IL-6 deficiency attenuates murine diet-induced non-alcoholic steatohepatitis

PLoS ONE

Volumn 4, Issue 11, 2009, Pages

  Mas, Emmanuel ^a,b,c   Danjoux, Marie ^d   Garcia, Virginie ^a,b   Carpentier, Stéphane ^a,b   Ségul, Bruno ^a,b   Levade, Thierry ^a,b,d  

^a INSERM   (France)

^b UNIVERSITÉ DE TOULOUSE   (France)

^c HÔPITAL DES ENFANTS   (France)

^d CHU PURPAN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; CERAMIDE; INTERLEUKIN 6; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; SPHINGOMYELIN; TRANSFORMING GROWTH FACTOR BETA; CHOLINE; METHIONINE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CHROMATOGRAPHY; CONTROLLED STUDY; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENOTYPE; LIPID METABOLISM; LIPID PEROXIDATION; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; ANIMAL; ANIMAL FOOD; C57BL MOUSE; DISEASE MODEL; FATTY LIVER; GENETICS; INFLAMMATION; LIVER; METABOLISM; TRANSGENIC MOUSE;

ANIMALIA; MURINAE; MUS;

ANIMAL FEED; ANIMALS; APOPTOSIS; CHOLINE; DISEASE MODELS, ANIMAL; FATTY LIVER; INFLAMMATION; INTERLEUKIN-6; LIPID PEROXIDATION; LIVER; MALE; METHIONINE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PPAR GAMMA;

EID: 70949094933     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0007929     Document Type: Article

References (60)

