Funding: the study was conducted under the state assignment АААА-А18-118053190012-9 (Development of assays for early diagnosis of breast and ovarian cancers based on the analysis of RNA circulating in the peripheral blood).
Acknowledgements: we thank the Center for Precision Genome Editing and Genetic Technologies for Biomedicine of Pirogov Russian National Medical Research University (Moscow, Russia) for their help in interpreting the data and analyzing some of the results.
Author contribution: Lolomadze EA — literature analysis and preparation of the manuscript draft; Kometova VV, Rodionov VV — editing and manuscript revision
Published online: 2020-06-30
Qiu J, Xu J, Zhang K, Gu W, Nie L. Refining Cancer Management Using Integrated Liquid Biopsy. Theranostics. 2020; 10 (5): 2374– 84. DOI: 10.7150/thno.40677.
Shen J, Kong W, Wu Y, Ren H, Wei J, Yang Y, et al. Plasma mRNA as liquid biopsy predicts chemo-sensitivity in advanced gastric cancer patients. J Cancer. 2017; 8 (3): 434–2. DOI: 10.7150/ jca.17369.
Perakis S, Speicher MR. Emerging concepts in liquid biopsies. BMC Med. 2017; 15 (1): 75.
Buder A, Tomuta C, Filipits M. The potential of liquid biopsies. Curr Opin Oncol. 2016; 28: 130–134.
Sozzi G, Conte D, Leon M, Ciricione R, Roz L, Ratcliffe C, et al. Quantification of free circulating DNA as a diagnostic marker in lung cancer. J Clin Oncol. 2003; 21: 3902–8.
Sozzi G, Musso K, Ratcliffe C, Goldstraw P, Pierotti MA, Pastorino U. Detection of microsatellite alterations in plasma DNA of non-small cell lung cancer patients: a prospect for early diagnosis. Clin Cancer Res. 1999. 5: 2689–92.
Egyud M, Sridhar P, Devaiah A, Yamada E, Saunders S, Ståhlberg A, et al. Plasma circulating tumor DNA as a potential tool for disease monitoring in head and neck cancer. Head Neck. 2019; 41 (5): 1351–8. DOI: 10.1002/hed.25563.
Kawakami K, Brabender J, Lord RV, Groshen S, Greenwald BD, Krasna MJ, et al. Hypermethylated APC DNA in plasma and prognosis of patients with esophageal adenocarcinoma. JNCI. 2000; 92 (22): 1805–11. Available from: https://doi.org/10.1093/ jnci/92.22.1805.
Shaw JA, Smith BA, Walsh T, Johnson S, Primrose L, Slade MJ. Microsatellite alterations plasma DNA of primary breast cancer patients. Clin Cancer Res. 2000; 6: 1119–24.
Kirk GD, Camus-Randon AM, Mendy M, Goedert JJ, Merle P, Trepo C, et al. Ser-249 p53 mutations in plasma DNA of patients with hepatocellular carcinoma from the Gambia. J Natl Cancer Inst (Bethesda). 2000; 92 (2): 148–53. DOI: 10.1093/jnci/92.2.148.
Koprenski MS, Benko FA, Borys DJ, Khan A, McGarrity TJ, Gocke C. D. Somatic mutation screening: identification of individuals harboring K-ras mutations with the use of plasma DNA. J Natl Cancer Inst (Bethesda). 2000; 92: 918–23.
Yamada T, Nakamori S, Ohzato H, Oshima S, Aoki T, Higaki N. Detection of K-ras gene mutations in plasma DNA of patients with pancreatic adenocarcinoma: correlation with clinicopathological features. Clin Cancer Res. 1998; 4: 1527–32.
Goessl C, Heicappell R, Muncher R, Anker P, Stroun M, Krause H, et al. Microsatellite analysis of plasma DNA from patients with clear cell renal carcinoma. Cancer Res. 1998; 58: 4728–32.
Bryzgunova OE, Laktionov PP. Current methods of extracellular DNA methylation analysis. Molecular Biology. 2017; 51 (2): 167– 83 DOI: 10.1134/S0026893317010071.
