Atherogenic diets exacerbate colitis in mice deficient in glutathione peroxidase

Inflammatory Bowel Diseases

Volumn 16, Issue 12, 2010, Pages 2043-2054

  Gao, Qiang ^a   Esworthy, R Steven ^a   Kim, Byung Wook ^a   Synold, Timothy W ^a   Smith, David D ^a   Chu, Fong Fong ^a  

^a CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

atherosclerosis; colitis; glutathione peroxidase; hypercholesterolemia; unfolded protein response

Indexed keywords

CHOLIC ACID; GLUTATHIONE PEROXIDASE; GLUTATHIONE PEROXIDASE 1; GLUTATHIONE PEROXIDASE 2; LIPOPOLYSACCHARIDE; SERUM AMYLOID A; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; AORTA; ARTICLE; ATHEROGENIC DIET; ATHEROSCLEROSIS; C57BL 6 MOUSE; CHOLESTEROL DIET; COLITIS; CONTROLLED STUDY; DIET; FEMALE; HYPERCHOLESTEROLEMIA; KNOCKOUT MOUSE; LIPID DIET; MOUSE; NONHUMAN; PRIORITY JOURNAL; TISSUE INJURY;

ANIMALS; ATHEROSCLEROSIS; BLOTTING, WESTERN; CHOLESTEROL; COLITIS; CROHN DISEASE; DEOXYCHOLIC ACID; DIET, ATHEROGENIC; FATTY LIVER; FECES; FEMALE; GAS CHROMATOGRAPHY-MASS SPECTROMETRY; GLUTATHIONE PEROXIDASE; INFLAMMATION; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SURVIVAL RATE; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78649538645     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.21317     Document Type: Article

References (54)

