Metabolic networks of longevity
Open accessAbstract
Molecular and cellular networks implicated in aging depend on a multitude of proteins that collectively mount adaptive and contingent metabolic responses to environmental challenges. Here, we discuss the intimate links between metabolic regulation and longevity and outline new approaches for analyzing and manipulating such links to promote human health span.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Natural variation in gene expression that is present in the human population is also recapitulated in these models and therefore more honestly reflect genotype-phenotype associations than artificial loss-of-function situations, such as gene knockouts or knock-down experiments.
“The natural variation in gene expression that is present in the human population is also recapitulated in these models and therefore more honestly reflect genotype-phenotype associations than artificial loss-of-function situations, such as gene knockouts or knock-down experiments (82).”
From Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease (2018) · cites this paper as [82]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Resveratrol improves health and survival of mice on a high-calorie diet
Baur, J. A., Pearson, K. J., Price, N. L., Jamieson, H. A., Lerin, C., Kalra, A., Prabhu, V. V., Allard, J. S., Lopez-Lluch, G., Lewis, K., et al. (2006) · Nature · doi:10.1038/nature05354 · Cited by 4,290 · see citing works
Lagouge, M., Argmann, C., Gerhart-Hines, Z., Meziane, H., Lerin, C., Daussin, F., Messadeq, N., Milne, J., Lambert, P., Elliott, P., et al. (2006) · Cell · doi:10.1016/j.cell.2006.11.013 · Cited by 4,057 · see citing works
Self-citationRapamycin fed late in life extends lifespan in genetically heterogeneous mice
Harrison, D. E., Strong, R., Sharp, Z. D., Nelson, J. F., Astle, C. M., Flurkey, K., Nadon, N. L., Wilkinson, J. E., Frenkel, K., Carter, C. S., et al. (2009) · Nature · doi:10.1038/nature08221 · Cited by 3,766 · see citing works
AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity
Cantó, C., Gerhart-Hines, Z., Feige, J. N., Lagouge, M., Noriega, L., Milne, J. C., Elliott, P. J., Puigserver, P., & Auwerx, J. (2009) · Nature · doi:10.1038/nature07813 · Cited by 3,300 · see citing works
Extending Healthy Life Span—From Yeast to Humans
Fontana, L., Partridge, L., & Longo, V. D. (2010) · Science · doi:10.1126/science.1172539 · Cited by 3,023 · see citing works
Kenyon, C. J. (2010) · Nature · doi:10.1038/nature08980 · Cited by 2,739 · see citing works
Caloric Restriction Delays Disease Onset and Mortality in Rhesus Monkeys
Colman, R. J., Anderson, R. M., Johnson, S. C., Kastman, E. K., Kosmatka, K. J., Beasley, T. M., Allison, D. B., Cruzen, C., Simmons, H. A., Kemnitz, J. W., et al. (2009) · Science · doi:10.1126/science.1173635 · Cited by 2,277 · see citing works
Induction of autophagy by spermidine promotes longevity
Eisenberg, T., Knauer, H., Schauer, A., Büttner, S., Ruckenstuhl, C., Carmona-Gutierrez, D., Ring, J., Schroeder, S., Magnes, C., Antonacci, L., et al. (2009) · Nature Cell Biology · doi:10.1038/ncb1975 · Cited by 1,680 · see citing works
Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity
Um, S. H., Frigerio, F., Watanabe, M., Picard, F., Joaquin, M., Sticker, M., Fumagalli, S., Allegrini, P. R., Kozma, S. C., Auwerx, J., et al. (2004) · Nature · doi:10.1038/nature02866 · Cited by 1,677 · see citing works
Rates of Behavior and Aging Specified by Mitochondrial Function During Development
Dillin, A., Hsu, A.-L., Arantes-Oliveira, N., Lehrer-Graiwer, J., Hsin, H., Fraser, A. G., Kamath, R. S., Ahringer, J., & Kenyon, C. (2002) · Science · doi:10.1126/science.1077780 · Cited by 1,121 · see citing works
Ribosomal Protein S6 Kinase 1 Signaling Regulates Mammalian Life Span
Selman, C., Tullet, J. M. A., Wieser, D., Irvine, E., Lingard, S. J., Choudhury, A. I., Claret, M., Al-Qassab, H., Carmignac, D., Ramadani, F., et al. (2009) · Science · doi:10.1126/science.1177221 · Cited by 1,120 · see citing works
Mechanisms of Life Span Extension by Rapamycin in the Fruit Fly Drosophila Melanogaster
Bjedov, I., Toivonen, J. M., Kerr, F., Slack, C., Jacobson, J., Foley, A., & Partridge, L. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2009.11.010 · Cited by 1,057 · see citing works
Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration
Lin, S.-J., Kaeberlein, M., Andalis, A. A., Sturtz, L. A., Defossez, P.-A., Culotta, V. C., Fink, G. R., & Guarente, L. (2002) · Nature · doi:10.1038/nature00829 · Cited by 1,057 · see citing works
