Fasting and refeeding differentially regulate NLRP3 inflammasome activation in human subjects

Journal of Clinical Investigation

Volumn 125, Issue 12, 2015, Pages 4592-4600

  Traba, Javier ^a   Kwarteng Siaw, Miriam ^a   Okoli, Tracy C ^a   Li, Jessica ^a   Huffstutler, Rebecca D ^a   Bray, Amanda ^a   Waclawiw, Myron A ^a   Han, Kim ^a   Pelletier, Martin ^b   Sauve, Anthony A ^c   Siegel, Richard M ^b   Sack, Michael N ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL INSTITUTE OF ARTHRITIS AND MUSCULOSKELETAL AND SKIN DISEASES   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRYOPYRIN; INFLAMMASOME; NICOTINAMIDE RIBOSIDE; REACTIVE OXYGEN METABOLITE; SIRTUIN 3; CARRIER PROTEIN; NICOTINAMIDE; NICOTINAMIDE-BETA-RIBOSIDE; NLRP3 PROTEIN, HUMAN;

ADULT; ARTICLE; CALORIC INTAKE; CELL FUNCTION; DIET RESTRICTION; ENZYME INHIBITION; FEMALE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; LEUKOCYTE; MACROPHAGE; MALE; MITOCHONDRION; NORMAL HUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; REFEEDING; REGULATORY MECHANISM; ANALOGS AND DERIVATIVES; BLOOD; CLINICAL TRIAL; EATING; METABOLISM;

ADULT; CARRIER PROTEINS; EATING; FASTING; FEMALE; HUMANS; INFLAMMASOMES; MALE; MITOCHONDRIA; NIACINAMIDE; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN;

EID: 84948807305     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI83260     Document Type: Article

References (47)

