Developmental influence of the cellular prion protein on the gene expression profile in mouse hippocampus

Physiological Genomics

Volumn 43, Issue 12, 2011, Pages 711-725

  Benvegnù, Stefano ^a   Roncaglia, Paola ^a   Agostini, Federica ^a   Casalone, Cristina ^b   Corona, Cristiano ^b   Gustincich, Stefano ^a   Legname, Giuseppe ^a,c  

^a SISSA   (Italy)

^b Istituto Zooprofilattico Sperimentale   (Italy)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Genetic regulation; Postnatal development; Transcriptome stability

Indexed keywords

CALCIUM; PRION PROTEIN;

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; CALCIUM SIGNALING; CELL ADHESION; CELL COMMUNICATION AND CELL CONTACT; DEVELOPMENTAL STAGE; DOWN REGULATION; FEMALE; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; HIPPOCAMPUS; HOMEOSTASIS; MALE; MICROARRAY ANALYSIS; MOUSE; NERVE FIBER; NERVE FIBER GROWTH; NERVOUS SYSTEM; NEWBORN; NEWBORN PERIOD; NONHUMAN; POSTNATAL DEVELOPMENT; PRION DISEASE; PRIORITY JOURNAL; RNA ISOLATION; SYNAPTIC TRANSMISSION; UPREGULATION; WILD TYPE;

AGE FACTORS; ANIMALS; BLOTTING, WESTERN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE SILENCING; GENE THERAPY; HIPPOCAMPUS; MICE; MICROARRAY ANALYSIS; PRION DISEASES; PRIONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

ANIMALIA; MUS;

EID: 79959845068     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00205.2010     Document Type: Article

References (90)

