Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-29T03:30:31.642Z Has data issue: false hasContentIssue false
  • English
  • Français

SOCE proteins, STIM1 and Orai1, are localized to the cleavage furrow during cytokinesis of the first and second cell division cycles in zebrafish embryos

Published online by Cambridge University Press:  05 October 2016

Ching Man Chan ,
Jacqueline T. M. Aw ,
Sarah E. Webb  and
Andrew L. Miller
Ching Man Chan
Affiliation:
Division of Life Science & State Key Laboratory of Molecular Neuroscience, HKUST, Clear Water Bay, Hong Kong, People's Republic of China.
Jacqueline T. M. Aw
Affiliation:
Division of Life Science & State Key Laboratory of Molecular Neuroscience, HKUST, Clear Water Bay, Hong Kong, People's Republic of China.
Sarah E. Webb
Affiliation:
Division of Life Science & State Key Laboratory of Molecular Neuroscience, HKUST, Clear Water Bay, Hong Kong, People's Republic of China.
Andrew L. Miller*
Affiliation:
Division of Life Science & State Key Laboratory of Molecular Neuroscience, HKUST, Clear Water Bay, Hong Kong, People's Republic of China. Marine Biological Laboratory, Woods Hole, MA 02543, USA.
*
All correspondence to: Andrew L. Miller. Division of Life Science & State Key Laboratory of Molecular Neuroscience, HKUST, Clear Water Bay, Hong Kong, People's Republic of China. E-mail: almiller@ust.hk
Get access Rights & Permissions [Opens in a new window]

Summary

In zebrafish embryos, distinct Ca2+ transients are localized to the early cleavage furrows during the first few cell division cycles. These transients are generated mainly by release via IP3Rs in the endoplasmic reticulum, and they are necessary for furrow positioning, propagation, deepening and apposition. We previously showed, via the use of inhibitors, that store-operated Ca2+ entry (SOCE) also appears to be essential for maintaining the IP3R-mediated elevated levels of [Ca2+]i for the extended periods required for the completion of successful furrow deepening and daughter cell apposition in these large embryonic cells. Here, newly fertilized, dechorionated embryos were fixed at various times during the first and second cell division cycles and immunolabelled with antibodies to STIM1 and/or Orai1 (key components of SOCE). We show that both of these proteins have a dynamic pattern of localization during cytokinesis of the first two cell division cycles. These new data help to support our previous inhibitor results, and provide additional evidence that SOCE contributes to the maintenance of the sustained elevated Ca2+ that is required for the successful completion of cytokinesis in the large cells of embryonic zebrafish.

