Increased infectivity of anchorless mouse scrapie prions in transgenic mice overexpressing human prion protein

Journal of Virology

Volumn 89, Issue 11, 2015, Pages 6022-6032

  Race, Brent ^a   Phillips, Katie ^a   Meade White, Kimberly ^a   Striebel, James ^a   Chesebro, Bruce ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOSYLPHOSPHATIDYLINOSITOL; PRION PROTEIN; PRION;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HUMAN; IMMUNOBLOTTING; NEUROPATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCRAPIE; SCRAPIE AGENT; SPECIES COMPARISON; TRANSGENIC MOUSE; VIRUS INFECTIVITY; VIRUS TRANSMISSION; WILD TYPE; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; METABOLISM; PATHOLOGY; PRION; PRION DISEASE; TRANSGENE; TRANSMISSION;

MAMMALIA; MUS; MUS MUSCULUS;

ANIMALS; DISEASE MODELS, ANIMAL; HUMANS; MICE, INBRED C57BL; MICE, TRANSGENIC; PRION DISEASES; PRIONS; TRANSGENES;

EID: 84929630735     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00362-15     Document Type: Article

References (76)

1. Castilla J, Saa P, Hetz C, Soto C. 2005. In vitro generation of infectious scrapie prions. Cell 121:195-206. http://dx.doi.org/10.1016/j.cell.2005.02.011.
2. Deleault NR, Harris BT, Rees JR, Supattapone S. 2007. Formation of native prions from minimal components in vitro. Proc Natl Acad SciUSA 104:9741-9746. http://dx.doi.org/10.1073/pnas.0702662104.
3. Weber P, Giese A, Piening N, Mitteregger G, Thomzig A, Beekes M, Kretzschmar HA. 2006. Cell-free formation of misfolded prion protein with authentic prion infectivity. Proc Natl Acad Sci U S A 103:15818-15823. http://dx.doi.org/10.1073/pnas.0605608103.
4. Klingeborn M, Race B, Meade-White KD, Chesebro B. 2011. Lower specific infectivity of protease-resistant prion protein generated in cellfree reactions. Proc Natl Acad Sci U S A 108:E1244-E1253. http://dx.doi.org/10.1073/pnas.1111255108.
5. Prusiner SB. 1982. Novel proteinaceous infectious particles cause scrapie. Science 216:136-144. http://dx.doi.org/10.1126/science.6801762.
6. Caughey B, Baron GS, Chesebro B, Jeffrey M. 2009. Getting a grip on prions: oligomers, amyloids, and pathological membrane interactions. Annu Rev Biochem 78:177-204. http://dx.doi.org/10.1146/annurev.biochem.78.082907.145410.
7. Tribouillard-Tanvier D, Race B, Striebel JF, Carroll JA, Phillips K, Chesebro B. 2012. Early cytokine elevation, PrPres deposition, and gliosis in mouse scrapie: no effect on disease by deletion of cytokine genes IL-12p40 and IL-12p35. J Virol 86:10377-10383. http://dx.doi.org/10.1128/JVI.01340-12.
8. Riemer C, Neidhold S, Burwinkel M, Schwarz A, Schultz J, Kratzschmar J, Monning U, Baier M. 2004. Gene expression profiling of scrapieinfected brain tissue. Biochem Biophys Res Commun 323:556-564. http://dx.doi.org/10.1016/j.bbrc.2004.08.124.
9. Carroll JA, Striebel JF, Race B, Phillips K, Chesebro B. 10 December 2014. Prion infection of mouse brain reveals multiple new upregulated genes involved in neuroinflammation or signal transduction. J Virol http://dx.doi.org/10.1128/JVI.02952-14.
10. Crespo I, Roomp K, Jurkowski W, Kitano H, del Sol A. 2012. Gene regulatory network analysis supports inflammation as a key neurodegeneration process in prion disease. BMC Syst Biol 6:132. http://dx.doi.org/10.1186/1752-0509-6-132.