1. Vandanmagsar B, et al. The NLRP3 inflam-masome instigates obesity-induced inflammation and insulin resistance. Nat Med. 2011;17(2):179-188.
2. Lee HM, Kim JJ, Kim HJ, Shong M, Ku BJ, Jo EK. Upregulated NLRP3 inflammasome activation in patients with type 2 diabetes. Diabetes. 2013;62(1):194-204.
3. Kim HY, et al. Interleukin-17-producing innate lymphoid cells and the NLRP3 inflammasome facilitate obesity-associated airway hyperreactiv-ity. Nat Med. 2014;20(1):54-61.
4. Sutterwala FS, Haasken S, Cassel SL. Mechanism of NLRP3 inflammasome activation. Ann N Y Acad Sci. 2014;1319:82-95.
5. Osborn O, Olefsky JM. The cellular and signaling networks linking the immune system and metabolism in disease. Nat Med. 2012;18(3):363-374.
6. Kheirandish-Gozal L, et al. Lipopolysaccha-ride-binding protein plasma levels in children: effects of obstructive sleep apnea and obesity. J Clin Endocrinol Metab. 2014;99(2):656-663.
7. Goossens GH, et al. Expression of NLRP3 inflam-masome and T cell population markers in adipose tissue are associated with insulin resistance and impaired glucose metabolism in humans. Mol Immunol. 2012;50(3):142-149.
8. Stienstra R, et al. Inflammasome is a central player in the induction of obesity and insulin resistance. Proc Natl Acad Sci USA. 2011;108(37):15324-15329.
9. Henao-Mejia J, Elinav E, Strowig T, Flavell RA. Inflammasomes: far beyond inflammation. Nat Immunol. 2012;13(4):321-324.
10. Strowig T, Henao-Mejia J, Elinav E, Flavell R. Inflammasomes in health and disease. Nature. 2012;481(7381):278-286.
11. Lumeng CN, Saltiel AR. Inflammatory links between obesity and metabolic disease. J Clin Invest. 2011;121(6):2111-2117.
12. Pagel-Langenickel I, Bao J, Pang L, Sack MN. The role of mitochondria in the pathophysiology of skeletal muscle insulin resistance. Endocr Rev. 2010;31(1):25-51.
13. Zhou R, Yazdi AS, Menu P, Tschopp J. A role for mitochondria in NLRP3 inflammasome activation. Nature. 2011;469(7329):221-225.
14. Shimada K, et al. Oxidized mitochondrial DNA activates the NLRP3 inflammasome during apoptosis. Immunity. 2012;36(3):401-414.
15. Zhang Q, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 2010;464(7285):104-107.
16. Nakahira K, et al. Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol. 2011;12(3):222-230.
17. Iyer SS, et al. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity. 2013;39(2):311-323.
18. West AP, Koblansky AA, Ghosh S. Recognition and signaling by toll-like receptors. Annu Rev Cell Dev Biol. 2006;22:409-437.
19. Longo VD, Mattson MP. Fasting: molecular mechanisms and clinical applications. Cell Metab. 2014;19(2):181-192.
20. Johnson JB, et al. Alternate day calorie restriction improves clinical findings and reduces markers of oxidative stress and inflammation in overweight adults with moderate asthma. Free Radic Biol Med. 2007;42(5):665-674.
21. Fontana L, Meyer TE, Klein S, Holloszy JO. Long-term calorie restriction is highly effective in reducing the risk for atherosclerosis in humans. Proc Natl Acad Sci USA. 2004; 101(17): 6659-6663.
22. Lu Z, et al. SIRT3-dependent deacetylation exacerbates acetaminophen hepatotoxicity. EMBO Rep. 2011;12(8):840-846.
23. Hirschey MD, et al. SIRT3 regulates mitochon-drial fatty-acid oxidation by reversible enzyme deacetylation. Nature. 2010;464(7285):121-125.
24. Bao J, et al. SIRT3 is regulated by nutrient excess and modulates hepatic susceptibility to lipotoxic-ity. Free Radic Biol Med. 2010;49(7):1230-1237.
25. Kendrick AA, et al. Fatty liver is associated with reduced SIRT3 activity and mitochon-drial protein hyperacetylation. Biochem J. 2011;433(3):505-514.
26. Sack MN, Finkel T. Mitochondrial metabolism, sirtuins, and aging. Cold Spring Harb Perspect Biol. 2012;4(12):a013102.
27. Webster BR, Scott I, Traba J, Han K, Sack MN. Regulation of autophagy and mitophagy by nutrient availability and acetylation. Biochim Biophys Acta. 2014;1841(4):525-534.
28. Youm YH, et al. The ketone metabolite β-hydroxybutyrate blocks NLRP3 inflam-masome-mediated inflammatory disease. Nat Med. 2015;21(3):263-269.
29. Sandler NG, et al. Plasma levels of soluble CD14 independently predict mortality in HIV infection. J Infec t Dis. 2011;203(6):780-790.
30. Vodanovic-Jankovic S, Hari P, Jacobs P, Komo-rowski R, Drobyski WR. NF-κB as a target for the prevention of graft-versus-host disease: comparative efficacy of bortezomib and PS-1145. Blood. 2006;107(2):827-834.
31. Webster BR, Lu Z, Sack MN, Scott I. The role of sirtuins in modulating redox stressors. Free Radic Biol Med. 2012;52(2):281-290.
32. Ozden O, et al. Acetylation of MnSOD directs enzymatic activity responding to cellular nutrient status or oxidative stress. Aging (Albany NY). 2011;3(2):102-107.
33. Bulua AC, et al. Mitochondrial reactive oxygen species promote production of proinflammatory cytokines and are elevated in TNFR1-associ-ated periodic syndrome (TRAPS). J Exp Med. 2011;208(3):519-533.
34. Brown KD, et al. Activation of SIRT3 by the NAD(+) precursor nicotinamide riboside protects from noise-induced hearing loss. Cell Metab. 2014;20(6):1059-1068.
35. Fontana L, Partridge L. Promoting health and longevity through diet: from model organisms to humans. Cell. 2015;161(1):106-118.
36. Brandhorst S, et al. A periodic diet that mimics fasting promotes multi-system regeneration, enhanced cognitive performance, and healthspan. Cell Metab. 2015;22(1):86-99.
37. Amar J, et al. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr. 2008;87(5):1219-1223.
38. van der Burgh R, et al. Defects in mitochon-drial clearance predispose human monocytes to interleukin-1β hypersecretion. J Biol Chem. 2014;289(8):5000-5012.
39. Zhou Z, et al. TRIM14 is a mitochondrial adaptor that facilitates retinoic acid-inducible gene-I-like receptor-mediated innate immune response. Proc Natl Acad Sci USA. 2014;111(2):E245-E254.
40. West AP, et al. Mitochondrial DNA stress primes the antiviral innate immune response. Nature. 2015;520(7548):553-557.
41. Weinberg SE, Sena LA, Chandel NS. Mitochondria in the regulation of innate and adaptive immunity. Immunity. 2015;42(3):406-417.
42. Steinberg GR, Schertzer JD. AMPK promotes macrophage fatty acid oxidative metabolism to mitigate inflammation: implications for diabetes and cardiovascular disease. Immunol Cell Biol. 2014;92(4):340-345.
43. Park EK, Jung HS, Yang HI, Yoo MC, Kim C, Kim KS. Optimized THP-1 differentiation is required for the detection of responses to weak stimuli. Inflamm Res. 2007;56(1):45-50.
44. Schnoor M, et al. Efficient non-viral trans-fection of THP-1 cells. J Immunol Methods. 2009;344(2):109-115.
45. Qu Y, et al. Pannexin-1 is required for ATP release during apoptosis but not for inflammasome activation. J Immunol. 2011;186(11):6553-6561.
46. Avila C, et al. Platelet mitochondrial dysfunction is evident in type 2 diabetes in association with modifications of mitochondrial anti-oxidant stress proteins. Exp Clin Endocrinol Diabetes. 2012;120(4):248-251.
47. Scott I, Webster BR, Chan CK, Okonkwo JU, Han K, Sack MN. GCN5-like protein 1 (GCN5L1) controls mitochondrial content through coordinated regulation of mitochondrial biogenesis and mitophagy. J Biol Chem. 2014;289(5):2864-2872.