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PMID: 21827950 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Structural basis for ESCRT-III CHMP3 recruitment of AMSH.

Structure (London, England : 1993) ·Vol. 19 ·No. 8 ·2011-08-10 ·Pages 1149-59

Solomons J, Sabin C, Poudevigne E, Usami Y, Hulsik DL, Macheboeuf P, Hartlieb B, Göttlinger H, Weissenhorn W

Abstract

Endosomal sorting complexes required for transport (ESCRT) recognize ubiquitinated cargo and catalyze diverse budding processes including multivesicular body biogenesis, enveloped virus egress, and cytokinesis. We present the crystal structure of an N-terminal fragment of the deubiquitinating enzyme AMSH (AMSHΔC) in complex with the C-terminal region of ESCRT-III CHMP3 (CHMP3ΔN). AMSHΔC folds into an elongated 90 Å long helical assembly that includes an unusual MIT domain. CHMP3ΔN is unstructured in solution and helical in complex with AMSHΔC, revealing a novel MIT domain interacting motif (MIM) that does not overlap with the CHMP1-AMSH binding site. ITC and SPR measurements demonstrate an unusual high-affinity MIM-MIT interaction. Structural analysis suggests a regulatory role for the N-terminal helical segment of AMSHΔC and its destabilization leads to a loss of function during HIV-1 budding. Our results indicate a tight coupling of ESCRT-III CHMP3 and AMSH functions and provide insight into the regulation of ESCRT-III.

MeSH Terms
Amino Acid Sequence Endosomal Sorting Complexes Required for Transport/chemistry,metabolism HEK293 Cells HIV Infections/virology HIV-1/physiology Humans Hydrogen Bonding Molecular Sequence Data Multiprotein Complexes/chemistry,metabolism Peptide Fragments/chemistry,metabolism Protein Structure, Quaternary Protein Structure, Secondary Protein Structure, Tertiary Ubiquitin Thiolesterase/chemistry,metabolism Virus Release
Chemicals
CHMP3 protein, human Endosomal Sorting Complexes Required for Transport Multiprotein Complexes Peptide Fragments STAMBP protein, human Ubiquitin Thiolesterase
Authors & Affiliations
9 authors, click to expand affiliations / ORCID
Solomons Julianna
Unit of Virus Host Cell Interactions (UVHCI) UMI 3265 Université Joseph Fourier-EMBL-CNRS, 6 rue Jules Horowitz 38042 Grenoble Cedex 9, France.
Sabin Charles
Poudevigne Emilie
Usami Yoshiko
Hulsik David Lutje
Macheboeuf Pauline
Hartlieb Bettina
Göttlinger Heinrich
Weissenhorn Winfried
References (77)
77 references, click to expand
  1. Scaling and assessment of data quality.
    Acta Crystallogr D Biol Crystallogr. 2006 Jan;62(Pt 1):72-82 PMID: 16369096
  2. The ESCRT machinery: new functions in viral and cellular biology.
    Biochem Soc Trans. 2009 Feb;37(Pt 1):195-9 PMID: 19143630
  3. Helical structures of ESCRT-III are disassembled by VPS4.
    Science. 2008 Sep 5;321(5894):1354-7 PMID: 18687924
  4. Ordered assembly of the ESCRT-III complex on endosomes is required to sequester cargo during MVB formation.
    Dev Cell. 2008 Oct;15(4):578-89 PMID: 18854142
  5. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes.
    Nature. 2010 Apr 8;464(7290):864-9 PMID: 20305637
  6. A crescent-shaped ALIX dimer targets ESCRT-III CHMP4 filaments.
    Structure. 2009 Jun 10;17(6):843-56 PMID: 19523902
  7. Ligand-induced lysosomal epidermal growth factor receptor (EGFR) degradation is preceded by proteasome-dependent EGFR de-ubiquitination.
    J Biol Chem. 2003 Sep 12;278(37):35781-90 PMID: 12829707
  8. AMSH interacts with ESCRT-0 to regulate the stability and trafficking of CXCR4.
    J Biol Chem. 2010 Apr 30;285(18):13990-4004 PMID: 20159979
  9. Macrophage-tropic human immunodeficiency virus isolates from different patients exhibit unusual V3 envelope sequence homogeneity in comparison with T-cell-tropic isolates: definition of critical amino acids involved in cell tropism.
