De novo generation of infectious prions with bacterially expressed recombinant prion protein

FASEB Journal

Volumn 27, Issue 12, 2013, Pages 4768-4775

  Zhang, Zhihong ^a   Zhang, Yi ^a,b   Wang, Fei ^b   Wang, Xinhe ^b   Xu, Yuanyuan ^a   Yang, Huaiyi ^c   Yu, Guohua ^a   Yuan, Chonggang ^a   Ma, Jiyan ^a,b  

^a B326 Science Building   (China)

^b OHIO STATE UNIVERSITY   (United States)

^c INSTITUTE OF MICROBIOLOGY   (China)

Author keywords

Bioassay; Recombinant PrP; SPMCA

Indexed keywords

PRION PROTEIN; PROTEINASE K; RECOMBINANT PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIUM CONTAMINATION; BIOASSAY; CHEMICAL ANALYSIS; CONTROLLED STUDY; GENE AMPLIFICATION; MALE; MOUSE; NONHUMAN; PARTICLE SIZE; PRION DISEASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERIAL PROTEIN MISFOLDING CYCLIC AMPLIFICATION; SURVIVAL TIME;

BIOASSAY; RECOMBINANT PRP; SPMCA;

ANIMALS; BRAIN; MICE; PRIONS; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS;

EID: 84890537961     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-233965     Document Type: Article

References (48)

