Short-term memory formation and long-term memory consolidation are enhanced by cellular prion association to stress-inducible protein 1

Neurobiology of Disease

Volumn 26, Issue 1, 2007, Pages 282-290

  Coitinho, Adriana S ^a   Lopes, Marilene H ^b,c   Hajj, Glaucia N M ^b   Rossato, Janine I ^d   Freitas, Adriana R ^b   Castro, Cibele C ^d   Cammarota, Martin ^e   Brentani, Ricardo R ^c,f   Izquierdo, Ivan ^e   Martins, Vilma R ^b  

^a UNIVERSIDADE FEEVALE   (Brazil)

^b HOSPITAL ALEMÃO OSWALDO CRUZ   (Brazil)

^c A C CAMARGO CANCER CENTER   (Brazil)

^d FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^e PONTIFICAL CATHOLIC UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^f UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Cellular prion protein; Learning; Memory; STI1

Indexed keywords

BINDING PROTEIN; CELL PRION PROTEIN; LAMININ; LIGAND; NERVE CELL ADHESION MOLECULE; PRION PROTEIN; STRESS INDUCIBLE PROTEIN 1 [230-245]; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING SITE; CELL ADHESION; CELL DIFFERENTIATION; CELL PROTECTION; CONTROLLED STUDY; DISEASE MODEL; LEARNING; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; SHORT TERM MEMORY;

ANIMALS; AVOIDANCE LEARNING; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; HEAT-SHOCK PROTEINS; HIPPOCAMPUS; INDICATORS AND REAGENTS; MALE; MEMORY; MEMORY, SHORT-TERM; NEURONAL PLASTICITY; PRPC PROTEINS; PSYCHOMOTOR PERFORMANCE; RATS; RATS, WISTAR; SYNAPSES;

EID: 33947214890     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2007.01.005     Document Type: Article

References (74)

