Antiobesity Effect of Exopolysaccharides Isolated from Kefir Grains

Journal of Agricultural and Food Chemistry

Volumn 65, Issue 46, 2017, Pages 10011-10019

  Lim, Juha ^a   Kale, Madhuvanti ^b   Kim, Dong Hyeon ^c   Kim, Hong Seok ^c   Chon, Jung Whan ^c   Seo, Kun Ho ^c   Lee, Hyeon Gyu ^a   Yokoyama, Wallace ^b   Kim, Hyunsook ^a  

^a Hanyang University   (South Korea)

^b U S DEPARTMENT OF AGRICULTURE   (United States)

^c Konkuk University   (South Korea)

Author keywords

Akkermansia; exopolysaccharides; intestinal microbiota; obesity; glucan

Indexed keywords

ANTHROPOMETRY; CELLULOSE; MAMMALS; POLYSACCHARIDES; TISSUE; VISCOSITY;

AKKERMANSIA; DOSE-DEPENDENT MANNER; EXOPOLYSACCHARIDES; MICRO-CRYSTALLINE CELLULOSE; MICROBIOTAS; OBESITY; PHYSIOLOGICAL PROPERTIES; VERY LOW DENSITY LIPOPROTEINS;

METABOLITES;

GRAIN; PHYSIOLOGY; POLYSACCHARIDES; RHEOLOGICAL PROPERTIES;

ANTIOBESITY AGENT; KEFIR; POLYSACCHARIDE;

3T3-L1 CELL LINE; ADIPOGENESIS; ADIPOSE TISSUE; ANIMAL; BOVINE; C57BL MOUSE; CHEMISTRY; DIET THERAPY; HUMAN; ISOLATION AND PURIFICATION; LIPID DIET; MALE; METABOLISM; MILK; MOUSE; OBESITY; PATHOPHYSIOLOGY;

3T3-L1 CELLS; ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; ANTI-OBESITY AGENTS; CATTLE; DIET, HIGH-FAT; HUMANS; KEFIR; MALE; MICE; MICE, INBRED C57BL; MILK; OBESITY; POLYSACCHARIDES;

EID: 85035051051     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.7b03764     Document Type: Article

References (50)

