The itinerary of circulating miRNAs – implications for cancer progression and diagnosis
DOI:
https://doi.org/10.20883/medical.e516Keywords:
microRNA, cancer, tumour microenvironment, exosomes, biomarkerAbstract
microRNAs (miRNAs) are non-coding RNAs that regulate gene expression and protect cells from foreign nucleic acids. miRNA is produced in the nucleus and processed in the cytoplasm. These small nucleic acid molecules are released from cells to the extracellular matrix (extracellular miRNA, ex-miRNA) and reach blood plasma (circulating miRNA). Circulating miRNA can also be detected in other biological fluids, such as saliva, cerebrospinal fluid or urine, and it is usually carried by proteins or extracellular vesicles. Argonaute-miRNA, or miRNA-lipoprotein complex, protect miRNA from being degraded. The entrance of extracellular miRNA into a target cell is mediated by endocytosis and membrane fusion of extracellular vesicles. Additionally, miRNA can also be delivered in high-density lipoproteins by means of interactions with scavenger receptors. miRNAs absorbed into a cell can act as tumour promoters (oncomirs), or suppressors by inhibiting the translation process of the target mRNAs, thus, affecting cells in the tumour microenvironment. miRNA can impact other cells by supporting tumour growth, promoting angiogenesis and modulating the immune system. Molecular high-throughput methods are employed to detect circulating miRNA, and a potentially helpful diagnostic test has been designed to characterise the cancer type. In this review, we aim to summarise the itinerary of miRNAs from a source cell to a target cell, as well as to show how this class of small nucleic acids participates in intercellular communication. Finally, we highlight examples of miRNAs usage as potential molecular markers and discuss treatment approaches in clinical trials.
Downloads
References
O'Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO. RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol. 2020 21(10): 585-606. PMID: 32457507.
Bartel DP. Metazoan MicroRNAs. Cell. 2018 173(1): 20-51. PMID: 29570994.
Thery C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD, Andriantsitohaina R, Antoniou A, Arab T, Archer F, Atkin-Smith GK, Ayre DC, Bach JM, Bachurski D, Baharvand H, Balaj L, Baldacchino S, Bauer NN, Baxter AA, Bebawy M, Beckham C, Bedina Zavec A, Benmoussa A, Berardi AC, Bergese P, Bielska E, Blenkiron C, Bobis-Wozowicz S, Boilard E, Boireau W, Bongiovanni A, BorrĂ s FE, Bosch S, Boulanger CM, Breakefield X, Breglio AM, Brennan M, Brigstock DR, Brisson A, Broekman ML, Bromberg JF, Bryl-GĂłrecka P, Buch S, Buck AH, Burger D, Busatto S, Buschmann D, Bussolati B, Buzás EI, Byrd JB, Camussi G, Carter DR, Caruso S, Chamley LW, Chang YT, Chen C, Chen S, Cheng L, Chin AR, Clayton A, Clerici SP, Cocks A, Cocucci E, Coffey RJ, Cordeiro-da-Silva A, Couch Y, Coumans FA, Coyle B, Crescitelli R, Criado MF, D'Souza-Schorey C, Das S, Datta Chaudhuri A, de Candia P, De Santana EF, De Wever O, Del Portillo HA, Demaret T, Deville S, Devitt A, Dhondt B, Di Vizio D, Dieterich LC, Dolo V, Dominguez Rubio AP, Dominici M, Dourado MR, Driedonks TA, Duarte FV, Duncan HM, Eichenberger RM, Ekström K, El Andaloussi S, Elie-Caille C, ErdbrĂĽgger U, FalcĂłn-PĂ©rez JM, Fatima F, Fish JE, Flores-Bellver M, Försönits A, Frelet-Barrand