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Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

General Review Article

Role of Ectonucleotidases in Synapse Formation During Brain Development: Physiological and Pathological Implications

Author(s): Ivana Grković*, Dunja Drakulić, Jelena Martinović and Nataša Mitrović

Volume 17, Issue 1, 2019

Page: [84 - 98] Pages: 15

DOI: 10.2174/1570159X15666170518151541

Price: $65

Abstract

Background: Extracellular adenine nucleotides and nucleosides, such as ATP and adenosine, are among the most recently identified and least investigated diffusible signaling factors that contribute to the structural and functional remodeling of the brain, both during embryonic and postnatal development. Their levels in the extracellular milieu are tightly controlled by various ectonucleotidases: ecto-nucleotide pyrophosphatase/phosphodiesterases (E-NPP), alkaline phosphatases (AP), ecto-nucleoside triphosphate diphosphohydrolases (E-NTPDases) and ecto-5'- nucleotidase (eN).

Methods: Studies related to the expression patterns of ectonucleotidases and their known features during brain development are reviewed, highlighting involvement of these enzymes in synapse formation and maturation in physiological as well as in pathological states.

Results: During brain development and in adulthood all ectonucleotidases have diverse expression pattern, cell specific localization and function. NPPs are expressed at early embryonic days, but the expression of NPP3 is reduced and restricted to ependymal area in adult brain. NTPDase2 is dominant ectonucleotidase existing in the progenitor cells as well as main astrocytic NTPDase in the adult brain, while NTPDase3 is fully expressed after third postnatal week, almost exclusively on varicose fibers. Specific brain AP is functionally associated with synapse formation and this enzyme is sufficient for adenosine production during neurite growth and peak of synaptogenesis. eN is transiently associated with synapses during synaptogenesis, however in adult brain it is more glial than neuronal enzyme.

Conclusion: Control of extracellular adenine nucleotide levels by ectonucleotidases are important for understanding the role of purinergic signaling in developing tissues and potential targets in developmental disorders such as autism.

Keywords: Brain development, ectonucleotidases, NPP, TNAP, NTPDase, ecto-5'-nucleotidase, synaptogenesis, autism.

