Altered lymphocyte homeostasis after oral prion infection in mouse

Veterinary Immunology and Immunopathology

Volumn 122, Issue 3-4, 2008, Pages 204-215

  Segundo, F Díaz San ^a   Sevilla, N ^a   Gutierrez J P ^b   Brun, A ^a  

^a Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria Consejo Superior de Investigaciones Científicas   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Lymphocyte homeostasis; Prion infection; T cell ratio

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CYTOKINE; LYMPHOTOXIN BETA; MESSENGER RNA; PRION PROTEIN;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; BLOOD; BRAIN; CD4 CD8 RATIO; CELL COUNT; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; DENDRITIC CELL; DISEASE COURSE; FLOW CYTOMETRY; HOMEOSTASIS; IMMUNOHISTOCHEMISTRY; INFECTION; INOCULATION; LEUKOCYTE; LYMPHOCYTE; LYMPHOID CELL; LYMPHOID ORGAN; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PEYER PATCH; PRION; PRION DISEASE; SPLEEN; STATISTICAL SIGNIFICANCE; T LYMPHOCYTE; THYMUS; TRANSGENIC MOUSE;

ANIMALS; DENDRITIC CELLS; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; HOMEOSTASIS; LYMPHOCYTES; LYMPHOID TISSUE; LYMPHOTOXIN-BETA; MICE; MICE, TRANSGENIC; PRION DISEASES; PRPC PROTEINS; TRANSFORMING GROWTH FACTOR BETA;

ANIMALIA; MUS; MUS MUSCULUS;

EID: 40849087986     PISSN: 01652427     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vetimm.2007.11.013     Document Type: Article

References (45)

