Advertisement

Biophysical Reviews

, Volume 10, Issue 5, pp 1241–1256 | Cite as

Epigenetic influences on genetically triggered thoracic aortic aneurysm

  • Stefanie S. PortelliEmail author
  • Elizabeth N. Robertson
  • Cassandra Malecki
  • Kiersten A. Liddy
  • Brett D. Hambly
  • Richmond W. Jeremy
Review

Abstract

Genetically triggered thoracic aortic aneurysms (TAAs) account for 30% of all TAAs and can result in early morbidity and mortality in affected individuals. Epigenetic factors are now recognised to influence the phenotype of many genetically triggered conditions and have become an area of interest because of the potential for therapeutic manipulation. Major epigenetic modulators include DNA methylation, histone modification and non-coding RNA. This review examines epigenetic modulators that have been significantly associated with genetically triggered TAAs and their potential utility for translation to clinical practice.

Keywords

Thoracic aortic aneurysm Aortic dilatation Epigenetics Non-coding RNA MicroRNA 

Notes

Acknowledgements

The authors would like to thank Morvarid Emami for providing the histology images.

Compliance with ethical standards

Conflict of interest

Stefanie Portelli declares that she has no conflict of interest. Elizabeth Robertson declares that she has no conflict of interest. Cassandra Malecki declares that she has no conflict of interest. Kiersten Liddy declares that she has no conflict of interest. Brett Hambly declares that he has no conflict of interest. Richmond Jeremy declares that he has no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

