Functional identification of neural stem cell-derived oligodendrocytes by means of calcium transients elicited by thrombin

Rejuvenation Research

Volumn 13, Issue 1, 2010, Pages 27-37

  Grade, Sofia ^a   Agasse, Fabienne ^a   Bernardino, Liliana ^a   Silva, Carla G ^a   Cortes, Luísa ^a   Malva, João O ^a  

^a UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; HISTAMINE; PHOSPHOLIPASE C; PROTEINASE ACTIVATED RECEPTOR 1; PROTEOLIPID PROTEIN; THROMBIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; NERVE CELL CULTURE; NERVE STIMULATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; CALCIUM SIGNALING; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL VENTRICLES; HISTAMINE; MICE; MICE, INBRED C57BL; NEURONS; OLIGODENDROGLIA; POTASSIUM CHLORIDE; RECEPTOR, PAR-1; STEM CELLS; THROMBIN;

EID: 77949493309     PISSN: 15491684     EISSN: None     Source Type: Journal    
DOI: 10.1089/rej.2009.0889     Document Type: Article

References (45)

1. Franklin RJ, Ffrench-Constant C. Remyelination in the CNS: From biology to therapy. Nat Rev Neurosci 2008;9: 839-855.
2. Levison SW, Goldman JE. Both oligodendrocytes and as-trocytes develop from progenitors in the subventricular zone of postnatal rat forebrain. Neuron 1993;10:201-212.
3. Menn B, Garcia-Verdugo JM, Yaschine C, Gonzalez-Perez O, Rowitch D, Alvarez-Buylla A. Origin of oligodendrocytes in the subventricular zone of the adult brain. J Neurosci 2006; 26:7907-7918.
4. Cayre M, Bancila M, Virard I, Borges A, Durbec P. Migrating and myelinating potential of subventricular zone neural progenitor cells in white matter tracts of the adult rodent brain. Mol Cell Neurosci 2006;31:748-758.
5. Smith PM, Blakemore WF. Porcine neural progenitors require commitment to the oligodendrocyte lineage prior to transplantation in order to achieve significant remyelination of demyelinated lesions in the adult CNS. Eur J Neurosci 2000;12:2414-2424.
6. Keirstead HS, Ben-Hur T, Rogister B, O'Leary MT, Dubois-Dalcq M, Blakemore WF. Polysialylated neural cell adhesion molecule-positive CNS precursors generate both oligoden-drocytes and schwann cells to remyelinate the CNS after transplantation. J Neurosci 1999;19:7529-7536.
7. Akiyama Y, Honmou O, Kato T, Uede T, Hashi K, Kocsis JD. Transplantation of clonal neural precursor cells derived from adult human brain establishes functional peripheral myelin in the rat spinal cord. Exp Neurol 2001;167:27-39.
8. Agasse F, Bernardino L, Silva B, Ferreira R, Grade S, Malva JO. Response to histamine allows the functional identification of neuronal progenitors, neurons, astrocytes, and immature cells in subventricular zone cell cultures. Rejuvenation Res 2008;11:187-200.
9. Agasse F, Bernardino L, Kristiansen H, Christiansen SH, Ferreira R, Silva B, Grade S, Woldbye DPD, Malva JO. Neu-ropeptide Y promotes neurogenesis in murine subventricular zone. Stem Cells 2008;26:1636-1645.
10. Bernardino L, Agasse F, Silva B, Ferreira R, Grade S, Malva JO. Tumor necrosis factor-alpha modulates survival, proliferation, and neuronal differentiation in neonatal subventricular zone cell cultures. Stem Cells 2008;26:2361-2371.
11. Wang Y, Richter-Landsberg C, Reiser G. Expression of pro-tease-activated receptors (PARs) in OLN-93 oligodendroglial cells and mechanism of PAR-1-induced calcium signaling. Neuroscience 2004;126:69-82.
12. Silva CG, Porciúncula LO, Canas PM, Oliveira CR, Cunha RA. Blockade of adenosine A(2A) receptors prevents staur-osporine-induced apoptosis of rat hippocampal neurons. Neurobiol Dis 2007;27:182-189.
13. Matos M, Augusto E, Oliveira CR, Agostinho P. Amyloid-beta peptide decreases glutamate uptake in cultured astro-cytes: involvement of oxidative stress and mitogen-activated protein kinase cascades. Neuroscience 2008;156:898-910.
14. Coughlin S.R. How the protease thrombin talks to cells. Proc Natl Acad Sci USA 1999;96:11023-11027.
15. Jacques SL, Kuliopulos A. Protease-activated receptor-4 uses dual prolines and an anionic retention motif for thrombin recognition and cleavage. Biochem J 2003;376:733-740.
16. Nakanishi-Matsui M, Zheng YW, Sulciner DJ, Weiss EJ, Ludeman MJ, Coughlin S.R. PAR3 is a cofactor for PAR4 activation by thrombin. Nature 2000;404:609-613.
17. Ahn HS, Foster C, Boykow G, Stamford A, Manna M, Gra-ziano M. Inhibition of cellular action of thrombin by n3-cyclopropyl-7-[4-(1-methylethyl) phenyl] methyl}-7h-pyrrolo [3, 2-f] quinazoline-1, 3-diamine (SCH 79797), a nonpeptide thrombin receptor antagonist. Biochem Pharmacol 2000;60: 1425-1434.
18. Fernández M, Paradisi M, Del Vecchio G, Giardino L, Calzà L. Thyroid hormone induces glial lineage of primary neu-rospheres derived from non-pathological and pathological rat brain: Implications for remyelination-enhancing therapies. Int J Dev Neurosci 2009;27:769-778.
