Orally administered prion protein is incorporated by M cells and spreads into lymphoid tissues with macrophages in prion protein knockout mice

American Journal of Pathology

Volumn 179, Issue 3, 2011, Pages 1301-1309

  Takakura, Ikuro ^a,e   Miyazawa, Kohtaro ^a,f   Kanaya, Takashi ^a   Itani, Wataru ^a   Watanabe, Kouichi ^a   Ohwada, Shyuichi ^a   Watanabe, Hitoshi ^a   Hondo, Tetsuya ^a   Rose, Michael T ^b   Mori, Tsuyoshi ^c   Sakaguchi, Suehiro ^c   Nishida, Noriyuki ^d   Katamine, Shigeru ^d   Yamaguchi, Takahiro ^a   Aso, Hisashi ^a  

^a TOHOKU UNIVERSITY   (Japan)

^b ABERYSTWYTH UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d NAGASAKI UNIVERSITY   (Japan)

^e KISSEI PHARMACEUTICAL CO LTD   (Japan)

^f NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD14 ANTIGEN; LIPOCORTIN 5; PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HOMOGENATE; HUMAN; IMMUNOHISTOCHEMISTRY; INTESTINE MUCOSA; MACROPHAGE; MALE; MESENTERY LYMPH NODE; MOUSE; NONHUMAN; PATHOGENESIS; PERIPHERAL NERVOUS SYSTEM; PEYER PATCH; PRION DISEASE; PRIORITY JOURNAL; SPLEEN;

ADMINISTRATION, ORAL; ANIMALS; BRAIN; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; INTESTINE, SMALL; LYMPH NODES; MACROPHAGES; MALE; MESENTERY; MICE; MICE, KNOCKOUT; PEYER'S PATCHES; PRION DISEASES; PRIONS; SPLEEN;

EID: 80052869514     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.05.058     Document Type: Article

References (53)

