Skip to main content
Log in

Checkpoint control in crane-fly spermatocytes: unattached chromosomes induced by cytochalasin D or latrunculin treatment do not prevent or delay the start of anaphase

  • Original Papers
  • Published:
Protoplasma Aims and scope Submit manuscript

Summary

Variable numbers of bivalents and sex chromosomes do not attach to the spindle when prophase or early prometaphase cranefly spermatocytes (2n=8) are treated with cytochalasin D or latrunculin. The unattached bivalents lie in the cytoplasm or at the spindle pole, and they do not delay onset of autosomal anaphase; sometimes they disjoin at the same time as the attached bivalents, so they respond to the global signals that initiate anaphase. Unattached sex chromosomes do not delay autosomal anaphase, either. Of various interpretations of these data, we think the best explanation is that the checkpoint system responds to physical rather than chemical cues; we think that the spindle is a “tensegral” structure, that chromosomes need to interact with the spindle in order to be recognised by the anaphase-onset “checkpoint control”, and that the physical interaction of chromosomes with spindle acts as a signalling network. Cytochalasin D and latrunculin treatments delay onset of sex chromosome anaphase (which normally occurs about 15 min after autosomal anaphase) and cause altered patterns of sex-chromosome segregation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Adames KA, Forer A (1996) Evidence for poleward forces on chromosome arms during anaphase. Cell Motil Cytoskeleton 34: 13–25

    CAS  PubMed  Google Scholar 

  • Callaini G, Dallai R, Riparbelli MG (1997) Wolbachia-induced delay of paternal chromatin condensation does not prevent maternal chromosomes from entering anaphase in incompatible crosses of Drosophila stimulans. J Cell Sci 110: 271–280

    CAS  PubMed  Google Scholar 

  • Campbell MS, Gorbsky GJ (1995) Microinjection of mitotic cells with the 3F3/2 anti-phosphoepitope antibody delays the onset of anaphase. J Cell Biol 129: 1195–1204

    CAS  PubMed  Google Scholar 

  • Dietz R (1956) Die Spermatocytenteilungen der Tipuliden II: graphische Analyse der Chromosomenbewegung während der Prometaphase I im Leben. Chromosoma 8: 183–211

    Google Scholar 

  • Dietz R (1969) Bau und Funktion des Spindelapparats. Naturwissenschaften 56: 237–248

    CAS  PubMed  Google Scholar 

  • — (1972) Die Assembly-Hypothese der Chromosomenbewegung und die Veränderungen der Spindellänge während der Anaphase I in Spermatocyten von Pales ferruginea (Tipulidae, Diptera). Chromosoma 38: 11–76

    CAS  PubMed  Google Scholar 

  • Forer A (1972) A method for making preparations of living crane fly spermatocytes for study with light microscopy followed by electron microscopy. Cytobiologie 6: 403–409

    Google Scholar 

  • — (1980) Chromosome movements in the meiosis of insects, especially crane-fly spermatocytes. In: Blackman RL, Hewitt GM, Ashburner M (ed) Insect cytogenetics. Blackwell, Oxford, pp 85–95

    Google Scholar 

  • — (1982) Crane fly spermatocytes and spermatids: a system for studying cytoskeletal components. Methods Cell Biol 25: 227–252

    PubMed  Google Scholar 

  • —, Koch C (1973) Influence of autosome movements and of sexchromosome movements on sex-chromosome segregation in crane fly spermatocytes. Chromosoma 40: 417–442

    CAS  PubMed  Google Scholar 

  • - Pickett-Heaps JD (1998) Cytochalasin D and latrunculin affect chromosome behaviour during meiosis in crane-fly spermatocytes. Chromosome Res (in press)

  • —, Spurck T, Pickett-Heaps JD (1997) Ultraviolet microbeam irradiations of spindle fibres in crane-fly spermatocytes and newt epithelial cells: resolution of previously conflicting observations. Protoplasma 197: 230–240

    Google Scholar 

  • Gorbsky GJ (1995) Kinetochores, microtubules and the metaphase checkpoint. Trends Cell Biol 5: 143–148

    CAS  PubMed  Google Scholar 

  • —, Ricketts WA (1993) Differential expression of a phosphoepitope at the kinetochores of moving chromosomes. J Cell Biol 122: 1311–1321

