Adoptive transfer of T lymphocytes sensitized against the prion protein attenuates prion invasion in scrapie-infected mice

Journal of Immunology

Volumn 183, Issue 10, 2009, Pages 6619-6628

  Gourdain, Pauline ^a   Grégoire, Sylvie ^a,d   Iken, Saci ^a   Bachy, Véronique ^a,e   Dorban, Gauthier ^b   Chaigneau, Thomas ^a   Debiec, Hanna ^c   Bergot, Anne Sophie ^d   Renault, Isabelle ^a   Aucouturier, Pierre ^a   Carnaud, Claude ^a  

^a HÔPITAL SAINT ANTOINE   (France)

^b UNIVERSITY OF LIÈGE   (Belgium)

^c Urgences Néphrologiques et Transplantation Rénale Hôpital Tenon 4   (France)

^d PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^e GUY S HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOKINE; PRION PROTEIN;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CELL TRANSFER; CONTROLLED STUDY; LYMPHOID ORGAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCRAPIE; T LYMPHOCYTE; TREATMENT OUTCOME;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, CD3; DNA-BINDING PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PRIONS; SCRAPIE; SPLEEN; T-LYMPHOCYTES;

EID: 77954226661     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0804385     Document Type: Article

References (77)

1. Prusiner, S. B. 1998. Prions. Proc. Natl. Acad. Sci. USA 95: 13363-13383.
2. Collinge, J. 2001. Prion diseases of humans and animals: their causes and molecular basis. Annu. Rev. Neurosci. 24: 519-550. (Pubitemid 32695238)
3. Aguzzi, A., and M. Heikenwalder. 2006. Pathogenesis of prion diseases: current status and future outlook. Nat. Rev. Microbiol. 4: 765-775.
4. Bolton, D. C., M. P. McKinley, and S. B. Prusiner. 1982. Identification of a protein that purifies with the scrapie prion. Science 218: 1309-1311.
5. Oesch, B., D. Westaway, M. Walchli, M. P. McKinley, S. B. Kent, R. Aebersold, R. A. Barry, P. Tempst, D. B. Teplow, L. E. Hood, et al. 1985. A cellular gene encodes scrapie PrP 27-30 protein. Cell. 40: 735-746. (Pubitemid 15240279)
6. Basler, K., B. Oesch, M. Scott, D. Westaway, M. Walchli, D. F. Groth, M. P. McKinley, S. B. Prusiner, and C. Weissmann. 1986. Scrapie and cellular PrP isoforms are encoded by the same chromosomal gene. Cell 46: 417-428. (Pubitemid 16031678)
7. Wopfner, F., G. Weidenhofer, R. Schneider, A. von Brunn, S. Gilch, T. F. Schwarz, T. Werner, and H. M. Schatzl. 1999. Analysis of 27 mammalian and 9 avian PrPs reveals high conservation of flexible regions of the prion protein. J. Mol. Biol. 289: 1163-1178.
8. Martins, V. R., A. F. Mercadante, A. L. Cabral, A. R. Freitas, and R. M. Castro. 2001. Insights into the physiological function of cellular prion protein. Braz. J. Med. Biol. Res. 34: 585-595.
9. Steele, A. D., S. Lindquist, and A. Aguzzi. 2007. The prion protein knockout mouse: a phenotype under challenge. Prion 1: 83-93.
10. Ballerini, C., P. Gourdain, V. Bachy, N. Blanchard, E. Levavasseur, S. Gregoire, P. Fontes, P. Aucouturier, C. Hivroz, and C. Carnaud. 2006. Functional implication of cellular prion protein in antigen-driven interactions between T cells and dendritic cells. J. Immunol. 176: 7254-7262.
11. Castilla, J., P. Saa, C. Hetz, and C. Soto. 2005. In vitro generation of infectious scrapie prions. Cell 121: 195-206.
12. Deleault, N. R., B. T. Harris, J. R. Rees, and S. Supattapone. 2007. From the cover: formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. USA 104: 9741-9746.
