The immune system and prion diseases: A relationship of complicity and blindness

Journal of Leukocyte Biology

Volumn 72, Issue 6, 2002, Pages 1075-1083

  Aucouturier, Pierre ^a   Carnaud, Claude ^a  

^a HÔPITAL SAINT ANTOINE   (France)

Author keywords

Anti PrP immunity; Lymphoinvasion; Neuroinvasion; TSE

Indexed keywords

PRION PROTEIN; PROTEIN ANTIBODY;

ANIMAL EXPERIMENT; ANIMAL MODEL; B LYMPHOCYTE; CELL INVASION; CELL LINE; CELL SUBPOPULATION; DENDRITIC CELL; DISEASE COURSE; IMMUNE SYSTEM; IMMUNITY; IMMUNOLOGICAL TOLERANCE; LYMPHOID CELL; MACROPHAGE; MOUSE; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; RETICULOENDOTHELIAL SYSTEM; REVIEW; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; HUMANS; IMMUNE SYSTEM; IMMUNOTHERAPY; PRION DISEASES; PRIONS; SELF TOLERANCE;

ANIMALIA; MUS MUSCULUS;

EID: 0036917840     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (87)

1. Berg, L. J. (1994) Insights into the role of the immune system in prion diseases. Proc. Natl. Acad. Sci. USA 91, 429-432.
2. Aucouturier, P., Carp, R. I., Carnaud, C., Wisniewski, T. (2000) Prion diseases and the immune system. Clin. Immunol. 96, 79-85.
3. Carp, R. I., Kascsak, R. J., Wisniewski, H. M., Merz, P. A., Rubenstein, R., Bendheim, P., Bolton, D. (1989) The nature of the unconventional slow infection agents remains a puzzle. Alzheimer Dis. Assoc. Disord. 3, 79-99.
4. Prusiner, S. B., Scott, M. R., DeArmond, S. J., Cohen, F. E. (1998) Prion protein biology. Cell 93, 337-348.
5. Wisniewski, T., Aucouturier, P., Soto, C., Frangione, B. (1998) The prionoses and other conformational disorders. Amyloid 5, 212-224.
6. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. USA 95, 13363-13383.
7. Tateishi, J., Ohta, M., Koga, M., Sato, Y., Kuroiwa, Y. (1979) Transmission of chronic spongiform encephalopathy with kuru plaques from humans to small rodents. Ann. Neurol. 5, 581-584.
8. Muramoto, T., Kitamoto, T., Hoque, M. Z., Tateishi, J., Goto, I. (1993) Species barrier prevents an abnormal isoform of prion protein from accumulating in follicular dendritic cells of mice with Creutzfeldt-Jakob disease. J. Virol. 67, 6808-6810.
9. Bueler, H., Aguzzi, A., Sailer, A., Greiner, R. A., Autenried, P., Aguet, M., Weissmann, C. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73, 1339-1347.
10. Kimberlin, R. H., Walker, C. A., Fraser, H. (1989) The genomic identity of different strains of mouse scrapie is expressed in hamsters and preserved on reisolation in mice. J. Gen. Virol. 70, 2017-2025.
11. Carp, R. I., Meeker, H., Sersen, E., Kozlowski, P. (1998) Analysis of the incubation periods, induction of obesity and histopathological changes in senescence-prone and senescence-resistant mice infected with various scrapie strains. J. Gen. Virol. 79, 2863-2869.
12. Kitamoto, T., Muramoto, T., Mohri, S., Doh-Ura, K., Tateishi, J. (1991) Abnormal isoform of prion protein accumulates in follicular dendritic cells in mice with Creutzfeldt-Jakob disease. J. Virol. 65, 6292-6295.
13. Lasmezas, C. I., Deslys, J. P., Robain, O., Jaegly, A., Beringue, V., Peyrin, J. M., Fournier, J. G., Hauw, J. J., Rossier, J., Dormont, D. (1997) Transmission of the BSE agent to mice in the absence of detectable abnormal prion protein. Science 275, 402-405.
14. Lasmezas, C. I., Fournier, J. G., Nouvel, V., Boe, H., Marce, D., Lamoury, F., Kopp, N., Hauw, J. J., Ironside, J., Bruce, M., Dormont, D., Deslys, J. P. (2001) Adaptation of the bovine spongiform encephalopathy agent to primates and comparison with Creutzfeldt-Jakob disease: Implications for human health. Proc. Natl. Acad. Sci. USA 98, 4142-4147.
