Nutrigenomic analysis of the protective effects of bilberry anthocyanin-rich extract in apo E-deficient mice

Genes and Nutrition

Volumn 5, Issue 4, 2010, Pages 343-353

  Mauray, Aurelie ^a,b   Felgines, Catherine ^c   Morand, Christine ^a   Mazur, Andrzej ^a   Scalbert, Augustin ^a   Milenkovic, Dragan ^a  

^a INRA and University of Auvergne   (France)

^b FERLUX S A   (France)

^c UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

Anthocyanins; Apo E deficient mice; Atherosclerosis; Liver; Microarray

Indexed keywords

ANTHO 50; ANTHOCYANIN; APOLIPOPROTEIN E; BILBERRY EXTRACT; BILE ACID; CHOLESTEROL; CHOLESTEROL 7ALPHA MONOOXYGENASE; HERBACEOUS AGENT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; LIPOPROTEIN LIPASE; MESSENGER RNA; PHOSPHATIDYLCHOLINE STEROL ACYLTRANSFERASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; ATHEROSCLEROSIS; BERRY; BILBERRY; BILE ACID SYNTHESIS; CELL ADHESION; CELL PROLIFERATION; CHOLESTEROL TRANSPORT; CONTROLLED STUDY; DIET SUPPLEMENTATION; DOWN REGULATION; DRUG DETERMINATION; DRUG ISOLATION; DRUG MECHANISM; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNE RESPONSE; LIPID METABOLISM; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUTRIGENOMICS; OXIDATION REDUCTION REACTION; PROTEIN DEFICIENCY; SIGNAL TRANSDUCTION;

IPOMOEA BATATAS; MUS; VACCINIUM MYRTILLUS;

EID: 78649672766     PISSN: 15558932     EISSN: 18653499     Source Type: Journal    
DOI: 10.1007/s12263-010-0171-0     Document Type: Article

References (59)

