10,425
Views
71
CrossRef citations to date
0
Altmetric
Research Paper

The P2RY12 receptor promotes VSMC-derived foam cell formation by inhibiting autophagy in advanced atherosclerosis

, , , , , , , , , , , , , , , , , , ORCID Icon & show all
Pages 980-1000 | Received 05 May 2019, Accepted 06 Mar 2020, Published online: 19 Mar 2020

References

  • Herrington W, Lacey B, Sherliker P, et al. Epidemiology of atherosclerosis and the potential to reduce the global burden of atherothrombotic disease. Circ Res. 2016 Feb 19;118(4):535–546.
  • Ward NC, Watts GF, Eckel RH. Statin Toxicity. Circ Res. 2019;124(2):328–350.
  • Solanki A, Bhatt LK, Johnston TP. Evolving targets for the treatment of atherosclerosis. Pharmacol Ther. 2018;187:1–12.
  • Hechler B, Gachet C. Purinergic receptors in thrombosis and inflammation. Arterioscler Thromb Vasc Biol. 2015;35(11):2307–2315.
  • Amarenco P, Albers GW, Denison H, et al. Efficacy and safety of ticagrelor versus aspirin in acute stroke or transient ischaemic attack of atherosclerotic origin: a subgroup analysis of SOCRATES, a randomised, double-blind, controlled trial. Lancet Neurol. 2017;16(4):301–310.
  • CAPRIE Steering Committee. A randomised, blinded, trial of clopidogrel versus aspirin in patients at risk of ischaemic events (CAPRIE). Lancet. 1996;348(9038):1329–1339.
  • Ringleb PA, Bhatt DL, Hirsch AT, et al. Benefit of clopidogrel over aspirin is amplified in patients with a history of ischemic events. Stroke. 2004;35(2):528–532.
  • Bhatt DL, Flather MD, Hacke W, et al. Patients with prior myocardial infarction, stroke, or symptomatic peripheral arterial disease in the CHARISMA trial. J Am Coll Cardiol. 2007 May 15;49(19):1982–1988.
  • West LE, Steiner T, Judge HM, et al. Vessel wall, not platelet, P2Y12 potentiates early atherogenesis. Cardiovasc Res. 2014;102(3):429–435.
  • Lee CW, Hwang I, Park C-S, et al. Comparison of differential expression of P2Y12 receptor in culprit coronary plaques in patients with acute myocardial infarction versus stable angina pectoris. Am J Cardiol. 2011;108(6):799–803.
  • Rauch BH, Rosenkranz AC, Ermler S, et al. Regulation of functionally active P2Y12 ADP receptors by thrombin in human smooth muscle cells and the presence of P2Y12 in carotid artery lesions. Arterioscler Thromb Vasc Biol. 2010 Dec;30(12):2434–2442.
  • Niu X, Pi SL, Baral S, et al. P2Y12 promotes migration of vascular smooth muscle cells through cofilin dephosphorylation during atherogenesis. Arterioscler Thromb Vasc Biol. 2017 Mar;37(3):515–524.
  • Shanker G, Kontos JL, Eckman DM, et al. Nicotine upregulates the expression of P2Y12 on vascular cells and megakaryoblasts. J Thromb Thrombolysis. 2006;22(3):213–220.
  • Bartels ED, Christoffersen C, Lindholm MW, et al. Altered metabolism of LDL in the arterial wall precedes atherosclerosis regression. Circ Res. 2015 Nov 6;117(11):933–942.
  • Allahverdian S, Chehroudi AC, McManus BM, et al. Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis. Circulation. 2014 Apr 15;129(15):1551–1559.
  • Klionsky DJ. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol. 2007 Nov;8(11):931–937.
  • Ouimet M, Franklin V, Mak E, et al. Autophagy regulates cholesterol efflux from macrophage foam cells via lysosomal acid lipase. Cell Metab. 2011 Jun 8;13(6):655–667.
