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Current Molecular Medicine

Editor-in-Chief

ISSN (Print): 1566-5240
ISSN (Online): 1875-5666

Mini-Review Article

Advances in Exosomal microRNAs and Proteins in Ovarian Cancer Diagnosis, Prognosis, and Treatment

Author(s): Tiansheng Qin*, Fan Chen, Jiaojiao Zhu, Yaoyao Ding and Qianqian Zhang

Volume 23, Issue 6, 2023

Published on: 17 August, 2022

Page: [509 - 520] Pages: 12

DOI: 10.2174/1566524022666220628160009

Price: $65

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Abstract

Late diagnosis, postoperative recurrence, and chemotherapy resistance are the main causes of the high mortality rate in ovarian cancer (OC). Understanding the molecular mechanisms in the pathogenesis and progression of OC may contribute to discovering new tumor biomarkers and therapeutic targets for OC. Exosomes are small extracellular vesicles derived from different types of cells that carry cargos, including nucleic acids, proteins, and lipids, and are pivotal mediators of intercellular communication in the tumor microenvironment. There is emerging evidence that exosomal proteins and nucleic acids play pivotal roles in facilitating the progression and drug resistance of OC. Identification of these factors may aid in the future diagnosis of OC. Furthermore, they also have promising value as OC therapeutic targets that can improve the prognosis. In the current review, we summarize the progress of exosomal research in OC, especially highlighting the most updated roles of exosomal microRNAs and proteins in the diagnosis, prognosis, therapy, and drug resistance of OC in order to facilitate future studies in this area.

Keywords: Exosomes, microRNAs, proteins, ovarian cancer, diagnosis, prognosis, therapy, drug resistance.

