Plasticity of calcium signaling cascades in human embryonic stem cell-derived neural precursors

Stem Cells and Development

Volumn 22, Issue 10, 2013, Pages 1506-1521

  Forostyak, Oksana ^a   Romanyuk, Nataliya ^a   Verkhratsky, Alexei ^b   Sykova, Eva ^a,c   Dayanithi, Govindan ^a,d  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Czech Republic)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c CHARLES UNIVERSITY   (Czech Republic)

^d INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BETA TUBULIN; CAFFEINE; CALCIUM; GLUTAMATE RECEPTOR; GLUTAMIC ACID; IONOTROPIC RECEPTOR; METABOTROPIC RECEPTOR; NEURON SPECIFIC NUCLEAR PROTEIN; NICARDIPINE; PROTEOCHONDROITIN SULFATE; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y RECEPTOR; RYANODINE RECEPTOR; SURAMIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL DEATH; CELL DIFFERENTIATION; CONTROLLED STUDY; DEPOLARIZATION; EMBRYONIC STEM CELL; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHYSIOLOGICAL PROCESS; PLASTICITY; PRIORITY JOURNAL;

BIOLOGICAL MARKERS; CALCIUM; CALCIUM CHANNELS; CALCIUM SIGNALING; CELL COUNT; CELL DIFFERENTIATION; EMBRYONIC STEM CELLS; GLUTAMATES; HUMANS; INTRACELLULAR SPACE; MICROSCOPY, CONFOCAL; NEURAL STEM CELLS; RECEPTORS, PURINERGIC; TIME FACTORS;

EID: 84877327486     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2012.0624     Document Type: Article

References (79)

