Identification of genes involved in the expression of atypical lipooligosaccharide structures from a second class of Haemophilus ducreyi

Infection and Immunity

Volumn 75, Issue 1, 2007, Pages 113-121

  Post, Deborah M B ^a   Munson Jr , Robert S ^b   Baker, Beth ^b   Zhong, Huachun ^b   Bozue, Joel A ^b,d   Gibson, Bradford W ^a,c  

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

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNITED STATES ARMY MEDICAL RESEARCH INSTITUTE OF INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXODEOXYRIBONUCLEASE III; GALACTOSYLTRANSFERASE; GLYCOSYLTRANSFERASE; HEPTOSE; LIPOOLIGOSACCHARIDE; RIBOSOME PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; DOT HYBRIDIZATION; GENE CLUSTER; GENE EXPRESSION; GENE IDENTIFICATION; GENE SEQUENCE; HAEMOPHILUS DUCREYI; HOUSEKEEPING GENE; LBGA GENE; LBGB GENE; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; RPME GENE; ULCUS MOLLE; XTHA GENE;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CLONING, MOLECULAR; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; GLYCOSYLTRANSFERASES; HAEMOPHILUS DUCREYI; IMMUNOBLOTTING; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; N-ACETYLLACTOSAMINE SYNTHASE; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 33846022736     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.01016-06     Document Type: Article

References (46)

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., 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.
3. Bauer, B. A., S. R. Lumbley, and E. J. Hansen. 1999. Characterization of a WaaF (RfaF) homolog expressed by Haemophilus ducreyi. Infect. Immun. 67:899-907.
4. Bauer, B. A., M. K. Stevens, and E. J. Hansen. 1998. Involvement of the Haemophilus ducreyi gmhA gene product in lipooligosaccharide expression and virulence. Infect. Immun. 66:4290-4298.
5. 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.
6. 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.
7. 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.
8. 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.
9. Dixon, L. G., W. L. Albritton, and P. J. Willson. 1994. An analysis of the complete nucleotide sequence of the Haemophilus ducreyi broad-host-range plasmid pLS88. Plasmid 32:228-232.
10. Dutro, S. M., G. E. Wood, and P. A. Totten. 1999. Prevalence of, antibody response to, and immunity induced by Haemophilus ducreyi hemolysin. Infect. Immun. 67:3317-3328.
11. Elkins, C. 1995. Identification and purification of a conserved heme-regulated hemoglobin-binding outer membrane protein from Haemophilus ducreyi. Infect. Immun. 63:1241-1245.
12. 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.
13. Filiatrault, M. J., B. W. Gibson, B. Schilling, S. Sun, R. S. Munson, Jr., and A. A. Campagnari. 2000. Construction and characterization of Haemophilus ducreyi lipooligosaccharide (LOS) mutants defective in expression of heptosyltransferase III and β1,4-glucosyltransferase: identification of LOS glycoforms containing lactosamine repeats. Infect. Immun. 68:3352-3361.
14. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. F. Tomb, B. A. Dougherty, J. M. Merrick, et al. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496-512.
15. 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 Tn916-generated mutant of Haemophilus ducreyi 35000 defective in lipooligosaccharide biosynthesis. J. Bacteriol. 179:5062-5071.
16. 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.
17. Hansen, E. J., J. L. Latimer, S. E. Thomas, M. Helminen, W. L. Albritton, and J. D. Radolf. 1992. Use of electroporation to construct isogenic mutants of Haemophilus ducreyi. J. Bacteriol. 174:5442-5449.
18. Inzana, T. J. 1983. Electrophoretic heterogeneity and interstrain variation of the lipopolysaccharide of Haemophilus influenzae. J. Infect. Dis. 148:492-499.
19. Inzana, T. J., J. Hensley, J. McQuiston, A. J. Lesse, A. A. Campagnari, S. M. Boyle, and M. A. Apicella. 1997. Phase variation and conservation of lipooligosaccharide epitopes in Haemophilus somnus. Infect. Immun. 65:4675-4681.
20. Jarosik, G. P., and E. J. Hansen. 1994. Identification of a new locus involved in expression of Haemophilus influenzae type b lipooligosaccharide. Infect. Immun. 62:4861-4867.
21. 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.
22. Jones, P. A., N. M. Samuels, N. J. Phillips, R. S. Munson, Jr., J. A. Bozue, J. A. Arseneau, W. A. Nichols, A. Zaleski, B. W. Gibson, and M. A. Apicella. 2002. Haemophilus influenzae type b strain A2 has multiple sialyltransferases involved in lipooligosaccharide sialylation. J. Biol. Chem. 277:14598-14611.
23. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
24. Leduc, L., 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.
25. Melaugh, W., A. A. Campagnari, and B. W. Gibson. 1996. The lipooligosaccharides of Haemophilus ducreyi are highly sialylated. J. Bacteriol. 178:564-570.
26. Melaugh, W., N. J. Phillips, A. A. Campagnari, R. Karalus, and B. W. Gibson. 1992. Partial characterization of the major lipooligosaccharide from a strain of Haemophilus ducreyi, the causative agent of chancroid, a genital ulcer disease. J. Biol. Chem. 267:13434-13439.
27. 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.
28. 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.
29. 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.
30. Pierson, V. L., and G. J. Barcak. 1999. Development of Escherichia coli host strains tolerating unstable DNA sequences on ColE1 vectors. Focus 21: 18-19.
31. Scheffler, N. K., A. M. Falick, S. C. Hall, W. C. Ray, D. M. Post, R. S. Munson, Jr., and B. W. Gibson. 2003. Proteome of Haemophilus ducreyi by 2-D SDS-PAGE and mass spectrometry: strain variation, virulence, and carbohydrate expression. J. Proteome Res. 2:523-533.
32. 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.
33. 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.
34. Steen, R. 2001. Eradicating chancroid. Bull. W. H. O. 79:818-826.
35. Stevens, M. K., J. Klesney-Tait, S. Lumbley, K. A. Walters, A. M. Joffe, J. D. Radolf, and E. J. Hansen. 1997. Identification of tandem genes involved in lipooligosaccharide expression by Haemophilus ducreyi. Infect. Immun. 65: 651-660.
36. 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.
37. 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.
38. Sun, S., B. Schilling, L. Tarantino, M. V. Tullius, B. W. Gibson, and R. S. Munson, Jr. 2000. Cloning and characterization of the lipooligosaccharide galactosyltransferase II gene of Haemophilus ducreyi. J. Bacteriol. 182:2292-2298.
39. 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 or without genital ulcer disease: a prospective study. Ann. Intern. Med. 119:1181-1186.
40. Trees, D. L., and S. A. Morse. 1995. Chancroid and Haemophilus ducreyi: an update. Clin. Microbiol. Rev. 8:357-375.
41. Tsai, C. M., and C. E. Frasch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
42. Tullius, M. V., N. J. Phillips, N. K. Scheffler, N. M. Samuels, R. S. Munson, Jr., E. J. Hansen, M. Stevens-Riley, A. A. Campagnari, and B. W. Gibson. 2002. The lbgAB gene cluster of Haemophilus ducreyi encodes a β-1,4-galactosyltransferase and an α-1,6-DD- heptosyltransferase involved in lipooligosaccharide biosynthesis. Infect. Immun. 70:2853-2861.
43. Wang, R. F., and S. R. Kushner. 1991. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 100:195-199.
44. White, C. D., I. Leduc, B. Olsen, C. Jeter, C. Harris, and C. Elkins. 2005. Haemophilus ducreyi Outer membrane determinants, including DsrA, define two clonal populations. Infect. Immun. 73:2387-2399.
45. 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.
46. Young, R. S., K. Fortney, J. C. Haley, A. F. Hood, A. A. Campagnari, J. Wang, J. A. Bozue, R. S. Munson, Jr., and S. M. Spinola. 1999. Expression of sialylated or paragloboside-like lipooligosaccharides are not required for pustule formation by Haemophilus ducreyi in human volunteers. Infect. Immun. 67:6335-6340.