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miRNA Expression Assays

  • Cornelia Braicu
  • Diana Gulei
  • Beatriz de Melo Maia
  • Ioana Berindan-Neagoe
  • George A. CalinEmail author
Chapter

Abstract

MicroRNAs (miRNAs) are small noncoding RNAs able to modulate at transcriptional level the expression of their target genes. Deregulations in miRNA expression profiles have been associated with pathological phenotypes, a fact that promotes the possible evaluation of these sequences for diagnosis and prognosis and newly as therapeutic tools. In this sense, evaluation of miRNA expression has come to play an important role in the research field with the potential of translational relevance in the clinical area. In this chapter, we provide an overview of several of the most recently developed assays, methods, and technologies used to identify, characterize, and confirm miRNA expression in human pathologies. We also outline principal workflows for different preparations of biological samples, taking into account advantages and disadvantages of each approach. Furthermore, we discuss the diagnostic and therapeutic efficacy of miRNAs as well as their future roles in personalized medicine, from a technical perspective.

Keywords

ncRNAs miRNAs Microarray Next-generation sequencing In situ hybridization Cancer RT-PCR Personalized therapy Validation approach miRNA panels for diagnostic 

Notes

Acknowledgments

This work was supported by the Competitively Operational Program, 2014–2020, entitled “Clinical and economical impact of personalized targeted anti-microRNA therapies in reconverting lung cancer chemoresistance” (CANTEMIR), grant no. 35/01.09.2016, MySMIS-103375.

Dr. Calin is the Alan M. Gewirtz Leukemia & Lymphoma Society Scholar. He is supported as a fellow of the University of Texas MD Anderson Cancer Center Research Trust, as the University of Texas System Regents Research Scholar, and by the CLL Global Research Foundation. Work in Dr. Calin’s laboratory is supported in part by the National Institutes of Health/National Cancer Institute (CA135444); Department of Defense Breast Cancer Idea Award; Developmental Research Awards in Breast Cancer, Ovarian Cancer, Brain Cancer, Prostate Cancer, Multiple Myeloma, Leukemia (P50 CA100632), and Head and Neck (P50 CA097007) Specialized Program of Research Excellence grants; Sister Institution Network Fund grants in CLL and colon cancer; the Laura and John Arnold Foundation; the RGK Foundation; and the Estate of C. G. Johnson, Jr. This research is supported in part by the MD Anderson Cancer Center Support Grant CA016672.

References

  1. 1.
    Esteller M. Non-coding RNAs in human disease. Nat Rev Genet. 2011;12(12):861–74.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Enfield KSS, Pikor LA, Martinez VD, Lam WL. Mechanistic roles of noncoding RNAs in lung cancer biology and their clinical implications. Genet Res Int. 2012;2012:16.Google Scholar
  3. 3.
    Shah MY, Calin GA. The mix of two worlds: non-coding RNAs and hormones. Nucleic Acid Ther. 2013;23(1):2–8.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Redis RS, Calin S, Yang Y, You MJ, Calin GA. Cell-to-cell miRNA transfer: from body homeostasis to therapy. Pharmacol Ther. 2012;136(2):169–74.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998;391(6669):806–11.CrossRefGoogle Scholar
  6. 6.
    Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell. 2004;116(2):281–97.CrossRefGoogle Scholar
  7. 7.
    Negrini M, Nicoloso MS, Calin GA. MicroRNAs and cancer–new paradigms in molecular oncology. Curr Opin Cell Biol. 2009;21(3):470–9.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Eastlack S, Alahari S. MicroRNA and breast cancer: understanding pathogenesis, improving management. Non-Coding RNA. 2015;1(1):17.CrossRefPubMedPubMedCentralGoogle Scholar
  9. 9.
    Irimie AI, Braicu C, Cojocneanu-Petric R, Berindan-Neagoe I, Campian RS. Novel technologies for oral squamous carcinoma biomarkers in diagnostics and prognostics. Acta Odontol Scand. 2015;73(3):161–8.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet. 2012;13(5):358–69.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Berindan-Neagoe I, Monroig Pdel C, Pasculli B, Calin GA. MicroRNAome genome: a treasure for cancer diagnosis and therapy. CA Cancer J Clin. 2014;64(5):311–36.CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Braicu C, Catana C, Calin GA, Berindan-Neagoe I. NCRNA combined therapy as future treatment option for cancer. Curr Pharm Des. 2014;20(42):6565–74.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Catana CS, Calin GA, Berindan-Neagoe I. Inflamma-miRs in aging and breast cancer: are they reliable players? Front Med. 2015;2:85.CrossRefGoogle Scholar
  14. 14.
    Etheridge A, Lee I, Hood L, Galas D, Wang K. Extracellular microRNA: a new source of biomarkers. Mutat Res. 2011;717(1–2):85–90.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Krichevsky AM. MicroRNA profiling: from dark matter to white matter, or identifying new players in neurobiology. Sci World J. 2007;7:155–66.CrossRefGoogle Scholar
  16. 16.
    Berindan-Neagoe I, Calin GA. Molecular pathways: microRNAs, cancer cells, and microenvironment. Clin Cancer Res. 2014;20(24):6247–53.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Braicu C, Calin GA, Berindan-Neagoe I. MicroRNAs and cancer therapy – from bystanders to major players. Curr Med Chem. 2013;20(29):3561–73.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB, et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr Biol. 2007;17(15):1298–307.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Mendell JT, Olson EN. MicroRNAs in stress signaling and human disease. Cell. 2012;148(6):1172–87.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Shi XB, Xue L, Yang J, Ma AH, Zhao J, Xu M, Tepper CG, Evans CP, Kung HJ, deVere White RW. An androgen-regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc Natl Acad Sci U S A. 2007;104(50):19983–8.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Cao P, Deng Z, Wan M, Huang W, Cramer SD, Xu J, Lei M, Sui G. MicroRNA-101 negatively regulates Ezh2 and its expression is modulated by androgen receptor and HIF-1alpha/HIF-1beta. Mol Cancer. 2010;9:108.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, Sportoletti P, Varmeh S, Egia A, Fedele G, et al. Identification of the miR-106b~25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal. 2010;3(117):ra29.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Zaman MS, Thamminana S, Shahryari V, Chiyomaru T, Deng G, Saini S, Majid S, Fukuhara S, Chang I, Arora S, et al. Inhibition of PTEN gene expression by oncogenic miR-23b-3p in renal cancer. PLoS One. 2012;7(11):e50203.CrossRefPubMedPubMedCentralGoogle Scholar
  24. 24.
