Home LiteratureArticle Details
PMID: 11378383 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Completion of cytokinesis in C. elegans requires a brefeldin A-sensitive membrane accumulation at the cleavage furrow apex.

Current biology : CB ·Vol. 11 ·No. 10 ·2001-05-15 ·Pages 735-46

Skop AR, Bergmann D, Mohler WA, White JG

Abstract

The terminal phase of cytokinesis in eukaryotic cells involves breakage of the intercellular canal containing the spindle midzone and resealing of the daughter cells. Recent observations suggest that the spindle midzone is required for this process. In this study, we investigated the possibility that targeted secretion in the vicinity of the spindle midzone is required for the execution of the terminal phase of cytokinesis. We inhibited secretion in early C. elegans embryos by treatment with brefeldin A (BFA). Using 4D recordings of dividing cells, we showed that BFA induced stereotyped failures in the terminal phase of cytokinesis; although the furrow ingressed normally, after a few minutes the furrow completely regressed, even though spindle midzone and midbody microtubules appeared normal. In addition, using an FM1-43 membrane probe, we found that membrane accumulated locally at the apices of the late cleavage furrows that form the persisting intercellular canals between daughter cells. However, in BFA-treated embryos this membrane accumulation did not occur, which possibly accounts for the observed cleavage failures. We have shown that BFA disrupts the terminal phase of cytokinesis in the embryonic blastomeres of C. elegans. We observed that membrane accumulates at the apices of the late cleavage furrow by means of a BFA-sensitive mechanism. We suggest that this local membrane accumulation is necessary for the completion of cytokinesis and speculate that the spindle midzone region of animal cells is functionally equivalent to the phragmoplast of plants and acts to target secretion to the equatorial plane of a cleaving cell.

