Beyond the crystal structure: Insight into the function and vaccine potential of TbpA expressed by Neisseria gonorrhoeae

Infection and Immunity

Volumn 83, Issue 11, 2015, Pages 4438-4449

  Cash, Devin R ^a   Noinaj, Nicholas ^b,c   Buchanan, Susan K ^b   Cornelissen, Cynthia Nau ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL VACCINE; IRON; NEISSERIA GONORRHOEAE VACCINE; TRANSFERRIN BINDING PROTEIN A; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; PROTEIN BINDING; TRANSFERRIN;

ARTICLE; BACTERIAL STRAIN; CRYSTAL STRUCTURE; GONORRHEA; IRON TRANSPORT; LIGAND BINDING; MUTAGENESIS; MUTANT; NEISSERIA GONORRHOEAE; NEISSERIACEAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MICROBIOLOGY; PROTEIN SECONDARY STRUCTURE;

BACTERIAL PROTEINS; BACTERIAL VACCINES; GONORRHEA; HUMANS; NEISSERIA GONORRHOEAE; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; TRANSFERRIN; TRANSFERRIN-BINDING PROTEIN A;

EID: 84947599881     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00762-15     Document Type: Article

References (49)

1. Walker CK, Sweet RL. 2011. Gonorrhea infection in women: prevalence, effects, screening, and management. Int J Womens Health 3:197-206.
2. World Health Organization. 2008. Global incidence and prevalence of selected curable sexually transmitted infections-2008. World Health Organization, Geneva, Switzerland. http://apps.who.int/iris/bitstream/10665/75181/1/9789241503839_eng.pdf.
3. Centers for Disease Control and Prevention (CDC). 2011. Cephalosporin susceptibility among Neisseria gonorrhoeae isolates-United States, 2000-2010. MMWR Morb Mortal Wkly Rep 60:873-877.
4. Liu Y, Feinen B, Russell MW. 2011. New concepts in immunity to Neisseria gonorrhoeae: innate responses and suppression of adaptive immunity favor the pathogen, not the host. Front Microbiol 2:52.
5. Farley TA, Cohen DA, Elkins W. 2003. Asymptomatic sexually transmitted diseases: the case for screening. Prev Med 36:502-509. http://dx.doi.org/10.1016/S0091-7435(02)00058-0.
6. Centers for Disease Control and Prevention (CDC). 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.
7. 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. http://dx.doi.org/10.1128/AAC.00325-11.
8. Ohnishi M, Saika T, Hoshina S, Iwasaku K, Nakayama S, Watanabe H, Kitawaki J. 2011. Ceftriaxone-resistant Neisseria gonorrhoeae, Japan. Emerg Infect Dis 17:148-149. http://dx.doi.org/10.3201/eid1701.100397.
9. Unemo M, Golparian D, Nicholas R, Ohnishi M, Gallay A, Sednaoui P.2012. High-level cefixime-and ceftriaxone-resistant Neisseria gonorrhoeae in France: novel penA mosaic allele in a successful international clone causes treatment failure. Antimicrob Agents Chemother 56:1273-1280. http://dx.doi.org/10.1128/AAC.05760-11.
10. Cámara J, Serra J, Ayats J, Bastida T, Carnicer-Pont D, Andreu A, Ardanuy C. 2012. Molecular characterization of two high-level ceftriaxone-resistant Neisseria gonorrhoeae isolates detected in Catalonia, Spain. J Antimicrob Chemother 67:1858-1860. http://dx.doi.org/10.1093/jac/dks162.
11. Lahra MM, Ryder N, Whiley DM. 2014. A new multidrug-resistant strain of Neisseria gonorrhoeae in Australia. N Engl J Med 371:1850-1851. http://dx.doi.org/10.1056/NEJMc1408109.
12. Briat JF. 1992. Iron assimilation and storage in prokaryotes. J Gen Microbiol 138:2475-2483. http://dx.doi.org/10.1099/00221287-138-12-2475.
13. Neilands JB. 1981. Microbial iron compounds. Annu Rev Biochem 50: 715-731. http://dx.doi.org/10.1146/annurev.bi.50.070181.003435.
14. Cornelissen CN, Hollander A. 2011. TonB-dependent transporters expressed by Neisseria gonorrhoeae. Front Microbiol 2:117.
15. Cornelissen CN. 2008. Identification and characterization of gonococcal iron transport systems as potential vaccine antigens. Future Microbiol 3:287-298. http://dx.doi.org/10.2217/17460913.3.3.287.
16. Mickelsen PA, Blackman E, Sparling PF. 1982. Ability of Neisseria gonorrhoeae, Neisseria meningitidis, and commensal Neisseria species to obtain iron from lactoferrin. Infect Immun 35:915-920.
17. Biswas GD, Anderson JE, Sparling PF. 1997. Cloning and functional characterization of Neisseria gonorrhoeae tonB, exbB and exbD genes. Mol Microbiol 24:169-179.
18. Anderson JE, Leone PA, Miller WC, Chen C, Hobbs MM, Sparling PF. 2001. Selection for expression of the gonococcal hemoglobin receptor during menses. J Infect Dis 184:1621-1623. http://dx.doi.org/10.1086/324564.
19. Noinaj N, Buchanan SK, Cornelissen CN. 2012. The transferrin-iron import system from pathogenic Neisseria species. Mol Microbiol 86:246-257. http://dx.doi.org/10.1111/mmi.12002.
20. 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. http://dx.doi.org/10.1046/j.1365-2958.1998.00710.x.
21. 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. http://dx.doi.org/10.1038/nature10823.
22. 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. http://dx.doi.org/10.1038/nsmb.2251.
23. Yost-Daljev MK, Cornelissen CN. 2004. Determination of surfaceexposed, functional domains of gonococcal transferrin-binding protein A. Infect Immun 72:1775-1785. http://dx.doi.org/10.1128/IAI.72.3.1775-1785.2004.
