BDNF stimulation of protein synthesis in cortical neurons requires the MAP kinase-interacting kinase MNK1

Journal of Neuroscience

Volumn 35, Issue 3, 2015, Pages 972-984

  Genheden, Maja ^a   Kenney, Justin W ^a,b   Johnston, Harvey E ^a   Manousopoulou, Antigoni ^a   Garbis, Spiros D ^a   Proud, Christopher G ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

BDNF; BONCAT; CYFIP1; eIF4E; MNK; SILAC

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; BRAIN DERIVED NEUROTROPHIC FACTOR; INITIATION FACTOR 4E; MITOGEN ACTIVATED PROTEIN KINASE; SELUMETINIB; UO 126; CYFIP1 PROTEIN, MOUSE; MKNK1 PROTEIN, MOUSE; NERVE PROTEIN; PROTEIN SERINE THREONINE KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CONTROLLED STUDY; GENE REGULATORY NETWORK; IMMUNOBLOTTING; MASS SPECTROMETRY; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING; ANIMAL; BRAIN CORTEX; DRUG EFFECTS; METABOLISM; NERVE CELL; PHOSPHORYLATION; PHYSIOLOGY;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CEREBRAL CORTEX; EUKARYOTIC INITIATION FACTOR-4E; MICE; NERVE TISSUE PROTEINS; NEURONS; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 84921503014     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2641-14.2015     Document Type: Article

References (76)

1. Almeida LE, Roby CD, Krueger BK (2014) Increased BDNF expression in fetal brain in the valproic acid model of autism. Mol Cell Neurosci 59:57-62. CrossRef Medline
2. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408:297-315. CrossRef Medline
3. Banko JL, Hou L, Poulin F, Sonenberg N, Klann E (2006) Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J Neurosci 26:2167-2173. CrossRef Medline
4. Bekinschtein P, Cammarota M, Medina JH (2014) BDNF and memory processing. Neuropharmacology 76:677-683. CrossRef Medline
5. Bidinosti M, Ran I, Sanchez-Carbente MR, Martineau Y, Gingras AC, Gkogkas C, Raught B, Bramham CR, Sossin WS, Costa-Mattioli M, DesGroseillers L, Lacaille JC, Sonenberg N (2010) Postnatal deamidation of 4E-BP2 in brain enhances its association with raptor and alters kinetics of excitatory synaptic transmission. Mol Cell 37:797-808. CrossRef Medline
6. Bozdagi O, Sakurai T, Dorr N, Pilorge M, Takahashi N, Buxbaum JD (2012) Haploinsufficiency of Cyfip1 produces fragile X-like phenotypes in mice. PLoS One 7:e42422. CrossRef Medline
7. Buxadé M, Parra JL, Rousseau S, Shpiro N, Marquez R, Morrice N, Bain J, Espel E, Proud CG (2005) The Mnks are novel components in the control of TNFalpha biosynthesis and phosphorylate and regulate hnRNP A1. Immunity 23:177-189. CrossRef Medline
8. Buxadé M, Morrice N, Krebs DL, Proud CG (2008) The PSF.p54nrb complex is a novel Mnk substrate that binds the mRNA for tumor necrosis factor alpha. J Biol Chem 283:57-65. CrossRef Medline
9. Carriere A, Romeo Y, Acosta-Jaquez HA, Moreau J, Bonneil E, Thibault P, Fingar DC, Roux PP (2011) ERK1/2 phosphorylate Raptor to promote Ras-dependent activation of mTOR complex 1 (mTORC1). J Biol Chem 286:567-577. CrossRef Medline
10. Castrén ML, Castrén E (2014) BDNF in fragile X syndrome. Neuropharmacology 76:729-736. CrossRef Medline
11. Darnell JC, Klann E (2013) The translation of translational control by FMRP: therapeutic targets for FXS. Nat Neurosci 16:1530-1536. CrossRef Medline
12. Darnell JC, Van Driesche SJ, Zhang C, Hung KY, Mele A, Fraser CE, Stone EF, Chen C, Fak JJ, Chi SW, Licatalosi DD, Richter JD, Darnell RB (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146:247-261. CrossRef Medline
13. DeRubeis S, Pasciuto E, Li KW, Fernández E, Di Marino D, Buzzi A, Ostroff LE, Klann E, Zwartkruis FJ, Komiyama NH, Grant SG, Poujol C, Choquet D, Achsel T, Posthuma D, Smit AB, Bagni C (2013) CYFIP1 coordinates mRNA translation and cytoskeleton remodeling to ensure proper dendritic spine formation. Neuron 79:1169-1182. CrossRef Medline
