Neuroinvasion by scrapie following inoculation via the skin is independent of migratory Langerhans cells

Journal of Virology

Volumn 79, Issue 3, 2005, Pages 1888-1897

  Mohan, Joanne ^a   Bruce, Moira E ^a   Mabbott, Neil A ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 ANTIGEN; CD40 LIGAND; DIMETHYL SULFOXIDE; INTERLEUKIN 1BETA CONVERTING ENZYME; PRION PROTEIN; PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTATION; ARTICLE; BRAIN TISSUE; CELL MIGRATION; GERMINAL CENTER; IMMUNOHISTOCHEMISTRY; INOCULATION; LANGERHANS CELL; MOUSE; NONHUMAN; PRION DISEASE; PRIORITY JOURNAL; PROTEIN DEGRADATION; SCAR FORMATION; SCRAPIE AGENT; VIRUS PATHOGENESIS; VIRUS TRANSMISSION; WILD TYPE; ANIMAL; BAGG ALBINO MOUSE; BRAIN; C57BL MOUSE; DISEASE PREDISPOSITION; DRUG ANTAGONISM; GENETICS; METABOLISM; PATHOGENICITY; PATHOLOGY; PATHOPHYSIOLOGY; SCRAPIE; SKIN;

ANIMALS; BRAIN; CASPASE 1; CD40 LIGAND; DISEASE SUSCEPTIBILITY; LANGERHANS CELLS; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PRPSC PROTEINS; SCRAPIE; SKIN;

EID: 13744252664     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.79.3.1888-1897.2005     Document Type: Article

References (61)

