Dietary procyanidins selectively modulate intestinal farnesoid X receptor-regulated gene expression to alter enterohepatic bile acid recirculation: Elucidation of a novel mechanism to reduce triglyceridemia

Molecular Nutrition and Food Research

Volumn 60, Issue 4, 2016, Pages 727-736

  Heidker, Rebecca M ^a   Caiozzi, Gianella C ^a,b   Ricketts, Marie Louise ^a  

^a UNIVERSITY OF NEVADA   (United States)

^b Hospital de Urgencia y Asistencia Pública Dr Alejandro Del Río   (Chile)

Author keywords

Bile acids; Enterohepatic recirculation; Fxr; Procyanidins; Triglycerides

Indexed keywords

BILE ACID; CELL RECEPTOR; CHOLESTEROL; FARNESOID X-ACTIVATED RECEPTOR; GRAPE SEED EXTRACT; PROANTHOCYANIDIN; TRIACYLGLYCEROL;

ANIMAL; BLOOD; C57BL MOUSE; CACO-2 CELL LINE; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; INTESTINE; INTESTINE ABSORPTION; KNOCKOUT MOUSE; MALE; METABOLISM;

ANIMALS; BILE ACIDS AND SALTS; CACO-2 CELLS; CHOLESTEROL; GENE EXPRESSION REGULATION; GRAPE SEED EXTRACT; HUMANS; INTESTINAL ABSORPTION; INTESTINES; MALE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROANTHOCYANIDINS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRIGLYCERIDES;

EID: 84959419800     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201500795     Document Type: Article

References (45)

