Proteolysis of proBDNF is a key regulator in the formation of memory

PLoS ONE

Volumn 3, Issue 9, 2008, Pages

  Barnes, Philip ^a   Thomas, Kerrie L ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLOHEPTANE DERIVATIVE; MESSENGER RNA; TPA STOP; UNCLASSIFIED DRUG;

ANIMAL; ANIMAL BEHAVIOR; ARTICLE; BIOLOGICAL MODEL; FEAR; GENETIC TRANSCRIPTION; GENETICS; HIPPOCAMPUS; HUMAN; LEARNING; MALE; MEMORY; METABOLISM; NERVE CELL; RAT;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN-DERIVED NEUROTROPHIC FACTOR; CYCLOHEPTANES; FEAR; HIPPOCAMPUS; HUMANS; LEARNING; MALE; MEMORY; MODELS, BIOLOGICAL; NEURONS; RATS; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 54749091291     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0003248     Document Type: Article

References (60)

1. McGaugh JL (2000) Memory-a century of consolidadon. Science 287: 248-251.
2. Routtenberg A, Rekart JL (2005) Post-translational protein modification as the substrate for long-lasting memory. Trends in neurosciences 28:12-19.
3. McClelland JL, Rumelhart DE (1985) Distributed memory and the representation of general and specific information. J Exp Psychol Gen 114: 159-197.
4. Rescorla RA, Wagner AR (1972) A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In Classical conditioning II: Current research and theory. AH Black, WK Prokasy, eds. New York: Appleton-Century-Crofts. pp 64-99.
5. McCloskey M, Cohen NJ (1989) Catastrophic interference in connectionist networks: The sequential learning problem. In The psychology of learning and motivation. San Diego, CA: Academic Press 24: 109-165.
6. Bouton ME (2004) Context and behavioral processes in extinction. Learning & memory (Cold Spring Harbor, NY 11: 485-494.
7. Berman DE, Dudai Y (2001) Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 291: 2417-2419.
8. Rodrigues SM, Schafe GE, LeDoux JE (2004) Molecular mechanisms underlying emotional learning and memory in the lateral amygdala. Neuron 44: 75-91.
9. Costa-Mattioli M, Gobert D, Stern E, Gamache K, Colina R, et al. (2007) eIF2alpha phosphorylation bidirectionally regulates the switch from short- to long-term synaptic plasticity and memory. Cell 129: 195-206.
10. LaLumiere RT, Nawar EM, McGaugh JL (2005) Modulation of memory consolidation by the basolateral amygdala or nucleus accumbens shell requires concurrent dopamine receptor activation in both brain regions. Learning & memory (Cold Spring Harbor, NY 12: 296-301.
11. Raymond CR (2007) LTP forms 1, 2 and 3: different mechanisms for the "long" in long-term potentiation. Trends in neurosciences 30: 167-175.
12. McKernan MG, Shinnick-Gallagher P (1997) Fear conditioning induces a lasting potentiation of synaptic currents in vitro. Nature 390: 607-611.
13. Rogan MT, Staubli UV, LeDoux JE (1997) Fear conditioning induces associative long-term potentiation in the amygdala. Nature 390: 604-607.
14. Falls WA, Miserendino MJ, Davis M (1992) Extinction of fear-potentiated startle: blockade by infusion of an NMDA antagonist into the amygdala. The Journal of neuroscience 12: 854-863.
15. Lee H, Kim JJ (1998) Amygdalar NMDA receptors are critical for new fear learning in previously fear-conditioned rats. The Journal of neuroscience 18: 8444-8454.
16. Szapiro G, Vianna MR, McGaugh JL, Medina JH, Izquierdo I (2003) The role of NMDA glutamate receptors, PKA, MAPK, and CAMKII in the hippocampus in extinction of conditioned fear. Hippocampus 13: 53-58.
17. Berlau DJ, McGaugh JL (2006) Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiology of learning and memory 86: 123-132.
18. Marsicano G, Wotjak CT, Azad SC, Bisogno T, Rammes G, et al. (2002) The endogenous cannabinoid system controls extinction of aversive memories. Nature 418: 530-534.
