{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,21]],"date-time":"2025-12-21T10:04:03Z","timestamp":1766311443627,"version":"build-2065373602"},"reference-count":80,"publisher":"MDPI AG","issue":"21","license":[{"start":{"date-parts":[[2021,10,20]],"date-time":"2021-10-20T00:00:00Z","timestamp":1634688000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Portuguese Oncology Institute of Porto","award":["PI 74-CI-IPOP-19-2015 and PI-27-CI-IPOP"],"award-info":[{"award-number":["PI 74-CI-IPOP-19-2015 and PI-27-CI-IPOP"]}]},{"DOI":"10.13039\/100010434","name":"\u201cla Caixa\u201d Foundation","doi-asserted-by":"publisher","award":["LCF\/BQ\/DR20\/11790013."],"award-info":[{"award-number":["LCF\/BQ\/DR20\/11790013."]}],"id":[{"id":"10.13039\/100010434","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cancers"],"abstract":"<jats:p>Renal cell carcinoma is the third most common urological cancer. Despite recent advances, late diagnosis and poor prognosis of advanced-stage disease remain a major problem, entailing the need for novel early diagnosis tools. Liquid biopsies represent a promising minimally invasive clinical tool, providing real-time feedback of tumor behavior and biological potential, addressing its clonal evolution and representing its heterogeneity. In particular, the study of circulating microRNAs and exosomal microRNAs in liquid biopsies experienced an exponential increase in recent years, considering the potential clinical utility and available technology that facilitates implementation. Herein, we provide a systematic review on the applicability of these biomarkers in the context of renal cell carcinoma. Issues such as additional benefit from extracting microRNAs transported in extracellular vesicles, use for subtyping and representation of different histological types, correlation with tumor burden, and prediction of patient outcome are also addressed. Despite the need for more conclusive research, available data indicate that exosomal microRNAs represent a robust minimally invasive biomarker for renal cell carcinoma. Thus, innovative research on microRNAs and novel detection techniques are likely to provide clinically relevant biomarkers, overcome current clinical challenges, and improve patient management.<\/jats:p>","DOI":"10.3390\/cancers13215252","type":"journal-article","created":{"date-parts":[[2021,10,20]],"date-time":"2021-10-20T07:05:57Z","timestamp":1634713557000},"page":"5252","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":12,"title":["Unveiling the World of Circulating and Exosomal microRNAs in Renal Cell Carcinoma"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-4687-3347","authenticated-orcid":false,"given":"Jos\u00e9 Pedro","family":"Sequeira","sequence":"first","affiliation":[{"name":"Cancer Biology & Epigenetics Group, IPO Porto Research Center (GEBC CI-IPOP), Portuguese Oncology Institute of Porto (IPO Porto), Porto Comprehensive Cancer Center (P.CCC), RISE@CI-IPOP (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto), R. Dr. Ant\u00f3nio Bernardino de Almeid, 4200-072 Porto, Portugal"},{"name":"Master Programme in Oncology, School of Medicine & Biomedical Sciences, University of Porto (ICBAS-UP), Rua Jorge Viterbo Ferreira 228, 4050-513 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3151-0367","authenticated-orcid":false,"given":"Vera","family":"Const\u00e2ncio","sequence":"additional","affiliation":[{"name":"Cancer Biology & Epigenetics Group, IPO Porto Research Center (GEBC CI-IPOP), Portuguese Oncology Institute of Porto (IPO Porto), Porto Comprehensive Cancer Center (P.CCC), RISE@CI-IPOP (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto), R. Dr. Ant\u00f3nio Bernardino de Almeid, 4200-072 Porto, Portugal"},{"name":"Doctoral Programme in Biomedical Sciences, School of Medicine & Biomedical Sciences, University of Porto (ICBAS-UP), Rua Jorge Viterbo Ferreira 228, 4050-513 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6829-1391","authenticated-orcid":false,"given":"Jo\u00e3o","family":"Lobo","sequence":"additional","affiliation":[{"name":"Cancer Biology & Epigenetics Group, IPO Porto Research Center (GEBC CI-IPOP), Portuguese Oncology Institute of Porto (IPO Porto), Porto Comprehensive Cancer Center (P.CCC), RISE@CI-IPOP (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto), R. Dr. Ant\u00f3nio Bernardino de Almeid, 4200-072 Porto, Portugal"},{"name":"Department of Pathology, Portuguese Oncology Institute of Porto (IPOP), R. Dr. Ant\u00f3nio Bernardino de Almeida, 4200-072 Porto, Portugal"},{"name":"Department of Pathology and Molecular Immunology, School of Medicine & Biomedical Sciences, University of Porto (ICBAS-UP), Rua Jorge Viterbo Ferreira 228, 4050-513 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3171-4666","authenticated-orcid":false,"given":"Rui","family":"Henrique","sequence":"additional","affiliation":[{"name":"Cancer Biology & Epigenetics Group, IPO Porto Research Center (GEBC CI-IPOP), Portuguese Oncology Institute of Porto (IPO Porto), Porto Comprehensive Cancer Center (P.CCC), RISE@CI-IPOP (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto), R. Dr. Ant\u00f3nio Bernardino de Almeid, 4200-072 Porto, Portugal"},{"name":"Department of Pathology, Portuguese Oncology Institute of Porto (IPOP), R. Dr. Ant\u00f3nio Bernardino de Almeida, 4200-072 Porto, Portugal"},{"name":"Department of Pathology and Molecular Immunology, School of Medicine & Biomedical Sciences, University of Porto (ICBAS-UP), Rua Jorge Viterbo Ferreira 228, 4050-513 Porto, Portugal"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4186-5345","authenticated-orcid":false,"given":"Carmen","family":"Jer\u00f3nimo","sequence":"additional","affiliation":[{"name":"Cancer Biology & Epigenetics Group, IPO Porto Research Center (GEBC CI-IPOP), Portuguese Oncology Institute of Porto (IPO Porto), Porto Comprehensive Cancer Center (P.CCC), RISE@CI-IPOP (Health Research Network), Portuguese Oncology Institute of Porto (IPO Porto), R. Dr. Ant\u00f3nio Bernardino de Almeid, 4200-072 Porto, Portugal"},{"name":"Department of Pathology and Molecular Immunology, School of Medicine & Biomedical Sciences, University of Porto (ICBAS-UP), Rua Jorge Viterbo Ferreira 228, 4050-513 Porto, Portugal"}]}],"member":"1968","published-online":{"date-parts":[[2021,10,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1590\/s1677-5538.ibju.2020.0149","article-title":"A comparison of oncologic and functional outcomes in patients with pt3a renal cell carcinoma treated with partial and radical nephrectomy","volume":"47","author":"Alvim","year":"2021","journal-title":"Int. Braz. J. Urol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1590\/s1677-5538.ibju.2020.0167","article-title":"Partial nephrectomy provides equivalent oncologic outcomes and better renal function preservation than radical nephrectomy for pathological T3a renal cell carcinoma: A meta-analysis","volume":"47","author":"Deng","year":"2021","journal-title":"Int. Braz. J. Urol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"894","DOI":"10.1016\/S0140-6736(15)00046-X","article-title":"Renal cancer","volume":"387","author":"Capitanio","year":"2016","journal-title":"Lancet"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.semnephrol.2019.12.004","article-title":"The Therapeutic Landscape of Renal Cell Carcinoma: From the Dark Age to the Golden Age","volume":"40","author":"Huang","year":"2020","journal-title":"Semin. Nephrol"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1016\/j.euf.2018.02.010","article-title":"Long-term Outcomes of Follow-up for Initially Localised Clear Cell Renal Cell Carcinoma: RECUR Database Analysis","volume":"5","author":"Dabestani","year":"2019","journal-title":"Eur. Urol. Focus"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Dias, F., Teixeira, A.L., Nogueira, I., Morais, M., Maia, J., Bodo, C., Ferreira, M., Silva, A., Vilhena, M., and Lobo, J. (2020). Extracellular Vesicles Enriched in hsa-miR-301a-3p and hsa-miR-1293 Dynamics in Clear Cell Renal Cell Carcinoma Patients: Potential Biomarkers of Metastatic Disease. Cancers, 12.","DOI":"10.3390\/cancers12061450"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1002\/cpph.19","article-title":"Biomarkers\u2014A General Review","volume":"76","author":"Aronson","year":"2017","journal-title":"Curr. Protoc. Pharmacol."