The DOI matches its Crossref record; 60 of the 60 references it cites were found in a registry or an index.
The Effect of Diet and Exercise on Intestinal Integrity and Microbial Diversity in Mice
Open accessAbstract
BACKGROUND: The gut microbiota is now known to play an important role contributing to inflammatory-based chronic diseases. This study examined intestinal integrity/inflammation and the gut microbial communities in sedentary and exercising mice presented with a normal or high-fat diet. METHODS: Thirty-six, 6-week old C57BL/6NTac male mice were fed a normal or high-fat diet for 12-weeks and randomly assigned to exercise or sedentary groups. After 12 weeks animals were sacrificed and duodenum/ileum tissues were fixed for immunohistochemistry for occludin, E-cadherin, and cyclooxygenase-2 (COX-2). The bacterial communities were assayed in fecal samples using terminal restriction fragment length polymorphism (TRFLP) analysis and pyrosequencing of 16S rRNA gene amplicons. RESULTS: Lean sedentary (LS) mice presented normal histologic villi while obese sedentary (OS) mice had similar villi height with more than twice the width of the LS animals. Both lean (LX) and obese exercise (OX) mice duodenum and ileum were histologically normal. COX-2 expression was the greatest in the OS group, followed by LS, LX and OX. The TRFLP and pyrosequencing indicated that members of the Clostridiales order were predominant in all diet groups. Specific phylotypes were observed with exercise, including Faecalibacterium prausnitzi, Clostridium spp., and Allobaculum spp. CONCLUSION: These data suggest that exercise has a strong influence on gut integrity and host microbiome which points to the necessity for more mechanistic studies of the interactions between specific bacteria in the gut and its host.
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“In accordance, animal studies by us and others have reported that high-intensity endurance training modified the gut microbiota (Campbell et al., 2016; Denou et al., 2016)”
From Six-Week Endurance Exercise Alters Gut Metagenome That Is not Reflected in Systemic Metabolism in Over-weight Women (2018) · cites this paper as Campbell et al., 2016
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“Campbell et al. [88] asserted that exercised mice have bacteria related to Faecalibacterium prausnitzii which may protect the digestive tract by producing butyrate and lowering the oxygen tension in the lumen by a flavin/thiol electron shuttle.”
From The athletic gut microbiota (2020) · cites this paper as [88]
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An obesity-associated gut microbiome with increased capacity for energy harvest
Turnbaugh, P. J., Ley, R. E., Mahowald, M. A., Magrini, V., Mardis, E. R., & Gordon, J. I. (2006) · Nature · doi:10.1038/nature05414 · Cited by 12,444
Human gut microbes associated with obesity
Ley, R. E., Turnbaugh, P. J., Klein, S., & Gordon, J. I. (2006) · Nature · doi:10.1038/4441022a · Cited by 8,785
Obesity alters gut microbial ecology
Ley, R. E., Bäckhed, F., Turnbaugh, P., Lozupone, C. A., Knight, R. D., & Gordon, J. I. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504978102 · Cited by 6,176
Cani, P. D., Bibiloni, R., Knauf, C., Waget, A., Neyrinck, A. M., Delzenne, N. M., & Burcelin, R. (2008) · Diabetes · doi:10.2337/db07-1403 · Cited by 4,819
Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity
Everard, A., Belzer, C., Geurts, L., Ouwerkerk, J. P., Druart, C., Bindels, L. B., Guiot, Y., Derrien, M., Muccioli, G. G., Delzenne, N. M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219451110 · Cited by 4,511
Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermúdez-Humarán, L. G., Gratadoux, J.-J., Blugeon, S., Bridonneau, C., Furet, J.-P., Corthier, G., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804812105 · Cited by 4,413
Inflammatory Mechanisms in Obesity
Gregor, M. F., & Hotamisligil, G. S. (2011) · Annual Review of Immunology · doi:10.1146/annurev-immunol-031210-101322 · Cited by 3,754
Mechanisms underlying the resistance to diet-induced obesity in germ-free mice
Bäckhed, F., Manchester, J. K., Semenkovich, C. F., & Gordon, J. I. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605374104 · Cited by 2,615
The gut microbiota and host health: a new clinical frontier
Marchesi, J. R., Adams, D. H., Fava, F., Hermes, G. D. A., Hirschfield, G. M., Hold, G., Quraishi, M. N., Kinross, J., Smidt, H., Tuohy, K. M., et al. (2016) · Gut · doi:10.1136/gutjnl-2015-309990 · Cited by 2,302 · cited 1×
“Microbiome dysbiosis has proven to be a major contributor to chronic gut inflammatory diseases, like Irritable Bowel Syndrome (IBS) and ulcerative colitis [1].”
