Fasting protects liver from ischemic injury through Sirt1-mediated downregulation of circulating HMGB1 in mice

Journal of Hepatology

Volumn 61, Issue 2, 2014, Pages 301-308

  Rickenbacher, Andreas ^a   Jang, Jae Hwi ^a   Limani, Perparim ^a   Ungethüm, Udo ^a   Lehmann, Kuno ^a   Oberkofler, Christian E ^a   Weber, Achim ^a   Graf, Rolf ^a   Humar, Bostjan ^a   Clavien, Pierre Alain ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Anti inflammatory; Autophagy; Fasting; HMGB1; Innate immunity; Kupffer cell; Liver ischemia; Sirtuin

Indexed keywords

HIGH MOBILITY GROUP B1 PROTEIN; LIVER ENZYME; NEUTRALIZING ANTIBODY; SIRTUIN 1; SIRT1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; AUTOPHAGY; C57BL 6 MOUSE; CALORIC RESTRICTION; CONTROLLED STUDY; CORRELATION ANALYSIS; DIET RESTRICTION; DOWN REGULATION; ENERGY CONSERVATION; ENERGY METABOLISM; HISTOLOGY; LIVER INJURY; LIVER ISCHEMIA; LIVER PROTECTION; MACROPHAGE; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REPERFUSION INJURY; SUPERNATANT; ANIMAL; BLOOD; C57BL MOUSE; INFLAMMATION; LIVER; MOUSE; PHYSIOLOGY; VASCULARIZATION;

ANIMALS; DOWN-REGULATION; FASTING; HMGB1 PROTEIN; INFLAMMATION; LIVER; MALE; MICE; MICE, INBRED C57BL; REPERFUSION INJURY; SIRTUIN 1;

EID: 84904607895     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2014.04.010     Document Type: Article

References (52)

