Close interactions between sympathetic neural fibres and follicular dendritic cells network are not altered in Peyer's patches and spleen of C57BL/6 mice during the preclinical stage of 139A scrapie infection
Piret, Joëlle ; Université de Liège - ULiège > Département de morphologie et pathologie > Département de morphologie et pathologie
Zorzi, Danièle ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Thellin, Olivier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Histologie
Heinen, Ernst ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Département des sciences biomédicales et précliniques
Language :
English
Title :
Close interactions between sympathetic neural fibres and follicular dendritic cells network are not altered in Peyer's patches and spleen of C57BL/6 mice during the preclinical stage of 139A scrapie infection
Aguzzi A., Heinkenwalder M. Pathogenesis of prion diseases: current status and future outlook. Nat. Rev. Microbiol. 2006, 4:765-775.
Andréoletti O., Berthon P., Marc D., Sarradin P., Grosclaude J., Van Keulen L., Schelcher F., Elsen J.M., Lantier F. Early accumulation of PrPSc in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J. Gen. Virol. 2000, 81:3115-3126.
Arnold M.E., Wilesmith J.W. Estimation of the age-dependent risk of infection to BSE of dairy cattle in Great Britain. Prev. Vet. Med. 2004, 66:35-47.
Avrahami D., Gabizon R. Age-related alterations affect the susceptibility of mice to prion infection. Neurobiol. Aging 2011, 32:2006-2025.
Aydar Y., Balogh P., Tew J.G., Szakal A.K. Age-related depression of FDC accessory functions and CD21 ligand-mediated repair of co-stimulation. J. Immunol. 2002, 32:2817-2826.
Aydar Y., Balogh P., Tew J.G., Szakal A.K. Altered regulation of FcgRII on aged follicular dendritic cells correlates with immunoreceptor tyrosin-based inhibition motif signalling in B cells and reduced germinal center formation. J. Immunol. 2003, 171:5975-5987.
Aydar Y., Balogh P., Tew J.G., Szakal A.K. Follicular dendritic cells in aging, a "bottle-neck" in the humoral response. Ageing Res. Rev. 2004, 3:15-29.
Beekes M., McBride P.A. Early accumulation of pathological PrP in the enteric nervous system and gut-associated lymphoid tissue of hamsters orally infected with scrapie. Neurosci. Lett. 2000, 278:181-184.
Beekes M., McBride P.A. The spread of prions through the body in naturally acquired transmissible spongiform encephalopathies. FEBS J. 2007, 274:588-605.
Bellinger D.L., Tran L., Kang J.I., Lubahn C., Felten D.L., Lorton D. Age-related changes in noradrenergic sympathetic innervation of the rat spleen is strain dependent. Brain Behav. Immun. 2002, 16:247-261.
Bellinger D.L., Lorton D., Hamill R.W., Felten S.Y., Felten D.L. Acetylcholinesterase staining and choline acetyltransferase activity in the young adult rat spleen: lack of evidence for cholinergic innervation. Brain Behav. Immun. 1993, 7:191-204.
Bencsik A., Lezmi S., Hunsmann G., Baron T. Close vicinity of PrP expressing cells (FDC) with noradrenergic fibers in healthy sheep spleen. Dev. Immunol. 2001, 8:235-241.
Boelle P.Y., Cesbron J.Y., Valleron A.J. Epidemiological evidence of higher susceptibility to vCJD in the young. BMC Infect. Dis. 2004, 4:26.
Bondiolotti G., Rossoni G., Puricelli M., Formentin E., Lucchini B., Poli G., Ponti W., Bareggi S.R. Changes in sympathetic activity in prion neuroinvasion. Neurobiol. Dis. 2010, 37:114-117.
Brown K.L., Stewart K., Ritchie D.L., Mabbott N.A., Williams A., Fraser H., Morrison W.I., Bruce M.E. Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat. Med. 1999, 5:1308-1312.