A, Fricke F, Fuhrmann G, Gabrielsson S, Gámez-Valero A, Gardiner C, Gärtner K, Gaudin R, Gho YS, Giebel B, Gilbert C, Gimona M, Giusti I, Goberdhan DC, Görgens A, Gorski SM, Greening DW, Gross JC, Gualerzi A, Gupta GN, Gustafson D, Handberg A, Haraszti RA, Harrison P, Hegyesi H, Hendrix A, Hill AF, Hochberg FH, Hoffmann KF, Holder B, Holthofer H, Hosseinkhani B, Hu G, Huang Y, Huber V, Hunt S, Ibrahim AG, Ikezu T, Inal JM, Isin M, Ivanova A, Jackson HK, Jacobsen S, Jay SM, Jayachandran M, Jenster G, Jiang L, Johnson SM, Jones JC, Jong A, Jovanovic-Talisman T, Jung S, Kalluri R, Kano SI, Kaur S, Kawamura Y, Keller ET, Khamari D, Khomyakova E, Khvorova A, Kierulf P, Kim KP, Kislinger T, Klingeborn M, Klinke DJ, 2nd, Kornek M, Kosanović MM, Kovács Ă F, Krämer-Albers EM, Krasemann S, Krause M, Kurochkin IV, Kusuma GD, Kuypers S, Laitinen S, Langevin SM, Languino LR, Lannigan J, Lässer C, Laurent LC, Lavieu G, Lázaro-Ibáñez E, Le Lay S, Lee MS, Lee YXF, Lemos DS, Lenassi M, Leszczynska A, Li IT, Liao K, Libregts SF, Ligeti E, Lim R, Lim SK, LinÄ“ A, Linnemannstöns K, Llorente A, Lombard CA, Lorenowicz MJ, Lörincz Ă M, Lötvall J, Lovett J, Lowry MC, Loyer X, Lu Q, Lukomska B, Lunavat TR, Maas SL, Malhi H, Marcilla A, Mariani J, Mariscal J, Martens-Uzunova ES, Martin-Jaular L, Martinez MC, Martins VR, Mathieu M, Mathivanan S, Maugeri M, McGinnis LK, McVey MJ, Meckes DG, Jr., Meehan KL, Mertens I, Minciacchi VR, Möller A, Møller Jørgensen M, Morales-Kastresana A, Morhayim J, Mullier F, Muraca M, Musante L, Mussack V, Muth DC, Myburgh KH, Najrana T, Nawaz M, Nazarenko I, Nejsum P, Neri C, Neri T, Nieuwland R, Nimrichter L, Nolan JP, Nolte-'t Hoen EN, Noren Hooten N, O'Driscoll L, O'Grady T, O'Loghlen A, Ochiya T, Olivier M, Ortiz A, Ortiz LA, Osteikoetxea X, Ăstergaard O, Ostrowski M, Park J, Pegtel DM, Peinado H, Perut F, Pfaffl MW, Phinney DG, Pieters BC, Pink RC, Pisetsky DS, Pogge von Strandmann E, Polakovicova I, Poon IK, Powell BH, Prada I, Pulliam L, Quesenberry P, Radeghieri A, Raffai RL, Raimondo S, Rak J, Ramirez MI, Raposo G, Rayyan MS, Regev-Rudzki N, Ricklefs FL, Robbins PD, Roberts DD, Rodrigues SC, Rohde E, Rome S, Rouschop KM, Rughetti A, Russell AE, Saá P, Sahoo S, Salas-Huenuleo E, Sánchez C, Saugstad JA, Saul MJ, Schiffelers RM, Schneider R, Schøyen TH, Scott A, Shahaj E, Sharma S, Shatnyeva O, Shekari F, Shelke GV, Shetty AK, Shiba K, Siljander PR, Silva AM, Skowronek A, Snyder OL, 2nd, Soares RP, SĂłdar BW, Soekmadji C, Sotillo J, Stahl PD, Stoorvogel W, Stott SL, Strasser EF, Swift S, Tahara H, Tewari M, Timms K, Tiwari S, Tixeira R, Tkach M, Toh WS, Tomasini R, Torrecilhas AC, Tosar JP, Toxavidis V, Urbanelli L, Vader P, van Balkom BW, van der Grein SG, Van Deun J, van Herwijnen MJ, Van Keuren-Jensen K, van Niel G, van Royen ME, van Wijnen AJ, Vasconcelos MH, Vechetti IJ, Jr., Veit TD, Vella LJ, Velot Ă, Verweij FJ, Vestad B, Viñas JL, Visnovitz T, Vukman KV, Wahlgren J, Watson DC, Wauben MH, Weaver A, Webber JP, Weber V, Wehman AM, Weiss DJ, Welsh JA, Wendt S, Wheelock AM, Wiener Z, Witte L, Wolfram J, Xagorari A, Xander P, Xu J, Yan X, Yáñez-MĂł M, Yin H, Yuana Y, Zappulli V, Zarubova J, Žėkas V, Zhang JY, Zhao Z, Zheng L, Zheutlin AR, Zickler AM, Zimmermann P, Zivkovic AM, Zocco D, Zuba-Surma EK. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018 7(1): 1535750. PMID: 30637094.
