The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon
Open accessAbstract
The microbiome is being characterized by large-scale sequencing efforts, yet it is not known whether it regulates host metabolism in a general versus tissue-specific manner or which bacterial metabolites are important. Here, we demonstrate that microbiota have a strong effect on energy homeostasis in the colon compared to other tissues. This tissue specificity is due to colonocytes utilizing bacterially produced butyrate as their primary energy source. Colonocytes from germfree mice are in an energy-deprived state and exhibit decreased expression of enzymes that catalyze key steps in intermediary metabolism including the TCA cycle. Consequently, there is a marked decrease in NADH/NAD(+), oxidative phosphorylation, and ATP levels, which results in AMPK activation, p27(kip1) phosphorylation, and autophagy. When butyrate is added to germfree colonocytes, it rescues their deficit in mitochondrial respiration and prevents them from undergoing autophagy. The mechanism is due to butyrate acting as an energy source rather than as an HDAC inhibitor.
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The pathophysiological consequences of low butyrate in critical illness are predictable (epithelial cell death and dysregulated inflammation), but the clinical consequences are unknown.
“The pathophysiological consequences of this condition are predictable (epithelial cell death and dysregulated inflammation), but the clinical consequences are unknown.”
From The microbiome and critical illness (2016) · cites this paper as [75]
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Martin‐Gallausiaux, C., Marinelli, L., Blottière, H. M., Larraufie, P., & Lapaque, N. (2020) · Proceedings of The Nutrition Society · doi:10.1017/s0029665120006916 · Cited by 1,533 · see citing works
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“Substantial quantities of short fatty acids are absorbed by the tissue epithelial cells; for example, butyrate seems to have a key role to play in colon epithelial protection and metabolism (49, 50).”
Bile acids and the gut microbiome
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“From these substrates, gut bacteria produce short-chain fatty acids (acetate, propionate, butyrate) that can account for up to 10% of the total caloric intake per day [2].”
BackgroundRegulation of immune cell function by short‐chain fatty acids
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“First, SCFAs-producing taxa are usually commensal, beneficial bacteria, with a direct positive effect on the gut barrier and immunity beyond the production of SCFAs [55,114].”
BackgroundHabitat degradation impacts black howler monkey ( Alouatta pigra ) gastrointestinal microbiomes
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“Butyrogenic and acetogenic metabolism are particularly beneficial as they allow optimal energy gain, and butyrate promotes intestinal development and health (Donohoe et al., 2011; Grootaert et al., 2011).”
BackgroundMicrobiota-activated PPAR-γ signaling inhibits dysbiotic Enterobacteriaceae expansion
Byndloss, M. X., Olsan, E. E., Rivera-Chávez, F., Tiffany, C. R., Cevallos, S. A., Lokken, K. L., Torres, T. P., Byndloss, A. J., Faber, F., Gao, Y., et al. (2017) · Science · doi:10.1126/science.aam9949 · Cited by 1,237 · see citing works
“We exposed the model epithelia to butyrate, a fermentation product of the gut microbiota that serves as the main carbon source of colonic epithelial cells (colonocytes) (5).”
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“Butyrate was also shown to regulate autophagy in colonocytes by acting as an energy source [28].”
BackgroundThe oral microbiome – an update for oral healthcare professionals
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“Short-chain fatty acids (SCFA) found in breast milk are also an important source of energy [22], as well as being essential for normal maturation of the gastrointestinal tract [23].”
BackgroundChemical transformation of xenobiotics by the human gut microbiota
Koppel, N., Maini Rekdal, V., & Balskus, E. P. (2017) · Science · doi:10.1126/science.aag2770 · Cited by 1,080 · see citing works
The Human Gut Microbiome – A Potential Controller of Wellness and Disease
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“Butyrate-producing microbes rescued the deficit mitochondrial respiration, ATP synthesis and autophagy in colonocytes of germfree mice (Donohoe et al., 2011), proving the importance of butyrate in colonic cellular respiration and energy production.”
BackgroundFree Fatty Acid Receptors in Health and Disease
Kimura, I., Ichimura, A., Ohue‐Kitano, R., & Igarashi, M. (2019) · Physiological Reviews · doi:10.1152/physrev.00041.2018 · Cited by 1,032 · see citing works
“Simultaneously, FFAs can be transported from the plasma to BAT, brown adipose tissue; CCK, cholecystokinin; FFAR, free fatty acid receptor; FGF21, fibroblast growth factor-21; GIP, gastric inhibitory polypeptide; GLP-1, glucagon-like peptide 1; NLRP, NACHT, LRR, and PYD domain-containing protein; PYY, peptide YY; TNF-…”
BackgroundInfluentialNew insights into activation and function of the AMPK
Steinberg, G. R., & Hardie, D. G. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00547-x · Cited by 1,028 · see citing works
Commensal bacteria at the interface of host metabolism and the immune system
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From gut dysbiosis to altered brain function and mental illness: mechanisms and pathways
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Dietary gut microbial metabolites, short-chain fatty acids, and host metabolic regulation
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“in muscle and liver tissues, and the expression of PGC-1α and mitochondrial uncoupling protein-1 (UCP-1) in brown adipose tissues [21].”
BackgroundHill‐Burns, E. M., Debelius, J. W., Morton, J. T., Wissemann, W. T., Lewis, M. R., Wallen, Z. D., Peddada, S. D., Factor, S. A., Molho, E., Zabetian, C. P., et al. (2017) · Movement Disorders · doi:10.1002/mds.26942 · Cited by 874 · see citing works
Obesity, inflammation, and the gut microbiota
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New insights into the interplay between autophagy, gut microbiota and inflammatory responses in IBD
Larabi, A. B., Barnich, N., & Nguyen, H. T. T. (2019) · Autophagy · doi:10.1080/15548627.2019.1635384 · Cited by 840 · see citing works
“pared to conventionally raised control mice [36].”
BackgroundInfluentialGut microbiota–generated metabolites in animal health and disease
Lee, W.-J., & Hase, K. (2014) · Nature Chemical Biology · doi:10.1038/nchembio.1535 · Cited by 756 · see citing works
Exercise alters gut microbiota composition and function in lean and obese humans
ALLEN, J. M., MAILING, L. J., NIEMIRO, G. M., MOORE, R., COOK, M. D., WHITE, B. A., HOLSCHER, H. D., & WOODS, J. A. (2018) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001495 · Cited by 820 · see citing works
“Butyrate is a primary fuel source for colonocytes (39), is required for maintaining gut barrier function (40), and is a critical metabolite regulating the antiinflammatory/regulatory phenotypes of gut-resident immune cells (41).”
BackgroundThe Reciprocal Interactions between Polyphenols and Gut Microbiota and Effects on Bioaccessibility
Özdal, T., Sela, D. A., Xiao, J., Boyacıoğlu, D., Chen, F., & Çapanoğlu, E. (2016) · Nutrients · doi:10.3390/nu8020078 · Cited by 812 · see citing works
“Higher bioavailability of phenolic compounds, and the resultant beneficial health effects as determined by the consumption of whole grains, vegetables and fruits, can be related to the end-products of microbial metabolism forming short-chain fatty acids such as butyrate, and phenolic acids such as protocatechuic acid…”
BackgroundRomano, K. A., Vivas, E. I., Amador-Noguez, D., & Rey, F. E. (2015) · mBio · doi:10.1128/mbio.02481-14 · Cited by 777 · see citing works
Colonocyte metabolism shapes the gut microbiota
Litvak, Y., Byndloss, M. X., & Bäumler, A. J. (2018) · Science · doi:10.1126/science.aat9076 · Cited by 765 · see citing works
Long-term benefit of microbiota transfer therapy on autism symptoms and gut microbiota
Kang, D.-W., Adams, J. B., Coleman, D. M., Pollard, E. L., Maldonado, J., McDonough-Means, S., Caporaso, J. G., & Krajmalnik-Brown, R. (2019) · Scientific Reports · doi:10.1038/s41598-019-42183-0 · Cited by 749 · see citing works
The Colonic Crypt Protects Stem Cells from Microbiota-Derived Metabolites
Kaiko, G. E., Ryu, H., Koues, O. I., Collins, P. L., Solnica‐Krezel, L., Pearce, E. J., Pearce, E. L., Oltz, E. M., & Stappenbeck, T. S. (2016) · Cell · doi:10.1016/j.cell.2016.05.018 · Cited by 738 · see citing works
“metabolic stress and upregulates the autophagy pathway for survival (Donohoe et al., 2011).”
Short chain fatty acids: Microbial metabolites for gut-brain axis signalling
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“…of SCFAs in immune cell metabolism (Kim et al., 2014); following conversion into acetyl-CoA and integration into the Krebs cycle (Blad et al., 2012; Donohoe et al., 2011; Kim et al., 2014), they can influence T helper cell differentiation via mTOR signaling (Kim et al., 2014) or accelerate recall…”
BackgroundInfluentialDiet-Induced Dysbiosis of the Intestinal Microbiota and the Effects on Immunity and Disease
Brown, K., DeCoffe, D., Molcan, E., & Gibson, D. L. (2012) · Nutrients · doi:10.3390/nu4081095 · Cited by 682 · see citing works
“Clostridium coccoides are major producers of short chain fatty acids, particularly butyrate, which is an energy source for colonocytes and has been shown to protect against damaging inflammatory responses [42].”
BackgroundGut microbiome and aging: physiological and mechanistic insights
Nagpal, R., Mainali, R., Ahmadi, S., Wang, S., Singh, R., Kavanagh, K., Kitzman, D. W., Kushugulova, A., Marotta, F., & Yadav, H. (2018) · Nutrition and Healthy Aging · doi:10.3233/nha-170030 · Cited by 670 · see citing works
“[148] Donohoe DR, Garge N, Zhang X, Sun W, O’Connell TM, Bunger MK, Bultman SJ.”
BackgroundHoneybee gut microbiota promotes host weight gain via bacterial metabolism and hormonal signaling
Zheng, H., Powell, J. E., Steele, M. I., Dietrich, C., & Moran, N. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1701819114 · Cited by 664 · see citing works
“Short-chain fatty acids (SCFAs), namely acetate, propionate, and butyrate, produced by the gut microbiota as main fermentation products of dietary fiber accumulate in the human colon in concentrations up to 80–130 mM (12) and serve as a major energy source for intestinal epithelial cells (13) or as the main respirator…”
BackgroundInsights into the role of the microbiome in obesity and type 2 diabetes
Hartstra, A. V., Bouter, K. E. C., Bäckhed, F., & Nieuwdorp, M. (2015) · Diabetes Care · doi:10.2337/dc14-0769 · Cited by 641 · see citing works
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“The dependence of colonocytes on butyrate produced by bacteria was demonstrated in an elegant study by Donohoe et al. [37] who showed ATP depletion and autophagy in colonocytes of the germ-free mice and their reversal by addition of butyrate.”
BackgroundButyrate, neuroepigenetics and the gut microbiome: Can a high fiber diet improve brain health?
Bourassa, M. W., Alim, I., Bultman, S. J., & Ratan, R. R. (2016) · Neuroscience Letters · doi:10.1016/j.neulet.2016.02.009 · Cited by 636 · see citing works
“It was recently shown that germ free mice, which lack a microbiome, had a significantly reduced NADH/NAD+ ratio and reduced ATP levels in the colon compared to conventionally raised mice with a normal microbiome [56].”
Gut-derived short-chain fatty acids are vividly assimilated into host carbohydrates and lipids
den Besten, G., Lange, K., Havinga, R., van Dijk, T. H., Gerding, A., van Eunen, K., Müller, M. M., Groen, A. K., Hooiveld, G. J. E. J., Bakker, B. M., et al. (2013) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00265.2013 · Cited by 606 · see citing works
“In the 41 last decades it became apparent that SCFAs might play a key role in the prevention and treatment of 42 metabolic syndrome, bowel disorders and certain types of cancer (14, 17, 45, 47).”
BackgroundFellows, R., Denizot, J., Stellato, C., Cuomo, A., Jain, P., Stoyanova, E., Balázsi, S., Hajnády, Z., Liebert, A., Kazakevych, J., et al. (2018) · Nature Communications · doi:10.1038/s41467-017-02651-5 · Cited by 568 · see citing works
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The gut microbiota influences skeletal muscle mass and function in mice
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Dysregulated Microbial Fermentation of Soluble Fiber Induces Cholestatic Liver Cancer
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Interactions between Roseburia intestinalis and diet modulate atherogenesis in a murine model
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“For example, the gut microbiota has a strong effect on energy homeostasis in the colon, attributed to the use of butyrate produced by gut bacteria as the primary energy source for colonocytes (Donohoe et al. 2011).”
BackgroundMcNabney, S. M., & Henagan, T. M. (2017) · Nutrients · doi:10.3390/nu9121348 · Cited by 513 · see citing works
“For example, isolated colonocytes from germ-free C57BL/6 mice exhibited NADH/NAD+ ratios that were 16-fold lower than their conventionally raised counterparts, as well as 56% lower ATP levels [9].”
BackgroundAlterations of the Gut Microbiome in Hypertension
Yan, Q., Gu, Y., Li, X., Yang, W. Q., Jia, L., Chen, C., Han, X., Huang, Y., Zhao, L., Li, P., et al. (2017) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2017.00381 · Cited by 496 · see citing works
“Functionally, SCFAs modulates the gut inflammation and metabolism via functioning as important colonocytes energy source and signaling molecules (Donohoe et al., 2011), suggesting that low level of SCFA production in gut microbiota may be a considerable risk factor of multiple metabolic syndromes…”
BackgroundSystemic short chain fatty acids limit antitumor effect of CTLA-4 blockade in hosts with cancer
Coutzac, C., Jouniaux, J.-M., Paci, A., Schmidt, J., Mallardo, D., Seck, A., Asvatourian, V., Cassard, L., Saulnier, P., Lacroix, L., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16079-x · Cited by 513 · see citing works
Intestinal Microbiota in Cardiovascular Health and Disease
Tang, W. H. W., Bäckhed, F., Landmesser, U., & Hazen, S. L. (2019) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2019.03.024 · Cited by 508 · see citing works
“SCFAs, in particular, butyrate, can serve as energy substrates for epithelial cells of the intestines (60,61).”
BackgroundZheng, L., Kelly, C. J., & Colgan, S. P. (2015) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00191.2015 · Cited by 488 · see citing works
Gut microbiota influence immunotherapy responses: mechanisms and therapeutic strategies
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“These processes provide intestinal mucosal epithelial cell energy, improve intestinal villus structure, inhibit autophagy, and preserve intestinal homeostasis [89, 90].”
BackgroundCalder, P. C., Bosco, N., Bourdet‐Sicard, R., Capuron, L., Delzenne, N. M., Dore, J. M., Franceschi, C., Lehtinen, M. J., Recker, T., Salvioli, S., et al. (2017) · Ageing Research Reviews · doi:10.1016/j.arr.2017.09.001 · Cited by 498 · see citing works
“SCFAs affect the intestinal mucosa (Donohoe et al., 2011) as well as peripheral tissues, influencing host metabolism (Tremaroli and Bäckhed, 2012).”
Microbiome, metabolites and host immunity
Levy, M., Blacher, E., & Elinav, E. (2016) · Current Opinion in Microbiology · doi:10.1016/j.mib.2016.10.003 · Cited by 488 · see citing works
Polyphenol-Mediated Gut Microbiota Modulation: Toward Prebiotics and Further
Rodríguez-Daza, M.-C., Pulido-Mateos, E. C., Lupien‐Meilleur, J., Guyonnet, D., Desjardins, Y., & Roy, D. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.689456 · Cited by 489 · see citing works
“Among the SCFA, butyrate reinforces the intestinal mucosal barrier (41, 42), suppresses proinflammatory effectors in macrophages, and promotes the differentiation of dendritic cells (9).”
BackgroundZeng, H., Umar, S., Rust, B., Lazarova, D., & Bordonaro, M. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20051214 · Cited by 480 · see citing works
“Butyrate is selectively taken up by the colonic epithelium (via monocarboxylate transporter 1 and other transporters) and provides colonocytes with approximately 70% of their energy [70] and is required for energy homeostasis [71,72]; whereas, acetate and propionate are primarily transported to muscle and liver tissue…”
BackgroundGut microbial metabolism drives transformation of MSH2-deficient colon epithelial cells
Belcheva, A., Irrazabal, T., Robertson, S. J., Streutker, C., Maughan, H., Rubino, S., Moriyama, E. H., Copeland, J. K., Surendra, A., Kumar, S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.04.051 · Cited by 473 · see citing works
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“Our data also support a molecular mechanism where microbial fermentation of fiber yields butyrate, which serves as the preferred energy source of normal colonocytes and supports homeostasis (11,25) but accumulates in cancerous colonocytes due to the Warburg effect and functions as an HDAC inhibitor to inhibit cell pro…”
BackgroundHealthy infants harbor intestinal bacteria that protect against food allergy
Feehley, T., Plunkett, C. H., Bao, R., Hong, S. M. C., Culleen, E., Belda‐Ferre, P., Campbell, E., Aitoro, R., Nocerino, R., Paparo, L., et al. (2019) · Nature Medicine · doi:10.1038/s41591-018-0324-z · Cited by 474 · see citing works
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Microbial dysbiosis-induced obesity: role of gut microbiota in homoeostasis of energy metabolism
Amabebe, E., Robert, F. O., Agbalalah, T., & Orubu, E. S. F. (2020) · British Journal Of Nutrition · doi:10.1017/s0007114520000380 · Cited by 459 · see citing works
The microbiome and critical illness
Dickson, R. P. (2016) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(15)00427-0 · Cited by 460 · see citing works
Trevelline, B. K., Fontaine, S. S., Hartup, B. K., & Kohl, K. D. (2019) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2018.2448 · Cited by 454 · see citing works
Lung microbiome: new insights into the pathogenesis of respiratory diseases
Li, R., Li, J., & Zhou, X. (2024) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01722-y · Cited by 466 · see citing works
“417 418 – 420 In addition to SCFAs, polysaccharide A inhibits the production of proin fl ammatory IL-17 and promotes the expression of IL-10 by CD4 + T cells.”
BackgroundHodgkinson, K. M., Abbar, F. E., Dobranowski, P., Manoogian, J., Butcher, J., Figeys, D., Mack, D. R., & Stintzi, A. P. (2022) · Clinical Nutrition · doi:10.1016/j.clnu.2022.10.024 · Cited by 446 · see citing works
Role of the Microbiome in Energy Regulation and Metabolism
Nieuwdorp, M., Gilijamse, P. W., Pai, N., & Kaplan, L. M. (2014) · Gastroenterology · doi:10.1053/j.gastro.2014.02.008 · Cited by 421 · see citing works
Surface components and metabolites of probiotics for regulation of intestinal epithelial barrier
Liu, Q., Yu, Z., Tian, F., Zhao, J., Zhang, H., Zhai, Q., & Chen, W. (2020) · Microbial Cell Factories · doi:10.1186/s12934-020-1289-4 · Cited by 438 · see citing works
Gut Microbiota Profiling: Metabolomics Based Approach to Unravel Compounds Affecting Human Health
Vernocchi, P., Del Chierico, F., & Putignani, L. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.01144 · Cited by 426 · see citing works
Quantifying Diet-Induced Metabolic Changes of the Human Gut Microbiome
Shoaie, S., Ghaffari, P., Kovatcheva‐Datchary, P., Mardinoğlu, A., Sen, P., Pujos‐Guillot, E., de Wouters, T., Juste, C., Rizkalla, S. W., Chilloux, J., et al. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.07.001 · Cited by 417 · see citing works
“…of dietary polysaccharides in the gut, are an important energy source for colonocytes and also function as signaling molecules, modulating intestinal inflammation and metabolism (Donohoe et al., 2011; Fernandes et al., 2014; Samuel et al., 2008; Smith et al., 2013b; Tolhurst et al., 2012).”
BackgroundInfluentialGut Microbiota: An Integral Moderator in Health and Disease
Feng, Q., Chen, W.-D., & Wang, Y.-D. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.00151 · Cited by 407 · see citing works
“For example, Donohoe et al. (2011) reported that microbiota-produced butyrate could provide energy to colonocytes and then prevent autophagy in the colon.”
BackgroundLecomte, V., Kaakoush, N. O., Maloney, C., Raipuria, M., Huinao, K. D., Mitchell, H. M., & Morris, M. J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0126931 · Cited by 418 · see citing works
“A decrease in butyrate content of the gut of germ-free mice has been shown to promote leakiness of the gut barrier [29,77], associated with increased endotoxemia and inflammation.”
BackgroundThe gut-bone axis: How bacterial metabolites bridge the distance
Zaiss, M. M., Jones, R. M., Schett, G., & Pacifici, R. (2019) · Journal of Clinical Investigation · doi:10.1172/jci128521 · Cited by 403 · see citing works
“In addition, efficient intestinal barrier function can be restored upon supplementation of butyrate to the diet (85).”
BackgroundGut microbiota as the key controllers of “healthy” aging of elderly people
Ragonnaud, E., & Biragyn, A. (2021) · Immunity & Ageing · doi:10.1186/s12979-020-00213-w · Cited by 417 · see citing works
“Extracellular SCFAs are also utilized as substrates for β-oxydation of fatty acids in CD8 T cell [70] and colonocyte metabolism [71] after they are taken up by several G-protein coupled receptors (GPRs).”
BackgroundDietary Fiber Intake and Gut Microbiota in Human Health
Fu, J., Zheng, Y., Gao, Y., & Xu, W. (2022) · Microorganisms · doi:10.3390/microorganisms10122507 · Cited by 432 · see citing works
“SCFAs can be used by gut mucosal cells as energy sources, with butyrate the preferred energy substrate for colonocytes [56,57].”
BackgroundGut microbiota-mediated inflammation in obesity: a link with gastrointestinal cancer
Cani, P. D., & Jordan, B. F. (2018) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/s41575-018-0025-6 · Cited by 383 · see citing works
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The Role of Short Chain Fatty Acids in Inflammation and Body Health
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“…receptor-gamma coactivator 1 α (PGC-1 α ) expression and adenosine monophosphate-activated kinase (AMPK) phosphorylation in muscle and liver tissue and PGC-1 α and mitochondrial uncoupling protein-1 (UCP-1) expression in brown adipose tissue, promoting fatty acid oxidation and thermogenesis [92].”
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Mirzaei, R., Bouzari, B., Hosseini‐Fard, S. R., Mazaheri, M., Ahmadyousefi, Y., Abdi, M., Jalalifar, S., Karimitabar, Z., Teimoori, A., Keyvani, H., et al. (2021) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2021.111661 · Cited by 400 · see citing works
Variable responses of human microbiomes to dietary supplementation with resistant starch
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“The conjugate base of the acid—butyrate—is the preferred energy source for colonocytes [7].”
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RETRACTED ARTICLE: Role of the gut microbiome in chronic diseases: a narrative review
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RetractedMicrobial Modulation of Energy Availability in the Colon Regulates Intestinal Transit
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“Given that colonocytes use SCFAs, particularly butyrate, as a primary energy source, colonocytes from GF mice are energy deprived (Donohoe et al., 2011).”
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“Butyrate and acetate, which are fermentation products from dietary fibers metabolized by gut microbiota exert anti-inflammatory activity and regulate the infiltration of macrophages [143].”
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Sanchez, H. N., Moroney, J. B., Gan, H., Shen, T., Im, J. L., Li, T., Taylor, J. R., Zan, H., & Casali, P. (2020) · Nature Communications · doi:10.1038/s41467-019-13603-6 · Cited by 369 · see citing works
Butyrate in Energy Metabolism: There Is Still More to Learn
Zhang, L., Liu, C.-D., Jiang, Q., & Yin, Y. (2021) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2020.12.003 · Cited by 370 · see citing works
- Authors
- Donohoe, D. R., Garge, N., Zhang, X., Sun, W., O'Connell, T. M., Bunger, M. K., & Bultman, S. J.
- Affiliations
- University of North Carolina at Chapel Hill (US)
- RTI International (US)
- Corresponding author
- Bultman, Scott J.
- Venue
- Cell Metabolism
- Publisher
- Elsevier BV
- Published
- 2011-05
- Volume
- 13
- Issue
- 5
- Pages
- 517-526
- ISSN
- 1550-4131 (ISSN-L)
- PMC
- PMC3099420
- OpenAlex
- W2082578477
- Cited by
- 2,003
- References
- 47
- Citations by year
- 2026: 203 · 2025: 192 · 2024: 170 · 2023: 171 · 2022: 190 · 2021: 228 · 2020: 182 · 2019: 148 · 2018: 115 · 2017: 104 · 2016: 96 · 2015: 68 · 2014: 56 · 2013: 44 · 2012: 23
- FWCI
- 17.16
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 844 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell Metabolism (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- National Institutes of Health (CA125237)
- Prevent Cancer Foundation
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- gut microbiota, butyrate, colonic epithelial cells, energy metabolism, autophagy, germ-free mice, TCA cycle, oxidative phosphorylation, AMPK, p27, mitochondrial respiration, bacterial metabolites, energy homeostasis
- MeSH terms
- Animals, Autophagy, Butyrates, Cells, Cultured, Colon, Energy Metabolism, Germ-Free Life, Glucose, Male, Mice, Inbred C57BL, Mitochondria, NAD, Magnetic Resonance Spectroscopy, Oxidative Phosphorylation, Phosphorylation, Blotting, Western, Signal Transduction, Biomarkers, Oligonucleotide Array Sequence Analysis, Gene Expression Profiling, Cyclin-Dependent Kinase Inhibitor p27, Mice, Metagenome, AMP-Activated Protein Kinases, Metabolomics
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