PrPSc is associated with B cells in the blood of scrapie-infected sheep

Virology

Volumn 405, Issue 1, 2010, Pages 110-119

  Edwards, Jane C ^a   Moore, S Jo ^a   Hawthorn, Jeremy A ^a   Neale, Michael H ^a   Terry, Linda A ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

B cells; Blood; Immunoassay; Prion; PrPSc; Scrapie

Indexed keywords

CD11B ANTIGEN; CELL SURFACE IMMUNOGLOBULIN; COMPLEMENT COMPONENT C3D RECEPTOR; GLYCOPROTEIN P 15095; HLA DQ ANTIGEN; L SELECTIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PRION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; CORRELATIONAL STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; NONHUMAN; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SCRAPIE; SHEEP; SHEEP DISEASE; TARGET CELL;

OVIS ARIES;

EID: 77955510888     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2010.05.023     Document Type: Article

References (77)

1. Sc in gut-associated lymphoid and nervous tissues of susceptible sheep from a Romanov flock with natural scrapie. J. Gen. Virol. 2000, 81:3115-3126.
2. Aucouturier P., Carnaud C. The immune system and prion diseases: a relationship of complicity and blindness. J. Leukoc. Biol. 2002, 72(6):1075-1083.
3. Aucouturier P., Geissmann F., Damotte D., Saborio G.P., Meeker H.C., Kascsak R., Kascsak R., Carp R.I., Wisniewski T. Infected splenic dendritic cells are sufficient for prion transmission to the CNS in mouse scrapie. J. Clin. Investig. 2001, 108(5):703-708.
4. Barclay G.R., Houston E.F., Halliday S.I., Farquhar C.F., Turner M.L. Comparative analysis of normal prion protein expression on human, rodent, and ruminant blood cells by using a panel of prion antibodies. Transfusion 2002, 42(5):517-526.
5. Bazin H., Gray D., Platteau B., MacLennan I.C. Distinct delta + and delta - B-lymphocyte lineages in the rat. Ann. N.Y. Acad. Sci. 1982, 399:157-174.
6. Bonneau M., Epardaud M., Payot F., Niborski V., Thoulouze M.I., Bernex F., Charley B., Riffault S., Guilloteau L.A., Schwartz-Cornil I. Migratory monocytes and granulocytes are major lymphatic carriers of Salmonella from tissue to draining lymph node. J. Leukoc. Biol. 2006, 79(2):268-276.
7. Brown P. B lymphocytes and neuroinvasion. Nature 1997, 390(6661):662-663.
8. 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(11):1308-1312.
9. Brown P., Cervenakova L., Diringer H. Blood infectivity and the prospects for a diagnostic screening test in Creutzfeldt-Jakob disease. J. Lab. Clin. Med. 2001, 137(1):5-13.
10. Bueler H., Aguzzi A., Sailer A., Greiner R.A., Autenried P., Aguet M., Weissmann C. Mice devoid of PrP are resistant to scrapie. Cell 1993, 73(7):1339-1347.
11. Castilla J., Saa P., Soto C. Detection of prions in blood. Nat. Med. 2005, 11(9):982-985.
12. Chevallier N., Berthelemy M., Laine V., Le Rhun D., Femenia F., Polack B., Naessens J., Levy D., Schwartz-Cornil I. B-1-like cells exist in sheep. Characterization of their phenotype and behaviour. Immunology 1998, 95(2):178-184.
13. Choi E.M., Geschwind M.D., Deering C., Pomeroy K., Kuo A., Miller B.L., Safar J.G., Prusiner S.B. Prion proteins in subpopulations of white blood cells from patients with sporadic Creutzfeldt-Jakob disease. Lab. Invest. 2009, 89(6):624-635.
14. Diringer H. Sustained viremia in experimental hamster scrapie. Brief report. Arch. Virol. 1984, 82(1-2):105-109.
15. Dutia B.M., McConnell I., Bird K., Keating P., Hopkins J. Patterns of major histocompatibility complex class II expression on T cell subsets in different immunological compartments: 1. Expression on resting T cells. Eur. J. Immunol. 1993, 23(11):2882-2888.
16. Flores-Langarica A., Sebti Y., Mitchell D.A., Sim R.B., MacPherson G.G. Scrapie pathogenesis: the role of complement C1q in scrapie agent uptake by conventional dendritic cells. J. Immunol. 2009, 182(3):1305-1313.
