Dysregulation of the IFN-I signaling pathway by Mycobacterium tuberculosis leads to exacerbation of HIV-1 infection of macrophages.
HIV-1
IFN-I signaling
coinfection
macrophages
tuberculosis
Journal
Journal of leukocyte biology
ISSN: 1938-3673
Titre abrégé: J Leukoc Biol
Pays: England
ID NLM: 8405628
Informations de publication
Date de publication:
11 2022
11 2022
Historique:
revised:
01
04
2022
received:
15
01
2022
pubmed:
20
5
2022
medline:
28
10
2022
entrez:
19
5
2022
Statut:
ppublish
Résumé
While tuberculosis (TB) is a risk factor in HIV-1-infected individuals, the mechanisms by which Mycobacterium tuberculosis (Mtb), the agent of TB in humans, worsens HIV-1 pathogenesis still need to be fully elucidated. Recently, we showed that HIV-1 infection and spread are exacerbated in macrophages exposed to TB-associated microenvironments. Transcriptomic analysis of macrophages conditioned with medium of Mtb-infected human macrophages (cmMTB) revealed an up-regulation of the typeI interferon (IFN-I) pathway, characterized by the overexpression of IFN-inducible genes. Historically, IFN-I are well known for their antiviral functions, but our previous work showed that this is not the case in the context of coinfection with HIV-1. Here, we show that the IFN-I response signature in cmMTB-treated macrophages matches the one observed in the blood of active TB patients, and depends on the timing of incubation with cmMTB. This suggests that the timing of macrophage's exposure to IFN-I can impact their capacity to control HIV-1 infection. Strikingly, we found that cmMTB-treated macrophages are hyporesponsive to extrastimulation with exogenous IFN-I, used to mimic HIV-1 infection. Yet, depleting STAT1 by gene silencing to block the IFN-I signaling pathway reduced TB-induced exacerbation of HIV-1 infection. Altogether, by aiming to understand why TB-derived IFN-I preexposure of macrophages did not induce antiviral immunity against HIV-1, we demonstrated that these cells are hyporesponsive to exogenous IFN-I, a phenomenon that prevents macrophage activation against HIV-1. Mycobacterium tuberculosis induces hyporesponsiveness of the IFN-I signaling pathway in macrophages, leading to the exacerbation of HIV-1 replication.
Autres résumés
Type: Publisher
(spa)
Mycobacterium tuberculosis induces hyporesponsiveness of the IFN-I signaling pathway in macrophages, leading to the exacerbation of HIV-1 replication.
Identifiants
pubmed: 35588259
doi: 10.1002/JLB.4MA0422-730R
doi:
Substances chimiques
Interferon Type I
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1329-1342Informations de copyright
©2022 Society for Leukocyte Biology.
Références
Esmail H, et al. The immune response to mycobacterium tuberculosis in HIV-1-coinfected persons. Annu Rev Immunol. 2018;36:603-638. https://doi.org/10.1146/annurev-immunol-042617-053420
Scott L, da Silva P, Boehme CC, Stevens W, Gilpin CM. Diagnosis of opportunistic infections: hIV co-infections - tuberculosis. Curr Opin HIV AIDS. 2017;12:129-138. https://doi.org/10.1097/COH.0000000000000345
Sharma SK, Mohan A, Kadhiravan T. HIV-TB co-infection: epidemiology, diagnosis & management. Indian J Med Res. 2005;121:550-567.
