Abstract
In both prokaryotes and eukaryotes, the survival at temperatures considerably exceeding the optimum is supported by intense synthesis of the so-called heat shock proteins (HSPs), which act to overcome the adverse effects of heat stress. Among mycoplasmas (class Mollicutes), which have significantly reduced genomes, only some members of the Acholeplasmataceae family possess small HSPs of the α-crystallin type. Overproduction of a recombinant HSP IbpA (Hsp20) from the free-living mycoplasma Acholeplasma laidlawii was shown to increase the resistance of Escherichia coli to short-term heat shock. It has been long assumed that IbpA prevents protein aggregation and precipitation thereby increasing viability of E. coli cells. Several potential target proteins interacting with IbpA under heat stress were identified, including biosynthetic enzymes, enzymes of energy metabolism, and components of the protein synthesis machinery. Statistical analysis of physicochemical properties indicated that IbpA interaction partners significantly differ in molecular weight, charge, and isoelectric point from other members of the E. coli proteome. Upon shortterm exposure to increased temperature, IbpA was found to preferentially interact with high-molecularweight proteins having a pI of about 5.1, significantly lower than the typical values of E. coli proteins.
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Abbreviations
- HSP:
-
heat shock protein
- sHSP:
-
α-crystallin-type small heat shock protein
References
Lindquist S. 1986. The heat-shock response. Annu. Rev. Biochem. 55, 1151–1191.
Borchsenius S.N., Budantseva E.V., Vonsky M.S. 1990. The heat shock proteins of Acholeplasma laidlawii. Zentralbl. Bakteriol. Suppl. 20, 657–658.
Vishnyakov I.E., Borchsenius S.N. 2013. Mycoplasma heat shock proteins and their genes. Microbiology (Moscow). 82 (6), 653–667.
Borchsenius S.N., Vishnyakov I.E., Budantseva E.V., Vonsky M.S., Yakobs E., Lazarev V.N. 2008. a-Crystallin-type heat-shock protein from mycoplasma Acholeplasma laidlawii (Mollicutes). Cell Tissue Biol. (Moscow). 2 (4), 360–365.
Vishnyakov I.E., Levitskii S.A., Manuvera V.A., Lazarev V.N., Ayala J.A., Ivanov V.A., Snigirevskaya E.S., Komissarchik Y.Y., Borchsenius S.N. 2012. The identification and characterization of IbpA, a novel alphacrystallin-type heat shock protein from mycoplasma. Cell Stress Chaperones. 17, 171–180.
Lazarev V.N., Levitskii S.A., Basovskii Y.I., Chukin M.M., Akopian T.A., Vereshchagin V.V., Kostrjukova E.S., Kovaleva G.Y., Kazanov M.D., Malko D.B., Vitreschak A.G., Sernova N.V., Gelfand M.S., Demina I.A., Serebryakova M.V., et al. 2011. Complete genome and proteome of Acholeplasma laidlawii. J. Bacteriol. 193, 4943–4953.
Chernov V.M., Mouzykantov A.A., Baranova N.B., Medvedeva E.S., Grygorieva T.Yu., Trushin M.V., Vishnyakov I.E., Sabantsev A.V., Borchsenius S.N., Chernova O.A. 2014. Extracellular membrane vesicles secreted by mycoplasma Acholeplasma laidlawii PG8 are enriched in virulence proteins. J. Proteomics. 110, 117–128.
Horwitz J. 1992. alpha-Crystallin can function as a molecular chaperone. Proc. Natl. Acad. Sci. U. S. A. 89, 10449–10453.
Jakob U., Gaestel M., Engel K., Buchner J. 1993. Small heat shock proteins are molecular chaperones. J. Biol. Chem. 268, 1517–1520.
Wong P., Houry W.A. 2004. Chaperone networks in bacteria: Analysis of protein homeostasis in minimal cells. J. Struct. Biol. 146, 79–89.
Horvath I., Glatz A., Varvasovszki V., Torok Z., Pali T., Balogh G., Kovacs E., Nidasdi L., Benki S., Joy F., Vigh L. 1998. Membrane physical state controls the signaling mechanism of the heat shock response in Synechocystis PCC 6803: Identification of hsp17 as a ‘fluidity gene’. Proc. Natl. Acad. Sci. U. S. A. 95, 3513–3518.
