1887

Abstract

Nearly all bacterial species express two or more chaperonin genes. Recent data indicate that type I chaperonins may be key players in bacterial infections. This is partly due to the well-known contribution of chaperonins in cellular proteostasis, the latter being compromised during bacterial host infection. In addition to their protein-folding activity, it has been revealed that certain chaperonins also exhibit moonlighting functions that can contribute in different ways to bacterial pathogenicity. Examples range from inducing adhesion molecules in Chlamydophila pneumoniae to supporting intracellular survival in Mycobacterium tuberculosis and Leishmania donovani, to inducing cytokines in Helicobacter pylori to promoting antimicrobial resistance in Escherichia coli, amongst others. This article provides a thorough reviews of our current understanding of the different mechanisms involving type I chaperonins during bacteria–host interactions, and suggests new areas to be explored and the potential of finding new targets for fighting bacterial infections.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000811
2018-08-03
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jmm/67/9/1203.html?itemId=/content/journal/jmm/10.1099/jmm.0.000811&mimeType=html&fmt=ahah

References

  1. Ribet D, Cossart P. How bacterial pathogens colonize their hosts and invade deeper tissues. Microbes Infect 2015; 17:173–183 [View Article][PubMed]
    [Google Scholar]
  2. Vanghele M, Ganea E. The role of bacterial molecular chaperones in pathogen survival within the host. Rom J Biochem 2010; 47:87–100
    [Google Scholar]
  3. Lund PA. Multiple chaperonins in bacteria–why so many?. FEMS Microbiol Rev 2009; 33:785–800 [View Article][PubMed]
    [Google Scholar]
  4. Weiss C, Jebara F, Nisemblat S, Azem A. Dynamic complexes in the chaperonin-mediated protein folding cycle. Front Mol Biosci 2016; 3:1–8 [View Article][PubMed]
    [Google Scholar]
  5. Saibil H. Chaperone machines for protein folding, unfolding and disaggregation. Nat Rev Mol Cell Biol 2013; 14:630–642 [View Article][PubMed]
    [Google Scholar]
  6. Niforou K, Cheimonidou C, Trougakos IP. Molecular chaperones and proteostasis regulation during redox imbalance. Redox Biol 2014; 2:323–332 [View Article][PubMed]
    [Google Scholar]
  7. Lebrasseur N. Specialized chaperones. J Cell Biol 2006; 172:483 [View Article]
    [Google Scholar]
  8. Santra M, Farrell DW, Dill KA. Bacterial proteostasis balances energy and chaperone utilization efficiently. Proc Natl Acad Sci USA 2017; 114:E2654E2661 [View Article][PubMed]
    [Google Scholar]
  9. Fares MA. The evolution of protein moonlighting: adaptive traps and promiscuity in the chaperonins. Biochem Soc Trans 2014; 42:1709–1714 [View Article][PubMed]
    [Google Scholar]
  10. Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011; 475:324–332 [View Article][PubMed]
    [Google Scholar]
  11. Skjærven L, Cuellar J, Martinez A, Valpuesta JM. Dynamics, flexibility, and allostery in molecular chaperonins. FEBS Lett 2015; 589:2522–2532 [View Article][PubMed]
    [Google Scholar]
  12. Ranford JC, Henderson B. Chaperonins in disease: mechanisms, models, and treatments. Mol Pathol 2002; 55:209–213 [View Article][PubMed]
    [Google Scholar]
  13. Vilasi S, Bulone D, Caruso Bavisotto C, Campanella C, Marino Gammazza A et al. Chaperonin of group I: oligomeric spectrum and biochemical and biological implications. Front Mol Biosci 2017; 4:99 [View Article][PubMed]
    [Google Scholar]
  14. Tyagi NK, Fenton WA, Horwich AL. GroEL/GroES cycling: ATP binds to an open ring before substrate protein favoring protein binding and production of the native state. Proc Natl Acad Sci USA 2009; 106:20264–20269 [View Article][PubMed]
    [Google Scholar]
