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Local and Global Spontaneous Calcium Events Regulate Neurite Outgrowth and Onset of GABAergic Phenotype during Neural Precursor Differentiation
Open accessAbstract
Neural stem cells can generate in vitro progenitors of the three main cell lineages found in the CNS. The signaling pathways underlying the acquisition of differentiated phenotypes in these cells are poorly understood. Here we tested the hypothesis that Ca(2+) signaling controls differentiation of neural precursors. We found low-frequency global and local Ca(2+) transients occurring predominantly during early stages of differentiation. Spontaneous Ca(2+) signals in individual precursors were not synchronized with Ca(2+) transients in surrounding cells. Experimentally induced changes in the frequency of local Ca(2+) signals and global Ca(2+) rises correlated positively with neurite outgrowth and the onset of GABAergic neurotransmitter phenotype, respectively. NMDA receptor activity was critical for alterations in neuronal morphology but not for the timing of the acquisition of the neurotransmitter phenotype. Thus, spontaneous Ca(2+) signals are an intrinsic property of differentiating neurosphere-derived precursors. Their frequency may specify neuronal morphology and acquisition of neurotransmitter phenotype.
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“These findings support our model in which CYFIP1 regulation of calcium channel subunits compromise intracellular calcium levels, resulting in delayed axonal development10,84,85 (Fig. 7).”
From CYFIP1 governs the development of cortical axons by modulating calcium availability (2025) · cites this paper as [84]
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Calcium signalling: dynamics, homeostasis and remodelling
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“However, spontaneous activity has been shown to result in calcium transients and to be critical for neurite outgrowth and pathfinding (Spitzer et al., 2000; Ciccolini et al., 2003; Tang et al., 2003).”
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BackgroundAxon diameter and axonal transport: In vivo and in vitro effects of androgens
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“In addition, spontaneous Ca 2+ signals specify neuronal morphology and dictate neurotransmitter choice in mice neuronal progenitor cells [120], whereas the onset of Ca 2+ spiking is a pre-requisite for adult liver stem cells to acquire a myocardial phenotype [121].”
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Timing in Cellular Ca2+ Signaling
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“Ca2+ signals observed during cellular differentiation [6,23,24], reinforce differentiative events and possibly impact their intrinsic timing.”
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“Moreover, the importance of calcium signaling for differentiation of NPC has been studied [67, 68], and direct evidence for the participation of P2Y1 receptor-activated pathways in the early development has been provided by Scemes et al.”
BackgroundResende, R. R., Alves, A. S., Britto, L. R. G., & Ulrich, H. (2008) · Experimental Cell Research · doi:10.1016/j.yexcr.2008.01.003 · Cited by 58
Warm, D., Schroer, J., & Sinning, A. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.807969 · Cited by 65
“Meanwhile, spontaneous calcium activity in parallel also critically impacts the further specification of neuronal phenotypes (Ciccolini et al., 2003; Borodinsky et al., 2004), which is no surprise considering the tight link between neuronal gene expression and neuronal activity (Flavell and Greenberg, 2008).”
BackgroundGlaser, T., Resende, R. R., & Ulrich, H. (2013) · Cell Communication and Signaling · doi:10.1186/1478-811x-11-12 · Cited by 67
“Surprisingly, spontaneous Ca signals in individual precursors were not synchronized with Ca transients in surrounding cells, indicating the existence of a different pathway, not depending on connexin 43-hemichannel-mediated intercellular Ca signaling [41].”
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Self-citationDendritic plasticity of CA1 pyramidal neurons after transient global ischemia
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“…plays a crucial role in the regulation of neurotransmitter release, synaptic plasticity, neurite outgrowth, and neurodegeneration (Berridge, 1998; Ciccolini et al., 2003), and several studies have suggested an altered calcium homeostasis in the pathophysiology of bipolar disorder (Emamghoreishi…”
Role of Nav1.9 in activity-dependent axon growth in motoneurons
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“As the role of mAchR in inducing NSC proliferation and differentiation in vitro has been established, further study will focus on details of the association between calcium transients and NSC differentiation (Ciccolini et al., 2003).”
