Inflammation-induced formation of fat-associated lymphoid clusters

Cécile Bénézech; Nguyet-Thin Luu; Jennifer A Walker; Andrei A Kruglov; Yunhua Loo; Kyoko Nakamura; Yang Zhang; Saba Nayar; Lucy H Jones; Adriana Flores-Langarica; Alistair McIntosh; Jennifer Marshall; Francesca Barone; Gurdyal Besra; Katherine Miles; Judith E Allen; Mohini Gray; George Kollias; Adam F Cunningham; David R Withers; Kai Michael Toellner; Nick D Jones; Marc Veldhoen; Sergei A Nedospasov; Andrew N J McKenzie; Jorge H Caamaño

doi:10.1038/ni.3215

Inflammation-induced formation of fat-associated lymphoid clusters

Cécile Bénézech, Nguyet-Thin Luu, Jennifer A Walker, Andrei A Kruglov, Yunhua Loo, Kyoko Nakamura, Yang Zhang, Saba Nayar, Lucy H Jones, Adriana Flores-Langarica, Alistair McIntosh, Jennifer Marshall, Francesca Barone, Gurdyal Besra, Katherine Miles, Judith E Allen, Mohini Gray, George Kollias, Adam F Cunningham, David R WithersKai Michael Toellner, Nick D Jones, Marc Veldhoen, Sergei A Nedospasov, Andrew N J McKenzie, Jorge H Caamaño

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Abstract

Fat-associated lymphoid clusters (FALCs) are a type of lymphoid tissue associated with visceral fat. Here we found that the distribution of FALCs was heterogeneous, with the pericardium containing large numbers of these clusters. FALCs contributed to the retention of B-1 cells in the peritoneal cavity through high expression of the chemokine CXCL13, and they supported B cell proliferation and germinal center differentiation during peritoneal immunological challenges. FALC formation was induced by inflammation, which triggered the recruitment of myeloid cells that expressed tumor-necrosis factor (TNF) necessary for signaling via the TNF receptors in stromal cells. Natural killer T cells (NKT cells) restricted by the antigen-presenting molecule CD1d were likewise required for the inducible formation of FALCs. Thus, FALCs supported and coordinated the activation of innate B cells and T cells during serosal immune responses.

Original language	English
Pages (from-to)	819-828
Number of pages	10
Journal	Nature Immunology
Volume	16
Issue number	8
Early online date	29 Jun 2015
DOIs	https://doi.org/10.1038/ni.3215
Publication status	Published - Aug 2015

Keywords

Lymphoid organs
Adipose Tissue
Inflammation
Immune response
iNKT cells
TNF
IL-13
Peritoneum

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BenezechC2015Inflammation
Final Version of Record available online at: http://dx.doi.10.1038/ni.3215 Eligibility for repository checked August 2015
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Utilising Invariant Natural Killer T Cell Activation to Promote the Survival of Cardiac Allografts
Jones, N.
British Heart Foundation
1/01/14 → 5/10/16
Project: Research
Lymphotoxin Beta Receptor Signalling Effects on Adipogenic Differentiation
Caamano, J., Hewett, P. & O'Neill, L.
Biotechnology & Biological Sciences Research Council
18/11/13 → 31/01/17
Project: Research Councils
Design, synthesis, and assessment of specific iNKT cell agonists for clinical applications
Besra, D., Cox, L., Cunningham, A. & Lammas, T.
Medical Research Council
1/03/12 → 29/02/16
Project: Research Councils
MRC Centre For Immune Regulation (Linked to DCDF.RRAK10540) (Linked to 14810 & 14835)
Jenkinson, E.
Medical Research Council
3/08/09 → 30/09/17
Project: Research Councils

Immunology 2017 Annual Mtg. of the American Association of Immunology
Jorge Caamano (Invited speaker)
13 May 2017
Activity: Academic and Industrial events › Conference, workshop or symposium

Cite this

Bénézech, C., Luu, N-T., Walker, J. A., Kruglov, A. A., Loo, Y., Nakamura, K., Zhang, Y., Nayar, S., Jones, L. H., Flores-Langarica, A., McIntosh, A., Marshall, J., Barone, F., Besra, G., Miles, K., Allen, J. E., Gray, M., Kollias, G., Cunningham, A. F., ... Caamaño, J. H. (2015). Inflammation-induced formation of fat-associated lymphoid clusters. Nature Immunology, 16(8), 819-828. Advance online publication. https://doi.org/10.1038/ni.3215

@article{a02107cf93044de99375c080c0246b21,

title = "Inflammation-induced formation of fat-associated lymphoid clusters",

abstract = "Fat-associated lymphoid clusters (FALCs) are a type of lymphoid tissue associated with visceral fat. Here we found that the distribution of FALCs was heterogeneous, with the pericardium containing large numbers of these clusters. FALCs contributed to the retention of B-1 cells in the peritoneal cavity through high expression of the chemokine CXCL13, and they supported B cell proliferation and germinal center differentiation during peritoneal immunological challenges. FALC formation was induced by inflammation, which triggered the recruitment of myeloid cells that expressed tumor-necrosis factor (TNF) necessary for signaling via the TNF receptors in stromal cells. Natural killer T cells (NKT cells) restricted by the antigen-presenting molecule CD1d were likewise required for the inducible formation of FALCs. Thus, FALCs supported and coordinated the activation of innate B cells and T cells during serosal immune responses.",

