The role of pilin glycan in neisserial pathogenesis

Molecular and Cellular Biochemistry

Volumn 253, Issue 1-2, 2003, Pages 179-190

  Banerjee, Asesh ^a   Ghosh, Salil K ^a  

^a CATHOLIC UNIVERSITY OF AMERICA   (United States)

Author keywords

DGI; Glycosyl transferase; Glycosylation; Gonorrhea; Meningitis; Neisseria; Phase variation; Pilin glycan; Pilus; Poly G tract

Indexed keywords

DNA; GLYCAN; GLYCOPROTEIN; GLYCOSYLTRANSFERASE; PILIN;

ALLELE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIUM ISOLATION; BACTERIUM PILUS; COMPLEX FORMATION; DNA POLYMORPHISM; GENE EXPRESSION; GENE TRANSFER; GONORRHEA; NEISSERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENESIS; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; REVIEW; SPECIES DIFFERENCE;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL ADHESION; EPITHELIAL CELLS; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GLYCOSYLATION; HUMANS; MOLECULAR SEQUENCE DATA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; POLYSACCHARIDES;

ANIMALIA; BACTERIA (MICROORGANISMS); NEGIBACTERIA; NEISSERIA; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS;

EID: 0142150237     PISSN: 03008177     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1026058311857     Document Type: Review

References (64)

