Expression, phosphorylation, and glycosylation of CNS proteins in aversive operant conditioning associated memory in Lymnaea stagnalis

Neuroscience

Volumn 186, Issue , 2011, Pages 94-109

  Silverman Gavrila, L B ^a   Senzel, A G ^a   Charlton, M P ^a   Feng, Z P ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Conditioned learning; Glycosylation; Long term memory; Phosphorylation; Protein expression; Proteomics

Indexed keywords

ACTIN; ASPARTIC ACID; CENTRAL NERVOUS SYSTEM PROTEIN; CHOLESTEROL; GLUTAMINE; GLYCOPROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; LIPOPROTEIN; NUCLEIC ACID; PHOSPHOPROTEIN; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AVERSIVE OPERANT CONDITIONING; CELL DIVISION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; ENERGY METABOLISM; GLYCOSYLATION; INSTRUMENTAL CONDITIONING; IRON TRANSPORT; LEARNING; LIPOPROTEIN METABOLISM; LONG TERM MEMORY; LYMNAEA; LYMNAEA STAGNALIS; MASS SPECTROMETRY; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEIC ACID SYNTHESIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEOMICS; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TWO DIMENSIONAL GEL ELECTROPHORESIS; UPREGULATION;

ANIMALS; AVOIDANCE LEARNING; CENTRAL NERVOUS SYSTEM; CONDITIONING, OPERANT; GLYCOSYLATION; LYMNAEA; MEMORY; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION;

EID: 79957984574     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.027     Document Type: Article

References (87)