1. Ferguson LR, Shelling AN, Browning BL, et al. Genes, diet and inflammatory bowel disease. Mutat Res. 2007; 622: 70-83.
2. O'sullivan M, O'Morain C,. Nutrition in inflammatory bowel disease. Best Pract Res Clin Gastroenterol. 2006; 20: 561-573.
3. Reif S, Klein I, Lubin F, et al. Pre-illness dietary factors in inflammatory bowel disease. Gut. 1997; 40: 754-760.
4. Ma X, Torbenson M, Hamad AR, et al. High-fat diet modulates non-CD1d-restricted natural killer T cells and regulatory T cells in mouse colon and exacerbates experimental colitis. Clin Exp Immunol. 2008; 151: 130-138.
5. Huang H, Liu T, Rose JL, et al. Sensitivity of mice to lipopolysaccharide is increased by a high saturated fat and cholesterol diet. J Inflamm (Lond). 2007; 4: 22
6. Naura AS, Hans CP, Zerfaoui M, et al. High-fat diet induces lung remodeling in ApoE-deficient mice: an association with an increase in circulatory and lung inflammatory factors. Lab Invest. 2009; 89: 1243-1251.
7. Chu FF, Esworthy RS, Chu PG, et al. Bacteria-induced intestinal cancer in mice with disrupted Gpx1 and Gpx2 genes. Cancer Res. 2004; 64: 962-968.
8. Lee DH, Esworthy RS, Chu C, et al. Mutation accumulation in the intestine and colon of mice deficient in two intracellular glutathione peroxidases. Cancer Res. 2006; 66: 9845-9851.
9. Getz GS, Reardon CA,. Diet and murine atherosclerosis. Arterioscler Thromb Vasc Biol. 2006; 26: 242-249.
10. Lewis P, Stefanovic N, Pete J, et al. Lack of the antioxidant enzyme glutathione peroxidase-1 accelerates atherosclerosis in diabetic apolipoprotein E-deficient mice. Circulation. 2007; 115: 2178-2187.
11. Torzewski M, Ochsenhirt V, Kleschyov AL, et al. Deficiency of glutathione peroxidase-1 accelerates the progression of atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2007; 27: 850-857.
12. Esworthy RS, Mann JR, Sam M, et al. Low glutathione peroxidase activity in Gpx1 knockout mice protects jejunum crypts from gamma-irradiation damage. Am J Physiol Gastrointest Liver Physiol. 2000; 279: G426-G436.
13. de Haan JB, Witting PK, Stefanovic N, et al. Lack of the antioxidant glutathione peroxidase-1 does not increase atherosclerosis in C57BL/J6 mice fed a high-fat diet. J Lipid Res. 2006; 47: 1157-1167.
14. Shimomura I, Bashmakov Y, Shimano H, et al. Cholesterol feeding reduces nuclear forms of sterol regulatory element binding proteins in hamster liver. Proc Natl Acad Sci U S A. 1997; 94: 12354-12359.
15. Field FJ, Born E, Murthy S, et al. Regulation of sterol regulatory element-binding proteins in hamster intestine by changes in cholesterol flux. J Biol Chem. 2001; 276: 17576-17583.
16. Bailey D, O'Hare P,. Transmembrane bZIP transcription factors in ER stress signaling and the unfolded protein response. Antioxid Redox Signal. 2007; 9: 2305-2321.
17. Brandl K, Rutschmann S, Li X, et al. Enhanced sensitivity to DSS colitis caused by a hypomorphic Mbtps1 mutation disrupting the ATF6-driven unfolded protein response. Proc Natl Acad Sci U S A. 2009; 106: 3300-3305.
18. Friedman G, Ben-Yehuda A, Dabach Y, et al. Macrophage cholesterol metabolism, apolipoprotein E, and scavenger receptor AI/II mRNA in atherosclerosis-susceptible and -resistant mice. Arterioscler Thromb Vasc Biol. 2000; 20: 2459-2464.
19. Whitman SC,. A Practical Approach to Using Mice in Atherosclerosis Research. Clin Biochem Rev. 2004; 25: 81-93.
20. Paigen B, Morrow A, Holmes PA, et al. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 1987; 68: 231-240.
21. Brunt EM, Janney CG, Di Bisceglie AM, et al. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. [see comment]. Am J Gastroenterol. 1999; 94: 2467-2474.
22. Ozcan E, Garibyan L, Lee JJ, et al. Transmembrane activator, calcium modulator, and cyclophilin ligand interactor drives plasma cell differentiation in LPS-activated B cells. J Allergy Clin Immunol. 2009; 123: 1277-1286.
23. Zinszner H, Kuroda M, Wang X, et al. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998; 12: 982-995.
24. Reigstad CS, Lunden GO, Felin J, et al. Regulation of serum amyloid A3 (SAA3) in mouse colonic epithelium and adipose tissue by the intestinal microbiota. PloS One. 2009; 4: e5842.
25. Kasbo J, Saleem M, Perwaiz S, et al. Biliary, fecal and plasma deoxycholic acid in rabbit, hamster, guinea pig, and rat: comparative study and implication in colon cancer. Biol Pharm Bull. 2002; 25: 1381-1384.
26. Vergnes L, Phan J, Strauss M, et al. Cholesterol and cholate components of an atherogenic diet induce distinct stages of hepatic inflammatory gene expression. J Biol Chem. 2003; 278: 42774-42784.
