Liquid Biopsy in Diagnosis and Prognosis of Non-Metastatic Prostate Cancer
Abstract
:1. Introduction
2. Search Strategy
3. Cell-Free DNA (cfDNA)
4. Exosomal miRNAs
5. Circulating Tumor Cells (CTCs)
6. Discussion
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Mettlin, C.; Littrup, P.J.; Kane, R.A.; Murphy, G.P.; Lee, F.; Chesley, A.; Badalament, R.; Mostofi, F.K. Relative sensitivity and specificity of serum prostate specific antigen (PSA) level compared with age-referenced PSA, PSA density, and PSA change. Cancer 1994, 74, 1615–1620. [Google Scholar] [CrossRef] [PubMed]
- Charrier, J.P.; Tournel, C.; Michel, S.; Comby, S.; Jolivet-Reynaud, C.; Passagot, J.; Dalbon, P.; Chautard, D.; Jolivet, M. Differential diagnosis of prostate cancer and benign prostate hyperplasia using two-dimensional electrophoresis. Electrophoresis 2001, 22, 1861–1866. [Google Scholar] [CrossRef] [PubMed]
- Loeb, S.; Gashti, S.N.; Catalona, W.J. Exclusion of inflammation in the differential diagnosis of an elevated prostate-specific antigen (PSA). Urol. Oncol. Semin. Orig. Investig. 2009, 27, 64–66. [Google Scholar] [CrossRef] [PubMed]
- Weiner, A.; Matulewicz, R.; Eggener, S.E.; Schaeffer, E.M. Increasing incidence of metastatic prostate cancer in the United States (2004–2013). Prostate Cancer Prostatic Dis. 2016, 19, 395–397. [Google Scholar] [CrossRef] [Green Version]
- Carter, H.B.; Albertsen, P.C.; Barry, M.J.; Etzioni, R.; Freedland, S.J.; Greene, K.L.; Holmberg, L.; Kantoff, P.; Konety, B.R.; Murad, M.H.; et al. Early Detection of Prostate Cancer: AUA Guideline. J. Urol. 2013, 190, 419–426. [Google Scholar] [CrossRef] [Green Version]
- Hussein, S.; Satturwar, S.; Van der Kwast, T. Young-age prostate cancer. J. Clin. Pathol. 2015, 68, 511–515. [Google Scholar] [CrossRef] [Green Version]
- Serefoglu, E.C.; Altinova, S.; Ugras, N.S.; Akincioglu, E.; Asil, E.; Balbay, D. How reliable is 12-core prostate biopsy procedure in the detection of prostate cancer? Can. Urol. Assoc. J. 2013, 7, e293-8. [Google Scholar] [CrossRef] [Green Version]
- Humphrey, P.A. Diagnosis of adenocarcinoma in prostate needle biopsy tissue. J. Clin. Pathol. 2007, 60, 35–42. [Google Scholar] [CrossRef]
- Fütterer, J.J.; Barentsz, J.O. MRI-guided and robotic-assisted prostate biopsy. Curr. Opin. Urol. 2012, 22, 316–319. [Google Scholar] [CrossRef]
- Galper, S.L.; Chen, M.-H.; Catalona, W.J.; Roehl, K.A.; Richie, J.P.; D’Amico, A.V. Evidence to Support a Continued Stage Migration and Decrease in Prostate Cancer Specific Mortality. J. Urol. 2006, 175, 907–912. [Google Scholar] [CrossRef]
- Fujita, K.; Landis, P.; McNeil, B.K.; Pavlovich, C.P. Serial Prostate Biopsies are Associated with an Increased Risk of Erectile Dysfunction in Men with Prostate Cancer on Active Surveillance. J. Urol. 2009, 182, 2664–2669. [Google Scholar] [CrossRef]
- Bill-Axelson, A.; Holmberg, L.; Garmo, H.; Rider, J.R.; Taari, K.; Busch, C.; Nordling, S.; Häggman, M.; Andersson, S.-O.; Spångberg, A.; et al. Radical Prostatectomy or Watchful Waiting in Early Prostate Cancer. N. Engl. J. Med. 2014, 370, 932–942. [Google Scholar] [CrossRef] [Green Version]
- Baca, S.C.; Prandi, D.; Lawrence, M.S.; Mosquera, J.M.; Romanel, A.; Drier, Y.; Park, K.; Kitabayashi, N.; MacDonald, T.Y.; Ghandi, M.; et al. Punctuated Evolution of Prostate Cancer Genomes. Cell 2013, 153, 666–677. [Google Scholar] [CrossRef] [Green Version]
- Joosse, S.A.; Gorges, T.M.; Pantel, K. Biology, detection, and clinical implications of circulating tumor cells. EMBO Mol. Med. 2014, 7, 1–11. [Google Scholar] [CrossRef]
- Joosse, S.A.; Pantel, K. Tumor-Educated Platelets as Liquid Biopsy in Cancer Patients. Cancer Cell 2015, 28, 552–554. [Google Scholar] [CrossRef] [Green Version]
- Ashworth, T.R. A case of cancer in which cells similar to those in the tumours were seen in the blood after death. Aust Med J. 1869, 14, 146. [Google Scholar]
- Mader, S.; Pantel, K. Liquid Biopsy: Current Status and Future Perspectives. Oncol. Res. Treat. 2017, 40, 404–408. [Google Scholar] [CrossRef]
- Allard, W.J.; Matera, J.; Miller, M.C.; Repollet, M.; Connelly, M.C.; Rao, C.; Tibbe, A.G.J.; Uhr, J.W.; Terstappen, L.W.M.M. Tumor cells circulate in the peripheral blood of all major carcinomas but not in healthy subjects or patients with nonmalignant diseases. Clin. Cancer Res. 2004, 10, 6897–6904. [Google Scholar] [CrossRef] [Green Version]
- Krebs, M.G.; Metcalf, R.L.; Carter, L.; Brady, G.; Blackhall, F.H.; Dive, C. Molecular analysis of circulating tumour cells—Biology and biomarkers. Nat. Rev. Clin. Oncol. 2014, 11, 129–144. [Google Scholar] [CrossRef]
- Tong, Y.-K.; Lo, Y.D. Diagnostic developments involving cell-free (circulating) nucleic acids. Clin. Chim. Acta 2006, 363, 187–196. [Google Scholar] [CrossRef]
- Elazezy, M.; Joosse, S.A. Techniques of using circulating tumor DNA as a liquid biopsy component in cancer management. Comput. Struct. Biotechnol. J. 2018, 16, 370–378. [Google Scholar] [CrossRef]
- Zhou, B.; Xu, K.; Zheng, X.; Chen, T.; Wang, J.; Song, Y.; Shao, Y.; Zheng, S. Application of exosomes as liquid biopsy in clinical diagnosis. Signal Transduct. Target. Ther. 2020, 5, 144. [Google Scholar] [CrossRef]
- Neuhaus, J.; Yang, B. Liquid Biopsy Potential Biomarkers in Prostate Cancer. Diagnostics 2018, 8, 68. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Romanini, A.; Pisani, G. Cytotopochemistry of leukopenia caused by roentgen irradiation. I. Quantitative variations of desoxyribonucleic acid of the polynuclears of circulating blood. Boll. Soc. Ital. Biol. Sper. 1954, 30, 880–882. [Google Scholar] [PubMed]
- Sozzi, G.; Conte, D.; Leon, M.; Cirincione, R.; Roz, L.; Ratcliffe, C.; Roz, E.; Cirenei, N.; Bellomi, M.; Pelosi, G.; et al. Quantification of Free Circulating DNA As a Diagnostic Marker in Lung Cancer. J. Clin. Oncol. 2003, 21, 3902–3908. [Google Scholar] [CrossRef] [PubMed]
