Bacterial Moonlighting Proteins and Bacterial Virulence

Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 358)

Abstract

Implicit in the central dogma is the hypothesis that each protein gene product has but one function. However, over the past decade, it has become clear that many proteins have one or more unique functions, over-and-above the principal biological action of the specific protein. This phenomenon is now known as protein moonlighting and many well-known proteins such as metabolic enzymes and molecular chaperones are now recognised as moonlighting proteins. A growing number of bacterial species are being found to have moonlighting proteins and the moonlighting activities of such proteins can contribute to bacterial virulence behaviour. The glycolytic enzymes, glyceraldehyde-3-phosphate dehydrogenase (GAPD) and enolase, and the cell stress proteins: chaperonin 60, Hsp70 and peptidyl prolyl isomerase, are among the most common of the bacterial moonlighting proteins which play a role in bacterial virulence. Moonlighting activities include adhesion and modulation of cell signalling processes. It is likely that only the tip of the bacterial moonlighting iceberg has been sighted and the next decade will bring with it many new discoveries of bacterial moonlighting proteins with a role in bacterial virulence.

Abbreviations

AFB

American foulbrood

AMF

Autocrine motility factor

ATP

Adenosine triphosphate

CD

Cluster of differentiation

Cpn

Chaperonin

DC-SIGN

Dendritic cell-specific intercellular adhesion molecule

ECM

Extracellular matrix

EMT

Epithelial-to-mesenchymal transition

ER

Endoplasmic reticulum

FBA

Fructose bisphosphate aldolase

FBP

Fibronectin-binding protein

FHL

Factor H-like (protein)

GAPD

Glyceraldehyde-3-phosphate dehydrogenase

GH-RH

Growth hormone releasing hormone

HDL

High-density lipoprotein

HGFR

Hepatocyte growth factor receptor

HSP

Heat shock protein

HtrA

High-temperature requirement

IFN-γ

Interferon-gamma

IRE

Iron-responsive elements

LAP

Listeria adhesion protein.

LCV

Legionella-containing vacuole

LDL

Low density lipoprotein

LPS

Lipopolysaccharide

MAP

Mitogen-activated protein (kinase)

