Tuning Specific Translation in Cancer Metastasis and Synaptic Memory: Control at the MNK–eIF4E Axis

Trends in Biochemical Sciences

Volumn 41, Issue 10, 2016, Pages 847-858

  Bramham, Clive R ^a   Jensen, Kirk B ^b,c   Proud, Christopher G ^b,c  

^a UNIVERSITY OF BERGEN   (Norway)

^b SOUTH AUSTRALIAN HEALTH AND MEDICAL RESEARCH INSTITUTE   (Australia)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Autism spectrum disorders.; cytoplasmic fragile X mental retardation protein; epithelial mesenchymal transition; long term synaptic plasticity; MAP kinase interacting kinase; protein synthesis

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; INITIATION FACTOR 4E; ISOPROTEIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE INTERACTING KINASE; TRANSCRIPTOME; UNCLASSIFIED DRUG; CAPPED RNA; CYFIP1 PROTEIN, HUMAN; PROTEIN BINDING; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AUTISM; BRAIN NERVE CELL; CANCER CELL; CYTOLOGY; CYTOSKELETON; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; FRAGILE X SYNDROME; GENE CONTROL; GENE EXPRESSION REGULATION; HIPPOCAMPUS; HUMAN; LONG TERM POTENTIATION; MEMORY; METASTASIS; NERVE CELL PLASTICITY; NEUROBIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN STRUCTURE; PROTEIN TARGETING; REVIEW; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; GENETICS; METABOLISM; NEOPLASM; PATHOLOGY; PHOSPHORYLATION; PROTEIN SYNTHESIS; SYNAPSE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; EUKARYOTIC INITIATION FACTOR-4E; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; NEURONAL PLASTICITY; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA CAPS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84991696071     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2016.07.008     Document Type: Review

References (90)