  • Martinet W, De Meyer GRY. Autophagy in Atherosclerosis. Circ Res. 2009;104(3):304–317.
  • Shchors K, Massaras A, Hanahan D. Dual targeting of the autophagic regulatory circuitry in gliomas with repurposed drugs elicits cell-lethal autophagy and therapeutic benefit. Cancer Cell. 2015;28(4):456–471.
  • Amato M, Veglia F, de Faire U, et al. Carotid plaque-thickness and common carotid IMT show additive value in cardiovascular risk prediction and reclassification. Atherosclerosis. 2017 Aug;263:412–419.
  • Rubin MR, Rundek T, McMahon DJ, et al. Carotid artery plaque thickness is associated with increased serum calcium levels: the Northern Manhattan study. Atherosclerosis. 2007 Oct;194(2):426–432.
  • Shankman LS, Gomez D, Cherepanova OA, et al. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat Med. 2015 Jun;21(6):628–637.
  • She ZG, Chang Y, Pang HB, et al. NG2 proteoglycan ablation reduces foam cell formation and atherogenesis via decreased low-density lipoprotein retention by synthetic smooth muscle cells. Arterioscler Thromb Vasc Biol. 2016 Jan;36(1):49–59.
  • Gachet C. P2Y(12) receptors in platelets and other hematopoietic and non-hematopoietic cells. Purinergic Signal. 2012 Sep;8(3):609–619.
  • Gao Y, Yu C, Pi S, et al. The role of P2Y12 receptor in ischemic stroke of atherosclerotic origin. Cell Mol Life Sci. 2018;76(2):341–354.
  • Li BH, Yin YW, Liu Y, et al. TRPV1 activation impedes foam cell formation by inducing autophagy in oxLDL-treated vascular smooth muscle cells. Cell Death Dis. 2014 Apr 17;5(4):e1182.
  • Singh R, Kaushik S, Wang Y, et al. Autophagy regulates lipid metabolism. Nature. 2009;458(7242):1131–1135.
  • Jia J, Abudu YP, Claude-Taupin A, et al. Galectins control MTOR and AMPK in response to lysosomal damage to induce autophagy. Autophagy. 2019 Jan;15(1):169–171.
  • Martinet W, Verheye S, De Meyer GRY. Everolimus-induced mTOR inhibition selectively depletes macrophages in atherosclerotic plaques by autophagy. Autophagy. 2014;3(3):241–244.
  • Schwarz JB, Langwieser N, Langwieser NN, et al. Novel role of the CXC chemokine receptor 3 in inflammatory response to arterial injury: involvement of mTORC1. Circ Res. 2009 Jan 30;104(2):189–200.
  • Wirka RC, Wagh D, Paik DT, et al. Atheroprotective roles of smooth muscle cell phenotypic modulation and the TCF21 disease gene as revealed by single-cell analysis. Nat Med. 2019 Aug;25(8):1280–1289.
  • Basatemur GL, Jorgensen HF, Clarke MCH, et al. Vascular smooth muscle cells in atherosclerosis. Nat Rev Cardiol. 2019 Dec;16(12):727–744.
  • Allahverdian S, Chaabane C, Boukais K, et al. Smooth muscle cell fate and plasticity in atherosclerosis. Cardiovasc Res. 2018 Mar 15;114(4):540–550.
  • Ouimet M, Marcel YL. Regulation of lipid droplet cholesterol efflux from macrophage foam cells. Arterioscler Thromb Vasc Biol. 2012;32(3):575–581.
  • Randolph GJ. Mechanisms that regulate macrophage burden in atherosclerosis. Circ Res. 2014 May 23;114(11):1757–1771.
  • De Meyer GRY, Grootaert MOJ, Michiels CF, et al. Autophagy in vascular disease. Circ Res. 2015;116(3):468–479.
  • Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13(2):132–141.
  • Rundek T, Arif H, Boden-Albala B, et al. Carotid plaque, a subclinical precursor of vascular events: the Northern Manhattan Study. Neurology. 2008 Apr 1;70(14):1200–1207.
