FMRP S499 is phosphorylated independent of mTORC1-S6K1 activity

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Bartley, Christopher M ^a   O'Keefe, Rachel A ^a   Bordey, Angélique ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; P70 S6 KINASE 1; S6 KINASE; SERINE; UNCLASSIFIED DRUG; FMR1 PROTEIN, MOUSE; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; RPS6KA1 PROTEIN, MOUSE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; HETEROZYGOTE; IN VITRO STUDY; IN VIVO STUDY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; UPREGULATION; ANIMAL; GENETICS; HUMAN; METABOLISM; MORTALITY; NERVE CELL PLASTICITY; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TUBEROUS SCLEROSIS;

ANIMALS; FRAGILE X MENTAL RETARDATION PROTEIN; HUMANS; MICE; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; NEURONAL PLASTICITY; PHOSPHORYLATION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES; TUBEROUS SCLEROSIS;

EID: 84900558218     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0096956     Document Type: Article

References (51)

1. Wang H, Doering LC (2013) Reversing autism by targeting downstream mTOR signaling. Front Cell Neurosci 7: 28.
2. Feliciano DM, Hartman NW, Lin TV, Bartley C, Kubera C et al. (2013) A circuitry and biochemical basis for tuberous sclerosis symptoms: from epilepsy to neurocognitive deficits. Int J Dev Neurosci 667-678.
3. Joinson C, O'Callaghan FJ, Osborne JP, Martyn C, Harris T et al. (2003) Learning disability and epilepsy in an epidemiological sample of individuals with tuberous sclerosis complex. Psychol Med 33: 335-344. (Pubitemid 36221465)
4. O'Callaghan FJ, Harris T, Joinson C, Bolton P, Noakes M et al. (2004) The relation of infantile spasms, tubers, and intelligence in tuberous sclerosis complex. Arch Dis Child 89: 530-533.
5. Ehninger D, Han S, Shilyansky C, Zhou Y, Li W et al. (2008) Reversal of learning deficits in a Tsc2+/- mouse model of tuberous sclerosis. Nat Med 14: 843-848.
6. Auerbach BD, Osterweil EK, Bear MF (2011) Mutations causing syndromic autism define an axis of synaptic pathophysiology. Nature 480: 63-68.
7. Goorden SM, van Woerden GM, van der WL, Cheadle JP, Elgersma Y (2007) Cognitive deficits in Tsc1+/- mice in the absence of cerebral lesions and seizures. Ann Neurol 62: 648-655.
8. Potter WB, Basu T, O'Riordan KJ, Kirchner A, Rutecki P et al. (2013) Reduced juvenile long-term depression in tuberous sclerosis complex is mitigated in adults by compensatory recruitment of mGluR5 and Erk signaling. PLoS Biol 11: e1001627.
9. Chevere-Torres I, Kaphzan H, Bhattacharya A, Kang A, Maki JM et al. (2012) Metabotropic glutamate receptor-dependent long-term depression is impaired due to elevated ERK signaling in the DeltaRG mouse model of tuberous sclerosis complex. Neurobiol Dis 45: 1101-1110.
10. Brown V, Jin P, Ceman S, Darnell JC, O'donnell WT et al. (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107: 477-487. (Pubitemid 33152783)
11. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A et al. (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146: 247-261.
12. Ascano M, Jr., Mukherjee N, Bandaru P, Miller JB, Nusbaum JD et al. (2012) FMRP targets distinct mRNA sequence elements to regulate protein expression. Nature 492: 382-386.
13. Eberhart DE, Warren ST (1996) The molecular basis of fragile X syndrome. Cold Spring Harb Symp Quant Biol 61: 679-687. (Pubitemid 27258014)
14. Sharma A, Hoeffer CA, Takayasu Y, Miyawaki T, McBride SM et al. (2010) Dysregulation of mTOR signaling in fragile X syndrome. J Neurosci 30: 694-702.
