Non-alcoholic steatohepatitis: New insights from OMICS studies

Current Pharmaceutical Biotechnology

Volumn 13, Issue 5, 2012, Pages 726-735

  Martel, Cécile ^a,b   Esposti, Davide Degli ^a,c   Bouchet, Antonin ^a   Brenner, Catherine ^b   Lemoine, Antoinette ^a,c,d  

^a INSERM   (France)

^b Universite Paris Sud   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d HÔPITAL PAUL BROUSSE   (France)

Author keywords

Biomarker; Inflammation; Liver; Mitochondria; NAFLD; Omics

Indexed keywords

ALANINE AMINOTRANSFERASE; BIOLOGICAL MARKER; FATTY ACID; GLUCOSE; GLYCOGEN SYNTHASE KINASE 3; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; MICRORNA; SOMATOMEDIN BINDING PROTEIN 1; TRANSCRIPTOME; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA;

AEROBIC METABOLISM; APOPTOSIS; BIOACCUMULATION; CAPILLARY GAS CHROMATOGRAPHY; CELL ORGANELLE; CHRONIC STRESS; DIABETES MELLITUS; DISEASE ASSOCIATION; DYSLIPIDEMIA; ENDOPLASMIC RETICULUM; GENETIC ASSOCIATION; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOMICS; GLUCOSE BLOOD LEVEL; HUMAN; HYPERINSULINEMIA; HYPERTENSION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INSULIN RESISTANCE; LIPID PEROXIDATION; LIPOGENESIS; LIPOTOXICITY; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER INJURY; METABOLIC SYNDROME X; MICROARRAY ANALYSIS; MITOCHONDRIAL RESPIRATION; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; OXIDATIVE STRESS; PATHOGENESIS; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM;

ANIMALS; FATTY LIVER; HUMANS;

EID: 84860294758     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920112799857558     Document Type: Review

References (66)