1. 1 Schwanhäusser, B., et al. Global quantification of mammalian gene expression control. Nature 473 (2011), 337–342.
2. 2 Bramham, C.R., Wells, D.G., Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 8 (2007), 776–789.
3. 3 Jung, H., et al. Remote control of gene function by local translation. Cell 157 (2014), 26–40.
4. 4 Truitt, M.L., et al. Differential requirements for eIF4E dose in normal development and cancer. Cell 162 (2015), 59–71.
5. 5 Gkogkas, C.G., Sonenberg, N., Translational control and autism-like behaviors. Cell. Logist., 3, 2013, e24551.
6. 6 Waltes, R., et al. Common EIF4E variants modulate risk for autism spectrum disorders in the high-functioning range. J. Neural Transm. 121 (2014), 1107–1116.
7. 7 Curatolo, P., et al. Neurological and neuropsychiatric aspects of tuberous sclerosis complex. Lancet Neurol. 14 (2015), 733–745.
8. 8 Proud, C.G., Mnks, eIF4E phosphorylation and cancer. Biochim. Biophys. Acta - Gene Regul. Mech. 1849 (2015), 766–773.
9. 9 Buxade, M., et al. The Mnks: MAP kinase-interacting kinases (MAP kinase signal-integrating kinases). Front. Biosci. 13 (2008), 5359–5373.
10. 10 Flynn, A., Proud, C.G., 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 (1995), 21684–21688.
11. 11 Ueda, T., et al. 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 (2004), 6539–6549.
12. 12 Fukunaga, R., Hunter, T., MNK1, a new MAP kinase-activated protein kinase, isolated by a novel expression screening method for identifying protein kinase substrates. EMBO J. 16 (1997), 1921–1933.
13. 13 Waskiewicz, A.J., et al. Mitogen-activated protein kinases activate the serine/threonine kinases Mnk1 and Mnk2. EMBO J. 16 (1997), 1909–1920.
14. 14 Cargnello, M., Roux, P.P., Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75 (2011), 50–83.
15. 15 Joshi, S., Mnk kinase pathway: cellular functions and biological outcomes. World J. Biol. Chem., 5, 2014, 321.
16. 16 Parra-Palau, J.L., et al. Features in the N and C termini of the MAPK-interacting kinase Mnk1 mediate its nucleocytoplasmic shuttling. J. Biol. Chem. 278 (2003), 44197–44204.
17. 17 Marcotrigiano, J., et al. Cocrystal structure of the messenger RNA 5’ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Nucleic Acids Symp. Ser. 89 (1997), 8–11.
18. 18 Scheper, G.C., et al. Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J. Biol. Chem. 277 (2002), 3303–3309.
19. 19 Scheper, G.C., et al. The N and C termini of the splice variants of the human mitogen-activated protein kinase-interacting kinase Mnk2 determine activity and localization. Mol. Cell. Biol. 23 (2003), 5692–5705.
20. 20 Pyronnet, S., et al. Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. EMBO J. 18 (1999), 270–279.
21. 21 Shveygert, M., et al. Regulation of eukaryotic initiation factor 4E (eIF4E) phosphorylation by mitogen-activated protein kinase occurs through modulation of Mnk1-eIF4G interaction. Mol. Cell Biol. 30 (2010), 5160–5167.
22. 22 Ueda, T., et al. Combined deficiency for MAP kinase-interacting kinase 1 and 2 (Mnk1 and Mnk2) delays tumor development. Proc. Natl. Acad. Sci. U.S.A. 107 (2010), 13984–13990.
23. 23 Furic, L., et al. eIF4E phosphorylation promotes tumorigenesis and is associated with prostate cancer progression. Proc. Natl. Acad. Sci. U.S.A. 107 (2010), 14134–14139.
24. 24 Tschopp, C., et al. 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 (2000), 205–211.
25. 25 Bain, J., et al. The selectivity of protein kinase inhibitors: a further update. Biochem. J. 408 (2007), 297–315.
26. 26 Konicek, B.W., et al. Therapeutic inhibition of MAP kinase interacting kinase blocks eukaryotic initiation factor 4E phosphorylation and suppresses outgrowth of experimental lung metastases. Cancer Res. 71 (2011), 1849–1857.
27. 27 Beggs, J.E., et al. The MAP kinase-interacting kinases regulate cell migration, vimentin expression and eIF4E/CYFIP1 binding. Biochem. J. 467 (2015), 63–76.
28. 28 Landon, A.L., et al. MNKs act as a regulatory switch for eIF4E1 and eIF4E3 driven mRNA translation in DLBCL. Nat. Commun., 5, 2014, 5413.
29. 29 Genheden, M., et al. BDNF stimulation of protein synthesis in cortical neurons requires the MAP kinase-interacting kinase MNK1. J. Neurosci. 35 (2015), 972–984.
30. 30 Bramham, C.R., Messaoudi, E., BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog. Neurobiol. 76 (2005), 99–125.
31. 31 Park, H., Poo, M.-M., Neurotrophin regulation of neural circuit development and function. Nat. Rev. Neurosci. 14 (2013), 7–23.
