Identification of pH-regulated antigen 1 released from Candida albicans as the major ligand for leukocyte integrin αMβ2

Journal of Immunology

Volumn 178, Issue 4, 2007, Pages 2038-2046

  Soloviev, Dmitry A ^a   Fonzi, William A ^b   Sentandreu, Rafael ^c   Pluskota, Elzbieta ^a   Forsyth, Christopher B ^a   Yadav, Satya ^a   Plow, Edward F ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; FUNGUS ANTIGEN; INTEGRIN ALPHAMBETA2; MONOCLONAL ANTIBODY; PROTEIN PRA1P; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANTIGEN RECOGNITION; ARTICLE; CANDIDA ALBICANS; CELLULAR IMMUNITY; CONTROLLED STUDY; ENZYME ACTIVITY; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNE DEFICIENCY; IMMUNOSURVEILLANCE; INNATE IMMUNITY; LEUKOCYTE ADHERENCE; LEUKOCYTE MIGRATION; NEUTROPHIL; NONHUMAN; OPPORTUNISTIC INFECTION; PHAGOCYTOSIS; PRIORITY JOURNAL; SEQUENCE ANALYSIS;

EID: 33846915360     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.4.2038     Document Type: Article

References (64)

1. Cole, G. T., A. A. Halawa, and E. J. Anaissie. 1996. The role of the gastrointestinal tract in hematogenous candidiasis: from the laboratory to the bedside. Clin. Infect. Dis. 22(Suppl. 2): 73-88.
2. Abelson, J. A., T. Moore, D. Bruckner, J. Deville, and K. Nielsen. 2005. Frequency of fungemia in hospitalized pediatric inpatients over 11 years at a tertiary care institution. Pediatrics 116: 61-67.
3. Wingard, J. R. 1994. Infections due to resistant Candida species in patients with cancer who are receiving chemotherapy. Clin. Infect. Dis. 19(Suppl. 1): 49-53.
4. Richardson, M. D. 2005. Changing patterns and trends in systemic fungal infections. J. Antimicrob. Chemother. 56(Suppl. 1): i5-i11.
5. Tavanti, A., A. D. Davidson, M. J. Fordyce, N. A. Gow, M. C. Maiden, and F. C. Odds. 2005. Population structure and properties of Candida albicans, as determined by multilocus sequence typing. J. Clin. Microbiol. 43: 5601-5613.
6. Pfaller, M. A., L. Boyken, R. J. Hollis, S. A. Messer, S. Tendolkar, and D. J. Diekema. 2005. In vitro activities of anidulafungin against more than 2,500 clinical isolates of Candida spp., including 315 isolates resistant to fluconazole. J. Clin. Microbiol. 43: 5425-5427.
7. Diamond, R. D. 1993. Interactions of phagocytic cells with Candida and other opportunistic fungi. Arch. Med. Res. 24: 361-369.
8. Lehrer, R. I., and M. J. Cline. 1969. Interaction of Candida albicans with human leukocytes and serum. J. Bacteriol. 98: 996-1004.
9. Smail, E. H., D. A. Melnick, R. Ruggeri, and R. D. Diamond. 1988. A novel natural inhibitor from Candida albicans hyphae causing dissociation of the neutrophil respiratory burst response to chemotactic peptides from other post-activation events. J. Immunol. 140: 3893-3899.
10. Baghian, A., and K. W. Lee. 1988. Role of activated macrophages in resistance to systemic candidosis. J. Leukocyte Biol. 44: 166-171.
11. Bistoni, F., A. Vecchiarelli, E. Cenci, P. Puccetti, P. Marconi, and A. Cassone. 1986. Evidence for macrophage-mediated protection against lethal Candida albicans infection. Infect. Immun. 51: 668-674.
12. Netea, M. G., K. Gijzen, N. Coolen, I. Verschueren, C. G. Figdor, J. W. Van der Meer, R. Torensma, and B. J. Kullberg. 2004. Human dendritic cells are less potent at killing Candida albicans than both monocytes and macrophages. Microbes Infect. 6: 985-989.
