Generic placeholder image

Current Drug Metabolism

Editor-in-Chief

ISSN (Print): 1389-2002
ISSN (Online): 1875-5453

Mini-Review Article

The Emerging Roles of Extracellular Vesicles in Ovarian Cancer

Author(s): Yin-Xue Wang, Yi-Xiang Wang, Yi-Ke Li, Shi-Yan Tu and Yi-Qing Wang*

Volume 22, Issue 2, 2021

Published on: 10 November, 2020

Page: [139 - 149] Pages: 11

DOI: 10.2174/1389200221666201110155721

Price: $65

Abstract

Ovarian cancer (OC) is one of the deadliest gynecological malignancy. Epithelial ovarian cancer (EOC) is its most common form. OC has both, a poor prognosis and a high mortality rate due to the difficulties of early diagnosis, limitation of current treatment and resistance to chemotherapy. Extracellular vesicles (EVs) is a heterogeneous group of cell-derived submicron vesicles, which can be detected in body fluids, and it can be classified into three main types including exosomes, micro-vesicles, and apoptotic bodies.

Cancer cells can produce more EVs than healthy cells. Moreover, the contents of these EVs have been found distinctive from each other. It has been considered that EVs shedding from tumor cells may be implicated in clinical applications, such as a tool for tumor diagnosis, prognosis and potential treatment of certain cancers.

In this review, we provide a brief description of EVs. in diagnosis, prognosis, treatment, and drug-resistantance of OC. Cancer-related EVs show powerful influences on tumors by various biological mechanisms. However, the contents mentioned above remain in the laboratory stage and there is a lack of large-scale clinical trials, and the maturity of the purification and detection methods is a constraint. In addition, amplification of oncogenes on ecDNA is remarkably prevalent in cancer. It may be possible that ecDNA can be encapsulated in EVs and thus detected by us. In summary, much more research on EVs needs to be performed to reveal breakthroughs in OC and to accelerate the process of its application in clinic.

Keywords: EVs, Exosomes, microRNAs, Ovarian cancer, Diagnosis, Drug resistance, Prognosis, Therapy.

