Alexandra O Johnson, Braden M Shipman, Benjamin C Hunt, Brian S Learman, Aimee L Brauer, Serena P Zhou, Rachael Hageman Blair, Nicole J De Nisco, Chelsie E Armbruster
{"title":"两种假定的粪肠球菌糖胺聚糖降解酶的功能及其对菌血症和导管相关性尿路感染的影响。","authors":"Alexandra O Johnson, Braden M Shipman, Benjamin C Hunt, Brian S Learman, Aimee L Brauer, Serena P Zhou, Rachael Hageman Blair, Nicole J De Nisco, Chelsie E Armbruster","doi":"10.1128/iai.00199-24","DOIUrl":null,"url":null,"abstract":"<p><p><i>Enterococcus faecalis</i> is a common cause of healthcare-acquired bloodstream infections and catheter-associated urinary tract infections (CAUTIs) in both adults and children. Treatment of <i>E. faecalis</i> infection is frequently complicated by multi-drug resistance. Based on protein homology, <i>E. faecalis</i> encodes two putative hyaluronidases, EF3023 (HylA) and EF0818 (HylB). In other Gram-positive pathogens, hyaluronidases have been shown to contribute to tissue damage and immune evasion, but the function in <i>E. faecalis</i> has yet to be explored. Here, we show that both <i>hylA</i> and <i>hylB</i> contribute to <i>E. faecalis</i> pathogenesis. In a CAUTI model, Δ<i>hylA</i> exhibited defects in bladder colonization and dissemination to the bloodstream, and Δ<i>hylB</i> exhibited a defect in kidney colonization. Furthermore, a Δ<i>hylA</i>Δ<i>hylB</i> double mutant exhibited a severe colonization defect in a model of bacteremia while the single mutants colonized to a similar level as the wild-type strain, suggesting potential functional redundancy within the bloodstream. We next examined enzymatic activity, and demonstrate that HylB is capable of digesting both hyaluronic acid (HA) and chondroitin sulfate <i>in vitro</i>, while HylA exhibits only a very modest activity against heparin. Importantly, HA degradation by HylB provided a modest increase in cell density during the stationary phase and also contributed to dampening of lipopolysaccharide-mediated NF-κB activation. Overall, these data demonstrate that glycosaminoglycan degradation is important for <i>E. faecalis</i> pathogenesis in the urinary tract and during bloodstream infection.</p>","PeriodicalId":13541,"journal":{"name":"Infection and Immunity","volume":" ","pages":"e0019924"},"PeriodicalIF":2.9000,"publicationDate":"2024-07-11","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11238560/pdf/","citationCount":"0","resultStr":"{\"title\":\"Function and contribution of two putative <i>Enterococcus faecalis</i> glycosaminoglycan degrading enzymes to bacteremia and catheter-associated urinary tract infection.\",\"authors\":\"Alexandra O Johnson, Braden M Shipman, Benjamin C Hunt, Brian S Learman, Aimee L Brauer, Serena P Zhou, Rachael Hageman Blair, Nicole J De Nisco, Chelsie E Armbruster\",\"doi\":\"10.1128/iai.00199-24\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p><i>Enterococcus faecalis</i> is a common cause of healthcare-acquired bloodstream infections and catheter-associated urinary tract infections (CAUTIs) in both adults and children. Treatment of <i>E. faecalis</i> infection is frequently complicated by multi-drug resistance. Based on protein homology, <i>E. faecalis</i> encodes two putative hyaluronidases, EF3023 (HylA) and EF0818 (HylB). In other Gram-positive pathogens, hyaluronidases have been shown to contribute to tissue damage and immune evasion, but the function in <i>E. faecalis</i> has yet to be explored. Here, we show that both <i>hylA</i> and <i>hylB</i> contribute to <i>E. faecalis</i> pathogenesis. In a CAUTI model, Δ<i>hylA</i> exhibited defects in bladder colonization and dissemination to the bloodstream, and Δ<i>hylB</i> exhibited a defect in kidney colonization. Furthermore, a Δ<i>hylA</i>Δ<i>hylB</i> double mutant exhibited a severe colonization defect in a model of bacteremia while the single mutants colonized to a similar level as the wild-type strain, suggesting potential functional redundancy within the bloodstream. We next examined enzymatic activity, and demonstrate that HylB is capable of digesting both hyaluronic acid (HA) and chondroitin sulfate <i>in vitro</i>, while HylA exhibits only a very modest activity against heparin. Importantly, HA degradation by HylB provided a modest increase in cell density during the stationary phase and also contributed to dampening of lipopolysaccharide-mediated NF-κB activation. Overall, these data demonstrate that glycosaminoglycan degradation is important for <i>E. faecalis</i> pathogenesis in the urinary tract and during bloodstream infection.</p>\",\"PeriodicalId\":13541,\"journal\":{\"name\":\"Infection and Immunity\",\"volume\":\" \",\"pages\":\"e0019924\"},\"PeriodicalIF\":2.9000,\"publicationDate\":\"2024-07-11\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11238560/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Infection and Immunity\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1128/iai.00199-24\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"2024/6/6 0:00:00\",\"PubModel\":\"Epub\",\"JCR\":\"Q3\",\"JCRName\":\"IMMUNOLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Infection and Immunity","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1128/iai.00199-24","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"2024/6/6 0:00:00","PubModel":"Epub","JCR":"Q3","JCRName":"IMMUNOLOGY","Score":null,"Total":0}
Function and contribution of two putative Enterococcus faecalis glycosaminoglycan degrading enzymes to bacteremia and catheter-associated urinary tract infection.
Enterococcus faecalis is a common cause of healthcare-acquired bloodstream infections and catheter-associated urinary tract infections (CAUTIs) in both adults and children. Treatment of E. faecalis infection is frequently complicated by multi-drug resistance. Based on protein homology, E. faecalis encodes two putative hyaluronidases, EF3023 (HylA) and EF0818 (HylB). In other Gram-positive pathogens, hyaluronidases have been shown to contribute to tissue damage and immune evasion, but the function in E. faecalis has yet to be explored. Here, we show that both hylA and hylB contribute to E. faecalis pathogenesis. In a CAUTI model, ΔhylA exhibited defects in bladder colonization and dissemination to the bloodstream, and ΔhylB exhibited a defect in kidney colonization. Furthermore, a ΔhylAΔhylB double mutant exhibited a severe colonization defect in a model of bacteremia while the single mutants colonized to a similar level as the wild-type strain, suggesting potential functional redundancy within the bloodstream. We next examined enzymatic activity, and demonstrate that HylB is capable of digesting both hyaluronic acid (HA) and chondroitin sulfate in vitro, while HylA exhibits only a very modest activity against heparin. Importantly, HA degradation by HylB provided a modest increase in cell density during the stationary phase and also contributed to dampening of lipopolysaccharide-mediated NF-κB activation. Overall, these data demonstrate that glycosaminoglycan degradation is important for E. faecalis pathogenesis in the urinary tract and during bloodstream infection.
期刊介绍:
Infection and Immunity (IAI) provides new insights into the interactions between bacterial, fungal and parasitic pathogens and their hosts. Specific areas of interest include mechanisms of molecular pathogenesis, virulence factors, cellular microbiology, experimental models of infection, host resistance or susceptibility, and the generation of innate and adaptive immune responses. IAI also welcomes studies of the microbiome relating to host-pathogen interactions.