Chemoproteomic identification of a DPP4 homolog in Bacteroides thetaiotaomicron

Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using bioinformatics and chemoproteomics, we identify serine hydrolases in the gut commensal Bacteroides thetaiotaomicron that are specific to the Bacteroide...

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Published inNature chemical biology Vol. 19; no. 12; pp. 1469 - 1479
Main Authors Keller, Laura J., Nguyen, Taylor H., Liu, Lawrence J., Hurysz, Brianna M., Lakemeyer, Markus, Guerra, Matteo, Gelsinger, Danielle J., Chanin, Rachael, Ngo, Nhi, Lum, Kenneth M., Faucher, Franco, Ipock, Phillip, Niphakis, Micah J., Bhatt, Ami S., O’Donoghue, Anthony J., Huang, Kerwyn Casey, Bogyo, Matthew
Format Journal Article
LanguageEnglish
Published New York Nature Publishing Group US 01.12.2023
Nature Publishing Group
Subjects
631/114/129
631/326/41
631/92/475
631/92/607/468
Bacteria
Bacteroides thetaiotaomicron
Biochemical Engineering
Biochemistry
Bioinformatics
Biology
Bioorganic Chemistry
Cell Biology
Chemistry
Chemistry and Materials Science
Chemistry/Food Science
Diabetes mellitus (non-insulin dependent)
Diabetes Mellitus, Type 2
Dipeptidyl Peptidase 4 - genetics
Drugs
Enzymes
FDA approval
Homology
Humans
Integrity
Medicine
Metabolism
Metabolites
Microbiota
Peptidases
Peptides
Proteins
Proteolysis
Scaffolding
Serine
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Abstract Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using bioinformatics and chemoproteomics, we identify serine hydrolases in the gut commensal Bacteroides thetaiotaomicron that are specific to the Bacteroidetes phylum. Two are predicted homologs of the human dipeptidyl peptidase 4 (hDPP4), a key enzyme that regulates insulin signaling. Our functional studies reveal that BT4193 is a true homolog of hDPP4 that can be inhibited by FDA-approved type 2 diabetes medications targeting hDPP4, while the other is a misannotated proline-specific triaminopeptidase. We demonstrate that BT4193 is important for envelope integrity and that loss of BT4193 reduces B. thetaiotaomicron fitness during in vitro growth within a diverse community. However, neither function is dependent on BT4193 proteolytic activity, suggesting a scaffolding or signaling function for this bacterial protease. Bioinformatic and chemoproteomic approaches resulted in the identification of a homolog of human dipeptidyl peptidase 4 in the gut bacterium Bacteroides thetaiotaomicron that regulates envelope integrity and community fitness.
AbstractList Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using bioinformatics and chemoproteomics, we identify serine hydrolases in the gut commensal Bacteroides thetaiotaomicron that are specific to the Bacteroidetes phylum. Two are predicted homologs of the human dipeptidyl peptidase 4 (hDPP4), a key enzyme that regulates insulin signaling. Our functional studies reveal that BT4193 is a true homolog of hDPP4 that can be inhibited by FDA-approved type 2 diabetes medications targeting hDPP4, while the other is a misannotated proline-specific triaminopeptidase. We demonstrate that BT4193 is important for envelope integrity and that loss of BT4193 reduces B. thetaiotaomicron fitness during in vitro growth within a diverse community. However, neither function is dependent on BT4193 proteolytic activity, suggesting a scaffolding or signaling function for this bacterial protease.Bioinformatic and chemoproteomic approaches resulted in the identification of a homolog of human dipeptidyl peptidase 4 in the gut bacterium Bacteroides thetaiotaomicron that regulates envelope integrity and community fitness.
Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using bioinformatics and chemoproteomics, we identify serine hydrolases in the gut commensal Bacteroides thetaiotaomicron that are specific to the Bacteroidetes phylum. Two are predicted homologs of the human dipeptidyl peptidase 4 (hDPP4), a key enzyme that regulates insulin signaling. Our functional studies reveal that BT4193 is a true homolog of hDPP4 that can be inhibited by FDA-approved type 2 diabetes medications targeting hDPP4, while the other is a misannotated proline-specific triaminopeptidase. We demonstrate that BT4193 is important for envelope integrity and that loss of BT4193 reduces B. thetaiotaomicron fitness during in vitro growth within a diverse community. However, neither function is dependent on BT4193 proteolytic activity, suggesting a scaffolding or signaling function for this bacterial protease.
Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using bioinformatics and chemoproteomics, we identify serine hydrolases in the gut commensal Bacteroides thetaiotaomicron that are specific to the Bacteroidetes phylum. Two are predicted homologs of the human dipeptidyl peptidase 4 (hDPP4), a key enzyme that regulates insulin signaling. Our functional studies reveal that BT4193 is a true homolog of hDPP4 that can be inhibited by FDA-approved type 2 diabetes medications targeting hDPP4, while the other is a misannotated proline-specific triaminopeptidase. We demonstrate that BT4193 is important for envelope integrity and that loss of BT4193 reduces B. thetaiotaomicron fitness during in vitro growth within a diverse community. However, neither function is dependent on BT4193 proteolytic activity, suggesting a scaffolding or signaling function for this bacterial protease.Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using bioinformatics and chemoproteomics, we identify serine hydrolases in the gut commensal Bacteroides thetaiotaomicron that are specific to the Bacteroidetes phylum. Two are predicted homologs of the human dipeptidyl peptidase 4 (hDPP4), a key enzyme that regulates insulin signaling. Our functional studies reveal that BT4193 is a true homolog of hDPP4 that can be inhibited by FDA-approved type 2 diabetes medications targeting hDPP4, while the other is a misannotated proline-specific triaminopeptidase. We demonstrate that BT4193 is important for envelope integrity and that loss of BT4193 reduces B. thetaiotaomicron fitness during in vitro growth within a diverse community. However, neither function is dependent on BT4193 proteolytic activity, suggesting a scaffolding or signaling function for this bacterial protease.
Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using bioinformatics and chemoproteomics, we identify serine hydrolases in the gut commensal Bacteroides thetaiotaomicron that are specific to the Bacteroidetes phylum. Two are predicted homologs of the human dipeptidyl peptidase 4 (hDPP4), a key enzyme that regulates insulin signaling. Our functional studies reveal that BT4193 is a true homolog of hDPP4 that can be inhibited by FDA-approved type 2 diabetes medications targeting hDPP4, while the other is a misannotated proline-specific triaminopeptidase. We demonstrate that BT4193 is important for envelope integrity and that loss of BT4193 reduces B. thetaiotaomicron fitness during in vitro growth within a diverse community. However, neither function is dependent on BT4193 proteolytic activity, suggesting a scaffolding or signaling function for this bacterial protease. Bioinformatic and chemoproteomic approaches resulted in the identification of a homolog of human dipeptidyl peptidase 4 in the gut bacterium Bacteroides thetaiotaomicron that regulates envelope integrity and community fitness.
Author Liu, Lawrence J.
O’Donoghue, Anthony J.
Hurysz, Brianna M.
Ngo, Nhi
Gelsinger, Danielle J.
Chanin, Rachael
Nguyen, Taylor H.
Bogyo, Matthew
Huang, Kerwyn Casey
Niphakis, Micah J.
Bhatt, Ami S.
Lum, Kenneth M.
Ipock, Phillip
Guerra, Matteo
Faucher, Franco
Keller, Laura J.
Lakemeyer, Markus
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2023. The Author(s), under exclusive licence to Springer Nature America, Inc.
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PublicationDate 2023-12-01
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PublicationDate_xml – month: 12
  year: 2023
  text: 2023-12-01
  day: 01
PublicationDecade 2020
PublicationPlace New York
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PublicationTitle Nature chemical biology
PublicationTitleAbbrev Nat Chem Biol
PublicationTitleAlternate Nat Chem Biol
PublicationYear 2023
Publisher Nature Publishing Group US
Nature Publishing Group
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Snippet Serine hydrolases have important roles in signaling and human metabolism, yet little is known about their functions in gut commensal bacteria. Using...
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pubmed
crossref
springer
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SubjectTerms 631/114/129
631/326/41
631/92/475
631/92/607/468
Bacteria
Bacteroides thetaiotaomicron
Biochemical Engineering
Biochemistry
Bioinformatics
Biology
Bioorganic Chemistry
Cell Biology
Chemistry
Chemistry and Materials Science
Chemistry/Food Science
Diabetes mellitus (non-insulin dependent)
Diabetes Mellitus, Type 2
Dipeptidyl Peptidase 4 - genetics
Drugs
Enzymes
FDA approval
Homology
Humans
Integrity
Medicine
Metabolism
Metabolites
Microbiota
Peptidases
Peptides
Proteins
Proteolysis
Scaffolding
Serine
Title Chemoproteomic identification of a DPP4 homolog in Bacteroides thetaiotaomicron
URI https://link.springer.com/article/10.1038/s41589-023-01357-8
https://www.ncbi.nlm.nih.gov/pubmed/37349583
https://www.proquest.com/docview/2892810303
https://www.proquest.com/docview/2829429229
Volume 19
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