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[1]
Zimmermann, H. Nucleotide signaling in nervous system development. Pflugers Arch., 2006, 452(5), 573-588. [http://dx.doi.org/ 10.1007/s00424-006-0067-4]. [PMID: 16639549].
[2]
Majumder, P.; Trujillo, C.A.; Lopes, C.G.; Resende, R.R.; Gomes, K.N.; Yuahasi, K.K.; Britto, L.R.; Ulrich, H. New insights into purinergic receptor signaling in neuronal differentiation, neuroprotection, and brain disorders. Purinergic Signal., 2007, 3(4), 317-331. [http://dx.doi.org/10.1007/s11302-007-9074-y]. [PMID: 18404445].
[3]
Burnstock, G.; Ulrich, H. Purinergic signaling in embryonic and stem cell development. Cell. Mol. Life Sci., 2011, 68(8), 1369-1394. [http://dx.doi.org/10.1007/s00018-010-0614-1]. [PMID: 21222015].
[4]
Burnstock, G.; Dale, N. Purinergic signalling during development and ageing. Purinergic Signal., 2015, 11(3), 277-305. [http://dx. doi.org/10.1007/s11302-015-9452-9]. [PMID: 25989750].
[5]
Oliveira, Á.; Illes, P.; Ulrich, H. Purinergic receptors in embryonic and adult neurogenesis. Neuropharmacology, 2016, 104, 272-281. [http://dx.doi.org/10.1016/j.neuropharm.2015.10.008]. [PMID: 26456352].
[6]
Cavaliere, F.; Donno, C.; D’Ambrosi, N. Purinergic signaling: a common pathway for neural and mesenchymal stem cell maintenance and differentiation. Front. Cell. Neurosci., 2015, 9, 211. [http://dx.doi.org/10.3389/fncel.2015.00211]. [PMID: 26082684].
[7]
Zimmermann, H. Purinergic signaling in neural development. Semin. Cell Dev. Biol., 2011, 22(2), 194-204. [http://dx.doi.org/10. 1016/j.semcdb.2011.02.007]. [PMID: 21320621].
[8]
Neary, J.T.; Zimmermann, H. Trophic functions of nucleotides in the central nervous system. Trends Neurosci., 2009, 32(4), 189-198. [http://dx.doi.org/10.1016/j.tins.2009.01.002]. [PMID: 19282037].
[9]
Franke, H.; Illes, P. Involvement of P2 receptors in the growth and survival of neurons in the CNS. Pharmacol. Ther., 2006, 109(3), 297-324. [http://dx.doi.org/10.1016/j.pharmthera.2005.06.002]. [PMID: 16102837].
[10]
Massé, K.; Dale, N. Purines as potential morphogens during embryonic development. Purinergic Signal., 2012, 8(3), 503-521. [http://dx.doi.org/10.1007/s11302-012-9290-y]. [PMID: 22270538].
[11]
Burnstock, G. Physiology and pathophysiology of purinergic neurotransmission. Physiol. Rev., 2007, 87(2), 659-797. [http://dx.doi. org/10.1152/physrev.00043.2006]. [PMID: 17429044].
[12]
Rebola, N.; Lujan, R.; Cunha, R.A.; Mulle, C. Adenosine A2A receptors are essential for long-term potentiation of NMDA-EPSCs at hippocampal mossy fiber synapses. Neuron, 2008, 57(1), 121-134. [http://dx.doi.org/10.1016/j.neuron.2007.11.023]. [PMID: 18184569].
[13]
Düster, R.; Prickaerts, J.; Blokland, A. Purinergic signaling and hippocampal long-term potentiation. Curr. Neuropharmacol., 2014, 12(1), 37-43. [http://dx.doi.org/10.2174/1570159X113119990045]. [PMID: 24533014].
[14]
Del Puerto, A.; Wandosell, F.; Garrido, J.J. Neuronal and glial purinergic receptors functions in neuron development and brain disease. Front. Cell. Neurosci., 2013, 7, 197. [PMID: 24191147].
[15]
Sebastião, A.M.; Ribeiro, J.A. Neuromodulation and metamodulation by adenosine: Impact and subtleties upon synaptic plasticity regulation. Brain Res., 2015, 1621, 102-113. [http://dx.doi.org/ 10.1016/j.brainres.2014.11.008]. [PMID: 25446444].
[16]
Dale, N. Dynamic ATP signalling and neural development. J. Physiol., 2008, 586(10), 2429-2436. [http://dx.doi.org/10.1113/ jphysiol.2008.152207]. [PMID: 18356200].
[17]
Burnstock, G.; Verkhratsky, A. Long-term (trophic) purinergic signalling: purinoceptors control cell proliferation, differentiation and death. Cell Death Dis., 2010, 1, e9. [http://dx.doi.org/10.1038/ cddis.2009.11]. [PMID: 21364628].
[18]
Franke, H.; Verkhratsky, A.; Burnstock, G.; Illes, P. Pathophysiology of astroglial purinergic signalling. Purinergic Signal., 2012, 8(3), 629-657. [http://dx.doi.org/10.1007/s11302-012-9300-0]. [PMID: 22544529].
[19]
Fumagalli, M.; Lecca, D.; Abbracchio, M.P. Role of purinergic signalling in neuro-immune cells and adult neural progenitors. Front. Biosci., 2011, 16, 2326-2341. [http://dx.doi.org/10.2741/ 3856]. [PMID: 21622179].
[20]
Pankratov, Y.; Lalo, U.; Verkhratsky, A.; North, R.A. Quantal release of ATP in mouse cortex. J. Gen. Physiol., 2007, 129(3), 257-265. [http://dx.doi.org/10.1085/jgp.200609693]. [PMID: 17325196].
[21]
Verkhratsky, A.; Krishtal, O.A.; Burnstock, G. Purinoceptors on neuroglia. Mol. Neurobiol., 2009, 39(3), 190-208. [http://dx.doi. org/10.1007/s12035-009-8063-2]. [PMID: 19283516].
[22]
Abbracchio, M.P.; Burnstock, G.; Verkhratsky, A.; Zimmermann, H. Purinergic signalling in the nervous system: an overview. Trends Neurosci., 2009, 32(1), 19-29. [http://dx.doi.org/10.1016/ j.tins.2008.10.001]. [PMID: 19008000].
[23]
Köles, L.; Kató, E.; Hanuska, A.; Zádori, Z.S.; Al-Khrasani, M.; Zelles, T.; Rubini, P.; Illes, P. Modulation of excitatory neurotransmission by neuronal/glial signalling molecules: interplay between purinergic and glutamatergic systems. Purinergic Signal., 2016, 12(1), 1-24. [http://dx.doi.org/10.1007/s11302-015-9480-5]. [PMID: 26542977].
[24]
Heine, C.; Sygnecka, K.; Franke, H. Purines in neurite growth and astroglia activation. Neuropharmacology, 2016, 104, 255-271. [http://dx.doi.org/10.1016/j.neuropharm.2015.10.022]. [PMID: 26498067].
[25]
Khakh, B.S.; North, R.A. Neuromodulation by extracellular ATP and P2X receptors in the CNS. Neuron, 2012, 76(1), 51-69. [http://dx.doi.org/10.1016/j.neuron.2012.09.024]. [PMID: 23040806].
[26]
Tozaki-Saitoh, H.; Tsuda, M.; Inoue, K. Role of purinergic receptors in CNS function and neuroprotection. Adv. Pharmacol., 2011, 61, 495-528. [http://dx.doi.org/10.1016/B978-0-12-385526-8.00015-1]. [PMID: 21586368].
[27]
Zimmermann, H.; Zebisch, M.; Sträter, N. Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal., 2012, 8(3), 437-502. [http://dx.doi.org/10.1007/s11302-012-9309-4]. [PMID: 22555564].
[28]
Robson, S.C.; Sévigny, J.; Zimmermann, H. The E-NTPDase family of ectonucleotidases: Structure function relationships and pathophysiological significance. Purinergic Signal., 2006, 2(2), 409-430. [http://dx.doi.org/10.1007/s11302-006-9003-5]. [PMID: 18404480].
[29]
Zimmermann, H. Biochemistry, localization and functional roles of ecto-nucleotidases in the nervous system. Prog. Neurobiol., 1996, 49(6), 589-618. [http://dx.doi.org/10.1016/0301-0082(96)00026-3]. [PMID: 8912394].
[30]
Yegutkin, G.G. Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade. Biochim. Biophys. Acta, 2008, 1783(5), 673-694. [http://dx.doi.org/10. 1016/j.bbamcr.2008.01.024]. [PMID: 18302942].
[31]
Ciruela, F.; Albergaria, C.; Soriano, A.; Cuffí, L.; Carbonell, L.; Sánchez, S.; Gandía, J.; Fernández-Dueñas, V. Adenosine receptors interacting proteins (ARIPs): Behind the biology of adenosine signaling. Biochim. Biophys. Acta, 2010, 1798(1), 9-20. [http://dx. doi.org/10.1016/j.bbamem.2009.10.016]. [PMID: 19883624].
[32]
Cunha, R.A. Different cellular sources and different roles of adenosine: A1 receptor-mediated inhibition through astrocytic-driven volume transmission and synapse-restricted A2A receptor-mediated facilitation of plasticity. Neurochem. Int., 2008, 52(1-2), 65-72. [http://dx.doi.org/10.1016/j.neuint.2007.06.026]. [PMID: 17664029].
