Resistance of neonatal mice to scrapie is associated with inefficient infection of the immature spleen

Journal of Virology

Volumn 80, Issue 1, 2006, Pages 474-482

  Ierna, Michelle ^a,b   Farquhar, Christine F ^a   Outram, George W ^a   Bruce, Moira E ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

^b MD Biosciences   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOASSAY; CATTLE; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; IMMATURITY; IMMUNOCYTOCHEMISTRY; INFECTION RESISTANCE; INFECTION SENSITIVITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SCRAPIE; SHEEP; SPLEEN; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS RESISTANCE;

ANIMALS; ANIMALS, NEWBORN; DENDRITIC CELLS, FOLLICULAR; INFUSIONS, PARENTERAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PRPSC PROTEINS; SCRAPIE; SPLEEN;

ANIMALIA; BOS TAURUS; OVIS ARIES;

EID: 33645995108     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.80.1.474-482.2006     Document Type: Article

References (57)

1. Andreoletti, O., P. Berthon, E. Levavasseur, D. Marc, F. Lantier, E. Monks, J.-M. Eisen, and F. Schelcher. 2002. Phenotyping of protein-prion (PrPsc)-accumulating cells in lymphoid and neural tissues of naturally scrapie-affected sheep by double labeling immunohistochemistry. J. Histochem. Cytochem. 50:1357-1370.
2. Sc accumulation in placentas of ewes exposed to natural scrapie: influence of foetal PrP genotype and effect on ewe-to-lamb transmission. J. Gen. Virol. 83:2607-2616.
3. Arnold, M. E., and J. W. Wilesmith. 2004. Estimation of the age-dependent risk of infection to BSE of dairy cattle in Great Britain. Prev. Vet. Med. 66:35-47.
4. Asano, S., Y. Akaike, T. Muramatsu, M. Mochizuki, T. Tsuda, and H. Wakasa. 1993. Immunohistological detection of the primary follicle (PF) in human fetal and newborn lymph node anlages. Pathol. Res. Pract. 189:921-927.
5. Balogh, P., Y. Aydar, J. G. Tew, and A. K. Szakal. 2001. Ontogeny of the follicular dendritic cell phenotype and function in the postnatal murine spleen. Cell. Immunol. 214:45-53.
6. Brown, K. L., D. L. Ritchie, P. A. McBride, and M. E. Bruce. 2000. Detection of PrP in extraneural tissues. Microsc. Res. Tech. 50:40-45.
7. 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. Nature Med. 5:1308-1312.
8. Bruce, M. E., I. McConnell, R. G. Will, and J. W. Ironside. 2001. Detection of variant Creutzfeldt-Jakob disease infectivity in extraneural tissues. Lancet 358:208-209.
9. Bueler, H., A. Aguzzi, A. Sailer, R.-A. Greiner, P. Autenried, M. Aguet, and C. Weissmann. 1993. Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.
10. Caramelli, M., G. Ru, C. Casalone, E. Bozzetta, P. L. Acutis, A. Calella, and G. Forloni. 2001. Evidence for the transmission of scrapie to sheep and goats from a vaccine against Mycoplasma agalactiae. Vet. Rec. 148:531-536.
11. Diaz, C., Z. G. Vitezica, R. Rupp, O. Andreoletti, and J. M. Elsen. 2005. Polygenic variation and transmission factors involved in the resistance/ susceptibility to scrapie in a Romanov flock. J. Gen. Virol. 86:849-857.
12. Dickinson, A. G., V. M. H. Meikle, and H. Fraser. 1969. Genetical control of the concentration of ME7 scrapie agent in the brain of mice. J. Comp. Pathol. 79:15-22.
13. Dickinson, A. G., V. M. H. Meikle, and H. Fraser. 1968. Identification of a gene which controls the incubation period of some strains of scrapie agent in mice. J. Comp. Pathol. 78:293-299.
14. Dickinson, A. G., J. T. Stamp, and C. C. Renwick. 1974. Maternal and lateral transmission of scrapie in sheep. J. Comp. Pathol. 84:19-25.
