Host Genotype-Specific Therapies Can Optimize the Inflammatory Response to Mycobacterial Infections
Susceptibility to tuberculosis is historically ascribed to an inadequate immune response that fails to control infecting mycobacteria. In zebrafish, we find that susceptibility to Mycobacterium marinum can result from either inadequate or excessive acute inflammation. Modulation of the leukotriene A...
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| Published in | Cell Vol. 148; no. 3; pp. 434 - 446 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
03.02.2012
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Susceptibility to tuberculosis is historically ascribed to an inadequate immune response that fails to control infecting mycobacteria. In zebrafish, we find that susceptibility to Mycobacterium marinum can result from either inadequate or excessive acute inflammation. Modulation of the leukotriene A4 hydrolase (LTA4H) locus, which controls the balance of pro- and anti-inflammatory eicosanoids, reveals two distinct molecular routes to mycobacterial susceptibility converging on dysregulated TNF levels: inadequate inflammation caused by excess lipoxins and hyperinflammation driven by excess leukotriene B4. We identify therapies that specifically target each of these extremes. In humans, we identify a single nucleotide polymorphism in the LTA4H promoter that regulates its transcriptional activity. In tuberculous meningitis, the polymorphism is associated with inflammatory cell recruitment, patient survival and response to adjunctive anti-inflammatory therapy. Together, our findings suggest that host-directed therapies tailored to patient LTA4H genotypes may counter detrimental effects of either extreme of inflammation.
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► Conserved eicosanoids are regulated by LTA4H activity and impact inflammatory state ► Genotype-directed modulation of TNF improves outcomes in a zebrafish tuberculosis model ► Drug therapies tailored to lta4h genotype improve infection outcome in zebrafish ► In humans, LTA4H genotype associates with responsiveness to therapy for TB meningitis
A polymorphism in a locus that controls the balance between pro- and anti-inflammatory mediators is predictive of response to anti-inflammatory therapy in tuberculous meningitis. |
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| AbstractList | Susceptibility to tuberculosis is historically ascribed to an inadequate immune response that fails to control infecting mycobacteria. In zebrafish, we find that susceptibility to Mycobacterium marinum can result from either inadequate or excessive acute inflammation. Modulation of the leukotriene A4 hydrolase (LTA4H) locus, which controls the balance of pro- and anti-inflammatory eicosanoids, reveals two distinct molecular routes to mycobacterial susceptibility converging on dysregulated TNF levels: inadequate inflammation caused by excess lipoxins and hyperinflammation driven by excess leukotriene B4. We identify therapies that specifically target each of these extremes. In humans, we identify a single nucleotide polymorphism in the LTA4H promoter that regulates its transcriptional activity. In tuberculous meningitis, the polymorphism is associated with inflammatory cell recruitment, patient survival and response to adjunctive anti-inflammatory therapy. Together, our findings suggest that host-directed therapies tailored to patient LTA4H genotypes may counter detrimental effects of either extreme of inflammation. Susceptibility to tuberculosis is historically ascribed to an inadequate immune response that fails to control infecting mycobacteria. In zebrafish, we find that susceptibility to Mycobacterium marinum can result from either inadequate or excessive acute inflammation. Modulation of the leukotriene A₄ hydrolase (LTA4H) locus, which controls the balance of pro- and anti-inflammatory eicosanoids, reveals two distinct molecular routes to mycobacterial susceptibility converging on dysregulated TNF levels: inadequate inflammation caused by excess lipoxins and hyperinflammation driven by excess leukotriene B₄. We identify therapies that specifically target each of these extremes. In humans, we identify a single nucleotide polymorphism in the LTA4H promoter that regulates its transcriptional activity. In tuberculous meningitis, the polymorphism is associated with inflammatory cell recruitment, patient survival and response to adjunctive anti-inflammatory therapy. Together, our findings suggest that host-directed therapies tailored to patient LTA4H genotypes may counter detrimental effects of either extreme of inflammation. Susceptibility to tuberculosis is historically ascribed to an inadequate immune response that fails to control infecting mycobacteria. In zebrafish, we find that susceptibility to Mycobacterium marinum can result from either inadequate or excessive acute inflammation. Modulation of the leukotriene A4 hydrolase (LTA4H) locus, which controls the balance of pro- and anti-inflammatory eicosanoids, reveals two