P2X7 receptor restrains pathogenic Tfh cell generation in systemic lupus erythematosus

Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively limit pathogenic responses without affecting the protective function of Tfh cells are unknown. Here we show that the ATP-gated ionotropic P2X...

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Published inThe Journal of experimental medicine Vol. 216; no. 2; pp. 317 - 336
Main Authors Faliti, Caterina E., Gualtierotti, Roberta, Rottoli, Elsa, Gerosa, Maria, Perruzza, Lisa, Romagnani, Andrea, Pellegrini, Giovanni, De Ponte Conti, Benedetta, Rossi, Riccardo L., Idzko, Marco, Mazza, Emilia M.C., Bicciato, Silvio, Traggiai, Elisabetta, Meroni, Pier Luigi, Grassi, Fabio
Format Journal Article
LanguageEnglish
Published United States Rockefeller University Press 04.02.2019
Subjects
Animals
Autoantibodies - genetics
Autoantibodies - immunology
Disease Models, Animal
Interferon-gamma - genetics
Interferon-gamma - immunology
Lupus Erythematosus, Systemic - genetics
Lupus Erythematosus, Systemic - immunology
Lupus Erythematosus, Systemic - pathology
Mice
Mice, Knockout
Pyroptosis - genetics
Pyroptosis - immunology
Receptors, Purinergic P2X7 - genetics
Receptors, Purinergic P2X7 - immunology
T-Lymphocytes, Helper-Inducer - immunology
T-Lymphocytes, Helper-Inducer - pathology
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Abstract Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively limit pathogenic responses without affecting the protective function of Tfh cells are unknown. Here we show that the ATP-gated ionotropic P2X7 receptor restricts the expansion of aberrant Tfh cells and the generation of self-reactive antibodies in experimental murine lupus, but its activity is dispensable for the expansion of antigen-specific Tfh cells during vaccination. P2X7 stimulation promotes caspase-mediated pyroptosis of Tfh cells and controls the development of pathogenic ICOS+ IFN-γ–secreting cells. Circulating Tfh cells from patients with systemic lupus erythematosus (SLE) but not primary antiphospholipid syndrome (PAPS), a nonlupus systemic autoimmune disease, were hyporesponsive to P2X7 stimulation and resistant to P2X7-mediated inhibition of cytokine-driven expansion. These data point to the P2X7 receptor as a checkpoint regulator of Tfh cells; thus, restoring P2X7 activity in SLE patients could selectively limit the progressive amplification of pathogenic autoantibodies, which deteriorate patients’ conditions.
AbstractList Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively limit pathogenic responses without affecting the protective function of Tfh cells are unknown. Here we show that the ATP-gated ionotropic P2X7 receptor restricts the expansion of aberrant Tfh cells and the generation of self-reactive antibodies in experimental murine lupus, but its activity is dispensable for the expansion of antigen-specific Tfh cells during vaccination. P2X7 stimulation promotes caspase-mediated pyroptosis of Tfh cells and controls the development of pathogenic ICOS+ IFN-γ-secreting cells. Circulating Tfh cells from patients with systemic lupus erythematosus (SLE) but not primary antiphospholipid syndrome (PAPS), a nonlupus systemic autoimmune disease, were hyporesponsive to P2X7 stimulation and resistant to P2X7-mediated inhibition of cytokine-driven expansion. These data point to the P2X7 receptor as a checkpoint regulator of Tfh cells; thus, restoring P2X7 activity in SLE patients could selectively limit the progressive amplification of pathogenic autoantibodies, which deteriorate patients' conditions.Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively limit pathogenic responses without affecting the protective function of Tfh cells are unknown. Here we show that the ATP-gated ionotropic P2X7 receptor restricts the expansion of aberrant Tfh cells and the generation of self-reactive antibodies in experimental murine lupus, but its activity is dispensable for the expansion of antigen-specific Tfh cells during vaccination. P2X7 stimulation promotes caspase-mediated pyroptosis of Tfh cells and controls the development of pathogenic ICOS+ IFN-γ-secreting cells. Circulating Tfh cells from patients with systemic lupus erythematosus (SLE) but not primary antiphospholipid syndrome (PAPS), a nonlupus systemic autoimmune disease, were hyporesponsive to P2X7 stimulation and resistant to P2X7-mediated inhibition of cytokine-driven expansion. These data point to the P2X7 receptor as a checkpoint regulator of Tfh cells; thus, restoring P2X7 activity in SLE patients could selectively limit the progressive amplification of pathogenic autoantibodies, which deteriorate patients' conditions.
Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively limit pathogenic responses without affecting the protective function of Tfh cells are unknown. Here we show that the ATP-gated ionotropic P2X7 receptor restricts the expansion of aberrant Tfh cells and the generation of self-reactive antibodies in experimental murine lupus, but its activity is dispensable for the expansion of antigen-specific Tfh cells during vaccination. P2X7 stimulation promotes caspase-mediated pyroptosis of Tfh cells and controls the development of pathogenic ICOS IFN-γ-secreting cells. Circulating Tfh cells from patients with systemic lupus erythematosus (SLE) but not primary antiphospholipid syndrome (PAPS), a nonlupus systemic autoimmune disease, were hyporesponsive to P2X7 stimulation and resistant to P2X7-mediated inhibition of cytokine-driven expansion. These data point to the P2X7 receptor as a checkpoint regulator of Tfh cells; thus, restoring P2X7 activity in SLE patients could selectively limit the progressive amplification of pathogenic autoantibodies, which deteriorate patients' conditions.
