Skip to main content
SpringerLink
Log in

Bacterial Cold Shock Proteins as a Tool in Adaption to Stress

  • REVIEW ARTICLE
  • Published:
Russian Journal of Bioorganic Chemistry Aims and scope Submit manuscript

Abstract

Bacteria have evolved a number of ways for a coping with stress and adapting to changing environmental conditions. A family of bacterial proteins which contain a functional cold shock domain involves highly conserved compounds. They bind nucleic acids and modulate transcription and posttranscriptional events in bacteria. The cold shock proteins have been shown to regulate the expression of various genes that are involved in virulence and resistance of many bacteria to stress. This review discusses new data on the actions and role of the cold shock proteins in the regulation of expression in intracellular bacterial pathogens.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.

REFERENCES

  1. Link, T.M., Valentin-Hansen, P., and Brennana, R.G., Proc. Natl. Acad. Sci. U. S. A., 2009, vol. 106, pp. 19292–19297. https://doi.org/10.1073/PNAS.0908744106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Vogel, J. and Luisi, B.F., Nat. Rev. Microbiol., 2011, vol. 9, pp. 578–589. https://doi.org/10.1038/NRMICRO2615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Smirnov, A., Forstner, K.U., Holmqvist, E., Otto, A., Gunster, R., Becher, D., Reinhardt, R., and Vogel, J., Proc. Natl. Acad. Sci. U. S. A., 2016, vol. 113, pp. 11591–11596. https://doi.org/10.1073/pnas.1609981113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Smirnov, A., Wang, C., Drewry, L.L., and Vogel, J., EMBO J., 2017, vol. 36, pp. 1029–1045. https://doi.org/10.15252/EMBJ.201696127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ermolenko, D.N. and Makhatadze, G.I., Cell. Mol. Life Sci., 2002, vol. 59, pp. 1902–1913. https://doi.org/10.1007/PL00012513

    Article  CAS  PubMed  Google Scholar 

  6. Schindelin, H., Jiang, W., Inouye, M., and Heinemann, U., Proc. Natl. Acad. Sci. U. S. A., 1994, vol. 91, pp. 5119–5123. https://doi.org/10.1073/PNAS.91.11.5119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Rennella, E., Sára, T., Juen, M., Wunderlich, C., Imbert, L., Solyom, Z., Favier, A., Ayala, I., Weinhäupl, K., Schanda, P., Konrat, R., Kreutz, C., and Brutscher, B., Nucleic Acids Res., 2017, vol. 45, pp. 4255–4268. https://doi.org/10.1093/NAR/GKX044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Horn, G., Hofweber, R., Kremer, W., and Kalbitzer, H.R., Cell. Mol. Life Sci., 2007, vol. 64, pp. 1457–1470. https://doi.org/10.1007/S00018-007-6388-4

    Article  CAS  PubMed  Google Scholar 

  9. Goldstein, J., Pollitt, N.S., and Inouye, M., Proc. Natl. Acad. Sci. U. S. A., 1990, vol. 87, pp. 283–287. https://doi.org/10.1073/PNAS.87.1.283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Yamanaka, K. and Inouye, M., J. Bacteriol., 1997, vol. 179, pp. 5126–5130. https://doi.org/10.1128/JB.179.16.5126-5130.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Yu, T., Keto-Timonen, R., Jiang, X., Virtanen, J.P., and Korkeala, H., Int. J. Mol. Sci., 2019, vol. 20, p. 4059. https://doi.org/10.3390/IJMS20164059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Jiang, W., Hou, Y., and Inouye, M., J. Biol. Chem., 1997, vol. 272, pp. 196–202. https://doi.org/10.1074/JBC.272.1.196

    Article  CAS  PubMed  Google Scholar 

  13. Giangrossi, M., Gualerzi, C.O., and Pon, C.L., Biochimie, 2001, vol. 83, pp. 251–259. https://doi.org/10.1016/S0300-9084(01)01233-0

