Recent advances in understanding the role of miRNAs in exosomes and their therapeutic potential

doi:10.1016/S2095-3119(16)61530-7

摘要/Abstract

Abstract: MicroRNAs (miRNAs) are small endogenous non-protein coding RNAs that range in size from 19–25 nucleotides. Thousands of miRNA genes have been identified in a variety of organisms, suggesting genetic exchange and distribution among species. miRNAs negatively regulate gene expression by binding to the 3´-untranslated regions (3´-UTRs) of their target genes and play an important role in growth, development and the occurrence of diseases. In this review, we summarize the recent advances in the understanding of the role of miRNAs in exosomes and their therapeutic potential, as well as provide an overview of the basic characteristics of miRNAs.

Key words: miRNA, gene expression, gene regulation, gene transcription, exosomes, non-coding RNA

. [J]. Journal of Integrative Agriculture, 2017, 16(04): 753-761.

MIAO Xiang-yang. Recent advances in understanding the role of miRNAs in exosomes and their therapeutic potential[J]. Journal of Integrative Agriculture, 2017, 16(04): 753-761.

参考文献

MicroRNAs (miRNAs) are small endogenous non-protein coding RNAs that range in size from 19–25 nucleotides. Thousands of miRNA genes have been identified in a variety of organisms, suggesting genetic exchange and distribution among species. miRNAs negatively regulate gene expression by binding to the 3´-untranslated regions (3´-UTRs) of their target genes and play an important role in growth, development and the occurrence of diseases. In this review, we summarize the recent advances in the understanding of the role of miRNAs in exosomes and their therapeutic potential, as well as provide an overview of the basic characteristics of miRNAs.
Ai J, Zhang R, Li Y, Pu J, Lu Y, Jiao J, Li K, Yu B, Li Z, Wang R, Wang L, Li Q, Wang N, Shan H, Li Z, Yang B. 2010. Circulating microRNA-1 as a potential novel biomarker for acute myocardial infarction. Biochemical and Biophysical Research Communications, 391, 73–77.
Alipoor S D, Adcock I M, Garssen J, Mortaz E, Varahram M, Mirsaeidi M, Velayati A. 2016. The roles of miRNAs as potential biomarkers in lung diseases. European Journal of Pharmacology, 791, 395–404.
Ambros V, Bartel B, Bartel D P, Burge C B, Carrington J C, Chen X, Dreyfuss G, Eddy S R, Griffiths-Jones S, Marshall M, Matzke M, Ruvkun G, Tuschl T. 2003. A uniform system for microRNA annotation. RNA, 9, 277–279.
Baer C, Claus R, Plass C. 2013. Genome-wide epigenetic regulation of miRNAs in cancer. Cancer Research, 73, 473–477.
Bak R O, Mikkelsen J G. 2014. miRNA sponges: Soaking up miRNAs for regulation of gene expression. WIREs RNA, 5, 317–333.
Bartel D P. 2004. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell, 116, 281–297.
Bartel D P. 2009. MicroRNAs: Target recognition and regulatory functions. Cell, 136, 215–233.
Bloch D B, Nobre R A, Yang W H. 2013. GW/P-bodies and autoimmune disease. Advances in Experimental Medicine and Biology, 768, 61–70.
Carninci P, Kasukawa T, Katayama S, Gough J, Frith M C, Maeda N, Oyama R, Ravasi T, Lenhard B, Wells C, Kodzius R, Shimokawa K, Bajic V B, Brenner S E, Batalov S, Forrest A R, Zavolan M, Davis M J, Wilming L G, Aidinis V, et al. 2005. The transcriptional landscape of the mammalian genome. Science, 309, 1559–1563.
Carrington J C, Ambros V. 2003. Role of microRNAs in plant and animal development. Science, 301, 336–338.
Cazalla D, Yario T, Steitz J A. 2010. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science, 328, 1563–1566.
Cha D J, Franklin J L, Dou Y, Liu Q, Higginbotham J N, Demory Beckler M, Weaver A M, Vickers K, Prasad N, Levy S, Zhang B, Coffey R J, Patton J G. 2015. KRAS-dependent sorting of miRNA to exosomes. Elife, 4, e07197.
