Translation of the prion protein mRNA is robust in astrocytes but does not amplify during reactive astrocytosis in the mouse brain

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Jackson, Walker S ^a,b   Krost, Clemens ^a   Borkowski, Andrew W ^b   Kaczmarczyk, Lech ^a  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; MESSENGER RNA; PRION PROTEIN; PRION; PRNP PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ASTROCYTOSIS; BRAIN HOMOGENATE; BRAIN REGION; CONTROLLED STUDY; FEMALE; FLUORESCENCE; FLUORESCENCE ACTIVATED CELL SORTING; GENE; GENE SEQUENCE; GENETIC MANIPULATION; GENOME; GLIOSIS; IMMUNOFLUORESCENCE; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRNP GENE; RNA TRANSLATION; SCRAPIE; ANIMAL; BRAIN; CYTOLOGY; GENETICS; METABOLISM; MUTANT MOUSE STRAIN; PRION;

ANIMALS; ASTROCYTES; BRAIN; FEMALE; GLIOSIS; MALE; MICE; MICE, MUTANT STRAINS; PRIONS; RNA, MESSENGER;

EID: 84899674455     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0095958     Document Type: Article

References (69)

1. Aguzzi A, Polymenidou M (2004) Mammalian prion biology: one century of evolving concepts. Cell 116: 313-327. (Pubitemid 38167320)
2. Parry HB (1962) Scrapie: a transmissible and hereditary disease of sheep. Heredity (Edinb) 17: 75-105.
3. Watts JC, Balachandran A, Westaway D (2006) The expanding universe of prion diseases. PLoS Pathog 2: e26.
4. Sigurdson CJ, Aguzzi A (2007) Chronic wasting disease. Biochim Biophys Acta 1772: 610-618. (Pubitemid 46880207)
5. Mathiason CK, Nalls AV, Seelig DM, Kraft SL, Carnes K, et al. (2013) Susceptibility of domestic cats to chronic wasting disease. J Virol 87: 1947-1956.
6. Bruce ME, Will RG, Ironside JW, McConnell I, Drummond D, et al. (1997) Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent. Nature 389: 498-501. (Pubitemid 27435325)
7. Hill AF, Desbruslais M, Joiner S, Sidle KC, Gowland I, et al. (1997) The same prion strain causes vCJD and BSE. Nature 389: 448-450, 526.
8. Wadsworth JD, Hill AF, Beck JA, Collinge J (2003) Molecular and clinical classification of human prion disease. Br Med Bull 66: 241-254. (Pubitemid 37173505)
9. Prusiner SB (1998) Prions. Proc Natl Acad Sci U S A 95: 13363-13383.
10. Kovacs GG, Trabattoni G, Hainfellner JA, Ironside JW, Knight RS, et al. (2002) Mutations of the prion protein gene phenotypic spectrum. J Neurol 249: 1567-1582. (Pubitemid 35477900)
11. Jackson WS (2014) Selective vulnerability to neurodegenerative disease: the curious case of Prion Protein. Dis Model Mech 7: 21-29.
12. Ford MJ, Burton LJ, Li H, Graham CH, Frobert Y, et al. (2002) A marked disparity between the expression of prion protein and its message by neurones of the CNS. Neuroscience 111: 533-551. (Pubitemid 34521894)
13. Haeberle AM, Ribaut-Barassin C, Bombarde G, Mariani J, Hunsmann G, et al. (2000) Synaptic prion protein immuno-reactivity in the rodent cerebellum. Microsc Res Tech 50: 66-75. (Pubitemid 30497407)
14. Moser M, Colello RJ, Pott U, Oesch B (1995) Developmental expression of the prion protein gene in glial cells. Neuron 14: 509-517.
15. Cahoy JD, Emery B, Kaushal A, Foo LC, Zamanian JL, et al. (2008) A transcriptome database for astrocytes, neurons, and oligodendrocytes: a new resource for understanding brain development and function. J Neurosci 28: 264-278.