13. Legname, G., I. V. Baskakov, H. O. Nguyen, D. Riesner, F. E. Cohen, S. J. DeArmond, and S. B. Prusiner. 2004. Synthetic mammalian prions. Science 305: 673-676.
14. Kimberlin, R. H., and C. A. Walker. 1979. Pathogenesis of mouse scrapie: dynamics of agent replication in spleen, spinal cord and brain after infection by different routes. J. Comp. Pathol. 89: 551-562.
15. Aucouturier, P., and C. Carnaud. 2002. The immune system and prion diseases: a relationship of complicity and blindness. J. Leukocyte Biol. 72: 1075-1083. (Pubitemid 36008877)
16. Brown, K. L., K. Stewart, D. L. Ritchie, N. A. Mabbott, A. Williams, H. Fraser, W. I. Morrison, and M. E. Bruce. 1999. Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat. Med. 5: 1308-1312.
17. Aucouturier, P., F. Geissmann, D. Damotte, G. P. Saborio, H. C. Meeker, R. Kascsak, R. Kascsak, R. I. Carp, and T. Wisniewski. 2001. Infected splenic dendritic cells are sufficient for prion transmission to the CNS in mouse scrapie. J. Clin. Invest. 108: 703-708.
18. Huang, F. P., C. F. Farquhar, N. A. Mabbott, M. E. Bruce, and G. G. MacPherson. 2002. Migrating intestinal dendritic cells transport PrP(Sc) from the gut. J. Gen. Virol. 83: 267-271.
19. + Cells impairs scrapie agent neuroinvasion from the intestine. J. Immunol. 179: 7758-7766.
20. Porter, D. D., H. G. Porter, and N. A. Cox. 1973. Failure to demonstrate a humoral immune response to scrapie infection in mice. J. Immunol. 111: 1407-1410.
21. Solomon, A., D. T. Weiss, and J. S. Wall. 2003. Immunotherapy in systemic primary (AL) amyloidosis using amyloid-reactive monoclonal antibodies. Cancer Biother. Radiopharm. 18: 853-860.
22. Schenk, D., R. Barbour, W. Dunn, G. Gordon, H. Grajeda, T. Guido, K. Hu, J. Huang, K. Johnson-Wood, K. Khan, et al. 1999. Immunization with amyloid-β attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 400: 173-177.
23. Janus, C., J. Pearson, J. McLaurin, P. M. Mathews, Y. Jiang, S. D. Schmidt, M. A. Chishti, P. Horne, D. Heslin, J. French, et al. 2000. A β peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer's disease. Nature 408: 979-982.
24. Beringue, V., D. Vilette, G. Mallinson, F. Archer, M. Kaisar, M. Tayebi, G. S. Jackson, A. R. Clarke, H. Laude, J. Collinge, and S. Hawke. 2004. PrPSc binding antibodies are potent inhibitors of prion replication in cell lines. J. Biol. Chem. 279: 39671-39676.
25. Enari, M., E. Flechsig, and C. Weissmann. 2001. Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc. Natl. Acad. Sci. USA 98: 9295-9299.
26. Peretz, D., R. A. Williamson, K. Kaneko, J. Vergara, E. Leclerc, G. Schmitt-Ulms, I. R. Mehlhorn, G. Legname, M. R. Wormald, P. M. Rudd, et al. 2001. Antibodies inhibit prion propagation and clear cell cultures of prion infectivity. Nature 412: 739-743.
27. Sigurdsson, E. M., M. S. Sy, R. Li, H. Scholtzova, R. J. Kascsak, R. Kascsak, R. Carp, H. C. Meeker, B. Frangione, and T. Wisniewski. 2003. Anti-prion antibodies for prophylaxis following prion exposure in mice. Neurosci. Lett. 336: 185-187.
28. White, A. R., P. Enever, M. Tayebi, R. Mushens, J. Linehan, S. Brandner, D. Anstee, J. Collinge, and S. Hawke. 2003. Monoclonal antibodies inhibit prion replication and delay the development of prion disease. Nature 422: 80-83.
29. Heppner, F. L., C. Musahl, I. Arrighi, M. A. Klein, T. Rulicke, B. Oesch, R. M. Zinkernagel, U. Kalinke, and A. Aguzzi. 2001. Prevention of scrapie pathogenesis by transgenic expression of anti-prion protein antibodies. Science 294: 178-182.
