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Biotechnology and Bioprocess Engineering

, Volume 20, Issue 4, pp 775–793 | Cite as

Hepatic proteome and its network response to supplementation of an anti-obesity herbal mixture in diet-induced obese mice

  • Sang Woo Kim
  • Tae-Jun Park
  • Harmesh N. Chaudhari
  • Jae Heon Choi
  • Ji-Young Choi
  • Ye Jin Kim
  • Myung-Sook ChoiEmail author
  • Jong Won YunEmail author
Research Paper

Abstract

In the present study, we investigated the effects of multi-herbal water extract mixture, Taeumjowi-tang (TH) on liver proteome alteration in mice using twodimensional electrophoresis combined with MALDI-TOFMS. Animals were fed high-fat diet with or without TH (0.3% wt/wt) supplement for 12 weeks. At the end of 5th week of experimental diet, mice fed high-fat diet only were subdivided into 2 groups, obesity-prone (OP) and obesityresistant (OR) mice based on weight gain. OR mice gained less body weight compared to OP mice despite of same food intake. TH significantly suppressed weight gain, and proteomic analysis enabled the identification of 49 liver proteins showing differential regulation between OP and OR/TH mice. Combined results of proteomic and western blot analyses revealed decreased lipogenesis via three fatty acid metabolic targets (AMPK, ACC, and FAS) in livers of OR and TH mice. Using bioinformatic classification and network analysis, most of the identified proteins were classified as hydrolases, oxidoreductases, transferases, defense/immunity proteins, and enzyme modulators based on functional analysis of the PANTHER classification system. Combined results of proteomic and bioinformatic analyses using GeneMANIA identified two proteins (LACTB2 and NIT2) in the liver that potentially interact with fatty acid metabolic proteins. Furthermore, these proteins were included in acetylation, phosphoprotein, and metabolic processes in DAVID classification. These proteins were highly expressed in OP mice; however both their transcription and protein expression were lowered by TH treatment. In conclusion, combined data from proteomic and network analyses suggest that TH exerts anti-obesity effects by modulating fatty acid metabolic proteins/genes, particularly via the AMPK pathway. Most targeted proteins/ genes were modulated toward enhancing lipid metabolism in response to TH treatment.

Keywords

anti-obesity obesity susceptibility obesity resistance proteome liver 

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References

  1. 1.
    Nakamuta, M., M. Kohjima, N. Higuchi, M. Kato, K. Kotoh, T. Yoshimoto, M. Yada, R. Yada, R. Takemoto, K. Fukuizumi, N. Harada, A. Taketomi, Y. Maehara, M. Nakashima, and M. Enjoji (2008) The significance of differences in fatty acid metabolism between obese and non-obese patients with non-alcoholic fatty liver disease. Int. J. Mol. Med. 22: 663–667.Google Scholar
  2. 2.
    Fabbrini, E., S. Sullivan, and S. Klein (2010) Obesity and nonalcoholic fatty liver disease: Biochemical, metabolic, and clinical implications. Hepatol. 51: 679–689.CrossRefGoogle Scholar
  3. 3.
    Lu, Y., W. Xi, X. Ding, S. Fan, Y. Zhang, D. Jiang, Y. Li, C. Huang, and Z. Zhou (2013) Citrange fruit extracts alleviate obesity-associated metabolic disorder in high-fat diet-induced obese C57BL/6 mouse. Int. J. Mol. Sci. 14: 23736–23750.CrossRefGoogle Scholar
  4. 4.
    Carmiel-Haggai, M., A. I. Cederbaum, and N. Nieto (2005) A high-fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats. FASEB J. 19: 136–138.Google Scholar
  5. 5.
    Seppala-Lindroos, A., S. Vehkavaara, A. M. Hakkinen, T. Goto, J. Westerbacka, A. Sovijarvi, J. Halavaara, and H. Yki-Jarvinen (2002) Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J. Clin. Endocrinol. Metab. 87: 3023–3028.CrossRefGoogle Scholar
  6. 6.