BackgroundMoccia, F. D., Bonetti, E., Dragoni, S., Fontana, J. M., Lodola, F., Berra‐Romani, R., Laforenza, U., Rosti, V., & Tanzi, F. (2012) · Current Signal Transduction Therapy · doi:10.2174/157436212800376672 · Cited by 44
Phosphatidylcholine restores neuronal plasticity of neural stem cells under inflammatory stress
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“ca2+ is an earlyresponse second messenger and as such plays a key role in a number of physiological processes including cell proliferation, differentiation and apoptosis as well as a wide variety of specific neuronal processes including dendritic spine growth, synaptic plasticity and neurotransmission (Berridge et al.…”
Homeostatic activity-dependent paradigm for neurotransmitter specification.
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Monitoring neuronal calcium signalling using a new method for ratiometric confocal calcium imaging
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“transients in growth cones in frog and mouse [25,26].”
BackgroundRole of calcium and kinases on the neurotrophic effect induced by γ‐aminobutyric acid
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“…affect several parameters of neuronal maturation, such as phenotypic expression, dendritic arbor complexity, axon guidance, and synaptic strength (Mattson et al., 1988; Rajan and Cline, 1998; Gomez and Spitzer, 1999; Wu et al., 1999; Wilson et al., 2000; Sin et al., 2002; Ciccolini et al., 2003).”
BackgroundExpression of calcium transporters in the retina of the tiger salamander (Ambystoma tigrinum)
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“Because Ca2 -regulated pathways can distinguish between calcium signals of differing properties, Ca2 can control a variety of different functions in different parts of the cell (Delmas and Brown, 2003).”
BackgroundRelationship between GABAergic interneurons migration and early neocortical network activity
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GABA Not Only a Neurotransmitter: Osmotic Regulation by GABAAR Signaling
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“In particular, changes (receptor-mediated) in intracellular Ca are known to be important intracellular signals in such responses (Ciccolini et al., 2003).”
BackgroundInfluentialSecondo, A., Esposito, A., Sirabella, R., Boscia, F., Pannaccione, A., Molinaro, P., Cantile, M., Ciccone, R., Sisalli, M., Scorziello, A., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.555516 · Cited by 29
“(29) reported that neurons become increasingly competent at Ca(2) signaling as differentiation proceeds and show an increased amount of Ca(2) in the ER in the late phase of the process (29).”
BackgroundIn Vivo Calcium Dynamics During Neural Crest Cell Migration and Patterning Using GCaMP3
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“Thus, our in vivo temporal measurements of NC cell calcium transients were comparable with recorded measurements in other cell types (Ciccolini et al., 2003; Gu and Spitzer, 1995; O'Donovan, 1999), but had unique dynamics compared to in vitro NC cell analysis.”
González‐Cota, A. L., Martínez-Flores, D., Rosendo‐Pineda, M. J., & Vaca, L. A. (2024) · Cell Calcium · doi:10.1016/j.ceca.2024.102856 · Cited by 40
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“[63] reported that P2 receptor activation increases neurite extension and GABAergic differentiation.”
BackgroundIntracellular Ca2+ Signals to Reconstruct A Broken Heart: Still A Theoretical Approach?
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“This has been shown in mouse primary culture of NSCs from embryonic day 14 where both global and local spontaneous Ca2þ signals were shown to be more frequent at early stages of neural precursor differentiation (Ciccolini et al., 2003).”
BackgroundNitric Oxide–mediated Modulation of Synaptic Activity by Astrocytic P2Y Receptors
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“Local and global spontaneous Ca 2+ oscillations are key regulators for onset of neuronal phenotype during neural precursor differentiation and cell specifi cation in the developing nervous system ( Ciccolini et al., 2003 ).”
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“An intriguing observation is that neurosphere-forming cells from various regions generate mostly GABAergic neurons (Hitoshi et al., 2002; Parmar et al., 2002; Ciccolini et al., 2003; Hack et al., 2004).”
