FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A

Journal of Neuroscience

Volumn 27, Issue 52, 2007, Pages 14349-14357

  Narayanan, Usha ^a   Nalavadi, Vijayalaxmi ^a   Nakamoto, Mika ^a   Pallas, David C ^a   Ceman, Stephanie ^b   Bassell, Gary J ^a   Warren, Stephen T ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

FMRP; Fragile X; mGluR; Phosphorylation; PP2A; Synaptic plasticity

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; METABOTROPIC RECEPTOR; PHOSPHOPROTEIN PHOSPHATASE 2A;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; FRAGILE X SYNDROME; HIPPOCAMPUS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; EMBRYO, MAMMALIAN; ENZYME ACTIVATION; EXCITATORY AMINO ACID AGENTS; FRAGILE X MENTAL RETARDATION PROTEIN; HIPPOCAMPUS; IMMUNOPRECIPITATION; METHOXYHYDROXYPHENYLGLYCOL; MUTATION; NEURONS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; PYRIDINES; RATS; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 37549044298     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2969-07.2007     Document Type: Article

References (44)

1. Adams DG, Coffee Jr RL, Zhang H, Pelech S, Strack S, Wadzinski BE (2005) Positive regulation of Raf1-MEK1/2-ERK1/2 signaling by protein serine/threonine phosphatase 2A holoenzymes. J Biol Chem 280:42644-42654.
2. Antar LN, Afroz R, Dictenberg JB, Carroll RC, Bassell GJ (2004) Metabotropic glutamate receptor activation regulates fragile x mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J Neurosci 24:2648-2655.
3. Bear MF, Huber KM, Warren ST (2004) The mGluR theory of fragile X mental retardation. Trends Neurosci 27:370-377.
4. Bottorff D, Stang S, Agellon S, Stone JC (1995) RAS signalling is abnormal in a c-raf1 MEK1 double mutant. Mol Cell Biol 15:5113-5122.
5. Brown V, Small K, Lakkis L, Feng Y, Gunter C, Wilkinson KD, Warren ST (1998) Purified recombinant Fmrp exhibits selective RNA binding as an intrinsic property of the fragile X mental retardation protein. J Biol Chem 273:15521-15527.
6. Brown V, Jin P, Ceman S, Darnell JC, O'Donnell WT, Tenenbaum SA, Jin X, Feng Y, Wilkinson KD, Keene JD, Darnell RB, Warren ST (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107:477-487.
7. Ceman S, O'Donnell WT, Reed M, Patton S, Pohl J, Warren ST (2003) Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum Mol Genet 12:3295-3305.
8. Corbin F, Bouillon M, Fortin A, Morin S, Rousseau F, Khandjian EW (1997) The fragile X mental retardation protein is associated with poly(A)(+) mRNA in actively translating polyribosomes. Hum Mol Genet 6:1465-1472.
9. Darnell JC, Jensen KB, Jin P, Brown V, Warren ST, Darnell RB (2001) Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107:489-499.
10. Daw MI, Bortolotto ZA, Saulle E, Zaman S, Collingridge GL, Isaac JT (2002) Phosphatidylinositol 3 kinase regulates synapse specificity of hippocampal long-term depression. Nat Neurosci 5:835-836.
11. Denman RB (2002) Methylation of the arginine-glycine-rich region in the fragile X mental retardation protein FMRP differentially affects RNA binding. Cell Mol Biol Lett 7:877-883.
12. Dounay AB, Forsyth CJ (2002) Okadaic acid: the archetypal serine/threonine protein phosphatase inhibitor. Curr Med Chem 9:1939-1980.
13. Evans DR, Myles T, Hofsteenge J, Hemmings BA (1999) Functional expression of human PP2Ac in yeast permits the identification of novel C-terminal and dominant-negative mutant forms. J Biol Chem 274:24038-24046.
14. Feng Y, Gutekunst CA, Eberhart DE, Yi H, Warren ST, Hersch SM (1997a) Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J Neurosci 17:1539-1547.
15. Feng Y, Absher D, Eberhart DE, Brown V, Malter HE, Warren ST (1997b) FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol Cell 1:109-118.
16. Honkanen RE, Zwiller J, Moore RE, Daily SL, Khatra BS, Dukelow M, Boynton AL (1990) Characterization of microcystin-LR, a potent inhibitor of type 1 and type 2A protein phosphatases. J Biol Chem 265:19401-19404.
17. Kindler S, Mohr E, Rehbein M, Richter D (2001) Extrasomatic targeting of MAP2, vasopressin and oxytocin mRNAs in mammalian neurons. Results Probl Cell Differ 34:83-104.
18. Kins S, Crameri A, Evans DR, Hemmings BA, Nitsch RM, Gotz J (2001) Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J Biol Chem 276:38193-38200.
19. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U (2001) Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet 10:329-338.
20. Lechward K, Awotunde OS, Swiatek W, Muszynska G (2001) Protein phosphatase 2A: variety of forms and diversity of functions. Acta Biochim Pol 48:921-933.
