MicroRNA-9 inhibits NLRP3 inflammasome activation in human atherosclerosis inflammation cell models through the JAK1/STAT signaling pathway

Cellular Physiology and Biochemistry

Volumn 41, Issue 4, 2017, Pages 1555-1571

  Wang, Yue ^a   Han, Zhihua ^a   Fan, Yuqi ^a   Zhang, Junfeng ^a   Chen, Kan ^a   Gao, Lin ^a   Zeng, Huasu ^a   Cao, Jiatian ^a,b   Wang, Changqian ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; CELL PROTEIN; COLLAGENASE 3; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1BETA; JANUS KINASE 1; LIPOPOLYSACCHARIDE; MICRORNA 9; OXIDIZED LOW DENSITY LIPOPROTEIN; SMALL INTERFERING RNA; STAT PROTEIN; STAT1 PROTEIN; JAK1 PROTEIN, HUMAN; LOW DENSITY LIPOPROTEIN; MICRORNA; MIRN92 MICRORNA, HUMAN; NLRP3 PROTEIN, HUMAN; STAT1 PROTEIN, HUMAN;

ARTICLE; ATHEROSCLEROSIS; CELL NUCLEUS; CYTOKINE RELEASE; CYTOPLASM; DOWN REGULATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE OVEREXPRESSION; GENE SILENCING; GENE TARGETING; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUCIFERASE ASSAY; MACROPHAGE; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; BIOLOGICAL MODEL; BIOSYNTHESIS; CHEMICALLY INDUCED; GENETICS; INFLAMMATION; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ATHEROSCLEROSIS; CELL LINE, TUMOR; HUMANS; INFLAMMASOMES; INFLAMMATION; JANUS KINASE 1; LIPOPROTEINS, LDL; MICRORNAS; MODELS, BIOLOGICAL; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR;

EID: 85016629290     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000470822     Document Type: Article

References (56)

