Changes in the proteome after neuronal Zif268 overexpression

Journal of Proteome Research

Volumn 8, Issue 7, 2009, Pages 3298-3316

  Baumgärtel, Karsten ^a,c   Tweedie Cullen, Ry Y ^a   Grossmann, Jonas ^b   Gehrig, Peter ^b   Livingstone Zatchej, Magdalena ^a   Mansuy, Isabelle M ^a  

^a University of Zurich Brain Research Institute   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Bioinformatics; Egr 1; iTRAQ; Mass spectrometry; Neuronal plasticity; Zif268

Indexed keywords

MEMBRANE PROTEIN; METAL ION; PROTEIN ZIF268; PROTEOME; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIVISION; CONTROLLED STUDY; GENE OVEREXPRESSION; IMMEDIATE EARLY GENE; LONG TERM MEMORY; MALE; MASS SPECTROMETRY; METABOLISM; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; SENSORY NERVE;

ANIMALS; BRAIN; CELL NUCLEUS; COMPUTATIONAL BIOLOGY; CYTOPLASM; EARLY GROWTH RESPONSE PROTEIN 1; GENE EXPRESSION REGULATION; IONS; MALE; MASS SPECTROMETRY; METALS; MICE; MICE, TRANSGENIC; NEURONAL PLASTICITY; PROTEOMICS;

EID: 67650355059     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr801000r     Document Type: Article

References (55)

