342
Views
16
CrossRef citations to date
0
Altmetric
Research Article

Effects of ambient ozone exposure on circulating extracellular vehicle microRNA levels in coronary artery disease patients

ORCID Icon, , , &

References

  • An, Z., Y. Jin, J. Li, W. Li, and W. Wu. 2018. Impact of particulate air pollution on cardiovascular health. Curr. Allergy Asthma Rep. 18:15. doi:10.1007/s11882-018-0768-8.
  • Breen, M., S. Y. Chang, M. Breen, Y. Xu, V. Isakov, S. Arunachalam, M. S. Carraway, and R. Devlin. 2020. Fine-Scale modeling of individual exposures to ambient PM2.5, EC, NOx, and CO for the coronary artery disease and environmental exposure (CADEE) study. Atmosphere 11:65. doi:10.3390/atmos11010065.
  • Breen, M., Y. Xu, A. Schneider, R. Williams, and R. Devlin. 2018. Modeling individual exposures to ambient PM2.5 in the diabetes and the environment panel study (DEPS). Sci. Total Environ. 626:807–16. doi:10.1016/j.scitotenv.2018.01.139.
  • Breen, M. S., T. C. Long, B. D. Schultz, R. W. Williams, J. Richmond-Bryant, M. Breen, J. E. Langstaff, R. B. Devlin, A. Schneider, J. M. Burke, et al. 2015. Air pollution exposure model for individuals (EMI) in health studies: Evaluation for ambient PM2.5 in Central North Carolina. Environ. Sci. Technol. 49:14184–94. doi:10.1021/acs.est.5b02765.
  • Breitner, S., A. Schneider, R. B. Devlin, C. K. Ward-Caviness, D. Diaz-Sanchez, L. M. Neas, W. E. Cascio, A. Peters, E. R. Hauser, S. H. Shah, et al. 2016. Associations among plasma metabolite levels and short-term exposure to PM2.5 and ozone in a cardiac catheterization cohort. Environ. Int. 97:76–84. doi:10.1016/j.envint.2016.10.012.
  • Bronze-da-Rocha, E. 2014. MicroRNAs expression profiles in cardiovascular diseases. Biomed. Res. Int. 2014:985408. doi:10.1155/2014/985408.
  • Brook, R. D., S. Rajagopalan, C. A. Pope 3rd, J. R. Brook, A. Bhatnagar, A. V. Diez-Roux, F. Holguin, Y. Hong, R. V. Luepker, M. A. Mittleman, et al., 2010. Particulate matter air pollution and cardiovascular disease: An update to the scientific statement from the American Heart Association Circulation 121: 2331–78. doi: 10.1161/CIR.0b013e3181dbece1.
  • Cao, R. Y., Q. Li, Y. Miao, Y. Zhang, W. Yuan, L. Fan, G. Liu, Q. Mi, and J. Yang. 2016. The emerging role of microRNA-155 in cardiovascular diseases. Biomed. Res. Int. 2016:9869208. doi:10.1155/2016/9869208.
  • Chen, Y.-C., Y.-H. Weng, Y.-W. Chiu, and C.-Y. Yang. 2015. Short-term effects of coarse particulate matter on hospital admissions for cardiovascular diseases: A case-crossover study in a tropical city. J. Toxicol. Environ. Health Part A 78:1241–53. doi:10.1080/15287394.2015.1083520.
  • Cheng, Y., and C. Zhang. 2010. MicroRNA-21 in cardiovascular disease. J. Cardiovasc. Transl. Res. 3:251–55. doi:10.1007/s12265-010-9169-7.
  • Chuang, K. J., C. C. Chan, T. C. Su, C. T. Lee, and C. S. Tang. 2007. The effect of urban air pollution on inflammation, oxidative stress, coagulation, and autonomic dysfunction in young adults. Am. J. Respir. Crit. Care Med. 176,:370–76. doi:10.1164/rccm.200611-1627OC.
  • Clay, C. C., K. Maniar-Hew, J. E. Gerriets, T. T. Wang, E. M. Postlethwait, M. J. Evans, J. H. Fontaine, and L. A. Miller. 2014. Early life ozone exposure results in dysregulated innate immune function and altered microRNA expression in airway epithelium. PLoS ONE 9:e90401. doi:10.1371/journal.pone.0090401.