Zhong XY, Laivuori H, Livingston JC, Ylikorkala O, Sibai BM, Holzgreve W, et al. Elevation of both maternal and fetal extracellular circulating deoxyribonucleic acid concentrations in the plasma of pregnant women with preeclampsia. Am J Obstet Gynecol. 2001; 184 (3): 414–9. DOI: 10.1067/mob.2001.109594.
Zhong XY, Burk MR, Troeger C, Jackson LR, Holzgreve W, Hahn S. Fetal DNA in maternal plasma is elevated in pregnancies with aneuploid fetuses. Prenatal Diagn. 2000; 20 (10): 795–8.
Sekizawa A, Sugito Y, Iwasaki M, Watanabe A, Jimbo M, Hoshi S, et al. Cell-free fetal DNA is increased in plasma of women with hyperemesis gravidarum. Clin Chem. 2001; 47 (12): 2164–5.
Tong Y, Lo YM. Diagnostic developments involving cell-free (circulating) nucleic acids. Clin Chim Acta. 2006; 363: 187–96.
Pachot A, Blond J-L, Mougin B, Miossec P. Peptidylpropyl isomerase B (PPIB): a suitable reference gene for mRNA quantification in peripheral whole blood. Biotechnol. 2004; 114 (1–2): 121–4. DOI: 10.1016/j.jbiotec.2004.07.001.
Hasselmann DO, Rappl G, Rossler M, Ugurel S, Tilgen W, Reinhold U. Detection of tumor-associated circulating mRNA in serum, plasma and blood cells from patients with disseminated malignant melanoma. Oncol Rep. 2001; 8 (1): 115–8. DOI: 10.3892/or.8.1.115.
El-Hefnawy T, Raja S, Kelly L, Bigbee WL, Kirkwood JM, Luketich JD, et al. Characterization of amplifiable, circulating RNA in plasma and its potential as a tool for cancer diagnostics. Clin Chem. 2004; 50: 564–73. DOI: 10.1373/clinchem.2003.028506.
Novakovic S, Hocevar M, Zgajnar J, Besic N, Stegel V. Detection of telomerase RNA in the plasma of patients with breast cancer, malignant melanoma or thyroid cancer. Oncology Reports. 2004; 11 (1): 245–52. DOI: 10.3892/or.11.1.245.
Dasi F, Lledo S, Garcia-Granero E, Ripoll R, Marugan M, Tormo M, et al. Real-time quantification in plasma of human telomerase reverse transcriptase (hTERT) mRNA: a simple blood test to monitor disease in cancer patients. Lab Invest. 2001; 81 (5): 767– 9. DOI: 10.1038/ labinvest.3780285.
Silva JM, Dominguez G, Silva J, Garcia JM, Sanchez A, Rodriguez O, et al. Detection of epithelial messenger RNA in the plasma of breast cancer patients is associated with poor prognosis tumor characteristics. Clin Cancer Res. 2001; 7 (9): 2821–5.
Perhavec A, Cerkovnik P, Novakovic S, Zgajnar J. The hTERT mRNA in plasma samples of early breast cancer patients, non-cancer patients and healthy individuals. Neoplasma. 2008; 55: 549–54.
Lee G-W, Kim J-Y, Koh E-H, Kang D, Choi DS, Maeng K-Y, et al. Plasma human mammaglobin mRNA associated with poor outcome in patients with breast cancer. Genet Mol Res. 2012; 11 (4): 4034–42. DOI: 10.4238/2012.November.28.2.
Silva J, García V, García JM, Peña C, Domínguez G, Díaz R, et al. Circulating Bmi-1 mRNA as a possible prognostic factor for advanced breast cancer patients. Breast Cancer Research. 2007; 9: R55.
Zhang K, Luo Z, Zhang Y, Wang Y, Cui M, Liu L, et al. Detection and Analysis of circulating large intergenic non-coding RNA regulator of reprogramming in plasma for breast cancer. Thorac Cancer. 2018; 9 (1): 66–74. DOI: 10.1111/1759-7714.12537.
