MicroRNA‑133b aggravates atherosclerosis by activating the Notch signaling pathway
- Authors:
- Baizhi Han
- Tao Li
- Shiliang Zheng
-
Affiliations: Department of General Medicine, Affiliated Hospital of Weifang Medical University, Weifang, Shandong 261031, P.R. China, Department of the Third Encephalopathy, Weifang Hospital of Traditional Chinese Medicine, Weifang, Shandong 261041, P.R. China - Published online on: June 11, 2020 https://doi.org/10.3892/mmr.2020.11222
- Pages: 1621-1630
This article is mentioned in:
Abstract
 |
 |
 |
 |
 |
 |
|
Liu J, Jiang C, Ma X and Wang J: Notoginsenoside Fc attenuates high glucose-induced vascular endothelial cell injury via upregulation of PPAR-γ in diabetic Sprague-Dawley rats. Vascul Pharmacol. 109:27–35. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Baumer Y, McCurdy S, Alcala M, Mehta N, Lee BH, Ginsberg MH and Boisvert WA: CD98 regulates vascular smooth muscle cell proliferation in atherosclerosis. Atherosclerosis. 256:105–114. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Hassan MO: The role of circulating endotoxaemia as a proinflammatory mediator of atherosclerosis in chronic kidney disease patients. BMJ. 288:283–284. 2016. | |
|
Groh L, Keating ST, Joosten LAB, Netea MG and Riksen NP: Monocyte and macrophage immunometabolism in atherosclerosis. Semin Immunopathol. 40:203–214. 2018. View Article : Google Scholar : PubMed/NCBI | |
|
Chistiakov DA, Melnichenko AA, Myasoedova VA, Grechko AV and Orekhov AN: Mechanisms of foam cell formation in atherosclerosis. J Mol Med (Berl). 95:1153–1165. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Lao KH, Zeng L and Xu Q: Endothelial and smooth muscle cell transformation in atherosclerosis. Curr Opin Lipidol. 26:449–456. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Francis GA, Allahverdian S, Cheroudi AC, Abraham T and McManus BM: Response to letter regarding article, “contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis”. Circulation. 131:e252015. View Article : Google Scholar : PubMed/NCBI | |
|
Huang Y, Ma XY, Yang YB, Ren HT, Sun XH and Wang LR: Identification and characterization of microRNAs and their target genes from Nile tilapia (Oreochromis niloticus). Z Natforsch C J Biosci. 71:215–223. 2016. | |
|
Xu X, Wang X, Fu B, Meng L and Lang B: Differentially expressed genes and microRNAs in bladder carcinoma cell line 5637 and T24 detected by RNA sequencing. Int J Clin Exp Pathol. 8:12678–12687. 2015.PubMed/NCBI | |
|
Gao ZG, Chen QJ, Shao M, Qian YZ, Zhang LF, Zhang YB and Xiong QX: Preliminary identification of key miRNAs, signaling pathways, and genes associated with Hirschsprung's disease by analysis of tissue microRNA expression profiles. World J Pediatr. 13:489–495. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Brennan E, Wang B, McClelland A, Mohan M, Marai M, Beuscart O, Derouiche S, Gray S, Pickering R, Tikellis C, et al: Protective effect of let-7 miRNA family in regulating inflammation in diabetes-associated atherosclerosis. Diabetes. 66:2266–2277. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Qun L, Wenda X, Weihong S, Jianyang M, Wei C, Fangzhou L, Zhenyao X and Pingjin G: miRNA-27b modulates endothelial cell angiogenesis by directly targeting Naa15 in atherogenesis. Atherosclerosis. 254:184–192. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