Keywords

Ca2+ signallingCytokinesisSTIM1 and Orai1SOCEZebrafish embryos
Type
Research Article
Information
Zygote , Volume 24 , Issue 6 , December 2016 , pp. 880 - 889
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arredouani, A., Yu, F., Sun, L. & Machaca, K. (2010). Regulation of store-operated Ca2+ entry during the cell cycle. J. Cell Sci. 123, 2155–6.CrossRefGoogle ScholarPubMed
Baba, Y., Hayashi, K., Fujii, Y., Mizushima, A., Wataral, H., Wakamori, M., Numaga, T., Mori, Y., Iino, M., Hikida, M. & Kurosaki, T. (2006). Coupling of STIM1 to store-operated Ca2+ entry through its constitutive and inducible movement in the endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 103, 16704–9.CrossRefGoogle ScholarPubMed
Barr, V.A., Bernot, K.M., Srikanth, S., Gwak, Y., Balagopalan, L., Regan, C.K., Helman, D.J., Sommers, C.L., Oh-hora, M., Rao, A. & Samelson, L.E. (2008). Dynamic movement of the calcium sensor STIM1 and the calcium channel Orai1 in activated T-cells: Puncta and distal caps. Mol. Biol. Cell 19, 2802–17.CrossRefGoogle ScholarPubMed
Berridge, M.J., Lipp, P. & Bootman, M. (2000). The versatility and universality of calcium signalling. Nature Rev. Mol. Cell Biol. 1, 11–21.CrossRefGoogle ScholarPubMed
Bezzerides, V.J., Ramsey, I.S., Kotecha, S., Greka, A. & Clapham, D.E. (2004). Rapid vesicular translocation and insertion of TRP channels. Nature Cell Biol. 6, 709–20.CrossRefGoogle ScholarPubMed
Bomben, V.C. & Sontheimer, H.W. (2008). Inhibition of transient receptor potential canonical channels impairs cytokinesis in human malignant gliomas. Cell Prolif. 41, 98–121.CrossRefGoogle ScholarPubMed
Boustany, C.E., Katsogiannou, M., Delcourt, P., Dewailly, E., Prevarskaya, N., Borowiec, A.-S. & Capiod, T. (2010). Differential roles of STIM1, STIM2 and Orai1 in the control of cell proliferation and SOCE amplitude in HEK293 cells. Cell Calcium 47, 350–9.CrossRefGoogle ScholarPubMed
Chan, C.M., Chen, Y., Hung, T.S., Miller, A.L., Shipley, A.M. & Webb, S.E. (2015). Inhibition of SOCE disrupts cytokinesis in zebrafish embryos mainly via inhibition of cleavage furrow deepening. Int. J. Dev. Biol. 59, 289–301.CrossRefGoogle ScholarPubMed
Chang, D.C. & Meng, C. (1995). A localized elevation of cytosolic free calcium is associated with cytokinesis in the zebrafish embryo. J. Cell Biol. 131, 1539–45.CrossRefGoogle ScholarPubMed
Cheng, K.T., Ong, H.L., Liu, X. & Ambudkar, I.S. (2010). Contribution of TRPC1 and Orai1 to Ca2+ entry activated by store depletion. Adv. Exp. Med. Biol. 704, 435–49.CrossRefGoogle Scholar
Chvanov, M., Walsh, C.M., Haynes, L.P., Voronina, S.G., Lur, G., Gerasimenko, O.V., Barraclough, R., Rudland, P.S., Peterson, O., Burgoyne, R.D. & Tepikin, A.V. (2008). ATP depletion induces translocation of STIM1 to puncta and formation of STIM1-ORAI1 clusters: translocation and re-translocation of STIM1 does not require ATP. Pflugers Arch.–Eur. J. Physiol. 457, 505–17.CrossRefGoogle Scholar
Courjaret, R. & Machaca, K. (2012). STIM and Orai in cellular proliferation and division. Front. Biosci. E4, 331–41.CrossRefGoogle Scholar
Créton, R., Speksnijder, J.E. & Jaffe, L.F. (1998). Patterns of free calcium in zebrafish embryos. J. Cell Sci. 111, 1613–22.CrossRefGoogle ScholarPubMed
Fluck, R.A., Miller, A.L. & Jaffe, L.A. (1991). Slow calcium waves accompany cytokinesis in medaka fish eggs. J. Cell Biol. 115, 1259–65.CrossRefGoogle ScholarPubMed
