MicroRNA 28-5p regulates ATP-binding cassette transporter A1 via inhibiting extracellular signal-regulated kinase 2

Liu,Jia; Liu,Xue‑Qing; Liu,Ying; Sun,Ya‑Nan; Li,Si; Li,Chun‑Mei; Li,Jie; Tian,Wei; Shang,Xiao‑Ming; Zhou,Yun‑Tao

doi:10.3892/mmr.2015.4563

MicroRNA 28-5p regulates ATP-binding cassette transporter A1 via inhibiting extracellular signal-regulated kinase 2

Authors:
- Jia Liu
- Xue‑Qing Liu
- Ying Liu
- Ya‑Nan Sun
- Si Li
- Chun‑Mei Li
- Jie Li
- Wei Tian
- Xiao‑Ming Shang
- Yun‑Tao Zhou
View Affiliations

Affiliations: Department of Internal Medicine, Hebei Medical University, Shijiazhuang, Hebei 050017, P.R. China, Department of Hepatobiliary Surgery, The Second Hospital of Hebei Medical University, Shijiazhuang, Hebei 050000, P.R. China, Department of Clinical Laboratory Center, Tangshan Gongren Hospital, Tangshan, Hebei 063000, P.R. China, Department of Cardiology, Tangshan Gongren Hospital, Tangshan, Hebei 063000, P.R. China
Published online on: November 12, 2015 https://doi.org/10.3892/mmr.2015.4563
Pages: 433-440

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

The biological function of the intronic microRNA-28 (miR-28) may be associated with the biological roles of its host gene, LIM domain lipoma‑preferred partner (LPP). LPP has been reported to promote smooth muscle cell migration in arterial injury and atherosclerosis. However, the mechanism of miR‑28 in atherosclerosis remains unclear. In the current study, the aim was to validate the inhibitory effect of miR‑28‑5p on extracellular signal‑regulated kinase 2 (ERK2), to investigate its biological role in atherosclerosis and its association with cardiovascular disease. Western blotting and stem‑loop reverse transcription‑quantitative polymerase chain reaction combined with TaqMAN microRNA analysis was conducted. The current study demonstrated that miR‑28‑5p upregulated the expression of ATP‑binding cassette transporter A1 (ABCA1) via the inhibition of ERK2 in HepG2 cells. In addition, increased levels of plasma miR‑28‑5p were positively correlated with the levels of high‑density lipoprotein cholesterol in patients with unstable angina. This suggests that miR-28-5p participates in atherosclerosis via ERK2-mediated upregulation of the ABCA1 pathway.

