Synaptic activity controls localization and function of CtBP1 via binding to Bassoon and Piccolo

EMBO Journal

Volumn 34, Issue 8, 2015, Pages 1056-1077

  Ivanova, Daniela ^a   Dirks, Anika ^a   Montenegro Venegas, Carolina ^a   Schöne, Cornelia ^a,d   Altrock, Wilko D ^a,b   Marini, Claudia ^a   Frischknecht, Renato ^a,b   Schanze, Denny ^b   Zenker, Martin ^b   Gundelfinger, Eckart D ^a,b   Fejtova, Anna ^a,b,c  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL MAGDEBURG   (Germany)

^d NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

cellular NAD NADH balance; neuronal activity regulated gene expression; neuronal plasticity; presynapse to nucleus signaling; synapto nuclear shuttling

Indexed keywords

BASSOON; NICOTINAMIDE ADENINE DINUCLEOTIDE; PICCOLO; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; BSN PROTEIN, RAT; CARRIER PROTEIN; CTBP1 PROTEIN, RAT; CYTOSKELETON PROTEIN; NERVE PROTEIN; NEUROPEPTIDE; PCLO PROTEIN, RAT; PROTEIN BINDING; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL BODY; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; NERVE CELL; NONHUMAN; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RAT; SYNAPSE; ANIMAL; C57BL MOUSE; CELL CULTURE; CHLOROCEBUS AETHIOPS; COS 1 CELL LINE; HEK293 CELL LINE; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; PROTEIN TRANSPORT; WISTAR RAT;

ANIMALS; CARRIER PROTEINS; CELLS, CULTURED; CERCOPITHECUS AETHIOPS; COS CELLS; CYTOSKELETAL PROTEINS; HEK293 CELLS; HUMANS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; NEUROPEPTIDES; PROTEIN BINDING; PROTEIN TRANSPORT; RATS; RATS, WISTAR; SYNAPSES; TRANSCRIPTION FACTORS;

EID: 84927693658     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201488796     Document Type: Article

References (62)