[1]
Chan JK, Cheung MK, Husain A, et al. Patterns and progress in ovarian cancer over 14 years. Obstet Gynecol 2006; 108(3 Pt 1): 521-8.
[http://dx.doi.org/10.1097/01.AOG.0000231680.58221.a7] [PMID: 16946210]
[2]
Jelovac D, Armstrong DK. Recent progress in the diagnosis and treatment of ovarian cancer. CA Cancer J Clin 2011; 61(3): 183-203.
[http://dx.doi.org/10.3322/caac.20113] [PMID: 21521830]
[3]
Kurnit KC, Fleming GF, Lengyel E. Updates and new options in advanced epithelial ovarian cancer treatment. Obstet Gynecol 2021; 137(1): 108-21.
[http://dx.doi.org/10.1097/AOG.0000000000004173] [PMID: 33278287]
[4]
Tewari KS, Burger RA, Enserro D, et al. Final overall survival of a randomized trial of bevacizumab for primary treatment of ovarian cancer. J Clin Oncol 2019; 37(26): 2317-28.
[http://dx.doi.org/10.1200/JCO.19.01009] [PMID: 31216226]
[5]
Hamanishi J, Mandai M, Ikeda T, et al. Safety and antitumor activity of anti-pd-1 antibody, nivolumab, in patients with platinum-resistant ovarian cancer. J Clin Oncol 2015; 33(34): 4015-22.
[http://dx.doi.org/10.1200/JCO.2015.62.3397] [PMID: 26351349]
[6]
Pujade-Lauraine E, Ledermann JA, Selle F, et al. Olaparib tablets as maintenance therapy in patients with platinum-sensitive, relapsed ovarian cancer and a BRCA1/2 mutation (SOLO2/ENGOT-Ov21): A double-blind, randomised, placebo-controlled, phase 3 trial. Lancet Oncol 2017; 18(9): 1274-84.
[http://dx.doi.org/10.1016/S1470-2045(17)30469-2] [PMID: 28754483]
[7]
Shetty M. Imaging and differential diagnosis of ovarian cancer. CT and MRI 2019; 40(4): 302-18.
[http://dx.doi.org/10.1053/j.sult.2019.04.002] [PMID: 31375171]
[8]
Mould T. An overview of current diagnosis and treatment in ovarian cancer. Int J Gynecol Cancer 2012; 1: 2-4.
[9]
Doubeni CA, Doubeni AR, Myers AE. Diagnosis and management of ovarian cancer. Am Fam Physician 2016; 93(11): 937-44.
[PMID: 27281838]
[10]
Zhang M, Cheng S, Jin Y, Zhao Y, Wang Y. Roles of CA125 in diagnosis, prediction, and oncogenesis of ovarian cancer. Biochim Biophys Acta Rev Cancer 2021; 1875(2): 188503.
[http://dx.doi.org/10.1016/j.bbcan.2021.188503] [PMID: 33421585]
[11]
Karam AK, Karlan BY. Ovarian cancer: The duplicity of CA125 measurement. Nat Rev Clin Oncol 2010; 7(6): 335-9.
[http://dx.doi.org/10.1038/nrclinonc.2010.44] [PMID: 20368726]
[12]
Wright JD, Hou JY, Burke WM, et al. Utilization and toxicity of alternative delivery methods of adjuvant chemotherapy for ovarian cancer. Obstet Gynecol 2016; 127(6): 985-91.
[http://dx.doi.org/10.1097/AOG.0000000000001436] [PMID: 27159764]
[13]
Cristea M, Han E, Salmon L, Morgan RJ Jr. Practical considerations in ovarian cancer chemotherapy. Ther Adv Med Oncol 2010; 2(3): 175-87.
[http://dx.doi.org/10.1177/1758834010361333] [PMID: 21789133]
[14]
Elies A, Rivière S, Pouget N, et al. The role of neoadjuvant chemotherapy in ovarian cancer. Expert Rev Anticancer Ther 2018; 18(6): 555-66.
[http://dx.doi.org/10.1080/14737140.2018.1458614] [PMID: 29633903]
[15]
Bristow RE, Chang J, Ziogas A, Campos B, Chavez LR, Anton-Culver H. Impact of national cancer institute comprehensive cancer centers on ovarian cancer treatment and survival. J Am Coll Surg 2015; 220(5): 940-50.
[http://dx.doi.org/10.1016/j.jamcollsurg.2015.01.056] [PMID: 25840536]
[16]
Gao Y, Foster R, Yang X, et al. Up-regulation of CD44 in the development of metastasis, recurrence and drug resistance of ovarian cancer. Oncotarget 2015; 6(11): 9313-26.
