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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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Maternal Obesity Is Associated with Alterations in the Gut Microbiome in Toddlers
Galley, J. D., Bailey, M. T., Dush, C. M. K., Schoppe‐Sullivan, S. J., & Christian, L. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113026 · Cited by 184
“Diet can substantially affect the composition of the gut microbiome [40,46,47].”
BackgroundPanwar, H., Rashmi, H. M., Batish, V. K., & Grover, S. (2012) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2376 · Cited by 167
“reduced proportions of lactobacilli in gut microbial profile, reduced transepithelial resistance and increased metabolic edotoxemia in HFD mice [23].”
BackgroundThe Role of Intestinal Mucosal Barrier in Autoimmune Disease: A Potential Target
An, J., Liu, Y., Wang, Y., Fan, R., Hu, X., Zhang, F., Yang, J., & Chen, J. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.871713 · Cited by 197
“TLR2 recognizes and binds LPS, then promotes the secretion of the mucus layer and the transfer of ZO-1 to the top of cells to strengthen tight junctions through the TLR2 signaling pathway (61, 62).”
BackgroundInulin-type fructan improves diabetic phenotype and gut microbiota profiles in rats
Zhang, Q., Yu, H., Xiao, X., Hu, L., Xin, F., & Yu, X. (2018) · PeerJ · doi:10.7717/peerj.4446 · Cited by 188
“Oscillibacter is one species within the Ruminococcaceae family whose abundance is positively correlated with gut permeability, which can affect gut barrier integrity (Lam et al., 2012).”
BackgroundThe role of diet and intestinal microbiota in the development of metabolic syndrome
Santos-Marcos, J. A., Pérez‐Jiménez, F., & Camargo, A. (2019) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.03.017 · Cited by 188
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Costa, F. R. C., Francozo, M., de Oliveira, G. G., Ignácio, A., Castoldi, Â., Zamboni, D. S., Ramos, S. G., Câmara, N. O. S., de Zoete, M. R., Palm, N. W., et al. (2016) · The Journal of Experimental Medicine · doi:10.1084/jem.20150744 · Cited by 176
Dietary cellulose prevents gut inflammation by modulating lipid metabolism and gut microbiota
Kim, Y., Hwang, S. W., Kim, S., Lee, Y., Kim, T., Lee, S.-H., Kim, S. J., Yoo, H. J., Kim, E. N., & Kweon, M. (2020) · Gut Microbes · doi:10.1080/19490976.2020.1730149 · Cited by 197
“Oscillibacter, in the family Ruminococcaceae, reportedly has a negative correlation with barrier function parameters in the colon.(58) Our metabolite analysis showed that LCD-fed mice had higher levels of saturated fatty acids, including palmitic, stearic, and myristic, and ceramides (Figure 5c), which may be crucial…”
BackgroundLiu, T., Kern, J. T., Jain, U., Sonnek, N. M., Xiong, S., Simpson, K. F., VanDussen, K. L., Winkler, E. S., Haritunians, T., Malique, A., et al. (2021) · Cell Host & Microbe · doi:10.1016/j.chom.2021.04.004 · Cited by 179
Straub, R. H., & Carsten Schradin, A. (2016) · Evolution Medicine and Public Health · doi:10.1093/emph/eow001 · Cited by 244
“The obesity-triggering microbiome has an increased capacity to harvest energy from the diet (95), but it is also linked to more inflammation in the gut and liver (96,97).”
BackgroundRegression analysis for microbiome compositional data
Shi, P., Zhang, A. R., & Li, H. (2016) · The Annals of Applied Statistics · doi:10.1214/16-aoas928 · Cited by 139
“A recent study also identified Oscillibacter-like organisms as a potentially important gut microbe that mediates high fat diet-induced gut dysfunction [Lam et al. (2012)].”
BackgroundJung, M., Lee, J., Shin, N., Kim, M., Hyun, D., Yun, J., Kim, P. S., Whon, T. W., & Bae, J. (2016) · Scientific Reports · doi:10.1038/srep30887 · Cited by 174
“Oscillibacter is positively correlated with gut permeability 43 , which can influence adiposity and systemic inflammation in obese prone donors and their GF recipients fed a HF diet 39 .”
Adipose-Tissue and Intestinal Inflammation – Visceral Obesity and Creeping Fat
Kredel, L. I., & Siegmund, B. (2014) · Frontiers in Immunology · doi:10.3389/fimmu.2014.00462 · Cited by 166
“In trinitrobenzenesulfonic acid-induced colitis in mice and rats TNFα and IL-10 in the mesenteric fat is increased while leptin and adiponectin release is not altered compared to healthy animals (40, 41).”
