Increase of intracellular Ca2+ by adenine and uracil nucleotides in human midbrain-derived neuronal progenitor cells

Cell Calcium

Volumn 45, Issue 5, 2009, Pages 485-498

  Rubini, Patrizia ^a   Milosevic, Javorina ^b   Engelhardt, Johannes ^a   Al Khrasani, Mahmoud ^a   Franke, Heike ^a   Heinrich, Attilla ^c   Sperlagh, Beata ^c   Schwarz, Sigrid C ^a   Schwarz, Johannes ^a   Nörenberg, Wolfgang ^a   Illes, Peter ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b Translational Center for Regenerative Medicine   (Germany)

^c INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Adenine nucleotides; Human neuronal progenitor cells; Midbrain dopaminergic neurons; P2X receptors; P2Y receptors; Uracil nucleotides

Indexed keywords

2' DEOXY 6 N METHYLADENOSINE 3',5' BISPHOSPHATE; ADENINE NUCLEOTIDE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APYRASE; CALCIUM ION; CYCLOPIAZONIC ACID; FURA 2; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PYRIDOXAL PHOSPHATE 6 AZOPHENYL 2',4' DISULFONIC ACID; SURAMIN; URACIL; URACIL DERIVATIVE; URIDINE DIPHOSPHATE; URIDINE TRIPHOSPHATE; CALCIUM; INTERMEDIATE FILAMENT PROTEIN; NERVE PROTEIN; NESTIN; PURINERGIC P2 RECEPTOR; PYRIMIDINE NUCLEOTIDE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM CURRENT; CALCIUM DEPLETION; CALCIUM TRANSPORT; CONCENTRATION RESPONSE; CONTROLLED STUDY; FETUS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; MESENCEPHALON; NEURAL STEM CELL; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN SECRETION; RECEPTOR UPREGULATION; ANIMAL; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG POTENTIATION; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; STEM CELL;

ADENINE NUCLEOTIDES; ANIMALS; CALCIUM; CELL PROLIFERATION; CELLS, CULTURED; HUMANS; INTERMEDIATE FILAMENT PROTEINS; MESENCEPHALON; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, PURINERGIC P2; STEM CELLS; URACIL NUCLEOTIDES;

EID: 66949124306     PISSN: 01434160     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceca.2009.03.008     Document Type: Article

References (59)

