Multiple moonlighting functions of mycobacterial molecular chaperones

Tuberculosis

Volumn 90, Issue 2, 2010, Pages 119-124

  Henderson, Brian ^a   Lund, Peter A ^b   Coates, Anthony R M ^c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^c ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Intercellular signalling; Molecular chaperones; Protein moonlighting

Indexed keywords

ALPHA CRYSTALLIN; CHAPERONE; CHAPERONE 10; CHAPERONE 60.1; CHAPERONE 60.2; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; HEAT SHOCK PROTEIN 70; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 12P40; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; PROTEIN DNAK; RANTES; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; VASCULAR CELL ADHESION MOLECULE 1;

BACTERIAL CELL WALL; MACROPHAGE; MYCOBACTERIUM; MYCOBACTERIUM BOVIS; MYCOBACTERIUM LEPRAE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN SECRETION; REVIEW; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; CELL COMMUNICATION; HUMANS; MOLECULAR CHAPERONES; MYCOBACTERIUM TUBERCULOSIS; SIGNAL TRANSDUCTION; TUBERCULOSIS;

EID: 77950593732     PISSN: 14729792     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tube.2010.01.004     Document Type: Review

References (67)

1. Hickey T.B., Thorson L.M., Speert D.P., Daffé M., and Stokes R.W. Mycobacterium tuberculosis Cpn60.2 and DnaK are located on the bacterial surface, where Cpn60.2 facilitates efficient bacterial association with macrophages. Infect Immun 77 (2009) 3389-3401
2. Hu Y., Henderson B., Lund P.A., Tormay P., Ahmed M.T., Gurcha S.S., et al. 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 (2008) 1535-1546
3. Shinnick T.M., Vodkin M.H., and Williams J.C. The Mycobacterium tuberculosis 65-kilodalton antigen is a heat shock protein which corresponds to common antigen and to the Escherichia coli GroEL protein. Infect Immun 56 (1988) 446-451
4. Lund P.A. Multiple chaperonins in bacteria - why so many?. FEMS Microbiol Rev 33 (2009) 785-800
5. van Eden W., Thole J.E., van der Zee R., Noordzij A., van Embden J.D., Hensen E.J., et al. Cloning of the mycobacterial epitope recognized by T lymphocytes in adjuvant arthritis. Nature 331 (1988) 171-173
6. van Eden W., Wick G., Albani S., and Cohen I. Stress, heat shock proteins, and autoimmunity: how immune responses to heat shock proteins are to be used for the control of chronic inflammatory diseases. Ann N Y Acad Sci 1113 (2007) 217-237
7. Friedland J.S., Shattock R., Remick D.G., and Griffin G.E. Mycobacterial 65-kDa heat shock protein induces release of proinflammatory cytokines from human monocytic cells. Clin Exp Immunol 91 (1993) 58-62
8. Peetermans W.E., Raats C.J., Langermans J.A., and van Furth R. Mycobacterial heat-shock protein 65 induces proinflammatory cytokines but does not activate human mononuclear phagocytes. Scand. J Immunol 1993 39 (1994) 613-617
9. Martinez F.O., Helming L., and Gordon S. Alternative activation of macrophages: an immunologic functional perspective. Annu Rev Immunol 27 (2009) 451-483
10. Verdegaal M.E., Zegveld S.T., and van Furth R. Heat shock protein 65 induces CD62e, CD106, and CD54 on cultured human endothelial cells and increases their adhesiveness for monocytes and granulocytes. J Immunol 151 (1996) 369-376
11. Kirby A., Meghji S., Nair S.P., White P., Reddi K., Nishihara T., et al. The potent bone resorbing mediator of Actinobacillus actinomycetemcomitans is homologous to the molecular chaperone GroEL. J Clin Invest 96 (1995) 1185-1194
