Immune system and peripheral nerves in propagation of prions to CNS

British Medical Bulletin

Volumn 66, Issue , 2003, Pages 141-159

  Aguzzi, Adriano ^a   Heppner, Frank L ^a   Heikenwalder, Mathias ^a   Prinz, Marco ^a   Mertz, Kirsten ^a   Seeger, Harald ^a   Glatzel, Markus ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN; PROTEIN ANTIBODY;

CENTRAL NERVOUS SYSTEM; DISEASE COURSE; IMMUNE DEFICIENCY; IMMUNE RESPONSE; IMMUNE SYSTEM; INFLAMMATORY INFILTRATE; LYMPHOID ORGAN; MAMMAL; PERIPHERAL NERVE; PRION; PRION DISEASE; PRIORITY JOURNAL; REVIEW; VIRUS REPLICATION;

AMYLOID; ANIMALS; BIOLOGICAL TRANSPORT; CATTLE; CENTRAL NERVOUS SYSTEM; CRICETINAE; DENDRITIC CELLS, FOLLICULAR; DNA REPLICATION; HUMANS; IMMUNE SYSTEM; IMMUNIZATION; INTESTINAL MUCOSA; LYMPHOCYTES; MACROPHAGES; MICE; PERIPHERAL NERVOUS SYSTEM; PRION DISEASES; PRIONS; PROTEIN PRECURSORS; RESEARCH DESIGN; SHEEP; SKIN; SPLEEN;

EID: 0141514778     PISSN: 00071420     EISSN: None     Source Type: Journal    
DOI: 10.1093/bmb/66.1.141     Document Type: Review

References (107)

1. Prusiner SB, Cochran SP, Groth DF, Downey DE, Bowman KA, Martinez HM. Measurement of the scrapie agent using an incubation time interval assay. Ann Neurol 1982; 11: 353-8
2. Kimberlin RH, Wilesmith JW. Bovine spongiform encephalopathy. Epidemiology, low dose exposure and risks. Ann NY Acad Sci 1994; 724: 210-20
3. Wells GA, Scott AC, Johnson CT et al. A novel progressive spongiform encephalopathy in cattle. Vet Rec 1987; 121: 419-420
4. Anderson RM, Donnelly CA, Ferguson NM et al. Transmission dynamics and epidemiology of BSE in British cattle. Nature 1996; 382: 779-88
5. Kimberlin RH, Walker CA. Pathogenesis of mouse scrapie: effect of route of inoculation on infectivity titres and dose-response curves. J Comp Pathol 1978; 88: 39-47
6. Scott JR, Foster JD, Fraser H. Conjunctival instillation of scrapie in mice can produce disease. Vet Microbiol 1993; 34: 305-9
7. Duffy P, Wolf J, Collins G, DeVoe AG, Streeten B, Cowen D. Possible person-to-person transmission of Creutzfeldt-Jakob disease. N Engl J Med 1974; 290: 692-3
8. Fraser H. Neuronal spread of scrapie agent and targeting of lesions within the retino-tectal pathway. Nature 1982; 295: 149-50
9. Glatzel M, Rogivue C, Ghani A, Streffer J, Amsler L, Aguzzi A. Incidence of Creutzfeldt-Jakob disease in Switzerland. Lancet 2002; 360: 139-41
10. Aguzzi A. Neuro-immune connection in spread of prions in the body? Lancet 1997; 349: 742-3
11. Nicotera P. A route for prion neuroinvasion. Neuron 2001; 31: 345-8
12. Wells GA, Dawson M, Hawkins SA et al. Infectivity in the ileum of cattle challenged orally with bovine spongiform encephalopathy. Vet Rec 1994; 135: 40-1
13. Vankeulen LJM, Schreuder BEC, Meloen RH, Mooijharkes G, Vromans MEW, Langeveld JPM. Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J Clin Microbiol 1996; 34: 1228-31
14. Hill AF, Zeidler M, Ironside J, Collinge J. Diagnosis of new variant Creutzfeldt-jakob disease by tonsil biopsy. Lancet 1997; 349: 99
15. Prinz M, Huber G, Macpherson AJS, Heppner FL, Glatzel M, Eugster HP et al. Oral prion infection requires normal numbers of Peyer's patches but not of enteric lymphocytes. Am J Pathol 2003; 162: 1103-11
16. Bradley R. Veterinary research at the Central Veterinary Laboratory, Weybridge, with special reference to scrapie and bovine spongiform encephalopathy. Rev Sci Tech 2000; 19: 819-30
17. Wells GA, Hawkins SA, Green RB et al. Preliminary observations on the pathogenesis of experimental bovine spongiform encephalopathy (BSE): an update. Vet Rec 1998; 142: 103-6
18. Neutra MR, Frey A, Kraehenbuhl JP. Epithelial M-cells: gateways for mucosal infection and immunization. Cell 1996; 86: 345-8
19. Kerneis S, Bogdanova A, Kraehenbuhl JP, Pringault E. Conversion by Peyer's patch lymphocytes of human enterocytes into M-cells that transport bacteria. Science 1997; 277: 949-52
20. Fischer M, Rülicke T, Raeber A et al. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J 1996; 15: 1255-64
21. Heppner FL, Christ AD, Klein MA et al. Transepithelial prion transport by M-cells. Nat Med 2001; 7: 976-7
22. Carp RI. Transmission of scrapie by oral route: effect of gingival scarification [letter]. Lancet 1982; 1: 170-1
23. Taylor DM, McConnell I, Fraser H. Scrapie infection can be established readily through skin scarification in immunocompetent but not immunodeficient mice. J Gen Virol 1996; 77: 1595-9
24. Huang FP, Farquhar CF, Mabbott NA, Bruce ME, MacPherson GG. Migrating intestinal dendritic cells transport PrP(Sc) from the gut. J Gen Virol 2002; 83: 267-71
25. Aucouturier PGF, Damotte D, Saborio GP et al. Infected splenic dendritic cells are sufficient for prion transmission to the CNS in mouse scrapie. J Clin Invest 2001; 108: 703-8
26. Race RE, Priola SA, Bessen RA et al. Neuron-specific expression of a hamster prion protein minigene in transgenic mice induces susceptibility to hamster scrapie agent. Neuron 1995; 15: 1183-91
27. Cashman NR, Loertscher R, Nalbantoglu J et al. Cellular isoform of the scrapie agent protein participates in lymphocyte activation. Cell 1990; 61: 185-92
28. Kitamoto T, Muramoto T, Mohri S, Dohura K, Tateishi J. Abnormal isoform of prion protein accumulates in follicular dendritic cells in mice with Creutzfeldt-Jakob disease. J Virol 1991; 65: 6292-5
29. Lasmezas CI, Cesbron JY, Deslys JP et al. Immune system-dependent and -independent replication of the scrapie agent. J Virol 1996; 70: 1292-5
30. Klein MA, Frigg R, Flechsig E et al. A crucial role for B cells in neuroinvasive scrapie. Nature 1997; 390: 687-90
31. Blättler T, Brandner S, Raeber AJ et al. PrP-expressing tissue required for transfer of scrapie infectivity from spleen to brain. Nature 1997; 389: 69-73
32. Klein MA, Frigg R, Raeber AJ et al. PrP expression in B lymphocytes is not required for prion neuroinvasion. Nat Med 1998; 4: 1429-33
33. Aguzzi A, Brandner S, Fischer MB et al. Spongiform encephalopathies: insights from transgenic models. Adv Virus Res 2001; 56: 313-52
34. Aguzzi A, Klein MA, Montrasio F et al. Prions: pathogenesis and reverse genetics. Ann NY Acad Sci 2000; 920: 140-57
35. Kaeser PS, Klein MA, Schwarz P, Aguzzi A. Efficient lymphoreticular prion propagation requires PrP(c) in stromal and hematopoietic cells. J Virol 2001; 75: 7097-106
36. Klein MA, Kaeser PS, Schwarz P et al. Complement facilitates early prion pathogenesis. Nat Med 2001; 7: 488-92
37. Prinz M, Montrasio F, Klein MA et al. Lymph nodal prion replication and neuroinvasion in mice devoid of follicular dendritic cells. Proc Natl Acad Sci USA 2002; 99: 919-24
38. Brown KL, Stewart K, Ritchie DL et al. Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat Med 1999; 5: 1308-12
39. Kooyman DL, Byrne GW, Logan JS. Glycosyl phosphatidylinositol anchor. Exp Nephrol 1998; 6: 148-51
40. Kapasi ZF, Qin D, Kerr WG et al. Follicular dendritic cell (FDC) precursors in primary lymphoid tissues. J Immunol 1998; 160: 1078-84
41. Szakal AK, Kapasi ZF, Haley ST, Tew JG. Multiple lines of evidence favoring a bone marrow derivation of follicular dendritic cells (FDCs). Adv Exp Med Biol 1995; 378: 267-72
42. Kooyman DL, Byme GW, McClellan S et al. In vivo transfer of GPI-linked complement restriction factors from erythrocytes to the endothelium. Science 1995; 269: 89-92
43. Liu T, Li R, Pan T et al. Intercellular transfer of the cellular prion protein. J Biol Chem 2002; 277: 47671-8
44. Kao RR, Gravenor MB, Baylis M et al. The potential size and duration of an epidemic of bovine spongiform encephalopathy in British sheep. Science 2002; 295: 332-5
45. Bruce ME, Boyle A, Cousens S et al. Strain characterization of natural sheep scrapie and comparison with BSE. J Gen Virol 2002; 83: 695-704
46. Glatzel M, Aguzzi A. The shifting biology of prions. Brain Res Brain Res Rev 2001; 36: 241-8
47. Aguzzi A. Prion diseases, blood and the immune system: concerns and reality. Haematologica 2000; 85: 3-10
48. Jeffrey M, McGovern G, Goodsir CM, Bruce ME. Sites of prion protein accumulation in scrapie-infected mouse spleen revealed by immuno-electron microscopy. J Pathol 2000; 191: 323-32
49. Bofill M, Akbar AN, Amlot PL. Follicular dendritic cells share a membrane-bound protein with fibroblasts. J Pathol 2000; 191: 217-26
50. Endres R, Alimzhanov MB, Plitz T et al. Mature follicular dendritic cell networks depend on expression of lymphotoxin beta receptor by radioresistant stromal cells and of lymphotoxin beta and tumor necrosis factor by B cells. J Exp Med 1999; 189: 159-68
51. Koni PA, Sacca R, Lawton P, Browning JL, Ruddle NH, Flavell RA. Distinct roles in lymphoid organogenesis for lymphotoxins alpha and beta revealed in lymphotoxin beta-deficient mice. Immunity 1997; 6: 491-500
52. Fu YX, Huang G, Matsumoto M, Molina H, Chaplin DD. Independent signals regulate development of primary and secondary follicle structure in spleen and mesenteric lymph node. Proc Natl Acad Sci USA 1997; 94: 5739-43
53. Ware CF, VanArsdale TL, Crowe PD, Browning JL. The ligands and receptors of the lymphotoxin system. Curr Top Microbiol Immunol 1995; 198: 175-218
54. Matsumoto M, Fu YX, Molina H et al. Distinct roles of lymphotoxin alpha and the type I tumor necrosis factor (TNF) receptor in the establishment of follicular dendritic cells from non-bone marrow-derived cells. J Exp Med 1997; 186: 1997-2004
55. Mackay F, Majeau GR, Lawton P, Hochman PS, Browning JL. Lymphotoxin but not tumor necrosis factor functions to maintain splenic architecture and humoral responsiveness in adult mice. Eur J Immunol 1997; 27: 2033-42
56. Browning JL, Ngam-ek A, Lawton P et al. Lymphotoxin beta, a novel member of the TNF family that forms a heteromeric complex with lymphotoxin on the cell surface. Cell 1993; 72: 847-56
57. Browning JL, Dougas I, Ngam-ek A et al. Characterization of surface lymphotoxin forms. Use of specific monoclonal antibodies and soluble receptors. J Immunol 1995; 154: 33-46
58. Gonzalez M, Mackay F, Browning JL, Kosco-Vilbois MH, Noelle RJ. The sequential role of lymphotoxin and B-cells in the development of splenic follicles. J Exp Med 1998; 187: 997-1007
59. Crowe PD, VanArsdale TL, Walter BN et al. A lymphotoxin-beta-specific receptor. Science 1994; 264: 707-10
60. Mackay F, Browning JL. Turning off follicular dendritic cells. Nature 1998; 395: 26-7
61. Büeler HR, Aguzzi A, Sailer A et al. Mice devoid of PrP are resistant to scrapie. Cell 1993; 73: 1339-47
62. Bruce ME. Agent replication dynamics in a long incubation period model of mouse scrapie. J Gen Virol 1985; 66: 2517-22