1. Prusiner, S. B. (1998) Prions. Proc. Natl. Acad. Sci. U. S. A. 95, 13363-13383
2. Caughey, B., and Chesebro, B. (1997) Prion protein and the transmissible spongiform encephalopathies. Trends Cell Biol. 7, 56-62
3. Saborio, G. P., Permanne, B., and Soto, C. (2001) Sensitive detection of pathological prion protein by cyclic amplification of protein misfolding. Nature 411, 810-813
4. Castilla, J., Saa, P., Hetz, C., and Soto, C. (2005) In vitro generation of infectious scrapie prions. Cell 121, 195-206
5. Deleault, N. R., Harris, B. T., Rees, J. R., and Supattapone, S. (2007) Formation of native prions from minimal components in vitro. Proc. Natl. Acad. Sci. U. S. A. 104, 9741-9746
6. Geoghegan, J. C., Miller, M. B., Kwak, A. H., Harris, B. T., and Supattapone, S. (2009) Trans-dominant inhibition of prion propagation in vitro is not mediated by an accessory cofactor. PLoS Pathog. 5, e1000535
7. Imamura, M., Kato, N., Yoshioka, M., Okada, H., Iwamaru, Y., Shimizu, Y., Mohri, S., Yokoyama, T., and Murayama, Y. (2011) Glycosylphosphatidylinositol anchor-dependent stimulation pathway required for generation of baculovirus-derived recombinant scrapie prion protein. J. Virol. 85, 2582-2588
8. Wang, F., Wang, X., Yuan, C. G., and Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327, 1132-1135
9. Wang, F., Zhang, Z., Wang, X., Li, J., Zha, L., Yuan, C. G., Weissmann, C., and Ma, J. (2012) Genetic informational RNA is not required for recombinant prion infectivity. J. Virol. 86, 1874-1876
10. Deleault, N. R., Piro, J. R., Walsh, D. J., Wang, F., Ma, J., Geoghegan, J. C., and Supattapone, S. (2012) Isolation of phosphatidylethanolamine as a solitary cofactor for prion formation in the absence of nucleic acids. Proc. Natl. Acad. Sci. U. S. A. 109, 8546-8551
11. Deleault, N. R., Walsh, D. J., Piro, J. R., Wang, F., Wang, X., Ma, J., Rees, J. R., and Supattapone, S. (2012) Cofactor molecules maintain infectious conformation and restrict strain properties in purified prions. Proc. Natl. Acad. Sci. U. S. A. 109, E1938-E1946
12. Cosseddu, G. M., Nonno, R., Vaccari, G., Bucalossi, C., Fernandez-Borges, N., Di Bari, M. A., Castilla, J., and Agrimi, U. (2011) Ultra-efficient PrP(Sc) amplification highlights potentialities and pitfalls of PMCA technology. PLoS Pathog. 7, e1002370
13. Saa, P., Castilla, J., and Soto, C. (2006) Ultra-efficient replication of infectious prions by automated protein misfolding cyclic amplification. J. Biol. Chem. 281, 35245-35252
14. Morales, R., Duran-Aniotz, C., Diaz-Espinoza, R., Camacho, M. V., and Soto, C. (2012) Protein misfolding cyclic amplification of infectious prions. Nat. Protoc. 7, 1397-1409
15. Wang, F., Wang, X., and Ma, J. (2011) Conversion of bacterially expressed recombinant prion protein. Methods 53, 208-213
16. Wang, F., Yang, F., Hu, Y., Wang, X., Jin, C., and Ma, J. (2007) Lipid interaction converts prion protein to a PrPSc-like proteinase K-resistant conformation under physiological conditions. Biochemistry 46, 7045-7053
17. Wang, F., Yin, S., Wang, X., Zha, L., Sy, M. S., and Ma, J. (2010) Role of the highly conserved middle region of prion protein (PrP) in PrP-lipid interaction. Biochemistry 49, 8169-8176
18. Wang, X., Bowers, S. L., Wang, F., Pu, X. A., Nelson, R. J., and Ma, J. (2009) Cytoplasmic prion protein induces forebrain neurotoxicity. Biochim. Biophys. Acta 1792, 555-563
19. U.S. Centers for Disease Control and Prevention (2009) Prion diseases. In Biosafety in Microbiological and Biomedical Laboratories, 5th Ed. HHS Publication No. (CDC) 21-1112 (Closewood, L. C., and Wilson, D. E., eds) Sec. VIII-H, pp 282-289, U.S. Department of Health and Human Services, Washington, DC
20. Li, R., Liu, T., Wong, B. S., Pan, T., Morillas, M., Swietnicki, W., O'Rourke, K., Gambetti, P., Surewicz, W. K., and Sy, M. S. (2000) Identification of an epitope in the C terminus of normal prion protein whose expression is modulated by binding events in the N terminus. J. Mol. Biol. 301, 567-573
21. Yin, S., Pham, N., Yu, S., Li, C., Wong, P., Chang, B., Kang, S. C., Biasini, E., Tien, P., Harris, D. A., and Sy, M. S. (2007) Human prion proteins with pathogenic mutations share common conformational changes resulting in enhanced binding to glycosaminoglycans. Proc. Natl. Acad. Sci. U. S. A. 104, 7546-7551
22. Feraudet, C., Morel, N., Simon, S., Volland, H., Frobert, Y., Creminon, C., Vilette, D., Lehmann, S., and Grassi, J. (2005) Screening of 145 anti-PrP monoclonal antibodies for their capacity to inhibit PrPSc replication in infected cells. J. Biol. Chem. 280, 11247-11258
23. Parchi, P., Zou, W., Wang, W., Brown, P., Capellari, S., Ghetti, B., Kopp, N., Schulz-Schaeffer, W. J., Kretzschmar, H. A., Head, M. W., Ironside, J. W., Gambetti, P., and Chen, S. G. (2000) Genetic influence on the structural variations of the abnormal prion protein. Proc. Natl. Acad. Sci. U. S. A. 97, 10168-10172
