Time-dependent changes in the mouse hippocampal synaptic membrane proteome after contextual fear conditioning

Hippocampus

Volumn 25, Issue 11, 2015, Pages 1250-1261

  Rao Ruiz, Priyanka ^a   Carney, Karen E ^a,b,c   Pandya, Nikhil ^a   Van der Loo, Rolinka J ^a   Verheijen, Mark H G ^a   Van Nierop, Pim ^a   Smit, August B ^a   Spijker, Sabine ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b INSTITUT FRANÇOIS MAGENDIE   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Hippocampus; ITRAQ; Memory; Proteomics; Stress

Indexed keywords

AMPHIPHYSIN; DYNAMIN; EXCITATORY AMINO ACID TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2; GABA TRANSPORTER 3; GLUTAMATE RECEPTOR; HIPPOCAMPAL SYNAPTIC MEMBRANE PROTEOME; MITOCHONDRIAL PROTEIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; PROTEOME; SCAFFOLD PROTEIN; SYNAPTOJANIN; UNCLASSIFIED DRUG;

ADULT; AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CONDITIONING; CONTROLLED STUDY; DORSAL HIPPOCAMPUS; ENDOCYTOSIS; FEAR; FOOTSHOCK; GLOBAL CHANGE; HIPPOCAMPUS; IMMEDIATE EARLY GENE; MALE; MEMORY CONSOLIDATION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STATE DEPENDENT LEARNING; STIMULUS RESPONSE; SYNAPSE; SYNAPTIC MEMBRANE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; MENTAL STRESS; METABOLISM; PHYSIOLOGY; TIME FACTOR;

ANIMALS; BEHAVIOR, ANIMAL; CONDITIONING (PSYCHOLOGY); FEAR; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; PROTEOME; STRESS, PSYCHOLOGICAL; SYNAPTIC MEMBRANES; TIME FACTORS;

EID: 84940072383     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22432     Document Type: Article

References (50)

