NLRP3 Inflammasome Expression and Activation in Human Atherosclerosis

Journal of the American Heart Association

Volumn 5, Issue 5, 2016, Pages

  Paramel Varghese, Geena ^a   Folkersen, Lasse ^b   Strawbridge, Rona J ^b   Halvorsen, Bente ^d,e   Yndestad, Arne ^d,e   Ranheim, Trine ^d,e   Krohg Sørensen, Kirsten ^d   Skjelland, Mona ^d   Espevik, Terje ^f   Aukrust, Pål ^d,e   Lengquist, Mariette ^c   Hedin, Ulf ^c   Jansson, Jan Håkan ^g   Fransén, Karin ^a   Hansson, Göran K ^b   Eriksson, Per ^b   Sirsjö, Allan ^a  

^a Örebro University   (Sweden)

^b KAROLINSKA INSTITUTE   (Sweden)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d OSLO UNIVERSITY HOSPITAL   (Norway)

^e UNIVERSITY OF OSLO   (Norway)

^f NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^g UMEÅ UNIVERSITY HOSPITAL   (Sweden)

Author keywords

NLRP3; Inflammasome; Interleukin 1 ; Myocardial infarction; Polymorphism

Indexed keywords

ADENOSINE TRIPHOSPHATE; CD68 ANTIGEN; CRYOPYRIN; DNA; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; MESSENGER RNA; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; CCL2 PROTEIN, HUMAN; IL1B PROTEIN, HUMAN; MONOCYTE CHEMOTACTIC PROTEIN 1; NLRP3 PROTEIN, HUMAN; PYCARD PROTEIN, HUMAN; TNF PROTEIN, HUMAN; TUMOR NECROSIS FACTOR;

ALLELE; ARTICLE; ATHEROSCLEROSIS; CARDIOVASCULAR RISK; CAROTID ATHEROSCLEROSIS; COHORT ANALYSIS; CONTROLLED STUDY; CYTOKINE RELEASE; DOWN REGULATION; GENE EXPRESSION; GENE FREQUENCY; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HEART INFARCTION; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; MACROPHAGE; MAJOR CLINICAL STUDY; NLRP3 GENE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SINGLE NUCLEOTIDE POLYMORPHISM; SMOOTH MUSCLE CELL; SYMPTOMATOLOGY; ATHEROSCLEROTIC PLAQUE; GENETICS; GENOTYPE; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; MONONUCLEAR CELL; SWEDEN;

ATHEROSCLEROSIS; CARD SIGNALING ADAPTOR PROTEINS; CASPASE 1; CHEMOKINE CCL2; GENOTYPE; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMASOMES; INTERLEUKIN-18; INTERLEUKIN-1BETA; LEUKOCYTES, MONONUCLEAR; MYOCARDIAL INFARCTION; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PLAQUE, ATHEROSCLEROTIC; POLYMORPHISM, SINGLE NUCLEOTIDE; RNA, MESSENGER; SWEDEN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84994573306     PISSN: None     EISSN: 20479980     Source Type: Journal    
DOI: 10.1161/JAHA.115.003031     Document Type: Article

References (45)

