Muscarinic acetylcholine receptors mediate oligodendrocyte progenitor survival through Src-like tyrosine kinases and PI3K/Akt pathways

Neurochemistry International

Volumn 48, Issue 5, 2006, Pages 383-393

  Cui, Qiao Ling ^a   Fogle, Eli ^a   Almazan, Guillermina ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Akt; MAPK; Muscarinic receptors; Myelin; Oligodendrocytes; PI3K; Src; Survival

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; 2 MORPHOLINO 8 PHENYLCHROMONE; 4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; ATROPINE; BINDING PROTEIN; CARBACHOL; CYCLIC AMP; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MUSCARINIC RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE FYN; PROTEIN TYROSINE KINASE; WORTMANNIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DRUG EFFECT; NEUROTRANSMISSION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; STEM CELL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACETYLCHOLINE; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; CASPASE 3; CASPASES; CELL DIFFERENTIATION; CELL SURVIVAL; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; ENZYME INHIBITORS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; MAP KINASE SIGNALING SYSTEM; MUSCARINIC AGONISTS; MUSCARINIC ANTAGONISTS; MYELIN SHEATH; OLIGODENDROGLIA; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-FYN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, MUSCARINIC; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; STEM CELLS;

ANIMALIA;

EID: 33644643568     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2005.11.014     Document Type: Article

References (65)