A systematic RNAi screen identifies a critical role for mitochondria in C. elegans longevity
Lee, S. S., Lee, R. Y. N., Fraser, A. G., Kamath, R. S., Ahringer, J., & Ruvkun, G. (2003) · Nature Genetics · doi:10.1038/ng1056 · Cited by 969 · see citing works
Cantó, C., Jiang, L. Q., Deshmukh, A. S., Mataki, C., Coste, A., Lagouge, M., Zierath, J. R., & Auwerx, J. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.02.006 · Cited by 921 · see citing works
SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1
Pacholec, M., Bleasdale, J. E., Chrunyk, B., Cunningham, D., Flynn, D., Garofalo, R. S., Griffith, D., Griffor, M., Loulakis, P., Pabst, B., et al. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.088682 · Cited by 915 · see citing works
The secret life of NAD+: an old metabolite controlling new metabolic signaling pathways
Houtkooper, R. H., Cantó, C., Wanders, R. J., & Auwerx, J. (2010) · Endocrine Reviews · doi:10.1210/er.2009-0026 · Cited by 899 · see citing works
Amino-acid imbalance explains extension of lifespan by dietary restriction in Drosophila
Grandison, R. C., Piper, M. D. W., & Partridge, L. (2009) · Nature · doi:10.1038/nature08619 · Cited by 777 · see citing works
Miller, R. A., Buehner, G., Chang, Y., Harper, J. M., Sigler, R. E., & Smith‐Wheelock, M. (2005) · Aging Cell · doi:10.1111/j.1474-9726.2005.00152.x · Cited by 734 · see citing works
AMP-activated protein kinase-deficient mice are resistant to the metabolic effects of resveratrol
Um, J.-H., Park, S.-J., Kang, H., Yang, S., Foretz, M., McBurney, M. W., Kim, M. K., Viollet, B., & Chung, J. H. (2010) · Diabetes · doi:10.2337/db09-0482 · Cited by 647 · see citing works
Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer
Herranz, D., Muñoz-Martin, M., Cañamero, M., Mulero, F., Martinez-Pastor, B., Fernandez-Capetillo, O., & Serrano, M. (2010) · Nature Communications · doi:10.1038/ncomms1001 · Cited by 612 · see citing works
4E-BP Extends Lifespan upon Dietary Restriction by Enhancing Mitochondrial Activity in Drosophila
Zid, B. M., Rogers, A. N., Katewa, S. D., Vargas, M. A., Kolipinski, M., Lu, T. A., Benzer, S., & Kapahi, P. (2009) · Cell · doi:10.1016/j.cell.2009.07.034 · Cited by 541 · see citing works
PHA-4/Foxa mediates diet-restriction-induced longevity of C. elegans
Panowski, S. H., Wolff, S., Aguilaniu, H., Durieux, J., & Dillin, A. G. (2007) · Nature · doi:10.1038/nature05837 · Cited by 538 · see citing works
Dissection of genetically complex traits with extremely large pools of yeast segregants
Ehrenreich, I. M., Torabi, N., Jia, Y., Kent, J. D., Martis, S., Shapiro, J. A., Gresham, D., Caudy, A. A., & Kruglyak, L. (2010) · Nature · doi:10.1038/nature08923 · Cited by 438 · see citing works
Resveratrol is not a direct activator of SIRT1 enzyme activity
Beher, D., Wu, J., Cumine, S., Kim, K. W., Lu, S., Atangan, L., & Wang, M. (2009) · Chemical Biology & Drug Design · doi:10.1111/j.1747-0285.2009.00901.x · Cited by 426 · see citing works
Caloric restriction, SIRT1 and longevity
Cantó, C., & Auwerx, J. (2009) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2009.03.008 · Cited by 395 · see citing works
Self-citationBellizzi, D., Rose, G., Cavalcante, P., Covello, G., Dato, S., De Rango, F., Greco, V., Maggiolini, M., Feraco, E., Mari, V., et al. (2005) · Genomics · doi:10.1016/j.ygeno.2004.11.003 · Cited by 367 · see citing works
Endocrine regulation of ageing
Russell, S. J., & Kahn, C. R. (2007) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2234 · Cited by 356 · see citing works
Metformin slows down aging and extends life span of female SHR mice
Anisimov, V. N., Berstein, L. M., Egormin, P. A., Piskunova, T. S., Popovich, I. G., Zabezhinski, M. A., Tyndyk, M. L., Yurova, M. V., Kovalenko, I. G., Poroshina, T. E., et al. (2008) · Cell Cycle · doi:10.4161/cc.7.17.6625 · Cited by 348 · see citing works
Stanfel, M. N., Shamieh, L. S., Kaeberlein, M. R., & Kennedy, B. K. (2009) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2009.06.007 · Cited by 339 · see citing works
The Human Ageing Genomic Resources: online databases and tools for biogerontologists
de Magalhães, J. P., Budovsky, A., Lehmann, G., Cósta, J., Li, Y., Fraifeld, V. E., & Church, G. M. (2008) · Aging Cell · doi:10.1111/j.1474-9726.2008.00442.x · Cited by 189 · see citing works
A modular network model of aging
Xue, H., Xian, B., Dong, D., Xia, K., Zhu, S., Zhang, Z., Hou, L., Zhang, Q., Zhang, Y., & Han, J. J. (2007) · Molecular Systems Biology · doi:10.1038/msb4100189 · Cited by 170 · see citing works
Murine chromosomal regions correlated with longevity.