References

  1. Abu-Halima M, Kahraman M, Henn D, Radle-Hurst T, Keller A, Abdul-Khaliq H, Meese E (2018) Deregulated microRNA and mRNA expression profiles in the peripheral blood of patients with Marfan syndrome. J Transl Med 16  https://doi.org/10.1186/s12967-018-1429-3
  2. Alajbegovic A et al (2017) Regulation of microRNA expression in vascular smooth muscle by MRTF-A and actin polymerization. Biochim Biophys Acta, Mol Cell Res 1864:1088–1098.  https://doi.org/10.1016/j.bbamcr.2016.12.005 CrossRefGoogle Scholar
  3. Albinsson S et al (2017) Patients with bicuspid and tricuspid aortic valve exhibit distinct regional microRNA signatures in mildly dilated ascending aorta. Heart Vessel 32:750–767.  https://doi.org/10.1007/s00380-016-0942-7 CrossRefGoogle Scholar
  4. Albornoz G, Coady MA, Roberts M, Davies RR, Tranquilli M, Rizzo JA, Elefteriades JA (2006) Familial thoracic aortic aneurysms and dissections—incidence, modes of inheritance, and phenotypic patterns. Ann Thorac Surg 82:1400–1405.  https://doi.org/10.1016/j.athoracsur.2006.04.098 CrossRefPubMedGoogle Scholar
  5. Andelfinger G, Loeys B, Dietz H (2016) A decade of discovery in the genetic understanding of thoracic aortic disease. Can J Cardiol 32:13–25.  https://doi.org/10.1016/j.cjca.2015.10.017 CrossRefPubMedGoogle Scholar
  6. Ballantyne MD, McDonald RA, Baker AH (2016) lncRNA/microRNA interactions in the vasculature. Clin Pharmacol Ther 99:494–501.  https://doi.org/10.1002/cpt.355 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Barker AJ et al (2012) Bicuspid aortic valve is associated with altered wall shear stress in the ascending aorta. Circ Cardiovasc Imaging 5:457–466.  https://doi.org/10.1161/CIRCIMAGING.112.973370 CrossRefPubMedGoogle Scholar
  8. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297CrossRefGoogle Scholar
  9. Beg MS et al (2017) Phase I study of MRX34, a liposomal miR-34a mimic, administered twice weekly in patients with advanced solid tumors. Investig New Drugs 35:180–188.  https://doi.org/10.1007/s10637-016-0407-y CrossRefGoogle Scholar
  10. Beighton P, De Paepe A, Steinmann B, Tsipouras P, Wenstrup RJ (1998) Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997. Am J Med Genet 77:31–37.  https://doi.org/10.1002/(SICI)1096-8628(19980428)77:1<31::AID-AJMG8>3.0.CO;2-O CrossRefPubMedGoogle Scholar
  11. Belz GG, Belz GG (1995) Elastic properties and Windkessel function of the human aorta. Cardiovasc Drugs Ther 9:73–83.  https://doi.org/10.1007/BF00877747 CrossRefPubMedGoogle Scholar
  12. Boettger T, Beetz N, Kostin S, Schneider J, Kruger M, Hein L, Braun T (2009) Acquisition of the contractile phenotype by murine arterial smooth muscle cells depends on the Mir143/145 gene cluster. J Clin Invest 119:2634–2647.  https://doi.org/10.1172/jci38864 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Boon RA et al (2011) MicroRNA-29 in aortic dilation: implications for aneurysm formation. Circ Res 109:1115–1119.  https://doi.org/10.1161/circresaha.111.255737 CrossRefPubMedGoogle Scholar
  14. Boucher JM, Peterson SM, Urs S, Zhang C, Liaw L (2011) The miR-143/145 cluster is a novel transcriptional target of Jagged-1/Notch signaling in vascular smooth muscle cells. J Biol Chem 286:28312–28321.  https://doi.org/10.1074/jbc.M111.221945 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Burn GL, Svensson L, Sanchez-Blanco C, Saini M, Cope AP (2011) Why is PTPN22 a good candidate susceptibility gene for autoimmune disease? FEBS Lett 585:3689–3698CrossRefGoogle Scholar
  16. Cao H et al (2016) A new plasmid-based microRNA inhibitor system that inhibits microRNA families in transgenic mice and cells: a potential new therapeutic reagent. Gene Ther 23:527–542.  https://doi.org/10.1038/gt.2016.22 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Cardenas CLL et al (2018) An HDAC9-MALAT1-BRG1 complex mediates smooth muscle dysfunction in thoracic aortic aneurysm. Nat Commun 9:1009–1014.  https://doi.org/10.1038/s41467-018-03394-7 CrossRefGoogle Scholar
  18. Carrion K, Dyo J, Patel V, Sasik R, Mohamed SA, Hardiman G, Nigam V (2014) The long non-coding HOTAIR is modulated by cyclic stretch and WNT/β-CATENIN in human aortic valve cells and is a novel repressor of calcification genes. PLoS One 9:e96577.  https://doi.org/10.1371/journal.pone.0096577 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Chakraborty C, Sharma AR, Sharma G, Doss CGP, Lee S-S (2017) Therapeutic miRNA and siRNA: moving from bench to clinic as next generation medicine. Mol Ther Nucleic Acids 8:132–143.  https://doi.org/10.1016/j.omtn.2017.06.005 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Chen K-C, Liao Y-C, Hsieh IC, Wang Y-S, Hu C-Y, Juo S-HH (2012) OxLDL causes both epigenetic modification and signaling regulation on the microRNA-29b gene: novel mechanisms for cardiovascular diseases. J Mol Cell Cardiol 52:587–595.  https://doi.org/10.1016/j.yjmcc.2011.12.005 CrossRefPubMedGoogle Scholar
