Home LiteratureArticle Details
PMID: 15166316 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Research Support, U.S. Gov't, P.H.S.

Dissection of the mammalian midbody proteome reveals conserved cytokinesis mechanisms.

Science (New York, N.Y.) ·Vol. 305 ·No. 5680 ·2004-07-02 ·Pages 61-6

Skop AR, Liu H, Yates J, Meyer BJ, Heald R

Abstract

Cytokinesis is the essential process that partitions cellular contents into daughter cells. To identify and characterize cytokinesis proteins rapidly, we used a functional proteomic and comparative genomic strategy. Midbodies were isolated from mammalian cells, proteins were identified by multidimensional protein identification technology (MudPIT), and protein function was assessed in Caenorhabditis elegans. Of 172 homologs disrupted by RNA interference, 58% displayed defects in cleavage furrow formation or completion, or germline cytokinesis. Functional dissection of the midbody demonstrated the importance of lipid rafts and vesicle trafficking pathways in cytokinesis, and the utilization of common membrane cytoskeletal components in diverse morphogenetic events in the cleavage furrow, the germline, and neurons.

MeSH Terms
Animals CHO Cells Caenorhabditis elegans/cytology,genetics,physiology Carrier Proteins/analysis,isolation & purification,physiology Cell Cycle/physiology Cell Division Cell Fractionation Cell Membrane/physiology Computational Biology Cricetinae Cytoskeletal Proteins/analysis,isolation & purification,physiology Cytoskeleton/physiology Germ Cells/physiology HeLa Cells Humans Membrane Microdomains/physiology Morphogenesis Organelles/chemistry,physiology Protein Transport Proteins/analysis,isolation & purification,physiology Proteome/analysis Proteomics Signal Transduction Spindle Apparatus/physiology,ultrastructure
Chemicals
Carrier Proteins Cytoskeletal Proteins Proteins Proteome
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Skop Ahna R
Department of Molecular and Cell Biology, University of California at Berkeley, Berkeley, CA 94720, USA. [email protected]
Liu Hongbin
Yates John
Meyer Barbara J
Heald Rebecca
References (65)
65 references, click to expand
  1. Reticuloplasmins: a novel group of proteins in the endoplasmic reticulum.
    J Cell Sci. 1987 May;87 ( Pt 4):491-2 PMID: 3308932
  2. Distribution of a matrix component of the midbody during the cell cycle in Chinese hamster ovary cells.
    J Cell Biol. 1988 Feb;106(2):431-9 PMID: 2448315
  3. Abnormal erythrocyte membrane cytoskeleton structure in chronic myelogenous leukaemia.
    Biochim Biophys Acta. 1988 Nov 22;945(2):121-6 PMID: 3191116
  4. Mitotic Golgi fragments in HeLa cells and their role in the reassembly pathway.
    J Cell Biol. 1989 Aug;109(2):463-74 PMID: 2503521
  5. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position.
    J Cell Biol. 1989 Sep;109(3):1185-93 PMID: 2768338
  6. Attachment of one spindle pole to the cortex in unequal cleavage.
    Ann N Y Acad Sci. 1990;582:108-19 PMID: 2192588
  7. Interblastomeric plasma membrane formation during cleavage of Xenopus laevis embryos.
    J Submicrosc Cytol Pathol. 1990 Jul;22(3):445-57 PMID: 2390768
  8. Analysis of the distribution of the INCENPs throughout mitosis reveals the existence of a pathway of structural changes in the chromosomes during metaphase and early events in cleavage furrow formation.
    J Cell Sci. 1991 Apr;98 ( Pt 4):443-61 PMID: 1860899
  9. Cytokinesis in higher plants.
    Cell. 1996 Mar 22;84(6):821-4 PMID: 8601305
  10. Differential translocation of rho family GTPases by lysophosphatidic acid, endothelin-1, and platelet-derived growth factor.
    J Biol Chem. 1996 Dec 20;271(51):33067-73 PMID: 8955154
  11. Functional rafts in cell membranes.
    Nature. 1997 Jun 5;387(6633):569-72 PMID: 9177342
  12. Expression of a minus-end-directed motor protein induces Sf9 cells to form axon-like processes with uniform microtubule polarity orientation.
    J Cell Sci. 1997 Oct;110 ( Pt 19):2373-80 PMID: 9410876
  13. Cytokinesis: IQGAPs find a function.
    Curr Biol. 1998 Mar 12;8(6):R202-5 PMID: 9512410
