Signaling logic of activity-triggered dendritic protein synthesis: An mTOR gate but not a feedback switch

PLoS Computational Biology

Volumn 5, Issue 2, 2009, Pages

  Jain, Pragati ^a   Bhalla, Upinder S ^a  

^a TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTICS; BIOSYNTHESIS; BRAIN; COMPUTER CIRCUITS; MAMMALS; PROTEINS; STABILITY;

ACTIVITY FACTOR; CELLULAR ACTIVITIES; CELLULAR GROWTH; CELLULARS; DENDRITICS; GROWTH FACTOR; MAMMALIAN TARGET; MULTIPLE INPUTS; PROTEIN SYNTHESIS; TARGET OF RAPAMYCIN;

FEEDBACK;

BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CALCIUM ION; ELONGATION FACTOR 2 KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE B; S6 KINASE; CALCIUM; NERVE PROTEIN; PROTEIN KINASE;

ARTICLE; CHEMICAL REACTION; DENDRITE; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; MOLECULAR MODEL; MOLECULAR STABILITY; POSITIVE FEEDBACK; PREDICTION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STEADY STATE; STIMULUS RESPONSE; ANIMAL; BIOSYNTHESIS; METABOLISM; MOUSE; MOUSE MUTANT;

MAMMALIA;

ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CALCIUM; DENDRITES; MICE; MICE, KNOCKOUT; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE TISSUE PROTEINS; PROTEIN KINASES; SIGNAL TRANSDUCTION;

EID: 61449146200     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1000287     Document Type: Article

References (82)