1. Alabi AA, Tsien RW, (2012) Synaptic vesicle pools and dynamics. Cold Spring Harb Perspect Biol 4: a013680
2. Barnes CJ, Vadlamudi RK, Mishra SK, Jacobson RH, Li F, Kumar R, (2003) Functional inactivation of a transcriptional corepressor by a signaling kinase. Nat Struct Biol 10: 622-628
3. Brennan AM, Connor JA, Shuttleworth CW, (2006) NAD(P)H fluorescence transients after synaptic activity in brain slices: predominant role of mitochondrial function. J Cereb Blood Flow Metab 26: 1389-1406
4. Chawla S, Vanhoutte P, Arnold FJ, Huang CL, Bading H, (2003) Neuronal activity-dependent nucleocytoplasmic shuttling of HDAC4 and HDAC5. J Neurochem 85: 151-159
5. Chinnadurai G, (2007) Transcriptional regulation by C-terminal binding proteins. Int J Biochem Cell Biol 39: 1593-1607
6. Chinnadurai G, (2009) The transcriptional corepressor CtBP: a foe of multiple tumor suppressors. Cancer Res 69: 731-734
7. Ch'ng TH, Martin KC, (2011) Synapse-to-nucleus signaling. Curr Opin Neurobiol 21: 345-352
8. Corda D, Colanzi A, Luini A, (2006) The multiple activities of CtBP/BARS proteins: the Golgi view. Trends Cell Biol 16: 167-173
9. Dick O, Hack I, Altrock WD, Garner CC, Gundelfinger ED, Brandstatter JH, (2001) Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: comparison with Bassoon. J Comp Neurol 439: 224-234
10. Dick O, tom Dieck S, Altrock WD, Ammermuller J, Weiler R, Garner CC, Gundelfinger ED, Brandstatter JH, (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37: 775-786
11. tom Dieck S, Sanmarti-Vila L, Langnaese K, Richter K, Kindler S, Soyke A, Wex H, Smalla KH, Kampf U, Franzer JT, Stumm M, Garner CC, Gundelfinger ED, (1998) Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J Cell Biol 142: 499-509
12. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtova A, Bracko O, Gundelfinger ED, Brandstatter JH, (2005) Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol 168: 825-836
13. Dresbach T, Hempelmann A, Spilker C, tom Dieck S, Altrock WD, Zuschratter W, Garner CC, Gundelfinger ED, (2003) Functional regions of the presynaptic cytomatrix protein bassoon: significance for synaptic targeting and cytomatrix anchoring. Mol Cell Neurosci 23: 279-291
14. Dresbach T, Torres V, Wittenmayer N, Altrock WD, Zamorano P, Zuschratter W, Nawrotzki R, Ziv NE, Garner CC, Gundelfinger ED, (2006) Assembly of active zone precursor vesicles: obligatory trafficking of presynaptic cytomatrix proteins Bassoon and Piccolo via a trans-Golgi compartment. J Biol Chem 281: 6038-6047
15. Fainzilber M, Budnik V, Segal RA, Kreutz MR, (2011) From synapse to nucleus and back again-communication over distance within neurons. J Neurosci 31: 16045-16048
16. Fejtova A, Davydova D, Bischof F, Lazarevic V, Altrock WD, Romorini S, Schone C, Zuschratter W, Kreutz MR, Garner CC, Ziv NE, Gundelfinger ED, (2009) Dynein light chain regulates axonal trafficking and synaptic levels of Bassoon. J Cell Biol 185: 341-355
17. Fenster SD, Chung WJ, Zhai R, Cases-Langhoff C, Voss B, Garner AM, Kaempf U, Kindler S, Gundelfinger ED, Garner CC, (2000) Piccolo, a presynaptic zinc finger protein structurally related to bassoon. Neuron 25: 203-214
18. Frank T, Rutherford MA, Strenzke N, Neef A, Pangrsic T, Khimich D, Fejtova A, Gundelfinger ED, Liberman MC, Harke B, Bryan KE, Lee A, Egner A, Riedel D, Moser T, (2010) Bassoon and the synaptic ribbon organize Ca(2)+ channels and vesicles to add release sites and promote refilling. Neuron 68: 724-738
19. Frischknecht R, Fejtova A, Viesti M, Stephan A, Sonderegger P, (2008) Activity-induced synaptic capture and exocytosis of the neuronal serine protease neurotrypsin. J Neurosci 28: 1568-1579
20. Garriga-Canut M, Schoenike B, Qazi R, Bergendahl K, Daley TJ, Pfender RM, Morrison JF, Ockuly J, Stafstrom C, Sutula T, Roopra A, (2006) 2-Deoxy-D-glucose reduces epilepsy progression by NRSF-CtBP-dependent metabolic regulation of chromatin structure. Nat Neurosci 9: 1382-1387
