An atlas of cells in the human tonsil

Ramon Massoni-Badosa; Sergio Aguilar-Fernández; Juan C. Nieto; Paula Soler-Vila; Marc Elosua-Bayes; Domenica Marchese; Marta Kulis; Amaia Vilas-Zornoza; Marco Matteo Bühler; Sonal Rashmi; Clara Alsinet; Ginevra Caratù; Catia Moutinho; Sara Ruiz; Patricia Lorden; Giulia Lunazzi; Dolors Colomer; Gerard Frigola; Will Blevins; Lucia Romero-Rivero; Víctor Jiménez-Martínez; Anna Vidal; Judith Mateos-Jaimez; Alba Maiques-Diaz; Sara Ovejero; Jérôme Moreaux; Sara Palomino; David Gomez-Cabrero; Xabier Agirre; Marc A. Weniger; Hamish W. King; Lucy C. Garner; Federico Marini; Francisco Javier Cervera-Paz; Peter M. Baptista; Isabel Vilaseca; Cecilia Rosales; Silvia Ruiz-Gaspà; Benjamin Talks; Keval Sidhpura; Anna Pascual-Reguant; Anja E. Hauser; Muzlifah Haniffa; Felipe Prosper; Ralf Küppers; Ivo Glynne Gut; Elias Campo; José Ignacio Martin-Subero; Holger Heyn

doi:10.1016/j.immuni.2024.01.006

An atlas of cells in the human tonsil

Ramon Massoni-Badosa^*, Sergio Aguilar-Fernández, Juan C. Nieto, Paula Soler-Vila, Marc Elosua-Bayes, Domenica Marchese, Marta Kulis, Amaia Vilas-Zornoza, Marco Matteo Bühler, Sonal Rashmi, Clara Alsinet, Ginevra Caratù, Catia Moutinho, Sara Ruiz, Patricia Lorden, Giulia Lunazzi, Dolors Colomer, Gerard Frigola, Will Blevins, Lucia Romero-RiveroVíctor Jiménez-Martínez, Anna Vidal, Judith Mateos-Jaimez, Alba Maiques-Diaz, Sara Ovejero, Jérôme Moreaux, Sara Palomino, David Gomez-Cabrero, Xabier Agirre, Marc A. Weniger, Hamish W. King, Lucy C. Garner, Federico Marini, Francisco Javier Cervera-Paz, Peter M. Baptista, Isabel Vilaseca, Cecilia Rosales, Silvia Ruiz-Gaspà, Benjamin Talks, Keval Sidhpura, Anna Pascual-Reguant, Anja E. Hauser, Muzlifah Haniffa, Felipe Prosper, Ralf Küppers, Ivo Glynne Gut, Elias Campo, José Ignacio Martin-Subero^*, Holger Heyn^*

^*Corresponding author for this work

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

18 Scopus citations

Abstract

Palatine tonsils are secondary lymphoid organs (SLOs) representing the first line of immunological defense against inhaled or ingested pathogens. We generated an atlas of the human tonsil composed of >556,000 cells profiled across five different data modalities, including single-cell transcriptome, epigenome, proteome, and immune repertoire sequencing, as well as spatial transcriptomics. This census identified 121 cell types and states, defined developmental trajectories, and enabled an understanding of the functional units of the tonsil. Exemplarily, we stratified myeloid slan-like subtypes, established a BCL6 enhancer as locally active in follicle-associated T and B cells, and identified SIX5 as putative transcriptional regulator of plasma cell maturation. Analyses of a validation cohort confirmed the presence, annotation, and markers of tonsillar cell types and provided evidence of age-related compositional shifts. We demonstrate the value of this resource by annotating cells from B cell-derived mantle cell lymphomas, linking transcriptional heterogeneity to normal B cell differentiation states of the human tonsil.

Original language	English (US)
Pages (from-to)	379-399.e18
Journal	Immunity
Volume	57
Issue number	2
DOIs	https://doi.org/10.1016/j.immuni.2024.01.006
State	Published - Feb 13 2024

Bibliographical note

Publisher Copyright:
© 2024 The Authors

Keywords

adaptive immunity
aging
Human Cell Atlas
human tonsil
innate immunity
mantle cell lymphoma
secondary lymphoid organs
single-cell genomics
spatial transcriptomics

