Purines as potential morphogens during embryonic development

Purinergic Signalling

Volumn 8, Issue 3, 2012, Pages 503-521

  Massé, Karine ^a   Dale, Nicholas ^b  

^a CNRS Bordeaux Segalen University   (France)

^b UNIVERSITY OF WARWICK   (United Kingdom)

Author keywords

Adenosine; ADP; ATP; Embryogenesis; Gastrulation; Morphogen; Neurulation; Organogenesis

Indexed keywords

ADENOSINE; ADENOSINE DEAMINASE; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ECTO 5' NUCLEOTIDASE; MORPHOGEN; PURINE DERIVATIVE; PURINERGIC RECEPTOR; RETINOIC ACID;

ANIMAL EMBRYO; ARTICLE; BIOLOGICAL MODEL; BLASTOCYST; EMBRYO DEVELOPMENT; EMBRYO GROWTH; GASTRULATION; GENE EXPRESSION; GENETIC MANIPULATION; HUMAN; LIFE CYCLE STAGE; MORPHOGENESIS; NEURULATION; NONHUMAN; OOCYTE CLEAVAGE; ORGANOGENESIS; PHENOTYPE; PROTEIN EXPRESSION; RECEPTOR GENE; SIGNAL TRANSDUCTION; VERTEBRATE;

ADENOSINE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; MICE; MODELS, BIOLOGICAL; PREGNANCY; PURINES; RECEPTORS, PURINERGIC; SIGNAL TRANSDUCTION; XENOPUS LAEVIS; ZEBRAFISH;

EID: 84861526979     PISSN: 15739538     EISSN: 15739546     Source Type: Journal    
DOI: 10.1007/s11302-012-9290-y     Document Type: Article

References (150)

1. Burnstock G (1997) The past, present and future of purine nucleotides as signalling molecules. Neuropharmacology 36: 1127-1139.
2. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32: 19-29.
3. Khakh BS, Burnstock G, Kennedy C, King BF, North RA, Seguela P, Voigt M, Humphrey PP (2001) International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol Rev 53: 107-118.
4. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL, Kennedy C, Knight GE, Fumagalli M, Gachet C, Jacobson KA, Weisman GA (2006) International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58: 281-341.
5. Fredholm BB, IJzerman AP, Jacobson KA, Klotz KN, Linden J (2001) International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 53: 527-552.
6. Zimmermann H (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol 362: 299-309.
7. Yegutkin GG (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783: 673-694.
8. Zimmermann H (2006) Nucleotide signaling in nervous system development. Pflugers Arch 452: 573-588.
9. Dale N (2008) Dynamic ATP signalling and neural development. J Physiol 586: 2429-2436.
10. Burnstock G, Ulrich H (2011) Purinergic signaling in embryonic and stem cell development. Cell Mol Life Sci 68: 1369-1394.
11. Hellsten U, Harland RM, Gilchrist MJ, Hendrix D, Jurka J, Kapitonov V, Ovcharenko I, Putnam NH, Shu S, Taher L, Blitz IL, Blumberg B, Dichmann DS, Dubchak I, Amaya E, Detter JC, Fletcher R, Gerhard DS, Goodstein D, Graves T, Grigoriev IV, Grimwood J, Kawashima T, Lindquist E, Lucas SM, Mead PE, Mitros T, Ogino H, Ohta Y, Poliakov AV, Pollet N, Robert J, Salamov A, Sater AK, Schmutz J, Terry A, Vize PD, Warren WC, Wells D, Wills A, Wilson RK, Zimmerman LB, Zorn AM, Grainger R, Grammer T, Khokha MK, Richardson PM, Rokhsar DS (2010) The genome of the Western clawed frog Xenopus tropicalis. Science 328: 633-636.
12. Solnica-Krezel L (2005) Conserved patterns of cell movements during vertebrate gastrulation. Curr Biol 15: R213-228.
13. Theiler K (1989) The house mouse: atlas of embryonic development. Springer, New York.
14. Downs KM, Davies T (1993) Staging of gastrulating mouse embryos by morphological landmarks in the dissecting microscope. Development 118: 1255-1266.
15. Nieuwkoop PD, Faber J (1994) Normal table of Xenopus laevis (Daudin). Garland, New York.
16. Hamburger V, Hamilton HL (1992) A series of normal stages in the development of the chick embryo. 1951. Dev Dyn 195: 231-272.
17. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203: 253-310.
18. Souslova V, Cesare P, Ding Y, Akopian AN, Stanfa L, Suzuki R, Carpenter K, Dickenson A, Boyce S, Hill R, Nebenuis-Oosthuizen D, Smith AJ, Kidd EJ, Wood JN (2000) Warm-coding deficits and aberrant inflammatory pain in mice lacking P2X3 receptors. Nature 407: 1015-1017.
19. Mulryan K, Gitterman DP, Lewis CJ, Vial C, Leckie BJ, Cobb AL, Brown JE, Conley EC, Buell G, Pritchard CA, Evans RJ (2000) Reduced vas deferens contraction and male infertility in mice lacking P2X1 receptors. Nature 403: 86-89.