1. Kopelman, P. G. Obesity as a medical problem Nature 2000, 404, 635-643 10.1038/35007508
2. Komaroff, A. L. The microbiome and risk for obesity and diabetes JAMA 2017, 317, 355-356 10.1001/jama.2016.20099
3. Turnbaugh, P. J.; Hamady, M.; Yatsunenko, T.; Cantarel, B. L.; Duncan, A.; Ley, R. E.; Sogin, M. L.; Jones, W. J.; Roe, B. A.; Affourtit, J. P. A core gut microbiome in obese and lean twins Nature 2009, 457, 480-484 10.1038/nature07540
4. Arora, T.; Anastasovska, J.; Gibson, G.; Tuohy, K.; Sharma, R. K.; Bell, J.; Frost, G. Effect of Lactobacillus acidophilus NCDC 13 supplementation on the progression of obesity in diet-induced obese mice Br. J. Nutr. 2012, 108, 1382-1389 10.1017/S0007114511006957
5. Kadooka, Y.; Sato, M.; Imaizumi, K.; Ogawa, A.; Ikuyama, K.; Akai, Y.; Okano, M.; Kagoshima, M.; Tsuchida, T. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial Eur. J. Clin. Nutr. 2010, 64, 636-643 10.1038/ejcn.2010.19
6. Delzenne, N. M.; Neyrinck, A. M.; Bäckhed, F.; Cani, P. D. Targeting gut microbiota in obesity: effects of prebiotics and probiotics Nat. Rev. Endocrinol. 2011, 7, 639-646 10.1038/nrendo.2011.126
7. Nwodo, U. U.; Green, E.; Okoh, A. I. Bacterial exopolysaccharides: functionality and prospects Int. J. Mol. Sci. 2012, 13, 14002-14015 10.3390/ijms131114002
8. Enikeev, R. Development of a new method for determination of exopolysaccharide quantity in fermented milk products and its application in technology of kefir production Food Chem. 2012, 134, 2437-2441 10.1016/j.foodchem.2012.04.050
9. Ghasemlou, M.; Khodaiyan, F.; Jahanbin, K.; Gharibzahedi, S. M.; Taheri, S. Structural investigation and response surface optimization for improvement of kefiran production yield from a low-cost culture medium Food Chem. 2012, 133, 383-389 10.1016/j.foodchem.2012.01.046
10. Duboc, P.; Mollet, B. Applications of exopolysaccharides in the dairy industry Int. Dairy J. 2001, 11, 759-768 10.1016/S0958-6946(01)00119-4
11. Piermaria, J. A.; Pinotti, A.; Garcia, M. A.; Abraham, A. G. Films based on kefiran, an exopolysaccharide obtained from kefir grain: Development and characterization Food Hydrocolloids 2009, 23, 684-690 10.1016/j.foodhyd.2008.05.003
12. Esnaashari, S. S.; Rezaei, S.; Mirzaei, E.; Afshari, H.; Rezayat, S. M.; Faridi-Majidi, R. Preparation and characterization of kefiran electrospun nanofibers Int. J. Biol. Macromol. 2014, 70, 50-56 10.1016/j.ijbiomac.2014.06.014
13. Maeda, H.; Zhu, X.; Mitsuoka, T. Effects of an exopolysaccharide (kefiran) from Lactobacillus kefiranofaciens on blood glucose in KKAy mice and constipation in SD rats induced by a low-fiber diet Biosci. Microflora 2004, 23, 149-153 10.12938/bifidus.23.149
14. Maeda, H.; Zhu, X.; Omura, K.; Suzuki, S.; Kitamura, S. Effects of an exopolysaccharide (kefiran) on lipids, blood pressure, blood glucose, and constipation BioFactors 2004, 22, 197-200 10.1002/biof.5520220141
15. Rodrigues, K. L.; Caputo, L. R. G.; Carvalho, J. C. T.; Evangelista, J.; Schneedorf, J. M. Antimicrobial and healing activity of kefir and kefiran extract Int. J. Antimicrob. Agents 2005, 25, 404-408 10.1016/j.ijantimicag.2004.09.020
16. Vinderola, G.; Perdigon, G.; Duarte, J.; Farnworth, E.; Matar, C. Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity Cytokine+ 2006, 36, 254-260 10.1016/j.cyto.2007.01.003
17. Uchida, M.; Ishii, I.; Inoue, C.; Akisato, Y.; Watanabe, K.; Hosoyama, S.; Toida, T.; Ariyoshi, N.; Kitada, M. Kefiran reduces atherosclerosis in rabbits fed a high cholesterol diet J. Atheroscler. Thromb. 2010, 17, 980-988 10.5551/jat.4812
18. Medrano, M.; Racedo, S. M.; Rolny, I. S.; Abraham, A. G.; Perez, P. F. Oral administration of kefiran induces changes in the balance of immune cells in a murine model J. Agric. Food Chem. 2011, 59, 5299-5304 10.1021/jf1049968
