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Increased Gut Permeability and Microbiota Change Associate with Mesenteric Fat Inflammation and Metabolic Dysfunction in Diet-Induced Obese Mice
Open accessAbstract
We investigated the relationship between gut health, visceral fat dysfunction and metabolic disorders in diet-induced obesity. C57BL/6J mice were fed control or high saturated fat diet (HFD). Circulating glucose, insulin and inflammatory markers were measured. Proximal colon barrier function was assessed by measuring transepithelial resistance and mRNA expression of tight-junction proteins. Gut microbiota profile was determined by 16S rDNA pyrosequencing. Tumor necrosis factor (TNF)-α and interleukin (IL)-6 mRNA levels were measured in proximal colon, adipose tissue and liver using RT-qPCR. Adipose macrophage infiltration (F4/80⁺) was assessed using immunohistochemical staining. HFD mice had a higher insulin/glucose ratio (P = 0.020) and serum levels of serum amyloid A3 (131%; P = 0.008) but reduced circulating adiponectin (64%; P = 0.011). In proximal colon of HFD mice compared to mice fed the control diet, transepithelial resistance and mRNA expression of zona occludens 1 were reduced by 38% (P<0.001) and 40% (P = 0.025) respectively and TNF-α mRNA level was 6.6-fold higher (P = 0.037). HFD reduced Lactobacillus (75%; P<0.001) but increased Oscillibacter (279%; P = 0.004) in fecal microbiota. Correlations were found between abundances of Lactobacillus (r = 0.52; P = 0.013) and Oscillibacter (r = -0.55; P = 0.007) with transepithelial resistance of the proximal colon. HFD increased macrophage infiltration (58%; P = 0.020), TNF-α (2.5-fold, P<0.001) and IL-6 mRNA levels (2.5-fold; P = 0.008) in mesenteric fat. Increased macrophage infiltration in epididymal fat was also observed with HFD feeding (71%; P = 0.006) but neither TNF-α nor IL-6 was altered. Perirenal and subcutaneous adipose tissue showed no signs of inflammation in HFD mice. The current results implicate gut dysfunction, and attendant inflammation of contiguous adipose, as salient features of the metabolic dysregulation of diet-induced obesity.
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“Increased intestinal barrier permeability is related to the metabolic dysfunction of visceral adipose tissue (Lam et al., 2012).”
From Akkermansia muciniphila alleviates high‐fat‐diet ‐related metabolic‐associated fatty liver disease by modulating gut microbiota and bile acids (2023) · cites this paper as Lam et al., 2012
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“Oscillibacter has been found to be associated with obesity (Xu et al., 2017), and its abundance is negatively correlated with intestinal barrier function (Lam et al., 2012).”
From Akkermansia muciniphila alleviates high‐fat‐diet ‐related metabolic‐associated fatty liver disease by modulating gut microbiota and bile acids (2023) · cites this paper as Lam et al., 2012
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“Bifidobacterium has been associated with reducing gut permeability (44) and Oscillospira is associated with increased gut permeability (45).”
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“Oscillibacter may directly regulate the components involved in the preservation of the intestinal barrier [33].”
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“They can also improve the intestinal barrier function and integrity [24] and influence gut microbiota composition in these metabolic pathologies [25–27].”
BackgroundWilson, S. M. G., Peach, J. T., Fausset, H., Miller, Z. J., Walk, S. T., Yeoman, C. J., Bothner, B. B., & Miles, M. P. (2023) · Frontiers in Nutrition · doi:10.3389/fnut.2023.1244692 · Cited by 16
Stability of human gut microbiome: Comparison of ecological modelling and observational approaches
Revel-Muroz, A., Akulinin, M., Shilova, P., Tyakht, A., & Klimenko, N. S. (2023) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2023.08.030 · Cited by 19
“Interestingly, Oscillibacter has also been associated with pro-inflammatory cytokines and intestinal permeability [95], as well as several disease states [81,96,97].”
BackgroundWiley, M., & DiPatrizio, N. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810549 · Cited by 15
“, IL-6, TNFα, and number of T-cells in the large intestine) [4,26].”