15. Mazroui R, Huot ME, Tremblay S, Boilard N, Labelle Y et al. (2003) Fragile X Mental Retardation protein determinants required for its association with polyribosomal mRNPs. Hum Mol Genet 12: 3087-3096. (Pubitemid 37508881)
16. Ceman S, O'donnell WT, Reed M, Patton S, Pohl J et al. (2003) Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum Mol Genet 12: 3295-3305.
17. Narayanan U, Nalavadi V, Nakamoto M, Thomas G, Ceman S et al. (2008) S6K1 phosphorylates and regulates fragile X mental retardation protein (FMRP) with the neuronal protein synthesis-dependent mammalian target of rapamycin (mTOR) signaling cascade. J Biol Chem 283: 18478-18482.
18. Ebert DH, Greenberg ME (2013) Activity-dependent neuronal signalling and autism spectrum disorder. Nature 493: 327-337.
19. Bassell GJ, Warren ST (2008) Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60: 201-214.
20. Siomi MC, Higashijima K, Ishizuka A, Siomi H (2002) Casein kinase II phosphorylates the fragile X mental retardation protein and modulates its biological properties. Mol Cell Biol 22: 8438-8447. (Pubitemid 35397160)
21. Zhang Y, O'Connor JP, Siomi MC, Srinivasan S, Dutra A et al. (1995) The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. EMBO J 14: 5358-5366.
22. Bernard PB, Castano AM, O'Leary H, Simpson K, Browning MD et al. (2013) Phosphorylation of FMRP and alterations of FMRP complex underlie enhanced mLTD in adult rats triggered by early life seizures. Neurobiol Dis 59: 1-17.
23. Evans TL, Mihailescu MR (2010) Recombinant bacterial expression and purification of human fragile X mental retardation protein isoform 1. Protein Expr Purif 74: 242-247.
24. Brackett DM, Qing F, Amieux PS, Sellers DL, Horner PJ et al. (2013) FMR1 transcript isoforms: association with polyribosomes; regional and developmental expression in mouse brain. PLoS ONE 8: e58296.
25. Prasad S, Singh K (2008) Age- and sex-dependent differential interaction of nuclear trans-acting factors with Fmr-1 promoter in mice brain. Neurochem Res 33: 1028-1035.
26. Singh K, Prasad S (2008) Differential expression of Fmr-1 mRNA and FMRP in female mice brain during aging. Mol Biol Rep 35: 677-684.
27. Hallett PJ, Collins TL, Standaert DG, Dunah AW (2008) Biochemical fractionation of brain tissue for studies of receptor distribution and trafficking. Curr Protoc Neurosci Chapter 1: Unit.
28. Simeone A, Gulisano M, Acampora D, Stornaiuolo A, Rambaldi M et al. (1992) Two vertebrate homeobox genes related to the Drosophila empty spiracles gene are expressed in the embryonic cerebral cortex. EMBO J 11: 2541-2550.
29. Copp J, Manning G, Hunter T (2009) TORC-specific phosphorylation of mammalian target of rapamycin (mTOR): phospho-Ser2481 is a marker for intact mTOR signaling complex 2. Cancer Res 69: 1821-1827.
30. Narayanan U, Nalavadi V, Nakamoto M, Pallas DC, Ceman S et al. (2007) FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J Neurosci 27: 14349-14357.
31. Pearce LR, Alton GR, Richter DT, Kath JC, Lingardo L et al. (2010) Characterization of PF-4708671, a novel and highly specific inhibitor of p70 ribosomal S6 kinase (S6K1). Biochem J 431: 245-255.
32. Marmy-Conus N, Hannan KM, Pearson RB (2002) Ro 31-6045, the inactive analogue of the protein kinase C inhibitor Ro 31-8220, blocks in vivo activation of p70(s6k)/p85(s6k): implications for the analysis of S6K signalling. FEBS Lett 519: 135-140. (Pubitemid 34522006)
33. Nalavadi VC, Muddashetty RS, Gross C, Bassell GJ (2012) Dephosphorylation-induced ubiquitination and degradation of FMRP in dendrites: a role in immediate early mGluR-stimulated translation. J Neurosci 32: 2582-2587.
