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      In Memoriam Geoffrey Burnstock: Creator of Purinergic Signaling

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          Abstract

          Geoff Burnstock (1929–2020) discovered purinergic signaling in a fastidious research that started in early 1960 and culminated in a concept of purinergic nerves in 1972. Subsequently, Geoff developed the concept of purinergic transmission and demonstrated ATP storage, release, and degradation in the context of cotransmission, which was another fundamental concept developed by him. Purinergic transmission contributes to the most fundamental physiological functions such as sensory transduction, regulation of heart rate, smooth muscle contraction, bile secretion, endocrine regulation, immune responses, as well as to various pathophysiological conditions, including inflammation, cancer, neuropathic pain, diabetes, and kidney failure.

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          International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy.

          Maria P Abbracchio, Geoffrey Burnstock, Jean-Marie Boeynaems … (2006)
          There have been many advances in our knowledge about different aspects of P2Y receptor signaling since the last review published by our International Union of Pharmacology subcommittee. More receptor subtypes have been cloned and characterized and most orphan receptors de-orphanized, so that it is now possible to provide a basis for a future subdivision of P2Y receptor subtypes. More is known about the functional elements of the P2Y receptor molecules and the signaling pathways involved, including interactions with ion channels. There have been substantial developments in the design of selective agonists and antagonists to some of the P2Y receptor subtypes. There are new findings about the mechanisms underlying nucleotide release and ectoenzymatic nucleotide breakdown. Interactions between P2Y receptors and receptors to other signaling molecules have been explored as well as P2Y-mediated control of gene transcription. The distribution and roles of P2Y receptor subtypes in many different cell types are better understood and P2Y receptor-related compounds are being explored for therapeutic purposes. These and other advances are discussed in the present review.
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            Adenosine 5'-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation.

            M.J.L. Bours, E.L.R. Swennen, F Di Virgilio … (2006)
            Human health is under constant threat of a wide variety of dangers, both self and nonself. The immune system is occupied with protecting the host against such dangers in order to preserve human health. For that purpose, the immune system is equipped with a diverse array of both cellular and non-cellular effectors that are in continuous communication with each other. The naturally occurring nucleotide adenosine 5'-triphosphate (ATP) and its metabolite adenosine (Ado) probably constitute an intrinsic part of this extensive immunological network through purinergic signaling by their cognate receptors, which are widely expressed throughout the body. This review provides a thorough overview of the effects of ATP and Ado on major immune cell types. The overwhelming evidence indicates that ATP and Ado are important endogenous signaling molecules in immunity and inflammation. Although the role of ATP and Ado during the course of inflammatory and immune responses in vivo appears to be extremely complex, we propose that their immunological role is both interdependent and multifaceted, meaning that the nature of their effects may shift from immunostimulatory to immunoregulatory or vice versa depending on extracellular concentrations as well as on expression patterns of purinergic receptors and ecto-enzymes. Purinergic signaling thus contributes to the fine-tuning of inflammatory and immune responses in such a way that the danger to the host is eliminated efficiently with minimal damage to healthy tissues.
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              Increased Level of Extracellular ATP at Tumor Sites: In Vivo Imaging with Plasma Membrane Luciferase

              Patrizia Pellegatti, Lizzia Raffaghello, Giovanna Bianchi … (2008)
              Background There is growing awareness that tumour cells build up a “self-advantageous” microenvironment that reduces effectiveness of anti-tumour immune response. While many different immunosuppressive mechanisms are likely to come into play, recent evidence suggests that extracellular adenosine acting at A2A receptors may have a major role in down-modulating the immune response as cancerous tissues contain elevated levels of adenosine and adenosine break-down products. While there is no doubt that all cells possess plasma membrane adenosine transporters that mediate adenosine uptake and may also allow its release, it is now clear that most of extracellularly-generated adenosine originates from the catabolism of extracellular ATP. Methodology/Principal Findings Measurement of extracellular ATP is generally performed in cell supernatants by HPLC or soluble luciferin-luciferase assay, thus it generally turns out to be laborious and inaccurate. We have engineered a chimeric plasma membrane-targeted luciferase that allows in vivo real-time imaging of extracellular ATP. With this novel probe we have measured the ATP concentration within the tumour microenvironment of several experimentally-induced tumours. Conclusions/Significance Our results show that ATP in the tumour interstitium is in the hundrends micromolar range, while it is basically undetectable in healthy tissues. Here we show that a chimeric plasma membrane-targeted luciferase allows in vivo detection of high extracellular ATP concentration at tumour sites. On the contrary, tumour-free tissues show undetectable extracellular ATP levels. Extracellular ATP may be crucial for the tumour not only as a stimulus for growth but also as a source of an immunosuppressive agent such as adenosine. Our approach offers a new tool for the investigation of the biochemical composition of tumour milieu and for development of novel therapies based on the modulation of extracellular purine-based signalling.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Function (Oxf)
                Journal ID (iso-abbrev): Function (Oxf)
                Journal ID (publisher-id): function
                Title: Function
                Publisher: Oxford University Press
                ISSN (Electronic): 2633-8823
                Publication date Collection: 2020
                Publication date (Electronic): 25 June 2020
                Publication date PMC-release: 25 June 2020
                Volume: 1
                Issue: 1
                Electronic Location Identifier: zqaa006
                Affiliations
                [1 ]Faculty of Biology, Medicine and Health, The University of Manchester , Manchester, M13 9PT, UK
                [2 ] Achucarro Centre for Neuroscience, IKERBASQUE , 48011 Bilbao, Spain
                [3 ]Institute of Cell Biology and Neuroscience, Molecular and Cellular Neurobiology, Goethe-University , Frankfurt am Main, Germany
                [4 ]Department of Pharmacological Sciences, Laboratory of Molecular and Cellular Pharmacology of Purinergic Transmission, University of Milan , Milan, Italy
                [5 ]Rudolf Boehm Institute for Pharmacology and Toxicology, University of Leipzig , Germany
                [6 ]Department of Medical Sciences, University of Ferrara , Ferrara, Leipzig, Italy
                Author notes
                Corresponding author. E-mail: alexej.verkhratsky@ 123456manchester.ac.uk
                Article
                Publisher ID: zqaa006
                DOI: 10.1093/function/zqaa006
                PMC ID: 8788863
                SO-VID: b308ee85-0cba-4634-ae06-37578317f29a
                Copyright © © The Author(s) 2020. Published by Oxford University Press on behalf of American Physiological Society.
                License:

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Date received : 20 June 2020
                Date accepted : 22 June 2020
                Page count
                Pages: 11
                Categories
                Subject: Invited Obituary

                Keywords: atp,purinergic signaling purinoceptors,vesicular release,ectonucleotidases,inflammation
                Data availability:
                Keywords: atp, purinergic signaling purinoceptors, vesicular release, ectonucleotidases, inflammation

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