Wong SC, Lo SF, Cheung MT, Ng KO, Tse CW, Lai BS, et al. Quantification of plasma beta-catenin mRNA in colorectal cancer and adenoma patients. Clin Cancer Res. 2004; 10 (5): 1613–7.
Abdelghany AM, Rezk NS, Osman MM, Hamid AI, Al-Breedy AM, Abdelsattar HA. Using Lamin B1 mRNA for the early diagnosis of hepatocellular carcinoma: a cross-sectional diagnostic accuracy study. F1000Res. 2018; 7: 1339. DOI: 10.12688/ f1000research.14795.1.
Fu X, Shen C, Li G, Zhang X, Wen Z. Quantitative detection of plasma level of human telomerase reverse transcriptase mRNA in patients with nasopharyngeal carcinoma. Journal of Southern Medical University. 2015; 35 (6): 894–7.
Leng Q, Tsou J-H, Zhan M, Jiang F. Fucosylation Genes as Circulating Biomarkers for Lung Cancer. J Cancer Res Clin Oncol. 2018; 144 (11): 2109–15. DOI: 10.1007/s00432-018-2735-0.
Rainer TH, Lam NY, Tsui NB, Ng EK, Chiu RW, Joynt GM, et al. Effects of filtration on glyceraldehyde-3-phosphate dehydrogenase mRNA in the plasma of trauma patients and healthy individuals. Clin Chem. 2004; 50 (1): 206–8. DOI: 10.1373/ clinchem.2003.022533.
Atamaniuk J, Vidotto C, Tschan H, et al. Increased concentrations of cell-free plasma DNA after exhaustive exercise. Clin Chem. 2004; 50: 1668–70.
Hamaoui K, Butt A, Powrie J, Swaminathan R. Realtime quantitative PCR measurement of circulatory rhodopsin mRNA in healthy subjects and patients with diabetic retinopathy. Ann N Y Acad Sci. 2004; 1022: 152–6. DOI: 10.1196 / annals.1318.025.
Tsui NB, Chim SS, Chiu RW, Lau TK, Ng EK, Leung TN, et al. Systematic micro-array based identification of placental mRNA in maternal plasma: towards non-invasive prenatal gene expression profiling. J Med Genet. 2004; 41: 461–7. DOI: 10.1136/ jmg.2003.016881.
Hu X, Li D, Zhang W, Zhou J, Tang B, Li L. Matrix metalloproteinase-9 expression correlates with prognosis and involved in ovarian cancer cell invasion. Archives of Gynecology and Obstetrics. 2012; 286 (6): 1537–43. DOI: 10.1007/s00404-012-2456-6.
Galdiero F, Romano A, Pasquinelli R, Pignata S, Greggi S, Vuttariello E, et al. Detection of high mobility group A2 specific mRNA in the plasma of patients affected by epithelial ovarian cancer. Oncotarget. 2015; 6 (22): 19328–35. DOI: 10.18632/oncotarget.2896.
Deligezer U, Yaman F, Darendeliler E, Dizdar Y, Holdenrieder S, Kovancilar M, et al. Post-treatment circulating plasma BMP6 mRNA and H3K27 methylation levels discriminate metastatic prostate cancer from localized disease. Clinica Chimica Acta. 2010; 411 (19–20): 1452–6. DOI: 10.1016/j.cca.2010.05.040.
March-Villalba JA, Martínez-Jabaloyas JM, Herrero MJ, Santamaría J, Aliño SF, Dasí F. Plasma hTERT mRNA discriminates between clinically localized and locally advanced disease and is a predictor of recurrence in prostate cancer patients. Expert Opin Biol Ther. 2012; 12: 69–77. DOI: 10.1517/14712598.2012.685716.
Peinado H, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012; 18: 883–91.
Hoshino A, Costa-Silva B, Shen T-L, Rodrigues G, Hashimoto A, Mark MT, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015; 527 (7578): 329–35. DOI: 10.1038/ nature15756.
Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014; 30: 255–89. DOI: 10.1146/annurev-cellbio-101512-122326.
van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018; 19 (4): 213–28. DOI: 10.1038/nrm.2017.125.
Shah R, Patel T, Freedman JE. Circulating extracellular vesicles in human disease. N Engl J Med. 2018; 379 (10): 958–66. DOI: 10.1056/NEJMra1704286.
Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Na Cell Biol. 2007; 9 (6): 654–59. DOI: 10.1038/ncb1596.
Zhang J, Li S, Li L, Li M, Guo C, Yao J, Mi S. Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics. 2015; 13 (1): 17–24. DOI: 10.1016/j. gpb.2015.02.001.
Li Y, Zhao J, Yu S, Wang Z, He X, Su Y, et al. Extracellular Vesicles Long RNA Sequencing reveals abundant mRNA, circRNA, and lncRNA in human blood as potential biomarkers for cancer diagnosis. Clin Chem. 2019; 65 (6): 798–808. DOI: 10.1373/ clinchem.2018.301291.
Weber JA, Baxter DH, Zhang S, Huang DY, Huang KH, Lee MJ, et al. The microRNA spectrum in 12 body fluids. Clin Chem. 2010; 56 (11): 1733–41. DOI: 10.1373/clinchem.2010.147405.
Boon RA, Vickers KC. Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol. 2013; 33 (2): 186–92. DOI: 10.1161/ATVBAHA.112.300139.
Arroyo JD, Chevillet JR, Kroh EM, Ruf IK, Pritchard CC, Gibson DF, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci USA. 2011; 108 (12): 5003–8. DOI: 10.1073/ pnas.1019055108.
Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 2011; 13: 423– 33. DOI: 10.1038/ncb2210.
Van Eijndhoven MA, Zijlstra JM, Groenewegen NJ, Drees EE, van Niele S, Baglio SR, et al. Plasma vesicle miRNAs for therapy response monitoring in Hodgkin lymphoma patients. JCI Insight. 2016; 1 (19): e89631. DOI: 10.1172/jci.insight.89631.
Watahiki A, Macfarlane RJ, Gleave ME, Crea F, Wang Y, Helgason CD, et al. Plasma miRNAs as biomarkers to identify patients with castration-resistant metastatic prostate cancer. Int J Mol Sci. 2013; 14 (4): 7757–70. DOI: 10.3390/ijms14047757.
Shen W, Song M, Liu J, Qiu G, Li T, Hu Y, et al. MiR-26a Promotes Ovarian Cancer Proliferation and Tumorigenesis. PLoS One. 2014; 9 (1): e86871. DOI: 10.1371/journal.pone.0086871.
Cuk K, Zucknick M, Heil J, Madhavan D, Schott S, Turchinovich A, et al. Circulating microRNAs in plasma as early detection markers for breast cancer. International Journal of Cancer. 2013; 132 (7): 1602–12. Available from: https://DOI.org/10.1002/ijc.27799.
Ng EK, Li R, Shin VY, Jin HC, Leung CP, Ma ES, et al. Circulating microRNAs as specific biomarkers for breast cancer detection. PLoS One. 2013; 8 (1). DOI: 10.1371/journal.pone.0053141.
Müllauer L. Next generation sequencing: Clinical applications in solid tumours. Memo. 2017; 10 (4): 244–7. DOI: 10.1007/ s12254-017-0361-1.
Giuffrida MC, Spoto G. Integration of isothermal amplification methods in microfluidic devices: Recent advances. Biosens Bioelectron. 2017; 90: 174–86. DOI: 10.1016/j.bios.2016.11.045.
Giuffrida MC, Zanoli LM, D'Agata R, Finotti A, Gambari R, Spoto G. Isothermal circular-strand-displacement polymerization of DNA and microRNA in digital microfluidic devices. Anal Bioanal Chem. 2015; 407 (6): 1533–43. DOI: 10.1007/s00216-014-8405-4.
Alix-Panabieres C, Pantel K. Challenges in circulating tumour cell research. Nat Rev Cancer. 2014; 14 (9): 623–31. DOI: 10.1038/ nrc3820.