Brown K.L., Wathne G.J., Sales J., Bruce M.E., Mabbott N.A. The effects of host age on follicular dendritic cell status dramatically impair scrapie agent neuroinvasion in aged mice. J. Immunol. 2009, 183:5199-5207.
Chiocchetti R., Mazzoli G., Albanese V., Mazzoni M., Clavenzani P., Lalatta-Consterbosa G., Lucchi M.L., Di Guardo G., Marruchella G., Furness J.B. Anatomical evidence for ileal Peyer's patches innervation by enteric nervous system: a potential route for prion neuroinvasion?. Cell Tissue Res. 2008, 332:195-194.
Defaweux V., Dorban G., Demonceau C., Piret J., Jolois O., Thellin O., Thielen C., Heinen E. Interfaces between dendritic cells, other immune cells, and nerve fibres in mouse Peyer's patches: potential sites for neuroinvasion in prion diseases. Microsc. Res. Tech. 2005, 66:1-9.
Defaweux V., Dorban G., Antoine N., Piret J., Gabriel A., Jacqmot O., Falisse-Poirier N., Flandroy S., Zorzi D., Heinen E. Neuroimmune connections in jejunal and ileal Peyer's patches at various bovine ages: potential sites for prion neuroinvasion. Cell Tissue Res. 2007, 329:35-44.
Demonceau C., Marshall A.S., Sales J., Heinen E. Investigation of close interactions between sympathetic neural fibres and the follicular dendritic cells network in the mouse spleen. Eur. J. Histochem. 2008, 52:85-92.
Dorban G., Defaweux V., Demonceau C., Flandroy S., Van Lerberghe P.B., Falisse-Poirrier N., Piret J., Heinen E., Antoine N. Interaction between dendritic cells and nerve fibres in lymphoid organs after oral scrapie exposure. Virchows Arch. 2007, 451:1057-1065.
Dorban G., Defaweux V., Levavasseur E., Demonceau C., Thellin O., Flandroy S., Piret J., Falisse-Poirrier N., Heinen E., Antoine N. Oral scrapie infection modifies the homeostasis of Peyer's patches dendritic cells. Histochem. Cell Biol. 2007, 128:243-251.
Felten D.L., Felten S.Y., Carlson S.L., Olschowka J.A., Livnat S. Noradrenergic and peptidergic innervation of lymphoid tissue. J. Immunol. 1985, 135:755s-765s.
Felten D.L., Felten S.Y., Bellinger D.L., Madden K.S. Fundamental aspects of neural-immune signalling. Psychother. Psychosom. 1993, 60:46-56.
Glatzel M., Heppner F.L., Albers K.M., Aguzzi A. Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 2001, 31:25-34.
Glaysher B.R., Mabbott N.A. Role of the GALT in scrapie agent neuroinvasion from the intestine. J. Immunol. 2007, 178:3757-3766.
Glaysher B.R., Mabbott N.A. Isolated lymphoid follicle maturation induces the development of follicular dendritic cells. Immunology 2007, 120:336-344.
Haik S., Faucheux B.A., Sazdovitch V., Privat N., Kemeny J.L., Perret-Liaudet A., Hauw J.J. The sympathetic nervous system is involved in variant Creutzfeldt-Jakob disease. Nat. Med. 2003, 9:1121-1123.
Heggebo R., Press C.M., Gunnes G., Gonzalez L., Jeffrey M. Distribution and accumulation of PrP in gut-associated and peripheral lymphoid tissue of scrapie-affected Suffolk sheep. J. Gen. Virol. 2002, 83:479-489.
Heggebo R., Gonzalez L., Press C.M., Gunnes G., Espenes A., Jeffrey M. Disease-associated PrP in the enteric nervous system of scrapie-affected Suffolk sheep. J. Gen. Virol. 2003, 84:1327-1338.
Hilton D.A., Fathers E., Edwards P., Ironside J.W., Zajicek J. Prion immunoreactivity in appendix before clinical onset of variant Creutzfeldt-Jakob disease. Lancet 1998, 352:703-704.