- Schwarzenbach, H.; Müller, V.; Stahmann, N.; Pantel, K. Detection and Characterization of Circulating Microsatellite-DNA in Blood of Patients with Breast Cancer. Ann. N. Y. Acad. Sci. 2004, 1022, 25–32. [Google Scholar] [CrossRef]
- Joosse, S.A.; Pantel, K. Circulating DNA and Liquid Biopsies in the Management of Patients with Cancer. Cancer Res. 2022, 82, 2213–2215. [Google Scholar] [CrossRef]
- Pisetsky, D.S. The origin and properties of extracellular DNA: From PAMP to DAMP. Clin. Immunol. 2012, 144, 32–40. [Google Scholar] [CrossRef] [Green Version]
- Campos-Carrillo, A.; Weitzel, J.N.; Sahoo, P.; Rockne, R.; Mokhnatkin, J.V.; Murtaza, M.; Gray, S.W.; Goetz, L.; Goel, A.; Schork, N.; et al. Circulating tumor DNA as an early cancer detection tool. Pharmacol. Ther. 2020, 207, 107458. [Google Scholar] [CrossRef]
- Joosse, S.A.; Pantel, K. Detection of Hypomethylation in Long-ctDNA. Clin. Chem. 2022, 68, 1115–1117. [Google Scholar] [CrossRef]
- Otandault, A.; Anker, P.; Al Amir Dache, Z.; Guillaumon, V.; Meddeb, R.; Pastor, B.; Pisareva, E.; Sanchez, C.; Tanos, R.; Tousch, G.; et al. Recent advances in circulating nucleic acids in oncology. Ann. Oncol. 2019, 30, 374–384. [Google Scholar] [CrossRef]
- Vandekerkhove, G.; Struss, W.J.; Annala, M.; Kallio, H.M.; Khalaf, D.; Warner, E.W.; Herberts, C.; Ritch, E.; Beja, K.; Loktionova, Y.; et al. Circulating Tumor DNA Abundance and Potential Utility in De Novo Metastatic Prostate Cancer. Eur. Urol. 2019, 75, 667–675. [Google Scholar] [CrossRef] [Green Version]
- Hennigan, S.T.; Trostel, S.Y.; Terrigino, N.T.; Voznesensky, O.S.; Schaefer, R.J.; Whitlock, N.C.; Wilkinson, S.; Carrabba, N.V.; Atway, R.; Shema, S.; et al. Low Abundance of Circulating Tumor DNA in Localized Prostate Cancer. JCO Precis. Oncol. 2019, 3, 1–13. [Google Scholar] [CrossRef]
- Gorgannezhad, L.; Umer, M.; Islam, M.N.; Nguyen, N.-T.; Shiddiky, M.J.A. Circulating tumor DNA and liquid biopsy: Opportunities, challenges, and recent advances in detection technologies. Lab Chip 2018, 18, 1174–1196. [Google Scholar] [CrossRef]
- Siravegna, G.; Marsoni, S.; Siena, S.; Bardelli, A. Integrating liquid biopsies into the management of cancer. Nat. Rev. Clin. Oncol. 2017, 14, 531–548. [Google Scholar] [CrossRef]
- Di Meo, A.; Bartlett, J.; Cheng, Y.; Pasic, M.D.; Yousef, G.M. Liquid biopsy: A step forward towards precision medicine in urologic malignancies. Mol. Cancer 2017, 16, 80. [Google Scholar] [CrossRef]
- Hendriks, R.J.; van Oort, I.M.; Schalken, J.A. Blood-based and urinary prostate cancer biomarkers: A review and comparison of novel biomarkers for detection and treatment decisions. Prostate Cancer Prostatic Dis. 2017, 20, 12–19. [Google Scholar] [CrossRef]
- Lin, S.Y.; Linehan, J.A.; Wilson, T.G.; Hoon, D.S. Emerging Utility of Urinary Cell-free Nucleic Acid Biomarkers for Prostate, Bladder, and Renal Cancers. Eur. Urol. Focus 2017, 3, 265–272. [Google Scholar] [CrossRef]
- Ponti, G.; Maccaferri, M.; Mandrioli, M.; Manfredini, M.; Micali, S.; Cotugno, M.; Bianchi, G.; Ozben, T.; Pellacani, G.; Del Prete, C.; et al. Seminal Cell-Free DNA Assessment as a Novel Prostate Cancer Biomarker. Pathol. Oncol. Res. 2018, 24, 941–945. [Google Scholar] [CrossRef]
- Wang, G.; Zhao, D.; Spring, D.J.; Depinho, R.A. Genetics and biology of prostate cancer. Genes Dev. 2018, 32, 1105–1140. [Google Scholar] [CrossRef] [Green Version]
- Mickey, D.D.; Stone, K.R.; Stone, M.P.; Paulson, D.F. Morphologic and immunologic studies of human prostatic carcinoma. Cancer Treat. Rep. 1977, 61, 133–138. [Google Scholar] [PubMed]
- Gerstung, M.; Jolly, C.; Leshchiner, I.; Dentro, S.C.; Gonzalez, S.; Rosebrock, D.; Mitchell, T.J.; Rubanova, Y.; Anur, P.; Yu, K.; et al. The evolutionary history of 2658 cancers. Nature 2020, 578, 122–128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, P.; Xia, J.; Zhu, J.; Gao, P.; Tian, Y.-J.; Du, M.; Guo, Y.-C.; Suleman, S.; Zhang, Q.; Kohli, M.; et al. High-throughput screening of prostate cancer risk loci by single nucleotide polymorphisms sequencing. Nat. Commun. 2018, 9, 2022. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Haffner, M.C.; Mosbruger, T.; Esopi, D.M.; Fedor, H.; Heaphy, C.M.; Walker, D.A.; Adejola, N.; Gürel, M.; Hicks, J.; Meeker, A.K.; et al. Tracking the clonal origin of lethal prostate cancer. J. Clin. Investig. 2013, 123, 4918–4922. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, E.; Cario, C.L.; Leong, L.; Lopez, K.; Márquez, C.P.; Li, P.S.; Oropeza, E.; Tenggara, I.; Cowan, J.; Simko, J.P.; et al. Cell-Free DNA Detection of Tumor Mutations in Heterogeneous, Localized Prostate Cancer Via Targeted, Multiregion Sequencing. JCO Precis. Oncol. 2021, 5, 710–725. [Google Scholar] [CrossRef]
- Kulis, M.; Esteller, M. DNA methylation and cancer. Adv. Genet. 2010, 70, 27–56. [Google Scholar]
- Zhao, S.G.; Chen, W.S.; Li, H.; Foye, A.; Zhang, M.; Sjöström, M.; Aggarwal, R.; Playdle, D.; Liao, A.; Alumkal, J.J.; et al. The DNA methylation landscape of advanced prostate cancer. Nat. Genet. 2020, 52, 778–789. [Google Scholar] [CrossRef]
- Brikun, I.; Nusskern, D.; Gillen, D.; Lynn, A.; Murtagh, D.; Feczko, J.; Nelson, W.G.; Freije, D. A panel of DNA methylation markers reveals extensive methylation in histologically benign prostate biopsy cores from cancer patients. Biomark. Res. 2014, 2, 25. [Google Scholar] [CrossRef] [Green Version]
- Brikun, I.; Nusskern, D.; Freije, D. An expanded biomarker panel for the detection of prostate cancer from urine DNA. Exp. Hematol. Oncol. 2019, 8, 13. [Google Scholar] [CrossRef]
- Brikun, I.; Nusskern, D.; Decatus, A.; Harvey, E.; Li, L.; Freije, D. A panel of DNA methylation markers for the detection of prostate cancer from FV and DRE urine DNA. Clin. Epigenetics 2018, 10, 91. [Google Scholar] [CrossRef] [Green Version]
