TOR signaling in growth and metabolism

Wullschleger, Stephan; Loewith, Robbie; Hall, Michael N.

doi:10.1016/j.cell.2006.01.016

Cited by 5,787PI3K/AKT/mTOR signaling in cancerMetabolism, Diabetes, and CancerAutophagy in Disease and Therapy

TOR signaling in growth and metabolism

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Wullschleger, Stephan, Loewith, Robbie, Hall, Michael N.·2006·Cell

DOI 10.1016/j.cell.2006.01.016

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Abstract

The target of rapamycin (TOR) is a conserved Ser/Thr kinase that regulates cell growth and metabolism in response to environmental cues. Here, highlighting contributions from studies in model organisms, we review mammalian TOR complexes and the signaling branches they mediate. TOR is part of two distinct multiprotein complexes, TOR complex 1 (TORC1), which is sensitive to rapamycin, and TORC2, which is not. The physiological consequences of mammalian TORC1 dysregulation suggest that inhibitors of mammalian TOR may be useful in the treatment of cancer, cardiovascular disease, autoimmunity, and metabolic disorders.

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Cellular stresses such as hypoxia or low energy status, sensed by AMPK, inhibit mTOR signaling.
“Cellular stresses, such as hypoxia, or low energy status, which can be sensed by the AMP-sensitive kinase (AMPK) inhibit mTOR signaling”
From Redox control of senescence and age-related disease. (2017) · cites this paper as [111]
Both mTOR complexes promote the transcription of genes involved in carbohydrate metabolism and lipogenesis, enhance protein translation by activating S6K, and downregulate catabolic processes through inhibiting FoxO and autophagy.
“Both complexes promote the transcription of genes involved in carbohydrate metabolism and lipogenesis, enhance protein translation by activating ribosomal protein 6 kinase (S6K) and, at the same time, downregulate catabolic processes through inhibiting the transcriptional activity of the forkhead box transcription factors family (FoxO) and autophagy”
From Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity (2017) · cites this paper as Wullschleger et al., 2006
Both mTOR complexes promote transcription of genes involved in carbohydrate metabolism and lipogenesis, enhance protein translation by activating S6K, and downregulate catabolic processes through inhibiting FoxO and autophagy.
“Both complexes promote the transcription of genes involved in carbohydrate metabolism and lipogenesis, enhance protein translation by activating ribosomal protein 6 kinase (S6K) and, at the same time, downregulate catabolic processes through inhibiting the transcriptional activity of the forkhead box transcription factors family (FoxO) and autophagy (Duvel et al., 2010; Wullschleger et al., 2006).”
From Mitochondrial Activity and Dynamics Changes Regarding Metabolism in Ageing and Obesity (2017) · cites this paper as Wullschleger et al., 2006
TOR is activated in presence of abundant nutrients and inactivated under starvation.
“For our purpose, suffice it to say that TOR is activated in the presence of abundant nutrients, and inactivated under starvation.”
From The common biology of cancer and ageing (2007) · cites this paper as [86]

