Insufficient autophagy contributes to mitochondrial dysfunction, organ failure, and adverse outcome in an animal model of critical illness

Critical Care Medicine

Volumn 41, Issue 1, 2013, Pages 182-194

  Gunst, Jan ^a   Derese, Inge ^a   Aertgeerts, Annelies ^a   Ververs, Eric Jan ^a   Wauters, Andy ^a   Van Den Berghe, Greet ^a   Vanhorebeek, Ilse ^a  

^a LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

Author keywords

autophagy; critical illness; hyperglycemia; insulin; mitochondria; multiple organ failure

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; PROTEIN P62; RAPAMYCIN;

ADVERSE OUTCOME; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; BIOGENESIS; CELL FUSION; CONTROLLED STUDY; CRITICAL ILLNESS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EXPERIMENTAL RABBIT; GLYCEMIC CONTROL; HYPERGLYCEMIA; KIDNEY; KIDNEY FUNCTION; LIGHT CHAIN; LIVER; LIVER MITOCHONDRION; MALE; METABOLISM; MITOCHONDRION; MORTALITY; MULTIPLE ORGAN FAILURE; NONHUMAN; NUTRITION; PHENOTYPE; PRIORITY JOURNAL; RENAL PROTECTION; SURVIVAL;

ANIMALS; AUTOPHAGY; BIOLOGICAL MARKERS; CRITICAL ILLNESS; HYPERGLYCEMIA; IMMUNOSUPPRESSIVE AGENTS; KIDNEY; MALE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA, LIVER; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DISEASES; MITOCHONDRIAL DYNAMICS; MULTIPLE ORGAN FAILURE; PROSPECTIVE STUDIES; RABBITS; RANDOM ALLOCATION; SIROLIMUS; SURVIVAL ANALYSIS;

EID: 84872066457     PISSN: 00903493     EISSN: 15300293     Source Type: Journal    
DOI: 10.1097/CCM.0b013e3182676657     Document Type: Article

References (48)

