Transcriptional profiling identifies the metabolic phenotype of gonococcal biofilms

Infection and Immunity

Volumn 77, Issue 9, 2009, Pages 3522-3532

  Falsetta, Megan L ^a   Bair, Thomas B ^a   Shan, Chi Ku ^b   Vanden Hoven, Rachel N ^b   Steichen, Christopher T ^a   McEwan, Alastair G ^b   Jennings, Michael P ^b   Apicella, Michael A ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL RNA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE;

ANAEROBIC METABOLISM; ANIA GENE; ARTICLE; BACTERIAL GENE; BIOFILM; CCP GENE; CONTROLLED STUDY; DOWN REGULATION; GENE CLUSTER; HUMAN; HUMAN CELL; NEISSERIA GONORRHOEAE; NONHUMAN; NORB GENE; PHENOTYPE; PRIORITY JOURNAL; SURFACE PROPERTY; UPREGULATION;

ANAEROBIOSIS; ANTIGENS, BACTERIAL; BACTERIAL OUTER MEMBRANE PROTEINS; BIOFILMS; CELLS, CULTURED; CYTOCHROME-C PEROXIDASE; FEMALE; GENE EXPRESSION PROFILING; HUMANS; NEISSERIA GONORRHOEAE; NITRIC OXIDE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYGEN CONSUMPTION; PHENOTYPE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 69049095029     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00036-09     Document Type: Article

References (68)

