Biology of purinergic signalling: Its ancient evolutionary roots, its omnipresence and its multiple functional significance

BioEssays

Volumn 36, Issue 7, 2014, Pages 697-705

  Verkhratsky, Alexei ^a,b,c   Burnstock, Geoffrey ^d,e  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b BASQUE FOUNDATION FOR SCIENCE   (Spain)

^c LOBACHEVSKY STATE UNIVERSITY OF NIZHNY NOVGOROD   (Russian Federation)

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

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Adenosine; ATP; Evolution; P1 receptors; P2X receptor; P2Y receptor; Purinoceptors

Indexed keywords

ACID PHOSPHATASE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; NUCLEOSIDE TRIPHOSPHATE; NUCLEOTIDE PYROPHOSPHATASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; PURINERGIC P2X RECEPTOR; REACTIVE OXYGEN METABOLITE; SEA WATER; URIDINE DIPHOSPHATE; URIDINE TRIPHOSPHATE; PURINERGIC RECEPTOR; PURINERGIC RECEPTOR STIMULATING AGENT;

ACTIVE TRANSPORT; ARTICLE; BACTERIAL GROWTH; CARDIOVASCULAR SYSTEM; CELL COMMUNICATION; CELL DIFFERENTIATION; CENTRAL NERVOUS SYSTEM; CHROMOBACTERIUM VIOLACEUM; DICTYOSTELIUM DISCOIDEUM; ENZYMATIC DEGRADATION; ENZYME RELEASE; GASTROINTESTINAL TRACT; GENE EXPRESSION; INVERTEBRATE; MOLECULAR EVOLUTION; NEMATOSTELLA VECTENSIS; NONHUMAN; OSSIFICATION; PARAMECIUM; PRESYNAPTIC INHIBITION; PROTEIN FUNCTION; PURINERGIC SIGNALLING; SIGNAL TRANSDUCTION; STREPTOMYCES COELICOLOR; TETRAHYMENA; ANIMAL; EVOLUTION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

ADENOSINE TRIPHOSPHATE; ANIMALS; BIOLOGICAL EVOLUTION; HUMANS; PURINERGIC AGONISTS; RECEPTORS, PURINERGIC; SIGNAL TRANSDUCTION;

EID: 84901841296     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201400024     Document Type: Article

References (93)

