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Germ‐free C57BL/6J mice are resistant to high‐fat‐diet‐induced insulin resistance and have altered cholesterol metabolism
Abstract
Recent studies showed that germ‐free (GF) mice are resistant to obesity when consuming a high‐fat, high‐carbohydrate Western diet. However, it remains unclear what mechanisms are involved in the antiobesity phenotype and whether GF mice develop insulin resistance and dyslipidemia with high‐fat (HF) feeding. In the present study, we compared the metabolic consequences of HF feeding on GF and conventional (conv) C57BL/6J mice. GFmice consumed fewer calories, excreted more fecal lipids, and weighed significantly less than conv mice. GF/HF animals also showed enhanced insulin sensitivity with improved glucose tolerance, reduced fasting and nonfasting insuline‐mia, and increased phospho‐Akt (Ser‐473) in adipose tissue. In association with enhanced insulin sensitivity, GF/HF mice had reduced plasma TNF‐α and total serum amyloid A concentrations. Reduced hypercholes‐terolemia, a moderate accretion of hepatic cholesterol, and an increase in fecal cholesterol excretion suggest an altered cholesterol metabolism in GF/HF mice. Pronounced nucleus SREBP2 proteins and up‐regulation of cholesterol biosynthesis genes indicate that enhanced cholesterol biosynthesis contributed to the cholesterol homeostasis in GF/HF mice. Our results demonstrate that fewer calorie consumption and increased lipid excretion contributed to the obesity‐resistant phenotype of GF/HF mice and reveal that insulin sensitivity and cholesterol metabolism are metabolic targets influenced by the gut microbiota.— Rabot, S., Membrez, M., Bruneau, A., Gerard, P., Harach, T., Moser, M., Raymond, F., Mansourian, R., Chou. C. J. Germ‐free C57BL/6J mice are resistant to high‐fat‐diet‐induced insulin resistance and have altered cholesterol metabolism. FASEB J. 24, 4948–4959 (2010). www.fasebj.org
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“germ-free mice are resistant to the obesogenic effects of high-fat diets243”
From Comorbidity between major depressive disorder and physical diseases: a comprehensive review of epidemiology, mechanisms and management (2023) · cites this paper as [243]
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“Germ-free (GF) mice are protected from the metabolic consequences of high-fat diets, suggesting that gut microbes may be important mediators of lipid-induced metabolic dysfunction (28).”
From The gut microbiota at the intersection of diet and human health (2018) · cites this paper as [28]
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“The gut microbiota has been shown to affect lipid metabolism and lipid levels in blood and tissues, both in mice and humans.”
From Dietary lipids, gut microbiota and lipid metabolism (2019) · cites this paper as [31]
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“In contrast, circulating triglycerides, HDL, and total cholesterol levels are increased by the gut microbiota in mice on a high-fat diet [31].”
From Dietary lipids, gut microbiota and lipid metabolism (2019) · cites this paper as [31]
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Gut microbiota of obese subjects with Prader-Willi syndrome is linked to metabolic health
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Sun, C., Zheng, Z., Chen, C., Lu, B.-W., & Liu, D. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.859206 · Cited by 47
Ohnishi, M., Kato, S., Akiyoshi, J., Atfi, A., & Razzaque, M. S. (2011) · The FASEB Journal · doi:10.1096/fj.10-167056 · Cited by 47
“with morphological changes of the liver (12, 20, 21).”
BackgroundMartinez, K., Pierre, J. F., & Chang, E. B. (2016) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2016.07.001 · Cited by 51
Tazi, A., Araújo, J. R., Mulet, C., Arena, E. T., Nigro, G., Pédron, T., & Sansonetti, P. J. (2018) · mBio · doi:10.1128/mbio.01493-18 · Cited by 46
“Importantly regarding the current work, the gut microbiota directly affects nutrients, especially fatty acids (FA), and cholesterol absorption by enterocytes (8, 9) and regulates key intestinal and metabolic functions such as insulin sensitivity, fat storage, and energy expenditure (10–12).”
BackgroundAsare‐Bediako, B., Noothi, S. K., Calzi, S. L., Athmanathan, B., Vieira, C. P., Adu-Agyeiwaah, Y., Dupont, M., Jones, B. A., Wang, X. X., Chakraborty, D., et al. (2020) · Cells · doi:10.3390/cells9020464 · Cited by 46
Su, C., Chen, C., Jiao, L., Long, S. R., Mao, T., Ji, Q., O’Donnell, S. T., Stanton, C., Zheng, S., Walker, W. A., et al. (2020) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2020.06.010 · Cited by 47
The intestinal mycobiome as a determinant of host immune and metabolic health
Gutierrez, M. W., & Arrieta, M. (2021) · Current Opinion in Microbiology · doi:10.1016/j.mib.2021.04.004 · Cited by 45
Wang, Y., Li, J., Tang, L., Wang, Y., Charnigo, R. J., de Villiers, W. J. S., & Eckhardt, E. R. M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013951 · Cited by 46
“However, high-fat diets fail to induce obesity and the associated chronic inflammation in germfree mice [19,20,29,30].”