  14. Iqg1p, a yeast homologue of the mammalian IQGAPs, mediates cdc42p effects on the actin cytoskeleton.
    J Cell Biol. 1998 Jul 27;142(2):443-55 PMID: 9679143
  15. The dynactin complex is required for cleavage plane specification in early Caenorhabditis elegans embryos.
    Curr Biol. 1998 Oct 8;8(20):1110-6 PMID: 9778526
  16. Molecular aspects of Huntington's disease.
    J Neurosci Res. 1998 Nov 1;54(3):301-8 PMID: 9819135
  17. Direct analysis of protein complexes using mass spectrometry.
    Nat Biotechnol. 1999 Jul;17(7):676-82 PMID: 10404161
  18. Evidence for the involvement of KIF4 in the anterograde transport of L1-containing vesicles.
    J Cell Biol. 2000 Apr 3;149(1):141-52 PMID: 10747093
  19. Cytokinesis: lessons from rappaport and the Drosophila blastoderm embryo.
    Cell Biol Int. 1999;23(12):871-6 PMID: 10772762
  20. A C. elegans patched gene, ptc-1, functions in germ-line cytokinesis.
    Genes Dev. 2000 Aug 1;14(15):1933-44 PMID: 10921907
  21. Annexins in cell membrane dynamics. Ca(2+)-regulated association of lipid microdomains.
    J Cell Biol. 2000 Sep 4;150(5):1113-24 PMID: 10973999
  22. Bim1p/Yeb1p mediates the Kar9p-dependent cortical attachment of cytoplasmic microtubules.
    Mol Biol Cell. 2000 Sep;11(9):2949-59 PMID: 10982392
  23. Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells.
    Plant Physiol. 2000 Sep;124(1):135-51 PMID: 10982429
  24. Functional genomic analysis of C. elegans chromosome I by systematic RNA interference.
    Nature. 2000 Nov 16;408(6810):325-30 PMID: 11099033
  25. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III.
    Nature. 2000 Nov 16;408(6810):331-6 PMID: 11099034
  26. INCENP binds directly to tubulin and requires dynamic microtubules to target to the cleavage furrow.
    Exp Cell Res. 2001 Jan 15;262(2):122-7 PMID: 11139336
  27. RNAi analysis of genes expressed in the ovary of Caenorhabditis elegans.
    Curr Biol. 2000 Dec 14-28;10(24):1619-22 PMID: 11137018
  28. Raft-partitioning of the ubiquitin ligases Cbl and Nedd4 upon IgE-triggered cell signaling.
    Proc Natl Acad Sci U S A. 2001 Mar 13;98(6):3180-4 PMID: 11248052
  29. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi.
    Curr Biol. 2001 Feb 6;11(3):171-6 PMID: 11231151
  30. Distinct roles for Galpha and Gbetagamma in regulating spindle position and orientation in Caenorhabditis elegans embryos.
    Nat Cell Biol. 2001 Mar;3(3):297-300 PMID: 11231580
  31. Rkp1/Cpc2, a fission yeast RACK1 homolog, is involved in actin cytoskeleton organization through protein kinase C, Pck2, signaling.
    Biochem Biophys Res Commun. 2001 Mar 23;282(1):10-5 PMID: 11263963
  32. SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis.
    EMBO J. 2001 May 1;20(9):2202-13 PMID: 11331586
  33. Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex.
    Curr Biol. 2001 May 15;11(10):735-46 PMID: 11378383
  34. Walther Flemming: pioneer of mitosis research.
    Nat Rev Mol Cell Biol. 2001 Jan;2(1):72-5 PMID: 11413469
  35. Roles of lipid rafts in membrane transport.
    Curr Opin Cell Biol. 2001 Aug;13(4):470-7 PMID: 11454454
  36. MYO6, the human homologue of the gene responsible for deafness in Snell's waltzer mice, is mutated in autosomal dominant nonsyndromic hearing loss.
    Am J Hum Genet. 2001 Sep;69(3):635-40 PMID: 11468689
  37. Cytoskeletal mechanisms of neuronal degeneration.
    Cell Tissue Res. 2001 Aug;305(2):255-65 PMID: 11545263
  38. Animal cell cytokinesis.
    Annu Rev Cell Dev Biol. 2001;17:351-86 PMID: 11687493
  39. Molecular machinery involved in the insulin-regulated fusion of GLUT4-containing vesicles with the plasma membrane (review).
    Mol Membr Biol. 2001 Oct-Dec;18(4):237-45 PMID: 11780752
  40. Aberrant expression of signaling-related proteins 14-3-3 gamma and RACK1 in fetal Down syndrome brain (trisomy 21).
    Electrophoresis. 2002 Jan;23(1):152-7 PMID: 11824616
  41. A human homologue of Drosophila kelch associates with myosin-VIIa in specialized adhesion junctions.
    Cell Motil Cytoskeleton. 2002 Mar;51(3):147-64 PMID: 11921171
  42. Studies in fission yeast on mechanisms of cell division site placement.