MeSH Terms
Animals Blastomeres/drug effects Brefeldin A/pharmacology Caenorhabditis elegans/embryology Cell Cycle/drug effects Cell Membrane/drug effects,metabolism Embryo, Nonmammalian/cytology Spindle Apparatus
Chemicals
Brefeldin A
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Skop A R
Laboratory of Molecular Biology, University of Colorado, Boulder, CO 80309, USA.
Bergmann D
Mohler W A
White J G
References (75)
75 references, click to expand
  1. Rab11 is required for trans-golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor.
    Mol Biol Cell. 1998 Nov;9(11):3241-57 PMID: 9802909
  2. Role of xklp3, a subunit of the Xenopus kinesin II heterotrimeric complex, in membrane transport between the endoplasmic reticulum and the Golgi apparatus.
    J Cell Biol. 1998 Dec 14;143(6):1559-73 PMID: 9852151
  3. AIR-2: An Aurora/Ipl1-related protein kinase associated with chromosomes and midbody microtubules is required for polar body extrusion and cytokinesis in Caenorhabditis elegans embryos.
    J Cell Biol. 1998 Dec 14;143(6):1635-46 PMID: 9852156
  4. Direct interaction of microtubule- and actin-based transport motors.
    Nature. 1999 Jan 21;397(6716):267-70 PMID: 9930703
  5. The mechanism of facilitated cell membrane resealing.
    J Cell Sci. 1999 Mar;112 ( Pt 5):719-31 PMID: 9973606
  6. Molecular cloning and functional characterization of brefeldin A-ADP-ribosylated substrate. A novel protein involved in the maintenance of the Golgi structure.
    J Biol Chem. 1999 Jun 18;274(25):17705-10 PMID: 10364211
  7. Depletion of syntaxins in the early Caenorhabditis elegans embryo reveals a role for membrane fusion events in cytokinesis.
    Curr Biol. 1999 Jul 15;9(14):738-45 PMID: 10421575
  8. Syntaxin is required for cell division.
    Mol Biol Cell. 1999 Aug;10(8):2735-43 PMID: 10436024
  9. Wnt pathway components orient a mitotic spindle in the early Caenorhabditis elegans embryo without requiring gene transcription in the responding cell.
    Genes Dev. 1999 Aug 1;13(15):2028-38 PMID: 10444600
  10. Microtubules are required for completion of cytokinesis in sea urchin eggs.
    Dev Biol. 1999 Oct 1;214(1):215-26 PMID: 10491270
  11. Cytoplasmic dynein is required for distinct aspects of MTOC positioning, including centrosome separation, in the one cell stage Caenorhabditis elegans embryo.
    J Cell Biol. 1999 Oct 4;147(1):135-50 PMID: 10508861
  12. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles.
    J Neurosci. 1997 Nov 1;17(21):8061-73 PMID: 9334382
  13. The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting.
    J Cell Biol. 1999 Nov 15;147(4):791-808 PMID: 10562281
  14. Divide and conquer: cytokinesis in plant cells.
    Curr Opin Plant Biol. 1999 Dec;2(6):447-53 PMID: 10607656
  15. Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system.
    Nat Cell Biol. 2000 Jan;2(1):7-12 PMID: 10620800
  16. Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane.
    J Cell Biol. 2000 Jan 10;148(1):45-58 PMID: 10629217
  17. Polarization of cell growth in yeast.
    J Cell Sci. 2000 Feb;113 ( Pt 4):571-85 PMID: 10652251
  18. Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP.
    J Cell Biol. 2000 Feb 7;148(3):519-30 PMID: 10662777
  19. Role of actin and Myo2p in polarized secretion and growth of Saccharomyces cerevisiae.
    Mol Biol Cell. 2000 May;11(5):1727-37 PMID: 10793147
  20. CYK-4: A Rho family gtpase activating protein (GAP) required for central spindle formation and cytokinesis.
    J Cell Biol. 2000 Jun 26;149(7):1391-404 PMID: 10871280
  21. Incenp and an aurora-like kinase form a complex essential for chromosome segregation and efficient completion of cytokinesis.
    Curr Biol. 2000 Oct 5;10(19):1172-81 PMID: 11050385
  22. The Rab6-binding kinesin, Rab6-KIFL, is required for cytokinesis.
    EMBO J. 2000 Nov 1;19(21):5711-9 PMID: 11060022
  23. Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization.
    J Cell Biol. 2000 Nov 13;151(4):905-18 PMID: 11076973
  24. Centrosome-dependent exit of cytokinesis in animal cells.
    Science. 2001 Feb 23;291(5508):1550-3 PMID: 11222861
  25. Spindle dynamics and the role of gamma-tubulin in early Caenorhabditis elegans embryos.
    Mol Biol Cell. 2001 Jun;12(6):1751-64 PMID: 11408582
  26. The genetics of Caenorhabditis elegans.
    Genetics. 1974 May;77(1):71-94 PMID: 4366476
  27. Isolation and initial characterization of the mammalian midbody.
    J Cell Biol. 1982 Sep;94(3):654-61 PMID: 7130277
  28. The embryonic cell lineage of the nematode Caenorhabditis elegans.
    Dev Biol. 1983 Nov;100(1):64-119 PMID: 6684600
  29. Midbody sealing after cytokinesis in embryos of the sea urchin Arabacia punctulata.
    Cell Tissue Res. 1985;240(2):287-92 PMID: 3995553
  30. Determination of cell division axes in the early embryogenesis of Caenorhabditis elegans.
    J Cell Biol. 1987 Nov;105(5):2123-35 PMID: 3680373
  31. 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
  32. Cleavage plane determination in amphibian eggs.
    Ann N Y Acad Sci. 1990;582:40-9 PMID: 2356982
  33. Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae.
    Cell. 1991 Mar 22;64(6):1183-95 PMID: 2004424
  34. Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences.
    EMBO J. 1991 Dec;10(12):3959-70 PMID: 1935914
  35. Beta 1-integrin is a maternal protein that is inserted into all newly formed plasma membranes during early Xenopus embryogenesis.
    Development. 1992 Jun;115(2):595-605 PMID: 1385064
  36. Inhibition by brefeldin A of a Golgi membrane enzyme that catalyses exchange of guanine nucleotide bound to ARF.
    Nature. 1992 Nov 26;360(6402):352-4 PMID: 1448152
  37. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons.
    Neuron. 1993 Oct;11(4):713-24 PMID: 8398156
  38. Rab8, a small GTPase involved in vesicular traffic between the TGN and the basolateral plasma membrane.
    J Cell Biol. 1993 Oct;123(1):35-45 PMID: 8408203
