Table of Contents
ISRN Oxidative Medicine
Volume 2014, Article ID 659029, 7 pages
http://dx.doi.org/10.1155/2014/659029
Research Article

Heme Consumption Reduces Hepatic Triglyceride and Fatty Acid Accumulation in a Rat Model of NAFLD Fed Westernized Diet

1Department of Biochemistry, Yong Loo Lin School of Medicine, National University of Singapore, 28 Medical Drive, Singapore 117456
2Institute for Translational Medicine and Therapeutics, 3400 Civic Center Boulevard Building 421, University of Pennsylvania, Philadelphia, PA 19104, USA
3School of Biological Sciences, Illawarra Health and Medical Research Institute, Building 32, University of Wollongong, Wollongong, NSW 2522, Australia

Received 28 October 2013; Accepted 15 December 2013; Published 9 January 2014

Academic Editors: C. J. Lieven, A. B. Salmon, A. Shukla, and E. L. Streck

Copyright © 2014 Soon Yew Tang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. J. McCullough, “Pathophysiology of nonalcoholic steatohepatitis,” Journal of Clinical Gastroenterology, vol. 40, supplement 1, pp. S17–S29, 2006. View at Publisher · View at Google Scholar · View at Scopus
  2. K. Das, K. Das, P. S. Mukherjee et al., “Nonobese population in a developing country has a high prevalence of nonalcoholic fatty liver and significant liver disease,” Hepatology, vol. 51, no. 5, pp. 1593–1602, 2010. View at Publisher · View at Google Scholar · View at Scopus
  3. S. Fargion, M. Mattioli, A. L. Fracanzani et al., “Hyperferritinemia, iron overload, and multiple metabolic alterations identify patients at risk for nonalcoholic steatohepatitis,” American Journal of Gastroenterology, vol. 96, no. 8, pp. 2448–2455, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. V. Trak-Smayra, D. Dargere, R. Noun et al., “Serum proteomic profiling of obese patients: correlation with liver pathology and evolution after bariatric surgery,” Gut, vol. 58, no. 6, pp. 825–832, 2009. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Xu, C.-F. Xu, C.-H. Yu, M. Miao, and Y.-M. Li, “Haemoglobin and non-alcoholic fatty liver disease: further evidence from a population-based study,” Gut, vol. 58, no. 12, pp. 1706–1707, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. C. Yu, C. Xu, L. Xu, J. Yu, M. Miao, and Y. Li, “Serum proteomic analysis revealed diagnostic value of hemoglobin for nonalcoholic fatty liver disease,” Journal of Hepatology, vol. 56, no. 1, pp. 241–247, 2012. View at Publisher · View at Google Scholar · View at Scopus
  7. C. P. Day and O. F. W. James, “Steatohepatitis: a tale of two ‘Hits’?” Gastroenterology, vol. 114, no. 4, pp. 842–845, 1998. View at Publisher · View at Google Scholar · View at Scopus
  8. A. P. Rolo, J. S. Teodoro, and C. M. Palmeira, “Role of oxidative stress in the pathogenesis of nonalcoholic steatohepatitis,” Free Radical Biology and Medicine, vol. 52, no. 1, pp. 59–69, 2012. View at Publisher · View at Google Scholar · View at Scopus
  9. C. S. Lieber, M. A. Leo, K. M. Mak et al., “Model of nonalcoholic steatohepatitis,” American Journal of Clinical Nutrition, vol. 79, no. 3, pp. 502–509, 2004. View at Google Scholar · View at Scopus
  10. S. K. Mantena, D. P. Vaughn Jr., K. K. Andringa et al., “High fat diet induces dysregulation of hepatic oxygen gradients and mitochondrial function in vivo,” Biochemical Journal, vol. 417, no. 1, pp. 183–193, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. G. L. Tipoe, C. T. Ho, E. C. Liong et al., “Voluntary oral feeding of rats not requiring a very high fat diet is a clinically relevant animal model of non-alcoholic fatty liver disease (NAFLD),” Histology and Histopathology, vol. 24, no. 9, pp. 1161–1169, 2009. View at Google Scholar · View at Scopus
