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PMID: 24719330 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Dennd3 functions as a guanine nucleotide exchange factor for small GTPase Rab12 in mouse embryonic fibroblasts.

The Journal of biological chemistry ·Vol. 289 ·No. 20 ·2014-05-16 ·Pages 13986-95

Matsui T, Noguchi K, Fukuda M

Abstract

Small GTPase Rab12 regulates mTORC1 (mammalian target of rapamycin complex 1) activity and autophagy through controlling PAT4 (proton/amino acid transporter 4) trafficking from recycling endosomes to lysosomes, where PAT4 is degraded. However, the precise regulatory mechanism of the Rab12-mediated membrane trafficking pathway remained to be determined because a physiological Rab12-GEF (guanine nucleotide exchange factor) had yet to be identified. In this study we performed functional analyses of Dennd3, which has recently been shown to possess a GEF activity toward Rab12 in vitro. The results showed that knockdown of Dennd3 in mouse embryonic fibroblast cells caused an increase in the amount of PAT4 protein, the same as Rab12 knockdown did, and knockdown of Dennd3 and overexpression of Dennd3 were found to result in an increase and a decrease, respectively, in the intracellular amino acid concentration. Dennd3 overexpression was also found to reduce mTORC1 activity and promoted autophagy in a Rab12-dependent manner. Unexpectedly, however, Dennd3 knockdown had no effect on mTORC1 activity or autophagy despite increasing the intracellular amino acid concentration. Further study showed that Dennd3 knockdown reduced Akt activity, and the reduction in Akt activity is likely to have canceled out amino acid-induced mTORC1 activation through PAT4. These findings indicated that Dennd3 not only functions as a Rab12-GEF but also modulates Akt signaling in mouse embryonic fibroblast cells.