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Reinke, A. W., Anderson, S., McCaffery, J. M., Yates, J. R., Aronova, S., Chu, S., Fairclough, S. R., Iverson, C., Wedaman, K. P., & Powers, T. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313062200 · Cited by 257 · see citing works
Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex
Sarbassov, D. D., & Sabatini, D. M. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m506096200 · Cited by 248 · see citing works
Growth-regulated recruitment of the essential yeast ribosomal protein gene activator Ifh1
Schawalder, S. B., Kabani, M., Howald, I., Choudhury, U., Werner, M., & Shore, D. (2004) · Nature · doi:10.1038/nature03200 · Cited by 242 · see citing works
Feedback inhibition of Akt signaling limits the growth of tumors lacking Tsc2Preprint
Manning, B. D., Logsdon, M. N., Lipovsky, A. I., Abbott, D. W., Kwiatkowski, D. J., & Cantley, L. C. (2005) · Genes & Development · doi:10.1101/gad.1314605 · Cited by 236 · see citing works
The transcription factor Ifh1 is a key regulator of yeast ribosomal protein genes
Wade, J. T., Hall, D. B., & Struhl, K. (2004) · Nature · doi:10.1038/nature03175 · Cited by 232 · see citing works
Molecular Organization of Target of Rapamycin Complex 2
Wullschleger, S., Loewith, R., Oppliger, W., & Hall, M. N. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m505553200 · Cited by 231 · see citing works
Self-citation
Quantitative phosphorylation profiling of the ERK/p90 ribosomal S6 kinase-signaling cassette and its targets, the tuberous sclerosis tumor suppressors
Ballif, B. A., Roux, P. P., Gerber, S. A., MacKeigan, J. P., Blenis, J., & Gygi, S. P. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0409143102 · Cited by 211 · see citing works
Tor2 Directly Phosphorylates the AGC Kinase Ypk2 To Regulate Actin Polarization
Kamada, Y., Fujioka, Y., Suzuki, N. N., Inagaki, F., Wullschleger, S., Loewith, R., Hall, M. N., & Ohsumi, Y. (2005) · Molecular and Cellular Biology · doi:10.1128/mcb.25.16.7239-7248.2005 · Cited by 207 · see citing works
Self-citation
Exogenous Amino Acids Regulate Trophectoderm Differentiation in the Mouse Blastocyst through an mTOR-Dependent Pathway
Martin, P. M., & Sutherland, A. E. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0461 · Cited by 196 · see citing works
TOR Complex 2 Integrates Cell Movement during Chemotaxis and Signal Relay in Dictyostelium
Lee, S. D., Comer, F. I., Sasaki, A. T., McLeod, I. X., Duong, Y., Okumura, K., Yates, J. R., Parent, C. A., & Firtel, R. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-04-0342 · Cited by 191 · see citing works
Lost in translation
Bjornsti, M., & Houghton, P. J. (2004) · Cancer Cell · doi:10.1016/j.ccr.2004.05.027 · Cited by 181 · see citing works
Control of Nutrient-Sensitive Transcription Programs by the Unconventional Prefoldin URI
Gstaiger, M., Luke, B., Heß, D., Oakeley, E. J., Wirbelauer, C., Blondel, M., Vigneron, M., Peter, M., & Krek, W. (2003) · Science · doi:10.1126/science.1088401 · Cited by 178 · see citing works
Tor Pathway Regulates Rrn3p-dependent Recruitment of Yeast RNA Polymerase I to the Promoter but Does Not Participate in Alteration of the Number of Active Genes
Claypool, J. A., French, S. L., Johzuka, K., Eliason, K., Vũ, L., Dodd, J. A., Beyer, A. L., & Nomura, M. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-08-0594 · Cited by 171 · see citing works
The Farnesyl Transferase Inhibitor (FTI) SCH66336 (lonafarnib) Inhibits Rheb Farnesylation and mTOR Signaling
Basso, A. D., Mirza, A., Liu, G., Long, B. J., Bishop, W. R., & Kirschmeier, P. T. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m503763200 · Cited by 162 · see citing works
Inhibition of Target of Rapamycin Signaling by Rapamycin in the Unicellular Green Alga Chlamydomonas reinhardtii
Crespo, J. L., Díaz‐Troya, S., & Florencio, F. J. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.070847 · Cited by 161 · see citing works
Cell growth : control of cell size
Hall, M. N., RAFF, M. C., & Thomas, G. (2004) · UCL Discovery (University College London) · Cited by 153 · see citing works
Self-citation
Tuberin, the tuberous sclerosis complex 2 tumor suppressor gene product, regulates Rho activation, cell adhesion and migration
Astrinidis, A., Cash, T. P., Hunter, D., Walker, C. L., Chernoff, J., & Henske, E. P. (2002) · Oncogene · doi:10.1038/sj.onc.1205962 · Cited by 151 · see citing works
LST8 negatively regulates amino acid biosynthesis as a component of the TOR pathway
Chen, E. J., & Kaiser, C. A. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200210141 · Cited by 139 · see citing works
Genome‐wide lethality screen identifies new PI4,5P2 effectors that regulate the actin cytoskeleton
Audhya, A., Loewith, R., Parsons, A. B., Gao, L., Tabuchi, M., Zhou, H., Boone, C. M., Hall, M. N., & Emr, S. D. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600384 · Cited by 136 · see citing works
Self-citation
The Solution Structure of the FATC Domain of the Protein Kinase Target of Rapamycin Suggests a Role for Redox-dependent Structural and Cellular Stability
Dames, S. A., Mulet, J. M., Rathgeb–Szabo, K., Hall, M. N., & Grzesiek, S. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m501116200 · Cited by 130 · see citing works
