Advertisement

Molecular Biology Reports

, Volume 45, Issue 6, pp 2883–2896 | Cite as

Recent research progress of microRNAs in hypertension pathogenesis, with a focus on the roles of miRNAs in pulmonary arterial hypertension

  • Chenggui Miao
  • Jun Chang
  • Guoxue Zhang
Review

Abstract

Hypertension is the most widespread disease in the world affecting humans and imparts a significant cardiovascular and renal risk to patients, and extensive research over the past few decades has enhanced our understanding of the underlying pathogenesis of hypertension. A growing number of studies have shown that miRNAs are involved in the pathological mechanisms of hypertension. This review summarizes the current understanding of miRNA-mediated modulation of gene expression in the hypertension pathogenesis in the past few years. A systematic review of PUBMED, EMBASE and SCOPUS was conducted for studies published in the past few years. The review covers three topics: miRNAs in pulmonary arterial hypertension (PAH), miRNAs and systemic arterial hypertension (SAH), miRNAs and application in hypertension. This review summarizes the current understanding of miRNA-mediated modulation in the hypertension pathogenesis in the past few years, with especially emphasis on miRNAs in PAH. We also discussed the roles of miRNAs in SAH, and the therapeutic applications of these miRNAs will be detailed discussed in this review. Evidence suggests that miRNAs are involved in the pathological mechanisms of hypertension, and the roles of miRNAs in the hypertension pathogenesis are confirmed. We need to further investigate the regulated roles of miRNAs in the pathogenesis of hypertension and the application of miRNAs in the diagnosis and treatment of this disease in the future.

Keywords

Hypertension microRNA Pulmonary arterial hypertension Systemic arterial hypertension Therapeutic application 

