Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages

Autores
Dupont, Maeva; Souriant, Shanti; Balboa, Luciana; Vu Manh, Thien Phong; Pingris, Karine; Rousset, Stella; Cougoule, Céline; Rombouts, Yoann; Poincloux, Renaud; Ben Neji, Myriam; Allers, Carolina; Kaushal, Deepak; Kuroda, Marcelo J.; Benet, Susana; Martinez Picado, Javier; Izquierdo Useros, Nuria; Sasiain, Maria del Carmen; Maridonneau Parini, Isabelle; Neyrolles, Olivier; Vérollet, Christel; Lugo Villarino, Geanncarlo
Año de publicación
2020
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
While tuberculosis (TB) is a risk factor in HIV-1-infected individuals, the mechanisms by which Mycobacterium tuberculosis (Mtb) worsens HIV-1 pathogenesis remain scarce. We showed that HIV-1 infection is exacerbated in macrophages exposed to TB-associated microenvironments due to tunneling nanotube (TNT) formation. To identify molecular factors associated with TNT function, we performed a transcriptomic analysis in these macrophages, and revealed the up-regulation of Siglec-1 receptor. Siglec-1 expression depends on Mtb-induced production of type I interferon (IFN-I). In co-infected non-human primates, Siglec-1 is highly expressed by alveolar macrophages, whose abundance correlates with pathology and activation of IFN-I/STAT1 pathway. Siglec-1 localizes mainly on microtubule-containing TNT that are long and carry HIV-1 cargo. Siglec-1 depletion decreases TNT length, diminishes HIV-1 capture and cell-to-cell transfer, and abrogates the exacerbation of HIV-1 infection induced by Mtb. Altogether, we uncover a deleterious role for Siglec-1 in TB-HIV-1 co-infection and opens new avenues to understand TNT biology.
Fil: Dupont, Maeva. International associated laboratory; Francia. Université de Toulouse; Francia
Fil: Souriant, Shanti. International associated laboratory; Francia. Université de Toulouse; Francia
Fil: Balboa, Luciana. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Medicina Experimental. Academia Nacional de Medicina de Buenos Aires. Instituto de Medicina Experimental; Argentina. International associated laboratory; Francia
Fil: Vu Manh, Thien Phong. Toulouse University Hospital; Francia
Fil: Pingris, Karine. Université de Toulouse; Francia
Fil: Rousset, Stella. Toulouse University Hospital; Francia
Fil: Cougoule, Céline. Université de Toulouse; Argentina
Fil: Rombouts, Yoann. Université de Toulouse; Argentina
Fil: Poincloux, Renaud. Université de Toulouse; Argentina
Fil: Ben Neji, Myriam. Université de Toulouse; Argentina
Fil: Allers, Carolina. Tulane University; Estados Unidos
Fil: Kaushal, Deepak. University of Tulane; Estados Unidos
Fil: Kuroda, Marcelo J.. University of California; Estados Unidos
Fil: Benet, Susana. Irsicaixa Aids Research Institute; España. Universitat Autònoma de Barcelona; España
Fil: Martinez Picado, Javier. Universitat Autònoma de Barcelona; España
Fil: Izquierdo Useros, Nuria. Irsicaixa Aids Research Institute; España
Fil: Sasiain, Maria del Carmen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Medicina Experimental. Academia Nacional de Medicina de Buenos Aires. Instituto de Medicina Experimental; Argentina
Fil: Maridonneau Parini, Isabelle. Université de Toulouse; Francia
Fil: Neyrolles, Olivier. Université de Toulouse; Francia
Fil: Vérollet, Christel. Université de Toulouse; Francia
Fil: Lugo Villarino, Geanncarlo. Université de Toulouse; Francia
Materia
coinfection TB / HIV
macrophages
SIGLEC-1
tunneling nanotube
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/146518
Acceder
id CONICETDig_771320b4ce93cd3709415975d9d667ba
oai_identifier_str oai:ri.conicet.gov.ar:11336/146518
network_acronym_str CONICETDig
repository_id_str 3498
network_name_str CONICET Digital (CONICET)
