Blueberry supplementation influences the gut microbiota, inflammation, and insulin resistance in high-fat-diet-fed rats

Journal of Nutrition

Volumn 148, Issue 2, 2018, Pages 209-219

  Lee, Sunhye ^a   Keirsey, Katherine I ^a   Kirkland, Rebecca ^a   Grunewald, Zachary I ^a   Fischer, Joan G ^a   de La Serre, Claire B ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

Blueberry; Gut microbiota; Inflammation; Insulin signaling; Intestinal epithelial barrier

Indexed keywords

ACETIC ACID; BETA DEFENSIN 2; FAT DROPLET; HERBACEOUS AGENT; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; ISOPROSTANE DERIVATIVE; MALONALDEHYDE; MUCIN 2; PROPIONIC ACID; RIBOSOME RNA; RNA 16S; TRANSCRIPTION FACTOR RELA; TUMOR NECROSIS FACTOR; ANTHOCYANIN; BACTERIAL DNA; PLANT EXTRACT;

ACTINOBACILLUS; AGGREGATIBACTER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLUEBERRY; CALORIC INTAKE; CELL COUNT; CONTROLLED STUDY; CYTOKINE RELEASE; DNA SEQUENCE; FIRMICUTES; FOOD INTAKE; FUSOBACTERIA; FUSOBACTERIACEAE; GAMMAPROTEOBACTERIA; GASTROINTESTINAL TISSUE; GENE EXPRESSION; GLUCOSE TOLERANCE; INFLAMMATION; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN SIGNALING; INTESTINE FLORA; INTRA-ABDOMINAL FAT; LIPID DIET; LIPID PEROXIDATION; LIVER HISTOLOGY; MALE; MESENTERIC FAT; MICROFLORA; NONHUMAN; OBESITY; OXIDATIVE STRESS; PASTEURELLALES; POLYMERASE CHAIN REACTION; PORPHYROMONADACEAE; POWDER; PROTEIN PHOSPHORYLATION; RAT; RETROPERITONEAL FAT; RNA SEQUENCE; SUPPLEMENTATION; ADIPOSE TISSUE; ADMINISTRATION AND DOSAGE; ANIMAL; BACTERIUM; CHEMISTRY; CLASSIFICATION; DIETARY FIBER; DIETARY SUPPLEMENT; DRUG EFFECT; FRUIT; GENETICS; GLUCOSE TOLERANCE TEST; LIVER; PHYSIOLOGY; WISTAR RAT;

ADIPOSE TISSUE; ANIMALS; ANTHOCYANINS; BACTERIA; BLUEBERRY PLANTS; DIET, HIGH-FAT; DIETARY FIBER; DIETARY SUPPLEMENTS; DNA, BACTERIAL; FRUIT; GASTROINTESTINAL MICROBIOME; GLUCOSE TOLERANCE TEST; INFLAMMATION; INSULIN RESISTANCE; LIVER; MALE; PLANT EXTRACTS; RATS; RATS, WISTAR; SEQUENCE ANALYSIS, DNA;

EID: 85046071105     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.1093/jn/nxx027     Document Type: Article

References (67)

