|
|
The formation of Ca 2+ gradients at the cleavage furrows during cytokinesis of Zebrafish
embryos |
Yun-Bo GUO,Ya WEN,Wen-Xue GAO,Jing-Chao LI,Peng ZHOU,Zai-Ling BAI,Bo ZHANG,Shi-Qiang WANG, |
State Key Laboratory
of Biomembrane and Membrane Biotechnology, and Center of Developmental
Biology and Genetics, College of Life Sciences, Peking University,
Beijing 100871, China; |
|
|
Abstract In dividing embryos, a localized elevation in intracellular Ca2+ ([Ca2+]i) at the cleavage furrow has been shown to be essential for cytokinesis. However, the underlying mechanisms for generating and maintaining these [Ca2+]i gradients throughout cytokinesis are not fully understood. In the present study, we analyzed the role of inositol 1,4,5-trisphosphate receptors (IP3Rs) and endoplasmic reticulum (ER) distribution in determining the intracellular Ca2+ gradients in early zebrafish blastomeres. Application of the injected Ca2+ indicator, Indo-1, showed that during the first cell division a standing Ca2+ gradient was formed ~35min after fertilization, with the [Ca2+]i spatially decaying from 500–600 nmol/L at the cleavage furrow to 100–200 nmol/L around the nucleus. While the IP3R immunohistochemical fluorescence was relatively concentrated in the peri-furrow region, ER labeling was relatively enriched in both peri-furrow and peri-nuclear regions. Numeric simulation suggested that a divergence in the spatial distribution of IP3R and the locations of Ca2+ uptake within the ER was essential for the formation of a standing Ca2+ gradient, and the Ca2+ gradient could only be well-established under an optimal stoichiometry of Ca2+ uptake and release. Indeed, while inhibition of IP3R Ca2+ release blocked the generation of the Ca2+ gradient at a lower [Ca2+]i level, both Ca2+ release stimulation by inositol 1,4,5-trisphosphate (IP3) injection and ER Ca2+ pump inhibition by cyclopiazonic acid also eliminated the Ca2+ gradients at higher [Ca2+]i levels. Our results suggest a dynamic relationship between ER-mediated Ca2+ release and uptake that underlies the maintenance of the peri-furrow Ca2+ gradient and is essential for cytokinesis of zebrafish embryos.
|
Keywords
Ca2+ gradients
cytokinesis
zebrafish
|
Issue Date: 01 August 2010
|
|
|
Chang D C, Meng C (1995). A localized elevation of cytosolic free calcium is associated withcytokinesis in the zebrafish embryo. J Cell Biol, 131(6 Pt 1): 1539–1545
doi: 10.1083/jcb.131.6.1539
|
|
Créton R, Speksnijder J E, Jaffe L F (1998). Patterns of free calcium in zebrafish embryos. J Cell Sci, 111(Pt 12): 1613–1622
|
|
Deguchi R, Shirakawa H, Oda S, Mohri T, Miyazaki S (2000). Spatiotemporal analysis of Ca(2+) waves in relationto the sperm entry site and animal-vegetal axis during Ca(2+) oscillationsin fertilized mouse eggs. Dev Biol, 218(2): 299–313
doi: 10.1006/dbio.1999.9573
|
|
Fluck R A, Miller A L, Jaffe L F (1991). Slow calcium waves accompany cytokinesis in medaka fish eggs. J Cell Biol, 115(5): 1259–1265
doi: 10.1083/jcb.115.5.1259
|
|
Fontanilla R A, Nuccitelli R (1998). Characterization of the sperm-induced calcium wave inXenopus eggs using confocal microscopy. Biophys J, 75(4): 2079–2087
doi: 10.1016/S0006-3495(98)77650-7
|
|
Gilkey J C, Jaffe L F, Ridgway E B, Reynolds G T (1978). A free calcium wave traverses the activating egg ofthe medaka, Oryzias latipes. J Cell Biol, 76(2): 448–466
doi: 10.1083/jcb.76.2.448
|
|
Hafner M, Petzelt C, Nobiling R, Pawley J B, Kramp D, Schatten G (1988). Wave of free calcium at fertilization in the sea urchin egg visualized with fura-2. Cell Motil Cytoskeleton, 9(3): 271–277
doi: 10.1002/cm.970090309
|
|
Krebs J, Michalak M (2007). Calcium: A Matter of Life or Death. Amsterdam: Elsevier B.V.
