Home LiteratureArticle Details
PMID: 22405001 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

The UBAP1 subunit of ESCRT-I interacts with ubiquitin via a SOUBA domain.

Structure (London, England : 1993) ·Vol. 20 ·No. 3 ·2012-03-07 ·Pages 414-28

Agromayor M, Soler N, Caballe A, Kueck T, Freund SM, Allen MD, Bycroft M, Perisic O, Ye Y, McDonald B, Scheel H, Hofmann K, Neil SJ, Martin-Serrano J, Williams RL

Abstract

The endosomal sorting complexes required for transport (ESCRTs) facilitate endosomal sorting of ubiquitinated cargo, MVB biogenesis, late stages of cytokinesis, and retroviral budding. Here we show that ubiquitin associated protein 1 (UBAP1), a subunit of human ESCRT-I, coassembles in a stable 1:1:1:1 complex with Vps23/TSG101, VPS28, and VPS37. The X-ray crystal structure of the C-terminal region of UBAP1 reveals a domain that we describe as a solenoid of overlapping UBAs (SOUBA). NMR analysis shows that each of the three rigidly arranged overlapping UBAs making up the SOUBA interact with ubiquitin. We demonstrate that UBAP1-containing ESCRT-I is essential for degradation of antiviral cell-surface proteins, such as tetherin (BST-2/CD317), by viral countermeasures, namely, the HIV-1 accessory protein Vpu and the Kaposi sarcoma-associated herpesvirus (KSHV) ubiquitin ligase K5.