  21. Chen KC, Wang YS, Hu CY, Chang WC, Liao YC, Dai CY, Juo SH (2011) OxLDL up-regulates microRNA-29b, leading to epigenetic modifications of MMP-2/MMP-9 genes: a novel mechanism for cardiovascular diseases. FASEB J 25:1718–1728.  https://doi.org/10.1096/fj.10-174904 CrossRefPubMedGoogle Scholar
  22. Chen LJ, Wei SY, Chiu JJ (2013) Mechanical regulation of epigenetics in vascular biology and pathobiology. J Cell Mol Med 17:437–448.  https://doi.org/10.1111/jcmm.12031 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Chen X et al (2008) Characterization of microRNAs in serum: a novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res 18:997–1006.  https://doi.org/10.1038/cr.2008.282 CrossRefPubMedGoogle Scholar
  24. Chernov A, Strongin A (2011) Epigenetic regulation of matrix metalloproteinases and their collagen substrates in cancer. Biomol Concepts 2:135–147CrossRefGoogle Scholar
  25. Chicoine E, Esteve PO, Robledo O, Van Themsche C, Potworowski EF, St-Pierre Y (2002) Evidence for the role of promoter methylation in the regulation of MMP-9 gene expression. Biochem Biophys Res Commun 297:765–772CrossRefGoogle Scholar
  26. Chopra S, Al-Sammarraie N, Lai Y, Azhar M (2017) Increased canonical WNT/β-catenin signalling and myxomatous valve disease. Cardiovasc Res 113:6–9.  https://doi.org/10.1093/cvr/cvw236 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Climent M, Quintavalle M, Miragoli M, Chen J, Condorelli G, Elia L (2015) TGFβ triggers miR-143/145 transfer from smooth muscle cells to endothelial cells, thereby modulating vessel stabilization. Circ Res 116:1753–1764.  https://doi.org/10.1161/circresaha.116.305178 CrossRefPubMedGoogle Scholar
  28. Clouse WD, Hallett JW Jr, Schaff HV, Gayari MM, Ilstrup DM, Melton LJ 3rd (1998) Improved prognosis of thoracic aortic aneurysms: a population-based study. JAMA 280:1926–1929CrossRefGoogle Scholar
  29. Conway SJ, Woster PM, Greenlee WJ, Georg G, Wang S (2016) Epigenetics: novel therapeutics targeting epigenetics. J Med Chem 59:1247–1248.  https://doi.org/10.1021/acs.jmedchem.6b00098 CrossRefPubMedGoogle Scholar
  30. Cordes KR et al (2009) miR-145 and miR-143 regulate smooth muscle cell fate and plasticity. Nature 460:705+PubMedPubMedCentralGoogle Scholar
  31. Couillard J, Demers M, Lavoie G, St-Pierre Y (2006) The role of DNA hypomethylation in the control of stromelysin gene expression. Biochem Biophys Res Commun 342:1233–1239.  https://doi.org/10.1016/j.bbrc.2006.02.068 CrossRefPubMedGoogle Scholar
  32. Curradi M, Izzo A, Badaracco G, Landsberger N (2002) Molecular mechanisms of gene silencing mediated by DNA methylation. Mol Cell Biol 22:3157–3173CrossRefGoogle Scholar
  33. De Backer J, Loeys B, Leroy B, Coucke P, Dietz H, De Paepe A (2007) Utility of molecular analyses in the exploration of extreme intrafamilial variability in the Marfan syndrome. Clin Genet 72:188–198.  https://doi.org/10.1111/j.1399-0004.2007.00845.x CrossRefPubMedGoogle Scholar
  34. De Lucia C et al (2017) MicroRNA in cardiovascular aging and age-related cardiovascular diseases. Front Med 4:74.  https://doi.org/10.3389/fmed.2017.00074 CrossRefGoogle Scholar
  35. Dietz HC et al (1991) Marfan syndrome caused by a recurrent de novo missense mutation in the fibrillin gene. Nature 352:337–339.  https://doi.org/10.1038/352337a0 CrossRefGoogle Scholar
  36. Elefteriades JA, Farkas EA (2010) Thoracic aortic aneurysm: clinically pertinent controversies and uncertainties. JACC 55:841–857.  https://doi.org/10.1016/j.jacc.2009.08.084 CrossRefPubMedGoogle Scholar
  37. Elia L et al (2009) The knockout of miR-143 and -145 alters smooth muscle cell maintenance and vascular homeostasis in mice: correlates with human disease. Cell Death Differ 16:1590–1598.  https://doi.org/10.1038/cdd.2009.153 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Emmott A et al (2016) Biomechanics of the ascending thoracic aorta: a clinical perspective on engineering data. Can J Cardiol 32:35–47.  https://doi.org/10.1016/j.cjca.2015.10.015 CrossRefPubMedGoogle Scholar
  39. Engreitz JM, Ollikainen N, Guttman M (2016) Long non-coding RNAs: spatial amplifiers that control nuclear structure and gene expression. Nat Rev Mol Cell Biol 17:756–770.  https://doi.org/10.1038/nrm.2016.126 CrossRefPubMedGoogle Scholar
  40. Esteller M (2011) Non-coding RNAs in human disease. Nat Rev Genet 12:861.  https://doi.org/10.1038/nrg3074 CrossRefPubMedGoogle Scholar
  41. Faivre L et al (2007) Effect of mutation type and location on clinical outcome in 1,013 probands with Marfan syndrome or related phenotypes and FBN1 mutations: an international study. Am J Hum Genet 81:454–466.  https://doi.org/10.1086/520125 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Feinberg AP (2007) Phenotypic plasticity and the epigenetics of human disease. Nature 447:433.  https://doi.org/10.1038/nature05919 CrossRefPubMedGoogle Scholar
  43. Forte A, Galderisi U, Cipollaro M, De Feo M, Della Corte A (2016) Epigenetic regulation of TGF-beta1 signalling in dilative aortopathy of the thoracic ascending aorta. Clin Sci (Lond) 130:1389–1405.  https://doi.org/10.1042/cs20160222 CrossRefGoogle Scholar
