Home LiteratureArticle Details
PMID: 19129480 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Essential role of hIST1 in cytokinesis.

Molecular biology of the cell ·Vol. 20 ·No. 5 ·2009-03-00 ·Pages 1374-87

Agromayor M, Carlton JG, Phelan JP, Matthews DR, Carlin LM, Ameer-Beg S, Bowers K, Martin-Serrano J

Abstract

The last steps of multivesicular body (MVB) formation, human immunodeficiency virus (HIV)-1 budding and cytokinesis require a functional endosomal sorting complex required for transport (ESCRT) machinery to facilitate topologically equivalent membrane fission events. Increased sodium tolerance (IST) 1, a new positive modulator of the ESCRT pathway, has been described recently, but an essential function of this highly conserved protein has not been identified. Here, we describe the previously uncharacterized KIAA0174 as the human homologue of IST1 (hIST1), and we report its conserved interaction with VPS4, CHMP1A/B, and LIP5. We also identify a microtubule interacting and transport (MIT) domain interacting motif (MIM) in hIST1 that is necessary for its interaction with VPS4, LIP5 and other MIT domain-containing proteins, namely, MITD1, AMSH, UBPY, and Spastin. Importantly, hIST1 is essential for cytokinesis in mammalian cells but not for HIV-1 budding, thus providing a novel mechanism of functional diversification of the ESCRT machinery. Last, we show that the hIST1 MIM activity is essential for cytokinesis, suggesting possible mechanisms to explain the role of hIST1 in the last step of mammalian cell division.

