Chronic Inflammation Permanently Reshapes Tissue-Resident Immunity in Celiac Disease

Toufic Mayassi; Kristin Ladell; Herman Gudjonson; James E. McLaren; Dustin G. Shaw; Mai T. Tran; Jagoda J. Rokicka; Ian Lawrence; Jean-Christophe Grenier; Vincent van Unen; Cezary Ciszewski; Matthew Dimaano; Hoda E. Sayegh; Vinod Kumar; Cisca Wijmenga; Peter H. R. Green; Ranjana Gokhale; Hilary Jericho; Carol E. Semrad; Stefano Guandalini; Aaron R. Dinner; Sonia S. Kupfer; Hugh H. Reid; Luis B. Barreiro; Jamie Rossjohn; David A. Price; Bana Jabri

doi:10.1016/j.cell.2018.12.039

Chronic Inflammation Permanently Reshapes Tissue-Resident Immunity in Celiac Disease

Toufic Mayassi, Kristin Ladell, Herman Gudjonson, James E. McLaren, Dustin G. Shaw, Mai T. Tran, Jagoda J. Rokicka, Ian Lawrence, Jean-Christophe Grenier, Vincent van Unen, Cezary Ciszewski, Matthew Dimaano, Hoda E. Sayegh, Vinod Kumar, Cisca Wijmenga, Peter H. R. Green, Ranjana Gokhale, Hilary Jericho, Carol E. Semrad, Stefano GuandaliniAaron R. Dinner, Sonia S. Kupfer, Hugh H. Reid, Luis B. Barreiro, Jamie Rossjohn, David A. Price, Bana Jabri

Groningen Institute for Gastro Intestinal Genetics and Immunology (3GI)

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

130 Citations (Scopus)

151 Downloads (Pure)

Abstract

Tissue-resident lymphocytes play a key role in immune surveillance, but it remains unclear how these inherently stable cell populations respond to chronic inflammation. In the setting of celiac disease (CeD), where exposure to dietary antigen can be controlled, gluten-induced inflammation triggered a profound depletion of naturally occurring V gamma 4(+)/V delta 1(+) intraepithelial lymphocytes (IELs) with innate cytolytic properties and specificity for the butyrophilin-like (BTNL) molecules BTNL3/BTNL8. Creation of a new niche with reduced expression of BTNL8 and loss of V gamma 4(+)/V delta 1(+) IELs was accompanied by the expansion of gluten-sensitive, interferon-gamma-producing V delta 1(+) IELs bearing T cell receptors (TCRs) with a shared non-germline-encoded motif that failed to recognize BTNL3/BTNL8. Exclusion of dietary gluten restored BTNL8 expression but was insufficient to reconstitute the physiological V gamma 4(+)/V delta 1(+) subset among TCR gamma delta(+) IELs. Collectively, these data show that chronic inflammation permanently reconfigures the tissue-resident TCR gamma delta(+) IEL compartment in CeD.

Original language	English
Pages (from-to)	967-981,e19
Number of pages	35
Journal	Cell
Volume	176
Issue number	5
DOIs	https://doi.org/10.1016/j.cell.2018.12.039
Publication status	Published - 7-Feb-2019

Keywords

T-CELL-RECEPTOR
MEMORY
LYMPHOCYTES
POPULATIONS
REGRESSION
MOLECULES
RESPONSES
CD4(+)
IMPACT
T(H)1

Access to Document

10.1016/j.cell.2018.12.039

Chronic Inflammation Permanently Reshapes Tissue-Resident ImmunityFinal publisher's version, 13.7 MBLicence: Taverne

Handle.net

Persistent link

Cite this

Mayassi, T., Ladell, K., Gudjonson, H., McLaren, J. E., Shaw, D. G., Tran, M. T., Rokicka, J. J., Lawrence, I., Grenier, J.-C., van Unen, V., Ciszewski, C., Dimaano, M., Sayegh, H. E., Kumar, V., Wijmenga, C., Green, P. H. R., Gokhale, R., Jericho, H., Semrad, C. E., ... Jabri, B. (2019). Chronic Inflammation Permanently Reshapes Tissue-Resident Immunity in Celiac Disease. Cell, 176(5), 967-981,e19. https://doi.org/10.1016/j.cell.2018.12.039