    Westerbacka, J., K. Lammi, A. M. Hakkinen, A. Rissanen, I. Salminen, A. Aro, and H. Yki-Jarvinen (2005) Dietary fat content modifies liver fat in overweight nondiabetic subjects. J. Clin. Endocrinol. Metab. 90: 2804–2809.CrossRefGoogle Scholar
  7. 7.
    Sim, M. -O., H. -I. Lee, J. R. Ham, K. -I. Seo, and M. -K. Lee (2015) Long-term supplementation of esculetin ameliorates hepatosteatosis and insulin resistance partly by activating AdipoR2-AMPK pathway in diet-induced obese mice. J. Funct. Foods. 15: 160–171.CrossRefGoogle Scholar
  8. 8.
    Mokiran, N. N., A. Ismail, A. Azlan, M. Hamid, and F. A. Hassan (2014) Effect of dabai (Canarium odontophyllum) fruit extract on biochemical parameters of induced obese-diabetic rats. J. Funct. Foods. 8: 139–149.CrossRefGoogle Scholar
  9. 9.
    Schmid, G. M., V. Converset, N. Walter, M. V. Sennitt, K. Y. Leung, H. Byers, M. Ward, D. F. Hochstrasser, M. A. Cawthorne, and J. C. Sanchez (2004) Effect of high-fat diet on the expression of proteins in muscle, adipose tissues, and liver of C57BL/6 mice. Proteomics 4: 2270–2282.CrossRefGoogle Scholar
  10. 10.
    Moraes, R. C., A. Blondet, K. Birkenkamp-Demtroeder, J. Tirard, T. F. Orntoft, A. Gertler, P. Durand, D. Naville, and M. Begeot (2003) Study of the alteration of gene expression in adipose tissue of diet-induced obese mice by microarray and reverse transcription-polymerase chain reaction analyses. Endocrinol. 144: 4773–4782.CrossRefGoogle Scholar
  11. 11.
    Levin, B. E., A. A. Dunn-Meynell, B. Balkan, and R. E. Keesey (1997) Selective breeding for diet-induced obesity and resistance in Sprague-Dawley rats. Am. J. Physiol. 273: R725–730.Google Scholar
  12. 12.
    Wang, X., J. W. Choi, T. S. Oh, D. K. Choi, R. Mukherjee, H. Liu, and J. W. Yun (2012) Comparative hepatic proteome analysis between lean and obese rats fed a high-fat diet reveals the existence of gender differences. Proteomics 12: 284–299.CrossRefGoogle Scholar
  13. 13.
    Wang, X., J. W. Choi, J. I. Joo, D. H. Kim, T. S. Oh, D. K. Choi, and J. W. Yun (2011) Differential expression of liver proteins between obesity-prone and obesity-resistant rats in response to a high-fat diet. Br. J. Nutr. 106: 612–626.CrossRefGoogle Scholar
  14. 14.
    Choi, J. W., H. Liu, D. K. Choi, T. S. Oh, R. Mukherjee, and J. W. Yun (2012) Profiling of gender-specific rat plasma proteins associated with susceptibility or resistance to diet-induced obesity. J. Proteomics. 75: 1386–1400.CrossRefGoogle Scholar
  15. 15.
    Ji, H., L. V. Outterbridge, and M. I. Friedman (2005) Phenotypebased treatment of dietary obesity: Differential effects of fenofibrate in obesity-prone and obesity-resistant rats. Metabolism. 54: 421–429.CrossRefGoogle Scholar
  16. 16.
    Suresh, S. and J. Mahendra (2014) Multifactorial relationship of obesity and periodontal disease. J. Clin Diagn. Res. 8: ZE01–03.CrossRefGoogle Scholar
  17. 17.
    Roh, C., U. Jung, and S. K. Jo (2012) Screening of anti-obesity agent from herbal mixtures. Molecules 17: 3630–3638.CrossRefGoogle Scholar
  18. 18.