Gelman, R. S., Watson, A., Bronson, R. T., & Yunis, E. J. (1988) · Genetics · doi:10.1093/genetics/118.4.693 · Cited by 156 · see citing works
SIRT1 mRNA expression may be associated with energy expenditure and insulin sensitivity
Rutanen, J., Yaluri, N., Modi, S., Pihlajamäki, J., Vänttinen, M., Itkonen, P., Kainulainen, S., Yamamoto, H., Lagouge, M., Sinclair, D. A., et al. (2010) · Diabetes · doi:10.2337/db09-1191 · Cited by 104 · see citing works
de Haan, G., & van Zant, G. (1999) · The FASEB Journal · doi:10.1096/fasebj.13.6.707 · Cited by 87 · see citing works
Pparγ2 Is a Key Driver of Longevity in the Mouse
Argmann, C., Dobrin, R., Heikkinen, S., Auburtin, A., Pouilly, L., Cock, T., Koutníková, H., Zhu, J., Schadt, E. E., & Auwerx, J. H. (2009) · PLoS Genetics · doi:10.1371/journal.pgen.1000752 · Cited by 87 · see citing works
Lifespan, QTLs, age-specificity, and pleiotropy in Drosophila
Curtsinger, J. W., & Khazaeli, A. A. (2002) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(01)00345-1 · Cited by 76 · see citing works
The Pro12Ala PPARγ2 Variant Determines Metabolism at the Gene-Environment Interface
Heikkinen, S., Argmann, C., Feige, J. N., Koutníková, H., Champy, M., Dali‐Youcef, N., Schadt, E. E., Laakso, M., & Auwerx, J. H. (2009) · Cell Metabolism · doi:10.1016/j.cmet.2008.11.007 · Cited by 72 · see citing works
Modulation of Longevity by Environmental Sensing
Libert, S., & Pletcher, S. D. (2007) · Cell · doi:10.1016/j.cell.2007.12.002 · Cited by 56 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
López-Otín, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013) · Cell · doi:10.1016/j.cell.2013.05.039 · Cited by 14,982 · see citing works
Sirtuins as regulators of metabolism and healthspan
Houtkooper, R. H., Pirinen, E., & Auwerx, J. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3293 · Cited by 2,008 · see citing works
Self-citationCantó, C., Menzies, K. J., & Auwerx, J. (2015) · Cell Metabolism · doi:10.1016/j.cmet.2015.05.023 · Cited by 1,648 · see citing works
Self-citationMouchiroud, L., Houtkooper, R. H., Moullan, N., Katsyuba, E., Ryu, D., Cantó, C., Mottis, A., Jo, Y.-S., Viswanathan, M., Schoonjans, K., et al. (2013) · Cell · doi:10.1016/j.cell.2013.06.016 · Cited by 1,210 · see citing works
Mitonuclear protein imbalance as a conserved longevity mechanism
Houtkooper, R. H., Mouchiroud, L., Ryu, D., Moullan, N., Katsyuba, E., Knott, G., Williams, R. W., & Auwerx, J. (2013) · Nature · doi:10.1038/nature12188 · Cited by 1,035 · see citing works
Quirós, P. M., Prado, M. A., Zamboni, N., D’Amico, D., Williams, R. W., Finley, D., Gygi, S. P., & Auwerx, J. (2017) · Journal of Cell Biology · doi:10.1083/jcb.201702058 · Cited by 832 · see citing works
Metabolic Flexibility as an Adaptation to Energy Resources and Requirements in Health and Disease
Smith, R. L., Soeters, M. R., Wüst, R. C. I., & Houtkooper, R. H. (2018) · Endocrine Reviews · doi:10.1210/er.2017-00211 · Cited by 787 · see citing works
The metabolic footprint of aging in mice
Houtkooper, R. H., Argmann, C., Houten, S. M., Cantó, C., Jeninga, E. H., Andreux, P. A., Thomas, C., Doenlen, R., Schoonjans, K., & Auwerx, J. (2011) · Scientific Reports · doi:10.1038/srep00134 · Cited by 528 · see citing works
A Ketogenic Diet Extends Longevity and Healthspan in Adult Mice
Roberts, M. N., Wallace, M. A., Tomilov, A. A., Zhou, Z., Marcotte, G. R., Tran, D., Perez, G., Gutierrez-Casado, E., Koike, S., Knotts, T. A., et al. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.08.005 · Cited by 514 · see citing works
Molecular and physiological manifestations and measurement of aging in humans
Khan, S. S., Singer, B. D., & Vaughan, D. E. (2017) · Aging Cell · doi:10.1111/acel.12601 · Cited by 530 · see citing works
The ageing epigenome and its rejuvenation
Zhang, W., Qu, J. T., Liu, G., & Belmonte, J. C. I. (2020) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-019-0204-5 · Cited by 472 · see citing works
The bile acid membrane receptor TGR5 as an emerging target in metabolism and inflammation
