Hypoxia induces expression of a GPI-anchorless splice variant of the prion protein

FEBS Journal

Volumn 275, Issue 11, 2008, Pages 2965-2976

  Kikuchi, Yutaka ^a   Kakeya, Tomoshi ^a   Nakajima, Osamu ^a   Sakai, Ayako ^a   Ikeda, Kikuko ^b   Yamaguchi, Naoto ^b   Yamazaki, Takeshi ^a   Tanamoto, Ken Ichi ^a   Matsuda, Haruo ^c   Sawada, Jun Ichi ^a   Takatori, Kosuke ^a  

^a NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^b CHIBA UNIVERSITY   (Japan)

^c HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Alternative splicing; Creudzfeldt Jakob disease; GPI anchor; Hypoxia; Prion

Indexed keywords

AMINO ACID; GLYCOSYLPHOSPHATIDYLINOSITOL; MESSENGER RNA; MONOCLONAL ANTIBODY; PRION PROTEIN;

ALTERNATIVE RNA SPLICING; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CYTOSOLIC FRACTION; EXON; GLIOBLASTOMA; GLYCOSYLATION; HUMAN; HYPOXIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; OXIDATIVE STRESS; OXYGEN TENSION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; RNA SPLICING; SEQUENCE ANALYSIS;

ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; ANOXIA; CELL LINE, TUMOR; CYTOSOL; EXONS; GENE EXPRESSION REGULATION; GLYCOPROTEINS; GLYCOSYLPHOSPHATIDYLINOSITOLS; HUMANS; IONS; MOLECULAR SEQUENCE DATA; NEURONS; PRIONS; PROTEIN STRUCTURE, TERTIARY;

EID: 43549092453     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06452.x     Document Type: Article

References (45)