1. D.R. Alessi, M. Deak, A. Casamayor, F.B. Caudwell, N. Morrice, D.G. Norman, P. Gaffney, C.B. Reese, C.N. MacDougall, D. Harbison, A. Ashworth, and M. Bownes 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase Curr. Biol. 7 1997 776 789
2. A. Bonni, A. Brunet, A.E. West, S.R. Datta, M.A. Takasu, and M.E. Greenberg Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and -independent mechanisms Science 286 1999 1358 1362
3. D.C. Budd, J. McDonald, N. Emsley, K. Cain, and A.B. Tobin The C-terminal tail of the M3-muscarinic receptor possesses anti-apoptotic properties J. Biol. Chem. 278 2003 19565 19573
4. L.C. Cantley The phosphoinositide 3-kinase pathway Science 296 2002 1655 1657
5. Y.H. Chen, J. Pouyssegur, S.A. Courtneidge, and E. Van Obberghen-Schilling Activation of Src family kinase activity by the G protein-coupled thrombin receptor in growth-responsive fibroblasts J. Biol. Chem. 269 1994 27372 27377
6. V. Cleghon, and D.K. Morrison Raf-1 interacts with Fyn and Src in a non-phosphotyrosine-dependent manner J. Biol. Chem. 269 1994 17749 17755
7. R.I. Cohen, and G. Almazan Rat oligodendrocytes express muscarinic receptors coupled to phosphoinositide hydrolysis and adenylyl cyclase Eur. J. Neurosci. 6 1994 1213 1224
8. R.I. Cohen, E. Molina-Holgado, and G. Almazan Carbachol stimulates c-fos expression and proliferation in oligodendrocyte progenitors Brain Res. Mol. Brain Res. 43 1996 193 201
9. Q.L. Cui, W.H. Zheng, R. Quirion, and G. Almazan Inhibition of Src-like kinases reveals Akt-dependent and -independent pathways in insulin-like growth factor I-mediated oligodendrocyte progenitor survival J. Biol. Chem. 280 2005 8918 8928
10. P. De Sarno, S.A. Shestopal, T.D. King, A. Zmijewska, L. Song, and R.S. Jope Muscarinic receptor activation protects cells from apoptotic effects of DNA damage, oxidative stress, and mitochondrial inhibition J. Biol. Chem. 278 2003 11086 11093
11. K. Du, and M. Montminy CREB is a regulatory target for the protein kinase Akt/PKB J. Biol. Chem. 273 1998 32377 32379
12. S. Ebner, M. Dunbar, and R.D. McKinnon Distinct roles for PI3K in proliferation and survival of oligodendrocyte progenitor cells J. Neurosci. Res. 62 2000 336 345
13. R.D. Fields Volume transmission in activity-dependent regulation of myelinating glia Neurochem. Int. 45 2004 503 509
14. A. Fisher Therapeutic strategies in Alzheimer's disease: M1 muscarinic agonists Jpn. J. Pharmacol. 84 2000 101 112
15. A.I. Flores, B.S. Mallon, T. Matsui, W. Ogawa, A. Rosenzweig, T. Okamoto, and W.B. Macklin Akt-mediated survival of oligodendrocytes induced by neuregulins J. Neurosci. 20 2000 7622 7630
16. O.V. Forlenza, J.M. Spink, R. Dayanandan, B.H. Anderton, O.F. Olesen, and S. Lovestone Muscarinic agonists reduce tau phosphorylation in non-neuronal cells via GSK-3beta inhibition and in neurons J. Neural. Transm. 107 2000 1201 1212
17. M. Guizzetti, and L.G. Costa Activation of phosphatidylinositol 3 kinase by muscarinic receptors in astrocytoma cells Neuroreport 12 2001 1639 1642
18. J.S. Gutkind, and K.C. Robbins Activation of transforming G protein-coupled receptors induces rapid tyrosine phosphorylation of cellular proteins, including p125FAK and the p130 v-src substrate Biochem. Biophys. Res. Commun. 188 1992 155 161
19. C.P. Hodgkinson, E.M. Sale, and G.J. Sale Characterization of PDK2 activity against protein kinase B gamma Biochemistry 41 2002 10351 10359
20. T. Igishi, and J.S. Gutkind Tyrosine kinases of the Src family participate in signaling to MAP kinase from both Gq and Gi-coupled receptors Biochem. Biophys. Res. Commun. 244 1998 5 10
21. T. Jelinek, P. Dent, T.W. Sturgill, and M.J. Weber Ras-induced activation of Raf-1 is dependent on tyrosine phosphorylation Mol. Cell. Biol. 16 1996 1027 1034
22. T. Jiang, and Y. Qiu Interaction between Src and a C-terminal proline-rich motif of Akt is required for Akt activation J. Biol. Chem. 278 2003 15789 15793
23. C. Jimenez, C. Hernandez, B. Pimentel, and A.C. Carrera The p85 regulatory subunit controls sequential activation of phosphoinositide 3-kinase by Tyr kinases and Ras J. Biol. Chem. 277 2002 41556 41562