[http://dx.doi.org/10.18632/oncotarget.3220] [PMID: 25823654]
[17]
Shen J, Zhu X, Fei J, Shi P, Yu S, Zhou J. Advances of exosome in the development of ovarian cancer and its diagnostic and therapeutic prospect. OncoTargets Ther 2018; 11: 2831-41.
[http://dx.doi.org/10.2147/OTT.S159829] [PMID: 29844681]
[18]
Croft PK, Sharma S, Godbole N, Rice GE, Salomon C. Ovarian-cancer-associated extracellular vesicles: Microenvironmental regulation and potential clinical applications. Cells 2021; 10(9): 2272.
[http://dx.doi.org/10.3390/cells10092272] [PMID: 34571921]
[19]
Alharbi M, Zuñiga F, Elfeky O, et al. The potential role of miRNAs and exosomes in chemotherapy in ovarian cancer. Endocr Relat Cancer 2018; 25(12): R663-85.
[http://dx.doi.org/10.1530/ERC-18-0019] [PMID: 30400025]
[20]
Wani TU, Mohi-Ud-Din R, Mir RH, et al. Exosomes harnessed as nanocarriers for cancer therapy - current status and potential for future clinical applications. Curr Mol Med 2021; 21(9): 707-23.
[http://dx.doi.org/10.2174/1566524020666200915111618] [PMID: 32933459]
[21]
Hu T, Wolfram J, Srivastava S. Extracellular vesicles in cancer detection: Hopes and hypes. Trends Cancer 2021; 7(2): 122-33.
[http://dx.doi.org/10.1016/j.trecan.2020.09.003] [PMID: 33008796]
[22]
Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: Cell-to-cell mediators of metastasis. Cancer Cell 2016; 30(6): 836-48.
[http://dx.doi.org/10.1016/j.ccell.2016.10.009] [PMID: 27960084]
[23]
Kalluri R. The biology and function of exosomes in cancer. J Clin Invest 2016; 126(4): 1208-15.
[http://dx.doi.org/10.1172/JCI81135] [PMID: 27035812]
[24]
Milane L, Singh A, Mattheolabakis G, Suresh M, Amiji MM. Exosome mediated communication within the tumor microenvironment. J Control Release 2015; 219: 278-94.
[25]
Yu W, Hurley J, Roberts D, et al. Exosome-based liquid biopsies in cancer: Opportunities and challenges. Ann Oncol 2021; 32(4): 466-77.
[http://dx.doi.org/10.1016/j.annonc.2021.01.074] [PMID: 33548389]
[26]
Giannopoulou L, Lianidou ES. Liquid biopsy in ovarian cancer. Adv Clin Chem 2020; 97: 13-71.
[http://dx.doi.org/10.1016/bs.acc.2020.01.001] [PMID: 32448432]
[27]
Linder M, Pogge von Strandmann E. The role of extracellular hsp70 in the function of tumor-associated immune cells. Cancers 2021; 13(18): 4721.
[http://dx.doi.org/10.3390/cancers13184721] [PMID: 34572948]
[28]
Yang J, Zhang Y, Gao X, et al. Plasma-derived exosomal alix as a novel biomarker for diagnosis and classification of pancreatic cancer. Front Oncol 2021; 11: 628346.
[http://dx.doi.org/10.3389/fonc.2021.628346] [PMID: 34026608]
[29]
Ge R, Tan E, Sharghi-Namini S, Asada HH. Exosomes in cancer microenvironment and beyond: Have we overlooked these extracellular messengers? Cancer Microenviron 2012; 5(3): 323-32.
[http://dx.doi.org/10.1007/s12307-012-0110-2] [PMID: 22585423]
[30]
Giannopoulou L, Zavridou M, Kasimir-Bauer S, Lianidou ES. 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]
[31]
Nakamura K, Sawada K, Kobayashi M, et al. Role of the exosome in ovarian cancer progression and its potential as a therapeutic target. Cancers 2019; 11(8): E1147.
[http://dx.doi.org/10.3390/cancers11081147] [PMID: 31405096]
[32]
Mashouri L, Yousefi H, Aref AR, Ahadi AM, Molaei F, Alahari SK. Exosomes: Composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol Cancer 2019; 18(1): 75.