1. Dutta P, Courties G, Wei Y, Leuschner F, Gorbatov R, Robbins CS, Iwamoto Y, Thompson B, Carlson AL, Heidt T, Majmudar MD, Lasitschka F, Etzrodt M, Waterman P, Waring MT, Chicoine AT, van der Laan AM, Niessen HW, Piek JJ, Rubin BB, Butany J, Stone JR, Katus HA, Murphy SA, Morrow DA, Sabatine MS, Vinegoni C, Moskowitz MA, Pittet MJ, Libby P, Lin CP, Swirski FK, Weissleder R, Nahrendorf M. Myocardial infarction accelerates atherosclerosis. Nature. 2012;487:325-329.
2. Galea J, Armstrong J, Gadsdon P, Holden H, Francis SE, Holt CM. Interleukin-1 beta in coronary arteries of patients with ischemic heart disease. Arterioscler Thromb Vasc Biol. 1996;16:1000-1006.
3. Gerdes N, Sukhova GK, Libby P, Reynolds RS, Young JL, Schonbeck U. Expression of interleukin (IL)-18 and functional IL-18 receptor on human vascular endothelial cells, smooth muscle cells, and macrophages: implications for atherogenesis. J Exp Med. 2002;195:245-257.
4. Mallat Z, Corbaz A, Scoazec A, Graber P, Alouani S, Esposito B, Humbert Y, Chvatchko Y, Tedgui A. Interleukin-18/interleukin-18 binding protein signaling modulates atherosclerotic lesion development and stability. Circ Res. 2001;89:E41-E45.
5. Olofsson PS, Sheikine Y, Jatta K, Ghaderi M, Samnegård A, Eriksson P, Sirsjö A. A functional interleukin-1 receptor antagonist polymorphism influences atherosclerosis development. The interleukin-1beta:interleukin-1 receptor antagonist balance in atherosclerosis. Circ J. 2009;73:1531-1536.
6. Kirii H, Niwa T, Yamada Y, Wada H, Saito K, Iwakura Y, Asano M, Moriwaki H, Seishima M. Lack of interleukin-1beta decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:656-660.
7. Elhage R, Jawien J, Rudling M, Ljunggren HG, Takeda K, Akira S, Bayard F, Hansson GK. Reduced atherosclerosis in interleukin-18 deficient apolipoprotein E-knockout mice. Cardiovasc Res. 2003;59:234-240.
8. Barker BR, Taxman DJ, Ting JPY. Cross-regulation between the IL-1β/IL-18 processing inflammasome and other inflammatory cytokines. Curr Opin Immunol. 2011;23:591-597.
9. Martinon F, Burns K, Tschopp J. The inflammasome: a molecular platform triggering activation of inflammatory caspases and processing of proIL-beta. Mol Cell. 2002;10:417-426.
10. Franchi L, Munoz-Planillo R, Nunez G. Sensing and reacting to microbes through the inflammasomes. Nat Immunol. 2012;13:325-332.
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. Martinon F, Petrilli V, Mayor A, Tardivel A, Tschopp J. Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature. 2006;440:237-241.
13. Rajamaki K, Lappalainen J, Oorni K, Välimäki 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.
14. Duewell P, Kono H, Rayner KJ, Sirois CM, Vladimer G, Bauernfeind FG, Abela GS, Franchi L, Nuñez 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.
15. Kawaguchi M, Takahashi M, Hata T, Kashima Y, Usui F, Morimoto H, Izawa A, Takahashi Y, Masumoto J, Koyama J, Hongo M, Noda T, Nakayama J, Sagara J, Taniguchi S, Ikeda U. Inflammasome activation of cardiac fibroblasts is essential for myocardial ischemia/reperfusion injury. Circulation. 2011;123:594-604.
16. Sandanger O, Ranheim T, Vinge LE, Bliksøen M, Alfsnes K, Finsen AV, Dahl CP, Askevold ET, Florholmen G, Christensen G, Fitzgerald KA, Lien E, Valen G, Espevik T, Aukrust P, Yndestad A. The NLRP3 inflammasome is up-regulated in cardiac fibroblasts and mediates myocardial ischaemia-reperfusion injury. Cardiovasc Res. 2013;99:164-174.