[33]
Dias, R.B.; Rombo, D.M.; Ribeiro, J.A.; Henley, J.M.; Sebastião, A.M. Adenosine: setting the stage for plasticity. Trends Neurosci., 2013, 36(4), 248-257. [http://dx.doi.org/10.1016/j.tins.2012.12.003]. [PMID: 23332692].
[34]
Gomes, C.V.; Kaster, M.P.; Tomé, A.R.; Agostinho, P.M.; Cunha, R.A. Adenosine receptors and brain diseases: neuroprotection and neurodegeneration. Biochim. Biophys. Acta, 2011, 1808(5), 1380-1399. [http://dx.doi.org/10.1016/j.bbamem.2010.12.001]. [PMID: 21145878].
[35]
Sperlágh, B.; Vizi, E.S. The role of extracellular adenosine in chemical neurotransmission in the hippocampus and Basal Ganglia: pharmacological and clinical aspects. Curr. Top. Med. Chem., 2011, 11(8), 1034-1046. [http://dx.doi.org/10.2174/156802611795347564]. [PMID: 21401497].
[36]
Coppi, E.; Cellai, L.; Maraula, G.; Dettori, I.; Melani, A.; Pugliese, A.M.; Pedata, F. Role of adenosine in oligodendrocyte precursor maturation. Front. Cell. Neurosci., 2015, 9, 155. [http://dx.doi.org/ 10.3389/fncel.2015.00155]. [PMID: 25964740].
[37]
Kashfi, S.; Ghaedi, K.; Baharvand, H.; Nasr-Esfahani, M.H.; Javan, M. A1 Adenosine receptor activation modulates central nervous system development and repair. Mol. Neurobiol., 2016, 54(10), 8128-8139. [http://dx.doi.org/10.1007/s12035-016-0292-6]. [PMID: 27889899].
[38]
Goding, J.W.; Grobben, B.; Slegers, H. Physiological and pathophysiological functions of the ecto-nucleotide pyrophosphatase/phosphodiesterase family. Biochim. Biophys. Acta, 2003, 1638(1), 1-19. [http://dx.doi.org/10.1016/S0925-4439(03)00058-9]. [PMID: 12757929].
[39]
Stefan, C.; Jansen, S.; Bollen, M. NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem. Sci., 2005, 30(10), 542-550. [http://dx.doi.org/10.1016/j.tibs.2005.08.005]. [PMID: 16125936].
[40]
Vollmayer, P.; Clair, T.; Goding, J.W.; Sano, K.; Servos, J.; Zimmermann, H. Hydrolysis of diadenosine polyphosphates by nucleotide pyrophosphatases/phosphodiesterases In: Eur. J. Biochem / FEBS, 2003, 270(4) 2971-2971
[41]
Emanuelli, T.; Bonan, C.D.; Sarkis, J.J.; Battastini, A.M. Catabolism of Ap4A and Ap5A by rat brain synaptosomes, Brazilian journal of medical and biological research = Revista brasileira de pesquisas medicas e biologicas / Sociedade Brasileira de Biofisica ... [et al.], 1998, 31, 1529-1532..
[42]
Bjelobaba, I.; Nedeljkovic, N.; Subasic, S.; Lavrnja, I.; Pekovic, S.; Stojkov, D.; Rakic, L.; Stojiljkovic, M. Immunolocalization of ecto-nucleotide pyrophosphatase/phosphodiesterase 1 (NPP1) in the rat forebrain. Brain Res., 2006, 1120(1), 54-63. [http://dx. doi.org/10.1016/j.brainres.2006.08.114]. [PMID: 17046728].
[43]
Oaknin, S.; Rodríguez-Ferrer, C.R.; Ramos, A.; Aguilar, J.S.; Rotllán, P. Binding of 5′-O-(2-thiodiphosphate) to rat brain membranes is prevented by diadenosine tetraphosphate and correlates with ecto-nucleotide pyrophosphatase phosphodiesterase 1 (NPP1) activity. Neurosci. Lett., 2008, 432(1), 25-29. [http://dx.doi.org/10. 1016/j.neulet.2007.11.056]. [PMID: 18162317].
[44]
Asensio, A.C.; Rodríguez-Ferrer, C.R.; Castañeyra-Perdomo, A.; Oaknin, S.; Rotllán, P. Biochemical analysis of ecto-nucleotide pyrophosphatase phosphodiesterase activity in brain membranes indicates involvement of NPP1 isoenzyme in extracellular hydrolysis of diadenosine polyphosphates in central nervous system. Neurochem. Int., 2007, 50(4), 581-590. [http://dx.doi.org/10.1016/j. neuint.2006.11.006]. [PMID: 17187902].
[45]
Fuss, B.; Baba, H.; Phan, T.; Tuohy, V.K.; Macklin, W.B.
Phosphodiesterase, I. Phosphodiesterase I, a novel adhesion molecule and/or cytokine involved in oligodendrocyte function. J. Neurosci., 1997, 17(23), 9095-9103. [http://dx.doi.org/10.1523/ JNEUROSCI.17-23-09095.1997]. [PMID: 9364056].
[46]
Xiang, Z.; Burnstock, G. Expression of P2X receptors in rat choroid plexus. Neuroreport, 2005, 16(9), 903-907. [http://dx.doi.org/ 10.1097/00001756-200506210-00006]. [PMID: 15931059].
[47]
Cognato, G. P.; Czepielewski, R.S.; Sarkis, J.J.; Bogo, M.R.; Bonan, C.D. Expression mapping of ectonucleotide pyrophosphatase/phosphodiesterase 1-3 (E-NPP1-3) in different brain structures during rat development. Int. J. Dev. Neurosci., 2008, 26(6), 593-598. [http://dx.doi.org/10.1016/j.ijdevneu.2008.05.001]. [PMID: 18565716].
[48]
Bächner, D.; Ahrens, M.; Betat, N.; Schröder, D.; Gross, G. Developmental expression analysis of murine autotaxin (ATX). Mech. Dev., 1999, 84(1-2), 121-125. [http://dx.doi.org/10.1016/S0925-4773(99)00048-9]. [PMID: 10473125].
[49]
Ohuchi, H.; Hayashibara, Y.; Matsuda, H.; Onoi, M.; Mitsumori, M.; Tanaka, M.; Aoki, J.; Arai, H.; Noji, S. Diversified expression patterns of autotaxin, a gene for phospholipid-generating enzyme during mouse and chicken development. Dev. Dyn., 2007, 236(4), 1134-1143. [http://dx.doi.org/10.1002/dvdy.21119]. [PMID: 17366625].
[50]
Fox, M.A.; Alexander, J.K.; Afshari, F.S.; Colello, R.J.; Fuss, B. Phosphodiesterase-I alpha/autotaxin controls cytoskeletal organization and FAK phosphorylation during myelination. Mol. Cell. Neurosci., 2004, 27(2), 140-150. [http://dx.doi.org/10.1016/j.mcn. 2004.06.002]. [PMID: 15485770].
[51]
Fox, M.A.; Colello, R.J.; Macklin, W.B.; Fuss, B. Phosphodiesterase-Ialpha/autotaxin: a counteradhesive protein expressed by oligodendrocytes during onset of myelination. Mol. Cell. Neurosci., 2003, 23(3), 507-519. [http://dx.doi.org/10.1016/S1044-7431(03) 00073-3]. [PMID: 12837632].
[52]
Dennis, J.; Nogaroli, L.; Fuss, B. Phosphodiesterase-Ialpha/ autotaxin (PD-Ialpha/ATX): a multifunctional protein involved in central nervous system development and disease. J. Neurosci. Res., 2005, 82(6), 737-742. [http://dx.doi.org/10.1002/jnr.20686]. [PMID: 16267828].
[53]
Yuelling, L.M.; Fuss, B. Autotaxin (ATX): a multi-functional and multi-modular protein possessing enzymatic lysoPLD activity and matricellular properties. Biochim. Biophys. Acta, 2008, 1781(9), 525-530. [http://dx.doi.org/10.1016/j.bbalip.2008.04.009]. [PMID: 18485925].
[54]
Ohuchi, H.; Fukui, H.; Matsuyo, A.; Tomonari, S.; Tanaka, M.; Arai, H.; Noji, S.; Aoki, J. Autotaxin controls caudal diencephalon-mesencephalon development in the chick. Dev. Dyn., 2010, 239(10), 2647-2658. [http://dx.doi.org/10.1002/dvdy.22403]. [PMID: 20737506].
[55]
Kingsbury, M.A.; Rehen, S.K.; Contos, J.J.; Higgins, C.M.; Chun, J. Non-proliferative effects of lysophosphatidic acid enhance cortical growth and folding. Nat. Neurosci., 2003, 6(12), 1292-1299. [http://dx.doi.org/10.1038/nn1157]. [PMID: 14625558].
[56]
van Meeteren, L.A.; Moolenaar, W.H. Regulation and biological activities of the autotaxin-LPA axis. Prog. Lipid Res., 2007, 46(2), 145-160. [http://dx.doi.org/10.1016/j.plipres.2007.02.001]. [PMID: 17459484].
[57]
Fotopoulou, S.; Oikonomou, N.; Grigorieva, E.; Nikitopoulou, I.; Paparountas, T.; Thanassopoulou, A.; Zhao, Z.; Xu, Y.; Kontoyiannis, D.L.; Remboutsika, E.; Aidinis, V. ATX expression and LPA signalling are vital for the development of the nervous system. Dev. Biol., 2010, 339(2), 451-464. [http://dx.doi.org/10.1016/ j.ydbio.2010.01.007]. [PMID: 20079728].
[58]
