Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility

Journal of Virology

Volumn 77, Issue 12, 2003, Pages 6845-6854

  Mabbott, Neil A ^a   Young, Janice ^a   McConnell, Irene ^a   Bruce, Moira E ^a  

^a INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BLOCKING AGENT; HYBRID PROTEIN; LYMPHOTOXIN; LYMPHOTOXIN BETA RECEPTOR IMMUNOGLOBULIN FUSION PROTEIN; PRION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BIOACCUMULATION; CELL DIFFERENTIATION; CELL MANIPULATION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE MODEL; DISEASE PREDISPOSITION; DRUG EFFECT; FOLLICULAR DENDRITIC CELL; IMMUNOHISTOCHEMISTRY; INFECTION RISK; INOCULATION; LYMPHOID TISSUE; MESENTERY LYMPH NODE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PEYER PATCH; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SCRAPIE; SIGNAL TRANSDUCTION; SURVIVAL RATE; TECHNIQUE; VIRUS INFECTIVITY; VIRUS REPLICATION; VIRUS TRANSMISSION;

ANIMALS; CELL DIFFERENTIATION; DENDRITIC CELLS, FOLLICULAR; DISEASE SUSCEPTIBILITY; IMMUNOGLOBULIN G; IMMUNOHISTOCHEMISTRY; LYMPHOID TISSUE; LYMPHOTOXIN BETA RECEPTOR; LYMPHOTOXIN-ALPHA; LYMPHOTOXIN-BETA; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PEYER'S PATCHES; PRPSC PROTEINS; RECEPTORS, TUMOR NECROSIS FACTOR; RECOMBINANT FUSION PROTEINS; SCRAPIE; SPLEEN;

EID: 0038618854     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.12.6845-6854.2003     Document Type: Article

References (59)

