Purinergic signalling: Pathophysiology and therapeutic potential

Keio Journal of Medicine

Volumn 62, Issue 3, 2013, Pages 63-73

  Burnstock, Geoffrey ^a,b  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

ATP; Bladder disorders; CNS diseases; Hypertension; Pain

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BOTULINUM TOXIN A; CHOLINERGIC RECEPTOR; CLOPIDOGREL; ECTO 5' NUCLEOTIDASE; GUANINE NUCLEOTIDE BINDING PROTEIN; NORADRENALIN; PURINERGIC P2X RECEPTOR AGONIST; PURINERGIC P2X RECEPTOR ANTAGONIST; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y RECEPTOR AGONIST; PURINERGIC P2Y RECEPTOR ANTAGONIST; PURINERGIC P2Y1 RECEPTOR; PURINERGIC P2Y2 RECEPTOR; PURINERGIC RECEPTOR; TETRODOTOXIN;

ACUPUNCTURE; BLADDER DISEASE; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CENTRAL NERVOUS SYSTEM DISEASE; CEREBROVASCULAR ACCIDENT; CYSTIC FIBROSIS; DIABETES MELLITUS; DRY EYE; ENTERITIS; ERECTILE DYSFUNCTION; FERTILIZATION IN VITRO; GANGLION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; HYPERVENTILATION; INFERTILITY; KIDNEY FAILURE; NEOPLASM; NERVE STIMULATION; NEUROMODULATION; NEUROPATHIC PAIN; NEUROTRANSMISSION; NONADRENERGIC NONCHOLINERGIC NERVE; NONHUMAN; OSTEOPOROSIS; PAIN; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; RESPIRATORY TRACT DISEASE; REVIEW; SIGNAL TRANSDUCTION; SYNAPSE; THROMBOSIS; URINE INCONTINENCE;

ADENOSINE TRIPHOSPHATE; ANIMALS; CENTRAL NERVOUS SYSTEM DISEASES; HUMANS; NEOPLASMS; PAIN; RECEPTORS, PURINERGIC; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

EID: 84884566998     PISSN: 00229717     EISSN: 18801293     Source Type: Journal    
DOI: 10.2302/kjm.2013-0003-RE     Document Type: Review

References (113)

1. Burnstock G: Pathophysiology and therapeutic potential of pu-rinergic signaling. Pharmacol Rev 2006; 58: 58-86.
2. Burnstock G: Purinergic receptors and pain. Curr Pharm Des 2009; 15: 1717-1735.
3. Burnstock G: Therapeutic potential of purinergic signalling for diseases of the urinary tract. BJU Int 2011; 107: 192-204.
4. Erlinge D, Burnstock G: P2 receptors in cardiovascular physiology and disease. Purinergic Signal 2008; 4: 1-20.
5. Shabbir M, Burnstock G: Purinergic receptor-mediated effects of adenosine 5′-triphosphate in urological malignant diseases. Int J Urol 2009; 16: 143-150.
6. Burnstock G, Kennedy C: P2X receptors in health and disease; in: Jacobson KA, Linden J, eds, Purine and Pyrimidine Receptor Pharmacology. Burlington, Academic Press, 2011; 333-372.
7. Burnstock G, Novak I: Purinergic signalling in the pancreas in health and disease. J Endocrinol 2012; 213: 123-141.
8. Burnstock G, Knight GE, Greig AV: Purinergic signalling in healthy and diseased skin. J Invest Dermatol 2012; 132: 526-546.
9. Burnstock G, Straub RW: A method for studying the effects of ions and drugs on the resting and action potentials in smooth muscle with external electrodes. J Physiol 1958; 140: 156-167.
10. Burnstock G: The effects of acetylcholine on membrane potential, spike frequency, conduction velocity and excitability in the taenia coli of the guinea-pig. J Physiol 1958; 143: 165-182.
11. Burnstock G: The action of adrenaline on excitability and membrane potential in the taenia coli of the guinea-pig and the effect of DNP on this action and on the action of acetylcholine. J Physiol 1958; 143: 183-194.