MeSH Terms
Amino Acid Sequence Binding Sites Carrier Proteins/metabolism Cytokinesis/physiology Endosomal Sorting Complexes Required for Transport Endosomes/metabolism HIV-1/physiology HeLa Cells Humans Molecular Sequence Data Nuclear Proteins/metabolism Oncogene Proteins/analysis,chemistry,physiology Protein Interaction Mapping Protein Structure, Tertiary Protein Transport/genetics Sequence Alignment Vesicular Transport Proteins
Chemicals
CHMP1A protein, human Carrier Proteins Endosomal Sorting Complexes Required for Transport IST1 protein, human Nuclear Proteins Oncogene Proteins VTA1 protein, human Vesicular Transport Proteins
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Agromayor Monica
Department of Infectious Diseases, King's College London School of Medicine, London, United Kingdom.
Carlton Jez G
Phelan John P
Matthews Daniel R
Carlin Leo M
Ameer-Beg Simon
Bowers Katherine
Martin-Serrano Juan
References (57)
57 references, click to expand
  1. Did2 coordinates Vps4-mediated dissociation of ESCRT-III from endosomes.
    J Cell Biol. 2006 Dec 4;175(5):715-20 PMID: 17130288
  2. Divergent retroviral late-budding domains recruit vacuolar protein sorting factors by using alternative adaptor proteins.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12414-9 PMID: 14519844
  3. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding.
    Cell. 2001 Oct 5;107(1):55-65 PMID: 11595185
  4. 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
  5. Breaking up is hard to do - membrane traffic in cytokinesis.
    J Cell Sci. 2008 May 15;121(Pt 10):1569-76 PMID: 18469013
  6. AIP1/ALIX is a binding partner for HIV-1 p6 and EIAV p9 functioning in virus budding.
    Cell. 2003 Sep 19;114(6):689-99 PMID: 14505569
  7. Human ESCRT-II complex and its role in human immunodeficiency virus type 1 release.
    J Virol. 2006 Oct;80(19):9465-80 PMID: 16973552
  8. Methods for studying the yeast vacuole.
    Methods Enzymol. 1991;194:644-61 PMID: 1706462
  9. 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
  10. 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
  11. Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae.
    Traffic. 2004 Mar;5(3):194-210 PMID: 15086794
  12. Vesicle trafficking during somatic cytokinesis.
    Plant Physiol. 2008 Aug;147(4):1544-52 PMID: 18678745
  13. ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1.
    Dev Cell. 2008 Jan;14(1):50-61 PMID: 18194652
  14. The role of ubiquitin in retroviral egress.
    Traffic. 2007 Oct;8(10):1297-303 PMID: 17645437
  15. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting.
    Dev Cell. 2002 Aug;3(2):271-82 PMID: 12194857
  16. Retrovirus budding.
    Annu Rev Cell Dev Biol. 2004;20:395-425 PMID: 15473846
  17. Structural and mechanistic studies of VPS4 proteins.
    EMBO J. 2005 Oct 19;24(20):3658-69 PMID: 16193069
  18. Plasma membrane deformation by circular arrays of ESCRT-III protein filaments.
    J Cell Biol. 2008 Jan 28;180(2):389-402 PMID: 18209100
  19. 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
  20. High-level and high-throughput recombinant protein production by transient transfection of suspension-growing human 293-EBNA1 cells.
    Nucleic Acids Res. 2002 Jan 15;30(2):E9 PMID: 11788735
  21. The protein network of HIV budding.
    Cell. 2003 Sep 19;114(6):701-13 PMID: 14505570
  22. 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
  23. Late budding domains and host proteins in enveloped virus release.
    Virology. 2006 Jan 5;344(1):55-63 PMID: 16364736
  24. Animal cell cytokinesis.
    Annu Rev Cell Dev Biol. 2001;17:351-86 PMID: 11687493
  25. The biogenesis of multivesicular endosomes.
    Nat Rev Mol Cell Biol. 2004 Apr;5(4):317-23 PMID: 15071556
  26. Vta1p and Vps46p regulate the membrane association and ATPase activity of Vps4p at the yeast multivesicular body.
    Proc Natl Acad Sci U S A. 2006 Apr 18;103(16):6202-7 PMID: 16601096
  27. Structural basis of Vta1 function in the multivesicular body sorting pathway.
    Dev Cell. 2008 Jan;14(1):37-49 PMID: 18194651
  28. Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body.
    Dev Cell. 2002 Aug;3(2):283-9 PMID: 12194858
  29. Retrovirus budding.
    Virus Res. 2004 Dec;106(2):87-102 PMID: 15567490
  30. Structural basis for budding by the ESCRT-III factor CHMP3.
    Dev Cell. 2006 Jun;10(6):821-30 PMID: 16740483
  31. Global landscape of protein complexes in the yeast Saccharomyces cerevisiae.
    Nature. 2006 Mar 30;440(7084):637-43 PMID: 16554755
  32. Ist1 regulates Vps4 localization and assembly.
    Mol Biol Cell. 2008 Feb;19(2):465-74 PMID: 18032582
  33. Structural characterization of the MIT domain from human Vps4b.
    Biochem Biophys Res Commun. 2005 Aug 26;334(2):460-5 PMID: 16018968
  34. Parallels between cytokinesis and retroviral budding: a role for the ESCRT machinery.
    Science. 2007 Jun 29;316(5833):1908-12 PMID: 17556548
  35. ESCRT-III recognition by VPS4 ATPases.
    Nature. 2007 Oct 11;449(7163):740-4 PMID: 17928862
  36. Structural basis for selective recognition of ESCRT-III by the AAA ATPase Vps4.
    Nature. 2007 Oct 11;449(7163):735-9 PMID: 17928861
  37. Viral late domains.
    J Virol. 2002 May;76(10):4679-87 PMID: 11967285
  38. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function.
    Proc Natl Acad Sci U S A. 2002 Jan 22;99(2):955-60 PMID: 11805336
  39. Cytokinesis: placing and making the final cut.
    Cell. 2007 Nov 30;131(5):847-60 PMID: 18045532
  40. 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
  41. The ESCRT complexes: structure and mechanism of a membrane-trafficking network.
    Annu Rev Biophys Biomol Struct. 2006;35:277-98 PMID: 16689637
  42. Cep55, a microtubule-bundling protein, associates with centralspindlin to control the midbody integrity and cell abscission during cytokinesis.
    Mol Biol Cell. 2006 Sep;17(9):3881-96 PMID: 16790497
  43. Final stages of cytokinesis and midbody ring formation are controlled by BRUCE.
    Cell. 2008 Mar 7;132(5):832-45 PMID: 18329369
  44. A protein interaction map of Drosophila melanogaster.
    Science. 2003 Dec 5;302(5651):1727-36 PMID: 14605208
  45. The MIT domain of UBPY constitutes a CHMP binding and endosomal localization signal required for efficient epidermal growth factor receptor degradation.
    J Biol Chem. 2007 Oct 19;282(42):30929-37 PMID: 17711858
  46. Novel Ist1-Did2 complex functions at a late step in multivesicular body sorting.
    Mol Biol Cell. 2008 Feb;19(2):475-84 PMID: 18032584
  47. Interaction of AMSH with ESCRT-III and deubiquitination of endosomal cargo.
    J Biol Chem. 2006 Aug 11;281(32):23083-91 PMID: 16760479
  48. Tsg101, a homologue of ubiquitin-conjugating (E2) enzymes, binds the L domain in HIV type 1 Pr55(Gag).
    Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):7724-9 PMID: 11427703
  49. Evidence for a new viral late-domain core sequence, FPIV, necessary for budding of a paramyxovirus.
    J Virol. 2005 Mar;79(5):2988-97 PMID: 15709019
  50. Phosphorylation of ZEN-4/MKLP1 by aurora B regulates completion of cytokinesis.
    Curr Biol. 2005 Apr 26;15(8):778-86 PMID: 15854913
  51. Recycling of ESCRTs by the AAA-ATPase Vps4 is regulated by a conserved VSL region in Vta1.
    J Cell Biol. 2006 Feb 27;172(5):705-17 PMID: 16505166
  52. 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
  53. Animal cytokinesis: from parts list to mechanisms.
    Annu Rev Biochem. 2006;75:543-66 PMID: 16756502
  54. Differential requirements for Alix and ESCRT-III in cytokinesis and HIV-1 release.
    Proc Natl Acad Sci U S A. 2008 Jul 29;105(30):10541-6 PMID: 18641129
  55. 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
  56. 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
  57. Genetic evidence that the Tat proteins of human immunodeficiency virus types 1 and 2 can multimerize in the eukaryotic cell nucleus.
    J Virol. 1993 Aug;67(8):5030-4 PMID: 8331738
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1939-4586
Published
2009-03-00
Epub
2009-00-07
Pages
1374-87
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC2649264
Subset
IM
Grants
Medical Research Council · G0601097 · United Kingdom
Medical Research Council · G0400207 · United Kingdom
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