BackgroundResultThe effect of a hydrolyzed protein diet on the fecal microbiota in cats with chronic enteropathy
Kathrani, A., Yen, S., Swann, J. R., & Hall, E. J. (2022) · Scientific Reports · doi:10.1038/s41598-022-06576-y · Cited by 22
Insulin resistance corresponds with a progressive increase in NOD1 in high fat diet-fed mice
Sharma, A., Singh, S., Mishra, A., Rai, A., Ahmad, I., Ahmad, S., Gulzar, F., Schertzer, J., Shrivastava, A., & Tamrakar, A. (2022) · Endocrine · doi:10.1007/s12020-022-02995-z · Cited by 15
“dysfunction [7, 8] leading to metabolic endotoxemia [9–11],”
Zhu, W., Xu, Y., Liu, J., Chen, D., Zhang, H., Yang, Z., & Zhou, X. (2021) · Foods · doi:10.3390/foods10123030 · Cited by 15
“[57] studied a high-fat diet intervention in rats and found an increase in the abundance of Firmicutes and a decrease in the abundance of”
BackgroundMediators of Host–Microbe Circadian Rhythms in Immunity and Metabolism
Frazier, K., Frith, M., Harris, D., & Leone, V. (2020) · Biology · doi:10.3390/biology9120417 · Cited by 16
“HFD alters oscillation patterns of hepatic Bmal1 gene expression in both GF and SPF mice, reducing the abundance of oscillating bacterial taxa while increasing inflammation in mesenteric adipose tissue in the latter [38,44].”
BackgroundEffects of Undaria pinnatifida and Laminaria japonica on Rat’s Intestinal Microbiota and Metabolite
Kim, J. Y., & Yu, D. Y. (2016) · Journal of Nutrition & Food Sciences · doi:10.4172/2155-9600.1000502 · Cited by 14
“Inflammatory signaling affects metabolic signaling pathways, as indicated by the promotion of obesity by mild-grade inflammations [42,43].”
BackgroundOliveira, S. D. (2022) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.121.316236 · Cited by 20
Lingaiah, S., Arffman, R. K., Morin-Papunen, L. C., Tapanainen, J. S., & Piltonen, T. (2021) · BMJ Open · doi:10.1136/bmjopen-2020-045324 · Cited by 18
Gu, W., Yang, M., Bi, Q., Zeng, L., Wang, X., Dong, J.-C., Li, F.-J., Yang, X., Li, J., & Yu, J. (2020) · BMC Complementary Medicine and Therapies · doi:10.1186/s12906-020-02897-5 · Cited by 15
Chen, Y.-H., Wang, Y., Chiu, C.-C., Lee, Y.-P., Hung, S.-W., Huang, C., Chiu, C., Chen, T.-H., Huang, W.-C., & Chuang, H.-L. (2020) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2020.108362 · Cited by 15
Fatty Acids, Gut Microbiota, and the Genesis of Obesity
de Velasco, P. C., Ferreira, A. R. D. C., Crovesy, L., Marine, T., & do Carmo, M. D. G. T. (2018) · IntechOpen eBooks · doi:10.5772/intechopen.80664 · Cited by 14
Su, Y.-B., Li, T.-H., Huang, C.-C., Tsai, H.-C., Huang, S.-F., Hsieh, Y., Yang, Y.-Y., Huang, Y.-H., Hou, M.-C., & Lin, H.-C. (2018) · PLoS ONE · doi:10.1371/journal.pone.0194867 · Cited by 14
Sheldon, R. D., Kanosky, K. M., Wells, K., Miles, L., Perfield, J., Xanthakos, S., Inge, T. H., & Rector, R. (2016) · Physiological Genomics · doi:10.1152/physiolgenomics.00020.2016 · Cited by 14
Neural Mechanisms of Exercise: Effects on Gut Miccrobiota and Depression
Yuan, T., Rocha, N., Paes, F., Arias-Carrión, Ó., Machado, S. E. D. C., & Filho, A. S. S. (2015) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527315666151111124729 · Cited by 15
“Keywords: Depression, exercise, gut microbiota.”
Sharma, U., Sahu, A., Thakur, N., Choudhary, R. K., Shekhar, H., Haque, S., Tuli, H. S., Aubakirova, A. T., & Sharma, B. (2025) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-025-05409-6 · Cited by 14
Role of the Gut Microbiome in Metabolic Dysfunction-Associated Steatotic Liver Disease
Maher, S., Rajapakse, J., El-Omar, E. M., & Zekry, A. (2024) · Seminars in Liver Disease · doi:10.1055/a-2438-4383 · Cited by 14
“21,33 Furthermore, with the imbalance in microbial composition seen in gut dysbiosis, this disruption often leads to an over-growth of Gram-negative bacteria, which are rich in LPS on their outer membranes.”