1. Yasui, K.; Hashimoto, E.; Komorizono, Y.; Koike, K.; Arii, S.; Imai, Y.; Shima, T.; Kanbara, Y.; Saibara, T.; Mori, T.; Kawata, S.; Uto, H.; Takami, S.; Sumida, Y.; Takamura, T.; Kawanaka, M.; Okanoue, T Japan NASH Study Group, Ministry of Health, Labour, and Welfare of Japan. Characteristics of patients with nonalcoholic steatohepatitis who develop hepatocellular carcinoma. Clin. Gastroenterol. Hepatol., 2011, 5, 428-433.
2. Welzel, T.M.; Graubard, B.I.; Zeuzem, S.; El-Serag, H.B.; Davila, J.A.; McGlynn, K.A. Metabolic syndrome increases the risk of primary liver cancer in the United States: A population-based casecontrol study. Hepatology, 2011, 54(2),463-471.
3. Sørensen, H.T.; Mellemkjaer, L.; Jepsen, P.; Thulstrup, A.M.; Baron, J.; Olsen, J.H.; Vilstrup, H. Risk of cancer in patients hospitalized with fatty liver: a Danish cohort study. J. Clin. Gastroenterol., 2003, 36(4), 356-359.
4. Anderson, N.; Borlak, J. Molecular mechanisms and therapeutic targets in steatosis and steatohepatitis. Pharmacol. Rev., 2008, 60(3), 311-357.
5. Neuschwander-Tetri, B.A. Hepatic lipotoxicity and the pathogenesis of nonalcoholic steatohepatitis: the central role of nontriglyceride fatty acid metabolites. Hepatology, 2010, 52(2), 774-788.
6. Day, C.P.; James, O.F. Steatohepatitis: a tale of two hits? Gastroenterology, 1998, 114(4):842-845.
7. Pessayre, D.; Fromenty, B.; Mansouri, A. Mitochondrial injury in steatohepatitis. Eur. J. Gastroenterol. Hepatol., 2004, 16(11), 1095-1105.
8. Vendemiale, G.; Grattagliano, I.; Caraceni, P.; Caraccio, G.; Domenicali, M.; Dall'Agata, M.; Trevisani, F.; Guerrieri, F.; Bernardi, M.; Altomare, E. Mitochondrial oxidative injury and energy metabolism alteration in rat fatty liver: effect of the nutritional status. Hepatology, 2001, 33(4), 808-815.
9. Peralta, C.; Bartrons, R.; Serafin, A.; Blázquez, C.; Guzmán, M.; Prats, N.; Xaus, C.; Cutillas, B.; Gelpí, E.; Roselló-Catafau, J. Adenosine monophosphate-activated protein kinase mediates the protective effects of ischemic preconditioning on hepatic ischemiareperfusion injury in the rat. Hepatology, 2001, 34(6), 1164-1173.
10. Videla, LA.; Rodrigo, R.; Araya, J.; Poniachik, J. Oxidative stress and depletion of hepatic long-chain polyunsaturated fatty acids may contribute to nonalcoholic fatty liver disease. Free Radic. Bio.l Med., 2004, 37(9), 1499-1507.
11. Malhi, H.; Gores, G.J.; Lemasters, J.J. Apoptosis and necrosis in the liver: a tale of two deaths? Hepatology, 2006, 43(2 Suppl 1), S31-44.
12. Malhi, H.; Guicciardi, M.E.; Gores, G.J. Hepatocyte death: a clear and present danger. Physiol. Rev., 2010, 90(3), 1165-1194.
13. Page, J.M.; Harrison, S.A. NASH and HCC. Clin. Liver Dis., 2009, 13(4), 631-647.
14. Hummasti, S.; Hotamisligil, G.S. Endoplasmic reticulum stress and inflammation in obesity and diabetes. Circ. Res., 2010, 107(5), 579-591.
15. Chavez-Tapia, N.C.; Tellez-Avila, F.I.; Barrientos-Gutierrez, T.; Mendez-Sanchez, N.; Lizardi-Cervera, J.; Uribe, M. Bariatric surgery for non-alcoholic steatohepatitis in obese patients. Cochrane Database Syst. Rev., 2010, 1, CD007340.
16. Shaffer, E.A. Bariatric surgery: a promising solution for nonalcoholic steatohepatitis in the very obese. J. Clin. Gastroenterol., 2006, 40(Suppl 1), S44-50.
17. Yilmaz, Y. The AGEs-RAGE axis and nonalcoholic steatohepatitis: the evidence mounts. J. Gastroenterol., 2010, 45(7), 782-783.
18. Yuan, X.; Waterworth, D.; Perry, J.R.; Lim, N.; Song, K.; Chambers, J.C.; Zhang, W.; Vollenweider, P.; Stirnadel, H.; Johnson, T.; Bergmann, S.; Beckmann, N.D.; Li, Y.; Ferrucci, L.; Melzer, D.; Hernandez, D.; Singleton, A.; Scott, J.; Elliott, P.; Waeber, G.; Cardon, L.; Frayling, T.M.; Kooner, J.S.; Mooser, V. Population-based genomewide association studies reveal six loci influencing plasma levels of liver enzymes. Am. J. Hum. Genet, 2008, 83(4), 520-528.