11. Kovacs GG, Budka H. 2008. Prion diseases: from protein to cell pathology. Am J Pathol 172:555-565. http://dx.doi.org/10.2353/ajpath.2008.070442.
12. Moore RA, Vorberg I, Priola SA. 2005. Species barriers in prion diseases-brief review, p 187-202. In Peters CJ, Calisher CH (ed), Infectious diseases from nature: mechanisms of viral emergence and persistence. Springer Vienna, Vienna, Austria. http://dx.doi.org/10.1007/3-211-29981-5.
13. Collinge J, Clarke AR. 2007. A general model of prion strains and their pathogenicity. Science 318:930-936. http://dx.doi.org/10.1126/science.1138718.
14. Priola SA. 2013. Species barriers in prion disease, p 139-154. In Zou W-Q, Gambetti P (ed), Prions and diseases, vol 2. Animals, humans and the environment. Springer, New York, NY.
15. Locht C, Chesebro B, Race R, Keith JM. 1986. Molecular cloning and complete sequence of prion protein cDNA from mouse brain infected with the scrapie agent. Proc Natl Acad Sci U S A 83:6372-6376. http://dx.doi.org/10.1073/pnas.83.17.6372.
16. Kretzschmar HA, Stowring LE, Westaway D, Stubblebine WH, Prusiner SB, Dearmond SJ. 1986. Molecular cloning of a human prion protein cDNA. DNA 5:315-324. http://dx.doi.org/10.1089/dna.1986.5.315.
17. Schätzl HM, Da Costa M, Taylor L, Cohen FE, Prusiner SB. 1995. Prion protein gene variation among primates. J Mol Biol 245:362-374. http://dx.doi.org/10.1006/jmbi.1994.0030.
18. Riek R, Hornemann S, Wider G, Billeter M, Glockshuber R, Wuthrich K. 1996. NMR structure of the mouse prion protein domain PrP(121-231). Nature 382:180-182. http://dx.doi.org/10.1038/382180a0.
19. Zahn R, Liu A, Luhrs T, Riek R, von Schroetter C, Lopez Garcia F, Billeter M, Calzolai L, Wider G, Wuthrich K. 2000. NMR solution structure of the human prion protein. Proc Natl Acad Sci U S A 97:145-150. http://dx.doi.org/10.1073/pnas.97.1.145.
20. Wadsworth JD, Joiner S, Linehan JM, Desbruslais M, Fox K, Cooper S, Cronier S, Asante EA, Mead S, Brandner S, Hill AF, Collinge J. 2008. Kuru prions and sporadic Creutzfeldt-Jakob disease prions have equivalent transmission properties in transgenic and wild-type mice. Proc Natl Acad SciUSA 105:3885-3890. http://dx.doi.org/10.1073/pnas.0800190105.
21. Telling GC, Scott M, Mastrianni J, Gabizon R, Torchia M, Cohen FE, DeArmond SJ, Prusiner SB. 1995. Prion propagation in mice expressing human and chimeric PrP transgenes implicates the interaction of cellular PrP with another protein. Cell 83:79-90. http://dx.doi.org/10.1016/0092-8674(95)90236-8.
22. Scott M, Groth D, Foster D, Torchia M, Yang SL, DeArmond SJ, Prusiner SB. 1993. Propagation of prions with artificial properties in transgenic mice expressing chimeric PrP genes. Cell 73:979-988. http://dx.doi.org/10.1016/0092-8674(93)90275-U.
23. Telling GC, Scott M, Hsiao KK, Foster D, Yang SL, Torchia M, Sidle KC, Collinge J, DeArmond SJ, Prusiner SB. 1994. Transmission of Creutzfeldt-Jakob disease from humans to transgenic mice expressing chimeric human-mouse prion protein. Proc Natl Acad Sci U S A 91:9936-9940. http://dx.doi.org/10.1073/pnas.91.21.9936.
24. Priola SA, Chesebro B. 1995. A single hamster PrP amino acid blocks conversion to protease-resistant PrP in scrapie-infected mouse neuroblastoma cells. J Virol 69:7754-7758.