12. Burnstock G, Campbell G, Bennett M, Holman ME: Innervation of the guinea-pig taenia coli: are there intrinsic inhibitory nerves which are distinct from sympathetic nerves? Int J Neuropharma-col 1964; 3: 163-166.
13. Burnstock G, Campbell G, Rand MJ: The inhibitory innervation of the taenia of the guinea-pig caecum. J Physiol 1966; 182: 504-526.
14. Drury AN, Szent-Györgyi A: The physiological activity of ad-enine compounds with special reference to their action upon the mammalian heart. J Physiol 1929; 68: 213-237.
15. Holton P: The liberation of adenosine triphosphate on antidrom-ic stimulation of sensory nerves. J Physiol 1959; 145: 494-504.
16. Burnstock G, Campbell G, Satchell D, Smythe A: Evidence that adenosine triphosphate or a related nucleotide is the transmitter substance released by non-adrenergic inhibitory nerves in the gut. Br J Pharmacol 1970; 40: 668-688.
17. Burnstock G, Dumsday B, Smythe A: Atropine resistant excitation of the urinary bladder: the possibility of transmission via nerves releasing a purine nucleotide. Br J Pharmacol 1972; 44: 451-461.
18. Burnstock G: Purinergic nerves. Pharmacol Rev 1972; 24: 509-581.
19. Burnstock G: Historical review: ATP as a neurotransmitter. Trends Pharmacol Sci 2006; 27: 166-176.
20. Burnstock G: The Gaddum Lecture. Discovery of purinergic signalling, the initial resistance and current explosion of interest. Br J Pharmacol 2012; 167: 238-255.
21. 3H]adenosine triphosphate: release during stimulation of enteric nerves. Science 1971; 173: 336-338.
22. Nakanishi H, Takeda H: The possible role of adenosine triphos-phate in chemical transmission between the hypogastric nerve terminal and seminal vesicle in the guinea-pig. Jpn J Pharmacol 1973; 23: 479-490.
23. Langer SZ, Pinto JE: Possible involvement of a transmitter different from norepinephrine in residual responses to nerve stimulation of cat nictitating membrane after pretreatment with reser-pine. J Pharmacol Exp Ther 1976; 196: 697-713.
24. Burnstock G: Do some nerve cells release more than one transmitter? Neuroscience 1976; 1: 239-248.
25. Burnstock G, Holman ME: Autonomic nerve-smooth muscle transmission. Nature 1960; 187: 951-952.
26. Burnstock G, Holman ME: The transmission of excitation from autonomic nerve to smooth muscle. J Physiol 1961; 155: 115-133.
27. Sneddon P, Burnstock G: Inhibition of excitatory junction potentials in guinea-pig vas deferens by α,β-methylene-ATP: further evidence for ATP and noradrenaline as cotransmitters. Eur J Pharmacol 1984; 100: 85-90.
28. Westfall DP, Stitzel RE, Rowe JN: The postjunctional effects and neural release of purine compounds in the guinea-pig vas defer-ens. Eur J Pharmacol 1978; 50: 27-38.
29. Burnstock G, Cocks T, Crowe R, Kasakov L: Purinergic innerva-tion of the guinea-pig urinary bladder. Br J Pharmacol 1978; 63: 125-138.
30. Burnstock G: Cotransmission; in: Robertson D, Biaggioni I, Burnstock G, Low P, Paton JF, eds, Primer of the Autonomic Nervous System 3rd Edition. Oxford, Academic Press, 2012; 27-34.
31. Burnstock G: A basis for distinguishing two types of purinergic receptor; in: Straub RW, Bolis L, eds, Cell Membrane Receptors for Drugs and Hormones: A Multidisciplinary Approach. New York, Raven Press, 1978; 107-118.
32. Burnstock G, Kennedy C: Is there a basis for distinguishing two types of P2-purinoceptor? Gen Pharmacol 1985; 16: 433-440.
