{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,10]],"date-time":"2026-09-10T00:08:14Z","timestamp":1788998894572,"version":"build-2803163510"},"reference-count":65,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2022,2,7]],"date-time":"2022-02-07T00:00:00Z","timestamp":1644192000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Zuoying Armed Forces General Hospital","award":["KAFGH-ZY-A-109011"],"award-info":[{"award-number":["KAFGH-ZY-A-109011"]}]},{"name":"NSYSU-KMU JOINT RESEARCH PROJECT","award":["NSYSUKMU 111-I06"],"award-info":[{"award-number":["NSYSUKMU 111-I06"]}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["AI123340 and AI141894"],"award-info":[{"award-number":["AI123340 and AI141894"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Gonorrhea is the second most common sexually transmitted infection, which is primarily localized but can be disseminated systemically. The mechanisms by which a localized infection becomes a disseminated infection are unknown. We used five pairs of Neisseria gonorrhoeae isolates from the cervix\/urethra (localized) and the blood (disseminated) of patients with disseminated gonococcal infection to examine the mechanisms that confine gonococci to the genital tract or enable them to disseminate to the blood. Multilocus sequence analysis found that the local and disseminated isolates from the same patients were isogenic. When culturing in vitro, disseminated isolates aggregated significantly less and transmigrated across a polarized epithelial monolayer more efficiently than localized isolates. While localized cervical isolates transmigrated across epithelial monolayers inefficiently, those transmigrated bacteria self-aggregated less and transmigrated more than cervical isolates but comparably to disseminating isolates. The local cervical isolates recruited the host receptors of gonococcal Opa proteins carcinoembryonic antigen-related cell adhesion molecules (CEACAMs) on epithelial cells. However, the transmigrated cervical isolate and the disseminated blood isolates recruit CEACAMs significantly less often. Our results collectively suggest that switching off the expression of CEACAM-binding Opa(s), which reduces self-aggregation, promotes gonococcal dissemination.<\/jats:p>","DOI":"10.3390\/pathogens11020217","type":"journal-article","created":{"date-parts":[[2022,2,7]],"date-time":"2022-02-07T08:38:48Z","timestamp":1644223128000},"page":"217","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["In Vitro Analysis of Matched Isolates from Localized and Disseminated Gonococcal Infections Suggests That Opa Expression Impacts Clinical Outcome"],"prefix":"10.3390","volume":"11","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3045-6669","authenticated-orcid":false,"given":"Cheng-Tai","family":"Wu","sequence":"first","affiliation":[{"name":"Department of Marine Biotechnology and Resources, National Sun Yat-Sen University, Kaohsiung 804, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Po-Wei","family":"Huang","sequence":"additional","affiliation":[{"name":"Division of Urology, Department of Surgery, Zuoying Branch of Kaohsiung Armed Forces General Hospital, Kaohsiung 813, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chia-Hsuan","family":"Lin","sequence":"additional","affiliation":[{"name":"Department of Marine Biotechnology and Resources, National Sun Yat-Sen University, Kaohsiung 804, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel C.","family":"Stein","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Molecular Genetics, University of Maryland, College Park 20742, MD, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wenxia","family":"Song","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Molecular Genetics, University of Maryland, College Park 20742, MD, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sung-Pin","family":"Tseng","sequence":"additional","affiliation":[{"name":"Department of Medical Laboratory Science and Biotechnology, Kaohsiung Medical University, Kaohsiung 807, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4977-4256","authenticated-orcid":false,"given":"Liang-Chun","family":"Wang","sequence":"additional","affiliation":[{"name":"Department of Marine Biotechnology and Resources, National Sun Yat-Sen University, Kaohsiung 804, Taiwan"},{"name":"Department of Cell Biology and Molecular Genetics, University of Maryland, College Park 20742, MD, USA"},{"name":"Department of Medical Laboratory Science and Biotechnology, Kaohsiung Medical University, Kaohsiung 807, Taiwan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,2,7]]},"reference":[{"key":"ref_1","unstructured":"CDC (2017, October 05). Gonorrhea\u2013CDC Fact Sheet (Detailed Version), Available online: http:\/\/www.cdc.gov\/std\/gonorrhea\/STDFact-gonorrhea-detailed.htm."