A localized elevation of cytosolic free calcium is associated with cytokinesis in the zebrafish embryo (original) (raw)
Abstract
Cytokinesis, a key step in cell division, is known to be precisely regulated both in its timing and location. At present, the regulatory mechanism of cytokinesis is not well understood, although it has been suggested that calcium signaling may play an important role in this process. To test this notion, we introduced a sensitive fluorescent Ca2+ indicator into the zebrafish embryo and used confocal microscopy to measure the spatiotemporal variation of intracellular free Ca2+ concentration ([Ca2+]i) during cell cleavage. It was evident that a localized elevation of [Ca2+]i is closely associated with cytokinesis. First, we found that during cytokinesis, the level of free Ca2+ was elevated locally precisely at the cleavage site. Second, the rise of free Ca2+ was very rapid and occurred just preceding the initiation of furrow contraction. These observations strongly suggest that cytokinesis may be triggered by a calcium signal. In addition, we found that this cytokinesis-associated calcium signal arose mainly from internal stores of Ca2+ rather than from external free Ca2+; it could be blocked by the antagonist of inositol trisphosphate (InsP3) receptors. These findings suggest that the localized elevation of [Ca2+]i is caused by the release of free Ca2+ from the endoplasmic reticulum through the InsP3-regulated calcium channels.
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- Amundson J., Clapham D. Calcium waves. Curr Opin Neurobiol. 1993 Jun;3(3):375–382. doi: 10.1016/0959-4388(93)90131-h. [DOI] [PubMed] [Google Scholar]
- Berridge M. J., Dupont G. Spatial and temporal signalling by calcium. Curr Opin Cell Biol. 1994 Apr;6(2):267–274. doi: 10.1016/0955-0674(94)90146-5. [DOI] [PubMed] [Google Scholar]
- Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Ciapa B., Pesando D., Wilding M., Whitaker M. Cell-cycle calcium transients driven by cyclic changes in inositol trisphosphate levels. Nature. 1994 Apr 28;368(6474):875–878. doi: 10.1038/368875a0. [DOI] [PubMed] [Google Scholar]
- Ehrlich B. E., Kaftan E., Bezprozvannaya S., Bezprozvanny I. The pharmacology of intracellular Ca(2+)-release channels. Trends Pharmacol Sci. 1994 May;15(5):145–149. doi: 10.1016/0165-6147(94)90074-4. [DOI] [PubMed] [Google Scholar]
- Fluck R. A., Miller A. L., Jaffe L. F. Slow calcium waves accompany cytokinesis in medaka fish eggs. J Cell Biol. 1991 Dec;115(5):1259–1265. doi: 10.1083/jcb.115.5.1259. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Girard S., Clapham D. Acceleration of intracellular calcium waves in Xenopus oocytes by calcium influx. Science. 1993 Apr 9;260(5105):229–232. doi: 10.1126/science.8385801. [DOI] [PubMed] [Google Scholar]
- Grandin N., Charbonneau M. Intracellular free calcium oscillates during cell division of Xenopus embryos. J Cell Biol. 1991 Feb;112(4):711–718. doi: 10.1083/jcb.112.4.711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Han J. K., Fukami K., Nuccitelli R. Reducing inositol lipid hydrolysis, Ins(1,4,5)P3 receptor availability, or Ca2+ gradients lengthens the duration of the cell cycle in Xenopus laevis blastomeres. J Cell Biol. 1992 Jan;116(1):147–156. doi: 10.1083/jcb.116.1.147. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hepler P. K. Calcium and mitosis. Int Rev Cytol. 1992;138:239–268. doi: 10.1016/s0074-7696(08)61590-9. [DOI] [PubMed] [Google Scholar]
- Hepler P. K., Callaham D. A. Free calcium increases during anaphase in stamen hair cells of Tradescantia. J Cell Biol. 1987 Nov;105(5):2137–2143. doi: 10.1083/jcb.105.5.2137. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kao J. P. Practical aspects of measuring [Ca2+] with fluorescent indicators. Methods Cell Biol. 1994;40:155–181. doi: 10.1016/s0091-679x(08)61114-0. [DOI] [PubMed] [Google Scholar]