Vittor AY, Garland JM, Schlossberg D. Improving the diagnosis of tuberculosis: from QuantiFERON to new techniques to diagnose tuberculosis infections. Curr HIV/AIDS Rep. 2011;8:153-163. https://doi.org/10.1007/s11904-011-0083-7
Lawn SD, Myer L, Edwards D, Bekker LG, Wood R. Short-term and long-term risk of tuberculosis associated with CD4 cell recovery during antiretroviral therapy in South Africa. AIDS. 2009;23:1717-1725. https://doi.org/10.1097/QAD.0b013e32832d3b6d
Imperiali FG, et al. Increased Mycobacterium tuberculosis growth in HIV-1-infected human macrophages: role of tumour necrosis factor-alpha. Clin Exp Immunol. 2001;123:435-442. https://doi.org/10.1046/j.1365-2249.2001.01481.x
Hoshino Y, et al. Maximal HIV-1 replication in alveolar macrophages during tuberculosis requires both lymphocyte contact and cytokines. J Exp Med. 2002;195:495-505. https://doi.org/10.1084/jem.20011614
Nakata K, et al. Mycobacterium tuberculosis enhances human immunodeficiency virus-1 replication in the lung. Am J Respir Crit Care Med. 1997;155:996-1003. https://doi.org/10.1164/ajrccm.155.3.9117038
Morris L, et al. High human immunodeficiency virus type 1 RNA load in the cerebrospinal fluid from patients with lymphocytic meningitis. J Infect Dis. 1998;177:473-476. https://doi.org/10.1086/517379
Lugo-Villarino G, Verollet C, Maridonneau-Parini I, Neyrolles O. Macrophage polarization: convergence point targeted by mycobacterium tuberculosis and HIV. Front Immunol. 2011;2:43. https://doi.org/10.3389/fimmu.2011.00043
O'Garra A, et al. The immune response in tuberculosis. Annu Rev Immunol. 2013;31:475-527. https://doi.org/10.1146/annurev-immunol-032712-095939
Rodrigues V, Ruffin N, San-Roman M, Benaroch P. Myeloid cell interaction with HIV: a complex relationship. Front Immunol. 2017;8:1698. https://doi.org/10.3389/fimmu.2017.01698
Ganor Y, et al. HIV-1 reservoirs in urethral macrophages of patients under suppressive antiretroviral therapy. Nat Microbiol. 2019;4:633-644. https://doi.org/10.1038/s41564-018-0335-z
Honeycutt JB, et al. Macrophages sustain HIV replication in vivo independently of T cells. J Clin Invest. 2016;126:1353-1366. https://doi.org/10.1172/JCI84456
Avalos CR, et al. Quantitation of productively infected monocytes and macrophages of simian immunodeficiency virus-infected macaques. J Virol. 2016;90:5643-5656. https://doi.org/10.1128/JVI.00290-16
Cribbs SK, Fontenot AP. The Impact of. Semin Respir Crit Care Med. 2016;37:157-165. https://doi.org/10.1055/s-0036-1572554
Cribbs SK, Lennox J, Caliendo AM, Brown LA, Guidot DM. Healthy HIV-1-infected individuals on highly active antiretroviral therapy harbor HIV-1 in their alveolar macrophages. AIDS Res Hum Retroviruses. 2015;31:64-70. https://doi.org/10.1089/AID.2014.0133
Goletti D, et al. Effect of Mycobacterium tuberculosis on HIV replication. Role of immune activation. J Immunol. 1996;157:1271-1278.
Lawn SD, et al. Anatomically compartmentalized human immunodeficiency virus replication in HLA-DR+ cells and CD14+ macrophages at the site of pleural tuberculosis coinfection. J Infect Dis. 2001;184:1127-1133. https://doi.org/10.1086/323649
Bell LCK, Noursadeghi M. Pathogenesis of HIV-1 and Mycobacterium tuberculosis co-infection. Nat Rev Microbiol. 2018;16:80-90. https://doi.org/10.1038/nrmicro.2017.128
Kuroda MJ, et al. High turnover of tissue macrophages contributes to tuberculosis reactivation in simian immunodeficiency virus-infected rhesus macaques. J Infect Dis. 2018;217:1865-1874. https://doi.org/10.1093/infdis/jix625
Lastrucci C, et al. Tuberculosis is associated with expansion of a motile, permissive and immunomodulatory CD16(+) monocyte population via the IL-10/STAT3 axis. Cell Res. 2015;25:1333-1351. https://doi.org/10.1038/cr.2015.123
Souriant S, et al. Tuberculosis exacerbates HIV-1 infection through IL-10/STAT3-dependent tunneling nanotube formation in macrophages. Cell Rep. 2019;26:3586-3599 e3587. https://doi.org/10.1016/j.celrep.2019.02.091
Dupont M, et al. Tuberculosis-associated IFN-I induces Siglec-1 on tunneling nanotubes and favors HIV-1 spread in macrophages. Elife. 2020;9. https://doi.org/10.7554/eLife.52535
Deeks SG, Odorizzi PM, Sekaly RP. The interferon paradox: can inhibiting an antiviral mechanism advance an HIV cure? J Clin Invest. 2017;127:103-105. https://doi.org/10.1172/JCI91916
Herbeuval JP, Shearer GM. HIV-1 immunopathogenesis: how good interferon turns bad. Clin Immunol. 2007;123:121-128. https://doi.org/10.1016/j.clim.2006.09.016
