Advertisement

Science China Life Sciences

, Volume 61, Issue 11, pp 1352–1368 | Cite as

Identification of Ca2+ signaling components in neural stem/progenitor cells during differentiation into neurons and glia in intact and dissociated zebrafish neurospheres

  • Man Kit Tse
  • Ting Shing Hung
  • Ching Man Chan
  • Tiffany Wong
  • Mike Dorothea
  • Catherine Leclerc
  • Marc Moreau
  • Andrew L. Miller
  • Sarah E. WebbEmail author
Research Paper
  • 97 Downloads

Abstract

The development of the CNS in vertebrate embryos involves the generation of different sub-types of neurons and glia in a complex but highly-ordered spatio-temporal manner. Zebrafish are commonly used for exploring the development, plasticity and regeneration of the CNS, and the recent development of reliable protocols for isolating and culturing neural stem/progenitor cells (NSCs/NPCs) from the brain of adult fish now enables the exploration of mechanisms underlying the induction/specification/differentiation of these cells. Here, we refined a protocol to generate proliferating and differentiating neurospheres from the entire brain of adult zebrafish. We demonstrated via RT-qPCR that some isoforms of ip3r, ryr and stim are upregulated/downregulated significantly in differentiating neurospheres, and via immunolabelling that 1,4,5-inositol trisphosphate receptor (IP3R) type-1 and ryanodine receptor (RyR) type-2 are differentially expressed in cells with neuron- or radial glial-like properties. Furthermore, ATP but not caffeine (IP3R and RyR agonists, respectively), induced the generation of Ca2+ transients in cells exhibiting neuron- or glial-like morphology. These results indicate the differential expression of components of the Ca2+-signaling toolkit in proliferating and differentiating cells. Thus, given the complexity of the intact vertebrate brain, neurospheres might be a useful system for exploring neurodegenerative disease diagnosis protocols and drug development using Ca2+ signaling as a read-out.

Keywords

Ca2+ signaling neurospheres zebrafish neural stem/progenitor cells differentiation IP3 receptors ryanodine receptors STIM and Orai 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgements

We would like to thank Dr. Jeffrey J. Kelu (Division of Life Science, HKUST) for helping us with the statistics. This work was supported by the ANR/RGC Joint Research Scheme Award (A-HKUST601/13), the HK RGC General Research Fund awards (662113, 16101714, 16100115) and Funding from the HKITC (ITCPD/17-9).