Graphical Abstract
[1]
Cancer Genome Atlas Research Network. Integrated genomic analyses of ovarian carcinoma. Nature, 2011, 474(7353), 609-615.
[http://dx.doi.org/10.1038/nature10166] [PMID: 21720365]
[2]
Patch, A-M.; Christie, E.L.; Etemadmoghadam, D.; Garsed, D.W.; George, J.; Fereday, S.; Nones, K.; Cowin, P.; Alsop, K.; Bailey, P.J.; Kassahn, K.S.; Newell, F.; Quinn, M.C.J.; Kazakoff, S.; Quek, K.; Wilhelm-Benartzi, C.; Curry, E.; Leong, H.S.; Hamilton, A.; Mileshkin, L.; Au-Yeung, G.; Kennedy, C.; Hung, J.; Chiew, Y-E.; Harnett, P.; Friedlander, M.; Quinn, M.; Pyman, J.; Cordner, S.; O’Brien, P.; Leditschke, J.; Young, G.; Strachan, K.; Waring, P.; Azar, W.; Mitchell, C.; Traficante, N.; Hendley, J.; Thorne, H.; Shackleton, M.; Miller, D.K.; Arnau, G.M.; Tothill, R.W.; Holloway, T.P.; Semple, T.; Harliwong, I.; Nourse, C.; Nourbakhsh, E.; Manning, S.; Idrisoglu, S.; Bruxner, T.J.C.; Christ, A.N.; Poudel, B.; Holmes, O.; Anderson, M.; Leonard, C.; Lonie, A.; Hall, N.; Wood, S.; Taylor, D.F.; Xu, Q.; Fink, J.L.; Waddell, N.; Drapkin, R.; Stronach, E.; Gabra, H.; Brown, R.; Jewell, A.; Nagaraj, S.H.; Markham, E.; Wilson, P.J.; Ellul, J.; McNally, O.; Doyle, M.A.; Vedururu, R.; Stewart, C.; Lengyel, E.; Pearson, J.V.; Waddell, N.; deFazio, A.; Grimmond, S.M.; Bowtell, D.D.L. Australian Ovarian Cancer Study Group. Corrigendum: Whole-genome characterization of chemoresistant ovarian cancer. Nature, 2015, 527(7578), 398.
[http://dx.doi.org/10.1038/nature15716] [PMID: 26503049]
[3]
Cho, K.R.; Shih, IeM. Ovarian cancer. Annu. Rev. Pathol., 2009, 4, 287-313.
[http://dx.doi.org/10.1146/annurev.pathol.4.110807.092246] [PMID: 18842102]
[4]
Torre, L.A.; Trabert, B.; DeSantis, C.E.; Miller, K.D.; Samimi, G.; Runowicz, C.D.; Gaudet, M.M.; Jemal, A.; Siegel, R.L. Ovarian cancer statistics, 2018. CA Cancer J. Clin., 2018, 68(4), 284-296.
[http://dx.doi.org/10.3322/caac.21456] [PMID: 29809280]
[5]
Roett, M.A.; Evans, P. Ovarian cancer: an overview. Am. Fam. Physician, 2009, 80(6), 609-616.
[PMID: 19817326]
[6]
Taylor, D.D.; Gercel-Taylor, C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol., 2008, 110(1), 13-21.
[http://dx.doi.org/10.1016/j.ygyno.2008.04.033] [PMID: 18589210]
[7]
Montagnana, M.; Benati, M.; Danese, E. Circulating biomarkers in epithelial ovarian cancer diagnosis: from present to future perspective. Ann. Transl. Med., 2017, 5(13), 276.
[http://dx.doi.org/10.21037/atm.2017.05.13] [PMID: 28758102]
[8]
Sturgeon, C.M.; Duffy, M.J.; Walker, G. The National Institute for Health and Clinical Excellence (NICE) guidelines for early detection of ovarian cancer: the pivotal role of the clinical laboratory. Ann. Clin. Biochem., 2011, 48(Pt 4), 295-299.
[http://dx.doi.org/10.1258/acb.2011.011117] [PMID: 21746796]
[9]
Seoung, J.; Park, Y-H.; Rhim, C.; Kim, S. Current possible drug therapies for ovarian cancer. J. Cancer Ther., 2014, 5(13), 1203.
[http://dx.doi.org/10.4236/jct.2014.513122]
[10]
Pinato, D.J.; Graham, J.; Gabra, H.; Sharma, R. Evolving concepts in the management of drug resistant ovarian cancer: dose dense chemotherapy and the reversal of clinical platinum resistance. Cancer Treat. Rev., 2013, 39(2), 153-160.
[http://dx.doi.org/10.1016/j.ctrv.2012.04.004] [PMID: 22595680]
[11]