1. MN Clifford 2000 Anthocyanins-nature, occurrence and dietary burden J Sci Food Agric 80 1063 1072 1:CAS:528:DC%2BD3cXjsFalsLs%3D 10.1002/(SICI)1097- 0010(20000515)80:7<1063::AID-JSFA605>3.0.CO;2-Q (Pubitemid 30319399)
2. NA Nyman JT Kumpulainen 2001 Determination of anthocyanidins in berries and red wine by high-performance liquid chromatography J Agric Food Chem 49 4183 4187 1:CAS:528:DC%2BD3MXlslWlsrw%3D 10.1021/jf010572i 11559107 (Pubitemid 32898669)
3. K Ogawa H Sakakibara R Iwata T Ishii T Sato T Goda K Shimoi S Kumazawa 2008 Anthocyanin composition and antioxidant activity of the Crowberry (Empetrum nigrum) and other berries J Agric Food Chem 56 4457 4462 1:CAS:528: DC%2BD1cXms1Gjt7Y%3D 10.1021/jf800406v 18522397 (Pubitemid 351999369)
4. AK Latti KR Riihinen PS Kainulainen 2008 Analysis of anthocyanin variation in wild populations of bilberry (Vaccinium myrtillus L.) in Finland J Agric Food Chem 56 190 196 1:CAS:528:DC%2BD2sXhsVWqsL7I 10.1021/jf072857m 18072741 (Pubitemid 351187572)
5. F Galvano L La Fauci P Vitaglione V Fogliano L Vanella C Felgines 2007 Bioavailability, antioxidant and biological properties of the natural free-radical scavengers cyanidin and related glycosides Ann Ist Super Sanita 43 382 393 1:CAS:528:DC%2BD1cXjt12nu7o%3D 18209272
6. PJ Mink CG Scrafford LM Barraj L Harnack CP Hong JA Nettleton DR Jacobs Jr 2007 Flavonoid intake and cardiovascular disease mortality: a prospective study in postmenopausal women Am J Clin Nutr 85 895 909 1:CAS:528: DC%2BD2sXjtleqtbc%3D 17344514
7. X Xia W Ling J Ma M Xia M Hou Q Wang H Zhu Z Tang 2006 An anthocyanin-rich extract from black rice enhances atherosclerotic plaque stabilization in apolipoprotein E-deficient mice J Nutr 136 2220 2225 1:CAS:528:DC%2BD28XnvF2msro%3D 16857844 (Pubitemid 44156828)
8. K Miyazaki K Makino E Iwadate Y Deguchi F Ishikawa 2008 Anthocyanins from purple sweet potato ipomoea batatas cultivar ayamurasaki suppress the development of atherosclerotic lesions and both enhancements of oxidative stress and soluble vascular cell adhesion molecule-1 in apolipoprotein e-deficient mice J Agric Food Chem 56 11485 11492 1:CAS:528:DC%2BD1cXhtlemt7fO 10.1021/jf801876n 18986148
9. S Zafra-Stone T Yasmin M Bagchi A Chatterjee JA Vinson D Bagchi 2007 Berry anthocyanins as novel antioxidants in human health and disease prevention Mol Nutr Food Res 51 675 683 1:CAS:528:DC%2BD2sXmvFamsr0%3D 10.1002/mnfr. 200700002 17533652 (Pubitemid 47083678)
10. M Xia M Hou H Zhu J Ma Z Tang Q Wang Y Li D Chi X Yu T Zhao P Han X Xia W Ling 2005 Anthocyanins induce cholesterol efflux from mouse peritoneal macrophages: the role of the peroxisome proliferator-activated receptor {gamma}-liver X receptor {alpha}-ABCA1 pathway J Biol Chem 280 36792 36801 1:CAS:528:DC%2BD2MXhtFKhtL%2FP 10.1074/jbc.M505047200 16107338 (Pubitemid 41587759)
11. DX Hou T Yanagita T Uto S Masuzaki M Fujii 2005 Anthocyanidins inhibit cyclooxygenase-2 expression in LPS-evoked macrophages: structure-activity relationship and molecular mechanisms involved Biochem Pharmacol 70 417 425 1:CAS:528:DC%2BD2MXlvVWms7o%3D 10.1016/j.bcp.2005.05.003 15963474 (Pubitemid 40905113)
