Biochemistry (Moscow)

, Volume 81, Issue 1, pp 34–46 | Cite as

Proteomic analysis of Escherichia coli protein fractions resistant to solubilization by ionic detergents

  • K. S. Antonets
  • K. V. Volkov
  • A. L. Maltseva
  • L. M. Arshakian
  • A. P. Galkin
  • A. A. Nizhnikov
Article

Abstract

Amyloids are protein fibrils adopting structure of cross-beta spine exhibiting either pathogenic or functionally significant properties. In prokaryotes, there are several groups of functional amyloids; however, all of them were identified by specialized approaches that do not reveal all cellular amyloids. Here, using our previously developed PSIA (Proteomic Screening and Identification of Amyloids) approach, we have conducted a proteomic screening for candidates for novel amyloid-forming proteins in Escherichia coli as one of the most important model organisms and biotechnological objects. As a result, we identified 61 proteins in fractions resistant to treatment with ionic detergents. We found that a fraction of proteins bearing potentially amyloidogenic regions predicted by bioinformatics algorithms was 3-5-fold more abundant among the identified proteins compared to those observed in the entire E. coli proteome. Almost all identified proteins contained potentially amyloidogenic regions, and four of them (BcsC, MukB, YfbK, and YghJ) have asparagineand glutamine-rich regions underlying a crucial feature of many known amyloids. In this study, we demonstrate for the first time that at the proteome level there is a correlation between experimentally demonstrated detergent-resistance of proteins and potentially amyloidogenic regions predicted by bioinformatics approaches. The data obtained enable further comprehensive characterization of entirety of amyloids (or amyloidome) in bacterial cells.

Keywords

amyloid prion E. coli fimbria curlin amyloidomics 

Abbreviations

2D-DIGE

two-dimensional difference gel electrophoresis

DRAF

detergent-resistant aggregate fraction

DTT

dithiothreitol

LC-MALDI

liquid chromatography coupled to matrix-assisted laser desorption/ionization mass-spectrometry