33. Daly JW: Adenosine receptors. Adv Cyclic Nucleotide Protein Phosphorylation Res 1985; 19: 29-46.
34. Fredholm BB, IJzerman AP, Jacobson KA, Klotz KN, Linden J: International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 2001; 53: 527-552.
35. Webb TE, Simon J, Krishek BJ, Bateson AN, Smart TG, King BF, Burnstock G, Barnard EA: Cloning and functional expression of a brain G-protein-coupled ATP receptor. FEBS Lett 1993; 324: 219-225.
36. Lustig KD, Shiau AK, Brake AJ, Julius D: Expression cloning of an ATP receptor from mouse neuroblastoma cells. Proc Natl Acad Sci USA 1993; 90: 5113-5117.
37. Brake AJ, Wagenbach MJ, Julius D: New structural motif for ligand-gated ion channels defned by an ionotropic ATP receptor. Nature 1994; 371: 519-523.
38. Valera S, Hussy N, Evans RJ, Adani N, North RA, Surprenant A, Buell G: A new class of ligand-gated ion channel defined by P2X receptor for extra-cellular ATP. Nature 1994; 371: 516-519.
39. Abbracchio MP, Burnstock G: Purinoceptors: are there families of P2X and P2Y purinoceptors? Pharmacol Ther 1994; 64: 445-475.
40. Kawate T, Michel JC, Birdsong WT, Gouaux E: Crystal structure of the ATP-gated P2X4 ion channel in the closed state. Nature 2009; 460: 592-598.
41. Burnstock G, Knight GE: Cellular distribution and functions of P2 receptor subtypes in different systems. Int Rev Cytol 2004; 240: 31-304.
42. Burnstock G, Verkhratsky A: Evolutionary origins of the puri-nergic signalling system. Acta Physiol (Oxf) 2009; 195: 415-447.
43. Evans RJ, Derkach V, Surprenant A: ATP mediates fast synaptic transmission in mammalian neurons. Nature 1992; 357: 503-505.
44. Silinsky EM, Gerzanich V, Vanner SM: ATP mediates excitatory synaptic transmission in mammalian neurones. Br J Pharmacol 1992; 106: 762-763.
45. Edwards FA, Gibb AJ, Colquhoun D: ATP receptor-mediated synaptic currents in the central nervous system. Nature 1992; 359: 144-147.
46. Burnstock G, Verkhratsky A: Long-term (trophic) purinergic signalling: purinoceptors control cell proliferation, differentiation and death. Cell Death Dis 2010; 1: e9.
47. Burnstock G: Purinergic signalling and vascular cell proliferation and death. Arterioscler Thromb Vasc Biol 2002; 22: 364-373.
48. Orriss IR, Burnstock G, Arnett TR: Purinergic signalling and bone remodelling. Curr Opin Pharmacol 2010; 10: 322-330.
49. White N, Burnstock G: P2 receptors and cancer. Trends Pharmacol Sci 2006; 27: 211-217.
50. Schäfer KH, Saffrey MJ, Burnstock G: Trophic actions of 2-chlo-roadenosine and bFGF on cultured myenteric neurones. Neurore-port 1995; 6: 937-941.
51. Burnstock G, Ulrich H: Purinergic signalling in embryonic and stem cell development. Cell Mol Life Sci 2011; 68: 1369-1394.
52. Ulrich H, Abbracchio MP, Burnstock G: Extrinsic purinergic regulation of neural stem/progenitor cells: implications for CNS development and repair. Stem Cell Rev 2012; 8: 755-767.
53. Bodin P, Burnstock G: Purinergic signalling: ATP release. Neuro-chem Res 2001; 26: 959-969.
54. Lazarowski ER: Vesicular and conductive mechanisms of nu-cleotide release. Purinergic Signal 2012; 8: 359-373.
55. Burnstock G: Release of vasoactive substances from endothelial cells by shear stress and purinergic mechanosensory transduc-tion. J Anat 1999; 194: 335-342.
56. Burnstock G: Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 2007; 87: 659-797.
57. Zimmermann H: Nucleotide signaling in nervous system development. Pfugers Arch 2006; 452: 573-588.
58. Yegutkin GG: Nucleotide- and nucleoside-converting ectoen-zymes: Important modulators of purinergic signalling cascade. Biochim Biophys Acta 2008; 1783: 673-694.