24. R.S. Jope, L. Song, C.A. Grimes, and L. Zhang Oxidative stress oppositely modulates protein tyrosine phosphorylation stimulated by muscarinic G protein-coupled and epidermal growth factor receptors J. Neurosci. Res. 55 1999 329 340
25. A. Khorchid, J.N. Larocca, and G. Almazan Characterization of the signal transduction pathways mediating noradrenaline-stimulated MAPK activation and c-fos expression in oligodendrocyte progenitors J. Neurosci. Res. 58 1999 765 778
26. T.D. King, G.N. Bijur, and R.S. Jope Caspase-3 activation induced by inhibition of mitochondrial complex I is facilitated by glycogen synthase kinase-3beta and attenuated by lithium Brain Res. 919 2001 106 114
27. J.N. Larocca, and G. Almazan Acetylcholine agonists stimulate mitogen-activated protein kinase in oligodendrocyte progenitors by muscarinic receptors J. Neurosci. Res. 50 1997 743 754
28. J.N. Larocca, A. Cervone, and R.W. Ledeen Stimulation of phosphoinositide hydrolysis in myelin by muscarinic agonist and potassium Brain Res. 436 1987 357 362
29. J.N. Larocca, R.W. Ledeen, B. Dvorkin, and M.H. Makman Muscarinic receptor binding and muscarinic receptor-mediated inhibition of adenylate cyclase in rat brain myelin J. Neurosci. 7 1987 3869 3876
30. C. Leloup, D.M. Michaelson, A. Fisher, T. Hartmann, K. Beyreuther, and R. Stein M1 muscarinic receptors block caspase activation by phosphoinositide 3-kinase- and MAPK/ERK-independent pathways Cell. Death Differ. 7 2000 825 833
31. L. Lindenboim, R. Pinkas-Kramarski, M. Sokolovsky, and R. Stein Activation of muscarinic receptors inhibits apoptosis in PC12M1 cells J. Neurochem. 64 1995 2491 2499
32. H.N. Liu, J.N. Larocca, and G. Almazan Molecular pathways mediating activation by kainate of mitogen-activated protein kinase in oligodendrocyte progenitors Brain Res. Mol. Brain Res. 66 1999 50 61
33. M. Lopez-Ilasaca, P. Crespo, P.G. Pellici, J.S. Gutkind, and R. Wetzker Linkage of G protein-coupled receptors to the MAPK signaling pathway through PI 3-kinase gamma Science 275 1997 394 397
34. Y. Lu, Q. Yu, J.H. Liu, J. Zhang, H. Wang, D. Koul, J.S. McMurray, X. Fang, W.K. Yung, K.A. Siminovitch, and G.B. Mills Src family protein-tyrosine kinases alter the function of PTEN to regulate phosphatidylinositol 3-kinase/AKT cascades J. Biol. Chem. 278 2003 40057 40066
35. Y.C. Ma, J. Huang, S. Ali, W. Lowry, and X.Y. Huang Src tyrosine kinase is a novel direct effector of G proteins Cell 102 2000 635 646
36. E. Molina-Holgado, A. Khorchid, H.N. Liu, and G. Almazan Regulation of muscarinic receptor function in developing oligodendrocytes by agonist exposure Br. J. Pharmacol. 138 2003 47 56
37. E. Molina-Holgado, J.M. Vela, A. Arevalo-Martin, G. Almazan, F. Molina-Holgado, J. Borrell, and C. Guaza Cannabinoids promote oligodendrocyte progenitor survival: involvement of cannabinoid receptors and phosphatidylinositol-3 kinase/Akt signaling J. Neurosci. 22 2002 9742 9753
38. C. Murga, S. Fukuhara, and J.S. Gutkind A novel role for phosphatidylinositol 3-kinase beta in signaling from G protein-coupled receptors to Akt J. Biol. Chem. 275 2000 12069 12073
39. C. Murga, L. Laguinge, R. Wetzker, A. Cuadrado, and J.S. Gutkind Activation of Akt/protein kinase B by G protein-coupled receptors. A role for alpha and beta gamma subunits of heterotrimeric G proteins acting through phosphatidylinositol-3-OH kinasegamma J. Biol. Chem. 273 1998 19080 19085
40. D.J. Osterhout, A. Wolven, R.M. Wolf, M.D. Resh, and M.V. Chao Morphological differentiation of oligodendrocytes requires activation of Fyn tyrosine kinase J. Cell. Biol. 145 1999 1209 1218
41. M. Pap, and G.M. Cooper Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway J. Biol. Chem. 273 1998 19929 19932
42. M. Pende, T.L. Fisher, P.B. Simpson, J.T. Russell, J. Blenis, and V. Gallo Neurotransmitter- and growth factor-induced cAMP-response element binding protein phosphorylation in glial cell progenitors: role of calcium ions, protein kinase C, and mitogen-activated protein kinase/ribosomal S6 kinase pathway J. Neurosci. 17 1997 1291 1301
43. S. Pugazhenthi, A. Nesterova, C. Sable, K.A. Heidenreich, L.M. Boxer, L.E. Heasley, and J.E. Reusch Akt/protein kinase B up-regulates Bcl-2 expression through cAMP-response element-binding protein J. Biol. Chem. 275 2000 10761 10766