de Ronde MWJ, Kok MGM, Moerland PD, Van den Bossche J, Neele AE, Halliani A, van der Made I, de Winther MPJ, Meijers JCM, Creemers EE, et al: High miR-124-3p expression identifies smoking individuals susceptible to atherosclerosis. Atherosclerosis. 263:377–384. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Kim J, Inoue K, Ishii J, Vanti WB, Voronov SV, Murchison E, Hannon G and Abeliovich A: A MicroRNA feedback circuit in midbrain dopamine neurons. Science. 317:1220–1224. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Sanchez-Simon FM, Zhang XX, Loh HH, Law P-Y and Rodriguez RE: Morphine regulates dopaminergic neuron differentiation via miR-133b. Mol Pharmacol. 78:935–942. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Yin H, Pasut A, Soleimani VD, Bentzinger CF, Antoun G, Thorn S, Seale P, Fernando P, van Ijcken W, Grosveld F, et al: MicroRNA-133 controls brown adipose determination in skeletal muscle satellite cells by targeting Prdm16. Cell Metab. 17:210–224. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Li X, Wan X, Chen H, Yang S, Liu Y, Mo W, Meng D, Du W, Huang Y, Wu H, et al: Identification of miR-133b and RB1CC1 as independent predictors for biochemical recurrence and potential therapeutic targets for prostate cancer. Clin Cancer Res. 20:2312–2325. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Li D, Xia L, Chen M, Lin C, Wu H, Zhang Y, Pan S and Li X: miR-133b, a particular member of myomiRs, coming into playing its unique pathological role in human cancer. Oncotarget. 8:50193–50208. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
de Mena L, Coto E, Cardo LF, Díaz M, Blázquez M, Ribacoba R, Salvador C, Pastor P, Samaranch L, Moris G, et al: Analysis of the Micro-RNA-133 and PITX3 genes in Parkinson's disease. Am J Med Genet B Neuropsychiatr Genet. 153B:1234–1239. 2010.PubMed/NCBI | |
|
Ferreira LRP, Frade AF, Santos RHB, Teixeira PC, Baron MA, Navarro IC, Benvenuti LA, Fiorelli AI, Bocchi EA, Stolf NA, et al: MicroRNAs miR-1, miR-133a, miR-133b, miR-208a and miR-208b are dysregulated in Chronic Chagas disease Cardiomyopathy. Int J Cardiol. 175:409–417. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Masè M, Grasso M, Avogaro L, Nicolussi Giacomaz M, D'Amato E, Tessarolo F, Graffigna A, Denti MA and Ravelli F: Upregulation of miR-133b and miR-328 in patients with atrial dilatation: Implications for stretch-induced atrial fibrillation. Front Physiol. 10:11332019. View Article : Google Scholar : PubMed/NCBI | |
|
Huang B, Jiang X-C, Zhang T-Y, Hu YL, Tabata Y, Chen Z, Pluchino S and Gao JQ: Peptide modified mesenchymal stem cells as targeting delivery system transfected with miR-133b for the treatment of cerebral ischemia. Int J Pharm. 531:90–100. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Zheng CG, Chen BY, Sun RH, Mou XZ, Han F, Li Q, Huang HJ, Liu JQ and Tu YX: miR-133b Downregulation Reduces Vulnerable Plaque Formation in Mice with AS through Inhibiting Macrophage Immune Responses. Mol Ther Nucleic Acids. 16:745–757. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Zhen Y, Liu J, Huang Y, Wang Y, Li W and Wu J: miR-133b inhibits cell growth, migration, and invasion by targeting MMP9 in non-small cell lung cancer. Oncol Res. 25:1109–1116. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Guo L, Bai H, Zou D, Hong T, Liu J, Huang J, He P, Zhou Q and He J: The role of microRNA-133b and its target gene FSCN1 in gastric cancer. J Exp Clin Cancer Res. 33:992014. View Article : Google Scholar : PubMed/NCBI | |
|
Cheng Y, Jia B, Wang Y and Wan S: miR-133b acts as a tumor suppressor and negatively regulates ATP citrate lyase via PPARγ in gastric cancer. Oncol Rep. 38:3220–3226. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Wang X, Bu J, Liu X, Wang W, Mai W, Lv B, Zou J, Mo X, Li X, Wang J, et al: miR-133b suppresses metastasis by targeting HOXA9 in human colorectal cancer. Oncotarget. 8:63935–63948. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou Y, Wu D, Tao J, Qu P, Zhou Z and Hou J: MicroRNA-133 inhibits cell proliferation, migration and invasion by targeting epidermal growth factor receptor and its downstream effector proteins in bladder cancer. Scand J Urol. 47:423–432. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Li Y, Xiao L, Li J, Sun P, Shang L, Zhang J, Zhao Q, Ouyang Y, Li L and Gong K: MicroRNA profiling of diabetic atherosclerosis in a rat model. Eur J Med Res. 23:552018. View Article : Google Scholar : PubMed/NCBI | |
