Geoffrey Burnstock 1929–2020†
R. Alan North A * and Marcello Costa B
+ Author Affiliations
- Author Affiliations
A University of Manchester, Oxford Road, Manchester M13 9PL, UK.
B Flinders University, Bedford Park, SA 5042, Australia.
* Correspondence to: alannorth@me.com, , r.a.north@manchester.ac.uk
Historical Records of Australian Science 33(2) 160-171 https://doi.org/10.1071/HR22004
Published: 8 June 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the Australian Academy of Science.
Abstract
Geoffrey Burnstock was a biomedical scientist who gained renown for his discovery that adenosine 5′-triphosphate (ATP) functions as an extracellular signalling molecule. Born in London and educated at King’s and University Colleges, he did postdoctoral work at Mill Hill and Oxford. He moved in 1959 to the Department of Zoology at the University of Melbourne because he sensed there a greater freedom to challenge established thinking in physiology. His group found that transmission from sympathetic and parasympathetic autonomic nerves to smooth muscle was in some places not mediated by the accepted chemical messengers (noradrenaline and acetylcholine). He amassed evidence that ATP was this non-adrenergic, non-cholinergic (NANC) transmitter, using biochemical, histological and electrophysiological approaches: heretically, he styled this ‘purinergic transmission’. Geoff further upset dogma in the 1970s by proposing ‘co-transmission’ in which some nerves released ATP in addition to either noradrenaline or acetylcholine. He distinguished pharmacologically P1 receptors (activated best by adenosine and blocked by xanthines) and P2 receptors (activated best by purine nucleotides such as ATP) and he proposed in 1985 that the latter embraced P2X (ion channel) and P2Y (G protein-coupled) subtypes: about ten years later these categories were substantiated by cDNA cloning. From 1975 until his retirement in 1997, Geoff was head of Anatomy and Embryology at University College London (UCL), which he developed energetically into a large and strong research department. Later, as head of the Autonomic Research Institute at the Royal Free (part of UCL), he continued to collaborate extensively, and founded several journals and international professional societies. He widely sought clinical benefit for his discoveries, and both P2X and P2Y receptors have been developed as the targets of useful therapeutics (gefapixant, clopidogrel). Geoff was proud of his modest, rather humble, background and eschewed formality. He may have smiled when his early discoveries were met with cynicism, even ridicule (‘pure-imagine’ transmission noted one amusing critic), but this just reinforced his resolve and encouraged his encyclopaedic oeuvre.
Keywords: ATP, biochemistry, physiology, protein-coupled, purinergic, transmission, zoology.
References
Abbracchio, M. P., Burnstock, G., Boeynaems, J. M., Barnard, E. A., Boyer, J. L., Kennedy, C., Knight, G. E., Fumagalli, M., Gachet, C., Jacobson, K. A., and Weisman, G. A. (2006) International union of pharmacology LVIII: update in the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy, Pharmacological Reviews, 58, 281–341.| International union of pharmacology LVIII: update in the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapyCrossref | GoogleScholarGoogle Scholar | 16968944PubMed |
Ahlquist, R. P. (1948) A study of adrenotropic receptors, American Journal of Physiology-Legacy Content, 153, 586–600.
| A study of adrenotropic receptorsCrossref | GoogleScholarGoogle Scholar |
Ambache, N., and Aboo Zar, M. (1971) Evidence against adrenergic motor transmission in the guinea-pig vas deferens, Journal of Physiology, 216, 359–389.
| Evidence against adrenergic motor transmission in the guinea-pig vas deferensCrossref | GoogleScholarGoogle Scholar | 4397760PubMed |
Barnard, E. A. (2000) Imagination and reality in the search for the P2Y receptors, Journal of the Autonomic Nervous System, 81, 10–15.
| Imagination and reality in the search for the P2Y receptorsCrossref | GoogleScholarGoogle Scholar | 10869694PubMed |
Bennett, M.R., Burnstock, G., and Holman, M. E. (1966) Transmission from intramural inhibitory nerves to the smooth muscle of the guinea pig taenia coli, Journal of Physiology, 182, 541–558.
| Transmission from intramural inhibitory nerves to the smooth muscle of the guinea pig taenia coliCrossref | GoogleScholarGoogle Scholar | 5943000PubMed |
Bennett, J. P., Cockcroft, S., and Gomperts, B. D. (1981) Rat mast cells permeabilized with ATP secrete histamine in response to calcium ions buffered in the micromolar range, Journal of Physiology, 317, 335–345.
