Reaction of complement factors varies with prion strains in vitro and in vivo

Virology

Volumn 423, Issue 2, 2012, Pages 205-213

  Hasebe, Rie ^a,b   Raymond, Gregory J ^a   Horiuchi, Motohiro ^b   Caughey, Byron ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Complement factors; Prion; Scrapie; Strain difference

Indexed keywords

BINDING PROTEIN; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C9; LIPOCORTIN 5; PHOSPHATIDYLSERINE BINDING PROTEIN; POLYCLONAL ANTIBODY; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CULTURE; COMPLEMENT DEPOSITION; CONTROLLED STUDY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRION; PRION DISEASE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SCRAPIE AGENT; STRAIN DIFFERENCE; VIRUS STRAIN;

ANIMALS; ANTIBODIES; BRAIN; CELL LINE; COMPLEMENT SYSTEM PROTEINS; HUMANS; MICE; MICE, INBRED C57BL; PRPSC PROTEINS; SCRAPIE;

EID: 84855792324     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.11.017     Document Type: Article

References (49)

1. Atarashi R., Sim V.L., Nishida N., Caughey B., Katamine S. Prion strain-dependent differences in conversion of mutant prion proteins in cell culture. J. Virol. 2006, 80:7854-7862.
2. Baron G.S., Hughson A.G., Raymond G.J., Offerdahl D.K., Barton K.A., Raymond L.D., Dorward D.W., Caughey B. Effect of glycans and the glycophosphatidylinositol anchor on strain dependent conformations of scrapie prion protein: improved purifications and infrared spectra. Biochemistry 2011, 50:4479-4490.
3. Benoit M.E., Tenner A.J. Complement protein C1q-mediated neuroprotection is correlated with regulation of neuronal gene and microRNA expression. J. Neurosci. 2011, 31:3459-3469.
4. Bessen R.A., Marsh R.F. Biochemical and physical properties of the prion protein from two strains of the transmissible mink encephalopathy agent. J. Virol. 1992, 66:2096-2101.
5. Bessen R.A., Marsh R.F. Distinct PrP properties suggest the molecular basis of strain variation in transmissible mink encephalopathy. J. Virol. 1994, 68:7859-7868.
6. Blanquet-Grossard F., Thielens N.M., Vendrely C., Jamin M., Arlaud G.J. Complement protein C1q recognizes a conformationally modified form of the prion protein. Biochemistry 2005, 44:4349-4356.
7. Bordin S., Whitfield D. Cutting edge: proliferating fibroblasts respond to collagenous C1q with phosphorylation of p38 mitogen-activated protein kinase and apoptotic features. J. Immunol. 2003, 170:667-671.
8. Bruce M.E., McBride P.A., Farquhar C.F. Precise targeting of the pathology of the sialoglycoprotein, PrP, and vacuolar degeneration in mouse scrapie. Neurosci. Lett. 1989, 102:1-6.
9. Caughey B., Raymond G.J., Bessen R.A. Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J. Biol. Chem. 1998, 273:32230-32235.
10. Dandoy-Dron F., Guillo F., Benboudjema L., Deslys J.P., Lasmezas C., Dormont D., Tovey M.G., Dron M. Gene expression in scrapie. Cloning of a new scrapie-responsive gene and the identification of increased levels of seven other mRNA transcripts. J. Biol. Chem. 1998, 273:7691-7697.
11. Dashiell S.M., Rus H., Koski C.L. Terminal complement complexes concomitantly stimulate proliferation and rescue of Schwann cells from apoptosis. Glia 2000, 30:187-198.
12. Dumestre-Perard C., Osmundson J., Lemaire-Vieille C., Thielens N., Grives A., Favier B., Csopaki F., Jamin M., Gagnon J., Cesbron J.Y. Activation of classical pathway of complement cascade by soluble oligomers of prion. Cell. Microbiol. 2007, 9:2870-2879.
13. Erlich P., Dumestre-Perard C., Ling W.L., Lemaire-Vieille C., Schoehn G., Arlaud G.J., Thielens N.M., Gagnon J., Cesbron J.Y. Complement protein C1q forms a complex with cytotoxic prion protein oligomers. J. Biol. Chem. 2010, 285:19267-19276.