Self-citation
The Pleckstrin Homology Domain Proteins Slm1 and Slm2 Are Required for Actin Cytoskeleton Organization in Yeast and Bind Phosphatidylinositol-4,5-Bisphosphate and TORC2
Fadri‐Moskwik, M., Daquinag, A. C., Wang, S., Xue, T., & Kunz, J. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-07-0564 · Cited by 128 · see citing works
Two Motifs in the Translational Repressor PHAS-I Required for Efficient Phosphorylation by Mammalian Target of Rapamycin and for Recognition by Raptor
Choi, K. M., McMahon, L. P., & Lawrence, J. C. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301142200 · Cited by 126 · see citing works
Rapamycin‐sensitive signalling in long‐term consolidation of auditory cortex‐dependent memory
Tischmeyer, W., Schicknick, H., Kraus, M., Seidenbecher, C. I., Staak, S., Scheich, H., & Gundelfinger, E. D. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02820.x · Cited by 120 · see citing works
Temporal Control of Differentiation by the Insulin Receptor/Tor Pathway in Drosophila
Bateman, J. E., & McNeill, H. (2004) · Cell · doi:10.1016/j.cell.2004.08.028 · Cited by 116 · see citing works
Drosophila Melted Modulates FOXO and TOR Activity
Teleman, A. A., Chen, Y., & Cohen, S. M. (2005) · Developmental Cell · doi:10.1016/j.devcel.2005.07.004 · Cited by 113 · see citing works
Genetic analysis of Pten and Tsc2 functional interactions in the mouse reveals asymmetrical haploinsufficiency in tumor suppressionPreprint
Ma, L., Teruya‐Feldstein, J., Behrendt, N., Chen, Z., Noda, T., Hino, O., Cordon‐Cardo, C., & Pandolfi, P. P. (2005) · Genes & Development · doi:10.1101/gad.1314405 · Cited by 112 · see citing works
Tsc2 is not a critical target of Akt during normal Drosophila developmentPreprint
Dong, J., & Pan, D. (2004) · Genes & Development · doi:10.1101/gad.1240504 · Cited by 105 · see citing works
Inhibitors of the mammalian target of rapamycin
Dancey, J. E. (2005) · Expert Opinion on Investigational Drugs · doi:10.1517/13543784.14.3.313 · Cited by 95 · see citing works
Identification of novel single amino acid changes that result in hyperactivation of the unique GTPase, Rheb, in fission yeast
Urano, J., Comiso, M. J., Guo, L., Aspuria, P.-J. P., Deniskin, R., Tabancay, A. P., Kato‐Stankiewicz, J., & Tamanoi, F. (2005) · Molecular Microbiology · doi:10.1111/j.1365-2958.2005.04877.x · Cited by 94 · see citing works
Stimulation of Signal Transducer and Activator of Transcription-1 (STAT1)-dependent Gene Transcription by Lipopolysaccharide and Interferon-γ Is Regulated by Mammalian Target of Rapamycin
Kristof, A. S., Marks-Kończalik, J., Billings, E. M., & Moss, J. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301053200 · Cited by 90 · see citing works
Identification of FIP200 interaction with the TSC1–TSC2 complex and its role in regulation of cell size control
Gan, B., Melkoumian, Z. K., Wu, X., Guan, K., & Guan, J. (2005) · The Journal of Cell Biology · doi:10.1083/jcb.200411106 · Cited by 86 · see citing works
Drosophila Target of Rapamycin Kinase Functions as a Multimer
Zhang, Y., Billington, C. J., Pan, D., & Neufeld, T. P. (2005) · Genetics · doi:10.1534/genetics.105.051979 · Cited by 81 · see citing works
Activated eIF4E-binding Protein Slows G1 Progression and Blocks Transformation by c-myc without Inhibiting Cell Growth
Lynch, M. C., Fitzgerald, C., Johnston, K. A., Wang, S., & Schmidt, E. V. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m310872200 · Cited by 73 · see citing works
Modulation of insulin action by dietary proteins and amino acids: role of the mammalian target of rapamycin nutrient sensing pathway
Tremblay, F., Jacques, H., & Marette, A. (2005) · Current Opinion in Clinical Nutrition and Metabolic Care · doi:10.1097/01.mco.0000172589.55434.03 · Cited by 71 · see citing works
Rpd3p Relocation Mediates a Transcriptional Response to Rapamycin in Yeast
Humphrey, E. L., Shamji, A. F., Bernstein, B., & Schreiber, S. L. (2004) · Chemistry & Biology · doi:10.1016/j.chembiol.2004.03.001 · Cited by 70 · see citing works
Farnesylthiosalicylic Acid Inhibits Mammalian Target of Rapamycin (mTOR) Activity Both in Cells andin Vitroby Promoting Dissociation of the mTOR-Raptor Complex
McMahon, L. P., Yue, W., Santen, R. J., & Lawrence, J. C. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0305 · Cited by 53 · see citing works
mTOR — beyond transplantation
YOUNG, D., & Nickerson‐Nutter, C. L. (2005) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2005.03.004 · Cited by 42 · see citing works
TOR
(2004) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-18930-2 · Cited by 26 · see citing works
Drug eluting stents in 2005
Gershlick, A. (2005) · Heart · doi:10.1136/hrt.2005.060277 · Cited by 18 · see citing works
TOR signaling in yeast : temporal and spatial control of cell growthPreprint
Loewith, R., & Hall, M. N. (2004) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969672.42.139 · Cited by 13 · see citing works
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Thomas, G., Sabatini, D.M., and Hall, M.N. (2004). TOR, Target of Rapamycin (Heidelberg, Germany: Springer-Verlag).