Abbreviations

MiRNAs

microRNAs

PAH

Pulmonary arterial hypertension

PDGFRa

Platelet-derived growth factor receptor alpha

3′UTR

3′ Untranslated region

COPD

Chronic obstructive pulmonary disease

MCU

Mitochondrial calcium uniporter

MCUC

Mitochondrial calcium uniporter (MCU) complex

Smurf1

SMAD-specific E3 ubiquitin protein ligase 1

HIF-1α

Hypoxia-inducible factor-1α

CDKN

Cyclin-dependent kinase inhibitors

PAEC

Pulmonary artery endothelial cell

ET-1

Endothelin-1

HIF-1α

Hypoxia-inducible factor-1α

CDKN

Cyclin-dependent kinase inhibitors

VSMCs

Vascular smooth muscle cells

CTGF

Connective tissue growth factor

CCND1

Cyclin D1

RUNX2

Runt-related transcription factor 2

NO

Nitric oxide

Mef2

Myocyte enhancer factor 2

SAH

Systemic arterial hypertension

Ang

Angiotensin

mt-Cytb

mtDNA-encoded cytochrome b

AVSMCs

Aortic vascular smooth muscle cells

SHRs

Spontaneously hypertensive rats

IGF1

Insulin-like growth factor 1

SIRT1

Sirtuin-1

CIMT

Carotid intima media thickness

eNOS

Endothelial nitric oxide synthase

MR

Mineralocorticoid receptor

SMCs

Smooth muscle cells

Notes

Acknowledgements

This project was supported by the National Natural Science Foundation of China (No. 81302783), the Stable Talent Personnel Project of Anhui Science and Technology University (No. ZRC2014473), the Excellent talent project of Anhui Science and Technology University (No. XJYXRC201801) and the Anhui Province Key Research and Development Plan (No. 1804a0802218).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. 1.
    Anupama YJ, Hegde SN, Uma G, Patil M (2017) Hypertension is an important risk determinant for chronic kidney disease: results from a cross-sectional, observational study from a rural population in South India. J Hum Hypertens 31:369–370PubMedGoogle Scholar
  2. 2.
    Papathanasiou G, Zerva E, Zacharis I, Papandreou M, Papageorgiou E, Tzima C et al (2015) Association of high blood pressure with body mass index, smoking and physical activity in healthy young adults. Open Cardiovasc Med J 9:5–17PubMedPubMedCentralGoogle Scholar
  3. 3.
    Gupta R, Mohan I, Narula J (2016) Trends in coronary heart disease epidemiology in India. Ann Glob Health 82:307–315PubMedGoogle Scholar
  4. 4.
    Schulte C, Karakas M, Zeller T (2017) microRNAs in cardiovascular disease—clinical application. Clin Chem Lab Med 55:687–704PubMedGoogle Scholar
  5. 5.
    Dua K, Hansbro NG, Foster PS, Hansbro PM (2017) MicroRNAs as therapeutics for future drug delivery systems in treatment of lung diseases. Drug Deliv Transl Res 7:168–178PubMedGoogle Scholar
  6. 6.
    Chen JQ, Papp G, Szodoray P, Zeher M (2016) The role of microRNAs in the pathogenesis of autoimmune diseases. Autoimmun Rev 15:1171–1180PubMedGoogle Scholar
  7. 7.
    Wang G, Wu L, Chen Z, Sun J (2017) Identification of crucial miRNAs and the targets in renal cortex of hypertensive patients by expression profiles. Ren Fail 39:92–99PubMedGoogle Scholar
  8. 8.
    Boucherat O, Potus F, Bonnet S (2015) microRNA and pulmonary hypertension. microRNA 888:237–252Google Scholar
  9. 9.
    Formosa A, Lena AM, Markert EK, Cortelli S, Miano R, Mauriello A et al (2013) DNA methylation silences miR-132 in prostate cancer. Oncogene 32:127–134PubMedGoogle Scholar
  10. 10.
    Davis BN, Hilyard AC, Lagna G, Hata A (2008) SMAD proteins control DROSHA-mediated microRNA maturation. Nature 454:56–61PubMedPubMedCentralGoogle Scholar
  11. 11.
    Green DE, Murphy TC, Kang BY, Searles CD, Hart CM (2015) PPARγ ligands attenuate hypoxia-induced proliferation in human pulmonary artery smooth muscle cells through modulation of MicroRNA-21. PLoS ONE 10:e0133391PubMedPubMedCentralGoogle Scholar
  12. 12.