Tsvetkova N.M., Horvath I., Torok Z., Wolkers W.F., Balogi Z., Shigapova N., Crowe L.M., Tablin F., Vierling E., Crowe J.H., Vigh L. 2002. Small heat-shock proteins regulate membrane lipid polymorphism. Proc. Natl. Acad. Sci. U. S. A. 99, 13504–13509.
Mounier N., Arrigo A.-P. 2002. Actin cytoskeleton and small heat shock proteins: How do they interact? Cell Stress Chaperones. 7, 167–176.
Day R.M., Gupta J.S., MacRae T.H. 2003. A small heat shock/alpha-crystallin protein from encysted Artemia embryos suppresses tubulin denaturation. Cell Stress Chaperones. 8, 183–193.
Horvath I., Multhoff G., Sonnleitner A., Vigh L. 2008. Membrane-associated stress proteins: More than simply chaperones. Biochem. Biophys. Acta. 1778, 1653–1664.
Kocabiyik S. 2009. Essential structural and functional features of small heat shock proteins in molecular chaperoning process. Protein Pept. Lett. 16, 613–622.
Mymrikov E.V., Seit-Nebi A.S., Gusev N.B. 2011. Large potentials of small heat shock proteins. Physiol. Rev. 91, 1123–1159.
Basha E., O’Neill H., Vierling E. 2012. Small heat shock proteins and alpha-crystallins: Dynamic proteins with flexible functions. Trends Biochem. Sci. 37, 106–117.
Renaudin J., Breton M., Citti C. 2014. Molecular genetics tools for Mollicutes. In: Mollicutes: Molecular Biology and Pathogenesis. Eds. Browning G.F., Citti C. Norfolk, UK: Horizon Scientific Press, pp. 55–76.
Dybvig K., Cassell G.H. 1987. Transposition of grampositive transposon Tn916 in Acholeplasma laidlawii and Mycoplasma pulmonis. Science. 235, 1392–1394.
Dybvig K. 1989. Transformation of Acholeplasma laidlawii with streptococcal plasmids pVA868 and pVA920. Plasmid. 21, 155–160.
Sundström T.K., Wieslander A. 1990. Plasmid transformation and replica filter plating of Acholeplasma laidlawii. FEMS Microbiol. Lett. 60, 147–151.
Soto A., Allona I., Collada C., Guevara M.A., Casado R., Rodriguez-Cerezo E., Aragoncillo C., Gomez L. 1999. Heterologous expression of a plant small heat-shock protein enhances Escherichia coli viability under heat and cold stress. Plant Physiol. 120, 521–528.
Mogk A., Deuerling E., Vorderwulbecke S., Vierling E., Bukau B. 2003. Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol. Microbiol. 50, 585–595.
Kayumov A., Heinrich A., Fedorova K., Ilinskaya O., Forchhammer K. 2011. Interaction of the general transcription factor TnrA with the PII-like protein GlnK and glutamine synthetase in Bacillus subtilis. FEBS J. 278, 1779–1789.
Laemmli U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227, 680–685.
Wan K.X., Vidavsky I., Gross M.L. 2002. Comparing similar spectra: From similarity index to spectral contrast angle. J. Am. Soc. Mass Spectrom. 13, 85–88.
Krasichkov A.S., Grigoriev E.B., Bogachev M.I., Nifontov E.M. 2015. Shape anomaly detection under strong measurement noise: An analytical approach to adaptive thresholding. Phys. Rev. E92, 042927.
Yeh C.H., Chang P.F.L., Yeh K.W., Lin W.C., Chen Y.M., Lin C.Y. 1997. Expression of a gene encoding a 16.9-kDa heat-shock protein, Oshsp16.9, in Escherichia coli enhances thermotolerance. Proc. Natl. Acad. Sci. U. S. A. 94, 10967–10972.
Treweek T.M., Meehan S., Ecroyd H., Carver J.A. 2015. Small heat-shock proteins: Important players in regulating cellular proteostasis. Cell Mol. Life Sci. 72, 429–451.
