Lymphotoxin-Dependent Prion Replication in Inflammatory Stromal Cells of Granulomas

Immunity

Volumn 29, Issue 6, 2008, Pages 998-1008

  Heikenwalder, Mathias ^a   Kurrer, Michael O ^b   Margalith, Ilan ^a   Kranich, Jan ^a   Zeller, Nicolas ^a   Haybaeck, Johannes ^a   Polymenidou, Magdalini ^a   Matter, Matthias ^a   Bremer, Juliane ^a   Jackson, Walker S ^c   Lindquist, Susan ^c,d   Sigurdson, Christina J ^a   Aguzzi, Adriano ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b Kantonsspital Aarau ^*  (Switzerland)

^c WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

MOLIMMUNO

Indexed keywords

CD45 ANTIGEN; LYMPHOTOXIN; LYMPHOTOXIN BETA RECEPTOR; PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL POPULATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; FIBROBLAST; FOLLICULAR DENDRITIC CELL; GRANULOMA; IMMUNOCOMPETENT CELL; INFLAMMATION; LYMPHOCYTE; LYMPHOID TISSUE; MACROPHAGE; MESENCHYME CELL; MOUSE; NONHUMAN; PRION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; SKIN; STROMA CELL; SUBCUTANEOUS TISSUE; VIRUS INFECTIVITY; VIRUS LOAD; VIRUS REPLICATION;

ANIMALS; DENDRITIC CELLS, FOLLICULAR; GRANULOMA; LYMPHOTOXIN BETA RECEPTOR; LYMPHOTOXIN-ALPHA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PRIONS; STROMAL CELLS;

EID: 57449112742     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2008.10.014     Document Type: Article

References (59)