1. Sc in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J. Gen. Virol. 81:3115-3126.
2. 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. Investig. 108:703-708.
3. Beekes, M., and P. A. McBride. 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.
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. 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.
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. Burton, G. F., A. Masuda, S. L. Heath, B. A. Smith, J. G. Tew, and A. K. Szakal. 1998. Follicular dendritic cells (FDC) in retroviral infection: host/pathogen perspectives. Immunol. Rev. 156:185-197.
9. 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.
10. Chaplin, D. D., and Y.-X. Fu. 1998. Cytokine regulation of secondary lymphoid organ development. Curr. Opin. Immunol. 10:289-297.
11. Dickinson, A. G., V. M. 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.
12. 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 turnout necrosis factor by B cells. J. Exp. Med. 189:159-168.
13. 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.
14. Farquhar, C. F., R. A. Somerville, and L. A. Ritchie. 1989. Post-mortem immunodiagnosis of scrapie and bovine spongiform encephalopathy. J. Virol. Methods 24:215-222.
15. Fischer, M. B., M. Ma, N. C. Hsu, and M. C. Carrol. 1998. Local synthesis of C3 within the splenic lymphoid compartment can reconstitute the impaired immune response in C3-deficient mice. J. Immunol. 160:2619-2625.
16. Force, W. R., B. N. Walter, C. Hession, R. Tizard, C. A. Kozak, J. L. Browning, and C. F. Ware. 1995. Mouse lymphotoxin-beta receptor. J. Immunol. 155:5280-5288.
17. 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.
18. Fraser, H., and A. G. Dickinson. 1973. Agent-strain differences in the distribution and intensity of grey matter vacuolation. J. Comp. Pathol. 83:29-40.
19. Fraser, H., and A. G. Dickinson. 1978. Studies on the lymphoreticular system in the pathogenesis of scrapie: the role of spleen and thymus. J. Comp. Pathol. 88:563-573.
20. Fütterer, A., K. Mink, A. Luz, M. H. Kosco-Vilbois, and K. Pfeffer. 1998. The lymphotoxin β receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity. 9:59-70.
21. 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.
22. Gommerman, J. L., F. Mackay, E. Donskoy, W. Meier, P. Martin, and J. L. Browning. 2002. Manipulation of lymphoid microenvironments in non-human primates by an inhibitor of the lymphotoxin pathway. J. Clin. Investig. 110:1359-1369.
23. Heggebo, R., C. M. Press, G. Gunnes, L. González, and M. Jeffrey. 2002. Distribution and accumulation of PrP in gut-associated and peripheral lymphoid tissue of scrapie-affected Suffolk sheep. J. Gen. Virol. 83:479-489.
24. 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.
25. Hill, A. F., M. Zeidler, J. Ironside, and J. Collinge. 1997. Diagnosis of new variant Creutzfeldt-Jakob disease by tonsil biopsy. Lancet 349:99-100.
26. Hilton, D., E. Fathers, P. Edwards, J. Ironside, and J. Zajicek. 1998. Prion immunoreactivity in appendix before clinical onset of variant Creutzfeldt-Jakob disease. Lancet 352:703-704.
27. Hilton, D. A., A. C. Ghani, L. Conyers, P. Edwards, L. McCardle, M. Penney, D. Ritchie, and J. W. Ironside. 2002. Accumulation of prion protein in tonsil and appendix: review of tissue samples. BMJ 325:633-634.
28. Jeffrey, M., G. McGovern, C. M. Goodsir, 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.
29. Kagami, Y., J. Jung, Y. S. Choi, K. Osumi, S. Nakamura, Y. Morishima, and M. Seto. 2001. Establishment of a follicular lymphoma cell line (FLK-1) dependent on follilcular dendritic cell-like cell line HK. Leukemia 15:148-156.
30. Kimberlin, R. H., and C. A. Walker. 1989. Pathogenesis of scrapie in mice after intragastric infection. Virus Res. 12:213-220.
31. 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.
32. 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.
33. Koni, P. A., R. Sacca, P. Lawton, J. L. Browning, N. H. Ruddle, and R. A. Flavell. 1997. Distinct roles in lymphoid organogenesis for lymphotoxins α and β revealed in lymphotoxin β-deficient mice. Immunity 6:491-500.
34. Kosco-Vilbois, M. H., H. Zentgraf, J. Gerdes, and J.-Y. Bonnefoy. 1997. To "B" or not to "B" a germinal center? Immunol. Today 18:225-230.
35. Lee, D. M., and M. E. Weinblatt. 2001. Rheumatoid arthritis. Lancet 358:903-912.
36. 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.
37. 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.
38. Mabbott, N. A., G. McGovern, M. Jeffrey, and M. E. Bruce. 2002. Temporary blockade of the tumour necrosis factor signaling pathway impedes the spread of scrapie to the brain. J. Virol. 76:5131-5139.
39. 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.
40. Mackay, F., and J. L. Browning. 1998. Turning off follicular dendritic cells. Nature 395:26-27.
41. Maignien, T., C. I. Lasmezas, V. Beringue, D. Dormont, and J. P. Deslys. 1999. Pathogenesis of the oral route of infection of mice with scrapie and bovine spongiform encephalopathy agents. J. Gen. Virol. 80:3035-3042.
42. Manuelidis, L., I. Zaitsev, P. Koni, Z. Y. Lu, R. A. Flavell, and W. Fritch. 2000. Follicular dendritic cells and dissemination of Creutzfeldt-Jakob disease. J. Virol. 74:8614-8622.
43. Matsumoto, M., S. F. Lo, C. J. L. Carruthers, J. Min, S. Mariathasan, G. Huang, D. R. Plas, S. M. Martin, R. S. Geha, M. H. Nahm, and D. D. Chaplin. 1996. Affinity maturation without germinal centres in lymphotoxin-α-deficient mice. Nature 382:462-466.
44. 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.
45. McBride, P. A., W. J. Schulz-Shaeffer, M. Donaldson, M. Bruce, H. Diringer, H. A. Kretzschmar, and M. Beekes. 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.
46. 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.
47. Nielsen, C. H., E. M. Fischer, and R. G. Q. Leslie. 2000. The role of complement in the acquired immune response. Immunology 100:4-12.
48. 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.
49. Pardridge, W. M. 2002. Drug and gene targeting to the brain with molecular trojan horses. Nat. Rev. Drug Discov. 1:131-139.
50. Pepys, M. B. 1976. Role of complement in the induction of immunological responses. Transplant. Rev. 32:93-120.
51. 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.
52. Schwaeble, W., M. K.-H. Schäfer, F. Petry, T. Fink, D. Knebel, E. Weihe, and M. Loos. 1995. Follicular dendritic cells, interdigitating cells, and cells of the monocyte-macrophage lineage are the C1q-producing sources in the spleen. J. Immunol. 155:4971-4978.
53. Shmakov, A. N., N. F. McLennan, P. McBride, C. F. Farquhar, J. Bode, K. A. Rennison, and S. Ghosh. 2000. Cellular prion protein is expressed in the human enteric nervous system. Nat. Med. 6:840-841.
54. Sigurdson, C. J., C. Barillas-Mury, M. W. Miller; B. Oesch, L. J. M. van Keulen, J. P. M. Langeveld, and E. A. Hoover. 2002. PrPCWD lymphoid cell targets in early and advanced chronic wasting disease of mule deer. J. Gen. Virol. 83:2617-2628.
55. Taylor, P. R., M. C. Pickering, M. H. 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. 32:1883-1896.
56. 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.
57. van Keulen, L. J. M., B. E. G. Schreuder, M. E. W. Vromans, J. P. M. Langeveld, and M. A. Smits. 1999. Scrapie-associated prion protein in the gastro-intestinal tract of sheep with scrapie. J. Comp. Pathol. 121:55-63.
58. Wu, Q., Y. Wang, E. O. Hedgeman, J. L. Browning, and Y.-X. Fu. 1999. The requirement of membrane lymphotoxin for the presence of dendritic cells in lymphoid tissues. J. Exp. Med. 190:629-638.
59. 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.