MHC

Major histocompatibility complex

MIP

Macrophage infectivity potentiator

MyD

Myeloid differentiation factor

NFAT

Nuclear factor of activated T cells

ORF

Open reading frame

PFC

Protein-folding catalyst

6PGD

Phosphogluconate dehydrogenase

PGI

Phosphoglucoisomerase

PPD

Purified protein derivative

PPI

Peptidyl prolyl isomerase

SDH

Streptococcal surface dehydrogenase

STAT

Signal transducer and activator of transcription

TCA

Tricarboxylic acid cycle

TLR

Toll-like receptor

TPI

Triose phosphate isomerase

uPAR

Urokinase plasminogen activator receptor

VDAC

Voltage dependent anion channel

References

  1. Abou-Zeid C, Ratliff TL, Wiker HG, Harboe M, Bennedsen J, Rook GA (1988) Characterization of fibronectin-binding antigens released by Mycobacterium tuberculosis and Mycobacterium bovis BCG. Infect Immun 56:3046–3051PubMedGoogle Scholar
  2. Allignet J, England P, Old I El Solh N (2001) Several regions of the repeat domain of the Staphylococcus caprae autolysin, AtlC, are involved in fibronectin binding. FEMS Microbiol Lett 213:193–197CrossRefGoogle Scholar
  3. Alloush HM, López-Ribot JL, Masten BJ, Chaffin WL (1997) 3-phosphoglycerate kinase: a glycolytic enzyme protein present in the cell wall of Candida albicans. Microbiology 143:321–330PubMedCrossRefGoogle Scholar
  4. Alvarez-Dominguez C, Barbieri AM, Berón W, Wandinger-Ness A, Stahl PD (1996) Phagocytosed live Listeria monocytogenes influences Rab5-regulated in vitro phagosome-endosome fusion. J Biol Chem 271:13834–13843PubMedCrossRefGoogle Scholar
  5. Alvarez-Dominguez C, Madrazo-Toca F, Fernandez-Prieto L, Vandekerckhove J, Pareja E, Tobes R, Gomez-Lopez MT, Del Cerro-Vadillo E, Fresno M, Leyva-Cobián F, Carrasco-Marín E (2008) Characterization of a Listeria monocytogenes protein interfering with Rab5a. Traffic 9:325–337PubMedCrossRefGoogle Scholar
  6. Amini HR, Ascencio F, Ruiz-Bustos E, Romero MJ, Wadström T (1996) Cryptic domains of a 60 kDa heat shock protein of Helicobacter pylori bound to bovine lactoferrin. FEMS Immunol Med Microbiol 16:247–255PubMedCrossRefGoogle Scholar
  7. Amraei M, Nabi IR (2002) Species specificity of the cytokine function of phosphoglucose isomerase. FEBS Lett 525:151–155PubMedCrossRefGoogle Scholar
  8. Anand K, Mathur D, Anant A, Garg LC (2010) Structural studies of phosphoglucose isomerase from Mycobacterium tuberculosis H37Rv. Acta Crystallogr Sect F Struct Biol Cryst Commun 66:490–497PubMedCrossRefGoogle Scholar
  9. Antikainen J, Kuparinen V, Lähteenmäki K, Korhonen TK (2007) pH-dependent association of enolase and glyceraldehyde-3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids. J Bacteriol 189:4539–4543PubMedCrossRefGoogle Scholar
  10. Antúnez K, Anido M, Arredondo D, Evans JD, Zunino P (2011) Paenibacillus larvae enolase as a virulence factor in honeybee larvae infection. Vet Microbiol 87:83–89CrossRefGoogle Scholar
  11. Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ (2004) Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 117:3645–3657PubMedCrossRefGoogle Scholar
  12. Atanassov C, Pezennec L, d’Alayer J, Grollier G, Picard B, Fauchère JL (2002) Novel antigens of Helicobacter pylori correspond to ulcer-related antibody pattern of sera from infected patients. J Clin Microbiol 40:547–552PubMedCrossRefGoogle Scholar
  13. Attali C, Durmort C, Vernet T, Di Guilmi AM (2008) The interaction of Streptococcus pneumoniae with plasmin mediates transmigration across endothelial and epithelial monolayers by intercellular junction cleavage. Infect Immun 76:5350–5356PubMedCrossRefGoogle Scholar
  14. Ausiello CM, Fedele G, Palazzo R, Spensieri F, Ciervo A, Cassone A (2006) 60-kDa heat shock protein of Chlamydia pneumoniae promotes a T helper type 1 immune response through IL-12/IL-23 production in monocyte-derived dendritic cells. Microbes Infect 8:714–720PubMedCrossRefGoogle Scholar
  15. Babaahmady K, Oehlmann W, Singh M, Lehner T (2007) Inhibition of human immunodeficiency virus type 1 infection of human CD4+ T cells by microbial HSP70 and the peptide epitope 407–426. J Virol 81:3354–3360PubMedCrossRefGoogle Scholar
  16. Balasubramanian S, Kannan TR, Baseman JB (2008) The surface-exposed carboxyl region of Mycoplasma pneumoniae elongation factor Tu interacts with fibronectin. Infect Immun 76:3116–3123PubMedCrossRefGoogle Scholar
  17. Balasubramanian S, Kannan TR, Hart PJ, Baseman JB (2009) Amino acid changes in elongation factor Tu of Mycoplasma pneumoniae and Mycoplasma genitalium influence fibronectin binding. Infect Immun 77:3533–3541PubMedCrossRefGoogle Scholar
  18. Banerjee S, Nandyala AK, Raviprasad P, Ahmed N, Hasnain SE (2007) Iron-dependent RNA-binding activity of Mycobacterium tuberculosis aconitase. J Bacteriol 189:4046–4052PubMedCrossRefGoogle Scholar
  19. Basak C, Pathak SK, Bhattacharyya A, Pathak S, Basu J, Kundu M (2005) The secreted peptidyl prolyl cis, trans-isomerase HP0175 of Helicobacter pylori induces apoptosis of gastric epithelial cells in a TLR4- and apoptosis signal-regulating kinase 1-dependent manner. J Immunol 174:5672–5680PubMedGoogle Scholar
  20. Becker T, Hartl FU, Wieland F (2002) CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J Cell Biol 158:1277–1285PubMedCrossRefGoogle Scholar
  21. Beckmann C, Waggoner JD, Harris TO, Tamura GS, Rubens CE (2002) Identification of novel adhesins from Group B Streptococci by use of phage display reveals that C5a peptidase mediates fibronectin binding. Infect Immun 70:2869–2876PubMedCrossRefGoogle Scholar
  22. Belisle JT, Vissart VD, Sievert T, Takayama K, Brennan PJ, Besra GS (1997) Role of the major antigen of Mycobacterium tuberculosis in cell wall biogenesis. Science 276:1420–1422PubMedCrossRefGoogle Scholar
  23. Bergmann S, Rohde M, Chhatwal GS, Hammerschmidt S (2001) Α-enolase of Streptococcus pneumoniae is a plasmin(ogen)-binding protein displayed on the bacterial cell surface. Mol Microbiol 40:1273–1287PubMedCrossRefGoogle Scholar
  24. Bergmann S, Wild D, Diekmann O, Frank R, Bracht D, Chhatwal GS, Hammerschmidt S (2003) Identification of a novel plasmin(ogen)-binding motif in surface displayed alpha-enolase of Streptococcus pneumoniae. Mol Microbiol 49:411–423PubMedCrossRefGoogle Scholar
  25. Bergmann S, Rohde M, Hammerschmidt S (2004) Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pneumoniae is a surface-displayed plasminogen-binding protein. Infect Immun 72:2416–2419PubMedCrossRefGoogle Scholar
  26. Bergonzelli GE, Granato D, Pridmore RD, Marvin-Guy LF, Donnicola D, Corthésy-Theulaz IE (2006) GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect Immun 74:425–434PubMedCrossRefGoogle Scholar
  27. Blau K, Portnoi M, Shagan M, Kaganovich A, Rom S, Kafka D, Chalifa Caspi V, Porgador A, Givon-Lavi N, Gershoni JM, Dagan R, Mizrachi Y, Nebenzahl YM (2007) Flamingo cadherin: a putative host receptor for Streptococcus pneumoniae. J Infect Dis 195:1828–1837PubMedCrossRefGoogle Scholar
  28. Boël G, Jin H, Pancholi V (2005) Inhibition of cell surface export of group A streptococcal anchorless surface dehydrogenase affects bacterial adherence and antiphagocytic properties. Infect Immun 73:6237–6248PubMedCrossRefGoogle Scholar
  29. Bonazzi M, Lecuit M, Cossart P (2009) Listeria monocytogenes internalin and E-cadherin: from bench to bedside. Cold Spring Harb Perspect Biol 1:a003087PubMedCrossRefGoogle Scholar
  30. Bulut Y, Shimada K, Wong MH, Chen S, Gray P, Alsabeh R, Doherty TM, Crother TR, Arditi M (2009) Chlamydial heat shock protein 60 induces acute pulmonary inflammation in mice via the toll-like receptor 4- and MyD88-dependent pathway. Infect Immun 77:2683–2690PubMedCrossRefGoogle Scholar
  31. Burillo A, Bouza E (2010) Chlamydia pneumoniae. Infect Dis Clin North Am 24:61–71PubMedCrossRefGoogle Scholar
  32. Burkholder KM, Bhunia AK (2010) Listeria monocytogenes uses Listeria adhesion protein (LAP) to promote bacterial transepithelial translocation and induces expression of LAP receptor Hsp60. Infect Immun 78:5062–5073PubMedCrossRefGoogle Scholar
  33. Burnham C-AD, Shokoples SE, Tyrrell GJ (2005) Phosphoglycerate kinase inhibits epithelial cell invasion by group B streptococci. Microbe Pathog 38:189–200CrossRefGoogle Scholar
  34. Burton MJ, Mabey DC (2009) The global burden of trachoma: a review. PLoS Negl Trop Dis 3:e460PubMedCrossRefGoogle Scholar
  35. Campbell RM, Scanes CG (1995) Endocrine peptides ‘moonlighting’ as immune modulators: roles for somatostatin and GH-releasing factor. J Endocrinol 147:383–396PubMedCrossRefGoogle Scholar
  36. Candela M, Biagi E, Centanni M, Turroni S, Vici M, Musiani F, Vitali B, Bergmann S, Hammerschmidt S, Brigidi P (2009) Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiology 155:3294–3303PubMedCrossRefGoogle Scholar
  37. Candela M, Centanni M, Fiori J, Biagi E, Turroni S, Orrico C, Bergmann S, Hammerschmidt S, Brigidi P (2010) DnaK from Bifidobacterium animalis subsp. lactis is a surface-exposed human plasminogen receptor upregulated in response to bile salts. Microbiology 156:1609–1618PubMedCrossRefGoogle Scholar
  38. Capello M, Ferri-Borgogno S, Cappello P, Novelli F (2011) α-Enolase: a promising therapeutic and diagnostic tumor target. FEBS J [Epub ahead of print]Google Scholar
  39. Carroll MV, Sim RB, Bigi F, Jäkel A, Antrobus R, Mitchell DA (2010) Identification of four novel DC-SIGN ligands on Mycobacterium bovis BCG. Protein Cell 1:859–870PubMedCrossRefGoogle Scholar
  40. Castaldo C, Vastano V, Siciliano RA, Candela M, Vici M, Muscariello L, Marasco R, Sacco M (2009) Surface displaced alfa-enolase of Lactobacillus plantarum is a fibronectin-binding protein. Microb Cell Fact 8:14PubMedCrossRefGoogle Scholar
  41. Cehovin A, Coates AR, Riffo-Vasquez Y, Tormay P, Botanch C, Altare F, Henderson B (2010) Comparison of the moonlighting actions of the two highly homologous chaperonin 60 proteins of Mycobacterium tuberculosis. Infect Immun 78:3196–3206PubMedCrossRefGoogle Scholar