1. Libby P, Ridker PM, Maseri A: Inflammation and atherosclerosis. Circulation 2002;105:1135-1143.
2. Ross R: The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature 1993;362:801-809.
3. Chen JW, Chen YH, Lin SJ: Long-term exposure to oxidized low-density lipoprotein enhances tumor necrosis factor-alpha-stimulated endothelial adhesiveness of monocytes by activating superoxide generation and redox-sensitive pathways. Free Radic Biol Med 2006;40:817-826.
4. Osterud B, Bjorklid E: Role of monocytes in atherogenesis. Physiol Rev 2003;83:1069-1112.
5. Shashkin P, Dragulev B, Ley K: Macrophage differentiation to foam cells. Curr Pharm Des 2005;11:3061-3072.
6. Tabas I: Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: The importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol 2005;25:2255-2264.
7. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nunez G, Schnurr M, Espevik T, Lien E, Fitzgerald KA, Rock KL, Moore KJ, Wright SD, Hornung V, Latz E: NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010;464:1357-1361.
8. Rajamaki K, Lappalainen J, Oorni K, Valimaki E, Matikainen S, Kovanen PT, Eklund KK: Cholesterol crystals activate the NLRP3 inflammasome in human macrophages: A novel link between cholesterol metabolism and inflammation. PLoS One 2010;5:e11765.
9. Wen H, Ting JP, O'Neill LA: A role for the NLRP3 inflammasome in metabolic diseases-did Warburg miss inflammation?. Nat Immunol 2012;13:352-357.
10. De Nardo D, Latz E: NLRP3 inflammasomes link inflammation and metabolic disease. Trends Immunol 2011;32:373-379.
11. Mariathasan S, Weiss DS, Newton K, McBride J, O'Rourke K, Roose-Girma M, Lee WP, Weinrauch Y, Monack DM, Dixit VM: Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006;440:228-232.
12. Halle A, Hornung V, Petzold GC, Stewart CR, Monks BG, Reinheckel T, Fitzgerald KA, Latz E, Moore KJ, Golenbock DT: The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 2008;9:857-865.
13. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J: Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 2006;440:237-241.
14. Liu W, Yin Y, Zhou Z, He M, Dai Y: OxLDL-induced IL-1 beta secretion promoting foam cells formation was mainly via CD36 mediated ROS production leading to NLRP3 inflammasome activation. Inflamm Res 2014;63:33-43.
15. Martinon F, Mayor A, Tschopp J: The inflammasomes: Guardians of the body. Annu Rev Immunol 2009;27:229-265.
16. Shao BZ, Xu ZQ, Han BZ, Su DF, Liu C: NLRP3 inflammasome and its inhibitors: A review. Front Pharmacol 2015;6:262.
17. Marchetti C, Chojnacki J, Toldo S, Mezzaroma E, Tranchida N, Rose SW, Federici M, Van Tassell BW, Zhang S, Abbate A: A novel pharmacologic inhibitor of the NLRP3 inflammasome limits myocardial injury after ischemia-reperfusion in the mouse. J Cardiovasc Pharmacol 2014;63:316-322.
18. O'Connell RM, Rao DS, Baltimore D: MicroRNA regulation of inflammatory responses. Annu Rev Immunol 2012;30:295-312.
19. Nazari-Jahantigh M, Egea V, Schober A, Weber C: MicroRNA-specific regulatory mechanisms in atherosclerosis. J Mol Cell Cardiol 2015;89:35-41.
20. Zhang T, Tian F, Wang J, Jing J, Zhou SS, Chen YD: Atherosclerosis-Associated Endothelial Cell Apoptosis by MiR-429-Mediated Down Regulation of Bcl-2. Cell Physiol Biochem 2015;37:1421-1430.
21. Yang Y, Yang L, Liang X, Zhu G: MicroRNA-155 Promotes Atherosclerosis Inflammation via Targeting SOCS1. Cell Physiol Biochem 2015;36:1371-1381.
22. Zhang T, Tian F, Wang J, Jing J, Zhou SS, Chen YD: Endothelial Cell Autophagy in Atherosclerosis is Regulated by miR-30-Mediated Translational Control of ATG6. Cell Physiol Biochem 2015;37:1369-1378.