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. Farquhar, C. F., R. A. Somerville, and L. A. Ritchie. 1989. Post-mortem immunodiagnosis of scrapie and bovine spongiform encephalopathy. J. Virol. Methods 24:215-221.
17. Finney, D. J. 1978. Statistical method in biological assay, 3rd ed. Charles Griffin and Co., London, United Kingdom.
18. Fraser, H. 1993. Diversity in the neuropathology of scrapie-like diseases in animals. Br. Med. Bull. 49:792-809.
19. 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.
20. Fraser, H., and A. G. Dickinson. 1978. Studies of the lymphoreticular system in the pathogenesis of scrapie: the role of spleen and thymus. J. Comp. Pathol. 88:563-573.
21. Ghani, A., N. M. Ferguson, C. A. Donnelly, and R. M. Anderson. 2003. Factors determining the pattern of the variant Creutzfeldt-Jakob disease (vCJD) epidemic in the UK. Proc. R. Soc. Lond. B 270:689-698.
22. Hadlow, W. J., R. C. Kennedy, and R. E. Race. 1982. Natural infection of Suffolk sheep with scrapie virus. J. Infect. Dis. 146:657-664.
23. Halleraker, M., C. M. Press, and T. Landsverk. 1994. Development and cell phenotypes in primary follicles of foetal sheep lymph nodes. Cell Tissue Res. 275:51-62.
24. Head, M. W., D. L. Ritchie, N. Smith, V. McLoughlin, W. Nailon, S. Samad, S. Masson, M. Bishop, L. McCardle, and J. W. Ironside. 2004. Peripheral tissue involvement in sporadic, iatrogenic, and variant Creutzfeldt-Jakob disease: an immunohistochemical, quantitative, and biochemical study. Am. J. Pathol. 164:143-153.
25. Hoshi, H., K. Horie, K. Tanaka, H. Nagata, S. Aizawa, M. Hiramoto, T. Ryouke, and H. Aijima. 2001. Patterns of age-dependent changes in the numbers of lymph follicles and germinal centres in somatic and mesenteric lymph nodes in growing C57B1/6 mice. J. Anat. 198:189-205.
26. Jeffrey, M., G. McGovern, C. M. Goodslr, K. L. Brown, and M. E. Bruce. 2000. Sites of prion protein accumulation in scrapie-infected mouse spleen revealed by immuno-electron microscopy. J. Pathol. 190:323-332.
27. 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.
28. Klein, M. A., R. Frigg, E. Flechsig, A. J. Raeber, U. Kalinke, H. Bluethmann, F. Bootz, M. Suter, R. M. Zinkernagel, and A. Aguzzi. 1997. A crucial rôle for B cells in neuroinvasive scrapie. Nature 390:687-690.
29. 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. Nature Med. 7:488-492.
30. Kosco, M. H., E. Pflugfelder, and D. Gray. 1992. Follicular dendritic cell-dependent adhesion and proliferation of B cells in vitro. J. Immunol. 148: 2331-2339.
31. Llewelyn, C. A., P. E. Hewitt, R. S. G. Knight, K. Amar, S. Cousens, J. MacKenzie, and R. G. Will. 2004. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 363:417-421.
32. Lotscher, M., M. Recher, L. Hunziker, and M. A. Klein. 2003. Immunologically induced, complement-dependent up-regulation of the prion protein in the mouse spleen: follicular dendritic cells versus capsule and trabeculae. J. Immunol. 170:6040-6047.
33. Mabbott, N. A., and M. E. Bruce. 2002. Follicular dendritic cells as targets for intervention in transmissible spongiform encephalopathies. Semin. Immunol. 14:285-293.
34. 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. Nature Med. 7:485-487.
35. Mabbott, N. A., F. Mackay, F. Minns, and M. E. Bruce. 2000. Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nature Med. 6:719-720.
36. Mabbott, N. A., G. McGovern, M. Jeffrey, and M. E. Bruce. 2002. Temporary blockade of the tumor necrosis factor receptor signaling pathway impedes the spread of scrapie to the brain. J. Virol. 76:5131-5139.
