PHCCC, a specific enhancer of type 4 metabotropic glutamate receptors, reduces proliferation and promotes differentiation of cerebellar granule cell neuroprecursors

Journal of Neuroscience

Volumn 24, Issue 46, 2004, Pages 10343-10352

  Canudas, A M ^a   Di Giorgi Gerevini, V ^a   Iacovelli, L ^a,b   Nano, G ^a   D'Onofrio, M ^b   Arcella, A ^b   Giangaspero, F ^a   Busceti, C ^b   Ricci Vitiani, L ^c   Battaglia, G ^b   Nicoletti, F ^a,b   Melchiorri, Daniela ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b IRCCS NEUROMED   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Cerebellar granule cell neuroprecursors; Development; Differentiation; PHCCC; Proliferation; Type 4 metabotropic glutamate receptor

Indexed keywords

AMIDE; CYCLIC AMP; FORSKOLIN; GLUTAMATE RECEPTOR AGONIST; METABOTROPIC RECEPTOR 4; N PHENYL 7 (HYDROXYAMINO)CYCLOPROPA[B]CHROMEN 1A CARBOXAMIDE; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CEREBELLUM; GRANULE CELL; HISTOLOGY; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; ANIMALS, NEWBORN; BENZOPYRANS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CEREBELLUM; CYCLIC AMP; DEPRESSION, CHEMICAL; MICE; MICE, KNOCKOUT; NEURITES; NEURONS; ORGAN SIZE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; STEM CELLS; THYMIDINE;

EID: 20844457754     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3229-04.2004     Document Type: Article

References (47)

