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PLOS ONE  2014 

Exercise Prevents Weight Gain and Alters the Gut Microbiota in a Mouse Model of High Fat Diet-Induced Obesity

DOI: 10.1371/journal.pone.0092193

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Abstract:

Background Diet-induced obesity (DIO) is a significant health concern which has been linked to structural and functional changes in the gut microbiota. Exercise (Ex) is effective in preventing obesity, but whether Ex alters the gut microbiota during development with high fat (HF) feeding is unknown. Objective Determine the effects of voluntary Ex on the gastrointestinal microbiota in LF-fed mice and in HF-DIO. Methods Male C57BL/6 littermates (5 weeks) were distributed equally into 4 groups: low fat (LF) sedentary (Sed) LF/Sed, LF/Ex, HF/Sed and HF/Ex. Mice were individually housed and LF/Ex and HF/Ex cages were equipped with a wheel and odometer to record Ex. Fecal samples were collected at baseline, 6 weeks and 12 weeks and used for bacterial DNA isolation. DNA was subjected both to quantitative PCR using primers specific to the 16S rRNA encoding genes for Bacteroidetes and Firmicutes and to sequencing for lower taxonomic identification using the Illumina MiSeq platform. Data were analyzed using a one or two-way ANOVA or Pearson correlation. Results HF diet resulted in significantly greater body weight and adiposity as well as decreased glucose tolerance that were prevented by voluntary Ex (p<0.05). Visualization of Unifrac distance data with principal coordinates analysis indicated clustering by both diet and Ex at week 12. Sequencing demonstrated Ex-induced changes in the percentage of major bacterial phyla at 12 weeks. A correlation between total Ex distance and the ΔCt Bacteroidetes: ΔCt Firmicutes ratio from qPCR demonstrated a significant inverse correlation (r2 = 0.35, p = 0.043). Conclusion Ex induces a unique shift in the gut microbiota that is different from dietary effects. Microbiota changes may play a role in Ex prevention of HF-DIO.