spelling Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophagesDupont, MaevaSouriant, ShantiBalboa, LucianaVu Manh, Thien PhongPingris, KarineRousset, StellaCougoule, CélineRombouts, YoannPoincloux, RenaudBen Neji, MyriamAllers, CarolinaKaushal, DeepakKuroda, Marcelo J.Benet, SusanaMartinez Picado, JavierIzquierdo Useros, NuriaSasiain, Maria del CarmenMaridonneau Parini, IsabelleNeyrolles, OlivierVérollet, ChristelLugo Villarino, Geanncarlocoinfection TB / HIVmacrophagesSIGLEC-1tunneling nanotubehttps://purl.org/becyt/ford/3.1https://purl.org/becyt/ford/3While tuberculosis (TB) is a risk factor in HIV-1-infected individuals, the mechanisms by which Mycobacterium tuberculosis (Mtb) worsens HIV-1 pathogenesis remain scarce. We showed that HIV-1 infection is exacerbated in macrophages exposed to TB-associated microenvironments due to tunneling nanotube (TNT) formation. To identify molecular factors associated with TNT function, we performed a transcriptomic analysis in these macrophages, and revealed the up-regulation of Siglec-1 receptor. Siglec-1 expression depends on Mtb-induced production of type I interferon (IFN-I). In co-infected non-human primates, Siglec-1 is highly expressed by alveolar macrophages, whose abundance correlates with pathology and activation of IFN-I/STAT1 pathway. Siglec-1 localizes mainly on microtubule-containing TNT that are long and carry HIV-1 cargo. Siglec-1 depletion decreases TNT length, diminishes HIV-1 capture and cell-to-cell transfer, and abrogates the exacerbation of HIV-1 infection induced by Mtb. Altogether, we uncover a deleterious role for Siglec-1 in TB-HIV-1 co-infection and opens new avenues to understand TNT biology.Fil: Dupont, Maeva. International associated laboratory; Francia. Université de Toulouse; FranciaFil: Souriant, Shanti. International associated laboratory; Francia. Université de Toulouse; FranciaFil: Balboa, Luciana. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Medicina Experimental. Academia Nacional de Medicina de Buenos Aires. Instituto de Medicina Experimental; Argentina. International associated laboratory; FranciaFil: Vu Manh, Thien Phong. Toulouse University Hospital; FranciaFil: Pingris, Karine. Université de Toulouse; FranciaFil: Rousset, Stella. Toulouse University Hospital; FranciaFil: Cougoule, Céline. Université de Toulouse; ArgentinaFil: Rombouts, Yoann. Université de Toulouse; ArgentinaFil: Poincloux, Renaud. Université de Toulouse; ArgentinaFil: Ben Neji, Myriam. Université de Toulouse; ArgentinaFil: Allers, Carolina. Tulane University; Estados UnidosFil: Kaushal, Deepak. University of Tulane; Estados UnidosFil: Kuroda, Marcelo J.. University of California; Estados UnidosFil: Benet, Susana. Irsicaixa Aids Research Institute; España. Universitat Autònoma de Barcelona; EspañaFil: Martinez Picado, Javier. Universitat Autònoma de Barcelona; EspañaFil: Izquierdo Useros, Nuria. Irsicaixa Aids Research Institute; EspañaFil: Sasiain, Maria del Carmen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Medicina Experimental. Academia Nacional de Medicina de Buenos Aires. Instituto de Medicina Experimental; ArgentinaFil: Maridonneau Parini, Isabelle. Université de Toulouse; FranciaFil: Neyrolles, Olivier. Université de Toulouse; FranciaFil: Vérollet, Christel. Université de Toulouse; FranciaFil: Lugo Villarino, Geanncarlo. Université de Toulouse; FranciaeLife Sciences Publications Ltd2020-03info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/146518Dupont, Maeva; Souriant, Shanti; Balboa, Luciana; Vu Manh, Thien Phong; Pingris, Karine; et al.; Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages; eLife Sciences Publications Ltd; eLife; 9; 3-2020; 1-392050-084XCONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/url/https://elifesciences.org/articles/52535info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.52535info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-17T10:56:58Zoai:ri.conicet.gov.ar:11336/146518instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-17 10:56:58.558CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
title Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
spellingShingle Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
Dupont, Maeva
coinfection TB / HIV
macrophages
SIGLEC-1
tunneling nanotube
title_short Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
title_full Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
title_fullStr Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
title_full_unstemmed Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
title_sort Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages
dc.creator.none.fl_str_mv Dupont, Maeva
Souriant, Shanti
Balboa, Luciana
Vu Manh, Thien Phong
Pingris, Karine
Rousset, Stella
Cougoule, Céline
Rombouts, Yoann
Poincloux, Renaud
Ben Neji, Myriam
Allers, Carolina
Kaushal, Deepak
Kuroda, Marcelo J.