Inoue, M.; Rashid, M.H.; Fujita, R.; Contos, J.J.; Chun, J.; Ueda, H. Initiation of neuropathic pain requires lysophosphatidic acid receptor signaling. Nat. Med., 2004, 10(7), 712-718. [http://dx.doi. org/10.1038/nm1060]. [PMID: 15195086].
[59]
Yung, Y.C.; Mutoh, T.; Lin, M.E.; Noguchi, K.; Rivera, R.R.; Choi, J.W.; Kingsbury, M.A.; Chun, J. Lysophosphatidic acid signaling may initiate fetal hydrocephalus. Sci. Transl. Med., 2011, 3(99), 99ra87. [http://dx.doi.org/10.1126/scitranslmed.3002095]. [PMID: 21900594].
[60]
Moolenaar, W.H.; Houben, A.J.; Lee, S.J.; van Meeteren, L.A. Autotaxin in embryonic development. Biochim. Biophys. Acta, 2013, 1831(1), 13-19. [http://dx.doi.org/10.1016/j.bbalip.2012. 09.013]. [PMID: 23022664].
[61]
Koike, S.; Keino-Masu, K.; Masu, M. Deficiency of autotaxin/lysophospholipase D results in head cavity formation in mouse embryos through the LPA receptor-Rho-ROCK pathway. Biochem. Biophys. Res. Commun., 2010, 400(1), 66-71. [http://dx. doi.org/10.1016/j.bbrc.2010.08.008]. [PMID: 20692235].
[62]
van Meeteren, L.A.; Ruurs, P.; Stortelers, C.; Bouwman, P.; van Rooijen, M.A.; Pradère, J.P.; Pettit, T.R.; Wakelam, M.J.; Saulnier-Blache, J.S.; Mummery, C.L.; Moolenaar, W.H.; Jonkers, J. Autotaxin, a secreted lysophospholipase D, is essential for blood vessel formation during development. Mol. Cell. Biol., 2006, 26(13), 5015-5022. [http://dx.doi.org/10.1128/MCB.02419-05]. [PMID: 16782887].
[63]
Blass-Kampmann, S.; Kindler-Röhrborn, A.; Deissler, H.; D’Urso, D.; Rajewsky, M.F. In vitro differentiation of neural progenitor cells from prenatal rat brain: common cell surface glycoprotein on three glial cell subsets. J. Neurosci. Res., 1997, 48(2), 95-111. [http://dx.doi.org/10.1002/(SICI)1097-4547(19970415)48:2<95: AID-JNR2>3.0.CO;2-7]. [PMID: 9130138].
[64]
Deissler, H.; Blass-Kampmann, S.; Bruyneel, E.; Mareel, M.
Rajewsky, M.F. Neural cell surface differentiation antigen gp130(RB13-6) induces fibroblasts and glioma cells to express astroglial proteins and invasive properties. FASEB J., 1999, 13(6), 657-666. [http://dx.doi.org/10.1096/fasebj.13.6.657]. [PMID: 10094926].
[65]
Gómez-Villafuertes, R.; Pintor, J.; Miras-Portugal, M.T.; Gualix, J. Ectonucleotide pyrophosphatase/phosphodiesterase activity in Neuro-2a neuroblastoma cells: changes in expression associated with neuronal differentiation. J. Neurochem., 2014, 131(3), 290-302. [http://dx.doi.org/10.1111/jnc.12794]. [PMID: 24947519].
[66]
Millán, J.L. Alkaline Phosphatases: Structure, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signal., 2006, 2(2), 335-341. [http://dx. doi.org/10.1007/s11302-005-5435-6]. [PMID: 18404473].
[67]
Sebastián-Serrano, Á.; de Diego-García, L.; Martínez-Frailes, C.; Ávila, J.; Zimmermann, H.; Millán, J.L.; Miras-Portugal, M.T.; Díaz-Hernández, M. Tissue-nonspecific Alkaline Phosphatase Regulates purinergic transmission in the central nervous System during development and disease. Comput. Struct. Biotechnol. J., 2014, 13, 95-100. [http://dx.doi.org/10.1016/j.csbj.2014.12.004]. [PMID: 25709758].
[68]
Langer, D.; Hammer, K.; Koszalka, P.; Schrader, J.; Robson, S.; Zimmermann, H. Distribution of ectonucleotidases in the rodent brain revisited. Cell Tissue Res., 2008, 334(2), 199-217. [http://dx.doi.org/10.1007/s00441-008-0681-x]. [PMID: 18843508].
[69]
Fonta, C.; Négyessy, L.; Renaud, L.; Barone, P. Areal and subcellular localization of the ubiquitous alkaline phosphatase in the primate cerebral cortex: evidence for a role in neurotransmission. Cereb. Cortex, 2004, 14(6), 595-609. [http://dx.doi.org/10.1093/ cercor/bhh021]. [PMID: 15054075].
[70]
Ermonval, M.; Baudry, A.; Baychelier, F.; Pradines, E.; Pietri, M.; Oda, K.; Schneider, B.; Mouillet-Richard, S.; Launay, J.M.; Kellermann, O. The cellular prion protein interacts with the tissue non-specific alkaline phosphatase in membrane microdomains of bioaminergic neuronal cells. PLoS One, 2009, 4(8), e6497. [http://dx.doi.org/10.1371/journal.pone.0006497]. [PMID: 19652718].
[71]
Scheibe, R.J.; Kuehl, H.; Krautwald, S.; Meissner, J.D.; Mueller, W.H. Ecto-alkaline phosphatase activity identified at physiological pH range on intact P19 and HL-60 cells is induced by retinoic acid. J. Cell. Biochem., 2000, 76(3), 420-436. [http://dx.doi.org/10.1002/ (SICI)1097-4644(20000301)76:3<420:AID-JCB10>3.0.CO;2-F]. [PMID: 10649440].
[72]
Noda, T.; Tokuda, H.; Yoshida, M.; Yasuda, E.; Hanai, Y.; Takai, S.; Kozawa, O. Possible involvement of phosphatidylinositol 3- kinase/Akt pathway in insulin-like growth factor-I-induced alkaline phosphatase activity in osteoblasts, Hormone and metabolic research = Hormon- und Stoffwechselforschung = Hormones et metabolisme, 2005, 37, 270-274.
[73]
Díez-Zaera, M.; Díaz-Hernández, J.I.; Hernández-Álvarez, E.; Zimmermann, H.; Díaz-Hernández, M.; Miras-Portugal, M.T. Tissue-nonspecific alkaline phosphatase promotes axonal growth of hippocampal neurons. Mol. Biol. Cell, 2011, 22(7), 1014-1024. [http://dx.doi.org/10.1091/mbc.e10-09-0740]. [PMID: 21289095].
[74]
Heo, J.S.; Han, H.J. ATP stimulates mouse embryonic stem cell proliferation via protein kinase C, phosphatidylinositol 3-kinase/Akt, and mitogen-activated protein kinase signaling pathways. Stem Cells, 2006, 24(12), 2637-2648. [http://dx.doi.org/ 10.1634/stemcells.2005-0588]. [PMID: 16916926].
[75]
Kermer, V.; Ritter, M.; Albuquerque, B.; Leib, C.; Stanke, M.; Zimmermann, H. Knockdown of tissue nonspecific alkaline phosphatase impairs neural stem cell proliferation and differentiation. Neurosci. Lett., 2010, 485(3), 208-211. [http://dx.doi.org/10.1016/ j.neulet.2010.09.013]. [PMID: 20849921].
[76]
Narisawa, S.; Hasegawa, H.; Watanabe, K.; Millán, J.L. Stage-specific expression of alkaline phosphatase during neural development in the mouse. Dev. Dyn., 1994, 201(3), 227-235. [http://dx. doi.org/10.1002/aja.1002010306]. [PMID: 7533563].
[77]
Harada, H.; Chan, C.M.; Loesch, A.; Unwin, R.; Burnstock, G. Induction of proliferation and apoptotic cell death via P2Y and P2X receptors, respectively, in rat glomerular mesangial cells. Kidney Int., 2000, 57(3), 949-958. [http://dx.doi.org/10.1046/j.1523-1755. 2000.00911.x]. [PMID: 10720948].
[78]
Buffo, A.; Vosko, M.R.; Ertürk, D.; Hamann, G.F.; Jucker, M.; Rowitch, D.; Götz, M. Expression pattern of the transcription factor Olig2 in response to brain injuries: implications for neuronal repair. Proc. Natl. Acad. Sci. USA, 2005, 102(50), 18183-18188. [http:// dx.doi.org/10.1073/pnas.0506535102]. [PMID: 16330768].
[79]
Caillé, I.; Allinquant, B.; Dupont, E.; Bouillot, C.; Langer, A.; Müller, U.; Prochiantz, A. Soluble form of amyloid precursor protein regulates proliferation of progenitors in the adult subventricular zone. Development, 2004, 131(9), 2173-2181. [http://dx.doi.org/ 10.1242/dev.01103]. [PMID: 15073156].
[80]
Langer, D.; Ikehara, Y.; Takebayashi, H.; Hawkes, R.; Zimmermann, H. 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, 2007, 150(4), 863-879. [http://dx.doi.org/10.1016/j.neuroscience.2007.07.064]. [PMID: 18031938].
[81]
Yoshioka, T.; Tanaka, O. Histochemical localization of Ca2+, Mg2+-ATPase of the rat cerebellar cortex during postnatal development. Int. J. Dev. Neurosci., 1989, 7(2), 181-193. [http://dx.doi. org/10.1016/0736-5748(89)90068-3]. [PMID: 2523632].
[82]
