Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Anti-Obesity Potential through Regulation of Carbohydrate Uptake and Gene Expression in Intestinal Epithelial Cells by the Probiotic Lactiplantibacillus plantarum MGEL20154 from Fermented Food

  • So Young Park (Department of Biotechnology, Pukyong National University) ;
  • Jin Won Choi (Department of Biotechnology, Pukyong National University) ;
  • Dong Nyoung Oh (Department of Biotechnology, Pukyong National University) ;
  • Eun Ji Lee (Department of Biotechnology, Pukyong National University) ;
  • Dong Pil Kim (Department of Biotechnology, Pukyong National University) ;
  • Sun Jay Yoon (Department of Biotechnology, Pukyong National University) ;
  • Won Je Jang (Department of Biotechnology, Pukyong National University) ;
  • Sang Jun Han (Department of Biotechnology, Pukyong National University) ;
  • Seungjun Lee (Department of Food Science and Nutrition, Pukyong National University) ;
  • Jong Min Lee (Department of Biotechnology, Pukyong National University)
  • Received : 2022.12.04
  • Accepted : 2023.01.30
  • Published : 2023.05.28
Download PDF
⟨ Previous Next ⟩

Abstract

We investigated the probiotic characteristics and anti-obesity effect of Lactiplantibacillus plantarum MGEL20154, a strain that possesses excellent intestinal adhesion and viability. The in vitro properties, e.g., gastrointestinal (GI) resistance, adhesion, and enzyme activity, demonstrated that MGEL20154 is a potential probiotic candidate. Oral administration of MGEL20154 to diet-induced obese C57BL/6J mice for 8 weeks resulted in a feed efficacy decrease by 44.7% compared to that of the high-fat diet (HFD) group. The reduction rate of weight gain was about 48.5% in the HFD+MGEL20154 group compared to that of the HFD group after 8 weeks, and the epididymal fat pad was also reduced in size by 25.2%. In addition, the upregulation of the zo-1, pparα, and erk2, and downregulation of the nf-κb and glut2 genes in Caco-2 cells by MGEL20154 were observed. Therefore, we propose that the anti-obesity effect of the strain is exerted by inhibiting carbohydrate absorption and regulating gene expression in the intestine.

Keywords

Acknowledgement

This research was supported by Pukyong National University Development Project Research Fund, 2022.

References

  1. Duar RM, Lin XB, Zheng J, Martino ME, Grenier T, Perez-Munoz ME, et al. 2017. Lifestyles in transition: evolution and natural history of the genus Lactobacillus. FEMS Mcrobiol. Rev. 41: S27-S48. https://doi.org/10.1093/femsre/fux030
  2. Fidanza M, Panigrahi P, Kollmann TR. 2021. Lactiplantibacillus plantarum-nomad and ideal probiotic. Front. Microbiol. 12: 712236.
  3. Jung S, Lee YJ, Kim M, Kim M, Kwak JH, Lee JW, et al. 2015. Supplementation with two probiotic strains, Lactobacillus curvatus HY7601 and Lactobacillus plantarum KY1032, reduced body adiposity and Lp-PLA2 activity in overweight subjects. J. Funct. Foods 19: 744-752. https://doi.org/10.1016/j.jff.2015.10.006
  4. Kim M, Kim M, Kang M, Yoo HJ, Kim MS, Ahn YT, et al. 2017. Effects of weight loss using supplementation with Lactobacillus strains on body fat and medium-chain acylcarnitines in overweight individuals. Food Funct. 8: 250-261. https://doi.org/10.1039/C6FO00993J
  5. Choi WJ, Dong HJ, Jeong HU, Ryu DW, Song SM, Kim YR, et al. 2020. Lactobacillus plantarum LMT1-48 exerts anti-obesity effect in high-fat diet-induced obese mice by regulating expression of lipogenic genes. Sci. Rep. 10: 869.
  6. Kim H, Lim JJ, Shin HY, Suh HJ, Choi HS. 2021. Lactobacillus plantarum K8-based paraprobiotics suppress lipid accumulation during adipogenesis by the regulation of JAK/STAT and AMPK signaling pathways. J. Funct. Foods 87: 104824.
  7. Lee E, Jung SR, Lee SY, Lee NK, Paik HD, Lim SI. 2018. Lactobacillus plantarum strain Ln4 attenuates diet-induced obesity, insulin resistance, and changes in hepatic mRNA levels associated with glucose and lipid metabolism. Nutrients 10: 643.