14. Fadok V.A., Voelker D.R., Campbell P.A., Cohen J.J., Bratton D.L., Henson P.M. Exposure of phosphatidylserine on the surface of apoptotic lymphocytes triggers specific recognition and removal by macrophages. J. Immunol. 1992, 148:2207-2216.
15. 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, 182:1305-1313.
16. Guan E., Robinson S.L., Goodman E.B., Tenner A.J. Cell-surface protein identified on phagocytic cells modulates the C1q-mediated enhancement of phagocytosis. J. Immunol. 1994, 152:4005-4016.
17. Hughes J., Nangaku M., Alpers C.E., Shankland S.J., Couser W.G., Johnson R.J. C5b-9 membrane attack complex mediates endothelial cell apoptosis in experimental glomerulonephritis. Am. J. Physiol. Ren. Physiol. 2000, 278:F747-F757.
18. Hwang D., Lee I.Y., Yoo H., Gehlenborg N., Cho J.H., Petritis B., Baxter D., Pitstick R., Young R., Spicer D., Price N.D., Hohmann J.G., Dearmond S.J., Carlson G.A., Hood L.E. A systems approach to prion disease. Mol. Syst. Biol. 2009, 5:252.
19. Ishii T., Haga S., Yagishita S., Tateishi J. The presence of complements in amyloid plaques of Creutzfeldt-Jakob disease and Gerstmann-Straussler-Scheinker disease. Appl. Pathol. 1984, 2:370-379.
20. Klein M.A., Kaeser P.S., Schwarz P., Weyd H., Xenarios I., Zinkernagel R.M., Carroll M.C., Verbeek J.S., Botto M., Walport M.J., Molina H., Kalinke U., Acha-Orbea H., Aguzzi A. Complement facilitates early prion pathogenesis. Nat. Med. 2001, 7:488-492.
21. Kocisko D.A., Baron G.S., Rubenstein R., Chen J., Kuizon S., Caughey B. New inhibitors of scrapie-associated prion protein formation in a library of 2000 drugs and natural products. J. Virol. 2003, 77:10288-10294.
22. Koopman G., Reutelingsperger C.P., Kuijten G.A., Keehnen R.M., Pals S.T., van Oers M.H. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 1994, 84:1415-1420.
23. Kovacs G.G., Gasque P., Strobel T., Lindeck-Pozza E., Strohschneider M., Ironside J.W., Budka H., Guentchev M. Complement activation in human prion disease. Neurobiol. Dis. 2004, 15:21-28.
24. Kuczius T., Groschup M.H. Differences in proteinase K resistance and neuronal deposition of abnormal prion proteins characterize bovine spongiform encephalopathy (BSE) and scrapie strains. Mol. Med. 1999, 5:406-418.
25. LÓbner M., Leslie R.G., Prodinger W.M., Nielsen C.H. Spontaneous complement activation on human B cells results in localized membrane depolarization and the clustering of complement receptor type 2 and C3 fragments. Immunology 2009, 128:e661-e669.
26. Mabbott N.A., Bruce M.E. Complement component C5 is not involved in scrapie pathogenesis. Immunobiology 2004, 209:545-549.
27. 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, 7:485-487.
28. Mahal S.P., Baker C.A., Demczyk C.A., Smith E.W., Julius C., Weissmann C. Prion strain discrimination in cell culture: the cell panel assay. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:20908-20913.
29. Marguet D., Luciani M.F., Moynault A., Williamson P., Chimini G. Engulfment of apoptotic cells involves the redistribution of membrane phosphatidylserine on phagocyte and prey. Nat. Cell Biol. 1999, 1:454-456.
30. Mitchell D.A., Kirby L., Paulin S.M., Villiers C.L., Sim R.B. Prion protein activates and fixes complement directly via the classical pathway: implications for the mechanism of scrapie agent propagation in lymphoid tissue. Mol. Immunol. 2007, 44:2997-3004.
31. Nishida N., Harris D.A., Vilette D., Laude H., Frobert Y., Grassi J., Casanova D., Milhavet O., Lehmann S. Successful transmission of three mouse-adapted scrapie strains to murine neuroblastoma cell lines overexpressing wild-type mouse prion protein. J. Virol. 2000, 74:320-325.
