Effects of NS lactobacillus strains on lipid metabolism of rats fed a high-cholesterol diet

Lipids in Health and Disease

Li Wang²  Feng Jin¹  Wei Li³  Tao Wang¹  Xu Hu¹ 

[1] Key Laboratory of Mental Health, Institute of Psychology, Chinese Academy of Sciences, Beijing, China;School of Medicine, Hangzhou Normal University, Zhejiang, China;University of Chinese Academy of Sciences, Beijing, China

关键词: mRNA Expression;    Intestinal microbiota;    Apolipoprotein;    Cholesterol;    NS lactobacillus;   

Others  :  834672
DOI  :  10.1186/1476-511X-12-67

 received in 2013-04-02, accepted in 2013-05-07,  发布年份 2013

【 摘 要 】

Background

Elevated serum cholesterol level is generally considered to be a risk factor for the development of cardiovascular diseases which seriously threaten human health. The cholesterol-lowering effects of lactic acid bacteria have recently become an area of great interest and controversy for many researchers. In this study, we investigated the effects of two NS lactobacillus strains, Lactobacillus plantarum NS5 and Lactobacillus delbrueckii subsp. bulgaricus NS12, on lipid metabolism of rats fed a high cholesterol diet.

Methods

Thirty-two SD rats were assigned to four groups and fed either a normal or a high-cholesterol diet. The NS lactobacillus treated groups received the high-cholesterol diet supplemented with Lactobacillus plantarum NS5 or Lactobacillus delbrueckii subsp. bulgaricus NS12 in drinking water. The rats were sacrificed after a 6-week feeding period. Body weights, visceral organ and fat weights, serum and liver cholesterol and lipid levels, intestinal microbiota and liver mRNA expression levels related to cholesterol metabolism were analyzed. Liver lipid deposition and adipocyte size were evaluated histologically.

Results

Compared with rats fed a high cholesterol diet, serum total cholesterol, low-density lipoprotein cholesterol, apolipoprotein B and free fatty acids levels were decreased and apolipoprotein A-I level was increased in NS5 or NS12 strain treated rats, and with no significant change in high-density lipoprotein cholesterol level. Liver cholesterol and triglyceride levels were also significantly decreased in NS lactobacillus strains treated groups. Meanwhile, the NS lactobacillus strains obviously alleviated hepatic injuries, decreased liver lipid deposition and reduced adipocyte size of high cholesterol diet fed rats. NS lactobacillus strains restored the changes in intestinal microbiota compositions, such as the increase in Bacteroides and the decrease in Clostridium. NS lactobacillus strains also regulated the mRNA expression levels of liver enzymes related to cholesterol metabolism, including the down regulation of acyl-CoA:cholesterol acyltransferase (ACAT) and the upregulation of cholesterol 7α-hydroxylase (CYP7A1).

Conclusion

This study suggested that the two NS lactobacillus strains may affect lipid metabolism and have cholesterol-lowering effects in rats fed a high cholesterol diet.

