Saturated fatty acids activate caspase-4/5 in human monocytes, triggering IL-1β and IL-18 release

American Journal of Physiology - Endocrinology and Metabolism

Volumn 311, Issue 5, 2016, Pages E825-E835

  Pillon, Nicolas J ^a   Chan, Kenny L ^a   Zhang, Shitian ^b   Mejdani, Marios ^a   Jacobson, Maya R ^a   Ducos, Alexandre ^a   Bilan, Philip J ^a   Niu, Wenyan ^b   Klip, Amira ^a  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Caspase; Fatty acids; Inflammation; Interleukin 1 ; Monocytes; Palmitate; Pyroptosis; THP 1

Indexed keywords

CASPASE 4; CASPASE 5; CHOLESTEROL; GLUCOSE; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; LACTATE DEHYDROGENASE; PALMITIC ACID; SATURATED FATTY ACID; TRIACYLGLYCEROL; UNSATURATED FATTY ACID; CASP4 PROTEIN, HUMAN; CASP5 PROTEIN, HUMAN; CASPASE; CASPASE INHIBITOR; FATTY ACID; IL1B PROTEIN, HUMAN; INITIATOR CASPASE; MESSENGER RNA; MONOUNSATURATED FATTY ACID; PALMITIC ACID DERIVATIVE; PALMITOLEIC ACID;

ANIMAL CELL; ARTICLE; BONE MARROW DERIVED MACROPHAGE; CELL DEATH; CELL VOLUME; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE SILENCING; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; MONOCYTE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PYROPTOSIS; TRIACYLGLYCEROL BLOOD LEVEL; ADULT; CELL LINE; COMPLICATION; DRUG EFFECTS; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOBLOTTING; MALE; METABOLISM; MIDDLE AGED; PILOT STUDY; POLYMERASE CHAIN REACTION; SECRETION (PROCESS);

ADULT; CASPASE INHIBITORS; CASPASES; CASPASES, INITIATOR; CELL LINE; DIABETES MELLITUS, TYPE 2; ENZYME-LINKED IMMUNOSORBENT ASSAY; FATTY ACIDS; FATTY ACIDS, MONOUNSATURATED; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; HUMANS; IMMUNOBLOTTING; INTERLEUKIN-18; INTERLEUKIN-1BETA; MALE; MIDDLE AGED; MONOCYTES; OBESITY; OVERWEIGHT; PALMITATES; PILOT PROJECTS; POLYMERASE CHAIN REACTION; PYROPTOSIS; RNA, MESSENGER;

EID: 84994613486     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00296.2016     Document Type: Article

References (54)

