Neisseria gonorrhoeae virulence factor NG1686 is a bifunctional M23B family metallopeptidase that influences resistance to hydrogen peroxide and colony morphology

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 11222-11233

  Stohl, Elizabeth A ^a   Chan, Yolande A ^b   Hackett, Kathleen T ^b   Kohler, Petra L ^b,c   Dillard, Joseph P ^b   Seifert, H Steven ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

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

^c 3M COMPANY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ACTIVE SITE RESIDUES; BACTERIAL CELLS; BIFUNCTIONAL; CELL MORPHOLOGY; CELL WALLS; COLONY MORPHOLOGY; DEGRADATIVE ACTIVITY; GONORRHOEAE; IN-VITRO; METALLOPEPTIDASES; MUTANT STRAIN; NEISSERIA GONORRHOEAE; NON-OXIDATIVE; OVER-EXPRESSION; PEPTIDOGLYCANS; POLYMORPHONUCLEAR LEUKOCYTES; VIRULENCE FACTORS;

CELL MEMBRANES; HYDROGEN PEROXIDE; PROTEINS;

POLYMORPHISM;

ANTIBIOTIC AGENT; CARBOXYPEPTIDASE TRANSPEPTIDASE; HYDROGEN PEROXIDE; PEPTIDOGLYCAN; PROTEIN NG1686; PROTEINASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CELL WALL; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; BACTERIUM COLONY; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; IN VITRO STUDY; MICROBIAL MORPHOLOGY; MINIMUM INHIBITORY CONCENTRATION; NEISSERIA GONORRHOEAE; NEUTROPHIL; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; SITE DIRECTED MUTAGENESIS; UPREGULATION;

ANTI-BACTERIAL AGENTS; CARBOXYPEPTIDASES; CATALYTIC DOMAIN; CONSERVED SEQUENCE; DRUG RESISTANCE, BACTERIAL; ENDOPEPTIDASES; ESCHERICHIA COLI; HYDROGEN PEROXIDE; METALLOPROTEASES; MUTATION; NEISSERIA GONORRHOEAE; NEUTROPHILS; PEPTIDOGLYCAN; PERIPLASM; PHENOTYPE; PROTEOLYSIS; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); NEISSERIA; NEISSERIA GONORRHOEAE;

EID: 84859498051     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.338830     Document Type: Article

References (57)