19. Lin CH, Yeh SH, Leu TH, Chang WC, Wang ST, et al. (2003) Identification of calcineurin as a key signal in the extinction of fear memory. The Journal of neuroscience 23: 1574-1579.
20. Chen X, Garelick MG, Wang H, Lil V, Athos J, et al. (2005) PI3 kinase signaling is required for retrieval and extinction of contextual memory. Nature neuroscience 8: 925-931.
21. Mulkey RM, Endo S, Shenolikar S, Malenka RC (1994) Involvement of a calcineurin/inhibitor-1 phosphatase cascade in hippocampal long-term depression. Nature 369: 486-488.
22. Chevaleyre V, Castillo PE (2004) Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 43: 871-881.
23. Lin CH, Lee CC, Huang YC, Wang SJ, Gean PW (2005) Activation of group II metabotropic glutamate receptors induces depotentiation in amygdala slices and reduces fear-potentiated startle in rats. Learning & memory (Cold Spring Harbor, NY 12: 130-137.
24. Lee JL, Everitt BJ, Thomas KL (2004) Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304: 839-843.
25. Seidah NG, Benjannet S, Pareek S, Chretien M, Murphy RA (1996) Cellular processing of the neurotrophin precursors of NT3 and BDNF by the mammalian proprotein convertases. FEBS letters 379: 247-250.
26. Lessmann V, Gottmann K, Malcangio M (2003) Neurotrophin secretion: current facts and future prospects. Progress in neurobiology 69: 341-374.
27. Woo NH, Teng HK, Siao CJ, Chiaruttini C, Pang PT, et al. (2005) Activation of p75NTR by proBDNF facilitates hippocampal long-term depression. Nature neuroscience 8: 1069-1077.
28. Pang PT, Teng HK, Zaitsev E, Woo NT, Sakata K, et al. (2004) Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science (New York, NY 306: 487-491.
29. Waltereit R, Dammermann B, Wulff P, Scafidi J, Staubli U, et al. (2001) Arg3.1/Arc mRNA induction by Ca2+ and cAMP requires protein kinase A and mitogen-activated protein kinase/extracellular regulated kinase activation. J Neurosci 21: 5484-5493.
30. Yin Y, Eddman GM, Vanderklish PW (2002) The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proceedings of the National Academy of Sciences of the United States of America 99: 2368-2373.
31. Ying SW, Futter M, Rosenblum K, Webber MJ, Hunt SP, et al. (2002) Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. The Journal of neuroscience 22: 1532-1540.
32. Plath N, Ohana O, Dammermann B, Errington ML, Schmitz D, et al. (2006) Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52: 437-444.
33. Guzowski JF, Lyford GL, Stevenson GD, Houston FP, McGaugh JL, et al. (2000) Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. The Journal of neuroscience 20: 3993-4001.
34. Messaoudi E, Kanhema T, Soule J, Tiron A, Dagyte G, et al. (2007) 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: 10445-10455.
35. Hall J, Thomas KL, Everitt BJ (2001) Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. The Journal of neuroscience 21: 2186-2193.
36. Hall J, Thomas KL, Everitt BJ (2000) Rapid and selective induction of BDNF expression in the hippocampus during contextual learning. Nature neuroscience 3: 533-535.
37. Lee I, Kesner RP (2003) Differential roles of dorsal hippocampal subregions in spatial working memory with short versus intermediate delay. Behav Neurosci 117: 1044-1053.
38. Liot G, Benchenane K, Leveille F, Lopez-Atalaya JP, Fernandez-Monreal M, et al. (2004) 2,7-Bis-(4-amidinobenzylidene)-cydoheptan-1-one dihydrochloride, tPA stop, prevents tPA-enhanced excitotoxicity both in vitro and in vivo. J Cereb Blood Flow Metab 24: 1153-1159.
39. Chen ZL, Strickland S (1997) Neuronal death in the hippocampus is promoted by plasmin-catalyzed degradation of laminin. Cell 91: 917-925.