Grunewald, T.; Ledermann, J.A. Targeted therapies for ovarian cancer. Best Pract. Res. Clin. Obstet. Gynaecol., 2017, 41, 139-152.
[http://dx.doi.org/10.1016/j.bpobgyn.2016.12.001] [PMID: 28111228]
[12]
ACOG Committee on Gynecologic Practice. The role of the generalist obstetrician-gynecologist in the early detection of ovarian cancer. Int. J. Gynaecol. Obstet., 2003, 80(2), 235-238.
[PMID: 12627605]
[13]
Xu, Y.; Xu, L.; Zheng, J.; Geng, L.; Zhao, S. MiR-101 inhibits ovarian carcinogenesis by repressing the expression of brain-derived neurotrophic factor. FEBS Open Bio, 2017, 7(9), 1258-1266.
[http://dx.doi.org/10.1002/2211-5463.12257] [PMID: 28904856]
[14]
Trams, E.G.; Lauter, C.J.; Salem, N., Jr; Heine, U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim. Biophys. Acta, 1981, 645(1), 63-70.
[http://dx.doi.org/10.1016/0005-2736(81)90512-5] [PMID: 6266476]
[15]
Hessvik, N.P.; Llorente, A. Current knowledge on exosome biogenesis and release. Cell. Mol. Life Sci., 2018, 75(2), 193-208.
[http://dx.doi.org/10.1007/s00018-017-2595-9] [PMID: 28733901]
[16]
Di Vizio, D.; Morello, M.; Dudley, A.C.; Schow, P.W.; Adam, R.M.; Morley, S.; Mulholland, D.; Rotinen, M.; Hager, M.H.; Insabato, L.; Moses, M.A.; Demichelis, F.; Lisanti, M.P.; Wu, H.; Klagsbrun, M.; Bhowmick, N.A.; Rubin, M.A.; D’Souza-Schorey, C.; Freeman, M.R. Large oncosomes in human prostate cancer tissues and in the circulation of mice with metastatic disease. Am. J. Pathol., 2012, 181(5), 1573-1584.
[http://dx.doi.org/10.1016/j.ajpath.2012.07.030] [PMID: 23022210]
[17]
Minciacchi, V.R.; You, S.; Spinelli, C.; Morley, S.; Zandian, M.; Aspuria, P-J.; Cavallini, L.; Ciardiello, C.; Reis Sobreiro, M.; Morello, M.; Kharmate, G.; Jang, S.C.; Kim, D-K.; Hosseini-Beheshti, E.; Tomlinson Guns, E.; Gleave, M.; Gho, Y.S.; Mathivanan, S.; Yang, W.; Freeman, M.R.; Di Vizio, D. Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles. Oncotarget, 2015, 6(13), 11327-11341.
[http://dx.doi.org/10.18632/oncotarget.3598] [PMID: 25857301]
[18]
Mathivanan, S.; Ji, H.; Simpson, R.J. Exosomes: extracellular organelles important in intercellular communication. J. Proteomics, 2010, 73(10), 1907-1920.
[http://dx.doi.org/10.1016/j.jprot.2010.06.006] [PMID: 20601276]
[19]
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.
[http://dx.doi.org/10.1038/ncb1596] [PMID: 17486113]
[20]
Skog, J.; Würdinger, T.; van Rijn, S.; Meijer, D.H.; Gainche, L.; Sena-Esteves, M.; Curry, W.T., Jr; Carter, B.S.; Krichevsky, A.M.; Breakefield, X.O. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol., 2008, 10(12), 1470-1476.
[http://dx.doi.org/10.1038/ncb1800] [PMID: 19011622]
[21]
Al-Nedawi, K.; Meehan, B.; Micallef, J.; Lhotak, V.; May, L.; Guha, A.; Rak, J. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol., 2008, 10(5), 619-624.
[http://dx.doi.org/10.1038/ncb1725] [PMID: 18425114]
[22]
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.
[http://dx.doi.org/10.1016/j.ccell.2014.09.005] [PMID: 25446899]
[23]