1. Ludwig J, Viggiano TR, McGill DB, Oh BJ (1980) Nonalcoholic steatohepatitis: Mayo Clinic experiences with a hitherto unnamed disease. Mayo Clin Proc 55: 434-438.
2. Haque M, Sanyal AJ (2002) The metabolic abnormalities associated with non-alcoholic fatty liver disease. Best Pract Res Clin Gastroenterol 16: 709-731.
3. Day CP, James OF (1998) Steatohepatitis: a tale of two "hits"? Gastroenterology 114: 842-845.
4. Larter CZ, Farrell GC (2006) Insulin resistance, adiponectin, cytokines in NASH: Which is the best target to treat? J Hepatol 44: 253-261.
5. Hotamisligil GS (1999) The role of TNFalpha and TNF receptors in obesity and insulin resistance. J Intern Med 245: 621-625.
6. Yin M, Wheeler MD, Kono H, Bradford BU, Gallucci RM, et al. (1999) Essential role of tumor necrosis factor alpha in alcohol-induced liver injury in mice. Gastroenterology 117: 942-952.
7. Crespo J, Cayon A, Fernandez-Gil P, Hernandez-Guerra M, Mayorga M, et al. (2001) Gene expression of tumor necrosis factor alpha and TNF-receptors, p55 and p75, in nonalcoholic steatohepatitis patients. Hepatology 34: 1158-1163.
8. Bahcecioglu IH, Yalniz M, Ataseven H, Ilhan N, Ozercan IH, et al. (2005) Levels of serum hyaluronic acid, TNF-alpha and IL-8 in patients with nonalcoholic steatohepatitis. Hepatogastroenterology 52: 1549-53.
9. Memon RA, Grunfeld C, Feingold KR (2001) TNF-alpha is not the cause of fatty liver disease in obese diabetic mice. Nat Med 7: 2-3.
10. Deng QG, She H, Cheng JH, French SW, Koop DR, et al. (2005) Steatohepatitis induced by intragastric overfeeding in mice. Hepatology 42: 905-914.
11. Feldstein AE, Werneburg NW, Canbay A, Guicciardi ME, Bronk SF, et al. (2004) Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathway. Hepatology 40: 185-194.
12. Tomita K, Tamiya G, Ando S, Oshumi K, Chiyo T, et al. (2006) Tumour necrosis factor alpha signalling through activation of Kupffer cells plays an essential role in liver fibrosis of non-alcoholic steatohepatitis in mice. Gut 55: 415-424.
13. McCuskey RS, Ito Y, Robertson GR, McCuskey MK, Perry M, et al. (2004) Hepatic microvascular dysfunction during evolution of dietary steatohepatitis in mice. Hepatology 40: 386-93.
14. Rinella ME, Green RM (2004) The methionine-choline deficient dietary model of steatohepatitis does not exhibit insulin resistance. J Hepatol 40: 47-51.
15. Diehl AM (2005) Lessons from animal models of NASH. Hepatol Res 33: 138-144.
16. Yao ZM, Vance DE (1988) The active synthesis of phosphatidylcholine is required for very low density lipoprotein secretion from rat hepatocytes. J Biol Chem 263: 2998-3004.
17. Rinella ME, Elias MS, Smolak RR, Fu T, Borensztajn J, et al. (2008) Mechanisms of steatohepatitis in mice fed a lipogenic methionine choline deficient (MCD) diet. J Lipid Res 49: 1068-1076.
18. Kopf M, Baumann H, Freer G, Freudenberg M, Lamers M, et al. (1994) Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 368: 339-342.
19. Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR (1999) Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol 94: 2467-2474.
20. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, et al. (2005) Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41: 1313-1321.
21. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
22. Folch J, Lees M, Sloane Stanley GH (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226: 497-509.
23. Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Meth Enzymol 8: 115-118.
24. Bielawska A, Perry DK, Hannun YA (2001) Determination of ceramides and diglycerides by the diglyceride kinase assay. Anal Biochem 298: 141-150.
25. George J, Pera N, Phung N, Leclercq I, Yun Hou J, et al. (2003) Lipid peroxidation, stellate cell activation and hepatic fibrogenesis in a rat model of chronic steatohepatitis. J Hepatol 39: 756-764.
26. Cuvillier O, Edsall L, Spiegel S (2000) Involvement of sphingosine in mitochondria-dependent Fas-induced apoptosis of type II Jurkat T cells. J Biol Chem 275: 15691-15700.
27. Natori S, Rust C, Stadheim LM, Srinivasan A, Burgart LJ, et al. (2001) Hepatocyte apoptosis is a pathologic feature of human alcoholic hepatitis. J Hepatol 34: 248-253.
28. Feldstein AE, Canbay A, Angulo P, Taniai M, Burgart LJ, et al. (2003) Hepatocyte apoptosis and fas expression are prominent features of human nonalcoholic steatohepatitis. Gastroenterology 125: 437-443.
29. Ribeiro PS, Cortez-Pinto H, Sola S, Castro RE, Ramalho RM, et al. (2004) Hepatocyte apoptosis, expression of death receptors, and activation of NF-kappaB in the liver of nonalcoholic and alcoholic steatohepatitis patients. Am J Gastroenterol 99: 1708-1717.
30. Jin X, Zimmers TA, Perez EA, Pierce RH, Zhang Z, et al. (2006) Paradoxical effects of short- and long-term interleukin-6 exposure on liver injury and repair. Hepatology 43: 474-484.
31. Kirsch R, Clarkson V, Verdonk RC, Marais AD, Shepard EG, et al. (2006) Rodent nutritional model of steatohepatitis: effects of endotoxin (lipopolysaccharide) and tumor necrosis factor alpha deficiency. J Gastroenterol Hepatol 21: 174-182.