15. Carp, R. I., Rubenstein, R. (1991) Diversity and significance of scrapie strains. Semin. Virol. 2, 203-213.
16. Aucouturier, P., Kascsak, R. J., Frangione, B., Wisniewski, T. (1999) Biochemical and conformational variability of human prion strains in sporadic Creutzfeldt-Jakob disease. Neurosci. Lett. 274, 33-36.
17. Somerville, R. A., Birkett, C. R., Farquhar, C. F., Hunter, N., Goldmann, W., Dornan, J., Grover, D., Hennion, R. M., Percy, C., Foster, J., Jeffrey, M. (1997) Immunodetection of PrPSc in spleens of some scrapie-infected sheep but not BSE-infected cows. J. Gen. Virol. 78, 2389-2396.
18. Eklund, C. M., Kennedy, R. C., Hadlow, W. J. (1967) Pathogenesis of scrapie virus infection in the mouse. J. Infect. Dis. 117, 15-22.
19. Kimberlin, R. H., Walker, C. A. (1979) Pathogenesis of mouse scrapie: Dynamics of agent replication in spleen, spinal cord and brain after injection by different routes. J. Comp. Pathol. 89, 551-562.
20. Kimberlin, R. H., Walker, C. A. (1986) Pathogenesis of scrapie (strain 263K) in hamsters infected intracerebrally, intraperitoneally or intraocularly. J. Gen. Virol. 67, 255-263.
21. van Keulen, L. J., Schreuder, B. E., Meloen, R. H., Mooij-Harkes, G., Vromans, M. E., Langeveld, J. P. (1996) Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J. Clin. Microbiol. 34, 1228-1231.
22. Hilton, D. A., Fathers, E., Edwards, P., Ironside, J. W., Zajicek, J. (1998) Prion immunoreactivity in appendix before clinical onset of variant Creutzfeldt-Jakob disease. Lancet 352, 703-704.
23. Sigurdson, C. J., Williams, E. S., Miller, M. W., Spraker, T. R., O'Rourke, K. I., Hoover, E. A. (1999) Oral transmission and early lymphoid tropism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus). J. Gen. Virol. 80, 2757-2764.
24. Maignien, T., Lasmezas, C. I., Beringue, V., Dormont, D., Deslys, J. P. (1999) Pathogenesis of the oral route of infection of mice with scrapie and bovine spongiform encephalopathy agents. J. Gen. Virol. 80, 3035-3042.
25. Heggebo, R., Press, C. M., Gunnes, G., Lie, K. I., Tranulis, M. A., Ulvund, M., Groschup, M. H., Landsverk, T. (2000) Distribution of prion protein in the ileal Peyer's patch of scrapie-free lambs and lambs naturally and experimentally exposed to the scrapie agent. J. Gen. Virol. 81, 2327-2337.
26. Andreoletti, O., Berthon, P., Marc, D., Sarradin, P., Grosclaude, J., vanKeulen, L., Schelcher, F., Elsen, J. M., Lantier, F. (2000) Early accumulation of PrPSc in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J. Gen. Virol. 81, 3115-3126.
27. Beekes, M., McBride, P. A. (2000) Early accumulation of pathological PrP in the enteric nervous system and gut-associated lymphoid tissue of hamsters orally infected with scrapie. Neurosci. Lett. 278, 181-184.
28. Heggebo, R., Press, C. M., Gunnes, G., Gonzalez, L., Jeffrey, M. (2002) Distribution and accumulation of PrP in gut-associated and peripheral lymphoid tissue of scrapie-affected Suffolk sheep. J. Gen. Virol. 83, 479-489.
29. Foster, J. D., Parnham, D. W., Hunter, N., Bruce, M. (2001) Distribution of the prion protein in sheep terminally affected with BSE following experimental oral transmission. J. Gen. Virol. 82, 2319-2326.
30. McBride, P. A., SchulzSchaeffer, W. J., Donaldson, M., Bruce, M., Diringer, H., Kretzschmar, H. A., Beekes, M. (2001) Early spread of scrapie from the gastrointestinal tract to the central nervous system involves autonomic fibers of the splanchnic and vagus nerves. J. Virol. 75, 9320-9327.
31. Sigurdson, C. J., Spraker, T. R., Miller, M. W., Oesch, B., Hoover, E. A. (2001) PrP(CWD) in the myenteric plexus, vagosympathetic trunk and endocrine glands of deer with chronic wasting disease. J. Gen. Virol. 82, 2327-2334.
