Biochemical properties of highly neuroinvasive prion strains

PLoS Pathogens

Volumn 8, Issue 2, 2012, Pages

  Bett, Cyrus ^a   Joshi Barr, Shivanjali ^a   Lucero, Melanie ^a   Trejo, Margarita ^a   Liberski, Pawel ^b   Kelly, Jeffery W ^c   Masliah, Eliezer ^a   Sigurdson, Christina J ^a,d  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MEDICAL UNIVERSITY OF LODZ   (Poland)

^c SCRIPPS RESEARCH INSTITUTE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOCHEMISTRY; BRAIN; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; ELECTROPHORETIC MOBILITY; INCUBATION TIME; MOUSE; NONHUMAN; PHENOTYPE; PRION; PROTEIN DEGRADATION; VIRUS REPLICATION; VIRUS STRAIN; AMYLOID PLAQUE; ANIMAL; CHEMISTRY; METABOLISM; PATHOGENICITY; PATHOLOGY; PRION DISEASE;

PRION PROTEIN;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM; MICE; PLAQUE, AMYLOID; PRION DISEASES; PRIONS; PRPSC PROTEINS;

EID: 84860903170     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002522     Document Type: Article

References (70)

1. Aguzzi A, Polymenidou M, (2004) Mammalian prion biology. One century of evolving concepts. Cell 116: 313-327.
2. Prusiner SB, (1982) Novel proteinaceous infectious particles cause scrapie. Science 216: 136-144.
3. Deleault NR, Harris BT, Rees JR, Supattapone S, (2007) Formation of native prions from minimal components in vitro. Proc Natl Acad Sci U S A 104: 9741-9746.
4. Wang F, Wang X, Yuan CG, Ma J, (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327: 1132-1135.
5. Makarava N, Kovacs GG, Bocharova O, Savtchenko R, Alexeeva I, et al. (2010) Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol 119: 177-187.
6. Fraser H, Dickinson AG, (1968) The sequential development of the brain lesion of scrapie in three strains of mice. J Comp Pathol 78: 301-311.
7. Fraser H, Dickinson AG, (1973) Scrapie in mice. Agent-strain differences in the distribution and intensity of grey matter vacuolation. J Comp Pathol 83: 29-40.
8. Bruce ME, McBride PA, Farquhar CF, (1989) Precise targeting of the pathology of the sialoglycoprotein, PrP, and vacuolar degeneration in mouse scrapie. Neurosci Lett 102: 1-6.
9. Collinge J, Clarke AR, (2007) A general model of prion strains and their pathogenicity. Science 318: 930-936.
10. Telling GC, (2011) Transgenic mouse models and prion strains. Top Curr Chem 305: 79-99.
11. Bessen RA, Marsh RF, (1992) Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J Virol 66: 2096-2101.
12. Hill AF, Joiner S, Beck JA, Campbell TA, Dickinson A, et al. (2006) Distinct glycoform ratios of protease resistant prion protein associated with PRNP point mutations. Brain 129: 676-685.
13. Safar J, Wille H, Itri V, Groth D, Serban H, et al. (1998) Eight prion strains have PrPSc molecules with different conformations. Nat Med 4: 1157-1165.
14. Peretz D, Williamson RA, Legname G, Matsunaga Y, Vergara J, et al. (2002) A change in the conformation of prions accompanies the emergence of a new prion strain. Neuron 34: 921-932.
15. Smirnovas V, Baron GS, Offerdahl DK, Raymond GJ, Caughey B, et al. (2011) Structural organization of brain-derived mammalian prions examined by hydrogen-deuterium exchange. Nat Struct Mol Biol 18: 504-506.
16. Bruce ME, McConnell I, Fraser H, Dickinson AG, (1991) The disease characteristics of different strains of scrapie in Sinc congenic mouse lines: implications for the nature of the agent and host control of pathogenesis. J Gen Virol 72: 595-603.
17. Legname G, Nguyen HO, Peretz D, Cohen FE, DeArmond SJ, et al. (2006) Continuum of prion protein structures enciphers a multitude of prion isolate-specified phenotypes. Proc Natl Acad Sci U S A 103: 19105-19110.
18. Ayers JI, Schutt CR, Shikiya RA, Aguzzi A, Kincaid AE, et al. (2011) The strain-encoded relationship between PrP replication, stability and processing in neurons is predictive of the incubation period of disease. PLoS Pathog 7: e1001317.
19. Silveira JR, Raymond GJ, Hughson AG, Race RE, Sim VL, et al. (2005) The most infectious prion protein particles. Nature 437: 257-261.
20. Tixador P, Herzog L, Reine F, Jaumain E, Chapuis J, et al. (2010) The physical relationship between infectivity and prion protein aggregates is strain-dependent. PLoS Pathog 6: e1000859.
21. Tzaban S, Friedlander G, Schonberger O, Horonchik L, Yedidia Y, et al. (2002) Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes. Biochemistry 41: 12868-12875.
22. Pastrana MA, Sajnani G, Onisko B, Castilla J, Morales R, et al. (2006) Isolation and Characterization of a Proteinase K-Sensitive PrP(Sc) Fraction. Biochemistry 45: 15710-15717.
23. Safar JG, Geschwind MD, Deering C, Didorenko S, Sattavat M, et al. (2005) Diagnosis of human prion disease. Proc Natl Acad Sci U S A 102: 3501-3506.
24. Kimberlin RH, Walker CA, (1988) Incubation periods in six models of intraperitoneally injected scrapie depend mainly on the dynamics of agent replication within the nervous system and not the lymphoreticular system. J Gen Virol 69: 2953-2960.
25. Klein MA, Frigg R, Raeber AJ, Flechsig E, Hegyi I, et al. (1998) PrP expression in B lymphocytes is not required for prion neuroinvasion. Nat Med 4: 1429-1433.
26. Glatzel M, Aguzzi A, (2000) PrP(C) expression in the peripheral nervous system is a determinant of prion neuroinvasion. J Gen Virol 81: 2813-2821.
27. Glatzel M, Heppner FL, Albers KM, Aguzzi A, (2001) Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 31: 25-34.
28. Haik S, Faucheux BA, Sazdovitch V, Privat N, Kemeny JL, et al. (2003) The sympathetic nervous system is involved in variant Creutzfeldt-Jakob disease. Nat Med 9: 1121-1122.
29. Bartz JC, Kincaid AE, Bessen RA, (2002) Retrograde transport of transmissible mink encephalopathy within descending motor tracts. J Virol 76: 5759-5768.
30. Bartz JC, Kincaid AE, Bessen RA, (2003) Rapid prion neuroinvasion following tongue infection. J Virol 77: 583-591.
31. Prinz M, Heikenwalder M, Junt T, Schwarz P, Glatzel M, et al. (2003) Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature 425: 957-962.
32. Kimberlin RH, Walker CA, (1989) Pathogenesis of scrapie in mice after intragastric infection. Virus Res 12: 213-220.
33. Beekes M, McBride PA, Baldauf E, (1998) Cerebral targeting indicates vagal spread of infection in hamsters fed with scrapie. J Gen Virol 79 Part 3: 601-607.
34. Kimberlin RH, Walker CA, (1986) Pathogenesis of scrapie (strain 263 K) in hamsters infected intracerebrally, intraperitoneally or intraocularly. J Gen Virol 67: 255-263.
35. Mabbott NA, Bruce ME, Botto M, Walport MJ, Pepys MB, (2001) Temporary depletion of complement component C3 or genetic deficiency of C1q significantly delays onset of scrapie. Nat Med 7: 485-487.
36. Klein MA, Kaeser PS, Schwarz P, Weyd H, Xenarios I, et al. (2001) Complement facilitates early prion pathogenesis. Nat Med 7: 488-492.
37. Zabel MD, Heikenwalder M, Prinz M, Arrighi I, Schwarz P, et al. (2007) Stromal complement receptor CD21/35 facilitates lymphoid prion colonization and pathogenesis. J Immunol 179: 6144-6152.
38. Collis SC, Kimberlin RH, (1985) Long-term persistence of scrapie infection in mouse spleens in the absence of clinical disease. FEMS Microbiol Lett 29: 111-114.
39. Moore RC, Hope J, McBride PA, McConnell I, Selfridge J, et al. (1998) Mice with gene targetted prion protein alterations show that Prnp, Sinc and Prni are congruent. Nat Genet 18: 118-125.
40. Mabbott NA, McGovern G, Jeffrey M, Bruce ME, (2002) Temporary blockade of the tumor necrosis factor receptor signaling pathway impedes the spread of scrapie to the brain. J Virol 76: 5131-5139.
41. Mabbott NA, Williams A, Farquhar CF, Pasparakis M, Kollias G, et al. (2000) Tumor necrosis factor alpha-deficient, but not interleukin-6-deficient, mice resist peripheral infection with scrapie. J Virol 74: 3338-3344.
42. Mabbott NA, Young J, McConnell I, Bruce ME, (2003) Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility. J Virol 77: 6845-6854.
43. Sadowski MJ, Pankiewicz J, Prelli F, Scholtzova H, Spinner DS, et al. (2009) Anti-PrP Mab 6D11 suppresses PrP(Sc) replication in prion infected myeloid precursor line FDC-P1/22 L and in the lymphoreticular system in vivo. Neurobiol Dis 34: 267-278.
44. Godsave SF, Wille H, Kujala P, Latawiec D, DeArmond SJ, et al. (2008) Cryo-immunogold electron microscopy for prions: toward identification of a conversion site. J Neurosci 28: 12489-12499.
45. Jeffrey M, Goodsir CM, Bruce ME, McBride PA, Fraser JR, (1997) In vivo toxicity of prion protein in murine scrapie: ultrastructural and immunogold studies. Neuropathol Appl Neurobiol 23: 93-101.
46. Peretz D, Scott MR, Groth D, Williamson RA, Burton DR, et al. (2001) Strain-specified relative conformational stability of the scrapie prion protein. Protein Sci 10: 854-863.
47. Tanaka M, Chien P, Naber N, Cooke R, Weissman JS, (2004) Conformational variations in an infectious protein determine prion strain differences. Nature 428: 323-328.
48. Mabbott NA, MacPherson GG, (2006) Prions and their lethal journey to the brain. Nat Rev Microbiol 4: 201-211.
49. Beringue V, Le Dur A, Tixador P, Reine F, Lepourry L, et al. (2008) Prominent and persistent extraneural infection in human PrP transgenic mice infected with variant CJD. PLoS ONE 3: e1419.
50. Klingeborn M, Race B, Meade-White KD, Rosenke R, Striebel JF, et al. (2011) Crucial role for prion protein membrane anchoring in the neuroinvasion and neural spread of prion infection. J Virol 85: 1484-1494.
51. Caughey B, Lansbury PT Jr, (2003) Protofibrils, Pores, Fibrils, and Neurodegeneration: Separating the Responsible Protein Aggregates from the Innocent Bystanders. Annu Rev Neurosci 26: 267-98.
52. Wadsworth JD, Asante EA, Desbruslais M, Linehan JM, Joiner S, et al. (2004) Human prion protein with valine 129 prevents expression of variant CJD phenotype. Science 306: 1793-1796.
53. Piccardo P, Manson JC, King D, Ghetti B, Barron RM, (2007) Accumulation of prion protein in the brain that is not associated with transmissible disease. Proc Natl Acad Sci U S A 104: 4712-4717.
54. Montrasio F, Frigg R, Glatzel M, Klein MA, Mackay F, et al. (2000) Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 288: 1257-1259.
55. Mabbott NA, Mackay F, Minns F, Bruce ME, (2000) Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie [letter]. Nat Med 6: 719-720.
56. Bruce ME, (1985) Agent replication dynamics in a long incubation period model of mouse scrapie. J Gen Virol 66: 2517-2522.
57. Cronier S, Gros N, Tattum MH, Jackson GS, Clarke AR, et al. (2008) Detection and characterization of proteinase K-sensitive disease-related prion protein with thermolysin. Biochem J 416: 297-305.
58. Kim C, Haldiman T, Cohen Y, Chen W, Blevins J, et al. (2011) Protease-sensitive conformers in broad spectrum of distinct PrPSc structures in sporadic Creutzfeldt-Jakob disease are indicator of progression rate. PLoS Pathog 7: e1002242.
59. Thackray AM, Hopkins L, Klein MA, Bujdoso R, (2007) Mouse-adapted ovine scrapie prion strains are characterized by different conformers of PrPSc. J Virol 81: 12119-12127.
60. Schutz AK, Soragni A, Hornemann S, Aguzzi A, Ernst M, et al. (2011) The amyloid-Congo red interface at atomic resolution. Angew Chem Int Ed Engl 50: 5956-5960.
61. Prusiner SB, McKinley MP, Bowman KA, Bolton DC, Bendheim PE, et al. (1983) Scrapie prions aggregate to form amyloid-like birefringent rods. Cell 35: 349-358.
62. McKinley MP, Meyer RK, Kenaga L, Rahbar F, Cotter R, et al. (1991) Scrapie prion rod formation in vitro requires both detergent extraction and limited proteolysis. J Virol 65: 1340-1351.
63. Sigurdson CJ, Manco G, Schwarz P, Liberski P, Hoover EA, et al. (2006) Strain fidelity of chronic wasting disease upon murine adaptation. J Virol 80: 12303-12311.
64. Tanaka M, Collins SR, Toyama BH, Weissman JS, (2006) The physical basis of how prion conformations determine strain phenotypes. Nature 442: 585-589.
65. Derdowski A, Sindi SS, Klaips CL, DiSalvo S, Serio TR, (2010) A size threshold limits prion transmission and establishes phenotypic diversity. Science 330: 680-683.
66. Knowles TP, Waudby CA, Devlin GL, Cohen SI, Aguzzi A, et al. (2009) An analytical solution to the kinetics of breakable filament assembly. Science 326: 1533-1537.
67. Sigurdson CJ, Nilsson KP, Hornemann S, Heikenwalder M, Manco G, et al. (2009) De novo generation of a transmissible spongiform encephalopathy by mouse transgenesis. Proc Natl Acad Sci U S A 106: 304-309.
68. Taraboulos A, Jendroska K, Serban D, Yang SL, DeArmond SJ, et al. (1992) Regional mapping of prion proteins in brain. Proc Natl Acad Sci U S A 89: 7620-7624.
69. Polymenidou M, Moos R, Scott M, Sigurdson C, Shi YZ, et al. (2008) The POM monoclonals: a comprehensive set of antibodies to non-overlapping prion protein epitopes. PLoS ONE 3: e3872.
70. Wadsworth JDF, Joiner S, Hill AF, Campbell TA, Desbruslais M, et al. (2001) Tissue distribution of protease resistant prion protein in variant CJD using a highly sensitive immuno-blotting assay. Lancet 358: 171-180.