P2X7 is expressed on human innate-like T lymphocytes and mediates susceptibility to ATP-induced cell death.


Journal

European journal of immunology
ISSN: 1521-4141
Titre abrégé: Eur J Immunol
Pays: Germany
ID NLM: 1273201

Informations de publication

Date de publication:
11 2022
Historique:
revised: 17 08 2022
received: 07 04 2022
accepted: 26 09 2022
pubmed: 1 10 2022
medline: 8 11 2022
entrez: 30 9 2022
Statut: ppublish

Résumé

Extracellular ATP activates the P2X7 receptor, leading to inflammasome activation and release of pro-inflammatory cytokines in monocytes. However, a detailed analysis of P2X7 receptor expression and function in the human T cell compartment has not been reported. Here, we used a P2X7-specific nanobody to assess cell membrane expression and function of P2X7 on peripheral T lymphocyte subsets. The results show that innate-like T cells, which effectively react to innate stimuli by secreting high amounts of pro-inflammatory cytokines, have the highest expression of P2X7 in the human T cell compartment. Using Tγδ cells as example for an innate-like lymphocyte population, we demonstrate that these cells are more sensitive to P2X7 receptor activation than conventional T cells, affecting fundamental cellular mechanisms like calcium signaling and ATP-induced cell death. The increased susceptibility of innate-like T cells to P2X7-mediated cell death provides a mechanism to control their homeostasis under inflammatory conditions. Understanding the expression and function of P2X7 on human immune cells is essential to assume the benefits and consequences of newly developed P2X7-based therapeutic approaches.

Identifiants

pubmed: 36178227
doi: 10.1002/eji.202249932
doi:

Substances chimiques

Receptors, Purinergic P2X7 0
Adenosine Triphosphate 8L70Q75FXE
Cytokines 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1805-1818

Informations de copyright

© 2022 The Authors. European Journal of Immunology published by Wiley-VCH GmbH.