|
Fung E, Tang SM, Canner JP, Morishige K, Arboleda-Velasquez JF, Cardoso AA, Carlesso N, Aster JC and Aikawa M: Delta-like 4 induces notch signaling in macrophages: Implications for inflammation. Circulation. 115:2948–2956. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Quillard T, Devallière J, Coupel S and Charreau B: Inflammation dysregulates Notch signaling in endothelial cells: Implication of Notch2 and Notch4 to endothelial dysfunction. Biochem Pharmacol. 80:2032–2041. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Liu ZJ, Tan Y, Beecham GW, Seo DM, Tian R, Li Y, Vazquez-Padron RI, Pericak-Vance M, Vance JM, Goldschmidt-Clermont PJ, et al: Notch activation induces endothelial cell senescence and pro-inflammatory response: Implication of Notch signaling in atherosclerosis. Atherosclerosis. 225:296–303. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Liu Z, Tan Y, Tian R, Li Y, Beecham GW, Seo DM, Vazquez-Padron RI, Pericak-Vance MA, Vance JM, Goldschmidt-Clermont PJ, et al: Notch Signaling Is A Potential Novel Target In Atherosclerosis. J Surg Res. 165:3262011. View Article : Google Scholar | |
|
Davis-Knowlton J, Turner JE, Turner A, Damian-Loring S, Hagler N, Henderson T, Emery IF, Bond K, Duarte CW, Vary CPH, et al: Characterization of smooth muscle cells from human atherosclerotic lesions and their responses to Notch signaling. Lab Invest. 99:290–304. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Z, Wang Z, Wang T, Yuan J, Wang X and Zhang Z: Inhibition of miR-34a-5p protected myocardial ischemia reperfusion injury-induced apoptosis and reactive oxygen species accumulation through regulation of Notch Receptor 1 signaling. Rev Cardiovasc Med. 20:187–197. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Lin D, Cui B, Ma J and Ren J: MiR-183-5p protects rat hearts against myocardial ischemia/reperfusion injury through targeting VDAC1. Biofactors. 46:83–93. 2019. View Article : Google Scholar : PubMed/NCBI | |
|
Ou M, Zhang C, Chen J, Zhao S, Cui S and Tu J: Overexpression of microRNA-340-5p inhibits pulmonary arterial hypertension induced by acute pulmonary embolism by down-regulating the expression of inflammatory factors interleukin-1β and interleukin-6. Available at SSRN 3365060. 2019. View Article : Google Scholar | |
|
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Kasiewicz LN and Whitehead KA: Silencing TNFα with lipidoid nanoparticles downregulates both TNFα and MCP-1 in an in vitro co-culture model of diabetic foot ulcers. Acta Biomater. 32:120–128. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Talora C, Campese AF, Bellavia D, Felli MP, Vacca A, Gulino A and Screpanti I: Notch signaling and diseases: An evolutionary journey from a simple beginning to complex outcomes. Biochim Biophys Acta. 1782:489–497. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Geng YR, Zhang HL, Dong Y, Liu GY, Xie J and Wang H: Relationship between intercellular adhesion molecule-1 and cerebral infarction. Progress in Modern Biomedicine. 22:4373–4375. 2010.(In Chinese). | |
|