59. MacKenzie I, Burnstock G, Dolly JO: The effects of purifed botulinum neurotoxin type A on cholinergic, adrenergic and non-adrenergic, atropine-resistant autonomic neuromuscular transmission. Neuroscience 1982; 7: 997-1006.
60. Chancellor MB, Fowler CJ, Apostolidis A, de Groat WC, Smith CP, Somogyi GT, Aoki KR: Drug Insight: biological effects of botulinum toxin A in the lower urinary tract. Nat Clin Pract Urol 2008; 5: 319-328.
61. Gachet C: Regulation of platelet functions by P2 receptors. Annu Rev Pharmacol Toxicol 2006; 46: 277-300.
62. Ahmad S, Storey RF: Development and clinical use of prasugrel and ticagrelor. Curr Pharm Des 2012; 18: 5240-5260.
63. Hou M, Malmsjö M, Möller S, Pantev E, Bergdahl A, Zhao XH, Sun XY, Hedner T, Edvinsson L, Erlinge D: Increase in cardiac P2X1- and P2Y2-receptor mRNA levels in congestive heart failure. Life Sci 1999; 65: 1195-1206.
64. Coutinho-Silva R, Parsons M, Robson T, Lincoln J, Burnstock G: P2X and P2Y purinoceptor expression in pancreas from strepto-zotocin-diabetic rats. Mol Cell Endocrinol 2003; 204: 141-154.
65. Burnstock G, Novak I: Purinergic signalling and diabetes. Puri-nergic Signalling 2013 (Epub ahead of print 3/4/13).
66. Agrawal A, Buckley KA, Bowers K, Furber M, Gallagher JA, Gartland A: The effects of P2X7 receptor antagonists on the formation and function of human osteoclasts in vitro. Purinergic Signal 2010; 6: 307-315.
67. Vonend O, Turner C, Chan CM, Loesch A, Dell'Anna GC, Srai SK, Burnstock G, Unwin R: Glomerular expression of the ATP-sensitive P2X7 receptor in diabetic and hypertensive rat models. Kidney Int 2004; 66: 157-166.
68. Bailey MA, Shirley DG, King BF, Burnstock G, Unwin RJ: Extracellular nucleotides and renal function. in: Alpern RJ, Herbert SCG, eds, The Kidney: Physiology and Pathophysiology, San Diego, Elsevier, 2007; 425-443.
69. Taylor SR, Turner CM, Elliott JI: P2X7 defciency attenuates renal injury in experimental glomerulonephritis. J Am Soc Nephrol 2009; 20: 1275-1281.
70. Faria M, Timóteo MA, Lafuente-de-Carvalho M, Correia-de-Sá P: P2 Purinoceptor subtype changes in patients with vasculogenic erectile dysfunction. Purinergic Signal 2010; 6: S115.
71. Hupertan V, Neuzillet Y, Stücker O, Pons C, Leammel E, Lebret T: Effects of nucleotides adenosine monophosphate and adenos-ine triphosphate in combination with L-arginine on male rabbit corpus cavernosum tissue. Int J Androl 2012; 35: 860-866.
72. Wen J, Xia Y: Adenosine signaling: good or bad in erectile function? Arterioscler Thromb Vasc Biol 2012; 32: 845-850.
73. Rossato M, La Sala GB, Balasini M, Taricco F, Galeazzi C, Ferlin A, Foresta C: Sperm treatment with extracellular ATP increases fertilization rates in in-vitro fertilization for male factor infertility. Hum Reprod 1999; 14: 694-697.
74. Vasudevan K, Sztein JM: Treatment of sperm with extracellular adenosine 5′-triphosphate improves the in vitro fertility rate of inbred and genetically modifed mice with low fertility. Therio-genology 2011; 76: 729-736.