17. Li X, Zhang Y, Xia M, Gulbins E, Boini KM, Li PL. Activation of Nlrp3 inflammasomes enhances macrophage lipid-deposition and migration: implication of a novel role of inflammasome in atherogenesis. PLoS One. 2014;9:e87552.
18. Menu P, Pellegrin M, Aubert JF, Bouzourene K, Tardivel A, Mazzolai L, Tschopp J. Atherosclerosis in ApoE-deficient mice progresses independently of the NLRP3 inflammasome. Cell Death Dis. 2011;2:e137.
19. Yu JR, Leslie KS. Cryopyrin-associated periodic syndrome: an update on diagnosis and treatment response. Curr Allergy Asthma Rep. 2011;11:12-20.
20. Pontillo A, Vendramin A, Catamo E, Fabris A, Crovella S. The missense variation Q705K in CIAS1/NALP3/NLRP3 gene and an NLRP1 haplotype are associated with celiac disease. Am J Gastroenterol. 2011;106:539-544.
21. Roberts RL, Van Rij AM, Phillips LV, Young S, McCormick SP, Merriman TR, Jones GT. Interaction of the inflammasome genes CARD8 and NLRP3 in abdominal aortic aneurysms. Atherosclerosis. 2011;218:123-126.
22. Kastbom A, Verma D, Eriksson P, Skogh T, Wingren G, Soderkvist P. Genetic variation in proteins of the cryopyrin inflammasome influences susceptibility and severity of rheumatoid arthritis (the Swedish TIRA project). Rheumatology. 2008;47:415-417.
23. Schoultz I, Verma D, Halfvarsson J, Törkvist L, Fredrikson M, Sjöqvist U, Lördal M, Tysk C, Lerm M, Söderkvist P, Söderholm JD. Combined polymorphisms in genes encoding the inflammasome components NALP3 and CARD8 confer susceptibility to Crohn's disease in Swedish men. Am J Gastroenterol. 2009;104:1180-1188.
24. Villani AC, Lemire M, Fortin G, Louis E, Silverberg MS, Collette C, Baba N, Libioulle C, Belaiche J, Bitton A, Gaudet D, Cohen A, Langelier D, Fortin PR, Wither JE, Sarfati M, Rutgeerts P, Rioux JD, Vermeire S, Hudson TJ, Franchimont D. Common variants in the NLRP3 region contribute to Crohn's disease susceptibility. Nat Genet. 2009;41:71-76.
25. Folkersen L, van't Hooft F, Chernogubova E, Agardh HE, Hansson GK, Hedin U, Liska J, Syvänen AC, Paulsson-Berne G, Franco-Cereceda A, Hamsten A, Gabrielsen A, Eriksson P; BiKE and ASAP study groups. Association of genetic risk variants with expression of proximal genes identifies novel susceptibility genes for cardiovascular disease. Circ Cardiovasc Genet. 2010;3:365-373.
26. Folkersen L, Persson J, Ekstrand J, Agardh HE, Hansson GK, Gabrielsen A, Hedin U, Paulsson-Berne G. Prediction of ischemic events on the basis of transcriptomic and genomic profiling in patients undergoing carotid endarterectomy. Mol Med. 2012;18:669-675.
27. Van Guelpen B, Hultdin J, Johansson I, Witthöft C, Weinehall L, Eliasson M, Hallmans G, Palmqvist R, Jansson JH, Winkvist A. Plasma folate and total homocysteine levels are associated with the risk of myocardial infarction, independently of each other and of renal function. J Intern Med. 2009;266:182-195.
28. Samnegard A, Silveira A, Lundman P, Boquist S, Odeberg J, Hulthe J, McPheat W, Tornvall P, Bergstrand L, Ericsson CG, Hamsten A, Eriksson P. Serum matrix metalloproteinase-3 concentration is influenced by MMP-3-1612 5A/6A promoter genotype and associated with myocardial infarction. J Intern Med. 2005;258:411-419.
29. Olofsson PS, Jatta K, Wagsater D, Gredmark S, Hedin U, Paulsson-Berne G, Söderberg-Nauclér C, Hansson GK, Sirsjö A. The antiviral cytomegalovirus inducible gene 5/viperin is expressed in atherosclerosis and regulated by proinflammatory agents. Arterioscler Thromb Vasc Biol. 2005;25:e113-e116.