@article{61d8eaf6a28d44bfb85eb2a2245e01f2,

title = "Chronic Inflammation Permanently Reshapes Tissue-Resident Immunity in Celiac Disease",

abstract = "Tissue-resident lymphocytes play a key role in immune surveillance, but it remains unclear how these inherently stable cell populations respond to chronic inflammation. In the setting of celiac disease (CeD), where exposure to dietary antigen can be controlled, gluten-induced inflammation triggered a profound depletion of naturally occurring V gamma 4(+)/V delta 1(+) intraepithelial lymphocytes (IELs) with innate cytolytic properties and specificity for the butyrophilin-like (BTNL) molecules BTNL3/BTNL8. Creation of a new niche with reduced expression of BTNL8 and loss of V gamma 4(+)/V delta 1(+) IELs was accompanied by the expansion of gluten-sensitive, interferon-gamma-producing V delta 1(+) IELs bearing T cell receptors (TCRs) with a shared non-germline-encoded motif that failed to recognize BTNL3/BTNL8. Exclusion of dietary gluten restored BTNL8 expression but was insufficient to reconstitute the physiological V gamma 4(+)/V delta 1(+) subset among TCR gamma delta(+) IELs. Collectively, these data show that chronic inflammation permanently reconfigures the tissue-resident TCR gamma delta(+) IEL compartment in CeD.",

keywords = "T-CELL-RECEPTOR, MEMORY, LYMPHOCYTES, POPULATIONS, REGRESSION, MOLECULES, RESPONSES, CD4(+), IMPACT, T(H)1",

author = "Toufic Mayassi and Kristin Ladell and Herman Gudjonson and McLaren, {James E.} and Shaw, {Dustin G.} and Tran, {Mai T.} and Rokicka, {Jagoda J.} and Ian Lawrence and Jean-Christophe Grenier and {van Unen}, Vincent and Cezary Ciszewski and Matthew Dimaano and Sayegh, {Hoda E.} and Vinod Kumar and Cisca Wijmenga and Green, {Peter H. R.} and Ranjana Gokhale and Hilary Jericho and Semrad, {Carol E.} and Stefano Guandalini and Dinner, {Aaron R.} and Kupfer, {Sonia S.} and Reid, {Hugh H.} and Barreiro, {Luis B.} and Jamie Rossjohn and Price, {David A.} and Bana Jabri",

year = "2019",

month = feb,

day = "7",

doi = "10.1016/j.cell.2018.12.039",

language = "English",

volume = "176",

pages = "967--981,e19",

journal = "Cell",

issn = "0092-8674",

publisher = "Cell Press",

number = "5",

}

Mayassi, T, Ladell, K, Gudjonson, H, McLaren, JE, Shaw, DG, Tran, MT, Rokicka, JJ, Lawrence, I, Grenier, J-C, van Unen, V, Ciszewski, C, Dimaano, M, Sayegh, HE, Kumar, V , Wijmenga, C, Green, PHR, Gokhale, R, Jericho, H, Semrad, CE, Guandalini, S, Dinner, AR, Kupfer, SS, Reid, HH, Barreiro, LB, Rossjohn, J, Price, DA & Jabri, B 2019, 'Chronic Inflammation Permanently Reshapes Tissue-Resident Immunity in Celiac Disease', Cell, vol. 176, no. 5, pp. 967-981,e19. https://doi.org/10.1016/j.cell.2018.12.039

TY - JOUR

T1 - Chronic Inflammation Permanently Reshapes Tissue-Resident Immunity in Celiac Disease

AU - Mayassi, Toufic

AU - Ladell, Kristin

AU - Gudjonson, Herman

AU - McLaren, James E.

