The lytic transglycosylases of Neisseria gonorrhoeae

Microbial Drug Resistance

Volumn 18, Issue 3, 2012, Pages 271-279

  Chan, Yolande A ^a   Hackett, Kathleen T ^a   Dillard, Joseph P ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOLYSIN; BACTERIAL ENZYME; MONOMER; PEPTIDOGLYCAN; PEPTIDOGLYCAN GLYCOSYLTRANSFERASE;

AUTOLYSIS; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL GROWTH; CELL DEATH; CELL SEPARATION; CILIATED EPITHELIUM; ENZYME DEGRADATION; GENE TRANSFER; HUMAN; MUTAGENESIS; NEISSERIA GONORRHOEAE; NEISSERIA MENINGITIDIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; TYPE IV SECRETION SYSTEM; UTERINE TUBE;

BACTERIAL PROTEINS; CILIA; EPITHELIAL CELLS; FALLOPIAN TUBES; FEMALE; GLYCOSYLTRANSFERASES; GONORRHEA; HUMANS; ISOENZYMES; MUTAGENESIS; MUTATION; NEISSERIA GONORRHOEAE; PEPTIDE FRAGMENTS; PEPTIDOGLYCAN;

BACTERIA (MICROORGANISMS); NEISSERIA GONORRHOEAE;

EID: 84862026325     PISSN: 10766294     EISSN: 19318448     Source Type: Journal    
DOI: 10.1089/mdr.2012.0001     Document Type: Review

References (63)

