Gi-coupled P2Y-ADP receptor mediates GSK-3 phosphorylation and β-catenin nuclear translocation in granule neurons

Journal of Neurochemistry

Volumn 104, Issue 1, 2008, Pages 62-73

  Ortega, Felipe ^a   Pérez Sen, Raquel ^a   Miras Portugal, Ma Teresa ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

catenin; 2 methyl thio ADP; Glycogen synthase kinase 3; Granule neurons; Insulin like growth factor I; Nucleotide receptors; Phosphatidyl inositol 3 kinase Akt

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE; PERTUSSIS TOXIN; PROTEIN KINASE B; WORTMANNIN;

ANIMAL EXPERIMENT; ARTICLE; CATALYST; CELL CULTURE; DNA SYNTHESIS; GRANULE CELL; MOUSE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STATISTICAL ANALYSIS;

ADENOSINE DIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; BETA CATENIN; CELL NUCLEUS; CELLS, CULTURED; CEREBELLUM; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME INHIBITORS; GLYCOGEN SYNTHASE KINASE 3; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; NEURONS; PHOSPHORYLATION; RATS; RATS, WISTAR; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; THIONUCLEOTIDES; TIME FACTORS;

EID: 37249031483     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2007.05021.x     Document Type: Article

References (72)

1. Aberle H., Bauer A., Stappert J., Kispet A. Kemler R. (1997) β-/Catenin is a target for the ubiquitin-proteasome pathway. EMBO J. 16, 3797 3804.
2. Álvarez G., Muñoz-Montano J. R., Satrústegui J., Ávila J., Bogoñez E. Díaz-Nido J. (1999) Lithium protects cultured neurons against β-amyloid-induced neurodegeneration. FEBBS Lett. 453, 260 264.
3. Bhat R. V., Budd Haeberlein S. L. B. Ávila J. (2004) Glycogen synthase kinase-3: a drug target for CNS therapies. J. Neurochem. 89, 1313 1317.
4. Boyer J. L., Mohanram A., Camaioni E., Jacobson K. A. Harden T. K. (1998) Competitive and selective antagonism of P2Y1 receptors by N6-methyl 2′-deoxyadenosine 3′,5′-bisphosphate. Br. J. Pharmacol. 124, 1 3.
5. Burnstock G. (2005) Purinergic signalling: therapeutic potential. Anal. Real. Acad. Nac. Farm. 71, 283 319.
6. Burnstock G. (2006) Historical review: ATP as a neurotransmitter. Trends Pharmacol. Sci. 27, 166 176.
7. Carrasquero L. M. G., Delicado E. G., Jiménez A. I., Pérez-Sen R. Miras-Portugal M. T. (2005) Cerebellar astrocytes co-express several ADP receptors. Presence of functional P2Y13-like receptors. Purinergic Signal. 1, 153 159.
8. Carrasquero L. M. G., Delicado E. G. Miras-Portugal M. T. (2006) Which is the receptor mediating ADP signaling in rat cerebellar astrocytes. Purinergic Signalling, Vol. 2 Abstract. 8th International Symposium on Adenosine and Adenine Nucleotides, Ferrara, Italy, pp. 323.
9. s-axin-β-catenin signalling axis. Science 310, 1504 1510.
10. Chen J., Wu A., Sun H., Drakas R., Garofalo C., Cascio S., Surmacz E. Baserga R. (2005) Functional significance of type 1 insulin-like growth factor-mediated nuclear translocation of the insulin receptor substrate-1 and β-catenin. J. Biol. Chem. 280, 29912 29920.
11. Chin P. C., Majdzadeh N. M. D'Mello S. R. (2005) Inhibition of GSK-3 β is a common event in neuroprotection by different survival factors. Mol. Brain Res. 137, 193 201.