    Wang P, Xu J, Hou Z, Wang F, Song Y, Wang J et al (2016) miRNA-34a promotes proliferation of human pulmonary artery smooth muscle cells by targeting PDGFRA. Cell Prolif 49:484–493PubMedGoogle Scholar
  13. 13.
    Xing Y, Zheng X, Li G, Liao L, Cao W, Xing H et al (2015) MicroRNA-30c contributes to the development of hypoxia pulmonary hypertension by inhibiting platelet-derived growth factor receptor β expression. Int J Biochem Cell Biol 64:155–166PubMedGoogle Scholar
  14. 14.
    Zeng Y, Liu H, Kang K, Wang Z, Hui G, Zhang X et al (2015) Hypoxia inducible factor-1 mediates expression of miR-322: potential role in proliferation and migration of pulmonary arterial smooth muscle cells. Sci Rep 5:12098PubMedPubMedCentralGoogle Scholar
  15. 15.
    Wang AP, Li XH, Gong SX, Li WQ, Hu CP, Zhang Z et al (2015) miR-100 suppresses mTOR signaling in hypoxia-induced pulmonary hypertension in rats. Eur J Pharmacol 765:565–573PubMedGoogle Scholar
  16. 16.
    Deng B, Du J, Hu R, Wang AP, Wu WH, Hu CP et al (2016) MicroRNA-103/107 is involved in hypoxia-induced proliferation of pulmonary arterial smooth muscle cells by targeting HIF-1β. Life Sci 147:117–124PubMedGoogle Scholar
  17. 17.
    Bertero T, Cottrill K, Krauszman A, Lu Y, Annis S, Hale A et al (2015) The microRNA-130/301 family controls vasoconstriction in pulmonary hypertension. J Biol Chem 290:2069–2085PubMedGoogle Scholar
  18. 18.
    Brock M, Haider TJ, Vogel J, Gassmann M, Speich R, Trenkmann M et al (2015) The hypoxia-induced microRNA-130a controls pulmonary smooth muscle cell proliferation by directly targeting CDKN1A. Int J Biochem Cell Biol 61:129–137PubMedGoogle Scholar
  19. 19.
    Jin Y, Pang T, Nelin LD, Wang W, Wang Y, Yan J et al (2015) MKP-1 is a target of miR-210 and mediate the negative regulation of miR-210 inhibitor on hypoxic hPASMC proliferation. Cell Biol Int 39:113–120PubMedGoogle Scholar
  20. 20.
    White K, Lu Y, Annis S, Hale AE, Chau BN, Dahlman JE et al (2015) Genetic and hypoxic alterations of the microRNA-210-ISCU1/2 axis promote iron-sulfur deficiency and pulmonary hypertension. EMBO Mol Med 7:695–713PubMedPubMedCentralGoogle Scholar
  21. 21.
    Liu H, Tao Y, Chen M, Yu J, Li WJ, Tao L et al (2016) Upregulation of MicroRNA-214 contributes to the development of vascular remodeling in hypoxia-induced pulmonary hypertension via targeting CCNL2. Sci Rep 6:24661PubMedPubMedCentralGoogle Scholar
  22. 22.
    Zeng Y, Zhang X, Kang K, Chen J, Wu Z, Huang J et al (2016) MicroRNA-223 attenuates hypoxia-induced vascular remodeling by targeting RhoB/MLC2 in pulmonary arterial smooth muscle cells. Sci Rep 6:24900PubMedPubMedCentralGoogle Scholar
  23. 23.
    Meloche J, Le Guen M, Potus F, Vinck J, Ranchoux B, Johnson I et al (2015) miR-223 reverses experimental pulmonary arterial hypertension. Am J Physiol Cell Physiol 309:C363–C372PubMedGoogle Scholar
  24. 24.
    Zhang Y, Xu J (2016) MiR-140-5p regulates hypoxia-mediated human pulmonary artery smooth muscle cell proliferation, apoptosis and differentiation by targeting Dnmt1 and promoting SOD2 expression. Biochem Biophys Res Commun 473:342–348PubMedGoogle Scholar
  25. 25.
    Zhang WF, Xiong YW, Zhu TT, Xiong AZ, Bao HH, Cheng XS (2017) MicroRNA let-7g inhibited hypoxia-induced proliferation of PASMCs via G0/G1 cell cycle arrest by targeting c-myc. Life Sci 170:9–15.PubMedGoogle Scholar
  26. 26.
    Zhang WF, Zhu TT, Xiong YW, Xiong AZ, Ge XY, Hu CP et al (2017) Negative feedback regulation between microRNA let-7g and LOX-1 mediated hypoxia-induced PASMCs proliferation. Biochem Biophys Res Commun 488:655–663PubMedGoogle Scholar
  27. 27.
    Hoffmann J, Wilhelm J, Olschewski A, Kwapiszewska G (2016) Microarray analysis in pulmonary hypertension. Eur Respir J 48:229–241PubMedPubMedCentralGoogle Scholar
  28. 28.