Pols, T. W. H., Noriega, L. G., Nomura, M., Auwerx, J., & Schoonjans, K. (2011) · Journal of Hepatology · doi:10.1016/j.jhep.2010.12.004 · Cited by 454 · see citing works
Zhu, X., Chen, Z., Shen, W., Huang, G., Sedivy, J. M., Wang, H., & Ju, Z. (2021) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-021-00646-9 · Cited by 410 · see citing works
Pharmacological approaches to restore mitochondrial function
Andreux, P. A., Houtkooper, R. H., & Auwerx, J. (2013) · Nature Reviews Drug Discovery · doi:10.1038/nrd4023 · Cited by 383 · see citing works
Repairing mitochondrial dysfunction in disease
Sorrentino, V., Menzies, K. J., & Auwerx, J. (2018) · Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010716-104908 · Cited by 337 · see citing works
Liu, Y. J., McIntyre, R. L., Janssens, G. E., & Houtkooper, R. H. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111212 · Cited by 334 · see citing works
Yang, K., Neale, G. A. M., Green, D. R., He, W., & Chi, H. (2011) · Nature Immunology · doi:10.1038/ni.2068 · Cited by 294 · see citing works
Cardiovascular effects and molecular targets of resveratrol
Li, H., Xia, N., & Förstermann, U. (2012) · Nitric Oxide · doi:10.1016/j.niox.2011.12.006 · Cited by 294 · see citing works
Calorie Restriction: Is AMPK a Key Sensor and Effector
Cantó, C., & Auwerx, J. (2011) · Physiology · doi:10.1152/physiol.00010.2011 · Cited by 282 · see citing works
Ketogenic diets, mitochondria, and neurological diseases
Gano, L. B., Patel, M., & Rho, J. M. (2014) · Journal of Lipid Research · doi:10.1194/jlr.r048975 · Cited by 279 · see citing works
Histone Methyl Transferases and Demethylases; Can They Link Metabolism and Transcription?
Teperino, R., Schoonjans, K., & Auwerx, J. H. (2010) · Cell Metabolism · doi:10.1016/j.cmet.2010.09.004 · Cited by 270 · see citing works
Regulation of Stem Cell Aging by Metabolism and Epigenetics
Ren, R., Ocampo, A., Liu, G., & Belmonte, J. C. I. (2017) · Cell Metabolism · doi:10.1016/j.cmet.2017.07.019 · Cited by 269 · see citing works
NCoR1 Is a Conserved Physiological Modulator of Muscle Mass and Oxidative Function
Yamamoto, H., Williams, E. G., Mouchiroud, L., Cantó, C., Fan, W., Downes, M., Héligon, C., Barish, G. D., Desvergne, B., Evans, R. M., et al. (2011) · Cell · doi:10.1016/j.cell.2011.10.017 · Cited by 261 · see citing works
Eisenberg, T., Schroeder, S., Andryushkova, A., Pendl, T., Küttner, V., Bhukel, A., Mariño, G., Pietrocola, F., Harger, A., Zimmermann, A., et al. (2014) · Cell Metabolism · doi:10.1016/j.cmet.2014.02.010 · Cited by 256 · see citing works
Reconsidering the Role of Mitochondria in Aging
Gonzalez-Freire, M., de Cabo, R., Bernier, M., Sollott, S. J., Fabbri, E., Navas, P., & Ferrucci, L. (2015) · The Journals of Gerontology Series A: Biological Sciences and Medical Sciences · doi:10.1093/gerona/glv070 · Cited by 244 · see citing works
AMP-activated protein kinase, stress responses and cardiovascular diseases
Wang, S., Song, P., & Zou, M. (2012) · Clinical Science · doi:10.1042/cs20110625 · Cited by 243 · see citing works
Mechanisms of Aging and the Preventive Effects of Resveratrol on Age-Related Diseases
Pyo, I. S., Yun, S., Yoon, Y. E., Choi, J. W., & Lee, S. (2020) · Molecules · doi:10.3390/molecules25204649 · Cited by 213 · see citing works
Inflammation and DNA damage: cause, effect or both
Pezone, A., Olivieri, F., Napoli, M. V., Procopio, A., Avvedimento, E. V., & Gabrielli, A. (2023) · Nature Reviews Rheumatology · doi:10.1038/s41584-022-00905-1 · Cited by 212 · see citing works
NAD <sup>+</sup> metabolism: A therapeutic target for age-related metabolic disease
Mouchiroud, L., Houtkooper, R. H., & Auwerx, J. (2013) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2013.789479 · Cited by 193 · see citing works
“De novo biosynthesis, which starts from the amino acid tryptophan, occurs primarily in the liver and kidney but is considered a minor contributor to the total pool of NAD+ (reviewed in detail in Houtkooper et al., 2010a).”