12. Communi D., González N. D., Detheux M., Brezillon S., Lannoy V., Parmentier M. Boeynaems J. M. (2001) Identification of a novel human ADP receptor coupled to G(i). J. Biol. Chem. 276, 41479 41485.
13. Contestabile A. (2002) Cerebellar granule cells as a model to study mechanisms of neuronal apoptosis or survival in vivo and in vitro. Cerebellum 1, 41 55.
14. Cross D. A. E., Culbert A. A., Chalmers K. A., Facci L., Skaper S. D. Reith A. D. (2001) Selective small-molecule inhibitors of glycogen synthase kinase-3 activity protect primary neurons from death. J. Neurochem. 77, 94 102.
15. D'Mello S. R., 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.
16. D'Mello S. R., Anelli R. Calissano P. (1994) Lithium induces apoptosis in immature cerebellar granule neurons but promotes survival of mature neurons. Exp. Cell Res. 211, 332 338.
17. Davies S. P., Reddy H., Caivano M. Cohen P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95 105.
18. Desbois-Mouthon C., Cadoret A., Blivet-Van Eggelpöel M-J., Bertrand F., Cherqui G., Perret C. Capeau J. (2001) Insulin and IGF-1 stimulate the β-catenin pathway through two signalling cascades involving GSK-3β inhibition and Ras activation. Oncogene 20, 252 259.
19. Ding V. W., Chen R.-H. McCormick F. (2000) Differential regulation of glycogen synthase kinase 3β by insulin and Wnt signalling. J. Biol. Chem. 275, 32475 32481.
20. DiVirgilio F. (2005) Purinergic mechanism in the immune system: a signal of danger for dendritic cells. Purinergic Signal. 1, 205 209.
21. Domínguez I. Green J. B. A. (2001) Missing links in GSK3 regulation. Dev. Biol. 235, 303 313.
22. Engel T., Hernández F., Ávila J. Lucas J. J. (2006) Full reversal of Alzheimer's disease-like phenotype in a mouse model with conditional overexpression of glycogen synthase kinase-3. J. Neurosci. 26, 5083 5090.
23. Erlinge D. (1998) Extracellular ATP: a growth factor for vascular smooth muscle cells. Gen. Pharmacol. 31, 1 8.
24. 13 receptor. Biochem. Pharmacol. 68, 113 124.
25. Gerasimovskaya E. V., Tucker D. A., Weiser-Evans M., Wenzlau J. M., Klemm D. J., Banks M. Stenmark K. R. (2005) Extracellular ATP-induced proliferation of adventitial fibroblasts requires phosphoinositide 3-kinase, Akt, mammalian target of rapamycin and p70 S6 kinase signaling pathways. J. Biol. Chem. 280, 1838 1848.
26. Gerevich Z. Illes P. (2004) P2Y receptors and pain transmission. Purinergic Signal. 1, 3 10.
27. Grimes C. A. Jope R. S. (2001) The multifaceted roles of glycogen synthase kinase 3β in cellular signalling. Prog. Neurobiol. 65, 391 426.
28. Hall A. C., Brennan A., Goold R. G., Cleverley K., Lucas F. R., Gordon-Weeks P. R. Salinas P. C. (2002) Valproate regulates GSK-3-mediated axonal remodelling and synapsin I clustering in developing neurons. Mol. Cell. Neurosci. 20, 257 270.
29. 12 receptors at the level of calcium signalling in human platelets. Blood 104, 1745 1752.
30. Harris T. J. C. Peifer M. (2005) Decisions: β-catenin chooses between adhesion and transcription. Trends Cell Biol. 15, 234 237.
31. Hashimoto M., Sagara Y., Langford D., Everall I. P., Mallory M., Everson A., Digicaylioglu M. Masliah E. (2002) Fibroblast growth factor 1 regulates signalling via the glycogen synthase kinase-3β pathway. J. Biol. Chem. 277, 32985 32991.
