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. 1991 Dec 1;115(5):1259–1265. doi: 10.1083/jcb.115.5.1259

Slow calcium waves accompany cytokinesis in medaka fish eggs

PMCID: PMC2289223  PMID: 1955473

Abstract

Animal cells are cleaved by the formation and contraction of an extremely thin actomyosin band. In most cases this contractile band seems to form synchronously around the whole equator of the cleaving cell; however in giant cells it first forms near the mitotic apparatus and then slowly grows outwards over the cell. We studied the relationship of calcium to such contractile band growth using aequorin injected medaka fish eggs: we see two successive waves of faint luminescence moving along each of the first three cleavage furrows at approximately 0.5 micron/s. The first, narrower waves accompany furrow extension, while the second, broader ones, accompany the subsequent apposition or slow zipping together of the separating cells. If the first waves travel within the assembling contractile band, they would indicate local increases of free calcium to concentrations of about five to eight micromolar. This is the first report to visualize high free calcium within cleavage furrows. Moreover, this is also the first report to visualize slow (0.3-1.0 micron/s) as opposed to fast (10-100 microns/s) calcium waves. We suggest that these first waves are needed for furrow growth; that in part they further furrow growth by speeding actomyosin filament shortening, while such shortening in turn acts to mechanically release calcium and thus propagates these waves as well as furrow growth. We also suggest that the second waves act to induce the exocytosis which provides new furrow membrane.