    Mlcochova H, Hezova R, Stanik M, Slaby O. Urine microRNAs as potential noninvasive biomarkers in urologic cancers. Urol Oncol. 2014;32(1):41.e41–9.CrossRefGoogle Scholar
  25. 25.
    Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, et al. Human microRNA genes are frequently located at fragile sites and genomic regions involved in cancers. Proc Natl Acad Sci U S A. 2004;101(9):2999–3004.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Yang BF, Lu YJ, Wang ZG. MicroRNA and disease associations. Clin Exp Pharmacol Physiol. 2009;36(10):951–60.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, et al. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A. 2002;99(24):15524–9.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Cimmino A, Calin GA, Fabbri M, Iorio MV, Ferracin M, Shimizu M, Wojcik SE, Aqeilan RI, Zupo S, Dono M, et al. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proc Natl Acad Sci U S A. 2005;102(39):13944–9.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Calin GA, Ferracin M, Cimmino A, Di Leva G, Shimizu M, Wojcik SE, Iorio MV, Visone R, Sever NI, Fabbri M, et al. A MicroRNA signature associated with prognosis and progression in chronic lymphocytic leukemia. N Engl J Med. 2005;353(17):1793–801.CrossRefPubMedPubMedCentralGoogle Scholar
  30. 30.
    Pekarsky Y, Santanam U, Cimmino A, Palamarchuk A, Efanov A, Maximov V, Volinia S, Alder H, Liu CG, Rassenti L, et al. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res. 2006;66(24):11590–3.CrossRefGoogle Scholar
  31. 31.
    Calin GA, Pekarsky Y, Croce CM. The role of microRNA and other non-coding RNA in the pathogenesis of chronic lymphocytic leukemia. Best Pract Res Clin Haematol. 2007;20(3):425–37.CrossRefGoogle Scholar
  32. 32.
    Rossi S, Shimizu M, Barbarotto E, Nicoloso MS, Dimitri F, Sampath D, Fabbri M, Lerner S, Barron LL, Rassenti LZ, et al. microRNA fingerprinting of CLL patients with chromosome 17p deletion identify a miR-21 score that stratifies early survival. Blood. 2010;116(6):945–52.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer. 2006;6(11):857–66.CrossRefGoogle Scholar
  34. 34.
    Wang JL, Hu Y, Kong X, Wang ZH, Chen HY, Xu J, Fang JY. Candidate microRNA biomarkers in human gastric cancer: a systematic review and validation study. PLoS One. 2013;8(9):e73683.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Wang Y, Li J, Tong L, Zhang J, Zhai A, Xu K, Wei L, Chu M. The prognostic value of miR-21 and miR-155 in non-small-cell lung cancer: a meta-analysis. Jpn J Clin Oncol. 2013;43(8):813–20.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Faruq O, Vecchione A. microRNA: diagnostic perspective. Front Med. 2015;2:51.CrossRefGoogle Scholar
  37. 37.
    Menendez P, Padilla D, Villarejo P, Palomino T, Nieto P, Menendez JM, Rodriguez-Montes JA. Prognostic implications of serum microRNA-21 in colorectal cancer. J Surg Oncol. 2013;108(6):369–73.CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Lee JA, Lee HY, Lee ES, Kim I, Bae JW. Prognostic implications of MicroRNA-21 overexpression in invasive ductal carcinomas of the breast. J Breast Cancer. 2011;14(4):269–75.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, Yoshida Y, Seto M. Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res. 2004;64(9):3087–95.CrossRefGoogle Scholar
  40. 40.
    Goblirsch M, Richtig G, Slaby O, Berindan-Neagoe I, Gerger A, Pichler M. MicroRNAs as a tool to aid stratification of colorectal cancer patients and to guide therapy. Pharmacogenomics. 2017;18(10):1027–38.CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Leichter AL, Sullivan MJ, Eccles MR, Chatterjee A. MicroRNA expression patterns and signalling pathways in the development and progression of childhood solid tumours. Mol Cancer. 2017;16:15.CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Chang CC, Yang YJ, Li YJ, Chen ST, Lin BR, Wu TS, Lin SK, Kuo MY, Tan CT. MicroRNA-17/20a functions to inhibit cell migration and can be used a prognostic marker in oral squamous cell carcinoma. Oral Oncol. 2013;49(9):923–31.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Gao X, Zhang R, Qu X, Zhao M, Zhang S, Wu H, Jianyong L, Chen L. MiR-15a, miR-16-1 and miR-17-92 cluster expression are linked to poor prognosis in multiple myeloma. Leuk Res. 2012;36(12):1505–9.CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Yu G, Tang JQ, Tian ML, Li H, Wang X, Wu T, Zhu J, Huang SJ, Wan YL. Prognostic values of the miR-17-92 cluster and its paralogs in colon cancer. J Surg Oncol. 2012;106(3):232–7.CrossRefGoogle Scholar
  45. 45.
