Proteolytic cleavage and shedding of the bovine prion protein in two cell culture systems

Virus Research

Volumn 115, Issue 1, 2006, Pages 43-55

  Zhao, Hongxing ^a,b   Klingeborn, Mikael ^a   Simonsson, Magnus ^a   Linné, Tommy ^a  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

Bovine prion; Cleavage site; Shedding; Soluble PrP

Indexed keywords

PRION PROTEIN; PROTEINASE;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOTINYLATION; BRAIN TISSUE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CELL LINE; CELL SURFACE; CONTROLLED STUDY; COW; CULTURE MEDIUM; ENZYME ACTIVITY; ENZYME INHIBITION; MOUSE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN SECRETION; PROTEIN TRANSPORT;

ANIMALS; CATTLE; CRICETINAE; MICE; PEPTIDE-N4-(N-ACETYL-BETA-GLUCOSAMINYL) ASPARAGINE AMIDASE; PRIONS; SOLUBILITY; SPECIES SPECIFICITY;

ANIMALIA; BOVINAE; CRICETINAE;

EID: 28844504671     PISSN: 01681702     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.virusres.2005.07.004     Document Type: Article

References (80)

1. A. Aguzzi, and M. Polymenidou Mammalian prion biology: one century of evolving concepts Cell 116 2004 313 327
2. J. Arribas, L. Coodly, P. Vollmer, T.K. Kishimoto, S. Rose-John, and J. Massague Diverse cell surface protein ectodomains are shed by a system sensitive to metalloprotease inhibitors J. Biol. Chem. 271 1996 11376 11382
3. V. Bazil, and J.L. Strominger Metalloprotease and serine protease are involved in cleavage of CD43, CD44, and CD16 from stimulated human granulocytes Induction of cleavage of L-selectin via CD16 J. Immunol. 152 1994 1314 1322
4. D.R. Borchelt, M. Rogers, N. Stahl, G. Telling, and S.B. Prusiner Release of the cellular prion protein from cultured cells after loss of its glycoinositol phospholipid anchor Glycobiology 3 1993 319 329
5. D.R. Borchelt, M. Scott, A. Taraboulos, N. Stahl, and S.B. Prusiner Scrapie and cellular prion proteins differ in their kinetics of synthesis and topology in cultured cells J. Cell Biol. 110 1990 743 752
6. D.R. Borchelt, A. Taraboulos, and S.B. Prusiner Evidence for synthesis of scrapie prion proteins in the endocytic pathway J. Biol. Chem. 267 1992 16188 16199
7. D.R. Brown Prion protein peptides: optimal toxicity and peptide blockade of toxicity Mol. Cell. Neurosci. 15 2000 66 78
8. M.E. Bruce, R.G. Will, J.W. Ironside, I. McConnell, D. Drummond, A. Suttie, L. McCardle, A. Chree, J. Hope, C. Birkett, S. Cousens, H. Fraser, and C.J. Bostock Transmissions to mice indicate that 'new variant' CJD is caused by the BSE agent Nature 389 1997 498 501
9. H. Bueler, A. Aguzzi, A. Sailer, R.A. Greiner, P. Autenried, M. Aguet, and C. Weissmann Mice devoid of PrP are resistant to scrapie Cell 73 1993 1339 1347
10. H. Bueler, M. Fischer, Y. Lang, H. Bluethmann, H.P. Lipp, S.J. DeArmond, S.B. Prusiner, M. Aguet, and C. Weissmann Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein Nature 356 1992 577 582
11. J.D. Buxbaum, K.N. Liu, Y. Luo, J.L. Slack, K.L. Stocking, J.J. Peschon, R.S. Johnson, B.J. Castner, D.P. Cerretti, and R.A. Black Evidence that tumor necrosis factor alpha converting enzyme is involved in regulated alpha-secretase cleavage of the Alzheimer amyloid protein precursor J. Biol. Chem. 273 1998 27765 27767
