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Substantial Dysregulation of miRNA Passenger Strands Underlies the Vascular Response to Injury

Pinel, Karine, Diver, Louise A., White, Katie, McDonald, Robert A., Baker, Andrew H.·2019·Cells

Abstract

Vascular smooth muscle cell (VSMC) dedifferentiation is a common feature of vascular disorders leading to pro-migratory and proliferative phenotypes, a process induced through growth factor and cytokine signaling cascades. Recently, many studies have demonstrated that small non-coding RNAs (miRNAs) can induce phenotypic effects on VSMCs in response to vessel injury. However, most studies have focused on the contribution of individual miRNAs. Our study aimed to conduct a detailed and unbiased analysis of both guide and passenger miRNA expression in vascular cells in vitro and disease models in vivo. We analyzed 100 miRNA stem loops by TaqMan Low Density Array (TLDA) from primary VSMCs in vitro. Intriguingly, we found that a larger proportion of the passenger strands was significantly dysregulated compared to the guide strands after exposure to pathological stimuli, such as platelet-derived growth factor (PDGF) and IL-1α. Similar findings were observed in response to injury in porcine vein grafts and stent models in vivo. In these studies, we reveal that the miRNA passenger strands are predominantly dysregulated in response to vascular injury.

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  • The phenomena of miRNA arm switching, so far only observed in cancer, extends to healthy mammalian tissues.

    “This highlights the complexity of tissue-dependent miRNA biogenesis and indicates that the phenomena of miRNA arm switching, so far only observed in cancer, extends to healthy mammalian tissues (43–45).”

    From A mouse tissue atlas of small noncoding RNA (2020) · cites this paper as [44]

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Research works printed but not linked: 26