19. Kim, D.-H.; Chon, J.-W.; Kim, H.; Seo, K.-H. Modulation of intestinal microbiota in mice by kefir administration Food Sci. Biotechnol. 2015, 24, 1397-1403 10.1007/s10068-015-0179-8
20. Kim, D. H.; Kim, H.; Jeong, D.; Kang, I. B.; Chon, J. W.; Kim, H. S.; Song, K. Y.; Seo, K. H. Kefir alleviates obesity and hepatic steatosis in high-fat diet-fed mice by modulation of gut microbiota and mycobiota: targeted and untargeted community analysis with correlation of biomarkers J. Nutr. Biochem. 2017, 44, 35-43 10.1016/j.jnutbio.2017.02.014
21. Kim, D. H.; Jeong, D.; Kang, I. B.; Kim, H.; Song, K. Y.; Seo, K. H. Dual function of Lactobacillus kefiri DH5 in preventing high-fat-diet-induced obesity: direct reduction of cholesterol and upregulation of PPARα in adipose tissue Mol. Nutr. Food Res. 2017, 61, 1700252 10.1002/mnfr.201700252
22. Rimada, P. S.; Abraham, A. G. Comparative study of different methodologies to determine the exopolysaccharide produced by kefir grains in milk and whey Lait 2003, 83, 79-87 10.1051/lait:2002051
23. Miller, G. L. Use of dinitrosalicylic acid reagent for determination of reducing sugar Anal. Chem. 1959, 31, 426-428 10.1021/ac60147a030
24. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 1976, 72, 248-254 10.1016/0003-2697(76)90527-3
25. Piermaria, J. A.; de la Canal, M. L.; Abraham, A. G. Gelling properties of kefiran, a food-grade polysaccharide obtained from kefir grain Food Hydrocolloids 2008, 22, 1520-1527 10.1016/j.foodhyd.2007.10.005
26. Ho, J. N.; Choi, J. W.; Lim, W. C.; Kim, M. K.; Lee, I. Y.; Cho, H. Y. Kefir inhibits 3T3-L1 adipocyte differentiation through down-regulation of adipogenic transcription factor expression J. Sci. Food Agric. 2013, 93, 485-490 10.1002/jsfa.5792
27. Popovich, D. G.; Li, L.; Zhang, W. Bitter melon (Momordica charantia) triterpenoid extract reduces preadipocyte viability, lipid accumulation and adiponectin expression in 3T3-L1 cells Food Chem. Toxicol. 2010, 48, 1619-1626 10.1016/j.fct.2010.03.035
28. German, J. B.; Xu, R.; Walzem, R.; Kinsella, J. E.; Knuckles, B.; Nakamura, M.; Yokoyama, W. H. Effect of dietary fats and barley fiber on total cholesterol and lipoprotein cholesterol distribution in plasma of hamsters Nutr. Res. (N. Y., NY, U. S.) 1996, 16, 1239-1249 10.1016/0271-5317(96)00127-3
29. Zhou, F.; Wu, Z.; Chen, C.; Han, J.; Ai, L.; Guo, B. Exopolysaccharides produced by Rhizobium radiobacter S10 in whey and their rheological properties Food Hydrocolloids 2014, 36, 362-368 10.1016/j.foodhyd.2013.08.016
30. Zhang, Z.; Zhou, Z.; Li, Y.; Zhou, L.; Ding, Q.; Xu, L. Isolated exopolysaccharides from Lactobacillus rhamnosus GG alleviated adipogenesis mediated by TLR2 in mice Sci. Rep. 2016, 6, 36083 10.1038/srep36083
31. Maeda, H.; Mizumoto, H.; Suzuki, M.; Tsuji, K. Effects of kefiran-feeding on fecal cholesterol excretion, hepatic injury and intestinal histamine concentration in rats Biosci. Microflora 2005, 24, 35-40 10.12938/bifidus.24.35
32. Lindström, C.; Holst, O.; Hellstrand, P.; Öste, R.; Andersson, K. E. Evaluation of commercial microbial hydrocolloids concerning their effects on plasma lipids and caecal formation of SCFA in mice Food Hydrocolloids 2012, 28, 367-372 10.1016/j.foodhyd.2012.01.019
33. Huang, M.; Wang, F.; Zhou, X.; Yang, H.; Wang, Y. Hypoglycemic and hypolipidemic properties of polysaccharides from Enterobacter cloacae Z0206 in KKAy mice Carbohydr. Polym. 2015, 117, 91-98 10.1016/j.carbpol.2014.09.008
34. Wanders, A. J.; van den Borne, J. J.; de Graaf, C.; Hulshof, T.; Jonathan, M. C.; Kristensen, M.; Mars, M.; Schols, H. A.; Feskens, E. J. Effects of dietary fibre on subjective appetite, energy intake and body weight: a systematic review of randomized controlled trials Obes. Rev. 2011, 12, 724-739 10.1111/j.1467-789X.2011.00895.x
