Effect of dark sweet cherry powder consumption on the gut microbiota, short-chain fatty acids, and biomarkers of gut health in obese db/db mice

PeerJ - Tập 6 - Trang e4195
José F. García-Mazcorro1,2, Nara Nunes Lage3,4, Susanne U. Mertens‐Talcott3, Stephen T. Talcott3, Boon P. Chew3, Scot E. Dowd5, Jorge R. Kawas6, Giuliana Noratto3
1Faculty of Veterinary Medicine, Universidad Autónoma de Nuevo León, General Escobedo, Mexico
2Research and Development, MNA de Mexico, San Nicolas de los Garza, Mexico
3Department of Nutrition and Food Science, Texas A&M University, College Station, TX, United States of America
4Research Center in Biological Sciences, Federal University of Ouro Preto, Minas Gerais, Brazil
5Molecular Research LP, Shallowater, TX, United States of America
6Faculty of Agronomy, Universidad Autónoma de Nuevo León, General Escobedo, Mexico

Tóm tắt

Cherries are fruits containing fiber and bioactive compounds (e.g., polyphenolics) with the potential of helping patients with diabetes and weight disorders, a phenomenon likely related to changes in the complex host-microbiota milieu. The objective of this study was to investigate the effect of cherry supplementation on the gut bacterial composition, concentrations of caecal short-chain fatty acids (SCFAs) and biomarkers of gut health using an in vivo model of obesity. Obese diabetic (db/db) mice received a supplemented diet with 10% cherry powder (supplemented mice, n = 12) for 12 weeks; obese (n = 10) and lean (n = 10) mice served as controls and received a standard diet without cherry. High-throughput sequencing of the 16S rRNA gene and quantitative real-time PCR (qPCR) were used to analyze the gut microbiota; SCFAs and biomarkers of gut health were also measured using standard techniques. According to 16S sequencing, supplemented mice harbored a distinct colonic microbiota characterized by a higher abundance of mucin-degraders (i.e., Akkermansia) and fiber-degraders (the S24-7 family) as well as lower abundances of Lactobacillus and Enterobacteriaceae. Overall this particular cherry-associated colonic microbiota did not resemble the microbiota in obese or lean controls based on the analysis of weighted and unweighted UniFrac distance metrics. qPCR confirmed some of the results observed in sequencing, thus supporting the notion that cherry supplementation can change the colonic microbiota. Moreover, the SCFAs detected in supplemented mice (caproate, methyl butyrate, propionate, acetate and valerate) exceeded those concentrations detected in obese and lean controls except for butyrate. Despite the changes in microbial composition and SCFAs, most of the assessed biomarkers of inflammation, oxidative stress, and intestinal health in colon tissues and mucosal cells were similar in all obese mice with and without supplementation. This paper shows that dietary supplementation with cherry powder for 12 weeks affects the microbiota and the concentrations of SCFAs in the lower intestinal tract of obese db/db diabetic mice. These effects occurred in absence of differences in most biomarkers of inflammation and other parameters of gut health. Our study prompts more research into the potential clinical implications of cherry consumption as a dietary supplement in diabetic and obese human patients.

Từ khóa


Tài liệu tham khảo

Barcenilla, 2000, Phylogenetic relationships of butyrate-producing bacteria from the human gut, Applied Environmental Microbiology, 66, 1654, 10.1128/AEM.66.4.1654-1661.2000

Baron, 2017, Pharmacokinetic profile of bilberry anthocyanins in rats and the role of glucose transporters: LC-MS/MS and computational studies, Journal of Pharmaceutical and Biomedical Analysis, 144, 112, 10.1016/j.jpba.2017.04.042

Bell, 2014, Faecal microbiota of cats with insulin-treated diabetes mellitus, PLOS ONE, 9, e108729, 10.1371/journal.pone.0108729

Belzer, 2016, Microbes inside-from diversity to function: the case of Akkermansia, ISME Journal, 6, 1449, 10.1038/ismej.2012.6

Bergström, 2012, Introducing Gut Low-Density Array (GULDA)—a validated approach for qPCR-based intestinal microbial community analysis, FEMS Microbiology Letters, 337, 38, 10.1111/1574-6968.12004