    Article  CAS  PubMed  Google Scholar 

  14. Jones, P.G., Krah, R., Tafuri, S.R., and Wolffe, A.P., J. Bacteriol., 1992, vol. 174, pp. 5798–5802. https://doi.org/10.1128/JB.174.18.5798-5802.1992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Bae, W., Xia, B., Inouye, M., and Severinov, K., Proc. Natl. Acad. Sci. U. S. A., 2000, vol. 97, pp. 7784–7789. https://doi.org/10.1073/pnas.97.14.7784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Bae, W., Jones, P.G., and Inouye, M., J. Bacteriol., 1997, vol. 179, pp. 7081–7088. https://doi.org/10.1128/JB.179.22.7081-7088.1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wu, L., Ma, L., Li, X., Huang, Z., and Gao, X., Mol. Plant Pathol., 2019, vol. 20, pp. 382–391. https://doi.org/10.1111/MPP.12763

    Article  CAS  PubMed  Google Scholar 

  18. la Teana, A., Brandi, A., Falconi, M., Spurio, R., Pon, C.L., and Gualerzi, C.O., Proc. Natl. Acad. Sci. U. S. A., 1991, vol. 88, pp. 10907–10911. https://doi.org/10.1073/PNAS.88.23.10907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Hwang, J., Severinov, K., Phadtare, S., and Inouye, M., Gen. Cells, 2003, vol. 8, pp. 801–810. https://doi.org/10.1046/j.1365-2443.2003.00675.x

    Article  CAS  Google Scholar 

  20. Caballero, C.J., Menendez-Gil, P., Catalan-Moreno, A., Vergara-Irigaray, M., Garcia, B., Segura, V., Irurzun, N., Villanueva, M., de Los, MozosI.R., Solano, C., Lasa, I., and Toledo-Arana, A., Nucleic Acids Res., 2018, vol. 46, p. 1345. https://doi.org/10.1093/NAR/GKX1284

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhang, Y., Burkhardt, D.H., Rouskin, S., Li, G.W., Weissman, J.S., and Gross, C.A., Mol. Cell, 2018, vol. 70, pp. 274–296.e7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Choi, J., Salvail, H., and Groisman, E.A., Nucleic Acids Res., 2021, vol. 49, pp. 11614–11628. https://doi.org/10.1016/J.MOLCEL.2018.02.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Hofweber, R., Horn, G., Langmann, T., Balbach, J., Kremer, W., Schmitz, G., and Kalbitzer, H.R., FEBS J., 2005, vol. 272, pp. 4691–4702. https://doi.org/10.1111/J.1742-4658.2005.04885.X

    Article  CAS  PubMed  Google Scholar 

  24. Faßhauer, P., Busche, T., Kalinowski, J., Mäder, U., Poehlein, A., Daniel, R., and Stülke, J., Microorganisms, 2021, vol. 9, p. 1434. https://doi.org/10.3390/microorganisms9071434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Michaux, C., Holmqvist, E., Vasicek, E., Sharan, M., Barquist, L., Westermann, A.J., Gunn, J.S., and Vogel, J., Proc. Natl. Acad. Sci. U. S. A., 2017, vol. 114, pp. 6824–6829. https://doi.org/10.1073/pnas.1620772114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Prezza, G., Ryan, D., Madler, G., Reichardt, S., Barquist, L., and Westermann, A.J., Mol. Microbiol., 2022, vol. 117, pp. 67–85. https://doi.org/10.1111/MMI.14793

    Article  CAS  PubMed  Google Scholar 

  27. Płociński, P., Macios, M., Houghton, J., Niemiec, E., Płocińska, R., Brzostek, A., Słomka, M., Dziadek, J., Young, D., and Dziembowski, A., Nucleic Acids Res., 2019, vol. 47, pp. 5892–5905. https://doi.org/10.1093/NAR/GKZ251

