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Calorie restriction alters mitochondrial protein acetylation
Open accessAbstract
Summary: Calorie restriction (CR) increases lifespan in organisms ranging from budding yeast through mammals. Mitochondrial adaptation represents a key component of the response to CR. Molecular mechanisms underlying this adaptation are largely unknown. Here we show that lysine acetylation of mitochondrial proteins is altered during CR in a tissue‐specific fashion. Via large‐scale mass spectrometry screening, we identify 72 candidate proteins involved in a variety of metabolic pathways with altered acetylation during CR. Mitochondrial acetylation changes may play an important role in the pro‐longevity CR response.
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“Metabolic supplier organs such as the liver and kidney demonstrate mitochondrial hyperacetylation under CR, as does the heart (Schwer et al. 2009); brain mitochondrial acetylation was unchanged, however, and skeletal muscle acetylation decreased.”
From The Mitochondrial Acylome Emerges: Proteomics, Regulation by Sirtuins, and Metabolic and Disease Implications (2018) · cites this paper as Schwer et al. 2009
In the citing paper
“Metabolic supplier organs such as the liver and kidney demonstrate mitochondrial hyperacetylation under CR, as does the heart (Schwer et al. 2009); brain mitochondrial acetylation was unchanged, however, and skeletal muscle acetylation decreased.”
From The Mitochondrial Acylome Emerges: Proteomics, Regulation by Sirtuins, and Metabolic and Disease Implications (2018) · cites this paper as Schwer et al. 2009
In the citing paper
“Intriguingly, CR enhances mitochondrial protein acetylation in diverse tissues, such as liver, heart, and kidney (Schwer et al, 2009).”
From Mitochondrial response to nutrient availability and its role in metabolic disease (2014) · cites this paper as Schwer et al, 2009
In the citing paper
“Additionally, acetylation is regulated by perturbation of energy metabolism as demonstrated by an increase in mitochondrial protein acetylation upon fasting (Kim et al., 2006) and caloric restriction (Schwer et al., 2009) in mice.”
From Mitochondrial (Dys)function and Insulin Resistance: From Pathophysiological Molecular Mechanisms to the Impact of Diet (2019) · cites this paper as Schwer et al., 2009
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Cites
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Molecular Nutrition Research—The Modern Way Of Performing Nutritional Science
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“Changes in the acetylation ofmitochondrial proteins with diet appear to vary from tissue to tissue and may be conceptually distinct from the above framework for proteins in the nuclear/cytoplasmic pool (Schwer et al., 2009).”
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“One of the paradoxes of mitochondrial protein acetylation is that not only does a high fat diet produce this phenotype (Hirschey et al., 2011), but calorie restriction also induces mitochondrial protein acetylation (Hebert et al., 2013; Schwer et al., 2009).”
BackgroundTop Down Proteomics of Human Membrane Proteins from Enriched Mitochondrial Fractions
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“In mouse liver, VDAC2 also was found to be acetylated; acetylation of lysine 32 and 75 was documented in [24] and on lysine 121 in [25].”
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“A previous study has noted a change in acetylation status of mitochondrial proteins with CR feeding [42].”
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“In parallel, within mitochondria there is evidence that with changes in acetyl-CoA levels there is concurrent modulation of acetylation levels on a multitude of proteins in response to diverse conditions including fasting, caloric restriction and overload, and following ethanol intoxication [19, 29-32].”
The biology of lysine acetylation integrates transcriptional programming and metabolism
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“Cellular-wide proteomic analyses on protein acetylation revealed a large number of acetylated proteins, mostly enzymes involved in intermediary metabolism in the cytoplasm as well as the mitochondrion [16,23,24].”
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“For example, large-scale mass spectrometry screening pre- and post-CR identified well over 100 reversibly acetylated lysines in 72 mitochondrial proteins from a wide variety of metabolic pathways [11].”
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“This gives rise to the extreme difficulty of identifying modified sites directly from the protein sequences [7], [8], [9].”
