Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection
Extraintestinal pathogenic Escherichia coli (ExPEC) is one of the leading causes of bloodstream infections in a broad spectrum of birds and mammals, thus poses a great threat to public health, while its underlying mechanism causing sepsis is not fully understood. Here we reported a high virulent ExP...
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Frontiers Media S.A.
2023-02-01
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| Series: | Frontiers in Cellular and Infection Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fcimb.2023.1138801/full |
| _version_ | 1797905175195680768 |
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| author | Xinming Pan Xinming Pan Xinming Pan Rong Chen Rong Chen Rong Chen Yating Zhang Yating Zhang Yating Zhang Yinchu Zhu Jin Zhao Huochun Yao Huochun Yao Huochun Yao Jiale Ma Jiale Ma Jiale Ma |
| author_facet | Xinming Pan Xinming Pan Xinming Pan Rong Chen Rong Chen Rong Chen Yating Zhang Yating Zhang Yating Zhang Yinchu Zhu Jin Zhao Huochun Yao Huochun Yao Huochun Yao Jiale Ma Jiale Ma Jiale Ma |
| author_sort | Xinming Pan |
| collection | DOAJ |
| description | Extraintestinal pathogenic Escherichia coli (ExPEC) is one of the leading causes of bloodstream infections in a broad spectrum of birds and mammals, thus poses a great threat to public health, while its underlying mechanism causing sepsis is not fully understood. Here we reported a high virulent ExPEC strain PU-1, which has a robust ability to colonize within host bloodstream, while induced a low level of leukocytic activation. Two serine protease autotransporters of Enterobacteriaceae (SPATEs), VatPU-1 and TshPU-1, were found to play critical roles for the urgent blood infection of strain PU-1. Although the Vat and Tsh homologues have been identified as virulence factors of ExPEC, their contributions to bloodstream infection are still unclear. In this study, VatPU-1 and TshPU-1 were verified to interact with the hemoglobin (a well-known mucin-like glycoprotein in red blood cell), degrade the mucins of host respiratory tract, and cleave the CD43 (a major cell surface component sharing similar O-glycosylated modifications with other glycoprotein expressed on leukocytes), suggesting that these two SPATEs have the common activity to cleave a broad array of mucin-like O-glycoproteins. These cleavages significantly impaired the chemotaxis and transmigration of leukocytes, and then inhibited the activation of diverse immune responses coordinately, especially downregulated the leukocytic and inflammatory activation during bloodstream infection, thus might mediate the evasion of ExPEC from immune clearance of blood leukocytes. Taken together, these two SPATEs play critical roles to cause a heavy bacterial load within bloodstream via immunomodulation of leukocytes, which provides a more comprehensive understanding how ExPEC colonize within host bloodstream and cause severe sepsis. |
| first_indexed | 2024-04-10T10:00:53Z |
| format | Article |
| id | doaj.art-276737b7e1134ece9a870cb404a5d2e0 |
| institution | Directory Open Access Journal |
| issn | 2235-2988 |
| language | English |
| last_indexed | 2024-04-10T10:00:53Z |
| publishDate | 2023-02-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular and Infection Microbiology |
| spelling | doaj.art-276737b7e1134ece9a870cb404a5d2e02023-02-16T08:18:19ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882023-02-011310.3389/fcimb.2023.11388011138801Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infectionXinming Pan0Xinming Pan1Xinming Pan2Rong Chen3Rong Chen4Rong Chen5Yating Zhang6Yating Zhang7Yating Zhang8Yinchu Zhu9Jin Zhao10Huochun Yao11Huochun Yao12Huochun Yao13Jiale Ma14Jiale Ma15Jiale Ma16Ministry of Education (MOE) Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaKey Lab of Animal Bacteriology, Ministry of Agriculture, Nanjing, ChinaOffice International Des (OIE) Reference Lab for Swine Streptococcosis, Nanjing Agricultural University, Nanjing, ChinaMinistry of Education (MOE) Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaKey Lab of Animal Bacteriology, Ministry of Agriculture, Nanjing, ChinaOffice International Des (OIE) Reference Lab for Swine Streptococcosis, Nanjing Agricultural University, Nanjing, ChinaMinistry of Education (MOE) Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaKey Lab of Animal Bacteriology, Ministry of Agriculture, Nanjing, ChinaOffice International Des (OIE) Reference Lab for Swine Streptococcosis, Nanjing Agricultural University, Nanjing, ChinaInstitute of Animal Husbandry and Veterinary Sciences, Zhejiang Academy of Agricultural Sciences, Hangzhou, ChinaDepartment of Animal Science, Yuxi Agriculture Vocation-Technical College, Yuxi, ChinaMinistry of Education (MOE) Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaKey Lab of Animal Bacteriology, Ministry of Agriculture, Nanjing, ChinaOffice International Des (OIE) Reference Lab for Swine Streptococcosis, Nanjing Agricultural University, Nanjing, ChinaMinistry of Education (MOE) Joint International Research Laboratory of Animal Health and Food Safety, College of Veterinary Medicine, Nanjing Agricultural University, Nanjing, ChinaKey Lab of Animal Bacteriology, Ministry of Agriculture, Nanjing, ChinaOffice International Des (OIE) Reference Lab for Swine Streptococcosis, Nanjing Agricultural University, Nanjing, ChinaExtraintestinal pathogenic Escherichia coli (ExPEC) is one of the leading causes of bloodstream infections in a broad spectrum of birds and mammals, thus poses a great threat to public health, while its underlying mechanism causing sepsis is not fully understood. Here we reported a high virulent ExPEC strain PU-1, which has a robust ability to colonize within host bloodstream, while induced a low level of leukocytic activation. Two serine protease autotransporters of Enterobacteriaceae (SPATEs), VatPU-1 and TshPU-1, were found to play critical roles for the urgent blood infection of strain PU-1. Although the Vat and Tsh homologues have been identified as virulence factors of ExPEC, their contributions to bloodstream infection are still unclear. In this study, VatPU-1 and TshPU-1 were verified to interact with the hemoglobin (a well-known mucin-like glycoprotein in red blood cell), degrade the mucins of host respiratory tract, and cleave the CD43 (a major cell surface component sharing similar O-glycosylated modifications with other glycoprotein expressed on leukocytes), suggesting that these two SPATEs have the common activity to cleave a broad array of mucin-like O-glycoproteins. These cleavages significantly impaired the chemotaxis and transmigration of leukocytes, and then inhibited the activation of diverse immune responses coordinately, especially downregulated the leukocytic and inflammatory activation during bloodstream infection, thus might mediate the evasion of ExPEC from immune clearance of blood leukocytes. Taken together, these two SPATEs play critical roles to cause a heavy bacterial load within bloodstream via immunomodulation of leukocytes, which provides a more comprehensive understanding how ExPEC colonize within host bloodstream and cause severe sepsis.https://www.frontiersin.org/articles/10.3389/fcimb.2023.1138801/fullextraintestinal pathogenic E. colibloodstreamserine protease autotransporterimmunomodulationmucin-like glycoprotein |
| spellingShingle | Xinming Pan Xinming Pan Xinming Pan Rong Chen Rong Chen Rong Chen Yating Zhang Yating Zhang Yating Zhang Yinchu Zhu Jin Zhao Huochun Yao Huochun Yao Huochun Yao Jiale Ma Jiale Ma Jiale Ma Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection Frontiers in Cellular and Infection Microbiology extraintestinal pathogenic E. coli bloodstream serine protease autotransporter immunomodulation mucin-like glycoprotein |
| title | Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection |
| title_full | Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection |
| title_fullStr | Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection |
| title_full_unstemmed | Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection |
| title_short | Porcine extraintestinal pathogenic Escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection |
| title_sort | porcine extraintestinal pathogenic escherichia coli delivers two serine protease autotransporters coordinately optimizing the bloodstream infection |
| topic | extraintestinal pathogenic E. coli bloodstream serine protease autotransporter immunomodulation mucin-like glycoprotein |
| url | https://www.frontiersin.org/articles/10.3389/fcimb.2023.1138801/full |
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