1. Brocks JJ, Logan GA, Buick R, Summons RE. 1999. Archean molecular fossils and the early rise of eukaryotes. Science 285: 1033-6.
2. Pflug HD. 1982. Early diversification of life in the Archean. Zbl Bakt Hyg I Abt Orig C3: 611-5.
3. Woese C. 1998. The universal ancestor. Proc Natl Acad Sci USA 95: 6854-9.
4. Forterre P, Philippe H. 1999. Where is the root of the universal tree of life? BioEssays 21: 871-9.
5. Di Giulio M. 2011. The last universal common ancestor (LUCA) and the ancestors of archaea and bacteria were progenotes. J Mol Evol 72: 119-26.
6. Nury H, Bocquet N, Le Poupon C, Raynal B, et al. 2010. Crystal structure of the extracellular domain of a bacterial ligand-gated ion channel. J Mol Biol 395: 1114-27.
7. Corringer PJ, Baaden M, Bocquet N, Delarue M, et al. 2010. Atomic structure and dynamics of pentameric ligand-gated ion channels: new insight from bacterial homologues. J Physiol 588: 565-72.
8. Chiu J, DeSalle R, Lam HM, Meisel L, et al. 1999. Molecular evolution of glutamate receptors: a primitive signaling mechanism that existed before plants and animals diverged. Mol Biol Evol 16: 826-38.
9. Chen GQ, Cui C, Mayer ML, Gouaux E. 1999. Functional characterization of a potassium-selective prokaryotic glutamate receptor. Nature 402: 817-21.
10. Ger MF, Rendon G, Tilson JL, Jakobsson E. 2010. Domain-based identification and analysis of glutamate receptor ion channels and their relatives in prokaryotes. PLoS One 5: e12827.
11. Hoyle CH. 2011. Evolution of neuronal signalling: transmitters and receptors. Auton Neurosci 165: 28-53.
12. Bryant DE, Greenfield D, Walshaw RD, Johnson BRG, et al. 2013. Hydrothermal modification of the Sikhote-Alin iron meteorite under low pH geothermal environments. A plausibly prebiotic route to activated phosphorus on the early Earth. Geochim Cosmochim Acta 109: 90-112.
13. Ponnamperuma C, Sagan C, Mariner R. 1963. Synthesis of adenosine triphosphate under possible primitive earth conditions. Nature 199: 222-6.
14. Galimov EM. 2009. Concept of sustained ordering and an ATP-related mechanism of life's origin. Int J Mol Sci 10: 2019-30.
15. Kazmierczak J, Kempe S, Kremer B. 2013. Calcium in the early evolution of living systems: a biohistorical approach. Curr Organic Chem 17: 1738-50.
16. Burnstock G, Verkhratsky A. 2012. Purinergic Signalling and the Nervous System. Heidelberg: Springer.
17. Naseem R, Wann KT, Holland IB, Campbell AK. 2009. ATP regulates calcium efflux and growth in E. coli. J Mol Biol 391: 42-56.
18. Li M, Kim TJ, Kwon HJ, Suh JW. 2008. Effects of extracellular ATP on the physiology of Streptomyces coelicolor A3(2). FEMS Microbiol Lett 286: 24-31.
19. Choi SB, Kim JU, Joo H, Min CK. 2010. Identification and characterization of a novel bacterial ATP-sensitive K+ channel. J Microbiol 48: 325-30.
20. Ivanova EP, Alexeeva YV, Pham DK, Wright JP, et al. 2006. ATP level variations in heterotrophic bacteria during attachment on hydrophilic and hydrophobic surfaces. Int Microbiol 9: 37-46.
21. Roux SJ, Steinebrunner I. 2007. Extracellular ATP: an unexpected role as a signaler in plants. Trends Plant Sci 12: 522-7.
22. Watson GM, Venable S, Hudson RR, Repass JJ. 1999. ATP enhances repair of hair bundles in sea anemones. Hear Res 136: 1-12.
23. Gounaris K, Selkirk ME. 2005. Parasite nucleotide-metabolizing enzymes and host purinergic signalling. Trends Parasitol 21: 17-21.
24. Gruenhagen JA, Lovell P, Moroz LL, Yeung ES. 2004. Monitoring real-time release of ATP from the molluscan central nervous system. J Neurosci Methods 139: 145-52.
25. Chen C-H, Chen J-H. 2007. Adenosine receptor-like molecules and related signaling transduction pathways regulate hemocyte adhesion in abalone (Haliotis diversicolor). FASEB J 21: 872-7.
26. Backus KH, Braum S, Lohner F, Deitmer JW. 1994. Neuronal responses to purinoceptor agonists in the leech central nervous system. J Neurobiol 25: 1283-92.
27. Yoshimura A, Nakano I, Shingyoji C. 2007. Inhibition by ATP and activation by ADP in the regulation of flagellar movement in sea urchin sperm. Cell Motil Cytoskel 64: 777-93.
28. Zimmer-Faust RK. 1993. ATP: a potent prey attractant evoking carnivory. Limnol Oceanogr 38: 1271-5.
29. Galun R, Kabayo JP. 1988. Gorging response of Glossina palpalis palpalis to ATP analogues. Physiol Entomol 13: 419-23.
30. Burnstock G. 1996. Purinoceptors: ontogeny and phylogeny. Drug Dev Res 39: 204-42.