63. Rubenstein R, Merz PA, Kascsak RJ et al. Scrapie-infected spleens: analysis of infectivity, scrapie-associated fibrils, and protease-resistant proteins. J Infect Dis 1991; 164: 29-35
64. Aguzzi A, CoRinge J. Post-exposure prophylaxis after accidental prion inoculation. Lancet 1997; 350: 1519-20
65. Aguzzi A, Glatzel M, Montrasio F, Prinz M, Heppner FL. Interventional strategies against prion diseases. Nat Rev Neurosci 2001; 2: 745-9
66. Montrasio F, Frigg P, Glatzel M et al. Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 2000; 288: 1257-9
67. Kitamura D, Roes J, Kuhn R, Rajewsky K. A B-cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin chain gene. Nature 1991; 350: 423-6
68. Frigg R, Klein MA, Hegyi I, Zinkernagel RM, Aguzzi A. Scrapie pathogenesis in subclinically infected B-cell-deficient mice. J Virol 1999; 73: 9584-8
69. Aguzzi A, Montrasio F, Kaeser PS. Prions: health scare and biological challenge. Nat Rev Mol Cell Biol 2001; 2: 118-26
70. Glatzel M, Aguzzi A. PrP(C) expression in the peripheral nervous system is a determinant of prion neuroinvasion. J Gen Virol 2000; 81: 2813-21
71. Beekes M, McBride PA, Baldauf E. Cerebral targeting indicates vagal spread of infection in hamsters fed with scrapie. J Gen Virol 1998; 79: 601-7
72. Clarke MC, Kimberlin RH. Pathogenesis of mouse scrapie: distribution of agent in the pulp and stroma of infected spleens. Vet Microbiol 1984; 9: 215-25
73. Cole S, Kimberlin RH. Pathogenesis of mouse scrapie: dynamics of vacuolation in brain and spinal cord after intraperitoneal infection. Neuropathol Appl Neurobiol 1985; 11: 213-27
74. McBride PA, Beekes M. Pathological PrP is abundant in sympathetic and sensory ganglia of hamsters fed with scrapie. Neurosci Lett 1999; 265: 135-8
75. Glatzel M, Flechsig E, Navarro B et al. Adenoviral and adeno-associated viral transfer of genes to the peripheral nervous system. Proc Natl Acad Sci USA 2000; 97: 442-7
76. Künzi V, Glatzel M, Nakano MY, Greber UF, Van Leuven F, Aguzzi A. Unhampered prion neuroinvasion despite impaired fast axonal transport in transgenic mice overexpressing four-repeat tau. J Neurosci 2002; 22: 7471-7
77. Race R, Oldstone M, Chesebro B. Entry versus blockade of brain infection following oral or intraperitoneal scrapie administration: role of prion protein expression in peripheral nerves and spleen. J Virol 2000; 74: 828-33
78. Felten DL, Felten SY. Sympathetic noradrenergic innervation of immune organs. Brain Behav Immun 1988; 2: 293-300
79. Kimberlin RH, Hall SM, Walker CA. Pathogenesis of mouse scrapie. Evidence for direct neural spread of infection to the CNS after injection of sciatic nerve. J Neurol Sci 1983; 61: 315-25
80. Hainfellner JA, Budka H. Disease associated prion protein may deposit in the peripheral nervous system in human tr transmissible spongiform encephalopathies. Acta Neuropathol (Berl) 1999; 98: 458-60
81. Baldauf E, Beekes M, Diringer H. Evidence for an alternative direct route of access for the scrapie agent to the brain bypassing the spinal cord. J Gen Virol 1997; 78: 1187-97
82. c) is required for scrapie spread within the central nervous system. Proc Natl Acad Sci USA 1996; 93: 13148-51
83. Heppner FL, Musahl C, Arrighi I et al. Prevention of scrapie pathogenesis by transgenic expression of anti-prion protein antibodies. Science 2001; 294: 178-82
84. Raeber AJ, Sailer A, Hegyi I et al. Ectopic expression of prion protein (PrP) in T lymphocytes or hepatocytes of PrP knockout mice is insufficient to sustain prion replication. Proc Natl Acad Sci USA 1999; 96: 3987-92
