Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosis

The BCG vaccine has been used against tuberculosis (TB) for over a hundred years; however, it does not protect adults from pulmonary TB. To develop alternative vaccines against TB, we generated Mycobacterium tuberculosis H37Rv (Mtb)-derived vaccine strains by rationally deleting key virulent genes,...

Full description

Saved in:
Bibliographic Details
Main Authors: Raja Veerapandian, Barbara Yang, Areanna Carmona, Melina J. Sedano, Victoria Reid, Rodrigo Jimenez, Jessica Chacon, Chinnaswamy Jagannath, Enrique I. Ramos, Shrikanth S. Gadad, Subramanian Dhandayuthapani
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-07-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2025.1583439/full
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849428507842576384
author Raja Veerapandian
Barbara Yang
Areanna Carmona
Melina J. Sedano
Victoria Reid
Victoria Reid
Rodrigo Jimenez
Rodrigo Jimenez
Jessica Chacon
Chinnaswamy Jagannath
Enrique I. Ramos
Enrique I. Ramos
Shrikanth S. Gadad
Shrikanth S. Gadad
Subramanian Dhandayuthapani
Subramanian Dhandayuthapani
author_facet Raja Veerapandian
Barbara Yang
Areanna Carmona
Melina J. Sedano
Victoria Reid
Victoria Reid
Rodrigo Jimenez
Rodrigo Jimenez
Jessica Chacon
Chinnaswamy Jagannath
Enrique I. Ramos
Enrique I. Ramos
Shrikanth S. Gadad
Shrikanth S. Gadad
Subramanian Dhandayuthapani
Subramanian Dhandayuthapani
author_sort Raja Veerapandian
collection DOAJ
description The BCG vaccine has been used against tuberculosis (TB) for over a hundred years; however, it does not protect adults from pulmonary TB. To develop alternative vaccines against TB, we generated Mycobacterium tuberculosis H37Rv (Mtb)-derived vaccine strains by rationally deleting key virulent genes, resulting in single (SKO; ΔfbpA), double (DKO; ΔfbpA-ΔsapM), triple (TKO-D; ΔfbpA-ΔsapM-ΔdosR and TKO-Z; ΔfbpA-ΔsapM-Δzmp1), and quadruple (QKO; ΔfbpA-ΔsapM-Δzmp1-dosR) strains. To understand how macrophages, the host cells that defend against infection and process antigens for presentation to immune cells, respond to these vaccine strains, we performed transcriptomic analyses of mouse bone marrow-derived macrophages (BMDMs) infected with these strains. The transcriptomic data were compared with similar data obtained from macrophages infected with Mtb H37Rv and BCG. Our analyses revealed that genes associated with various immune and cell signaling pathways, such as NF-kappa B signaling, TNF signaling, cytokine-cytokine receptor interaction, chemokine signaling, hematopoietic cell lineage, Toll-like receptor signaling, IL-17 signaling, Th1 and Th2 cell differentiation, Th17 cell differentiation, and T cell receptor signaling were differentially expressed in BMDMs infected with our vaccine strains. Enhanced expression of cytokines and chemokines, including proinflammatory cytokines such as TNF-α, IL-6, GM-CSF, and IL-1, which are essential for the immune response against Mtb infection, was also observed in BMDMs infected with these strains. In particular, BMDMs infected with all vaccine strains exhibited a significant upregulation of genes associated with the IL-17 pathway. These results may indicate that our vaccine strains could induce a protective immune response against TB.
format Article
id doaj-art-96ae53c29686486e81a6772394fb0e85
institution Kabale University
issn 1664-3224
language English
publishDate 2025-07-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj-art-96ae53c29686486e81a6772394fb0e852025-08-20T03:28:41ZengFrontiers Media S.A.Frontiers in Immunology1664-32242025-07-011610.3389/fimmu.2025.15834391583439Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosisRaja Veerapandian0Barbara Yang1Areanna Carmona2Melina J. Sedano3Victoria Reid4Victoria Reid5Rodrigo Jimenez6Rodrigo Jimenez7Jessica Chacon8Chinnaswamy Jagannath9Enrique I. Ramos10Enrique I. Ramos11Shrikanth S. Gadad12Shrikanth S. Gadad13Subramanian Dhandayuthapani14Subramanian Dhandayuthapani15Center of Emphasis in Infectious Diseases, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesCenter of Emphasis in Cancer, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesCenter of Emphasis in Infectious Diseases, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesCenter of Emphasis in Cancer, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesCenter of Emphasis in Infectious Diseases, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesCenter of Emphasis in Cancer, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesCenter of Emphasis in Infectious Diseases, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesFrederick L. Francis School of Biomedical Sciences, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesDepartment of Medical Education, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesDepartment of Pathology and Genomic Medicine, Houston Methodist Research Institute & Weill Cornell Medical College, Houston, TX, United StatesCenter