Grigoriev, I., Gouveia, S.M., van der Vaart, B., Demmers, J., Smyth, J.T., Honnappa, S., Splinter, D., Steinmetz, M.O., Putney, J.W., Hoogenraad, C.C. & Akhmanova, A. (2008). STIM1 is a MT-plus-end-tracking protein involved in remodeling of the ER. Curr. Biol. 18, 177–82.CrossRefGoogle ScholarPubMed
Gwack, Y., Srikanth, S., Feske, S., Cruz-Guilloty, F., Oh-Hora, M., Neems, D.S., Hogan, P.G. & Rao, A. (2007). Biochemical and functional characterization of Orai proteins. J. Biol. Chem. 282, 16232–43.CrossRefGoogle ScholarPubMed
Halbleib, J.M. & Nelson, W. J. (2016). Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20, 3199–214.CrossRefGoogle Scholar
Henquin, J.-C., Mourad, N.I. & Nenquin, M. (2012). Disruption and stabilization of β-cell actin microfilaments differently influence insulin secretion triggered by intracellular Ca2+ mobilization or store operated Ca2+ entry. FEBS Lett. 586, 89–95.CrossRefGoogle ScholarPubMed
Iezzi, G., Karjalainen, K. & Lanzaveccia, A. (1998). The duration of antigenic stimulation determines the fate of naïve and effector T cells. Immunity 8, 89–95.CrossRefGoogle ScholarPubMed
Jesuthasan, S. (1998). Furrow-associated microtubule arrays are required for the cohesion of zebrafish blastomeres following cytokinesis. J. Cell Biol. 111, 3695–703.Google ScholarPubMed
Kito, H., Yamamura, H., Suzuki, Y., Yamamura, H., Ohya, S., Asai, K. & Imaizumi, Y. (2015). Regulation of store-operated Ca2+ entry activity by cell cycle dependent up-regulation of Orai2 in brain capillary endothelial cells. Biochem. Biophys. Res. Communs. 459, 457–62.CrossRefGoogle ScholarPubMed
Lee, K.W., Webb, S.E. & Miller, A.L. (2003). Ca2+ released via IP3 receptors is required for furrow deepening during cytokinesis in zebrafish eggs. Int. J. Dev. Biol. 47, 411–21.Google Scholar
Lee, K.W., Ho, S.M., Wong, C.H., Webb, S.E. & Miller, A.L. (2004). Characterization of mid-spindle microtubules during furrow positioning in early cleavage period zebrafish embryos. Zygote 12, 221–30.CrossRefGoogle ScholarPubMed
Lee, K.W., Webb, S.E. & Miller, A.L. (2006). Requirement for a localized, IP3R-generated Ca2+ transient during the furrow positioning process in zebrafish zygotes. Zygote 14, 143–55.CrossRefGoogle ScholarPubMed
Lewis, R. S. (2001). Calcium signaling mechanisms in T lymphocytes. Annu. Rev. Immunol. 19, 497–521.CrossRefGoogle ScholarPubMed
Li, M., Chen, C., Zhou, Z., Xu, S. & Yu, Z. (2012). A TRPC1-mediated increase in store-operated Ca2+ entry is required for the proliferation of adult hippocampal neural progenitor cells. Cell Calcium 51, 486–96.CrossRefGoogle ScholarPubMed
Li, W.M., Lee, K.W., Webb, S.E. & Miller, A.L. (2006). The role of localized Ca2+ transients in SNARE-mediated vesicle transport and exocytosis during ingression and zipping of cleavage furrows during cytokinesis in zebrafish embryos. Exp. Cell Res. 312, 3260–75.Google Scholar
Li, W.M., Webb, S.E., Chan, C.M. & Miller, A.L. (2008). Multiple roles of the furrow deepening Ca2+ transient during cytokinesis in zebrafish embryos. Dev. Biol. 316, 228–48.CrossRefGoogle ScholarPubMed
Liou, J., Kim, M.L., Heo, W.D., Jones, J.T., Myers, J.W., Ferrell, J.E. & Myer, T. (2005). STIM is a Ca2+ sensor essential for Ca2+-store-depletion-triggered Ca2+ influx. Curr. Biol. 15, 1235–41.CrossRefGoogle ScholarPubMed
Machaca, K. & Huan, S. (2000). Store-operated calcium entry inactivates at the germinal vesicle breakdown stage of Xenopus meiosis. J. Biol. Chem. 275, 38710–15.CrossRefGoogle ScholarPubMed