AU - Shaw, Dustin G.

AU - Tran, Mai T.

AU - Rokicka, Jagoda J.

AU - Lawrence, Ian

AU - Grenier, Jean-Christophe

AU - van Unen, Vincent

AU - Ciszewski, Cezary

AU - Dimaano, Matthew

AU - Sayegh, Hoda E.

AU - Kumar, Vinod

AU - Wijmenga, Cisca

AU - Green, Peter H. R.

AU - Gokhale, Ranjana

AU - Jericho, Hilary

AU - Semrad, Carol E.

AU - Guandalini, Stefano

AU - Dinner, Aaron R.

AU - Kupfer, Sonia S.

AU - Reid, Hugh H.

AU - Barreiro, Luis B.

AU - Rossjohn, Jamie

AU - Price, David A.

AU - Jabri, Bana

PY - 2019/2/7

Y1 - 2019/2/7

N2 - Tissue-resident lymphocytes play a key role in immune surveillance, but it remains unclear how these inherently stable cell populations respond to chronic inflammation. In the setting of celiac disease (CeD), where exposure to dietary antigen can be controlled, gluten-induced inflammation triggered a profound depletion of naturally occurring V gamma 4(+)/V delta 1(+) intraepithelial lymphocytes (IELs) with innate cytolytic properties and specificity for the butyrophilin-like (BTNL) molecules BTNL3/BTNL8. Creation of a new niche with reduced expression of BTNL8 and loss of V gamma 4(+)/V delta 1(+) IELs was accompanied by the expansion of gluten-sensitive, interferon-gamma-producing V delta 1(+) IELs bearing T cell receptors (TCRs) with a shared non-germline-encoded motif that failed to recognize BTNL3/BTNL8. Exclusion of dietary gluten restored BTNL8 expression but was insufficient to reconstitute the physiological V gamma 4(+)/V delta 1(+) subset among TCR gamma delta(+) IELs. Collectively, these data show that chronic inflammation permanently reconfigures the tissue-resident TCR gamma delta(+) IEL compartment in CeD.

AB - Tissue-resident lymphocytes play a key role in immune surveillance, but it remains unclear how these inherently stable cell populations respond to chronic inflammation. In the setting of celiac disease (CeD), where exposure to dietary antigen can be controlled, gluten-induced inflammation triggered a profound depletion of naturally occurring V gamma 4(+)/V delta 1(+) intraepithelial lymphocytes (IELs) with innate cytolytic properties and specificity for the butyrophilin-like (BTNL) molecules BTNL3/BTNL8. Creation of a new niche with reduced expression of BTNL8 and loss of V gamma 4(+)/V delta 1(+) IELs was accompanied by the expansion of gluten-sensitive, interferon-gamma-producing V delta 1(+) IELs bearing T cell receptors (TCRs) with a shared non-germline-encoded motif that failed to recognize BTNL3/BTNL8. Exclusion of dietary gluten restored BTNL8 expression but was insufficient to reconstitute the physiological V gamma 4(+)/V delta 1(+) subset among TCR gamma delta(+) IELs. Collectively, these data show that chronic inflammation permanently reconfigures the tissue-resident TCR gamma delta(+) IEL compartment in CeD.

KW - T-CELL-RECEPTOR

KW - MEMORY

KW - LYMPHOCYTES

KW - POPULATIONS

KW - REGRESSION

KW - MOLECULES

KW - RESPONSES

KW - CD4(+)

KW - IMPACT

KW - T(H)1

U2 - 10.1016/j.cell.2018.12.039

DO - 10.1016/j.cell.2018.12.039

M3 - Article

C2 - 30739797

SN - 0092-8674

VL - 176

SP - 967-981,e19

JO - Cell

JF - Cell

IS - 5

ER -

Chronic Inflammation Permanently Reshapes Tissue-Resident Immunity in Celiac Disease

Abstract

Keywords

Access to Document

Handle.net

Fingerprint

Cite this