35. Beck, E. J.; Tosh, S. M.; Batterham, M. J.; Tapsell, L. C.; Huang, X. F. Oat β-glucan increases postprandial cholecystokinin levels, decreases insulin response and extends subjective satiety in overweight subjects Mol. Nutr. Food Res. 2009, 53, 1343-1351 10.1002/mnfr.200800343
36. Ho, J. N.; Choi, J. W.; Lim, W. C.; Kim, M. K.; Lee, I. Y.; Cho, H. Y. Kefir inhibits 3T3-L1 adipocyte differentiation through down-regulation of adipogenic transcription factor expression J. Sci. Food Agric. 2013, 93, 485-490 10.1002/jsfa.5792
37. Kim, D.-H.; Kim, H.; Jeong, D.; Kang, I.-B.; Chon, J.-W.; Kim, H.-S.; Song, K.-Y.; Seo, K.-H. Kefir alleviates obesity and hepatic steatosis in high-fat diet-fed mice by modulation of gut microbiota and mycobiota: targeted and untargeted community analysis with correlation of biomarkers J. Nutr. Biochem. 2017, 44, 35-43 10.1016/j.jnutbio.2017.02.014
38. Kahlon, T.; Chow, F.; Knuckles, B.; Chiu, M. Cholesterol lowering effects in hamsters of b-glucan enriched barley fraction, dehulled whole barley, rice bran, and oat bran and their combinations Cereal Chem. 1993, 70, 435-440
39. Queenan, K. M.; Stewart, M. L.; Smith, K. N.; Thomas, W.; Fulcher, R. G.; Slavin, J. L. Concentrated oat beta-glucan, a fermentable fiber, lowers serum cholesterol in hypercholesterolemic adults in a randomized controlled trial Nutr. J. 2007, 6, 6 10.1186/1475-2891-6-6
40. Behall, K. M.; Scholfield, D. J.; Hallfrisch, J. Effect of beta-glucan level in oat fiber extracts on blood lipids in men and women J. Am. Coll. Nutr. 1997, 16, 46-51 10.1080/07315724.1997.10718648
41. Braaten, J.; Wood, P.; Scott, F.; Wolynetz, M.; Lowe, M.; Bradley-White, P.; Collins, M. Oat beta-glucan reduces blood cholesterol concentration in hypercholesterolemic subjects Eur. J. Clin. Nutr. 1994, 48, 465-474
42. Beer, M.; Arrigoni, E.; Amado, R. Effects of oat gum on blood cholesterol levels in healthy young men Eur. J. Clin. Nutr. 1995, 49, 517-522
43. Wang, L.; Newman, R. K.; Newman, C. W.; Hofer, P. J. Barley beta-glucans alter intestinal viscosity and reduce plasma cholesterol concentrations in chicks J. Nutr. 1992, 122, 2292
44. Othman, R. A.; Moghadasian, M. H.; Jones, P. J. Cholesterol-lowering effects of oat β-glucan Nutr. Rev. 2011, 69, 299-309 10.1111/j.1753-4887.2011.00401.x
45. -/- mice Microbiome 2017, 5, 30 10.1186/s40168-017-0246-x
46. Schneeberger, M.; Everard, A.; Gomez-Valades, A. G.; Matamoros, S.; Ramirez, S.; Delzenne, N. M.; Gomis, R.; Claret, M.; Cani, P. D. Akkermansia muciniphila inversely correlates with the onset of inflammation, altered adipose tissue metabolism and metabolic disorders during obesity in mice Sci. Rep. 2015, 5, 16643 10.1038/srep16643
47. Everard, A.; Belzer, C.; Geurts, L.; Ouwerkerk, J. P.; Druart, C.; Bindels, L. B.; Guiot, Y.; Derrien, M.; Muccioli, G. G.; Delzenne, N. M.; de Vos, W. M.; Cani, P. D. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity Proc. Natl. Acad. Sci. U. S. A. 2013, 110, 9066-9071 10.1073/pnas.1219451110
48. Plovier, H.; Everard, A.; Druart, C.; Depommier, C.; Van Hul, M.; Geurts, L.; Chilloux, J.; Ottman, N.; Duparc, T.; Lichtenstein, L.; Myridakis, A.; Delzenne, N. M.; Klievink, J.; Bhattacharjee, A.; van der Ark, K. C.; Aalvink, S.; Martinez, L. O.; Dumas, M. E.; Maiter, D.; Loumaye, A.; Hermans, M. P.; Thissen, J. P.; Belzer, C.; de Vos, W. M.; Cani, P. D. A purified membrane protein from Akkermansia muciniphila or the pasteurized bacterium improves metabolism in obese and diabetic mice Nat. Med. 2016, 23, 107-113 10.1038/nm.4236
49. Everard, A.; Lazarevic, V.; Gaia, N.; Johansson, M.; Stahlman, M.; Backhed, F.; Delzenne, N. M.; Schrenzel, J.; Francois, P.; Cani, P. D. Microbiome of prebiotic-treated mice reveals novel targets involved in host response during obesity ISME J. 2014, 8, 2116-2130 10.1038/ismej.2014.45
50. Marsland, B. J. Regulating inflammation with microbial metabolites Nat. Med. 2016, 22, 581-583 10.1038/nm.4117