    CAS  PubMed  Google Scholar 

  • Ilagan AI, Forer A (1997) Effects of ultraviolet-microbeam irradiation of kinetochores in crane-fly spermatocytes. Cell Motil Cytoskeleton 36: 266–275

    CAS  PubMed  Google Scholar 

  • Ingber DE (1993) Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. J Cell Sci 104: 613–627

    PubMed  Google Scholar 

  • Jang JK, Messina L, Erdman MB, Arbel T, Hawley RS (1995) Induction of metaphase arrest in Drosophila oocytes by chiasmabased kinetochore tension. Science 268: 1917–1919

    CAS  PubMed  Google Scholar 

  • Janicke MA, LaFountain JR Jr (1982) Chromosome segregation in crane-fly spermatocytes: cold treatment and cold recovery induce anaphase lag. Chromosoma 85: 619–631

    CAS  PubMed  Google Scholar 

  • — — (1984) Malorientation in half-bivalents at anaphase: analysis of autosomal laggards in untreated, cold-treated, and cold-recovering crane fly spermatocytes. J Cell Biol 98: 859–869

    CAS  PubMed  Google Scholar 

  • — — (1986) Bivalent orientation and behavior in crane-fly spermatocytes recovering from cold exposure. Cell Motil Cytoskeleton 6: 492–501

    CAS  PubMed  Google Scholar 

  • Ladrach KS, LaFountain JR Jr (1986) Malorientation and abnormal segregation of chromosomes during recovery from colcemid and nocodazole. Cell Motil Cytoskeleton 6: 419–427

    CAS  PubMed  Google Scholar 

  • LaFountain JR Jr (1985a) Chromosome segregation and spindle structure in crane fly spermatocytes following colcemid treatment. Chromosoma 91: 329–336

    PubMed  Google Scholar 

  • — (1985b) Malorientation in half-bivalents at anaphase in crane fly spermatocytes following colcemid treatment. Chromosoma 91: 337–346

    PubMed  Google Scholar 

  • —, Janicke MA, Balczon R, Rickards GK (1992) Cytochalasin induces abnormal anaphase in crane-fly spermatocytes and causes altered distribution of actin and centromeric antigens. Chromosoma 101: 425–441

    CAS  Google Scholar 

  • Li X, Nicklas RB (1995) Mitotic forces control a cell-cycle checkpoint. Nature 373: 630–632

    CAS  PubMed  Google Scholar 

  • — — (1997) Tension-sensitive kinetochore phosphorylation and the chromosome distribution checkpoint in praying mantid spermatocytes. J Cell Sci 110: 537–545

    CAS  PubMed  Google Scholar 

  • Maniotis AJ, Chen CS, Ingber DE (1997) Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc Natl Acad Sci USA 94: 849–854

    CAS  PubMed  Google Scholar 

  • McIntosh JR (1991) Structural and mechanical control of mitotic progression. Cold Spring Harbor Symp Quant Biol 56: 613–619

    CAS  PubMed  Google Scholar 

  • McKim KS, Hawley RS (1995) Chromosomal control of meiotic cell division. Science 270: 1595–1601

    CAS  PubMed  Google Scholar 

  • Nicklas RB (1997) How cells get the right chromosomes. Science 275: 632–637

    CAS  PubMed  Google Scholar 

  • —, Ward SC, Gorbsky GJ (1995) Kinetochore chemistry is sensitive to tension and may link mitotic forces to a cell cycle checkpoint. J Cell Biol 130: 929–939

    CAS  PubMed  Google Scholar 

  • Pangilinan F, Spencer F (1996) Abnormal kinetochore structure activates the spindle assembly checkpoint in budding yeast. Mol Biol Cell 7: 1195–1208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pickett-Heaps JD, Spurck T (1982) Studies on kinetochore function in mitosis I: the effects of colchicine and cytochalasin on mitosis in the diatom Hantzschia amphioxys. Eur J Cell Biol 28: 77–82

    CAS  PubMed  Google Scholar 

  • —, Forer A, Spurck T (1996) Rethinking anaphase: where “Pac-Man” fails and why a role for the spindle matrix is likely. Protoplasma 192: 1–10

    Google Scholar 

  • — — — (1997) The traction fibre: toward a “tensegral” model of the spindle. Cell Motil Cytoskeleton 37: 1–6

