Endoplasmic reticulum stress is sufficient for the induction of IL-1β production via activation of the NF-κB and inflammasome pathways

Innate Immunity

Volumn 20, Issue 8, 2014, Pages 799-815

  Kim, Sena ^a   Joe, Yeonsoo ^a   Jeong, Sun Oh ^a   Zheng, Min ^a,b   Back, Sung Hoon ^a   Park, Sang Won ^c   Ryter, Stefan W ^d   Chung, Hun Taeg ^a  

^a University of Ulsan   (South Korea)

^b YANBIAN UNIVERSITY   (China)

^c Gyeongsang National University School of Medicine   (South Korea)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

carbon monoxide; ER stress; heme oxygenase 1; inflammasome; reactive oxygen species

Indexed keywords

CARBON MONOXIDE; CHAPERONE; CRYOPYRIN; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PALMITIC ACID; REACTIVE OXYGEN METABOLITE; THIOREDOXIN; THIOREDOXIN INTERACTING PROTEIN; CARRIER PROTEIN; CYTOKINE; NLRP3 PROTEIN, HUMAN; PALMITIC ACID DERIVATIVE; TXNIP PROTEIN, MOUSE;

ADIPOCYTE; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL; MALE; MESSENGER RNA SYNTHESIS; MONOCYTIC LEUKEMIA; MOUSE; NONHUMAN; PERITONEUM MACROPHAGE; PROTEIN EXPRESSION; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; GENETICS; LIPID DIET; MACROPHAGE; METABOLISM; PHYSIOLOGY;

ANIMALS; CARRIER PROTEINS; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIET, HIGH-FAT; ENDOPLASMIC RETICULUM STRESS; INFLAMMASOMES; INTERLEUKIN-1BETA; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; NF-KAPPA B; PALMITATES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; THIOREDOXINS;

EID: 84908222221     PISSN: 17534259     EISSN: 17534267     Source Type: Journal    
DOI: 10.1177/1753425913508593     Document Type: Article

References (58)