1. Hyman, S. E.; Malenka, R. C.; Nestler, E. J. Neural mechanisms of addiction: the role of reward-related learning and memory. Annu. Rev. Neurosci. 2006, 29, 565-98.
2. Schulman, H. Protein phosphorylation in neuronal plasticity and gene expression. Curr. Opin. Neurobiol. 1995, 5 (3), 375-81.
3. McClung, C. A.; Nestler, E. J. Neuroplasticity mediated by altered gene expression. Neuropsychopharmacology 2008, 33 (1), 3-17.
4. Baumgartel, K.; Fernandez, C.; Johansson, T.; Mansuy, I. M. Conditional transgenesis and recombination to study the molecular mechanisms of brain plasticity and memory. Handb. Exp. Pharmacol. 2007, (178), 315-45.
5. Trinidad, J. C.; Thalhammer, A.; Specht, C. G.; Lynn, A. J.; Baker, P. R.; Schoepfer, R.; Burlingame, A. L. Quantitative analysis of synaptic phosphorylation and protein expression. Mol. Cell. Proteomics 2008, 7 (4), 684-96.
6. Munton, R. P.; Tweedie-Cullen, R.; Livingstone-Zatchej, M.; Weinandy, F.; Waidelich, M.; Longo, D.; Gehrig, P.; Potthast, F.; Rutishauser, D.; Gerrits, B.; Panse, C.; Schlapbach, R.; Mansuy, I. M. Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol. Cell. Proteomics 2007, 6 (2), 283-93.
7. Collins, M. O.; Yu, L.; Coba, M. P.; Husi, H.; Campuzano, I.; Blackstock, W. P.; Choudhary, J. S.; Grant, S. G. Proteomic analysis of in vivo phosphorylated synaptic proteins. J. Biol. Chem. 2005, 280 (7), 5972-82.
8. Tweedie-Cullen, R. Y.; Livingstone-Zatchej, M.; Wollscheid, B.; Mansuy, I. M. Neuroproteomics and the detection of regulatory phosphosites. Curr. Proteomics 2007, 4 (4), 209-22.
9. Lanahan, A.; Worley, P. Immediate-early genes and synaptic function. Neurobiol. Learn. Mem. 1998, 70 (1-2), 37-43.
10. Fleischmann, A.; Hvalby, O.; Jensen, V.; Strekalova, T.; Zacher, C.; Layer, L. E.; Kvello, A.; Reschke, M.; Spanagel, R.; Sprengel, R.; Wagner, E. F.; Gass, P. Impaired long-term memory and NR2A-type NMDA receptor-dependent synaptic plasticity in mice lacking c-Fos in the CNS. J. Neurosci. 2003, 23 (27), 9116-22.
11. Jones, M. W.; Errington, M. L.; French, P. J.; Fine, A.; Bliss, T. V.; Garel, S.; Charnay, P.; Bozon, B.; Laroche, S.; Davis, S. A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat. Neurosci. 2001, 4 (3), 289-96.
12. Lee, J. L. Memory reconsolidation mediates the strengthening of memories by additional learning. Nat. Neurosci. 2008, 11 (11), 1264-6.
13. Rudy, J. W. Destroying memories to strengthen them. Nat. Neurosci. 2008, 11 (11), 1241-2.
14. Baumgartel, K.; Genoux, D.; Welzl, H.; Tweedie-Cullen, R. Y.; Koshibu, K.; Livingstone-Zatchej, M.; Mamie, C.; Mansuy, I. M. Control of the establishment of aversive memory by calcineurin and Zif268. Nat. Neurosci. 2008, 11 (5), 572-8.
15. Malkani, S.; Wallace, K. J.; Donley, M. P.; Rosen, J. B. An egr-1 (zif268) antisense oligodeoxynucleotide infused into the amygdala disrupts fear conditioning. Learn. Mem. 2004, 11 (5), 617-24.
16. Lee, J. L.; Everitt, B. J.; Thomas, K. L. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 2004, 304 (5672), 839-43.
17. Valjent, E.; Aubier, B.; Corbille, A. G.; Brami-Cherrier, K.; Caboche, J.; Topilko, P.; Girault, J. A.; Herve, D. Plasticity-associated gene Krox24/Zif268 is required for long-lasting behavioral effects of cocaine. J. Neurosci. 2006, 26 (18), 4956-60.
18. Olsson, A.; Phelps, E. A. Social learning of fear. Nat. Neurosci. 2007, 10 (9), 1095-102.
19. Liberzon, I.; Britton, J. C.; Phan, K. L. Neural correlates of traumatic recall in posttraumatic stress disorder. Stress 2003, 6 (3), 151-6.
20. Adinoff, B. Neurobiologic processes in drug reward and addiction. Harv. Rev. Psychiatry 2004, 12 (6), 305-20.
21. Koob, G. F. Neuroadaptive mechanisms of addiction: studies on the extended amygdala. Eur. Neuropsychopharmacol. 2003, 13 (6), 442-52.
22. Olsen, J. V.; Ong, S. E.; Mann, M. Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 2004, 3 (6), 608-14.
23. Peng, J.; Elias, J. E.; Thoreen, C. C.; Licklider, L. J.; Gygi, S. P. Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. J. Proteome Res. 2003, 2 (1), 43-50.
24. Zhang, B.; Schmoyer, D.; Kirov, S.; Snoddy, J. GOTree Machine (GOTM): a web-based platform for interpreting sets of interesting genes using Gene Ontology hierarchies. BMC Bioinformatics 2004, 5, 16.
25. Quandt, K.; Frech, K.; Karas, H.; Wingender, E.; Werner, T. MatInd and MatInspector: new fast and versatile tools for detection of consensus matches in nucleotide sequence data. Nucleic Acids Res. 1995, 23 (23), 4878-84.
26. Michalon, A.; Koshibu, K.; Baumgartel, K.; Spirig, D. H.; Mansuy, I. M. Inducible and neuron-specific gene expression in the adult mouse brain with the rtTA2S-M2 system. Genesis 2005, 43 (4), 205-12.
27. Guzowski, J. F.; Setlow, B.; Wagner, E. K.; McGaugh, J. L. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 2001, 21 (14), 5089-98.
28. Mokin, M.; Keifer, J. Expression of the immediate-early gene-encoded protein Egr-1 (zif268) during in vitro classical conditioning. Learn Mem 2005, 12 (2), 144-9.
