Glycine protects against high sucrose and high fat-induced non-alcoholic steatohepatitis in rats

Oncotarget

Volumn 7, Issue 49, 2016, Pages 80223-80237

  Zhou, Xin ^a   Han, Dewu ^a   Xu, Ruiling ^a   Wu, Huiwen ^a   Qu, Chongxiao ^b   Wang, Feng ^a   Wang, Xiangyu ^a   Zhao, Yuanchang ^a  

^a SHANXI MEDICAL UNIVERSITY   (China)

^b SHAANXI PROVINCIAL PEOPLE S HOSPITAL   (China)

Author keywords

Endoplasmic reticulum stress; Glycine; Intestinal endotoxin; Non alcoholic steatohepatitis; Oxidative stress; Pathology Section

Indexed keywords

ALANINE AMINOTRANSFERASE; CD68 ANTIGEN; ENDOTOXIN; FATTY ACID; GLUCOSE REGULATED PROTEIN 78; GLYCINE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; I KAPPA B KINASE BETA; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE OXYGEN METABOLITE; SUCROSE; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR; ANTIOXIDANT; AUTACOID; BIOLOGICAL MARKER;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL INFILTRATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; INFLAMMATORY CELL; INSULIN RESISTANCE INDEX; LIPID BLOOD LEVEL; LIPID DIET; LIVER CELL; LIVER HISTOLOGY; MALE; MEDICAL PARAMETERS; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; ANIMAL; BLOOD; CELL PROTECTION; DISEASE MODEL; DRUG EFFECTS; ENDOTOXEMIA; LIVER; MACROPHAGE; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; SUGAR INTAKE; TIME FACTOR;

ANIMALS; ANTIOXIDANTS; APOPTOSIS; BIOMARKERS; CYTOPROTECTION; DIET, HIGH-FAT; DIETARY SUCROSE; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; ENDOTOXEMIA; ENDOTOXINS; GLYCINE; HEPATOCYTES; INFLAMMATION MEDIATORS; LIVER; MACROPHAGES; MALE; NON-ALCOHOLIC FATTY LIVER DISEASE; OXIDATIVE STRESS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TIME FACTORS;

EID: 85001114564     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.12831     Document Type: Article

References (42)