| Rat mast cells permeabilized with ATP secrete histamine in response to calcium ions buffered in the micromolar rangeCrossref | GoogleScholarGoogle Scholar | 6171640PubMed |
Bo, X., Zhang, Y., Nassar, M., Burnstock, G., and Schoepfer, R. (1995) A P2X purinoceptor cDNA conferring a novel pharmacological profile, FEBS Letters, 375, 129–133.
| A P2X purinoceptor cDNA conferring a novel pharmacological profileCrossref | GoogleScholarGoogle Scholar | 7498461PubMed |
Born, G. V. R. (1962) Aggregation of blood platelets by adenosine diphosphate and its reversal, Nature, 194, 927–929.
| Aggregation of blood platelets by adenosine diphosphate and its reversalCrossref | GoogleScholarGoogle Scholar |
Brake, A. J., Wagenbach, M. J., and Julius, D. (1994) New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptor, Nature, 371, 519–523.
| New structural motif for ligand-gated ion channels defined by an ionotropic ATP receptorCrossref | GoogleScholarGoogle Scholar | 7523952PubMed |
Brownstein, M. J., Saavedra, J. M., Axelrod, J., Zeman, G. H., and Carpenter, D. O. (1974) Coexistence of several putative neurotransmitters in single identified neurons of Aplysia, Proceedings of the National Academy of Sciences, 71, 4662–4665.
| Coexistence of several putative neurotransmitters in single identified neurons of AplysiaCrossref | GoogleScholarGoogle Scholar |
Bülbring, E., Burnstock, G., and Holman, M. E. (1958) Excitation and conduction in the smooth muscle of the isolated taenia coli of the guinea-pig, Journal of Physiology, 142, 420–437.
| Excitation and conduction in the smooth muscle of the isolated taenia coli of the guinea-pigCrossref | GoogleScholarGoogle Scholar | 13576445PubMed |
Burnstock, G. (1957) A ‘window’ technique for observing fish viscera in vivo, Nature, 180, 1491–1492.
| A ‘window’ technique for observing fish viscera in vivoCrossref | GoogleScholarGoogle Scholar | 13493582PubMed |
Burnstock, G. (1958) The effects of acetylcholine on membrane potential, spike frequency, conduction velocity and excitability in the taenia coli of the guinea-pig, Journal of Physiology, 143, 165–182.
| The effects of acetylcholine on membrane potential, spike frequency, conduction velocity and excitability in the taenia coli of the guinea-pigCrossref | GoogleScholarGoogle Scholar | 13576467PubMed |
Burnstock, G. (1960) Membrane potential changes associated with stimulation of smooth muscle by adrenalin, Nature, 186, 727–728.
| Membrane potential changes associated with stimulation of smooth muscle by adrenalinCrossref | GoogleScholarGoogle Scholar | 13806275PubMed |
Burnstock, G. (1971) Neural nomenclature, Nature, 229, 282–283.
| Neural nomenclatureCrossref | GoogleScholarGoogle Scholar | 4396222PubMed |
Burnstock, G. (1972) Purinergic nerves, Pharmacological Reviews, 24, 509–581.
| Purinergic nervesCrossref | GoogleScholarGoogle Scholar | 4404211PubMed |
Burnstock, G. (1976) Do some nerve cells release more than one transmitter?, Neuroscience, 1, 239–248.
| Do some nerve cells release more than one transmitter?Crossref | GoogleScholarGoogle Scholar | 11370511PubMed |
Burnstock, G. (1978) A basis for distinguishing two types of purinergic receptors, in Cell Membrane Receptors for Drugs and Hormones: a Multidisciplinary Approach, eds R. W. Straub, L. Bolis, New York, pp. 107–118.
Burnstock, G. (2018) Against the Odds: an Autobiography, Suffolk, UK.