13. Anderson, D. C., F. C. Schmalsteig, M. J. Finegold, B. J. Hughes, R. Rothlein, L. J. Miller, S. Kohl, M. F. Tosi, R. L. Jacobs, T. C. Waldrop, et al. 1985. The severe and moderate phenotypes of heritable Mac-1, LFA-1 deficiency: their quantitative definition and relation to leukocyte dysfunction and clinical features. J. Infect. Dis. 152: 668-689.
14. Andrews, T., and K. E. Sullivan. 2003. Infections in patients with inherited defects in phagocytic function. Clin. Microbiol. Rev. 16: 597-613.
15. Forsyth, C. B., and H. L. Mathews. 1996. Lymphocytes utilize CD11b/CD18 for adhesion to Candida albicans. Cell Immunol. 170: 91-100.
16. Forsyth, C. B., E. F. Plow, and L. Zhang. 1998. Interaction of the fungal pathogen Candida albicans with integrin CD11b/CD18: recognition by the I domain is modulated by the lectin-like domain and the CD18 subunit. J. Immunol. 161: 6198-6205.
17. Edens, H. A., C. A. Parkos, T. W. Liang, A. J. Jesaitis, J. E. Cutler, and H. M. Miettinen. 1999. Non-serum-dependent chemotactic factors produced by Candida albicans stimulate chemotaxis by binding to the formyl peptide receptor on neutrophils and to an unknown receptor on macrophages. Infect. Immun. 67: 1063-1071.
18. Forsyth, C. B., and H. L. Mathews. 1993. A quantitative radiometric assay to measure mammalian cell binding to hyphae of Candida albicans. J. Immunol. Methods 165: 113-119.
19. Forsyth, C. B., and H. L. Mathews. 2002. Lymphocyte adhesion to Candida albicans. Infect. Immun. 70: 517-527.
20. Cutler, J. E. 1977. Chemotactic factor produced by Candida albicans. Infect. Immun. 18: 568-573.
21. Geiger, J., D. Wessels, R. S. Lockhart, and D. R. Soll. 2004. Release of a potent polymorphonuclear leukocyte chemoattractant is regulated by white-opaque switching in Candida albicans. Infect. Immun. 72: 667-677.
22. Diamond, R. D., F. Oppenheim, Y. Nakagawa, R. Krzesicki, and C. C. Haudenschild. 1980. Properties of a product of Candida albicans hyphae and pseudohyphae that inhibits contact between the fungi and human neutrophils in vitro. J. Immunol. 125: 2797-2804.
23. Fonzi, W. A. 1999. PHR1 and PHR2 of Candida albicans encode putative glycosidases required for proper cross-linking of β-1,3- and β-1,6-glucans. J. Bacteriol. 181: 7070-7079.
24. Sentandreu, M., M. V. Elorza, R. Sentandrreu, and W. A. Fonzi. 1998. Cloning and characterization of PRA1, a gene encoding a novel pH-regulated antigen of Candida albicans. J. Bacteriol. 180: 282-289.
25. Vosbeck, K. D., B. D. Greenberg, M. S. Ochoa, P. L. Whitney, and W. M. Awad, Jr. 1979. Proteolytic enzymes of the K-I strain of Streptomyces griseus obtained from a commercial preparation (Pronase): effect of pH, metal ions, and amino acids on aminopeptidase activity. J. Biol. Chem. 253: 257-260.
26. 2 for a specific and high affinity ligand, NIF. J. Biol. Chem. 272: 17558-17564.
27. 2. J. Biol. Chem. 271: 29953-29957.
28. Herren, T., T. A. Burke, M. Jardi, J. Felez, and E. F. Plow. 2001. Regulation of plasminogen binding to neutrophils. Blood 97: 1070-1078.
29. Miller, L. J., J. Wiebe, and T. A. Springer. 1987. Purification and α subunit N-terminal sequences of human Mac-1 and p150,95 leukocyte adhesion proteins. J. Immunol. 138: 2381-2383.
30. 2 orchestrates and accelerates plasminogen activation and fibrinolysis by neutrophils. J. Biol. Chem. 279: 18063-18072.
31. 2. J. Biol. Chem. 280: 1336-1345.
32. Muhlschlegel, F. A., and W. A. Fonzi. 1997. PHR2 of Candida albicans encodes a functional homolog of the pH-regulated gene PHR1 with an inverted pattern of pH-dependent expression. Mol. Cell Biol. 17: 5960-5967.