1. Organization WH. (2012). Obesity and Overweight Fact Sheet No.311. (Geneva: World Health Organization).
2. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science. 2011; 332: 1519-23. doi: 10.1126/science.1204265.
3. Tarantino G, Saldalamacchia G, Conca P, Arena A. Non-alcoholic fatty liver disease: further expression of the metabolic syndrome. J Gastroenterol Hepatol. 2007; 22: 293-303. doi: 10.1111/j.1440-1746.2007.04824.x.
4. Smith BW, Adams LA. Non-alcoholic fatty liver disease. Crit Rev Clin Lab Sci. 2011; 48: 97-113. doi: 10.3109/10408363.2011.596521.
5. Argo CK, Northup PG, Al-Osaimi AM, Caldwell SH. Systematic review of risk factors for fibrosis progression in non-alcoholic steatohepatitis. J Hepatol. 2009; 51: 371-9. doi: 10.1016/j.jhep.2009.03.019.
6. Henao-Mejia J, Elinav E, Jin C, Hao L, Mehal WZ, Strowig T, Thaiss CA, Kau AL, Eisenbarth SC, Jurczak MJ, Camporez JP, Shulman GI, Gordon JI, et al. Inflammasome-mediated dysbiosis regulates progression of NAFLD and obesity. Nature. 2012; 482: 179-85. doi: 10.1038/nature10809.
7. Day CP, James OF. Steatohepatitis: a tale of two "hits"? Gastroenterology. 1998; 114: 842-5.
8. Sanyal AJ, Campbell-Sargent C, Mirshahi F, Rizzo WB, Contos MJ, Sterling RK, Luketic VA, Shiffman ML, Clore JN. Nonalcoholic steatohepatitis: association of insulin resistance and mitochondrial abnormalities. Gastroenterology. 2001; 120: 1183-92. doi: 10.1053/gast.2001.23256.
9. Zhang XQ, Xu CF, Yu CH, Chen WX, Li YM. Role of endoplasmic reticulum stress in the pathogenesis of nonalcoholic fatty liver disease. World J Gastroenterol. 2014; 20: 1768-76. doi: 10.3748/wjg.v20.i7.1768.
10. Harte AL, da Silva NF, Creely SJ, McGee KC, Billyard T, Youssef-Elabd EM, Tripathi G, Ashour E, Abdalla MS, Sharada HM, Amin AI, Burt AD, Kumar S, et al. Elevated endotoxin levels in non-alcoholic fatty liver disease. J Inflamm (Lond). 2010; 7: 15. doi: 10.1186/1476-9255-7-15.
11. Brun P, Castagliuolo I, Di Leo V, Buda A, Pinzani M, Palu G, Martines D. Increased intestinal permeability in obese mice: new evidence in the pathogenesis of nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol. 2007; 292: G518-25. doi: 10.1152/ajpgi.00024.2006.
12. Kadiiska MB, Peddada S, Herbert RA, Basu S, Hensley K, Jones DP, Hatch GE, Mason RP. Biomarkers of oxidative stress study VI. Endogenous plasma antioxidants fail as useful biomarkers of endotoxin-induced oxidative stress. Free Radic Biol Med. 2015; 81: 100-6. doi: 10.1016/j.freeradbiomed.2015.01.006.
13. Coope A, Milanski M, Arruda AP, Ignacio-Souza LM, Saad MJ, Anhe GF, Velloso LA. Chaperone insufficiency links TLR4 protein signaling to endoplasmic reticulum stress. J Biol Chem. 2012; 287: 15580-9. doi: 10.1074/jbc.M111.315218.
14. Ishizaki-Koizumi S, Sonaka I, Takei Y, Ikejima K, Sato N. The glycine analogue, aminomethanesulfonic acid, inhibits LPS-induced production of TNF-alpha in isolated rat Kupffer cells and exerts hepatoprotective effects in mice. Biochem Biophys Res Commun. 2004; 322: 514-9. doi: 10.1016/j.bbrc.2004.07.147.
15. Xu FL, You HB, Li XH, Chen XF, Liu ZJ, Gong JP. Glycine attenuates endotoxin-induced liver injury by downregulating TLR4 signaling in Kupffer cells. Am J Surg. 2008; 196: 139-48. doi: 10.1016/j.amjsurg.2007.09.045.
16. Zhou X, Han D, Xu R, Li S, Wu H, Qu C, Wang F, Wang X, Zhao Y. A model of metabolic syndrome and related diseases with intestinal endotoxemia in rats fed a high fat and high sucrose diet. PLoS One. 2014; 9: e115148. doi: 10.1371/journal.pone.0115148.
17. Verdam FJ, Rensen SS, Driessen A, Greve JW, Buurman WA. Novel evidence for chronic exposure to endotoxin in human nonalcoholic steatohepatitis. J Clin Gastroenterol. 2011; 45: 149-52. doi: 10.1097/MCG.0b013e3181e12c24.
18. Sabate JM, Jouet P, Harnois F, Mechler C, Msika S, Grossin M, Coffin B. High prevalence of small intestinal bacterial overgrowth in patients with morbid obesity: a contributor to severe hepatic steatosis. Obes Surg. 2008; 18: 371-7. doi: 10.1007/s11695-007-9398-2.
19. Miele L, Valenza V, La Torre G, Montalto M, Cammarota G, Ricci R, Masciana R, Forgione A, Gabrieli ML, Perotti G, Vecchio FM, Rapaccini G, Gasbarrini G, et al. Increased intestinal permeability and tight junction alterations in nonalcoholic fatty liver disease. Hepatology. 2009; 49: 1877-87. doi: 10.1002/hep.22848.
20. Lichtman SN, Keku J, Schwab JH, Sartor RB. Hepatic injury associated with small bowel bacterial overgrowth in rats is prevented by metronidazole and tetracycline. Gastroenterology. 1991; 100: 513-9.
21. Wigg AJ, Roberts-Thomson IC, Dymock RB, McCarthy PJ, Grose RH, Cummins AG. The role of small intestinal bacterial overgrowth, intestinal permeability, endotoxaemia, and tumour necrosis factor alpha in the pathogenesis of non-alcoholic steatohepatitis. Gut. 2001; 48: 206-11.