References

  1. Adolf, B., Chapouton, P., Lam, C.S., Topp, S., Tannhäuser, B., Strähle, U., Götz, M., and Bally-Cuif, L. (2006). Conserved and acquired features of adult neurogenesis in the zebrafish telencephalon. Dev Biol 295, 278–293.CrossRefPubMedGoogle Scholar
  2. Akamatsu, W., Fujihara, H., Mitsuhashi, T., Yano, M., Shibata, S., Hayakawa, Y., Okano, H.J., Sakakibara, S.I., Takano, H., Takano, T., et al. (2005). The RNA-binding protein HuD regulates neuronal cell identity and maturation. Proc Natl Acad Sci USA 102, 4625–4630.CrossRefPubMedGoogle Scholar
  3. Alzayady, K.J., Sebé-Pedrós, A., Chandrasekhar, R., Wang, L., Ruiz-Trillo, I., and Yule, D.I. (2015). Tracing the evolutionary history of inositol 1,4,5-trisphosphate receptor: insights from analysis of Capsaspora owczarzaki Ca2+ release channel orthologues. Mol Biol Evol 32, 2236–2253.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Azari, H., Rahman, M., Sharififar, S., and Reynolds, B.A. (2010). Isolation and expansion of the adult mouse neural stem cells using the neurosphere assay. J Vis Exp in press doi: 10.3791/2393.Google Scholar
  5. Barami, K., Iversen, K., Furneaux, H., and Goldman, S.A. (1995). Hu protein as an early marker of neuronal phenotypic differentiation by subependymal zone cells of the adult songbird forebrain. J Neurobiol 28, 82–101.CrossRefPubMedGoogle Scholar
  6. Barnes, E.M., and Mandel, P. (1981). Calcium transport by primary cultured neuronal and glial cells from chick embryo brain. J Neurochem 36, 82–85.CrossRefPubMedGoogle Scholar
  7. Berridge, M.J., Bootman, M.D., and Roderick, H.L. (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4, 517–529.CrossRefPubMedGoogle Scholar
  8. Bolsover, S.R. (2005). Calcium signalling in growth cone migration. Cell Calcium 37, 395–402.CrossRefPubMedGoogle Scholar
  9. Bretaud, S., Allen, C., Ingham, P.W., and Bandmann, O. (2007). P53- dependent neuronal cell death in a DJ-1-deficient zebrafish model of Parkinson’s disease. J Neurochem 100, 1626–1635.PubMedGoogle Scholar
  10. Brewer, G.J., and Torricelli, J.R. (2007). Isolation and culture of adultneurons and neurospheres. Nat Protoc 2, 1490–1498.CrossRefPubMedGoogle Scholar
  11. Casadei, R., Pelleri, M.C., Vitale, L., Facchin, F., Lenzi, L., Canaider, S., Strippoli, P., and Frabetti, F. (2011). Identification of housekeeping genes suitable for gene expression analysis in the zebrafish. Gene Express Patterns 11, 271–276.CrossRefGoogle Scholar
  12. Chan, C.M., Chen, Y., Hung, T.S., Miller, A.L., Shipley, A.M., and Webb, S.E. (2015). Inhibition of SOCE disrupts cytokinesis in zebrafish embryos via inhibition of cleavage furrow deepening. Int J Dev Biol 59, 289–301.CrossRefPubMedGoogle Scholar
  13. Chan, C.M., Aw, J.T.M., Webb, S.E., and Miller, A.L. (2016a). SOCE proteins, STIM1 and Orai1, are localized to the cleavage furrow during cytokinesis of the first and second cell division cycles in zebrafish embryos. Zygote 24, 880–889.CrossRefPubMedGoogle Scholar
  14. Chan, H.Y.S., Cheung, M.C., Gao, Y., Miller, A.L., and Webb, S.E. (2016b). Expression and reconstitution of the bioluminescent Ca2+ reporter aequorin in human embryonic stem cells, and exploration of the presence of functional IP3 and ryanodine receptors during the early stages of their differentiation into cardiomyocytes. Sci China Life Sci 59, 811–824.CrossRefPubMedGoogle Scholar
  15. Cheek, T.R., Moreton, R.B., Berridge, M.J., Stauderman, K.A., Murawsky, M.M., and Bootman, M.D. (1993). Quantal Ca2+ release from caffeinesensitive stores in adrenal chromaffin cells. J Biol Chem 268, 27076–27083.PubMedGoogle Scholar
  16. Cortés-Campos, C., Letelier, J., Ceriani, R., and Whitlock, K.E. (2015). Zebrafish adult-derived hypothalamic neurospheres generate gonadotropin- releasing hormone (GnRH) neurons. Biol Open 4, 1077–1086.CrossRefPubMedPubMedCentralGoogle Scholar
