Home LiteratureArticle Details
PMID: 23723238 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

A Tumor suppressor complex with GAP activity for the Rag GTPases that signal amino acid sufficiency to mTORC1.

Science (New York, N.Y.) ·Vol. 340 ·No. 6136 ·2013-05-31 ·Pages 1100-6

Bar-Peled L, Chantranupong L, Cherniack AD, Chen WW, Ottina KA, Grabiner BC, Spear ED, Carter SL, Meyerson M, Sabatini DM

Abstract

The mTOR complex 1 (mTORC1) pathway promotes cell growth in response to many cues, including amino acids, which act through the Rag guanosine triphosphatases (GTPases) to promote mTORC1 translocation to the lysosomal surface, its site of activation. Although progress has been made in identifying positive regulators of the Rags, it is unknown if negative factors also exist. Here, we identify GATOR as a complex that interacts with the Rags and is composed of two subcomplexes we call GATOR1 and -2. Inhibition of GATOR1 subunits (DEPDC5, Nprl2, and Nprl3) makes mTORC1 signaling resistant to amino acid deprivation. In contrast, inhibition of GATOR2 subunits (Mios, WDR24, WDR59, Seh1L, and Sec13) suppresses mTORC1 signaling, and epistasis analysis shows that GATOR2 negatively regulates DEPDC5. GATOR1 has GTPase-activating protein (GAP) activity for RagA and RagB, and its components are mutated in human cancer. In cancer cells with inactivating mutations in GATOR1, mTORC1 is hyperactive and insensitive to amino acid starvation, and such cells are hypersensitive to rapamycin, an mTORC1 inhibitor. Thus, we identify a key negative regulator of the Rag GTPases and reveal that, like other mTORC1 regulators, Rag function can be deregulated in cancer.