Xu R, Yin X, Xu W, Jin L, Lu M and Wang Y: Assessment of carotid plaque neovascularization by contrast-enhanced ultrasound and high sensitivity C-reactive protein test in patients with acute cerebral infarction: A comparative study. Neurol Sci. 37:1107–1112. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Wang Y, Liu T, Huang P, Zhao H, Zhang R, Ma B, Chen K, Huang F, Zhou X, Cui C, et al: A novel Golgi protein (GOLPH2)-regulated oncolytic adenovirus exhibits potent antitumor efficacy in hepatocellular carcinoma. Oncotarget. 6:13564–13578. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Yang L, Hou J, Cui XH, Suo LN and Lv YW: MiR-133b regulates the expression of CTGF in epithelial-mesenchymal transition of ovarian cancer. Eur Rev Med Pharmacol Sci. 21:5602–5609. 2017.PubMed/NCBI | |
|
Trajkovski M, Ahmed K, Esau CC and Stoffel M: MyomiR-133 regulates brown fat differentiation through Prdm16. Nat Cell Biol. 14:1330–1335. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Dumitriu IE and Kaski JC: The role of lymphocytes in the pathogenesis of atherosclerosis: Focus on CD4+ T cell subsets. Inflammatory Response in Cardiovascular Surgery. Gabriel EA and Gabriel SA: Springer; London: pp. 9–14. 2013, View Article : Google Scholar | |
|
Qin M, Luo Y, Meng XB, Wang M, Wang HW, Song SY, Ye JX, Pan RL, Yao F, Wu P, et al: Myricitrin attenuates endothelial cell apoptosis to prevent atherosclerosis: An insight into PI3K/Akt activation and STAT3 signaling pathways. Vascul Pharmacol. 70:23–34. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Chhour P, Naha PC, O'Neill SM, Litt HI, Reilly MP, Ferrari VA and Cormode DP: Labeling monocytes with gold nanoparticles to track their recruitment in atherosclerosis with computed tomography. Biomaterials. 87:93–103. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Fuhrman B, Koren L, Volkova N, Keidar S, Hayek T and Aviram M: Atorvastatin therapy in hypercholesterolemic patients suppresses cellular uptake of oxidized-LDL by differentiating monocytes. Atherosclerosis. 164:179–185. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
He B, Zhou L, Shen LH, Ha LH, Pu J, Shao Q, Wang L and Zeng JZ: RXR agonists inhibit PMA-induced differentiation of monocytic THP-1 cells into macrophages. Circulation. 118:S2772008. | |
|
Wang YS, Hsi E, Cheng HY, Hsu SH, Liao YC and Juo SH: Let-7g suppresses both canonical and non-canonical NF-κB pathways in macrophages leading to anti-atherosclerosis. Oncotarget. 8:101026–101041. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Ping S, Li Y, Liu S, Zhang Z, Wang J, Zhou Y, Liu K, Huang J, Chen D, Wang J, et al: Simultaneous increases in proliferation and apoptosis of vascular smooth muscle cells accelerate diabetic mouse venous atherosclerosis. PLoS One. 10:e01413752015. View Article : Google Scholar : PubMed/NCBI | |
|
Lee GL, Wu JY, Tsai CS, Lin CY, Tsai YT, Lin CS, Wang YF, Yet SF, Hsu YJ and Kuo CC: TLR4-activated MAPK-IL-6 axis regulates vascular smooth muscle cell function. Int J Mol Sci. 17:172016. View Article : Google Scholar | |
|
Liang Y, Gao H, Wang J, Wang Q, Zhao S, Zhang J and Qiu J: Alleviative effect of grape seed proanthocyanidin extract on small artery vascular remodeling in spontaneous hypertensive rats via inhibition of collagen hyperplasia. Mol Med Rep. 15:2643–2652. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Yang L, Yaling H, Chenghui Y and Xiaoxiang T: ASSA14-03-19 The change of cellular repressor of E1A-stimulated genes during vascular remodelling in a mouse model of arterial injury. Heart. 101 (Suppl 1):A14–A15. 2015. View Article : Google Scholar | |
|