Baj-Krzyworzeka M, Szatanek R, Weglarczyk K, Baran J, Urbanowicz B, Brański P, Ratajczak MZ, Zembala M. Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol Immunother. 2006 55(7): 808-18. PMID: 16283305.
Santangelo L, Giurato G, Cicchini C, Montaldo C, Mancone C, Tarallo R, Battistelli C, Alonzi T, Weisz A, Tripodi M. The RNA-Binding Protein SYNCRIP Is a Component of the Hepatocyte Exosomal Machinery Controlling MicroRNA Sorting. Cell Rep. 2016 17(3): 799-808. PMID: 27732855.
Temoche-Diaz MM, Shurtleff MJ, Nottingham RM, Yao J, Fadadu RP, Lambowitz AM, Schekman R. Distinct mechanisms of microRNA sorting into cancer cell-derived extracellular vesicle subtypes. Elife. 2019 8. PMID: 31436530.
Wei H, Chen Q, Lin L, Sha C, Li T, Liu Y, Yin X, Xu Y, Chen L, Gao W, Li Y, Zhu X. Regulation of exosome production and cargo sorting. Int J Biol Sci. 2021 17(1): 163-177. PMID: 33390841.
Perez-Boza J, Lion M, Struman I. Exploring the RNA landscape of endothelial exosomes. Rna. 2018 24(3): 423-435. PMID: 29282313.
Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, Martinez-Herrera DJ, Pascual-Montano A, Mittelbrunn M, Sanchez-Madrid F. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013 4: 2980. PMID: 24356509.
Xu YF, Hannafon BN, Khatri U, Gin A, Ding WQ. The origin of exosomal miR-1246 in human cancer cells. RNA Biol. 2019 16(6): 770-784. PMID: 30806147.
Boon RA, Vickers KC. Intercellular transport of microRNAs. Arterioscler Thromb Vasc Biol. 2013 33(2): 186-92. PMID: 23325475.
Rayner KJ, Hennessy EJ. Extracellular communication via microRNA: lipid particles have a new message. J Lipid Res. 2013 54(5): 1174-81. PMID: 23505318.
Liu H, Fu Y, Jiang D, Li G, Xie J, Cheng J, Peng Y, Ghabrial SA, Yi X. Widespread horizontal gene transfer from double-stranded RNA viruses to eukaryotic nuclear genomes. J Virol. 2010 84(22): 11876-87. PMID: 20810725.
Han L, Luan YS. Horizontal Transfer of Small RNAs to and from Plants. Front Plant Sci. 2015 6: 1113. PMID: 26697056.
