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image of Superbug Neisseria gonorrhoeae Infections: The Role of the Moonlighting Protein Glutamate Racemase in Treatment and Prevention

Abstract

Introduction

is a notorious superbug responsible for causing ‘Gonorrhoea’ in humans. Recently, it has been classified as a high-priority pathogen by the World Health Organization due to its increasing resistance to available antibiotics. A multi-prolonged approach is needed to combat the growing problem of drug resistance caused by . This study evaluates Glutamate Racemase (GR), a moonlight protein of (-GR), as a novel therapeutic target with potential for both inhibitor design and peptide vaccine development. GR plays a crucial role in the peptidoglycan biosynthetic pathway and is highly conserved across bacterial species. Additionally, this protein moonlights to perform a secondary function by binding to DNA gyrase in various organisms.

Methods

Homology modeling, molecular docking, and molecular dynamics simulations were used to design inhibitors targeting the moonlight function of GR. The immunogenicity of this protein was assessed using ABCPred-2.0, BepiPred-2.0, and ProPred softwares.

Results

Bisleucocurine A was found to bind at the ectopic site of -GR, disrupting its crucial moonlight function and interfering its interaction with DNA Gyrase (gyrase). Interestingly, residues important for its moonlight function were also identified as key immunogenic sites using ABCPred-2.0, BepiPred-2.0, and ProPred softwares, enhancing the potential of this protein as a vaccine candidate.

Conclusion

The GR enzyme’s moonlight function is highlighted as a promising novel target for therapeutic intervention and vaccine development in

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2025-04-23
2025-09-13
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References