Kim, D-K.; Lee, J.; Kim, S.R.; Choi, D-S.; Yoon, Y.J.; Kim, J.H.; Go, G.; Nhung, D.; Hong, K.; Jang, S.C.; Kim, S-H.; Park, K-S.; Kim, O.Y.; Park, H.T.; Seo, J.H.; Aikawa, E.; Baj-Krzyworzeka, M.; van Balkom, B.W.M.; Belting, M.; Blanc, L.; Bond, V.; Bongiovanni, A.; Borràs, F.E.; Buée, L.; Buzás, E.I.; Cheng, L.; Clayton, A.; Cocucci, E.; Dela Cruz, C.S.; Desiderio, D.M.; Di Vizio, D.; Ekström, K.; Falcon-Perez, J.M.; Gardiner, C.; Giebel, B.; Greening, D.W.; Gross, J.C.; Gupta, D.; Hendrix, A.; Hill, A.F.; Hill, M.M.; Nolte-’t Hoen, E.; Hwang, D.W.; Inal, J.; Jagannadham, M.V.; Jayachandran, M.; Jee, Y-K.; Jørgensen, M.; Kim, K.P.; Kim, Y-K.; Kislinger, T.; Lässer, C.; Lee, D.S.; Lee, H.; van Leeuwen, J.; Lener, T.; Liu, M-L.; Lötvall, J.; Marcilla, A.; Mathivanan, S.; Möller, A.; Morhayim, J.; Mullier, F.; Nazarenko, I.; Nieuwland, R.; Nunes, D.N.; Pang, K.; Park, J.; Patel, T.; Pocsfalvi, G.; Del Portillo, H.; Putz, U.; Ramirez, M.I.; Rodrigues, M.L.; Roh, T-Y.; Royo, F.; Sahoo, S.; Schiffelers, R.; Sharma, S.; Siljander, P.; Simpson, R.J.; Soekmadji, C.; Stahl, P.; Stensballe, A.; Stępień, E.; Tahara, H.; Trummer, A.; Valadi, H.; Vella, L.J.; Wai, S.N.; Witwer, K.; Yáñez-Mó, M.; Youn, H.; Zeidler, R.; Gho, Y.S. EVpedia: a community web portal for extracellular vesicles research. Bioinformatics, 2015, 31(6), 933-939.
[http://dx.doi.org/10.1093/bioinformatics/btu741] [PMID: 25388151]
[24]
Camussi, G.; Deregibus, M-C.; Bruno, S.; Grange, C.; Fonsato, V.; Tetta, C. Exosome/microvesicle-mediated epigenetic reprogramming of cells. Am. J. Cancer Res., 2011, 1(1), 98-110.
[PMID: 21969178]
[25]
Carollo, E.; Paris, B.; Samuel, P.; Pantazi, P.; Bartelli, T.F.; Dias-Neto, E.; Brooks, S.A.; Pink, R.C.; Carter, D.R.F. Detecting ovarian cancer using extracellular vesicles: progress and possibilities. Biochem. Soc. Trans., 2019, 47(1), 295-304.
[http://dx.doi.org/10.1042/BST20180286] [PMID: 30700499]
[26]
King, H.W.; Michael, M.Z.; Gleadle, J.M. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer, 2012, 12, 421.
[http://dx.doi.org/10.1186/1471-2407-12-421] [PMID: 22998595]
[27]
Kerr, J.F.; Wyllie, A.H.; Currie, A.R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer, 1972, 26(4), 239-257.
[http://dx.doi.org/10.1038/bjc.1972.33] [PMID: 4561027]
[28]
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.
[http://dx.doi.org/10.1073/pnas.0804543106] [PMID: 19234131]
[29]
Mitchell, P.J.; Welton, J.; Staffurth, J.; Court, J.; Mason, M.D.; Tabi, Z.; Clayton, A. Can urinary exosomes act as treatment response markers in prostate cancer? J. Transl. Med., 2009, 7, 4.
[http://dx.doi.org/10.1186/1479-5876-7-4] [PMID: 19138409]
[30]
Ge, Q.; Zhou, Y.; Lu, J.; Bai, Y.; Xie, X.; Lu, Z. miRNA in plasma exosome is stable under different storage conditions. Molecules, 2014, 19(2), 1568-1575.
[http://dx.doi.org/10.3390/molecules19021568] [PMID: 24473213]
[31]
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]
[32]
Giannopoulou, L.; Zavridou, M.; Kasimir-Bauer, S.; Lianidou, E.S. Liquid biopsy in ovarian cancer: the potential of circulating miRNAs and exosomes. Transl. Res., 2019, 205, 77-91.
[http://dx.doi.org/10.1016/j.trsl.2018.10.003] [PMID: 30391474]
[33]
Sharma, R.; Huang, X.; Brekken, R.A.; Schroit, A.J. Detection of phosphatidylserine-positive exosomes for the diagnosis of early-stage malignancies. Br. J. Cancer, 2017, 117(4), 545-552.
[http://dx.doi.org/10.1038/bjc.2017.183] [PMID: 28641308]
[34]