Burnstock, G., and Holman, M. E. (1960) Autonomic nerve-smooth muscle transmission, Nature, 187, 951–952.
| Autonomic nerve-smooth muscle transmissionCrossref | GoogleScholarGoogle Scholar | 13689212PubMed |
Burnstock, G., and Holman, M. E. (1963) Smooth muscle—autonomic nerve transmission, Annual Reviews of Physiology, 25, 61–90.
| Smooth muscle—autonomic nerve transmissionCrossref | GoogleScholarGoogle Scholar |
Burnstock, G., and Kennedy, C. (1985) Is there a basis for distinguishing two types of P2-purinoceptor?, General Pharmacology: the Vascular System, 16, 433–440.
| Is there a basis for distinguishing two types of P2-purinoceptor?Crossref | GoogleScholarGoogle Scholar | 2996968PubMed |
Burnstock, G., and Straub, R. W. (1958) A method for studying the effects of ions and drugs on the resting and action potentials in smooth muscle with external electrodes, Journal of Physiology, 140, 156–167.
| A method for studying the effects of ions and drugs on the resting and action potentials in smooth muscle with external electrodesCrossref | GoogleScholarGoogle Scholar | 13514658PubMed |
Burnstock, G., Holman, M. E., and Prosser, C. L. (1963a) Electrophysiology of smooth muscle, Physiological Reviews, 43, 482–527.
| Electrophysiology of smooth muscleCrossref | GoogleScholarGoogle Scholar | 14017173PubMed |
Burnstock, G., Campbell, G., Bennett, M., and Holman, M. E. (1963b) The effect of drugs on the transmission of inhibition from autonomic nerves to the smooth muscle of the guinea pig taenia coli, Biochemical Pharmacology, 12, 134–135.
| The effect of drugs on the transmission of inhibition from autonomic nerves to the smooth muscle of the guinea pig taenia coliCrossref | GoogleScholarGoogle Scholar |
Burnstock, G., Campbell, G., Bennett, M., and Holman, M. E. (1963c) Inhibition of the smooth muscle on the taenia coli, Nature, 200, 581–582.
| Inhibition of the smooth muscle on the taenia coliCrossref | GoogleScholarGoogle Scholar | 14082235PubMed |
Burnstock, G., Campbell, G., Bennett, M., and Holman, M. E. (1964) Innervation of the guinea pig taenia coli: are there intrinsic inhibitory nerves which are distinct from sympathetic nerves?, International Journal of Neuropharmacology, 3, 163–166.
| Innervation of the guinea pig taenia coli: are there intrinsic inhibitory nerves which are distinct from sympathetic nerves?Crossref | GoogleScholarGoogle Scholar | 14336522PubMed |
Burnstock, G., Campbell, G., and Rand, M. J. (1966) The inhibitory innervation of the taenia of the guinea-pig caecum, Journal of Physiology, 182, 504–526.
| The inhibitory innervation of the taenia of the guinea-pig caecumCrossref | GoogleScholarGoogle Scholar | 5942999PubMed |
Burnstock, G., Satchell, D. G., and Campbell, G. (1969) Evidence for a purine compound as of transmitter in non-adrenergic inhibitory neurons in gut, Australian Journal of Experimental Biology and Medical Science, 47, 24.
| Evidence for a purine compound as of transmitter in non-adrenergic inhibitory neurons in gutCrossref | GoogleScholarGoogle Scholar |
Burnstock, G., Campbell, G., Stachell, D., and Smythe, A. (1970) Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut, British Journal of Pharmacology, 40, 668–688.
| Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gutCrossref | GoogleScholarGoogle Scholar | 4322041PubMed |
Campbell, G. (1966) The inhibitory nerve fibres in the vagal supply to the guinea-pig stomach, Journal of Physiology, 185, 600–612.
| The inhibitory nerve fibres in the vagal supply to the guinea-pig stomachCrossref | GoogleScholarGoogle Scholar | 5950555PubMed |
Campbell, G. (1969) The autonomic innervation of the stomach of a toad (Bufo marinus), Comparative Biochemistry and Physiology, 31, 693–706.
| The autonomic innervation of the stomach of a toad (Bufo marinus)Crossref | GoogleScholarGoogle Scholar | 5366179PubMed |
Campbell, G. (1970) The identification of neurotransmitters to smooth muscle, in Smooth Muscle, eds E. Bülbring, A. F. Brading, A. W. Jones, T. Tomita, Baltimore, pp. 496–524.
Campbell, G. (1991) Early experiences in the discovery of nonadrenergic, noncholinergic (NANC) autonomic neurons, in Novel Peripheral Neurotransmitters, ed. C. Bell, New York, pp. 1–7.