[http://dx.doi.org/10.1186/s12943-019-0991-5] [PMID: 30940145]
[33]
Crow J, Atay S, Banskota S, Artale B, Schmitt S, Godwin AK. Exosomes as mediators of platinum resistance in ovarian cancer. Oncotarget 2017; 8(7): 11917-36.
[http://dx.doi.org/10.18632/oncotarget.14440] [PMID: 28060758]
[34]
Kazemi NY, Gendrot B, Berishvili E, Markovic SN, Cohen M. The role and clinical interest of extracellular vesicles in pregnancy and ovarian cancer. Biomedicines 2021; 9(9): 1257.
[http://dx.doi.org/10.3390/biomedicines9091257] [PMID: 34572444]
[35]
Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: Selective externalization of the receptor. Cell 1983; 33(3): 967-78.
[http://dx.doi.org/10.1016/0092-8674(83)90040-5] [PMID: 6307529]
[36]
Lai RC, Arslan F, Lee MM, et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res 2010; 4(3): 214-22.
[http://dx.doi.org/10.1016/j.scr.2009.12.003] [PMID: 20138817]
[37]
Blanchard N, Lankar D, Faure F, et al. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol 2002; 168(7): 3235-41.
[http://dx.doi.org/10.4049/jimmunol.168.7.3235] [PMID: 11907077]
[38]
Park JE, Tan HS, Datta A, et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 2010; 9(6): 1085-99.
[http://dx.doi.org/10.1074/mcp.M900381-MCP200] [PMID: 20124223]
[39]
Hedlund M, Nagaeva O, Kargl D, Baranov V, Mincheva-Nilsson L. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS One 2011; 6(2): e16899.
[http://dx.doi.org/10.1371/journal.pone.0016899] [PMID: 21364924]
[40]
King HW, Michael MZ, Gleadle JM. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 2012; 12(1): 421.
[http://dx.doi.org/10.1186/1471-2407-12-421] [PMID: 22998595]
[41]
Henderson MC, Azorsa DO. The genomic and proteomic content of cancer cell-derived exosomes. Front Oncol 2012; 2: 38.
[http://dx.doi.org/10.3389/fonc.2012.00038] [PMID: 22649786]
[42]
Logozzi M, De Milito A, Lugini L, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One 2009; 4(4): e5219.
[http://dx.doi.org/10.1371/journal.pone.0005219] [PMID: 19381331]
[43]
Hegmans JP, Bard MP, Hemmes A, et al. Proteomic analysis of exosomes secreted by human mesothelioma cells. Am J Pathol 2004; 164(5): 1807-15.
[http://dx.doi.org/10.1016/S0002-9440(10)63739-X] [PMID: 15111327]
[44]
Simpson RJ, Jensen SS, Lim JW. Proteomic profiling of exosomes: Current perspectives. Proteomics 2008; 8(19): 4083-99.
[http://dx.doi.org/10.1002/pmic.200800109] [PMID: 18780348]
[45]
Pfeffer SR. Two Rabs for exosome release. Nat Cell Biol 2010; 12(1): 3-4.
[http://dx.doi.org/10.1038/ncb0110-3] [PMID: 20027197]
[46]
McCready J, Sims JD, Chan D, Jay DG. Secretion of extracellular hsp90alpha via exosomes increases cancer cell motility: A role for plasminogen activation. BMC Cancer 2010; 10(1): 294.
[http://dx.doi.org/10.1186/1471-2407-10-294] [PMID: 20553606]
[47]
Beermann J, Piccoli MT, Viereck J, Thum T. Non-coding RNAs in development and disease: Background, mechanisms, and therapeutic approaches. Physiol Rev 2016; 96(4): 1297-325.
[http://dx.doi.org/10.1152/physrev.00041.2015] [PMID: 27535639]
[48]
Tomasetti M, Lee W, Santarelli L, Neuzil J. Exosome-derived microRNAs in cancer metabolism: Possible implications in cancer diagnostics and therapy. Exp Mol Med 2017; 49(1): e285.
[http://dx.doi.org/10.1038/emm.2016.153] [PMID: 28104913]
[49]