1. Antonopoulos, C., M. Cumberbatch, R. J. Dearman, R. J. Daniel, I. Kimber, and R. W. Groves. 2001. Functional caspase-1 is required for Langerhans cell migration and optimal contact sensitization in mice. J. Immunol. 166:3672-3677.
2. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18:767-811.
3. Bartz, J. C., A. E. Kincaid, and R. A. Bessen. 2003. Rapid prion neuroinvasion following tongue infection. J. Virol. 77:583-591.
4. Beringue, V., M. Demoy, C. I. Lasmezas, B. Gouritin, C. Weingarten, J.-P. Deslys, J.-P. Adreux, P. Couvreur, and D. Dormont. 2000. Role of spleen macrophages in the clearance of scrapie agent early in pathogenesis. J. Pathol. 190:495-502.
5. Bosque, P. J., and S. B. Prusiner. 2000. Cultured cell sublines highly susceptible to prion infection. J. Virol. 74:4377-4386.
6. Brown, K. L., K. Stewart, D. Ritchie, N. A. Mabbott, A. Williams, H. Fraser, W. I. Morrison, and M. E. Bruce. 1999. Scrapie replication in lymphoid tissues depends on PrP-expressing follicular dendritic cells. Nat. Med. 5:1308-1312.
7. Bruce, M. E., R. G. Will, J. W. Ironside, I. McConnell, D. Drummond, A. Suttie, L. McCardle, A. Chree, J. Hope, C. Birkett, S. Cousens, H. Fraser, and C. J. Bostock. 1997. Transmissions to mice indicate that "new variant" CJD is caused by the BSE agent. Nature 389:498-501.
8. Burwinkel, M., A. Schwarz, C. Riemer, J. Schultz, F. van Landeghem, and M. Baier. 2004. Rapid disease development in scrapie-infected mice deficient for CD40 ligand. EMBO Rep. 5:527-531.
9. Campbell, K. A., P. J. Ovendale, M. K. Kennedy, W. C. Fanslow, S. G. Reed, and C. R. Maliszewski. 1996. CD40 ligand is required for protective cell-mediated immunity to Leishmania major. Immunity 4:283-289.
10. 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.
11. Carp, R. I., and S. M. Callahan. 1981. In vitro interaction of scrapie agent and mouse peritoneal macrophages. Intervirology 16:8-13.
12. Cumberbatch, M., R. J. Dearman, and I. Kimber. 1997. Langerhans cells require signals from both tumour necrosis factor-α and interleukin-1β for migration. Immunology 92:388-396.
13. 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.
14. Endres, R., M. B. Alimzhanov, T. Plitz, A. Futterer, M. H. Kosco-Vilbois, S. A. Nedospasov, K. Rajewsky, and K. Pfeffer. 1999. Mature follicular dendritic cell networks depend on expression of lymphotoxin β receptor by radioresistant stromal cells and of lymphotoxin β and tumour necrosis factor by B cells. J. Exp. Med. 189:159-168.
15. Farquhar, C. F., J. Dornan, R. A. Somerville, A. M. Tunstall, and J. Hope. 1994. 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. 75:495-504.
16. Fraser, H., K. L. Brown, K. Stewart, I. McConnell, P. McBride, and A. Williams. 1996. Replication of scrapie in spleens of SCID mice follows reconstitution with wild-type mouse bone marrow. J. Gen. Virol. 77:1935-1940.
17. Fraser, H., and A. G. Dickinson. 1973. Agent-strain differences in the distribution and intensity of gray matter vacuolation. J. Comp. Pathol. 83:29-40.
18. Fraser, H., and A. G. Dickinson. 1968. The sequential development of the brain lesions of scrapie in three strains of mice. J. Comp. Pathol. 78:301-311.
19. Garcia Calvo, M., E. P. Peterson, B. Leiting, R. Ruel, D. W. Nicholson, and N. A. Thornberry. 1998. Inhibition of human caspases by peptide-based and macromolecular inhibitors. J. Biol. Chem. 273:32608-32613.
20. Glatzel, M., F. L. Heppner, K. M. Albers, and A. Aguzzi. 2001. Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 31:25-34.
21. Hill, A. F., R. J. Butterworth, S. Joiner, G. Jackson, M. N. Rossor, D. J. Thomas, A. Frosh, N. Tolley, J. E. Bell, M. Spencer, A. King, S. Al-Sarraj, J. W. Ironside, P. L. Lantos, and J. Collinge. 1999. Investigation of variant Creutzfeldt-Jakob disease and other prion diseases with tonsil biopsy samples. Lancet 353:183-189.
22. Hill, A. F., M. Desbruslais, S. Joiner, K. C. L. Sidle, I. Gowland, and J. Collinge. 1997. The same prion strain causes vCJD and BSE. Nature 389: 448-450.
