Differential representation of liver proteins in obese human subjects suggests novel biomarkers and promising targets for drug development in obesity

References

• Savini I, Catani MV, Evangelista D, et al. Obesity-associated oxidative stress: strategies finalized to improve redox state. Int J Mol Sci 2013;14:10497–538.
   PubMed Web of Science ®Google Scholar
• Matos JM, Witzmann FA, Cummings OW, Schmidt CM. A pilot study of proteomic profiles of human hepatocellular carcinoma in the United States. J Surg Res 2009;155:237–43.
   PubMed Web of Science ®Google Scholar
• Codarin E, Renzone G, Poz A, et al. Differential proteomic analysis of subfractioned human hepatocellular carcinoma tissues. J Proteome Res 2009;8:2273–84.
   PubMed Web of Science ®Google Scholar
• Cesaratto L, Vascotto C, D'Ambrosio C, et al. Overoxidation of peroxiredoxins as an immediate and sensitive marker of oxidative stress in HepG2 cells and its application to the redox effects induced by ischemia/reperfusion in human liver. Free Radic Res 2005;39:255–68.
   PubMed Web of Science ®Google Scholar
• Kimhofer T, Fye H, Taylor-Robinson S, et al. Proteomic and metabonomic biomarkers for hepatocellular carcinoma: a comprehensive review. Br J Cancer 2015;112:1141–56.
   PubMed Web of Science ®Google Scholar
• Scaloni A, Codarin E, Di Maso V, et al. Modern strategies to identify new molecular targets for the treatment of liver diseases: The promising role of proteomics and redox proteomics investigations. Clin Appl 2009;3:242–62.
   PubMed Web of Science ®Google Scholar
• Takahashi Y, Soejima Y, Fukusato T. Animal models of nonalcoholic fatty liver disease/nonalcoholic steatohepatitis. World J Gastroenterol 2012;18:2300–8.
   PubMed Web of Science ®Google Scholar
• Meneses-Lorente G, Watt A, Salim K, et al. Identification of early proteomic markers for hepatic steatosis. Chem Res Toxicol 2006;19:986–98.
   PubMed Web of Science ®Google Scholar
• Zhang X, Yang J, Guo Y, et al. Functional proteomic analysis of nonalcoholic fatty liver disease in rat models: enoyl-coenzyme a hydratase down-regulation exacerbates hepatic steatosis. Hepatology 2010;51:1190–9.
   PubMed Web of Science ®Google Scholar
• Douette P, Navet R, Gerkens P, et al. Steatosis-induced proteomic changes in liver mitochondria evidenced by two-dimensional differential in-gel electrophoresis. J Proteome Res 2005;4:2024–31.
   PubMed Web of Science ®Google Scholar
• Meierhofer D, Weidner C, Sauer S. Integrative analysis of transcriptomics, proteomics, and metabolomics data of white adipose and liver tissue of high-fat diet and rosiglitazone-treated insulin-resistant mice identified pathway alterations and molecular hubs. J Proteome Res 2014;13:5592–602.
   PubMed Web of Science ®Google Scholar
• Guo Y, Darshi M, Ma Y, et al. Quantitative proteomic and functional analysis of liver mitochondria from high fat diet (HFD) diabetic mice. Mol Cell Proteomics 2013;12:3744–58.
   PubMed Web of Science ®Google Scholar
• Edvardsson U, von Löwenhielm HB, Panfilov O, et al. Hepatic protein expression of lean mice and obese diabetic mice treated with peroxisome proliferator-activated receptor activators. Proteomics 2003;3:468–78.
   PubMed Web of Science ®Google Scholar
• Santamaria E, Avila MA, Latasa MU, et al. Functional proteomics of nonalcoholic steatohepatitis: mitochondrial proteins as targets of S-adenosylmethionine. Proc Natl Acad Sci USA 2003;100:3065–70.
   PubMed Web of Science ®Google Scholar
• Wang X, Choi JW, Oh TS, et al. Comparative hepatic proteome analysis between lean and obese rats fed a high-fat diet reveals the existence of gender differences. Proteomics 2012;12:284–99.
   PubMed Web of Science ®Google Scholar
• Hölper S, Nolte H, Bober E, et al. Dissection of metabolic pathways in the Db/Db mouse model by integrative proteome and acetylome analysis. Mol Biosyst 2015;11:908–22.
   PubMed Web of Science ®Google Scholar
• Sabidó E, Wu Y, Bautista L, et al. Targeted proteomics reveals strain-specific changes in the mouse insulin and central metabolic pathways after a sustained high-fat diet. Mol Syst Biol 2013;9:681.