Hilton D.A., Ghani A.C., Conyers L., Edwards P., McCardle L., Ritchie D., Penney M., Hegazy D., Ironside J.W. Prevalence of lymphoreticular prion protein accumulation in UK tissue samples. J. Pathol. 2004, 203:733-739.
Hourrigan J.L., Klingsporn A.L., McDaniel H.A., Riemenschneider M.N. Natural scrapie in a goat. J. Am. Vet. Med. Assoc. 1969, 154:538-539.
Ierna M., Farquhar C., Outram G.W., Bruce M.E. Resistance of neonatal mice to scrapie is associated with inefficient infection of the immature spleen. J. Virol. 2006, 80:474-482.
Jeffrey M., McGovern G., Goodsir C.M., Brown K.L., Bruce M.E. Sites of prion protein accumulation in scrapie-infected mouse spleen revealed by immuno-electron microscopy. J. Pathol. 2000, 191:323-332.
Jeffrey M., Gonzalez L., Espenes A., Press C.M., Martin S., Chaplin M., Davis L., Landsverk T., Macaldowie C., Eaton S., McGovern G. Transportation of prion protein across the intestinal mucosa of scrapie-susceptible and scrapie-resistant sheep. J. Pathol. 2006, 209:4-14.
Kimberlin R.H., Walker C.A. The role of the spleen in the neuroinvasion of scrapie in mice. Virus Res. 1989, 12:201-212.
Kujala P., Raymond C.R., Romeijn M., Godsave S.F., van Kasteren S.I., Wille H., Prusiner S.B., Mabbott N.A., Peters P.J. Prion uptake in the gut: identification of the first uptake and replication sites. PLoS Pathog. 2011, 7(12):e1002449.
Lorton D., Lubahn C., Sweeney S., Major A., Lindquist C.A., Schaller J., Washington C., Bellinger D.L. Differences in the injury/sprouting response of splenic noradrenergic nerves in Lewis rats with adjuvant-induced arthritis compared with rats treated with 6-hydroxydopamine. Brain Behav. Immun. 2009, 23:276-285.
Ma B., Wang L., von Wasielewski R., Lindenmaier W., Dittmar K.E. Serial sectioning and three-dimensional reconstruction of mouse Peyer's patch. Micron 2008, 39:967-975.
Mabbott N.A., MacPherson G.G. Prions and their lethal journey to the brain. Nat. Rev. Microbiol. 2006, 4:201-211.
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. 2003, 77:6845-6854.
Madden K.S., Bellinger D.L., Felten S.Y., Snyder E., Maida M.E., Felten D.L. Alterations in sympathetic innervations of thymus and spleen in aged mice. Mech. Ageing Dev. 1997, 94:165-175.
Madden K.S., ThyagaRajan S., Bellinger D.L., Felten S.Y., Felten D.L. Age-associated alterations in sympathetic neural interactions with the immune system. Dev. Comp. Immunol. 1997, 21:479-486.
Marruchella G., Ligios C., Baffoni M., Cancedda M.G., Demontis F., Donatucci G., Chiocchetti R., Clavenzani P., Lalatta-Costerbosa G., Di Guardo G. Ileal tract and Peyer's patch innervation in scrapie-free versus scrapie-affected ovines. Arch. Virol. 2009, 154:709-714.
Marruchella G., Ligios C., Di Guardo G. Age, scrapie status, PrP genotype and follicular dendritic cells in ovine ileal Peyer's patches. Res. Vet. Sci. 2011, 93:853-856.
Maruchella G., Ligios C., Albanese V., Cancedda M.G., Madau L., Lalatta-Costerbosa G., Mazzoni M., Clavenzani P., Chiocchetti R., Sarli G., De Grossi L., Agrimi U., Aguzzi A., Di Guardo G. Enteroglial and neuronal involvement without apparent neuron loss in ileal enteric nervous system plexuses from scrapie-affected sheep. J. Gen. Virol. 2007, 88:2899-2904.
