[en] In this study, we examined where immune cells and nerve fibres are located in mouse Peyer's patches, with a view to identifying potential sites for neuroinvasion by prions. Special attention was paid to dendritic cells, viewed as candidate transporters of infectious prion. Double immunofluorescence labellings with anti-CD11c antibody and marker for other immune cells (B cells, T cells, follicular dendritic cells) were carried out and analysed by confocal microscopy on Peyer's patch cryosections. To reveal the extensive ganglionated networks of the myenteric and submucosal plexi and the sparse meshworks of nerve strands, we used antibodies directed against different neurofilament subunits or against glial fibrillary acidic protein. In the suprafollicular dome, dendritic cells connect, via their cytoplasmic extensions, enterocytes with M cells of the follicle-associated epithelium. They are also close to B and T cells. Nerve fibres are detected in the suprafollicular dome, notably in contact with dendritic cells. Similar connections between dendritic cells, T cells, and nerve fibres are seen in the interfollicular region. Germinal centres are not innervated; inside them dendritic cells establish contacts with follicular dendritic cells and with B cells. After immunolabelling of normal prion protein, dendritic cells of the suprafollicular dome are intensely positive labelled. (c) 2005 Wiley-Liss, Inc.
Disciplines :
Life sciences: Multidisciplinary, general & others Anatomy (cytology, histology, embryology...) & physiology
Author, co-author :
Defaweux, Valérie ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie humaine
Dorban, Gauthier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie humaine
Demonceau, Christine ; Université de Liège - ULiège > Département de personne et société > Psychologie du travail et des entreprises
Piret, Julie ; Centre Hospitalier Universitaire de Liège - CHU > HOSPITALISATION - CHIR. APP. LOCOMOT. (SN +2A)
Jolois, Olivier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie humaine
Thellin, Olivier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie humaine
Thielen, Caroline ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Anatomie et cytologie pathologiques
Heinen, Ernst ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie humaine
Antoine, Nadine ; Université de Liège - ULiège > Département de morphologie et pathologie > Histologie
Language :
English
Title :
Interfaces between dendritic cells, other immune cells, and nerve fibres in mouse Peyer's patches: Potential sites for neuroinvasion in prion diseases
Publication date :
01 January 2005
Journal title :
Microscopy Research and Technique
ISSN :
1059-910X
eISSN :
1097-0029
Publisher :
Wiley Liss, Inc., Hoboken, United States - New Jersey
Andreoletti O, Berthon P, Marc D, Sarradin P, Grosclaude J, van Keulen L, Schelcher F, Elsen JM, Lantier F. 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.
Aucouturier P, Geissmann F, Damotte D, Saborio GP, Meeker HC, Kascsak R, Kascsak R, Carp RI, Wisniewski T. 2001. Infected splenic dendritic cells are sufficient for prion transmission to the CNS in mouse scrapie. J Clin Invest 108:703-708.
Balemba OB, Mbassa GK, Semuguruka WD, Assey RJ, Kahwa CK, Hay-Schmidt A, Dantzer V. 1999. The topography, architecture and structure of the enteric nervous system in the jejunum and ileum of cattle. J Anat 195:1-9.
Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, Pulendran B, Palucka K. 2000. Immunobiology of dendritic cells. Annu Rev Immunol 18:767-811.
Beringue V, demoy M, Lazmezas CI, Gouritin B, Weingarten C, Des JP, Andreux JP, Couvreur P, Dormont D. 2000. Role of spleen macrophages in the clearance of scrapie agent early in pathogenesis. J Pathol 190:495-502.
Blattler T, Brandner S, Raeber AJ, Klein MA, Voigtlander T, Weissmann C, Aguzzi A. 1997. PrP-expressing tissue required for transfer of scrapie infectivity from spleen to brain. Nature 389:69-73.
Bolton DC, Bendheim PE. 1991. Purification of scrapie agent: how far we come? Curr Top Microbiol Immunol 172:39-55.
Brown KL, Stewart K, Ritchie DL, Mabbott NA, Williams A, Fraser H, Morrison WI, Bruce ME. 1999. Scrapie replication in lymphoid tissues depends on prion protein-expression follicular dendritic cells. Nat Med 5:1308-1312.
Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, Weissmann C. 1993. Mice devoid of PrP are resistant to scrapie. Cell 73:1339-1347.
Burthem J, Urban B, Pain A, Roberts DJ. 2001. The normal cellular prion protein is strongly expressed by myeloid dendritic cells. Blood 98:3733-3738.
Clayton A, Court J, Navabi H, Adams M, Mason MD, Hobot JA, Newman GR, Jasani B. 2001. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J Immunol Methods 247:163-174.
Collinge J. 1999. Variant Creutzfeldt-Jakob disease. Lancet 354:317-323.
Collinge J, Hawke S. 1998. B lymphocytes in prion neuroinvasion: central and peripheral players? Nat Med 4:1369-1370.
Demart S, Fournier JG, Creminon C, Frobert Y, Lamoury F, Marce D, Lasmezas C, Dormont D, Grassi J, Deslys JP. 1999. New insight into abnormal prion protein using monoclonal antibodies. Biochem Biophys Res Commun 265:652-657.
Denzer K, Kleijmeer MJ, Heijnen HF, Stoorvogel W, Geuze HJ. 2000. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113:3365-3374.