  42. Chaput M, Claes V, Portetelle D, Cludts I, Cravador A, Burny A, Gras H, Tartar A (1988) The neurotrophic factor neuroleukin is 90% homologous with phosphohexose isomerase. Nature 332:454–455PubMedCrossRefGoogle Scholar
  43. Chaturvedi R, Bansal K, Narayana Y, Kapoor N, Sukumar N, Togarsimalemath SK, Chandra N, Mishra S, Ajitkumar P, Joshi B, Katoch VM, Patil SA, Balaji KN (2010) The multifunctional PE_PGRS11 protein from Mycobacterium tuberculosis plays a role in regulating resistance to oxidative stress. J Biol Chem 285:30389–30403PubMedCrossRefGoogle Scholar
  44. 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 77:4724–4739PubMedCrossRefGoogle Scholar
  45. Cianciotto NP (2001) Pathogenicity of Legionella pneumophila. Int J Med Microbiol 291331–291343Google Scholar
  46. Commichau FM, Rothe FM, Herzberg C, Wagner E, Hellwig D, Lehnik-Habrink M, Hammer E, Völker U, Stülke J (2009) Novel activities of glycolytic enzymes in Bacillus subtilis: interactions with essential proteins involved in mRNA processing. Mol Cell Proteomics 8:1350–1360PubMedCrossRefGoogle Scholar
  47. Copley SD (2003) Enzymes with extra talents: moonlighting functions and catalytic promiscuity. Curr Opin Chem Biol 7:265–272PubMedCrossRefGoogle Scholar
  48. Cork AJ, Jergic S, Hammerschmidt S, Kobe B, Pancholi V, Benesch JL, Robinson CV, Dixon NE, Aquilina JA, Walker MJ (2009) Defining the structural basis of human plasminogen binding by streptococcal surface enolase. J Biol Chem 284:17129–17137PubMedCrossRefGoogle Scholar
  49. Corriden R, Insel PA (2010) Basal release of ATP: an autocrine-paracrine mechanism for cell regulation. Sci Signal 3:re1Google Scholar
  50. Costa CP, Kirschning CJ, Busch D, Dürr S, Jennen L, Heinzmann U, Prebeck S, Wagner H, Miethke T (2002) Role of chlamydial heat shock protein 60 in the stimulation of innate immune cells by Chlamydia pneumoniae. Eur J Immunol 32:2460–2470PubMedCrossRefGoogle Scholar
  51. Courtney HS, Pownall HJ (2010) The structure and function of serum opacity factor: a unique streptococcal virulence determinant that targets high-density lipoproteins. J Biomed Biotechnol 2010:956071PubMedCrossRefGoogle Scholar
  52. Courtney HS, Li Y, Twal WO, Argraves WS (2009) Serum opacity factor is a streptococcal receptor for the extracellular matrix protein fibulin-1. J Biol Chem 284:12966–12971PubMedCrossRefGoogle Scholar
  53. Crowe JD, Sievwright IK, Auld GC, Moore NR, Gow NA, Booth NA (2003) Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol Microbiol 47:1637–1651PubMedCrossRefGoogle Scholar
  54. Da Costa CU, Wantia N, Kirschning CJ, Busch DH, Rodriguez N, Wagner H, Miethke T (2004) Heat shock protein 60 from Chlamydia pneumoniae elicits an unusual set of inflammatory responses via toll-like receptor 2 and 4 in vivo. Eur J Immunol 34:2874–2884PubMedCrossRefGoogle Scholar
  55. Dale RC, Candler PM, Church AJ, Wait R, Pocock JM, Giovannoni G (2006) Neuronal surface glycolytic enzymes are autoantigen targets in post-streptococcal autoimmune CNS disease. J Neuroimmunol 172:187–197PubMedCrossRefGoogle Scholar
  56. Dallo SF, Kannan TR, Blaylock MW, Baseman JB (2002) Elongation factor Tu and E1 β subunit of pyruvate dehydrogenase complex act as fibronectin-binding proteins in Mycoplasma pneumonia. Mol Microbiol 46:1041–1051PubMedCrossRefGoogle Scholar
  57. Daniely D, Portnoi M, Shagan M, Porgador A, Givon-Lavi N, Ling E, Dagan R, Mizrachi Nebenzahl Y (2006) Pneumococcal 6-phosphogluconate-dehydrogenase, a putative adhesin, induces protective immune response in mice. Clin Exp Immunol 144:254–263PubMedCrossRefGoogle Scholar
  58. Danø K, Behrendt N, Høyer-Hansen G, Johnsen M, Lund LR, Ploug M, Rømer J (2005) Plasminogen activation and cancer. Thromb Haemost 93:676–681PubMedGoogle Scholar
  59. Darville T, Hiltke TJ (2010) Pathogenesis of genital tract disease due to Chlamydia trachomatis. J Infect Dis 201(2):S114–S125PubMedCrossRefGoogle Scholar
  60. de Jesus MC, Urban AA, Marasigan ME, Barnett Foster DE (2005) Acid and bile-salt stress of enteropathogenic Escherichia coli enhances adhesion to epithelial cells and alters glycolipid receptor binding specificity. J Infect Dis 192:1430–1440PubMedCrossRefGoogle Scholar
  61. Degrassi G, Devescovi G, Bigirimana J, Venturi V (2010) Xanthomonas oryzae pv. oryzae XKK.12 contains an AroQgamma chorismate mutase that is involved in rice virulence. Phytopathology 100:262–270PubMedCrossRefGoogle Scholar
  62. Derbise A, Song YP, Parikh S, Fischetti VA, Pancholi V (2004) Role of the C-terminal lysine residues of streptococcal surface enolase in Glu- and Lys-plasminogen-binding activities of group A streptococci. Infect Immun 72:94–105PubMedCrossRefGoogle Scholar
  63. Deveze-Alvarez M, García-Soto J, Martínez-Cadena G (2001) Glyceraldehyde-3-phosphate dehydrogenase is negatively regulated by ADP-ribosylation in the fungus Phycomyces blakesleeanus. Microbiology 147:2579–2584PubMedGoogle Scholar
  64. Dimmeler S, Lottspeich F, Brüne B (1992) Nitric oxide causes ADP-ribosylation and inhibition of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 267:16771–16774PubMedGoogle Scholar
  65. Dinis M, Tavares D, Veiga-Malta I, Fonseca AJ, Andrade EB, Trigo G, Ribeiro A, Videira A, Cabrita AM, Ferreira P (2009) Oral therapeutic vaccination with Streptococcus sobrinus recombinant enolase confers protection against dental caries in rats. J Infect Dis 199:116–123PubMedCrossRefGoogle Scholar
  66. Dobocan MC, Sadvakassova G, Congote LF (2009) Chaperonin 10 as an endothelial-derived differentiation factor: role of glycogen synthase kinase-3. J Cell Physiol 219:470–476PubMedCrossRefGoogle Scholar
  67. Du RJ, Ho B (2003) Surface localized heat shock protein 20 (HslV) of Helicobacter pylori. Helicobacter 8:257–267PubMedCrossRefGoogle Scholar
  68. Ebanks RO, Goguen M, McKinnon S, Pinto DM, Ross NW (2005) Identification of the major outer membrane proteins of Aeromonas salmonicida. Dis Aquat Organ 68:29–38PubMedCrossRefGoogle Scholar
  69. Eberhard T, Kronvall G, Ullberg M (1999) Surface bound plasmin promotes migration of Streptococcus pneumoniae through reconstituted basement membranes. Microb Pathog 26:175–181PubMedCrossRefGoogle Scholar
  70. Egea L, Aguilera L, Giménez R, Sorolla MA, Aguilar J, Badía J, Baldoma L (2007) Role of secreted glyceraldehyde-3-phosphate dehydrogenase in the infection mechanism of enterohemorrhagic and enteropathogenic Escherichia coli: interaction of the extracellular enzyme with human plasminogen and fibrinogen. Int J Biochem Cell Biol 39:1190–1203PubMedCrossRefGoogle Scholar
  71. Ellis RJ, Minton AP (2006) Protein aggregation in crowded environments. Biol Chem 387:485–497PubMedCrossRefGoogle Scholar
  72. Emelyanov VV, Loukianov EV (2004) A 29.5 kDa heat-modifiable major outer membrane protein of Rickettsia prowazekii, putative virulence factor, is a peptidyl-prolyl cis/trans isomerase. IUBMB Life 56:215–219PubMedCrossRefGoogle Scholar
  73. Ensgraber M, Loos M (1992) A 66-kilodalton heat shock protein of Salmonella typhimurium is responsible for binding of the bacterium to intestinal mucus. Infect Immun 60:3072–3078PubMedGoogle Scholar
  74. Erttmann KD, Kleensang A, Schneider E, Hammerschmidt S, Büttner DW, Gallin M (2005) Cloning, characterization and DNA immunization of an Onchocerca volvulus glyceraldehyde-3-phosphate dehydrogenase (Ov-GAPDH). Biochim Biophys Acta 1741:85–94PubMedCrossRefGoogle Scholar
  75. Esaguy N, Aguas AP (1997) Subcellular localization of the 65-kDa heat shock protein in mycobacteria by immunoblotting and immunogold ultracytochemistry. J Submicrosc Cytol Pathol 29:85–90PubMedGoogle Scholar
  76. Esgleas M, Li Y, Hancock MA, Harel J, Dubreuil JD, Gottschalk M (2008) Isolation and characterization of alpha-enolase, a novel fibronectin-binding protein from Streptococcus suis. Microbiology 154:2668–2679PubMedCrossRefGoogle Scholar
  77. Fairbank M, St-Pierre P, Nabi IR (2009) The complex biology of autocrine motility factor/phosphoglucose isomerase (AMF/PGI) and its receptor, the gp78/AMFR E3 ubiquitin ligase. Mol Biosyst 5:793–801PubMedCrossRefGoogle Scholar
  78. Floto RA, MacAry PA, Boname JM, Mien TS, Kampmann B, Hair JR, Huey OS, Houben EN, Pieters J, Day C, Oehlmann W, Singh M, Smith KG, Lehner PJ (2006) Dendritic cell stimulation by mycobacterial Hsp70 is mediated through CCR5. Science 314:454–458PubMedCrossRefGoogle Scholar
  79. Fraiberg M, Borovok I, Weiner RM, Lamed R (2010) Discovery and characterization of cadherin domains in Saccharophagus degradans 2–40. J Bacteriol 192:1066–1074PubMedCrossRefGoogle Scholar
  80. Freedman R (1978) Moonlighting molecules. New Sci 79:560–562Google Scholar
  81. Friedland JS, Shattock R, Remick DG, Griffin GE (1993) Mycobacterial 65-kD heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 91:58–62PubMedCrossRefGoogle Scholar
  82. Frisk A, Ison CA, Lagergård T (1998) GroEL heat shock protein of Haemophilus ducreyi: association with cell surface and capacity to bind to eukaryotic cells. Infect Immun 66:1252–1257PubMedGoogle Scholar
  83. Fu M, Li L, Albrecht T, Johnson JD, Kojic LD, Nabi IR (2011) Autocrine motility factor/phosphoglucose isomerase regulates ER stress and cell death through control of ER calcium release. Cell Death Differ [Epub ahead of print]Google Scholar
  84. Funasaka T, Hogan V, Raz A (2009) Phosphoglucose isomerase/autocrine motility factor mediates epithelial and mesenchymal phenotype conversions in breast cancer. Cancer Res 69:5349–5356PubMedCrossRefGoogle Scholar
  85. Furuya H, Ikeda R (2009) Interaction of triosephosphate isomerase from the cell surface of Staphylococcus aureus and alpha-(1-> 3)-mannooligosaccharides derived from glucuronoxylomannan of Cryptococcus neoformans. Microbiology 155:2707–2713PubMedCrossRefGoogle Scholar
  86. Garduño RA, Faulkner G, Trevors MA, Vats N, Hoffman PS (1998a) Immunolocalization of Hsp60 in Legionella pneumophila. J Bacteriol 180:505–513PubMedGoogle Scholar
  87. Garduño RA, Garduño E, Hoffman PS (1998b) Surface-associated hsp60 chaperonin of Legionella pneumophila mediates invasion in a HeLa cell model. Infect Immun 66:4602–4610PubMedGoogle Scholar