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Heijer, C.D.J.D., Hoebe, C.J.P.A., Van Liere, G.A.F.S., Van Bergen, J.E.A.M., Cals, J.W.L., Stals, F.S., and Dukers-Muijrers, N.H.T.M. (2017). A comprehensive overview of urogenital, anorectal and oropharyngeal Neisseria gonorrhoeae testing and diagnoses among different STI care providers: A cross-sectional study. BMC Infect. Dis., 17.","DOI":"10.1186\/s12879-017-2402-0"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"634","DOI":"10.1016\/S0022-3476(77)80388-0","article-title":"Asymptomatic gonorrhea: Prevalence in apopulation of urban adolescents","volume":"90","author":"Hein","year":"1977","journal-title":"J. Pediatr."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1097\/OLQ.0000000000000510","article-title":"Gonorrhea in Indonesia: High Prevalence of Asymptomatic Urogenital Gonorrhea but No Circulating Extended Spectrum Cephalosporins-Resistant Neisseria gonorrhoeae Strains in Jakarta, Yogyakarta, and Denpasar, Indonesia","volume":"43","author":"Hananta","year":"2016","journal-title":"Sex. Transm. Dis."},{"key":"ref_5","first-page":"931","article-title":"Diagnosis and management of gonococcal infections","volume":"86","author":"Mayor","year":"2012","journal-title":"Am. Fam. Physician"},{"key":"ref_6","doi-asserted-by":"crossref","unstructured":"Alirol, E., Wi, T.E., Bala, M., Bazzo, M.L., Chen, X.-S., Deal, C., Dillon, J.-A.R., Kularatne, R., Heim, J., and van Huijsduijnen, R.H. (2017). Multidrug-resistant gonorrhea: A research and development roadmap to discover new medicines. PLoS Med., 14.","DOI":"10.1371\/journal.pmed.1002366"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"735","DOI":"10.3201\/eid2404.171873","article-title":"Cooperative Recognition of Internationally Disseminated Ceftriaxone-Resistant Neisseriagonorrhoeae Strain","volume":"24","author":"Lahra","year":"2018","journal-title":"Emerg. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Wi, T., Lahra, M.M., Ndowa, F., Bala, M., Dillon, J.-A.R., Ramon-Pardo, P., Eremin, S.R., Bolan, G., and Unemo, M. (2017). Antimicrobial resistance in Neisseria gonorrhoeae: Global surveillance and a call for international collaborative action. PLoS Med., 14.","DOI":"10.1371\/journal.pmed.1002344"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"e413","DOI":"10.1016\/j.ijid.2009.02.006","article-title":"Underreporting and underestimation of gonorrhea cases in the Taiwan National Gonorrhea Notifiable Disease System in the Tainan region: Evaluation by a pilot physician-based sentinel surveillance on Neisseria gonorrhoeae infection","volume":"13","author":"Hsieh","year":"2009","journal-title":"Int. J. Infect. Dis."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Unemo, M., Seifert, H.S., Hook, E.W., Hawkes, S., Ndowa, F., and Dillon, J.-A.R. (2019). Gonorrhoea. Nat. Rev. Dis. Prim., 5.","DOI":"10.1038\/s41572-019-0128-6"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3439","DOI":"10.1111\/j.1365-2958.1992.tb02211.x","article-title":"Interaction of two variable proteins (PilE and PilC) required for pilus-mediated adherence of Neisseria gonorrhoeae to human epithelial cells","volume":"6","author":"Rudel","year":"1992","journal-title":"Mol. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1084\/jem.137.3.571","article-title":"Studies on gonococcus infection: IV. Pili: Their role in attachment of gonococci to tissue culture cells","volume":"137","author":"Swanson","year":"1973","journal-title":"J. Exp. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1111\/j.1574-6976.2010.00260.x","article-title":"Opa proteins and CEACAMs: Pathways of immune engagement for pathogenicNeisseria","volume":"35","author":"Sadarangani","year":"2011","journal-title":"FEMS Microbiol. Rev."},{"key":"ref_14","doi-asserted-by":"crossref","unstructured":"Stein, D.C., LeVan, A., Hardy, B., Wang, L.-C., Zimmerman, L., and Song, W. (2015). Expression of Opacity Proteins Interferes with the Transmigration of Neisseria gonorrhoeae across Polarized Epithelial Cells. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0134342"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"6468","DOI":"10.1128\/JB.00969-12","article-title":"Construction and Characterization of a Derivative of Neisseria gonorrhoeae Strain MS11 Devoid of All opa Genes","volume":"194","author":"LeVan","year":"2012","journal-title":"J. Bacteriol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"12151","DOI":"10.1038\/s41598-017-12472-7","article-title":"Phase and antigenic variation govern competition dynamics through positioning in bacterial colonies","volume":"7","author":"Oldewurtel","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1434","DOI":"10.1128\/iai.63.4.1434-1439.1995","article-title":"Gonococcal opacity: Lectin-like interactions between Opa proteins and lipooligosaccharide","volume":"63","author":"Blake","year":"1995","journal-title":"Infect. Immun."