Histoplasma capsulatum heat-shock 60 orchestrates the adaptation of the fungus to temperature stress

PLoS ONE

Volumn 6, Issue 2, 2011, Pages

  Guimarães, Allan Jefferson ^a   Nakayasu, Ernesto S ^b   Sobreira, Tiago J P ^c   Cordero, Radames J B ^a   Nimrichter, Leonardo ^d   Almeida, Igor C ^e   Nosanchuk, Joshua Daniel ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

^d FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^e UNIVERSITY OF TEXAS AT EL PASO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEAT SHOCK PROTEIN 60; VIRULENCE FACTOR;

ARTICLE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; CYTOPLASM; FUNGAL CELL; HEAT SHOCK RESPONSE; HISTOPLASMA CAPSULATUM; NONHUMAN; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TEMPERATURE ACCLIMATIZATION; TEMPERATURE STRESS;

ADAPTATION, PHYSIOLOGICAL; ANTIBODIES, MONOCLONAL; CHAPERONIN 60; CYTOPLASM; FUNGAL PROTEINS; HEAT-SHOCK RESPONSE; HISTOPLASMA; IMMUNOPRECIPITATION; INTRACELLULAR SPACE; PROTEIN TRANSPORT; SUBSTRATE SPECIFICITY; TEMPERATURE; UP-REGULATION;

AJELLOMYCES CAPSULATUS; FUNGI;

EID: 79951844190     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014660     Document Type: Article

References (67)

