Endogenous proteolytic cleavage of normal and disease-associated isoforms of the human prion protein in neural and non-neural tissues

American Journal of Pathology

Volumn 153, Issue 5, 1998, Pages 1561-1572

  Jiménez Huete, Adolfo ^a   Lievens, Patricia M J ^b   Vidal, Rubén ^a   Piccardo, Pedro ^c   Ghetti, Bernardino ^c   Tagliavini, Fabrizio ^b   Frangione, Blas ^a   Prelli, Frances ^a  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b DEPARTMENT OF NEUROSURGERY   (Italy)

^c INDIANA UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; METALLOPROTEINASE; PRION PROTEIN; PROTEINASE;

ARTICLE; CONTROLLED STUDY; CREUTZFELDT JAKOB DISEASE; DISEASE CLASSIFICATION; GENETIC POLYMORPHISM; GERSTMANN STRAUSSLER SCHEINKER SYNDROME; GLYCOSYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOREACTIVITY; NEUROPATHOLOGY; NEUROTROPISM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION;

EID: 0031765769     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0002-9440(10)65744-6     Document Type: Article

References (61)

1. Stahl N, Borchelt DR, Prusiner SB: Differential release of cellular and scrapie prion proteins from cellular membranes by phosphatidylinositol-specific phospholipase. Biochemistry 1990, 29:5405-5412
2. Robakis NK, Devine-Gage EA, Jenkins EC, Kascak RJ, Brown WT, Krawczun MS, Silverman WP: Localization of a human gene homologous to the PrP gene on the p arm of chromosome 20 and detection of PrP-related antigens in normal brain. Biochem Biophys Res Commun 1986, 140:758-765
3. Bendheim PE, Brown HR, Rudelli RD, Scala LJ, Goller NL, Wen GY, Kascak RJ, Cashman NR, Bolton DC: Nearly ubiquitous tissue distribution of the scrapie agent precursor protein. Neurology 1992, 42: 149-156
4. Kretzschmar HA, Prusiner SB, Stowring LE, DeArmond SJ: Scrapie prion proteins are synthesized in neurons. Am J Pathol 1986, 722:1-5
5. Hope J, Morton LDJ, Farquhar CF, Multhraup G, Beyreuther K, Kimberlin RH: The major polypeptide of scrapie-associated fibrils (SAF) has the same size, charge, distribution and N-terminal protein sequence as predicted for the normal brain protein (PrP). EMBO J 1986, 5:2591-2597
6. 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 1988, 85:9811-9815
7. Wion D, Le Bert M, Brachet P: Messenger RNAs of beta-amyloid precursor protein and prion protein are regulated by nerve growth factor in PC12 cells. Int J Dev Neurosci 1988, 6:387-393
8. Cashman NR, Loertscher R, Nalbantoglu J, Shaw I, Kascak RJ, Bolton DC, Bendheim PE: Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell 1990, 61:185-192
9. Collinge J, Whittington MA, Sidle KC, Smith CJ, Palmer MS, Clarke AR, Jefferys JG: Prion protein is necessary for normal synaptic function. Nature 1994, 370:295-297
10. Tobler I, Gaus SE, Deboer T, Achermann P, Fischer M, Rülicke T, Moser M, Oesch B, McBride PA, Manson JC: Altered circadian activity rhythms and sleep in mice devoid of prion protein. Nature 1996, 380:639-642
11. Yehiely F, Bamborough P, Da Costa M, Perry BJ, Thinakaran G, Cohen FE, Carlson GA, Prusiner SB: Identification of candidate proteins binding to prion protein. Neurobiol Dis 1997, 3:339-355
12. Budka H, Aguzzi A, Brown P, Brucher JM, Bugiani O, Gullotta F, Haltia M, Hauw JJ, Ironside JW, Jellinger K, Kretzschmar HA, Lantos PL, Masullo C, Schlote W, Tateishi J, Weller RO: Neurological diagnostic criteria for Creutzfeldt-Jakob disease (CJD) and other human spongiform encephalopathies (prion diseases). Brain Pathol 1995, 5:459-466