12. Reddi K., Meghji S., Nair S.P., Arnett T.R., Miller A.D., Preuss M., et al. The Escherichia coli chaperonin 60 (groEL) is a potent stimulator of osteoclast formation. J Bone Miner Res 13 (1998) 1260-1266
13. Meghji S., White P.A., Nair S.P., Reddi K., Heron K., Henderson B., et al. Mycobacterium tuberculosis chaperonin 10 stimulates bone resorption: a potential contributory factor in Pott's disease. J Exp Med 186 (1997) 1241-1246
14. Meghji S., Lillicrap M., Maguire M., Tabona P., Gaston J.S., Poole S., et al. Human chaperonin 60 (Hsp60) stimulates bone resorption: structure/function relationships. Bone 33 (2003) 419-425
15. Lewthwaite J.C., Coates A.R., Tormay P., Singh M., Mascagni P., Poole S., et al. 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 (2001) 7349-7355
16. Henderson B., and Mesher J. The search for the chaperonin 60 receptor. Methods 43 (2007) 223-228
17. Tormay P., Coates A.R., and Henderson B. Structure:function relationships of Mycobacterium tuberculosis chaperonin 60 proteins: the cell signalling activity of M. tuberculosis chaperonin 60.1 resides in the equatorial domain. J Biol Chem 280 (2005) 14272-14277
18. Rha Y.H., Taube C., Haczku A., Joetham A., Takeda K., Duez C., et al. Effect of microbial heat shock proteins on airway inflammation and hyperresponsiveness. J Immunol 169 (2002) 5300-5307
19. Riffo-Vasquez Y., Spina D., Page C., Desel C., Whelan M., Tormay P., et al. Differential effects of Mycobacterium tuberculosis chaperonins on bronchial eosinophilia and hyperresponsiveness in a murine model of allergic inflammation. Clin Exp Allergy 34 (2004) 712-719
20. Novartis Foundation Symposium 291. The biology of extracellular molecular chaperones. Wiley: Chichester, 2008.
21. Winrow V.R., Mesher J., Meghji S., Morris C.J., Fox S., Coates A.R.M., et al. The two homologous chaperonin 60 proteins of Mycobacterium tuberculosis have distinct effects on monocyte differentiation into osteoclasts. Cell Microbiol 10 (2008) 2091-2104
22. Kong Y.Y., Feige U., Sarosi I., Bolon B., Tafuri A., Morony S., et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 402 (1999) 304-309
23. Khan N., Alam K., Mande S.C., Valluri V.L., Hasnain S.E., and Mukhopadhyay S. Mycobacterium tuberculosis heat shock protein 60 modulates immune response to PPD by manipulating the surface expression of TLR2 on macrophages. Cell Microbiol 10 (2008) 1711-1722
24. Qamra R., Srinivas V., and Mande S.C. Mycobacterium tuberculosis GroEL homologues unusually exist as lower oligomers and retain the ability to suppress aggregation of substrate proteins. J Mol Biol 342 (2004) 605-617
25. Qamra R., and Mande S.C. Crystal structure of the 65-kilodalton heat shock protein, chaperonin 60.2, of Mycobacterium tuberculosis. J. Bacteriol 186 (2004) 8105-8113
26. Ojha A., Anand M., Bhatt A., Kremer L., Jacobs Jr. W.R., and Hatfull G.F. GroEL1: a dedicated chaperone involved in mycolic acid biosynthesis during biofilm formation in mycobacteria. Cell 123 (2005) 861-873
27. Basu D., Khare G., Singh S., Tyagi A., Khosla S., and Mande S.C. A novel nucleoid-associated protein of Mycobacterium tuberculosis is a sequence homolog of GroEL. Nucleic Acids Res 37 (2009) 4944-4954
28. Retzlaff C., Yamamoto Y., Hoffman P.S., Friedman H., and Klein T.W. Bacterial heat shock proteins directly induce cytokine mRNA and interleukin-1 secretion in macrophage cultures. Infect Immun 62 (1994) 5689-5693
29. Ragno S., Winrow V.R., Mascagni P., Lucietto P., Di Pierro F., Morris C.J., et al. A synthetic 10-kD heat shock protein (hsp10) from Mycobacterium tuberculosis modulates adjuvant arthritis. Clin Exp Immunol 103 (1996) 384-390