Fonta, C.; Negyessy, L.; Renaud, L.; Barone, P. Postnatal development of alkaline phosphatase activity correlates with the maturation of neurotransmission in the cerebral cortex. J. Comp. Neurol., 2005, 486(2), 179-196. [http://dx.doi.org/10.1002/cne.20524]. [PMID: 15844208].
[83]
Hanics, J.; Barna, J.; Xiao, J.; Millán, J.L.; Fonta, C.; Négyessy, L. Ablation of TNAP function compromises myelination and synaptogenesis in the mouse brain. Cell Tissue Res., 2012, 349(2), 459-471. [http://dx.doi.org/10.1007/s00441-012-1455-z]. [PMID: 22696173].
[84]
Waymire, K.G.; Mahuren, J.D.; Jaje, J.M.; Guilarte, T.R.; Coburn, S.P.; MacGregor, G.R. Mice lacking tissue non-specific alkaline phosphatase die from seizures due to defective metabolism of vitamin B-6. Nat. Genet., 1995, 11(1), 45-51. [http://dx.doi.org/10. 1038/ng0995-45]. [PMID: 7550313].
[85]
Narisawa, S.; Wennberg, C.; Millán, J.L. Abnormal vitamin B6 metabolism in alkaline phosphatase knock-out mice causes multiple abnormalities, but not the impaired bone mineralization. J. Pathol., 2001, 193(1), 125-133. [http://dx.doi.org/10.1002/1096-9896(2000)9999:9999<:AID-PATH722>3.0.CO;2-Y]. [PMID: 11169525].
[86]
Vorhoff, T.; Zimmermann, H.; Pelletier, J.; Sévigny, J.; Braun, N. Cloning and characterization of the ecto-nucleotidase NTPDase3 from rat brain: Predicted secondary structure and relation to other members of the E-NTPDase family and actin. Purinergic Signal., 2005, 1(3), 259-270. [http://dx.doi.org/10.1007/s11302-005-6314-x]. [PMID: 18404510].
[87]
Cunha, R.A. Regulation of the ecto-nucleotidase pathway in rat hippocampal nerve terminals. Neurochem. Res., 2001, 26(8-9), 979-991. [http://dx.doi.org/10.1023/A:1012392719601]. [PMID: 11699950].
[88]
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.; Weisman, G.A. International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol. Rev., 2006, 58(3), 281-341. [http://dx.doi.org/10.1124/ pr.58.3.3]. [PMID: 16968944].
[89]
Wu, Y.; Sun, X.; Kaczmarek, E.; Dwyer, K.M.; Bianchi, E.; Usheva, A.; Robson, S.C. RanBPM associates with CD39 and modulates ecto-nucleotidase activity. Biochem. J., 2006, 396(1), 23-30. [http://dx.doi.org/10.1042/BJ20051568]. [PMID: 16478441].
[90]
Wang, T.F.; Guidotti, G. Widespread expression of ecto-apyrase (CD39) in the central nervous system. Brain Res., 1998, 790(1-2), 318-322. [http://dx.doi.org/10.1016/S0006-8993(97)01562-X]. [PMID: 9593967].
[91]
Braun, N.; Sévigny, J.; Robson, S.C.; Enjyoji, K.; Guckelberger, O.; Hammer, K.; Di Virgilio, F.; Zimmermann, H. Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculature of the brain. Eur. J. Neurosci., 2000, 12(12), 4357-4366. [PMID: 11122346].
[92]
Bjelobaba, I.; Stojiljkovic, M.; Pekovic, S.; Dacic, S.; Lavrnja, I.; Stojkov, D.; Rakic, L.; Nedeljkovic, N. Immunohistological determination of ecto-nucleoside triphosphate diphosphohydrolase1 (NTPDase1) and 5′-nucleotidase in rat hippocampus reveals overlapping distribution. Cell. Mol. Neurobiol., 2007, 27(6), 731-743. [http://dx.doi.org/10.1007/s10571-007-9159-8]. [PMID: 17619139].
[93]
Aliagas, E.; Villar-Menéndez, I.; Sévigny, J.; Roca, M.; Romeu, M.; Ferrer, I.; Martín-Satué, M.; Barrachina, M. Reduced striatal ecto-nucleotidase activity in schizophrenia patients supports the “adenosine hypothesis”. Purinergic Signal., 2013, 9(4), 599-608. [http://dx.doi.org/10.1007/s11302-013-9370-7]. [PMID: 23771238].
[94]
Braun, N.; Sévigny, J.; Mishra, S.K.; Robson, S.C.; Barth, S.W.; Gerstberger, R.; Hammer, K.; Zimmermann, H. Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur. J. Neurosci., 2003, 17(7), 1355-1364. [http://dx.doi.org/10.1046/j.1460-9568.2003.02567.x]. [PMID: 12713638].
[95]
Wink, M.R.; Braganhol, E.; Tamajusuku, A.S.; Lenz, G.; Zerbini, L.F.; Libermann, T.A.; Sévigny, J.; Battastini, A.M.; Robson, S.C. Nucleoside triphosphate diphosphohydrolase-2 (NTPDase2/ CD39L1) is the dominant ectonucleotidase expressed by rat astrocytes. Neuroscience, 2006, 138(2), 421-432. [http://dx.doi. org/10.1016/j.neuroscience.2005.11.039]. [PMID: 16414200].
[96]
Gampe, K.; Hammer, K.; Kittel, Á.; Zimmermann, H. The medial habenula contains a specific nonstellate subtype of astrocyte expressing the ectonucleotidase NTPDase2. Glia, 2012, 60(12), 1860-1870. [http://dx.doi.org/10.1002/glia.22402]. [PMID: 22865704].
[97]
Wink, M.R.; Braganhol, E.; Tamajusuku, A.S.; Casali, E.A.; Karl, J.; Barreto-Chaves, M.L.; Sarkis, J.J.; Battastini, A.M. Extracellular adenine nucleotides metabolism in astrocyte cultures from different brain regions. Neurochem. Int., 2003, 43(7), 621-628. [http:// dx.doi.org/10.1016/S0197-0186(03)00094-9]. [PMID: 12892649].
[98]
Shukla, V.; Zimmermann, H.; Wang, L.; Kettenmann, H.; Raab, S.; Hammer, K.; Sévigny, J.; Robson, S.C.; Braun, N. Functional expression of the ecto-ATPase NTPDase2 and of nucleotide receptors by neuronal progenitor cells in the adult murine hippocampus. J. Neurosci. Res., 2005, 80(5), 600-610. [http://dx. doi.org/10.1002/jnr.20508]. [PMID: 15884037].
[99]
Belcher, S.M.; Zsarnovszky, A.; Crawford, P.A.; Hemani, H.; Spurling, L.; Kirley, T.L. Immunolocalization of ecto-nucleoside triphosphate diphosphohydrolase 3 in rat brain: implications for modulation of multiple homeostatic systems including feeding and sleep-wake behaviors. Neuroscience, 2006, 137(4), 1331-1346. [http://dx.doi.org/10.1016/j.neuroscience.2005.08.086]. [PMID: 16338080].
[100]
Grković, I.; Bjelobaba, I.; Mitrović, N.; Lavrnja, I.; Drakulić, D.; Martinović, J.; Stanojlović, M.; Horvat, A.; Nedeljković, N. Expression of ecto-nucleoside triphosphate diphosphohydrolase3 (NTPDase3) in the female rat brain during postnatal development. J. Chem. Neuroanat., 2016, 77, 10-18. [http://dx.doi.org/10.1016/ j.jchemneu.2016.04.001]. [PMID: 27049676].
[101]
Kiss, D.S.; Zsarnovszky, A.; Horvath, K.; Gyorffy, A.; Bartha, T.; Hazai, D.; Sotonyi, P.; Somogyi, V.; Frenyo, L.V.; Diano, S. Ecto-nucleoside triphosphate diphosphohydrolase 3 in the ventral and lateral hypothalamic area of female rats: morphological characterization and functional implications. Reprod. Biol. Endocrinol., 2009, 7, 31. [http://dx.doi.org/10.1186/1477-7827-7-31]. [PMID: 19383175].
[102]
Bjelobaba, I.; Lavrnja, I.; Parabucki, A.; Stojkov, D.; Stojiljkovic, M.; Pekovic, S.; Nedeljkovic, N. The cortical stab injury induces beading of fibers expressing ecto-nucleoside triphosphate diphosphohydrolase 3. Neuroscience, 2010, 170(1), 107-116. [http://dx. doi.org/10.1016/j.neuroscience.2010.06.063]. [PMID: 20620196].
[103]
Stoyanova, I.I., II; Rutten, W.L.; le Feber, J. Orexin-A and orexin-B during the postnatal development of the rat brain. Cell. Mol. Neurobiol., 2010, 30(1), 81-89. [http://dx.doi.org/10.1007/s10571-009-9433-z]. [PMID: 19633949].
[104]
Yamamoto, Y.; Ueta, Y.; Hara, Y.; Serino, R.; Nomura, M.; Shibuya, I.; Shirahata, A.; Yamashita, H. Postnatal development of orexin/hypocretin in rats. Brain Res. Mol. Brain Res., 2000, 78(1-2), 108-119. [http://dx.doi.org/10.1016/S0169-328X(00)00080-2]. [PMID: 10891590].
[105]
Kulesskaya, N.; Võikar, V.; Peltola, M.; Yegutkin, G.G.; Salmi, M.; Jalkanen, S.; Rauvala, H. CD73 is a major regulator of adenosinergic signalling in mouse brain. PLoS One, 2013, 8(6), e66896. [http://dx.doi.org/10.1371/journal.pone.0066896]. [PMID: 23776700].