  • Coffey, A. R., M. Kanke, T. L. Smallwood, J. Albright, W. Pitman, R. Z. Gharaibeh, K. Hua, E. Gertz, S. B. Biddinger, R. E. Temel, et al. 2019. microRNA-146a-5p association with the cardiometabolic disease risk factor TMAO. Physiol. Genom. 51:59–71. doi:10.1152/physiolgenomics.00079.2018.
  • Collaborators, G.B.D.R.F. 2018. Global, regional, and national comparative risk assessment of 84 behavioural, environmental and occupational, and metabolic risks or clusters of risks for 195 countries and territories, 1990-2017: A systematic analysis for the Global burden of disease study 2017. Lancet 392: 1923–94. doi:10.1016/S0140-6736(18)32225-6.
  • Dai, B., H. Li, J. Fan, Y. Zhao, Z. Yin, X. Nie, D. W. Wang, and C. Chen. 2018. MiR-21 protected against diabetic cardiomyopathy induced diastolic dysfunction by targeting gelsolin. Cardiovasc. Diabetol. 17:123. doi:10.1186/s12933-018-0767-z.
  • Day, D. B., J. Xiang, J. Mo, F. Li, M. Chung, J. Gong, C. J. Weschler, P. A. Ohman-Strickland, J. Sundell, W. Weng, et al. 2017. Association of ozone exposure with cardiorespiratory pathophysiologic mechanisms in healthy adults. J. Am. Med. Assoc. Intern. Med. 177:1344–53.
  • Faccini, J., J. B. Ruidavets, P. Cordelier, F. Martins, J. J. Maoret, V. Bongard, J. Ferrieres, J. Roncalli, M. Elbaz, and C. Vindis. 2017. Circulating miR-155, miR-145 and let-7c as diagnostic biomarkers of the coronary artery disease. Sci. Rep. 7:42916. doi:10.1038/srep42916.
  • Fernandez-Hernando, C., and Y. Suarez. 2018. MicroRNAs in endothelial cell homeostasis and vascular disease. Curr. Opin. Hematol. 25:227–36. doi:10.1097/MOH.0000000000000424.
  • Fry, R. C., J. E. Rager, R. Bauer, E. Sebastian, D. B. Peden, I. Jaspers, and N. E. Alexis. 2014. Air toxics and epigenetic effects: Ozone altered microRNAs in the sputum of human subjects. Am. J. Physiol. Lung Cell Mol. Physiol. 306:L1129–L1137. doi:10.1152/ajplung.00348.2013.
  • Fuentes, N., A. Roy, V. Mishra, N. Cabello, and P. Silveyra. 2018. Sex-specific microRNA expression networks in an acute mouse model of ozone-induced lung inflammation. Biol. Sex Differ. 9:18. doi:10.1186/s13293-018-0177-7.
  • Furuyama, A., S. Kanno, T. Kobayashi, and S. Hirano. 2009. Extrapulmonary translocation of intratracheally instilled fine and ultrafine particles via direct and alveolar macrophage-associated routes. Arch. Toxicol. 83:429–37. doi:10.1007/s00204-008-0371-1.
  • Ghio, A. J., M. S., C. Carraway, and R. B. Devlin. 2012. Composition of air pollution particles and oxidative stress in cells, tissues and living systems. J. Toxicol. Environ. Health B. 15:1–21. doi:10.1080/10937404.2012.632359.
  • Ghio, A. J., C. Kim, and R. B. Devlin. 2000. Concentrated ambient air particles induce mild pulmonary inflammation in healthy human volunteers. Am. J. Respir. Crit. Care Med. 162:981–88. doi:10.1164/ajrccm.162.3.9911115.
  • Hammond, S. M. 2015. An overview of microRNAs. Adv. Drug Deliv. Rev. 87:3–14. doi:10.1016/j.addr.2015.05.001.
  • Heron, M. 2018. Deaths: Leading causes for 2016. Natl. Vital Stat. Rep. 67:1–77.
  • Jia, Q. W., Z. H. Chen, X. Q. Ding, J. Y. Liu, P. C. Ge, F. H. An, L. H. Li, L. S. Wang, W. Z. Ma, Z. J. Yang, et al. 2017. Predictive effects of circulating miR-221, miR-130a and miR-155 for coronary heart disease: A multi-ethnic study in China. Cell. Physiol. Biochem. 42:808–23. doi:10.1159/000478071.
