Infectious Prions Accumulate to High Levels in Non Proliferative C2C12 Myotubes

PLoS Pathogens

Volumn 9, Issue 11, 2013, Pages

  Herbst, Allen ^a,b   Banser, Pamela ^a,b   Velasquez, Camilo Duque ^a,b   Mays, Charles E ^a,b   Sim, Valerie L ^a,b   Westaway, David ^a,b   Aiken, Judd M ^a,b   McKenzie, Debbie ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PENTOSAN POLYSULFATE; PRION PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; INFECTION; MOUSE; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRION; PRION DISEASE; PROTEIN EXPRESSION; UPREGULATION; VIRUS REPLICATION; WESTERN BLOTTING;

ANIMALS; CELL LINE; CELL PROLIFERATION; CRICETINAE; MICE; MUSCLE FIBERS, SKELETAL; PRPSC PROTEINS; SPECIES SPECIFICITY;

EID: 84888219286     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003755     Document Type: Article

References (62)

1. Leblanc P, Alais S, Porto-Carreiro I, Lehmann S, Grassi J, et al. (2006) Retrovirus infection strongly enhances scrapie infectivity release in cell culture. EMBO J 25: 2674-2685.
2. Alais S, Simoes S, Baas D, Lehmann S, Raposo G, et al. (2008) Mouse neuroblastoma cells release prion infectivity associated with exosomal vesicles. Biol Cell 100: 603-615.
3. Bueler H, Aguzzi A, Sailer A, Greiner RA, Autenried P, et al. (1993) Mice devoid of PrP are resistant to scrapie. Cell 73: 1339-1347.
4. Enari M, Flechsig E, Weissmann C, (2001) Scrapie prion protein accumulation by scrapie-infected neuroblastoma cells abrogated by exposure to a prion protein antibody. Proc Natl Acad Sci U S A 98: 9295-9299.
5. Safar JG, DeArmond SJ, Kociuba K, Deering C, Didorenko S, et al. (2005) Prion clearance in bigenic mice. J Gen Virol 86: 2913-2923.
6. Weissmann C, Li J, Mahal SP, Browning S, (2011) Prions on the move. EMBO Rep 12: 1109-1117.
7. Haig DA, Pattison IH, (1967) In-vitro growth of pieces of brain from scrapie-affected mice. J Pathol Bacteriol 93: 724-727.
8. Clarke MC, Haig DA, (1970) Evidence for the multiplication of scrapie agent in cell culture. Nature 225: 100-101.
9. Haig DA, Clarke MC, (1971) Multiplication of the scrapie agent. Nature 234: 106-107.
10. Clarke MC, Millson GC, (1976) Infection of a cell line of mouse L fibroblasts with scrapie agent. Nature 261: 144-145.
11. Vorberg I, Raines A, Story B, Priola SA, (2004) Susceptibility of common fibroblast cell lines to transmissible spongiform encephalopathy agents. J Infect Dis 189: 431-439.
12. Vilette D, Andreoletti O, Archer F, Madelaine MF, Vilotte JL, et al. (2001) Ex vivo propagation of infectious sheep scrapie agent in heterologous epithelial cells expressing ovine prion protein. Proc Natl Acad Sci U S A 98: 4055-4059.
13. Markovits P, Dautheville C, Dormont D, Dianoux L, Latarjet R, (1983) In vitro propagation of the scrapie agent. I. Transformation of mouse glia and neuroblastoma cells after infection with the mouse-adapted scrapie strain c-506. Acta Neuropathol 60: 75-80.
14. Roikhel VM, Fokina GI, Lisak VM, Kondakova LI, Korolev MB, et al. (1987) Persistence of the scrapie agent in glial cells from rat Gasserian ganglion. Acta Virol 31: 36-42.
15. Iwamaru Y, Takenouchi T, Ogihara K, Hoshino M, Takata M, et al. (2007) Microglial cell line established from prion protein-overexpressing mice is susceptible to various murine prion strains. J Virol 81: 1524-1527.
16. Rubenstein R, Carp RI, Callahan SM, (1984) In vitro replication of scrapie agent in a neuronal model: infection of PC12 cells. J Gen Virol 65 (Pt 12):: 2191-2198.
17. Follet J, Lemaire-Vieille C, Blanquet-Grossard F, Podevin-Dimster V, Lehmann S, et al. (2002) PrP expression and replication by Schwann cells: implications in prion spreading. J Virol 76: 2434-2439.