Chakraborty C, Wen Z H, Agoramoorthy G, Lin C S. 2016. Therapeutic microRNA delivery strategies with special emphasis on cancer therapy and tumorigenesis: Current trends and future challenges. Current Drug Metabolism, 17, 469–477.
Chen P S, Su J L, Hung M C. 2012. Dysregulation of microRNAs in cancer. Journal of Biomedical Science, 19, doi: 10.1186/1423-0127-19-90
Chen X, Liang H, Zhang J, Zen K, Zhang C Y. 2012. Horizontal transfer of microRNAs: Molecular mechanisms and clinical applications. Protein & Cell, 3, 28–37.
Cimmino A, Calin G A, Fabbri M, Iorio M V, Ferracin M, Shimizu M, Wojcik S E, Aqeilan R I, Zupo S, Dono M, Rassenti L, Alder H, Volinia S, Liu C G, Kipps T J, Negrini M, Croce C M. 2005. miR-15 and miR-16 induce apoptosis by targeting BCL2. Proceedings of the National Academy of Sciences of the United States of America, 102, 13944–13949.
Costa-Silva B, Aiello N M, Ocean A J, Singh S, Zhang H, Thakur B K, Becker A, Hoshino A, Mark M T, Molina H, Xiang J, Zhang T, Theilen T M, García-Santos G, Williams C, Ararso Y, Huang Y, Rodrigues G, Shen T L, Labori K J, et al. 2015. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nature Cell Biology, 17, 816–826.
Demory Beckler M, Higginbotham J N, Franklin J L, Ham A J, Halvey P J, Imasuen I E, Whitwell C, Li M, Liebler D C, Coffey R J. 2013. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Molecular & Cellular Proteomics, 12, 343–355.
Diederichs S, Haber D A. 2007. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell, 131, 1097–1108.
Ding J, Huang S, Wu S, Zhao Y, Liang L, Yan M, Ge C, Yao J, Chen T, Wan D, Wang H, Gu J, Yao M, Li J, Tu H, He X. 2010. Gain of miR-151 on chromosome 8q24.3 facilitates tumour cell migration and spreading through downregulating RhoGDIA. Nature Cell Biology, 12, 390–399.
Elbashir S M, Lendeckel W, Tuschl T. 2001. RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes & Development, 15, 188–200.
ElHefnawi M, Soliman B, Abu-Shahba N, Amer M. 2013. An integrative meta-analysis of microRNAs in hepatocellular carcinoma. Genomics, Proteomics & Bioinformatics, 11, 354–367.
Esquela-Kerscher A, Slack F J. 2006. Oncomirs - microRNAs with a role in cancer. Cancer, 6, 259–269.
Fernandez-Hernando C, Ramirez C M, Goedeke L, Suarez Y. 2013. MicroRNAs in metabolic disease. Arteriosclerosis Thrombosis and Vascular Biology, 33, 178–185.
Forterre A, Jalabert A, Chikh K, Pesenti S, Euthine V, Granjon A, Errazuriz E, Lefai E, Vidal H, Rome S. 2014. Myotube-derived exosomal miRNAs downregulate Sirtuin1 in myoblasts during muscle cell differentiation. Cell Cycle, 13, 78–89.
Franco-Zorrilla J M, Valli A, Todesco M, Mateos I, Puga M I, Rubio-Somoza I, Leyva A, Weigel D, Garcia J A, Paz-Ares J. 2007. Target mimicry provides a new mechanism for regulation of microRNA activity. Nature Genetics, 39, 1033–1037.
Friedlander M R, Chen W, Adamidi C, Maaskola J, Einspanier R, Knespel S, Rajewsky N. 2008. Discovering microRNAs from deep sequencing data using miRDeep. Nature Biotechnology, 26, 407–415.
Friedman R C, Farh K K, Burge C B, Bartel D P. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Research, 19, 92–105.