[106]
Zimmermann, H. 5′-Nucleotidase: molecular structure and functional aspects. Biochem. J., 1992, 285(Pt 2), 345-365. [http://dx. doi.org/10.1042/bj2850345]. [PMID: 1637327].
[107]
Bjelobaba, I.; Parabucki, A.; Lavrnja, I.; Stojkov, D.; Dacic, S.; Pekovic, S.; Rakic, L.; Stojiljkovic, M.; Nedeljkovic, N. Dynamic changes in the expression pattern of ecto-5′-nucleotidase in the rat model of cortical stab injury. J. Neurosci. Res., 2011, 89(6), 862-873. [http://dx.doi.org/10.1002/jnr.22599]. [PMID: 21337375].
[108]
Vogel, M.; Zimmermann, H.; Singer, W. Transient association of the HNK-1 epitope with 5′-nucleotidase during development of the cat visual cortex. Eur. J. Neurosci., 1993, 5(11), 1423-1425. [http://dx.doi.org/10.1111/j.1460-9568.1993.tb00209.x]. [PMID: 7506969].
[109]
Fenoglio, C.; Scherini, E.; Vaccarone, R.; Bernocchi, G. A re-evaluation of the ultrastructural localization of 5′-nucleotidase activity in the developing rat cerebellum, with a cerium-based method. J. Neurosci. Methods, 1995, 59(2), 253-263. [http://dx. doi.org/10.1016/0165-0270(94)00211-X]. [PMID: 8531494].
[110]
Schoen, S.W.; Graeber, M.B.; Tóth, L.; Kreutzberg, G.W. 5′-Nucleotidase in postnatal ontogeny of rat cerebellum: a marker for migrating nerve cells? Brain Res., 1988, 467(1), 125-136. [http://dx.doi.org/10.1016/0165-3806(88)90074-0]. [PMID: 2834026].
[111]
Lie, A.A.; Blümcke, I.; Beck, H.; Wiestler, O.D.; Elger, C.E.; Schoen, S.W. 5′-Nucleotidase activity indicates sites of synaptic plasticity and reactive synaptogenesis in the human brain. J. Neuropathol. Exp. Neurol., 1999, 58(5), 451-458. [http://dx.doi.org/10. 1097/00005072-199905000-00004]. [PMID: 10331433].
[112]
de Paula Cognato, G.; Bruno, A.N.; Vuaden, F.C.; Sarkis, J.J.; Bonan, C.D. Ontogenetic profile of ectonucleotidase activities from brain synaptosomes of pilocarpine-treated rats. Int. J. Dev. Neurosci., 2005, 23(8), 703-709. [http://dx.doi.org/10.1016/j.ijdevneu. 2005.09.001]. [PMID: 16274951].
[113]
Mackiewicz, M.; Nikonova, E.V.; Zimmermann, J.E.; Romer, M.A.; Cater, J.; Galante, R.J.; Pack, A.I. Age-related changes in adenosine metabolic enzymes in sleep/wake regulatory areas of the brain. Neurobiol. Aging, 2006, 27(2), 351-360. [http://dx.doi. org/10.1016/j.neurobiolaging.2005.01.015]. [PMID: 16399217].
[114]
Grkovic, I.; Bjelobaba, I.; Nedeljkovic, N.; Mitrovic, N.; Drakulic, D.; Stanojlovic, M.; Horvat, A. Developmental increase in ecto-5′-nucleotidase activity overlaps with appearance of two immunologically distinct enzyme isoforms in rat hippocampal synaptic plasma membranes. J. Mol. Neurosci., 2014, 54, 109-118.
[115]
Stanojević, I.; Bjelobaba, I.; Nedeljković, N.; Drakulić, D.; Petrović, S.; Stojiljković, M.; Horvat, A. Ontogenetic profile of ecto-5′-nucleotidase in rat brain synaptic plasma membranes. Int. J. Dev. Neurosci., 2011, 29(4), 397-403. [http://dx.doi.org/10.1016/ j.ijdevneu.2011.03.003]. [PMID: 21414400].
[116]
Torres, I.L.; Battastini, A.M.; Buffon, A.; Fürstenau, C.R.; Siqueira, I.; Sarkis, J.J.; Dalmaz, C.; Ferreira, M.B. Ecto-nucleotidase activities in spinal cord of rats changes as function of age. Int. J. Dev. Neurosci., 2003, 21(8), 425-429. [http://dx.doi.org/ 10.1016/j.ijdevneu.2003.10.001]. [PMID: 14659993].
[117]
Fuchs, J.L. 5′-Nucleotidase activity increases in aging rat brain. Neurobiol. Aging, 1991, 12(5), 523-530. [http://dx.doi.org/10. 1016/0197-4580(91)90083-V]. [PMID: 1770988].
[118]
Spychala, J.; Zimmermann, A.G.; Mitchell, B.S. Tissue-specific regulation of the ecto-5′-nucleotidase promoter. Role of the camp response element site in mediating repression by the upstream regulatory region. J. Biol. Chem., 1999, 274(32), 22705-22712. [http://dx.doi.org/10.1074/jbc.274.32.22705]. [PMID: 10428853].
[119]
Dickins, E.M.; Salinas, P.C. Wnts in action: from synapse formation to synaptic maintenance. Front. Cell. Neurosci., 2013, 7, 162. [http://dx.doi.org/10.3389/fncel.2013.00162]. [PMID: 24223536].
[120]
Ille, F.; Sommer, L. Wnt signaling: multiple functions in neural development. Cell. Mol. Life Sci., 2005, 62(10), 1100-1108. [http://dx.doi.org/10.1007/s00018-005-4552-2]. [PMID: 15928805].
[121]
Salinas, P.C. Wnt signaling in the vertebrate central nervous system: from axon guidance to synaptic function. Cold Spring Harb. Perspect. Biol., 2012, 4(2), 4. [http://dx.doi.org/10.1101/ cshperspect.a008003]. [PMID: 22300976].
[122]
Kohring, K.; Zimmermann, H. Upregulation of ecto-5′-nucleotidase in human neuroblastoma SH-SY5Y cells on differentiation by retinoic acid or phorbolester. Neurosci. Lett., 1998, 258(3), 127-130. [http://dx.doi.org/10.1016/S0304-3940(98)00833-7]. [PMID: 9885947].
[123]
Spychala, J.; Mitchell, B.S.; Barankiewicz, J. Adenosine metabolism during phorbol myristate acetate-mediated induction of HL-60 cell differentiation: changes in expression pattern of adenosine kinase, adenosine deaminase, and 5′-nucleotidase. J. Immunol., 1997, 158(10), 4947-4952. [PMID: 9144513].
[124]
Bavaresco, L.; Bernardi, A.; Braganhol, E.; Wink, M.R.; Battastini, A.M. Dexamethasone inhibits proliferation and stimulates ecto-5′-nucleotidase/CD73 activity in C6 rat glioma cell line. J. Neurooncol., 2007, 84(1), 1-8. [http://dx.doi.org/10.1007/s11060-007-9342-2]. [PMID: 17453149].
[125]
Mitrović, N.; Guševac, I.; Drakulić, D.; Stanojlović, M.; Zlatković, J.; Sévigny, J.; Horvat, A.; Nedeljković, N.; Grković, I. Regional and sex-related differences in modulating effects of female sex steroids on ecto-5′-nucleotidase expression in the rat cerebral cortex and hippocampus. Gen. Comp. Endocrinol., 2016, 235, 100-107. [http://dx.doi.org/10.1016/j.ygcen.2016.06.018]. [PMID: 27296672].
[126]
Mitrović, N.; Zarić, M.; Drakulić, D.; Martinović, J.; Stanojlović, M.; Sévigny, J.; Horvat, A.; Nedeljković, N.; Grković, I. 17β-Estradiol upregulates ecto-5′-nucleotidase (CD73) in hippocampal synaptosomes of female rats through action mediated by estrogen receptor-α and -β. Neuroscience, 2016, 324, 286-296. [http://dx. doi.org/10.1016/j.neuroscience.2016.03.022]. [PMID: 26987957].
[127]
Díaz-Hernandez, M.; del Puerto, A.; Díaz-Hernandez, J.I.; Diez-Zaera, M.; Lucas, J.J.; Garrido, J.J.; Miras-Portugal, M.T. Inhibition of the ATP-gated P2X7 receptor promotes axonal growth and branching in cultured hippocampal neurons. J. Cell Sci., 2008, 121(Pt 22), 3717-3728. [http://dx.doi.org/10.1242/jcs.034082]. [PMID: 18987356].
[128]
Cheung, K.K.; Chan, W.Y.; Burnstock, G. Expression of P2X purinoceptors during rat brain development and their inhibitory role on motor axon outgrowth in neural tube explant cultures. Neuroscience, 2005, 133(4), 937-945. [http://dx.doi.org/10.1016/ j.neuroscience.2005.03.032]. [PMID: 15964486].
[129]
Abbracchio, M.P.; Cattabeni, F.; Clementi, F.; Sher, E. Adenosine receptors linked to adenylate cyclase activity in human neuroblastoma cells: modulation during cell differentiation. Neuroscience, 1989, 30(3), 819-825. [http://dx.doi.org/10.1016/0306-4522(89) 90173-5]. [PMID: 2771050].
[130]
Heilbronn, A.; Maienschein, V.; Carstensen, K.; Gann, W.; Zimmermann, H. Crucial role of ecto-5′-nucleotidase in differentiation and survival of developing neural cells. Neuroreport, 1995, 7(1), 257-261. [PMID: 8742465].