1. Fink MP, Evans TW: Mechanisms of organ dysfunction in critical illness: Report from a Round Table Conference held in Brussels. Intensive Care Med 2002; 28:369-375
2. Abraham E, Singer M: Mechanisms of sepsis-induced organ dysfunction. Crit Care Med 2007; 35:2408-2416
3. Brealey D, Brand M, Hargreaves I, et al: Association between mitochondrial dysfunction and severity and outcome of septic shock. Lancet 2002; 360:219-223
4. Brealey D, Karyampudi S, Jacques TS, et al: Mitochondrial dysfunction in a long-term rodent model of sepsis and organ failure. Am J Physiol Regul Integr Comp Physiol 2004; 286:R491-R497
5. Vanhorebeek I, De Vos R, Mesotten D, et al: Protection of hepatocyte mitochondrial ultrastructure and function by strict blood glucose control with insulin in critically ill patients. Lancet 2005; 365:53-59
6. Vanhorebeek I, Ellger B, De Vos R, et al: Tissue-specific glucose toxicity induces mitochondrial damage in a burn injury model of critical illness. Crit Care Med 2009; 37:1355-1364
7. Vanhorebeek I, Gunst J, Ellger B, et al: Hyperglycemic kidney damage in an animal model of prolonged critical illness. Kidney Int 2009; 76: 512-520
8. Van den Berghe G, Wouters P, Weekers F, et al: Intensive insulin therapy in critically ill patients. N Engl J Med 2001; 345:1359-1367
9. Finfer S, Chittock DR, Su SY, et al; NICE-SUGAR Study Investigators: Intensive versus conventional glucose control in critically ill patients. N Engl J Med 2009; 360:1283-1297
10. Van den Berghe G, Schetz M, Vlasselaers D, et al: Clinical review: Intensive insulin therapy in critically ill patients: NICE-SUGAR or Leuven blood glucose target? J Clin Endocrinol Metab 2009; 94:3163-3170
11. Dare AJ, Phillips AR, Hickey AJ, et al: A systematic review of experimental treatments for mitochondrial dysfunction in sepsis and multiple organ dysfunction syndrome. Free Radic Biol Med 2009; 47:1517-1525
12. Terman A, Kurz T, Navratil M, et al: Mitochondrial turnover and aging of long-lived postmitotic cells: The mitochondrial-lysosomal axis theory of aging. Antioxid Redox Signal 2010; 12:503-535
13. Vanhorebeek I, Gunst J, Derde S, et al: Insufficient activation of autophagy allows cellular damage to accumulate in critically ill patients. J Clin Endocrinol Metab 2011; 96:E633-E645
14. Vanhorebeek I, Gunst J, Derde S, et al: Mitochondrial fusion, fission, and biogenesis in prolonged critically ill patients. J Clin Endocrinol Metab 2012; 97:E59-E64
15. He C, Klionsky DJ: Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 2009; 43:67-93
16. Kaniuk NA, Kiraly M, Bates H, et al: Ubiquitinated-protein aggregates form in pancreatic beta-cells during diabetes-induced oxidative stress and are regulated by autophagy. Diabetes 2007; 56:930-939
17. Sreekumar R, Halvatsiotis P, Schimke JC, et al: Gene expression profile in skeletal muscle of type 2 diabetes and the effect of insulin treatment. Diabetes 2002; 51:1913-1920
18. Yoon Y, Galloway CA, Jhun BS, et al: Mitochondrial dynamics in diabetes. Antioxid Redox Signal 2011; 14:439-457
19. Weekers F, Van Herck E, Coopmans W, et al: A novel in vivo rabbit model of hypercatabolic critical illness reveals a biphasic neuroendocrine stress response. Endocrinology 2002; 143:764-774
20. Weekers F, Giulietti AP, Michalaki M, et al: Metabolic, endocrine, and immune effects of stress hyperglycemia in a rabbit model of prolonged critical illness. Endocrinology 2003; 144:5329-5338
21. Langouche L, Vander Perre S, Wouters PJ, et al: Effect of intensive insulin therapy on insulin sensitivity in the critically ill. J Clin Endocrinol Metab 2007; 92:3890-3897
22. Ellger B, Debaveye Y, Vanhorebeek I, et al: Survival benefits of intensive insulin therapy in critical illness: Impact of maintaining normoglycemia versus glycemia-independent actions of insulin. Diabetes 2006; 55:1096-1105
23. Langouche L, Vanhorebeek I, Vlasselaers D, et al: Intensive insulin therapy protects the endothelium of critically ill patients. J Clin Invest 2005; 115:2277-2286
24. Derde S, Vanhorebeek I, Ververs EJ, et al: Increasing intravenous glucose load in the presence of normoglycemia: Effect on outcome and metabolism in critically ill rabbits. Crit Care Med 2010; 38:602-611
25. Nakai A, Yamaguchi O, Takeda T, et al: The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med 2007; 13:619-624
26. Masiero E, Agatea L, Mammucari C, et al: Autophagy is required to maintain muscle mass. Cell Metab 2009; 10:507-515
27. Scarpulla RC: Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 2008; 88:611-638
28. Detmer SA, Chan DC: Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol 2007; 8:870-879
29. Levine B, Kroemer G: Autophagy in the pathogenesis of disease. Cell 2008; 132:27-42
30. Komatsu M, Waguri S, Ueno T, et al: Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol 2005; 169: 425-434
31. Watanabe E, Muenzer JT, Hawkins WG, et al: Sepsis induces extensive autophagic vacuolization in hepatocytes: A clinical and laboratory-based study. Lab Invest 2009; 89:549-561
32. Watts JA, Kline JA, Thornton LR, et al: Metabolic dysfunction and depletion of mitochondria in hearts of septic rats. J Mol Cell Cardiol 2004; 36: 141-150
33. Ceylan-Isik AF, Zhao P, Zhang B, et al: Cardiac overexpression of metallothionein rescues cardiac contractile dysfunction and endoplasmic reticulum stress but not autophagy in sepsis. J Mol Cell Cardiol 2010; 48:367-378
34. Hussain SN, Mofarrahi M, Sigala I, et al: Mechanical ventilation-induced diaphragm disuse in humans triggers autophagy. Am J Respir Crit Care Med 2010; 182:1377-1386
35. Klionsky DJ, Abeliovich H, Agostinis P, et al: Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008; 4:151-175
36. Hsieh CH, Pai PY, Hsueh HW, et al: Complete induction of autophagy is essential for cardioprotection in sepsis. Ann Surg 2011; 253: 1190-1200
37. Carchman EH, Rao J, Loughran PA, et al: Heme oxygenase-1-mediated autophagy protects against hepatocyte cell death and hepatic injury from infection/sepsis in mice. Hepatology 2011; 53:2053-2062
38. Kroemer G, Mariño G, Levine B: Autophagy and the integrated stress response. Mol Cell 2010; 40:280-293
39. Casaer MP, Mesotten D, Hermans G, et al: Early versus late parenteral nutrition in critically ill adults. N Engl J Med 2011; 365:506-517
40. Morselli E, Mariño G, Bennetzen MV, et al: Spermidine and resveratrol induce autophagy by distinct pathways converging on the acetylproteome. J Cell Biol 2011; 192:615-629
41. Alamdari N, Smith IJ, Aversa Z, et al: Sepsis and glucocorticoids upregulate p300 and downregulate HDAC6 expression and activity in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 2010; 299:R509-R520
42. Rabinowitz JD, White E: Autophagy and metabolism. Science 2010; 330:1344-1348
43. Han K, Lehringer-Polzin M, Zhou H, et al: Cellular autophagy in proximal tubules of early diabetic rats following insulin treatment and islet transplantation. Virchows Arch, B, Cell Pathol 1992; 61:367-373
44. Carré JE, Orban JC, Re L, et al: Survival in critical illness is associated with early activation of mitochondrial biogenesis. Am J Respir Crit Care Med 2010; 182:745-751
45. Fredriksson K, Tjäder I, Keller P, et al: Dysregulation of mitochondrial dynamics and the muscle transcriptome in ICU patients suffering from sepsis induced multiple organ failure. PLoS One 2008; 3:e3686
46. Crouser ED, Julian MW, Huff JE, et al: Carbamoyl phosphate synthase-1: A marker of mitochondrial damage and depletion in the liver during sepsis. Crit Care Med 2006; 34:2439-2446
47. Haden DW, Suliman HB, Carraway MS, et al: Mitochondrial biogenesis restores oxidative metabolism during Staphylococcus aureus sepsis. Am J Respir Crit Care Med 2007; 176:768-777
48. Vincent JL, Nelson DR, Williams MD: Is worsening multiple organ failure the cause of death in patients with severe sepsis? Crit Care Med 2011; 39:1050-1055