30. Agnello D., Scanziani E., Di G.M., Leoni F., Modena D., Mascagni P., et al. Preventive administration of Mycobacterium tuberculosis 10-kDa heat shock protein (hsp10) suppresses adjuvant arthritis in Lewis rats. Int. Immunopharmacol 2 (2002) 463-474
31. Vanags D., Williams B., Johnson B., Hall S., Nash P., Taylor A., et al. Therapeutic efficacy and safety of chaperonin 10 in patients with rheumatoid arthritis: a double-blind randomised trial. Lancet 368 (2006) 855-863
32. Jee B., Katoch V.M., and Awasthi S.K. Dissection of relationship between small heat shock proteins and mycobacterial diseases. Indian J Lepr 80 (2008) 231-245
33. Lee B.Y., Hefta S.A., and Brennan P.J. Characterisation of the major membrane protein of virulent Mycobacterium tuberculosis. Infect Immun 60 (1992) 2066-2074
34. Cunningham A.F., and Spreadbury C.L. Mycobacterial stationary phase induced by low oxygen tension: cell wall thickening and localization of the 16-kilodalton alpha-crystallin homolog. J Bacteriol 180 (1998) 801
35. Hu Y., Movahedzadeh F., Stoker N.G., and Coates A.R. Deletion of the Mycobacterium tuberculosis alpha-crystallin-like hspX gene causes increased bacterial growth in vivo. Infect Immun 74 (2006) 861-868
36. Yuan Y., Crane D.D., and Barry C.E. Stationary phase-associated protein expression in Mycobacterium tuberculosis: function of the mycobacterial alpha-crystallin homolog. J Bacteriol 178 (1996) 4484-4492
37. Kendall S.L., Movahedzadeh F., Rison S.C., Wernisch L., Parish T., Duncan K., et al. The Mycobacterium tuberculosis dosRS two-component system is induced by multiple stresses. Tuberculosis (Edinb) 84 (2004) 247-255
38. Wilkinson K.A., Stewart G.R., Newton S.M., Vordermeier H.M., Wain J.R., Murphy H.N., et al. Infection biology of a novel alpha-crystallin of Mycobacterium tuberculosis: Acr2. J Immunol 174 (2005) 4237-4243
39. Stewart G.R., Newton S.M., Wilkinson K.A., Humphreys I.R., Murphy H.N., Robertson B.D., et al. The stress-responsive chaperone alpha-crystallin 2 is required for pathogenesis of Mycobacterium tuberculosis. Mol Microbiol 55 (2005) 1127-1137
40. Meimaridou E., Gooljar S.B., and Chapple J.P. From hatching to dispatching: the multiple cellular roles of the Hsp70 molecular chaperone machinery. J Mol Endocrinol 42 (2009) 1-9
41. Méndez-Samperio P. Expression and regulation of chemokines in mycobacterial infection. J Infect 57 (2008) 374-384
42. Lehner T., Bergmeier L.A., Wang Y., Tao L., Sing M., Spallek R., et al. Heat shock proteins generate beta-chemokines which function as innate adjuvants enhancing adaptive immunity. Eur J Immunol 30 (2000) 594-603
43. Vabulas R.M., Ahmad-Nejad P., Ghose S., Kirschning C.J., Issels R.D., and Wagner H. Hsp70 as endogenous stimulus of the toll/interleukin-1 receptor signal pathway. J Biol Chem 277 (2002) 15107-15112
44. Wang Y., Kelly C.G., Karttunen J.T., Whittall T., Lehner P.J., Duncan L., et al. CD40 is a cellular receptor mediating mycobacterial heat shock protein 70 stimulation of CC-chemokines. Immunity 15 (2001) 971-983
45. Lazarevic V., Myers A.J., Scanga C.A., and Flynn J.L. CD40, but not CD40L, is required for the optimal priming of T cells and control of aerosol M. tuberculosis infection. Immunity 19 (2003) 823-835
46. Wang Y., Kelly C.G., Singh M., McGowan E.G., Carrara A.S., Bergmeier L.A., et al. 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 (2002) 2422-2429
47. Becker T., Hartl F.U., and Wieland F. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J Cell Biol 158 (2002) 1277-1285