BackgroundMetabolic Syndrome and Altered Gut Microbiota in Mice Lacking Toll-Like Receptor 5
Vijay-Kumar, M., Aitken, J. D., Carvalho, F. A., Cullender, T. C., Mwangi, S., Srinivasan, S., Sitaraman, S. V., Knight, R., Ley, R. E., & Gewirtz, A. T. (2010) · Science · doi:10.1126/science.1179721 · Cited by 2,068
Exercise and associated dietary extremes impact on gut microbial diversity
Clarke, S. F., Murphy, E. F., O'Sullivan, O., Lucey, A. J., Humphreys, M., Hogan, A., Hayes, P., O'Reilly, M., Jeffery, I. B., Wood-Martin, R., et al. (2014) · Gut · doi:10.1136/gutjnl-2013-306541 · Cited by 1,439
A taxonomic distinctness index and its statistical properties
Clarke, K. R., & Warwick, R. M. (1998) · Journal of Applied Ecology · doi:10.1046/j.1365-2664.1998.3540523.x · Cited by 1,141
Dowd, S. E., Callaway, T. R., Wolcott, R. D., Sun, Y., McKeehan, T., Hagevoort, R. G., & Edrington, T. S. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-125 · Cited by 1,121 · cited 1×
“Operational taxonomic units (OTUs) were clustered using a sequence similarity threshold of 97% and taxonomically classified by BLASTN against a curated GreenGenes database as described previously [45,46].”
Methodde La Serre, C. B., Ellis, C. L., Lee, J., Hartman, A. L., Rutledge, J. C., & Raybould, H. E. (2010) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00098.2010 · Cited by 949
Dowd, S. E., Sun, Y., Secor, P. R., Rhoads, D. D., Wolcott, B. M., James, G. A., & Wolcott, R. D. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-43 · Cited by 783
An opportunistic pathogen isolated from the gut of an obese human causes obesity in germfree mice
Fei, N., & Zhao, L. (2012) · The ISME Journal · doi:10.1038/ismej.2012.153 · Cited by 775
Aging and vascular endothelial function in humans
Seals, D. R., Jablonski, K. L., & Donato, A. J. (2011) · Clinical Science · doi:10.1042/cs20100476 · Cited by 725
Meehan, C. J., & Beiko, R. G. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu050 · Cited by 724
Ding, S., Chi, M. M., Scull, B. P., Rigby, R., Schwerbrock, N. M. J., Magness, S., Jobin, C., & Lund, P. K. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012191 · Cited by 713
Bastard, J., Maachi, M., Nhieu, J. T. V., Jardel, C., Bruckert, É., Grimaldi, A., Robert, J., Capeau, J., & Hainque, B. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.5.8450 · Cited by 636
Lam, Y. Y., Ha, C. W. Y., Campbell, C. R., Mitchell, A. J., Dinudom, A., Oscarsson, J., Cook, D. I., Hunt, N. H., Caterson, I. D., Holmes, A. J., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0034233 · Cited by 604
Evans, C. C., LePard, K. J., Kwak, J. W., Stancukas, M. C., Laskowski, S., Dougherty, J., Moulton, L., Glawe, A., Wang, Y., Leone, V., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092193 · Cited by 587
Muscle triglyceride utilization during exercise: effect of training
Hurley, B. F., Nemeth, P. M., Martin, W. H., Hagberg, J. M., Dalsky, G. P., & Holloszy, J. O. (1986) · Journal of Applied Physiology · doi:10.1152/jappl.1986.60.2.562 · Cited by 522
Itallie, C. M. V., Fanning, A. S., Bridges, A. S., & Anderson, J. M. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e09-04-0320 · Cited by 479
Versatile functions for IL-6 in metabolism and cancer
Mauer, J., Denson, J. L., & Brüning, J. C. (2015) · Trends in Immunology · doi:10.1016/j.it.2014.12.008 · Cited by 415
Itallie, C. M. V., Holmes, J. C., Bridges, A. S., Gookin, J. L., Coccaro, M. R., Proctor, W. R., Colegio, O. R., & Anderson, J. M. (2008) · Journal of Cell Science · doi:10.1242/jcs.021485 · Cited by 410
Effects of exercise on gut peptides, energy intake and appetite
Martins, C., Morgan, L., Bloom, S. R., & Robertson, M. D. (2007) · Journal of Endocrinology · doi:10.1677/joe-06-0030 · Cited by 356
MATSUMOTO, M., INOUE, R., TSUKAHARA, T., USHIDA, K., CHIJI, H., MATSUBARA, N., & HARA, H. (2008) · Bioscience, Biotechnology, and Biochemistry · doi:10.1271/bbb.70474 · Cited by 352
Hamilton, M. K., Boudry, G., Lemay, D. G., & Raybould, H. E. (2015) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00029.2015 · Cited by 339
Gut microflora as a target for energy and metabolic homeostasis
