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Pathogenesis is attributed to a wide array of virulence factors, including several potent exotoxins such as the pore-forming \u03b1-toxin. In this study, we found that patients with\n S. aureus<\/jats:italic>\n respiratory tract infections had elevated CX\n 3<\/jats:sub>\n CL1 levels in airway fluid and plasma. Using human-organotypic lung models, we observed that stimulation of lung epithelium with \u03b1-toxin induces an intensified CX\n 3<\/jats:sub>\n CL1 expression apically in the epithelium as well as the release of CX\n 3<\/jats:sub>\n CL1. Blocking \u03b1-toxin or ADAM10 activity in organotypic lung using an \u03b1-toxin-blocking antibody or a specific ADAM10 inhibitor confirmed their role in modulating CX\n 3<\/jats:sub>\n CL1 cleavage and release. Analyses of CD14\n +<\/jats:sup>\n human monocytes in combination with a CX\n 3<\/jats:sub>\n CR1 inhibitor revealed that \u03b1-toxin-mediated CX\n 3<\/jats:sub>\n CL1 release induces CX\n 3<\/jats:sub>\n CL1-dependent chemotaxis. In line with these data, lung tissue from patients with\n S. aureus<\/jats:italic>\n respiratory tract infection showed elevated CX\n 3<\/jats:sub>\n CL1 and CD14 staining as compared with tissue from patients with non-infectious lung diseases. Functional studies of monocytes showed that CX\n 3<\/jats:sub>\n CL1 released by lung models resulted in upregulated CD83 and downregulated CD86, as well as impaired killing of phagocytosed\n S. aureus<\/jats:italic>\n . Furthermore, stimulation of monocytes with soluble CX\n 3<\/jats:sub>\n CL1 hampered their reactive-oxygen and nitric-oxide production. Taken together our data show that\n S. aureus<\/jats:italic>\n triggers the release of lung epithelial CX\n 3<\/jats:sub>\n CL1, and we identify an immunomodulatory effect of \u03b1-toxin involving its cytotoxic and ADAM10-interacting properties, inducing CX\n 3<\/jats:sub>\n CL1 release leading to impaired monocyte effector function.\n <\/jats:p>\n \n IMPORTANCE<\/jats:title>\n \n Exotoxins are essential virulence factors for the pathobiont\n S. aureus<\/jats:italic>\n and contribute toward severe invasive infections such as pneumonia.\n S. aureus<\/jats:italic>\n \u03b1-toxin is a pore-forming exotoxin that causes host cell lysis and severe lung pathology. We found that \u03b1-toxin drives the release of membrane-bound chemokine CX\n 3<\/jats:sub>\n CL1 by involving ADAM10-mediated proteolytic activity. Furthermore, the release of CX\n 3<\/jats:sub>\n CL1 modulated immune responses locally, as demonstrated by enhanced monocyte migration and reduced capacity of monocytes to kill ingested bacteria. CX\n 3<\/jats:sub>\n CL1-induced reduction in bacterial killing coincided with impaired production of reactive oxygen and nitric oxide species. This reveals a novel mechanism in the pathogenesis of\n S. aureus<\/jats:italic>\n lung infections involving \u03b1-toxin-induced release of CX\n 3<\/jats:sub>\n CL1, leading to impaired bacterial killing by monocytes.\n <\/jats:p>\n <\/jats:sec>\n <\/jats:sec>","DOI":"10.1128\/mbio.02689-25","type":"journal-article","created":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T13:01:19Z","timestamp":1760360479000},"update-policy":"https:\/\/doi.org\/10.1128\/asmj-crossmark-policy-page","source":"Crossref","is-referenced-by-count":4,"title":["Alpha-toxin-elicited CX\n 3<\/sub>\n CL1 release in\n Staphylococcus aureus<\/i>\n pneumonia impairs bactericidal function of human monocytes"],"prefix":"10.1128","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0527-3978","authenticated-orcid":true,"given":"Srikanth","family":"Mairpady Shambat","sequence":"first","affiliation":[{"id":[{"id":"https:\/\/ror.org\/00m8d6786","id-type":"ROR","asserted-by":"publisher"}],"name":"Center 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