A DNA-promoted amyloid proteinopathy in Escherichia coli

Molecular Microbiology

Volumn 77, Issue 6, 2010, Pages 1456-1469

  Fernández Tresguerres, M Elena ^a   Moreno Díaz De La Espina, Susana ^a   Gasset Rosa, Fátima ^a   Giraldo, Rafael ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; DNA; ESCHERICHIA COLI PROTEIN; HYBRID PROTEIN; PROTEIN REPA; RED FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR WH1; UNCLASSIFIED DRUG; WINGED HELIX TRANSCRIPTION FACTOR;

ARTICLE; CONTROLLED STUDY; CYTOKINESIS; DNA SEQUENCE; ESCHERICHIA COLI; GENE FUSION; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN VARIANT;

AMINO ACID SEQUENCE; AMYLOID; BASE SEQUENCE; DNA HELICASES; DNA, BACTERIAL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE FUSION; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; TRANS-ACTIVATORS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MAMMALIA;

EID: 77956631474     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2010.07299.x     Document Type: Article

References (63)

1. Abid, K., Morales, R. Soto, C. (2010) Cellular factors implicated in prion replication. FEBS Lett 584: 2409 2414.
2. Anand, S.P. Khan, S.A. (2010) Plasmid segregation: birds of a feather try not to flock together. J Bacteriol 192: 1171 1174.
3. Bauer, P.O. Nukina, N. (2009) The pathogenic mechanism of polyglutamine diseases and current therapeutic strategies. J Neurochem 110: 1737 1765.
4. Bellotti, V. Chiti, F. (2008) Amyloidogenesis in its biological environment: challenging a fundamental issue in protein misfolding diseases. Curr Opin Struct Biol 18: 771 779.
5. Boehr, D.D., Nussinov, R. Wright, P.E. (2009) The role of dynamic conformational ensembles in biomolecular recognition. Nat Chem Biol 5: 789 796.
6. Byrne, L.J., Cole, D.J., Cox, B.S., Ridout, M.S., Morgan, B.J.T. Tuite, M.F. (2009) The number and transmission of [PSI+] seeds (propagons) in the yeast Saccharomyces cerevisiae. PLoS ONE 4: e4670.
7. Cherny, D., Hoyer, W., Subramaniam, V. Jovin, T.M. (2004) Double-stranded DNA stimulates the fibrillation of α-synuclein in vitro and is associated with the mature fibrils: an electron microscopy study. J Mol Biol 344: 929 938.
8. Chiti, F. Dobson, C.M. (2006) Protein misfolding, functional amyloid, and human disease. Annu Rev Biochem 75: 333 366.
9. Cobb, N.J. Surewicz, W.K. (2009) Prion diseases and their biochemical mechanisms. Biochemistry 48: 2574 2585.
10. Cordeiro, Y., Machado, F., Juliano, L., Juliano, M.A., Brentani, R.R., Foguel, D. Silva, J.L. (2001) DNA converts cellular prion protein into the β-sheet conformation and inhibits prion peptide aggregation. J Biol Chem 276: 49400 49409.
11. Davidson, C.J. Surette, M.G. (2008) Individuality in bacteria. Annu Rev Genet 42: 253 268.
12. De Groot, N.S., Sabaté, R. Ventura, S. (2009) Amyloids in bacterial inclusion bodies. Trends Biochem Sci 34: 408 416.
13. De Lorenzo, V. (2010) Synthetic biology: something old, something new. BioEssays 32: 267 270.
14. De Palmenaer, D., Siguier, P. Mahillon, J. (2008) IS4 family goes genomic. BMC Evol Biol 8: 18.
15. De Rooij, K.E., Dorsman, J.C., Smoor, M.A., Den Dunnen, J.T. Van Ommen, G.J.B. (1996) Subcellular localization of the Huntington's disease gene product in cell lines by immunofluorescence and biochemical subcellular fractionation. Hum Mol Genet 5: 1093 1099.
16. Deleault, N.R., Lucassen, R.W. Supattapone, S. (2003) RNA molecules stimulate prion protein conversion. Nature 425: 717 720.
17. Deleault, N.R., Harris, B.T., Rees, J.R. Supattapone, S. (2007) Formation of native prions from minimal components in vitro. Proc Natl Acad Sci USA 104: 9741 9746.
18. Deleault, N.R., Kascsak, R., Geoghegan, J.C. Supattapone, S. (2010) Species-dependent differences in cofactor utilization for formation of the protease-resistant prion protein in vitro. Biochemistry 49: 3928 3934.
19. Deplazes, A. (2009) Piecing together a puzzle: an exposition of synthetic biology. EMBO Rep 10: 428 432.
20. Díaz-López, T., Lages-Gonzalo, M., Serrano-López, A., Alfonso, C., Rivas, G., Díaz-Orejas, R. Giraldo, R. (2003) Structural changes in RepA, a plasmid replication initiator, upon binding to origin DNA. J Biol Chem 278: 18606 18616.