Carlsson, A., and Hillarp, N. A. (1956) Release of adenosine triphosphate along with adrenaline and noradrenaline following stimulation of adrenal medulla, Acta Physiologica Scandinavica, 37, 235–239.
| Release of adenosine triphosphate along with adrenaline and noradrenaline following stimulation of adrenal medullaCrossref | GoogleScholarGoogle Scholar | 13361903PubMed |
Chen, C. C., Akopian, A. N., Sivilottit, L., Colquhoun, D., Burnstock, G., and Wood, J. N. (1995) A P2X purinoceptor expressed by a subset of sensory neurons, Nature, 377, 428–431.
| A P2X purinoceptor expressed by a subset of sensory neuronsCrossref | GoogleScholarGoogle Scholar | 7566119PubMed |
Cockcroft, S., and Gomperts, B. D. (1979) ATP induces nucleotide permeability in rat mast cells, Nature, 279, 541–542.
| ATP induces nucleotide permeability in rat mast cellsCrossref | GoogleScholarGoogle Scholar | 450099PubMed |
Cockcroft, S., and Gomperts, B. D. (1980) The ATP4- receptor of rat mast cells, Biochemical Journal, 188, 789–798.
| The ATP4- receptor of rat mast cellsCrossref | GoogleScholarGoogle Scholar | 6162453PubMed |
Cohen, P. (2002) The origins of protein phosphorylation, Nature Cell Biology, 4, E127–E130.
| The origins of protein phosphorylationCrossref | GoogleScholarGoogle Scholar | 11988757PubMed |
Collo, G., North, R. A., Kawashima, E., Merlo-Pich, E., Neidhart, S., Surprenant, A., and Buell, G. (1996) Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channels, Journal of Neuroscience, 16, 2495–2507.
| Cloning of P2X5 and P2X6 receptors and the distribution and properties of an extended family of ATP-gated ion channelsCrossref | GoogleScholarGoogle Scholar | 8786426PubMed |
Costa, M., Furness, J. B., and Humphreys, C. M. S. (1986) Apamin distinguishes two types of relaxation mediated by enteric nerves in the guinea-pig gastrointestinal tract, Naunyn-Schmiedeberg's Archives of Pharmacology, 332, 79–88.
| Apamin distinguishes two types of relaxation mediated by enteric nerves in the guinea-pig gastrointestinal tractCrossref | GoogleScholarGoogle Scholar | 3005886PubMed |
Dale, H. (1935) Pharmacology and nerve endings, Proceedings of the Royal Society of Medicine, 28, 319–332.
| Pharmacology and nerve endingsCrossref | GoogleScholarGoogle Scholar | 19990108PubMed |
Dixon, R. A. F., Kobilka, B. K., Strader, D. J., Benovic, J. L., Dohlman, H. G., Frielle, T., Bolanowski, M. A., Bennett, C. D., Rands, E., Diehl, R. E., Mumford, R. A., Slater, E.E., Sigal, I. S., Caron, M. G., Lefkowitz, R. J., and Strader, C. D. (1986) Cloning of the gene and cDNA for mammalian β-adrenergic receptor and homology with rhodopsin, Nature, 321, 75–79.
| Cloning of the gene and cDNA for mammalian β-adrenergic receptor and homology with rhodopsinCrossref | GoogleScholarGoogle Scholar |
Douguet, L., Janho dit Hreich, S., Benzaquen, J., Seguin, L., Juhel, T., Dezitter, X., Duranton, C., Ryffel, B., Kanellopoulos, J., Delarasse, C., Renault, N., Furman, C., Homerin, G., Féral, C., Cherfils-Vicini, J., Millet, R., Adriouch, S., Ghinet, A., Hofman, P., and Vouret-Craviari, V. (2021) A small-molecule P2RX7 activator promotes anti-tumor immune responses and sensitizes lung tumor to immunotherapy, Nature Communications, 12, 653.
| A small-molecule P2RX7 activator promotes anti-tumor immune responses and sensitizes lung tumor to immunotherapyCrossref | GoogleScholarGoogle Scholar | 33510147PubMed |
Drury, A. N., and Szent-Györgyi, A. (1929) The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart, Journal of Physiology, 68, 213–237.
| The physiological activity of adenine compounds with especial reference to their action upon the mammalian heartCrossref | GoogleScholarGoogle Scholar | 16994064PubMed |
Dubyak, G. R., and De Young, M. B. (1985) Intracellular Ca2+ mobilization activated by extracellular ATP in Ehrlich ascites tumor cells, Journal of Biological Chemistry, 260, 10653–10661.
