Protease-sensitive prion species in neoplastic spleens of prion-infected mice with uncoupling of PrPSc and prion infectivity

Journal of General Virology

Volumn 94, Issue PART2, 2013, Pages 453-463

  Krasemann, Susanne ^a   Neumann, Melanie ^a   Szalay, Beata ^a   Stocking, Carol ^b   Glatzel, Markus ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN; PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CONTROLLED STUDY; KINETICS; LYMPH FOLLICLE; MOUSE; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; SPLEEN; TISSUE STRUCTURE;

ANIMALS; DISEASE MODELS, ANIMAL; MICE; PEPTIDE HYDROLASES; PRION DISEASES; PRIONS; SPLEEN; SPLENIC NEOPLASMS;

MUS;

EID: 84872478852     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.045922-0     Document Type: Article

References (67)

1. Aguzzi, A. (1997). Neuro-immune connection in spread of prions in the body? Lancet 349, 742-743.
2. Aguzzi, A. (2003). Prions and the immune system: a journey through gut, spleen, and nerves. Adv Immunol 81, 123-171.
3. Aguzzi, A. (2004). Understanding the diversity of prions. Nat Cell Biol 6, 290-292.
4. Aguzzi, A. & Rajendran, L. (2009). The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64, 783-790.
5. Barria, M. A., Mukherjee, A., Gonzalez-Romero, D., Morales, R. & Soto, C. (2009). De novo generation of infectious prions in vitro produces a new disease phenotype. PLoS Pathog 5, e1000421.
6. Barron, R. M., Campbell, S. L., King, D., Bellon, A., Chapman, K. E., Williamson, R. A. & Manson, J. C. (2007). High titers of transmissible spongiform encephalopathy infectivity associated with extremely low levels of PrPSc in vivo. J Biol Chem 282, 35878-35886.
7. Blattler, 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.
8. Bolton, D. C., McKinley, M. P. & Prusiner, S. B. (1982). Identification of a protein that purifies with the scrapie prion. Science 218, 1309-1311.
9. 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.
10. Brown, K. L., Stewart, K., Ritchie, D., Fraser, H., Morrison, W. I. & Bruce, M. E. (2000). Follicular dendritic cells in scrapie pathogenesis. Arch Virol Suppl 16, 13-21.
11. Bueler, H. R., Fischer, M., Lang, Y., Bluethmann, H., Lipp, H. P., DeArmond, S. J., Prusiner, S. B., Aguet, M. & Weissmann, C. (1992). Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356, 577-582.
12. Castro-Seoane, R., Hummerich, H., Sweeting, T., Tattum, M. H., Linehan, J. M., Fernandez de Marco, M., Brandner, S., Collinge, J. & Klohn, P. C. (2012). Plasmacytoid dendritic cells sequester high prion titres at early stages of prion infection. PLoS Pathog 8, e1002538.
13. Caughey, B., Raymond, G. J., Ernst, D. & Race, R. E. (1991). N-terminal truncation of the scrapie-associated form of PrP by lysosomal protease(s): implications regarding the site of conversion of PrP to the protease-resistant state. J Virol 65, 6597-6603.
14. Cronier, S., Gros, N., Tattum, M. H., Jackson, G. S., Clarke, A. R., Collinge, J. & Wadsworth, J. D. (2008). Detection and characterization of proteinase K-sensitive disease-related prion protein with thermolysin. Biochem J 416, 297-305.
15. Fischer, M., Rulicke, T., Raeber, A., Sailer, A., Moser, M., Oesch, B., Brandner, S., Aguzzi, A. & Weissmann, C. (1996). Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J 15, 1255-1264.