1. Sam S, Haffner S, Davidson MH, D'Agostino RB Sr., Feinstein S, Kondos G, Perez A, Mazzone T. Relation of abdominal fat depots to systemic markers of inflammation in type 2 diabetes. Diabetes Care 2009;32:932-7
2. Cancello R, Tordjman J, Poitou C, Guilhem G, Bouillot JL, Hugol D, Coussieu C, Basdevant A, Bar Hen A, Bedossa P, et al. Increased infiltration of macrophages in omental adipose tissue is associated with marked hepatic lesions in morbid human obesity. Diabetes 2006;55:1554-61
3. Jager J, Gremeaux T, Cormont M, Le Marchand-Brustel Y, Tanti JF. Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 2007;148:241-51
4. Aguirre V, Werner ED, Giraud J, Lee YH, Shoelson SE, White MF. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J Biol Chem 2002;277:1531-7
5. de La Serre CB, Ellis CL, Lee J, Hartman AL, Rutledge JC, Raybould HE. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. Am J Physiol Gastrointest Liver Physiol 2010;299:G440-8
6. Ding S, Chi MM, Scull BP, Rigby R, Schwerbrock NM, Magness S, Jobin C, Lund PK. High-fat diet: bacteria interactions promote intestinal inflammation which precedes and correlates with obesity and insulin resistance in mouse. PLoS One 2010;5:e12191
7. Hamilton MK, Boudry G, Lemay DG, Raybould HE. Changes in intestinal barrier function and gut microbiota in high-fat diet-fed rats are dynamic and region dependent. Am J Physiol Gastrointest Liver Physiol 2015;308:G840-51
8. Tomas J, Mulet C, Saffarian A, Cavin JB, Ducroc R, Regnault B, Kun Tan C, Duszka K, Burcelin R, Wahli W, et al. High-fat diet modifies the PPAR-gamma pathway leading to disruption of microbial and physiological ecosystem in murine small intestine. Proc Natl Acad Sci USA 2016;113:E5934-43
9. Cani PD, Amar J, IglesiasMA, Poggi M, Knauf C, Bastelica D, Neyrinck AM, Fava F, Tuohy KM, Chabo C, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007;56:1761-72
10. Moreira AP, Texeira TFS, Ferreira AB, Peluzio MCG, Alfenas RCG. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr 2012;108:801-9
11. Lawrence T. The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol 2009;1:a001651
12. de La Serre CB, de Lartigue G, Raybould HE. Chronic exposure to low dose bacterial lipopolysaccharide inhibits leptin signaling in vagal afferent neurons. Physiol Behav 2015;139:188-94
13. Cani PD, Knauf C, Iglesias MA, Drucker DJ, Delzenne NM, Burcelin R. Improvement of glucose tolerance and hepatic insulin sensitivity by oligofructose requires a functional glucagon-like peptide 1 receptor. Diabetes 2006;55:1484-90
14. Carvalho BM, Guadagnini D, Tsukumo DM, Schenka AA, Latuf-Filho P, Vassallo J, Dias JC, Kubota LT, Carvalheira JB, Saad MJ. Modulation of gut microbiota by antibiotics improves insulin signalling in high-fat fed mice. Diabetologia 2012;55:2823-34
15. Wu X, Beecher GR, Holden JM, Haytowitz DB, Gebhardt SE, Prior RL. Concentrations of anthocyanins in common foods in the United States and estimation of normal consumption. J Agric Food Chem 2006;54:4069-75
16. Dulebohn RV, Yi W, Srivastava A, Akoh CC, Krewer G, Fischer JG. Effects of blueberry (Vaccinium ashei) on DNA damage, lipid peroxidation, and phase II enzyme activities in rats. J Agric Food Chem 2008;56:11700-6
17. Riso P, Klimis-Zacas D, Del Bo C, Martini D, Campolo J, Vendrame S, Moller P, Loft S, De Maria R, Porrini M. Effect of a wild blueberry (Vaccinium angustifolium) drink intervention on markers of oxidative stress, inflammation and endothelial function in humans with cardiovascular risk factors. Eur J Nutr 2013;52:949-61
18. DeFuria J, Bennett G, Strissel KJ, Perfield JW II, Milbury PE, Greenberg AS, Obin MS. Dietary blueberry attenuates whole-body insulin resistance in high fat-fed mice by reducing adipocyte death and its inflammatory sequelae. J Nutr 2009;139:1510-6
19. Prior RL, Wu X, Gu L, Hager TJ, Hager A, Howard LR. Whole berries versus berry anthocyanins: interactions with dietary fat levels in the C57BL/6J mousemodel of obesity. J Agric Food Chem 2008;56:647-53
20. Prior RL, Wu X, Gu L, Hager T, Hager A, Wilkes S, Howard L. Purified berry anthocyanins but not whole berries normalize lipid parameters in mice fed an obesogenic high fat diet. Mol Nutr Food Res 2009;53:1406-18
21. Prior RL, Wilkes SE, Rogers TR, Khanal RC, Wu X, Howard LR. Purified blueberry anthocyanins and blueberry juice alter development of obesity in mice fed an obesogenic high-fat diet. J Agric Food Chem 2010;58:3970-6
