Moderate hypoxia potentiates interleukin-1â production in activated human macrophages

Circulation Research

Volumn 115, Issue 10, 2014, Pages 875-883

  Folco, Eduardo J ^a   Sukhova, Galina K ^a   Quillard, Thibaut ^a   Libby, Peter ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Autophagy; Hypoxia; Inflammasomes; Inflammation; Interleukins

Indexed keywords

CHOLESTEROL; HEXOKINASE; HEXOKINASE 2; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; UNCLASSIFIED DRUG;

ARTICLE; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; CATABOLISM; CHOLESTEROL METABOLISM; CONTROLLED STUDY; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MACROPHAGE ACTIVATION; MONONUCLEAR PHAGOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BIOSYNTHESIS; CELL CULTURE; CELL HYPOXIA; MACROPHAGE; METABOLISM; MONONUCLEAR CELL; PHYSIOLOGY;

CELL HYPOXIA; CELLS, CULTURED; HUMANS; INTERLEUKIN-1BETA; LEUKOCYTES, MONONUCLEAR; MACROPHAGES;

EID: 84917736664     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.304437     Document Type: Article

References (52)

1. Dinarello CA. Immunological and infammatory functions of the interleu-kin-1 family. Annu Rev Immunol. 2009;27:519-550.
2. Kurt-Jones EA, Beller DI, Mizel SB, Unanue ER. Identifcation of a membrane-associated interleukin 1 in macrophages. Proc Natl Acad Sci USA. 1985;82:1204-1208.
3. Latz E, Xiao TS, Stutz A. Activation and regulation of the infammasomes. Nat Rev Immunol. 2013;13:397-411.
4. Schönbeck U, Mach F, Libby P. Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing. J Immunol. 1998;161:3340-3346.
5. Duewell P, Kono H, Rayner KJ, et al. NLRP3 infammasomes are required for atherogenesis and activated by cholesterol crystals. Nature. 2010;464:1357-1361.
6. Alexander MR, Moehle CW, Johnson JL, Yang Z, Lee JK, Jackson CL, Owens GK. Genetic inactivation of IL-1 signaling enhances atherosclerotic plaque instability and reduces outward vessel remodeling in advanced atherosclerosis in mice. J Clin Invest. 2012;122:70-79.
7. Chamberlain J, Evans D, King A, Dewberry R, Dower S, Crossman D, Francis S. Interleukin-1beta and signaling of interleukin-1 in vascular wall and circulating cells modulates the extent of neointima formation in mice. Am J Pathol. 2006;168:1396-1403.
8. Isoda K, Shiigai M, Ishigami N, Matsuki T, Horai R, Nishikawa K, Kusuhara M, Nishida Y, Iwakura Y, Ohsuzu F. Defciency of interleu-kin-1 receptor antagonist promotes neointimal formation after injury. Circulation. 2003;108:516-518.
9. Merhi-Soussi F, Kwak BR, Magne D, Chadjichristos C, Berti M, Pelli G, James RW, Mach F, Gabay C. Interleukin-1 plays a major role in vascular infammation and atherosclerosis in male apolipoprotein E-knockout mice. Cardiovasc Res. 2005;66:583-593.
10. Olofsson PS, Sheikine Y, Jatta K, Ghaderi M, Samnegård A, Eriksson P, Sirsjö A. A functional interleukin-1 receptor antagonist polymorphism in-fuences atherosclerosis development. The interleukin-1beta:interleukin-1 receptor antagonist balance in atherosclerosis. Circ J. 2009;73:1531-1536.
11. Freigang S, Ampenberger F, Weiss A, Kanneganti TD, Iwakura Y, Hersberger M, Kopf M. Fatty acid-induced mitochondrial uncoupling elicits infammasome-independent IL-1α and sterile vascular infammation in atherosclerosis. Nat Immunol. 2013;14:1045-1053.
12. Kamari Y, Werman-Venkert R, Shaish A, Werman A, Harari A, Gonen A, Voronov E, Grosskopf I, Sharabi Y, Grossman E, Iwakura Y, Dinarello CA, Apte RN, Harats D. Differential role and tissue specifcity of inter-leukin-1alpha gene expression in atherogenesis and lipid metabolism. Atherosclerosis. 2007;195:31-38.
13. 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-defcient mice. Arterioscler Thromb Vasc Biol. 2003;23:656-660.