12. ES Kao TH Tseng HJ Lee KC Chan CJ Wang 2009 Anthocyanin extracted from Hibiscus attenuate oxidized LDL-mediated foam cell formation involving regulation of CD36 gene Chem Biol Interact 179 212 218 1:CAS:528: DC%2BD1MXjsFajsb0%3D 10.1016/j.cbi.2009.01.009 19330881
13. MC Lazze R Pizzala P Perucca O Cazzalini M Savio L Forti V Vannini L Bianchi 2006 Anthocyanidins decrease endothelin-1 production and increase endothelial nitric oxide synthase in human endothelial cells Mol Nutr Food Res 50 44 51 1:CAS:528:DC%2BD28XhsFehsr8%3D 10.1002/mnfr.200500134 16288501 (Pubitemid 43158372)
14. J Chen T Uto S Tanigawa T Kumamoto M Fujii DX Hou 2008 Expression profiling of genes targeted by bilberry (Vaccinium myrtillus) in macrophages through DNA microarray Nutr Cancer 60 Suppl 1 43 50 1:CAS:528: DC%2BD1MXjvV2gtw%3D%3D 10.1080/01635580802381279 19003580
15. M Lefevre JE Wiles X Zhang LR Howard S Gupta AA Smith ZY Ju JP DeLany 2008 Gene expression microarray analysis of the effects of grape anthocyanins in mice: a test of a hypothesis-generating paradigm Metabolism 57 S52 S57 1:CAS:528:DC%2BD1cXnt1emtb0%3D 10.1016/j.metabol.2008.03.005 18555855 (Pubitemid 351814699)
16. R Ohashi H Mu X Wang Q Yao C Chen 2005 Reverse cholesterol transport and cholesterol efflux in atherosclerosis Qjm 98 845 856 1:STN:280: DC%2BD2MnhvVehsw%3D%3D 10.1093/qjmed/hci136 16258026 (Pubitemid 43071450)
17. PC Choy YL Siow D Mymin OK 2004 Lipids and atherosclerosis Biochem Cell Biol 82 212 224 1:CAS:528:DC%2BD2cXjtVehs74%3D 10.1139/o03-085 15052339 (Pubitemid 38584583)
18. S Talavera C Felgines O Texier C Besson A Mazur JL Lamaison C Remesy 2006 Bioavailability of a bilberry anthocyanin extract and its impact on plasma antioxidant capacity in rats J Sci Food Agric 86 90 97 1:CAS:528: DC%2BD2MXhtlekur7O 10.1002/jsfa.2327 (Pubitemid 41820210)
19. VL Singleton JA Rossi 1965 Colorimetry of total phenolics with phospomolybdic-phosphotungstic reagents Am J Enol Vitic 16 144 158 1:CAS:528:DyaF28Xit1yhuw%3D%3D
20. A Mazur C Remesy E Gueux MA Levrat C Demigne 1990 Effects of diets rich in fermentable carbohydrates on plasma lipoprotein levels and on lipoprotein catabolism in rats J Nutr 120 1037 1045 1:CAS:528:DyaK3cXlvFShs74%3D 2168942
21. D Huang B Ou M Hampsch-Woodill JA Flanagan RL Prior 2002 High-throughput assay of oxygen radical absorbance capacity (ORAC) using a multichannel liquid handling system coupled with a microplate fluorescence reader in 96-well format J Agric Food Chem 50 4437 4444 1:CAS:528:DC%2BD38XkvF2ksr0%3D 10.1021/jf0201529 12137457 (Pubitemid 34823962)
22. R Pandey RK Guru DW Mount 2004 Pathway Miner: extracting gene association networks from molecular pathways for predicting the biological significance of gene expression microarray data Bioinformatics 20 2156 2158 1:CAS:528: DC%2BD2cXnsVyiur0%3D 10.1093/bioinformatics/bth215 15145817 (Pubitemid 39236574)
23. Auclair S, Milenkovic D, Besson C, Chauvet S, Gueux E, Morand C, Mazur A, Scalbert A (2008) Catechin reduces atherosclerotic lesion development in apo E-deficient mice: a transcriptomic study. Atherosclerosis