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BackgroundGCN5L1 controls renal lipotoxicity through regulating acetylation of fatty acid oxidation enzymes
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“Subsequently, several hundred acetylated proteins were also identified in other studies using either nutritional or acetylase/deacetylase enzymatic manipulations (18, 19).”
BackgroundSIRT3 Weighs Heavily in the Metabolic Balance: A New Role for SIRT3 in Metabolic Syndrome
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“The authors found that protein acetylation was significantly increased in liver mitochondria (despite a moderate increase in SIRT3 protein levels), significantly decreased in brown adipose tissue, but almost unaffected in heart, kidney, and brain (Schwer et al. 2009).”
BackgroundThe gateway to guanine nucleotides: Allosteric regulation of IMP dehydrogenases
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“Indeed, CR increases protein acetylation in the liver mitochondria, but in several other tissues the effect is minimal if any (Schwer et al., 2009).”
BackgroundResultInfluentialTGF-β1 is a regulator of the pyruvate dehydrogenase complex in fibroblasts
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“Multiple mitochondrial proteins are deacetylated upon caloric restriction in a SIRT3-dependent manner (Schwer et al., 2009).”
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“In the liver, mitochondrial proteins undergo nutrient-dependent lysine acetylation and deacetylation [71, 72].”
BackgroundDietary, Metabolic, and Potentially Environmental Modulation of the Lysine Acetylation Machinery
Kim, G.-W., Gocevski, G., Wu, C.-J., & Yang, X. (2010) · International Journal of Cell Biology · doi:10.1155/2010/632739 · Cited by 34
“A proteomicwide survey revealed that among 287 unique acetylated proteins from mouse liver, 165 of them (about 57%) are mitochondrial proteins [117].”
BackgroundHDAC4 Does Not Act as a Protein Deacetylase in the Postnatal Murine Brain In Vivo
Mielcarek, M., Seredenina, T. S., Stokes, M. P., Osborne, G. F., Landles, C., Inuabasi, L., Franklin, S., Silva, J. C., Luthi‐Carter, R., Beaumont, V., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0080849 · Cited by 30
“We used Cell Signalling Technology’s AcetylScan proteomics platform [18-21] to identify and quantify differences in acetylation between WT and Hdac4KO mouse brains.”
MethodSelf-citationPhosphorylation and Acetylation of Acyl-Coa Synthetase- I
Frahm, J. L. (2011) · Journal of Proteomics & Bioinformatics · doi:10.4172/jpb.1000180 · Cited by 30
“7-fold while protein expression of SIRT3 and lysine acetylation of acyl-CoA synthetase medium chain-1 (ACSM1) and ACSS2 increased [25].”
BackgroundMechanisms of transcription factor acetylation and consequences in hearts
Thiagarajan, D., Vedantham, S., Ananthakrishnan, R., Schmidt, A. M., & Ramasamy, R. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.08.011 · Cited by 29
“Proteomic studies and bioinformatic analysis revealed acetylation of metabolic enzymes and transcription factors in various cell types [12, 15-17].”
BackgroundXu, G., Quan, S., Schell, J. R., Gao, Y., Varmazyad, M., Sreenivas, P., Cruz, D., Jiang, H., Pan, M., Han, X., et al. (2024) · Science Advances · doi:10.1126/sciadv.adj5942 · Cited by 30
The role of lysine acetylation in metabolic sensing and proteostasis
Eftekhari, A., Sabir, U., & Kasumov, T. (2025) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2025.108908 · Cited by 30
Shulyakova, N., Sidorova‐Darmos, E., Fong, J., Zhang, G., Mills, L. R., & Eubanks, J. H. (2014) · Brain Research · doi:10.1016/j.brainres.2014.08.066 · Cited by 26
“Sirt3 is one of three mitochondrially-targeted mammalian sirtuins, and its deacetylase activity influences the acetylation state of at least 165 proteins within the mitochondrial proteome (Schwer et al., 2009, Lombard et al., 2007; Hebert et al., 2013).”