  17. Daynac, M., and Petritsch, C.K. (2017). Regulation of asymmetric cell division in mammalian neural stem cell and cancer precursor cells. Results Probl Cell Diff 61, 375–399.CrossRefGoogle Scholar
  18. Deitmer, J.W., Verkhratsky, A.J., and Lohr, C. (1998). Calcium signalling in glial cells. Cell Calcium 24, 405–416.CrossRefPubMedGoogle Scholar
  19. Deleyrolle, L.P., and Reynolds, B.A. (2009). Isolation, and expansion, and differentiation of adult mammalian neural stem and progenitor cells using the neurosphere assay. Methods Mol Biol 549, 91–101.CrossRefPubMedGoogle Scholar
  20. Dinno, A. (2015). Nonparametric pairwise multiple comparisons in independent groups using Dunn’s test. Stata J 15, 292–300.CrossRefGoogle Scholar
  21. Faure, A.V., Grunwald, D., Moutin, M.-J., Hilly, M., Mauger, J.-P., Marty, I., De Waard, M., Villaz, M., and Albrieux, M. (2002). Developmental expression of the calcium release channels during early neurogenesis of the mouse cerebral cortex. Eur J Neurosci 14, 1613–1622.CrossRefGoogle Scholar
  22. Ferris, C.D., Huganir, R.L., and Snyder, S.H. (1990). Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosterically regulated by adenine nucleotides. Proc Natl Acad Sci USA 87, 2147–2151.CrossRefPubMedGoogle Scholar
  23. Fiedler, M.J., and Nathanson, M.H. (2011). The type I inositol 1,4,5-trisphosphate receptor interacts with protein 4.1N to mediate neurite formation through intracellular Ca2+ waves. Neurosignals 19, 75–85.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Fong, H., Hohenstein, K.A., and Donovan, P.J. (2008). Regulation of selfrenewal and pluripotency by Sox2 in human embryonic stem cells. Stem Cells 26, 1931–1938.CrossRefPubMedGoogle Scholar
  25. Furlan, G., Cuccioli, V., Vuillemin, N., Dirian, L., Muntasell, A.J., Coolen, M., Dray, N., Bedu, S., Houart, C., Beaurepaire, E., et al. (2017). Lifelong neurogenic activity of individual neural stem cells and continuous growth establish an outside-in architecture in the teleost pallium. Curr Biol 27, 3288–3301.e3.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Furuichi, T., Furutama, D., Hakamata, Y., Nakai, J., Takeshima, H., and Mikoshiba, K. (1994). Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain. J Neurosci 14, 4794–4805.CrossRefPubMedGoogle Scholar
  27. Goffart, N., Kroonen, J., and Rogister, B. (2013). Glioblastoma-initiating cells: relationship with neural stem cells and the micro-environment. Cancers 5, 1049–1071.CrossRefPubMedPubMedCentralGoogle Scholar
  28. Grandel, H., Kaslin, J., Ganz, J., Wenzel, I., and Brand, M. (2006). Neural stem cells and neurogenesis in the adult zebrafish brain: origin, proliferation dynamics, migration and cell fate. Dev Biol 295, 263–277.CrossRefPubMedGoogle Scholar
  29. Gu, X., Olson, E., and Spitzer, N. (1994). Spontaneous neuronal calcium spikes and waves during early differentiation. J Neurosci 14, 6325–6335.CrossRefPubMedGoogle Scholar
  30. Guan, C.B., Xu, H.T., Jin, M., Yuan, X.B., and Poo, M.M. (2007). Longrange Ca2+ signaling from growth cone to soma mediates reversal of neuronal migration induced by Slit-2. Cell 129, 385–395.CrossRefPubMedGoogle Scholar
  31. Guo, W., Patzlaff, N.E., Jobe, E.M., and Zhao, X. (2012). Isolation of multipotent neural stem or progenitor cells from both the dentate gyrus and subventricular zone of a single adult mouse. Nat Protoc 7, 2005–2012.CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hakamata, Y., Nakai, J., Takeshima, H., and Imoto, K. (1992). Primary structure and distribution of a novel ryanodine receptor/calcium release channel from rabbit brain. FEBS Lett 312, 229–235.CrossRefPubMedGoogle Scholar
  33. Hao, B., Webb, S.E., Miller, A.L., and Yue, J. (2016). The role of Ca2+ signaling on the self-renewal and neural differentiation of embryonic stem cells (ESCs). Cell Calcium 59, 67–74.CrossRefPubMedGoogle Scholar
