Skip to main content
Log in

The role of calcium ions during mitosis

Calcium participates in the anaphase trigger

  • Published:
Chromosoma Aims and scope Submit manuscript

    We’re sorry, something doesn't seem to be working properly.

    Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Abstract

Calcium-containing solutions were microinjected into dividing PtK1 cells to assess the effect of calcium ion concentration on the morphology and physiology of the mitotic spindle. Solutions containing 50 μM or more CaCl2 are immediately and irreversibly toxic to PtK1 cells. Those containing 5–10 μM CaCl2 cause reversible reduction in spindle birefringence followed by normal anaphase and cytokinesis. Microinjection of 5 μM or less CaCl2 into anaphase PtK1 cells has no detectable effect on the rate or extent of chromosome movement. Metaphase cells tend to enter anaphase 4–5 min after injection with 1–10 μM CaCl2, compared with an average of 16 min after injection with calcium-free buffer. Reducing the intracellular calcium concentration by injection of EGTA-CaCl2 buffers increases the lag between injection and anaphase to 20 min or more. Microinjection of calcium solutions does not promote precocious chromatid separation in nocodazole-arrested metaphase cells, indicating that the increase in calcium concentration does not induce centromere separation directly. An increase in the concentration of free calcium ions during metaphase appears to stimulate the onset of anaphase. Such an increase, regulated by the cell itself, may contribute to the initiation of chromosome separation in mammalian cells.

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.

Similar content being viewed by others

References

  • Anderson B, Osborn M, Weber K (1978) Specific visualization of the distribution of the calcium-dependent regulatory protein of cyclic nucleotide phosphodiesterase (modulator protein) in tissue culture cells by immunofluorescence microscopy: mitosis and intercellular bridge. Cytobiologie 17:354–364

    Google Scholar 

  • Berkowitz SA, Wolff (1981) Intrinsic calcium sensitivity of tubulin polymerization. The contributions of temperature, tubulin concentration, and associated proteins. J Biol Chem 256:11216–11223

    Google Scholar 

  • Blum JJ, Hayes A, Jamieson GA, Vanamon TC (1980) Calmodulin confers calcium sensitivity on ciliary dynein ATPase. J Cell Biol 87:386–397

    Google Scholar 

  • Bygrave FL (1978) Mitochondria and the control of intracellular calcium. Biol Rev 53:43–79

    Google Scholar 

  • Cande WZ (1981) Physiology of chromosome movement in lysed cell models. In: Schweiger H.G., ed, International cell biology, 1980–81, Springer, Berlin·Heidelberg·New York, pp 382–391

    Google Scholar 

  • Cande WZ (1982) Inhibition of spindle elongation in permeabilized mitotic cells by erythro-9-[3-(2-hydroxynonyl)]adenine. Nature 295:700–701

    Google Scholar 

  • Cande WZ, Wolniak SM (1978) Chromosome movement in lysed mitotic cells is inhibited by vanadate. J Cell Biol 79:573–580

    Google Scholar 

  • Carafoli E, Crompton M (1976) Calcium ions and mitochondria. Symp Soc Exp Biol 30:89–115

    Google Scholar 

  • Fuller GM, Brinkley BR (1976) Structure and control of assembly of cytoplasmic microtubules in normal and transformed cells. J Supramol Struct 5:497–514

    Google Scholar 

  • Goldstein DA (1979) Calculation of the concentrations of free cations and cation-like complexes in solutions containing multiple divalent cations and ligands. Biophys J 26:235–242

    Google Scholar 

  • Goldstein LSB (1981) Kinetochore structure and its role in chromosome orientation during the first meiotic division in male D. melanogaster. Cell 25:591–602

    Google Scholar 

  • Hallet MB, Campbell AK (1982) Measurement of changes in cytoplasmic free Ca2+ in fused cell hybrids. Nature 295:155–158

    Google Scholar 

  • Hepler PK (1980) Membranes in the mitotic apparatus of barley cells. J Cell Biol 86:490–499

    Google Scholar 

  • Hyams J (1982) Dynein in the spindle? Nature 295:648–649

    Google Scholar 

  • Inoue S (1981) Video image processing greatly enhances contrast, quality and speed in polarization-based microscopy. J Cell Biol 89:346–356

