Dynamic MAIT cell response with progressively enhanced innateness during acute HIV-1 infection.


Journal

Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555

Informations de publication

Date de publication:
14 01 2020
Historique:
received: 14 03 2019
accepted: 10 12 2019
entrez: 16 1 2020
pubmed: 16 1 2020
medline: 24 4 2020
Statut: epublish

Résumé

Mucosa-associated invariant T (MAIT) cell loss in chronic HIV-1 infection is a significant insult to antimicrobial immune defenses. Here we investigate the response of MAIT cells during acute HIV-1 infection utilizing the RV217 cohort with paired longitudinal pre- and post-infection samples. MAIT cells are activated and expand in blood and mucosa coincident with peak HIV-1 viremia, in a manner associated with emerging microbial translocation. This is followed by a phase with elevated function as viral replication is controlled to a set-point level, and later by their functional decline at the onset of chronic infection. Interestingly, enhanced innate-like pathways and characteristics develop progressively in MAIT cells during infection, in parallel with TCR repertoire alterations. These findings delineate the dynamic MAIT cell response to acute HIV-1 infection, and show how the MAIT compartment initially responds and expands with enhanced function, followed by progressive reprogramming away from TCR-dependent antibacterial responses towards innate-like functionality.

Identifiants

pubmed: 31937782
doi: 10.1038/s41467-019-13975-9
pii: 10.1038/s41467-019-13975-9
pmc: PMC6959336
doi:

Substances chimiques

Biomarkers 0
CD14 protein, human 0
Interferon Regulatory Factors 0
Lipopolysaccharide Receptors 0
Receptors, Antigen, T-Cell 0
interferon regulatory factor-4 0
C-Reactive Protein 9007-41-4

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

272

Subventions

Organisme : NIDDK NIH HHS
ID : R01 DK108350
Pays : United States
Organisme : U.S. Department of Defense (United States Department of Defense)
ID : W81XWH-07-2-0067
Pays : International