30. Ishibashi, D., H. Yamanaka, N. Yamaguchi, D. Yoshikawa, R. Nakamura, N. Okimura, Y. Yamaguchi, K. Shigematsu, S. Katamine, and S. Sakaguchi. 2007. Immunization with recombinant bovine but not mouse prion protein delays the onset of disease in mice inoculated with a mouse-adapted prion. Vaccine 25: 985-992.
31. Sigurdsson, E. M., D. R. Brown, M. Daniels, R. J. Kascsak, R. Kascsak, R. Carp, H. C. Meeker, B. Frangione, and T. Wisniewski. 2002. Immunization delays the onset of prion disease in mice. Am. J. Pathol. 161: 13-17.
32. Magri, G., M. Clerici, P. Dall'Ara, M. Biasin, M. Caramelli, C. Casalone, M. L. Giannino, R. Longhi, L. Piacentini, S. Della Bella, et al. 2005. Decrease in pathology and progression of scrapie after immunisation with synthetic prion protein peptides in hamsters. Vaccine 23: 2862-2868.
33. Schwarz, A., O. Kratke, M. Burwinkel, C. Riemer, J. Schultz, P. Henklein, T. Bamme, and M. Baier. 2003. Immunisation with a synthetic prion protein-derived peptide prolongs survival times of mice orally exposed to the scrapie agent. Neurosci. Lett. 350: 187-189.
34. Bade, S., M. Baier, T. Boetel, and A. Frey. 2006. Intranasal immunization of BALB/c mice against prion protein attenuates orally acquired transmissible spongiform encephalopathy. Vaccine 24: 1242-1253.
35. Goni, F., E. Knudsen, F. Schreiber, H. Scholtzova, J. Pankiewicz, R. Carp, H. C. Meeker, R. Rubenstein, D. R. Brown, M. S. Sy, et al. 2005. Mucosal vaccination delays or prevents prion infection via an oral route. Neuroscience 133: 413-421.
36. Goni, F., F. Prelli, F. Schreiber, H. Scholtzova, E. Chung, R. Kascsak, D. R. Brown, E. M. Sigurdsson, J. A. Chabalgoity, and T. Wisniewski. 2008. High titers of mucosal and systemic anti-PrP antibodies abrogate oral prion infection in mucosal-vaccinated mice. Neuroscience 153: 679-686.
37. Yamanaka, H., D. Ishibashi, N. Yamaguchi, D. Yoshikawa, R. Nakamura, N. Okimura, T. Arakawa, T. Tsuji, S. Katamine, and S. Sakaguchi. 2006. Enhanced mucosal immunogenicity of prion protein following fusion with B subunit of Escherichia coli heat-labile enterotoxin. Vaccine 24: 2815-2823.
38. McGavern, D. B. 2006. Immunotherapeutic relief from persistent infections and amyloid disorders. Neurology 66: S59-S64.
39. Bueler, H., M. Fischer, Y. Lang, H. Bluethmann, H. P. Lipp, S. J. DeArmond, S. B. Prusiner, M. Aguet, and C. Weissmann. 1992. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356: 577-582.
40. Williamson, R. A., D. Peretz, N. Smorodinsky, R. Bastidas, H. Serban, I. Mehlhorn, S. J. DeArmond, S. B. Prusiner, and D. R. Burton. 1996. Circumventing tolerance to generate autologous monoclonal antibodies to the prion protein. Proc. Natl. Acad. Sci. USA 93: 7279-7282.
41. Muller-Schiffmann, A., and C. Korth. 2008. Vaccine approaches to prevent and treat prion infection: progress and challenges. BioDrugs 22: 45-52. (Pubitemid 351158534)
42. Jones, M., V. McLoughlin, J. G. Connolly, C. F. Farquhar, I. R. Macgregor, and M. W. Head. 2009. Production and characterization of a panel of monoclonal antibodies against native human cellular prion protein. Hybridoma 28: 13-20.
43. Bainbridge, J., and B. Walker. 2003. Cell mediated immune responses against human prion protein. Clin. Exp. Immunol. 133: 310-317.
44. Gregoire, S., A. S. Bergot, C. Feraudet, C. Carnaud, P. Aucouturier, and M. B. Rosset. 2005. The murine B cell repertoire is severely selected against endogenous cellular prion protein. J. Immunol. 175: 6443-6449. (Pubitemid 41598885)