Driessen A, Creemers J, Geboes K. 1992. The innervation of the lymphoid tissue at the ileocolonic transition: an enzyme and immunohistochemical study. Acta Anat 144:304-310.
Feher E, Fodor M, Burnstock G. 1992. Distribution of somatostatin- immunoreactive nerve fibres in Peyer's patches. Gut 33:1195-1198.
Follet J, Lemaire-Vieille C, Blanquet-Grossard F, Podevin-Dimster V, Lehmann S, Chauvin JP, Decavel JP, Varea R, Grassi J, Fontes M, Cesbron JY. 2002. PrP expression and replication by Schwann cells: implications in prion spreading. J Virol 76:2434-2439.
Ford MJ, Burton LJ, Morris RJ, Hall SM. 2002. Selective expression of prion protein in peripheral tissues of the adult mouse. Neuroscience 113:177-192.
Fraser H, Dickinson AG. 1978. Studies of lymphoreticular system in the pathogenesis of scrapie: role of spleen and thymus. J Comp Pathol 88:563-573.
Fraser H, Brown KL, Stewart K, McConnell I, McBride P, Williams A. 1996. Replication of scrapie in spleens of SCID mice follows reconstitution with wild-type mouse bone marrow. J Gen Virol 77:1935-1940.
Hadlow WJ, Kennedy RC, Race RE. 1982. Natural infection of Suffolk sheep with scrapie virus. J Infect Dis 146:657-664.
Heggebo R, Gonzalez L, Press CM, Gunnes G, Espenes A, Jeffrey M. 2003. Disease-associated PrP in the enteric nervous system of scrapie-affected Suffolk sheep. J Gen Virol 84:1327-1338.
Heppner FL, Christ AD, Klein MA, Prinz M, Fried M, Kraehenbuhl JP, Aguzzi A. 2001. Transepithelial prion transport by M cells. Nature 7:976-977.
Huang FP, Platt N, Wykes M, Major JR, Powell TJ, Jenkins CD, MacPherson GG. 2000. A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T cell areas of mesenteric lymph nodes. J Exp Med 191:435-444.
Huang FP, Farquhar CF, Mabbott NA, Bruce M, MacPherson GG. 2002. Migrating dendritic cells transport PrPsc from the gut. J Gen Virol 83:267-271.
Krammer HJ, Kuhnel W. 1993. Topography of the enteric nervous system in Peyer's patches of the porcine small intestine. Cell Tissue Res 272:267-272.
Kulkarni-Narla A, Beitz AJ, Brown DR. 1999. Catecholaminergic, cholinergic and peptidergic innervation of gut-associated lymphoid tissue in porcine jejunum and ileum. Cell Tissue Res 298:275-286.
Luhr KM, Wallin RP, Ljunggren HG, Low P, Taraboulos A, Kristensson K. 2002. Processing and degradation of exogenous prion protein by CD11c(+) myeloid dendritic cells in vitro. J Virol 76:12259-12264.
Mabbott AN, Mackay F, Minns F, Bruce ME. 2000. Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nat Med 6:719-720.
Maignien T, Lasmézas CI, Beringue V, Dormont D, Deslys JP. 1999. Pathogenesis of the oral route of infection of mice with scrapie and bovine spongiform encephalopathy agents. J Gen Virol 80:3035-3042.
McBride PA, Eikelenboom P, Kraal G, Fraser H, Bruce ME. 1992. PrP protein is associated with follicular dendritic cells of spleen and lymph nodes in uninfected and scrapie-infected mice. J Pathol 168:413-418.
McBride PA, Schulz-Schaeffer WJ, Donaldson M, Bruce M, Diringer H, Kretzschmar HA, Beekes M. 2001. Early spread of scrapie from the gastrointestinal tract to the central nervous system involves autonomic fibers of the splanchnic and vagus nerves. J Virol 75:9320-9327.
Montrasio F, Frigg R, Glatzel M, Klein MA, Mackay F, Aguzzi A, Weissmann C. 2000. Impaired prion replication of mice lacking functional follicular dendritic cells. Science 288:1257-1259.
Neutra M. 1999. M cells in antigen sampling in mucosal tissue. Curr Top Microb Immunol 236:17-32.
Pfoch M, Unsicker K. 1972. Electron microscopic study on the innervation of Peyer's patches of the Syrian hamster. Z Zellforsch Mikrosk Anat 123:425-429.
Prinz M, Huber G, Macpherson AJ, Heppner FL, Glatzel M, Eugster HP, Wagner N, Aguzzi A. 2003. Oral prion infection requires normal numbers of Peyer's patches but not of enteric lymphocytes. Am J Pathol 162:1103-1111.
Prusiner SB. 1982. Novel proteinaceous infectious particles cause scrapie. Science 216:136-144.
Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, Granucci F, Kraehenbuhl JP, Ricciardi-Castagnoli P. 2001. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2:361-367.
van Keulen LJ, Vromans ME, van Zijderveld FG. 2002. Early and late pathogenesis of natural scrapie infection in sheep. APMIS 110:23-32.
Vidal M, Mangeat P, Hoekstra D. 1997. Aggregation reroutes molecules from a recycling to a vesicle-mediated secretion pathway during reticulocyte maturation. J Cell Sci 110:1867-1877.
