Skip to main content

Advertisement

SpringerLink
Log in

Distribution of ectonucleotidases in the rodent brain revisited

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Nucleotides comprise a major class of signaling molecules in the nervous system. They can be released from nerve cells, glial cells, and vascular cells where they exert their function via ionotropic (P2X) or metabotropic (P2Y) receptors. Signaling via extracellular nucleotides and also adenosine is controlled and modulated by cell-surface-located enzymes (ectonucleotidases) that hydrolyze the nucleotide to the respective nucleoside. Extracellular hydrolysis of nucleotide ligands involves a considerable number of enzymes with differing catalytic properties differentially affecting the nucleotide signaling pathway. It is therefore important to investigate which type of ectonucleotidase(s) contributes to the control of nucleotide signaling in distinct cellular and physiological settings. By using a classical enzyme histochemical approach and employing various substrates, inhibitors, and knockout animals, we provide, for the first time, a comparative analysis of the overall distribution of catalytic activities reflecting four ectonucleotidase families: ecto-5′-nucleotidase, alkaline phosphatases, ectonucleoside triphosphate diphosphohydrolases (E-NTPDases), and ectonucleotide pyrophyphatases/phosphodiesterases (E-NPPs). We place into perspective the earlier literature and provide novel evidence for a parenchymal localization of tissue non-specific alkaline phosphatase, E-NPPs, and E-NTPDases in the mouse brain. In addition, we specify the location of ectonucleotidases within the brain vasculature. Most notably, brain vessels do not express ecto-5′-nucleotidase. The preponderance of individual enzymes differs considerably between brain locations. The contribution of all types of ectonucleotidases thus needs to be considered in physiological and pharmacological studies of purinergic signaling in the brain.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Asensio AC, Rodriguez-Ferrera CR, Castaneyra-Perdomo A, Oaknin S, Rotllán P (2007) 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 50:581–590

    Article  PubMed  CAS  Google Scholar 

  • Belcher SM, Zsarnovzky A, Crawford PA, Hemani H, Spurling L, Kirley TL (2006) Immunolocalization of ecto-nucleoside triphosphate diphosphohydrolase 3 in rat brain: implications for modulation of multiple homeostatic systems including feeding and sleep wake bahaviors. Neuroscience 137:1331–1346

    Article  PubMed  CAS  Google Scholar 

  • Bianchi V, Spychala J (2003) Mammalian 5′-nucleotidases. J Biol Chem 278:46195–46198

    Article  PubMed  CAS  Google Scholar 

  • Bjelobaba I, Nedeljkovic N, Subasic S, Lavrnja I, Pekovic S, Stojkov D, Rakic L, Stojiljkovic M (2006) Immunolocalization of ecto-nucleotide pyrophosphatase/phosphodiesterase 1 (NPP1) in the rat forebrain. Brain Res 1120:54–63

    Article  PubMed  CAS  Google Scholar 

  • Bjelobaba I, Stojiljkovic M, Pekovic S, Dacic S, Lavrnja I, Stojkov D, Rakic L, Nedeljkovic N (2007) Immunohistological determination of ecto-nucleoside triphosphate diphosphohydrolase1 (NTPDase1) and 5′-nucleotidase in rat hippocampus reveals overlapping distribution. Cell Mol Neurobiol 27:731–743

    Article  PubMed  CAS  Google Scholar 

  • Blass-Kampmann S, Kindler-Rohrborn A, Deissler H, D’Urso D, Rajewsky MF (1997) In vitro differentiation of neural progenitor cells from prenatal rat brain: common cell surface glycoprotein on three glial cell subsets. J Neurosci Res 48:95–111

    Article  PubMed  CAS  Google Scholar 

  • Braun JS, Lehir M, Kaissling B (1994) Morphology and distribution of ecto-5′-nucleotidase-positive cells in the rat choroid plexus. J Neurocytol 23:193–200

    Article  PubMed  CAS  Google Scholar 

  • Braun N, Sévigny J, Robson SC, Enjyoji K, Guckelberger O, Hammer K, Di Virgilio F, Zimmermann H (2000a) Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/cd39 expression to microglia and vasculature of the brain. Eur J Neurosci 12:4357–4366