  8. Lim JJ, Jung AH, Suh HJ, Choi HS, Kim H. 2022. Lactiplantibacillus plantarum K8-based paraprobiotics prevents obesity and obesity-induced inflammatory responses in high fat diet-fed mice. Food Res. Int. 155: 111066.
  9. Valenlia KB, Morshedi M, Saghafi-Asl M, Shahabi P, Abbasi MM. 2018. Beneficial impacts of Lactobacillus plantarum and inulin on hypothalamic levels of insulin, leptin, and oxidative markers in diabetic rats. J. Funct. Foods 46: 529-537. https://doi.org/10.1016/j.jff.2018.04.069
  10. Buntin N, de Vos WM, Hongpattarakere T. 2017. Variation of mucin adhesion, cell surface characteristics, and molecular mechanisms among Lactobacillus plantarum isolated from different habitats. Appl. Microbiol. Biotechnol. 101: 7663-7674. https://doi.org/10.1007/s00253-017-8482-3
  11. Castaldo C, Vastano V, Siciliano RA, Candela M, Vici M, Muscariello L, et al. 2009. Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin binding protein. Microb. Cell Fact. 8: 14.
  12. Gross G, Snel J, Boekhorst JT, Smits M, Kleerebezem M. 2010. Biodiversity of mannose-specific adhesion in Lactobacillus plantarum revisited: strain-specific domain composition of the mannose-adhesin. Benef. Microb. 1: 61-66. https://doi.org/10.3920/BM2008.1006
  13. Ramiah K, Van Reenen CA, Dicks LMT. 2007. Expression of the mucus adhesion genes Mub and MapA, adhesion-like factor EF-Tu and bacteriocin gene plaA of Lactobacillus plantarum 423, monitored with real-time PCR. Int. J. Food Microbiol. 116: 405-409. https://doi.org/10.1016/j.ijfoodmicro.2007.02.011
  14. Yadav AK, Tyagi A, Kaushik JK, Saklani AC, Grover S, Batish VK. 2013. Role of surface layer collagen binding protein from indigenous Lactobacillus plantarum 91 in adhesion and its anti-adhesion potential against gut pathogen. Microbiol. Res. 168: 639-645. https://doi.org/10.1016/j.micres.2013.05.003
  15. Wang G, Zhang M, Zhao J, Xia Y, Lai PFH, Ai L. 2018. A surface protein from Lactobacillus plantarum increases the adhesion of lactobacillus strains to human epithelial cells. Front. Microbiol. 9: 2858.
  16. Yadav AK, Tyagi A, Kumar A, Panwar S, Grover S, Saklani AC, et al. 2017. Adhesion of lactobacilli and their anti-infectivity potential. Crit. Rev. Food Sci. Nutr. 57: 2042-2056. https://doi.org/10.1080/10408398.2014.918533
  17. Kumar S, Stecher G, Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33: 1870-1874. https://doi.org/10.1093/molbev/msw054
  18. Lee JM, Jang WJ, Park SH, Kong IS. 2020. Antioxidant and gastrointestinal cytoprotective effect of edible polypeptide poly-γ-glutamic acid. Int. J. Biol. Macromol. 153: 616-624. https://doi.org/10.1016/j.ijbiomac.2020.03.050
  19. Lee JM, Jang WJ, Hasan MT, Lee BJ, Kim KW, Lim SG, et al. 2019. Characterization of a Bacillus sp. isolated from fermented food and its synbiotic effect with barley β-glucan as a biocontrol agent in the aquaculture industry. Appl. Microbiol. Biotechnol. 103: 1429-1439. https://doi.org/10.1007/s00253-018-9480-9
  20. Nagaoka S, Hojo K, Murata S, Mori T, Ohshima T, Maeda N. 2008. Interactions between salivary Bifidobacterium adolescentis and other oral bacteria: in vitro coaggregation and coadhesion assays. FEMS Microbiol. Lett. 281: 183-189. https://doi.org/10.1111/j.1574-6968.2008.01092.x