【 授权许可】

   
2013 Hu et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】

• [1]WHO: Cardiovascular Disease (CVDs). Geneva, Switzerland: Fact sheet N°317; 2011. Available at: http://www.who.int/mediacentre/factsheets/fs317/en/ webcite (accessed on 22 September 2012)
• [2]Manson JE, Tosteson H, Ridker PM, Satterfield S, Hebert P, O’Connor GT, Buring JE, Hennekens CH: The primary prevention of myocardial infarction. N Engl J Med 1992, 326(21):1406-1416.
• [3]Taylor F, Ward K, Moore TH, Burke M, Davey Smith G, Casas JP, Ebrahim S: Statins for the primary prevention of cardiovascular disease. Cochrane Database Syst Rev 2011, 1:CD004816.
• [4]Young VB: The intestinal microbiota in health and disease. Curr Opin Gastroenterol 2012, 28(1):63-69.
• [5]Stepankova R, Tonar Z, Bartova J, Nedorost L, Rossman P, Poledne R, Schwarzer M, Tlaskalova-Hogenova H: Absence of microbiota (germ-free conditions) accelerates the atherosclerosis in ApoE-deficient mice fed standard low cholesterol diet. J Atheroscler Thromb 2010, 17(8):796-804.
• [6]Velagapudi VR, Hezaveh R, Reigstad CS, Gopalacharyulu P, Yetukuri L, Islam S, Felin J, Perkins R, Borén J, Oresic M, Bäckhed F: The gut microbiota modulates host energy and lipid metabolism in mice. J Lipid Res 2010, 51(5):1101-1112.
• [7]Mann GV, Spoerry A: Studies of a surfactant and cholesteremia in the Maasai. Am J Clin Nutr 1974, 27(5):464-469.
• [8]Gilliland SE, Nelson CR, Maxwell C: Assimilation of cholesterol by Lactobacillus acidophilus. Appl Environ Microbiol 1985, 49(2):377-381.
• [9]Fukushima M, Nakano M: Effects of a mixture of organisms, Lactobacillus acidophilus or Streptococcus faecalis on cholesterol metabolism in rats fed on a fat- and cholesterol-enriched diet. Br J Nutr 1996, 76(6):857-867.
• [10]Akalin AS, Gönç S, Düzel S: Influence of yogurt and acidophilus yogurt on serum cholesterol levels in mice. J Dairy Sci 1997, 80(11):2721-2725.
• [11]Nguyen TD, Kang JH, Lee MS: Characterization of Lactobacillus plantarum PH04, a potential probiotic bacterium with cholesterol-lowering effects. Int J Food Microbiol 2007, 113(3):358-361.
• [12]Jeun J, Kim S, Cho SY, Jun HJ, Park HJ, Seo JG, Chung MJ, Lee SJ: Hypocholesterolemic effects of Lactobacillus plantarum KCTC3928 by increased bile acid excretion in C57BL/6 mice. Nutrition 2010, 26(3):321-330.
• [13]Gauffin Cano P, Santacruz A, Moya Á, Sanz Y: Bacteroides uniformis CECT 7771 Ameliorates Metabolic and Immunological Dysfunction in Mice with High-Fat-Diet Induced Obesity. PLoS One 2012, 7(7):e41079.
• [14]Agerbaek M, Gerdes LU, Richelsen B: Hypocholesterolaemic effect of a new fermented milk product in healthy middle-aged men. Eur J Clin Nutr 1995, 49(5):346-352.
• [15]Richelsen B, Kristensen K, Pedersen SB: Long-term (6 months) effect of a new fermented milk product on the level of plasma lipoproteins — a placebo-controlled and double blind study. Eur J Clin Nutr 1996, 50(12):811-815.
• [16]Anderson JW, Gilliland SE: Effect of fermented milk (yogurt) containing Lactobacillus acidophilus L1 on serum cholesterol in hypercholesterolemic humans. J Am Coll Nutr 1999, 18(1):43-50.
• [17]Schaafsma G, Meuling WJ, Van Dokkum W, Bouley C: Effects of a milk product, fermented by Lactobacillus acidophilus and with fructo-oligosaccharides added, on blood lipids in male volunteers. Eur J Clin Nutr 1998, 52(6):436-440.
• [18]Xiao JZ, Kondo S, Takahashi N, Miyaji K, Oshida K, Hiramatsu A, Iwatsuki K, Kokubo S, Hosono A: Effects of milk products fermented by Bifidobacterium longum on blood lipids in rats and healthy adult male volunteers. J Dairy Sci 2003, 86(7):2452-2461.
• [19]Simons LA, Amansec SG, Conway P: Effect of Lactobacillus fermentum on serum lipids in subjects with elevated serum cholesterol. Nutr Metab Cardiovasc Dis 2006, 16(6):531-535.
• [20]Hatakka K, Mutanen M, Holma R, Saxelin M, Korpela R: Lactobacillus rhamnosus LC705 together with Propionibacterium freudenreichii ssp shermanii JS administered in capsules is ineffective in lowering serum lipids. J Am Coll Nutr 2008, 27(4):441-447.
• [21]Pereira DI, Gibson GR: Cholesterol assimilation by lactic acid bacteria and bifidobacteria isolated from the human gut. Appl Environ Microbiol 2002, 68(9):4689-4693.