1. Aguzzi A., and Heikenwalder M. Pathogenesis of prion diseases: Current status and future outlook. Nat. Rev. Microbiol. 4 (2006) 765-775
2. Aguzzi A., and Polymenidou M. Mammalian prion biology. One century of evolving concepts. Cell 116 (2004) 313-327
3. Aguzzi A., and Weissmann C. Prion research: The next frontiers. Nature 389 (1997) 795-798
4. Andreoletti O., Simon S., Lacroux C., Morel N., Tabouret G., Chabert A., Lugan S., Corbiere F., Ferre P., Foucras G., et al. PrPSc accumulation in myocytes from sheep incubating natural scrapie. Nat. Med. 10 (2004) 591-593
5. Blättler T., Brandner S., Raeber A.J., Klein M.A., Voigtländer T., Weissmann C., and Aguzzi A. PrP-expressing tissue required for transfer of scrapie infectivity from spleen to brain. Nature 389 (1997) 69-73
6. Brandner S., Isenmann S., Raeber A., Fischer M., Sailer A., Kobayashi Y., Marino S., Weissmann C., and Aguzzi A. Normal host prion protein necessary for scrapie-induced neurotoxicity. Nature 379 (1996) 339-343
7. Britton W.J., and Lockwood D.N. Leprosy. Lancet 363 (2004) 1209-1219
8. Büeler H., Aguzzi A., Sailer A., Greiner R.A., Autenried P., Aguet M., and Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell 73 (1993) 1339-1347
9. Büeler H., Fischer M., Lang Y., Bluethmann H., Lipp H.P., DeArmond S.J., Prusiner S.B., Aguet M., and Weissmann C. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 356 (1992) 577-582
10. De Togni P., Goellner J., Ruddle N.H., Streeter P.R., Fick A., Mariathasan S., Smith S.C., Carlson R., Shornick L.P., Strauss-Schoenberger J., et al. Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264 (1994) 703-707
11. Dlakic W.M., Grigg E., and Bessen R.A. Prion infection of muscle cells in vitro. J. Virol. 81 (2007) 4615-4624
12. Drayton D.L., Liao S., Mounzer R.H., and Ruddle N.H. Lymphoid organ development: From ontogeny to neogenesis. Nat. Immunol. 7 (2006) 344-353
13. Ernst J.D., Trevejo-Nunez G., and Banaiee N. Genomics and the evolution, pathogenesis, and diagnosis of tuberculosis. J. Clin. Invest. 117 (2007) 1738-1745
14. Falsig J., Julius C., Margalith I., Schwarz P., Heppner F.L., and Aguzzi A. A versatile prion replication assay in organotypic brain slices. Nat. Neurosci. 11 (2008) 109-117
15. Fischer M., Rülicke T., Raeber A., Sailer A., Moser M., Oesch B., Brandner S., Aguzzi A., and Weissmann C. Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J. 15 (1996) 1255-1264
16. Fraser H., and Dickinson A.G. Pathogenesis of scrapie in the mouse: The role of the spleen. Nature 226 (1970) 462-463
17. Futterer A., Mink K., Luz A., Kosco-Vilbois M.H., and Pfeffer K. The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 9 (1998) 59-70
18. 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
19. Hamir A.N., Kunkle R.A., Miller J.M., and Hall S.M. Abnormal prion protein in Ectopic lymphoid tissue in a kidney of an asymptomatic white-tailed deer experimentally inoculated with the agent of chronic wasting disease. Vet. Pathol. 43 (2006) 367-369
20. Hanayama R., Tanaka M., Miyasaka K., Aozasa K., Koike M., Uchiyama Y., and Nagata S. Autoimmune disease and impaired uptake of apoptotic cells in MFG-E8-deficient mice. Science 304 (2004) 1147-1150
21. Heikenwalder M., Zeller N., Seeger H., Prinz M., Klohn P.C., Schwarz P., Ruddle N.H., Weissmann C., and Aguzzi A. Chronic lymphocytic inflammation specifies the organ tropism of prions. Science 307 (2005) 1107-1110
22. Iannuzzi M.C., Rybicki B.A., and Teirstein A.S. Sarcoidosis. N. Engl. J. Med. 357 (2007) 2153-2165
23. Kaeser P.S., Klein M.A., Schwarz P., and Aguzzi A. Efficient lymphoreticular prion propagation requires prp(c) in stromal and hematopoietic cells. J. Virol. 75 (2001) 7097-7106
24. 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
25. 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
26. Klohn P.C., Stoltze L., Flechsig E., Enari M., and Weissmann C. A quantitative, highly sensitive cell-based infectivity assay for mouse scrapie prions. Proc. Natl. Acad. Sci. USA 100 (2003) 11666-11671
27. Kovacs G.G., Lindeck-Pozza E., Chimelli L., Araujo A.Q., Gabbai A.A., Strobel T., Glatzel M., Aguzzi A., and Budka H. Creutzfeldt-Jakob disease and inclusion body myositis. Ann. Neurol. 55 (2004) 121-125
28. Kranich J., Krautler N.J., Heinen E., Polymenidou M., Bridel C., Schildknecht A., Huber C., Kosco-Vilbois M.H., Zinkernagel R., Miele G., and Aguzzi A. Follicular dendritic cells control engulfment of apoptotic bodies by secreting Mfge8. J. Exp. Med. 205 (2008) 1293-1302
29. Kumar V., Abbas A.K., Fausto N., Robbins S.L., and Cotran R.S. Robbins and Cotran Pathologic Basis of Disease (2004), Elsevier Science, Amsterdam
30. Legname G., Baskakov I.V., Nguyen H.O., Riesner D., Cohen F.E., DeArmond S.J., and Prusiner S.B. Synthetic mammalian prions. Science 305 (2004) 673-676
31. Ligios C., Sigurdson C.J., Santucciu C., Carcassola G., Manco G., Basagni M., Maestrale C., Cancedda M.G., Madau L., and Aguzzi A. PrP(Sc) in mammary glands of sheep affected by scrapie and mastitis. Nat. Med. 11 (2005) 1137-1138
32. Link A., Vogt T.K., Favre S., Britschgi M.R., Acha-Orbea H., Hinz B., Cyster J.G., and Luther S.A. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat. Immunol. 8 (2007) 1255-1265
33. 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