  21. Rafiquzzaman SM, Lee JM, Ahmed R, Lee JH, Kim JM, Kong IS. 2015. Characterisation of the hypoglycaemic activity of glycoprotein purified from the edible brown seaweed, Undaria pinnatifida. Int. J. Food Sci. Technol. 50: 143-150. https://doi.org/10.1111/ijfs.12663
  22. Kim SK, Jang WJ, Kim CE, Lee SJ, Jeon MH, Kim TY, et al. 2021. Characterization of Latilactobacillus curvatus MS2 isolated from Korean traditional fermented seafood and cholesterol reduction effect as synbiotics with isomalto-oligosaccharide in BALB/c mice. Biochem. Biophys. Res. Commun. 571: 125-130. https://doi.org/10.1016/j.bbrc.2021.07.073
  23. Kim EY, Rafiquzzaman SM, Lee JM, Noh G, Jo G, Lee JH, et al. 2015. Structural features of glycoprotein purified from Saccharina japonica and its effects on the selected probiotic properties of Lactobacillus plantarum in Caco-2 cell. J. Appl. Phycol. 27: 965-973. https://doi.org/10.1007/s10811-014-0390-7
  24. Suraiya S, Lee JM, Cho HJ, Jang WJ, Kim DG, Kim YO, et al. 2018. Monascus spp. fermented brown seaweeds extracts enhance biofunctional activities. Food Biosci. 21: 90-99. https://doi.org/10.1016/j.fbio.2017.12.005
  25. Lee JM, Jin CZ, Kang MK, Park SH, Park DJ, Kim DG, et al. 2022. Nocardioides humilatus sp. nov., isolated from farmland soil in the Republic of Korea. Int. J. Syst. Evol. Microbiol. 72: 004928.
  26. Lee JM, Jin CZ, Park SH, Kang MK, Park DJ, Kim CJ. 2021. Nocardioides antri sp. nov., isolated from soil in a rock cave. Curr. Microbiol. 78: 2130-2135. https://doi.org/10.1007/s00284-021-02370-7
  27. Jang WJ, Jeon MH, Lee SJ, Park SY, Lee YS, Noh DI, et al. 2022. Dietary supplementation of Bacillus sp. PM8313 with β-glucan modulates the intestinal microbiota of red sea bream (Pagrus major) to increase growth, immunity, and disease resistance. Front. Immunol. 13: 960554.
  28. Bae M, Cassilly CD, Liu X, Park SM, Tusi BK, Chen X, et al. 2022. Akkermansia muciniphila phospholipid induces homeostatic immune responses. Nature 608: 168-173. https://doi.org/10.1038/s41586-022-04985-7
  29. Morais LH, Schreiber HL, Mazmanian SK. 2021. The gut microbiota-brain axis in behaviour and brain disorders. Nat. Rev. Microbiol. 19: 241-255. https://doi.org/10.1038/s41579-020-00460-0
  30. Verma R, Lee C, Jeun EJ, Yi J, Kim KS, Ghosh A, et al. 2018. Cell surface polysaccharides of Bifidobacterium bifidum induce the generation of Foxp3+ regulatory T cells. Sci. Immunol. 3: eaat6975.
  31. Sanders ME, Merenstein DJ, Reid G, Gibson GR, Rastall RA. 2019. Probiotics and prebiotics in intestinal health and disease: from biology to the clinic. Nat. Rev. Gastroenterol. Hepatol. 16: 605-616. https://doi.org/10.1038/s41575-019-0173-3
  32. Heavey MK, Durmusoglu D, Crook N, Anselmo AC. 2021. Discovery and delivery strategies for engineered live biotherapeutic products. Trends Biotechnol. 40: 354-369. https://doi.org/10.1016/j.tibtech.2021.08.002
  33. Monteagudo-Mera A, Rastall RA, Gibson GR, Charalampopoulos D, Chatzifragkou A. 2019. Adhesion mechanisms mediated by probiotics and prebiotics and their potential impact on human health. Appl. Microbiol. Biotechnol. 103: 6463-6472. https://doi.org/10.1007/s00253-019-09978-7
  34. Pan WH, Li PL, Liu Z. 2006. The correlation between surface hydrophobicity and adherence of Bifidobacterium strains from centenarians' faeces. Anaerobe 12: 148-152. https://doi.org/10.1016/j.anaerobe.2006.03.001