- Diehl, F.; Li, M.; He, Y.; Kinzler, K.W.; Vogelstein, B.; Dressman, D. BEAMing: Single-molecule PCR on microparticles in water-in-oil emulsions. Nat. Methods 2006, 3, 551–559. [Google Scholar] [CrossRef]
- O’Reilly, E.; Tuzova, A.V.; Walsh, A.L.; Russell, N.M.; O’Brien, O.; Kelly, S.; Ni Dhomhnallain, O.; DeBarra, L.; Dale, C.M.; Brugman, R.; et al. epiCaPture: A Urine DNA Methylation Test for Early Detection of Aggressive Prostate Cancer. JCO Precis. Oncol. 2019, 2019, 1–18. [Google Scholar] [CrossRef]
- Sooriakumaran, P.; Kaba, R. The risks and benefits of cyclo-oxygenase-2 inhibitors in prostate cancer: A review. Int. J. Surg. 2005, 3, 278–285. [Google Scholar] [CrossRef] [Green Version]
- Bjerre, M.T.; Nørgaard, M.; Larsen, O.H.; Jensen, S.; Strand, S.H.; Østergren, P.; Fode, M.; Fredsøe, J.; Ulhøi, B.P.; Mortensen, M.M.; et al. Epigenetic Analysis of Circulating Tumor DNA in Localized and Metastatic Prostate Cancer: Evaluation of Clinical Biomarker Potential. Cells 2020, 9, 1362. [Google Scholar] [CrossRef]
- Lau, E.; McCoy, P.; Reeves, F.; Chow, K.; Clarkson, M.; Kwan, E.M.; Packwood, K.; Northen, H.; He, M.; Kingsbury, Z.; et al. Detection of ctDNA in plasma of patients with clinically localised prostate cancer is associated with rapid disease progression. Genome Med. 2020, 12, 72. [Google Scholar] [CrossRef]
- Corbetta, M.; Chiereghin, C.; De Simone, I.; Soldà, G.; Zuradelli, M.; Giunta, M.; Lughezzani, G.; Buffi, N.M.; Hurle, R.; Saita, A.; et al. Post-Biopsy Cell-Free DNA from Blood: An Open Window on Primary Prostate Cancer Genetics and Biology. Front. Oncol. 2021, 11, 1691. [Google Scholar] [CrossRef]
- Chen, E.; Cario, C.L.; Leong, L.; Lopez, K.; Márquez, C.P.; Chu, C.; Li, P.S.; Oropeza, E.; Tenggara, I.; Cowan, J.; et al. Cell-free DNA concentration and fragment size as a biomarker for prostate cancer. Sci. Rep. 2021, 11, 5040. [Google Scholar] [CrossRef]
- Ponti, G.; Maccaferri, M.; Manfredini, M.; Micali, S.; Torricelli, F.; Milandri, R.; del Prete, C.; Ciarrocchi, A.; Ruini, C.; Benassi, L.; et al. Quick assessment of cell-free DNA in seminal fluid and fragment size for early non-invasive prostate cancer diagnosis. Clin. Chim. Acta 2019, 497, 76–80. [Google Scholar] [CrossRef] [Green Version]
- Ponti, G.; Maccaferri, M.; Micali, S.; Manfredini, M.; Milandri, R.; Bianchi, G.; Pellacani, G.; Kaleci, S.; Chester, J.; Conti, A.; et al. Seminal cell free DNA concentration levels discriminate between prostate cancer and benign prostatic hyperplasia. Anticancer Res. 2018, 38, 5121–5125. [Google Scholar] [CrossRef]
- Simons, M.; Raposo, G. Exosomes—vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 21, 575–581. [Google Scholar] [CrossRef]
- Jia, Y.; Chen, Y.; Wang, Q.; Jayasinghe, U.; Luo, X.; Wei, Q.; Wang, J.; Xiong, H.; Chen, C.; Xu, B.; et al. Exosome: Emerging biomarker in breast cancer. Oncotarget 2017, 8, 41717–41733. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pashazadeh, M. The role of tumor-isolated exosomes on suppression of immune reactions and cancer progression: A systematic review. Med. J. Islam. Repub. Iran 2020, 34, 639–645. [Google Scholar] [CrossRef]
- Mashouri, L.; Yousefi, H.; Aref, A.R.; Ahadi, A.M.; Molaei, F.; Alahari, S.K. Exosomes: Composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol. Cancer 2019, 18, 75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, I.; Nabet, B.Y. Exosomes in the tumor microenvironment as mediators of cancer therapy resistance. Mol. Cancer 2019, 18, 32. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.; Lee, S.; Shin, E.; Seong, K.M.; Jin, Y.W.; Youn, H.; Youn, B. The Emerging Roles of Exosomes as EMT Regulators in Cancer. Cells 2020, 9, 861. [Google Scholar] [CrossRef]
- Yu, X.; Odenthal, M.; Fries, J.W. Exosomes as miRNA Carriers: Formation-Function-Future. Int. J. Mol. Sci. 2016, 17, 2028. [Google Scholar] [CrossRef] [Green Version]
- Huang, X.; Liang, M.; Dittmar, R.; Wang, L. Extracellular MicroRNAs in Urologic Malignancies: Chances and Challenges. Int. J. Mol. Sci. 2013, 14, 14785–14799. [Google Scholar] [CrossRef] [Green Version]
- Bertoli, G.; Cava, C.; Castiglioni, I. MicroRNAs as Biomarkers for Diagnosis, Prognosis and Theranostics in Prostate Cancer. Int. J. Mol. Sci. 2016, 17, 421. [Google Scholar] [CrossRef] [Green Version]
- Javidi, M.M.; Ahmadi, A.; Bakhshinejad, B.; Nouraee, N.; Babashah, S.; Sadeghizadeh, M. Cell-free microRNAs as cancer biomarkers: The odyssey of miRNAs through body fluids. Med. Oncol. 2014, 31, 295. [Google Scholar] [CrossRef]
- Lv, L.-L.; Cao, Y.; Liu, D.; Xu, M.; Liu, H.; Tang, R.-N.; Ma, K.-L.; Liu, B.-C. Isolation and Quantification of MicroRNAs from Urinary Exosomes/Microvesicles for Biomarker Discovery. Int. J. Biol. Sci. 2013, 9, 1021–1031. [Google Scholar] [CrossRef] [Green Version]
- Occhipinti, G.; Giulietti, M.; Principato, G.; Piva, F. The choice of endogenous controls in exosomal microRNA assessments from biofluids. Tumor Biol. 2016, 37, 11657–11665. [Google Scholar] [CrossRef]
- Endzeliņš, E.; Melne, V.; Kalnina, Z.; Lietuvietis, V.; Riekstina, U.; Llorente, A.; Linē, A. Diagnostic, prognostic and predictive value of cell-free miRNAs in prostate cancer: A systematic review. Mol. Cancer 2016, 15, 41. [Google Scholar] [CrossRef]
- Fabris, L.; Ceder, Y.; Chinnaiyan, A.M.; Jenster, G.W.; Sørensen, K.D.; Tomlins, S.; Visakorpi, T.; Calin, G.A. The Potential of MicroRNAs as Prostate Cancer Biomarkers. Eur. Urol. 2016, 70, 312–322. [Google Scholar] [CrossRef] [Green Version]
- Adhami, M.; Haghdoost, A.A.; Sadeghi, B.; Afshar, R.M. Candidate miRNAs in human breast cancer biomarkers: A systematic review. Breast Cancer 2017, 25, 198–205. [Google Scholar] [CrossRef]
