Conserved regions of gonococcal TbpB are critical for surface exposure and transferrin iron utilization

Infection and Immunity

Volumn 81, Issue 9, 2013, Pages 3442-3450

  Ostberg, Karen L ^a   DeRocco, Amanda J ^a,b   Mistry, Shreni D ^a   Dickinson, Mary Kathryne ^a   Cornelissen, Cynthia Nau ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

^b UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSFERRIN; TRANSFERRIN BINDING PROTEIN B;

ARTICLE; BACTERIAL GROWTH; BACTERIAL MEMBRANE; BACTERIAL OUTER MEMBRANE; BACTERIAL STRAIN; CELL MEMBRANE; CROSS LINKING; CYTOPLASM; DNA SEQUENCE; GENE EXPRESSION; INTERNALIZATION; IRON METABOLISM; IRON TRANSPORT; NEISSERIA GONORRHOEAE; NONHUMAN; PHENOTYPE; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS;

EID: 84884219205     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00280-13     Document Type: Article

References (42)

1. Centers for Disease Control and Prevention. 2011. Sexually transmitted disease surveillance 2010. U.S. Department of Health and Human Services, Atlanta, GA.
2. Barlow D, Phillips I. 1978. Gonorrhoea in women. Diagnostic, clinical, and laboratory aspects. Lancet i:761-764.
3. McCormack WM, Stumacher RJ, Johnson K, Donner A. 1977. Clinical spectrum of gonococcal infection in women. Lancet i:1182-1185.
4. Holmes KK, Counts GW, Beaty HN. 1971. Disseminated gonococcal infection. Ann. Intern. Med. 74:979-993.
5. Sparling PF. 1990. Biology of Neisseria gonorrhoeae, p 131-138. In Holmes KK, Mardh P-A,, Sparling PF, Weisner PJ (ed), Sexually transmitted diseases, 2nd ed. McGraw Hill, New York, NY.
6. Westrom L. 1980. Incidence, prevalence, and trends of acute pelvic inflammatory disease and its consequences in industrialized countries. Am. J. Obstet. Gynecol. 138:880-892.
7. Cohen MS, Hoffman IF, Royce RA, Kazembe P, Dyer JR, Daly CC, Zimba D, Vernazza PL, Maida M, Fiscus SA, Eron JJ, AIDSCAP Malawi Research Group. 1997. Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. Lancet 349:1868-1873.
8. McClelland RS, Wang CC, Mandaliya K, Overbaugh J, Reiner MT, PenteleeffDD, Lavreys L, Ndinya-Achola J, Bwayo JJ, Kreiss JK. 2001. Treatment of cervicitis is associated with decreased cervical shedding of HIV-1. AIDS 15:105-110.
9. Ohnishi M, Golparian D, Shimuta K, Saika T, Hoshina S, Iwasaku K, Nakayama S, Kitawaki J, Unemo M. 2011. 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.
10. Unemo M, Shafer WM. 2011. Antibiotic resistance in Neisseria gonorrhoeae: origin, evolution, and lessons learned for the future. Ann. N. Y. Acad. Sci. 1230:E19-28.
11. Cornelissen CN, Hollander A. 2011. TonB-dependent transporters expressed by N. gonorrhoeae. Front. Microbiol. 2:117. doi:10.3389/fmicb.2011.00117.
12. Cornelissen CN, Anderson JE, Boulton IC, Sparling PF. 2000. Antigenic and sequence diversity in gonococcal transferrin-binding protein A (TbpA). Infect. Immun. 68:4725-4735.
13. Cornelissen CN, Anderson JE, Sparling PF. 1997. Characterization of the diversity and the transferrin-binding domain of gonococcal transferrinbinding protein 2. Infect. Immun. 65:822-828.
14. Mickelsen PA, Sparling PF. 1981. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from transferrin and iron compounds. Infect. Immun. 33:555-564.
15. Cornelissen CN, Kelley M, Hobbs MM, Anderson JE, Cannon JG, Cohen MS, Sparling PF. 1998. The transferrin receptor expressed by gonococcal strain FA1090 is required for the experimental infection of human male volunteers. Mol. Microbiol. 27:611-616.
16. Anderson JE, Sparling PF, Cornelissen CN. 1994. Gonococcal transferrin-binding protein 2 facilitates but is not essential for transferrin utilization. J. Bacteriol. 176:3162-3170.
17. Cornelissen CN, Biswas GD, Tsai J, Paruchuri DK, Thompson SA, Sparling PF. 1992. Gonococcal transferrin-binding protein 1 is required for transferrin utilization and is homologous to TonB-dependent outer membrane receptors. J. Bacteriol. 174:5788-5797.
18. Noinaj N, Buchanan SK, Cornelissen CN. 2012. The transferrin-iron import system from pathogenic Neisseria species. Mol. Microbiol. 86:246-257.