  12. A. Kennedy, K. Martinez, C. Chuang, K. Lapoint, and M. Mcintosh, “Saturated fatty acid-mediated inflammation and insulin resistance in adipose tissue: mechanisms of action and implications,” Journal of Nutrition, vol. 139, no. 1, pp. 1–4, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Kaser, C. F. Ebenbichler, and H. Tilg, “Pharmacological and non-pharmacological treatment of non-alcoholic fatty liver disease,” International Journal of Clinical Practice, vol. 64, no. 7, pp. 968–983, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. M. Dhibi, F. Brahmi, A. Mnari et al., “The intake of high fat diet with different trans fatty acid levels differentially induces oxidative stress and non alcoholic fatty liver disease (NAFLD) in rats,” Nutrition and Metabolism, vol. 8, pp. 65–76, 2011. View at Publisher · View at Google Scholar · View at Scopus
  15. M. S. Jacobson, “Cholesterol oxides in Indian ghee: possible cause of unexplained high risk of atherosclerosis in Indian immigrant populations,” The Lancet, vol. 2, no. 8560, pp. 656–658, 1987. View at Google Scholar · View at Scopus
  16. A. Pan, Q. Sun, A. M. Bernstein et al., “Red meat consumption and mortality: results from 2 prospective cohort studies,” Archives of Internal Medicine, vol. 172, no. 7, pp. 555–563, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Puppo and B. Halliwell, “Formation of hydroxyl radicals from hydrogen peroxide in the presence of iron. Is haemoglobin a biological Fenton reagent?” Biochemical Journal, vol. 249, no. 1, pp. 185–190, 1988. View at Google Scholar · View at Scopus
  18. B. Halliwell and J. M. C. Gutteridge, Free Radicals in Biology and Medicine, Clarendon Press, Oxford, UK, 2007.
  19. W. Liu, S. S. Baker, R. D. Baker, N. J. Nowak, and L. Zhu, “Upregulation of hemoglobin expression by oxidative stress in hepatocytes and its implication in nonalcoholic steatohepatitis,” PLoS ONE, vol. 6, no. 9, Article ID e24363, 2011. View at Publisher · View at Google Scholar · View at Scopus
  20. H. Nishi, R. Inagi, H. Kato et al., “Hemoglobin is expressed by mesangial cells and reduces oxidant stress,” Journal of the American Society of Nephrology, vol. 19, no. 8, pp. 1500–1508, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. C. C. Widmer, C. P. Pereira, P. Gehrig et al., “Hemoglobin can attenuate hydrogen peroxide-induced oxidative stress by acting as an antioxidative peroxidase,” Antioxidants and Redox Signaling, vol. 12, no. 2, pp. 185–198, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. W. M. J. Butler, H. M. Maling, M. G. Horning et al., “The direct determination of liver triglycerides,” Journal of Lipid Research, vol. 2, pp. 95–96, 1961. View at Google Scholar
  23. J. F. Woessner Jr., “The determination of hydroxyproline in tissue and protein samples containing small proportions of this imino acid,” Archives of Biochemistry and Biophysics, vol. 93, no. 2, pp. 440–447, 1961. View at Google Scholar · View at Scopus
  24. A. Jenner, M. Ren, R. Rajendran et al., “Zinc supplementation inhibits lipid peroxidation and the development of atherosclerosis in rabbits fed a high cholesterol diet,” Free Radical Biology and Medicine, vol. 42, no. 4, pp. 559–566, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. A. A. Nanji, “Animal models of nonalcoholic fatty liver disease and steatohepatitis,” Clinics in Liver Disease, vol. 8, no. 3, pp. 559–574, 2004. View at Publisher · View at Google Scholar · View at Scopus
  26. U. Riserus, “Fatty acids and insulin sensitivity,” Current Opinion in Clinical Nutrition & Metabolic Care, vol. 11, pp. 100–105, 2008. View at Publisher · View at Google Scholar