12. A.J. Carozzi, S. Roy, I.C. Morrow, A. Pol, B. Wyse, J. Clyde-Smith, I.A. Prior, S.J. Nixon, J.F. Hancock, and R.G. Parton Inhibition of lipid raft-dependent signaling by a dystrophy-associated mutant of caveolin-3 J. Biol. Chem. 277 2002 17944 17949
13. B. Caughey, R.E. Race, D. Ernst, M.J. Buchmeier, and B. Chesebro Prion protein biosynthesis in scrapie-infected and uninfected neuroblastoma cells J. Virol. 63 1989 175 181
14. B. Caughey, G.J. Raymond, D. Ernst, and R.E. Race N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state J. Virol. 65 1991 6597 6603
15. F. Checler, and B. Vincent Alzheimer's and prion diseases: distinct pathologies, common proteolytic denominators Trends Neurosci. 25 2002 616 620
16. S.G. Chen, D.B. Teplow, P. Parchi, J.K. Teller, P. Gambetti, and L. Autilio-Gambetti Truncated forms of the human prion protein in normal brain and in prion diseases J. Biol. Chem. 270 1995 19173 19180
17. J. Collinge Variant Creutzfeldt-Jakob disease Lancet 354 1999 317 323
18. J. Collinge Prion diseases of humans and animals: their causes and molecular basis Annu. Rev. Neurosci. 24 2001 519 550
19. A.A. Cunningham, J.K. Kirkwood, M. Dawson, Y.I. Spencer, R.B. Green, and G.A. Wells Bovine spongiform encephalopathy infectivity in greater kudu (Tragelaphus strepsiceros) Emerg. Infect. Dis. 10 2004 1044 1049
20. M. Daniels, G.M. Cereghetti, and D.R. Brown Toxicity of novel C-terminal prion protein fragments and peptides harbouring disease-related C-terminal mutations Eur. J. Biochem. 268 2001 6155 6164
21. A.D. Elbein Glycosidase inhibitors: inhibitors of N-linked oligosaccharide processing FASEB J. 5 1991 3055 3063
22. P.T. Englund The structure and biosynthesis of glycosyl phosphatidylinositol protein anchors Annu. Rev. Biochem. 62 1993 121 138
23. M. Ettaiche, R. Pichot, J.P. Vincent, and J. Chabry In vivo cytotoxicity of the prion protein fragment 106-126 J. Biol. Chem. 275 2000 36487 36490
24. G. Forloni, N. Angeretti, R. Chiesa, E. Monzani, M. Salmona, O. Bugiani, and F. Tagliavini Neurotoxicity of a prion protein fragment Nature 362 1993 543 546
25. J.M. Gabriel, B. Oesch, H. Kretzschmar, M. Scott, and S.B. Prusiner Molecular cloning of a candidate chicken prion protein Proc. Natl. Acad. Sci. U.S.A. 89 1992 9097 9101
26. G.J. Garssen, L.J. Van Keulen, C.F. Farquhar, M.A. Smits, J.G. Jacobs, A. Bossers, R.H. Meloen, and J.P. Langeveld Applicability of three anti-PrP peptide sera including staining of tonsils and brainstem of sheep with scrapie Microsc. Res. Tech. 50 2000 32 39
27. A. Gorodinsky, and D.A. Harris Glycolipid-anchored proteins in neuroblastoma cells form detergent-resistant complexes without caveolin J. Cell Biol. 129 1995 619 627
28. G. Griffiths, P. Quinn, and G. Warren Dissection of the Golgi complex I. Monensin inhibits the transport of viral membrane proteins from medial to trans Golgi cisternae in baby hamster kidney cells infected with Semliki Forest virus J. Cell Biol. 96 1983 835 850
29. G. Griffiths, and K. Simons The trans Golgi network: sorting at the exit site of the Golgi complex Science 234 1986 438 443
30. D.A. Harris Trafficking, turnover and membrane topology of PrP Br. Med. Bull. 66 2003 71 85
31. D.A. Harris, D.L. Falls, F.A. Johnson, and G.D. Fischbach A prion-like protein from chicken brain copurifies with an acetylcholine receptor-inducing activity Proc. Natl. Acad. Sci. U.S.A. 88 1991 7664 7668