  35. Wardman JF, Bains RK, Rahfeld P, Withers SG. 2022. Carbohydrate-active enzymes (CAZymes) in the gut microbiome. Nat. Rev. Microbiol. 20: 542-556. https://doi.org/10.1038/s41579-022-00712-1
  36. Coyne MJ, Chatzidaki-Livanis M, Paoletti LC, Comstock LE. 2008. Role of glycan synthesis in colonization of the mammalian gut by the bacterial symbiont Bacteroides fragilis. Proc. Natl. Acad. Sci. USA 105: 13099-13104. https://doi.org/10.1073/pnas.0804220105
  37. Goodrich-Blair H. 2021. Interactions of host-associated multispecies bacterial communities. Periodontol. 2000. 86: 14-31. https://doi.org/10.1111/prd.12360
  38. Pyclik M, Srutkova D, Schwarzer M, Gorska S. 2020. Bifidobacteria cell wall-derived exo-polysaccharides, lipoteichoic acids, peptidoglycans, polar lipids and proteins-their chemical structure and biological attributes. Int. J. Biol. Macromol. 147: 333-349. https://doi.org/10.1016/j.ijbiomac.2019.12.227
  39. Kaoutari AE, Armougom F, Gordon JI, Raoult D, Henrissat B. 2013. The abundance and variety of carbohydrate-active enzymes in the human gut microbiota. Nat. Rev. Microbiol. 11: 497-504. https://doi.org/10.1038/nrmicro3050
  40. Turnbaugh PJ, Backhed F, Fulton L, Gordon JI. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host Microbe 3: 213-223. https://doi.org/10.1016/j.chom.2008.02.015
  41. Wang X, Liu F, Gao Y, Xue CH, Li RW, Tang QJ. 2018. Transcriptome analysis revealed anti-obesity effects of the Sodium Alginate in high-fat diet-induced obese mice. Int. J. Biol. Macromol. 115: 861-870. https://doi.org/10.1016/j.ijbiomac.2018.04.042
  42. Fukui H. 2016. Endotoxin and other microbial translocation markers in the blood: a clue to understand leaky gut syndrome. Cell. Mol. Med. 2: 1-14. https://doi.org/10.21767/2573-5365.100023
  43. Harte AL, Varma MC, Tripathi G, McGee KC, Al-Daghri NM, Al-Attas OS, et al. 2012. High fat intake leads to acute postprandial exposure to circulating endotoxin in type 2 diabetic subjects. Diabetes Care 35: 375-382. https://doi.org/10.2337/dc11-1593
  44. Sonnenburg JL, Backhed F. 2016. Diet-microbiota interactions as moderators of human metabolism. Nature 535: 56-64. https://doi.org/10.1038/nature18846
  45. Agus A, Clement K, Sokol H. 2021. Gut microbiota-derived metabolites as central regulators in metabolic disorders. Gut 70: 1174-1182. https://doi.org/10.1136/gutjnl-2020-323071
  46. Bouter KE, van Raalte DH, Groen AK, Nieuwdorp M. 2017. Role of the gut microbiome in the pathogenesis of obesity and obesity-related metabolic dysfunction. Gastroenterology 152: 1671-1678. https://doi.org/10.1053/j.gastro.2016.12.048
  47. Che SY, Yuan JW, Zhang L, Ruan Z, Sun XM, Lu H. 2020. Puerarin prevents epithelial tight junction dysfunction induced by ethanol in Caco-2 cell model. J. Funct. Foods 73:104079.
  48. Aggarwal S, Suzuki T, Taylor WL, Bhargava A, Rao RK. 2011. Contrasting effects of ERK on tight junction integrity in differentiated and under-differentiated Caco-2 cell monolayers. Biochem. J. 433: 51-63. https://doi.org/10.1042/BJ20100249
  49. Davalos-Salas M, Montgomery MK, Reehorst CM, Nightingale R, Ng I, Anderton H, et al. 2019. Deletion of intestinal Hdac3 remodels the lipidome of enterocytes and protects mice from diet-induced obesity. Nat. Commun. 10: 5291.