14. Shimokawa H, Ito A, Fukumoto Y, Kadokami T, Nakaike R, Sakata M, Takayanagi T, Egashira K, Takeshita A. Chronic treatment with interleu-kin-1 beta induces coronary intimal lesions and vasospastic responses in pigs in vivo. The role of platelet-derived growth factor. J Clin Invest. 1996;97769-776.
15. 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.
16. Dalekos GN, Elisaf M, Bairaktari E, Tsolas O, Siamopoulos KC. Increased serum levels of interleukin-1beta in the systemic circulation of patients with essential hypertension: additional risk factor for atherogenesis in hypertensive patients? J Lab Clin Med. 1997;129:300-308.
17. Ridker PM, Thuren T, Zalewski A, Libby P. Interleukin-1β inhibition and the prevention of recurrent cardiovascular events: rationale and design of the Canakinumab Anti-infammatory Thrombosis Outcomes Study (CANTOS). Am Heart J. 2011;162:597-605.
18. Heughan C, Niinikoski J, Hunt TK. Oxygen tensions in lesions of experimental atherosclerosis of rabbits. Atherosclerosis. 1973;17:361-367.
19. Björnheden T, Levin M, Evaldsson M, Wiklund O. Evidence of hypox-ic areas within the arterial wall in vivo. Arterioscler Thromb Vasc Biol. 1999;19:870-876.
20. Sluimer JC, Gasc JM, van Wanroij JL, Kisters N, Groeneweg M, Sollewijn Gelpke MD, Cleutjens JP, van den Akker LH, Corvol P, Wouters BG, Daemen MJ, Bijnens AP. Hypoxia, hypoxia-inducible transcription factor, and macrophages in human atherosclerotic plaques are correlated with intraplaque angiogenesis. J Am Coll Cardiol. 2008;51:1258-1265.
21. Jun J, Reinke C, Bedja D, Berkowitz D, Bevans-Fonti S, Li J, Barouch LA, Gabrielson K, Polotsky VY. Effect of intermittent hypoxia on atherosclerosis in apolipoprotein E-defcient mice. Atherosclerosis. 2010;209:381-386.
22. Nakano D, Hayashi T, Tazawa N, Yamashita C, Inamoto S, Okuda N, Mori T, Sohmiya K, Kitaura Y, Okada Y, Matsumura Y. Chronic hypoxia accelerates the progression of atherosclerosis in apolipoprotein E-knockout mice. Hypertens Res. 2005;28:837-845.
23. Libby P, Folco E. Tension in the plaque: hypoxia modulates metabolism in atheroma. Circ Res. 2011;109:1100-1102.
24. Marsch E, Sluimer JC, Daemen MJ. Hypoxia in atherosclerosis and in-fammation. Curr Opin Lipidol. 2013;24:393-400.
25. Moulton KS, Heller E, Konerding MA, Flynn E, Palinski W, Folkman J. Angiogenesis inhibitors endostatin or TNP-470 reduce intimal neo-vascularization and plaque growth in apolipoprotein E-defcient mice. Circulation. 1999;99:1726-1732.
26. Boström P, Magnusson B, Svensson PA, Wiklund O, Borén J, Carlsson LM, Ståhlman M, Olofsson SO, Hultén LM. Hypoxia converts human macrophages into triglyceride-loaded foam cells. Arterioscler Thromb Vasc Biol. 2006;26:1871-1876.
27. Parathath S, Mick SL, Feig JE, Joaquin V, Grauer L, Habiel DM, Gassmann M, Gardner LB, Fisher EA. Hypoxia is present in murine atherosclerotic plaques and has multiple adverse effects on macrophage lipid metabolism. Circ Res. 2011;109:1141-1152.
28. Folco EJ, Sheikine Y, Rocha VZ, Christen T, Shvartz E, Sukhova GK, Di Carli MF, Libby P. Hypoxia but not infammation augments glucose uptake in human macrophages: Implications for imaging atherosclerosis with 18fuorine-labeled 2-deoxy-D-glucose positron emission tomography. J Am Coll Cardiol. 2011;58:603-614.
29. Semenza GL. Oxygen-dependent regulation of mitochondrial respiration by hypoxia-inducible factor 1. Biochem J. 2007;405:1-9.
30. Burke B, Giannoudis A, Corke KP, Gill D, Wells M, Ziegler-Heitbrock L, Lewis CE. Hypoxia-induced gene expression in human macrophages: implications for ischemic tissues and hypoxia-regulated gene therapy. Am J Pathol. 2003;163:1233-1243.