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Const\u00e2ncio, V., Nunes, S.P., Henrique, R., and Jer\u00f3nimo, C. (2020). DNA Methylation-Based Testing in Liquid Biopsies as Detection and Prognostic Biomarkers for the Four Major Cancer Types. Cells, 9.","DOI":"10.3390\/cells9030624"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1016\/j.lungcan.2017.12.012","article-title":"Exosomes as a liquid biopsy for lung cancer","volume":"116","author":"Cui","year":"2018","journal-title":"Lung Cancer"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1159\/000478018","article-title":"Liquid Biopsy: Current Status and Future Perspectives","volume":"40","author":"Mader","year":"2017","journal-title":"Oncol. Res. Treat."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"S9","DOI":"10.1038\/d41586-020-00844-5","article-title":"The future of liquid biopsy","volume":"579","year":"2020","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1002\/gcc.22695","article-title":"Liquid biopsies","volume":"58","author":"Lianidou","year":"2019","journal-title":"Genes Chromosomes Cancer"},{"key":"ref_13","first-page":"11","article-title":"Cancer diagnosis: From tumor to liquid biopsy and beyond","volume":"19","author":"Vaidyanathan","year":"2018","journal-title":"Lab. Chip."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1373\/clinchem.2014.222679","article-title":"Circulating tumor DNA as a liquid biopsy for cancer","volume":"61","author":"Heitzer","year":"2015","journal-title":"Clin. Chem."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"22","DOI":"10.1016\/j.euo.2020.12.011","article-title":"Novel Liquid Biomarkers and Innovative Imaging for Kidney Cancer Diagnosis: What Can Be Implemented in Our Practice Today? A Systematic Review of the Literature","volume":"4","author":"Campi","year":"2021","journal-title":"Eur. Urol. Oncol."},{"key":"ref_16","first-page":"2092","article-title":"A miRNA-based classification of renal cell carcinoma subtypes by PCR and in situ hybridization","volume":"9","author":"Saleeb","year":"2017","journal-title":"Oncotarget"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"209","DOI":"10.3322\/caac.21660","article-title":"Global Cancer Statistics 2020: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries","volume":"71","author":"Sung","year":"2021","journal-title":"CA Cancer J. Clin."},{"key":"ref_18","unstructured":"Pandey, J., and Syed, W. (2021). Renal Cancer. StatPearls, StatPearls Publishing LLC."},{"key":"ref_19","unstructured":"Arora, R.D., and Limaiem, F. (2021). Renal Clear Cell Cancer. StatPearls, StatPearls Publishing LLC."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.celrep.2018.03.075","article-title":"The Cancer Genome Atlas Comprehensive Molecular Characterization of Renal Cell Carcinoma","volume":"23","author":"Ricketts","year":"2018","journal-title":"Cell Rep."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1016\/j.eururo.2014.04.029","article-title":"Understanding pathologic variants of renal cell carcinoma: Distilling therapeutic opportunities from biologic complexity","volume":"67","author":"Shuch","year":"2015","journal-title":"Eur. Urol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.eururo.2018.08.036","article-title":"Epidemiology of Renal Cell Carcinoma","volume":"75","author":"Capitanio","year":"2019","journal-title":"Eur. Urol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1007\/s12032-020-1346-1","article-title":"Extracellular vesicle isolation from human renal cancer tissue","volume":"37","author":"Zieren","year":"2020","journal-title":"Med. Oncol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1016\/j.eururo.2019.02.011","article-title":"European Association of Urology Guidelines on Renal Cell Carcinoma: The 2019 Update","volume":"75","author":"Ljungberg","year":"2019","journal-title":"Eur. Urol."