22. Seymour EM, Tanone II, Urcuyo-Llanes DE, Lewis SK, Kirakosyan A, Kondoleon MG, Kaufman PB, Bolling SF. Blueberry intake alters skeletal muscle and adipose tissue peroxisome proliferator-activated receptor activity and reduces insulin resistance in obese rats. JMed Food 2011;14:1511-8
23. Stull AJ, Cash KC, Johnson WD, Champagne CM, Cefalu WT. Bioactives in blueberries improve insulin sensitivity in obese, insulinresistant men and women. J Nutr 2010;140:1764-8
24. Lin Z, Fischer J, Wicker L. Intermolecular binding of blueberry pectinrich fractions and anthocyanin. Food Chem 2016;194:986-93
25. McGhie TK, Stevenson DE. Bioavailability and bioabsorption of anthocyanins. In: Wallace TCGiusti MM, eds. Anthocyanins in health and disease. Boca Raton (FL): CRC Press; 2014. p. 91-113
26. Puupponen-PimiaR, Nohynek L, AlakomiHL, Oksman-Caldentey KM. The action of berry phenolics against human intestinal pathogens. Biofactors 2005;23:243-51
27. Lacombe A, Li RW, Klimis-Zacas D, Kristo AS, Tadepalli S, Krauss E, Young R, Wu VC. Lowbush wild blueberries have the potential to modify gutmicrobiota and xenobiotic metabolism in the rat colon. PLoS One 2013;8:e67497
28. Paturi G, Mandimika T, Butts CA, Zhu S, Roy NC, McNabb WC, Ansell J. Influence of dietary blueberry and broccoli on cecal microbiota activity and colon morphology in mdr1a(-/-) mice, a model of inflammatory bowel diseases. Nutrition 2012;28:324-30
29. Vendrame S, Guglielmetti S, Riso P, Arioli S, Klimis-Zacas D, Porrini M. Six-week consumption of a wild blueberry powder drink increases bifidobacteria in the human gut. J Agric Food Chem 2011;59:12815-20
30. Cummings JH, Pomare EW, Branch WJ, Naylor CP, Macfarlane GT. Short chain fatty acids in human large intestine, portal, hepatic and venous blood. Gut 1987;28:1221-7
31. Tolhurst G, Heffron H, Lam YS, Parker HE, Habib AM, Diakogiannaki E, Cameron J, Grosse J, Reimann F, Gribble FM. Short-chain fatty acids stimulate glucagon-like peptide-1 secretion via the G-protein-coupled receptor FFAR2. Diabetes 2012;61:364-71
32. Xie C, Kang J, Chen JR, Nagarajan S, Badger TM, Wu X. Phenolic acids are in vivo atheroprotective compounds appearing in the serum of rats after blueberry consumption. J Agric Food Chem 2011;59: 10381-7
33. Arndt D, Xia J, Liu Y, Zhou Y, Guo AC, Cruz JA, Sinelnikov I, Budwill K, Nesbo CL, Wishart DS. METAGENassist: a comprehensive web server for comparative metagenomics. Nucleic Acids Res 2012;40:W88-95
34. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60
35. Moreau NM, Goupry SM, Antignac JP, Monteau FJ, Le Bizec BJ, Champ MM, Martin LJ, Dumon HJ. Simultaneous measurement of plasma concentrations and 13C-enrichment of short-chain fatty acids, lactic acid and ketone bodies by gas chromatography coupled to mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 2003;784:395-403
36. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402-8
37. Rui L, Aguirre V, Kim JK, Shulman GI, Lee A, Corbould A, Dunaif A, White MF. Insulin/IGF-1 and TNF-alpha stimulate phosphorylation of IRS-1 at inhibitory Ser307 via distinct pathways. J Clin Invest 2001;107:181-9
38. Chassaing B, Miles-Brown J, Pellizzon M, Ulman E, Ricci M, Zhang L, Patterson AD, Vijay-KumarM, Gewirtz AT. Lack of soluble fiber drives diet-induced adiposity in mice. Am J Physiol Gastrointest Liver Physiol 2015;309:G528-41
39. Boozer CN, Schoenbach G, Atkinson RL. Dietary fat and adiposity: a dose-response relationship in adult male rats fed isocalorically. Am J Physiol 1995;268:E546-50
40. Varga T, Czimmerer Z, Nagy L. PPARs are a unique set of fatty acid regulated transcription factors controlling both lipid metabolism and inflammation. Biochim Biophys Acta 2011;1812:1007-22
41. Daniel H, Gholami AM, Berry D, Desmarchelier C, Hahne H, Loh G, Mondot S, Lepage P, Rothballer M, Walker A, et al. High-fat diet alters gut microbiota physiology in mice. ISME J 2014;8:295-308
42. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 2005;102:11070-5
43. Fak F, Jakobsdottir G, Kulcinskaja E, Marungruang N, Matziouridou C, Nilsson U, Stalbrand H, NymanM. The physico-chemical properties of dietary fibre determine metabolic responses, short-chain Fatty Acid profiles and gut microbiota composition in rats fed low-and high-fat diets. PLoS One 2015;10:e0127252
44. Hidalgo M, Oruna-Concha MJ, Kolida S, Walton GE, Kallithraka S, Spencer JP, de Pascual-Teresa S. Metabolism of anthocyanins by human gut microflora and their influence on gut bacterial growth. J Agric Food Chem 2012;60:3882-90
45. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, et al. The long-term stability of the human gut microbiota. Science 2013;341:1237439
46. Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, Stombaugh J, Knights D, Gajer P, Ravel J, Fierer N, et al. Moving pictures of the human microbiome. Genome Biol 2011;12:R50
47. Morgan XC, Tickle TL, Sokol H, Gevers D, Devaney KL, Ward DV, Reyes JA, Shah SA, LeLeiko N, Snapper SB, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol 2012;13:R79
48. Shao Y, Ding R, Xu B, Hua R, Shen Q, He K, Yao Q. Alterations of gut microbiota after Roux-en-Y gastric bypass and sleeve gastrectomy in Sprague-Dawley rats. Obes Surg 2017;27:295-302
49. Graessler J, Qin Y, Zhong H, Zhang J, Licinio J, Wong ML, Xu A, Chavakis T, Bornstein AB, Ehrhart-Bornstein M, et al. Metagenomic sequencing of the human gutmicrobiome before and after bariatric surgery in obese patients with type 2 diabetes: correlation with inflammatory and metabolic parameters. Pharmacogenomics J 2013;13:514-22
50. Osman N, Adawi D, Ahrné S, Jeppsson B, Molin G. Probiotics and blueberry attenuate the severity of dextran sulfate sodium (DSS)-induced colitis. Dig Dis Sci 2008;53:2464-73
51. Moreno-Navarrete JM, Ortega F, Serino M, Luche E, Waget A, Pardo G, Salvador J, Ricart W, Fruhbeck G, Burcelin R, et al. Circulating lipopolysaccharide-binding protein (LBP) as a marker of obesity-related insulin resistance. Int J Obes (Lond) 2012;36:1442-9
52. Paturi G, Butts CA, Bentley-Hewitt KL, Ansell J. Influence of green and gold kiwifruit on indices of large bowel function in healthy rats. J Food Sci 2014;79:H1611-20
53. Johansson ME, Ambort D, Pelaseyed T, Schutte A, Gustafsson JK, Ermund A, Subramani DB, Holmen-Larsson JM, Thomsson KA Bergstrom JH, et al. Composition and functional role of the mucus layers in the intestine. Cell Mol Life Sci 2011;68:3635-41
54. Ling K. Polyphenol-mediated protective effects against bacterial translocation across intestinal epithelial cells and their mechanisms (Doctoral dissertation). University of Hong Kong, Pokfulam, Hong Kong SAR; 2015. Retrieved from http://dx.doi.org/10.5353/th_b5699899
55. Wehkamp J, Harder J, Wehkamp K, Wehkamp-von Meissner B, Schlee M, Enders C, Sonnenborn U, Nuding S, Bengmark S, Fellermann K, et al. NF-kappaB-and AP-1-mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: a novel effect of a probiotic bacterium. Infect Immun 2004;72:5750-8
56. Henningsson AM, Bjorck IM, Nyman EM. Combinations of indigestible carbohydrates affect short-chain fatty acid formation in the hindgut of rats. J Nutr 2002;132:3098-104
57. Frankel WL, Zhang W, Singh A, Klurfeld DM, Don S, Sakata T, Modlin I, Rombeau JL. Mediation of the trophic effects of short-chain fatty acids on the rat jejunum and colon. Gastroenterology 1994;106:375-80
58. Park JH, Kotani T, Konno T, Setiawan J, Kitamura Y, Imada S, Usui Y, Hatano N, Shinohara M, Saito Y, et al. Promotion of intestinal epithelial cell turnover by commensal bacteria: role of short-chain fatty acids. PLoS One 2016;11:e0156334
59. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol 2006;40:235-43
60. Zhong Y, Nyman M, Fak F. Modulation of gut microbiota in rats fed high-fat diets by processing whole-grain barley to barleymalt. MolNutr Food Res 2015;59:2066-76
61. Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, Misu H, Ota T, Yokoyama M, Honda M, Miyamoto K, et al. Increased oxidative stress precedes the onset of high-fat diet-induced insulin resistance and obesity. Metabolism 2008;57: 1071-7
62. Rains JL, Jain SK. Oxidative stress, insulin signaling, and diabetes. Free Radic Biol Med 2011;50:567-75
63. Vinayagamoorthi R, Bobby Z, Sridhar MG. Antioxidants preserve redox balance and inhibit c-Jun-N-terminal kinase pathway while improving insulin signaling in fat-fed rats: evidence for the role of oxidative stress on IRS-1 serine phosphorylation and insulin resistance. J Endocrinol 2008;197:287-96
64. Wu T, Yin J, Zhang G, Long H, Zheng X. Mulberry and cherry anthocyanin consumption prevents oxidative stress and inflammation in diet-induced obese mice. Mol Nutr Food Res 2016;60:687-94
65. Vella A, Rizza RA. Extrapancreatic effects of GIP and GLP-1. Horm Metab Res 2004;36:830-6
66. Duca FA, Swartz TD, Sakar Y, Covasa M. Decreased intestinal nutrient response in diet-induced obese rats: role of gut peptides and nutrient receptors. Int J Obes (Lond) 2013;37:375-81
67. Milne GL, Dai Q, Roberts LJ II. The isoprostanes-25 years later. Biochim Biophys Acta 2015;1851:433-45