Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
권호 표지
DOI QR코드

DOI QR Code

Effects of fermented ginseng root and ginseng berry on obesity and lipid metabolism in mice fed a high-fat diet

  • Li, Zhipeng (Department of Food and Nutrition, Research Institute of Human Ecology, Seoul National University) ;
  • Kim, Hee Jung (Department of Food and Nutrition, Research Institute of Human Ecology, Seoul National University) ;
  • Park, Myeong Soo (Department of Hotel Culinary Arts, Yeonsung University) ;
  • Ji, Geun Eog (Department of Food and Nutrition, Research Institute of Human Ecology, Seoul National University)
  • Received : 2017.01.03
  • Accepted : 2017.04.07
  • Published : 2018.07.15
Download PDF
⟨ Previous Next ⟩

Abstract

Background: Previous studies have shown that both ginseng root and ginseng berry exhibit antiobesity and antidiabetic effects. However, a direct comparison of the efficacy and mechanisms between the root and the berry after oral administration remains to be illuminated. Methods: In this study, we observed the effects of fermented ginseng root (FGR) and fermented ginseng berry (FGB) on obesity and lipid metabolism in high-fat diet induced obese mice. Results: FGR and FGB significantly inhibited the activity of pancreatic lipase in vitro. Both FGR and FGB significantly suppressed weight gain and excess food intake and improved hypercholesterolemia and fatty liver, while only FGR significantly attenuated hyperglycemia and insulin resistance. Both FGR and FGB significantly inhibited the mRNA expression of Ldlr and Acsl1 while FGR also significantly inhibited expression of Cebpa and Dgat2 in liver. FGR significantly decreased the epididymal fat weight of mice while FGB significantly inhibited the mRNA expression of genes Cebpa, Fas, Hsl, Il1b, and Il6 in adipose tissue. Conclusion: Saponin from both FGR and FGB had a beneficial effect on high-fat diet-induced obesity. Compared to FGB, FGR exhibited more potent antihyperglycemic and antiobesity effect. However, only FGB significantly inhibited mRNA expression of inflammatory markers such as interleukins $1{\beta}$ and 6 in adipose tissue.