25. Priola SA, Chabry J, Chan K. 2001. Efficient conversion of normal prion protein (PrP) by abnormal hamster PrP is determined by homology at amino acid residue 155. J Virol 75:4673-4680. http://dx.doi.org/10.1128/JVI.75.10.4673-4680.2001.
26. Barron RM, Thomson V, Jamieson E, Melton DW, Ironside J, Will R, Manson JC. 2001. Changing a single amino acid in the N-terminus of murine PrP alters TSE incubation time across three species barriers. EMBO J 20:5070-5078. http://dx.doi.org/10.1093/emboj/20.18.5070.
27. Damberger FF, Christen B, Perez DR, Hornemann S, Wuthrich K. 2011. Cellular prion protein conformation and function. Proc Natl Acad Sci U S A 108:17308-17313. http://dx.doi.org/10.1073/pnas.1106325108.
28. Caughey B, Raymond GJ, Bessen RA. 1998. Strain-dependent differences in beta-sheet conformations of abnormal prion protein. J Biol Chem 273:32230-32235. http://dx.doi.org/10.1074/jbc.273.48.32230.
29. Baron GS, Hughson AG, Raymond GJ, Offerdahl DK, Barton KA, Raymond LD, Dorward DW, Caughey B. 2011. Effect of glycans and the glycophosphatidylinositol anchor on strain dependent conformations of scrapie prion protein: improved purifications and infrared spectra. Biochemistry 50:4479-4490. http://dx.doi.org/10.1021/bi2003907.
30. Spassov S, Beekes M, Naumann D. 2006. Structural differences between TSEs strains investigated by FT-IR spectroscopy. Biochim Biophys Acta 1760:1138-1149. http://dx.doi.org/10.1016/j.bbagen.2006.02.018.
31. Tuzi NL, Cancellotti E, Baybutt H, Blackford L, Bradford B, Plinston C, Coghill A, Hart P, Piccardo P, Barron RM, Manson JC. 2008. Host PrP glycosylation: a major factor determining the outcome of prion infection. PLoS Biol 6:e100. http://dx.doi.org/10.1371/journal.pbio.0060100.
32. Neuendorf E, Weber A, Saalmueller A, Schatzl H, Reifenberg K, Pfaff E, Groschup MH. 2004. Glycosylation deficiency at either one of the two glycan attachment sites of cellular prion protein preserves susceptibility to bovine spongiform encephalopathy and scrapie infections. J Biol Chem 279:53306-53316. http://dx.doi.org/10.1074/jbc.M410796200.
33. Cancellotti E, Bradford BM, Tuzi NL, Hickey RD, Brown D, Brown KL, Barron RM, Kisielewski D, Piccardo P, Manson JC. 2010. Glycosylation of PrPCdetermines timing of neuroinvasion and targeting in the brain following transmissible spongiform encephalopathy infection by a peripheral route. J Virol 84:3464-3475. http://dx.doi.org/10.1128/JVI.02374-09.
34. Priola SA, Lawson VA. 2001. Glycosylation influences cross-species formation of protease-resistant prion protein. EMBO J 20:6692-6699. http://dx.doi.org/10.1093/emboj/20.23.6692.
35. Wiseman FK, Cancellotti E, Piccardo P, Iremonger K, Boyle A, Brown D, Ironside JW, Manson JC, Diack AB. 11 February 2015. The glycosylation status of PrPC is a key factor in determining TSE transmission between species. J Virol http://dx.doi.org/10.1128/JVI.02296-14.
36. Chesebro B, Race B, Meade-White K, Lacasse R, Race R, Klingeborn M, Striebel J, Dorward D, McGovern G, Jeffrey M. 2010. Fatal transmissible amyloid encephalopathy: a new type of prion disease associated with lack of prion protein membrane anchoring. PLoS Pathog 6:e1000800. http://dx.doi.org/10.1371/journal.ppat.1000800.