  44. Garg V et al (2005) Mutations in NOTCH1 cause aortic valve disease. Nature 437:270–274.  https://doi.org/10.1038/nature03940 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Germain DP (2007) Ehlers-Danlos syndrome type IV. Orphanet J Rare Dis 2:32–32.  https://doi.org/10.1186/1750-1172-2-32 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Gilad S et al (2008) Serum microRNAs are promising novel biomarkers. PLoS One 3:e3148.  https://doi.org/10.1371/journal.pone.0003148 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Girdauskas E et al (2018a) Evaluation of microribonucleic acids as potential biomarkers in the bicuspid aortic valve-associated aortopathy. Interact Cardiovasc Thorac Surg 27:60–66.  https://doi.org/10.1093/icvts/ivy033 CrossRefPubMedGoogle Scholar
  48. Girdauskas E et al (2018b) Novel approaches for BAV aortopathy prediction—is there a need for cohort studies and biomarkers? Biomolecules 8:58.  https://doi.org/10.3390/biom8030058 CrossRefPubMedCentralGoogle Scholar
  49. Goldfinger JZ, Halperin JL, Marin ML, Stewart AS, Eagle KA, Fuster V (2014) Thoracic aortic aneurysm and dissection. JACC 64:1725–1739.  https://doi.org/10.1016/j.jacc.2014.08.025 CrossRefPubMedGoogle Scholar
  50. Gomez D, Coyet A, Ollivier V, Jeunemaitre X, Jondeau G, Michel J-B, Vranckx R (2011) Epigenetic control of vascular smooth muscle cells in Marfan and non-Marfan thoracic aortic aneurysms. Cardiovasc Res 89:446–456.  https://doi.org/10.1093/cvr/cvq291 CrossRefPubMedGoogle Scholar
  51. Gomez D, Kessler K, Michel J-B, Vranckx R (2013) Modifications of chromatin dynamics control the Smad2 pathway activation in aneurysmal smooth muscle cells. Circ Res 113:881–890CrossRefGoogle Scholar
  52. Gommans WM, Berezikov E (2012) Controlling miRNA regulation in disease. Methods Mol Biol 822:1–18.  https://doi.org/10.1007/978-1-61779-427-8_1 CrossRefPubMedGoogle Scholar
  53. Greer E, Shi Y (2012) Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet 13:343–357CrossRefGoogle Scholar
  54. Griffin CT, Brennan J, Magnuson T (2008) The chromatin-remodeling enzyme BRG1 plays an essential role in primitive erythropoiesis and vascular development. Development 135:493–500.  https://doi.org/10.1242/dev.010090 CrossRefPubMedGoogle Scholar
  55. Groth KA et al (2015) Prevalence, incidence, and age at diagnosis in Marfan syndrome. Orphanet J Rare Dis 10:153.  https://doi.org/10.1186/s13023-015-0369-8 CrossRefPubMedPubMedCentralGoogle Scholar
  56. Gulyaeva LF, Kushlinskiy NE (2016) Regulatory mechanisms of microRNA expression. J Transl Med 14:143.  https://doi.org/10.1186/s12967-016-0893-x CrossRefPubMedPubMedCentralGoogle Scholar
  57. Guo X, Chang Q, Pei H, Sun X, Qian X, Tian C, Lin H (2017) Long non-coding RNA–mRNA correlation analysis reveals the potential role of HOTAIR in pathogenesis of sporadic thoracic aortic aneurysm. J Vasc Surg 66:1305–1305.  https://doi.org/10.1016/j.jvs.2017.08.013 CrossRefGoogle Scholar
  58. Guo X, Yu L, Chen M, Wu T, Peng X, Guo R, Zhang B (2016) miR-145 mediated the role of aspirin in resisting VSMCs proliferation and anti-inflammation through CD40. J Transl Med 14:211.  https://doi.org/10.1186/s12967-016-0961-2 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Gupta RA et al (2010) Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:1071–1076.  https://doi.org/10.1038/nature08975 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15:509.  https://doi.org/10.1038/nrm3838 CrossRefPubMedGoogle Scholar
  61. Halushka MK et al (2016) Consensus statement on surgical pathology of the aorta from the Society for Cardiovascular Pathology and the Association For European Cardiovascular Pathology: II. Noninflammatory degenerative diseases—nomenclature and diagnostic criteria. Cardiovasc Pathol 25:247–257.  https://doi.org/10.1016/j.carpath.2016.03.002 CrossRefPubMedGoogle Scholar
  62. Han Y et al (2016) Histone acetylation and histone acetyltransferases show significant alterations in human abdominal aortic aneurysm. Clin Epigenetics 8:3.  https://doi.org/10.1186/s13148-016-0169-6 CrossRefPubMedPubMedCentralGoogle Scholar
  63. He R et al (2008) Characterization of the inflammatory cells in ascending thoracic aortic aneurysms in patients with Marfan syndrome, familial thoracic aortic aneurysms and sporadic aneurysms. J Thorac Cardiovasc Surg 136:922–929.e921.  https://doi.org/10.1016/j.jtcvs.2007.12.063 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Hiratzka LF et al (2010) 2010 ACCF/AHA/AATS/ACR/ASA/SCA/SCAI/SIR/STS/SVM guidelines for the diagnosis and management of patients with thoracic aortic disease. A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines, American Association for Thoracic Surgery, American College of Radiology, American Stroke Association, Society of Cardiovascular Anesthesiologists, Society for Cardiovascular Angiography and Interventions, Society of Interventional Radiology, Society of Thoracic Surgeons, and Society for Vascular Medicine. J Am Coll Cardiol 55:e27–e129.  https://doi.org/10.1016/j.jacc.2010.02.015 CrossRefPubMedGoogle Scholar