BackgroundSpatiotemporal integration of developmental cues in neural development
Borodinsky, L. N., Belgacem, Y. H., Swapna, I., Visina, O., Balashova, O. A., Sequerra, E. B., Tu, M. K., Levin, J. B., Spencer, K. A., Castro, P. A., et al. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22254 · Cited by 21
“, 2003) to neurotransmitter specification (Gu and Spitzer, 1995; Ciccolini et al., 2003; Borodinsky et al., 2004).”
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Bikbaev, A. F., Ciuraszkiewicz, A., Heck, J., Klatt, O., Freund, R., Mitlöhner, J., Lacalle, S. E., Sun, M., Repetto, D., Frischknecht, R., et al. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.1707-19.2020 · Cited by 41
“These outcomes corroborate previous reports showing an important role of spontaneous Ca21 transients in regulation of the neurite outgrowth and branching (Ciccolini et al., 2003) and structural maturation of synapses (Choi et al., 2014).”
ResultViéro, C., & Dayanithi, G. (2008) · Progress in brain research · doi:10.1016/s0079-6123(08)00416-0 · Cited by 24
“Intracellular Ca concentration [Ca]i changes play a major role in the control of several neuronal functions (Burgoyne, 2007), notably during the development of the CNS (Ciccolini et al., 2003; Zamoner et al., 2007) and the PNS (Dayanithi et al.”
BackgroundInfluentialANO1/TMEM16A regulates process maturation in radial glial cells in the developing brain
Hong, G., Lee, S. H., Lee, B., Choi, J. H., Oh, S., Jang, Y., Hwang, E. M., Kim, H., Jung, J., Kim, I., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901067116 · Cited by 28
“Spontaneous Ca spikes are observed in cultured neural precursor cells and are correlated with neurite length (9).”
BackgroundGaleotti, N., Vivoli, E., Norcini, M., Bartolini, A., & Ghelardini, C. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.07.029 · Cited by 19
“Calcium is a ubiquitous intracellular signalling molecule that is required for initiating and regulating a wide range of neuronal functions, including neurotransmitter release, synaptic plasticity, neurite outgrowth, and neurodegeneration (Berridge, 1998; Ciccolini et al., 2003).”
Stradecki, H. M., Cohan, C. H., Raval, A. P., Dave, K. R., Reginensi, D., Gittens, R. A., Youbi, M., & Pérez‐Pinzón, M. A. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170057 · Cited by 23
“…an over-activation of the CA3 cells during ischemia and reperfusion caused the changes in CA1 morphology as calcium influx through NMDA receptors is necessary for dendritic outgrowth [119–121] and excessive dendritic outgrowth has been observed in states of over-activation such as epilepsy [122].”
Mizuno, K., Kurokawa, K., & Ohkuma, S. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.03.036 · Cited by 18
“Increased intracellular calcium concentration is a key factor to initiate and regulate a wide range of neuronal functions including neurotransmitter release, synaptic plasticity, neurite outgrowth, and neurodegeneration (Berridge, 1998; Ciccolini et al., 2003).”
Sun, C., Shao, J., Su, L., Zhao, J., Bi, J.-Z., Yang, S.-N., Zhang, S. L., Gao, J., & Miao, J. (2013) · Cell Transplantation · doi:10.3727/096368912x657413 · Cited by 18
Rubini, P., Milošević, J., Engelhardt, J., Al-Khrasani, M., Franke, H., Heinrich, A., Sperlágh, B., Schwarz, S., Schwarz, J., Nörenberg, W., et al. (2009) · Cell Calcium · doi:10.1016/j.ceca.2009.03.008 · Cited by 18
Deng, L., Ruan, Y., Chen, C., Frye, C. C., Xiong, W., Jin, X., Jones, K. J., Sengelaub, D. R., & Xu, X. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.12.018 · Cited by 16
“Activation of NMDA receptors stimulates dendritic outgrowth by increasing intracellular calcium (Cambray-Deakin and Burgoyne, 1992; Ciccolini et al., 2003; Hirai and Launey, 2000).”
