Identification of a novel sialic acid transporter in Haemophilus ducreyi

Infection and Immunity

Volumn 73, Issue 10, 2005, Pages 6727-6735

  Post, Deborah M B ^a   Mungur, Rachna ^b   Gibson, Bradford W ^a,c   Munson Jr , Robert S ^b  

^a BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; AGGLUTININ; CARRIER PROTEIN; GALACTOSE; LECTIN; MONOCLONAL ANTIBODY; MONOCLONAL ANTIBODY 3F11; N ACETYLLACTOSAMINE; SIALIC ACID; SIALIC ACID TRANSPORTER; SILVER; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CARBOHYDRATE TRANSPORT; GENE CLUSTER; GENE MAPPING; HAEMOPHILUS DUCREYI; ISOTOPE LABELING; MAACKIA; MAACKIA AMURENSIS; MASS SPECTROMETRY; MOLECULAR RECOGNITION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; SILVER STAINING; TRANSPOSON; ULCUS MOLLE;

AMINO SUGARS; ANTIBODIES, MONOCLONAL; BACTERIAL PROTEINS; BIOLOGICAL TRANSPORT; CHROMOSOME MAPPING; GENE SILENCING; HAEMOPHILUS DUCREYI; LIPOPOLYSACCHARIDES; MUTAGENESIS, INSERTIONAL; MUTATION; N-ACETYLNEURAMINIC ACID; ORGANIC ANION TRANSPORTERS; SYMPORTERS;

EID: 25444493368     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.73.10.6727-6735.2005     Document Type: Article

References (71)

1. Ahmed, H. J., A. Frisk, J. E. Mansson, E. K. Schweda, and T. Lagergard. 1997. Structurally defined epitopes of Haemophilus ducreyi lipooligosaccharides recognized by monoclonal antibodies. Infect. Immun. 65:3151-3158.
2. Alfa, M. J., and P. DeGagne. 1997. Attachment of Haemophilus ducreyi to human foreskin fibroblasts involves LOS and fibronectin. Microb. Pathog. 22:39-46.
3. Alfa, M. J., P. DeGagne, and P. A. Totten. 1996. Haemophilus ducreyi hemolysin acts as a contact cytotoxin and damages human foreskin fibroblasts in cell culture. Infect. Immun. 64:2349-2352.
4. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
5. Apicella, M. A., R. E. Mandrell, M. Shero, M. E. Wilson, J. M. Griffiss, G. F. Brooks, C. Lammel, J. F. Breen, and P. A. Rice. 1990. Modification by sialic acid of Neisseria gonorrhoeae lipooligosaccharide epitope expression in human urethral exudates: an immunoelectron microscopic analysis. J. Infect. Dis. 162:506-512.
6. Bozue, J. A., M. V. Tullius, J. Wang, B. W. Gibson, and R. S. Munson, Jr. 1999. Haemophilus ducreyi produces a novel sialyltransferase. Identification of the sialyltransferase gene and construction of mutants deficient in the production of the sialic acid-containing glycoform of the lipooligosaccharide. J. Biol. Chem. 274:4106-4114.
7. Campagnari, A. A., R. Karalus, M. Apicella, W. Melaugh, A. J. Lesse, and B. W. Gibson. 1994. Use of pyocin to select a Haemophilus ducreyi variant defective in lipooligosaccharide biosynthesis. Infect. Immun. 62:2379-2386.
8. Campagnari, A. A., S. M. Spinola, A. J. Lesse, Y. A. Kwaik, R. E. Mandrell, and M. A. Apicella. 1990. Lipooligosaccharide epitopes shared among gram-negative non-enteric mucosal pathogens. Microb. Pathog. 8:353-362.
9. Cole, L. E., T. H. Kawula, K. L. Toffer, and C. Elkins. 2002. The Haemophilus ducreyi serum resistance antigen DsrA confers attachment to human keratinocytes. Infect. Immun. 70:6158-6165.