    Rubio-Ruiz, M. E., M. El Hafidi, I. Perez-Torres, G. Banos, and V. Guarner (2013) Medicinal agents and metabolic syndrome. Curr. Med. Chem. 20: 2626–2640.CrossRefGoogle Scholar
  19. 19.
    Milosevic, N., M. Milanovic, L. Abenavoli, and N. Milic (2014) Phytotherapy and NAFLD—from goals and challenges to clinical practice. Rev. Recent Clin. Trials. 9: 195–203.CrossRefGoogle Scholar
  20. 20.
    Dong, H., F. E. Lu, and L. Zhao (2012) Chinese herbal medicine in the treatment of nonalcoholic fatty liver disease. Chin. J. Integr. Med. 18: 152–160.CrossRefGoogle Scholar
  21. 21.
    Vasudeva, N., N. Yadav, and S. K. Sharma (2012) Natural products: A safest approach for obesity. Chin. J. Integr. Med. 18: 473–480.CrossRefGoogle Scholar
  22. 22.
    Marles, R. J. and N. R. Farnsworth (1995) Antidiabetic plants and their active constituents. Phytomed. 2: 137–189.CrossRefGoogle Scholar
  23. 23.
    Wang, H. X. and T. B. Ng (1999) Natural products with hypoglycemic, hypotensive, hypocholesterolemic, antiatherosclerotic and antithrombotic activities. Life Sci. 65: 2663–2677.CrossRefGoogle Scholar
  24. 24.
    Qi, F., L. Zhao, A. Zhou, B. Zhang, A. Li, Z. Wang, and J. Han (2015) The advantages of using traditional Chinese medicine as an adjunctive therapy in the whole course of cancer treatment instead of only terminal stage of cancer. Biosci. Trends. 9: 16–34.CrossRefGoogle Scholar
  25. 25.
    Ling, C. Q., L. N. Wang, Y. Wang, Y. H. Zhang, Z. F. Yin, M. Wang, and C. Ling (2014) The roles of traditional Chinese medicine in gene therapy. J. Integr. Med. 12: 67–75.CrossRefGoogle Scholar
  26. 26.
    Zhao, C. Q., Y. Zhou, J. Ping, and L. M. Xu (2014) Traditional Chinese medicine for treatment of liver diseases: Progress, challenges and opportunities. J. Integr. Med. 12: 401–408.CrossRefGoogle Scholar
  27. 27.
    Park, S., J. S. Park, C. Cheon, Y. J. Yang, C. An, B. H. Jang, Y. K. Song, H. Go, J. A. Lee, Y. Shin, and S. G. Ko (2012) A pilot study to evaluate the effect of Taeumjowi-tang on obesity in Korean adults: Study protocol for a randomised, double-blind, placebo-controlled, multicentre trial. Trials. 13: 33.CrossRefGoogle Scholar
  28. 28.
    Park, S., W. Nahmkoong, C. Cheon, J. S. Park, B. H. Jang, Y. Shin, K. S. Kim, H. Go, Y. K. Song, and S. G. Ko (2013) Efficacy and safety of Taeeumjowi-tang in obese Korean adults: A double-blind, randomized, and placebo-controlled pilot trial. Evid. Based Complement. Alternat. Med. 2013: 498935.Google Scholar
  29. 29.
    Park, S.-M., I. -S. Ahn, D. -S. Kim, S. -A. Kang, D. -Y. Kwon, and H. -J. Yang (2010) Anti-obesity effects of Tae-Um-Jo-Wee-Tang and Do-Dam-Tang in female rats with diet-induced obesity. J. Appl. Biol. Chem. 53: 44–50.CrossRefGoogle Scholar
  30. 30.