1. Aguzzi A, Baumann F, Bremer J. The prion's elusive reason for being. Annu Rev Neurosci 31: 439-477, 2008.
2. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R. A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Biol Chem 270: 8730-8738, 1995.
3. Beggs HE, Baragona SC, Hemperly JJ, Maness PF. NCAM140 interacts with the focal adhesion kinase p125(fak) and the SRC-related tyrosine kinase p59(fyn). J Biol Chem 272: 8310-8319, 1997.
4. Belay ED. Transmissible spongiform encephalopathies in humans. Annu Rev Microbiol 53: 283-314, 1999.
5. Benvegnù S, Poggiolini I, Legname G. Neurodevelopmental expression and localization of the cellular prion protein in the central nervous system of the mouse. J Comp Neurol 518: 1879-1891, 2010.
6. Birchmeier C. ErbB receptors and the development of the nervous system. Exp Cell Res 315: 611-618, 2009.
7. Bretteville A, Planel E. Tau aggregates: toxic, inert, or protective species? J Alzheimers Dis 14: 431-436, 2008.
8. Brown DR, Schmidt B, Kretzschmar HA. Effects of oxidative stress on prion protein expression in PC12 cells. Int J Dev Neurosci 15: 961-972, 1997.
9. Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell 73: 1339-1347, 1993.
10. Bueler H, Fischer M, Lang Y, Bluethmann H, Lipp HP, DeArmond SJ, Prusiner SB, Aguet M, Weissmann C. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356: 577-582, 1992.
11. Carleton A, Tremblay P, Vincent JD, Lledo PM. Dose-dependent, prion protein (PrP)-mediated facilitation of excitatory synaptic transmission in the mouse hippocampus. Pflügers Arch 442: 223-239, 2001.
12. Chadi S, Young R, Le Guillou S, Tilly G, Bitton F, Martin-Magniette M, Soubigou-Taconnat L, Balzergue S, Vilotte M, Peyre C, Passet B, Béringue V, Renou J, Le Provost F, Laude H, Vilotte J. Brain transcriptional stability upon prion protein-encoding gene invalidation in zygotic or adult mouse. BMC Genomics 11: 448, 2010.
13. Charriere-Bertrand C, Nunez J. Regulation of tubulin, Tau and microtubule associated protein 2 expression during mouse brain development. Neurochem Int 21: 535-541, 1992.
14. Chaudhari N, Hahn WE. Genetic expression in the developing brain. Science 220: 924-928, 1983.
15. Checler F, Vincent B. Alzheimer's and prion diseases: distinct pathologies, common proteolytic denominators. Trends Neurosci 25: 616-620, 2002.
16. Clinton M, Manson J, McBride D, Miele G. Gene expression changes during murine postnatal brain development. Genome Biol 1: RESEARCH0005, 2000.
17. + currents. Neurosci Lett 209: 49-52, 1996.
18. Collinge J, Whittington MA, Sidle KC, Smith CJ, Palmer MS, Clarke AR, Jefferys JG. Prion protein is necessary for normal synaptic function. Nature 370: 295-297, 1994.
19. Crecelius AC, Helmstetter D, Strangmann J, Mitteregger G, Fröhlich T, Arnold GJ, Kretzschmar HA. The brain proteome profile is highly conserved between Prnp-/- and Prnp+/+ mice. Neuroreport 19: 1027- 1031, 2008.
20. Criado JR, Sanchez-Alavez M, Conti B, Giacchino JL, Wills DN, Henriksen SJ, Race R, Manson JC, Chesebro B, Oldstone MB. Mice devoid of prion protein have cognitive deficits that are rescued by reconstitution of PrP in neurons. Neurobiol Dis 19: 255-265, 2005.
21. Curtis J, Errington M, Bliss T, Voss K, MacLeod N. Age-dependent loss of PTP and LTP in the hippocampus of PrP-null mice. Neurobiol Dis 13: 55-62, 2003.
22. DeArmond SJ. Discovering the mechanisms of neurodegeneration in prion diseases. Neurochem Res 29: 1979-1998, 2004.
23. Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4: P3, 2003.
24. Deriziotis P, Tabrizi SJ. Prions and the proteasome. Biochim Biophys Acta 1782: 713-722, 2008.
25. Falls DL. Neuregulins: functions, forms, and signaling strategies. Exp Cell Res 284: 14-30, 2003.
26. Fournier JG, Escaig-Haye F, Billette de Villemeur T, Robain O. Ultrastructural localization of cellular prion protein (PrPc) in synaptic boutons of normal hamster hippocampus. C R Acad Sci III 318: 339-344, 1995.
