The diverse roles of mononuclear phagocytes in prion disease pathogenesis

Prion

Volumn 6, Issue 2, 2012, Pages 124-133

  Wathne, Gwennaelle J ^a   Mabbott, Neil A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Dendritic cells; Macrophages; Mononuclear phagocytes; Prion transmission; PrPSc; TSE

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; PRION PROTEIN;

ALZHEIMER DISEASE; BOVINE SPONGIFORM ENCEPHALOPATHY; CELL INVASION; CHRONIC WASTING DISEASE; CONFERENCE PAPER; DISEASE ASSOCIATION; FAMILIAL CREUTZFELDT JAKOB DISEASE; FELINE SPONGIFORM ENCEPHALOPATHY; FOLLICULAR DENDRITIC CELL; HUMAN; IATROGENIC CREUTZFELDT JAKOB DISEASE; INTESTINE LYMPHATIC TISSUE; MACROPHAGE; MICROGLIA; MONONUCLEAR PHAGOCYTE; NEUROPATHOLOGY; NONHUMAN; PATHOGENESIS; POLYMERASE CHAIN REACTION; PRION DISEASE; RETICULOENDOTHELIAL SYSTEM; SCRAPIE; SPORADIC CREUTZFELDT JAKOB DISEASE; TRANSMISSIBLE MINK ENCEPHALOPATHY; VARIANT CREUTZFELDT JAKOB DISEASE;

ANIMALS; CATTLE; HUMANS; MONONUCLEAR PHAGOCYTE SYSTEM; PRION DISEASES; PRIONS;

MAMMALIA;

EID: 84861757328     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.18853     Document Type: Conference Paper

References (126)

1. Bruce ME, Brown KL, Mabbott NA, Farquhar CF, Jeffrey M. Follicular dendritic cells in TSE pathogenesis. Immunol Today 2000; 21:442-6; PMID:10953096; http://dx.doi.org/10.1016/S0167-5699(00)01696-0.
2. Brown KL, Ritchie DL, McBride PA, Bruce ME. Detection of PrP in extraneural tissues. Microsc Res Tech 2000; 50:40-5; PMID:10871547; http://dx.doi.org/10.1002/1097-0029(20000701)50:1〈40::AID-JEMT7〉3.0. CO;2-M.
3. Heggebø R, Press CM, Gunnes G, González L, Jeffrey M. Distribution and accumulation of PrP in gut-associated and peripheral lymphoid tissue of scrapie-affected Suffolk sheep. J Gen Virol 2002; 83:479-89; PMID:11807242.
4. Andréoletti O, Berthon P, Marc D, Sarradin P, Grosclaude J, van Keulen L, et al. 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 2000; 81:3115-26; PMID:11086143.
5. Somerville RA, Birkett CR, Farquhar CF, Hunter N, Goldmann W, Dornan J, et al. Immunodetection of PrPSc in spleens of some scrapie-infected sheep but not BSE-infected cows. J Gen Virol 1997; 78:2389-96; PMID:9292029.
6. Buschmann A, Groschup MH. Highly bovine spongiform encephalopathy- sensitive transgenic mice confirm the essential restriction of infectivity to the nervous system in clinically diseased cattle. J Infect Dis 2005; 192:934-42; PMID:16088845; http://dx.doi.org/10.1086/431602.
7. Hoffmann C, Eiden M, Kaatz M, Keller M, Ziegler U, Rogers R, et al. BSE infectivity in jejunum, ileum and ileocaecal junction of incubating cattle. Vet Res 2011; 42:21; PMID:21314904; http://dx.doi.org/10.1186/1297-9716-42-21.
8. Iwata N, Sato Y, Higuchi Y, Nohtomi K, Nagata N, Hasegawa H, et al. Distribution of PrP(Sc) in cattle with bovine spongiform encephalopathy slaughtered at abattoirs in Japan. Jpn J Infect Dis 2006; 59:100-7; PMID:16632909.
9. Terry LA, Marsh S, Ryder SJ, Hawkins SAC, Wells GAH, Spencer YI. Detection of disease-specific PrP in the distal ileum of cattle exposed orally to the agent of bovine spongiform encephalopathy. Vet Rec 2003; 152:387-92; PMID:12696704; http://dx.doi.org/10.1136/vr.152.13.387.
10. Wells GA, Dawson M, Hawkins SA, Green RB, Dexter I, Francis ME, et al. Infectivity in the ileum of cattle challenged orally with bovine spongiform encephalopathy. Vet Rec 1994; 135:40-1; PMID:7975074; http://dx.doi.org/10.1136/ vr.135.2.40.