Berry, 2012, Phylotype-level 16S rRNA analysis reveals new bacterial indicators of health state in acute murine colitis, ISME Journal, 6, 2091, 10.1038/ismej.2012.39

Berry, 2013, Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing, Proceedings of the National Academy of Sciences of the United States of America, 110, 4720, 10.1073/pnas.1219247110

Borton, 2017, Chemical and pathogen-induced inflammation disrupt the murine intestinal microbiome, Microbiome, 5, 47, 10.1186/s40168-017-0264-8

Budak, 2017, Bioactive components of Prunus avium L. black gold (red cherry) and Prunus avium L. stark gold (white cherry) juices, wines and vinegars, Journal of Food Science and Technology, 54, 62, 10.1007/s13197-016-2434-2

Caesar, 2015, Crosstalk between gut microbiota and dietary lipids aggravates WAT inflammation through TLR signaling, Cell Metabolism, 22, 658, 10.1016/j.cmet.2015.07.026

Campos, 2012, Prebiotic effects of yacon (Smallanthus sonchifolius Poepp. & Endl), a source of fructooligosaccharides and phenolic compounds with antioxidant activity, Food Chemistry, 135, 1592, 10.1016/j.foodchem.2012.05.088

Caporaso, 2012, Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms, ISME Journal, 6, 1621, 10.1038/ismej.2012.8

Chen, 2017, Fiber-utilizing capacity varies in Prevotella- versus Bacteroides-dominated gut microbiota, Scientific Reports, 7, 2594, 10.1038/s41598-017-02995-4

Cho, 2017, Terpenes from forests and human health, Toxicological Research, 33, 97, 10.5487/TR.2017.33.2.097

Cires, 2017, The gastrointestinal tract as a key target organ for the health-promoting effects of dietary proanthocyanidins, Frontiers in Nutrition, 3, 57, 10.3389/fnut.2016.00057

Condezo-Hoyos, 2014, Assessing non-digestible compounds in apple cultivars and their potential as modulators of obese faecal microbiota in vitro, Food Chemistry, 161, 208, 10.1016/j.foodchem.2014.03.122

Conlon, 2014, The impact of diet and lifestyle on gut microbiota and human health, Nutrients, 7, 17, 10.3390/nu7010017

Dahan, 2017, Dietary factors in rheumatic autoimmune diseases: a recipe for therapy?, Nature Reviews Rheumatology, 13, 348, 10.1038/nrrheum.2017.42

Dao, 2016, Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology, Gut, 65, 426, 10.1136/gutjnl-2014-308778

De Vadder, 2014, Microbiota-generated metabolites promote metabolic benefits via gut-brain neural circuits, Cell, 156, 84, 10.1016/j.cell.2013.12.016

Derrien, 2008, The mucin degrader Akkermansia muciniphila is an abundant resident of the human intestinal tract, Applied Environmental Microbiology, 74, 1646, 10.1128/AEM.01226-07

Derrien, 2011, Modulation of mucosal immune response, tolerance and proliferation in mice colonized by the mucin-degrader Akkermansia muciniphila, Frontiers in Microbiology, 2, 166, 10.3389/fmicb.2011.00166

DeSantis, 2006, Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB, Applied Environmental Microbiology, 72, 5069, 10.1128/AEM.03006-05

De Vos, 2017, Microbe profile: Akkermansia muciniphila: a conserved intestinal symbiont that acts as the gatekeeper of our mucosa, Microbiology, 163, 646, 10.1099/mic.0.000444

Everard, 2013, Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity, Proceedings of the National Academy of Sciences of the United States of America, 110, 9066, 10.1073/pnas.1219451110

Everard, 2011, Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice, Diabetes, 60, 2775, 10.2337/db11-0227

Faria, 2014, Interplay between anthocyanins and gut microbiota, Journal of Agricultural and Food Chemistry, 62, 6898, 10.1021/jf501808a

Ganesh, 2013, Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella typhimurium-infected gnotobiotic mice, PLOS ONE, 8, e74963, 10.1371/journal.pone.0074963

Garcia-Mazcorro, 2016, Influence of whole-wheat consumption on fecal microbial ecology of obese diabetic mice, PeerJ, 4, e1702, 10.7717/peerj.1702

