The P2X7 Receptor-Interleukin-1 Liaison

Giuliani, Anna Lisa; Sarti, Alba C.; Falzoni, Simonetta; Di Virgilio, Francesco

doi:10.3389/fphar.2017.00123

Cited by 166Adenosine and Purinergic SignalingInflammasome and immune disordersImmune Response and Inflammation

The P2X7 Receptor-Interleukin-1 Liaison

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Giuliani, Anna Lisa, Sarti, Alba C., Falzoni, Simonetta, Di Virgilio, Francesco·2017·Frontiers in Pharmacology

DOI 10.3389/fphar.2017.00123PMC PMC5353276

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Abstract

Interleukin-1β (IL-1β) plays a central role in stimulation of innate immune system and inflammation and in several chronic inflammatory diseases. These include rare hereditary conditions, e.g., auto-inflammatory syndromes, as well as common pathologies, such as type II diabetes, gout and atherosclerosis. A better understanding of IL-1β synthesis and release is particularly relevant for the design of novel anti-inflammatory drugs. One of the molecules mainly involved in IL-1β maturation is the P2X7 receptor (P2X7R), an ATP-gated ion channel that chiefly acts through the recruitment of the NLRP3 inflammasome-caspase-1 complex. In this review, we will summarize evidence supporting the key role of the P2X7R in IL-1β production, with special emphasis on the mechanism of release, a process that is still a matter of controversy. Four different models have been proposed: (i) exocytosis via secretory lysosomes, (ii) microvesicles shedding from plasma membrane, (iii) release of exosomes, and (iv) passive efflux across a leaky plasma membrane during pyroptotic cell death. All these models involve the P2X7R.

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The opening of P2X7 receptor channels leads to IL-1β production mainly through NLRP3 inflammasome activation, thus contributing to the disruption of the BBB.
“The opening of P2X7 receptor channels leads to IL-1β production mainly through NLRP3 inflammasome activation [123], thus contributing to the disruption of the BBB.”
From Hyperactivation of P2X7 receptors as a culprit of COVID-19 neuropathology (2021) · cites this paper as [123]