11. Foster JD, Parnham DW, Hunter N, Bruce M. Distribution of the prion protein in sheep terminally affected with BSE following experimental oral transmission. J Gen Virol 2001; 82:2319-26; PMID:11562525.
12. Hill AF, Zeidler M, Ironside J, Collinge J. Diagnosis of new variant Creutzfeldt-Jakob disease by tonsil biopsy. Lancet 1997; 349:99-100; PMID:8996424; http://dx.doi.org/10.1016/S0140-6736(97)24002-X.
13. Büeler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, Aguet M, et al. Mice devoid of PrP are resistant to scrapie. Cell 1993; 73:1339-47; PMID:8100741; http://dx.doi.org/10.1016/0092-8674(93)90360-3.
14. Burthem J, Urban B, Pain A, Roberts DJ. The normal cellular prion protein is strongly expressed by myeloid dendritic cells. Blood 2001; 98:3733-8; PMID:11739179; http://dx.doi.org/10.1182/blood.V98.13.3733.
15. Mabbott NA, Brown KL, Manson J, Bruce ME. T-lymphocyte activation and the cellular form of the prion protein. Immunology 1997; 92:161-5; PMID:9415021; http://dx.doi.org/10.1046/j.1365-2567.1997.00331.x.
16. Mabbott NA, Farquhar CF, Brown KL, Bruce ME. Involvement of the immune system in TSE pathogenesis. Immunol Today 1998; 19:201-3; PMID:9613034; http://dx.doi.org/10.1016/S0167-5699(98)01253-5.
17. Sugaya M, Nakamura K, Watanabe T, Asahina A, Yasaka N, Koyama Yi, et al. Expression of cellular prion-related protein by murine Langerhans cells and keratinocytes. J Dermatol Sci 2002; 28:126-34; PMID:11858951; http://dx.doi.org/10.1016/S0923-1811(01)00160-8.
18. Horiuchi M, Yamazaki N, Ikeda T, Ishiguro N, Shinagawa M. A cellular form of prion protein (PrPC) exists in many non-neuronal tissues of sheep. J Gen Virol 1995; 76:2583-7; PMID:7595362; http://dx.doi.org/10.1099/0022-1317-76-10- 2583.
19. Brown KL, Stewart K, Ritchie DL, Mabbott NA, Williams A, Fraser H, et al. Scrapie replication in lymphoid tissues depends on prion protein-expressing follicular dendritic cells. Nat Med 1999; 5:1308-12; PMID:10545999; http://dx.doi.org/10.1038/15264.
20. Pan KM, Baldwin M, Nguyen J, Gasset M, Serban A, Groth D, et al. Conversion of alpha-helices into beta-sheets features in the formation of the scrapie prion proteins. Proc Natl Acad Sci USA 1993; 90:10962-6; PMID:7902575; http://dx.doi.org/10.1073/pnas.90.23.10962.
21. Stahl N, Borchelt DR, Hsiao K, Prusiner SB. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 1987; 51:229-40; PMID:2444340; http://dx.doi.org/10.1016/0092-8674(87)90150-4.
22. Büeler H, Fischer M, Lang Y, Bluethmann H, Lipp HP, DeArmond SJ, et al. Normal development and behaviour of mice lacking the neuronal cell-surface PrP protein. Nature 1992; 356:577-82; PMID:1373228; http://dx.doi.org/10.1038/ 356577a0.
23. Isaacs JD, Jackson GS, Altmann DM. The role of the cellular prion protein in the immune system. Clin Exp Immunol 2006; 146:1-8; PMID:16968391; http://dx.doi.org/10.1111/j.1365-2249.2006.03194.x.
24. Manson JC, Clarke AR, Hooper ML, Aitchison L, McConnell I, Hope J. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 1994; 8:121-7; PMID:7999308; http://dx.doi.org/10.1007/BF02780662.
25. Gimbel DA, Nygaard HB, Coffey EE, Gunther EC, Laurén J, Gimbel ZA, et al. Memory impairment in transgenic Alzheimer mice requires cellular prion protein. J Neurosci 2010; 30:6367-74; PMID:20445063; http://dx.doi.org/10.1523/ JNEUROSCI.0395-10.2010.
26. Gadotti VM, Zamponi GW. Cellular prion protein protects from inflammatory and neuropathic pain. Mol Pain 2011; 7:59; PMID:21843375; http://dx.doi.org/10. 1186/1744-8069-7-59.
27. Walz R, Amaral OB, Rockenbach IC, Roesler R, Izquierdo I, Cavalheiro EA, et al. Increased sensitivity to seizures in mice lacking cellular prion protein. Epilepsia 1999; 40:1679-82; PMID:10612329; http://dx.doi.org/10.1111/j.1528- 157.1999.tb01583.x.