    Kim, K.-S., D. -U. Lee, Y. -L. Kim, M. -J. Hwang, G. -W. Kim, and B. -S. Koo. (2007) Anti-obesity and anti-hyperlipidemic effects of Taeyeumjowee-tang and its modified prescription. J. Orient. Neuropsych. 18: 57–74.Google Scholar
  31. 31.
    Perry, B., J. Zhang, T. Saleh, and Y. Wang (2014) Liuwei Dihuang, a traditional Chinese herbal formula, suppresses chronic inflammation and oxidative stress in obese rats. J. Integr. Med. 12: 447–454.CrossRefGoogle Scholar
  32. 32.
    Chen, Y., D. Y. Fu, Y. Chen, Y. M. He, X. D. Fu, Y. Q. Xu, Y. Liu, X. T. Feng, T. Zhang, and W. J. Wang (2013) Effects of Chinese herbal medicine Yiqi Huaju Formula on hypertensive patients with metabolic syndrome: a randomized, placebo-controlled trial. J. Integr. Med. 11: 184–194.CrossRefGoogle Scholar
  33. 33.
    Zolg, J. W. and H. Langen (2004) How industry is approaching the search for new diagnostic markers and biomarkers. Mol. Cell. Proteomics 3: 345–354.CrossRefGoogle Scholar
  34. 34.
    Honore, B., M. Ostergaard, and H. Vorum (2004) Functional genomics studied by proteomics. BioEssays. 26: 901–915.CrossRefGoogle Scholar
  35. 35.
    Lanne, B., B. Dahllof, C. Lindahl, K. Ebefors, I. Kanmert, H. von Bahr, T. Miliotis, A. C. Nystrom, G. Arnerup, I. Paulsons, S. Kerb, and N. Oakes (2006) PPARalpha and PPARgamma regulation of liver and adipose proteins in obese and dyslipidemic rodents. J. Proteome Res. 5: 1850–1859.CrossRefGoogle Scholar
  36. 36.
    Mukherjee, R., J. W. Choi, D. K. Choi, T. S. Oh, H. Liu, and J. W. Yun (2012) Gender-dependent protein expression in white adipose tissues of lean and obese rats fed a high fat diet. Cell. Physiol. Biochem. 29: 617–634.CrossRefGoogle Scholar
  37. 37.
    Oh, T. S., J. W. Choi, D. K. Choi, R. Mukherjee, H. Liu, and J. W. Yun (2011) Gender dimorphism in skeletal muscle proteome between lean and diet-induced obese rats. Cell. Physiol. Biochem. 28: 981–996.CrossRefGoogle Scholar
  38. 38.
    Matta, A., R. Ralhan, L. V. DeSouza, and K. W. Siu (2010) Mass spectrometry-based clinical proteomics: Head-and-neck cancer biomarkers and drug-targets discovery. Mass spectrom. Rev. 29: 945–961.CrossRefGoogle Scholar
  39. 39.
    Rodriguez-Suarez, E., J. M. Mato, and F. Elortza (2012) Proteomics analysis of human nonalcoholic fatty liver. Methods Mol. Biol. 909: 241–258.Google Scholar
  40. 40.
    Xie, Z., H. Li, K. Wang, J. Lin, Q. Wang, G. Zhao, W. Jia, and Q. Zhang (2010) Analysis of transcriptome and metabolome profiles alterations in fatty liver induced by high-fat diet in rat. Metabol. 59: 554–560.CrossRefGoogle Scholar
  41. 41.
    Choi, D. K., T. S. Oh, J. W. Choi, R. Mukherjee, X. Wang, H. Liu, and J. W. Yun (2011) Gender difference in proteome of brown adipose tissues between male and female rats exposed to a high fat diet. Cell. Physiol. Biochem. 28: 933–948.CrossRefGoogle Scholar
  42. 42.
    Joo, J. I., T. S. Oh, D. H. Kim, D. K. Choi, X. Wang, J. W. Choi, and J. W. Yun (2011) Differential expression of adipose tissue proteins between obesity-susceptible and -resistant rats fed a high-fat diet. Proteomics 11: 1429–1448.CrossRefGoogle Scholar
  43. 43.