   PubMed Web of Science ®Google Scholar
• Meneses-Lorente G, Guest PC, Lawrence J, et al. A proteomic investigation of drug-induced steatosis in rat liver. Chem Res Toxicol 2004;17:605–12.
   PubMed Web of Science ®Google Scholar
• Chang J, Oikawa S, Ichihara G, et al. Altered gene and protein expression in liver of the obese spontaneously hypertensive/NDmcr-cp rat. Nutr Metab 2012;9:87.
   Google Scholar
• Eccleston HB, Andringa KK, Betancourt AM, et al. Chronic exposure to a high-fat diet induces hepatic steatosis, impairs nitric oxide bioavailability, and modifies the mitochondrial proteome in mice. Antioxid Redox Signal 2011;15:447–59.
   PubMed Web of Science ®Google Scholar
• Valle A, Catalán V, Rodríguez A, et al. Identification of liver proteins altered by type 2 diabetes mellitus in obese subjects. Liver Int 2012;32:951–61.
   PubMed Web of Science ®Google Scholar
• Younossi ZM, Baranova A, Ziegler K, et al. A genomic and proteomic study of the spectrum of nonalcoholic fatty liver disease. Hepatology 2005;42:665–74.
   PubMed Web of Science ®Google Scholar
• Charlton M, Viker K, Krishnan A, et al. Differential expression of lumican and fatty acid binding protein-1: new insights into the histologic spectrum of nonalcoholic fatty liver disease. Hepatology 2009;49:1375–84.
   PubMed Web of Science ®Google Scholar
• Shevchenko A, Tomas H, Havlis J, et al. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006;1:2856–60.
   PubMed Web of Science ®Google Scholar
• Scippa GS, Rocco M, Ialicicco M, et al. The proteome of lentil (Lens culinaris Medik.) seeds: discriminating between landraces. Electrophoresis 2010;31:497–506.
   PubMed Web of Science ®Google Scholar
• Chinese Human Liver Proteome Profiling Consortium: First insight into the human liver proteome from PROTEOME(SKY)-LIVER(Hu) 1.0, a publicly available database. J Proteome Res 2010;9:79–94.
   PubMed Web of Science ®Google Scholar
• Sun A, Jiang Y, Wang X, et al. Liverbase: a comprehensive view of human liver biology. J Proteome Res 2010;9:50–8.
   PubMed Web of Science ®Google Scholar
• Pearce SG, Thosani NC, Pan J-J. Noninvasive biomarkers for the diagnosis of steatohepatitis and advanced fibrosis in NAFLD. Biomarker Res 2013;1:1–11.
   PubMedGoogle Scholar
• Lee SB, Cho HI, Jin YW, et al. Wild ginseng cambial meristematic cells ameliorate hepatic steatosis and mitochondrial dysfunction in high-fat diet-fed mice. J Pharm Pharmacol 2016;68:119–27.
   PubMed Web of Science ®Google Scholar
• Narayan SB, Master SR, Sireci AN, et al. Short-chain 3-hydroxyacyl-coenzyme A dehydrogenase associates with a protein super-complex integrating multiple metabolic pathways. PLoS One 2012;7:e35048.
   PubMed Web of Science ®Google Scholar
• Hazen SA, Waheed A, Sly WS, et al. Differentiation-dependent expression of CA V and the role of carbonic anhydrase isozymes in pyruvate carboxylation in adipocytes. FASEB J 1996;10:481–90.
   PubMed Web of Science ®Google Scholar
• Lynch CJ, Hazen SA, Horetsky RL, et al. Differentiation-dependent expression of carbonic anhydrase II and III in 3T3 adipocytes. Am J Physiol 1993;265:C234–243.
   PubMed Web of Science ®Google Scholar
• Kheterpal I, Ku G, Coleman L, et al. Proteome of human subcutaneous adipose tissue stromal vascular fraction cells versus mature adipocytes based on DIGE. J Proteome Res 2011;10:1519–27.
   PubMed Web of Science ®Google Scholar
• De Simone G, Supuran CT. Antiobesity carbonic anhydrase inhibitors. Curr Top Med Chem 2007;7:879–84.
   PubMed Web of Science ®Google Scholar
• Fernández-Irigoyen J, Santamaría E, Sesma L, et al. Oxidation of specific methionine and tryptophan residues of apolipoprotein A-I in hepatocarcinogenesis. Proteomics 2005;5:4964–72.
   PubMed Web of Science ®Google Scholar
• Dörmann P, Börchers T, Korf U, et al. Amino acid exchange and covalent modification by cysteine and glutathione explain isoforms of fatty acid-binding protein occurring in bovine liver. J Biol Chem 1993;268:16286–92.