37. 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.
38. 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.
39. Manson, J. C., A. R. Clarke, P. A. McBride, I. McConnell, and J. Hope. 1994. PrP gene dosage determines the timing but not the final intensity or distribution of lesions in scrapie pathology. Neurodegeneration 3:331-340.
40. Miller, M. W., and E. S. Williams. 2003. Horizontal prion transmission in mule deer. Nature 425:35-36.
41. Miller, M. W., E. S. Williams, N. T. Hobbs, and L. L. Wolfe. 2004. Environmental sources of prion transmission in mule deer. Emerg. Infect. Dis. 10:1003-1006.
42. Montrasio, F., R. Frigg, M. Glatzel, M. 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.
43. Namikawa, R., T. Mizuno, H. Matsuoka, H. Fukami, R. Ueda, G. Itoh, M. Matsuyama, and T. Takahashi. 1986. Ontogenic development of T and B cells and non-lymphoid cells in the white pulp of human spleen. Immunology 57:61-69.
44. Nathanson, N., J. Wilesmith, G. A. Wells, and C. Griot. 1999. Bovine spongiform encephalopathy and related diseases, p. 431-463. In S. B. Prusiner (ed.), Prion biology and diseases. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
45. Onodera, T., T. Ikeda, Y. Murumatsu, and M. Shinagawa. 1993. Isolation of scrapie agent from the placenta of sheep with natural scrapie in Japan. Microbiol. Immunol. 37:311-316.
46. Outram, G. W., A. G. Dickinson, and H. Fraser. 1973. Developmental maturation of susceptibility to scrapie in mice. Nature 241:536-537.
47. Peden, A. H., M. W. Head, D. L. Ritchie, J. E. Bell, and J. W. Ironside. 2004. Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 364:527-529.
48. Race, R., A. Jenny, and D. Sutton. 1998. Scrapie infectivity and proteinase K-resistant prion protein in sheep placenta, brain, spleen, and lymph node: implications for transmission and antemortem diagnosis. J. Infect. Dis. 178: 949-953.
49. Ryder, S., G. Dexter, S. Bellworthy, and S. Tongue. 2004. Demonstration of lateral transmission of scrapie between sheep kept under natural conditions using lymphoid tissue biopsy. Res. Vet. Sci. 76:211-217.
50. CWD lymphoid cell targets in early and advanced chronic wasting disease of mule deer. J. Gen. Virol. 83:2617-2628.
51. Taylor, P. R., M. C. Pickering, M. C. Kosco-Vilbois, M. J. Walport, M. Botto, S. Gordon, and L. Martinez-Pomares. 2002. The follicular dendritic cell restricted epitope, FDC-M2, is complement C4; localization of immune complexes in mouse tissues. Eur. J. Immunol. 32:1888-1896.
52. van den Berg, T. K., K. Yoshida, and C. D. Dgkstra. 1995. Mechanism of immune complex trapping by follicular dendritic cells. Curr. Top. Microbiol. Immunol. 201:49-67.
53. 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. Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J. Clin. Microbiol. 34:1228-1231.
54. Wadsworth, J. D. F., S. Joiner, A, Hill, T. A. Campbell, P. J. Luthert, and J. Collinge. 2001. Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 358:171-180.
55. Wilesmith, J. W. 1994. An epidemiologists view of bovine spongiform encephalopathy. Phil. Trans. R. Soc. Lond. B 343:357-361.
56. Will, R. G., M. P. Alpers, D. Dormont, L. B. Schonberger, and J. Tateishi. 1999. Infectious and sporadic prion diseases, p. 465-507. In S. B. Prusiner (ed.), Prion biology and diseases. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
57. Will, R. G., J. W. Ironside, M. Zeidler, S. N. Cousens, K. Estibeiro, A. Alperovitch, S. Poser, M. Pocchiari, A. Hofman, and P. G. Smith. 1996. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347:921-925.