    Article  PubMed  CAS  Google Scholar 

  • Braun N, Fengler S, Ebeling C, Servos J, Zimmermann H (2000b) Sequencing, functional expression and characterization of NTPDase6, a nucleoside diphosphatase and novel member of the ecto-nucleoside triphosphate diphosphohydrolase family. Biochem J 351:639–647

    Article  PubMed  CAS  Google Scholar 

  • Braun N, Sévigny J, Mishra S, Robson SC, Barth SW, Gerstberger R, Hammer K, Zimmermann H (2003) Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain. Eur J Neurosci 17:1355–1364

    Article  PubMed  Google Scholar 

  • Brundege JM, Diao LH, Proctor WR, Dunwiddie TV (1997) The role of cyclic AMP as a precursor of extracellular adenosine in the rat hippocampus. Neuropharmacology 36:1201–1210

    Article  PubMed  CAS  Google Scholar 

  • Burnstock G (2007a) Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87:659–797

    Article  PubMed  CAS  Google Scholar 

  • Burnstock G (2007b) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483

    Article  PubMed  CAS  Google Scholar 

  • Chilingaryan A, Chilingaryan AM, Martin GG (2006) The three-dimensional detection of microvasculatory bed in the brain of white rat Rattus norvegicus by a Ca2+-ATPase method. Brain Res 1070:131–138

    Article  PubMed  CAS  Google Scholar 

  • Coles JA, Deitmer JW (2005) Extracellular potassium and pH: homeostasis and signaling. In: Kettenmann H, Ransom BR (eds) Neuroglia. Oxford University Press, Oxford, pp 334–345

    Google Scholar 

  • Cunha RA (2001a) Adenosine as a neuromodulator and as a homeostatic regulator in the nervous system: different roles, different sources and different receptors. Neurochem Int 38:107–125

    Article  PubMed  CAS  Google Scholar 

  • Cunha RA (2001b) Regulation of the ecto-nucleotidase pathway in rat hippocampal nerve terminals. Neurochem Res 26:979–991

    Article  PubMed  CAS  Google Scholar 

  • Doengi M, Deitmer JW, Lohr C (2008) New evidence for purinergic signaling in the olfactory bulb: A2A and P2Y1 receptors mediate intracellular calcium release in astrocytes. FASEB J 22:2368–2378

    Article  PubMed  CAS  Google Scholar 

  • Dulla CG, Dobelis P, Pearson T, Frenguelli BG, Staley KJ, Masino SA (2005) Adenosine and ATP link P-CO2 to cortical excitability via pH. Neuron 48:1011–1023

    Article  PubMed  CAS  Google Scholar 

  • Enjyoji K, Sévigny J, Lin Y, Frenette P, Christie PD, Schulte am Esch J, Imai M, Edelberger JM, Rayburn H, Lech M, Beeler DM, 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

    Article  PubMed  CAS  Google Scholar 

  • Fastbom J, Pazos A, Palacios JM (1987) The distribution of adenosine A1 receptors and 5′-nucleotidase in the brain of some commonly used experimental animals. Neuroscience 22:813–826

    Article  PubMed  CAS  Google Scholar 

  • Fonta C, Negyessy L, Renaud L, Barone P (2004) Areal and subcellular localization of the ubiquitous alkaline phosphatase in the primate cerebral cortex: evidence for a role in neurotransmission. Cereb Cortex 14:595–609

    Article  PubMed  Google Scholar 

  • Fonta C, Negyessy L, Renaud L, Barone P (2005) Postnatal development of alkaline phosphatase activity correlates with the maturation of neurotransmission in the cerebral cortex. J Comp Neurol 486:179–196

    Article  PubMed  Google Scholar 

  • Friede RL (1966) A quantitative mapping of alkaline phosphatase in the brain of the rhesus monkey. J Neurochem 13:197–203

    Article  PubMed  CAS  Google Scholar 

  • Fuss B, Baba H, Phan T, Tuohy VK, Macklin WB (1997) Phosphodiesterase I, a novel adhesion molecule and/or cytokine involved in oligodendrocyte function. J Neurosci 17:9095–9103

    PubMed  CAS  Google Scholar 

  • Goding JW, Grobben B, Slegers H (2003) Physiological and pathophysiological functions of the ecto-nucleotide pyrophosphatase/phosphodiesterase family. Biochim Biophys Acta Mol Basis Dis 1638:1–19