   PubMed Web of Science ®Google Scholar
• Smathers RL, Galligan JJ, Stewart BJ, Petersen DR. Overview of lipid peroxidation products and hepatic protein modification in alcoholic liver disease. Chem Biol Interact 2011;192:107–12.
   PubMed Web of Science ®Google Scholar
• Smathers RL, Fritz KS, Galligan JJ, et al. Characterization of 4-HNE modified L-FABP reveals alterations in structural and functional dynamics. PLoS One 2012;7:e38459.
   PubMed Web of Science ®Google Scholar
• Yang F, Yin Y, Wang F, et al. An altered pattern of liver apolipoprotein A-I isoforms is implicated in male chronic hepatitis B progression. J Proteome Res 2010;9:134–43.
   PubMed Web of Science ®Google Scholar
• Atshaves BP, Martin GG, Hostetler HA, et al. Liver fatty acid-binding protein and obesity. J Nutr Biochem 2010;21:1015–32.
   PubMed Web of Science ®Google Scholar
• Cesaratto L, Vascotto C, Calligaris S, Tell G. The importance of redox state in liver damage. Ann Hepatol 2004;3:86–92.
   PubMedGoogle Scholar
• Mantena SK, King AL, Andringa KK, et al. Mitochondrial dysfunction and oxidative stress in the pathogenesis of alcohol- and obesity-induced fatty liver diseases. Free Radic Biol Med 2008;44:1259–72.
   PubMed Web of Science ®Google Scholar
• Rhee SG, Yang KS, Kang SW, et al. Controlled elimination of intracellular H2O2: regulation of peroxiredoxin, catalase, and glutathione peroxidase via post-translational modification. Antioxid Redox Signal 2005;7:619–26.
   PubMed Web of Science ®Google Scholar
• Latimer HR, Veal EA. Peroxiredoxins in regulation of MAPK signalling pathways; sensors and barriers to signal transduction. Mol Cells 2016;39:40–5.
   PubMed Web of Science ®Google Scholar
• Bachi A, Dalle-Donne I, Scaloni A. Redox proteomics: chemical principles, methodological approaches and biological/biomedical promises. Chem Rev 2013;113:596–698.
   PubMed Web of Science ®Google Scholar
• Knobbe CB, Revett TJ, Bai Y, et al. Choice of biological source material supersedes oxidative stress in its influence on DJ-1 in vivo interactions with Hsp90. J Proteome Res 2011;10:4388–404.
   PubMed Web of Science ®Google Scholar
• Taira T, Saito Y, Niki T, et al. DJ-1 has a role in antioxidative stress to prevent cell death. EMBO Rep 2004;5:213–18.
   PubMed Web of Science ®Google Scholar
• Liu W, Baker SS, Baker RD, et al. Upregulation of haemoglobin expression by oxidative stress in hepatocytes and its implication in non-alcoholic steatohepatitis. PLoS One 2011;6:e24363.
   PubMed Web of Science ®Google Scholar
• Xu L, Xu CF, Yu CH, et al. Haemoglobin and non-alcoholic fatty liver disease: further evidence from a population-based study. Gut 2009;58:1706–7.
   PubMed Web of Science ®Google Scholar
• Trak-Smayra V, Dargere D, Noun R, et al. Serum proteomic profiling of obese patients: correlation with liver pathology and evolution after bariatric surgery. Gut 2009;58:825–32.
   PubMed Web of Science ®Google Scholar
• Noeman SA, Hamooda HE, Baalash AA. Biochemical study of oxidative stress markers in the liver, kidney and heart of high fat diet induced obesity in rats. Diabetol Metab Syndr 2011;3:17.
   PubMed Web of Science ®Google Scholar
• Kurzawski M, Dziedziejko V, Urasińska E, et al. Nuclear factor erythroid 2-like 2 (Nrf2) expression in end-stage liver disease. Environ Toxicol Pharmacol 2012;34:87–95.
   PubMed Web of Science ®Google Scholar
• Tsuchiya H, Ebata Y, Sakabe T. High-fat, high-fructose diet induces hepatic iron overload via a hepcidin-independent mechanism prior to the onset of liver steatosis and insulin resistance in mice. Metabolism 2013;62:62–9.
   PubMed Web of Science ®Google Scholar
• Böhm T, Berger H, Nejabat M, et al. Food-derived peroxidized fatty acids may trigger hepatic inflammation: a novel hypothesis to explain steatohepatitis. J Hepatol 2013;59:563–70.
   PubMed Web of Science ®Google Scholar
• Curtis JM, Grimsrud PA, Wright WS, et al. Downregulation of adipose glutathione S-transferase A4 leads to increased protein carbonylation, oxidative stress, and mitochondrial dysfunction. Diabetes 2010;59:1132–42.
