Tuberculosis Exacerbates HIV-1 Infection through IL-10/STAT3-Dependent Tunneling Nanotube Formation in Macrophages
The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present...
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| Published in | Cell reports (Cambridge) Vol. 26; no. 13; pp. 3586 - 3599.e7 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
26.03.2019
Elsevier |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironment, produce high levels of HIV-1. In vivo, M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Furthermore, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics.
[Display omitted]
•TB-induced anti-inflammatory M(IL-10) macrophages are prone to HIV-1 overproduction•Tunneling nanotubes between TB-induced M(IL-10) macrophages promote HIV-1 spread•The IL-10/STAT3 axis triggers tunneling nanotube induction in the TB microenvironment•M(IL-10) macrophages accumulate in TB/HIV co-infected patients and non-human primates
Tuberculosis is a clear, yet confounding, risk factor for HIV-1-induced morbidity and mortality. In this issue, Souriant et al. reveal that a tuberculosis-associated microenvironment triggers IL-10/STAT3-dependent tunneling nanotube formation in M(IL-10) macrophages, which promotes HIV-1 exacerbation during co-infection. M(IL-10) macrophage accumulation is also observed in vivo in co-infected subjects. |
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| AbstractList | The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironments, produce high levels of HIV-1. In vivo, M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Further, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics. The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironment, produce high levels of HIV-1. In vivo, M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Furthermore, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics. The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironment, produce high levels of HIV-1. In vivo, M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Furthermore, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics. : Tuberculosis is a clear, yet confounding, risk factor for HIV-1-induced morbidity and mortality. In this issue, Souriant et al. reveal that a tuberculosis-associated microenvironment triggers IL-10/STAT3-dependent tunneling nanotube formation in M(IL-10) macrophages, which promotes HIV-1 exacerbation during co-infection. M(IL-10) macrophage accumulation is also observed in vivo in co-infected subjects. Keywords: AIDS, HIV-1, tuberculosis, Mycobacterium tuberculosis, co-infection, macrophage, monocyte, IL-10, STAT3, viral spread, tunneling nanotubes, biomarker The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironment, produce high levels of HIV-1. In vivo, M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Furthermore, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics. [Display omitted] •TB-induced anti-inflammatory M(IL-10) macrophages are prone to HIV-1 overproduction•Tunneling nanotubes between TB-induced M(IL-10) macrophages promote HIV-1 spread•The IL-10/STAT3 axis triggers tunneling nanotube induction in the TB microenvironment•M(IL-10) macrophages accumulate in TB/HIV co-infected patients and non-human primates Tuberculosis is a clear, yet confounding, risk factor for HIV-1-induced morbidity and mortality. In this issue, Souriant et al. reveal that a tuberculosis-associated microenvironment triggers IL-10/STAT3-dependent tunneling nanotube formation in M(IL-10) macrophages, which promotes HIV-1 exacerbation during co-infection. M(IL-10) macrophage accumulation is also observed in vivo in co-infected subjects. The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironment, produce high levels of HIV-1. In vivo, M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Furthermore, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics.The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironment, produce high levels of HIV-1. In vivo, M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Furthermore, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics. The tuberculosis (TB) bacillus, Mycobacterium tuberculosis (Mtb), and HIV-1 act synergistically; however, the mechanisms by which Mtb exacerbates HIV-1 pathogenesis are not well known. Using in vitro and ex vivo cell culture systems, we show that human M(IL-10) anti-inflammatory macrophages, present in TB-associated microenvironments, produce high levels of HIV-1. In vivo , M(IL-10) macrophages are expanded in lungs of co-infected non-human primates, which correlates with disease severity. Further, HIV-1/Mtb co-infected patients display an accumulation of M(IL-10) macrophage markers (soluble CD163 and MerTK). These M(IL-10) macrophages form direct cell-to-cell bridges, which we identified as tunneling nanotubes (TNTs) involved in viral transfer. TNT formation requires the IL-10/STAT3 signaling pathway, and targeted inhibition of TNTs substantially reduces the enhancement of HIV-1 cell-to-cell transfer and overproduction in M(IL-10) macrophages. Our study reveals that TNTs facilitate viral transfer and amplification, thereby promoting TNT formation as a mechanism to be explored in TB/AIDS potential therapeutics. |