1. Dinarello CA. Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood. 2011; 117: 3720-3732
2. Davis BK, Wen H, Ting JP. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu Rev Immunol. 2011; 29: 707-735
3. Lamkanfi M, Dixit VM. The inflammasomes. PLoS Pathog. 2009; 5: e1000510 - e1000510
4. Schroder K, Tschopp J. The inflammasomes. Cell. 2010; 140: 821-832
5. Kersse K, Bertrand MJ, Lamkanfi M, Vandenabeele P. NOD-like receptors and the innate immune system: coping with danger, damage and death. Cytokine Growth Factor Rev. 2011; 22: 257-276
6. Netea MG, Simon A, van de Veerdonk F, et al. IL-1beta processing in host defense: beyond the inflammasomes. PLoS Pathog. 2010; 6: e1000661 - e1000661
7. Dinarello CA. IL-1: discoveries, controversies and future directions. Eur J Immunol. 2010; 40: 599-606
8. Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature. 2012; 481: 278-286
9. Dostert C, Petrilli V, Van Bruggen R, et al. Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science. 2008; 320: 674-677
10. Martinon F. Signaling by ROS drives inflammasome activation. Eur J Immunol. 2010; 40: 616-619
11. Sorbara MT, Girardin SE. Mitochondrial ROS fuel the inflammasome. Cell Res. 2011; 21: 558-560
12. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature. 2011; 469: 221-225
13. Nakahira K, Haspel JA, Rathinam VA, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol. 2011; 12: 222-230
14. Zhou R, Tardivel A, Thorens B, et al. Thioredoxin-interacting protein links oxidative stress to inflammasome activation. Nat Immunol. 2010; 11: 136-140
15. Berndt C, Lillig CH, Holmgren A. Thiol-based mechanisms of the thioredoxin and glutaredoxin systems: implications for diseases in the cardiovascular system. Am J Physiol Heart Circ Physiol. 2007; 292: H1227 - H1236
16. Chung JW, Jeon JH, Yoon SR, Choi I. Vitamin D3 upregulated protein 1 (VDUP1) is a regulator for redox signaling and stress-mediated diseases. J Dermatol. 2006; 33: 662-669
17. Nishiyama A, Matsui M, Iwata S, et al. Identification of thioredoxin-binding protein-2/vitamin D(3) up-regulated protein 1 as a negative regulator of thioredoxin function and expression. J Biol Chem. 1999; 274: 21645-21650
18. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 1999; 13: 1211-1233
19. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005; 74: 739-789
20. Zhang K, Kaufman RJ. Signaling the unfolded protein response from the endoplasmic reticulum. J Biol Chem. 2004; 279: 25935-25938
21. Harding HP, Zhang Y, Ron D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature. 1999; 397: 271-274
22. Haze K, Yoshida H, Yanagi H, et al. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol Biol Cell. 1999; 10: 3787-3799
23. Rutkowski DT, Kaufman RJ. That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci. 2007; 32: 469-476
24. Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007; 8: 519-529
25. Kim I, Xu W, Reed JC. Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov. 2008; 7: 1013-1030
26. Kitamura M. Biphasic, bidirectional regulation of NF-kappaB by endoplasmic reticulum stress. Antioxid Redox Signal. 2009; 11: 2353-2364
27. Hu P, Han Z, Couvillon AD, et al. Autocrine tumor necrosis factor alpha links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol. 2006; 26: 3071-3084
28. Kaneko M, Niinuma Y, Nomura Y. Activation signal of nuclear factor-kappa B in response to endoplasmic reticulum stress is transduced via IRE1 and tumor necrosis factor receptor-associated factor 2. Biol Pharm Bull. 2003; 26: 931-935
29. Jiang HY, Wek SA, McGrath BC, et al. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol Cell Biol. 2004; 24: 1365-1377
30. Menu P, Mayor A, Zhou R, et al. ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis. 2012; 3: e261 - e261
31. Watt MJ, Hoy AJ, Muoio DM, Coleman RA. Distinct roles of specific fatty acids in cellular processes: implications for interpreting and reporting experiments. Am J Physiol Endocrinol Metab. 2012; 302: E1 - E3
32. Achard CS, Laybutt DR. Lipid-induced endoplasmic reticulum stress in liver cells results in two distinct outcomes: adaptation with enhanced insulin signaling or insulin resistance. Endocrinology. 2012; 153: 2164-2177
33. Cao J, Dai DL, Yao L, et al. Saturated fatty acid induction of endoplasmic reticulum stress and apoptosis in human liver cells via the PERK/ATF4/CHOP signaling pathway. Mol Cell Biochem. 2012; 364: 115-129
34. Ozcan L, Ergin AS, Lu A, et al. Endoplasmic reticulum stress plays a central role in development of leptin resistance. Cell Metab. 2009; 9: 35-51
35. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal. 2007; 9: 2277-2293
36. Santos CX, Tanaka LY, Wosniak J, Laurindo FR. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal. 2009; 11: 2409-2427
37. Tu BP, Weissman JS. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol. 2004; 164: 341-346
38. Brookes PS, Yoon Y, Robotham JL, et al. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol. 2004; 287: C817 - C833
39. Tenhunen R, Marver HS, Schmid R. Microsomal heme oxygenase. Characterization of the enzyme. J Biol Chem. 1969; 244: 6388-6394
40. Ryter SW, Choi AM. Heme oxygenase-1/carbon monoxide: from metabolism to molecular therapy. Am J Respir Cell Mol Biol. 2009; 41: 251-260
41. Lakshmanan AP, Thandavarayan RA, Palaniyandi SS, et al. Modulation of AT-1R/CHOP-JNK-Caspase12 pathway by olmesartan treatment attenuates ER stress-induced renal apoptosis in streptozotocin-induced diabetic mice. Eur J Pharm Sci. 2011; 44: 627-634
42. Zhang R, Kim JS, Kang KA, et al. Protective mechanism of KIOM-4 in streptozotocin-induced pancreatic beta-cells damage is involved in the inhibition of endoplasmic reticulum stress. Evid Based Complement Alternat Med. 2011; 2011: 1-10
43. Coe LM, Zhang J, McCabe LR. Both spontaneous Ins2(+/-) and streptozotocin-induced type I diabetes cause bone loss in young mice. J Cell Physiol. 2013; 228: 689-695
44. Gotoh T, Endo M, Oike Y. Endoplasmic reticulum stress-related inflammation and cardiovascular diseases. Int J Inflam. 2011; 2011: 259462-259462
45. Zhao L, Ackerman SL. Endoplasmic reticulum stress in health and disease. Curr Opin Cell Biol. 2006; 18: 444-452
46. Lin JH, Walter P, Yen TS. Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol. 2008; 3: 399-425
47. Ozcan U, Cao Q, Yilmaz E, et al. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science. 2004; 306: 457-461
48. Nakatani Y, Kaneto H, Kawamori D, et al. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem. 2005; 280: 847-851
49. Ozcan U, Yilmaz E, Ozcan L, et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science. 2006; 313: 1137-1140
50. Pahl HL, Baeuerle PA. Activation of NF-kappa B by ER stress requires both Ca2+and reactive oxygen intermediates as messengers. FEBS Lett. 1996; 392: 129-136
51. Kretz-Remy C, Mehlen P, Mirault ME, Arrigo AP. Inhibition of I kappa B-alpha phosphorylation and degradation and subsequent NF-kappa B activation by glutathione peroxidase overexpression. J Cell Biol. 1996; 133: 1083-1093
52. Wen H, Gris D, Lei Y, et al. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011; 12: 408-415
53. Kim KM, Pae HO, Zheng M, et al. Carbon monoxide induces heme oxygenase-1 via activation of protein kinase R-like endoplasmic reticulum kinase and inhibits endothelial cell apoptosis triggered by endoplasmic reticulum stress. Circ Res. 2007; 101: 919-927
54. Li G, Mongillo M, Chin KT, et al. Role of ERO1-alpha-mediated stimulation of inositol 1,4,5-triphosphate receptor activity in endoplasmic reticulum stress-induced apoptosis. J Cell Biol. 2009; 186: 783-792
55. Chami M, Oules B, Szabadkai G, et al. Role of SERCA1 truncated isoform in the proapoptotic calcium transfer from ER to mitochondria during ER stress. Mol Cell. 2008; 32: 641-651
56. Deniaud A, Sharaf el dein O, Maillier E, et al. Endoplasmic reticulum stress induces calcium-dependent permeability transition, mitochondrial outer membrane permeabilization and apoptosis. Oncogene. 2008; 27: 285-299
57. Hovind P, Rossing P, Tarnow L, et al. Serum uric acid as a predictor for development of diabetic nephropathy in type 1 diabetes: an inception cohort study. Diabetes. 2009; 58: 1668-1671
58. Vilaysane A, Chun J, Seamone ME, et al. The NLRP3 inflammasome promotes renal inflammation and contributes to CKD. J Am Soc Nephrol. 2010; 21: 1732-1744