T follicular helper cells promote the generation of protective antibodies, but can also foster pathogenic antibodies. The ATP-gated P2X7 receptor selectively limits the expansion of Tfh cells that amplify self-reactive antibodies in systemic lupus erythematosus. Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively limit pathogenic responses without affecting the protective function of Tfh cells are unknown. Here we show that the ATP-gated ionotropic P2X7 receptor restricts the expansion of aberrant Tfh cells and the generation of self-reactive antibodies in experimental murine lupus, but its activity is dispensable for the expansion of antigen-specific Tfh cells during vaccination. P2X7 stimulation promotes caspase-mediated pyroptosis of Tfh cells and controls the development of pathogenic ICOS + IFN-γ–secreting cells. Circulating Tfh cells from patients with systemic lupus erythematosus (SLE) but not primary antiphospholipid syndrome (PAPS), a nonlupus systemic autoimmune disease, were hyporesponsive to P2X7 stimulation and resistant to P2X7-mediated inhibition of cytokine-driven expansion. These data point to the P2X7 receptor as a checkpoint regulator of Tfh cells; thus, restoring P2X7 activity in SLE patients could selectively limit the progressive amplification of pathogenic autoantibodies, which deteriorate patients’ conditions.
Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively limit pathogenic responses without affecting the protective function of Tfh cells are unknown. Here we show that the ATP-gated ionotropic P2X7 receptor restricts the expansion of aberrant Tfh cells and the generation of self-reactive antibodies in experimental murine lupus, but its activity is dispensable for the expansion of antigen-specific Tfh cells during vaccination. P2X7 stimulation promotes caspase-mediated pyroptosis of Tfh cells and controls the development of pathogenic ICOS+ IFN-γ–secreting cells. Circulating Tfh cells from patients with systemic lupus erythematosus (SLE) but not primary antiphospholipid syndrome (PAPS), a nonlupus systemic autoimmune disease, were hyporesponsive to P2X7 stimulation and resistant to P2X7-mediated inhibition of cytokine-driven expansion. These data point to the P2X7 receptor as a checkpoint regulator of Tfh cells; thus, restoring P2X7 activity in SLE patients could selectively limit the progressive amplification of pathogenic autoantibodies, which deteriorate patients’ conditions.
Author Rossi, Riccardo L.
Grassi, Fabio
Faliti, Caterina E.
Rottoli, Elsa
Idzko, Marco
Gualtierotti, Roberta
Mazza, Emilia M.C.
Meroni, Pier Luigi
De Ponte Conti, Benedetta
Perruzza, Lisa
Traggiai, Elisabetta
Bicciato, Silvio
Pellegrini, Giovanni
Romagnani, Andrea
Gerosa, Maria
AuthorAffiliation 6 Laboratory for Animal Model Pathology, Institute of Veterinary Pathology, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland
1 Institute for Research in Biomedicine, Università della Svizzera Italiana, Bellinzona, Switzerland
9 Department of Life Sciences, University of Modena and Reggio Emilia, Modena, Italy
11 Istituto Auxologico Italiano, Milan, Italy
5 Department of Medical Biotechnology and Translational Medicine, University of Milan, Milan, Italy
7 Istituto Nazionale Genetica Molecolare “Romeo ed Enrica Invernizzi,” Milan, Italy
10 Novartis Institute for Biomedical Research, Basel, Switzerland
2 Graduate School for Cellular and Biomedical Sciences, University of Bern, Bern, Switzerland
3 Department of Clinical Science and Community Health, University of Milan, Milan, Italy
4 Lupus Clinic, IASST-Istituto Gaetano Pini, Milan, Italy
8 Division of Pulmonology, Department of Medicine II, Medical University of Vienna, Vienna, Austria
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  start-page: 789
  year: 2014
  ident: 2023072604412787600_bib46
  article-title: ATP-gated ionotropic P2X7 receptor controls follicular T helper cell numbers in Peyer’s patches to promote host-microbiota mutualism
  publication-title: Immunity.
  doi: 10.1016/j.immuni.2014.10.010
– reference: 30728450 - Nat Rev Rheumatol. 2019 Mar;15(3):125
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Snippet Altered control of T follicular helper (Tfh) cells can lead to generation of autoantibodies and autoimmune manifestations. Signaling pathways that selectively...
T follicular helper cells promote the generation of protective antibodies, but can also foster pathogenic antibodies. The ATP-gated P2X7 receptor selectively...
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StartPage 317
SubjectTerms Animals
Autoantibodies - genetics
Autoantibodies - immunology
Disease Models, Animal
Interferon-gamma - genetics
Interferon-gamma - immunology
Lupus Erythematosus, Systemic - genetics
Lupus Erythematosus, Systemic - immunology
Lupus Erythematosus, Systemic - pathology
Mice
Mice, Knockout
Pyroptosis - genetics
Pyroptosis - immunology
Receptors, Purinergic P2X7 - genetics
Receptors, Purinergic P2X7 - immunology
T-Lymphocytes, Helper-Inducer - immunology
T-Lymphocytes, Helper-Inducer - pathology
Title P2X7 receptor restrains pathogenic Tfh cell generation in systemic lupus erythematosus
URI https://www.ncbi.nlm.nih.gov/pubmed/30655308
https://www.proquest.com/docview/2179396821
https://pubmed.ncbi.nlm.nih.gov/PMC6363434
Volume 216
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