45. Rosset, M. B., C. Ballerini, S. Gregoire, P. Metharom, C. Carnaud, and P. Aucouturier. 2004. Breaking immune tolerance to the prion protein using prion protein peptides plus oligodeoxynucleotide-CpG in mice. J. Immunol. 172: 5168-5174.
46. Krasemann, S., M. Groschup, G. Hunsmann, and W. Bodemer. 1996. Induction of antibodies against human prion proteins (PrP) by DNA-mediated immunization of PrP0/0 mice. J. Immunol. Methods 199: 109-118. (Pubitemid 26412940)
47. Fernandez-Borges, N., A. Brun, J. L. Whitton, B. Parra, F. Diaz-San Segundo, F. J. Salguero, J. M. Torres, and F. Rodriguez. 2006. DNA vaccination can break immunological tolerance to PrP in wild-type mice and attenuates prion disease after intracerebral challenge. J. Virol. 80: 9970-9976.
48. Nikles, D., P. Bach, K. Boller, C. A. Merten, F. Montrasio, F. L. Heppner, A. Aguzzi, K. Cichutek, U. Kalinke, and C. J. Buchholz. 2005. Circumventing tolerance to the prion protein (PrP): vaccination with PrP-displaying retrovirus particles induces humoral immune responses against the native form of cellular PrP. J. Virol. 79: 4033-4042.
49. Alexandrenne, C., A. Wijkhuisen, F. Dkhissi, V. Hanoux, C. Creminon, D. Boquet, and J. Y. Couraud. 2009. Generating antibodies against the native form of the human prion protein (hPrP) in wild-type animals: a comparison between DNA and protein immunizations. J. Immunol. Methods 341: 41-49.
50. Gregoire, S., C. Logre, P. Metharom, E. Loing, J. Chomilier, M. B. Rosset, P. Aucouturier, and C. Carnaud. 2004. Identification of two immunogenic domains of the prion protein-PrP-which activate class II-restricted T cells and elicit antibody responses against the native molecule. J. Leukocyte Biol. 76: 125-134.
51. Polymenidou, M., F. L. Heppner, E. C. Pellicioli, E. Urich, G. Miele, N. Braun, F. Wopfner, H. M. Schatzl, B. Becher, and A. Aguzzi. 2004. Humoral immune response to native eukaryotic prion protein correlates with anti-prion protection. Proc. Natl. Acad. Sci. USA 101(Suppl. 2): 14670-14676.
52. Malissen, M., A. Gillet, L. Ardouin, G. Bouvier, J. Trucy, P. Ferrier, E. Vivier, and B. Malissen. 1995. Altered T cell development in mice with a targeted mutation of the CD3-ε gene. EMBO J. 14: 4641-4653.
53. Shinkai, Y., G. Rathbun, K. P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68: 855-867.
54. Fischer, M., T. Rulicke, A. Raeber, A. Sailer, M. Moser, B. Oesch, S. Brandner, A. Aguzzi, and C. Weissmann. 1996. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15: 1255-1264.
55. Sacquin, A., A. S. Bergot, P. Aucouturier, and M. Bruley-Rosset. 2008. Contribution of antibody and T cell-specific responses to the progression of 139Ascrapie in C57BL/6 mice immunized with prion protein peptides. J. Immunol. 181: 768-775.
56. Tanchot, C., and B. Rocha. 1997. Peripheral selection of T cell repertoires: the role of continuous thymus output. J. Exp. Med. 186: 1099-1106.
57. Heikenwalder, M., M. O. Kurrer, I. Margalith, J. Kranich, N. Zeller, J. Haybaeck, M. Polymenidou, M. Matter, J. Bremer, W. S. Jackson, et al. 2008. Lymphotoxindependent prion replication in inflammatory stromal cells of granulomas. Immunity. 29: 998-1008.
58. Montrasio, F., R. Frigg, M. Glatzel, M. A. Klein, F. Mackay, A. Aguzzi, and C. Weissmann. 2000. Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 288: 1257-1259.