  88. Gase K, Gase A, Schirmer H, Malke H (1996) Cloning, sequencing and functional overexpression of the Streptococcus equisimilis H46A gapC gene encoding a glyceraldehyde-3-phosphate dehydrogenase that also functions as a plasmin(ogen)-binding protein. Purification and biochemical characterization of the protein. Eur J Biochem 239:42–51PubMedCrossRefGoogle Scholar
  89. Gething M-J (1997) Guidebook to Molecular Chaperones and Protein-Folding Catalysts. Oxford University Press, OxfordGoogle Scholar
  90. Gobert AP, Bambou JC, Werts C, Balloy V, Chignard M, Moran AP, Ferrero RL (2004) Helicobacter pylori heat shock protein 60 mediates interleukin-6 production by macrophages via a toll-like receptor (TLR)-2-, TLR-4-, and myeloid differentiation factor 88-independent mechanism. J Biol Chem 279:245–250PubMedCrossRefGoogle Scholar
  91. Gomez FJ, Pilcher-Roberts R, Alborzi A, Newman SL (2008) Histoplasma capsulatum cyclophilin A mediates attachment to dendritic cell VLA-5. J Immunol 181:7106–7114PubMedGoogle Scholar
  92. Goulhen F, Hafezi A, Uitto VJ, Hinode D, Nakamura R, Grenier D, Mayrand D (1998) Subcellular localization and cytotoxic activity of the GroEL-like protein isolated from Actinobacillus actinomycetemcomitans. Infect Immun 66:5307–5313PubMedGoogle Scholar
  93. Gray MW, Burger G, Lang BF (1999) Mitochondrial evolution. Science 283:1476–1481PubMedCrossRefGoogle Scholar
  94. Gregersen N, Bross P (2010) Protein misfolding and cellular stress: an overview. Methods Mol Biol 648:3–23PubMedCrossRefGoogle Scholar
  95. Guimarães AJ, Frases S, Gomez FJ, Zancopé-Oliveira RM, Nosanchuk JD (2009) Monoclonal antibodies to heat shock protein 60 alter the pathogenesis of Histoplasma capsulatum. Infect Immun 77:1357–1367PubMedCrossRefGoogle Scholar
  96. Gunka K, Newman JA, Commichau FM, Herzberg C, Rodrigues C, Hewitt L, Lewis RJ, Stülke J (2010) Functional dissection of a trigger enzyme: mutations of the Bacillus subtilis glutamate dehydrogenase RocG that affect differentially its catalytic activity and regulatory properties. J Mol Biol 400:815–827PubMedCrossRefGoogle Scholar
  97. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108PubMedCrossRefGoogle Scholar
  98. Hartmann E, Lingwood C (1997) Brief heat shock treatment induces a long-lasting alteration in the glycolipid receptor binding specificity and growth rate of Haemophilus influenzae. Infect Immun 65:1729–1733PubMedGoogle Scholar
  99. Hartmann E, Lingwood CA, Reidl J (2001) Heat-inducible surface stress protein (Hsp70) mediates sulfatide recognition of the respiratory pathogen Haemophilus influenzae. Infect Immun 69:3438–3441PubMedCrossRefGoogle Scholar
  100. Hasegawa T, Minami M, Okamoto A, Tatsuno I, Isaka M, Ohta M (2010) Characterization of a virulence-associated and cell-wall-located DNase of Streptococcus pyogenes. Microbiology 156:184–190PubMedCrossRefGoogle Scholar
  101. Hayashi T, Rao SP, Catanzaro A (1997) Binding of the 68-kilodalton protein of Mycobacterium avium to alpha(v)beta3 on human monocyte-derived macrophages enhances complement receptor type 3 expression. Infect Immun 65:1211–1216PubMedGoogle Scholar
  102. Heilmann C, Thumm G, Chhatwal GS, Hartleib J, Uekötter A, Peters G (2003) Identification and characterization of a novel autolysin (Aae) with adhesive properties from Staphylococcus epidermidis. Microbiology 149:2769–2778PubMedCrossRefGoogle Scholar
  103. Heilmann C, Hartleib J, Hussain MS, Peters G (2005) The multifunctional Staphylococcus aureus autolysin aaa mediates adherence to immobilized fibrinogen and fibronectin. Infect Immun 73:4793–4802PubMedCrossRefGoogle Scholar
  104. Helbig JH, Lück PC, Steinert M, Jacobs E, Witt M (2001) Immunolocalization of the Mip protein of intracellularly and extracellularly grown Legionella pneumophila. Lett Appl Microbiol 32:83–88PubMedCrossRefGoogle Scholar
  105. Helbig JH, König B, Knospe H, Bubert B, Yu C, Lück CP, Riboldi-Tunnicliffe A, Hilgenfeld R, Jacobs E, Hacker J, Fischer G (2003) The PPIase active site of Legionella pneumophila Mip protein is involved in the infection of eukaryotic host cells. Biol Chem 384:125–137PubMedCrossRefGoogle Scholar
  106. Hell W, Meyer HG, Gatermann SG (1998) Cloning of aas, a gene encoding a Staphylococcus saprophyticus surface protein with adhesive and autolytic properties. Mol Microbiol 29:871–881PubMedCrossRefGoogle Scholar
  107. Henderson B, Allan E, Coates ARM (2006) Stress wars: the direct role of host and bacterial molecular chaperones in bacterial Infection. Infect Immun 74:3693–3706PubMedCrossRefGoogle Scholar
  108. Henderson B, Henderson S (2009) Unfolding the relationship between secreted molecular chaperones and macrophage activation states. Cell Stress Chaperones 14:329–341PubMedCrossRefGoogle Scholar
  109. Henderson B, Pockley AG (2010) Molecular chaperones and protein-folding catalysts as intercellular signaling regulators in immunity and inflammation. J Leukoc Biol 88:445–462PubMedCrossRefGoogle Scholar
  110. Henderson B, Pockley AG (2011) Proteotoxic stress and secreted cell stress proteins in cardiovascular disease. (submitted to Circulation)Google Scholar
  111. Henderson B, Wilson M, McNab R, Lax AR (1999) Cellular microbiology. Wiley, ChichesterGoogle Scholar
  112. Henderson B, Lund PA, Coates ARM (2010) Multiple moonlighting functions of mycobacterial molecular chaperones. Tuberculosis 90:119–124PubMedCrossRefGoogle Scholar
  113. Henderson B, Nair S, Pallas J, Williams MA (2011) Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol Rev 35:147–200PubMedCrossRefGoogle Scholar
  114. Henkel JS, Baldwin MR, Barbieri JT (2010) Toxins from bacteria. EXS 100:1–29PubMedGoogle Scholar
  115. Hennequin C, Porcheray F, Waligora-Dupriet A, Collignon A, Barc M, Bourlioux P, Karjalainen T (2001) GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 147:87–96PubMedGoogle Scholar
  116. Herbert EE, Goodrich-Blair H (2007) Friend and foe: the two faces of Xenorhabdus nematophila. Nat Rev Microbiol 5:634–646PubMedCrossRefGoogle Scholar
  117. Hermans PW, Adrian PV, Albert C, Estevão S, Hoogenboezem T, Luijendijk IH, Kamphausen T, Hammerschmidt S (2006) The streptococcal lipoprotein rotamase A (SlrA) is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization. J Biol Chem 281:968–976PubMedCrossRefGoogle Scholar
  118. Hickey TB, Thorson LM, Speert DP, Daffé M, Stokes RW (2009) Mycobacterium tuberculosis Cpn60.2 and DnaK are located on the bacterial surface, where Cpn60.2 facilitates efficient bacterial association with macrophages. Infect Immun 77:3389–3401PubMedCrossRefGoogle Scholar
  119. Hickey TB, Ziltener HJ, Speert DP, Stokes RW (2010) Mycobacterium tuberculosis employs Cpn60.2 as an adhesin that binds CD43 on the macrophage surface. Cell Microbiol 12:1634–1647PubMedCrossRefGoogle Scholar
  120. Hoelzle LE, Hoelzle K, Helbling M, Aupperle H, Schoon HA, Ritzmann M, Heinritzi K, Felder KM, Wittenbrink MM (2007) MSG1, a surface-localised protein of Mycoplasma suis is involved in the adhesion to erythrocytes. Microbes Infect 9:466–474PubMedCrossRefGoogle Scholar
  121. Hoffman PS, Garduno RA (1999) Surface-associated heat shock proteins of Legionella pneumophila and Helicobacter pylori: roles in pathogenesis and immunity. Infect Dis Obstet Gynecol 7:58–63PubMedGoogle Scholar
  122. Horwich AL, Apetri AC, Fenton WA (2009) The GroEL/GroES cis cavity as a passive anti-aggregation device. FEBS Lett 583:2654–2662PubMedCrossRefGoogle Scholar
  123. Hottiger MO, Hassa PO, Lüscher B, Schüler H, Koch-Nolte F (2010) Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem Sci 35:208–219PubMedCrossRefGoogle Scholar
  124. Hoy B, Löwer M, Weydig C, Carra G, Tegtmeyer N, Geppert T, Schröder P, Sewald N, Backert S, Schneider G, Wessler S (2010) Helicobacter pylori HtrA is a new secreted virulence factor that cleaves E-cadherin to disrupt intercellular adhesion. EMBO Rep 11:798–804PubMedCrossRefGoogle Scholar
  125. Hu Y, Henderson B, Lund PA, Tormay P, Ahmed MT, Gurcha SS, Besra GS, Coates AR (2008) A mycobacterium tuberculosis mutant lacking the groEL homologue cpn60.1 is viable but fails to induce an inflammatory response in animal models of infection. Infect Immun 76:1535–1546PubMedCrossRefGoogle Scholar
  126. Huesca M, Goodwin A, Bhagwansingh A, Hoffman P, Lingwood CA (1998) Characterization of an acidic-pH-inducible stress protein (hsp70), a putative sulfatide binding adhesin, from Helicobacter pylori. Infect Immun 66:4061–4067PubMedGoogle Scholar
  127. Hughes MJ, Moore JC, Lane JD, Wilson R, Pribul PK, Younes ZN, Dobson RJ, Everest P, Reason AJ, Redfern JM, Greer FM, Paxton T, Panico M, Morris HR, Feldman RG, Santangelo JD (2002) Identification of major outer surface proteins of Streptococcus agalactiae. Infect Immun 70:1254–1259PubMedCrossRefGoogle Scholar
  128. Hurmalainen V, Edelman S, Antikainen J, Baumann M, Lähteenmäki K, Korhonen TK (2007) Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology 153:1112–1122PubMedCrossRefGoogle Scholar
  129. Ikeda R, Saito F, Matsuo M, Kurokawa K, Sekimizu K, Yamaguchi M, Kawamoto S (2007) Contribution of the mannan backbone of cryptococcal glucuronoxylomannan and a glycolytic enzyme of Staphylococcus aureus to contact-mediated killing of Cryptococcus neoformans. J Bacteriol 189:4815–4826PubMedCrossRefGoogle Scholar
  130. Jagadeesan B, Koo OK, Kim KP, Burkholder KM, Mishra KK, Aroonnual A, Bhunia AK (2010) LAP, an alcohol acetaldehyde dehydrogenase enzyme in Listeria, promotes bacterial adhesion to enterocyte-like Caco-2 cells only in pathogenic species. Microbiology 156:2782–2795PubMedCrossRefGoogle Scholar
  131. Jeffery CJ (1999) Moonlighting proteins. Trends Biochem Sci 24:8–11PubMedCrossRefGoogle Scholar
  132. Jeffery CJ (2005) Mass spectrometry and the search for moonlighting proteins. Mass Spec Revs 24:772–782CrossRefGoogle Scholar
  133. Jin H, Youngmia P, Boel G, Kochar J, Pancholi V (2005) Group A streptococcal surface GAPDF, SDH recognises uPAR/CD87 as its receptor on the human pharyngeal cell and mediates bacterial adherence to host cells. J Mol Biol 350:27–41PubMedCrossRefGoogle Scholar