BackgroundMehta, N. N., Heffron, S. P., Patel, P. N., Ferguson, J. F., Shah, R. D., Hinkle, C. C., Krishnamoorthy, P. M., Shah, R., Tabita‐Martinez, J., Terembula, K., et al. (2012) · Journal of Translational Medicine · doi:10.1186/1479-5876-10-124 · Cited by 45
Scott, F. H., Malagon, S. G. G., O’Brien, B. A., Fennema, D., Veeravalli, S., Coveney, C. R., Phillips, I. R., & Shephard, E. A. (2017) · Drug Metabolism and Disposition · doi:10.1124/dmd.117.076612 · Cited by 43
“Indeed, Fmo5 mice display metabolic characteristics associated with mice raised in the absence of microorganisms, that is, germ-free, which, in comparison with conventionally reared mice, weigh less, store less fat, have lower plasma glucose and insulin and greater insulin sensitivity and glucose tolerance (Backhed et…”
BackgroundLynch, A., Crowley, E., Casey, E., Cano, R., Shanahan, R., McGlacken, G. P., Marchesi, J. R., & Clarke, D. J. (2017) · Scientific Reports · doi:10.1038/s41598-017-13774-6 · Cited by 46
Sample storage conditions induce post-collection biases in microbiome profiles
Jenkins, S. V., Vang, K. B., Gies, A. J., Griffin, R. J., Jun, S., Nookaew, I., & Dings, R. P. M. (2018) · BMC Microbiology · doi:10.1186/s12866-018-1359-5 · Cited by 45
“The fecal matter of C57BL/6 mice was used, as they are one of the most common animals employed in research, especially in regards to studying gut microbiota related diseases [13].”
MethodThe Gut Microbiota: How Does It Influence the Development and Progression of Liver Diseases
Kanmani, P., Kanmani, S., & Kim, H. (2020) · Biomedicines · doi:10.3390/biomedicines8110501 · Cited by 44
“Germ-free mice fed a high-fat diet (HFD) showed lower levels of lipids in the liver compared to HFD fed conventional mice [110].”
BackgroundChen, S., Yang, M., Wang, R., Fan, X., Tang, T., Li, P., Zhou, X., & Qi, K. (2022) · European Journal of Nutrition · doi:10.1007/s00394-021-02769-9 · Cited by 43
Deciphering Human Microbiota–Host Chemical Interactions
Silpe, J. E., & Balskus, E. P. (2020) · ACS Central Science · doi:10.1021/acscentsci.0c01030 · Cited by 43
Periodontal bacteria influence systemic diseases through the gut microbiota
Xi, M., Ruan, Q., Zhong, S., Li, J., Qi, W., Xie, C., Wang, X., Abuduxiku, N., & Ni, J. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1478362 · Cited by 49
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Estrogen receptor beta mediates hepatotoxicity induced by perfluorooctane sulfonate in mouse
Xu, C. Y., Jiang, Z., Liu, Q., Liu, H., & Gu, A. (2017) · Environmental Science and Pollution Research · doi:10.1007/s11356-017-8943-3 · Cited by 43
“Previous studies using conventional and germ-free mice demonstrated that cholesterol metabolism is modulated by gut microbiota (Rabot et al. 2010).”
BackgroundGut microbiota impairs insulin clearance in obese mice
Foley, K. P., Zlitni, S., Duggan, B. M., Barra, N. G., Anhê, F. F., Cavallari, J. F., Henriksbo, B. D., Chen, C. Y., Huang, M., Lau, T. C., et al. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101067 · Cited by 42
“This antibiotic cocktail was chosen speci fi cally for its ability to lower blood glucose and improve insulin sensitivity in HFD-fed mice without causing weight loss [21,28].”
Li, L., Ma, L., Wen, Y., Xie, J., Yan, L., Ji, A., Zeng, Y., Tian, Y., & Sheng, J. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.861588 · Cited by 41
Yao, M., Qv, L., Lu, Y., Wang, B., Berglund, B., & Li, L. (2020) · Engineering · doi:10.1016/j.eng.2020.01.017 · Cited by 44
Iron Reshapes the Gut Microbiome and Host Metabolism
Botta, A. M., Barra, N. G., Lam, N. H., Chow, S., Pantopoulos, K., Schertzer, J. D., & Sweeney, G. (2021) · Journal of Lipid and Atherosclerosis · doi:10.12997/jla.2021.10.2.160 · Cited by 44
NOD1 in the interplay between microbiota and gastrointestinal immune adaptations
Fernández-García, V., González-Ramos, S., Martín‐Sanz, P., del Portillo, F. G., Laparra, J. M., & Boscá, L. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105775 · Cited by 41
“Sucrose and other simple CHO, alone or included in a Western-style high-fat, high-sugar diet, rapidly trigger microbiota remodeling and dysbiosis [94,95].”