    Hong Z, Chen KH, DasGupta A, Potus F, Dunham-Snary K, Bonnet S et al (2017) MicroRNA-138 and MicroRNA-25 down-regulate mitochondrial calcium uniporter, causing the pulmonary arterial hypertension cancer phenotype. Am J Respir Crit Care Med 195:515–529PubMedPubMedCentralGoogle Scholar
  29. 29.
    Wallace E, Morrell NW, Yang XD, Long L, Stevens H, Nilsen M et al (2015) A sex-specific MicroRNA-96/5-hydroxytryptamine 1B axis influences development of pulmonary hypertension. Am J Respir Crit Care Med 191:1432–1442PubMedPubMedCentralGoogle Scholar
  30. 30.
    Chen T, Zhou G, Zhou Q, Tang H, Ibe JC, Cheng H et al (2015) Loss of microRNA-17∼92 in smooth muscle cells attenuates experimental pulmonary hypertension via induction of PDZ and LIM domain 5. Am J Respir Crit Care Med 191:678–692PubMedPubMedCentralGoogle Scholar
  31. 31.
    Rothman AM, Arnold ND, Pickworth JA, Iremonger J, Ciuclan L, Allen RM et al (2016) MicroRNA-140-5p and SMURF1 regulate pulmonary arterial hypertension. J Clin Invest 126:2495–2508PubMedPubMedCentralGoogle Scholar
  32. 32.
    Courboulin A, Paulin R, Giguère NJ, Saksouk N, Perreault T, Meloche J et al (2011) Role for miR-204 in human pulmonary arterial hypertension. J Exp Med 208:535–548PubMedPubMedCentralGoogle Scholar
  33. 33.
    Meloche J, Potus F, Vaillancourt M, Bourgeois A, Johnson I, Deschamps L et al (2015) Bromodomain-containing protein 4: the epigenetic origin of pulmonary arterial hypertension. Circ Res 117:525–535PubMedGoogle Scholar
  34. 34.
    Meloche J, Lampron MC, Nadeau V, Maltais M, Potus F, Lambert C et al (2017) Implication of inflammation and epigenetic readers in coronary artery remodeling in patients with pulmonary arterial hypertension. Arterioscler Thromb Vasc Biol 37:1513–1523PubMedGoogle Scholar
  35. 35.
    Meloche J, Pflieger A, Vaillancourt M, Paulin R, Potus F, Zervopoulos S et al (2014) Role for DNA damage signaling in pulmonary arterial hypertension. Circulation 129:786–797PubMedGoogle Scholar
  36. 36.
    Luo Y, Dong HY, Zhang B, Feng Z, Liu Y, Gao YQ et al (2015) miR-29a-3p attenuates hypoxic pulmonary hypertension by inhibiting pulmonary adventitial fibroblast activation. Hypertension 65:414–420PubMedGoogle Scholar
  37. 37.
    Kang BY, Park KK, Kleinhenz JM, Murphy TC, Green DE, Bijli KM et al (2016) Peroxisome proliferator-activated receptor γ and microRNA 98 in hypoxia-induced endothelin-1 signaling. Am J Respir Cell Mol Biol 54:136–146PubMedPubMedCentralGoogle Scholar
  38. 38.
    Li C, Mpollo MS, Gonsalves CS, Tahara SM, Malik P, Kalra VK (2014) Peroxisome proliferator-activated receptor-α-mediated transcription of miR-199a2 attenuates endothelin-1 expression via hypoxia-inducible factor-1α. J Biol Chem 289:36031–36047PubMedPubMedCentralGoogle Scholar
  39. 39.
    Bi R, Bao C, Jiang L, Liu H, Yang Y, Mei J et al (2015) MicroRNA-27b plays a role in pulmonary arterial hypertension by modulating peroxisome proliferator-activated receptor γ dependent Hsp90-eNOS signaling and nitric oxide production. Biochem Biophys Res Commun 460:469–475PubMedGoogle Scholar
  40. 40.
    Li C, Gonsalves CS, Eiymo Mwa Mpollo MS, Malik P, Tahara SM, Kalra VK (2015) MicroRNA 648 Targets ET-1 mRNA and is cotranscriptionally regulated with MICAL3 by PAX5. Mol Cell Biol 35:514–528PubMedPubMedCentralGoogle Scholar
  41. 41.
    Huber LC, Ulrich S, Leuenberger C, Gassmann M, Vogel J, von Blotzheim LG et al (2015) Featured article: microRNA-125a in pulmonary hypertension: regulator of a proliferative phenotype of endothelial cells. Exp Biol Med 240:1580–1589Google Scholar
  42. 42.
    Bertero T, Lu Y, Annis S, Hale A, Bhat B, Saggar R et al (2014) Systems-level regulation of microRNA networks by miR-130/301 promotes pulmonary hypertension. J Clin Invest 124:3514–3528PubMedPubMedCentralGoogle Scholar