14. Dieterich DC, Link AJ, Graumann J, Tirrell DA, Schuman EM (2006) Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc Natl Acad Sci U S A 103:9482-9487. CrossRef Medline
15. Flynn A, Proud CG (1995) Serine 209, not serine 53, is the major site of phosphorylation in initiation factor eIF-4E in serum-treated Chinese hamster ovary cells. J Biol Chem 270:21684-21688. CrossRef Medline
16. Fonseca BD, Alain T, Finestone LK, Huang BP, Rolfe M, Jiang T, Yao Z, Hernandez G, Bennett CF, Proud CG (2011) Pharmacological and genetic evaluation of proposed roles of mitogen-activated protein kinase/ extracellular signal-regulated kinase kinase (MEK), extracellular signalregulated kinase (ERK), and p90RSK in the control of mTORC1 protein signaling by phorbol esters. J Biol Chem 286:27111-27122. CrossRef Medline
17. Franceschini A, Szklarczyk D, Frankild S, Kuhn M, Simonovic M, Roth A, Lin J, Minguez P, Bork P, von Mering C, Jensen LJ (2013) STRING v9.1: protein-protein interaction networks, with increased coverage and integration. Nucleic Acid Res 41:D808-D815. CrossRef Medline
18. Fukunaga R, Hunter T (1997) Mnk1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J 16:1921-1933. CrossRef Medline
19. Furic L, Rong L, Larsson O, Koumakpayi IH, Yoshida K, Brueschke A, Petroulakis E, Robichaud N, Pollak M, Gaboury LA, Pandolfi PP, Saad F, Sonenberg N (2010) eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc Natl Acad Sci U S A 107:14134-14139. CrossRef Medline
20. Gingras AC, Raught B, Sonenberg N (1999) eIF4 translation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68:913-963. CrossRef Medline
21. Gkogkas CG, Khoutorsky A, Ran I, Rampakakis E, Nevarko T, Weatherill DB, Vasuta C, Yee S, Truitt M, Dallaire P, Major F, Lasko P, Ruggero D, Nader K, Lacaille JC, Sonenberg N (2013) Autism-related deficits via dysregulated eIF4E-dependent translational control. Nature 493:371-377. CrossRef Medline
22. Howden AJ, Geoghegan V, Katsch K, Efstathiou G, Bhushan B, Boutureira O, Thomas B, Trudgian DC, Kessler BM, Dieterich DC, Davis BG, Acuto O (2013) QuaNCAT: quantitating proteome dynamics in primary cells. Nat Methods 10:343-346. CrossRef Medline
23. Huang da W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4:44-57. CrossRef Medline
24. Huo Y, Iadevaia V, Yao Z, Kelly I, Cosulich S, Guichard S, Foster LJ, Proud CG (2012) Stable isotope-labelling analysis of the impact of inhibition of the mammalian target of rapamycin on protein synthesis. Biochem J 444: 141-151. CrossRef Medline
25. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS (2009) Genomewide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science 324:218-223. CrossRef Medline
26. Joshi S, Platanias LC (2014) Mnk kinase pathway: cellular functions and biological outcomes. World J Biol Chem 5:321-333. CrossRef Medline
27. Kalkman HO (2012) Potential opposite roles of the extracellular signalregulated kinase (ERK) pathway in autism spectrum and bipolar disorders. Neurosci Biobehav Rev 36:2206-2213. CrossRef Medline
28. Kang H, Schuman EM (1995) Long-lasting neurotrophin-induced enhancement of synaptic transmission in the adult hippocampus. Science 267:1658-1662. CrossRef Medline
29. Kanhema T, Dagestad G, Panja D, Tiron A, Messaoudi E, Håvik B, Ying SW, Nairn AC, Sonenberg N, Bramham CR (2006) Dual regulation of translation initiation and peptide chain elongation during BDNF-induced LTP in vivo: evidence for compartment-specific translation control. J Neurochem 99:1328-1337. CrossRef Medline
30. Karpova NN (2014) Role of BDNF epigenetics in activity-dependent neuronal plasticity. Neuropharmacology 76:709-718. CrossRef Medline