Max KEA, Bertram K, Akat KM, Bogardus KA, Li J, Morozov P, Ben-Dov IZ, Li X, Weiss ZR, Azizian A, Sopeyin A, Diacovo TG, Adamidi C, Williams Z, Tuschl T. Human plasma and serum extracellular small RNA reference profiles and their clinical utility. Proc Natl Acad Sci U S A. 2018 115(23): E5334-E5343. PMID: 29777089.
Pritchard CC, Kroh E, Wood B, Arroyo JD, Dougherty KJ, Miyaji MM, Tait JF, Tewari M. Blood cell origin of circulating microRNAs: a cautionary note for cancer biomarker studies. Cancer Prev Res (Phila). 2012 5(3): 492-497. PMID: 22158052.
Han X, Wang X. Opportunities and Challenges in Tunneling Nanotubes Research: How Far from Clinical Application? Int J Mol Sci. 2021 22(5). PMID: 33669068.
Turchinovich A, Weiz L, Langheinz A, Burwinkel B. Characterization of extracellular circulating microRNA. Nucleic Acids Res. 2011 39(16): 7223-33. PMID: 21609964.
Wang K, Zhang S, Weber J, Baxter D, Galas DJ. Export of microRNAs and microRNA-protective protein by mammalian cells. Nucleic Acids Res. 2010 38(20): 7248-59. PMID: 20615901.
Sapp RM, Shill DD, Roth SM, Hagberg JM. Circulating microRNAs in acute and chronic exercise: more than mere biomarkers. J Appl Physiol (1985). 2017 122(3): 702-717. PMID: 28035018.
Zhu H, Xue C, Xu X, Guo Y, Li X, Lu J, Ju S, Wang Y, Cao Z, Gu X. Rab8a/Rab11a regulate intercellular communications between neural cells via tunneling nanotubes. Cell Death Dis. 2016 7(12): e2523. PMID: 28005071.
Beckmann A, Hainz N, Tschernig T, Meier C. Facets of Communication: Gap Junction Ultrastructure and Function in Cancer Stem Cells and Tumor Cells. Cancers (Basel). 2019 11(3). PMID: 30823688.
Bhat SA, Majid S, Hassan T. MicroRNAs and its emerging role as breast cancer diagnostic marker - A review. Adv Biomark Sci Technol. 2019 1: 1-8. PMID:
Li M, Zeringer E, Barta T, Schageman J, Cheng A, Vlassov AV. Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers. Philos Trans R Soc Lond B Biol Sci. 2014 369(1652). PMID: 25135963.
Bosson AD, Zamudio JR, Sharp PA. Endogenous miRNA and target concentrations determine susceptibility to potential ceRNA competition. Mol Cell. 2014 56(3): 347-59. PMID: 25449132.
Janas T, Janas MM, Sapoń K, Janas T. Mechanisms of RNA loading into exosomes. FEBS Lett. 2015 589(13): 1391-8. PMID: 25937124.
Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009 11(9): 1143-9. PMID: 19684575.
Wagner J, Riwanto M, Besler C, Knau A, Fichtlscherer S, Röxe T, Zeiher AM, Landmesser U, Dimmeler S. Characterization of levels and cellular transfer of circulating lipoprotein-bound microRNAs. Arterioscler Thromb Vasc Biol. 2013 33(6): 1392-400. PMID: 23559634.
Dragomir M, Chen B, Calin GA. Exosomal lncRNAs as new players in cell-to-cell communication. Transl Cancer Res. 2018 7(Suppl 2): S243-S252. PMID: 30148073.
Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, Sun Q, Wang K, Ba Y, Wang Q, Wang D, Yang J, Liu P, Xu T, Yan Q, Zhang J, Zen K, Zhang CY. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell. 2010 39(1): 133-44. PMID: 20603081.
Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, BorrĂ s FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, Colás E, Cordeiro-da Silva A, Fais S, Falcon-Perez JM, Ghobrial IM, Giebel B, Gimona M, Graner M, Gursel I, Gursel M, Heegaard NH, Hendrix A, Kierulf P, Kokubun K, Kosanovic M, Kralj-Iglic V, Krämer-Albers EM, Laitinen S, Lässer C, Lener T, Ligeti E, LinÄ“ A, Lipps G, Llorente A, Lötvall J, ManÄŤek-Keber M, Marcilla A, Mittelbrunn M, Nazarenko I, Nolte-'t Hoen EN, Nyman TA, O'Driscoll L, Olivan M, Oliveira C, Pállinger Ă, Del Portillo HA, ReventĂłs J, Rigau M, Rohde E, Sammar M, Sánchez-Madrid F, SantarĂ©m N, Schallmoser K, Ostenfeld MS, Stoorvogel W, Stukelj R, Van der Grein SG, Vasconcelos MH, Wauben MH, De Wever O. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015 4: 27066. PMID: 25979354.
Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, Coscia C, Iessi E, Logozzi M, Molinari A, Colone M, Tatti M, Sargiacomo M, Fais S. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 2009 284(49): 34211-22. PMID: 19801663.
Pardini B, Calin GA. MicroRNAs and Long Non-Coding RNAs and Their Hormone-Like Activities in Cancer. Cancers (Basel). 2019 11(3). PMID: 30884898.
Fabbri M. MicroRNAs and miRceptors: a new mechanism of action for intercellular communication. Philos Trans R Soc Lond B Biol Sci. 2018 373(1737). PMID: 29158315.
Josson S, Gururajan M, Sung SY, Hu P, Shao C, Zhau HE, Liu C, Lichterman J, Duan P, Li Q, Rogatko A, Posadas EM, Haga CL, Chung LW. Stromal fibroblast-derived miR-409 promotes epithelial-to-mesenchymal transition and prostate tumorigenesis. Oncogene. 2015 34(21): 2690-9. PMID: 25065597.
Kroiss A, Vincent S, Decaussin-Petrucci M, Meugnier E, Viallet J, Ruffion A, Chalmel F, Samarut J, Allioli N. Androgen-regulated microRNA-135a decreases prostate cancer cell migration and invasion through downregulating ROCK1 and ROCK2. Oncogene. 2015 34(22): 2846-55. PMID: 25065599.
Liu Q, Peng F, Chen J. The Role of Exosomal MicroRNAs in the Tumor Microenvironment of Breast Cancer. Int J Mol Sci. 2019 20(16). PMID: 31395836.
Puppo M, Valluru MK, Clézardin P. MicroRNAs and Their Roles in Breast Cancer Bone Metastasis. Curr Osteoporos Rep. 2021. PMID: 33830428.
Zhou W, Fong MY, Min Y, Somlo G, Liu L, Palomares MR, Yu Y, Chow A, O'Connor ST, Chin AR, Yen Y, Wang Y, Marcusson EG, Chu P, Wu J, Wu X, Li AX, Li Z, Gao H, Ren X, Boldin MP, Lin PC, Wang SE. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell. 2014 25(4): 501-15. PMID: 24735924.
Di Modica M, Regondi V, Sandri M, Iorio MV, Zanetti A, Tagliabue E, Casalini P, Triulzi T. Breast cancer-secreted miR-939 downregulates VE-cadherin and destroys the barrier function of endothelial monolayers. Cancer Lett. 2017 384: 94-100. PMID: 27693459.
Bayraktar R, Van Roosbroeck K, Calin GA. Cell-to-cell communication: microRNAs as hormones. Mol Oncol. 2017 11(12): 1673-1686. PMID: 29024380.
Arkhypov I, Lasser S, Petrova V, Weber R, Groth C, Utikal J, Altevogt P, Umansky V. Myeloid Cell Modulation by Tumor-Derived Extracellular Vesicles. Int J Mol Sci. 2020 21(17). PMID: 32878277.