    J Virol. 1992 Nov;66(11):6547-54 PMID: 1404602
  10. Effect of mutations affecting the p6 gag protein on human immunodeficiency virus particle release.
    Proc Natl Acad Sci U S A. 1991 Apr 15;88(8):3195-9 PMID: 2014240
  11. The CCP4 suite: programs for protein crystallography.
    Acta Crystallogr D Biol Crystallogr. 1994 Sep 1;50(Pt 5):760-3 PMID: 15299374
  12. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding.
    Cell. 2001 Oct 5;107(1):55-65 PMID: 11595185
  13. Preparation of selenomethionyl proteins for phase determination.
    Methods Enzymol. 1997;276:523-30 PMID: 9048379
  14. Evolution and assembly of ESCRTs.
    Biochem Soc Trans. 2009 Feb;37(Pt 1):151-5 PMID: 19143621
  15. Two distinct modes of ESCRT-III recognition are required for VPS4 functions in lysosomal protein targeting and HIV-1 budding.
    Dev Cell. 2008 Jul;15(1):62-73 PMID: 18606141
  16. Divergent pathways lead to ESCRT-III-catalyzed membrane fission.
    Trends Biochem Sci. 2011 Apr;36(4):199-210 PMID: 21030261
  17. A deubiquitinating enzyme UBPY regulates the level of protein ubiquitination on endosomes.
    Traffic. 2006 Aug;7(8):1017-31 PMID: 16771824
  18. A role for the ESCRT system in cell division in archaea.
    Science. 2008 Dec 12;322(5908):1710-3 PMID: 19008417
  19. UBPY-mediated epidermal growth factor receptor (EGFR) de-ubiquitination promotes EGFR degradation.
    J Biol Chem. 2007 Jan 19;282(3):1658-69 PMID: 17121848
  20. Retrovirus budding.
    Annu Rev Cell Dev Biol. 2004;20:395-425 PMID: 15473846
  21. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments.
    J Cell Biol. 2008 Jan 28;180(2):389-402 PMID: 18209100
  22. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis.
    EMBO J. 2007 Oct 3;26(19):4215-27 PMID: 17853893
  23. Structure and disassembly of filaments formed by the ESCRT-III subunit Vps24.
    Structure. 2008 Sep 10;16(9):1345-56 PMID: 18786397
  24. Refinement of macromolecular structures by the maximum-likelihood method.
    Acta Crystallogr D Biol Crystallogr. 1997 May 1;53(Pt 3):240-55 PMID: 15299926
  25. ESCRT complexes and the biogenesis of multivesicular bodies.
    Curr Opin Cell Biol. 2008 Feb;20(1):4-11 PMID: 18222686
  26. Clathrin anchors deubiquitinating enzymes, AMSH and AMSH-like protein, on early endosomes.
    Genes Cells. 2006 Jun;11(6):593-606 PMID: 16716190
  27. Release of autoinhibition converts ESCRT-III components into potent inhibitors of HIV-1 budding.
    Proc Natl Acad Sci U S A. 2006 Dec 12;103(50):19140-5 PMID: 17146056
  28. Computational model of membrane fission catalyzed by ESCRT-III.
    PLoS Comput Biol. 2009 Nov;5(11):e1000575 PMID: 19936052
  29. Evidence for a direct role of the Doa4 deubiquitinating enzyme in protein sorting into the MVB pathway.
    Traffic. 2007 May;8(5):566-81 PMID: 17376168
  30. Amino-terminal dimerization, NRDP1-rhodanese interaction, and inhibited catalytic domain conformation of the ubiquitin-specific protease 8 (USP8).