1. World Health Organization (2011) Emergence of multi-drug resistant Neisseria gonorrhoeae. Threat of global rise in untreatable sexually transmitted disease. in WHO/RHR/11.4 Department of Reproductive Health and Research, World Health Organization, Geneva
2. Hook, E. W., 3rd, and Holmes, K. K. (1985) Gonococcal infections. Ann. Int. Med. 102, 229-243
3. Edwards, J. L., and Apicella, M. A. (2004) The molecular mechanisms used by Neisseria gonorrhoeae to initiate infection differ between men and women. Clin. Microbiol. Rev. 17, 965-981 (Pubitemid 39372526)
4. Dokter, W. H., Dijkstra, A. J., Koopmans, S. B., Stulp, B. K., Keck, W., Halie, M. R., and Vellenga, E. (1994) G(Anh)MTetra, a natural bacterial cell wall breakdown product, induces interleukin-1 β and interleukin-6 expression in human monocytes. A study of the molecular mechanisms involved in inflammatory cytokine expression. J. Biol. Chem. 269, 4201-4206 (Pubitemid 24237776)
5. Melly, M. A., McGee, Z. A., and Rosenthal, R. S. (1984) Ability of monomeric peptidoglycan fragments from Neisseria gonorrhoeae to damage human fallopian-tube mucosa. J. Infect. Dis. 149, 378-386 (Pubitemid 14138240)
6. Melly, M. A., Gregg, C. R., and McGee, Z. A. (1981) Studies of toxicity of Neisseria gonorrhoeae for human fallopian tube mucosa. J. Infect. Dis. 143, 423-431 (Pubitemid 11113663)
7. Burg, N. D., and Pillinger, M. H. (2001) The neutrophil. Function and regulation in innate and humoral immunity. Clin. Immunol. 99, 7-17
8. Tseng, H. J., Srikhanta, Y., McEwan, A. G., and Jennings, M. P. (2001) Accumulation of manganese in Neisseria gonorrhoeae correlates with resistance to oxidative killing by superoxide anion and is independent of superoxide dismutase activity. Mol. Microbiol. 40, 1175-1186 (Pubitemid 32574984)
9. Turner, S., Reid, E., Smith, H., and Cole, J. (2003) A novel cytochrome c peroxidase from Neisseria gonorrhoeae. A lipoprotein from a Gram-negative bacterium. Biochem. J. 373, 865-873 (Pubitemid 36981096)
10. Soler-García, A. A., and Jerse, A. E. (2004) A Neisseria gonorrhoeae catalase mutant is more sensitive to hydrogen peroxide and paraquat, an inducer of toxic oxygen radicals. Microb. Pathog. 37, 55-63 (Pubitemid 39093877)
11. Seib, K. L., Tseng, H. J., McEwan, A. G., Apicella, M. A., and Jennings, M. P. (2004) Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis. Distinctive systems for different lifestyles. J. Infect. Dis. 190, 136-147 (Pubitemid 38858414)
12. Skaar, E. P., Tobiason, D. M., Quick, J., Judd, R. C., Weissbach, H., Etienne, F., Brot, N., and Seifert, H. S. (2002) The outer membrane localization of the Neisseria gonorrhoeae MsrA/B is involved in survival against reactive oxygen species. Proc. Natl. Acad. Sci. U.S.A. 99, 10108-10113 (Pubitemid 34831180)
13. Stohl, E. A., and Seifert, H. S. (2006) Neisseria gonorrhoeae DNA recombination and repair enzymes protect against oxidative damage caused by hydrogen peroxide. J. Bacteriol. 188, 7645-7651 (Pubitemid 44646264)
14. Shafer, W. M., Qu, X., Waring, A. J., and Lehrer, R. I. (1998) Modulation of Neisseria gonorrhoeae susceptibility to vertebrate antibacterial peptides due to a member of the resistance/nodulation/division efflux pump family. Proc. Natl. Acad. Sci. U.S.A. 95, 1829-1833 (Pubitemid 28103479)
15. Lee, E. H., and Shafer, W. M. (1999) The farAB-encoded efflux pump mediates resistance of gonococci to long-chained antibacterial fatty acids. Mol. Microbiol. 33, 839-845 (Pubitemid 29392663)
16. Jerse, A. E., Sharma, N. D., Simms, A. N., Crow, E. T., Snyder, L. A., and Shafer, W. M. (2003)Agonococcal efflux pump system enhances bacterial survival in a female mouse model of genital tract infection. Infect. Immun. 71, 5576-5582 (Pubitemid 37205608)
17. Rest, R. F., Fischer, S. H., Ingham, Z. Z., and Jones, J. F. (1982) Interactions of Neisseria gonorrhoeae with human neutrophils. Effects of serum and gonococcal opacity on phagocyte killing and chemiluminescence. Infect. Immun. 36, 737-744 (Pubitemid 12101905)
18. Frangipane, J. V., and Rest, R. F. (1992) Anaerobic growth of gonococci does not alter their Opa-mediated interactions with human neutrophils. Infect. Immun. 60, 1793-1799