  134. Jobin MC, Brassard J, Quessy S, Gottschalk M, Grenier D (2004) Acquisition of host plasmin activity by the swine pathogen Streptococcus suis serotype 2. Infect Immun 72:606–610PubMedCrossRefGoogle Scholar
  135. Johnson BJ, Le TT, Dobbin CA, Banovic T, Howard CB, Flores Fde M, Vanags D, Naylor DJ, Hill GR, Suhrbier A (2005) Heat shock protein 10 inhibits lipopolysaccharide-induced inflammatory mediator production. J Biol Chem 280:4037–4047PubMedCrossRefGoogle Scholar
  136. Joshi MC, Sharma A, Kant S, Birah A, Gupta GP, Khan SR, Bhatnagar R, Banerjee N (2008) An insecticidal GroEL protein with chitin binding activity from Xenorhabdus nematophila. J Biol Chem 283:28287–28296PubMedCrossRefGoogle Scholar
  137. Juli C, Sippel M, Jäger J, Thiele A, Weiwad M, Schweimer K, Rösch P, Steinert M, Sotriffer CA, Holzgrabe U (2010) Pipecolic acid derivatives as small-molecule inhibitors of the Legionella MIP protein. J Med Chem [Epub ahead of print] Google Scholar
  138. Jung CJ, Zheng QH, Shieh YH, Lin CS, Chia JS (2009) Streptococcus mutans autolysin AtlA is a fibronectin-binding protein and contributes to bacterial survival in the bloodstream and virulence for infective endocarditis. Mol Microbiol 74:888–902PubMedCrossRefGoogle Scholar
  139. Kalayoglu MV, Indrawati, Morrison RP, Morrison SG, Yuan Y, Byrne GI (2000) Chlamydial virulence determinants in atherogenesis: the role of chlamydial lipopolysaccharide and heat shock protein 60 in macrophage-lipoprotein interactions. J Infect Dis 181(3):S483–489Google Scholar
  140. Kaneda K, Masuzawa T, Yasugami K, Suzuki T, Suzuki Y, Yanagihara Y (1997) Glycosphingolipid-binding protein of Borrelia burgdorferi sensu lato. Infect Immun 65:3180–3185PubMedGoogle Scholar
  141. Karunakaran KP, Noguchi Y, Read TD, Cherkasov A, Kwee J, Shen C, Nelson CC, Brunham RC (2003) Molecular analysis of the multiple GroEL proteins of Chlamydiae. J Bacteriol 185:1958–1966PubMedCrossRefGoogle Scholar
  142. Katakura Y, Sano R, Hashimoto T, Ninomiya K, Shioya S (2010) Lactic acid bacteria display on the cell surface cytosolic proteins that recognize yeast mannan. Appl Microbiol Biotechnol 86:319–326PubMedCrossRefGoogle Scholar
  143. Kesimer M, Kiliç N, Mehrotra R, Thornton DJ, Sheehan JK (2009) Identification of salivary mucin MUC7 binding proteins from Streptococcus gordonii. BMC Microbiol 9:163PubMedCrossRefGoogle Scholar
  144. Khan N, Alam K, Mande SC, Valluri VL, Hasnain SE, Mukhopadhyay S (2008) Mycobacterium tuberculosis heat shock protein 60 modulates immune response to PPD by manipulating the surface expression of TLR2 on macrophages. Cell Microbiol 10:1711–1722PubMedCrossRefGoogle Scholar
  145. Kim KP, Jagadeesan B, Burkholder KM, Jaradat ZW, Wampler JL, Lathrop AA, Morgan MT, Bhunia AK (2006) Adhesion characteristics of Listeria adhesion protein (LAP)-expressing Escherichia coli to Caco-2 cells and of recombinant LAP to eukaryotic receptor Hsp60 as examined in a surface plasmon resonance sensor. FEMS Microbiol Lett 256:324–332PubMedCrossRefGoogle Scholar
  146. Kinhikar AG, Vargas D, Li H, Mahaffey SB, Hinds L, Belisle JT, Laal S (2006) Mycobacterium tuberculosis malate synthase is a laminin-binding adhesin. Mol Microbiol 60:999–1013PubMedCrossRefGoogle Scholar
  147. Kinnby B, Booth NA, Svensater G (2008) Plasminogen binding by oral streptococci from dental plaque and inflammatory lesions. Microbiology 154:924–931PubMedCrossRefGoogle Scholar
  148. Kirby AC, Meghji S, Nair SP, White P, Reddi K, Nishihara T, Nakashima K, Willis AC, Sim R, Wilson M, Henderson B (1995) The potent bone resorbing mediator of Actinobacillus actinomycetemcomitans is homologous to the molecular chaperone GroEL. J Clin Invest 96:1185–1194PubMedCrossRefGoogle Scholar
  149. Knaust A, Weber MV, Hammerschmidt S, Bergmann S, Frosch M, Kurzai O (2007) Cytosolic proteins contribute to surface plasminogen recruitment of Neisseria meningitidis. J Bacteriol 189:3246–3255PubMedCrossRefGoogle Scholar
  150. Kol A, Sukhova GK, Lichtman AH, Libby P (1998) Chlamydial heat shock protein 60 localizes in human atheroma and regulates macrophage tumor necrosis factor-alpha and matrix metalloproteinase expression. Circulation 98:300–307PubMedCrossRefGoogle Scholar
  151. Kong TH, Coates AR, Butcher PD, Hickman CJ, Shinnick TM (1993) Mycobacterium tuberculosis expresses two chaperonin-60 homologs. Proc Natl Acad Sci U S A 90:2608–2612PubMedCrossRefGoogle Scholar
  152. Krishna KA, Rao GV, Rao KR (2007) Chaperonin GroEL: structure and reaction cycle. Curr Protein Pept Sci 8:418–425PubMedCrossRefGoogle Scholar
  153. Krishnamurthy G, Vikram R, Singh SB, Patel N, Agarwal S, Mukhopadhyay G, Basu SK, Mukhopadhyay A (2005) Hemoglobin receptor in Leishmania is a hexokinase located in the flagellar pocket. J Biol Chem 280:5884–5891PubMedCrossRefGoogle Scholar
  154. Lähteenmäki K, Kuusela P, Korhonen TK (2001) Bacterial plasminogen activators and receptors. FEMS Microbiol Rev 25:531–552PubMedGoogle Scholar
  155. Lähteenmäki K, Edelman S, Korhonen TK (2005) Bacterial metastasis: the host plasminogen system in bacterial invasion. Trends Microbiol 13:79–85PubMedCrossRefGoogle Scholar
  156. Lama A, Kucknoor A, Mundodi V, Alderete JF (2009) Glyceraldehyde-3-phosphate dehydrogenase is a surface-associated, fibronectin-binding protein of Trichomonas vaginalis. Infect Immun 77:2703–2711PubMedCrossRefGoogle Scholar
  157. LeaRue RW, Dill BD, Giles DK, Whittimore JD, Raulston JE (2007) Chlamydial Hsp60–2 is iron responsive in Chlamydia trachomatis serovar E-infected human endometrial epithelial cells in vitro. Infect Immun 75:2374–2380CrossRefGoogle Scholar
  158. Launois P, N’Diaye MN, Cartel JL, Mane I, Drowart A, Van Vooren JP, Sarthou JL, Huygen K (1995) Fibronectin-binding antigen 85 and the 10-kilodalton GroES-related heat shock protein are the predominant TH-1 response inducers in leprosy contacts. Infect Immun 63:88–93PubMedGoogle Scholar
  159. Lay AJ, Jiang XM, Kisker O, Flynn E, Underwood A, Condron R, Hogg PJ (2000) Phosphoglycerate kinase acts in tumour angiogenesis as a disulphide reductase. Nature 408:869–873PubMedCrossRefGoogle Scholar
  160. Lehner T, Bergmeier LA, Wang Y, Tao L, Sing M, Spallek R, van der Zee R (2000) Heat shock proteins generate beta-chemokines which function as innate adjuvants enhancing adaptive immunity. Eur J Immunol 30:594–603PubMedCrossRefGoogle Scholar
  161. Leuzzi R, Serino L, Scarselli M, Savino S, Fontana MR, Monaci E, Taddei A, Fischer G, Rappuoli R, Pizza M (2005) Ng-MIP, a surface-exposed lipoprotein of Neisseria gonorrhoeae, has a peptidyl-prolyl cis/trans isomerase (PPIase) activity and is involved in persistence in macrophages. Mol Microbiol 58:669–681PubMedCrossRefGoogle Scholar
  162. Lewthwaite JC, Coates AR, Tormay P, Singh M, Mascagni P, Poole S, Roberts M, Sharp L, Henderson B (2001) Mycobacterium tuberculosis chaperonin 60.1 is a more potent cytokine stimulator than chaperonin 60.2 (hsp 65) and contains a CD14-binding domain. Infect Immun 69:7349–7355PubMedCrossRefGoogle Scholar
  163. Lewthwaite J, George R, Lund PA, Poole S, Tormay P, Sharp L, Coates AR, Henderson B (2002) Rhizobium leguminosarum chaperonin 60.3, but not chaperonin 60.1, induces cytokine production by human monocytes: activity is dependent on interaction with cell surface CD14. Cell Stress Chaperones 7:130–136PubMedCrossRefGoogle Scholar
  164. Li N, Xiang GS, Dokainish H, Ireton K, Elferink LA (2005) The Listeria protein internalin B mimics hepatocyte growth factor-induced receptor trafficking. Traffic 6:459–473PubMedCrossRefGoogle Scholar
  165. Lin SN, Ayada K, Zhao Y, Yokota K, Takenaka R, Okada H, Kan R, Hayashi S, Mizuno M, Hirai Y, Fujinami Y, Oguma K (2005) Helicobacter pylori heat-shock protein 60 induces production of the proinflammatory cytokine IL8 in monocytic cells. J Med Microbiol 54:225–233PubMedCrossRefGoogle Scholar
  166. Lin CY, Huang YS, Li CH, Hsieh YT, Tsai NM, He PJ, Hsu WT, Yeh YC, Chiang FH, Wu MS, Chang CC, Liao KW (2009) Characterizing the polymeric status of Helicobacter pylori heat shock protein 60. Biochem Biophys Res Commun 388:283–289PubMedCrossRefGoogle Scholar
  167. Lin CS, He PJ, Tsai NM, Li CH, Yang SC, Hsu WT, Wu MS, Wu CJ, Cheng TL, Liao KW (2010) A potential role for Helicobacter pylori heat shock protein 60 in gastric tumorigenesis. Biochem Biophys Res Commun 392:183–189PubMedCrossRefGoogle Scholar
  168. Ling E, Feldman G, Portnoi M, Dagan R, Overweg K, Mulholland F, Chalifa-Caspi V, Wells J, Mizrachi-Nebenzahl Y (2004) Glycolytic enzymes associated with the cell surface of Streptococcus pneumoniae are antigenic in humans and elicit protective immune responses in the mouse. Clin Exp Immunol 138:290–298PubMedCrossRefGoogle Scholar
  169. 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 170:487–494PubMedGoogle Scholar
  170. Lottenberg R, Broder CC, Boyle MD, Kain SJ, Schroeder BL, Curtiss R (1992) Cloning, sequence analysis, and expression in Escherichia coli of a streptococcal plasmin receptor. J Bacteriol 174:5204–5210PubMedGoogle Scholar
  171. Lund PA (2009) Multiple chaperonins in bacteria—why so many? FEMS Microbiol Revs 3:785–800CrossRefGoogle Scholar
  172. Lundemose AG, Kay JE, Pearce JH (1993) Chlamydia trachomatis Mip-like protein has peptidyl-prolyl cis/trans isomerase activity that is inhibited by FK506 and rapamycin and is implicated in initiation of chlamydial infection. Mol Microbiol 7:777–783PubMedCrossRefGoogle Scholar
  173. Macchia G, Massone A, Burroni D, Covacci A, Censini S, Rappuoli R (1993) The Hsp60 protein of Helicobacter pylori: structure and immune response in patients with gastroduodenal diseases. Mol Microbiol 9:645–652PubMedCrossRefGoogle Scholar
  174. Macellaro A, Tujulin E, Hjalmarsson K, Norlander L (1998) Identification of a 71-kilodalton surface-associated Hsp70 homologue in Coxiella burneti. Infect Immun 66:5882–5888PubMedGoogle Scholar