28. Martins VR, Beraldo FH, Hajj GN, Lopes MH, Lee KS, Prado MM, et al. Prion protein: orchestrating neurotrophic activities. Curr Issues Mol Biol 2010; 12:63-86; PMID:19767651.
29. Li R, Liu D, Zanusso G, Liu T, Fayen JD, Huang JH, et al. The expression and potential function of cellular prion protein in human lymphocytes. Cell Immunol 2001; 207:49-58; PMID:11161453; http://dx.doi.org/10.1006/cimm.2000. 1751.
30. Mattei V, Garofalo T, Misasi R, Circella A, Manganelli V, Lucania G, et al. Prion protein is a component of the multimolecular signaling complex involved in T cell activation. FEBS Lett 2004; 560:14-8; PMID:14987990; http://dx.doi.org/10.1016/S0014-5793(04)00029-8.
31. Lawson VA, Collins SJ, Masters CL, Hill AF. Prion protein glycosylation. J Neurochem 2005; 93:793-801; PMID:15857383; http://dx.doi.org/10.1111/j.1471- 4159.2005.03104.x.
32. Prusiner SB. Novel proteinaceous infectious particles cause scrapie. Science 1982; 216:136-44; PMID:6801762; http://dx.doi.org/10.1126/science. 6801762.
33. Atarashi R, Wilham JM, Christensen L, Hughson AG, Moore RA, Johnson LM, et al. Simplified ultrasensitive prion detection by recombinant PrP conversion with shaking. Nat Methods 2008; 5:211-2; PMID:18309304; http://dx.doi.org/10. 1038/nmeth0308-211.
34. Saborio GP, Permanne B, Soto C. Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 2001; 411:810-3; PMID:11459061; http://dx.doi.org/10.1038/35081095.
35. Soto C, Saborio GP, Anderes L. Cyclic amplification of protein misfolding: application to prion-related disorders and beyond. Trends Neurosci 2002; 25:390-4; PMID:12127750; http://dx.doi.org/10.1016/S0166-2236(02)02195-1.
36. Kim JI, Cali I, Surewicz K, Kong Q, Raymond GJ, Atarashi R, et al. Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J Biol Chem 2010; 285:14083-7; PMID:20304915; http://dx.doi.org/10.1074/jbc.C110.113464.
37. Glaysher BR, Mabbott NA. Role of the GALT in scrapie agent neuroinvasion from the intestine. J Immunol 2007; 178:3757-66; PMID:17339474.
38. Hilton DA, Fathers E, Edwards P, Ironside JW, Zajicek J. Prion immunoreactivity in appendix before clinical onset of variant Creutzfeldt-Jakob disease. Lancet 1998; 352:703-4; PMID:9728989; http://dx.doi.org/10.1016/S0140- 6736(98)24035-9.
39. Mabbott NA, Young J, McConnell I, Bruce ME. Follicular dendritic cell dedifferentiation by treatment with an inhibitor of the lymphotoxin pathway dramatically reduces scrapie susceptibility. J Virol 2003; 77:6845-54; PMID:12768004; http://dx.doi.org/10.1128/JVI.77.12.6845-54.2003.
40. Prinz M, Huber G, Macpherson AJS, Heppner FL, Glatzel M, Eugster HP, et al. Oral prion infection requires normal numbers of Peyer's patches but not of enteric lymphocytes. Am J Pathol 2003; 162:1103-11; PMID:12651603; http://dx.doi.org/10.1016/S0002-9440(10)63907-7.
41. Sigurdson CJ, Williams ES, Miller MW, Spraker TR, O'Rourke KI, Hoover EA. Oral transmission and early lymphoid tropism of chronic wasting disease PrPres in mule deer fawns (Odocoileus hemionus). J Gen Virol 1999; 80:2757-64; PMID:10573172.
42. Mabbott NA, Kenneth Baillie J, Kobayashi A, Donaldson DS, Ohmori H, Yoon SO, et al. Expression of mesenchyme-specific gene signatures by follicular dendritic cells: insights from the meta-analysis of microarray data from multiple mouse cell populations. Immunology 2011; 133:482-98; PMID:21635249; http://dx.doi.org/10.1111/j.1365-2567.2011.03461.x.
43. Mabbott NA, Mackay F, Minns F, Bruce ME. Temporary inactivation of follicular dendritic cells delays neuroinvasion of scrapie. Nat Med 2000; 6:719-20; PMID:10888894; http://dx.doi.org/10.1038/77401.
