Heat killed lactobacillus reuteri GMNL-263 reduces fibrosis effects on the liver and heart in high fat diet-hamsters via TGF-β suppression

International Journal of Molecular Sciences

Volumn 16, Issue 10, 2015, Pages 25881-25896

  Ting, Wei Jen ^a   Kuo, Wei Wen ^a   Hsieh, Dennis Jine Yuan ^b   Yeh, Yu Lan ^c,d   Day, Cecilia Hsuan ^e   Chen, Ya Hui ^f   Chen, Ray Jade ^g   Padma, Viswanadha Vijaya ^h   Chen, Yi Hsing ^f   Huang, Chih Yang ^a,i  

^a CHINA MEDICAL UNIVERSITY   (Taiwan)

^b CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^c CHANGHUA CHRISTIAN HOSPITAL   (Taiwan)

^d JEN TEH JUNIOR COLLEGE OF MEDICINE   (Taiwan)

^e MEIHO UNIVERSITY   (Taiwan)

^f Research and Development Firstep Bioresearch Incorporation   (Taiwan)

^g TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^h BHARATHIAR UNIVERSITY   (India)

ⁱ ASIA UNIVERSITY   (Taiwan)

Author keywords

Cardiovascular diseases; Lactobacillus reuteri GMNL 263; Transforming growth factor

Indexed keywords

CHOLESTEROL 7ALPHA MONOOXYGENASE; CONNECTIVE TISSUE GROWTH FACTOR; FATTY ACID SYNTHASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LOW DENSITY LIPOPROTEIN RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROBIOTIC AGENT; PROTEIN; SMAD3 PROTEIN; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARDIOVASCULAR DISEASE; CONTROLLED STUDY; ECHOCARDIOGRAPHY; FATTY LIVER; FECES ANALYSIS; HAMSTER; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEAT TREATMENT; LACTOBACILLUS REUTERI; LIPID ANALYSIS; LIPID DIET; LIVER FIBROSIS; LIVER PROTECTION; MALE; MASSON TRICHROME STAINING; NONHUMAN; OBESITY; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; STAINING; WESTERN BLOTTING; ADVERSE EFFECTS; ANIMAL; DIET THERAPY; FIBROSIS; GENETICS; HEART DISEASES; METABOLISM; PATHOLOGY;

ANIMALS; CRICETINAE; DIET, HIGH-FAT; FATTY LIVER; FIBROSIS; HEART DISEASES; LACTOBACILLUS REUTERI; MALE; OBESITY; PROBIOTICS; TRANSFORMING GROWTH FACTOR BETA;

EID: 84962469562     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms161025881     Document Type: Article

References (45)