1. Aguzzi A. Prions and the immune system: a journey through gut, spleen, and nerves. Adv. Immunol. 81 (2003) 123-171
2. Aguzzi A., and Heikenwalder M. Prions, cytokines, and chemokines: a meeting in lymphoid organs. Immunity 22 (2005) 145-154
3. Aguzzi A., and Heikenwalder M. Pathogenesis of prion diseases: current status and future outlook. Nat. Rev. Microbiol. 4 (2006) 765-775
4. Aguzzi A., Heppner F.L., Heikenwalder M., Prinz M., Mertz K., Seeger H., and Glatzel M. Immune system and peripheral nerves in propagation of prions to CNS. Br. Med. Bull. 66 (2003) 141-159
5. Ansel K.M., Ngo V.N., Hyman P.L., Luther S.A., Forster R., Sedgwick J.D., Browning J.L., Lipp M., and Cyster J.G. A chemokine-driven positive feedback loop organizes lymphoid follicles. Nature 406 (2000) 309-314
6. Aucouturier P., and Carnaud C. The immune system and prion diseases: a relationship of complicity and blindness. J. Leukoc. Biol. 72 (2002) 1075-1083
7. Ballerini C., Gourdain P., Bachy V., Blanchard N., Levavasseur E., Gregoire S., Fontes P., Aucouturier P., Hivroz C., and Carnaud C. Functional implication of cellular prion protein in antigen-driven interactions between T cells and dendritic cells. J. Immunol. 176 (2006) 7254-7262
8. Brun A., Castilla J., Ramirez M.A., Prager K., Parra B., Salguero F.J., Shiveral D., Sanchez C., Sanchez-Vizcaino J.M., Douglas A., and Torres J.M. Proteinase K enhanced immunoreactivity of the prion protein-specific monoclonal antibody 2A11. Neurosci. Res. 48 (2004) 75-83
9. Castilla J., Gutierrez Adan A., Brun A., Pintado B., Ramirez M.A., Parra B., Doyle D., Rogers M., Salguero F.J., Sanchez C., Sanchez-Vizcaino J.M., and Torres J.M. Early detection of PrP(res) in BSE-infected bovine PrP transgenic mice. Arch. Virol. 148 (2003) 677-691
10. Castilla J., Gutierrez-Adan A., Brun A., Doyle D., Pintado B., Ramirez M.A., Salguero F.J., Parra B., Segundo F.D., Sanchez-Vizcaino J.M., Rogers M., and Torres J.M. Subclinical bovine spongiform encephalopathy infection in transgenic mice expressing porcine prion protein. J. Neurosci. 24 (2004) 5063-5069
11. Chaplin D.D., and Fu Y. Cytokine regulation of secondary lymphoid organ development. Curr. Opin. Immunol. 10 (1998) 289-297
12. Defaweux V., Dorban G., Demonceau C., Piret J., Jolois O., Thellin O., Thielen C., Heinen E., and Antoine N. Interfaces between dendritic cells, other immune cells, and nerve fibres in mouse Peyer's patches: potential sites for neuroinvasion in prion diseases. Microsci. Res. Tech. 66 (2005) 1-9
13. Foster J.D., Parnham D.W., Hunter N., and Bruce M. Distribution of the prion protein in sheep terminally affected with BSE following experimental oral transmission. J. Gen. Virol. 82 (2001) 2319-2326
14. Fraser H., and Dickinson A.G. Studies of the lymphoreticular system in the pathogenesis of scrapie: the role of spleen and thymus. J. Comp. Pathol. 88 (1978) 563-573
15. Fu Y.X., Huang G., Wang Y., and Chaplin D.D. B lymphocytes induce the formation of follicular dendritic cell clusters in a lymphotoxin alpha-dependent fashion. J. Exp. Med. 187 (1998) 1009-1018
16. Glatzel M., Abela E., Maissen M., and Aguzzi A. Extraneural pathologic prion protein in sporadic Creutzfeldt-Jakob disease. N. Engl. J. Med. 349 (2003) 1812-1820
17. Heggebo R., Press C.M., Gunnes G., Lie K.I., Tranulis M.A., Ulvund M., Groschup M.H., and Landsverk T. Distribution of prion protein in the ileal Peyer's patch of scrapie-free lambs and lambs naturally and experimentally exposed to the scrapie agent. J. Gen. Virol. 81 (2000) 2327-2337
18. Heppner F.L., Christ A.D., Klein M.A., Prinz M., Fried M., Kraehenbuhl J.P., and Aguzzi A. Transepithelial prion transport by M cells. Nat. Med. 7 (2001) 976-977
19. Huang F.P., Farquhar C.F., Mabbott N.A., Bruce M.E., and MacPherson G.G. Migrating intestinal dendritic cells transport PrP(Sc) from the gut. J. Gen. Virol. 83 (2002) 267-271
20. Kadowaki N., Antonenko S., Lau J.Y., and Liu Y.J. Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J. Exp. Med. 192 (2000) 219-226
21. Klein M.A., Frigg R., Flechsig E., Raeber A.J., Kalinke U., Bluethmann H., Bootz F., Suter M., Zinkernagel R.M., and Aguzzi A. A crucial role for B cells in neuroinvasive scrapie. Nature 390 (1997) 687-690
22. Klein M.A., Frigg R., Raeber A.J., Flechsig E., Hegyi I., Zinkernagel R.M., Weissmann C., and Aguzzi A. PrP expression in B lymphocytes is not required for prion neuroinvasion. Nat. Med. 4 (1998) 1429-1433