  15. Wang X, Chi H, Li S, Xu Y. Binding of CXCR4 transmembrane peptides to the bacterial chaperonin GroEL. Protein Pept Lett 2017; 24:962–968 [View Article][PubMed]
    [Google Scholar]
  16. Henderson B, Allan E, Coates AR. Stress wars: the direct role of host and bacterial molecular chaperones in bacterial infection. Infect Immun 2006; 74:3693–3706 [View Article][PubMed]
    [Google Scholar]
  17. Hennequin C, Porcheray F, Waligora-Dupriet A, Collignon A, Barc M et al. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 2001; 147:87–96 [View Article][PubMed]
    [Google Scholar]
  18. Kirk JA, Banerji O, Fagan RP. Characteristics of the Clostridium difficile cell envelope and its importance in therapeutics. Microb Biotechnol 2017; 10:76–90 [View Article][PubMed]
    [Google Scholar]
  19. Yamaguchi H, Osaki T, Kurihara N, Taguchi H, Hanawa T et al. Heat-shock protein 60 homologue of Helicobacter pylori is associated with adhesion of H. pylori to human gastric epithelial cells. J Med Microbiol 1997; 46:825–831 [View Article][PubMed]
    [Google Scholar]
  20. Zhou M, Zhu F, Li Y, Zhang H, Wu H. Gap1 functions as a molecular chaperone to stabilize its interactive partner Gap3 during biogenesis of serine-rich repeat bacterial adhesin. Mol Microbiol 2012; 83:866–878 [View Article][PubMed]
    [Google Scholar]
  21. Govender VS, Ramsugit S, Pillay M. Mycobacterium tuberculosis adhesins: potential biomarkers as anti-tuberculosis therapeutic and diagnostic targets. Microbiology 2014; 160:1821–1831 [View Article][PubMed]
    [Google Scholar]
  22. Hickey TB, Ziltener HJ, Speert DP, Stokes RW. Mycobacterium tuberculosis employs Cpn60.2 as an adhesin that binds CD43 on the macrophage surface. Cell Microbiol 2010; 12:1634–1647 [View Article][PubMed]
    [Google Scholar]
  23. Hagemann L, Gründel A, Jacobs E, Dumke R. The surface-displayed chaperones GroEL and DnaK of Mycoplasma pneumoniae interact with human plasminogen and components of the extracellular matrix. Pathog Dis 2017; 75: [View Article][PubMed]
    [Google Scholar]
  24. Sanderson-Smith ML, de Oliveira DM, Ranson M, McArthur JD. Bacterial plasminogen receptors: mediators of a multifaceted relationship. J Biomed Biotechnol 2012; 2012:1–14 [View Article][PubMed]
    [Google Scholar]
  25. Kaul G, Thippeswamy H. Role of heat shock proteins in diseases and their therapeutic potential. Indian J Microbiol 2011; 51:124–131 [View Article][PubMed]
    [Google Scholar]
  26. Friedland JS, Shattock R, Remick DG, Griffin GE. Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 1993; 91:58–62 [View Article][PubMed]
    [Google Scholar]
  27. Péchiné S, Hennequin C, Boursier C, Hoys S, Collignon A. Immunization using GroEL decreases Clostridium difficile intestinal colonization. PLoS One 2013; 8:e81112 [View Article][PubMed]
    [Google Scholar]
  28. Lin CY, Huang YS, Li CH, Hsieh YT, Tsai NM et al. Characterizing the polymeric status of Helicobacter pylori heat shock protein 60. Biochem Biophys Res Commun 2009; 388:283–289 [View Article][PubMed]
    [Google Scholar]
  29. Fan M, Rao T, Zacco E, Ahmed MT, Shukla A et al. The unusual mycobacterial chaperonins: evidence for in vivo oligomerization and specialization of function. Mol Microbiol 2012; 85:934–944 [View Article][PubMed]
    [Google Scholar]
  30. Joseph S, Yuen A, Singh V, Hmama Z. Mycobacterium tuberculosis Cpn60.2 (GroEL2) blocks macrophage apoptosis via interaction with mitochondrial mortalin. Biol Open 2017; 6:481–488 [View Article][PubMed]
    [Google Scholar]
  31. Sharma A, Rustad T, Mahajan G, Kumar A, Rao KV et al. Towards understanding the biological function of the unusual chaperonin Cpn60.1 (GroEL1) of Mycobacterium tuberculosis. Tuberculosis 2016; 97:137–146 [View Article][PubMed]
    [Google Scholar]
  32. Colineau L, Clos J, Moon KM, Foster LJ, Reiner NE. Leishmania donovani chaperonin 10 regulates parasite internalization and intracellular survival in human macrophages. Med Microbiol Immunol 2017; 206:235–257 [View Article][PubMed]