24. KJ Livak TD Schmittgen 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method Methods 25 402 408 1:CAS:528:DC%2BD38XhtFelt7s%3D 10.1006/meth.2001.1262 11846609 (Pubitemid 34164012)
25. M Garcia-Alonso AM Minihane G Rimbach JC Rivas-Gonzalo S de Pascual-Teresa 2009 Red wine anthocyanins are rapidly absorbed in humans and affect monocyte chemoattractant protein 1 levels and antioxidant capacity of plasma J Nutr Biochem 20 521 529 1:CAS:528:DC%2BD1MXnt1Glsrc%3D 10.1016/j.jnutbio.2008.05.011 18789665
26. M Garcia-Alonso G Rimbach M Sasai M Nakahara S Matsugo Y Uchida JC Rivas-Gonzalo S De Pascual-Teresa 2005 Electron spin resonance spectroscopy studies on the free radical scavenging activity of wine anthocyanins and pyranoanthocyanins Mol Nutr Food Res 49 1112 1119 1:CAS:528: DC%2BD28XltVKgsQ%3D%3D 10.1002/mnfr.200500100 16254886 (Pubitemid 43008394)
27. M Xia WH Ling J Ma DD Kitts J Zawistowski 2003 Supplementation of diets with the black rice pigment fraction attenuates atherosclerotic plaque formation in apolipoprotein e deficient mice J Nutr 133 744 751 1:CAS:528: DC%2BD3sXhvFyltbk%3D 12612147
28. B Angelin 1995 1994 Mack-Forster award lecture. Review. Studies on the regulation of hepatic cholesterol metabolism in humans Eur J Clin Invest 25 215 224 1:CAS:528:DyaK2MXlslCiurY%3D 10.1111/j.1365-2362.1995.tb01552.x 7601197
29. J Shepherd 2001 The role of exogenous pathway in hypercholesterolemia Eur Heart J Suppl 3 E2 E5 1:CAS:528:DC%2BD3MXos12murY%3D 10.1016/S1520-765X(01) 90105-1
30. JH Miyake XT Duong-Polk JM Taylor EZ Du LW Castellani AJ Lusis RA Davis 2002 Transgenic expression of cholesterol-7-alpha-hydroxylase prevents atherosclerosis in C57BL/6 J mice Arterioscler Thromb Vasc Biol 22 121 126 1:CAS:528:DC%2BD38XmslOitA%3D%3D 10.1161/hq0102.102588 11788471 (Pubitemid 34076242)
31. JM Del Bas J Fernandez-Larrea M Blay A Ardevol MJ Salvado L Arola C Blade 2005 Grape seed procyanidins improve atherosclerotic risk index and induce liver CYP7A1 and SHP expression in healthy rats Faseb J 19 479 481 1:CAS:528:DC%2BD2MXit1Kkt7s%3D 15637110
32. MH Hofker BJ van Vlijmen LM Havekes 1998 Transgenic mouse models to study the role of APOE in hyperlipidemia and atherosclerosis Atherosclerosis 137 1 11 1:CAS:528:DyaK1cXitlSmurk%3D 10.1016/S0021-9150(97)00266-9 9568731 (Pubitemid 28175371)
33. KS Meir E Leitersdorf 2004 Atherosclerosis in the apolipoprotein-E- deficient mouse: a decade of progress Arterioscler Thromb Vasc Biol 24 1006 1014 1:CAS:528:DC%2BD2cXkt1Ogsbk%3D 10.1161/01.ATV.0000128849.12617.f4 15087308 (Pubitemid 38737824)
34. J Jawien P Nastalek R Korbut 2004 Mouse models of experimental atherosclerosis J Physiol Pharmacol 55 503 517 1:CAS:528:DC%2BD2cXptlKhsbs%3D 15381823
35. TF Daniels KM Killinger JJ Michal RW Wright Jr Z Jiang 2009 Lipoproteins, cholesterol homeostasis and cardiac health Int J Biol Sci 5 474 488 1:CAS:528:DC%2BD1MXosFWgurk%3D 19584955
36. E Zsigmond Y Fuke L Li K Kobayashi L Chan 1998 Resistance of chylomicron and VLDL remnants to post-heparin lipolysis in ApoE-deficient mice: the role of apoE in lipoprotein lipase-mediated lipolysis in vivo and in vitro J Lipid Res 39 1852 1861 1:CAS:528:DyaK1cXlvVyrsrc%3D 9741698