},{"key":"ref_25","doi-asserted-by":"crossref","unstructured":"Drula, R., Ott, L.F., Berindan-Neagoe, I., Pantel, K., and Calin, G.A. (2020). MicroRNAs from Liquid Biopsy Derived Extracellular Vesicles: Recent Advances in Detection and Characterization Methods. Cancers, 12.","DOI":"10.3390\/cancers12082009"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"2302","DOI":"10.3389\/fonc.2020.582843","article-title":"Liquid Biopsies in Renal Cell Carcinoma\u2014Recent Advances and Promising New Technologies for the Early Detection of Metastatic Disease","volume":"10","author":"Lakshminarayanan","year":"2020","journal-title":"Front. Oncol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1186\/s13073-020-00723-8","article-title":"Comprehensive characterization of cell-free tumor DNA in plasma and urine of patients with renal tumors","volume":"12","author":"Smith","year":"2020","journal-title":"Genome Med."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1016\/j.urology.2011.02.039","article-title":"Urinary collecting system invasion is a predictor for overall and disease-specific survival in locally invasive renal cell carcinoma","volume":"78","author":"Anderson","year":"2011","journal-title":"Urology"},{"key":"ref_29","unstructured":"Ballard, B.D., and Guzman, N. (2021). Renal Mass. StatPearls, StatPearls Publishing LLC."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1081","DOI":"10.1007\/s00345-016-1773-y","article-title":"Renal cell carcinoma recurrences and metastases in primary non-metastatic patients: A population-based study","volume":"34","author":"Dabestani","year":"2016","journal-title":"World J. Urol."},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Dias, F., Teixeira, A.L., Nogueira, I., Morais, M., Maia, J., Bodo, C., Ferreira, M., Vieira, I., Silva, J., and Lobo, J. (2020). Plasma Extracellular Vesicle-Derived TIMP-1 mRNA as a Prognostic Biomarker in Clear Cell Renal Cell Carcinoma: A Pilot Study. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21134624"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"715","DOI":"10.1515\/cclm-2015-1073","article-title":"miRNAs as novel biomarkers in the management of prostate cancer","volume":"55","author":"Filella","year":"2017","journal-title":"Clin. Chem. Lab. Med."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"834","DOI":"10.1038\/nature03702","article-title":"MicroRNA expression profiles classify human cancers","volume":"435","author":"Lu","year":"2005","journal-title":"Nature"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/j.biocel.2008.09.005","article-title":"DNA methylomes, histone codes and miRNAs: Tying it all together","volume":"41","author":"Guil","year":"2009","journal-title":"Int. J. Biochem. Cell Biol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Outeiro-Pinho, G., Barros-Silva, D., Correia, M.P., Henrique, R., and Jer\u00f3nimo, C. (2020). Renal Cell Tumors: Uncovering the Biomarker Potential of ncRNAs. Cancers, 12.","DOI":"10.3390\/cancers12082214"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Campomenosi, P., Gini, E., Noonan, D.M., Poli, A., D\u2019Antona, P., Rotolo, N., Dominioni, L., and Imperatori, A. (2016). A comparison between quantitative PCR and droplet digital PCR technologies for circulating microRNA quantification in human lung cancer. BMC Biotechnol., 16.","DOI":"10.1186\/s12896-016-0292-7"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"483","DOI":"10.1016\/j.euo.2020.11.004","article-title":"Utility of Serum miR-371a-3p in Predicting Relapse on Surveillance in Patients with Clinical Stage I Testicular Germ Cell Cancer","volume":"4","author":"Lobo","year":"2020","journal-title":"Eur. Urol. Oncol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Cirillo, P.D.R., Margiotti, K., Mesoraca, A., and Giorlandino, C. (2020). Quantification of circulating microRNAs by droplet digital PCR for cancer detection. BMC Res. Notes, 13.","DOI":"10.1186\/s13104-020-05190-3"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"445","DOI":"10.1007\/978-1-4939-7778-9_25","article-title":"Quantification of Circulating MicroRNAs by Droplet Digital PCR","volume":"1768","author":"Ferracin","year":"2018","journal-title":"Methods Mol. Biol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"900","DOI":"10.3389\/fonc.2019.00900","article-title":"Circulating MicroRNAs as Biomarkers for Prostate Cancer Detection and Metastasis Development Prediction","volume":"9","author":"Bidarra","year":"2019","journal-title":"Front. Oncol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1186\/s12967-016-1025-3","article-title":"Decoding the usefulness of non-coding RNAs as breast cancer markers","volume":"14","author":"Amorim","year":"2016","journal-title":"J. Transl. Med."