1. World Health Organization., The top 10 causes of death. Fact sheet N°310, May 2014.
2. Berglund, L., Brunzell, J. D., Goldberg, A. C., Goldberg, I. J. et al., Evaluation and treatment of hypertriglyceridemia: an Endocrine Society clinical practice guideline. J. Clin. Endocrinol. Metab. 2012, 97, 2969-2989.
3. Lu, T. T., Makishima, M., Repa, J. J., Schoonjans, K. et al., Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol. Cell 2000, 6, 507-515.
4. Lefebvre, P., Cariou, B., Lien, F., Kuipers, F. et al., Role of bile acids and bile acid receptors in metabolic regulation. Physiol. Rev. 2009, 89, 147-191.
5. Dawson, P. A., Lan, T., Rao, A., Bile acid transporters. J. Lipid Res. 2009, 50, 2340-2357.
6. Matsubara, T., Li, F., Gonzalez, F. J., FXR signaling in the enterohepatic system. Mol. Cell. Endocrinol. 2013, 368, 17-29.
7. Stroeve, J. H., Brufau, G., Stellaard, F., Gonzalez, F. J. et al., Intestinal FXR-mediated FGF15 production contributes to diurnal control of hepatic bile acid synthesis in mice. Lab. Invest. 2010, 90, 1457-1467.
8. Gonzalez, F. J., Nuclear receptor control of enterohepatic circulation. Comprehensive Physiology 2012, 2, 2811-2828.
9. Makishima, M., Okamoto, A. Y., Repa, J. J., Tu, H. et al., Identification of a nuclear receptor for bile acids. Science 1999, 284, 1362-1365.
10. Parks, D. J., Blanchard, S. G., Bledsoe, R. K., Chandra, G. et al., Bile acids: natural ligands for an orphan nuclear receptor. Science 1999, 284, 1365-1368.
11. Houten, S. M., Volle, D. H., Cummins, C. L., Mangelsdorf, D. J. et al., In vivo imaging of farnesoid X receptor activity reveals the ileum as the primary bile acid signaling tissue. Mol. Endocrinol. 2007, 21, 1312-1323.
12. Dawson, P. A., Haywood, J., Craddock, A. L., Wilson, M. et al., Targeted deletion of the ileal bile acid transporter eliminates enterohepatic cycling of bile acids in mice. J. Biol. Chem. 2003, 278, 33920-33927.
13. Praslickova, D., Torchia, E. C., Sugiyama, M. G., Magrane, E. J. et al., The ileal lipid binding protein is required for efficient absorption and transport of bile acids in the distal portion of the murine small intestine. PloS one 2012, 7, e50810.
14. Dawson, P. A., Hubbert, M., Haywood, J., Craddock, A. L. et al., The heteromeric organic solute transporter alpha-beta, Ostalpha-Ostbeta, is an ileal basolateral bile acid transporter. J. Biol. Chem. 2005, 280, 6960-6968.
15. Inagaki, T., Choi, M., Moschetta, A., Peng, L. et al., Fibroblast growth factor 15 functions as an enterohepatic signal to regulate bile acid homeostasis. Cell Metab. 2005, 2, 217-225.
16. Kim, I., Ahn, S. H., Inagaki, T., Choi, M. et al., Differential regulation of bile acid homeostasis by the farnesoid X receptor in liver and intestine. J. Lipid Res. 2007, 48, 2664-2672.
17. Xie, M. H., Holcomb, I., Deuel, B., Dowd, P. et al., FGF-19, a novel fibroblast growth factor with unique specificity for FGFR4. Cytokine 1999, 11, 729-735.
18. Holt, J. A., Luo, G., Billin, A. N., Bisi, J. et al., Definition of a novel growth factor-dependent signal cascade for the suppression of bile acid biosynthesis. Genes Dev. 2003, 17, 1581-1591.
19. Kok, T., Hulzebos, C. V., Wolters, H., Havinga, R. et al., Enterohepatic circulation of bile salts in farnesoid X receptor-deficient mice: efficient intestinal bile salt absorption in the absence of ileal bile acid-binding protein. J. Biol. Chem. 2003, 278, 41930-41937.
20. Li, H., Chen, F., Shang, Q., Pan, L. et al., FXR-activating ligands inhibit rabbit ASBT expression via FXR-SHP-FTF cascade. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288, G60-G66.
21. Grober, J., Zaghini, I., Fujii, H., Jones, S. A. et al., Identification of a bile acid-responsive element in the human ileal bile acid-binding protein gene. Involvement of the farnesoid X receptor/9-cis-retinoic acid receptor heterodimer. J. Biol. Chem. 1999, 274, 29749-29754.
22. Landrier, J. F., Eloranta, J. J., Vavricka, S. R., Kullak-Ublick, G. A., The nuclear receptor for bile acids, FXR, transactivates human organic solute transporter-alpha and -beta genes. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290, G476-485.
23. Song, K. H., Li, T., Owsley, E., Strom, S. et al., Bile acids activate fibroblast growth factor 19 signaling in human hepatocytes to inhibit cholesterol 7alpha-hydroxylase gene expression. Hepatology 2009, 49, 297-305.