10. Cope, L. D., S. Lumbley, J. L. Latimer, J. Klesney-Tait, M. K. Stevens, L. S. Johnson, M. Purven, R. S. Munson, Jr., T. Lagergard, J. D. Radolf, and E. J. Hansen. 1997. A diffusible cytotoxin of Haemophilus ducreyi. Proc. Natl. Acad. Sci. USA 94:4056-4061.
11. Cortes-Bratti, X., C. Karlsson, T. Lagergard, M. Thelestam, and T. Frisan. 2001. The Haemophilus ducreyi cytolethal distending toxin induces cell cycle arrest and apoptosis via the DNA damage checkpoint pathways. J. Biol. Chem. 276:5296-5302.
12. Davidson, A. L., and J. Chen. 2004. ATP-binding cassette transporters in bacteria. Annu. Rev. Biochem. 73:241-268.
13. Deng, K., and E. J. Hansen. 2003. A CdtA-CdtC complex can block killing of HeLa cells by Haemophilus ducreyi cytolethal distending toxin. Infect. Immun. 71:6633-6640.
14. De Pina, K., V. Desjardin, M. A. Mandrand-Berthelot, G. Giordano, and L. F. Wu. 1999. Isolation and characterization of the nikR gene encoding a nickel-responsive regulator in Escherichia coli. J. Bacteriol. 181:670-674.
15. Ducey, T. F., and D. W. Dyer. 2002. Rapid identification of EZ::TN insertion sites in the genome of Neisseria gonorrhoeae. Epicentre Forum 9:6-7.
16. Elkins, C. 1995. Identification and purification of a conserved heme-regulated hemoglobin-binding outer membrane protein from Haemophilus ducreyi. Infect. Immun. 63:1241-1245.
17. Elkins, C., K. J. Morrow, Jr., and B. Olsen. 2000. Serum resistance in Haemophilus ducreyi requires outer membrane protein DsrA. Infect. Immun. 68:1608-1619.
18. Escolar, L., J. Perez-Martin, and V. de Lorenzo. 1999. Opening the iron box: transcriptional metalloregulation by the Fur protein. J. Bacteriol. 181:6223-6229.
19. Frisk, A., C. A. Ison, and T. Lagergard. 1998. GroEL heat shock protein of Haemophilus ducreyi: association with cell surface and capacity to bind to eukaryotic cells. Infect. Immun. 66:1252-1257.
20. Gibson, B. W., A. A. Campagnari, W. Melaugh, N. J. Phillips, M. A. Apicella, S. Grass, J. Wang, K. L. Palmer, and R. S. Munson, Jr. 1997. Characterization of a transposon Tn976-generated mutant of Haemophilus ducreyi 35000 defective in lipooligosaccharide biosynthesis. J. Bacteriol. 179:5062-5071.
21. Gibson, B. W., W. Melaugh, N. J. Phillips, M. A. Apicella, A. A. Campagnari, and J. M. Griffiss. 1993. Investigation of the structural heterogeneity of lipooligosaccharides from pathogenic Haemophilus and Neisseria species and of R-type lipopolysaccharides from Salmonella typhimurium by electrospray mass spectrometry. J. Bacteriol. 175:2702-2712.
22. Goon, S., B. Schilling, M. V. Tullius, B. W. Gibson, and C. R. Bertozzi. 2003. Metabolic incorporation of unnatural sialic acids into Haemophilus ducreyi lipooligosaccharides. Proc. Natl. Acad. Sci. USA 100:3089-3094.
23. Greiner, L. L., H. Watanabe, N. J. Phillips, J. Shao, A. Morgan, A. Zaleski, B. W. Gibson, and M. A. Apicella. 2004. Nontypeable Haemophilus influenzae strain 2019 produces a biofilm containing N-acetylneuraminic acid that may mimic sialylated O-linked glycans. Infect. Immun. 72:4249-4260.
24. Harvey, H. A., M. P. Jennings, C. A. Campbell, R. Williams, and M. A. Apicella. 2001. Receptor-mediated endocytosis of Neisseria gonorrhoeae into primary human urethral epithelial cells: the role of the asialoglycoprotein receptor. Mol. Microbiol. 42:659-672.
