AAV-mediated overexpression of neuroserpin in the hippocampus decreases PSD-95 expression but does not affect hippocampal-dependent learning and memory

PLoS ONE

Volumn 9, Issue 3, 2014, Pages

  Tsang, Vicky W K ^a,b   Young, Deborah ^b   During, Matthew J ^b,c   Birch, Nigel P ^a,b  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b UNIVERSITY OF AUCKLAND   (New Zealand)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NEUROSERPIN; PLASMINOGEN ACTIVATOR INHIBITOR 1; POSTSYNAPTIC DENSITY PROTEIN 95; TISSUE PLASMINOGEN ACTIVATOR; VIRUS VECTOR; DLGH4 PROTEIN, RAT; HYBRID PROTEIN; MEMBRANE PROTEIN; NEUROPEPTIDE; SERINE PROTEINASE INHIBITOR; SIGNAL PEPTIDE;

ADENO ASSOCIATED VIRUS; ADULT; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; ASSOCIATIVE MEMORY; CONDITIONING; CONTROLLED STUDY; ELEVATED T-MAZE TEST; ESCAPE BEHAVIOR; FEAR; GENE; GENE LOCATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HIPPOCAMPUS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEARNING; LOCOMOTION; MEMORY; MEMORY CONSOLIDATION; MEMORY DISORDER; NERVE CELL PLASTICITY; NEUROSERPIN GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN FIELD TEST; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RAT; RNA TRANSLATION; SECRETORY PATHWAY; SPATIAL LEARNING; SPATIAL MEMORY; STATE DEPENDENT LEARNING; TASK PERFORMANCE; TISSUE DISTRIBUTION; TRANSGENE; YOUNG ADULT; ZYMOGRAPHY; ANIMAL; DEPENDOPARVOVIRUS; GENE EXPRESSION; GENE VECTOR; GENETIC TRANSDUCTION; HEK293 CELL LINE; MALE; METABOLISM; WISTAR RAT;

ANIMALS; ANXIETY; DEPENDOVIRUS; FEAR; GENE EXPRESSION; GENETIC VECTORS; HEK293 CELLS; HIPPOCAMPUS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MEMBRANE PROTEINS; MEMORY; NEURONAL PLASTICITY; NEUROPEPTIDES; PLASMINOGEN ACTIVATOR INHIBITOR 1; RATS, WISTAR; RECOMBINANT FUSION PROTEINS; SECRETORY PATHWAY; SERPINS; TISSUE PLASMINOGEN ACTIVATOR; TRANSDUCTION, GENETIC; TRANSGENES;

EID: 84897392542     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0091050     Document Type: Article

References (63)