1. Adu-Bobie, J., P. Lupetti, B. Brunelli, D. Granoff, N. Norais, G. Ferrari, G. Grandi, R. Rappuoli, and M. Pizza. 2004. GNA33 of Neisseria meningitidis is a lipoprotein required for cell separation, membrane architecture and virulence. Infect. Immun. 72:1914-1919.
2. Aral, S.O., W.D. Mosher, and W. Cates Jr. 1991. Self-eported Pelvic Inflammatory Disease in the United States, 1988. JAMA. 266:2570-2573.
3. Barry, P.M., and J.D. Klausner. 2009. The use of cephalosporins for gonorrhea: the impending problem of resistance. Expert. Opin. Pharmacother. 10:555-577.
4. Beachey, E.H., W. Keck, M.A.d. Pedro, and U. Schwarz. 1981. Exoenzymatic activity of transglycosylase isolated from Escherichia coli. Eur. J. Biochem. 116:355-358.
5. Bienkowska-Szewczyk, K., B. Lipinska, and A. Taylor. 1981. The R gene product of bacteriophage lambda is the murein transglycosylase. Mol. Gen. Genet. 184:111-114.
6. Blackburn, N.T., and A.J. Clarke. 2002. Characterization of soluble and membrane-bound family 3 lytic transglycosylases from Pseudomonas aeruginosa. Biochemistry 41:1001-1013.
7. Chaput, C., A. Labigne, and I.G. Boneca. 2007. Characterization of Helicobacter pylori lytic transglycosylases Slt and MltD. J. Bacteriol. 189:422-429.
8. Cloud, K.A., and J.P. Dillard. 2002. A lytic transglycosylase of Neisseria gonorrhoeae is involved in peptidoglycan-derived cytotoxin production. Infect. Immun. 70:2752-2757.
9. Cloud, K.A., and J.P. Dillard. 2004. Mutation of a single lytic transglycosylase causes aberrant septation and inhibits cell separation of Neisseria gonorrhoeae. J. Bacteriol. 186:7811-7814.
10. Cloud-Hansen, K.A., K.T. Hackett, D.L. Garcia, and J.P. Dillard. 2008. Neisseria gonorrhoeae uses two lytic transglycosylases to produce cytotoxic peptidoglycan monomers. J. Bacteriol. 190:5989-5994.
11. Dillard, J.P., and K.T. Hackett. 2005. Mutations affecting peptidoglycan acetylation in Neisseria gonorrhoeae and Neisseria meningitidis. Infect. Immun. 73:5697-5705.
12. Dillard, J.P., and H.S. Seifert. 1997. A peptidoglycan hydrolase similar to bacteriophage endolysins acts as an autolysin in Neisseria gonorrhoeae. Mol. Microbiol. 25:893-901.
13. Dillard, J.P., and H.S. Seifert. 2001. 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.
14. Dokter, W.H.A., A.J. Dijkstra, S.B. Koopmans, B.K. Stulp, W. Keck, M.R. Halie, and E. Vellenga. 1994. G(Anh)MTetra, a natural bacterial cell wall breakdown product induces interleukin-1beta and interleukin-6 expression in human monocytes. J. Biol. Chem. 269:4201-4206.
15. Engel, H., A.J. Smink, L. van Wijngaarden, and W. Keck. 1992. Murein-metabolizing enzymes from Escherichia coli: existence of a second lytic transglycosylase. J. Bacteriol. 174:6394-6403.
16. Fleming, T.J., D.E. Wallsmith, and R.S. Rosenthal. 1986. Arthropathic properties of gonococcal peptidoglycan fragments: implications for the pathogenesis of disseminated gonococcal disease. Infect. Immun. 52:600-608.
17. Garcia, D.L., and J.P. Dillard. 2006. AmiC functions as an N-acetylmuramyl-L-alanine amidase necessary for cell separation and can promote autolysis in Neisseria gonorrhoeae. J. Bacteriol. 188:7211-7221.
18. Garcia, D.L., and J.P. Dillard. 2008. Mutations in ampG or ampD affect peptidoglycan fragment release from Neisseria gonorrhoeae. J. Bacteriol. 190:3799-3807.
19. García, K.P., P.S. Rubilar, M.F. Vargas, H. Cárdenas, M.A. Rios, P.A. Orihuela, R.H. Vargas, J. Fuhrer, J.E. Heckels, M. Christodoulides, and L.A. Velásquez. 2010. Nitric oxide is not involved in Neisseria gonorrhoeae-induced cellular damage of human Fallopian tubes in vitro. Biol. Res. 43:39-50.
20. Girardin, S.E., I.G. Boneca, L.A. Carneiro, A. Antignac, M. Jéhanno, J. Viala, K. Tedin, M.K. Taha, A. Labigne, U. Zähringer, A.J. Coyle, P.S. DiStefano, J. Bertin, P.J. Sansonetti, and D.J. Philpott. 2003. Nod1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan. Science 300:1584-1587.
21. Goldman, W.E., D.G. Klapper, and J.B. Baseman. 1982. Detection, isolation, and analysis of a released Bordetella pertussis product toxic to cultured tracheal cells. Infect. Immun. 36:782-794.
22. Goodell, E.W. 1985. Recycling of murein by Escherichia coli. J. Bacteriol. 163:305-310.