References

[1]  Flegal KM, Carroll MD, Kit BK, Ogden CL (2012) Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA 307: 491–497. doi: 10.1001/jama.2012.39
[2]  Ogden CL, Carroll MD, Kit BK, Flegal KM (2012) Prevalence of obesity and trends in body mass index among US children and adolescents, 1999–2010. JAMA 307: 483–490. doi: 10.1001/jama.2012.40
[3]  Eeg-Olofsson K, Cederholm J, Nilsson P, Zethelius B, Nunez L, et al. (2009) Risk of cardiovascular disease and mortality in overweight and obese patients with type 2 diabetes: an observational study in 13,087 patients. Diabetologia 52: 65–73. doi: 10.1007/s00125-008-1190-x
[4]  Finkelstein EA, Trogdon JG, Cohen JW, Dietz W (2009) Annual medical spending attributable to obesity: payer-and service-specific estimates. Health Aff (Milwood) 28: w822–w831. doi: 10.1377/hlthaff.28.5.w822
[5]  Wright JD, Borrud LG, McDowell MA, Wang C-Y, Radimer K, et al. (2007) Nutrition assessment in the national health and nutrition examination survey 1999–2002. J Am Diet Assoc 107: 822–829. doi: 10.1016/j.jada.2007.02.017
[6]  Lichtenstein AH, Appel LJ, Brands M, Carnethon M, Daniels S, et al. (2006) Diet and lifestyle recommendations revision 2006 A scientific statement from the American Heart Association Nutrition Committee. Circulation 114: 82–96. doi: 10.1161/circulationaha.106.176158
[7]  Matsuzawa-Nagata N, Takamura T, Ando H, Nakamura S, Kurita S, et al. (2008) Increased oxidative stress precedes the onset of high-fat diet–induced insulin resistance and obesity. Metabolism 57: 1071–1077. doi: 10.1016/j.metabol.2008.03.010
[8]  Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Microbial ecology - Human gut microbes associated with obesity. Nature 444: 1022–1023. doi: 10.1038/4441022a
[9]  Tehrani AB, Nezami BG, Gewirtz A, Srinivasan S (2012) Obesity and its associated disease: a role for microbiota? Neurogastroenterol Motil 24: 305–311. doi: 10.1111/j.1365-2982.2012.01895.x
[10]  Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, et al. (2006) An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 444: 1027–1031. doi: 10.1038/nature05414
[11]  Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, et al. (2005) Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 102: 11070–11075. doi: 10.1073/pnas.0504978102
[12]  Turnbaugh PJ, Backhed F, Fulton L, Gordon JI (2008) Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host & Microbe 3: 213–223. doi: 10.1016/j.chom.2008.02.015
[13]  Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, et al. (2009) The effect of diet on the human gut microbiome: A metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med. 1: 6ra14. doi: 10.1126/scitranslmed.3000322
[14]  Hildebrandt MA, Hoffmann C, Sherrill–Mix SA, Keilbaugh SA, Hamady M, et al. (2009) High-fat diet determines the composition of the murine gut microbiome independently of obesity. Gastroenterology 137: 1716–1724. doi: 10.1053/j.gastro.2009.08.042
[15]  Bradley RL, Jeon JY, Liu F-F, Maratos-Flier E (2008) Voluntary exercise improves insulin sensitivity and adipose tissue inflammation in diet-induced obese mice. Am J Physiol Endocrinol Metab 295: E586–E594. doi: 10.1152/ajpendo.00309.2007
[16]  Huang P, Li S, Shao M, Qi Q, Zhao F, et al. (2010) Calorie restriction and endurance exercise share potent anti-inflammatory function in adipose tissues in ameliorating diet-induced obesity and insulin resistance in mice. Nutr Metab 7: 59. doi: 10.1186/1743-7075-7-59
[17]  Colditz GA, Cannuscio CC, Frazier AL (1997) Physical activity and reduced risk of colon cancer: implications for prevention. Cancer Causes Control 8: 649–667. doi: 10.1023/a:1018458700185
[18]  de Oliveira EP, Burini RC (2009) The impact of physical exercise on the gastrointestinal tract. Curr Opin Clin Nutr Metab Care 12: 533–538. doi: 10.1097/mco.0b013e32832e6776
[19]  Peters H, De Vries W, Vanberge-Henegouwen G, Akkermans L (2001) Potential benefits and hazards of physical activity and exercise on the gastrointestinal tract. Gut 48: 435–439. doi: 10.1136/gut.48.3.435
[20]  Oliveira AG, Carvalho BM, Tobar N, Ropelle ER, Pauli JR, et al. (2011) Physical exercise reduces circulating lipopolysaccharide and TLR4 activation and improves insulin signaling in tissues of DIO rats. Diabetes 60: 784–796. doi: 10.2337/db09-1907
[21]  Matsumoto M, Inoue R, Tsukahara T, Ushida K, Chiji H, et al. (2008) Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem 72: 572–576. doi: 10.1271/bbb.70474
[22]  Choi JJ, Eum SY, Rampersaud E, Daunert S, Abreu MT, et al. (2013) Exercise attenuates PCB-induced changes in the mouse gut microbiome. Environ Health Perspect 121: 725–730. doi: 10.1289/ehp.1306534