  27. J. E. Galgani, R. D. Uauy, C. A. Aguirre, and E. O. Díaz, “Effect of the dietary fat quality on insulin sensitivity,” British Journal of Nutrition, vol. 100, no. 3, pp. 471–479, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Kubow, “Routes of formation and toxic consequences of lipid oxidation products in foods,” Free Radical Biology and Medicine, vol. 12, no. 1, pp. 63–81, 1992. View at Publisher · View at Google Scholar · View at Scopus
  29. J. Westerbacka, K. Lammi, A. Häkkinen et al., “Dietary fat content modifies liver fat in overweight nondiabetic subjects,” Journal of Clinical Endocrinology and Metabolism, vol. 90, no. 5, pp. 2804–2809, 2005. View at Publisher · View at Google Scholar · View at Scopus
  30. K. L. Donnelly, C. I. Smith, S. J. Schwarzenberg, J. Jessurun, M. D. Boldt, and E. J. Parks, “Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease,” Journal of Clinical Investigation, vol. 115, no. 5, pp. 1343–1351, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. V. T. Samuel, Z. Liu, X. Qu et al., “Mechanism of hepatic insulin resistance in non-alcoholic fatty liver disease,” Journal of Biological Chemistry, vol. 279, no. 31, pp. 32345–32353, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. E. Vanni, E. Bugianesi, A. Kotronen, S. De Minicis, H. Yki-Järvinen, and G. Svegliati-Baroni, “From the metabolic syndrome to NAFLD or vice versa?” Digestive and Liver Disease, vol. 42, no. 5, pp. 320–330, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. L. Juurinen, M. Tiikkainen, A. Häkkinen, A. Hakkarainen, and H. Yki-Järvinen, “Effects of insulin therapy on liver fat content and hepatic insulin sensitivity in patients with type 2 diabetes,” American Journal of Physiology, vol. 292, no. 3, pp. E829–E835, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. G. C. Ness, R. C. Holland, and D. Lopez, “Selective compensatory induction of hepatic HMG-CoA reductase in response to inhibition of cholesterol absorption,” Experimental Biology and Medicine, vol. 231, no. 5, pp. 559–565, 2006. View at Google Scholar · View at Scopus
  35. L. R. Boone, P. A. Brooks, M. I. Niesen et al., “Mechanism of resistance to dietary cholesterol,” Journal of Lipids, vol. 2011, Article ID 101242, 9 pages, 2011. View at Publisher · View at Google Scholar
  36. W. Y. Ong, A. M. Jenner, N. Pan, C. Ong, and B. Halliwell, “Elevated oxidative stress, iron accumulation around microvessels and increased 4-hyroxynonenal immunostainig in zone 1 of the liver acinus in hypercholesterolemic rabbits,” Free Radical Research, vol. 43, no. 3, pp. 241–249, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Lettéron, B. Fromenty, B. Terris, C. Degott, and D. Pessayre, “Acute and chronic hepatic steatosis lead to in vivo lipid peroxidation in mice,” Journal of Hepatology, vol. 24, no. 2, pp. 200–208, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. I. Staprans, X. Pan, J. H. Rapp, and K. R. Feingold, “The role of dietary oxidized cholesterol and oxidized fatty acids in the development of atherosclerosis,” Molecular Nutrition and Food Research, vol. 49, no. 11, pp. 1075–1082, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. L. Valenti, A. L. Fracanzani, P. Dongiovanni et al., “Iron depletion by phlebotomy improves insulin resistance in patients with nonalcoholic fatty liver disease and hyperferritinemia: evidence from a case-control study,” American Journal of Gastroenterology, vol. 102, no. 6, pp. 1251–1258, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. E. Aigner, I. Theurl, M. Theurl et al., “Pathways underlying iron accumulation in human nonalcoholic fatty liver disease,” American Journal of Clinical Nutrition, vol. 87, no. 5, pp. 1374–1383, 2008. View at Google Scholar · View at Scopus