21. Díaz-López, T., Dávila-Fajardo, C., Blaesing, F., Lillo, M.P. Giraldo, R. (2006) Early events in the binding of the pPS10 replication protein RepA to single iteron and operator DNA sequences. J Mol Biol 364: 909 920.
22. Ferenci, T., Zhou, Z., Betteridge, T., Ren, Y., Liu, Y., Feng, L., et al. (2009) Genomic sequencing reveals regulatory mutations and recombinational events in the widely used MC4100 lineage of Escherichia coli K-12. J Bacteriol 191: 4025 4029.
23. Fernández-Tresguerres, M.E., Martín, M., García de Viedma, D., Giraldo, R. Díaz-Orejas, R. (1995) Host growth temperature and a conservative amino acid substitution in the replication protein of pPS10 influence plasmid host range. J Bacteriol 177: 4377 4384.
24. García-Fruitós, E., González-Montalbán, N., Morell, M., Vera, A., Ferraz, R.M., Arís, A., et al. (2005) Aggregation as bacterial inclusion bodies does not imply inactivation of enzymes and fluorescent proteins. Microb Cell Fact 4: 27.
25. Garrity, S.J., Sivanathan, V., Dong, J., Lindquist, S. Hochschild, A. (2010) Conversion of a yeast prion protein to an infectious form in bacteria. Proc Natl Acad Sci USA 107: 10596 10601.
26. Gasset-Rosa, F., Díaz-López, T., Lurz, R., Prieto, A., Fernández-Tresguerres, M.E. Giraldo, R. (2008a) Negative regulation of pPS10 plasmid replication: origin pairing by zipping-up DNA-bound RepA monomers. Mol Microbiol 68: 560 572.
27. Gasset-Rosa, F., Maté, M.J., Dávila-Fajardo, C., Bravo, J. Giraldo, R. (2008b) Binding of sulphonated indigo derivatives to RepA-WH1 inhibits DNA-induced protein amyloidogenesis. Nucleic Acids Res 36: 2249 2256.
28. Geoghegan, J.C., Valdes, P.A., Orem, N.R., Deleault, N.R., Williamson, R.A., Harris, B.T. Supattapone, S. (2007) Selective incorporation of polyanionic molecules into hamster prions. J Biol Chem 282: 36341 36353.
29. Giraldo, R. (2007) Defined DNA sequences promote the assembly of a bacterial protein into distinct amyloid nanostructures. Proc Natl Acad Sci USA 104: 17388 17393.
30. Giraldo, R. Fernández-Tresguerres, M.E. (2004) Twenty years of the pPS10 replicon: insights on the molecular mechanism for the activation of DNA replication in iteron-containing bacterial plasmids. Plasmid 52: 69 83.
31. Giraldo, R., Fernández-Tornero, C., Evans, P.R., Díaz-Orejas, R. Romero, A. (2003) A conformational switch between transcriptional repression and replication initiation in the RepA dimerization domain. Nat Struct Biol 10: 565 571.
32. Hegde, M.L., Vasudevaraju, P. Rao, K.J. (2010) DNA induced folding/fibrillation of alpha-synuclein: new insights in Parkinson's disease. Front Biosci 15: 418 436.
33. Knowles, T.P.J., Waudby, C.A., Devlin, G.L., Cohen, S.I.A., Aguzzi, A., Vendruscolo, M., et al. (2009) An analytical solution to the kinetics of breakable filament assembly. Science 326: 1533 1537.
34. Krishnan, R. Lindquist, S.L. (2005) Structural insights into a yeast prion illuminate nucleation and strain diversity. Nature 435: 765 772.
35. Liebman, S.W., Bagriantsev, S.N. Derkatch, I.L. (2006) Biochemical and genetic methods for characterization of [PIN+] prions in yeast. Methods 39: 23 34.
36. Lindner, A.B., Madden, R., Demarez, A., Stewart, E.J. Taddei, F. (2008) Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA 105: 3076 3081.
37. Mangé, A., Crozet, C., Lehmann, S. Béranger, F. (2004) Scrapie-like prion protein is translocated to the nuclei of infected cells independently of proteasome inhibition and interacts with chromatin. J Cell Sci 117: 2411 2416.
38. Martínez-Alonso, M., González-Montalbán, N., García-Fruitós, E. Villaverde, A. (2009) Learning about protein solubility from bacterial inclusion bodies. Microb Cell Fact 8: 4.
39. Montero-Llopis, P., Jackson, A.F., Sliusarenko, O., Surovtsev, I., Heinritz, J., Emonet, T. Jacobs-Wagner, C. (2010) Spatial organization of the flow of genetic information in bacteria. Nature 466: 77 81.
40. Morell, M., Bravo, R., Espargaró, A., Sisquella, X., Avilés, F.X., Fernández-Busquets, X. Ventura, S. (2008) Inclusion bodies: specificity in their aggregation process and amyloid-like structure. Biochim Biophys Acta 1783: 1815 1825.