33. 2-mediated cell migration to fibrinogen and its recognition peptides. J. Exp. Med. 193: 1123-1131.
34. Willard, B. B., C. I. Ruse, J. A. Keightley, M. Bond, and M. Kinter. 2003. Site-specific quantitation of protein nitration using liquid chromatography/tandem mass spectrometry. Anal. Chem. 75: 2370-2376.
35. 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. J. Immunol. 156: 1235-1246.
36. Lopez-Ribot, J. L., P. Sepulveda, A. M. Cervera, P. Roig, D. Gozalbo, and J. P. Martinez. 1997. Cloning of a cDNA fragment encoding part of the protein moiety of the 58-kDa fibrinogen-binding mannoprotein of Candida albicans. Microbiol. Rev. 157: 273-278.
37. Gomez, M. J., A. Torosantucci, S. Arancia, B. Maras, L. Parisi, and A. Cassone. 1996. Purification and biochemical characterization of a 65-kilodalton mannoprotein (MP65), a main target of anti-Candida cell-mediated immune responses in humans. Infect. Immun. 64: 2577-2584.
38. Bailey, D. A., P. J. Feldmann, M. Bovey, N. A. Gow, and A. J. Brown. 1996. The Candida albicans HYR1 gene, which is activated in response to hyphal development, belongs to a gene family encoding yeast cell wall proteins. J. Bacteriol. 178: 5353-5360.
39. Diamond, M. S., J. Garcia-Aguilar, J. K. Bickford, A. L. Corbí, and T. A. Springer. 1993. The I domain is a major recognition site on the leukocyte integrin MAC-1 (CD11b/CD18) for four distinct adhesion ligands. J. Cell Biol. 120: 1031-1043.
40. Landis, R. C., A. McDowall, C. L. Holness, A. J. Littler, D. L. Simmons, and N. Hogg. 1994. Involvement of the "I" domain of LFA-1 in selective binding to ligands ICAM-I and ICAM-3. J. Cell Biol. 126: 529-537.
41. 2 as well as by the urokinase receptor regulates cell adhesion and migration. Blood 101: 1582-1590.
42. López-Ribot, J. L., C. Monteagudo, P. Sepúlveda, M. Casanova, J. P. Martinez, and W. L. Chaffin. 1996. Expression of the fibrinogen binding mannoprotein and the laminin receptor of Candida albicans in vitro and in infected tissues. FEMS Microb. Lett. 142: 117-122.
43. Saporito-Irwin, S. M., C. E. Birse, P. S. Sypherd, and W. A. Fonzi. 1995. PHR1, a pH-regulated gene of Candida albicans, is required for morphogenesis. Mol. Cell Biol. 15: 601-613.
44. Choi, W., Y. J. Yoo, M. Kim, D. Shin, H. B. Jeon, and W. Choi. 2003. Identification of proteins highly expressed in the hyphae of Candida albicans by two-dimensional electrophoresis. Yeast 20: 1053-1060.
45. Parkos, C. A., C. Delp, M. A. Arnaout, and J. L. Madara. 1991. Neutrophil migration across a cultured intestinal epithelium: dependence on a CD11b/CD18-mediated event and enhanced efficiency in physiological direction. J. Clin. Invest. 88: 1605-1612.
46. Springer, T. A., D. Davignon, M. K. Ho, K. Kurzinger, E. Martz, and F. Sanchez-Madrid. 1982. LFA-1 and Lyt-2,3,molecules associated with T lymphocyte-mediated killing; and Mac-1, an LFA-1 homologue associated with complement receptor function. Immunol. Rev. 68: 171-195.
47. 2 integrins: moderators of life or death decisions. Trends Immunol. 26: 388-395.
48. Jongstra-Bilen, J., R. Harrison, and S. Grinstein. 2003. Fcγ-receptors induce Mac-1 (CD11b/CD18) mobilization and accumulation in the phagocytic cup for optimal phagocytosis. J. Biol. Chem. 278: 45720-45729.