32. Hervás C., Pérez-Sen R. Miras-Portugal M. T. (2003) Coexpression of functional P2X and P2Y nucleotide receptors in single cerebellar granule cells. J. Neurosci. Res. 73, 384 399.
33. Hetman M., Cavanaugh J. E., Kimelman D. Xia Z. (2000) Role of glycogen synthase kinase-3β in neuronal apoptosis induced by trophic withdrawal. J. Neurosci. 20, 2567 2574.
34. Hollopeter G., Jantzen H.-M., Vincent D. et al. (2001) Identification of platelet ADP receptor targeted by antithrombotic drugs. Nature 409, 202 207.
35. Holnthoner W., Pillinger M., Gröger M., Wolff K., Ashton A. W., Albanese C., Neumeister P., Pestell R. G. Petzelbauer P. (2002) Fibroblast growth factor-2 induces Lef/Tcf-dependent transcription in human endothelial cells. J. Biol. Chem. 277, 45847 45853.
36. 4 receptors. Purinergic Signal. 1, 95 100.
37. 2B receptors stimulation and other signals coupled to Gs proteins in type-1 cerebellar astrocytes. Glia 26, 119 128.
38. Jope R. S. Johnson G. V. W. (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29, 95 102.
39. Kim S-E., Lee W-J. Choi K-Y. (2007) The PI3 kinase-Akt pathway mediates Wnt3a-induced proliferation. Cell. Signal. 19, 511 518.
40. Kucher B. M. Neary J. T. (2005) Bi-functional effects of ATP/P2 receptor activation on tumour necrosis factor-α release in lipopolysaccharide- stimulated astrocytes. J. Neurochem. 82, 525 535.
41. ADP receptor. J. Neurochem. 77, 505 518.
42. 7 receptors induce calcium/calmodulin- dependent protein kinase II phosphorylation in cerebellar granule neurons. Eur. J. Neurosci. 23, 2999 3013.
43. Lucas J. J., Hernández F., Gómez-Ramos P., Moran M. A., Hen R. Ávila J. (2001) Decreased nuclear beta-catenin, tau hyperphorphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J. 20, 27 39.
44. McManus E. J., Sakamoto K., Armit L. J., Ronaldson L., Shpiro N., Marquez R. Alessi D. R. (2005) Role that phosphorylation of GSK-3 plays in insulin and Wnt signalling defined by knocking analysis. EMBO J. 24, 1571 1583.
45. 13. Mol. Pharmacol. 64, 104 112.
46. Marteau F., Communi D., Boeynaems J.-M. Suarez-Gonzalez N. (2004) Involvement of multiple P2Y receptors and signalling pathways in the action of adenine nucleotides diphosphates on human monocyte-derived dendritic cells. J. Leukoc. Biol. 76, 796 803.
47. Meyer-Franke A., Kaplan M. R., Pfrieger F. W. Barres B. A. (1995) Characterisation of the signalling interactions that promote the survival and growth of developing retinal ganglion cells in culture. Neuron 15, 805 819.
48. Miller T. M., Tansey M. G., Johnson E. M. Creedon D. J. (1997) Inhibition of phosphatidylinositol 3-kinase activity blocks depolarization- and insulin-like growth factor I-mediated survival of cerebellar granule neurons. J. Biol. Chem. 272, 9847 9853.
49. Naito A. T., Akazawa H., Takano H., Minamino T., Nagai T., Aburatani H. Komuro I. (2005) Phosphatidylinositol 3-kinase-Akt pathway plays a critical role in early cardiomyogenesis by regulating canonical Wnt signaling. Circ. Res. 97, 144 151.
50. Neary J. T. Kang Y. (2005) Signaling from P2 nucleotide receptors to protein kinase cascades induced by CNS injury. Mol. Neurobiol. 31, 95 103.
51. Neary J. T. Kang Y. (2006) P2 purinergic receptors signal to glycogen synthase kinase-3beta in astrocytes. J. Neurosci. Res. 84, 515 524.