    Butz H, Nofech-Mozes R, Ding Q, Khella HWZ, Szabo PM, Jewett M, Finelli A, Lee J, Ordon M, Stewart R, et al. Exosomal microRNAs are diagnostic biomarkers and can mediate cell-cell communication in renal cell carcinoma. Eur Urol Focus. 2016;2(2):210–8.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Hanke M, Hoefig K, Merz H, Feller AC, Kausch I, Jocham D, Warnecke JM, Sczakiel G. A robust methodology to study urine microRNA as tumor marker: microRNA-126 and microRNA-182 are related to urinary bladder cancer. Urol Oncol. 2010;28(6):655–61.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Van Roosbroeck K, Fanini F, Setoyama T, Ivan C, Rodriguez-Aguayo C, Fuentes-Mattei E, Xiao L, Vannini I, Redis RS, D'Abundo L, et al. Combining anti-miR-155 with chemotherapy for the treatment of lung cancers. Clin Cancer Res. 2017;23(11):2891–904.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Blower PE, Chung JH, Verducci JS, Lin S, Park JK, Dai Z, Liu CG, Schmittgen TD, Reinhold WC, Croce CM, et al. MicroRNAs modulate the chemosensitivity of tumor cells. Mol Cancer Ther. 2008;7(1):1–9.CrossRefGoogle Scholar
  49. 49.
    Kovalchuk O, Filkowski J, Meservy J, Ilnytskyy Y, Tryndyak VP, Chekhun VF, Pogribny IP. Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther. 2008;7(7):2152–9.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Xu K, Liang X, Shen K, Sun L, Cui D, Zhao Y, Tian J, Ni L, Liu J. MiR-222 modulates multidrug resistance in human colorectal carcinoma by down-regulating ADAM-17. Exp Cell Res. 2012;318(17):2168–77.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Zhong S, Li W, Chen Z, Xu J, Zhao J. MiR-222 and miR-29a contribute to the drug-resistance of breast cancer cells. Gene. 2013;531(1):8–14.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Yu PN, Yan MD, Lai HC, Huang RL, Chou YC, Lin WC, Yeh LT, Lin YW. Downregulation of miR-29 contributes to cisplatin resistance of ovarian cancer cells. Int J Cancer. 2014;134(3):542–51.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Chen Y, Ke G, Han D, Liang S, Yang G, Wu X. MicroRNA-181a enhances the chemoresistance of human cervical squamous cell carcinoma to cisplatin by targeting PRKCD. Exp Cell Res. 2014;320(1):12–20.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Ke G, Liang L, Yang JM, Huang X, Han D, Huang S, Zhao Y, Zha R, He X, Wu X. MiR-181a confers resistance of cervical cancer to radiation therapy through targeting the pro-apoptotic PRKCD gene. Oncogene. 2013;32(25):3019–27.CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Woyengo TA, Ramprasath VR, Jones PJ. Anticancer effects of phytosterols. Eur J Clin Nutr. 2009;63(7):813–20.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Yu X, Chen Y, Tian R, Li J, Li H, Lv T, Yao Q. miRNA-21 enhances chemoresistance to cisplatin in epithelial ovarian cancer by negatively regulating PTEN. Oncol Lett. 2017;14(2):1807–10.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Son JW. Year-in-review of lung cancer. Tuberc Respir Dis. 2012;73(3):137–42.CrossRefGoogle Scholar
  58. 58.
    Kita Y, Vincent K, Natsugoe S, Berindan-Neagoe I, Calin GA. Epigenetically regulated microRNAs and their prospect in cancer diagnosis. Expert Rev Mol Diagn. 2014;14(6):673–83.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Strmsek Z, Kunej T. MicroRNA silencing by DNA methylation in human cancer: a literature analysis. Non-Coding RNA. 2015;1(1):44.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Irimie AI, Ciocan C, Gulei D, Mehterov N, Atanasov AG, Dudea D, Berindan-Neagoe I. Current insights into oral cancer epigenetics. Int J Mol Sci. 2018;19(3):670.CrossRefGoogle Scholar
  61. 61.
    Wong KY, Yim RL, Kwong YL, Leung CY, Hui PK, Cheung F, Liang R, Jin DY, Chim CS. Epigenetic inactivation of the MIR129-2 in hematological malignancies. J Hematol Oncol. 2013;6:16.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Lu CY, Lin KY, Tien MT, Wu CT, Uen YH, Tseng TL. Frequent DNA methylation of MiR-129-2 and its potential clinical implication in hepatocellular carcinoma. Genes Chromosomes Cancer. 2013;52(7):636–43.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Fabbri M, Garzon R, Cimmino A, Liu Z, Zanesi N, Callegari E, Liu S, Alder H, Costinean S, Fernandez-Cymering C, et al. MicroRNA-29 family reverts aberrant methylation in lung cancer by targeting DNA methyltransferases 3A and 3B. Proc Natl Acad Sci U S A. 2007;104(40):15805–10.CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Chen H, Xu Z. Hypermethylation-associated silencing of miR-125a and miR-125b: a potential marker in colorectal cancer. Dis Markers. 2015;2015:345080.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Wang Z, Chang C, Peng M, Lu Q. Translating epigenetics into clinic: focus on lupus. Clin Epigenetics. 2017;9:78.CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Suzuki H, Maruyama R, Yamamoto E, Kai M. Epigenetic alteration and microRNA dysregulation in cancer. Front Genet. 2013;4:258.CrossRefPubMedPubMedCentralGoogle Scholar
  67. 67.
    Scott GK, Mattie MD, Berger CE, Benz SC, Benz CC. Rapid alteration of microRNA levels by histone deacetylase inhibition. Cancer Res. 2006;66(3):1277–81.CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Roccaro AM, Sacco A, Jia X, Azab AK, Maiso P, Ngo HT, Azab F, Runnels J, Quang P, Ghobrial IM. microRNA-dependent modulation of histone acetylation in Waldenström macroglobulinemia. Blood. 2010;116(9):1506–14.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Gong A-Y, Eischeid AN, Xiao J, Zhao J, Chen D, Wang Z-Y, Young CYF, Chen X-M. miR-17-5p targets the p300/CBP-associated factor and modulates androgen receptor transcriptional activity in cultured prostate cancer cells. BMC Cancer. 2012;12:492.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Sacco J, Adeli K. MicroRNAs: emerging roles in lipid and lipoprotein metabolism. Curr Opin Lipidol. 2012;23(3):220–5.CrossRefPubMedPubMedCentralGoogle Scholar
  71. 71.