[131]
Brändle, U.; Zenner, H.P.; Ruppersberg, J.P. Gene expression of P2X-receptors in the developing inner ear of the rat. Neurosci. Lett., 1999, 273(2), 105-108. [http://dx.doi.org/10.1016/S0304-3940(99)00648-5]. [PMID: 10505627].
[132]
Kukulski, F.; Komoszynski, M. Purification and characterization of NTPDase1 (ecto-apyrase) and NTPDase2 (ecto-ATPase) from porcine brain cortex synaptosomes. Eur. J. Biochem / FEB, 2003, 270(16), 3447-3454.
[133]
Mitrovic, N.; Zaric, M.; Drakulic, D.; Martinovic, J.; Sevigny, J.; Stanojlovic, M.; Nedeljkovic, N.; Grkovic, I. 17beta-Estradiol-induced synaptic rearrangements are accompanied by altered ectonucleotidase activities in male rat hippocampal synaptosomes. J. Mol. Neurosci., 2016, 61(3), 412-422.
[134]
Augusto, E.; Matos, M.; Sévigny, J.; El-Tayeb, A.; Bynoe, M.S.; Müller, C.E.; Cunha, R.A.; Chen, J.F. Ecto-5′-nucleotidase (CD73)-mediated formation of adenosine is critical for the striatal adenosine A2A receptor functions. J. Neurosci., 2013, 33(28), 11390-11399. [http://dx.doi.org/10.1523/JNEUROSCI.5817-12.2013]. [PMID: 23843511].
[135]
Négyessy, L.; Xiao, J.; Kántor, O.; Kovács, G.G.; Palkovits, M.; Dóczi, T.P.; Renaud, L.; Baksa, G.; Glasz, T.; Ashaber, M.; Barone, P.; Fonta, C. Layer-specific activity of tissue non-specific alkaline phosphatase in the human neocortex. Neuroscience, 2011, 172, 406-418. [http://dx.doi.org/10.1016/j.neuroscience.2010.10. 049]. [PMID: 20977932].
[136]
Müller, J.; Rocha, J.B.; Battastini, A.M.; Sarkis, J.J.; Dias, R.D. Postnatal development of ATPase-ADPase activities in synaptosomal fraction from cerebral cortex of rats. Neurochem. Int., 1993, 23(5), 471-477. [http://dx.doi.org/10.1016/0197-0186(93)90132-O]. [PMID: 8251929].
[137]
Oliveira, E.M.; Rocha, J.B.; Sarkis, J.J. In vitro and in vivo effects of HgCl2 on synaptosomal ATP diphosphohydrolase (EC 3.6.1.5) from cerebral cortex of developing rats. Arch. Int. Physiol. Biochim. Biophys., 1994, 102(5), 251-254. [http://dx.doi.org/10.3109/ 13813459409003939]. [PMID: 7849271].
[138]
Muller, J.; Rocha, J.B.; Battastini, A.M.; Sarkis, J.J.; Dias, R.D. dias, ontogeny of ATP and ADP hydrolysis by cerebral cortex synaptosomes from rats. Braz.J. Med. Biol., 1990, 23(10), 935-939.
[139]
Nedeljkovic, N.; Banjac, A.; Horvat, A.; Stojiljkovic, M.; Nikezic, G. Developmental profile of NTPDase activity in synaptic plasma membranes isolated from rat cerebral cortex. Int. J. Dev. Neurosci., 2005, 23(1), 45-51. [http://dx.doi.org/10.1016/j.ijdevneu.2004.09.001]. [PMID: 15730886].
[140]
Banjac, A.; Nedeljkovic, N.; Horvat, A.; Kanazir, D.; Nikezic, G. Ontogenetic profile of ecto-ATPase activity in rat hippocampal and caudate nucleus synaptic plasma membrane fractions. Physiol. Res., 2001, 50, 411-417.
[141]
Johansson, B.; Georgiev, V.; Fredholm, B.B. Distribution and postnatal ontogeny of adenosine A2A receptors in rat brain: comparison with dopamine receptors. Neuroscience, 1997, 80(4), 1187-1207. [http://dx.doi.org/10.1016/S0306-4522(97)00143-7]. [PMID: 9284070].
[142]
Ahmed, O.M.; El-Gareib, A.W.; El-Bakry, A.M.; Abd El-Tawab, S.M.; Ahmed, R.G. Thyroid hormones states and brain development interactions. Int. J. Dev. Neurosci., 2008, 26(2), 147-209. [http:// dx.doi.org/10.1016/j.ijdevneu.2007.09.011]. [PMID: 18031969].
[143]
Bruno, A.N.; Ricachenevsky, F.K.; Pochmann, D.; Bonan, C.D.; Battastini, A.M.; Barreto-Chaves, M.L.; Sarkis, J.J. Hypothyroidism changes adenine nucleotide hydrolysis in synaptosomes from hippocampus and cerebral cortex of rats in different phases of development. Int. J. Dev. Neurosci., 2005, 23(1), 37-44. [http://dx. doi.org/10.1016/j.ijdevneu.2004.09.003]. [PMID: 15730885].
[144]
Bruno, A.N.; Da Silva, R.S.; Bonan, C.D.; Battastini, A.M.; Barreto-chaves, M.L.; Sarkis, J.J. Hyperthyroidism modifies ecto-nucleotidase activities in synaptosomes from hippocampus and cerebral cortex of rats in different phases of development. Int. J. Dev. Neurosci., 2003, 21(7), 401-408. [http://dx.doi.org/10.1016/ S0736-5748(03)00088-1]. [PMID: 14599486].
[145]
Braganhol, E.; Bruno, A.N.; Bavaresco, L.; Barreto-Chaves, M.L.; Sarkis, J.J.; Battastini, A.M. Neonatal hypothyroidism affects the adenine nucleotides metabolism in astrocyte cultures from rat brain. Neurochem. Res., 2006, 31(4), 449-454. [http://dx.doi.org/ 10.1007/s11064-006-9041-y]. [PMID: 16758352].
[146]
Cognato, G.P.; Vuaden, F.C.; Savio, L.E.; Bellaver, B.; Casali, E.; Bogo, M.R.; Souza, D.O.; Sévigny, J.; Bonan, C.D. Nucleoside triphosphate diphosphohydrolases role in the pathophysiology of cognitive impairment induced by seizure in early age. Neuroscience, 2011, 180, 191-200. [http://dx.doi.org/10.1016/j.neuroscience. 2011.01.065]. [PMID: 21315806].
[147]
Stanwood, G.D.; Levitt, P. Drug exposure early in life: functional repercussions of changing neuropharmacology during sensitive periods of brain development. Curr. Opin. Pharmacol., 2004, 4(1), 65-71. [http://dx.doi.org/10.1016/j.coph.2003.09.003]. [PMID: 15018841].
[148]
Nestler, E.J. Molecular mechanisms of drug addiction. Neuropharmacology, 2004, 47(Suppl. 1), 24-32. [http://dx.doi.org/10. 1016/j.neuropharm.2004.06.031]. [PMID: 15464123].
[149]
Hack, S.P.; Christie, M.J. Adaptations in adenosine signaling in drug dependence: therapeutic implications. Crit. Rev. Neurobiol., 2003, 15(3-4), 235-274. [http://dx.doi.org/10.1615/v15.i34.30]. [PMID: 15248812].
[150]
Rozisky, J.R.; da Silva, R.S.; Adachi, L.S.; Capiotti, K.M.; Ramos, D.B.; Bogo, M.R.; Bonan, C.D.; Sarkis, J.J.; Torres, I.L. Neonatal morphine exposure alters E-NTPDase activity and gene expression pattern in spinal cord and cerebral cortex of rats. Eur. J. Pharmacol., 2010, 642(1-3), 72-76. [http://dx.doi.org/10.1016/j.ejphar. 2010.05.044]. [PMID: 20553911].
[151]
de Mendonça, A.; Cunha, R.A. Therapeutic opportunities for caffeine in Alzheimer’s disease and other neurodegenerative disorders. J. Alzheimers Dis., 2010, 20(Suppl. 1), S1-S2. [http://dx.doi.org/ 10.3233/JAD-2010-01420]. [PMID: 20448305].
[152]
Millar, D.; Schmidt, B. Controversies surrounding xanthine therapy, Seminars in neonatology : SN ,2004, 9(3), 239-244
[153]
Marcus, C.L.; Meltzer, L.J.; Roberts, R.S.; Traylor, J.; Dix, J.; D’ilario, J.; Asztalos, E.; Opie, G.; Doyle, L.W.; Biggs, S.N.; Nixon, G.M.; Narang, I.; Bhattacharjee, R.; Davey, M.; Horne, R.S.; Cheshire, M.; Gibbons, J.; Costantini, L.; Bradford, R.; Schmidt, B. Long-term effects of caffeine therapy for apnea of prematurity on sleep at school age. Am. J. Respir. Crit. Care Med., 2014, 190(7), 791-799. [http://dx.doi.org/10.1164/rccm.201406-1092OC]. [PMID: 25171195].
[154]
Da Silva, R.S.; Richetti, S.K.; Tonial, E.M.; Bogo, M.R.; Bonan, C.D. Profile of nucleotide catabolism and ectonucleotidase expression from the hippocampi of neonatal rats after caffeine exposure. Neurochem. Res., 2012, 37(1), 23-30. [http://dx.doi.org/10.1007/ s11064-011-0577-0]. [PMID: 21842269].
[155]
Chao, H.T.; Chen, H.; Samaco, R.C.; Xue, M.; Chahrour, M.; Yoo, J.; Neul, J.L.; Gong, S.; Lu, H.C.; Heintz, N.; Ekker, M.; Rubenstein, J.L.; Noebels, J.L.; Rosenmund, C.; Zoghbi, H.Y. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature, 2010, 468(7321), 263-269. [http://dx.doi.org/10.1038/nature09582]. [PMID: 21068835].