    Mi, H., A. Muruganujan, J. T. Casagrande, and P. D. Thomas (2013) Large-scale gene function analysis with the PANTHER classification system. Nat. protoc. 8: 1551–1566.CrossRefGoogle Scholar
  44. 44.
    Huang da, W., B. T. Sherman, and R. A. Lempicki (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. protoc. 4: 44–57.CrossRefGoogle Scholar
  45. 45.
    Warde-Farley, D., S. L. Donaldson, O. Comes, K. Zuberi, R. Badrawi, P. Chao, M. Franz, C. Grouios, F. Kazi, C. T. Lopes, A. Maitland, S. Mostafavi, J. Montojo, Q. Shao, G. Wright, G. D. Bader, and Q. Morris (2010) The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 38: W214–220.CrossRefGoogle Scholar
  46. 46.
    Sverdlov, A. L., A. Elezaby, J. B. Behring, M. M. Bachschmid, I. Luptak, V. H. Tu, D. A. Siwik, E. J. Miller, M. Liesa, O. S. Shirihai, D. R. Pimentel, R. A. Cohen, and W. S. Colucci (2014) High fat, high sucrose diet causes cardiac mitochondrial dysfunction due in part to oxidative post-translational modification of mitochondrial complex II. J. Mol. Cell. Cardiol. 78: 165–173.CrossRefGoogle Scholar
  47. 47.
    Li, S. Y., Y. Liu, V. K. Sigmon, A. McCort, and J. Ren (2005) High-fat diet enhances visceral advanced glycation end products, nuclear O-Glc-Nac modification, p38 mitogen-activated protein kinase activation and apoptosis. Diabetes Obes. Metab. 7: 448–454.CrossRefGoogle Scholar
  48. 48.
    Brocker, C., N. Lassen, T. Estey, A. Pappa, M. Cantore, V. V. Orlova, T. Chavakis, K. L. Kavanagh, U. Oppermann, and V. Vasiliou (2010) Aldehyde dehydrogenase 7A1 (ALDH7A1) is a novel enzyme involved in cellular defense against hyperosmotic stress. J. Biol. Chem. 285: 18452–18463.Google Scholar
  49. 49.
    Mills, P. B., E. Struys, C. Jakobs, B. Plecko, P. Baxter, M. Baumgartner, M. A. Willemsen, H. Omran, U. Tacke, B. Uhlenberg, B. Weschke, and P. T. Clayton (2006) Mutations in antiquitin in individuals with pyridoxine-dependent seizures. Nat. Med. 12: 307–309.CrossRefGoogle Scholar
  50. 50.
    Krupenko, N. I., M. E. Dubard, K. C. Strickland, K. M. Moxley, N. V. Oleinik, and S. A. Krupenko (2010) ALDH1L2 is the mitochondrial homolog of 10-formyltetrahydrofolate dehydrogenase. J. Biol. Chem. 285: 23056–23063.CrossRefGoogle Scholar
  51. 51.
    Edvardsson, U., H. B. von Lowenhielm, O. Panfilov, A. C. Nystrom, F. Nilsson, and B. Dahllof (2003) Hepatic protein expression of lean mice and obese diabetic mice treated with peroxisome proliferator-activated receptor activators. Proteomics 3: 468–478.CrossRefGoogle Scholar
  52. 52.
    Liu, Y., H. Dang, D. Li, W. Pang, B. D. Hammock, and Y. Zhu (2012) Inhibition of soluble epoxide hydrolase attenuates highfat-diet-induced hepatic steatosis by reduced systemic inflammatory status in mice. PloS one. 7: e39165.Google Scholar
  53. 53.
    Visinoni, S., N. F. Khalid, C. N. Joannides, A. Shulkes, M. Yim, J. Whitehead, T. Tiganis, B. J. Lamont, J. M. Favaloro, J. Proietto, S. Andrikopoulos, and B. C. Fam (2012) The role of liver fructose-1,6-bisphosphatase in regulating appetite and adiposity. Diabetes. 61: 1122–1132.CrossRefGoogle Scholar
  54. 54.