17. Freudenthal P.S., Bhardwaj N. Dendritic cells in human blood and synovial exudates. Int. Rev. Immunol. 1990, 6(2-3):103-116.
18. Frigg R., Klein M.A., Hegyi I., Zinkernagel R.M., Aguzzi A. Scrapie pathogenesis in subclinically infected B-cell-deficient mice. J. Virol. 1999, 73(11):9584-9588.
19. Gregori L., Rohwer R.G. Characterization of scrapie-infected and normal hamster blood as an experimental model for TSE-infected human blood. Dev. Biol. (Basel) 2007, 127:123-133.
20. Gregori L., Gurgel P.V., Lathrop J.T., Edwardson P., Lambert B.C., Carbonell R.G., Burton S.J., Hammond D.J., Rohwer R.G. Reduction in infectivity of endogenous transmissible spongiform encephalopathies present in blood by adsorption to selective affinity resins. Lancet 2006, 368(9554):2226-2230.
21. Gregori L., Lambert B.C., Gurgel P.V., Gheorghiu L., Edwardson P., Lathrop J.T., Macauley C., Carbonell R.G., Burton S.J., Hammond D., Rohwer R.G. Reduction of transmissible spongiform encephalopathy infectivity from human red blood cells with prion protein affinity ligands. Transfusion 2006, 46(7):1152-1161.
22. Gupta V.K., McConnell I., Hopkins J. Reactivity of the CD11/CD18 workshop monoclonal antibodies in the sheep. Vet. Immunol. Immunopathol. 1993, 39(1-3):93-102.
23. Gupta V.K., McConnell I., Dalziel R.G., Hopkins J. Identification of the sheep homologue of the monocyte cell surface molecule CD14. Vet. Immunol. Immunopathol. 1996, 51(1-2):89-99.
24. Gupta V.K., McConnell I., Dalziel R.G., Hopkins J. Two B cell subpopulations have distinct recirculation characteristics. Eur. J. Immunol. 1998, 28(5):1597-1603.
25. C on cellular components of sheep blood. J. Gen. Virol. 2005, 86(Pt 5):1571-1579.
26. Herrmann L.M., Davis W.C., Knowles D.P., Wardrop K.J., Sy M.S., Gambetti P., ORourke K.I. Cellular prion protein is expressed on peripheral blood mononuclear cells but not platelets of normal and scrapie-infected sheep. Haematologica 2001, 86(2):146-153.
27. Herzenberg L.A., Tung J.W. B cell lineages: documented at last!. Nat. Immunol. 2006, 7(3):225-226.
28. Hewitt P. vCJD and blood transfusion in the United Kingdom. Transfus. Clin. Biol. 2006, 13(5):312-316.
29. Holada K., Vostal J.G., Theisen P.W., MacAuley C., Gregori L., Rohwer R.G. Scrapie infectivity in hamster blood is not associated with platelets. J. Virol. 2002, 76(9):4649-4650.
30. Hopkins J., Dutia B.M., McConnell I. Monoclonal antibodies to sheep lymphocytes. I. Identification of MHC class II molecules on lymphoid tissue and changes in the level of class II expression on lymph-borne cells following antigen stimulation in vivo. Immunology 1986, 59(3):433-438.
31. Houston F., Foster J.D., Chong A., Hunter N., Bostock C.J. Transmission of BSE by blood transfusion in sheep. Lancet 2000, 356(9234):999-1000.
32. Houston F., McCutcheon S., Goldmann W., Chong A., Foster J., Siso S., Gonzalez L., Jeffrey M., Hunter N. Prion diseases are efficiently transmitted by blood transfusion in sheep. Blood 2008, 112(12):4739-4745.
33. Howard C.J., Naessens J. Summary of workshop findings for cattle. Vet. Immunol. Immunopathol. 1993, 39(1-3):25-47.
34. Howard C.J., Morrison W.I., Bensaid A., Davis W., Eskra L., Gerdes J., Hadam M., Hurley D., Leibold W., Letesson J.J., et al. Summary of workshop findings for leukocyte antigens of cattle. Vet. Immunol. Immunopathol. 1991, 27(1-3):21-27.
35. HPA 4th case of variant CJD infection associated with blood transfusion 2007, http://www.hpa.org.uk/hpa/news/articles/press_releases/2007/070118_vCJD.htm.
36. sc from the gut. J. Gen. Virol. 2002, 83:267-271.