13. Prusiner SB: Molecular biology and pathogenesis of prion diseases. Trends Biochem Sci 1996, 21:482-487
14. Bolton DC, McKinley MP, Prusiner SB: Identification of a protein that purifies with the scrapie prion. Science 1982, 218:1309-1311
15. Oesch B, Westaway D, Wälchli M, McKinley MP, Kent SBH, Aebersold R, Barry RA, Tempst P, Teplow DB, Hood LE, Prusiner SB, Weissman C: A cellular gene encodes scrapie PrP 27-30 protein. Cell 1985, 40:735-746
16. Meyer RK, McKinley MP, Bowman KA, Braunfeld MB, Barry RA, Prusiner SB: Separation and properties of cellular and scrapie prion protein. Proc Natl Acad Sci USA 1986, 83:2310-2314
17. Borchelt DR, Scott M, Taraboulos A, Stahl N, Prusiner SB: Scrapie and cellular prion protein differ in their kinetics of synthesis and topology in cultured cells. J Cell Biol 1990, 110:743-752
18. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, Mehlhorn I, Huang Z, Fletterick RJ, Cohen FE, Prusiner SB: Conversion of alpha-helices into beta-sheets features in the formation of scrapie prion proteins. Proc Natl Acad Sci USA 1993, 90:10962-10966
19. Palmer MS, Dryden AJ, Hughes JT, Collinge J: Homozygous prion protein genotype predisposes to sporadic Creutzfeldt-Jakob disease. Nature 1991, 352:340-342
20. Collinge J, Palmer MS, Dryden AJ: Genetic predisposition to iatrogenic Creutzfeldt-Jakob disease. Lancet 1991, 337:1441-1442
21. Goldfarb LG, Petersen RB, Tabaton M, Brown P, LeBlanc AC, Montagna P, Cortelli P, Julien J, Vital C, Pendelbury WW, Haltia M, Wills PR, Hauw JJ, McKeever PE, Monari L, Schrank B, Swergold GD, Autilio-Gambetti L, Gajdusek DC, Lugaresi E, Gambetti P: Fatal familial insomnia and familial Creutzfeldt-Jakob disease: disease phenotype determined by a DNA polymorphism. Science 1992, 258:806-808
22. Prusiner SB: Inherited prion diseases. Proc Natl Acad Sci USA 1994, 91:4611-4614
23. Collinge J, Sidle KC, Meads J, Ironside J, Hill AF: Molecular analysis of prion strain variation and the aetiology of "new variant' CJD. Nature 1996, 383:685-690
24. Telling GC, Scott M, Mastrianni J, Gabizon R, Torchia M, Cohen FE, DeArmond SJ, Prusiner SB: Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 1995, 83:79-90
25. Telling GC, Scott M, Hsiao KK, Foster D, Yang SL, Torchia M, Sidle KC, Collinge J, DeArmond SJ, Prusiner SB: Transmission of Creutzfeldt-Jakob disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proc Natl Acad Sci USA 1994, 91:9936-9940
26. Chen SG, Teplow DS, Parchi P, Teller JK, Gambetti P, Autilio-Gambetti L: Truncated forms of the human prion protein in normal brain and in prion diseases. J Biol Chem 1995, 270:19173-19180
27. Gasset M, Baldwin MA, Lloyd DH, Gabriel JM, Holtzman DM, Cohen F, Fletterick R, Prusiner SB: Predicted alpha-helical regions of the prion protein when synthesized as peptides form amyloid. Proc Natl Acad Sci USA 1992, 89:10940-10944
28. Huang Z, Prusiner SB, Cohen FE: Scrapie prions: a three-dimensional model of an infectious fragment Fold Des 1996, 1:13-19
29. Peretz D, Williamson RA, Matsunaga Y, Serban H, Pinilla C, Bastidas RB, Rozenshteyn R, James TL, Houghten RA, Cohen FE, Prusiner SB, Burton DR: A conformational transition at the N terminus of the prion protein features in formation of the scrapie isoform. J Mol Biol 1997, 273:614-622