1. Arai, H., Y. Igarashi, and T. Kodama. 1995. The structural genes for nitric oxide reductase from Pseudomonas aeruginosa. Biochim. Biophys. Acta 1261:279-284.
2. Barraud, N., D. J. Hassett, S. H. Hwang, S. A. Rice, S. Kjelleberg, and J. S. Webb. 2006. Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J. Bacteriol. 188:7344-7353.
3. Brown, G. C., and V. Borutaite. 2004. Inhibition of mitochondrial respiratory complex I by nitric oxide, peroxynitrite and S-nitrosothiols. Biochim. Biophys. Acta 1658:44-49.
4. Cardinale, J. A., and V. L. Clark. 2005. Determinants of nitric oxide steadystate levels during anaerobic respiration by Neisseria gonorrhoeae. Mol. Microbiol. 58:177-188.
5. Cardinale, J. A., and V. L. Clark. 2000. Expression of AniA, the major anaerobically induced outer membrane protein of Neisseria gonorrhoeae, provides protection against killing by normal human sera. Infect. Immun. 68:4368-4369.
6. Carreras, M. C., G. A. Pargament, S. D. Catz, J. J. Poderoso, and A. Boveris. 1994. Kinetics of nitric oxide and hydrogen peroxide production and formation of peroxynitrite during the respiratory burst of human neutrophils. FEBS Lett. 341:65-68.
7. Centers for Disease Control and Prevention. 2007. Update to CDC's sexually transmitted diseases treatment guidelines, 2006: fluoroquinolones no longer recommended for treatment of gonococcal infections. MMWR Morb. Mortal. Wkly. Rep. 56:332-336.
8. Centers for Disease Control and Prevention. 2007. Sexually transmitted disease surveillance 2006. The Department of Health and Human Services, Atlanta, GA.
9. Ceri, H., M. E. Olson, C. Stremick, R. R. Read, D. Morck, and A. Buret. 1999. The Calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 37:1771-1776.
10. Chen, A., I. C. Boulton, J. Pongoski, A. Cochrane, and S. D. Gray-Owen. 2003. Induction of HIV-1 long terminal repeat-mediated transcription by Neisseria gonorrhoeae. AIDS 17:625-628.
11. Clark, V. L., L. A. Campbell, D. A. Palermo, T. M. Evans, and K. W. Klimpel. 1987. Induction and repression of outer membrane proteins by anaerobic growth of Neisseria gonorrhoeae. Infect. Immun. 55:1359-1364.
12. Clark, V. L., J. S. Knapp, S. Thompson, and K. W. Klimpel. 1988. Presence of antibodies to the major anaerobically induced gonococcal outer membrane protein in sera from patients with gonococcal infections. Microb. Pathog. 5:381-390.
13. Costerton, J. W., P. S. Stewart, and E. P. Greenberg. 1999. Bacterial biofilms: a common cause of persistent infections. Science 284:1318-1322.
14. Davis, K. L., E. Martin, I. V. Turko, and F. Murad. 2001. Novel effects of nitric oxide. Annu. Rev. Pharmacol. Toxicol. 41:203-236.
15. Dunn, G. M., R. A. Herbert, and C. M. Brown. 1979. Influence of oxygen tension on nitrate reduction by a Klebsiella sp. growing in chemostat culture. J. Gen. Microbiol. 112:379-383.
16. Dunne, W. M., Jr. 2002. Bacterial adhesion: seen any good biofilms lately? Clin. Microbiol. Rev. 15:155-166.
17. Edwards, J. L., and M. A. Apicella. 2005. I-domain-containing integrins serve as pilus receptors for Neisseria gonorrhoeae adherence to human epithelial cells. Cell. Microbiol. 7:1197-1211.
18. Edwards, J. L., E. J. Brown, K. A. Ault, and M. A. Apicella. 2001. The role of complement receptor 3 (CR3) in Neisseria gonorrhoeae infection of human cervical epithelia. Cell. Microbiol. 3:611-622.
19. Eschenbach, D. A., P. R. Davick, B. L. Williams, S. J. Klebanoff, K. Young-Smith, C. M. Critchlow, and K. K. Holmes. 1989. Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis. J. Clin. Microbiol. 27:251-256.
20. Fang, F. C. 1997. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J. Clin. Investig. 99:2818-2825.
21. Filiatrault, M. J., K. F. Picardo, H. Ngai, L. Passador, and B. H. Iglewski. 2006. Identification of Pseudomonas aeruginosa genes involved in virulence and anaerobic growth. Infect. Immun. 74:4237-4245.
22. Fleming, D. T., and J. N. Wasserheit. 1999. From epidemiological synergy to public health policy and practice: the contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex. Transm. Infect. 75:3-17.
23. Forte, E., A. Urbani, M. Saraste, P. Sarti, M. Brunori, and A. Giuffre. 2001. The cytochrome cbb3 from Pseudomonas stutzeri displays nitric oxide reductase activity. Eur. J. Biochem. 268:6486-6491.
24. Gerbase, A. C., J. T. Rowley, D. H. Heymann, S. F. Berkley, and P. Piot. 1998. Global prevalence and incidence estimates of selected curable STDs. Sex. Transm. Infect. 74(Suppl. 1):S12-S16.
25. Greiner, L. L., J. L. Edwards, J. Shao, C. Rabinak, D. Entz, and M. A. Apicella. 2005. Biofilm formation by Neisseria gonorrhoeae. Infect. Immun. 73:1964-1970.