    Romao JM, Jin W, Dodson MV, Hausman GJ, Moore SS, Guan LL. MicroRNA regulation in mammalian adipogenesis. Exp Biol Med (Maywood, NJ). 2011;236(9):997–1004.CrossRefGoogle Scholar
  72. 72.
    Ortega FJ, Mercader JM, Catalan V, Moreno-Navarrete JM, Pueyo N, Sabater M, Gomez-Ambrosi J, Anglada R, Fernandez-Formoso JA, Ricart W, et al. Targeting the circulating microRNA signature of obesity. Clin Chem. 2013;59(5):781–92.CrossRefGoogle Scholar
  73. 73.
    McGregor RA, Choi MS. microRNAs in the regulation of adipogenesis and obesity. Curr Mol Med. 2011;11(4):304–16.CrossRefPubMedPubMedCentralGoogle Scholar
  74. 74.
    Chen Z, Shi H, Sun S, Xu H, Cao D, Luo J. MicroRNA-181b suppresses TAG via target IRS2 and regulating multiple genes in the Hippo pathway. Exp Cell Res. 2016;348(1):66–74.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Chu B, Wu T, Miao L, Mei Y, Wu M. MiR-181a regulates lipid metabolism via IDH1. Sci Rep. 2015;5:8801.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    Li H, Chen X, Guan L, Qi Q, Shu G, Jiang Q, Yuan L, Xi Q, Zhang Y. MiRNA-181a regulates Adipogenesis by targeting tumor necrosis factor-α (TNF-α) in the porcine model. PLoS One. 2013;8(10):e71568.CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Ouyang D, Xu L, Zhang L, Guo D, Tan X, Yu X, Qi J, Ye Y, Liu Q, Ma Y, et al. MiR-181a-5p regulates 3T3-L1 cell adipogenesis by targeting Smad7 and Tcf7l2. Acta Biochim Biophys Sin. 2016;48(11):1034–41.CrossRefPubMedPubMedCentralGoogle Scholar
  78. 78.
    Ono K, Kuwabara Y, Han J. MicroRNAs and cardiovascular diseases. FEBS J. 2011;278(10):1619–33.CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Thum T, Catalucci D, Bauersachs J. MicroRNAs: novel regulators in cardiac development and disease. Cardiovasc Res. 2008;79(4):562–70.CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Care A, Catalucci D, Felicetti F, Bonci D, Addario A, Gallo P, Bang ML, Segnalini P, Gu Y, Dalton ND, et al. MicroRNA-133 controls cardiac hypertrophy. Nat Med. 2007;13(5):613–8.CrossRefGoogle Scholar
  81. 81.
    Yang B, Lin H, Xiao J, Lu Y, Luo X, Li B, Zhang Y, Xu C, Bai Y, Wang H, et al. The muscle-specific microRNA miR-1 regulates cardiac arrhythmogenic potential by targeting GJA1 and KCNJ2. Nat Med. 2007;13(4):486–91.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Oliveira-Carvalho V, da Silva MM, Guimaraes GV, Bacal F, Bocchi EA. MicroRNAs: new players in heart failure. Mol Biol Rep. 2013;40(3):2663–70.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Fichtlscherer S, Zeiher AM, Dimmeler S. Circulating microRNAs: biomarkers or mediators of cardiovascular diseases? Arterioscler Thromb Vasc Biol. 2011;31(11):2383–90.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Zhu J, Yao K, Wang Q, Guo J, Shi H, Ma L, Liu H, Gao W, Zou Y, Ge J. Circulating miR-181a as a potential novel biomarker for diagnosis of acute myocardial infarction. Cell Physiol Biochem. 2016;40(6):1591–602.CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Hu R, O’Connell RM. MicroRNA control in the development of systemic autoimmunity. Arthritis Res Ther. 2013;15(1):202.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Meisgen F, Xu N, Wei T, Janson PC, Obad S, Broom O, Nagy N, Kauppinen S, Kemeny L, Stahle M, et al. MiR-21 is up-regulated in psoriasis and suppresses T cell apoptosis. Exp Dermatol. 2012;21(4):312–4.CrossRefPubMedPubMedCentralGoogle Scholar
  87. 87.
    Mi QS, He HZ, Dong Z, Isales C, Zhou L. microRNA deficiency in pancreatic islet cells exacerbates streptozotocin-induced murine autoimmune diabetes. Cell Cycle. 2010;9(15):3127–9.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Yoshizawa JM, Wong DT. Salivary microRNAs and oral cancer detection. Methods Mol Biol (Clifton, NJ). 2013;936:313–24.CrossRefGoogle Scholar
  89. 89.
    Allegra A, Alonci A, Campo S, Penna G, Petrungaro A, Gerace D, Musolino C. Circulating microRNAs: new biomarkers in diagnosis, prognosis and treatment of cancer (review). Int J Oncol. 2012;41(6):1897–912.CrossRefPubMedPubMedCentralGoogle Scholar
  90. 90.
    Yanaihara N, Caplen N, Bowman E, Seike M, Kumamoto K, Yi M, Stephens RM, Okamoto A, Yokota J, Tanaka T, et al. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell. 2006;9(3):189–98.CrossRefGoogle Scholar
  91. 91.
    Li J, Smyth P, Flavin R, Cahill S, Denning K, Aherne S, Guenther SM, O’Leary JJ, Sheils O. Comparison of miRNA expression patterns using total RNA extracted from matched samples of formalin-fixed paraffin-embedded (FFPE) cells and snap frozen cells. BMC Biotechnol. 2007;7:36.CrossRefPubMedPubMedCentralGoogle Scholar
  92. 92.
    Liu A, Xu X. MicroRNA isolation from formalin-fixed, paraffin-embedded tissues. Methods Mol Biol (Clifton, NJ). 2011;724:259–67.CrossRefGoogle Scholar
  93. 93.
