Skip to main content
SpringerLink
Log in

The Legionella pneumophila Chaperonin 60 and the Art of Keeping Several Moonlighting Jobs

  • Chapter
  • First Online:
Moonlighting Cell Stress Proteins in Microbial Infections

Part of the book series: Heat Shock Proteins ((HESP,volume 7))

Abstract

The title of this chapter intends to emphasize the fact that, as the essential chaperonin 60 of the bacterial pathogen Legionella pneumophila, HtpB has a main day job in protein folding, in addition to several alternate night jobs, depending on where it is located. The alternate virulence-related jobs that we have described for HtpB include the interaction with host cell surface receptors (which results in signaling and a variety of host cell responses), attraction of host cell mitochondria, modification of the host cell actin cytoskeleton, induction of bacterial filamentation, and interaction with specific host cell proteins, i.e. S-adenosyl methionine decarboxylase (which plays a role in the synthesis of host cell polyamines). These alternate HtpB jobs were primarily discovered as strong phenotypes after expression of recombinant HtpB in bacteria, yeast and mammalian cells. It is fascinating that HtpB possesses the extraordinary ability to functionally adapt to the disparate cellular environments of prokaryotic and eukaryotic cells. Although we have not yet been able to decipher the molecular basis for this adaptation, HtpB stands out as an artful moonlighting chaperonin capable of serving several night jobs.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allan DS (2002) Secretion of Hsp60 chaperonins (GroEL) homologs by Legionella pneumophila. MSc thesis, Dalhousie University, Halifax, NS, Canada

    Google Scholar 

  • Al-Quadan T, Abu Kwaik Y (2011) Molecular characterization of exploitation of the polyubiquitination and farnesylation machineries of Dictiostelium discoideum by the AnkB F-box effector of Legionella pneumophila. Front Microbiol 2:23. doi:10.3389/fmicb.2011.00023

    Article  CAS  PubMed  Google Scholar 

  • Al-Quadan T, Price CT, Abu Kwaik Y (2012) Exploitation of evolutionarily conserved amoeba and mammalian processes by Legionella. Trends Microbiol 20:299–306

    Article  CAS  PubMed  Google Scholar 

  • Atkinson PH, Summers DF (1971) Purification and properties of HeLa cell plasma membranes. J Biol Chem 246:5162–5175

    CAS  PubMed  Google Scholar 

  • Becker T, Böttinger L, Pfanner N (2012) Mitochondrial protein import: from transport pathways to an integrated network. Trends Biochem Sci 37:85–91

    Article  CAS  PubMed  Google Scholar 

  • Bethke K, Staib F, Distler M, Schmitt U, Jonuleit H, Enk AH, Galle PR, Heike M (2002) Different efficiency of heat shock proteins (HSP) to activate human monocytes and dendritic cells: superiority of Hsp60. J Immunol 169:6141–6148

    CAS  PubMed  Google Scholar 

  • Blander SJ, Horwitz MA (1993) Major cytoplasmic membrane protein of Legionella pneumophila, a genus common antigen and member of the hsp 60 family of heat shock proteins, induces protective immunity in a guinea pig model of Legionnaires’ disease. J Clin Invest 91:717–723

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty P, Sturgill-Koszycki S, Russell DG (1994) Isolation and characterization of pathogen-containing phagosomes. Methods Cell Biol 45:261–276

    Article  CAS  PubMed  Google Scholar 

  • Chong A, Riveroll A, Allan DS, Garduño E, Garduño RA (2006) The Hsp60 chaperonin of Legionella pneumophila: an intriguing player in infection of host cells. In: Cianciotto NP, Abu Kwaik Y, Edelstein PH, Fields BS, Geary DF, Harrison TG, Joseph CA, Ratcliff RM, Stout JE, Swanson MS (eds) Legionella: state of the art 30 years after its recognition. ASM Press, Washington, DC, pp 255–260

    Google Scholar 

  • Chong A, Lima CA, Allan DS, Nasrallah GK, Garduño RA (2009) The purified and recombinant Legionella pneumophila chaperonin alters mitochondrial trafficking and microfilament organization. Infect Immun 77:4724–4739