1. Adler R., Jerdan J., and Hewitt A.T. Responses of cultured neural retinal cells to substratum-bound laminin and other extracellular matrix molecules. Dev. Biol. 112 (1985) 100-114
2. Aguzzi A., and Polymenidou M. Mammalian prion biology: one century of evolving concepts. Cell 116 (2004) 313-327
3. Ambrosini M.V., Mariucci G., Tantucci M., Van Hooijdonk L., and Ammassari-Teule M. Hippocampal 72-kDa heat shock protein expression varies according to mice learning performance independently from chronic exposure to stress. Hippocampus 15 (2005) 413-417
4. Arami S., Jucker M., Schachner M., and Welzl H. The effect of continuous intraventricular infusion of L1 and NCAM antibodies on spatial learning in rats. Behav. Brain Res. 81 (1996) 81-87
5. Aumailley M., and Smyth N. The role of laminins in basement membrane function. J. Anat. 193 Pt. 1 (1998) 1-21
6. Baldwin T.J., Fazeli M.S., Doherty P., and Walsh F.S. Elucidation of the molecular actions of NCAM and structurally related cell adhesion molecules. J. Cell. Biochem. 61 (1996) 502-513
7. Banbury Conference, 1997. Mutant mice and neuroscience: recommendations concerning genetic background. Banbury Conference on genetic background in mice1. Neuron 19, 755-759
8. Bernabeu R., Bevilaqua L., Ardenghi P., Bromberg E., Schmitz P., Bianchin M., Izquierdo I., and Medina J.H. Involvement of hippocampal cAMP/cAMP-dependent protein kinase signaling pathways in a late memory consolidation phase of aversively motivated learning in rats. Proc. Natl. Acad. Sci. U. S. A. 94 (1997) 7041-7046
9. Berr C., Richard F., Dufouil C., Amant C., Alperovitch A., and Amouyel P. Polymorphism of the prion protein is associated with cognitive impairment in the elderly: the EVA study. Neurology 51 (1998) 734-737
10. Brown D.R. Prion and prejudice: normal protein and the synapse. Trends Neurosci. 24 (2001) 85-90
11. Bueler H., Fischer M., Lang Y., Bluethmann H., Lipp H.P., DeArmond S.J., Prusiner S.B., Aguet M., and Weissmann C. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356 (1992) 577-582
12. Cammarota M., Bevilaqua L.R., Medina J.H., and Izquierdo I. Retrieval does not induce reconsolidation of inhibitory avoidance memory. Learn. Mem. 11 (2004) 572-578
13. Cammarota M., Bevilaqua L.R., Barros D.M., Vianna M.R., Izquierdo L.A., Medina J.H., and Izquierdo I. Retrieval and the extinction of memory. Cell. Mol. Neurobiol. 25 (2005) 465-474
14. Cammarota M., Bevilaqua L.R., Rossato J.I., Ramirez M., Medina J.H., and Izquierdo I. Relationship between short- and long-term memory and short- and long-term extinction. Neurobiol. Learn. Mem. 84 (2005) 25-32
15. Carrigan P.E., Sikkink L.A., Smith D.F., and Ramirez-Alvarado M. Domain:domain interactions within Hop, the Hsp70/Hsp90 organizing protein, are required for protein stability and structure. Protein Sci. 15 (2006) 522-532
16. Chiarini L.B., Freitas A.R., Zanata S.M., Brentani R.R., Martins V.R., and Linden R. Cellular prion protein transduces neuroprotective signals. EMBO J. 21 (2002) 3317-3326
17. Cohen J., Burne J.F., Winter J., and Bartlett P. Retinal ganglion cells lose response to laminin with maturation. Nature 322 (1986) 465-467
18. Cohen J., Burne J.F., McKinlay C., and Winter J. The role of laminin and the laminin/fibronectin receptor complex in the outgrowth of retinal ganglion cell axons. Dev. Biol. 122 (1987) 407-418
19. Coitinho A.S., Roesler R., Martins V.R., Brentani R.R., and Izquierdo I. Cellular prion protein ablation impairs behavior as a function of age. NeuroReport 14 (2003) 1375-1379
20. Coitinho A., Freitas A., Lopes M., Hajj G., Roesler R., Walz R., Rossato J., Cammarota M., Izquierdo I., Martins V., and Brentani R. The interaction between prion protein and laminin modulates memory consolidation. Eur. J. Neurosci. 24 11 (2006) 3255-3264
21. Colognato H., and Yurchenco P.D. Form and function: the laminin family of heterotrimers. Dev. Dyn. 218 (2000) 213-234
22. Criado J.R., Sanchez-Alavez M., Conti B., Giacchino J.L., Wills D.N., Henriksen S.J., Race R., Manson J.C., Chesebro B., and Oldstone M.B. Mice devoid of prion protein have cognitive deficits that are rescued by reconstitution of PrP in neurons. Neurobiol. Dis. 19 (2005) 255-265
23. Cui T., Daniels M., Wong B.S., Li R., Sy M.S., Sassoon J., and Brown D.R. Mapping the functional domain of the prion protein. Eur. J. Biochem. 270 (2003) 3368-3376
24. Del Bo R., Comi G.P., Giorda R., Crimi M., Locatelli F., Martinelli-Boneschi F., Pozzoli U., Castelli E., Bresolin N., and Scarlato G. The 129 codon polymorphism of the prion protein gene influences earlier cognitive performance in Down syndrome subjects. J. Neurol. 250 (2003) 688-692