Friedrich K.L., Giese K.C., Buan N.R., Vierling E. 2004. Interactions between small heat shock protein subunits and substrate in small heat shock protein-substrate complexes. J. Biol. Chem. 279, 1080–1089.
Haslbeck M., Weinkauf S., Buchner J. 2015. Regulation of the chaperone function of small Hsps. In: The Big Book on Small Heat Shock Proteins. Eds. Tanguay R.M., Hightower L.E. Switzerland: Springer, pp. 155–178.
Lee G.J., Roseman A.M., Saibil H.R., Vierling E. 1997. A small heat shock protein stably binds heat denatured model substrates and can maintain a substrate in a folding competent state. EMBO J. 16, 659–671.
Delbecq S.P., Klevit R.E. 2013. One size does not fit all: The oligomeric states of aB crystallin. FEBS Lett. 587, 1073–1080.
Braun N., Zacharias M., Peschek J., Kastenmuller A., Zou J., Hanzlik M., Haslbeck M., Rappsilber J., Buchner J., Weinkauf S. 2011. Multiple molecular architectures of the eye lens chaperone aB-crystallin elucidated by a triple hybrid approach. Proc. Natl. Acad. Sci. U. S. A. 108, 20491–20496.
Leroux M.R., Ma B.J., Batelier G., Melki R., Candido E.P.M. 1997. Unique structural features of a novel class of small heat shock proteins. J. Biol. Chem. 272, 12847–12853.
Dudkina E., Kayumov A., Ulyanova V., Ilinskaya O. 2014. New insight into secreted ribonuclease structure: Binase is a natural dimer. PLoS ONE. 9, e115818.
Heinrich A., Woyda K., Brauburger K., Meiss G., Detsch C., Stülke J., Forchhammer K. 2006. Interaction of the membrane-bound GlnK–AmtB complex with the master regulator of nitrogen metabolism TnrA in Bacillus subtilis. J. Biol. Chem. 281, 34909–34917.
Kayumov A., Heinrich A., Sharipova M., Iljinskaya O., Forchhammer K. 2008. Inactivation of the general transcription factor TnrA in Bacillus subtilis by proteolysis. Microbiology. 154, 2348–2355.
Bepperling A., Alte F., Kriehuber T., Braun N., Weinkauf S., Groll M., Haslbeck M., Buchner J. 2012. Alternative bacterial two-component small heat shock protein systems. Proc. Natl. Acad. Sci. U. S. A. 109, 20407–20412.
Sturm N., Jortzik E., Mailu B.M., Koncarevic S., Deponte M., Forchhammer K., Rahlfs S., Becker K. 2009. Identification of proteins targeted by the thioredoxin superfamily in Plasmodium falciparum. PLoS Pathog. 5, e1000383.
Reyes-Del Valle J., Chávez-Salinas S., Medina F., Del Angel R.M. 2005. Heat shock protein 90 and heat shock protein 70 are components of dengue virus receptor complex in human cells. J. Virol. 79, 4557–4567.
Arifuzzaman M., Maeda M., Itoh A., Nishikata K., Takita C., Saito R., Ara T., Nakahigashi K., Huang H.C., Hirai A., Tsuzuki K., Nakamura S., Altaf- Ul-Amin M., Oshima T., Baba T., et al. 2006. Large-scale identification of protein-protein interaction of Escherichia coli K-12. Genome Res. 16, 686–691.
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Original Russian Text © A.R. Kayumov, M.I. Bogachev, V.A. Manuvera, V.N. Lazarev, A.V. Sabantsev, T.O. Artamonova, S.N. Borchsenius, I.E. Vishnyakov, 2017, published in Molekulyarnaya Biologiya, 2017, Vol. 51, No. 00000, pp. 00000–00000.
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Kayumov, A.R., Bogachev, M.I., Manuvera, V.A. et al. Recombinant small heat shock protein from Acholeplasma laidlawii increases the Escherichia coli viability in thermal stress by selective protein rescue. Mol Biol 51, 112–121 (2017). https://doi.org/10.1134/S0026893317010083
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DOI: https://doi.org/10.1134/S0026893317010083