    Article  PubMed  PubMed Central  Google Scholar 

  28. Feng, Y., Huang, H., Liao, J., and Cohen, S.N., J. Biol. Chem., 2001, vol. 276, pp. 31651–31656. https://doi.org/10.1074/JBC.M102855200

    Article  CAS  PubMed  Google Scholar 

  29. Loepfe, C., Raimann, E., Stephan, R., and Tasara, T., Foodborne Pathogens Dis., 2010, vol. 7, pp. 775–783. https://doi.org/10.1089/FPD.2009.0458

    Article  CAS  Google Scholar 

  30. Schmid, B., Klumpp, J., Raimann, E., Loessner, M.J., Stephan, R., and Tasara, T., Appl. Environ. Microbiol., 2009, vol. 75, pp. 1621–1627. https://doi.org/10.1128/AEM.02154-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Eshwar, A.K., Guldimann, C., Oevermann, A., and Tasara, T., Front. Cell. Infect. Microbiol., 2017, vol. 7, p. 453. https://doi.org/10.3389/fcimb.2017.00453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Portnoy, D.A., Suzanne, JacksP., and Hinrichs, D.J., J. Exp. Med., 1988, vol. 167, pp. 1459–1471. https://doi.org/10.1084/JEM.167.4.1459

    Article  CAS  PubMed  Google Scholar 

  33. Slepkov, E.R., Bitar, A.P., and Marquis, H., Biochem. J., 2010, vol. 432, pp. 557–566. https://doi.org/10.1042/BJ20100557

    Article  CAS  PubMed  Google Scholar 

  34. Glomski, I.J., Gedde, M.M., Tsang, A.W., Swanson, J.A., and Portnoy, D.A., J. Cell Biol., 2002, vol. 156, pp. 1029–1038. https://doi.org/10.1083/JCB.200201081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Kocks, C., Gouin, E., Tabouret, M., Berche, P., Ohayon, H., and Cossart, P., Cell, 1992, vol. 68, pp. 521–531. https://doi.org/10.1016/0092-8674(92)90188-I

    Article  CAS  PubMed  Google Scholar 

  36. Welch, M.D., Iwamatsu, A., and Mitchison, T.J., Nature, 1997, vol. 385, pp. 265–269. https://doi.org/10.1038/385265a0

    Article  CAS  PubMed  Google Scholar 

  37. Travier, L., Guadagnini, S., Gouin, E., Dufour, A., Chenal-Francisque, V., Cossart, P., Olivo-Marin, J.C., Ghigo, J.M., Disson, O., and Lecuit, M., PLoS Pathog., 2013, vol. 9, p. e1003131. https://doi.org/10.1371/JOURNAL.PPAT.1003131

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Crawford, R.W., Rosales-Reyes, R., Ramirez-Aguilar, M.D.L.L., Chapa-Azuela, O., Alpuche-Aranda, C., and Gunn, J.S., Proc. Natl. Acad. Sci. U. S. A., 2010, vol. 107, pp. 4353–4358. https://doi.org/10.1073/pnas.1000862107

    Article  PubMed  PubMed Central  Google Scholar 

  39. Ray, S., Costa, R., Das, M., and Nandi, D., J. Biol. Chem., 2019, vol. 294, pp. 9084–9099. https://doi.org/10.1074/JBC.RA119.008209

    Article  PubMed  PubMed Central  Google Scholar 

  40. Batte, J.L., Samanta, D., and Elasri, M.O., Microbiology (Reading), 2016, vol. 162, pp. 575–589. https://doi.org/10.1099/MIC.0.000243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Pandey, S., Sahukhal, G.S., and Elasri, M.O., J. Bacteriol., 2019, vol. 201. https://doi.org/10.1128/JB.00417-19

  42. Wang, Z., Wang, S., and Wu, Q., FEMS Microbiol. Lett., 2014, vol. 354, pp. 27–36. https://doi.org/10.1111/1574-6968.12430