Cani, P. D., & Delzenne, N. M. (2007) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/mco.0b013e3282efdebb · Cited by 332
Broom, D. R., Batterham, R. L., King, J. A., & Stensel, D. J. (2008) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90706.2008 · Cited by 325
Vicente, J. J., Galardi‐Castilla, M., Escalante, R., & Sastre, L. (2008) · BMC Microbiology · doi:10.1186/1471-2180-8-1 · Cited by 321
Exercise-induced suppression of acylated ghrelin in humans
Broom, D. R., Stensel, D. J., Bishop, N. C., Burns, S. F., & Miyashita, M. (2007) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00759.2006 · Cited by 294
Effect of endurance training on plasma free fatty acid turnover and oxidation during exercise
Martin, W. H., Dalsky, G. P., Hurley, B. F., Matthews, D. E., Bier, D. M., Hagberg, J. M., Rogers, M. A., King, D. S., & Holloszy, J. O. (1993) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.1993.265.5.e708 · Cited by 236
Pond, C. M. (1998) · Cambridge University Press eBooks · doi:10.1017/cbo9780511584633 · Cited by 236
The impact of physical exercise on the gastrointestinal tract
de Oliveira, E. P., & Burini, R. C. (2009) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32832e6776 · Cited by 225
Pedersen, B. K., Steensberg, A., & Schjerling, P. (2001) · Current Opinion in Hematology · doi:10.1097/00062752-200105000-00002 · Cited by 223
Molecular characterization of the ligand-receptor interaction of the neuropeptide Y family
Cabrele, C., & Beck‐Sickinger, A. G. (2000) · Journal of Peptide Science · doi:10.1002/(sici)1099-1387(200003)6:3 · Cited by 200
A molecular technique for identification of bacteria using small subunit ribosomal RNA sequences.
Avaniss-Aghajani, E., Jones, K. C., Chapman, D. J., & Brunk, C. F. (1994) · PubMed · Cited by 199
Klare, P., Nigg, J., Nold, J., Haller, B., Krug, A., Mair, S., Thoeringer, C. K., Christle, J. W., Schmid, R. M., Halle, M., et al. (2015) · Digestion · doi:10.1159/000371795 · Cited by 199
Ueda, S.-Y., Yoshikawa, T., Katsura, Y., Usui, T., Nakao, H., & Fujimoto, S. (2009) · Journal of Endocrinology · doi:10.1677/joe-08-0500 · Cited by 192
Ueda, S.-Y., Yoshikawa, T., Katsura, Y., Usui, T., & Fujimoto, S. (2009) · Journal of Endocrinology · doi:10.1677/joe-09-0190 · Cited by 178
Exercise, Appetite and Appetite-Regulating Hormones: Implications for Food Intake and Weight Control
Stensel, D. (2010) · Annals of Nutrition and Metabolism · doi:10.1159/000322702 · Cited by 171
Exercise regulation of intestinal tight junction proteins
Zuhl, M., Schneider, S., Lanphere, K., Conn, C., Dokladny, K., & Moseley, P. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2012-091585 · Cited by 167
Pond, C. M. (1998) · Cited by 166
Intestinal Permeability Is Associated With Visceral Adiposity in Healthy Women
Gummesson, A., Carlsson, L. M. S., Storlien, L. H., Bäckhed, F., Lundin, P., Löfgren, L., Stenlöf, K., Lam, Y. Y., Fagerberg, B., & Carlsson, B. (2011) · Obesity · doi:10.1038/oby.2011.251 · Cited by 165
Gill, J. M. R., & Hardman, A. E. (2003) · The Journal of Nutritional Biochemistry · doi:10.1016/s0955-2863(02)00275-9 · Cited by 159
Naylor, L. H., Carter, H. H., Fitzsimons, M., Cable, N. T., Thijssen, D. H. J., & GREEN, D. J. (2010) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00985.2010 · Cited by 130
Guo, Y., Ma, L., Enriori, P. J., Koška, J., Franks, P. W., Brookshire, T., Cowley, M. A., Salbe, A. D., DelParigi, A., & Tataranni, P. A. (2006) · Obesity · doi:10.1038/oby.2006.180 · Cited by 116
Molecular aspects of tight junction barrier function
Liang, G. H., & Weber, C. R. (2014) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2014.07.017 · Cited by 111
HUDLICKÁ, O., Brown, M. D., MAY, S., Zakrzewicz, A., & Pries, A. R. (2006) · Microcirculation · doi:10.1080/10739680600556951 · Cited by 69
The relationship between body weight and inflammation: Lesson from anti-TNF-α antibody therapy
Peluso, I., & Palmery, M. (2015) · Human Immunology · doi:10.1016/j.humimm.2015.10.008 · Cited by 67
Hoffman‐Goetz, L., Pervaiz, N., & Guan, J. (2009) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2009.01.015 · Cited by 66
How Can Faecalibacterium prausnitzii Employ Riboflavin for Extracellular Electron Transfer?