  1. Igietseme J.U. Omosun Y. Black C.M. Bacterial sexually transmitted infections (STIs): A clinical overview. Molecular Medical Microbiology Academic Press 2014 1403 1420
    [Google Scholar]
  2. Ahmadi A. Mousavi A. Salimizand H. Hedayati M.A. Ramazanzadeh R. Farhadifar F. Khodabandehloo M. Roshani D. Taherpour A. Prevalence of Neisseria gonorrhoeae in Western Iran. Jpn. J. Infect. Dis. 2022 75 1 JJID.2021.006 10.7883/yoken.JJID.2021.006 34053955
    [Google Scholar]
  3. Unemo M. Lahra M.M. Escher M. Eremin S. Cole M.J. Galarza P. Ndowa F. Martin I. Dillon J.A.R. Galas M. Ramon-Pardo P. Weinstock H. Wi T. WHO global antimicrobial resistance surveillance for Neisseria gonorrhoeae 2017–18: A retrospective observational study. Lancet Microbe 2021 2 11 e627 e636 10.1016/S2666‑5247(21)00171‑3 35544082
    [Google Scholar]
  4. Kreisel K.M. Weston E.J. St Cyr S.B. Spicknall I.H. Estimates of the prevalence and incidence of chlamydia and gonorrhea among US Men and Women, 2018. Sex. Transm. Dis. 2021 48 4 222 231 10.1097/OLQ.0000000000001382 33492094
    [Google Scholar]
  5. Unemo M. Shafer W.M. Antibiotic resistance in Neisseria gonorrhoeae : Origin, evolution, and lessons learned for the future. Ann. N. Y. Acad. Sci. 2011 1230 1 E19 E28 10.1111/j.1749‑6632.2011.06215.x 22239555
    [Google Scholar]
  6. Shaskolskiy B. Kandinov I. Dementieva E. Gryadunov D. Antibiotic resistance in Neisseria gonorrhoeae: Challenges in research and treatment. Microorganisms 2022 10 9 1699 10.3390/microorganisms10091699 36144300
    [Google Scholar]
  7. Klausner J.D. Bristow C.C. Soge O.O. Shahkolahi A. Waymer T. Bolan R.K. Philip S.S. Asbel L.E. Taylor S.N. Mena L.A. Goldstein D.A. Powell J.A. Wierzbicki M.R. Morris S.R. Resistance-guided treatment of gonorrhea: A prospective clinical study. Clin. Infect. Dis. 2021 73 2 298 303 10.1093/cid/ciaa596 32766725
    [Google Scholar]
  8. Boyajian A.J. Murray M. Tucker M. Neu N. Identifying variations in adherence to the CDC sexually transmitted disease treatment guidelines of Neisseria gonorrhoeae. Public Health 2016 136 161 165 10.1016/j.puhe.2016.04.004 27179879
    [Google Scholar]
  9. Rostamian M. Chegene Lorestani R. Jafari S. Mansouri R. Rezaeian S. Ghadiri K. Akya A. A systematic review and meta-analysis on the antibiotic resistance of Neisseria meningitidis in the last 20 years in the world. Indian J. Med. Microbiol. 2022 40 3 323 329 10.1016/j.ijmmb.2022.05.005 35654713
    [Google Scholar]
  10. Rubin D.H.F. Ross J.D.C. Grad Y.H. The frontiers of addressing antibiotic resistance in Neisseria gonorrhoeae. Transl. Res. 2020 220 122 137 10.1016/j.trsl.2020.02.002 32119845
    [Google Scholar]
  11. Sethi S. Golparian D. Bala M. Dorji D. Ibrahim M. Jabeen K. Unemo M. Antimicrobial susceptibility and genetic characteristics of Neisseria gonorrhoeae isolates from India, Pakistan and Bhutan in 2007–2011. BMC Infect. Dis. 2013 13 1 35 10.1186/1471‑2334‑13‑35 23347339
    [Google Scholar]
  12. Jeffery C.J. Why study moonlighting proteins? Front. Genet. 2015 6 211 10.3389/fgene.2015.00211 26150826
    [Google Scholar]
  13. Jeffery C.J. Protein moonlighting: What is it, and why is it important? Philos. Trans. R. Soc. Lond. B Biol. Sci. 2018 373 1738 20160523 10.1098/rstb.2016.0523 29203708
    [Google Scholar]
  14. Jeffery C.J. An introduction to protein moonlighting. Biochem. Soc. Trans. 2014 42 6 1679 1683 10.1042/BST20140226 25399589
    [Google Scholar]
  15. Yadav P. Singh R. Sur S. Bansal S. Chaudhry U. Tandon V. Moonlighting proteins: Beacon of hope in era of drug resistance in bacteria. Crit. Rev. Microbiol. 2023 49 1 57 81 10.1080/1040841X.2022.2036695 35220864
    [Google Scholar]
  16. Henderson B. Martin A. Bacterial moonlighting proteins and bacterial virulence. Curr. Top. Microbiol. Immunol. 2011 358 155 213 10.1007/82_2011_188 22143554
