{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,25]],"date-time":"2026-04-25T07:05:14Z","timestamp":1777100714891,"version":"3.51.4"},"reference-count":29,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,5,12]],"date-time":"2022-05-12T00:00:00Z","timestamp":1652313600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Cell. Infect. Microbiol."],"abstract":"<jats:p>Pertussis is a respiratory infection caused by the Gram-negative bacterium <jats:italic>Bordetella pertussis<\/jats:italic>. Despite high vaccination coverage this disease remains a public health concern worldwide. A better understanding of the protective immune responses to <jats:italic>B. pertussis<\/jats:italic> is required for the development of improved vaccines. The aim of this study was to determine the production of reactive oxygen species (ROS) by human neutrophils in response to <jats:italic>B. pertussis<\/jats:italic> and to determine the contribution of opsonizing antibodies from convalescent pertussis patients in this response. The serum samples from convalescent patients were taken at &amp;lt;3, 9, 18 and 36 months after diagnosis of pertussis. Also included were sera from healthy age-matched controls. We show that neutrophils produced high levels of ROS in response to opsonized, compared to non-opsonized, <jats:italic>B. pertussis<\/jats:italic> and that this effect was independent of the time the convalescent serum samples were taken. This indicates the presence of functional opsonizing antibodies up to 3 years after <jats:italic>B. pertussis<\/jats:italic> infection. While opsonization of <jats:italic>B. pertussis<\/jats:italic> with serum samples from uninfected controls also induced ROS production, sera from infected individuals induced significantly higher ROS levels. Spearman correlations analysis showed that IgG antibodies targeting fimbriae3 followed by pertactin, and BrkA correlate with ROS production. Additionally, we observed that neutrophils killed opsonized <jats:italic>B. pertussis<\/jats:italic> in a ROS-dependent manner. Searching for other antigen-specific antibodies from convalescent pertussis patients involved in ROS production by neutrophils may assist in the identification of novel antigens to improve the current pertussis vaccines.<\/jats:p>","DOI":"10.3389\/fcimb.2022.888412","type":"journal-article","created":{"date-parts":[[2022,5,12]],"date-time":"2022-05-12T06:22:18Z","timestamp":1652336538000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":7,"title":["Long Lasting Antibodies From Convalescent Pertussis Patients Induce ROS Production and Bacterial Killing by Human Neutrophils"],"prefix":"10.3389","volume":"12","author":[{"given":"Michiel M.","family":"Kroes","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lars C.","family":"van Vliet","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ronald H. J.","family":"Jacobi","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Betsy","family":"Kuipers","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Daan K. J.","family":"Pieren","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Alberto","family":"Miranda-Bedate","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"C\u00e9cile A. C. M.","family":"van Els","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elena","family":"Pinelli","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1965","published-online":{"date-parts":[[2022,5,12]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"783","DOI":"10.1016\/j.cell.2006.02.015","article-title":"Pathogen Recognition and Innate Immunity","volume":"124","author":"Akira","year":"2006","journal-title":"Cell"},{"key":"B2","doi-asserted-by":"publisher","first-page":"1182","DOI":"10.1128\/IAI.01150-08","article-title":"Role of Neutrophils in Response to Bordetella Pertussis Infection in Mice","volume":"77","author":"Andreasen","year":"2009","journal-title":"Infect. Immun."