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1186\/s12943-017-0604-0","article-title":"MiR-193b promoter methylation accurately detects prostate cancer in urine sediments and miR-34b\/c or miR-129-2 promoter methylation define subsets of clinically aggressive tumors","volume":"16","author":"Gomez","year":"2017","journal-title":"Mol. Cancer"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"79","DOI":"10.3233\/CBM-160676","article-title":"Functional analysis of serum microRNAs miR-21 and miR-106a in renal cell carcinoma","volume":"18","author":"Tusong","year":"2017","journal-title":"Cancer Biomark."},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Wulfken, L.M., Moritz, R., Ohlmann, C., Holdenrieder, S., Jung, V., Becker, F., Herrmann, E., Walgenbach-Br\u00fcnagel, G., von Ruecker, A., and M\u00fcller, S.C. (2011). MicroRNAs in Renal Cell Carcinoma: Diagnostic Implications of Serum miR-1233 Levels. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0025787"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1016\/j.urology.2017.03.013","article-title":"Serum microRNA Expression Profiling: Potential Diagnostic Implications of a Panel of Serum microRNAs for Clear Cell Renal Cell Cancer","volume":"104","author":"Yadav","year":"2017","journal-title":"Urology"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"23382","DOI":"10.3390\/ijms161023382","article-title":"Combination of MiR-378 and MiR-210 Serum Levels Enables Sensitive Detection of Renal Cell Carcinoma","volume":"16","author":"Fedorko","year":"2015","journal-title":"Int. J. Mol. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"53","DOI":"10.3892\/ijo.2013.2169","article-title":"Serum miR-210 as a potential biomarker of early clear cell renal cell carcinoma","volume":"44","author":"Iwamoto","year":"2014","journal-title":"Int. J. Oncol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/j.yexmp.2012.10.005","article-title":"Serum miR-210 as a novel biomarker for molecular diagnosis of clear cell renal cell carcinoma","volume":"94","author":"Zhao","year":"2013","journal-title":"Exp. Mol. Pathol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"569","DOI":"10.7754\/Clin.Lab.2017.171103","article-title":"Detection Performance of Circulating MicroRNA-210 for Renal Cell Carcinoma: A Meta-Analysis","volume":"64","author":"Chen","year":"2018","journal-title":"Clin. Lab."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"851","DOI":"10.1007\/s11255-018-1841-x","article-title":"MicroRNA-15a expression measured in urine samples as a potential biomarker of renal cell carcinoma","volume":"50","author":"Mytsyk","year":"2018","journal-title":"Int. Urol. Nephrol"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"623","DOI":"10.2217\/bmm.13.44","article-title":"Stability of miRNA in human urine supports its biomarker potential","volume":"7","author":"Mall","year":"2013","journal-title":"Biomark Med."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"55","DOI":"10.1186\/1479-5876-10-55","article-title":"Circulating miR-378 and miR-451 in serum are potential biomarkers for renal cell carcinoma","volume":"10","author":"Redova","year":"2012","journal-title":"J. Transl. Med."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1492","DOI":"10.1002\/jcb.27347","article-title":"Serum exosomal miR-210 as a potential biomarker for clear cell renal cell carcinoma","volume":"120","author":"Wang","year":"2018","journal-title":"J. Cell Biochem."