20. Sun D, Samuelson LC, Yang T, Huang Y, Paliege A, Saunders T, Briggs J, Schnermann J (2001) Mediation of tubuloglomerular feedback by adenosine: evidence from mice lacking adenosine 1 receptors. Proc Natl Acad Sci USA 98: 9983-9988.
21. -/- mice. Immunol Lett 113: 83-89.
22. Sim JA, Chaumont S, Jo J, Ulmann L, Young MT, Cho K, Buell G, North RA, Rassendren F (2006) Altered hippocampal synaptic potentiation in P2X4 knock-out mice. J Neurosci 26: 9006-9009.
23. Yang D, Zhang Y, Nguyen HG, Koupenova M, Chauhan AK, Makitalo M, Jones MR, St Hilaire C, Seldin DC, Toselli P, Lamperti E, Schreiber BM, Gavras H, Wagner DD, Ravid K (2006) The A2B adenosine receptor protects against inflammation and excessive vascular adhesion. J Clin Invest 116: 1913-1923.
24. Bassil AK, Bourdu S, Townson KA, Wheeldon A, Jarvie EM, Zebda N, Abuin A, Grau E, Livi GP, Punter L, Latcham J, Grimes AM, Hurp DP, Downham KM, Sanger GJ, Winchester WJ, Morrison AD, Moore GB (2009) UDP-glucose modulates gastric function through P2Y14 receptor-dependent and -independent mechanisms. Am J Physiol Gastrointest Liver Physiol 296: G923-930.
25. Magdaleno S, Jensen P, Brumwell CL, Seal A, Lehman K, Asbury A, Cheung T, Cornelius T, Batten DM, Eden C, Norland SM, Rice DS, Dosooye N, Shakya S, Mehta P, Curran T (2006) BGEM: an in situ hybridization database of gene expression in the embryonic and adult mouse nervous system. PLoS Biol 4: e86.
26. Diez-Roux G, Banfi S, Sultan M, Geffers L, Anand S, Rozado D, Magen A, Canidio E, Pagani M, Peluso I, Lin-Marq N, Koch M, Bilio M, Cantiello I, Verde R, De Masi C, Bianchi SA, Cicchini J, Perroud E, Mehmeti S, Dagand E, Schrinner S, Nurnberger A, Schmidt K, Metz K, Zwingmann C, Brieske N, Springer C, Hernandez AM, Herzog S, Grabbe F, Sieverding C, Fischer B, Schrader K, Brockmeyer M, Dettmer S, Helbig C, Alunni V, Battaini MA, Mura C, Henrichsen CN, Garcia-Lopez R, Echevarria D, Puelles E, Garcia-Calero E, Kruse S, Uhr M, Kauck C, Feng G, Milyaev N, Ong CK, Kumar L, Lam M, Semple CA, Gyenesei A, Mundlos S, Radelof U, Lehrach H, Sarmientos P, Reymond A, Davidson DR, Dolle P, Antonarakis SE, Yaspo ML, Martinez S, Baldock RA, Eichele G, Ballabio A (2011) A high-resolution anatomical atlas of the transcriptome in the mouse embryo. PLoS Biol 9: e1000582.
27. Cui XS, Li XY, Shen XH, Bae YJ, Kang JJ, Kim NH (2007) Transcription profile in mouse four-cell, morula, and blastocyst: genes implicated in compaction and blastocoel formation. Mol Reprod Dev 74: 133-143.
28. Kucenas S, Li Z, Cox JA, Egan TM, Voigt MM (2003) Molecular characterization of the zebrafish P2X receptor subunit gene family. Neuroscience 121: 935-945.
29. Boehmler W, Petko J, Woll M, Frey C, Thisse B, Thisse C, Canfield VA, Levenson R (2009) Identification of zebrafish A2 adenosine receptors and expression in developing embryos. Gene Expr Patterns 9: 144-151.
30. Ryten M, Hoebertz A, Burnstock G (2001) Sequential expression of three receptor subtypes for extracellular ATP in developing rat skeletal muscle. Dev Dyn 221: 331-341.
31. Masse K, Bhamra S, Allsop G, Dale N, Jones EA (2010) Ectophosphodiesterase/nucleotide phosphohydrolase (Enpp) nucleotidases: cloning, conservation and developmental restriction. Int J Dev Biol 54: 181-193.
32. Masse K, Eason R, Bhamra S, Dale N, Jones EA (2006) Comparative genomic and expression analysis of the conserved NTPDase gene family in Xenopus. Genomics 87: 366-381.
33. Bachner D, Ahrens M, Betat N, Schroder D, Gross G (1999) Developmental expression analysis of murine autotaxin (ATX). Mech Dev 84: 121-125.