23. Goodell, E.W., and U. Schwarz. 1985. Release of cell wall peptides into culture medium by exponentially growing Escherichia coli. J. Bacteriol. 162:391-397.
24. Granoff, D.M., G.R. Moe, M.M. Giuliani, J. Adu-Bobie, L. Santini, B. Brunelli, F. Piccinetti, P. Zuno-Mitchell, S.S. Lee, P. Neri, L. Bracci, L. Lozzi, and R. Rappuoli. 2001. A novel mimetic antigen eliciting protective antibody to Neisseria meningitidis. J. Immunol. 167:6487-6496.
25. Greenway, D.L., and H.R. Perkins. 1985. Turnover of the cell wall peptidoglycan during growth of Neisseria gonorrhoeae and Escherichia coli. Relative stability of newly synthesized material. J. Gen. Microbiol. 131:253-263.
26. Hamilton, H.L., N.M. Domínguez, K.J. Schwartz, K.T. Hackett, and J.P. Dillard. 2005. Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55:1704-1721.
27. Hamilton, H.L., K.J. Schwartz, and J.P. Dillard. 2001. Insertion-duplication mutagenesis of Neisseria: use in characterization of DNA transfer genes in the gonococcal genetic island. J. Bacteriol. 183:4718-4726.
28. Hebeler, B.H., and F.E. Young. 1975. Autolysis of Neisseria gonorrhoeae. J. Bacteriol. 122:385-392.
29. Heidrich, C., A. Ursinus, J. Berger, H. Schwarz, and J.-V. Höltje. 2002. Effects of multiple deletions of murein hydrolases on viability, septum cleavage, and sensitivity to large toxic molecules in Escherichia coli. J. Bacteriol. 184: 6093-6099.
30. Heiss, L.N., J.R. Lancaster, J.A. Corbett, and W.E. Goldman. 1994. Epithelial autotoxicity of nitric oxide: role in the respiratory cytopathoology of pertussis. Proc. Natl. Acad. Sci. U. S. A. 91:267-270.
31. Heiss, L.N., S.A. Moser, E.R. Unanue, and W.E. Goldman. 1993. Interleukin-1 is linked to the respiratory epithelial cytopathology of pertussis. Infect. Immun. 61:3123-3128.
32. Höltje, J.V. 1996. A hypothetical holoenzyme involved in the replication of the murein sacculus of Escherichia coli. Microbiology 142 (Pt 8):1911-1918.
33. Höltje, J.V. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62:181-203.
34. Kohler, P.L., K.A. Cloud, K.T. Hackett, E.T. Beck, and J.P. Dillard. 2005. Characterization of the role of LtgB, a putative lytic transglycosylase in Neisseria gonorrhoeae. Microbiology 151:3081-3088.
35. Kohler, P.L., H.L. Hamilton, K. Cloud-Hansen, and J.P. Dillard. 2007. AtlA functions as a peptidoglycan lytic transglycosylase in the Neisseria gonorrhoeae type IV secretion system. J. Bacteriol. 189:5421-5428.
36. Koraimann, G. 2003. Lytic transglycosylases in macromolecular transport systems of Gram-negative bacteria. Cell Mol. Life Sci. 60:2371-2388.
37. Magalhaes, J.G., D.J. Philpott, M.A. Nahori, M. Jehanno, J. Fritz, L. Le Bourhis, J. Viala, J.P. Hugot, M. Giovannini, J. Bertin, M. Lepoivre, D. Mengin-Lecreulx, P.J. Sansonetti, and S.E. Girardin. 2005. Murine Nod1 but not its human orthologue mediates innate immune detection of tracheal cytotoxin. EMBO Rep. 6:1201-1207.
38. Maisey, K., G. Nardocci, M. Imarai, H. Cardenas, M. Rios, H.B. Croxatto, J.E. Heckels, M. Christodoulides, and L.A. Velasquez. 2003. Expression of proinflammatory cytokines and receptors by human fallopian tubes in organ culture following challenge with Neisseria gonorrhoeae. Infect. Immun. 71:527-532.
39. McGee, Z.A., C.M. Clemens, R.L. Jensen, J.J. Klein, L.R. Barley, and G.L. Gorby. 1992. Local induction of tumor necrosis factor as a molecular mechanism of mucosal damage by gonococci. Microb. Pathog. 12:333-341.
40. Melly, M.A., Z.A. McGee, and R.S. Rosenthal. 1984. Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J. Infect. Dis. 149:378-386.
41. Nigro,G., L.L. Fazio,M.C.Martino, G. Rossi, I. Tattoli, V. Liparoti, C. De Castro, A. Molinaro, D.J. Philpott, and M.L. Bernardini. 2008. Muramylpeptide shedding modulates cell sensing of Shigella flexneri. Cell Microbiol. 10:682-695.
42. Ohnishi, M., D. Golparian, K. Shimuta, T. Saika, S. Hoshina, K. Iwasaku, S. Nakayama, J. Kitawaki, and M. Unemo. Is Neisseria gonorrhoeae initiating a future era of untreatable gonorrhea?: detailed characterization of the first strain with high-level resistance to ceftriaxone. Antimicrob. Agents Chemother. 55:3538-3545.
43. Pariser, H. 1972. Asymptomatic gonorrhea. Med. Clin. North Am. 56:1127-1132.
44. Park, J.T. 1995. Why does Escherichia coli recycle its cell wall peptides? Mol. Microbiol. 17:421-426.
45. Pizza, M., V. Scarlato, V. Masignani, M.M. Giulianl, B. Arlco, M. Comanducci, G.T. Jennings, L. Baldl, E. Bartolini, B. Capecchi, C.L. Galeotti, E. Luzzi, R. Manetti, E. Marchetti, M. Mora, S. Nutti, G. Ratti, L. Santini, S. Savino, M. Scarselli, E. Stornl, P. Zuo, M. Broeker, E. Hundt, B. Knapp, E. Blair, T. Manson, H. Tettelin, D.W. Hood, A.C. Jeffries, N.J. Saunders, D.M. Granoff, J.C. Venter, E.R. Moxon, G. Grandl, and R. Rappuoli. 2000. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 287:1816-1820.
46. Powell, A.J., Z.J. Liu, R.A. Nicholas, and C. Davies. 2006. Crystal structures of the lytic transglycosylase MltA from N. gonorrhoeae and E. coli: insights into interdomain movements and substrate binding. J. Mol. Biol. 359:122-136.
47. Rosenthal, R.S. 1979. Release of soluble peptidoglycan from growing gonococci: hexaminidase and amidase activities. Infect. Immun. 24:869-878.
48. Rosenthal, R.S., J.K. Blundell, and H.R. Perkins. 1982. Strain-related differences in lysozyme sensitivity and extent of O-acetylation of gonococcal peptidoglycan. Infect. Immun. 37:826-829.
49. Rosenthal, R.S., W.J. Folkening, D.R. Miller, and S.C. Swim. 1983. Resistance of O-acetylated gonococcal peptidoglycan to human peptidoglycan-degrading enzymes. Infect. Immun. 40:903-911.
50. Rosenthal, R.S., W. Nogami, B.T. Cookson, W.E. Goldman, and W.J. Folkening. 1987. Major fragment of soluble peptidoglycan released from growing Bordetella pertussis is tracheal cytotoxin. Infect. Immun. 55:2117-2120.
51. Salgado-Pabón, W., S. Jain, N. Turner, C. van der Does, and J.P. Dillard. 2007. A novel relaxase homologue is involved in chromosomal DNA processing for type IV secretion in Neisseria gonorrhoeae. Mol. Microbiol. 66:930-947.
52. Serruto, D., and C.L. Galeotti. 2004. The signal peptide sequence of a lytic transglycosylase of Neisseria meningitidis is involved in regulation of gene expression. Microbiology 150:1427-1437.
53. Sinha, R.K., and R.S. Rosenthal. 1980. Release of soluble peptidoglycan from growing gonococci: demonstration of anhydro-muramyl-containing fragments. Infect. Immun. 29:914-925.
54. Steinmoen, H., E. Knutsen, and L.S. Havarstein. 2002. Induction of natural competence in Streptococcus pneumoniae triggers lysis and DNA release from a subfraction of the cell population. Proc. Natl. Acad. Sci. U. S. A. 99:7681-7686.
55. Suvorov, M., M. Lee, D. Hesek, B. Boggess, and S. Mobashery. 2008. Lytic transglycosylase MltB of Escherichia coli and its role in recycling of peptidoglycan strands of bacterial cell wall. J. Am. Chem. Soc. 130:11878-11879.
56. Thunnissen, A.-M.W.H., A.J. Dijkstra, K.H. Kalk, H.J. Rozeboom, H. Engel, W. Keck, and B.W. Dijkstra. 1994. Doughnut-shaped structure of a bacterial muramidase revealed by X-ray crystallography. Nature 367:750-753.
57. Thunnissen, A.-M.W.H., H.J. Rozeboom, K.H. Kalk, and B.W. Dijkstra. 1995. Structure of the 70 kDa soluble lytic transglycosylase complexed with bulgecin A. Implications for the enzymatic mechanism. Biochemistry 34:12729-12737.
58. van Asselt, E.J., A.J. Dijkstra, K.H. Kalk, B. Takacs, W. Keck, and B.W. Dijkstra. 1999. Crystal structure of Escherichia coli lytic transglycosylase Slt35 reveals a lysozyme-like catalytic domain with an EF-hand. Structure 7:1167-1180.
59. van Asselt, E.J., and B.W. Dijkstra. 1999. Binding of calcium in the EF-hand of Escherichia coli lytic transglycosylase Slt35 is important for stability. FEBS Lett. 458:429-435.
60. van Asselt, E.J., K.H. Kalk, and B.W. Dijkstra. 2000. Crystallographic studies of the interactions of Escherichia coli lytic transglycosylase Slt35 with peptidoglycan. Biochemistry 39:1924-1934.
61. van Asselt, E.J., A.-M.W.H. Thunnissen, and B.W. Dijkstra. 1999. High resolution crystal structures of the Escherichia coli lytic translycosylase Slt70 and its complex with a peptidoglycan fragment. J. Mol. Biol. 291:877-898.
62. Weadge, J.T., and A.J. Clarke. 2006. Identification and characterization of O-acetylpeptidoglycan esterase: a novel enzyme discovered in Neisseria gonorrhoeae. Biochemistry 45:839-851.
63. WHO. 2011. Emergence of multi-drug resistant Neisseria gonorrhoeae-threat of global rise in untreatable sexually transmitted disease. Available at: whqlibdoc.who.int/hq/2011/WHO-RHR-11.14-eng.pdf (Online.) Accessed Oct 20, 2011.