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PMID: 15728719 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

A mutation in dVps28 reveals a link between a subunit of the endosomal sorting complex required for transport-I complex and the actin cytoskeleton in Drosophila.

Molecular biology of the cell ·Vol. 16 ·No. 5 ·2005-05-00 ·Pages 2301-12

Sevrioukov EA, Moghrabi N, Kuhn M, Krämer H

Abstract

Proteins that constitute the endosomal sorting complex required for transport (ESCRT) are necessary for the sorting of proteins into multivesicular bodies (MVBs) and the budding of several enveloped viruses, including HIV-1. The first of these complexes, ESCRT-I, consists of three proteins: Vps28p, Vps37p, and Vps23p or Tsg101 in mammals. Here, we characterize a mutation in the Drosophila homolog of vps28. The dVps28 gene is essential: homozygous mutants die at the transition from the first to second instar. Removal of maternally contributed dVps28 causes early embryonic lethality. In such embryos lacking dVps28, several processes that require the actin cytoskeleton are perturbed, including axial migration of nuclei, formation of transient furrows during cortical divisions in syncytial embryos, and the subsequent cellularization. Defects in actin cytoskeleton organization also become apparent during sperm individualization in dVps28 mutant testis. Because dVps28 mutant cells contained MVBs, these defects are unlikely to be a secondary consequence of disrupted MVB formation and suggest an interaction between the actin cytoskeleton and endosomal membranes in Drosophila embryos earlier than previously appreciated.

MeSH Terms
Actins/metabolism Amino Acid Sequence Animals Cytoskeleton/metabolism Drosophila/embryology,genetics,metabolism Drosophila Proteins/genetics,metabolism Endosomes/metabolism Female Genes, Insect Male Microscopy, Electron Molecular Sequence Data Mutation Sequence Homology, Amino Acid Spermatogenesis Vesicular Transport Proteins/genetics,metabolism
Chemicals
Actins Drosophila Proteins Vesicular Transport Proteins
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Sevrioukov Evgueni A
Center for Basic Neuroscience and Department of Cell Biology, University of Texas Southwestern Medical Center, Dallas, TX 75390-9111, USA.
Moghrabi Nabil
Kuhn Mary
Krämer Helmut
References (96)
96 references, click to expand
  1. A pathway for association of receptors, adaptors, and actin during endocytic internalization.
    Cell. 2003 Nov 14;115(4):475-87 PMID: 14622601
  2. Fusion between phagosomes, early and late endosomes: a role for actin in fusion between late, but not early endocytic organelles.
    Mol Biol Cell. 2004 Jan;15(1):345-58 PMID: 14617814
  3. Role of LBPA and Alix in multivesicular liposome formation and endosome organization.
    Science. 2004 Jan 23;303(5657):531-4 PMID: 14739459
  4. Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos.
    Mol Biol Cell. 2004 Feb;15(2):838-50 PMID: 14657248
  5. The biogenesis of multivesicular endosomes.
    Nat Rev Mol Cell Biol. 2004 Apr;5(4):317-23 PMID: 15071556
  6. Protein-protein interactions of ESCRT complexes in the yeast Saccharomyces cerevisiae.
    Traffic. 2004 Mar;5(3):194-210 PMID: 15086794
  7. 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
  8. 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
  9. A family of rhomboid-like genes: Drosophila rhomboid-1 and roughoid/rhomboid-3 cooperate to activate EGF receptor signaling.
    Genes Dev. 2000 Jul 1;14(13):1651-63 PMID: 10887159
  10. A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila.
    Mol Cell. 1999 Oct;4(4):479-86 PMID: 10549280
  11. Endocytic vesicles move at the tips of actin tails in cultured mast cells.
    Nat Cell Biol. 1999 May;1(1):72-4 PMID: 10559868
  12. GFP-tagged balancer chromosomes for Drosophila melanogaster.
    Mech Dev. 2000 Mar 1;91(1-2):451-4 PMID: 10704882
  13. Discontinuous actin hexagon, a protein essential for cortical furrow formation in Drosophila, is membrane associated and hyperphosphorylated.
    Mol Biol Cell. 2000 Mar;11(3):1011-22 PMID: 10712516
  14. The genome sequence of Drosophila melanogaster.
    Science. 2000 Mar 24;287(5461):2185-95 PMID: 10731132
  15. Distinct membrane domains on endosomes in the recycling pathway visualized by multicolor imaging of Rab4, Rab5, and Rab11.
