M cell-depletion blocks oral prion disease pathogenesis

Mucosal Immunology

Volumn 5, Issue 2, 2012, Pages 216-225

  Donaldson, D S ^a   Kobayashi, A ^a,b   Ohno, H ^c   Yagita, H ^d   Williams, I R ^e   Mabbott, N A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c RIKEN Center for Integrative Medical Sciences   (Japan)

^d JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EPITHELIUM CELL; FOLLICULAR DENDRITIC CELL; FOOD CONTAMINATION; INTESTINE EPITHELIUM; INTESTINE MUCOSA PERMEABILITY; MICROFOLD CELL; MOUSE; NONHUMAN; PATHOGENESIS; PEYER PATCH; PRION; PRION DISEASE; PRIORITY JOURNAL; TRANSCYTOSIS; VIRUS INHIBITION; VIRUS REPLICATION;

EID: 84857212312     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2011.68     Document Type: Article

References (50)

1. Mabbott, N. A ., Young, J ., McConnell, I. & Bruce, M. E. Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility. J. Virol. 77, 6845-6854 (2003). (Pubitemid 36666878)
2. Prinz, M. et al. Oral prion infection requires normal numbers of Peyer's patches but not of enteric lymphocytes. Am. J. Pathol. 162, 1103-1111 (2003). (Pubitemid 36350656)
3. Glaysher, B. R. & Mabbott, N. A. Role of the GALT in scrapie agent neuroinvasion from the intestine. J. Immunol. 178, 3757-3766 (2007). (Pubitemid 46417644)
4. Andreoletti, O. et al. Early accumulation of PrP Sc in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J. Gen. Virol. 81, 3115-3126 (2000). (Pubitemid 32000659)
5. Sigurdson, C. J. et al. Oral transmission and early lymphoid tropism of chronic wasting disease PrP res in mule deer fawns (Odocoileus hemionus ). J. Gen. Virol. 80, 2757-2764 (1999). (Pubitemid 29458640)
6. Mabbott, N. A. et al. Expression of mesenchyme-specific gene signatures by follicular dendritic cells: insights from the meta-analysis of microarray data from multiple mouse cell populations. Immunology 133, 482-498 (2011).
7. McCulloch, L. et al. Follicular dendritic cell-specific prion protein (PrP C ) expression alone is sufficient to sustain prion infection in the spleen. PloS Pathogens 7, e1002402 (2011).
8. Bolton, D. C ., McKinley, M. P. & Prusiner, S. B. Identification of a protein that purifies with the scrapie prion. Science 218, 1309-1311 (1982).
9. Legname, G. et al. Synthetic mammalian prions. Science 305, 673-676 (2004). (Pubitemid 39006757)
10. Brown, K. L. et al. Scrapie replication in lymphoid tissues depends on PrP-expressing follicular dendritic cells. Nat. Med. 5, 1308-1312 (1999). (Pubitemid 29535610)
11. Klein, M. A. et al. PrP expression in B lymphocytes is not required for prion neuroinvasion. Nat. Med. 4, 1429-1433 (1998). (Pubitemid 28553468)
12. Glatzel, M ., Heppner, F. L ., Albers, K. M. & Aguzzi, A. Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 31, 25-34 (2001). (Pubitemid 32757086)
13. Knoop, K. A. et al. RANKL is necessary and sufficient to initiate development of antigen-sampling M cells in the intestinal epithelium. J. Immunol. 183, 5738-5747 (2009).
14. Nakato, G. et al. New approach for M-cell-specific molecules by screening comprehensive transcriptome analysis. DNA Res. 16, 227-235 (2009).
15. Neutra, M. R ., Frey, A. & Kraehenbuhl, J .- P. Epithelial M cells: gateways for mucosal infection and immunization. Cell 86, 345-348 (1996). (Pubitemid 26272074)
16. Takakura, I. et al. Orally administered prion protein is incorporated by M cells and spreads to lymphoid tissues with macrophages in prion protein knockout mice. Am. J. Pathol. 179, 1301-1309 (2011).
17. Foster, N. & Macpherson, G. G. Murine cecal patch M cells transport infectious prions in vivo. J. Infect. Dis. 202, 1916-1919 (2010).
18. Heppner, F. L. et al. Transepithelial prion transport by M cells. Nat. Med. 7, 976-977 (2001).
19. Jeffrey, M. et al. Transportation of prion protein across the intestinal mucosa of scrapie-susceptible and scrapie-resistant sheep. J. Pathol. 209, 4-14 (2006).
20. Mishra, R. S. et al. Protease-resistant human prion protein and ferritin are cotransported across Caco-2 epithelial cells: implications for species barrier in prion uptake from the intestine. J. Neurosci. 24, 11280-11290 (2004). (Pubitemid 39658263)
21. Rescigno, M. et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367 (2001). (Pubitemid 33706348)
22. Chieppa, M ., Rescigno, M ., Huang, A. Y. C. & Germain, R. N. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J. Exp. Med. 203, 2841-2852 (2006). (Pubitemid 46026162)
23. Raymond, C. R ., Aucouturier, P. & Mabbott, N. A. In vivo depletion of CD11c + cells impairs scrapie agent neuroinvasion from the intestine. J. Immunol. 179, 7758-7766 (2007).