31. Burnstock G, Verkhratsky A. 2009. Evolutionary origins of the purinergic signalling system. Acta Physiol (Oxf) 195: 415-47.
32. Mulkidjanian AY, Galperin MY, Koonin EV. 2009. Co-evolution of primordial membranes and membrane proteins. Trends Biochem Sci 34: 206-15.
33. Bodin P, Burnstock G. 2001. Purinergic signalling: ATP release. Neurochem Res 26: 959-69.
34. Lazarowski ER, Sesma JI, Seminario-Vidal L, Kreda SM. 2011. Molecular mechanisms of purine and pyrimidine nucleotide release. Adv Pharmacol 61: 221-61.
35. Parpura V, Scemes E, Spray DC. 2004. Mechanisms of glutamate release from astrocytes: gap junction "hemichannels", purinergic receptors and exocytotic release. Neurochem. Int. 45: 259-64.
36. Fields RD. 2011. Nonsynaptic and nonvesicular ATP release from neurons and relevance to neuron-glia signaling. Semin Cell Dev Biol 22: 214-9.
37. Sabirov RZ, Dutta AK, Okada Y. 2001. Volume-dependent ATP-conductive large-conductance anion channel as a pathway for swelling-induced ATP release. J Gen Physiol 118: 251-66.
38. Suadicani SO, Brosnan CF, Scemes E. 2006. P2X7 receptors mediate ATP release and amplification of astrocytic intercellular Ca2+ signaling. J Neurosci 26: 1378-85.
39. Samuels SE, Lipitz JB, Dahl G, Muller KJ. 2010. Neuroglial ATP release through innexin channels controls microglial cell movement to a nerve injury. J Gen Physiol 136: 425-42.
40. Samuels SE, Lipitz JB, Wang J, Dahl G, et al. 2013. Arachidonic acid closes innexin/pannexin channels and thereby inhibits microglia cell movement to a nerve injury. Dev Neurobiol 73: 621-31.
41. Sauvage V, Aubert D, Escotte-Binet S, Villena I. 2009. The role of ATP-binding cassette (ABC) proteins in protozoan parasites. Mol Biochem Parasitol 167: 81-94.
42. Pankratov Y, Lalo U, Verkhratsky A, North RA. 2006. Vesicular release of ATP at central synapses. Pflugers Arch 452: 589-97.
43. Sawada K, Echigo N, Juge N, Miyaji T, et al. 2008. Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 105: 5683-6.
44. Sreedharan S, Shaik JH, Olszewski PK, Levine AS, et al. 2010. Glutamate, aspartate and nucleotide transporters in the SLC17 family form four main phylogenetic clusters: evolution and tissue expression. BMC Genomics 11: 17.
45. Zhang Z, Chen G, Zhou W, Song A, et al. 2007. Regulated ATP release from astrocytes through lysosome exocytosis. Nat Cell Biol 9: 945-53.
46. Sesma JI, Esther CR Jr, Kreda SM, Jones L, et al. 2009. Endoplasmic reticulum/golgi nucleotide sugar transporters contribute to the cellular release of UDP-sugar signaling molecules. J Biol Chem 284: 12572-83.
47. Ralevic V, Burnstock G. 1998. Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-92.
48. Thimm D, Knospe M, Abdelrahman A, Moutinho M, et al. 2013. Characterization of new G protein-coupled adenine receptors in mouse and hamster. Purinergic Signal 9: 415-26.
49. Meima M, Schaap P. 1999. Dictyostelium development-socializing through cAMP. Semin Cell Dev Biol 10: 567-76.
50. Mustard JA. 2014. The buzz on caffeine in invertebrates: effects on behavior and molecular mechanisms. Cell Mol Life Sci 71: 1375-82.
51. Kukulski F, Levesque SA, Sevigny J. 2011. Impact of ectoenzymes on p2 and p1 receptor signaling. Adv Pharmacol 61: 263-99.
52. Millan JL. 2006. Alkaline phosphatases: structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal 2: 335-41.
53. Zimmermann H. 2006. Ectonucleotidases in the nervous system. In Novartis Foundation Symposium 276: Purinergic Signalling in Neuron-Glial Interactions. Chichester: John Wiley & Sons. p. 113-28.
54. Yegutkin GG. 2008. Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783: 673-94.
55. Vivian JP, Riedmaier P, Ge H, Le Nours J, et al. 2010. Crystal structure of a Legionella pneumophila ecto -triphosphate diphosphohydrolase, a structural and functional homolog of the eukaryotic NTPDases. Structure 18: 228-38.
56. Zimmermann H, Zebisch M, Strater N. 2012. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8: 437-502.
57. Burnstock G, Verkhratsky A. 2010. Long-term (trophic) purinergic signalling: purinoceptors control cell proliferation, differentiation and death. Cell Death Dis 1: e9.
58. Di Virgilio F, Ceruti S, Bramanti P, Abbracchio MP. 2009. Purinergic signalling in inflammation of the central nervous system. Trends Neurosci 32: 79-87.
59. Burnstock G. 2009. Purinergic receptors and pain. Curr Pharm Des 15: 1717-35.