34. Ohuchi H, Hayashibara Y, Matsuda H, Onoi M, Mitsumori M, Tanaka M, Aoki J, Arai H, Noji S (2007) Diversified expression patterns of autotaxin, a gene for phospholipid-generating enzyme during mouse and chicken development. Dev Dyn 236: 1134-1143.
35. Nakanaga K, Hama K, Aoki J (2010) Autotaxin-an LPA producing enzyme with diverse functions. J Biochem 148: 13-24.
36. Nureddin A, Epsaro E, Kiessling AA (1990) Purines inhibit the development of mouse embryos in vitro. J Reprod Fertil 90: 455-464.
37. Zylka MJ, Sowa NA, Taylor-Blake B, Twomey MA, Herrala A, Voikar V, Vihko P (2008) Prostatic acid phosphatase is an ectonucleotidase and suppresses pain by generating adenosine. Neuron 60: 111-122.
38. Zimmermann H (2009) Prostatic acid phosphatase, a neglected ectonucleotidase. Purinergic Signal 5: 273-275.
39. Quintero IB, Araujo CL, Pulkka AE, Wirkkala RS, Herrala AM, Eskelinen EL, Jokitalo E, Hellstrom PA, Tuominen HJ, Hirvikoski PP, Vihko PT (2007) Prostatic acid phosphatase is not a prostate specific target. Cancer Res 67: 6549-6554.
40. Taylor-Blake B, Zylka MJ (2010) Prostatic acid phosphatase is expressed in peptidergic and nonpeptidergic nociceptive neurons of mice and rats. PLoS One 5: e8674.
41. Boldogkoi Z, Schutz B, Sallach J, Zimmer A (2002) P2X(3) receptor expression at early stage of mouse embryogenesis. Mech Dev 118: 255-260.
42. Norton WH, Rohr KB, Burnstock G (2000) Embryonic expression of a P2X(3) receptor encoding gene in zebrafish. Mech Dev 99: 149-152.
43. Kucenas S, Soto F, Cox JA, Voigt MM (2006) Selective labeling of central and peripheral sensory neurons in the developing zebrafish using P2X(3) receptor subunit transgenes. Neuroscience 138: 641-652.
44. Appelbaum L, Skariah G, Mourrain P, Mignot E (2007) Comparative expression of p2x receptors and ecto-nucleoside triphosphate diphosphohydrolase 3 in hypocretin and sensory neurons in zebrafish. Brain Res 1174: 66-75.
45. Robaye B, Ghanem E, Wilkin F, Fokan D, van Driessche W, Schurmans S, Boeynaems JM, Beauwens R (2003) Loss of nucleotide regulation of epithelial chloride transport in the jejunum of P2Y4-null mice. Mol Pharmacol 63: 777-783.
46. Cockayne DA, Dunn PM, Zhong Y, Rong W, Hamilton SG, Knight GE, Ruan HZ, Ma B, Yip P, Nunn P, McMahon SB, Burnstock G, Ford AP (2005) P2X2 knockout mice and P2X2/P2X3 double knockout mice reveal a role for the P2X2 receptor subunit in mediating multiple sensory effects of ATP. J Physiol 567: 621-639.
47. Cockayne DA, Hamilton SG, Zhu QM, Dunn PM, Zhong Y, Novakovic S, Malmberg AB, Cain G, Berson A, Kassotakis L, Hedley L, Lachnit WG, Burnstock G, McMahon SB, Ford AP (2000) Urinary bladder hyporeflexia and reduced pain-related behaviour in P2X3-deficient mice. Nature 407: 1011-1015.
48. Lewis C, Neidhart S, Holy C, North RA, Buell G, Surprenant A (1995) Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 377: 432-435.
49. Salvatore CA, Tilley SL, Latour AM, Fletcher DS, Koller BH, Jacobson MA (2000) Disruption of the A(3) adenosine receptor gene in mice and its effect on stimulated inflammatory cells. J Biol Chem 275: 4429-4434.
50. Eckle T, Fullbier L, Wehrmann M, Khoury J, Mittelbronn M, Ibla J, Rosenberger P, Eltzschig HK (2007) Identification of ectonucleotidases CD39 and CD73 in innate protection during acute lung injury. J Immunol 178: 8127-8137.
51. Masse K, Bhamra S, Eason R, Dale N, Jones EA (2007) Purine-mediated signalling triggers eye development. Nature 449: 1058-1062.
52. Fabre JE, Nguyen M, Latour A, Keifer JA, Audoly LP, Coffman TM, Koller BH (1999) Decreased platelet aggregation, increased bleeding time and resistance to thromboembolism in P2Y1-deficient mice. Nat Med 5: 1199-1202.
53. Leon C, Hechler B, Freund M, Eckly A, Vial C, Ohlmann P, Dierich A, LeMeur M, Cazenave JP, Gachet C (1999) Defective platelet aggregation and increased resistance to thrombosis in purinergic P2Y(1) receptor-null mice. J Clin Invest 104: 1731-1737.