1. Meitzner TA, Cohen MS: Vaccines against gonococcal infection. In: M.M. Levin, G.C. Woodrow, J.B. Kaper, G.S. Cobon (eds). New Generation Vaccines. Marcel Dekker, New York, 1997, pp 817-842
2. World Health Organization: Sexually Transmitted Diseases (STDs) - WHO Information Fact Sheet, World Health Organization, Geneva, Switzerland, 1996
3. Morse SA: Neisseria, Moraxella, Kingella and Eikenella. In: S. Baron (ed). Medical Microbiology. UTMB Press, Galveston, 1996, pp 217-231 (www.gsbs.utmb.edu/microbook/ch014.htm)
4. Virji M: Glycosylation of the meningococcus pilus protein. ASM News 64: 398-405, 1998
5. World Health Organization: Meningococcal disease: Public health burden and control. WHO Information Fact Sheet, World Health Organization, Geneva, Switzerland, 2002
6. Evans BA: Ultrastructural study of cervical gonorrhea. J Infect Dis 136: 248-255, 1977
7. Hultgren SJ, Abraham S, Caparon M, Falk P, St. Geme, JW III, Normark S: Pilus and nonpilus bacterial adhesins: Assembly and function in cell recognition. Cell 73: 887-901, 1993
8. Gubish ER Jr, Chen KC, Buchanan TM: Attachment of gonococcal pili to lectin-resistant clones of Chinese hamster ovary cells. Infect Immun 37: 189-194, 1982
9. Stephens DS, McGee ZA: Attachment of Neisseria meningitidis to human mucosal surfaces: Influence of pili and type of receptor cell. J Infect Dis 143: 525-532, 1981
10. Winther-Larsen HC, Hegge FT, Wolfgang M, Hayes SF, van Putten JP, Koomey M: Neisseria gonorrhoeae PilV, a type IV pilus-associated protein essential to human epithelial cell adherence. Proc Natl Acad Sci USA 98: 15276-15281, 2001
11. Scheuerpflug I, Rudel T, Ryll R, Pandit J, Meyer TF: Roles of PilC and PilE proteins in pilus-mediated adherence of Neisseria gonorrhoeae and Neisseria meningitidis to human erythrocytes and endothelial and epithelial cells. Infect Immun 67: 834-843, 1999
12. Virji M, Alexandrescu C, Ferguson DJ, Saunders JR, Moxon ER: Variations in the expression of pili: The effect on adherence of Neisseria meningitidis to human epithelial and endothelial cells. Mol Microbiol 6: 1271-1279, 1992
13. McGee ZA, Johnson AP, Taylor-Robinson D: Pathogenic mechanisms of Neisseria gonorrhoeae: Observations on damage to human fallopian tubes in organ culture by gonococci of colony type 1 or type 4. J Infect Dis 143: 413-421, 1981
14. Swanson JL, Robbins K, Barrera O, Corwin D, Boslego J, Ciak J, Blake MS, Koomey JM: Gonococcal pilin variants in experimental gonorrhea. J Exp Med 165: 1344-1357, 1987
15. Seifert HS: Questions about gonococcal pilus phase- and antigenic variation. Mol Microbiol 21: 433-440, 1996
16. Hagblom P, Segal E, Billyard E, So M: Intragenic recombination leads to pilus antigenic variation in Neisseria gonorrhoeae. Nature 315: 156-158, 1985
17. Haas R, Meyer TF: The repertoire of silent pilus genes in Neisseria gonorrhoeae: Evidence for gene conversion. Cell 44: 107-115, 1986
18. Segal E, Hagblom P, Seifert HS, So M: Antigenic variation of gonococcal pilus involves assembly of separated silent gene segments. Proc Natl Acad Sci USA 83: 2177-2181, 1986
19. Koomey M, Gotschlich EC, Robbins K, Bergstrom S, Swanson JL: Effects of recA mutations on pilus antigenic variation and phase transitions in Neisseria gonorrhoeae. Genetics 117: 391-398, 1987
20. Jonsson AB, Ilver D, Falk P, Pepose J, Normark S: Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue. Mol Microbiol 13: 403-416, 1994
21. Swanson J, Bergstrom S, Barrera O, Robbins K, Corwin D: Pilus-gonococcal variants. Evidence for multiple forms of piliation control. J Exp Med 162: 729-744, 1985
22. Jonsson A-B, Nyberg G, Normark S: Phase variation of gonococcal pili by frameshift mutation in pilC, a novel gene for pilus assembly. EMBO J 10: 477-488, 1991
23. Messner P, Sleytr UB: Bacterial surface layer glycoproteins. Glycobiology 1: 545-551, 1991
24. Benz I, Schimdt AM: Never say never again: protein glycosylation in pathogenic bacteria. Mol Microbiol 45: 267-276, 2002