1. Studer L., Tabar V., and McKay R.D. Transplantation of expanded mesencephalic precursors leads to recovery in parkinsonian rats. Nat. Neurosci. 1 (1998) 290-295
2. Kim J.H., Auerbach J.M., Rodríguez-Gómez J.A., Velasco I., Gavin D., Lumelsky N., Lee S.H., Nguyen J., Sánchez-Pernaute R., Bankiewicz K., and McKay R. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418 (2002) 50-56
3. Storch A., Sabolek M., Milosevic J., Schwarz S.C., and Schwarz J. Midbrain-derived neural stem cells: from basic science to therapeutic approaches. Cell Tissue Res. 318 (2004) 15-22
4. Milosevic J., Brandt A., Roemuss U., Arnold A., Wegner F., Schwarz S.C., Storch A., Zimmermann H., and Schwarz J. Uracil nucleotides stimulate human neural precursor cell proliferation and dopaminergic differentiation: involvement of MEK/ERK signalling. J. Neurochem. 99 (2006) 913-923
5. Schwarz J., Schwarz S.C., and Storch A. Developmental perspectives on human midbrain-derived neural stem cells. Neurodegener. Dis. 3 (2006) 45-49
6. Morest D.K., and Silver J. Precursors of neurons, neuroglia, and ependymal cells in the CNS: what are they? Where are they from? How do they get where they are going?. Glia 43 (2003) 6-18
7. Gritti A., Rosati B., Lecchi M., Vescovi A.L., and Wanke E. Excitable properties in astrocytes derived from human embryonic CNS stem cells. Eur. J. Neurosci. 12 (2000) 3549-3559
8. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev. 87 (2007) 659-797
9. Nguyen L., Rigo J.M., Rocher V., Belachew S., Malgrange B., Rogister B., Leprince P., and Moonen G. Neurotransmitters as early signals for central nervous system development. Cell Tissue Res. 305 (2001) 187-202
10. Martins R.A., and Pearson R.A. Control of cell proliferation by neurotransmitters in the developing vertebrate retina. Brain Res. 1192 (2008) 37-60
11. Abbracchio M.P., and Burnstock G. Purinoceptors: are there families of P2X and P2Y purinoceptors?. Pharmacol. Ther. 64 (1994) 445-475
12. Kawano S., Otsu K., Kuruma A., Shoji S., Yanagida E., Muto Y., Yoshikawa F., Hirayama Y., Mikoshiba K., and Furuichi T. ATP autocrine/paracrine signaling induces calcium oscillations and NFAT activation in human mesenchymal stem cells. Cell Calcium 39 (2006) 313-324
13. Heo J.S., and Han H.J. ATP stimulates mouse embryonic stem cell proliferation via protein kinase C, phosphatidylinositol 3-kinase/Akt, and mitogen-activated protein kinase signaling pathways. Stem Cells 24 (2006) 2637-2648
14. Wegner F., Kraft R., Busse K., Härtig W., Schaarschmidt G., Schwarz S.C., Schwarz J., and Hevers W. Functional and molecular analysis of GABA receptors in human midbrain-derived neural progenitor cells. J. Neurochem. 107 (2008) 1056-1069
15. Storch A., Paul G., Csete M., Boehm B.O., Carvey P.M., Kupsch A., and Schwarz J. Long-term proliferation and dopaminergic differentiation of human mesencephalic neural precursor cells. Exp. Neurol. 170 (2001) 317-325
16. Milosevic J., Schwarz S.C., Krohn K., Poppe M., Storch A., and Schwarz J. Low atmospheric oxygen avoids maturation, senescence and cell death of murine mesencephalic neural precursors. J. Neurochem. 92 (2005) 718-729
17. 1 receptors may depend on the developmental stage of cultured rat striatal neurons. J. Cell. Physiol. 209 (2006) 81-93
18. Llaudet E., Botting N.P., Crayston J.A., and Dale N. A three-enzyme microelectrode sensor for detecting purine release from central nervous system. Biosens. Bioelectron. 18 (2003) 43-52
19. Franke H., Krügel U., Grosche J., Heine C., Härtig W., Allgaier C., and Illes P. P2Y receptor expression on astrocytes in the nucleus accumbens of rats. Neuroscience 127 (2004) 431-441
20. Richards C.D., Shiroyama T., and Kitai S.T. Electrophysiological and immunocytochemical characterization of GABA and dopamine neurons in the substantia nigra of the rat. Neuroscience 80 (1997) 545-557
21. Liu R.H., Morassutti D.J., Whittemore S.R., Sosnowski J.S., and Magnuson D.S.K. Electrophysiological properties of mitogen-expanded adult rat spinal cord and subventricular zone neural precursor cells. Exp. Neurol. 158 (1999) 143-154
22. Carleton A., Petreanu L.T., Lansford R., Alvarez-Buylla A., and Lledo P.M. Becoming a new neuron in the adult olfactory bulb. Nat. Neurosci. 6 (2003) 507-518
23. Feldman D.H., Thinschmidt J.S., Peel A.L., Papke R.L., and Reier P.J. Differentiation of ionic currents in CNS progenitor cells: dependence upon substrate attachment and epidermal growth factor. Exp. Neurol. 140 (1996) 206-217
24. Piper D.R., Mujtaba T., Rao M.S., and Lucero M.T. Immunocytochemical and physiological characterization of a population of cultured human neural precursors. J. Neurophysiol. 84 (2000) 534-548
25. Wang D.D., Krueger D.D., and Bordey A. Biophysical properties and ionic signature of neuronal progenitors of the postnatal subventricular zone in situ. J. Neurophysiol. 90 (2003) 2291-2302
26. Gever J.R., Cockayne D.A., Dillon M.P., Burnstock G., and Ford A.P.D.W. Pharmacology of P2X channels. Pflügers Arch. 452 (2006) 513-537
27. Gerevich Z., Borvendeg S.J., Schröder W., Franke H., Wirkner K., Nörenberg W., Fürst S., Gillen C., and Illes P. Inhibition of N-type voltage-activated calcium channels in rat dorsal root ganglion neurons by P2Y receptors is a possible mechanism of ADP-induced analgesia. J. Neurosci. 24 (2004) 797-807