1. Aachoui Y, Sagulenko V, Miao EA, Stacey KJ. Inflammasome-mediated pyroptotic and apoptotic cell death, and defense against infection. Curr Opin Microbiol 16: 319-326, 2013.
2. Baker PJ, Boucher D, Bierschenk D, Tebartz C, Whitney PG, D’Silva DB, Tanzer MC, Monteleone M, Robertson AAB, Cooper MA, Alvarez-Diaz S, Herold MJ, Bedoui S, Schroder K, Masters SL. NLRP3 inflammasome activation downstream of cytoplasmic LPS recognition by both caspase-4 and caspase-5. Eur J Immunol 45: 2918-2926, 2015.
3. Bergsbaken T, Fink SL, Cookson BT. Pyroptosis: host cell death and inflammation. Nat Rev Microbiol 7: 99-109, 2009.
4. Bergsbaken T, Fink SL, den Hartigh AB, Loomis WP, Cookson BT. Coordinated host responses during pyroptosis: caspase-1-dependent lysosome exocytosis and inflammatory cytokine maturation. J Immunol 187: 2748-2754, 2011.
5. Chan KL, Pillon NJ, Sivaloganathan DM, Costford SR, Liu Z, Théret M, Chazaud B, Klip A. Palmitoleate reverses high fat-induced proinflammatory macrophage polarization via AMP-activated protein kinase (AMPK). J Biol Chem 290: 16979-16988, 2015.
6. Dimopoulos N, Watson M, Sakamoto K, Hundal HS. Differential effects of palmitate and palmitoleate on insulin action and glucose utilization in rat L6 skeletal muscle cells. Biochem J 399: 473-481, 2006.
7. Dinarello CA, Donath MY, Mandrup-Poulsen T. Role of IL-1beta in type 2 diabetes. Curr Opin Endocrinol Diabetes Obes 17: 314-321, 2010.
8. Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol 11: 98-107, 2011.
9. Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol 35: 495-516, 2007.
10. Fink SL, Cookson BT. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect Immun 73: 1907-1916, 2005.
11. Fink SL, Cookson BT. Caspase-1-dependent pore formation during pyroptosis leads to osmotic lysis of infected host macrophages. Cell Microbiol 8: 1812-1825, 2006.
12. Garcia-Calvo M, Peterson EP, Leiting B, Ruel R, Nicholson DW, Thornberry NA. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J Biol Chem 273: 32608-32613, 1998.
13. Grimstad Ø, Husebye H, Espevik T. TLR3 mediates release of IL-1β and cell death in keratinocytes in a caspase-4 dependent manner. J Dermatol Sci 72: 45-53, 2013.
14. Han J, Zhong CQ, Zhang DW. Programmed necrosis: backup to and competitor with apoptosis in the immune system. Nat Immunol 12: 1143-1149, 2011.
15. He X, Qian Y, Li Z, Fan EK, Li Y, Wu L, Billiar TR, Wilson MA, Shi X, Fan J. TLR4-upregulated IL-1β and IL-1RI promote alveolar macrophage pyroptosis and lung inflammation through an autocrine mechanism. Sci Rep 6: 31663, 2016.
16. Idziorek T, Estaquier J, De Bels F, Ameisen JC. YOPRO-1 permits cytofluorometric analysis of programmed cell death (apoptosis) without interfering with cell viability. J Immunol Methods 185: 249-258, 1995.
17. Inoue H, Tani K. Multimodal immunogenic cancer cell death as a consequence of anticancer cytotoxic treatments. Cell Death Differ 21: 39-49, 2014.
18. Jorgensen I, Miao EA. Pyroptotic cell death defends against intracellular pathogens. Immunol Rev 265: 130-142, 2015.
19. Kahlenberg JM, Dubyak GR. Differing caspase-1 activation states in monocyte versus macrophage models of IL-1beta processing and release. J Leukoc Biol 76: 676-684, 2004.
20. Kajiwara Y, Schiff T, Voloudakis G, Gama Sosa MA, Elder G, Bozdagi O, Buxbaum JD. A critical role for human caspase-4 in endotoxin sensitivity. J Immunol 193: 335-343, 2014.
21. Klassen NV, Walker PR, Ross CK, Cygler J, Lach B. Two-stage cell shrinkage and the OER for radiation-induced apoptosis of rat thymocytes. Int J Radiat Biol 64: 571-581, 1993.
22. Lakshmanan U, Porter AG. Caspase-4 interacts with TNF receptorassociated factor 6 and mediates lipopolysaccharide-induced NF-kappaBdependent production of IL-8 and CC chemokine ligand 4 (macrophageinflammatory protein-1). J Immunol 179: 8480-8490, 2007.
23. Latz E, Xiao TS, Stutz A. Activation and regulation of the inflammasomes. Nat Rev Immunol 13: 397-411, 2013.
24. McIlwain DR, Berger T, Mak TW. Caspase functions in cell death and disease. Cold Spring Harb Perspect Biol 5: a008656, 2013.
25. Mei S, Ni HM, Manley S, Bockus A, Kassel KM, Luyendyk JP, Copple BL, Ding WX. Differential roles of unsaturated and saturated fatty acids on autophagy and apoptosis in hepatocytes. J Pharmacol Exp Ther 339: 487-498, 2011.
26. Miao EA, Rajan JV, Aderem A. Caspase-1-induced pyroptotic cell death. Immunol Rev 243: 206-214, 2011.
27. Netea MG, van de Veerdonk FL, Kullberg BJ, Van der Meer JWM, Joosten LAB. The role of NLRs and TLRs in the activation of the inflammasome. Expert Opin Biol Ther 8: 1867-1872, 2008.
28. Oh DY, Morinaga H, Talukdar S, Bae EJ, Olefsky JM. Increased macrophage migration into adipose tissue in obese mice. Diabetes 61: 346-354, 2012.
29. Pecht T, Haim Y, Bashan N, Shapiro H, Harman-Boehm I, Kirshtein B, Clément K, Shai I, Rudich A. Circulating blood monocyte subclasses and lipid-laden adipose tissue macrophages in human obesity. PLoS One 11: e0159350, 2016.