37. G Lambert N Sakai BL Vaisman EB Neufeld B Marteyn CC Chan B Paigen E Lupia A Thomas LJ Striker J Blanchette-Mackie G Csako JN Brady R Costello GE Striker AT Remaley HB Brewer Jr S Santamarina-Fojo 2001 Analysis of glomerulosclerosis and atherosclerosis in lecithin cholesterol acyltransferase-deficient mice J Biol Chem 276 15090 15098 1:CAS:528: DC%2BD3MXjs1Orsb4%3D 10.1074/jbc.M008466200 11278414
38. G Lambert CJ Sinal 2000 Nuclear receptors LXR and FXR control cholesterol and bile acid metabolism Med Sci (Paris) 16 1456 1458
39. ML Hubbert Y Zhang FY Lee PA Edwards 2007 Regulation of hepatic Insig-2 by the farnesoid X receptor Mol Endocrinol 21 1359 1369 1:CAS:528: DC%2BD2sXmtlKlt7c%3D 10.1210/me.2007-0089 17440045 (Pubitemid 46984742)
40. S Modica A Moschetta 2006 Nuclear bile acid receptor FXR as pharmacological target: are we there yet? FEBS Lett 580 5492 5499 1:CAS:528:DC%2BD28XhtVajsr7F 10.1016/j.febslet.2006.07.082 16904670 (Pubitemid 44488553)
41. N Matsumoto K Okushio Y Hara 1998 Effect of black tea polyphenols on plasma lipids in cholesterol-fed rats J Nutr Sci Vitaminol (Tokyo) 44 337 342 1:CAS:528:DyaK1cXjtlKqt7o%3D
42. SM Jeon YB Park MS Choi 2004 Antihypercholesterolemic property of naringin alters plasma and tissue lipids, cholesterol-regulating enzymes, fecal sterol and tissue morphology in rabbits Clin Nutr 23 1025 1034 1:CAS:528:DC%2BD2cXnslKlt7s%3D 10.1016/j.clnu.2004.01.006 15380892 (Pubitemid 39243016)
43. S Gorinstein H Leontowicz M Leontowicz J Drzewiecki Z Jastrzebski MS Tapia E Katrich S Trakhtenberg 2005 Red Star Ruby (Sunrise) and blond qualities of Jaffa grapefruits and their influence on plasma lipid levels and plasma antioxidant activity in rats fed with cholesterol-containing and cholesterol-free diets Life Sci 77 2384 2397 1:CAS:528:DC%2BD2MXpsVWktLs%3D 10.1016/j.lfs.2004.12.049 15964022 (Pubitemid 41206865)
44. K Osada T Suzuki Y Kawakami M Senda A Kasai M Sami Y Ohta T Kanda M Ikeda 2006 Dose-dependent hypocholesterolemic actions of dietary apple polyphenol in rats fed cholesterol Lipids 41 133 139 1:CAS:528:DC%2BD28Xjt1Grsbs%3D 10.1007/s11745-006-5081-y 17707979
45. N Ferre M Martinez-Clemente M Lopez-Parra A Gonzalez-Periz R Horrillo A Planaguma J Camps J Joven A Tres F Guardiola R Bataller V Arroyo J Claria 2009 Increased susceptibility to exacerbated liver injury in hypercholesterolemic ApoE-deficient mice: potential involvement of oxysterols Am J Physiol Gastrointest Liver Physiol 296 G553 G562 1:CAS:528:DC%2BD1MXjtFGrtbs%3D 10.1152/ajpgi.00547.2007 19136384
46. A Chait CY Han JF Oram JW Heinecke 2005 Thematic review series: the immune system and atherogenesis. Lipoprotein-associated inflammatory proteins: markers or mediators of cardiovascular disease? J Lipid Res 46 389 403 1:CAS:528:DC%2BD2MXit1SlsLw%3D
47. R Kleemann T Kooistra 2005 HMG-CoA reductase inhibitors: effects on chronic subacute inflammation and onset of atherosclerosis induced by dietary cholesterol Curr Drug Targets Cardiovasc Haematol Disord 5 441 453 1:CAS:528:DC%2BD28XitlylsQ%3D%3D 10.2174/156800605774962077 16503864 (Pubitemid 43012568)