    [Google Scholar]
  33. Ghazaei C. Molecular chaperones impacts in growth, metabolism, pathogenicity and production of virulence factors in bacterial pathogen. Rev Med Microbiol 2018; 29:24–29
    [Google Scholar]
  34. Du Y, Lenz J, Arvidson CG. Global gene expression and the role of sigma factors in Neisseria gonorrhoeae in interactions with epithelial cells. Infect Immun 2005; 73:4834–4845 [View Article][PubMed]
    [Google Scholar]
  35. Castanié-Cornet MP, Bruel N, Genevaux P. Chaperone networking facilitates protein targeting to the bacterial cytoplasmic membrane. Biochim Biophys Acta 2014; 1843:1442–1456 [View Article][PubMed]
    [Google Scholar]
  36. Macchia G, Massone A, Burroni D, Covacci A, Censini S et al. The Hsp60 protein of Helicobacter pylori: structure and immune response in patients with gastroduodenal diseases. Mol Microbiol 1993; 9:645–652 [View Article][PubMed]
    [Google Scholar]
  37. Cehovin A, Coates AR, Hu Y, Riffo-Vasquez Y, Tormay P et al. Comparison of the moonlighting actions of the two highly homologous chaperonin 60 proteins of Mycobacterium tuberculosis. Infect Immun 2010; 78:3196–3206 [View Article][PubMed]
    [Google Scholar]
  38. Green ER, Mecsas J. Bacterial secretion systems: an overview. Microbiol Spectr 2016; 4: [View Article][PubMed]
    [Google Scholar]
  39. Graubner W, Schierhorn A, Brüser T. DnaK plays a pivotal role in Tat targeting of CueO and functions beside SlyD as a general Tat signal binding chaperone. J Biol Chem 2007; 282:7116–7124 [View Article][PubMed]
    [Google Scholar]
  40. Li H, Chang L, Howell JM, Turner RJ. DmsD, a Tat system specific chaperone, interacts with other general chaperones and proteins involved in the molybdenum cofactor biosynthesis. Biochim Biophys Acta 2010; 1804:1301–1309 [View Article][PubMed]
    [Google Scholar]
  41. Ghazaei C. Role and mechanism of the Hsp70 molecular chaperone machines in bacterial pathogens. J Med Microbiol 2017; 66:259–265 [View Article][PubMed]
    [Google Scholar]
  42. Cardoso K, Gandra RF, Wisniewski ES, Osaku CA, Kadowaki MK et al. DnaK and GroEL are induced in response to antibiotic and heat shock in Acinetobacter baumannii. J Med Microbiol 2010; 59:1061–1068 [View Article][PubMed]
    [Google Scholar]
  43. Lund PA. Microbial molecular chaperones. Adv Microb Physiol 2001; 44:93-140[PubMed]
    [Google Scholar]
  44. Lenz G, Ron EZ. Novel interaction between the major bacterial heat shock chaperone (GroESL) and an RNA chaperone (CspC). J Mol Biol 2014; 426:460–466 [View Article][PubMed]
    [Google Scholar]
  45. Goltermann L, Sarusie MV, Bentin T. Chaperonin GroEL/GroES Over-expression promotes aminoglycoside resistance and reduces drug susceptibilities in Escherichia coli following exposure to sublethal aminoglycoside doses. Front Microbiol 2015; 6:1572 [View Article][PubMed]
    [Google Scholar]
  46. Williams TA, Codoñer FM, Toft C, Fares MA. Two chaperonin systems in bacterial genomes with distinct ecological roles. Trends Genet 2010; 26:47–51 [View Article][PubMed]
    [Google Scholar]
  47. Fayet O, Ziegelhoffer T, Georgopoulos C. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol 1989; 171:1379–1385 [View Article][PubMed]
    [Google Scholar]
  48. Sugimoto S, Abdullah-Al-Mahin, Sonomoto K. Molecular chaperones in lactic acid bacteria: physiological consequences and biochemical properties. J Biosci Bioeng 2008; 106:324–336 [View Article][PubMed]
    [Google Scholar]
  49. Abdeen S, Salim N, Mammadova N, Summers CM, Frankson R et al. GroEL/ES inhibitors as potential antibiotics. Bioorg Med Chem Lett 2016; 26:3127–3134 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000811
Loading
/content/journal/jmm/10.1099/jmm.0.000811
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error