Transcytosis of murine-adapted bovine spongiform encephalopathy agents in an in vitro bovine M cell model

Journal of Virology

Volumn 84, Issue 23, 2010, Pages 12285-12291

  Miyazawa, Kohtaro ^a,d   Kanaya, Takashi ^a   Takakura, Ikuro ^a   Tanaka, Sachi ^a   Hondo, Tetsuya ^a   Watanabe, Hitoshi ^a   Rose, Michael T ^b   Kitazawa, Haruki ^a   Yamaguchi, Takahiro ^a   Katamine, Shigeru ^c   Nishida, Noriyuki ^c   Aso, Hisashi ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b ABERYSTWYTH UNIVERSITY   (United Kingdom)

^c NAGASAKI UNIVERSITY   (Japan)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BOVINE SPONGIFORM ENCEPHALOPATHY AGENT; CELL DIFFERENTIATION; CELL INVASION; CELL TRANSPORT; CELL TYPE; COCULTURE; CONTROLLED STUDY; COW; IN VITRO STUDY; INTESTINE EPITHELIUM CELL; LYMPHOCYTE; MICROFOLD CELL; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; TRANSCYTOSIS; VIRUS INACTIVATION; VIRUS TRANSMISSION;

ANIMALS; ANTIGEN PRESENTATION; ANTIGEN-PRESENTING CELLS; CATTLE; CELL LINE; ENCEPHALOPATHY, BOVINE SPONGIFORM; IMMUNOBLOTTING; INTERLEUKIN-2; INTESTINAL MUCOSA; MICE; MICE, INBRED C57BL; MICROSPHERES; PRIONS; TRANSCYTOSIS;

ANIMALIA; BOS; BOVINAE; BOVINE SPONGIFORM ENCEPHALOPATHY PRION; MURINAE;

EID: 78049500082     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00969-10     Document Type: Article

References (45)