19. Romeo, S.; Kozlitina, J.; Xing, C.; Pertsemlidis, A.; Cox, D.; Pennacchio, L.A.; Boerwinkle, E.; Cohen, J.C.; Hobbs, H.H. Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nat. Genet., 2008, 40(12), 1461-1465.
20. Krawczyk, M.; Grünhage, F.; Zimmer, V.; Lammert, F. Variant adiponutrin (PNPLA3) represents a common fibrosis risk gene: non-invasive elastography-based study in chronic liver disease. J. Hepatol., 2010, Dec 17. [Epub ahead of print]
21. Sookoian, S.; Pirola, CJ. Meta-analysis of the influence of I148M variant of patatin-like phospholipase domain containing 3 gene (PNPLA3) on the susceptibility and histological severity of nonalcoholic fatty liver disease. Hepatology, 2011, 53(6), 1883-1894.
22. Chalasani, N.; Guo, X.; Loomba, R.; Goodarzi, MO.; Haritunians, T.; Kwon, S.; Cui, J.; Taylor, K.D.; Wilson, L.; Cummings, O.W.; Chen, Y.D.; Rotter, J.I. Nonalcoholic Steatohepatitis Clinical Research Network. Genome-wide association study identifies variants associated with histologic features of nonalcoholic Fatty liver disease. Gastroenterology, 2010, 139(5), 1567-1576, 1576.e1-6.
23. Sreekumar, R.; Rosado, B.; Rasmussen, D.; Charlton, M. Hepatic gene expression in histologically progressive nonalcoholic steatohepatitis. Hepatology, 2003, 38(1), 244-251.
24. Younossi, Z.M.; Baranova, A.; Ziegler, K.; Del Giacco, L.; Schlauch, K.; Born, T.L.; Elariny, H.; Gorreta, F.; VanMeter, A.; Younoszai, A.; Ong, J.P.; Goodman, Z.; Chandhoke, V. A genomic and proteomic study of the spectrum of nonalcoholic fatty liver disease. Hepatology, 2005, 42(3), 665-674.
25. Washington, K.; Wright, K.; Shyr, Y.; Hunter, E.B.; Olson, S.; Raiford, D.S. Hepatic stellate cell activation in nonalcoholic steatohepatitis and fatty liver. Hum. Pathol., 2000, 31(7), 822-828.
26. Omary, M.B.; Ku, N.O.; Toivola, D.M. Keratins: guardians of the liver. Hepatology, 2002, 35, 251-257.
27. Chiappini, F.; Barrier, A.; Saffroy, R.; Domart, M.C.; Dagues, N.; Azoulay, D.; Sebagh, M.; Franc, B.; Chevalier, S.; Debuire, B.; Dudoit, S.; Lemoine, A. Exploration of global gene expression in human liver steatosis by high-density oligonucleotide microarray. Lab. Invest., 2006, 86(2), 154-165.
28. Cheung, O.; Puri, P.; Eicken, C.; Contos, M.J.; Mirshahi, F.; Maher, J.W.; Kellum, J.M.; Min, H.; Luketic, V.A.; Sanyal, A.J. Nonalcoholic steatohepatitis is associated with altered hepatic MicroRNA expression. Hepatology, 2008, 48(6), 1810-1820.
29. Filipowicz, W.; Grosshans, H. The liver-specific microRNA miR-122: biology and therapeutic potential. Prog. Drug. Res., 2011, 67, 221-238.
30. Douette, P.; Navet, R.; Gerkens, P.; de Pauw, E.; Leprince, P.; Sluse-Goffart, C.; Sluse, F.E. Steatosis-induced proteomic changes in liver mitochondria evidenced by two-dimensional differential ingel electrophoresis. J. Proteome Res., 2005, 4(6), 2024-2031.
31. Kirpich, I.A.; Gobejishvili, L.N.; Bon Homme, M.; Waigel, S.; Cave, M.; Arteel, G.; Barve, SS.; McClain, C.J.; Deaciuc, I.V. Integrated hepatic transcriptome and proteome analysis of mice with high-fat diet-induced nonalcoholic fatty liver disease. J. Nutr. Biochem., 2011, 22(1), 38-45.
32. Sokolovic, M.; Sokolovic, A.; van Roomen, C.P.; Gruber, A.; Ottenhoff, R.; Scheij, S.; Hakvoort, T.B.; Lamers, W.H.; Groen, A.K. Unexpected effects of fasting on murine lipid homeostasistranscriptomic and lipid profiling. J. Hepatol., 2010, 52(5), 737-744.
33. De Gottardi, A.; Vinciguerra, M.; Sgroi, A.; Moukil, M.; Ravier-Dall'Antonia, F.; Pazienza, V.; Pugnale, P.; Foti, M.; Hadengue, A. Microarray analyses and molecular profiling of steatosis induction in immortalized human hepatocytes. Lab. Invest., 2007, 87(8), 792-806.
