Log in

Identification and characterization of MicroRNAs in acrolein-stimulated endothelial cells: Implications for vascular disease

  • Original Article
  • Published:
BioChip Journal Aims and scope Submit manuscript

Abstract

MicroRNAs (miRNAs) have been implicated in the regulation of physiological and pathophysiological processes such as vascular disease. Analysis of miRNA expression profiles in vascular disease provides new insights into the possible mechanisms underlying and therapeutic targets of disease. Acrolein is a highly reactive component of cigarette smoke, which has been implicated in the development of vascular disease. In this study, we investigated whether miRNAs play a role in the modulation of various gene expression responses to acrolein in human endothelial cells. We analyzed whole-genome miRNA and mRNA expression and found that acrolein induced differential expression of 151 miRNAs in endothelial cells. We further classified a number of target genes of the differentially expressed miRNAs. Among the differentially expressed miRNAs, miR-342-3p and 422a were upregulated, and the expression levels demonstrated a high inverse correlation with their targets, the vascular disease- related genes CLDN1 and PON1. Thus, integrating specific patterns of miRNA and mRNA levels may improve the diagnosis of vascular diseases induced by exposure to environmental pollutants such as acrolein.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Gutierrez, E. et al. Endothelial dysfunction over the course of coronary artery disease. Eur. Heart J. 34, 3175–3181 (2013).

    Article  Google Scholar 

  2. Reilly, M.P. Tobacco-related cardiovascular diseases in the 21st century. Arterioscler. Thromb. Vasc. Biol. 33, 1458–1459 (2014).

    Article  Google Scholar 

  3. Aldini, G., Orioli, M. & Carini, M. Protein modification by acrolein: relevance to pathological conditions and inhibition by aldehyde sequestering agents. Mol. Nutr. Food Res. 55, 1301–1319 (2011).

    Article  CAS  Google Scholar 

  4. Abraham, K. et al. Toxicology and risk assessment of acrolein in food. Mol. Nutr. Food Res. 55, 1277–1290 (2011).

    Article  CAS  Google Scholar 

  5. Myers, C.R., Myers, J.M., Kufahl, T.D., Forbes, R. & Szadkowski, A. The effects of acrolein on the thioredoxin system: implications for redox-sensitive signaling. Mol. Nutr. Food Res. 55, 1361–1374 (2011).

    Article  CAS  Google Scholar 

  6. Moretto, N., Volpi, G., Pastore, F. & Facchinetti, F. Acrolein effects in pulmonary cells: relevance to chronic obstructive pulmonary disease. Ann. N. Y. Acad. Sci. 1259, 39–46 (2012).

    Article  CAS  Google Scholar 

  7. Sultana, R., Perluigi, M. & Butterfield, D.A. Lipid peroxidation triggers neurodegeneration: A redox proteomics view into the Alzheimer disease brain. Free Radic. Biol. Med. 62, 157–169 (2013).

    Article  CAS  Google Scholar 

  8. Anderson, E.J., Katunga, L.A. & Willis, M.S. Mitochondria as a source and target of lipid peroxidation products in healthy and diseased heart. Clin. Exp. Pharmacol. Physiol. 39, 179–193 (2012).

    CAS  Google Scholar 

  9. Bartel, D.P. MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell 116, 281–297 (2004).

    Article  CAS  Google Scholar 

  10. Zeng, Y. Principles of micro-RNA production and maturation. Oncogene 25, 6156–6162 (2006).

    Article  CAS  Google Scholar 

  11. Hayashita, Y. et al. A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res. 65, 9628–9632 (2005).

    Article  CAS  Google Scholar 

  12. Jovanovic, M. & Hengartner, M.O. miRNAs and apoptosis: RNAs to die for. Oncogene 25, 6176–6187 (2006).

    Article  CAS  Google Scholar 

  13. Schickel, R., Boyerinas, B., Park, S.M. & Peter, M.E. MicroRNAs: key players in the immune system, differentiation, tumorigenesis and cell death. Oncogene 27, 5959–5974 (2008).

    Article  CAS  Google Scholar 

  14. Joshi, S.R., McLendon, J.M., Comer, B.S. & Gerthoffer, W.T. MicroRNAs-control of essential genes: Implications for pulmonary vascular disease. Pulm Circ. 1, 357–364 (2011).

    Article  CAS  Google Scholar 

  15. Sayed, A.S., **a, K., Salma, U., Yang, T. & Peng, J. Diagnosis, Prognosis and Therapeutic Role of Circulating miRNAs in Cardiovascular Diseases. Heart, Lung &Circulation 23, 503–510 (2014).

    Article  Google Scholar 

  16. Lee, S.E. et al. MicroRNA and gene expression analysis of melatonin-exposed human breast cancer cell lines indicating involvement of the anticancer effect. J. Pineal Res. 51, 345–352 (2011).

    Article  CAS  Google Scholar 

  17. Katoh, M. Therapeutics targeting angiogenesis: genetics and epigenetics, extracellular miRNAs and signaling networks (Review). Int. J. Mol. Med. 32, 763–767 (2013).