31. Kelleher RJ 3rd, Govindarajan A, Jung HY, Kang H, Tonegawa S (2004) Translational control by MAPK signaling in long-term synaptic plasticity and memory. Cell 116:467-479. CrossRef Medline
32. Kelleher RJ 3rd, Bear MF (2008) The autistic neuron: troubled translation? Cell 135:401-406. CrossRef Medline
33. Leal G, Comprido D, Duarte CB (2014) BDNF-induced local protein synthesis and synaptic plasticity. Neuropharmacology 76:639-656. CrossRef Medline
34. Liao L, Pilotte J, Xu T, Wong CC, Edelman GM, Vanderklish P, Yates JR 3rd (2007) BDNF induces widespread changes in synaptic protein content and up-regulates components of the translation machinery: an analysis using high-throughput proteomics. J Proteome Res 6:1059-1071. CrossRef Medline
35. Li YX, Zhang Y, Lester HA, Schuman EM, Davidson N (1998) Enhancement of neurotransmitter release induced by brain-derived neurotrophic factor in cultured hippocampal neurons. J Neurosci 18:10231-10240. Medline
36. Liu-Yesucevitz L, Bassell GJ, Gitler AD, Hart AC, Klann E, Richter JD, Warren ST, Wolozin B (2011) Local RNA translation at the synapse and in disease. J Neurosci 31:16086-16093. CrossRef Medline
37. Ma L, Chen Z, Erdjument-Bromage H, Tempst P, Pandolfi PP (2005) Phosphorylation and functional inactivation of TSC2 by Erk implications for tuberous sclerosis and cancer pathogenesis. Cell 121:179-193. CrossRef Medline
38. Manadas B, Santos AR, Szabadfi K, Gomes JR, Garbis SD, Fountoulakis M, Duarte CB (2009) BDNF-induced changes in the expression of the translation machinery in hippocampal neurons: protein levels and dendritic mRNA. J Proteome Res 8:4536-4552. CrossRef Medline
39. Napoli I, Mercaldo V, Boyl PP, Eleuteri B, Zalfa F, De Rubeis S, Di Marino D, Mohr E, Massimi M, Falconi M, Witke W, Costa-Mattioli M, Sonenberg N, Achsel T, Bagni C (2008) The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134: 1042-1054. CrossRef Medline
40. Narayanan U, Nalavadi V, Nakamoto M, Pallas DC, Ceman S, Bassell GJ, Warren ST (2007) FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J Neurosci 27:14349-14357. CrossRef Medline
41. Narayanan U, Nalavadi V, Nakamoto M, Thomas G, Ceman S, Bassell GJ, Warren ST (2008) S6K1 phosphorylates and regulates fragile X mental retardation protein (FMRP) with the neuronal protein synthesisdependent mammalian target of rapamycin (mTOR) signaling cascade. J Biol Chem 283:18478-18482. CrossRef Medline
42. Nelson KB, Grether JK, Croen LA, Dambrosia JM, Dickens BF, Jelliffe LL, Hansen RL, Phillips TM (2001) Neuropeptides and neurotrophins in neonatal blood of children with autism or mental retardation. Ann Neurol 49:597-606. CrossRef Medline
43. Neves-Pereira M, Müller B, Massie D, Williams JH, O'Brien PC, Hughes A, Shen SB, St CD, Miedzybrodzka Z (2009) Deregulation of EIF4E: a novel mechanism for autism. J Med Genet 46:759-765. CrossRef Medline
44. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, Pandey A, Mann M (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1:376-386. CrossRef Medline
45. Panja D, Bramham CR (2014) BDNF mechanisms in late LTP formation: a synthesis and breakdown. Neuropharmacology 76:664-676. CrossRef Medline
46. Panja D, Dagyte G, Bidinosti M, Wibrand K, Kristiansen AM, Sonenberg N, Bramham CR (2009) Novel translational control in Arc-dependent long term potentiation consolidation in vivo. J Biol Chem 284:31498-31511. CrossRef Medline
47. Panja D, Kenney JW, D'Andrea L, Zalfa F, Vedeler A, Wibrand K, Fukunaga R, Bagni C, Proud CG, Bramham CR (2014) Two-stage translational control of dentate gyrus LTP consolidation mediated by sustained BDNFTrkB signaling to MNK. Cell Rep 9:1430-1445. CrossRef Medline
48. Pathania M, Davenport EC, Muir J, Sheehan DF, López-Doménech G, Kittler JT (2014) The autism and schizophrenia associated gene CYFIP1 is critical for the maintenance of dendritic complexity and the stabilization of mature spines. Transl Psychiatry 4:e374. CrossRef Medline