Keywords
Amino Acids Transport Autophagy Endosomes G Proteins Guanine Nucleotide Exchange Factor (GEF) Low Molecular Weight G Proteins Membrane Trafficking Rab Proteins mTOR Complex (mTORC)
MeSH Terms
Amino Acid Transport Systems/metabolism Amino Acids/metabolism Animals Autophagy Cell Line Fibroblasts/cytology,metabolism Gene Knockdown Techniques Guanine Nucleotide Exchange Factors/deficiency,genetics,metabolism Intracellular Space/metabolism Mechanistic Target of Rapamycin Complex 1 Mice Multiprotein Complexes/metabolism Proteolysis Proto-Oncogene Proteins c-akt/metabolism TOR Serine-Threonine Kinases/metabolism rab GTP-Binding Proteins/metabolism
Chemicals
Amino Acid Transport Systems Amino Acids Dennd3 protein, mouse Guanine Nucleotide Exchange Factors Multiprotein Complexes PAT4 protein, mouse Mechanistic Target of Rapamycin Complex 1 Proto-Oncogene Proteins c-akt TOR Serine-Threonine Kinases rab12 protein, mouse rab GTP-Binding Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Matsui Takahide
From the Laboratory of Membrane Trafficking Mechanisms, Department of Developmental Biology and Neurosciences, Graduate School of Life Sciences, Tohoku University, Aobayama, Aoba-ku, Sendai, Miyagi 980-8578, Japan.
Noguchi Kenta
From the Laboratory of Membrane Trafficking Mechanisms, Department of Developmental Biology and Neurosciences, Graduate School of Life Sciences, Tohoku University, Aobayama, Aoba-ku, Sendai, Miyagi 980-8578, Japan.
Fukuda Mitsunori
From the Laboratory of Membrane Trafficking Mechanisms, Department of Developmental Biology and Neurosciences, Graduate School of Life Sciences, Tohoku University, Aobayama, Aoba-ku, Sendai, Miyagi 980-8578, Japan nori@m.tohoku.ac.jp.
References (36)
36 references, click to expand
  1. NDR2-mediated Rabin8 phosphorylation is crucial for ciliogenesis by switching binding specificity from phosphatidylserine to Sec15.
    EMBO J. 2013 Mar 20;32(6):874-85 PMID: 23435566
  2. SLC36A4 (hPAT4) is a high affinity amino acid transporter when expressed in Xenopus laevis oocytes.
    J Biol Chem. 2011 Jan 28;286(4):2455-60 PMID: 21097500
  3. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation.
    Mol Biol Cell. 2009 Apr;20(7):2004-14 PMID: 19225150
  4. Role of Rab GTPases in membrane traffic and cell physiology.
    Physiol Rev. 2011 Jan;91(1):119-49 PMID: 21248164
  5. Small GTPase Rab12 regulates constitutive degradation of transferrin receptor.
    Traffic. 2011 Oct;12(10):1432-43 PMID: 21718402
  6. Metabolic stress controls mTORC1 lysosomal localization and dimerization by regulating the TTT-RUVBL1/2 complex.
    Mol Cell. 2013 Jan 10;49(1):172-85 PMID: 23142078
  7. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery.
    Mol Biol Cell. 2009 Apr;20(7):1992-2003 PMID: 19225151
  8. Rab12 regulates mTORC1 activity and autophagy through controlling the degradation of amino-acid transporter PAT4.
    EMBO Rep. 2013 May;14(5):450-7 PMID: 23478338
  9. Rab GEFs and GAPs.
    Curr Opin Cell Biol. 2010 Aug;22(4):461-70 PMID: 20466531
  10. DENN domain proteins: regulators of Rab GTPases.
    J Biol Chem. 2011 Apr 22;286(16):13791-800 PMID: 21330364
  11. Identification of EPI64 as a GTPase-activating protein specific for Rab27A.
    J Biol Chem. 2006 Oct 20;281(42):31823-31 PMID: 16923811
  12. mTOR in aging, metabolism, and cancer.
    Curr Opin Genet Dev. 2013 Feb;23(1):53-62 PMID: 23317514
  13. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy.
    J Biol Chem. 2009 May 1;284(18):12297-305 PMID: 19258318
  14. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling.
    Science. 2011 Jun 10;332(6035):1322-6 PMID: 21659605
  15. TBC proteins: GAPs for mammalian small GTPase Rab?
    Biosci Rep. 2011 Jun;31(3):159-68 PMID: 21250943
  16. Family-wide characterization of the DENN domain Rab GDP-GTP exchange factors.
    J Cell Biol. 2010 Oct 18;191(2):367-81 PMID: 20937701
  17. Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells.
    J Cell Sci. 2006 Jun 1;119(Pt 11):2196-203 PMID: 16684812
  18. Golgi-resident small GTPase Rab33B interacts with Atg16L and modulates autophagosome formation.
    Mol Biol Cell. 2008 Jul;19(7):2916-25 PMID: 18448665
  19. Regulation of secretory vesicle traffic by Rab small GTPases.
    Cell Mol Life Sci. 2008 Sep;65(18):2801-13 PMID: 18726178
  20. Differential contribution of insulin and amino acids to the mTORC1-autophagy pathway in the liver and muscle.
    J Biol Chem. 2013 Jul 19;288(29):21074-21081 PMID: 23744068
  21. Guidelines for the use and interpretation of assays for monitoring autophagy.
    Autophagy. 2012 Apr;8(4):445-544 PMID: 22966490
  22. TWEAK induces NF-kappaB2 p100 processing and long lasting NF-kappaB activation.
    J Biol Chem. 2003 Sep 19;278(38):36005-12 PMID: 12840022
  23. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling.
    Science. 2011 Jun 10;332(6035):1317-22 PMID: 21659604
  24. The TSC1-2 tumor suppressor controls insulin-PI3K signaling via regulation of IRS proteins.
    J Cell Biol. 2004 Jul 19;166(2):213-23 PMID: 15249583
  25. Rabex-5 protein regulates the endocytic trafficking pathway of ubiquitinated neural cell adhesion molecule L1.
    J Biol Chem. 2012 Sep 21;287(39):32312-23 PMID: 22846990
  26. Plat-E: an efficient and stable system for transient packaging of retroviruses.
    Gene Ther. 2000 Jun;7(12):1063-6 PMID: 10871756
  27. mTOR: from growth signal integration to cancer, diabetes and ageing.
    Nat Rev Mol Cell Biol. 2011 Jan;12(1):21-35 PMID: 21157483
  28. Inappropriate activation of the TSC/Rheb/mTOR/S6K cassette induces IRS1/2 depletion, insulin resistance, and cell survival deficiencies.
    Curr Biol. 2004 Sep 21;14(18):1650-6 PMID: 15380067
  29. Rab GTPases as coordinators of vesicle traffic.
    Nat Rev Mol Cell Biol. 2009 Aug;10(8):513-25 PMID: 19603039
  30. Rab10, a target of the AS160 Rab GAP, is required for insulin-stimulated translocation of GLUT4 to the adipocyte plasma membrane.
    Cell Metab. 2007 Apr;5(4):293-303 PMID: 17403373
  31. Glutaminolysis activates Rag-mTORC1 signaling.
    Mol Cell. 2012 Aug 10;47(3):349-58 PMID: 22749528
  32. Sin1 phosphorylation impairs mTORC2 complex integrity and inhibits downstream Akt signalling to suppress tumorigenesis.
    Nat Cell Biol. 2013 Nov;15(11):1340-50 PMID: 24161930
  33. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1.
    J Biol Chem. 2009 Mar 20;284(12):8023-32 PMID: 19150980
  34. Large scale screening for novel rab effectors reveals unexpected broad Rab binding specificity.
    Mol Cell Proteomics. 2008 Jun;7(6):1031-42 PMID: 18256213
  35. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy.
    Mol Biol Cell. 2009 Apr;20(7):1981-91 PMID: 19211835
  36. Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity.
    Genes Cells. 2006 Sep;11(9):1023-37 PMID: 16923123
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
1083-351X
Published
2014-05-16
Epub
2014-00-09
Pages
13986-95
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC4022869
Subset
IM
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