  43. 43.
    Li Y, Huang J, Jiang Z, Zhong Y, Xia M, Wang H et al (2016) 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
  44. 44.
    Sahoo S, Meijles DN, Al Ghouleh I, Tandon M, Cifuentes-Pagano E, Sembrat J et al (2016) MEF2C-MYOCD and leiomodin1 suppression by miRNA-214 promotes smooth muscle cell phenotype switching in pulmonary arterial hypertension. PLoS ONE 11:e0153780PubMedPubMedCentralGoogle Scholar
  45. 45.
    Sang HY, Jin YL, Zhang WQ, Chen LB (2016) Downregulation of microRNA-637 increases risk of hypoxia-induced pulmonary hypertension by modulating expression of cyclin dependent kinase 6 (CDK6) in pulmonary smooth muscle cells. Med Sci Monit 22:4066–4072PubMedPubMedCentralGoogle Scholar
  46. 46.
    Yang F, Li H, Du Y, Shi Q, Zhao L (2017) Downregulation of microRNA–34b is responsible for the elevation of blood pressure in spontaneously hypertensive rats. Mol Med Rep 15:1031–1036PubMedPubMedCentralGoogle Scholar
  47. 47.
    Wang R, Ding X, Zhou S, Li M, Sun L, Xu X et al (2016) Microrna-26b attenuates monocrotaline- induced pulmonary vascular remodeling via targeting connective tissue growth factor (CTGF) and cyclin D1 (CCND1). Oncotarget 7:72746–72757PubMedPubMedCentralGoogle Scholar
  48. 48.
    Deng L, Blanco FJ, Stevens H, Lu R, Caudrillier A, McBride M et al (2015) MicroRNA-143 activation regulates smooth muscle and endothelial cell crosstalk in pulmonary arterial hypertension. Circ Res 117:870–883PubMedPubMedCentralGoogle Scholar
  49. 49.
    Wu D, Talbot CC Jr, Liu Q, Jing ZC, Damico RL, Tuder R et al (2016) Identifying microRNAs targeting Wnt/β-catenin pathway in end-stage idiopathic pulmonary arterial hypertension. J Mol Med 94:875–885PubMedPubMedCentralGoogle Scholar
  50. 50.
    Ruffenach G, Chabot S, Tanguay VF, Courboulin A, Boucherat O, Potus F et al (2016) Role for runt-related transcription factor 2 in proliferative and calcified vascular lesions in pulmonary arterial hypertension. Am J Respir Crit Care Med 194:1273–1285PubMedGoogle Scholar
  51. 51.
    Potus F, Ruffenach G, Dahou A, Thebault C, Breuils-Bonnet S, Tremblay È et al (2015) Downregulation of MicroRNA-126 contributes to the failing right ventricle in pulmonary arterial hypertension. Circulation 132:932–943PubMedGoogle Scholar
  52. 52.
    Joshi SR, Dhagia V, Gairhe S, Edwards JG, McMurtry IF, Gupte SA (2016) MicroRNA-140 is elevated and mitofusin-1 is downregulated in the right ventricle of the Sugen5416/hypoxia/normoxia model of pulmonary arterial hypertension. Am J Physiol Heart Circ Physiol 311:H689–H698PubMedGoogle Scholar
  53. 53.
    Xiao T, Xie L, Huang M, Shen J (2017) Differential expression of microRNA in the lungs of rats with pulmonary arterial hypertension. Mol Med Rep 15:591–596PubMedGoogle Scholar
  54. 54.
    Ogorodnikova N, Arenz C (2015) MicroRNA-145-targeted drug and its preventive effect on pulmonary arterial hypertension (patent WO2012153135 A1). Expert Opin Ther Pat 25:723–727PubMedGoogle Scholar
  55. 55.
    Liu Y, Liu G, Zhang H, Wang J (2016) MiRNA-199a-5p influences pulmonary artery hypertension via downregulating Smad3. Biochem Biophys Res Commun 473:859–866PubMedGoogle Scholar
  56. 56.
    Paulin R, Sutendra G, Gurtu V, Dromparis P, Haromy A, Provencher S et al (2015) A miR-208-Mef2 axis drives the decompensation of right ventricular function in pulmonary hypertension. Circ Res 116:56–69PubMedGoogle Scholar
  57. 57.
    Ekmekcioglu C, Elmadfa I, Meyer AL, Moeslinger T (2016) The role of dietary potassium in hypertension and diabetes. J Physiol Biochem 72:93–106PubMedGoogle Scholar
  58. 58.
    Reiter LM, Christensen DL, Gjesing AP (2016) Renin angiotensinogen system gene polymorphisms and essential hypertension among people of West African descent: a systematic review. J Hum Hypertens 30:467–478PubMedGoogle Scholar