Fukaya T, Tomari Y. 2012. MicroRNAs mediate gene silencing via multiple different pathways in Drosophila. Molecular Cell, 48, 825–836.
Gaal Z, Olah E. 2012. MicroRNAs and their role in malignant hematologic diseases. Orvosi Hetilap, 153, 2051–2059.
Gambari R, Brognara E, Spandidos D A, Fabbri E. 2016. Targeting oncomiRNAs and mimicking tumor suppressor miRNAs: New trends in the development of miRNA therapeutic strategies in oncology. International Journal of Oncology, 49, 5–32.
Georgantas R W III, Hildreth R, Morisot S, Alder J, Liu C G, Heimfeld S, Calin G A, Croce C M, Civin C I. 2007. CD34⁺hematopoietic stem-progenitor cell microRNA expression and function: A circuit diagram of differentiation control. Proceedings of the National Academy of Sciences of the United States of America, 104, 2750–2755.
Guo H, Ingolia N T, Weissman J S, Bartel D P. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature, 466, 835–840.
Hannon G J, Rossi J J. 2004. Unlocking the potential of the human genome with RNA interference. Nature, 431, 371–378.
Hoshino D, Kirkbride K C, Costello K, Clark E S, Sinha S, Grega-Larson N, Tyska M J, Weaver A M. 2013. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Reports, 5, 1159–1168.
Huang Z, Huang D, Ni S, Peng Z, Sheng W, Du X. 2010. Plasma microRNAs are promising novel biomarkers for early detection of colorectal cancer. International Journal of Cancer, 127, 118–126.
Iorio M V, Piovan C, Croce C M. 2010. Interplay between microRNAs and the epigenetic machinery: An intricate network. Biochimica et Biophysica Acta, 1799, 694–701.
Ivanov M, Kacevska M, Ingelman-Sundberg M. 2012. Epigenomics and interindividual differences in drug response. Clinical Pharmacology and Therapeutics, 92, 727–736.
Di Lisio L, Martinez N, Montes-Moreno S, Piris-Villaespesa M, Sanchez-Beato M, Piris M A. 2012. The role of miRNAs in the pathogenesis and diagnosis of B-cell lymphomas. Blood, 120, 1782–1790.
Jagadeeswaran G, Zheng Y, Sumathipala N, Jiang H, Arrese E L, Soulages J L, Zhang W, Sunkar R. 2010. Deep sequencing of small RNA libraries reveals dynamic regulation of conserved and novel microRNAs and microRNA-stars during silkworm development. BMC Genomics, 11, 52.
Jinek M, Doudna J A. 2009. A three-dimensional view of the molecular machinery of RNA interference. Nature, 457, 405–412.
Khraiwesh B, Arif M A, Seumel G I, Ossowski S, Weigel D, Reski R, Frank W. 2010. Transcriptional control of gene expression by microRNAs. Cell, 140, 111–122.
Kim D H, Saetrom P, Snove Jr O, Rossi J J. 2008. MicroRNA-directed transcriptional gene silencing in mammalian cells. Proceedings of the National Academy of Sciences of the United States of America, 105, 16230–16235.
Kloosterman W P, Plasterk R H. 2006. The diverse functions of microRNAs in animal development and disease. Developmental Cell, 11, 441–450.
Kozomara A, Griffiths-Jones S. 2011. miRBase: Integrating microRNA annotation and deep-sequencing data. Nucleic Acids Research, 39, D152–D157.
Lagos-Quintana M, Rauhut R, Lendeckel W, Tuschl T. 2001. Identification of novel genes coding for small expressed RNAs. Science, 294, 853–858.
Lagos-Quintana M, Rauhut R, Meyer J, Borkhardt A, Tuschl T. 2003. New microRNAs from mouse and human. RNA, 9, 175–179.
Lanford R E, Hildebrandt-Eriksen E S, Petri A, Persson R, Lindow M, Munk M E, Kauppinen S, Orum H. 2010. Therapeutic silencing of microRNA-122 in primates with chronic hepatitis C virus infection. Science, 327, 198–201.
Lee R C, Feinbaum R L, Ambros V. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 75, 843–854.