  • Jin, F., and J. Xing. 2018. Circulating miR-126 and miR-130a levels correlate with lower disease risk, disease severity, and reduced inflammatory cytokine levels in acute ischemic stroke patients. Neurol. Sci. 39:1757–65. doi:10.1007/s10072-018-3499-7.
  • Kao, C. Y., and E. T. Papoutsakis. 2019. Extracellular vesicles: Exosomes, microparticles, their parts, and their targets to enable their biomanufacturing and clinical applications. Curr. Opin. Biotechnol. 60:89–98. doi:10.1016/j.copbio.2019.01.005.
  • Krauskopf, J., K. van Veldhoven, M. Chadeau-Hyam, R. Vermeulen, G. Carrasco-Turigas, M. Nieuwenhuijsen, P. Vineis, T. M. de Kok, and J. C. Kleinjans. 2019. Short-term exposure to traffic-related air pollution reveals a compound-specific circulating miRNA profile indicating multiple disease risks. Environ. Int. 128:193–200. doi:10.1016/j.envint.2019.04.063.
  • Kurtz, M. L., F. Astort, C. Lezon, S. A. Ferraro, G. A. Magloine, N. S. Orona, S. M. Friedman, P. M. Boyer, and D. R. Tasat. 2018. Oxidative stress response to air pollution in a rat nutritional growth retardation model. J. Toxicol. Environ. Health Part A. 81:1028–40. doi:10.1080/15287394.2018.1519747.
  • Lawal, A. O. 2017. Air particulate matter induced oxidative stress and inflammation in cardiovascular disease and atherosclerosis: The role of Nrf2 and AhR-mediated pathways. Toxicol. Lett. 270:88–95. doi:10.1016/j.toxlet.2017.01.017.
  • Li, H., P. Zhang, F. Li, G. Yuan, X. Wang, A. Zhang, and F. Li. 2019. Plasma miR-22-5p, miR-132-5p, and miR-150-3p are associated with acute myocardial infarction. Biomed. Res. Int. 2019:5012648.
  • Li, X., D. Kong, H. Chen, S. Liu, H. Hu, T. Wu, J. Wang, W. Chen, Y. Ning, Y. Li, et al. 2016. miR-155 acts as an anti-inflammatory factor in atherosclerosis-associated foam cell formation by repressing calcium-regulated heat stable protein 1. Sci. Rep. 6:21789. doi:10.1038/srep21789.
  • Liu, Q., W. Wang, and W. Jing. 2019. Indoor air pollution aggravates asthma in Chinese children and induces the changes in serum level of miR-155. Int. J. Environ. Health Res. 29:22–30. doi:10.1080/09603123.2018.1506569.
  • Louwies, T., C. Vuegen, L. I. Panis, B. Cox, K. Vrijens, T. S. Nawrot, and P. De Boever. 2016. miRNA expression profiles and retinal blood vessel calibers are associated with short-term particulate matter air pollution exposure. Environ. Res. 147:24–31. doi:10.1016/j.envres.2016.01.027.
  • Luo, X. Y., X. Q. Zhu, Y. Li, X. B. Wang, W. Yin, Y. S. Ge, and W. M. Ji. 2018. MicroRNA-150 restores endothelial cell function and attenuates vascular remodeling by targeting PTX3 through the NF-kappaB signaling pathway in mice with acute coronary syndrome. Cell Biol. Int. 42:1170–81. doi:10.1002/cbin.10985.
  • Medina-Ramon, M., and J. Schwartz. 2008. Who is more vulnerable to die from ozone air pollution? Epidemiology 19:672–79. doi:10.1097/EDE.0b013e3181773476.
  • Mirowsky, J. E., M. S. Carraway, R. Dhingra, H. Tong, L. Neas, D. Diaz-Sanchez, W. Cascio, M. Case, J. Crooks, E. R. Hauser, et al. 2017. Ozone exposure is associated with acute changes in inflammation, fibrinolysis, and endothelial cell function in coronary artery disease patients. Environ. Health 16:126. doi:10.1186/s12940-017-0335-0.