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The Role of Inflammation in the Pathogenesis of Osteoarthritis
Chow, Y. Y., & Chin, K. (2020) · Mediators of Inflammation · doi:10.1155/2020/8293921 · Cited by 536 · see citing works
Purinergic Signalling: Therapeutic Developments
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Interleukin-1β is a potential therapeutic target for periodontitis: a narrative review
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The P2X7 Receptor
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Extracellular nucleotides and nucleosides as signalling molecules
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P2X7 Interactions and Signaling – Making Head or Tail of It
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Damage-associated molecular patterns in trauma
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A multiancestry genome-wide association study of unexplained chronic ALT elevation as a proxy for nonalcoholic fatty liver disease with histological and radiological validation
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P2X receptor channels in chronic pain pathways
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Targeted P2X7/NLRP3 signaling pathway against inflammation, apoptosis, and pyroptosis of retinal endothelial cells in diabetic retinopathy
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P2X7 receptor mediates NLRP3-dependent IL-1β secretion and parasite proliferation in Toxoplasma gondii-infected human small intestinal epithelial cells
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Hyperactivation of P2X7 receptors as a culprit of COVID-19 neuropathology
Ribeiro, D. E., Oliveira-Giacomelli, Á., Glaser, T., Arnaud-Sampaio, V. F., Andrejew, R., Dieckmann, L., Baranova, J., Lameu, C., Ratajczak, M. Z., & Ulrich, H. (2021) · Molecular Psychiatry · doi:10.1038/s41380-020-00965-3 · Cited by 145 · see citing works
Modulation of three key innate immune pathways for the most common retinal degenerative diseases
Akhtar‐Schäfer, I., Wang, L., Krohne, T. U., Xu, H., & Langmann, T. (2018) · EMBO Molecular Medicine · doi:10.15252/emmm.201708259 · Cited by 127 · see citing works
Recent advances in CNS P2X7 physiology and pharmacology: Focus on neuropsychiatric disorders
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Advances in the study of emodin: an update on pharmacological properties and mechanistic basis
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Ubiquitination of RIPK1 regulates its activation mediated by TNFR1 and TLRs signaling in distinct manners
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P2X7 Receptor: A Potential Therapeutic Target for Depression?
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Danger signals from mitochondrial DAMPS in trauma and post-injury sepsis
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P2X7 receptor antagonism: Implications in diabetic retinopathy
Platania, C. B. M., Giurdanella, G., Paola, L. D., Leggio, G. M., Drago, F., Salomone, S., & Bucolo, C. (2017) · Biochemical Pharmacology · doi:10.1016/j.bcp.2017.05.001 · Cited by 85 · see citing works
Clemastine Alleviates Depressive-Like Behavior Through Reversing the Imbalance of Microglia-Related Pro-inflammatory State in Mouse Hippocampus
Su, W.-J., Zhang, T., Jiang, C.-L., & Wang, W. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00412 · Cited by 84 · see citing works
Neuropsychopharmacology of JNJ-55308942: evaluation of a clinical candidate targeting P2X7 ion channels in animal models of neuroinflammation and anhedonia
Bhattacharya, A., Lord, B., Grigoleit, J., He, Y., Fraser, I. C., Campbell, S. N., Taylor, N., Aluisio, L. E., O’Connor, J. C., Papp, M., et al. (2018) · Neuropsychopharmacology · doi:10.1038/s41386-018-0141-6 · Cited by 82 · see citing works
Disruption of the Na+/K+-ATPase-purinergic P2X7 receptor complex in microglia promotes stress-induced anxiety
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Serum amyloid A primes microglia for ATP-dependent interleukin-1β release
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Ectonucleotidases in Acute and Chronic Inflammation
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Danger signals: Chemotherapy enhancers?
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The Tumor Microenvironment in Colorectal Cancer Therapy
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Role of P2X7 Receptors in Immune Responses During Neurodegeneration
Oliveira-Giacomelli, Á., Petiz, L. L., Andrejew, R., Turrini, N., Silva, J. B., Sack, U., & Ulrich, H. (2021) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2021.662935 · Cited by 68 · see citing works
Betaine Inhibits Interleukin-1β Production and Release: Potential Mechanisms
Xia, Y., Chen, S., Zhu, G., Huang, R., Yin, Y., & Ren, W. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2018.02670 · Cited by 61 · see citing works
Blood-retinal barrier protection against high glucose damage: The role of P2X7 receptor
Platania, C. B. M., Lazzara, F., Fidilio, A., Fresta, C. G., Conti, F., Giurdanella, G., Leggio, G. M., Salomone, S., Drago, F., & Bucolo, C. (2019) · Biochemical Pharmacology · doi:10.1016/j.bcp.2019.07.010 · Cited by 61 · see citing works
Shaping of Innate Immune Response by Fatty Acid Metabolite Palmitate
Tzeng, H., Chyuan, I., & Chen, W.-Y. (2019) · Cells · doi:10.3390/cells8121633 · Cited by 50 · see citing works
P2X7, a critical regulator and potential target for bone and joint diseases
Zeng, D., Yao, P., & Zhao, H. W. (2018) · Journal of Cellular Physiology · doi:10.1002/jcp.27544 · Cited by 50 · see citing works
Inflammatory Response During Myocardial Infarction
Oliveira, J., Soares, A. A. S. M., & Sposito, A. C. (2018) · Advances in clinical chemistry · doi:10.1016/bs.acc.2017.12.002 · Cited by 50 · see citing works
Autoinflammatory Diseases and Cytokine Storms—Imbalances of Innate and Adaptative Immunity