  1. [1]Wu L. Belasco J.G. Let me count the ways: Mechanisms of gene regulation by miRNAs and siRNAs Mol. Cell 2008 29 1 7 10.1016/j.molcel.2007.12.010 18206964 · DOI
  2. [2]Eulalio A. Huntzinger E. Izaurralde E. Getting to the root of miRNA-mediated gene silencing Cell 2008 132 9 14 10.1016/j.cell.2007.12.024 18191211 · DOI
  3. [3]Filipowicz W. Bhattacharyya S.N. Sonenberg N. Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight? Nat. Rev. Genet. 2008 9 102 114 10.1038/nrg2290 18197166 · DOI
  4. [4]Bartel D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function Cell 2004 116 281 297 10.1016/S0092-8674(04)00045-5 14744438 · DOI
  5. [5]Guo L. Zhang H. Zhao Y. Yang S. Chen F. Selected isomiR expression profiles via arm switching? Gene 2014 533 149 155 10.1016/j.gene.2013.09.102 24120620 · DOI
  6. [6]Winter J. Diederichs S. Argonaute-3 activates the let-7a passenger strand microRNA RNA Biol. 2013 10 1631 1643 10.4161/rna.26424 24100239 PMC3866245 · DOI
  7. [7]Owens G.K. Kumar M.S. Wamhoff B.R. Molecular regulation of vascular smooth muscle cell differentiation in development and disease Physiol. Rev. 2004 84 767 801 10.1152/physrev.00041.2003 15269336 · DOI
  8. [8]Dzau V.J. Braun-Dullaeus R.C. Sedding D.G. Vascular proliferation and atherosclerosis: New perspectives and therapeutic strategies Nat. Med. 2002 8 1249 1256 10.1038/nm1102-1249 12411952 · DOI
  9. [9]Ferns G.A. Raines E.W. Sprugel K.H. Motani A.S. Reidy M.A. Ross R. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF Science 1991 253 1129 1132 10.1126/science.1653454 1653454 · DOI
  10. [10]Yang J.-S. Phillips M.D. Betel D. Mu P. Ventura A. Siepel A.C. Chen K.C. Lai E.C. Widespread regulatory activity of vertebrate microRNA* species RNA Soc. 2011 17 312 326 10.1261/rna.2537911 PMC3022280 21177881 · DOI · Paper page
  11. [11]Okamura K. Phillips M.D. Tyler D.M. Duan H. Chou Y. Lai E.C. The regulatory activity of microRNA* species has substantial influence on microRNA and 3’ UTR evolution Nat. Struct. Mol. Biol. 2008 15 354 363 10.1038/nsmb.1409 18376413 PMC2698667 · DOI · Paper page
  12. [12]Griffiths-Jones S. Hui J.H.L. Marco A. Ronshaugen M. microRNA evolution by arm switching EMBO Rep. 2011 12 172 177 10.1038/embor.2010.191 21212805 PMC3049427 · DOI · Paper page
  13. [13]Poissonnier L. Villain G. Soncin F. Mattot V. miR126-5p repression of ALCAM and SetD5 in endothelial cells regulates leucocyte adhesion and transmigration Cardiovasc. Res. 2014 102 436 447 10.1093/cvr/cvu040 24562769 · DOI
  14. [14]Zhu S. Deng S. Ma Q. Zhang T. Jia C. Zhuo D. Yang F. Wei J. Wang L. Dykxhoorn D.M. microRNA-10A* and microRNA-21 modulate endothelial progenitor cell senescence via suppressing high-mobility group A2 Circ. Res. 2013 112 152 164 10.1161/CIRCRESAHA.112.280016 23072816 PMC3719009 · DOI
  15. [15]Chang K.-W. Kao S.-Y. Wu Y.-H. Tsai M.-M. Tu H.-F. Liu C.-J. Lui M.-T. Lin S.-C. Passenger strand miRNA miR-31* regulates the phenotypes of oral cancer cells by targeting RhoA Oral Oncol. 2013 49 27 33 10.1016/j.oraloncology.2012.07.003 22854067 · DOI
  16. [16]Yang X. Du W.W. Li H. Liu F. Khorshidi A. Rutnam Z.J. Yang B.B. Both mature miR-17-5p and passenger strand miR-17-3p target TIMP3 and induce prostate tumor growth and invasion Nucleic Acids Res. 2013 41 9688 9704 10.1093/nar/gkt680 23990326 PMC3834805 · DOI
  17. [17]McDonald R.A. White K.M. Wu J. Cooley B.C. Robertson K.E. Halliday C.A. McClure J.D. Francis S. Lu R. Kennedy S. miRNA-21 is dysregulated in response to vein grafting in multiple models and genetic ablation in mice attenuates neointima formation Eur. Heart J. 2013 34 1636 1643 10.1093/eurheartj/eht105 23530023 PMC3675389 · DOI
  18. [18]McDonald R.A. Halliday C.A. Miller A.M. Diver L.A. Dakin R.S. Montgomery J. McBride M.W. Kennedy S. McClure J.D. Robertson K.E. Reducing In-Stent Restenosis: Therapeutic Manipulation of miRNA in Vascular Remodeling and Inflammation J. Am. Coll. Cardiol. 2015 65 2314 2327 10.1016/j.jacc.2015.03.549 26022821 PMC4444526 · DOI
  19. [19]Angelini G.D. Bryan A.J. Williams H.M. Morgan R. Newby A.C. Distention promotes platelet and leukocyte adhesion and reduces short-term patency in pig arteriovenous bypass grafts J. Thorac. Cardiovasc. Surg. 1990 99 433 439 2308361
  20. [20]Southgate K.M. Davies M. Booth R.F. Newby A.C. Involvement of extracellular-matrix-degrading metalloproteinases in rabbit aortic smooth-muscle cell proliferation Biochem. J. 1992 288 93 99 10.1042/bj2880093 1445285 PMC1132084 · DOI
  21. [21]Raitoharju E. Lyytikäinen L.-P. Levula M. Oksala N. Mennander A. Tarkka M. Klopp N. Illig T. Kähönen M. Karhunen P.J. miR-21, miR-210, miR-34a, and miR-146a/b are up-regulated in human atherosclerotic plaques in the Tampere Vascular Study Atherosclerosis 2011 219 211 217 10.1016/j.atherosclerosis.2011.07.020 21820659 · DOI
  22. [22]Liu X. Cheng Y. Yang J. Xu L. Zhang C. Cell-specific effects of miR-221/222 in vessels: Molecular mechanism and therapeutic application J. Mol. Cell. Cardiol. 2012 52 245 255 10.1016/j.yjmcc.2011.11.008 22138289 PMC3664545 · DOI
  23. [23]Kee H.J. Kim G.R. Cho S.-N. Kwon J.-S. Ahn Y. Kook H. Jeong M.H. miR-18a-5p MicroRNA Increases Vascular Smooth Muscle Cell Differentiation by Downregulating Syndecan4 Korean Circ. J. 2014 44 255 263 10.4070/kcj.2014.44.4.255 25089138 PMC4117847 · DOI
  24. [24]Cheng Y. Liu X. Yang J. Lin Y. Xu D.-Z. Lu Q. Deitch E.A. Huo Y. Delphin E.S. Zhang C. MicroRNA-145, a novel smooth muscle cell phenotypic marker and modulator, controls vascular neointimal lesion formation Circ. Res. 2009 105 158 166 10.1161/CIRCRESAHA.109.197517 19542014 PMC2728297 · DOI
  25. [25]Chiang H.R. Schoenfeld L.W. Ruby J.G. Auyeung V.C. Spies N. Baek D. Johnston W.K. Russ C. Luo S. Babiarz J.E. Mammalian microRNAs: Experimental evaluation of novel and previously annotated genes Genes Dev. 2010 24 992 1009 10.1101/gad.1884710 20413612 PMC2867214 · DOI · Paper page
  26. [26]Ro S. Park C. Young D. Sanders K.M. Yan W. Tissue-dependent paired expression of miRNAs Nucleic Acids Res. 2007 35 5944 5953 10.1093/nar/gkm641 17726050 PMC2034466 · DOI · Paper page

Cited by

Sorted by citations

Authors
Pinel, K., Diver, L. A., White, K., McDonald, R. A., & Baker, A. H.
Affiliations
Institute of Cardiovascular and Medical Sciences, BHF Glasgow Cardiovascular Research Centre, University of Glasgow, Glasgow G12 8TA, UK
Venue
Cells
Publisher
MDPI AG
Published
2019-01-23
Volume
8
Issue
2
Pages
83
ISSN
2073-4409
Cited by
13
References
0
Language
en

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