44. Montrasio F, Frigg R, Glatzel M, Klein MA, Mackay F, Aguzzi A, et al. Impaired prion replication in spleens of mice lacking functional follicular dendritic cells. Science 2000; 288:1257-9; PMID:10818004; http://dx.doi.org/10. 1126/science.288.5469.1257.
45. McCulloch L, Brown KL, Bradford BM, Hopkins J, Bailey M, Rajewsky K, et al. Follicular dendritic cell-specific prion protein (PrP) expression alone is sufficient to sustain prion infection in the spleen. PLoS Pathog 2011; 7:1002402; PMID:22144895; http://dx.doi.org/10.1371/journal.ppat.1002402.
46. Bradford BM, Sester DP, Hume DA, Mabbott NA. Defining the anatomical localisation of subsets of the murine mononuclear phagocyte system using integrinalpha X (Itgax, CD11c) and colony stimulating factor 1 receptor (Csf1r, CD115) expression fails to discriminate dendritic cells from macrophages. Immunobiology 2011; 216:1228-37; PMID:21885153; http://dx.doi.org/10.1016/j. imbio.2011.08.006.
47. Hume DA. Macrophages as APC and the dendritic cell myth. J Immunol 2008; 181:5829-35; PMID:18941170.
48. Mabbott NA, Kenneth Baillie J, Hume DA, Freeman TC. Meta-analysis of lineage-specific gene expression signatures in mouse leukocyte populations. Immunobiology 2010; 215:724-36; PMID:20580463; http://dx.doi.org/10.1016/j. imbio.2010.05.012.
49. Austin JM. Dendritic Cells in Spleen and Lymph Node. In: Lotze MT, Thomson AW, Eds. Dendritic Cells Biology and Clinical Applications: Academic Press 1999; 179-204.
50. Valladeau J, Duvert-Frances V, Pin JJ, Dezutter-Dambuyant C, Vincent C, Massacrier C, et al. The monoclonal antibody DCGM4 recognizes Langerin, a protein specific of Langerhans cells, and is rapidly internalized from the cell surface. Eur J Immunol 1999; 29:2695-704; PMID:10508244; http://dx.doi.org/10. 1002/(SICI)1521-4141(199909)29:09〈2695::AIDIMMU2695〉3.0.CO;2-Q.
51. Valladeau J, Ravel O, Dezutter-Dambuyant C, Moore K, Kleijmeer M, Liu Y, et al. Langerin, a novel C-type lectin specific to Langerhans cells, is an endocytic receptor that induces the formation of Birbeck granules. Immunity 2000; 12:71-81; PMID:10661407; http://dx.doi.org/10.1016/S1074-7613(00)80160-0.
52. Takahara K, Omatsu Y, Yashima Y, Maeda Y, Tanaka S, Iyoda T, et al. Identification and expression of mouse Langerin (CD207) in dendritic cells. Int Immunol 2002; 14:433-44; PMID:11978773; http://dx.doi.org/10.1093/intimm/14.5. 433.
53. Valladeau J, Clair-Moninot V, Dezutter-Dambuyant C, Pin JJ, Kissenpfennig A, Mattéi MG, et al. Identification of mouse langerin/CD207 in Langerhans cells and some dendritic cells of lymphoid tissues. J Immunol 2002; 168:782-92; PMID:11777972.
54. Probst HC, Tschannen K, Odermatt B, Schwendener R, Zinkernagel RM, Van Den Broek M. Histological analysis of CD11c-DTR/GFP mice after in vivo depletion of dendritic cells. Clin Exp Immunol 2005; 141:398-404; PMID:16045728; http://dx.doi.org/10.1111/j.1365-2249.2005.02868.x.
55. + T cells by exogenous cell-associated antigens. Immunity 2002; 17:211-20; PMID:12196292; http://dx.doi.org/10.1016/S1074-7613(02)00365-5.
56. Sallusto F, Cella M, Danieli C. Dendritic cells use macropinocytosis and the mannose receptor to concentrate macromolecules in the major histocompatibility complex class II compartment: downregulation by cytokines and bacterial products. J Exp Med 1995; 182:389-400; PMID:7629494; http://dx.doi.org/10.1084/jem.182.2.389.
57. Steinman RM. The dendritic cell system and its role in immunogenicity. Annu Rev Immunol 1991; 9:271-96; PMID:1910679; http://dx.doi.org/10.1146/ annurev.iy.09.040191.001415.
58. MacPherson G, Kushnir N, Wykes M. Dendritic cells, B cells and the regulation of antibody synthesis. Immunol Rev 1999; 172:325-34; PMID:10631957; http://dx.doi.org/10.1111/j.1600-065X.1999.tb01376.x.