1. Osterwalder T, Contartese J, Stoeckli ET, Kuhn TB, Sonderegger P (1996) Neuroserpin, an axonally secreted serine protease inhibitor. EMBO J 15: 2944-2953. (Pubitemid 26188167)
2. Hastings GA, Coleman TA, Haudenschild CC, Stefansson S, Smith EP, et al. (1997) Neuroserpin, a brain-associated inhibitor of tissue plasminogen activator is localized primarily in neurons. Implications for the regulation of motor learning and neuronal survival. J Biol Chem 272: 33062-33067. (Pubitemid 28023647)
3. Krueger SR, Ghisu GP, Cinelli P, Gschwend TP, Osterwalder T, et al. (1997) Expression of neuroserpin, an inhibitor of tissue plasminogen activator, in the developing and adult nervous system of the mouse. J Neurosci 17: 8984-8996. (Pubitemid 27498427)
4. Osterwalder T, Cinelli P, Baici A, Pennella A, Krueger SR, et al. (1998) The axonally secreted serine proteinase inhibitor, neuroserpin, inhibits plasminogen activators and plasmin but not thrombin. J Biol Chem 273: 2312-2321. (Pubitemid 28069285)
5. Teesalu T, Kulla A, Simisker A, Siren V, Lawrence DA, et al. (2004) Tissue plasminogen activator and neuroserpin are widely expressed in the human central nervous system. Thromb Haemost 92: 358-368. (Pubitemid 39172317)
6. Frey U, Muller M, Kuhl D (1996) A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J Neurosci 16: 2057-2063. (Pubitemid 26144018)
7. Huang YY, Bach ME, Lipp HP, Zhuo M, Wolfer DP, et al. (1996) Mice lacking the gene encoding tissue-type plasminogen activator show a selective interference with late-phase long-term potentiation in both Schaffer collateral and mossy fiber pathways. Proc Natl Acad Sci U S A 93: 8699-8704. (Pubitemid 26269623)
8. Madani R, Hulo S, Toni N, Madani H, Steimer T, et al. (1999) Enhanced hippocampal long-term potentiation and learning by increased neuronal expression of tissue-type plasminogen activator in transgenic mice. EMBO J 18: 3007-3012. (Pubitemid 29255609)
9. Calabresi P, Napolitano M, Centonze D, Marfia GA, Gubellini P, et al. (2000) Tissue plasminogen activator controls multiple forms of synaptic plasticity and memory. Eur J Neurosci 12: 1002-1012. (Pubitemid 30168779)
10. Pawlak R, Nagai N, Urano T, Napiorkowska-Pawlak D, Ihara H, et al. (2002) Rapid, specific and active site-catalyzed effect of tissue-plasminogen activator on hippocampus-dependent learning in mice. Neuroscience 113: 995-1001. (Pubitemid 35245266)
11. Meiri N, Masos T, Rosenblum K, Miskin R, Dudai Y (1994) Overexpression of urokinase-type plasminogen activator in transgenic mice is correlated with impaired learning. Proc Natl Acad Sci U S A 91: 3196.
12. Wannier-Morino P, Rager G, Sonderegger P, Grabs D (2003) Expression of neuroserpin in the visual cortex of the mouse during the developmental critical period. Eur J Neurosci 17: 1853-1860. (Pubitemid 36645335)
13. Mataga N, Nagai N, Hensch TK (2002) Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci U S A 99: 7717-7721. (Pubitemid 34568757)
14. Madani R, Kozlov S, Akhmedov A, Cinelli P, Kinter J, et al. (2003) Impaired explorative behavior and neophobia in genetically modified mice lacking or overexpressing the extracellular serine protease inhibitor neuroserpin. Mol Cell Neurosci 23: 473-494. (Pubitemid 36802016)
15. Xu R, Janson C, Mastakov M, Lawlor P, Young D, et al. (2001) Quantitative comparison of expression with adeno-associated virus (AAV-2) brain-specific gene cassettes. Gene Ther 8: 1323-1332. (Pubitemid 32834301)
16. Cao L, Jiao X, Zuzga DS, Liu Y, Fong DM, et al. (2004) VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 36: 827-835. (Pubitemid 39014099)
17. Burger C, Gorbatyuk OS, Velardo MJ, Peden CS, Williams P, et al. (2004) Recombinant AAV viral vectors pseudotyped with viral capsids from serotypes 1, 2, and 5 display differential efficiency and cell tropism after delivery to different regions of the central nervous system. Mol Ther 10: 302-317. (Pubitemid 39117875)
18. Li SF, Wang RZ, Meng QH, Li GL, Hu GJ, et al. (2006) Intra-ventricular infusion of rAAV1-EGFP resulted in transduction in multiple regions of adult rat brain: a comparative study with rAAV2 and rAAV5 vectors. Brain Res 1122: 1-9.
19. Kaplitt MG, Leone P, Samulski RJ, Xiao X, Pfaff DW, et al. (1994) Long-term gene expression and phenotypic correction using adeno-associated virus vectors in the mammalian brain. Nat Genet 8: 148-154. (Pubitemid 24308362)