25. Doyle E., Nolan P.M., Bell R., and Regan C.M. Intraventricular infusions of anti-neural cell adhesion molecules in a discrete posttraining period impair consolidation of a passive avoidance response in the rat. J. Neurochem. 59 (1992) 1570-1573
26. Edgar D., Timpl R., and Thoenen H. Structural requirements for the stimulation of neurite outgrowth by two variants of laminin and their inhibition by antibodies. J. Cell Biol. 106 (1988) 1299-1306
27. Ettaiche M., Pichot R., Vincent J.P., and Chabry J. In vivo cytotoxicity of the prion protein fragment 106-126. J. Biol. Chem. 275 (2000) 36487-36490
28. Foley A.G., Hartz B.P., Gallagher H.C., Ronn L.C., Berezin V., Bock E., and Regan C.M. A synthetic peptide ligand of neural cell adhesion molecule (NCAM) IgI domain prevents NCAM internalization and disrupts passive avoidance learning. J. Neurochem. 74 (2000) 2607-2613
29. Forloni G., Angeretti N., Chiesa R., Monzani E., Salmona M., Bugiani O., and Tagliavini F. Neurotoxicity of a prion protein fragment. Nature 362 (1993) 543-546
30. Fournier J.G., Escaig-Haye F., Billette D.V., and Robain O. Ultrastructural localization of cellular prion protein (PrPc) in synaptic boutons of normal hamster hippocampus. C. R. Acad. Sci., Ser. III 318 (1995) 339-344
31. Gohel C., Grigoriev V., Escaig-Haye F., Lasmezas C.I., Deslys J.P., Langeveld J., Akaaboune M., Hantai D., and Fournier J.G. Ultrastructural localization of cellular prion protein (PrPc) at the neuromuscular junction. J. Neurosci. Res. 55 (1999) 261-267
32. Gold P.E. The use of avoidance training in studies of modulation of memory storage. Behav. Neural Biol. 46 (1986) 87-98
33. Graner E., Mercadante A.F., Zanata S.M., Forlenza O.V., Cabral A.L., Veiga S.S., Juliano M.A., Roesler R., Walz R., Minetti A., Izquierdo I., Martins V.R., and Brentani R.R. Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res. Mol. Brain Res. 76 (2000) 85-92
34. Graner E., Mercadante A.F., Zanata S.M., Martins V.R., Jay D.G., and Brentani R.R. Laminin-induced PC-12 cell differentiation is inhibited following laser inactivation of cellular prion protein. FEBS Lett. 482 (2000) 257-260
35. Herms J., Tings T., Gall S., Madlung A., Giese A., Siebert H., Schurmann P., Windl O., Brose N., and Kretzschmar H. Evidence of presynaptic location and function of the prion protein. J. Neurosci. 19 (1999) 8866-8875
36. Hernandez M.P., Sullivan W.P., and Toft D.O. The assembly and intermolecular properties of the hsp70-Hop-hsp90 molecular chaperone complex. J. Biol. Chem. 277 (2002) 38294-38304
37. Hetz C., Maundrell K., and Soto C. Is loss of function of the prion protein the cause of prion disorders?. Trends Mol. Med. 9 (2003) 237-243
38. Hung C.H., Lin M.T., Liao J.F., and Wang J.J. Scopolamine-induced amnesia can be prevented by heat shock pretreatment in rats. Neurosci. Lett. 364 (2004) 63-66
39. Ishimoto T., Kamei A., Koyanagi S., Nishide N., Uyeda A., Kasai M., and Taguchi T. HSP90 has neurite-promoting activity in vitro for telencephalic and spinal neurons of chick embryos. Biochem. Biophys. Res. Commun. 253 (1998) 283-287
40. Izquierdo I., and Medina J.H. Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem. 68 (1997) 285-316
41. Izquierdo I., and McGaugh J.L. Behavioural pharmacology and its contribution to the molecular basis of memory consolidation. Behav. Pharmacol. 11 (2000) 517-534
42. Izquierdo I., Quillfeldt J.A., Zanatta M.S., Quevedo J., Schaeffer E., Schmitz P.K., and Medina J.H. Sequential role of hippocampus and amygdala, entorhinal cortex and parietal cortex in formation and retrieval of memory for inhibitory avoidance in rats. Eur. J. Neurosci. 9 (1997) 786-793
43. Izquierdo I., Barros D.M., Mello e Souza T., de Souza M.M., Izquierdo L.A., and Medina J.H. Mechanisms for memory types differ. Nature 393 (1998) 635-636
44. Izquierdo I., Bevilaqua L.R., Rossato J.I., Bonini J.S., Medina J.H., and Cammarota M. Different molecular cascades in different sites of the brain control memory consolidation. Trends Neurosci. 29 (2006) 496-505
45. Kachiwala S.J., Harris S.E., Wright A.F., Hayward C., Starr J.M., Whalley L.J., and Deary I.J. Genetic influences on oxidative stress and their association with normal cognitive ageing. Neurosci. Lett. 386 (2005) 116-120
46. Kanaani J., Prusiner S.B., Diacovo J., Baekkeskov S., and Legname G. Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J. Neurochem. 95 (2005) 1373-1386
47. Kerr D.S., Bevilaqua L.R., Bonini J.S., Rossato J.I., Kohler C.A., Medina J.H., Izquierdo I., and Cammarota M. Angiotensin II blocks memory consolidation through an AT2 receptor-dependent mechanism. Psychopharmacology (Berlin) 179 (2005) 529-535
48. Kleinman H.K., Ogle R.C., Cannon F.B., Little C.D., Sweeney T.M., and Luckenbill-Edds L. Laminin receptors for neurite formation. Proc. Natl. Acad. Sci. U. S. A. 85 (1988) 1282-1286