BackgroundObesity-Driven Gut Microbiota Inflammatory Pathways to Metabolic Syndrome
Silva, L. H. A. C., Galvão, J. G. F. M., da Silva, J. S. D. F., de Sales-Neto, J. M., & Rodrigues‐Mascarenhas, S. (2015) · Frontiers in Physiology · doi:10.3389/fphys.2015.00341 · Cited by 42
“Gastrointestinal microbiota also interferes with carbohydrate, lipid and amino acid metabolism (Hooper et al., 2002), complementing our own human metabolic apparatus (Bäckhed et al., 2004, 2007; Cani and Delzenne, 2009; Rabot et al., 2010).”
BackgroundNon-alcoholic fatty liver disease and obesity: the role of the gut bacteria
Schwenger, K. J. P., Bolzon, C. M., Li, C., & Allard, J. P. (2018) · European Journal of Nutrition · doi:10.1007/s00394-018-1844-5 · Cited by 40
Human Gut Microbiome and Liver Diseases: From Correlation to Causation
Li, R., Mao, Z., Ye, X., & Zuo, T. (2021) · Microorganisms · doi:10.3390/microorganisms9051017 · Cited by 40
“tected against high fat diet (HFD) induced obesity, and conventionalization of GF mice leads to an increase in body-fat content and insulin resistance [35,36].”
BackgroundMaturational patterns of the infant gut mycobiome are associated with early-life body mass index
Gutierrez, M. W., Mercer, E. M., Moossavi, S., Laforest‐Lapointe, I., Reyna, M. E., Becker, A. B., Simons, E., Mandhane, P. J., Turvey, S. E., Moraes, T. J., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.100928 · Cited by 39
Adaptive Immunity and Antigen‐Specific Activation in Obesity‐Associated Insulin Resistance
Chng, M. H. Y., Alonso, M. N., Barnes, S. E., Nguyen, K. D., & Engleman, E. G. (2015) · Mediators of Inflammation · doi:10.1155/2015/593075 · Cited by 39
“Germ free mice, for example, are resistant to weight gain and IR [135].”
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Oral–Gut Microbiome Axis in Gastrointestinal Disease and Cancer
Park, S.-Y., Hwang, B.-O., Lim, M., Ok, S. H., Lee, S., Chun, K., Park, K.-K., Hu, Y., Chung, W., & Song, N. (2021) · Cancers · doi:10.3390/cancers13071748 · Cited by 44
Jiang, L.-L., Hong, Y., Xiao, P., Wang, X., Zhang, J., Liu, E., Li, H., & Cai, Z. (2022) · Environmental Health Perspectives · doi:10.1289/ehp10281 · Cited by 38
“26,45 Here, we found the metabolic pathway involving amino acid metabolism strongly associated with PFOS-induced liver injury.”
Li, Y., Huang, J., Zhang, S., Yang, F., Zhou, H., Song, Y., Wang, B., & Li, H. (2022) · International Journal of Biological Macromolecules · doi:10.1016/j.ijbiomac.2022.06.073 · Cited by 40
Metadata
- Authors
- Rabot, S., Membrez, M., Bruneau, A., Gérard, P., Harach, T., Moser, M., Raymond, F., Mansourian, R., & Chou, C. J.
- Affiliations
- Microbiologie de l’alimentation au service de la santé (FR)
- Department of Nutrition and Health Nestlé Research Center Lausanne Switzerland
- Nestlé (Switzerland) (CH)
- Department of Bioanalytical Science Nestlé Research Center Lausanne Switzerland
- Venue
- The FASEB Journal
- Publisher
- Wiley
- Published
- 2010-08-19
- Volume
- 24
- Issue
- 12
- Pages
- 4948-4959
- ISSN
- 0892-6638 (ISSN-L)
- 1530-6860
- OpenAlex
- W2088697466
- Cited by
- 610
- References
- 41
- Citations by year
- 2026: 9 · 2025: 19 · 2024: 34 · 2023: 43 · 2022: 50 · 2021: 64 · 2020: 75 · 2019: 49 · 2018: 42 · 2017: 40 · 2016: 39 · 2015: 44 · 2014: 24 · 2013: 33 · 2012: 22
- FWCI
- 10.17
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The FASEB Journal (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- 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 › Endocrinology, Diabetes and Metabolism › Diet, Metabolism, and Disease
- Keywords
- germ-free mice, gut microbiota, high-fat diet, insulin resistance, cholesterol metabolism, hypercholesterolemia, obesity resistance, glucose tolerance, TNF-α, serum amyloid A, SREBP2, cholesterol biosynthesis, liver cholesterol, fecal cholesterol excretion, C57BL/6J mice
- MeSH terms
- Animals, Body Weight, Cholesterol, Dietary Fats, Germ-Free Life, Glucose Tolerance Test, Glycogen, Insulin Resistance, Lipids, Liver, Male, Mice, Inbred C57BL, Obesity, Blotting, Western, Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, Mice
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