  65. Holmberg J et al (2018) Loss of vascular myogenic tone in miR-143/145 knockout mice is associated with hypertension-induced vascular lesions in small mesenteric arteries. Arterioscler Thromb Vasc Biol 38:414–424.  https://doi.org/10.1161/ATVBAHA.117.310499 CrossRefPubMedGoogle Scholar
  66. Hrdlickova B, de Almeida RC, Borek Z, Withoff S (2014) Genetic variation in the non-coding genome: involvement of micro-RNAs and long non-coding RNAs in disease. Biochim Biophys Acta Mol basis Dis 1842:1910–1922.  https://doi.org/10.1016/j.bbadis.2014.03.011 CrossRefGoogle Scholar
  67. Hu JZ et al (2016) The angiogenic effect of microRNA-21 targeting TIMP3 through the regulation of MMP2 and MMP9. PLoS One 11:e0149537.  https://doi.org/10.1371/journal.pone.0149537 CrossRefPubMedPubMedCentralGoogle Scholar
  68. Humphrey JD, Schwartz MA, Tellides G, Milewicz DM (2015) Role of mechanotransduction in vascular biology: focus on thoracic aortic aneurysms and dissections. Circ Res 116:1448–1461.  https://doi.org/10.1161/CIRCRESAHA.114.304936 CrossRefPubMedPubMedCentralGoogle Scholar
  69. Ikonomidis JS et al (2013) Plasma biomarkers for distinguishing etiologic subtypes of thoracic aortic aneurysm disease. J Thorac Cardiovasc Surg 145:1326–1333.  https://doi.org/10.1016/j.jtcvs.2012.12.027 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Iwata J, Parada C, Chai Y (2011) The mechanism of TGF-beta signaling during palate development. Oral Dis 17:733–744.  https://doi.org/10.1111/j.1601-0825.2011.01806.x CrossRefPubMedPubMedCentralGoogle Scholar
  71. Jabbari K, Bernardi G (2004) Cytosine methylation and CpG, TpG (CpA) and TpA frequencies. Gene 333:143–149.  https://doi.org/10.1016/j.gene.2004.02.043 CrossRefPubMedGoogle Scholar
  72. Janssen HLA et al (2013) Treatment of HCV infection by targeting microRNA. N Engl J Med 368:1685–1694.  https://doi.org/10.1056/NEJMoa1209026 CrossRefPubMedGoogle Scholar
  73. Jones JA et al (2011) Selective microRNA suppression in human thoracic aneurysms: relationship of miR-29a to aortic size and proteolytic induction. Circ Cardiovasc Genet 4:605–613.  https://doi.org/10.1161/CIRCGENETICS.111.960419 CrossRefPubMedPubMedCentralGoogle Scholar
  74. Jones PA, Issa J-PJ, Baylin S (2016) Targeting the cancer epigenome for therapy. Nat Rev Genet 17:630CrossRefGoogle Scholar
  75. Kallenbach K et al (2013) Treatment of ascending aortic aneurysms using different surgical techniques: a single-centre experience with 548 patients. Eur J Cardiothorac Surg 44:337–345.  https://doi.org/10.1093/ejcts/ezs661 CrossRefPubMedGoogle Scholar
  76. Kopp F, Mendell JT (2018) Functional classification and experimental dissection of long noncoding RNAs. Cell 172:393–407.  https://doi.org/10.1016/j.cell.2018.01.011 CrossRefPubMedGoogle Scholar
  77. Kouzarides T (2007) Chromatin modifications and their function. Cell 128:693–705.  https://doi.org/10.1016/j.cell.2007.02.005 CrossRefPubMedGoogle Scholar
  78. Larsen F, Gundersen G, Lopez R, Prydz H (1992) CpG islands as gene markers in the human genome. Genomics 13:1095–1107CrossRefGoogle Scholar
  79. Leeper NJ, Maegdefessel L (2018) Non-coding RNAs: key regulators of smooth muscle cell fate in vascular disease. Cardiovasc Res 114:611–621.  https://doi.org/10.1093/cvr/cvx249 CrossRefPubMedGoogle Scholar
  80. Lewis BP, Burge CB, Bartel DP (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20.  https://doi.org/10.1016/j.cell.2004.12.035 CrossRefGoogle Scholar
  81. Li Y, Huang J, Jiang Z, Zhong Y, Xia M, Wang H, Jiao Y (2016a) MicroRNA-145 regulates platelet-derived growth factor-induced human aortic vascular smooth muscle cell proliferation and migration by targeting CD40. Am J Transl Res 8:1813–1825PubMedPubMedCentralGoogle Scholar
  82. Li Y, Maegdefessel L (2017) Non-coding RNA contribution to thoracic and abdominal aortic aneurysm disease development and progression. Front Physiol 8:429.  https://doi.org/10.3389/fphys.2017.00429 CrossRefPubMedPubMedCentralGoogle Scholar
  83. Li Y, Xu J, Chen M, Du B, Li Q, Xing Q, Zhang Y (2016b) A FBN1 mutation association with different phenotypes of Marfan syndrome in a Chinese family. Clin Chim Acta 460:102–106.  https://doi.org/10.1016/j.cca.2016.06.031 CrossRefPubMedGoogle Scholar
  84. Liao M et al (2011) A microRNA profile comparison between thoracic aortic dissection and normal thoracic aorta indicates the potential role of microRNAs in contributing to thoracic aortic dissection pathogenesis. J Vasc Surg 53:1341–1349.e1343.  https://doi.org/10.1016/j.jvs.2010.11.113 CrossRefPubMedGoogle Scholar
  85. Licholai S, Blaz M, Kapelak B, Sanak M (2016) Unbiased profile of microRNA expression in ascending aortic aneurysm tissue appoints molecular pathways contributing to the pathology. Ann Thorac Surg 102:1245–1252.  https://doi.org/10.1016/j.athoracsur.2016.03.061 CrossRefPubMedGoogle Scholar