54. Grindley JC, Davidson DR, Hill RE (1995) The role of Pax-6 in eye and nasal development. Development 121: 1433-1442.
55. Kucenas S, Cox JA, Soto F, Lamora A, Voigt MM (2009) Ectodermal P2X receptor function plays a pivotal role in craniofacial development of the zebrafish. Purinergic Signal 5: 395-407.
56. Funakoshi H, Chan TO, Good JC, Libonati JR, Piuhola J, Chen X, MacDonnell SM, Lee LL, Herrmann DE, Zhang J, Martini J, Palmer TM, Sanbe A, Robbins J, Houser SR, Koch WJ, Feldman AM (2006) Regulated overexpression of the A1-adenosine receptor in mice results in adverse but reversible changes in cardiac morphology and function. Circulation 114: 2240-2250.
57. Zhao Z, Yaar R, Ladd D, Cataldo LM, Ravid K (2002) Overexpression of A3 adenosine receptors in smooth, cardiac, and skeletal muscle is lethal to embryos. Microvasc Res 63: 61-69.
58. Tsuchimori N, Miyashiro S, Shibai H, Ikegami S (1988) Adenosine induces dormancy in starfish blastulas. Development 103: 345-351.
59. Adair TH, Montani JP, Strick DM, Guyton AC (1989) Vascular development in chick embryos: a possible role for adenosine. Am J Physiol 256: H240-246.
60. Ghatpande SK, Billington CJ Jr, Rivkees SA, Wendler CC (2008) Hypoxia induces cardiac malformations via A1 adenosine receptor activation in chicken embryos. Birth Defects Res A Clin Mol Teratol 82: 121-130.
61. Iijima R, Kunieda T, Yamaguchi S, Kamigaki H, Fujii-Taira I, Sekimizu K, Kubo T, Natori S, Homma KJ (2008) The extracellular adenosine deaminase growth factor, ADGF/CECR1, plays a role in Xenopus embryogenesis via the adenosine/P1 receptor. J Biol Chem 283: 2255-2264.
62. Knudsen TB, Blackburn MR, Chinsky JM, Airhart MJ, Kellems RE (1991) Ontogeny of adenosine deaminase in the mouse decidua and placenta: immunolocalization and embryo transfer studies. Biol Reprod 44: 171-184.
63. Chechik BE, Sengupta S, Hibi T, Fernandes B (1985) Immunomorphological localization of adenosine deaminase in rat tissues during ontogeny. Histochem J 17: 153-170.
64. Wakamiya M, Blackburn MR, Jurecic R, McArthur MJ, Geske RS, Cartwright J Jr, Mitani K, Vaishnav S, Belmont JW, Kellems RE et al (1995) Disruption of the adenosine deaminase gene causes hepatocellular impairment and perinatal lethality in mice. Proc Natl Acad Sci USA 92: 3673-3677.
65. Migchielsen AA, Breuer ML, van Roon MA, te Riele H, Zurcher C, Ossendorp F, Toutain S, Hershfield MS, Berns A, Valerio D (1995) Adenosine-deaminase-deficient mice die perinatally and exhibit liver-cell degeneration, atelectasis and small intestinal cell death. Nat Genet 10: 279-287.
66. Nofech-Mozes Y, Blaser SI, Kobayashi J, Grunebaum E, Roifman CM (2007) Neurologic abnormalities in patients with adenosine deaminase deficiency. Pediatr Neurol 37: 218-221.
67. Franco R, Casado V, Ciruela F, Saura C, Mallol J, Canela EI, Lluis C (1997) Cell surface adenosine deaminase: much more than an ectoenzyme. Prog Neurobiol 52: 283-294.
68. Wolpert L (1969) Positional information and the spatial pattern of cellular differentiation. J Theor Biol 25: 1-47.
69. Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-689.
70. Ingham PW, McMahon AP (2001) Hedgehog signaling in animal development: paradigms and principles. Genes Dev 15: 3059-3087.
71. van Amerongen R, Nusse R (2009) Towards an integrated view of Wnt signaling in development. Development 136: 3205-3214.
72. Moustakas A, Heldin CH (2009) The regulation of TGFbeta signal transduction. Development 136: 3699-3714.
73. Dorey K, Amaya E (2010) FGF signalling: diverse roles during early vertebrate embryogenesis. Development 137: 3731-3742.
74. Campo-Paysaa F, Marletaz F, Laudet V, Schubert M (2008) Retinoic acid signaling in development: tissue-specific functions and evolutionary origins. Genesis 46: 640-656.
75. Mic FA, Molotkov A, Benbrook DM, Duester G (2003) Retinoid activation of retinoic acid receptor but not retinoid X receptor is sufficient to rescue lethal defect in retinoic acid synthesis. Proc Natl Acad Sci USA 100: 7135-7140.
76. Benazet JD, Zeller R (2009) Vertebrate limb development: moving from classical morphogen gradients to an integrated 4-dimensional patterning system. Cold Spring Harb Perspect Biol 1: a001339.