Garcia-Mazcorro, 2017, Effect of barley supplementation on the fecal microbiota, caecal biochemistry, and key biomarkers of obesity and inflammation in obese db/db mice, European Journal of Nutrition, 10.1007/s00394-017-1523-y

Garcia-Mazcorro, 2016, Molecular exploration of fecal microbiome in quinoa-supplemented obese mice, FEMS Microbiology Ecology, 92, fiw089, 10.1093/femsec/fiw089

Garcia-Mazcorro, 2012, Effect of the proton pump inhibitor omeprazole on the gastrointestinal bacterial microbiota of healthy dogs, FEMS Microbiology Ecology, 80, 624, 10.1111/j.1574-6941.2012.01331.x

Håkansson, 2015, Immunological alteration and changes of gut microbiota after dextran sulfate sodium (DSS) administration in mice, Clinical and Experimental Medicine, 15, 107, 10.1007/s10238-013-0270-5

Hammer, 2001, PAST: paleontological statistics software package for education and data analysis, Paleontologia Electronica, 4, 1

Hariri, 2010, High-fat diet-induced obesity in animal models, Nutrition Research Reviews, 23, 270, 10.1017/S0954422410000168

He, 2015, Stability of operational taxonomic units: an important but neglected property for analyzing microbial diversity, Microbiome, 3, 20, 10.1186/s40168-015-0081-x

Henning, 2017, Pomegranate ellagitannins stimulate the growth of Akkermansia muciniphila in vivo, Anaerobe, 43, 56, 10.1016/j.anaerobe.2016.12.003

Huang, 2017, Short-chain fatty acids inhibit oxidative stress and inflammation in mesangial cells induced by high glucose and lipopolysaccharide, Experimental and Clinical Endocrinology & Diabetes, 125, 98, 10.1055/s-0042-121493

Jeyakumar, 2006, Chronic dietary vitamin A supplementation regulates obesity in an obese mutant WNIN/Ob rat model, Obesity, 14, 52, 10.1038/oby.2006.7

Johansson, 2008, The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria, Proceedings of the National Academy of Sciences of the United States of America, 105, 15064, 10.1073/pnas.0803124105

Kang, 2013, Extracellular vesicles derived from gut microbiota, especially Akkermansia muciniphila, protect the progression of dextran sulfate sodium-induced colitis, PLOS ONE, 8, e76520, 10.1371/journal.pone.0076520

Karlsson, 2010, A closer look at Bacteroides: phylogenetic relationship and genomic implications of a life in the human gut, Microbiology Ecology, 61, 473, 10.1007/s00248-010-9796-1

Khan, 2016, Effect of methyl butyrate aroma on the survival and viability of human breast cancer cells in vitro, Journal of the Egyptian National Cancer Institute, 28, 81, 10.1016/j.jnci.2016.02.005

Klaassens, 2009, Mixed-species genomic microarray analysis of fecal samples reveals differential transcriptional responses of bifidobacteria in breast- and formula-fed infants, Applied Environmental Microbiology, 75, 2668, 10.1128/AEM.02492-08

Langille, 2013, Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences, Nature Biotechnology, 31, 814, 10.1038/nbt.2676

Liehr, 2017, Olive oil bioactives protect pigs against experimentally-induced chronic inflammation independently of alterations in gut microbiota, PLOS ONE, 12, e0174239, 10.1371/journal.pone.0174239

Lozupone, 2007, Quantitative and qualitative β diversity measures lead to different insights into factors that structure microbial communities, Applied Environmental Microbiology, 73, 1576, 10.1128/AEM.01996-06

Lozupone, 2005, UniFrac: a new phylogenetic method for comparing microbial communities, Applied Environmental Microbiology, 71, 8228, 10.1128/AEM.71.12.8228-8235.2005

Luo, 2016, Antioxidant, antibacterial, and antiproliferative activities of free and bound phenolics from peel and flesh of fuji apple, Journal of Food Science, 81, M1735, 10.1111/1750-3841.13353

Martini, 2017, Phenolic compounds profile and antioxidant properties of six sweet cherry (Prunus avium) cultivars, Food Research International, 97, 15, 10.1016/j.foodres.2017.03.030

McCune, 2011, Cherries and health: a review, Critical Reviews in Food Science and Nutrition, 51, 1, 10.1080/10408390903001719