Omar HA, El-Serafi AT, Hersi F, Arafa EA, Zaher DM, Madkour M, Arab HH, Tolba MF. Immunomodulatory MicroRNAs in cancer: targeting immune checkpoints and the tumor microenvironment. Febs J. 2019 286(18): 3540-3557. PMID: 31306553.
Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ, Zanesi N, Crawford M, Ozer GH, Wernicke D, Alder H, Caligiuri MA, Nana-Sinkam P, Perrotti D, Croce CM. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A. 2012 109(31): E2110-6. PMID: 22753494.
Zhou M, Chen J, Zhou L, Chen W, Ding G, Cao L. Pancreatic cancer derived exosomes regulate the expression of TLR4 in dendritic cells via miR-203. Cell Immunol. 2014 292(1-2): 65-9. PMID: 25290620.
Ding G, Zhou L, Qian Y, Fu M, Chen J, Chen J, Xiang J, Wu Z, Jiang G, Cao L. Pancreatic cancer-derived exosomes transfer miRNAs to dendritic cells and inhibit RFXAP expression via miR-212-3p. Oncotarget. 2015 6(30): 29877-88. PMID: 26337469.
Si W, Shen J, Zheng H, Fan W. The role and mechanisms of action of microRNAs in cancer drug resistance. Clin Epigenetics. 2019 11(1): 25. PMID: 30744689.
Ma Y, Li X, Cheng S, Wei W, Li Y. MicroRNA-106a confers cisplatin resistance in non-small cell lung cancer A549 cells by targeting adenosine triphosphatase-binding cassette A1. Mol Med Rep. 2015 11(1): 625-32. PMID: 25339370.
Zhao Z, Zhang L, Yao Q, Tao Z. miR-15b regulates cisplatin resistance and metastasis by targeting PEBP4 in human lung adenocarcinoma cells. Cancer Gene Ther. 2015 22(3): 108-14. PMID: 25721211.
Shang J, Yang F, Wang Y, Wang Y, Xue G, Mei Q, Wang F, Sun S. MicroRNA-23a antisense enhances 5-fluorouracil chemosensitivity through APAF-1/caspase-9 apoptotic pathway in colorectal cancer cells. J Cell Biochem. 2014 115(4): 772-84. PMID: 24249161.
Yoshida K, Yokoi A, Kato T, Ochiya T, Yamamoto Y. The clinical impact of intra- and extracellular miRNAs in ovarian cancer. Cancer Sci. 2020 111(10): 3435-3444. PMID: 32750177.
Gajos-Michniewicz A, Czyz M. Role of miRNAs in Melanoma Metastasis. Cancers (Basel). 2020 11(3). PMID: 30866509.
Mowla M, Hashemi A. Functional roles of exosomal miRNAs in multi-drug resistance in cancer chemotherapeutics. Exp Mol Pathol. 2021 118: 104592. PMID: 33296693.
Goossens N, Nakagawa S, Sun X, Hoshida Y. Cancer biomarker discovery and validation. Transl Cancer Res. 2015 4(3): 256-269. PMID: 26213686.
Marcuello M, Vymetalkova V, Neves RPL, Duran-Sanchon S, Vedeld HM, Tham E, van Dalum G, FlĂĽgen G, Garcia-Barberan V, Fijneman RJ, Castells A, Vodicka P, Lind GE, Stoecklein NH, Heitzer E, Gironella M. Circulating biomarkers for early detection and clinical management of colorectal cancer. Mol Aspects Med. 2019 69: 107-122. PMID: 31189073.
Galvao-Lima LJ, Morais AHF, Valentim RAM, Barreto E. miRNAs as biomarkers for early cancer detection and their application in the development of new diagnostic tools. Biomed Eng Online. 2021 20(1): 21. PMID: 33593374.
Ellsworth RE, Blackburn HL, Shriver CD, Soon-Shiong P, Ellsworth DL. Molecular heterogeneity in breast cancer: State of the science and implications for patient care. Semin Cell Dev Biol. 2017 64: 65-72. PMID: 27569190.