  • Mozaffarian, D., E. J. Benjamin, A. S. Go, D. K. Arnett, M. J. Blaha, M. Cushman, S. de Ferranti, J. P. Despres, H. J. Fullerton, V. J. Howard, et al., 2015. Heart disease and stroke statistics–2015 update: A report from the American Heart Association Circulation 131: e29–322. doi: 10.1161/CIR.0000000000000152.
  • Nariman-Saleh-Fam, Z., S. Z. Vahed, S. H. Aghaee-Bakhtiari, A. Daraei, Z. Saadatian, H. S. Kafil, B. Yousefi, S. Eyvazi, I. Khaheshi, S. A. Parsa, et al. 2019. Expression pattern of miR-21, miR-25 and PTEN in peripheral blood mononuclear cells of patients with significant or insignificant coronary stenosis. Gene 698:170–78. doi:10.1016/j.gene.2019.02.074.
  • Nuvolone, D., D. Balzi, P. Pepe, M. Chini, D. Scala, F. Giovannini, F. Cipriani, and A. Barchielli. 2013. Ozone short-term exposure and acute coronary events: A multicities study in Tuscany (Italy). Environ. Res. 126:17–23. doi:10.1016/j.envres.2013.08.002.
  • Paterson, M. R., and A. J. Kriegel. 2017. MiR-146a/b: A family with shared seeds and different roots. Physiol. Genom. 49:243–52. doi:10.1152/physiolgenomics.00133.2016.
  • Pereira-da-Silva, T., M. Coutinho Cruz, C. Carrusca, R. Cruz Ferreira, P. Napoleao, and M. Mota Carmo. 2018. Circulating microRNA profiles in different arterial territories of stable atherosclerotic disease: A systematic review. Am. J. Cardiovasc. Dis. 8:1–13.
  • Qiu, M., J. Ma, J. Zhang, X. Guo, Q. Liu, and Z. Yang. 2019. MicroRNA-150 deficiency accelerates intimal hyperplasia by acting as a novel regulator of macrophage polarization. Life Sci. 240:116985. doi:10.1016/j.lfs.2019.116985
  • Rodosthenous, R. S., B. A. Coull, Q. Lu, P. S. Vokonas, J. D. Schwartz, and A. A. Baccarelli. 2016. Ambient particulate matter and microRNAs in extracellular vesicles: A pilot study of older individuals. Part Fibre Toxicol. 13:13. doi:10.1186/s12989-016-0121-0.
  • Rodosthenous, R. S., I. Kloog, E. Colicino, J. Zhong, L. A. Herrera, P. Vokonas, J. Schwartz, A. A. Baccarelli, and D. Prada. 2018. Extracellular vesicle-enriched microRNAs interact in the association between long-term particulate matter and blood pressure in elderly men. Environ. Res. 167:640–49. doi:10.1016/j.envres.2018.09.002.
  • Ruiz-Vera, T., A. C. Ochoa-Martinez, L. G. Pruneda-Alvarez, G. Dominguez-Cortinas, and I. N. Perez-Maldonado. 2019. Expression levels of circulating microRNAs-126, −155, and −145 in Mexican women exposed to polycyclic aromatic hydrocarbons through biomass fuel use. Environ. Mol. Mutagen. 60:546–58. doi:10.1002/em.22273.
  • Salvi, S., A. Blomberg, B. Rudell, F. Kelly, T. Sandstrom, S. T. Holgate, and A. Frew. 1999. Acute inflammatory responses in the airways and peripheral blood after short-term exposure to diesel exhaust in healthy human volunteers. Am. J. Respir. Crit. Care Med. 159:702–09. doi:10.1164/ajrccm.159.3.9709083.
  • Scherrer, N., F. Fays, B. Mueller, A. Luft, F. Fluri, M. Christ-Crain, Y. Devaux, and M. Katan. 2017. MicroRNA 150-5p improves risk classification for mortality within 90 days after acute ischemic stroke. J. Stroke 19:323–32. doi:10.5853/jos.2017.00423.
  • Schmittgen, T. D., and K. J. Livak. 2008. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3:1101–08. doi:10.1038/nprot.2008.73.
  • Snow, S. J., W. Y. Cheng, A. Henriquez, M. Hodge, V. Bass, G. M. Nelson, G. Carswell, J. E. Richards, M. C. Schladweiler, A. D. Ledbetter, et al. 2018. Ozone-induced vascular contractility and pulmonary injury are differentially impacted by diets enriched with coconut oil, fish oil, and olive oil. Toxicol. Sci. 163:57–69. doi:10.1093/toxsci/kfy003.
