DOI QR코드

DOI QR Code

Improvement of blood lipid metabolism and obesity through the administration of mixed lactic acid bacteria including Lactobacillus plantarum K-1 in mice fed a high-fat diet

  • Hyeon Ju Lim (Department of Biomedical Science, Jungwon University) ;
  • Young Geol Yoon (Department of Biomedical Science, Jungwon University)
  • Received : 2023.07.04
  • Accepted : 2023.07.31
  • Published : 2023.12.31

Abstract

We investigated the effects of single and combined administrations of Lactobacillus species (L. plantarum, LP; L. gasseri, LG; L. casei, LC) on blood lipid metabolism and obesity in mice fed a high-fat diet (HFD). The mice were continuously supplemented with LP, LP/LG, or LP/LG/LC, along with HFD, for 12 weeks. The consumption of HFD led to significant increases in body weight, total cholesterol, and triglyceride levels compared to the normal control group. However, administration of LP, LP/LG, or LP/LG/LC to HFD-fed mice reduced body weight gain and showed a tendency to suppress the levels of total cholesterol, triglycerides, and LDL-cholesterol, while increasing HDL-cholesterol levels. The HFD group exhibited increased abdominal fat weight and larger adipocytes in the epididymal adipose tissue compared to the NC group. However, the administered probiotics led to a significant reduction in adipocyte size with decreasing tendency in abdominal fat weight compared with the HFD group. Additionally, the deposition of giant vesicular fat cells in the liver of the HFD group considerably decreased in the probiotic-administered group. Microbiome analysis revealed an imbalance in intestinal microbes in the HFD group, characterized by lower Bacteroidetes and higher Proteobacteria ratios. However, probiotic administration tended to restore the microbial distribution by controlling the abundance of Bacteroidetes and Proteobacteria, resulting in decreased Firmicutes/Bacteroidetes and Proteobacteria/Bacteroidetes ratios. These results suggest that single and combined administration of LP and other probiotics holds enormous potential in reducing obesity in HFD-fed mice as they regulate lipid metabolism, reduce adipocyte size, and restore the balance of intestinal microbes.

Keywords

Acknowledgement

The authors sincerely thank Biorhythm Co., Ltd. for providing lactobacillus products. This research was supported by the "Regional Innovation Strategy (RIS)" through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (MOE) (2021RIS-001).