23. Natarelli L, Schober A: MicroRNAs and the response to injury in atherosclerosis. Hamostaseologie 2015;35:142-150.
24. Chen T, Huang Z, Wang L, Wang Y, Wu F, Meng S, Wang C: MicroRNA-125a-5p partly regulates the inflammatory response, lipid uptake, and ORP9 expression in oxLDL-stimulated monocyte/macrophages. Cardiovasc Res 2009;83:131-139.
25. Wei Y, Nazari-Jahantigh M, Neth P, Weber C, Schober A: MicroRNA-126, -145, and -155: A therapeutic triad in atherosclerosis?. Arterioscler Thromb Vasc Biol 2013;33:449-454.
26. Wang JG, Williams JC, Davis BK, Jacobson K, Doerschuk CM, Ting JP, Mackman N: Monocytic microparticles activate endothelial cells in an IL-1beta-dependent manner. Blood 2011;118:2366-2374.
27. Ding Z, Liu S, Wang X, Dai Y, Khaidakov M, Deng X, Fan Y, Xiang D, Mehta JL: LOX-1, mtDNA damage, and NLRP3 inflammasome activation in macrophages: Implications in atherogenesis. Cardiovasc Res 2014;103:619-628.
28. Meyre D, Froguel P, Horber FF, Kral JG: Comment on: Valette et al. Melanocortin-4 receptor mutations and polymorphisms do not affect weight loss after bariatric surgery. PLOS ONE 2012; 7(11):E48221.
29. PLoS One 2014;9:e93324.
30. Sun B, Ji Z, Liao YP, Wang M, Wang X, Dong J, Chang CH, Li R, Zhang H, Nel AE, Xia T: Engineering an effective immune adjuvant by designed control of shape and crystallinity of aluminum oxyhydroxide nanoparticles. ACS Nano 2013;7:10834-10849.
31. Wang Y, Cao J, Fan Y, Xie Y, Xu Z, Yin Z, Gao L, Wang C: Artemisinin inhibits monocyte adhesion to HUVECs through the NF-kappaB and MAPK pathways in vitro. Int J Mol Med 2016;37:1567-1575.
32. Hecker A, Kullmar M, Wilker S, Richter K, Zakrzewicz A, Atanasova S, Mathes V, Timm T, Lerner S, Klein J, Kaufmann A, Bauer S, Padberg W, Kummer W, Janciauskiene S, Fronius M, Schweda EK, Lochnit G, Grau V: Phosphocholine-Modified Macromolecules and Canonical Nicotinic Agonists Inhibit ATP-Induced IL-1beta Release. J Immunol 2015;195:2325-2334.
33. Meng S, Cao J, Zhang X, Fan Y, Fang L, Wang C, Lv Z, Fu D, Li Y: Downregulation of microRNA-130a contributes to endothelial progenitor cell dysfunction in diabetic patients via its target Runx3. PLoS One 2013;8:e68611.
34. Krichevsky AM, King KS, Donahue CP, Khrapko K, Kosik KS: A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 2003;9:1274-1281.
35. Li H, Ambade A, Re F: Cutting edge: Necrosis activates the NLRP3 inflammasome. J Immunol 2009;183:1528-1532.
36. Deguchi JO, Aikawa E, Libby P, Vachon JR, Inada M, Krane SM, Whittaker P, Aikawa M: Matrix metalloproteinase-13/collagenase-3 deletion promotes collagen accumulation and organization in mouse atherosclerotic plaques. Circulation 2005;112:2708-2715.
37. Bazzoni F, Rossato M, Fabbri M, Gaudiosi D, Mirolo M, Mori L, Tamassia N, Mantovani A, Cassatella MA, Locati M: Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc Natl Acad Sci U S A 2009;106:5282-5287.
38. Nie K, Gomez M, Landgraf P, Garcia JF, Liu Y, Tan LH, Chadburn A, Tuschl T, Knowles DM, Tam W: MicroRNA-mediated down-regulation of PRDM1/Blimp-1 in Hodgkin/Reed-Sternberg cells: A potential pathogenetic lesion in Hodgkin lymphomas. Am J Pathol 2008;173:242-252.
39. Xu J, Hu G, Lu M, Xiong Y, Li Q, Chang CC, Song B, Chang T, Li B: MiR-9 reduces human acyl-coenzyme A:cholesterol acyltransferase-1 to decrease THP-1 macrophage-derived foam cell formation. Acta Biochim Biophys Sin (Shanghai) 2013;45:953-962.
40. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS: Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 2006;24:857-864.
41. Jeyabal P, Thandavarayan RA, Joladarashi D, Suresh Babu S, Krishnamurthy S, Bhimaraj A, Youker KA, Kishore R, Krishnamurthy P: MicroRNA-9 inhibits hyperglycemia-induced pyroptosis in human ventricular cardiomyocytes by targeting ELAVL1. Biochem Biophys Res Commun 2016;471:423-429.