Heijnen BF, Pelkmans LP, Danser AH, Garrelds IM, Mullins JJ, De Mey JG, Struijker-Boudier HA and Janssen BJ: Cardiac remodeling during and after renin-angiotensin system stimulation in Cyp1a1-Ren2 transgenic rats. J Renin Angiotensin Aldosterone Syst. 15:69–81. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Bodle JD, Feldmann E, Swartz RH, Rumboldt Z, Brown T and Turan TN: High-resolution magnetic resonance imaging: An emerging tool for evaluating intracranial arterial disease. Stroke. 44:287–292. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Lim TT, Liang DH, Botas J, Schroeder JS, Oesterle SN and Yeung AC: Role of compensatory enlargement and shrinkage in transplant coronary artery disease. Serial intravascular ultrasound study. Circulation. 95:855–859. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Hecht HS, Achenbach S, Kondo T and Narula J: High-Risk Plaque Features on Coronary CT Angiography. JACC Cardiovasc Imaging. 8:1336–1339. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Madrigal-Matute J, López-Franco O, Blanco-Colio LM, Muñoz-García B, Ramos-Mozo P, Ortega L, Egido J and Martín-Ventura JL: Heat shock protein 90 inhibitors attenuate inflammatory responses in atherosclerosis. Cardiovasc Res. 86:330–337. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Yang M, Deng C, Wu D, Zhong Z, Lv X, Huang Z, Lian N, Liu K and Zhang Q: The role of mononuclear cell tissue factor and inflammatory cytokines in patients with chronic thromboembolic pulmonary hypertension. J Thromb Thrombolysis. 42:38–45. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Torisu H, Ono M, Kiryu H, Furue M, Ohmoto Y, Nakayama J, Nishioka Y, Sone S and Kuwano M: Macrophage infiltration correlates with tumor stage and angiogenesis in human malignant melanoma: Possible involvement of TNFalpha and IL-1α. Int J Cancer. 85:182–188. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Tay C, Liu YH, Hosseini H, Kanellakis P, Cao A, Peter K, Tipping P, Bobik A, Toh BH and Kyaw T: B cell-specific depletion of TNFα inhibits atherosclerosis development and plaque vulnerability to rupture by reducing cell death and inflammation. Cardiovasc Res. 111:385–397. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Voloshyna I, Seshadri S, Anwar K, Littlefield MJ, Belilos E, Carsons SE and Reiss AB: Infliximab reverses suppression of cholesterol efflux proteins by TNF-α: A possible mechanism for modulation of atherogenesis. BioMed Res Int. 2014:3126472014. View Article : Google Scholar : PubMed/NCBI | |
|
Gandhirajan RK, Staib PA, Minke K, Gehrke I, Plickert G, Schlösser A, Schmitt EK, Hallek M and Kreuzer KA: Small molecule inhibitors of Wnt/β-catenin/lef-1 signaling induces apoptosis in chronic lymphocytic leukemia cells in vitro and in vivo. Neoplasia. 12:326–335. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Z, Ma N, Zheng Y and Zhang L: Association of serum immunoglobulin-G to Porphyromonas gingivalis with acute cerebral infarction in the Chinese population. J Indian Soc Periodontol. 19:628–632. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
He X, Li DR, Cui C and Wen LJ: Clinical significance of serum MCP-1 and VE-cadherin levels in patients with acute cerebral infarction. Eur Rev Med Pharmacol Sci. 21:804–808. 2017.PubMed/NCBI | |
|
Baeten JT and Lilly B: Differential Regulation of NOTCH2 and NOTCH3 Contribute to Their Unique Functions in Vascular Smooth Muscle Cells. J Biol Chem. 290:16226–16237. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Baeten JT and Lilly B: Notch Signaling in Vascular Smooth Muscle Cells. Adv Pharmacol. 78:351–382. 2017. View Article : Google Scholar : PubMed/NCBI | |
|
Sweeney C, Morrow D, Birney YA, Coyle S, Hennessy C, Scheller A, Cummins PM, Walls D, Redmond EM and Cahill PA: Notch 1 and 3 receptor signaling modulates vascular smooth muscle cell growth, apoptosis, and migration via a CBF-1/RBP-Jk dependent pathway. FASEB J. 18:1421–1423. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Zhao-Jun L, Yurong T, Beecham GW, et al: Notch activation induces endothelial cell senescence and pro-inflammatory response: Implication of Notch signaling in atherosclerosis. J Vasc Surg. 53:81S–82S. 2015. |
