Changes in the hepatic mitochondrial and membrane proteome in mice fed a non-alcoholic steatohepatitis inducing diet

Journal of Proteomics

Volumn 80, Issue , 2013, Pages 107-122

  Thomas, Anja ^a   Klein, Matthias S ^a   Stevens, Axel P ^a,c   Reinders, Yvonne ^a   Hellerbrand, Claus ^b   Dettmer, Katja ^a   Gronwald, Wolfram ^a   Oefner, Peter J ^a   Reinders, Jörg ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

^b UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^c HELMHOLTZ CENTRE FOR ENVIRONMENTAL RESEARCH UFZ   (Germany)

Author keywords

Differential two dimensional gel electrophoresis; Metabolomics; Non alcoholic steatohepatitis; Proteomics; Stable isotope labeling

Indexed keywords

CD147 ANTIGEN; CHOLESTEROL; GLUTATHIONE TRANSFERASE; GLYCEROL; HEAT SHOCK PROTEIN; LIPID; MEMBRANE PROTEIN; METHIONINE; METHYLTRANSFERASE; MICROSOME ENZYME; PROTEOME; CATION; POLYAMINE; UREA;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ENERGY METABOLISM; FATTY LIVER; FEMALE; HEPATITIS; LIPID DIET; LIVER MITOCHONDRION; METABOLIC REGULATION; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; PROTEOMICS; QUANTITATIVE ANALYSIS; UREA CYCLE; ANIMAL; C57BL MOUSE; CELL MEMBRANE; CHEMISTRY; DIET; DISEASE MODEL; FIBROSIS; GENE EXPRESSION PROFILING; INFLAMMATION; LIVER; LIVER MICROSOME; MASS SPECTROMETRY; METABOLISM; PATHOPHYSIOLOGY; PROCEDURES; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ANIMALS; CATIONS; CELL MEMBRANE; CHOLESTEROL; DIET; DISEASE MODELS, ANIMAL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FEMALE; FIBROSIS; GENE EXPRESSION PROFILING; GLUTATHIONE TRANSFERASE; GLYCEROL; INFLAMMATION; LIPIDS; LIVER; MASS SPECTROMETRY; METHIONINE; MICE; MICE, INBRED C57BL; MICROSOMES, LIVER; MITOCHONDRIA, LIVER; NON-ALCOHOLIC FATTY LIVER DISEASE; POLYAMINES; PROTEOME; PROTEOMICS; UREA;

EID: 84873628834     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2012.12.027     Document Type: Article

References (80)