- A Joosse, S.; Müller, V.; Steinbach, B.; Pantel, K.; Schwarzenbach, H. Circulating cell-free cancer-testis MAGE-A RNA, BORIS RNA, let-7b and miR-202 in the blood of patients with breast cancer and benign breast diseases. Br. J. Cancer 2014, 111, 909–917. [Google Scholar] [CrossRef] [Green Version]
- Zhong, S.; Golpon, H.; Zardo, P.; Borlak, J. miRNAs in lung cancer. A systematic review identifies predictive and prognostic miRNA candidates for precision medicine in lung cancer. Transl. Res. 2021, 230, 164–196. [Google Scholar] [CrossRef]
- Toiyama, Y.; Okugawa, Y.; Fleshman, J.; Boland, C.R.; Goel, A. MicroRNAs as potential liquid biopsy biomarkers in colorectal cancer: A systematic review. Biochim. Biophys. Acta BBA Rev. Cancer 2018, 1870, 274–282. [Google Scholar] [CrossRef]
- Parizadeh, S.M.; Jafarzadeh-Esfehani, R.; Ghandehari, M.; Hasanzadeh, M.; Parizadeh, S.M.; Hassanian, S.M.; Rezaei-Kalat, A.; Aghabozorgi, A.S.; Rahimi-Kakhki, R.; Zargaran, B.; et al. Circulating and tissue microRNAs as biomarkers for ovarian cancer prognosis. Curr. Drug Targets 2019, 20, 1447–1460. [Google Scholar] [CrossRef]
- Jayaraj, R.; Raymond, G.; Krishnan, S.; Tzou, K.S.; Baxi, S.; Ram, M.R.; Govind, S.K.; Chandramoorthy, H.C.; Abu-Khzam, F.N.; Shaw, P. Clinical Theragnostic Potential of Diverse miRNA Expressions in Prostate Cancer: A Systematic Review and Meta-Analysis. Cancers 2020, 12, 1199. [Google Scholar] [CrossRef]
- Hrovatin, K.; Kunej, T. Classification of heterogeneous genetic variations of microRNA regulome in cancer. Cancer Lett. 2018, 419, 128–138. [Google Scholar] [CrossRef]
- Ding, H.-X.; Lv, Z.; Yuan, Y.; Xu, Q. MiRNA Polymorphisms and Cancer Prognosis: A Systematic Review and Meta-Analysis. Front. Oncol. 2018, 8, 596. [Google Scholar] [CrossRef] [PubMed]
- Mulrane, L.; McGee, S.F.; Gallagher, W.M.; O’Connor, D.P. miRNA Dysregulation in Breast Cancer. Cancer Res. 2013, 73, 6554–6562. [Google Scholar] [CrossRef] [PubMed]
- Khan, S.; Ayub, H.; Khan, T.; Wahid, F. MicroRNA biogenesis, gene silencing mechanisms and role in breast, ovarian and prostate cancer. Biochimie 2019, 167, 12–24. [Google Scholar] [CrossRef] [PubMed]
- Verma, S.; Pandey, M.; Shukla, G.C.; Singh, V.; Gupta, S. Integrated analysis of miRNA landscape and cellular networking pathways in stage-specific prostate cancer. PLoS ONE 2019, 14, e0224071. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Endzeliņš, E.; Berger, A.; Melne, V.; Bajo-Santos, C.; Soboļevska, K.; Ābols, A.; Rodriguez, M.; Šantare, D.; Rudņickiha, A.; Lietuvietis, V.; et al. Detection of circulating miRNAs: Comparative analysis of extracellular vesicle-incorporated miRNAs and cell-free miRNAs in whole plasma of prostate cancer patients. BMC Cancer 2017, 17, 730. [Google Scholar] [CrossRef] [PubMed]
- Bryant, R.J.; Pawlowski, T.; Catto, J.; Marsden, G.; Vessella, R.L.; Rhees, B.; Kuslich, C.; Visakorpi, T.; Hamdy, F.C. Changes in circulating microRNA levels associated with prostate cancer. Br. J. Cancer 2012, 106, 768–774. [Google Scholar] [CrossRef] [Green Version]
- Hao, X.-K.; Li, Z.; Ma, Y.-Y.; Wang, J.; Zeng, X.-F.; Li, R.; Kang, W. Exosomal microRNA-141 is upregulated in the serum of prostate cancer patients. OncoTargets Ther. 2015, 9, 139–148. [Google Scholar] [CrossRef] [Green Version]
- Samsonov, R.; Shtam, T.; Burdakov, V.; Glotov, A.; Tsyrlina, E.; Berstein, L.; Nosov, A.; Evtushenko, V.; Filatov, M.; Malek, A. Lectin-induced agglutination method of urinary exosomes isolation followed by mi-RNA analysis: Application for prostate cancer diagnostic. Prostate 2016, 76, 68–79. [Google Scholar] [CrossRef]
- Foj, L.; Ferrer, F.; Serra, M.; Arévalo, A.; Gavagnach, M.; Gimenez, N.; Filella, X. Exosomal and Non-Exosomal Urinary miRNAs in Prostate Cancer Detection and Prognosis. Prostate 2017, 77, 573–583. [Google Scholar] [CrossRef]
- Zhou, C.; Chen, Y.; He, X.; Zheng, Z.; Xue, D. Functional Implication of Exosomal miR-217 and miR-23b-3p in the Progression of Prostate Cancer. OncoTargets Ther. 2020, 13, 11595–11606. [Google Scholar] [CrossRef]
- Alix-Panabières, C. The future of liquid biopsy. Nature 2020, 579, S9. [Google Scholar] [CrossRef] [Green Version]
- Barceló, M.; Castells, M.; Bassas, L.; Vigués, F.; Larriba, S. Semen miRNAs Contained in Exosomes as Non-Invasive Biomarkers for Prostate Cancer Diagnosis. Sci. Rep. 2019, 9, 13772. [Google Scholar] [CrossRef]
- Ruiz-Plazas, X.; Altuna-Coy, A.; Alves-Santiago, M.; Vila-Barja, J.; García-Fontgivell, J.F.; Martínez-González, S.; Segarra-Tomás, J.; Chacón, M.R. Liquid Biopsy-Based Exo-oncomiRNAs Can Predict Prostate Cancer Aggressiveness. Cancers 2021, 13, 250. [Google Scholar] [CrossRef]
- Mercadal, M.; Herrero, C.; López-Rodrigo, O.; Castells, M.; de la Fuente, A.; Vigués, F.; Bassas, L.; Larriba, S. Impact of Extracellular Vesicle Isolation Methods on Downstream Mirna Analysis in Semen: A Comparative Study. Int. J. Mol. Sci. 2020, 21, 5949. [Google Scholar] [CrossRef]
- Watahiki, A.; Macfarlane, R.J.; Gleave, M.E.; Crea, F.; Wang, Y.; Helgason, C.D.; Chi, K.N. Plasma miRNAs as Biomarkers to Identify Patients with Castration-Resistant Metastatic Prostate Cancer. Int. J. Mol. Sci. 2013, 14, 7757–7770. [Google Scholar] [CrossRef] [Green Version]
- Bhagirath, D.; Yang, T.L.; Bucay, N.; Sekhon, K.; Majid, S.; Shahryari, V.; Dahiya, R.; Tanaka, Y.; Saini, S. microRNA-1246 Is an Exosomal Biomarker for Aggressive Prostate Cancer. Cancer Res. 2018, 78, 1833–1844. [Google Scholar] [CrossRef] [Green Version]
- Bhagirath, D.; Yang, T.L.; Akoto, T.; Patel, N.; Tabatabai, L.Z.; Saini, S. MicroRNA-4287 is a novel tumor suppressor microRNA controlling epithelial-to mesenchymal transition in prostate cancer. Oncotarget 2020, 11, 4681–4692. [Google Scholar] [CrossRef]
- Guo, T.; Wang, Y.; Jia, J.; Mao, X.; Stankiewicz, E.; Scandura, G.; Burke, E.; Xu, L.; Marzec, J.; Davies, C.R.; et al. The Identification of Plasma Exosomal miR-423-3p as a Potential Predictive Biomarker for Prostate Cancer Castration-Resistance Development by Plasma Exosomal miRNA Sequencing. Front. Cell Dev. Biol. 2021, 8, 602493. [Google Scholar] [CrossRef]