21. 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
22. Hagenston AM, Bading H, (2011) Calcium signaling in synapse-to-nucleus communication. Cold Spring Harb Perspect Biol 3: a004564
23. Hallermann S, Fejtova A, Schmidt H, Weyhersmuller A, Silver RA, Gundelfinger ED, Eilers J, (2010) Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68: 710-723
24. 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
25. Hara D, Fukuchi M, Miyashita T, Tabuchi A, Takasaki I, Naruse Y, Mori N, Kondo T, Tsuda M, (2009) Remote control of activity-dependent BDNF gene promoter-I transcription mediated by REST/NRSF. Biochem Biophys Res Commun 384: 506-511
26. Hubler D, Rankovic M, Richter K, Lazarevic V, Altrock WD, Fischer KD, Gundelfinger ED, Fejtova A, (2012) Differential spatial expression and subcellular localization of CtBP family members in rodent brain. PLoS One 7: e39710
27. Jordan BA, Kreutz MR, (2009) Nucleocytoplasmic protein shuttling: the direct route in synapse-to-nucleus signaling. Trends Neurosci 32: 392-401
28. Jose M, Nair DK, Altrock WD, Dresbach T, Gundelfinger ED, Zuschratter W, (2008) Investigating interactions mediated by the presynaptic protein bassoon in living cells by Foerster's resonance energy transfer and fluorescence lifetime imaging microscopy. Biophys J 94: 1483-1496
29. Kasischke KA, Vishwasrao HD, Fisher PJ, Zipfel WR, Webb WW, (2004) Neural activity triggers neuronal oxidative metabolism followed by astrocytic glycolysis. Science 305: 99-103
30. Katsanis N, Fisher EM, (1998) A novel C-terminal binding protein (CTBP2) is closely related to CTBP1, an adenovirus E1A-binding protein, and maps to human chromosome 21q21.3. Genomics 47: 294-299
31. Khimich D, Nouvian R, Pujol R, tom Dieck S, Egner A, Gundelfinger ED, Moser T, (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434: 889-894
32. Kim JH, Cho EJ, Kim ST, Youn HD, (2005) CtBP represses p300-mediated transcriptional activation by direct association with its bromodomain. Nat Struct Mol Biol 12: 423-428
33. Kraszewski K, Mundigl O, Daniell L, Verderio C, Matteoli M, De Camilli P, (1995) Synaptic vesicle dynamics in living cultured hippocampal neurons visualized with CY3-conjugated antibodies directed against the lumenal domain of synaptotagmin. J Neurosci 15: 4328-4342
34. Kumar V, Carlson JE, Ohgi KA, Edwards TA, Rose DW, Escalante CR, Rosenfeld MG, Aggarwal AK, (2002) Transcription corepressor CtBP is an NAD(+)-regulated dehydrogenase. Mol Cell 10: 857-869
35. Kuppuswamy M, Vijayalingam S, Zhao LJ, Zhou Y, Subramanian T, Ryerse J, Chinnadurai G, (2008) Role of the PLDLS-binding cleft region of CtBP1 in recruitment of core and auxiliary components of the corepressor complex. Mol Cell Biol 28: 269-281
36. Lazarevic V, Schone C, Heine M, Gundelfinger ED, Fejtova A, (2011) Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J Neurosci 31: 10189-10200
37. Leal-Ortiz S, Waites CL, Terry-Lorenzo R, Zamorano P, Gundelfinger ED, Garner CC, (2008) Piccolo modulation of Synapsin1a dynamics regulates synaptic vesicle exocytosis. J Cell Biol 181: 831-846
38. Lin X, Sun B, Liang M, Liang YY, Gast A, Hildebrand J, Brunicardi FC, Melchior F, Feng XH, (2003) Opposed regulation of corepressor CtBP by SUMOylation and PDZ binding. Mol Cell 11: 1389-1396
39. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D, (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295: 868-872
40. Mihaly A, Joo F, Szente M, (1983) Neuropathological alterations in the neocortex of rats subjected to focal aminopyridine seizures. Acta Neuropathol 61: 85-94
41. Mukherjee K, Yang X, Gerber SH, Kwon HB, Ho A, Castillo PE, Liu X, Sudhof TC, (2010) Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc Natl Acad Sci USA 107: 6504-6509
42. Nagy A, Moens C, Ivanyi E, Pawling J, Gertsenstein M, Hadjantonakis AK, Pirity M, Rossant J, (1998) Dissecting the role of N-myc in development using a single targeting vector to generate a series of alleles. Curr Biol 8: 661-664