Szajnik, M.; Derbis, M.; Lach, M.; Patalas, P.; Michalak, M.; Drzewiecka, H.; Szpurek, D.; Nowakowski, A.; Spaczynski, M.; Baranowski, W.; Whiteside, T.L. Exosomes in plasma of patients with ovarian carcinoma: potential biomarkers of tumor progression and response to therapy. Gynecol. Obstet. (Sunnyvale), 2013,(Suppl. 4), 3.
[PMID: 24466501]
[35]
Li, J.; Sherman-Baust, C.A.; Tsai-Turton, M.; Bristow, R.E.; Roden, R.B.; Morin, P.J. Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer. BMC Cancer, 2009, 9, 244.
[http://dx.doi.org/10.1186/1471-2407-9-244] [PMID: 19619303]
[36]
Kabe, Y.; Suematsu, M.; Sakamoto, S.; Hirai, M.; Koike, I.; Hishiki, T.; Matsuda, A.; Hasegawa, Y.; Tsujita, K.; Ono, M.; Minegishi, N.; Hozawa, A.; Murakami, Y.; Kubo, M.; Itonaga, M.; Handa, H. Development of a highly sensitive device for counting the number of disease-specific exosomes in human sera. Clin. Chem., 2018, 64(10), 1463-1473.
[http://dx.doi.org/10.1373/clinchem.2018.291963] [PMID: 30021922]
[37]
Gobbo, J.; Marcion, G.; Cordonnier, M.; Dias, A.M.M.; Pernet, N.; Hammann, A.; Richaud, S.; Mjahed, H.; Isambert, N.; Clausse, V.; Rébé, C.; Bertaut, A.; Goussot, V.; Lirussi, F.; Ghiringhelli, F.; de Thonel, A.; Fumoleau, P.; Seigneuric, R.; Garrido, C. Restoring anticancer immune response by targeting tumor-derived exosomes with a HSP70 peptide aptamer. J. Natl. Cancer Inst., 2015, 108(3) , doi: 10.1093/jnci/djv330
[http://dx.doi.org/10.1093/jnci/djv330] [PMID: 26598503]
[38]
Yokoi, A.; Yoshioka, Y.; Hirakawa, A.; Yamamoto, Y.; Ishikawa, M.; Ikeda, S-I.; Kato, T.; Niimi, K.; Kajiyama, H.; Kikkawa, F.; Ochiya, T. A combination of circulating miRNAs for the early detection of ovarian cancer. Oncotarget, 2017, 8(52), 89811-89823.
[http://dx.doi.org/10.18632/oncotarget.20688] [PMID: 29163790]
[39]
Kobayashi, M.; Sawada, K.; Nakamura, K.; Yoshimura, A.; Miyamoto, M.; Shimizu, A.; Ishida, K.; Nakatsuka, E.; Kodama, M.; Hashimoto, K.; Mabuchi, S.; Kimura, T. Exosomal miR-1290 is a potential biomarker of high-grade serous ovarian carcinoma and can discriminate patients from those with malignancies of other histological types. J. Ovarian Res., 2018, 11(1), 81.
[http://dx.doi.org/10.1186/s13048-018-0458-0] [PMID: 30219071]
[40]
Meng, X.; Müller, V.; Milde-Langosch, K.; Trillsch, F.; Pantel, K.; Schwarzenbach, H. Diagnostic and prognostic relevance of circulating exosomal miR-373, miR-200a, miR-200b and miR-200c in patients with epithelial ovarian cancer. Oncotarget, 2016, 7(13), 16923-16935.
[http://dx.doi.org/10.18632/oncotarget.7850] [PMID: 26943577]
[41]
Pan, C.; Stevic, I.; Müller, V.; Ni, Q.; Oliveira-Ferrer, L.; Pantel, K.; Schwarzenbach, H. Exosomal microRNAs as tumor markers in epithelial ovarian cancer. Mol. Oncol., 2018, 12(11), 1935-1948.
[http://dx.doi.org/10.1002/1878-0261.12371] [PMID: 30107086]
[42]
Kim, S.; Choi, M.C.; Jeong, J-Y.; Hwang, S.; Jung, S.G.; Joo, W.D.; Park, H.; Song, S.H.; Lee, C.; Kim, T.H.; An, H-J. Serum exosomal miRNA-145 and miRNA-200c as promising biomarkers for preoperative diagnosis of ovarian carcinomas. J. Cancer, 2019, 10(9), 1958-1967.
[http://dx.doi.org/10.7150/jca.30231] [PMID: 31205555]
[43]
Zhang, H.; Xu, S.; Liu, X. MicroRNA profiling of plasma exosomes from patients with ovarian cancer using high-throughput sequencing. Oncol. Lett., 2019, 17(6), 5601-5607.
[http://dx.doi.org/10.3892/ol.2019.10220] [PMID: 31186782]
[44]