1. Altman J, Bayer S (1996) An overview of the postnatal development of the rat cerebellum. In: Development of the cerebellar system: in relation to its evolution, structure, and function, pp 324-333. Boca Raton, FL: CRC.
2. Annoura H, Fukunaga A, Uesugi M, Tatuoka T, Horikawa Y (1996) A novel class of antagonists for metabotropic glutamate receptors, 7-(hydroxyimino) cyclopropa[b]chromen-1a-carbozylates. Bioorg Med Chem Lett 5:223-228.
3. Cameron HA, McEwen BS, Gould E (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687-4692.
4. Catania MV, Landwehrmeyer GB, Testa CM, Standaert DG, Penney Jr JB, Young AB (1994) Metabotropic glutamate receptors are differentially regulated during development. Neuroscience 61:481-495.
5. Catania MV, Bellomo M, Di Giorgi-Gerevini V, Seminara G, Giuffrida R, Romeo R, De Blasi A, Nicoletti F (2001) Endogenous activation of group-I metabotropic glutamate receptors is required for differentiation and survival of cerebellar Purkinje cells. J Neurosci 21:7664-7673.
6. Copani A, Casabona G, Bruno V, Caruso A, Condorelli DF, Messina A, Di Giorgi Gerevini V, Pin JP, Kuhn R, Knopfel T, Nicoletti F (1998) The metabotropic glutamate receptor mGlu5 controls the onset of developmental apoptosis in cultured cerebellar neurons. Eur J Neurosci 10:2173-2184.
7. Dahmane N, Ruiz-i-Altaba A (1999) Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126:3089-3100.
8. De Blasi A, Conn PJ, Pin J, Nicoletti F (2001) Molecular determinants of metabotropic glutamate receptor signaling. Trends Pharmacol Sci 22:114-120.
9. DiCicco-Bloom E, Black IB (1989) Depolarization and insulin-like growth factor-I (IGF-I) differentially regulate the mitotic cycle in cultured rat sympathetic neuroblasts. Brain Res 10:403-406.
10. D'Mello SR, Galli C, Ciotti T, Calissano P (1993) Induction of apoptosis in cerebellar granule neurons by low potassium: inhibition of death by insulin-like growth factor I and cAMP. Proc Natl Acad Sci USA 90:10989-10993.
11. Dudek SM, Bear MF (1989) A biochemical correlate of the critical period for synaptic modification in the visual cortex. Science 246:673-675.
12. Flint AC, Dammerman RS, Kriegstein AR (1999) Endogenous activation of metabotropic glutamate receptors in neocortical development causes neuronal calcium oscillations. Proc Natl Acad Sci USA 12:12144-12149.
13. Follenzi A, Ailles LE, Bakovic S, Geuna M, Naldini L (2000) Gene transfer by lentiviralvectors is limited by nuclear translocation and rescued by HIV-1 pol sequences. Nat Genet 25:217-222.
14. Furuta A, Martin LJ (1999) Laminar segregation of the cortical plate during corticogenesis is accompanied by changes in glutamate receptor expression. J Neurobiol 39:67-80.
15. Gao WQ, Heintz N, Hatten ME (1991) Cerebellar granule cell neurogenesis is regulated by cell-cell interaction in vitro. Neuron 6:705-715.
16. Gould E, Cameron HA, McEwen BS (1994) Blockade of NMDA receptors increases cell death and birth in the developing rat dentate gyrus. J Comp Neurol 340:551-565.
17. Hahn H, Christiansen J, Wicking C, Zaphiropoulos PG, Chidambaram A, Gerrard B, Vorechovsky I, Bale AE, Toftgard R, Dean M, Wainwright B (1996) A mammalian patched homolog is expressed in target tissues of sonic hedgehog and maps to a region associated with developmental abnormalities. J Biol Chem 271:12125-12128.
18. Hannan AJ, Blakemore C, Katsnelson A, Vitalis T, Huber KM, Bear M, Roder J, Kim D, Shin HS, Kind PC (2001) PLC-beta1, activated via mGluRs, mediates activity-dependent differentiation in cerebral cortex. Nat Neurosci 4:282-288.
19. Heck S, Enz R, Richter-Landsberg C, Blohm DH (1997) Expression of eight metabotropic glutamate receptor subtypes during neuronal differentiation of P19 embryocarcinoma cells: a study by RT-PCR and in situ hybridization. Brain Res Dev Brain Res 18:85-91.
20. Huber KM, Sawtell NB, Bear MF (1998) Effects of the metabotropic glutamate receptor antagonist MCPG on phosphoinositide turnover and synaptic plasticity in visual cortex. J Neurosci 18:1-9.
21. Huber KM, Gallagher SM, Warren ST, Bear MF (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 99:7746-7750.
22. Hynes M, Stone DM, Dowd M, Pitts-Meek S, Goddard A, Gurney A, Rosenthal A (1997) Control of cell pattern in the neural tube by the zinc finger transcription factor and oncogene Gli-1. Neuron 19:15-26.
23. Iacovelli L, Bruno V, Salvatore L, Melchiorri D, Gradini R, Caricasole A, Barletta E, De Blasi A, Nicoletti F (2002) Native group-III metabotropic glutamate receptors are coupled to the mitogen-activated protein kinase/ phosphatidylinositol-3-kinase pathways. J Neurochem 82:216-223.