   PubMed Web of Science ®Google Scholar
• Rashid S, Alexander S, Roberts R. Enhanced synthesis of hydrogen sulfide in liver and kidney from Zucker diabetic Fatty rats (ZDF) compared to Zucker Lean (ZL) rats. Nitric Oxide 2013;31:S54.
   Web of Science ®Google Scholar
• Módis K, Coletta C, Erdélyi K, et al. Intramitochondrial hydrogen sulfide production by 3-mercaptopyruvate sulfurtransferase maintains mitochondrial electron flow and supports cellular bioenergetics. FASEB J 2013;27:601–11.
   PubMed Web of Science ®Google Scholar
• Zhang W, Ambati S, Della-Fera MA, et al. Leptin modulated changes in adipose tissue protein expression in ob/ob mice. Obesity (Silver Spring) 2011;19:255–61.
   PubMed Web of Science ®Google Scholar
• Boden G, Duan X, Homko C, et al. Increase in endoplasmic reticulum stress-related proteins and genes in adipose tissue of obese, insulin-resistant individuals. Diabetes 2008;57:2438–44.
   PubMed Web of Science ®Google Scholar
• Labbus K, Henning M, Borkham-Kamphorst E, et al. Proteomic profiling in lipocalin 2 deficient mice under normal and inflammatory conditions. J Proteomics 2013;78:188–96.
   PubMed Web of Science ®Google Scholar
• Li A, Yan Q, Zhao X, et al. Decreased expression of PBLD correlates with poor prognosis and functions as a tumor suppressor in human hepatocellular carcinoma. Oncotarget 2016;7:524–37.
   PubMed Web of Science ®Google Scholar
• Calzadilla P, Gómez-Serrano M, García-Santos E, et al. N-Acetylcysteine affects obesity-related protein expression in 3T3-L1 adipocytes. Redox Rep 2013;18:210–18.
   PubMed Web of Science ®Google Scholar
• Pérez-Pérez R, García-Santos E, Ortega-Delgado FJ, et al. Attenuated metabolism is a hallmark of obesity as revealed by comparative proteomic analysis of human omental adipose tissue. J Proteomics 2012;75:783–95.
   PubMed Web of Science ®Google Scholar
• Maceyka M, Nava VE, Milstien S, Spiegel S. Aminoacylase 1 is a sphingosine kinase 1-interacting protein. FEBS Lett 2004;568:30–4.
   PubMed Web of Science ®Google Scholar
• Hu X, Duan Z, Hu H, et al. Proteomic profile of carbonylated proteins in rat liver: exercise attenuated oxidative stress may be involved in fatty liver improvement. Proteomics 2013; 13:1755–64.
   PubMed Web of Science ®Google Scholar
• Deng Z, Yan S, Hu H, et al. Proteomic profile of carbonylated proteins in rat liver: discovering possible mechanisms for tetracycline-induced steatosis. Proteomics 2015;15:148–59.
   PubMed Web of Science ®Google Scholar
• Curtis JM, Hahn WS, Stone MD, et al. Protein carbonylation and adipocyte mitochondrial function. J Biol Chem 2012;287:32967–80.
   PubMed Web of Science ®Google Scholar
• Piemonte F, Petrini S, Gaeta LM, et al. Protein glutathionylation increases in the liver of patients with non-alcoholic fatty liver disease. J Gastroenterol Hepatol 2008;23:e457–64.
   PubMed Web of Science ®Google Scholar
• Shi J, Zhang Y, Gu W, et al. Serum liver fatty acid binding protein levels correlate positively with obesity and insulin resistance in Chinese young adults. PLoS One 2012;7:e48777.
   PubMedGoogle Scholar
• Bril F, Sninsky JJ, Baca AM, et al. Hepatic Steatosis and Insulin Resistance, But Not Steatohepatitis, Promote Atherogenic Dyslipidemia in NAFLD. J Clin Endocrinol Metab 2016;101:644–52.
   PubMed Web of Science ®Google Scholar
• Supuran CT, Di Fiore A, De Simone G. Oncologic, endocrine and metabolic carbonic anhydrase inhibitors as emerging drugs for the treatment of obesity. Expert Opin Emerging Drugs 2008;13:383–92.
   PubMed Web of Science ®Google Scholar
• Han SJ, Choi SE, Yi SA, et al. Glutamate dehydrogenase activator BCH stimulating reductive amination prevents high fat/high fructose diet-induced steatohepatitis and hyperglycemia in C57BL/6J mice. Sci Rep 2016;5:37468.
   PubMed Web of Science ®Google Scholar