.2022.1089410] [PMID: 36741380]
[95]
Zhang, M.; Hu, S.; Liu, L.; Dang, P.; Liu, Y.; Sun, Z.; Qiao, B.; Wang, C. Engineered exosomes from different sources for cancer- targeted therapy. Signal Transduct. Target. Ther., 2023, 8(1), 124.
[http://dx.doi.org/10.1038/s41392-023-01382-y] [PMID: 36922504]
[96]
Peterson, M.F.; Otoc, N.; Sethi, J.K.; Gupta, A.; Antes, T.J. Integrated systems for exosome investigation. Methods, 2015, 87, 31-45.
[http://dx.doi.org/10.1016/j.ymeth.2015.04.015] [PMID: 25916618]
[97]
Davies, R.T.; Kim, J.; Jang, S.C.; Choi, E.J.; Gho, Y.S.; Park, J. Microfluidic filtration system to isolate extracellular vesicles from blood. Lab Chip, 2012, 12(24), 5202-5210.
[http://dx.doi.org/10.1039/c2lc41006k] [PMID: 23111789]
[98]
Huang, X.; Wu, W.; Jing, D.; Yang, L.; Guo, H.; Wang, L.; Zhang, W.; Pu, F.; Shao, Z. Engineered exosome as targeted lncRNA MEG3 delivery vehicles for osteosarcoma therapy. J. Control. Release, 2022, 343, 107-117.
[http://dx.doi.org/10.1016/j.jconrel.2022.01.026] [PMID: 35077741]
[99]
Wang, J.; Wang, C.; Li, Y.; Li, M.; Zhu, T.; Shen, Z.; Wang, H.; Lv, W.; Wang, X.; Cheng, X.; Xie, X. Potential of peptide-engineered exosomes with overexpressed miR-92b-3p in anti-angiogenic therapy of ovarian cancer. Clin. Transl. Med., 2021, 11(5), e425.
[http://dx.doi.org/10.1002/ctm2.425] [PMID: 34047469]
[100]
Wan, Y.; Wang, L.; Zhu, C.; Zheng, Q.; Wang, G.; Tong, J.; Fang, Y.; Xia, Y.; Cheng, G.; He, X.; Zheng, S.Y. Aptamer-conjugated extracellular nanovesicles for targeted drug delivery. Cancer Res., 2018, 78(3), 798-808.
[http://dx.doi.org/10.1158/0008-5472.CAN-17-2880] [PMID: 29217761]
[101]
Yi, K.; Rong, Y.; Huang, L.; Tang, X.; Zhang, Q.; Wang, W.; Wu, J.; Wang, F. Aptamer–exosomes for tumor theranostics. ACS Sens., 2021, 6(4), 1418-1429.
[http://dx.doi.org/10.1021/acssensors.0c02237] [PMID: 33755415]
[102]
Zhang, J.; Ji, C.; Zhang, H.; Shi, H.; Mao, F.; Qian, H.; Xu, W.; Wang, D.; Pan, J.; Fang, X.; Santos, H.A.; Zhang, X. Engineered neutrophil-derived exosome-like vesicles for targeted cancer therapy. Sci. Adv., 2022, 8(2), eabj8207.
[http://dx.doi.org/10.1126/sciadv.abj8207] [PMID: 35020437]
[103]
Cheng, L.; Zhang, X.; Tang, J.; Lv, Q.; Liu, J. Gene-engineered exosomes-thermosensitive liposomes hybrid nanovesicles by the blockade of CD47 signal for combined photothermal therapy and cancer immunotherapy. Biomaterials, 2021, 275, 120964.
[http://dx.doi.org/10.1016/j.biomaterials.2021.120964] [PMID: 34147721]
[104]
Guo, Y.; Wan, Z.; Zhao, P.; Wei, M.; Liu, Y.; Bu, T.; Sun, W.; Li, Z.; Yuan, L. Ultrasound triggered topical delivery of Bmp7 mRNA for white fat browning induction via engineered smart exosomes. J. Nanobiotechnology, 2021, 19(1), 402.
[http://dx.doi.org/10.1186/s12951-021-01145-3] [PMID: 34863187]
[105]
Feng, L.; Dong, Z.; Tao, D.; Zhang, Y.; Liu, Z. The acidic tumor microenvironment: A target for smart cancer nano-theranostics. Natl. Sci. Rev., 2018, 5(2), 269-286.
[http://dx.doi.org/10.1093/nsr/nwx062]

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