    Nelson PT, Wang WX, Wilfred BR, Tang G. Technical variables in high-throughput miRNA expression profiling: much work remains to be done. Biochim Biophys Acta. 2008;1779(11):758–65.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Mraz M, Malinova K, Mayer J, Pospisilova S. MicroRNA isolation and stability in stored RNA samples. Biochem Biophys Res Commun. 2009;390(1):1–4.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Wang K, Yuan Y, Cho JH, McClarty S, Baxter D, Galas DJ. Comparing the MicroRNA spectrum between serum and plasma. PLoS One. 2012;7(7):e41561.CrossRefPubMedPubMedCentralGoogle Scholar
  96. 96.
    Becker C, Hammerle-Fickinger A, Riedmaier I, Pfaffl MW. mRNA and microRNA quality control for RT-qPCR analysis. Methods (San Diego, Calif). 2010;50(4):237–43.CrossRefGoogle Scholar
  97. 97.
    Rio DC, Ares M Jr, Hannon GJ, Nilsen TW. Purification of RNA using TRIzol (TRI reagent). Cold Spring Harb Protoc. 2010;2010(6):pdb.prot5439.CrossRefPubMedPubMedCentralGoogle Scholar
  98. 98.
    Ach RA, Wang H, Curry B. Measuring microRNAs: comparisons of microarray and quantitative PCR measurements, and of different total RNA prep methods. BMC Biotechnol. 2008;8:69.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, et al. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem. 2009;55(4):611–22.CrossRefPubMedPubMedCentralGoogle Scholar
  100. 100.
    Kim YK, Yeo J, Kim B, Ha M, Kim VN. Short structured RNAs with low GC content are selectively lost during extraction from a small number of cells. Mol Cell. 2012;46(6):893–5.CrossRefPubMedPubMedCentralGoogle Scholar
  101. 101.
    Yoo CE, Kim G, Kim M, Park D, Kang HJ, Lee M, Huh N. A direct extraction method for microRNAs from exosomes captured by immunoaffinity beads. Anal Biochem. 2012;431(2):96–8.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Robin JD, Ludlow AT, LaRanger R, Wright WE, Shay JW. Comparison of DNA quantification methods for next generation sequencing. Sci Rep. 2016;6:24067.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Bravo V, Rosero S, Ricordi C, Pastori RL. Instability of miRNA and cDNAs derivatives in RNA preparations. Biochem Biophys Res Commun. 2007;353(4):1052–5.CrossRefPubMedPubMedCentralGoogle Scholar
  104. 104.
    Pop LA, Pileczki V, Cojocneanu-Petric RM, Petrut B, Braicu C, Jurj AM, Buiga R, Achimas-Cadariu P, Berindan-Neagoe I. Normalization of gene expression measurement of tissue samples obtained by transurethral resection of bladder tumors. OncoTargets Ther. 2016;9:3369–80.CrossRefGoogle Scholar
  105. 105.
    Kim SW, Li Z, Moore PS, Monaghan AP, Chang Y, Nichols M, John B. A sensitive non-radioactive northern blot method to detect small RNAs. Nucleic Acids Res. 2010;38(7):e98.CrossRefPubMedPubMedCentralGoogle Scholar
  106. 106.
    Wang B, Howel P, Bruheim S, Ju J, Owen LB, Fodstad O, Xi Y. Systematic evaluation of three microRNA profiling platforms: microarray, beads array, and quantitative real-time PCR array. PLoS One. 2011;6(2):e17167.CrossRefPubMedPubMedCentralGoogle Scholar
  107. 107.
    Vaz C, Ahmad HM, Sharma P, Gupta R, Kumar L, Kulshreshtha R, Bhattacharya A. Analysis of microRNA transcriptome by deep sequencing of small RNA libraries of peripheral blood. BMC Genomics. 2010;11:288.CrossRefPubMedPubMedCentralGoogle Scholar
  108. 108.
    Jensen SG, Lamy P, Rasmussen MH, Ostenfeld MS, Dyrskjot L, Orntoft TF, Andersen CL. Evaluation of two commercial global miRNA expression profiling platforms for detection of less abundant miRNAs. BMC Genomics. 2011;12:435.CrossRefPubMedPubMedCentralGoogle Scholar
  109. 109.
    Sablok G, Milev I, Minkov G, Minkov I, Varotto C, Yahubyan G, Baev V. isomiRex: web-based identification of microRNAs, isomiR variations and differential expression using next-generation sequencing datasets. FEBS Lett. 2013;587(16):2629–34.CrossRefPubMedPubMedCentralGoogle Scholar
  110. 110.
    Magee R, Telonis AG, Cherlin T, Rigoutsos I, Londin E. Assessment of isomiR discrimination using commercial qPCR methods. Non-Coding RNA. 2017;3(2):18.CrossRefPubMedPubMedCentralGoogle Scholar
  111. 111.
    Sempere LF, Freemantle S, Pitha-Rowe I, Moss E, Dmitrovsky E, Ambros V. Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 2004;5(3):R13.CrossRefPubMedPubMedCentralGoogle Scholar
  112. 112.
    Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75(5):843–54.CrossRefGoogle Scholar
  113. 113.
    Setoyama T, Ling H, Natsugoe S, Calin GA. Non-coding RNAs for medical practice in oncology. Keio J Med. 2011;60(4):106–13.CrossRefPubMedPubMedCentralGoogle Scholar
  114. 114.
    de Planell-Saguer M, Rodicio MC. Analytical aspects of microRNA in diagnostics: a review. Anal Chim Acta. 2011;699(2):134–52.CrossRefPubMedPubMedCentralGoogle Scholar
  115. 115.
    Schwarzkopf M, Pierce NA. Multiplexed miRNA northern blots via hybridization chain reaction. Nucleic Acids Res. 2016;44(15):e12.Google Scholar
  116. 116.