52. Neary J. T., McCarthy M., Cornel-Bell A. Kang Y. (1999) Trophic signalling pathways activated by purinergic receptors in rat and human astroglia. Prog. Brain Res. 120, 323 332.
53. North R. A. (2002) Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013 1067.
54. Novak A. Dedhar S. (1999) Signaling through β-catenin and Lef/Tcf. Cell. Mol. Life Sci. 56, 532 537.
55. Pap M. Cooper G. M. (1998) Role of glycogen synthase kinase-3 in the phosphotidylinositol 3-kinase/Akt cell survival pathway. J. Biol. Chem. 273, 19929 19932.
56. Papkoff J. (1996) Regulation of complexed and free catenin pools by distinct mechanisms. J. Biol. Chem. 272, 4536 4543.
57. Papkoff J. Aikawa M. (1998) Wnt and HGF regulate GSK3 beta activity and beta-catenin signalling in mammary epithelial cells. Biochem. Biophys. Res Comm. 247, 851 858.
58. Playford M. P., Bicknell D., Bodmer W. F. Macaulay V. M. (2000) Insulin-like growth factor 1 regulates the location, stability, and transcriptional activity of β-catenin. Proc. Natl Acad. Sci. 97, 12103 12108.
59. Pons S., Trejo J. L., Martínez-Morales J. R. Martí E. (2001) Vitronectin regulates sonic hedgehog activity during cerebellum development through CREB phosphorylation. Development 128, 1481 1492.
60. Ralevic V. Burnstock G. (1998) Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413 492.
61. Sayas C. L., Ávila J. Wandosell F. (2002) Regulation of neuronal cytoskeleton by lysophosphatidic acid: role of GSK-3. Biochim. Biophys. Acta 1582, 144 153.
62. 1 receptor stimulate mitogen-activated protein kinases and induce apoptosis. J. Biol. Chem. 276, 16379 16390.
63. 2 stimulates the β-catenin/T cell factor-dependent transcription in colon cancer. J. Biol. Chem. 280, 26565 26572.
64. Shevtsov S. P., Haq S. Force T. (2006) Activation of β-catenin signalling pathways by classical G-protein-coupled receptors. Cell Cycle 5, 2295 2300.
65. Spychala J. Kitajewski J. (2004) Wnt and β-catenin signalling target the expression of ecto-5′-nucleotidase and increase extracellular adenosine generation. Exp. Cell Res. 296, 99 108.
66. Stambolic V. Woodgett J. R. (1994) Mitogen inactivation of glycogen synthase kinase-3b in intact cells via serine 9 phosphorylation. Biochem. J. 303, 701 704.
67. Subramaniam S., Strelau J. Unsicker K. (2003) Growth differentiation factor-15 prevents low potassium-induced cell death of cerebellar granule neurons by differential regulation of Akt and ERK pathways. J. Biol. Chem. 278, 8904 8912.
68. 12 receptor signalling towards PKB proceeds through IGF-I receptor cross-talk and requires activation of Src, Pyk2 and Rap1. Cell. Signal. 18, 1169 1181.
69. Vitolo O. V., Ciotti M. T., Galli C., Borsello T. Calissano P. (1998) Adenosine and ADP prevent apoptosis in cultured rat cerebellar granule cells. Brain Res. 809, 297 301.
70. Yang M., Zhong W. W., Srivastava N., Slavin A., Yang J., Hoey T. An S. (2005) G protein-coupled lysophosphatidic acid receptors stimulate proliferation of colon cancer cells through the β-catenin pathway. Proc. Natl Acad. Sci. 102, 6027 6032.
71. Zhang F. L., Luo L., Gustafson E. et al. (2001) ADP is the cognate ligand for the orphan G-protein-coupled receptor SP1999. J. Biol. Chem. 276, 8608 8615.
72. 13: identification and characterization of a novel Gαi-coupled ADP receptor from human and mouse. J. Pharmacol. Exp. Ther. 301, 705 713.