23. Klein M.A., Kaeser P.S., Schwarz P., Weyd H., Xenarios I., Zinkernagel R.M., Carroll M.C., Verbeek J.S., Botto M., Walport M.J., Molina H., Kalinke U., Acha-Orbea H., and Aguzzi A. Complement facilitates early prion pathogenesis. Nat. Med. 7 (2001) 488-492
24. Lewicki H., Tishon A., Homann D., Mazarguil H., Laval F., Asensio V.C., Campbell I.L., DeArmond S., Coon B., Teng C., Gairin J.E., and Oldstone M.B. T cells infiltrate the brain in murine and human transmissible spongiform encephalopathies. J. Virol. 77 (2003) 3799-3808
25. Mabbott N.A., and Bruce M.E. The immunobiology of TSE diseases. J. Gen. Virol. 82 (2001) 2307-2318
26. Mabbott N.A., and Bruce M.E. Prion disease: bridging the spleen-nerve gap. Nat. Med. 9 (2003) 1463-1464
27. Mabbott N.A., Mackay F., Minns F., and Bruce M.E. Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nat. Med. 6 (2000) 719-720
28. Maignien T., Lasmezas C.I., Beringue V., Dormont D., and Deslys J.P. Pathogenesis of the oral route of infection of mice with scrapie and bovine spongiform encephalopathy agents. J. Gen. Virol. 80 Pt 11 (1999) 3035-3042
29. Mattei V., Garofalo T., Misasi R., Circella A., Manganelli V., Lucania G., Pavan A., and Sorice M. Prion protein is a component of the multimolecular signaling complex involved in T cell activation. FEBS Lett. 560 (2004) 14-18
30. Mayordomo J.I., Zorina T., Storkus W.J., Zitvogel L., Garcia-Prats M.D., DeLeo A.B., and Lotze M.T. Bone marrow-derived dendritic cells serve as potent adjuvants for peptide-based antitumor vaccines. Stem Cells 15 (1997) 94-103
31. McBride P.A., Schulz-Schaeffer W.J., Donaldson M., Bruce M., Diringer H., Kretzschmar H.A., and Beekes M. 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 (2001) 9320-9327
32. McFarlin D.E., Raff M.C., Simpson E., and Nehlsen S.H. Scrapie in immunologically deficient mice. Nature 233 (1971) 336
33. Montrasio F., Cozzio A., Flechsig E., Rossi D., Klein M.A., Rulicke T., Raeber A.J., Vosshenrich C.A., Proft J., Aguzzi A., and Weissmann C. B lymphocyte-restricted expression of prion protein does not enable prion replication in prion protein knockout mice. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 4034-4037
34. Neutra M.R., Frey A., and Kraehenbuhl J.P. Epithelial M cells: gateways for mucosal infection and immunization. Cell 86 (1996) 345-348
35. Neutra M.R., Pringault E., and Kraehenbuhl J.P. Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu. Rev. Immunol. 14 (1996) 275-300
36. O'Keeffe M., Hochrein H., Vremec D., Caminschi I., Miller J.L., Anders E.M., Wu L., Lahoud M.H., Henri S., Scott B., Hertzog P., Tatarczuch L., and Shortman K. Mouse plasmacytoid cells: long-lived cells, heterogeneous in surface phenotype and function, that differentiate into CD8(+) dendritic cells only after microbial stimulus. J. Exp. Med. 196 (2002) 1307-1319
37. Perry V.H., Cunningham C., and Boche D. Atypical inflammation in the central nervous system in prion disease. Curr. Opin. Neurol. 15 (2002) 349-354
38. Prinz M., Huber G., Macpherson A.J., Heppner F.L., Glatzel M., Eugster H.P., Wagner N., and Aguzzi A. Oral prion infection requires normal numbers of Peyer's patches but not of enteric lymphocytes. Am. J. Pathol. 162 (2003) 1103-1111
39. Race R., Oldstone M., and Chesebro B. Entry versus blockade of brain infection following oral or intraperitoneal scrapie administration: role of prion protein expression in peripheral nerves and spleen. J. Virol. 74 (2000) 828-833
40. Schlecht G., Garcia S., Escriou N., Freitas A.A., Leclerc C., and Dadaglio G. Murine plasmacytoid dendritic cells induce effector/memory CD8+ T-cell responses in vivo after viral stimulation. Blood 104 (2004) 1808-1815
41. Sevilla N., Kunz S., Holz A., Lewicki H., Homann D., Yamada H., Campbell K.P., de La Torre J.C., and Oldstone M.B.. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J. Exp. Med. 192 (2000) 1249-1260
42. Steinman R.M., Pack M., and Inaba K. Dendritic cells in the T-cell areas of lymphoid organs. Immunol. Rev. 156 (1997) 25-37
43. Terry L.A., Marsh S., Ryder S.J., Hawkins S.A., Wells G.A., and Spencer Y.I. Detection of disease-specific PrP in the distal ileum of cattle exposed orally to the agent of bovine spongiform encephalopathy. Vet. Rec. 152 (2003) 387-392
44. Thackray A.M., Klein M.A., and Bujdoso R. Subclinical prion disease induced by oral inoculation. J. Virol. 77 (2003) 7991-7998
45. Wadsworth J.D., Joiner S., Hill A.F., Campbell T.A., Desbruslais M., Luthert P.J., and Collinge J. Tissue distribution of protease resistant prion protein in variant Creutzfeldt-Jakob disease using a highly sensitive immunoblotting assay. Lancet 358 (2001) 171-180