[156]
Giovedí, S.; Corradi, A.; Fassio, A.; Benfenati, F. Involvement of synaptic genes in the pathogenesis of autism spectrum disorders: the case of synapsins. Front Pediatr., 2014, 2, 94. [PMID: 25237665].
[157]
Al-Mosalem, O.A.; El-Ansary, A.; Attas, O.; Al-Ayadhi, L. Metabolic biomarkers related to energy metabolism in Saudi autistic children. Clin. Biochem., 2009, 42(10-11), 949-957. [http://dx.doi. org/10.1016/j.clinbiochem.2009.04.006]. [PMID: 19376103].
[158]
Persico, A.M.; Militerni, R.; Bravaccio, C.; Schneider, C.; Melmed, R.; Trillo, S.; Montecchi, F.; Palermo, M.T.; Pascucci, T.; Puglisi-Allegra, S.; Reichelt, K.L.; Conciatori, M.; Baldi, A.; Keller, F. Adenosine deaminase alleles and autistic disorder: case-control and family-based association studies. Am. J. Med. Genet., 2000, 96(6), 784-790. [http://dx.doi.org/10.1002/1096-8628(20001204)96:6 <784:AID-AJMG18>3.0.CO;2-7]. [PMID: 11121182].
[159]
Theoharides, T.C. Extracellular mitochondrial ATP, suramin, and autism? Clin. Ther., 2013, 35(9), 1454-1456. [http://dx.doi.org/ 10.1016/j.clinthera.2013.07.419]. [PMID: 23954092].
[160]
Page, T.; Coleman, M. De novo purine synthesis is increased in the fibroblasts of purine autism patients. Adv. Exp. Med. Biol., 1998, 431, 793-796. [http://dx.doi.org/10.1007/978-1-4615-5381-6_152]. [PMID: 9598172].
[161]
Masino, S.A.; Kawamura, M., Jr; Cote, J.L.; Williams, R.B.; Ruskin, D.N. Adenosine and autism: a spectrum of opportunities. Neuropharmacology, 2013, 68, 116-121. [http://dx.doi.org/10. 1016/j.neuropharm.2012.08.013]. [PMID: 22940000].
[162]
Masino, S.A.; Kawamura, M., Jr; Plotkin, L.M.; Svedova, J.; DiMario, F.J., Jr; Eigsti, I.M. The relationship between the neuromodulator adenosine and behavioral symptoms of autism. Neurosci. Lett., 2011, 500(1), 1-5. [http://dx.doi.org/10.1016/j.neulet. 2011.06.007]. [PMID: 21693172].
[163]
Malow, B.A. Sleep disorders, epilepsy, and autism. Ment. Retard. Dev. Disabil. Res. Rev., 2004, 10(2), 122-125. [http://dx.doi.org/10. 1002/mrdd.20023]. [PMID: 15362168].
[164]
Ikemoto, S. Dopamine reward circuitry: two projection systems from the ventral midbrain to the nucleus accumbens-olfactory tubercle complex. Brain Res. Brain Res. Rev., 2007, 56(1), 27-78. [http:// dx.doi.org/10.1016/j.brainresrev.2007.05.004]. [PMID: 17574681].
[165]
Crawley, J.N. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol., 2007, 17(4), 448-459. [http://dx.doi.org/ 10.1111/j.1750-3639.2007.00096.x]. [PMID: 17919130].
[166]
Freitag, C.M.; Agelopoulos, K.; Huy, E.; Rothermundt, M.; Krakowitzky, P.; Meyer, J.; Deckert, J.; von Gontard, A.; Hohoff, C.; Adenosine, A. Adenosine A(2A) receptor gene (ADORA2A) variants may increase autistic symptoms and anxiety in autism spectrum disorder. Eur. Child Adolesc. Psychiatry, 2010, 19(1), 67-74. [http://dx.doi.org/10.1007/s00787-009-0043-6]. [PMID: 19565319].
[167]
Ghanizadeh, A. Possible role of caffeine in autism spectrum disorders, a new testable hypothesis. J. Food Sci., 2010, 75(6), ix. [http://dx.doi.org/10.1111/j.1750-3841.2010.01760.x]. [PMID: 20722962].
[168]
Masino, S.A.; Kawamura, M.; Wasser, C.D.; Pomeroy, L.T.; Ruskin, D.N. Adenosine, ketogenic diet and epilepsy: the emerging therapeutic relationship between metabolism and brain activity. Curr. Neuropharmacol., 2009, 7(3), 257-268. [http://dx.doi.org/ 10.2174/157015909789152164]. [PMID: 20190967].
[169]
Tanimura, Y.; Vaziri, S.; Lewis, M.H. Indirect basal ganglia pathway mediation of repetitive behavior: attenuation by adenosine receptor agonists. Behav. Brain Res., 2010, 210(1), 116-122. [http:// dx.doi.org/10.1016/j.bbr.2010.02.030]. [PMID: 20178817].
[170]
Naviaux, R.K.; Zolkipli, Z.; Wang, L.; Nakayama, T.; Naviaux, J.C.; Le, T.P.; Schuchbauer, M.A.; Rogac, M.; Tang, Q.; Dugan, L.L.; Powell, S.B. Antipurinergic therapy corrects the autism-like features in the poly(IC) mouse model. PLoS One, 2013, 8(3), e57380. [http://dx.doi.org/10.1371/journal.pone.0057380]. [PMID: 23516405].
[171]
Naviaux, J.C.; Wang, L.; Li, K.; Bright, A.T.; Alaynick, W.A.; Williams, K.R.; Powell, S.B.; Naviaux, R.K. Antipurinergic therapy corrects the autism-like features in the Fragile X (Fmr1 knockout) mouse model. Mol. Autism, 2015, 6, 1. [http://dx.doi.org/10. 1186/2040-2392-6-1]. [PMID: 25705365].
[172]
Naviaux, J.C.; Schuchbauer, M.A.; Li, K.; Wang, L.; Risbrough, V.B.; Powell, S.B.; Naviaux, R.K. Reversal of autism-like behaviors and metabolism in adult mice with single-dose antipurinergic therapy. Transl. Psychiatry, 2014, 4, e400. [http://dx.doi.org/10. 1038/tp.2014.33]. [PMID: 24937094].
[173]
North, R.A.; Jarvis, M.F. P2X receptors as drug targets. Mol. Pharmacol., 2013, 83(4), 759-769. [http://dx.doi.org/10.1124/ mol.112.083758]. [PMID: 23253448].
[174]
Yegutkin, G.G.; Jankowski, J.; Jalkanen, S.; Günthner, T.; Zidek, W.; Jankowski, V. Dinucleotide polyphosphates contribute to purinergic signalling via inhibition of adenylate kinase activity. Biosci. Rep., 2008, 28(4), 189-194. [http://dx.doi.org/10.1042/BSR 20080052]. [PMID: 18576946].
[175]
Schetinger, M.R.; Vieira, V.L.; Morsch, V.M.; Balz, D. ATP and ADP hydrolysis in fish, chicken and rat synaptosomes. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2001, 128(4), 731-741. [http:// dx.doi.org/10.1016/S1096-4959(00)00367-5]. [PMID: 11290455].
[176]
Heine, P.; Braun, N.; Heilbronn, A.; Zimmermann, H. Jankowski, Dinucleotide polyphosphates contribute to purinergic signalling via inhibition of adenylate kinase activity. Biosci. Rep., 2008, 28(4), 189-194.
[177]
Czarnecka, J.; Roszek, K.; Jabłoński, A.; Smoliński, D.J.; Komoszyński, M. Some aspects of purinergic signaling in the ventricular system of porcine brain. Acta Vet. Scand., 2011, 53, 54. [http://dx.doi.org/10.1186/1751-0147-53-54]. [PMID: 21995888].
[178]
al-Rashida, M.; Batool, G.; Sattar, A.; Ejaz, S.A.; Khan, S.
Lecka, J.; Sévigny, J.; Hameed, A.; Iqbal, J. 2-Alkoxy-3-(sulfonylarylaminomethylene)-chroman-4-ones as potent and selective inhibitors of ectonucleotidases. Eur. J. Med. Chem., 2016, 115, 484-494. [http://dx.doi.org/10.1016/j.ejmech.2016.02.073]. [PMID: 27054295].
[179]
Corbelini, P.F.; Figueiro, F.G.M. das Neves, S.; Andrade, D.F.; Kawano, A.M.; Oliveira, B. V.L. Eifler-Lima, insights into Ecto-5′-Nucleotidase as a new target for cancer therapy: A medicinal chemistry study. Curr. Med. Chem., 2015. [http://dx. doi.org/10.2174/0929867322666150408112615].
[180]
Channar, P.A.; Shah, S.J.; Hassan, S.; Nisa, Z.U.; Lecka, J.; Sevigny, J.; Bajorath, J.; Saeed, A.; Iqbal, J. Isonicotinohydrazones as inhibitors of alkaline phosphatase and ecto-5′-nucleotidase. Chem. Biol. Drug Des., 2017, 89(3), 365-370. [PMID: 27589035].
[181]
Baqi, Y. Ecto-nucleotidase inhibitors: recent developments in drug discovery. Mini Rev. Med. Chem., 2015, 15(1), 21-33. [http://dx. doi.org/10.2174/1389557515666150219115141]. [PMID: 25694081].
[182]
Naviaux, R.K. Mitochondria and autism spectrum disorders. The Neuroscience of Autism Spectrum Disorders; Buxbaum, J.D; Hof, P.R., Ed.; Academic Press: Amsterdam, 2013, pp. 179-193. [http://dx.doi.org/10.1016/B978-0-12-391924-3.00012-0]

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