of Emphasis in Cancer, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesDepartment of Biology, University of Texas El Paso, El Paso, TX, United StatesCenter of Emphasis in Cancer, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesFrederick L. Francis School of Biomedical Sciences, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesCenter of Emphasis in Infectious Diseases, Department of Molecular and Translational Medicine, Paul L. Foster School of Medicine, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesFrederick L. Francis School of Biomedical Sciences, Texas Tech University Health Sciences Center El Paso, El Paso, TX, United StatesThe BCG vaccine has been used against tuberculosis (TB) for over a hundred years; however, it does not protect adults from pulmonary TB. To develop alternative vaccines against TB, we generated Mycobacterium tuberculosis H37Rv (Mtb)-derived vaccine strains by rationally deleting key virulent genes, resulting in single (SKO; ΔfbpA), double (DKO; ΔfbpA-ΔsapM), triple (TKO-D; ΔfbpA-ΔsapM-ΔdosR and TKO-Z; ΔfbpA-ΔsapM-Δzmp1), and quadruple (QKO; ΔfbpA-ΔsapM-Δzmp1-dosR) strains. To understand how macrophages, the host cells that defend against infection and process antigens for presentation to immune cells, respond to these vaccine strains, we performed transcriptomic analyses of mouse bone marrow-derived macrophages (BMDMs) infected with these strains. The transcriptomic data were compared with similar data obtained from macrophages infected with Mtb H37Rv and BCG. Our analyses revealed that genes associated with various immune and cell signaling pathways, such as NF-kappa B signaling, TNF signaling, cytokine-cytokine receptor interaction, chemokine signaling, hematopoietic cell lineage, Toll-like receptor signaling, IL-17 signaling, Th1 and Th2 cell differentiation, Th17 cell differentiation, and T cell receptor signaling were differentially expressed in BMDMs infected with our vaccine strains. Enhanced expression of cytokines and chemokines, including proinflammatory cytokines such as TNF-α, IL-6, GM-CSF, and IL-1, which are essential for the immune response against Mtb infection, was also observed in BMDMs infected with these strains. In particular, BMDMs infected with all vaccine strains exhibited a significant upregulation of genes associated with the IL-17 pathway. These results may indicate that our vaccine strains could induce a protective immune response against TB.https://www.frontiersin.org/articles/10.3389/fimmu.2025.1583439/fullMtb-vaccinesBCGmousemacrophagesRNA-sequencingtranscripts
spellingShingle Raja Veerapandian
Barbara Yang
Areanna Carmona
Melina J. Sedano
Victoria Reid
Victoria Reid
Rodrigo Jimenez
Rodrigo Jimenez
Jessica Chacon
Chinnaswamy Jagannath
Enrique I. Ramos
Enrique I. Ramos
Shrikanth S. Gadad
Shrikanth S. Gadad
Subramanian Dhandayuthapani
Subramanian Dhandayuthapani
Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosis
Frontiers in Immunology
Mtb-vaccines
BCG
mouse
macrophages
RNA-sequencing
transcripts
title Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosis
title_full Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosis
title_fullStr Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosis
title_full_unstemmed Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosis
title_short Comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of Mycobacterium tuberculosis
title_sort comparative transcriptomic analysis of mouse macrophages infected with live attenuated vaccine strains of mycobacterium tuberculosis
topic Mtb-vaccines
BCG
mouse
macrophages
RNA-sequencing
transcripts
url https://www.frontiersin.org/articles/10.3389/fimmu.2025.1583439/full
work_keys_str_mv AT rajaveerapandian comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT barbarayang comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT areannacarmona comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT melinajsedano comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT victoriareid comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT victoriareid comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT rodrigojimenez comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT rodrigojimenez comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT jessicachacon comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT chinnaswamyjagannath comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT enriqueiramos comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT enriqueiramos comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT shrikanthsgadad comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT shrikanthsgadad comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT subramaniandhandayuthapani comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis
AT subramaniandhandayuthapani comparativetranscriptomicanalysisofmousemacrophagesinfectedwithliveattenuatedvaccinestrainsofmycobacteriumtuberculosis