16. Barmada S, Piccardo P, Yamaguchi K, Ghetti B, Harris DA (2004) GFP-tagged prion protein is correctly localized and functionally active in the brains of transgenic mice. Neurobiol Dis 16: 527-537. (Pubitemid 38942985)
17. Steele AD, Emsley JG, Ozdinler PH, Lindquist S, Macklis JD (2006) Prion protein (PrPc) positively regulates neural precursor proliferation during developmental and adult mammalian neurogenesis. Proc Natl Acad Sci U S A 103: 3416-3421. (Pubitemid 43346483)
18. Le Pichon CE, Firestein S (2008) Expression and localization of the prion protein PrP(C) in the olfactory system of the mouse. J Comp Neurol 508: 487-499. (Pubitemid 351562031)
19. Laine J, Marc ME, Sy MS, Axelrad H (2001) Cellular and subcellular morphological localization of normal prion protein in rodent cerebellum. Eur J Neurosci 14: 47-56. (Pubitemid 32738473)
20. Diedrich JF, Bendheim PE, Kim YS, Carp RI, Haase AT (1991) Scrapie-associated prion protein accumulates in astrocytes during scrapie infection. Proc Natl Acad Sci U S A 88: 375-379. (Pubitemid 21915467)
21. Raeber AJ, Race RE, Brandner S, Priola SA, Sailer A, et al. (1997) Astrocyte-specific expression of hamster prion protein (PrP) renders PrP knockout mice susceptible to hamster scrapie. Embo J 16: 6057-6065. (Pubitemid 27458325)
22. Haigh CL, Brown DR (2006) Regulation of prion protein expression: a potential site for therapeutic intervention in the transmissible spongiform encephalopathies. Int J Biomed Sci 2: 315-323.
23. Bueler H, Raeber A, Sailer A, Fischer M, Aguzzi A, et al. (1994) High prion and PrPSc levels but delayed onset of disease in scrapie-inoculated mice heterozygous for a disrupted PrP gene. Mol Med 1: 19-30.
24. Ghetti B, Tagliavini F, Masters CL, Beyreuther K, Giaccone G, et al. (1989) Gerstmann-Straussler-Scheinker disease. II. Neurofibrillary tangles and plaques with PrP-amyloid coexist in an affected family. Neurology 39: 1453-1461. (Pubitemid 19286000)
25. Muramoto T, Kitamoto T, Koga H, Tateishi J (1992) The coexistence of Alzheimer's disease and Creutzfeldt-Jakob disease in a patient with dementia of long duration. Acta Neuropathol 84: 686-689.
26. Bugiani O, Giaccone G, Verga L, Pollo B, Frangione B, et al. (1993) Beta PP participates in PrP-amyloid plaques of Gerstmann-Straussler-Scheinker disease, Indiana kindred. J Neuropathol Exp Neurol 52: 64-70. (Pubitemid 23016640)
27. Ghetti B, Tagliavini F, Giaccone G, Bugiani O, Frangione B, et al. (1994) Familial Gerstmann-Straussler-Scheinker disease with neurofibrillary tangles. Mol Neurobiol 8: 41-48.
28. Hainfellner JA, Wanschitz J, Jellinger K, Liberski PP, Gullotta F, et al. (1998) Coexistence of Alzheimer-type neuropathology in Creutzfeldt-Jakob disease. Acta Neuropathol 96: 116-122. (Pubitemid 28356523)
29. Tsuchiya K, Yagishita S, Ikeda K, Sano M, Taki K, et al. (2004) Coexistence of CJD and Alzheimer's disease: an autopsy case showing typical clinical features of CJD. Neuropathology 24: 46-55. (Pubitemid 38391494)
30. Haraguchi T, Terada S, Ishizu H, Sakai K, Tanabe Y, et al. (2009) Coexistence of Creutzfeldt-Jakob disease, Lewy body disease, and Alzheimer's disease pathology: an autopsy case showing typical clinical features of Creutzfeldt-Jakob disease. Neuropathology 29: 454-459.
31. Yoshida H, Terada S, Ishizu H, Ikeda K, Hayabara T, et al. (2010) An autopsy case of Creutzfeldt-Jakob disease with a V180I mutation of the PrP gene and Alzheimer-type pathology. Neuropathology 30: 159-164.
32. Reiniger L, Lukic A, Linehan J, Rudge P, Collinge J, et al. (2011) Tau, prions and Abeta: the triad of neurodegeneration. Acta Neuropathol 121: 5-20.