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Selected References

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  1. Bozhkova V. P., Palmback L. R., Khariton VYu, Chaylakhyan L. M. Organization of the surface and adhesive properties of cleavage furrows in loach (Misgurnus fossilis) eggs. Exp Cell Res. 1983 Nov;149(1):129–139. doi: 10.1016/0014-4827(83)90386-5. [DOI] [PubMed] [Google Scholar]
  2. Bray D., White J. G. Cortical flow in animal cells. Science. 1988 Feb 19;239(4842):883–888. doi: 10.1126/science.3277283. [DOI] [PubMed] [Google Scholar]
  3. Byers T. J., Armstrong P. B. Membrane protein redistribution during Xenopus first cleavage. J Cell Biol. 1986 Jun;102(6):2176–2184. doi: 10.1083/jcb.102.6.2176. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Cande W. Z. A permeabilized cell model for studying cytokinesis using mammalian tissue culture cells. J Cell Biol. 1980 Nov;87(2 Pt 1):326–335. doi: 10.1083/jcb.87.2.326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cao L. G., Wang Y. L. Mechanism of the formation of contractile ring in dividing cultured animal cells. II. Cortical movement of microinjected actin filaments. J Cell Biol. 1990 Nov;111(5 Pt 1):1905–1911. doi: 10.1083/jcb.111.5.1905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Cassidy P. S., Kerrick W. G., Hoar P. E., Malencik D. A. Exogenous calmodulin increases Ca2+ sensitivity of isometric tension activation and myosin phosphorylation in skinned smooth muscle. Pflugers Arch. 1981 Dec;392(2):115–120. doi: 10.1007/BF00581258. [DOI] [PubMed] [Google Scholar]
  7. Cheer A., Vincent J. P., Nuccitelli R., Oster G. Cortical activity in vertebrate eggs. I: The activation waves. J Theor Biol. 1987 Feb 21;124(4):377–404. doi: 10.1016/s0022-5193(87)80217-5. [DOI] [PubMed] [Google Scholar]
  8. Conrad G. W., Glackin P. V., Hay R. A., Patron R. R. Effects of calcium antagonists, calmodulin antagonists, and methylated xanthines on polar lobe formation and cytokinesis in fertilized eggs of Ilyanassa obsoleta. J Exp Zool. 1987 Aug;243(2):245–258. doi: 10.1002/jez.1402430210. [DOI] [PubMed] [Google Scholar]
  9. Donahue B. S., Abercrombie R. F. Free diffusion coefficient of ionic calcium in cytoplasm. Cell Calcium. 1987 Dec;8(6):437–448. doi: 10.1016/0143-4160(87)90027-3. [DOI] [PubMed] [Google Scholar]
  10. Franco A., Jr, Lansman J. B. Calcium entry through stretch-inactivated ion channels in mdx myotubes. Nature. 1990 Apr 12;344(6267):670–673. doi: 10.1038/344670a0. [DOI] [PubMed] [Google Scholar]
  11. Gilkey J. C., Jaffe L. F., Ridgway E. B., Reynolds G. T. A free calcium wave traverses the activating egg of the medaka, Oryzias latipes. J Cell Biol. 1978 Feb;76(2):448–466. doi: 10.1083/jcb.76.2.448. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. HIRAMOTO Y. Microinjection of the live spermatozoa into sea urchin eggs. Exp Cell Res. 1962 Sep;27:416–426. doi: 10.1016/0014-4827(62)90006-x. [DOI] [PubMed] [Google Scholar]
  13. Hepler P. K. Calcium transients during mitosis: observations in flux. J Cell Biol. 1989 Dec;109(6 Pt 1):2567–2573. doi: 10.1083/jcb.109.6.2567. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Jaffe L. F. The path of calcium in cytosolic calcium oscillations: a unifying hypothesis. Proc Natl Acad Sci U S A. 1991 Nov 1;88(21):9883–9887. doi: 10.1073/pnas.88.21.9883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kline D., Robinson K. R., Nuccitelli R. Ion currents and membrane domains in the cleaving Xenopus egg. J Cell Biol. 1983 Dec;97(6):1753–1761. doi: 10.1083/jcb.97.6.1753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Mabuchi I. Biochemical aspects of cytokinesis. Int Rev Cytol. 1986;101:175–213. doi: 10.1016/s0074-7696(08)60249-1. [DOI] [PubMed] [Google Scholar]
  17. Mabuchi I., Tsukita S., Tsukita S., Sawai T. Cleavage furrow isolated from newt eggs: contraction, organization of the actin filaments, and protein components of the furrow. Proc Natl Acad Sci U S A. 1988 Aug;85(16):5966–5970. doi: 10.1073/pnas.85.16.5966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Means A. R., Tash J. S., Chafouleas J. G. Physiological implications of the presence, distribution, and regulation of calmodulin in eukaryotic cells. Physiol Rev. 1982 Jan;62(1):1–39. doi: 10.1152/physrev.1982.62.1.1. [DOI] [PubMed] [Google Scholar]
  19. Rappaport R. Role of the mitotic apparatus in furrow initiation. Ann N Y Acad Sci. 1990;582:15–21. doi: 10.1111/j.1749-6632.1990.tb21663.x. [DOI] [PubMed] [Google Scholar]
  20. Roberson M., Armstrong J., Armstrong P. Adhesive and non-adhesive membrane domains of amphibian embryo cells. J Cell Sci. 1980 Aug;44:19–31. doi: 10.1242/jcs.44.1.19. [DOI] [PubMed] [Google Scholar]
  21. Salmon E. D. Cytokinesis in animal cells. Curr Opin Cell Biol. 1989 Jun;1(3):541–547. doi: 10.1016/0955-0674(89)90018-5. [DOI] [PubMed] [Google Scholar]
  22. Sanger J. M., Mittal B., Dome J. S., Sanger J. W. Analysis of cell division using fluorescently labeled actin and myosin in living PtK2 cells. Cell Motil Cytoskeleton. 1989;14(2):201–219. doi: 10.1002/cm.970140207. [DOI] [PubMed] [Google Scholar]
  23. Sawai T., Yomota A. Cleavage plane determination in amphibian eggs. Ann N Y Acad Sci. 1990;582:40–49. doi: 10.1111/j.1749-6632.1990.tb21666.x. [DOI] [PubMed] [Google Scholar]
  24. Schantz A. R. Cytosolic free calcium-ion concentration in cleaving embryonic cells of Oryzias latipes measured with calcium-selective microelectrodes. J Cell Biol. 1985 Mar;100(3):947–954. doi: 10.1083/jcb.100.3.947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Schroeder T. E. The contractile ring and furrowing in dividing cells. Ann N Y Acad Sci. 1990;582:78–87. doi: 10.1111/j.1749-6632.1990.tb21669.x. [DOI] [PubMed] [Google Scholar]
  26. Shimomura O., Inouye S., Musicki B., Kishi Y. Recombinant aequorin and recombinant semi-synthetic aequorins. Cellular Ca2+ ion indicators. Biochem J. 1990 Sep 1;270(2):309–312. doi: 10.1042/bj2700309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Singal P. K., Sanders E. J. An ultrastructural study of the first cleavage of Xenopus embryos. J Ultrastruct Res. 1974 Jun;47(3):433–451. doi: 10.1016/s0022-5320(74)90019-7. [DOI] [PubMed] [Google Scholar]
  28. Speksnijder J. E., Miller A. L., Weisenseel M. H., Chen T. H., Jaffe L. F. Calcium buffer injections block fucoid egg development by facilitating calcium diffusion. Proc Natl Acad Sci U S A. 1989 Sep;86(17):6607–6611. doi: 10.1073/pnas.86.17.6607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Speksnijder J. E., Sardet C., Jaffe L. F. The activation wave of calcium in the ascidian egg and its role in ooplasmic segregation. J Cell Biol. 1990 May;110(5):1589–1598. doi: 10.1083/jcb.110.5.1589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Thomas R. J. Cytokinesis during early development of a teleost embryo: Brachydanio rerio. J Ultrastruct Res. 1968 Aug;24(3):232–238. doi: 10.1016/s0022-5320(68)90060-9. [DOI] [PubMed] [Google Scholar]
  31. Yoneda M., Kobayakawa Y., Kubota H. Y., Sakai M. Surface contraction waves in amphibian eggs. J Cell Sci. 1982 Apr;54:35–46. doi: 10.1242/jcs.54.1.35. [DOI] [PubMed] [Google Scholar]
  32. Yoshimoto Y., Hiramoto Y. Cleavage in a saponin model of the sea urchin egg. Cell Struct Funct. 1985 Mar;10(1):29–36. doi: 10.1247/csf.10.29. [DOI] [PubMed] [Google Scholar]
  33. ZOTIN A. I. THE MECHANISM OF CLEAVAGE IN AMPHIBIAN AND STURGEON EGGS. J Embryol Exp Morphol. 1964 Jun;12:247–262. [PubMed] [Google Scholar]

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