Divangahi M, King IL, Pernet E. Alveolar macrophages and type I IFN in airway homeostasis and immunity. Trends Immunol. 2015;36:307-314. https://doi.org/10.1016/j.it.2015.03.005
McNab F, Mayer-Barber K, Sher A, Wack A, O'Garra A. Type I interferons in infectious disease. Nat Rev Immunol. 2015;15:87-103. https://doi.org/10.1038/nri3787
Moreira-Teixeira L, Mayer-Barber K, Sher A, O'Garra A. Type I interferons in tuberculosis: foe and occasionally friend. J Exp Med. 2018;215:1273-1285. https://doi.org/10.1084/jem.20180325
Manca C, et al. Virulence of a Mycobacterium tuberculosis clinical isolate in mice is determined by failure to induce Th1 type immunity and is associated with induction of IFN-alpha /beta. Proc Natl Acad Sci USA. 2001;98:5752-5757. https://doi.org/10.1073/pnas.091096998
Manca C, et al. Hypervirulent M. tuberculosis W/Beijing strains upregulate type I IFNs and increase expression of negative regulators of the Jak-Stat pathway. J Interferon Cytokine Res. 2005;25:694-701. https://doi.org/10.1089/jir.2005.25.694
Berry MP, et al. An interferon-inducible neutrophil-driven blood transcriptional signature in human tuberculosis. Nature. 2010;466:973-977. https://doi.org/10.1038/nature09247
Lindenmann J, Burke DC, Isaacs A. Studies on the production, mode of action and properties of interferon. Br J Exp Pathol. 1957;38:551-562.
Lindenmann J, Gifford GE. Studies on vaccinia virus plaque formation and its inhibition by interferon. I. Dynamics of plaque formation by vaccinia virus. Virology. 1963;19:283-293. https://doi.org/10.1016/0042-6822(63)90066-7
Baca-Regen L, Heinzinger N, Stevenson M, Gendelman HE. Alpha interferon-induced antiretroviral activities: restriction of viral nucleic acid synthesis and progeny virion production in human immunodeficiency virus type 1-infected monocytes. J Virol. 1994;68:7559-7565. https://doi.org/10.1128/JVI.68.11.7559-7565.1994
Meylan PR, Guatelli JC, Munis JR, Richman DD, Kornbluth RS. Mechanisms for the inhibition of HIV replication by interferons-alpha, -beta, and -gamma in primary human macrophages. Virology. 1993;193:138-148. https://doi.org/10.1006/viro.1993.1110
Noel N, et al. Interferon-associated therapies toward HIV control: the back and forth. Cytokine Growth Factor Rev. 2018;40:99-112. https://doi.org/10.1016/j.cytogfr.2018.03.004
Sandler NG, et al. Type I interferon responses in rhesus macaques prevent SIV infection and slow disease progression. Nature. 2014;511:601-605. https://doi.org/10.1038/nature13554
Gordien E, et al. Inhibition of hepatitis B virus replication by the interferon-inducible MxA protein. J Virol. 2001;75:2684-2691. https://doi.org/10.1128/JVI.75.6.2684-2691.2001
Verhelst J, Hulpiau P, Saelens X. Mx proteins: antiviral gatekeepers that restrain the uninvited. Microbiol Mol Biol Rev. 2013;77:551-566. https://doi.org/10.1128/MMBR.00024-13
Goujon C, et al. Human MX2 is an interferon-induced post-entry inhibitor of HIV-1 infection. Nature. 2013;502:559-562. https://doi.org/10.1038/nature12542
Perng YC, Lenschow DJ. ISG15 in antiviral immunity and beyond. Nat Rev Microbiol. 2018;16:423-439. https://doi.org/10.1038/s41579-018-0020-5
Doyle T, Goujon C, Malim MH. HIV-1 and interferons: who's interfering with whom? Nat Rev Microbiol. 2015;13:403-413. https://doi.org/10.1038/nrmicro3449
Nganou-Makamdop K, Douek DC. Manipulating the Interferon Signaling Pathway: implications for HIV Infection. Virol Sin. 2019;34:192-196. https://doi.org/10.1007/s12250-019-00085-5
Tomasello E, Pollet E, Vu Manh TP, Uze G, Dalod M. Harnessing mechanistic knowledge on beneficial versus deleterious IFN-I effects to design innovative immunotherapies targeting cytokine activity to specific cell types. Front Immunol. 2014;5. https://doi.org/10.3389/fimmu.2014.00526
Zhen A, et al. Targeting type I interferon-mediated activation restores immune function in chronic HIV infection. J Clin Invest. 2017;127:260-268. https://doi.org/10.1172/JCI89488
Decalf J, et al. Sensing of HIV-1 entry triggers a type I interferon response in human primary macrophages. J Virol. 2017;91. https://doi.org/10.1128/JVI.00147-17
Abraham S, et al. Gene therapy with plasmids encoding IFN-beta or IFN-alpha14 confers long-term resistance to HIV-1 in humanized mice. Oncotarget. 2016;7:78412-78420. https://doi.org/10.18632/oncotarget.12512
Michaelis B, Levy JA. HIV replication can be blocked by recombinant human interferon beta. AIDS. 1989;3:27-31.