| Intracellular Ca2+ mobilization activated by extracellular ATP in Ehrlich ascites tumor cellsCrossref | GoogleScholarGoogle Scholar | 4030763PubMed |
Fedan, J. S., Hogaboom, G. K., O’Donnell, J. P., Colby, J., and Westfall, D. P. (1981) Contribution by purines to the neurogenic response of he vas deferens of the guinea pig, European Journal of Pharmacology, 69, 41–53.
| Contribution by purines to the neurogenic response of he vas deferens of the guinea pigCrossref | GoogleScholarGoogle Scholar | 7202512PubMed |
Fiske, C. H., and Subbarow, Y. (1929) Phosphorus compounds of muscle and liver, Science, 70, 381–382.
| Phosphorus compounds of muscle and liverCrossref | GoogleScholarGoogle Scholar | 17756191PubMed |
Flower, R. (2020) Gustav Victor Rudolph Born. 29 July 1921—16 April 2018, Biographical Memoirs of Fellows of the Royal Society, 68, 23–47.
| Gustav Victor Rudolph Born. 29 July 1921—16 April 2018Crossref | GoogleScholarGoogle Scholar |
Furness, J. B., Costa, M., and Walsh, J. H. (1981) Evidence for and significance of the projections of VIP neurons from the myenteric plexus to the taenia coli in the guinea-pig, Gastroenterology, 80, 1557–1561.
| Evidence for and significance of the projections of VIP neurons from the myenteric plexus to the taenia coli in the guinea-pigCrossref | GoogleScholarGoogle Scholar | 6262184PubMed |
Gaarder, A., Jonsen, J., Laland, S., Heilen, A., and Owren, P. A. (1961) Adenosine diphosphate in red cells as a factor in adhesiveness of human blood platelets, Nature, 192, 531–532.
| Adenosine diphosphate in red cells as a factor in adhesiveness of human blood plateletsCrossref | GoogleScholarGoogle Scholar | 13896038PubMed |
Gomperts, B. D. (1983) Involvement of guanine nucleotide-binding protein in the gating of Ca2+ by receptors, Nature, 306, 64–66.
| Involvement of guanine nucleotide-binding protein in the gating of Ca2+ by receptorsCrossref | GoogleScholarGoogle Scholar | 6195532PubMed |
Hökfelt, T., Johansson, O., Efendic, S., Luft, R., and Arimura, A. (1975a) Are there somatostatin-containing nerves in rat gut—immunohistochemical evidence for a new type of peripheral nerves, Experientia, 31, 852–854.
| Are there somatostatin-containing nerves in rat gut—immunohistochemical evidence for a new type of peripheral nervesCrossref | GoogleScholarGoogle Scholar | 1095398PubMed |
Hökfelt, T., Kellerth, J. O., Nilsson, G., and Pernow, B. (1975b) Substance P localization in central nervous system and in some primary afferent neurons, Science, 190, 889–890.
| Substance P localization in central nervous system and in some primary afferent neuronsCrossref | GoogleScholarGoogle Scholar | 242075PubMed |
Jahr, C. E., and Jessell, T. M. (1983) ATP excites a subpopulation of rat dorsal horn neurones, Nature, 304, 730–733.
| ATP excites a subpopulation of rat dorsal horn neuronesCrossref | GoogleScholarGoogle Scholar | 6888539PubMed |
Kalckar, H. M. (1941) The nature of energetic coupling in biological syntheses, Chemical Review, 28, 71–178.
| The nature of energetic coupling in biological synthesesCrossref | GoogleScholarGoogle Scholar |
Kamata-Sakurai, M., Narita, Y., Hori, Y., Nemoto, T., Uchikawa, R., Honda, M., Hironiwa, N., Taniguchi, K., Shida-Kawazoe, M., Metsugi, S., Miyazaki, T., Wada, N. A., Ohte, Y., Shimizu, S., Mikami, H., Tachibana, T., Ono, N., Adachi, K., Sakiyama, T., Matsushita, T., Kadono, S., Komatsu, S-I., Sakamoto, A., Horikawa, S., Hirako, A., Hamada, K., Naoi, S., Savory, N., Satoh, Y., Sato, M., Noguchi, Y., Shinozuka, J., Kuroi, H., Ito, A., Wakabayashi, T., Kamimura, M., Isomura, F., Tomii, Y., Sawada, N., Kato, A., Ueda, O., Nakanishi, Y., Endo, M., Jishage, K-I., Kawabe, Y., Kitazawa, T., and Igawa, T. (2021) Antibody to CD137 activated by extracellular adenosine triphosphate is tumor selective and broadly effective in vivo without systemic immune activation, Cancer Discovery, 11, 158–175.