Kashyap D, Kaur H. Cell-free miRNAs as non-invasive biomarkers in breast cancer: Significance in early diagnosis and metastasis prediction. Life Sci. 2020 246: 117417. PMID: 32044304.
Sabit H, Cevik E, Tombuloglu H, Abdel-Ghany S, Tombuloglu G, Esteller M. Triple negative breast cancer in the era of miRNA. Crit Rev Oncol Hematol. 2021 157: 103196. PMID: 33307198.
Seijo LM, Peled N, Ajona D, Boeri M, Field JK, Sozzi G, Pio R, Zulueta JJ, Spira A, Massion PP, Mazzone PJ, Montuenga LM. Biomarkers in Lung Cancer Screening: Achievements, Promises, and Challenges. J Thorac Oncol. 2019 14(3): 343-357. PMID: 30529598.
Wu KL, Tsai YM, Lien CT, Kuo PL, Hung AJ. The Roles of MicroRNA in Lung Cancer. Int J Mol Sci. 2019 20(7). PMID: 30935143.
Ciarletto AM, Narick C, Malchoff CD, Massoll NA, Labourier E, Haugh K, Mireskandari A, Finkelstein SD, Kumar G. Analytical and clinical validation of pairwise microRNA expression analysis to identify medullary thyroid cancer in thyroid fine-needle aspiration samples. Cancer Cytopathol. 2021 129(3): 239-249. PMID: 33017868.
Kanaan Z, Roberts H, Eichenberger MR, Billeter A, Ocheretner G, Pan J, Rai SN, Jorden J, Williford A, Galandiuk S. A plasma microRNA panel for detection of colorectal adenomas: a step toward more precise screening for colorectal cancer. Ann Surg. 2013 258(3): 400-8. PMID: 24022433.
Aghdam AM, Amiri A, Salarinia R, Masoudifar A, Ghasemi F, Mirzaei H. MicroRNAs as Diagnostic, Prognostic, and Therapeutic Biomarkers in Prostate Cancer. Crit Rev Eukaryot Gene Expr. 2019 29(2): 127-139. PMID: 31679268.
Sohel MMH. Circulating microRNAs as biomarkers in cancer diagnosis. Life Sci. 2020 248: 117473. PMID: 32114007.
Saliminejad K, Khorram Khorshid HR, Ghaffari SH. Why have microRNA biomarkers not been translated from bench to clinic? Future Oncol. 2019 15(8): 801-803. PMID: 30652506.
Condrat CE, Thompson DC, Barbu MG, Bugnar OL, Boboc A, Cretoiu D, Suciu N, Cretoiu SM, Voinea SC. miRNAs as Biomarkers in Disease: Latest Findings Regarding Their Role in Diagnosis and Prognosis. Cells. 2020 9(2). PMID: 31979244.
Calin GA, Sevignani C, Dumitru CD, Hyslop T, Noch E, Yendamuri S, Shimizu M, Rattan S, Bullrich F, Negrini M, Croce CM. 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. PMID: 14973191.
Ferro E, Enrico Bena C, Grigolon S, Bosia C. microRNA-mediated noise processing in cells: A fight or a game? Comput Struct Biotechnol J. 2020 18: 642-649. PMID: 32257047.
Hamam R, Hamam D, Alsaleh KA, Kassem M, Zaher W, Alfayez M, Aldahmash A, Alajez NM. Circulating microRNAs in breast cancer: novel diagnostic and prognostic biomarkers. Cell Death Dis. 2017 8(9): e3045. PMID: 28880270.
Pritchard CC, Cheng HH, Tewari M. MicroRNA profiling: approaches and considerations. Nat Rev Genet. 2012 13(5): 358-69. PMID: 22510765.
GalvĂŁo-Lima LJ, Morais AHF, Valentim RAM, Barreto E. miRNAs as biomarkers for early cancer detection and their application in the development of new diagnostic tools. Biomed Eng Online. 2021 20(1): 21. PMID: 33593374.