1. Casavalle, P. L.; Lifshitz, F.; Romano; Pandolfo, M.; Caamaño, A.; Boyer, P. M.; Rodríguez, P. N.; Friedman, S. M. Prevalence of dyslipidemia and metabolic syndrome risk factor in overweight and obese children. Pediatr. Endocrinol. Rev. 2014, 12, 213–223.
2. Cortez, M.; Singleton, J. R.; Smith, A. G. Glucose intolerance, metabolic syndrome, and neuropathy. Handb. Clin. Neurol. 2014, 126, 109–122.
3. El-Bassossy, H. M.; Shaltout, H. A. Allopurinol alleviates hypertension and proteinuria in high fructose, high salt and high fat induced model of metabolic syndrome. Transl. Res. 2014, 165, 621–630.
4. Geliebter, A.; Ochner, C. N.; Dambkowski, C. L.; Hashim, S. A. Obesity-related hormones and metabolic risk factors: A randomized trial of diet plus either strength or aerobic training versus diet alone in overweight participants. J. Diabetes Obes. 2014, 1, 1–7.
5. Suh, S.; Baek, J.; Bae, J. C.; Kim, K. N.; Park, M. K.; Kim, D. K.; Cho, N. H.; Lee, M. K. Sex factors in the metabolic syndrome as a predictor of cardiovascular disease. Endocrinol. Metab. 2014, 29, 522–529.
6. Moh, M. C.; Sum, C. F.; Lam, B. C.; Ng, X. W.; Su, C.; Tavintharan, S.; Yeoh, L. Y.; Wong, M. D.; Lee, S. B.; Tang, W. E.; et al. Evaluation of body adiposity index as a predictor of aortic stiffness in multi-ethnic Asian population with type 2 diabetes. Diabetes Vasc. Dis. Res. 2014, 12, 111–118.
7. Ruff, R. R.; Akhund, A.; Adjoian, T.; Kansagra, S. M. Calorie intake, sugar-sweetened beverage consumption, and obesity among New York City adults: Findings from a 2013 population study using dietary recalls. J. Community Health. 2014, 39, 1117–1123.
8. Huang, K. C.; Lee, L. T.; Chen, C. Y.; Sung, P. K. All-cause and cardiovascular disease mortality increased with metabolic syndrome in Taiwanese. Obesity 2008, 16, 684–689.
9. Ma, J. Q.; Ding, J.; Zhao, H.; Liu, C. M. Puerarin attenuates carbon tetrachloride-induced liver oxidative stress and hyperlipidaemia in mouse by JNK/c-Jun/CYP7A1 pathway. Basic Clin. Pharmacol. Toxicol. 2014, 115, 389–395.
10. Tomita, K.; Teratani, T.; Suzuki, T.; Shimizu, M.; Sato, H.; Narimatsu, K.; Usui, S.; Furuhashi, H.; Kimura, A.; Nishiyama, K.; et al. Acyl-CoA: Cholesterol acyltransferase 1 mediates liver fibrosis by regulating free cholesterol accumulation in hepatic stellate cells. J. Hepatol. 2014, 61, 98–106.
11. Fede, G.; Privitera, G.; Tomaselli, T.; Spadaro, L.; Purrello, F. Cardiovascular dysfunction in patients with liver cirrhosis. Ann. Gastroenterol. 2015, 28, 31–40.
12. Yang, C. H.; Ting, W. J.; Day, C. H.; Ju, D. T.; Yeh, Y. L.; Chung, L. C.; Tsai, F. J.; Tsai, C. H.; Tsai, Y.; Huang, C. Y. SHSST cyclodextrin complex prevents the fibrosis effect on CCl₄-induced cirrhotic cardiomyopathy in rats through TGF-β pathway inhibition effects. Int. J. Mol. Sci. 2014, 15, 8037–8048.
13. Owens, A. P., III; Passam, F. H.; Antoniak, S.; Marshall, S. M.; McDaniel, A. L.; Rudel, L.; Williams, J. C.; Hubbard, B. K.; Dutton, J. A.; Wang, J.; et al. Monocyte tissue factor-dependent activation of coagulation in hypercholesterolemic mice and monkeys is inhibited by simvastatin. J. Clin. Investig. 2012, 122, 558–568.
14. Ramspoth, T.; Roehl, A. B.; Macko, S.; Heidenhain, C.; Junge, K.; Binnebösel, M.; Schmeding, M.; Neumann, U. P.; Rossaint, R.; Hein, M. Risk factors for coagulopathy after liver resection. J. Clin. Anesth. 2014, 26, 654–662.
15. Dobaczewski, M.; Chen, W.; Frangogiannis, N. G. Transforming growth factor (TGF)-β signaling in cardiac remodeling. J. Mol. Cell. Cardiol. 2011, 51, 600–606.
16. Leask, A. Potential therapeutic targets for cardiac fibrosis: TGFβ, angiotensin, endothelin, CCN2, and PDGF, partners in fibroblast activation. Circ. Res. 2010, 106, 1675–1680.