PSIA

proteomic screening and identification of amyloids

SDS-PAGE

one-dimensional gel electrophoresis according to Laemmli

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References

  1. 1.
    Nizhnikov, A. A., Antonets, K. S., and Inge-Vechtomov, S. G. (2015) Amyloids: from pathogenesis to function, Biochemistry (Moscow), 80, 1127–1144.CrossRefGoogle Scholar
  2. 2.
    Sipe, J. D., Benson, M. D., Buxbaum, J. N., Ikeda, S., Merlini, G., Saraiva, M. J., and Westermark, P. (2014) Nomenclature 2014: amyloid fibril proteins and clinical classification of amyloidosis, Amyloid, 21, 221–224.CrossRefPubMedGoogle Scholar
  3. 3.
    Si, K., Giustetto, M., Etkin, A., Hsu, R., Janisiewicz, A. M., Miniaci, M. C., Kim, J. H., Zhu, H., and Kandel, E. R. (2003) A neuronal isoform of CPEB regulates local protein synthesis and stabilizes synapse-specific long-term facilitation in Aplysia, Cell, 115, 893–904.CrossRefPubMedGoogle Scholar
  4. 4.
    Majumdar, A., Cesario, W. C., White-Grindley, E., Jiang, H., Ren, F., Khan, M. R., Li, L., Choi, E. M., Kannan, K., Guo, F., Unruh, J., Slaughter, B., and Si, K. (2012) Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory, Cell, 148, 515–529.CrossRefPubMedGoogle Scholar
  5. 5.
    Fowler, D. M., Koulov, A. V., Alory-Jost, C., Marks, M. S., Balch, W. E., and Kelly, J. W. (2006) Functional amyloid formation within mammalian tissue, PLoS Biol., 4, e6.PubMedCentralCrossRefPubMedGoogle Scholar
  6. 6.
    Maji, S. K., Perrin, M. H., Sawaya, M. R., Jessberger, S., Vadodaria, K., Rissman, R. A., Singru, P. S., Nilsson, K. P., Simon, R., Schubert, D., Eisenberg, D., Rivier, J., Sawchenko, P., Vale, W., and Riek, R. (2009) Functional amyloids as natural storage of peptide hormones in pituitary secretory granules, Science, 325, 328–332.PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Bolton, D. C., McKinley, M. P., and Prusiner, S. B. (1982) Identification of a protein that purifies with the scrapie prion, Science, 218, 1309–1311.CrossRefPubMedGoogle Scholar
  8. 8.
    Wickner, R. B. (1994) [URE3] as an altered Ure2 protein: evidence for a prion analog in Saccharomyces cerevisiae, Science, 264, 566–569.CrossRefPubMedGoogle Scholar
  9. 9.
    Wickner, R., Masison, D. C., and Edskes, H. K. (1995) [PSI] and [URE3] as yeast prions, Yeast, 11, 1671–1685.CrossRefPubMedGoogle Scholar
  10. 10.
    Derkatch, I. L., Bradley, M. E., Hong, J. Y., and Liebman, S. W. (2001) Prions affect the appearance of other prions. The story of [PIN(+)], Cell, 106, 171–182.CrossRefPubMedGoogle Scholar
  11. 11.
    Du, Z., Park, K. W., Yu, H., Fan, Q., and Li, L. (2008) Newly identified prion linked to the chromatin-remodeling factor Swi1 in Saccharomyces cerevisiae, Nat. Genet., 40, 460–465.PubMedCentralCrossRefPubMedGoogle Scholar
  12. 12.
    Patel, B. K., Gavin-Smyth, J., and Liebman, S. W. (2009) The yeast global transcriptional co-repressor protein Cyc8 can propagate as a prion, Nat. Cell Biol., 11, 344–349.PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Alberti, S., Halfmann, R., King, O., Kapila, A., and Lindquist, S. (2009) A systematic survey identifies prions and illuminates sequence features of prionogenic proteins, Cell, 137, 146–158.PubMedCentralCrossRefPubMedGoogle Scholar
  14. 14.
    Rogoza, T., Goginashvili, A., Rodionova, S., Ivanov, M., Viktorovskaya, O., Rubel, A., Volkov, K., and Mironova, L. (2010) Non-Mendelian determinant [ISP +] in yeast is a nuclear-residing prion form of the global transcriptional regulator Sfp1, PNAS, 107, 10573–10577.PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Saifitdinova, A. F., Nizhnikov, A. A., Lada, A. G., Rubel, A. A., Magomedova, Z. M., Ignatova, V. V., IngeVechtomov, S. G., and Galkin, A. P. (2010) [NSI+]: a novel non-Mendelian nonsense suppressor determinant in Saccharomyces cerevisiae, Curr. Genet., 56, 467–478.CrossRefPubMedGoogle Scholar
  16. 16.
    Nizhnikov, A. A., Magomedova, Z. M., Rubel, A. A., Kondrashkina, A. M., Inge-Vechtomov, S. G., and Galkin, A. P. (2012) [NSI+] determinant has a pleiotropic phenotypic manifestation that is modulated by SUP35, SUP45, and VTS1 genes, Curr. Genet., 58, 35–47.CrossRefPubMedGoogle Scholar
  17. 17.
    Nizhnikov, A. A., Magomedova, Z. M., Saifitdinova, A. F., Inge-Vechtomov, S. G., and Galkin, A. P. (2012) Identification of genes encoding potentially amyloidogenic proteins that take part in the regulation of nonsense suppression in yeast Saccharomyces cerevisiae, Russ. J. Genet. Appl. Res., 2, 398–404.CrossRefGoogle Scholar
  18. 18.
    Nizhnikov, A. A., Kondrashkina, A. M., and Galkin, A. P. (2013) Interactions of [NSI+] prion-like determinant with SUP35 and VTS1 genes in Saccharomyces cerevisiae, Russ. J. Genet., 49, 1004–1012.CrossRefGoogle Scholar
  19. 19.
    Suzuki, G., Shimazu, N., and Tanaka, M. (2012) A yeast prion, Mod5, promotes acquired drug resistance and cell survival under environmental stress, Science, 336, 355–359.CrossRefPubMedGoogle Scholar
  20. 20.
    Holmes, D. L., Lancaster, A. K., Lindquist, S., and Halfmann, R. (2013) Heritable remodeling of yeast multicellularity by an environmentally responsive prion, Cell, 153, 153–165.PubMedCentralCrossRefPubMedGoogle Scholar
  21. 21.
    Nizhnikov, A. A., Antonets, K. S., Inge-Vechtomov, S. G., and Derkatch, I. L. (2014) Modulation of efficiency of translation termination in Saccharomyces cerevisiae: turning nonsense into sense, Prion, 8, 247–260.PubMedCentralCrossRefPubMedGoogle Scholar