| Antibody to CD137 activated by extracellular adenosine triphosphate is tumor selective and broadly effective in vivo without systemic immune activationCrossref | GoogleScholarGoogle Scholar | 32847940PubMed |
Kolb, H.-A., and Wakelam, M. J. O. (1983) Transmitter-like action of ATP on patched membranes of cultured myoblasts and myotubes, Nature, 303, 621–623.
| Transmitter-like action of ATP on patched membranes of cultured myoblasts and myotubesCrossref | GoogleScholarGoogle Scholar | 6304532PubMed |
Konijn, T. M., Van de Meene, J. G., Bonner, J. T., and Barkley, D. S. (1967) The acrasin activity of adenosine-3’,5’-cyclic phosphate, Proceedings of the National Academies of Science USA, 58, 1152–1154.
| The acrasin activity of adenosine-3’,5’-cyclic phosphateCrossref | GoogleScholarGoogle Scholar |
Konishi, S., and Otsuka, M. (1974) The effects of substance P and other peptides on spinal neurons of the frog, Brain Research, 65, 397–410.
| The effects of substance P and other peptides on spinal neurons of the frogCrossref | GoogleScholarGoogle Scholar | 4153509PubMed |
Krishtal, O. A., Marchenko, S. M., and Pidoplichko, V. I. (1983) Receptor for ATP in the membrane of mammalian sensory neurones, Neuroscience Letters, 35, 41–45.
| Receptor for ATP in the membrane of mammalian sensory neuronesCrossref | GoogleScholarGoogle Scholar | 6302606PubMed |
Lewis, C., Neidhart, S., Holy, C., North, R. A., Buell, G., and Surprenant, A. (1995) Coexpression of P2X(2) and P2X(3) receptor subunits can account for ATP-gated currents in sensory neurons, Nature, 377, 432–435.
| Coexpression of P2X(2) and P2X(3) receptor subunits can account for ATP-gated currents in sensory neuronsCrossref | GoogleScholarGoogle Scholar | 7566120PubMed |
Lieberman, A. R. (1997) Now and then: cell and developmental Biology at UCL: a history. Transcript Available at https://www.ucl.ac.uk/biosciences/sites/biosciences/files/cdb-about-short-history.pdf [viewed May 2021]
Lipmann, F. (1941) Metabolic generation and utilization of phosphate bond energy, in Advances in Enzymology and Related Areas of Molecular Biology, eds F. F. Nord, C. H. Werkman, New York, Vol. 1, pp. 100–162.
| Crossref |
Lohmann, K. (1929) On the pyrophosphate fraction in muscle, Naturwissenschaften, 17, 624–625.
Lustig, K. D., Shiau, A. K., Brake, A. J., and Julius, D. (1993) Expression cloning of an ATP receptor from mouse neuroblastoma cells, Proceedings of the National Academy of Sciences, 90, 5113–5117.
| Expression cloning of an ATP receptor from mouse neuroblastoma cellsCrossref | GoogleScholarGoogle Scholar |
Maruyama, K. (1991) The discovery of adenosine triphosphate and the establishment of its structure, Journal of the History of Biology, 24, 145–154.
| The discovery of adenosine triphosphate and the establishment of its structureCrossref | GoogleScholarGoogle Scholar |
Meldrum, L. A., and Burnstock, G. (1983) Evidence that ATP acts as a co-transmitter with noradrenaline in sympathetic nerves supplying the guinea-pig vas deferens, European Journal of Pharmacology, 92, 161–163.
| Evidence that ATP acts as a co-transmitter with noradrenaline in sympathetic nerves supplying the guinea-pig vas deferensCrossref | GoogleScholarGoogle Scholar | 6685044PubMed |
Mimoto, F., Tatsumi, K., Shimizu, S., Kadono, S., Haraya, K., Nagayasu, M., Suzuki, Y., Fujii, E., Kamimura, M., Hayasaka, A., Kawauchi, H., Ohara, K., Matsushita, M., Baba, T., Susumu, H., Sakashita, T., Muraoka, T., Aso, K., Katada, H., Tanaka, E., Nakagawa, K., Hasegawa, M., Ayabe, M., Yamamoto, T., Tanba, S., Ishiguro, T., Kamikawa, T., Nambu, T., Kibayashi, T., Azuma, Y., Tomii, Y., Kato, A., Ozeki, K., Murao, N., Endo, M., Kikuta, J., Kamata-Sakurai, M., Ishii, M., Hattori, K., and Igawa, T. (2020) Exploitation of elevated extracellular ATP to specifically direct antibody to tumor microenvironment, Cell Reports, 33, 108542.
