Constitutively opa-expressing and opa-deficient neisseria gonorrhoeae strains differentially stimulate and survive exposure to human neutrophils

Journal of Bacteriology

Volumn 195, Issue 13, 2013, Pages 2982-2990

  Ball, Louise M ^a   Criss, Alison K ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; OPACITY ASSOCIATED PROTEIN; POLYMYXIN B; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIUM COLONY; EPITHELIUM CELL; GENE DELETION; GENE EXPRESSION; GONORRHEA; HUMAN; HUMAN CELL; INTERNALIZATION; NEISSERIA GONORRHOEAE; NEUTROPHIL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RESPIRATORY BURST;

BACTERIAL OUTER MEMBRANE PROTEINS; HUMANS; NEISSERIA GONORRHOEAE; NEUTROPHILS;

BACTERIA (MICROORGANISMS); NEISSERIA; NEISSERIA GONORRHOEAE;

EID: 84880005880     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00171-13     Document Type: Article

References (67)

1. Allen VG, Mitterni L, Seah C, Rebbapragada A, Martin IE, Lee C, Siebert H, Towns L, Melano RG, Low DE. 2013. Neisseria gonorrhoeae treatment failure and susceptibility to cefixime in Toronto, Canada. JAMA 309:163-170.
2. Unemo M, Shafer WM. 2011. Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future. Ann. N. Y. Acad. Sci. 1230:E19-E28.
3. Schmid G. 2009. Global incidence and prevalence of four curable sexually transmitted infections (STIs): new estimates from WHO. The 2nd Global HIV/AIDS Surveillance Meeting, Bangkok, Thailand.
4. Criss AK, Seifert HS. 2012. A bacterial siren song: intimate interactions between Neisseria and neutrophils. Nat. Rev. Microbiol. 10:178-190.
5. Virji M. 2009. Pathogenic Neisseriae: surface modulation, pathogenesis and infection control. Nat. Rev. Microbiol. 7:274-286.
6. Swanson J. 1978. Studies on gonococcus infection. XIV. Cell wall protein differences among color/opacity colony variants of Neisseria gonorrhoeae. Infect. Immun. 21:292-302.
7. Bhat KS, Gibbs CP, Barrera O, Morrison SG, Jahnig F, Stern A, Kupsch EM, Meyer TF, Swanson J. 1991. The opacity proteins of Neisseria gonorrhoeae strain MS11 are encoded by a family of 11 complete genes. Mol. Microbiol. 5:1889-1901.
8. Dempsey JA, Litaker W, Madhure A, Snodgrass TL, Cannon JG. 1991. Physical map of the chromosome of Neisseria gonorrhoeae FA1090 with locations of genetic markers, including opa and pil genes. J. Bacteriol. 173:5476-5486.
9. Connell TD, Shaffer D, Cannon JG. 1990. Characterization of the repertoire of hypervariable regions in the protein II (opa) gene family of Neisseria gonorrhoeae. Mol. Microbiol. 4:439-449.
10. Vandeputte-Rutten L, Bos MP, Tommassen J, Gros P. 2003. Crystal structure of neisserial surface protein A (NspA), a conserved outer membrane protein with vaccine potential. J. Biol. Chem. 278:24825-24830.
11. de Jonge MI, Hamstra HJ, van Alphen L, Dankert J, van der Ley P. 2003. Mapping the binding domains on meningococcal Opa proteins for CEACAM1 and CEA receptors. Mol. Microbiol. 50:1005-1015.
12. Malorny B, Morelli G, Kusecek B, Kolberg J, Achtman M. 1998. Sequence diversity, predicted two-dimensional protein structure, and epitope mapping of Neisserial Opa proteins. J. Bacteriol. 180:1323-1330.
13. Sadarangani M, Pollard AJ, Gray-Owen SD. 2011. Opa proteins and CEACAMs: pathways of immune engagement for pathogenic Neisseria. FEMS Microbiol. Rev. 35:498-514.