1. Prusiner SB (1998) Prions. Proc Natl Acad Sci USA 95, 13363 13383.
2. Parchi P, Giese A, Capellari S, Brown P, Schulz-Schaeffer W, Windl O, Zerr I, Budka H, Kopp N, Piccardo P et al. (1999) Classification of sporadic Creutzfeldt-Jakob disease based on molecular and phenotypic analysis of 300 subjects. Ann Neurol 46, 224 233.
3. Kikuchi Y, Kakeya T, Sakai A, Takatori K, Nakamura N, Matsuda H, Yamazaki T, Tanamoto K Sawada J (2004) Propagation of a protease-resistant form of prion protein in long-term cultured human glioblastoma cell line T98G. J Gen Virol 85, 3449 3457.
4. Zanusso G, Farinazzo A, Prelli F, Fiorini M, Gelati M, Ferrari S, Righetti PG, Rizzuto N, Frangione B Monaco S (2004) Identification of distinct N-terminal truncated forms of prion protein in different Creutzfeldt-Jakob disease subtypes. J Biol Chem 279, 38936 38942.
5. Taylor JP, Hardy J Fischbeck KH (2002) Toxic proteins in neurodegenerative disease. Science 296, 1991 1995.
6. Meyer-Luehmann M, Coomaraswamy J, Bolmont T, Kaeser S, Schaefer C, Kilger E, Neuenschwander A, Abramowski D, Frey P, Jaton AL et al. (2006) Exogenous induction of cerebral beta-amyloidogenesis is governed by agent and host. Science 313, 1781 1784.
7. Kokmen E, Whisnant JP, O'Fallon WM, Chu CP Beard CM (1996) Dementia after ischemic stroke: a population-based study in Rochester, Minnesota (1960-1984). Neurology 46, 154 159.
8. Tatemichi TK, Paik M, Bagiella E, Desmond DW, Stern Y, Sano M, Hauser WA Mayeux R (1994) Risk of dementia after stroke in a hospitalized cohort: results of a longitudinal study. Neurology 44, 1885 1891.
9. Bazan NG, Palacios-Pelaez R Lukiw WJ (2002) Hypoxia signaling to genes: significance in Alzheimer's disease. Mol Neurobiol 26, 283 298.
10. Collins SJ, Sanchez-Juan P, Masters CL, Klug GM, van Duijn C, Poleggi A, Pocchiari M, Almonti S, Cuadrado-Corrales N, de Pedro-Cuesta J et al. (2006) Determinants of diagnostic investigation sensitivities across the clinical spectrum of sporadic Creutzfeldt-Jakob disease. Brain 129, 2278 2287.
11. Rachinger J, Fellner FA, Stieglbauer K Trenkler J (2002) MR changes after acute cyanide intoxication. Am J Neuroradiol 23, 1398 1401.
12. McLennan NF, Brennan PM, McNeill A, Davies I, Fotheringham A, Rennison KA, Ritchie D, Brannan F, Head MW, Ironside JW et al. (2004) Prion protein accumulation and neuroprotection in hypoxic brain damage. Am J Pathol 165, 227 235.
13. Goldberg MA, Dunning SP Bunn HF (1988) Regulation of the erythropoietin gene: evidence that the oxygen sensor is a heme protein. Science 242, 1412 1415.
14. Lai LP, Tsai CC, Su MJ, Lin JL, Chen YS, Tseng YZ Huang SK (2003) Atrial fibrillation is associated with accumulation of aging-related common type mitochondrial DNA deletion mutation in human atrial tissue. Chest 123, 539 544.
15. Breathnach R Chambon P (1981) Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50, 349 383.
16. Ohshima Y Gotoh Y (1987) Signals for the selection of a splice site in pre-mRNA. Computer analysis of splice junction sequences and like sequences. J Mol Biol 195, 247 259.
17. Makrinou E, Collinge J Antoniou M (2002) Genomic characterization of the human prion protein (PrP) gene locus. Mamm Genome 13, 696 703.
18. Peoc'h K, Serres C, Frobert Y, Martin C, Lehmann S, Chasseigneaux S, Sazdovitch V, Grassi J, Jouannet P, Launay JM et al. (2002) The human 'prion-like' protein Doppel is expressed in both Sertoli cells and spermatozoa. J Biol Chem 277, 43071 43078.
19. Comincini S, Facoetti A, Del-Vecchio I, Peoc'h K, Laplanche JL, Magrassi L, Ceroni M, Ferretti L Nano R (2004) Differential expression of the prion-like protein doppel gene (PRND) in astrocytomas: a new molecular marker potentially involved in tumor progression. Anticancer Res 24, 1507 1517.
20. Walmsley AR Hooper NM (2003) Distance of sequons to the C-terminus influences the cellular N-glycosylation of the prion protein. Biochem J 370, 351 355.
21. Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, LaCasse R, Raymond L, Favara C, Baron G, Priola S et al. (2005) Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308, 1435 1439.
22. Norstrom EM, Ciaccio MF, Rassbach B, Wollmann R Mastrianni JA (2007) Cytosolic prion protein toxicity is independent of cellular prion protein expression and prion propagation. J Virol 81, 2831 2837.