48. Whittall T., Wang Y., Younson J., Kelly C., Bergmeier L., Peters B., et al. Interaction between the CCR5 chemokine receptors and microbial HSP70. Eur. J. Immunol 36 (2006) 2304-2314
49. Floto R.A., MacAry P.A., Boname J.M., Mien T.S., Kampmann B., Hair J.R., et al. Dendritic cell stimulation by mycobacterial Hsp70 is mediated through CCR5. Science 314 (2006) 454-458
50. Babaahmady K., Oehlmann W., Singh M., and Lehner T. 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 (2007) 3354-3360
51. Triantafilou K., Triantafilou M., and Dedrick R.L. A CD14-independent LPS receptor cluster. Nat Immunol 2 (2001) 338-345
52. Xolalpa W., Vallecillo A.J., Lara M., Mendoza-Hernandez G., Comini M., Spallek R., et al. Identification of novel bacterial plasminogen-binding proteins in the human pathogen Mycobacterium tuberculosis. Proteomics 7 (2008) 3332-3341
53. Aravundham V., Christy A.J., Roy S., Ajitkumar P., Narayanan P.R., and Narayanan S. Mycobacterium tuberculosis groE promoter controls the expression of the bicistronic groESL1 operon and shows differential regulation under stress conditions. FEMS Microbiol Lett 292 (2009) 42-49
54. Canova M.J., Kremer L., and Molle V. The Mycobacterium tuberculosis GroEL1 chaperone is a substrate of Ser/Thr protein kinases. J Bacteriol 191 (2009) 2876-2883
55. Cumar C.M., Khare G., Srikanth C.V., Tyagi A.K., Sardesai A.A., and Mande S.C. Facilitated oligomerisation of mycobacterial GroEL: evidence for phosphorylation-mediated oligomerization. J Bacteriol (2009) [Epub ahead of print]
56. Lukacs K.V., Lowrie D.B., Stokes R.W., and Colston M.J. Tumor cells transfected with a bacterial heat-shock gene lose tumorigenicity and induce protection against tumors. J Exp Med 178 (1993) 343-348
57. Jeffery C.J. Moonlighting proteins - an update. Mol Biosyst 5 (2009) 345-350
58. Gancedo C., and Flores C.L. Moonlighting proteins in yeast. Microbiol Mol Biol Rev 72 (2008) 197-210
59. Asquith K.L., Baleato R.M., McLaughlin E.A., Nixon B., and Aitken R.J. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 117 (2004) 3645-3657
60. Mitchell L.A., Nixon B., and Aitken R.J. Analysis of chaperone proteins associated with human spermatozoa during capacitation. Mol Hum Reprod 13 (2007) 605-613
61. Sengupta S., Ghosh S., and Nagaraja V. Moonlighting function of glutamate racemase from Mycobacterium tuberculosis: racemization and DNA gyrase inhibition are two independent activities of the enzyme. Microbiology 154 (2008) 2796-2803
62. Kremer L., Maughan W.N., Wilson R.A., Dover L.G., and Besra G.S. The M. tuberculosis antigen 85 complex and mycosyltransferase activity. Letts Appl Microbiol 34 (2002) 233-237
63. Kinhikar A.G., Vargas D., Li H., Mahaffey S.B., Hinds L., Belisle J.T., et al. Mycobacterium tuberculosis malate synthase is a laminin-binding adhesin. Mol Microbiol 60 (2006) 999-1013
64. Banerjee S., Nandyala A.K., Raviprasad P., Ahmed N., and Hasnain S.E. Iron-dependent RNA-binding activity of Mycobacterium tuberculosis aconitase. J Bacteriol 189 (2007) 4046-4052
65. Reddy V.M., and Suleman F.G. Mycobacterium avium-superoxide dismutase binds to epithelial cell aldolase, glyceraldehyde-3-phosphate dehydrogenase and cyclophilin A. Microb Pathog 36 (2004) 67-74
66. Podobnik M., Tyagi R., Matange N., Dermol U., Gupta A.K., Mattoo R., et al. A mycobacterial cyclic AMP phosphodiesterase that moonlights as a modifier of cell wall permeability. J Biol Chem 284 (2009) 32846-32857
67. Hazy E., and Tompa P. Limitations of induced folding in molecular recognition by intrinsically disordered proteins. Chemphyschem 10 (2009) 1415-1419