Lee Y, Jeon K, Lee J T, Kim S, Kim V N. 2002. MicroRNA maturation: Stepwise processing and subcellular localization. The EMBO Journal, 21, 4663–4670.
Leong J W, Sullivan R P, Fehniger T A. 2012. Natural killer cell regulation by microRNAs in health and disease. Journal of Biomedicine & Biotechnology, 2012, doi: 10.1155/2012/632329
Li X Q, Guo Y Y, De W. 2012. DNA methylation and microRNAs in cancer. World Journal of Gastroenterology, 18, 882–888.
Litwińska Z, Machaliński B. 2016. miRNAs in chronic myeloid leukemia: Small molecules, essential function. Leuk Lymphoma, 13, 1–9.
Liu H. 2012. MicroRNAs in breast cancer initiation and progression. Cellular and Molecular Life Sciences, 69, 3587–3599.
Luedde T. 2010. MicroRNA-151 and its hosting gene FAK (focal adhesion kinase) regulate tumor cell migration and spreading of hepatocellular carcinoma. Hepatology, 52, 1164–1166.
Lund E, Guttinger S, Calado A, Dahlberg J E, Kutay U. 2004. Nuclear export of microRNA precursors. Science, 303, 95–98.
Mattes J, Collison A, Plank M, Phipps S, Foster P S. 2009. Antagonism of microRNA-126 suppresses the effector function of TH2 cells and the development of allergic airways disease. Proceedings of the National Academy of Sciences of the United States of America, 106, 18704–18709.
Miao X, Luo Q, Qin X. 2015a. Genome-wide analysis reveals the differential regulations of mRNAs and miRNAs in Dorset and Small Tail Han sheep muscles. Gene, 562, 188–196.
Miao X, Luo Q, Qin X. 2015b. Genome-wide transcriptome analysis of mRNAs and microRNAs in Dorset and Small Tail Han sheep to explore the regulation of fecundity. Molecular and Cellular Endocrinology, 402, 32–42.
Miao X, Luo Q, Qin X, Guo Y. 2015c. Genome-wide analysis of microRNAs identifies the lipid metabolism pathway to be a defining factor in adipose tissue from different sheep. Scientific Reports, 5, 18470.
Moldovan L, Batte K, Wang Y, Wisler J, Piper M. 2013. Analyzing the circulating microRNAs in exosomes/extracellular vesicles from serum or plasma by qRT-PCR. Methods in Molecular Biology, 1024, 129–145.
Morita K, Han M. 2006. Multiple mechanisms are involved in regulating the expression of the developmental timing regulator lin-28 in Caenorhabditis elegans. The EMBO Journal, 25, 5794–5804.
Morozova N, Zinovyev A, Nonne N, Pritchard L L, Gorban A N, Harel-Bellan A. 2012. Kinetic signatures of microRNA modes of action. RNA, 18, 1635–1655.
Mourelatos Z, Dostie J, Paushkin S, Sharma A, Charroux B, Abel L, Rappsilber J, Mann M, Dreyfuss G. 2002. miRNPs: A novel class of ribonucleoproteins containing numerous microRNAs. Genes & Development, 16, 720–728.
Mukherji S, Ebert M S, Zheng G X, Tsang J S, Sharp P A, van Oudenaarden A. 2011. MicroRNAs can generate thresholds in target gene expression. Nature Genetics, 43, 854–859.
Nana-Sinkam S P, Croce C M. 2013. Clinical applications for microRNAs in cancer. Clinical Pharmacology and Therapeutics, 93, 98–104.
tenOever B R. 2013. RNA viruses and the host microRNA machinery. Nature reviews. Microbiology, 11, 169–180.
Pasquinelli A E, Ruvkun G. 2002. Control of developmental timing by micrornas and their targets. Annual Review of Cell and Developmental Biology, 18, 495–513.
Petersen C P, Bordeleau M E, Pelletier J, Sharp P A. 2006. Short RNAs repress translation after initiation in mammalian cells. Molecular Cell, 21, 533–542.
van der Pol E, Boing A N, Harrison P, Sturk A, Nieuwland R. 2012. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacological Reviews, 64, 676–705.