23. Sc from the gut. J. Gen. Virol. 83:267-271.
24. Kaneider, N. C., A. Kaser, S. Dunzendorfer, H. Tilg, and C. J. Wiedermann. 2003. Sphingosine kinase-dependent migration of immature dendritic cells in response to neurotoxic prion protein fragment. J. Virol. 77:5535-5539.
25. Kapasi, Z. F., G. F. Burton, L. D. Schultz, J. G. Tew, and A. K. Szakal. 1993. Induction of functional follicular dendritic cell development in severe combined immunodeficiency mice. J. Immunol. 150:2648-2658.
26. Klein, M. A., R. Frigg, E. Flechsig, A. J. Raeber, U. Kalinke, H. Bluethman, F. Bootz, M. Suter, R. M. Zinkernagel, and A. Aguzzi. 1997. A crucial role for B cells in neuroinvasive scrapie. Nature 390:687-691.
27. Klein, M. A., R. Frigg, A. J. Raeber, E. Flechsig, I. Hegyi, R. M. Zinkernagel, C. Weissmann, and A. Aguzzi. 1998. PrP expression in B lymphocytes is not required for prion neuroinvasion. Nat. Med. 4:1429-1433.
28. Klein, M. A., P. S. Kaeser, P. Schwarz, H. Weyd, I. Xenarios, R. M. Zinkernagel, M. C. Carroll, J. S. Verbeek, M. Botto, M. J. Walport, H. Molina, U. Kalinke, H. Acha-Orbea, and A. Aguzzi. 2001. Complement facilitates early prion pathogenesis. Nat. Med. 7:488-492.
29. Kopf, M., S. Herren, M. V. Wiles, M. B. Pepys, and M. H. Kosco-Vilbois. 1998. Interleukin 6 influences germinal center development and antibody production via a contribution of C3 complement component. J. Exp. Med. 188:1895-1906.
30. + myeloid dendritic cells in vitro. J. Virol. 76:12259-12264.
31. Mabbott, N. A., M. E. Bruce, M. Botto, M. J. Walport, and M. B. Pepys. 2001. Temporary depletion of complement component C3 or genetic deficiency of C1q significantly delays onset of scrapie. Nat. Med. 7:485-487.
32. Mabbott, N. A., F. Mackay, F. Minns, and M. E. Bruce. 2000. Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nat. Med. 6:719-720.
33. Mabbott, N. A., A. Williams, C. F. Farquhar, M. Pasparakis, G. Kollias, and M. E. Bruce. 2000. Tumor necrosis factor-alpha-deficient, but not interleukin-6-deficient, mice resist peripheral infection with scrapie. J. Virol. 74: 3338-3344.
34. Mabbott, N. A., J. Young, I. McConnell, and M. E. Bruce. 2003. Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility. J. Virol. 77:6845-6854.
35. MacDonald, G. H., and R. E. Johnston. 2000. Role of dendritic cell targeting in Venezuelan equine encephalitis virus pathogenesis. J. Virol. 62:914-922.
36. Marriott, I., E. K. Thomas, and K. L. Bost. 1999. CD40-CD40 ligand interactions augment survival of normal mice, but not CD40 ligand knockout mice, challenged orally with Salmonella dublin. Infect. Immun. 67:5253-5257.
37. McBride, P., P. Eikelenboom, G. Kraal, H. Fraser, and M. E. Bruce. 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.
38. Meyer, R. K., M. P. McKinley, K. A. Bowman, M. B. Braunfeld, R. A. Barry, and S. B. Prusiner. 1986. Separation and properties of cellular and scrapie priori proteins. Proc. Natl. Acad. Sci. USA 83:2310-2314.
39. 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.
40. Moodycliffe, A. M., V. Shreedhar, S. E. Ullrich, J. Walterscheid, C. Bucana, M. L. Kripke, and L. Flores-Romo. 2000. CD40-CD40 ligand interactions in vivo regulate migration of antigen-bearing dendritic cells from the skin to draining lymph nodes. J. Exp. Med. 191:2011-2020.
41. Oldstone, M. B. A., R. Race, D. Thomas, H. Lewicki, D. Homman, S. Smelt, A. Holz, P. Koni, D. Lo, B. Chesebro, and R. Flavell. 2002. Lymphotoxin-α- and lymphotoxin-β-deficient mice differ in susceptibility to scrapie: evidence against dendritic cell involvement. J. Virol. 76:4357-4363.
42. Prinz, M., M. Heikenwalder, T. Junt, P. Schwarz, M. Glatzel, F. L. Heppner, Y.-X. Fu, M. Lipp, and A. Aguzzi. 2003. Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature 425:957-962.
43. Prinz, M., F. Montrasio, M. A. Klein, P. Schwarz, J. Priller, B. Odermatt, K. Pfeffer, and A. Aguzzi. 2002. Lymph nodal prion replication and neuroinvasion in mice devoid of follicular dendritic cells. Proc. Natl. Acad. Sci. USA 99:919-924.