Ozawa PMM, Jucoski TS, Vieira E, Carvalho TM, Malheiros D, Ribeiro E. Liquid biopsy for breast cancer using extracellular vesicles and cell-free microRNAs as biomarkers. Transl Res. 2020 223: 40-60. PMID: 32413499.
Miroshnichenko S, Patutina O. Enhanced Inhibition of Tumorigenesis Using Combinations of miRNA-Targeted Therapeutics. Front Pharmacol. 2019 10: 488. PMID: 31156429.
Beg MS, Brenner AJ, Sachdev J, Borad M, Kang YK, Stoudemire J, Smith S, Bader AG, Kim S, Hong DS. Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Invest New Drugs. 2017 35(2): 180-188. PMID: 27917453.
Hanna J, Hossain GS, Kocerha J. The Potential for microRNA Therapeutics and Clinical Research. Front Genet. 2019 10: 478. PMID: 31156715.
Mosoyan G, Kraus T, Ye F, Eng K, Crispino JD, Hoffman R, Iancu-Rubin C. Imetelstat, a telomerase inhibitor, differentially affects normal and malignant megakaryopoiesis. Leukemia. 2017 31(11): 2458-2467. PMID: 28270692.
Wang X, Hu CS, Petersen B, Qiu J, Ye F, Houldsworth J, Eng K, Huang F, Hoffman R. Imetelstat, a telomerase inhibitor, is capable of depleting myelofibrosis stem and progenitor cells. Blood Adv. 2018 2(18): 2378-2388. PMID: 30242099.
Sheedy P, Medarova Z. The fundamental role of miR-10b in metastatic cancer. Am J Cancer Res. 2018 8(9): 1674-1688. PMID: 30323962.
Li X, Yu S, Lee D, Kim G, Lee B, Cho Y, Zheng BY, Ke MR, Huang JD, Nam KT, Chen X, Yoon J. Facile Supramolecular Approach to Nucleic-Acid-Driven Activatable Nanotheranostics That Overcome Drawbacks of Photodynamic Therapy. ACS Nano. 2018 12(1): 681-688. PMID: 29232105.
Reid G, Kao SC, Pavlakis N, Brahmbhatt H, MacDiarmid J, Clarke S, Boyer M, van Zandwijk N. Clinical development of TargomiRs, a miRNA mimic-based treatment for patients with recurrent thoracic cancer. Epigenomics. 2016 8(8): 1079-85. PMID: 27185582.
Witten L, Slack FJ. miR-155 as a novel clinical target for hematological malignancies. Carcinogenesis. 2020 41(1): 2-7. PMID: 31711135.
Lieberman J. Tapping the RNA world for therapeutics. Nat Struct Mol Biol. 2018 25(5): 357-364. PMID: 29662218.
Coutinho MF, Matos L, Santos JI, Alves S. RNA Therapeutics: How Far Have We Gone? Adv Exp Med Biol. 2019 1157: 133-177. PMID: 31342441.
Zhupanyn P, Ewe A, BĂĽch T, Malek A, Rademacher P, MĂĽller C, Reinert A, Jaimes Y, Aigner A. Extracellular vesicle (ECV)-modified polyethylenimine (PEI) complexes for enhanced siRNA delivery in vitro and in vivo. J Control Release. 2020 319: 63-76. PMID: 31866504.
Pardi N, Hogan MJ, Porter FW, Weissman D. mRNA vaccines - a new era in vaccinology. Nat Rev Drug Discov. 2018 17(4): 261-279. PMID: 29326426.
Downloads
Published
Issue
Section
License
Copyright (c) 2021 The copyright to the submitted manuscript is held by the Author, who grants the Journal of Medical Science (JMS) a nonexclusive licence to use, reproduce, and distribute the work, including for commercial purposes.
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