McBride P.A., Schulz-Schaeffer W.J., Donaldson M., Bruce M., Diringer H., Kretzschmar H.A., Beekes M. Early spread of scrapie from the gastrointestinal tract to the CNS involves autonomic fibers of the splanchnic and vagus nerves. J. Virol. 2001, 75:9320-9327.
McCulloch L., Brown K.L., Bradford B.M., Hopkins J., Bailey M., Rajewsky K., Manson J.C., Mabbott N.A. Follicular dendritic cell-specific prion protein (PrPC) expression alone is sufficient to sustain prion infection in the spleen. PLoS Pathog. 2011, 7:e1002402.
McGovern G., Jeffrey M. Scrapie-specific pathology of sheep lymphoid tissues. PLoS ONE 2007, 2:e1304.
McGovern G., Brown K.L., Bruce M.E., Jeffrey M. Murine scrapie infection causes an abnormal germinal centre reaction in the spleen. J. Comp. Pathol. 2004, 130:181-194.
McGovern G., Mabbott N.A., Jeffrey M. Scrapie affects the maturation cycle and immune complex trapping by follicular dendritic cells in mice. PLoS ONE 2009, 4:e8186.
McGovern G., Martin S., Gonzalez L., Witz J., Jeffrey M. Frequency and distribution of nerves in scrapie-affected and unaffected Peyer's patches and lymph nodes. Vet. Pathol. 2009, 46:233-240.
Montrasio F., Frigg R., Glatzel M., Klein M.A., Mackay F., Aguzzi A., Weissmann C. Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 2000, 288:1257-1259.
Novotny G.E., Heuer T., Schotelndreier A., Fleisgarten C. Plasticity of innervation of the medulla of axillary lymph nodes in the rat after antigenic stimulation. Anat. Rec. 1994, 238:213-224.
Novotny G.E., Heuer T., Schotelndreier A., Fleisgarten C. Ultrastructural quantitative analysis of innervation of axillary lymph nodes of the rat after antigenic stimulation. Anat. Rec. 1995, 243:208-222.
Perez S.D., Silva D., Millar A.B., Molinaro C.A., Carter J., Bassett K., Lorton D., Garcia P., Tan L., Gross J., Lubahn C., ThyagaRajan S., Bellinger D.L. Sympathetic innervations of the spleen in male Brown Norway rats: a longitudinal aging study. Brain Res. 2009, 1302:106-117.
Prinz M., Heikenwalder M., Junt T., Schwarz P., Glatzel M., Heppner F.L., Fu Y.X., Lipp M., Aguzzi A. Positioning of follicular dendritic cells within the spleen controls prion neuroinvasion. Nature 2003, 425:957-962.
Prinz M., Huber G., MacPherson A.J., Heppner F.L., Glatzel M., Eugster H.P., Wagner N., Aguzzi A. Oral prion infection requires normal numbers of Peyer's patches but not of enteric lymphocytes. Am. J. Pathol. 2003, 162:1103-1111.
Prusiner S.B. Prions. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:13363-13383.
Raymond C.R., Aucouturier P., Mabbott N.A. In vivo depletion of CD11c+ cells impairs scrapie agent neuroinvasion from the intestine. J. Immunol. 2007, 179:7758-7766.
Shi Q., Zhang B.Y., Gao C., Zhang J., Jiang H.Y., Chen C., Han J., Dong X.P. Mouse-adapted scrapie strains 139A and ME7 overcome species barrier to induce experimental scrapie in hamsters and changed their pathogenic features. Virol. J. 2012, 9:63.
Sigurdson C.J., Williams E.S., Miller M.W., Spraker T.R., O'Rourke K.I., Hoover E.A. Oral transmission and early lymphoid tropism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus). J. Gen. Virol. 1999, 80:2757-2764.
St Rose S., Hunter N., Matthews D., Foster J., Chase-Topping M.E., Kruuk L.E., Shaw D.J., Rhind S.M., Will R.G., Woolhouse M.E. Comparative evidence for a link between Peyer's patch development and susceptibility to transmissible spongiform encephalopathies. BMC Infect. Dis. 2006, 6:5.