Benet, Susana
Martinez Picado, Javier
Izquierdo Useros, Nuria
Sasiain, Maria del Carmen
Maridonneau Parini, Isabelle
Neyrolles, Olivier
Vérollet, Christel
Lugo Villarino, Geanncarlo
author Dupont, Maeva
author_facet Dupont, Maeva
Souriant, Shanti
Balboa, Luciana
Vu Manh, Thien Phong
Pingris, Karine
Rousset, Stella
Cougoule, Céline
Rombouts, Yoann
Poincloux, Renaud
Ben Neji, Myriam
Allers, Carolina
Kaushal, Deepak
Kuroda, Marcelo J.
Benet, Susana
Martinez Picado, Javier
Izquierdo Useros, Nuria
Sasiain, Maria del Carmen
Maridonneau Parini, Isabelle
Neyrolles, Olivier
Vérollet, Christel
Lugo Villarino, Geanncarlo
author_role author
author2 Souriant, Shanti
Balboa, Luciana
Vu Manh, Thien Phong
Pingris, Karine
Rousset, Stella
Cougoule, Céline
Rombouts, Yoann
Poincloux, Renaud
Ben Neji, Myriam
Allers, Carolina
Kaushal, Deepak
Kuroda, Marcelo J.
Benet, Susana
Martinez Picado, Javier
Izquierdo Useros, Nuria
Sasiain, Maria del Carmen
Maridonneau Parini, Isabelle
Neyrolles, Olivier
Vérollet, Christel
Lugo Villarino, Geanncarlo
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.subject.none.fl_str_mv coinfection TB / HIV
macrophages
SIGLEC-1
tunneling nanotube
topic coinfection TB / HIV
macrophages
SIGLEC-1
tunneling nanotube
purl_subject.fl_str_mv https://purl.org/becyt/ford/3.1
https://purl.org/becyt/ford/3
dc.description.none.fl_txt_mv While tuberculosis (TB) is a risk factor in HIV-1-infected individuals, the mechanisms by which Mycobacterium tuberculosis (Mtb) worsens HIV-1 pathogenesis remain scarce. We showed that HIV-1 infection is exacerbated in macrophages exposed to TB-associated microenvironments due to tunneling nanotube (TNT) formation. To identify molecular factors associated with TNT function, we performed a transcriptomic analysis in these macrophages, and revealed the up-regulation of Siglec-1 receptor. Siglec-1 expression depends on Mtb-induced production of type I interferon (IFN-I). In co-infected non-human primates, Siglec-1 is highly expressed by alveolar macrophages, whose abundance correlates with pathology and activation of IFN-I/STAT1 pathway. Siglec-1 localizes mainly on microtubule-containing TNT that are long and carry HIV-1 cargo. Siglec-1 depletion decreases TNT length, diminishes HIV-1 capture and cell-to-cell transfer, and abrogates the exacerbation of HIV-1 infection induced by Mtb. Altogether, we uncover a deleterious role for Siglec-1 in TB-HIV-1 co-infection and opens new avenues to understand TNT biology.
