Circulating monocytes (Mo) play an essential role in the host immune response to chronic infections. We previously demonstrated that CD16pos Mo were expanded in TB (tuberculosis) patients, correlated with disease severity and were refractory to dendritic cell differentiation. In the present study, we investigated whether human Mo subsets (CD16neg and CD16pos) differed in their ability to influence the early inflammatory response against Mycobacterium tuberculosis. We first evaluated the capacity of the Mo subsets to migrate and engage a microbicidal response in vitro. Accordingly, CD16neg Mo were more prone to migrate in response to different mycobacteria-derived gradients, were more resistant to M. tuberculosis intracellular growth and produced higher reactive oxygen species than their CD16pos counterpart. To assess further the functional dichotomy among the human Mo subsets, we carried out an in vivo analysis by adapting a hybrid mouse model (SCID/Beige, where SCID is severe combined immunodeficient) to transfer each Mo subset, track their migratory fate during M. tuberculosis infection, and determine their impact on the host immune response. In M. tuberculosis-infected mice, the adoptively transferred CD16neg Mo displayed a higher lung migration index, induced a stronger pulmonary infiltration of murine leucocytes expressing pro- and anti-inflammatory cytokines, and significantly decreased the bacterial burden, in comparison with CD16pos Mo. Collectively, our results indicate that human Mo subsets display divergent biological roles in the context of M. tuberculosis infection, a scenario in which CD16neg Mo may contribute to the anti-mycobacterial immune response, whereas CD16pos Mo might promote microbial resilience, shedding light on a key aspect of the physiopathology of TB disease.
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Research Article|
May 21 2015
Diverging biological roles among human monocyte subsets in the context of tuberculosis infection
Luciana Balboa;
*Institute of Experimental Medicine-CONICET, National Academy of Medicine, Pacheco de Melo 3081 (1425), Buenos Aires, Argentina
Correspondence: Dr Luciana Balboa (email luciana_balboa@hotmail.com).
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Jorge Barrios-Payan;
Jorge Barrios-Payan
1
†Department of Experimental Pathology, National Institute of Medical Sciences & Nutrition “Salvador Zubirán”, Vasco de Quiroga 15, Sección 16, Delegación Tlalpan (14000), Mexico City, Mexico
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Erika González-Domínguez;
Erika González-Domínguez
1
‡Department of Molecular Biomedicine, Center for Research and Advances Studies, National Polytechnic Institute, Av. Instituto Politécnico Nacional 2508, Gustavo A. Madero, San Pedro Zacatenco (07360), Mexico City, Mexico
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Claire Lastrucci;
Claire Lastrucci
§CNRS, Institut de Pharmacologie et de Biologie Structurale, 205 route de Narbonne (31077), Toulouse, France
║Institut de Pharmacologie et de Biologie Structurale, Université de Toulouse, Université Paul Sabatier, 118 route de Narbonne (31062), Toulouse, France
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Geanncarlo Lugo-Villarino;
Geanncarlo Lugo-Villarino
§CNRS, Institut de Pharmacologie et de Biologie Structurale, 205 route de Narbonne (31077), Toulouse, France
║Institut de Pharmacologie et de Biologie Structurale, Université de Toulouse, Université Paul Sabatier, 118 route de Narbonne (31062), Toulouse, France
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Dulce Mata-Espinoza;
Dulce Mata-Espinoza
†Department of Experimental Pathology, National Institute of Medical Sciences & Nutrition “Salvador Zubirán”, Vasco de Quiroga 15, Sección 16, Delegación Tlalpan (14000), Mexico City, Mexico
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Pablo Schierloh;
Pablo Schierloh
*Institute of Experimental Medicine-CONICET, National Academy of Medicine, Pacheco de Melo 3081 (1425), Buenos Aires, Argentina
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Denise Kviatcovsky;
Denise Kviatcovsky
*Institute of Experimental Medicine-CONICET, National Academy of Medicine, Pacheco de Melo 3081 (1425), Buenos Aires, Argentina
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Olivier Neyrolles;
Olivier Neyrolles
§CNRS, Institut de Pharmacologie et de Biologie Structurale, 205 route de Narbonne (31077), Toulouse, France
║Institut de Pharmacologie et de Biologie Structurale, Université de Toulouse, Université Paul Sabatier, 118 route de Narbonne (31062), Toulouse, France
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Isabelle Maridonneau-Parini;
Isabelle Maridonneau-Parini
§CNRS, Institut de Pharmacologie et de Biologie Structurale, 205 route de Narbonne (31077), Toulouse, France
║Institut de Pharmacologie et de Biologie Structurale, Université de Toulouse, Université Paul Sabatier, 118 route de Narbonne (31062), Toulouse, France
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Carmen Sánchez-Torres;
Carmen Sánchez-Torres
‡Department of Molecular Biomedicine, Center for Research and Advances Studies, National Polytechnic Institute, Av. Instituto Politécnico Nacional 2508, Gustavo A. Madero, San Pedro Zacatenco (07360), Mexico City, Mexico
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María del Carmen Sasiain;
María del Carmen Sasiain
2
*Institute of Experimental Medicine-CONICET, National Academy of Medicine, Pacheco de Melo 3081 (1425), Buenos Aires, Argentina
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Rogelio Hernández-Pando
Rogelio Hernández-Pando
2
†Department of Experimental Pathology, National Institute of Medical Sciences & Nutrition “Salvador Zubirán”, Vasco de Quiroga 15, Sección 16, Delegación Tlalpan (14000), Mexico City, Mexico
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Publisher: Portland Press Ltd
Received:
January 05 2015
Revision Received:
April 09 2015
Accepted:
April 10 2015
Accepted Manuscript online:
April 10 2015
Online ISSN: 1470-8736
Print ISSN: 0143-5221
© The Authors Journal compilation © 2015 Biochemical Society
2015
Clin Sci (Lond) (2015) 129 (4): 319–330.
Article history
Received:
January 05 2015
Revision Received:
April 09 2015
Accepted:
April 10 2015
Accepted Manuscript online:
April 10 2015
Citation
Luciana Balboa, Jorge Barrios-Payan, Erika González-Domínguez, Claire Lastrucci, Geanncarlo Lugo-Villarino, Dulce Mata-Espinoza, Pablo Schierloh, Denise Kviatcovsky, Olivier Neyrolles, Isabelle Maridonneau-Parini, Carmen Sánchez-Torres, María del Carmen Sasiain, Rogelio Hernández-Pando; Diverging biological roles among human monocyte subsets in the context of tuberculosis infection. Clin Sci (Lond) 1 August 2015; 129 (4): 319–330. doi: https://doi.org/10.1042/CS20150021
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