17. Dobaczewski, M.; Bujak, M.; Li, N.; Gonzalez-Quesada, C.; Mendoza, L. H.; Wang, X. F.; Frangogiannis, N. G. Smad3 signaling critically regulates fibroblast phenotype and function in healing myocardial infarction. Circ. Res. 2010, 107, 418–428.
18. Panek, A. N.; Posch, M. G.; Alenina, N.; Ghadge, S. K.; Erdmann, B.; Popova, E.; Perrot, A.; Geier, C.; Dietz, R.; Morano, I.; et al. Connective tissue growth factor overexpression in cardiomyocytes promotes cardiac hypertrophy and protection against pressure overload. PLoS ONE 2009, 4, e6743.
19. Ettinger, G.; MacDonald, K.; Reid, G.; Burton, J. P. The influence of the human microbiome and probiotics on cardiovascular health. Gut Microbes 2014, 5, 719–728.
20. Lin, P. P.; Hsieh, Y. M.; Kuo, W. W.; Lin, Y. M.; Yeh, Y. L.; Lin, C. C.; Tsai, F. J.; Tsai, C. H.; Huang, C. Y.; Tsai, C. C. Probiotic-fermented purple sweet potato yogurt activates compensatory IGF-IR/PI3K/Akt survival pathways and attenuates cardiac apoptosis in the hearts of spontaneously hypertensive rats. Int. J. Mol. Med. 2013, 32, 1319–1328.
21. Wang, H. F.; Lin, P. P.; Chen, C. H.; Yeh, Y. L.; Huang, C. C.; Huang, C. Y.; Tsai, C. C. Effects of lactic acid bacteria on cardiac apoptosis are mediated by activation of the phosphatidylinositol-3 kinase/AKT survival-signalling pathway in rats fed a high-fat diet. Int. J. Mol. Med. 2015, 35, 460–470.
22. Sanders, M. E. Probiotics: Definition, sources, selection, and uses. Clin. Infect. Dis. 2008, 2, S58–S61.
23. Elkins, C. A.; Moser, S. A.; Savage, D. C. Genes encoding bile salt hydrolases and conjugated bile salt transporters in Lactobacillus johnsonii 100-100 and other Lactobacillus species. Microbiology 2001, 147, 3403–3412.
24. Joyce, S. A.; MacSharry, J.; Casey, P. G.; Kinsella, M.; Murphy, E. F.; Shanahan, F.; Hill, C.; Gahan, C. G. Regulation of host weight gain and lipid metabolism by bacterial bile acid modification in the gut. Proc. Natl. Acad. Sci. USA 2014, 111, 7421–7426.
25. Kumar, M.; Nagpal, R.; Kumar, R.; Hemalatha, R.; Verma, V.; Kumar, A.; Chakraborty, C.; Singh, B.; Marotta, F.; et al. Cholesterol-lowering probiotics as potential biotherapeutics for metabolic diseases. Exp. Diabetes Res. 2012, 2012, 902917.
26. Tsai, C. C.; Lin, P. P.; Hsieh, Y. M.; Zhang, Z. Y.; Wu, H. C.; Huang, C. C. Cholesterol-lowering potentials of lactic Acid bacteria based on bile-salt hydrolase activity and effect of potent strains on cholesterol metabolism in vitro and in vivo. Sci. World J. 2014, 2014, 690752.
27. Hsieh, F. C.; Lee, C. L.; Chai, C. Y.; Chen, W. T.; Lu, Y. C.; Wu, C. S. Oral administration of Lactobacillus reuteri GMNL-263 improves insulin resistance and ameliorates hepatic steatosis in high fructose-fed rats. Nutr. Metab. 2013, 10, 35.
28. Lu, Y. C.; Yin, L. T.; Chang, W. T.; Huang, J. S. Effect of Lactobacillus reuteri GMNL-263 treatment on renal fibrosis in diabetic rats. J. Biosci. Bioeng. 2010, 110, 709–715.
29. Ting, W. J.; Kuo, W. W.; Kuo, C. H.; Yeh, Y. L.; Shen, C. Y.; Chen, Y. H.; Ho, T. J.; Viswanadha, V. P.; Chen, Y. H.; Huang, C. Y. Supplementary heat-killed Lactobacillus reuteri GMNL-263 ameliorates hyperlipidaemic and cardiac apoptosis in high-fat diet-fed hamsters to maintain cardiovascular function. Br. J. Nutr. 2015, 114, 706–712.
30. Wang, S.; Miller, B.; Matthan, N. R.; Goktas, Z.; Wu, D.; Reed, D. B.; Yin, X.; Grammas, P.; Moustaid-Moussa, N.; Shen, C.L.; et al. Aortic cholesterol accumulation correlates with systemic inflammation but not hepatic and gonadal adipose tissue inflammation in low-density lipoprotein receptor null mice. Nutr. Res. 2013, 33, 1072–1082.