  34. Henley, J., and Poo, M. (2004). Guiding neuronal growth cones using Ca2+ signals. Trends Cell Biol 14, 320–330.CrossRefPubMedPubMedCentralGoogle Scholar
  35. Hinsch, K., and Zupanc, G.K.H. (2007). Generation and long-term persistence of new neurons in the adult zebrafish brain: a quantitative analysis. Neuroscience 146, 679–696.CrossRefPubMedGoogle Scholar
  36. Hol, E.M., and Pekny, M. (2015). Glial fibrillary acidic protein (GFAP) and the astrocyte intermediate filament system in diseases of the central nervous system. Curr Opin Cell Biol 32, 121–130.CrossRefPubMedGoogle Scholar
  37. Johnson, K., Barragan, J., Bashiruddin, S., Smith, C.J., Tyrrell, C., Parsons, M.J., Doris, R., Kucenas, S., Downes, G.B., Velez, C.M., et al. (2016). Gfap-positive radial glial cells are an essential progenitor population for later-born neurons and glia in the zebrafish spinal cord. Glia 64, 1170–1189.CrossRefPubMedPubMedCentralGoogle Scholar
  38. Kaslin, J., Ganz, J., and Brand, M. (2008). Proliferation, neurogenesis and regeneration in the non-mammalian vertebrate brain. Philos Trans R Soc B-Biol Sci 363, 101–122.CrossRefGoogle Scholar
  39. Kaslin, J., Ganz, J., Geffarth, M., Grandel, H., Hans, S., and Brand, M. (2009). Stem cells in the adult zebrafish cerebellum: initiation and maintenance of a novel stem cell niche. J Neurosci 29, 6142–6153.CrossRefPubMedGoogle Scholar
  40. Kim, C.H., Ueshima, E., Muraoka, O., Tanaka, H., Yeo, S.Y., Huh, T.L., and Miki, N. (1996). Zebrafish elav/HuC homologue as a very early neuronal marker. Neurosci Lett 216, 109–112.CrossRefPubMedGoogle Scholar
  41. Lai, F.A., Dent, M., Wickenden, C., Xu, L., Kumari, G., Misra, M., Lee, H. B., Sar, M., and Meissner, G. (1992). Expression of a cardiac Ca2+-release channel isoform in mammalian brain. Biochem J 288, 553–564.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lam, C.S., März, M., and Strähle, U. (2009). gfap and nestin reporter lines reveal characteristics of neural progenitors in the adult zebrafish brain. Dev Dyn 238, 475–486.CrossRefPubMedGoogle Scholar
  43. Lanner, J.T., Georgiou, D.K., Joshi, A.D., and Hamilton, S.L. (2010). Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harbor Perspect Biol 2, a003996–a003996.CrossRefGoogle Scholar
  44. Leclerc, C., Webb, S.E., Daguzan, C., Moreau, M., and Miller, A.L. (2000). Imaging patterns of calcium transients during neural induction in Xenopus laevis embryos. J Cell Sci 113, 3519–3529.PubMedGoogle Scholar
  45. Leclerc, C., Lee, M., Webb, S.E., Moreau, M., and Miller, A.L. (2003). Calcium transients triggered by planar signals induce the expression of ZIC3 gene during neural induction in Xenopus. Dev Biol 261, 381–390.CrossRefPubMedGoogle Scholar
  46. Leclerc, C., Haeich, J., Aulestia, F.J., Kilhoffer, M.C., Miller, A.L., Néant, I., Webb, S.E., Schaeffer, E., Junier, M.P., Chneiweiss, H., et al. (2016). Calcium signaling orchestrates glioblastoma development: facts and conjunctures. Biochim Biophys Acta 1863, 1447–1459.CrossRefPubMedGoogle Scholar
  47. Lee, K.W., Webb, S.E., and Miller, A.L. (2003). Ca2+ released via IP3 receptors is required for furrow deepening during cytokinesis in zebrafish embryos. Int J Dev Biol 47, 411–421.PubMedGoogle Scholar
  48. Lopez-Ramirez, M.A., Calvo, C.F., Ristori, E., Thomas, J.L., and Nicoli, S. (2016). Isolation and culture of adult zebrafish brain-derived neurospheres. J Vis Exp (108), 53617.Google Scholar
  49. Makhija, D.T., and Jagtap, A.G. (2014). Studies on sensitivity of zebrafish as a model organism for Parkinson’s disease: comparison with rat model. J Pharmacol Pharmacother 5, 39–46.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Marichal, N., García, G., Radmilovich, M., Trujillo-Cenóz, O., and Russo, R.E. (2009). Enigmatic central canal contacting cells: immature neuronsin “Standby Mode”? J Neurosci 29, 10010–10024.CrossRefPubMedPubMedCentralGoogle Scholar