- Huang, X.; Yuan, T.; Liang, M.; Du, M.; Xia, S.; Dittmar, R.; Wang, D.; See, W.; Costello, B.A.; Quevedo, F.; et al. Exosomal miR-1290 and miR-375 as Prognostic Markers in Castration-resistant Prostate Cancer. Eur. Urol. 2014, 67, 33–41. [Google Scholar] [CrossRef] [Green Version]
- Rodríguez, M.; Bajo-Santos, C.; Hessvik, N.P.; Lorenz, S.; Fromm, B.; Berge, V.; Sandvig, K.; Linē, A.; Llorente, A. Identification of non-invasive miRNAs biomarkers for prostate cancer by deep sequencing analysis of urinary exosomes. Mol. Cancer 2017, 16, 156. [Google Scholar] [CrossRef]
- Li, W.; Dong, Y.; Wang, K.J.; Deng, Z.; Zhang, W.; Shen, H.F. Plasma exosomal miR-125a-5p and miR-141-5p as non-invasive biomarkers for prostate cancer. Neoplasma 2021, 67, 1314–1318. [Google Scholar] [CrossRef] [PubMed]
- Chaffer, C.L.; Weinberg, R.A. A perspective on cancer cell metastasis. Science 2011, 331, 1559–1564. [Google Scholar] [CrossRef] [PubMed]
- Cristofanilli, M.; Budd, G.T.; Ellis, M.J.; Stopeck, A.; Matera, J.; Miller, M.C.; Reuben, J.M.; Doyle, G.V.; Allard, W.J.; Terstappen, L.W.; et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med. 2004, 351, 781–791. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gkountela, S.; Szczerba, B.; Donato, C.; Aceto, N. Recent advances in the biology of human circulating tumour cells and metastasis. ESMO Open 2016, 1, e000078. [Google Scholar] [CrossRef] [PubMed]
- Sharma, S.; Zhuang, R.; Long, M.; Pavlovic, M.; Kang, Y.; Ilyas, A.; Asghar, W. Circulating tumor cell isolation, culture, and downstream molecular analysis. Biotechnol. Adv. 2018, 36, 1063–1078. [Google Scholar] [CrossRef] [PubMed]
- Giesing, M.; Suchy, B.; Driesel, G.; Molitor, D. Clinical utility of antioxidant gene expression levels in circulating cancer cell clusters for the detection of prostate cancer in patients with prostate-specific antigen levels of 4–10 ng/mL and disease prognostication after radical prostatectomy. BJU Int. 2010, 105, 1000–1010. [Google Scholar] [CrossRef]
- Kolostova, K.; Broul, M.; Schraml, J.; Cegan, M.; Matkowski, R.; Fiutowski, M.; Bobek, V. Circulating tumor cells in localized prostate cancer: Isolation, cultivation in vitro and relationship to T-stage and Gleason score. Anticancer Res. 2014, 34, 3641–3646. [Google Scholar]
- Todenhöfer, T.; Park, E.S.; Duffy, S.; Deng, X.; Jin, C.; Abdi, H.; Ma, H.; Black, P.C. Microfluidic enrichment of circulating tumor cells in patients with clinically localized prostate cancer. Urol. Oncol. Semin. Orig. Investig. 2016, 34, 483.e9–483.e16. [Google Scholar] [CrossRef]
- Renier, C.; Pao, E.; Che, J.; Liu, H.E.; Lemaire, C.A.; Matsumoto, M.; Triboulet, M.; Srivinas, S.; Jeffrey, S.S.; Rettig, M.; et al. Label-free isolation of prostate circulating tumor cells using Vortex microfluidic technology. NPJ Precis. Oncol. 2017, 1, 15. [Google Scholar] [CrossRef]
- Awe, J.A.; Saranchuk, J.; Drachenberg, D.; Mai, S. Filtration-based enrichment of circulating tumor cells from all prostate cancer risk groups. Urol. Oncol. Semin. Orig. Investig. 2017, 35, 300–309. [Google Scholar] [CrossRef]
- Miyamoto, D.T.; Sequist, L.V.; Lee, R.J. Circulating tumour cells—monitoring treatment response in prostate cancer. Nat. Rev. Clin. Oncol. 2014, 11, 401–412. [Google Scholar] [CrossRef]
- Miyamoto, D.T.; Lee, R.J.; Kalinich, M.; LiCausi, J.A.; Zheng, Y.; Chen, T.; Milner, J.D.; Emmons, E.; Ho, U.; Broderick, K.; et al. An RNA-based digital circulating tumor cell signature is predictive of drug response and early dissemination in prostate cancer. Cancer Discov. 2018, 8, 288–303. [Google Scholar] [CrossRef] [Green Version]
- Murray, N.P.; Aedo, S.; Fuentealba, C.; Reyes, E.; Minzer, S.; Salazar, A. The presence of secondary circulating prostate tumour cells determines the risk of biochemical relapse for patients with low- and intermediate-risk prostate cancer who are treated only with external radiotherapy. Ecancermedicalscience 2018, 12, 844. [Google Scholar] [CrossRef]
- Nickens, K.P.; Ali, A.; Scoggin, T.; Tan, S.; Ravindranath, L.; McLeod, D.G.; Dobi, A.; Tacha, D.; Sesterhenn, I.A.; Srivastava, S.; et al. Prostate cancer marker panel with single cell sensitivity in urine. Prostate 2015, 75, 969–975. [Google Scholar] [CrossRef] [Green Version]
- Campbell, D.H.; Lund, M.E.; Nocon, A.L.; Cozzi, P.J.; Frydenberg, M.; De Souza, P.; Schiller, B.; Beebe-Dimmer, J.L.; Ruterbusch, J.J.; Walsh, B.J. Detection of glypican-1 (GPC-1) expression in urine cell sediments in prostate cancer. PLoS ONE 2018, 13, e0196017. [Google Scholar] [CrossRef] [Green Version]
- Lund, M.E.; Campbell, D.H.; Walsh, B.J. The Role of Glypican-1 in the Tumour Microenvironment. Tumor Microenviron. 2020, 1245, 163–176. [Google Scholar]
- Rzhevskiy, A.S.; Bazaz, S.R.; Ding, L.; Kapitannikova, A.; Sayyadi, N.; Campbell, D.; Walsh, B.; Gillatt, D.; Warkiani, M.E.; Zvyagin, A.V. Rapid and Label-Free Isolation of Tumour Cells from the Urine of Patients with Localised Prostate Cancer Using Inertial Microfluidics. Cancers 2019, 12, 81. [Google Scholar] [CrossRef] [Green Version]
- Gardiner, R.; Samaratunga, M.; Gwynne, R.; Clague, A.; Seymour, G.; Lavin, M. Abnormal prostatic cells in ejaculates from men with prostatic cancer - a preliminary report. Br. J. Urol. 1996, 78, 414–418. [Google Scholar] [CrossRef]
- Rzhevskiy, A.S.; Kapitannikova, A.Y.; Vasilescu, S.A.; Karashaeva, T.A.; Bazaz, S.R.; Taratkin, M.S.; Enikeev, D.V.; Lekarev, V.Y.; Shpot, E.V.; Butnaru, D.V.; et al. Isolation of Circulating Tumor Cells from Seminal Fluid of Patients with Prostate Cancer Using Inertial Microfluidics. Cancers 2022, 14, 3364. [Google Scholar] [CrossRef]
