Enhanced enteric invasion of scrapie agents into the villous columnar epithelium via maternal immunoglobulin

International Journal of Molecular Medicine

Volumn 26, Issue 6, 2010, Pages 845-851

  Ano, Yasuhisa ^a,b   Sakudo, Akikazu ^c   Uraki, Ryuta ^a   Sato, Yukita ^d   Kono, Jyuri ^d   Sugiura, Katsuaki ^e   Yokoyama, Takashi ^f   Itohara, Shigeyoshi ^g   Nakayama, Hiroyuki ^a   Yukawa, Masayoshi ^d   Onodera, Takashi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b KIRIN HOLDINGS CO LTD   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d NIHON UNIVERSITY   (Japan)

^e Food and Agricultural Materials Inspection Centre   (Japan)

^f NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^g RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

Columnar epithelial cells; Maternal immunoglobulin; Prion protein; SCID mice; Scrapie; Suckling period

Indexed keywords

IMMUNOGLOBULIN G; MATERNAL ANTIBODY; PRION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DUODENUM; EPIDEMIOLOGICAL DATA; EPITHELIUM CELL; HISTOPATHOLOGY; INTESTINE EPITHELIUM; INTESTINE VILLUS; JEJUNUM; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SCRAPIE; SCRAPIE AGENT; SUCKLING; WEANING; WILD TYPE;

ADMINISTRATION, ORAL; AGE FACTORS; ANIMALS; ANIMALS, SUCKLING; BRAIN CHEMISTRY; CATTLE; DISEASE TRANSMISSION, INFECTIOUS; HOST-PATHOGEN INTERACTIONS; IMMUNOGLOBULINS; IMMUNOHISTOCHEMISTRY; INTESTINAL MUCOSA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, SCID; PRION DISEASES; PRPSC PROTEINS;

EID: 78649975684     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm-00000533     Document Type: Article

References (42)