1. Abel T., Lattal K.M. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr Opin Neurobiol 2001, 11:180-187.
2. Alberini C.M. Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 2009, 89:121-145.
3. Alberio T., Bossi A.M., Milli A., Parma E., Gariboldi M.B., Tosi G., Lopiano L., Fasano M. Proteomic analysis of dopamine and alpha-synuclein interplay in a cellular model of Parkinson's disease pathogenesis. FEBS J 2010, 277:4909-4919.
4. Antonov A.V., Dietmann S., Rodchenkov I., Mewes H.W. PPI spider: a tool for the interpretation of proteomics data in the context of protein-protein interaction networks. Proteomics 2009, 9:2740-2749.
5. Antonov I., Kandel E.R., Hawkins R.D. Presynaptic and postsynaptic mechanisms of synaptic plasticity and metaplasticity during intermediate-term memory formation in Aplysia. J Neurosci 2010, 30:5781-5791.
6. Bailey C.H., Bartsch D., Kandel E.R. Toward a molecular definition of long-term memory storage. Proc Natl Acad Sci U S A 1996, 93:13445-13452.
7. Ballif B.A., Villen J., Beausoleil S.A., Schwartz D., Gygi S.P. Phosphoproteomic analysis of the developing mouse brain. Mol Cell Proteomics 2004, 3:1093-1101.
8. Barco A., Pittenger C., Kandel E.R. CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert Opin Ther Targets 2003, 7:101-114.
9. Barrie A., Chieregatti E., Miloso M., Benfenati F., Valtorta F. Epidermal growth factor-mediated inhibition of neurotransmitter glutamate release from rat forebrain synaptosomes. Mol Pharmacol 1996, 49:399-403.
10. Bartsch D., Ghirardi M., Skehel P.A., Karl K.A., Herder S.P., Chen M., Bailey C.H., Kandel E.R. Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 1995, 83:979-992.
11. Bittins C.M., Eichler T.W., Hammer J.A., Gerdes H.H. Dominant-negative myosin Va impairs retrograde but not anterograde axonal transport of large dense core vesicles. Cell Mol Neurobiol 2010, 30:369-379.
12. Blackstone C., Murphy T.H., Moss S.J., Baraban J.M., Huganir R.L. Cyclic AMP and synaptic activity-dependent phosphorylation of AMPA-preferring glutamate receptors. J Neurosci 1994, 14:7585-7593.
13. Blain J.F., Poirier J. Cholesterol homeostasis and the pathophysiology of Alzheimer's disease. Expert Rev Neurother 2004, 4:823-829.
14. Burre J., Beckhaus T., Schagger H., Corvey C., Hofmann S., Karas M., Zimmermann H., Volknandt W. Analysis of the synaptic vesicle proteome using three gel-based protein separation techniques. Proteomics 2006, 6:6250-6262.
15. Canales J.J. Comparative neuroscience of stimulant-induced memory dysfunction: role for neurogenesis in the adult hippocampus. Behav Pharmacol 2010, 21:379-393.
16. Charriaut-Marlangue C., Pollard H., Kadri-Hassani N., Khrestchatisky M., Moreau J., Dessi F., Kang K.I., Ben-Ari Y. Increase in specific proteins and mRNAs following transient anoxia-Aglycaemia in rat CA1 hippocampal slices. Eur J Neurosci 1992, 4:766-776.
17. Cobb S.R., Pitt A. Proteomics in the study of hippocampal plasticity. Expert Rev Proteomics 2008, 5:393-404.
18. 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, 280:5972-5982.
19. DeGiorgis J.A., Jaffe H., Moreira J.E., Carlotti C.G., Leite J.P., Pant H.C., Dosemeci A. Phosphoproteomic analysis of synaptosomes from human cerebral cortex. J Proteome Res 2005, 4:306-315.
20. Ding Q., Vaynman S., Souda P., Whitelegge J.P., Gomez-Pinilla F. Exercise affects energy metabolism and neural plasticity-related proteins in the hippocampus as revealed by proteomic analysis. Eur J Neurosci 2006, 24:1265-1276.
21. Dominguez J., Ordonez L.A. Developmental changes in the folate-dependent enzymes of de novo purine biosynthesis in rat brain. J Neurochem 1982, 38:625-630.
22. Evans G.J., Pocock J.M. Modulation of neurotransmitter release by dihydropyridine-sensitive calcium channels involves tyrosine phosphorylation. Eur J Neurosci 1999, 11:279-292.