  22. 22.
    Roberts, B. T., and Wickner, R. B. (2003) Heritable activity: a prion that propagates by covalent autoactivation, Genes Dev., 17, 2083–2087.PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Chapman, M. R., Robinson, L. S., Pinkner, J. S., Roth, R., Heuser, J., Hammar, M., Normark, S., and Hultgren, S. J. (2002) Role of Escherichia coli curli operons in directing amyloid fiber formation, Science, 295, 851–855.PubMedCentralCrossRefPubMedGoogle Scholar
  24. 24.
    Oh, J., Kim, J.-G., Jeon, E., Yoo, C.-H., Moon, J. S., Rhee, S., and Hwang, I. (2007) Amyloidogenesis of type III-dependent hairpins from plant pathogenic bacteria, J. Biol. Chem., 282, 13601–13609.CrossRefPubMedGoogle Scholar
  25. 25.
    Claessen, D., Rink, R., De Jong, W., Siebring, J., De Vreugd, P., Boersma, F. G., Dijkhuizen, L., and Wosten, H. A. (2003) A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils, Genes Dev., 17, 1714–1726.PubMedCentralCrossRefPubMedGoogle Scholar
  26. 26.
    Bieler, S., Estrada, L., Lagos, R., Baeza, M., Castilla, J., and Soto, C. (2005) Amyloid formation modulates the biological activity of a bacterial protein, J. Biol. Chem., 280, 26880–26885.CrossRefPubMedGoogle Scholar
  27. 27.
    Wang, R., Braughton, K. R., Kretschmer, D., Bach, T.-H., Queck, S. Y., Li, M., Kennedy, A. D., Dorward, D. W., Klebanoff, S. J., Peschel, A., DeLeo, F. R., and Otto, M. (2007) Identification of novel cytolytic peptides as key virulence determinants for community-associated MRSA, Nat. Med., 13, 1510–1514.CrossRefPubMedGoogle Scholar
  28. 28.
    Bavdek, A., Kostanjsek, R., Antonini, V., Lakey, J. H., Dalla Serra, M., Gilbert, R. J. C., and Anderluh, G. (2012) pH dependence of listeriolysin O aggregation and poreforming ability, FEBS J., 279, 126–141.CrossRefPubMedGoogle Scholar
  29. 29.
    Chimileski, S., Franklin, M. J., and Papke, R. T. (2014) Biofilms formed by the archaeon Haloferax volcanii exhibit cellular differentiation and social motility, and facilitate horizontal gene transfer, BMC Biol., 12, 65.PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Nizhnikov, A. A., Alexandrov, A. I., Ryzhova, T. A., Mitkevich, O. V., Dergalev, A. A., Ter-Avanesyan, M. D., and Galkin, A. P. (2014) Proteomic screening for amyloid proteins, PLoS One, 9, e116003.Google Scholar
  31. 31.
    Maurer-Stroh, S., Debulpaep, M., Kuemmerer, N., Lopez de la Paz, M., Martins, I. C., Reumers, J., Morris, K. L., Copland, A., Serpell, L., Serrano, L., Schymkowitz, J. W., and Rousseau, F. (2010) Exploring the sequence determinants of amyloid structure using position-specific scoring matrices, Nat. Methods, 7, 237–242.CrossRefPubMedGoogle Scholar
  32. 32.
    Antonets, K. S., and Nizhnikov, A. A. (2013) SARP: a novel algorithm to assess compositional biases in protein sequences, Evol. Bioinform., 9, 263–273.Google Scholar
  33. 33.
    Woodcock, D. M., Crowther, P. J., Doherty, J., Jefferson, S., De Cruz, E., Noyer-Weidner, M., Smith, S. S., Michael, M. Z., and Graham, M. W. (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants, Nucleic Acids Res., 17, 3469–3478.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Miroux, B., and Walker, J. E. (1996) Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels, J. Mol. Biol., 19, 289–298.CrossRefGoogle Scholar
  35. 35.
    Kryndushkin, D., Pripuzova, N., Burnett, B. G., and Shewmaker, F. (2013) Non-targeted identification of prions and amyloid-forming proteins from yeast and mammalian cells, J. Biol. Chem., 288, 27100–27111.PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    Ma, J., and Lindquist, S. (1999) De novo generation of a PrPSc-like conformation in living cells, Nat. Cell. Biol., 1, 358–361.CrossRefPubMedGoogle Scholar
  37. 37.
    Bagriantsev, S., and Liebman, S. (2006) Modulation of Abeta42 low-n oligomerization using a novel yeast reporter system, BMC Biol., 4, 32.PubMedCentralCrossRefPubMedGoogle Scholar
  38. 38.
    Rubel, A. A., Saifitdinova, A. F., Lada, A. G., Nizhnikov, A. A., Inge-Vechtomov, S. G., and Galkin, A. P. (2008) Yeast chaperone Hspl04 regulates gene expression on the posttranscriptional level, Mol. Biol. (Moscow), 42, 123–130.CrossRefGoogle Scholar
  39. 39.
    Majumdar, A., Cesario, W. C., White-Grindley, E., Jiang, H., Ren, F., Khan, M. R., Li, L., Choi, E. M., Kannan, K., Guo, F., Unruh, J., Slaughter, B., and Si, K. (2012) Critical role of amyloid-like oligomers of Drosophila Orb2 in the persistence of memory, Cell, 148, 515–529.CrossRefPubMedGoogle Scholar
  40. 40.
    Pilsl, H., and Braun, V. (1995) Evidence that the immunity protein inactivates colicin 5 immediately prior to the formation of the transmembrane channel, J. Bacteriol., 177, 6966–6972.PubMedCentralPubMedGoogle Scholar
  41. 41.
    Lillington, J., Geibel, S., and Waksman, G. (2014) Biogenesis and adhesion of type 1 and P pili, Biochim. Biophys. Acta, 1840, 2783–2793.CrossRefPubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2016

Authors and Affiliations

  • K. S. Antonets
    • 1
    • 2
  • K. V. Volkov
    • 1
  • A. L. Maltseva
    • 1
  • L. M. Arshakian
    • 1
  • A. P. Galkin
    • 1
    • 2
  • A. A. Nizhnikov
    • 1
    • 2
  1. 1.Department of Genetics and BiotechnologySt. Petersburg State UniversitySt. PetersburgRussia
  2. 2.Vavilov Institute of General Genetics, St. Petersburg BranchRussian Academy of SciencesSt. PetersburgRussia

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