24. Terahara, K. et al. Comprehensive gene expression profiling of Peyer's patch M cells, villous M-like cells, and intestinal epithelial cells. J. Immunol. 180, 7840-7846 (2008).
25. Hase, K. et al. Uptake through glycoprotein 2 of FimH + bacteria by M cells initiates mucosal immune responses. Nature 462, 226-231 (2009).
26. Zabel, M. D. et al. Stromal complement receptor CD21/35 facilitates lymphoid prion colonization and pathogenesis. J. Immunol. 179, 6144-6152 (2007).
27. Kong, Y. Y. et al. OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph node organogenesis. Nature 397, 315-323 (1999).
28. Knoop, K. A ., Butler, B. R ., Kumar, N ., Newberry, R. D. & Williams, I. R. Distinct developmental requirements for isolated lymphoid follicle formation in the small and large intestine. Am. J. Pathol. 179, 1861-1871 (2011).
29. Schulz-Schaeffer, W. J. et al. The paraffin-embedded tissue blot detects PrP sc early in the incubation time in prion diseases. Am. J. Pathol. 156, 51-56 (2000). (Pubitemid 30644438)
30. Watarai, M. et al. Cellular prion protein promotes Brucella infection into macrophages. J. Exp. Med. 198, 5-17 (2003). (Pubitemid 36870181)
31. Gousset, K. et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat. Cell. Biol. 11, 328 (2009).
32. Hase, K. et al. M-Sec promotes membrane nanotube formation by interacting with Ral and the exocyst complex. Nat. Cell. Biol. 11, 1427-1432 (2009).
33. Wang, J ., Gusti, V ., Saraswati, A. & Lo, D. D. Convergent and divergent development among M cell lineages in mouse mucosal epithelium. J. Immunol 187, 5277-5285 (2011).
34. Kim, D. et al. Regulation of peripheral lymph node genesis by the tumour necrosis factor family member TRANCE. J. Exp. Med. 192, 1467-1478 (2000).
35. Ebisawa, M. et al. CCR6 hi CD11c int B cells promote M-cell differentiation in Peyer's patch. Int. Immunol. 23, 261-269 (2011).
36. Wong, B. R. et al. TRANCE (tumour necrosis factor [TNF]-related activation-induced cytokine), a new TNF family member predominantly expressed in T cells, is a dendritic cell-specific survival factor. J. Exp. Med. 186, 2075-2080 (1997). (Pubitemid 28013694)
37. Chino, T ., Draves, K. E. & Clark, E. A. Regulation of dendritic cell survival and cytokine production by osteoprotegerin. J. Leukoc. Biol. 86, 933-940 (2009).
38. Mabbott, N. A ., Baillie, J. C ., Hume, D. A. & Freeman, T. C. Meta-analysis of co-expressed gene signatures in mouse leukocyte populations. Immunobiology 215, 724-736 (2010).
39. Williamson, E ., Bilsborough, J. M. & Viney, J. L. Regulation of mucosal dendritic cell function by receptor activator of NF-kB (RANK)/RANKL interactions: impact on tolerance induction. J. Immunol. 169, 3606-3612 (2002).
40. Seeger, H. et al. Coincident scrapie infection and nephritis lead to urinary prion excretion. Science 310, 324-326 (2005). (Pubitemid 41457200)
41. Heikenwalder, M. et al. Lymphotoxin-dependent prion replication in inflammatory stromal cells of granulomas. Immunity 29, 998-1008 (2008).
42. Sigurdson, C. J. et al. Bacterial colitis increases susceptibility to oral prion pathogenesis. J. Infect. Dis. 199, 243-252 (2009).
43. Borghesi, C. & Nicoletti, C. Rapid appearance of M cells after microbial challenge is restricted at the periphery of the follicle-associated epithelium of Peyer's patch. Lab. Invest. 79, 1393-1401 (1999).
44. Meynell, H. M. et al. Up-regulation of microsphere transport across the follicle-associated epithelium of Peyer's patch by exposure to Streptococcus pneumoniae R36a. FASEB J. 13, 611-619 (1999). (Pubitemid 29156393)
45. Nochi, T. et al. A novel M cell-specific carbohydrate-targeted mucosal vaccine effectively induces antigen-specific immune responses. J. Exp. Med. 204, 2789-2796 (2007). (Pubitemid 350179549)
46. Goñi, F. et al. Mucosal vaccination delays or prevents prion infection via the oral route. Neuroscience 133, 413-421 (2005). (Pubitemid 40726209)
47. Kamijo, S. et al. Amelioration of bone loss in collagen-induced arthritis by neutralizing anti-RANKL monoclonal antibody. Biochem. Biophys. Res. Commun. 347, 124-132 (2006). (Pubitemid 44026486)
48. Fraser, H. & Dickinson, A. G. Agent-strain differences in the distribution and intensity of grey matter vacuolation. J. Comp. Pathol. 83, 29-40 (1973).
49. Fraser, H. & Dickinson, A. G. The sequential development of the brain lesions of scrapie in three strains of mice. J. Comp. Pathol. 78, 301-311 (1968).
50. Farquhar, C. F ., Somerville, R. A. & Ritchie, L. A. Post-mortem immunodiagnosis of scrapie and bovine spongiform encephalopathy. J. Virol. Met. 24, 215-222 (1989). (Pubitemid 19134895)