16. Gambetti, P., Dong, Z., Yuan, J., Xiao, X., Zheng, M., Alshekhlee, A., Castellani, R., Cohen, M., Barria, M. A. & other authors (2008). A novel human disease with abnormal prion protein sensitive to protease. Ann Neurol 63, 697-708.
17. Ganor, Y., Grinberg, I., Reis, A., Cooper, I., Goldstein, R. S. & Levite, M. (2009). Human T-leukemia and T-lymphoma express glutamate receptor AMPA GluR3, and the neurotransmitter glutamate elevates the cancer-related matrix-metalloproteinases inducer CD147/ EMMPRIN, MMP-9 secretion and engraftment of T-leukemia in vivo. Leuk Lymphoma 50, 985-997.
18. Geissen, M., Krasemann, S., Matschke, J. & Glatzel, M. (2007). Understanding the natural variability of prion diseases. Vaccine 25, 5631-5636.
19. C expression in the peripheral nervous system is a determinant of prion neuroinvasion. J Gen Virol 81, 2813-2821.
20. Glatzel, M. & Aguzzi, A. (2001). Sympathetic prions. ScientificWorldJournal 1, 555-556.
21. Glatzel, M., Abela, E., Maissen, M. & Aguzzi, A. (2003). Extraneural pathologic prion protein in sporadic Creutzfeldt-Jakob disease. N Engl J Med 349, 1812-1820.
22. Glatzel, M., Stoeck, K., Seeger, H., Luhrs, T. & Aguzzi, A. (2005). Human prion diseases: molecular and clinical aspects. Arch Neurol 62, 545-552.
23. González, L., Thorne, L., Jeffrey, M., Martin, S., Spiropoulos, J., Beck, K. E., Lockey, R. W., Vickery, C. M., Holder, T. & Terry, L. (2012). Infectious titres of sheep scrapie and bovine spongiform encephalopathy agents cannot be accurately predicted from quantitative laboratory test results. J Gen Virol 93, 2518-2527.
24. Harbers, K., Schnieke, A., Stuhlmann, H., Jahner, D. & Jaenisch, R. (1981). DNA methylation and gene expression: endogenous retroviral genome becomes infectious after molecular cloning. Proc Natl Acad Sci U S A 78, 7609-7613.
25. Hoffmann, C., Eiden, M., Kaatz, M., Keller, M., Ziegler, U., Rogers, R., Hills, B., Balkema-Buschmann, A., van Keulen, L. & other authors (2011). BSE infectivity in jejunum, ileum and ileocaecal junction of incubating cattle. Vet Res 42, 21.
26. Horiuchi, M. & Caughey, B. (1999). Specific binding of normal prion protein to the scrapie form via a localized domain initiates its conversion to the protease-resistant state. EMBO J 18, 3193-3203.
27. Hsiao, K. K., Groth, D., Scott, M., Yang, S. L., Serban, H., Rapp, D., Foster, D., Torchia, M., Dearmond, S. J. & Prusiner, S. B. (1994). Serial transmission in rodents of neurodegeneration from transgenic mice expressing mutant prion protein. Proc Natl Acad Sci U S A 91, 9126-9130.
28. Jeffrey, M. & González, L. (2004). Pathology and pathogenesis of bovine spongiform encephalopathy and scrapie. Curr Top Microbiol Immunol 284, 65-97.
29. 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 immuno-electron microscopy. J Pathol 191, 323-332.
30. Jewell, J. E., Brown, J., Kreeger, T. & Williams, E. S. (2006). Prion protein in cardiac muscle of elk (Cervus elaphus nelsoni) and white-tailed deer (Odocoileus virginianus) infected with chronic wasting disease. J Gen Virol 87, 3443-3450.
31. c in stromal and hematopoietic cells. J Virol 75, 7097-7106.
32. Kimberlin, R. H. & Walker, C. A. (1989). The role of the spleen in the neuroinvasion of scrapie in mice. Virus Res 12, 201-211.