29. Aicher, W. K.; Alexander, D.; Haas, C.; Kuchen, S.; Pagenstecher, A.; Gay, S.; Peter, H. H.; Eibel, H. Transcription factor early growth response 1 activity up-regulates expression of tissue inhibitor of metalloproteinases 1 in human synovial fibroblasts. Arthritis Rheum 2003, 48 (2), 348-59.
30. Baron, V.; Adamson, E. D.; Calogero, A.; Ragona, G.; Mercola, D. The transcription factor Egr1 is a direct regulator of multiple tumor suppressors including TGFbeta1, PTEN, p53, and fibronectin. Cancer Gene Ther. 2006, 13 (2), 115-24.
31. Gosslar, U.; Schmid, R. M.; Holzmann, B. Regulation of Egr-1-dependent gene expression by the C-terminal activation domain. Biochem. Biophys. Res. Commun. 1999, 255 (2), 208-15.
32. Zhang, X.; Liu, Y. Suppression of HGF receptor gene expression by oxidative stress is mediated through the interplay between Sp1 and Egr-1. Am. J. Physiol. Renal Physiol. 2003, 284 (6), F1216-25.
33. Lomax, J. Get ready to GO! A biologist's guide to the Gene Ontology. Brief Bioinform. 2005, 6 (3), 298-304.
34. James, A. B.; Conway, A. M.; Morris, B. J. Regulation of the neuronal proteasome by Zif268 (Egr1). J. Neurosci. 2006, 26 (5), 1624-34.
35. Conway, A. M.; James, A. B.; Zang, J.; Morris, B. J. Regulation of neuronal cdc20 (p55cdc) expression by the plasticity-related transcription factor zif268. Synapse 2007, 61 (6), 463-8.
36. Christy, B.; Nathans, D. DNA binding site of the growth factor-inducible protein Zif268. Proc. Natl. Acad. Sci. U.S.A. 1989, 86 (22), 8737-41.
37. Lemaire, P.; Vesque, C.; Schmitt, J.; Stunnenberg, H.; Frank, R.; Charnay, P. The serum-inducible mouse gene Krox-24 encodes a sequence-specific transcriptional activator. Mol. Cell. Biol. 1990, 10 (7), 3456-67.
38. Cao, X.; Mahendran, R.; Guy, G. R.; Tan, Y. H. Detection and characterization of cellular EGR-1 binding to its recognition site. J. Biol. Chem. 1993, 268 (23), 16949-57.
39. Meng, Z.; Camalier, C. E.; Lucas, D. A.; Veenstra, T. D.; Beck, G. R., Jr.; Conrads, T. P. Probing early growth response 1 interacting proteins at the active promoter in osteoblast cells using oligoprecipitation and mass spectrometry. J. Proteome Res. 2006, 5 (8), 1931-9.
40. Hamilton, T. B.; Borel, F.; Romaniuk, P. J. Comparison of the DNA binding characteristics of the related zinc finger proteins WT1 and EGR1. Biochemistry 1998, 37 (7), 2051-8.
41. Pfenning, A. R.; Schwartz, R.; Barth, A. L. A comparative genomics approach to identifying the plasticity transcriptome. BMC Neurosci. 2007, 8, 20.
42. Russo, M. W.; Sevetson, B. R.; Milbrandt, J. Identification of NAB1, a repressor of NGFI-A- and Krox20-mediated transcription. Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (15), 6873-7.
43. Svaren, J.; Sevetson, B. R.; Apel, E. D.; Zimonjic, D. B.; Popescu, N. C.; Milbrandt, J. NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol. Cell. Biol. 1996, 16 (7), 3545-53.
44. Ehlers, M. D. Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat. Neurosci. 2003, 6 (3), 231-42.
45. Fonseca, R.; Vabulas, R. M.; Hartl, F. U.; Bonhoeffer, T.; Nagerl, U. V. A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 2006, 52 (2), 239-45.
46. Lee, S. H.; Choi, J. H.; Lee, N.; Lee, H. R.; Kim, J. I.; Yu, N. K.; Choi, S. L.; Lee, S. H.; Kim, H.; Kaang, B. K. Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 2008, 319 (5867), 1253-6.
47. Artinian, J.; McGauran, A. M.; De Jaeger, X.; Mouledous, L.; Frances, B.; Roullet, P. Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation. Eur. J. Neurosci. 2008, 27 (11), 3009-19.
48. Chaudhuri, A.; Zangenehpour, S.; Rahbar-Dehgan, F.; Ye, F. Molecular maps of neural activity and quiescence. Acta Neurobiol. Exp. (Wars) 2000, 60 (3), 403-10.
49. Kaplan, I. V.; Guo, Y.; Mower, G. D. Developmental expression of the immediate early gene EGR-1 mirrors the critical period in cat visual cortex. Brain Res. Dev. Brain Res. 1995, 90 (1-2), 174-9.
50. Yau, J. L.; Olsson, T.; Morris, R. G.; Noble, J.; Seckl, J. R. Decreased NGFI-A gene expression in the hippocampus of cognitively impaired aged rats. Brain Res. Mol. Brain Res. 1996, 42 (2), 354-7.
51. Toscano, C. D.; McGlothan, J. L.; Guilarte, T. R. Experience-dependent regulation of zif268 gene expression and spatial learning. Exp. Neurol. 2006, 200 (1), 209-15.
52. Bekinschtein, P.; Cammarota, M.; Igaz, L. M.; Bevilaqua, L. R.; Izquierdo, I.; Medina, J. H. Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus. Neuron 2007, 53 (2), 261-77.
53. Yu, J.; de Belle, I.; Liang, H.; Adamson, E. D. Coactivating factors p300 and CBP are transcriptionally crossregulated by Egr1 in prostate cells, leading to divergent responses. Mol. Cell 2004, 15 (1), 83-94.
54. Gygi, S. P.; Rochon, Y.; Franza, B. R.; Aebersold, R. Correlation between protein and mRNA abundance in yeast. Mol. Cell. Biol. 1999, 19 (3), 1720-30.
55. Bramham, C. R.; Wells, D. G. Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 2007, 8 (10), 776-89.