59. Heikenwalder, M., M. Polymenidou, T. Junt, C. Sigurdson, H. Wagner, S. Akira, R. Zinkernagel, and A. Aguzzi. 2004. Lymphoid follicle destruction and immunosuppression after repeated CpG oligodeoxynucleotide administration. Nat. Med. 10: 187-192.
60. White, A. R., and S. H. Hawke. 2003. Immunotherapy as a therapeutic treatment for neurodegenerative disorders. J. Neurochem. 87: 801-808.
61. Ravnskov, U. 1998. The subepithelial formation of immune complexes in membranous glomerulonephritis may be harmless and secondary to toxic or allergic factors. Scand. J. Immunol. 48: 469-474. (Pubitemid 28505669)
62. Liu, J., M. W. Marino, G. Wong, D. Grail, A. Dunn, J. Bettadapura, A. J. Slavin, L. Old, and C. C. Bernard. 1998. TNF is a potent anti-inflammatory cytokine in autoimmune-mediated demyelination. Nat. Med. 4: 78-83.
63. + T cells. Curr. Opin. Immunol. 21: 200-208.
64. Ayuk, F. A., A. R. Zander, and B. Fehse. 2001. T lymphocytes as targets of gene transfer with Moloney-type retroviral vectors. Curr. Gene Ther. 1: 325-337.
65. Morgan, R. A., M. E. Dudley, Y. Y. Yu, Z. Zheng, P. F. Robbins, M. R. Theoret, J. R. Wunderlich, M. S. Hughes, N. P. Restifo, and S. A. Rosenberg. 2003. High efficiency TCR gene transfer into primary human lymphocytes affords avid recognition of melanoma tumor antigen glycoprotein 100 and does not alter the recognition of autologous melanoma antigens. J. Immunol. 171: 3287-3295.
66. + Tregs by TCR gene transfer favors transplantation tolerance in mice. J. Clin. Invest. 118: 3619-3628.
67. Levavasseur, E., P. Metharom, G. Dorban, H. Nakano, T. Kakiuchi, C. Carnaud, P. Sarradin, and P. Aucouturier. 2007. Experimental scrapie in 'plt' mice: an assessment of the role of dendritic-cell migration in the pathogenesis of prion diseases. J. Gen. Virol. 88: 2353-2360.
68. + T lymphocytes in vivo. J. Immunol. 162: 766-773.
69. + regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22: 531-562.
70. Butcher, E. C. 1991. Leukocyte-endothelial cell recognition: three (or more) steps to specificity and diversity. Cell 67: 1033-1036.
71. Beringue, V., P. Couvreur, and D. Dormont. 2002. Involvement of macrophages in the pathogenesis of transmissible spongiform encephalopathies. Dev. Immunol. 9: 19-27.
72. Carp, R. I., and S. M. Callahan. 1982. Effect of mouse peritoneal macrophages on scrapie infectivity during extended in vitro incubation. Intervirology 17: 201-207. (Pubitemid 12092085)
73. Spinner, D. S., I. S. Cho, S. Y. Park, J. I. Kim, H. C. Meeker, X. Ye, G. Lafauci, D. J. Kerr, M. J. Flory, B. S. Kim, et al. 2008. Accelerated prion disease pathogenesis in Toll-like receptor 4 signaling-mutant mice. J. Virol. 82: 10701-10708.
74. Betmouni, S., V. H. Perry, and J. L. Gordon. 1996. Evidence for an early inflammatory response in the central nervous system of mice with scrapie. Neuroscience 74: 1-5.
75. Lewicki, H., A. Tishon, D. Homann, H. Mazarguil, F. Laval, V. C. Asensio, I. L. Campbell, S. DeArmond, B. Coon, C. Teng, et al. 2003. T cells infiltrate the brain in murine and human transmissible spongiform encephalopathies. J. Virol. 77: 3799-3808.
76. Nicoll, J. A., D. Wilkinson, C. Holmes, P. Steart, H. Markham, and R. O. Weller. 2003. Neuropathology of human Alzheimer disease after immunization with amyloid-β peptide: a case report. Nat. Med. 9: 448-452.
77. Orgogozo, J. M., S. Gilman, J. F. Dartigues, B. Laurent, M. Puel, L. C. Kirby, P. Jouanny, B. Dubois, L. Eisner, S. Flitman, et al. 2003. Subacute meningoencephalitis in a subset of patients with AD after Aβ42 immunization. Neurology 61: 46-54.