- Davis, J.W.; Nakanishi, H.; Kumar, V.S.; Bhadkamkar, V.A.; McCormack, R.; Fritsche, H.A.; Handy, B.; Gornet, T.; Babaian, R.J. Circulating Tumor Cells in Peripheral Blood Samples from Patients with Increased Serum Prostate Specific Antigen: Initial Results in Early Prostate Cancer. J. Urol. 2008, 179, 2187–2191. [Google Scholar] [CrossRef]
- Lowes, L.E.; Lock, M.; Rodrigues, G.; D’Souza, D.; Bauman, G.; Ahmad, B.; Venkatesan, V.; Allan, A.L.; Sexton, T. Circulating tumour cells in prostate cancer patients receiving salvage radiotherapy. Clin. Transl. Oncol. 2012, 14, 150–156. [Google Scholar] [CrossRef] [PubMed]
- Thalgott, M.; Rack, B.; Maurer, T.; Souvatzoglou, M.; Eiber, M.; Kreß, V.; Heck, M.M.; Andergassen, U.; Nawroth, R.; Gschwend, J.E.; et al. Detection of circulating tumor cells in different stages of prostate cancer. J. Cancer Res. Clin. Oncol. 2013, 139, 755–763. [Google Scholar] [CrossRef] [PubMed]
- Khurana, K.; Grane, R.; Borden, E.C.; Klein, E.A. Prevalence of Circulating Tumor Cells in Localized Prostate Cancer. Curr. Urol. 2013, 7, 65–69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Loh, J.; Jovanovic, L.; Lehman, H.M.; Capp, A.; Pryor, D.; Harris, M.; Nelson, C.; Martin, J. Circulating tumor cell detection in high-risk non-metastatic prostate cancer. J. Cancer Res. Clin. Oncol. 2014, 140, 2157–2162. [Google Scholar] [CrossRef] [PubMed]
- Pal, S.K.; He, M.; Wilson, T.; Liu, X.; Zhang, K.; Carmichael, C.; Torres, A.; Hernandez, S.; Lau, C.; Agarwal, N.; et al. Detection and Phenotyping of Circulating Tumor Cells in High-Risk Localized Prostate Cancer. Clin. Genitourin. Cancer 2014, 13, 130–136. [Google Scholar] [CrossRef] [Green Version]
- Thalgott, M.; Rack, B.; Horn, T.; Heck, M.M.; Eiber, M.; Kübler, H.; Retz, M.; E Gschwend, J.; Andergassen, U.; Nawroth, R. Detection of Circulating Tumor Cells in Locally Advanced High-risk Prostate Cancer During Neoadjuvant Chemotherapy and Radical Prostatectomy. Anticancer Res. 2015, 35, 5679–5685. [Google Scholar]
- Meyer, C.P.; Pantel, K.; Tennstedt, P.; Stroelin, P.; Schlomm, T.; Heinzer, H.; Riethdorf, S.; Steuber, T. Limited prognostic value of preoperative circulating tumor cells for early biochemical recurrence in patients with localized prostate cancer. Urol. Oncol. Semin. Orig. Investig. 2016, 34, 235.e11–235.e16. [Google Scholar] [CrossRef]
- Tsumura, H.; Satoh, T.; Ishiyama, H.; Tabata, K.-I.; Takenaka, K.; Sekiguchi, A.; Nakamura, M.; Kitano, M.; Hayakawa, K.; Iwamura, M. Perioperative Search for Circulating Tumor Cells in Patients Undergoing Prostate Brachytherapy for Clinically Nonmetastatic Prostate Cancer. Int. J. Mol. Sci. 2017, 18, 128. [Google Scholar] [CrossRef] [Green Version]
- Kuske, A.; Gorges, T.M.; Tennstedt, P.; Tiebel, A.-K.; Pompe, R.; Preißer, F.; Prues, S.; Mazel, M.; Markou, A.; Lianidou, E.; et al. Improved detection of circulating tumor cells in non-metastatic high-risk prostate cancer patients. Sci. Rep. 2016, 6, 39736. [Google Scholar] [CrossRef] [Green Version]
- Stott, S.L.; Lee, R.J.; Nagrath, S.; Yu, M.; Miyamoto, D.T.; Ulkus, L.; Inserra, E.J.; Ulman, M.; Springer, S.; Nakamura, Z.; et al. Isolation and Characterization of Circulating Tumor Cells from Patients with Localized and Metastatic Prostate Cancer. Sci. Transl. Med. 2010, 2, 25ra23. [Google Scholar] [CrossRef] [Green Version]
- Russo, G.I.; Bier, S.; Hennenlotter, J.; Beger, G.; Pavlenco, L.; Van De Flierdt, J.; Hauch, S.; Maas, M.; Walz, S.; Rausch, S.; et al. Expression of tumour progression-associated genes in circulating tumour cells of patients at different stages of prostate cancer. Br. J. Urol. 2018, 122, 152–159. [Google Scholar] [CrossRef] [Green Version]
- Puche-Sanz, I.; Cubero, M.J.A.; Pascual-Geler, M.; Rodriguez-Martinez, A.; Delgado-Rodríguez, M.; García-Puche, J.L.; Expósito, J.; Robles-Fernández, I.; Entrala-Bernal, C.; Lorente, J.A.; et al. A comprehensive study of circulating tumour cells at the moment of prostate cancer diagnosis: Biological and clinical implications of EGFR, AR and SNPs. Oncotarget 2017, 8, 70472–70480. [Google Scholar] [CrossRef]
- García, J.L.; Lozano, R.; Misiewicz-Krzeminska, I.; Fernández-Mateos, J.; Krzeminski, P.; Alfonso, S.; Marcos, R.A.; García, R.; Gómez-Veiga, F.; Virseda, Á.; et al. A novel capillary nano-immunoassay for assessing androgen receptor splice variant 7 in plasma. Correlation with CD133 antigen expression in circulating tumor cells. A pilot study in prostate cancer patients. Clin. Transl. Oncol. 2017, 19, 1350–1357. [Google Scholar] [CrossRef] [Green Version]
- Mohme, M.; Riethdorf, S.; Dreimann, M.; Werner, S.; Maire, C.L.; Joosse, S.A.; Bludau, F.; Mueller, V.; Neves, R.P.L.; Stoecklein, N.H.; et al. Circulating Tumour Cell Release after Cement Augmentation of Vertebral Metastases. Sci. Rep. 2017, 7, 7196. [Google Scholar] [CrossRef]
- Joosse, S.A.; Beyer, B.; Gasch, C.; Nastały, P.; Kuske, A.; Isbarn, H.; Horst, L.J.; Hille, C.; Gorges, T.M.; Cayrefourcq, L.; et al. Tumor-associated release of prostatic cells into the blood after transrectal ultrasound-guided biopsy in patients with histologically confirmed prostate cancer. Clin. Chem. 2020, 66, 161–168. [Google Scholar] [CrossRef]
- Chambers, A.F.; Groom, A.C.; MacDonald, I.C. Dissemination and growth of cancer cells in metastatic sites. Nat. Rev. Cancer 2002, 2, 563–572. [Google Scholar] [CrossRef]
- Gorin, M.A.; Verdone, J.E.; Van Der Toom, E.; Bivalacqua, T.J.; Allaf, M.E.; Pienta, K.J. Circulating tumour cells as biomarkers of prostate, bladder, and kidney cancer. Nat. Rev. Urol. 2017, 14, 90–97. [Google Scholar] [CrossRef]
- Nastały, P.; Ruf, C.; Becker, P.; Bednarz-Knoll, N.; Stoupiec, M.; Kavsur, R.; Isbarn, H.; Matthies, C.; Wagner, W.; Höppner, D.; et al. Circulating Tumor Cells in Patients with Testicular Germ Cell TumorsCirculating Tumor Cells in Testicular Germ Cell Tumors. Clin. Cancer Res. 2014, 20, 3830–3841. [Google Scholar] [CrossRef] [Green Version]