    Kumar P, Johnston BH, Kazakov SA. miR-ID: a novel, circularization-based platform for detection of microRNAs. RNA (New York, NY). 2011;17(2):365–80.CrossRefGoogle Scholar
  117. 117.
    Schmittgen TD, Jiang J, Liu Q, Yang L. A high-throughput method to monitor the expression of microRNA precursors. Nucleic Acids Res. 2004;32(4):e43.CrossRefPubMedPubMedCentralGoogle Scholar
  118. 118.
    Reichenstein I, Aizenberg N, Goshen M, Bentwich Z, Avni YS. A novel qPCR assay for viral encoded microRNAs. J Virol Methods. 2010;163(2):323–8.CrossRefPubMedPubMedCentralGoogle Scholar
  119. 119.
    Ro S, Park C, Jin J, Sanders KM, Yan W. A PCR-based method for detection and quantification of small RNAs. Biochem Biophys Res Commun. 2006;351(3):756–63.CrossRefPubMedPubMedCentralGoogle Scholar
  120. 120.
    Leung AK, Sharp PA. Function and localization of microRNAs in mammalian cells. Cold Spring Harb Symp Quant Biol. 2006;71:29–38.CrossRefPubMedPubMedCentralGoogle Scholar
  121. 121.
    Nass D, Rosenwald S, Meiri E, Gilad S, Tabibian-Keissar H, Schlosberg A, Kuker H, Sion-Vardy N, Tobar A, Kharenko O, et al. MiR-92b and miR-9/9* are specifically expressed in brain primary tumors and can be used to differentiate primary from metastatic brain tumors. Brain Pathol (Zurich, Switzerland). 2009;19(3):375–83.CrossRefGoogle Scholar
  122. 122.
    Bustos-Sanmamed P, Laffont C, Frugier F, Lelandais-Briere C, Crespi M. Analyzing small and long RNAs in plant development using non-radioactive in situ hybridization. Methods Mol Biol (Clifton, NJ). 2013;959:303–16.CrossRefGoogle Scholar
  123. 123.
    Obernosterer G, Leuschner PJ, Alenius M, Martinez J. Post-transcriptional regulation of microRNA expression. RNA (New York, NY). 2006;12(7):1161–7.CrossRefGoogle Scholar
  124. 124.
    Shi Z, Johnson JJ, Stack MS. Fluorescence in situ hybridization for MicroRNA detection in archived oral cancer tissues. J Oncol. 2012;2012:903581.CrossRefPubMedPubMedCentralGoogle Scholar
  125. 125.
    Yauk CL, Rowan-Carroll A, Stead JD, Williams A. Cross-platform analysis of global microRNA expression technologies. BMC Genomics. 2010;11:330.CrossRefPubMedPubMedCentralGoogle Scholar
  126. 126.
    Aldridge S, Hadfield J. Introduction to miRNA profiling technologies and cross-platform comparison. Methods Mol Biol (Clifton, NJ). 2012;822:19–31.CrossRefGoogle Scholar
  127. 127.
    Duttagupta R, DiRienzo S, Jiang R, Bowers J, Gollub J, Kao J, Kearney K, Rudolph D, Dawany NB, Showe MK, et al. Genome-wide maps of circulating miRNA biomarkers for ulcerative colitis. PLoS One. 2012;7(2):e31241.CrossRefPubMedPubMedCentralGoogle Scholar
  128. 128.
    Chen J, April CS, Fan JB. miRNA expression profiling using Illumina Universal BeadChips. Methods Mol Biol (Clifton, NJ). 2012;822:103–16.CrossRefGoogle Scholar
  129. 129.
    D’Andrade PN, Fulmer-Smentek S. Agilent microRNA microarray profiling system. Methods Mol Biol (Clifton, NJ). 2012;822:85–102.CrossRefGoogle Scholar
  130. 130.
    Benes V, Castoldi M. Expression profiling of microRNA using real-time quantitative PCR, how to use it and what is available. Methods (San Diego, Calif). 2010;50(4):244–9.CrossRefGoogle Scholar
  131. 131.
    Ono S, Lam S, Nagahara M, Hoon DSB. Circulating microRNA biomarkers as liquid biopsy for cancer patients: pros and cons of current assays. J Clin Med. 2015;4(10):1890–907.CrossRefPubMedPubMedCentralGoogle Scholar
  132. 132.
    M'Boutchou MN, van Kempen LC. Analysis of the tumor microenvironment transcriptome via NanoString mRNA and miRNA expression profiling. Methods Mol Biol (Clifton, NJ). 2016;1458:291–310.CrossRefGoogle Scholar
  133. 133.
    Tam S, de Borja R, Tsao M-S, McPherson JD. Robust global microRNA expression profiling using next-generation sequencing technologies. Lab Investig. 2014;94(3):350–8.CrossRefPubMedPubMedCentralGoogle Scholar
  134. 134.
    Wang H, Ach RA, Curry B. Direct and sensitive miRNA profiling from low-input total RNA. RNA (New York, NY). 2007;13(1):151–9.CrossRefGoogle Scholar
  135. 135.
    Liu J, Jennings SF, Tong W, Hong H. Next generation sequencing for profiling expression of miRNAs: technical progress and applications in drug development. J Biomed Sci Eng. 2011;4(10):666–76.CrossRefPubMedPubMedCentralGoogle Scholar
  136. 136.
    Yang Q, Lu J, Wang S, Li H, Ge Q, Lu Z. Application of next-generation sequencing technology to profile the circulating microRNAs in the serum of preeclampsia versus normal pregnant women. Clin Chim Acta. 2011;412(23–24):2167–73.CrossRefPubMedPubMedCentralGoogle Scholar
  137. 137.
    Schulte JH, Marschall T, Martin M, Rosenstiel P, Mestdagh P, Schlierf S, Thor T, Vandesompele J, Eggert A, Schreiber S, et al. Deep sequencing reveals differential expression of microRNAs in favorable versus unfavorable neuroblastoma. Nucleic Acids Res. 2010;38(17):5919–28.CrossRefPubMedPubMedCentralGoogle Scholar
  138. 138.