18. Schatzl HM, Laszlo L, Holtzman DM, Tatzelt J, DeArmond SJ, et al. (1997) A hypothalamic neuronal cell line persistently infected with scrapie prions exhibits apoptosis. J Virol 71: 8821-8831.
19. Dron M, Dandoy-Dron F, Farooq Salamat MK, Laude H, (2009) Proteasome inhibitors promote the sequestration of PrPSc into aggresomes within the cytosol of prion-infected CAD neuronal cells. J Gen Virol 90: 2050-2060.
20. Race RE, Fadness LH, Chesebro B, (1987) Characterization of scrapie infection in mouse neuroblastoma cells. J Gen Virol 68 (Pt 5):: 1391-1399.
21. Butler DA, Scott MR, Bockman JM, Borchelt DR, Taraboulos A, et al. (1988) Scrapie-infected murine neuroblastoma cells produce protease-resistant prion proteins. J Virol 62: 1558-1564.
22. Nishida N, Harris DA, Vilette D, Laude H, Frobert Y, et al. (2000) Successful transmission of three mouse-adapted scrapie strains to murine neuroblastoma cell lines overexpressing wild-type mouse prion protein. J Virol 74: 320-325.
23. Race RE, Caughey B, Graham K, Ernst D, Chesebro B, (1988) Analyses of frequency of infection, specific infectivity, and prion protein biosynthesis in scrapie-infected neuroblastoma cell clones. J Virol 62: 2845-2849.
24. Bosque PJ, Prusiner SB, (2000) Cultured cell sublines highly susceptible to prion infection. J Virol 74: 4377-4386.
25. Courageot MP, Daude N, Nonno R, Paquet S, Di Bari MA, et al. (2008) A cell line infectible by prion strains from different species. J Gen Virol 89: 341-347.
26. Lawson VA, Vella LJ, Stewart JD, Sharples RA, Klemm H, et al. (2008) Mouse-adapted sporadic human Creutzfeldt-Jakob disease prions propagate in cell culture. Int J Biochem Cell Biol 40: 2793-2801.
27. Bian J, Napier D, Khaychuck V, Angers R, Graham C, et al. (2010) Cell-based quantification of chronic wasting disease prions. J Virol 84: 8322-8326.
28. Ghaemmaghami S, Phuan PW, Perkins B, Ullman J, May BC, et al. (2007) Cell division modulates prion accumulation in cultured cells. Proc Natl Acad Sci U S A 104: 17971-17976.
29. Yaffe D, Saxel O, (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725-727.
30. Brown DR, Schmidt B, Groschup MH, Kretzschmar HA, (1998) Prion protein expression in muscle cells and toxicity of a prion protein fragment. Eur J Cell Biol 75: 29-37.
31. Stella R, Massimino ML, Sandri M, Sorgato MC, Bertoli A, (2010) Cellular prion protein promotes regeneration of adult muscle tissue. Mol Cell Biol 30: 4864-4876.
32. Bosque PJ, Ryou C, Telling G, Peretz D, Legname G, et al. (2002) Prions in skeletal muscle. Proc Natl Acad Sci U S A 99: 3812-3817.
33. Angers RC, Browning SR, Seward TS, Sigurdson CJ, Miller MW, et al. (2006) Prions in skeletal muscles of deer with chronic wasting disease. Science 311: 1117.
34. Dlakic WM, Grigg E, Bessen RA, (2007) Prion infection of muscle cells in vitro. J Virol 81: 4615-4624.
35. Chasseigneaux S, Pastore M, Britton-Davidian J, Manie E, Stern MH, et al. (2008) Genetic heterogeneity versus molecular analysis of prion susceptibility in neuroblasma N2a sublines. Arch Virol 153: 1693-1702.
36. Benjamini Y, Hochberg Y, (1995) Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological) 57: 289-300.
37. Hwang D, Lee IY, Yoo H, Gehlenborg N, Cho JH, et al. (2009) A systems approach to prion disease. Mol Syst Biol 5: 252.
38. Gehlenborg N, Hwang D, Lee IY, Yoo H, Baxter D, et al. (2009) The Prion Disease Database: a comprehensive transcriptome resource for systems biology research in prion diseases. Database (Oxford) 2009: bap011.
39. Caughey B, Raymond GJ, (1993) Sulfated polyanion inhibition of scrapie-associated PrP accumulation in cultured cells. J Virol 67: 643-650.
40. Birkett CR, Hennion RM, Bembridge DA, Clarke MC, Chree A, et al. (2001) Scrapie strains maintain biological phenotypes on propagation in a cell line in culture. EMBO J 20: 3351-3358.