Ponce‐España, E., Cruz‐Chamorro, I., Santos‐Sánchez, G., Álvarez‐López, A. I., Fernández-Santos, J. M., Pedroche, J., Millán-Linares, M. C., Bejarano, I., Lardone, P. J., & Carrillo‐Vico, A. (2024) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2024.117198 · Cited by 16
Hashemnia, S. M. R., Meshkani, R., Zamani‐Garmsiri, F., Shabani, M., Ebrahimi, M. T., Kashani, I. R., Siadat, S. D., Azadi, S. M., & Emamgholipour, S. (2022) · Life Sciences · doi:10.1016/j.lfs.2022.121286 · Cited by 13
Wu, Z.-H., Yang, J., Chen, L., Du, C., Zhang, Q., Zhao, S.-S., Wang, X., Yang, J., Liu, Y., Cai, D., et al. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.899829 · Cited by 14
“Several studies have shown that mice fed an HF diet showed increased levels of inflammatory cytokines (Tnf α and Il6) in the ileum, colon, and surrounding mesenteric fat, even before the development of obesity (28, 29).”
BackgroundInter-vendor variance of enteric eukaryotic DNA viruses in specific pathogen free C57BL/6N mice
Rasmussen, T. S., Jakobsen, R. R., Castro-Mejía, J. L., Kot, W., Thomsen, A. R., Vogensen, F. K., Nielsen, D. S., & Hansen, A. K. (2021) · Research in Veterinary Science · doi:10.1016/j.rvsc.2021.01.022 · Cited by 15
Using Autoencoders for Predicting Latent Microbiome Community Shifts Responding to Dietary Changes
Reiman, D., & Dai, Y. (2019) · IEEE International Conference on Bioinformatics and Biomedicine · doi:10.1109/bibm47256.2019.8983124 · Cited by 13
“Among the OTUs that were highly abundant, the model found that eating a HFHS diet led to an increase in Clostridium, Lactococcus, Eubacterium, and Ruminococcus and a decrease in Odoribacter, Porphyromonas, and Lactobacillus.”
ResultYin, X., Lee, B., Zaragoza, J., & Marco, M. L. (2017) · Scientific Reports · doi:10.1038/s41598-017-07428-w · Cited by 13
Jacouton, E., Mondot, S., Langella, P., & Bermúdez‐Humarán, L. G. (2023) · Bioengineering · doi:10.3390/bioengineering10101151 · Cited by 13
“In addition, obesity and metabolic syndrome are characterized by altered gut microbiota, inflammation, and barrier dysfunction [1–4].”
BackgroundWang, J., Dong, L., Hu, J., Wang, Y.-Y.-F., Li, A., Peng, B., Zhang, B., Liu, J., & Wang, S. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.992815 · Cited by 11
“Oscillibacter can decreased the levels of the proteins related to gut mucosal barrier, which are considered to have strongly associated with HFDinduced obesity (33).”
BackgroundWang, C., Yuan, Z.-X., Sun, Y.-X., Yao, X.-L., Li, R., & Li, S. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.782611 · Cited by 12
Li, J.-M., Wan, Y., Zheng, Z., Zhang, H.-Q., Li, Y., Guo, X.-F., Li, K.-L., & Li, D. (2021) · Food & Function · doi:10.1039/d1fo00906k · Cited by 12
Hu, Y.-H., Huang, X.-Y., Zong, X., Bi, Z., Cheng, Y.-Z., Xiao, X., Wang, F.-Q., Wang, Y.-Z., & Lu, Z.-Q. (2020) · Journal of Applied Microbiology · doi:10.1111/jam.14679 · Cited by 12
“Moreover, there was a lower relative abundance of Desulfovibrio, Oscillibacter, f__Erysipelotrichaceae_Unclassified and Sutterella in the SD rats consuming CF feed, which might result in gut inflammation (Chen et al. 2012; Lam et al. 2012; Hiippala et al. 2016).”
BackgroundZebrafish Axenic Larvae Colonization with Human Intestinal Microbiota
Arias-Jayo, N., Alonso-Sáez, L., Ramírez-García, A., & Pardo, M. (2017) · Zebrafish · doi:10.1089/zeb.2017.1460 · Cited by 12
“45,46 The second most abundant phylum in Human was Bac-teroidetes.”