22. Shanab AA, Scully P, Crosbie O, Buckley M, O'Mahony L, Shanahan F, Gazareen S, Murphy E, Quigley EM. Small intestinal bacterial overgrowth in nonalcoholic steatohepatitis: association with toll-like receptor 4 expression and plasma levels of interleukin 8. Dig Dis Sci. 2011; 56: 1524-34. doi: 10.1007/s10620-010-1447-3.
23. Arslan N. Obesity, fatty liver disease and intestinal microbiota. World J Gastroenterol. 2014; 20: 16452-63. doi: 10.3748/wjg.v20.i44.16452.
24. Cubero FJ, Trautwein C, 2011. 5(4): p. 427-435. (2011). Oxidative Stress and Liver Injury. Molecular Pathology of Liver Diseases, pp. 427-35.
25. Alhusaini S, McGee K, Schisano B, Harte A, McTernan P, Kumar S, Tripathi G. Lipopolysaccharide, high glucose and saturated fatty acids induce endoplasmic reticulum stress in cultured primary human adipocytes: Salicylate alleviates this stress. Biochem Biophys Res Commun. 2010; 397: 472-8. doi: 10.1016/j.bbrc.2010.05.138.
26. Wheeler MD. Endotoxin and Kupffer cell activation in alcoholic liver disease. Alcohol Res Health. 2003; 27: 300-6. doi:
27. Zu L, He J, Jiang H, Xu C, Pu S, Xu G. Bacterial endotoxin stimulates adipose lipolysis via toll-like receptor 4 and extracellular signal-regulated kinase pathway. J Biol Chem. 2009; 284: 5915-26. doi: 10.1074/jbc.M807852200.
28. Mitsuyoshi H, Itoh Y, Okanoue T. [Role of oxidative stress in non-alcoholic steatohepatitis]. Nihon Rinsho. 2006; 64: 1077-82. doi:
29. Schroder M. Endoplasmic reticulum stress responses. Cell Mol Life Sci. 2008; 65: 862-94. doi: 10.1007/s00018-007-7383-5.
30. Hiramatsu N, Kasai A, Hayakawa K, Yao J, Kitamura M. Real-time detection and continuous monitoring of ER stress in vitro and in vivo by ES-TRAP: evidence for systemic, transient ER stress during endotoxemia. Nucleic Acids Res. 2006; 34: e93. doi: 10.1093/nar/gkl515.
31. Hotamisligil GS. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell. 2010; 140: 900-17. doi: 10.1016/j.cell.2010.02.034.
32. Schroder M, Sutcliffe L. Consequences of stress in the secretory pathway: The ER stress response and its role in the metabolic syndrome. Methods Mol Biol. 2010; 648: 43-62. doi: 10.1007/978-1-60761-756-3_3.
33. Itsumi M, Inoue S, Elia AJ, Murakami K, Sasaki M, Lind EF, Brenner D, Harris IS, Chio, II, Afzal S, Cairns RA, Cescon DW, Elford AR, et al. Idh1 protects murine hepatocytes from endotoxin-induced oxidative stress by regulating the intracellular NADP(+)/NADPH ratio. Cell Death Differ. 2015; 22: 1837-45. doi: 10.1038/cdd.2015.38.
34. Lebeaupin C, Proics E, de Bieville CH, Rousseau D, Bonnafous S, Patouraux S, Adam G, Lavallard VJ, Rovere C, Le Thuc O, Saint-Paul MC, Anty R, Schneck AS, et al. ER stress induces NLRP3 inflammasome activation and hepatocyte death. Cell Death Dis. 2015; 6: e1879. doi: 10.1038/cddis.2015.248.
35. Kim HJ, Jeong JS, Kim SR, Park SY, Chae HJ, Lee YC. Inhibition of endoplasmic reticulum stress alleviates lipopolysaccharide-induced lung inflammation through modulation of NF-kappaB/HIF-1alpha signaling pathway. Sci Rep. 2013; 3: 1142. doi: 10.1038/srep01142.
36. Yang S, Koo DJ, Chaudry IH, Wang P. Glycine attenuates hepatocellular depression during early sepsis and reduces sepsis-induced mortality. Crit Care Med. 2001; 29: 1201-6. doi:
37. Ikejima K, Iimuro Y, Forman DT, Thurman RG. A diet containing glycine improves survival in endotoxin shock in the rat. Am J Physiol. 1996; 271: G97-103.
38. Liu J, Han D, Xu R, Zhao Y. [Effect of glycine on the expression of CD(14) gene and protein of hepatic tissue in the course of developing cirrhosis of rats]. Zhonghua Gan Zang Bing Za Zhi. 2002; 10: 181-4.
39. Pal PB, Pal S, Das J, Sil PC. Modulation of mercury-induced mitochondria-dependent apoptosis by glycine in hepatocytes. Amino Acids. 2012; 42: 1669-83. doi: 10.1007/s00726-011-0869-3.
40. Ruiz-Ramirez A, Ortiz-Balderas E, Cardozo-Saldana G, Diaz-Diaz E, El-Hafidi M. Glycine restores glutathione and protects against oxidative stress in vascular tissue from sucrose-fed rats. Clin Sci (Lond). 2014; 126: 19-29. doi: 10.1042/CS20130164.
41. El Hafidi M, Perez I, Zamora J, Soto V, Carvajal-Sandoval G, Banos G. Glycine intake decreases plasma free fatty acids, adipose cell size, and blood pressure in sucrose-fed rats. Am J Physiol Regul Integr Comp Physiol. 2004; 287: R1387-93. doi: 10.1152/ajpregu.00159.2004.
42. Hsieh PS. Inflammatory change of fatty liver induced by intraportal low-dose lipopolysaccharide infusion deteriorates pancreatic insulin secretion in fructose-induced insulin-resistant rats. Liver Int. 2008; 28: 1167-75. doi: 10.1111/j.1478-3231.2008.01714.x.