1. Sutton MA, Schuman EM (2006) Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127: 49-58.
2. Schuman EM, Dynes JL, Steward O (2006) Synaptic regulation of translation of dendritic mRNAs. J Neurosci 26: 7143-7146.
3. Tang SJ, Schuman EM (2002) Protein synthesis in the dendrite. Philos Trans R Soc Lond B Biol Sci 357: 521-529.
4. Bramham CR, Wells DG (2007) Dendritic mRNA: transport, translation and function. Nat Rev Neurosci 8: 776-789.
5. Klann E, Antion MD, Banko JL, Hou L (2004) Synaptic plasticity and translation initiation. Learn Mem 11: 365-372.
6. Schuman EM, Seeburg PH (2006) Signalling mechanisms. Curr Opin Neurobiol 16: 247-250.
7. Govindarajan A, Kelleher RJ, Tonegawa S (2006) A clustered plasticity model of long-term memory engrams. Nat Rev Neurosci 7: 575-583.
8. Frey S, Frey JU (2008) 'Synaptic tagging' and 'cross-tagging' and related associative reinforcement processes of functional plasticity as the cellular basis for memory formation. Prog Brain Res 169: 117-143.
9. Bhalla US (2003) Understanding complex signaling networks through models and metaphors. Prog Biophys Mol Biol 81: 45-65.
10. Song H, Smolen P, Av-Ron E, Baxter DA, Byrne JH (2007) Dynamics of a minimal model of interlocked positive and negative feedback loops of transcriptional regulation by cAMP-response element binding proteins. Biophys J92: 3407-3424.
11. Lisman JE, Mclntyre CC (2001) Synaptic plasticity: a molecular memory switch. Curr Biol 11: R788-R791.
12. Bhalla US, Iyengar R (1999) Emergent properties of networks of biological signaling pathways. Science 283: 381-387.
13. Tanaka K, Augustine GJ (2008) A positive feedback signal transduction loop determines timing of cerebellar long-term depression. Neuron 59: 608-620.
14. Xia Y, Carroll RC, Nawy S (2006) State-dependent AMPA receptor trafficking in the mammalian retina. J Neurosci 26: 5028-5036.
15. Kang H, Schuman EM (1996) A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity. Science 273: 1402-1406.
16. Huber KM, Kayser MS, Bear MF (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288:1254-1257.
17. Wells DG, Dong X, Quinlan EM, Huang YS, Bear MF, et al. (2001) A role for the cytoplasmic polyadenylation element in NMDA receptor-regulated mRNA translation in neurons. J Neurosci 21: 9541-9548.
18. Hou L, Klann E (2004) Activation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin signaling pathway is required for metabotropic glutamate receptor-dependent long-term depression. JNeurosci 24: 6352-6361.
19. Saarelainen T, Vaittinen S, Castren E (2001) trk B-receptor activation contributes to the kainate-induced increase in BDNF mRNA synthesis. Cell Mol Neurobiol 21: 429-435.
20. Dijkhuizen PA, Ghosh A (2005) BDNF regulates primary dendrite formation in cortical neurons via the PI3-kinase and MAP kinase signaling pathways. J Neurobiol 62: 278-288.
21. Obermeier A, Lammers R, Wiesmuller KH, Jung G, Schlessinger J, et al. (1993) Identification of Trk binding sites for SHC and phosphatidylinositol 3'-kinase and formation of a multimeric signaling complex. J Biol Chem 268:22963-22966.
22. Holgado-Madruga M, Moscatello DK, Emlet DR, Dieterich R, Wong AJ(1997) Grb2-associated binder-1 mediates phosphatidylinositol 3-kinase activation and the promotion of cell survival by nerve growth factor. Proc Natl Acad Sci USA 94: 12419-12424.
23. Ohmichi M, Decker SJ, Saltiel AR (1992) Activation of phosphatidylinositol-3 kinase by nerve growth factor involves indirect coupling of the trk proto-oncogene with src homology 2 domains. Neuron 9: 769-777.
24. Huang EJ, Reichardt LF (2001) Neurotrophins: roles in neuronal development and function. Annu Rev Neurosci 24: 677-736.
25. Schlessinger J, Lemmon MA (2003) SH2 and PTB domains in tyrosine kinase signaling. Sci STKE 2003: RE12.
26. Patapoutian A, Reichardt LF (2001) Trk receptors: mediators of neurotrophin action. Curr Opin Neurobiol 11: 272-280.
27. Kodaki T, Woscholski R, Hallberg B, Rodriguez-Viciana P, Downward J, et al. (1994) The activation of phosphatidylinositol 3-kinase by Ras. Curr Biol 4: 798-806.
28. Yuen EC, Mobley WC (1999) Early BDNF, NT-3, and NT-4 signaling events. Exp Neurol 159: 297-308.