30. Peter ME. Programmed cell death: apoptosis meets necrosis. Nature 471: 310-312, 2011.
31. Pillon NJ, Li YE, Fink LN, Brozinick JT, Nikolayev A, Kuo MS, Bilan PJ, Klip A. Nucleotides released from palmitate-challenged muscle cells through pannexin-3 attract monocytes. Diabetes 63: 3815-3826, 2014.
32. Plantin-Carrenard E, Bringuier A, Derappe C, Pichon J, Guillot R, Bernard M, Foglietti MJ, Feldmann G, Aubery M, Braut-Boucher F. A fluorescence microplate assay using yopro-1 to measure apoptosis: application to HL60 cells subjected to oxidative stress. Cell Biol Toxicol 19: 121-133, 2003.
33. Poitou C, Dalmas E, Renovato M, Benhamo V, Hajduch F, Abdennour M, Kahn JF, Veyrie N, Rizkalla S, Fridman WH, Sautès-Fridman C, Clément K, Cremer I. CD14dimCD16 and CD14CD16 monocytes in obesity and during weight loss: relationships with fat mass and subclinical atherosclerosis. Arterioscler Thromb Vasc Biol 31: 2322-2330, 2011.
34. Pop C, Salvesen Human caspases: activation GS, specificity, regulation. J Biol Chem 284: 21777-21781, 2009.
35. Rayamajhi M, Zhang Y, Miao EA. Detection of pyroptosis by measuring released lactate dehydrogenase activity. Methods Mol Biol 1040: 85-90, 2013.
36. Reynolds CM, McGillicuddy FC, Harford KA, Finucane OM, Mills KHG, Roche HM. Dietary saturated fatty acids prime the NLRP3 inflammasome via TLR4 in dendritic cells-implications for diet-induced insulin resistance. Mol Nutr Food Res 56: 1212-1222, 2012.
37. Sahoo M, Ceballos-Olvera I, del Barrio L, Re F. Role of the inflammasome, IL-1β, and IL-18 in bacterial infections. Sci World J 11: 2037-2050, 2011.
38. Schilling JD, Machkovech HM, He L, Diwan A, Schaffer JE. TLR4 activation under lipotoxic conditions leads to synergistic macrophage cell death through a TRIF-dependent pathway. J Immunol 190: 1285-1296, 2013.
39. Schmid-Burgk JL, Gaidt MM, Schmidt T, Ebert TS, Bartok E, Hornung V. Caspase-4 mediates non-canonical activation of the NLRP3 inflammasome in human myeloid cells. Eur J Immunol 45: 2911-2917, 2015.
40. Seo SU, Kamada N, Muñoz-Planillo R, Kim YG, Kim D, Koizumi Y, Hasegawa M, Himpsl SD, Browne HP, Lawley TD, Mobley HLT, Inohara N, Núñez G. Distinct commensals induce interleukin-1β via NLRP3 inflammasome in inflammatory monocytes to promote intestinal inflammation in response to injury. Immunity 42: 744-755, 2015.
41. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116: 3015-3025, 2006.
42. Shi J, Zhao Y, Wang Y, Gao W, Ding J, Li P, Hu L, Shao F. Inflammatory caspases are innate immune receptors for intracellular LPS. Nature 514: 187-192, 2014.
43. Shikama Y, Aki N, Hata A, Nishimura M, Oyadomari S, Funaki M. Palmitate-stimulated monocytes induce adhesion molecule expression in endothelial cells via IL-1 signaling pathway. J Cell Physiol 230: 732-742, 2015.
44. Snodgrass RG, Huang S, Choi IW, Rutledge JC, Hwang DH. Inflammasome- mediated secretion of IL-1β in human monocytes through TLR2 activation; modulation by dietary fatty acids. J Immunol 191: 4337-4347, 2013.
45. Sollberger G, Strittmatter GE, Kistowska M, French LE, Beer HD. Caspase-4 is required for activation of inflammasomes. J Immunol 188: 1992-2000, 2012.
46. Sun GW, Lu J, Pervaiz S, Cao WP, Gan YH. Caspase-1 dependent macrophage death induced by Burkholderia pseudomallei. Cell Microbiol 7: 1447-1458, 2005.
47. Thorand B, Kolb H, Baumert J, Koenig W, Chambless L, Meisinger C, Illig T, Martin S, Herder C. Elevated levels of interleukin-18 predict the development of Type 2 diabetes results from the MONICA/KORA Augsburg Study, 1984-2002. Diabetes 54: 2932-2938, 2005.
48. Troegeler A, Lastrucci C, Duval C, Tanne A, Cougoule C, Maridonneau-Parini I, Neyrolles O, Lugo-Villarino G. An efficient siRNAmediated gene silencing in primary human monocytes, dendritic cells and macrophages. Immunol Cell Biol 92: 699-708, 2014.
49. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM, Dixit VD. The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 17: 179-188, 2011.
50. Viganò E, Diamond CE, Spreafico R, Balachander A, Sobota RM, Mortellaro A. Human caspase-4 and caspase-5 regulate the one-step non-canonical inflammasome activation in monocytes. Nat Commun 6: 8761, 2015.
51. de Vries JE, Vork MM, Roemen TH, de Jong YF, Cleutjens JP, van der Vusse GJ, van Bilsen M. Saturated but not mono-unsaturated fatty acids induce apoptotic cell death in neonatal rat ventricular myocytes. J Lipid Res 38: 1384-1394, 1997.
52. Wallach D, Kang TB, Kovalenko A. Concepts of tissue injury and cell death in inflammation: a historical perspective. Nat Rev Immunol 14: 51-59, 2014.
53. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MTH, Brickey WJ, Ting JPY. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 12: 408-415, 2011.
54. Zanoni I, Tan Y, Di Gioia M, Broggi A, Ruan J, Shi J, Donado CA, Shao F, Wu H, Springstead JR, Kagan JC. An endogenous caspase-11 ligand elicits interleukin-1 release from living dendritic cells. Science 352: 1232-1236, 2016.