  175. Madureira P, Baptista M, Vieira M, Magalhães V, Camelo A, Oliveira L, Ribeiro A, Tavares D, Trieu-Cuot P, Vilanova M, Ferreira P (2007) Streptococcus agalactiae GAPDH is a virulence-associated immunomodulatory protein. J Immunol 178:1379–1387PubMedGoogle Scholar
  176. Magalhães V, Veiga-Malta I, Almeida MR, Baptista M, Ribeiro A, Trieu-Cuot P, Ferreira P (2007) Interaction with human plasminogen system turns on proteolytic activity in Streptococcus agalactiae and enhances its virulence in a mouse model. Microbes Infect 9:1276–1284PubMedCrossRefGoogle Scholar
  177. Makarow M, Braakman I (2010) Chaperones. Springer, HeidelbergGoogle Scholar
  178. Mamelak D, Mylvaganam M, Whetstone H, Hartmann E, Lennarz W, Wyrick PB, Raulston J, Han H, Hoffman P, Lingwood CA (2001) Hsp70s contain a specific sulfogalactolipid binding site. Differential aglycone influence on sulfogalactosyl ceramide binding by recombinant prokaryotic and eukaryotic hsp70 family members. Biochemistry 40:3572–3582PubMedCrossRefGoogle Scholar
  179. Martinez FO, Helming L, Gordon S (2009) Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27:451–483PubMedCrossRefGoogle Scholar
  180. Matta SK, Agarwal S, Bhatnagar R (2010) Surface localized and extracellular Glyceraldehyde-3-phosphate dehydrogenase of Bacillus anthracis is a plasminogen binding protein. Biochim Biophys Acta 1804:2111–2120PubMedCrossRefGoogle Scholar
  181. McFadden JP, Baker BS, Powles AV, Fry L (2009) Psoriasis and streptococci: the natural selection of psoriasis revisited. Br J Dermatol 160:929–937PubMedCrossRefGoogle Scholar
  182. Meghji S, White PA, Nair SP, Reddi K, Heron K, Henderson B, Zaliani A, Fossati G, Mascagni P, Hunt JF, Roberts MM, Coates AR (1997) Mycobacterium tuberculosis chaperonin 10 stimulates bone resorption: a potential contributory factor in Pott’s disease. J Exp Med 186:1241–1246PubMedCrossRefGoogle Scholar
  183. Méndez-Samperio P (2008) Expression and regulation of chemokines in mycobacterial infection. J Infect 57:374–384PubMedCrossRefGoogle Scholar
  184. Mitchell LA, Nixon B, Aitken RJ (2007) Analysis of chaperone proteins associated with human spermatozoa during capacitation. Mol Hum Reprod 13:605–613PubMedCrossRefGoogle Scholar
  185. Modun B, Williams P (1999) The staphylococcal transferrin-binding protein is a cell wall glyceraldehyde-3-phosphate dehydrogenase. Infect Immun 67:1086–1092PubMedGoogle Scholar
  186. Moore BD (2004) Bifunctional and moonlighting enzymes: lighting the way to regulatory control. Trends Plant Sci 9:221–228PubMedCrossRefGoogle Scholar
  187. Moreno-Brito V, Yáñez-Gómez C, Meza-Cervantez P, Avila-González L, Rodríguez MA, Ortega-López J, González-Robles A, Arroyo R (2005) A Trichomonas vaginalis 120 kDa protein with identity to hydrogenosome pyruvate:ferredoxin oxidoreductase is a surface adhesin induced by iron. Cell Microbiol 7:245–258PubMedCrossRefGoogle Scholar
  188. Mortellaro A, Robinson L, Ricciardi-Castagnoli P (2009) Spotlight on mycobacteria and dendritic cells: will novel targets to fight tuberculosis emerge? EMBO Mol Med 1:19–29PubMedCrossRefGoogle Scholar
  189. Mukai C, Bergkvist M, Nelson JL, Travis AJ (2009) Sequential reactions of surface- tethered glycolytic enzymes. Chem Biol 16:1013–1020PubMedCrossRefGoogle Scholar
  190. Naito M, Ohara N, Matsumoto S, Yamada T (1998) The novel fibronectin-binding motif and key residues of mycobacteria. J Biol Chem 273:2905–2909PubMedCrossRefGoogle Scholar
  191. Naito M, Fukuda T, Sekiguchi K, Yamada T, Naito M (2000) The domains of human fibronectin mediating the binding of alpha antigen, the most immunopotent antigen of mycobacteria that induces protective immunity against mycobacterial infection. Biochem J 347:725–731PubMedCrossRefGoogle Scholar
  192. Natarajaseenivasan K, Artiushin SC, Velineni S, Vedhagiri K, Vijayachari P, Timoney JF (2011) Surface-associated Hsp60 chaperonin of Leptospira interrogans serovar Autumnalis N2 strain as an immunoreactive protein. Eur J Clin Microbiol Infect Dis [Epub ahead of print]Google Scholar
  193. Noah CE, Malik M, Bublitz DC, Camenares D, Sellati TJ, Benach JL, Furie MB (2010) GroEL and lipopolysaccharide from Francisella tularensis live vaccine strain synergistically activate human macrophages. Infect Immun 78:1797–1806PubMedCrossRefGoogle Scholar
  194. Noonan FP, Halliday WJ, Morton H, Clunie GJ (1979) Early pregnancy factor is immunosuppressive. Nature 278:649–651PubMedCrossRefGoogle Scholar
  195. Nowalk AJ, Nolder C, Clifton DR, Carroll JA (2006) Comparative proteome analysis of subcellular fractions from Borrelia burgdorferi by NEPHGE and IPG. Proteomics 6:2121–2134PubMedCrossRefGoogle Scholar
  196. Ofek I, Hasty DL, Doyle RJ (2003) Bacterial adhesion. Washington, ASM PressGoogle Scholar
  197. Ohnishi H, Mizunoe Y, Takade A, Tanaka Y, Miyamoto H, Harada M, Yoshida S (2004) Legionella dumoffii DjlA, a member of the DnaJ family, is required for intracellular growth. Infect Immun 72:3592–3603PubMedCrossRefGoogle Scholar
  198. Ojha A, Anand M, Bhatt A, Kremer L, Jacobs WR Jr, Hatfull GF (2005) GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123:861–873PubMedCrossRefGoogle Scholar
  199. Oliver MA, Rojo JM, Rodríguez de Córdoba S, Alberti S (2008) Binding of complement regulatory proteins to group A Streptococcus. Vaccine 26(8):I75–I178PubMedCrossRefGoogle Scholar
  200. Pancholi V (2001) Multifunctional alpha-enolase: its role in diseases. Cell Mol Life Sci 58:902–920PubMedCrossRefGoogle Scholar
  201. Pancholi V, Fischetti VA (1992) A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med 176:415–426PubMedCrossRefGoogle Scholar
  202. Pancholi V, Fischetti VA (1993) Glyceraldehyde-3-phosphate dehydrogenase on the surface of group A streptococci is also an ADP-ribosylating enzyme. Proc Natl Acad Sci U S A 90:8154–8158PubMedCrossRefGoogle Scholar
  203. Pancholi V, Fischetti VA (1997) Regulation of the phosphorylation of human pharyngeal cell proteins by group A streptoccal surface dehydrogenase: signal transduction between streptococci and pharyngeal cells. J Exp Med 186:1633–1643PubMedCrossRefGoogle Scholar
  204. Pancholi V, Fischetti VA (1998) Alpha-enolase, a novel strong plasmin(ogen) binding protein on the surface of pathogenic streptococci. J Biol Chem 273:14503–14515PubMedCrossRefGoogle Scholar
  205. Pantzar M, Teneberg S, Lagergård T (2006) Binding of Haemophilus ducreyi to carbohydrate receptors is mediated by the 58.5-kDa GroEL heat shock protein. Microbes Infect 8:2452–2458PubMedCrossRefGoogle Scholar
  206. Pathak SK, Basu S, Bhattacharyya A, Pathak S, Banerjee A, Basu J, Kundu M (2006) TLR4-dependent NF-kappaB activation and mitogen- and stress-activated protein kinase 1-triggered phosphorylation events are central to Helicobacter pylori peptidyl prolyl cis-, trans-isomerase (HP0175)-mediated induction of IL-6 release from macrophages. J Immunol 177:7950–7958PubMedGoogle Scholar
  207. Peake P, Gooley A, Britton WJ (1993) Mechanism of interaction of the 85B secreted protein of Mycobacterium bovis with fibronectin. Infect Immun 61:4828–4832PubMedGoogle Scholar
  208. Peetermans WE, Raats CJ, Langermans JA, van Furth R (1994) Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand J Immunol 39:613–617PubMedCrossRefGoogle Scholar
  209. Perucho M, Salas J, Salas ML (1980) Study of the interaction of glyceraldehyde-3-phosphate dehydrogenase with DNA. Biochim Biophys Acta 606:181–195PubMedCrossRefGoogle Scholar
  210. Piatigorsky J (1998) Multifunctional lens crystallins and corneal enzymes. More than meets the eye. Ann N Y Acad Sci 842:7–15PubMedCrossRefGoogle Scholar
  211. Piatigorsky J (2007) Gene Sharing and Evolution. Harvard University Press, CambridgeGoogle Scholar
  212. Piatigorsky J, O’Brien WE, Norman BL, Kalumuck K, Wistow GJ, Borras T, Nickerson JM, Wawrousek EF (1988) Gene sharing by delta-crystallin and argininosuccinate lyase. Proc Natl Acad Sci U S A 85:3479–8343PubMedCrossRefGoogle Scholar
  213. Pidot SJ, Porter JL, Tobias NJ, Anderson J, Catmull D, Seemann T, Kidd S, Davies JK, Reynolds E, Dashper S, Stinear TP (2010) Regulation of the 18 kDa heat shock protein in Mycobacterium ulcerans: an alpha-crystallin orthologue that promotes biofilm formation. Mol Microbiol 78:1216–1231PubMedCrossRefGoogle Scholar
  214. Podobnik M, Tyagi R, Matange N, Dermol U, Gupta AK, Mattoo R, Seshadri K, Visweswariah SS (2009) A mycobacterial cyclic AMP phosphodiesterase that moonlights as a modifier of cell wall permeability. J Biol Chem 284:32846–32857PubMedCrossRefGoogle Scholar
  215. Poltermann S, Kunert A, von der Heide M, Eck R, Hartmann A, Zipfel PF (2007) Gpm1p is a factor H-, FHL-1-, and plasminogen-binding surface protein of Candida albicans. J Biol Chem 282:37537–37544PubMedCrossRefGoogle Scholar
  216. Puech V, Guilhot C, Perez E, Tropis M, Armitige LY, Gicquel B, Daffé M (2002) Evidence for a partial redundancy of the fibronectin-binding proteins for the transfer of mycoloyl residues onto the cell wall arabinogalactan termini of Mycobacterium tuberculosis. Mol Microbiol 44:1109–1122PubMedCrossRefGoogle Scholar
  217. Qamra R, Mande SC (2004) Crystal structure of the 65-kilodalton heat shock protein, chaperonin 60.2, of Mycobacterium tuberculosis. J Bacteriol 186:8105–8113PubMedCrossRefGoogle Scholar
  218. Qamra R, Srinivas V, Mande SC (2004) Mycobacterium tuberculosis GroEL homologues unusually exist as lower oligomers and retain the ability to suppress aggregation of substrate proteins. J Mol Biol 342:605–617PubMedCrossRefGoogle Scholar
  219. Quan S, Koldewey P, Tapley T, Kirsch N, Ruane KM, Pfizenmaier J, Shi R, Hofmann S, Foit L, Ren G, Jakob U, Xu Z, Cygler M, Bardwell JC (2011) Genetic selection designed to stabilize proteins uncovers a chaperone called Spy. Nat Struct Mol Biol [Epub ahead of print]Google Scholar
  220. Ragno S, Winrow VR, Mascagni P, Lucietto P, Di Pierro F, Morris CJ, Blake DR (1996) A synthetic 10-kD heat shock protein (hsp10) from Mycobacterium tuberculosis modulates adjuvant arthritis. Clin Exp Immunol 103:384–390PubMedCrossRefGoogle Scholar