24. Iacovelli L, Capobianco L, Iula M, Di Giorgi Gerevini V, Picascia A, Blahos J, Melchiorri D, Nicoletti F, De Blasi A (2004) Regulation of mGlu4 metabotropic glutamate receptor signaling by type-2 G-protein coupled receptor kinase (GRK2). Mol Pharmacol 65:1103-1110.
25. Katoh-Semba R, Asano T, Ueda H, Morishita R, Takeuchi IK, Inaguma Y, Kato K (2002) Riluzole enhances expression of brain-derived neurotrophic factor with consequent proliferation of granule precursor cells in the rat hippocampus. FASEB J 16:1328-1330.
26. Kinzie JM, Saugstad JA, Westbrook GL, Segerson TP (1995) Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain. Neuroscience 69:167-176.
27. Lee JJ, Ekker SC, von Kessler DP, Porter JA, Sun BI, Beachy PA (1994) Autoproteolysis in hedgehog protein biogenesis. Science 266:1528-1537.
28. Lin X, Bulleit RF (1997) Insulin-like growth factor I (IGF-I) is a critical trophic factor for developing cerebellar granule cells. Brain Res Dev Brain Res 99:234-242.
29. Lo Turco JJ, Owens DF, Heath MJ, Davis MB, Kriegstein AR (1995) GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis. Neuron 15:1287-1298.
30. Maj M, Bruno V, Dragic Z, Yamamoto R, Battaglia G, Inderbitzin W, Stoehr N, Stein T, Gasparini F, Vranesic I, Kuhn R, Nicoletti F, Flor PJ (2003) (-)-PHCCC, a positive allosteric modulator of mGluR4: characterization, mechanism of action, and neuroprotection. Neuropharmacology 45:895-906.
31. Melchiorri D, Bruno V, Besong G, Ngomba RT, Cuomo L, De Blasi A, Copani A, Moschella C, Storto M, Nicoletti F, Lepperdinger G, Passarelli F (2001) The mammalian homologue of the novel peptide Bv8 is expressed in the central nervous system and supports neuronal survival by activating the MAP kinase/PI-3-kinase pathways. Eur J Neurosci 13:1694-1702.
32. Nicoletti F, Iadarola MJ, Wroblewski JT, Novelli A, Alho H, Guidotti A, Costa E (1986) The activation of inositol phospholipid hydrolysis as a signal transducing system for excitatory amino acids in primary cultures of cerebellar granule cells. J Neurosci 6:1905-1911.
33. Nicot A, Lelievre V, Tam J, Waschek JA, DiCicco-Bloom E (2002) Pituitary adenylate cyclase-activating polypeptide and sonic hedgehog interact to control cerebellar granule precursor cell proliferation. J Neurosci 22:9244-9254.
34. Nielsen HS, Hannibal J, Fahrenkrug J (1998) Expression of pituitary adenylate cyclase activating polypeptide (PACAP) in the postnatal and adult rat cerebellar cortex. NeuroReport 9:2639-2642.
35. Pekhletski R, Gerlai R, Overstreet LS, Huang XP, Agopyan N, Slater NT, Abramow-Newerly W, Roder JC, Hampson DR (1996) Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J Neurosci 16:6364-6373.
36. Pons S, Trejo JL, Martinez-Morales JR, Marti E (2001) Vitronectin regulates Sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128:35-43.
37. Provias JP, Becker LE (1996) Cellular and molecular pathology of medulloblastoma. J Neuro-oncol 29:35-43.
38. Ruiz-i-Altaba A (1998) Combinatorial Gli gene function in floor plate and neuronal inductions by Sonic hedgehog. Development 125:2203-2212.
39. Schoepp DD, Jane DE, Monn JA (1999) Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38:1431-1476.
40. Schwartz HL, Ross ME, Oppenheimer JH (1997) Lack of effect of thyroid hormone on late fetal rat brain development. Endocrinology 138:3119-3124.
41. Skoglosa Y, Patrone C, Lindholm D (1999) Pituitary adenylate cyclase activating polypeptide is expressed by developing rat Purkinje cells and decreases the number of cerebellar gamma-amino butyric acid positive neurons in culture. Neurosci Lett 23:207-210.
42. Valerio A, Rizzonelli P, Paterlini M, Moretto G, Knopfel T, Kuhn R, Memo M, Spano P (1997) mGluR5 metabotropic glutamate receptor distribution in rat and human spinal cord: a developmental study. Neurosci Res 28:49-57.
43. Van den Pol AN, Kogelman L, Ghosh P, Liljelund P, Blackstone C (1994) Developmental regulation of the hypothalamic metabotropic glutamate receptor mGluR1. J Neurosci 14:3816-3834.
44. Wallace VA (1999) Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. Curr Biol 22:445-448.
45. Wechsler-Reya RJ, Scott MP (1999) Control of neuronal precursor proliferation in the cerebellum by Sonic hedgehog. Neuron 22:103-114.
46. Ye P, Xing Y, Dai Z, D'Ercole AJ (1996) In vivo actions of insulin-like growth factor-I (IGF-I) on cerebellum development in transgenic mice: evidence that IGF-I increases proliferation of granule cell progenitors. Brain Res Dev Brain Res 20:44-54.
47. Zirpel L, Janowiak MA, Taylor DA, Parks TN (2000) Developmental changes in metabotropic glutamate receptor-mediated calcium homeostasis. J Comp Neurol 22:95-106.