BackgroundInfluentialThe bile acid membrane receptor TGR5: a valuable metabolic target
Pols, T. W. H., Noriega, L. G., Nomura, M., Auwerx, J., & Schoonjans, K. (2011) · Digestive Diseases · doi:10.1159/000324126 · Cited by 185 · see citing works
Stenesen, D., Suh, J. M., Seo, J. H., Yu, K., Lee, K., Kim, J.-S., Min, K., & Graff, J. M. (2013) · Cell Metabolism · doi:10.1016/j.cmet.2012.12.006 · Cited by 203 · see citing works
The RNA-Binding Protein PUM2 Impairs Mitochondrial Dynamics and Mitophagy During Aging
D’Amico, D., Mottis, A., Potenza, F., Sorrentino, V., Li, H., Romani, M., Lemos, V., Schoonjans, K., Zamboni, N., Knott, G., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2018.11.034 · Cited by 159 · see citing works
Self-citationAging of mesenchymal stem cell: machinery, markers, and strategies of fighting
Al‐Azab, M., Safi, M., Idiiatullina, E., Al‐Shaebi, F., & Zaky, M. Y. (2022) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-022-00366-0 · Cited by 172 · see citing works
The metabolomics of human aging: Advances, challenges, and opportunities
Panyard, D. J., Yu, B., & Snyder, M. P. (2022) · Science Advances · doi:10.1126/sciadv.add6155 · Cited by 155 · see citing works
Metabolomics signature improves the prediction of cardiovascular events in elderly subjects
Rizza, S., Copetti, M., Rossi, C., Cianfarani, M. A., Zucchelli, M., Luzi, A., Pecchioli, C., Porzio, O., Cola, G. D., Urbani, A., et al. (2013) · Atherosclerosis · doi:10.1016/j.atherosclerosis.2013.10.029 · Cited by 158 · see citing works
FOXOs and Sirtuins in Vascular Growth, Maintenance, and Aging
Oellerich, M. F., & Potente, M. (2012) · Circulation Research · doi:10.1161/circresaha.111.246488 · Cited by 157 · see citing works
IL‐10 prevents aging‐associated inflammation and insulin resistance in skeletal muscle
Dağdeviren, S., Jung, D. Y., Friedline, R. H., Noh, H. L., Kim, J. H., Patel, P. R., Tsitsilianos, N., Inashima, K., Tran, D. A., Hu, X., et al. (2016) · The FASEB Journal · doi:10.1096/fj.201600832r · Cited by 151 · see citing works
The different axes of the mammalian mitochondrial unfolded protein response
Münch, C. (2018) · BMC Biology · doi:10.1186/s12915-018-0548-x · Cited by 154 · see citing works
Mitochondrial response to nutrient availability and its role in metabolic disease
Gao, A. W., Cantó, C., & Houtkooper, R. H. (2014) · EMBO Molecular Medicine · doi:10.1002/emmm.201303782 · Cited by 148 · see citing works
Cellular Senescence as the Causal Nexus of Aging
Bhatia‐Dey, N., Kanherkar, R. R., Stair, S. E., Makarev, E., & Csoka, A. B. (2016) · Frontiers in Genetics · doi:10.3389/fgene.2016.00013 · Cited by 147 · see citing works
Lettieri‐Barbato, D., Tatulli, G., Aquilano, K., & Ciriolo, M. R. (2013) · Cell Death and Disease · doi:10.1038/cddis.2013.404 · Cited by 144 · see citing works
Gruber, J., Fong, S., Chen, C.-B., Yoong, S. L., Pastorin, G., Schaffer, S., Cheah, I. K.-M., & Halliwell, B. B. (2012) · Biotechnology Advances · doi:10.1016/j.biotechadv.2012.09.005 · Cited by 138 · see citing works
The mitochondrial unfolded protein response–synchronizing genomes
Jovaisaite, V., & Auwerx, J. (2015) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2014.12.003 · Cited by 131 · see citing works
Jubin, T., Kadam, A. A., Jariwala, M., Bhatt, S., Sutariya, S., Gani, A. R., Gautam, S., & Begum, R. (2016) · Cell Proliferation · doi:10.1111/cpr.12268 · Cited by 130 · see citing works
Cellular Respiration: The Nexus of Stress, Condition, and Ornamentation
Hill, G. E. (2014) · Integrative and Comparative Biology · doi:10.1093/icb/icu029 · Cited by 127 · see citing works
LKB1 and AMPK regulate synaptic remodeling in old age
Samuel, M. A., Voinescu, P. E., Lilley, B. N., de Cabo, R., Foretz, M., Viollet, B., Pawlyk, B., Sandberg, M. A., Vavvas, D. G., & Sanes, J. R. (2014) · Nature Neuroscience · doi:10.1038/nn.3772 · Cited by 114 · see citing works
Deng, J., Wang, P., Chen, X., Cheng, H., Liu, J., Fushimi, K., Zhu, L., & Wu, J. Y. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1806655115 · Cited by 119 · see citing works
From molecular promise to preclinical results: HDAC inhibitors in the race for healthy aging drugs
McIntyre, R. L., Daniels, E. G., Molenaars, M., Houtkooper, R. H., & Janssens, G. E. (2019) · EMBO Molecular Medicine · doi:10.15252/emmm.201809854 · Cited by 115 · see citing works
Cytosolic Proteostasis Networks of the Mitochondrial Stress Response