1. Bellentani S., Scaglioni F., Marino M., Bedogni G. Epidemiology of non-alcoholic fatty liver disease. Dig Dis 2010, 28:155-161.
2. Basaranoglu M., Kayacetin S., Yilmaz N., Kayacetin E., Tarcin O., Sonsuz A. Understanding mechanisms of the pathogenesis of nonalcoholic fatty liver disease. World J Gastroenterol 2010, 16:2223-2226.
3. Day C.P., James O.F. Steatohepatitis: a tale of two "hits"?. Gastroenterology 1998, 114:842-845.
4. Fromenty B., Robin M.A., Igoudjil A., Mansouri A., Pessayre D. The ins and outs of mitochondrial dysfunction in NASH. Diabetes Metab 2004, 30:121-138.
5. Caldwell S.H., Crespo D.M., Kang H.S., Al-Osaimi A.M. Obesity and hepatocellular carcinoma. Gastroenterology 2004, 127:S97-S103.
6. Bugianesi E., Manzini P., D'Antico S., Vanni E., Longo F., Leone N., et al. Relative contribution of iron burden, HFE mutations, and insulin resistance to fibrosis in nonalcoholic fatty liver. Hepatology 2004, 39:179-187.
7. Reddy J.K., Rao M.S. Lipid metabolism and liver inflammation. II. Fatty liver disease and fatty acid oxidation. Am J Physiol Gastrointest Liver Physiol 2006, 290:G852-G858.
8. Charlton M., Sreekumar R., Rasmussen D., Lindor K., Nair K.S. Apolipoprotein synthesis in nonalcoholic steatohepatitis. Hepatology 2002, 35:898-904.
9. Desai M.S., Mariscalco M.M., Tawil A., Vallejo J.G., Smith C.W. Atherogenic diet-induced hepatitis is partially dependent on murine TLR4. J Leukoc Biol 2008, 83:1336-1344.
10. Vergnes L., Phan J., Strauss M., Tafuri S., Reue K. Cholesterol and cholate components of an atherogenic diet induce distinct stages of hepatic inflammatory gene expression. J Biol Chem 2003, 278:42774-42784.
11. Dorn C., Riener M.O., Kirovski G., Saugspier M., Steib K., Weiss T.S., et al. Expression of fatty acid synthase in nonalcoholic fatty liver disease. Int J Clin Exp Pathol 2010, 3:505-514.
12. Jeong W.I., Jeong D.H., Do S.H., Kim Y.K., Park H.Y., Kwon O.D., et al. Mild hepatic fibrosis in cholesterol and sodium cholate diet-fed rats. J Vet Med Sci 2005, 67:235-242.
13. Anstee Q.M., Goldin R.D. Mouse models in non-alcoholic fatty liver disease and steatohepatitis research. Int J Exp Pathol 2006, 87:1-16.
14. Thomas A., Stevens A.P., Klein M.S., Hellerbrand C., Dettmer K., Gronwald W., et al. Early changes in the liver-soluble proteome from mice fed a nonalcoholic steatohepatitis inducing diet. Proteomics 2012, 12:1437-1451.
15. Heitzmann D., Derand R., Jungbauer S., Bandulik S., Sterner C., Schweda F., et al. Invalidation of TASK1 potassium channels disrupts adrenal gland zonation and mineralocorticoid homeostasis. EMBO J 2008, 27:179-187.
16. Gabele E., Dostert K., Dorn C., Patsenker E., Stickel F., Hellerbrand C. A new model of interactive effects of alcohol and high-fat diet on hepatic fibrosis. Alcohol Clin Exp Res 2011, 35:1361-1367.
17. Dorn C., Heilmann J., Hellerbrand C. Protective effect of xanthohumol on toxin-induced liver inflammation and fibrosis. Int J Clin Exp Pathol 2012, 5:29-36.
18. Klein M., Dorn C., Saugspier M., Hellerbrand C., Oefner P., Gronwald W. Discrimination of steatosis and NASH in mice using nuclear magnetic resonance spectroscopy. Metabolomics 2010, 7:237-246.
19. Johnson N.A., Walton D.W., Sachinwalla T., Thompson C.H., Smith K., Ruell P.A., et al. Noninvasive assessment of hepatic lipid composition: advancing understanding and management of fatty liver disorders. Hepatology 2008, 47:1513-1523.
20. Cobbold J.F., Anstee Q.M., Goldin R.D., Williams H.R., Matthews H.C., North B.V., et al. Phenotyping murine models of non-alcoholic fatty liver disease through metabolic profiling of intact liver tissue. Clin Sci (Lond) 2009, 116:403-413.
21. Stevens A.P., Dettmer K., Kirovski G., Samejima K., Hellerbrand C., Bosserhoff A.K., et al. Quantification of intermediates of the methionine and polyamine metabolism by liquid chromatography-tandem mass spectrometry in cultured tumor cells and liver biopsies. J Chromatogr A 2010, 1217:3282-3288.