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]
[45]
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]
[46]
Su, Y.Y.; Sun, L.; Guo, Z.R.; Li, J.C.; Bai, T.T.; Cai, X.X.; Li, W.H.; Zhu, Y.F. Upregulated expression of serum exosomal miR-375 and miR-1307 enhance the diagnostic power of CA125 for ovarian cancer. J. Ovarian Res., 2019, 12(1), 6.
[http://dx.doi.org/10.1186/s13048-018-0477-x] [PMID: 30670062]
[47]
Hang, W.; Feng, Y.; Sang, Z.; Yang, Y.; Zhu, Y.; Huang, Q.; Xi, X. Downregulation of miR-145-5p in cancer cells and their derived exosomes may contribute to the development of ovarian cancer by targeting CT. Int. J. Mol. Med., 2019, 43(1), 256-266.
[PMID: 30365097]
[48]
Zhang, S.; Zhang, X.; Fu, X.; Li, W.; Xing, S.; Yang, Y. Identification of common differentially-expressed miRNAs in ovarian cancer cells and their exosomes compared with normal ovarian surface epithelial cell cells. Oncol. Lett., 2018, 16(2), 2391-2401.
[http://dx.doi.org/10.3892/ol.2018.8954] [PMID: 30013629]
[49]
Yang, C.; Kim, H.S.; Song, G.; Lim, W. The potential role of exosomes derived from ovarian cancer cells for diagnostic and therapeutic approaches. J. Cell. Physiol., 2019, 234(12), 21493-21503.
[http://dx.doi.org/10.1002/jcp.28905] [PMID: 31144314]
[50]
Kim, S.; Kim, B.; Song, Y.S. Ascites modulates cancer cell behavior, contributing to tumor heterogeneity in ovarian cancer. Cancer Sci., 2016, 107(9), 1173-1178.
[http://dx.doi.org/10.1111/cas.12987] [PMID: 27297561]
[51]
Yamamoto, C.M.; Oakes, M.L.; Murakami, T.; Muto, M.G.; Berkowitz, R.S.; Ng, S-W. Comparison of benign peritoneal fluid- and ovarian cancer ascites-derived extracellular vesicle RNA biomarkers. J. Ovarian Res., 2018, 11(1), 20.
[http://dx.doi.org/10.1186/s13048-018-0391-2] [PMID: 29499737]
[52]
Cappellesso, R.; Tinazzi, A.; Giurici, T.; Simonato, F.; Guzzardo, V.; Ventura, L.; Crescenzi, M.; Chiarelli, S.; Fassina, A. Programmed cell death 4 and microRNA 21 inverse expression is maintained in cells and exosomes from ovarian serous carcinoma effusions. Cancer Cytopathol., 2014, 122(9), 685-693.
[http://dx.doi.org/10.1002/cncy.21442] [PMID: 24888238]
[53]
Reiner, A.T.; Tan, S.; Agreiter, C.; Auer, K.; Bachmayr-Heyda, A.; Aust, S.; Pecha, N.; Mandorfer, M.; Pils, D.; Brisson, A.R.; Zeillinger, R.; Lim, S.K. EV-associated MMP9 in high-grade serous ovarian cancer is preferentially localized to annexin V-binding EVs. Dis. Markers, 2017, 2017, 9653194.
[http://dx.doi.org/10.1155/2017/9653194] [PMID: 28607529]
[54]
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]
[55]
Yunusova, N.V.; Patysheva, M.R.; Molchanov, S.V.; Zambalova, E.A.; Grigor’eva, A.E.; Kolomiets, L.A.; Ochirov, M.O.; Tamkovich, S.N.; Kondakova, I.V. Metalloproteinases at the surface of small extrcellular vesicles in advanced ovarian cancer: relationships with ascites volume and peritoneal canceromatosis index. Clin. Chim. Acta, 2019, 494, 116-122.
[http://dx.doi.org/10.1016/j.cca.2019.03.1621] [PMID: 30904547]
[56]
Chen, X.; Zhou, J.; Li, X.; Wang, X.; Lin, Y.; Wang, X. Exosomes derived from hypoxic epithelial ovarian cancer cells deliver microRNAs to macrophages and elicit a tumor-promoted phenotype. Cancer Lett., 2018, 435, 80-91.
[http://dx.doi.org/10.1016/j.canlet.2018.08.001] [PMID: 30098399]