  59. 59.
    Murphy MS, Casselman RC, Tayade C, Smith GN (2015) Differential expression of plasma microRNA in preeclamptic patients at delivery and 1 year postpartum. Am J Obstet Gynecol 213:367.e1–367.e9Google Scholar
  60. 60.
    Celic T, Metzinger-Le Meuth V, Six I, Massy ZA, Metzinger L (2017) The mir-221/222 Cluster is a key player in vascular biology via the fine-tuning of endothelial cell physiology. Curr Vasc Pharmacol 15:40–46PubMedGoogle Scholar
  61. 61.
    Yang Q, Jia C, Wang P, Xiong M, Cui J, Li L et al (2014) MicroRNA-505 identified from patients with essential hypertension impairs endothelial cell migration and tube formation. Int J Cardiol 177:925–934PubMedGoogle Scholar
  62. 62.
    Luo P, Zhang WF, Qian ZX, Xiao LF, Wang H, Zhu TT et al (2016) MiR-590-5p-meidated LOX-1 upregulation promotes Angiotensin II-induced endothelial cell apoptosis. Biochem Biophys Res Commun 471:402–408PubMedGoogle Scholar
  63. 63.
    Wang ZC, Qi J, Liu LM, Li J, Xu HY, Liang B et al (2017) Valsartan reduces AT1-AA-induced apoptosis through suppression oxidative stress mediated ER stress in endothelial progenitor cells. Eur Rev Med Pharmacol Sci 21:1159–1168PubMedGoogle Scholar
  64. 64.
    Shi J, Bei Y, Kong X, Liu X, Lei Z, Xu T et al (2017) miR-17-3p contributes to exercise-induced cardiac growth and protects against myocardial ischemia-reperfusion injury. Theranostics 7:664–676PubMedPubMedCentralGoogle Scholar
  65. 65.
    Li H, Zhang X, Wang F, Zhou L, Yin Z, Fan J et al (2016) MicroRNA-21 lowers blood pressure in spontaneous hypertensive rats by upregulating mitochondrial translation. Circulation 134:734–751PubMedPubMedCentralGoogle Scholar
  66. 66.
    Nosalski R, McGinnigle E, Siedlinski M, Guzik TJ (2017) Novel immune mechanisms in hypertension and cardiovascular risk. Curr Cardiovasc Risk Rep 11:12–19PubMedPubMedCentralGoogle Scholar
  67. 67.
    Huang Y, Tang S, Huang C, Chen J, Li J, Cai A et al (2017) Circulating miRNA29 family expression levels in patients with essential hypertension as potential markers for left ventricular hypertrophy. Clin Exp Hypertens 39:119–125PubMedGoogle Scholar
  68. 68.
    Parthenakis F, Marketou M, Kontaraki J, Patrianakos A, Nakou H, Touloupaki M et al (2017) Low levels of MicroRNA-21 are a marker of reduced arterial stiffness in well-controlled hypertension. J Clin Hypertens 19:235–240Google Scholar
  69. 69.
    Zhang B, Yao Y, Sun QF, Liu SQ, Jing B, Yuan C et al (2017) Circulating mircoRNA-21 as a predictor for vascular restenosis after interventional therapy in patients with lower extremity arterial occlusive disease. Biosci Rep 37:502–509Google Scholar
  70. 70.
    Bertero T, Cottrill KA, Lu Y, Haeger CM, Dieffenbach P, Annis S et al (2015) Matrix remodeling promotes pulmonary hypertension through feedback mechanoactivation of the YAP/TAZ-miR-130/301 circuit. Cell Rep 13:1016–1032PubMedPubMedCentralGoogle Scholar
  71. 71.
    Carr G, Barrese V, Stott JB, Povstyan OV, Jepps TA, Figueiredo HB et al (2016) MicroRNA-153 targeting of KCNQ4 contributes to vascular dysfunction in hypertension. Cardiovasc Res 112:581–589PubMedPubMedCentralGoogle Scholar
  72. 72.
    Wang S, Tang L, Zhou Q, Lu D, Duan W, Chen C et al (2017) miR-185/P2Y6 axis inhibits angiotensin ii-induced human aortic vascular smooth muscle cell proliferation. DNA Cell Biol.  https://doi.org/10.1089/dna.2016.3605 CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Liu K, Ying Z, Qi X, Shi Y, Tang Q (2015) MicroRNA-1 regulates the proliferation of vascular smooth muscle cells by targeting insulin-like growth factor 1. Int J Mol Med 36:817–824PubMedGoogle Scholar
  74. 74.