25. Harvey, H. A., N. Porat, C. A. Campbell, M. Jennings, B. W. Gibson, N. J. Phillips, M. A. Apicella, and M. S. Blake. 2000. Gonococcal lipooligosac-charide is a ligand for the asialoglycoprotein receptor on human sperm. Mol. Microbiol. 36:1059-1070.
26. Harvey, H. A., W. E. Swords, and M. A. Apicella. 2001. The mimicry of human glycolipids and glycosphingolipids by the lipooligosaccharides of pathogenic Neisseria and Haemophilus. J. Autoimmun. 16:257-262.
27. Inzana, T. J. 1983. Electrophoretic heterogeneity and interstrain variation of the lipopolysaccharide of Haemophilus influenzae. J. Infect. Dis. 148:492-499.
28. Jessamine, P. G., and A. R. Ronald. 1990. Chancroid and the role of genital ulcer disease in the spread of human retroviruses. Med. Clin. N. Am. 74:1417-1431.
29. Kahler, C. M., L. E. Martin, G. C. Shih, M. M. Rahman, R. W. Carlson, and D. S. Stephens. 1998. The (α2→8)-linked polysialic acid capsule and lipooligosaccharide structure both contribute to the ability of serogroup B Neisseria meningitidis to resist the bactericidal activity of normal human serum. Infect. Immun. 66:5939-5947.
30. Kalivoda, K. A., S. M. Steenbergen, E. R. Vimr, and J. Plumbridge. 2003. Regulation of sialic acid catabolism by the DNA binding protein NanR in Escherichia coli. J. Bacteriol. 185:4806-4815.
31. Koman, A., S. Harayama, and G. L. Hazelbauer. 1979. Relation of chemotactic response to the amount of receptor: evidence for different efficiencies of signal transduction. J. Bacteriol. 138:739-747.
32. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
33. Langford, P. R., and J. S. Kroll. 1997. Distribution, cloning, characterisation and mutagenesis of sodC, the gene encoding copper/zinc superoxide dismutase, a potential determinant of virulence, in Haemophilus ducreyi. FEMS Immunol. Med. Microbiol. 17:235-242.
34. Leduc, I., P. Richards, C. Davis, B. Schilling, and C. Elkins. 2004. A novel lectin, DltA, is required for expression of a full serum resistance phenotype in Haemophilus ducreyi. Infect. Immun. 72:3418-3428.
35. Mandrell, R. E., J. M. Griffiss, and B. A. Macher. 1988. Lipooligosaccharides (LOS) of Neisseria gonorrhoeae and Neisseria meningitidis have components that are immunochemically similar to precursors of human blood group antigens. Carbohydrate sequence specificity of the mouse monoclonal antibodies that recognize crossreacting antigens on LOS and human erythrocytes. J. Exp. Med. 168:107-126.
36. Mandrell, R. E., R. McLaughlin, Y. Aba Kwaik, A. Lesse, R. Yamasaki, B. Gibson, S. M. Spinola, and M. A. Apicella. 1992. Lipooligosaccharides (LOS) of some Haemophilus species mimic human glycosphingolipids, and some LOS are sialylated. Infect. Immun. 60:1322-1328.
37. Manson, M. D., W. Boos, P. J. Bassford, Jr., and B. A. Rasmussen. 1985. Dependence of maltose transport and chemotaxis on the amount of maltose-binding protein. J. Biol. Chem. 260:9727-9733.
38. Martinez, J., S. Steenbergen, and E. Vimr. 1995. Derived structure of the putative sialic acid transporter from Escherichia coli predicts a novel sugar permease domain. J. Bacteriol. 177:6005-6010.
39. Melaugh, W., A. A. Campagnari, and B. W. Gibson. 1996. The lipooligosaccharides of Haemophilus ducreyi are highly sialylated. J. Bacteriol. 178:564-570.
40. Melaugh, W., N. J. Phillips, A. A. Campagnari, M. V. Tullius, and B. W. Gibson. 1994. Structure of the major oligosaccharide from the lipooligosaccharide of Haemophilus ducreyi strain 35000 and evidence for additional glycoforms. Biochemistry 33:13070-13078.