23. Farah C.A., Weatherill D., Dunn T.W., Sossin W.S. PKC differentially translocates during spaced and massed training in Aplysia. J Neurosci 2009, 29:10281-10286.
24. Fei G., Guo C., Sun H.S., Feng Z.P. Chronic hypoxia stress-induced differential modulation of heat-shock protein 70 and presynaptic proteins. J Neurochem 2007, 100:50-61.
25. Fioravante D., Smolen P.D., Byrne J.H. The 5-HT- and FMRFa-activated signaling pathways interact at the level of the Erk MAPK cascade: potential inhibitory constraints on memory formation. Neurosci Lett 2006, 396:235-240.
26. Frank D.A., Greenberg M.E. CREB: a mediator of long-term memory from mollusks to mammals. Cell 1994, 79:5-8.
27. Furuhashi K. Involvement of actin dephosphorylation in germination of Physarum sclerotium. J Eukaryot Microbiol 2002, 49:129-133.
28. Gardzinski P., Lee D.W., Fei G.H., Hui K., Huang G.J., Sun H.S., Feng Z.P. The role of synaptotagmin I C2A calcium-binding domain in synaptic vesicle clustering during synapse formation. J Physiol 2007, 581:75-90.
29. Genoud S., Pralong W., Riederer B.M., Eder L., Catsicas S., Muller D. Activity-dependent phosphorylation of SNAP-25 in hippocampal organotypic cultures. J Neurochem 1999, 72:1699-1706.
30. Gillardon F., Schrattenholz A., Sommer B. Investigating the neuroprotective mechanism of action of a CDK5 inhibitor by phosphoproteome analysis. J Cell Biochem 2005, 95:817-826.
31. Grant S.G., Husi H. Proteomics of multiprotein complexes: answering fundamental questions in neuroscience. Trends Biotechnol 2001, 19:S49-S54.
32. Guo C.H., Senzel A., Li K., Feng Z.P. De novo protein synthesis of syntaxin-1 and dynamin-1 in long-term memory formation requires CREB1 gene transcription in Lymnaea stagnalis. Behav Genet 2010, 40:680-693.
33. Hargreaves G.A., Quinn H., Kashem M.A., Matsumoto I., McGregor I.S. Proteomic analysis demonstrates adolescent vulnerability to lasting hippocampal changes following chronic alcohol consumption. Alcohol Clin Exp Res 2009, 33:86-94.
34. Hassel B. Carboxylation and anaplerosis in neurons and glia. Mol Neurobiol 2000, 22:21-40.
35. Hirling H., Scheller R.H. Phosphorylation of synaptic vesicle proteins: modulation of the alpha SNAP interaction with the core complex. Proc Natl Acad Sci U S A 1996, 93:11945-11949.
36. Hooghe-Peters E.L. Autoradiographic study of proline incorporation into cerebral proteins. The influence of learning and of asparaginase administration. Acta Neurol Belg 1975, 75:143-150. (author's transl).
37. Hooghe-Peters E.L. A new inhibitor of long-term memory. Acta Neurol Belg 1973, 73:395-401. (author's transl).
38. Houeland G., Nakhost A., Sossin W.S., Castellucci V.F. PKC modulation of transmitter release by SNAP-25 at sensory-to-motor synapses in Aplysia. J Neurophysiol 2007, 97:134-143.
39. Kaang B.K., Kandel E.R., Grant S.G. Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons. Neuron 1993, 10:427-435.
40. Kandel E.R. Genes, synapses, and long-term memory. J Cell Physiol 1997, 173:124-125.
41. Kemenes G., Benjamin P.R. Lymnaea. Curr Biol 2009, 19:R9-R11.
42. Kemenes G., Kemenes I., Michel M., Papp A., Muller U. Phase-dependent molecular requirements for memory reconsolidation: differential roles for protein synthesis and protein kinase A activity. J Neurosci 2006, 26:6298-6302.
43. Khidekel N., Ficarro S.B., Clark P.M., Bryan M.C., Swaney D.L., Rexach J.E., Sun Y.E., Coon J.J., Peters E.C., Hsieh-Wilson L.C. Probing the dynamics of O-GlcNAc glycosylation in the brain using quantitative proteomics. Nat Chem Biol 2007, 3:339-348.
44. Khidekel N., Ficarro S.B., Clark P.M., Bryan M.C., Swaney D.L., Rexach J.E., Sun Y.E., Coon J.J., Peters E.C., Hsieh-Wilson L.C. Probing the dynamics of O-GlcNAc glycosylation in the brain using quantitative proteomics. Nat Chem Biol 2007, 3:339-348.