32. 32 Napoli, I., et al. The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134 (2008), 1042–1054.
33. 33 Di Marino, D., et al. A unique binding mode of the eukaryotic translation initiation factor 4E for guiding the design of novel peptide inhibitors. Protein Sci. 24 (2015), 1370–1382.
34. 34 Richter, J.D., et al. Dysregulation and restoration of translational homeostasis in fragile X syndrome. Nat. Rev. Neurosci. 16 (2015), 595–605.
35. 35 Chen, E., et al. Fragile X mental retardation protein regulates translation by binding directly to the ribosome. Mol. Cell 54 (2014), 407–417.
36. 36 Darnell, J.C., et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell. 146 (2011), 247–261.
37. 37 Panja, D., et al. Two-stage translational control of dentate gyrus LTP consolidation is mediated by sustained BDNF-TrkB signaling to MNK. Cell Rep. 9 (2014), 1430–1445.
38. 38 Panja, D., et al. Novel translational control in Arc-dependent long term potentiation consolidation in vivo. J. Biol. Chem. 284 (2009), 31498–31511.
39. 39 Panja, D., Bramham, C.R., BDNF mechanisms in late LTP formation: a synthesis and breakdown. Neuropharmacology 76 (2014), 664–676.
40. 40 Costa-Mattioli, M., et al. Translational control of long-lasting synaptic plasticity and memory. Neuron 61 (2009), 10–26.
41. 41 Huber, K.M., et al. Dysregulation of mammalian target of rapamycin signaling in mouse models of autism. J. Neurosci. 35 (2015), 13836–13842.
42. 42 Gelinas, J.N., et al. ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation. J. Biol. Chem. 282 (2007), 27527–27535.
43. 43 Banko, J.L., et al. Regulation of eukaryotic initiation factor 4E by converging signaling pathways during metabotropic glutamate receptor-dependent long-term depression. J. Neurosci. 26 (2006), 2167–2173.
44. 44 Gkogkas, C.G., et al. Pharmacogenetic inhibition of eIF4E-dependent Mmp9 mRNA translation reverses fragile X syndrome-like phenotypes. Cell Rep. 9 (2014), 1–14.
45. 45 Lucá, R., et al. The Fragile X Protein binds mRNAs involved in cancer progression and modulates metastasis formation. EMBO Mol. Med. 5 (2013), 1523–1536.
46. 46 Robichaud, N., et al. Phosphorylation of eIF4E promotes EMT and metastasis via translational control of SNAIL and MMP-3. Oncogene 34 (2014), 1–11.
47. 47 Zheng, J., et al. Phosphorylated Mnk1 and eIF4E are associated with lymph node metastasis and poor prognosis of nasopharyngeal carcinoma. PLoS ONE, 9, 2014, e89220.
48. 48 Carter, J.H., et al. Phosphorylation of eIF4E serine 209 is associated with tumour progression and reduced survival in malignant melanoma. Br. J. Cancer 114 (2016), 444–453.
49. 49 Ramalingam, S., et al. First MNKs degrading agents block phosphorylation of eIF4E, induce apoptosis, inhibit cell growth, migration and invasion in triple negative and Her2-overexpressing breast cancer cell lines. Oncotarget 2 (2014), 20–30.
50. 50 Diab, S., et al. MAP kinase-interacting kinases-emerging targets against cancer. Chem. Biol. 21 (2014), 441–452.
51. 51 Bhat, M., et al. Targeting the translation machinery in cancer. Nat. Rev. Drug Discov. 14 (2015), 261–278.
52. 52 Shi, Y., et al. MNK kinases facilitate c-myc IRES activity in rapamycin-treated multiple myeloma cells. Oncogene 32 (2013), 190–197.
53. 53 Buxade, M., et al. The PSF-p54nrb complex is a novel Mnk substrate that binds the mRNA for tumor necrosis factor α. J. Biol. Chem. 283 (2008), 57–65.
54. 54 Buxadé, M., et al. The Mnks are novel components in the control of TNFα biosynthesis and phosphorylate and regulate hnRNP A1. Immunity 23 (2005), 177–189.
55. 55 DaSilva, J., et al. Regulation of sprouty stability by Mnk1-dependent phosphorylation. Mol. Cell. Biol. 26 (2006), 1898–1907.
56. 56 Edwin, F., et al. HECT domain-containing E3 ubiquitin ligase Nedd4 interacts with and ubiquitinates sprouty2. J. Biol. Chem. 285 (2010), 255–264.
57. 57 Stead, R.L., Proud, C.G., Rapamycin enhances eIF4E phosphorylation by activating MAP kinase-interacting kinase 2a (Mnk2a). FEBS Lett. 587 (2013), 2623–2628.
58. 58 Eckerdt, F., et al. Regulatory effects of a Mnk2-eIF4E feedback loop during mTORC1 targeting of human medulloblastoma cells. Oncotarget 5 (2014), 8442–8451.
59. 59 Grzmil, M., et al. MNK1 pathway activity maintains protein synthesis in rapalog-treated gliomas. J. Clin. Invest. 124 (2014), 742–754.
60. 60 Teo, T., et al. Pharmacologic co-inhibition of Mnks and mTORC1 synergistically suppresses proliferation and perturbs cell cycle progression in blast crisis-chronic myeloid leukemia cells. Cancer Lett. 357 (2015), 612–623.