    Hu X, Chi L, Zhang W, Bai T, Zhao W, Feng Z et al (2015) Down-regulation of the miR-543 alleviates insulin resistance through targeting the SIRT1. Biochem Biophys Res Commun 468:781–787PubMedGoogle Scholar
  75. 75.
    Sarrion I, Milian L, Juan G, Ramon M, Furest I, Carda C et al (2015) Role of circulating miRNAs as biomarkers in idiopathic pulmonary arterial hypertension: possible relevance of miR-23a. Oxid Med Cell Longev 2015:792846PubMedPubMedCentralGoogle Scholar
  76. 76.
    Han W, Han Y, Liu X, Shang X (2015) Effect of miR-29a inhibition on ventricular hypertrophy induced by pressure overload. Cell Biochem Biophys 71:821–826PubMedGoogle Scholar
  77. 77.
    Huang Y, Tang S, Ji-Yan C, Huang C, Li J, Cai AP et al (2017) Circulating miR-92a expression level in patients with essential hypertension: a potential marker of atherosclerosis. J Hum Hypertens 31:200–205PubMedGoogle Scholar
  78. 78.
    Huang Y, Chen J, Zhou Y, Tang S, Li J, Yu X et al (2016) Circulating miR155 expression level is positive with blood pressure parameters: potential markers of target-organ damage. Clin Exp Hypertens 38:331–336PubMedGoogle Scholar
  79. 79.
    Cengiz M, Yavuzer S, Kılıçkıran Avcı B, Yürüyen M, Yavuzer H, Dikici SA et al (2015) Circulating miR-21 and eNOS in subclinical atherosclerosis in patients with hypertension. Clin Exp Hypertens 37:643–649PubMedGoogle Scholar
  80. 80.
    Chun HJ, Bonnet S, Chan SY (2017) Translational advances in the field of pulmonary hypertension. Translating MicroRNA biology in pulmonary hypertension. It will take more than “miR” words. Am J Respir Crit Care Med 195:167–178PubMedPubMedCentralGoogle Scholar
  81. 81.
    Courboulin A, Ranchoux B, Cohen-Kaminsky S, Perros F, Bonnet S (2016) MicroRNA networks in pulmonary arterial hypertension: share mechanisms with cancer?Curr. Opin Oncol 28:72–82Google Scholar
  82. 82.
    Boucherat O, Vitry G, Trinh I, Paulin R, Provencher S, Bonnet S (2017) The cancer theory of pulmonary arterial hypertension. Pulm Circ 7:285–299PubMedPubMedCentralGoogle Scholar
  83. 83.
    Meloche J, Pflieger A, Vaillancourt M, Graydon C, Provencher S, Bonnet S (2014) miRNAs in PAH: biomarker, therapeutic target or both? Drug Discov Today 19:1264–1269PubMedGoogle Scholar
  84. 84.
    McLendon JM, Joshi SR, Sparks J, Matar M, Fewell JG, Abe K et al (2015) Lipid nanoparticle delivery of a microRNA-145 inhibitor improves experimental pulmonary hypertension. J Control Release 210:67–75PubMedPubMedCentralGoogle Scholar
  85. 85.
    Lee HW, Park SH (2017) Elevated microRNA-135a is associated with pulmonary arterial hypertension in experimental mouse model. Oncotarget 8:35609–35618PubMedPubMedCentralGoogle Scholar
  86. 86.
    Sharma S, Umar S, Centala A, Eghbali M (2015) Role of miR206 in genistein-induced rescue of pulmonary hypertension in monocrotaline model. J Appl Physiol 119:1374–1382PubMedPubMedCentralGoogle Scholar
  87. 87.
    Diao L, Wang S, Sun Z (2018) Long noncoding RNA GAPLINC promotes gastric cancer cell proliferation by acting as a molecular sponge of miR-378 to modulate MAPK1 expression. Onco Targets Ther 11:2797–2804PubMedPubMedCentralGoogle Scholar
  88. 88.
    Weiser-Evans MCM (2017) Smooth muscle differentiation control comes full circle: the circular noncoding RNA, circActa2, functions as a miRNA sponge to fine-tune α-SMA expression. Circ Res 121:591–593PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.School of Life and Health ScienceAnhui Science and Technology UniversityFengyangChina
  2. 2.Fourth Affiliated HospitalAnhui Medical UniversityHefeiChina
  3. 3.State Key Laboratory of Tea Biochemistry and Biotechnology, School of Science and Technology of Tea and FoodAnhui Agricultural UniversityHefeiChina

Personalised recommendations