  51. McKeown, S.J., Mohsenipour, M., Bergner, A.J., Young, H.M., and Stamp, L.A. (2017). Exposure to GDNF enhances the ability of enteric neural progenitors to generate an enteric nervous system. Stem Cell Rep 8, 476–488.CrossRefGoogle Scholar
  52. Mirsadeghi, S., Shahbazi, E., Hemmesi, K., Nemati, S., Baharvand, H., Mirnajafi-Zadeh, J., and Kiani, S. (2017). Development of membrane ion channels during neural differentiation from human embryonic stem cells. Biochem Biophys Res Commun 491, 166–172.CrossRefPubMedGoogle Scholar
  53. Morgan, P.J., Hübner, R., Rolfs, A., and Frech, M.J. (2013). Spontaneous calcium transients in human neural progenitor cells mediated by transient receptor potential channels. Stem Cells Dev 22, 2477–2486.CrossRefPubMedGoogle Scholar
  54. Mori, F., Fukaya, M., Abe, H., Wakabayashi, K., and Watanabe, M. (2000). Developmental changes in expression of the three ryanodine receptor mRNAs in the mouse brain. Neurosci Lett 285, 57–60.CrossRefPubMedGoogle Scholar
  55. Morshead, C.M., Reynolds, B.A., Craig, C.G., McBurney, M.W., Staines, W.A., Morassutti, D., Weiss, S., and van der Kooy, D. (1994). Neural stem cells in the adult mammalian forebrain: a relatively quiescent subpopulation of subependymal cells. Neuron 13, 1071–1082.CrossRefPubMedGoogle Scholar
  56. Murayama, T., and Ogawa, Y. (1996). Properties of Ryr3 ryanodine receptor isoform in mammalian brain. J Biol Chem 271, 5079–5084.CrossRefPubMedGoogle Scholar
  57. Newman, M., Ebrahimie, E., and Lardelli, M. (2014). Using the zebrafish model for Alzheimer’s disease research. Front Genet 5, 189.PubMedPubMedCentralGoogle Scholar
  58. Pastrana, E., Silva-Vargas, V., and Doetsch, F. (2011). Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8, 486–498.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Ray, B., Chopra, N., Long, J.M., and Lahiri, D.K. (2014). Human primary mixed brain cultures: preparation, differentiation, characterization and application to neuroscience research. Mol Brain 7, 63.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Reynolds, B.A., and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707–1710.CrossRefPubMedGoogle Scholar
  61. Ringler, S.L., Aye, J., Byrne, E., Anderson, M., and Turner, C.P. (2008). Effects of disrupting calcium homeostasis on neuronal maturation: early inhibition and later recovery. Cell Mol Neurobiol 28, 389–409.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ristori, E., Lopez-Ramirez, M.A., Narayanan, A., Hill-Teran, G., Moro, A., Calvo, C.F., Thomas, J.L., and Nicoli, S. (2015). A Dicer-miR-107 interaction regulates biogenesis of specific miRNAs crucial for neurogenesis. Dev Cell 32, 546–560.CrossRefPubMedGoogle Scholar
  63. Rosenberg, S.S., and Spitzer, N.C. (2011). Calcium signaling in neuronal development. Cold Spring Harbor Perspect Biol 3, a004259.CrossRefGoogle Scholar
  64. Salter, M., and Hicks, J. (1994). ATP-evoked increases in intracellular calcium in neurons and glia from the dorsal spinal cord. J Neurosci 14, 1563–1575.CrossRefPubMedGoogle Scholar
  65. Schmidt, R., Strähle, U., and Scholpp, S. (2013). Neurogenesis in zebrafish —from embryo to adult. Neural Dev 8, 3.CrossRefPubMedPubMedCentralGoogle Scholar
  66. Sharp, A.H., Nucifora, F.C., Blondel, O., Sheppard, C.A., Zhang, C., Snyder, S.H., Russell, J.T., Ryugoand, D.K., and Ross, C.A. (1999). Differential cellular expression of isoforms of inositol 1,4,5-triphosphate receptors in neurons and glia in brain. J Comp Neurol 406, 207–220.CrossRefPubMedGoogle Scholar