View Figures

View References

1	Bartel DP: MicroRNAs: Genomics, biogenesis, mechanism, and function. Cell. 116:281–297. 2004. View Article : Google Scholar : PubMed/NCBI
2	Calin GA and Croce CM: MicroRNA signatures in human cancers. Nat Rev Cancer. 6:857–866. 2006. View Article : Google Scholar : PubMed/NCBI
3	Ambros V, Lee RC, Lavanway A, Williams PT and Jewell D: MicroRNAs and other tiny endogenous RNAs in C. elegans. Curr Biol. 13:807–818. 2003. View Article : Google Scholar : PubMed/NCBI
4	Lin SL, Miller JD and Ying SY: Intronic microRNA (miRNA). J Biomed Biotechnol. 2006:268182006. View Article : Google Scholar : PubMed/NCBI
5	Hooper CL, Dash PR and Boateng SY: Lipoma preferred partner is a mechanosensitive protein regulated by nitric oxide in the heart. FEBS Open Bio. 2:135–144. 2012. View Article : Google Scholar : PubMed/NCBI
6	Jin L, Hastings NE, Blackman BR and Somlyo AV: Mechanical properties of the extracellular matrix alter expression of smooth muscle protein LPP and its partner palladin; relationship to early atherosclerosis and vascular injury. J Muscle Res Cell Motil. 30:41–55. 2009. View Article : Google Scholar : PubMed/NCBI
7	Gorenne I, Jin L, Yoshida T, Sanders JM, Sarembock IJ, Owens GK, Somlyo AP and Somlyo AV: LPP expression during in vitro smooth muscle differentiation and stent induced vascular injury. Circ Res. 98:378–385. 2006. View Article : Google Scholar : PubMed/NCBI
8	Almeida MI, Nicoloso MS, Zeng L, Ivan C, Spizzo R, Gafà R, Xiao L, Zhang X, Vannini I, Fanini F, et al: Strand-specific miR-28-5p and miR-28-3p have distinct effects in colorectal cancer cells. Gastroenterology. 142:886–896.e9. 2012. View Article : Google Scholar : PubMed/NCBI
9	Yang M, Yao Y, Eades G, Zhang Y and Zhou Q: MiR-28 regulates Nrf2 expression through a Keap1 independent mechanism. Breast Cancer Res Treat. 129:983–991. 2011. View Article : Google Scholar : PubMed/NCBI
10	Liu J, Liu Y, Sun YN, Li S, Liu XQ, Li J, Li CM, Tian W, Zhou YT and Shang XM: miR-28-5p involved in LXR-ABCA1 pathway is increased in the plasma of unstable angina patients. Heat Lung Circ. 24:724–730. 2015. View Article : Google Scholar
11	Sebolt-Leopold JS and Herrera R: Targeting the mitogen activated protein kinase cascade to treat cancer. Nat Rev Cancer. 4:937–947. 2004. View Article : Google Scholar : PubMed/NCBI
12	Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K and Cobb MH: Mitogen-activated protein (MAP) kinase pathways: Regulation and physiological functions. Endocr Rev. 22:153–183. 2001.PubMed/NCBI
13	Wang Y: Mitogen-activated protein kinases in heart development and diseases. Circulation. 116:1413–1423. 2007. View Article : Google Scholar : PubMed/NCBI
14	Zhou X, Yin Z, Guo X, Hajjar DP and Han J: Inhibition of ERK1/2 and activation of liver X receptor synergistically induce macrophage ABCA1 expression and cholesterol efflux. J Biol Chem. 285:6316–6326. 2010. View Article : Google Scholar :
15	Tall AR: Cholesterol efflux pathways and other potential mechanisms involved in the athero protective effect of high density lipoproteins. J Intern Med. 263:256–273. 2008. View Article : Google Scholar : PubMed/NCBI
16	Tall AR, Yvan Charvet L, Terasaka N, Pagler T and Wang N: HDL, ABC transporters, and cholesterol efflux: Implications for the treatment of atherosclerosis. Cell Metab. 7:365–375. 2008. View Article : Google Scholar : PubMed/NCBI
17	Bodzioch M, Orsó E, Klucken J, Langmann T, Böttcher A, Diederich W, Drobnik W, Barlage S, Büchler C, Porsch-Ozcürümez M, et al: The gene encoding ATP binding cassette transporter 1 is mutated in Tangier disease. Nat Genet. 22:347–351. 1999. View Article : Google Scholar : PubMed/NCBI
18	Brooks Wilson A, Marcil M, Clee SM, Zhang LH, Roomp K, van Dam M, Yu L, Brewer C, Collins JA, Molhuizen HO, et al: Mutations in ABC1 in Tangier disease and familial high density lipoprotein deficiency. Nat Genet. 22:336–345. 1999. View Article : Google Scholar
19	Rust S, Rosier M, Funke H, Real J, Amoura Z, Piette JC, Deleuze JF, Brewer HB, Duverger N, Denèfle P and Assmann G: Tangier disease is caused by mutations in the gene encoding ATP binding cassette transporter 1. Nat Genet. 22:352–355. 1999. View Article : Google Scholar : PubMed/NCBI
20	Dweep H, Sticht C, Pandey P and Gretz N: miRWalk database: Prediction of possible miRNA binding sites by “walking” the genes of three genomes. J Biomed Inform. 44:839–847. 2011. View Article : Google Scholar : PubMed/NCBI
21	Girardot M, Pecquet C, Boukour S, Knoops L, Ferrant A, Vainchenker W, Giraudier S and Constantinescu SN: miR 28 is a thrombopoietin receptor targeting microRNA detected in a fraction of myeloproliferative neoplasm patient platelets. Blood. 116:437–445. 2010. View Article : Google Scholar : PubMed/NCBI