    Article  CAS  PubMed  Google Scholar 

  • Cox JV, Naher N, Abdelrahman YM, Belland RJ (2012) Host HDL biogenesis machinery is recruited to the inclusion of Chlamydia trachomatis-infected cells and regulates chlamydial growth. Cell Microbiol 14:1497–1512

    Article  CAS  PubMed  Google Scholar 

  • England J, Lucent D, Pande V (2008) Rattling the cage: computational models of chaperonin-mediated protein folding. Curr Opin Struct Biol 18:163–169

    Article  CAS  PubMed  Google Scholar 

  • Ensminger AW, Isberg RR (2009) Legionella pneumophila Dot/Icm translocated substrates: a sum of parts. Curr Opin Microbiol 12:67–73

    Article  CAS  PubMed  Google Scholar 

  • Fernandez RC, Logan SM, Lee SH, Hoffman PS (1996) Elevated levels of Legionella pneumophila stress protein Hsp60 early in infection of human monocytes and L929 cells correlate with virulence. Infect Immun 64:1968–1976

    CAS  PubMed  Google Scholar 

  • Franco IS, Shohdy N, Shuman HA (2012) The Legionella pneumophila effector VipA is an actin nucleator that alters host cell organelle trafficking. PLoS Pathog 8:e1002546. doi:10.1371/journal.ppat.1002546

    Article  CAS  PubMed  Google Scholar 

  • Gabay JE, Horwitz MA (1985) Isolation and characterization of the cytoplasmic and outer membranes of the Legionnaires’ disease bacterium (Legionella pneumophila). J Exp Med 161:409–422

    Article  CAS  PubMed  Google Scholar 

  • Galka F, Wai SN, Kusch H, Engelmann S, Hecker M, Schmeck B, Hippenstiel S, Uhlin BE, Steinert M (2008) Proteomic characterization of the whole secretome of Legionella pneumophila and functional analysis of outer membrane vesicles. Infect Immun 76:1825–1836

    Article  CAS  PubMed  Google Scholar 

  • Garduño RA, Faulkner G, Trevors MA, Vats N, Hoffman PS (1998a) Immunolocalization of Hsp60 in Legionella pneumophila. J Bacteriol 180:505–513

    PubMed  Google Scholar 

  • Garduño RA, Garduño E, Hoffman PS (1998b) Surface-associated Hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect Immun 66:4602–4610

    PubMed  Google Scholar 

  • Garduño RA, Garduño E, Hiltz M, Hoffman PS (2002) Intracellular growth of Legionella pneumophila gives rise to a differentiated form dissimilar to stationary phase forms. Infect Immun 70:6273–6283

    Article  PubMed  Google Scholar 

  • Garduño RA, Chong A, Nasrallah GK, Allan DS (2011) The Legionella pneumophila chaperonin–an unusual multifunctional protein in unusual locations. Front Microbiol 2:122. doi:10.3389/fmicb.2011.00122

    Article  PubMed  Google Scholar 

  • Haenssler E, Isberg RR (2011) Control of host cell phosphorylation by Legionella pneumophila. Front Microbiol 2:64. doi:10.3389/fmicb.2011.00064

    Article  CAS  PubMed  Google Scholar 

  • Helsel LO, Bibb WF, Butler CA, Hoffman PS, McKinney RM (1988) Recognition of a genus-wide antigen of Legionella by a monoclonal-antibody. Curr Microbiol 16:201–208

    Article  CAS  Google Scholar 

  • Henderson B (2010) Integrating the cell stress response: a new view of molecular chaperones as immunological and physiological homeostatic regulators. Cell Biochem Funct 28:1–14

    Article  CAS  PubMed  Google Scholar 

  • Herrero AB, Lopez MC, Garcia S, Schmidt A, Spaltmann F, Ruiz-Herrera J, Dominguez A (1999) Control of filament formation in Candida albicans by polyamine levels. Infect Immun 67:4870–4878

    CAS  PubMed  Google Scholar 

  • Hoffman PS, Houston L, Butler CA (1990) Legionella pneumophila htpAB heat shock operon: nucleotide sequence and expression of the 60 kilodalton antigen in L. pneumophila-infected HeLa cells. Infect Immun 58:3380–3387

    CAS  PubMed  Google Scholar 

  • Horwich AL, Fenton WA, Chapman E, Farr GW (2007) Two families of chaperonin: physiology and mechanism. Annu Rev Cell Dev Biol 23:115–145

