Intersecting infections: the enhancing effect of Neisseria gonorrhoeae pathogenesis on HIV-1.
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| Název: | Intersecting infections: the enhancing effect of Neisseria gonorrhoeae pathogenesis on HIV-1. |
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| Autoři: | Dhanjal A; School of Clinical Dentistry.; Florey Institute of Infection., Shaw JG; Florey Institute of Infection.; School of Medicine and Population Health, University of Sheffield., Cole J; Florey Institute of Infection.; School of Medicine and Population Health, University of Sheffield.; Department of Infectious Diseases and Tropical Medicine, Sheffield Teaching Hospitals NHS, Sheffield, UK., Green LR; School of Clinical Dentistry.; Florey Institute of Infection. |
| Zdroj: | AIDS (London, England) [AIDS] 2025 Dec 01; Vol. 39 (15), pp. 2151-2160. Date of Electronic Publication: 2025 Nov 13. |
| Způsob vydávání: | Journal Article; Review |
| Jazyk: | English |
| Informace o časopise: | Publisher: Lippincott Williams & Wilkins Country of Publication: England NLM ID: 8710219 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1473-5571 (Electronic) Linking ISSN: 02699370 NLM ISO Abbreviation: AIDS Subsets: MEDLINE |
| Imprint Name(s): | Publication: 1998- : London, England : Lippincott Williams & Wilkins Original Publication: London : Gower Academic Journals, c1987- |
| Výrazy ze slovníku MeSH: | Gonorrhea*/complications , Gonorrhea*/microbiology , Gonorrhea*/pathology , HIV Infections*/complications , HIV Infections*/epidemiology , HIV-1*/physiology , HIV-1*/pathogenicity , Neisseria gonorrhoeae*/pathogenicity , Coinfection*/microbiology , Coinfection*/virology, Humans |
| Abstrakt: | Despite the relatively low transmission rates of HIV-1, the virus accounted for 1.5 million new infections in 2020, with widespread infection and devastating sequelae. Various mechanisms have been described, which exacerbate HIV-1 progression, including concurrent infection with other sexually transmitted infections (STIs). Epidemiological evidence has suggested the strongest association between Neisseria gonorrhoeae and HIV-1 compared to other STIs and the presence of untreated N. gonorrhoeae before infection with HIV-1 has been shown to enhance viral infection. Molecular investigation has corroborated this by showing that presence of N. gonorrhoeae enables transmission of HIV-1 across the epithelial membrane, enhances replication of HIV-1, increases viral shedding, and heightens immune dysregulation. Gonorrhoea infections are rapidly increasing worldwide providing a potential platform for increased HIV-1 incidence. Furthermore, whilst treatment of N. gonorrhoeae in parallel infection alleviates HIV-1 progression and transmission, this is becoming a less viable option as the threat of multidrug resistance within N. gonorrhoeae proliferates. These findings highlight the requirement for greater surveillance of concurrent infections to tackle the HIV-1 epidemic and warrant monitoring of the resistance crisis in N. gonorrhoeae to prevent worsening outcomes of HIV-1 patients. (Copyright © 2025 Wolters Kluwer Health, Inc. All rights reserved.) |
| References: | World Health Organisation. Global progress report on HIV, viral hepatitis and sexually transmitted infections, 2021. Accountability for the Global Health Sector Strategies 2016-2021: Actions for Impact. 1st ed. Geneva: World Health Organization; 2021. p. 1. Kalichman SC, Pellowski J, Turner C. Prevalence of sexually transmitted co-infections in people living with HIV/AIDS: systematic review with implications for using HIV treatments for prevention. Sex Transm Infect 2011; 87:183–190. Bekker LG, Beyrer C, Mgodi N, Lewin SR, Delany-Moretlwe S, Taiwo B, et al. HIV infection. Nat Rev Dis Primer 2023; 9:42. Maartens G, Celum C, Lewin SR. HIV infection: epidemiology, pathogenesis, treatment, and prevention. Lancet 2014; 384:258–271. Jarvis G, Chang T. Modulation of HIV transmission by Neisseria gonorrhoeae: molecular and immunological aspects. Curr HIV Res 2012; 10:211–217. Quillin SJ, Seifert HS. Neisseria gonorrhoeae host adaptation and pathogenesis. Nat Rev Microbiol 2018; 16:226–240. Unemo M, Seifert HS, Hook EW, Hawkes S, Ndowa F, Dillon JAR. Gonorrhoea. Nat Rev Dis Primer 2019; 5:79. UK Health Security Agency. Gonococcal resistance to antimicrobials surveillance (GRASP) [Internet]. UK Health Security Agency; 2024. Available at: https://www.gov.uk/government/publications/gonococcal-resistance-to-antimicrobials-surveillance-programme-grasp-report/grasp-report-data-to-june-2024#main-findings. [Accessed 23 January 2025]. World Health Organisation. WHO Bacterial Priority Pathogens List 2024: Bacterial Pathogens of Public Health Importance, to Guide Research, Development, and Strategies to Prevent and Control Antimicrobial Resistance. 1st ed. Geneva: World Health Organization; 2024. p.1. Galvin SR, Cohen MS. The role of sexually transmitted diseases in HIV transmission. Nat Rev Microbiol 2004; 2:33–42. Naik PA, Zu J, Owolabi KM. Global dynamics of a fractional order model for the transmission of HIV epidemic with optimal control. Chaos Solitons Fractals 2020; 138:109826. Malek R, Mitchell H, Furegato M, Simms I, Mohammed H, Nardone A, et al. Contribution of transmission in HIV-positive men who have sex with men to evolving epidemics of sexually transmitted infections in England: an analysis using multiple data sources, 2009–2013. Eurosurveillance 2024; 20:21093. Taylor M, Newman D, Gonzalez J, Skinner J, Khurana R, Mickey T. HIV status and viral loads among men testing positive for rectal gonorrhoea and chlamydia, Maricopa County, Arizona, USA, 2011-2013. HIV Med 2015; 16:249–254. Omori R, Chemaitelly H, Abu-Raddad LJ. Understanding dynamics and overlapping epidemiologies of HIV, HSV-2, chlamydia, gonorrhea, and syphilis in sexual networks of men who have sex with men. Front Public Health 2024; 12:1335693. Klotman ME, Rapista A, Teleshova N, Micsenyi A, Jarvis GA, Lu W, et al. Neisseria gonorrhoeae -induced human defensins 5 and 6 increase HIV infectivity: role in enhanced transmission. J Immunol 2008; 180:6176–6185. Ding J, Rapista A, Teleshova N, Mosoyan G, Jarvis GA, Klotman ME, et al. Neisseria gonorrhoeae enhances HIV-1 infection of primary resting CD4+ T cells through TLR2 activation. J Immunol 2010; 184:2814–2824. Sanyal A, Shen C, Ding M, Reinhart TA, Chen Y, Sankapal S, et al. Neisseria gonorrhoeae uses cellular proteins CXCL10 and IL8 to enhance HIV-1 transmission across cervical mucosa. Am J Reprod Immunol 2019; 81:e13111. Mohammed H, Blomquist P, Ogaz D, Duffell S, Furegato M, Checchi M, et al. 100 years of STIs in the UK: a review of national surveillance data. Sex Transm Infect 2018; 94:553–558. Catalan J, Ridge D, Hedge B. HIV in the UK; voices from the epidemic (1st ed). Routledge. 2020. O’Brien A, Sherrard-Smith E, Sile B, Watts C, Simms I. Spatial clusters of gonorrhoea in England with particular reference to the outcome of partner notification: 2012 and 2013. PLoS One 2018; 13:e0195178. Zhang Q, Peng L, Yuan Y, Hu Z, Zeng Y, Zeng W, et al. High rates of Treponema pallidum, Neisseria gonorrhoeae, Chlamydia trachomatis, or Trichomonas vaginalis co-infection in people with HIV: a systematic review and meta-analysis. Eur J Clin Microbiol Infect Dis 2025; 44:1–15. Bala M, Mullick JB, Muralidhar S, Kumar J, Ramesh V. Gonorrhoea & its co-infection with other ulcerative, nonulcerative sexually transmitted & HIV infection in a Regional STD Centre. Indian J Med Res 2011; 133:346–349. Ghassabi F, Malekzadegan Y, Sedigh Ebrahim-Saraie H, Heidari H, Sabet M, Bagheri A, et al. Gonorrhea and syphilis co-infection and related risk factors in HIV patients from Shiraz, South of Iran. Casp J Intern Me 2018; 9:397–402. Sentís A, Martin-Sanchez M, Arando M, Vall M, Barbera MJ, Ocaña I, et al. STI-HIV group of Barcelona. Sexually transmitted infections in young people and factors associated with HIV coinfection: an observational study in a large city. BMJ Open 2019; 9:e027245. Sheung A, Rebbapragada A, Shin LY, Dobson-Belaire W, Kimani J, Ngugi E, et al. Kibera HIV Study Group. Mucosal Neisseria gonorrhoeae coinfection during HIV acquisition is associated with enhanced systemic HIV-specific CD8 T-cell responses. AIDS 2008; 22:1729–1737. Callander D, Guy R, Fairley CK, McManus H, Prestage G, Chow EPF, et al. Gonorrhoea gone wild: rising incidence of gonorrhoea and associated risk factors among gay and bisexual men attending Australian sexual health clinics. Sex Health 2019; 16:457. Grewal R, Allen VG, Gardner S, Moravan V, Tan DHS, Raboud J, et al. OHTN Cohort Study Research Team. Serosorting and recreational drug use are risk factors for diagnosis of genital infection with chlamydia and gonorrhoea among HIV-positive men who have sex with men: results from a clinical cohort in Ontario, Canada. Sex Transm Infect 2017; 93:71–75. Cunha CB, Friedman RK, De Boni RB, Gaydos C, Guimarães MRC, Siqueira BH, et al. Chlamydia trachomatis, Neisseria gonorrhoeae and syphilis among men who have sex with men in Brazil. BMC Public Health 2015; 15:686. Neal TMS, Lichtenstein B, Brodsky SL. Clinical implications of stigma in HIV/AIDS and other sexually transmitted infections. Int J STD AIDS 2010; 21:158–160. Keshinro B, Crowell TA, Nowak RG, Adebajo S, Peel S, Gaydos CA, et al. TRUST/RV368 Study Group. High prevalence of HIV, chlamydia and gonorrhoea among men who have sex with men and transgender women attending trusted community centres in Abuja and Lagos, Nigeria. J Int AIDS Soc 2016; 19:21270. Guvenc F, Kaul R, Gray-Owen SD. Intimate relations: molecular and immunologic interactions between Neisseria gonorrhoeae and HIV-1. Front Microbiol 2020; 11:1299. Nicoll A. Assessing the impact of national anti-HIV sexual health campaigns: trends in the transmission of HIV and other sexually transmitted infections in England. Sex Transm Infect 2001; 77:242–247. Nagington M, Sandset T. Putting the NHS England on trial: uncertainty-as-power, evidence and the controversy of PrEP in England. Med Humanit 2020; 46:176–179. Celum C, Grinsztejn B, Ngure K. Preparing for long-acting PrEP delivery: building on lessons from oral PrEP. J Int AIDS Soc 2023; 26 (Suppl 2):e26103. Deeks SG, Overbaugh J, Phillips A, Buchbinder S. HIV infection. Nat Rev Dis Primer 2015; 1:15035. Jansen K, Potthoff A, Schuppe AK, Beer D, Jessen H, Scholten S, et al. MSM Screening Study group. STI in times of PrEP: high prevalence of chlamydia, gonorrhea, and mycoplasma at different anatomic sites in men who have sex with men in Germany. BMC Infect Dis 2020; 20:110. Montaño MA, Dombrowski JC, Dasgupta S, Golden MR, Duerr A, Manhart LE, et al. Changes in sexual behavior and STI diagnoses among MSM initiating PrEP in a clinic setting. AIDS Behav 2019; 23:548–555. Traeger MW, Cornelisse VJ, Asselin J, Price B, Roth NJ, Willcox J, et al. PrEPX Study Team. Association of HIV preexposure prophylaxis with incidence of sexually transmitted infections among individuals at high risk of HIV infection. JAMA 2019; 321:1380–1390. Sokoll PR, Migliavaca CB, Döring S, Traub U, Stark K, Sardeli AV. Efficacy of postexposure prophylaxis with doxycycline (Doxy-PEP) in reducing sexually transmitted infections: a systematic review and meta-analysis. Sex Transm Infect 2025; 101:59–67. Molina JM, Charreau I, Chidiac C, Pialoux G, Cua E, Delaugerre C, et al. Postexposure prophylaxis with doxycycline to prevent sexually transmitted infections in men who have sex with men: an open-label randomised substudy of the ANRS IPERGAY trial. Lancet Infect Dis 2018; 18:308–317. Cehovin A, Harrison OB, Lewis SB, Ward PN, Ngetsa C, Graham SM, et al. Identification of novel Neisseria gonorrhoeae lineages harboring resistance plasmids in coastal Kenya. J Infect Dis 2018; 218:801–808. Cornelisse VJ, Riley B, Medland NA. Australian consensus statement on doxycycline postexposure prophylaxis doxy-PEP for the prevention of syphilis, chlamydia and gonorrhoea among gay, bisexual and other men who have sex with men. Med J Aust 2024; 220:381–386. Xu SX, Leontyev D, Kaul R, Gray-Owen SD. Neisseria gonorrhoeae co-infection exacerbates vaginal HIV shedding without affecting systemic viral loads in human CD34+ engrafted mice. PLoS One 2018; 13:e0191672. Ghys PDF. The associations between cervicovaginal HIV shedding, sexually transmitted diseases and immunosuppression in female sex workers in Abidjan, Côte d’Ivoire. AIDS 1997; 11:F85–93. Cohen MS, Hoffman IF, Royce RA, Kazembe P, Dyer JR, Daly CC, et al. Reduction of concentration of HIV-1 in semen after treatment of urethritis: implications for prevention of sexual transmission of HIV-1. Lancet 1997; 349:1868–1873. Sadiq ST, Taylor S, Copas AJ, Bennett J, Kaye S, Drake SM, et al. The effects of urethritis on seminal plasma HIV-1 RNA loads in homosexual men not receiving antiretroviral therapy. Sex Transm Infect 2005; 81:120–123. Baeten JM, Kahle E, Lingappa JR, Coombs RW, Delany-Moretlwe S, Nakku-Joloba E, et al. Genital HIV-1 RNA predicts risk of heterosexual HIV-1 transmission. Sci Transl Med 2011; 3:77ra29. Srifeungfung S, Roongpisuthipong A, Asavapiriyanont S, Lolekha R, Tribuddharat C, Lokpichart S, et al. Prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae in HIV-seropositive patients and gonococcal antimicrobial susceptibility: an update in Thailand. Jpn J Infect Dis 2009; 62:467–470. Bell SF, Lambert SB, Jennison AV, Guglielmino CJ, Ware RS. HIV risk and gonococcal genotype: Opportunities to improve passive surveillance for prompt identification of syndemics? [Internet]. 2022. Available from: https://www1.health.gov.au/internet/main/publishing.nsf/Content/2A15CD097063EF40CA2587CE008354F1/$File/hiv_risk_and_gonococcal_genotype_opportunities_to_improve_passive_surveillance_for_prompt_identification_of_syndemics.pdf. [Accessed 29 January 2025]. Town K, Field N, Furegato M, Cole M, Harris S, Hughes G. The emergence and spread of antimicrobial resistant Neisseria gonorrhoeae in HIV positive men who have sex with men. Sex Transm Infect 2017; 93 (Suppl 2):A27. Valere K, Rapista A, Eugenin E, Lu W, Chang TL. Human alpha-defensin HNP1 increases HIV traversal of the epithelial barrier: a potential role in STI-mediated enhancement of HIV transmission. Viral Immunol 2015; 28:609–615. Tugizov S. Human immunodeficiency virus-associated disruption of mucosal barriers and its role in HIV transmission and pathogenesis of HIV/AIDS disease. Tissue Barriers 2016; 4:e1159276. Day CJ, Hardison RL, Spillings BL, Poole J, Jurcisek JA, Mak J, et al. Complement receptor 3 mediates HIV-1 transcytosis across an intact cervical epithelial cell barrier: new insight into HIV transmission in women. mBio 2022; 13:e02177-21. Walker E, Van Niekerk S, Hanning K, Kelton W, Hicks J. Mechanisms of host manipulation by Neisseria gonorrhoeae. Front Microbiol 2023; 14:1119834. Rapista A, Ding J, Benito B, Lo YT, Neiditch MB, Lu W, et al. Human defensins 5 and 6 enhance HIV-1 infectivity through promoting HIV attachment. Retrovirology 2011; 8:45. Porter E, Yang H, Yavagal S, Preza GC, Murillo O, Lima H, et al. Distinct defensin profiles in Neisseria gonorrhoeae and Chlamydia trachomatis urethritis reveal novel epithelial cell-neutrophil interactions. Infect Immun 2005; 73:4823–4833. Masson L, Mlisana K, Little F, Werner L, Mkhize NN, Ronacher K, et al. Defining genital tract cytokine signatures of sexually transmitted infections and bacterial vaginosis in women at high risk of HIV infection: a cross-sectional study. Sex Transm Infect 2014; 90:580–587. Veretennikova A, Chang TL. Chlamydia trachomatis enhances HIV infection of non-activated PBMCs. EC Microbiol 2022; 18:13–17. Roebuck KA, Saifuddin M. Regulation of HIV-1 Transcription. Gene Expr 1999; 8:67–84. Chen A, Boulton IC, Pongoski J, Cochrane A, Gray-Owen SD. Induction of HIV-1 long terminal repeat-mediated transcription by Neisseria gonorrhoeae. AIDS 2003; 17:625–628. Malott RJ, Keller BO, Gaudet RG, McCaw SE, Lai CCL, Dobson-Belaire WN, et al. Neisseria gonorrhoeae derived heptose elicits an innate immune response and drives HIV-1 expression. Proc Natl Acad Sci USA 2013; 110:10234–10239. Green LR, Cole J, Parga EFD, Shaw JG. Neisseria gonorrhoeae physiology and pathogenesis. Adv Microb Physiol 2022; 80:. Dobson-Belaire WN, Cochrane A, Ostrowski MA, Gray-Owen SD. Differential response of primary and immortalized CD4+ T cells to Neisseria gonorrhoeae-induced cytokines determines the effect on HIV-1 replication. PLoS One 2011; 6:e18133. Douek DC, Brenchley JM, Betts MR, Ambrozak DR, Hill BJ, Okamoto Y, et al. HIV preferentially infects HIV-specific CD4+ T cells. Nature 2002; 417:95–98. Vieira VA, Avelino-Silva VI, Cerqueira NB, Costa DA, Costa PR, Vasconcelos RP, et al. PrEP Brasil Study Team. Asymptomatic anorectal Chlamydia trachomatis and Neisseria gonorrhoeae infections are associated with systemic CD8+ T-cell activation. AIDS 2017; 31:2069–2076. Yu Q, Chow EMC, McCaw SE, Hu N, Byrd D, Amet T, et al. Association of Neisseria gonorrhoeae OpaCEA with dendritic cells suppresses their ability to elicit an HIV-1-specific T cell memory response. PLoS One 2013; 8:e56705. Engering A, Van Vliet SJ, Geijtenbeek TBH, Van Kooyk Y. Subset of DC-SIGN+ dendritic cells in human blood transmits HIV-1 to T lymphocytes. Blood 2002; 100:1780–1786. Zhu W, Ventevogel MS, Knilans KJ, Anderson JE, Oldach LM, McKinnon KP, et al. Neisseria gonorrhoeae suppresses dendritic cell-induced, antigen-dependent CD4 T cell proliferation. PLoS One 2012; 7:e41260. Zhang J, Li G, Bafica A, Pantelic M, Zhang P, Broxmeyer H, et al. Neisseria gonorrhoeae enhances infection of dendritic cells by HIV type 1. J Immunol 2005; 174:7995–8002. Poole J, Day CJ, Haselhorst T, Jen FEC, Torres VJ, Edwards JL, et al. Repurposed drugs that block the Gonococcus-complement receptor 3 interaction can prevent and cure gonococcal infection of primary human cervical epithelial cells. mBio 2020; 11:e03046-19. |
| Contributed Indexing: | Keywords: ; HIV-1; co-infection; synergy; transmission |
| Entry Date(s): | Date Created: 20251114 Date Completed: 20251114 Latest Revision: 20251114 |
| Update Code: | 20251114 |
| DOI: | 10.1097/QAD.0000000000004295 |
| PMID: | 41235651 |
| Databáze: | MEDLINE |
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Nájsť tento článok vo Web of Science | Abstrakt: | Despite the relatively low transmission rates of HIV-1, the virus accounted for 1.5 million new infections in 2020, with widespread infection and devastating sequelae. Various mechanisms have been described, which exacerbate HIV-1 progression, including concurrent infection with other sexually transmitted infections (STIs). Epidemiological evidence has suggested the strongest association between Neisseria gonorrhoeae and HIV-1 compared to other STIs and the presence of untreated N. gonorrhoeae before infection with HIV-1 has been shown to enhance viral infection. Molecular investigation has corroborated this by showing that presence of N. gonorrhoeae enables transmission of HIV-1 across the epithelial membrane, enhances replication of HIV-1, increases viral shedding, and heightens immune dysregulation. Gonorrhoea infections are rapidly increasing worldwide providing a potential platform for increased HIV-1 incidence. Furthermore, whilst treatment of N. gonorrhoeae in parallel infection alleviates HIV-1 progression and transmission, this is becoming a less viable option as the threat of multidrug resistance within N. gonorrhoeae proliferates. These findings highlight the requirement for greater surveillance of concurrent infections to tackle the HIV-1 epidemic and warrant monitoring of the resistance crisis in N. gonorrhoeae to prevent worsening outcomes of HIV-1 patients.<br /> (Copyright © 2025 Wolters Kluwer Health, Inc. All rights reserved.) |
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| ISSN: | 1473-5571 |
| DOI: | 10.1097/QAD.0000000000004295 |