49. Pop AS, Gomez-Mancilla B, Neri G, Willemsen R, Gasparini F (2014) Fragile X syndrome: a preclinical review on metabotropic glutamate receptor 5 (mGluR5) antagonists and drug development. Psychopharmacology (Berl) 231:1217-1226. CrossRef Medline
50. Santini E, Huynh TN, MacAskill AF, Carter AG, Pierre P, Ruggero D, Kaphzan H, Klann E (2013) Exaggerated translation causes synaptic and behavioural aberrations associated with autism. Nature 493:411-415. CrossRef Medline
51. Scheper GC, Morrice NA, Kleijn M, Proud CG (2001) The MAP kinase signal-integrating kinase Mnk2 is an eIF4E kinase with high basal activity in mammalian cells. Mol Cell Biol 21:743-754. CrossRef Medline
52. Schratt GM, Nigh EA, Chen WG, Hu L, Greenberg ME (2004) BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development. J Neurosci 24:7366-7377. CrossRef Medline
53. Schwanhäusser B, Busse D, Li N, Dittmar G, Schuchhardt J, Wolf J, Chen W, Selbach M (2011) Global quantification of mammalian gene expression control. Nature 473:337-342. CrossRef Medline
54. Seese RR, Maske AR, Lynch G, Gall CM (2014) Long-term memory deficits are associated with elevated synaptic ERK1/2 activation and reversed by mGluR5 antagonism in an animal model of autism. Neuropsychopharmacology 39:1664-1673. CrossRef Medline
55. Silverman JL, Smith DG, Rizzo SJ, Karras MN, Turner SM, Tolu SS, Bryce DK, Smith DL, Fonseca K, Ring RH, Crawley JN (2012) Negative allosteric modulation of the mGluR5 receptor reduces repetitive behaviors and rescues social deficits in mouse models of autism. Sci Transl Med 4:131ra51. CrossRef Medline
56. Somasekharan SP, Stoynov N, Rotblat B, Leprivier G, Galpin JD, Ahern CA, Foster LJ, Sorensen PH (2012) Identification and quantification of newly synthesized proteins translationally regulated by YB-1 using a novel click-SILAC approach. J Proteomics 77:e1-10. CrossRef Medline
57. Spellman DS, Deinhardt K, Darie CC, Chao MV, Neubert TA (2008) Stable isotopic labeling by amino acids in cultured primary neurons: application to brain-derived neurotrophic factor-dependent phosphotyrosineassociated signaling. Mol Cell Proteomics 7:1067-1076. CrossRef Medline
58. Stead RL, Proud CG (2013) Rapamycin enhances eIF4E phosphorylation by activating MAP kinase-interacting kinase 2a (Mnk2a). FEBS Lett 587: 2623-2628. CrossRef Medline
59. Takei N, Sasaoka K, Inoue K, Takahashi M, Endo Y, Hatanaka H (1997) Brain-derived neurotrophic factor increases the stimulation-evoked release of glutamate and the levels of exocytosis-associated proteins in cultured cortical neurons from embryonic rats. J Neurochem 68:370-375. CrossRef Medline
60. Takei N, Kawamura M, Hara K, Yonezawa K, Nawa H (2001) Brain-derived neurotrophic factor enhances neuronal translation by activating multiple initiation processes: comparison with the effects of insulin. J Biol Chem 276:42818-42825. CrossRef Medline
61. Takei N, Inamura N, Kawamura M, Namba H, Hara K, Yonezawa K, Nawa H (2004) Brain-derived neurotrophic factor induces mammalian target of rapamycin-dependent local activation of translation machinery and protein synthesis in neuronal dendrites. J Neurosci 24:9760-9769. CrossRef Medline
62. Takei N, Kawamura M, Ishizuka Y, Kakiya N, Inamura N, Namba H, Nawa H (2009) Brain-derived neurotrophic factor enhances the basal rate of protein synthesis by increasing active eukaryotic elongation factor 2 levels and promoting translation elongation in cortical neurons. J Biol Chem 284:26340-26348. CrossRef Medline