    Amano, S., S. Yamagishi, N. Kato, Y. Inagaki, T. Okamoto, M. Makino, K. Taniko, H. Hirooka, T. Jomori, and M. Takeuchi (2002) Sorbitol dehydrogenase overexpression potentiates glucose toxicity to cultured retinal pericytes. Biochem. Biophys. Res. Commun. 299: 183–188.CrossRefGoogle Scholar
  55. 55.
    Kahn, B. B., T. Alquier, D. Carling, and D. G. Hardie (2005) AMP-activated protein kinase: Ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 1: 15–25.CrossRefGoogle Scholar
  56. 56.
    Gething, M. J. and J. Sambrook (1992) Protein folding in the cell. Nature 355: 33–45.CrossRefGoogle Scholar
  57. 57.
    Thaler, J. P., C. X. Yi, E. A. Schur, S. J. Guyenet, B. H. Hwang, M. O. Dietrich, X. Zhao, D. A. Sarruf, V. Izgur, K. R. Maravilla, H. T. Nguyen, J. D. Fischer, M. E. Matsen, B. E. Wisse, G. J. Morton, T. L. Horvath, D. G. Baskin, M. H. Tschop, and M. W. Schwartz (2012) Obesity is associated with hypothalamic injury in rodents and humans. J. Clin. Invest. 122: 153–162.CrossRefGoogle Scholar
  58. 58.
    Pipatpiboon, N., W. Pratchayasakul, N. Chattipakorn, and S. C. Chattipakorn (2012) PPARgamma agonist improves neuronal insulin receptor function in hippocampus and brain mitochondria function in rats with insulin resistance induced by long term highfat diets. Endocrinol. 153: 329–338.CrossRefGoogle Scholar
  59. 59.
    Kleinridders, A., H. P. Lauritzen, S. Ussar, J. H. Christensen, M. A. Mori, P. Bross, and C. R. Kahn (2013) Leptin regulation of Hsp60 impacts hypothalamic insulin signaling. J. Clin. Invest. 123: 4667–4680.CrossRefGoogle Scholar
  60. 60.
    Woods, A., D. Azzout-Marniche, M. Foretz, S. C. Stein, P. Lemarchand, P. Ferre, F. Foufelle, and D. Carling (2000) Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase. Mol. Cell. Biol. 20: 6704–6711.CrossRefGoogle Scholar
  61. 61.
    Choudhary, C., C. Kumar, F. Gnad, M. L. Nielsen, M. Rehman, T. C. Walther, J. V. Olsen, and M. Mann (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Sci. 325: 834–840.CrossRefGoogle Scholar
  62. 62.
    Iyer, A., D. P. Fairlie, and L. Brown (2012) Lysine acetylation in obesity, diabetes and metabolic disease. Immun. Cell Biol. 90: 39–46.CrossRefGoogle Scholar
  63. 63.
    Chakraborty, S., M. Gogoi, and D. Chakravortty (2015) Lactoylglutathione lyase, a critical enzyme in methylglyoxal detoxification, contributes to survival of Salmonella in the nutrient rich environment. Virulence. 6: 50–65.CrossRefGoogle Scholar
  64. 64.
    Birkenmeier, G., C. Stegemann, R. Hoffmann, R. Gunther, K. Huse, and C. Birkemeyer (2010) Posttranslational modification of human glyoxalase 1 indicates redox-dependent regulation. PloS one 5: e10399.CrossRefGoogle Scholar
  65. 65.
    Rardin, M. J., J. C. Newman, J. M. Held, M. P. Cusack, D. J. Sorensen, B. Li, B. Schilling, S. D. Mooney, C. R. Kahn, E. Verdin, and B. W. Gibson (2013) Label-free quantitative proteomics of the lysine acetylome in mitochondria identifies substrates of SIRT3 in metabolic pathways. Proc. Natl. Acad. Sci. USA. 110: 6601–6606.CrossRefGoogle Scholar
  66. 66.