    CAS  Google Scholar 

  18. An, Y.R. & Hwang, S.Y. Toxicology study with micro-RNA. Mol. Cell. Toxicol. 10, 127–134 (2014).

    Article  CAS  Google Scholar 

  19. Sumpio, B.E., Riley, J.T. & Dardik, A. Cells in focus: endothelial cell. Int. J. Biochem Cell Biol. 34, 1508–1512 (2002).

    Article  CAS  Google Scholar 

  20. Lee, S.E. & Park, Y.S. Role of lipid peroxidation-derived alpha, beta-unsaturated aldehydes in vascular dysfunction. Oxid. Med. Cell Longev. 2013, 629028 (2013).

    Google Scholar 

  21. Dennis, G., Jr. et al. DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol. 4, P3 (2003).

    Article  Google Scholar 

  22. Saunders, M.A. & Lim, L.P. (micro)genomic medicine microRNAs as therapeutics and biomarkers. RNA Biol. 6, 324–328 (2009).

    Article  CAS  Google Scholar 

  23. Hoffmann, D., Melikian, A.A. & Brunnemann, K.D. Studies in tobacco carcinogenesis. IARC scientific publications 482–484 (1991).

    Google Scholar 

  24. Ranganna, K. et al. Acrolein activates mitogen-activated protein kinase signal transduction pathways in rat vascular smooth muscle cells. Mol. Cell. Biochem. 240, 83–98 (2002).

    Article  CAS  Google Scholar 

  25. Lee, S.E. & Park, Y.S. Korean Red Ginseng water extract inhibits COX-2 expression by suppressing p38 in acrolein-treated human endothelial cells. J. Ginseng Res. 38, 34–39 (2014).

    Article  CAS  Google Scholar 

  26. Lovell, M.A., **e, C. & Markesbery, W.R. Acrolein is increased in Alzheimer’s disease brain and is toxic to primary hippocampal cultures. Neurobiology of Aging 22, 187–194 (2001).

    Article  CAS  Google Scholar 

  27. Puranik, R. & Celermajer, D.S. Smoking and endothelial function. Prog. Cardiovasc. Dis. 45, 443–458 (2003).

    Article  CAS  Google Scholar 

  28. Lee, S.E. & Park, Y.S. The role of antioxidant enzymes in adaptive responses to environmental toxicants in vascular disease. Mol. Cell. Toxicol. 9, 95–101 (2013).

    Article  CAS  Google Scholar 

  29. Park, Y.S. et al. Induction of thioredoxin reductase as an adaptive response to acrolein in human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 327, 1058–1065 (2005).

    Article  CAS  Google Scholar 

  30. Foncea, R., Carvajal, C., Almarza, C. & Leighton, F. Endothelial cell oxidative stress and signal transduction. Biol. Res. 33, 89–96 (2000).

    Article  CAS  Google Scholar 

  31. Boren, T. et al. MicroRNAs and their target messenger RNAs associated with endometrial carcinogenesis. Gynecol. Oncol. 110, 206–215 (2008).

    Article  CAS  Google Scholar 

  32. Blower, P.E. et al. MicroRNA expression profiles for the NCI-60 cancer cell panel. Mol. Cancer Ther. 6, 1483–1491 (2007).

    Article  CAS  Google Scholar 

  33. Fickert, P., Moustafa, T. & Trauner, M. Primary sclerosing cholangitis—the arteriosclerosis of the bile duct? Lipids Health Dis. 6, 3 (2007).

    Article  Google Scholar 

  34. Chanet, A. et al. Flavanone metabolites decrease monocyte adhesion to TNF-alpha-activated endothelial cells by modulating expression of atherosclerosis-related genes. Br. J. Nutr. 110, 587–598 (2013).

    Article  CAS  Google Scholar 

  35. Mackness, B. & Mackness, M. Anti-inflammatory properties of paraoxonase-1 in atherosclerosis. Adv. Exp. Med. Biol. 660, 143–151 (2010).

    CAS  Google Scholar 

  36. Rozenberg, O., Rosenblat, M., Coleman, R., Shih, D.M. & Aviram, M. Paraoxonase (PON1) deficiency is associated with increased macrophage oxidative stress: Studies in PON1-knockout mice. Free Radic. Biol. Med. 34, 774–784 (2003).

    Article  CAS  Google Scholar 

  37. Mackness, B., Turkie, W. & Mackness, M. Paraoxonase-1 (PON1) promoter region polymorphisms, serum PON1 status and coronary heart disease. Arch. Med. Sci. 9, 8–13 (2012).

    Google Scholar 

  38. Maloyan, A. et al. Identification and comparative analyses of myocardial miRNAs involved in the fetal response to maternal obesity. Physiol. Genomics 45, 889–900 (2013).

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Yong Seek Park.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, S.E., Yang, H., Son, G.W. et al. Identification and characterization of MicroRNAs in acrolein-stimulated endothelial cells: Implications for vascular disease. BioChip J 9, 144–155 (2015). https://doi.org/10.1007/s13206-015-9303-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13206-015-9303-3

Keywords

Navigation