    J Biol Chem. 2006 Dec 8;281(49):38061-70 PMID: 17035239
  31. Bro1 coordinates deubiquitination in the multivesicular body pathway by recruiting Doa4 to endosomes.
    J Cell Biol. 2004 Aug 30;166(5):717-29 PMID: 15326198
  32. Filovirus assembly and budding.
    Virology. 2006 Jan 5;344(1):64-70 PMID: 16364737
  33. Essential role of hIST1 in cytokinesis.
    Mol Biol Cell. 2009 Mar;20(5):1374-87 PMID: 19129480
  34. Dynamic regulation of ubiquitylation and deubiquitylation at the central spindle during cytokinesis.
    J Cell Sci. 2008 Apr 15;121(Pt 8):1325-33 PMID: 18388320
  35. The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways.
    Mol Biol Cell. 2000 Oct;11(10):3365-80 PMID: 11029042
  36. Substructure solution with SHELXD.
    Acta Crystallogr D Biol Crystallogr. 2002 Oct;58(Pt 10 Pt 2):1772-9 PMID: 12351820
  37. No strings attached: the ESCRT machinery in viral budding and cytokinesis.
    J Cell Sci. 2009 Jul 1;122(Pt 13):2167-77 PMID: 19535732
  38. Targeting of AMSH to endosomes is required for epidermal growth factor receptor degradation.
    J Biol Chem. 2007 Mar 30;282(13):9805-9812 PMID: 17261583
  39. A conserved late endosome-targeting signal required for Doa4 deubiquitylating enzyme function.
    J Cell Biol. 2006 Dec 4;175(5):825-35 PMID: 17145966
  40. Breaking the chains: structure and function of the deubiquitinases.
    Nat Rev Mol Cell Biol. 2009 Aug;10(8):550-63 PMID: 19626045
  41. Auto-rickshaw: an automated crystal structure determination platform as an efficient tool for the validation of an X-ray diffraction experiment.
    Acta Crystallogr D Biol Crystallogr. 2005 Apr;61(Pt 4):449-57 PMID: 15805600
  42. Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains.
    Nature. 2008 Sep 18;455(7211):358-62 PMID: 18758443
  43. Membrane scission by the ESCRT-III complex.
    Nature. 2009 Mar 12;458(7235):172-7 PMID: 19234443
  44. Automated detection of remote homology.
    Curr Opin Struct Biol. 2002 Jun;12(3):362-7 PMID: 12127456
  45. A unique cell division machinery in the Archaea.
    Proc Natl Acad Sci U S A. 2008 Dec 2;105(48):18942-6 PMID: 18987308
  46. Structural basis for budding by the ESCRT-III factor CHMP3.
    Dev Cell. 2006 Jun;10(6):821-30 PMID: 16740483
  47. Structure/function analysis of four core ESCRT-III proteins reveals common regulatory role for extreme C-terminal domain.
    Traffic. 2007 Aug;8(8):1068-79 PMID: 17547705
  48. Endosomal deubiquitinating enzymes control ubiquitination and down-regulation of protease-activated receptor 2.
    J Biol Chem. 2009 Oct 9;284(41):28453-28466 PMID: 19684015
  49. Structural basis for the Golgi membrane recruitment of Sly1p by Sed5p.
    EMBO J. 2002 Nov 15;21(22):6114-24 PMID: 12426383
  50. The ubiquitin isopeptidase UBPY regulates endosomal ubiquitin dynamics and is essential for receptor down-regulation.
    J Biol Chem. 2006 May 5;281(18):12618-24 PMID: 16520378
  51. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B.
    Nat Struct Mol Biol. 2008 Dec;15(12):1278-86 PMID: 18997780
  52. Deubiquitination step in the endocytic pathway of yeast plasma membrane proteins: crucial role of Doa4p ubiquitin isopeptidase.
    Mol Cell Biol. 2001 Jul;21(14):4482-94 PMID: 11416128
  53. Intra-endosomal membrane traffic.
    Trends Cell Biol. 2006 Oct;16(10):514-21 PMID: 16949287
  54. The ESCRT pathway and HIV-1 budding.
    Biochem Soc Trans. 2009 Feb;37(Pt 1):181-4 PMID: 19143627
  55. Functional reconstitution of ESCRT-III assembly and disassembly.
    Cell. 2009 Jan 9;136(1):97-109 PMID: 19135892
  56. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery.
    Science. 2007 Jun 29;316(5833):1908-12 PMID: 17556548
  57. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins.
    Nature. 2009 Mar 26;458(7237):445-52 PMID: 19325624
  58. ESCRT-III recognition by VPS4 ATPases.
    Nature. 2007 Oct 11;449(7163):740-4 PMID: 17928862
  59. Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4.