| Author | Allers, Carolina González-Montaner, Pablo Balboa, Luciana Kuroda, Marcelo J. Gasser, Romain Neyrolles, Olivier Raynaud-Messina, Brigitte Al Saati, Talal Lugo-Villarino, Geanncarlo Vérollet, Christel Maridonneau-Parini, Isabelle Dupont, Maeva Bah, Aicha Poggi, Susana Kviatcovsky, Denise Pingris, Karine Cougoule, Céline Sasiain, Maria del Carmen Moraña, Eduardo Jose Lastrucci, Claire Corti, Marcelo Lagane, Bernard Kaushal, Deepak Poincloux, Renaud Souriant, Shanti Vergne, Isabelle Inwentarz, Sandra |
| AuthorAffiliation | 2 International associated laboratory (LIA) CNRS “IM-TB/HIV” , Toulouse, France and Buenos Aires, Argentina 7 Instituto de Tisioneumonologia « Raúl F. Vaccarezza », Universitad de Buenos Aires, Argentina 1 Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France 5 Centre de Physiopathologie de Toulouse Purpan, INSERM UMR 1043, CNRS UMR 5282, Université Toulouse III Paul Sabatier, Toulouse, France 9 Tulane National Primate Research Center, Covington, LA 70433; Department of Microbiology and Immunology, School of Medicine, Tulane University, New Orleans, LA 70112 4 Centre for Genomic Regulation, Barcelona, Spain 6 INSERM/UPS/ENVT - US006/CREFRE, Service d’Histopathologie, CHU Purpan, 31024, Toulouse, France 8 Division de SIDA, Hospital de Infecciosas Dr. F.J. Muñiz, Buenos Aires, Argentina 3 Institute of Experimental Medicine-CONICET, National Academy of Medicine, Buenos Aires, Argentina |
| AuthorAffiliation_xml | – name: 4 Centre for Genomic Regulation, Barcelona, Spain – name: 2 International associated laboratory (LIA) CNRS “IM-TB/HIV” , Toulouse, France and Buenos Aires, Argentina – name: 8 Division de SIDA, Hospital de Infecciosas Dr. F.J. Muñiz, Buenos Aires, Argentina – name: 9 Tulane National Primate Research Center, Covington, LA 70433; Department of Microbiology and Immunology, School of Medicine, Tulane University, New Orleans, LA 70112 – name: 1 Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – name: 5 Centre de Physiopathologie de Toulouse Purpan, INSERM UMR 1043, CNRS UMR 5282, Université Toulouse III Paul Sabatier, Toulouse, France – name: 6 INSERM/UPS/ENVT - US006/CREFRE, Service d’Histopathologie, CHU Purpan, 31024, Toulouse, France – name: 3 Institute of Experimental Medicine-CONICET, National Academy of Medicine, Buenos Aires, Argentina – name: 7 Instituto de Tisioneumonologia « Raúl F. Vaccarezza », Universitad de Buenos Aires, Argentina |
| Author_xml | – sequence: 1 givenname: Shanti surname: Souriant fullname: Souriant, Shanti organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 2 givenname: Luciana surname: Balboa fullname: Balboa, Luciana organization: International Associated Laboratory (LIA) CNRS “IM-TB/HIV” , Toulouse, France, and Buenos Aires, Argentina – sequence: 3 givenname: Maeva surname: Dupont fullname: Dupont, Maeva organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 4 givenname: Karine surname: Pingris fullname: Pingris, Karine organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 5 givenname: Denise surname: Kviatcovsky fullname: Kviatcovsky, Denise organization: International Associated Laboratory (LIA) CNRS “IM-TB/HIV” , Toulouse, France, and Buenos Aires, Argentina – sequence: 6 givenname: Céline surname: Cougoule fullname: Cougoule, Céline organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 7 givenname: Claire surname: Lastrucci fullname: Lastrucci, Claire organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 8 givenname: Aicha surname: Bah fullname: Bah, Aicha organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 9 givenname: Romain surname: Gasser fullname: Gasser, Romain organization: Centre de Physiopathologie de Toulouse Purpan, INSERM UMR 1043, CNRS UMR 5282, Université Toulouse III Paul Sabatier, Toulouse, France – sequence: 10 givenname: Renaud surname: Poincloux fullname: Poincloux, Renaud organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 11 givenname: Brigitte surname: Raynaud-Messina