19. Franco PG, Silvestroff L, Soto EF, Pasquini JM. Thyroid hormones promote differentiation of oligodendrocyte progenitor cells and improve remyelination after cuprizone-induced demyelination. Exp Neurol 2008;212:458-467.
20. Johe KK, Hazel TG, Muller T, Dugich-Djordjevic MM, McKay RD. Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes Dev 1996;10:3129-3140.
21. Baumann N, Pham-Dinh D. Biology of oligodendrocyte and myelin in the mammalian central nervous system. Physiol Rev 2001;81:871-927.
22. Aguirre AA, Chittajallu R, Belachew S, Gallo V. NG2-expressing cells in the subventricular zone are type C-like cells and contribute to interneuron generation in the postnatal hippocampus. J Cell Biol 2004;165:575-589.
23. Coughlin S.R. Thrombin signalling and protease-activated receptors. Nature 2000;407:258-264.
24. Grand RJ, Turnell AS, Grabham PW. Cellular consequences of thrombin-receptor activation. Biochem J 1996;313:353-368.
25. McLaughlin JN, Shen L, Holinstat M, Brooks JD, DiBenedetto E, Hamm HE. Functional selectivity of G protein signaling by agonist peptides and thrombin for the protease-activated receptor-1. J Biol Chem 2005;280:25048-25059.
26. Hains MD, Wing MR, Maddileti S, Siderovski DP, Harden TK. Galpha12=13-and rho-dependent activation of phos-pholipase c-epsilon by lysophosphatidic acid and thrombin receptors. Mol Pharmacol 2006;69:2068-2075.
27. Whittemore SR, Morassutti DJ, Walters WM, Liu RH, Magnuson DS. Mitogen and substrate differentially affect the lineage restriction of adult rat subventricular zone neural precursor cell populations. Exp Cell Res 1999;252:75-95.
28. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, Faravelli L, Morassutti DJ, Roisen F, Nickel DD, Vescovi AL. Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 1996;16:1091-1100.
29. Barres BA, Lazar MA, Raff MC. A novel role for thyroid hormone, glucocorticoids and retinoic acid in timing oligodendrocyte development. Development 1994;120:1097-1108.
30. Zhang P, Chebath J, Lonai P, Revel M. Enhancement of ol-igodendrocyte differentiation from murine embryonic stem cells by an activator of gp130 signaling. Stem Cells 2004;22: 344-354.
31. Kang SM, Cho MS, Seo H, Yoon CJ, Oh SK, Choi YM, Kim DW. Efficient induction of oligodendrocytes from human embryonic stem cells. Stem Cells 2007;25:419-424.
32. Murray K, Dubois-Dalcq M. Emergence of oligodendrocytes from human neural spheres. J Neurosci Res 1997;50:146-156.
33. Ravin R, Hoeppner DJ, Munno DM, Carmel L, Sullivan J, Levitt DL, Miller JL, Athaide C, Panchision DM, McKay RD. Potency and fate specification in CNS stem cell populations in vitro. Cell Stem Cell 2008;3:670-680.
34. Jin K, Mao XO, Sun Y, Xie L, Greenberg DA. Stem cell factor stimulates neurogenesis in vitro and in vivo. J Clin Invest 2002;110:311-319.
35. Laywell ED, Rakic P, Kukekov VG, Holland EC, Steindler DA. Identification of a multipotent astrocytic stem cell in the immature and adult mouse brain. Proc Natl Acad Sci USA 2000;97:13883-13888.
36. Rodríguez-Peña A. Oligodendrocyte development and thyroid hormone. J Neurobiol 1999;40:497-512.
37. Bernal J. Thyroid hormones and brain development. Vitam Horm 2005;71:95-122.
38. Baas D, Legrand C, Samarut J, Flamant F. Persistence of oligodendrocyte precursor cells and altered myelination in optic nerve associated to retina degeneration in mice devoid of all thyroid hormone receptors. Proc Natl Acad Sci USA 2002;99:2907-2911.
39. Shavit E, Beilin O, Korczyn AD, Sylantiev C, Aronovich R, Drory VE, Gurwitz D, Horresh I, Bar-Shavit R, Peles E, Chapman J. Thrombin receptor PAR-1 on myelin at the node of Ranvier: a new anatomy and physiology of conduction block. Brain 2008;131:1113-1122.
40. 2\+ mobilization, and apoptosis. J. Neurobiol 2001;48:87-100.
41. Olianas MC, Dedoni S, Onali P. Proteinase-activated receptors 1 and 2 in rat olfactory system: Layer-specific regulation of multiple signaling pathways in the main olfactory bulb and induction of neurite retraction in olfactory sensory neurons. Neuroscience 2007;146:1289-1301.
42. Gorbacheva LR, Storozhevykh TP, Pinelis VG, Ishiwata S, Strukova SM. Modulation of hippocampal neuron survival by thrombin and factor Xa. Biochemistry (Moscow) 2006; 71:1082-1089.
43. Yang Y, Akiyama H, Fenton JW 2nd, Brewer GJ. Thrombin receptor on rat primary hippocampal neurons: Coupled calcium and cAMP responses. Brain Res 1997;761:11-18.
44. Wang H, Ubl JJ, Reiser G. Four subtypes of protease-activated receptors, co-expressed in rat astrocytes, evoke different physiological signaling. Glia 2002;37:53-63.
45. Sorensen SD, Nicole O, Peavy RD, Montoya LM, Lee CJ, Murphy TJ, Traynelis SF, Hepler JR. Common signaling pathways link activation of murine PAR-1, LPA, and S1P receptors to proliferation of astrocytes. Mol Pharmacol 2003;64:1199-1209.