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Wagner Fellowship"],"award-info":[{"award-number":["Robert R. Wagner Fellowship"]}],"id":[{"id":"10.13039\/100008457","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"abstract":"<jats:p><jats:italic>Neisseria gonorrhoeae<\/jats:italic> (the gonococcus, Gc) causes the sexually transmitted infection gonorrhea. Gc is a prominent threat to human health by causing severe lifelong sequelae, including infertility and chronic pelvic pain, which is amplified by the emergence of \u201csuperbug\u201d strains resistant to all current antibiotics. Gc is highly adapted to colonize human mucosal surfaces, where it survives despite initiating a robust inflammatory response and influx of polymorphonuclear leukocytes (PMNs, neutrophils) that typically clear bacteria. Here, dual-species RNA-sequencing was used to define Gc and PMN transcriptional profiles alone and after infection. Core host and bacterial responses were assessed for two strains of Gc and three human donors\u2019 PMNs. Comparative analysis of Gc transcripts revealed overlap between Gc responses to PMNs, iron, and hydrogen peroxide; 98 transcripts were differentially expressed across both Gc strains in response to PMN co-culture, including iron-responsive and oxidative stress response genes. We experimentally determined that the iron-dependent TbpB is suppressed by PMN co-culture, and iron-limited Gc have a survival advantage when cultured with PMNs. Analysis of PMN transcripts modulated by Gc infection revealed differential expression of genes driving cell adhesion, migration, inflammatory responses, and inflammation resolution pathways. Production of pro-inflammatory cytokines, including IL1B and IL8, the adhesion factor ICAM1, and prostaglandin PGE2 were induced in PMNs in response to Gc. Together, this study represents a comprehensive and experimentally validated dual-species transcriptomic analysis of two isolates of Gc and primary human PMNs that gives insight into how this bacterium survives innate immune onslaught to cause disease.<\/jats:p>","DOI":"10.1371\/journal.ppat.1012369","type":"journal-article","created":{"date-parts":[[2024,7,8]],"date-time":"2024-07-08T19:05:52Z","timestamp":1720465552000},"page":"e1012369","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":4,"title":["Dual species transcriptomics reveals conserved metabolic and immunologic processes in interactions between human neutrophils and Neisseria gonorrhoeae"],"prefix":"10.1371","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1473-1149","authenticated-orcid":true,"given":"Aimee D.","family":"Potter","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Vonetta L.","family":"Edwards","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Adonis","family":"D\u2019Mello","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Mary C.","family":"Gray","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amol C.","family":"Shetty","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Amy L.","family":"Forehand","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Camille S.","family":"Westlake","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Evan R.","family":"Lamb","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xuechu","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Stephanie A.","family":"Ragland","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7738-3757","authenticated-orcid":true,"given":"Alison K.","family":"Criss","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0615-3257","authenticated-orcid":true,"given":"Herv\u00e9","family":"Tettelin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2024,7,8]]},"reference":[{"key":"ppat.1012369.ref001","doi-asserted-by":"crossref","unstructured":"CDC. Sexually Transmitted Disease Surveillance 2018. Atlanta: U.S.: 2019. doi: 10.15620\/cdc.79370","DOI":"10.15620\/cdc.79370"},{"key":"ppat.1012369.ref002","unstructured":"WHO. Sexually transmitted infections (STIs). Available from: https:\/\/www.who.int\/news-room\/fact-sheets\/detail\/sexually-transmitted-infections-(stis)."},{"key":"ppat.1012369.ref003","article-title":"Antibiotic resistance in Neisseria gonorrhoeae is diminishing available treatment options for gonorrhea: some possible remedies.","author":"J. Tapsall","year":"2006","journal-title":"Expert review of anti-infective therapy."},{"key":"ppat.1012369.ref004","article-title":"Meeting the public health challenge of multidrug- and extensively drug-resistant Neisseria gonorrhoeae.","author":"J Tapsall","year":"2009","journal-title":"Expert review of anti-infective therapy."},{"key":"ppat.1012369.ref005","article-title":"Emerging antimicrobial resistance in Neisseria gonorrhoeae: urgent need to strengthen prevention strategies","author":"K Workowski","year":"2008","journal-title":"Annals of internal medicine"},{"key":"ppat.1012369.ref006","article-title":"Sexually Transmitted Infections Treatment Guidelines.","author":"BL Workowski KA","year":"2021","journal-title":"CDC"},{"key":"ppat.1012369.ref007","article-title":"High-level cefixime- and ceftriaxone-resistant Neisseria gonorrhoeae in France: novel penA mosaic allele in a successful international clone causes treatment failure","author":"M Unemo","year":"2012","journal-title":"Antimicrobial agents and chemotherapy"},{"key":"ppat.1012369.ref008","article-title":"Retrospective analysis of antimicrobial susceptibility trends (2000\u20132009) in Neisseria gonorrhoeae isolates from countries in Latin America and the Caribbean shows evolving resistance to ciprofloxacin, azithromycin and decreased susceptibility to ceftriaxone.","author":"S Starnino","year":"2012","journal-title":"Sexually transmitted diseases."},{"key":"ppat.1012369.ref009","article-title":"Emergence of multidrug-resistant, extensively drug-resistant and untreatable gonorrhea","author":"M Unemo","year":"2012","journal-title":"Future microbiology"},{"key":"ppat.1012369.ref010","article-title":"Ceftriaxone-resistant Neisseria gonorrhoeae, Japan","author":"M Ohnishi","year":"2011","journal-title":"Emerging infectious diseases"},{"key":"ppat.1012369.ref011","article-title":"Human Immune Responses and the Natural History of Neisseria gonorrhoeae Infection.","author":"A Lovett","year":"2019","journal-title":"Frontiers in immunology"},{"issue":"6","key":"ppat.1012369.ref012","first-page":"357","article-title":"Pelvic Inflammatory Disease: Diagnosis, Management, and Prevention","volume":"100","author":"A Curry","year":"2019","journal-title":"American family physician"},{"key":"ppat.1012369.ref013","article-title":"Sexually transmitted diseases and infertility","author":"D Tsevat","year":"2017","journal-title":"American journal of obstetrics and gynecology"},{"key":"ppat.1012369.ref014","article-title":"Neutrophils, from marrow to microbes","author":"N. Borregaard","year":"2010","journal-title":"Immunity"},{"key":"ppat.1012369.ref015","article-title":"Cytokine and antibody responses in women infected with Neisseria gonorrhoeae: effects of concomitant infections","author":"SR Hedges","year":"1998","journal-title":"J Infect Dis"},{"key":"ppat.1012369.ref016","article-title":"Inflammatory cytokines produced in response to experimental human gonorrhea","author":"KH Ramsey","year":"1995","journal-title":"J Infect Dis"},{"key":"ppat.1012369.ref017","article-title":"Neutrophils: Their Role in Innate and Adaptive Immunity 2017.","author":"C Rosales","year":"2017","journal-title":"Journal of immunology research"},{"key":"ppat.1012369.ref018","article-title":"Gonococcal Defenses against Antimicrobial Activities of Neutrophils","author":"A Palmer","year":"2018","journal-title":"Trends Microbiol"},{"key":"ppat.1012369.ref019","article-title":"Cell intrinsic functions of neutrophils and their manipulation by pathogens","author":"L Allen","year":"2019","journal-title":"Current opinion in immunology"},{"key":"ppat.1012369.ref020","article-title":"Defenses against oxidative stress in Neisseria gonorrhoeae: a system tailored for a challenging environment","author":"KL Seib","year":"2006","journal-title":"Microbiol Mol Biol Rev"},{"key":"ppat.1012369.ref021","article-title":"Neutrophil heterogeneity: implications for homeostasis and pathogenesis","author":"C Silvestre-Roig","year":"2016","journal-title":"Blood"},{"key":"ppat.1012369.ref022","article-title":"The transcriptome response of Neisseria gonorrhoeae to hydrogen peroxide reveals genes with previously uncharacterized roles in oxidative damage protection","author":"E Stohl","year":"2005","journal-title":"Molecular microbiology"},{"key":"ppat.1012369.ref023","article-title":"Interactions of Neisseria gonorrhoeae with adherent polymorphonuclear leukocytes","author":"MP Simons","year":"2005","journal-title":"Infect 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during neutrophil co-culture.","author":"AD Potter","year":"2023","journal-title":"mSystems"},{"key":"ppat.1012369.ref028","article-title":"Characterization of the Neisseria gonorrhoeae Iron and Fur Regulatory Network","author":"C Yu","year":"2016","journal-title":"Journal of bacteriology"},{"key":"ppat.1012369.ref029","article-title":"Neisseria gonorrhoeae Exposed to Sublethal Levels of Hydrogen Peroxide Mounts a Complex Transcriptional Response.","author":"S Quillin","year":"2018","journal-title":"mSystems"},{"key":"ppat.1012369.ref030","article-title":"Deep sequencing-based analysis of the anaerobic stimulon in Neisseria gonorrhoeae","author":"V Isabella","year":"2011","journal-title":"BMC genomics"},{"key":"ppat.1012369.ref031","article-title":"Global Network Analysis of Neisseria gonorrhoeae Identifies Coordination between Pathways, Processes, and Regulators Expressed during Human Infection.","author":"R McClure","year":"2020","journal-title":"mSystems"},{"key":"ppat.1012369.ref032","article-title":"Transcriptome Analysis of Neisseria gonorrhoeae during Natural Infection Reveals Differential Expression of Antibiotic Resistance Determinants between Men and Women.","author":"K Nudel","year":"2018","journal-title":"mSphere"},{"key":"ppat.1012369.ref033","article-title":"The Neisseria gonorrhoeae Methionine Sulfoxide Reductase (MsrA\/B) Is a Surface Exposed, Immunogenic, Vaccine Candidate.","author":"F Jen","year":"2019","journal-title":"Frontiers in immunology"},{"key":"ppat.1012369.ref034","article-title":"Ecf, an alternative sigma factor from Neisseria gonorrhoeae, controls expression of msrAB, which encodes methionine sulfoxide reductase","author":"I Gunesekere","year":"2006","journal-title":"Journal of bacteriology"},{"key":"ppat.1012369.ref035","article-title":"The transferrin receptor expressed by gonococcal strain FA1090 is required for the experimental infection of human male volunteers","author":"CN Cornelissen","year":"1998","journal-title":"Mol Microbiol"},{"key":"ppat.1012369.ref036","article-title":"Neisseria gonorrhoeae requires expression of TonB and the putative transporter TdfF to replicate within cervical epithelial cells","author":"TA Hagen","year":"2006","journal-title":"Mol Microbiol"},{"key":"ppat.1012369.ref037","article-title":"Specificity of the lactoferrin and transferrin receptors in Neisseria gonorrhoeae","author":"BC Lee","year":"1988","journal-title":"Mol Microbiol"},{"key":"ppat.1012369.ref038","article-title":"Endocervical and Neutrophil Lipoxygenases Coordinate Neutrophil Transepithelial Migration to Neisseria gonorrhoeae","author":"JS Stevens","year":"2018","journal-title":"J Infect Dis"},{"key":"ppat.1012369.ref039","article-title":"Modulation of phagocytosis-induced cell death of human neutrophils by Neisseria gonorrhoeae","author":"C Cho","year":"2020","journal-title":"Journal of leukocyte biology"},{"key":"ppat.1012369.ref040","article-title":"Neisseria gonorrhoeae-mediated inhibition of apoptotic signalling in polymorphonuclear leukocytes","author":"A Chen","year":"2011","journal-title":"Infection and immunity"},{"key":"ppat.1012369.ref041","article-title":"Neisseria gonorrhoeae delays the onset of apoptosis in polymorphonuclear leukocytes","author":"M Simons","year":"2006","journal-title":"Cellular microbiology"},{"key":"ppat.1012369.ref042","article-title":"The GeneCards Suite: From Gene Data Mining to Disease Genome Sequence Analyses.","author":"G Stelzer","year":"2016","journal-title":"Curr Protoc Bioinformatics"},{"key":"ppat.1012369.ref043","article-title":"Phagocytosing neutrophils produce and release high amounts of the neutrophil-activating peptide 1\/interleukin 8","author":"F Bazzoni","year":"1991","journal-title":"The Journal of experimental medicine"},{"key":"ppat.1012369.ref044","article-title":"Characterization of prostaglandin E2 generation through the cyclooxygenase (COX)-2 pathway in human neutrophils.","author":"M St-Onge","year":"2007","journal-title":"Biochimica et biophysica acta"},{"key":"ppat.1012369.ref045","article-title":"PGE 2 production at sites of tissue injury promotes an anti-inflammatory neutrophil phenotype and determines the outcome of inflammation resolution in vivo","author":"CA Loynes","year":"2018","journal-title":"Science advances"},{"key":"ppat.1012369.ref046","article-title":"ICAM-1-expressing neutrophils exhibit enhanced effector functions in murine models of endotoxemia","author":"A Woodfin","year":"2016","journal-title":"Blood"},{"key":"ppat.1012369.ref047","article-title":"Neutrophil transendothelial migration: updates and new perspectives","author":"M-D Filippi","year":"2019","journal-title":"Blood"},{"key":"ppat.1012369.ref048","article-title":"Granulocytes: New Members of the Antigen-Presenting Cell Family.","author":"A Lin","year":"2017","journal-title":"Frontiers in immunology"},{"key":"ppat.1012369.ref049","article-title":"Phagocytosis via complement receptor 3 enables microbes to evade killing by neutrophils","author":"A Smirnov","year":"2023","journal-title":"Journal of leukocyte biology"},{"key":"ppat.1012369.ref050","article-title":"Is Neisseria gonorrhoeae initiating a future era of untreatable gonorrhea?: detailed characterization of the first strain with high-level resistance to ceftriaxone","author":"M Ohnishi","year":"2011","journal-title":"Antimicrobial agents and chemotherapy"},{"key":"ppat.1012369.ref051","article-title":"Phasevarions mediate random switching of gene expression in pathogenic Neisseria","author":"YN Srikhanta","year":"2009","journal-title":"PLoS pathogens"},{"key":"ppat.1012369.ref052","article-title":"Isolation and analysis of a fur mutant of Neisseria gonorrhoeae","author":"CE Thomas","year":"1996","journal-title":"Journal of bacteriology"},{"key":"ppat.1012369.ref053","article-title":"The gonococcal fur regulon: identification of additional genes involved in major catabolic, recombination, and secretory pathways","author":"S Sebastian","year":"2002","journal-title":"Journal of bacteriology"},{"key":"ppat.1012369.ref054","article-title":"Transcriptional and functional analysis of the Neisseria gonorrhoeae Fur regulon","author":"LA Jackson","year":"2010","journal-title":"Journal of bacteriology"},{"key":"ppat.1012369.ref055","article-title":"Investigation of oxidative stress defenses of Neisseria gonorrhoeae by using a human polymorphonuclear leukocyte survival assay","author":"KL Seib","year":"2005","journal-title":"Infect Immun"},{"key":"ppat.1012369.ref056","article-title":"Role of neutrophils in innate immunity: a systems biology-level approach.","author":"SD Kobayashi","year":"2009","journal-title":"Wiley interdisciplinary reviews Systems biology and medicine"},{"issue":"12","key":"ppat.1012369.ref057","doi-asserted-by":"crossref","first-page":"4286","DOI":"10.4049\/jimmunol.140.12.4286","article-title":"Selective synthesis of mRNA and proteins by human peripheral blood neutrophils","volume":"140","author":"RM Jack","year":"1988","journal-title":"Journal of immunology"},{"key":"ppat.1012369.ref058","article-title":"Gene expression in mature neutrophils: early responses to inflammatory stimuli","author":"X Zhang","year":"2004","journal-title":"Journal of leukocyte biology"},{"key":"ppat.1012369.ref059","article-title":"Global analysis of neutrophil responses to Neisseria gonorrhoeae reveals a self-propagating inflammatory program.","author":"A Sintsova","year":"2014","journal-title":"PLoS Pathog."},{"key":"ppat.1012369.ref060","article-title":"Selection for a CEACAM receptor-specific binding phenotype during Neisseria gonorrhoeae infection of the human genital tract","author":"A Sintsova","year":"2015","journal-title":"Infect Immun"},{"key":"ppat.1012369.ref061","article-title":"Nutritional immunity: the battle for nutrient metals at the host-pathogen interface.","author":"CC Murdoch","year":"2022","journal-title":"Nature reviews Microbiology"},{"key":"ppat.1012369.ref062","article-title":"Structural Basis for Evasion of Nutritional Immunity by the Pathogenic Neisseriae.","author":"R Yadav","year":"2020","journal-title":"Frontiers in microbiology"},{"key":"ppat.1012369.ref063","article-title":"Acclimation to Nutritional Immunity and Metal Intoxication Requires Zinc, Manganese, and Copper Homeostasis in the Pathogenic Neisseriae.","author":"AH Branch","year":"2022","journal-title":"Front Cell Infect Microbiol."},{"key":"ppat.1012369.ref064","article-title":"Iron and innate antimicrobial immunity-Depriving the pathogen, defending the host","author":"M Nairz","year":"2018","journal-title":"J Trace Elem Med Biol"},{"key":"ppat.1012369.ref065","article-title":"Subversion of nutritional immunity by the pathogenic Neisseriae","author":"CN Cornelissen","year":"2018","journal-title":"Pathog Dis"},{"key":"ppat.1012369.ref066","article-title":"Neisseria gonorrhoeae Evades Calprotectin-Mediated Nutritional Immunity and Survives Neutrophil Extracellular Traps by Production of TdfH","author":"S Jean","year":"2016","journal-title":"Infect Immun"},{"key":"ppat.1012369.ref067","article-title":"Iron uptake from lactoferrin and transferrin by Neisseria gonorrhoeae","author":"WR McKenna","year":"1988","journal-title":"Infection and immunity"},{"key":"ppat.1012369.ref068","doi-asserted-by":"crossref","first-page":"1274","DOI":"10.1128\/jb.85.6.1274-1279.1963","article-title":"Neisseria Gonorrhoeae. I. Virulence Genetically Linked to Clonal Variation.","volume":"85","author":"DS Kellogg","year":"1963","journal-title":"J Bacteriol"},{"key":"ppat.1012369.ref069","article-title":"Neisseria gonorrhoeae suppresses the oxidative burst of human polymorphonuclear leukocytes","author":"AK Criss","year":"2008","journal-title":"Cell Microbiol"},{"key":"ppat.1012369.ref070","article-title":"Immune Modulation by Human Secreted RNases at the Extracellular Space.","author":"L Lu","year":"2018","journal-title":"Frontiers in immunology"},{"key":"ppat.1012369.ref071","article-title":"Ultrafast and memory-efficient alignment of short DNA sequences to the human genome","author":"B Langmead","year":"2009","journal-title":"Genome biology"},{"key":"ppat.1012369.ref072","article-title":"HISAT: a fast spliced aligner with low memory requirements","author":"D Kim","year":"2015","journal-title":"Nature methods"},{"key":"ppat.1012369.ref073","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","author":"M Love","year":"2014","journal-title":"Genome biology"},{"key":"ppat.1012369.ref074","article-title":"Causal analysis approaches in Ingenuity Pathway Analysis","author":"A Kr\u00e4mer","year":"2014","journal-title":"Bioinformatics (Oxford, England)."},{"key":"ppat.1012369.ref075","article-title":"Gonococcal transferrin binding protein chimeras induce bactericidal and growth inhibitory antibodies in mice","author":"G Price","year":"2007","journal-title":"Vaccine"},{"key":"ppat.1012369.ref076","article-title":"Functional and structural studies on the Neisseria gonorrhoeae GmhA, the first enzyme in the glycero-manno-heptose biosynthesis pathways, demonstrate a critical role in lipooligosaccharide synthesis and gonococcal viability.","author":"IH Wierzbicki","year":"2017","journal-title":"Microbiologyopen"}],"updated-by":[{"DOI":"10.1371\/journal.ppat.1012369","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2024,7,18]],"date-time":"2024-07-18T00:00:00Z","timestamp":1721260800000}}],"container-title":["PLOS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1012369","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,7,18]],"date-time":"2024-07-18T18:04:42Z","timestamp":1721325882000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1012369"}},"subtitle":[],"editor":[{"given":"Christoph","family":"Dehio","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2024,7,8]]},"references-count":76,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2024,7,8]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1012369","relation":{"new_version":[{"id-type":"doi","id":"10.1371\/journal.ppat.1012369","asserted-by":"object"}]},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,7,8]]}}}