Parekh, A.B. & Putney, J.W. (2005). Store-operated calcium channels. Physiol. Rev. 85, 757–810.CrossRefGoogle ScholarPubMed
Prakriya, M. & Lewis, R.S. (2015). Store-operated calcium channels. Physiol. Rev. 95, 1383–436.CrossRefGoogle ScholarPubMed
Preston, S.F., Sha'afi, R.I. & Berlin, R.D. (1991). Regulation of Ca2+ influx during mitosis: Ca2+ influx and depletion of intracellular Ca2+ stores are coupled in interphase but not mitosis. Cell Regul. 2, 915–25.CrossRefGoogle Scholar
Russa, A.D., Ishikita, N., Masu, K., Akutsu, H., Saino, T. & Satoh, Y. (2008). Microtubule remodeling mediates the inhibition of store-operated calcium entry (SOCE) during mitosis in COS-7 cells. Arch. Histol. Cytol. 71, 249–63.CrossRefGoogle ScholarPubMed
Scharenberg, A.M., Humphries, L.A. & Rawlings, D.J. (2007). Calcium signaling and cell-fate choice in B cells. Nat. Rev. Immunol. 7, 778–89.CrossRefGoogle ScholarPubMed
Smyth, J.T. & Putney, J.W. (2012). Regulation of store-operated calcium entry during cell division. Biochem. Soc. Trans. 40, 119–23.CrossRefGoogle ScholarPubMed
Smyth, J.T., DeHaven, W.I., Bird, G.S. & Putney, J.W., Jnr (2007). Role of the microtubule cytoskeleton in the function of the store-operated Ca2+ channel activator STIM1. J. Cell Sci. 120, 3762–71.CrossRefGoogle ScholarPubMed
Smyth, J.T., Petranka, J.G., Boyles, R.R., DeHaven, W.I., Fukushima, M., Johnson, K.L., Williams, J.G. & Putney, J.W., Jnr (2009). Phosphorylation of STIM1 underlies suppression of store-operated calcium entry during mitosis. Nat. Cell Biol. 11, 1465–72.CrossRefGoogle ScholarPubMed
Tani, D., Monteilh-Zoller, M.K., Fleig, A. & Penner, R. (2007). Cell cycle-dependent regulation of store-operated ICRAC and Mg2+-nucleotide-regulated MagNuM (TRPM7) currents. Cell Calcium 41, 249–60.CrossRefGoogle ScholarPubMed
Urven, L.E., Yabe, T. & Pelegri, F. (2006). A role for non-muscle myosin II function in furrow maturation in the early zebrafish embryo. J. Cell Sci. 119, 4342–52.CrossRefGoogle ScholarPubMed
van Roy, F. & Berx, G. (2008). The cell–cell adhesion molecule E-cadherin. Cell Mol. Life Sci. 65, 3756–88.CrossRefGoogle ScholarPubMed
Webb, S.E. & Miller, A.L. (2007). Ca2+ signaling during embryonic cytokinesis in animal systems. In Calcium: A Matter of Life and Death (eds Krebs, J. & Michalak, M.), pp. 445–70. Amsterdam, The Netherlands: Elsevier, B.V. CrossRefGoogle Scholar
Webb, S.E., Fluck, R.A. & Miller, A.L. (2011). Calcium signaling during the early development of medaka and zebrafish. Biochimie 93, 2112–25.CrossRefGoogle ScholarPubMed
Webb, S.E., Goulet, C., Chan, C.M., Yuen, M.Y.F. & Miller, A.L. (2013). Biphasic assembly of the contractile apparatus during the first two cell division cycles in zebrafish embryos. Zygote 22, 218–28.CrossRefGoogle ScholarPubMed
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 zebrafish embryos. Dev. Biol. 192, 78–92.CrossRefGoogle ScholarPubMed
Webb, S.E. & Miller, A.L. (2013). Microinjecting holo-aequorin into dechorionated and intact zebrafish embryos. Cold Spring Harb. Protoc. doi:10.1101/pdb.prot072967.CrossRefGoogle ScholarPubMed
Westerfield, M. (1994). The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Brachydanio rerio). Eugene, Oregon: University of Oregon Press.Google Scholar
Wu, M.M., Buchanan, J., Luik, R.M. & Lewis, R.S. (2006). Ca2+ store depletion causes STIM1 to accumulate in ER regions closely associated with the plasma membrane. J. Cell Biol. 174, 803–13.CrossRefGoogle ScholarPubMed