33. Klohn, P. C., Stoltze, L., Flechsig, E., Enari, M. & Weissmann, C. (2003). A quantitative, highly sensitive cell-based infectivity assay for mouse scrapie prions. Proc Natl Acad Sci U S A 100, 11666-11671.
34. Kranich, J., Krautler, N. J., Heinen, E., Polymenidou, M., Bridel, C., Schildknecht, A., Huber, C., Kosco-Vilbois, M. H., Zinkernagel, R. &other authors (2008). Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8. J Exp Med 205, 1293-1302.
35. Krasemann, S., Neumann, M., Luepke, J. P., Grashorn, J., Wurr, S., Stocking, C. & Glatzel, M. (2012). Persistent retroviral infection with MoMuLV influences neuropathological signature and phenotype of prion disease. Acta Neuropathol 124, 111-126.
36. Lasmézas, 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, 402-404.
37. res level disparity. Mol Neurodegener 7, 18.
38. 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 C1q significantly delays onset of scrapie. Nat Med 7, 485-487.
39. Mahal, S. P., Baker, C. A., Demczyk, C. A., Smith, E. W., Julius, C. & Weissmann, C. (2007). Prion strain discrimination in cell culture: the cell panel assay. Proc Natl Acad Sci U S A 104, 20908-20913.
40. Manson, J. C., Jamieson, E., Baybutt, H., Tuzi, N. L., Barron, R., McConnell, I., Somerville, R., Ironside, J., Will, R. & other authors (1999). A single amino acid alteration (101L) introduced into murine PrP dramatically alters incubation time of transmissible spongiform encephalopathy. EMBO J 18, 6855-6864.
41. McCulloch, L., Brown, K. L., Bradford, B. M., Hopkins, J., Bailey, M., Rajewsky, K., Manson, J. C. & Mabbott, N. A. (2011). Follicular dendritic cell-specific prion protein (PrP) expression alone is sufficient to sustain prion infection in the spleen. PLoS Pathog 7, e1002402.
42. 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.
43. Oesch, B., Westaway, D., Walchli, M., McKinley, M. P., Kent, S. B., Aebersold, R., Barry, R. A., Tempst, P., Teplow, D. B. & other authors (1985). A cellular gene encodes scrapie PrP 27-30 protein. Cell 40, 735-746.
44. Owen, J. L., Torroella-Kouri, M. & Iragavarapu-Charyulu, V. (2008). Molecular events involved in the increased expression of matrix metalloproteinase-9 by T lymphocytes of mammary tumor-bearing mice. Int J Mol Med 21, 125-134.
45. Piccardo, P., Manson, J. C., King, D., Ghetti, B. & Barron, R. M. (2007). Accumulation of prion protein in the brain that is not associated with transmissible disease. Proc Natl Acad Sci U S A 104, 4712-4717.
46. Polymenidou, M., Moos, R., Scott, M., Sigurdson, C., Shi, Y. Z., Yajima, B., Hafner-Bratkovic, I., Jerala, R., Hornemann, S. & other authors (2008). The POM monoclonals: a comprehensive set of antibodies to non-overlapping prion protein epitopes. PLoS ONE 3, e3872.
47. Prinz, M., Heikenwalder, M., Junt, T., Schwarz, P., Glatzel, M., Heppner, F. L., Fu, Y.-X., Lipp, M. & Aguzzi, A. (2003a). Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature 425, 957-962.
48. Prinz, M., Heikenwalder, M., Schwarz, P., Takeda, K., Akira, S. & Aguzzi, A. (2003b). Prion pathogenesis in the absence of Toll-like receptor signalling. EMBO Rep 4, 195-199.
49. Prusiner, S. B. (1982). Novel proteinaceous infectious particles cause scrapie. Science 216, 136-144.
50. Prusiner, S. B. (1998). Prions. Proc Natl Acad Sci U S A 95, 13363-13383.