24. Pejic, R. N., Lee, D. T., Hypertriglyceridemia. J. Am. Board Fam. Med. 2006, 19, 310-316.
25. Baiges, I., Palmfeldt, J., Blade, C., Gregersen, N. et al., Lipogenesis is decreased by grape seed proanthocyanidins according to liver proteomics of rats fed a high fat diet. Mol. Cell. Proteomics 2010, 9, 1499-1513.
26. Del Bas, J. M., Ricketts, M. L., Vaque, M., Sala, E. et al., Dietary procyanidins enhance transcriptional activity of bile acid-activated FXR in vitro and reduce triglyceridemia in vivo in a FXR-dependent manner. Mol. Nutr. Food Res. 2009, 53, 805-814.
27. Del Bas, J. M., Ricketts, M. L., Baiges, I., Quesada, H. et al., Dietary procyanidins lower triglyceride levels signaling through the nuclear receptor small heterodimer partner. Mol. Nutr. Food Res. 2008, 52, 1172-1181.
28. Del Bas, J. M., Fernandez-Larrea, J., Blay, M., Ardevol, A. et al., Grape seed procyanidins improve atherosclerotic risk index and induce liver CYP7A1 and SHP expression in healthy rats. FASEB J. 2005, 19, 479-481.
29. Jiao, R., Zhang, Z., Yu, H., Huang, Y. et al., Hypocholesterolemic activity of grape seed proanthocyanidin is mediated by enhancement of bile acid excretion and up-regulation of CYP7A1. J. Nutr. Biochem. 2010, 21, 1134-1139.
30. Baselga-Escudero, L., Blade, C., Ribas-Latre, A., Casanova, E. et al., Chronic supplementation of proanthocyanidins reduces postprandial lipemia and liver miR-33a and miR-122 levels in a dose-dependent manner in healthy rats. J. Nutr. Biochem. 2014, 25, 151-156.
31. Sinal, C. J., Tohkin, M., Miyata, M., Ward, J. M. et al., Targeted disruption of the nuclear receptor FXR/BAR impairs bile acid and lipid homeostasis. Cell 2000, 102, 731-744.
32. Yamakoshi, J., Saito, M., Kataoka, S., Kikuchi, M., Safety evaluation of proanthocyanidin-rich extract from grape seeds. Food Chem. Toxicol. 2002, 40, 599-607.
33. Li-Hawkins, J., Lund, E. G., Turley, S. D., Russell, D. W., Disruption of the oxysterol 7alpha-hydroxylase gene in mice. J. Biol. Chem. 2000, 275, 16536-16542.
34. Modica, S., Murzilli, S., Moschetta, A., Characterizing bile acid and lipid metabolism in the liver and gastrointestinal tract of mice. Current Protocols Mouse Biology 2011, 1, 289-321.
35. Dussault, I., Beard, R., Lin, M., Hollister, K. et al., Identification of gene-selective modulators of the bile acid receptor FXR. J. Biol. Chem. 2003, 278, 7027-7033.
36. Li, G., Lin, W., Araya, J. J., Chen, T. et al., A tea catechin, epigallocatechin-3-gallate, is a unique modulator of the farnesoid X receptor. Toxicol. Appl. Pharmacol. 2012, 258, 268-274.
37. Vergnes, L., Lee, J. M., Chin, R. G., Auwerx, J. et al., Diet1 functions in the FGF15/19 enterohepatic signaling axis to modulate bile acid and lipid levels. Cell Metab. 2013, 17, 916-928.
38. Rucker, R., Storms, D., Interspecies comparisons of micronutrient requirements: metabolic vs. absolute body size. J. Nutr. 2002, 132, 2999-3000.
39. Wang, Y., Chung, S. J., Song, W. O., Chun, O. K., Estimation of daily proanthocyanidin intake and major food sources in the U.S. diet. J. Nutr. 2011, 141, 447-452.
40. Ovaskainen, M. L., Torronen, R., Koponen, J. M., Sinkko, H. et al., Dietary intake and major food sources of polyphenols in Finnish adults. J. Nutr. 2008, 138, 562-566.
41. Alrefai, W. A., Gill, R. K., Bile acid transporters: structure, function, regulation and pathophysiological implications. Pharm. Res. 2007, 24, 1803-1823.
42. Kullak-Ublick, G. A., Stieger, B., Meier, P. J., Enterohepatic bile salt transporters in normal physiology and liver disease. Gastroenterology 2004, 126, 322-342.
43. Lundasen, T., Andersson, E. M., Snaith, M., Lindmark, H. et al., Inhibition of intestinal bile acid transporter Slc10a2 improves triglyceride metabolism and normalizes elevated plasma glucose levels in mice. PloS one 2012, 7, e37787.
44. Quesada, H., Diaz, S., Pajuelo, D., Fernandez-Iglesias, A. et al., The lipid-lowering effect of dietary proanthocyanidins in rats involves both chylomicron-rich and VLDL-rich fractions. Br. J. Nutr. 2012, 108, 208-217.
45. Fang, S., Suh, J. M., Reilly, S. M., Yu, E. et al., Intestinal FXR agonism promotes adipose tissue browning and reduces obesity and insulin resistance. Nat. Med. 2015, 21, 159-165.