    Urgese G, Paciello G, Acquaviva A, Ficarra E. isomiR-SEA: an RNA-Seq analysis tool for miRNAs/isomiRs expression level profiling and miRNA-mRNA interaction sites evaluation. BMC Bioinform. 2016;17:148.CrossRefGoogle Scholar
  139. 139.
    Amsel D, Vilcinskas A, Billion A. Evaluation of high-throughput isomiR identification tools: illuminating the early isomiRome of Tribolium castaneum. BMC Bioinform. 2017;18(1):359.CrossRefGoogle Scholar
  140. 140.
    Zhang Y, Zang Q, Xu B, Zheng W, Ban R, Zhang H, Yang Y, Hao Q, Iqbal F, Li A, et al. IsomiR Bank: a research resource for tracking IsomiRs. Bioinformatics (Oxford, England). 2016;32(13):2069–71.CrossRefGoogle Scholar
  141. 141.
    Lu C, Meyers BC, Green PJ. Construction of small RNA cDNA libraries for deep sequencing. Methods (San Diego, Calif). 2007;43(2):110–7.CrossRefGoogle Scholar
  142. 142.
    Buermans HP, Ariyurek Y, van Ommen G, den Dunnen JT, t Hoen PA. New methods for next generation sequencing based microRNA expression profiling. BMC Genomics. 2010;11:716.CrossRefPubMedPubMedCentralGoogle Scholar
  143. 143.
    Wang WC, Lin FM, Chang WC, Lin KY, Huang HD, Lin NS. miRExpress: analyzing high-throughput sequencing data for profiling microRNA expression. BMC Bioinform. 2009;10:328.CrossRefGoogle Scholar
  144. 144.
    Moxon S, Schwach F, Dalmay T, Maclean D, Studholme DJ, Moulton V. A toolkit for analysing large-scale plant small RNA datasets. Bioinformatics (Oxford, England). 2008;24(19):2252–3.CrossRefGoogle Scholar
  145. 145.
    Bargaje R, Hariharan M, Scaria V, Pillai B. Consensus miRNA expression profiles derived from interplatform normalization of microarray data. RNA (New York, NY). 2010;16(1):16–25.CrossRefGoogle Scholar
  146. 146.
    Meyer SU, Pfaffl MW, Ulbrich SE. Normalization strategies for microRNA profiling experiments: a ‘normal’ way to a hidden layer of complexity? Biotechnol Lett. 2010;32(12):1777–88.CrossRefPubMedPubMedCentralGoogle Scholar
  147. 147.
    Deo A, Carlsson J, Lindlof A. How to choose a normalization strategy for miRNA quantitative real-time (qPCR) arrays. J Bioinforma Comput Biol. 2011;9(6):795–812.CrossRefGoogle Scholar
  148. 148.
    Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A. 2006;103(7):2257–61.CrossRefPubMedPubMedCentralGoogle Scholar
  149. 149.
  150. 150.
  151. 151.
    Liu CG, Calin GA, Meloon B, Gamliel N, Sevignani C, Ferracin M, Dumitru CD, Shimizu M, Zupo S, Dono M, et al. An oligonucleotide microchip for genome-wide microRNA profiling in human and mouse tissues. Proc Natl Acad Sci U S A. 2004;101(26):9740–4.CrossRefPubMedPubMedCentralGoogle Scholar
  152. 152.
    Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, et al. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 2005;65(16):7065–70.CrossRefPubMedPubMedCentralGoogle Scholar
  153. 153.
    Huang X, Liang M, Dittmar R, Wang L. Extracellular microRNAs in urologic malignancies: chances and challenges. Int J Mol Sci. 2013;14(7):14785–99.CrossRefPubMedPubMedCentralGoogle Scholar
  154. 154.
    Zhang L, Miller D, Yang Q, Wu B. MicroRNA regulatory networks as biomarkers in obesity: the emerging role. Methods Mol Biol (Clifton, NJ). 2017;1617:241–60.CrossRefGoogle Scholar
  155. 155.
    Mo YY. MicroRNA regulatory networks and human disease. Cell Mol Life Sci. 2012;69(21):3529–31.CrossRefPubMedPubMedCentralGoogle Scholar
  156. 156.
    Salmena L, Poliseno L, Tay Y, Kats L, Pandolfi PP. A ceRNA hypothesis: the Rosetta Stone of a hidden RNA language? Cell. 2011;146(3):353–8.CrossRefPubMedPubMedCentralGoogle Scholar
  157. 157.
    Irimie AI, Zimta AA, Ciocan C, Mehterov N, Dudea D, Braicu C, Berindan-Neagoe I. The unforeseen non-coding RNAs in head and neck cancer. Genes. 2018;9(3):134.CrossRefGoogle Scholar
  158. 158.
    Ojamaa K. Signaling mechanisms in thyroid hormone-induced cardiac hypertrophy. Vasc Pharmacol. 2010;52(3–4):113–9.CrossRefGoogle Scholar
  159. 159.
    Callis TE, Pandya K, Seok HY, Tang RH, Tatsuguchi M, Huang ZP, Chen JF, Deng Z, Gunn B, Shumate J, et al. MicroRNA-208a is a regulator of cardiac hypertrophy and conduction in mice. J Clin Invest. 2009;119(9):2772–86.CrossRefPubMedPubMedCentralGoogle Scholar
  160. 160.
    Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science (New York, NY). 2005;309(5740):1577–81.CrossRefGoogle Scholar
  161. 161.
    Yue J. miRNA and vascular cell movement. Adv Drug Deliv Rev. 2011;63(8):616–22.CrossRefPubMedPubMedCentralGoogle Scholar
  162. 162.
    Li W, Szoka FC Jr. Lipid-based nanoparticles for nucleic acid delivery. Pharm Res. 2007;24(3):438–49.CrossRefPubMedPubMedCentralGoogle Scholar
  163. 163.