1. Andréoletti, O., P. Berthon, D. Marc, P. Sarradin, J. Grosclaude, L. van Keulen, F. Schelcher, J. M. Elsen, and F. Lantier. 2000. 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.
2. Arima, K., N. Nishida, S. Sakaguchi, K. Shigematsu, R. Atarashi, N. Yamaguchi, D. Yoshikawa, J. Yoon, K. Watanabe, N. Kobayashi, S. Mouillet- Richard, S. Lehmann, and S. Katamine. 2005. Biological and biochemical characteristics of prion strains conserved in persistently infected cell cultures. J. Virol. 79:7104-7112.
3. Arjona, A., L. Simarro, F. Islinger, N. Nishida, and L. Manuelidis. 2004. Two Creutzfeldt-Jakob disease agents reproduce prion protein-independent identities in cell cultures. Proc. Natl. Acad. Sci. U. S. A. 101:8768-8773.
4. 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.
5. Beringue, V., M. Demoy, C. I. Lasmezas, B. Gouritin, C. Weingarten, J. P. Deslys, J. P. Andreux, P. Couvreur, and D. Dormont. 2000. Role of spleen macrophages in the clearance of scrapie agent early in pathogenesis. J. Pathol. 190:495-502. (Pubitemid 30163592)
6. 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.
7. Büeler, 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. (Pubitemid 23201147)
8. Buschmann, A., and M. H. Groschup. 2005. Highly bovine spongiform encephalopathy- sensitive transgenic mice confirm the essential restriction of infectivity to the nervous system in clinically diseased cattle. J. Infect. Dis. 192:934-942.
9. Hamir, A. N., R. A. Kunkle, J. A. Richt, J. M. Miller, and J. J. Greenlee. 2008. Experimental transmission of US scrapie agent by nasal, peritoneal, and conjunctival routes to genetically susceptible sheep. Vet. Pathol. 45: 7-11.
10. Heggebø, R., C. M. Press, G. Gunnes, K. I. Lie, M. A. Tranulis, M. Ulvund, M. H. Groschup, and T. Landsverk. 2000. 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. 81:2327-2337.
11. Heggebø, R., C. M. Press, G. Gunnes, M. J. Ulvund, M. A. Tranulis, and T. Lsverk. 2003. Detection of PrPSc in lymphoid tissues of lambs experimentally exposed to the scrapie agent. J. Comp. Pathol. 128:172-181.
12. Heppner, F. L., A. D. Christ, M. A. Klein, M. Prinz, M. Fried, J. P. Kraehenbuhl, and A. Aguzzi. 2001. Transepithelial prion transport by M cells. Nat. Med. 7:976-977.
13. Hill, A. F., M. Desbruslais, S. Joiner, K. C. Sidle, I. Gowland, J. Collinge, L. J. Doey, and P. Lantos. 1997. The same prion strain causes vCJD and BSE. Nature 389:448-450.
14. Hoffmann, C., U. Ziegler, A. Buschmann, A. Weber, L. Kupfer, A. Oelschlegel, B. Hammerschmidt, and M. H. Groschup. 2007. Prions spread via the autonomic nervous system from the gut to the central nervous system in cattle incubating bovine spongiform encephalopathy. J. Gen. Virol. 88:1048-1055.
15. Huang, F. P., and G. G. MacPherson. 2004. Dendritic cells and oral transmission of prion diseases. Adv. Drug Deliv Rev. 56:901-913.
16. Jeffrey, M., L. Gonzalez, A. Espenes, C. M. Press, S. Martin, M. Chaplin, L. Davis, T. Landsverk, C. MacAldowie, S. Eaton, and G. McGovern. 2006. Transportation of prion protein across the intestinal mucosa of scrapie-susceptible and scrapie-resistant sheep. J. Pathol. 209:4-14.
17. Jeffrey, M., S. Ryder, S. Martin, S. A. Hawkins, L. Terry, C. Berthelin-Baker, and S. J. Bellworthy. 2001. Oral inoculation of sheep with the agent of bovine spongiform encephalopathy (BSE). 1. Onset and distribution of disease- specific PrP accumulation in brain and viscera. J. Comp. Pathol. 124: 280-289.
18. Kanaya, T., H. Aso, K. Miyazawa, T. Kido, T. Minashima, K. Watanabe, S. Ohwada, H. Kitazawa, M. T. Rose, and T. Yamaguchi. 2007. Staining patterns for actin and villin distinguish M cells in bovine follicle-associated epithelium. Res. Vet. Sci. 82:141-149.
19. Kanaya, T., K. Miyazawa, I. Takakura, W. Itani, K. Watanabe, S. Ohwada, H. Kitazawa, M. T. Rose, H. R. McConochie, H. Okano, T. Yamaguchi, and H. Aso. 2008. Differentiation of a murine intestinal epithelial cell line (MIE) toward the M cell lineage. Am. J. Physiol. Gastrointest. Liver Physiol. 295: G273-G284.
20. Kucharzik, T., N. Lugering, K. Rautenberg, A. Lugering, M. A. Schmidt, R. Stoll, and W. Domschke. 2000. Role of M cells in intestinal barrier function. Ann. N. Y. Acad. Sci. 915:171-183.
21. Mabbott, N. A., and G. G. MacPherson. 2006. Prions and their lethal journey to the brain. Nat. Rev. Microbiol. 4:201-211.
22. Maignien, T., M. Shakweh, P. Calvo, D. Marce, N. Sales, E. Fattal, J. P. Deslys, P. Couvreur, and C. I. Lasmezas. 2005. Role of gut macrophages in mice orally contaminated with scrapie or BSE. Int. J. Pharm. 298:293-304.
23. Mishra, R. S., S. Basu, Y. Gu, X. Luo, W. Q. Zou, R. Mishra, R. Li, S. G. Chen, P. Gambetti, H. Fujioka, and N. Singh. 2004. 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.