- Kraan, J.; Sleijfer, S.; Strijbos, M.H.; Ignatiadis, M.; Peeters, D.; Pierga, J.-Y.; Farace, F.; Riethdorf, S.; Fehm, T.; Zorzino, L.; et al. External quality assurance of circulating tumor cell enumeration using the CellSearch® system: A feasibility study. Cytom. Part B Clin. Cytom. 2010, 80, 112–118. [Google Scholar] [CrossRef]
- Todenhoefer, T.; Hennenlotter, J.; Feyerabend, S.; Aufderklamm, S.; Mischinger, J.; Kuehs, U.; Gerber, V.; Fetisch, J.; Schilling, D.; Hauch, S.; et al. Preliminary experience on the use of the Adnatest® system for detection of circulating tumor cells in prostate cancer patients. Anticancer. Res. 2012, 32, 3507–3513. [Google Scholar]
- Alix-Panabières, C.; Pantel, K. Circulating tumor cells: Liquid biopsy of cancer. Clin. Chem. 2013, 59, 110–118. [Google Scholar] [CrossRef] [PubMed]
- Koch, C.; Kuske, A.; Joosse, S.A.; Yigit, G.; Sflomos, G.; Thaler, S.; Smit, D.J.; Werner, S.; Borgmann, K.; Gärtner, S.; et al. Characterization of circulating breast cancer cells with tumorigenic and metastatic capacity. EMBO Mol. Med. 2020, 12, e11908. [Google Scholar] [CrossRef] [PubMed]
miRNA | Biological Fluid | Patients/ Healthy Controls | Isolation Method | Diagnostic Value | Prognostic Value | Reference |
---|---|---|---|---|---|---|
miR-342-3p | Seminal fluid | 11 HC, 7 BPH, 40 PCa | Centrifugation + microfiltration + ultracentrifugation | Discrimination between GS ≥ 7 and GS = 6 (Sn: 63.6%; Sp: 90%) | [92] | |
miR-374b-5p | Discrimination between GS ≥ 7 and GS = 6 (Sn: 45.5%; Sp: 90%) | |||||
miR-342-3p+ miR-374b-5p | Discrimination between GS ≥ 7 and GS = 6 (Sn: 54.5%; Sp: 80%) | |||||
miR-142-3p+ miR-142-5p+ miR-223-3p | Discrimination between PCa and BPH (Sn:91.7% Sp:42.9%) | |||||
MiR-375 | Plasma | 50 PCa, 22 BPH | Size exclusion chromatography | Discrimination between PCa and BPH (N/A) | [85] | |
miR-200c-3p+ miR-21-5p | Discrimination between PCa and BPH | |||||
Let-7a-5p | Discrimination between GS ≥ 7 and GS = 6 | |||||
let-7c | Urine | 10 HC, 52 PCa | Differential centrifugation | Discrimination between HC and low-, intermediate-, and high-risk PCa | Discrimination between GS > 8 and GS = 6 | [89] |
miR-21 | Discrimination between HC and low-, intermediate-, and high-risk PCa | |||||
miR-375 | Discrimination between HC and low-, intermediate-, and high-risk PCa | |||||
miR-574-3p | Urine | 35 HC, 35 PCa | Differential centrifugation + Lectin-Based Agglutination | Discrimination between HC and PCa (Sn: 0.71) | [88] | |
miR-141-5p | Discrimination between HC and PCa (Sn: 0.66) | |||||
miR-21-5p | Discrimination between HC and PCa (Sn: 0.46) | |||||
miR-196a-5p | Urine | 20 PCa, 10 HC | Differential centrifugation | Discrimination between HC and PCa (Sp: 89%, Sn: 100%) | [100] | |
miR-501-3p | Discrimination between HC and PCa | |||||
miR-217 | Plasma | 10 PCa, 10 HC | Differential centrifugation + RNeasy Mini Spin kit | Discrimination between HC and PCa | [90] | |
miR-23b-3p | Discrimination between HC and PCa | |||||
miRNA-125a-5p | Plasma | 31 PCa, 20 HC | Differential centrifugation | Discrimination between HC and PCa | [101] | |
miR-141-5p | Discrimination between HC and PCa | |||||
miR-141 | Serum | 20 PCa, 20 BPH, 20 HC | ExoQuick Exosome Precipitation Solution | Discrimination between HC + BPH and PCa | [87] | |
miR-141+ miR-375 | Plasma | 78 PCa (12 GS<8), 28 HC | Qiagen miRNeasy kit | Discrimination between low-risk and high-risk PCa | [86] | |
miR-107+ miR-574-3p | Urine | mirVana kit | Discrimination between HC and PCa | |||
miR-205 | Plasma | 25 localized PCa, 25 mCRPCa | Differential centrifugation | Discrimination between localized and metastatic PCa, correlation with lower risk of poor outcome | [95] | |
miR-141 | Discrimination between low-risk and high-risk PCa, strong correlation with poor outcome; Discrimination between localized PCa and mCRPCa | |||||
miR-151-3p | Discrimination between localized and mCRPCa | |||||
miR-423-3p | Discrimination between localized and mCRPCa | |||||
miR-152 | Discrimination between low-risk and high-risk PCa, strong correlation with poor outcome | |||||
miR-375 | Discrimination between localized PCa and mCRPCa | |||||
miR-21 | Discrimination between docetaxel-resistant and docetaxel-sensitive PCa patients | |||||
miR-141+ miR151-3p+ miR-16 | Discrimination between mCRPC and localized PCa | |||||
miR-126 | Discrimination between mCRPC and localized PCa | |||||
miR-1290 | Plasma | Differential centrifugation | Discrimination between low-risk and high-risk PCa; association with poor outcome; prediction of androgen deprivation (ADT) failure | [99] | ||
miR-375 | Discrimination between low-risk and high-risk PCa; association with poor outcome; prediction of ADT failure | |||||
miR-1290 + miR-375 | Discrimination between low-risk and high-risk PCa; association with poor outcome; prediction of ADT failure | |||||
miR-221-3p | Seminal fluid, urine | 97 PCa | Differential centrifugation | Discrimination between low-risk and high-risk PCa | [93] | |
miR-31-5p | Discrimination between low-risk and high-risk PCa | |||||
miR-222-3p | Discrimination between low-risk and high-risk PCa | |||||
miR-193-3p | Discrimination between low-risk and high-risk PCa | |||||
miR-423-5p | Discrimination between low-risk and high-risk PCa | |||||
miR- 221-3p+ miR-222-3p+ TWEAK | Discrimination between low-risk and high-risk aggressive PCa (Sp: 85.7%, Sn: 76.9%) | |||||
miR-1246 | Serum | 44 PCa | Total exosome isolation reagent | Discrimination between HC and PCa (Sp: 100%, Sn: 75%) | Discrimination between localized and metastatic PCa | [96] |
miR-4287 | Serum | 68 PCa, BPH, HC | Total exosome isolation reagent | Discrimination between HC and PCa (Sp: 88.24%) | Discrimination between localized PCa (GS 4-6) and metastatic PCa (GS > 7) | [97] |