1. Prusiner SB: Prion diseases and the BSE crisis. Science 278: 245-251, 1997.
2. Ano Y, Sakudo A, Nakayama H and Onodera T: Uptake and distribution of infectious prion protein after oral exposure. Protein Peptide Lett 16: 247-255, 2009.
3. Hoinville LJ: A review of the epidemiology of scrapie in sheep. Rev Sci Tech 15: 827-852, 1996.
4. Will RG: Acquired prion disease: iatrogenic CJD, variant CJD, kuru. Br Med Bull 66: 255-265, 2003.
5. Press CM, Heggebo R and Espenes A: Involvement of gut-associated lymphoid tissue of ruminants in the spread of transmissible spongiform encephalopathies. Adv Drug Deliv 56: 885-899, 2004.
6. Robinson MM, Hadlow WJ, Huff TP, Wells GA, Dawson M, Marsh RF and Gorham JR: Experimental infection of mink with bovine spongiform encephalopathy. J Gen Virol 75: 2151-2155, 1994. (Pubitemid 24282226)
7. Gonzalez L, Terry L and Jeffrey M: Expression of prion protein in the gut of mice infected orally with the 301V murine strain of the bovine spongiform encephalopathy agent. J Comp Pathol 132: 273-282, 2005.
8. Foster JD, Paruham DW, Hunter N and Bruce M: Distribution of the prion protein in sheep terminally affected with BSE following experimental oral transmission. J Gen Virol 82: 2319-2326, 2001.
9. Jeffrey M, Ryder S, Martin S, Hawkins SA, Terry L, Berthelin-Baker C and Bellworthy SJ: 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, 2001.
10. Bons N, Mestre-Frances N, Belli P, Cathala F, Gajdusek DC and Brown P: Natural and experimental oral infection of non-human primates by bovine spongiform encephalopathy agents. Proc Natl Acad Sci USA 96: 4046-4051, 1999.
11. Herzog C, Sales N, Etchegary N, Charbonnier A, Freire S, Dormont D, Deslys JP and Lasmezas CI: Tissue distribution of bovine spongiform encephalopathy agent in primates after intravenous or oral infection. Lancet 363: 422-428, 2004.
12. Prusiner SB, Cochran SP and Alpers MP: Transmission of scrapie in hamsters. J Infect Dis 152: 971-978, 1985.
13. McBride PA and Beekes M: Pathological PrP is abundant in sympathetic and sensory ganglia of hamsters fed with scrapie. Neurosci Lett 265: 135-138, 1999.
14. Maignein T, Lasmezas CI, Beringue V, Dormont D and Deslys JP: Pathogenesis of the oral route of infection of mice with scrapie and bovine spongiform encephalopathy agents. J Gen Virol 80: 3035-3042, 1999. (Pubitemid 29504678)
15. Jeffrey M, McGovern G, Goodsir CM, Brown KL and Bruce ME: Sites of prion protein accumulation in scrapie-infected mouse spleen revealed by immuno-electron microscopy. J Pathol 191: 323-332, 2000.
16. Heggebo R, Press CM, Gunnes G, Lie KI, Tranulis MA, Ulvund M, Groschup MH 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: 2327-2337, 2000.
17. Mabbott NA and Bruce ME: Follicular dendritic cells as targets for intervention in transmissible spongiform encephalopathies. Semin Immunol 14: 285-293, 2002.
18. Jeffrey M, Gonzales L, Espenes A, et al: Transportation of prion protein across the intestinal mucosa of scrapie-susceptible and scrapie-resistant sheep. J Pathol 209: 4-14, 2006.
19. Arnold ME and Wilesmith JW: Estimation of the age-dependent risk of infection to BSE of dairy cattle in Great Britain. Prev Vet Med 66: 35-47, 2004.
20. Ano Y, Nakayama H, Sakudo A, Sawano Y, Tanokura M, Itohara S and Onodera T: Intestinal uptake of amyloid β protein through columnar epithelial cells in suckling mice. Histol Histopathol 24: 283-292, 2009.
21. Ano Y, Nakayama H, Sakai Y, et al: Incorporation of β-amyloid protein through the bovine ileal epithelium before and after weaning: model for orally transmitted amyloidoses. Microbiol Immunol 52: 429-434, 2008.
22. Hirogari Y, Kubo M, Kimura KM, Haritani M and Yokoyama T: Two different scrapie prions isolated in Japanese sheep flocks. Microbiol Immunol 47: 871-876, 2003.
23. Yokoyama T, Masujin K, Iwamura Y, Imamura M and Mohri S: Alteration of the biological and biochemical characteristics of bovine spongiform encephalopathy prions during interspecies transmission in transgenic mice models. J Gen Vriol 90: 261-268, 2009.
24. Inoue Y, Yamakawa Y, Sakudo A, et al: Infection route-independent accumulation of splenic abnormal prion protein. Jpn J Infect Dis 58: 78-82, 2005.
25. Yokoyama T, Kimura KM, Ushiki Y, et al: In vivo conversion of cellular prion protein to pathogenic isoforms, as monitored by conformation-specific antibodies. J Biol Chem 276: 11265-11271, 2001.
26. Hosokawa T, Tsuchiya K, Sato I, et al: A monoclonal antibody (1D12) defines novel distribution patterns of prion protein (PrP) as granules in nucleus. Biochem Biophys Res Commun 366: 657-663, 2008.
27. Hunyady B, Mezey E and Palkovits M: Gastrointestinal immunology: cell types in the lamina propria a morphological review. Acta Physiol Hung 87: 305-328, 2002. (Pubitemid 33601129)
28. Clark MA, Jepson MA, Simmons NL, Booth TA and Hirst BH: Differential expression of lectin-binding sites defines mouse intestinal M-cells. J Histochem Cytochem 41: 1679-1687, 1993.
29. Neutra MR, Frey A and Kraehenbuhl JP: Epithelial M cells: gateways for mucosal infection and immunization. Cell 86: 345-348, 1996. (Pubitemid 26272074)
30. Heppner FL, Christ AD, Klein MA, Prinz M, Fried M, Kraehenbuhl JP and Aguzzi A: Transepithelial prion transport by M cells. Nat Med 7: 976-977, 2002.
31. Beekes M and McBride PA: Early accumulation of pathological PrP in the enteric nervous system and gut-associated lymphoid tissue of hamster orally infected with scrapie. Neurosci Lett 278: 181-184, 2000. (Pubitemid 30009487)
32. Guyer RL, Koshland ME and Knopf PM: Immunoglobulin binding by mouse intestinal epithelial cell receptors. J Immunol 117: 587-593, 1976.
33. Udall JN, Colony P, Fritze L, Pang K, Trier JS and Walker WA: Development of gastrointestinal mucosal barrier: the effect of natural versus artificial feeding on intestinal permeability to macromolecules. Pediatr Res 15: 245-249, 1981. (Pubitemid 11150880)
34. Axelsson L, Jakobsson L, Lindberg T, Polberger S, Benediktsson B and Räihä N: Macromolecular absorption in preterm and term infant. Acta Paediatr Scand 78: 532-537, 1989. (Pubitemid 19218298)
35. Chu SH and Walker WA: Growth factor signal transduction in human intestinal cells. Adv Exp Med Biol 310: 107-112, 1991.
36. Teichberg S, Waprnir RA, Moyse J and Lifshitz F: Development of the neonatal rat small intestinal barrier to non-specific macromolecular absorption. Role of dietary corticosterone. Pediatr Res 32: 50-57, 1992.
37. Rumbo M and Schiffrin EJ: Ontogeny of intestinal epithelium immune functions: developmental and environmental regulation. Cell Mol Life Sci 62: 1288-1296, 2005. (Pubitemid 40853816)
38. Smyth SH, Feldhaus S, Schumacher U and Carr KE: Uptake of inert microparticles in normal and immune deficient mice. Int J Pharm 346: 109-118, 2008. (Pubitemid 350101999)
39. Israel EJ, Patel VK, Taylor SF, Marshak-Rothstein A and Simister NE: Requirement for a beta 2-microglobulin-associated Fc receptor for acquisition of maternal IgG by fetal and neonatal mice. J Immunol 154: 6246-6251, 1995.
40. Roopenian DC and Akilesh S: FcRn: the neonatal Fc receptor comes of age. Nat Rev Immunol 7: 715-725, 2007.
41. Kramer DR and Cebra JJ: Early appearance of 'natural' mucosal IgA responses and germinal centers in suckling mice developing in the absence of maternal antibodies. J Immunol 154: 2051-2062, 1995.
42. Johnson CJ, Pedersen JA, Chappell RJ, McKenzie D and Aiken JM: Oral transmissibility of prion disease is enhanced by binding to soil paticles. PLoS Pathog 3: e93, 2007.