32. D.A. Harris, M.T. Huber, P. van Dijken, S.L. Shyng, B.T. Chait, and R. Wang Processing of a cellular prion protein: identification of N- and C-terminal cleavage sites Biochemistry 32 1993 1009 1016
33. A.F. Hill, M. Desbruslais, S. Joiner, K.C. Sidle, I. Gowland, J. Collinge, L.J. Doey, and P. Lantos The same prion strain causes vCJD and BSE Nature 389 1997 448 450 526
34. A. Jimenez-Huete, P.M. Lievens, R. Vidal, P. Piccardo, B. Ghetti, F. Tagliavini, B. Frangione, and F. Prelli Endogenous proteolytic cleavage of normal and disease-associated isoforms of the human prion protein in neural and non-neural tissues Am. J. Pathol. 153 1998 1561 1572
35. S.C. Kang, R. Li, C. Wang, T. Pan, T. Liu, R. Rubenstein, G. Barnard, B.S. Wong, and M.S. Sy Guanidine hydrochloride extraction and detection of prion proteins in mouse and hamster prion diseases by ELISA J. Pathol. 199 2003 534 541
36. R.D. Klausner, J.G. Donaldson, and J. Lippincott-Schwartz Brefeldin A: insights into the control of membrane traffic and organelle structure J. Cell Biol. 116 1992 1071 1080
37. S. Lammich, E. Kojro, R. Postina, S. Gilbert, R. Pfeiffer, M. Jasionowski, C. Haass, and F. Fahrenholz Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease Proc. Natl. Acad. Sci. U.S.A. 96 1999 3922 3927
38. S. Lehmann, and D.A. Harris A mutant prion protein displays an aberrant membrane association when expressed in cultured cells J. Biol. Chem. 270 1995 24589 24597
39. R. Li, D. Liu, G. Zanusso, T. Liu, J.D. Fayen, J.H. Huang, R.B. Petersen, P. Gambetti, and M.S. Sy The expression and potential function of cellular prion protein in human lymphocytes Cell. Immunol. 207 2001 49 58
40. R. Li, T. Liu, B.S. Wong, T. Pan, M. Morillas, W. Swietnicki, K. O'Rourke, P. Gambetti, W.K. Surewicz, and M.S. Sy Identification of an epitope in the C terminus of normal prion protein whose expression is modulated by binding events in the N terminus J. Mol. Biol. 301 2000 567 573
41. P. Liljestrom, and H. Garoff A new generation of animal cell expression vectors based on the Semliki Forest virus replicon Biotechnology (N. Y.) 9 1991 1356 1361
42. T. Liu, T. Zwingman, R. Li, T. Pan, B.S. Wong, R.B. Petersen, P. Gambetti, K. Herrup, and M.S. Sy Differential expression of cellular prion protein in mouse brain as detected with multiple anti-PrP monoclonal antibodies Brain Res. 896 2001 118 129
43. E. Lopez-Perez, Y. Zhang, S.J. Frank, J. Creemers, N. Seidah, and F. Checler Constitutive alpha-secretase cleavage of the beta-amyloid precursor protein in the furin-deficient LoVo cell line: involvement of the pro-hormone convertase 7 and the disintegrin metalloprotease ADAM10 J. Neurochem. 76 2001 1532 1539
44. X. Lu, and J. Silver Ecotropic murine leukemia virus receptor is physically associated with caveolin and membrane rafts Virology 276 2000 251 258
45. A. Mange, F. Beranger, K. Peoc'h, T. Onodera, Y. Frobert, and S. Lehmann Alpha- and beta-cleavages of the amino-terminus of the cellular prion protein Biol. Cell 96 2004 125 132
46. R. Narwa, and D.A. Harris Prion proteins carrying pathogenic mutations are resistant to phospholipase cleavage of their glycolipid anchors Biochemistry 38 1999 8770 8777
47. A. Negro, C. Ballarin, A. Bertoli, M.L. Massimino, and M.C. Sorgato The metabolism and imaging in live cells of the bovine prion protein in its native form or carrying single amino acid substitutions Mol. Cell. Neurosci. 17 2001 521 538