29. Chan TO, Tsichlis PN(2001) PDK2: a complextailin one Akt. Sci STKE 2001: PE1.
30. Koh G, Teong HF, Clement MV, Hsu D, Thiagarajan PS (2006) A decompositional approach to parameter estimation in pathway modeling: a case study of the Akt and MAPK pathways and their crosstalk. Bioinformatics 22: e271-e280.
31. McManus EJ, Alessi DR (2002) TSC1-TSC2: a complex tale of PKB-mediated S6K regulation. Nat Cell Biol 4: E214-E216.
32. Inoki K, Li Y, Xu T, Guan KL (2003) Rheb GTPase is a direct target ofTSC2 GAP activity and regulates mTOR signaling. Genes Dev 17: 1829-1834.
33. Tsokas P, Ma T, Iyengar R, Landau EM, Blitzer RD (2007) Mitogen-activated protein kinase upregulates the dendritic translation machinery in long-term potentiation by controlling the mammalian target of rapamycin pathway. J Neurosci 27: 5885-5894.
34. Zheng F, Soellner D, Nunez J, Wang H (2008) The basal level of intracellular calcium gates the activation of phosphoinositide 3-kinase-Akt signaling by brain-derived neurotrophic factor in cortical neurons. J Neurochem 106: 1259-1274.
35. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, et al. (1997) Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr Biol 7: 261-269.
36. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J (2005) Rheb binds and regulates the mTOR kinase. Curr Biol 15: 702-713.
37. Isotani S, Hara K, Tokunaga C, Inoue H, Avruch J, et al. (1999) Immunopurified mammalian target of rapamycin phosphorylates and activates p70 S6 kinase a in vitro. J Biol Chem 274: 34493-34498.
38. Alessi DR, Kozlowski MT, Weng QP, Morrice N, Avruch J (1998) 3-Phosphoinositide-dependent protein kinase 1 (PDK1) phosphorylates and activates the p70 S6 kinase in vivo and in vitro. Curr Biol 8: 69-81.
39. Hara K, Maruki Y, Long X, Yoshino K, Oshiro N, et al. (2002) Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 110:177-189.
40. Kim DH, Sarbassov DD, Ali SM, Latek RR, Guntur KV, et al. (2003) GβL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol Cell 11: 895-904.
41. Ballou LM, Jeno P, Thomas G (1988) Protein phosphatase 2A inactivates the mitogen-stimulated S6 kinase from Swiss mouse 3T3 cells. J Biol Chem 263:1188-1194.
42. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18: 1926-1945.
43. Shahbazian D, Roux PP, Mieulet V, Cohen MS, Raught B, et al. (2006) The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. EMBO J 25: 2781-2791.
44. Toral-Barza L, Zhang WG, Lamison C, Larocque J, Gibbons J, et al. (2005) Characterization of the cloned full-length and a truncated human target of rapamycin: activity, specificity, and enzyme inhibition as studied by a high capacity assay. Biochem Biophys Res Commun 332: 304-310.
45. Karim MM, Hughes JM, Warwicker J, Scheper GC, Proud CG, et al. (2001) A quantitative molecular model for modulation of mammalian translation by the eIF4E-binding protein 1. J Biol Chem 276: 20750-20757.
46. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, et al. (1999) Regulation of 4E-BP1 phosphorylation: a novel two-step mechanism. Genes Dev 13: 1422-1437.
47. Ptushkina M, von der Haar T, Karim MM, Hughes JM, McCarthy JE (1999) Repressor binding to a dorsal regulatory site traps human eIF4E in a high cap-affinity state. EMBO J 18: 4068-4075.
48. Ryazanov AG, Shestakova EA, Natapov PG (1988) Phosphorylation of elongation factor 2 by EF-2 kinase affects rate of translation. Nature 334: 170-173.
49. Redpath NT, Price NT, Severinov KV, Proud CG (1993) Regulation of elongation factor-2 by multisite phosphorylation. Eur JBiochem 213: 689-699.
50. Wang X, Li W, Williams M, Terada N, Alessi DR, et al. (2001) Regulation of elongation factor 2 kinase by p90(RSK1) and p70 S6 kinase. EMBO J 20: 4370-4379.
51. Mitsui K, Brady M, Palfrey HC, Nairn AC (1993) Purification and characterization of calmodulin-dependent protein kinase III from rabbit reticulocytes and rat pancreas. J Biol Chem 268: 13422-13433.
52. Manchester KL (1997) Binding constants in the formation of mammalian protein synthesis initiation complexes and the role of mRNA. Biochem Biophys Res Commun 230: 27-29.