44. F. Ragheb, E. Molina-Holgado, Q.L. Cui, A. Khorchid, H.N. Liu, J.N. Larocca, and G. Almazan Pharmacological and functional characterization of muscarinic receptor subtypes in developing oligodendrocytes J. Neurochem. 77 2001 1396 1406
45. K. Rosenblum, M. Futter, M. Jones, E.C. Hulme, and T.V. Bliss ERKI/II regulation by the muscarinic acetylcholine receptors in neurons J. Neurosci. 20 2000 977 985
46. H.S. Saini, K.M. Gorse, L.M. Boxer, and C. Sato-Bigbee Neurotrophin-3 and a CREB-mediated signaling pathway regulate Bcl-2 expression in oligodendrocyte progenitor cells J. Neurochem. 89 2004 951 961
47. C. Sato-Bigbee, S. Pal, and A.K. Chu Different neuroligands and signal transduction pathways stimulate CREB phosphorylation at specific developmental stages along oligodendrocyte differentiation J. Neurochem. 72 1999 139 147
48. U.B. Schambra, K.K. Sulik, P. Petrusz, and J.M. Lauder Ontogeny of cholinergic neurons in the mouse forebrain J. Comp. Neurol. 288 1989 101 122
49. M. Schlumpf, J.M. Palacios, R. Cortes, and W. Lichtensteiger Regional development of muscarinic cholinergic binding sites in the prenatal rat brain Neuroscience 45 1991 347 357
50. B.E. Slack The m3 muscarinic acetylcholine receptor is coupled to mitogen-activated protein kinase via protein kinase C and epidermal growth factor receptor kinase Biochem. J. 348 Pt 2 2000 381 387
51. L. Soane, H.J. Cho, F. Niculescu, H. Rus, and M.L. Shin C5b-9 terminal complement complex protects oligodendrocytes from death by regulating Bad through phosphatidylinositol 3-kinase/Akt pathway J. Immunol. 167 2001 2305 2311
52. T.C. Somervaille, D.C. Linch, and A. Khwaja Growth factor withdrawal from primary human erythroid progenitors induces apoptosis through a pathway involving glycogen synthase kinase-3 and Bax Blood 98 2001 1374 1381
53. B.R. Sperber, E.A. Boyle-Walsh, M.J. Engleka, P. Gadue, A.C. Peterson, P.L. Stein, S.S. Scherer, and F.A. McMorris A unique role for Fyn in CNS myelination J. Neurosci. 21 2001 2039 2047
54. B.R. Sperber, and F.A. McMorris Fyn tyrosine kinase regulates oligodendroglial cell development but is not required for morphological differentiation of oligodendrocytes J. Neurosci. Res. 63 2001 303 312
55. E. Sykova, and A. Chvatal Glial cells and volume transmission in the CNS Neurochem. Int. 36 2000 397 409
56. S.M. Thomas, and J.S. Brugge Cellular functions regulated by Src family kinases Annu. Rev. Cell. Dev. Biol. 13 1997 513 609
57. K. Touhara, B.E. Hawes, T. van Biesen, and R.J. Lefkowitz G protein beta gamma subunits stimulate phosphorylation of Shc adapter protein Proc. Natl. Acad. Sci. U.S.A. 92 1995 9284 9287
58. H. Umemori, Y. Kadowaki, K. Hirosawa, Y. Yoshida, K. Hironaka, H. Okano, and T. Yamamoto Stimulation of myelin basic protein gene transcription by Fyn tyrosine kinase for myelination J. Neurosci. 19 1999 1393 1397
59. B. Vanhaesebroeck, S.J. Leevers, K. Ahmadi, J. Timms, R. Katso, P.C. Driscoll, R. Woscholski, P.J. Parker, and M.D. Waterfield Synthesis and function of 3-phosphorylated inositol lipids Annu. Rev. Biochem. 70 2001 535 602
60. G.S. Vemuri, and F.A. McMorris Oligodendrocytes and their precursors require phosphatidylinositol 3-kinase signaling for survival Development 122 1996 2529 2537
61. Y. Wan, T. Kurosaki, and X.Y. Huang Tyrosine kinases in activation of the MAP kinase cascade by G-protein-coupled receptors Nature 380 1996 541 544
62. W.C. Watt, H. Sakano, Z.Y. Lee, J.E. Reusch, K. Trinh, and D.R. Storm Odorant stimulation enhances survival of olfactory sensory neurons via MAPK and CREB Neuron 41 2004 955 967
63. I.A. Yamboliev, K.M. Wiesmann, C.A. Singer, J.C. Hedges, and W.T. Gerthoffer Phosphatidylinositol 3-kinases regulate ERK and p38 MAP kinases in canine colonic smooth muscle Am. J. Physiol. Cell. Physiol. 279 2000 C352 C360
64. G.M. Yan, S.Z. Lin, R.P. Irwin, and S.M. Paul Activation of muscarinic cholinergic receptors blocks apoptosis of cultured cerebellar granule neurons Mol. Pharmacol. 47 1995 248 257
65. M. Zoli, A. Jansson, E. Sykova, L.F. Agnati, and K. Fuxe Volume transmission in the CNS and its relevance for neuropsychopharmacology Trends Pharmacol. Sci. 20 1999 142 150