34. Feliciano DM, Su T, Lopez J, Platel JC, Bordey A (2011) Single-cell Tsc1 knockout during corticogenesis generates tuber-like lesions and reduces seizure threshold in mice. J Clin Invest 121: 1596-1607.
35. Pende M, Um SH, Mieulet V, Sticker M, Goss VL et al. (2004) S6K1(-/-)/S6K2(-/-) mice exhibit perinatal lethality and rapamycin-sensitive 5'-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol Cell Biol 24: 3112-3124. (Pubitemid 38452057)
36. Cheever A, Ceman S (2009) Phosphorylation of FMRP inhibits association with Dicer. RNA 15: 362-366.
37. Wang H, Morishita Y, Miura D, Naranjo JR, Kida S et al. (2012) Roles of CREB in the regulation of FMRP by group I metabotropic glutamate receptors in cingulate cortex. Mol Brain 5: 27.
38. Zhao W, Chuang SC, Bianchi R, Wong RK (2011) Dual regulation of fragile X mental retardation protein by group I metabotropic glutamate receptors controls translation-dependent epileptogenesis in the hippocampus. J Neurosci 31: 725-734.
39. Iliff AJ, Renoux AJ, Krans A, Usdin K, Sutton MA et al. (2013) Impaired activity-dependent FMRP translation and enhanced mGluR-dependent LTD in Fragile X premutation mice. Hum Mol Genet 22: 1180-1192.
40. Westmark CJ, Malter JS (2007) FMRP mediates mGluR5-dependent translation of amyloid precursor protein. PLoS Biol 5: e52.
41. Hou L, Antion MD, Hu D, Spencer CM, Paylor R et al. (2006) Dynamic translational and proteasomal regulation of fragile X mental retardation protein controls mGluR-dependent long-term depression. Neuron 51: 441-454. (Pubitemid 44189802)
42. Ruvinsky I, Meyuhas O (2006) Ribosomal protein S6 phosphorylation: from protein synthesis to cell size. Trends Biochem Sci 31: 342-348. (Pubitemid 43903237)
43. Meyuhas O, Dreazen A (2009) Ribosomal protein S6 kinase from TOP mRNAs to cell size. Prog Mol Biol Transl Sci 90: 109-153.
44. Hornbeck PV, Kornhauser JM, Tkachev S, Zhang B, Skrzypek E et al. (2012) PhosphoSitePlus: a comprehensive resource for investigating the structure and function of experimentally determined post-translational modifications in man and mouse. Nucleic Acids Res 40: D261-D270.
45. Coffee RL, Jr., Williamson AJ, Adkins CM, Gray MC, Page TL et al. (2012) In vivo neuronal function of the fragile X mental retardation protein is regulated by phosphorylation. Hum Mol Genet 21: 900-915.
46. Siomi MC, Higashijima K, Ishizuka A, Siomi H (2002) Casein kinase II phosphorylates the fragile X mental retardation protein and modulates its biological properties. Mol Cell Biol 22: 8438-8447. (Pubitemid 35397160)
47. Kang A, Hoeffer CA, Arnold EC, Cziko A-M, Ramaswami M et al. (2008) Casein kinase inhibitors block fragile X mental retardation protein binding with fragile X mental retardation autosomal homolog 1. Neuroscience meeting planner Washington, DC: Society for Neuroscience 38.20.
48. Villasana LE, Klann E, Tejada-Simon MV (2006) Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J Neurosci Methods 158: 30-36. (Pubitemid 44528760)
49. Maehama T, Tanaka M, Nishina H, Murakami M, Kanaho Y et al. (2008) RalA functions as an indispensable signal mediator for the nutrient-sensing system. J Biol Chem 283: 35053-35059.
50. Pasumarthi KB, Nakajima H, Nakajima HO, Jing S, Field LJ (2000) Enhanced cardiomyocyte DNA synthesis during myocardial hypertrophy in mice expressing a modified TSC2 transgene. Circ Res 86: 1069-1077. (Pubitemid 30367866)
51. Urano J, Sato T, Matsuo T, Otsubo Y, Yamamoto M et al. (2007) Point mutations in TOR confer Rheb-independent growth in fission yeast and nutrient-independent mammalian TOR signaling in mammalian cells. Proc Natl Acad Sci U S A 104: 3514-3519. (Pubitemid 46364190)