37. Hunter N., Foster J., Chong A., McCutcheon S., Parnham D., Eaton S., MacKenzie C., Houston F. Transmission of prion diseases by blood transfusion. J. Gen. Virol. 2002, 83:2897-2905.
38. Jeffrey M., Gonzalez L. Classical sheep transmissible spongiform encephalopathies: pathogenesis, pathological phenotypes and clinical disease. Neuropathol. Appl. Neurobiol. 2007, 33(4):373-394.
39. Kaeser P.S., Klein M.A., Schwarz P., Aguzzi A. Efficient lymphoreticular prion propagation requires PrP(c) in stromal and hematopoietic cells. J. Virol. 2001, 75(15):7097-7106.
40. Kearney J.F. Innate-like B cells. Springer Semin. Immunopathol. 2005, 26(4):377-383.
41. Klein M.A., Frigg R., Flechsig E., Raeber A.J., Kalinke U., Bluethmann H., Bootz F., Suter M., Zinkernagel R.M., Aguzzi A. A crucial role for B-cells in neuroinvasive scrapie. Nature 1997, 390(6661):687-690.
42. Klein M.A., Frigg R., Raeber A.J., Flechsig E., Hegyi I., Zinkernagel R.M., Weissmann C., Aguzzi A. PrP expression in B lymphocytes is not required for prion neuroinvasion. Nat. Med. 1998, 4(12):1429-1433.
43. Sc)-specific epitope defined by a monoclonal antibody. Nature 1997, 390(6655):74-77.
44. Levavasseur E., Metharom P., Dorban G., Nakano H., Kakiuchi T., Carnaud C., Sarradin P., Aucouturier P. 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(Pt 8):2353-2360.
45. Llewelyn C.A., Hewitt P.E., Knight R.S.G., Amar K., Cousens S., Mackenzie J., Will R.G. Possible transmission of variant Creutzfeldt-Jakob disease by blood transfusion. Lancet 2004, 363(9407):417-421.
46. Luhr K.M., Wallin R.P.A., Ljunggren H.G., Low P., Taraboulos A., Kristensson K. Processing and degradation of exogenous prion protein by CD11c(+) myeloid dendritic cells in vitro. J. Virol. 2002, 76(23):12259-12264.
47. Mabbott N.A., Bruce M.E., Botto M., Walport M.J., Pepys M.B. Temporary depletion of complement component C3 or genetic deficiency of C1q significantly delays onset of scrapie. Nat. Med. 2001, 7(4):485-487.
48. Mackay C.R., Beya M.F., Matzinger P. Gamma/delta T cells express a unique surface molecule appearing late during thymic development. Eur. J. Immunol. 1989, 19(8):1477-1483.
49. Manuelidis E.E., Gorgacs E.J., Manuelidis L. Viremia in experimental Creutzfeldt-Jakob disease. Science 1978, 200(4345):1069-1071.
50. Mathiason C.K., Hays S.A., Powers J., Hayes-Klug J., Langenberg J., Dahmes S.J., Osborn D.A., Miller K.V., Warren R.J., Mason G.L., Hoover E.A. Infectious prions in pre-clinical deer and transmission of chronic wasting disease solely by environmental exposure. PLoS ONE 2009, 4(6):e5916.
51. Munro J.M., Briscoe D.M., Tedder T.F. Differential regulation of leucocyte L-selectin (CD62L) expression in normal lymphoid and inflamed extralymphoid tissues. J. Clin. Pathol. 1996, 49(9):721-727.
52. Murayama Y., Yoshioka M., Okada H., Takata M., Yokoyama T., Mohri S. Urinary excretion and blood level of prions in scrapie-infected hamsters. J. Gen. Virol. 2007, 88(Pt 10):2890-2898.
53. Naessens J., Newson J., McHugh N., Howard C.J., Parsons K., Jones B. Characterization of a bovine leucocyte differentiation antigen of 145,000 MW restricted to B lymphocytes. Immunology 1990, 169(4):525-530.
54. Naessens J., Olubayo R.O., Davis W.C., Hopkins J. Cross-reactivity of workshop antibodies with cells from domestic and wild ruminants. Vet. Immunol. Immunopathol. 1993, 39(1-3):283-290.
55. Paramithiotis E., Pinard M., Lawton T., LaBoissiere S., Leathers V.L., Zou W.Q., Estey L.A., Lamontagne J., Lehto M.T., Kondejewski L.H., Francoeur G.P., Papadopoulos M., Haghighat A., Spatz S.J., Head M., Will R., Ironside J., ORourke K., Tonelli Q., Ledebur H.C., Chakrabartty A., Cashman N.R. A prion protein epitope selective for the pathologically misfolded conformation. Nat. Med. 2003, 9(7):893-899.