1. Lindquist S, (1986) The heat-shock response. Annu Rev Biochem 55: 1151-1191.
2. Wu C, (1995) Heat shock transcription factors: structure and regulation. Annu Rev Cell Dev Biol 11: 441-469.
3. Santoro MG, (2000) Heat shock factors and the control of the stress response. Biochem Pharmacol 59: 55-63.
4. Saibil HR, (2008) Chaperone machines in action. Curr Opin Struct Biol 18: 35-42.
5. Li Z, Srivastava P, (2004) Heat-shock proteins. Curr Protoc Immunol Appendix 1: Appendix 1T.
6. Burnie JP, Carter TL, Hodgetts SJ, Matthews RC, (2006) Fungal heat-shock proteins in human disease. FEMS Microbiol Rev 30: 53-88.
7. 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.
8. Habich C, Kempe K, Gomez FJ, Lillicrap M, Gaston H, et al. (2006) Heat shock protein 60: identification of specific epitopes for binding to primary macrophages. FEBS Lett 580: 115-120.
9. Guimaraes AJ, Frases S, Gomez FJ, Zancope-Oliveira RM, Nosanchuk JD, (2009) Monoclonal antibodies to heat shock protein 60 alter the pathogenesis of Histoplasma capsulatum. Infect Immun 77: 1357-1367.
10. Guimaraes AJ, Frases S, Pontes B, MD DEC, Rodrigues ML, et al. (2010) Agglutination of Histoplasma capsulatum by IgG monoclonal antibodies against Hsp60 impacts macrophage effector functions. Infect Immun.
11. Gomez BL, Figueroa JI, Hamilton AJ, Ortiz BL, Robledo MA, et al. (1997) Development of a novel antigen detection test for histoplasmosis. J Clin Microbiol 35: 2618-2622.
12. Gomez FJ, Gomez AM, Deepe GS Jr, (1992) An 80-kilodalton antigen from Histoplasma capsulatum that has homology to heat shock protein 70 induces cell-mediated immune responses and protection in mice. Infect Immun 60: 2565-2571.
13. Lopes LC, Guimaraes AJ, de Cerqueira MD, Gomez BL, Nosanchuk JD, (2010) A Histoplasma capsulatum-specific IgG1 isotype monoclonal antibody, H1C, to a 70-kilodalton cell surface protein is not protective in murine histoplasmosis. Clin Vaccine Immunol 17: 1155-1158.
14. Shapiro RS, Cowen L Coupling temperature sensing and development: Hsp90 regulates morphogenetic signalling in Candida albicans. Virulence 1: 45-48.
15. Shapiro RS, Uppuluri P, Zaas AK, Collins C, Senn H, et al. (2009) Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr Biol 19: 621-629.
16. Shaner L, Gibney PA, Morano KA, (2008) The Hsp110 protein chaperone Sse1 is required for yeast cell wall integrity and morphogenesis. Curr Genet 54: 1-11.
17. Gophna U, Ron EZ, (2003) Virulence and the heat shock response. Int J Med Microbiol 292: 453-461.
18. Cabiscol E, Belli G, Tamarit J, Echave P, Herrero E, et al. (2002) Mitochondrial Hsp60, resistance to oxidative stress, and the labile iron pool are closely connected in Saccharomyces cerevisiae. J Biol Chem 277: 44531-44538.
19. Voos W, (2003) A new connection: chaperones meet a mitochondrial receptor. Mol Cell 11: 1-3.
20. Voos W, (2009) Mitochondrial protein homeostasis: the cooperative roles of chaperones and proteases. Res Microbiol 160: 718-725.
21. Voos W, Rottgers K, (2002) Molecular chaperones as essential mediators of mitochondrial biogenesis. Biochim Biophys Acta 1592: 51-62.
22. Kamei K, Brummer E, Clemons KV, Stevens DA, (1992) Induction of stress protein synthesis in Histoplasma capsulatum by heat, low pH and hydrogen peroxide. J Med Vet Mycol 30: 385-393.
23. Allendoerfer R, Biovin GP, Deepe GS Jr, (1997) Modulation of immune responses in murine pulmonary histoplasmosis. J Infect Dis 175: 905-914.
24. Pitarch A, Sanchez M, Nombela C, Gil C, (2002) Sequential fractionation and two-dimensional gel analysis unravels the complexity of the dimorphic fungus Candida albicans cell wall proteome. Mol Cell Proteomics 1: 967-982.
25. Mrsa V, Seidl T, Gentzsch M, Tanner W, (1997) Specific labelling of cell wall proteins by biotinylation. Identification of four covalently linked O-mannosylated proteins of Saccharomyces cerevisiae. Yeast 13: 1145-1154.
26. Nosanchuk JD, Steenbergen JN, Shi L, Deepe GS Jr, Casadevall A, (2003) Antibodies to a cell surface histone-like protein protect against Histoplasma capsulatum. J Clin Invest 112: 1164-1175.
27. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
28. Pizzini CV, Zancope-Oliveira RM, Reiss E, Hajjeh R, Kaufman L, et al. (1999) Evaluation of a western blot test in an outbreak of acute pulmonary histoplasmosis. Clin Diagn Lab Immunol 6: 20-23.
29. Guimaraes AJ, Hamilton AJ, de MGHL, Nosanchuk JD, Zancope-Oliveira RM, (2008) Biological function and molecular mapping of M antigen in yeast phase of Histoplasma capsulatum. PLoS One 3: e3449.
30. Guimaraes AJ, Almeida MA, Pizzini CV, Peralta JM, Nosanchuk JD, et al. (2010) Evaluation of an Enzyme Linked Immunosorbent Assay (ELISA) using purified, deglycosylated histoplasmin for different clinical manifestations of Histoplasmosis. Microbiology Research 2.
31. Gomez FJ, Allendoerfer R, Deepe GS Jr, (1995) Vaccination with recombinant heat shock protein 60 from Histoplasma capsulatum protects mice against pulmonary histoplasmosis. Infect Immun 63: 2587-2595.
32. Stone KL, Williams KR, (1996) Enzymatic Digestion of Proteins in Solution and in SDS Polyacrylamide Gels. Totowa, NJ Humana Press.
33. Jurado JD, Rael ED, Lieb CS, Nakayasu E, Hayes WK, et al. (2007) Complement inactivating proteins and intraspecies venom variation in Crotalus oreganus helleri. Toxicon 49: 339-350.
34. Lundgren DH, Han DK, Eng JK, (2005) Protein identification using TurboSEQUEST. Curr Protoc Bioinformatics Chapter 13: Unit 13 13.
35. Albuquerque PC, Nakayasu ES, Rodrigues ML, Frases S, Casadevall A, et al. (2008) Vesicular transport in Histoplasma capsulatum: an effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes. Cell Microbiol 10: 1695-1710.