37. Rangel A, Race B, Phillips K, Striebel J, Kurtz N, Chesebro B. 2014. Distinct patterns of spread of prion infection in brains of mice expressing anchorless or anchored forms of prion protein. Acta Neuropathol Commun 2:8. http://dx.doi.org/10.1186/2051-5960-2-8.
38. Mahal SP, Jablonski J, Suponitsky-Kroyter I, Oelschlegel AM, Herva ME, Oldstone M, Weissmann C. 2012. Propagation of RML prions in mice expressing PrP devoid of GPI anchor leads to formation of a novel, stable prion strain. PLoS Pathog 8:e1002746. http://dx.doi.org/10.1371/journal.ppat.1002746.
39. Dvorakova E, Vranac T, Janouskova O, Cernilec M, Koren S, Lukan A, Novakova J, Matej R, Holada K, Curin Serbec V. 2013. Detection of the GPI-anchorless prion protein fragment PrP226* in human brain. BMC Neurol 13:126. http://dx.doi.org/10.1186/1471-2377-13-126.
40. Tagliavini F, Prelli F, Porro M, Salmona M, Bugiani O, Frangione B. 1992. A soluble form of prion protein in human cerebrospinal-fluid-implications for prion-related encephalopathies. Biochem Biophys Res Commun 184: 1398-1404. http://dx.doi.org/10.1016/S0006-291X(05)80038-5.
41. Parizek P, Roeckl C, Weber J, Flechsig E, Aguzzi A, Raeber AJ. 2001. Similar turnover and shedding of the cellular prion protein in primary lymphoid and neuronal cells. J Biol Chem 276:44627-44632. http://dx.doi.org/10.1074/jbc.M107458200.
42. Borchelt DR, Rogers M, Stahl N, Telling G, Prusiner SB. 1993. Release of the cellular prion protein from cultured cells after loss of its glycoinositol phospholipid anchor. Glycobiology 3:319-329. http://dx.doi.org/10.1093/glycob/3.4.319.
43. Stahl N, Borchelt DR, Hsiao K, Prusiner SB. 1987. Scrapie prion protein contains a phosphatidylinositol glycolipid. Cell 51:229-240. http://dx.doi.org/10.1016/0092-8674(87)90150-4.
44. Kocisko DA, Come JH, Priola SA, Chesebro B, Raymond GJ, Lansbury PT, Caughey B. 1994. Cell-free formation of protease-resistant prion protein. Nature 370:471-474. http://dx.doi.org/10.1038/370471a0.
45. Rogers M, Yehiely F, Scott M, Prusiner SB. 1993. Conversion of truncated and elongated prion proteins into the scrapie isoform in cultured cells. Proc Natl Acad Sci U S A 90:3182-3186. http://dx.doi.org/10.1073/pnas.90.8.3182.
46. Chesebro B, Trifilo M, Race R, Meade-White K, Teng C, LaCasse R, Raymond L, Favara C, Baron G, Priola S, Caughey B, Masliah E, Oldstone M. 2005. Anchorless prion protein results in infectious amyloid disease without clinical scrapie. Science 308:1435-1439. http://dx.doi.org/10.1126/science.1110837.
47. Budka H, Aguzzi A, Brown P, Brucher JM, Bugiani O, Gullotta F, Haltia M, Hauw JJ, Ironside JW, Jellinger K, Kretzschmar HA, Lantos PL, Masullo C, Schlote W, Tateishi J, Weller RO. 1995. Neuropathological diagnostic criteria for Creutzfeldt-Jakob disease (CJD) and other human spongiform encephalopathies (prion diseases). Brain Pathol 5:459-466. http://dx.doi.org/10.1111/j.1750-3639.1995.tb00625.x.
48. González L, Martin S, Begara-McGorum I, Hunter N, Houston F, Simmons M, Jeffrey M. 2002. Effects of agent strain and host genotype on PrP accumulation in the brain of sheep naturally and experimentally affected with scrapie. J Comp Pathol 126:17-29. http://dx.doi.org/10.1053/jcpa.2001.0516.