22. Meisinger C., Sommer T., Pfanner N. Purification of Saccharomcyes cerevisiae mitochondria devoid of microsomal and cytosolic contaminations. Anal Biochem 2000, 287:339-342.
23. Wang W., Scali M., Vignani R., Spadafora A., Sensi E., Mazzuca S., et al. Protein extraction for two-dimensional electrophoresis from olive leaf, a plant tissue containing high levels of interfering compounds. Electrophoresis 2003, 24:2369-2375.
24. Blum H., Beier H., Gross H.J. Improved silver staining of plant-proteins, Rna and DNA in polyacrylamide gels. Electrophoresis 1987, 8:93-99.
25. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006, 1:2856-2860.
26. Wagner Y., Sickmann A., Meyer H.E., Daum G. Multidimensional nano-HPLC for analysis of protein complexes. J Am Soc Mass Spectrom 2003, 14:1003-1011.
27. Ishihama Y., Oda Y., Tabata T., Sato T., Nagasu T., Rappsilber J., et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005, 4:1265-1272.
28. Galli F., Varga Z., Balla J., Ferraro B., Canestrari F., Floridi A., et al. Vitamin E, lipid profile, and peroxidation in hemodialysis patients. Kidney Int Suppl 2001, 78:S148-S154.
29. Santamaria E., Avila M.A., Latasa M.U., Rubio A., Martin-Duce A., Lu S.C., et al. Functional proteomics of nonalcoholic steatohepatitis: mitochondrial proteins as targets of S-adenosylmethionine. Proc Natl Acad Sci U S A 2003, 100:3065-3070.
30. Rodriguez-Suarez E., Mato J.M., Elortza F. Proteomics analysis of human nonalcoholic fatty liver. Methods Mol Biol 2012, 909:241-258.
31. Rodriguez-Suarez E., Duce A.M., Caballeria J., Martinez Arrieta F., Fernandez E., Gomara C., et al. Non-alcoholic fatty liver disease proteomics. Proteomics Clin Appl 2010, 4:362-371.
32. Martel C., Esposti D.D., Bouchet A., Brenner C., Lemoine A. Non-alcoholic steatohepatitis: new insights from OMICS studies. Curr Pharm Biotechnol 2012, 13:726-735.
33. Berasain C., Hevia H., Fernandez-Irigoyen J., Larrea E., Caballeria J., Mato J.M., et al. Methylthioadenosine phosphorylase gene expression is impaired in human liver cirrhosis and hepatocarcinoma. Biochim Biophys Acta 2004, 1690:276-284.
34. Teng Y.W., Mehedint M.G., Garrow T.A., Zeisel S.H. Deletion of betaine-homocysteine S-methyltransferase in mice perturbs choline and 1-carbon metabolism, resulting in fatty liver and hepatocellular carcinomas. J Biol Chem 2011, 286:36258-36267.
35. Martinez-Chantar M.L., Vazquez-Chantada M., Ariz U., Martinez N., Varela M., Luka Z., et al. Loss of the glycine N-methyltransferase gene leads to steatosis and hepatocellular carcinoma in mice. Hepatology 2008, 47:1191-1199.
36. Lu S.C., Alvarez L., Huang Z.Z., Chen L., An W., Corrales F.J., et al. Methionine adenosyltransferase 1A knockout mice are predisposed to liver injury and exhibit increased expression of genes involved in proliferation. Proc Natl Acad Sci U S A 2001, 98:5560-5565.
37. Kalhan S.C., Edmison J., Marczewski S., Dasarathy S., Gruca L.L., Bennett C., et al. Methionine and protein metabolism in non-alcoholic steatohepatitis: evidence for lower rate of transmethylation of methionine. Clin Sci (Lond) 2011, 121:179-189.
38. Abdelmalek M.F., Angulo P., Jorgensen R.A., Sylvestre P.B., Lindor K.D. Betaine, a promising new agent for patients with nonalcoholic steatohepatitis: results of a pilot study. Am J Gastroenterol 2001, 96:2711-2717.
39. Friedman S.L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol Rev 2008, 88:125-172.
40. Simonen P., Kotronen A., Hallikainen M., Sevastianova K., Makkonen J., Hakkarainen A., et al. Cholesterol synthesis is increased and absorption decreased in non-alcoholic fatty liver disease independent of obesity. J Hepatol 2011, 54:153-159.
41. Warner G.J., Stoudt G., Bamberger M., Johnson W.J., Rothblat G.H. Cell toxicity induced by inhibition of acyl coenzyme A: cholesterol acyltransferase and accumulation of unesterified cholesterol. J Biol Chem 1995, 270:5772-5778.
42. Sevanian A., Peterson A.R. The cytotoxic and mutagenic properties of cholesterol oxidation products. Food Chem Toxicol 1986, 24:1103-1110.