BackgroundInfluentialThe Role of the Gut Microbiome in Diabetes and Obesity-Related Kidney Disease
Zaky, A. A., Glastras, S. J., Wong, M. Y. W., Pollock, C. A., & Saad, S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22179641 · Cited by 176
Ma, L., Kim, J.-W., Hatzenpichler, R., Karymov, M. A., Hubert, N., Hanan, I. M., Chang, E. B., & Ismagilov, R. F. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404753111 · Cited by 158
“The genus Oscillibacter is frequently observed in the Most Wanted list (2) and other sequencing data sets (29 – 31), but no human-associated member of this genus has been cultivated yet.”
BackgroundDe Munck, T. J. I., Xu, P., Verwijs, H. J. A., Masclee, A. A. M., Jonkers, D., Verbeek, J., & Koek, G. H. (2020) · Liver International · doi:10.1111/liv.14696 · Cited by 145
Pathophysiological role of host microbiota in the development of obesity
Kobyliak, N. M., Virchenko, O., & Falalyeyeva, T. M. (2015) · Nutrition Journal · doi:10.1186/s12937-016-0166-9 · Cited by 156
“037) expression in proximal colon was observed [78].”
BackgroundB Lymphocytes in obesity-related adipose tissue inflammation and insulin resistance
Winer, D. A., Winer, S., Chng, M. H. Y., Shen, L., & Engleman, E. G. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-013-1486-y · Cited by 150
Impact of Westernized Diet on Gut Microbiota in Children on Leyte Island
Nakayama, J., Yamamoto, A., Conde, L. A., Higashi, K., Sonomoto, K., Tan, J. D., & Lee, Y. K. (2017) · Frontiers in Microbiology · doi:10.3389/fmicb.2017.00197 · Cited by 171
“For instance, Oscillibacterlike bacteria are known as a potentially important gut microbe that mediates high-fat diet-induced gut dysfunction (Lam et al., 2012).”
BackgroundMethodInfluentialMechanistic links between gut microbial community dynamics, microbial functions and metabolic health
Ha, C. W. (2014) · World Journal of Gastroenterology · doi:10.3748/wjg.v20.i44.16498 · Cited by 137
Self-citationPellegrini, S., Sordi, V., Bolla, A. M., Saita, D., Ferrarese, R., Canducci, F., Clementi, M., Invernizzi, F., Mariani, A., Bonfanti, R., et al. (2017) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-3222 · Cited by 153
“junctions (6) in rodent models (30, 31) and human subjects.”
BackgroundIntestinal epithelial barrier function in liver cirrhosis: an extensive review of the literature
Pijls, K. E., Jonkers, D. M. A. E., Elamin, E. E., Masclee, A., & Koek, G. H. (2013) · Liver International · doi:10.1111/liv.12271 · Cited by 124
High Fat Diet Causes Depletion of Intestinal Eosinophils Associated with Intestinal Permeability
Johnson, A. M. F., Costanzo, A. E., Gareau, M. G., Armando, A. M., Quehenberger, O., Jameson, J., & Olefsky, J. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0122195 · Cited by 164
“Specifically, macrophage/DC IL-10 production and induction of regulatory T (Treg) cells can promote tolerance, whereas depletion of intestinal macrophages renders mice susceptible to bacterial penetration [17,18].”
BackgroundMethodInfluentialIntestinal microbiota and the immune system in metabolic diseases
Sittipo, P., Lobionda, S., Lee, Y. K., & Maynard, C. L. (2018) · The Journal of Microbiology · doi:10.1007/s12275-018-7548-y · Cited by 150
“(ZO-1, claudin-1, and occludin) expression were decreased (Lam et al., 2012; Shen et al., 2014).”
BackgroundPedersen, R., Ingerslev, H.-C., Sturek, M. S., Alloosh, M., Cirera, S., Christoffersen, B. Ø., Moesgaard, S. G., Larsen, N., & Boyé, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0056612 · Cited by 135
“Together our results suggest that the obese Ossabaw minipigs’ gut microbiota display a profile that resembles the intestinal microbiota observed in obese mice and humans in response to HFD.”
InfluentialFleshner, M. (2013) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2012.08.012 · Cited by 126
Wu, W., Kaicen, W., Bian, X., Yang, L., Ding, S., Li, Y., Li, S., Zhuge, A., & Li, L. (2023) · Microbial Biotechnology · doi:10.1111/1751-7915.14293 · Cited by 129
Differential Analysis of Hypertension-Associated Intestinal Microbiota
Dan, X., Mushi, Z., Baili, W., Han, L., Enqi, W., Huanhu, Z., & Li, S. (2019) · International Journal of Medical Sciences · doi:10.7150/ijms.29322 · Cited by 158
“This genus might generate metabolites that directly regulate the integrity of epithelium, or it might have a double effect following changes in the overall composition of the microbiota [38].”