fullname: Raynaud-Messina, Brigitte organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 12 givenname: Talal surname: Al Saati fullname: Al Saati, Talal organization: INSERM/UPS/ENVT–US006/CREFRE, Service d’Histopathologie, CHU Purpan, 31024 Toulouse, France – sequence: 13 givenname: Sandra surname: Inwentarz fullname: Inwentarz, Sandra organization: Instituto de Tisioneumonologia “Raúl F. Vaccarezza,” Universitad de Buenos Aires, Argentina – sequence: 14 givenname: Susana surname: Poggi fullname: Poggi, Susana organization: Instituto de Tisioneumonologia “Raúl F. Vaccarezza,” Universitad de Buenos Aires, Argentina – sequence: 15 givenname: Eduardo Jose surname: Moraña fullname: Moraña, Eduardo Jose organization: Instituto de Tisioneumonologia “Raúl F. Vaccarezza,” Universitad de Buenos Aires, Argentina – sequence: 16 givenname: Pablo surname: González-Montaner fullname: González-Montaner, Pablo organization: Instituto de Tisioneumonologia “Raúl F. Vaccarezza,” Universitad de Buenos Aires, Argentina – sequence: 17 givenname: Marcelo surname: Corti fullname: Corti, Marcelo organization: Division de SIDA, Hospital de Infecciosas Dr. F.J. Muñiz, Buenos Aires, Argentina – sequence: 18 givenname: Bernard surname: Lagane fullname: Lagane, Bernard organization: Centre de Physiopathologie de Toulouse Purpan, INSERM UMR 1043, CNRS UMR 5282, Université Toulouse III Paul Sabatier, Toulouse, France – sequence: 19 givenname: Isabelle surname: Vergne fullname: Vergne, Isabelle organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 20 givenname: Carolina surname: Allers fullname: Allers, Carolina organization: Tulane National Primate Research Center, Covington, LA 70433, USA – sequence: 21 givenname: Deepak surname: Kaushal fullname: Kaushal, Deepak organization: Tulane National Primate Research Center, Covington, LA 70433, USA – sequence: 22 givenname: Marcelo J. surname: Kuroda fullname: Kuroda, Marcelo J. organization: Tulane National Primate Research Center, Covington, LA 70433, USA – sequence: 23 givenname: Maria del Carmen surname: Sasiain fullname: Sasiain, Maria del Carmen organization: International Associated Laboratory (LIA) CNRS “IM-TB/HIV” , Toulouse, France, and Buenos Aires, Argentina – sequence: 24 givenname: Olivier surname: Neyrolles fullname: Neyrolles, Olivier organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 25 givenname: Isabelle surname: Maridonneau-Parini fullname: Maridonneau-Parini, Isabelle organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 26 givenname: Geanncarlo orcidid: 0000-0003-4620-8491 surname: Lugo-Villarino fullname: Lugo-Villarino, Geanncarlo email: lugo@ipbs.fr organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France – sequence: 27 givenname: Christel surname: Vérollet fullname: Vérollet, Christel email: verollet@ipbs.fr organization: Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30917314$$D View this record in MEDLINE/PubMed https://hal.science/hal-03034321$$DView record in HAL |
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| ContentType | Journal Article |
| Copyright | 2019 The Author(s) Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved. Distributed under a Creative Commons Attribution 4.0 International License |
| Copyright_xml | – notice: 2019 The Author(s) – notice: Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved. – notice: Distributed under a Creative Commons Attribution 4.0 International License |
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| Keywords | HIV-1 Mycobacterium tuberculosis co-infection tuberculosis STAT3 AIDS macrophage monocyte tunneling nanotubes viral spread biomarker IL-10 Biomarker Co-infection Tuberculosis Monocyte Tunneling nanotubes Viral spread Macrophage |
| Language | English |
| License | This is an open access article under the CC BY-NC-ND license. Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 PMCID: PMC6733268 These authors contributed equally to this work AUTHOR CONTRIBUTIONS Conceptualization & methodology: SS, LB, MdCS, ON, IMP, GLV, CV. Software: SS, RP. Investigation: SS, LB, MD, KP, CL, DK, CC, AB, RG, RP, BRM. Resources: SI, EJM, PGM, SP, MC. Writing: SS, ON, IMP, GLV, CV. Visualization: SS. Supervision: ON, IMP, GLV, CV. Corresponding authors: GLV is responsible for ownership and responsibility that are inherent to aspects on tuberculosis and CV on HIV1. Lead contact |
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| Title | Tuberculosis Exacerbates HIV-1 Infection through IL-10/STAT3-Dependent Tunneling Nanotube Formation in Macrophages |
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