61. 61 Lim, S., et al. Targeting of the MNK-eIF4E axis in blast crisis chronic myeloid leukemia inhibits leukemia stem cell function. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), E2298–E2307.
62. 62 Kumar, K., et al. Differential regulation of ZEB1 and EMT by MAPK-interacting protein kinases (MNKs) and eIF4E in pancreatic cancer. Mol. Cancer Res. 14 (2016), 216–227.
63. 63 Korneeva, N.L., et al. Mnk mediates integrin alpha6beta4-dependent eIF4E phosphorylation and translation of VEGF mRNA. Mol. Cancer Res. 8 (2010), 1571–1578.
64. 64 Kamenska, A., et al. eIF4E-binding proteins: new factors, new locations, new roles. Biochem. Soc. Trans. 42 (2014), 1238–1245.
65. 65 Kong, J., Lasko, P., Translational control in cellular and developmental processes. Nat. Rev. Genet. 13 (2012), 383–394.
66. 66 Santini, E., et al. Exaggerated translation causes synaptic and behavioural aberrations associated with autism. Nature 493 (2012), 411–415.
67. 67 Ronesi, J.A., et al. Disrupted Homer scaffolds mediate abnormal mGluR5 function in a mouse model of fragile X syndrome. Nat. Neurosci. 15 (2012), 431–440.
68. 68 Sharma, A., et al. Dysregulation of mTOR signaling in fragile X syndrome. J. Neurosci. 30 (2010), 694–702.
69. 69 Guo, W., et al. Selective disruption of metabotropic glutamate receptor 5-Homer interactions mimics phenotypes of Fragile X Syndrome in mice. J. Neurosci. 36 (2016), 2131–2147.
70. 70 Alvarez-Castelao, B., Schuman, E.M., The regulation of synaptic protein turnover. J. Biol. Chem. 290 (2015), 28623–28630.
71. 71 Gal-Ben-Ari, S., et al. Consolidation and translation regulation. Learn. Mem. 19 (2012), 410–422.
72. 72 Buxbaum, A.R., et al. Single-molecule insights into mRNA dynamics in neurons. Trends Cell Biol. 25 (2015), 468–475.
73. 73 Willett, M., et al. Translation initiation factors and active sites of protein synthesis co-localize at the leading edge of migrating fibroblasts. Biochem. J. 438 (2011), 217–227.
74. 74 Dziembowska, M., et al. Activity-dependent local translation of matrix metalloproteinase-9. J. Neurosci. 32 (2012), 14538–14547.
75. 75 Feoktistova, K., et al. Human eIF4E promotes mRNA restructuring by stimulating eIF4A helicase activity. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 13339–13344.
76. 76 Kenney, J.W., et al. Eukaryotic elongation factor 2 kinase, an unusual enzyme with multiple roles. Adv. Biol. Regul. 55 (2014), 15–27.
77. 77 Niere, F., et al. Evidence for a fragile X mental retardation protein-mediated translational switch in metabotropic glutamate receptor-triggered Arc translation and long-term depression. J. Neurosci. 32 (2012), 5924–5936.
78. 78 Nalavadi, V.C., et al. Dephosphorylation-Induced Ubiquitination and Degradation of FMRP in Dendrites: A Role in Immediate Early mGluR-Stimulated Translation. J. Neurosci. 32 (2012), 2582–2587.
79. 79 Graber, T.E., et al. Reactivation of stalled polyribosomes in synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 16205–16210.
80. 80 Richter, J.D., Coller, J., Pausing on polyribosomes: make way for elongation in translational control. Cell 163 (2015), 292–300.
81. 81 Fernandez, E., et al. The FMRP regulon: from targets to disease convergence. Front. Neurosci. 7 (2013), 1–9.
82. 82 Richter, J.D., CPEB: a life in translation. Trends Biochem. 32 (2007), 279–285.
83. 83 Cajigas, I.J., et al. The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74 (2012), 453–466.
84. 84 Wang, C., et al. Real-time imaging of translation on single mRNA transcripts in live cells. Cell 165 (2016), 990–1001.
85. 85 Buxbaum, A.R., et al. Single β-actin mRNA detection in neurons reveals a mechanism for regulating its translatability. Science 343 (2014), 419–422.
86. 86 Chen, B., et al. The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156 (2014), 195–207.
87. 87 Anitei, M., et al. Protein complexes containing CYFIP/Sra/PIR121 coordinate Arf1 and Rac1 signalling during clathrin-AP-1-coated carrier biogenesis at the TGN. Nat. Cell Biol. 12 (2010), 330–340.
88. 88 De Rubeis, S., et al. CYFIP1 Coordinates mRNA translation and cytoskeleton remodeling to ensure proper dendritic spine formation. Neuron 79 (2013), 1169–1182.
89. 89 Messaoudi, E., et al. Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo. J. Neurosci. 27 (2007), 10445–10455.
90. 90 Silva, J.M., et al. Cyfip1 is a putative invasion suppressor in epithelial cancers. Cell 137 (2009), 1047–1061.