D'Amico, D. F., Sorrentino, V., & Auwerx, J. H. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.05.002 · Cited by 106 · see citing works
Exploring the therapeutic space around NAD+
Houtkooper, R. H., & Auwerx, J. H. (2012) · The Journal of Cell Biology · doi:10.1083/jcb.201207019 · Cited by 109 · see citing works
Hypothalamic microinflammation: a common basis of metabolic syndrome and aging
Tang, Y., Purkayastha, S., & Cai, D. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.10.002 · Cited by 109 · see citing works
Regulation of Glucose Metabolism by NAD+ and ADP-Ribosylation
Hopp, A.-K., Grüter, P., & Hottiger, M. O. (2019) · Cells · doi:10.3390/cells8080890 · Cited by 107 · see citing works
Mitochondrial function is impaired in the skeletal muscle of pre-frail elderly
Andreux, P. A., van Diemen, M. P. J., Heezen, M. R., Auwerx, J. H., Rinsch, C., Groeneveld, G. J., & Singh, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-26944-x · Cited by 108 · see citing works
Integrating the Hallmarks of Aging Throughout the Tree of Life: A Focus on Mitochondrial Dysfunction
van der Rijt, S., Molenaars, M., McIntyre, R. L., Janssens, G. E., & Houtkooper, R. H. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.594416 · Cited by 97 · see citing works
Emerging role of aging in the progression of NAFLD to HCC
He, Y., Su, Y., Duan, C., Wang, S., He, W. G., Zhang, Y., An, X., & He, M. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101833 · Cited by 98 · see citing works
Orexin Restores Aging-Related Brown Adipose Tissue Dysfunction in Male Mice
Sellayah, D., & Sikder, D. S. (2013) · Endocrinology · doi:10.1210/en.2013-1629 · Cited by 92 · see citing works
Redmann, M., Darley-Usmar, V. M., & Zhang, J. (2016) · Aging and Disease · doi:10.14336/ad.2015.0820 · Cited by 92 · see citing works
Proteomics and metabolomics in ageing research: from biomarkers to systems biology
Hoffman, J. M., Lyu, Y., Pletcher, S. D., & Promislow, D. (2017) · Essays in Biochemistry · doi:10.1042/ebc20160083 · Cited by 90 · see citing works
Aging Biomarkers: From Functional Tests to Multi‐Omics Approaches
Kudryashova, K. S., Burka, K., Kulaga, A. Y., Vorobyeva, N. S., & Kennedy, B. K. (2020) · PROTEOMICS · doi:10.1002/pmic.201900408 · Cited by 86 · see citing works
Glycine promotes longevity in Caenorhabditis elegans in a methionine cycle-dependent fashion
Liu, Y. J., Janssens, G. E., McIntyre, R. L., Molenaars, M., Kamble, R., Gao, A. W., Jongejan, A., van Weeghel, M., MacInnes, A. W., & Houtkooper, R. H. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1007633 · Cited by 80 · see citing works
The controversial links among calorie restriction, SIRT1, and resveratrol
Hu, Y., Liu, J., Wang, J., & Liu, Q. (2011) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2011.04.034 · Cited by 79 · see citing works
Identification of key pathways and metabolic fingerprints of longevity in C. elegans
Gao, A. W., Smith, R. L., van Weeghel, M., Kamble, R., Janssens, G. E., & Houtkooper, R. H. (2018) · Experimental Gerontology · doi:10.1016/j.exger.2018.10.003 · Cited by 80 · see citing works
Tannous, C., Booz, G. W., Altara, R., Muhieddine, D. H., Mericskay, M., Refaat, M. M., & Zouein, F. A. (2020) · Acta Physiologica · doi:10.1111/apha.13551 · Cited by 79 · see citing works
Gao, A. W., Chatzispyrou, I. A., Kamble, R., Liu, Y. J., Herzog, K., Smith, R. L., van Lenthe, H., Vervaart, M. A. T., van Cruchten, A., Luyf, A. C., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-02539-w · Cited by 77 · see citing works
Kuehne, A., Hildebrand, J., Soehle, J., Wenck, H., Terstegen, L., Gallinat, S., Knott, A., Winnefeld, M., & Zamboni, N. (2017) · BMC Genomics · doi:10.1186/s12864-017-3547-3 · Cited by 78 · see citing works
Cau, P., Navarro, C. L., Harhouri, K., Roll, P., Sigaudy, S., Kaspi, É., Perrin, S., Sandre‐Giovannoli, A. D., & Lévy, N. (2014) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2014.03.021 · Cited by 75 · see citing works
Network medicine, multimorbidity and the lung in the elderly
Faner, R., Cruz, T., López-Giraldo, A., & Agustí, A. G. N. (2014) · European Respiratory Journal · doi:10.1183/09031936.00078714 · Cited by 73 · see citing works
Park, J., Glass, Z., Sayed, K., Michurina, T. V., Lazutkin, A. A., Mineyeva, O. A., Velmeshev, D., Ward, W. F., Richardson, A. G., & Enikolopov, G. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12249 · Cited by 71 · see citing works