45. Khidekel N., Hsieh-Wilson L.C. A 'molecular switchboard'-covalent modifications to proteins and their impact on transcription. Org Biomol Chem 2004, 2:1-7.
46. Kimura R., Matsuki N. Protein kinase CK2 modulates synaptic plasticity by modification of synaptic NMDA receptors in the hippocampus. J Physiol 2008, 586:3195-3206.
47. Kubo T., Endo M., Hata K., Taniguchi J., Kitajo K., Tomura S., Yamaguchi A., Mueller B.K., Yamashita T. Myosin IIA is required for neurite outgrowth inhibition produced by repulsive guidance molecule. J Neurochem 2008, 105:113-126.
48. Kuhl D., Kennedy T.E., Barzilai A., Kandel E.R. Long-term sensitization training in Aplysia leads to an increase in the expression of BiP, the major protein chaperon of the ER. J Cell Biol 1992, 119:1069-1076.
49. Lalonde R., Strazielle C. The effects of cerebellar damage on maze learning in animals. Cerebellum 2003, 2:300-309.
50. Lukowiak K., Martens K., Orr M., Parvez K., Rosenegger D., Sangha S. Modulation of aerial respiratory behaviour in a pond snail. Respir Physiol Neurobiol 2006, 154:61-72.
51. Lukowiak K., Ringseis E., Spencer G., Wildering W., Syed N. Operant conditioning of aerial respiratory behaviour in Lymnaea stagnalis. J Exp Biol 1996, 199:683-691.
52. Martins-de-Souza D., Gattaz W.F., Schmitt A., Novello J.C., Marangoni S., Turck C.W., Dias-Neto E. Proteome analysis of schizophrenia patients Wernicke's area reveals an energy metabolism dysregulation. BMC Psychiatry 2009, 9:17.
53. Matthies H., Kretlow J., Matthies H., Smalla K.H., Staak S., Krug M. Glycosylation of proteins during a critical time window is necessary for the maintenance of long-term potentiation in the hippocampal CA1 region. Neuroscience 1999, 91:175-183.
54. Mayford M., Kandel E.R. Genetic approaches to memory storage. Trends Genet 1999, 15:463-470.
55. McNair K., Davies C.H., Cobb S.R. Plasticity-related regulation of the hippocampal proteome. Eur J Neurosci 2006, 23:575-580.
56. Merlo E., Romano A. Long-term memory consolidation depends on proteasome activity in the crab Chasmagnathus. Neuroscience 2007, 147:46-52.
57. Morales M., Colicos M.A., Goda Y. Actin-dependent regulation of neurotransmitter release at central synapses. Neuron 2000, 27:539-550.
58. Morley J.E., Banks W.A. Lipids and cognition. J Alzheimers Dis 2010, 20:737-747.
59. O'Sullivan N.C., McGettigan P.A., Sheridan G.K., Pickering M., Conboy L., O'Connor J.J., Moynagh P.N., Higgins D.G., Regan C.M., Murphy K.J. Temporal change in gene expression in the rat dentate gyrus following passive avoidance learning. J Neurochem 2007, 101:1085-1098.
60. Okumura N., Okada M., Nakagawa H. Depolarization-induced tyrosine phosphorylation in PC12h cells. J Biochem 1994, 116:346-350.
61. Owen J.B., Di D.F., Sultana R., Perluigi M., Cini C., Pierce W.M., Butterfield D.A. Proteomics-determined differences in the concanavalin-A-fractionated proteome of hippocampus and inferior parietal lobule in subjects with Alzheimer's disease and mild cognitive impairment: implications for progression of AD. J Proteome Res 2009, 8:471-482.
62. Parvez K., Stewart O., Sangha S., Lukowiak K. Boosting intermediate-term into long-term memory. J Exp Biol 2005, 208:1525-1536.
63. Pittenger C., Kandel E.R. In search of general mechanisms for long-lasting plasticity: Aplysia and the hippocampus. Philos Trans R Soc Lond B Biol Sci 2003, 358:757-763.
64. Ribeiro M.J., Schofield M.G., Kemenes I., O'Shea M., Kemenes G., Benjamin P.R. Activation of MAPK is necessary for long-term memory consolidation following food-reward conditioning. Learn Mem 2005, 12:538-545.