49. Polonelli, L., M. Gerloni, S. Conti, P. Fisicaro, C. Cantelli, P. Portincasa, F. Almondo, P. L. Barea, F. L. Hernando, and J. Ponton. 1994. Heat-shock mannoproteins as targets of secretory IgA in Candida albicans. J. Infect. Dis. 169: 1401-1405.
50. Chaffin, W. L., J. L. Lopez-Ribot, M. Casanova, D. Gozalbo, and J. P. Martinez. 1998. Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol. Mol. Biol. Rev. 62: 130-180.
51. Sepulveda, P., J. L. Lopez-Ribot, D. Gozalbo, A. Cervera, J. P. Martinez, and W. L. Chaffin. 1996. Ubiquitin-like epitopes associated with Candida albicans cell surface receptors. Infect. Immun. 64: 4406-4408.
52. Welzenbach, K., U. Hommel, and G. Weitz-Schmidt. 2002. Small molecule inhibitors induce conformational changes in the I Domain and the I-like domain of lymphocyte function-associated antigen-1. J. Biol. Chem. 277: 10590-10598.
53. Ustinov, V. A., and E. F. Plow. 2005. Identity of the amino acid residues involved in C3bi binding to the I-domain supports a mosaic model to explain the broad ligand repertoire of integrin α M β 2. Biochemistry 44: 4357-4364.
54. 2 to recognize multiple ligands. J. Biol. Chem. 277: 18769-18776.
55. Tronchin, G., R. Robert, A. Bouali, and J. M. Senet. 1987. Immunocytochemical localization of in vitro binding of human fibrinogen to Candida albicans germ tube and mycelium. Ann. Inst. Pasteur Microbiol. 138: 177-187.
56. Lopez-Ribot, J. L., J. P. Martinez, and W. L. Chaffin. 1995. Comparative study of the C3d receptor and 58-kilodalton fibrinogen-binding mannoproteins of Candida albicans. Infect. Immun. 63: 2126-2132.
57. Sepulveda, P., J. L. Lopez-Ribot, A. Murgui, E. Canton, D. Navarro, and J. P. Martinez. 1998. Candida albicans fibrinogen binding mannoprotein: expression in clinical strains and immunogenicity in patients with candidiasis. Int. Microbiol. 1: 209-216.
58. Cheung, A. L., M. Krishnan, E. A. Jaffe, and V. A. Fischetti. 1991. Fibrinogen acts as a bridging molecule in the adherence of Staphylococcus aureus to cultured human endothelial cells. J. Clin. Invest. 87: 2236-2245.
59. Sepúlveda, P., A. Mirgui, J. L. Lopez-Ribot, M. Casanova, J. Timoneda, and J. P. Martinez. 1995. Evidence for the presence of collagenous domains in Candida albicans cell surface proteins. Infect. Immun. 63: 2173-2179.
60. Muhlschlegal, F., W. A. Fonzi, L. W. Hoyer, T. Payne, F. M. Poulet, J. Clevenger, J. P. Latge, J. Calera, A. Beauvais, S. Paris, et al. 1998. Molecular mechanisms of virulence in fungus-host interactions for Aspergillus fumigatus and Candida albicans. Med. Mycol. 36(Suppl. 1): 238-348.
61. De Bernardis, F., F. A. Muhlschlegel, A. Cassone, and W. A. Fonzi. 1998. The pH of the host niche controls gene expression in and virulence of Candida albicans. Infect. Immun. 66: 3317-3325.
62. Smith, C., T. Davis, D. Anderson, L. Solam, M. Becman, R. Jerzy, S. Dower, D. Cosman, and R. Goodwin. 1990. A receptor for tumor necrosis factor defines an unusual family of cellular and viral proteins. Science 248: 1019-1023.
63. Smith, C., F. Hu, T. Smith, C. Richards, P. Smolac, R. Goodwin, and D. Pickup. 1996. Compox virus genome encodes a second soluble homologue of cellular TNF receptors, distinct from CrmB, that binds TNF but not LT α. Virology 223: 134-147.
64. Torosantucci, A., C. Bromuro, M. J. Gomez, C. M. Ausiello, F. Urbani, and A. Cassone. 1993. Identification of a 65-kDa mannoprotein as a main target of human cell-mediated immune response to Candida albicans. J. Infect. Dis. 168: 427-435.