77. von Albertini M, Palmetshofer A, Kaczmarek E, Koziak K, Stroka D, Grey ST, Stuhlmeier KM, Robson SC (1998) Extracellular ATP and ADP activate transcription factor NF-kappa B and induce endothelial cell apoptosis. Biochem Biophys Res Commun 248: 822-829.
78. Basheer R, Rainnie DG, Porkka-Heiskanen T, Ramesh V, McCarley RW (2001) Adenosine, prolonged wakefulness, and A1-activated NF-kappaB DNA binding in the basal forebrain of the rat. Neuroscience 104: 731-739.
79. Korcok J, Raimundo LN, Ke HZ, Sims SM, Dixon SJ (2004) Extracellular nucleotides act through P2X7 receptors to activate NF-kappaB in osteoclasts. J Bone Miner Res 19: 642-651.
80. Fishman P, Bar-Yehuda S, Ohana G, Barer F, Ochaion A, Erlanger A, Madi L (2004) An agonist to the A3 adenosine receptor inhibits colon carcinoma growth in mice via modulation of GSK-3 beta and NF-kappa B. Oncogene 23: 2465-2471.
81. Schafer R, Hartig R, Sedehizade F, Welte T, Reiser G (2006) Adenine nucleotides inhibit proliferation of the human lung adenocarcinoma cell line LXF-289 by activation of nuclear factor kappaB1 and mitogen-activated protein kinase pathways. FEBS J 273: 3756-3767.
82. Liu Q, Li J, Khoury J, Colgan SP, Ibla JC (2009) Adenosine signaling mediates SUMO-1 modification of IkappaBalpha during hypoxia and reoxygenation. J Biol Chem 284: 13686-13695.
83. Molliver DC, Cook SP, Carlsten JA, Wright DE, McCleskey EW (2002) ATP and UTP excite sensory neurons and induce CREB phosphorylation through the metabotropic receptor, P2Y2. Eur J Neurosci 16: 1850-1860.
84. Lynge J, Schulte G, Nordsborg N, Fredholm BB, Hellsten Y (2003) Adenosine A 2B receptors modulate cAMP levels and induce CREB but not ERK1/2 and p38 phosphorylation in rat skeletal muscle cells. Biochem Biophys Res Commun 307: 180-187.
85. Gavala ML, Pfeiffer ZA, Bertics PJ (2008) The nucleotide receptor P2RX7 mediates ATP-induced CREB activation in human and murine monocytic cells. J Leukoc Biol 84: 1159-1171.
86. Dooley R, Mashukova A, Toetter B, Hatt H, Neuhaus EM (2011) Purinergic receptor antagonists inhibit odorant-mediated CREB phosphorylation in sustentacular cells of mouse olfactory epithelium. BMC Neurosci 12: 86.
87. Sandell LL, Sanderson BW, Moiseyev G, Johnson T, Mushegian A, Young K, Rey JP, Ma JX, Staehling-Hampton K, Trainor PA (2007) RDH10 is essential for synthesis of embryonic retinoic acid and is required for limb, craniofacial, and organ development. Genes Dev 21: 1113-1124.
88. Niederreither K, Subbarayan V, Dolle P, Chambon P (1999) Embryonic retinoic acid synthesis is essential for early mouse post-implantation development. Nat Genet 21: 444-448.
89. Pennimpede T, Cameron DA, MacLean GA, Li H, Abu-Abed S, Petkovich M (2010) The role of CYP26 enzymes in defining appropriate retinoic acid exposure during embryogenesis. Birth Defects Res A Clin Mol Teratol 88: 883-894.
90. Sirbu IO, Gresh L, Barra J, Duester G (2005) Shifting boundaries of retinoic acid activity control hindbrain segmental gene expression. Development 132: 2611-2622.
91. Abu-Abed S, Dolle P, Metzger D, Beckett B, Chambon P, Petkovich M (2001) The retinoic acid-metabolizing enzyme, CYP26A1, is essential for normal hindbrain patterning, vertebral identity, and development of posterior structures. Genes Dev 15: 226-240.
92. Mark M, Ghyselinck NB, Chambon P (2009) Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 7: e002.
93. Slakey LL, Cosimini K, Earls JP, ThomasC GEL (1986) Simulation of extracellular nucleotide hydrolysis and determination of kinetic constants for the ectonucleotidases. J Biol Chem 261: 15505-15507.
94. James S, Richardson PJ (1993) Production of adenosine from extracellular ATP at the striatal cholinergic synapse. J Neurochem 60: 219-227.
95. Dale N (1998) Delayed production of adenosine underlies temporal modulation of swimming in frog embryo. J Physiol (Lond) 511: 265-272.
96. Dale N, Frenguelli BG (2011) Measurement of purine release with microelectrode biosensors. Purinergic Signal. doi: 10. 1007/s11302-011-9273-4.
97. Hoffmann C, Gaietta G, Bunemann M, Adams SR, Oberdorff-Maass S, Behr B, Vilardaga JP, Tsien RY, Ellisman MH, Lohse MJ (2005) A FlAsH-based FRET approach to determine G protein-coupled receptor activation in living cells. Nat Methods 2: 171-176.