27. Figge A, Lammert F, Paigen B, et al. Hepatic overexpression of murine Abcb11 increases hepatobiliary lipid secretion and reduces hepatic steatosis. J Biol Chem. 2004; 279: 2790-2799.
28. Goel R, Boylan B, Gruman L, et al. The proinflammatory phenotype of PECAM-1-deficient mice results in atherogenic diet-induced steatohepatitis. Am J Physiol Gastrointest Liver Physiol. 2007; 293: G1205-G1214.
29. Hengstermann A, Muller T,. Endoplasmic reticulum stress induced by aqueous extracts of cigarette smoke in 3T3 cells activates the unfolded-protein-response-dependent PERK pathway of cell survival. Free Radic Biol Med. 2008; 44: 1097-1107.
30. Scheja L, Heese B, Zitzer H, et al. Acute-phase serum amyloid A as a marker of insulin resistance in mice. Exp Diabetes Res. 2008; 2008: 230837.
31. Bernstein H, Holubec H, Bernstein C, et al. Unique dietary-related mouse model of colitis. Inflamm Bowel Dis. 2006; 12: 278-293.
32. Geerling BJ, Dagnelie PC, Badart-Smook A, et al. Diet as a risk factor for the development of ulcerative colitis. Am J Gastroenterol. 2000; 95: 1008-1013.
33. Li H, Lelliott C, Hakansson P, et al. Intestinal, adipose, and liver inflammation in diet-induced obese mice. Metab Clin Exp. 2008; 57: 1704-1710.
34. Chapman-Kiddell CA, Davies PS, Gillen L, et al. Role of diet in the development of inflammatory bowel disease. Inflamm Bowel Dis. 2009; 16: 15.
35. Wang DQ, Lammert F, Cohen DE, et al. Cholic acid aids absorption, biliary secretion, and phase transitions of cholesterol in murine cholelithogenesis. Am J Physiol. 1999; 276: G751-G760.
36. Esworthy RS, Aranda R, Martin MG, et al. Mice with combined disruption of Gpx1 and Gpx2 genes have colitis. Am J Physiol Gastrointest Liver Physiol. 2001; 281: G848-G855.
37. Lin JA, Watanabe J, Rozengurt N, et al. Atherogenic diet causes lethal ileo-ceco-colitis in cyclooxygenase-2 deficient mice. Prostaglandins Other Lipid Mediat. 2007; 84: 98-107.
38. Paradkar PN, Blum PS, Berhow MA, et al. Dietary isoflavones suppress endotoxin-induced inflammatory reaction in liver and intestine. Cancer Lett. 2004; 215: 21-28.
39. Bertolotti A, Wang X, Novoa I, et al. Increased sensitivity to dextran sodium sulfate colitis in IRE1beta-deficient mice. J Clin Invest. 2001; 107: 585-593.
40. Kaser A, Lee AH, Franke A, et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell. 2008; 134: 743-756.
41. Tu BP, Weissman JS,. Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol. 2004; 164: 341-346.
42. Ron D, Walter P,. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev. 2007; 8: 519-529.
43. Ma A,. Unresolved ER stress inflames the intestine. Cell. 2008; 134: 724-725.
44. Iwakoshi NN, Lee AH, Vallabhajosyula P, et al. Plasma cell differentiation and the unfolded protein response intersect at the transcription factor XBP-1. Nat Immunol. 2003; 4: 321-329.
45. Latiano A, Palmieri O, Corritore G, et al. Variants at the 3p21 locus influence susceptibility and phenotype both in adults and early-onset patients with inflammatory bowel disease. Inflamm Bowel Dis. 2009 [Epub ahead of print].
46. Esworthy RS, Binder SW, Doroshow JH, et al. Microflora trigger colitis in mice deficient in selenium-dependent glutathione peroxidase and induce Gpx2 gene expression. Biol Chem. 2003; 384: 597-607.
47. Esworthy RS, Yang L, Frankel PH, et al. Epithelium-specific glutathione peroxidase, Gpx2, is involved in the prevention of intestinal inflammation in selenium-deficient mice. J Nutr. 2005; 135: 740-745.
48. Jones BV, Begley M, Hill C, et al. Functional and comparative metagenomic analysis of bile salt hydrolase activity in the human gut microbiome. Proc Natl Acad Sci U S A. 2008; 105: 13580-13585.
49. Ortega-Cava CF, Ishihara S, Rumi MA, et al. Strategic compartmentalization of Toll-like receptor 4 in the mouse gut. J Immunol. 2003; 170: 3977-3985.
50. Davis CP, Cleven D, Balish E, et al. Bacterial association in the gastrointestinal tract of beagle dogs. Appl Environ Microbiol. 1977; 34: 194-206.
51. Cani PD, Neyrinck AM, Fava F, et al. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia. 2007; 50: 2374-2383.
52. Martinez I, Wallace G, Zhang C, et al. Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota. Appl Environ Microbiol. 2009; 75: 4175-4184.
53. Bernstein H, Holubec H, Bernstein C, et al. Deoxycholate-induced colitis is markedly attenuated in Nos2 knockout mice in association with modulation of gene expression profiles. Dig Dis Sci. 2007; 52: 628-642.
54. Adachi Y, Yamamoto K, Okada T, et al. ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct Funct. 2008; 33: 75-89.