Marcuzzi, A., Melloni, E., Zauli, G., Romani, A., Secchiero, P., Maximova, N., & Rimondi, E. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011241 · Cited by 49 · see citing works
Prenatal Poly I:C Challenge Affects Behaviors and Neurotransmission via Elevated Neuroinflammation Responses in Female Juvenile Rats
Su, Y., Lian, J., Hodgson, J., Zhang, W., & Deng, C. (2021) · The International Journal of Neuropsychopharmacology · doi:10.1093/ijnp/pyab087 · Cited by 49 · see citing works
The P2X7 receptor: a new therapeutic target in Alzheimer’s disease
Illés, P., Rubini, P., Huang, L., & Tang, Y. (2019) · Expert Opinion on Therapeutic Targets · doi:10.1080/14728222.2019.1575811 · Cited by 49 · see citing works
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Gürsel (2018) · doi:10.1016/j.neubiorev.2018.02.005 · Cited by 47 · see citing works
Novel biologics targeting the P2X7 ion channel.
Koch-Nolte, F., Eichhoff, A., Pinto-Espinoza, C., Schwarz, N., Schäfer, T., Menzel, S., Haag, F., Demeules, M., Gondé, H., & Adriouch, S. (2019) · Current opinion in pharmacology (Print) · doi:10.1016/j.coph.2019.03.001 · Cited by 44 · see citing works
ATP-Gated P2X7 Receptors Require Chloride Channels To Promote Inflammation in Human Macrophages
Janks, L., Sprague, R. S., & Egan, T. M. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801101 · Cited by 45 · see citing works
Rutin mitigates hepatic fibrogenesis and inflammation through targeting TLR4 and P2X7 receptor signaling pathway in vitro and in vivo
Hou, L., Cui, Z., Sun, P., Piao, H.-Q., Han, X., Song, J., Wang, G., Zheng, S., Dong, X.-X., Gao, L., et al. (2019) · Journal of Functional Foods · doi:10.1016/j.jff.2019.103700 · Cited by 43 · see citing works
The P2X7 Receptor Is Shed Into Circulation: Correlation With C-Reactive Protein Levels
Giuliani, A. L., Berchan, M., Sanz, J. M., Passaro, A., Pizzicotti, S., Vultaggio-Poma, V., Sarti, A. C., & Virgilio, F. D. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00793 · Cited by 42 · see citing works
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Peripheral Inflammatory Hyperalgesia Depends on P2X7 Receptors in Satellite Glial Cells
Neves, A. F., Farias, F. H., de Magalhães, S. F., Araldi, D., Pagliusi, M., Tambeli, C. H., Sartori, C. R., Lotufo, C. M. D. C., & Parada, C. A. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.00473 · Cited by 42 · see citing works
Dihydrotanshinone, a Natural Diterpenoid, Preserves Blood-Retinal Barrier Integrity via P2X7 Receptor
Fresta, C. G., Caruso, G., Fidilio, A., Platania, C. B. M., Musso, N., Caraci, F., Drago, F., & Bucolo, C. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239305 · Cited by 41 · see citing works
Emodin attenuated severe acute pancreatitis via the P2X ligand‑gated ion channel�7/NOD‑like receptor protein�3 signaling pathway
Zhang, Q., Tao, X., Xia, S., Qu, J., Song, H., Liu, J., Li, H., & Shang, D. (2018) · Oncology Reports · doi:10.3892/or.2018.6844 · Cited by 40 · see citing works
P2X7 receptor in cardiovascular disease: The heart side
Martinez, C. G. (2019) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.13079 · Cited by 40 · see citing works
Therapeutic Potential of Mesenchymal Stromal Cell-Derived Extracellular Vesicles in the Prevention of Organ Injuries Induced by Traumatic Hemorrhagic Shock
Valade, G., Libert, N., Martinaud, C., Vicaut, É., Banzet, S., & Peltzer, J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.749659 · Cited by 40 · see citing works
Blockade of Pannexin-1 Channels and Purinergic P2X7 Receptors Shows Protective Effects Against Cytokines-Induced Colitis of Human Colonic Mucosa
Diezmos, E. F., Markus, I., Perera, D. S., Gan, S., Zhang, L., Sandow, S. L., Bertrand, P. P., & Liu, L. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00865 · Cited by 39 · see citing works
P2X7 receptor‐targeted regulation by tetrahydroxystilbene glucoside in alcoholic hepatosteatosis: A new strategy towards macrophage–hepatocyte crosstalk
Zhang, Y., Jiang, M., Cui, B., Jin, C. H., Wu, Y., Shang, Y., Yang, H., Wu, M., Liu, J., Qiao, C., et al. (2020) · British Journal of Pharmacology · doi:10.1111/bph.15007 · Cited by 39 · see citing works
Purinergic signaling and tumor microenvironment in cervical Cancer
Pfaffenzeller, M. S., Franciosi, M. L. M., & Cardoso, A. M. (2020) · Purinergic Signalling · doi:10.1007/s11302-020-09693-3 · Cited by 39 · see citing works
P2 Purinergic Signaling in the Distal Lung in Health and Disease
Wirsching, E., Fauler, M., Fois, G., & Frick, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21144973 · Cited by 40 · see citing works
P2X receptor-ion channels in the inflammatory response in adipose tissue and pancreas — potential triggers in onset of type 2 diabetes?
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Authors: Giuliani, A. L., Sarti, A. C., Falzoni, S., & Di Virgilio, F.
Affiliations: University of Ferrara (IT)
ORCID: Giuliani, Anna Lisa
Sarti, Alba C.
Falzoni, Simonetta
Venue: Frontiers in Pharmacology
Publisher: Frontiers Media SA
Published: 2017-03-16
Volume: 8
Pages: 123-123
ISSN: 1663-9812 (ISSN-L)
DOI: 10.3389/fphar.2017.00123
PMC: PMC5353276
OpenAlex: W2597076579
Cited by: 166
References: 126
Citations by year: 2026: 8 · 2025: 9 · 2024: 12 · 2023: 12 · 2022: 17 · 2021: 23 · 2020: 28 · 2019: 20 · 2018: 29 · 2017: 8
FWCI: 2.44
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Pharmacology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Institutional Research Information System University of Ferrara (University of Ferrara) (submittedVersion, cc-by)
Funders: Associazione Italiana per la Ricerca sul Cancro
Ministero della Salute
Università degli Studi di Ferrara
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Adenosine and Purinergic Signaling
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Keywords: P2X7 receptor, IL-1β, IL-1β maturation, NLRP3 inflammasome, caspase-1, ATP-gated ion channels, exocytosis, secretory lysosomes, microvesicles, exosomes, pyroptosis, innate immunity, inflammation, anti-inflammatory drug design

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