NAD+ regulates nucleotide metabolism and genomic DNA replication
Munk, S. H. N., Merchut‐Maya, J. M., Adelantado-Rubio, A., Hall, A., Pappas, G. D., Milletti, G., Lee, M., Johnsen, L. G., Guldberg, P., Bártek, J., et al. (2023) · Nature Cell Biology · doi:10.1038/s41556-023-01280-z · Cited by 71 · see citing works
van Beek, H., Kirkwood, T. B. L., & Bassingthwaighte, J. B. (2016) · Interface Focus · doi:10.1098/rsfs.2015.0079 · Cited by 68 · see citing works
Pharmaceutical and nutraceutical activation of FOXO3 for healthy longevity
McIntyre, R. L., Liu, Y. J., Hu, I. M., Morris, B. J., Willcox, B. J., Donlon, T. A., Houtkooper, R. H., & Janssens, G. E. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101621 · Cited by 64 · see citing works
MicroRNAs and the metabolic hallmarks of aging
Victoria, B., López, Y. O. N., & Masternak, M. M. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.12.021 · Cited by 63 · see citing works
Antagonistic functions of LMNA isoforms in energy expenditure and lifespan
López‐Mejía, I. C., de Toledo, M., Chavey, C., Lapasset, L., Cavelier, P., Herrera, C. L., Chébli, K., Fort, P., Béranger, G. E., Fajas, L., et al. (2014) · EMBO Reports · doi:10.1002/embr.201338126 · Cited by 59 · see citing works
Metabolomics and lipidomics in Caenorhabditis elegans using a single-sample preparation
Molenaars, M., Schomakers, B. V., Elfrink, H. L., Gao, A. W., Vervaart, M. A. T., Pras‐Raves, M. L., Luyf, A. C. M., Smith, R. L., Sterken, M. G., Kammenga, J. E., et al. (2021) · Disease Models & Mechanisms · doi:10.1242/dmm.047746 · Cited by 58 · see citing works
Catic, A. (2018) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2017.12.003 · Cited by 58 · see citing works
Roles of SIRT1 in granulosa cell apoptosis during the process of follicular atresia in porcine ovary
Zhao, F., Zhao, W., Ren, S., Fu, Y., Fang, X., Wang, X., & Li, B. (2014) · Animal Reproduction Science · doi:10.1016/j.anireprosci.2014.10.002 · Cited by 57 · see citing works
Kumar, V., Asokan, A. K., Kshemada, K., Ajith, K. G. S., Raj, B., Deora, N., Sanjay, G., Jaleel, A., Muraleedharan, T. S., Anandan, E. M., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-09225-x · Cited by 56 · see citing works
Galow, A.-M., & Peleg, S. (2022) · Cells · doi:10.3390/cells11030468 · Cited by 58 · see citing works
The effect of dichloroacetate on health- and lifespan in C. elegans
Schaffer, S., Gruber, J., Ng, L. C., Fong, S., Wong, Y. T., Tang, S. Y., & Halliwell, B. B. (2010) · Biogerontology · doi:10.1007/s10522-010-9310-7 · Cited by 54 · see citing works
Role of PARP-1 in mitochondrial homeostasis
Kadam, A. A., Jubin, T., Roychowdhury, R., & Begum, R. (2020) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2020.129669 · Cited by 55 · see citing works
Oxysterols are potential physiological regulators of ageing
de Médina, P., Silvente‐Poirot, S., & Poirot, M. (2022) · Ageing Research Reviews · doi:10.1016/j.arr.2022.101615 · Cited by 51 · see citing works
Molecular pathways of arterial aging
Paneni, F., Costantino, S., & Cosentino, F. (2014) · Clinical Science · doi:10.1042/cs20140302 · Cited by 52 · see citing works
Breitenbach, M., Laun, P., & Jazwinski, S. M. (2011) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-94-007-2561-4 · Cited by 50 · see citing works
Age-related proteostasis and metabolic alterations in Caspase-2-deficient mice
Wilson, C. H., Shalini, S., Filipovska, A., Richman, T. R., Davies, S. K., Martin, S. D., McGee, S. L., Puccini, J., Nikolic, A., Dorstyn, L., et al. (2015) · Cell Death and Disease · doi:10.1038/cddis.2014.567 · Cited by 48 · see citing works
Verburgh, K. (2014) · Aging Cell · doi:10.1111/acel.12284 · Cited by 48 · see citing works
Density dependence in Caenorhabditis larval starvation
Artyukhin, A. B., Schroeder, F. C., & Avery, L. (2013) · Scientific Reports · doi:10.1038/srep02777 · Cited by 47 · see citing works
The potential of PARP inhibitors in targeted cancer therapy and immunotherapy
Hunia, J., Gawalski, K., Szredzka, A., Suskiewicz, M. J., & Nowis, D. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.1073797 · Cited by 44 · see citing works
Icariin, a natural flavonol glycoside, extends healthspan in mice
Zhang, S., Cai, W., Huang, J., Wu, B., Xia, S.-J., Chen, X., Zhang, X.-M., & Shen, Z.-Y. (2015) · Experimental Gerontology · doi:10.1016/j.exger.2015.06.020 · Cited by 43 · see citing works