    Scrutton, M. C. and M. D. White (1974) Pyruvate carboxylase. Inhibition of the mammalian and avian liver enzymes by alphaketoglutarate and L-glutamate. J. Biol. Chem. 249: 5405–5415.Google Scholar
  67. 67.
    Lo, A. S., C. T. Liew, S. M. Ngai, S. K. Tsui, K. P. Fung, C. Y. Lee, and M. M. Waye (2005) Developmental regulation and cellular distribution of human cytosolic malate dehydrogenase (MDH1). J. Biol. Chem. 94: 763–773.Google Scholar
  68. 68.
    Kim, E. Y., W. K. Kim, H. J. Kang, J. H. Kim, S. J. Chung, Y. S. Seo, S. G. Park, S. C. Lee, and K. H. Bae (2012) Acetylation of malate dehydrogenase 1 promotes adipogenic differentiation via activating its enzymatic activity. J. Lipid Res. 53: 1864–1876.CrossRefGoogle Scholar
  69. 69.
    Jing, E., B. Emanuelli, M. D. Hirschey, J. Boucher, K. Y. Lee, D. Lombard, E. M. Verdin, and C. R. Kahn (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc. Natl. Acad. Sci. USA. 108: 14608–14613.CrossRefGoogle Scholar
  70. 70.
    Chang, P. W., S. K. Tsui, C. Liew, C. C. Lee, M. M. Waye, and K. P. Fung (1997) Isolation, characterization, and chromosomal mapping of a novel cDNA clone encoding human selenium binding protein. J. Cell. Biochem. 64: 217–224.CrossRefGoogle Scholar
  71. 71.
    Porat, A., Y. Sagiv, and Z. Elazar (2000) A 56-kDa seleniumbinding protein participates in intra-Golgi protein transport. J. Biol. Chem. 275: 14457–14465.CrossRefGoogle Scholar
  72. 72.
    Li, T., W. Yang, M. Li, D. S. Byun, C. Tong, S. Nasser, M. Zhuang, D. Arango, J. M. Mariadason, and L. H. Augenlicht (2008) Expression of selenium-binding protein 1 characterizes intestinal cell maturation and predicts survival for patients with colorectal cancer. Mol. Nutr. Food Res. 52: 1289–1299.CrossRefGoogle Scholar
  73. 73.
    Jeong, J. Y., Y. Wang, and A. J. Sytkowski (2009) Human selenium binding protein-1 (hSP56) interacts with VDU1 in a selenium-dependent manner. Biochem. Biophys. Res. Commun. 379: 583–588.CrossRefGoogle Scholar
  74. 74.
    Fountoulakis, M., P. Berndt, U. A. Boelsterli, F. Crameri, M. Winter, S. Albertini, and L. Suter (2000) Two-dimensional database of mouse liver proteins: Changes in hepatic protein levels following treatment with acetaminophen or its nontoxic regioisomer 3-acetamidophenol. Electrophoresis. 21: 2148–2161.CrossRefGoogle Scholar
  75. 75.
    Kirpich, I. A., L. N. Gobejishvili, M. Bon Homme, S. Waigel, M. Cave, G. Arteel, S. S. Barve, C. J. McClain, and I. V. Deaciuc (2011) Integrated hepatic transcriptome and proteome analysis of mice with high-fat diet-induced nonalcoholic fatty liver disease. J. Nutr. Biochem. 22: 38–45.CrossRefGoogle Scholar
  76. 76.
    Jaisson, S., M. Veiga-da-Cunha, and E. Van Schaftingen (2009) Molecular identification of omega-amidase, the enzyme that is functionally coupled with glutamine transaminases, as the putative tumor suppressor Nit2. Biochimie. 91: 1066–1071.CrossRefGoogle Scholar
  77. 77.