    CAS  PubMed  Google Scholar 

  • Pluta AF, Mackay AM, Ainsztein AM, Goldberg IG, Earnshaw WC (1995) The centromere: hub of chromosomal activities. Science 270: 1591–1594

    CAS  PubMed  Google Scholar 

  • Rieder CL, Schulz A, Cole R, Sluder G (1994) Anaphase onset in vertebrate somatic cells is controlled by a checkpoint that monitors sister kinetochore attachment to the spindle. J Cell Biol 127: 1301–1310

    CAS  PubMed  Google Scholar 

  • —, Cole RW, Khodjakov A, Sluder G (1995) The checkpoint delay in anaphase in response to chromosome monoorientation is mediated by an inhibitory signal produced by unattached kinetochores. J Cell Biol 130: 941–948

    CAS  PubMed  Google Scholar 

  • —, Khodjakov A, Paliulis LV, Fortier TM, Cole RW, Sluder G (1997) Mitosis in vertebrate somatic cells with two spindles: implications for the metaphase/anaphase transition checkpoint and cleavage. Proc Natl Acad Sci USA 94: 5107–5112

    CAS  PubMed  Google Scholar 

  • Rudner AD, Murray AW (1996) The spindle assembly checkpoint. Curr Opin Cell Biol 8: 773–780

    CAS  PubMed  Google Scholar 

  • Sampson K, Pickett-Heaps JD, Forer A (1996) Cytochalasin D blocks chromosomal attachment to the spindle in the green alga Oedogonium. Protoplasma 192: 130–144

    CAS  Google Scholar 

  • Sillers PJ, Forer A (1981) Autosomal spindle fibres influence subsequent sex-chromosome movements in crane-fly spermatocytes. J Cell Sci 49: 51–67

    CAS  PubMed  Google Scholar 

  • Sluder G, Miller FJ, Thompson EA, Wolf DE (1994) Feedback control of the metaphase-anaphase transition in sea urchin zygotes: role of maloriented chromosomes. J Cell Biol 126: 189–198

    CAS  PubMed  Google Scholar 

  • —, Thompson EA, Miller FJ, Hayes J, Rieder CL (1997) The checkpoint control for anaphase onset does not monitor excess numbers of spindle poles or bipolar spindle symmetry. J Cell Sci 110: 421–429

    CAS  PubMed  Google Scholar 

  • Spurck T, Forer A, Pickett-Heaps J (1997) Ultraviolet microbeam irradiations of epithelial and spermatoctye spindles suggest that forces act on the kinetochore fibre and are not generated by its disassembly. Cell Motil Cytoskeleton 36: 136–148

    CAS  PubMed  Google Scholar 

  • Wells WAE (1996) The spindle-assembly checkpoint: aiming for a perfect mitosis, every time. Trends Cell Biol 6: 228–234

    CAS  PubMed  Google Scholar 

  • —, Murray AW (1996) Aberrantly segregating centromeres activate the spindle assembly checkpoint in budding yeast. J Cell Biol 133: 75–84

    CAS  PubMed  Google Scholar 

  • Wilson PJ, Forer A, Leggiadro C (1994) Evidence that kinetochore microtubules in crane-fly spermatocytes disassemble during anaphase primarily at the poleward end. J Cell Sci 107: 3015–3027

    CAS  PubMed  Google Scholar 

  • Wrench GA, Snyder JA (1997) Cytochalasin J treatment significantly alters mitotic spindle organization and kinetochore structure in PtK1 cells. Cell Motil Cytoskeleton 36: 112–124

    CAS  PubMed  Google Scholar 

  • Yen TJ, Schaar BT (1996) Kinetochore function: molecular motors, switches and gates. Curr Opin Cell Biol 8: 381–388

    CAS  PubMed  Google Scholar 

  • Zhang D, Nicklas RB (1996) “Anaphase” and cytokinesis in the absence of chromosomes. Nature 382: 466–468

    CAS  PubMed  Google Scholar 

  • Zirkle RE (1957) Partial-cell irradiation. Adv Biol Med Phys 5: 103–146

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Forer, A., Pickett-Heaps, J.D. Checkpoint control in crane-fly spermatocytes: unattached chromosomes induced by cytochalasin D or latrunculin treatment do not prevent or delay the start of anaphase. Protoplasma 203, 100–111 (1998). https://doi.org/10.1007/BF01280592

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01280592

Keywords

Navigation