40. Horwood JM, Ripley TL, Stephens DN (2004) Evidence for disrupted NMDA receptor function in tissue plasminogen activator knockout mice. Behav Brain Res 150: 127-138.
41. Wu YP, Siao CJ, Lu W, Sung TC, Frohman MA, et al. (2000) The tissue plasminogen activator (tPA)/plasmin extracellular proteolytic system regulates seizure-induced hippocampal mossy fiber outgrowth through a proteoglycan substrate. J Cell Biol 148: 1295-1304.
42. Zhuo M, Holtzman DM, Li Y, Osaka H, DeMaro J, et al. (2000) Role of tissue plasminogen activator receptor LRP in hippocampal long-term potentiation. J Neurosci 20: 542-549.
43. Chhatwal JP, Stanek-Rattiner L, Davis M, Ressler KJ (2006) Amygdala BDNF signaling is required for consolidation but not encoding of extinction. Nat Neurosci 9: 870-872.
44. Heldt SA, Stanek L, Chhatwal JP, Ressler KJ (2007) Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol Psychiatry 12: 656-670.
45. Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, et al. (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. The Journal of neuroscience 24: 4787-4795.
46. Eisenberg M, Kobilo T, Berman DE, Dudai Y (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301: 1102-1104.
47. Farhadi HF, Mowla SJ, Petrecca K, Morris SJ, Seidah NG, et al. (2000) Neurotrophin-3 sorts to the constitutive secretory pathway of hippocampal neurons and is diverted to the regulated secretory pathway by coexpression with brain-derived neurotrophic factor. J Neurosci 20: 4059-4068.
48. Mowla SJ, Farhadi HF, Pareek S, Atwal JK, Morris SJ, et al. (2001) Biosynthesis and post-translational processing of the precursor m brain-derived neurotrophic factor. J Biol Chem 276: 12660-12666.
49. Baranes D, Lederfein D, Huang YY, Chen M, Bailey CH, et al. (1998) Tissue plasminogen activator contributes to the late phase of LTP and to synaptic growth in the hippocampal mossy fiber pathway. Neuron 21: 813-825.
50. Ullal GR, Michalski B, Xu B, Racine RJ, Fahnestock M (2007) NT-3 modulates BDNF and proBDNF levels in naive and kindled rat hippocampus. Neurochem Int 50: 866-871.
51. Matsumoto T, Rauskolb S, Polack M, Klose J, Kolbeck R, et al. (2008) Biosynthesis and processing of endogenous BDNF: CNS neurons store and secrete BDNF, not pro-BDNF. Nat Neurosci 11: 131-133.
52. Summerton JE (2007) Morpholino, siRNA, and S-DNA compared: impact of structure and mechanism of action on off-target effects and sequence specificity. Curr Top Med Chem 7: 651-660.
53. Liu QR, Walther D, Drgon T, Polesskaya O, Lesnick TG, et al. (2005) Human brain derived neurotrophic factor (BDNF) genes, splicing patterns, and assessments of associations with substance abuse and Parkinson's Disease. Am J Med Genet B Neuropsychiatr Genet 134: 93-103.
54. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T (2007) Mouse and rat BDNF gene structure and expression revisited. Journal of neuroscience research 85: 525-535.
55. Lu B, Pang PT, Woo NH (2005) The yin and yang of neurotrophin action. Nat Rev Neurosci 6: 603-614.
56. Lin CH, Yeh SH, Lu HY, Gean PW (2003) The similarities and diversities of signal pathways leading to consolidation of conditioning and consolidation of extinction of fear memory. The Journal of neuroscience 23: 8310-8317.
57. Shema R, Sacktor TC, Dudai Y (2007) Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM zeta. Science 317: 951-953.
58. Lewis DJ (1979) Psychobiology of active and inactive memory. Psychol Bull 86: 1054-1083.
59. Bisson JI, Jenkins PL, Alexander J, Bannister C (1997) Randomised controlled trial of psychological debriefing for victims of acute burn trauma. Br J Psychiatry 171: 78-81.
60. Mayou RA, Ehlers A, Hobbs M (2000) Psychological debriefing for road traffic accident victims. Three-year follow-up of a randomised controlled trial. Br J Psychiatry 176: 589-593.