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

Kerri G. Lal; Dohoon Kim; Margaret C. Costanzo; Matthew Creegan; Edwin Leeansyah; Joana Dias; Dominic Paquin-Proulx; Leigh Anne Eller; Alexandra Schuetz; Yuwadee Phuang-ngern; Shelly J. Krebs; Bonnie M. Slike; Hannah Kibuuka; Lucas Maganga; Sorachai Nitayaphan; Josphat Kosgei; Carlo Sacdalan; Jintanat Ananworanich; Diane L. Bolton; Nelson L. Michael; Barbara L. Shacklett; Merlin L. Robb; Michael A. Eller; Johan K. Sandberg

doi:10.1038/s41467-019-13975-9

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

Kerri G. Lal, Dohoon Kim, Margaret C. Costanzo, Matthew Creegan, Edwin Leeansyah, Joana Dias, Dominic Paquin-Proulx, Leigh Anne Eller, Alexandra Schuetz, Yuwadee Phuang-ngern, Shelly J. Krebs, Bonnie M. Slike, Hannah Kibuuka, Lucas Maganga, Sorachai Nitayaphan, Josphat Kosgei, Carlo Sacdalan, Jintanat Ananworanich, Diane L. Bolton, Nelson L. MichaelBarbara L. Shacklett, Merlin L. Robb, Michael A. Eller, Johan K. Sandberg^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

41 Scopus citations

Abstract

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.

Original language	English
Article number	272
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-019-13975-9
State	Published - 1 Dec 2020
Externally published	Yes

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Lal, K. G., Kim, D., Costanzo, M. C., Creegan, M., Leeansyah, E., Dias, J., Paquin-Proulx, D., Eller, L. A., Schuetz, A., Phuang-ngern, Y., Krebs, S. J., Slike, B. M., Kibuuka, H., Maganga, L., Nitayaphan, S., Kosgei, J., Sacdalan, C., Ananworanich, J., Bolton, D. L., ... Sandberg, J. K. (2020). Dynamic MAIT cell response with progressively enhanced innateness during acute HIV-1 infection. Nature Communications, 11(1), Article 272. https://doi.org/10.1038/s41467-019-13975-9

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title = "Dynamic MAIT cell response with progressively enhanced innateness during acute HIV-1 infection",

abstract = "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.",

author = "Lal, {Kerri G.} and Dohoon Kim and Costanzo, {Margaret C.} and Matthew Creegan and Edwin Leeansyah and Joana Dias and Dominic Paquin-Proulx and Eller, {Leigh Anne} and Alexandra Schuetz and Yuwadee Phuang-ngern and Krebs, {Shelly J.} and Slike, {Bonnie M.} and Hannah Kibuuka and Lucas Maganga and Sorachai Nitayaphan and Josphat Kosgei and Carlo Sacdalan and Jintanat Ananworanich and Bolton, {Diane L.} and Michael, {Nelson L.} and Shacklett, {Barbara L.} and Robb, {Merlin L.} and Eller, {Michael A.} and Sandberg, {Johan K.}",

note = "Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

day = "1",

doi = "10.1038/s41467-019-13975-9",

language = "English",

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Lal, KG, Kim, D, Costanzo, MC, Creegan, M, Leeansyah, E, Dias, J, Paquin-Proulx, D, Eller, LA, Schuetz, A, Phuang-ngern, Y, Krebs, SJ, Slike, BM, Kibuuka, H, Maganga, L, Nitayaphan, S, Kosgei, J, Sacdalan, C, Ananworanich, J, Bolton, DL, Michael, NL, Shacklett, BL, Robb, ML, Eller, MA & Sandberg, JK 2020, 'Dynamic MAIT cell response with progressively enhanced innateness during acute HIV-1 infection', Nature Communications, vol. 11, no. 1, 272. https://doi.org/10.1038/s41467-019-13975-9

TY - JOUR

T1 - Dynamic MAIT cell response with progressively enhanced innateness during acute HIV-1 infection

AU - Lal, Kerri G.

AU - Kim, Dohoon

AU - Costanzo, Margaret C.

AU - Creegan, Matthew

AU - Leeansyah, Edwin

AU - Dias, Joana

AU - Paquin-Proulx, Dominic

AU - Eller, Leigh Anne

AU - Schuetz, Alexandra

AU - Phuang-ngern, Yuwadee

AU - Krebs, Shelly J.

AU - Slike, Bonnie M.

AU - Kibuuka, Hannah

AU - Maganga, Lucas

AU - Nitayaphan, Sorachai

AU - Kosgei, Josphat

AU - Sacdalan, Carlo

AU - Ananworanich, Jintanat

AU - Bolton, Diane L.

AU - Michael, Nelson L.

AU - Shacklett, Barbara L.

AU - Robb, Merlin L.

AU - Eller, Michael A.

AU - Sandberg, Johan K.

PY - 2020/12/1

Y1 - 2020/12/1

N2 - 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.

AB - 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.

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U2 - 10.1038/s41467-019-13975-9

DO - 10.1038/s41467-019-13975-9

M3 - Article

C2 - 31937782

AN - SCOPUS:85077844981

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 272

ER -

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

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