43. Gaemers I.C., Stallen J.M., Kunne C., Wallner C., van Werven J., Nederveen A., et al. Lipotoxicity and steatohepatitis in an overfed mouse model for non-alcoholic fatty liver disease. Biochim Biophys Acta 2011, 1812:447-458.
44. Newberry E.P., Xie Y., Kennedy S., Han X., Buhman K.K., Luo J., et al. Decreased hepatic triglyceride accumulation and altered fatty acid uptake in mice with deletion of the liver fatty acid-binding protein gene. J Biol Chem 2003, 278:51664-51672.
45. Zannis V.I., Kan H.Y., Kritis A., Zanni E.E., Kardassis D. Transcriptional regulatory mechanisms of the human apolipoprotein genes in vitro and in vivo. Curr Opin Lipidol 2001, 12:181-207.
46. Zhang S.H., Reddick R.L., Piedrahita J.A., Maeda N. Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1992, 258:468-471.
47. Sparks L.M., Xie H., Koza R.A., Mynatt R., Hulver M.W., Bray G.A., et al. A high-fat diet coordinately downregulates genes required for mitochondrial oxidative phosphorylation in skeletal muscle. Diabetes 2005, 54:1926-1933.
48. Serviddio G., Bellanti F., Tamborra R., Rollo T., Romano A.D., Giudetti A.M., et al. Alterations of hepatic ATP homeostasis and respiratory chain during development of non-alcoholic steatohepatitis in a rodent model. Eur J Clin Invest 2008, 38:245-252.
49. Lieber C.S. CYP2E1: from ASH to NASH. Hepatol Res 2004, 28:1-11.
50. Weltman M.D., Farrell G.C., Liddle C. Increased hepatocyte CYP2E1 expression in a rat nutritional model of hepatic steatosis with inflammation. Gastroenterology 1996, 111:1645-1653.
51. Chalasani N., Gorski J.C., Asghar M.S., Asghar A., Foresman B., Hall S.D., et al. Hepatic cytochrome P450 2E1 activity in nondiabetic patients with nonalcoholic steatohepatitis. Hepatology 2003, 37:544-550.
52. Mantena S.K., Vaughn D.P., Andringa K.K., Eccleston H.B., King A.L., Abrams G.A., et al. High fat diet induces dysregulation of hepatic oxygen gradients and mitochondrial function in vivo. Biochem J 2009, 417:183-193.
53. Leclercq I.A., Farrell G.C., Field J., Bell D.R., Gonzalez F.J., Robertson G.R. CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J Clin Invest 2000, 105:1067-1075.
54. Li N., Muthusamy S., Liang R., Sarojini H., Wang E. Increased expression of miR-34a and miR-93 in rat liver during aging, and their impact on the expression of Mgst1 and Sirt1. Mech Ageing Dev 2011, 132:75-85.
55. Li S., Chen X., Zhang H., Liang X., Xiang Y., Yu C., et al. Differential expression of microRNAs in mouse liver under aberrant energy metabolic status. J Lipid Res 2009, 50:1756-1765.
56. Abdelmegeed M.A., Yoo S.H., Henderson L.E., Gonzalez F.J., Woodcroft K.J., Song B.J. PPARalpha expression protects male mice from high fat-induced nonalcoholic fatty liver. J Nutr 2011, 141:603-610.
57. Huet E., Vallee B., Szul D., Verrecchia F., Mourah S., Jester J.V., et al. Extracellular matrix metalloproteinase inducer/CD147 promotes myofibroblast differentiation by inducing alpha-smooth muscle actin expression and collagen gel contraction: implications in tissue remodeling. FASEB J 2008, 22:1144-1154.
58. Igolnikov A.C., Green R.M. Mice heterozygous for the Mdr2 gene demonstrate decreased PEMT activity and diminished steatohepatitis on the MCD diet. J Hepatol 2006, 44:586-592.
59. Geubel A.P., Mairlot M.C., Buchet J.P., Dive C., Lauwerys R. Abnormal methylation capacity in human liver cirrhosis. Int J Clin Pharmacol Res 1988, 8:117-122.
60. Turro S., Ingelmo-Torres M., Estanyol J.M., Tebar F., Fernandez M.A., Albor C.V., et al. Identification and characterization of associated with lipid droplet protein 1: a novel membrane-associated protein that resides on hepatic lipid droplets. Traffic 2006, 7:1254-1269.
61. Perna A.F., Sepe I., Lanza D., Pollastro R.M., De Santo N.G., Ingrosso D. Hyperhomocysteinemia in chronic renal failure: alternative therapeutic strategies. J Ren Nutr 2012, 22:191-194.
62. Vacek T.P., Vacek J.C., Tyagi N., Tyagi S.C. Autophagy and heart failure: a possible role for homocysteine. Cell Biochem Biophys 2012, 62:1-11.