Références

Di Virgilio, F., Dal Ben, D., Sarti, A.C., Giuliani, A.L., Falzoni, S., 2017. The P2X7 Receptor in Infection and Inflammation. Immunity 47, 15-31.
Labasi, J.M., Petrushova, N., Donovan, C., McCurdy, S., Lira, P., Payette, M. M., Brissette, W. et al., 2002. Absence of the P2X7 Receptor Alters Leukocyte Function and Attenuates an Inflammatory Response. J. Immunol. 168, 6436-6445.
Matute, C., Torre, I., Pérez-Cerdá, F., Pérez-Samartín, A., Alberdi, E., Etxebarria, E., Arranz, A.M. et al., 2007. P2X7 receptor blockade prevents ATP excitotoxicity in oligodendrocytes and ameliorates experimental autoimmune encephalomyelitis. J. Neurosci. 27, 9525-9533.
Vieira, F.S., Nanini, H.F., Takiya, C.M., Coutinho-Silva, R., 2016. P2X7 receptor knockout prevents streptozotocin-induced type 1 diabetes in mice. Mol. Cell. Endocrinol. 419, 148-157.
Illes, P., Müller, C.E., Jacobson, K.A., Grutter, T., Nicke, A., Fountain, S.J., Kennedy, C. et al., 2021. Update of P2X receptor properties and their pharmacology: IUPHAR Review 30. Br. J. Pharmacol. 178, 489-514.
Surprenant, A., Rassendren, F., Kawashima, E., North, R.A., Buell, G., 1996. The cytolytic P2Z receptor for extracellular ATP identified as a P2X receptor (P2X7). Science (80-.). 272, 735-738. https://doi.org/10.1126/science.272.5262.735
Xing, S., Grol, M.W., Grutter, P.H., Dixon, S.J., Komarova, S. V., 2016. Modeling interactions among individual P2 receptors to explain complex response patterns over a wide range of ATP concentrations. Front. Physiol. 7, 294.
Medina, C.B., Chiu, Y.H., Stremska, M.E., Lucas, C.D., Poon, I., Tung, K.S., Elliott, M.R. et al., 2021. Pannexin 1 channels facilitate communication between T cells to restrict the severity of airway inflammation. Immunity 54, 1715-1727.e7.
Schenk, U., Westendorf, A.M., Radaelli, E., Casati, A., Ferro, M., Fumagalli, M., Verderio, C. et al., 2008. Purinergic control of T cell activation by ATP released through pannexin-1 hemichannels. Sci. Signal. 1. https://doi.org/10.1126/scisignal.1160583
Rissiek, B., Haag, F., Boyer, O., Koch-Nolte, F., Adriouch, S., 2014. ADP-ribosylation of P2X7: A matter of life and death for regulatory T cells and natural killer T cells. Curr. Top. Microbiol. Immunol. 384, 107-126.
Seman, M., Adriouch, S., Scheuplein, F., Krebs, C., Freese, D., Glowacki, G., Deterre, P. et al., 2003. NAD-induced T cell death: ADP-ribosylation of cell surface proteins by ART2 activates the cytolytic P2X7 purinoceptor. Immunity 19, 571-582.
Gu, B.J., Zhang, W.Y., Bendall, L.J., Chessell, I.P., Buell, G.N., Wiley, J.S., 2000. Expression of P2X7 purinoceptors on human lymphocytes and monocytes: Evidence for nonfunctional P2X7 receptors. Am. J. Physiol. - Cell Physiol. 279. https://doi.org/10.1152/ajpcell.2000.279.4.c1189
Mutini, C., Falzoni, S., Ferrari, D., Chiozzi, P., Morelli, A., Baricordi, O.R., Collo, G. et al., 1999. Mouse dendritic cells express the P2X7 purinergic receptor: characterization and possible participation in antigen presentation. J. Immunol. 163, 1958-1965.
Uhlen, M., Karlsson, M.J., Zhong, W., Tebani, A., Pou, C., Mikes, J., Lakshmikanth, T. et al., 2019. A genome-wide transcriptomic analysis of protein-coding genes in human blood cells. Science (80-.). 366. https://doi.org/10.1126/science.aax9198
Beura, L.K., Fares-Frederickson, N.J., Steinert, E.M., Scott, M.C., Thompson, E.A., Fraser, K.A., Schenkel, J.M. et al., 2019. CD4+ resident memory T cells dominate immunosurveillance and orchestrate local recall responses. J. Exp. Med. 216, 1214-1229.
Borges da Silva, H., Peng, C., Wang, H., Wanhainen, K.M., Ma, C., Lopez, S., Khoruts, A. et al., 2020. Sensing of ATP via the Purinergic Receptor P2RX7 Promotes CD8+ Trm Cell Generation by Enhancing Their Sensitivity to the Cytokine TGF-β. Immunity 53, 158-171.e6.
Borges da Silva, H., Beura, L.K., Wang, H., Hanse, E.A., Gore, R., Scott, M.C., Walsh, D.A. et al., 2018. The purinergic receptor P2RX7 directs metabolic fitness of long-lived memory CD8+ T cells. Nature 559, 264-268.
Heiss, K., Jänner, N., Mähnß, B., Schumacher, V., Koch-Nolte, F., Haag, F., Mittrücker, H.-W., 2008. High Sensitivity of Intestinal CD8 + T Cells to Nucleotides Indicates P2X7 as a Regulator for Intestinal T Cell Responses. J. Immunol. 181, 3861-3869.
Heng, T.S.P., Painter, M.W., Elpek, K., Lukacs-Kornek, V., Mauermann, N., Turley, S.J., Koller, D. et al., 2008. The immunological genome project: Networks of gene expression in immune cells. Nat. Immunol. https://doi.org/10.1038/ni1008-1091
Hubert, S., Rissiek, B., Klages, K., Huehn, J., Sparwasser, T., Haag, F., Koch-Nolte, F. et al., 2010. Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2-P2X7 pathway. J. Exp. Med. 207, 2561-2568.
Proietti, M., Cornacchione, V., RezzonicoJost, T., Romagnani, A., Faliti, C.E., Perruzza, L., Rigoni, R. et al., 2014. ATP-gated ionotropic P2X7 receptor controls follicular T helper cell numbers in peyer's patches to promote host-microbiota mutualism. Immunity 41, 789-801.
Stark, R., Wesselink, T.H., Behr, F.M., Kragten, N.A.M., Arens, R., Koch-Nolte, F., van Gisbergen, K.P.J.M. et al., 2018. TRM maintenance is regulated by tissue damage via P2RX7. Sci. Immunol. 3. https://doi.org/10.1126/sciimmunol.aau1022
Danquah, W., Meyer-Schwesinger, C., Rissiek, B., Pinto, C., Serracant-Prat, A., Amadi, M., Iacenda, D. et al., 2016. Nanobodies that block gating of the P2X7 ion channel ameliorate inflammation. Sci. Transl. Med. 8. https://doi.org/10.1126/scitranslmed.aaf8463
Perregaux, D.G., McNiff, P., Laliberte, R., Conklyn, M., Gabel, C.A., 2000. ATP Acts as an Agonist to Promote Stimulus-Induced Secretion of IL-1β and IL-18 in Human Blood. J. Immunol. 165, 4615-4623.
Pizzirani, C., Ferrari, D., Chiozzi, P., Adinolfi, E., Sandonà, D., Savaglio, E., Di Virgilio, F., 2007. Stimulation of P2 receptors causes release of IL-1β-loaded microvesicles from human dendritic cells. Blood 109, 3856-3864.
Baricordi, O.R., Ferrari, D., Melchiorri, L., Chiozzi, P., Hanau, S., Chiari, E., Rubini, M. et al., 1996. An ATP-activated channel is involved in mitogenic stimulation of human T lymphocytes. Blood 87, 682-690.
Yip, L., Woehrle, T., Corriden, R., Hirsh, M., Chen, Y., Inoue, Y., Ferrari, V. et al., 2009. Autocrine regulation of T-cell activation by ATP release and P2X7 receptors. FASEB J. 23, 1685-1693.
Rivas-Yáñez, E., Barrera-Avalos, C., Parra-Tello, B., Briceño, P., Rosemblatt, Mariana V., Saavedra-Almarza, J., Rosemblatt, Mario et al., 2020. P2X7 Receptor at the Crossroads of T Cell Fate. Int. J. Mol. Sci. https://doi.org/10.3390/ijms21144937
Godfrey, D.I., Uldrich, A.P., Mccluskey, J., Rossjohn, J., Moody, D.B., 2015. The burgeoning family of unconventional T cells. Nat. Immunol. https://doi.org/10.1038/ni.3298
Gutierrez-Arcelus, M., Teslovich, N., Mola, A.R., Polidoro, R.B., Nathan, A., Kim, H., Hannes, S. et al., 2019. Lymphocyte innateness defined by transcriptional states reflects a balance between proliferation and effector functions. Nat. Commun. 10, 1-15.
Regev, A., Teichmann, S.A., Lander, E.S., Amit, I., Benoist, C., Birney, E., Bodenmiller, B. et al., 2017. The human cell atlas. Elife6. https://doi.org/10.7554/eLife.27041
Haag, F., Koch-Nolte, F., Kühl, M., Lorenzen, S., Thiele, H.G., 1994. Premature stop codons inactivate the RT6 genes of the human and chimpanzee species. J. Mol. Biol. 243, 537-546.
Reantragoon, R., Corbett, A.J., Sakala, I.G., Gherardin, N.A., Furness, J.B., Chen, Z., Eckle, S.B.G. et al., 2013. Antigen-loaded MR1 tetramers define T cell receptor heterogeneity in mucosal-associated invariant T cells. J. Exp. Med. 210, 2305-2320.
Manohar, M., Hirsh, M.I., Chen, Y., Woehrle, T., Karande, A.A., Junger, W.G., 2012. ATP release and autocrine signaling through P2X4 receptors regulate γδ T cell activation. J. Leukoc. Biol. 92, 787.
Gu, B., Bendall, L.J., Wiley, J.S., 1998. Adenosine triphosphate-induced shedding of CD23 and L-selectin (CD62L) from lymphocytes is mediated by the same receptor but different metalloproteases. Blood 92, 946-951.
Jamieson, G.P., Snook, M.B., Thurlow, P.J., Wiley, J.S., 1996. Extracellular ATP causes loss of L-selectin from human lymphocytes via occupancy of P2Z purinoceptors. J. Cell. Physiol. 166, 637-642.