Références

Dusseaux, M. et al. Human MAIT cells are xenobiotic-resistant, tissue-targeted, CD161hi IL-17-secreting T cells. Blood 117, 1250–1259 (2011).
pubmed: 21084709 doi: 10.1182/blood-2010-08-303339
Martin, E. et al. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 7, e54 (2009).
pubmed: 19278296 doi: 10.1371/journal.pbio.1000054
Treiner, E. et al. Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1 (vol 422, pg 164, 2003). Nature 423, 1018–1018 (2003).
doi: 10.1038/nature01700
Tilloy, F. et al. An invariant T cell receptor alpha chain defines a novel TAP-independent major histocompatibility complex class Ib-restricted alpha/beta T cell subpopulation in mammals. J. Exp. Med. 189, 1907–1921 (1999).
pubmed: 10377186 pmcid: 2192962 doi: 10.1084/jem.189.12.1907
Walker, L. J. et al. Human MAIT and CD8alphaalpha cells develop from a pool of type-17 precommitted CD8+ T cells. Blood 119, 422–433 (2012).
pubmed: 22086415 pmcid: 3257008 doi: 10.1182/blood-2011-05-353789
Lepore, M. et al. Parallel T-cell cloning and deep sequencing of human MAIT cells reveal stable oligoclonal TCRbeta repertoire. Nat. Commun. 5, 3866 (2014).
pubmed: 24832684 doi: 10.1038/ncomms4866
Kjer-Nielsen, L. et al. MR1 presents microbial vitamin B metabolites to MAIT cells. Nature 491, 717–723 (2012).
pubmed: 23051753 doi: 10.1038/nature11605
Corbett, A. J. et al. T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature 509, 361–365 (2014).
pubmed: 24695216 doi: 10.1038/nature13160
Le Bourhis, L. et al. Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol. 11, 701–708 (2010).
pubmed: 20581831 doi: 10.1038/ni.1890
Le Bourhis, L. et al. MAIT cells detect and efficiently lyse bacterially-infected epithelial cells. PLoS Pathog. 9, e1003681 (2013).
pubmed: 24130485 pmcid: 3795036 doi: 10.1371/journal.ppat.1003681
Leeansyah, E. et al. Arming of MAIT cell cytolytic antimicrobial activity is induced by IL-7 and defective in HIV-1 infection. PLoS Pathog. 11, e1005072 (2015).
pubmed: 26295709 pmcid: 4546682 doi: 10.1371/journal.ppat.1005072
Kurioka, A. et al. MAIT cells are licensed through granzyme exchange to kill bacterially sensitized targets. Mucosal Immunol. 8, 429–440 (2015).
pubmed: 25269706 doi: 10.1038/mi.2014.81
Savage, A. K. et al. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29, 391–403 (2008).
pubmed: 18703361 pmcid: 2613001 doi: 10.1016/j.immuni.2008.07.011
Chua, W. J. et al. Polyclonal mucosa-associated invariant T cells have unique innate functions in bacterial infection. Infect. Immun. 80, 3256–3267 (2012).
pubmed: 22778103 pmcid: 3418730 doi: 10.1128/IAI.00279-12
Georgel, P., Radosavljevic, M., Macquin, C. & Bahram, S. The non-conventional MHC class I MR1 molecule controls infection by Klebsiella pneumoniae in mice. Mol. Immunol. 48, 769–775 (2011).
pubmed: 21190736 doi: 10.1016/j.molimm.2010.12.002
Gold, M. C. et al. Human mucosal associated invariant T cells detect bacterially infected cells. PLoS Biol. 8, e1000407 (2010).
pubmed: 20613858 pmcid: 2893946 doi: 10.1371/journal.pbio.1000407
Meierovics, A., Yankelevich, W. J. & Cowley, S. C. MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection. Proc Natl Acad Sci USA 110, E3119–E3128 (2013).
Wang, H. et al. MAIT cells protect against pulmonary Legionella longbeachae infection. Nat. Commun. 9, 3350 (2018).
pubmed: 30135490 pmcid: 6105587 doi: 10.1038/s41467-018-05202-8
Ussher, J. E. et al. TLR signaling in human antigen-presenting cells regulates MR1-dependent activation of MAIT cells. Eur. J. Immunol. 46, 1600–1614 (2016).
pubmed: 27105778 pmcid: 5297987 doi: 10.1002/eji.201545969
Slichter, C. K. et al. Distinct activation thresholds of human conventional and innate-like memory T cells. JCI insight 1 (2016).
Loh, L. et al. Human mucosal-associated invariant T cells contribute to antiviral influenza immunity via IL-18-dependent activation. Proc. Natl Acad. Sci. USA 113, 10133–10138 (2016).
pubmed: 27543331 pmcid: 5018778 doi: 10.1073/pnas.1610750113
Ussher, J. E. et al. CD161++ CD8+ T cells, including the MAIT cell subset, are specifically activated by IL-12+IL-18 in a TCR-independent manner. Eur. J. Immunol. 44, 195–203 (2014).
pubmed: 24019201 doi: 10.1002/eji.201343509
Dias, J., Leeansyah, E. & Sandberg, J. K. Multiple layers of heterogeneity and subset diversity in human MAIT cell responses to distinct microorganisms and to innate cytokines. Proc. Natl Acad. Sci. USA 114, E5434–E5443 (2017).
pubmed: 28630305 pmcid: 5502643 doi: 10.1073/pnas.1705759114
Leeansyah, E. et al. Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood 121, 1124–1135 (2013).
pubmed: 23243281 pmcid: 3575756 doi: 10.1182/blood-2012-07-445429
Cosgrove, C. et al. Early and nonreversible decrease of CD161++/MAIT cells in HIV infection. Blood 121, 951–961 (2013).
pubmed: 23255555 pmcid: 3567342 doi: 10.1182/blood-2012-06-436436
van Wilgenburg, B. et al. MAIT cells are activated during human viral infections. Nat. Commun. 7, 11653 (2016).
pubmed: 27337592 pmcid: 4931007 doi: 10.1038/ncomms11653
Spaan, M. et al. Frequencies of circulating MAIT cells are diminished in chronic HCV, HIV and HCV/HIV co-infection and do not recover during therapy. PLoS ONE 11, e0159243 (2016).
pubmed: 27416100 pmcid: 4945024 doi: 10.1371/journal.pone.0159243
Hengst, J. et al. Nonreversible MAIT cell-dysfunction in chronic hepatitis C virus infection despite successful interferon-free therapy. Eur. J. Immunol. 46, 2204–2210 (2016).
pubmed: 27296288 doi: 10.1002/eji.201646447
Wilgenburg, B. V. et al. MAIT cells contribute to protection against lethal influenza infection in vivo. Nat. Commun. 9, 4706 (2018).
pubmed: 30413689 pmcid: 6226485 doi: 10.1038/s41467-018-07207-9