32. Glatzel, M., Heppner, F. L., Albers, K. M., Aguzzi, A. (2001) Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 31, 25-34.
33. Gardiner, A. C., Marucci, A. A. (1969) Immunological responsiveness of scrapie infected mice. J. Comp. Pathol. 79, 233-235.
34. Kingsbury, D. T., Smeltzer, D. A., Gibbs Jr., C. J., Gajdusek, D. C. (1981) Evidence for normal cell-mediated immunity in scrapie-infected mice. Infect. Immun. 32, 1176-1180.
35. Fraser, H., Dickinson, A. G. (1970) Pathogenesis of scrapie in the mouse: The role of the spleen. Nature 226, 462-463.
36. Fraser, H., Dickinson, A. G. (1978) Studies of the lymphoreticular system in the pathogenesis of scrapie: The role of spleen and thymus. J. Comp. Pathol. 88, 563-573.
37. Outram, G. W., Dickinson, A. G., Fraser, H. (1973) Developmental maturation of susceptibility to scrapie in mice. Nature 241, 536-537.
38. Outram, G. W., Dickinson, A. G., Fraser, H. (1974) Reduced susceptibility to scrapie in mice after steroid administration. Nature 249, 855-856.
39. Dickinson, A. G., Fraser, H., McConnell, I., Outram, G. W. (1978) Mitogenic stimulation of the host enhances susceptibility to scrapie. Nature 272, 54-55.
40. O'Rourke, K. I., Huff, T. P., Leathers, C. W., Robinson, M. M., Gorham, J. R. (1994) SCID mouse spleen does not support scrapie agent replication. J. Gen. Virol. 75, 1511-1514.
41. Klein, M. A., Frigg, R., Flechsig, E., Raeber, A. J., Kalinke, U., Bluethmann, H., Bootz, F., Suter, M., Zinkernagel, R. M., Aguzzi, A. (1997) A crucial role for B cells in neuroinvasive scrapie. Nature 390, 687-690.
42. Lasmézas, C. I., Cesbron, J-Y., Deslys, J-P., Demaimay, R., Adjou, K. T., Rioux, R., Lemaire, C., Locht, C., Dormont, D. (1996) Immune system-dependent and -independent replication of the scrapie agent. J. Virol. 70, 1292-1295.
43. Klein, M. A., Frigg, R., Raeber, A. J., Flechsig, E., Hegyi, I., Zinkernagel, R. M., Weissmann, C., Aguzzi, A. (1998) PrP expression in B lymphocytes is not required for prion neuroinvasion. Nat. Med. 4, 1429-1433.
44. Frigg, R., Klein, M. A., Hegyi, I., Zinkernagel, R. M., Aguzzi, A. (1999) Scrapie pathogenesis in subclinically infected B-cell-deficient mice. J. Virol. 73, 9584-9588.
45. Shlomchik, M. J., Radebold, K., Duclos, N., Manuelidis, L. (2001) Neuroinvasion by a Creutzfeldt-Jakob disease agent in the absence of B cells and follicular dendritic cells. Proc. Natl. Acad. Sci. USA 98, 9289-9294.
46. Blättler, T., Brandner, S., Raeber, A. J., Klein, M. A., Voigtlander, T., Weissmann, C., Aguzzi, A. (1997) PrP-expressing tissue required for transfer of scrapie infectivity from spleen to brain. Nature 389, 69-73.
47. Brown, K. L., Stewart, K., Ritchie, D. L., Mabbott, N. A., Williams, A., Fraser, H., Morrison, W. I., Bruce, M. E. (1999) Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat. Med. 5, 1308-1312.
48. Montrasio, F., Cozzio, A., Flechsig, E., Rossi, D., Klein, M. A., Rulicke, T., Raeber, A. J., Vosshenrich, C. A. J., Proft, J., Aguzzi, A., Weissmann, C. (2001) B lymphocyte-restricted expression of prion protein does not enable prion replication in prion protein knockout mice. Proc. Natl. Acad. Sci. USA 98, 4034-4037.
49. Raeber, A. J., Klein, M. A., Frigg, R., Flechsig, E., Aguzzi, A., Weissmann, C. (1999) PrP-dependent association of prions with splenic but not circulating lymphocytes of scrapie-infected mice. EMBO J. 18, 2702-2706.
50. Aucouturier, P., Geissmann, F., Damotte, D., Saborio, G. P., Meeker, H. C., Kascsak, R., Kascsak, R., Carp, R. I., Wisniewski, T. (2001) Infected splenic dendritic cells are sufficient for prion transmission to the CNS in mouse scrapie. J. Clin. Investig. 108, 703-708.