25. Chia JS, Chang LY, Shun CT, Chang YY, Tsay YG, Chen JY: A 60-kilodalton immunodominant glycoprotein is essential for cell wall integrity and the maintenance of cell shape in Streptococcus mutans. Infect Immun 69: 6987-6998, 2001
26. Robertson JN, Vincent P, Ward ME: The preparation and properties of gonococcal pili. J Gen Microbiol 102: 169-177, 1977
27. Schoolnik GK, Fernandez R, Tai JY, Rothbard J, Gotschlich EC: Gonococcal Pili: Primary structure and receptor binding domain. J Exp Med 159: 1351-1370, 1984
28. Hardy MR: Methods for the analysis of glycoprotein carbohydrates. ABRF News 5: 12-19, 1994 (www.abrf.org/ABRFNews/1994/April1994/apr94methods.html)
29. Parge HE, Forest KT, Hickey MJ, Christensen DA, Getzoff ED, Tainer JA: Structure of the fibre-forming protein pilin at 2.6 A resolution. Nature 378: 32-38, 1995
30. Virji M: Post-translational modifications of meningococcal pili. Identification of common substituents: Glycans and alpha-glycerophosphate - a review. Gene 192: 141-147, 1997
31. Virji M, Saunders JR, Sims G, Makepeace K, Maskell D, Ferguson DJ: Pilus-facilitated adherence of Neisseria meningitidis to human epithelial and endothelial cells: Modulation of adherence phenotype occurs concurrently with changes in primary amino acid sequence and the glycosylation status of pilin. Mol Microbiol 10: 1013-1028, 1993
32. Stimson E, Virji M, Makepeace K, Dell A, Morris HR, Payne G, Saunders JR, Jennings MP, Barker S, Panico M: Meningococcal pilin: A glycoprotein substituted with digalactosyl 2,4-diacetamido-2,4,6-trideoxyhexose. Mol Microbiol 17: 1201-1214, 1995
33. Marceau M, Forest K, Beretti JL, Tainer J, Nassif X: Consequences of the loss of O-linked glycosylation of meningococcal type IV pilin on piliation and pilus-mediated adhesion. Mol Microbiol 27: 705-715, 1998
34. Hamadeh RM, Estabrook MM, Zhou P, Jarvis GA, Griffiss JM: Anti-Gal binds to pili of Neisseria meningitidis: the immunoglobulin A isotype blocks complement-mediated killing. Infect Immun 63: 4900-4906, 1995
35. Aho EL: Characterization of a class II pilin expression locus from Neisseria meningitidis: Evidence for increased diversity among pilin genes in pathogenic Neisseria species. Infect Immun 65: 2613-2620, 2002
36. Kahler CM, Martin LE, Tzeng YL, Miller YK, Sharkey K, Stephens DS, Davies JK: Polymorphisms in pilin glycosylation locus of Neisseria meningitidis expressing class II pili. Infect Immun 69: 3597-3604, 2001
37. Marceau M, Nassif X: Role of glycosylation at Ser63 in production of soluble pilin in pathogenic Neisseria. J Bacteriol 181: 656-661, 1999
38. Meyer TF, Gibbs CP, Haas R: Variation and control of protein expression in Neisseria. Annu Rev Microbiol 44: 451-477, 1990
39. Jennings MP, Virji M, Evans D, Foster V, Srikhanta YN, Steeghs L, van der LP, Moxon ER: Identification of a novel gene involved in pilin glycosylation in Neisseria meningitidis. Mol Microbiol 29: 975-984, 1998
40. Jennings MP, Hood DW, Peak IRA, Virji M, Moxon ER: Molecular analysis of a locus for the biosynthesis and phase-variable expression of the lacto-N-neotetraose terminal lipopolysaccharide structure in Neisseria meningitidis. Mol Microbiol 18: 729-740, 1995
41. Gotschlich EC: Genetic locus for the biosynthesis of the variable portion of Neisseria gonorrhoeae LOS. J Exp Med 180: 2181-2190, 1994
42. Banerjee A, Wang R, Uljon SN, Rice PA, Gotschlich EC, Stein DC: Identification of the gene (lgtG) encoding the lipooligosaccharide beta chain synthesizing glucosyl transferase from Neisseria gonorrhoeae. Proc Natl Acad Sci USA 95: 10872-10877, 1998
43. Hammerschmidt S, Muller A, Sillmann H, Muhlenhoff M, Borrow R, Fox A, van Putten J, Zollinger WD, Gerardy-Schahn R, Frosch M: Capsule phase variation in Neisseria meningitidis serogroup B by slipped-strand mispairing in the polysialyltransferase gene (siaD): Correlation with bacterial invasion and the outbreak of meningococcal disease. Mol Microbiol 20: 1211-1220, 1996