  221. Raje CI, Kumar S, Harle A, Nanda JS, Raje M (2007) The macrophage cell surface glyceraldehyde-3-phosphate dehydrogenase is a novel transferrin receptor. J Biol Chem 282:3252–3261PubMedCrossRefGoogle Scholar
  222. Ramajo-Hernández A, Pérez-Sánchez R, Ramajo-Martín V, Oleaga A (2007) Schistosoma bovis: plasminogen binding in adults and the identification of plasminogen-binding proteins from the worm tegument. Exp Parasitol 115:83–91PubMedCrossRefGoogle Scholar
  223. Randhawa AK, Ziltener HJ, Stokes RW (2008) CD43 controls the intracellular growth of Mycobacterium tuberculosis through the induction of TNF-alpha-mediated apoptosis. Cell Microbiol 10:2105–2117PubMedCrossRefGoogle Scholar
  224. Rao T, Lund PA (2010) Differential expression of the multiple chaperonins of Mycobacterium smegmatis. FEMS Microbiol Lett 310:24–31PubMedCrossRefGoogle Scholar
  225. Ratnakar P, Rao SP, Catanzaro A (1996) Isolation and characterization of a 70 kDa protein from Mycobacterium avium. Microb Pathog 21:471–486PubMedCrossRefGoogle Scholar
  226. Reddi K, Meghji S, Nair SP, Arnett TR, Miller AD, Preuss M, Wilson M, Henderson B, Hill P (1998) The Escherichia coli chaperonin 60 (groEL) is a potent stimulator of osteoclast formation. J Bone Miner Res 13:1260–1266PubMedCrossRefGoogle Scholar
  227. Reddy VM, Suleman FG (2004) Mycobacterium avium-superoxide dismutase binds to epithelial cell aldolase, glyceraldehyde-3-phosphate dehydrogenase and cyclophilin A. Microb Pathog 36:67–74PubMedCrossRefGoogle Scholar
  228. Redlitz A, Fowler BJ, Plow EF, Miles LA (1995) The role of an enolase-related molecule in plasminogen binding to cells. Eur J Biochem 227:407–415PubMedCrossRefGoogle Scholar
  229. Rha YH, Taube C, Haczku A, Joetham A, Takeda K, Duez C, Siegel M, Aydintug MK, Born WK, Dakhama A, Gelfand EW (2002) Effect of microbial heat shock proteins on airway inflammation and hyperresponsiveness. J Immunol 169:5300–5307PubMedGoogle Scholar
  230. Richter K, Haslbeck M, Buchner J (2010) The heat shock response: life on the verge of death. Mol Cell 40:253–266PubMedCrossRefGoogle Scholar
  231. Riffo-Vasquez Y, Spina D, Page C, Desel C, Whelan M, Tormay P, Singh M, Henderson B, Coates ARM (2004) Differential effects of Mycobacterium tuberculosis chaperonins on bronchial eosinophilia and hyperresponsiveness in a murine model of allergic inflammation. Clin Exp Allergy 34:712–719PubMedCrossRefGoogle Scholar
  232. Ronning DR, Klabunde T, Besra GS, Vissa VD, Belisle JT, Sacchettini JC (2000) Crystal structure of the secreted form of antigen 85C reveals potential targets for mycobacterial drugs and vaccines. Nature Struct Biol 7:141–146PubMedCrossRefGoogle Scholar
  233. Rosano C (2011) Molecular model of hexokinase binding to the outer mitochondrial membrane porin (VDAC1): implication for the design of new cancer therapies. Mitochondrion [Epub ahead of print]Google Scholar
  234. Saad N, Urdaci M, Vignoles C, Chaignepain S, Tallon R, Schmitter JM, Bressollier P (2009) Lactobacillus plantarum 299v surface-bound GAPDH: a new insight into enzyme cell walls location. J Microbiol Biotechnol 19:1635–1643PubMedCrossRefGoogle Scholar
  235. Saito F, Ikeda R (2005) Killing of cryptococcus neoformans by Staphylococcus aureus: the role of cryptococcal capsular polysaccharide in the fungal–bacteria interaction. Med Mycol 43:603–612PubMedCrossRefGoogle Scholar
  236. Santiago NI, Zipf A, Bhunia AK (2006) Influence of temperature and growth phase on expression of a 104-kilodalton Listeria adhesion protein in Listeria monocytogenes. Appl Environ Microbiol 65:2765–2769Google Scholar
  237. Sasu S, LaVerda D, Qureshi N, Golenbock DT, Beasley D (2001) Chlamydia pneumoniae and chlamydial heat shock protein 60 stimulate proliferation of human vascular smooth muscle cells via toll-like receptor 4 and p44/p42 mitogen-activated protein kinase activation. Circ Res 89:244–250PubMedCrossRefGoogle Scholar
  238. Schauer K, Muller C, Carrière M, Labigne A, Cavazza C, De Reuse H (2010) The Helicobacter pylori GroES cochaperonin HspA functions as a specialized nickel chaperone and sequestration protein through its unique C-terminal extension. J Bacteriol 192:1231–1237PubMedCrossRefGoogle Scholar
  239. Schulz LC, Bahr JM (2003) Glucose-6-phosphate isomerase is necessary for embryo implantation in the domestic ferret. Proc Natl Acad Sci U S A 100:8561–8566PubMedCrossRefGoogle Scholar
  240. Segovia-Gamboa NC, Chávez-Munguía B, Medina-Flores Y, Cázares-Raga FE, Hernández-Ramírez VI, Martínez-Palomo A, Talamás-Rohana P (2010) Entamoeba invadens, encystation process and enolase. Exp Parasitol 125:63–69PubMedCrossRefGoogle Scholar
  241. Seifert KN, McArthur WP, Bleiweis AS, Brady LJ (2003) Characterization of group B streptococcal glyceraldehyde-3-phosphate dehydrogenase: surface localization, enzymatic activity, and protein–protein interactions. Can J Microbiol 49:350–356PubMedCrossRefGoogle Scholar
  242. Sengupta S, Ghosh S, Nagaraja V (2008) Moonlighting function of glutamate racemase from Mycobacterium tuberculosis: racemization and DNA gyrase inhibition are two independent activities of the enzyme. Microbiology 154:2796–2803PubMedCrossRefGoogle Scholar
  243. Sha J, Erova TE, Alyea RA, Wang S, Olano JP, Pancholi V, Chopra AK (2009) Surface-expressed enolase contributes to the pathogenesis of clinical isolate SSU of Aeromonas hydrophila. J Bacteriol 191:3095–3107PubMedCrossRefGoogle Scholar
  244. Sirover MA (2005) New nuclear functions of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in mammalian cells. J Cell Biochem 95:45–52PubMedCrossRefGoogle Scholar
  245. Smith HW, Marshall CJ (2010) Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol 11:23–36PubMedCrossRefGoogle Scholar
  246. Smitherman LS, Minnick MF (2005) Bartonella bacilliformis GroEL: effect on growth of human vascular endothelial cells in infected cocultures. Ann N Y Acad Sci 1063:286–298PubMedCrossRefGoogle Scholar
  247. Spurbeck RR, Arvidson CG (2010) Lactobacillus jensenii surface associated proteins inhibit Neisseria gonorrhoeae adherence to epithelial cells. Infect Immun 78:3103–3111PubMedCrossRefGoogle Scholar
  248. Sriram G, Martinez JA, McCabe ER, Liao JC, Dipple KM (2005) Single-gene disorders: what role could moonlighting enzymes play? Am J Hum Genet 76:911–924PubMedCrossRefGoogle Scholar
  249. Sriram G, Parr LS, Rahib L, Liao JC, Dipple KM (2010) Moonlighting function of glycerol kinase causes systems-level changes in rat hepatoma cells. Metab Eng 12:332–340PubMedCrossRefGoogle Scholar
  250. Starnes GL, Coincon M, Sygusch J, Sibley LD (2009) Aldolase is essential for energy production and bridging adhesin-actin cytoskeletal interactions during parasite invasion of host cells. Cell Host Microbe 5:353–364PubMedCrossRefGoogle Scholar
  251. Stein M, Keshav S, Harris N, Gordon S (1992) Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J Exp Med 176:287–292PubMedCrossRefGoogle Scholar
  252. Stillman B, Stewart D (2004) The genome of Homo Sapiens. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  253. Sun YJ, Chou CC, Chen WS, Wu RT, Meng M, Hsiao CD (1999) The crystal structure of a multifunctional protein: phosphoglucose isomerase/autocrine motility factor/neuroleukin. Proc Natl Acad Sci U S A 96:5412–5417PubMedCrossRefGoogle Scholar
  254. Takayanagi H (2009) Osteoimmunology and the effects of the immune system on bone. Nat Rev Rheumatol 5:667–676PubMedCrossRefGoogle Scholar
  255. Takenaka R, Yokota K, Ayada K, Mizuno M, Zhao Y, Fujinami Y, Lin SN, Toyokawa T, Okada H, Shiratori Y, Oguma Y (2004) Helicobacter pylori heat-shock protein 60 induces inflammatory responses through the toll-like receptor-triggered pathway in cultured human gastric epithelial cells. Microbiology 150:3913–3922PubMedCrossRefGoogle Scholar
  256. Tan C, Liu M, Liu J, Yuan F, Fu S, Liu Y, Jin M, Bei W, Chen H (2009) Vaccination with Streptococcus suis serotype 2 recombinant 6PGD protein provides protection against S. suis infection in swine. FEMS Microbiol Lett 296:78–83PubMedCrossRefGoogle Scholar
  257. Tanaka T, Abe Y, Inoue N, Kim WS, Kumura H, Nagasawa H, Igarashi I, Shimazaki K (2004) The detection of bovine lactoferrin binding protein on Trypanosoma brucei. J Vet Med Sci 66:619–625PubMedCrossRefGoogle Scholar
  258. Taylor JM, Heinrichs DE (2002) Transferrin binding in Staphylococcus aureus: involvement of a cell wall-anchored protein. Mol Microbiol 43:1603–1614PubMedCrossRefGoogle Scholar
  259. Tegtmeyer N, Hartig R, Delahay RM, Rohde M, Brandt S, Conradi J, Takahashi S, Smolka AJ, Sewald N, Backert S (2010) A small fibronectin-mimicking protein from bacteria induces cell spreading and focal adhesion formation. J Biol Chem 285:23515–23526PubMedCrossRefGoogle Scholar
  260. Terao Y, Yamaguchi M, Hamada S, Kawabata S (2006) Multifunctional glyceraldehyde-3-phosphate dehydrogenase of Streptococcus pyogenes is essential for evasion from neutrophils. J Biol Chem 281:14215–14223PubMedCrossRefGoogle Scholar
  261. Tormay P, Coates AR, Henderson B (2005) The intercellular signaling activity of the Mycobacterium tuberculosis chaperonin 60.1 protein resides in the equatorial domain. J Biol Chem 280:14272–14277PubMedCrossRefGoogle Scholar
  262. Tsugawa H, Ito H, Ohshima M, Okawa Y (2007) Cell adherence-promoted activity of Plesiomonas shigelloides groEL. J Med Microbiol 56:23–29PubMedCrossRefGoogle Scholar
  263. Tunio SA, Oldfield NJ, Berry A, Ala’Aldeen DA, Wooldridge KG, Turner DP (2010a) The moonlighting protein fructose-1, 6-bisphosphate aldolase of Neisseria meningitidis: surface localization and role in host cell adhesion. Mol Microbiol 76:605–615PubMedCrossRefGoogle Scholar
  264. Tunio SA, Oldfield NJ, Ala’Aldeen DA, Wooldridge KG, Turner DP (2010b) The role of glyceraldehyde 3-phosphate dehydrogenase (GapA-1) in Neisseria meningitidis adherence to human cells. BMC Microbiol 10:280PubMedCrossRefGoogle Scholar
  265. Van Eden W, van der Zee R, Prakken B (2005) Heat-shock proteins induce T-cell regulation of chronic inflammation. Nature Revs Immunol 5:318–330CrossRefGoogle Scholar