MeSH Terms
Amino Acids/metabolism Carrier Proteins/antagonists & inhibitors,genetics,metabolism Cell Line, Tumor GTPase-Activating Proteins HEK293 Cells Humans Lysosomes/enzymology Mechanistic Target of Rapamycin Complex 1 Monomeric GTP-Binding Proteins/metabolism Multiprotein Complexes Mutation Neoplasms/enzymology,genetics Nuclear Proteins/antagonists & inhibitors,genetics,metabolism Proteins/metabolism RNA, Small Interfering/genetics TOR Serine-Threonine Kinases Tumor Suppressor Proteins/antagonists & inhibitors,genetics,metabolism
Chemicals
Amino Acids Carrier Proteins GTPase-Activating Proteins Multiprotein Complexes NPRL2 protein, human NPRL3 protein, human Nuclear Proteins Proteins RNA, Small Interfering SEC13 protein, human Tumor Suppressor Proteins WDR24 protein, human Mechanistic Target of Rapamycin Complex 1 TOR Serine-Threonine Kinases Monomeric GTP-Binding Proteins
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Bar-Peled Liron
Whitehead Institute for Biomedical Research and Massachusetts Institute of Technology, Department of Biology, Cambridge, MA 02142, USA.
Chantranupong Lynne
Cherniack Andrew D
Chen Walter W
Ottina Kathleen A
Grabiner Brian C
Spear Eric D
Carter Scott L
Meyerson Matthew
Sabatini David M
References (31)
31 references, click to expand
  1. Selective regulation of autophagy by the Iml1-Npr2-Npr3 complex in the absence of nitrogen starvation.
    Mol Biol Cell. 2011 Nov;22(21):4124-33 PMID: 21900499
  2. A conserved coatomer-related complex containing Sec13 and Seh1 dynamically associates with the vacuole in Saccharomyces cerevisiae.
    Mol Cell Proteomics. 2011 Jun;10(6):M110.006478 PMID: 21454883
  3. mTOR signaling in growth control and disease.
    Cell. 2012 Apr 13;149(2):274-93 PMID: 22500797
  4. Absolute quantification of somatic DNA alterations in human cancer.
    Nat Biotechnol. 2012 May;30(5):413-21 PMID: 22544022
  5. missing oocyte encodes a highly conserved nuclear protein required for the maintenance of the meiotic cycle and oocyte identity in Drosophila.
    Development. 2004 Mar;131(5):1029-39 PMID: 14973288
  6. Mammalian target of rapamycin inhibition promotes response to epidermal growth factor receptor kinase inhibitors in PTEN-deficient and PTEN-intact glioblastoma cells.
    Cancer Res. 2006 Aug 15;66(16):7864-9 PMID: 16912159
  7. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR.
    Proc Natl Acad Sci U S A. 2001 Aug 28;98(18):10314-9 PMID: 11504908
  8. Complex chromosome 22 rearrangements in astrocytic tumors identified using microsatellite and chromosome 22 tile path array analysis.
    Genes Chromosomes Cancer. 2005 Jun;43(2):181-93 PMID: 15770670
  9. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery.
    Cell. 2002 Jul 26;110(2):163-75 PMID: 12150925
  10. Ragulator-Rag complex targets mTORC1 to the lysosomal surface and is necessary for its activation by amino acids.
    Cell. 2010 Apr 16;141(2):290-303 PMID: 20381137
  11. Membrane-coating lattice scaffolds in the nuclear pore and vesicle coats: commonalities, differences, challenges.
    Nucleus. 2010 Jul-Aug;1(4):314-8 PMID: 21327078
  12. Comprehensive genomic characterization defines human glioblastoma genes and core pathways.
    Nature. 2008 Oct 23;455(7216):1061-8 PMID: 18772890
  13. Novel G proteins, Rag C and Rag D, interact with GTP-binding proteins, Rag A and Rag B.
    J Biol Chem. 2001 Mar 9;276(10):7246-57 PMID: 11073942
  14. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex.
    Science. 2005 Feb 18;307(5712):1098-101 PMID: 15718470
  15. The 630-kb lung cancer homozygous deletion region on human chromosome 3p21.3: identification and evaluation of the resident candidate tumor suppressor genes. The International Lung Cancer Chromosome 3p21.3 Tumor Suppressor Gene Consortium.
    Cancer Res. 2000 Nov 1;60(21):6116-33 PMID: 11085536
  16. Regulation of TORC1 by Rag GTPases in nutrient response.
    Nat Cell Biol. 2008 Aug;10(8):935-45 PMID: 18604198
  17. Leucyl-tRNA synthetase is an intracellular leucine sensor for the mTORC1-signaling pathway.
    Cell. 2012 Apr 13;149(2):410-24 PMID: 22424946
  18. Integrated genomic analyses of ovarian carcinoma.
    Nature. 2011 Jun 29;474(7353):609-15 PMID: 21720365
  19. Three-dimensional structures of H-ras p21 mutants: molecular basis for their inability to function as signal switch molecules.
    Cell. 1990 Aug 10;62(3):539-48 PMID: 2199064
  20. Functional characterization of the candidate tumor suppressor gene NPRL2/G21 located in 3p21.3C.
    Cancer Res. 2004 Sep 15;64(18):6438-43 PMID: 15374952
  21. mTORC1 senses lysosomal amino acids through an inside-out mechanism that requires the vacuolar H(+)-ATPase.
    Science. 2011 Nov 4;334(6056):678-83 PMID: 22053050
  22. Target of rapamycin (TOR) in nutrient signaling and growth control.
    Genetics. 2011 Dec;189(4):1177-201 PMID: 22174183
  23. Expression of several genes in the human chromosome 3p21.3 homozygous deletion region by an adenovirus vector results in tumor suppressor activities in vitro and in vivo.
    Cancer Res. 2002 May 1;62(9):2715-20 PMID: 11980673
  24. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1.
    Science. 2008 Jun 13;320(5882):1496-501 PMID: 18497260
  25. A practical approach to crosslinking.
    Mol Biol Rep. 1993 Apr;17(3):167-83 PMID: 8326953
  26. A genome-wide screen for regulators of TORC1 in response to amino acid starvation reveals a conserved Npr2/3 complex.
    PLoS Genet. 2009 Jun;5(6):e1000515 PMID: 19521502
  27. Mitochondria regulate autophagy by conserved signalling pathways.
    EMBO J. 2011 Jun 1;30(11):2101-14 PMID: 21468027
  28. mTOR and cancer: insights into a complex relationship.
    Nat Rev Cancer. 2006 Sep;6(9):729-34 PMID: 16915295
  29. PIK3CA/PTEN mutations and Akt activation as markers of sensitivity to allosteric mTOR inhibitors.
    Clin Cancer Res. 2012 Mar 15;18(6):1777-89 PMID: 22422409
  30. Ragulator is a GEF for the rag GTPases that signal amino acid levels to mTORC1.
    Cell. 2012 Sep 14;150(6):1196-208 PMID: 22980980
  31. Molecular mechanisms of mTOR-mediated translational control.
    Nat Rev Mol Cell Biol. 2009 May;10(5):307-18 PMID: 19339977
Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
1095-9203
Published
2013-05-31
Pages
1100-6
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC3728654
Subset
IM
Grants
Howard Hughes Medical Institute · United States
NCI NIH HHS · P30 CA014051 · United States
NCI NIH HHS · CA103866 · United States
NCI NIH HHS · F31 CA180271 · United States
NCI NIH HHS · R01 CA129105 · United States
NIAID NIH HHS · AI47389 · United States
NCI NIH HHS · U24 CA143867 · United States
NIAID NIH HHS · R01 AI047389 · United States
NCI NIH HHS · R01 CA103866 · United States
NIAID NIH HHS · R37 AI047389 · United States
NCI NIH HHS · U24CA143867 · United States
Corrections
CommentIn
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