19. Cornelissen CN, Anderson JE, Sparling PF. 1997. Energy-dependent changes in the gonococcal transferrin receptor. Mol. Microbiol. 26:25-35.
20. Cornelissen CN, Sparling PF. 1996. Binding and surface exposure characteristics of the gonococcal transferrin receptor are dependent on both transferrin-binding proteins. J. Bacteriol. 178:1437-1444.
21. Hayashi S, Wu HC. 1990. Lipoproteins in bacteria. J. Bioenerg. Biomembr. 22:451-471.
22. Yamaguchi K, Yu F, Inouye M. 1988. A single amino acid determinant of the membrane localization of lipoproteins in E. coli. Cell 53:423-432.
23. Kellogg DS, Jr, Peacock WL, Jr, Deacon WE, Brown L, Pirkle CI. 1963. Neisseria gonorrhoeae. I. Virulence genetically linked to clonal variation. J. Bacteriol. 85:1274-1279.
24. West SEH, Sparling PF. 1987. Aerobactin utilization by Neisseria gonorrhoeae and cloning of a genomic DNA fragment that complements Escherichia coli fhuB mutations. J. Bacteriol. 169:3414-3421.
25. Horton RM, Cai ZL, Ho SN, Pease LR. 1990. Gene splicing by overlap extension: tailor-made genes using the polymerase chain reaction. Biotechniques 8:528-535.
26. Elkins C, Thomas CE, Seifert HS, Sparling PF. 1991. Species-specific uptake of DNA by gonococci is mediated by a 10-base-pair sequence. J. Bacteriol. 173:3911-3913.
27. Yost-Daljev MK, Cornelissen CN. 2004. Determination of surfaceexposed, functional domains of gonococcal transferrin-binding protein A. Infect. Immun. 72:1775-1785.
28. Kenney CD, Cornelissen CN. 2002. Demonstration and characterization of a specific interaction between gonococcal transferrin binding protein A and TonB. J. Bacteriol. 184:6138-6145.
29. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
30. Thomas CE, Zhu W, Dam CNV, Davis NL, Johnson RE, Sparling PF. 2006. Vaccination of mice with gonococcal TbpB expressed in vivo from Venezuelan Equine Encephalitis viral replicon particles. Infect. Immun. 74:1612-1620.
31. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9:671-675.
32. Cornelissen CN. 2008. Identification and characterization of gonococcal iron transport systems as potential vaccine antigens. Future Microbiol. 3:287-298.
33. Moraes TF, Yu RH, Strynadka NC, Schryvers AB. 2009. Insights into the bacterial transferrin receptor: the structure of transferrin-binding protein B from Actinobacillus pleuropneumoniae. Mol. Cell 35:523-533.
34. Noinaj N, Easley NC, Oke M, Mizuno N, Gumbart J, Boura E, Steere AN, Zak O, Aisen P, Tajkhorshid E, Evans RW, Gorringe AR, Mason AB, Steven AC, Buchanan SK. 2012. Structural basis for iron piracy by pathogenic Neisseria. Nature 483:53-58.
35. DeRocco AJ, Cornelissen CN. 2007. Identification of transferrin-binding domains in TbpB expressed by Neisseria gonorrhoeae. Infect. Immun. 75:3220-3232.
36. Coutte L, Willery E, Antoine R, Drobecq H, Locht C, Jacob-Dubuisson F. 2003. Surface anchoring of bacterial subtilisin important for maturation function. Mol. Microbiol. 49:529-539.
37. d'Enfert C, Ryter A, Pugsley AP. 1987. Cloning and expression in Escherichia coli of the Klebsiella pneumoniae genes for production, surface localization and secretion of the lipoprotein pullulanase. EMBO J. 6:3531-3538.
38. Haake DA. 2000. Spirochaetal lipoproteins and pathogenesis. Microbiology 146:1491-1504.
39. Tokuda H, Matsuyama S. 2004. Sorting of lipoproteins to the outer membrane in E. coli. Biochim. Biophys. Acta 1694:5-13.
40. Fuller CA, Yu RH, Irwin SW, Schryvers AB. 1998. Biochemical evidence for a conserved interaction between bacterial transferrin binding protein A and transferrin binding protein B. Microb. Pathog. 24:75-87.
41. Calmettes C, Alcantara J, Yu RH, Schryvers AB, Moraes TF. 2012. The structural basis of transferrin sequestration by transferrin-binding protein B. Nat. Struct. Mol. Biol. 19:358-360.
42. Yang X, Yu RH, Calmettes C, Moraes TF, Schryvers AB. 2011. Anchor peptide of transferrin-binding protein B is required for interaction with transferrin-binding protein A. J. Biol. Chem. 286:45165-45173.