48. M. Nunziante, S. Gilch, and H.M. Schatzl Essential role of the prion protein N terminus in subcellular trafficking and half-life of cellular prion protein J. Biol. Chem. 278 2003 3726 3734
49. Pan, K.M., Stahl, N., Prusiner, S.B., 1992. Purification and properties of the cellular prion protein from Syrian hamster brain. In: Micke's Protocols Binder, vol. 1, pp. 1343-1352.
50. T. Pan, R. Li, B.S. Wong, T. Liu, P. Gambetti, and M.S. Sy Heterogeneity of normal prion protein in two-dimensional immunoblot: presence of various glycosylated and truncated forms J. Neurochem. 81 2002 1092 1101
51. E. Paramithiotis, M. Pinard, T. Lawton, S. LaBoissiere, V.L. Leathers, W.Q. Zou, L.A. Estey, J. Lamontagne, M.T. Lehto, L.H. Kondejewski, G.P. Francoeur, M. Papadopoulos, A. Haghighat, S.J. Spatz, M. Head, R. Will, J. Ironside, K. O'Rourke, Q. Tonelli, H.C. Ledebur, A. Chakrabartty, and N.R. Cashman A prion protein epitope selective for the pathologically misfolded conformation Nat. Med. 9 2003 893 899
52. P. Parizek, C. Roeckl, J. Weber, E. Flechsig, A. Aguzzi, and A.J. Raeber Similar turnover and shedding of the cellular prion protein in primary lymphoid and neuronal cells J. Biol. Chem. 276 2001 44627 44632
53. E.T. Parkin, N.T. Watt, A.J. Turner, and N.M. Hooper Dual mechanisms for shedding of the cellular prion protein. J. Biol. Chem. 279 2004 11170 11178 Epub 2004 Jan 7
54. F. Perini, B. Frangione, and F. Prelli Prion protein released by platelets Lancet 347 1996 1635 1636
55. S.B. Prusiner Prions Proc. Natl. Acad. Sci. U.S.A. 95 1998 13363 13383
56. P.M. Rudd, T. Endo, C. Colominas, D. Groth, S.F. Wheeler, D.J. Harvey, M.R. Wormald, H. Serban, S.B. Prusiner, A. Kobata, and R.A. Dwek Glycosylation differences between the normal and pathogenic prion protein isoforms Proc. Natl. Acad. Sci. U.S.A. 96 1999 13044 13049
57. S.L. Shyng, J.E. Heuser, and D.A. Harris A glycolipid-anchored prion protein is endocytosed via clathrin-coated pits J. Cell. Biol. 125 1994 1239 1250
58. S.L. Shyng, M.T. Huber, and D.A. Harris A prion protein cycles between the cell surface and an endocytic compartment in cultured neuroblastoma cells J. Biol. Chem. 268 1993 15922 15928
59. S.L. Shyng, K.L. Moulder, A. Lesko, and D.A. Harris The N-terminal domain of a glycolipid-anchored prion protein is essential for its endocytosis via clathrin-coated pits J. Biol. Chem. 270 1995 14793 14800
60. C.J. Sigurdson, and M.W. Miller Other animal prion diseases Br. Med. Bull. 66 2003 199 212
61. D.M. Skovronsky, D.B. Moore, M.E. Milla, R.W. Doms, and V.M. Lee Protein kinase C-dependent alpha-secretase competes with beta-secretase for cleavage of amyloid-beta precursor protein in the trans-golgi network J. Biol. Chem. 275 2000 2568 2575
62. N. Stahl, M.A. Baldwin, A.L. Burlingame, and S.B. Prusiner Identification of glycoinositol phospholipid linked and truncated forms of the scrapie prion protein Biochemistry 29 1990 8879 8884
63. N. Stahl, D.R. Borchelt, K. Hsiao, and S.B. Prusiner Scrapie prion protein contains a phosphatidylinositol glycolipid Cell 51 1987 229 240
64. M. Suomalainen, K. Hultenby, and H. Garoff Targeting of Moloney murine leukemia virus gag precursor to the site of virus budding J. Cell. Biol. 135 1996 1841 1852