    J Cell Biol. 2000 May 15;149(4):901-14 PMID: 10811830
  16. Functions of dystrophin and dystrophin associated proteins.
    Curr Opin Neurol. 1997 Oct;10(5):436-42 PMID: 9330892
  17. The AP-3 adaptor complex is essential for cargo-selective transport to the yeast vacuole.
    Cell. 1997 Oct 3;91(1):109-18 PMID: 9335339
  18. Nuclear-fallout, a Drosophila protein that cycles from the cytoplasm to the centrosomes, regulates cortical microfilament organization.
    Development. 1998 Apr;125(7):1295-303 PMID: 9477328
  19. The kinetics of mannose 6-phosphate receptor trafficking in the endocytic pathway in HEp-2 cells: the receptor enters and rapidly leaves multivesicular endosomes without accumulating in a prelysosomal compartment.
    Mol Biol Cell. 1998 Apr;9(4):809-16 PMID: 9529379
  20. Genetic dissection of sperm individualization in Drosophila melanogaster.
    Development. 1998 May;125(10):1833-43 PMID: 9550716
  21. Not just pretty eyes: Drosophila eye-colour mutations and lysosomal delivery.
    Trends Cell Biol. 1998 Jul;8(7):257-9 PMID: 9714595
  22. Protein traffic in the yeast endocytic and vacuolar protein sorting pathways.
    Curr Opin Cell Biol. 1998 Aug;10(4):513-22 PMID: 9719873
  23. Cellularization in Drosophila melanogaster is disrupted by the inhibition of rho activity and the activation of Cdc42 function.
    Dev Biol. 1998 Dec 1;204(1):151-64 PMID: 9851849
  24. Fab1p PtdIns(3)P 5-kinase function essential for protein sorting in the multivesicular body.
    Cell. 1998 Dec 11;95(6):847-58 PMID: 9865702
  25. Several levels of EGF receptor signaling during photoreceptor specification in wild-type, Ellipse, and null mutant Drosophila.
    Dev Biol. 1999 Jan 1;205(1):129-44 PMID: 9882502
  26. Genetic analysis of hook, a gene required for endocytic trafficking in drosophila.
    Genetics. 1999 Feb;151(2):675-84 PMID: 9927460
  27. Genetic dissection of endocytic trafficking in Drosophila using a horseradish peroxidase-bride of sevenless chimera: hook is required for normal maturation of multivesicular endosomes.
    Mol Biol Cell. 1999 Apr;10(4):847-59 PMID: 10198042
  28. A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype.
    Genetics. 1999 Aug;152(4):1631-9 PMID: 10430588
  29. The Drosophila centrosomal protein Nuf is required for recruiting Dah, a membrane associated protein, to furrows in the early embryo.
    J Cell Sci. 1999 Sep;112 ( Pt 17):2885-93 PMID: 10444383
  30. The Berkeley Drosophila Genome Project gene disruption project: Single P-element insertions mutating 25% of vital Drosophila genes.
    Genetics. 1999 Sep;153(1):135-77 PMID: 10471706
  31. Tsg101 is essential for cell growth, proliferation, and cell survival of embryonic and adult tissues.
    Mol Cell Biol. 2003 Jan;23(1):150-62 PMID: 12482969
  32. A Drosophila full-length cDNA resource.
    Genome Biol. 2002;3(12):RESEARCH0080 PMID: 12537569
  33. A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster.
    Development. 2003 May;130(9):1805-16 PMID: 12642486
  34. Role of ESCRT-I in retroviral budding.
    J Virol. 2003 Apr;77(8):4794-804 PMID: 12663786
  35. Defects in human immunodeficiency virus budding and endosomal sorting induced by TSG101 overexpression.
    J Virol. 2003 Jun;77(11):6507-19 PMID: 12743307
  36. TSG101 interaction with HRS mediates endosomal trafficking and receptor down-regulation.
    Proc Natl Acad Sci U S A. 2003 Jun 24;100(13):7626-31 PMID: 12802020
  37. Echinoid is essential for regulation of Egfr signaling and R8 formation during Drosophila eye development.
    Development. 2003 Aug;130(16):3725-33 PMID: 12835389
  38. Unequal segregation of Neuralized biases Notch activation during asymmetric cell division.
    Dev Cell. 2003 Jul;5(1):139-48 PMID: 12852858
  39. Arfophilins are dual Arf/Rab 11 binding proteins that regulate recycling endosome distribution and are related to Drosophila nuclear fallout.
    Mol Biol Cell. 2003 Jul;14(7):2908-20 PMID: 12857874
  40. Protein sorting into multivesicular endosomes.
    Curr Opin Cell Biol. 2003 Aug;15(4):446-55 PMID: 12892785
  41. Vps27 recruits ESCRT machinery to endosomes during MVB sorting.
    J Cell Biol. 2003 Aug 4;162(3):413-23 PMID: 12900393
  42. HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein.
    J Cell Biol. 2003 Aug 4;162(3):425-34 PMID: 12900394
  43. Hrs regulates multivesicular body formation via ESCRT recruitment to endosomes.
    J Cell Biol. 2003 Aug 4;162(3):435-42 PMID: 12900395
  44. The protein network of HIV budding.
    Cell. 2003 Sep 19;114(6):701-13 PMID: 14505570
  45. HIV's great escape.
    Nat Med. 2003 Oct;9(10):1262-3 PMID: 14520374
  46. Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11.