    CAS  Google Scholar 

  • Gordon JS, Torack RM (1967) Inhibition of cerebral adenosinetriphosphatase activity by various aldehyde fixatives. J Neurochem 14:1155–1160

    Article  PubMed  CAS  Google Scholar 

  • Harahap AR, Goding JW (1988) Distribution of murine plasma cell antigen PC-1 in non-lymphoid tissues. J Immunol 141:2317–2320

    PubMed  CAS  Google Scholar 

  • Heine P, Braun N, Zimmermann H (1999) Functional characterization of rat ecto-ATPase and ecto-ATP diphosphohydrolase after heterologous expression in CHO cells. Eur J Biochem 262:102–107

    Article  PubMed  CAS  Google Scholar 

  • Ibrahim MZM, Khreis Y, Koshayan DS (1974) The histochemical identification of microglia. J Neurol Sci 22:211–233

    Article  PubMed  CAS  Google Scholar 

  • King AE, Ackley MA, Cass CE, Young JD, Baldwin SA (2006) Nucleoside transporters: from scavengers to novel therapeutic targets. Trends Pharmacol Sci 27:416–425

    Article  PubMed  CAS  Google Scholar 

  • Kittel A (1994) Distribution of Ca-ATPases in the medial habenula in mouse. Scanning Microsc 8:337–343

    PubMed  CAS  Google Scholar 

  • Kittel A, Siklós L, Thuróczy G, Somosy Z (1996) Qualitative enzyme histochemistry and microanalysis reveals changes in ultrastructural distribution of calcium and calcium-activated ATPases after microwave irradiation of the medial habenula. Acta Neuropathol (Berl) 92:362–368

    Article  CAS  Google Scholar 

  • Koszalka P, Ozuyaman B, Huo YQ, Zernecke A, Flogel U, Braun N, Buchheiser A, Decking UKM, Smith ML, Sévigny J, Gear A, Weber AA, Molojavyi A, Ding ZP, Weber C, Ley K, Zimmermann H, Gödecke A, Schrader J (2004) Targeted disruption of cd73/ecto-5′-nucleotidase alters thromboregulation and augments vascular inflammatory response. Circ Res 95:814–821

    Article  PubMed  CAS  Google Scholar 

  • Kozlenkov A, LeDu MH, Cuniasse P, Ny T, Hoylaerts MF, Millán JL (2004) Residues determining the binding specificity of uncompetitive inhibitors to tissue-nonspecific alkaline phosphatase. J Bone Miner Res 19:1862–1872

    Article  PubMed  CAS  Google Scholar 

  • Kukulski F, Lévesque SA, Lavoie ÉG, Lecka J, Bigonnesse F, Knowles AF, Robson SC, Kirley TL, Sévigny J (2005) Comparative hydrolysis of P2 receptor agonists by NTPDase 1, 2, 3 and 8. Purinergic Signalling 1:193–204

    Article  PubMed  CAS  Google Scholar 

  • Langer D, Ikehara Y, Takebayashi H, Hawkes R, Zimmermann H (2007) The ectonucleotidases alkaline phosphatase and nucleoside triphosphate diphosphohydrolas 2 are associated with subsets of progenitor cell populations in the mouse embryonic, postnatal and adult neurogenic zones. Neuroscience 150:863–879

    Article  PubMed  CAS  Google Scholar 

  • Lee KS, Schubert P, Reddington M, Kreutzberg GW (1986) The distribution of adenosine A1 receptors and 5′-nucleotidase in the hippocampal formation of several mammalian species. J Comp Neurol 246:427–434

    Article  PubMed  CAS  Google Scholar 

  • Lojda Z, Gossrau R, Schiebler TH (1979) Enzyme histochemistry. A laboratory manual. Springer, New York

    Google Scholar 

  • Millán JL (2006) Structurte, substrate specificity and functional relatedness to other members of a large superfamily of enzymes. Purinergic Signalling 2:335–341

    Article  PubMed  CAS  Google Scholar 

  • Miras-Portugal MT, Gualix J, Mateo J, Díaz-Hernández M, Gómez-Villafuertes R, Castro E, Pintor J (1999) Diadenosine polyphosphates, extracellular function and catabolism. Prog Brain Res 120:397–409