[23]  Konhilas JP, Widegren U, Allen DL, Paul AC, Cleary A, et al. (2005) Loaded wheel running and muscle adaptation in the mouse. Am J Physiol Heart Circ Physiol 289: H455–H465. doi: 10.1152/ajpheart.00085.2005
[24]  Fraulob JC, Ogg-Diamantino R, Fernandes-Santos C, Aguila MB, Mandarim-de-Lacerda CA (2010) A mouse model of metabolic syndrome: insulin resistance, fatty liver and non-alcoholic fatty pancreas disease (NAFPD) in C57BL/6 mice fed a high fat diet. J Clin Biochem Nutr 46: 212–223. doi: 10.3164/jcbn.09-83
[25]  Golde WT, Gollobin P, Rodriguez LL (2005) A rapid, simple, and humane method for submandibular bleeding of mice using a lancet. Lab Animal 34: 39–43. doi: 10.1038/laban1005-39
[26]  Miller MS, Galligan JJ, Burks TF (1981) Accurate measurement of intestinal transit in the rat. J Pharmacol Methods 6: 211–217. doi: 10.1016/0160-5402(81)90110-8
[27]  Aube AC, Cabarrocas J, Bauer J, Philippe D, Aubert P, et al. (2006) Changes in enteric neurone phenotype and intestinal functions in a transgenic mouse model of enteric glia disruption. Gut 55: 630–637. doi: 10.1136/gut.2005.067595
[28]  Wang YW, Hoenig JD, Malin KJ, Qamar S, Petrof EO, et al. (2009) 16S rRNA genebased analysis of fecal microbiota from preterm infants with and without necrotizing enterocolitis. ISME J 3: 944–954. doi: 10.1038/ismej.2009.37
[29]  Culman SW, Bukowski R, Gauch HG, Cadillo-Quiroz H, Buckley DH (2009) T-REX: software for the processing and analysis of T-RFLP data. BMC Bioinformatics 10: 171. doi: 10.1186/1471-2105-10-171
[30]  Armougom F, Henry M, Vialettes B, Raccah D, Raoult D (2009) Monitoring bacterial community of human gut microbiota reveals an increase in Lactobacillus in obese patients and Methanogens in anorexic patients. PLoS One 4: e7125. doi: 10.1371/journal.pone.0007125
[31]  Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148: 257–266.
[32]  Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, et al. (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26: 266–267. doi: 10.1093/bioinformatics/btp636
[33]  Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, et al. (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7: 335–336. doi: 10.1038/nmeth.f.303
[34]  DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72: 5069–5072. doi: 10.1128/aem.03006-05
[35]  Han M, Zmasek C (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10: 356. doi: 10.1186/1471-2105-10-356
[36]  Ley RE (2010) Obesity and the human microbiome. Curr Opin Gastroenterol 26: 5–11. doi: 10.1097/mog.0b013e328333d751
[37]  Angelakis E, Armougom F, Million M, Raoult D (2012) The relationship between gut microbiota and weight gain in humans. Future Microbiol 7: 91–109. doi: 10.2217/fmb.11.142
[38]  Simoes CD, Maukonen J, Kaprio J, Rissanen A, Pietilainen KH, et al. (2013) Habitual dietary intake is associated with stool microbiota composition in monozygotic twins. J Nutr 143: 417–423. doi: 10.3945/jn.112.166322
[39]  Mujico JR, Baccan GC, Gheorghe A, Diaz LE, Marcos A (2013) Changes in gut microbiota due to supplemented fatty acids in diet-induced obese mice. Br J Nutr 110: 711–720. doi: 10.1017/s0007114512005612
[40]  Rastmanesh R (2011) High polyphenol, low probiotic diet for weight loss because of intestinal microbiota interaction. Chem Biol Interact 189: 1–8. doi: 10.1016/j.cbi.2010.10.002
[41]  Le Chatelier E, Nielsen T, Qin J, Prifti E, Hildebrand F, et al. (2013) Richness of human gut microbiome correlates with metabolic markers. Nature 500: 541–546. doi: 10.1038/nature12506
[42]  Cotillard A, Kennedy SP, Kong LC, Prifti E, Pons N, et al. (2013) Dietary intervention impact on gut microbial gene richness. Nature 500: 585–588. doi: 10.1038/nature12738
[43]  Huang EY, Leone VA, Devkota S, Wang Y, Brady MJ, et al. (2013) Composition of dietary fat source shapes gut microbiota architecture and alters host inflammatory mediators in mouse adipose tissue. J Parenter Enteral Nutr 37: 746–754. doi: 10.1177/0148607113486931
[44]  Devkota S, Wang Y, Musch MW, Leone V, Fehlner-Peach H, et al. (2012) Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in IL10-/-mice. Nature 487: 104–108. doi: 10.1038/nature11225
[45]  Barcenilla A, Pryde SE, Martin JC, Duncan SH, Stewart CS, et al. (2000) Phylogenetic relationships of butyrate-producing bacteria from the human gut. Appl Environ Microbiol 66: 1654–1661. doi: 10.1128/aem.66.4.1654-1661.2000
[46]  Malago JJ, Koninkx JF, van Dijk JE (2002) The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress Chaperones 7: 191–199. doi: 10.1379/1466-1268(2002)007<0191:thsrac>2.0.co;2
[47]  Musch MW, Ciancio M, Sarge K, Chang EB (1996) Induction of heat shock protein 70 protects intestinal epithelial IEC-18 cells from oxidant and thermal injury. Am J Physiol Cell Physiol 270: C429–C436.