41. Pacello, F., P. R. Langford, J. S. Kroll, C. Indiani, G. Smulevich, A. Desideri, G. Rotilio, and A. Battistoni. 2001. A novel heme protein, the Cu,Zn-superoxide dismutase from Haemophilus ducreyi. J. Biol. Chem. 276:30326-30334.
42. Palmer, K. L., W. E. Goldman, and R. S. Munson, Jr. 1996. An isogenic haemolysin-deficient mutant of Haemophilus ducreyi lacks the ability to produce cytopathic effects on human foreskin fibroblasts. Mol. Microbiol. 21:13-19.
43. Parsons, N. J., J. A. Cole, and H. Smith. 1990. Resistance to human serum of gonococci in urethral exudates is reduced by neuraminidase. Proc. R. Soc. Lond. B Biol. Sci. 241:3-5.
44. Phillips, N. J., C. M. John, L. G. Reinders, B. W. Gibson, M. A. Apicella, and J. M. Griffiss. 1990. Structural models for the cell surface lipooligosaccharides of Neisseria gonorrhoeae and Haemophilus influenzae. Biomed. Environ. Mass Spectrom. 19:731-745.
45. Plumbridge, J., and E. Vimr. 1999. Convergent pathways for utilization of the amino sugars N-acetylglucosamine, N-acetylmannosamine, and N-acetylneuraminic acid by Escherichia coli. J. Bacteriol. 181:47-54.
46. Post, D. M., R. Mungur, B. W. Gibson, and R. S. Munson, Jr. Unpublished data.
47. Preston, A., R. E. Mandrell, B. W. Gibson, and M. A. Apicella. 1996. The lipooligosaccharides of pathogenic gram-negative bacteria. Crit. Rev. Microbiol. 22:139-180.
48. Ringenberg, M. A., S. M. Steenbergen, and E. R. Vimr. 2003. The first committed step in the biosynthesis of sialic acid by Escherichia coli K1 does not involve a phosphorylated N-acetylmannosamine intermediate. Mol. Microbiol. 50:961-975.
49. San Mateo, L. R., M. M. Hobbs, and T. H. Kawula. 1998. Periplasmic copper-zinc superoxide dismutase protects Haemophilus ducreyi from exogenous superoxide. Mol. Microbiol. 27:391-404.
50. 13C-labeled N-acetylneuraminic acid. Biochemistry 40:12666-12677.
51. Schweda, E. K., J. A. Jonasson, and P. E. Jansson. 1995. Structural studies of lipooligosaccharides from Haemophilus ducreyi ITM 5535, ITM 3147, and a fresh clinical isolate, ACY1: evidence for intrastrain heterogeneity with the production of mutually exclusive sialylated or elongated glycoforms. J. Bacteriol. 177:5316-5321.
52. Schweda, E. K., A. C. Sundstrom, L. M. Eriksson, J. A. Jonasson, and A. A. Lindberg. 1994. Structural studies of the cell envelope lipopolysaccharides from Haemophilus ducreyi strains ITM 2665 and ITM 4747. J. Biol. Chem. 269:12040-12048.
53. Spinola, S. M., A. Orazi, J. N. Arno, K. Fortney, P. Kotylo, C. Y. Chen, A. A. Campagnari, and A. F. Hood. 1996. Haemophilus ducreyi elicits a cutaneous infiltrate of CD4 cells during experimental human infection. J. Infect. Dis. 173:394-402.
54. Steen, R. 2001. Eradicating chancroid. Bull. W. H. O. 79:818-826.
55. Steenbergen, S. M., C. A. Lichtensteiger, R. Caughlan, J. Garfinkle, T. E. Fuller, and E. R. Vimr. 2005. Sialic acid metabolism and systemic pasteurellosis. Infect. Immun. 73:1284-1294.
56. Stevens, M. K., S. Porcella, J. Klesney-Tait, S. Lumbley, S. E. Thomas, M. V. Norgard, J. D. Radolf, and E. J. Hansen. 1996. A hemoglobin-binding outer membrane protein is involved in virulence expression by Haemophilus ducreyi in an animal model. Infect. Immun. 64:1724-1735.