ASJC Scopus subject areas

Immunology and Allergy
Immunology
Infectious Diseases

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

Access to Document

10.1016/j.immuni.2024.01.006

Cite this

Massoni-Badosa, R., Aguilar-Fernández, S., Nieto, J. C., Soler-Vila, P., Elosua-Bayes, M., Marchese, D., Kulis, M., Vilas-Zornoza, A., Bühler, M. M., Rashmi, S., Alsinet, C., Caratù, G., Moutinho, C., Ruiz, S., Lorden, P., Lunazzi, G., Colomer, D., Frigola, G., Blevins, W., ... Heyn, H. (2024). An atlas of cells in the human tonsil. Immunity, 57(2), 379-399.e18. https://doi.org/10.1016/j.immuni.2024.01.006

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title = "An atlas of cells in the human tonsil",

abstract = "Palatine tonsils are secondary lymphoid organs (SLOs) representing the first line of immunological defense against inhaled or ingested pathogens. We generated an atlas of the human tonsil composed of >556,000 cells profiled across five different data modalities, including single-cell transcriptome, epigenome, proteome, and immune repertoire sequencing, as well as spatial transcriptomics. This census identified 121 cell types and states, defined developmental trajectories, and enabled an understanding of the functional units of the tonsil. Exemplarily, we stratified myeloid slan-like subtypes, established a BCL6 enhancer as locally active in follicle-associated T and B cells, and identified SIX5 as putative transcriptional regulator of plasma cell maturation. Analyses of a validation cohort confirmed the presence, annotation, and markers of tonsillar cell types and provided evidence of age-related compositional shifts. We demonstrate the value of this resource by annotating cells from B cell-derived mantle cell lymphomas, linking transcriptional heterogeneity to normal B cell differentiation states of the human tonsil.",

keywords = "adaptive immunity, aging, Human Cell Atlas, human tonsil, innate immunity, mantle cell lymphoma, secondary lymphoid organs, single-cell genomics, spatial transcriptomics",

author = "Ramon Massoni-Badosa and Sergio Aguilar-Fern{\'a}ndez and Nieto, {Juan C.} and Paula Soler-Vila and Marc Elosua-Bayes and Domenica Marchese and Marta Kulis and Amaia Vilas-Zornoza and B{\"u}hler, {Marco Matteo} and Sonal Rashmi and Clara Alsinet and Ginevra Carat{\`u} and Catia Moutinho and Sara Ruiz and Patricia Lorden and Giulia Lunazzi and Dolors Colomer and Gerard Frigola and Will Blevins and Lucia Romero-Rivero and V{\'i}ctor Jim{\'e}nez-Mart{\'i}nez and Anna Vidal and Judith Mateos-Jaimez and Alba Maiques-Diaz and Sara Ovejero and J{\'e}r{\^o}me Moreaux and Sara Palomino and David Gomez-Cabrero and Xabier Agirre and Weniger, {Marc A.} and King, {Hamish W.} and Garner, {Lucy C.} and Federico Marini and Cervera-Paz, {Francisco Javier} and Baptista, {Peter M.} and Isabel Vilaseca and Cecilia Rosales and Silvia Ruiz-Gasp{\`a} and Benjamin Talks and Keval Sidhpura and Anna Pascual-Reguant and Hauser, {Anja E.} and Muzlifah Haniffa and Felipe Prosper and Ralf K{\"u}ppers and Gut, {Ivo Glynne} and Elias Campo and Martin-Subero, {Jos{\'e} Ignacio} and Holger Heyn",

note = "Publisher Copyright: {\textcopyright} 2024 The Authors",

year = "2024",

month = feb,

day = "13",

doi = "10.1016/j.immuni.2024.01.006",

language = "English (US)",

volume = "57",

pages = "379--399.e18",

journal = "Immunity",

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Massoni-Badosa, R, Aguilar-Fernández, S, Nieto, JC, Soler-Vila, P, Elosua-Bayes, M, Marchese, D, Kulis, M, Vilas-Zornoza, A, Bühler, MM, Rashmi, S, Alsinet, C, Caratù, G, Moutinho, C, Ruiz, S, Lorden, P, Lunazzi, G, Colomer, D, Frigola, G, Blevins, W, Romero-Rivero, L, Jiménez-Martínez, V, Vidal, A, Mateos-Jaimez, J, Maiques-Diaz, A, Ovejero, S, Moreaux, J, Palomino, S, Gomez-Cabrero, D, Agirre, X, Weniger, MA, King, HW, Garner, LC, Marini, F, Cervera-Paz, FJ, Baptista, PM, Vilaseca, I, Rosales, C, Ruiz-Gaspà, S, Talks, B, Sidhpura, K, Pascual-Reguant, A, Hauser, AE, Haniffa, M, Prosper, F, Küppers, R, Gut, IG, Campo, E, Martin-Subero, JI & Heyn, H 2024, 'An atlas of cells in the human tonsil', Immunity, vol. 57, no. 2, pp. 379-399.e18. https://doi.org/10.1016/j.immuni.2024.01.006

TY - JOUR

T1 - An atlas of cells in the human tonsil

AU - Massoni-Badosa, Ramon

AU - Aguilar-Fernández, Sergio

AU - Nieto, Juan C.

AU - Soler-Vila, Paula

AU - Elosua-Bayes, Marc

AU - Marchese, Domenica

AU - Kulis, Marta

AU - Vilas-Zornoza, Amaia

AU - Bühler, Marco Matteo

AU - Rashmi, Sonal

AU - Alsinet, Clara

AU - Caratù, Ginevra

AU - Moutinho, Catia

AU - Ruiz, Sara

AU - Lorden, Patricia

AU - Lunazzi, Giulia

AU - Colomer, Dolors

AU - Frigola, Gerard

AU - Blevins, Will

AU - Romero-Rivero, Lucia

AU - Jiménez-Martínez, Víctor

AU - Vidal, Anna

AU - Mateos-Jaimez, Judith

AU - Maiques-Diaz, Alba

AU - Ovejero, Sara

AU - Moreaux, Jérôme

AU - Palomino, Sara

AU - Gomez-Cabrero, David

AU - Agirre, Xabier

AU - Weniger, Marc A.

AU - King, Hamish W.

AU - Garner, Lucy C.

AU - Marini, Federico

AU - Cervera-Paz, Francisco Javier

AU - Baptista, Peter M.

AU - Vilaseca, Isabel

AU - Rosales, Cecilia

AU - Ruiz-Gaspà, Silvia

AU - Talks, Benjamin

AU - Sidhpura, Keval

AU - Pascual-Reguant, Anna

AU - Hauser, Anja E.

AU - Haniffa, Muzlifah

AU - Prosper, Felipe

AU - Küppers, Ralf

AU - Gut, Ivo Glynne

AU - Campo, Elias

AU - Martin-Subero, José Ignacio

AU - Heyn, Holger

PY - 2024/2/13

Y1 - 2024/2/13

N2 - Palatine tonsils are secondary lymphoid organs (SLOs) representing the first line of immunological defense against inhaled or ingested pathogens. We generated an atlas of the human tonsil composed of >556,000 cells profiled across five different data modalities, including single-cell transcriptome, epigenome, proteome, and immune repertoire sequencing, as well as spatial transcriptomics. This census identified 121 cell types and states, defined developmental trajectories, and enabled an understanding of the functional units of the tonsil. Exemplarily, we stratified myeloid slan-like subtypes, established a BCL6 enhancer as locally active in follicle-associated T and B cells, and identified SIX5 as putative transcriptional regulator of plasma cell maturation. Analyses of a validation cohort confirmed the presence, annotation, and markers of tonsillar cell types and provided evidence of age-related compositional shifts. We demonstrate the value of this resource by annotating cells from B cell-derived mantle cell lymphomas, linking transcriptional heterogeneity to normal B cell differentiation states of the human tonsil.

AB - Palatine tonsils are secondary lymphoid organs (SLOs) representing the first line of immunological defense against inhaled or ingested pathogens. We generated an atlas of the human tonsil composed of >556,000 cells profiled across five different data modalities, including single-cell transcriptome, epigenome, proteome, and immune repertoire sequencing, as well as spatial transcriptomics. This census identified 121 cell types and states, defined developmental trajectories, and enabled an understanding of the functional units of the tonsil. Exemplarily, we stratified myeloid slan-like subtypes, established a BCL6 enhancer as locally active in follicle-associated T and B cells, and identified SIX5 as putative transcriptional regulator of plasma cell maturation. Analyses of a validation cohort confirmed the presence, annotation, and markers of tonsillar cell types and provided evidence of age-related compositional shifts. We demonstrate the value of this resource by annotating cells from B cell-derived mantle cell lymphomas, linking transcriptional heterogeneity to normal B cell differentiation states of the human tonsil.

KW - adaptive immunity

KW - aging

KW - Human Cell Atlas

KW - human tonsil

KW - innate immunity

KW - mantle cell lymphoma

KW - secondary lymphoid organs

KW - single-cell genomics

KW - spatial transcriptomics

UR - http://www.scopus.com/inward/record.url?scp=85184741238&partnerID=8YFLogxK

U2 - 10.1016/j.immuni.2024.01.006

DO - 10.1016/j.immuni.2024.01.006

M3 - Article

C2 - 38301653

AN - SCOPUS:85184741238

SN - 1074-7613

VL - 57

SP - 379-399.e18

JO - Immunity

JF - Immunity

IS - 2

ER -

An atlas of cells in the human tonsil

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

UN SDGs

Access to Document

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Cite this