65. Rivera A., Agnati L.F., Horvath T.L., Valderrama J.J., de La C.A., Fuxe K. Uncoupling protein 2/3 immunoreactivity and the ascending dopaminergic and noradrenergic neuronal systems: relevance for volume transmission. Neuroscience 2006, 137:1447-1461.
66. Rosenegger D., Parvez K., Lukowiak K. Enhancing memory formation by altering protein phosphorylation balance. Neurobiol Learn Mem 2008, 90:544-552.
67. Rosenegger D., Wright C., Lukowiak K. A quantitative proteomic analysis of long-term memory. Mol Brain 2010, 3:9.
68. Sadamoto H., Azami S., Ito E. The expression pattern of CREB genes in the central nervous system of the pond snail Lymnaea stagnalis. Acta Biol Hung 2004, 55:163-166.
69. Sangha S., Scheibenstock A., Morrow R., Lukowiak K. Extinction requires new RNA and protein synthesis and the soma of the cell right pedal dorsal 1 in Lymnaea stagnalis. J Neurosci 2003, 23:9842-9851.
70. Sharma S.K., Sherff C.M., Stough S., Hsuan V., Carew T.J. A tropomyosin-related kinase B ligand is required for ERK activation, long-term synaptic facilitation, and long-term memory in Aplysia. Proc Natl Acad Sci U S A 2006, 103:14206-14210.
71. Siciliano J.C., Gelman M., Girault J.A. Depolarization and neurotransmitters increase neuronal protein tyrosine phosphorylation. J Neurochem 1994, 62:950-959.
72. Silverman-Gavrila L.B., Charlton M.P. Calcineurin and cytoskeleton in low-frequency depression. J Neurochem 2009, 109:716-732.
73. Silverman-Gavrila L.B., Lu T.Z., Prashad R.C., Nejatbakhsh N., Charlton M.P., Feng Z.P. Neural phosphoproteomics of a chronic hypoxia model-Lymnaea stagnalis. Neuroscience 2009, 161:621-634.
74. Silverman-Gavrila L.B., Orth P.M., Charlton M.P. Phosphorylation-dependent low-frequency depression at phasic synapses of a crayfish motoneuron. J Neurosci 2005, 25:3168-3180.
75. Silverman-Gavrila LB, Senzel A, Feng Z-P (2009) Proteomics of operant conditioning: analysis of CNS proteins in a Lymnaea learning model. Society for Neuroscience 39th Annual Meeting, Chicago, IL, October 17-21, program number 889. 8 109:716-732.
76. Spencer G.E., Syed N.I., Lukowiak K. Neural changes after operant conditioning of the aerial respiratory behavior in Lymnaea stagnalis. J Neurosci 1999, 19:1836-1843.
77. Sun Y., Monje F.J., Pollak D.D., Lubec G. A first partial Aplysia californica proteome. Amino Acids 2010.
78. Sweatt J.D. Mitogen-activated protein kinases in synaptic plasticity and memory. Curr Opin Neurobiol 2004, 14:311-317.
79. Syed N.I., Bulloch A.G., Lukowiak K. In vitro reconstruction of the respiratory central pattern generator of the mollusk Lymnaea. Science 1990, 250:282-285.
80. T'jampens D., Bailey J., Cook L.J., Constantin B., Vandekerckhove J., Gettemans J. Physarum amoebae express a distinct fragmin-like actin-binding protein that controls in vitro phosphorylation of actin by the actin-fragmin kinase. Eur J Biochem 1999, 265:240-250.
81. Trinidad J.C., Thalhammer A., Specht C.G., Schoepfer R., Burlingame A.L. Phosphorylation state of postsynaptic density proteins. J Neurochem 2005, 92:1306-1316.
82. Vandekerckhove J., Weber K. The amino acid sequence of Physarum actin. Nature 1978, 276:720-721.
83. Wang Y., Meriin A.B., Zaarur N., Romanova N.V., Chernoff Y.O., Costello C.E., Sherman M.Y. Abnormal proteins can form aggresome in yeast: aggresome-targeting signals and components of the machinery. FASEB J 2009, 23:451-463.
84. Wang Y.E., Esbensen P., Bentley D. Arginine kinase expression and localization in growth cone migration. J Neurosci 1998, 18:987-998.
85. Woodrow S., Bissoon N., Gurd J.W. Depolarization-dependent tyrosine phosphorylation in rat brain synaptosomes. J Neurochem 1992, 59:857-862.
86. Yin J.C., Tully T. CREB and the formation of long-term memory. Curr Opin Neurobiol 1996, 6:264-268.
87. Zubay G. Glycoproteins. Biochemistry 1983, 23:151. Wm. C. Brown Publishers, 451-463. K. Kane (Ed.).