33. Lauren J, Gimbel DA, Nygaard HB, Gilbert JW, Strittmatter SM (2009) Cellular prion protein mediates impairment of synaptic plasticity by amyloid-beta oligomers. Nature 457: 1128-1132.
34. Freir DB, Nicoll AJ, Klyubin I, Panico S, Mc Donald JM, et al. (2011) Interaction between prion protein and toxic amyloid beta assemblies can be therapeutically targeted at multiple sites. Nat Commun 2: 336.
35. Larson M, Sherman MA, Amar F, Nuvolone M, Schneider JA, et al. (2012) The complex PrP(c)-Fyn couples human oligomeric Abeta with pathological tau changes in Alzheimer's disease. J Neurosci 32: 16857-16871a.
36. Fluharty BR, Biasini E, Stravalaci M, Sclip A, Diomede L, et al. (2013) An N-terminal fragment of the prion protein binds to amyloid-beta oligomers and inhibits their neurotoxicity in vivo. J Biol Chem 288: 7857-7866.
37. You H, Tsutsui S, Hameed S, Kannanayakal TJ, Chen L, et al. (2012) Abeta neurotoxicity depends on interactions between copper ions, prion protein, and N-methyl-D-aspartate receptors. Proc Natl Acad Sci U S A 109: 1737-1742.
38. Jackson WS, Borkowski AW, Faas H, Steele AD, King OD, et al. (2009) Spontaneous generation of prion infectivity in fatal familial insomnia knockin mice. Neuron 63: 438-450.
39. Moore RC, Lee IY, Silverman GL, Harrison PM, Strome R, et al. (1999) Ataxia in prion protein (PrP)-deficient mice is associated with upregulation of the novel PrP-like protein doppel. J Mol Biol 292: 797-817. (Pubitemid 29465475)
40. Rossi D, Cozzio A, Flechsig E, Klein MA, Rulicke T, et al. (2001) Onset of ataxia and Purkinje cell loss in PrP null mice inversely correlated with Dpl level in brain. EMBO J 20: 694-702. (Pubitemid 32167634)
41. Jackson WS, Borkowski AW, Watson NE, King OD, Faas H, et al. (2013) Profoundly different prion diseases in knock-in mice carrying single PrP codon substitutions associated with human diseases. Proc Natl Acad Sci U S A 110: 14759-14764.
42. Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, et al. (2008) Genomic anatomy of the hippocampus. Neuron 60: 1010-1021.
43. Karapetyan YE, Saa P, Mahal SP, Sferrazza GF, Sherman A, et al. (2009) Prion strain discrimination based on rapid in vivo amplification and analysis by the cell panel assay. PLoS One 4: e5730.
44. Stichel CC, Muller CM, Zilles K (1991) Distribution of glial fibrillary acidic protein and vimentin immunoreactivity during rat visual cortex development. J Neurocytol 20: 97-108.
45. Bushong EA, Martone ME, Jones YZ, Ellisman MH (2002) Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci 22: 183-192. (Pubitemid 34033496)
46. Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119: 7-35.
47. Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, et al. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73: 1339-1347. (Pubitemid 23201147)
48. Manson JC, Clarke AR, McBride PA, McConnell I, Hope J (1994) PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration 3: 331-340.
49. Lemaire-Vieille C, Schulze T, Podevin-Dimster V, Follet J, Bailly Y, et al. (2000) Epithelial and endothelial expression of the green fluorescent protein reporter gene under the control of bovine prion protein (PrP) gene regulatory sequences in transgenic mice. Proc Natl Acad Sci U S A 97: 5422-5427. (Pubitemid 30313734)
50. Bailly Y, Haeberle AM, Blanquet-Grossard F, Chasserot-Golaz S, Grant N, et al. (2004) Prion protein (PrPc) immunocytochemistry and expression of the green fluorescent protein reporter gene under control of the bovine PrP gene promoter in the mouse brain. J Comp Neurol 473: 244-269. (Pubitemid 38569231)
51. Bian J, Nazor KE, Angers R, Jernigan M, Seward T, et al. (2006) GFP-tagged PrP supports compromised prion replication in transgenic mice. Biochem Biophys Res Commun 340: 894-900. (Pubitemid 43053913)
52. Encalada SE, Szpankowski L, Xia CH, Goldstein LS (2011) Stable kinesin and dynein assemblies drive the axonal transport of mammalian prion protein vesicles. Cell 144: 551-565.