[48]  Atalay M, Oksala NK, Laaksonen DE, Khanna S, Nakao C, et al. (2004) Exercise training modulates heat shock protein response in diabetic rats. J Appl Physiol 97: 605–611. doi: 10.1152/japplphysiol.01183.2003
[49]  Musch MW, Sugi K, Straus D, Chang EB (1999) Heat-shock protein 72 protects against oxidant-induced injury of barrier function of human colonic epithelial Caco2/bbe cells. Gastroenterology 117: 115–122. doi: 10.1016/s0016-5085(99)70557-3
[50]  Noble E, Ho R, Dzialoszynski T (2006) Exercise is the primary factor associated with Hsp70 induction in muscle of treadmill running rats. Acta Physiol 187: 495–501. doi: 10.1111/j.1748-1716.2006.01591.x
[51]  Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, et al. (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet–induced obesity and diabetes in mice. Diabetes 57: 1470–1481. doi: 10.2337/db07-1403
[52]  Nathan C (2008) Epidemic inflammation: pondering obesity. Mol Med 14: 485–492.
[53]  Bervoets L, Van Hoorenbeeck K, Kortleven I, Van Noten C, Hens N, et al. (2013) Differences in gut microbiota composition between obese and lean children: a cross-sectional study. Gut Pathog 5: 10. doi: 10.1186/1757-4749-5-10
[54]  Million M, Angelakis E, Paul M, Armougom F, Leibovici L, et al. (2012) Comparative meta-analysis of the effect of Lactobacillus species on weight gain in humans and animals. Microb Pathog 53: 100–108. doi: 10.1016/j.micpath.2012.05.007
[55]  Bernardeau M, Vernoux JP, Gueguen M (2002) Safety and efficacy of probiotic lactobacilli in promoting growth in post-weaning Swiss mice. Int J Food Microbiol 77: 19–27. doi: 10.1016/s0168-1605(02)00059-4
[56]  Angelakis E, Bastelica D, Ben Amara A, El Filali A, Dutour A, et al. (2012) An evaluation of the effects of Lactobacillus ingluviei on body weight, the intestinal microbiome and metabolism in mice. Microb Pathog 52: 61–68. doi: 10.1016/j.micpath.2011.10.004
[57]  Andersson U, Br?nning C, Ahrné S, Molin G, Alenfall J, et al. (2010) Probiotics lower plasma glucose in the high-fat fed C57BL/6J mouse. Benef Microbes 1: 189–196. doi: 10.3920/bm2009.0036
[58]  Naito E, Yoshida Y, Makino K, Kounoshi Y, Kunihiro S, et al. (2011) Beneficial effect of oral administration of Lactobacillus casei strain Shirota on insulin resistance in diet-induced obesity mice. J Appl Microbiol 110: 650–657. doi: 10.1111/j.1365-2672.2010.04922.x
[59]  Cani PD (2013) Gut microbiota and obesity: lessons from the microbiome. Brief Funct Genomics 12: 381–387. doi: 10.1093/bfgp/elt014
[60]  Macfarlane S, Macfarlane GT (2003) Regulation of short-chain fatty acid production. In: Proceeding-Nutrition Society of London 62: 67–72. doi: 10.1079/pns2002207
[61]  B?ckhed F, Manchester JK, Semenkovich CF, Gordon JI (2007) Mechanisms underlying the resistance to diet-induced obesity in germ-free mice. Proc Natl Acad Sci USA 104: 979–984. doi: 10.1073/pnas.0605374104
[62]  Dapoigny M, Sarna SK (1991) Effects of physical exercise on colonic motor activity. American Journal of Physiology-Gastrointestinal and Liver Physiology 260: G646–G652.
[63]  Rao SS, Beaty J, Chamberlain M, Lambert PG, Gisolfi C (1999) Effects of acute graded exercise on human colonic motility. Am J Physiol Gastrointest Liver Physiol 276: G1221–G1226.
[64]  Martins C, Morgan LM, Bloom SR, Robertson MD (2007) Effects of exercise on gut peptides, energy intake and appetite. J Endocrinol 193: 251–258. doi: 10.1677/joe-06-0030
[65]  Konturek SJ, Tasler J, Obtulowicz W (1973) Effect of exercise on gastrointestinal secretions. J Appl Physiol 34: 324–328. doi: 10.1159/000197317
[66]  Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1: 15–25. doi: 10.1016/j.cmet.2004.12.003
[67]  Geurts L, Neyrinck AM, Delzenne NM, Knauf C, Cani PD (2013) Gut microbiota controls adipose tissue expansion, gut barrier and glucose metabolism: novel insights into molecular targets and interventions using prebiotics. Benef Microbes, 1–15.
[68]  Pedersen B, Steensberg A, Fischer C, Keller C, Keller P, et al. (2004) The metabolic role of IL-6 produced during exercise: is Il-6 an exercise factor? Proc Nutr Soc 63: 263–268. doi: 10.1079/pns2004338
[69]  Petersen A, Pedersen B (2006) The role of Il-6 in mediating the anti-inflammatory. J Physiol Pharmacol 57: 43–51.
[70]  Haange SB, Oberbach A, Schlichting N, Hugenholtz F, Smidt H, et al. (2012) Metaproteome analysis and molecular genetics of rat intestinal microbiota reveals section and localization resolved species distribution and enzymatic functionalities. J Proteome Res 11: 5406–5417. doi: 10.1021/pr3006364

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