Fil: Dupont, Maeva. International associated laboratory; Francia. Université de Toulouse; Francia
Fil: Souriant, Shanti. International associated laboratory; Francia. Université de Toulouse; Francia
Fil: Balboa, Luciana. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Medicina Experimental. Academia Nacional de Medicina de Buenos Aires. Instituto de Medicina Experimental; Argentina. International associated laboratory; Francia
Fil: Vu Manh, Thien Phong. Toulouse University Hospital; Francia
Fil: Pingris, Karine. Université de Toulouse; Francia
Fil: Rousset, Stella. Toulouse University Hospital; Francia
Fil: Cougoule, Céline. Université de Toulouse; Argentina
Fil: Rombouts, Yoann. Université de Toulouse; Argentina
Fil: Poincloux, Renaud. Université de Toulouse; Argentina
Fil: Ben Neji, Myriam. Université de Toulouse; Argentina
Fil: Allers, Carolina. Tulane University; Estados Unidos
Fil: Kaushal, Deepak. University of Tulane; Estados Unidos
Fil: Kuroda, Marcelo J.. University of California; Estados Unidos
Fil: Benet, Susana. Irsicaixa Aids Research Institute; España. Universitat Autònoma de Barcelona; España
Fil: Martinez Picado, Javier. Universitat Autònoma de Barcelona; España
Fil: Izquierdo Useros, Nuria. Irsicaixa Aids Research Institute; España
Fil: Sasiain, Maria del Carmen. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Medicina Experimental. Academia Nacional de Medicina de Buenos Aires. Instituto de Medicina Experimental; Argentina
Fil: Maridonneau Parini, Isabelle. Université de Toulouse; Francia
Fil: Neyrolles, Olivier. Université de Toulouse; Francia
Fil: Vérollet, Christel. Université de Toulouse; Francia
Fil: Lugo Villarino, Geanncarlo. Université de Toulouse; Francia
description While tuberculosis (TB) is a risk factor in HIV-1-infected individuals, the mechanisms by which Mycobacterium tuberculosis (Mtb) worsens HIV-1 pathogenesis remain scarce. We showed that HIV-1 infection is exacerbated in macrophages exposed to TB-associated microenvironments due to tunneling nanotube (TNT) formation. To identify molecular factors associated with TNT function, we performed a transcriptomic analysis in these macrophages, and revealed the up-regulation of Siglec-1 receptor. Siglec-1 expression depends on Mtb-induced production of type I interferon (IFN-I). In co-infected non-human primates, Siglec-1 is highly expressed by alveolar macrophages, whose abundance correlates with pathology and activation of IFN-I/STAT1 pathway. Siglec-1 localizes mainly on microtubule-containing TNT that are long and carry HIV-1 cargo. Siglec-1 depletion decreases TNT length, diminishes HIV-1 capture and cell-to-cell transfer, and abrogates the exacerbation of HIV-1 infection induced by Mtb. Altogether, we uncover a deleterious role for Siglec-1 in TB-HIV-1 co-infection and opens new avenues to understand TNT biology.
publishDate 2020
dc.date.none.fl_str_mv 2020-03
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
http://purl.org/coar/resource_type/c_6501
info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/146518
Dupont, Maeva; Souriant, Shanti; Balboa, Luciana; Vu Manh, Thien Phong; Pingris, Karine; et al.; Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages; eLife Sciences Publications Ltd; eLife; 9; 3-2020; 1-39
2050-084X
CONICET Digital
CONICET
url http://hdl.handle.net/11336/146518
identifier_str_mv Dupont, Maeva; Souriant, Shanti; Balboa, Luciana; Vu Manh, Thien Phong; Pingris, Karine; et al.; Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages; eLife Sciences Publications Ltd; eLife; 9; 3-2020; 1-39
2050-084X
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/url/https://elifesciences.org/articles/52535
info:eu-repo/semantics/altIdentifier/doi/10.7554/eLife.52535
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
application/pdf
dc.publisher.none.fl_str_mv eLife Sciences Publications Ltd
publisher.none.fl_str_mv eLife Sciences Publications Ltd
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
instname:Consejo Nacional de Investigaciones Científicas y Técnicas
reponame_str CONICET Digital (CONICET)
collection CONICET Digital (CONICET)
instname_str Consejo Nacional de Investigaciones Científicas y Técnicas
repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
repository.mail.fl_str_mv dasensio@conicet.gov.ar; lcarlino@conicet.gov.ar
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score 13.000565

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