BackgroundMizuno, K., Kurokawa, K., & Ohkuma, S. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07827.x · Cited by 17
“Calcium is a ubiquitous intracellular signaling molecule required for initiating and regulating a wide variety of neuronal functions including neurotransmitter release, synaptic plasticity, neurite outgrowth, and neurodegeneration (Berridge 1998; Ciccolini et al. 2003).”
BackgroundCoincidence detection enhances appropriate wiring of the nervous system.
Spitzer, N. (2004) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0401270101 · Cited by 17
Redondo, C., López-Toledano, M. A., Lobo, M. V. T., Gonzalo‐Gobernado, R., Reimers, D., Herranz, A. S., Paı́no, C. L., & Bazán, E. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21245 · Cited by 15
“In fact, Ca is a key regulator of multiple cellular processes, including neurite outgrowth in neurospherederived precursors (Ciccolini et al., 2003) and hypertrophy of astrocytes (Schubert et al.”
BackgroundInfluentialRebellato, P., Kaczyńska, D., Kanatani, S., Rayyes, I. A., Zhang, S., Villaescusa, C., Falk, A., Arenas, E., Hermanson, O., Louhivuori, L. M., et al. (2019) · Neuroscience · doi:10.1016/j.neuroscience.2019.01.015 · Cited by 17
Liljelund, P., Ferguson, C., Homanics, G. E., & Olsen, R. W. (2005) · Epilepsy Research · doi:10.1016/j.eplepsyres.2005.07.005 · Cited by 14
Use of calcium channel blockers after stroke is not associated with poor outcome
Dowlatshahi, D., Fang, J., Kawaja, M., & Hakim, A. (2006) · Journal of Neurology · doi:10.1007/s00415-006-0249-1 · Cited by 12
“More recent data suggest that neurite outgrowth requires activation of the calcium channels [3].”
BackgroundSamarasinghe, R. A., Kanuparthi, P. S., Greenamyre, J., DeFranco, D., & Maio, R. D. (2014) · Neurobiology of Disease · doi:10.1016/j.nbd.2014.06.020 · Cited by 11
Shao, J., Sun, C., Su, L., Zhao, J., Zhang, S. L., & Miao, J. (2012) · International Journal of Biochemistry and Cell Biology · doi:10.1016/j.biocel.2012.09.013 · Cited by 11
“Ca2+ imaging experiments were performed as described by Ciccolini et al. (2003). In brief, after loaded with 2 M Fluo3 plus pluronic F127 (Invitrogen, USA) for 30 min in an extracellular medium (EM) containing (in mM): 140 NaCl, 3 KCl, 1 MgCl2, 2 CaCl2, 10 HEPES, 10 glucose, the cells were monitored by using a laser s…”
MethodGakhar‐Koppole, N., Bengtson, C., Parlato, R., Horsch, K., Eckstein, V., & Ciccolini, F. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.06020.x · Cited by 11
“entiation, and that membrane depolarization with HiK increases the frequency of Ca signals, the number of cells displaying Ca transients and the number of neurons expressing GABA (Ciccolini et al., 2003).”
BackgroundInfluentialSelf-citationGafarov, F. (2006) · Journal of Integrative Neuroscience · doi:10.1142/s0219635206001136 · Cited by 11
“In this paper, we propose a new theoretical approach for description of activity-dependent evolution and self-wiring between binary neurons.”
BackgroundAltering the fate of stem cells from midgut of Heliothis virescens:the effect of calcium ions.
Loeb, M. (2005) · Archives of Insect Biochemistry and Physiology · doi:10.1002/arch.20060 · Cited by 11
Glyphosate‐based herbicide induces long‐lasting impairment in neuronal and glial differentiation
Reis, L. T. C., Raciti, M., Rodriguez, P. G., Joseph, B., Rayyes, I. A., Uhlén, P., Falk, A., Lima, S. T. D. C., & Ceccatelli, S. (2022) · Environmental Toxicology · doi:10.1002/tox.23549 · Cited by 9
Haijima, A., Lesmana, R., Shimokawa, N., Amano, I., Takatsuru, Y., & Koibuchi, N. (2017) · The Journal of Toxicological Sciences · doi:10.2131/jts.42.407 · Cited by 13
“Intracellular Ca2+ plays important roles in various neurodevelopmental processes including cell proliferation, differentiation, dendritic spine growth, synaptic plasticity and neurotransmission (Berridge et al., 2000; Ciccolini et al., 2003).”