    Article  PubMed  CAS  Google Scholar 

  • Mori S, Nagano M (1985) Ultracytochemical demonstration of alkaline phosphatase activity in astrocytes and subependymal cells in the rat brain. Arch Hist Jpn 48:511–517

    CAS  Google Scholar 

  • Murabe Y, Sano Y (1981) Thiaminepyrophosphatase activity in the plasma membrane of microglia. Histochemistry 71:45–52

    Article  PubMed  CAS  Google Scholar 

  • Murabe Y, Sano Y (1982) Morphological studies on microglia. V. Microglial cells in the cerebral cortex of the rat, with special reference to their possible involvement in synaptic function. Cell Tissue Res 223:493–506

    Article  PubMed  CAS  Google Scholar 

  • Nagy AK (1997) Ecto-ATPases of the nervous system. In: Plesner L, Kirley TL, Knowles AF (eds) Ecto-ATPases: recent progress in structure and function. Plenum, New York, pp 1–13

    Google Scholar 

  • Nagy AK, Shuster TA, Delgado-Escueta AV (1986) Ecto-ATPase of mammalian synaptosomes: identification and enzymic characterization. J Neurochem 47:976–986

    PubMed  CAS  Google Scholar 

  • Narisawa S, Hasegawa H, Watanabe K, Millán JL (1994) Stage-specific expression of alkaline phosphatase during neural development of the mouse. Dev Dyn 201:227–235

    PubMed  CAS  Google Scholar 

  • Narisawa S, Hoylaerts MF, Doctor KS, Fukuda MN, Alpers DH, Millán JL (2007) A novel phosphatase upregulated in Akp3 knockout mice. Am J Physiol Gastrointest Liver Physiol 293:G1068–G1077

    Article  PubMed  CAS  Google Scholar 

  • Narita M, Goji J, Nakamura H, Sano K (1994) Molecular cloning, expression, and localization of a brain- specific phosphodiesterase I/nucleotide pyrophosphatase (PD-I alpha) from rat brain. J Biol Chem 269:28235–28242

    PubMed  CAS  Google Scholar 

  • Nishihara Y, Hayashi Y, Fujii T, Adachi T, Stigbrand T, Hirano K (1994) The alkaline phosphatase in human plexus chorioideus. Biochim Biophys Acta 1209:274–278

    PubMed  Google Scholar 

  • Novikoff AB, Drucker J, Shin WY, Goldfischer S (1961) Further studies of the apparent adenosinetriphosphatase activity of cell membranes in formol-calcium-fixed tissues. J Histochem Cytochem 9:434–451

    PubMed  CAS  Google Scholar 

  • Ogilvie A (1992) Extracellular functions for ApnA. In: McLennan AG (ed) Ap4A and other dinucleoside polyphosphates. CRC, Boca Raton, pp 229–273

    Google Scholar 

  • Ohkubo S, Kimura J, Matsuoka I (2000) Ecto-alkaline phosphatase in NG108-15 cells: a key enzyme mediating P1 antagonist-sensitive ATP response. Br J Pharmacol 131:1667–1672

    Article  PubMed  CAS  Google Scholar 

  • Robson SC, Candinas D, Siegel JB, Kopp C, Millan M, Hancock WW, Bach FH (1996) Potential mechanism of abnormal thromboregulation in xenograft rejection: loss of ecto-ATPases upon endothelial cell activation. Transplant Proc 1996 28:536

    Google Scholar 

  • Robson SC, Sévigny J, Zimmermann H (2006) The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signalling 2:409–430

    Article  PubMed  CAS  Google Scholar 

  • Salmi M, Jalkanen S (2005) Cell-surface enzymes in control of leukocyte trafficking. Nat Rev Immunol 5:760–771

    Article  PubMed  CAS  Google Scholar 

  • Sano S, Matsuda Y, Nakagawa H (1988) Thiamine pyrophosphatase (nucleoside diphosphatase) in the Golgi apparatus is distinct from microsomal nucleoside diphosphatase. J Biochem 103:678–681