Skotland T, Hessvik NP, Sandvig K, Llorente A. Exosomal lipid composition and the role of ether lipids and phosphoinositides in exosome biology. J Lipid Res 2019; 60(1): 9-18.
[http://dx.doi.org/10.1194/jlr.R084343] [PMID: 30076207]
[50]
Pan C, Stevic I, Müller V, et al. Exosomal microRNAs as tumor markers in epithelial ovarian cancer. Mol Oncol 2018; 12(11): 1935-48.
[http://dx.doi.org/10.1002/1878-0261.12371] [PMID: 30107086]
[51]
Cheng L, Zhang K, Qing Y, et al. Proteomic and lipidomic analysis of exosomes derived from ovarian cancer cells and ovarian surface epithelial cells. J Ovarian Res 2020; 13(1): 9.
[http://dx.doi.org/10.1186/s13048-020-0609-y] [PMID: 31969186]
[52]
Zhang W, Ou X, Wu X. Proteomics profiling of plasma exosomes in epithelial ovarian cancer: A potential role in the coagulation cascade, diagnosis and prognosis. Int J Oncol 2019; 54(5): 1719-33.
[http://dx.doi.org/10.3892/ijo.2019.4742] [PMID: 30864689]
[53]
Han FJ, Li J, Shen Y, et al. microRNA-1271-5p/TIAM1 suppresses the progression of ovarian cancer through inactivating Notch signaling pathway. J Ovarian Res 2020; 13(1): 110.
[http://dx.doi.org/10.1186/s13048-020-00720-w] [PMID: 32948241]
[54]
Liu B, Zhang J, Yang D. miR-96-5p promotes the proliferation and migration of ovarian cancer cells by suppressing Caveolae1. J Ovarian Res 2019; 12(1): 57.
[http://dx.doi.org/10.1186/s13048-019-0533-1] [PMID: 31228941]
[55]
Zhang Y, Wei YJ, Zhang YF, Liu HW, Zhang YF. Emerging functions and clinical applications of exosomal ncRNAs in ovarian cancer. Front Oncol 2021; 11: 765458.
[http://dx.doi.org/10.3389/fonc.2021.765458] [PMID: 34804970]
[56]
Shiao MS, Chang JM, Lertkhachonsuk AA, Rermluk N, Jinawath N. Circulating exosomal miRNAs as biomarkers in epithelial ovarian cancer. Biomedicines 2021; 9(10): 1433.
[http://dx.doi.org/10.3390/biomedicines9101433] [PMID: 34680550]
[57]
Taylor DD, 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]
[58]
Wei NA, Liu SS, Leung TH, et al. Loss of programmed cell death 4 (PDCD4) associates with the progression of ovarian cancer. Mol Cancer 2009; 8(1): 70.
[http://dx.doi.org/10.1186/1476-4598-8-70] [PMID: 19728867]
[59]
Cappellesso R, Tinazzi A, Giurici T, et al. 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): 685-93.
[http://dx.doi.org/10.1002/cncy.21442] [PMID: 24888238]
[60]
Choi PW, Ng SW. The functions of MicroRNA-200 family in ovarian cancer: Beyond epithelial-mesenchymal transition. Int J Mol Sci 2017; 18(6): 1207.
[http://dx.doi.org/10.3390/ijms18061207] [PMID: 28587302]
[61]
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): 16923-35.
[http://dx.doi.org/10.18632/oncotarget.7850] [PMID: 26943577]
[62]
Xiong J, He X, Xu Y, Zhang W, Fu F. MiR-200b is upregulated in plasma-derived exosomes and functions as an oncogene by promoting macrophage M2 polarization in ovarian cancer. J Ovarian Res 2021; 14(1): 74.
[http://dx.doi.org/10.1186/s13048-021-00826-9] [PMID: 34078414]
[63]
Kim S, Choi MC, Jeong JY, et al. Serum exosomal miRNA-145 and miRNA-200c as promising biomarkers for preoperative diagnosis of ovarian carcinomas. J Cancer 2019; 10(9): 1958-67.
[http://dx.doi.org/10.7150/jca.30231] [PMID: 31205555]
[64]
Liu J, Yoo J, Ho JY, et al. Plasma-derived exosomal miR-4732-5p is a promising noninvasive diagnostic biomarker for epithelial ovarian cancer. J Ovarian Res 2021; 14(1): 59.
[http://dx.doi.org/10.1186/s13048-021-00814-z] [PMID: 33910598]
[65]