34. Mabbott N.A., McGovern G., Jeffrey M., and Bruce M.E. Temporary blockade of the tumor necrosis factor receptor signaling pathway impedes the spread of scrapie to the brain. J. Virol. 76 (2002) 5131-5139
35. Mabbott N.A., Young J., McConnell I., and Bruce M.E. Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility. J. Virol. 77 (2003) 6845-6854
36. Mackay F., and Browning J.L. Turning off follicular dendritic cells. Nature 395 (1998) 26-27
37. Mackay F., Majeau G.R., Lawton P., Hochman P.S., and Browning J.L. Lymphotoxin but not tumor necrosis factor functions to maintain splenic architecture and humoral responsiveness in adult mice. Eur. J. Immunol. 27 (1997) 2033-2042
38. Mahal S.P., Baker C.A., Demczyk C.A., Smith E.W., Julius C., and Weissmann C. Prion strain discrimination in cell culture: The cell panel assay. Proc. Natl. Acad. Sci. USA 104 (2007) 20908-20913
39. Mathiason C.K., Powers J.G., Dahmes S.J., Osborn D.A., Miller K.V., Warren R.J., Mason G.L., Hays S.A., Hayes-Klug J., Seelig D.M., et al. Infectious prions in the saliva and blood of deer with chronic wasting disease. Science 314 (2006) 133-136
40. 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. USA 98 (2001) 4034-4037
41. Montrasio F., Frigg R., Glatzel M., Klein M.A., Mackay F., Aguzzi A., and Weissmann C. Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 288 (2000) 1257-1259
42. Moore R.C., Redhead N.J., Selfridge J., Hope J., Manson J.C., and Melton D.W. Double replacement gene targeting for the production of a series of mouse strains with different prion protein gene alterations. Biotechnology (N. Y.) 13 (1995) 999-1004
43. Okabe M., Ikawa M., Kominami K., Nakanishi T., and Nishimune Y. Green mice as a source of ubiquitous green cells. FEBS Lett. 407 (1997) 313-319
44. Oldstone M.B., Race R., Thomas D., Lewicki H., Homann D., Smelt S., Holz A., Koni P., Lo D., Chesebro B., and Flavell R. Lymphotoxin-alpha- and lymphotoxin-beta-deficient mice differ in susceptibility to scrapie: Evidence against dendritic cell involvement in neuroinvasion. J. Virol. 76 (2002) 4357-4363
45. Ordway D., Henao-Tamayo M., Orme I.M., and Gonzalez-Juarrero M. Foamy macrophages within lung granulomas of mice infected with Mycobacterium tuberculosis express molecules characteristic of dendritic cells and antiapoptotic markers of the TNF receptor-associated factor family. J. Immunol. 175 (2005) 3873-3881
46. Polymenidou M., Stoeck K., Glatzel M., Vey M., Bellon A., and Aguzzi A. Coexistence of multiple PrPSc types in individuals with Creutzfeldt-Jakob disease. Lancet Neurol. 4 (2005) 805-814
47. Priller J., Prinz M., Heikenwalder M., Zeller N., Schwarz P., and Aguzzi A. Early and rapid engraftment of bone marrow-derived microglia in scrapie. J. Neurosci. 26 (2006) 11753-11762
48. Prinz M., Heikenwalder M., Junt T., Schwarz P., Glatzel M., Heppner F.L., Fu Y.X., Lipp M., and Aguzzi A. Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature 425 (2003) 957-962
49. Prinz M., Montrasio F., Klein M.A., Schwarz P., Priller J., Odermatt B., Pfeffer K., and Aguzzi A. Lymph nodal prion replication and neuroinvasion in mice devoid of follicular dendritic cells. Proc. Natl. Acad. Sci. USA 99 (2002) 919-924
50. Prusiner S.B., Cochran S.P., Groth D.F., Downey D.E., Bowman K.A., and Martinez H.M. Measurement of the scrapie agent using an incubation time interval assay. Ann. Neurol. 11 (1982) 353-358
51. Russell D.G. Who puts the tubercle in tuberculosis?. Nat. Rev. Microbiol. 5 (2007) 39-47
52. Scandella E., Bolinger B., Lattmann E., Miller S., Favre S., Littman D.R., Finke D., Luther S.A., Junt T., and Ludewig B. Restoration of lymphoid organ integrity through the interaction of lymphoid tissue-inducer cells with stroma of the T cell zone. Nat. Immunol. 9 (2008) 667-675
53. Seeger H., Heikenwalder M., Zeller N., Kranich J., Schwarz P., Gaspert A., Seifert B., Miele G., and Aguzzi A. Coincident scrapie infection and nephritis lead to urinary prion excretion. Science 310 (2005) 324-326
54. Selfridge J., Pow A.M., McWhir J., Magin T.M., and Melton D.W. Gene targeting using a mouse HPRT minigene/HPRT-deficient embryonic stem cell system: Inactivation of the mouse ERCC-1 gene. Somat. Cell Mol. Genet. 18 (1992) 325-336
55. Taraboulos A., Jendroska K., Serban D., Yang S.L., DeArmond S.J., and Prusiner S.B. Regional mapping of prion proteins in brain. Proc. Natl. Acad. Sci. USA 89 (1992) 7620-7624
56. Thomzig A., Schulz-Schaeffer W., Wrede A., Wemheuer W., Brenig B., Kratzel C., Lemmer K., and Beekes M. Accumulation of pathological prion protein PrPSc in the skin of animals with experimental and natural scrapie. PLoS Pathog. 3 (2007) e66
57. Vascellari M., Nonno R., Mutinelli F., Bigolaro M., Di Bari M.A., Melchiotti E., Marcon S., D'Agostino C., Vaccari G., Conte M., et al. PrPSc in Salivary Glands of Scrapie-Affected Sheep. J. Virol. 81 (2007) 4872-4876
58. Vorberg I., Buschmann A., Harmeyer S., Saalmüller A., Pfaff E., and Groschup M.H. A novel epitope for the specific detection of exogenous prion proteins in transgenic mice and transfected murine cell lines. Virology 255 (1999) 26-31
59. Vorberg I., Raines A., Story B., and Priola S.A. Susceptibility of common fibroblast cell lines to transmissible spongiform encephalopathy agents. J. Infect. Dis. 189 (2004) 431-439