Poliseno L, Salmena L, Zhang J, Carver B, Haveman W J, Pandolfi P P. 2010. A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature, 465, 1033–1038.
Portnoy V, Huang V, Place R F, Li L C. 2011. Small RNA and transcriptional upregulation. Wiley Interdisciplinary Reviews RNA, 2, 748–760.
Reinhart B J, Slack F J, Basson M, Pasquinelli A E, Bettinger J C, Rougvie A E, Horvitz H R, Ruvkun G. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature, 403, 901–906.
Robins H, Li Y, Padgett R W. 2005. Incorporating structure to predict microRNA targets. Proceedings of the National Academy of Sciences of the United States of America, 102, 4006–4009.
Rossi S, Di Narzo A F, Mestdagh P, Jacobs B, Bosman F T, Gustavsson B, Majoie B, Roth A, Vandesompele J, Rigoutsos I, Delorenzi M, Tejpar S. 2012. microRNAs in colon cancer: A roadmap for discovery. FEBS Letters, 586, 3000–3007.
Ruegger S, Grosshans H. 2012. MicroRNA turnover: when, how, and why. Trends in Biochemical Sciences, 37, 436–446.
Rutnam Z J, Yang B B. 2012. The involvement of microRNAs in malignant transformation. Histology and Histopathology, 27, 1263–1270.
Shaw W R, Armisen J, Lehrbach N J, Miska E A. 2010. The conserved miR-51 microRNA family is redundantly required for embryonic development and pharynx attachment in Caenorhabditis elegans. Genetics, 185, 897–905.
Shen J, Stass S A, Jiang F. 2013. MicroRNAs as potential biomarkers in human solid tumors. Cancer Letters, 329, 125–136.
Shimura H, Masuta C. 2012. RNA silencing and viral disease induction in plants. Uirusu, 62, 19–26. (in Japanese)
Sieber P, Wellmer F, Gheyselinck J, Riechmann J L, Meyerowitz E M. 2007. Redundancy and specialization among plant microRNAs: Role of the MIR164 family in developmental robustness. Development, 134, 1051–1060.
Small E M, Olson E N. 2011. Pervasive roles of microRNAs in cardiovascular biology. Nature, 469, 336–342.
Tay Y, Zhang J, Thomson A M, Lim B, Rigoutsos I. 2008. MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature, 455, 1124–1128.
Treiber T, Treiber N, Meister G. 2012. Regulation of microRNA biogenesis and function. Thrombosis and Haemostasis, 107, 605–610.
Tsitkanou S, Della Gatta P A, Russell A P. 2016. Skeletal muscle satellite cells, mitochondria, and MicroRNAs: Their involvement in the pathogenesis of ALS. Frontiers in Physiology, 7, 403.
Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee J J, Lotvall J O. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nature Cell Biology, 9, 654–659.
Wang B, Yanez A, Novina C D. 2008. MicroRNA-repressed mRNAs contain 40S but not 60S components. Proceedings of the National Academy of Sciences of the United States of America, 105, 5343–5348.
Wang J F, Yu M L, Yu G, Bian J J, Deng X M, Wan X J, Zhu K M. 2010. Serum miR-146a and miR-223 as potential new biomarkers for sepsis. Biochemical and Biophysical Research Communications, 394, 184–188.
Williams A H, Valdez G, Moresi V, Qi X, McAnally J, Elliott J L, Bassel-Duby R, Sanes J R, Olson E N. 2009. MicroRNA-206 delays ALS progression and promotes regeneration of neuromuscular synapses in mice. Science, 326, 1549–1554.
Wong R, Cunningham D. 2008. Using predictive biomarkers to select patients with advanced colorectal cancer for treatment with epidermal growth factor receptor antibodies. Journal of Clinical Oncology, 26, 5668–5670.
Wu L, Fan J, Belasco J G. 2006. MicroRNAs direct rapid deadenylation of mRNA. Proceedings of the National Academy of Sciences of the United States of America, 103, 4034–4039.