Taft J, Bogunovic D. The goldilocks zone of type I IFNs: lessons from human genetics. J Immunol. 2018;201:3479-3485. https://doi.org/10.4049/jimmunol.1800764
Snell LM, McGaha TL, Brooks DG. Type I interferon in chronic virus infection and cancer. Trends Immunol. 2017;38:542-557. https://doi.org/10.1016/j.it.2017.05.005
Jacob JT, Mehta AK, Leonard MK. Acute forms of tuberculosis in adults. Am J Med. 2009;122:12-17. https://doi.org/10.1016/j.amjmed.2008.09.018
Verollet C, et al. HIV-1 Nef triggers macrophage fusion in a p61Hck- and protease-dependent manner. J Immunol. 2010;184:7030-7039. https://doi.org/10.4049/jimmunol.0903345
Verollet C, et al. HIV-1 reprograms the migration of macrophages. Blood. 2015;125:1611-1622. https://doi.org/10.1182/blood-2014-08-596775
Murray PJ. Macrophage polarization. Annu Rev Physiol. 2017;79:541-566. https://doi.org/10.1146/annurev-physiol-022516-034339
Larner AC, Chaudhuri A, Darnell JE. Transcriptional induction by interferon. New protein(s) determine the extent and length of the induction. J Biol Chem. 1986;261:453-459.
Schneider WM, Chevillotte MD, Rice CM. Interferon-stimulated genes: a complex web of host defenses. Annu Rev Immunol. 2014;32:513-545. https://doi.org/10.1146/annurev-immunol-032713-120231
Arimoto KI, et al. STAT2 is an essential adaptor in USP18-mediated suppression of type I interferon signaling. Nat Struct Mol Biol. 2017;24:279-289. https://doi.org/10.1038/nsmb.3378
Dauphinee SM, et al. Contribution of increased ISG15, ISGylation and deregulated type I IFN signaling in Usp18 mutant mice during the course of bacterial infections. Genes Immun. 2014;15:282-292. https://doi.org/10.1038/gene.2014.17
Ritchie KJ, et al. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat Med. 2004;10:1374-1378. https://doi.org/10.1038/nm1133
Malakhova OA, et al. Protein ISGylation modulates the JAK-STAT signaling pathway. Genes Dev. 2003;17:455-460. https://doi.org/10.1101/gad.1056303
Lee MS, Kim B, Oh GT, Kim YJ. OASL1 inhibits translation of the type I interferon-regulating transcription factor IRF7. Nat Immunol. 2013;14:346-355. https://doi.org/10.1038/ni.2535
Zhu J, et al. Antiviral activity of human OASL protein is mediated by enhancing signaling of the RIG-I RNA sensor. Immunity. 2014;40:936-948. https://doi.org/10.1016/j.immuni.2014.05.007
Lugo-Villarino G, et al. The C-type lectin receptor DC-SIGN has an anti-inflammatory role in human M(IL-4) macrophages in response to Mycobacterium tuberculosis. Front Immunol. 2018;9:1123. https://doi.org/10.3389/fimmu.2018.01123
Troegeler A, et al. An efficient siRNA-mediated gene silencing in primary human monocytes, dendritic cells and macrophages. Immunology and cell biology. 2014;92:699-708. https://doi.org/10.1038/icb.2014.39