49. Kleinman H.K., Weeks B.S., Schnaper H.W., Kibbey M.C., Yamamura K., and Grant D.S. The laminins: a family of basement membrane glycoproteins important in cell differentiation and tumor metastases. Vitam. Horm. 47 (1993) 161-186
50. Linnemann D., and Bock E. Cell adhesion molecules in neural development. Dev. Neurosci. 11 (1989) 149-173
51. Lopes M.H., Hajj G.N., Muras A.G., Mancini G.L., Castro R.M., Ribeiro K.C., Brentani R.R., Linden R., and Martins V.R. Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J. Neurosci. 25 (2005) 11330-11339
52. Luckenbill-Edds L. Laminin and the mechanism of neuronal outgrowth. Brain Res. Brain Res. Rev. 23 (1997) 1-27
53. Mallucci G.R., Ratte S., Asante E.A., Linehan J., Gowland I., Jefferys J.G., and Collinge J. Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBO J. 21 (2002) 202-210
54. Manson J.C., Clarke A.R., Hooper M.L., Aitchison L., McConnell I., and Hope J. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol. Neurobiol. 8 (1994) 121-127
55. Manthorpe M., Engvall E., Ruoslahti E., Longo F.M., Davis G.E., and Varon S. Laminin promotes neuritic regeneration from cultured peripheral and central neurons. J. Cell Biol. 97 (1983) 1882-1890
56. Martins V.R., Graner E., Garcia-Abreu J., de Souza S.J., Mercadante A.F., Veiga S.S., Zanata S.M., Neto V.M., and Brentani R.R. Complementary hydropathy identifies a cellular prion protein receptor. Nat. Med. 3 (1997) 1376-1382
57. Martins V.R., Linden R., Prado M.A., Walz R., Sakamoto A.C., Izquierdo I., and Brentani R.R. Cellular prion protein: on the road for functions. FEBS Lett. 512 (2002) 25-28
58. McGaugh J.L. Time-dependent processes in memory storage. Science 153 (1966) 1351-1358
59. McGaugh J.L. Memory-A century of consolidation. Science 287 (2000) 248-251
60. Morris R.G. Elements of a neurobiological theory of hippocampal function: the role of synaptic plasticity, synaptic tagging and schemas. Eur. J. Neurosci. 23 (2006) 2829-2846
61. Papassotiropoulos A., Wollmer M.A., Aguzzi A., Hock C., Nitsch R.M., and de Quervain D.J. The prion gene is associated with human long-term memory. Hum. Mol. Genet. 14 (2005) 2241-2246
62. Paxinos G., Watson C., Pennisi M., and Topple A. Bregma, lambda and the interaural midpoint in stereotaxic surgery with rats of different sex, strain and weight. J. Neurosci. Methods 13 (1985) 139-143
63. Petchanikow C., Saborio G.P., Anderes L., Frossard M.J., Olmedo M.I., and Soto C. Biochemical and structural studies of the prion protein polymorphism. FEBS Lett. 509 (2001) 451-456
64. Pizarro J.M., Haro L.S., and Barea-Rodriguez E.J. Learning associated increase in heat shock cognate 70 mRNA and protein expression. Neurobiol. Learn. Mem. 79 (2003) 142-151
65. Re L., Rossini F., Re F., Bordicchia M., Mercanti A., Fernandez O.S., and Barocci S. Prion protein potentiates acetylcholine release at the neuromuscular junction. Pharmacol. Res. 53 (2006) 62-68
66. Roucou X., and LeBlanc A.C. Cellular prion protein neuroprotective function: implications in prion diseases. J. Mol. Med. 83 (2005) 3-11
67. Sales N., Hassig R., Rodolfo K., Di Giamberardino L., Traiffort E., Ruat M., Fretier P., and Moya K.L. Developmental expression of the cellular prion protein in elongating axons. Eur. J. Neurosci. 15 (2002) 1163-1177
68. Santuccione A., Sytnyk V., Leshchyns'ka I., and Schachner M. Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J. Cell Biol. 169 (2005) 341-354
69. Shamsir M.S., and Dalby A.R. One gene, two diseases and three conformations: molecular dynamics simulations of mutants of human prion protein at room temperature and elevated temperatures. Proteins 59 (2005) 275-290
70. Stahl N., Borchelt D.R., Hsiao K., and Prusiner S.B. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51 (1987) 229-240
71. van der S.J., Kana B.D., Dirr H.W., and Blatch G.L. Heat shock cognate protein 70 chaperone-binding site in the co-chaperone murine stress-inducible protein 1 maps to within three consecutive tetratricopeptide repeat motifs. Biochem. J. 345 Pt. 3 (2000) 645-651
72. Vassallo N., and Herms J. Cellular prion protein function in copper homeostasis and redox signalling at the synapse. J. Neurochem. 86 (2003) 538-544
73. Whitlock J.R., Heynen A.J., Shuler M.G., and Bear M.F. Learning induces long-term potentiation in the hippocampus. Science 313 (2006) 1093-1097
74. Zanata S.M., Lopes M.H., Mercadante A.F., Hajj G.N., Chiarini L.B., Nomizo R., Freitas A.R., Cabral A.L., Lee K.S., Juliano M.A., de Oliveira E., Jachieri S.G., Burlingame A., Huang L., Linden R., Brentani R.R., and Martins V.R. Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 21 (2002) 3307-3316