1. Thomson JA, J Itskovitz-Eldor, SS Shapiro, MA Waknitz, JJ Swiergiel, VS Marshall, JM Jones. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282:1145-1147
2. Zhang SC, M Wernig, ID Duncan, O Brustle, JA Thomson. (2001). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19:1129-1133
3. Reubinoff BE, P Itsykson, T Turetsky, MF Pera, E Reinhartz, A Itzik, T Ben-Hur. (2001). Neural progenitors from human embryonic stem cells. Nat Biotechnol 19:1134-1140
4. Schulz TC, SA Noggle, GM Palmarini, DA Weiler, IG Lyons, KA Pensa, AC Meedeniya, BP Davidson, NA Lambert, BG Condie. (2004). Differentiation of human embryonic stem cells to dopaminergic neurons in serum-free suspension culture. Stem Cells 22:1218-1238
5. Li XJ, ZW Du, ED Zarnowska, M Pankratz, LO Hansen, RA Pearce, SC Zhang. (2005). Specification of motoneurons from human embryonic stem cells. Nat Biotechnol 23:215-221
6. De Smedt H, A Verkhratsky, S Muallem. (2011). Ca(2 + ) signaling mechanisms of cell survival, cell death: an introduction. Cell Calcium 50:207-210
7. Dayanithi G, O Forostyak, Y Ueta, A Verkhratsky, EC Toescu. (2012). Segregation of calcium signalling mechanisms in magnocellular neurones, terminals. Cell Calcium 51:293-299
8. Toescu EC, G Dayanithi. (2012). Neuroendocrine signalling: natural variations on a Ca(2 + ) theme. Cell Calcium 51:207-211
9. Berridge MJ, P Lipp, MD Bootman. (2000). The versatility, universality of calcium signalling. Nat Rev Mol Cell Biol 1:11-21
10. Carafoli E, L Santella, D Branca, M Brini. (2001). Generation, control,, processing of cellular calcium signals. Crit Rev Biochem Mol Biol 36:107-260
11. Munaron L, S Antoniotti, D Lovisolo. (2004). Intracellular calcium signals, control of cell proliferation: how many mechanisms? J Cell Mol Med 8:161-168
12. Orrenius S, B Zhivotovsky, P Nicotera. (2003). Regulation of cell death: the calcium-apoptosis link. Nat Rev Mol Cell Biol 4:552-565
13. Majumder P, CA Trujillo, CG Lopes, RR Resende, KN Gomes, KK Yuahasi, LR Britto, H Ulrich. (2007). New insights into purinergic receptor signaling in neuronal differentiation, neuroprotection,, brain disorders. Purinergic Signal 3:317-331
14. North RA, A Verkhratsky. (2006). Purinergic transmission in the central nervous system. Pflugers Arch 452:479-485
15. Berridge MJ. (1998). Neuronal calcium signaling. Neuron 21:13-26
16. Spitzer NC. (2006). Electrical activity in early neuronal development. Nature 444:707-712
17. LoTurco JJ, DF Owens, MJ Heath, MB Davis, AR Kriegstein. (1995). GABA, glutamate depolarize cortical progenitor cells, inhibit DNA synthesis. Neuron 15:1287-1298
18. Haydar TF, F Wang, ML Schwartz, P Rakic. (2000). Differential modulation of proliferation in the neocortical ventricular, subventricular zones. J Neurosci 20:5764-5774
19. Kozubenko N, K Turnovcova, M Kapcalova, O Butenko, M Anderova, V Rusnakova, M Kubista, A Hampl, P Jendelova, E Sykova. (2010). Analysis of in vitro, in vivo characteristics of human embryonic stem cell-derived neural precursors. Cell Transplant 19:471-486
20. Rowe EW, DM Jeftinija, K Jeftinija, S Jeftinija. (2005). Development of functional neurons from postnatal stem cells in vitro. Stem Cells 23:1044-1049
21. Arnhold S, C Andressen, DN Angelov, R Vajna, SG Volsen, J Hescheler, K Addicks. (2000). Embryonic stem-cell derived neurones express a maturation dependent pattern of voltage-gated calcium channels, calcium-binding proteins. Int J Dev Neurosci 18:201-212
22. Malmersjo S, I Liste, O Dyachok, A Tengholm, E Arenas, P Uhlen. (2010). Ca2 +, cAMP signaling in human embryonic stem cell-derived dopamine neurons. Stem Cells Dev 19:1355-1364
23. Young A, DW Machacek, SK Dhara, PR Macleish, M Benveniste, MC Dodla, CD Sturkie, SL Stice. (2011). Ion channels, ionotropic receptors in human embryonic stem cell derived neural progenitors. Neuroscience 192:793-805
24. Zhang L, BE Blackman, MD Schonemann, T Zogovic-Kapsalis, X Pan, M Tagliaferri, HA Harris, I Cohen, RA Pera, et al. (2010). Estrogen receptor beta-selective agonists stimulate calcium oscillations in human, mouse embryonic stem cell-derived neurons. PLoS One 5:e11791
25. Weick JP, M Austin Johnson, SC Zhang. (2009). Developmental regulation of human embryonic stem cell-derived neurons by calcium entry via transient receptor potential channels. Stem Cells 27:2906-2916
26. Komori Y, M Tanaka, M Kuba, M Ishii, M Abe, N Kitamura, A Verkhratsky, I Shibuya, G Dayanithi. (2010). Ca(2 + ) homeostasis, Ca(2 + ) signalling, somatodendritic vasopressin release in adult rat supraoptic nucleus neurones. Cell Calcium 48:324-332
27. Dayanithi G, H Widmer, P Richard. (1996). Vasopressininduced intracellular Ca2 + increase in isolated rat supraoptic cells. J Physiol 490 (Pt 3):713-727