27. Gauczynski S, Peyrin JM, Haik S, Leucht C, Hundt C, Rieger R, Krasemann S, Deslys JP, Dormont D, Lasmezas CI, Weiss S. The 37-kDa/67-kDa laminin receptor acts as the cell-surface receptor for the cellular prion protein. EMBO J 20: 5863-5875, 2001.
28. Graner E, Mercadante AF, Zanata SM, Forlenza OV, Cabral AL, Veiga SS, Juliano MA, Roesler R, Walz R, Minetti A, Izquierdo I, Martins VR, Brentani RR. Cellular prion protein binds laminin and mediates neuritogenesis. Brain Res Mol Brain Res 76: 85-92, 2000.
29. Grant SG, O'Dell TJ, Karl KA, Stein PL, Soriano P, Kandel ER. Impaired long-term potentiation, spatial learning, and hippocampal development in fyn mutant mice. Science 258: 1903-1910, 1992.
30. Hanger DP, Seereeram A, Noble W. Mediators of tau phosphorylation in the pathogenesis of Alzheimer's disease. Expert Rev Neurother 9: 1647-1666, 2009.
31. Herms J, Tings T, Gall S, Madlung A, Giese A, Siebert H, Schurmann P, Windl O, Brose N, Kretzschmar H. Evidence of presynaptic location and function of the prion protein. J Neurosci 19: 8866-8875, 1999.
32. + currents in cerebellar purkinje cells. Neurobiol Dis 8: 324-330, 2001.
33. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med 9: 811-818, 1990.
34. Holbro T, Hynes NE. ErbB receptors: directing key signaling networks throughout life. Annu Rev Pharmacol Toxicol 44: 195-217, 2004.
35. Hu W, Rosenberg RN, Stuve O. Prion proteins: a biological role beyond prion diseases. Acta Neurol Scand 116: 75-82, 2007.
36. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57, 2009.
37. Isaacson RL, Pribram KH. The Hippocampus. New York: Plenum Press, 1986.
38. Ishikura N, Clever JL, Bouzamondo-Bernstein E, Samayoa E, Prusiner SB, Huang EJ, DeArmond SJ. Notch-1 activation and dendritic atrophy in prion disease. Proc Natl Acad Sci USA 102: 886-891, 2005.
39. Jacobson M, Rao MS. Developmental Neurobiology. New York: Kluwer Academic/Plenum, 2005.
40. Kanaani J, Prusiner SB, Diacovo J, Baekkeskov S, Legname G. Recombinant prion protein induces rapid polarization and development of synapses in embryonic rat hippocampal neurons in vitro. J Neurochem 95: 1373-1386, 2005.
41. Kenessey A, Yen SH. The extent of phosphorylation of fetal tau is comparable to that of PHF-tau from Alzheimer paired helical filaments. Brain Res 629: 40-46, 1993.
42. Kim BH, Lee HG, Choi JK, Kim JI, Choi EK, Carp RI, Kim YS. The cellular prion protein (PrPC) prevents apoptotic neuronal cell death and mitochondrial dysfunction induced by serum deprivation. Brain Res Mol Brain Res 124: 40-50, 2004.
43. Kraus F, Haenig B, Kispert A. Cloning and expression analysis of the mouse T-box gene Tbx18. Mech Dev 100: 83-86, 2001.
44. Lauren J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM. Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457: 1128-1132, 2009.
45. Lazarini F, Deslys JP, Dormont D. Regulation of the glial fibrillary acidic protein, beta actin and prion protein mRNAs during brain development in mouse. Brain Res Mol Brain Res 10: 343-346, 1991.
46. Lim KL, Tan JM. Role of the ubiquitin proteasome system in Parkinson's disease. BMC Biochem 8, Suppl 1: S13, 2007.
47. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25: 402-408, 2001.
48. Lledo PM, Tremblay P, DeArmond SJ, Prusiner SB, Nicoll RA. Mice deficient for prion protein exhibit normal neuronal excitability and synaptic transmission in the hippocampus. Proc Natl Acad Sci USA 93: 2403-2407, 1996.
49. Lobao-Soares B, Walz R, Prediger RD, Freitas RL, Calvo F, Bianchin MM, Leite JP, Landemberger MC, Coimbra NC. Cellular prion protein modulates defensive attention and innate fear-induced behaviour evoked in transgenic mice submitted to an agonistic encounter with the tropical coral snake Oxyrhopus guibei. Behav Brain Res 194: 129-137, 2008.