60. Inoue K, Tsuda M. 2009. Microglia and neuropathic pain. Glia 57: 1469-79.
61. Di Virgilio F. 2007. Liaisons dangereuses: P2X7 and the inflammasome. Trends Pharmacol Sci 28: 465-72.
62. Li L, Lundkvist A, Andersson D, Wilhelmsson U, et al. 2008. Protective role of reactive astrocytes in brain ischemia. J Cereb Blood Flow Metab 28: 468-81.
63. Sofroniew MV. 2009. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci 32: 638-47.
64. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H. 2009. Purinergic signalling in the nervous system: an overview. Trends Neurosci 32: 19-29.
65. Burnstock G, Fredholm BB, Verkhratsky A. 2011. Adenosine and ATP receptors in the brain. Curr Top Med Chem 11: 973-1011.
66. Franke H, Verkhratsky A, Burnstock G, Illes P. 2012. Pathophysiology of astroglial purinergic signalling. Purinergic Signal 8: 629-57.
67. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. 2011. Physiology of microglia. Physiol Rev 91: 461-553.
68. Burnstock G. 2008. Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7: 575-90.
69. Burnstock G. 2006. Vessel tone and remodeling. Nat Med 12: 16-7.
70. Burnstock G. 2009. Purinergic regulation of vascular tone and remodelling. Auton Autacoid Pharmacol 29: 63-72.
71. Burnstock G, Ralevic V. 2014. Purinergic signaling and blood vessels in health and disease. Pharmacol Rev 66: 102-92.
72. Burnstock G. 2013. Purinergic signalling in the reproductive system in health and disease. Purinergic Signal 10: 147-87.
73. Burnstock G. 2008. The journey to establish purinergic signalling in the gut. Neurogastroenterol Motil 20: 8-19.
74. Burnstock G. 2013. Purinergic signalling in the gastrointestinal tract and related organs in health and disease. Purinergic Signal 10: 3-50.
75. Burnstock G, Arnett TR, Orriss IR. 2013. Purinergic signalling in the musculoskeletal system. Purinergic Signal 9: 541-72.
76. Grol MW, Panupinthu N, Korcok J, Sims SM, et al. 2009. Expression, signaling, and function of P2X7 receptors in bone. Purinergic Signal 5: 205-21.
77. Burnstock G, Brouns I, Adriaensen D, Timmermans JP. 2012. Purinergic signaling in the airways. Pharmacol Rev 64: 834-68.
78. Burnstock G, Knight GE, Greig AV. 2012. Purinergic signaling in healthy and diseased skin. J Invest Dermatol 132: 526-46.
79. Burnstock G, Novak I. 2012. Purinergic signalling in the pancreas in health and disease. J Endocrinol 213: 123-41.
80. Burnstock G, Evans LC, Bailey MA. 2013. Purinergic signalling in the kidney in health and disease. Purinergic Signal 10: 71-101.
81. Burnstock G. 2013. Purinergic signalling in endocrine organs. Purinergic Signal 10: 189-231.
82. Burnstock G. 2013. Purinergic signalling in the urinary tract in health and disease. Purinergic Signal 10: 103-55.
83. Burnstock G, Vaughn B, Robson SC. 2013. Purinergic signalling in the liver in health and disease. Purinergic Signal 10: 51-70.
84. Baines A, Parkinson K, Sim JA, Bragg L, et al. 2013. Functional properties of five Dictyostelium discoideum P2X receptors. J Biol Chem 288: 20992-1000.
85. Fountain SJ, Parkinson K, Young MT, Cao L, et al. 2007. An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 448: 200-3.
86. Ludlow MJ, Traynor D, Fisher PR, Ennion SJ. 2008. Purinergic-mediated Ca2+ influx in Dictyostelium discoideum. Cell Calcium 44: 567-79.
87. Fountain SJ, Cao L, Young MT, North RA. 2008. Permeation properties of a P2X receptor in the green algae Ostreococcus tauri. J Biol Chem 283: 15122-6.
88. Fountain SJ. 2013. Primitive ATP-activated P2X receptors: discovery, function and pharmacology. Front Cell Neurosci 7: 247.
89. Agboh KC, Webb TE, Evans RJ, Ennion SJ. 2004. Functional characterization of a P2X receptor from Schistosoma mansoni. J Biol Chem 279: 41650-7.
90. Raouf R, Blais D, Seguela P. 2005. High zinc sensitivity and pore formation in an invertebrate P2X receptor. Biochim Biophys Acta 1669: 135-41.
91. Bavan S, Straub VA, Blaxter ML, Ennion SJ. 2009. A P2X receptor from the tardigrade species Hypsibius dujardini with fast kinetics and sensitivity to zinc and copper. BMC Evol Biol 9: 17.
92. Bavan S, Straub VA, Webb TE, Ennion SJ. 2012. Cloning and characterization of a P2X receptor expressed in the central nervous system of Lymnaea stagnalis. PLoS One 7: e50487.
93. Sakurai T, Lee H, Kashima M, Saito Y, et al. 2012. The planarian P2X homolog in the regulation of asexual reproduction. Int J Dev Biol 56: 173-82.