Mikulic-Petkovsek, 2016, Wild prunus fruit species as a rich source of bioactive compounds, Journal of Food Science, 81, C1928, 10.1111/1750-3841.13398

Mithieux, 2004, Induction of control genes in intestinal gluconeogenesis is sequential during fasting and maximal in diabetes, American Journal of Physiology, Endocrinology and Metabolism, 286, E370, 10.1152/ajpendo.00299.2003

Modi, 2014, Antibiotics and the gut microbiota, The Journal of Clinical Investigation, 124, 4212, 10.1172/JCI72333

Negroni, 2014, Endoplasmic reticulum stress and unfolded protein response are involved in paediatric inflammatory bowel disease, Digestive Liver Disease, 46, 788, 10.1016/j.dld.2014.05.013

Noratto, 2016, Red raspberry decreases heart biomarkers of cardiac remodeling associated with oxidative and inflammatory stress in obese diabetic db/db mice, Food & Function, 7, 4944, 10.1039/c6fo01330a

Noratto, 2014, Carbohydrate-free peach (Prunus persica) and plum (Prunus salicina) juice affects fecal microbial ecology in an obese animal model, PLOS ONE, 9, e101723, 10.1371/journal.pone.0101723

Ormerod, 2016, Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals, Microbiome, 4, 36, 10.1186/s40168-016-0181-2

Ottman, 2017, Pili-like proteins of Akkermansia muciniphila modulate host immune responses and gut barrier function, PLOS ONE, 12, e0173004, 10.1371/journal.pone.0173004

Palmer, 2017, Dietary interventions for adults with chronic kidney disease, The Cochrane Database of Systematic Reviews, 4, CD011998, 10.1002/14651858.CD011998.pub2

Panche, 2016, Flavonoids: an overview, Journal of Nutritional Science, 5, e47, 10.1017/jns.2016.41

Parks, 2010, Identifying biologically relevant differences between metagenomic communities, Bioinformatics, 26, 715, 10.1093/bioinformatics/btq041

Pelaseyed, 2014, The mucus and mucins of the goblet cells and enterocytes provide the first defense line of the gastrointestinal tract and interact with the immune system, Immnological Reviews, 260, 8, 10.1111/imr.12182

Pérez-Jiménez, 2010, Identification of the 100 richest dietary sources of polyphenols: an application of the Phenol-Explorer database, European Journal of Clinical Nutrition, 64, S112, 10.1038/ejcn.2010.221

Png, 2010, Mucolytic bacteria with increased prevalence in IBD mucosa augment in vitro utilization of mucin by other bacteria, American Journal of Gastroenterology, 115, 2420, 10.1038/ajg.2010.281

Pryde, 2002, The microbiology of butyrate formation in the human colon, FEMS Microbiology Letters, 217, 133, 10.1111/j.1574-6968.2002.tb11467.x

Rahman, 2016, Loss of junctional adhesion molecule A promotes severe steatohepatitis in mice on a diet high in saturated fat, fructose, and cholesterol, Gastroenterology, 151, 733, 10.1053/j.gastro.2016.06.022

Ramos, 1997, Oral administration of short-chain fatty acids reduces the intestinal mucositis caused by treatment with Ara-C in mice fed commercial or elemental diets, Nutrition and Cancer, 28, 212, 10.1080/01635589709514577

Rao, 2013, Lipopolysaccharide preconditioning protects hepatocytes from ischemia/reperfusion injury (IRI) through inhibiting ATF4-CHOP pathway in mice, PLOS ONE, 8, e65568, 10.1371/journal.pone.0065568

Redondo, 2017, Thinned stone fruits are a source of polyphenols and antioxidant compounds, Journal of the Science of Food and Agriculture, 97, 902, 10.1002/jsfa.7813

Rideout, 2014, Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences, PeerJ, 2, e545, 10.7717/peerj.545

Rios-Covian, 2017, Shaping the metabolism of intestinal Bacteroides population through diet to improve human health, Frontiers in Microbiology, 8, 376, 10.3389/fmicb.2017.00376

Rowland, 2017, Gut microbiota functions: metabolism of nutrients and other food components, European Journal of Nutrition, 10.1007/s00394-017-1445-8