75. Burnstock G: The journey to establish purinergic signalling in the gut. Neurogastroenterol Motil 2008; 20: 8-19.
76. Burnstock G: Commentary. Purinergic receptors as future targets for treatment of functional GI disorders. Gut 2008; 57: 119 3-1194.
77. Yiangou Y, Facer P, Baecker PA, Ford AP, Knowles CH, Chan CL, Williams NS, Anand P: ATP-gated ion channel P2X3 is increased in human infammatory bowel disease. Neurogastroenterol Motil 2001; 13: 365-369.
78. Yerxa BR: Therapeutic use of nucleotides in respiratory and ophthalmic diseases. Drug Dev Res 2001; 52: 196-201.
79. Brouns I, Adriaensen D, Burnstock G, Timmermans JP: Intraepi-thelial vagal sensory nerve terminals in rat pulmonary neuroepi-thelial bodies express P2X3 receptors. Am J Respir Cell Mol Biol 2000; 23: 52-61.
80. Brouns I, Van Genechten J, Burnstock G, Timmermans JP, Adri-aensen D: Ontogenesis of P2X3 receptor-expressing nerve fbres in the rat lung, with special reference to neuroepithelial bodies. Biomed Res 2003; 14: 80-86.
81. Séror C, Melki MT, Subra F, Raza SQ, Bras M, Saïdi H, Nardacci R, Voisin L, Paoletti A, Law F, Martins I, Amendola A, Abdul-Sater AA, Ciccosanti F, Delelis O, Niedergang F, Thierry S, Said-Sadier N, Lamaze C, Métivier D, Estaquier J, Fimia GM, Falasca L, Casetti R, Modjtahedi N, Kanellopoulos J, Mouscadet JF, Oj-cius DM, Piacentini M, Gougeon ML, Kroemer G, Perfettini JL: Extracellular ATP acts on P2Y2 purinergic receptors to facilitate HIV-1 infection. J Exp Med 2011; 208: 1823-1834.
82. Wagner MC: The therapeutic potential of adenosine triphosphate as an immune modulator in the treatment of HIV/AIDS: a combination approach with HAART. Curr HIV Res 2011; 9: 209-222.
83. Narayanan A, Sampey G, Van Duyne R, Guendel I, Kehn-Hall K, Roman J, Currer R, Galons H, Oumata N, Joseph B, Meijer L, Caputi M, Nekhai S, Kashanchi F: Use of ATP analogs to inhibit HIV-1 transcription. Virology 2012; 432: 219-231.
84. Burnstock G: A unifying purinergic hypothesis for the initiation of pain. Lancet 1996; 347: 1604-1605.
85. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN: A P2X purinoceptor expressed by a subset of sensory neurons. Nature 1995; 377: 428-431.
86. Burnstock G: Purinergic mechanosensory transduction and visceral pain. Mol Pain 2009; 5: 69.
87. Burnstock G: Targeting the visceral purinergic system for pain control. Curr Opin Pharmacol 2012; 12: 80-86.
88. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K: Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004; 45: 89-95.
89. Trang T, Salter MW: P2X4 purinoceptor signaling in chronic pain. Purinergic Signal 2012; 8: 621-628.
90. Al-Shukaili A, Al-Kaabi J, Hassan B: A comparative study of interleukin-1β production and P2X7 expression after ATP stimulation by peripheral blood mononuclear cells isolated from rheumatoid arthritis patients and normal healthy controls. Infamma-tion 2008; 31: 84-90.
91. Varani K, De Mattei M, Vincenzi F, Tosi A, Targa M, Masieri FF, Pellati A, Massari L, Borea PA: P2X1 and P2X3 purinergic receptors differentially modulate the infammatory response in human osteoarthritic synovial fibroblasts. Cell Physiol Biochem 2010; 25: 325-336.
92. Burnstock G: Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 2008; 7: 575-590.
93. Burnstock G, Krügel U, Abbracchio MP, Illes P: Purinergic signalling: from normal behaviour to pathological brain function. Prog Neurobiol 2011; 95: 229-274.
94. Rapaport E: Treatment of human tumor cells with ADP or ATP yields arrest of growth in the S phase of the cell cycle. J Cell Physiol 1983; 114: 279-283.