30. James TL, Liu H, Ulyanov NB, Farr-Jones S, Zhang H, Donne DG, Kaneko K, Groth D, Mehlhorn I, Prusiner SB, Cohen FE: Solution structure of a 142-residue recombinant prion protein corresponding to the infectious fragment of the scrapie isoform. Proc Natl Acad Sci USA 1997, 94:10086-10091
31. Parchi P, Castellani R, Capellari S, Ghetti B, Young K, Chen SG, Farlow M, Dickson DW, Sima AAF, Trojanowski JQ, Petersen RB, Gambetti P: Molecular basis of phenotypic variability in sporadic Creutzfeldt-Jakob disease. Ann Neurol 1996, 39:767-778
32. Gearing M, Mirra SS, Hedreen JC, Sumi SM, Hansen LA, Heyman A: The consortium to establish a registry for Alzheimer's disease (CERAD). X. Neuropathology confirmation of the clinical diagnosis of Alzheimer's disease. Neurology 1995, 45:461-466
33. Schlossmacher MG, Ostaszeweski BL, Hecker LI, Celi A, Haas C, Chin D, Lieberburg I, Furie BC, Selkoe DJ: Detection of distinct isoform patterns of the beta-amyloid precursor protein in human platelets and lymphocytes. Neurobiol Aging 1992, 13:421-434
34. Dlouhy SR, Hsiao K, Farlow MR, Foroud T, Conneally PM, Johnson P, Prusiner SB, Hodes ME, Ghetti B: Linkage of the Indiana kindred of Gerstmann-Sträussler-Scheinker disease to the prion protein gene. Nature Genet 1992, 1:64-67
35. Bolton DC, Seligman SJ, Bablanian G, Windsor D, Scala LJ, Kim KS, Chen CM, Kascak RJ, Bendheim PE: Molecular location of a species-specific epitope on the hamster scrapie agent protein. J Virology 1991, 65:3667-3675
36. Xi YG, Cardone F, Pocchiari M: Detection of proteinase-resistant protein (PrP) in small brain tissue samples from Creutzfeldt-Jakob disease patients. J Neurol Sci 1994, 124:171-173
37. Fischer M, Rülicke T, Raeber A, Sailer A, Moser M, Oesch B, Brandner S, Aguzzi A, Weissmann C: Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J 1996, 15:1255-1264
38. Haraguchi T, Fisher S, Olofsson S, Endo T, Groth D, Tarantino A, Borchelt DR, Teplow DB, Hood L, Burlingame A, Lycke E, Kobata A, Prusiner SB: Asparagine-linked glycosylation of the scrapie and cellular prion proteins. Arch Biochem Biophys 1989, 274:1-13
39. Piccardo P, Seiler C, Dlouhy SR, Young K, Farlow MR, Prelli F, Frangione B, Bugiani O, Tagliavini F, Ghetti B: Proteinase-K resistant prion protein isoforms in Gerstmann-Sträussler-Scheinker disease (Indiana kindred). J Neuropathol Exp Neurol 1996, 55:1157-1163
40. Medori R, Tritschler HJ, LeBlanc A, Villare F, Manetto V, Chen HY, Xue R, Leal S, Montagna P, Cortelli P, Tinuper P, Avoni P, Mochi M, Baruzzi A, Hauw JJ, Ott J, Lagaresi E, Autilio-Gambetti L, Gambetti P: Fatal familial insomnia, a prion disease with a mutation at codon 178 of the prion protein gene. N Engl J Med 1992, 326:444-449
41. Prusiner SB, Scott M, Foster D, Pan KM, Groth D, Mirenda C, Torchia M, Yang S-L, Serban D, Carlson GA, Hoppe PC, Westaway D, DeArmond S: Transgenic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 1990, 63:673-686
42. Perini F, Vidai R, Ghetti B, Tagliavini F, Frangione B, Prelli F: PrP27-30 is a normal soluble prion protein fragment released by human platelets. Biochem Biophys Res Commun 1996, 223:572-577
43. Palmer MS, Collinge J: Mutations and polymorphisms in the prion protein gene. Hum Mutat 1993, 2:168-173
44. Wisniewski T, Frangione B: Apolipoprotein E: a pathological chaperone protein in patients with cerebral and systemic amyloid. Neurosci Lett 1992, 135:235-238
45. Carlson GA, Ebeling C, Yang S-L, Telling G, Torchia M, Groth D, Westway D, DeArmond SJ, Prusiner SB: Transmission of Creutzfeldt-Jakob disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proc Natl Acad Sci USA 1994, 91:5690-5694