1. A. Aguzzi Prion diseases of humans and farm animals: epidemiology, genetics and pathogenesis J Neurochem 97 2006 1726 1739 (Pubitemid 43873663)
2. C.L. Masters, and E.P. Richardson Jr Subacute spongiform encephalopathy (Creutzfeldt-Jakob Disease) The nature and progression of spongiform change Brain 101 1978 333 344 (Pubitemid 8372325)
3. B. van Everbroeck, I. Dobbeleir, M. De Waele, E. De Leenheir, U. Lubke, J.J. Martin, and P. Cras Extracellular protein deposition correlates with glial activation and oxidative stress in Creutzfeldt-Jakob and Alzheimer's disease Acta Neuropathol 108 2004 194 200 (Pubitemid 39199510)
4. L.J. van Keulen, M.E. Vromans, C.H. Dolstra, A. Bossers, and F.G. van Zijderveld Pathogenesis of bovine spongiform encephalopathy in sheep Arch Virol 153 2008 445 453
5. D.C. Bolton, M.P. McKinley, and S.B. Prusiner Identification of a protein that purifies with the scrapie prion Science 218 1982 1309 1311
6. A.F. Hill, M. Desbruslais, S. Joiner, K.C. Sidle, I. Gowland, J. Collinge, L.J. Doey, and P. Lantos The same prion strain causes vCJD and BSE Nature 389 1997 448 450 (Pubitemid 27435311)
7. N. Mabbott, and M. Turner Prions and the blood and immune systems Haematologica 90 2005 542 548 (Pubitemid 40592898)
8. M.R. Neutra, A. Frey, and J.P. Kraehenbuhl Epithelial M cells: gateways for mucosal infection and immunization Cell 86 1996 345 348 (Pubitemid 26272074)
9. F.L. Heppner, A.D. Christ, M.A. Klein, M. Prinz, M. Fried, J.P. Kraehenbuhl, and A. Aguzzi Transepithelial prion transport by M cells Nat Med 7 2001 976 977
10. T. Maignien, C.I. Lasmézas, V. Beringue, D. Dormont, and J.P. Deslys Pathogenesis of the oral route of infection of mice with scrapie and bovine spongiform encephalopathy agents J Gen Virol 80 1999 3035 3042 (Pubitemid 29504678)
11. L. Vulchanova, M.A. Casey, G.W. Crabb, W.R. Kennedy, and D.R. Brown Anatomical evidence for enteric neuroimmune interactions in Peyer's patches J Neuroimmunol 185 2007 64 74 (Pubitemid 46497442)
12. P.A. McBride, W.J. Schulz-Schaeffer, M. Donaldson, M. Bruce, H. Diringer, H.A. Kretzschmar, and M. Beekes 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 (Pubitemid 32851936)
13. Sc in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie J Gen Virol 81 2000 3115 3126 (Pubitemid 32000659)
14. R.I. Carp, and S.M. Callahan In vitro interaction of scrapie agent and mouse peritoneal macrophages Intervirology 16 1981 8 13 (Pubitemid 12200956)
15. F.P. Huang, N. Platt, M. Wykes, J.R. Major, T.J. Powell, C.D. Jenkins, and G.G. MacPherson A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes J Exp Med 191 2000 435 444
16. Sc from the gut J Gen Virol 83 2002 267 271 (Pubitemid 34030831)
17. T. Kitamoto, T. Muramoto, S. Mohri, K. Doh-Ura, and J. Tateishi Abnormal isoform of prion protein accumulates in follicular dendritic cells in mice with Creutzfeldt-Jakob disease J Virol 65 1991 6292 6295
18. K. Miyazawa, T. Kanaya, S. Tanaka, I. Takakura, K. Watanabe, S. Ohwada, H. Kitazawa, M.T. Rose, S. Sakaguchi, S. Katamine, T. Yamaguchi, and H. Aso Immunohistochemical characterization of cell types expressing the cellular prion protein in the small intestine of cattle and mice Histochem Cell Biol 127 2007 291 301
19. S. Sakaguchi, S. Katamine, K. Shigematsu, A. Nakatani, R. Moriuchi, N. Nishida, K. Kurokawa, R. Nakaoke, H. Sato, K. Jishage, J. Kuno, T. Noda, and T. Miyamoto Accumulation of proteinase K-resistant prion protein (PrP) is restricted by the expression level of normal PrP in mice inoculated with a mouse-adapted strain of the Creutzfeldt-Jakob disease agent J Virol 69 1995 7586 7592
