Growth of Mycobacterium tuberculosis in vivo segregates with host macrophage metabolism and ontogeny

To understand how infection by (Mtb) is modulated by host cell phenotype, we characterized those host phagocytes that controlled or supported bacterial growth during early infection, focusing on the ontologically distinct alveolar macrophage (AM) and interstitial macrophage (IM) lineages. Using fluo...

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Published in:	The Journal of experimental medicine Vol. 215; no. 4; p. 1135
Main Authors:	Huang, Lu, Nazarova, Evgeniya V, Tan, Shumin, Liu, Yancheng, Russell, David G
Format:	Journal Article
Language:	English
Published:	United States 02.04.2018
Subjects:	Animals Bystander Effect Cell Cycle Cell Proliferation Cellular Reprogramming Fatty Acids - metabolism Genes, Reporter Glycolysis Host-Pathogen Interactions Macrophages, Alveolar - metabolism Macrophages, Alveolar - microbiology Macrophages, Alveolar - pathology Metabolic Networks and Pathways Mice, Inbred C57BL Models, Biological Monocytes - pathology Mycobacterium tuberculosis - growth & development Oxidation-Reduction Phagocytes - metabolism Transcription, Genetic Tuberculosis - microbiology Tuberculosis - pathology
ISSN:	1540-9538, 1540-9538
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Abstract	To understand how infection by (Mtb) is modulated by host cell phenotype, we characterized those host phagocytes that controlled or supported bacterial growth during early infection, focusing on the ontologically distinct alveolar macrophage (AM) and interstitial macrophage (IM) lineages. Using fluorescent Mtb reporter strains, we found that bacilli in AM exhibited lower stress and higher bacterial replication than those in IM. Interestingly, depletion of AM reduced bacterial burden, whereas depletion of IM increased bacterial burden. Transcriptomic analysis revealed that IMs were glycolytically active, whereas AMs were committed to fatty acid oxidation. Intoxication of infected mice with the glycolytic inhibitor, 2-deoxyglucose, decreased the number of IMs yet increased the bacterial burden in the lung. Furthermore, in in vitro macrophage infections, 2-deoxyglucose treatment increased bacterial growth, whereas the fatty acid oxidation inhibitor etomoxir constrained bacterial growth. We hypothesize that different macrophage lineages respond divergently to Mtb infection, with IMs exhibiting nutritional restriction and controlling bacterial growth and AMs representing a more nutritionally permissive environment.
AbstractList	To understand how infection by (Mtb) is modulated by host cell phenotype, we characterized those host phagocytes that controlled or supported bacterial growth during early infection, focusing on the ontologically distinct alveolar macrophage (AM) and interstitial macrophage (IM) lineages. Using fluorescent Mtb reporter strains, we found that bacilli in AM exhibited lower stress and higher bacterial replication than those in IM. Interestingly, depletion of AM reduced bacterial burden, whereas depletion of IM increased bacterial burden. Transcriptomic analysis revealed that IMs were glycolytically active, whereas AMs were committed to fatty acid oxidation. Intoxication of infected mice with the glycolytic inhibitor, 2-deoxyglucose, decreased the number of IMs yet increased the bacterial burden in the lung. Furthermore, in in vitro macrophage infections, 2-deoxyglucose treatment increased bacterial growth, whereas the fatty acid oxidation inhibitor etomoxir constrained bacterial growth. We hypothesize that different macrophage lineages respond divergently to Mtb infection, with IMs exhibiting nutritional restriction and controlling bacterial growth and AMs representing a more nutritionally permissive environment. To understand how infection by Mycobacterium tuberculosis (Mtb) is modulated by host cell phenotype, we characterized those host phagocytes that controlled or supported bacterial growth during early infection, focusing on the ontologically distinct alveolar macrophage (AM) and interstitial macrophage (IM) lineages. Using fluorescent Mtb reporter strains, we found that bacilli in AM exhibited lower stress and higher bacterial replication than those in IM. Interestingly, depletion of AM reduced bacterial burden, whereas depletion of IM increased bacterial burden. Transcriptomic analysis revealed that IMs were glycolytically active, whereas AMs were committed to fatty acid oxidation. Intoxication of infected mice with the glycolytic inhibitor, 2-deoxyglucose, decreased the number of IMs yet increased the bacterial burden in the lung. Furthermore, in in vitro macrophage infections, 2-deoxyglucose treatment increased bacterial growth, whereas the fatty acid oxidation inhibitor etomoxir constrained bacterial growth. We hypothesize that different macrophage lineages respond divergently to Mtb infection, with IMs exhibiting nutritional restriction and controlling bacterial growth and AMs representing a more nutritionally permissive environment.To understand how infection by Mycobacterium tuberculosis (Mtb) is modulated by host cell phenotype, we characterized those host phagocytes that controlled or supported bacterial growth during early infection, focusing on the ontologically distinct alveolar macrophage (AM) and interstitial macrophage (IM) lineages. Using fluorescent Mtb reporter strains, we found that bacilli in AM exhibited lower stress and higher bacterial replication than those in IM. Interestingly, depletion of AM reduced bacterial burden, whereas depletion of IM increased bacterial burden. Transcriptomic analysis revealed that IMs were glycolytically active, whereas AMs were committed to fatty acid oxidation. Intoxication of infected mice with the glycolytic inhibitor, 2-deoxyglucose, decreased the number of IMs yet increased the bacterial burden in the lung. Furthermore, in in vitro macrophage infections, 2-deoxyglucose treatment increased bacterial growth, whereas the fatty acid oxidation inhibitor etomoxir constrained bacterial growth. We hypothesize that different macrophage lineages respond divergently to Mtb infection, with IMs exhibiting nutritional restriction and controlling bacterial growth and AMs representing a more nutritionally permissive environment.
Author	Huang, Lu Tan, Shumin Nazarova, Evgeniya V Liu, Yancheng Russell, David G
Author_xml	– sequence: 1 givenname: Lu orcidid: 0000-0002-7820-2177 surname: Huang fullname: Huang, Lu organization: Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY – sequence: 2 givenname: Evgeniya V orcidid: 0000-0001-5745-3172 surname: Nazarova fullname: Nazarova, Evgeniya V organization: Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY – sequence: 3 givenname: Shumin surname: Tan fullname: Tan, Shumin organization: Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, MA – sequence: 4 givenname: Yancheng surname: Liu fullname: Liu, Yancheng organization: Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY – sequence: 5 givenname: David G orcidid: 0000-0002-9748-750X surname: Russell fullname: Russell, David G email: dgr8@cornell.edu organization: Department of Microbiology and Immunology, College of Veterinary Medicine, Cornell University, Ithaca, NY dgr8@cornell.edu
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/29500179$$D View this record in MEDLINE/PubMed
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Copyright	2018 Huang et al.
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PublicationTitle	The Journal of experimental medicine
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Snippet	To understand how infection by (Mtb) is modulated by host cell phenotype, we characterized those host phagocytes that controlled or supported bacterial growth... To understand how infection by Mycobacterium tuberculosis (Mtb) is modulated by host cell phenotype, we characterized those host phagocytes that controlled or...
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SubjectTerms	Animals Bystander Effect Cell Cycle Cell Proliferation Cellular Reprogramming Fatty Acids - metabolism Genes, Reporter Glycolysis Host-Pathogen Interactions Macrophages, Alveolar - metabolism Macrophages, Alveolar - microbiology Macrophages, Alveolar - pathology Metabolic Networks and Pathways Mice, Inbred C57BL Models, Biological Monocytes - pathology Mycobacterium tuberculosis - growth & development Oxidation-Reduction Phagocytes - metabolism Transcription, Genetic Tuberculosis - microbiology Tuberculosis - pathology
Title	Growth of Mycobacterium tuberculosis in vivo segregates with host macrophage metabolism and ontogeny
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