59. Huang FP, Farquhar CF, Mabbott NA, Bruce ME, MacPherson GG. Migrating intestinal dendritic cells transport PrP(Sc) from the gut. J Gen Virol 2002; 83:267-71; PMID:11752724.
60. Luhr KM, Wallin RPA, Ljunggren HG, Löw P, Taraboulos A, Kristensson K. Processing and degradation of exogenous prion protein by CD11c(+) myeloid dendritic cells in vitro. J Virol 2002; 76:12259-64; PMID:12414965; http://dx.doi.org/10.1128/JVI.76.23.12259-64.2002.
61. Lai L, Alaverdi N, Maltais L, Morse HC, 3rd. Mouse cell surface antigens: nomenclature and immunophenotyping. J Immunol 1998; 160:3861-8; PMID:9558091.
62. Kaneider NC, Kaser A, Dunzendorfer S, Tilg H, Wiedermann CJ. Sphingosine kinase-dependent migration of immature dendritic cells in response to neurotoxic prion protein fragment. J Virol 2003; 77:5535-9; PMID:12692258; http://dx.doi.org/10.1128/JVI.77.9.5535-9.2003.
63. + dendritic cells delays lymphoinvasion after intraperitonal scrapie infection. J Virol 2008; 244-7.
64. + dendritic cell subset in transmission of prions. J Virol 2007; 81:4877-80; PMID:17301133; http://dx.doi.org/10.1128/JVI.02345-06.
65. + cells impairs scrapie agent neuroinvasion from the intestine. J Immunol 2007; 179:7758-66; PMID:18025222.
66. Levavasseur E, Metharom P, Dorban G, Nakano H, Kakiuchi T, Carnaud C, et al. Experimental scrapie in 'plt' mice: an assessment of the role of dendritic-cell migration in the pathogenesis of prion diseases. J Gen Virol 2007; 88:2353-60; PMID:17622642; http://dx.doi.org/10.1099/vir.0.82816-0.
67. Glaysher BR, Mabbott NA. Role of the draining lymph node in scrapie agent transmission from the skin. Immunol Lett 2007; 109:64-71; PMID:17292972; http://dx.doi.org/10.1016/j.imlet.2007.01.003.
68. Mohan J, Brown KL, Farquhar CF, Bruce ME, Mabbott NA. Scrapie transmission following exposure through the skin is dependent on follicular dendritic cells in lymphoid tissues. J Dermatol Sci 2004; 35:101-11; PMID:15265522; http://dx.doi.org/10.1016/j.jdermsci.2004.05.005.
69. Mohan J, Bruce ME, Mabbott NA. Neuroinvasion by scrapie following inoculation via the skin is independent of migratory Langerhans cells. J Virol 2005; 79:1888-97; PMID:15650212; http://dx.doi.org/10.1128/JVI.79.3.1888-97. 2005.
70. Taylor DM, McConnell I, Fraser H. Scrapie infection can be established readily through skin scarification in immunocompetent but not immunodeficient mice. J Gen Virol 1996; 77:1595-9; PMID:8758004; http://dx.doi.org/10.1099/0022- 1317-77-7-1595.
71. Bartz JC, Kincaid AE, Bessen RA. Rapid prion neuroinvasion following tongue infection. J Virol 2003; 77:583-91; PMID:12477862; http://dx.doi.org/10. 1128/JVI.77.1.583-91.2003.
72. Carp RI. Transmission of scrapie by oral route: effect of gingival scarification. Lancet 1982; 1:170-1; PMID:6119548; http://dx.doi.org/10.1016/ S0140-6736(82)90421-4.
73. Denkers ND, Telling GC, Hoover EA. Minor oral lesions facilitate transmission of chronic wasting disease. J Virol 2011; 85:1396-9; PMID:21084472; http://dx.doi.org/10.1128/JVI.01655-10.
74. Cunningham AA, Kirkwood JK, Dawson M, Spencer YI, Green RB, Wells GAH. Bovine spongiform encephalopathy infectivity in greater kudu (Tragelaphus strepsiceros). Emerg Infect Dis 2004; 10:1044-9; PMID:15207051.
75. Notari S, Moleres FJ, Hunter SB, Belay ED, Schonberger LB, Cali I, et al. Multiorgan detection and characterization of protease-resistant prion protein in a case of variant CJD examined in the United States. PLoS One 2010; 5:8765; PMID:20098730; http://dx.doi.org/10.1371/journal.pone.0008765.
76. Sc in the skin of animals with experimental and natural scrapie. PLoS Pathog 2007; 3:66; PMID:17530923; http://dx.doi.org/10.1371/journal.ppat.0030066.