1. S. Imai, C.M. Armstrong, M. Kaeberlein, and L. Guarente Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase Nature 403 2000 795 800
2. H.A. Tissenbaum, and L. Guarente Increased dosage of a sir-2 gene extends lifespan in Caenorhabditis elegans Nature 410 2001 227 230
3. R.J. Colman, R.M. Anderson, S.C. Johnson, E.K. Kastman, K.J. Kosmatka, and T.M. Beasley et al. Caloric restriction delays disease onset and mortality in rhesus monkeys Science 325 2009 201 204
4. S. Libert, and L. Guarente Metabolic and neuropsychiatric effects of calorie restriction and sirtuins Annu Rev Physiol 75 2013 669 684
5. C. Lee, and V.D. Longo Fasting vs. dietary restriction in cellular protection and cancer treatment: from model organisms to patients Oncogene 30 2011 3305 3316
6. C. Canto, and J. Auwerx Caloric restriction, SIRT1 and longevity Trends Endocrinol Metab 20 2009 325 331
7. Y. Zhai, R.W. Busuttil, and J.W. Kupiec-Weglinski Liver ischemia and reperfusion injury: new insights into mechanisms of innate-adaptive immune-mediated tissue inflammation Am J Transplant 11 2011 1563 1569
8. B. Mosher, R. Dean, J. Harkema, D. Remick, J. Palma, and E. Crockett Inhibition of Kupffer cells reduced CXC chemokine production and liver injury J Surg Res 99 2001 201 210
9. L. Ulloa, and D. Messmer High-mobility group box 1 (HMGB1) protein: friend and foe Cytokine Growth Factor Rev 17 2006 189 201
10. A. Tsung, R. Sahai, H. Tanaka, A. Nakao, M.P. Fink, and M.T. Lotze et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion J Exp Med 201 2005 1135 1143
11. N. Selzner, M. Selzner, W. Jochum, and P.A. Clavien Ischemic preconditioning protects the steatotic mouse liver against reperfusion injury: an ATP dependent mechanism J Hepatol 39 2003 55 61
12. M. Selzner, N. Selzner, W. Jochum, R. Graf, and P.A. Clavien Increased ischemic injury in old mouse liver: an ATP-dependent mechanism Liver Transpl 13 2007 382 390
13. J.H. Wang, I.S. Ahn, T.D. Fischer, J.I. Byeon, W.A. Dunn Jr., and K.E. Behrns et al. Autophagy suppresses age-dependent ischemia and reperfusion injury in livers of mice Gastroenterology 141 2011 2188 2199
14. Z.F. Yu, and M.P. Mattson Dietary restriction and 2-deoxyglucose administration reduce focal ischemic brain damage and improve behavioral outcome: evidence for a preconditioning mechanism J Neurosci Res 57 1999 830 839
15. B. Chandrasekar, J.F. Nelson, J.T. Colston, and G.L. Freeman Calorie restriction attenuates inflammatory responses to myocardial ischemia-reperfusion injury Am J Physiol Heart Circ Physiol 280 2001 H2094 H2102
16. S.I. Kawai, S. Vora, S. Das, E. Gachie, B. Becker, and A.H. Neufeld Modeling of risk factors for the degeneration of retinal ganglion cells after ischemia/reperfusion in rats: effects of age, caloric restriction, diabetes, pigmentation, and glaucoma FASEB J 15 2001 1285 1287
17. I. Ahmet, R. Wan, M.P. Mattson, E.G. Lakatta, and M. Talan Cardioprotection by intermittent fasting in rats Circulation 112 2005 3115 3121
18. J.R. Mitchell, M. Verweij, K. Brand, M. van de Ven, N. Goemaere, and S. van den Engel et al. Short-term dietary restriction and fasting precondition against ischemia reperfusion injury in mice Aging Cell 9 2010 40 53
19. J.H. Jang, W. Moritz, R. Graf, and P.A. Clavien Preconditioning with death ligands FasL and TNF-alpha protects the cirrhotic mouse liver against ischaemic injury Gut 57 2008 492 499
20. M. Sokolovic, A. Sokolovic, D. Wehkamp, E.V. van Themaat, D.R. de Waart, and L.A. Gilhuijs-Pederson et al. The transcriptomic signature of fasting murine liver BMC Genomics 9 2008 528
21. M. Tschop, D.L. Smiley, and M.L. Heiman Ghrelin induces adiposity in rodents Nature 407 2000 908 913
22. R. Takeda, H. Nishimatsu, E. Suzuki, H. Satonaka, D. Nagata, and S. Oba et al. Ghrelin improves renal function in mice with ischemic acute renal failure J Am Soc Nephrol 17 2006 113 121
23. M. Abu-Amara, S.Y. Yang, N. Tapuria, B. Fuller, B. Davidson, and A. Seifalian Liver ischemia/reperfusion injury: processes in inflammatory networks - a review Liver Transpl 16 2010 1016 1032
24. S. Suzuki, L.H. Toledo-Pereyra, F. Rodriguez, and F. Lopez Role of Kupffer cells in neutrophil activation and infiltration following total hepatic ischemia and reperfusion Circ Shock 42 1994 204 209
25. H. Yang, and K.J. Tracey Targeting HMGB1 in inflammation Biochim Biophys Acta 1799 2010 149 156
26. A. Castiglioni, V. Canti, P. Rovere-Querini, and A.A. Manfredi High-mobility group box 1 (HMGB1) as a master regulator of innate immunity Cell Tissue Res 343 2011 189 199
27. D. Tang, R. Kang, K.M. Livesey, C.W. Cheh, A. Farkas, and P. Loughran et al. Endogenous HMGB1 regulates autophagy J Cell Biol 190 2010 881 892