Maeda K, Sasaki H, Ueda S, et al. Serum exosomal microRNA-34a as a potential biomarker in epithelial ovarian cancer. J Ovarian Res 2020; 13(1): 47.
[http://dx.doi.org/10.1186/s13048-020-00648-1] [PMID: 32336272]
[66]
Su YY, Sun L, Guo ZR, et al. 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]
[67]
Kobayashi M, Sawada K, Nakamura K, et al. 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]
[68]
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): 5601-7.
[http://dx.doi.org/10.3892/ol.2019.10220] [PMID: 31186782]
[69]
Li Y, Liu C, Liao Y, et al. Characterizing the landscape of peritoneal exosomal microRNAs in patients with ovarian cancer by high-throughput sequencing. Oncol Lett 2019; 17(1): 539-47. [J].
[PMID: 30655799]
[70]
Welponer H, Tsibulak I, Wieser V, et al. The miR-34 family and its clinical significance in ovarian cancer. J Cancer 2020; 11(6): 1446-56.
[http://dx.doi.org/10.7150/jca.33831] [PMID: 32047551]
[71]
Zhang W, Su X, Li S, Liu Z, Wang Q, Zeng H. Low serum exosomal miR-484 expression predicts unfavorable prognosis in ovarian cancer. Dis Markers 2020; 27(4): 485-91.
[http://dx.doi.org/10.3233/CBM-191123] [PMID: 32065786]
[72]
Hang W, Feng Y, Sang Z, et al. 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): 256-66.
[PMID: 30365097]
[73]
Wong MY, Yu Y, Walsh WR, Yang JL. microRNA-34 family and treatment of cancers with mutant or wild-type p53 (Review). Int J Oncol 2011; 38(5): 1189-95.
[PMID: 21399872]
[74]
Hermeking H. The miR-34 family in cancer and apoptosis. Cell Death Differ 2010; 17(2): 193-9.
[http://dx.doi.org/10.1038/cdd.2009.56] [PMID: 19461653]
[75]
Lu S, Liu W, Shi H, Zhou H. Exosomal miR-34b inhibits proliferation and the epithelial-mesenchymal transition by targeting Notch2 in ovarian cancer. Oncol Lett 2020; 20(3): 2721-8.
[http://dx.doi.org/10.3892/ol.2020.11837] [PMID: 32782588]
[76]
Cao J, Zhang Y, Mu J, Yang D, Gu X, Zhang J. Exosomal miR-21-5p contributes to ovarian cancer progression by regulating CDK6. Hum Cell 2021; 34(4): 1185-96.
[http://dx.doi.org/10.1007/s13577-021-00522-2] [PMID: 33813728]
[77]
He L, Zhu W, Chen Q, et al. Ovarian cancer cell-secreted exosomal miR-205 promotes metastasis by inducing angiogenesis. Theranostics 2019; 9(26): 8206-20.
[http://dx.doi.org/10.7150/thno.37455] [PMID: 31754391]
[78]
Campos A, Sharma S, Obermair A, Salomon C. Extracellular vesicle-associated mirnas and chemoresistance: A systematic review. Cancers (Basel) 2021; 13(18): 4608.
[http://dx.doi.org/10.3390/cancers13184608] [PMID: 34572835]
[79]
Rodríguez-Martínez A, de Miguel-Pérez D, Ortega FG, et al. Exosomal miRNA profile as complementary tool in the diagnostic and prediction of treatment response in localized breast cancer under neoadjuvant chemotherapy. Breast Cancer Res 2019; 21(1): 21.
[http://dx.doi.org/10.1186/s13058-019-1109-0] [PMID: 30728048]
[80]
Stevic I, Müller V, Weber K, et al. Specific microRNA signatures in exosomes of triple-negative and HER2-positive breast cancer patients undergoing neoadjuvant therapy within the GeparSixto trial. BMC Med 2018; 16(1): 179.
[http://dx.doi.org/10.1186/s12916-018-1163-y] [PMID: 30301470]
[81]
de Miguel Pérez D, Rodriguez Martínez A, Ortigosa Palomo A, et al. Extracellular vesicle-miRNAs as liquid biopsy biomarkers for disease identification and prognosis in metastatic colorectal cancer patients. Sci Rep 2020; 10(1): 3974.