    Islinger, M., G. H. Luers, K. W. Li, M. Loos, and A. Volkl (2007) Rat liver peroxisomes after fibrate treatment. A survey using quantitative mass spectrometry. J. Biol. Chem. 282: 23055–23069.CrossRefGoogle Scholar
  78. 78.
    Gronemeyer, T., S. Wiese, R. Ofman, C. Bunse, M. Pawlas, H. Hayen, M. Eisenacher, C. Stephan, H. E. Meyer, H. R. Waterham, R. Erdmann, R. J. Wanders, and B. Warscheid (2013) The proteome of human liver peroxisomes: identification of five new peroxisomal constituents by a label-free quantitative proteomics survey. PloS one. 8: e57395.Google Scholar
  79. 79.
    Chen, Y., J. Zhu, P. Y. Lum, X. Yang, S. Pinto, D. J. MacNeil, C. Zhang, J. Lamb, S. Edwards, S. K. Sieberts, A. Leonardson, L. W. Castellini, S. Wang, M. F. Champy, B. Zhang, V. Emilsson, S. Doss, A. Ghazalpour, S. Horvath, T. A. Drake, A. J. Lusis, and E. E. Schadt (2008) Variations in DNA elucidate molecular networks that cause disease. Nature 452: 429–435.CrossRefGoogle Scholar
  80. 80.
    Pan, S. Y., Q. Yu, Y. Zhang, X. Y. Wang, N. Sun, Z. L. Yu, and K. M. Ko (2012) Dietary Fructus schisandrae extracts and fenofibrate regulate the serum/hepatic lipid-profile in normal and hypercholesterolemic mice, with attention to hepatotoxicity. Lipids Health Dis. 11: 120.CrossRefGoogle Scholar
  81. 81.
    Pan, S. Y., Z. L. Yu, H. Dong, C. J. Xiang, W. F. Fong, and K. M. Ko (2011) Ethanol extract of Fructus schisandrae decreases hepatic triglyceride level in mice fed with a high fat/cholesterol diet, with attention to acute toxicity. Evid. Based Complement. Alternat. Med. 2011: 729412.Google Scholar
  82. 82.
    Go, R. E., K. A. Hwang, S. H. Kim, M. Y. Lee, C. W. Kim, S. Y. Jeon, Y. B. Kim, and K. C. Choi (2014) Effects of anti-obesity drugs, phentermine and mahuang, on the behavioral patterns in Sprague-Dawley rat model. Lab. Anim. Res. 30: 73–78.CrossRefGoogle Scholar
  83. 83.
    Han, L. K., Y. N. Zheng, B. J. Xu, H. Okuda, and Y. Kimura (2002) Saponins from platycodi radix ameliorate high fat dietinduced obesity in mice. J. Nutr. 132: 2241–2245.Google Scholar
  84. 84.
    Lee, C. E., H. J. Hur, J. T. Hwang, M. J. Sung, H. J. Yang, H. J. Kim, J. H. Park, D. Y. Kwon, and M. S. Kim (2012) Long-term consumption of platycodi radix ameliorates obesity and insulin resistance via the activation of AMPK pathways. Evid. Based Complement. Alternat. Med. 2012: 759143.Google Scholar

Copyright information

© The Korean Society for Biotechnology and Bioengineering and Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Sang Woo Kim
    • 1
  • Tae-Jun Park
    • 1
  • Harmesh N. Chaudhari
    • 1
  • Jae Heon Choi
    • 1
  • Ji-Young Choi
    • 2
  • Ye Jin Kim
    • 2
  • Myung-Sook Choi
    • 2
    Email author
  • Jong Won Yun
    • 1
    Email author
  1. 1.Department of BiotechnologyDaegu UniversityKyungsanKorea
  2. 2.Center for Food and Nutritional Genomics Research, Department of Food Science and NutritionKyungpook National UniversityDaeguKorea

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