Construction and characterization of Haemophilus ducreyi lipooligosaccharide (LOS) mutants defective in expression of heptosyltransferase III and β,4-glucosyltransferase: Identification of LOS glycoforms containing lactosamine repeats

Infection and Immunity

Volumn 68, Issue 6, 2000, Pages 3352-3361

  Filiatrault, Melanie J ^a,b   Gibson, Bradford W ^c   Schilling, Birgit ^c   Sun, Shuhua ^d   Munson Jr , Robert S ^d   Campagnari, Anthony A ^a,b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSYLTRANSFERASE; OLIGOSACCHARIDE;

AMINO ACID SEQUENCE; ARTICLE; CARBOHYDRATE SYNTHESIS; HAEMOPHILUS DUCREYI; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; ULCUS MOLLE;

AMINO SUGARS; BACTERIAL PROTEINS; CARBOHYDRATE SEQUENCE; CHANCROID; ESCHERICHIA COLI PROTEINS; GENETIC COMPLEMENTATION TEST; GLUCOSYLTRANSFERASES; GLYCOSYLTRANSFERASES; HAEMOPHILUS DUCREYI; HUMANS; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; MUTATION; PYOCINS; SELECTION (GENETICS); SEQUENCE ANALYSIS; SEQUENCE ANALYSIS, DNA; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION;

EID: 0034034899     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.68.6.3352-3361.2000     Document Type: Article

References (46)

1. Alfa, M. J., and P. DeGagne. 1997. Attachment of Haemophilus ducreyi to human foreskin fibroblasts involves LOS and fibronectin. Microb. Pathog. 22:39-46.
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. Apicella, M. A., J. M. Griffiss, and H. Schneider. 1994. Isolation and characterization of lipopolysaccharides, lipooligosaccharides, and lipid A. Methods Enzymol. 235:242-252.
4. 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.
5. 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.
6. Bozue, J. A., L. Tarantino, and R. S. Munson, Jr. 1998. Facile construction of mutations in Haemophilus ducreyi using lacZ as a counter-selectable marker. FEMS Microbiol. Lett. 164:269-273.
7. 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.
8. 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.
9. 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.
10. Campagnari, A. A., L. M. Wild, G. E. Griffiths, R. J. Karalus, M. A. Wirth, and S. M. Spinola. 1991. Role of lipooligosaccharides in experimental dermal lesions caused by Haemophilus ducreyi. Infect. Immun. 59:2601-2608.
11. Centers for Disease Control and Prevention. 1998. HIV prevention through early detection and treatment of other sexually transmitted diseases - United States. Recommendations of the Advisory Committee for HIV and STD prevention. Morbid. Mortal. Weekly Rep. 47:1-24.
12. 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 94:4056-61.
13. 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.
14. Dudas, K. C., and M. A. Apicella. 1988. Selection and immunochemical analysis of lipooligosaccharide mutants of Neisseria gonorrhoeae. Infect. Immun. 56:499-504.
15. Filip, C., G. Fletcher, J. L. Wulff, and C. F. Earhart. 1973. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent sodium-lauryl sarcosinate. J. Bacteriol. 115:717-722.
16. 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.
17. Gibson, B. W., J. J. Engstrom, C. M. John, W. Hines, and A. M. Falick. 1997. Characterization of bacterial lipooligosaccharides by delayed extraction matrix-assisted laser desorption ionization time-flight mass spectrometry. J. Am. Soc. Mass Spectrosc. 8:645-658.
18. 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.
19. Hammond, G. W., C. J. Lian, J. C. Wilt, and A. R. Ronald. 1978. Antimicrobial susceptibility of Haemophilus ducreyi. Antimicrob. Agents Chemother. 13:608-12.
20. Heinrichs, D. E., J. A. Yethon, and C. Whilfield. 1998. Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica. Mol. Microbiol. 30:221-232.
21. Helander, I. M., K. Nummila, I. Kilpelainen, and M. Vaara. 1995. Increased substitution of phosphate groups in lipooligosaccharides and lipid A of polymyxin-resistant mutants of Salmonella typhimurium and Escherichia coli. Prog. Clin. Biol. Res. 392:15-23.
22. Ison, C. A., J. A. Dillon, and J. W. Tapsall. 1998. The epidemiology of global antibiotic resistance among Neisseria gonorrhoeae and Haemophilus ducreyi. Lancet 351(Suppl. 3):8-11. (Erratum, 352:1316.)
23. Johnson, K. G., and M. B. Perry. 1976. Improved techniques for the preparation of bacterial lipopolysaccharides. Can. J. Microbiol. 22:29-34.
24. Kahler, C. M., R. W. Carlson, M. M. Rahman, L. E. Martin, and D. S. Stephens. 1996. Two glycosyltransferase genes, IgtF and rfaK, constitute the lipooligosaccharide ice (inner core extension) biosynthesis operon of Neisseria meningitidis. J. Bacteriol. 178:6677-6684.
25. Klesney-Tait, J., T. J. Hiltke, I. Maciver, S. M. Spinola, J. D. Radolf, and E. J. Hansen. 1997. The major outer membrane protein of Haemophilus ducreyi consists of two OmpA homologs. J. Bacteriol. 179:1764-1773.
26. Knecht, D. A., and R. L. Dimond. 1984. Visualization of antigenic proteins on Western blots. Anal. Biochem. 136:180-184.
27. Lee, F. K., K. C. Dudas, J. A. Hanson, M. B. Nelson, P. T. LoVerde, and M. A. Apicella. 1999. The R-type pyocin of Pseudomonas aeruginosa C is a bacteriophage tail-like particle that contains single-stranded DNA. Infect. Immun. 67:717-25.
28. Mandrell, R., H. Schneider, M. Apicella, W. Zollinger, P. A. Rice, and J. M. Griffiss. 1986. Antigenic and physical diversity of Neisseria gonorrhoeae lipooligosaccharides. Infect. Immun. 54:63-69.
29. 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.
30. Mohr, M. D., K. O. Bornsen, and H. M. Widmer. 1995. Matrix-assisted laser desorption ionization mass spectrometry - improved matrix for oligosaccharides. Rapid Commun. Mass Spectrom. 9:809-914.
31. Morse, S. A., P. Vaughan, D. Johnson, and B. H. Iglewski. 1976. Inhibition of Neisseria gonorrhoeae by a bacteriocin from Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 10:354-362.
32. 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 fibrobiasts. Mol. Microbiol. 21: 13-19.
33. Palmer, K. L., S. Grass, and R. S. Munson, Jr. 1994. Identification of a hemolytic activity elaborated by Haemophilus ducreyi. Infect. Immun. 62: 3041-3043.
34. Palmer, K. L., A. C. Thornton, K. R. Fortney, A. F. Hood, R. S. Munson, Jr., and S. M. Spinola. 1998. Evaluation of an isogenic hemolysin-deficient mutant in the human model of Haemophilus ducreyi infection. J. Infect. Dis. 178:191-199.
35. 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.
36. Russo, T. A., J. E. Guenther, S. Wenderoth, and M. M. Frank. 1993. Generation of isogenic K54 capsule-deficient Escherichia coli strains through TnphoA-mediated gene disruption. Mol. Microbiol. 9:357-364.
37. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
38. Spinola, S. M., A. Castellazzo, M. Shero, and M. A. Apicella. 1990. Characterization of pili expressed by Haemophilus ducreyi. Microb. Pathog. 9:417-426.
39. 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.
40. 39a. 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.
41. Trees, D. L., and S. A. Morse. 1995. Chancroid and Haemophilus ducreyi: an update. Clin. Microbiol. Rev. 8:357-375.
42. Tsai, C. M., and C. E. Frasch. 1982. A sensitive silver stain for detecting lipopolysaccharides in polyacrylamide gels. Anal. Biochem. 119:115-119.
43. Vestal, M. L., P. Juhasz, and S. A. Martin. 1995. Delayed extraction matrix-assisted laser desorption time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 9:1044-1050.
44. Westphal, O., and K. Jann. 1965. Bacterial lipopolysaccharide extraction with phenol-water and further application of the procedure. Methods Carbohydr. Chem. 5:83-91.
45. Yethon, J. A., D. E. Heinrichs, M. A. Monteiro, M. B. Perry, and C. Whitfield. 1998. Involvement of waaY, waaQ, and waaP in the modification of Escherichia coli lipopolysaccharide and their role in the formation of a stable outer membrane. J. Biol. Chem. 273:26310-26316.
46. Zaretzky, F. R., and T. H. Kawula. 1999. Examination of early interactions between Haemophilus ducreyi and host cells by using cocultured HaCaT keratinocytes and foreskin fibroblasts. Infect. Immun. 67:5352-5360.