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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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The Role of Gut Microbiota and Leaky Gut in the Pathogenesis of Food Allergy
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“In addition, a diet high in saturated fats decreases the abundance of Lactobacilli, while increasing the number of Oscillospiraceae , which is negatively correlated with the mRNA expression of Zonulin-1 (ZO-1), a barrier-forming TJ protein, leading to the condition of leaky gut [70].”
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“Disturbance of the intestinal barrier function is involved in adipose tissue inflammation in obesity((4,35)).”
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“190,191 Importantly, significant differences in the microbial diversity and composition of gut microbiota between the MHO and MUHO phenotypes have been reported.”
BackgroundMilard, M., Laugerette, F., Durand, A., Buisson, C., Meugnier, E., Loizon, E., Louche‐Pélissier, C., Sauvinet, V., Garnier, L., Viel, S., et al. (2019) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.201801078 · Cited by 59
Role of Dietary Lipids in Modulating Inflammation through the Gut Microbiota
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“At present, studies have corroborated these findings and strongly suggest that dietary lipids indeed play a part in enhancing gut inflammation and permeability wherein concomitant shifts in microbial community structure follow [80,81].”
ResultDiet alters probiotic L actobacillus persistence and function in the intestine
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Ginsenoside Rc ameliorated atherosclerosis via regulating gut microbiota and fecal metabolites
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“Moreover, citrulline in arginine biosynthesis was negatively correlated with gut microbiota (Eubacterium_coprostanoligenes_group and Oscillibacter) and AS indexes, while it was positively connected with Muribaculaceae and Ileibacterium.”
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“Bacterial-induced inflammation is derived from LPS increase but also intestinal barrier-enhanced permeability, producing chain reactions with adverse effects [50].”
BackgroundThe Association between Gut Microbiota and Uremia of Chronic Kidney Disease
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“Elevated Oscillibacter abundance had been found in patients with stroke and closely related to gut permeability and host inflammation [34,35].”
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Update on gut microbiota in cardiovascular diseases
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“The role of gut inflammation in VAT dysfunction is supported by data showing that in both obesity and Crohn’s disease, VAT displays similar metabolic dysfunctions and inflammatory cytokine profile (12, 37).”
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Gut barrier impairment by high-fat diet in mice depends on housing conditions.
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“[26] reported a decrease in TER only in the proximal colon, whereas Stenman et al.”
BackgroundCharacterization of the fecal microbiome in different swine groups by high-throughput sequencing
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Oral Infections, Metabolic Inflammation, Genetics, and Cardiometabolic Diseases
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“However, metainflammation can increase intestinal cell permeability and alter gut microbiota (Lam et al. 2012).”
BackgroundA high-fat diet alters genome-wide DNA methylation and gene expression in SM/J mice
Keleher, M. R., Zaidi, R., Hicks, L., Shah, S., Xing, X., Li, D., Wang, T., & Cheverud, J. M. (2018) · BMC Genomics · doi:10.1186/s12864-018-5327-0 · Cited by 57
Probiotic B420 and prebiotic polydextrose improve efficacy of antidiabetic drugs in mice
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Changing views on diverticular disease: impact of aging, obesity, diet, and microbiota
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Nutritional modulators of ulcerative colitis: Clinical efficacies and mechanistic view
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“Similarly, obesity is linked to IBDpathogenesis (Boutros andMaron, 2011; Ding et al., 2010; Ding and Lund, 2011; Goncalves et al., 2015; Zhang et al., 2012), partly due to mesenteric WAT hypertrophy.”