Trinh, H.-H., Reid, J., Shin, E., Liapi, A., Parnavelas, J., & Nadarajah, B. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05194.x · Cited by 8
“Further, experimentally induced changes in the frequency of Ca2+ transients have been correlated with the onset of GABAergic phenotype in neural precursors (Ciccolini et al., 2003; for review, see Spitzer et al., 2004).”
BackgroundRac1, Rac3 GTPases and TPC2 are required for axonal outgrowth and migration of cortical interneuronsPreprint
Kounoupa, Z., Tivodar, S., Theodorakis, K., Kyriakis, D., Denaxa, M., & Karagogeos, D. (2022) · bioRxiv · doi:10.1101/2022.11.07.515393 · Cited by 7
“Spontaneous Ca+2 signaling was identified as an intrinsic characteristic of differentiating neurosphere precursors derived from embryonic striatal cells (Ciccolini et al., 2003).”
BackgroundMizuno, K., Kurokawa, K., & Ohkuma, S. (2014) · Journal of Neuroscience Research · doi:10.1002/jnr.23518 · Cited by 6
Su, L., Zhao, J., Zhao, B.-X., Zhang, S. L., & Miao, J.-Y. (2011) · International Journal of Biochemistry and Cell Biology · doi:10.1016/j.biocel.2011.07.002 · Cited by 7
Nair, S., Agrawal, N., & Hasan, G. (2007) · Invertebrate Neuroscience · doi:10.1007/s10158-007-0048-0 · Cited by 7
“Recent work from ex vivo studies in Xenopus and mouse has shown that neurotransmitters and their cognate receptors as well as neurite growth and branching are specified by patterns of spontaneous electrical activity, measured as the frequency of Ca-spikes and global Ca transients, in developing networks (Borodinsky et…”
BackgroundPaudel, S., Ablondi, E. F., Sehdev, M., Marken, J. P., Halleran, A. D., Rahman, A., Kemper, P. F., & Saha, M. S. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20081880 · Cited by 7
“Different groups have defined a spike as: (i) an instance of fluorescence intensity greater than 150% of the baseline (dF/F0) [34]; (ii) a transient amplitude with a rise time of 5 s reaching more than 20% of the baseline value (dF/F0) as determined by the values over the previous 10 min [39]; (iii) a transient amplit…”
Background
Metadata
- Authors
- Ciccolini, F., Collins, T. J., Sudhoelter, J., Lipp, P., Berridge, M. J., & Bootman, M. D.
- Affiliations
- Babraham Institute (GB)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2003-01-01
- Volume
- 23
- Issue
- 1
- Pages
- 103-111
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6742163
- OpenAlex
- W2159977558
- Cited by
- 135
- References
- 36
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 1 · 2023: 3 · 2022: 4 · 2021: 3 · 2020: 5 · 2019: 5 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 6 · 2014: 7 · 2013: 13 · 2012: 11
- FWCI
- 2.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Open Research Online - ORO (The Open University) (acceptedVersion)
- Funders
- Directorate for Biological Sciences
- Merck Sharp and Dohme
- Biotechnology and Biological Sciences Research Council
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Keywords
- calcium signaling, neural precursor differentiation, neurite outgrowth, NMDA receptor, neuronal morphology, calcium transients
- MeSH terms
- Animals, Cell Differentiation, Cells, Cultured, Central Nervous System, gamma-Aminobutyric Acid, Kinetics, Neurons, Phenotype, Potassium Chloride, Stem Cells, Receptors, N-Methyl-D-Aspartate, Neurites, Calcium Signaling, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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