    Google Scholar 

  • Inoué S, Sato H (1967) Cell motility by labile association of molecules. The nature of mitotic spindle fibers and their role in chromosome movement. J Gen Physiol 50:259–292

    Google Scholar 

  • Izant JG, Weatherbee JA, McIntosh JR (1983) A microtubule-associated protein antigen unique to the mitotic spindle in PtK1 cells. J Cell Biol 96:424–434

    Google Scholar 

  • Jamieson GA, Vanamon TC, Blum JJ (1979) Presence of calmodulin in Tetrahymena. Proc Natl Acad Sci 76:6471–6475

    Google Scholar 

  • Job D, Rauch CT, Fisher EH, Margolis RL (1981) Ca2+-calmodulin and protein kinase regulation of brain microtubule cold-stability. J Cell Biol 91:322a

    Google Scholar 

  • Keller TCS III, Jemiolo DK, Burgess WH, Rebhun LI (1982) Strongylocentrotus purpuratus spindle tubulin II. Characteristics of its sensitivity to Ca++ and the effects of calmodulin isolated from bovine brain and S. purpuratus eggs. J Cell Biol 93:797–803

    Google Scholar 

  • Kiehart DP (1981) Studies on the in vivo sensitivity of spindle microtubules to calcium ions and evidence for a vesicular calcium-sequestering system. J Cell Biol 88:604–617

    Google Scholar 

  • Luby-Phelps K, Porter KR (1982) The control of Pigment migration in isolated erythrophores of Holoceutrus ascensionis (Osbeck) II. The role of calcium. Cell 292:441–450

    Google Scholar 

  • Marcum JM, Dedman JR, Brinkley BR, Means AR (1978) Control of microtubule assembly-disassembly by calcium dependent regulator protein. Proc Natl Acad Sci 75:3771–3775

    Google Scholar 

  • Mazia D, Petzelt C, Williams RO, Meza I (1972) A calcium activated ATPase in the mitotic apparatus of the sea urchin (isolated by a new method). Exp Cell Res 70:325–332

    Google Scholar 

  • McIntosh JR, Landis SC (1971) The distribution of spindle micro-tubules during mitosis in cultured human cells. J Cell Biol 49:468–497

    Google Scholar 

  • Means AR, Dedman JR (1980) Calmodulin — an intracellular calcium receptor. Nature 285:73–77

    Google Scholar 

  • Mohri H, Mabuchi I, Ogawa K, Kuriyama R, Sakai H (1976) Evidence for participation of dynein in chromosome movement in mitosis. In: Perry SV, Margreth A, Adelstein RS, eds. Contractile systems in non-muscle cells, North-Holland, New York

    Google Scholar 

  • Mueller C, Graessmann M, Graessmann A (1981) A microinjection technique converting living cells into test tubes. In: Schweiger HG, ed. International cell biology, 1980–81, Springer, Berlin-Heidelberg-New York, pp 119–127

    Google Scholar 

  • Nishida E, Kumagai H (1980) Calcium sensitivity of sea urchin tubulin in in vitro assembly and the effects of calcium-dependent regulator (CDR) proteins isolated from sea urchin eggs and porcine brains. J Biochem 87:143–151

    Google Scholar 

  • Olmsted JB, Borisy GG (1975) Ionic and nucleotide requirements for microtubule polymerization in vitro. Biochemistry 14:2996–3005

    Google Scholar 

  • Pratt MM, Otter T, Salmon ED (1980) Dynein-like Mg+2-ATPase in mitotic spindles isolated from sea urchin embryos (Strongylocentrotus droebachiensis). J Cell Biol 86:738–745

    Google Scholar 

  • Rasmussen H, Clayberger C, Gustin M (1979) The messenger function of calcium in cell activation. Symp Soc Exp Biol 33:161–197

    Google Scholar 

  • Rebhun LI (1977) Cyclic nucleotides, calcium and cell division. Int Rev Cytol 49:1–54

    Google Scholar 

  • Rebhun LI, Jemiolo D, Keller T, Burgess W, Kretsinger R (1980) Calcium, calmodulin and control of assembly of brain and spindle microtubules. In: DeBrabander, DeMey, eds. Microtubules and microtubule inhibitors, Elsevier/North-Holland

