Cell shape sensing licenses dendritic cells for homeostatic migration to lymph nodes

Zahraa Alraies; Claudia A. Rivera; Maria Graciela Delgado; Doriane Sanséau; Mathieu Maurin; Roberto Amadio; Giulia Maria Piperno; Garett Dunsmore; Aline Yatim; Livia Lacerda Mariano; Anna Kniazeva; Vincent Calmettes; Pablo J. Sáez; Alice Williart; Henri Popard; Matthieu Gratia; Olivier Lamiable; Aurélie Moreau; Zoé Fusilier; Lou Crestey; Benoit Albaud; Patricia Legoix; Anne S. Dejean; Anne Louise Le Dorze; Hideki Nakano; Donald N. Cook; Toby Lawrence; Nicolas Manel; Federica Benvenuti; Florent Ginhoux; Hélène D. Moreau; Guilherme P. F. Nader; Matthieu Piel; Ana Maria Lennon-Duménil

doi:10.1038/s41590-024-01856-3

Cell shape sensing licenses dendritic cells for homeostatic migration to lymph nodes

Zahraa Alraies, Claudia A. Rivera, Maria Graciela Delgado, Doriane Sanséau, Mathieu Maurin, Roberto Amadio, Giulia Maria Piperno, Garett Dunsmore, Aline Yatim, Livia Lacerda Mariano, Anna Kniazeva, Vincent Calmettes, Pablo J. Sáez, Alice Williart, Henri Popard, Matthieu Gratia, Olivier Lamiable, Aurélie Moreau, Zoé Fusilier, Lou CresteyBenoit Albaud, Patricia Legoix, Anne S. Dejean, Anne Louise Le Dorze, Hideki Nakano, Donald N. Cook, Toby Lawrence, Nicolas Manel, Federica Benvenuti, Florent Ginhoux, Hélène D. Moreau, Guilherme P. F. Nader, Matthieu Piel, Ana Maria Lennon-Duménil

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

3 Citations (Scopus)

Abstract

Immune cells experience large cell shape changes during environmental patrolling because of the physical constraints that they encounter while migrating through tissues. These cells can adapt to such deformation events using dedicated shape-sensing pathways. However, how shape sensing affects immune cell function is mostly unknown. Here, we identify a shape-sensing mechanism that increases the expression of the chemokine receptor CCR7 and guides dendritic cell migration from peripheral tissues to lymph nodes at steady state. This mechanism relies on the lipid metabolism enzyme cPLA₂, requires nuclear envelope tensioning and is finely tuned by the ARP2/3 actin nucleation complex. We also show that this shape-sensing axis reprograms dendritic cell transcription by activating an IKKβ–NF-κB-dependent pathway known to control their tolerogenic potential. These results indicate that cell shape changes experienced by immune cells can define their migratory behavior and immunoregulatory properties and reveal a contribution of the physical properties of tissues to adaptive immunity.

Original language	English
Pages (from-to)	1193-1206
Number of pages	14
Journal	Nature Immunology
Volume	25
Issue number	7
DOIs	https://doi.org/10.1038/s41590-024-01856-3
Publication status	Published - 1 Jul 2024
Externally published	Yes

Access to Document

10.1038/s41590-024-01856-3

Cite this

Alraies, Z., Rivera, C. A., Delgado, M. G., Sanséau, D., Maurin, M., Amadio, R., Maria Piperno, G., Dunsmore, G., Yatim, A., Lacerda Mariano, L., Kniazeva, A., Calmettes, V., Sáez, P. J., Williart, A., Popard, H., Gratia, M., Lamiable, O., Moreau, A., Fusilier, Z., ... Lennon-Duménil, A. M. (2024). Cell shape sensing licenses dendritic cells for homeostatic migration to lymph nodes. Nature Immunology, 25(7), 1193-1206. https://doi.org/10.1038/s41590-024-01856-3

@article{169ebd9f341f4c728979d007abcf9b04,

title = "Cell shape sensing licenses dendritic cells for homeostatic migration to lymph nodes",

abstract = "Immune cells experience large cell shape changes during environmental patrolling because of the physical constraints that they encounter while migrating through tissues. These cells can adapt to such deformation events using dedicated shape-sensing pathways. However, how shape sensing affects immune cell function is mostly unknown. Here, we identify a shape-sensing mechanism that increases the expression of the chemokine receptor CCR7 and guides dendritic cell migration from peripheral tissues to lymph nodes at steady state. This mechanism relies on the lipid metabolism enzyme cPLA2, requires nuclear envelope tensioning and is finely tuned by the ARP2/3 actin nucleation complex. We also show that this shape-sensing axis reprograms dendritic cell transcription by activating an IKKβ–NF-κB-dependent pathway known to control their tolerogenic potential. These results indicate that cell shape changes experienced by immune cells can define their migratory behavior and immunoregulatory properties and reveal a contribution of the physical properties of tissues to adaptive immunity.",

author = "Zahraa Alraies and Rivera, {Claudia A.} and Delgado, {Maria Graciela} and Doriane Sans{\'e}au and Mathieu Maurin and Roberto Amadio and {Maria Piperno}, Giulia and Garett Dunsmore and Aline Yatim and {Lacerda Mariano}, Livia and Anna Kniazeva and Vincent Calmettes and S{\'a}ez, {Pablo J.} and Alice Williart and Henri Popard and Matthieu Gratia and Olivier Lamiable and Aur{\'e}lie Moreau and Zo{\'e} Fusilier and Lou Crestey and Benoit Albaud and Patricia Legoix and Dejean, {Anne S.} and {Le Dorze}, {Anne Louise} and Hideki Nakano and Cook, {Donald N.} and Toby Lawrence and Nicolas Manel and Federica Benvenuti and Florent Ginhoux and Moreau, {H{\'e}l{\`e}ne D.} and {P. F. Nader}, Guilherme and Matthieu Piel and Lennon-Dum{\'e}nil, {Ana Maria}",