19. Seib, K. L., Simons, M. P., Wu, H. J., McEwan, A. G., Nauseef, W. M., Apicella, M. A., and Jennings, M. P. (2005) Investigation of oxidative stress defenses of Neisseria gonorrhoeae by using a human polymorphonuclear leukocyte survival assay. Infect. Immun. 73, 5269-5272 (Pubitemid 41105695)
20. Criss, A. K., Katz, B. Z., and Seifert, H. S. (2009) Resistance of Neisseriagonorrhoeae to non-oxidative killing by adherent human polymorphonuclear leukocytes. Cell Microbiol. 11, 1074-1087
21. Criss, A. K., and Seifert, H. S. (2008) Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes. Cell Microbiol. 10, 2257-2270
22. Stohl, E. A., Criss, A. K., and Seifert, H. S. (2005) The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection. Mol. Microbiol. 58, 520-532 (Pubitemid 41476166)
23. Höltje, J. V. (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev. 62, 181-203
24. Boneca, I. G. (2005) The role of peptidoglycan in pathogenesis. Curr. Opin. Microbiol. 8, 46-53
25. Cloud-Hansen, K. A., Peterson, S. B., Stabb, E. V., Goldman, W. E., McFall- Ngai, M. J., and Handelsman, J. (2006) Breaching the great wall. Peptidoglycan and microbial interactions. Nat. Rev. Microbiol. 4, 710-716
26. Rosenthal, R. S., Nogami, W., Cookson, B. T., Goldman, W. E., and Folkening, W. J. (1987) Major fragment of soluble peptidoglycan released from growing Bordetella pertussis is tracheal cytotoxin. Infect. Immun. 55, 2117-2120 (Pubitemid 17139290)
27. Sycuro, L. K., Pincus, Z., Gutierrez, K. D., Biboy, J., Stern, C. A., Vollmer, W., and Salama, N. R. (2010) Peptidoglycan cross-linking relaxation promotes Helicobacter pylori's helical shape and stomach colonization. Cell 141, 822-833
28. Bonis, M., Ecobichon, C., Guadagnini, S., Prévost, M. C., and Boneca, I. G. (2010)AM23B family metallopeptidase of Helicobacter pylori required for cell shape, pole formation, and virulence. Mol. Microbiol. 78, 809-819
29. Mehr, I. J., and Seifert, H. S. (1998) Differential roles of homologous recombination pathways in Neisseria gonorrhoeae pilin antigenic variation, DNA transformation, and DNA repair. Mol. Microbiol. 30, 697-710 (Pubitemid 28528590)
30. Stohl, E. A., and Seifert, H. S. (2001) The recX gene potentiates homologous recombination in Neisseria gonorrhoeae. Mol. Microbiol. 40, 1301-1310 (Pubitemid 32635300)
31. Hamilton, H. L., Domínguez, N. M., Schwartz, K. J., Hackett, K. T., and Dillard, J. P. (2005) Neisseria gonorrhoeae secretes chromosomal DNA via a novel type IV secretion system. Mol. Microbiol. 55, 1704-1721 (Pubitemid 40445208)
32. Zahrl, D., Wagner, M., Bischof, K., Bayer, M., Zavecz, B., Beranek, A., Ruckenstuhl, C., Zarfel, G. E., and Koraimann, G. (2005) Peptidoglycan degradation by specialized lytic transglycosylases associated with type III and type IV secretion systems. Microbiology 151, 3455-3467 (Pubitemid 41632060)
33. Dillard, J. P., and Hackett, K. T. (2005) Mutations affecting peptidoglycan acetylation in Neisseria gonorrhoeae and Neisseria meningitidis. Infect. Immun. 73, 5697-5705 (Pubitemid 41193005)
34. Jayaswal, R. K., Lee, Y. I., and Wilkinson, B. J. (1990) Cloning and expression of a Staphylococcus aureus gene encoding a peptidoglycan hydrolase activity. J. Bacteriol. 172, 5783-5788 (Pubitemid 20317115)
35. Bernadsky, G., Beveridge, T. J., and Clarke, A. J. (1994) Analysis of the sodium dodecyl sulfate-stable peptidoglycan autolysins of select gram-negative pathogens by using renaturing polyacrylamide gel electrophoresis. J. Bacteriol. 176, 5225-5232 (Pubitemid 24273507)
36. Ohnishi, R., Ishikawa, S., and Sekiguchi, J. (1999) Peptidoglycan hydrolase LytF plays a role in cell separation with CwlF during vegetative growth of Bacillus subtilis. J. Bacteriol. 181, 3178-3184 (Pubitemid 29236924)
37. Clarke, T. B., Kawai, F., Park, S. Y., Tame, J. R., Dowson, C. G., and Roper, D. I. (2009) Mutational analysis of the substrate specificity of Escherichia coli penicillin binding protein 4. Biochemistry 48, 2675-2683
38. Lloyd, A. J., Gilbey, A. M., Blewett, A. M., De Pascale, G., El Zoeiby, A., Levesque, R. C., Catherwood, A. C., Tomasz, A., Bugg, T. D., Roper, D. I., and Dowson, C. G. (2008) Characterization of tRNA-dependent peptide bond formation by MurM in the synthesis of Streptococcus pneumoniae peptidoglycan. J. Biol. Chem. 283, 6402-6417