distinct molecular routes to mycobacterial susceptibility converging on dysregulated TNF levels: inadequate inflammation caused by excess lipoxins and hyperinflammation driven by excess leukotriene B4. We identify therapies that specifically target each of these extremes. In humans, we identify a single nucleotide polymorphism in the LTA4H promoter that regulates its transcriptional activity. In tuberculous meningitis, the polymorphism is associated with inflammatory cell recruitment, patient survival and response to adjunctive anti-inflammatory therapy. Together, our findings suggest that host-directed therapies tailored to patient LTA4H genotypes may counter detrimental effects of either extreme of inflammation. [Display omitted] ► Conserved eicosanoids are regulated by LTA4H activity and impact inflammatory state ► Genotype-directed modulation of TNF improves outcomes in a zebrafish tuberculosis model ► Drug therapies tailored to lta4h genotype improve infection outcome in zebrafish ► In humans, LTA4H genotype associates with responsiveness to therapy for TB meningitis A polymorphism in a locus that controls the balance between pro- and anti-inflammatory mediators is predictive of response to anti-inflammatory therapy in tuberculous meningitis. Susceptibility to tuberculosis is historically ascribed to an inadequate immune response that fails to control infecting mycobacteria. In zebrafish, we find that susceptibility to Mycobacterium marinum can result from either inadequate or excessive acute inflammation. Modulation of the leukotriene A(4) hydrolase (LTA4H) locus, which controls the balance of pro- and anti-inflammatory eicosanoids, reveals two distinct molecular routes to mycobacterial susceptibility converging on dysregulated TNF levels: inadequate inflammation caused by excess lipoxins and hyperinflammation driven by excess leukotriene B(4). We identify therapies that specifically target each of these extremes. In humans, we identify a single nucleotide polymorphism in the LTA4H promoter that regulates its transcriptional activity. In tuberculous meningitis, the polymorphism is associated with inflammatory cell recruitment, patient survival and response to adjunctive anti-inflammatory therapy. Together, our findings suggest that host-directed therapies tailored to patient LTA4H genotypes may counter detrimental effects of either extreme of inflammation. Susceptibility to tuberculosis is historically ascribed to an inadequate immune response that fails to control infecting mycobacteria. In zebrafish, we find that susceptibility to Mycobacterium marinum can result from either inadequate or excessive acute inflammation. Modulation of the leukotriene A 4 hydrolase ( LTA4H ) locus, which controls the balance of pro- and anti-inflammatory eicosanoids, reveals two distinct molecular routes to mycobacterial susceptibility converging on dysregulated TNF levels: inadequate inflammation caused by excess lipoxins and hyperinflammation driven by excess leukotriene B 4 . We identify therapies that specifically target each of these extremes. In humans, we identify a single nucleotide polymorphism in the LTA4H promoter that regulates its transcriptional activity. In tuberculous meningitis, the polymorphism is associated with inflammatory cell recruitment, patient survival and response to adjunctive anti-inflammatory therapy. Together, our findings suggest that host-directed therapies tailored to patient LTA4H genotypes may counter detrimental effects of either extreme of inflammation. |
| Author | Ko, Dennis C. Vickery, Thad W. McFarland, Ross Ray, John P. Roca, Francisco J. Serhan, Charles N. Thwaites, Guy E. Oh, Sungwhan F. Farrar, Jeremy J. King, Mary-Claire Tobin, David M. Zou, Yuxia Chau, Tran T.H. Dunstan, Sarah J. Vary, Jay C. Ramakrishnan, Lalita Hawn, Thomas R. Bang, Nguyen D. |
| AuthorAffiliation | 5 Hospital for Tropical Diseases, 190 Ben Ham Tu, Quan 5, Ho Chi Minh City, Vietnam 7 Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 190 Ben Ham Tu, Quan 5, Ho Chi Minh City, Vietnam 2 Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710 4 Pham Ngoc Thach Hospital for Tuberculosis and Lung Disease, Ho Chi Minh City, Vietnam 3 Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115 6 Department of Medicine, University of Washington, Seattle, WA 98195 10 Department of Genome Sciences, University of Washington, Seattle, WA 98195 11 Department of Immunology, University of Washington, Seattle, WA 98195 9 Kings College London, Centre for Clinical Infection and Diagnostics Research, St. Thomas’ Hospital, London SE1 9RT, UK 1 Department of Microbiology, University of Washington, Sea |