    J Cell Biol. 2003 Oct 13;163(1):143-54 PMID: 14530382
  47. EGF receptor signaling: putting a new spin on eye development.
    Curr Biol. 2003 Oct 14;13(20):R813-4 PMID: 14561424
  48. Distinct requirements for the AP-3 adaptor complex in pigment granule and synaptic vesicle biogenesis in Drosophila melanogaster.
    Mol Gen Genet. 2000 Jul;263(6):1003-14 PMID: 10954086
  49. p53 accumulation, defective cell proliferation, and early embryonic lethality in mice lacking tsg101.
    Proc Natl Acad Sci U S A. 2001 Feb 13;98(4):1859-64 PMID: 11172041
  50. A new visualization approach for identifying mutations that affect differentiation and organization of the Drosophila ommatidia.
    Development. 2001 Mar;128(6):815-26 PMID: 11222137
  51. Mammalian tumor susceptibility gene 101 (TSG101) and the yeast homologue, Vps23p, both function in late endosomal trafficking.
    Traffic. 2000 Mar;1(3):248-58 PMID: 11208108
  52. TSG101/mammalian VPS23 and mammalian VPS28 interact directly and are recruited to VPS4-induced endosomes.
    J Biol Chem. 2001 Apr 13;276(15):11735-42 PMID: 11134028
  53. 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
  54. The Drosophila JNK pathway controls the morphogenesis of the egg dorsal appendages and micropyle.
    Dev Biol. 2001 Sep 15;237(2):282-94 PMID: 11543614
  55. Late endosomes: sorting and partitioning in multivesicular bodies.
    Traffic. 2001 Sep;2(9):612-21 PMID: 11555415
  56. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding.
    Cell. 2001 Oct 5;107(1):55-65 PMID: 11595185
  57. Pmel17 initiates premelanosome morphogenesis within multivesicular bodies.
    Mol Biol Cell. 2001 Nov;12(11):3451-64 PMID: 11694580
  58. Rab11 polarization of the Drosophila oocyte: a novel link between membrane trafficking, microtubule organization, and oskar mRNA localization and translation.
    Development. 2002 Jan;129(2):517-26 PMID: 11807042
  59. Protein degradation: four E3s for the notch pathway.
    Curr Biol. 2002 Jan 22;12(2):R74-8 PMID: 11818085
  60. Hrs regulates endosome membrane invagination and tyrosine kinase receptor signaling in Drosophila.
    Cell. 2002 Jan 25;108(2):261-9 PMID: 11832215
  61. Mammalian class E vps proteins recognize ubiquitin and act in the removal of endosomal protein-ubiquitin conjugates.
    J Cell Biol. 2002 Apr 1;157(1):91-101 PMID: 11916981
  62. Sorting out signals in fly endosomes.
    Traffic. 2002 Feb;3(2):87-91 PMID: 11929598
  63. When cell biology meets development: endocytic regulation of signaling pathways.
    Genes Dev. 2002 Jun 1;16(11):1314-36 PMID: 12050111
  64. Membrane trafficking in Drosophila wing and eye development.
    Semin Cell Dev Biol. 2002 Apr;13(2):91-7 PMID: 12127141
  65. Genomic screen for vacuolar protein sorting genes in Saccharomyces cerevisiae.
    Mol Biol Cell. 2002 Jul;13(7):2486-501 PMID: 12134085
  66. Remodeling of organelle-bound actin is required for yeast vacuole fusion.
    J Cell Biol. 2002 Aug 19;158(4):669-79 PMID: 12177043
  67. Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting.
    Dev Cell. 2002 Aug;3(2):271-82 PMID: 12194857
  68. 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
  69. Targeted deletion of the Tsg101 gene results in cell cycle arrest at G1/S and p53-independent cell death.
    J Biol Chem. 2002 Nov 8;277(45):43216-23 PMID: 12205095
  70. Hsc70 is required for endocytosis and clathrin function in Drosophila.
    J Cell Biol. 2002 Nov 11;159(3):477-87 PMID: 12427870
  71. A role for myosin VI in actin dynamics at sites of membrane remodeling during Drosophila spermatogenesis.
    J Cell Sci. 2002 Dec 15;115(Pt 24):4855-65 PMID: 12432073
  72. Receptor downregulation and multivesicular-body sorting.
    Nat Rev Mol Cell Biol. 2002 Dec;3(12):893-905 PMID: 12461556
  73. The sevenless+ protein is expressed apically in cell membranes of developing Drosophila retina; it is not restricted to cell R7.