28. Verkhratsky A., and Steinhäuser C. Ion channels in glial cells. Brain Res. Brain Res. Rev. 32 (2000) 380-412
29. Ralevic V., and Burnstock G. Receptors for purines and pyrimidines. Pharmacol. Rev. 50 (1998) 413-492
30. Illes P., and Ribeiro A.J. Molecular physiology of P2 receptors in the central nervous system. Eur. J. Pharmacol. 483 (2004) 5-17
31. von Kügelgen I. Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol. Ther. 110 (2006) 415-432
32. Lin J.H., Takano T., Arcuino G., Wang X., Hu F., Darzynkiewicz Z., Nunes M., Goldman S.A., and Nedergaard M. Purinergic signaling regulates neural progenitor cell expansion and neurogenesis. Dev. Biol. 302 (2007) 356-366
33. Abdipranoto A., Liu G.J., Werry E.L., and Bennett M.R. Mechanisms of secretion of ATP from cortical astrocytes triggered by uridine triphosphate. Neuroreport 14 (2003) 2177-2181
34. Liu G.J., Werry E.L., and Bennett M.R. Secretion of ATP from Schwann cells in response to uridine triphosphate. Eur. J. Neurosci. 21 (2005) 151-160
35. Luhmann H.J., Reiprich R.A., Hanganu I., and Kilb W. Cellular physiology of the neonatal rat cerebral cortex: intrinsic membrane properties, sodium and calcium currents. J. Neurosci. Res. 62 (2000) 574-584
36. Arias-Carrión O., Hernández-López S., Ibañez-Sandoval O., Bargas J., Hernández-Cruz A., and Drucker-Colín R. Neuronal precursors within the adult rat subventricular zone differentiate into dopaminergic neurons after substantia nigra lesion and chromaffin cell transplant. J. Neurosci. Res. 84 (2006) 1425-1437
37. Piper D.R., Mujtaba T., Keyoung H., Roy N.S., Goldman S.A., Rao M.S., and Lucero M.T. Identification and characterization of neuronal precursors and their progeny from human fetal tissue. J. Neurosci. Res. 66 (2001) 356-368
38. Belluzzi O., Benedusi M., Ackman J., and LoTurco J.J. Electrophysiological differentiation of new neurons in the olfactory bulb. J. Neurosci. 23 (2003) 10411-10418
39. Hogg R.C., Chipperfield H., Whyte K.A., Stafford M.R., Hansen M.A., Cool S.M., Nurcombe V., and Adams D.J. Functional maturation of isolated neural progenitor cells from the adult rat hippocampus. Eur. J. Neurosci. 19 (2004) 2410-2420
40. Shukla V., Zimmermann H., Wang L., Kettenmann H., Raab S., Hammer K., Sévigny J., Robson S.C., and Braun N. Functional expression of the ecto-ATPase NTPDase2 and of nucleotide receptors by neuronal progenitor cells in the adult murine hippocampus. J. Neurosci. Res. 80 (2005) 600-610
41. Schlesinger F., Meywirth J., Krampfl K., Grosskreutz J., Petri S., Mauth C., Just L., Bader A., and Bufler J. Ligand-gated channels in early mesencephalic neuronal precursors: immunocytochemical and electrophysiological analysis. Eur. J. Neurosci. 19 (2004) 2371-2376
42. Parekh A.B., and Putney J.W. Store-operated calcium channels. Physiol. Rev. 85 (2005) 757-810
43. 2+ entry, and spontaneous transmitter release. Neuron 29 (2001) 197-208
44. Moran M.M., Xu H., and Clapham D.E. TRP ion channels in the nervous system. Curr. Opin. Neurobiol. 14 (2004) 362-369
45. Schaefer M., Plant T.D., Obukhov A.G., Hofmann T., Gudermann T., and Schultz G. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J. Biol. Chem. 275 (2000) 17517-17526
46. 2+ entry. Naunyn-Schmiedebergs Arch. Pharmacol. 359 (1999) 92-101
47. 1 receptor. Neuropharmacology 43 (2002) 966-978
48. Weissman T.A., Riquelme P.A., Ivic L., Flint A.C., and Kriegstein A.R. Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43 (2004) 647-661
49. Mishra S.K., Braun N., Shukla V., Füllgrabe M., Schomerus C., Korf H.W., Gachet C., Ikehara Y., Sévigny J., Robson S.C., and Zimmermann H. Extracellular nucleotide signaling in adult neural stem cells: synergism with growth factor-mediated cellular proliferation. Development 133 (2006) 675-684
50. Abbracchio M.P., Burnstock G., Boeynaems J.M., Barnard E.A., Boyer J.L., Kennedy C., Knight G.E., Fumagalli M., Gachet C., Jacobson K.A., and Weisman G.A. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev. 58 (2006) 281-341
51. North R.A., and Verkhratsky A. Purinergic transmission in the central nervous system. Pflügers Arch. 452 (2006) 479-485
52. Ciccolini F., Collins T.J., Sudhoelter J., Lipp P., Berridge M.J., and Bootman M.D. Local and global spontaneous calcium events regulate neurite outgrowth and onset of GABAergic phenotype during neural precursor differentiation. J. Neurosci. 23 (2003) 103-111
53. Uckermann O., Grosche J., Reichenbach A., and Bringmann A. ATP-evoked calcium responses of radial glial (Müller) cells in the postnatal rabbit retina. J. Neurosci. Res. 70 (2002) 209-218
54. Zimmermann H. Nucleotide signaling in nervous system development. Pflügers Arch. 452 (2006) 573-588
55. 1 receptors in connexin43-null mice alters calcium signaling and migration of neural progenitor cells. J. Neurosci. 23 (2003) 11444-11452
56. Pearson R.A., Dale N., Llaudet E., and Mobbs P. ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46 (2005) 731-744
57. Braun N., Sévigny J., Mishra S.K., Robson S.C., Barth S.W., Gerstberger R., Hammer K., and Zimmermann H. Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur. J. Neurosci. 17 (2003) 1355-1364
58. Franke H., and Illes P. Involvement of P2 receptors in the growth and survival of neurons in the CNS. Pharmacol. Ther. 109 (2006) 297-324
59. 2 receptor activates nerve growth factor/TrkA signaling to enhance neuronal differentiation. Proc. Natl. Acad. Sci. U.S.A. (2005) 19138-19143