30. Samstad EO, Niyonzima N, Nymo S, Aune MH, Ryan L, Bakke SS, Lappegård KT, Brekke OL, Lambris JD, Damås JK, Latz E, Mollnes TE, Espevik T. Cholesterol crystals induce complement-dependent inflammasome activation and cytokine release. J Immunol. 2014;192:2837-2845.
31. Hulthe J, McPheat W, Samnegard A, Tornvall P, Hamsten A, Eriksson P. Plasma interleukin (IL)-18 concentrations is elevated in patients with previous myocardial infarction and related-to severity of coronary atherosclerosis independently of C-reactive protein and IL-6. Atherosclerosis. 2006;188:450-454.
32. Samnegård A, Hulthe J, Silveira A, Ericsson CG, Hamsten A, Eriksson P. Gender specific associations between matrix metalloproteinases and inflammatory markers in post myocardial infarction patients. Atherosclerosis. 2009;202:550-556.
33. Wennberg P, Wensley F, Di Angelantonio E, Johansson L, Boman K, Rumley A, Lowe G, Hallmans G, Danesh J, Jansson JH. Haemostatic and inflammatory markers are independently associated with myocardial infarction in men and women. Thromb Res. 2012;129:68-73.
34. Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MA, Bender D, Maller J, Sklar P, de Bakker PI, Daly MJ, Sham PC. PLINK: a tool set for whole-genome association and population-based linkage analyses. Am J Hum Genet. 2007;81:559-575.
35. Zheng F, Xing SS, Gong ZS, Xing QC. NLRP3 inflammasomes show high expression in aorta of patients with atherosclerosis. Heart Lung Circ. 2013;22:746-750.
36. Folkersen L, Kurtovic S, Razuvaev A, Agardh HE, Gabrielsen A, Paulsson-Berne G. Endogenous control genes in complex vascular tissue samples. BMC Genomics. 2009;10:516.
37. Bauernfeind FG, Horvath G, Stutz A, Alnemri ES, MacDonald K, Speert D, Fernandes-Alnemri T, Wu J, Monks BG, Fitzgerald KA, Hornung V, Latz E. Cutting edge: NF-kappaB activating pattern recognition and cytokine receptors license NLRP3 inflammasome activation by regulating NLRP3 expression. J Immunol. 2009;183:787-791.
38. Carr SC, Farb A, Pearce WH, Virmani R, Yao JST. Activated inflammatory cells are associated with plaque rupture in carotid artery stenosis. Surgery. 1997;122:757-763.
39. Peng K, Liu L, Wei D, Lv Y, Wang G, Xiong W, Wang X, Altaf A, Wang L, He D, Wang H, Qu P. P2X7R is involved in the progression of atherosclerosis by promoting NLRP3 inflammasome activation. Int J Mol Med. 2015;35:1179-1188.
40. Tangi TN, Elmabsout AA, Bengtsson T, Sirsjo A, Fransén K. Role of NLRP3 and CARD8 in the regulation of TNF-alpha induced IL-1beta release in vascular smooth muscle cells. Int J Mol Med. 2012;30:697-702.
41. Jander S, Sitzer M, Schumann R, Schroeter M, Siebler M, Steinmetz H, Stoll G. Inflammation in high-grade carotid stenosis: a possible role for macrophages and T cells in plaque destabilization. Stroke. 1998;29:1625-1630.
42. Griffiths RJ, Stam EJ, Downs JT, Otterness IG. ATP induces the release of IL-1 from LPS-primed cells in vivo. J Immunol. 1995;154:2821-2828.
43. Lewis GJ, Massey DCO, Zhang H, Bredin F, Tremelling M, Lee JC, Berzuini C, Parkes M. Genetic association between NLRP3 variants and Crohn's disease does not replicate in a large UK panel. Inflamm Bowel Dis. 2011;17:1387-1391.
44. Kastbom A, Klingberg E, Verma D, Carlsten H, Forsblad-d'Elia H, Wesamaa J, Cedergren J, Eriksson P, Söderkvist P.Genetic variants in CARD8 but not in NLRP3 are associated with ankylosing spondylitis. Scand J Rheumatol. 2013;42:465-468.
45. Lappalainen T, Hannelius U, Salmela E, von Döbeln U, Lindgren CM, Huoponen K, Savontaus ML, Kere J, Lahermo P. Population structure in contemporary Sweden-a Y-chromosomal and mitochondrial DNA analysis. Ann Hum Genet. 2009;73:61-73.