  266. Vanags D, Williams B, Johnson B, Hall S, Nash P, Taylor A, Weiss J, Feeney D (2006) Therapeutic efficacy and safety of chaperonin 10 in patients with rheumatoid arthritis: a double-blind randomised trial. Lancet 368:855–863PubMedCrossRefGoogle Scholar
  267. Vander Heiden MG, Locasale JW, Swanson KD, Sharfi H, Heffron GJ, Amador-Noguez D, Christofk HR, Wagner G, Rabinowitz JD, Asara JM, Cantley LC (2010) Evidence for an alternative glycolytic pathway in rapidly proliferating cells. Science 329:1492–1499PubMedCrossRefGoogle Scholar
  268. Vantourout P, Radojkovic C, Lichtenstein L, Pons V, Champagne E, Martinez LO (2010) Ecto-F1-ATPase: a moonlighting protein complex and an unexpected apoA-I receptor. World J Gastroenterol 16:5925–5935PubMedGoogle Scholar
  269. Veiga-Malta I, Duarte M, Dinis M, Tavares D, Videira A, Ferreira P (2004) Enolase from Streptococcus sobrinus is an immunosuppressive protein. Cell Microbiol 6:79–88PubMedCrossRefGoogle Scholar
  270. Vesosky B, Rottinghaus EK, Stromberg P, Turner J, Beamer G (2010) CCL5 participates in early protection against Mycobacterium tuberculosis. J Leukoc Biol 87:1153–1165PubMedCrossRefGoogle Scholar
  271. Wagner C, Khan AS, Kamphausen T, Schmausser B, Unal C, Lorenz U, Fischer G, Hacker J, Steinert M (2007) Collagen binding protein Mip enables Legionella pneumophila to transmigrate through a barrier of NCI-H292 lung epithelial cells and extracellular matrix. Cell Microbiol 9:450–462PubMedCrossRefGoogle Scholar
  272. Walsh A, Whelan D, Bielanowicz A, Skinner B, Aitken RJ, O’Bryan MK, Nixon B (2008) Identification of the molecular chaperone, heat shock protein 1 (chaperonin 10), in the reproductive tract and in capacitating spermatozoa in the male mouse. Biol Reprod 78:983–993PubMedCrossRefGoogle Scholar
  273. Wampler JL, Kim KP, Jaradat Z, Bhunia AK (2004) Heat shock protein 60 acts as a receptor for the Listeria adhesion protein in Caco-2 cells. Infect Immun 72:931–936PubMedCrossRefGoogle Scholar
  274. Wang L, Lin M (2008) A novel cell wall-anchored peptidoglycan hydrolase (autolysin), IspC, essential for Listeria monocytogenes virulence: genetic and proteomic analysis. Microbiology 154:1900–1913PubMedCrossRefGoogle Scholar
  275. Wang Y, Kelly CG, Karttunen JT, Whittall T, Lehner PJ, Duncan L, MacAry P, Younson JS, Singh M, Oehlmann W, Cheng G, Bergmeier L, Lehner T (2001) CD40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 15:971–983PubMedCrossRefGoogle Scholar
  276. Wang Y, Kelly CG, Singh M, McGowan EG, Carrara AS, Bergmeier LA, Lehner T (2002) Stimulation of Th1-polarizing cytokines, C–C chemokines, maturation of dendritic cells, and adjuvant function by the peptide binding fragment of heat shock protein 70. J Immunol 169:2422–2429PubMedGoogle Scholar
  277. Wang Y, Whittall T, McGowan E, Younson J, Kelly C, Bergmeier LA, Singh M, Lehner T (2005) Identification of stimulating and inhibitory epitopes within the heat shock protein 70 molecule that modulate cytokine production and maturation of dendritic cells. J Immunol 174:3306–3316PubMedGoogle Scholar
  278. Watanabe H, Takehana K, Date M, Shinozaki T, Raz A (1996) Tumor cell autocrine motility factor is the neuroleukin/phosphohexose isomerase polypeptide. Cancer Res 56:2960–2963PubMedGoogle Scholar
  279. Watarai M, Kim S, Erdenebaatar J, Makino S, Horiuchi M, Shirahata T, Sakaguchi S, Katamine S (2003) Cellular prion protein promotes Brucella infection into macrophages. J Exp Med 198:5–17PubMedCrossRefGoogle Scholar
  280. Watson C, Alp NJ (2008) Role of Chlamydia pneumoniae in atherosclerosis. Clin Sci (Lond) 114:509–531CrossRefGoogle Scholar
  281. Weaver DT (1998) Telomeres: moonlighting by DNA repair proteins. Curr Biol 8:R492–R494PubMedCrossRefGoogle Scholar
  282. Wegrzyn J, Potla R, Chwae YJ, Sepuri NB, Zhang Q, Koeck T, Derecka M, Szczepanek K, Szelag M, Gornicka A, Moh A, Moghaddas S, Chen Q, Bobbili S, Cichy J, Dulak J, Baker DP, Wolfman A, Stuehr D, Hassan MO, Fu XY, Avadhani N, Drake JI, Fawcett P, Lesnefsky EJ, Larner AC (2009) Function of mitochondrial Stat3 in cellular respiration. Science 323:793–797PubMedCrossRefGoogle Scholar
  283. Whittall T, Wang Y, Younson J, Kelly C, Bergmeier L, Peters B, Singh M, Lehner T (2006) Interaction between the CCR5 chemokine receptors and microbial HSP70. Eur J Immunol 36:2304–2314PubMedCrossRefGoogle Scholar
  284. Wicker HG, Harboe M (1992) The antigen 85 complex: a major secretion product of Mycobacterium tuberculosis. Microbiol Rev 56:648–661Google Scholar
  285. Wilkins JC, Beighton D, Homer KA (2003) Effect of acidic pH on expression of surface-associated proteins of Streptococcus oralis. Appl Environ Microbiol 69:5290–5296PubMedCrossRefGoogle Scholar
  286. Williams B, Vanags D, Hall S, McCormack C, Foley P, Weiss J, Johnson B, Latz E, Feeney D (2008) Efficacy and safety of chaperonin 10 in patients with moderate to severe plaque psoriasis: evidence of utility beyond a single indication. Arch Dermatol 144:683–685PubMedCrossRefGoogle Scholar
  287. Winram SB, Lottenberg R (1998) Site-directed mutagenesis of streptococcal plasmin receptor protein (Plr) identifies the C-terminal Lys334 as essential for plasmin binding, but mutation of the plr gene does not reduce plasmin binding to group A streptococci. Microbiology 144:2025–2035PubMedCrossRefGoogle Scholar
  288. Winrow VR, Mesher J, Meghji S, Morris CJ, Fox S, Coates AR, Tormay P, Blake D, Henderson B (2008) The two homologous chaperonin 60 proteins of Mycobacterium tuberculosis have distinct effects on monocyte differentiation into osteoclasts. Cell Microbiol 10:2091–2104PubMedCrossRefGoogle Scholar
  289. Wu Z, Zhang W, Lu C (2008) Comparative proteome analysis of secreted proteins of Streptococcus suis serotype 9 isolates from diseased and healthy pigs. Microb Pathog 45:159–166PubMedCrossRefGoogle Scholar
  290. Wuppermann FN, Mölleken K, Julien M, Jantos CA, Hegemann JH (2008) Chlamydia pneumoniae GroEL1 protein is cell surface associated and required for infection of HEp-2 cells. J Bacteriol 190:3757–3767PubMedCrossRefGoogle Scholar
  291. Xu W, Seiter K, Feldman E, Ahmed T, Chiao JW (1996) The differentiation and maturation mediator for human myeloid leukemia cells shares homology with neuroleukin or phosphoglucose isomerase. Blood 87:4502–4506PubMedGoogle Scholar
  292. Yamaguchi H, Osaki T, Taguchi H, Hanawa T, Yamamoto T, Kamiya S (1996) Flow cytometric analysis of the heat shock protein 60 expressed on the cell surface of Helicobacter pylori. J Med Microbiol 45:270–277PubMedCrossRefGoogle Scholar
  293. Yamaguchi H, Osaki T, Taguchi H, Hanawa T, Yamamoto T, Fukuda M, Kawakami H, Hirano H, Kamiya S (1997a) Growth inhibition of Helicobacter pylori by monoclonal antibody to heat-shock protein 60. Microbiol Immunol 41:909–916PubMedGoogle Scholar
  294. Yamaguchi H, Osaki T, Kurihara N, Taguchi H, Hanawa T, Yamamoto T, Kamiya S (1997b) Heat-shock protein 60 homologue of Helicobacter pylori is associated with adhesion of H. pylori to human gastric epithelial cells. J Med Microbiol 46:825–831PubMedCrossRefGoogle Scholar
  295. Yamaguchi H, Osaki T, Kurihara N, Kitajima M, Kai M, Takahashi M, Taguchi H, Kamiya S (1999) Induction of secretion of interleukin-8 from human gastric epithelial cells by heat-shock protein 60 homologue of Helicobacter pylori. J Med Microbiol 48:927–933PubMedCrossRefGoogle Scholar
  296. Yamaguchi M, Ikeda R, Nishimura M, Kawamoto S (2010) Localization by scanning immunoelectron microscopy of triosephosphate isomerase, the molecules responsible for contact-mediated killing of Cryptococcus, on the surface of Staphylococcus. Microbiol Immunol 54:368–370PubMedCrossRefGoogle Scholar
  297. Yoshida N, Oeda K, Watanabe E, Mikami T, Fukita Y, Nishimura K, Komai K, Matsuda K (2001) Protein function. Chaperonin turned insect toxin. Nature 411:44PubMedCrossRefGoogle Scholar
  298. Yunoki N, Yokota K, Mizuno M, Kawahara Y, Adachi M, Okada H, Hayashi S, Hirai Y, Oguma K, Tsuji T (2000) Antibody to heat shock protein can be used for early serological monitoring of Helicobacter pylori eradication treatment. Clin Diagn Lab Immunol 7:574–577PubMedGoogle Scholar
  299. Zaborina O, Li X, Cheng G, Kapatral V, Chakrabarty AM (1999) Secretion of ATP-utilizing enzymes, nucleoside diphosphate kinase and ATPase, by Mycobacterium bovis BCG: sequestration of ATP from macrophage P2Z receptors? Mol Microbiol 31:1333–1343PubMedCrossRefGoogle Scholar
  300. Zhang B, Walsh MD, Nguyen KB, Hillyard NC, Cavanagh AC, McCombe PA, Morton H (2003) Early pregnancy factor treatment suppresses the inflammatory response and adhesion molecule expression in the spinal cord of SJL/J mice with experimental autoimmune encephalomyelitis and the delayed-type hypersensitivity reaction to trinitrochlorobenzene in normal BALB/c mice. J Neurol Sci 212:37–46PubMedCrossRefGoogle Scholar
  301. Zhang L, Pelech S, Uitto VJ (2004a) Long-term effect of heat shock protein 60 from Actinobacillus actinomycetemcomitans on epithelial cell viability and mitogen-activated protein kinases. Infect Immun 72:38–45PubMedCrossRefGoogle Scholar
  302. Zhang L, Koivisto L, Heino J, Uitto VJ (2004b) Bacterial heat shock protein 60 may increase epithelial cell migration through activation of MAP kinases and inhibition of alpha6beta4 integrin expression. Biochem Biophys Res Commun 319:1088–1095PubMedCrossRefGoogle Scholar
  303. Zhao Y, Yokota K, Ayada K, Yamamoto Y, Okada T, Shen L, Oguma K (2007) Helicobacter pylori heat-shock protein 60 induces interleukin-8 via a toll-like receptor (TLR)2 and mitogen-activated protein (MAP) kinase pathway in human monocytes. J Med Microbiol 56:154–164PubMedCrossRefGoogle Scholar

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© Springer-Verlag Berlin Heidelberg 2011

Authors and Affiliations

  1. 1.Department of Microbial DiseasesUCL-Eastman Dental Institute, University College LondonLondonUK
  2. 2.Division of BiosciencesInstitute of Structural and Molecular Biology, University College LondonLondonUK

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