50. Malaga-Trillo E, Solis GP, Schrock Y, Geiss C, Luncz L, Thomanetz V, Stuermer CA. Regulation of embryonic cell adhesion by the prion protein. PLoS Biol 7: e55, 2009.
51. Mallucci G, Dickinson A, Linehan J, Klohn PC, Brandner S, Collinge J. Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302: 871-874, 2003.
52. Mallucci GR, Ratte S, Asante EA, Linehan J, Gowland I, Jefferys JG, Collinge J. Post-natal knockout of prion protein alters hippocampal CA1 properties, but does not result in neurodegeneration. EMBOJ 21: 202-210, 2002.
53. Mallucci GR, White MD, Farmer M, Dickinson A, Khatun H, Powell AD, Brandner S, Jefferys JG, Collinge J. Targeting cellular prion protein reverses early cognitive deficits and neurophysiological dysfunction in prion-infected mice. Neuron 53: 325-335, 2007.
54. Manson J, West JD, Thomson V, McBride P, Kaufman MH, Hope J. The prion protein gene: a role in mouse embryogenesis? Development 115: 117-122, 1992.
55. Manson JC, Clarke AR, Hooper ML, Aitchison L, McConnell I, Hope J. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 8: 121-127, 1994.
56. McLennan NF, Brennan PM, McNeill A, Davies I, Fotheringham A, Rennison KA, Ritchie D, Brannan F, Head MW, Ironside JW, Williams A, Bell JE. Prion protein accumulation and neuroprotection in hypoxic brain damage. Am J Pathol 165: 227-235, 2004.
57. Mobley WC, Neve RL, Prusiner SB, McKinley MP. Nerve growth factor increases mRNA levels for the prion protein and the beta-amyloid protein precursor in developing hamster brain. Proc Natl Acad Sci USA 85: 9811-9815, 1988.
58. Mody M, Cao Y, Cui Z, Tay KY, Shyong A, Shimizu E, Pham K, Schultz P, Welsh D, Tsien JZ. Genome-wide gene expression profiles of the developing mouse hippocampus. Proc Natl Acad Sci USA 98: 8862-8867, 2001.
59. Moore DJ, Dawson VL, Dawson TM. Role for the ubiquitin-proteasome system in Parkinson's disease and other neurodegenerative brain amyloidoses. Neuromolecular Med 4: 95-108, 2003.
60. Mouillet-Richard S, Ermonval M, Chebassier C, Laplanche JL, Lehmann S, Launay JM, Kellermann O. Signal transduction through prion protein. Science 289: 1925-1928, 2000.
61. Moya KL, Sales N, Hassig R, Creminon C, Grassi J, Di Giamberardino L. Immunolocalization of the cellular prion protein in normal brain. Microsc Res Tech 50: 58-65, 2000.
62. Nelson WJ. Regulation of cell-cell adhesion by the cadherin-catenin complex. Biochem Soc Trans 36: 149-155, 2008.
63. Parkin ET, Watt NT, Hussain I, Eckman EA, Eckman CB, Manson JC, Baybutt HN, Turner AJ, Hooper NM. Cellular prion protein regulates beta-secretase cleavage of the Alzheimer's amyloid precursor protein. Proc Natl Acad Sci USA 104: 11062-11067, 2007.
64. Pokorný J, Yamamoto T. Postnatal ontogenesis of hippocampal CA1 area in rats. I. Development of dendritic arborisation in pyramidal neurons. Brain Res Bull 7: 113-120, 1981.
65. Pokorný J, Yamamoto T. Postnatal ontogenesis of hippocampal CA1 area in rats. II. Development of ultrastructure in stratum lacunosum and moleculare. Brain Res Bull 7: 121-130, 1981.
66. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 216: 136-144, 1982.
67. Prusiner SB. Prions. Proc Natl Acad Sci USA 95: 13363-13383, 1998.
68. Rangel A, Madronal N, Gruart i Masso A, Gavin R, Llorens F, Sumoy L, Torres JM, Delgado-Garcia JM, Del Rio JA. Regulation of GABA(A) and glutamate receptor expression, synaptic facilitation and long-term potentiation in the hippocampus of prion mutant mice. PLoS One 4: e7592, 2009.
69. Rieger R, Edenhofer F, Lasmezas CI, Weiss S. The human 37-kDa laminin receptor precursor interacts with the prion protein in eukaryotic cells. Nat Med 3: 1383-1388, 1997.
70. Roucou X, LeBlanc AC. Cellular prion protein neuroprotective function: implications in prion diseases. J Mol Med 83: 3-11, 2005.