    PubMed  CAS  Google Scholar 

  • Sato K, Malchinkhuu E, Muraki T, Ishikawa K, Hayashi K, Tosaka M, Mochiduki A, Inoue K, Tomura H, Mogi C, Nochi H, Tamoto K, Okajima F (2005) Identification of autotaxin as a neurite retraction- inducing factor of PC12 cells in cerebrospinal fluid and its possible sources. J Neurochem 92:904–914

    Article  PubMed  CAS  Google Scholar 

  • Savaskan NE, Rocha L, Kotter MR, Baer A, Lubec G, vanMeeteren LA, Kishi Y, Aoki J, Moolenaar WH, Nitsch R, Brauer AU (2007) Autotaxin (NPP-2) in the brain: cell type-specific expression and regulation during development and after neurotrauma. Cell Mol Life Sci 64:230–243

    Article  PubMed  CAS  Google Scholar 

  • Schoen SW, Graybiel AM (1993) Species-specific patterns of glycoprotein expression in the developing rodent caudoputamen—association of 5′-nucleotidase activity with dopamine islands and striosomes in rat, but with extrastriosomal matrix in mouse. J Comp Neurol 333:578–596

    Article  PubMed  CAS  Google Scholar 

  • Schoen SW, Kreutzberg GW (1997) 5′-Nucleotidase enzyme cyctochemistry as a tool for revealing activated glial cells and malleable synapses in CNS development and regeneration. Brain Res Brain Res Protoc 1:33–43

    Article  PubMed  CAS  Google Scholar 

  • Schoen SW, Graeber MB, Tóth L, Kreutzberg GW (1988) 5′-Nucleotidase in postnatal ontogeny of rat cerebellum: a marker for migrating nerve cells. Dev Brain Res 39:125–136

    Article  CAS  Google Scholar 

  • Scott TG (1967) The distribution of 5′-nucleotidase in the brain of the mouse. J Comp Neurol 129:97–114

    Article  CAS  Google Scholar 

  • Shukla V, Zimmermann H, Wang LP, Kettenmann H, Raab S, Hammer K, Sévigny J, Robson SC, Braun N (2005) Functional expression of the ecto-ATPase NTPDase2 and of nucleotide receptors by neuronal progenitor cells in the adult murine hippocampus. J Neurosci Res 80:600–610

    Article  PubMed  CAS  Google Scholar 

  • Sjöstrand J (1966) Changes in nucleoside phosphatase activity in the hypoglossal nucleus during nerve regeneration. Acta Physiol Scand 67:219–228

    Article  PubMed  Google Scholar 

  • Sommer JR, Hasselbach W (1967) The effect of glutaraldehyde and formaldehyde on the calcium pump of the sarcoplasmic reticulum. J Cell Biol 34:902–905

    Article  PubMed  CAS  Google Scholar 

  • Stefan C, Jansen S, Bollen M (2005) NPP-type ectophosphodiesterases: unity in diversity. Trends Biochem Sci 30:542–550

    Article  PubMed  CAS  Google Scholar 

  • Sugimura K, Mizutani A (1979) Histochemical and cytochemical studies of alkaline phosphatase activity in the synapses of rat brain. Histochemistry 61:123–129

    Article  PubMed  CAS  Google Scholar 

  • Vollmayer P, Clair T, Goding JW, Sano K, Servos J, Zimmermann H (2003) Hydrolysis of diadenosine polyphosphates by nucleotide pyrophosphatases/phosphodiesterases. Eur J Biochem 270:2971–2978

    Article  PubMed  CAS  Google Scholar 

  • Vorbrodt AW, Wisniewski HM (1982) Plasmalemma-bound nucleoside diphosphatase as a cytochemical marker of central nervous system (CNS) mesodermal cells. J Histochem Cytochem 30:418–424

    PubMed  CAS  Google Scholar 

  • Vorbrodt AW, Lossinsky AS, Wisniewski HM (1986) Localization of alkaline phosphatase activity in endothelia of developing and mature mouse blood-brain barrier. Dev Neurosci 8:1–13

    Article  PubMed  CAS  Google Scholar 

  • Wachstein M, Meisel E (1957) Histochemistry of hepatic phosphatases at a physiologic pH with special reference to the demonstration of bile canaliculi. Am J Clin Pathol 27:13–23

    PubMed  CAS  Google Scholar 

  • Wang TF, Guidotti G (1996) CD39 is an ecto-(Ca2+,Mg2+)-apyrase. J Biol Chem 271:9898–9901

