Unhampered prion neuroinvasion despite impaired fast axonal transport in transgenic mice overexpressing four-repeat tau

Journal of Neuroscience

Volumn 22, Issue 17, 2002, Pages 7471-7477

  Künzi, Valérie ^a   Glatzel, Markus ^a   Nakano, Michel Y ^b   Greber, Urs F ^b   Van Leuven, Fred ^c   Aguzzi, Adriano ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

impaired fast axonal transport; peripheral nervous system; prion neuroinvasion; tau hyperphosphorylation; tau overexpression; transmissible spongiform encephalopathy

Indexed keywords

TAU PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GERSTMANN STRAUSSLER SCHEINKER SYNDROME; MOUSE; NERVE DEGENERATION; NERVE FIBER TRANSPORT; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; SCRAPIE; TRANSGENIC MOUSE;

EID: 0036759121     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-17-07471.2002     Document Type: Article

References (40)

1. Aguzzi A, Montrasio F, Kaeser PS (2001) Prions: Health scare and biological challenge. Nat Rev Mol Cell Biol 2:118-126.
2. Beekes M, McBride PA, Baldauf E (1998) Cerebral targeting indicates vagal spread of infection in hamsters fed with scrapie. J Gen Virol 79[Pt 3]:601-607.
3. Blättler T, Brandner S, Raeber AJ, Klein MA, Voigtländer T, Weissmann C, Aguzzi A (1997) PrP-expressing tissue required for transfer of scrapie infectivity from spleen to brain. Nature 389:69-73.
4. Borchelt DR, Koliatsos VE, Guarnieri M, Pardo CA, Sisodia SS, Price DL (1994) Rapid anterograde axonal transport of the cellular prion glycoprotein in the peripheral and central nervous systems. J Biol Chem 269:14711-14714.
5. c) is required for scrapie spread within the central nervous system. Proc Natl Acad Sci USA 93:13148-13151.
6. Brandner S, Isenmann S, Raeber A, Fischer M, Sailer A, Kobayashi Y, Marino S, Weissmann C, Aguzzi A (1996b) Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379:339-343.
7. 117→ Val mutation. Biochem J 346:785-791.
8. Brown KL, Stewart K, Ritchie DL, Mabbott NA, Williams A, Fraser H, Morrison WI, Bruce ME (1999) Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat Med 5:1308-1312.
9. Büeler HR, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C (1993) Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.
10. Collinge J, Sidle KC, Meads J, Ironside J, Hill AF (1996) Molecular analysis of prion strain variation and the etiology of "new variant" CJD. Nature 383:685-690.
11. Eklund CM, Kennedy RC, Hadlow WJ (1967) Pathogenesis of scrapie virus infection in the mouse. J Infect Dis 117:15-22.
12. Fischer M, Rülicke T, Raeber A, Sailer A, Moser M, Oesch B, Brandner S, Aguzzi A, Weissmann C (1996) Prion protein (PrP) with aminoproximal deletions restoring susceptibility of PrP knock-out mice to scrapie. EMBO J 15:1255-1264.
13. Fraser H, Brown KL, Stewart K, McConnell I, McBride P, Williams A (1996) Replication of scrapie in spleens of SCID mice follows reconstitution with wild-type mouse bone marrow. J Gen Virol 77: 1935-1940.
14. Ghetti B, Tagliavini F, Giaccone G, Bugiani O, Frangione B, Farlow MR, Dlouhy SR (1994) Familial Gerstmann-Sträussler-Scheinker disease with neurofibrillary tangles. Mol Neurobiol 8:41-48.
15. Ghetti B, Piccardo P, Spillantini MG, Ichimiya Y, Porro M, Perini F, Kitamoto T, Tateishi J, Seiler C, Frangione B, Bugiani O, Giaccone G, Prelli F, Goedert M, Dlouhy SR, Tagliavini F (1996) Vascular variant of prion protein cerebral amyloidosis with tau-positive neurofibrillary tangles: The phenotype of the stop codon 145 mutation in PRNP. Proc Natl Acad Sci USA 93:744-748.
16. Glatzel M, Aguzzi A (2000) PrPc expression in the peripheral nervous system is a determinant of prion neuroinvasion. J Gen Virol 81:2813-2821.
17. Glatzel M, Heppner FL, Albers KM, Aguzzi A (2001) Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 31:25-34.
18. 42 fibrils. Science 293:1491-1495.
19. Hainfellner JA, Wanschitz J, Jellinger K, Liberski PP, Gullotta F, Budka H (1998) Coexistence of Alzheimer-type neuropathology in Creutzfeldt-Jakob disease. Acta Neuropathol (Berl) 96:116-122.
20. c in stromal and hematopoietic cells. J Virol 75:7097-7106.
21. Kaneko K, Ball HL, Wille H, Zhang H, Groth D, Torchia M, Tremblay P, Safar J, Prusiner SB, DeArmond SJ, Baldwin MA, Cohen FE 2000) A synthetic peptide initiates Gerstmann-Sträussler-Scheinker GSS) disease in transgenic mice. J Mol Biol 295:997-1007.
22. Kimberlin RH, Walker CA (1986) Pathogenesis of scrapie (strain 263K) in hamsters infected intracerebrally, intraperitoneally, or intraocularly. J Gen Virol 67:255-263.
23. Kimberlin RH, Hall SM, Walker CA (1983) Pathogenesis of mouse scrapie. Evidence for direct neural spread of infection to the CNS after injection of sciatic nerve. J Neurol Sci 61:315-325.
24. Klein MA, Frigg R, Flechsig E, Raeber AJ, Kalinke U, Bluethmann H, Bootz F, Suter M, Zinkernagel RM, Aguzzi A (1997) A crucial role for B cells in neuroinvasive scrapie. Nature 390:687-690.
25. Klein MA, Kaeser PS, Schwarz P, Weyd H, Xenarios I, Zinkernagel RM, Carroll MC, Verbeek JS, Botto M, Walport MJ, Molina H, Kalinke U, Acha-Orbea H, Aguzzi A (2001) Complement facilitates early prion pathogenesis. Nat Med 7:488-492.
26. Lasmezas CI, Cesbron JY, Deslys JP, Demaimay R, Adjou KT, Rioux R, Lemaire C, Locht C, Dormont D (1996) Immune system-dependent and -independent replication of the scrapie agent. J Virol 70:1292-1295.
27. Mandelkow E, Mandelkow EM (1995) Microtubules and microtubule-associated proteins. Curr Opin Cell Biol 7:72-81.
28. Manson JC, Jamieson E, Baybutt H, Tuzi NL, Barron R, McConnell I, Somerville R, Ironside J, Will R, Sy MS, Melton DW, Hope J, Bostock C (1999) A single amino acid alteration (101L) introduced into murine PrP dramatically alters incubation time of transmissible spongiform encephalopathy. EMBO J 18:6855-6864.
29. Montrasio F, Frigg R, Glatzel M, Klein MA, Mackay F, Aguzzi A, Weissmann C (2000) Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 288:1257-1259.
30. Nakano MY, Greber UF (2000) Quantitative microscopy of fluorescent adenovirus entry. J Struct Biol 129:57-68.
31. Prinz M, Montrasio F, Klein MA, Schwarz P, Priller J, Odermatt B, Pfeffer K, Aguzzi A (2002) Lymph nodal prion replication and neuroinvasion in mice devoid of follicular dendritic cells. Proc Natl Acad Sci USA 99:919-924.
32. Prusiner SB (1991) Molecular biology of prion diseases. Science 252:1515-1522.
33. Prusiner SB, Cochran SP, Groth DF, Downey DE, Bowman KA, Martinez HM (1982) Measurement of the scrapie agent using an incubation time interval assay. Ann Neurol 11:353-358.
34. Race R, Oldstone M, Chesebro B (2000) Entry versus blockade of brain infection following oral or intraperitoneal scrapie administration: Role of prion protein expression in peripheral nerves and spleen. J Virol 74:828-833.
35. Robertson G, Garrick D, Wu W, Kearns M, Martin D, Whitelaw E (1995) Position-dependent variegation of globin transgene expression in mice. Proc Natl Acad Sci USA 92:5371-5375.
36. Spittaels K, Van den Haute C, Van Dorpe J, Bruynseels K, Vandezande K, Laenen I, Geerts H, Mercken M, Sciot R, Van Lommel A, Loos R, Van Leuven F (1999) Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. Am J Pathol 155:2153-2165.
37. Spittaels K, Van den Haute C, Van Dorpe J, Geerts H, Mercken M, Bruynseels K, Lasrado R, Vandezande K, Laenen I, Boon T, Van Lint J, Vandenheede J, Moechars D, Loos R, Van Leuven F (2000) Glycogen synthase kinase-3β phosphorylates protein tau and rescues the axonopathy in the central nervous system of human four-repeat tau transgenic mice. J Biol Chem 275:41340-41349.
38. Suomalainen M, Nakano MY, Keller S, Bouke K, Stidwill RP, Greber UF (1999) Microtubule-dependent plus- and minus end-directed motilities are competing processes for nuclear targeting of adenovirus. J Cell Biol 144:657-672.
39. Tranchant C, Sergeant N, Wattez A, Mohr M, Warter JM, Delacourte A (1997) Neurofibrillary tangles in Gerstmann-Sträussler-Scheinker syndrome with the A117V prion gene mutation. J Neurol Neurosurg Psychiatry 63:240-246.
40. Vercelli A, Repici M, Garbossa D, Grimaldi A (2000) Recent techniques for tracing pathways in the central nervous system of developing and adult mammals. Brain Res Bull 51:11-28.