57. Sun, S., N. K. Scheffler, B. W. Gibson, J. Wang, and R. S. Munson, Jr. 2002. Identification and characterization of the N-acetylglucosamine glycosyltransferase gene of Haemophilus ducreyi. Infect. Immun. 70:5887-5892.
58. Swords, W. E., B. A. Buscher, K. Ver Steeg II, A. Preston, W. A. Nichols, J. N. Weiser, B. W. Gibson, and M. A. Apicella. 2000. Non-typeable Haemophilus influenzae adhere to and invade human bronchial epithelial cells via an interaction of lipooligosaccharide with the PAF receptor. Mol. Microbiol. 37:13-27.
59. Swords, W. E., M. R. Ketterer, J. Shao, C. A. Campbell, J. N. Weiser, and M. A. Apicella. 2001. Binding of the non-typeable Haemophilus influenzae lipooligosaccharide to the PAF receptor initiates host cell signalling. Cell. Microbiol. 3:525-536.
60. Swords, W. E., M. L. Moore, L. Godzicki, G. Bukofzer, M. J. Mitten, and J. VonCannon. 2004. Sialylation of lipooligosaccharides promotes biofilm formation by nontypeable Haemophilus influenzae. Infect. Immun. 72:106-113.
61. Telzak, E. E., M. A. Chiasson, P. J. Bevier, R. L. Stoneburner, K. G. Castro, and H. W. Jaffe. 1993. HIV-1 seroconversion in patients with and without genital ulcer disease. A prospective study. Ann. Intern. Med. 119:1181-1186.
62. Trees, D. L., and S. A. Morse. 1995. Chancroid and Haemophilus ducreyi: an update. Clin. Microbiol. Rev. 8:357-375.
63. Tsai, C. M. 2001. Molecular mimicry of host structures by lipooligosaccharides of Neisseria meningitidis: characterization of sialylated and nonsialylated lacto-N-neotetraose (Galβ1-4GlcNAcβ1-3Galβ1- 4Glc) structures in lipooligosaccharides using monoclonal antibodies and specific lectins. Adv. Exp. Med. Biol. 491:525-542.
64. Tsai, C. M., and C. E. Frasch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
65. Unkmeir, A., U. Kammerer, A. Stade, C. Hubner, S. Haller, A. Kolb-Maurer, M. Frosch, and G. Dietrich. 2002. Lipooligosaccharide and polysaccharide capsule: virulence factors of Neisseria meningitidis that determine meningococcal interaction with human dendritic cells. Infect. Immun. 70:2454-2462.
66. Vimr, E., C. Lichtensteiger, and S. Steenbergen. 2000. Sialic acid metabolism's dual function in Haemophilus influenzae. Mol. Microbiol. 36:1113-1123.
67. Vimr, E. R., K. A. Kalivoda, E. L. Deszo, and S. M. Steenbergen. 2004. Diversity of microbial sialic acid metabolism. Microbiol. Mol. Biol. Rev. 68:132-153.
68. Vimr, E. R., and F. A. Troy. 1985. Identification of an inducible catabolic system for sialic acids (nan) in Escherichia coli. J. Bacteriol. 164:845-853.
69. Vimr, E. R., and F. A. Troy. 1985. Regulation of sialic acid metabolism in Escherichia coli: role of N-acylneuraminate pyruvate-lyase. J. Bacteriol. 164:854-860.
70. Vogel, U., A. Weinberger, R. Frank, A. Muller, J. Kohl, J. P. Atkinson, and M. Frosch. 1997. Complement factor C3 deposition and serum resistance in isogenic capsule and lipooligosaccharide sialic acid mutants of serogroup B Neisseria meningitidis. Infect. Immun. 65:4022-4029.
71. Wood, G. E., S. M. Dutro, and P. A. Totten. 1999. Target cell range of Haemophilus ducreyi hemolysin and its involvement in invasion of human epithelial cells. Infect. Immun. 67:3740-3749.