• [22]Liong MT, Shah NP: Acid and bile tolerance and cholesterol removal ability of lactobacilli strains. J Dairy Sci 2005, 88(1):55-66.
• [23]Lye HS, Rahmat-Ali GR, Liong MT: Mechanisms of cholesterol removal by lactobacilli under conditions that mimic the human gastrointestinal tract. Int Dairy J 2010, 20(3):169-175.
• [24]Lye HS, Rusul G, Liong MT: Removal of cholesterol by lactobacilli via incorporation and conversion to coprostanol. J Dairy Sci 2010, 93(4):1383-1392.
• [25]Begley M, Hill C, Gahan CG: Bile salt hydrolase activity in probiotics. Appl Environ Microbiol 2006, 72(3):1729-1738.
• [26]Ooi LG, Liong MT: Cholesterol-Lowering Effects of Probiotics and Prebiotics: A Review of in Vivo and in Vitro Findings. Int J Mol Sci 2010, 11(6):2499-2522.
• [27]Law MR, Wald NJ, Wu T, Hackshaw A, Bailey A: Systematic underestimation of association between serum cholesterol concentration and ischaemic heart disease in observational studies: data from the BUPA study. BMJ 1994, 308(6925):363-366.
• [28]Kneifel W, Salminen S: Probiotics and Health Claims. New York: John Wiley & Sons, Ltd; 2011.
• [29]Ross R: The pathogenesis of atherosclerosis: a perspective for 1990s. Nature 1993, 362(6423):801-809.
• [30]Millán J, Pintó X, Muñoz A, Zúñiga M, Rubiés-Prat J, Pallardo LF, Masana L, Mangas A, Hernández-Mijares A, González-Santos P, Ascaso JF, Pedro-Botet J: Lipoprotein ratios: Physiological significance and clinical usefulness in cardiovascular prevention. Vasc Health Risk Manag 2009, 5:757-765.
• [31]FAO, WHO: Health and Nutritional Properties of Probiotics in Food including Powder Milk with Live Lactic Acid Bacteria. Cordoba, Argentina: Report of a Joint FAO/WHO Expert Consultation on Evaluation of Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria; 2001. http://www.who.int/foodsafety/publications/fs_management/en/probiotics.pdf webcite
• [32]Walldius G, Junger I: The apoB/apoA-I ratio: a strong, new risk factor for cardiovascular disease and a target for lipid-lowering therapy — a review of evidence. J Intern Med 2006, 259(5):493-519.
• [33]Walldius G, Junger I, Aastveit A, Holme I, Furberg CD, Sniderman AD: The apoB/apoA-I ratio is better than the cholesterol ratios to estimate the balance between the plasma proatherogenic and antiatherogenic lipoproteins and to predict coronary risk. Clin Chem Lab Med 2004, 42(12):1355-1363.
• [34]Semenkovich CF: Fatty acid metabolism and vascular disease. Trends Cardiovas Med 2004, 14(2):72-76.
• [35]Mathew M, Tay E, Cusi K: Elevated plasma free fatty acids increase cardiovascular risk by inducing plasma biomarkers of endothelial activation, myeloperoxidase and PAI-1 in healthy subjects. Cardiovasc Diabetol 2010, 9:9. BioMed Central Full Text
• [36]Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R: Changes in Gut Microbiota Control Metabolic Endotoxemia-Induced Inflammation in High-Fat Diet–Induced Obesity and Diabetes in Mice. Diabetes 2008, 57(6):1470-1481.
• [37]Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI: Obesity alters gut microbial ecology. PNAS 2005, 102(31):11070-11075.
• [38]Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI: An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444(7122):1027-1031.
• [39]Bäckhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI: The gut microbiota as an environmental factor that regulates fat storage. PNAS 2004, 101(44):15718-15723.
• [40]Brown MS, Goldstein JL: A receptor-mediated pathway for cholesterol homeostasis. Science 1986, 232(4746):34-47.
• [41]Goldstein JL, Brown MS: Regulation of the mevalonate pathway. Nature 1990, 343(6257):425-428.
• [42]Shefer S, Hauser S, Lapar V, Mosbach EH: HMG-CoA reductase of intestinal mucosa and liver of the rat. J Lipid Res 1972, 13(3):402-412.
• [43]Spady DK, Cuthbert JA, Willard MN, Meidell RS: Adenovirus-mediated transfer of a gene encoding cholesterol 7a-hydroxylase into hamsters increases hepatic enzyme activity and reduces plasma total and low density lipoprotein (LDL) cholesterol. J Clin Invest 1995, 96(2):700-709.
• [44]Llaverias G, Laguna JC, Alegret M: Pharmacology of the ACAT inhibitor avasimibe (CI-1011). Cardiovasc Drug Rev 2003, 21(1):33-50.