98. Rivkees SA (1995) The ontogeny of cardiac and neural A1 adenosine receptor expression in rats. Brain Res Dev Brain Res 89: 202-213.
99. Weaver DR (1996) A1-adenosine receptor gene expression in fetal rat brain. Brain Res Dev Brain Res 94: 205-223.
100. Cheung KK, Chan WY, Burnstock G (2005) Expression of P2X purinoceptors during rat brain development and their inhibitory role on motor axon outgrowth in neural tube explant cultures. Neuroscience 133: 937-945.
101. Brandle U, Zenner HP, Ruppersberg JP (1999) Gene expression of P2X-receptors in the developing inner ear of the rat. Neurosci Lett 273: 105-108.
102. Liang SX, Motin L, Moussa CE, Lavidis NA, Phillips WD (2001) Spatial distribution and developmental appearance of postjunctional P2X1 receptors on smooth muscle cells of the mouse vas deferens. Synapse 42: 1-11.
103. Hoffman BG, Zavaglia B, Witzsche J, Ruiz de Algara T, Beach M, Hoodless PA, Jones SJ, Marra MA, Helgason CD (2008) Identification of transcripts with enriched expression in the developing and adult pancreas. Genome Biol 9: R99.
104. Ruan HZ, Moules E, Burnstock G (2004) Changes in P2X3 purinoceptors in sensory ganglia of the mouse during embryonic and postnatal development. Histochem Cell Biol 122: 539-551.
105. Kidd EJ, Miller KJ, Sansum AJ, Humphrey PP (1998) Evidence for P2X3 receptors in the developing rat brain. Neuroscience 87: 533-539.
106. Cheung KK, Burnstock G (2002) Localization of P2X3 receptors and coexpression with P2X2 receptors during rat embryonic neurogenesis. J Comp Neurol 443: 368-382.
107. Cheung KK, Coutinho-Silva R, Chan WY, Burnstock G (2007) Early expression of adenosine 5′-triphosphate-gated P2X7 receptors in the developing rat pancreas. Pancreas 35: 164-168.
108. Freeman TC, Dixon AK, Campbell EA, Tait TM, Richardson PJ, Rice KM, Maslen GL, Metcalfe AD, Streuli CH, Bentley DR (1998) Expression mapping of mouse genes. MGI Direct Data Submission J: 46439.
109. Hahnel AC, Rappolee DA, Millan JL, Manes T, Ziomek CA, Theodosiou NG, Werb Z, Pedersen RA, Schultz GA (1990) Two alkaline phosphatase genes are expressed during early development in the mouse embryo. Development 110: 555-564.
110. Langer D, Ikehara Y, Takebayashi H, Hawkes R, Zimmermann H (2007) The ectonucleotidases alkaline phosphatase and nucleoside triphosphate diphosphohydrolase 2 are associated with subsets of progenitor cell populations in the mouse embryonic, postnatal and adult neurogenic zones. Neuroscience 150: 863-879.
111. Brun-Heath I, Ermonval M, Chabrol E, Xiao J, Palkovits M, Lyck R, Miller F, Couraud PO, Mornet E, Fonta C (2011) Differential expression of the bone and the liver tissue non-specific alkaline phosphatase isoforms in brain tissues. Cell Tissue Res 343: 521-536.
112. Sharov AA, Piao Y, Matoba R, Dudekula DB, Qian Y, VanBuren V, Falco G, Martin PR, Stagg CA, Bassey UC, Wang Y, Carter MG, Hamatani T, Aiba K, Akutsu H, Sharova L, Tanaka TS, Kimber WL, Yoshikawa T, Jaradat SA, Pantano S, Nagaraja R, Boheler KR, Taub D, Hodes RJ, Longo DL, Schlessinger D, Keller J, Klotz E, Kelsoe G, Umezawa A, Vescovi AL, Rossant J, Kunath T, Hogan BL, Curci A, D'Urso M, Kelso J, Hide W, Ko MS (2003) Transcriptome analysis of mouse stem cells and early embryos. PLoS Biol 1: E74.
113. Brown P, Dale N (2000) Adenosine A1 receptors modulate high voltage-activated Ca2+ currents and motor pattern generation in the xenopus embryo. J Physiol 525(Pt 3): 655-667.
114. Cheng AW, Kong LW, Tung EK, Siow NL, Choi RC, Zhu SQ, Peng BH, Tsim KW (2003) cDNA encodes Xenopus P2Y(1) nucleotide receptor: expression at the neuromuscular junctions. Neuroreport 14: 351-357.
115. Bogdanov YD, Dale L, King BF, Whittock N, Burnstock G (1997) Early expression of a novel nucleotide receptor in the neural plate of Xenopus embryos. J Biol Chem 272: 12583-12590.
116. Devader C, Drew CM, Geach TJ, Tabler J, Townsend-Nicholson A, Dale L (2007) A novel nucleotide receptor in Xenopus activates the cAMP second messenger pathway. FEBS Lett 581: 5332-5336.