Juno, J. A., Phetsouphanh, C., Klenerman, P. & Kent, S. J. Perturbation of mucosal-associated invariant T cells and iNKT cells in HIV infection. Curr. Opin. HIV AIDS (2018).
Sandberg, J. K., Dias, J., Shacklett, B. L. & Leeansyah, E. Will loss of your MAITs weaken your HAART? AIDS 27, 2501–2504 (2013).
pubmed: 23595154 doi: 10.1097/QAD.0b013e3283620726
Haase, A. T. Early events in sexual transmission of HIV and SIV and opportunities for interventions. Annu. Rev. Med. 62, 127–139 (2011).
pubmed: 21054171 doi: 10.1146/annurev-med-080709-124959
McMichael, A. J., Borrow, P., Tomaras, G. D., Goonetilleke, N. & Haynes, B. F. The immune response during acute HIV-1 infection: clues for vaccine development. Nat. Rev. Immunol. 10, 11–23 (2010).
pubmed: 20010788 doi: 10.1038/nri2674
Robb, M. L. et al. Prospective study of acute HIV-1 infection in adults in East Africa and Thailand. N. Engl. J. Med. 374, 2120–2130 (2016).
pubmed: 27192360 pmcid: 5111628 doi: 10.1056/NEJMoa1508952
Brenchley, J. M. & Douek, D. C. Microbial translocation across the GI tract. Annu. Rev. Immunol. 30, 149–173 (2012).
pubmed: 22224779 pmcid: 3513328 doi: 10.1146/annurev-immunol-020711-075001
Rouxel, O. et al. Cytotoxic and regulatory roles of mucosal-associated invariant T cells in type 1 diabetes. Nat. Immunol. 18, 1321–1331 (2017).
pubmed: 28991267 pmcid: 6025738 doi: 10.1038/ni.3854
Leeansyah, E., Loh, L., Nixon, D. F. & Sandberg, J. K. Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat. Commun. 5, 3143 (2014).
pubmed: 24452018 doi: 10.1038/ncomms4143
Gibbs, A. et al. MAIT cells reside in the female genital mucosa and are biased towards IL-17 and IL-22 production in response to bacterial stimulation. Mucosal Immunol. 10, 35–45 (2017).
pubmed: 27049062 doi: 10.1038/mi.2016.30
Ananworanich, J. et al. Impact of multi-targeted antiretroviral treatment on gut T cell depletion and HIV reservoir seeding during acute HIV infection. PLoS ONE 7, e33948 (2012).
pubmed: 22479485 pmcid: 3316511 doi: 10.1371/journal.pone.0033948
Eller, M. A. et al. Expansion of inefficient HIV-specific CD8 T cells during acute infection. J. Virol. 90, 4005–4016 (2016).
pubmed: 26842474 pmcid: 4810544 doi: 10.1128/JVI.02785-15
Demers, K. R. et al. Temporal dynamics of CD8+ T cell effector responses during primary HIV infection. PLoS Pathog. 12, e1005805 (2016).
pubmed: 27486665 pmcid: 4972399 doi: 10.1371/journal.ppat.1005805
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).
pubmed: 16199517 pmcid: 1239896 doi: 10.1073/pnas.0506580102
Mootha, V. K. et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat. Genet. 34, 267–273 (2003).
pubmed: 12808457 doi: 10.1038/ng1180
Howson, L. J. et al. MAIT cell clonal expansion and TCR repertoire shaping in human volunteers challenged with Salmonella Paratyphi A. Nat. Commun. 9, 253 (2018).
pubmed: 29343684 pmcid: 5772558 doi: 10.1038/s41467-017-02540-x
Dias, J., Sobkowiak, M. J., Sandberg, J. K. & Leeansyah, E. Human MAIT-cell responses to Escherichia coli: activation, cytokine production, proliferation, and cytotoxicity. J. Leukoc. Biol. 100, 233–240 (2016).
pubmed: 27034405 pmcid: 4946616 doi: 10.1189/jlb.4TA0815-391RR
Stacey, A. R. et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J. Virol. 83, 3719–3733 (2009).
pubmed: 19176632 pmcid: 2663284 doi: 10.1128/JVI.01844-08
Godfrey, D. I., Uldrich, A. P., McCluskey, J., Rossjohn, J. & Moody, D. B. The burgeoning family of unconventional T cells. Nat. Immunol. 16, 1114–1123 (2015).
pubmed: 26482978 doi: 10.1038/ni.3298
Kloverpris, H. N. et al. Innate lymphoid cells are depleted irreversibly during acute HIV-1 infection in the absence of viral suppression. Immunity 44, 391–405 (2016).
pubmed: 26850658 pmcid: 6836297 doi: 10.1016/j.immuni.2016.01.006
Man, K. et al. Transcription Factor IRF4 promotes CD8(+) T cell exhaustion and limits the development of memory-like T cells during chronic infection. Immunity 47, 1129–1141 e1125 (2017).
pubmed: 29246443 doi: 10.1016/j.immuni.2017.11.021
Gutierrez-Arcelus, M. et al. Lymphocyte innateness defined by transcriptional states reflects a balance between proliferation and effector functions. Nat. Commun. 10, 687 (2019).
pubmed: 30737409 pmcid: 6368609 doi: 10.1038/s41467-019-08604-4
Dias, J. et al. The CD4(-)CD8(-) MAIT cell subpopulation is a functionally distinct subset developmentally related to the main CD8(+) MAIT cell pool. Proc. Natl Acad. Sci. USA 115, E11513–E11522 (2018).
pubmed: 30442667 pmcid: 6298106 doi: 10.1073/pnas.1716689115
Juno, J. A. et al. MAIT cells upregulate alpha4beta7 in Response to Acute Simian Immunodeficiency Virus/Simian HIV Infection but Are Resistant to Peripheral Depletion in Pigtail Macaques. J. Immunol. 202, 2105–2120 (2019).
pubmed: 30777923 doi: 10.4049/jimmunol.1801405
Vinton, C. et al. Mucosa-associated invariant T cells are systemically depleted in Simian immunodeficiency virus-infected Rhesus Macaques. J. Virol. 90, 4520–4529 (2016).
pubmed: 26912615 pmcid: 4836342 doi: 10.1128/JVI.02876-15
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886 doi: 10.1093/bioinformatics/bts635
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinforma. 12, 323 (2011).
doi: 10.1186/1471-2105-12-323
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677 doi: 10.1093/bioinformatics/btt656
Risso, D., Ngai, J., Speed, T. P. & Dudoit, S. Normalization of RNA-seq data using factor analysis of control genes or samples. Nat. Biotechnol. 32, 896–902 (2014).
pubmed: 25150836 pmcid: 4404308 doi: 10.1038/nbt.2931
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
pubmed: 19910308 doi: 10.1093/bioinformatics/btp616
Lal, K. G., Leeansyah, E., Sandberg, J. K. & Eller, M. A. OMIP-046: characterization of invariant T cell subset activation in humans. Cytom. Part A 93, 499–503 (2018).
doi: 10.1002/cyto.a.23357