85. Fournier JG, Escaig Haye F, Billette de Villemeur T, Robain O. Ultrastructural localization of cellular prion protein (PrPc) in synaptic boutons of normal hamster hippocampus. C R Acad Sci III 1995; 318:339-44
86. Collinge J, Whittington MA, Sidle KC et al. Prion protein is necessary for normal synaptic function. Nature 1994; 370: 295-7
87. Whittington MA, Sidle KC, Gowland I et al. Rescue of neurophysiological phenotype seen in PrP null mice by transgene encoding human prion protein. Nat Genet 1995; 9: 197-201
88. Sethi S, Lipford G, Wagner H, Kretzschmar H. Postexposure prophylaxis against prion disease with a stimulator of innate immunity. Lancet 2002; 360: 229-30
89. Adachi O, Kawai T, Takeda K et al. Targeted disruption of the MyD88 gene results in loss of IL-1- and IL-18-mediated function. Immunity 1998; 9: 143-50
90. Mabbott NA, Bruce ME, Botto M, Walport MJ, Pepys MB. Temporary depletion of complement component C3 or genetic deficiency of C1q significantly delays onset of scrapie. Nat Med 2001; 7: 485-7
91. Park SY, Ueda S, Ohno H et al. Resistance of Fc receptor-deficient mice to fatal glomerulonephritis. J Clin Invest 1998; 102: 1229-38
92. Takai T, Ono M, Hikida M, Ohmori H, Ravetch JV. Augmented humoral and anaphylactic responses in Fc gamma RII-deficient mice. Nature 1996; 379: 346-9
93. Takai T, Li M, Sylvestre D, Clynes R, Ravetch JV. FcR gamma chain deletion results in pleiotrophic effector cell defects. Cell 1994; 76: 519-29
94. Hazenbos WL, Gessner JE, Hofhuis FM et al. Impaired IgG-dependent anaphylaxis and Arthus reaction in Fc gamma RIII (CD16) deficient mice. Immunity 1996; 5: 181-8
95. Szakal AK, Hanna Jr MG. The ultrastructure of antigen localization and virus-like particles in mouse spleen germinal centers. Exp Mol Pathol 1968; 8: 75-89
96. Carroll MC. CD21/CD35 in B-cell activation. Semin Immunol 1998; 10: 279-86
97. Fischer MB, Goerg S, Shen L et al. Dependence of germinal center B-cells on expression of CD21/CD35 for survival. Science 1998; 280: 582-5
98. -/- mice is rescued by adjuvants without improvement in germinal center development. J Immunol 2000; 165: 3119-27
99. Gabizon R, McKinley MP, Groth D, Prusiner SB. Immunoaffinity purification and neutralization of scrapie prion infectivity. Proc Natl Acad Sci USA 1988; 85: 6617-21
100. Horiuchi M, Caughey B. Specific binding of normal prion protein to the scrapie form via a localized domain initiates its conversion to the protease-resistant state. EMBO J 1999; 18: 3193-203
101. Enari M, Flechsig E, Weissmann C. Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc Natl Acad Sci USA 2001; 98: 9295-9
102. Peretz D, Williamson RA, Kaneko K et al. Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 2001; 412: 739-43
103. Büeler HR, Fischer M, Lang Y et al. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 1992; 356: 577-82
104. Prusiner SB, Groth D, Serban A et al. Ablation of the prion protein (PrP) gene in mice prevents scrapie and facilitates production of anti-PrP antibodies. Proc Natl Acad Sci USA 1993; 90: 10608-12
105. Sc)-specific epitope defined by a monoclonal antibody. Nature 1997; 390: 74-7
106. Korth C, Streit P, Oesch B. Monoclonal antibodies specific for the native, disease-associated isoform of the prion protein. Methods Enzymol 1999; 309: 106-22
107. Farquhar CF, Dornan J, Somerville RA, Tunstall AM, Hope J. Effect of Sinc genotype, agent isolate and route of infection on the accumulation of protease-resistant PrP in non-central nervous system tissues during the development of murine scrapie. J Gen Virol 1994; 75: 495-504