24. Kang, H. E., Weng, C. C., Saijo, E., Saylor, V., Bian, J., Kim, S., Ramos, L., Angers, R., Langenfeld, K., Khaychuk, V., Calvi, C., Bartz, J., Hunter, N., and Telling, G. C. (2012) Characterization of conformation-dependent prion protein epitopes. J. Biol. Chem. 287, 37219-37232
25. Tamguney, G., Giles, K., Glidden, D. V., Lessard, P., Wille, H., Tremblay, P., Groth, D. F., Yehiely, F., Korth, C., Moore, R. C., Tatzelt, J., Rubinstein, E., Boucheix, C., Yang, X., Stanley, P., Lisanti, M. P., Dwek, R. A., Rudd, P. M., Moskovitz, J., Epstein, C. J., Cruz, T. D., Kuziel, W. A., Maeda, N., Sap, J., Ashe, K. H., Carlson, G. A., Tesseur, I., Wyss-Coray, T., Mucke, L., Weisgraber, K. H., Mahley, R. W., Cohen, F. E., and Prusiner, S. B. (2008) Genes contributing to prion pathogenesis. J. Gen. Virol. 89, 1777-1788
26. Kim, J. I., Cali, I., Surewicz, K., Kong, Q., Raymond, G. J., Atarashi, R., Race, B., Qing, L., Gambetti, P., Caughey, B., and Surewicz, W. K. (2010) Mammalian prions generated from bacterially expressed prion protein in the absence of any mammalian cofactors. J. Biol. Chem. 285, 14083-14087
27. Legname, G., Baskakov, I. V., Nguyen, H. O., Riesner, D., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (2004) Synthetic mammalian prions. Science 305, 673-676
28. Colby, D. W., Wain, R., Baskakov, I. V., Legname, G., Palmer, C. G., Nguyen, H. O., Lemus, A., Cohen, F. E., DeArmond, S. J., and Prusiner, S. B. (2010) Protease-sensitive synthetic prions. PLoS Pathog. 6, e1000736
29. Makarava, N., Kovacs, G. G., Bocharova, O., Savtchenko, R., Alexeeva, I., Budka, H., Rohwer, R. G., and Baskakov, I. V. (2010) Recombinant prion protein induces a new transmissible prion disease in wild-type animals. Acta Neuropathol. 119, 177-187
30. Ma, J. (2012) The role of cofactors in prion propagation and infectivity. PLoS Pathog. 8, e1002589
31. Kazlauskaite, J., Sanghera, N., Sylvester, I., Venien-Bryan, C., and Pinheiro, T. J. (2003) Structural changes of the prion protein in lipid membranes leading to aggregation and fibrillization. Biochemistry 42, 3295-3304
32. Kazlauskaite, J., and Pinheiro, T. J. (2005) Aggregation and fibrillization of prions in lipid membranes. Biochem. Soc. Symp. 72, 211-222
33. Morillas, M., Swietnicki, W., Gambetti, P., and Surewicz, W. K. (1999) Membrane environment alters the conformational structure of the recombinant human prion protein. J. Biol. Chem. 274, 36859-36865
34. Gomes, M. P., Millen, T. A., Ferreira, P. S., e Silva, N. L., Vieira, T. C., Almeida, M. S., Silva, J. L., and Cordeiro, Y. (2008) Prion protein complexed to N2a cellular RNAs through its N-terminal domain forms aggregates and is toxic to murine neuroblastoma cells. J. Biol. Chem. 283, 19616-19625
35. Adler, V., Zeiler, B., Kryukov, V., Kascsak, R., Rubenstein, R., and Grossman, A. (2003) Small, highly structured RNAs participate in the conversion of human recombinant PrP(Sen) to PrP(Res) in vitro. J. Mol. Biol. 332, 47-57
36. Wang, F., and Ma, J. (2013) Role of lipid in forming an infectious prion? Acta Biochim. Biophys. Sin. (Shanghai) 45, 485-493
37. Barria, M. A., Mukherjee, A., Gonzalez-Romero, D., Morales, R., and Soto, C. (2009) De novo generation of infectious prions in vitro produces a new disease phenotype. PLoS Pathog. 5, e1000421
38. Makarava, N., and Baskakov, I. V. (2008) The same primary structure of the prion protein yields two distinct self-propagating states. J. Biol. Chem. 283, 15988-15996
39. Saa, P., Castilla, J., and Soto, C. (2006) Presymptomatic detection of prions in blood. Science 313, 92-94
40. Castilla, J., Saa, P., and Soto, C. (2005) Detection of prions in blood. Nat. Med. 11, 982-985
41. Gonzalez-Romero, D., Barria, M. A., Leon, P., Morales, R., and Soto, C. (2008) Detection of infectious prions in urine. FEBS Lett. 582, 3161-3166
42. Aguzzi, A. (2009) Cell biology: beyond the prion principle. Nature 459, 924-925
43. Aguzzi, A., and Rajendran, L. (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64, 783-790
44. Brundin, P., Melki, R., and Kopito, R. (2010) Prion-like transmission of protein aggregates in neurodegenerative diseases. Nat. Rev. Mol. Cell Biol. 11, 301-307
45. Polymenidou, M., and Cleveland, D. W. (2011) The seeds of neurodegeneration: prion-like spreading in ALS. Cell 147, 498-508
46. Polymenidou, M., and Cleveland, D. W. (2012) Prion-like spread of protein aggregates in neurodegeneration. J. Exp. Med. 209, 889-893
47. Prusiner, S. B. (2012) Cell biology. A unifying role for prions in neurodegenerative diseases. Science 336, 1511-1513
48. Soto, C. (2012) Transmissible proteins: expanding the prion heresy. Cell 149, 968-977