Auteurs

Kerri G Lal (KG)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.
Center for Infectious Medicine, Department of Medicine, Karolinska Institutet, Stockholm, Sweden.

Dohoon Kim (D)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Margaret C Costanzo (MC)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Matthew Creegan (M)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Edwin Leeansyah (E)

Center for Infectious Medicine, Department of Medicine, Karolinska Institutet, Stockholm, Sweden.
Program in Emerging Infectious Diseases, Duke-National University of Singapore Medical School, Singapore, Singapore.

Joana Dias (J)

Center for Infectious Medicine, Department of Medicine, Karolinska Institutet, Stockholm, Sweden.

Dominic Paquin-Proulx (D)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Leigh Anne Eller (LA)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Alexandra Schuetz (A)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.
Department of Retrovirology, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand.

Yuwadee Phuang-Ngern (Y)

Department of Retrovirology, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand.

Shelly J Krebs (SJ)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Bonnie M Slike (BM)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Hannah Kibuuka (H)

Makerere University Walter Reed Project, Kampala, Uganda.

Lucas Maganga (L)

National Institute for Medical Research-Mbeya Medical Research Center, Mbeya, Tanzania.

Sorachai Nitayaphan (S)

Royal Thai Army Component, Armed Forces Research Institute of Medical Sciences, Bangkok, Thailand.

Josphat Kosgei (J)

Kenya Medical Research Institute/U.S. Army Medical Research Directorate-Africa/Kenya, Kericho, Kenya.

Carlo Sacdalan (C)

SEARCH, The Thai Red Cross AIDS Research Centre, Bangkok, Thailand.

Jintanat Ananworanich (J)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.
SEARCH, The Thai Red Cross AIDS Research Centre, Bangkok, Thailand.

Diane L Bolton (DL)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Nelson L Michael (NL)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.

Barbara L Shacklett (BL)

Department of Medical Microbiology and Immunology, School of Medicine, University of California Davis, Davis, CA, USA.

Merlin L Robb (ML)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Michael A Eller (MA)

U.S. Military HIV Research Program, Walter Reed Army Institute of Research, Silver Spring, MD, USA.
Henry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, USA.

Johan K Sandberg (JK)

Center for Infectious Medicine, Department of Medicine, Karolinska Institutet, Stockholm, Sweden. johan.sandberg@ki.se.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH