Phosphodiesterase-4 inhibition alters gene expression and improves isoniazid-mediated clearance of Mycobacterium tuberculosis in rabbit lungs
Tuberculosis (TB) treatment is hampered by the long duration of antibiotic therapy required to achieve cure. This indolent response has been partly attributed to the ability of subpopulations of less metabolically active Mycobacterium tuberculosis (Mtb) to withstand killing by current anti-TB drugs....
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Published in | PLoS pathogens Vol. 7; no. 9; p. e1002262 |
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Main Authors | , , , , , , , , , |
Format | Journal Article |
Language | English |
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United States
Public Library of Science
01.09.2011
Public Library of Science (PLoS) |
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Abstract | Tuberculosis (TB) treatment is hampered by the long duration of antibiotic therapy required to achieve cure. This indolent response has been partly attributed to the ability of subpopulations of less metabolically active Mycobacterium tuberculosis (Mtb) to withstand killing by current anti-TB drugs. We have used immune modulation with a phosphodiesterase-4 (PDE4) inhibitor, CC-3052, that reduces tumor necrosis factor alpha (TNF-α) production by increasing intracellular cAMP in macrophages, to examine the crosstalk between host and pathogen in rabbits with pulmonary TB during treatment with isoniazid (INH). Based on DNA microarray, changes in host gene expression during CC-3052 treatment of Mtb infected rabbits support a link between PDE4 inhibition and specific down-regulation of the innate immune response. The overall pattern of host gene expression in the lungs of infected rabbits treated with CC-3052, compared to untreated rabbits, was similar to that described in vitro in resting Mtb infected macrophages, suggesting suboptimal macrophage activation. These alterations in host immunity were associated with corresponding down-regulation of a number of Mtb genes that have been associated with a metabolic shift towards dormancy. Moreover, treatment with CC-3052 and INH resulted in reduced expression of those genes associated with the bacterial response to INH. Importantly, CC-3052 treatment of infected rabbits was associated with reduced ability of Mtb to withstand INH killing, shown by improved bacillary clearance, from the lungs of co-treated animals compared to rabbits treated with INH alone. The results of our study suggest that changes in Mtb gene expression, in response to changes in the host immune response, can alter the responsiveness of the bacteria to antimicrobial agents. These findings provide a basis for exploring the potential use of adjunctive immune modulation with PDE4 inhibitors to enhance the efficacy of existing anti-TB treatment. |
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AbstractList | Tuberculosis (TB) treatment is hampered by the long duration of antibiotic therapy required to achieve cure. This indolent response has been partly attributed to the ability of subpopulations of less metabolically active Mycobacterium tuberculosis (Mtb) to withstand killing by current anti-TB drugs. We have used immune modulation with a phosphodiesterase-4 (PDE4) inhibitor, CC-3052, that reduces tumor necrosis factor alpha (TNF-α) production by increasing intracellular cAMP in macrophages, to examine the crosstalk between host and pathogen in rabbits with pulmonary TB during treatment with isoniazid (INH). Based on DNA microarray, changes in host gene expression during CC-3052 treatment of Mtb infected rabbits support a link between PDE4 inhibition and specific down-regulation of the innate immune response. The overall pattern of host gene expression in the lungs of infected rabbits treated with CC-3052, compared to untreated rabbits, was similar to that described in vitro in resting Mtb infected macrophages, suggesting suboptimal macrophage activation. These alterations in host immunity were associated with corresponding down-regulation of a number of Mtb genes that have been associated with a metabolic shift towards dormancy. Moreover, treatment with CC-3052 and INH resulted in reduced expression of those genes associated with the bacterial response to INH. Importantly, CC-3052 treatment of infected rabbits was associated with reduced ability of Mtb to withstand INH killing, shown by improved bacillary clearance, from the lungs of co-treated animals compared to rabbits treated with INH alone. The results of our study suggest that changes in Mtb gene expression, in response to changes in the host immune response, can alter the responsiveness of the bacteria to antimicrobial agents. These findings provide a basis for exploring the potential use of adjunctive immune modulation with PDE4 inhibitors to enhance the efficacy of existing anti-TB treatment. Tuberculosis (TB) treatment is hampered by the long duration of antibiotic therapy required to achieve cure. This indolent response has been partly attributed to the ability of subpopulations of less metabolically active Mycobacterium tuberculosis ( Mtb ) to withstand killing by current anti-TB drugs. We have used immune modulation with a phosphodiesterase-4 (PDE4) inhibitor, CC-3052, that reduces tumor necrosis factor alpha (TNF-α) production by increasing intracellular cAMP in macrophages, to examine the crosstalk between host and pathogen in rabbits with pulmonary TB during treatment with isoniazid (INH). Based on DNA microarray, changes in host gene expression during CC-3052 treatment of Mtb infected rabbits support a link between PDE4 inhibition and specific down-regulation of the innate immune response. The overall pattern of host gene expression in the lungs of infected rabbits treated with CC-3052, compared to untreated rabbits, was similar to that described in vitro in resting Mtb infected macrophages, suggesting suboptimal macrophage activation. These alterations in host immunity were associated with corresponding down-regulation of a number of Mtb genes that have been associated with a metabolic shift towards dormancy. Moreover, treatment with CC-3052 and INH resulted in reduced expression of those genes associated with the bacterial response to INH. Importantly, CC-3052 treatment of infected rabbits was associated with reduced ability of Mtb to withstand INH killing, shown by improved bacillary clearance, from the lungs of co-treated animals compared to rabbits treated with INH alone. The results of our study suggest that changes in Mtb gene expression, in response to changes in the host immune response, can alter the responsiveness of the bacteria to antimicrobial agents. These findings provide a basis for exploring the potential use of adjunctive immune modulation with PDE4 inhibitors to enhance the efficacy of existing anti-TB treatment. Tuberculosis (TB) caused by Mycobacterium tuberculosis ( Mtb ) is a leading infectious cause of morbidity and mortality. Although current antibiotic regimens can cure TB, treatment requires at least six months for completion. Recent studies indicate that bacteria in a less metabolically active state are less responsive to antibiotic killing and suggest that this may partly explain the long duration required for TB treatment. In this study, using a rabbit model of pulmonary TB, we show that immune modulation of Mtb infected animals with CC-3052, a phosphodiesterase-4 (PDE4) inhibitor that reduces tumor necrosis factor alpha (TNF-α) production by increasing intracellular cAMP levels, resulted in the down-regulation of host genes involved in the innate immune response. Bacteria from the lungs of CC-3052 treated rabbits displayed differential expression of those genes associated with stress responses. In addition, co-treatment of INH with CC-3052 abolished the INH-induced Mtb gene expression in the infected rabbits. Importantly, bacillary clearance from the lungs of rabbits co-treated with CC-3052 and INH was improved over that in animals treated with INH alone. The results of this study provide a basis for novel use of immune modulation to improve the efficacy of antibiotic therapy and to shorten the duration of TB treatment. Tuberculosis (TB) treatment is hampered by the long duration of antibiotic therapy required to achieve cure. This indolent response has been partly attributed to the ability of subpopulations of less metabolically active Mycobacterium tuberculosis (Mtb) to withstand killing by current anti-TB drugs. We have used immune modulation with a phosphodiesterase-4 (PDE4) inhibitor, CC-3052, that reduces tumor necrosis factor alpha (TNF-α) production by increasing intracellular cAMP in macrophages, to examine the crosstalk between host and pathogen in rabbits with pulmonary TB during treatment with isoniazid (INH). Based on DNA microarray, changes in host gene expression during CC-3052 treatment of Mtb infected rabbits support a link between PDE4 inhibition and specific down-regulation of the innate immune response. The overall pattern of host gene expression in the lungs of infected rabbits treated with CC-3052, compared to untreated rabbits, was similar to that described in vitro in resting Mtb infected macrophages, suggesting suboptimal macrophage activation. These alterations in host immunity were associated with corresponding down-regulation of a number of Mtb genes that have been associated with a metabolic shift towards dormancy. Moreover, treatment with CC-3052 and INH resulted in reduced expression of those genes associated with the bacterial response to INH. Importantly, CC-3052 treatment of infected rabbits was associated with reduced ability of Mtb to withstand INH killing, shown by improved bacillary clearance, from the lungs of co-treated animals compared to rabbits treated with INH alone. The results of our study suggest that changes in Mtb gene expression, in response to changes in the host immune response, can alter the responsiveness of the bacteria to antimicrobial agents. These findings provide a basis for exploring the potential use of adjunctive immune modulation with PDE4 inhibitors to enhance the efficacy of existing anti-TB treatment. |
Audience | Academic |
Author | Peixoto, Blas Muller, George Yang, Guibin Koo, Mi-Sun Dartois, Veronique O'Brien, Paul Subbian, Selvakumar Tsenova, Liana Kaplan, Gilla Fallows, Dorothy |