20. A. Li, S. Sakaguchi, K. Shigematsu, R. Atarashi, B.C. Roy, R. Nakaoke, K. Arima, N. Okimura, J. Kopacek, and S. Katamine Physiological expression of the gene for PrP-like protein PrPLP/Dpl, by brain endothelial cells and its ectopic expression in neurons of PrP-deficient mice ataxic due to purkinje cell degeneration Am J Pathol 157 2000 1447 1452
21. C.R. Moore, P. Mastrangelo, E. Bouzamondo, C. Heinrich, G. Legname, S.B. Prusiner, L. Hood, D. Westaway, J.S. DeArmond, and P. Tremblay Doppel-induced cerebellar degeneration in transgenic mice Proc Natl Acad Sci USA 98 2001 15288 15293 (Pubitemid 34014007)
22. N.L. Tuzi, E. Gall, D. Melton, and J.C. Manson Expression of doppel in the CNS of mice does not modulate transmissible spongiform encephalopathy disease J Gen Virol 83 2002 705 711 (Pubitemid 34183015)
23. R.L. Coffman Surface antigen expression and immunoglobulin gene rearrangement during mouse pre-B cell development Immunol Rev 69 1982 5 23
24. K. Matsuura, T. Ishida, M. Setoguchi, Y. Higuchi, S. Akizuki, and S. Yamamoto Upregulation of mouse CD14 expression in Kupffer cells by lipopolysaccharide J Exp Med 179 1994 1671 1676 (Pubitemid 24129585)
25. J.L. Whiteland, S.M. Nicholls, C. Shimeld, D.L. Easty, N.A. Williams, and T.J. Hill Immunohistochemical detection of T-cell subsets and other leukocytes in paraffin-embedded rat and mouse tissues with monoclonal antibodies J Histochem Cytochem 43 1995 313 320
26. J.L. Owen, V. Iragavarapu-Charyulu, Z. Gunja-Smith, L.M. Herbert, J.F. Grosso, and D.M. Lopez Up-regulation of matrix metalloproteinase-9 in T lymphocytes of mammary tumor bearers: role of vascular endothelial growth factor J Immunol 171 2003 4340 4351 (Pubitemid 37238712)
27. P. Verbrugghe, W. Waelput, B. Dieriks, A. Waeytens, J. Vandesompele, and C.A. Cuvelier Murine M cells express annexin V specifically J Pathol 209 2006 240 249 (Pubitemid 43805420)
28. C. Huber, C. Thielen, H. Seeger, P. Schwarz, F. Montrasio, M.R. Wilson, E. Heinen, Y.X. Fu, G. Miele, and A. Aguzzi Lymphotoxin-beta receptor-dependent genes in lymph node and follicular dendritic cell transcriptomes J Immunol 174 2005 5526 5536 (Pubitemid 40593193)
29. J. Tateishi, M. Ohta, M. Koga, Y. Sato, and Y. Kuroiwa Transmission of chronic spongiform encephalopathy with kuru plaques from humans to small rodents Ann Neurol 5 1979 581 584 (Pubitemid 9183601)
30. P. Balogh, Y. Aydar, J.G. Tew, and A.K. Szakal Appearance and phenotype of murine follicular dendritic cells expressing VCAM-1 Anat Rec 268 2002 160 168
31. M. Breel, R.E. Mebius, and G. Kraal Dendritic cells of the mouse recognized by two monoclonal antibodies Eur J Immunol 17 1987 1555 1559 (Pubitemid 18000191)
32. R.J. Thompson, J.F. Doran, P. Jackson, A.P. Dhillon, and J. Rode PGP 9.5 a new marker for vertebrate neurons and neuroendocrine cells Brain Res 278 1983 224 228 (Pubitemid 14219291)
33. M. Beekes, and P.A. McBride Early accumulation of pathological PrP in the enteric nervous system and gut-associated lymphoid tissue of hamsters orally infected with scrapie Neurosci Lett 278 2000 181 184 (Pubitemid 30009487)
34. K. Miyazawa, T. Kanaya, I. Takakura, S. Tanaka, T. Hondo, H. Watanabe, M.T. Rose, H. Kitazawa, T. Yamaguchi, S. Katamine, N. Nishida, and H. Aso Transcytosis of murine-adapted BSE agent in an in vitro bovine M cell model J Virol 84 2010 12285 12291
35. T. Nochi, Y. Yuki, A. Matsumura, M. Mejima, K. Terahara, D.Y. Kim, S. Fukuyama, K. Iwatsuki-Horimoto, Y. Kawaoka, T. Kohda, S. Kozaki, O. Igarashi, and H. Kiyono A novel M cell-specific carbohydrate-targeted mucosal vaccine effectively induces antigen-specific immune responses J Exp Med 204 2007 2789 2796 (Pubitemid 350179549)