23. Devasahayam M, Catalino PD, Rudd PM, Dwek RA Barclay AN (1999) The glycan processing and site occupancy of recombinant Thy-1 is markedly affected by the presence of a glycosylphosphatidylinositol anchor. Glycobiology 9, 1381 1387.
24. Franzke CW, Has C, Schulte C, Huilaja L, Tasanen K, Aumailley M Bruckner-Tuderman L (2006) C-terminal truncation impairs glycosylation of transmembrane collagen XVII and leads to intracellular accumulation. J Biol Chem 281, 30260 30268.
25. Campana V, Caputo A, Sarnataro D, Paladino S, Tivodar S Zurzolo C (2007) Characterization of the properties and trafficking of an anchorless form of the prion protein. J Biol Chem 282, 22747 22756.
26. Ma J, Wollmann R Lindquist S (2002) Neurotoxicity and neurodegeneration when PrP accumulates in the cytosol. Science 298, 1781 1785.
27. Wang X, Wang F, Sy MS Ma J (2005) Calpain and other cytosolic proteases can contribute to the degradation of retro-translocated prion protein in the cytosol. J Biol Chem 280, 317 325.
28. Sato N, Hori O, Yamaguchi A, Lambert JC, Chartier-Harlin MC, Robinson PA, Delacourte A, Schmidt AM, Furuyama T, Imaizumi K et al. (1999) A novel presenilin-2 splice variant in human Alzheimer's disease brain tissue. J Neurochem 72, 2498 2505.
29. Matsuzaki S, Manabe T, Katayama T, Nishikawa A, Yanagita T, Okuda H, Yasuda Y, Miyata S, Meshitsuka S Tohyama M (2004) Metals accelerate production of the aberrant splicing isoform of the presenilin-2. J Neurochem 88, 1345 1351.
30. Brown DR, Hafiz F, Glasssmith LL, Wong BS, Jones IM, Clive C Haswell SJ (2000) Consequences of manganese replacement of copper for prion protein function and proteinase resistance. EMBO J 19, 1180 1186.
31. Maissen M, Roeckl C, Glatzel M, Goldmann W Aguzzi A (2001) Plasminogen binds to disease-associated prion protein of multiple species. Lancet 357, 2026 2028.
32. Ellis V, Daniels M, Misra R Brown DR (2002) Plasminogen activation is stimulated by prion protein and regulated in a copper-dependent manner. Biochemistry 41, 6891 6896.
33. Pearson WR Lipman DJ (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85, 2444 2448.
34. Kruithof EK, Tran-Thang C, Ransijn A Bachmann F (1984) Demonstration of a fast-acting inhibitor of plasminogen activators in human plasma. Blood 64, 907 913.
35. Black DL (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu Rev Biochem 72, 291 336.
36. Horiuchi M, Ishiguro N, Nagasawa H, Toyoda Y Shinagawa M (1997) Alternative usage of exon 1 of bovine PrP mRNA. Biochem Biophys Res Commun 233, 650 654.
37. Schröder B, Groschup M, Hunsmann G Bodemer W (1998) A differentially expressed prion gene mRNA is found in prion-infected mouse brains and in N2A cells but not in uninfected mice. Biochem Biophys Res Commun 251, 423 428.
38. Goldmann W, O'Neill G, Cheung F, Charleson F, Ford P Hunter N (1999) PrP (prion) gene expression in sheep may be modulated by alternative polyadenylation of its messenger RNA. J Gen Virol 80, 2275 2283.
39. Satoh J, Kurohara K, Yukitake M Kuroda Y (1998) Constitutive and cytokine-inducible expression of prion protein gene in human neural cell lines. J Neuropathol Exp Neurol 57, 131 139.
40. Kikuchi Y, Irie M, Ikebuchi H, Sawada J Terao T (1992) Identification of metallothionein in cultured cells by immunoblotting and immunofluorescence using a new monoclonal antibody. Hybridoma 11, 295 300.
41. Matsuda H, Mitsuda H, Nakamura N, Furusawa S, Mohri S Kitamoto T (1999) A chicken monoclonal antibody with specificity for the N-terminal of human prion protein. FEMS Immunol Med Microbiol 23, 189 194.
42. Miyamoto K, Nakamura N, Aosasa M, Nishida N, Yokoyama T, Horiuchi H, Furusawa S Matsuda H (2005) Inhibition of prion propagation in scrapie-infected mouse neuroblastoma cell lines using mouse monoclonal antibodies against prion protein. Biochem Biophys Res Commun 335, 197 204.
43. Kikuchi Y, Kakeya T, Yamazaki T, Takekida K, Nakamura N, Matsuda H, Takatori K, Tanimura A, Tanamoto K Sawada J (2002) G1-dependent prion protein expression in human glioblastoma cell line T98G. Biol Pharm Bull 25, 728 733.
44. Stein GH (1979) T98G: an anchorage-independent human tumor cell line that exhibits stationary phase G1 arrest in vitro. J Cell Physiol 99, 43 54.
45. Capellari S, Parchi P, Russo CM, Sanford J, Sy MS, Gambetti P Petersen RB (2000) Effect of the E200K mutation on prion protein metabolism. Comparative study of a cell model and human brain. Am J Pathol 157, 613 622.