BackgroundVildagliptin increases butyrate-producing bacteria in the gut of diabetic rats
Zhang, Q., Xiao, X., Li, M., Yu, M., Ping, F., Zheng, J., Wang, T., & Wang, X. (2017) · PLOS ONE · doi:10.1371/journal.pone.0184735 · Cited by 124
Lai, W., Deng, W.-F., Xu, S., Zhao, J., Xu, D., Liu, Y., Guo, Y., Wang, M., He, F.-S., Ye, S.-W., et al. (2019) · Psychological Medicine · doi:10.1017/s0033291719003027 · Cited by 143
“demonstrated that Oscillibacter could produce anti-inflammatory metabolites and play a pivotal role in the maintenance of gut barrier integrity (Lam et al., 2012).”
BackgroundZhao, X., Jiang, Y., Xi, H., Chen, L., & Feng, X. (2020) · Geburtshilfe und Frauenheilkunde · doi:10.1055/a-1081-2036 · Cited by 124
“…Tremellen et al. [80] proposed that one of the pathogenic mechanisms of PCOS could be that obesity and a high-sugar, high-fat diet with low-dietary fiber encourages GM imbalance, thus destroying the junction between intestinal epithelial cells and reducing the expression of ZO-1 and occludin [81].”
Bested, A. C., Logan, A. C., & Selhub, E. M. (2013) · Gut Pathogens · doi:10.1186/1757-4749-5-3 · Cited by 121
“barrier and limit the detrimental effects of LPS [112-114].”
BackgroundToral, M., Gómez‐Guzmán, M., Jiménez, R., Romero, M., Sánchez, M., Utrilla, M. P., Garrido‐Mesa, N., Rodríguez‐Cabezas, M. E., Olivares, M. M., Gálvez, J., et al. (2014) · Clinical Science · doi:10.1042/cs20130339 · Cited by 134
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“In addition, animal studies indicate that high-fat diet (HFD)-induced obesity promotes intestinal inflammatory processes on a cellular level [5], and perturbs barrier function [6], but the underlying mechanisms remain largely unidentified.”
BackgroundRole of Obesity, Mesenteric Adipose Tissue, and Adipokines in Inflammatory Bowel Diseases
Bilski, J., Mazur-Biały, A. I., Wójcik-Grzybek, D., Surmiak, M., Magierowski, M., Śliwowski, Z., Pajdo, R., Kwiecień, S., Danielak, A., Ptak‐Belowska, A., et al. (2019) · Biomolecules · doi:10.3390/biom9120780 · Cited by 144
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“the translocation of gut bacteria derived products from the gut to blood circulation (51).”
BackgroundHigh dietary fat intake induces a microbiota signature that promotes food allergy
Hussain, M., Bonilla‐Rosso, G., Chung, C. K. C. K., Bäriswyl, L., Rodriguez, M. P., Kim, B., Engel, P., & Noti, M. (2019) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2019.01.043 · Cited by 137
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“This is in agreement with previous study suggesting that HFD triggers metabolic changes that impair gut barrier function, as reflected both by the decrease in TEER and gene expression of ZO-1 in the proximal colon [54].”
ResultImpaired Intestinal Barrier and Tissue Bacteria: Pathomechanisms for Metabolic Diseases
Massier, L., Blüher, M., Kovacs, P. L., & Chakaroun, R. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.616506 · Cited by 130
“intestinal permeability to inflammation (91, 92).”
Impairments to Thermoregulation in the Elderly During Heat Exposure Events
Millyard, A., Layden, J. D., Pyne, D. B., Edwards, A. M., & Bloxham, S. (2020) · Gerontology and Geriatric Medicine · doi:10.1177/2333721420932432 · Cited by 128
“Evidence suggests that with age there are alterations in the gut microbiota that lead to an increase in gut permeability and cytokine expression, and thus a reduced ability to repair damaged DNA (Guedj et al., 2020; Lam et al., 2012; Qi et al., 2017; Thevaranjan et al., 2017).”
BackgroundRole and Effective Therapeutic Target of Gut Microbiota in Heart Failure
Jia, Q., Li, H., Zhou, H., Zhang, X., Zhang, A., Xie, Y., Li, Y., Lv, S., & Zhang, J. (2019) · Cardiovascular Therapeutics · doi:10.1155/2019/5164298 · Cited by 119
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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