34. Eccleston, H.B.; Andringa, K.K.; Betancourt, A.M.; King, A.L.; Mantena, S.K.; Swain, T.M.; Tinsley, H.N.; Nolte, R.N.; Nagy T.R.; Abrams, G.A. Bailey, S.M. 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, 5(2), 447-459.
35. Wang, H.; Chan, P.K.; Pan, S.Y.; Kwon, K.H.; Ye, Y.; Chu, J.H.; Fong, W.F.; Tsui, W.M.; Yu, Z.L. ERp57 is up-regulated in free fatty acids-induced steatotic L-02 cells and human nonalcoholic fatty livers. J. Cell. Biochem., 2010, 110(6), 1447-1456.
36. Zhang, X.; Yang, J.; Guo, Y.; Ye, H.; Yu, C.; Xu, C.; Xu, L.; Wu, S.; Sun, W.; Wei, H.; Gao, X.; Zhu, Y., Qian, X.; Jiang, Y.; Li, Y.; He, F. Functional proteomic analysis of nonalcoholic fatty liver disease in rat models: enoyl-coenzyme a hydratase down-regulation exacerbates hepatic steatosis. Hepatology, 2010, 51(4), 1190-1199.
37. Li, H.; Wang, L.; Yan, X.; Liu, Q.; Yu, C.; Wei, H.; Li, Y.; Zhang, X.; He, F.; Jiang, Y. A proton nuclear magnetic resonance metabonomics approach for biomarker discovery in nonalcoholic Fatty liver disease. J. Proteome Res., 2011, 10(6), 2797-2806.
38. Kalhan S.C.; Guo L.; Edmison J.; Dasarathy S.; McCullough AJ.; Hanson RW.; Milburn M. Plasma metabolomic profile in nonalcoholic fatty liver disease. Metabolism, 2011, 60(3), 404-413.
39. Younossi, Z.M.; Jarrar, M.; Nugent, C.; Randhawa, M.; Afendy, M.; Stepanova, M.; Rafiq, N.; Goodman, Z.; Chandhoke, V.; Baranova, A. A novel diagnostic biomarker panel for obesity-related nonalcoholic steatohepatitis (NASH). Obes. Surg., 2008, 18(11), 1430-1437.
40. Younossi, Z.M.; Baranova, A.; Stepanova, M.; Page, S.; Calvert, V.S.; Afendy, A.; Goodman, Z.; Chandhoke, V.; Liotta, L.; Petricoin, E. Phosphoproteomic biomarkers predicting histologic nonalcoholic steatohepatitis and fibrosis. J. Proteome Res., 2010, 9(6), 3218-3224.
41. Trak-Smayra, V.; Dargere, D.; Noun, R.; Albuquerque, M.; Yaghi, C.; Gannagé-Yared, M.H.; Bedossa, P.; Paradis, V. Serum proteomic profiling of obese patients: correlation with liver pathology and evolution after bariatric surgery. Gut, 2009, 58(6), 825-832.
42. Ulukaya, E.; Yilmaz, Y.; Moshkovskii, S.; Karpova, M.; Pyatnitskiy, M.; Atug, O.; Dolar, E. Proteomic analysis of serum in patients with non-alcoholic steatohepatitis using matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Scand. J. Gastroenterol., 2009, 44(12), 1471-1476.
43. Bell, L.N.; Theodorakis, J.L.; Vuppalanchi, R.; Saxena, R.; Bemis, K.G.; Wang, M.: Chalasani, N. Serum proteomics and biomarker discovery across the spectrum of nonalcoholic fatty liver disease. Hepatology, 2010, 51(1), 111-120.
44. Cusi, K. Role of insulin resistance and lipotoxicity in non-alcoholic steatohepatitis. Clin. Liver. Dis., 2009, 13, 545-563.
45. Donnelly, K.L.; Smith, C.I.; Schwarzenberg, S.J.; Jessurun, J.; Boldt, M.D.; Parks, E.J. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J. Clin. Invest., 2005, 115(5), 1343-1351.
46. Cheung, O.; Kapoor, A.; Puri, P.; Sistrun, S.; Luketic, V.A.; Sargeant, C.C.; Contos, M.J.; Shiffman, M.L.; Stravitz, R.T.; Sterling, R.K.; Sanyal, A.J. The impact of fat distribution on the severity of nonalcoholic fatty liver disease and metabolic syndrome. Hepatology, 2007, 46(4), 1091-1100.
47. Malhi, H.; Gores, G.J. Molecular mechanisms of lipotoxicity in nonalcoholic fatty liver disease. Semin. Liver Dis., 2008, 28, 360-369.
48. Gentile, C.L.; Pagliassotti, M.J. The role of fatty acids in the development and progression of nonalcoholic fatty liver disease. J. Nutr. Biochem., 2008, 19, 567-576.
49. Han, M.S.; Park, S.Y.; Shinzawa, K.; Kim, S.; Chung, K.W.; Lee, J.H.; Kwon, C.H.; Lee, K.W.; Lee, J.H.; Park, C.K.; Chung, W.J.; Hwang, J.S.; Yan, J.J.; Song, D.K.; Tsujimoto, Y.; Lee, MS. Lysophosphatidylcholine as a death effector in the lipoapoptosis of hepatocytes. J. Lipid. Res., 2008, 49, 84-97.