28. Viero C, I Mechaly, H Aptel, S Puech, J Valmier, F Bancel, G Dayanithi. (2006). Rapid inhibition of Ca2 + influx by neurosteroids in murine embryonic sensory neurones. Cell Calcium 40:383-391
29. Dayanithi G, M Chen-Kuo-Chang, C Viero, C Hamel, A Muller, G Lenaers. (2010). Characterization of Ca2 + signalling in postnatal mouse retinal ganglion cells: involvement of OPA1 in Ca2 + clearance. Ophthalmic Genet 31:53-65
30. Dayanithi G, N Sabatier, H Widmer. (2000). Intracellular calcium signalling in magnocellular neurones of the rat supraoptic nucleus: understanding the autoregulatory mechanisms. Exp Physiol 85 Spec No:75S-84S
31. Viero C, G Dayanithi. (2008). Neurosteroids are excitatory in supraoptic neurons but inhibitory in the peripheral nervous system: it is all about oxytocin, progesterone receptors. Prog Brain Res 170:177-192
32. Lambert RC, G Dayanithi, FC Moos, P Richard. (1994). A rise in the intracellular Ca2 + concentration of isolated rat supraoptic cells in response to oxytocin. J Physiol 478 (Pt 2):275-287
33. Jamen F, G Alonso, I Shibuya, H Widmer, CM Vacher, A Calas, J Bockaert, P Brabet, G Dayanithi. (2003). Impaired somatodendritic responses to pituitary adenylate cyclase-activating polypeptide (PACAP) of supraoptic neurones in PACAP type I-receptor deficient mice. J Neuroendocrinol 15:871-881
34. Widmer H, M Ludwig, F Bancel, G Leng, G Dayanithi. (2003). Neurosteroid regulation of oxytocin, vasopressin release from the rat supraoptic nucleus. J Physiol 548:233-244
35. Dayanithi G, I Mechaly, C Viero, H Aptel, S Alphandery, S Puech, F Bancel, J Valmier. (2006). Intracellular Ca2 + regulation in rat motoneurons during development. Cell Calcium 39:237-246
36. Sabatier N, P Richard, G Dayanithi. (1997). L-, N-, Tbut neither P-nor Q-type Ca2 + channels control vasopressininduced Ca2 + influx in magnocellular vasopressin neurones isolated from the rat supraoptic nucleus. J Physiol 503 (Pt 2):253-268
37. Tsien RW, D Lipscombe, DV Madison, KR Bley, AP Fox. (1988). Multiple types of neuronal calcium channels, their selective modulation. Trends Neurosci 11:431-438
38. Deisseroth K, S Singla, H Toda, M Monje, TD Palmer, RC Malenka. (2004). Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron 42:535-552
39. Webb SE, M Moreau, C Leclerc, AL Miller. (2005). Calcium transients, neural induction in vertebrates. Cell Calcium 37:375-385
40. Yu HM, J Wen, R Wang, WH Shen, S Duan, HT Yang. (2008). Critical role of type 2 ryanodine receptor in mediating activity-dependent neurogenesis from embryonic stem cells. Cell Calcium 43:417-431
41. Pouille F, P Cavelier, T Desplantez, H Beekenkamp, PJ Craig, RE Beattie, SG Volsen, JL Bossu. (2000). Dendrosomatic distribution of calcium-mediated electrogenesis in purkinje cells from rat cerebellar slice cultures. J Physiol 527 (Pt 2):265-282
42. Khosravani H, GW Zamponi. (2006). Voltage-gated calcium channels, idiopathic generalized epilepsies. Physiol Rev 86:941-966
43. Lemos JR, SI Ortiz-Miranda, AE Cuadra, C Velazquez-Marrero, EE Custer, T Dad, G Dayanithi. (2012). Modulation/physiology of calcium channel sub-types in neurosecretory terminals. Cell Calcium 51:284-292
44. Abbracchio MP, G Burnstock, A Verkhratsky, H Zimmermann. (2009). Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19-29
45. Burnstock G, A Verkhratsky. (2010). Long-term (trophic) purinergic signalling: purinoceptors control cell proliferation, differentiation, death. Cell Death Dis 1:e9
46. Zimmermann H. (2011). Purinergic signaling in neural development. Semin Cell Dev Biol 22:194-204
47. Ralevic V, G Burnstock. (1998). Receptors for purines, pyrimidines. Pharmacol Rev 50:413-492
48. Allodi I, MS Guzman-Lenis, J Hernandez, X Navarro, E Udina. (2011). In vitro comparison of motor, sensory neuron outgrowth in a 3D collagen matrix. J Neurosci Methods 198:53-61
49. Khaira SK, CW Pouton, JM Haynes. (2009). P2X2, P2X4, P2Y1 receptors elevate intracellular Ca2 + in mouse embryonic stem cell-derived GABAergic neurons. Br J Pharmacol 158:1922-1931
50. Rose CR, A Konnerth. (2001). Stores not just for storage. intracellular calcium release, synaptic plasticity. Neuron 31:519-522
51. Meldolesi J. (2001). Rapidly exchanging Ca2 + stores in neurons: molecular, structural, functional properties. Prog Neurobiol 65:309-338
52. Rizzuto R. (2001). Intracellular Ca(2 + ) pools in neuronal signalling. Curr Opin Neurobiol 11:306-311
53. Kettenmann H, UK Hanisch, M Noda, A Verkhratsky. (2011). Physiology of microglia. Physiol Rev 91:461-553
54. Berridge MJ. (2002). The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium 32:235-249
55. Bootman MD, MJ Berridge, HL Roderick. (2002). Calcium signalling: more messengers, more channels, more complexity. Curr Biol 12:R563-R565