51. Qi, X., Moore, R. A. & McGuirl, M. A. (2012). Dissociation of recombinant prion protein fibrils into short protofilaments: implica-tions for the endocytic pathway and involvement of the N-terminal domain. Biochemistry 51, 4600-4608.
52. Race, R. E. & Ernst, D. (1992). Detection of proteinase K-resistant prion protein and infectivity in mouse spleen by 2 weeks after scrapie agent inoculation. J Gen Virol 73, 3319-3323.
53. Rodenburg, M., Fischer, M., Engelmann, A., Harbers, S. O., Ziegler, M., Lohler, J. & Stocking, C. (2007). Importance of receptor usage, Fli1 activation, and mouse strain for the stem cell specificity of 10A1 murine leukemia virus leukemogenicity. J Virol 81, 732-742.
54. Rosenberg, N. & Jolicoeur, P. (1997). Retroviral pathogenesis. In Retroviruses, pp. 475-585. Edited by J. M. Coffin, S. H. Hughes & H. E. Varmus. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
55. Sc molecules with different conformations. Nat Med 4, 1157-1165.
56. Sajnani, G., Silva, C. J., Ramos, A., Pastrana, M. A., Onisko, B. C., Erickson, M. L., Antaki, E. M., Dynin, I., Vázquez-Fernández, E. & other authors (2012). PK-sensitive PrP is infectious and shares basic structural features with PK-resistant PrP. PLoS Pathog 8, e1002547.
57. Sakaguchi, S., Katamine, S., Yamanouchi, K., Kishikawa, M., Moriuchi, R., Yasukawa, N., Doi, T. & Miyamoto, T. (1993). Kinetics of infectivity are dissociated from PrP accumulation in salivary glands of Creutzfeldt-Jakob disease agent-inoculated mice. J Gen Virol 74, 2117-2123.
58. Sandberg, M. K., Al-Doujaily, H., Sharps, B., Clarke, A. R. & Collinge, J. (2011). Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 470, 540-542.
59. Sc profiling in sporadic Creutzfeldt-Jakob disease. PLoS Med 3, e14.
60. Schwieger, M., Lohler, J., Friel, J., Scheller, M., Horak, I. & Stocking, C. (2002). AML1-ETO inhibits maturation of multiple lympho-hematopoietic lineages and induces myeloblast transformation in synergy with ICSBP deficiency. J Exp Med 196, 1227-1240.
61. Silveira, J. R., Raymond, G. J., Hughson, A. G., Race, R. E., Sim, V. L., Hayes, S. F. & Caughey, B. (2005). The most infectious prion protein particles. Nature 437, 257-261.
62. Supattapone, S. (2004). Prion protein conversion in vitro. J Mol Med (Berl) 82, 348-356.
63. Thackray, A. M., Hopkins, L. & Bujdoso, R. (2007). Proteinase K-sensitive disease-associated ovine prion protein revealed by conformation-dependent immunoassay. Biochem J 401, 475-483.
64. Tzaban, S., Friedlander, G., Schonberger, O., Horonchik, L., Yedidia, Y., Shaked, G., Gabizon, R. & Taraboulos, A. (2002). Protease-sensitive scrapie prion protein in aggregates of heterogeneous sizes. Biochemistry 41, 12868-12875.
65. Urayama, A., Morales, R., Niehoff, M. L., Banks, W. A. & Soto, C. (2011). Initial fate of prions upon peripheral infection: half-life, distribution, clearance, and tissue uptake. FASEB J 25, 2792-2803.
66. Wadsworth, J. D. F., Joiner, S., Hill, A. F., Campbell, T. A., Desbruslais, M., Luthert, P. J. & Collinge, J. (2001). Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 358, 171-180.
67. Zabel, M. D., Heikenwalder, M., Prinz, M., Arrighi, I., Schwarz, P., Kranich, J., von Teichman, A., Haas, K. M., Zeller, N. & other authors (2007). Stromal complement receptor CD21/35 facilitates lymphoid prion colonization and pathogenesis. J Immunol 179, 6144-6152