Keywords

References

  1. Attele AS, Zhou YP, Xie JT, Wu JA, Zhang L, Dey L, Pugh W, Rue PA, Polonsky KS, Yuan CS. Antidiabetic effects of Panax ginseng berry extract and the identification of an effective component. Diabetes 2002;51:1851-8. https://doi.org/10.2337/diabetes.51.6.1851
  2. Dey L, Xie J, Wang A, Wu J, Maleckar S, Yuan CS. Anti-hyperglycemic effects of ginseng: comparison between root and berry. Phytomedicine 2003;10:600-5. https://doi.org/10.1078/094471103322331908
  3. Xie J, Zhou YP, Dey L, Attele A, Wu J, Gu M, Polonsky K, Yuan CS. Ginseng berry reduces blood glucose and body weight in db/db mice. Phytomedicine 2002;9:254-8. https://doi.org/10.1078/0944-7113-00106
  4. Lee MR, Kim BC, Kim R, Oh HI, Kim HK, Choi KJ, Sung CK. Anti-obesity effects of black ginseng extract in high fat diet-fed mice. J Ginseng Res 2013;37:308-14. https://doi.org/10.5142/jgr.2013.37.308
  5. Liu R, Zhang J, Liu W, Kimura Y, Zheng Y. Anti-obesity effects of protopanaxdiol types of ginsenosides isolated from the leaves of American ginseng (Panax quinquefolius L.) in mice fed with a high-fat diet. Fitoterapia 2010;81:1079-87. https://doi.org/10.1016/j.fitote.2010.07.002
  6. Kobashi K, Akao T. Relation of intestinal bacteria to pharmacological effects of glycosides. Biosci Microflora 1997;16:1-7. https://doi.org/10.12938/bifidus1996.16.1
  7. Yim JS, Kim YS, Moon SK, Cho KH, Bae HS, Kim JJ, Park EK, Kim DH. Metabolic activities of ginsenoside Rb1, baicalin, glycyrrhizin and geniposide to their bioactive compounds by human intestinal microflora. Biol Pharm Bull 2004;27:1580-3. https://doi.org/10.1248/bpb.27.1580
  8. Kim NY, Lee I, Ji GE. Reliable and simple detection of ochratoxin and fumonisin production in black Aspergillus. J Food Prot 2014;77:653-8. https://doi.org/10.4315/0362-028X.JFP-13-396
  9. Li Z, Ahn HJ, Kim NY, Lee YN, Ji GE. Korean ginseng berry fermented by mycotoxin non-producing Aspergillus niger and Aspergillus oryzae: ginsenoside analyses and anti-proliferative activities. Biol Pharm Bull 2016;39:1461-7. https://doi.org/10.1248/bpb.b16-00239
  10. Li Z, Jin H, Oh SY, Ji GE. Anti-obese effects of two Lactobacilli and two Bifidobacteria on ICR mice fed on a high fat diet. Biochem Biophys Res Commun 2016;480:222-7. https://doi.org/10.1016/j.bbrc.2016.10.031
  11. Liu W, Zheng Y, Han L, Wang H, Saito M, Ling M, Kimura Y, Feng Y. Saponins (Ginsenosides) from stems and leaves of Panax quinquefolium prevented highfat diet-induced obesity in mice. Phytomedicine 2008;15:1140-5. https://doi.org/10.1016/j.phymed.2008.07.002
  12. Jung S, Lee MS, Shin Y, Kim CT, Kim IH, Kim YS, Kim Y. Anti-obesity and antiinflammatory effects of high hydrostatic pressure extracts of ginseng in highfat diet induced obese rats. J Funct Foods 2014;10:169-77. https://doi.org/10.1016/j.jff.2014.06.007
  13. Manousopoulou A, Koutmani Y, Karaliota S, Woelk C, Manolakos E, Karalis K, Garbis S. Hypothalamus proteomics from mouse models with obesity and anorexia reveals therapeutic targets of appetite regulation. Nutr Diabetes 2016;6:e204. https://doi.org/10.1038/nutd.2016.10
  14. Wu Y, Yu Y, Szabo A, Han M, Huang XF. Central inflammation and leptin resistance are attenuated by ginsenoside Rb1 treatment in obese mice fed a high-fat diet. PLoS One 2014;9:e92618. https://doi.org/10.1371/journal.pone.0092618
  15. Kim JH, Kang SA, Han SM, Shim I. Comparison of the antiobesity effects of the protopanaxadiol-and protopanaxatriol-type saponins of red ginseng. Phytother Res 2009;23:78-85. https://doi.org/10.1002/ptr.2561
  16. Li Z, Ji GE. Ginseng and obesity. J Ginseng Res 2018;42:1-8. https://doi.org/10.1016/j.jgr.2016.12.005
  17. Lemieux I, Lamarche B, Couillard C, Pascot A, Cantin B, Bergeron J, Dagenais GR, Despres JP. Total cholesterol/HDL cholesterol ratio vs LDL cholesterol/HDL cholesterol ratio as indices of ischemic heart disease risk in men: the Quebec Cardiovascular Study. Arch Intern Med 2001;161:2685-92. https://doi.org/10.1001/archinte.161.22.2685
  18. Nuno-Lambarri N, Dominguez-Perez M, Baulies-Domenech A, Monte MJ, Marin JJ, Rosales-Cruz P, Souza V, Miranda RU, Bucio L, Montalvo-Jave EE, et al. Liver cholesterol overload aggravates obstructive cholestasis by inducing oxidative stress and premature death in mice. Oxid Med Cell Longev 2016;2016:9895176.