36. Mewes HW, Frishman D, Mayer KF, Munsterkotter M, Noubibou O, et al. (2006) MIPS: analysis and annotation of proteins from whole genomes in 2005. Nucleic Acids Res 34: D169-172.
37. Stark C, Breitkreutz BJ, Reguly T, Boucher L, Breitkreutz A, et al. (2006) BioGRID: a general repository for interaction datasets. Nucleic Acids Res 34: D535-539.
38. Krogan NJ, Cagney G, Yu H, Zhong G, Guo X, et al. (2006) Global landscape of protein complexes in the yeast Saccharomyces cerevisiae. Nature 440: 637-643.
39. Liu H, Sadygov RG, Yates JR 3rd, (2004) A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal Chem 76: 4193-4201.
40. Ishihama Y, Oda Y, Tabata T, Sato T, Nagasu T, et al. (2005) Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 4: 1265-1272.
41. Gomez FJ, Gomez AM, Deepe GS Jr, (1991) Protective efficacy of a 62-kilodalton antigen, HIS-62, from the cell wall and cell membrane of Histoplasma capsulatum yeast cells. Infect Immun 59: 4459-4464.
42. Kaufmann SH, (1990) Heat-shock proteins: a missing link in the host-parasite relationship? Med Microbiol Immunol 179: 61-66.
43. Elad N, Farr GW, Clare DK, Orlova EV, Horwich AL, et al. (2007) Topologies of a substrate protein bound to the chaperonin GroEL. Mol Cell 26: 415-426.
44. Horwich AL, Fenton WA, Chapman E, Farr GW, (2007) Two families of chaperonin: physiology and mechanism. Annu Rev Cell Dev Biol 23: 115-145.
45. Habich C, Burkart V, (2007) Heat shock protein 60: regulatory role on innate immune cells. Cell Mol Life Sci 64: 742-751.
46. Jethmalani SM, Henle KJ, Gazitt Y, Walker PD, Wang SY, (1997) Intracellular distribution of heat-induced stress glycoproteins. J Cell Biochem 66: 98-111.
47. Soltys BJ, Gupta RS, (1997) Cell surface localization of the 60 kDa heat shock chaperonin protein (hsp60) in mammalian cells. Cell Biol Int 21: 315-320.
48. Jethmalani SM, Henle KJ, (1997) Intracellular distribution of stress glycoproteins in a heat-resistant cell model expressing human HSP70. Biochem Biophys Res Commun 237: 382-387.
49. Barreto A, Gonzalez JM, Kabingu E, Asea A, Fiorentino S, (2003) Stress-induced release of HSC70 from human tumors. Cell Immunol 222: 97-104.
50. Davies EL, Bacelar MM, Marshall MJ, Johnson E, Wardle TD, et al. (2006) Heat shock proteins form part of a danger signal cascade in response to lipopolysaccharide and GroEL. Clin Exp Immunol 145: 183-189.
51. Hunter-Lavin C, Davies EL, Bacelar MM, Marshall MJ, Andrew SM, et al. (2004) Hsp70 release from peripheral blood mononuclear cells. Biochem Biophys Res Commun 324: 511-517.
52. Eissenberg LG, Goldman WE, (1987) Histoplasma capsulatum fails to trigger release of superoxide from macrophages. Infect Immun 55: 29-34.
53. Wolf AM, (1987) Histoplasma capsulatum osteomyelitis in the cat. J Vet Intern Med 1: 158-162.
54. Wolf JE, Kerchberger V, Kobayashi GS, Little JR, (1987) Modulation of the macrophage oxidative burst by Histoplasma capsulatum. J Immunol 138: 582-586.
55. Maresca B, Kobayashi G, (1993) Changes in membrane fluidity modulate heat shock gene expression and produced attenuated strains in the dimorphic fungus Histoplasma capsulatum. Arch Med Res 24: 247-249.
56. Maresca B, Kobayashi GS, (1989) Dimorphism in Histoplasma capsulatum: a model for the study of cell differentiation in pathogenic fungi. Microbiol Rev 53: 186-209.
57. Shearer G Jr, Birge CH, Yuckenberg PD, Kobayashi GS, Medoff G, (1987) Heat-shock proteins induced during the mycelial-to-yeast transitions of strains of Histoplasma capsulatum. J Gen Microbiol 133: 3375-3382.
58. Minchiotti G, Gargano S, Maresca B, (1992) Molecular cloning and expression of hsp82 gene of the dimorphic pathogenic fungus Histoplasma capsulatum. Biochim Biophys Acta 1131: 103-107.
59. Caruso M, Sacco M, Medoff G, Maresca B, (1987) Heat shock 70 gene is differentially expressed in Histoplasma capsulatum strains with different levels of thermotolerance and pathogenicity. Mol Microbiol 1: 151-158.
60. Keath EJ, Painter AA, Kobayashi GS, Medoff G, (1989) Variable expression of a yeast-phase-specific gene in Histoplasma capsulatum strains differing in thermotolerance and virulence. Infect Immun 57: 1384-1390.
61. Patriarca EJ, Kobayashi GS, Maresca B, (1992) Mitochondrial activity and heat-shock response during morphogenesis in the pathogenic fungus Histoplasma capsulatum. Biochem Cell Biol 70: 207-214.
62. Tapley TL, Franzmann TM, Chakraborty S, Jakob U, Bardwell JC, Protein refolding by pH-triggered chaperone binding and release Proc Natl Acad Sci U S A 107: 1071-1076.
63. Tapley TL, Korner JL, Barge MT, Hupfeld J, Schauerte JA, et al. (2009) Structural plasticity of an acid-activated chaperone allows promiscuous substrate binding. Proc Natl Acad Sci U S A 106: 5557-5562.
64. Gong Y, Kakihara Y, Krogan N, Greenblatt J, Emili A, et al. (2009) An atlas of chaperone-protein interactions in Saccharomyces cerevisiae: implications to protein folding pathways in the cell. Mol Syst Biol 5: 275.
65. Lambowitz AM, Kobayashi GS, Painter A, Medoff G, (1983) Possible relationship of morphogenesis in pathogenic fungus, Histoplasma capsulatum, to heat shock response. Nature 303: 806-808.
66. Borgia G, Tallarino A, Crowell J, Lambiase A, Cicciarello S, et al. (1990) The effect of temperature on the ultrastructure of Histoplasma capsulatum during the mycelium-yeast transition. Mycoses 33: 405-410.
67. Maresca B, Lambowitz AM, Kumar VB, Grant GA, Kobayashi GS, et al. (1981) Role of cysteine in regulating morphogenesis and mitochondrial activity in the dimorphic fungus Histoplasma capsulatum. Proc Natl Acad Sci U S A 78: 4596-4600.