Cellular distribution of the NMDA-receptor activated synapto-nuclear messenger Jacob in the rat brain

Brain Structure and Function

Volumn 219, Issue 3, 2014, Pages 843-860

  Mikhaylova, Marina ^a,b   Karpova, Anna ^a   Bär, Julia ^a   Bethge, Philipp ^a,d   YuanXiang, Pingan ^c   Chen, Ying ^c   Zuschratter, Werner ^a   Behnisch, Thomas ^c   Kreutz, Michael R ^a  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

^c FUDAN UNIVERSITY   (China)

^d University of Bordeaux   (France)

Author keywords

Excitatory and inhibitory synapses; Jacob; NELF; NMDA receptor; Postsynaptic density; STED microscopy; Synapse to nucleus signaling; Synaptic plasticity

Indexed keywords

N METHYL DEXTRO ASPARTIC ACID RECEPTOR; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN DERIVATIVE; PROTEIN MESSENGER JACOB; UNCLASSIFIED DRUG; NELF PROTEIN, RAT; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN REGION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GENE EXPRESSION; HIPPOCAMPAL CA1 REGION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTERNEURON; LONG TERM POTENTIATION; MICROGLIA; MOSSY FIBER; NERVE CELL; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; ANIMAL; HIPPOCAMPUS; MEMBRANE POTENTIAL; METABOLISM; PHYSIOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION; WISTAR RAT;

RATTUS;

ANIMALS; AXONS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MEMBRANE POTENTIALS; NERVE TISSUE PROTEINS; NEURONAL PLASTICITY; NEURONS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84902362486     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-013-0539-1     Document Type: Article

References (33)