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Ras, PI(3)K and mTOR signalling controls tumour cell growth
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Bidirectional Transport of Amino Acids Regulates mTOR and Autophagy
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Termination of autophagy and reformation of lysosomes regulated by mTOR
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mTOR controls mitochondrial oxidative function through a YY1–PGC-1α transcriptional complex
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TSC2 Integrates Wnt and Energy Signals via a Coordinated Phosphorylation by AMPK and GSK3 to Regulate Cell Growth
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SREBP activity is regulated by mTORC1 and contributes to Akt-dependent cell growth
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p53 Target Genes Sestrin1 and Sestrin2 Connect Genotoxic Stress and mTOR Signaling
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ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS
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Authors: Wullschleger, S., Loewith, R., & Hall, M. N.
Affiliations: University of Basel (CH)
University of Geneva (CH)
Corresponding author: Hall, Michael N.
ORCID: Wullschleger, Stephan
Loewith, Robbie
Hall, Michael N.
Venue: Cell
Publisher: Elsevier BV
Published: 2006-02
Volume: 124
Issue: 3
Pages: 471-484
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2006.01.016
OpenAlex: W2134138119
Cited by: 5,787
References: 119
Citations by year: 2026: 93 · 2025: 121 · 2024: 161 · 2023: 189 · 2022: 248 · 2021: 275 · 2020: 243 · 2019: 250 · 2018: 253 · 2017: 279 · 2016: 326 · 2015: 375 · 2014: 350 · 2013: 387 · 2012: 418
FWCI: 23.80
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, 2723 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 (publishedVersion)
PubMed (publishedVersion)
Archive ouverte UNIGE (University of Geneva) (publishedVersion, other-oa)
Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by)
Funders: Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › PI3K/AKT/mTOR signaling in cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords: TOR signaling, rapamycin, mTOR inhibitors, cell growth regulation, metabolism, Ser/Thr kinase, cancer therapy, cardiovascular disease, autoimmunity, metabolic disorders
MeSH terms: Aging, Animals, Humans, Memory, Models, Biological, Protein Kinases, Signal Transduction, Protein Serine-Threonine Kinases, Saccharomyces cerevisiae Proteins, Cell Proliferation, TOR Serine-Threonine Kinases

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