1. Abel T, Lattal KM. 2001. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 11:180-187.
2. Andersson F, Jakobsson J, Löw P, Shupliakov O, Brodin L. 2008. Perturbation of syndapin/PACSIN impairs synaptic vesicle recycling evoked by intense stimulation. J Neurosci 28:3925-3933.
3. Biesemann C, Gronborg M, Luquet E, Wichert SP, Bernard V, Bungers SR, Cooper B, Varoqueaux F, Li L, Byrne JA, Urlaub H, Jahn O, Brose N, Herzog E. 2014. Proteomic screening of glutamatergic mouse brain synaptosomes isolated by fluorescence activated sorting. EMBO J 33:157-170.
4. Bourtchouladze R, Abel T, Berman N, Gordon R, Lapidus K, Kandel ER. 1998. Different training procedures recruit either one or two critical periods for contextual memory consolidation, each of which requires protein synthesis and PKA. Learn Mem 5:365-374.
5. Bushong EA, Martone ME, Jones YZ, Ellisman MH. 2002. Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22:183-192.
6. Cajigas IJ, Will T, Schuman EM. 2010. Protein homeostasis and synaptic plasticity. EMBO J 29:2746-2752.
7. Caroni P, Donato F, Muller D. 2012. Structural plasticity upon learning: Regulation and functions. Nat Rev Neurosci 13:478-490.
8. Chicurel ME, Terrian DM, Potter H. 1993. mRNA at the synapse: Analysis of a synaptosomal preparation enriched in hippocampal dendritic spines. J Neurosci 13:4054-4063.
9. Counotte DS, Li KW, Wortel J, Gouwenberg Y, Van Der Schors RC, Smit AB, Spijker S. 2010. Changes in molecular composition of rat medial prefrontal cortex synapses during adolescent development. Eur J Neurosci 32:1452-1460.
10. Cui Z, Feng R, Jacobs S, Duan Y, Wang H, Cao X, Tsien JZ. 2013. Increased NR2A:NR2B ratio compresses long-term depression range and constrains long-term memory. Sci Rep 3:1036.
11. Davis HP, Squire LR. 1984. Protein synthesis and memory: A review. Psychol Bull 96:518-559.
12. Fanselow MS. 1986. Associative vs topographical accounts of the immediate shock-freezing deficit in rats: Implications for the response selection rules governing species-specific defensive reactions. Learn Motiv 17:16-39.
13. Fanselow MS. 2000. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110:73-81.
14. Fonzo LS, Golini RS, Delgado SM, Ponce IT, Bonomi MR, Rezza IG, Gimenez MS, Anzulovich AC. 2009. Temporal patterns of lipoperoxidation and antioxidant enzymes are modified in the hippocampus of vitamin a-deficient rats. Hippocampus 19:869-880.
15. Frankland PW, Josselyn SA, Anagnostaras SG, Kogan JH, Takahashi E, Silva AJ. 2004. Consolidation of CS and US representations in associative fear conditioning. Hippocampus 14:557-569.
16. Freeman FM, Rose SP, Scholey AB. 1995. Two time windows of anisomycin-induced amnesia for passive avoidance training in the day-old chick. Neurobiol Learn Mem 63:291-295.
17. Goosens KA. 2011. Hippocampal regulation of aversive memories. Curr Opin Neurobiol 21:460-466.
18. Goudriaan A, de Leeuw C, Ripke S, Hultman CM, Sklar P, Sullivan PF, Smit AB, Posthuma D, Verheijen MH. 2014. Specific glial functions contribute to schizophrenia susceptibility. Schizophr Bull 40:925-935.
19. Halassa MM, Fellin T, Takano H, Dong JH, Haydon PG. 2007. Synaptic islands defined by the territory of a single astrocyte. J Neurosci 27:6473-6477.
20. Harbour VL, Weigl Y, Robinson B, Amir S. 2013. Comprehensive mapping of regional expression of the clock protein PERIOD2 in rat forebrain across the 24-h day. PLoS One 8:e76391.
21. Hernandez PJ, Abel T. 2008. The role of protein synthesis in memory consolidation: Progress amid decades of debate. Neurobiol Learn Mem 89:293-311.
22. Hoeffer CA, Klann E. 2010. mTOR signaling: At the crossroads of plasticity, memory and disease. Trends Neurosci 33:67-75.
23. Howland JG, Wang YT. 2008. Synaptic plasticity in learning and memory: Stress effects in the hippocampus. Prog Brain Res 169:145-158.
24. Huang CC, Yang CH, Hsu KS. 2005. Do stress and long-term potentiation share the same molecular mechanisms? Mol Neurobiol 32:223-235.
25. Hulme SR, Jones OD, Abraham WC. 2013. Emerging roles of metaplasticity in behaviour and disease. Trends Neurosci 36:353-362.
26. Kandel ER. 2001. The molecular biology of memory storage: A dialog between genes and synapses. Biosci Rep 21:565-611.
27. Karp NA, Huber W, Sadowski PG, Charles PD, Hester SV, Lilley KS. 2010. Addressing accuracy and precision issues in iTRAQ quantitation. Mol Cell Proteomics 9:1885-1897.
28. Kim JJ, Yoon KS. 1998. Stress: Metaplastic effects in the hippocampus. Trends Neurosci 21:505-509.