42. Jones SW, Watkins G, Le Good N, Roberts S, Murphy CL, Brockbank SM, Needham MR, Read SJ, Newham P: The identification of differentially expressed microRNA in osteoarthritic tissue that modulate the production of TNF-alpha and MMP13. Osteoarthritis Cartilage 2009;17:464-472.
43. Medzhitov R: Toll-like receptors and innate immunity. Nat Rev Immunol 2001;1:135-145.
44. Sheedy FJ, Grebe A, Rayner KJ, Kalantari P, Ramkhelawon B, Carpenter SB, Becker CE, Ediriweera HN, Mullick AE, Golenbock DT, Stuart LM, Latz E, Fitzgerald KA, Moore KJ: CD36 coordinates NLRP3 inflammasome activation by facilitating intracellular nucleation of soluble ligands into particulate ligands in sterile inflammation. Nat Immunol 2013;14:812-820.
45. Abderrazak A, Couchie D, Mahmood DF, Elhage R, Vindis C, Laffargue M, Mateo V, Buchele B, Ayala MR, El Gaafary M, Syrovets T, Slimane MN, Friguet B, Fulop T, Simmet T, El Hadri K, Rouis M: Anti-inflammatory and antiatherogenic effects of the NLRP3 inflammasome inhibitor arglabin in ApoE2.Ki mice fed a high-fat diet. Circulation 2015;131:1061-1070.
46. Usui F, Shirasuna K, Kimura H, Tatsumi K, Kawashima A, Karasawa T, Hida S, Sagara J, Taniguchi S, Takahashi M: Critical role of caspase-1 in vascular inflammation and development of atherosclerosis in Western diet-fed apolipoprotein E-deficient mice. Biochem Biophys Res Commun 2012;425:162-168.
47. Li S, Fan Q, He S, Tang T, Liao Y, Xie J: MicroRNA-21 negatively regulates Treg cells through a TGF-beta1/Smad-independent pathway in patients with coronary heart disease. Cell Physiol Biochem 2015;37:866-878.
48. Zuo K, Zhi K, Zhang X, Lu C, Wang S, Li M, He B: A dysregulated microRNA-26a/EphA2 axis impairs endothelial progenitor cell function via the p38 MAPK/VEGF pathway. Cell Physiol Biochem 2015;35:477-488.
49. Zhao J, Lin Q, Kim KJ, Dardashti FD, Kim J, He F, Sun Y: Ngn1 inhibits astrogliogenesis through induction of miR-9 during neuronal fate specification. Elife 2015;4:e06885.
50. Zhang C, Zhao YX, Zhang YH, Zhu L, Deng BP, Zhou ZL, Li SY, Lu XT, Song LL, Lei XM, Tang WB, Wang N, Pan CM, Song HD, Liu CX, Dong B, Zhang Y, Cao Y: Angiotensin-converting enzyme 2 attenuates atherosclerotic lesions by targeting vascular cells. Proc Natl Acad Sci U S A 2010;107:15886-15891.
51. O'Shea JJ, Plenge R: JAK and STAT signaling molecules in immunoregulation and immune-mediated disease. Immunity 2012;36:542-550.
52. Maziere C, Alimardani G, Dantin F, Dubois F, Conte MA, Maziere JC: Oxidized LDL activates STAT1 and STAT3 transcription factors: Possible involvement of reactive oxygen species. FEBS Lett 1999;448:49-52.
53. Maziere C, Conte MA, Maziere JC: Activation of JAK2 by the oxidative stress generated with oxidized low-density lipoprotein. Free Radic Biol Med 2001;31:1334-1340.
54. Capiralla H, Vingtdeux V, Zhao H, Sankowski R, Al-Abed Y, Davies P, Marambaud P: Resveratrol mitigates lipopolysaccharide- and Abeta-mediated microglial inflammation by inhibiting the TLR4/NF-kappaB/STAT signaling cascade. J Neurochem 2012;120:461-472.
55. Lu B, Antoine DJ, Kwan K, Lundback P, Wahamaa H, Schierbeck H, Robinson M, Van Zoelen MA, Yang H, Li J, Erlandsson-Harris H, Chavan SS, Wang H, Andersson U, Tracey KJ: JAK/STAT1 signaling promotes HMGB1 hyperacetylation and nuclear translocation. Proc Natl Acad Sci U S A 2014;111:3068-3073.
56. Guarda G, Braun M, Staehli F, Tardivel A, Mattmann C, Forster I, Farlik M, Decker T, Du Pasquier RA, Romero P, Tschopp J: Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011;34:213-223.