References

  1. van der Vossen EWJ, de Goffau MC, Levin E, Nieuwdorp M (2022) Recent insights into the role of microbiome in the pathogenesis of obesity. Therap Adv Gastroenterol 15: 17562848221115320. doi: 10.1177/17562848221115320
  2. Ooi LG, Liong MT (2011) Cholesterol-lowering effects of probiotics and prebiotics: a review of in vivo and in vitro findings. Int J Mol Sci 11: 2499-2522. doi: 10.3390/ijms11062499
  3. Choi SY, Park HA, Yoon YG (2022) Anti-obesity effect of the combination of fermented extracts from Momordica charanatia and Withania somnifera in mice fed a high-fat diet. J Appl Biol Chem 65: 143-152. doi: 10.3839/jabc.2022.019
  4. Kang JG, Park CY (2012) Anti-obesity drugs: A review about their effects and safety. Diabetes Metab J 36: 13-25. doi: 10.4093/dmj.2012.36.1.13
  5. Kim KK (2011) Pharmacotherapy for obesity. J Korean Med Assoc 54: 409-418. doi: 10.5124/jkma.2011.54.4.409
  6. Park HE, Do KH, Jeong JW, Jung YH, Lee WK (2018) Cholesterol and visceral fat lowering effects of combined lactic acid bacteria (Lactobacillus casei WK3, Enterococcus faecium WK5, Bifidobacterium longum WK9, and Lactobacillus plantarum K-1) in high fat diet-fed C57BL/6J mice. J Korean Soc Food Sci Nutr 47: 1210-1216. doi: 10.3746/jkfn.2018.47.12.1210
  7. Kang JH, Yun SI, Park MH, Park JH, Jeong SY, Park HO (2013) Anti-obesity effect of Lactobacillus gasseri BNR17 in high-sucrose diet-induced obese mice. PLoS ONE 8: e54617. doi: 10.1371/journal.pone.005461
  8. Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66: 365-378. PMID: 2666378 https://doi.org/10.1111/j.1365-2672.1989.tb05105.x
  9. Fan Y, Pedersen O (2021) Gut microbiota in human metabolic health and disease. Nat Rev Microbiol 19: 55-71. doi: 10.1038/s41579-020-0433-9
  10. Lidbeck A, Edlund C, Gustafsson JA, Kager L, Nord CE (1988) Impact of Lactobacillus acidophilus on the normal intestinal microflora after administration of two antimicrobial agents. Infection 16: 329-336. doi: 10.1007/BF01644541
  11. Collins EB, Aramaki K (1980) Production of hydrogen peroxide by Lactobacillus acidophilus. J Dairy Sci 63: 353-357. doi: 10.3168/jds.S0022-0302(80)82938-9
  12. Choi HJ, Shin MS, Lee SM, Lee WK (2012) Immunomodulatory properties of Enterococcus faecium JWS 833 isolated from duck intestinal tract and suppression of Listeria monocytogenes infection. Microbiol Immunol 56: 613-620. doi: 10.1111/j.1348-0421.2012.00486.x
  13. Park HE, Kang KW, Kim BS, Lee SM, Lee WK (2017) Immunomodulatory potential of Weissella cibaria in aged C57BL/6J mice. J Microbiol Biotechnol 27: 2094-2103. doi: 10.4014/jmb.1708.08016
  14. Kerry RG, Patra JK, Gouda S, Park Y, Shin HS, Das G (2018) Benefaction of probiotics for human health: A review. J Food Drug Anal 26: 927-939. doi: 10.1016/j.jfda.2018.01.002
  15. Karimi G, Sabran MR, Jamaluddin R, Parvaneh K, Mohtarrudin N, Ahmad Z, Khazaai H, Khodavandi A (2015) The anti-obesity effects of Lactobacillus casei strain Shirota versus Orlistat on high fat diet-induced obese rats. Food Nutr Res 59: 29273. doi: 10.3402/fnr.v59.29273
  16. Ma Y, Fei Y, Han X, Liu G, Fang J (2022) Lactobacillus plantarum alleviates obesity by altering the composition of the gut microbiota in high-fat diet-fed mice. Front Nutr 9: 947367. doi: 10.3389/fnut.2022.947367
  17. Haglund O, Luostarinen R, Wallin R, Wibell L, Saldeen T (1991) The effects of fish oil on triglyceride, cholesterol, fibrinogen and malondialdehyde in humans supplemented with vitamin E. J Nutr 121: 165-169. doi: 10.1093/jn/121.2.165
  18. Rosenfeld L (1989) Lipoprotein analysis. Early methods in the diagnosis of atherosclerosis. Arch Pathol Lab Med 113: 1101-1110. PMID: 2679486
  19. Park SJ, Jeon YJ, Kim HJ, Han JS (2013) Anti-obesity effects of Ishige okamurae extract in C57BL/6J mice fed high-fat diet. Korean J Food Sci Technol 45: 199-205. doi: 10.9721/KJFST.2013.45.2.199
  20. Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJ, Holmes SP (2016) DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods 13: 581-583. doi: 10.1038/nmeth.3869
  21. An SJ, Jung UJ, Choi MS, Chae CK, Oh GT, Park YB (2013) Functions of monocyte chemotactic protein-3 in transgenic mice fed a high-fat, high-cholesterol diet. J Microbiol Biotechnol 23: 405-413. doi: 10.4014/jmb.1210.10057
  22. Koo HJ, Kang SC, Jang SA, Kwon JE, Sohn E, Sohn EH (2014) Effects of protocatechuic acid derived from Rubus coreanus on the lipid metabolism in high cholesterol diet-induced mice. Korean J Plant Res 27: 271278. doi: 10.7732/kjpr.2014.27.4.271
  23. Kim JY, Shin M, Heo YR (2014) Effects of stabilized rice bran on obesity and antioxidative enzyme activity in high fat diet-induced obese C57BL/6 mice. Korean Soc Food Sci Nutr 43: 1148-1157. doi: 10.3746/jkfn.2014.43.8.1148
  24. Park SH, Jang MJ, Hong JH, Rhee SJ, Choi KH, Park MR (2007) Effects of mulberry leaf extract feeding on lipid status of rats fed high cholesterol diets. J Korean Soc Food Sci Nutr 36: 43-50. doi: 10.3746/jkfn.2007.36.1.043
  25. Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, Lallone RL, Burley SK, Friedman JM (1995) Weight-reducing effects of the plasma protein encoded by the obese gene. Science 269: 543-546. doi: 10.1126/science.7624777
  26. Ahren B, Larsson H, Wilhelmsson C, Nasman B, Olsson T (1997) Regulation of circulating leptin in humans. Endocrine 7: 1-8. doi: 10.1007/BF02778056
  27. Matsuzawa Y, Funahashi T, Kihara S, Shimomura I (2004) Adiponectin and metabolic syndrome. Arterioscler Thromb Vasc Biol 24: 29-33. doi: 10.1161/01.ATV.0000099786.99623.EF
  28. Havel PJ (2002) Control of energy homeostasis and insulin action by adipocyte hormones: leptin, acylation stimulating protein, and adiponectin. Curr Opin Lipidol 13: 51-59. doi: 10.1097/00041433-200202000-00008
  29. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102: 11070-11075. doi: 10.1073/pnas.0504978102
  30. Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology: human gut microbes associated with obesity. Nature 444: 1022-1023. doi: 10.1038/4441022a
  31. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027-1031. doi: 10.1038/nature05414
  32. Hildebrandt MA, Hoffmann C, Sherrill-Mix SA, Keilbaugh SA, Hamady M, Chen YY, Knight R, Ahima RS, Bushman F, Wu GD (2009) High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137: 1716-1724.e1-2. doi: 10.1053/j.gastro.2009.08.042