26. Hassett, D. J., J. Cuppoletti, B. Trapnell, S. V. Lymar, J. J. Rowe, S. S. Yoon, G. M. Hilliard, K. Parvatiyar, M. C. Kamani, D. J. Wozniak, S. H. Hwang, T. R. McDermott, and U. A. Ochsner. 2002. Anaerobic metabolism and quorum sensing by Pseudomonas aeruginosa biofilms in chronically infected cystic fibrosis airways: rethinking antibiotic treatment strategies and drug targets. Adv. Drug Deliv. Rev. 54:1425-1443.
27. Hedges, S. R., D. A. Sibley, M. S. Mayo, E. W. Hook III, and M. W. Russell. 1998. Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections. J. Infect. Dis. 178:742-751.
28. Heydorn, A., A. T. Nielsen, M. Hentzer, C. Sternberg, M. Givskov, B. K. Ersboll, and S. Molin. 2000. Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395-2407.
29. Hoehn, G. T., and V. L. Clark. 1992. The major anaerobically induced outer membrane protein of Neisseria gonorrhoeae, Pan 1, is a lipoprotein. Infect. Immun. 60:4704-4708.
30. Hook, E. W., III, and H. H. Handsfield. 1999. Biology of Neisseria gonorrhoeae, p. 433-449. In K. K. Holmes, P. A. Mardh, P. F. Sparling, S. M. Lemon, W. E. Stamm, P. Piot, and J. N. Wasserjeot (ed.), Sexually transmitted diseases, 3rd ed. McGraw Hill, New York, NY.
31. Hook, E. W., III, and H. H. Handsfield. 1999. Gender perspectives and STDs, p. 117-127. In K. K. Holmes, P. A. Mardh, P. F. Sparling, S. M. Lemon, W. E. Stamm, P. Piot, and J. N. Wasserjeot (ed.), Sexually transmitted diseases, 3rd ed. McGraw Hill, New York, NY.
32. Hook, E. W., III, and H. H. Handsfield. 1999. Gonococcal infections in the adult, p. 451-466. In K. K. Holmes, P. A. Mardh, P. F. Sparling, S. M. Lemon, W. E. Stamm, P. Piot, and J. N. Wasserjeot (ed.), Sexually transmitted diseases, 3rd ed. McGraw Hill, New York, NY.
33. Householder, T. C., W. A. Belli, S. Lissenden, J. A. Cole, and V. L. Clark. 1999. cis- and trans-acting elements involved in regulation of aniA, the gene encoding the major anaerobically induced outer membrane protein in Neisseria gonorrhoeae. J. Bacteriol. 181:541-551.
34. Householder, T. C., E. M. Fozo, J. A. Cardinale, and V. L. Clark. 2000. Gonococcal nitric oxide reductase is encoded by a single gene, norB, which is required for anaerobic growth and is induced by nitric oxide. Infect. Immun. 68:5241-5246.
35. James-Holmquest, A. N., R. D. Wende, R. L. Mudd, and R. P. Williams. 1973. Comparison of atmospheric conditions for culture of clinical specimens of Neisseria gonorrhoeae. Appl. Microbiol. 26:466-469.
36. Jennings, M. P., M. Bisercic, K. L. Dunn, M. Virji, A. Martin, K. E. Wilks, J. C. Richards, and E. R. Moxon. 1995. Cloning and molecular analysis of the Isi1 (rfaF) gene of Neisseria meningitidis which encodes a heptosyl-2-transferase involved in LPS biosynthesis: evaluation of surface exposed carbohydrates in LPS mediated toxicity for human endothelial cells. Microb. Pathog. 19:391-407.
37. Kellogg, D. S., Jr., W. L. Peacock, Jr., W. E. Deacon, L. Brown, and D. I. Pirkle. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J. Bacteriol. 85:1274-1279.
38. Klingelhutz, A. J., S. A. Barber, P. P. Smith, K. Dyer, and J. K. McDougall. 1994. Restoration of telomeres in human papillomavirus- immortalized human anogenital epithelial cells. Mol. Cell. Biol. 14:961-969.
39. Knapp, J. S., and V. L. Clark. 1984. Anaerobic growth of Neisseria gonorrhoeae coupled to nitrite reduction. Infect. Immun. 46:176-181.
40. Ledingham, M. A., A. J. Thomson, A. Young, L. M. Macara, I. A. Greer, and J. E. Norman. 2000. Changes in the expression of nitric oxide synthase in the human uterine cervix during pregnancy and parturition. Mol. Hum. Reprod. 6:1041-1048.
41. Liaudet, L., F. G. Soriano, and C. Szabo. 2000. Biology of nitric oxide signaling. Crit. Care Med. 28:N37-N52.
42. Lissenden, S., S. Mohan, T. Overton, T. Regan, H. Crooke, J. A. Cardinale, T. C. Householder, P. Adams, C. D. O'Conner, V. L. Clark, H. Smith, and J. A. Cole. 2000. Identification of transcription activators that regulate gonococcal adaptation from aerobic to anaerobic or oxygen-limited growth. Mol. Microbiol. 37:839-855.
43. Loesche, W. J., F. Gusberti, G. Mettraux, T. Higgins, and S. Syed. 1983. Relationship between oxygen tension and subgingival bacterial flora in untreated human periodontal pockets. Infect. Immun. 42:659-667.
44. MacMicking, J., Q. W. Xie, and C. Nathan. 1997. Nitric oxide and macrophage function. Annu. Rev. Immunol. 15:323-350.
45. McCall, T. B., N. K. Boughton-Smith, R. M. Palmer, B. J. Whittle, and S. Moncada. 1989. Synthesis of nitric oxide from L-arginine by neutrophils. Release and interaction with superoxide anion. Biochem. J. 261:293-296.
46. Mellies, J., J. Jose, and T. F. Meyer. 1997. The Neisseria gonorrhoeae gene aniA encodes an inducible nitrite reductase. Mol. Gen. Genet. 256:525-532.
47. Ortega Mateo, A., and A. A. de Artiñano. 2000. Nitric oxide reactivity and mechanisms involved in its biological effects. Pharmacol. Res. 42:421-427.
48. Overton, T. W., R. Whitehead, Y. Li, L. A. Snyder, N. J. Saunders, H. Smith, and J. A. Cole. 2006. Coordinated regulation of the Neisseria gonorrhoeae-truncated denitrification pathway by the nitric oxide-sensitive repressor, NsrR, and nitrite-insensitive NarQ-NarP. J. Biol. Chem. 281:33115-33126.
49. Rock, J. D., and J. W. Moir. 2005. Microaerobic denitrification in Neisseria meningitidis. Biochem. Soc. Trans. 33:134-136.
50. Russell, M. W., S. R. Hedges, H. Y. Wu, E. W. Hook III, and J. Mestecky. 1999. Mucosal immunity in the genital tract: prospects for vaccines against sexually transmitted diseases-a review. Am. J. Reprod. Immunol. 42:58-63.
51. Schierholz, J. M., J. Beuth, D. Konig, A. Nurnberger, and G. Pulverer. 1999. Antimicrobial substances and effects on sessile bacteria. Zentralbl. Bakteriol. 289:165-177.
52. Schlag, S., C. Nerz, T. A. Birkenstock, F. Altenberend, and F. Gotz. 2007. Inhibition of staphylococcal biofilm formation by nitrite. J. Bacteriol. 189:7911-7919.
53. Seib, K. L., H. J. Tseng, A. G. McEwan, M. A. Apicella, and M. P. Jennings. 2004. Defenses against oxidative stress in Neisseria gonorrhoeae and Neisseria meningitidis: distinctive systems for different lifestyles. J. Infect. Dis. 190:136-147.
54. Seib, K. L., H. J. Wu, S. P. Kidd, M. A. Apicella, M. P. Jennings, and A. G. McEwan. 2006. Defenses against oxidative stress in Neisseria gonorrhoeae: a system tailored for a challenging environment. Microbiol. Mol. Biol. Rev. 70:344-361.
55. Short, H. B., V. L. Clark, D. S. Kellogg, Jr., and F. E. Young. 1982. Anaerobic survival of clinical isolates and laboratory strains of Neisseria gonorrhoeae: use in transfer and storage. J. Clin. Microbiol. 15:915-919.
56. Smith, L. D. 1975. The pathogenic anaerobic bacteria. Charles C. Thomas, Springfield, IL.
57. St. Amant, D. C., I. E. Valentin-Bon, and A. E. Jerse. 2002. Inhibition of Neisseria gonorrhoeae by Lactobacillus species that are commonly isolated from the female genital tract. Infect. Immun. 70:7169-7171.
58. Stefano, G. B., Y. Goumon, T. V. Bilfinger, I. D. Welters, and P. Cadet. 2000. Basal nitric oxide limits immune, nervous and cardiovascular excitation: human endothelia express a mu opiate receptor. Prog. Neurobiol. 60:513-530.
59. Steichen, C. T., J. Q. Shao, M. R. Ketterer, and M. A. Apicella. 2008. Gonococcal cervicitis: a role for biofilm in pathogenesis. J. Infect. Dis. 198:1856-1861.
60. Tschugguel, W., C. Schneeberger, H. Lass, F. Stonek, M. B. Zaghlula, K. Czerwenka, C. Schatten, A. Kaider, P. Husslein, and J. C. Huber. 1999. Human cervical ripening is associated with an increase in cervical inducible nitric oxide synthase expression. Biol. Reprod. 60:1367-1372.
61. Turner, S., E. Reid, H. Smith, and J. Cole. 2003. A novel cytochrome c peroxidase from Neisseria gonorrhoeae: a lipoprotein from a gram-negative bacterium. Biochem. J. 373:865-873.
62. Van Alst, N. E., K. F. Picardo, B. H. Iglewski, and C. G. Haidaris. 2007. Nitrate sensing and metabolism modulate motility, biofilm formation, and virulence in Pseudomonas aeruginosa. Infect. Immun. 75:3780-3790.
63. Wang, S. A., A. B. Harvey, S. M. Conner, A. A. Zaidi, J. S. Knapp, W. L. Whittington, C. del Rio, F. N. Judson, and K. K. Holmes. 2007. Antimicrobial resistance for Neisseria gonorrhoeae in the United States, 1988 to 2003: the spread of fluoroquinolone resistance. Ann. Intern. Med. 147:81-88.
64. Wang, W., L. Reitzer, D. A. Rasko, M. M. Pearson, R. J. Blick, C. Laurence, and E. J. Hansen. 2007. Metabolic analysis of Moraxella catarrhalis and the effect of selected in vitro growth conditions on global gene expression. Infect. Immun. 75:4959-4971.
65. Yagi, T., S. Di Bernardo, E. Nakamuro-Ogiso, M. C. Kao, B. B. Seo, and A. Matsuno-Yagi. 2004. NADH dehydrogenases (NADH:quinone oxidoreductase), p. 15-40. In D. Zannoni (ed.), Respiration in archaea and bacteria, vol. 2. Kluwer Publishing, Dordrecht, The Netherlands.
66. Yoon, S. S., R. F. Hennigan, G. M. Hilliard, U. A. Ochsner, K. Parvatiyar, M. C. Kamani, H. L. Allen, T. R. DeKievit, P. R. Gardner, U. Schwab, J. J. Rowe, B. H. Iglewski, T. R. McDermott, R. P. Mason, D. J. Wozniak, R. E. Hancock, M. R. Parsek, T. L. Noah, R. C. Boucher, and D. J. Hassett. 2002. Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. Dev. Cell 3:593-603.
67. 2-producing lactobacilli on Neisseria gonorrhoeae growth and catalase activity. J. Infect. Dis. 170:1209-1215.
68. Zumft, W. G. 1997. Cell biology and molecular basis of denitrification. Microbiol. Mol. Biol. Rev. 61:533-616.