49. Rangel A, Race B, Klingeborn M, Striebel J, Chesebro B. 2013. Unusual cerebral vascular prion protein amyloid distribution in scrapie-infected transgenic mice expressing anchorless prion protein. Acta Neuropathol Commun 1:25-36. http://dx.doi.org/10.1186/2051-5960-1-25.
50. Raymond GJ, Race B, Hollister JR, Offerdahl DK, Moore RA, Kodali R, Raymond LD, Hughson AG, Rosenke R, Long D, Dorward DW, Baron GS. 2012. Isolation of novel synthetic prion strains by amplification in transgenic mice coexpressing wild-type and anchorless prion proteins. J Virol 86:11763-11778. http://dx.doi.org/10.1128/JVI.01353-12.
51. Chiti F, Dobson CM. 2006. Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75:333-366. http://dx.doi.org/10.1146/annurev.biochem.75.101304.123901.
52. National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
53. Race B, Meade-White KD, Miller MW, Barbian KD, Rubenstein R, LaFauci G, Cervenakova L, Favara C, Gardner D, Long D, Parnell M, Striebel J, Priola SA, Ward A, Williams ES, Race R, Chesebro B. 2009. Susceptibilities of nonhuman primates to chronic wasting disease. Emerg Infect Dis 15:1366-1376. http://dx.doi.org/10.3201/eid1509.090253.
54. Manson JC, Clarke AR, Hooper ML, Aitchison L, McConnell I, Hope J. 1994. 129/Ola mice carrying a null mutation in PrP that abolishes mRNA production are developmentally normal. Mol Neurobiol 8:121-127. http://dx.doi.org/10.1007/BF02780662.
55. Striebel JF, Race B, Pathmajeyan M, Rangel A, Chesebro B. 2013. Lack of influence of prion protein gene expression on kainate-induced seizures in mice: studies using congenic, coisogenic and transgenic strains. Neuroscience 238:11-18. http://dx.doi.org/10.1016/j.neuroscience.2013.02.004.
56. Kascsak RJ, Rubenstein R, Merz PA, Tonna-DeMasi M, Fersko R, Carp RI, Wisniewski HM, Diringer H. 1987. Mouse polyclonal and monoclonal antibody to scrapie-associated fibril proteins. J Virol 61:3688-3693.
57. Vorberg I, Buschmann A, Harmeyer S, Saalmuller A, Pfaff E, Groschup MH. 1999. A novel epitope for the specific detection of exogenous prion proteins in transgenic mice and transfected murine cell lines. Virology 255:26-31. http://dx.doi.org/10.1006/viro.1998.9561.
58. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A, Poser S, Pocchiari M, Hofman A, Smith PG. 1996. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet 347:921-925. http://dx.doi.org/10.1016/S0140-6736(96)91412-9.
59. Sánchez-Juan P, Houben MPWA, Hoff JI, Jansen C, Sie MPS, van Rijn MJE, Ironside JW, Will RG, van Duijn CM, Rozemuller A. 2007. The first case of variant Creutzfeldt-Jakob disease in the Netherlands. J Neurol 254:958-960. http://dx.doi.org/10.1007/s00415-006-0360-3.
60. Lloyd SE, Mead S, Collinge J. 2013. Genetics of prion diseases. Curr Opin Genet Dev 23:345-351. http://dx.doi.org/10.1016/j.gde.2013.02.012.
61. Cancellotti E, Mahal SP, Somerville R, Diack A, Brown D, Piccardo P, Weissmann C, Manson JC. 2013. Post-translational changes to PrP alter transmissible spongiform encephalopathy strain properties. EMBO J 32: 756-769. http://dx.doi.org/10.1038/emboj.2013.6.
62. Collinge J, Sidle KC, Meads J, Ironside J, Hill AF. 1996. Molecular analysis of prion strain variation and the aetiology of 'new variant' CJD. Nature 383:685-690. http://dx.doi.org/10.1038/383685a0.