},{"key":"B3","doi-asserted-by":"publisher","first-page":"935","DOI":"10.1182\/blood-2007-12-077917","article-title":"The Phagocytes: Neutrophils and Monocytes","volume":"112","author":"Dale","year":"2008","journal-title":"Blood"},{"key":"B4","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1189\/jlb.0605338","article-title":"Common Methodology is Inadequate for Studies on the Microbicidal Activity of Neutrophils","volume":"79","author":"Decleva","year":"2006","journal-title":"J. Leukoc. Biol."},{"key":"B5","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0014183","article-title":"Seroprevalence of Pertussis in The Netherlands: Evidence for Increased Circulation of Bordetella Pertussis","volume":"5","author":"de Greeff","year":"2010","journal-title":"PloS One"},{"key":"B6","doi-asserted-by":"publisher","first-page":"657","DOI":"10.1189\/jlb.1012544","article-title":"ROS Production in Phagocytes: Why, When, and Where","volume":"94","author":"Dupre-Crochet","year":"2013","journal-title":"J. Leukoc. Biol."},{"key":"B7","doi-asserted-by":"publisher","DOI":"10.1093\/femspd\/ftv081","article-title":"Review of the Neutrophil Response to Bordetella Pertussis Infection","volume":"73","author":"Eby","year":"2015","journal-title":"Pathog. Dis."},{"key":"B8","doi-asserted-by":"publisher","first-page":"12039","DOI":"10.1038\/s41598-018-30558-8","article-title":"Detection of Opsonizing Antibodies Directed Against a Recently Circulating Bordetella Pertussis Strain in Paired Plasma Samples From Symptomatic and Recovered Pertussis Patients","volume":"8","author":"Hovingh","year":"2018","journal-title":"Sci. Rep."},{"key":"B9","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.02030","article-title":"Activation of Human NK Cells by Bordetella Pertussis Requires Inflammasome Activation in Macrophages","volume":"10","author":"Kroes","year":"2019","journal-title":"Front. Immunol."},{"key":"B10","doi-asserted-by":"publisher","first-page":"1358","DOI":"10.1080\/22221751.2021.1943537","article-title":"Naturally Circulating Pertactin-Deficient Bordetella Pertussis Strains Induce Distinct Gene Expression and Inflammatory Signatures in Human Dendritic Cells","volume":"10","author":"Kroes","year":"2021","journal-title":"Emerging. Microbes Infect."},{"key":"B11","doi-asserted-by":"publisher","first-page":"515","DOI":"10.1038\/s41577-020-0407-1","article-title":"Tissue Damage From Neutrophil-Induced Oxidative Stress in COVID-19","volume":"20","author":"Laforge","year":"2020","journal-title":"Nat. Rev. Immunol."},{"key":"B12","doi-asserted-by":"publisher","first-page":"956","DOI":"10.1128\/iai.68.2.956-959.2000","article-title":"Phagocytosed Bordetella Pertussis Fails to Survive in Human Neutrophils","volume":"68","author":"Lenz","year":"2000","journal-title":"Infect. Immun."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2020.02108","article-title":"Acellular Pertussis Vaccines Induce Anti-Pertactin Bactericidal Antibodies Which Drives the Emergence of Pertactin-Negative Strains","volume":"11","author":"Lesne","year":"2020","journal-title":"Front. Microbiol."},{"key":"B14","doi-asserted-by":"publisher","first-page":"S34","DOI":"10.1016\/j.jinf.2016.04.020","article-title":"Pertussis: Where did We Go Wrong and What can We do About it","author":"Locht","year":"2016","journal-title":"J. Infect."},{"key":"B15","doi-asserted-by":"publisher","first-page":"274","DOI":"10.1038\/nrmicro3235","article-title":"Bordetella Pertussis Pathogenesis: Current and Future Challenges","volume":"12","author":"Melvin","year":"2014","journal-title":"Nat. Rev. Microbiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"349","DOI":"10.1038\/nri3423","article-title":"Beyond Oxidative Stress: An Immunologist's Guide to Reactive Oxygen Species","volume":"13","author":"Nathan","year":"2013","journal-title":"Nat. Rev. Immunol."},{"key":"B17","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2017.00373","article-title":"Neutrophils to the ROScue: Mechanisms of NADPH Oxidase Activation and Bacterial Resistance","volume":"7","author":"Nguyen","year":"2017","journal-title":"Front. Cell Infect. Microbiol."},{"key":"B18","doi-asserted-by":"crossref","first-page":"311","DOI":"10.1128\/9781555819453.ch17","article-title":"Bordetella Pertussis","volume-title":"Emerging Infections 10","author":"Nieves","year":"2016"},{"key":"B19","doi-asserted-by":"publisher","first-page":"328","DOI":"10.1086\/589753","article-title":"Pathology and Pathogenesis of Fatal Bordetella Pertussis Infection in Infants","volume":"47","author":"Paddock","year":"2008","journal-title":"Clin. Infect. Dis."},{"key":"B20","doi-asserted-by":"publisher","first-page":"134","DOI":"10.1038\/nri.2017.105","article-title":"Neutrophil Extracellular Traps in Immunity and Disease","volume":"18","author":"Papayannopoulos","year":"2018","journal-title":"Nat. Rev. Immunol."},{"key":"B21","doi-asserted-by":"publisher","first-page":"429","DOI":"10.3390\/vaccines8030429","article-title":"The Role of Virulence Proteins in Protection Conferred by Bordetella Pertussis Outer Membrane Vesicle Vaccines","volume":"8","author":"Raeven","year":"2020","journal-title":"Vaccines (Basel)."},{"key":"B22","doi-asserted-by":"publisher","first-page":"6545","DOI":"10.4049\/jimmunol.167.11.6545","article-title":"Fc Receptor-Mediated Immunity Against Bordetella Pertussis","volume":"167","author":"Rodriguez","year":"2001","journal-title":"J. Immunol."},{"key":"B23","doi-asserted-by":"publisher","first-page":"2017","DOI":"10.1128\/iai.69.4.2017-2024.2001","article-title":"Chemokine-Dependent Neutrophil Recruitment in a Murine Model of Legionella Pneumonia: Potential Role of Neutrophils as Immunoregulatory Cells","volume":"69","author":"Tateda","year":"2001","journal-title":"Infect. Immun."},{"key":"B24","doi-asserted-by":"publisher","first-page":"4289","DOI":"10.1128\/iai.68.7.4289-4296.2000","article-title":"CXC Chemokine Receptor CXCR2 is Essential for Protective Innate Host Response in Murine Pseudomonas Aeruginosa Pneumonia","volume":"68","author":"Tsai","year":"2000","journal-title":"Infect. Immun."},{"key":"B25","doi-asserted-by":"publisher","DOI":"10.1038\/srep40328","article-title":"Impact of Age and Vaccination History on Long-Term Serological Responses After Symptomatic B. Pertussis Infection, a High Dimensional Data Analysis","volume":"7","author":"van Twillert","year":"2017","journal-title":"Sci. Rep."},{"key":"B26","doi-asserted-by":"publisher","first-page":"101","DOI":"10.3102\/10769986025002101","article-title":"A Critique and Improvement of the CL Common Language Effect Size Statistics of McGraw and Wong","volume":"25","author":"Vargha","year":"2000","journal-title":"J. Educ. Behav. Stat"},{"key":"B27","doi-asserted-by":"publisher","first-page":"519","DOI":"10.1084\/jem.194.4.519","article-title":"Requirement of Interleukin 17 Receptor Signaling for Lung CXC Chemokine and Granulocyte Colony-Stimulating Factor Expression, Neutrophil Recruitment, and Host Defense","volume":"194","author":"Ye","year":"2001","journal-title":"J. Exp. Med."},{"key":"B28","doi-asserted-by":"publisher","first-page":"974","DOI":"10.1016\/s1473-3099(17)30390-0","article-title":"An Update of the Global Burden of Pertussis in Children Younger Than 5 Years: A Modelling Study","volume":"17","author":"Yeung","year":"2017","journal-title":"Lancet Infect. Dis."},{"key":"B29","doi-asserted-by":"publisher","first-page":"2371","DOI":"10.1128\/iai.00336-13","article-title":"The Stimulated Innate Resistance Event in Bordetella Pertussis Infection is Dependent on Reactive Oxygen Species Production","volume":"81","author":"Zurita","year":"2013","journal-title":"Infect. Immun."}],"container-title":["Frontiers in Cellular and Infection Microbiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2022.888412\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,5,12]],"date-time":"2022-05-12T06:22:22Z","timestamp":1652336542000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fcimb.2022.888412\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,5,12]]},"references-count":29,"alternative-id":["10.3389\/fcimb.2022.888412"],"URL":"https:\/\/doi.org\/10.3389\/fcimb.2022.888412","relation":{},"ISSN":["2235-2988"],"issn-type":[{"value":"2235-2988","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,5,12]]},"article-number":"888412"}}