Sengstake, S., Boneberg, E.-M., Illges, H., 2006. CD21 and CD62L shedding are both inducible via P2X7Rs. Int. Immunol. 18, 1171-1178.
Pelegrin, P., Surprenant, A., 2009. The P2X7 receptor - Pannexin connection to dye uptake and IL-1β release. Purinergic Signal. https://doi.org/10.1007/s11302-009-9141-7
Steinberg, T.H., Newman, A.S., Swanson, J.A., Silverstein, S.C., 1987. ATP4- permeabilizes the plasma membrane of mouse macrophages to fluorescent dyes. J. Biol. Chem. 262, 8884-8888.
Diercks, B.P., Werner, R., Weidemüller, P., Czarniak, F., Hernandez, L., Lehmann, C., Rosche, A. et al., 2018. ORAI1, STIM1/2, and RYR1 shape subsecond Ca2+ microdomains upon T cell activation, Science Signaling. https://doi.org/10.1126/scisignal.aat0358
Guse, A.H., Gil Montoya, D.C., Diercks, B.P., 2021. Mechanisms and functions of calcium microdomains produced by ORAI channels, D-myo-inositol 1,4,5-trisphosphate receptors, or ryanodine receptors. Pharmacol. Ther. https://doi.org/10.1016/j.pharmthera.2021.107804
Moulin, M., Alguacil, J., Gu, S., Mehtougui, A., Adams, E.J., Peyrottes, S., Champagne, E., 2017. Vγ9Vδ2 T cell activation by strongly agonistic nucleotidic phosphoantigens. Cell. Mol. Life Sci. 74, 4353-4367.
Kawamura, H., Aswad, F., Minagawa, M., Govindarajan, S., Dennert, G., 2006. P2X7 Receptors Regulate NKT Cells in Autoimmune Hepatitis. J. Immunol. 176, 2152-2160.
Fernandez-Ruiz, D., Ng, W.Y., Holz, L.E., Ma, J.Z., Zaid, A., Wong, Y.C., Lau, L.S. et al., 2016. Liver-Resident Memory CD8+ T Cells Form a Front-Line Defense against Malaria Liver-Stage Infection. Immunity 45, 889-902.
Buell, G., Chessell, I.P., Michel, A.D., Collo, G., Salazzo, M., Herren, S., Gretener, D. et al., 1998. Blockade of Human P2X7 Receptor Function With a Monoclonal Antibody. Blood 92, 3521-3528.
Adriouch, S., Bannas, P., Schwarz, N., Fliegert, R., Guse, A.H., Seman, M., Haag, F. et al., 2008. ADP-ribosylation at R125 gates the P2X7 ion channel by presenting a covalent ligand to its nucleotide binding site. FASEB J. 22, 861-869.
Schwarz, N., Drouot, L., Nicke, A., Fliegert, R., Boyer, O., Guse, A.H., Haag, F. et al., 2012. Alternative splicing of the N-terminal cytosolic and transmembrane domains of P2X7 controls gating of the ion channel by ADP-ribosylation. PLoS One 7, e41269.
Faliti, C.E., Gualtierotti, R., Rottoli, E., Gerosa, M., Perruzza, L., Romagnani, A., Pellegrini, G. et al., 2019. P2X7 receptor restrains pathogenic Tfh cell generation in systemic lupus erythematosus. J. Exp. Med. 216, 317.
Domae, E., Hirai, Y., Ikeo, T., Goda, S., Shimizu, Y., 2017. Cytokine-mediated activation of human ex vivo-expanded Vγ9Vδ2 T cells. Oncotarget 8, 45928-45942.
Slichter, C.K., McDavid, A., Miller, H.W., Finak, G., Seymour, B.J., McNevin, J.P., Diaz, G. et al., 2016. Distinct activation thresholds of human conventional and innate-like memory T cells. JCI Insight 1, 86292.
Beetz, S., Wesch, D., Marischen, L., Welte, S., Oberg, H.H., Kabelitz, D., 2008. Innate immune functions of human gammadelta T cells. Immunobiology 213, 173-182.
Liu, X., Zhang, Z., Ruan, J., Pan, Y., Magupalli, V.G., Wu, H., Lieberman, J., 2016. Inflammasome-activated gasdermin D causes pyroptosis by forming membrane pores. Nature 535, 153-158.
Rühl, S., Shkarina, K., Demarco, B., Heilig, R., Santos, J.C., Broz, P., 2018. ESCRT-dependent membrane repair negatively regulates pyroptosis downstream of GSDMD activation. Science (80-.). 362, 956-960.
Shi, J., Zhao, Y., Wang, K., Shi, X., Wang, Y., Huang, H., Zhuang, Y. et al., 2015. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature 526, 660-665.
Linder, A., Bauernfried, S., Cheng, Y., Albanese, M., Jung, C., Keppler, O.T., Hornung, V., 2020. CARD8 inflammasome activation triggers pyroptosis in human T cells. EMBO J. 39, e105071.
Zhang, C., Song, J.-W., Huang, H.-H., Fan, X., Huang, L., Deng, J.-N., Tu, B. et al., 2021. NLRP3 inflammasome induces CD4+ T cell loss in chronically HIV-1-infected patients. J. Clin. Invest. 131. https://doi.org/10.1172/JCI138861
Frascoli, M., Marcandalli, J., Schenk, U., Grassi, F., 2012. Purinergic P2X7 Receptor Drives T Cell Lineage Choice and Shapes Peripheral γδ Cells. J. Immunol. 189, 174-180.