117. Durand IH, Green RD (2001) Cloning of a chick A3 adenosine receptor: characterization of ligand binding and receptor-effector coupling of chick A1 and A3 adenosine receptors. Naunyn Schmiedebergs Arch Pharmacol 363: 81-86.
118. Soto F, Krause U, Borchardt K, Ruppelt A (2003) Cloning, tissue distribution and functional characterization of the chicken P2X1 receptor. FEBS Lett 533: 54-58.
119. Ruppelt A, Liang BT, Soto F (1999) Cloning, functional characterization and developmental expression of a P2X receptor from chick embryo. Prog Brain Res 120: 81-90.
120. Ruppelt A, Ma W, Borchardt K, Silberberg SD, Soto F (2001) Genomic structure, developmental distribution and functional properties of the chicken P2X(5) receptor. J Neurochem 77: 1256-1265.
121. Meyer MP, Groschel-Stewart U, Robson T, Burnstock G (1999) Expression of two ATP-gated ion channels, P2X5 and P2X6, in developing chick skeletal muscle. Dev Dyn 216: 442-449.
122. Bo X, Schoepfer R, Burnstock G (2000) Molecular cloning and characterization of a novel ATP P2X receptor subtype from embryonic chick skeletal muscle. J Biol Chem 275: 14401-14407.
123. Choi RC, Man ML, Ling KK, Ip NY, Simon J, Barnard EA, Tsim KW (2001) Expression of the P2Y1 nucleotide receptor in chick muscle: its functional role in the regulation of acetylcholinesterase and acetylcholine receptor. J Neurosci 21: 9224-9234.
124. Meyer MP, Clarke JD, Patel K, Townsend-Nicholson A, Burnstock G (1999) Selective expression of purinoceptor cP2Y1 suggests a role for nucleotide signalling in development of the chick embryo. Dev Dyn 214: 152-158.
125. Johansson B, Halldner L, Dunwiddie TV, Masino SA, Poelchen W, Gimenez-Llort L, Escorihuela RM, Fernandez-Teruel A, Wiesenfeld-Hallin Z, Xu XJ, Hardemark A, Betsholtz C, Herlenius E, Fredholm BB (2001) Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc Natl Acad Sci USA 98: 9407-9412.
126. Ledent C, Vaugeois JM, Schiffmann SN, Pedrazzini T, El Yacoubi M, Vanderhaeghen JJ, Costentin J, Heath JK, Vassart G, Parmentier M (1997) Aggressiveness, hypoalgesia and high blood pressure in mice lacking the adenosine A2a receptor. Nature 388: 674-678.
127. Chen JF, Huang Z, Ma J, Zhu J, Moratalla R, Standaert D, Moskowitz MA, Fink JS, Schwarzschild MA (1999) A(2A) adenosine receptor deficiency attenuates brain injury induced by transient focal ischemia in mice. J Neurosci 19: 9192-9200.
128. Hua X, Kovarova M, Chason KD, Nguyen M, Koller BH, Tilley SL (2007) Enhanced mast cell activation in mice deficient in the A2b adenosine receptor. J Exp Med 204: 117-128.
129. Yamamoto K, Sokabe T, Matsumoto T, Yoshimura K, Shibata M, Ohura N, Fukuda T, Sato T, Sekine K, Kato S, Isshiki M, Fujita T, Kobayashi M, Kawamura K, Masuda H, Kamiya A, Ando J (2006) Impaired flow-dependent control of vascular tone and remodeling in P2X4-deficient mice. Nat Med 12: 133-137.
130. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, Griffiths RJ, Gabel CA (2001) Altered cytokine production in mice lacking P2X(7) receptors. J Biol Chem 276: 125-132.
131. Chessell IP, Hatcher JP, Bountra C, Michel AD, Hughes JP, Green P, Egerton J, Murfin M, Richardson J, Peck WL, Grahames CB, Casula MA, Yiangou Y, Birch R, Anand P, Buell GN (2005) Disruption of the P2X7 purinoceptor gene abolishes chronic inflammatory and neuropathic pain. Pain 114: 386-396.
132. Homolya L, Watt WC, Lazarowski ER, Koller BH, Boucher RC (1999) Nucleotide-regulated calcium signaling in lung fibroblasts and epithelial cells from normal and P2Y(2) receptor (-/-) mice. J Biol Chem 274: 26454-26460.
133. Cressman VL, Lazarowski E, Homolya L, Boucher RC, Koller BH, Grubb BR (1999) Effect of loss of P2Y(2) receptor gene expression on nucleotide regulation of murine epithelial Cl(-) transport. J Biol Chem 274: 26461-26468.
134. Bar I, Guns PJ, Metallo J, Cammarata D, Wilkin F, Boeynams JM, Bult H, Robaye B (2008) Knockout mice reveal a role for P2Y6 receptor in macrophages, endothelial cells, and vascular smooth muscle cells. Mol Pharmacol 74: 777-784.