miR-423-3p | Plasma | 132 PCa, 66 mCRPCa | Differential centrifugation | Discrimination between mCRPC and localized PCa | [98] |
Type of CTC Isolation | CTC Isolation Technique (Label-Free or Affinity-Based) | Biological Fluid (Volume) | Number of PCa Patients/HCs and BPH Patients | Cut-Off Number of CTCs for CTC+ Patients | Percentage of CTC+ Patients/Healthy Volunteers | Min-Max Number of CTCs per mL in Patients | Correlation between the Amount or Presence of CTCs and Clinico-Pathological Parameters of PCa | Ref. |
---|---|---|---|---|---|---|---|---|
Label-free | Filtration + RT PCR for PSA and antioxidant genes | Blood (NA) | 129 patients with non-metastatic PCa/NA | NA | 32.5%/NA | NA | Strong correlation between the expression of SOD2 or TXNRD1, and tumor size or GS | [106] |
Filtration + CK dependent ICC * | Blood (8 mL) | 55 patients with non-metastatic PCa/NA | ≥1 | 52%/NA | NA | No correlation between the presence of CTCs and GS or T stage. No correlation between the CTC count and response to treatment | [107] | |
Microfluidics + EPCAM. CK dependent ICC | Blood (2 mL) | 50 patients with non-metastatic PCa/NA | ≥1 | 50%/NA | 0.5 – 208.5 | No correlation between the presence of CTCs and the PSA serum level, age, GS, T stage, or N stage. No correlation between the number of CTCs and GS, T stage, or N stage | [108] | |
Filtration + CK, AR dependent ICC | Blood (3 mL) | 41 patients with non-metastatic PCa/NA | ≥1 | 100%/NA | NA | NA | [110] | |
Microfluidics + droplet digital PCR (dd-PCR) | Blood (20 mL) | 34 patients with non-metastatic PCa/34 HCs | NA | NA/NA | NA | d-PCR ** for 8 PCa-specific genes allowed to predict dissemination of CTCs to seminal vesicles and lymph nodes | [112] | |
Filtration + ERG, AMACR, PSA dependent ICC | Urine (NA) | 25 patients with non-metastatic/32 HCs | ≥1 | 64%/21.2% | NA | NA | [116] | |
Sedimentation + GPC-1 dependent ICC | Urine (50–100 mL) | 41 patients with non-metastatic PCa/47 HCs and 37 BPH patients | ≥ 1 | 71%/30% and 24% | NA | NA | [115] | |
Gel centrifugation + PSA dependent ICC | Blood (8 mL) | 241 patients with non-metastatic PCa at 3 months post-radiotherapy/NA | ≥1 | 47.8%/NA | NA | NA | [113] | |
Microfluidics + GPC-1 dependent ICC | Urine (30–100 mL) | 14 patients with non-metastatic PCa/14 HCs | >8 | 79%/21% | 0.1–4.9 | Moderate correlation between the amount of CTCs and GS, or PSA serum level | [117] | |
Affinity-based | Microfluidics + EPCAM dependent ICC | Blood (20 mL) | 19 patients with non-metastatic PCa/17 HCs | ≥14 mL−1 | 42%/47% | 38–222 | Poor correlation between the amount of CTCs and PSA serum level | [130] |
CellSearch | Blood (7.5 mL) | 26 patients with non-metastatic PCa/7 HCs | ≥1 | 73%/0% | NA | No correlation between the number of CTCs and GS, or PSA serum level, or T stage | [121] | |
CellSearch | Blood (7.5 mL) | 10 patients with non-metastatic PCa/NA | ≥1 | 10%/NA | 0.0–0.1 | NA | [123] | |
CellSearch | Blood (7.5 mL) | 20 patients with non-metastatic PCa/15 HCs | ≥1 | 5%/0% | 0.0–0.1 | NA | [122] | |
CellSearch | Blood (7.5 mL) | 36/NA | ≥1 | 14%/NA | 0.0–0.4 | NA | [124] | |
CellSearch | Blood (22.5 mL) | 32 patients with non-metastatic PCa/5 HCs | ≥1 | 45%/0% | 0.0–0.1 | No correlation between CTC amount and biochemical recurrence of PCa | [125] | |
CellSearch | Blood (20.0 mL) | 15 patients with non-metastatic PCa/15 HCs | ≥1 | 20%/0% | 0.0–0.2 | No correlation between CTC detection and GS, PSA serum level, T and N stages, positive surgical margin | [126] | |
CellSearch | Blood (7.5 mL) | 152 patients with non-metastatic PCa/NA | ≥1 | 11%/NA | 0.13–13.3 | Weak correlation between CTC detection and GS, PSA serum level, or T stage | [127] | |
CellSearch EPISPOT CellCollector | Blood (7.5 mL) | 86 patients with non-metastatic PCa/NA | ≥1 | 37%/NA 54.9%/NA 58.7%/NA | 0.13–1.3 0.13–1.6 0.13–1.7 | Significant correlation between CTC detection and PSA serum values, or clinical tumor stage. No correlations in case of CellSearch and CellCollector | [129] | |
CellSearch | Blood (7.5 mL) | 59 patients with non-metastatic PCa/NA | ≥1 | 0%/NA | NA | NA | [128] | |
Assessment of AR-V7 through a capillary nano-immunoassay | Blood (10 mL) | 16 patients with non-metastatic PCa/11 HCs | NA | 18.7%/0% | NA | Significant correlation between presence of AR-V7 and expression of CD133 antigen | [131] | |
Multi-CK dependent immune-magnetic collection | Blood (10 mL) | 86 patients with non-metastatic PCa/17 HCs | ≥1 | 18.6%/0% | 0–0.4 | NA | [132] | |
AdnaTest Prostate-Cancer | Blood (5 mL) | 47 patients with non-metastatic PCa/NA | NA | 25.5%/NA | NA | NA | [109] |
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Rzhevskiy, A.S.; Kapitannikova, A.Y.; Butnaru, D.V.; Shpot, E.V.; Joosse, S.A.; Zvyagin, A.V.; Ebrahimi Warkiani, M. Liquid Biopsy in Diagnosis and Prognosis of Non-Metastatic Prostate Cancer. Biomedicines 2022, 10, 3115. https://doi.org/10.3390/biomedicines10123115
Rzhevskiy AS, Kapitannikova AY, Butnaru DV, Shpot EV, Joosse SA, Zvyagin AV, Ebrahimi Warkiani M. Liquid Biopsy in Diagnosis and Prognosis of Non-Metastatic Prostate Cancer. Biomedicines. 2022; 10(12):3115. https://doi.org/10.3390/biomedicines10123115
Chicago/Turabian StyleRzhevskiy, Alexey S., Alina Y. Kapitannikova, Denis V. Butnaru, Evgeniy V. Shpot, Simon A. Joosse, Andrei V. Zvyagin, and Majid Ebrahimi Warkiani. 2022. "Liquid Biopsy in Diagnosis and Prognosis of Non-Metastatic Prostate Cancer" Biomedicines 10, no. 12: 3115. https://doi.org/10.3390/biomedicines10123115
APA StyleRzhevskiy, A. S., Kapitannikova, A. Y., Butnaru, D. V., Shpot, E. V., Joosse, S. A., Zvyagin, A. V., & Ebrahimi Warkiani, M. (2022). Liquid Biopsy in Diagnosis and Prognosis of Non-Metastatic Prostate Cancer. Biomedicines, 10(12), 3115. https://doi.org/10.3390/biomedicines10123115