MeSH Terms
Amino Acid Sequence Antigens, CD/metabolism Carrier Proteins/genetics,metabolism Chromatography, Gel Crystallography, X-Ray Endosomal Sorting Complexes Required for Transport/metabolism GPI-Linked Proteins/metabolism Human Immunodeficiency Virus Proteins/metabolism Humans Immediate-Early Proteins/metabolism Models, Molecular Molecular Sequence Data Nuclear Magnetic Resonance, Biomolecular Protein Binding Protein Structure, Tertiary Ubiquitin/metabolism Viral Regulatory and Accessory Proteins/metabolism
Chemicals
Antigens, CD BST2 protein, human Carrier Proteins Endosomal Sorting Complexes Required for Transport GPI-Linked Proteins Human Immunodeficiency Virus Proteins Immediate-Early Proteins K5 protein, Human herpesvirus 8 UBAP1 protein, human Ubiquitin Viral Regulatory and Accessory Proteins vpu protein, Human immunodeficiency virus 1
Authors & Affiliations
15 authors, click to expand affiliations / ORCID
Agromayor Monica
Department of Infectious Diseases, King's College London School of Medicine, London SE1 9RT, UK.
Soler Nicolas
Caballe Anna
Kueck Tonya
Freund Stefan M
Allen Mark D
Bycroft Mark
Perisic Olga
Ye Yu
McDonald Bethan
Scheel Hartmut
Hofmann Kay
Neil Stuart J D
Martin-Serrano Juan
Williams Roger L
References (60)
60 references, click to expand
  1. Structure of the UBA domain of Dsk2p in complex with ubiquitin molecular determinants for ubiquitin recognition.
    Structure. 2005 Apr;13(4):521-32 PMID: 15837191
  2. Essential ingredients for HIV-1 budding.
    Cell Host Microbe. 2011 Mar 17;9(3):172-174 PMID: 21402355
  3. A flexible motif search technique based on generalized profiles.
    Comput Chem. 1996 Mar;20(1):3-23 PMID: 8867839
  4. UMA and MABP domains throw light on receptor endocytosis and selection of endosomal cargoes.
    Bioinformatics. 2010 Jun 15;26(12):1477-80 PMID: 20448139
  5. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery.
    Science. 2007 Jun 29;316(5833):1908-12 PMID: 17556548
  6. A perturbed ubiquitin landscape distinguishes between ubiquitin in trafficking and in proteolysis.
    Mol Cell Proteomics. 2011 May;10(5):M111.009753 PMID: 21427232
  7. The ESCRT-0 component HRS is required for HIV-1 Vpu-mediated BST-2/tetherin down-regulation.
    PLoS Pathog. 2011 Feb 03;7(2):e1001265 PMID: 21304933
  8. The emerging shape of the ESCRT machinery.
    Nat Rev Mol Cell Biol. 2007 May;8(5):355-68 PMID: 17450176
  9. It's all in the crystals….
    Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):243-8 PMID: 21460442
  10. Role of ESCRT-I in retroviral budding.
    J Virol. 2003 Apr;77(8):4794-804 PMID: 12663786
  11. The ESCRT pathway.
    Dev Cell. 2011 Jul 19;21(1):77-91 PMID: 21763610
  12. Ubiquitin-dependent sorting into the multivesicular body pathway requires the function of a conserved endosomal protein sorting complex, ESCRT-I.
    Cell. 2001 Jul 27;106(2):145-55 PMID: 11511343
  13. The human endosomal sorting complex required for transport (ESCRT-I) and its role in HIV-1 budding.
    J Biol Chem. 2004 Aug 20;279(34):36059-71 PMID: 15218037
  14. Host factors involved in retroviral budding and release.
    Nat Rev Microbiol. 2011 Jun 16;9(7):519-31 PMID: 21677686
  15. Molecular mechanisms of ubiquitin-dependent membrane traffic.
    Annu Rev Biophys. 2011;40:119-42 PMID: 21332354
  16. Ubiquitin: same molecule, different degradation pathways.
    Cell. 2010 Nov 24;143(5):682-5 PMID: 21111229
  17. Solution structures of UBA domains reveal a conserved hydrophobic surface for protein-protein interactions.
    J Mol Biol. 2002 Jun 21;319(5):1243-55 PMID: 12079361
  18. Retrovirus budding.
    Annu Rev Cell Dev Biol. 2004;20:395-425 PMID: 15473846
  19. Ubiquitin associated protein 1 is a risk factor for frontotemporal lobar degeneration.
    Neurobiol Aging. 2009 Apr;30(4):656-65 PMID: 19217189
  20. Structure of the Tsg101 UEV domain in complex with the PTAP motif of the HIV-1 p6 protein.
    Nat Struct Biol. 2002 Nov;9(11):812-7 PMID: 12379843
  21. 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
  22. The UBA domain: a sequence motif present in multiple enzyme classes of the ubiquitination pathway.
    Trends Biochem Sci. 1996 May;21(5):172-3 PMID: 8871400
  23. HIV-1 accessory protein Vpu internalizes cell-surface BST-2/tetherin through transmembrane interactions leading to lysosomes.
    J Biol Chem. 2009 Dec 11;284(50):35060-72 PMID: 19837671
  24. Essential role of hIST1 in cytokinesis.
    Mol Biol Cell. 2009 Mar;20(5):1374-87 PMID: 19129480
  25. The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation.
    Mol Biol Cell. 2004 Sep;15(9):4337-46 PMID: 15240819
  26. How ubiquitin functions with ESCRTs.
    Traffic. 2011 Oct;12(10):1306-17 PMID: 21722280
  27. Identification of human VPS37C, a component of endosomal sorting complex required for transport-I important for viral budding.
    J Biol Chem. 2005 Jan 7;280(1):628-36 PMID: 15509564
  28. Regulation of Tsg101 expression by the steadiness box: a role of Tsg101-associated ligase.
    Mol Biol Cell. 2008 Feb;19(2):754-63 PMID: 18077552
  29. Structure and interaction of ubiquitin-associated domain of human Fas-associated factor 1.
    Protein Sci. 2009 Nov;18(11):2265-76 PMID: 19722279
  30. Dual control of cytokinesis by the ubiquitin and autophagy pathways.
    Autophagy. 2009 May;5(4):561-2 PMID: 19242118
  31. Isolation and characterization of a novel cDNA, UBAP1, derived from the tumor suppressor locus in human chromosome 9p21-22.