    Han D, Li J, Wang H, Su X, Hou J, Gu Y, Qian C, Lin Y, Liu X, Huang M, et al. Circular RNA circMTO1 acts as the sponge of microRNA-9 to suppress hepatocellular carcinoma progression. Hepatology (Baltimore, Md). 2017;66:1151.CrossRefGoogle Scholar
  164. 164.
    Li JF, Song YZ. Circular RNA hsa_circ_0001564 facilitates tumorigenesis of osteosarcoma via sponging miR-29c-3p. Tumour Biol. 2017;39(8):1010428317709989.Google Scholar
  165. 165.
    Walther W, Stein U. Viral vectors for gene transfer: a review of their use in the treatment of human diseases. Drugs. 2000;60(2):249–71.CrossRefPubMedPubMedCentralGoogle Scholar
  166. 166.
    Al-Dosari MS, Gao X. Nonviral gene delivery: principle, limitations, and recent progress. AAPS J. 2009;11(4):671–81.CrossRefPubMedPubMedCentralGoogle Scholar
  167. 167.
    Geisler A, Fechner H. MicroRNA-regulated viral vectors for gene therapy. World J Exp Med. 2016;6(2):37–54.CrossRefPubMedPubMedCentralGoogle Scholar
  168. 168.
    Rai K, Takigawa N, Ito S, Kashihara H, Ichihara E, Yasuda T, Shimizu K, Tanimoto M, Kiura K. Liposomal delivery of MicroRNA-7-expressing plasmid overcomes epidermal growth factor receptor tyrosine kinase inhibitor-resistance in lung cancer cells. Mol Cancer Ther. 2011;10(9):1720–7.CrossRefPubMedPubMedCentralGoogle Scholar
  169. 169.
    Gondi CS, Rao JS. Concepts in in vivo siRNA delivery for cancer therapy. J Cell Physiol. 2009;220(2):285–91.CrossRefPubMedPubMedCentralGoogle Scholar
  170. 170.
    Lujambio A, Lowe SW. The microcosmos of cancer. Nature. 2012;482(7385):347–55.CrossRefPubMedPubMedCentralGoogle Scholar
  171. 171.
    Ferracin M, Zagatti B, Rizzotto L, Cavazzini F, Veronese A, Ciccone M, Saccenti E, Lupini L, Grilli A, De Angeli C, et al. MicroRNAs involvement in fludarabine refractory chronic lymphocytic leukemia. Mol Cancer. 2010;9:123.CrossRefPubMedPubMedCentralGoogle Scholar
  172. 172.
    Ru P, Steele R, Newhall P, Phillips NJ, Toth K, Ray RB. miRNA-29b suppresses prostate cancer metastasis by regulating epithelial-mesenchymal transition signaling. Mol Cancer Ther. 2012;11(5):1166–73.CrossRefPubMedPubMedCentralGoogle Scholar
  173. 173.
    Kandalam MM, Beta M, Maheswari UK, Swaminathan S, Krishnakumar S. Oncogenic microRNA 17-92 cluster is regulated by epithelial cell adhesion molecule and could be a potential therapeutic target in retinoblastoma. Mol Vis. 2012;18:2279–87.PubMedPubMedCentralGoogle Scholar
  174. 174.
    Fassina A, Marino F, Siri M, Zambello R, Ventura L, Fassan M, Simonato F, Cappellesso R. The miR-17-92 microRNA cluster: a novel diagnostic tool in large B-cell malignancies. Lab Invest. 2012;92(11):1574–82.CrossRefPubMedPubMedCentralGoogle Scholar
  175. 175.
    Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, Sweet-Cordero A, Ebert BL, Mak RH, Ferrando AA, et al. MicroRNA expression profiles classify human cancers. Nature. 2005;435(7043):834–8.CrossRefGoogle Scholar
  176. 176.
    Slabakova E, Culig Z, Remsik J, Soucek K. Alternative mechanisms of miR-34a regulation in cancer. Cell Death Dis. 2017;8(10):e3100.CrossRefPubMedPubMedCentralGoogle Scholar
  177. 177.
    Zeng Y, Xu Y, Shu R, Sun L, Tian Y, Shi C, Zheng Z, Wang K, Luo H. Altered expression profiles of circular RNA in colorectal cancer tissues from patients with lung metastasis. Int J Mol Med. 2017;40(6):1818–28.PubMedPubMedCentralGoogle Scholar
  178. 178.
    Cao Q, Mani RS, Ateeq B, Dhanasekaran SM, Asangani IA, Prensner JR, Kim JH, Brenner JC, Jing X, Cao X, et al. Coordinated regulation of polycomb group complexes through microRNAs in cancer. Cancer Cell. 2011;20(2):187–99.CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2019

Authors and Affiliations

  • Cornelia Braicu
    • 1
  • Diana Gulei
    • 2
    • 3
  • Beatriz de Melo Maia
    • 4
  • Ioana Berindan-Neagoe
    • 1
    • 2
    • 5
  • George A. Calin
    • 3
    • 6
    Email author
  1. 1.Research Center for Functional Genomics, Biomedicine and Translational Medicine,Iuliu Hatieganu University of Medicine and PharmacyCluj-NapocaRomania
  2. 2.Medfuture Research Center for Advanced Medicine, Iuliu Hatieganu University of Medicine and PharmacyCluj-NapocaRomania
  3. 3.Department of Experimental TherapeuticsThe University of Texas MD Anderson Cancer CenterHoustonUSA
  4. 4.Research and DevelopmentPHD Laboratory – Surgical and Molecular PathologySão PauloBrazil
  5. 5.Department of Functional Genomics and Experimental PathologyThe Oncology Institute “Prof. Dr. Ion Chiricuta”Cluj-NapocaRomania
  6. 6.Center for RNA Interference and Non-Coding RNAs, The University of Texas MD Anderson Cancer CenterHoustonUSA

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