  86. Liu R et al (2013a) TET2 is a master regulator of smooth muscle cell plasticity. Circulation 128:2047–2057CrossRefGoogle Scholar
  87. Liu R, Leslie KL, Martin KA (2014) Epigenetic regulation of smooth muscle cell plasticity. Biochim Biophys Acta, Gene Regul Mech 1849:448–453.  https://doi.org/10.1016/j.bbagrm.2014.06.004 CrossRefGoogle Scholar
  88. Liu X et al (2013b) Flank sequences of miR-145/143 and their aberrant expression in vascular disease: mechanism and therapeutic application. J Am Heart Assoc 2:e000407.  https://doi.org/10.1161/JAHA.113.000407 CrossRefPubMedPubMedCentralGoogle Scholar
  89. Liu Y et al (2010) Renal medullary microRNAs in Dahl salt-sensitive rats: miR-29b regulates several collagens and related genes. Hypertension 55:974–982.  https://doi.org/10.1161/hypertensionaha.109.144428 CrossRefPubMedPubMedCentralGoogle Scholar
  90. Loeys B (2016) The search for genotype/phenotype correlation in Marfan syndrome: to be or not to be? Eur Heart J 37:3291–3293.  https://doi.org/10.1093/eurheartj/ehw154 CrossRefPubMedGoogle Scholar
  91. Loeys BL, Dietz HC (2008) Loeys Dietz syndrome. University of Washington, Seattle https://www.ncbi.nlm.nih.gov/books/NBK1133/. Accessed Jul 12 2018Google Scholar
  92. Loeys BL et al (2010) The revised Ghent nosology for the Marfan syndrome. J Med Genet 47:476–485.  https://doi.org/10.1136/jmg.2009.072785 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Loeys BL et al (2006) Aneurysm syndromes caused by mutations in the TGF-β receptor. N Engl J Med 355:788–798.  https://doi.org/10.1056/NEJMoa055695 CrossRefPubMedPubMedCentralGoogle Scholar
  94. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 angstrom resolution. Nature 389:251–260.  https://doi.org/10.1038/38444 CrossRefPubMedGoogle Scholar
  95. Luo T, Cui S, Bian C, Yu X (2014) Crosstalk between TGF-β/Smad3 and BMP/BMPR2 signaling pathways via miR-17–92 cluster in carotid artery restenosis. Mol Cell Biochem 389:169–176.  https://doi.org/10.1007/s11010-013-1938-6 CrossRefPubMedGoogle Scholar
  96. Maegdefessel L et al (2012) Inhibition of microRNA-29b reduces murine abdominal aortic aneurysm development. J Clin Invest 122:497–506.  https://doi.org/10.1172/JCI61598 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Martinez-Micaelo N, Beltran-Debon R, Baiges I, Faiges M, Alegret JM (2017) Specific circulating microRNA signature of bicuspid aortic valve disease. J Transl Med 15.  https://doi.org/10.1186/s12967-017-1176-x
  98. McDonald OG, Wamhoff BR, Hoofnagle MH, Owens GK (2006) Control of SRF binding to CArG box chromatin regulates smooth muscle gene expression in vivo. J Clin Invest 116:36–48.  https://doi.org/10.1172/JCI26505 CrossRefPubMedPubMedCentralGoogle Scholar
  99. McKellar SH, Tester DJ, Yagubyan M, Majumdar R, Ackerman MJ, Sundt TM 3rd (2007) Novel NOTCH1 mutations in patients with bicuspid aortic valve disease and thoracic aortic aneurysms. J Thorac Cardiovasc Surg 134:290–296.  https://doi.org/10.1016/j.jtcvs.2007.02.041 CrossRefPubMedGoogle Scholar
  100. Mellis D, Caporali A (2018) MicroRNA-based therapeutics in cardiovascular disease: screening and delivery to the target. Biochem Soc Trans 46:11–21.  https://doi.org/10.1042/BST20170037 CrossRefPubMedGoogle Scholar
  101. Melvinsdottir IH, Lund SH, Agnarsson BA, Sigvaldason K, Gudbjartsson T, Geirsson A (2016) The incidence and mortality of acute thoracic aortic dissection: results from a whole nation study. Eur J Cardiothorac Surg 50:1111–1117.  https://doi.org/10.1093/ejcts/ezw235 CrossRefPubMedGoogle Scholar
  102. Merk DR et al (2012) miR-29b participates in early aneurysm development in Marfan syndrome. Circ Res 110:312–324.  https://doi.org/10.1161/circresaha.111.253740 CrossRefPubMedGoogle Scholar
  103. Michel J-B, Jondeau G, Milewicz DM (2018) From genetics to response to injury: vascular smooth muscle cells in aneurysms and dissections of the ascending aorta. Cardiovasc Res 114:578–589.  https://doi.org/10.1093/cvr/cvy006 CrossRefPubMedGoogle Scholar
  104. Michelena HI et al (2011) Incidence of aortic complications in patients with bicuspid aortic valves. JAMA 306:1104–1112.  https://doi.org/10.1001/jama.2011.1286 CrossRefPubMedGoogle Scholar
  105. Milewicz DM, Regalado ES, Shendure J, Nickerson DA, Guo D-c (2013) Successes and challenges of using whole exome sequencing to identify novel genes underlying an inherited predisposition for thoracic aortic aneurysms and acute aortic dissections. Trends Cardiovascul Med 24:53–60.  https://doi.org/10.1016/j.tcm.2013.06.004 CrossRefGoogle Scholar
  106. Mill C, George SJ (2012) Wnt signalling in smooth muscle cells and its role in cardiovascular disorders. Cardiovasc Res 95:233–240.  https://doi.org/10.1093/cvr/cvs141 CrossRefPubMedGoogle Scholar
  107. Mitchell PS et al (2008) Circulating microRNAs as stable blood-based markers for cancer detection. Proc Natl Acad Sci U S A 105:10513–10518.  https://doi.org/10.1073/pnas.0804549105 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Mogilyansky E, Rigoutsos I (2013) The miR-17/92 cluster: a comprehensive update on its genomics, genetics, functions and increasingly important and numerous roles in health and disease. Cell Death Differ 20:1603–1614.  https://doi.org/10.1038/cdd.2013.125 CrossRefPubMedPubMedCentralGoogle Scholar