53. Barmada SJ, Harris DA (2005) Visualization of prion infection in transgenic mice expressing green fluorescent protein-tagged prion protein. J Neurosci 25: 5824-5832. (Pubitemid 40847895)
54. Borchelt DR, Davis J, Fischer M, Lee MK, Slunt HH, et al. (1996) A vector for expressing foreign genes in the brains and hearts of transgenic mice. Genet Anal 13: 159-163. (Pubitemid 27063321)
55. Faas H, Jackson WS, Borkowski AW, Wang X, Ma J, et al. (2010) Context-dependent perturbation of neural systems in transgenic mice expressing a cytosolic prion protein. Neuroimage 49: 2607-2617.
56. Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, et al. (2003) A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 425: 917-925. (Pubitemid 37376918)
57. Kleene R, Loers G, Langer J, Frobert Y, Buck F, et al. (2007) Prion protein regulates glutamate-dependent lactate transport of astrocytes. J Neurosci 27: 12331-12340. (Pubitemid 350085463)
58. Lima FR, Arantes CP, Muras AG, Nomizo R, Brentani RR, et al. (2007) Cellular prion protein expression in astrocytes modulates neuronal survival and differentiation. J Neurochem 103: 2164-2176. (Pubitemid 350173555)
59. Foo LC, Allen NJ, Bushong EA, Ventura PB, Chung WS, et al. (2011) Development of a method for the purification and culture of rodent astrocytes. Neuron 71: 799-811.
60. Ye X, Scallet A, Carp RI (1999) Abnormal periodic acid-Schiff (PAS)-positive substance in the islets of Langerhans, pituitaries and adrenal glands of 139H scrapie-infected hamsters. Histol Histopathol 14: 673-678. (Pubitemid 29320330)
61. Heikenwalder M, Kurrer MO, Margalith I, Kranich J, Zeller N, et al. (2008) Lymphotoxin-dependent prion replication in inflammatory stromal cells of granulomas. Immunity 29: 998-1008.
62. Spudich A, Frigg R, Kilic E, Kilic U, Oesch B, et al. (2005) Aggravation of ischemic brain injury by prion protein deficiency: role of ERK-1/-2 and STAT-1. Neurobiol Dis 20: 442-449. (Pubitemid 41476270)
63. Weise J, Sandau R, Schwarting S, Crome O, Wrede A, et al. (2006) Deletion of cellular prion protein results in reduced Akt activation, enhanced postischemic caspase-3 activation, and exacerbation of ischemic brain injury. Stroke 37: 1296-1300. (Pubitemid 43731879)
64. Jeong JK, Seo JS, Moon MH, Lee YJ, Seol JW, et al. (2012) Hypoxia-inducible factor-1 alpha regulates prion protein expression to protect against neuron cell damage. Neurobiol Aging 33: 1006 e1001-1010.
65. Shyu WC, Lin SZ, Chiang MF, Ding DC, Li KW, et al. (2005) Overexpression of PrPC by adenovirus-mediated gene targeting reduces ischemic injury in a stroke rat model. J Neurosci 25: 8967-8977.
66. Dery MA, Jodoin J, Ursini-Siegel J, Aleynikova O, Ferrario C, et al. (2013) Endoplasmic reticulum stress induces PRNP prion protein gene expression in breast cancer. Breast Cancer Res 15: R22.
67. Yap YH, Say YH (2012) Resistance against tumour necrosis factor alpha apoptosis by the cellular prion protein is cell-specific for oral, colon and kidney cancer cell lines. Cell Biol Int 36: 273-277.
68. Magin TM, McWhir J, Melton DW (1992) A new mouse embryonic stem cell line with good germ line contribution and gene targeting frequency. Nucleic Acids Res 20: 3795-3796.
69. Jackson WS, Tallaksen-Greene SJ, Albin RL, Detloff PJ (2003) Nucleocytoplasmic transport signals affect the age at onset of abnormalities in knock-in mice expressing polyglutamine within an ectopic protein context. Hum Mol Genet 12: 1621-1629. (Pubitemid 36857308)