BackgroundPopular Exclusionary Diets for Inflammatory Bowel Disease
Hwang, C., Ross, V., & Mahadevan, U. (2014) · Inflammatory Bowel Diseases · doi:10.1097/01.mib.0000438427.48726.b0 · Cited by 53
“On a cellular level, multiple animal studies have shown that prolonged feeding of a high-fat diet seems to promote colitis/ ileitis and to perturb barrier function.(46,47) In addition, several groups have demonstrated that a high-fat diet does seem to cause significant shifts in microbiome composition and gene express…”
BackgroundMain characteristics of metabolically obese normal weight and metabolically healthy obese phenotypes
Teixeira, T. F., Alves, R. D. M., Moreira, A. P. B., & Pelúzio, M. D. C. G. (2015) · Nutrition Reviews · doi:10.1093/nutrit/nuu007 · Cited by 61
Tousoulis, D., Guzik, T. J., Padró, T., Duncker, D. J., Luca, G. D., Eringa, E. C., Vavlukis, M., Antonopoulos, A. S., Katsimichas, T., Cenko, E., et al. (2022) · Cardiovascular Research · doi:10.1093/cvr/cvac057 · Cited by 67
“129 Thus, targeting the interactions between the host and gut microorganisms through change of dietary patterns may lead to prevention of CVD.”
BackgroundSohn, W., Jun, D. W., Lee, K. N., Lee, H. L., Lee, O. Y., Choi, H. S., & Yoon, B. C. (2015) · Digestive Diseases and Sciences · doi:10.1007/s10620-015-3770-1 · Cited by 56
“Increased gut permeability and dysbiosis-related endotoxemia were demonstrated in obesity as well as in NAFLD [3, 26].”
BackgroundGoodrich, K. M., Fundaro, G., Griffin, L. E., Grant, A., Hulver, M., Ponder, M., & Neilson, A. (2012) · Nutrition Research · doi:10.1016/j.nutres.2012.09.004 · Cited by 53
“[23] Lam YY, Ha CWY, Campbell CR, Mitchell AJ, Dinudom A, Oscarsson J, et al.”
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“It is reported that Oscillibacter was increased in the diet-induced metabolic dysfunctions, and associated with impaired intestinal barrier integrity (Lam et al., 2012).”
BackgroundDelahaye, L. B., Bloomer, R. J., Butawan, M. B., Wyman, J. M., Hill, J. L., Lee, H. W., Liu, A. C., McAllan, L., Han, J. C., & van der Merwe, M. (2018) · Applied Physiology, Nutrition, and Metabolism · doi:10.1139/apnm-2017-0706 · Cited by 52
Microbiota in mesenteric adipose tissue from Crohn’s disease promote colitis in mice
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“Alteration of intestinal microbiota in high-fat-diet-fed mice associated with transmucosal bacterial translocation to mAT and blood [10, 11].”
BackgroundBiodiversity of protists and nematodes in the wild nonhuman primate gut
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“, Oscillibacter) [94], but also those that may be protective against infection (e.”
BackgroundInfluentialDeficiency of essential dietary n-3 PUFA disrupts the caecal microbiome and metabolome in mice
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“For example, high n -6 dietary intake induces gut microbiota dysbiosis resulting in increased intestinal permeability, metabolic dysfunction and adipose tissue in fl ammation, which is reversed by n -3 feeding (10) .”
Klingbeil, E. A., Cawthon, C. R., Kirkland, R. A., & Serre, C. B. D. L. (2019) · Nutrients · doi:10.3390/nu11112710 · Cited by 58
“Obesity-associated microbiota is characterized by an increase in its pro-inflammatory potential [12,13] Additionally, dysbiosis alters GI epithelial barrier function, allowing bacterial by-product to exit the gut into the circulatory system [6,13,14].”
BackgroundA general framework for association analysis of microbial communities on a taxonomic tree
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Farsi, D. N., Lara, J., Koutsidis, G., Nelson, A., Finnigan, T. J. A., Cheung, W., Muñoz-Muñoz, J., & Commane, D. M. (2023) · European Journal of Nutrition · doi:10.1007/s00394-023-03088-x · Cited by 62
“While observational data are conflicting, with studies showing Alistipes to be associated with both health and disease [47], Oscillobacter has been linked with weight gain, metabolic dysfunction and a leaky gut [48].”
Result
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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