    Article  PubMed  CAS  Google Scholar 

  • Wang TF, Guidotti G (1998) Widespread expression of ecto-apyrase (CD39) in the central nervous system. Brain Res 790:318–322

    Article  PubMed  CAS  Google Scholar 

  • Wink MR, Braganhol E, Tamajusuku ASK, Lenz G, Zerbini LF, Libermann TA, Sévigny J, Battastini AMO, Robson SC (2006) Nucleoside triphosphate diphosphohydrolase-2 (NTPdase2/ CD39L1) is the dominant ectonucleotidase expressed by rat astrocytes. Neuroscience 138:421–432

    Article  PubMed  CAS  Google Scholar 

  • Yegutkin GG (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783:673–694

    Article  PubMed  CAS  Google Scholar 

  • Zernecke A, Bidzhekov K, Ozuyaman B, Fraemohs L, Liehn EA, LuscherFirzlaff JM, Luscher B, Schrader J, Weber C (2006) CD73/Ecto-5′-nucleotidase protects against vascular inflammation and neointima formation. Circulation 113:2120–2127

    Article  PubMed  CAS  Google Scholar 

  • Ziganshin AU, Hoyle CHV, Burnstock G (1994) Ecto-enzymes and metabolism of extracellular ATP. Drug Dev Res 32:134–146

    Article  CAS  Google Scholar 

  • Zimmermann H (1992) 5′-Nucleotidase—molecular structure and functional aspects. Biochem J 285:345–365

    PubMed  CAS  Google Scholar 

  • Zimmermann H (1996a) Biochemistry, localization and functional roles of ecto-nucleotidases in the nervous system. Prog Neurobiol 49:589–618

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann H (1996b) Extracellular purine metabolism. Drug Dev Res 39:337–352

    Article  CAS  Google Scholar 

  • Zimmermann H (2000) Extracellular metabolism of ATP and other nucleotides. Naunyn-Schmiedeberg’s Arch Pharmacol 362:299–309

    Article  CAS  Google Scholar 

  • Zimmermann H (2006) Ecto-nucleotidases in the nervous system. Novartis Found Symp 275:113–128

    Article  Google Scholar 

  • Zimmermann H, Braun N (1999) Ecto-nucleotidases: molecular structures, catalytic properties, and functional roles in the nervous system. Prog Brain Res 120:371–385

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann H, Vogel M, Laube U (1993) Hippocampal localization of 5′-nucleotidase as revealed by immunocytochemistry. Neuroscience 55:105–112

    Article  PubMed  CAS  Google Scholar 

  • Zimmermann H, Mishra SK, Shukla V, Langer D, Gampe K, Grimm I, Delic J, Braun N (2007) Ecto-nucleotidases, molecular properties and functional impact. A R Acad Nac Farm 73:537–566

    CAS  Google Scholar 

  • Zisapel N, Haklai R (1980) Localization of an alkaline phosphatase and other synaptic vesicle proteins. Neuroscience 5:2297–2303

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Cell Biology and Neuroscience, Biocenter, Goethe University Frankfurt am Main, Max-von-Laue-Str. 9, 60438, Frankfurt, Germany

    David Langer, Klaus Hammer & Herbert Zimmermann

  2. Department of Cardiovascular Physiology, Heinrich Heine University Duesseldorf, Duesseldorf, Germany

    Patrycja Koszalka & Jürgen Schrader

  3. Department of Medicine, Beth Israel Deaconess Medical Center, Harvard Medical School, Boston, Mass., USA

    Simon Robson

Authors
  1. David Langer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Klaus Hammer
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Patrycja Koszalka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jürgen Schrader
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Simon Robson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Herbert Zimmermann
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Herbert Zimmermann.

Additional information

This work was supported by the Deutsche Forschungsgemeinschaft (140/17-3).

Rights and permissions

Reprints and permissions

About this article

Cite this article

Langer, D., Hammer, K., Koszalka, P. et al. Distribution of ectonucleotidases in the rodent brain revisited. Cell Tissue Res 334, 199–217 (2008). https://doi.org/10.1007/s00441-008-0681-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-008-0681-x

Keywords

Search

Navigation