    J Cancer Res Clin Oncol. 2001 Oct;127(10):613-8 PMID: 11599797
  32. UBAP1 is a component of an endosome-specific ESCRT-I complex that is essential for MVB sorting.
    Curr Biol. 2011 Jul 26;21(14):1245-50 PMID: 21757351
  33. Diverse polyubiquitin interaction properties of ubiquitin-associated domains.
    Nat Struct Mol Biol. 2005 Aug;12(8):708-14 PMID: 16007098
  34. Structural determinants for selective recognition of a Lys48-linked polyubiquitin chain by a UBA domain.
    Mol Cell. 2005 Jun 10;18(6):687-98 PMID: 15949443
  35. Avid interactions underlie the Lys63-linked polyubiquitin binding specificities observed for UBA domains.
    Nat Struct Mol Biol. 2009 Aug;16(8):883-9 PMID: 19620964
  36. Biochemical analyses of human IST1 and its function in cytokinesis.
    Mol Biol Cell. 2009 Mar;20(5):1360-73 PMID: 19129479
  37. Identification of human MVB12 proteins as ESCRT-I subunits that function in HIV budding.
    Cell Host Microbe. 2007 Jul 12;2(1):41-53 PMID: 18005716
  38. The trafficking and regulation of membrane receptors by the RING-CH ubiquitin E3 ligases.
    Exp Cell Res. 2009 May 15;315(9):1593-600 PMID: 19013150
  39. Dynamics of ESCRT protein recruitment during retroviral assembly.
    Nat Cell Biol. 2011 Apr;13(4):394-401 PMID: 21394083
  40. Molecular mechanism of BST2/tetherin downregulation by K5/MIR2 of Kaposi's sarcoma-associated herpesvirus.
    J Virol. 2009 Oct;83(19):9672-81 PMID: 19605472
  41. A single ubiquitin is sufficient for cargo protein entry into MVBs in the absence of ESCRT ubiquitination.
    J Cell Biol. 2011 Jan 24;192(2):229-42 PMID: 21242292
  42. Ubiquitin-binding domains - from structures to functions.
    Nat Rev Mol Cell Biol. 2009 Oct;10(10):659-71 PMID: 19773779
  43. Vpu directs the degradation of the human immunodeficiency virus restriction factor BST-2/Tetherin via a {beta}TrCP-dependent mechanism.
    J Virol. 2009 Aug;83(16):7931-47 PMID: 19515779
  44. Molecular architecture and functional model of the complete yeast ESCRT-I heterotetramer.
    Cell. 2007 May 4;129(3):485-98 PMID: 17442384
  45. Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu.
    Nature. 2008 Jan 24;451(7177):425-30 PMID: 18200009
  46. Quantitative membrane proteomics reveals new cellular targets of viral immune modulators.
    PLoS Pathog. 2006 Oct;2(10):e107 PMID: 17238276
  47. ESCRT ubiquitin-binding domains function cooperatively during MVB cargo sorting.
    J Cell Biol. 2009 Apr 20;185(2):213-24 PMID: 19380877
  48. The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin.
    PLoS Pathog. 2010 Apr 15;6(4):e1000843 PMID: 20419159
  49. Ubiquitin recognition by the ubiquitin-associated domain of p62 involves a novel conformational switch.
    J Biol Chem. 2008 Feb 29;283(9):5427-40 PMID: 18083707
  50. HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor.
    Cell Host Microbe. 2009 Mar 19;5(3):285-97 PMID: 19286137
  51. Live-cell visualization of dynamics of HIV budding site interactions with an ESCRT component.
    Nat Cell Biol. 2011 Apr;13(4):469-74 PMID: 21394086
  52. Affinity makes the difference: nonselective interaction of the UBA domain of Ubiquilin-1 with monomeric ubiquitin and polyubiquitin chains.
    J Mol Biol. 2008 Mar 14;377(1):162-80 PMID: 18241885
  53. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress.
    Nat Med. 2001 Dec;7(12):1313-9 PMID: 11726971
  54. Toward rational protein crystallization: A Web server for the design of crystallizable protein variants.
    Protein Sci. 2007 Aug;16(8):1569-76 PMID: 17656576
  55. ESCRT-I core and ESCRT-II GLUE domain structures reveal role for GLUE in linking to ESCRT-I and membranes.
    Cell. 2006 Apr 7;125(1):99-111 PMID: 16615893
  56. Sensitivity of human immunodeficiency virus type 1 to the fusion inhibitor T-20 is modulated by coreceptor specificity defined by the V3 loop of gp120.
    J Virol. 2000 Sep;74(18):8358-67 PMID: 10954535
  57. Structural and functional organization of the ESCRT-I trafficking complex.
    Cell. 2006 Apr 7;125(1):113-26 PMID: 16615894
  58. Vpu antagonizes BST-2-mediated restriction of HIV-1 release via beta-TrCP and endo-lysosomal trafficking.
    PLoS Pathog. 2009 May;5(5):e1000450 PMID: 19478868
  59. ESCRT-III protein requirements for HIV-1 budding.
    Cell Host Microbe. 2011 Mar 17;9(3):235-242 PMID: 21396898
  60. Mechanism of Lys48-linked polyubiquitin chain recognition by the Mud1 UBA domain.
    EMBO J. 2005 Sep 21;24(18):3178-89 PMID: 16138082
Article Info
Journal
Structure (London, England : 1993)
Abbr.
Structure
ISSN
1878-4186
DOI
10.1016/j.str.2011.12.013
Published
2012-03-07
Pages
414-28
Language
English
Region
United States
NLM ID
101087697
PMCID
PMC3314968
Subset
IM
Grants
Wellcome Trust · 092096 · United Kingdom
Medical Research Council · G0802777 · United Kingdom
Wellcome Trust · WT093056MA · United Kingdom
Medical Research Council · U105184308 · United Kingdom
Medical Research Council · MC_U105184308 · United Kingdom
Wellcome Trust · 83639/Z/07/Z · United Kingdom
Medical Research Council · G0801937 · United Kingdom
Medical Research Council · MC_U105184326 · United Kingdom
Corrections
CommentIn
PMID: 22404994
External Links
PubMed source DOI: 10.1016/j.str.2011.12.013 PMC Full Text View journal details
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

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2