24. Frandoloso R, Martinez-Martinez S, Calmettes C, Fegan J, Costa E, Curran D, Yu RH, Gutierrez-Martin CB, Rodriguez-Ferri EF, Moraes TF, Schryvers AB. 2015. Nonbinding site-directed mutants of transferrin binding protein B exhibit enhanced immunogenicity and protective capabilities. Infect Immun 83:1030-1038. http://dx.doi.org/10.1128/IAI.02572-14.
25. 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.
26. West SE, 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.
27. Arnold K, Bordoli L, Kopp J, Schwede T. 2006. The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22:195-201. http://dx.doi.org/10.1093/bioinformatics/bti770.
28. Masri HP, Cornelissen CN. 2002. Specific ligand binding attributable to individual epitopes of gonococcal transferrin binding protein A. Infect Immun 70:732-740. http://dx.doi.org/10.1128/IAI.70.2.732-740.2002.
29. 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.
30. Blanton KJ, Biswas GD, Tsai J, Adams J, Dyer DW, Davis SM, Koch GG, Sen PK, Sparling PF. 1990. Genetic evidence that Neisseria gonorrhoeae produces specific receptors for transferrin and lactoferrin. J Bacteriol 172:5225-5235.
31. 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.
32. 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.
33. Noto JM, Cornelissen CN. 2008. Identification of TbpA residues required for transferrin-iron utilization by Neisseria gonorrhoeae. Infect Immun 76:1960-1969. http://dx.doi.org/10.1128/IAI.00020-08.
34. DeRocco AJ, Cornelissen CN. 2007. Identification of transferrin-binding domains in TbpB expressed by Neisseria gonorrhoeae. Infect Immun 75: 3220-3232. http://dx.doi.org/10.1128/IAI.00072-07.
35. Cornelissen CN, Anderson JE, Sparling PF. 1997. Energy-dependent changes in the gonococcal transferrin receptor. Mol Microbiol 26:25-35. http://dx.doi.org/10.1046/j.1365-2958.1997.5381914.x.
36. 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.
37. Halbrooks PJ, He QY, Briggs SK, Everse SJ, Smith VC, MacGillivray RT, Mason AB. 2003. Investigation of the mechanism of iron release from the C-lobe of human serum transferrin: mutational analysis of the role of a pH sensitive triad. Biochemistry 42:3701-3707. http://dx.doi.org/10.1021/bi027071q.
38. Cornelissen CN, Anderson JE, Boulton IC, Sparling PF. 2000. Antigenic and sequence diversity in gonococcal transferrin-binding protein A. Infect Immun 68:4725-4735. http://dx.doi.org/10.1128/IAI.68.8.4725-4735.2000.
39. Price GA, Hobbs MM, Cornelissen CN. 2004. Immunogenicity of gonococcal transferrin binding proteins during natural infections. Infect Immun 72:277-283. http://dx.doi.org/10.1128/IAI.72.1.277-283.2004.
40. Price GA, Russell MW, Cornelissen CN. 2005. Intranasal administration of recombinant Neisseria gonorrhoeae transferrin binding proteins A and B conjugated to the cholera toxin B subunit induces systemic and vaginal antibodies in mice. Infect Immun 73:3945-3953. http://dx.doi.org/10.1128/IAI.73.7.3945-3953.2005.
41. Jerse AE, Crow ET, Bordner AN, Rahman I, Cornelissen CN, Moench TR, Mehrazar K. 2002. Growth of Neisseria gonorrhoeae in the female mouse genital tract does not require the gonococcal transferrin or hemoglobin receptors and may be enhanced by commensal lactobacilli. Infect Immun 70:2549-2558. http://dx.doi.org/10.1128/IAI.70.5.2549-2558.2002.
42. 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.
43. Boulton IC, Yost MK, Anderson JE, Cornelissen CN. 2000. Identification of discrete domains within gonococcal transferrin-binding protein A that are necessary for ligand binding and iron uptake functions. Infect Immun 68:6988-6996. http://dx.doi.org/10.1128/IAI.68.12.6988-6996.2000.
44. Masri HP. 2003. Function and immunogenicity of individual epitopes of gonococcal transferrin binding protein A. Ph.D. dissertation Virginia Commonwealth University, Richmond, VA.
45. Hansen JK, Demick KP, Mansfield JM, Forest KT. 2007. Conserved regions from Neisseria gonorrhoeae pilin are immunosilent and not immunosuppressive. Infect Immun 75:4138-4147. http://dx.doi.org/10.1128/IAI.02015-06.
46. Beernink PT, Shaughnessy J, Braga EM, Liu Q, Rice PA, Ram S, Granoff DM. 2011. A meningococcal factor H binding protein mutant that eliminates factor H binding enhances protective antibody responses to vaccination. J Immunol 186:3606-3614. http://dx.doi.org/10.4049/jimmunol.1003470.
47. Rossi R, Granoff DM, Beernink PT. 2013. Meningococcal factor H-binding protein vaccines with decreased binding to human complement factor H have enhanced immunogenicity in human factor H transgenic mice. Vaccine 31:5451-5457. http://dx.doi.org/10.1016/j.vaccine.2013.08.099.
48. Granoff DM, Costa I, Konar M, Giuntini S, Van Rompay KK, Beernink PT. 2015. Binding of complement factor H (FH) decreases protective anti-FH binding protein antibody responses of infant rhesus macaques immunized With a meningococcal serogroup B vaccine. J Infect Dis 212: 784-792. http://dx.doi.org/10.1093/infdis/jiv081.
49. 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.