Identification of heat shock protein 60 as the ligand on Histoplasma capsulatum that mediates binding to CD18 receptors on human macrophages

Journal of Immunology

Volumn 170, Issue 1, 2003, Pages 487-494

  Long, Kristin H ^a   Gomez, Francisco J ^a,b   Morris, Randall E ^a   Newman, Simon L ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11 ANTIGEN; CD18 ANTIGEN; COMPLEMENT COMPONENT C3 RECEPTOR; HEAT SHOCK PROTEIN 60; LIGAND; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; MONOCLONAL ANTIBODY; POLYSTYRENE; RECOMBINANT PROTEIN; STREPTAVIDIN;

ANIMAL CELL; ARTICLE; BIOTINYLATION; CELL ADHESION; CELL MEMBRANE; CHO CELL; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC CELL; ELECTRON MICROSCOPY; FREEZING; GENETIC TRANSFECTION; HISTOPLASMA CAPSULATUM; HUMAN; HUMAN CELL; MACROPHAGE; MOLECULAR RECOGNITION; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRECIPITATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; WESTERN BLOTTING;

EID: 0037223264     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.170.1.487     Document Type: Article

References (57)

1. Deepe, G. S., and W. E. Bullock. 1992. Histoplasmosis: a granulomatous inflammatory response. In Inflammation: Basic Principles and Clinical Correlates. J. I. Gallin, I. M. Goldstein, and R. Snyderman, eds. Raven Press, New York, p. 943.
2. Bullock, W. E., and S. D. Wright. 1987. Role of the adherence-promoting receptors, CR3, LFA-1, and pI50,95, in binding of Histoplasma capsulatum by human macrophages. J. Exp. Med. 165:195.
3. Newman, S. L., C. Bucher, J. Rhodes, and W. E. Bullock. 1990. Phagocytosis of Histoplasma capsulatum yeasts and microconidia by human cultured macrophages and alveolar macrophages: Cellular cytoskeleton requirement for attachment and ingestion. J. Clin. Invest. 85:223.
4. Newman, S. L., L. Gootee, C. Bucher, and W. E. Bullock. 1991. Inhibition of intracellular growth of Histoplasma capsulatum yeast cells by cytokine-activated human monocytes and macrophages. Infect. Immun. 59:737.
5. Worsham, P. L., and W. E. Goldman. 1988. Quantitative plating of Histoplasma capsulatum without addition of conditioned medium or siderophores. J. Med. Vet. Mycol. 26:137.
6. Gomez, A. M., J. C. Rhodes, and G. S. Deepe, Jr. 1991. Antigenicity and immunogenicity of an extract from the cell wall and cell membrane of Histoplasma capsulatum yeast cells. Infect. Immun. 59:330.
7. Klein, B. S., and J. M. Jones. 1990. Isolation, purification, and radiolabeling of a novel 120-kD surface protein on Blastomyces dermatitidis yeasts to detect antibody in infected patients. J. Clin. Invest. 85:152.
8. Lumeng, J., L. Blickenstaff, and J. Miller. 1971. A rapid spectrophotometric system for measurement of lactic acid dehydrogenase activity. Am. J. Clin. Pathol. 55:471.
9. Gildea, L. A., R. E. Morris, and S. L. Newman. 2001. Histoplasma capsulatum yeasts are phagocytosed via very late antigen-5, killed, and processed for antigen presentation by human dendritic cells. J. Immunol. 166:1049.
10. Schnur, R. A., and S. L. Newman. 1990. The respiratory burst response to Histoplasma capsulatum by human neutrophils: Evidence for intracellular trapping of superoxide anion. J. Immunol. 144:4765.
