Home LiteratureArticle Details
PMID: 19458266 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, U.S. Gov't, Non-P.H.S.

Rheb controls misfolded protein metabolism by inhibiting aggresome formation and autophagy.

Zhou X, Ikenoue T, Chen X, Li L, Inoki K, Guan KL

Abstract

Perinuclear aggresome formation is a key mechanism to dispose of misfolded proteins that exceed the degradative capacity of ubiquitin-proteasome and autophagy-lysosome systems. Functional blockade of either degradative system leads to an enhanced aggresome formation. The tuberous sclerosis complex-Ras homologue enriched in brain-mammalian target of rapamycin (TSC-Rheb-mTOR) pathway is known to play a central role in modulating protein synthesis and autophagy. However, in spite of the constitutive activation of mTOR and the abrogated autophagy activity in TSC1- or TSC2-deficient cells, the TSC mutant cells are defective in aggresome formation and undergo apoptosis upon misfolded protein accumulation both in vitro and in vivo. High Rheb activity in TSC mutant cells inhibits aggresome formation and sensitizes cell death in response to misfolded proteins. Surprisingly, this previously unrecognized function of Rheb is independent of TOR complex 1. Active Rheb disrupts the interaction between dynein and misfolded protein cargos, and therefore blocks aggresome formation by inhibiting dynein-dependent transportation of misfolded proteins. This study reveals a function of Rheb in controlling misfolded protein metabolism by modulating aggresome formation.

MeSH Terms
Animals Autophagy/genetics Dyneins/metabolism ErbB Receptors/metabolism Green Fluorescent Proteins/metabolism Liver/metabolism Mice Mice, Knockout Microtubules/metabolism Monomeric GTP-Binding Proteins/metabolism Neuropeptides/metabolism Protein Folding Ras Homolog Enriched in Brain Protein Transcription Factors/metabolism Tuberous Sclerosis Complex 1 Protein Tumor Suppressor Proteins/genetics,metabolism
Chemicals
Crtc1 protein, mouse Neuropeptides Ras Homolog Enriched in Brain Protein Rheb protein, mouse Transcription Factors Tsc1 protein, mouse Tuberous Sclerosis Complex 1 Protein Tumor Suppressor Proteins Green Fluorescent Proteins ErbB Receptors Dyneins Monomeric GTP-Binding Proteins
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Zhou Xiaoming
Life Sciences Institute, University of Michigan, Ann Arbor, MI 48109, USA.
Ikenoue Tsuneo
Chen Xiaowei
Li Li
Inoki Ken
Guan Kun-Liang
References (31)
31 references, click to expand
  1. Stress and mTORture signaling.
    Oncogene. 2006 Oct 16;25(48):6373-83 PMID: 17041623
  2. Huntingtin acts in the nucleus to induce apoptosis but death does not correlate with the formation of intranuclear inclusions.
    Cell. 1998 Oct 2;95(1):55-66 PMID: 9778247
  3. Cargo transport: molecular motors navigate a complex cytoskeleton.
    Curr Opin Cell Biol. 2008 Feb;20(1):41-7 PMID: 18226515
  4. The roles of intracellular protein-degradation pathways in neurodegeneration.
    Nature. 2006 Oct 19;443(7113):780-6 PMID: 17051204
  5. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells.
    J Cell Sci. 2004 Jun 1;117(Pt 13):2687-97 PMID: 15138286
  6. Loss of autophagy in the central nervous system causes neurodegeneration in mice.
    Nature. 2006 Jun 15;441(7095):880-4 PMID: 16625205
  7. Cytoplasmic dynein/dynactin mediates the assembly of aggresomes.
    Cell Motil Cytoskeleton. 2002 Sep;53(1):26-38 PMID: 12211113
  8. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease.
    Nat Genet. 2004 Jun;36(6):585-95 PMID: 15146184
  9. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control.
    Mol Cell. 2002 Sep;10(3):457-68 PMID: 12408816
  10. A mouse model of TSC1 reveals sex-dependent lethality from liver hemangiomas, and up-regulation of p70S6 kinase activity in Tsc1 null cells.
    Hum Mol Genet. 2002 Mar 1;11(5):525-34 PMID: 11875047
  11. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling.
    Nat Cell Biol. 2002 Sep;4(9):648-57 PMID: 12172553
  12. Suppression of tumorigenicity by the wild-type tuberous sclerosis 2 (Tsc2) gene and its C-terminal region.
    Proc Natl Acad Sci U S A. 1996 Aug 20;93(17):9154-9 PMID: 8799170
  13. Tuberous sclerosis complex gene products, Tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb.
    Curr Biol. 2003 Aug 5;13(15):1259-68 PMID: 12906785
  14. The mammalian unfolded protein response.
    Annu Rev Biochem. 2005;74:739-89 PMID: 15952902
  15. The deacetylase HDAC6 regulates aggresome formation and cell viability in response to misfolded protein stress.
    Cell. 2003 Dec 12;115(6):727-38 PMID: 14675537
  16. Autophagy: process and function.
    Genes Dev. 2007 Nov 15;21(22):2861-73 PMID: 18006683
  17. Inclusion body formation reduces levels of mutant huntingtin and the risk of neuronal death.
    Nature. 2004 Oct 14;431(7010):805-10 PMID: 15483602
  18. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1.
    Science. 2008 Jun 13;320(5882):1496-501 PMID: 18497260
  19. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice.
    Nature. 2006 Jun 15;441(7095):885-9 PMID: 16625204
  20. Rapamycin alleviates toxicity of different aggregate-prone proteins.
    Hum Mol Genet. 2006 Feb 1;15(3):433-42 PMID: 16368705
  21. Autophagy in health and disease: a double-edged sword.
    Science. 2004 Nov 5;306(5698):990-5 PMID: 15528435
  22. Rheb promotes cell growth as a component of the insulin/TOR signalling network.
    Nat Cell Biol. 2003 Jun;5(6):566-71 PMID: 12766776
  23. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase.
    Mol Cell. 2007 Mar 23;25(6):903-15 PMID: 17386266
  24. Insulin activation of Rheb, a mediator of mTOR/S6K/4E-BP signaling, is inhibited by TSC1 and 2.
    Mol Cell. 2003 Jun;11(6):1457-66 PMID: 12820960
  25. TSC2 mediates cellular energy response to control cell growth and survival.
    Cell. 2003 Nov 26;115(5):577-90 PMID: 14651849
  26. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing.
    EMBO J. 2000 Nov 1;19(21):5720-8 PMID: 11060023
  27. Rheb is a direct target of the tuberous sclerosis tumour suppressor proteins.
    Nat Cell Biol. 2003 Jun;5(6):578-81 PMID: 12771962
  28. Aggresomes: a cellular response to misfolded proteins.
    J Cell Biol. 1998 Dec 28;143(7):1883-98 PMID: 9864362
  29. Ligands for clathrin-mediated endocytosis are differentially sorted into distinct populations of early endosomes.
    Cell. 2006 Mar 10;124(5):997-1009 PMID: 16530046
  30. TOR signaling in growth and metabolism.
    Cell. 2006 Feb 10;124(3):471-84 PMID: 16469695
  31. Rheb is an essential regulator of S6K in controlling cell growth in Drosophila.
    Nat Cell Biol. 2003 Jun;5(6):559-65 PMID: 12766775
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-06-02
Epub
2009-00-20
Pages
8923-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2690031
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com