  50. Bunger M, van den Bosch HM, van der Meijde J, Kersten S, Hooiveld GJ, Muller M. 2007. Genome-wide analysis of PPARα activation in murine small intestine. Physiol. Genomics 30: 192-204. https://doi.org/10.1152/physiolgenomics.00198.2006
  51. Karwad MA, Couch DG, Wright KL, Tufarelli C, Larvin M, Lund J, et al. 2019. Endocannabinoids and endocannabinoid-like compounds modulate hypoxia-induced permeability in CaCo-2 cells via CB1, TRPV1, and PPARα. Biochem. Pharmacol. 168: 465-472. https://doi.org/10.1016/j.bcp.2019.07.017
  52. Kersten S. 2014. Integrated physiology and systems biology of PPARα. Mol. Metab. 3: 354-371. https://doi.org/10.1016/j.molmet.2014.02.002
  53. Huang Y, Zheng Y. 2010. The probiotic Lactobacillus acidophilus reduces cholesterol absorption through the down-regulation of Niemann-Pick C1-like 1 in Caco-2 cells. Br. J. Nutr. 103: 473-478. https://doi.org/10.1017/S0007114509991991
  54. Le B, Yang SH. 2019. Identification of a novel potential probiotic Lactobacillus plantarum FB003 isolated from salted-fermented shrimp and its effect on cholesterol absorption by regulation of NPC1L1 and PPARα. Probiotics Antimicrob. Proteins 11: 785-793. https://doi.org/10.1007/s12602-018-9469-9
  55. Tazi A, Araujo JR, Mulet C, Arena ET, Nigro G, PUdron T, et al. 2018. Disentangling host-microbiota regulation of lipid secretion by enterocytes: insights from commensals Lactobacillus paracasei and Escherichia coli. mBio 9: e01493-18.
  56. Le B, Yang SH. 2019. Effect of potential probiotic Leuconostoc mesenteroides FB111 in prevention of cholesterol absorption by modulating NPC1L1/PPARα/SREBP-2 pathways in epithelial Caco-2 cells. Int. Microbiol. 22: 279-287. https://doi.org/10.1007/s10123-018-00047-z
  57. Iwayanagi Y, Takada T, Tomura F, Yamanashi Y, Terada T, Inui KI, et al. 2011. Human NPC1L1 expression is positively regulated by PPARα. Pharm. Res. 28: 405-412. https://doi.org/10.1007/s11095-010-0294-4
  58. Jang WJ, Kim CE, Jeon MH, Lee SJ, Lee JM, Lee EW, et al. 2021. Characterization of Pediococcus acidilactici FS2 isolated from Korean traditional fermented seafood and its blood cholesterol reduction effect in mice. J. Funct. Foods 87: 104847.
  59. Kellett GL, Brot-Laroche E, Mace OJ, Leturque A. 2008. Sugar absorption in the intestine: the role of GLUT2. Annu. Rev. Nutr. 28: 35-54. https://doi.org/10.1146/annurev.nutr.28.061807.155518
  60. Ait-Omar A, Monteiro-Sepulveda M, Poitou C, Le Gall M, Cotillard A, Gilet J, et al. 2011. GLUT2 accumulation in enterocyte apical and intracellular membranes: a study in morbidly obese human subjects and ob/ob and high fat-fed mice. Diabetes 60: 2598-2607. https://doi.org/10.2337/db10-1740
  61. Krimi RB, Letteron P, Chedid P, Nazaret C, Ducroc R, Marie JC. 2009. Resistin-like molecule-β inhibits SGLT-1 activity and enhances GLUT2-dependent jejunal glucose transport. Diabetes 58: 2032-2038. https://doi.org/10.2337/db08-1786
  62. Baldea LAN, Martineau LC, Benhaddou-Andaloussi A, Arnason JT, Levy E, Haddad PS. 2010. Inhibition of intestinal glucose absorption by anti-diabetic medicinal plants derived from the James Bay Cree traditional pharmacopeia. J. Ethnopharmacol. 132: 473-482. https://doi.org/10.1016/j.jep.2010.07.055
  63. Li T, Yang J, Zhang H, Xie Y, Jin J. 2020. Bifidobacterium from breastfed infant faeces prevent high-fat-diet-induced glucose tolerance impairment, mediated by the modulation of glucose intake and the incretin hormone secretion axis. J. Sci. FoodAgric. 100: 3308-3318. https://doi.org/10.1002/jsfa.10360
  64. Primec M, Skorjanc D, Langerholc T, Micetic-Turk D, Gorenjak M. 2021. Specific Lactobacillus probiotic strains decrease transepithelial glucose transport through GLUT2 downregulation in intestinal epithelial cell models. Nutr. Res. 86: 10-22. https://doi.org/10.1016/j.nutres.2020.11.008