32. Païdassi H., Tacnet-Delorme P., Garlatti V., Darnault C., Ghebrehiwet B., Gaboriaud C., Arlaud G.J., Frachet P. C1q binds phosphatidylserine and likely acts as a multiligand-bridging molecule in apoptotic cell recognition. J. Immunol. 2008, 180:2329-2338.
33. Race R., Jenny A., Sutton D. Scrapie infectivity and proteinase K-resistant prion protein in sheep placenta, brain, spleen, and lymph node: implications for transmission and antemortem diagnosis. J. Infect. Dis. 1998, 178:949-953.
34. Ren G., Huynh C., Bijian K., Cybulsky A.V. Role of apoptosis signal-regulating kinase 1 in complement-mediated glomerular epithelial cell injury. Mol. Immunol. 2008, 45:2236-2246.
35. Rus H.G., Niculescu F., Shin M.L. Sublytic complement attack induces cell cycle in oligodendrocytes. J. Immunol. 1996, 156:4892-4900.
36. Safar J., Wille H., Itri V., Groth D., Serban H., Torchia M., Cohen F.E., Prusiner S.B. Eight prion strains have PrP (Sc) molecules with different conformations. Nat. Med. 1998, 4:1157-1165.
37. Sarvari M., Vago I., Weber C.S., Nagy J., Gal P., Mak M., Kosa J.P., Zavodszky P., Pazmany T. Inhibition of C1q-beta-amyloid binding protects hippocampal cells against complement mediated toxicity. J. Neuroimmunol. 2003, 137:12-18.
38. Shinjyo N., Stahlberg A., Dragunow M., Pekny M., Pekna M. Complement-derived anaphylatoxin C3a regulates in vitro differentiation and migration of neural progenitor cells. Stem Cells 2009, 27:2824-2832.
39. Sim V.L., Caughey B. Ultrastructures and strain comparison of under-glycosylated scrapie prion fibrils. Neurobiol. Aging 2009, 30:2031-2042.
40. Sim R.B., Kishore U., Villiers C.L., Marche P.N., Mitchell D.A. C1q binding and complement activation by prions and amyloids. Immunobiology 2007, 212:355-362.
41. Sjoberg A.P., Nystrom S., Hammarstrom P., Blom A.M. Native, amyloid fibrils and beta-oligomers of the C-terminal domain of human prion protein display differential activation of complement and bind C1q, factor H and C4b-binding protein directly. Mol. Immunol. 2008, 45:3213-3221.
42. Skinner P.J., Abbassi H., Chesebro B., Race R.E., Reilly C., Haase A.T. Gene expression alterations in brains of mice infected with three strains of scrapie. BMC Genomics 2006, 7:114.
43. Soane L., Rus H., Niculescu F., Shin M.L. Inhibition of oligodendrocyte apoptosis by sublytic C5b-9 is associated with enhanced synthesis of bcl-2 and mediated by inhibition of caspase-3 activation. J. Immunol. 1999, 163:6132-6138.
44. Soane L., Cho H.J., Niculescu F., Rus H., Shin M.L. C5b-9 terminal complement complex protects oligodendrocytes from death by regulating Bad through phosphatidylinositol 3-kinase/Akt pathway. J. Immunol. 2001, 167:2305-2311.
45. Speth C., Prodinger W.M., Wurzner R., Stoiber H., Dierich M.P. Complement 2008, 1047-1060.
46. Stevens B., Allen N.J., Vazquez L.E., Howell G.R., Christopherson K.S., Nouri N., Micheva K.D., Mehalow A.K., Huberman A.D., Stafford B., Sher A., Litke A.M., Lambris J.D., Smith S.J., John S.W., Barres B.A. The classical complement cascade mediates CNS synapse elimination. Cell 2007, 131:1164-1178.
47. Veerhuis R., Boshuizen R.S., Morbin M., Mazzoleni G., Hoozemans J.J., Langedijk J.P., Tagliavini F., Langeveld J.P., Eikelenboom P. Activation of human microglia by fibrillar prion protein-related peptides is enhanced by amyloid-associated factors SAP and C1q. Neurobiol. Dis. 2005, 19:273-282.
48. Webster S., Bonnell B., Rogers J. Charge-based binding of complement component C1q to the Alzheimer amyloid beta-peptide. Am. J. Pathol. 1997, 150:1531-1536.
49. Zabel M.D., Heikenwalder M., Prinz M., Arrighi I., Schwarz P., Kranich J., von Teichman A., Haas K.M., Zeller N., Tedder T.F., Weis J.H., Aguzzi A. Stromal complement receptor CD21/35 facilitates lymphoid prion colonization and pathogenesis. J. Immunol. 2007, 179:6144-6152.