43. Nardini M, Spano S, Cericola C, Pesce A, Massaro A, Millo E, Luini A, Corda D, Bolognesi M, (2003) CtBP/BARS: a dual-function protein involved in transcription co-repression and Golgi membrane fission. EMBO J 22: 3122-3130
44. Patterson GH, Lippincott-Schwartz J, (2002) A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297: 1873-1877
45. Quinlan KG, Verger A, Kwok A, Lee SH, Perdomo J, Nardini M, Bolognesi M, Crossley M, (2006) Role of the C-terminal binding protein PXDLS motif binding cleft in protein interactions and transcriptional repression. Mol Cell Biol 26: 8202-8213
46. Riefler GM, Firestein BL, (2001) Binding of neuronal nitric-oxide synthase (nNOS) to carboxyl-terminal-binding protein (CtBP) changes the localization of CtBP from the nucleus to the cytosol: a novel function for targeting by the PDZ domain of nNOS. J Biol Chem 276: 48262-48268
47. Rylski M, Amborska R, Zybura K, Mioduszewska B, Michaluk P, Jaworski J, Kaczmarek L, (2008) Yin Yang 1 is a critical repressor of matrix metalloproteinase-9 expression in brain neurons. J Biol Chem 283: 35140-35153
48. Schlumm F, Mauceri D, Freitag HE, Bading H, (2013) Nuclear calcium signaling regulates nuclear export of a subset of class IIa histone deacetylases following synaptic activity. J Biol Chem 288: 8074-8084
49. Schmitz F, Konigstorfer A, Sudhof TC, (2000) RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28: 857-872
50. Schroder MS, Stellmacher A, Romorini S, Marini C, Montenegro-Venegas C, Altrock WD, Gundelfinger ED, Fejtova A, (2013) Regulation of presynaptic anchoring of the scaffold protein Bassoon by phosphorylation-dependent interaction with 14-3-3 adaptor proteins. PLoS ONE 8: e58814
51. Soriano FX, Chawla S, Skehel P, Hardingham GE, (2013) SMRT-mediated co-shuttling enables export of class IIa HDACs independent of their CaM kinase phosphorylation sites. J Neurochem 124: 26-35
52. 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
53. Vaithianathan T, Akmentin W, Henry D, Matthews G, (2013) The ribbon-associated protein C-terminal-binding protein 1 is not essential for the structure and function of retinal ribbon synapses. Mol Vis 19: 917-926
54. Valente C, Luini A, Corda D, (2013) Components of the CtBP1/BARS-dependent fission machinery. Histochem Cell Biol 140: 407-421
55. Vashishta A, Habas A, Pruunsild P, Zheng JJ, Timmusk T, Hetman M, (2009) Nuclear factor of activated T-cells isoform c4 (NFATc4/NFAT3) as a mediator of antiapoptotic transcription in NMDA receptor-stimulated cortical neurons. J Neurosci 29: 15331-15340
56. Verger A, Quinlan KG, Crofts LA, Spano S, Corda D, Kable EP, Braet F, Crossley M, (2006) Mechanisms directing the nuclear localization of the CtBP family proteins. Mol Cell Biol 26: 4882-4894
57. Voskuyl RA, Albus H, (1985) Spontaneous epileptiform discharges in hippocampal slices induced by 4-aminopyridine. Brain Res 342: 54-66
58. Wiegert JS, Bengtson CP, Bading H, (2007) Diffusion and not active transport underlies and limits ERK1/2 synapse-to-nucleus signaling in hippocampal neurons. J Biol Chem 282: 29621-29633
59. Wu C, Ramirez A, Cui B, Ding J, Delcroix JD, Valletta JS, Liu JJ, Yang Y, Chu S, Mobley WC, (2007) A functional dynein-microtubule network is required for NGF signaling through the Rap1/MAPK pathway. Traffic 8: 1503-1520
60. Xiang G, Pan L, Xing W, Zhang L, Huang L, Yu J, Zhang R, Wu J, Cheng J, Zhou Y, (2007) Identification of activity-dependent gene expression profiles reveals specific subsets of genes induced by different routes of Ca(2 +) entry in cultured rat cortical neurons. J Cell Physiol 212: 126-136
61. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelfinger ED, Ziv NE, Garner CC, (2001) Assembling the presynaptic active zone: a characterization of an active one precursor vesicle. Neuron 29: 131-143
62. Zhang Q, Piston DW, Goodman RH, (2002) Regulation of corepressor function by nuclear NADH. Science 295: 1895-1897