21. Lu R, Wang H, Liang Z, Ku L, O'Donnell WT, Li W, Warren ST, Feng Y (2004) The fragile X protein controls microtubule-associated protein 1B translation and microtubule stability in brain neuron development. Proc Natl Acad Sci USA 101:15201-15206.
22. Maher P, Davis JB (1996) The role of monoamine metabolism in oxidative glutamate toxicity. J Neurosci 16:6394-6401.
23. Mao L, Yang L, Arora A, Choe ES, Zhang G, Liu Z, Fibuch EE, Wang JQ (2005) Role of protein phosphatase 2A in mGluR5-regulated MEK/ERK phosphorylation in neurons. J Biol Chem 280:12602-12610.
24. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y, Khandjian EW (2002) Trapping of messenger RNA by Fragile X mental retardation protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11:3007-3017.
25. McBride SM, Choi CH, Wang Y, Liebelt D, Braunstein E, Ferreiro D, Sehgal A, Siwicki KK, Dockendorff TC, Nguyen HT, McDonald TV, Jongens TA (2005) Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome. Neuron 45:753-764.
26. Morimoto BH, Koshland Jr DE (1990) Excitatory amino acid uptake and N-methyl-D-aspartate-mediated secretion in a neural cell line. Proc Natl Acad Sci USA 87:3518-3521.
27. Muddashetty RS, Kelic S, Gross C, Xu M, Bassell GJ (2007) Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J Neurosci 27:5338-5348.
28. Namboodiripad AN, Jennings ML (1996) Permeability characteristics of erythrocyte membrane to okadaic acid and calyculin A. Am J Physiol 270:C449-C456.
29. Nosyreva ED, Huber KM (2006) Metabotropic receptor-dependent long-term depression persists in the absence of protein synthesis in the mouse model of fragile X syndrome. J Neurophysiol 95:3291-3295.
30. Peterson RT, Desai BN, Hardwick JS, Schreiber SL (1999) Protein phosphatase 2A interacts with the 70-kDa S6 kinase and is activated by inhibition of FKBP12-rapamycinassociated protein. Proc Natl Acad Sci USA 96:4438-4442.
31. Raymond CR, Thompson VL, Tate WP, Abraham WC (2000) Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J Neurosci 20:969-976.
32. Routtenberg A, Rekart JL (2005) Post-translational protein modification as the substrate for long-lasting memory. Trends Neurosci 28:12-19.
33. Sagara Y, Schubert D (1998) The activation of metabotropic glutamate receptors protects nerve cells from oxidative stress. J Neurosci 18:6662-6671.
34. Schaeffer C, Bardoni B, Mandel JL, Ehresmann B, Ehresmann C, Moine H (2001) The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J 20:4803-4813.
35. Stefani G, Fraser CE, Darnell JC, Darnell RB (2004) Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J Neurosci 24:7272-7276.
36. Stetler A, Winograd C, Sayegh J, Cheever A, Patton E, Zhang X, Clarke S, Ceman S (2006) Identification and characterization of the methyl arginines in the fragile X mental retardation protein Fmrp. Hum Mol Genet 15:87-96.
37. Thelin WR, Kesimer M, Tarran R, Kreda SM, Grubb BR, Sheehan JK, Stutts MJ, Milgram SL (2005) The cystic fibrosis transmembrane conductance regulator is regulated by a direct interaction with the protein phosphatase 2A. J Biol Chem 280:41512-41520.
38. Todd PK, Mack KJ, Malter JS (2003) The fragile X mental retardation protein is required for type-I metabotropic glutamate receptor-dependent translation of PSD-95. Proc Natl Acad Sci USA 100:14374-14378.
39. Vanderklish PW, Edelman GM (2002) Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc Natl Acad Sci USA 99:1639-1644.
40. Van Kanegan MJ, Adams DG, Wadzinski BE, Strack S (2005) Distinct protein phosphatase 2A heterotrimers modulate growth factor signaling to extracellular signal-regulated kinases and Akt. J Biol Chem 280:36029-36036.
41. Weiler IJ, Spangler CC, Klintsova AY, Grossman AW, Kim SH, Bertaina-Anglade V, Khaliq H, de Vries FE, Lambers FA, Hatia F, Base CK, Greenough WT (2004) Fragile X mental retardation protein is necessary for neurotransmitter-activated protein translation at synapses. Proc Natl Acad Sci USA 101:17504-17509.
42. Winder DG, Sweatt JD (2001) Roles of serine/threonine phosphatases in hippocampal synaptic plasticity. Nat Rev Neurosci 2:461-474.
43. Yan QJ, Rammal M, Tranfaglia M, Bauchwitz RP (2005) Suppression of two major fragile X syndrome mouse model phenotypes by the mGluR5 antagonist MPEP. Neuropharmacology 49:1053-1066.
44. Zhang YQ, Bailey AM, Matthies HJ, Renden RB, Smith MA, Speese SD, Rubin GM, Broadie K (2001) Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107:591-603.