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1186\/s13148-018-0444-9","article-title":"Serum miR-122-5p and miR-206 expression: Non-invasive prognostic biomarkers for renal cell carcinoma","volume":"10","author":"Heinemann","year":"2018","journal-title":"Clin. Epigenetics"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1787","DOI":"10.1016\/j.ajpath.2012.01.014","article-title":"MicroRNA 15a, inversely correlated to PKC\u03b1, is a potential marker to differentiate between benign and malignant renal tumors in biopsy and urine samples","volume":"180","author":"Pandarakalam","year":"2012","journal-title":"Am. J. Pathol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"7610","DOI":"10.1038\/srep07610","article-title":"A panel of five serum miRNAs as a potential diagnostic tool for early-stage renal cell carcinoma","volume":"5","author":"Wang","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/j.bbrc.2012.02.060","article-title":"Identification of miR-508-3p and miR-509-3p that are associated with cell invasion and migration and involved in the apoptosis of renal cell carcinoma","volume":"419","author":"Zhai","year":"2012","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"4057","DOI":"10.1007\/s13277-013-1531-3","article-title":"Higher circulating expression levels of miR-221 associated with poor overall survival in renal cell carcinoma patients","volume":"35","author":"Teixeira","year":"2014","journal-title":"Tumour Biol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"9245","DOI":"10.1007\/s13277-015-3604-y","article-title":"High serum miR-183 level is associated with poor responsiveness of renal cancer to natural killer cells","volume":"36","author":"Zhang","year":"2015","journal-title":"Tumour Biol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"411","DOI":"10.11613\/BM.2017.043","article-title":"Detection of let-7 miRNAs in urine supernatant as potential diagnostic approach in non-metastatic clear-cell renal cell carcinoma","volume":"27","author":"Fedorko","year":"2017","journal-title":"Biochem. Med."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1730","DOI":"10.1002\/ijc.30845","article-title":"Large-scale genome-wide screening of circulating microRNAs in clear cell renal cell carcinoma reveals specific signatures in late-stage disease","volume":"141","author":"Chanudet","year":"2017","journal-title":"Int. J. Cancer"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1007\/s00441-017-2621-0","article-title":"Urinary extracellular vesicles. A promising shortcut to novel biomarker discoveries","volume":"369","author":"Barreiro","year":"2017","journal-title":"Cell Tissue Res."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Jella, K.K., Nasti, T.H., Li, Z., Malla, S.R., Buchwald, Z.S., and Khan, M.K. (2018). Exosomes, Their Biogenesis and Role in Inter-Cellular Communication, Tumor Microenvironment and Cancer Immunotherapy. Vaccines, 6.","DOI":"10.3390\/vaccines6040069"},{"key":"ref_64","doi-asserted-by":"crossref","unstructured":"Louren\u00e7o, C., Const\u00e2ncio, V., Henrique, R., Carvalho, \u00c2., and Jer\u00f3nimo, C. (2021). Urinary Extracellular Vesicles as Potential Biomarkers for Urologic Cancers: An Overview of Current Methods and Advances. Cancers, 13.","DOI":"10.3390\/cancers13071529"},{"key":"ref_65","unstructured":"Edelstein, L., Smythies, J., Quesenberry, P., and Noble, D. (2020). Chapter 2\u2014Methods for exosome isolation and characterization. Exosomes, Academic Press."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"210","DOI":"10.1016\/j.euf.2015.11.006","article-title":"Exosomal MicroRNAs Are Diagnostic Biomarkers and Can Mediate Cell-Cell Communication in Renal Cell Carcinoma","volume":"2","author":"Butz","year":"2016","journal-title":"Eur. Urol. Focus"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1960","DOI":"10.7150\/jca.16123","article-title":"The Three-Gene Signature in Urinary Extracellular Vesicles from Patients with Clear Cell Renal Cell Carcinoma","volume":"7","author":"Sallustio","year":"2016","journal-title":"J. Cancer"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1002\/elps.201100375","article-title":"A hyphenated microLC-Q-TOF-MS platform for exosomal lipidomics investigations: Application to RCC urinary exosomes","volume":"33","author":"Raimondo","year":"2012","journal-title":"Electrophoresis"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"1220","DOI":"10.1039\/c3mb25582d","article-title":"Differential protein profiling of renal cell carcinoma urinary exosomes","volume":"9","author":"Raimondo","year":"2013","journal-title":"Mol. Biosyst."