BackgroundMitochondrial Acetylation and Genetic Models of Parkinson's Disease
Auburger, G. W. J., Gispert, S., & Jendrach, M. (2014) · Progress in molecular biology and translational science · doi:10.1016/b978-0-12-394625-6.00006-4 · Cited by 27
Sirtuins in Multiple Sclerosis: The crossroad of neurodegeneration, autoimmunity and metabolism
Foolad, F., Khodagholi, F., & Javan, M. (2019) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2019.06.004 · Cited by 26
Dhillon, R. S., Qin, Y., van Ginkel, P. R., Fu, V. X., Vann, J. M., Lawton, A. J., Green, C. L., Manchado-Gobatto, F. D. B., Gobatto, C. A., Lamming, D. W., et al. (2022) · Aging Cell · doi:10.1111/acel.13721 · Cited by 25
Pérez, H., Finocchietto, P. V., Alippe, Y., Rebagliati, I., Elguero, M. E., Villalba, N., Poderoso, J. J., & Carreras, M. C. (2018) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2018/8561892 · Cited by 23
“Recent studies have shown that the acetylation levels of mouse mitochondrial proteins are modulated in fasting conditions or during caloric restriction [20].”
BackgroundMitochondrial sirtuins – a new therapeutic target for repair and protection in multiple sclerosis
Rice, C. M., Sun, M., Kemp, K. C., Gray, E., Wilkins, A., & Scolding, N. J. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08150.x · Cited by 25
“SIRT3 can influence the Krebs cycle both directly (Schlicker et al., 2008; Cimen et al., 2010) and indirectly (Hallows et al., 2006; Lombard et al., 2007; Schlicker et al., 2008; Schwer et al., 2009).”
BackgroundPerumal, N., Straßburger, L., Herzog, D. P., Müller, M. B., Pfeiffer, N., Grus, F. H., & Manicam, C. (2020) · Redox Biology · doi:10.1016/j.redox.2020.101597 · Cited by 23
Acceleration of adipogenic differentiation via acetylation of malate dehydrogenase 2
Kim, E. Y., Han, B., Kim, W. K., Lee, S. C., & Bae, K. (2013) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2013.10.016 · Cited by 23
c-MYC responds to glucose deprivation in a cell-type-dependent manner
Wu, S., Yin, X., Fang, X., Zheng, J., Li, L., Liu, X., & Chu, L. (2015) · Cell Death Discovery · doi:10.1038/cddiscovery.2015.57 · Cited by 23
Histone H3 N-terminal mimicry drives a novel network of methyl-effector interactions
Chen, J., Horton, J. R., Sagum, C. A., Zhou, J., Cheng, X., & Bedford, M. T. (2021) · Biochemical Journal · doi:10.1042/bcj20210203 · Cited by 24
Autophagy in Ischemic Livers: A Critical Role of Sirtuin 1/Mitofusin 2 Axis in Autophagy Induction
Chun, S. K., Go, K. L., Yang, M., Zendejas, I. R., Behrns, K. E., & Js, K. (2016) · Toxicological Research · doi:10.5487/tr.2016.32.1.035 · Cited by 19
“The mitochondria-localized SIRT3, for instance, modulates intramitochondrial metabolic activities and ROS formation by deacetylating the NDUFA9 subunit of Complex 1 in the mitochondrial electron transfer chain (108-112).”
BackgroundMetabolomics and mitochondrial dysfunction in cardiometabolic disease
Shastry, A., & Dunham‐Snary, K. J. (2023) · Life Sciences · doi:10.1016/j.lfs.2023.122137 · Cited by 23
Post-translational modifications of mitochondrial outer membrane proteins
Kerner, J., Lee, K., & Hoppel, C. L. (2010) · Free Radical Research · doi:10.3109/10715762.2010.515218 · Cited by 20
“[57] reported that in liver of adult C57BL/6 mice kynurenine-3-monooxygenase Table II.”
BackgroundEdgett, B. A., Hughes, M. C., Matusiak, J. B. L., Perry, C. G. R., Simpson, C. A., & Gurd, B. J. (2016) · Experimental Physiology · doi:10.1113/ep085744 · Cited by 19
VDACs Post-Translational Modifications Discovery by Mass Spectrometry: Impact on Their Hub Function
Pittalà, M. G. G., Nibali, S. C., Reina, S., Cunsolo, V., Francesco, A. D., Pinto, V. D., Messina, A. A., Foti, S., & Saletti, R. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312833 · Cited by 19
“In addition, lysines 63 and 109 were identified acetylated in mouse liver, with no differences between fed and calorie-restricted animals [80].”