  109. Monaghan MG et al (2018) Exogenous miR-29B delivery through a hyaluronan-based injectable system yields functional maintenance of the infarcted myocardium. Tissue Eng Part A 24:57–67.  https://doi.org/10.1089/ten.TEA.2016.0527 CrossRefPubMedPubMedCentralGoogle Scholar
  110. Okamura H et al (2017) Long-term miR-29b suppression reduces aneurysm formation in a Marfan mouse model. Phys Rep 5:e13257.  https://doi.org/10.14814/phy2.13257 CrossRefGoogle Scholar
  111. Osler W (1886) The bicuspid condition of the aortic valves. Trans Assoc Am Phys 2:185–192Google Scholar
  112. Prakash SK et al (2014) A roadmap to investigate the genetic basis of bicuspid aortic valve and its complications: insights from the International BAVCon (Bicuspid Aortic Valve Consortium). J Am Coll Cardiol 64:832–839.  https://doi.org/10.1016/j.jacc.2014.04.073 CrossRefPubMedPubMedCentralGoogle Scholar
  113. Qiu P, Li L (2002) Histone acetylation and recruitment of serum responsive factor and CREB-binding protein onto SM22 promoter during SM22 gene expression. Circ Res 90:858–865CrossRefGoogle Scholar
  114. Quiat D, Olson EN (2013) MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment. J Clin Invest 123:11–18.  https://doi.org/10.1172/JCI62876 CrossRefPubMedPubMedCentralGoogle Scholar
  115. Rabkin SW (2014) Differential expression of MMP-2, MMP-9 and TIMP proteins in thoracic aortic aneurysm—comparison with and without bicuspid aortic valve: a meta-analysis. VASA 43:433–442.  https://doi.org/10.1024/0301-1526/a000390 CrossRefPubMedGoogle Scholar
  116. Rangrez AY, Massy ZA, Metzinger-Le Meuth V, Metzinger L (2011) miR-143 and miR-145: molecular keys to switch the phenotype of vascular smooth muscle cells. Circ Cardiovasc Genet 4:197–205.  https://doi.org/10.1161/circgenetics.110.958702 CrossRefPubMedGoogle Scholar
  117. Rensen SS, Doevendans PA, van Eys GJ (2007) Regulation and characteristics of vascular smooth muscle cell phenotypic diversity. Neth Hear J 15:100–108CrossRefGoogle Scholar
  118. Ries RJ, Yu W, Holton N, Cao H, Amendt BA (2017) Inhibition of the miR-17-92 cluster separates stages of palatogenesis. J Dent Res 96:1257–1264.  https://doi.org/10.1177/0022034517716915 CrossRefPubMedPubMedCentralGoogle Scholar
  119. Robertson EN, van der Linde D, Sherrah AG, Vallely MP, Wilson M, Bannon PG, Jeremy RW (2016) Familial non-syndromal thoracic aortic aneurysms and dissections—incidence and family screening outcomes. Int J Cardiol 220:43–51.  https://doi.org/10.1016/j.ijcard.2016.06.086 CrossRefPubMedGoogle Scholar
  120. Roman MJ et al (2017) Aortic dilatation associated with bicuspid aortic valve: relation to sex, hemodynamics, and valve morphology (the National Heart Lung and Blood Institute-sponsored national registry of genetically triggered thoracic aortic aneurysms and cardiovascular conditions). Am J Cardiol 120:1171–1175.  https://doi.org/10.1016/j.amjcard.2017.06.061 CrossRefPubMedPubMedCentralGoogle Scholar
  121. Schepers D et al (2018) A mutation update on the LDS-associated genes TGFB2/3 and SMAD2/3. Hum Mutat 39:621–634.  https://doi.org/10.1002/humu.23407 CrossRefPubMedPubMedCentralGoogle Scholar
  122. Schiattarella GG, Madonna R, Van Linthout S, Thum T, Schulz R, Ferdinandy P, Perrino C (2018) Epigenetic modulation of vascular diseases: assessing the evidence and exploring the opportunities. Vasc Pharmacol  https://doi.org/10.1016/j.vph.2018.02.009 CrossRefGoogle Scholar
  123. Shah AA et al (2015) Epigenetic profiling identifies novel genes for ascending aortic aneurysm formation with bicuspid aortic valves. Heart Surg Forum 18:E134–E139.  https://doi.org/10.1532/hsf.1247 CrossRefPubMedGoogle Scholar
  124. Sherrah AG et al (2016) Nonsyndromic thoracic aortic aneurysm and dissection. JACC 67:618–626.  https://doi.org/10.1016/j.jacc.2015.11.039 CrossRefPubMedGoogle Scholar
  125. Sievers HH, Stierle U, Hachmann RM, Charitos EI (2016) New insights in the association between bicuspid aortic valve phenotype, aortic configuration and valve haemodynamics. Eur J Cardiothorac Surg 49:439–446.  https://doi.org/10.1093/ejcts/ezv087 CrossRefPubMedGoogle Scholar
  126. Simion V, Haemmig S, Feinberg MW (2018) LncRNAs in vascular biology and disease. Vasc Pharmacol  https://doi.org/10.1016/j.vph.2018.01.003
  127. Siu SC, Silversides CK (2010) Bicuspid aortic valve disease. JACC 55:2789–2800.  https://doi.org/10.1016/j.jacc.2009.12.068 CrossRefPubMedGoogle Scholar
  128. Song Z, Jin R, Yu S, Nanda A, Granger DN, Li G (2012) Crucial role of CD40 signaling in vascular wall cells in neointimal formation and vascular remodeling after vascular interventions. Arterioscler Thromb Vasc Biol 32:50–64.  https://doi.org/10.1161/ATVBAHA.111.238329 CrossRefPubMedGoogle Scholar