[http://dx.doi.org/10.1038/s41598-020-60212-1] [PMID: 32132553]
[82]
Zare N, Haghjooy Javanmard S, Mehrzad V, Eskandari N, Kefayat A. Evaluation of exosomal miR-155, let-7g and let-7i levels as a potential noninvasive biomarker among refractory/relapsed patients, responsive patients and patients receiving R-CHOP. Leuk Lymphoma 2019; 60(8): 1877-89.
[http://dx.doi.org/10.1080/10428194.2018.1563692] [PMID: 30714442]
[83]
Li T, Lin L, Liu Q, et al. Exosomal transfer of miR-429 confers chemoresistance in epithelial ovarian cancer. Am J Cancer Res 2021; 11(5): 2124-41.
[PMID: 34094673]
[84]
Alharbi M, Sharma S, Guanzon D, et al. miRNa signature in small extracellular vesicles and their association with platinum resistance and cancer recurrence in ovarian cancer. Nanomedicine 2020; 28: 102207.
[http://dx.doi.org/10.1016/j.nano.2020.102207] [PMID: 32334098]
[85]
Qiu L, Wang J, Chen M, Chen F, Tu W. Exosomal microRNA-146a derived from mesenchymal stem cells increases the sensitivity of ovarian cancer cells to docetaxel and taxane via a LAMC2-mediated PI3K/Akt axis. Int J Mol Med 2020; 46(2): 609-20.
[http://dx.doi.org/10.3892/ijmm.2020.4634] [PMID: 32626953]
[86]
Guo H, Ha C, Dong H, Yang Z, Ma Y, Ding Y. Cancer-associated fibroblast-derived exosomal microRNA-98-5p promotes cisplatin resistance in ovarian cancer by targeting CDKN1A. Cancer Cell Int 2019; 19(1): 347.
[http://dx.doi.org/10.1186/s12935-019-1051-3] [PMID: 31889899]
[87]
Dochez V, Caillon H, Vaucel E, Dimet J, Winer N, Ducarme G. Biomarkers and algorithms for diagnosis of ovarian cancer: CA125, HE4, RMI and ROMA, a review. J Ovarian Res 2019; 12(1): 28.
[http://dx.doi.org/10.1186/s13048-019-0503-7] [PMID: 30917847]
[88]
Chen Z, Liang Q, Zeng H, et al. Exosomal CA125 as a promising biomarker for ovarian cancer diagnosis. J Cancer 2020; 11(21): 6445-53.
[http://dx.doi.org/10.7150/jca.48531] [PMID: 33033528]
[89]
Szajnik M, Derbis M, Lach M, et al. 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]
[90]
Runz S, Keller S, Rupp C, et al. Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 2007; 107(3): 563-71.
[http://dx.doi.org/10.1016/j.ygyno.2007.08.064] [PMID: 17900673]
[91]
Li J, Sherman-Baust CA, Tsai-Turton M, Bristow RE, Roden RB, Morin PJ. Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer. BMC Cancer 2009; 9(1): 244.
[http://dx.doi.org/10.1186/1471-2407-9-244] [PMID: 19619303]
[92]
Tang MKS, Yue PYK, Ip PP, et al. Soluble E-cadherin promotes tumor angiogenesis and localizes to exosome surface. Nat Commun 2018; 9(1): 2270.
[http://dx.doi.org/10.1038/s41467-018-04695-7] [PMID: 29891938]
[93]
Zhang P, He M, Zeng Y. Ultrasensitive microfluidic analysis of circulating exosomes using a nanostructured graphene oxide/polydopamine coating. Lab Chip 2016; 16(16): 3033-42.
[http://dx.doi.org/10.1039/C6LC00279J] [PMID: 27045543]
[94]
Hisey CL, Dorayappan KDP, Cohn DE, Selvendiran K, Hansford DJ. Microfluidic affinity separation chip for selective capture and release of label-free ovarian cancer exosomes. Lab Chip 2018; 18(20): 3144-53.
[http://dx.doi.org/10.1039/C8LC00834E] [PMID: 30191215]
[95]
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): 489-96.
[http://dx.doi.org/10.1039/C5LC01117E] [PMID: 26645590]
[96]
Dorayappan KDP, Gardner ML, Hisey CL, et al. 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): 3503-13.