22	Anderson JL, Adams CD, Antman EM, Bridges CR, Califf RM, Casey DE Jr, Chavey WE II, Fesmire FM, Hochman JS, Levin TN, et al American College of Cardiology; American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 2002 Guidelines for the Management of Patients With Unstable Angina/Non-ST-Elevation Myocardial Infarction); American College of Emergency Physicians; Society for Cardiovascular Angiography and Interventions; Society of Thoracic Surgeons; American Association of Cardiovascular and Pulmonary Rehabilitation; Society for Academic Emergency Medicine: ACC/AHA 2007 guidelines for the management of patients with unstable angina/non-ST-Elevation myocardial infarction: A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Writing Committee to Revise the 2002 Guidelines for the Management of Patients With Unstable Angina/Non ST Elevation Myocardial Infarction) developed in collaboration with the American College of Emergency Physicians, the Society for Cardiovascular Angiography and Interventions, and the Society of Thoracic Surgeons endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation and the Society for Academic Emergency Medicine. J Am Coll Cardiol. 50:e1–e157. 2007. View Article : Google Scholar
23	Mestdagh P, Van Vlierberghe P, De Weer A, Muth D, Westermann F, Speleman F and Vandesompele J: A novel and universal method for microRNA RT qPCR data normalization. Genome Biol. 10:R642009. View Article : Google Scholar
24	Schwindt H, Akasaka T, Zühlke Jenisch R, Hans V, Schaller C, Klapper W, Dyer MJS, Siebert R and Deckert M: Chromosomal translocations fusing the BCL6 gene to different partner loci are recurrent in primary central nervous system lymphoma and may be associated with aberrant somatic hypermutation or defective class switch recombination. J Neuropathol Exp Neurol. 65:776–782. 2006. View Article : Google Scholar : PubMed/NCBI
25	Rayner KJ, Sheedy FJ, Esau CC, Hussain FN, Temel RE, Parathath S, van Gils JM, Rayner AJ, Chang AN, Suarez Y, et al: Antagonism of miR-33 in mice promotes reverse cholesterol transport and regression of atherosclerosis. J Clin Invest. 121:2921–2931. 2011. View Article : Google Scholar : PubMed/NCBI
26	Ramirez CM, Dávalos A, Goedeke L, Salerno AG, Warrier N, Cirera Salinas D, Suárez Y and Fernández Hernando C: MicroRNA-758 regulates cholesterol efflux through posttranscrip tional repression of ATP binding cassette transporter A1. Arterioscler Thromb Vasc Biol. 31:2707–2714. 2011. View Article : Google Scholar : PubMed/NCBI
27	Ramírez CM, Rotllan N, Vlassov AV, Dávalos A, Li M, Goedeke L, Aranda JF, Cirera Salinas D, Araldi E, Salerno A, et al: Control of cholesterol metabolism and plasma high–density lipoprotein levels by microRNA 144. Circ Res. 112:1592–1601. 2013. View Article : Google Scholar
28	Fernández Hernando C, Ramírez CM, Goedeke L and Suárez Y: MicroRNAs in metabolic disease. Arterioscler Thromb Vasc Biol. 33:178–185. 2013. View Article : Google Scholar : PubMed/NCBI
29	Park SY, Lee JH, Ha M, Nam JW and Kim VN: miR 29 miRNAs activate p53 by targeting p85 α and CDC42. Nat Struct Mol Biol. 16:23–29. 2009. View Article : Google Scholar
30	Liu P and Wilson MJ: miR-520c and miR-373 upregulate MMP9 expression by targeting mTOR and SIRT1, and activate the Ras/Raf/MEK/Erk signaling pathway and NF-κB factor in human fibrosarcoma cells. J Cell Physiol. 227:867–876. 2012. View Article : Google Scholar
31	Cai J, Guan H, Fang L, Yang Y, Zhu X, Yuan J, Wu J and Li M: MicroRNA-374a activates Wnt/β-catenin signaling to promote breast cancer metastasis. J Clin Invest. 123:566–579. 2013.PubMed/NCBI
32	Xiang P, Deng HY, Li K, Huang GY, Chen Y, Tu L, Ng PC, Pong NH, Zhao H, Zhang L and Sung RY: Dexrazoxane protects against doxorubicin-induced cardiomyopathy: Upregulation of Akt and Erk phosphorylation in a rat model. Cancer Chemother Pharmacol. 63:343–349. 2009. View Article : Google Scholar
33	Dangwal S, Bang C and Thum T: Novel techniques and targets in cardiovascular microRNA research. Cardiovasc Res. 93:545–554. 2012. View Article : Google Scholar
34	Joyce CW, Amar MJ, Lambert G, Vaisman BL, Paigen B, Najib Fruchart J, Hoyt RF Jr, Neufeld ED, Remaley AT, Fredrickson DS, et al: The ATP binding cassette transporter A1 (ABCA1) modulates the development of aortic atherosclerosis in C57BL/6 and apoE knockout mice. Proc Natl Acad Sci USA. 99:407–412. 2002. View Article : Google Scholar
35	Cavelier LB, Qiu Y, Bielicki JK, Afzal V, Cheng JF and Rubin EM: Regulation and activity of the human ABCA1 gene in transgenic mice. J Biol Chem. 276:18046–18051. 2001. View Article : Google Scholar : PubMed/NCBI