71. Sales N, Hassig R, Rodolfo K, Di Giamberardino L, Traiffort E, Ruat M, Fretier P, Moya KL. Developmental expression of the cellular prion protein in elongating axons. Eur J Neurosci 15: 1163-1177, 2002.
72. Sanchez-Alavez M, Conti B, Moroncini G, Criado JR. Contributions of neuronal prion protein on sleep recovery and stress response following sleep deprivation. Brain Res 1158: 71-80, 2007.
73. Sanchez-Alavez M, Criado JR, Klein I, Moroncini G, Conti B. Hypothalamic- pituitary-adrenal axis disregulation in PrPC-null mice. Neuroreport 19: 1473-1477, 2008.
74. Santuccione A, Sytnyk V, Leshchyns'ka I, Schachner M. Prion protein recruits its neuronal receptor NCAM to lipid rafts to activate p59fyn and to enhance neurite outgrowth. J Cell Biol 169: 341-354, 2005.
75. Schmitt-Ulms G, Legname G, Baldwin MA, Ball HL, Bradon N, Bosque PJ, Crossin KL, Edelman GM, DeArmond SJ, Cohen FE, Prusiner SB. Binding of neural cell adhesion molecules (N-CAMs) to the cellular prion protein. J Mol Biol 314: 1209-1225, 2001.
76. Schmitt-Ulms G, Hansen K, Liu J, Cowdrey C, Yang J, DeArmond SJ, Cohen FE, Prusiner SB, Baldwin MA. Time-controlled transcardiac perfusion cross-linking for the study of protein interactions in complex tissues. Nat Biotechnol 22: 724-731, 2004.
77. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3, 2004.
78. Spilman P, Lessard P, Sattavat M, Bush C, Tousseyn T, Huang EJ, Giles K, Golde T, Das P, Fauq A, Prusiner SB, Dearmond SJ. A gamma-secretase inhibitor and quinacrine reduce prions and prevent dendritic degeneration in murine brains. Proc Natl Acad Sci USA 105: 10595-10600, 2008.
79. Steele AD, Emsley JG, Ozdinler PH, Lindquist S, Macklis JD. Prion protein (PrPc) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis. Proc Natl Acad Sci USA 103: 3416-3421, 2006.
80. Talora C, Campese AF, Bellavia D, Felli MP, Vacca A, Gulino A, Screpanti I. Notch signaling and diseases: an evolutionary journey from a simple beginning to complex outcomes. Biochim Biophys Acta 1782: 489-497, 2008.
81. Tobler I, Gaus SE, Deboer T, Achermann P, Fischer M, Rulicke T, Moser M, Oesch B, McBride PA, Manson JC. Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 380: 639-642, 1996.
82. Tremblay P, Bouzamondo-Bernstein E, Heinrich C, Prusiner SB, DeArmond SJ. Developmental expression of PrP in the post-implantation embryo. Brain Res 1139: 60-67, 2007.
83. Umemori H, Kadowaki Y, Hirosawa K, Yoshida Y, Hironaka K, Okano H, Yamamoto T. Stimulation of myelin basic protein gene transcription by Fyn tyrosine kinase for myelination. J Neurosci 19: 1393-1397, 1999.
84. Upadhya SC, Hegde AN. Role of the ubiquitin proteasome system in Alzheimer's disease. BMC Biochem 8, Suppl 1: S12, 2007.
85. Vincent B, Sunyach C, Orzechowski HD, St George-Hyslop P, Checler F. p53-Dependent transcriptional control of cellular prion by presenilins. J Neurosci 29: 6752-6760, 2009.
86. Walz R, Amaral OB, Rockenbach IC, Roesler R, Izquierdo I, Cavalheiro EA, Martins VR, Brentani RR. Increased sensitivity to seizures in mice lacking cellular prion protein. Epilepsia 40: 1679-1682, 1999.
87. Whatley BR, Li L, Chin LS. The ubiquitin-proteasome system in spongiform degenerative disorders. Biochim Biophys Acta 1782: 700-712, 2008.
88. White AR, Collins SJ, Maher F, Jobling MF, Stewart LR, Thyer JM, Beyreuther K, Masters CL, Cappai R. Prion protein-deficient neurons reveal lower glutathione reductase activity and increased susceptibility to hydrogen peroxide toxicity. Am J Pathol 155: 1723-1730, 1999.
89. White MD, Farmer M, Mirabile I, Brandner S, Collinge J, Mallucci GR. Single treatment with RNAi against prion protein rescues early neuronal dysfunction and prolongs survival in mice with prion disease. Proc Natl Acad Sci USA 105: 10238-10243, 2008.
90. Yu Y, Run X, Liang Z, Li Y, Liu F, Liu Y, Iqbal K, Grundke-Iqbal I, Gong CX. Developmental regulation of tau phosphorylation, tau kinases, and tau phosphatases. J Neurochem 108: 1480-1494, 2009.