    Cell Struct Funct. 2001 Dec;26(6):539-44 PMID: 11942607
  43. A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility.
    Nat Cell Biol. 2002 Jun;4(6):399-407 PMID: 12032545
  44. Kinesin-like protein CHO1 is required for the formation of midbody matrix and the completion of cytokinesis in mammalian cells.
    Mol Biol Cell. 2002 Jun;13(6):1832-45 PMID: 12058052
  45. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone.
    J Cell Biol. 2002 Jun 24;157(7):1175-86 PMID: 12082078
  46. Membrane trafficking during plant cytokinesis.
    Traffic. 2002 Sep;3(9):621-9 PMID: 12191014
  47. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits.
    Nat Cell Biol. 2002 Sep;4(9):691-8 PMID: 12198492
  48. Furrow-specific endocytosis during cytokinesis of zebrafish blastomeres.
    Exp Cell Res. 2002 Sep 10;279(1):14-20 PMID: 12213209
  49. Three-dimensional fibroblast-tumor cell interaction causes downregulation of RACK1 mRNA expression in breast cancer cells in vitro.
    Int J Cancer. 2002 Nov 10;102(2):129-36 PMID: 12385007
  50. The vesicle- and target-SNARE proteins that mediate Glut4 vesicle fusion are localized in detergent-insoluble lipid rafts present on distinct intracellular membranes.
    J Biol Chem. 2002 Dec 20;277(51):49750-4 PMID: 12376543
  51. The large GTPase dynamin associates with the spindle midzone and is required for cytokinesis.
    Curr Biol. 2002 Dec 23;12(24):2111-7 PMID: 12498685
  52. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi.
    Nature. 2003 Jan 16;421(6920):231-7 PMID: 12529635
  53. Sterol-rich plasma membrane domains in the fission yeast Schizosaccharomyces pombe.
    J Cell Sci. 2003 Mar 1;116(Pt 5):867-74 PMID: 12571284
  54. Calcyclin (S100A6) regulates pulmonary fibroblast proliferation, morphology, and cytoskeletal organization in vitro.
    J Cell Biochem. 2003 Mar 1;88(4):848-54 PMID: 12577318
  55. Monocyte lipid rafts contain proteins implicated in vesicular trafficking and phagosome formation.
    Proteomics. 2003 Apr;3(4):536-48 PMID: 12687620
  56. Role for NudC, a dynein-associated nuclear movement protein, in mitosis and cytokinesis.
    J Cell Sci. 2003 May 15;116(Pt 10):1991-2003 PMID: 12679384
  57. Citron kinase is a regulator of mitosis and neurogenic cytokinesis in the neocortical ventricular zone.
    Cereb Cortex. 2003 Jun;13(6):588-91 PMID: 12764032
  58. Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells.
    Proc Natl Acad Sci U S A. 2003 Jul 8;100(14):8241-6 PMID: 12826615
  59. Protein disregulation in red blood cell membranes of type 2 diabetic patients.
    Biochem Biophys Res Commun. 2003 Sep 12;309(1):196-200 PMID: 12943682
  60. Accumulation of flotillin-1 in tangle-bearing neurones of Alzheimer's disease.
    Neuropathol Appl Neurobiol. 2003 Oct;29(5):451-61 PMID: 14507337
  61. The cellular geography of aurora kinases.
    Nat Rev Mol Cell Biol. 2003 Nov;4(11):842-54 PMID: 14625535
  62. Microtubule-targeted anticancer agents and apoptosis.
    Oncogene. 2003 Dec 8;22(56):9075-86 PMID: 14663486
  63. Fine-structural studies of the gametes and embryo of Fucus vesiculosus L. (Phaeophyta). III. Cytokinesis and the multicellular embryo.
    J Cell Sci. 1977 Apr;24:275-94 PMID: 893547
  64. Valve morphogenesis and the microtubule center of the diatom Hantzschia amphioxys.
    Eur J Cell Biol. 1981 Aug;25(1):150-70 PMID: 7285949
  65. Isolation and initial characterization of the mammalian midbody.
    J Cell Biol. 1982 Sep;94(3):654-61 PMID: 7130277
Article Info
Journal
Science (New York, N.Y.)
Abbr.
Science
ISSN
1095-9203
Published
2004-07-02
Epub
2004-00-27
Pages
61-6
Language
English
Region
United States
NLM ID
0404511
PMCID
PMC3679889
Subset
IM
Grants
NIGMS NIH HHS · F32 GM064159-02 · United States
NIGMS NIH HHS · F32 GM064159-03 · United States
NCRR NIH HHS · P41 RR011823 · United States
NIGMS NIH HHS · F32 GM064159-01 · United States
NIGMS NIH HHS · F32 GM64159-01 · United States
NCRR NIH HHS · RR1823 · United States
NIGMS NIH HHS · F32 GM064159 · United States
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: [email protected]