  • Carrelli AL, Walker MD, Lowe H, et al. Vitamin D deficiency is associated with subclinical carotid atherosclerosis: the Northern Manhattan study. Stroke. 2011 Aug;42(8):2240–2245.
  • Chung KW, Kim KM, Choi YJ, et al. The critical role played by endotoxin-induced liver autophagy in the maintenance of lipid metabolism during sepsis. Autophagy. 2017 Jul 3;13(7):1113–1129.
  • Yu Y, Wang L, Delguste F, et al. Advanced glycation end products receptor RAGE controls myocardial dysfunction and oxidative stress in high-fat fed mice by sustaining mitochondrial dynamics and autophagy-lysosome pathway. Free Radic Biol Med. 2017 Nov;112:397–410.
  • Xu J, Cui X, Li J, et al. Chloroquine improves the response to ischemic muscle injury and increases HMGB1 after arterial ligation. J Vasc Surg. 2018;67(3):910–921.
  • Hamczyk MR, Villa‐Bellosta R, Quesada V, et al. Progerin accelerates atherosclerosis by inducing endoplasmic reticulum stress in vascular smooth muscle cells. EMBO Mol Med. 2019;11(4):4.
  • Suzanne M, Eken HJ, Ekaterina C, et al. MicroRNA-210 enhances fibrous cap stability in advanced atherosclerotic lesions. Circ Res. 2017;120(4):633–644.
  • Wu JH, Zhou YF, Hong CD, et al. Semaphorin-3A protects against neointimal hyperplasia after vascular injury. EBioMedicine. 2019 Jan;39:95–108.
  • Jeong S-J, Kim S, Park J-G, et al. Prdx1 (peroxiredoxin 1) deficiency reduces cholesterol efflux via impaired macrophage lipophagic flux. Autophagy. 2017;14(1):120–133.
  • Li Z, Martin M, Zhang J, et al. Kruppel-like factor 4 regulation of cholesterol-25-hydroxylase and liver X receptor mitigates atherosclerosis susceptibility. Circulation. 2017 Oct 3;136(14):1315–1330.
  • Le Guezennec X, Brichkina A, Huang YF, et al. Wip1-dependent regulation of autophagy, obesity, and atherosclerosis. Cell Metab. 2012 Jul 3;16(1):68–80.
  • Liu Y, Zhong Y, Chen H, et al. Retinol-binding protein-dependent cholesterol uptake regulates macrophage foam cell formation and promotes atherosclerosis. Circulation. 2017 Apr 4;135(14):1339–1354.
  • Rousselle A, Qadri F, Leukel L, et al. CXCL5 limits macrophage foam cell formation in atherosclerosis. J Clin Invest. 2013 Mar;123(3):1343–1347.
  • Yoshii SR, Mizushima N. Monitoring and measuring autophagy. Int J Mol Sci. 2017 Aug 28;18(9):9.
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2016;12(1):1–222. 3rd edition.
  • Tanida I, Ueno T, Kominami E. LC3 and autophagy. Methods Mol Biol. 2008;445:77–88.
  • Chu CT, Plowey ED, Dagda RK, et al. Autophagy in neurite injury and neurodegeneration: in vitro and in vivo models. Methods Enzymol. 2009;453:217–249.
  • Martinez-Lopez N, Garcia-Macia M, Sahu S, et al. Autophagy in the CNS and periphery coordinate lipophagy and lipolysis in the brown adipose tissue and liver. Cell Metab. 2016 Jan 12;23(1):113–127.
  • Kaushik S, Arias E, Kwon H, et al. Loss of autophagy in hypothalamic POMC neurons impairs lipolysis. EMBO Rep. 2012 Mar 1;13(3):258–265.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001 Dec;25(4):402–408.
  • Huang K-L, Li S, Mertins P, et al. Proteogenomic integration reveals therapeutic targets in breast cancer xenografts. Nat Commun. 2017;8(1):14864.
  • Moriya Y, Itoh M, Okuda S, et al. KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res. 2007;35(WebServer):W182–W185.

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.