| AuthorAffiliation_xml | – name: 9 Kings College London, Centre for Clinical Infection and Diagnostics Research, St. Thomas’ Hospital, London SE1 9RT, UK – name: 2 Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710 – name: 5 Hospital for Tropical Diseases, 190 Ben Ham Tu, Quan 5, Ho Chi Minh City, Vietnam – name: 7 Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 190 Ben Ham Tu, Quan 5, Ho Chi Minh City, Vietnam – name: 11 Department of Immunology, University of Washington, Seattle, WA 98195 – name: 1 Department of Microbiology, University of Washington, Seattle, WA 98195 – name: 3 Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women’s Hospital, Harvard Medical School, Boston, Massachusetts 02115 – name: 8 Centre for Tropical Medicine, Nuffield Department of Clinical Medicine, Oxford University, Oxford OX3 7LJ, UK – name: 10 Department of Genome Sciences, University of Washington, Seattle, WA 98195 – name: 6 Department of Medicine, University of Washington, Seattle, WA 98195 – name: 4 Pham Ngoc Thach Hospital for Tuberculosis and Lung Disease, Ho Chi Minh City, Vietnam |
| Author_xml | – sequence: 1 givenname: David M. surname: Tobin fullname: Tobin, David M. organization: Department of Microbiology, University of Washington, Seattle, WA 98195, USA – sequence: 2 givenname: Francisco J. surname: Roca fullname: Roca, Francisco J. organization: Department of Microbiology, University of Washington, Seattle, WA 98195, USA – sequence: 3 givenname: Sungwhan F. surname: Oh fullname: Oh, Sungwhan F. organization: Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 4 givenname: Ross surname: McFarland fullname: McFarland, Ross organization: Department of Microbiology, University of Washington, Seattle, WA 98195, USA – sequence: 5 givenname: Thad W. surname: Vickery fullname: Vickery, Thad W. organization: Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 6 givenname: John P. surname: Ray fullname: Ray, John P. organization: Department of Microbiology, University of Washington, Seattle, WA 98195, USA – sequence: 7 givenname: Dennis C. surname: Ko fullname: Ko, Dennis C. organization: Department of Microbiology, University of Washington, Seattle, WA 98195, USA – sequence: 8 givenname: Yuxia surname: Zou fullname: Zou, Yuxia organization: Department of Molecular Genetics and Microbiology, Duke University Medical Center, Durham, NC 27710, USA – sequence: 9 givenname: Nguyen D. surname: Bang fullname: Bang, Nguyen D. organization: Pham Ngoc Thach Hospital for Tuberculosis and Lung Disease, Ho Chi Minh City, Vietnam – sequence: 10 givenname: Tran T.H. surname: Chau fullname: Chau, Tran T.H. organization: Hospital for Tropical Diseases, 190 Ben Ham Tu, Quan 5, Ho Chi Minh City, Vietnam – sequence: 11 givenname: Jay C. surname: Vary fullname: Vary, Jay C. organization: Department of Medicine, University of Washington, Seattle, WA 98195, USA – sequence: 12 givenname: Thomas R. surname: Hawn fullname: Hawn, Thomas R. organization: Department of Medicine, University of Washington, Seattle, WA 98195, USA – sequence: 13 givenname: Sarah J. surname: Dunstan fullname: Dunstan, Sarah J. organization: Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 190 Ben Ham Tu, Quan 5, Ho Chi Minh City, Vietnam – sequence: 14 givenname: Jeremy J. surname: Farrar fullname: Farrar, Jeremy J. organization: Oxford University Clinical Research Unit, Hospital for Tropical Diseases, 190 Ben Ham Tu, Quan 5, Ho Chi Minh City, Vietnam – sequence: 15 givenname: Guy E. surname: Thwaites fullname: Thwaites, Guy E. organization: Kings College London, Centre for Clinical Infection and Diagnostics Research, St. Thomas' Hospital, London SE1 9RT, UK – sequence: 16 givenname: Mary-Claire surname: King fullname: King, Mary-Claire organization: Department of Medicine, University of Washington, Seattle, WA 98195, USA – sequence: 17 givenname: Charles N. surname: Serhan fullname: Serhan, Charles N. organization: Center for Experimental Therapeutics and Reperfusion Injury, Department of Anesthesiology, Perioperative and Pain Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA 02115, USA – sequence: 18 givenname: Lalita surname: Ramakrishnan fullname: Ramakrishnan, Lalita email: lalitar@uw.edu organization: Department of Microbiology, University of Washington, Seattle, WA 98195, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/22304914$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Animals Danio rerio Disease Models, Animal eicosanoids genotype Humans immune response inflammation Inflammation - immunology Leukotriene A4 - genetics Leukotriene A4 - immunology Leukotriene B4 - genetics Leukotriene B4 - immunology Lipoxins - immunology loci meningitis Mitochondria - metabolism Mycobacterium Mycobacterium Infections - drug therapy Mycobacterium Infections - genetics Mycobacterium Infections - immunology Mycobacterium marinum patients polymorphism Polymorphism, Genetic Polymorphism, Single Nucleotide Promoter Regions, Genetic Signal Transduction single nucleotide polymorphism therapeutics transcription (genetics) Transcription, Genetic tuberculosis Tuberculosis, Meningeal - drug therapy Tuberculosis, Meningeal - genetics Tuberculosis, Meningeal - immunology Tumor Necrosis Factor-alpha - metabolism tumor necrosis factors Zebrafish - embryology Zebrafish - immunology |
| Title | Host Genotype-Specific Therapies Can Optimize the Inflammatory Response to Mycobacterial Infections |
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