    Article  CAS  PubMed  Google Scholar 

  43. Wang, Z., Liu, W., Wu, T., Bie, P., and Wu, Q., Sci. China Life Sci., 2016, vol. 59, pp. 417–424. https://doi.org/10.1007/S11427-015-4981-6

    Article  CAS  PubMed  Google Scholar 

  44. Weldingh, K. and Andersen, P., FEMS Immunol. Med. Microbiol., 1999, vol. 23, pp. 159–164. https://doi.org/10.1111/J.1574-695X.1999.TB01235.X

    Article  CAS  PubMed  Google Scholar 

  45. D’Auria, G., Esposito, C., Falcigno, L., Calvanese, L., Iaccarino, E., Ruggiero, A., Pedone, C., Pedone, E., and Berisio, R., Biochem. Biophys. Res. Commun., 2010, vol. 402, pp. 693–698. https://doi.org/10.1016/J.BBRC.2010.10.086

    Article  PubMed  Google Scholar 

  46. Kumar, A., Alam, A., Tripathi, D., Rani, M., Khatoon, H., Pandey, S., Ehtesham, N.Z., and Hasnain, S.E., Semin. Cell Dev. Biol., 2018, vol. 84, pp. 147–157. https://doi.org/10.1016/J.SEMCDB.2018.01.003

    Article  CAS  PubMed  Google Scholar 

  47. Huang, L., Liu, W., Jiang, Q., Zuo, Y., Su, Y., Zhao, L., Qin, Y., and Yan, Q., Front. Cell. Infect. Microbiol., 2018, vol. 8, p. 207. https://doi.org/10.3389/FCIMB.2018.00207/BIBTEX

    Article  PubMed  PubMed Central  Google Scholar 

  48. Huang, L., Zhao, L., Qi, W., Xu, X., Zhang, J., Zhang, J., and Yan, Q., Aquaculture, 2020, vol. 518, p. 734861. https://doi.org/10.1016/J.AQUACULTURE.2019.734861

    Article  CAS  Google Scholar 

  49. Liu, Y., Tan, X., Cheng, H., Gong, J., Zhang, Y., Wang, D., and Ding, W., Microb. Pathog., 2020, vol. 142, p. 104091. https://doi.org/10.1016/J.MICPATH.2020.104091

    Article  CAS  PubMed  Google Scholar 

  50. Schwenk, S. and Arnvig, K.B., Pathogens Dis., 2018, vol. 76, p. 35. https://doi.org/10.1093/FEMSPD/FTY035

    Article  Google Scholar 

  51. Wexler, A.G. and Goodman, A.L., Nat. Microbiol., 2017, vol. 2, pp. 1–11. https://doi.org/10.1038/nmicrobiol.2017.26

    Article  CAS  Google Scholar 

Download references

Funding

This study was supported by the Russian Foundation for Basic Research, project no. 20-34-90149, “Post-graduates.”

Author information

Authors and Affiliations

  1. Shemyakin–Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, 117997, Moscow, Russia

    A. S. Grigorov & T. L. Azhikina

Authors
  1. A. S. Grigorov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. T. L. Azhikina
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. S. Grigorov.

Ethics declarations

The authors declare that they have no conflicts of interest.

This article does not contain any studies involving human participants and animals performed by any of the authors.

Additional information

Translated by L. Onoprienko

Abbreviations: CSD, the cold shock domain; CSP, the cold shock protein; RBP, the RNA binding protein; ncRNA, non-coding RNA; SD, the Shine–Dalgarno sequence.

Corresponding author; phone: +7 (495) 330-69-92.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grigorov, A.S., Azhikina, T.L. Bacterial Cold Shock Proteins as a Tool in Adaption to Stress. Russ J Bioorg Chem 49, 19–27 (2023). https://doi.org/10.1134/S1068162023010107

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1068162023010107

Keywords:

Search

Navigation