    Nature. 2007 Oct 11;449(7163):735-9 PMID: 17928861
  60. Coot: model-building tools for molecular graphics.
    Acta Crystallogr D Biol Crystallogr. 2004 Dec;60(Pt 12 Pt 1):2126-32 PMID: 15572765
  61. ESCRTing proteins in the endocytic pathway.
    Trends Biochem Sci. 2007 Dec;32(12):561-73 PMID: 17988873
  62. A systematic analysis of human CHMP protein interactions: additional MIT domain-containing proteins bind to multiple components of the human ESCRT III complex.
    Genomics. 2006 Sep;88(3):333-46 PMID: 16730941
  63. Possible involvement of a novel STAM-associated molecule "AMSH" in intracellular signal transduction mediated by cytokines.
    J Biol Chem. 1999 Jul 2;274(27):19129-35 PMID: 10383417
  64. A protein's final ESCRT.
    Traffic. 2005 Jan;6(1):2-9 PMID: 15569240
  65. AMSH is an endosome-associated ubiquitin isopeptidase.
    J Cell Biol. 2004 Aug 16;166(4):487-92 PMID: 15314065
  66. Structure and ESCRT-III protein interactions of the MIT domain of human VPS4A.
    Proc Natl Acad Sci U S A. 2005 Sep 27;102(39):13813-8 PMID: 16174732
  67. Calcium-sensing receptor endocytosis links extracellular calcium signaling to parathyroid hormone-related peptide secretion via a Rab11a-dependent and AMSH-sensitive mechanism.
    Mol Endocrinol. 2007 Jun;21(6):1394-407 PMID: 17426287
  68. Structural basis for ESCRT-III protein autoinhibition.
    Nat Struct Mol Biol. 2009 Jul;16(7):754-62 PMID: 19525971
  69. Interaction of AMSH with ESCRT-III and deubiquitination of endosomal cargo.
    J Biol Chem. 2006 Aug 11;281(32):23083-91 PMID: 16760479
  70. AMSH, an ESCRT-III associated enzyme, deubiquitinates cargo on MVB/late endosomes.
    Cell Struct Funct. 2007;31(2):159-72 PMID: 17159328
  71. Ubiquitination regulates proteolytic processing of G protein-coupled receptors after their sorting to lysosomes.
    J Biol Chem. 2009 Jul 17;284(29):19361-70 PMID: 19433584
  72. Activation of the endosome-associated ubiquitin isopeptidase AMSH by STAM, a component of the multivesicular body-sorting machinery.
    Curr Biol. 2006 Jan 24;16(2):160-5 PMID: 16431367
  73. The cell biology of HIV-1 virion genesis.
    Cell Host Microbe. 2009 Jun 18;5(6):550-8 PMID: 19527882
  74. Structural basis for autoinhibition of ESCRT-III CHMP3.
    J Mol Biol. 2008 May 9;378(4):818-27 PMID: 18395747
  75. The Vps4p AAA ATPase regulates membrane association of a Vps protein complex required for normal endosome function.
    EMBO J. 1998 Jun 1;17(11):2982-93 PMID: 9606181
  76. Automated protein model building combined with iterative structure refinement.
    Nat Struct Biol. 1999 May;6(5):458-63 PMID: 10331874
  77. Regulation of epidermal growth factor receptor down-regulation by UBPY-mediated deubiquitination at endosomes.
    Mol Biol Cell. 2005 Nov;16(11):5163-74 PMID: 16120644
Article Info
Journal
Structure (London, England : 1993)
Abbr.
Structure
ISSN
1878-4186
DOI
10.1016/j.str.2011.05.011
Published
2011-08-10
Pages
1149-59
Language
English
Region
United States
NLM ID
101087697
PMCID
PMC3154637
Subset
IM
Grants
NIAID NIH HHS · R37 AI029873 · United States
NIAID NIH HHS · R37 AI029873-22 · United States
NIAID NIH HHS · R37AI029873 · United States
Databases
PDB
2XZE
Corrections
CommentIn
PMID: 21827939
External Links
PubMed source DOI: 10.1016/j.str.2011.05.011 PMC Full Text View journal details
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