65. S.J. Tabrizi, C.L. Elliott, and C. Weissmann Ethical issues in human prion diseases Br. Med. Bull. 66 2003 305 316
66. F. Tagliavini, F. Prelli, M. Porro, M. Salmona, O. Bugiani, and B. Frangione A soluble form of prion protein in human cerebrospinal fluid: implications for prion-related encephalopathies Biochem. Biophys. Res. Commun. 184 1992 1398 1404
67. K. Takekida, Y. Kikuchi, T. Yamazaki, M. Horiuchi, T. Kakeya, M. Shinagawa, K. Takatori, A. Tanimura, K. Tanamoto, and J. Sawada Quantitative analysis of prion protein by immunoblotting J. Health Sci. 48 2002 288 291
68. A. Taraboulos, M. Scott, A. Semenov, D. Avrahami, L. Laszlo, S.B. Prusiner, and D. Avraham Cholesterol depletion and modification of COOH-terminal targeting sequence of the prion protein inhibit formation of the scrapie isoform J. Cell. Biol. 129 1995 121 132
69. A. Taraboulos, D. Serban, and S.B. Prusiner Scrapie prion proteins accumulate in the cytoplasm of persistently infected cultured cells J. Cell. Biol. 110 1990 2117 2132
70. A.M. Tartakoff Perturbation of vesicular traffic with the carboxylic ionophore monensin Cell 32 1983 1026 1028
71. L.J. van Keulen, B.E. Schreuder, R.H. Meloen, M. Poelen-van den Berg, G. Mooij-Harkes, M.E. Vromans, and J.P. Langeveld Immunohistochemical detection and localization of prion protein in brain tissue of sheep with natural scrapie Vet. Pathol. 32 1995 299 308
72. M. Vey, S. Pilkuhn, H. Wille, R. Nixon, S.J. DeArmond, E.J. Smart, R.G. Anderson, A. Taraboulos, and S.B. Prusiner Subcellular colocalization of the cellular and scrapie prion proteins in caveolae-like membranous domains Proc. Natl. Acad. Sci. U.S.A. 93 1996 14945 14949
73. B. Vincent, E. Paitel, Y. Frobert, S. Lehmann, J. Grassi, and F. Checler Phorbol ester-regulated cleavage of normal prion protein in HEK293 human cells and murine neurons J. Biol. Chem. 275 2000 35612 35616
74. B. Vincent, E. Paitel, P. Saftig, Y. Frobert, D. Hartmann, B. De Strooper, J. Grassi, E. Lopez-Perez, and F. Checler The disintegrins ADAM10 and TACE contribute to the constitutive and phorbol ester-regulated normal cleavage of the cellular prion protein J. Biol. Chem. 276 2001 37743 37746
75. D. Volkel, K. Zimmermann, I. Zerr, M. Bodemer, T. Lindner, P.L. Turecek, S. Poser, and H.P. Schwarz Immunochemical determination of cellular prion protein in plasma from healthy subjects and patients with sporadic CJD or other neurologic diseases Transfusion 41 2001 441 448
76. C. Wegner, A. Romer, R. Schmalzbauer, H. Lorenz, O. Windl, and H.A. Kretzschmar Mutant prion protein acquires resistance to protease in mouse neuroblastoma cells J. Gen. Virol. 83 2002 1237 1245
77. D. Wessel, and U.I. Flugge A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids Anal. Biochem. 138 1984 141 143
78. R.A. Williamson, D. Peretz, C. Pinilla, H. Ball, R.B. Bastidas, R. Rozenshteyn, R.A. Houghten, S.B. Prusiner, and D.R. Burton Mapping the prion protein using recombinant antibodies J. Virol. 72 1998 9413 9418
79. R. Yadavalli, R.P. Guttmann, T. Seward, A.P. Centers, R.A. Williamson, and G.C. Telling Calpain-dependent endoproteolytic cleavage of PrPSc modulates scrapie prion propagation J. Biol. Chem. 279 2004 21948 21956
80. H. Zhao, and H. Garoff Role of cell surface spikes in alphavirus budding J. Virol. 66 1992 7089 7095