77. Angers RC, Seward TS, Napier D, Green M, Hoover EA, Spraker T, et al. Chronic wasting disease prions in elk antler velvet. Emerg Infect Dis 2009; 15:696-703; PMID:19402954; http://dx.doi.org/10.3201/eid1505.081458.
78. de Jong MAWP, Geijtenbeek TBH. Langerhans cells in innate defense against pathogens. Trends Immunol 2010; 31:452-9; PMID:21030306; http://dx.doi.org/10. 1016/j.it.2010.08.002.
79. Wu SJL, Grouard-Vogel G, Sun W, Mascola JR, Brachtel E, Putvatana R, et al. Human skin Langerhans cells are targets of dengue virus infection. Nat Med 2000; 6:816-20; PMID:10888933; http://dx.doi.org/10.1038/77553.
80. Mohan J, Bruce ME, Mabbott NA. Follicular dendritic cell dedifferentiation reduces scrapie susceptibility following inoculation via the skin. Immunology 2005; 114:225-34; PMID:15667567; http://dx.doi.org/10.1111/j. 1365-2567.2004.02074.x.
81. Gossner A, Hunter N, Hopkins J. Role of lymph-borne cells in the early stages of scrapie agent dissemination from the skin. Vet Immunol Immunopathol 2006; 109:267-78; PMID:16169089; http://dx.doi.org/10.1016/j.vetimm.2005.08.021.
82. Mohan J, Hopkins J, Mabbott NA. Skin-derived dendritic cells acquire and degrade the scrapie agent following in vitro exposure. Immunology 2005; 116:122-33; PMID:16108824; http://dx.doi.org/10.1111/j.1365-2567.2005.02207.x.
83. Kissenpfennig A, Henri S, Dubois B, Laplace-BuilhéC, Perrin P, Romani N, et al. Dynamics and function of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 2005; 22:643-54; PMID:15894281; http://dx.doi.org/10. 1016/j.immuni.2005.04.004.
84. Flacher V, Douillard P, Aït-Yahia S, Stoitzner P, Clair-Moninot V, Romani N, et al. Expression of langerin/CD207 reveals dendritic cell heterogeneity between inbred mouse strains. Immunology 2008; 123:339-47; PMID:18217955; http://dx.doi.org/10.1111/j.1365-2567.2007.02785.x.
85. + dendritic cells. J Exp Med 2007; 204:3147-56; PMID:18086865; http://dx.doi.org/10.1084/ jem.20071966.
86. + dendritic cells survey the skin in the steady state. J Exp Med 2007; 204:3133-46; PMID:18086862; http://dx.doi.org/10. 1084/jem.20071733.
87. + dendritic cells that develop and function independently of epidermal Langerhans cells. J Exp Med 2007; 204:3119-31; PMID:18086861; http://dx.doi.org/10.1084/jem.20071724.
88. Bennett CL, van Rijn E, Jung S, Inaba K, Steinman RM, Kapsenberg ML, et al. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J Cell Biol 2005; 169:569-76; PMID:15897263; http://dx.doi.org/10.1083/jcb.200501071.
89. Nagao K, Ginhoux F, Leitner WW, Motegi SI, Bennett CL, Clausen BE, et al. Murine epidermal Langerhans cells and langerin-expressing dermal dendritic cells are unrelated and exhibit distinct functions. Proc Natl Acad Sci USA 2009; 106:3312-7; PMID:19218433; http://dx.doi.org/10.1073/pnas.0807126106.
90. + dermal dendritic cells cross-present keratinocyte-derived antigens irrespective of the presence of Langerhans cells. J Exp Med 2010; 207:189-206; PMID:20038600; http://dx.doi.org/10.1084/jem. 20091964.
91. Gousset K, Schiff E, Langevin C, Marijanovic Z, Caputo A, Browman DT, et al. Prions hijack tunnelling nanotubes for intercellular spread. Nat Cell Biol 2009; 11:328-36; PMID:19198598; http://dx.doi.org/10.1038/ncb1841.
92. Raymond CR, Mabbott NA. Assessing the involvement of migratory dendritic cells in the transfer of the scrapie agent from the immune to peripheral nervous systems. J Neuroimmunol 2007; 187:114-25; PMID:17561271; http://dx.doi.org/10. 1016/j.jneuroim.2007.05.006.
93. Aucouturier P, Geissmann F, Damotte D, Saborio GP, Meeker HC, Kascsak R, et al. Infected splenic dendritic cells are sufficient for prion transmission to the CNS in mouse scrapie. J Clin Invest 2001; 108:703-8; PMID:11544275.
