Calcitonin gene-related peptide (CGRP) triggers Ca2+ responses in cultured astrocytes and in Bergmann glial cells from cerebellar slices

European Journal of Neuroscience

Volumn 28, Issue 11, 2008, Pages 2213-2220

  Morara, Stefano ^a   Wang, Li Ping ^b   Filippov, Vitaly ^b   Dickerson, Ian M ^c   Grohovaz, Fabio ^d,e,f   Provini, Luciano ^a,g   Kettenmann, Helmut ^b  

^a CNR   (Italy)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF ROCHESTER   (United States)

^d SAN RAFFAELE HOSPITAL   (Italy)

^e ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^f National Institute of Neuroscience   (Italy)

^g UNIVERSITY OF MILAN   (Italy)

Author keywords

Differentiation; Mouse; Neuron glia transmission; Receptor; Receptor component protein

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; FURA 2; NEUROPEPTIDE; THAPSIGARGIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ASTROCYTE; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CELL CULTURE; CELL DIFFERENTIATION; CEREBELLUM; CONFOCAL MICROSCOPY; GLIA CELL; IMMUNOFLUORESCENCE; MOUSE; NEUROMODULATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL;

ANIMALS; ASTROCYTES; CALCITONIN GENE-RELATED PEPTIDE; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; FURA-2; INDICATORS AND REAGENTS; MEMBRANE POTENTIALS; MICE; NEUROGLIA; ORGAN CULTURE TECHNIQUES; PATCH-CLAMP TECHNIQUES; RECEPTORS, CALCITONIN GENE-RELATED PEPTIDE; THAPSIGARGIN;

EID: 56749177206     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2008.06514.x     Document Type: Article

References (44)