Szakal A.K., Taylor J.K., Smith J.P., Kosco-Vilbois M.H., Burton G.F., Tew J.G. Kinetics of germinal center development in lymph nodes of young and aging immune mice. Anat. Rec. 1990, 227:475-485.
Szakal A.K., Aydar Y., Balogh P., Tew J.G. Molecular interactions of FDCs with B cells in aging. Immunol. 2002, 14:267-274.
Takakura I., Miyazawa K., Kanaya T., Itani W., Watanabe H., Hondo T., Rose M.T., Mori T., Sakaguchi S., Nishida N., Katamine S., Yamaguchi T., Aso H. Orally administered prion protein is incorporated by M cells and spreads to lymphoid tissues with macrophages in prion protein knockout mice. Am. J. Pathol. 2011, 179:1301-1309.
Terry L.A., Marsh S., Ryder S.J., Hawkins S.A., Wells G.A., Spencer Y.I. Detection of disease-specific PrP in the distal ileum of cattle exposed orally to the agent of bovine spongiform encephalopathy. Vet. Rec. 2003, 152:387-392.
ThyagaRajan S., Madden K.S., Teruya B., Stevens S.Y., Felten D.L., Bellinger D.L. Age-alterations in sympathetic noradrenergic innervations of primary and secondary organs in female Fischer 344 rats. J. Neuroimmunol. 2011, 233:54-64.
Toppets V., Piret J., Kirschvink N., Lantier F., Lantier I., Berthon P., Daube G., Massart L., Grobet L., Antoine N. Neuroimmunne connections in ovine pharyngeal tonsil: potential site for prion neuroinvasion. Cell Tissue Res. 2012, 348:167-176.
Ueyama T., Kozuki K., Houtani T., Ikeda M., Kitajiri M., Yamashita T., Kumazawa T., Nagatsu I., Sugimoto T. Immunolocalization of tyrosine hydroxylase and vasoactive intestinal polypeptide in nerve fibers innervating human palatine tonsil and paratonsillar glands. Neurosci. Lett. 1990, 116:70-74.
Valleron A.J., Boelle P.Y., Will R., Cesbron J.Y. Estimation of epidemic size and incubation time based on age characteristics of vCJD in the United Kingdom. Science 2001, 294:1726-1728.
Van Keulen L.J., Schreuder B.E., Meloen R.H., Mooij-Harkes G., Vromans M.E., Langeveld J.P. Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J. Clin. Microbiol. 1996, 34:1228-1231.
Van Keulen L.J., Vromans M.E., Dolstra C.H., Bossers A., van Zijderveld F.G. Pathogenesis of bovine spongiform encephalopathy in sheep. Arch. Virol. 2008, 153:445-453.
Von Poser-Klein C., Flechsig E., Hoffmann T., Scwarz P., Harms H., Bujdoso R., Aguzzi A., Klein M.A. Alteration of B-cell subsets enhances neuroinvasion in mouse scrapie infection. J. Virol. 2008, 82:3791-3795.
Vulchanova L., Casey M.A., Crabb G.W., Kennedy W.R., Brown D.R. Anatomical evidence for enteric neuroimmune interactions in Peyer's patches. J. Neuroimmunol. 2007, 185:64-74.
Wathne G.J., Mabbott N.A. The diverse roles of mononuclear phagocytes in prion disease pathogenesis. Prion 2012, 6:124-133.
Weihe E., Krekel J. The neuroimmune connection in human tonsils. Brain Behav. Immun. 1991, 5:41-54.
Zabel M.D., Heikenwalder M., Prinz M., Arrighi I., Schwarz P., Kranich J., von Teichman A., Haas K.M., Zeller N., Tedder T.F. Stromal complement receptor CD21/35 facilitates lymphoid prion colonization and pathogenesis. J. Immunol. 2007, 179:6144-6152.