29. Koch D, Spiwoks-Becker I, Sabanov V, Sinning A, Dugladze T, Stellmacher A, Ahuja R, Grimm J, Schuler S Müller A, Angenstein F, Ahmed T, Diesler A, Moser M, Tom Dieck S, Spessert R, Boeckers TM, Fässler R, Hübner CA, Balschun D, Gloveli T, Kessels MM, Qualmann B. 2011. Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I. EMBO J 30:4955-6969.
30. Landeira-Fernandez J, DeCola JP, Kim JJ, Fanselow MS. 2006. Immediate shock deficit in fear conditioning: Effects of shock manipulations. Behav Neurosci 120:873-879.
31. Lattal KM, Abel T. 2001. An immediate-shock freezing deficit with discrete cues: A possible role for unconditioned stimulus processing mechanisms. J Exp Psychol Anim Behav Process 27:394-406.
32. Lips ES, Cornelisse LN, Toonen RF, Min JL, Hultman CM, Holmans PA, O'Donovan MC, Purcell SM, Smit AB, Verhage M, Sullivan PF, Visscher PM, Posthuma D. 2012. Functional gene group analysis identifies synaptic gene groups as risk factor for schizophrenia. Mol Psychiatry 17:996-1006.
33. Liu X, Ramirez S, Pang PT, Puryear CB, Govindarajan A, Deisseroth K, Tonegawa S. 2012. Optogenetic stimulation of a hippocampal engram activates fear memory recall. Nature 484:381-385.
34. Matsuo N, Reijmers L, Mayford M. 2008. Spine-type-specific recruitment of newly synthesized AMPA receptors with learning. Science 319:1104-1107.
35. McGaugh JL. 2000. Memory-A century of consolidation. Science 287:248-251.
36. Meyer-Arendt K, Old WM, Houel S, Renganathan K, Eichelberger B, Resing KA, Ahn NG. 2011. IsoformResolver: A peptide-centric algorithm for protein inference. J Proteome Res 10:3060-3075.
37. Modregger J, Ritter B, Witter B, Paulsson M, Plomann M. 2000. All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis. J Cell Sci 113 Pt 24:4511-4521.
38. Morgado-Bernal I. 2011. Learning and memory consolidation: Linking molecular and behavioral data. Neuroscience 176:12-19.
39. Oliet SH, Piet R, Poulain DA. 2001. Control of glutamate clearance and synaptic efficacy by glial coverage of neurons. Science 292:923-926.
40. Pannasch U, Freche D, Dallerac G, Ghezali G, Escartin C, Ezan P, Cohen-Salmon M, Benchenane K, Abudara V Dufour A, Lübke JH, Déglon N, Knott G, Holcman D, Rouach N. 2014. Connexin 30 sets synaptic strength by controlling astroglial synapse invasion. Nat Neurosci 17:549-558.
41. Pérez-Otaño I, Lujan R, Tavalin SJ, Plomann M, Modregger J, Liu XB, Jones EG, Heinemann SF, Lo DC, Ehlers MD. 2006. Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1. Nat Neurosci 9:611-621.
42. Quevedo J, Vianna MR, Roesler R, de-Paris F, Izquierdo I, Rose SP. 1999. Two time windows of anisomycin-induced amnesia for inhibitory avoidance training in rats: Protection from amnesia by pretraining but not pre-exposure to the task apparatus. Learn Mem 6:600-607.
43. Rao-Ruiz P, Rotaru DC, van der Loo RJ, Mansvelder HD, Stiedl O, Smit AB, Spijker S. 2011. Retrieval-specific endocytosis of GluA2-AMPARs underlies adaptive reconsolidation of contextual fear. Nat Neurosci 14:1302-1308.
44. Reiter L, Claassen M, Schrimpf SP, Jovanovic M, Schmidt A, Buhmann JM, Hengartner MO, Aebersold R. 2009. Protein identification false discovery rates for very large proteomics data sets generated by tandem mass spectrometry. Mol Cell Proteomics 8:2405-2417.
45. Ruano D, Abecasis GR, Glaser B, Lips ES, Cornelisse LN, de Jong AP, Evans DM, Davey Smith G, Timpson NJ, Smit AB, Heutink P, Verhage M, Posthuma D. 2010. Functional gene group analysis reveals a role of synaptic heterotrimeric G proteins in cognitive ability. Am J Hum Genet 86:113-125.
46. Shors TJ, Seib TB, Levine S, Thompson RF. 1989. Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244:224-226.
47. Sutton MA, Schuman EM. 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:49-58.
48. Van den Oever MC, Goriounova NA, Li KW, Van der Schors RC, Binnekade R, Schoffelmeer AN, Mansvelder HD, Smit AB, Spijker S, De Vries TJ. 2008. Prefrontal cortex AMPA receptor plasticity is crucial for cue-induced relapse to heroin-seeking. Nat Neurosci 11:1053-1058.
49. Végh MJ, de Waard MC, van der Pluijm I, Ridwan Y, Sassen MJ, van Nierop P, van der Schors RC, Li KW, Hoeijmakers JH, Smit AB, van Kesteren RE. 2012. Synaptic proteome changes in a DNA repair deficient ercc1 mouse model of accelerated aging. J Proteome Res 11:1855-1867.
50. Whitlock JR, Heynen AJ, Shuler MG, Bear MF. 2006. Learning induces long-term potentiation in the hippocampus. Science 313:1093-1097.