31. Choi, Y. J.; Shin, H. S.; Choi, H. S.; Park, J. W.; Jo, I.; Oh, E. S.; Lee, K. Y.; Lee, B. H.; Johnson, R. J.; Kang, D. H. Uric acid induces fat accumulation via generation of endoplasmic reticulum stress and SREBP-1c activation in hepatocytes. Lab. Investig. 2014, 94, 1114–1125.
32. Yao, X.; Hou, S.; Zhang, D.; Xia, H.; Wang, Y. C.; Jiang, J.; Yin, H.; Ying, H. Regulation of fatty acid composition and lipid storage by thyroid hormone in mouse liver. Cell Biosci. 2014, 4, 38.
33. Yiu, W. F.; Kwan, P. L.; Wong, C. Y.; Kam, T. S.; Chiu, S. M.; Chan, S. W.; Chan, R. Attenuation of fatty liver and prevention of hypercholesterolemia by extract of Curcuma longa through regulating the expression of CYP7A1, LDL-receptor, HO-1, and HMG-CoA reductase. J. Food Sci. 2011, 76, 80–89.
34. Mansoor, S.; Yerian, L.; Kohli, R.; Xanthakos, S.; Angulo, P.; Ling, S.; Lopez, R.; Christine, C. K.; Feldstein, A. E.; Alkhouri, N. The evaluation of hepatic fibrosis scores in children with nonalcoholic fatty liver disease. Dig. Dis. Sci. 2015, 60, 1440–1447.
35. Kim, D.; Kim, W. R.; Kim, H. J.; Therneau, T. M. Association between noninvasive fibrosis markers and mortality among adults with nonalcoholic fatty liver disease in the United States. Hepatology 2013, 57, 1357–1365.
36. Treeprasertsuk, S.; Bjornsson, E.; Enders, F.; Suwanwalaikorn, S.; Lindor, K. D. NAFLD fibrosis score: A prognostic predictor for mortality and liver complications among NAFLD patients. World J. Gastroenterol. 2013, 19, 1219–1229.
37. Yilmaz, Y.; Kurt, R.; Yonal, O.; Polat, N.; Celikel, C. A.; Gurdal, A.; Oflaz, H.; Ozdogan, O.; Imeryuz, N.; Kalayci, C.; et al. Coronary flow reserve is impaired in patients with nonalcoholic fatty liver disease: Association with liver fibrosis. Atherosclerosis 2010, 211, 182–186.
38. Ji, Y. S.; Kim, H. N.; Park, H. J.; Lee, J. E.; Yeo, S. Y.; Yang, J. S.; Park, S. Y.; Yoon, H. S.; Cho, G. S.; Franz, C.M.; et al. Modulation of the murine microbiome with a concomitant anti-obesity effect by Lactobacillus rhamnosus GG and Lactobacillus sakei NR28. Benef. Microbes 2012, 3, 13–22.
39. Tomaro-Duchesneau, C.; Jones, M. L.; Shah, D.; Jain, P.; Saha, S.; Prakash, S. Cholesterol assimilation by Lactobacillus probiotic bacteria: An in vitro investigation. CholesteBiomed. Res. Int. 2014, 2014, 380316.
40. Hemmi, H.; Takeuchi, O.; Kawai, T.; Kaisho, T.; Sato, S.; Sanjo, H.; Matsumoto, M.; Hoshino, K.; Wagner, H.; Takeda, K.; et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408, 740–745.
41. Jung, J. Y.; Shin, J. S.; Lee, S. G.; Rhee, Y. K.; Cho, C. W.; Hong, H. D.; Lee, K. T. Lactobacillus sakei K040706 evokes immunostimulatory effects on macrophages through TLR 2-mediated activation. Int. Immunopharmacol. 2015, 28, 88–96.
42. Fusaru, A. M.; Stănciulescu, C. E.; Surlin, V.; Taisescu, C.; Bold, A.; Pop, O. T.; Baniţă, I. M.; Crăiţoiu, S.; Pisoschi, C. G. Role of innate immune receptors TLR2 and TLR4 as mediators of the inflammatory reaction in human visceral adipose tissue. Rom. J. Morphol. Embryol. 2012, 53, 693–701.
43. Ikeuchi, M.; Tsutsui, H.; Shiomi, T.; Matsusaka, H.; Matsushima, S.; Wen, J.; Kubota, T.; Takeshita, A. Inhibition of TGF-β signaling exacerbates early cardiac dysfunction but prevents late remodeling after infarction. Cardiovasc. Res. 2004, 64, 526–535.
44. Frantz, S.; Hu, K.; Adamek, A.; Wolf, J.; Sallam, A.; Maier, S. K.; Lonning, S.; Ling, H.; Ertl, G.; Bauersachs, J. Transforming growth factor beta inhibition increases mortality and left ventricular dilatation after myocardial infarction. Basic Res. Cardiol. 2008, 103, 485–492.
45. Bujak, M.; Ren, G.; Kweon, H. J.; Dobaczewski, M.; Reddy, A.; Taffet, G.; Wang, X. F.; Frangogiannis, N. G. Essential role of Smad3 in infarct healing and in the pathogenesis of cardiac remodeling. Circulation 2007, 116, 2127–2138.