    Article  CAS  PubMed  Google Scholar 

  • Horwitz MA, Silverstein SC (1983) Intracellular multiplication of Legionnaires’ disease bacteria (Legionella pneumophila) in human monocytes is reversibly inhibited by erythromycin and rifampin. J Clin Investig 71:15–26

    Article  CAS  PubMed  Google Scholar 

  • Houry WA, Frishman D, Eckerskorn C, Lottspeich F, Hartl FU (1999) Identification of in vivo substrates of the chaperonin GroEL. Nature 402:147–154

    Article  CAS  PubMed  Google Scholar 

  • Hubber A, Roy CR (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26:261–283

    Article  CAS  PubMed  Google Scholar 

  • Isberg RR, O’Connor TJ, Heidtman M (2009) The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7:13–24

    Article  CAS  PubMed  Google Scholar 

  • Jin Y, Bok JW, Guzman-de-Peña D, Keller NP (2002) Requirement of spermidine for developmental transitions in Aspergillus nidulans. Mol Microbiol 46:801–812

    Article  CAS  PubMed  Google Scholar 

  • Kerner MJ, Naylor DJ, Ishihama Y, Maier T, Chang H-C, Stines A, Georgopoulos C, Frishman D, Hayer-Hartl M, Mann M, Hartl FU (2005) Proteome-wide analysis of chaperonin-dependent protein folding in Escherichia coli. Cell 122:209–220

    Article  CAS  PubMed  Google Scholar 

  • Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163–184

    Article  CAS  PubMed  Google Scholar 

  • Long KH, Gomez FJ, Morris RE, Newman SL (2003) Identification of heat shock protein 60 as the ligand on Histoplasma capsulatum that mediates binding to CD18 receptors on human macrophages. J Immunol 170:487–494

    CAS  PubMed  Google Scholar 

  • Luo Z-Q (2012) Legionella secreted effectors and innate immune responses. Cell Microbiol 14:19–27

    Article  PubMed  Google Scholar 

  • McClatchey AI, Fehon RG (2009) Merlin and the ERM proteins – regulators of receptor distribution and signaling at the cell cortex. Trends Cell Biol 19:198–206

    Article  PubMed  Google Scholar 

  • Nasrallah GK, Gagnon E, Orton DJ, Garduño RA (2011a) The htpAB operon of Legionella pneumophila cannot be deleted in the presence of the groE chaperonin operon of Escherichia coli. Can J Microbiol 57:943–952

    Article  CAS  PubMed  Google Scholar 

  • Nasrallah GK, Riveroll AL, Chong A, Murray LE, Lewis PJ, Garduño RA (2011b) Legionella pneumophila requires polyamines for optimal intracellular growth. J Bacteriol 193:4346–4360. Author correction for this paper: (2012) J Bacteriol 194:3032

    Google Scholar 

  • Neunuebel MR, Mohammadi S, Jarnik M, Machner MP (2012) Legionella pneumophila LidA affects nucleotide binding and activity of the host GTPase Rab1. J Bacteriol 194:1389–1400

    Article  CAS  PubMed  Google Scholar 

  • Newton HJ, Ang DKY, van Driel IR, Hartland EL (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23:274–298

    Article  CAS  PubMed  Google Scholar 

  • Ninio S, Roy CR (2007) Effector proteins translocated by Legionella pneumophila: strength in numbers. Trends Microbiol 15:372–380

    Article  CAS  PubMed  Google Scholar 

  • Nussbaum G, Zanin-Zhorov A, Quintana F, Lider O, Cohen IR (2006) Peptide p277 of HSP60 signals T cells: inhibition of inflammatory chemotaxis. Int Immunol 18:1413–1419

    Article  CAS  PubMed  Google Scholar 

  • Ohashi K, Burkhart V, Flohe S, Kolb H (2000) Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J Immunol 164:558–561

    CAS  PubMed  Google Scholar 

  • Piao Z, Sze CC, Barysheva O, Iida K-I, Yoshida S-I (2006) Temperature-regulated formation of mycelial mat-like biofilms by Legionella pneumophila. Appl Environ Microbiol 72:1613–1622