  67. Simpson, P.B., Holtzclaw, L.A., Langley, D.B., and Russell, J.T. (1998). Characterization of ryanodine receptors in oligodendrocytes, type 2 astrocytes, and O-2A progenitors. J Neurosci Res 52, 468–482.CrossRefPubMedGoogle Scholar
  68. Schneider, C.A., Rasband, W.S., and Eliceiri, K.W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671–675.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Somasundaram, A., Shum, A.K., McBride, H.J., Kessler, J.A., Feske, S., Miller, R.J., and Prakriya, M. (2014). Store-operated CRAC channels regulate gene expression and proliferation in neural progenitor cells. J Neurosci 34, 9107–9123.CrossRefPubMedPubMedCentralGoogle Scholar
  70. Takei, K., Shin, R.M., Inoue, T., Kato, K., and Mikoshiba, K. (1998). Regulation of nerve growth mediated by inositol 1,4,5-trisphosphate receptors in growth cones. Science 282, 1705–1708.CrossRefPubMedGoogle Scholar
  71. Torrado, E.F., Gomes, C., Santos, G., Fernandes, A., Brites, D., and Falcão, A.S. (2014). Directing mouse embryonic neurosphere differentiation toward an enriched neuronal population. Int J Dev Neurosci 37, 94–99.CrossRefPubMedGoogle Scholar
  72. Toth, A.B., Shum, A.K., and Prakriya, M. (2016). Regulation of neurogenesis by calcium signaling. Cell Calcium 59, 124–134.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Urbán, N., and Guillemot, F. (2014). Neurogenesis in the embryonic and adult brain: same regulators, different roles. Front Cell Neurosci 8, 396.CrossRefPubMedPubMedCentralGoogle Scholar
  74. Usachev, Y., Shmigol, A., Pronchuk, N., Kostyuk, P., and Verkhratsky, A. (1993). Caffeine-induced calcium release from internal stores in cultured rat sensory neurons. Neuroscience 57, 845–859.CrossRefPubMedGoogle Scholar
  75. Weissman, T.A., Riquelme, P.A., Ivic, L., Flint, A.C., and Kriegstein, A.R. (2004). Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43, 647–661.CrossRefPubMedGoogle Scholar
  76. Whalley, K., Gögel, S., Lange, S., and Ferretti, P. (2009). Changes in progenitor populations and ongoing neurogenesis in the regenerating chick spinal cord. Dev Biol 332, 234–245.CrossRefPubMedGoogle Scholar
  77. Wie, M.B., Koh, J.Y., Won, M.H., Lee, J.C., Shin, T.K., Moon, C.J., Ha, H. J., Park, S.M., and Kim, H.C. (2001). BAPTA/AM, an intracellular calcium chelator, induces delayed necrosis by lipoxygenase-mediated free radicals in mouse cortical cultures. Prog Neuropsychopharmacol Biol Psychiatry 25, 1641–1659.CrossRefPubMedGoogle Scholar
  78. Wu, H.H., Brennan, C., and Ashworth, R. (2011). Ryanodine receptors, a family of intracellular calcium ion channels, are expressed throughout early vertebrate development. BMC Res Notes 4, 541.CrossRefPubMedPubMedCentralGoogle Scholar
  79. Yuan, X., Curtin, J., Xiong, Y., Liu, G., Waschsmann-Hogiu, S., Farkas, D. L., Black, K.L., and Yu, J.S. (2004). Isolation of cancer stem cells from adult glioblastoma multiforme. Oncogene 23, 9392–9400.CrossRefPubMedGoogle Scholar
  80. Zhang, S., Fritz, N., Ibarra, C., and Uhlén, P. (2011). Inositol 1,4,5-trisphosphate receptor subtype-specific regulation of calcium oscillations. Neurochem Res 36, 1175–1185.CrossRefPubMedPubMedCentralGoogle Scholar
  81. Zheng, J.Q., and Poo, M. (2007). Calcium signaling in neuronal motility. Annu Rev Cell Dev Biol 23, 375–404.CrossRefPubMedGoogle Scholar

Copyright information

© Science China Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Man Kit Tse
    • 1
  • Ting Shing Hung
    • 1
  • Ching Man Chan
    • 1
  • Tiffany Wong
    • 1
  • Mike Dorothea
    • 1
  • Catherine Leclerc
    • 2
  • Marc Moreau
    • 2
  • Andrew L. Miller
    • 1
  • Sarah E. Webb
    • 1
    Email author
  1. 1.Division of Life Science & State Key Laboratory of Molecular NeuroscienceHKUSTHong KongChina
  2. 2.Centre de Biologie du Développement (CBD), Centre de Biologie Intégrative (CBI)Université de Toulouse, CNRS, UPSToulouseFrance

Personalised recommendations