  • Syed, M., J. P. Ball, K. W. Mathis, M. E. Hall, M. J. Ryan, M. E. Rothenberg, L. L. Yanes Cardozo, and D. G. Romero. 2018. MicroRNA-21 ablation exacerbates aldosterone-mediated cardiac injury, remodeling, and dysfunction. Am. J. Physiol. Endocrinol. Metab. 315:E1154E1167. doi:10.1152/ajpendo.00155.2018.
  • Tran Quang, T., B. Rozec, L. Audigane, and C. Gauthier. 2009. Investigation of the different adrenoceptor targets of nebivolol enantiomers in rat thoracic aorta. Br. J. Pharmacol. 156:601–08. doi:10.1111/j.1476-5381.2009.00074.x.
  • Tsai, -S.-S., C.-Y. Tsai, and C.-Y. Yang. 2018. Fine particulate air pollution associated with risk of hospital admissions for hypertension in a tropical city, Kaohsiung, Taiwan. J. Toxicol. Environ. Health Part A 81:567–75. doi:10.1080/15287394.2018.1460788.
  • van Eeden, S. F., W. C. Tan, T. Suwa, H. Mukae, T. Terashima, T. Fujii, D. Qui, R. Vincent, and J. C. Hogg. 2001. Cytokines involved in the systemic inflammatory response induced by exposure to particulate matter air pollutants (PM(10)). Am. J. Respir. Crit. Care Med. 164:826–30. doi:10.1164/ajrccm.164.5.2010160.
  • Wang, W., Y. Zheng, M. Wang, M. Yan, J. Jiang, and Z. Li. 2019. Exosomes derived miR-126 attenuates oxidative stress and apoptosis from ischemia and reperfusion injury by targeting ERRFI1. Gene 690:75–80. doi:10.1016/j.gene.2018.12.044.
  • WHO. 2018. The top 10 causes of death. Geneva, Switzerland: World Health Organization.
  • Xiao, J., Y. Pan, X. H. Li, X. Y. Yang, Y. L. Feng, H. H. Tan, L. Jiang, J. Feng, and X. Y. Yu. 2016. Cardiac progenitor cell-derived exosomes prevent cardiomyocytes apoptosis through exosomal miR-21 by targeting PDCD4. Cell Death Dis. 7:e2277. doi:10.1038/cddis.2016.181.
  • Xiao, Q., X. Zhu, S. Yang, J. Wang, R. Yin, J. Song, A. Ma, and X. Pan. 2019a. LPS induces CXCL16 expression in HUVECs through the miR-146a-mediated TLR4 pathway. Int. Immunopharmacol. 69:143–49. doi:10.1016/j.intimp.2019.01.011.
  • Xiao, T., M. Ling, H. Xu, F. Luo, J. Xue, C. Chen, J. Bai, Q. Zhang, Y. Wang, Q. Bian, et al. 2019b. NF-kappaB-regulation of miR-155, via SOCS1/STAT3, is involved in the PM2.5-accelerated cell cycle and proliferation of human bronchial epithelial cells. Toxicol. Appl. Pharmacol. 377:114616. doi:10.1016/j.taap.2019.114616.
  • Xue, S., D. Liu, W. Zhu, Z. Su, L. Zhang, C. Zhou, and P. Li. 2019. Circulating MiR-17-5p, MiR-126-5p and MiR-145-3p are novel biomarkers for diagnosis of acute myocardial infarction. Front. Physiol. 10:123. doi:10.3389/fphys.2019.00123.
  • Yang, J., Y. Liu, X. Fan, Z. Li, and Y. Cheng. 2014. A pathway and network review on beta-adrenoceptor signaling and beta blockers in cardiac remodeling. Heart Fail Rev. 19:799–814. doi:10.1007/s10741-013-9417-4.
  • Zhao, D., J. Zhao, J. Sun, Y. Su, J. Jian, H. Ye, J. Lin, Z. Yang, J. Feng, and Z. Wang. 2018. The expression level of miR-155 in plasma and peripheral blood mononuclear cells in coronary artery disease patients and the associations of these levels with the apoptosis rate of peripheral blood mononuclear cells. Exp. Ther. Med. 16:4373–78. doi:10.3892/etm.2018.6797.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.