    Article  CAS  PubMed  Google Scholar 

  • Prashar A, Bhatia S, Tabatabaeiyazdi Z, Duncan C, Garduño RA, Tang P, Low D, Guyard C, Terebiznik MR (2012) Mechanism of invasion of lung epithelial cells by filamentous Legionella pneumophila. Cell Microbiol 14:1632–1655

    Article  CAS  PubMed  Google Scholar 

  • Retzlaff C, Yamamoto Y, Okubo S, Hoffman PS, Friedman H, Klein TW (1996) Legionella pneumophila heat-shock protein-induced increase of interleukin-1β mRNA involves protein kinase C signalling in macrophages. Immunology 89:281–288

    Article  CAS  PubMed  Google Scholar 

  • Riveroll AL (2005) The Legionella pneumophila chaperonin – an investigation of virulence-related roles in a yeast model. PhD thesis, Dalhousie University, Halifax, NS, Canada

    Google Scholar 

  • Roy CR, Berger KH, Isberg RR (1998) Legionella pneumophila DotA protein is required for early phagosome trafficking decisions that occur within minutes of bacterial uptake. Mol Microbiol 28:663–674

    Article  CAS  PubMed  Google Scholar 

  • Schmidt O, Pfanner N, Meisinger C (2010) Mitochondrial protein import: from proteomics to functional mechanisms. Nat Rev Mol Cell Biol 11:655–667

    Article  CAS  PubMed  Google Scholar 

  • Török Z, Horváth I, Goloubinoff P, Kovács E, Glatz A, Balogh G, Vigh L (1997) Evidence for a lipochaperonin: association of active protein-folding GroESL oligomers with lipids can stabilize membranes under heat shock. Proc Natl Acad Sci USA 94:2192–2197

    Article  PubMed  Google Scholar 

  • Vabulas RM, Ahmad-Nejad P, da Costa C, Miethke T, Kirschning CJ, Häcker H, Wagner H (2001) Endocytosed HSP60s use Toll-like receptor 2 (TLR2) and TLR4 to activate the Toll/Interleukin-1 receptor signaling pathway in innate immune cells. J Biol Chem 276:31332–31339

    Article  CAS  PubMed  Google Scholar 

  • Watarai M, Kim S, Erdenebaatar J, Makino S-I, Horiuchi M, Shirahata T, Sakeguchi S, Katamine S (2003) Cellular prion protein promotes Brucella infection into macrophages. J Exp Med 198:5–17

    Article  CAS  PubMed  Google Scholar 

  • Weber SS, Ragaz C, Reus K, Nyfeler Y, Hilbi H (2006) Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog 2:e46

    Article  PubMed  Google Scholar 

  • Winn WC Jr (1988) Legionnaires disease: historical perspective. Clin Microbiol Rev 1:60–81

    PubMed  Google Scholar 

  • Xu H-M, Gutmann DH (1998) Merlin differentially associates with the microtubule and actin cytoskeleton. J Neurosci Res 51:403–415

    Article  CAS  PubMed  Google Scholar 

  • Zorko M, Langel Ü (2005) Cell penetrating peptides: mechanism and kinetics of cargo delivery. Adv Drug Deliv Rev 57:529–545

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology and Immunology, Dalhousie University, Sir Charles Tupper Medical Building, 7th floor, 5850 College Street, Halifax, NS, Canada, B3H-1X5

    Rafael A. Garduño

  2. Department of Medicine – Division of Infectious Diseases, Dalhousie University, Halifax, NS, Canada

    Rafael A. Garduño

  3. Laboratory of Intracellular Parasites, NIAID, NIH Rocky Mountain Laboratories, Hamilton, MT, USA

    Audrey Chong

Authors
  1. Rafael A. Garduño
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Audrey Chong
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rafael A. Garduño .

Editor information

Editors and Affiliations

  1. Eastman Dental Institute, Div. Microbial Diseases, University College, London, Gray's Inn Road 256, London, WC1X 8LD, United Kingdom

    Brian Henderson

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer Science+Business Media Dordrecht

About this chapter

Cite this chapter

Garduño, R.A., Chong, A. (2013). The Legionella pneumophila Chaperonin 60 and the Art of Keeping Several Moonlighting Jobs. In: Henderson, B. (eds) Moonlighting Cell Stress Proteins in Microbial Infections. Heat Shock Proteins, vol 7. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-6787-4_9

Download citation

Publish with us

Policies and ethics

Search

Navigation