- McPherson S. M., McPherson P. S., Mathews L., Campbell K. P., Longo F. J. Cortical localization of a calcium release channel in sea urchin eggs. J Cell Biol. 1992 Mar;116(5):1111–1121. doi: 10.1083/jcb.116.5.1111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Meng C. L., Chang D. C. Study of calcium signaling in cell cleavage using confocal microscopy. Biol Bull. 1994 Oct;187(2):234–235. doi: 10.1086/BBLv187n2p234. [DOI] [PubMed] [Google Scholar]
- Miller A. L., Fluck R. A., McLaughlin J. A., Jaffe L. F. Calcium buffer injections inhibit cytokinesis in Xenopus eggs. J Cell Sci. 1993 Oct;106(Pt 2):523–534. doi: 10.1242/jcs.106.2.523. [DOI] [PubMed] [Google Scholar]
- Mittal B., Sanger J. M., Sanger J. W. Visualization of myosin in living cells. J Cell Biol. 1987 Oct;105(4):1753–1760. doi: 10.1083/jcb.105.4.1753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parys J. B., Sernett S. W., DeLisle S., Snyder P. M., Welsh M. J., Campbell K. P. Isolation, characterization, and localization of the inositol 1,4,5-trisphosphate receptor protein in Xenopus laevis oocytes. J Biol Chem. 1992 Sep 15;267(26):18776–18782. [PubMed] [Google Scholar]
- Poenie M., Alderton J., Tsien R. Y., Steinhardt R. A. Changes of free calcium levels with stages of the cell division cycle. Nature. 1985 May 9;315(6015):147–149. doi: 10.1038/315147a0. [DOI] [PubMed] [Google Scholar]
- Rink T. J., Tsien R. Y., Warner A. E. Free calcium in Xenopus embryos measured with ion-selective microelectrodes. Nature. 1980 Feb 14;283(5748):658–660. doi: 10.1038/283658a0. [DOI] [PubMed] [Google Scholar]
- 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]
- Satterwhite L. L., Lohka M. J., Wilson K. L., Scherson T. Y., Cisek L. J., Corden J. L., Pollard T. D. Phosphorylation of myosin-II regulatory light chain by cyclin-p34cdc2: a mechanism for the timing of cytokinesis. J Cell Biol. 1992 Aug;118(3):595–605. doi: 10.1083/jcb.118.3.595. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Satterwhite L. L., Pollard T. D. Cytokinesis. Curr Opin Cell Biol. 1992 Feb;4(1):43–52. doi: 10.1016/0955-0674(92)90057-j. [DOI] [PubMed] [Google Scholar]
- 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]
- Sellers J. R. Regulation of cytoplasmic and smooth muscle myosin. Curr Opin Cell Biol. 1991 Feb;3(1):98–104. doi: 10.1016/0955-0674(91)90171-t. [DOI] [PubMed] [Google Scholar]
- Silver R. B. Nuclear envelope breakdown and mitosis in sand dollar embryos is inhibited by microinjection of calcium buffers in a calcium-reversible fashion, and by antagonists of intracellular Ca2+ channels. Dev Biol. 1989 Jan;131(1):11–26. doi: 10.1016/s0012-1606(89)80034-x. [DOI] [PubMed] [Google Scholar]
- Snow P., Nuccitelli R. Calcium buffer injections delay cleavage in Xenopus laevis blastomeres. J Cell Biol. 1993 Jul;122(2):387–394. doi: 10.1083/jcb.122.2.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stith B. J., Goalstone M., Silva S., Jaynes C. Inositol 1,4,5-trisphosphate mass changes from fertilization through first cleavage in Xenopus laevis. Mol Biol Cell. 1993 Apr;4(4):435–443. doi: 10.1091/mbc.4.4.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thomas A. P., Renard D. C., Rooney T. A. Spatial organization of Ca2+ signalling and Ins(1,4,5)P3 action. Adv Second Messenger Phosphoprotein Res. 1992;26:225–263. [PubMed] [Google Scholar]
- Whitaker M., Patel R. Calcium and cell cycle control. Development. 1990 Apr;108(4):525–542. doi: 10.1242/dev.108.4.525. [DOI] [PubMed] [Google Scholar]
- Yamakita Y., Yamashiro S., Matsumura F. In vivo phosphorylation of regulatory light chain of myosin II during mitosis of cultured cells. J Cell Biol. 1994 Jan;124(1-2):129–137. doi: 10.1083/jcb.124.1.129. [DOI] [PMC free article] [PubMed] [Google Scholar]