51. Mohri, S., Handa, S., Tateishi, J. (1987) Lack of effect of thymus and spleen on the incubation period of Creutzfeldt-Jakob disease in mice. J. Gen. Virol. 68, 1187-1189.
52. Raeber, A. J., Sailer, A., Hegyi, I., Klein, M. A., Rulicke, T., Fischer, M., Brandner, S., Aguzzi, A., Weissmann, C. (1999) 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 96, 3987-3992.
53. McBride, P. A., Eikelenboom, P., Kraal, G., Fraser, H., Bruce, M. E. (1992) PrP protein is associated with follicular dendritic cells of spleens and lymph nodes in uninfected and scrapie-infected mice. J. Pathol. 168, 413-418.
54. Hill, A. F., Zeidler, M., Ironside, J., Collinge, J. (1997) Diagnosis of new variant Creutzfeldt-Jakob disease by tonsil biopsy. Lancet 349, 99-100.
55. Hill, A. F., Butterworth, R. J., Joiner, S., Jackson, G., Rossor, M. N., Thomas, D. J., Frosh, A., Tolley, N., Bell, J. E., Spencer, M., King, A., Al-Sarraj, S., Ironside, J. W., Lantos, P. L., Collinge, J. (1999) Investigation of variant Creutzfeldt-Jakob disease and other human prion diseases with tonsil biopsy samples. Lancet 353, 183-189.
56. Brown, K. L., Ritchie, D. L., McBride, P. A., Bruce, M. E. (2000) Detection of PrP in extraneural tissues. Microsc. Res. Tech. 50, 40-45.
57. Fraser, H., Farquhar, C. F. (1987) Ionising radiation has no influence on scrapie incubation period in mice. Vet. Microbiol. 13, 211-223.
58. Mabbott, N. A., Bruce, M. E., Botto, M., Walport, M. J., Pepys, M. B. (2001) Temporary depletion of complement component C3 or genetic deficiency of Clq significantly delays onset of scrapie. Nat. Med. 7, 485-487.
59. Klein, M. A., Kaeser, P. S., Schwarz, P., Weyd, H., Xenarios, I., Zinkernagel, R. M., Carroll, M. C., Verbeek, J. S., Botto, M., Walport, M. J., Molina, H., Kalinke, U., Acha-Orbea, H., Aguzzi, A. (2001) Complement facilitates early prion pathogenesis. Nat. Med. 7, 488-492.
60. Wang, Y., Wang, J., Sun, Y., Wu, Q., Fu, Y. X. (2001) Complementary effects of TNF and lymphotoxin on the formation of germinal center and follicular dendritic cells. J. Immunol. 166, 330-337.
61. Mabbott, N. A., Mackay, F., Minns, F., Bruce, M. E. (2000) Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nat. Med. 6, 719-720.
62. Montrasio, F., Frigg, R., Glatzel, M., Klein, M. A., Mackay, F., Aguzzi, A., Weissmann, C. (2000) Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 288, 1257-1259.
63. Prinz, M., Montrasio, F., Klein, M. A., 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.
64. Manuelidis, L., Zaitsev, I., Koni, P., Lu, Z. Y., Flavell, R. A., Fritch, W. (2000) Follicular dendritic cells and dissemination of Creutzfeldt-Jakob disease. J. Virol. 74, 8614-8622.
65. Jeffrey, M., McGovern, G., Goodsir, C. M., Brown, K. L., Bruce, M. E. (2000) Sites of prion protein accumulation in scrapie-infected mouse spleen revealed by immune-electron microscopy. J. Pathol. 191, 323-332.
66. Carp, R. I., Callahan, S. M. (1982) Effect of mouse peritoneal macrophages on scrapie infectivity during extended in vitro incubation. Intervirology 17, 201-207.
67. Beringue, V., Demoy, M., Lasmezas, C. I., Gouritin, B., Weingarten, C., Deslys, J. P., Andreux, J. P., Couvreur, P., Dormont, D. (2000) Role of spleen macrophages in the clearance of scrapie agent early in pathogenesis. J. Pathol. 190, 495-502.
68. Sy, M. S., Gambetti, P. (1999) Prion replication - Once again blaming the dendritic cell. Nat. Med. 5, 1235-1237.
69. Ardavin, C., Martinez del Hoyo, G., Martin, P., Anjuere, F., Arias, C. F., Marin, A. R., Ruiz, S., Parrillas, V., Hernandez, H. (2001) Origin and differentiation of dendritic cells. Trends Immunol. 22, 691-700.