53. Wang X, Proud CG (2006) The mTOR pathway in the control of protein synthesis. Physiology (Bethesda) 21: 362-369.
54. Parkhurst KM, Hileman RE, Saha D, Gupta NK, Parkhurst LJ (1994) Thermodynamic characterization of the cooperativity of40S complex formation during the initiation of eukaryotic protein synthesis. Biochemistry 33: 15168-15177.
55. Ajay SM, Bhalla US (2004) A role for ERKII in synaptic pattern selectivity on the time-scale of minutes. Eur J Neurosci 20: 2671-2680.
56. Takei N, Inamura N, Kawamura M, Namba H, Hara K, et al. (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.
57. Kelleher RJ III, 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.
58. 2+/calmodulin-dependent protein kinase II and protein phosphatase 1 during hippocampal long-term potentiation. J Neurosci 25: 5604-5610.
59. Marshall CJ (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80: 179-185.
60. Treisman R (1996) Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol 8: 205-215.
61. Waskiewicz AJ, Cooper JA (1995) Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr Opin Cell Biol 7: 798-805.
62. Dudek SM, Bear MF (1992) Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proc Natl Acad Sci U S A 89: 4363-4367.
63. Kleijn M, Scheper GC, Voorma HO, Thomas AA (1998) Regulation of translation initiation factors by signal transduction. Eur J Biochem 253: 531-544.
64. Huang S, Houghton PJ(2001) Mechanisms of resistance to rapamycins. Drug Resist Updat 4: 378-391.
65. Kanhema T, Dagestad G, Panja D, Tiron A, Messaoudi E, et al. (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.
66. Kolarow R, Brigadski T, Lessmann V (2007) Postsynaptic secretion of BDNF and NT-3 from hippocampal neurons depends on calcium calmodulin kinase II signaling and proceeds via delayed fusion pore opening. J Neurosci 27: 10350-10364.
67. Lu Y, Christian K, Lu B (2008) BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 89: 312-323.
68. Kovalchuk Y, Hanse E, Kafitz KW, Konnerth A (2002) Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295: 1729-1734.
69. Lessmann V, Gottmann K, Malcangio M (2003) Neurotrophin secretion: current facts and future prospects. Prog Neurobiol 69: 341-374.
70. Blitzer RD, Iyengar R, Landau EM (2005) Postsynaptic signaling networks: cellular cogwheels underlying long-term plasticity. Biol Psychiatry 57: 113-119.
71. Lisman JE, Fallon JR (1999) What maintains memories? Science 283: 339-340.
72. Eberwine J, Miyashiro K, Kacharmina JE, Job C (2001) Local translation of classes of mRNAs that are targeted to neuronal dendrites. Proc Natl Acad Sci USA 98: 7080-7085.
73. Ferrell JE Jr (2008) Feedback regulation of opposing enzymes generates robust, all-or-none bistable responses. Curr Biol 18: R244-R245.
74. Ferrell JE Jr (2002) Self-perpetuating states in signal transduction: positive feedback, double-negative feedback and bistability. Curr Opin Cell Biol 14: 140-148.
75. Hayer A, Bhalla US (2005) Molecular switches at the synapse emerge from receptor and kinase traffic. PLoS Comput Biol 1: e20. doi:10.1371/journal. pcbi.0010020.
76. Marin P, Nastiuk KL, Daniel N, Girault JA, Czernik AJ, et al. (1997) Glutamate-dependent phosphorylation of elongation factor-2 and inhibition of protein synthesis in neurons. J Neurosci 17: 3445-3454.
77. Bray D, Levin MD, Lipkow K (2007) The chemotactic behavior of computer-based surrogate bacteria. Curr Biol 17: 12-19.
78. Shimizu TS, Bray D (2002) Modelling the bacterial chemotaxis receptor complex. Novartis Found Symp 247: 162-177; discussion 177-181, 198-206, 244-152.
79. Mullasseril P, Dosemeci A, Lisman JE, Griffith LC (2007) A structural mechanism for maintaining the 'on-state' of the CaMKII memory switch in the post-synaptic density. J Neurochem 103: 357-364.
80. Vayttaden SJ, Bhalla US (2004) Developing complex signaling models using GENESIS/Kinetikit. Sci STKE 2004: pl4.
81. Hoops S, Sahle S, Gauges R, Lee C, Pahle J, et al. (2006) COPASI-a COmplex PAthway SImulator. Bioinformatics 22: 3067-3074.
82. Funahashi A, Tanimura N, Morohashi M, Kitano H (2003) Cell Designer: a process diagram editor for gene-regulatory and biochemical networks. BIOSILICO 1: 159-162.