28. S. Zhu, W. Li, J. Li, A. Jundoria, A.E. Sama, and H. Wang It is not just folklore: the aqueous extract of mung bean coat is protective against sepsis Evid Based Complement Altern Med 2012 2012 498467
29. I.H. Lee, L. Cao, R. Mostoslavsky, D.B. Lombard, J. Liu, and N.E. Bruns et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy Proc Natl Acad Sci U S A 105 2008 3374 3379
30. B. Peck, C.Y. Chen, K.K. Ho, P. Di Fruscia, S.S. Myatt, and R.C. Coombes et al. SIRT inhibitors induce cell death and p53 acetylation through targeting both SIRT1 and SIRT2 Mol Cancer Ther 9 2010 844 855
31. H.N. Sankary, A. Chong, P. Foster, E. Brown, J. Shen, and R. Kimura et al. Inactivation of Kupffer cells after prolonged donor fasting improves viability of transplanted hepatic allografts Hepatology 22 1995 1236 1242
32. B.W. Ritz, I. Aktan, S. Nogusa, and E.M. Gardner Energy restriction impairs natural killer cell function and increases the severity of influenza infection in young adult male C57BL/6 mice J Nutr 138 2008 2269 2275
33. J. Shen, H. Ren, C. Tomiyama-Miyaji, M. Watanabe, E. Kainuma, and M. Inoue et al. Resistance and augmentation of innate immunity in mice exposed to starvation Cell Immunol 259 2009 66 73
34. R.F. van Golen, T.M. van Gulik, and M. Heger The sterile immune response during hepatic ischemia/reperfusion Cytokine Growth Factor Rev 23 2012 69 84
35. M. Yu, H. Wang, A. Ding, D.T. Golenbock, E. Latz, and C.J. Czura et al. HMGB1 signals through toll-like receptor (TLR) 4 and TLR2 Shock 26 2006 174 179
36. M. Frink, Y.C. Hsieh, B.M. Thobe, M.A. Choudhry, M.G. Schwacha, and K.I. Bland et al. TLR4 regulates Kupffer cell chemokine production, systemic inflammation and lung neutrophil infiltration following trauma-hemorrhage Mol Immunol 44 2007 2625 2630
37. D. Cantino, R. Mosso, and F.M. Baccino Changes induced by fasting and cycloheximide in the vacuolar apparatus of rat hepatocytes. A morphometric investigation Boll Soc Ital Biol Sper 55 1979 1884 1889
38. N. Mizushima, and T. Yoshimori How to interpret LC3 immunoblotting Autophagy 3 2007 542 545
39. S.R. Powell, and A. Divald The ubiquitin-proteasome system in myocardial ischaemia and preconditioning Cardiovasc Res 85 2010 303 311
40. P. Huebener, G.Y. Gwak, J.P. Pradere, C.M. Quinzii, R. Friedman, and C.S. Lin et al. High-mobility group box 1 is dispensable for autophagy, mitochondrial quality control, and organ function in vivo Cell Metab 19 2014 539 547
41. G.W. Nace, H. Huang, J.R. Klune, R.E. Eid, B.R. Rosborough, and S. Korff et al. Cellular-specific role of toll-like receptor 4 in hepatic ischemia-reperfusion injury in mice Hepatology 58 2013 374 387
42. P.E. Rautou, D. Cazals-Hatem, R. Moreau, C. Francoz, G. Feldmann, and D. Lebrec et al. Acute liver cell damage in patients with anorexia nervosa: a possible role of starvation-induced hepatocyte autophagy Gastroenterology 135 2008 840 848
43. X. Zhao, D. Allison, B. Condon, F. Zhang, T. Gheyi, and A. Zhang et al. The 2.5 A crystal structure of the SIRT1 catalytic domain bound to nicotinamide adenine dinucleotide (NAD+) and an indole (EX527 analogue) reveals a novel mechanism of histone deacetylase inhibition J Med Chem 56 2013 963 969
44. S. Timmers, E. Konings, L. Bilet, R.H. Houtkooper, T. van de Weijer, and G.H. Goossens et al. Calorie restriction-like effects of 30 days of resveratrol supplementation on energy metabolism and metabolic profile in obese humans Cell Metab 14 2011 612 622
45. T. Bonaldi, F. Talamo, P. Scaffidi, D. Ferrera, A. Porto, and A. Bachi et al. Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion EMBO J 22 2003 5551 5560
46. J.T. Lee, and W. Gu SIRT1: regulator of p53 deacetylation Genes Cancer 4 2013 112 117
47. K.M. Livesey, R. Kang, P. Vernon, W. Buchser, P. Loughran, and S.C. Watkins et al. P53/HMGB1 complexes regulate autophagy and apoptosis Cancer Res 72 2012 1996 2005
48. S.M. Nadtochiy, E. Redman, I. Rahman, and P.S. Brookes Lysine deacetylation in ischaemic preconditioning: the role of SIRT1 Cardiovasc Res 89 2011 643 649
49. C.P. Hsu, P. Zhai, T. Yamamoto, Y. Maejima, S. Matsushima, and N. Hariharan et al. Silent information regulator 1 protects the heart from ischemia/reperfusion Circulation 122 2010 2170 2182
50. H. Fan, H.C. Yang, L. You, Y.Y. Wang, W.J. He, and C.M. Hao The histone deacetylase, SIRT1, contributes to the resistance of young mice to ischemia/reperfusion-induced acute kidney injury Kidney Int 83 2013 404 413
51. S.M. Nadtochiy, H. Yao, M.W. McBurney, W. Gu, L. Guarente, and I. Rahman et al. SIRT1-mediated acute cardioprotection Am J Physiol Heart Circ Physiol 301 2011 H1506 H1512
52. J. Cardinal, P. Pan, R. Dhupar, M. Ross, A. Nakao, and M. Lotze et al. Cisplatin prevents high mobility group box 1 release and is protective in a murine model of hepatic ischemia/reperfusion injury Hepatology 50 2009 565 574