14. + gonococci to epithelial cells in vitro involves heparan sulfate. J. Exp. Med. 182:511-517.
15. van Putten JP, Paul SM. 1995. Binding of syndecan-like cell surface proteoglycan receptors is required for Neisseria gonorrhoeae entry into human mucosal cells. EMBO J. 14:2144-2154.
16. Duensing TD, van Putten JP. 1997. Vitronectin mediates internalization of Neisseria gonorrhoeae by Chinese hamster ovary cells. Infect. Immun. 65:964-970.
17. Gomez-Duarte OG, Dehio M, Guzman CA, Chhatwal GS, Dehio C, Meyer TF. 1997. Binding of vitronectin to opa-expressing Neisseria gonorrhoeae mediates invasion of HeLa cells. Infect. Immun. 65:3857-3866.
18. Blake MS, Blake CM, Apicella MA, Mandrell RE. 1995. Gonococcal opacity: lectin-like interactions between Opa proteins and lipooligosaccharide. Infect. Immun. 63:1434-1439.
19. Levan A, Zimmerman LI, Mahle AC, Swanson KV, Deshong P, Park J, Edwards VL, Song W, Stein DC. 2012. Construction and characterization of a derivative of Neisseria gonorrhoeae strain MS11 devoid of all opa genes. J. Bacteriol. 194:6468-6478.
20. Stern A, Brown M, Nickel P, Meyer TF. 1986. Opacity genes in Neisseria gonorrhoeae: control of phase and antigenic variation. Cell 47:61-71.
21. Murphy GL, Connell TD, Barritt DS, Koomey M, Cannon JG. 1989. Phase variation of gonococcal protein II: regulation of gene expression by slipped-strand mispairing of a repetitive DNA sequence. Cell 56:539-547.
22. Mayer LW. 1982. Rates in vitro changes of gonococcal colony opacity phenotypes. Infect. Immun. 37:481-485.
23. Black WJ, Schwalbe RS, Nachamkin I, Cannon JG. 1984. Characterization of Neisseria gonorrhoeae protein II phase variation by use of monoclonal antibodies. Infect. Immun. 45:453-457.
24. Simms AN, Jerse AE. 2006. In vivo selection for Neisseria gonorrhoeae opacity protein expression in the absence of human carcinoembryonic antigen cell adhesion molecules. Infect. Immun. 74:2965-2974.
25. Jerse AE, Cohen MS, Drown PM, Whicker LG, Isbey SF, Seifert HS, Cannon JG. 1994. Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male. J. Exp. Med. 179:911-920.
26. Swanson J, Barrera O, Sola J, Boslego J. 1988. Expression of outer membrane protein II by gonococci in experimental gonorrhea. J. Exp. Med. 168:2121-2129.
27. Roos D, van Bruggen R, Meischl C. 2003. Oxidative killing of microbes by neutrophils. Microbes Infect. 5:1307-1315.
28. Rest RF, Fischer SH, Ingham ZZ, Jones JF. 1982. Interactions of Neisseria gonorrhoeae with human neutrophils: effects of serum and gonococcal opacity on phagocyte killing and chemiluminescence. Infect. Immun. 36:737-744.
29. Virji M, Heckels JE. 1986. The effect of protein II and pili on the interaction of Neisseria gonorrhoeae with human polymorphonuclear leucocytes. J. Gen. Microbiol. 132:503-512.
30. Fischer SH, Rest RF. 1988. Gonococci possessing only certain P.II outer membrane proteins interact with human neutrophils. Infect. Immun. 56: 1574-1579.
31. Kupsch EM, Knepper B, Kuroki T, Heuer I, Meyer TF. 1993. Variable opacity (Opa) outer membrane proteins account for the cell tropisms displayed by Neisseria gonorrhoeae for human leukocytes and epithelial cells. EMBO J. 12:641-650.