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"6755","DOI":"10.1111\/jcmm.14553","article-title":"Urinary exosome miR-30c-5p as a biomarker of clear cell renal cell carcinoma that inhibits progression by targeting HSPA5","volume":"23","author":"Song","year":"2019","journal-title":"J. Cell Mol. Med."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1016\/j.euf.2016.09.007","article-title":"MicroRNAs in Serum Exosomes as Potential Biomarkers in Clear-cell Renal Cell Carcinoma","volume":"4","author":"Zhang","year":"2018","journal-title":"Eur. Urol. Focus"},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"63703","DOI":"10.18632\/oncotarget.19476","article-title":"Plasma exosomal miRNAs-based prognosis in metastatic kidney cancer","volume":"8","author":"Du","year":"2017","journal-title":"Oncotarget"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1016\/j.ccell.2016.03.004","article-title":"Exosome-Transmitted lncARSR Promotes Sunitinib Resistance in Renal Cancer by Acting as a Competing Endogenous RNA","volume":"29","author":"Qu","year":"2016","journal-title":"Cancer Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"109877","DOI":"10.18632\/oncotarget.22436","article-title":"Extracellular miR-224 as a prognostic marker for clear cell renal cell carcinoma","volume":"8","author":"Fujii","year":"2017","journal-title":"Oncotarget"},{"key":"ref_75","first-page":"6513","article-title":"Non-Exosomal and Exosomal Circulatory MicroRNAs: Which Are More Valid as Biomarkers?","volume":"10","author":"Shahidan","year":"2020","journal-title":"Front. Pharmacol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1304816","DOI":"10.1155\/2017\/1304816","article-title":"No Significant Difference between Plasma miRNAs and Plasma-Derived Exosomal miRNAs from Healthy People","volume":"2017","author":"Tian","year":"2017","journal-title":"BioMed Res. Int."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"121","DOI":"10.4149\/neo_2016_015","article-title":"Supernatant versus exosomal urinary microRNAs. Two fractions with different outcomes in gynaecological cancers","volume":"63","author":"Zavesky","year":"2016","journal-title":"Neoplasma"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"6513","DOI":"10.18632\/oncotarget.14311","article-title":"A six-microRNA panel in plasma was identified as a potential biomarker for lung adenocarcinoma diagnosis","volume":"8","author":"Zhou","year":"2017","journal-title":"Oncotarget"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"188","DOI":"10.1158\/1055-9965.EPI-16-0607","article-title":"Six Serum-Based miRNAs as Potential Diagnostic Biomarkers for Gastric Cancer","volume":"26","author":"Huang","year":"2017","journal-title":"Cancer Epidemiol. Biomark. Prev."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"9650","DOI":"10.18632\/oncotarget.2520","article-title":"Increased serum levels of circulating exosomal microRNA-373 in receptor-negative breast cancer patients","volume":"5","author":"Eichelser","year":"2014","journal-title":"Oncotarget"}],"container-title":["Cancers"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2072-6694\/13\/21\/5252\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T07:18:50Z","timestamp":1760167130000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2072-6694\/13\/21\/5252"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,10,20]]},"references-count":80,"journal-issue":{"issue":"21","published-online":{"date-parts":[[2021,11]]}},"alternative-id":["cancers13215252"],"URL":"https:\/\/doi.org\/10.3390\/cancers13215252","relation":{},"ISSN":["2072-6694"],"issn-type":[{"type":"electronic","value":"2072-6694"}],"subject":[],"published":{"date-parts":[[2021,10,20]]}}}