63. Oussalah A., Gueant J.L., Peyrin-Biroulet L. Meta-analysis: hyperhomocysteinaemia in inflammatory bowel diseases. Aliment Pharmacol Ther 2011, 34:1173-1184.
64. Polyzos S.A., Anastasilakis A.D., Efstathiadou Z., Litsas I., Kita M., Panagiotou A., et al. Serum homocysteine, folate and vitamin B12 in patients with Paget's disease of bone: the effect of zoledronic acid. J Bone Miner Metab 2010, 28:314-319.
65. Christensen K.E., Wu Q., Wang X., Deng L., Caudill M.A., Rozen R. Steatosis in mice is associated with gender, folate intake, and expression of genes of one-carbon metabolism. J Nutr 2010, 140:1736-1741.
66. Avila M.A., Berasain C., Torres L., Martin-Duce A., Corrales F.J., Yang H., et al. Reduced mRNA abundance of the main enzymes involved in methionine metabolism in human liver cirrhosis and hepatocellular carcinoma. J Hepatol 2000, 33:907-914.
67. Baiges I., Palmfeldt J., Blade C., Gregersen N., Arola L. Lipogenesis is decreased by grape seed proanthocyanidins according to liver proteomics of rats fed a high fat diet. Mol Cell Proteomics 2010, 9:1499-1513.
68. Koturbash I., Melnyk S., James S.J., Beland F.A., Pogribny I.P. Role of epigenetic and miR-22 and miR-29b alterations in the downregulation of Mat1a and Mthfr genes in early preneoplastic livers in rats induced by 2-acetylaminofluorene. Mol Carcinog 2012, 10.1002/mc.21861.
69. Frau M., Tomasi M.L., Simile M.M., Demartis M.I., Salis F., Latte G., et al. Role of transcriptional and post-transcriptional regulation of methionine adenosyltransferases in liver cancer progression. Hepatology 2012, 56:165-175.
70. Hellerbrand C., Muhlbauer M., Wallner S., Schuierer M., Behrmann I., Bataille F., et al. Promoter-hypermethylation is causing functional relevant downregulation of methylthioadenosine phosphorylase (MTAP) expression in hepatocellular carcinoma. Carcinogenesis 2006, 27:64-72.
71. Scaglia F., Brunetti-Pierri N., Kleppe S., Marini J., Carter S., Garlick P., et al. Clinical consequences of urea cycle enzyme deficiencies and potential links to arginine and nitric oxide metabolism. J Nutr 2004, 134:2775S-2782S. [discussion 96S-97S].
72. Li L.O., Hu Y.F., Wang L., Mitchell M., Berger A., Coleman R.A. Early hepatic insulin resistance in mice: a metabolomics analysis. Mol Endocrinol 2010, 24:657-666.
73. Petrak J., Myslivcova D., Man P., Cmejla R., Cmejlova J., Vyoral D., et al. Proteomic analysis of hepatic iron overload in mice suggests dysregulation of urea cycle, impairment of fatty acid oxidation, and changes in the methylation cycle. Am J Physiol Gastrointest Liver Physiol 2007, 292:G1490-G1498.
74. Cockell K.A., Wotherspoon A.T., Belonje B., Fritz M.E., Madere R., Hidiroglou N., et al. Limited effects of combined dietary copper deficiency/iron overload on oxidative stress parameters in rat liver and plasma. J Nutr Biochem 2005, 16:750-756.
75. Brown K.E., Dennery P.A., Ridnour L.A., Fimmel C.J., Kladney R.D., Brunt E.M., et al. Effect of iron overload and dietary fat on indices of oxidative stress and hepatic fibrogenesis in rats. Liver Int 2003, 23:232-242.
76. Fujita N., Miyachi H., Tanaka H., Takeo M., Nakagawa N., Kobayashi Y., et al. Iron overload is associated with hepatic oxidative damage to DNA in nonalcoholic steatohepatitis. Cancer Epidemiol Biomarkers Prev 2009, 18:424-432.
77. Wang P., Bouwman F.G., Mariman E.C. Generally detected proteins in comparative proteomics-a matter of cellular stress response?. Proteomics 2009, 9:2955-2966.
78. Petrak J., Ivanek R., Toman O., Cmejla R., Cmejlova J., Vyoral D., et al. Deja vu in proteomics. A hit parade of repeatedly identified differentially expressed proteins. Proteomics 2008, 8:1744-1749.
79. Ko K.S., Tomasi M.L., Iglesias-Ara A., French B.A., French S.W., Ramani K., et al. Liver-specific deletion of prohibitin 1 results in spontaneous liver injury, fibrosis, and hepatocellular carcinoma in mice. Hepatology 2010, 52:2096-2108.
80. Valle A., Catalan V., Rodriguez A., Rotellar F., Valenti V., Silva C., et al. Identification of liver proteins altered by type 2 diabetes mellitus in obese subjects. Liver Int 2012, 32:951-961.