BackgroundChen, I., Chiang, W., Chen, P., & Chiang, H. (2013) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24667 · Cited by 19
“Interestingly, four of the eleven proteins that make up complex III in mitochondria were shown to be acetylated [Schwer et al., 2009].”
BackgroundJiang, W., Zhu, Z., & Thompson, H. J. (2012) · Carcinogenesis · doi:10.1093/carcin/bgs350 · Cited by 18
“The induction of SIRT1 implies that intracellular energy sensing is perturbed even at the modest level of LEA that was investigated (37,38).”
BackgroundAn integrated perspective and functional impact of the mitochondrial acetylome
Amado, F. M. L., Barros, A. S., Azevedo, A. L., Vitorino, R. M. P., & Ferreira, R. M. (2014) · Expert Review of Proteomics · doi:10.1586/14789450.2014.899470 · Cited by 17
“Despite the recognized biological relevance of protein acetylation, few studies have performed large-scale surveys of mitochondria acetylome [12,13,15,16,22,23].”
BackgroundPei, J., Yuan, Y., Tian, D., Huang, F., Zhang, C., Wang, C., Zhou, M., Chen, H., Fu, Z., & Zhao, L. (2021) · Journal of Virology · doi:10.1128/jvi.01942-21 · Cited by 16
“be caused by a nonenzymatic reaction due to metabolites, such as acetyl-CoA (34).”
BackgroundKawakami, K., Nakamura, A., & Goto, S. (2012) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2012.01.120 · Cited by 15
“reported that DR increased protein acetylation in mouse liver mitochondria [38].”
BackgroundShinmura, K. (2013) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2012.08.006 · Cited by 15
“Three members of the sirtuin family target mitochondria, and increasing evidence demonstrates that mitochondrial sirtuins play an important role in modifying mitochondrial metabolism and function by deacetylating target mitochondrial proteins in various organs under metabolic stress (Haigis and Sinclair 2010; Houtkoop…”
BackgroundMass Spectrometry-Based Detection of Protein Acetylation
Li, Y., Silva, J. C., Skinner, M. E., & Lombard, D. B. (2013) · Methods in molecular biology · doi:10.1007/978-1-62703-637-5_6 · Cited by 14
“Alternatively, tissues may be used (1) (see Note 2).”
BackgroundSelf-citationTemporal analysis of protein lysine acetylation during adipocyte differentiation
Xu, Z., Ande, S. R., & Mishra, S. (2012) · Adipocyte · doi:10.4161/adip.21916 · Cited by 14
“To further confirm this, membranes were reprobed with antiprohibitin antibody as prohibitin is known to undergo posttranslational modification by acetylation and phosphorylation as well as upregulated during adipocyte differentiation.(15,24,25) Indeed a series of prohibitin spots were identified matching acetylation s…”
BackgroundCorrection: Quantitating the Specificity and Selectivity of Gcn5-Mediated Acetylation of Histone H3
Kuo, Y., & Andrews, A. J. (2013) · PLoS ONE · doi:10.1371/annotation/b2bf9c2e-90a9-4228-9b38-2f1bc977a437 · Cited by 14
Jia, R., Chen, S., Wang, L., Zhang, J., Qu, B., Qiao, J., Meng, X., Yu, S., Liu, X., Xu, B., et al. (2025) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2025.101377 · Cited by 15
“In identifying the role of protein acetylation in calorie restriction, Schwer et al. found that CYP4V3 was acetylated at the Lys376 site in the mouse liver, which may have important consequences for the activity, complex formation, turnover, or other functions of CYP4V3 (Schwer et al., 2009).”