    [Google Scholar]
  17. Mani M. Chen C. Amblee V. Liu H. Mathur T. Zwicke G. Zabad S. Patel B. Thakkar J. Jeffery C.J. MoonProt: A database for proteins that are known to moonlight. Nucleic Acids Res. 2015 43 D1 D277 D282 10.1093/nar/gku954 25324305
    [Google Scholar]
  18. Hernández S. Ferragut G. Amela I. Perez-Pons J. Piñol J. Mozo-Villarias A. Cedano J. Querol E. MultitaskProtDB: A database of multitasking proteins. Nucleic Acids Res. 2014 42 D1 D517 D520 10.1093/nar/gkt1153 24253302
    [Google Scholar]
  19. Ashiuchi M. Kuwana E. Yamamoto T. Komatsu K. Soda K. Misono H. Glutamate racemase is an endogenous DNA gyrase inhibitor. J. Biol. Chem. 2002 277 42 39070 39073 10.1074/jbc.C200253200 12213801
    [Google Scholar]
  20. Fisher S.L. Glutamate racemase as a target for drug discovery. Microb. Biotechnol. 2008 1 5 345 360 10.1111/j.1751‑7915.2008.00031.x 21261855
    [Google Scholar]
  21. Saluja D. Pawar A. Konwar C. Chaudhry U. Chopra M. Jha P. Bactericidal activity of esculetin is associated with impaired cell wall synthesis by targeting glutamate racemase of Neisseria gonorrhoeae. Sexually Transmitted Infections 2021 97 A108 A109 10.1136/sextrans‑2021‑sti.284
    [Google Scholar]
  22. Glavas S. Tanner M.E. Active site residues of glutamate racemase. Biochemistry 2001 40 21 6199 6204 10.1021/bi002703z 11371180
    [Google Scholar]
  23. Sengupta S. Shah M. Nagaraja V. Glutamate racemase from Mycobacterium tuberculosis inhibits DNA gyrase by affecting its DNA-binding. Nucleic Acids Res. 2006 34 19 5567 5576 10.1093/nar/gkl704 17020913
    [Google Scholar]
  24. Mehboob S. Guo L. Fu W. Mittal A. Yau T. Truong K. Johlfs M. Long F. Fung L.W.M. Johnson M.E. Glutamate racemase dimerization inhibits dynamic conformational flexibility and reduces catalytic rates. Biochemistry 2009 48 29 7045 7055 10.1021/bi9005072 19552402
    [Google Scholar]
  25. Rogers H. J. Perkins H. R. Ward J. B. Microbial Cell Walls and Membranes. Springer eBooks 1980 10.1007/978‑94‑011‑6014‑8
    [Google Scholar]
  26. Sengupta S. Nagaraja V. Inhibition of DNA gyrase activity by Mycobacterium smegmatis MurI. FEMS Microbiol. Lett. 2008 279 1 40 47 10.1111/j.1574‑6968.2007.01005.x 18177305
    [Google Scholar]
  27. Khisimuzi Mdluli Zhenkun Ma Mycobacterium tuberculosis DNA gyrase as a target for drug discovery. Infect. Disord. Drug Targets 2007 7 2 159 168 10.2174/187152607781001763 17970226
    [Google Scholar]
  28. Doublet P. van Heijenoort J. Bohin J.P. Mengin-Lecreulx D. The murI gene of Escherichia coli is an essential gene that encodes a glutamate racemase activity. J. Bacteriol. 1993 175 10 2970 2979 10.1128/jb.175.10.2970‑2979.1993 8098327
    [Google Scholar]
  29. Chen M.Y. McNulty A. Avery A. Whiley D. Tabrizi S.N. Hardy D. Das A.F. Nenninger A. Fairley C.K. Hocking J.S. Bradshaw C.S. Donovan B. Howden B.P. Oldach D. Solitaire-U Team Solithromycin versus ceftriaxone plus azithromycin for the treatment of uncomplicated genital gonorrhoea (SOLITAIRE-U): A randomised phase 3 non-inferiority trial. Lancet Infect. Dis. 2019 19 8 833 842 10.1016/S1473‑3099(19)30116‑1 31196813
    [Google Scholar]
  30. Taylor S.N. Marrazzo J. Batteiger B.E. Hook E.W. III Seña A.C. Long J. Wierzbicki M.R. Kwak H. Johnson S.M. Lawrence K. Mueller J. Single-dose zoliflodacin (ETX0914) for treatment of Urogenital Gonorrhea. N. Engl. J. Med. 2018 379 19 1835 1845 10.1056/NEJMoa1706988 30403954
    [Google Scholar]
  31. Taylor S.N. Morris D.H. Avery A.K. Workowski K.A. Batteiger B.E. Tiffany C.A. Perry C.R. Raychaudhuri A. Scangarella-Oman N.E. Hossain M. Dumont E.F. Gepotidacin for the treatment of uncomplicated urogenital gonorrhea: A phase 2, randomized, doseranging, single-oral dose evaluation. Clin. Infect. Dis. 2018 67 4 504 512 10.1093/cid/ciy145 29617982
    [Google Scholar]
  32. Williams E. Fairley C.K. Williamson D. Novel strategies for prevention and treatment of antimicrobial resistance in sexually-transmitted infections. Curr. Opin. Infect. Dis. 2021 34 6 591 598 10.1097/QCO.0000000000000793 34545855
    [Google Scholar]
  33. Cabral M.P. García P. Beceiro A. Rumbo C. Pérez A. Moscoso M. Bou G. Design of live attenuated bacterial vaccines based on D-glutamate auxotrophy. Nat. Commun. 2017 8 1 15480 10.1038/ncomms15480 28548079
    [Google Scholar]
  34. Pawar A. Jha P. Chopra M. Chaudhry U. Saluja D. Screening of natural compounds that targets glutamate racemase of Mycobacterium tuberculosis reveals the anti-tubercular potential of flavonoids. Sci. Rep. 2020 10 1 949 10.1038/s41598‑020‑57658‑8 31969615
    [Google Scholar]
  35. Pawar A. Jha P. Konwar C. Chaudhry U. Chopra M. Saluja D. Ethambutol targets the glutamate racemase of Mycobacterium tuberculosis—an enzyme involved in peptidoglycan biosynthesis. Appl. Microbiol. Biotechnol. 2019 103 2 843 851 10.1007/s00253‑018‑9518‑z 30456576
    [Google Scholar]
  36. Berman H.M. Kleywegt G.J. Nakamura H. Markley J.L. The protein data bank archive as an open data resource. J. Comput. Aided Mol. Des. 2014 28 10 1009 1014 10.1007/s10822‑014‑9770‑y 25062767
    [Google Scholar]
  37. Apweiler R. UniProt: The universal protein knowledgebase. Nucleic Acids Res 2004 32 10.1093/nar/gky092
    [Google Scholar]
  38. Waterhouse A. Bertoni M. Bienert S. Studer G. Tauriello G. Gumienny R. Heer F.T. de Beer T.A.P. Rempfer C. Bordoli L. Lepore R. Schwede T. SWISS-MODEL: Homology modelling of protein structures and complexes. Nucleic Acids Res. 2018 46 W1 W296 W303 10.1093/nar/gky427 29788355
    [Google Scholar]
  39. Laskowski R.A. MacArthur M.W. Moss D.S. Thornton J.M. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Cryst. 1993 26 2 283 291 10.1107/S0021889892009944
    [Google Scholar]
  40. Colovos C. Yeates T.O. Verification of protein structures: Patterns of nonbonded atomic interactions. Protein Sci. 1993 2 9 1511 1519 10.1002/pro.5560020916 8401235
    [Google Scholar]
  41. Yan Y. Tao H. He J. Huang S.Y. The HDOCK server for integrated protein–protein docking. Nat. Protoc. 2020 15 5 1829 1852 10.1038/s41596‑020‑0312‑x 32269383
    [Google Scholar]
  42. Trott O. Olson A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2010 31 2 455 461 10.1002/jcc.21334 19499576
    [Google Scholar]
  43. Irwin J.J. Shoichet B.K. ZINC--a free database of commercially available compounds for virtual screening. J. Chem. Inf. Model. 2005 45 1 177 182 10.1021/ci049714+ 15667143
    [Google Scholar]
  44. Daina A. Michielin O. Zoete V. SwissADME: A free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci. Rep. 2017 7 1 42717 10.1038/srep42717 28256516
    [Google Scholar]
  45. Release S. Research D.E.S. Desmond Molecular. Dyn. Syst. 2019
    [Google Scholar]
  46. Barh D. Misra A.N. Kumar A. Azevedo V. A novel strategy of epitope design in Neisseria gonorrhoeae. Bioinformation 2010 5 2 77 82 10.6026/97320630005077 21346868
    [Google Scholar]
  47. Bateman A. UniProt Consortium UniProt: A worldwide hub of protein knowledge. Nucleic Acids Res. 2019 47 D1 D506 D515 10.1093/nar/gky1049 30395287
    [Google Scholar]
  48. Saha S. Raghava G.P.S. Prediction of continuous B‐cell epitopes in an antigen using recurrent neural network. Proteins 2006 65 1 40 48 10.1002/prot.21078 16894596
    [Google Scholar]
  49. Jespersen M.C. Peters B. Nielsen M. Marcatili P. BepiPred-2.0: Improving sequence-based B-cell epitope prediction using conformational epitopes. Nucleic Acids Res. 2017 45 W1 W24 W29 10.1093/nar/gkx346 28472356
    [Google Scholar]
  50. Doytchinova I.A. Flower D.R. VaxiJen: A server for prediction of protective antigens, tumour antigens and subunit vaccines. BMC Bioinformatics 2007 8 1 4 10.1186/1471‑2105‑8‑4 17207271
    [Google Scholar]
  51. Singh H. Raghava G.P.S. ProPred1: Prediction of promiscuous MHC Class-I binding sites. Bioinformatics 2003 19 8 1009 1014 10.1093/bioinformatics/btg108 12761064
    [Google Scholar]
  52. Sturniolo T. Bono E. Ding J. Raddrizzani L. Tuereci O. Sahin U. Braxenthaler M. Gallazzi F. Protti M.P. Sinigaglia F. Hammer J. Generation of tissue-specific and promiscuous HLA ligand databases using DNA microarrays and virtual HLA class II matrices. Nat. Biotechnol. 1999 17 6 555 561 10.1038/9858 10385319
    [Google Scholar]
  53. Singh H. Raghava G.P.S. ProPred: Prediction of HLA-DR binding sites. Bioinformatics 2001 17 12 1236 1237 10.1093/bioinformatics/17.12.1236 11751237
    [Google Scholar]
  54. Luo H. Lin Y. Gao F. Zhang C.T. Zhang R. DEG 10, an update of the database of essential genes that includes both protein-coding genes and noncoding genomic elements: Table 1. Nucleic Acids Res. 2014 42 D1 D574 D580 10.1093/nar/gkt1131 24243843
    [Google Scholar]
  55. Altschul S.F. Gish W. Miller W. Myers E.W. Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990 215 3 403 410 10.1016/S0022‑2836(05)80360‑2 2231712
    [Google Scholar]
  56. Corpet F. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 1988 16 22 10881 10890 10.1093/nar/16.22.10881 2849754
    [Google Scholar]
  57. Cho Y. Hwang K.Y. Cho C-S. Kim S.S. Sung H-C. Yu Y.G. Structure and mechanism of glutamate racemase from Aquifex pyrophilus. Nat. Struct. Biol. 1999 6 5 422 426 10.1038/8223 10331867
    [Google Scholar]
  58. Ruzheinikov S.N. Taal M.A. Sedelnikova S.E. Baker P.J. Rice D.W. Substrate-induced conformational changes in Bacillus subtilis glutamate racemase and their implications for drug discovery. Structure 2005 13 11 1707 1713 10.1016/j.str.2005.07.024 16271894
    [Google Scholar]
  59. Wiederstein M. Sippl M.J. ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Res. 2007 35 Web Server W407 W410 10.1093/nar/gkm290 17517781
    [Google Scholar]
  60. WHO WHO guidelines for the treatment of Neisseria gonorrhoeae. World Health Organization Geneva 2016
    [Google Scholar]
  61. Workowski K.A. Bachmann L.H. Chan P.A. Johnston C.M. Muzny C.A. Park I. Reno H. Zenilman J.M. Bolan G.A. Sexually transmitted infections treatment guidelines, 2021. MMWR Recomm. Rep. 2021 70 4 1 187 10.15585/mmwr.rr7004a1 34292926
    [Google Scholar]
  62. Trajanoska K. Bhérer C. Taliun D. Zhou S. Richards J.B. Mooser V. From target discovery to clinical drug development with human genetics. Nature 2023 620 7975 737 745 10.1038/s41586‑023‑06388‑8 37612393
    [Google Scholar]
  63. Zhang Y. Hu C. Anticancer activity of bisindole alkaloids derived from natural sources and synthetic bisindole hybrids. Arch. Pharm. 2020 353 9 2000092 10.1002/ardp.202000092 32468606
    [Google Scholar]
  64. Kim M.Y. Sohn J.H. Ahn J.S. Oh H. Alternaramide, a cyclic depsipeptide from the marine-derived fungus Alternaria sp. SF-5016. J. Nat. Prod. 2009 72 11 2065 2068 10.1021/np900464p 19943624
    [Google Scholar]
  65. Ko W. Sohn J.H. Jang J.H. Ahn J.S. Kang D.G. Lee H.S. Kim J.S. Kim Y.C. Oh H. Inhibitory effects of alternaramide on inflammatory mediator expression through TLR4-MyD88-mediated inhibition of NF-кB and MAPK pathway signaling in lipopolysaccharide-stimulated RAW264.7 and BV2 cells. Chem. Biol. Interact. 2016 244 16 26 10.1016/j.cbi.2015.11.024 26620692
    [Google Scholar]
  66. Forgue S.T. Patterson B.E. Bedding A.W. Payne C.D. Phillips D.L. Wrishko R.E. Mitchell M.I. Tadalafil pharmacokinetics in healthy subjects. Br. J. Clin. Pharmacol. 2006 61 3 280 288 10.1111/j.1365‑2125.2005.02553.x 16487221
    [Google Scholar]
  67. Camilleri M. Hale M. Morlion B. Tack J. Webster L. Wild J. Naldemedine improves patient-reported outcomes of opioid-induced constipation in patients with chronic non-cancer pain in the compose phase 3 studies. J. Pain Res. 2021 14 2179 2189 10.2147/JPR.S282738 34295186
    [Google Scholar]
  68. Wild J. Webster L. Yamada T. Hale M. Safety and efficacy of naldemedine for the treatment of opioid-induced constipation in patients with chronic non-cancer pain receiving opioid therapy: A subgroup analysis of patients ≥ 65 years of age. Drugs Aging 2020 37 4 271 279 10.1007/s40266‑020‑00753‑2 32086791
    [Google Scholar]
  69. Hollingsworth S.A. Dror R.O. Molecular dynamics simulation for all. Neuron 2018 99 6 1129 1143 10.1016/j.neuron.2018.08.011 30236283
    [Google Scholar]
  70. Rich R.L. Myszka D.G. Survey of the 1999 surface plasmon resonance biosensor literature. J. Mol. Recognit. 2000 13 6 388 407 10.1002/1099‑1352(200011/12)13:6<388::AID‑JMR516>3.0.CO;2‑# 11114072
    [Google Scholar]
  71. Bastos M. Velazquez-Campoy A. Isothermal titration calorimetry (ITC): A standard operating procedure (SOP). Eur. Biophys. J. 2021 50 3-4 363 371 10.1007/s00249‑021‑01509‑5 33665758
    [Google Scholar]
  72. Fuchs P.C. Barry A.L. Brown S.D. In vitro activities of ertapenem (MK-0826) against clinical bacterial isolates from 11 North American medical centers. Antimicrob. Agents Chemother. 2001 45 6 1915 1918 10.1128/AAC.45.6.1915‑1918.2001 11353653
    [Google Scholar]
  73. Unemo M. Golparian D. Eyre D.W. Antimicrobial resistance in Neisseria gonorrhoeae and treatment of gonorrhea. Methods Mol Biol. 2019 1997 37 58 10.1007/978‑1‑4939‑9496‑0_3
    [Google Scholar]
  74. Comas I. Chakravartti J. Small P.M. Galagan J. Niemann S. Kremer K. Ernst J.D. Gagneux S. Human T cell epitopes of Mycobacterium tuberculosis are evolutionarily hyperconserved. Nat. Genet. 2010 42 6 498 503 10.1038/ng.590 20495566
    [Google Scholar]
  75. Lindestam Arlehamn C.S. Paul S. Mele F. Huang C. Greenbaum J.A. Vita R. Sidney J. Peters B. Sallusto F. Sette A. Immunological consequences of intragenus conservation of Mycobacterium tuberculosis T-cell epitopes. Proc. Natl. Acad. Sci. USA 2015 112 2 E147 E155 10.1073/pnas.1416537112 25548174
    [Google Scholar]
  76. Pizza M. Scarlato V. Masignani V. Giuliani M.M. Aricò B. Comanducci M. Jennings G.T. Baldi L. Bartolini E. Capecchi B. Galeotti C.L. Luzzi E. Manetti R. Marchetti E. Mora M. Nuti S. Ratti G. Santini L. Savino S. Scarselli M. Storni E. Zuo P. Broeker M. Hundt E. Knapp B. Blair E. Mason T. Tettelin H. Hood D.W. Jeffries A.C. Saunders N.J. Granoff D.M. Venter J.C. Moxon E.R. Grandi G. Rappuoli R. Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 2000 287 5459 1816 1820 10.1126/science.287.5459.1816 10710308
    [Google Scholar]
  77. Seib K.L. Brunelli B. Brogioni B. Palumbo E. Bambini S. Muzzi A. DiMarcello F. Marchi S. van der Ende A. Aricó B. Savino S. Scarselli M. Comanducci M. Rappuoli R. Giuliani M.M. Pizza M. Characterization of diverse subvariants of the meningococcal factor H (fH) binding protein for their ability to bind fH, to mediate serum resistance, and to induce bactericidal antibodies. Infect. Immun. 2011 79 2 970 981 10.1128/IAI.00891‑10 21149595
    [Google Scholar]
  78. Abara W.E. Bernstein K.T. Lewis F.M.T. Schillinger J.A. Feemster K. Pathela P. Hariri S. Islam A. Eberhart M. Cheng I. Ternier A. Slutsker J.S. Mbaeyi S. Madera R. Kirkcaldy R.D. Effectiveness of a serogroup B outer membrane vesicle meningococcal vaccine against gonorrhoea: A retrospective observational study. Lancet Infect. Dis. 2022 22 7 1021 1029 10.1016/S1473‑3099(21)00812‑4 35427490
    [Google Scholar]
  79. Bruxvoort K.J. Lewnard J.A. Chen L.H. Tseng H.F. Chang J. Veltman J. Marrazzo J. Qian L. Prevention of Neisseria gonorrhoeae with meningococcal B vaccine: A matched cohort study in Southern California. Clin. Infect. Dis. 2023 76 3 e1341 e1349 10.1093/cid/ciac436 35642527
    [Google Scholar]
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