24. Miyazawa, K., H. Aso, T. Kanaya, T. Kido, T. Minashima, K. Watanabe, S. Ohwada, H. Kitazawa, M. T. Rose, K. Tahara, T. Yamasaki, and T. Yamaguchi. 2006. Apoptotic process of porcine intestinal M cells. Cell Tissue Res. 323:425-432. (Pubitemid 43228098)
25. Miyazawa, K., T. Hondo, T. Kanaya, S. Tanaka, I. Takakura, W. Itani, M. T. Rose, H. Kitazawa, T. Yamaguchi, and H. Aso. 2010. Characterization of newly established bovine intestinal epithelial cell line. Histochem. Cell Biol. 133:125-134.
26. Miyazawa, K., T. Kanaya, S. Tanaka, I. Takakura, K. Watanabe, S. Ohwada, H. Kitazawa, M. T. Rose, S. Sakaguchi, S. Katamine, T. Yamaguchi, and H. Aso. 2007. Immunohistochemical characterization of cell types expressing the cellular prion protein in the small intestine of cattle and mice. Histochem. Cell Biol. 127:291-301.
27. Morel, E., T. Andrieu, F. Casagrande, S. Gauczynski, S. Weiss, J. Grassi, M. Rousset, D. Dormont, and J. Chambaz. 2005. Bovine prion is endocytosed by human enterocytes via the 37 kDa/67 kDa laminin receptor. Am. J. Pathol. 167:1033-1042.
28. Neutra, M. R. 1998. Current concepts in mucosal immunity. V. Role of M cells in transepithelial transport of antigens and pathogens to the mucosal immune system. Am. J. Physiol. 274:G785-G791.
29. Neutra, M. R., A. Frey, and J. P. Kraehenbuhl. 1996. Epithelial M cells: gateways for mucosal infection and immunization. Cell 86:345-348.
30. Nishida, N., D. A. Harris, D. Vilette, H. Laude, Y. Frobert, J. Grassi, D. Casanova, O. Milhavet, and S. Lehmann. 2000. Successful transmission of three mouse-adapted scrapie strains to murine neuroblastoma cell lines overexpressing wild-type mouse prion protein. J. Virol. 74:320-325. (Pubitemid 30002912)
31. Nishida, N., S. Katamine, and L. Manuelidis. 2005. Reciprocal interference between specific CJD and scrapie agents in neural cell cultures. Science 310:493-496. (Pubitemid 41507963)
32. Novakofski, J., M. S. Brewer, N. Mateus-Pinilla, J. Killefer, and R. H. McCusker. 2005. Prion biology relevant to bovine spongiform encephalopathy. J. Anim. Sci. 83:1455-1476.
33. Okamoto, M., H. Furuoka, M. Horiuchi, T. Noguchi, K. Hagiwara, Y. Muramatsu, K. Tomonaga, M. Tsuji, C. Ishihara, K. Ikuta, and H. Taniyama. 2003. Experimental transmission of abnormal prion protein (PrPsc) in the small intestinal epithelial cells of neonatal mice. Vet. Pathol. 40:723-727.
34. Press, C. M., R. Heggebo, and A. Espenes. 2004. Involvement of gut-associated lymphoid tissue of ruminants in the spread of transmissible spongiform encephalopathies. Adv. Drug Deliv. Rev. 56:885-899.
35. Prinz, M., G. Huber, A. J. Macpherson, F. L. Heppner, M. Glatzel, H. P. Eugster, N. Wagner, and A. Aguzzi. 2003. Oral prion infection requires normal numbers of Peyer's patches but not of enteric lymphocytes. Am. J. Pathol. 162:1103-1111.
36. Roucou, X., and A. C. LeBlanc. 2005. Cellular prion protein neuroprotective function: implications in prion diseases. J. Mol. Med. 83:3-11.
37. Sakaguchi, S., S. Katamine, K. Yamanouchi, M. Kishikawa, R. Moriuchi, N. Yasukawa, T. Doi, and T. Miyamoto. 1993. Kinetics of infectivity are dissociated from PrP accumulation in salivary glands of Creutzfeldt-Jakob disease agent-inoculated mice. J. Gen. Virol. 74:2117-2123.
38. Sassa, Y., Y. Inoshima, and N. Ishiguro. 2010. Bovine macrophage degradation of scrapie and BSE PrPSc. Vet. Immunol. Immunopathol. 133:33-39.
39. Silveira, J. R., G. J. Raymond, A. G. Hughson, R. E. Race, V. L. Sim, S. F. Hayes, and B. Caughey. 2005. The most infectious prion protein particles. Nature 437:257-261.
40. Sklaviadis, T., R. Dreyer, and L. Manuelidis. 1992. Analysis of Creutzfeldt- Jakob disease infectious fractions by gel permeation chromatography and sedimentation field flow fractionation. Virus Res. 26:241-254. (Pubitemid 23007826)
41. Smith, P. G., and R. Bradley. 2003. Bovine spongiform encephalopathy (BSE) and its epidemiology. Br. Med. Bull. 66:185-198.
42. Stanley, A. C., J. F. Huntley, M. Jeffrey, and D. Buxton. 2001. Characterization of ovine nasal-associated lymphoid tissue and identification of M cells in the overlying follicle-associated epithelium. J. Comp. Pathol. 125:262-270.
43. Turner, J. R. 2006. Molecular basis of epithelial barrier regulation: from basic mechanisms to clinical application. Am. J. Pathol. 169:1901-1909.
44. van Keulen, L. J., B. E. Schreuder, R. H. Meloen, G. Mooij-Harkes, M. E. Vromans, and J. P. Langeveld. 1996. Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J. Clin. Microbiol. 34:1228-1231.
45. 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.