AuthorAffiliation | 1 Laboratory of Mycobacterial Immunity and Pathogenesis, the Public Health Research Institute (PHRI) at the University of Medicine and Dentistry of New Jersey (UMDNJ), Newark, New Jersey, United States of America 3 Novartis Institute for Tropical Diseases, Singapore Harvard School of Public Health, United States of America 4 Celgene Corporation, Summit, New Jersey, United States of America 2 Biological Sciences Department, New York City College of Technology, Brooklyn, New York, United States of America |
AuthorAffiliation_xml | – name: Harvard School of Public Health, United States of America – name: 4 Celgene Corporation, Summit, New Jersey, United States of America – name: 3 Novartis Institute for Tropical Diseases, Singapore – name: 1 Laboratory of Mycobacterial Immunity and Pathogenesis, the Public Health Research Institute (PHRI) at the University of Medicine and Dentistry of New Jersey (UMDNJ), Newark, New Jersey, United States of America – name: 2 Biological Sciences Department, New York City College of Technology, Brooklyn, New York, United States of America |
Author_xml | – sequence: 1 givenname: Selvakumar surname: Subbian fullname: Subbian, Selvakumar organization: Laboratory of Mycobacterial Immunity and Pathogenesis, the Public Health Research Institute (PHRI) at the University of Medicine and Dentistry of New Jersey (UMDNJ), Newark, New Jersey, United States of America – sequence: 2 givenname: Liana surname: Tsenova fullname: Tsenova, Liana – sequence: 3 givenname: Paul surname: O'Brien fullname: O'Brien, Paul – sequence: 4 givenname: Guibin surname: Yang fullname: Yang, Guibin – sequence: 5 givenname: Mi-Sun surname: Koo fullname: Koo, Mi-Sun – sequence: 6 givenname: Blas surname: Peixoto fullname: Peixoto, Blas – sequence: 7 givenname: Dorothy surname: Fallows fullname: Fallows, Dorothy – sequence: 8 givenname: Veronique surname: Dartois fullname: Dartois, Veronique – sequence: 9 givenname: George surname: Muller fullname: Muller, George – sequence: 10 givenname: Gilla surname: Kaplan fullname: Kaplan, Gilla |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/21949656$$D View this record in MEDLINE/PubMed |
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ContentType | Journal Article |
Copyright | COPYRIGHT 2011 Public Library of Science 2011 Subbian et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Subbian S, Tsenova L, O'Brien P, Yang G, Koo M-S, et al. (2011) Phosphodiesterase-4 Inhibition Alters Gene Expression and Improves Isoniazid - Mediated Clearance of Mycobacterium tuberculosis in Rabbit Lungs. PLoS Pathog 7(9): e1002262. doi:10.1371/journal.ppat.1002262 Subbian et al. 2011 |
Copyright_xml | – notice: COPYRIGHT 2011 Public Library of Science – notice: 2011 Subbian et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Subbian S, Tsenova L, O'Brien P, Yang G, Koo M-S, et al. (2011) Phosphodiesterase-4 Inhibition Alters Gene Expression and Improves Isoniazid - Mediated Clearance of Mycobacterium tuberculosis in Rabbit Lungs. PLoS Pathog 7(9): e1002262. doi:10.1371/journal.ppat.1002262 – notice: Subbian et al. 2011 |
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DocumentTitleAlternate | Adjunctive Immune Modulation Improves TB Therapy |
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Editor | Rubin, Eric J. |
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Notes | Conceived and designed the experiments: SS DF LT GK. Performed the experiments: SS PO LT GY MK VD BP. Analyzed the data: SS GK. Contributed reagents/materials/analysis tools: VD GM. Wrote the paper: SS DF LT GK. |
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Snippet | Tuberculosis (TB) treatment is hampered by the long duration of antibiotic therapy required to achieve cure. This indolent response has been partly attributed... Tuberculosis (TB) treatment is hampered by the long duration of antibiotic therapy required to achieve cure. This indolent response has been partly... |
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SubjectTerms | Animals Antibiotics Antitubercular Agents - therapeutic use Bacteria Bacterial Load Biology Chemistry Cyclic AMP - metabolism Cyclic Nucleotide Phosphodiesterases, Type 4 - metabolism Deoxyribonucleic acid DNA Drug Resistance, Bacterial Experiments Female Gene expression Gene Expression Regulation Genetic aspects Health aspects Immune system Infections Isoniazid - therapeutic use Lung - immunology Lung - microbiology Lung - pathology Lungs Macrophages - immunology Male Medicine Mycobacterium tuberculosis Mycobacterium tuberculosis - drug effects Mycobacterium tuberculosis - immunology Oligonucleotide Array Sequence Analysis Phosphodiesterase 4 Inhibitors - therapeutic use Phosphodiesterases Physiological aspects Rabbits Standard deviation Thalidomide - analogs & derivatives Thalidomide - therapeutic use Tuberculosis Tuberculosis - drug therapy Tuberculosis - genetics Tuberculosis - microbiology Tuberculosis - pathology Tumor Necrosis Factor-alpha - biosynthesis Veterinary Science |
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Title | Phosphodiesterase-4 inhibition alters gene expression and improves isoniazid-mediated clearance of Mycobacterium tuberculosis in rabbit lungs |
URI | https://www.ncbi.nlm.nih.gov/pubmed/21949656 https://www.proquest.com/docview/1289082582 https://pubmed.ncbi.nlm.nih.gov/PMC3174258 https://doaj.org/article/05f5258dcd2f4fbc8ca0de57d17de563 http://dx.doi.org/10.1371/journal.ppat.1002262 |
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