20. Hill RM, Parmar PK, Coates LC, Mezey E, Pearson JF, et al. (2000) Neuroserpin is expressed in the pituitary and adrenal glands and induces the extension of neurite-like processes in AtT-20 cells. Biochem J 345 Pt 3: 595-601. (Pubitemid 30099089)
21. Hauck B, Chen L, Xiao W (2003) Generation and characterization of chimeric recombinant AAV vectors. Mol Ther 7: 419-425. (Pubitemid 36503866)
22. During MJ, Young D, Baer K, Lawlor P, Klugmann M (2003) Development and optimization of adeno-associated virus vector transfer into the central nervous system. Methods Mol Med 76: 221-236.
23. Borges VM, Lee TW, Christie DL, Birch NP (2010) Neuroserpin regulates the density of dendritic protrusions and dendritic spine shape in cultured hippocampal neurons. J Neurosci Res 88: 2610-2617.
24. Klugmann M, Wymond Symes C, Leichtlein CB, Klaussner BK, Dunning J, et al. (2005) AAV-mediated hippocampal expression of short and long Homer 1 proteins differentially affect cognition and seizure activity in adult rats. Mol Cell Neurosci 28: 347-360. (Pubitemid 40202595)
25. Mastakov MY, Baer K, Xu R, Fitzsimons H, During MJ (2001) Combined injection of rAAV with mannitol enhances gene expression in the rat brain. Mol Ther 3: 225-232. (Pubitemid 32509825)
26. Paxinos Watson (1986) The Rat Brain in Stereotaxic Coordinates: San Diego, CA: Academic.
27. Vassalli JD, Dayer JM, Wohlwend A, Belin D (1984) Concomitant secretion of prourokinase and of a plasminogen activator-specific inhibitor by cultured human monocytes-macrophages. J Exp Med 159: 1653.
28. Bolivar VJ, Manley K, Messer A (2003) Exploratory activity and fear conditioning abnormalities develop early in R6/2 Huntington's disease transgenic mice. Behav Neurosci 117: 1233-1242. (Pubitemid 37549425)
29. Olson ST, Gettins PG (2011) Regulation of proteases by protein inhibitors of the serpin superfamily. Prog Mol Biol Transl Sci 99: 185-240.
30. Dobo J, Gettins PG (2004) alpha1-Proteinase inhibitor forms initial non-covalent and final covalent complexes with elastase analogously to other serpin-proteinase pairs, suggesting a common mechanism of inhibition. J Biol Chem 279: 9264-9269. (Pubitemid 38295989)
31. Miranda E, Romisch K, Lomas DA (2004) Mutants of neuroserpin that cause dementia accumulate as polymers within the endoplasmic reticulum. J Biol Chem 279: 28283-28291. (Pubitemid 38900106)
32. Miranda E, Lomas DA (2006) Neuroserpin: a serpin to think about. Cell Mol Life Sci 63: 709-722.
33. Cinelli P, Madani R, Tsuzuki N, Vallet P, Arras M, et al. (2001) Neuroserpin, a neuroprotective factor in focal ischemic stroke. Mol Cell Neurosci 18: 443-457. (Pubitemid 34008386)
34. Kirik D, Rosenblad C, Burger C, Lundberg C, Johansen TE, et al. (2002) Parkinson-like neurodegeneration induced by targeted overexpression of α-synuclein in the nigrostriatal system. J Neurosci 22: 2780-2791. (Pubitemid 37465827)
35. Mouravlev A, Dunning J, Young D, During MJ (2006) Somatic gene transfer of cAMP response element-binding protein attenuates memory impairment in aging rats. Proc Natl Acad Sci U S A 103: 4705-4710.
36. Kiyota T, Ingraham KL, Swan RJ, Jacobsen MT, Andrews SJ, et al. (2011) AAV serotype 2/1-mediated gene delivery of anti-inflammatory interleukin-10 enhances neurogenesis and cognitive function in APP+PS1 mice. Gene Ther 19: 724-733.
37. Hall C, Ballachey EL (1932) A study of the rat's behavior in a field. A contribution to method in comparative psychology. University of California Publications in Psychology.
38. Conde CA, Costa V, Tomaz C (1999) Measuring emotional memory in the elevated T-maze using a training-to-criterion procedure. Pharmacol Biochem Behav 63: 63-69. (Pubitemid 29206563)
39. Berger P, Kozlov SV, Cinelli P, Kruger SR, Vogt L, et al. (1999) Neuronal depolarization enhances the transcription of the neuronal serine protease inhibitor neuroserpin. Mol Cell Neurosci 14: 455-467. (Pubitemid 30026588)
40. Ishigami S, Sandkvist M, Tsui F, Moore E, Coleman TA, et al. (2007) Identification of a novel targeting sequence for regulated secretion in the serine protease inhibitor neuroserpin. Biochem J 402: 25-34.
41. Miranda E, MacLeod I, Davies MJ, Perez J, Romisch K, et al. (2008) The intracellular accumulation of polymeric neuroserpin explains the severity of the dementia FENIB. Hum Mol Genet 17: 1527-1539. (Pubitemid 351737158)