95. Burnstock G: Acupuncture: a novel hypothesis for the involvement of purinergic signalling. Med Hypotheses 2009; 73: 470-472.
96. Baqi Y, Lee SY, Iqbal J, Ripphausen P, Lehr A, Scheiff AB, Zim-mermann H, Bajorath J, Müller CE: Development of potent and selective inhibitors of ecto-5′-nucleotidase based on an anthra-quinone scaffold. J Med Chem 2010; 53: 2076-2086.
97. Gever JR, Soto R, Henningsen RA, Martin RS, Hackos DH, Pan-icker S, Rubas W, Oglesby IB, Dillon MP, Milla ME, Burnstock G, Ford AP: AF-353, a novel, potent orally bioavailable P2X3/ P2X2/3 receptor antagonist. Br J Pharmacol 2010; 160: 1387-1398.
98. Burnstock G: The changing face of autonomic neurotransmission. (The First von Euler Lecture in Physiology). Acta Physiol Scand 1986; 126: 67-91.
99. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H: Purinergic signalling in the nervous system: an overview. Trends Neurosci 2009; 32: 19-29.
100. Burnstock G: Noradrenaline and ATP as cotransmitters in sympathetic nerves. Neurochem Int 1990; 17: 357-368.
101. Hoyle CH: Purinergic cotransmission: parasympathetic and enteric nerves. Semin Neurosci 1996; 8: 207-215.
102. Burnstock G: Introduction: Changing face of autonomic and sensory nerves in the circulation. in: Edvinsson L, Uddman R, eds, Vascular Innervation and Receptor mechanisms: New Perspectives, San Diego, Academic Press Inc, 1993; 1-22.
103. Belai A, Burnstock G: Evidence for coexistence of ATP and nitric oxide in non-adrenergic, non-cholinergic (NANC) inhibitory neurones in the rat ileum, colon and anococcygeus muscle. Cell Tissue Res 1994; 278: 197-200.
104. Burnstock G: Purinergic signalling in gut; in. Abbracchio MP, Williams M, eds, Handbook of Experimental Pharmacology, Volume 151/II. Purinergic and Pyrimidinergic Signalling II - Cardiovascular, Respiratory, Immune, Metabolic and Gastrointestinal Tract Function. Handbook of Experimental Pharmacology, Berlin, Springer-Verlag, 2001. vol 151/II, 141-238.
105. Silinsky EM, Hubbard JI: Release of ATP from rat motor nerve terminals. Nature 1973; 243: 404-405.
106. Henning RH: Purinoceptors in neuromuscular transmission. Pharmacol Ther 1997; 74: 115-128.
107. Richardson PJ, Brown SJ: ATP release from affnity-purifed rat cholinergic nerve terminals. J Neurochem 1987; 48: 622-630.
108. 3H]noradrenaline from rat hypothalamic slices: origin and modulation by α2-adrenoceptors. Neuroscience 1998; 82: 511-520.
109. Poelchen W, Sieler D, Wirkner K, Illes P: Co-transmitter function of ATP in central catecholaminergic neurons of the rat. Neuroscience 2001; 102: 593-602.
110. Jo YH, Role LW: Cholinergic modulation of purinergic and GAB-Aergic co-transmission at in vitro hypothalamic synapses. J Neu-rophysiol 2002; 88: 2501-2508.
111. Krügel U, Schraft T, Kittner H, Kiess W, Illes P: Basal and feeding-evoked dopamine release in the rat nucleus accumbens is depressed by leptin. Eur J Pharmacol 2003; 482: 185-187.
112. Mori M, Heuss C, Gahwiler BH, Gerber U: Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J Physiol 2001; 535: 115-123.
113. Fujii S, Sasaki H, Mikoshiba K, Kuroda Y, Yamazaki Y, Mostafa TA, Kato H: A chemical LTP induced by co-activation of metabo-tropic and N-methyl-D-aspartate glutamate receptors in hippocampal CA1 neurons. Brain Res 2004; 999: 20-28.