  19. Mari M, Caballero F, Colell A, Morales A, Caballeria J, Fernandez A, Enrich C, Fernandez-Checa JC, Garcia-Ruiz C. Mitochondrial free cholesterol loading sensitizes to TNF-and Fas-mediated steatohepatitis. Cell Metab 2006;4:185-98. https://doi.org/10.1016/j.cmet.2006.07.006
  20. Dowman JK, Tomlinson J, Newsome P. Pathogenesis of non-alcoholic fatty liver disease. QJM 2010;103:71-83. https://doi.org/10.1093/qjmed/hcp158
  21. Shi J, Zhang Y, Gu W, Cui B, Xu M, Yan Q, Wang W, Ning G, Hong J. Serum liver fatty acid binding protein levels correlate positively with obesity and insulin resistance in Chinese young adults. PLoS One 2012;7:e48777. https://doi.org/10.1371/journal.pone.0048777
  22. Coleman RA, Lewin TM, Muoio DM. Physiological and nutritional regulation of enzymes of triacylglycerol synthesis. Annu Rev Nutr 2000;20:77-103. https://doi.org/10.1146/annurev.nutr.20.1.77
  23. Benard O, Lim J, Apontes P, Jing X, Angeletti RH, Chi Y. Impact of high-fat diet on the proteome of mouse liver. J Nutr Biochem 2016;31:10-9. https://doi.org/10.1016/j.jnutbio.2015.12.012
  24. Patsouris D, Reddy JK, Muller M, Kersten S. Peroxisome proliferator-activated receptor ${\alpha}$ mediates the effects of high-fat diet on hepatic gene expression. Endocrinology 2006;147:1508-16. https://doi.org/10.1210/en.2005-1132
  25. Gu X, Xie Z, Wang Q, Liu G, Qu Y, Zhang L, Pan J, Zhao G, Zhang Q. Transcriptome profiling analysis reveals multiple modulatory effects of Ginkgo biloba extract in the liver of rats on a high-fat diet. FEBS J 2009;276:1450-8. https://doi.org/10.1111/j.1742-4658.2009.06886.x
  26. Saraswathi V, Hasty AH. Inhibition of long-chain acyl coenzyme A synthetases during fatty acid loading induces lipotoxicity in macrophages. Arterioscler Thromb Vasc Biol 2009;29:1937-43. https://doi.org/10.1161/ATVBAHA.109.195362
  27. Matsusue K, Gavrilova O, Lambert G, Brewer Jr HB, Ward JM, Inoue Y, LeRoith D, Gonzalez FJ. Hepatic CCAAT/enhancer binding protein ${\alpha}$ mediates induction of lipogenesis and regulation of glucose homeostasis in leptindeficient mice. Mol Endocrinol 2004;18:2751-64. https://doi.org/10.1210/me.2004-0213
  28. Inoue M, Ohtake T, Motomura W, Takahashi N, Hosoki Y, Miyoshi S, Suzuki Y, Saito H, Kohgo Y, Okumura T. Increased expression of $PPAR{\gamma}$ in high fat dietinduced liver steatosis in mice. Biochem Biophys Res Commun 2005;336:215-22. https://doi.org/10.1016/j.bbrc.2005.08.070
  29. Maeda K, Cao H, Kono K, Gorgun CZ, Furuhashi M, Uysal KT, Cao Q, Atsumi G, Malone H, Krishnan B, et al. Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes. Cell Metab 2005;1:107-19. https://doi.org/10.1016/j.cmet.2004.12.008
  30. Jones JR, Barrick C, Kim KA, Lindner J, Blondeau B, Fujimoto Y, Shiota M, Kesterson RA, Kahn BB, Magnuson MA. Deletion of $PPAR{\gamma}$ in adipose tissues of mice protects against high fat diet-induced obesity and insulin resistance. Proc Natl Acad Sci USA 2005;102:6207-12. https://doi.org/10.1073/pnas.0306743102
  31. Gaidhu MP, Anthony NM, Patel P, Hawke TJ, Ceddia RB. Dysregulation of lipolysis and lipid metabolism in visceral and subcutaneous adipocytes by high-fat diet: role of ATGL, HSL, and AMPK. Am J Physiol Cell Physiol 2010;298:C961-71. https://doi.org/10.1152/ajpcell.00547.2009
  32. Crandall DL, Goldstein BM, Huggins F, Cervoni P. Adipocyte blood flow: influence of age, anatomic location, and dietary manipulation. Am J Physiol Regul Integr Comp Physiol 1984;247:R46-51. https://doi.org/10.1152/ajpregu.1984.247.1.R46
  33. Karalis KP, Giannogonas P, Kodela E, Koutmani Y, Zoumakis M, Teli T. Mechanisms of obesity and related pathology: linking immune responses to metabolic stress. FEBS J 2009;276:5747-54. https://doi.org/10.1111/j.1742-4658.2009.07304.x
  34. Lagathu C, Yvan-Charvet L, Bastard JP, Maachi M, Quignard-Boulange A, Capeau J, Caron M. Long-term treatment with interleukin-$1{\beta}$ induces insulin resistance in murine and human adipocytes. Diabetologia 2006;49:2162-73. https://doi.org/10.1007/s00125-006-0335-z
  35. Gu W, Kim KA, Kim DH. Ginsenoside Rh1 ameliorates high fat diet-induced obesity in mice by inhibiting adipocyte differentiation. Biol Pharm Bull 2013;36:102-7.

Cited by

  1. Tangduqing Granules Attenuate Insulin Resistance and Abnormal Lipid Metabolism through the Coordinated Regulation of PPAR γ and DGAT2 in Type 2 Diabetic Rats vol.2019, pp.None, 2018, https://doi.org/10.1155/2019/7403978
  2. Ginseng Berry Extract Rich in Phenolic Compounds Attenuates Oxidative Stress but not Cardiac Remodeling post Myocardial Infarction vol.20, pp.4, 2019, https://doi.org/10.3390/ijms20040983
  3. Ulmus parvifolia Jacq. Exhibits Antiobesity Properties and Potentially Induces Browning of White Adipose Tissue vol.2020, pp.None, 2018, https://doi.org/10.1155/2020/9358563
  4. Bok-choy promotes growth performance, lipid metabolism and related gene expression in Syrian golden hamsters fed with a high-fat diet vol.11, pp.3, 2018, https://doi.org/10.1039/c9fo02975c
  5. Protective Mechanism of Common Buckwheat (Fagopyrum esculentum Moench.) against Nonalcoholic Fatty Liver Disease Associated with Dyslipidemia in Mice Fed a High-Fat and High-Cholesterol Diet vol.68, pp.24, 2020, https://doi.org/10.1021/acs.jafc.9b08211
  6. Enhanced uronic acid content, antioxidant, and anti‐inflammatory activities of polysaccharides from ginseng fermented by Saccharomyces cerevisiae GIW‐1 vol.44, pp.11, 2020, https://doi.org/10.1111/jfpp.14885
  7. Herbal formulation MIT ameliorates high-fat diet-induced non-alcoholic fatty liver disease vol.9, pp.4, 2018, https://doi.org/10.1016/j.imr.2020.100422
  8. Multi-Enzyme Supplementation Modifies the Gut Microbiome and Metabolome in Breeding Hens vol.12, pp.None, 2018, https://doi.org/10.3389/fmicb.2021.711905
  9. The effects of ginseng on the metabolic syndrome: An updated review vol.9, pp.9, 2021, https://doi.org/10.1002/fsn3.2475
  10. In Vitro Evaluation of Anti-Lung Cancer and Anti-COVID-19 Effects using Fermented Black Color Ginseng Extract vol.16, pp.9, 2018, https://doi.org/10.1177/1934578x211034387