keywords = "Lymphoid organs, Adipose Tissue, Inflammation, Immune response, iNKT cells, TNF, IL-13, Peritoneum",

author = "C{\'e}cile B{\'e}n{\'e}zech and Nguyet-Thin Luu and Walker, {Jennifer A} and Kruglov, {Andrei A} and Yunhua Loo and Kyoko Nakamura and Yang Zhang and Saba Nayar and Jones, {Lucy H} and Adriana Flores-Langarica and Alistair McIntosh and Jennifer Marshall and Francesca Barone and Gurdyal Besra and Katherine Miles and Allen, {Judith E} and Mohini Gray and George Kollias and Cunningham, {Adam F} and Withers, {David R} and Toellner, {Kai Michael} and Jones, {Nick D} and Marc Veldhoen and Nedospasov, {Sergei A} and McKenzie, {Andrew N J} and Caama{\~n}o, {Jorge H}",

year = "2015",

month = aug,

doi = "10.1038/ni.3215",

language = "English",

volume = "16",

pages = "819--828",

journal = "Nature Immunology",

issn = "1529-2908",

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Bénézech, C, Luu, N-T, Walker, JA, Kruglov, AA, Loo, Y, Nakamura, K, Zhang, Y , Nayar, S, Jones, LH, Flores-Langarica, A, McIntosh, A, Marshall, J, Barone, F, Besra, G, Miles, K, Allen, JE, Gray, M, Kollias, G, Cunningham, AF , Withers, DR , Toellner, KM , Jones, ND, Veldhoen, M, Nedospasov, SA, McKenzie, ANJ & Caamaño, JH 2015, 'Inflammation-induced formation of fat-associated lymphoid clusters', Nature Immunology, vol. 16, no. 8, pp. 819-828. https://doi.org/10.1038/ni.3215

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AU - Bénézech, Cécile

AU - Luu, Nguyet-Thin

AU - Walker, Jennifer A

AU - Kruglov, Andrei A

AU - Loo, Yunhua

AU - Nakamura, Kyoko

AU - Zhang, Yang

AU - Nayar, Saba

AU - Jones, Lucy H

AU - Flores-Langarica, Adriana

AU - McIntosh, Alistair

AU - Marshall, Jennifer

AU - Barone, Francesca

AU - Besra, Gurdyal

AU - Miles, Katherine

AU - Allen, Judith E

AU - Gray, Mohini

AU - Kollias, George

AU - Cunningham, Adam F

AU - Withers, David R

AU - Toellner, Kai Michael

AU - Jones, Nick D

AU - Veldhoen, Marc

AU - Nedospasov, Sergei A

AU - McKenzie, Andrew N J

AU - Caamaño, Jorge H

PY - 2015/8

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N2 - Fat-associated lymphoid clusters (FALCs) are a type of lymphoid tissue associated with visceral fat. Here we found that the distribution of FALCs was heterogeneous, with the pericardium containing large numbers of these clusters. FALCs contributed to the retention of B-1 cells in the peritoneal cavity through high expression of the chemokine CXCL13, and they supported B cell proliferation and germinal center differentiation during peritoneal immunological challenges. FALC formation was induced by inflammation, which triggered the recruitment of myeloid cells that expressed tumor-necrosis factor (TNF) necessary for signaling via the TNF receptors in stromal cells. Natural killer T cells (NKT cells) restricted by the antigen-presenting molecule CD1d were likewise required for the inducible formation of FALCs. Thus, FALCs supported and coordinated the activation of innate B cells and T cells during serosal immune responses.

AB - Fat-associated lymphoid clusters (FALCs) are a type of lymphoid tissue associated with visceral fat. Here we found that the distribution of FALCs was heterogeneous, with the pericardium containing large numbers of these clusters. FALCs contributed to the retention of B-1 cells in the peritoneal cavity through high expression of the chemokine CXCL13, and they supported B cell proliferation and germinal center differentiation during peritoneal immunological challenges. FALC formation was induced by inflammation, which triggered the recruitment of myeloid cells that expressed tumor-necrosis factor (TNF) necessary for signaling via the TNF receptors in stromal cells. Natural killer T cells (NKT cells) restricted by the antigen-presenting molecule CD1d were likewise required for the inducible formation of FALCs. Thus, FALCs supported and coordinated the activation of innate B cells and T cells during serosal immune responses.

KW - Lymphoid organs

KW - Adipose Tissue

KW - Inflammation

KW - Immune response

KW - iNKT cells

KW - TNF

KW - IL-13

KW - Peritoneum

U2 - 10.1038/ni.3215

DO - 10.1038/ni.3215

M3 - Article

C2 - 26147686

SN - 1529-2908

VL - 16

SP - 819

EP - 828

JO - Nature Immunology

JF - Nature Immunology

IS - 8

ER -

Inflammation-induced formation of fat-associated lymphoid clusters

Abstract

Keywords

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Projects

Utilising Invariant Natural Killer T Cell Activation to Promote the Survival of Cardiac Allografts

Lymphotoxin Beta Receptor Signalling Effects on Adipogenic Differentiation

Design, synthesis, and assessment of specific iNKT cell agonists for clinical applications

MRC Centre For Immune Regulation (Linked to DCDF.RRAK10540) (Linked to 14810 & 14835)

Activities

Immunology 2017 Annual Mtg. of the American Association of Immunology

Cite this