32. King GJ, Swanson J. 1978. Studies on gonococcus infection. XV. Identification of surface proteins of Neisseria gonorrhoeae correlated with leukocyte association. Infect. Immun. 21:575-584.
33. Criss AK, Seifert HS. 2008. Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes. Cell. Microbiol. 10:2257-2270.
34. Simons MP, Nauseef WM, Apicella MA. 2005. Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes. Infect. Immun. 73:1971-1977.
35. Criss AK, Katz BZ, Seifert HS. 2009. Resistance of Neisseria gonorrhoeae to non-oxidative killing by adherent human polymorphonuclear leucocytes. Cell. Microbiol. 11:1074-1087.
36. Farrell CF, Rest RF. 1990. Up-regulation of human neutrophil receptors for Neisseria gonorrhoeae expressing PII outer membrane proteins. Infect. Immun. 58:2777-2784.
37. Sarantis H, Gray-Owen SD. 2007. The specific innate immune receptor CEACAM3 triggers neutrophil bactericidal activities via a Syk kinasedependent pathway. Cell. Microbiol. 9:2167-2180.
38. Dekker NP, Lammel CJ, Mandrell RE, Brooks GF. 1990. Opa (protein II) influences gonococcal organization in colonies, surface appearance, size and attachment to human fallopian tube tissues. Microb. Pathog. 9:19-31.
39. Seifert HS, Wright CJ, Jerse AE, Cohen MS, Cannon JG. 1994. Multiple gonococcal pilin antigenic variants are produced during experimental human infections. J. Clin. Invest. 93:2744-2749.
40. Cahoon LA, Seifert HS. 2009. An alternative DNA structure is necessary for pilin antigenic variation in Neisseria gonorrhoeae. Science 325:764-767.
41. Kellogg DS, Jr, Peacock WL, Jr, Deacon WE, Brown L, Pirkle DI. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J. Bacteriol. 85:1274-1279.
42. Heckman KL, Pease LR. 2007. Gene splicing and mutagenesis by PCRdriven overlap extension. Nat. Protoc. 2:924-932.
43. Stohl EA, Seifert HS. 2001. The recX gene potentiates homologous recombination in Neisseria gonorrhoeae. Mol. Microbiol. 40:1301-1310.
44. Criss AK, Seifert HS. 2006. Gonococci exit apically and basally from polarized epithelial cells and exhibit dynamic changes in type IV pili. Cell. Microbiol. 8:1430-1443.
45. Davis MR, Jr, Goldberg JB. 2012. Purification and visualization of lipopolysaccharide from Gram-negative bacteria by hot aqueous-phenol extraction. J. Vis. Exp. 63:3916. doi:10.3791/3916.
46. Sechman EV, Kline KA, Seifert HS. 2006. Loss of both Holliday junction processing pathways is synthetically lethal in the presence of gonococcal pilin antigenic variation. Mol. Microbiol. 61:185-193.
47. Stohl EA, Criss AK, Seifert HS. 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.
48. Johnson MB, Criss AK. 4 February 2013, posting date. Neisseria gonorrhoeae phagosomes delay fusion with primary granules to enhance bacterial survival inside human neutrophils. Cell. Microbiol. [Epub ahead of print.] doi:10.1111/cmi.12117.
49. Shafer WM, Qu X, Waring AJ, Lehrer RI. 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.
50. Cole JG, Fulcher NB, Jerse AE. 2010. Opacity proteins increase Neisseria gonorrhoeae fitness in the female genital tract due to a factor under ovarian control. Infect. Immun. 78:1629-1641.
51. Cohen MS, Cannon JG, Jerse AE, Charniga LM, Isbey SF, Whicker LG. 1994. Human experimentation with Neisseria gonorrhoeae: rationale, methods, and implications for the biology of infection and vaccine development. J. Infect. Dis. 169:532-537.
52. Jerse AE. 1999. Experimental gonococcal genital tract infection and opacity protein expression in estradiol-treated mice. Infect. Immun. 67:5699-5708.
53. Fulcher NB. 2004. The role of Neisseria gonorrhoeae opacity proteins in host cell interactions and pathogenesis. Ph.D. thesis. University of North Carolina, Chapel Hill, NC.
54. Frangipane JV, Rest RF. 1992. Anaerobic growth of gonococci does not alter their Opa-mediated interactions with human neutrophils. Infect. Immun. 60:1793-1799.
55. Seib KL, Simons MP, Wu HJ, McEwan AG, Nauseef WM, Apicella MA, Jennings MP. 2005. Investigation of oxidative stress defenses of Neisseria gonorrhoeae by using a human polymorphonuclear leukocyte survival assay. Infect. Immun. 73:5269-5272.
56. Wu H, Soler-Garcia AA, Jerse AE. 2009. A strain-specific catalase mutation and mutation of the metal-binding transporter gene mntC attenuate Neisseria gonorrhoeae in vivo but not by increasing susceptibility to oxidative killing by phagocytes. Infect. Immun. 77:1091-1102.
57. Hobbs MM, Sparling PF, Cohen MS, Shafer WM, Deal CD, Jerse AE. 2011. Experimental gonococcal infection in male volunteers: cumulative experience with Neisseria gonorrhoeae strains FA1090 and MS11mkC. Front. Microbiol. 2:123.
58. Jerse AE, Wu H, Packiam M, Vonck RA, Begum AA, Garvin LE. 2011. Estradiol-treated female mice as surrogate hosts for Neisseria gonorrhoeae genital tract infections. Front. Microbiol. 2:107.
59. Sadarangani M, Hoe JC, Callaghan MJ, Jones C, Chan H, Makepeace K, Daniels-Treffandier H, Deadman ME, Bayliss C, Feavers I, van der Ley P, Pollard AJ. 2012. Construction of Opa-positive and Opa-negative strains of Neisseria meningitidis to evaluate a novel meningococcal vaccine. PLoS One 7:e51045. doi:10.1371/journal.pone.0051045.
60. Lim JP, Gleeson PA. 2011. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol. Cell Biol. 89:836-843.
61. Shafer WM, Onunka VC, Martin LE. 1986. Antigonococcal activity of human neutrophil cathepsin G. Infect. Immun. 54:184-188.
62. James JF, Swanson J. 1978. Studies on gonococcus infection. XIII. Occurrence of color/opacity colonial variants in clinical cultures. Infect. Immun. 19:332-340.
63. Merz AJ, So M. 2000. Interactions of pathogenic Neisseriae with epithelial cell membranes. Annu. Rev. Cell Dev. Biol. 16:423-457.
64. Wang J, Gray-Owen SD, Knorre A, Meyer TF, Dehio C. 1998. Opa binding to cellular CD66 receptors mediates the transcellular traversal of Neisseria gonorrhoeae across polarized T84 epithelial cell monolayers. Mol. Microbiol. 30:657-671.
65. Boulton IC, Gray-Owen SD. 2002. Neisserial binding to CEACAM1 arrests the activation and proliferation of CD4+ T lymphocytes. Nat. Immunol. 3:229-236.
66. Liu Y, Islam EA, Jarvis GA, Gray-Owen SD, Russell MW. 2012. Neisseria gonorrhoeae selectively suppresses the development of Th1 and Th2 cells, and enhances Th17 cell responses, through TGF-beta-dependent mechanisms. Mucosal Immunol. 5:320-331.
67. Pantelic M, Kim YJ, Bolland S, Chen I, Shively J, Chen T. 2005. Neisseria gonorrhoeae kills carcinoembryonic antigen-related cellular adhesion molecule 1 (CD66a)-expressing human B cells and inhibits antibody production. Infect. Immun. 73:4171-4179.