Grassi, F., 2020. The P2X7 Receptor as Regulator of T Cell Development and Function. Front. Immunol. 11, 1179.
Schenk, U., Frascoli, M., Proietti, M., Geffers, R., Traggiai, E., Buer, J., Ricordi, C. et al., 2011. ATP inhibits the generation and function of regulatory T cells through the activation of purinergic P2X receptors. Sci. Signal. 4. https://doi.org/10.1126/scisignal.2001270
Zimmermann, H., Zebisch, M., Sträter, N., 2012. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal. 8, 437-502.
Rissiek, A., Baumann, I., Cuapio, A., Mautner, A., Kolster, M., Arck, P.C., Dodge-Khatami, A. et al., 2015. The expression of CD39 on regulatory T cells is genetically driven and further upregulated at sites of inflammation. J. Autoimmun. 58, 12-20.
Libera, J., Wittner, M., Kantowski, M., Woost, R., Eberhard, J.M., de Heer, J., Reher, D. et al., 2020. Decreased Frequency of Intestinal CD39+ γδ+ T Cells With Tissue-Resident Memory Phenotype in Inflammatory Bowel Disease. Front. Immunol. 11. https://doi.org/10.3389/fimmu.2020.567472
Atarashi, K., Nishimura, J., Shima, T., Umesaki, Y., Yamamoto, M., Onoue, M., Yagita, H. et al., 2008. ATP drives lamina propria TH17 cell differentiation. Nature 455, 808-812.
Proietti, M., Perruzza, L., Scribano, D., Pellegrini, G., D'Antuono, R., Strati, F., Raffaelli, M. et al., 2019. ATP released by intestinal bacteria limits the generation of protective IgA against enteropathogens. Nat. Commun. 10. https://doi.org/10.1038/s41467-018-08156-z
Scott, B.M., Gutiérrez-Vázquez, C., Sanmarco, L.M., da Silva Pereira, J.A., Li, Z., Plasencia, A., Hewson, P. et al., 2021. Self-tunable engineered yeast probiotics for the treatment of inflammatory bowel disease. Nat. Med. 27, 1212-1222.
Ferrari, D., Pizzirani, C., Adinolfi, E., Forchap, S., Sitta, B., Turchet, L., Falzoni, S. et al., 2004. The Antibiotic Polymyxin B Modulates P2X7 Receptor Function. J. Immunol. 173, 4652-4660.
Tomasinsig, L., Pizzirani, C., Skerlavaj, B., Pellegatti, P., Gulinelli, S., Tossi, A., Di Virgilio, F. et al., 2008. The human cathelicidin LL-37 modulates the activities of the P2X7 receptor in a structure-dependent manner. J. Biol. Chem. 283, 30471-30481.
Bidula, S., Dhuna, K., Helliwell, R., Stokes, L., 2019. Positive allosteric modulation of P2X7 promotes apoptotic cell death over lytic cell death responses in macrophages. Cell Death Dis. 10, 1-16.
Dreisig, K., Sund, L., Dommer, M.W., Kristensen, N.P., Boddum, K., Viste, R., Fredholm, S. et al., 2018. Human P2Y11 expression level affects human P2X7 receptor-mediated cell death. Front. Immunol. 9, 1. https://doi.org/10.3389/fimmu.2018.01159
Koch-Nolte, F., Reyelt, J., Schößow, B., Schwarz, N., Scheuplein, F., Rothenburg, S., Haag, F. et al., 2007. Single domain antibodies from llama effectively and specifically block T cell ecto-ADP-ribosyltransferase ART2.2 in vivo. FASEB J. 21, 3490-3498.

Auteurs

Riekje Winzer (R)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Arnau Serracant-Prat (A)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Valerie J Brock (VJ)

Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Carolina Pinto-Espinoza (C)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.
Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Björn Rissiek (B)

Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Miriam Amadi (M)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Niklas Eich (N)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Anne Rissiek (A)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Enja Schneider (E)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Tim Magnus (T)

Department of Neurology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Andreas H Guse (AH)

Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Björn-Philipp Diercks (BP)

Department of Biochemistry and Molecular Cell Biology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Friedrich Koch-Nolte (F)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

Eva Tolosa (E)

Department of Immunology, University Medical Center Hamburg-Eppendorf, Hamburg, Germany.

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