Lactate production by Staphylococcus aureus biofilm inhibits HDAC11 to reprogramme the host immune response during persistent infection

Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment. It is known that host leukocyte IL-10 production is required for S. aureus biofilm persistence in PJI. An S. aureus bursa aurealis Tn library...

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Published inNature microbiology Vol. 5; no. 10; pp. 1271 - 1284
Main Authors Heim, Cortney E., Bosch, Megan E., Yamada, Kelsey J., Aldrich, Amy L., Chaudhari, Sujata S., Klinkebiel, David, Gries, Casey M., Alqarzaee, Abdulelah A., Li, Yixuan, Thomas, Vinai C., Seto, Edward, Karpf, Adam R., Kielian, Tammy
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.10.2020
Nature Publishing Group
Subjects
13/1
13/106
13/21
13/31
38/39
38/91
631/250/255
631/250/262
631/326/41
631/326/46
64/110
64/60
Acetylation
Bacteria
Biofilms
Biomarkers
Biomedical and Life Sciences
Biosynthetic Pathways
Cell culture
Cytokines - metabolism
Epigenetics
Histone deacetylase
Histone Deacetylases - metabolism
Host-Pathogen Interactions - immunology
Immune response
Infectious Diseases
Inflammation Mediators - metabolism
Interleukin 10
Joint diseases
Lactic acid
Lactic Acid - metabolism
Life Sciences
Macrophages
Macrophages - immunology
Macrophages - metabolism
Medical Microbiology
Microbiology
Monocytes
Mutants
Myeloid-Derived Suppressor Cells - immunology
Myeloid-Derived Suppressor Cells - metabolism
Parasitology
Penicillin
Staphylococcal Infections - immunology
Staphylococcal Infections - metabolism
Staphylococcal Infections - microbiology
Staphylococcus aureus
Staphylococcus aureus - physiology
Suppressor cells
Synovial fluid
Transcription
Virology
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Abstract Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment. It is known that host leukocyte IL-10 production is required for S. aureus biofilm persistence in PJI. An S. aureus bursa aurealis Tn library consisting of 1,952 non-essential genes was screened for mutants that failed to induce IL-10 in myeloid-derived suppressor cells (MDSCs), which identified a critical role for bacterial lactic acid biosynthesis. We generated an S. aureus ddh/ldh1/ldh2 triple Tn mutant that cannot produce d - or l -lactate. Co-culture of MDSCs or macrophages with ddh/ldh1/ldh2 mutant biofilm produced substantially less IL-10 compared with wild-type S. aureus , which was also observed in a mouse model of PJI and led to reduced biofilm burden. Using MDSCs recovered from the mouse PJI model and in vitro leukocyte–biofilm co-cultures, we show that bacterial-derived lactate inhibits histone deacetylase 11, causing unchecked HDAC6 activity and increased histone 3 acetylation at the Il-10 promoter, resulting in enhanced Il-10 transcription in MDSCs and macrophages. Finally, we show that synovial fluid of patients with PJI contains elevated amounts of d -lactate and IL-10 compared with control subjects, and bacterial lactate increases IL-10 production by human monocyte-derived macrophages. Bacteria-derived lactate mediates inhibition of HDAC11 during Staphylococcus aureus biofilm infections, resulting in epigenetic changes that reprogramme the host immune response.
AbstractList Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment. It is known that host leukocyte IL-10 production is required for S. aureus biofilm persistence in PJI. An S. aureus bursa aurealis Tn library consisting of 1,952 non-essential genes was screened for mutants that failed to induce IL-10 in myeloid-derived suppressor cells (MDSCs), which identified a critical role for bacterial lactic acid biosynthesis. We generated an S. aureus ddh/ldh1/ldh2 triple Tn mutant that cannot produce D- or L-lactate. Co-culture of MDSCs or macrophages with ddh/ldh1/ldh2 mutant biofilm produced substantially less IL-10 compared with wild-type S. aureus, which was also observed in a mouse model of PJI and led to reduced biofilm burden. Using MDSCs recovered from the mouse PJI model and in vitro leukocyte-biofilm co-cultures, we show that bacterial-derived lactate inhibits histone deacetylase 11, causing unchecked HDAC6 activity and increased histone 3 acetylation at the Il-10 promoter, resulting in enhanced Il-10 transcription in MDSCs and macrophages. Finally, we show that synovial fluid of patients with PJI contains elevated amounts of D-lactate and IL-10 compared with control subjects, and bacterial lactate increases IL-10 production by human monocyte-derived macrophages.Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment. It is known that host leukocyte IL-10 production is required for S. aureus biofilm persistence in PJI. An S. aureus bursa aurealis Tn library consisting of 1,952 non-essential genes was screened for mutants that failed to induce IL-10 in myeloid-derived suppressor cells (MDSCs), which identified a critical role for bacterial lactic acid biosynthesis. We generated an S. aureus ddh/ldh1/ldh2 triple Tn mutant that cannot produce D- or L-lactate. Co-culture of MDSCs or macrophages with ddh/ldh1/ldh2 mutant biofilm produced substantially less IL-10 compared with wild-type S. aureus, which was also observed in a mouse model of PJI and led to reduced biofilm burden. Using MDSCs recovered from the mouse PJI model and in vitro leukocyte-biofilm co-cultures, we show that bacterial-derived lactate inhibits histone deacetylase 11, causing unchecked HDAC6 activity and increased histone 3 acetylation at the Il-10 promoter, resulting in enhanced Il-10 transcription in MDSCs and macrophages. Finally, we show that synovial fluid of patients with PJI contains elevated amounts of D-lactate and IL-10 compared with control subjects, and bacterial lactate increases IL-10 production by human monocyte-derived macrophages.
Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment. It is known that host leukocyte IL-10 production is required for S. aureus biofilm persistence in PJI. An S. aureus bursa aurealis Tn library consisting of 1,952 non-essential genes was screened for mutants that failed to induce IL-10 in myeloid-derived suppressor cells (MDSCs), which identified a critical role for bacterial lactic acid biosynthesis. We generated an S. aureus ddh/ldh1/ldh2 triple Tn mutant that cannot produce d - or l -lactate. Co-culture of MDSCs or macrophages with ddh/ldh1/ldh2 mutant biofilm produced substantially less IL-10 compared with wild-type S. aureus , which was also observed in a mouse model of PJI and led to reduced biofilm burden. Using MDSCs recovered from the mouse PJI model and in vitro leukocyte–biofilm co-cultures, we show that bacterial-derived lactate inhibits histone deacetylase 11, causing unchecked HDAC6 activity and increased histone 3 acetylation at the Il-10 promoter, resulting in enhanced Il-10 transcription in MDSCs and macrophages. Finally, we show that synovial fluid of patients with PJI contains elevated amounts of d -lactate and IL-10 compared with control subjects, and bacterial lactate increases IL-10 production by human monocyte-derived macrophages. Bacteria-derived lactate mediates inhibition of HDAC11 during Staphylococcus aureus biofilm infections, resulting in epigenetic changes that reprogramme the host immune response.
Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment. It is known that host leukocyte IL-10 production is required for S. aureus biofilm persistence in PJI. An S. aureus bursa aurealis Tn library consisting of 1,952 non-essential genes was screened for mutants that failed to induce IL-10 in myeloid-derived suppressor cells (MDSCs), which identified a critical role for bacterial lactic acid biosynthesis. We generated an S. aureus ddh/ldh1/ldh2 triple Tn mutant that cannot produce D- or L-lactate. Co-culture of MDSCs or macrophages with ddh/ldh1/ldh2 mutant biofilm produced substantially less IL-10 compared with wild-type S. aureus, which was also observed in a mouse model of PJI and led to reduced biofilm burden. Using MDSCs recovered from the mouse PJI model and in vitro leukocyte-biofilm co-cultures, we show that bacterial-derived lactate inhibits histone deacetylase 11, causing unchecked HDAC6 activity and increased histone 3 acetylation at the Il-10 promoter, resulting in enhanced Il-10 transcription in MDSCs and macrophages. Finally, we show that synovial fluid of patients with PJI contains elevated amounts of D-lactate and IL-10 compared with control subjects, and bacterial lactate increases IL-10 production by human monocyte-derived macrophages.
Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment. It is known that host leukocyte IL-10 production is required for S. aureus biofilm persistence in PJI. An S. aureus bursa aurealis Tn library consisting of 1,952 non-essential genes was screened for mutants that failed to induce IL-10 in myeloid-derived suppressor cells (MDSCs), which identified a critical role for bacterial lactic acid biosynthesis. We generated an S. aureus ddh/ldh1/ldh2 triple Tn mutant that cannot produce d- or l-lactate. Co-culture of MDSCs or macrophages with ddh/ldh1/ldh2 mutant biofilm produced substantially less IL-10 compared with wild-type S. aureus, which was also observed in a mouse model of PJI and led to reduced biofilm burden. Using MDSCs recovered from the mouse PJI model and in vitro leukocyte–biofilm co-cultures, we show that bacterial-derived lactate inhibits histone deacetylase 11, causing unchecked HDAC6 activity and increased histone 3 acetylation at the Il-10 promoter, resulting in enhanced Il-10 transcription in MDSCs and macrophages. Finally, we show that synovial fluid of patients with PJI contains elevated amounts of d-lactate and IL-10 compared with control subjects, and bacterial lactate increases IL-10 production by human monocyte-derived macrophages.Bacteria-derived lactate mediates inhibition of HDAC11 during Staphylococcus aureus biofilm infections, resulting in epigenetic changes that reprogramme the host immune response.
Author Klinkebiel, David
Seto, Edward
Alqarzaee, Abdulelah A.
Yamada, Kelsey J.
Aldrich, Amy L.
Karpf, Adam R.
Bosch, Megan E.
Li, Yixuan
Gries, Casey M.
Kielian, Tammy
Heim, Cortney E.
Thomas, Vinai C.
Chaudhari, Sujata S.
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  givenname: Cortney E.
  orcidid: 0000-0001-5975-9722
  surname: Heim
  fullname: Heim, Cortney E.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center
– sequence: 2
  givenname: Megan E.
  surname: Bosch
  fullname: Bosch, Megan E.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center, Department of Neurology, Washington University School of Medicine
– sequence: 3
  givenname: Kelsey J.
  orcidid: 0000-0003-1071-8836
  surname: Yamada
  fullname: Yamada, Kelsey J.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center
– sequence: 4
  givenname: Amy L.
  surname: Aldrich
  fullname: Aldrich, Amy L.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center, Moffitt Cancer Center
– sequence: 5
  givenname: Sujata S.
  orcidid: 0000-0002-9609-152X
  surname: Chaudhari
  fullname: Chaudhari, Sujata S.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center
– sequence: 6
  givenname: David
  orcidid: 0000-0001-9963-8909
  surname: Klinkebiel
  fullname: Klinkebiel, David
  organization: Department of Biochemistry and Molecular Biology, University of Nebraska Medical Center, Fred and Pamela Buffett Cancer Center, University of Nebraska Medical Center
– sequence: 7
  givenname: Casey M.
  orcidid: 0000-0001-5291-7564
  surname: Gries
  fullname: Gries, Casey M.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center, Division of Biomedical Sciences, University of California Riverside School of Medicine
– sequence: 8
  givenname: Abdulelah A.
  orcidid: 0000-0003-0000-9040
  surname: Alqarzaee
  fullname: Alqarzaee, Abdulelah A.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center
– sequence: 9
  givenname: Yixuan
  surname: Li
  fullname: Li, Yixuan
  organization: Department of Biochemistry and Molecular Medicine, George Washington University School of Medicine and Health Sciences
– sequence: 10
  givenname: Vinai C.
  orcidid: 0000-0002-7886-0727
  surname: Thomas
  fullname: Thomas, Vinai C.
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center
– sequence: 11
  givenname: Edward
  surname: Seto
  fullname: Seto, Edward
  organization: Department of Biochemistry and Molecular Medicine, George Washington University School of Medicine and Health Sciences
– sequence: 12
  givenname: Adam R.
  orcidid: 0000-0002-0866-0666
  surname: Karpf
  fullname: Karpf, Adam R.
  organization: Eppley Institute, University of Nebraska Medical Center, Fred and Pamela Buffett Cancer Center, University of Nebraska Medical Center
– sequence: 13
  givenname: Tammy
  orcidid: 0000-0001-7624-670X
  surname: Kielian
  fullname: Kielian, Tammy
  email: tkielian@unmc.edu
  organization: Department of Pathology and Microbiology, University of Nebraska Medical Center
BackLink https://www.ncbi.nlm.nih.gov/pubmed/32661313$$D View this record in MEDLINE/PubMed
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Snippet Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment....
Staphylococcus aureus is a leading cause of biofilm-associated prosthetic joint infection (PJI), resulting in considerable disability and prolonged treatment....
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Acetylation
Bacteria
Biofilms
Biomarkers
Biomedical and Life Sciences
Biosynthetic Pathways
Cell culture
Cytokines - metabolism
Epigenetics
Histone deacetylase
Histone Deacetylases - metabolism
Host-Pathogen Interactions - immunology
Immune response
Infectious Diseases
Inflammation Mediators - metabolism
Interleukin 10
Joint diseases
Lactic acid
Lactic Acid - metabolism
Life Sciences
Macrophages
Macrophages - immunology
Macrophages - metabolism
Medical Microbiology
Microbiology
Monocytes
Mutants
Myeloid-Derived Suppressor Cells - immunology
Myeloid-Derived Suppressor Cells - metabolism
Parasitology
Penicillin
Staphylococcal Infections - immunology
Staphylococcal Infections - metabolism
Staphylococcal Infections - microbiology
Staphylococcus aureus
Staphylococcus aureus - physiology
Suppressor cells
Synovial fluid
Transcription
Virology
Title Lactate production by Staphylococcus aureus biofilm inhibits HDAC11 to reprogramme the host immune response during persistent infection
URI https://link.springer.com/article/10.1038/s41564-020-0756-3
https://www.ncbi.nlm.nih.gov/pubmed/32661313
https://www.proquest.com/docview/2474987740
https://www.proquest.com/docview/2423801730
Volume 5
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