44. Sarkari J, Pandit N, Moxon ER, Achtman M: Variable expression of the Opc outer membrane protein in Neisseria meningitidis is caused by size variation of a promoter containing poly-cytidine. Mol Microbiol 13: 207-217, 1994
45. Vander EA, Hopman CT, Zaat S, Essink BB, Berkhout B, Dankert J: Variable expression of class 1 outer membrane protein in Neisseria meningitidis is caused by variation in the spacing between the -10 and - 35 regions of the promoter. J Bacteriol 177: 2475-2480, 1995
46. Power PM, Roddam LF, Dieckelmann M, Srikhanta YN, Tan YC, Berrington AW, Jennings MP: Genetic characterization of pilin glycosylation in Neisseria meningitidis. Microbiology 146: 967-979, 2000
47. Banerjee A, Wang R, Supernavage SL, Ghosh SK, Parker J, Ganesh NF, Wang PG, Gulati S, Rice PA: Implications of phase variation of a gene (pgtA) encoding a pilin galactosyl transferase in gonococcal pathogenesis. J Exp Med 196: 147-162, 2002
48. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ: Basic local alignment search tool. J Mol Biol 215: 403-410, 1990
49. Gohmann S, Manning PA, Alpert CA, Walker MJ, Timmis KN: Lipopolysaccharide O-antigen biosynthesis in Shigella dysenteriae serotype 1: Analysis of the plasmid-carried rfp determinant. Microb Pathog 16: 53-64, 1994
50. Hardy MR, Townsend RR: High-pH anion-exchange chromatography of glycoprotein-derived carbohydrates. Meth Enzymol: 208-225, 1994
51. Saunders NJ, Jeffries AC, Peden JF, Hood DW, Tettelin H, Rappuoli R, Moxon ER: Repeat-associated phase variable genes in the complete genome sequence of Neisseria meningitidis strain MC58. Mol Microbiol 37: 207-215, 2000
52. Galili U, Shohet SB, Kobrin E, Stults CL, Macher BA: Man, apes, and Old World monkeys differ from other mammals in the expression of alpha-galactosyl epitopes on nucleated cells. J Biol Chem 263: 17755-17762, 1988
53. Minor S, Gotschlich EC: The genetics of LPS synthesis by the gonococcus. In: J.B. Goldberg (ed). Genetics of Bacterial Polysaccharides. CRS Press, Florida, 1999, pp 111-131
54. Knapp JS, Holmes KK: Disseminated gonococcal infections caused by Neisseria gonorrhoeae with unique nutritional requirements. J Infect Dis 132: 204-208, 1975
55. Cannon JG, Buchanan TM, Sparling PF: Confirmation of association of protein I serotype of Neisseria gonorrhoeae with ability to cause disseminated infection. Infect Immun 40: 816-819, 1983
56. Dillard JP, Seifert HS: A variable genetic island specific for Neisseria gonorrhoeae is involved in providing DNA for natural transformation and is found more often in disseminated infection isolates. Mol Microbiol 41: 263-277, 2001
57. Burrman ET, Westwater C, Hube B, Brown AJP, Odds FC, Gow NAR: Molecular analysis of CaMnt1p, a mannosyl transferase important for adhesion and virulence of Candida albicans. Proc Natl Acad Sci USA 95: 7670-7675, 1998
58. Imperiali B, Shannon KL, Rickert KW: Role of peptide conformation in asparagine-linked glycosylation. J Am Chem Soc 114: 7942-7944, 1992
59. Sun WY, Xiong J, Shulman MJ: Substitution of asparagine for serine-406 of the immunoglobulin mu heavy chain alters glycosylation at asparagine-402. Biochem Biophys Res Commun 179: 1627-1634, 1991
60. Bisaria VS, Mishra S: Regulatory aspects of cellulase biosynthesis and secretion. Crit Rev Biotechnol 9: 61-103, 1989
61. Molecular Glycobiology: Frontiers in Molecular Biology. Oxford University Press, 1994
62. Moxon ER, Rainey PB, Nowak MA, Lenski RE: Adaptive evolution of highly mutable loci in pathogenic bacteria. Curr Biol 4: 24-33, 1994
63. Power PM, Roddam LF, Warren MJ, Dieckelmann M, Srikanta Y, Apicella MA, Jennings MP: The genetics of glycosylation in Neisseria meningitidis. Thirteenth International Pathogenic confererence, Norwegian Institute of Public Health, Oslo, September 1-6, 2002
64. Power PM, Jennings MP: The genetics of glycosylation in gram-negative bacteria. FEMS Microbiol Lett 218: 211-222, 2003