41. Diringer H, Ehlers B, (1991) Chemoprophylaxis of scrapie in mice. J Gen Virol 72 (Pt 2):: 457-460.
42. Rainov NG, Tsuboi Y, Krolak-Salmon P, Vighetto A, Doh-Ura K, (2007) Experimental treatments for human transmissible spongiform encephalopathies: is there a role for pentosan polysulfate? Expert Opin Biol Ther 7: 713-726.
43. Weissmann C, (2004) The state of the prion. Nat Rev Microbiol 2: 861-871.
44. Rubenstein R, Deng H, Race RE, Ju W, Scalici CL, et al. (1992) Demonstration of scrapie strain diversity in infected PC12 cells. J Gen Virol 73 (Pt 11):: 3027-3031.
45. Lehmann S, (2005) Prion propagation in cell culture. Methods Mol Biol 299: 227-234.
46. Arima K, Nishida N, Sakaguchi S, Shigematsu K, Atarashi R, et al. (2005) Biological and biochemical characteristics of prion strains conserved in persistently infected cell cultures. J Virol 79: 7104-7112.
47. Mahal SP, Baker CA, Demczyk CA, Smith EW, Julius C, et al. (2007) Prion strain discrimination in cell culture: the cell panel assay. Proc Natl Acad Sci U S A 104: 20908-20913.
48. Hardeman EC, Minty A, Benton-Vosman P, Kedes L, Blau HM, (1988) In vivo system for characterizing clonal variation and tissue-specific gene regulatory factors based on function. J Cell Biol 106: 1027-1034.
49. Julius C, Hutter G, Wagner U, Seeger H, Kana V, et al. (2008) Transcriptional stability of cultured cells upon prion infection. J Mol Biol 375: 1222-1233.
50. Race R, Chesebro B, (1998) Scrapie infectivity found in resistant species. Nature 392: 770.
51. Rubenstein R, Scalici CL, Papini MC, Callahan SM, Carp RI, (1990) Further characterization of scrapie replication in PC12 cells. J Gen Virol 71 (Pt 4):: 825-831.
52. Mallucci G, Dickinson A, Linehan J, Klohn PC, Brandner S, et al. (2003) Depleting neuronal PrP in prion infection prevents disease and reverses spongiosis. Science 302: 871-874.
53. Prusiner SB, Scott M, Foster D, Pan KM, Groth D, et al. (1990) Transgenetic studies implicate interactions between homologous PrP isoforms in scrapie prion replication. Cell 63: 673-686.
54. Raymond GJ, Raymond LD, Meade-White KD, Hughson AG, Favara C, et al. (2007) Transmission and adaptation of chronic wasting disease to hamsters and transgenic mice: evidence for strains. J Virol 81: 4305-4314.
55. Kärber G, (1931) Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Naunyn-Schmiedebergs Archiv für experimentelle Pathologie und Pharmakologie 162: 480-483.
56. Prusiner SB, Cochran SP, Groth DF, Downey DE, Bowman KA, et al. (1982) Measurement of the scrapie agent using an incubation time interval assay. Ann Neurol 11: 353-358.
57. Fischer M, Rulicke T, Raeber A, Sailer A, Moser M, et al. (1996) Prion protein (PrP) with amino-proximal deletions restoring susceptibility of PrP knockout mice to scrapie. EMBO J 15: 1255-1264.
58. Sandberg MK, Al-Doujaily H, Sharps B, Clarke AR, Collinge J, (2011) Prion propagation and toxicity in vivo occur in two distinct mechanistic phases. Nature 470: 540-542.
59. Kascsak R, (2010) Reiterating the epitope specificity of prion-specific mAb 3F4. J Biol Chem 285: le5 author reply le6.
60. Choi JK, Park SJ, Jun YC, Oh JM, Jeong BH, et al. (2006) Generation of monoclonal antibody recognized by the GXXXG motif (glycine zipper) of prion protein. Hybridoma (Larchmt) 25: 271-277.
61. Feraudet C, Morel N, Simon S, Volland H, Frobert Y, et al. (2005) Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J Biol Chem 280: 11247-11258.
62. Moody LR, Herbst AJ, Yoo HS, Vanderloo JP, Aiken JM, (2009) Comparative prion disease gene expression profiling using the prion disease mimetic, cuprizone. Prion 3: 99-109.