50. Puri, P.; Baillie, R.A.; Wiest, M.M.; Mirshahi, F.; Choudhury, J.; Cheung, O.; Sargeant, C.; Contos, M.J.; Sanyal, A.J. A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology, 2007, 46(4), 1081-1090.
51. Araya, J.; Rodrigo, R.; Videla, L.A.; Thielemann, L.; Orellana, M.; Pettinelli, P.; Poniachik, J. Increase in long-chain polyunsaturated fatty acid n - 6/n - 3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clin. Sci. (Lond), 2004, 106(6), 635-643.
52. Feldstein, A.E.; Werneburg, N.W.; Canbay, A.; Guicciardi, M.E.; Bronk, S.F.; Rydzewski, R.; Burgart, L.J.; Gores, G.J. Free fatty acids promote hepatic lipotoxicity by stimulating TNF-alpha expression via a lysosomal pathway. Hepatology, 2004, 40(1), 185-194.
53. Neuschwander-Tetri, B.A.; Caldwell, S.H. Nonalcoholic steatohepatitis: summary of an AASLD Single Topic Conference. Hepatology, 2003, 37(5), 1202-1219.
54. Yao, P.M. and Ira, T. Free cholesterol loading of macrophages is associated with widespread mitochondrial dysfunction and activation of the mitochondrial apoptosis pathway J. Biol. Chem., 2000, 275, 23807-23813.
55. Nair, S.P.; Arnold, C.; Diehl, A.M. Hepatic ATP reserve and efficiency of replenishing: comparison between obese and nonobese normal individuals. Am. J. Gastroenterol., 2003, 98(2), 466-470.
56. Sanyal, A.J.; Campbell-Sargent, C.; Mirshahi, F.; Rizzo, W.B.; Contos, M.J.; Sterling, R.K.; Luketic, V.A.; Shiffman, M.L.; Clore, J.N. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology, 2001, 120(5), 1183-1192.
57. Yao, P.M.; Tabas, I. Free cholesterol loading of macrophages is associated with widespread mitochondrial dysfunction and activation of the mitochondrial apoptosis pathway. J. Biol. Chem., 2001, 276(45), 42468-42476.
58. Duncan, R.E.; El-Sohemy, A.; Archer, M.C. Regulation of HMGCoA reductase in MCF-7 cells by genistein, EPA, and DHA, alone and in combination with mevastatin. Cancer Lett., 2005, 224(2), 221-228.
59. Puri, P.; Wiest, M.M.; Cheung, O.; Mirshahi, F.; Sargeant, C.; Min, H.K.; Contos, M.J.; Sterling, R.K.; Fuchs, M.; Zhou, H.; Watkins, S.M.; Sanyal, A.J. The plasma lipidomic signature of nonalcoholic steatohepatitis. Hepatology, 2009, 50(6), 1827-1838.
60. Bass, N.M.; Merriman, R.B. Fatty acid metabolism and lipotoxicity in the pathogenesis of NASH. In: Non-Alcoholic Steatohepatitis, Farrell GC, George J, Hall P, McCullough AJ, Eds.; Blackwell Publishing: Oxford, UK; pp 109-122, 2005.
61. Cong, W.N.; Tao, R.Y.; Tian, J.Y.; Liu, G.T.; Ye, F. The establishment of a novel non-alcoholic steatohepatitis model accompanied with obesity and insulin resistance in mice. Life Sci., 2008, 82, 983-990.
62. Kallwitz, E.R.; McLachlan, A.; Cotler, S.J. Role of peroxisome proliferatorsactivated receptors in the pathogenesis and treatment of nonalcoholic fatty liver disease. World J. Gastroenterol., 2008, 14, 22-28.
63. Debois, D.; Bralet, M.P.; Le Naour, F.; Brunelle, A.; Laprévote, O. In situ lipidomic analysis of nonalcoholic fatty liver by cluster TOF-SIMS imaging. Anal. Chem., 2009, 81(8), 2823-2831.
64. Le Naour, F.; Bralet, M.P.; Debois, D.; Sandt, C.; Guettier, C.; Dumas, P.; Brunelle, A.; Laprévote, O. Chemical imaging on liver steatosis using synchrotron infrared and ToF-SIMS microspectroscopies. PLoS One, 2009, 4(10), e7408.
65. Tamimi, T.I.; Elgouhari, H.M.; Alkhouri, N.; Yerian, L.M.; Berk, M.P.; Lopez, R.; Schauer, P.R.; Zein, N.N.; Feldstein, A.E. An apoptosis panel for non alcoholic steatohepatitis diagnosis. J. Hepatol., 2011, 54(6), 1224-1229.
66. Tan, B.; Bradshaw, H.B.; Rimmerman, N.; Srinivasan, H.; Yu, Y.W.; Krey, J.F.; Monn, M.F.; Shih-Chieh Chen, J.; Shu-Jung Hu, S.; Pickens, S.R.; Walker, J.M. Targeted Lipidomics: Discovery of New Fatty Acyl Amides. AAPS J., 2006, 8(3), E461-E465.