1. Behnisch T, Yuanxiang P, Bethge P, Parvez S, Chen Y, Yu J, Karpova A, Frey JU, Mikhaylova M, Kreutz MR (2011) Nuclear translocation of Jacob in hippocampal neurons after stimuli inducing long-term potentiation but not long-term depression. PLoS One 6:e17276
2. Ch'ng TH, Martin KC (2011) Synapse-to-nucleus signaling. Curr Opin Neurobiol 21:345-352
3. Ch'ng TH, Uzgil B, Lin P, Avliyakulov NK, O'Dell TJ, Martin KC (2012) Activity-dependent transport of the transcriptional coactivator CRTC1 from synapse to nucleus. Cell 150:207-221
4. Cohen S, Greenberg ME (2008) Communication between the synapse and the nucleus in neuronal development, plasticity, and disease. Annu Rev Cell Dev Biol 24:183-209
5. Deisseroth K, Mermelstein PG, Xia H, Tsien RW (2003) Signaling from synapse to nucleus: the logic behind the mechanisms. Curr Opin Neurobiol 13:354-365 (Pubitemid 36805579)
6. Dieterich DC, Karpova A, Mikhaylova M, Zdobnova I, König I, Landwehr M, Kreutz M, Smalla KH, Richter K, Landgraf P, Reissner C, Böckers TM, Zuschratter W, Spilker C, Seidenbecher CI, Garner CC, Gundelfinger ED, Kreutz MR (2008) Caldendrin-Jacob: a protein liaison that couples NMDA receptor signalling to the nucleus. PLoS Biol 6(2):e34
7. Fainzilber M, Budnik V, Segal R, Kreutz MR (2011) From synapse to nucleus and back again - communication over distance within neurons. J Neurosci 31:16045-16048
8. Fritschy JM, Harvey RJ, Schwarz G (2008) Gephyrin: where do we stand, where do we go? Trends Neurosci 31:257-264
9. Greer PL, Greenberg ME (2008) From synapse to nucleus: calcium-dependent gene transcription in the control of synapse development and function. Neuron 59:846-860
10. Hanz S, Perlson E, Willis D, Zheng JQ, Massarwa R, Huerta JJ, Koltzenburg M, Kohler M, van-Minnen J, Twiss JL, Fainzilber M (2003) Axoplasmic importins enable retrograde injury signaling in lesioned nerve. Neuron 40:1095-1104 (Pubitemid 38032787)
11. Hardingham GE, Bading H (2010) Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 11:682-696
12. Ivanov A, Pellegrino C, Rama S, Dumalska I, Salyha Y, Ben-Ari Y, Medina I (2006) Opposing role of synaptic and extrasynaptic NMDA receptors in regulation of the extracellular signal-regulated kinases (ERK) activity in cultured rat hippocampal neurons. J Physiol 572:789-798
13. Jordan BA, Kreutz MR (2009) Nucleocytoplasmic protein shuttling: the direct route in synapse-to-nucleus signaling. Trends Neurosci 32:392-401
14. Karpova A, Mikhaylova M, Bera S, Bär J, Reddy PP, Behnisch T, Rankovic V, Spilker C, Bethge P, Sahin J, Kaushik R, Zuschratter W, Kähne T, Naumann M, Gundelfinger ED, Kreutz MR (2013) Encoding and transducing the synaptic or extrasynaptic origin of NMDA receptor signals to the nucleus. Cell 152(5):1119-1133
15. Karpova A, Mikhaylova M, Thomas U, Knöpfel T, Behnisch T (2006) Involvement of protein synthesis and degradation in long-term potentiation of Schaffer collateral CA1 synapses. J Neurosci 26:4949-4955 (Pubitemid 44315337)
16. Karpova A, Bär J, Kreutz MR (2012) Long-distance signaling from synapse to nucleus via protein messengers. Adv Exp Med Biol 970:355-376
17. Kim MJ, Dunah AW, Wang YT, Sheng M (2005) Differential roles of NR2A- and NR2B-containing NMDA receptors in Ras-ERK signalling and AMPA receptor trafficking. Neuron 46:745-760 (Pubitemid 40733130)
18. Kindler S, Dieterich DC, Schütt J, Sahin J, Karpova A, Mikhaylova M, Schob C, Gundelfinger ED, Kreienkamp HJ, Kreutz MR (2009) Dendritic mRNA targeting of Jacob and NMDA-induced nuclear translocation after Calpain-mediated proteolysis. J Biol Chem 284:25431-25440
19. Kramer PR, Wray S (2000) Novel gene expressed in nasal region influences outgrowth of olfactory axons and migration of luteinizing hormone-releasing hormone (LHRH) neurons. Genes Dev 14:1824-1834 (Pubitemid 30603000)
20. 2+- binding protein caldendrin: gene structure, splice isoforms and expression in the rat central nervous system. Mol Cell Neurosci 19:459-475
21. Malenka RC, Bear MF (2004) LTP and LTD: an embarrassment of riches. Neuron 44:5-21 (Pubitemid 39348827)
22. Martin SJ, Grimwood PD, Morris RGM (2003) Synaptic plasticity and memory: an evaluation of the hypothesis. Ann Rev Neurosci 23:649-711
23. Miura K, Acierno JS Jr, Seminara SB (2004) Characterization of the human nasal embryonic LHRH factor gene, NELF, and a mutation screening among 65 patients with idiopathic hypogonadotropic hypogonadism (IHH). J Hum Genet 49:265-268 (Pubitemid 38856018)
24. Nicoll RA, Schmitz D (2005) Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6:863-876 (Pubitemid 41568728)
25. Okabe S (2007) Molecular anatomy of the postsynaptic density. Mol Cell Neurosci 34:503-518
26. Perlson E, Hanz S, Ben-Yaakov K, Segal-Ruder Y, Seger R, Fainzilber M (2005) Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 45:715-726 (Pubitemid 40320706)
27. Reymann KG, Frey J (2007) The late maintenance of hippocampal LTP: requirements, phases, "synaptic tagging" "late associativity" and implications. Neuropharmacology 52:24-40
28. Rönicke R, Mikhaylova M, Rönicke S, Meinhardt J, Schröder UH, Fändrich M, Reiser G, Kreutz MR, Reymann KG (2011) Early neuronal dysfunction by amyloid b oligomers depends on activation of NR2B-containing NMDA receptors. Neurobiol Aging 32:2219-2228
29. Seidenbecher CI, Langnaese K, Sanmartí-Vila L, Boeckers TM, Smalla KH, Sabel BA, Garner CC, Gundelfinger ED, Kreutz MR (1998) Caldendrin, a novel neuronal calcium-binding protein confined to the somato-dendritic compartment. J Biol Chem 273:21324-21331 (Pubitemid 28385426)
30. Sheng M, Hoogenraad CC (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76:823-847
31. Thomas GM, Huganir RL (2004) MAPK cascade signalling and synaptic plasticity. Nat Rev Neurosci 5:173-183 (Pubitemid 38252474)
32. Thompson KR, Otis KO, Chen DY, Zhao Y, O'Dell TJ, Martin KC (2004) Synapse to nucleus signaling during long-term synaptic plasticity; a role for the classical active nuclear import pathway. Neuron 44:997-1009 (Pubitemid 39643095)
33. Tsuriel S, Geva R, Zamorano P, Dresbach T, Boeckers T, Gundelfinger ED, Garner CC, Ziv NE (2006) Local sharing as a predominant determinant of synaptic matrix molecular dynamics. PLoS Biol 4:e271