[57]
Ying, X.; Wu, Q.; Wu, X.; Zhu, Q.; Wang, X.; Jiang, L.; Chen, X.; Wang, X. Epithelial ovarian cancer-secreted exosomal miR-222-3p induces polarization of tumor-associated macrophages. Oncotarget, 2016, 7(28), 43076-43087.
[http://dx.doi.org/10.18632/oncotarget.9246] [PMID: 27172798]
[58]
Chen, X.; Ying, X.; Wang, X.; Wu, X.; Zhu, Q.; Wang, X. Exosomes derived from hypoxic epithelial ovarian cancer deliver microRNA-940 to induce macrophage M2 polarization. Oncol. Rep., 2017, 38(1), 522-528.
[http://dx.doi.org/10.3892/or.2017.5697] [PMID: 28586039]
[59]
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]
[60]
X, Z.; H, S.; X, Y.; M, Y.; H, W.; Q, C.; F, F.; Y, L.; W, X.; Y, L., Macrophages derived exosomes deliver miR-223 to epithelial ovarian cancer cells to elicit a chemoresistant phenotype. J. Exp. Clin. Cancer Res., 2019, 38(1), 81.
[61]
Tang, X.; Liu, S.; Liu, Y.; Lin, X.; Zheng, T.; Liu, X.; Qiu, J.; Hua, K. Circulating serum exosomal aHIF is a novel prognostic predictor for epithelial ovarian cancer. OncoTargets Ther., 2019, 12, 7699-7711.
[http://dx.doi.org/10.2147/OTT.S220533] [PMID: 31571921]
[62]
Zhang, F.F.; Zhu, Y.F.; Zhao, Q.N.; Yang, D.T.; Dong, Y.P.; Jiang, L.; Xing, W.X.; Li, X.Y.; Xing, H.; Shi, M.; Chen, Y.; Bruce, I.C.; Jin, J.; Ma, X. Microvesicles mediate transfer of P-glycoprotein to paclitaxel-sensitive A2780 human ovarian cancer cells, conferring paclitaxel-resistance. Eur. J. Pharmacol., 2014, 738, 83-90.
[http://dx.doi.org/10.1016/j.ejphar.2014.05.026] [PMID: 24877693]
[63]
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.
[http://dx.doi.org/10.1158/1535-7163.MCT-05-0102] [PMID: 16227410]
[64]
Yin, J.; Yan, X.; Yao, X.; Zhang, Y.; Shan, Y.; Mao, N.; Yang, Y.; Pan, L. Secretion of annexin A3 from ovarian cancer cells and its association with platinum resistance in ovarian cancer patients. J. Cell. Mol. Med., 2012, 16(2), 337-348.
[http://dx.doi.org/10.1111/j.1582-4934.2011.01316.x] [PMID: 21435174]
[65]
Prat, J. FIGO Committee on Gynecologic Oncology. Abridged republication of FIGO’s staging classification for cancer of the ovary, fallopian tube, and peritoneum. Cancer, 2015, 121(19), 3452-3454.
[http://dx.doi.org/10.1002/cncr.29524] [PMID: 26110780]
[66]
Kanlikilicer, P.; Rashed, M.H.; Bayraktar, R.; Mitra, R.; Ivan, C.; Aslan, B.; Zhang, X.; Filant, J.; Silva, A.M.; Rodriguez-Aguayo, C.; Bayraktar, E.; Pichler, M.; Ozpolat, B.; Calin, G.A.; Sood, A.K.; Lopez-Berestein, G. Ubiquitous release of exosomal tumor suppressor miR-6126 from ovarian cancer cells. Cancer Res., 2016, 76(24), 7194-7207.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-0714] [PMID: 27742688]
[67]
Au Yeung, C.L.; Co, N.N.; Tsuruga, T.; Yeung, T.L.; Kwan, S.Y.; Leung, C.S.; Li, Y.; Lu, E.S.; Kwan, K.; Wong, K.K.; Schmandt, R.; Lu, K.H.; Mok, S.C. Exosomal transfer of stroma-derived miR21 confers paclitaxel resistance in ovarian cancer cells through targeting APAF1. Nat. Commun., 2016, 7, 11150.
[http://dx.doi.org/10.1038/ncomms11150] [PMID: 27021436]
[68]
Crow, J.; Atay, S.; Banskota, S.; Artale, B.; Schmitt, S.; Godwin, A.K. Exosomes as mediators of platinum resistance in ovarian cancer. Oncotarget, 2017, 8(7), 11917-11936.
[http://dx.doi.org/10.18632/oncotarget.14440] [PMID: 28060758]