[http://dx.doi.org/10.1158/0008-5472.CAN-18-3538] [PMID: 31097475]
[97]
Liang B, Peng P, Chen S, et al. Characterization and proteomic analysis of ovarian cancer-derived exosomes. J Proteomics 2013; 80: 171-82.
[http://dx.doi.org/10.1016/j.jprot.2012.12.029] [PMID: 23333927]
[98]
Malla RR, Pandrangi S, Kumari S, Gavara MM, Badana AK. Exosomal tetraspanins as regulators of cancer progression and metastasis and novel diagnostic markers. Asia Pac J Clin Oncol 2018; 14(6): 383-91.
[http://dx.doi.org/10.1111/ajco.12869] [PMID: 29575602]
[99]
Li X, Tang M, Zhu Q, Wang X, Lin Y, Wang X. The exosomal integrin α5β1/AEP complex derived from epithelial ovarian cancer cells promotes peritoneal metastasis through regulating mesothelial cell proliferation and migration. Cell Oncol 2020; 43(2): 263-77.
[http://dx.doi.org/10.1007/s13402-019-00486-4] [PMID: 32080801]
[100]
Li W, Lu Y, Yu X, Yong M, Ma D, Gao Q. Detection of exosomal tyrosine receptor kinase B as a potential biomarker in ovarian cancer. J Cell Biochem 2019; 120(4): 6361-9.
[http://dx.doi.org/10.1002/jcb.27923] [PMID: 30304550]
[101]
Broner EC, Tropé CG, Reich R, Davidson B. TSAP6 is a novel candidate marker of poor survival in metastatic high-grade serous carcinoma. Hum Pathol 2017; 60: 180-7.
[http://dx.doi.org/10.1016/j.humpath.2016.10.017] [PMID: 27825812]
[102]
Luo Y, Gui R. Circulating exosomal circFoxp1 confers cisplatin resistance in epithelial ovarian cancer cells. J Gynecol Oncol 2020; 31(5): e75.
[http://dx.doi.org/10.3802/jgo.2020.31.e75] [PMID: 32808501]
[103]
Li W, Zhang X, Wang J, et al. TGFβ1 in fibroblasts-derived exosomes promotes epithelial-mesenchymal transition of ovarian cancer cells. Oncotarget 2017; 8(56): 96035-47.
[http://dx.doi.org/10.18632/oncotarget.21635] [PMID: 29221185]
[104]
Shen X, Wang C, Zhu H, et al. Exosome-mediated transfer of CD44 from high-metastatic ovarian cancer cells promotes migration and invasion of low-metastatic ovarian cancer cells. J Ovarian Res 2021; 14(1): 38.
[http://dx.doi.org/10.1186/s13048-021-00776-2] [PMID: 33627162]
[105]
Abedini MR, Qiu Q, Yan X, Tsang BK. Possible role of FLICE-Like Inhibitory Protein (FLIP) in chemoresistant ovarian cancer cells in vitro. Oncogene 2004; 23(42): 6997-7004.
[http://dx.doi.org/10.1038/sj.onc.1207925] [PMID: 15258564]
[106]
Asare-Werehene M, Nakka K, Reunov A, et al. The exosome-mediated autocrine and paracrine actions of plasma gelsolin in ovarian cancer chemoresistance. Oncogene 2020; 39(7): 1600-16.
[http://dx.doi.org/10.1038/s41388-019-1087-9] [PMID: 31700155]
[107]
Asare-Werehene M, Communal L, Carmona E, et al. Plasma gelsolin inhibits cd8+ t-cell function and regulates glutathione production to confer chemoresistance in ovarian cancer. Cancer Res 2020; 80(18): 3959-71.
[http://dx.doi.org/10.1158/0008-5472.CAN-20-0788] [PMID: 32641415]
[108]
Dorayappan KDP, Wanner R, Wallbillich JJ, et al. Hypoxia-induced exosomes contribute to a more aggressive and chemoresistant ovarian cancer phenotype: A novel mechanism linking STAT3/Rab proteins. Oncogene 2018; 37(28): 3806-21.
[http://dx.doi.org/10.1038/s41388-018-0189-0] [PMID: 29636548]
[109]
Cao YL, Zhuang T, Xing BH, Li N, Li Q. Exosomal DNMT1 mediates cisplatin resistance in ovarian cancer. Cell Biochem Funct 2017; 35(6): 296-303.
[http://dx.doi.org/10.1002/cbf.3276] [PMID: 28791708]

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