Methionine transsulfuration pathway is upregulated in long-lived humans
Mota-Martorell, N., Jové, M., Borrás, C., Berdún, R., Obis, È., Sol, J., Cabré, R., Pradas, I., Galo-Licona, J. D., Puig, J., et al. (2021) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2020.11.026 · Cited by 43 · see citing works
Germain, D. (2016) · Advances in cancer research · doi:10.1016/bs.acr.2016.01.004 · Cited by 37 · see citing works
Targeting miRNAs by polyphenols: Novel therapeutic strategy for aging
Majidinia, M., Karimian, A., Alemi, F., Yousefi, B., & Safa, A. (2019) · Biochemical Pharmacology · doi:10.1016/j.bcp.2019.113688 · Cited by 37 · see citing works
FAHFA footprint in the visceral fat of mice across their lifespan
Zhu, Q., Yan, J., Ni, J., & Feng, Y. (2020) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/j.bbalip.2020.158639 · Cited by 38 · see citing works
Caloric restriction mimetics for the treatment of cardiovascular diseases
Sciarretta, S., Forte, M., Castoldi, F., Frati, G., Versaci, F., Sadoshima, J., Kroemer, G., & Maiuri, M. C. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa297 · Cited by 38 · see citing works
Aging and the Biological Response to Liver Injury
Marzioni, M., Pinto, C., Ninfole, E., Gaggiano, L., Benedetti, A., & Maroni, L. (2020) · Seminars in Liver Disease · doi:10.1055/s-0039-3402033 · Cited by 36 · see citing works
Metabolaging: a new geroscience perspective linking aging pathologies and metabolic dysfunction
Khalaf, F., Barayan, D., Saldanha, S., & Jeschke, M. G. (2025) · Metabolism · doi:10.1016/j.metabol.2025.156158 · Cited by 37 · see citing works
Li, B., Skinner, C., Castello, P. R., Kato, M., Easlon, E. J., Xie, L., Li, T., Lu, S.-P., Wang, C., Tsang, F. A., et al. (2011) · Journal of Aging Research · doi:10.4061/2011/673185 · Cited by 35 · see citing works
Meng, G., Zhong, X., & Mei, H. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150624 · Cited by 34 · see citing works
Genetic cartography of longevity in humans and mice: Current landscape and horizons
Hook, M., Roy, S., Williams, E. G., Sleiman, M. S. B., Mozhui, K., Nelson, J. F., Lu, L., Auwerx, J. H., & Williams, R. W. (2018) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2018.01.026 · Cited by 33 · see citing works
Sirtuin Deacetylation Mechanism and Catalytic Role of the Dynamic Cofactor Binding Loop
Shi, Y., Zhou, Y., Wang, S., & Zhang, Y. (2013) · The Journal of Physical Chemistry Letters · doi:10.1021/jz302015s · Cited by 32 · see citing works
Natural genetic variation in C. elegans identified genomic loci controlling metabolite levelsPreprint
Gao, A. W., Sterken, M. G., de Bos, J. U., van Creij, J., Kamble, R., Snoek, B. L., Kammenga, J. E., & Houtkooper, R. H. (2018) · Genome Research · doi:10.1101/gr.232322.117 · Cited by 32 · see citing works
- Authors
- Houtkooper, R. H., Williams, R. W., & Auwerx, J.
- Affiliations
- École Polytechnique Fédérale de Lausanne (CH)
- Corresponding author
- Auwerx, Johan
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2010-07
- Volume
- 142
- Issue
- 1
- Pages
- 9-14
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC3852811
- OpenAlex
- W1993355054
- Cited by
- 217
- References
- 39
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 7 · 2023: 20 · 2022: 17 · 2021: 10 · 2020: 20 · 2019: 22 · 2018: 12 · 2017: 14 · 2016: 13 · 2015: 12 · 2014: 25 · 2013: 17 · 2012: 11
- FWCI
- 4.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Pure Amsterdam UMC (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Data Archiving and Networked Services (DANS) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion)
- Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
- Funders
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (124713)
- National Institute on Alcohol Abuse and Alcoholism
- National Institute of Diabetes and Digestive and Kidney Diseases (DK-59820, P01DK059820)
- 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 › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Geriatrics and Gerontology › Sirtuins and Resveratrol in Medicine
- Keywords
- aging, longevity, metabolic regulation, metabolic networks, healthspan, metabolic adaptation, cellular networks, molecular networks
- MeSH terms
- Aging, Amino Acids, Essential, Animals, Humans, Longevity, Methionine, Metabolic Networks and Pathways
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review