[69]
Dorayappan, K.D.P.; Wanner, R.; Wallbillich, J.J.; Saini, U.; Zingarelli, R.; Suarez, A.A.; Cohn, D.E.; Selvendiran, K. Hypoxia-induced exosomes contribute to a more aggressive and chemoresistant ovarian cancer phenotype: a novel mechanism linking STAT3/Rab proteins. Oncogene, 2018, 37(28), 3806-3821.
[http://dx.doi.org/10.1038/s41388-018-0189-0] [PMID: 29636548]
[70]
Reza, A.M.M.T.; Choi, Y-J.; Yasuda, H.; Kim, J-H. Human adipose mesenchymal stem cell-derived exosomal-miRNAs are critical factors for inducing anti-proliferation signalling to A2780 and SKOV-3 ovarian cancer cells. Sci. Rep., 2016, 6, 38498.
[http://dx.doi.org/10.1038/srep38498] [PMID: 27929108]
[71]
Zhang, W.; Yang, J.; Cao, D.; You, Y.; Shen, K.; Peng, P. Regulation of exosomes released from normal ovarian epithelial cells and ovarian cancer cells. Tumour Biol., 2016. Epub Ahead of Print.
[http://dx.doi.org/10.1007/s13277-016-5394-2] [PMID: 27714673]
[72]
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]
[73]
Shenoy, G.N.; Loyall, J.; Berenson, C.S.; Kelleher, R.J., Jr; Iyer, V.; Balu-Iyer, S.V.; Odunsi, K.; Bankert, R.B. Sialic acid-dependent inhibition of T cells by exosomal ganglioside GD3 in ovarian tumor microenvironments. J. Immunol., 2018, 201(12), 3750-3758.
[http://dx.doi.org/10.4049/jimmunol.1801041] [PMID: 30446565]
[74]
Toffoli, G.; Hadla, M.; Corona, G.; Caligiuri, I.; Palazzolo, S.; Semeraro, S.; Gamini, A.; Canzonieri, V.; Rizzolio, F. Exosomal doxorubicin reduces the cardiac toxicity of doxorubicin. Nanomedicine (Lond.), 2015, 10(19), 2963-2971.
[http://dx.doi.org/10.2217/nnm.15.118] [PMID: 26420143]
[75]
Hadla, M.; Palazzolo, S.; Corona, G.; Caligiuri, I.; Canzonieri, V.; Toffoli, G.; Rizzolio, F. Exosomes increase the therapeutic index of doxorubicin in breast and ovarian cancer mouse models. Nanomedicine (Lond.), 2016, 11(18), 2431-2441.
[http://dx.doi.org/10.2217/nnm-2016-0154] [PMID: 27558906]
[76]
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), E798.
[http://dx.doi.org/10.3390/cancers11060798] [PMID: 31181850]
[77]
Samuel, P.; Mulcahy, L.A.; Furlong, F.; McCarthy, H.O.; Brooks, S.A.; Fabbri, M.; Pink, R.C.; Carter, D.R.F. Cisplatin induces the release of extracellular vesicles from ovarian cancer cells that can induce invasiveness and drug resistance in bystander cells. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2018, 373(1737), 373.
[http://dx.doi.org/10.1098/rstb.2017.0065] [PMID: 29158318]
[78]
Wu, S.; Turner, K.M.; Nguyen, N.; Raviram, R.; Erb, M.; Santini, J.; Luebeck, J.; Rajkumar, U.; Diao, Y.; Li, B.; Zhang, W.; Jameson, N.; Corces, M.R.; Granja, J.M.; Chen, X.; Coruh, C.; Abnousi, A.; Houston, J.; Ye, Z.; Hu, R.; Yu, M.; Kim, H.; Law, J.A.; Verhaak, R.G.W.; Hu, M.; Furnari, F.B.; Chang, H.Y.; Ren, B.; Bafna, V.; Mischel, P.S. Circular ecDNA promotes accessible chromatin and high oncogene expression. Nature, 2019, 575(7784), 699-703.
[http://dx.doi.org/10.1038/s41586-019-1763-5] [PMID: 31748743]
[79]
Khatami, F.; Larijani, B.; Tavangar, S.M. The presence of tumor extrachomosomal circular DNA (ecDNA) as a component of liquid biopsy in blood. Med. Hypotheses, 2018, 114, 5-7.
[http://dx.doi.org/10.1016/j.mehy.2018.02.018] [PMID: 29602465]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy