Cyclopropane Modification of Trehalose Dimycolate Drives Granuloma Angiogenesis and Mycobacterial Growth through Vegf Signaling
Mycobacterial infection leads to the formation of characteristic immune aggregates called granulomas, a process accompanied by dramatic remodeling of the host vasculature. As granuloma angiogenesis favors the infecting mycobacteria, it may be actively promoted by bacterial determinants during infect...
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Published in | Cell host & microbe Vol. 24; no. 4; pp. 514 - 525.e6 |
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Abstract | Mycobacterial infection leads to the formation of characteristic immune aggregates called granulomas, a process accompanied by dramatic remodeling of the host vasculature. As granuloma angiogenesis favors the infecting mycobacteria, it may be actively promoted by bacterial determinants during infection. Using Mycobacterium marinum-infected zebrafish as a model, we identify the enzyme proximal cyclopropane synthase of alpha-mycolates (PcaA) as an important bacterial determinant of granuloma-associated angiogenesis. cis-Cyclopropanation of mycobacterial mycolic acids by pcaA drives the activation of host Vegf signaling within granuloma macrophages. Cyclopropanation of the mycobacterial cell wall glycolipid trehalose dimycolate is both required and sufficient to induce robust host angiogenesis. Inducible genetic inhibition of angiogenesis and Vegf signaling during granuloma formation results in bacterial growth deficits. Together, these data reveal a mechanism by which PcaA-mediated cis-cyclopropanation of mycolic acids promotes bacterial growth and dissemination in vivo by eliciting granuloma vascularization and suggest potential approaches for host-directed therapies.
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•Mycobacterial granuloma angiogenesis requires the cell wall glycolipid TDM•The mycobacterial enzyme PcaA promotes angiogenesis via cis-cyclopropanation of TDM•Cyclopropanated TDM induces granuloma vascularization through activating Vegfa signaling•pcaA mutation or Vegfa pathway blockade reduces bacterial growth in vivo
Granuloma formation during tuberculosis is accompanied by remodeling of host vasculature. Walton et al. identify the mycobacterial enzyme PcaA, which catalyzes proximal cis-cyclopropanation of trehalose dimycolate, as an important determinant of granuloma-associated angiogenesis. This form of trehalose dimycolate induces Vegfa-mediated angiogenesis at the granuloma, promoting bacterial growth. |
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AbstractList | Mycobacterial infection leads to the formation of characteristic immune aggregates called granulomas, a process accompanied by dramatic remodeling of the host vasculature. As granuloma angiogenesis favors the infecting mycobacteria, it may be actively promoted by bacterial determinants during infection. Using Mycobacterium marinum-infected zebrafish as a model, we identify the enzyme proximal cyclopropane synthase of alpha-mycolates (PcaA) as an important bacterial determinant of granuloma-associated angiogenesis. cis-Cyclopropanation of mycobacterial mycolic acids by pcaA drives the activation of host Vegf signaling within granuloma macrophages. Cyclopropanation of the mycobacterial cell wall glycolipid trehalose dimycolate is both required and sufficient to induce robust host angiogenesis. Inducible genetic inhibition of angiogenesis and Vegf signaling during granuloma formation results in bacterial growth deficits. Together, these data reveal a mechanism by which PcaA-mediated cis-cyclopropanation of mycolic acids promotes bacterial growth and dissemination in vivo by eliciting granuloma vascularization and suggest potential approaches for host-directed therapies. Mycobacterial infection leads to the formation of characteristic immune aggregates called granulomas, a process accompanied by dramatic remodeling of the host vasculature. As granuloma angiogenesis favors the infecting mycobacteria, it may be actively promoted by bacterial determinants during infection. Using Mycobacterium marinum -infected zebrafish as a model, we identify the enzyme Proximal Cyclopropane Synthase of alpha-Mycolates (PcaA) as an important bacterial determinant of granuloma-associated angiogenesis. Cis-cyclopropanation of mycobacterial mycolic acids by pcaA drives the activation of host Vegf signaling within granuloma macrophages. Cyclopropanation of the mycobacterial cell wall glycolipid trehalose dimycolate (TDM) is both required and sufficient to induce robust host angiogenesis. Inducible genetic inhibition of angiogenesis and Vegf signaling during granuloma formation results in bacterial growth deficits. Together, these data reveal a mechanism by which PcaA-mediated cis-cyclopropanation of mycolic acids promotes bacterial growth and dissemination in vivo by eliciting granuloma vascularization and suggest potential approaches for host-directed therapies. Granuloma formation during tuberculosis is accompanied by remodeling of host vasculature. Walton et al. identify the mycobacterial enzyme PcaA, which catalyzes proximal cis-cyclopropanation of trehalose dimycolate, as an important determinant of granuloma-associated angiogenesis. This form of trehalose dimycolate induces Vegfa-mediated angiogenesis at the granuloma, promoting bacterial growth. Mycobacterial infection leads to the formation of characteristic immune aggregates called granulomas, a process accompanied by dramatic remodeling of the host vasculature. As granuloma angiogenesis favors the infecting mycobacteria, it may be actively promoted by bacterial determinants during infection. Using Mycobacterium marinum-infected zebrafish as a model, we identify the enzyme proximal cyclopropane synthase of alpha-mycolates (PcaA) as an important bacterial determinant of granuloma-associated angiogenesis. cis-Cyclopropanation of mycobacterial mycolic acids by pcaA drives the activation of host Vegf signaling within granuloma macrophages. Cyclopropanation of the mycobacterial cell wall glycolipid trehalose dimycolate is both required and sufficient to induce robust host angiogenesis. Inducible genetic inhibition of angiogenesis and Vegf signaling during granuloma formation results in bacterial growth deficits. Together, these data reveal a mechanism by which PcaA-mediated cis-cyclopropanation of mycolic acids promotes bacterial growth and dissemination in vivo by eliciting granuloma vascularization and suggest potential approaches for host-directed therapies. Mycobacterial infection leads to the formation of characteristic immune aggregates called granulomas, a process accompanied by dramatic remodeling of the host vasculature. As granuloma angiogenesis favors the infecting mycobacteria, it may be actively promoted by bacterial determinants during infection. Using Mycobacterium marinum-infected zebrafish as a model, we identify the enzyme proximal cyclopropane synthase of alpha-mycolates (PcaA) as an important bacterial determinant of granuloma-associated angiogenesis. cis-Cyclopropanation of mycobacterial mycolic acids by pcaA drives the activation of host Vegf signaling within granuloma macrophages. Cyclopropanation of the mycobacterial cell wall glycolipid trehalose dimycolate is both required and sufficient to induce robust host angiogenesis. Inducible genetic inhibition of angiogenesis and Vegf signaling during granuloma formation results in bacterial growth deficits. Together, these data reveal a mechanism by which PcaA-mediated cis-cyclopropanation of mycolic acids promotes bacterial growth and dissemination in vivo by eliciting granuloma vascularization and suggest potential approaches for host-directed therapies. [Display omitted] •Mycobacterial granuloma angiogenesis requires the cell wall glycolipid TDM•The mycobacterial enzyme PcaA promotes angiogenesis via cis-cyclopropanation of TDM•Cyclopropanated TDM induces granuloma vascularization through activating Vegfa signaling•pcaA mutation or Vegfa pathway blockade reduces bacterial growth in vivo Granuloma formation during tuberculosis is accompanied by remodeling of host vasculature. Walton et al. identify the mycobacterial enzyme PcaA, which catalyzes proximal cis-cyclopropanation of trehalose dimycolate, as an important determinant of granuloma-associated angiogenesis. This form of trehalose dimycolate induces Vegfa-mediated angiogenesis at the granuloma, promoting bacterial growth. |
Author | Brewer, W. Jared Cronan, Mark R. Marass, Michele Tobin, David M. Stainier, Didier Y.R. Foglia, Matthew D. Walton, Eric M. Rossi, Andrea Cambier, C.J. Poss, Kenneth D. Bertozzi, Carolyn R. |
AuthorAffiliation | 5 Regeneration Next, Duke University, Durham, NC 27710, USA 1 Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA 3 Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Bad Nauheim, Germany 4 Department of Cell Biology, Duke University School of Medicine, Durham, NC 27710 USA 6 Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305 8 Lead contact 2 Department of Chemistry, Stanford University, Stanford, CA 94305, USA 7 Department of Immunology, Duke University School of Medicine, Durham, NC 27710, USA |
AuthorAffiliation_xml | – name: 1 Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – name: 2 Department of Chemistry, Stanford University, Stanford, CA 94305, USA – name: 4 Department of Cell Biology, Duke University School of Medicine, Durham, NC 27710 USA – name: 3 Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Bad Nauheim, Germany – name: 5 Regeneration Next, Duke University, Durham, NC 27710, USA – name: 8 Lead contact – name: 6 Howard Hughes Medical Institute, Stanford University, Stanford, CA 94305 – name: 7 Department of Immunology, Duke University School of Medicine, Durham, NC 27710, USA |
Author_xml | – sequence: 1 givenname: Eric M. surname: Walton fullname: Walton, Eric M. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 2 givenname: Mark R. surname: Cronan fullname: Cronan, Mark R. organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 3 givenname: C.J. surname: Cambier fullname: Cambier, C.J. organization: Department of Chemistry, Stanford University, Stanford, CA 94305, USA – sequence: 4 givenname: Andrea surname: Rossi fullname: Rossi, Andrea organization: Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Bad Nauheim, Germany – sequence: 5 givenname: Michele surname: Marass fullname: Marass, Michele organization: Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Bad Nauheim, Germany – sequence: 6 givenname: Matthew D. surname: Foglia fullname: Foglia, Matthew D. organization: Department of Cell Biology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 7 givenname: W. Jared surname: Brewer fullname: Brewer, W. Jared organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 8 givenname: Kenneth D. surname: Poss fullname: Poss, Kenneth D. organization: Department of Cell Biology, Duke University School of Medicine, Durham, NC 27710, USA – sequence: 9 givenname: Didier Y.R. surname: Stainier fullname: Stainier, Didier Y.R. organization: Department of Developmental Genetics, Max Planck Institute for Heart and Lung Research, Bad Nauheim, Germany – sequence: 10 givenname: Carolyn R. surname: Bertozzi fullname: Bertozzi, Carolyn R. organization: Department of Chemistry, Stanford University, Stanford, CA 94305, USA – sequence: 11 givenname: David M. orcidid: 0000-0003-3465-5518 surname: Tobin fullname: Tobin, David M. email: david.tobin@duke.edu organization: Department of Molecular Genetics and Microbiology, Duke University School of Medicine, Durham, NC 27710, USA |
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Keywords | angiogenesis PcaA tuberculosis granuloma vegf macrophage host-directed therapy zebrafish trehalose dimycolate |
Language | English |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS Conceptualization, E.M.W. and D.M.T.; Methodology, E.M.W., M.R.C., C.J.C., A.R., M.M., M.D.F., K.D.P., D.Y.R.S., C.R.B., and D.M.T.; Investigation, E.M.W., M.R.C., C.J.C., and W.J.B.; Writing – Original Draft, E.M.W. and D.M.T.; Writing – Review & Editing, E.M.W., M.R.C., C.J.C., A.R., M.M., M.D.F., W.J.B., K.D.P., D.Y.R.S., C.R.B., and D.M.T.; Funding Acquisition, M.R.C., C.J.C., K.D.P. D.Y.R.S., C.R.B., D.M.T.; Resources, E.M.W., A.R., M.M., M.D.F., K.D.P., D.Y.R.S. Supervision, K.D.P., D.Y.R.S., C.R.B., and D.M.T. |
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SubjectTerms | angiogenesis Angiogenesis Inhibitors - pharmacology Animals Bacterial Proteins - genetics Bacterial Proteins - metabolism Cord Factors - metabolism Disease Models, Animal granuloma host-directed therapy Humans Indazoles macrophage Macrophages - immunology Macrophages - microbiology Methyltransferases - genetics Methyltransferases - metabolism Mycobacterium Infections, Nontuberculous - immunology Mycobacterium Infections, Nontuberculous - microbiology Mycobacterium marinum - enzymology Mycobacterium marinum - genetics Mycobacterium marinum - pathogenicity Mycolic Acids - metabolism Neovascularization, Pathologic - immunology Neovascularization, Pathologic - microbiology Neovascularization, Pathologic - pathology PcaA Pyrimidines - pharmacology Receptors, Vascular Endothelial Growth Factor - antagonists & inhibitors Receptors, Vascular Endothelial Growth Factor - drug effects Receptors, Vascular Endothelial Growth Factor - metabolism Signal Transduction Sulfonamides - pharmacology trehalose dimycolate Tuberculoma - immunology Tuberculoma - microbiology Tuberculoma - pathology tuberculosis vegf Zebrafish |
Title | Cyclopropane Modification of Trehalose Dimycolate Drives Granuloma Angiogenesis and Mycobacterial Growth through Vegf Signaling |
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