70. Burthem, J., Urban, B., Pain, A., Roberts, D. J. (2001) The normal cellular prion protein is strongly expressed by myeloid dendritic cells. Blood 98, 3733-3738.
71. Huang, F. P., Farquhar, C. F., Mabbott, N. A., Bruce, M. E., MacPherson, G. G. (2002) Migrating intestinal dendritic cells transport PrPsc from the gut. J. Gen. Virol. 83, 267-271.
72. Neutra, M. R., Mantis, N. J., Kraehenbuhl, J. P. (2001) Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat. Immunol. 2, 1004-1009.
73. Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., Granucci, F., Kraehenbuhl, J. P., Ricciardi-Castagnoli, P. (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367.
74. Oldstone, M. B. A., Race, R., Thomas, D., Lewicki, H., Homann, D., Smelt, S., Holz, A., Koni, P., Lo, D., Chesebro, B., Flavell, R. (2002) Lymphotoxin-alpha- and lymphotoxin-beta-deficient mice differ in susceptibility to scrapie: Evidence against dendritic cell involvement in neuroinvasion. J. Virol. 76, 4357-4363.
75. Wu, Q., Wang, Y., Wang, J., Hedgeman, E. O., Browning, J. L., Fu, Y. X. (1999) The requirement of membrane lymphotoxin for the presence of dendritic cells in lymphoid tissues. J. Exp. Med. 190, 629-638.
76. Rubenstein, R., Merz, P. A., Kascsak, R. J., Scalici, C. L., Papini, M. C., Carp, R. I., Kimberlin, R. H. (1991) Scrapie-infected spleens: Analysis of infectivity, scrapie-associated fibrils, and protease-resistant proteins. J. Infect. Dis. 164, 29-35.
77. Porter, D. D., Porter, H. G., Cox, N. A. (1973) Failure to demonstrate a humoral immune response to scrapie infection in mice. J. Immunol. 111, 1407-1410.
78. Kascsak, R. J., Rubenstein, R., Merz, P. A., Tonna-DeMasi, M., Fersko, R., Carp, R. I., Wisniewski, H. M., Diringer, H. (1987) Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J. Virol. 61, 3688-3693.
79. Williamson, R. A., Peretz, D., Smorodinsky, N., Bastidas, R., Serban, H., Mehlhorn, I., DeArmond, S. J., Prusiner, S. B., Burton, D. R. (1996) Circumventing tolerance to generate autologous monoclonal antibodies to the prion protein. Proc. Natl. Acad. Sci. USA 93, 7279-7282.
80. Williamson, R. A., Peretz, D., Pinilla, C., Ball, H., Bastidas, R. B., Rozenshteyn, R., Houghten, R. A., Prusiner, S. B., Burton, D. R. (1998) Mapping the prion protein using recombinant antibodies. J. Virol. 72, 9413-9418.
81. Peretz, D., Williamson, R. A., Kaneko, K., Vergara, J., Leclerc, E., Schmitt-Ulms, G., Mehlhorn, I. R., Legname, G., Wormald, M. R., Rudd, P. M., Dwek, R. A., Burton, D. R., Prusiner, S. B. (2001) Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 412, 739-743.
82. Enari, M., Flechsig, E., Weissmann, C. (2001) Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc. Natl. Acad. Sci. USA 98, 92959299.
83. Bosque, P. J., Prusiner, S. B. (2000) Cultured cell sublines highly susceptible to prion infection. J. Virol. 74, 4377-4386.
84. Beranger, F., Mange, A., Solassol, J., Lehmann, S. (2001) Cell culture models of transmissible spongiform encephalopathies. Biochem. Biophys. Res. Commun. 289, 311-316.
85. Heppner, F. L., Musahl, C., Arrighi, I., Klein, M. A., Rulicke, T., Oesch, B., Zinkernagel, R. M., Kalinke, U., Aguzzi, A. (2001) Prevention of scrapie pathogenesis by transgenic expression of anti-prion protein antibodies. Science 294, 178-182.
86. Souan, L., Margalit, R., Brenner, O., Cohen, I. R., Mor, F. (2001) Self prion protein peptides are immunogenic in Lewis rats. J. Autoimmun. 17, 303-310.
87. Souan, L., Tal, Y., Felling, Y., Cohen, I. R., Taraboulos, A., Mor, F. (2001) Modulation of proteinase-K resistant prion protein by prion peptide immunization. Eur. J. Immunol. 31, 2338-2346.