46. Gasset M, Baldwin MA, Fletterick RJ, Prusiner SB: Perturbation of the secondary structure of the scrapie prion protein under conditions that alter infectivity. Proc Natl Acad Sci USA 1993, 90:1-5
47. Heller J, Kolbert AC, Larsen R, Ernst M, Bekker T, Baldwin M, Prusiner SB, Pines A, Wemmer DE: Solid-state NMR studies of the prion protein H1 fragment. Protein Sci 1996, 5:1655-1661
48. Hornemann S, Korth C, Oesch B, Riek R, Wider G, Wüthrich K, Glockshuber R: Recombinant full-length murine prion protein, mPrP(23-231): purification and spectroscopic characterization. FEBS Lett 1997, 413:277-281
49. Hsiao K, Baker HF, Crow TJ, Poulter M, Owen F, Terwilliger JD, Westaway D, Ott J, Prusiner SB: Linkage of a prion protein missense variant to Gerstmann-Sträussler-Scheinker syndrome. Nature 1989, 338:342-345
50. Harris DA, Huber MT, van Dijken P, Shyng SL, Chait BT, Wang R: Processing of a cellular prion protein: identification of N- and C-terminal cleavage sites. Biochemistry 1993, 32:1009-1016
51. Singh N, Zanusso G, Chen SG, Fujioka H, Richardson S, Gambetti P, Petersen RB: Prion protein aggregation reverted by low temperature in transfected cells carrying a prion protein gene mutation. J Biol Chem 1997, 272:28461-28470
52. Miura T, Hori-i A, Takeuchi H: Metal-dependent alpha-helix formation promoted by the glycine-rich octapeptide region of prion protein. FEBS Lett 1996, 396:248-252
53. Guiroy DC, Wakayama I, Liberski PP, Gajdusek DC: Relationship of microglia and scrapie amyloid-immunoreactive plaques in kuru, Creutzfeldt-Jakob disease and Gerstmann-Sträussler syndrome. Acta Neuropathol (Berl) 1994, 87:526-530
54. Tagliavini F, Prelli F, Ghiso J, Bugiani O, Serban D, Prusiner SB, Farlow MR, Ghetti B, Frangione B: Amyloid protein of Gerstmann-Sträussler-Scheinker disease (Indiana kindred) is an 11 kd fragment of prion protein with an N-terminal glycine at codon 58. EMBO J 1991, 10:513-519
55. Tagliavini F, Prelli F, Porro M, Rossi G, Giaccone G, Farlow MR, Dlouhy SR, Ghetti B, Bugiani O, Frangione B: Amyloid fibrils in Gerstmann-Sträussler-Scheinker disease (Indiana and Swedish kindreds) express only PrP peptides encoded by the mutant allele. Cell 1994, 79:695-703
56. Forloni G, Del Bo R, Angeretti N, Chiesa R, Monzani E, Salmona M, Bugiani O, Tagliavini F: Neurotoxicity of a prion protein fragment. Nature 1993, 362:543-545
57. Tagliavini F, Prelli F, Verga L, Giaccone G, Sarma R, Gorevic P, Ghetti B, Passerini F, Ghibaudi E, Forloni G, Salmona M, Bugiani O, Frangione B: Synthetic peptides homologous to prion protein residues 106-147 form amyloid-like fibrils in vitro. Proc Natl Acad Sci USA 1993, 90:9678-9682
58. Castaño EM, Frangione B: Non-Alzheimer's disease amyloidoses of the nervous system. Curr Opin Neurol 1995, 8:279-285
59. Eklund CM, Kennedy RC, Hadlow WJ: Pathogenesis of scrapie virus infection in the mouse. J Infect Dis 1967, 117:15-22
60. DeArmond SJ, Sanchez H, Yehiely F, Qiu Y, Ninchak-Casey A, Daggett V, Camerino AP, Cayetano J, Rogers M, Groth D, Torchia M, Tremblay P, Scott MR, Cohen FE, Prusiner SB: Selective neuronal targeting in prion disease. Neuron 1997, 19:1337-1348
61. Lehmann S, Harris DA: Blockade of glycosylation promotes acquisition of scrapie-like properties by the prion protein in cultured cells. J Biol Chem 1997, 272:21479-21487