  39. Cell membrane resealing by a vesicular mechanism similar to neurotransmitter release.
    Science. 1994 Jan 21;263(5145):390-3 PMID: 7904084
  40. Transient localized accumulation of actin in Caenorhabditis elegans blastomeres with oriented asymmetric divisions.
    Development. 1994 Aug;120(8):2317-28 PMID: 7925032
  41. Heterogeneity and microtubule interaction of the CHO1 antigen, a mitosis-specific kinesin-like protein. Analysis of subdomains expressed in insect sf9 cells.
    J Cell Sci. 1994 Dec;107 ( Pt 12):3485-99 PMID: 7706400
  42. The Drosophila kinesin-like protein KLP3A is a midbody component required for central spindle assembly and initiation of cytokinesis.
    J Cell Biol. 1995 May;129(3):709-23 PMID: 7730406
  43. Cell contacts orient some cell division axes in the Caenorhabditis elegans embryo.
    J Cell Biol. 1995 May;129(4):1071-80 PMID: 7744956
  44. Actin- and microtubule-dependent organelle motors: interrelationships between the two motility systems.
    Curr Opin Cell Biol. 1995 Feb;7(1):82-8 PMID: 7755993
  45. Effects of brefeldin A on the formation of the cell plate in tobacco BY-2 cells.
    Eur J Cell Biol. 1995 Mar;66(3):274-81 PMID: 7539746
  46. Fluorescent conjugates of brefeldin A selectively stain the endoplasmic reticulum and Golgi complex of living cells.
    J Histochem Cytochem. 1995 Sep;43(9):907-15 PMID: 7543914
  47. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product.
    Cell. 1996 Jan 12;84(1):61-71 PMID: 8548827
  48. Phragmoplastin, a dynamin-like protein associated with cell plate formation in plants.
    EMBO J. 1996 Feb 15;15(4):695-704 PMID: 8631291
  49. Cytokinesis in higher plants.
    Cell. 1996 Mar 22;84(6):821-4 PMID: 8601305
  50. A kinesin-like protein, KatAp, in the cells of arabidopsis and other plants.
    Plant Cell. 1996 Jan;8(1):119-132 PMID: 8597656
  51. Time-dependent responses to glp-1-mediated inductions in early C. elegans embryos.
    Development. 1996 Jul;122(7):2043-50 PMID: 8681785
  52. Four-dimensional imaging: computer visualization of 3D movements in living specimens.
    Science. 1996 Aug 2;273(5275):603-7 PMID: 8662545
  53. The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes.
    Development. 1996 Sep;122(9):2623-30 PMID: 8787737
  54. Rab8 promotes polarized membrane transport through reorganization of actin and microtubules in fibroblasts.
    J Cell Biol. 1996 Oct;135(1):153-67 PMID: 8858170
  55. Midzone microtubule bundles are continuously required for cytokinesis in cultured epithelial cells.
    J Cell Biol. 1996 Nov;135(4):981-9 PMID: 8922381
  56. Dynamics of phragmoplastin in living cells during cell plate formation and uncoupling of cell elongation from the plane of cell division.
    Plant Cell. 1997 Feb;9(2):157-69 PMID: 9061948
  57. Chromosomal proteins and cytokinesis: patterns of cleavage furrow formation and inner centromere protein positioning in mitotic heterokaryons and mid-anaphase cells.
    J Cell Biol. 1997 Mar 24;136(6):1169-83 PMID: 9087435
  58. The synaptic protein syntaxin1 is required for cellularization of Drosophila embryos.
    J Cell Biol. 1997 Aug 25;138(4):861-75 PMID: 9265652
  59. Kinesin- and myosin-driven steps of vesicle recruitment for Ca2+-regulated exocytosis.
    J Cell Biol. 1997 Sep 8;138(5):999-1008 PMID: 9281579
  60. Wnt signaling polarizes an early C. elegans blastomere to distinguish endoderm from mesoderm.
    Cell. 1997 Aug 22;90(4):695-705 PMID: 9288749
  61. Wnt signaling and an APC-related gene specify endoderm in early C. elegans embryos.
    Cell. 1997 Aug 22;90(4):707-16 PMID: 9288750
  62. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin.
    J Cell Biol. 1997 Dec 15;139(6):1485-93 PMID: 9396754
  63. The mechanism and control of cytokinesis.
    Curr Opin Cell Biol. 1997 Dec;9(6):815-23 PMID: 9425346
  64. Interaction of a Golgi-associated kinesin-like protein with Rab6.
    Science. 1998 Jan 23;279(5350):580-5 PMID: 9438855
  65. Requirement for microtubules in new membrane formation during cytokinesis of Xenopus embryos.
    Dev Biol. 1998 Feb 1;194(1):47-60 PMID: 9473331
  66. pavarotti encodes a kinesin-like protein required to organize the central spindle and contractile ring for cytokinesis.
    Genes Dev. 1998 May 15;12(10):1483-94 PMID: 9585508
  67. Stereo-4-D reconstruction and animation from living fluorescent specimens.
    Biotechniques. 1998 Jun;24(6):1006-10, 1012 PMID: 9631195
  68. cyk-1: a C. elegans FH gene required for a late step in embryonic cytokinesis.
    J Cell Sci. 1998 Jul 30;111 ( Pt 14):2017-27 PMID: 9645949
  69. A genetic screen for temperature-sensitive cell-division mutants of Caenorhabditis elegans.
    Genetics. 1998 Jul;149(3):1303-21 PMID: 9649522
  70. Cytokinesis and midzone microtubule organization in Caenorhabditis elegans require the kinesin-like protein ZEN-4.
    Mol Biol Cell. 1998 Aug;9(8):2037-49 PMID: 9693365
  71. Involvement of an actomyosin contractile ring in Saccharomyces cerevisiae cytokinesis.
    J Cell Biol. 1998 Sep 7;142(5):1301-12 PMID: 9732290
  72. Multiphoton excitation provides optical sections from deeper within scattering specimens than confocal imaging.
    Biophys J. 1998 Oct;75(4):2015-24 PMID: 9746543
  73. Dynamics and ultrastructure of developmental cell fusions in the Caenorhabditis elegans hypodermis.
    Curr Biol. 1998 Sep 24;8(19):1087-90 PMID: 9768364
  74. 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
  75. A nematode kinesin required for cleavage furrow advancement.
    Curr Biol. 1998 Oct 8;8(20):1133-6 PMID: 9778533
Article Info
Journal
Current biology : CB
Abbr.
Curr Biol
ISSN
0960-9822
Published
2001-05-15
Pages
735-46
Language
English
Region
England
NLM ID
9107782
PMCID
PMC3733387
Subset
IM
Grants
NIGMS NIH HHS · F32 GM064159 · United States
NIGMS NIH HHS · R01 GM052454 · United States
NIGMS NIH HHS · R01 GM057583 · United States
NIGMS NIH HHS · GM-52454 · 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]