|
|
Kume S, Muto A, Aruga J, Nakagawa T, Michikawa T, Furuichi T, Nakade S, Okano H, Mikoshiba K (1993). The Xenopus IP3 receptor: structure, function, and localization in oocytes and eggs. Cell, 73(3): 555–570
|
|
Lee K W, Webb S E, Miller A L (2003). Ca2+ released via IP3 receptors is required for furrow deepening during cytokinesisin zebrafish embryos. Int J Dev Biol, 47(6): 411–421
|
|
Li W M, Webb S E, Chan C M, Miller A L (2008). Multiple roles of the furrow deepening Ca2+ transientduring cytokinesis in zebrafish embryos. Dev Biol, 316(2): 228–248
doi: 10.1016/j.ydbio.2008.01.027
|
|
Miller A L, Fluck R A, McLaughlin J A, Jaffe L F (1993). Calcium buffer injections inhibit cytokinesis in Xenopus eggs. J Cell Sci, 106(Pt 2): 523–534
|
|
Muto A, Kume S, Inoue T, Okano H, Mikoshiba K (1996). Calcium waves along the cleavage furrows in cleavage-stage Xenopus embryosand its inhibition by heparin. J Cell Biol, 135(1): 181–190
doi: 10.1083/jcb.135.1.181
|
|
Naito Y, Okada M, Yagisawa H (2006). Phospholipase C isoforms are localized at the cleavage furrow during cytokinesis. J Biochem, 140(6): 785–791
doi: 10.1093/jb/mvj209
|
|
Noguchi T, Mabuchi I (2002). Localized calcium signals along the cleavage furrowof the Xenopus egg are not involved in cytokinesis. Mol Biol Cell, 13(4): 1263–1273
doi: 10.1091/mbc.01-10-0501
|
|
Samuel A D, Murthy V N, Hengartner M O (2001). Calcium dynamics during fertilization in C. elegans. BMC Dev Biol, 1: 8–13
doi: 10.1186/1471-213X-1-8
|
|
Snow P, Nuccitelli R (1993). Calcium buffer injections delay cleavage in Xenopuslaevis blastomeres. J Cell Biol, 122(2): 387–394
doi: 10.1083/jcb.122.2.387
|
|
Speksnijder J E, Miller A L, Weisenseel M H, Chen T H, Jaffe L F (1989). Calcium buffer injections block fucoid egg development by facilitatingcalcium diffusion. Proc Natl Acad Sci US A, 86(17): 6607–6611
doi: 10.1073/pnas.86.17.6607
|
|
Terasaki M, Jaffe L A (1991). Organization of the sea urchin egg endoplasmic reticulum and itsreorganization at fertilization. J Cell Biol, 114(5): 929–940
doi: 10.1083/jcb.114.5.929
|
|
Webb S E, Lee K W, Karplus E, Miller A L (1997). Localized calcium transients accompany furrow positioning,propagation, and deepening during the early cleavage period of zebrafishembryos. Dev Biol, 192(1): 78–92
doi: 10.1006/dbio.1997.8724
|
|
Whitaker M (2006). Calcium at fertilization and in earlydevelopment. Physiol Rev, 86(1): 25–88
doi: 10.1152/physrev.00023.2005
|
|
Wong R, Hadjiyanni I, Wei H C, Polevoy G, McBride R, Sem K P, Brill J A (2005). PIP2 hydrolysis and calcium release are required for cytokinesis in Drosophila spermatocytes. Curr Biol, 15(15): 1401–1406
doi: 10.1016/j.cub.2005.06.060
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|