  • Roos UP (1973) Light and electron microscopy of rat kangaroo cells in mitosis. II. Kinetochore structure and function. Chromosoma 41:198–220

    Google Scholar 

  • Rosenfeld AC, Zackroff RV, Weisenberg (1976) Magnesium stimulation of calcium binding to tubulin and calcium-induced depolymerization of microtubules. FEBS Lett 65:144–147

    Google Scholar 

  • Roth LE, Daniels EW (1962) Electron microscopic studies of mitosis in amoebae. J Cell Biol 12:57–78

    Google Scholar 

  • Salmon ED (1975) Pressure-induced depolymerization of spindle microtubules: I Changes in birefringence and spindle length. J Cell Biol 65:603–614

    Google Scholar 

  • Salmon ED (1982) Calcium, spindle microtubule dynamics and chromosome movement. Cell Differ 11:353–355

    Google Scholar 

  • Salmon ED, Segall RR (1980) Calcium-labile mitotic spindles isolated from sea urchin eggs (Lytechinus variegatus). J Cell Biol 86:355–365

    Google Scholar 

  • Salmon ED, McKeel M, Hays T (1982) The rapid rate of tubulin dissociation from microtubules in the mitotic spindle in vivo. J Cell Biol 95:309a

    Google Scholar 

  • Schliwa M (1976) The role of divalent cations in the regulation of microtubule assembly in vivo studies on microtubules of the heliozoan axopodium using the ionophore A23187. J Cell Biol 70:527–540

    Google Scholar 

  • Schliwa M (1981) Proteins associated with cytoplasmic actin. Cell 25:587–590

    Google Scholar 

  • Schliwa M, Euteneur U, Bulinski JC, Izant JG (1981) Calcium lability of cytoplasmic microbutules and its modulation by microtubule-associated proteins. Proc Natl Acad Sci 78:1037–1041

    Google Scholar 

  • Sillen LG, Martell A (1964) Stability constants of metal-ion complexes, 2nd Edition, Chemical Society, London

    Google Scholar 

  • Silver RB, Cole RD, Cande WZ (1980) Isolation of mitotic apparatus containing vesicles with calcium sequestration activity. Cell 19:505–516

    Google Scholar 

  • Sisken JE, VedBrat SS (1977) On the effects of variations in intracellular and extracellular calcium ions on mitosis and cytokinesis of HeLa cells. J Cell Biol 75:263a

    Google Scholar 

  • Tsien RY, Pozzau T, Rink TJ (1982) T-cell mitogens cause early changes in cytoplasmic free Ca2+ and membrane potential in lymphocytes. Nature 295:68–71

    Google Scholar 

  • Weisenberg RC (1972) Microtubule formation in vitro in solutions containing low calcium concentrations. Science 177:1104–1105

    Google Scholar 

  • Welsh MJ, Dedman JR, Brinkley BR, Means AR (1978) Calcium-dependent regulator protein: Localization in mitotic apparatus of eukaryotic cells. Proc Natl Acad Sci 75:1867–1871

    Google Scholar 

  • Welsh MJ, Dedman JR, Brinkley BR, Means AR (1979) Tubulin and calmodulin. Effects of microtubule and microfilament inhibitors on localization in the mitotic apparatus. J Cell Biol 81:624–634

    Google Scholar 

  • Wick SM, Hepler PK (1980) Localization of Ca++-containing antimonate precipitates during mitosis. J Cell Biol 86:500–513

    Google Scholar 

  • Wolniak SM, Hepler PK, Jackson WT (1980) Detection of the membrane-calcium distribution during mitosis in Haemauthus endosperm with chlorotetracycline. J Cell Biol 87:23–32

    Google Scholar 

  • Wolniak SM, Hepler PK, Jackson WT (1981) Ionic changes in the mitotic apparatus during the metaphase/anaphase transition. J Cell Biol 91:313a

    Google Scholar 

  • Zirkle RE (1970) Involvement of the prometaphase kinetochore in prevention of precocious anaphase. J Cell Biol 47:235a

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Izant, J.G. The role of calcium ions during mitosis. Chromosoma 88, 1–10 (1983). https://doi.org/10.1007/BF00329497

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00329497

Keywords

Navigation