    Cell. 1987 Oct 9;51(1):151-8 PMID: 3115594
  74. Characterization and use of the Drosophila metallothionein promoter in cultured Drosophila melanogaster cells.
    Nucleic Acids Res. 1988 Feb 11;16(3):1043-61 PMID: 3125519
  75. A stable genomic source of P element transposase in Drosophila melanogaster.
    Genetics. 1988 Mar;118(3):461-70 PMID: 2835286
  76. Interaction of bride of sevenless membrane-bound ligand and the sevenless tyrosine-kinase receptor.
    Nature. 1991 Jul 18;352(6332):207-12 PMID: 1857416
  77. Retarded nuclear migration in Drosophila embryos with aberrant F-actin reorganization caused by maternal mutations and by cytochalasin treatment.
    Development. 1991 Apr;111(4):909-20 PMID: 1879360
  78. Intracellular sperm/egg interactions in Drosophila: a three-dimensional structural analysis of a paternal product in the developing egg.
    Mech Dev. 1991 Jun;34(2-3):101-11 PMID: 1911395
  79. Induction in the developing compound eye of Drosophila: multiple mechanisms restrict R7 induction to a single retinal precursor cell.
    Cell. 1991 Dec 20;67(6):1145-55 PMID: 1760842
  80. Actin and fimbrin are required for the internalization step of endocytosis in yeast.
    EMBO J. 1993 Jul;12(7):2855-62 PMID: 8335001
  81. Analysis of genetic mosaics in developing and adult Drosophila tissues.
    Development. 1993 Apr;117(4):1223-37 PMID: 8404527
  82. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes.
    Development. 1993 Jun;118(2):401-15 PMID: 8223268
  83. Delays in anaphase initiation occur in individual nuclei of the syncytial Drosophila embryo.
    Mol Biol Cell. 1993 Sep;4(9):885-96 PMID: 8257792
  84. How an actin network might cause fountain streaming and nuclear migration in the syncytial Drosophila embryo.
    J Cell Biol. 1994 Dec;127(6 Pt 1):1637-53 PMID: 7798318
  85. Drosophila nonmuscle myosin II is required for rapid cytoplasmic transport during oogenesis and for axial nuclear migration in early embryos.
    Development. 1995 Jun;121(6):1937-46 PMID: 7601006
  86. Relationships between complex Delta expression and the specification of retinal cell fates during Drosophila eye development.
    Mech Dev. 1995 Apr;50(2-3):201-16 PMID: 7619731
  87. Multivesicular endosomes containing internalized EGF-EGF receptor complexes mature and then fuse directly with lysosomes.
    J Cell Biol. 1996 Mar;132(6):1011-23 PMID: 8601581
  88. Mutations in the Drosophila hook gene inhibit endocytosis of the boss transmembrane ligand into multivesicular bodies.
    J Cell Biol. 1996 Jun;133(6):1205-15 PMID: 8682859
  89. Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis.
    J Cell Biol. 1996 Jul;134(1):133-48 PMID: 8698810
  90. Isolation and characterization of a Drosophila gene essential for early embryonic development and formation of cortical cleavage furrows.
    J Cell Biol. 1996 Aug;134(4):923-34 PMID: 8769417
  91. Multilamellar endosome-like compartment accumulates in the yeast vps28 vacuolar protein sorting mutant.
    Mol Biol Cell. 1996 Jun;7(6):985-99 PMID: 8817003
  92. Uncoupling cadherin-based adhesion from wingless signalling in Drosophila.
    Nature. 1996 Oct 17;383(6601):627-30 PMID: 8857539
  93. The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster.
    Genetics. 1996 Dec;144(4):1673-9 PMID: 8978054
  94. Altered expression of a novel adaptin leads to defective pigment granule biogenesis in the Drosophila eye color mutant garnet.
    EMBO J. 1997 Aug 1;16(15):4508-18 PMID: 9303295
  95. Actin assembly and endocytosis: from yeast to mammals.
    Annu Rev Cell Dev Biol. 2003;19:287-332 PMID: 14570572
  96. Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis.
    Curr Biol. 2003 Oct 28;13(21):1848-57 PMID: 14588240
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
Published
2005-05-00
Epub
2005-00-23
Pages
2301-12
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC1087236
Subset
IM
Grants
NEI NIH HHS · R01 EY010199 · United States
NINDS NIH HHS · R01 NS043406 · United States
NEI NIH HHS · EY-10199 · United States
NINDS NIH HHS · NS-43406 · United States
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