note = "Publisher Copyright: {\textcopyright} The Author(s) 2024.",

year = "2024",

month = jul,

day = "1",

doi = "10.1038/s41590-024-01856-3",

language = "English",

volume = "25",

pages = "1193--1206",

journal = "Nature Immunology",

issn = "1529-2908",

number = "7",

}

Alraies, Z, Rivera, CA, Delgado, MG, Sanséau, D, Maurin, M, Amadio, R, Maria Piperno, G, Dunsmore, G, Yatim, A, Lacerda Mariano, L, Kniazeva, A, Calmettes, V, Sáez, PJ, Williart, A, Popard, H, Gratia, M, Lamiable, O, Moreau, A, Fusilier, Z, Crestey, L, Albaud, B, Legoix, P, Dejean, AS, Le Dorze, AL, Nakano, H, Cook, DN, Lawrence, T, Manel, N, Benvenuti, F, Ginhoux, F, Moreau, HD, P. F. Nader, G, Piel, M & Lennon-Duménil, AM 2024, 'Cell shape sensing licenses dendritic cells for homeostatic migration to lymph nodes', Nature Immunology, vol. 25, no. 7, pp. 1193-1206. https://doi.org/10.1038/s41590-024-01856-3

TY - JOUR

T1 - Cell shape sensing licenses dendritic cells for homeostatic migration to lymph nodes

AU - Alraies, Zahraa

AU - Rivera, Claudia A.

AU - Delgado, Maria Graciela

AU - Sanséau, Doriane

AU - Maurin, Mathieu

AU - Amadio, Roberto

AU - Maria Piperno, Giulia

AU - Dunsmore, Garett

AU - Yatim, Aline

AU - Lacerda Mariano, Livia

AU - Kniazeva, Anna

AU - Calmettes, Vincent

AU - Sáez, Pablo J.

AU - Williart, Alice

AU - Popard, Henri

AU - Gratia, Matthieu

AU - Lamiable, Olivier

AU - Moreau, Aurélie

AU - Fusilier, Zoé

AU - Crestey, Lou

AU - Albaud, Benoit

AU - Legoix, Patricia

AU - Dejean, Anne S.

AU - Le Dorze, Anne Louise

AU - Nakano, Hideki

AU - Cook, Donald N.

AU - Lawrence, Toby

AU - Manel, Nicolas

AU - Benvenuti, Federica

AU - Ginhoux, Florent

AU - Moreau, Hélène D.

AU - P. F. Nader, Guilherme

AU - Piel, Matthieu

AU - Lennon-Duménil, Ana Maria

PY - 2024/7/1

Y1 - 2024/7/1

N2 - Immune cells experience large cell shape changes during environmental patrolling because of the physical constraints that they encounter while migrating through tissues. These cells can adapt to such deformation events using dedicated shape-sensing pathways. However, how shape sensing affects immune cell function is mostly unknown. Here, we identify a shape-sensing mechanism that increases the expression of the chemokine receptor CCR7 and guides dendritic cell migration from peripheral tissues to lymph nodes at steady state. This mechanism relies on the lipid metabolism enzyme cPLA2, requires nuclear envelope tensioning and is finely tuned by the ARP2/3 actin nucleation complex. We also show that this shape-sensing axis reprograms dendritic cell transcription by activating an IKKβ–NF-κB-dependent pathway known to control their tolerogenic potential. These results indicate that cell shape changes experienced by immune cells can define their migratory behavior and immunoregulatory properties and reveal a contribution of the physical properties of tissues to adaptive immunity.

AB - Immune cells experience large cell shape changes during environmental patrolling because of the physical constraints that they encounter while migrating through tissues. These cells can adapt to such deformation events using dedicated shape-sensing pathways. However, how shape sensing affects immune cell function is mostly unknown. Here, we identify a shape-sensing mechanism that increases the expression of the chemokine receptor CCR7 and guides dendritic cell migration from peripheral tissues to lymph nodes at steady state. This mechanism relies on the lipid metabolism enzyme cPLA2, requires nuclear envelope tensioning and is finely tuned by the ARP2/3 actin nucleation complex. We also show that this shape-sensing axis reprograms dendritic cell transcription by activating an IKKβ–NF-κB-dependent pathway known to control their tolerogenic potential. These results indicate that cell shape changes experienced by immune cells can define their migratory behavior and immunoregulatory properties and reveal a contribution of the physical properties of tissues to adaptive immunity.

UR - http://www.scopus.com/inward/record.url?scp=85195167109&partnerID=8YFLogxK

U2 - 10.1038/s41590-024-01856-3

DO - 10.1038/s41590-024-01856-3

M3 - Article

AN - SCOPUS:85195167109

SN - 1529-2908

VL - 25

SP - 1193

EP - 1206

JO - Nature Immunology

JF - Nature Immunology

IS - 7

ER -

Cell shape sensing licenses dendritic cells for homeostatic migration to lymph nodes

Abstract

Access to Document

Other files and links

Cite this