Elmansi, A. M., & Miller, R. A. (2023) · GeroScience · doi:10.1007/s11357-023-00849-8 · Cited by 13
“There are also multiple reports that post-translational modifications of those enzymes (e.g., SIRT3-mediated hyperacety-lation of OXPHOS and FAO enzymes) contribute to their modulated activity and stability [8, 73–75].”
BackgroundTaghizadeh, N., Mohammadi, S., Yousefi, Z., Golpour, P., Taheri, A., Maleki, M. H., Nourbakhsh, M., Nourbakhsh, M., & Azar, M. R. (2023) · PLoS ONE · doi:10.1371/journal.pone.0293217 · Cited by 14
“Schwer and colleagues conducted a comprehensive analysis of acetylation of mitochondrial enzymes in mice models of calorie restriction and found that calorie restriction significantly reduced the acetylation of mitochondrial proteins, specifically in brown adipose tissue [27].”
BackgroundLatorre‐Muro, P., Baeza, J., Hurtado‐Guerrero, R., Hicks, T., Delso, I., Hernández-Ruiz, C., Velázquez‐Campoy, A., Lawton, A. J., Angulo, J., Denu, J. M., et al. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.ra120.015103 · Cited by 13
Sirtuins, Healthspan, and Longevity in Mammals
Giblin, W., & Lombard, D. B. (2015) · Elsevier eBooks · doi:10.1016/b978-0-12-411596-5.00003-4 · Cited by 12
Self-citationAging-induced MCPH1 translocation activates necroptosis and impairs hematopoietic stem cell function
He, H., Wang, Y., Tang, B., Dong, Q., Wu, C., Sun, W., & Wang, J. (2024) · Nature Aging · doi:10.1038/s43587-024-00609-z · Cited by 11
“Prior research has demonstrated that calorie restriction induces changes in lysine acetylation of mitochondrial proteins 51 .”
Anjo, S. I., Figueiredo, F., Fernandes, R., Manadas, B. J., & Oliveira, M. T. D. S. (2017) · Journal of Proteomics · doi:10.1016/j.jprot.2017.03.021 · Cited by 11
Zhang, L., Liu, T., Hu, C., Zhang, X., Zhang, Q., & Shi, K. (2021) · BMC Genomics · doi:10.1186/s12864-021-07950-2 · Cited by 11
Aleshina, Y. A., & Aleshin, V. A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084341 · Cited by 10
Metadata
- Authors
- Schwer, B., Eckersdorff, M., Li, Y., Silva, J. C., Fermin, D., Kurtev, M. V., Giallourakis, C., Comb, M. J., Alt, F. W., & Lombard, D. B.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Michigan (US)
- Cell Signaling Technology (United States) (US)
- Harvard University (US)
- Corresponding author
- Alt, Frederick W.
- Lombard, David B.
- ORCID
- Venue
- Aging Cell
- Publisher
- Wiley
- Published
- 2009-09-24
- Volume
- 8
- Issue
- 5
- Pages
- 604-606
- ISSN
- 1474-9718 (ISSN-L)
- 1474-9726
- PMC
- PMC2752488
- OpenAlex
- W2095235693
- Cited by
- 259
- References
- 16
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 6 · 2023: 4 · 2022: 10 · 2021: 15 · 2020: 8 · 2019: 15 · 2018: 8 · 2017: 11 · 2016: 24 · 2015: 13 · 2014: 26 · 2013: 37 · 2012: 32
- FWCI
- 7.48
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Aging Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Deep Blue (University of Michigan) (acceptedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute on Aging (AG022325, K08AG022325)
- National Institute of General Medical Sciences (T32GM007753)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Mitochondrial Function and Pathology
- Health Sciences › Medicine › Geriatrics and Gerontology › Sirtuins and Resveratrol in Medicine
- Keywords
- caloric restriction, mitochondrial protein acetylation, lysine acetylation, mitochondrial adaptation, longevity, lifespan extension, tissue-specific effects, metabolic pathways, aging
- MeSH terms
- Acetylation, Animals, Saccharomycetales, Humans, Life Expectancy, Longevity, Mammals, Mice, Inbred C57BL, Mitochondria, Mitochondria, Liver, Proteins, Caloric Restriction, Mice
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