Khan, M. T., Browne, W. R., van Dijl, J. M., & Harmsen, H. J. M. (2012) · Antioxidants & Redox Signaling · doi:10.1089/ars.2012.4701 · Cited by 65
Exercise Training Reduces Inflammatory Mediators in the Intestinal Tract of Healthy Older Adult Mice
Packer, N., & Hoffman‐Goetz, L. (2012) · Canadian Journal on Aging / La Revue canadienne du vieillissement · doi:10.1017/s0714980812000104 · Cited by 60
McGuinness, L. M., Salganik, M., Vega, L. M., Pickering, K. D., & Kerkhof, L. J. (2005) · Environmental Science & Technology · doi:10.1021/es050900l · Cited by 58
Self-citationHood, L. (2012) · Science · doi:10.1126/science.1225475 · Cited by 50
Douglass, J. D., Malik, N., Chon, S., Wells, K., Zhou, Y. X., Choi, A. S., Joseph, L. B., & Storch, J. (2012) · Frontiers in Physiology · doi:10.3389/fphys.2012.00025 · Cited by 47
Self-citationExercise in Individuals With Inflammatory Bowel Disease
Nathan, I., Norton, C. S., Czuber‐Dochan, W., & Forbes, A. (2013) · Gastroenterology Nursing · doi:10.1097/sga.0000000000000005 · Cited by 41
Exercise and Dietary-Mediated Reductions in Postprandial Lipemia
Plaisance, E. P., & Fisher, G. (2014) · Journal of Nutrition and Metabolism · doi:10.1155/2014/902065 · Cited by 34
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Metadata
- Authors
- Campbell, S. C., Wisniewski, P. J., Noji, M., McGuinness, L. R., Häggblom, M. M., Lightfoot, S. A., Joseph, L. B., & Kerkhof, L. J.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Corresponding author
- Campbell, Sara C.
- Venue
- PLOS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2016-03-08
- Volume
- 11
- Issue
- 3
- Pages
- e0150502
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC4783017
- OpenAlex
- W2295140408
- Cited by
- 268
- References
- 60
- Citations by year
- 2026: 18 · 2025: 18 · 2024: 33 · 2023: 24 · 2022: 33 · 2021: 34 · 2020: 33 · 2019: 25 · 2018: 16 · 2017: 26 · 2016: 8
- FWCI
- 12.99
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Rutgers University Community Repository (Rutgers University) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Funders
- National Institutes of Health
- National Institute of Arthritis and Musculoskeletal and Skin Diseases (U54AR055073)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Agricultural and Biological Sciences › Food Science › Probiotics and Fermented Foods
- Keywords
- gut microbiota, high-fat diet, physical activity, intestinal integrity, intestinal inflammation, cyclooxygenase-2, occludin, E-cadherin, villus morphology, Clostridiales, Faecalibacterium prausnitzii, Clostridium, Allobaculum, obesity, sedentary behavior, host-microbe interactions
- MeSH terms
- Animals, Animal Feed, Bacteria, Body Weight, Feces, Intestines, Male, Phylogeny, Physical Conditioning, Animal, RNA, Ribosomal, 16S, Biomarkers, Cadherins, Biodiversity, Mice, Metagenome, Occludin, Microbiota
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