48. Kleemann R, Verschuren L, van Erk MJ, Nikolsky Y, Cnubben NH, Verheij ER, Smilde AK, Hendriks HF, Zadelaar S, Smith GJ, Kaznacheev V, Nikolskaya T, Melnikov A, Hurt-Camejo E, van der Greef J, van Ommen B, Kooistra T (2007) Atherosclerosis and liver inflammation induced by increased dietary cholesterol intake: a combined transcriptomics and metabolomics analysis. Genome Biol 8:R200
49. E Titos J Claria A Planaguma M Lopez-Parra A Gonzalez-Periz J Gaya R Miquel V Arroyo J Rodes 2005 Inhibition of 5-lipoxygenase-activating protein abrogates experimental liver injury: role of Kupffer cells J Leukoc Biol 78 871 878 1:CAS:528:DC%2BD2MXhtVOrtbbL 10.1189/jlb.1204747 16033810 (Pubitemid 41384403)
50. Kmiec Z (2001) Cooperation of liver cells in health and disease. Adv Anat Embryol Cell Biol 161:III-XIII (1-151)
51. EB Friedrich AM Tager E Liu A Pettersson C Owman L Munn AD Luster RE Gerszten 2003 Mechanisms of leukotriene B4-triggered monocyte adhesion Arterioscler Thromb Vasc Biol 23 1761 1767 1:CAS:528:DC%2BD3sXnslWit7w%3D 10.1161/01.ATV.0000092941.77774.3C 12947016 (Pubitemid 37254860)
52. CL Bone-Larson KJ Simpson LM Colletti NW Lukacs SC Chen S Lira SL Kunkel CM Hogaboam 2000 The role of chemokines in the immunopathology of the liver Immunol Rev 177 8 20 1:CAS:528:DC%2BD3cXptVensbo%3D 10.1034/j.1600-065X.2000. 17703.x 11138788
53. KJ Simpson NC Henderson CL Bone-Larson NW Lukacs CM Hogaboam SL Kunkel 2003 Chemokines in the pathogenesis of liver disease: so many players with poorly defined roles Clin Sci (Lond) 104 47 63 1:CAS:528:DC%2BD3sXitVyjsw%3D%3D 10.1042/CS20020137 (Pubitemid 36249923)
54. G Ramadori T Armbrust 2001 Cytokines in the liver Eur J Gastroenterol Hepatol 13 777 784 1:CAS:528:DC%2BD3MXlvFais7o%3D 10.1097/00042737-200107000- 00004 11474306 (Pubitemid 32656590)
55. WH Lee SH Kim Y Lee BB Lee B Kwon H Song BS Kwon JE Park 2001 Tumor necrosis factor receptor superfamily 14 is involved in atherogenesis by inducing proinflammatory cytokines and matrix metalloproteinases Arterioscler Thromb Vasc Biol 21 2004 2010 1:CAS:528:DC%2BD38XjtVOk 10.1161/hq1201.098945 11742877 (Pubitemid 34219754)
56. T Sampietro F Bigazzi G Rossi B Dal Pino MR Puntoni F Sbrana E Chella A Bionda 2005 Upregulation of the immune system in primary hypercholesterolemia: effect of atorvastatin therapy J Intern Med 257 523 530 1:CAS:528: DC%2BD2MXlslClt70%3D 10.1111/j.1365-2796.2005.01488.x 15910556 (Pubitemid 40776512)
57. MS Wright NJ Sund TG Abrahamsen 2001 Modulation of C3 gene expression in HepG2 human hepatoma cells Immunol Lett 76 119 123 1:CAS:528: DC%2BD3MXitF2kurw%3D 10.1016/S0165-2478(01)00180-8 11274730 (Pubitemid 32234389)
58. JM Stapp V Sjoelund HA Lassiter RC Feldhoff PW Feldhoff 2005 Recombinant rat IL-1beta and IL-6 synergistically enhance C3 mRNA levels and complement component C3 secretion by H-35 rat hepatoma cells Cytokine 30 78 85 1:CAS:528:DC%2BD2MXivVSnt7g%3D 10.1016/j.cyto.2004.12.007 15804599 (Pubitemid 40432633)
59. M Garcia-Alonso G Rimbach JC Rivas-Gonzalo S De Pascual-Teresa 2004 Antioxidant and cellular activities of anthocyanins and their corresponding vitisins A-studies in platelets, monocytes, and human endothelial cells J Agric Food Chem 52 3378 3384 1:CAS:528:DC%2BD2cXjslOhsrY%3D 10.1021/jf035360v 15161201