1. Adams, J.C., Mroz, E.A. Sewell, W.F. (1987) A possible neurotransmitter role for CGRP in a hair-cell sensory organ. Brain Res., 419, 347 351.
2. 2+ signaling pathways. Mol. Cell. Biochem., 197, 179 185.
3. Altman, J. 1982) Morphological development of the rat cerebellum and some of its mechanisms. In Palay, S.L. Chan-Palay, V. (Eds The Cerebellum. New Vistas. Springer Verlag, Berlin-Heidelberg, pp. 8 46.
4. Armengol, J.A. Sotelo, C. (1991) Early dendritic development of Purkinje cells in the rat cerebellum. A light and electron microscopic study using axonal tracing in 'in vitro' slices. Dev. Brain Res., 64, 95 114.
5. Burns, D.M., Stehno-Bittel, L. Kawase, T. (2004) Calcitonin gene-related peptide elevates calcium and polarizes membrane potential in MG-63 cells by both cAMP-independent and -dependent mechanisms. Am. J. Physiol. Cell Physiol., 287, C457 C467.
6. Chedotal, A. Sotelo, C. (1993) The 'creeper stage' in cerebellar climbing fiber synaptogenesis precedes the 'pericellular nest'- ultrastructural evidence from parvalbumin immunocytochemistry. Dev. Brain Res., 76, 207 220.
7. Cheng, L., Khan, M. Mudge, A.W. (1995) Calcitonin gene-related peptide promotes Schwann cell proliferation. J. Cell Biol., 129, 789 796.
8. Delaney, C.L., Brenner, M. Messing, A. (1996) Conditional ablation of cerebellar astrocytes in postnatal transgenic mice. J. Neurosci., 16, 6908 6918.
9. Di Cesare, A., Del Piccolo, P., Zacchetti, D. Grohovaz, F. (2006) EP2 receptor stimulation promotes calcium responses in astrocytes via activation of the adenylyl cyclase pathway. Cell. Mol. Life Sci., 63, 2546 2553.
10. 2+ concentration. Am. J. Physiol. Heart Circ. Physiol., 289, H960 H967.
11. Drissi, H., Lasmoles, F., Le Malley, V., Marie, P.J. Lieberherr, M. (1998) Activation of phospholipase C-b1 via Galphaq/11 during calcium mobilization by calcitonin gene-related peptide. J. Biol. Chem., 273, 20168 20174.
12. 2+ concentrations but not cyclic AMP formation in CGRP receptor-positive osteosarcoma cells (OHS-4). Cytokine, 11, 200 207.
13. Evans, B.N., Rosenblatt, M.I., Mnayer, L.O., Oliver, K.R. Dickerson, I.M. (2000) CGRP-RCP, a novel protein required for signal transduction at calcitonin gene-related peptide and adrenomedullin receptors. J. Biol. Chem., 275, 31438 31443.
14. 2+ in rat chromaffin cells in vitro. J. Neurosci., 19, 2945 2953.
15. Haas, C.A., Streit, W.J. Kreutzberg, G.W. (1990) Rat facial motoneurons express increased levels of calcitonin gene-related peptide mRNA in response to axotomy. J. Neurosci. Res., 27, 270 275.
16. 2+- decrease. J. Membr. Biol., 189, 225 236.
17. Kirischuk, S., Möller, T., Voitenko, N., Kettenmann, H. Verkhratsky, A. (1995a) ATP-induced cytoplasmic calcium mobilization in Bergmann glial cells. J. Neurosci., 15, 7861 7871.
18. 2+ release from InsP3-sensitive internal stores in mammalian oligodendrocytes. J. Physiol., 483 (PT 1 41 57.
19. Komuro, H. Yacubova, E. (2003) Recent advances in cerebellar granule cell migration. Cell. Mol. Life Sci., 60, 1084 1098.
20. Lazar, P., Reddington, M., Streit, W., Raivich, G. Kreutzberg, G.W. (1991) The action of calcitonin gene-related peptide on astrocyte morphology and cyclic AMP accumulation in astrocyte cultures from neonatal rat brain. Neurosci. Lett., 130, 99 102.
21. Lordkipanidze, T. Dunaevsky, A. (2005) Purkinje cell dendrites grow in alignment with Bergmann glia. Glia, 51, 229 234.
22. Luebke, A.E., Dahl, G.P., Roos, B.A. Dickerson, I.M. (1996) Identification of a protein that confers calcitonin gene-related peptide responsiveness to oocytes by using a cystic fibrosis transmembrane conductance regulator assay. Proc. Natl. Acad. Sci. U.S.A., 93, 3455 3460.
23. Lyons, S.A. Kettenmann, H. (1998) Oligodendrocytes and microglia are selectively vulnerable to combined hypoxia and hypoglycemia injury in vitro. J. Cereb. Blood Flow Metab., 18, 521 530.
24. Mason, C.A., Christakos, S. Catalano, S.M. (1990) Early climbing fiber interactions with Purkinje cells in the postnatal mouse cerebellum. J. Comp. Neurol., 297, 77 90.
25. Morara, S., Provini, L. Rosina, A. (1989) CGRP expression in the rat olivocerebellar system during postnatal development. Brain Res., 504, 315 319.
26. Morara, S., Sternini, C., Provini, L. Rosina, A. (1995) Developmentally regulated expression of α- and β-CGRP mRNA and CGRP-immunoreactivity in the rat inferior olive. J. Comp. Neurol., 354, 27 38.
27. Morara, S., Marcotti, W., Provini, L. Rosina, A. (1997) Neuropeptide Y (NPY) expression is up-regulated in the rat inferior olive during development. Neuroreport, 8, 3743 3747.
28. Morara, S., Wimalawansa, S.J. Rosina, A. (1998) Monoclonal antibodies reveal expression of the CGRP receptor in Purkinje cells, interneurons and astrocytes of rat cerebellar cortex. Neuroreport, 9, 3755 3759.
29. Morara, S., Rosina, A., Provini, L., Forloni, G., Caretti, A. Wimalawansa, S.J. (2000) Calcitonin gene-related peptide receptor expression in the neurons and glia of developing rat cerebellum: an autoradiographic and immunohistochemical analysis. Neuroscience, 100, 381 391.
30. Morara, S., van der Want, J.J.L., De Weerd, H., Provini, L. Rosina, A. (2001) Ultrastructural analysis of climbing fiber-Purkinje cell synaptogenesis in the rat cerebellum. Neuroscience, 108, 655 671.
31. Moreno, M.J., Cohen, Z., Stanimirovic, D.B. Hamel, E. (1999) Functional calcitonin gene-related peptide type 1 and adrenomedullin receptors in human trigeminal ganglia, brain vessels, and cerebromicrovascular or astroglial cells in culture. J. Cereb. Blood Flow Metab., 19, 1270 1278.
32. Moreno, M.J., Terron, J.A., Stanimirovic, D.B., Doods, H. Hamel, E. (2002) Characterization of calcitonin gene-related peptide (CGRP) receptors and their receptor-activity-modifying proteins (RAMPs) in human brain microvascular and astroglial cells in culture. Neuropharmacology, 42, 270 280.
33. Müller, T., Möller, T., Berger, T., Schnitzer, J. Kettenmann, H. (1992) Calcium entry through kainate receptors and resulting potassium-channel blockade in Bergmann glial cells. Science, 256, 1563 1566.
34. Pokabla, M.J., Dickerson, I.M. Papka, R.E. (2002) Calcitonin gene-related peptide-receptor component protein expression in the uterine cervix, lumbosacral spinal cord, and dorsal root ganglia. Peptides, 23, 507 514.
35. Prado, M.A., Evans-Bain, B., Oliver, K.R. Dickerson, I.M. (2001) The role of the CGRP-receptor component protein (RCP) in adrenomedullin receptor signal transduction. Peptides, 22, 1773 1781.
36. Priller, J., Haas, C.A., Reddington, M. Kreutzberg, G.W. (1995) Calcitonin gene-related peptide and ATP induce immediate early gene expression in cultured rat microglial cells. Glia, 15, 447 457.
37. Rakic, P. (1971) Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus rhesus. J. Comp. Neurol., 141, 283 312.
38. Ramón y Cajal, S. (1911) Histologie du Système Nerveux de l'Homme et de Vertébrés, vol. II. Maloine, Paris.
39. Schiess, M.C., Poindexter, B.J., Brown, B.S. Bick, R.J. (2005) The effects of CGRP on calcium transients of dedifferentiating cultured adult rat cardiomyocytes compared to noncultured adult cardiomyocytes: possible protective and deleterious results in cardiac function. Peptides, 26, 525 530.
40. Schipke, C.G. Kettenmann, H. (2004) Astrocyte responses to neuronal activity. Glia, 47, 226 232.
41. Schmidt, M., Evellin, S., Oude Weernink, P.A., vom Dorp, F., Rehmann, H., Lomasney, J.W. Jacobs, K.H. (2001) A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat. Cell Biol., 3, 1020 1024.
42. Tuschick, S., Kirischuk, S., Kirchhoff, F., Liefeldt, L., Paul, M., Verkhratsky, A. Kettenmann, H. (1997) Bergmann glial cells in situ express endothelinB receptors linked to cytoplasmic calcium signals. Cell Calcium, 21, 409 419.
43. Volterra, A. Steinhäuser, C. (2004) Glial modulation of synaptic transmission in the hippocampus. Glia, 47, 249 257.
44. Yamada, K. Watanabe, M. (2002) Cytodifferentiation of Bergmann glia and its relationship with Purkinje cells. Anat. Sci. Int., 77, 94 108.