11. Diamond, M. S., D. E. Staunton, A. R. de Fougerolles, S. A. Stacker, J. Garcia-Aguilar, M. L. Hibbs, and T. A. Springer. 1990. ICAM-1 (CD54): A counter-receptor for Mac-1 (CD11b/CD18). J. Cell Biol. 111:3129.
12. Todd, R. F., and M. A. Arnaout. 1986. Monoclonal antibodies that identify Mol and LFA-1, two human leukocyte membrane glycoproteins: A review. In Leukocyte Typing II, Vol. 3. E. L. Rheinerz, B. F. Haynes, L. M. Nadler, and I. D. Bernstein, eds. Springer-Verlag, New York, p. 95.
13. Eddy, A., S. L. Newman, F. Cosio, T. LeBien, and A. Michael. 1984. The distribution of the CR3 receptor on human cells and tissue as revealed by a monoclonal antibody. Clin. Immunol. Immunopathol. 31:371.
14. Lanier, L. L., M. A. Arnaout, R. Schwarting, N. L. Warner, and G. D. Ross. 1985. p150/95, third member of the LFA-1/CR3 polypeptide family identified by antiLeu M5 monoclonal antibody. Eur. J. Immunol. 15:713.
15. Wright, S. D., P. E. Rao, W. C. Van Voorhis, L. S. Craigmyle, K. Iida, M. A. Talle, E. F. Westberg, G. Goldstein, and S. C. Silverstein. 1983. Identification of the C3bi receptor of human monocytes and macrophages by using monoclonal antibodies. Proc. Natl. Acad. Sci. USA 80:5699.
16. Gomez, F. J., R. Allendoerfer, and G. S. Deepe, Jr. 1995. Vaccination with recombinant heat shock protein 60 from Histoplasma capsulatum protects mice against pulmonary histoplasmosis. Infect. Immun. 63:2587.
17. Gomez, F. J., A. M. Gomez, and G. S. Deepe, Jr. 1991. Protective efficacy of a 62-kilodalton antigen, HIS-62, from the cell wall and cell membrane of Histoplasma capsulatum yeast cells. Infect. Immmun. 59:4459.
18. Thornton, B. P., V. Vetvicka, M. Pitman, R. C. Goldman, and G. D. Ross. 1996. Analysis of the sugar specificity and molecular location of the β-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J. Immunol. 156:1235.
19. Newman, S. L., L. Gootee, R. Morris, and W. E. Bullock. 1992. Digestion of Histoplasma capsulatum yeasts by human macrophages [Published erratum appears in 1992 J. Immunol. 149:3127]. J. Immunol. 149:574.
20. Williams, M. A. 1981. Quantitative methods in biology. In Practical Methods in Electron Microscopy, Vol. 6. A. M. Glauert, ed. New Holland, New York. p. 2.
21. Griffiths, G. 1993. Fine Structure Immunocytochemistry. Springer-Verlag, New York.
22. Howard, C. V., and M. G. Reed. 1998. Unbiased Stereology: Three Dimensional Measurements in Microscopy. Springer-Verlag, New York.
23. Frydman, J., and F. Hartl. 1994. Molecular chaperone of Hsp70 and Hsp60 in protein folding. In The Biology of Heat Shock Protein and Molecular Chaperones. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, p. 251.
24. Kubota, H., G. Hynes, and K. Willison. 1995. The chaperonin containing t-complex polypeptide I (TCP-1): Multisubunit machinery assisting in protein folding and assembly in the eukaryotic cytosol. Eur. J. Biochem. 230:3.
25. Deepe, G. S., Jr., and R. Gibbons. 2001. Protective efficacy of H antigen from Histoplasma capsulatum in a murine model of pulmonary histoplasmosis. Infect. Immun. 69:3128.
26. Fisher, K. L.. and J. P. Woods. 2000. Determination of β-glucosidase enzymatic function of the Histoplasma capsulatum H antigen using a native expression system, Gene 247:191.