TL1A regulates TCRγδ+ intraepithelial lymphocytes and gut microbial composition
Tougaard, P., Skov, S., Pedersen, A. E., Krych, Ł., Nielsen, D. S., Bahl, M. I., Christensen, E. G., Licht, T. R., Poulsen, S. S., Metzdorff, S. B., et al. (2014) · European Journal of Immunology · doi:10.1002/eji.201444528 · Cited by 32
(−)-Epigallocatechin Gallate Inhibits TNF-α-Induced PAI-1 Production in Vascular Endothelial Cells
Cao, Y., Wang, D., Wang, X., Zhang, J., Shan, Z., & Teng, W. (2013) · Journal of Cardiovascular Pharmacology · doi:10.1097/fjc.0b013e3182a18ba8 · Cited by 15
Hasegawa‐Ishii, S., Komaki, S., Asano, H., Imai, R., & Osaki, T. (2024) · Brain Behavior & Immunity - Health · doi:10.1016/j.bbih.2024.100848 · Cited by 8
“A high fat diet also increases the abundance of Oscillibacter in fecal microbiota, which is correlated with increased permeability in the proximal colon (Lam et al., 2012).”
Shiratori, H., Hattori, K. M., Nakata, K., Okawa, T., Komiyama, S., Kinashi, Y., Kabumoto, Y., Kaneko, Y., Nagai, M., Shindo, T., et al. (2024) · International Immunology · doi:10.1093/intimm/dxae003 · Cited by 11
“Bifidobacterium and Lactobacillus stabilize tight junctions (27, 28), whereas Oscillibacter and Desulfovibrio increase the gut permeability (29).”
Lane, J. M., Wright, R. O., & Eggers, S. I. (2023) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2023.105337 · Cited by 14
Gao, T., Feng, M., Wang, Z., Cao, J., & Chen, Y. (2023) · Microbes and Infection · doi:10.1016/j.micinf.2023.105125 · Cited by 13
The impact of herbal medicine in regulating intestinal flora on female reproductive disorders
Liu, M., Yan, J. C., Wu, Y., Zhu, H., Huang, Y., & Ke-ming, W. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1026141 · Cited by 15
Czajeczny, D., Kabzińska, K., & Wójciak, R. W. (2021) · Applied Neuropsychology Adult · doi:10.1080/23279095.2021.1967155 · Cited by 11
“A study on mice by Lam et al. (2012) reported increased gut permeability and an altered gut microbiota profile along with systemic inflammation after feeding with a high fat diet.”
BackgroundBilski, J., Wójcik-Grzybek, D., Danielak, A., Mazur-Biały, A. I., Magierowski, M., Tønnesen, K., Brzozowski, B., Surmiak, M., Magierowska, K., Pajdo, R., et al. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200427090127 · Cited by 10
Ou, Y., Chen, K., Guo, J. Q., Ye, C., Zhou, X., Chen, D., Bian-sheng, L., Liu, C., & Liu, J. (2025) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2025.145679 · Cited by 9
Temporary dietary fiber depletion prompts rapid and lasting gut microbiota restructuring in mice
Rous, C., Cadiou, J., Yazbek, H., Monzel, E., Desai, M. S., Dore, J. M., van de Guchte, M., & Mondot, S. (2025) · Microbiology Spectrum · doi:10.1128/spectrum.01517-24 · Cited by 11
“Although less characterized, this genus has been negatively correlated with transepithelial resistance of the proximal colon (56), thereby favoring permeability.”
Metadata
- Authors
- 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., & Storlien, L. H.
- Affiliations
- The University of Sydney (AU)
- Corresponding author
- Lam, Yan Y.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-03-23
- Volume
- 7
- Issue
- 3
- Pages
- e34233
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3311621
- OpenAlex
- W2000450805
- Cited by
- 604
- References
- 72
- Citations by year
- 2026: 24 · 2025: 33 · 2024: 39 · 2023: 58 · 2022: 62 · 2021: 59 · 2020: 58 · 2019: 53 · 2018: 44 · 2017: 41 · 2016: 41 · 2015: 34 · 2014: 29 · 2013: 21 · 2012: 8
- FWCI
- 11.84
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Figshare (submittedVersion, cc-by)
- Minerva Access (University of Melbourne) (submittedVersion, cc-by)
- Funders
- Medical Research Council
- National Health and Medical Research Council (633240)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- diet-induced obesity, high saturated fat diet, intestinal permeability, gut microbiota, mesenteric fat inflammation, visceral adipose tissue, metabolic dysfunction, tight junctions, ZO-1, TNF-α, interleukin-6, adipose tissue macrophages, Lactobacillus, Oscillibacter, adiponectin, serum amyloid A
- MeSH terms
- Animals, Diet, Female, Inflammation, Intestinal Mucosa, Intestines, Mesentery, Mice, Inbred C57BL, Permeability, Mice
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