Tuberculosis Exacerbates HIV-1 Infection through IL-10/STAT3-Dependent Tunneling Nanotube Formation in Macrophages.


Journal

Cell reports
ISSN: 2211-1247
Titre abrégé: Cell Rep
Pays: United States
ID NLM: 101573691

Informations de publication

Date de publication:
26 03 2019
Historique:
received: 23 08 2018
revised: 08 12 2018
accepted: 21 02 2019
entrez: 28 3 2019
pubmed: 28 3 2019
medline: 21 5 2020
Statut: ppublish

Résumé

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.

Identifiants

pubmed: 30917314
pii: S2211-1247(19)30277-3
doi: 10.1016/j.celrep.2019.02.091
pmc: PMC6733268
mid: NIHMS1044115
pii:
doi:

Substances chimiques

IL10 protein, human 0
STAT3 Transcription Factor 0
STAT3 protein, human 0
Interleukin-10 130068-27-8

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Pagination

3586-3599.e7

Subventions

Organisme : NIH HHS
ID : P51 OD011107
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI097059
Pays : United States
Organisme : NIH HHS
ID : P51 OD011104
Pays : United States
Organisme : NIAID NIH HHS
ID : R33 AI110163
Pays : United States
Organisme : NIAID NIH HHS
ID : R21 AI110163
Pays : United States
Organisme : NIAID NIH HHS
ID : UC6 AI058609
Pays : United States

Informations de copyright

Copyright © 2019 The Author(s). Published by Elsevier Inc. All rights reserved.

Auteurs

Shanti Souriant (S)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina.

Luciana Balboa (L)

International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina; Institute of Experimental Medicine-CONICET, National Academy of Medicine, Buenos Aires, Argentina.

Maeva Dupont (M)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina.

Karine Pingris (K)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France.

Denise Kviatcovsky (D)

International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina; Institute of Experimental Medicine-CONICET, National Academy of Medicine, Buenos Aires, Argentina.

Céline Cougoule (C)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina.

Claire Lastrucci (C)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; Centre for Genomic Regulation, Barcelona, Spain.

Aicha Bah (A)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France.

Romain Gasser (R)

Centre de Physiopathologie de Toulouse Purpan, INSERM UMR 1043, CNRS UMR 5282, Université Toulouse III Paul Sabatier, Toulouse, France.

Renaud Poincloux (R)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France.

Brigitte Raynaud-Messina (B)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France.

Talal Al Saati (T)

INSERM/UPS/ENVT-US006/CREFRE, Service d'Histopathologie, CHU Purpan, 31024 Toulouse, France.

Sandra Inwentarz (S)

Instituto de Tisioneumonologia "Raúl F. Vaccarezza," Universitad de Buenos Aires, Argentina.

Susana Poggi (S)

Instituto de Tisioneumonologia "Raúl F. Vaccarezza," Universitad de Buenos Aires, Argentina.

Eduardo Jose Moraña (EJ)

Instituto de Tisioneumonologia "Raúl F. Vaccarezza," Universitad de Buenos Aires, Argentina.

Pablo González-Montaner (P)

Instituto de Tisioneumonologia "Raúl F. Vaccarezza," Universitad de Buenos Aires, Argentina.

Marcelo Corti (M)

Division de SIDA, Hospital de Infecciosas Dr. F.J. Muñiz, Buenos Aires, Argentina.

Bernard Lagane (B)

Centre de Physiopathologie de Toulouse Purpan, INSERM UMR 1043, CNRS UMR 5282, Université Toulouse III Paul Sabatier, Toulouse, France.

Isabelle Vergne (I)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France.

Carolina Allers (C)

Tulane National Primate Research Center, Covington, LA 70433, USA; Department of Microbiology and Immunology, School of Medicine, Tulane University, New Orleans, LA 70112, USA.

Deepak Kaushal (D)

Tulane National Primate Research Center, Covington, LA 70433, USA; Department of Microbiology and Immunology, School of Medicine, Tulane University, New Orleans, LA 70112, USA.

Marcelo J Kuroda (MJ)

Tulane National Primate Research Center, Covington, LA 70433, USA; Department of Microbiology and Immunology, School of Medicine, Tulane University, New Orleans, LA 70112, USA.

Maria Del Carmen Sasiain (MDC)

International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina; Institute of Experimental Medicine-CONICET, National Academy of Medicine, Buenos Aires, Argentina.

Olivier Neyrolles (O)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina.

Isabelle Maridonneau-Parini (I)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina.

Geanncarlo Lugo-Villarino (G)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina. Electronic address: lugo@ipbs.fr.

Christel Vérollet (C)

Institut de Pharmacologie et Biologie Structurale, IPBS, Université de Toulouse, CNRS, UPS, Toulouse, France; International Associated Laboratory (LIA) CNRS "IM-TB/HIV" (1167), Toulouse, France, and Buenos Aires, Argentina. Electronic address: verollet@ipbs.fr.

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