56. Peden A.H., Head M.W., Ritchie D.L., Bell J.E., Ironside J.W. Preclinical vCJD after blood transfusion in a PRNP codon 129 heterozygous patient. Lancet 2004, 364(9433):527-529.
57. Prusiner S.B. Prions. Proc. Natl. Acad. Sci. USA 1998, 95(23):13363-13383.
58. Puri N.K., Mackay C.R., Brandon M.R. Sheep lymphocyte antigens (OLA). II. Major histocompatibility complex class II molecules. Immunology 1985, 56(4):725-733.
59. Randolph G.J., Ochando J., Partida-Sanchez S. Migration of dendritic cell subsets and their precursors. Annu. Rev. Immunol. 2008, 26:293-316.
60. 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(11):7758-7766.
61. Rocchi M.S., Anderson M.J., Eaton S.L., Hamilton S., Finlayson J., Steele P., Barclay G.R., Chianini F. Three-colour flow cytometric detection of PrP in ovine leukocytes. Vet. Immunol. Immunopathol. 2007, 116(3-4):172-181.
62. Saa P., Castilla J., Soto C. Presymptomatic detection of prions in blood. Science 2006, 313(5783):92-94.
63. Sethi S., Kerksiek K.M., Brocker T., Kretzschmar H. Role of the CD8+ dendritic cell subset in transmission of prions. J. Virol. 2007, 81(9):4877-4880.
64. Sopp P., Howard C.J. IFN gamma and IL-4 production by CD4, CD8 and WC1 gamma delta TCR(+) T cells from cattle lymph nodes and blood. Vet. Immunol. Immunopathol. 2001, 81(1-2):85-96.
65. Sc accumulation and innervation of splenic compartments in sheep experimentally infected with scrapie. PLoS ONE 2009, 4(9):e6885.
66. Tang M.L., Steeber D.A., Zhang X.Q., Tedder T.F. Intrinsic differences in L-selectin expression levels affect T and B lymphocyte subset-specific recirculation pathways. J. Immunol. 1998, 160(10):5113-5121.
67. Tayebi M., Enever P., Sattar Z., Collinge J., Hawke S. Disease-associated prion protein elicits immunoglobulin M responses in vivo. Mol. Med. 2004, 10(7-12):104-111.
68. sc in blood from sheep infected with the scrapie and bovine spongiform encephalopathy agents. J. Virol. 2009, 83(23):12552-12558.
69. Thackray A.M., Fitzmaurice T.J., Hopkins L., Bujdoso R. Ovine plasma prion protein levels show genotypic variation detected by C-terminal epitopes not exposed in cell-surface PrPC. Biochem. J. 2006, 400:349-358.
70. Sc derived from the brain and blood of sheep infected with scrapie. J. Gen. Virol. 2008, 89(Pt 12):3177-3184.
71. Tung J.W., Mrazek M.D., Yang Y., Herzenberg L.A. Phenotypically distinct B cell development pathways map to the three B cell lineages in the mouse. Proc. Natl. Acad. Sci. USA 2006, 103(16):6293-6298.
72. van Keulen L.J., Schreuder B.E., Meloen R.H., Mooij-Harkes G., Vromans M.E., Langeveld J.P.M. Immunohistochemical detection of prion protein in lymphoid tissues of sheep with natural scrapie. J. Clin. Microbiol. 1996, 34(5):1228-1231.
73. van Keulen L.J., Vromans M.E., van Zijderveld F.G. Early and late pathogenesis of natural scrapie infection in sheep. APMIS 2006, 110:23-32.
74. von Poser-Klein C., Flechsig E., Hoffmann T., Schwarz 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(7):3791-3795.
75. Wroe S.J., Pal S., Siddique D., Hyare H., Macfarlane R., Joiner S., Linehan J.M., Brandner S., Wadsworth J.D., Hewitt P., Collinge J. Clinical presentation and pre-mortem diagnosis of variant Creutzfeldt-Jakob disease associated with blood transfusion: a case report. Lancet 2006, 368(9552):2061-2067.
76. Young A.J., Marston W.L., Dessing M., Dudler L., Hein W.R. Distinct recirculating and non-recirculating B-lymphocyte pools in the peripheral blood are defined by coordinated expression of CD21 and L-selectin. Blood 1997, 90(12):4865-4875.
77. Young A.J., Dudler L., Yamaguchi K., Marston W., Hein W.R. Structure and expression of ovine complement receptor type 2. Vet. Immunol. Immunopathol. 1999, 72:67-72.