56. Verkhratsky A. (2005). Physiology, pathophysiology of the calcium store in the endoplasmic reticulum of neurons. Physiol Rev 85:201-279
57. Vyleta NP, SM Smith. (2008). Fast inhibition of glutamate-activated currents by caffeine. PLoS One 3:e3155
58. Sedan O, K Dolnikov, N Zeevi-Levin, N Leibovich, M Amit, J Itskovitz-Eldor, O Binah. (2008). 1,4,5-Inositol trisphosphate-operated intracellular Ca(2 + ) stores, angiotensin-II/endothelin-1 signaling pathway are functional in human embryonic stem cell-derived cardiomyocytes. Stem Cells 26:3130-3138
59. Satin J, I Itzhaki, S Rapoport, EA Schroder, L Izu, G Arbel, R Beyar, CW Balke, J Schiller, L Gepstein. (2008). Calcium handling in human embryonic stem cell-derived cardiomyocytes. Stem Cells 26:1961-1972
60. Spitzer NC, NJ Lautermilch, RD Smith, TM Gomez. (2000). Coding of neuronal differentiation by calcium transients. Bioessays 22:811-817
61. Spitzer NC. (1994). Spontaneous Ca2 + spikes, waves in embryonic neurons: signaling systems for differentiation. Trends Neurosci 17:115-118
62. Desarmenien MG, NC Spitzer. (1991). Role of calcium, protein kinase C in development of the delayed rectifier potassium current in Xenopus spinal neurons. Neuron 7:797-805
63. Spitzer NC, RC Debaca, KA Allen, J Holliday. (1993). Calcium dependence of differentiation of GABA immunoreactivity in spinal neurons. J Comp Neurol 337:168-175
64. Gu X, EC Olson, NC Spitzer. (1994). Spontaneous neuronal calcium spikes, waves during early differentiation. J Neurosci 14:6325-6335
65. Ben-Ari Y, JLGaiarsa, R Tyzio, R Khazipov. (2007). GABA: a pioneer transmitter that excites immature neurons, generates primitive oscillations. Physiol Rev 87:1215-1284
66. Wang J, DB Reichling, A Kyrozis, AB MacDermott. (1994). Developmental loss of GABA-, glycine-induced depolarization, Ca2 + transients in embryonic rat dorsal horn neurons in culture. Eur J Neurosci 6:1275-1280
67. Obrietan K, AN van den Pol. (1995). GABA neurotransmission in the hypothalamus: developmental reversal from Ca2 + elevating to depressing. J Neurosci 15:5065-5077
68. Maric D, I Maric, X Wen, JM Fritschy, W Sieghart, JL Barker, R Serafini. (1999). GABAA receptor subunit composition, functional properties of Cl-channels with differential sensitivity to zolpidem in embryonic rat hippocampal cells. J Neurosci 19:4921-4937
69. Schlett K. (2006). Glutamate as a modulator of embryonic, adult neurogenesis. Curr Top Med Chem 6:949-960
70. Melchiorri D, I Cappuccio, C Ciceroni, P Spinsanti, P Mosillo, I Sarichelou, P Sale, F Nicoletti. (2007). Metabotropic glutamate receptors in stem/progenitor cells. Neuropharmacology 53:473-480
71. Piper DR, T Mujtaba, MS Rao, MT Lucero. (2000). Immunocytochemical, physiological characterization of a population of cultured human neural precursors. J Neurophysiol 84:534-548
72. Draberova E, L Del Valle, J Gordon, V Markova, B Smejkalova, L Bertrand, JP de Chadarevian, DP Agamanolis, A Legido, et al. (2008). Class III beta-tubulin is constitutively coexpressed with glial fibrillary acidic protein, nestin in midgestational human fetal astrocytes: implications for phenotypic identity. J Neuropathol Exp Neurol 67: 341-354
73. Hol EM, RF Roelofs, E Moraal, MA Sonnemans, JA Sluijs, EA Proper, PN de Graan, DF Fischer, FW van Leeuwen. (2003). Neuronal expression of GFAP in patients with Alzheimer pathology, identification of novel GFAP splice forms. Mol Psychiatry 8:786-796
74. Casper KB, KD McCarthy. (2006). GFAP-positive progenitor cells produce neurons, oligodendrocytes throughout the CNS. Mol Cell Neurosci 31:676-684
75. Wernig M, JP Zhao, J Pruszak, E Hedlund, D Fu, F Soldner, V Broccoli, M Constantine-Paton, O Isacson, R Jaenisch. (2008). Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain, improve symptoms of rats with Parkinson's disease. Proc Natl Acad Sci U S A 105:5856-5861
76. Dimos JT, KT Rodolfa, KK Niakan, LM Weisenthal, H Mitsumoto, W Chung, GF Croft, G Saphier, R Leibel, et al. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321:1218-1221
77. Yuan SH, J Martin, J Elia, J Flippin, RI Paramban, MP Hefferan, JG Vidal, Y Mu, RL Killian, et al. (2011). Cell-surface marker signatures for the isolation of neural stem cells, glia, neurons derived from human pluripotent stem cells. PLoS One 6:e17540
78. Forostyak O, N Kozubenko, S Bernascone, E Sykova, G Dayanithi. (2010). Physiology of calcium signalling in human embryonic stem cell-derived neural precursors. 7th Federation of European Neuroscience Scocieties. Forum of European Neuroscience, FENS Abstract, 5: 041.8
79. Forostyak O, N Romanyuk, E Sykova, G Dayanithi. (2011). Physiology of Ca2 + signalling in human embryonic stem cell-derived neural precursors. GLIA 59 Suppl:1 Pages:S119-S119