31. Deguchi JO, Yamazaki H, Aikawa E, Aikawa M. Chronic hypoxia activates the Akt and beta-catenin pathways in human macrophages. Arterioscler Thromb Vasc Biol. 2009;29:1664-1670.
32. Kolev K, Skopál J, Simon L, Csonka E, Machovich R, Nagy Z. Matrix metalloproteinase-9 expression in post-hypoxic human brain capillary en-dothelial cells: H2O2 as a trigger and NF-kappaB as a signal transducer. Thromb Haemost. 2003;90:528-537.
33. Liu J, Sukhova GK, Sun JS, Xu WH, Libby P, Shi GP. Lysosomal cys-teine proteases in atherosclerosis. Arterioscler Thromb Vasc Biol. 2004;24:1359-1366.
34. Rajamäki K, Lappalainen J, Oörni K, Välimäki E, Matikainen S, Kovanen PT, Eklund KK. Cholesterol crystals activate the NLRP3 infammasome in human macrophages: a novel link between cholesterol metabolism and infammation. PLoS One. 2010;5:e11765.
35. Folco EJ, Koren G. Degradation of the inducible cAMP early repressor (ICER) by the ubiquitin-proteasome pathway. Biochem J. 1997;328 (Pt 1):37-43.
36. Freigang S, Ampenberger F, Spohn G, Heer S, Shamshiev AT, Kisielow J, Hersberger M, Yamamoto M, Bachmann MF, Kopf M. Nrf2 is essential for cholesterol crystal-induced infammasome activation and exacerbation of atherosclerosis. Eur J Immunol. 2011;41:2040-2051.
37. Radwan M, Stiefvater R, Grunert T, Sharif O, Miller I, Marchetti-Deschmann M, Allmaier G, Gemeiner M, Knapp S, Kovarik P, Müller M, Strobl B. Tyrosine kinase 2 controls IL-1ß production at the translational level. J Immunol. 2010;185:3544-3553.
38. Harris J, Hartman M, Roche C, Zeng SG, O'Shea A, Sharp FA, Lambe EM, Creagh EM, Golenbock DT, Tschopp J, Kornfeld H, Fitzgerald KA, Lavelle EC. Autophagy controls IL-1beta secretion by targeting pro-IL-1beta for degradation. J Biol Chem. 2011;286:9587-9597.
39. Mazure NM, Pouysségur J. Hypoxia-induced autophagy: cell death or cell survival? Curr Opin Cell Biol. 2010;22:177-180.
40. Klionsky DJ, Abdalla FC, Abeliovich H et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012;8:445-544.
41. Small DM. George Lyman Duff memorial lecture. Progression and regression of atherosclerotic lesions. Insights from lipid physical biochemistry. Arteriosclerosis. 1988;8:103-129.
42. Muñoz-Planillo R, Kuffa P, Martínez-Colón G, Smith BL, Rajendiran TM, Núñez G. K+ effux is the common trigger of NLRP3 infammasome activation by bacterial toxins and particulate matter. Immunity. 2013;38:1142-1153.
43. 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 infammasome in response to toxins and ATP. Nature. 2006;440:228-232.
44. 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 cy-tokine receptors license NLRP3 infammasome activation by regulating NLRP3 expression. J Immunol. 2009;183:787-791.
45. Tanahill GM, Curtis AM, Adamik J, et al. Succinate is an infammatory signal that induces IL-1β through HIF-1α. Nature. 2013;496:238-242.
46. Liao X, Sluimer JC, Wang Y, Subramanian M, Brown K, Pattison JS, Robbins J, Martinez J, Tabas I. Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab. 2012;15:545-553.
47. Razani B, Feng C, Coleman T, Emanuel R, Wen H, Hwang S, Ting JP, Virgin HW, Kastan MB, Semenkovich CF. Autophagy links infamma-somes to atherosclerotic progression. Cell Metab. 2012;15:534-544.
48. Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280-293.
49. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728-741.
50. Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy. 2011;7:279-296.
51. Xavier RJ, Huett A, Rioux JD. Autophagy as an important process in gut homeostasis and Crohn's disease pathogenesis. Gut. 2008;57:717-720.
52. de Luca A, Smeekens SP, Casagrande A, et al. IL-1 receptor blockade restores autophagy and reduces infammation in chronic granu-lomatous disease in mice and in humans. Proc Natl Acad Sci USA. 2014;111:3526-3531.