| Exploitation of elevated extracellular ATP to specifically direct antibody to tumor microenvironmentCrossref | GoogleScholarGoogle Scholar | 33357423PubMed |
Nicoll, R. A., and Barker, J. L. (1971) Excitation of supraoptic neurosecretory cells by angiotensin: II, Nature New Biology, 233, 172–174.
| Excitation of supraoptic neurosecretory cells by angiotensin: IICrossref | GoogleScholarGoogle Scholar | 4330552PubMed |
Noda, M., Takahashi, H., Tanabe, T., Toyosato, M., Kikyotani, S., Furutani, Y., Hirose, T., Takashima, H., Inayama, S., Miyata, T., and Numa, S. (1983) Structural homology of Torpedo californica acetylcholine receptor subunits, Nature, 302, 528–532.
| Structural homology of Torpedo californica acetylcholine receptor subunitsCrossref | GoogleScholarGoogle Scholar | 6188060PubMed |
North, R. A. (2002) Molecular physiology of P2X receptors, Physiological Reviews, 82, 1013–1067.
| Molecular physiology of P2X receptorsCrossref | GoogleScholarGoogle Scholar | 12270951PubMed |
Sanders, K. M., and Ward, S. M. (1992) Nitric oxide as a mediator of nonadrenergic, noncholinergic neurotransmission, American Journal of Physiology-Gastrointestinal and Liver Physiology, 262, G379–G392.
| Nitric oxide as a mediator of nonadrenergic, noncholinergic neurotransmissionCrossref | GoogleScholarGoogle Scholar |
Schild, H. O. (1947) pA, a new scale for the measurement of drug antagonism, British Journal of Pharmacology and Chemotherapy, 2, 189–206.
| pA, a new scale for the measurement of drug antagonismCrossref | GoogleScholarGoogle Scholar | 20258355PubMed |
Smith, A. D. (1972) Subcellular localization of noradrenaline in sympathetic neurons, Pharmacological Reviews, 24, 435–457.
| 4561223PubMed |
Sneddon, P., and Burnstock, G. (1984) ATP as a co-transmitter in rat tail artery, European Journal of Pharmacology, 106, 149–152.
| ATP as a co-transmitter in rat tail arteryCrossref | GoogleScholarGoogle Scholar | 6152212PubMed |
Sneddon, P., Westfall, D. P., and Fedan, J. S. (1982) Co-transmitters in the motor nerves of the guinea-pig vas deferens: electrophysiological evidence, Science, 218, 693–695.
| Co-transmitters in the motor nerves of the guinea-pig vas deferens: electrophysiological evidenceCrossref | GoogleScholarGoogle Scholar | 6291151PubMed |
Stämpfli, R. (1954) A new method for measuring membrane potentials with external electrodes, Experientia, 10, 508–509.
| A new method for measuring membrane potentials with external electrodesCrossref | GoogleScholarGoogle Scholar | 14353097PubMed |
Stephenson, F. A. (2020) Eric A. Barnard. 2 July 1927—23 May 2018, Biographical Memoirs of Fellows of the Royal Society, 69, 37–61.
| Eric A. Barnard. 2 July 1927—23 May 2018Crossref | GoogleScholarGoogle Scholar |
Valera, S., Hussy, N., Evans, R. J., Adami, N., North, R. A., Surprenant, A., and Buell, G. (1994) A new class of ligand-gated ion channel defined by P2X receptor for extracellular ATP, Nature, 371, 516–519.
| A new class of ligand-gated ion channel defined by P2X receptor for extracellular ATPCrossref | GoogleScholarGoogle Scholar | 7523951PubMed |
Webb, T. E., Simon, J., Krishek, B. J., Bateson, A. N., Smart, T. G., King, B. F., Burnstock, G., and Barnard, E. A. (1993) Cloning and functional expression of a brain G-protein-coupled ATP receptor, FEBS Letters, 324, 219–225.
| Cloning and functional expression of a brain G-protein-coupled ATP receptorCrossref | GoogleScholarGoogle Scholar | 8508924PubMed |