39. Kyte, J., and Doolittle, R. F. (1982) A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157, 105-132
40. Sechman, E. V., Rohrer, M. S., and Seifert, H. S. (2005) A genetic screen identifies genes and sites involved in pilin antigenic variation in Neisseria gonorrhoeae. Mol. Microbiol. 57, 468-483 (Pubitemid 40979346)
41. Odintsov, S. G., Sabala, I., Marcyjaniak, M., and Bochtler, M. (2004) Latent LytM at 1.3 Å resolution. J. Mol. Biol. 335, 775-785
42. Wang, X., Yang, X., Yang, C., Wu, Z., Xu, H., and Shen, Y. (2011) Crystal structure of outer membrane protein NMB0315 from Neisseria meningitidis. PLoS One 6, e26845
43. Stefanova, M. E., Tomberg, J., Davies, C., Nicholas, R. A., and Gutheil, W. G. (2004) Overexpression and enzymatic characterization of Neisseria gonorrhoeae penicillin-binding protein 4. Eur. J. Biochem. 271, 23-32 (Pubitemid 38122162)
44. Stefanova, M. E., Tomberg, J., Olesky, M., Höltje, J. V., Gutheil, W. G., and Nicholas, R. A. (2003) Neisseria gonorrhoeae penicillin-binding protein 3 exhibits exceptionally high carboxypeptidase and β-lactam binding activities. Biochemistry 42, 14614-14625 (Pubitemid 37532008)
45. Fussenegger, M., Kahrs, A. F., Facius, D., and Meyer, T. F. (1996) Tetrapac (tpc), a novel genotype of Neisseria gonorrhoeae affecting epithelial cell invasion, natural transformation competence, and cell separation. Mol. Microbiol. 19, 1357-1372 (Pubitemid 26111506)
46. Garcia, D. L., and Dillard, J. P. (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 (Pubitemid 44547626)
47. Cloud, K. A., and Dillard, J. P. (2004) Mutation of a single lytic transglycosylase causes aberrant septation and inhibits cell separation of Neisseria gonorrhoeae. J. Bacteriol. 186, 7811-7814 (Pubitemid 39463749)
48. Layec, S., Gérard, J., Legué, V., Chapot-Chartier, M. P., Courtin, P., Borges, F., Decaris, B., and Leblond-Bourget, N. (2009) The CHAP domain of Cse functions as an endopeptidase that acts at mature septa to promote Streptococcus thermophilus cell separation. Mol. Microbiol. 71, 1205-1217
49. Stentz, R., Wegmann, U., Parker, M., Bongaerts, R., Lesaint, L., Gasson, M., and Shearman, C. (2009) CsiA is a bacterial cell wall synthesis inhibitor contributing toDNAtranslocation through the cell envelope. Mol. Microbiol. 72, 779-794
50. Camiade, E., Peltier, J., Bourgeois, I., Couture-Tosi, E., Courtin, P., Antunes, A., Chapot-Chartier, M. P., Dupuy, B., and Pons, J. L. (2010) Characterization of Acp, a peptidoglycan hydrolase of Clostridium perfringens with N-acetylglucosaminidase activity that is implicated in cell separation and stress-induced autolysis. J. Bacteriol. 192, 2373-2384
51. Uehara, T., Dinh, T., and Bernhardt, T. G. (2009) LytM-domain factors are required for daughter cell separation and rapid ampicillin-induced lysis in Escherichia coli. J. Bacteriol. 191, 5094-5107
52. Poggio, S., Takacs, C. N., Vollmer, W., and Jacobs-Wagner, C. (2010) A protein critical for cell constriction in the Gram-negative bacterium Caulobacter crescentus localizes at the division site through its peptidoglycan-binding LysM domains. Mol. Microbiol. 77, 74-89
53. Goley, E. D., Comolli, L. R., Fero, K. E., Downing, K. H., and Shapiro, L. (2010) DipM links peptidoglycan remodeling to outer membrane organization in Caulobacter. Mol. Microbiol. 77, 56-73
54. Möll, A., Schlimpert, S., Briegel, A., Jensen, G. J., and Thanbichler, M. (2010) DipM, a new factor required for peptidoglycan remodeling during cell division in Caulobacter crescentus. Mol. Microbiol. 77, 90-107
55. Nambu, T., Minamino, T., Macnab, R. M., and Kutsukake, K. (1999) Peptidoglycan- hydrolyzing activity of the FlgJ protein, essential for flagellar rod formation in Salmonella typhimurium. J. Bacteriol. 181, 1555-1561 (Pubitemid 29110816)
56. Dijkstra, A. J., and Keck, W. (1996) Peptidoglycan as a barrier to transenvelope transport. J. Bacteriol. 178, 5555-5562 (Pubitemid 26327652)
57. Dillard, J. P., and Seifert, H. S. (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 (Pubitemid 32661001)