Schmittgen, 2008, Analyzing real-time PCR data by the comparative C(T) method, Nature Protocols, 3, 1101, 10.1038/nprot.2008.73

Sheflin, 2016, Linking dietary patterns with gut microbial composition and function, Gut Microbes, 8, 113, 10.1080/19490976.2016.1270809

Song, 2016, Dietary sweet cherry anthocyanins attenuates diet-induced hepatic steatosis by improving hepatic lipid metabolism in mice, Nutrition, 32, 827, 10.1016/j.nut.2016.01.007

Sonnenburg, 2005, Glycan foraging in vivo by an intestine-adapted bacterial symbiont, Science, 307, 1955, 10.1126/science.1109051

Stalmach, 2010, Absorption, metabolism, and excretion of green tea flavan-3-ols in humans with an ileostomy, Molecular Nutrition and Food Research, 54, 323, 10.1002/mnfr.200900194

Suzuki, 2008, Physiological concentrations of short-chain fatty acids immediately suppress colonic epithelial permeability, The British Journal of Nutrition, 100, 297, 10.1017/S0007114508888733

Swidsinski, 2011, Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum, Gut, 60, 34, 10.1136/gut.2009.191320

Swidsinski, 2008, Active Crohn’s disease and ulcerative colitis can be specifically diagnosed and monitored based on the biostructure of the fecal flora, Inflammatory Bowel Diseases, 14, 147, 10.1002/ibd.20330

Tan, 2014, The role of short-chain fatty acids in health and disease, Advances in Immunology, 121, 91, 10.1016/B978-0-12-800100-4.00003-9

Totsuka, 2014, Toll-like receptor 4 and MAIR-II/CLM-4/LMIR2 immunoreceptor regulate VLA-4-mediated inflammatory monocyte migration, Nature Communications, 5, 4710, 10.1038/ncomms5710

Van den Abbeele, 2011, Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats, Environmental Microbiology, 13, 2667, 10.1111/j.1462-2920.2011.02533.x

Van Passel, 2011, The genome of Akkermansia muciniphila, a dedicated intestinal mucin degrader, and its use in exploring intestinal metagenomes, PLOS ONE, 6, e16876, 10.1371/journal.pone.0016876

Velly, 2016, Mechanisms of cross-talk between the diet, the intestinal microbiome, and the undernourished host, Gut Microbes, 8, 98, 10.1080/19490976.2016.1267888

Via, 2016, Nutrition in type 2 diabetes and the metabolic syndrome, The Medical Clinics of North America, 100, 1285, 10.1016/j.mcna.2016.06.009

Vitali, 2012, An in vitro evaluation of the effect of probiotics and prebiotics on the metabolic profile of human microbiota, Anaerobe, 18, 386, 10.1016/j.anaerobe.2012.04.014

Wang, 2017, Characterization of phenolic compounds from early and late ripening sweet cherries and their antioxidant and antifungal activities, Journal of Agricultural and Food Chemistry, 65, 5413, 10.1021/acs.jafc.7b01409

Wu, 2011, Linking long-term dietary patterns with gut microbial enterotypes, Science, 334, 105, 10.1126/science.1208344

Wu, 2014, Inhibitory effects of sweet cherry anthocyanins on the obesity development in C57BL/6 mice, International Journal of Food Sciences and Nutrition, 65, 351, 10.3109/09637486.2013.854749

Wu, 2016, Mulberry and cherry anthocyanin consumption prevents oxidative stress and inflammation in diet-induced obese mice, Molecular Nutrition & Food Research, 60, 687, 10.1002/mnfr.201500734

Yamada, 2015, Terpene synthases are widely distributed in bacteria, Proceedings of the National Academy of Sciences of the United States of America, 112, 857, 10.1073/pnas.1422108112

Yang, 2015, Use of 16S rRNA gene-targeted group-specific primers for real-time PCR analysis of predominant bacteria in mouse feces, Applied Environmental Microbiology, 81, 6749, 10.1128/AEM.70.12.7220-7228.2004

Zhang, 2009, Current progress on butyric acid production by fermentation, Current Microbiology, 59, 656, 10.1007/s00284-009-9491-y

Thông tin
Thông tin xuất bản

PeerJ

Tập 6

e4195

Thông tin tác giả