32. Baumgardner JN, Shankar K, Hennings L, Badger TM, Ronis MJ (2007) A New Model For Non-Alcoholic Steatohepatitis in the Rat Utilizing Total Enteral Nutrition to Overfeed a High Polyunsaturated Fat Diet. Am J Physiol Gastrointest Liver Physiol 294: G27-38.
33. Li Z, Agellon LB, Allen TM, Umeda M, Jewell L, et al. (2006) The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab 3: 321-331.
34. Puri P, Baillie RA, Wiest MM, Mirshahi F, Choudhury J, et al. (2007) A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 46: 1081-1090.
35. Holland WL, Brozinick JT, Wang LP, Hawkins ED, Sargent KM, et al. (2007) Inhibition of ceramide synthesis ameliorates glucocorticoid-, saturated-fat-, and obesity-induced insulin resistance. Cell Metab 5: 167-179.
36. Mari M, Fernandez-Checa JC (2007) Sphingolipid signalling and liver diseases. Liver Int 27: 440-450.
37. Malagarie-Cazenave S, Andrieu-Abadie N, Ségui B, Gouaz V, Tardy C, et al. (2002) Sphingolipid signalling: molecular basis and role in TNF-induced cell death. Expert Rev Mol Med 2002. 1-15.
38. Malagarie-Cazenave S, Ségui B, Leveque S, Garcia V, Carpentier S, et al. (2004) Role of FAN in tumor necrosis factor-alpha and lipopolysaccharide-induced interleukin-6 secretion and lethality in D-galactosamine-sensitized mice. J Biol Chem 279: 18648-18655.
39. Leclercq IA, Farrell GC, Field J, Bell DR, Gonzalez FJ, et al. (2000) CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J Clin Invest 105: 1067-1075.
40. Dela Pena A, Leclercq I, Field J, George J, Jones B, et al. (2005) NF-kappaB activation, rather than TNF, mediates hepatic inflammation in a murine dietary model of steatohepatitis. Gastroenterology 129: 1663-1674.
41. Gyamfi MA, Damjanov I, French S, Wan YJ (2008) The pathogenesis of ethanol versus methionine and choline deficient diet-induced liver injury. Biochem Pharmacol 75: 981-995.
42. Wallenius V, Wallenius K, Ahren B, Rudling M, Carlsten H, et al. (2002) Interleukin-6-deficient mice develop mature-onset obesity. Nat Med 8: 75-79.
43. Senn JJ, Klover PJ, Nowak IA, Mooney RA (2002) Interleukin-6 induces cellular insulin resistance in hepatocytes. Diabetes 51: 3391-3399.
44. Abiru S, Migita K, Maeda Y, Daikoku M, Ito M, et al. (2006) Serum cytokine and soluble cytokine receptor levels in patients with non-alcoholic steatohepatitis. Liver Int 26: 39-45.
45. Haukeland JW, Damas JK, Konopski Z, Loberg EM, Haaland T, et al. (2006) Systemic inflammation in nonalcoholic fatty liver disease is characterized by elevated levels of CCL2. J Hepatol 44: 1167-1174.
46. Hill DB, Marsano L, Cohen D, Allen J, Shedlofsky S, et al. (1992) Increased plasma interleukin-6 concentrations in alcoholic hepatitis. J Lab Clin Med 119: 547-552.
47. Pedersen BK, Fischer CP (2007) Physiological roles of muscle-derived interleukin-6 in response to exercise. Curr Opin Clin Nutr Metab Care 10: 265-271.
48. Mooney RA (2007) Counterpoint: Interleukin-6 does not have a beneficial role in insulin sensitivity and glucose homeostasis. J Appl Physiol 102: 816-818; discussion 818-9.
49. Pedersen BK, Febbraio MA (2007) Point: Interleukin-6 does have a beneficial role in insulin sensitivity and glucose homeostasis. J Appl Physiol 102: 814-816.
50. Cressman DE, Greenbaum LE, DeAngelis RA, Ciliberto G, Furth EE, et al. (1996) Liver failure and defective hepatocyte regeneration in interleukin-6-deficient mice. Science 274: 1379-1383.
51. Deutschman CS, Cereda M, Ochroch EA, Raj NR (2006) Sepsis-induced cholestasis, steatosis, hepatocellular injury, and impaired hepatocellular regeneration are enhanced in interleukin-6 -/- mice. Crit Care Med 34: 2613-2620.
52. Hong F, Radaeva S, Pan HN, Tian Z, Veech R, et al. (2004) Interleukin 6 alleviates hepatic steatosis and ischemia/reperfusion injury in mice with fatty liver disease. Hepatology 40: 933-941.
53. Hong F, Kim WH, Tian Z, Jaruga, Ishac E, et al. (2002) Elevated interleukin-6 during ethanol consumption acts as a potential endogenous protective cytokine against ethanol-induced apoptosis in the liver: involvement of induction of Bcl-2 and Bcl-x(L) proteins. Oncogene 21: 32-43.
54. El-Assal O, Hong F, Kim WH, Radaeva S, Gao B (2004) IL-6-deficient mice are susceptible to ethanol-induced hepatic steatosis: IL-6 protects against ethanol-induced oxidative stress and mitochondrial permeability transition in the liver. Cell Mol Immunol 1: 205-211.
55. McGettrick HM, Smith E, Filer A, Kissane S, Salmon M, et al. (2009) Fibroblasts from different sites may promote or inhibit recruitment of flowing lymphocytes by endothelial cells. Eur J Immunol 39: 113-125.
56. Kim JH, Bachmann RA, Chen J (2009) Interleukin-6 and insulin resistance. Vitam Horm 80: 613-633.
57. Korn T, Betteli E, Oukka M, Kuchroo VK (2009) IL-17 and Th17 Cells. Annu Rev Immunol 27: 485-517.
58. Scheller J, Rose-John S (2006) Interleukin-6 and its receptor: from bench to bedside. Med Microbiol Immunol 195: 173-183.
59. Fernandez-Checa JC, Colell A, Mari M, Garcia-Ruiz C (2005) Ceramide, tumor necrosis factor and alcohol-induced liver disease. Alcohol Clin Exp Res 29: 151S-157S.
60. Wieckowska A, Papouchado BG, Li Z, Lopez R, Zein NN, et al. (2008) Increased hepatic and circulating interleukin-6 levels in human nonalcoholic steatohepatitis. Am J Gastroenterol 103: 1372-1379.