41. Morris, D.M. Jensen, G.J. (2008) Toward a biomechanical understanding of whole bacterial cells. Annu Rev Biochem 77: 583 613.
42. Nandi, P.K., Leclerc, E., Nicole, J.C. Takahashi, M. (2002) DNA-induced partial unfolding of prion protein leads to its polymerisation to amyloid. J Mol Biol 322: 153 161.
43. Otzen, D. Nielsen, P.H. (2008) We find them here, we find them there: functional bacterial amyloid. Cell Mol Life Sci 65: 910 927.
44. Pogliano, J., Ho, T.Q., Zhong, Z. Helinski, D.R. (2001) Multicopy plasmids are clustered and localized in Escherichia coli. Proc Natl Acad Sci USA 98: 4486 4491.
45. Robert, L., Paul, G., Chen, Y., Taddei, F., Baigl, D. Lindner, A.B. (2010) Pre-dispositions and epigenetic inheritance in the Escherichia coli lactose operon bistable switch. Mol Syst Biol 6: 357.
46. Rogoza, T., Goginashvili, A., Rodionova, S., Viktorovskaya, O., Rubel, A., Volkov, K. Mironova, L. (2010) Non-Mendelian determinant [ISP+] in yeast is a nuclear-residing prion form of the global transcriptional regulator Sfp1. Proc Natl Acad Sci USA 107: 10573 10577.
47. Rokney, A., Shagan, M., Kessel, M., Smith, Y., Rosenshine, I. Oppenheim, A.B. (2009) E. coli transports aggregated proteins to the poles by a specific and energy-dependent process. J Mol Biol 392: 589 601.
48. Sawaya, M.R., Sambashivan, S., Nelson, R., Ivanova, M.I., Sievers, S.A., Apostol, M.I., et al. (2007) Atomic structures of amyloid cross-βspines reveal varied steric zippers. Nature 447: 453 457.
49. Shanner, N.C., Campbell, R.E., Steinbach, P.A., Giepmans, B.N., Palmer, A.E. Tsien, R.Y. (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22: 1567 1572.
50. Shorter, J. Lindquist, S. (2008) Hsp104, Hsp70 and Hsp40 interplay regulates formation, growth and elimination of Sup35 prions. EMBO J 27: 2712 2724.
51. Silva, J.L., Lima, L.M., Foguel, D. Cordeiro, Y. (2008) Intriguing nucleic-acid-binding features of mammalian prion protein. Trends Biochem Sci 33: 132 140.
52. Simonian, M.H. Smith, J.A. (2006) Spectrophotometric and colorimetric determination of protein concentration. Curr Protoc Mol Biol 76: 10.1.A.1 10.1.A.9.
53. Sindi, S.S. Serio, T.R. (2009) Prion dynamics and the quest for the genetic determinant in protein-only inheritance. Curr Opin Microbiol 12: 623 630.
54. Stewart, E.J., Madden, E., Paul, G. Taddei, F. (2005) Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol 3: e45.
55. Tessier, P.M. Lindquist, S. (2009) Unraveling infectious structures, strain variants and species barriers for the yeast prion [PSI+]. Nat Struct Mol Biol 16: 598 605.
56. Tyedmers, J., Treusch, S., Dong, J., McCaffery, J.M., Bevis, B. Lindquist, S. (2010) Prion induction involves an ancient system for the sequestration of aggregated proteins and heritable changes in prion fragmentation. Proc Natl Acad Sci USA 107: 8633 8638.
57. Wang, F., Wang, X., Yuan, C.G. Ma, J. (2010) Generating a prion with bacterially expressed recombinant prion protein. Science 327: 1132 1135.
58. Wang, L., Maji, S.K., Sawaya, M.R., Eisenberg, D. Riek, R. (2008) Bacterial inclusion bodies contain amyloid-like structure. PLoS Biol 6: e195.
59. Wasmer, C., Benkemoun, L., Sabaté, R., Steinmetz, M.O., Coulary-Salin, B., Wang, L., et al. (2009) Solid-state NMR spectroscopy reveals that E. coli inclusion bodies of HET-s(218-289) are amyloids. Angew Chem Int Ed Engl 48: 4858 4860.
60. Wickner, R.B., Edskes, H.K., Shewmaker, F. Nakayashiki, T. (2007) Prions of fungi: inherited structures and biological roles. Nat Rev Microbiol 5: 611 618.
61. Wiltzius, J.J.W., Landau, M., Nelson, R., Sawaya, M.R., Apostol, M.I., Goldschmidt, L., et al. (2009) Molecular mechanisms for protein-encoded inheritance. Nat Struct Mol Biol 16: 973 979.
62. Winkler, J., Seybert, A., König, L., Pruggnaller, S., Haselmann, U., Sourjik, V., et al. (2010) Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J 29: 910 923.
63. Wu, C., Wang, Z., Lei, H., Duan, Y., Bowers, M.T. Shea, J.E. (2008) The binding of thioflavin T and its neutral analog BTA-1 to protofibrils of the Alzheimer's disease Aβ(16-22) peptide probed by molecular dynamics simulations. J Mol Biol 384: 718 729.