27. Sanchez-Madrid, F., J. A. Nagy, E. Robbins, P. Simon, and T. A. Springer. 1983. A human leukocyte differentiation antigen family with distinct α-subunits and a common β-subunit: The lymphocyte function-associated antigen (LFA-1), the C3bi complement receptor (OKM1/Mac-1), and the p150,95 molecule. J. Exp. Med. 158:1785.
28. Payne, N. R., and M. A. Horwitz. 1987. Phagocytosis of Legionella pneumophila is mediated by human monocyte complement receptors. J. Exp. Med. 166:1377.
29. Hirsch, C. S., J. J. Ellner, D. G. Russell, and E. A. Rich. 1994. Complement receptor-mediated uptake and tumor necrosis factor-α-mediated growth inhibition of Mycobacterium tuberculosis by human alveolar macrophages. J. Immunol. 152:743.
30. Da Silva, R. P., B. F. Hall, K. A. Joiner, and D. L. Sacks. 1989. CRI, the C3b receptor, mediates binding of infective Leishmania major metacyclic promastigotes to human macrophages. J. Immunol. 143:617.
31. Rosenthal, L. A., F. S. Sutterwala, M. E. Kehrli, and D. M. Mosser. 1996. Leishmania major-human macrophage interactions: Cooperation between Mac-1 (CD11b/CD18) and complement receptor type 1 (CD35) in promastigote adhesion. Infect. Immun. 64:2206.
32. Hmama, Z., A. Mey, G. Normier, H. Binz, and'J. P. Revillard. 1994. CD14 and CD11b mediate serum-independent binding to human monocytes of an acylpolygalactoside isolated from Klebsiella pneumoniae. Infect. Immun. 62:1520.
33. Hallberg, R. L. 1990. A mitochondrial chaperonin: Genetic, biochemical, and molecular characteristics. Semin. Cell. Biol. 1:37.
34. Hansen, K., J. M. Bangsborg, H. Fjordvang, N. S. Pedersen, and P. Hindersson. 1988. Immunochemical characterization of and isolation of the gene for a Borrelia burgdorferi immunodominant 60-kilodalton antigen common to a wide range of bacteria. Infect. Immun. 56:2047.
35. Luft, B. J., P. D. Gorevic, W. Jiang, P. Munoz, and R. J. Dattwyler. 1991. Immunologic and structural characterization of the dominant 66- to 73-kDa antigens of Borrelia burgdorferi. J. Immunol. 146:2776.
36. Bangsborg, J. M., M. T. Collins, N. Hoiby, and P. Hindersson. 1989. Cloning and expression of the Legionella micdadei "common antigen" in Escherichia coli. Apmis 97:14.
37. Morrison, R. P., R. J. Belland, K. Lyng, and H. D. Caldwell. 1989. Chlamydial disease pathogenesis: The 57-kD chlamydial hypersensitivity antigen is a stress response protein. J. Exp. Med. 170:1271.
38. Peeling, R. W., J. Kimani, F. Plummer, I. Maclean, M. Cheang, J. Bwayo, and R. C. Brunham. 1997. Antibody to chlamydial hsp60 predicts an increased risk for chlamydial pelvic inflammatory disease. J. Infect. Dis. 175:1153.
39. Vodkin, M. H., and J. C. Williams. 1988. A heat shock operon in Coxiella burnetti produces a major antigen homologous to a protein in both mycobacteria and Escherichia coli. J. Bacteriol. 170:1227.
40. Pannekoek, Y., I. G. Schuurman, J. Dankert, and J. P. van Putten. 1993. Immunogenicity of the meningococcal stress protein MSP63 during natural infection. Clin. Exp. Immunol. 93:377.
41. Stover, C. K., D. P. Marana, G. A. Dasch, and E. V. Oaks. 1990. Molecular cloning and sequence analysis of the Sta58 major antigen gene of Rickettsia tsutsugamushi: Sequence homology and antigenic comparison of Sta58 to the 60-kilodalton family of stress proteins. Infect. Immun. 58:1360.