94. Glatzel M, Heppner FL, Albers KM, Aguzzi A. Sympathetic innervation of lymphoreticular organs is rate limiting for prion neuroinvasion. Neuron 2001; 31:25-34; PMID:11498048; http://dx.doi.org/10.1016/S0896-6273(01)00331-2.
95. Sisó S, Jeffrey M, González L. Neuroinvasion in sheep transmissible spongiform encephalopathies: the role of the haematogenous route. Neuropathol Appl Neurobiol 2009; 35:232-46; PMID:19473292; http://dx.doi.org/10. 1111/j.1365-2990.2008.00978.x.
96. Delamarre L, Pack M, Chang H, Mellman I, Trombetta ES. Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005; 307:1630-4; PMID:15761154; http://dx.doi.org/10.1126/science. 1108003.
97. Bergtold A, Desai DD, Gavhane A, Clynes R. Cell surface recycling of internalized antigen permits dendritic cell priming of B cells. Immunity 2005; 23:503-14; PMID:16286018; http://dx.doi.org/10.1016/j.immuni.2005.09.013.
98. Wykes M, Pombo A, Jenkins C, MacPherson GG. Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J Immunol 1998; 161:1313-9; PMID:9686593.
99. Carp RI, Callahan SM. In vitro interaction of scrapie agent and mouse peritoneal macrophages. Intervirology 1981; 16:8-13; PMID:6799420; http://dx.doi.org/10.1159/000149241.
100. Carp RI, Callahan SM. Effect of mouse peritoneal macrophages on scrapie infectivity during extended in vitro incubation. Intervirology 1982; 17:201-7; PMID:6813286; http://dx.doi.org/10.1159/000149289.
101. Sassa Y, Inoshima Y, Ishiguro N. Bovine macrophage degradation of scrapie and BSE PrPSc. Vet Immunol Immunopathol 2010; 133:33-9; PMID:19647878; http://dx.doi.org/10.1016/j.vetimm.2009.06.018.
102. Beringue V, Demoy M, Lasmézas CI, Gouritin B, Weingarten C, Deslys JP, et al. Role of spleen macrophages in the clearance of scrapie agent early in pathogenesis. J Pathol 2000; 190:495-502; PMID:10700001; http://dx.doi.org/ 10.1002/(SICI)1096-9896(200003)190:4〈495::AID-PATH535〉3.0.CO;2-T.
103. Sassa Y, Yamasaki T, Horiuchi M, Inoshima Y, Ishiguro N. The effects of lysosomal and proteasomal inhibitors on abnormal forms of prion protein degradation in murine macrophages. Microbiol Immunol 2010; 54:763-8; PMID:21223366; http://dx.doi.org/10.1111/j.1348-0421.2010.00272.x.
104. Takakura I, Miyazawa K, Kanaya T, Itani W, Watanabe K, Ohwada S, et al. Orally administered prion protein is incorporated by m cells and spreads into lymphoid tissues with macrophages in prion protein knockout mice. Am J Pathol 2011; 179:1301-9; PMID:21763679; http://dx.doi.org/10.1016/j.ajpath.2011.05.058.
105. Swartzendruber DC, Congdon CC. ELECTRON MICROSCOPE OBSERVATIONS ON TINGIBLE BODY MACROPHAGES IN MOUSE SPLEEN. J Cell Biol 1963; 19:641-6; PMID:14086143; http://dx.doi.org/10.1083/jcb.19.3.641.
106. Jeffrey M, Martin S, Thomson JR, Dingwall WS, Begara-McGorum I, González L. Onset and distribution of tissue prp accumulation in scrapie-affected suffolk sheep as demonstrated by sequential necropsies and tonsillar biopsies. J Comp Pathol 2001; 125:48-57; PMID:11437516; http://dx.doi.org/10.1053/jcpa.2001.0476.
107. Jeffrey M, McGovern G, Martin S, Goodsir CM, Brown KL. Cellular and sub-cellular localisation of PrP in the lymphoreticular system of mice and sheep. Arch virol Supp 2000; 16:23-8.
108. Ryder SJ, Dexter GE, Heasman L, Warner R, Moore SJ. Accumulation and dissemination of prion protein in experimental sheep scrapie in the natural host. BMC Vet Res 2009; 5:9; PMID:19243608; http://dx.doi.org/10.1186/1746-6148- 5-9.
109. Hilton DA, Ghani AC, Conyers L, Edwards P, McCardle L, Ritchie D, et al. Prevalence of lymphoreticular prion protein accumulation in UK tissue samples. J Pathol 2004; 203:733-9; PMID:15221931; http://dx.doi.org/10.1002/path.1580.
