Home LiteratureArticle Details
PMID: 7896879 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Microtubule polarity and dynamics in the control of organelle positioning, segregation, and cytokinesis in the trypanosome cell cycle.

The Journal of cell biology ·Vol. 128 ·No. 6 ·1995-03-00 ·Pages 1163-72

Robinson DR, Sherwin T, Ploubidou A, Byard EH, Gull K

Abstract

Trypanosoma brucei has a precisely ordered microtubule cytoskeleton whose morphogenesis is central to cell cycle events such as organelle positioning, segregation, mitosis, and cytokinesis. We have defined microtubule polarity and show the + ends of the cortical microtubules to be at the posterior end of the cell. Measurements of organelle positions through the cell cycle reveal a high degree of coordinate movement and a relationship with overall cell extension. Quantitative analysis of the segregation of the replicated mitochondrial genome (the kinetoplast) by the flagellar basal bodies identifies a new G2 cell cycle event marker. The subsequent mitosis then positions one "daughter" nucleus into the gap between the segregated basal bodies/kinetoplasts. The anterior daughter nucleus maintains its position relative to the anterior of the cell, suggesting an effective yet cryptic nuclear positioning mechanism. Inhibition of microtubule dynamics by rhizoxin results in a phenomenon whereby cells, which have segregated their kinetoplasts yet are compromised in mitosis, cleave into a nucleated portion and a flagellated, anucleate, cytoplast. We term these cytoplasts "zoids" and show that they contain the posterior (new) flagellum and associated basal-body/kinetoplast complex. Examination of zoids suggests a role for the flagellum attachment zone (FAZ) in defining the position for the axis of cleavage in trypanosomes. Progression through cytokinesis, (zoid formation) while mitosis is compromised, suggests that the dependency relationships leading to the classical cell cycle check points may be altered in trypanosomes, to take account of the need to segregate two unit genomes (nuclear and mitochondrial) in this cell.

MeSH Terms
Animals Cell Cycle Cell Division Microtubules/ultrastructure Trypanosoma brucei brucei/cytology,ultrastructure
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Robinson D R
School of Biological Sciences, University of Manchester, United Kingdom.
Sherwin T
Ploubidou A
Byard E H
Gull K
References (24)
24 references, click to expand
  1. Inhibition by griseofulvin of microtubule assembly in vitro.
    FEBS Lett. 1976 Sep 1;67(3):248-51 PMID: 964356
  2. A repetitive protein from Trypanosoma brucei which caps the microtubules at the posterior end of the cytoskeleton.
    Mol Biochem Parasitol. 1993 Mar;58(1):83-96 PMID: 8459837
  3. Head-to-tail polymerization of microtubules in vitro. Electron microscope analysis of seeded assembly.
    J Cell Biol. 1980 Jan;84(1):141-50 PMID: 7350166
  4. Polarity of microtubules nucleated by centrosomes and chromosomes of Chinese hamster ovary cells in vitro.
    J Cell Biol. 1980 Jan;84(1):151-9 PMID: 7350167
  5. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication.
    Acta Trop. 1979 Sep;36(3):289-92 PMID: 43092
  6. Visualization of the structural polarity of microtubules.
    Nature. 1980 Jul 31;286(5772):517-9 PMID: 7402333
  7. Polarity of axoplasmic microtubules in the olfactory nerve of the frog.
    Proc Natl Acad Sci U S A. 1981 May;78(5):3269-73 PMID: 6973153
  8. Rat monoclonal antitubulin antibodies derived by using a new nonsecreting rat cell line.
    J Cell Biol. 1982 Jun;93(3):576-82 PMID: 6811596
  9. Amino acid sequence requirements in the epitope recognized by the alpha-tubulin-specific rat monoclonal antibody YL 1/2.
    EMBO J. 1984 Jun;3(6):1295-300 PMID: 6204858
  10. Spatial organization of axonal microtubules.
    J Cell Biol. 1984 Oct;99(4 Pt 1):1289-95 PMID: 6480693
  11. Rhizoxin, a macrocyclic lactone antibiotic, as a new antitumor agent against human and murine tumor cells and their vincristine-resistant sublines.
    Cancer Res. 1986 Jan;46(1):381-5 PMID: 3753552
  12. Distinct localization and cell cycle dependence of COOH terminally tyrosinolated alpha-tubulin in the microtubules of Trypanosoma brucei brucei.
    J Cell Biol. 1987 Mar;104(3):439-46 PMID: 3546334
  13. Structure and transcription of the actin gene of Trypanosoma brucei.
    Mol Cell Biol. 1988 May;8(5):2166-76 PMID: 3386635
  14. Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite.
    Proc Natl Acad Sci U S A. 1988 Nov;85(21):8335-9 PMID: 3054884
  15. Replication of kinetoplast DNA in trypanosomes.
    Annu Rev Microbiol. 1988;42:339-58 PMID: 2849370
  16. Visualization of detyrosination along single microtubules reveals novel mechanisms of assembly during cytoskeletal duplication in trypanosomes.
    Cell. 1989 Apr 21;57(2):211-21 PMID: 2649249
  17. Improved separation of chromosome-sized DNA from Trypanosoma brucei, stock 427-60.
    Nucleic Acids Res. 1989 Apr 25;17(8):3217-27 PMID: 2726456
  18. The cell division cycle of Trypanosoma brucei brucei: timing of event markers and cytoskeletal modulations.
    Philos Trans R Soc Lond B Biol Sci. 1989 Jun 12;323(1218):573-88 PMID: 2568647
  19. Definition of individual components within the cytoskeleton of Trypanosoma brucei by a library of monoclonal antibodies.
    J Cell Sci. 1989 Jul;93 ( Pt 3):491-500 PMID: 2606940
  20. Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei.
    J Cell Sci. 1990 Jan;95 ( Pt 1):49-57 PMID: 2190996
  21. Microtubule polarity determination based on formation of protofilament hooks.
    Methods Enzymol. 1991;196:469-77 PMID: 2034135
  22. The cytoskeletal architecture of Trypanosoma brucei.
    J Parasitol. 1991 Aug;77(4):603-12 PMID: 1865269
  23. Basal body movements as a mechanism for mitochondrial genome segregation in the trypanosome cell cycle.
    Nature. 1991 Aug 22;352(6337):731-3 PMID: 1876188
  24. Opposite end assembly and disassembly of microtubules at steady state in vitro.
    Cell. 1978 Jan;13(1):1-8 PMID: 620419
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1995-03-00
Pages
1163-72
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2120423
Subset
IM
Grants
Wellcome Trust · 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: [email protected]