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"4043","DOI":"10.1002\/j.1460-2075.1993.tb06088.x","article-title":"Phase variation of lipopolysaccharide directs interconversion of invasive and immuno-resistant phenotypes of Neisseria gonorrhoeae","volume":"12","year":"1993","journal-title":"EMBO J."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"403","DOI":"10.1111\/j.1365-2958.1994.tb00435.x","article-title":"Sequence changes in the pilus subunit lead to tropism variation of Neisseria gonorrhoeae to human tissue","volume":"13","author":"Jonsson","year":"1994","journal-title":"Mol. Microbiol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1307","DOI":"10.1002\/j.1460-2075.1991.tb07649.x","article-title":"Phase variation of the opacity outer membrane protein controls invasion by Neisseria gonorrhoeae into human epithelial cells","volume":"10","author":"Makino","year":"1991","journal-title":"EMBO J."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1097\/00005792-198311000-00005","article-title":"Disseminated gonococcal infection: A prospective analysis of 49 patients and a review of pathophysiology and immune mechanisms","volume":"62","author":"Goldenberg","year":"1983","journal-title":"Medicine"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1172\/JCI108569","article-title":"Gonococci causing disseminated gonococcal infection are resistant to the bactericidal action of normal human sera","volume":"58","author":"Schoolnik","year":"1976","journal-title":"J. Clin. Investig."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1128\/iai.40.2.816-819.1983","article-title":"Confirmation of association of protein I serotype of Neisseria gonorrhoeae with ability to cause disseminated infection","volume":"40","author":"Cannon","year":"1983","journal-title":"Infect. Immun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1221","DOI":"10.1056\/NEJM197306072882308","article-title":"Low Antibiotic Resistance of Gonococci Causing Disseminated Infection","volume":"288","author":"Wiesner","year":"1973","journal-title":"N. Engl. J. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1093\/infdis\/132.2.204","article-title":"Disseminated Gonococcal Infections Caused by Neisseria gonorrhoeae with Unique Nutritional Requirements","volume":"132","author":"Knapp","year":"1975","journal-title":"J. Infect. Dis."},{"key":"ref_26","doi-asserted-by":"crossref","unstructured":"Yu, Q., Wang, L.-C., Di Benigno, S., Gray-Owen, S.D., Stein, D., and Song, W. (2019). Neisseria gonorrhoeae infects the heterogeneous epithelia of the human cervix using distinct mechanisms. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1008136"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"971","DOI":"10.1046\/j.1365-2958.1997.6342006.x","article-title":"Differential Opa specificities for CD66 receptors influence tissue interactions and cellular response to Neisseria gonorrhoeae","volume":"26","author":"Lorenzen","year":"1997","journal-title":"Mol. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"575","DOI":"10.1128\/iai.21.2.575-584.1978","article-title":"Studies on gonococcus infection. XV. Identification of surface proteins of Neisseria gonorrhoeae correlated with leukocyte association","volume":"21","author":"King","year":"1978","journal-title":"Infect. Immun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1097\/00007435-198604000-00003","article-title":"Approximate Molecular Weight of Envelope Protein 1 and Colony Opacity of Neisseria gonorrhoeae Strains Isolated from Patients with Disseminated or Localized Infection","volume":"13","author":"Martin","year":"1986","journal-title":"Sex. Transm. Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"882","DOI":"10.1128\/iai.27.3.882-888.1980","article-title":"Comparison of Virulence Markers of Peritoneal and Fallopian Tube Isolates with Endocervical Neisseria gonorrhoeae Isolates from Women with Acute Salpingitis","volume":"27","author":"Draper","year":"1980","journal-title":"Infect. Immun."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"911","DOI":"10.1084\/jem.179.3.911","article-title":"Multiple gonococcal opacity proteins are expressed during experimental urethral infection in the male","volume":"179","author":"Jerse","year":"1994","journal-title":"J. Exp. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1093\/infdis\/172.1.180","article-title":"Experimental Human Gonococcal Urethritis: 250 Neisseria gonorrhoeae MS11mkC Are Infective","volume":"172","author":"Schneider","year":"1995","journal-title":"J. Infect. Dis."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1186\/1741-7007-5-35","article-title":"Species status of Neisseria gonorrhoeae: Evolutionary and epidemiological inferences from multilocus sequence typing","volume":"5","author":"Bennett","year":"2007","journal-title":"BMC Biol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Vidovic, S., Horsman, G.B., Liao, M., and Dillon, J.-A.R. (2011). Influence of Conserved and Hypervariable Genetic Markers on Genotyping Circulating Strains of Neisseria gonorrhoeae. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0028259"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1128\/JCM.43.1.368-375.2005","article-title":"Genetic Typing of the Porin Protein of Neisseria gonorrhoeae from Clinical Noncultured Samples for Strain Characterization and Identification of Mixed Gonococcal Infections","volume":"43","author":"Lynn","year":"2005","journal-title":"J. Clin. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Wang, L.-C., Yu, Q., Edwards, V., Lin, B., Qiu, J., Turner, J.R., Stein, D., and Song, W. (2017). Neisseria gonorrhoeae infects the human endocervix by activating non-muscle myosin II-mediated epithelial exfoliation. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006269"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"30345","DOI":"10.1016\/S0021-9258(18)43819-7","article-title":"The structure of lipooligosaccharide produced by Neisseria gonorrhoeae, strain 15253, isolated from a patient with disseminated infection. Evidence for a new glycosylation pathway of the gonococcal lipooligosaccharide","volume":"269","author":"Yamasaki","year":"1994","journal-title":"J. Biol. Chem."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"93","DOI":"10.1128\/IAI.68.12.6526-6534.2000","article-title":"Effect of \u03b1-Oligosaccharide Phenotype of Neisseria gonorrhoeae Strain MS11 on Invasion of Chang Conjunctival, HEC-1-B Endometrial, and ME-180 Cervical Cells","volume":"68","author":"Minor","year":"2000","journal-title":"Infect. Immun."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"865","DOI":"10.1111\/j.1365-2958.1995.mmi_17050865.x","article-title":"Opa-typing: A high-resolution tool for studying the epidemiology of gonorrhoea","volume":"17","author":"Ison","year":"1995","journal-title":"Mol. Microbiol."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Khaki, P., Bhalla, P., Fayaz, A.M., Bidhendi, S.M., Esmailzadeh, M., and Sharma, P. (2009). Molecular Typing ofNeisseria gonorrhoeaeIsolates by Opa-Typing and Ribotyping in New Delhi, India. Int. J. Microbiol., 2009.","DOI":"10.1155\/2009\/934823"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1016\/S0966-842X(98)01365-1","article-title":"The role of neisserial Opa proteins in interactions with host cells","volume":"6","author":"Dehio","year":"1998","journal-title":"Trends Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1084\/jem.185.9.1557","article-title":"Several Carcinoembryonic Antigens (CD66) Serve as Receptors for Gonococcal Opacity Proteins","volume":"185","author":"Chen","year":"1997","journal-title":"J. Exp. Med."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1323","DOI":"10.1128\/JB.180.5.1323-1330.1998","article-title":"Sequence Diversity, Predicted Two-Dimensional Protein Structure, and Epitope Mapping of Neisserial Opa Proteins","volume":"180","author":"Malorny","year":"1998","journal-title":"J. Bacteriol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"290","DOI":"10.1016\/j.micinf.2011.11.002","article-title":"Neisseria gonorrhoeae induced disruption of cell junction complexes in epithelial cells of the human genital tract","volume":"14","author":"Maisey","year":"2012","journal-title":"Microbes Infect."},{"key":"ref_45","unstructured":"CDC (2021, August 27). Sexually Transmitted Diseases (STDs)-Sexually Transmitted Infections Prevalence, Incidence, and Cost Estimates in the United States, Available online: https:\/\/www.cdc.gov\/std\/statistics\/prevalence-2020-at-a-glance.htm."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1136\/sextrans-2014-051893","article-title":"The epidemiology of gonococcal arthritis in an Indigenous Australian population","volume":"91","author":"Tuttle","year":"2015","journal-title":"Sex. Transm. Infect."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1099\/00221287-114-2-305","article-title":"Variations in Surface Protein Composition Associated with Virulence Properties in Opacity Types of Neisseria gonorrhoeae","volume":"114","author":"Lambden","year":"1979","journal-title":"J. Gen. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1128\/iai.19.1.332-340.1978","article-title":"Studies on gonococcus infection. XIII. Occurrence of color\/opacity colonial variants in clinical cultures","volume":"19","author":"James","year":"1978","journal-title":"Infect. Immun."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/S0966-842X(97)01056-1","article-title":"Adhesion and invasion by the pathogenic neisseria","volume":"5","author":"Jerse","year":"1997","journal-title":"Trends Microbiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1084\/jem.191.6.949","article-title":"Role of Lipooligosaccharide in Opa-Independent Invasion of Neisseria gonorrhoeae into Human Epithelial Cells","volume":"191","author":"Song","year":"2000","journal-title":"J. Exp. Med."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/0882-4010(88)90103-9","article-title":"Cytidine 5\u2032-monophospho-N-acetyl neuraminic acid and a low molecular weight factor from human blood cells induce lipopolysaccharide alteration in gonococci when conferring resistance to killing by human serum","volume":"5","author":"Parsons","year":"1988","journal-title":"Microb. Pathog."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Wang, L.-C., Litwin, M., Sahiholnasab, Z., Song, W., and Stein, D.C. (2018). Neisseria gonorrhoeae Aggregation Reduces Its Ceftriaxone Susceptibility. Antibiotics, 7.","DOI":"10.3390\/antibiotics7020048"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"1856","DOI":"10.1086\/593336","article-title":"Gonococcal Cervicitis: A Role for Biofilm in Pathogenesis","volume":"198","author":"Steichen","year":"2008","journal-title":"J. Infect. Dis."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1878","DOI":"10.1128\/JB.01518-08","article-title":"Relative Contributions of Recombination and Mutation to the Diversification of the opa Gene Repertoire of Neisseria gonorrhoeae","volume":"191","author":"Bilek","year":"2009","journal-title":"J. Bacteriol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.1111\/j.1365-2958.1991.tb00807.x","article-title":"The role of pili in the interactions of pathogenic Neisseria with cultured human endothelial cells","volume":"5","author":"Virji","year":"1991","journal-title":"Mol. Microbiol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1197","DOI":"10.1111\/j.1462-5822.2005.00547.x","article-title":"I-domain-containing integrins serve as pilus receptors for Neisseria gonorrhoeae adherence to human epithelial cells","volume":"7","author":"Edwards","year":"2005","journal-title":"Cell. Microbiol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1046\/j.1462-5822.2002.t01-1-00215.x","article-title":"A co-operative interaction between Neisseria gonorrhoeae and complement receptor 3 mediates infection of primary cervical epithelial cells","volume":"4","author":"Edwards","year":"2002","journal-title":"Cell. Microbiol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"941","DOI":"10.1084\/jem.188.5.941","article-title":"Gonococcal Invasion of Epithelial Cells Driven by P.IA, a Bacterial Ion Channel with GTP Binding Properties","volume":"188","author":"Duensing","year":"1998","journal-title":"J. Exp. Med."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1136\/sti.2007.026914","article-title":"Prevalence of Neisseria gonorrhoeae infection in young subjects attending community clinics in South London","volume":"84","author":"Rao","year":"2008","journal-title":"Sex. Transm. Infect."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1097\/01.olq.0000158496.00315.04","article-title":"Chlamydia trachomatis and Neisseria gonorrhoeae Prevalence and Coinfection in Adolescents Entering Selected US Juvenile Detention Centers, 1997\u20132002","volume":"32","author":"Kahn","year":"2005","journal-title":"Sex. Transm. Dis."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"243","DOI":"10.1093\/infdis\/135.2.243","article-title":"Bactericidal Antibody in Genital Infection Due to Neisseria gonorrhoeae","volume":"135","author":"Kasper","year":"1977","journal-title":"J. Infect. Dis."},{"key":"ref_62","first-page":"238","article-title":"An improved fermentation medium for Neisseria gonorrhoeae and other Neisseria","volume":"2","author":"Kellogg","year":"1965","journal-title":"Health Lab. Sci."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"124","DOI":"10.12688\/wellcomeopenres.14826.1","article-title":"Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications","volume":"3","author":"Jolley","year":"2018","journal-title":"Wellcome Open Res."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"269","DOI":"10.1128\/jb.154.1.269-277.1983","article-title":"Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels","volume":"154","author":"Hitchcock","year":"1983","journal-title":"J. Bacteriol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1359","DOI":"10.1002\/1615-9861(200111)1:11<1359::AID-PROT1359>3.0.CO;2-Q","article-title":"Improved silver staining protocols for high sensitivity protein identification using matrix-assisted laser desorption\/ionization-time of flight analysis","volume":"1","author":"Mortz","year":"2001","journal-title":"Proteomics"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/2\/217\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:15:28Z","timestamp":1760134528000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/11\/2\/217"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,7]]},"references-count":65,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2022,2]]}},"alternative-id":["pathogens11020217"],"URL":"https:\/\/doi.org\/10.3390\/pathogens11020217","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,7]]}}}