110. Rezaie P, Lantos PL. Microglia and the pathogenesis of spongiform encephalopathies. Brain Res Brain Res Rev 2001; 35:55-72; PMID:11245886; http://dx.doi.org/10.1016/S0165-0173(01)00042-X.
111. Perry VH, Cunningham C, Boche D. Atypical inflammation in the central nervous system in prion disease. Curr Opin Neurol 2002; 15:349-54; PMID:12045736; http://dx.doi.org/10.1097/00019052-200206000-00020.
112. Rezaie P, Al-Sarraj S. Vacuolar degeneration affecting brain macrophages/microglia in variant CJD: a report on two cases. Acta Neuropathol 2007; 114:651-8; PMID:17943296; http://dx.doi.org/10.1007/s00401-007-0294-6.
113. Kovács GG, Preusser M, Strohschneider M, Budka H. Subcellular localization of disease-associated prion protein in the human brain. Am J Pathol 2005; 166:287-94; PMID:15632020; http://dx.doi.org/10.1016/S0002-9440(10)62252- 3.
114. Ciesielski-Treska J, Grant NJ, Ulrich G, Corrotte M, Bailly Y, Haeberle AM, et al. Fibrillar prion peptide (106-126) and scrapie prion protein hamper phagocytosis in microglia. Glia 2004; 46:101-15; PMID:15042579; http://dx.doi.org/10.1002/glia.10363.
115. Hughes MM, Field RH, Perry VH, Murray CL, Cunningham C. Microglia in the degenerating brain are capable of phagocytosis of beads and of apoptotic cells, but do not efficiently remove PrPSc, even upon LPS stimulation. Glia 2010; 58:2017-30; PMID:20878768; http://dx.doi.org/10.1002/glia.21070.
116. Boche D, Cunningham C, Docagne F, Scott H, Perry VH. TGFbeta1 regulates the inflammatory response during chronic neurodegeneration. Neurobiol Dis 2006; 22:638-50; PMID:16510291; http://dx.doi.org/10.1016/j.nbd.2006.01.004.
117. Perry VH, Cunningham C, Holmes C. Systemic infections and inflammation affect chronic neurodegeneration. Nat Rev Immunol 2007; 7:161-7; PMID:17220915; http://dx.doi.org/10.1038/nri2015.
118. Bulloch K, Miller MM, Gal-Toth J, Milner TA, Gottfried-Blackmore A, Waters EM, et al. CD11c/EYFP transgene illuminates a discrete network of dendritic cells within the embryonic, neonatal, adult and injured mouse brain. J Comp Neurol 2008; 508:687-710; PMID:18386786; http://dx.doi.org/10.1002/cne. 21668.
119. Phan TG, Green JA, Gray EE, Xu Y, Cyster JG. Immune complex relay by subcapsular sinus macrophages and noncognate B cells drives antibody affinity maturation. Nat Immunol 2009; 10:786-93; PMID:19503106; http://dx.doi.org/10. 1038/ni.1745.
120. Phan TG, Grigorova I, Okada T, Cyster JG. Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat Immunol 2007; 8:992-1000; PMID:17660822; http://dx.doi.org/10.1038/ni1494.
121. Carrasco YR, Batista FD. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 2007; 27:160-71; PMID:17658276; http://dx.doi.org/10.1016/j.immuni.2007.06.007.
122. Junt T, Moseman EA, Iannacone M, Massberg S, Lang PA, Boes M, et al. Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 2007; 450:110-4; PMID:17934446; http://dx.doi.org/10.1038/nature06287.
123. Roozendaal R, Mempel TR, Pitcher LA, Gonzalez SF, Verschoor A, Mebius RE, et al. Conduits mediate transport of low-molecular-weight antigen to lymph node follicles. Immunity 2009; 30:264-76; PMID:19185517; http://dx.doi.org/10.1016/ j.immuni.2008.12.014.
124. Jeffrey M, González L, Espenes A, Press CM, Martin S, Chaplin M, et al. Transportation of prion protein across the intestinal mucosa of scrapie-susceptible and scrapie-resistant sheep. J Pathol 2006; 209:4-14; PMID:16575799; http://dx.doi.org/10.1002/path.1962.
125. Ligios C, Cancedda MG, Carta A, Santucciu C, Maestrale C, Demontis F, et al. Sheep with scrapie and mastitis transmit infectious prions through the milk. J Virol 2011; 85:1136-9; PMID:21084475; http://dx.doi.org/10.1128/JVI.02022-10.
126. Farquhar CF, Somerville RA, Ritchie LA. Post-mortem immunodiagnosis of scrapie and bovine spongiform encephalopathy. J Virol Methods 1989; 24:215-21; PMID:2569471; http://dx.doi.org/10.1016/0166-0934(89)90023-2.