63. Taurines R, Segura M, Schecklmann M, Albantakis L, Grünblatt E, Walitza S, Jans T, Lyttwin B, Haberhausen M, Theisen FM, Martin B, Briegel W, Thome J, Schwenck C, Romanos M, Gerlach M (2014) Altered peripheral BDNF mRNA expression and BDNF protein concentrations in blood of children and adolescents with autism spectrum disorder. J Neural Transm 121:1117-1128. CrossRef Medline
64. Tschopp C, Knauf U, Brauchle M, Zurini M, Ramage P, Glueck D, New L, Han J, Gram H (2000) Phosphorylation of eIF-4E on Ser 209 in response to mitogenic and inflammatory stimuli is faithfully detected by specific antibodies. Mol Cell Biol Res Commun 3:205-211. CrossRef Medline
65. Ueda T, Watanabe-Fukunaga R, Fukuyama H, Nagata S, Fukunaga R (2004) Mnk2 and Mnk1 are essential for constitutive and inducible phosphorylation of eukaryotic initiation factor 4E but not for cell growth or development. Mol Cell Biol 24:6539-6549. CrossRef Medline
66. Ueda T, Sasaki M, Elia AJ, Chio II, Hamada K, Fukunaga R, Mak TW (2010) Combined deficiency for MAP kinase-interacting kinase 1 and 2 (Mnk1 and Mnk2) delays tumor development. Proc Natl Acad Sci U S A 107: 13984-13990. CrossRef Medline
67. Vizcaíno JA, Côté RG, Csordas A, Dianes JA, Fabregat A, Foster JM, Griss J, Alpi E, Birim M, Contell J, O'Kelly G, Schoenegger A, Ovelleiro D, Pérez-Riverol Y, Reisinger F, Ríos D, Wang R, Hermjakob H (2013) The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013. Nucleic Acids Res 41:D1063-D1069. CrossRef Medline
68. Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Ríos D, Dianes JA, Sun Z, Farrah T, Bandeira N, Binz PA, Xenarios I, Eisenacher M, Mayer G, Gatto L, Campos A, Chalkley RJ, Kraus HJ, Albar JP, Martinez-Bartolomé S, et al. (2014) Proteome Xchange provides globally coordinated proteomics data submission and dissemination. Nat Biotechnol 32:223-226. CrossRef Medline
69. Wang X, Yue P, Chan CB, Ye K, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Fu H, Khuri FR, Sun SY (2007) Inhibition of mammalian target of rapamycin induces phosphatidylinositol 3-kinase-dependent and Mnkmediated eukaryotic translation initiation factor 4E phosphorylation. Mol Cell Biol 27:7405-7413. CrossRef Medline
70. Waskiewicz AJ, Flynn A, Proud CG, Cooper JA (1997) Mitogen-activated kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J 16:1909-1920. CrossRef Medline
71. Waskiewicz AJ, Johnson JC, Penn B, Mahalingam M, Kimball SR, Cooper JA (1999) Phosphorylation of the cap-binding protein eukaryotic translation factor 4E by protein kinase Mnk1 in vivo. Mol Cell Biol 19:1871-1880. Medline
72. Wendel HG, Silva RL, Malina A, Mills JR, Zhu H, Ueda T, Watanabe-Fukunaga R, Fukunaga R, Teruya-Feldstein J, Pelletier J, Lowe SW (2007) Dissecting eIF4E action in tumorigenesis. Genes Dev 21:3232-3237. CrossRef Medline
73. Wong HK, Fricker M, Wyttenbach A, Villunger A, Michalak EM, Strasser A, Tolkovsky AM (2005) Mutually exclusive subsets of BH3-only proteins are activated by the p53 and c-Jun N-terminal kinase/c-Jun signaling pathways during cortical neuron apoptosis induced by arsenite. Mol Cell Biol 25:8732-8747. CrossRef Medline
74. Yang K, Cao F, Sheikh AM, Malik M, Wen G, Wei H, Ted Brown W, Li X (2013) Up-regulation of Ras/Raf/ERK1/2 signaling impairs cultured neuronal cell migration, neurogenesis, synapse formation, and dendritic spine development. Brain Struct Funct 218:669-682. CrossRef Medline
75. Yeh TC, Marsh V, Bernat BA, Ballard J, Colwell H, Evans RJ, Parry J, Smith D, Brandhuber BJ, Gross S, Marlow A, Hurley B, Lyssikatos J, Lee PA, Winkler JD, Koch K, Wallace E (2007) Biological characterization of ARRY-142886 (AZD6244), a potent, highly selective mitogen-activated protein kinase kinase 1/2 inhibitor. Clin Cancer Res 13:1576-1583. CrossRef Medline
76. Yin A, Qiu Y, Jia B, Song T, Yu Y, Alberts I, Zhong M (2014) The developmental pattern of the RAS/RAF/Erk1/2 pathway in the BTBR autism mouse model. Int J Dev Neurosci 39:2-8. CrossRef Medline