42. Kaufmann. S. H., U. Vath, J. E. Thole, J. D. Van Embden, and F. Emmrich. 1987. Enumeration of T cells reactive with Mycobacterium tuberculosis organisms and specific for the recombinant mycobacterial 64-kDa protein. Eur. J. Immunol. 17:351.
43. Amini, H. R., F. Ascencio, A. Cruz-Villacorta, E. Ruiz-Bustos, and T. Wadstrom. 1996. Immunochemical properties of a 60 kDa cell surface-associated heat shockprotein (Hsp60) from Helicobacter pylori. FEMS Immunol. Med. Microbiol. 16:163.
44. Noll, A., and Autenriethlb. 1996. Immunity against Yersinia enterocolitica by vaccination with Yersinia HSP60 immunostimulating complexes or Yersinia HSP60 plus interleukin-12. Infect. Immun. 64:2955.
45. Sanchez, G. I., M. Sedegah, W. O. Rogers, T. R. Jones, J. Sacci, A. Witney, D. J. Carucci, N. Kumar, and S. L. Hoffman. 2001. Immunogenicity and protective efficacy of a Plasmodium yoelii Hsp60 DNA vaccine in BALB/c mice. Infect. Immun. 69:3897.
46. Ulanova, M., T. D. Petersen, O. Ciofu, P. Jensen, M. Hahn-Zoric, L. A. Hanson, and N. Hoiby. 1997. The clonal antibody response to Pseudomonas aeruginosa heat shock protein is highly diverse in cystic fibrosis patients. Apmis 105:449.
47. Thomas, P. W., E. E. Wyckoff, E. J. Pishko, J. J. Yu, T. N. Kirkland, and G. T. Cole. 1997. The hsp60 gene of the human pathogenic fungus Coccidioides immitis encodes a T-cell reactive protein. Gene 199:83.
48. Yamaguchi, H., T. Osaki, N. Kurihara, H. Taguchi, T. Hanawa, T. Yamamoto, and S. Kamiya. 1997. 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.
49. Hennequin, C., F. Porcheray, A. Waligora-Dupriet. A. Collignon, M. Barc, P. Bourlioux, and T. Karjalainen. 2001. GroEL (Hsp60) of Clostridium difficile is involved in cell adherence. Microbiology 147:87.
50. Garduno, R. A., G. Faulkner. M. A. Trevors, N. Vats, and P. S. Hoffman. 1998. Immunolocalization of Hsp60 in Legionella pneumophila. J. Bacteriol. 180:505.
51. Garduno, R. A., E. Garduno, and P. S. Hoffman. 1998. Surface-associated hsp60 chaperone of Legionella pneumophila mediates invasion in a HeLa cell model. Infect. Immun. 66:4602.
52. Newman, S. L., L. Gootee, C. Kidd, G. M. Ciraolo, and R. Morris. 1997. Activation of human macrophage fungistatic activity against Histoplasma capsulatum upon adherence to type 1 collagen matrices. J. Immunol. 158:1779.
53. 3 on human monocyte-derived macrophages enhances complement receptor type 3 expression. Infect. Immun. 65:1211.
54. Roecklein, J. A., R. P. Swartz. and H. Yeager, Jr. 1992. Nonopsonic uptake of Mycobacterium avium complex by human monocytes and alveolar macrophages. J. Lab. Clin. Med. 119:772.
55. Kol, A., A. H. Lichtman, R. W. Finberg, P. Libby, and E. A. Kurt-Jones. 2000. Cutting edge: Heat shock protein (HSP) 60 activates the innate immune response: CD14 is an essential receptor for HSP60 activation of mononuclear cells. J. Immunol. 164:13.
56. Ohashi, K., V. Burkart, S. Flohe. and H. Kolb. 2000. Cutting edge: Heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J. Immunol. 164:558.
57. Vabulas, R. M., P. Ahmad-Nejad, C. da Costa, T. Miethke, C. J. Kirschning, H. Hacker, and H. Wagner. 2001. Endocytosed HSP60s use Toll-like receptor 2 (TLR2) and TLR4 to activate the Toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276:31332.