44. Prusiner, S. B., D. C. Bolton, D. F. Groth, K. A. Bowman, S. P. Cochran, and M. P. McKinley. 1982. Further purification and characterisation of scrapie prions. Biochemistry 21:6942-6950.
45. Reece, J. C., A. J. Handley, E. J. Anstee, W. A. Morrison, S. M. Crowe, and P. U. Cameron. 1998. HIV-1 selection by epidermal dendritic cells during transmission across human skin. J. Exp. Med. 187:1623-1631.
46. Ryan, S., L. Tiley, I. McConnell, and B. Blacklaws. 2000. Infection of dendritic cells by the maedi-visna lentivirus. J. Virol. 74:10096-10103.
47. res in mule deer fawns (Odocoileus hemionus). J. Gen. Virol. 80:2757-2764.
48. Soong, L., J. C. Xu, I. S. Grewal, P. Kima, J. Sun, B. J. Longley, Jr., N. H. Ruddle, D. McMahon-Pratt, and R. A. Flavell. 1996. Disruption of CD40-CD40 ligand interactions results in an enhanced susceptibility to Leishmania amazonensis infection. Immunity 4:263-273.
49. Stoitzner, P., M. Zanella, U. Ortner, M. Lukas, A. Tagwerker, K. Janke, M. B. Lutz, G. Schuler, B. Echtenacher, B. Ryffel, F. Koch, and N. Romani. 1999. Migration of Langerhans cells and dermal dendritic cells in skin organ cultures: augmentation by TNF-α and IL-1β. J. Leukoc. Biol. 66:462-470.
50. Tan, J., T. Town, T. Mori, D. Obregon, Y. Wu, A. DelleDonne, A. Rojiani, F. Crawford, R. A. Flavell, and M. Mullan. 2002. CD40 is expressed and functional on neuronal cells. EMBO J. 21:643-652.
51. Taylor, D. M., I. McConnell, and H. Fraser. 1996. Scrapie infection can be established readily through skin scarification in immunocompetent but not immunodeficient mice. J. Gen. Virol. 77:1595-1599.
52. Thornberry, N. A., H. G. Bull, J. R. Calaycay, K. T. Chapman, A. D. Howard, M. J. Kostura, D. K. Miller, S. M. Molineaux, J. R. Weidner, J. Aunins, et al. 1992. A novel heterodimeric cysteine protease is required for interleukin-1b processing in monocytes. Nature 356:768-784.
53. Thornberry, N. A., E. P. Peterson, J. J. Zhao, A. D. Howard, P. R. Griffin, and K. T. Chapman. 1994. Inactivation of interleukin-1β converting enzyme by peptide (acyloxy)methyl ketones. Biochemistry 33:3934-3940.
54. Timares, L., A. Takashima, and S. A. Johnston. 1998. Quantitative analysis of the immunopotency of genetically transfected dendritic cells. Proc. Natl. Acad. Sci. USA 95:13147-13152.
55. van Keulen, L. J. M., B. E. C. Schreuder, R. H. Meloen, G. Mooij-Harkes, M. E. W. Vromans, and J. P. M. Langeveld. 1996. Immunohistological detection of prion protein in lymphoid tissues of sheep with natural scrapie. J. Clin. Microbiol. 34:1228-1231.
56. Wu, S.-J. L., G. Grouard-Vogel, W. Sun, J. R. Mascola, E. Brachtel, R. Putvatana, M. K. Louder, L. Filgueira, M. A. Marovich, H. K. Wong, A. Blauvelt, G. S. Murphy, M. L. Robb, B. L. Innes, D. L. Birx, C. G. Hayes, and S. Schlesinger Frankel. 2000. Human skin Langerhans cells are targets of dengue virus infection. Nat. Med. 6:816-820.
57. Wykes, M., A. Pombo, C. Jenkins, and G. G. MacPherson. 1998. Dendritic cells interact directly with Naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 161:1313-1319.
58. Xu, J., T. M. Foy, J. D. Laman, E. A. Elliot, J. J. Dunn, T. J. Waldschmidt, R. Elsemore, R. J. Noelle, and R. A. Flavell. 1994. Mice deficient for the CD40 ligand. Immunity 1:423-431.
59. Xu, S., K. Ariizumi, G. Caceres-Dittmar, D. Edelbaum, K. Hashimoto, P. R. Bergstresser, and A. Takashima. 1995. Successive generation of antigen-presenting dendritic cell lines from murine epidermis. J. Immunol. 154:2697-2705.
60. + cell line (XS52) by IL-4, TNF-α, IL-1β, and agonistic anit-CD40 monoclonal antibody. J. Immunol. 163:5331-5337.
61. Zanusso, G., D. Liu, S. Ferrari, I. Hegyi, X. Yin, A. Aguzzi, S. Hornemann, S. Liemann, R. Glockshuber, J. C. Manson, P. Brown, R. B. Petersen, P. Gambetti, and M.-S. Sy. 1998. Prion protein expression in different species: analysis with a panel of new mAbs. Proc. Natl. Acad. Sci. USA 95:8812-8816.