36. N.A. Mabbott, and G.G. MacPherson Prions and their lethal journey to the brain Nat Rev Mcirobiol 4 2006 201 211
37. K. Vana, C. Zuber, D. Nikles, and S. Weiss Novel aspects of prions, their receptor molecules, and innovative approaches for TSE therapy Cell Mol Neurobiol 27 2007 107 128 (Pubitemid 46169898)
38. B. Ma, R. von Wasielewski, W. Lindenmaier, and K.E. Dittmar Immunohistochemical study of blood and lymphatic vasculature and the innervation of mouse gut and gut-associated lymphoid tissue Anat Histol Embryol 36 2007 62 74 (Pubitemid 46192825)
39. Sc by the Peyer's patches in hamsters after oral exposure to scrapie J Comp Pathol 134 2006 126 133
40. L.J. van Keulen, M.E. Vromans, and F.G. van Zijderveld Early and late pathogenesis of natural scrapie infection in sheep APMIS 110 2002 23 32 (Pubitemid 34289466)
41. C. Scherbel, R. Pichner, M.H. Groschup, S. Mueller-Hellwig, S. Scherer, R. Dietrich, E. Maertlbauer, and M. Gareis Degradation of scrapie associated prion protein (PrPSc) by the gastrointestinal microbiota of cattle Vet Res 37 2006 695 703 (Pubitemid 44543954)
42. C.J. de Almeida, L.B. Chiarini, J.P. da Silva, P.M. E Silva, M.A. Martins, and R. Linden The cellular prion protein modulates phogocytosis and inflammatory response J Leukoc Biol 77 2005 238 246 (Pubitemid 40315058)
43. B. Krebs, C. Dorner-Ciossek, R. Schmalzbauer, N. Vassallo, J. Herms, and H.A. Kretzschmer Prion protein induced signaling cascades in monocytes Biochem Biophys Res Commun 340 2006 13 22 (Pubitemid 41829575)
44. K.M. Luhr, R.P. Wallin, H.G. Lunggren, P. Low, A. Taraboulos, and K. Kristensson Processing and degradation of exogenous prion protein by CD11c(+) myeloid dendritic cells in vitro J Virol 23 2002 12259 12264 (Pubitemid 35304323)
45. V. Beringue, M. Demoy, C.I. Lasmézas, B. Gouritin, C. Weingarten, J.P. Deslys, J.P. Andreux, P. Couvreur, and D. Dormont Role of spleen macrophages in the clearance of scrapie agent early in pathogenesis J Pathol 190 2000 495 502 (Pubitemid 30163592)
46. R. Heggebø, C.M. Press, G. Gunnes, K.I. Lie, M.A. Tranulis, M. Ulvund, M.H. Groschup, and T. Landsverk 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
47. D.A. Hilton, A.C. Ghani, L. Conyers, P. Edwards, L. McCardle, D. Ritchie, M. Penney, D. Hegazy, and J.W. Ironside Prevalence of lymphoreticular prion protein accumulation in UK tissue samples J Pathol 203 2004 733 739 (Pubitemid 38961558)
48. M. Jeffrey, G. McGovern, C.M. Goodsir, K.L. Brown, and M.E. Bruce Sites of prion protein accumulation in scrapie-infected mouse spleen revealed by immuno-electron microscopy J Pathol 191 2000 323 332 (Pubitemid 30441258)
49. A. Iwasaki, and B.L. Kelsall Unique functions of CD11b+ CD8α+, and double-negative Peyer's patch dendritic cells J Immunol 166 2001 4884 4890 (Pubitemid 32280697)
50. P.W. Bland, and C.V. Whiting Differential control of major histocompatibility complex class II I-Ek alpha protein expression in the epithelium and in subsets of lamina propria antigen-presenting cells of the gut Immunology 79 1993 107 111 (Pubitemid 23151201)
51. M. Prinz, M. Heikenwalder, T. Junt, P. Schwarz, M. Glatzel, F.L. Heppner, Y.X. Fu, M. Lipp, and A. Aguzzi Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion Nature 425 2003 957 962 (Pubitemid 37376926)
52. G. Dorban, V. Defaweux, C. Demonceau, S. Flandroy, P.B. van Lerberghe, N. Falisse-Poirrier, J. Piret, E. Heinen, and N. Antoine Interaction between dendritic cells and nerve fibres in lymphoid organs after oral scrapie exposure Virchows Arch 451 2007 1057 1065 (Pubitemid 350165257)
53. B.R. Glaysher, and N.A. Mabbott Role of the GALT in scrapie agent neuroinvasion from the intestine J Immunol 178 2007 3757 3766 (Pubitemid 46417644)