  129. Takada S, Berezikov E, Choi YL, Yamashita Y, Mano H (2009) Potential role of miR-29b in modulation of Dnmt3a and Dnmt3b expression in primordial germ cells of female mouse embryos. RNA 15:1507–1514.  https://doi.org/10.1261/rna.1418309 CrossRefPubMedPubMedCentralGoogle Scholar
  130. Tollefsbol TO (2018) Chapter 1—epigenetics of human disease. In: Tollefsbol TO (ed) Epigenetics in human disease, vol 6. 2nd edn. Academic Press, pp 3–10.  https://doi.org/10.1016/B978-0-12-812215-0.00001-7 CrossRefGoogle Scholar
  131. Tzemos N et al (2008) Outcomes in adults with bicuspid aortic valves. JAMA 300:1317–1325.  https://doi.org/10.1001/jama.300.11.1317 CrossRefPubMedGoogle Scholar
  132. van Rooij E et al (2008) Dysregulation of microRNAs after myocardial infarction reveals a role of miR-29 in cardiac fibrosis. Proc Natl Acad Sci U S A 105:13027–13032.  https://doi.org/10.1073/pnas.0805038105 CrossRefPubMedPubMedCentralGoogle Scholar
  133. Verdone L, Caserta M, Mauro ED (2005) Role of histone acetylation in the control of gene expression. Biochem Cell Biol 83:344–353CrossRefGoogle Scholar
  134. Verhagen JMA et al (2018) Expert consensus recommendations on the cardiogenetic care for patients with thoracic aortic disease and their first-degree relatives. Int J Cardiol 258:243–248.  https://doi.org/10.1016/j.ijcard.2018.01.145 CrossRefPubMedGoogle Scholar
  135. Wang J et al (2013) MicroRNA-17-92, a direct Ap-2alpha transcriptional target, modulates T-box factor activity in orofacial clefting. PLoS Genet 9:e1003785.  https://doi.org/10.1371/journal.pgen.1003785 CrossRefPubMedPubMedCentralGoogle Scholar
  136. Wang LL et al (2017) Local and sustained miRNA delivery from an injectable hydrogel promotes cardiomyocyte proliferation and functional regeneration after ischemic injury. Nat Biomed Eng 1:983–992.  https://doi.org/10.1038/s41551-017-0157-y CrossRefPubMedPubMedCentralGoogle Scholar
  137. Wang S et al (2015) BRG1 expression is increased in thoracic aortic aneurysms and regulates proliferation and apoptosis of vascular smooth muscle cells through the long non-coding RNA HIF1A-AS1 in vitro. Eur J Cardiothorac Surg 47:439–446.  https://doi.org/10.1093/ejcts/ezu215 CrossRefPubMedGoogle Scholar
  138. Wang X et al (2018) Dual-targeted theranostic delivery of miRs arrests abdominal aortic aneurysm development. Mol Ther 26:1056–1065.  https://doi.org/10.1016/j.ymthe.2018.02.010 CrossRefPubMedGoogle Scholar
  139. Webster ALH, Yan MS-C, Marsden PA (2013) Epigenetics and cardiovascular disease. Can J Cardiol 29:46–57.  https://doi.org/10.1016/j.cjca.2012.10.023 CrossRefPubMedGoogle Scholar
  140. Wu J et al (2016) Progressive aortic dilation is regulated by miR-17-associated miRNAs. JACC 67:2965–2977.  https://doi.org/10.1016/j.jacc.2016.04.027 CrossRefPubMedGoogle Scholar
  141. Wutz A, Rasmussen TP, Jaenisch R (2002) Chromosomal silencing and localization are mediated by different domains of Xist RNA. Nat Genet 30:167–174.  https://doi.org/10.1038/ng820 CrossRefPubMedGoogle Scholar
  142. Xin M et al (2009) MicroRNAs miR-143 and miR-145 modulate cytoskeletal dynamics and responsiveness of smooth muscle cells to injury. Genes Dev 23:2166–2178.  https://doi.org/10.1101/gad.1842409 CrossRefPubMedPubMedCentralGoogle Scholar
  143. Yang X, Du WW, Li H, Liu F, Khorshidi A, Rutnam ZJ, Yang BB (2013) Both mature miR-17-5p and passenger strand miR-17-3p target TIMP3 and induce prostate tumor growth and invasion. Nucleic Acids Res 41:9688–9704.  https://doi.org/10.1093/nar/gkt680 CrossRefPubMedPubMedCentralGoogle Scholar
  144. Yang X, Han H, De Carvalho Daniel D, Lay Fides D, Jones Peter A, Liang G (2014) Gene body methylation can alter gene expression and is a therapeutic target in cancer. Cancer Cell 26:577–590.  https://doi.org/10.1016/j.ccr.2014.07.028 CrossRefPubMedPubMedCentralGoogle Scholar
  145. Yu C, Jeremy RW (2018) Angiotensin, transforming growth factor β and aortic dilatation in Marfan syndrome: of mice and humans. Int J Cardiol Heart Vasc 18:71–80.  https://doi.org/10.1016/j.ijcha.2018.02.009 CrossRefPubMedPubMedCentralGoogle Scholar
  146. Yu CK, Xu TN, Assoian RK, Rader DJ (2018) Mining the stiffness-sensitive transcriptome in human vascular smooth muscle cells identifies long noncoding RNA stiffness regulators. Arterioscler Thromb Vasc Biol 38:164–173.  https://doi.org/10.1161/ATVBAHA.117.310237 CrossRefPubMedGoogle Scholar
  147. Yue M et al (2018) MSDD: a manually curated database of experimentally supported associations among miRNAs, SNPs and human diseases. Nucleic Acids Res 46:D181–D185.  https://doi.org/10.1093/nar/gkx1035 CrossRefPubMedGoogle Scholar
  148. Zhao Y, Feng G, Wang Y, Yue Y, Zhao W (2014) Regulation of apoptosis by long non-coding RNA HIF1A-AS1 in VSMCs: implications for TAA pathogenesis. Int J Clin Exp Pathol 7:7643–7652PubMedPubMedCentralGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Discipline of Pathology and Bosch InstituteThe University of SydneySydneyAustralia
  2. 2.Cardiology DepartmentRoyal Prince Alfred HospitalSydneyAustralia

Personalised recommendations