42. Caroni P (1997) Overexpression of growth-associated proteins in the neurons of adult transgenic mice. J Neurosci Meth 71: 3-9.
43. Tye KM, Prakash R, Kim S-Y, Fenno LE, Grosenick L, et al. (2011) Amygdala circuitry mediating reversible and bidirectional control of anxiety. Nature 471: 358-362.
44. Wang DV, Wang F, Liu J, Zhang L, Wang Z, et al. (2011) Neurons in the amygdala with response-selectivity for anxiety in two ethologically based tests. PLoS One 6: e18739.
45. Barker-Carlson K, Lawrence DA, Schwartz BS (2002) Acyl-enzyme complexes between tissue-type plasminogen activator and neuroserpin are short-lived in vitro. J Biol Chem 277: 46852-46857. (Pubitemid 36159187)
46. Ricagno S, Caccia S, Sorrentino G, Antonini G, Bolognesi M (2009) Human neuroserpin: structure and time-dependent inhibition. J Mol Biol 388: 109-121.
47. Zhou A, Carrell RW, Huntington JA (2001) The serpin inhibitory mechanism is critically dependent on the length of the reactive center loop. J Biol Chem 276: 27541-27547.
48. Chen X, Vinade L, Leapman RD, Petersen JD, Nakagawa T, et al. (2005) Mass of the postsynaptic density and enumeration of three key molecules. Proc Natl Acad Sci U S A 102: 11551-11556. (Pubitemid 41153857)
49. Xu W (2011) PSD-95-like membrane associated guanylate kinases (PSD-MAGUKs) and synaptic plasticity. Curr Opin Neurobiol 21: 306-312.
50. El-Husseini AED, Schnell E, Chetkovich DM, Nicoll RA, Bredt DS (2000) PSD-95 involvement in maturation of excitatory synapses. Science 290: 1364-1368.
51. Carretón O, Giralt A, Torres-Peraza JF, Brito V, Lucas JJ, et al. (2012) Age-dependent decline of motor neocortex but not hippocampal performance in heterozygous BDNF mice correlates with a decrease of cortical PSD-95 but an increase of hippocampal TrkB levels. Exp Neurol 237: 335-345.
52. Okabe S, Miwa A, Okado H (2001) Spine formation and correlated assembly of presynaptic and postsynaptic molecules. J Neurosci 21: 6105-6114. (Pubitemid 32743148)
53. De Roo M, Klauser P, Mendez P, Poglia L, Muller D (2008) Activity-dependent PSD formation and stabilization of newly formed spines in hippocampal slice cultures. Cereb Cortex 18: 151-161. (Pubitemid 350233061)
54. Woods GF, Oh WC, Boudewyn LC, Mikula SK, Zito K (2011) Loss of PSD-95 Enrichment Is Not a Prerequisite for Spine Retraction. J Neurosci 31: 12129-12138.
55. Martin AM, Kuhlmann C, Trossbach S, Jaeger S, Waldron E, et al. (2008) The functional role of the second NPXY motif of the LRP1 β-chain in tissue-type plasminogen activator-mediated activation of N-methyl-d-aspartate receptors. J Biol Chem 283: 12004-12013.
56. Makarova A, Mikhailenko I, Bugge TH, List K, Lawrence DA, et al. (2003) The low density lipoprotein receptor-related protein modulates protease activity in the brain by mediating the cellular internalization of both neuroserpin and neuroserpin-tissue-type plasminogen activator complexes. J Biol Chem 278: 50250-50258. (Pubitemid 37548866)
57. Fassio A, Raimondi A, Lignani G, Benfenati F, Baldelli P (2011) Synapsins: from synapse to network hyperexcitability and epilepsy. Semin Cell Dev Biol 22: 408-415.
58. Toro C, Deakin JF (2005) NMDA receptor subunit NRI and postsynaptic protein PSD-95 in hippocampus and orbitofrontal cortex in schizophrenia and mood disorder. Schizophr Res 80: 323-330. (Pubitemid 41713658)
59. Feyissa AM, Chandran A, Stockmeier CA, Karolewicz B (2009) Reduced levels of NR2A and NR2B subunits of NMDA receptor and PSD-95 in the prefrontal cortex in major depression. Prog Neuropsychopharmacol Biol Psychiatry 33: 70-75.
60. Karolewicz B, Szebeni K, Gilmore T, Maciag D, Stockmeier CA, et al. (2009) Elevated levels of NR2A and PSD-95 in the lateral amygdala in depression. Int J Neuropsychopharmacol 12: 143-153.
61. Hall RA, Soderling TR (1997) Differential surface expression and phosphorylation of the N-methyl-D-aspartate receptor subunits NR1 and NR2 in cultured hippocampal neurons. J Biol Chem 272: 4135-4140. (Pubitemid 27078479)
62. Huh KH, Wenthold RJ (1999) Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J Biol Chem 274: 151-157.
63. Lee TW, Coates LC, Birch NP (2008) Neuroserpin regulates N-cadherin-mediated cell adhesion independently of its activity as an inhibitor of tissue plasminogen activator. J Neurosci Res 86: 1243-1253. (Pubitemid 351571899)