63. DeArmond SJ, Sanchez H, Yehiely F, Qiu Y, Ninchak-Casey A, Daggett V, Camerino AP, Cayetano J, Rogers M, Groth D, Torchia M, Tremblay P, Scott MR, Cohen FE, Prusiner SB. 1997. Selective neuronal targeting in prion disease. Neuron 19:1337-1348. http://dx.doi.org/10.1016/S0896-6273(00)80424-9.
64. Priola SA, McNally KL. 2009. The role of the prion protein membrane anchor in prion infection. Prion 3:134-138. http://dx.doi.org/10.4161/pri.3.3.9771.
65. Puig B, Altmeppen H, Glatzel M. 2014. The GPI-anchoring of PrP: implications in sorting and pathogenesis. Prion 8:11-18. http://dx.doi.org/10.4161/pri.27892.
66. Bate C, Tayebi M, Williams A. 2010. The glycosylphosphatidylinositol anchor is a major determinant of prion binding and replication. Biochem J 428:95-101. http://dx.doi.org/10.1042/BJ20091469.
67. McNally KL, Ward AE, Priola SA. 2009. Cells expressing anchorless prion protein are resistant to scrapie infection. J Virol 83:4469-4475. http://dx.doi.org/10.1128/JVI.02412-08.
68. Race B, Meade-White K, Oldstone MB, Race R, Chesebro B. 2008. Detection of prion infectivity in fat tissues of scrapie-infected mice. PLoS Pathog 4:e1000232. http://dx.doi.org/10.1371/journal.ppat.1000232.
69. Trifilo MJ, Yajima T, Gu Y, Dalton N, Peterson KL, Race RE, Meade-White K, Portis JL, Masliah E, Knowlton KU, Chesebro B, Oldstone MB. 2006. Prion-induced amyloid heart disease with high blood infectivity in transgenic mice. Science 313:94-97. http://dx.doi.org/10.1126/science.1128635.
70. Cassard H, Torres JM, Lacroux C, Douet JY, Benestad SL, Lantier F, Lugan S, Lantier I, Costes P, Aron N, Reine F, Herzog L, Espinosa JC, Beringue V, Andreoletti O. 2014. Evidence for zoonotic potential of ovine scrapie prions. Nat Commun 5:5821. http://dx.doi.org/10.1038/ncomms6821.
71. Race R, Raines A, Raymond GJ, Caughey B, Chesebro B. 2001. Longterm subclinical carrier state precedes scrapie replication and adaptation in a resistant species: analogies to bovine spongiform encephalopathy and variant Creutzfeldt-Jakob disease in humans. J Virol 75:10106-10112. http://dx.doi.org/10.1128/JVI.75.21.10106-10112.2001.
72. Hill AF, Joiner S, Linehan J, Desbruslais M, Lantos PL, Collinge J. 2000. Species-barrier-independent prion replication in apparently resistant species. Proc Natl Acad Sci U S A 97:10248-10253. http://dx.doi.org/10.1073/pnas.97.18.10248.
73. Kimberlin RH, Walker CA. 1978. Evidence that the transmission of one source of scrapie agent to hamsters involves separation of agent strains from a mixture. J Gen Virol 39:487-496. http://dx.doi.org/10.1099/0022-1317-39-3-487.
74. Li J, Browning S, Mahal SP, Oelschlegel AM, Weissmann C. 2010. Darwinian evolution of prions in cell culture. Science 327:869-872. http://dx.doi.org/10.1126/science.1183218.
75. Mahal SP, Browning S, Li J, Suponitsky-Kroyter I, Weissmann C. 2010. Transfer of a prion strain to different hosts leads to emergence of strain variants. Proc Natl Acad Sci U S A 107:22653-22658. http://dx.doi.org/10.1073/pnas.1013014108.
76. Stahl N, Baldwin MA, Burlingame AL, Prusiner SB. 1990. Identification of glycoinositol phospholipid linked and truncated forms of the scrapie prion protein. Biochemistry 29:8879-8884. http://dx.doi.org/10.1021/bi00490a001.