135. Foster CJ, Prosser DM, Agans JM, Zhai Y, Smith MD, Lachowicz JE, Zhang FL, Gustafson E, Monsma FJ Jr, Wiekowski MT, Abbondanzo SJ, Cook DN, Bayne ML, Lira SA, Chintala MS (2001) Molecular identification and characterization of the platelet ADP receptor targeted by thienopyridine antithrombotic drugs. J Clin Invest 107: 1591-1598.
136. Andre P, Delaney SM, LaRocca T, Vincent D, DeGuzman F, Jurek M, Koller B, Phillips DR, Conley PB (2003) P2Y12 regulates platelet adhesion/activation, thrombus growth, and thrombus stability in injured arteries. J Clin Invest 112: 398-406.
137. Fabre AC, Malaval C, Ben Addi A, Verdier C, Pons V, Serhan N, Lichtenstein L, Combes G, Huby T, Briand F, Collet X, Nijstad N, Tietge UJ, Robaye B, Perret B, Boeynaems JM, Martinez LO (2010) P2Y13 receptor is critical for reverse cholesterol transport. Hepatology 52: 1477-1483.
138. Enjyoji K, Sevigny J, Lin Y, Frenette PS, Christie PD, Esch JS 2nd, Imai M, Edelberg JM, Rayburn H, Lech M, Beeler DL, Csizmadia E, Wagner DD, Robson SC, Rosenberg RD (1999) Targeted disruption of cd39/ATP diphosphohydrolase results in disordered hemostasis and thromboregulation. Nat Med 5: 1010-1017.
139. Castrop H, Huang Y, Hashimoto S, Mizel D, Hansen P, Theilig F, Bachmann S, Deng C, Briggs J, Schnermann J (2004) Impairment of tubuloglomerular feedback regulation of GFR in ecto-5′-nucleotidase/CD73-deficient mice. J Clin Invest 114: 634-642.
140. Koszalka P, Ozuyaman B, Huo Y, Zernecke A, Flogel U, Braun N, Buchheiser A, Decking UK, Smith ML, Sevigny J, Gear A, Weber AA, Molojavyi A, Ding Z, Weber C, Ley K, Zimmermann H, Godecke A, Schrader J (2004) Targeted disruption of cd73/ecto-5′-nucleotidase alters thromboregulation and augments vascular inflammatory response. Circ Res 95: 814-821.
141. Babij P, Roudier M, Graves T, Han CY, Chhoa M, Li CM, Juan T, Morony S, Grisanti M, Li X, Yu L, Dwyer D, Lloyd DJ, Bass MB, Richards WG, Ebeling C, Amato J, Carlson G (2009) New variants in the Enpp 1 and Ptpn6 genes cause low BMD, crystal-related arthropathy, and vascular calcification. J Bone Miner Res 24: 1552-1564.
142. Okawa A, Nakamura I, Goto S, Moriya H, Nakamura Y, Ikegawa S (1998) Mutation in Npps in a mouse model of ossification of the posterior longitudinal ligament of the spine. Nat Genet 19: 271-273.
143. van Meeteren LA, Ruurs P, Stortelers C, Bouwman P, van Rooijen MA, Pradere JP, Pettit TR, Wakelam MJ, Saulnier-Blache JS, Mummery CL, Moolenaar WH, Jonkers J (2006) Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol Cell Biol 26: 5015-5022.
144. Fotopoulou S, Oikonomou N, Grigorieva E, Nikitopoulou I, Paparountas T, Thanassopoulou A, Zhao Z, Xu Y, Kontoyiannis DL, Remboutsika E, Aidinis V (2010) ATX expression and LPA signalling are vital for the development of the nervous system. Dev Biol 339: 451-464.
145. Narisawa S, Frohlander N, Millan JL (1997) Inactivation of two mouse alkaline phosphatase genes and establishment of a model of infantile hypophosphatasia. Dev Dyn 208: 432-446.
146. Dehghani H, Narisawa S, Millan JL, Hahnel AC (2000) Effects of disruption of the embryonic alkaline phosphatase gene on preimplantation development of the mouse. Developmental dynamics: an official publication of the American Association of Anatomists 217: 440-448.
147. Kalin RE, Banziger-Tobler NE, Detmar M, Brandli AW (2009) An in vivo chemical library screen in Xenopus tadpoles reveals novel pathways involved in angiogenesis and lymphangiogenesis. Blood 114: 1110-1122.
148. Gerhart J, Danilchik M, Doniach T, Roberts S, Rowning B, Stewart R (1989) Cortical rotation of the Xenopus egg: consequences for the anteroposterior pattern of embryonic dorsal development. Development 107(Suppl): 37-51.
149. Ludlow MJ, Durai L, Ennion SJ (2009) Functional characterization of intracellular Dictyostelium discoideum P2X receptors. J Biol Chem 284: 35227-35239.
150. Fountain SJ, Parkinson K, Young MT, Cao L, Thompson CR, North RA (2007) An intracellular P2X receptor required for osmoregulation in Dictyostelium discoideum. Nature 448: 200-203.