Regional changes in ectonucleotidase activity after cortical stab injury in rat.

During a variety of insults to the brain adenine nucleotides are released in large quantities from damaged cells, triggering local cellular and biochemical responses to injury. Different models of brain injury reveal that the local increase in adenine nucleotides levels is followed by a compensatory up-regulation of ectonucleotidase enzymes that catalyze sequential hydrolysis of ATP to ADP, AMP and adenosine. However, recent studies imply that changes in adenine nucleotides release may also occur in the areas distant from the site of direct damage. Therefore, in the present study we have used the model of cortical stab injury to analyze extracellular ATP, ADP and AMP hydrolysis in the membrane preparations obtained from the brain regions that were not subjected to direct tissue damage. The brain regions analyzed were contralateral cortex, hippocampus, caudate nucleus, thalamus and hypothalamus. It was evidenced that cortical stab injury induced early widespread decrease in AMP hydrolysis in all brain areas tested, except in the hypothalamus, without changes in ATP hydrolysis. These findings imply that brain injury affects global extracellular adenine nucleotide and nucleoside levels, consequently affecting neuronal function in the regions distant to the primary damage.

[1]  J. Schrader,et al.  Distribution of ectonucleotidases in the rodent brain revisited , 2008, Cell and Tissue Research.

[2]  L. Rakić,et al.  Early Temporal Changes in Ecto-Nucleotidase Activity after Cortical Stab Injury in Rat , 2008, Neurochemical Research.

[3]  L. Rakić,et al.  Immunohistological Determination of Ecto-nucleoside Triphosphate Diphosphohydrolase1 (NTPDase1) and 5′-nucleotidase in Rat Hippocampus Reveals Overlapping Distribution , 2007, Cellular and Molecular Neurobiology.

[4]  H. Laurer,et al.  Changes in cortical and subcortical energy metabolism after repetitive and single controlled cortical impact injury in the mouse , 2007, Journal of Molecular Neuroscience.

[5]  N. Dale,et al.  Temporal and mechanistic dissociation of ATP and adenosine release during ischaemia in the mammalian hippocampus1 , 2007, Journal of neurochemistry.

[6]  L. Rakić,et al.  Immunolocalization of ecto-nucleotide pyrophosphatase/phosphodiesterase 1 (NPP1) in the rat forebrain , 2006, Brain Research.

[7]  L. Rakić,et al.  Up‐regulation of ectonucleotidase activity after cortical stab injury in rats , 2006, Cell biology international.

[8]  Ralf Regenthal,et al.  Changes in purinergic signaling after cerebral injury – involvement of glutamatergic mechanisms? , 2006, International Journal of Developmental Neuroscience.

[9]  F. Pedata,et al.  ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia , 2005, Neurochemistry International.

[10]  W. Gan,et al.  ATP mediates rapid microglial response to local brain injury in vivo , 2005, Nature Neuroscience.

[11]  S. Hand,et al.  Depression of cell metabolism and proliferation by membrane-permeable and -impermeable modulators: role for AMP-to-ATP ratio. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[12]  S. Hoyer,et al.  ATPases of Synaptic Plasma Membranes from Hippocampus After Ischemia and Recovery During Ageing , 2002, Neurochemical Research.

[13]  P. Séguéla,et al.  ADP and AMP Induce Interleukin-1β Release from Microglial Cells through Activation of ATP-Primed P2X7 Receptor Channels , 2002, The Journal of Neuroscience.

[14]  M. Yacoub,et al.  Regulation of ecto-5′-nucleotidase by TNF-α in human endothelial cells , 2002, Molecular and Cellular Biochemistry.

[15]  G. Bernardi,et al.  P2 receptor modulation and cytotoxic function in cultured CNS neurons , 2002, Neuropharmacology.

[16]  F. Sharom,et al.  PI-specific phospholipase C cleavage of a reconstituted GPI-anchored protein: modulation by the lipid bilayer. , 2002, Biochemistry.

[17]  S. Latini,et al.  Adenosine in the central nervous system: release mechanisms and extracellular concentrations , 2001, Journal of neurochemistry.

[18]  R. Cunha,et al.  Regulation of the Ecto-Nucleotidase Pathway in Rat Hippocampal Nerve Terminals , 2001, Neurochemical Research.

[19]  Kazuhide Inoue,et al.  Extracellular ATP Triggers Tumor Necrosis Factor‐α Release from Rat Microglia , 2000 .

[20]  H. Zimmermann.  Extracellular metabolism of ATP and other nucleotides , 2000, Naunyn-Schmiedeberg's Archives of Pharmacology.

[21]  I. Izquierdo,et al.  Altered ATP Hydrolysis Induced by Pentylenetetrazol Kindling in Rat Brain Synaptosomes , 2000, Neurochemical Research.

[22]  I. Izquierdo,et al.  Changes in synaptosomal ectonucleotidase activities in two rat models of temporal lobe epilepsy , 2000, Epilepsy Research.

[23]  P. Illés,et al.  P2 receptor‐mediated proliferative effects on astrocytes in vivo , 1999, Glia.

[24]  M. Ciotti,et al.  Neuroprotective effects of modulators of P2 receptors in primary culture of CNS neurones , 1999, Neuropharmacology.

[25]  K. Jacobson,et al.  Adenosine-induced cell death: evidence for receptor-mediated signalling , 1999, Apoptosis.

[26]  E. Vizi,et al.  Involvement of P2 purinoceptors and the nitric oxide pathway in [ 3 H ]purine outflow evoked by short-term hypoxia and hypoglycemia in rat hippocampal slices , 1999, Brain Research.

[27]  D. Hardie,et al.  AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. , 1999, The Biochemical journal.

[28]  G Burnstock,et al.  Receptors for purines and pyrimidines. , 1998, Pharmacological reviews.

[29]  C. Culmsee,et al.  Upregulation of the Enzyme Chain Hydrolyzing Extracellular ATP after Transient Forebrain Ischemia in the Rat , 1998, The Journal of Neuroscience.

[30]  F. Sharom,et al.  Release of the glycosylphosphatidylinositol-anchored enzyme ecto-5'-nucleotidase by phospholipase C: catalytic activation and modulation by the lipid bilayer. , 1998, The Biochemical journal.

[31]  M. Stojiljkovic,et al.  Properties of Mg(2+)-ATPase rat brain synaptic plasma membranes. , 1998, General physiology and biophysics.

[32]  D. Treiman,et al.  Reduced cortical ecto-ATPase activity in rat brains during prolonged status epilepticus induced by sequential administration of lithium and pilocarpine. , 1997, Molecular and chemical neuropathology.

[33]  H. Zimmermann.  BIOCHEMISTRY, LOCALIZATION AND FUNCTIONAL ROLES OF ECTO-NUCLEOTIDASES IN THE NERVOUS SYSTEM , 1996, Progress in Neurobiology.

[34]  M. Rathbone,et al.  Stimulation of reactive astrogliosis in vivo by extracellular adenosine diphosphate or an adenosine A2 receptor agonist , 1994, Journal of neuroscience research.

[35]  G. Kreutzberg,et al.  Synaptic 5′-Nucleotidase Activity Reflects Lesion-Induced Sprouting within the Adult Rat Dentate Gyrus , 1994, Experimental Neurology.

[36]  M. Rathbone,et al.  Extracellular purine nucleosides stimulate cell division and morphogenesis: pathological and physiological implications. , 1992, Medical hypotheses.

[37]  M. Rathbone,et al.  Purinergic stimulation of cell division and differentiation: mechanisms and pharmacological implications. , 1992, Medical hypotheses.

[38]  M. Rathbone,et al.  Adenosine and its nucleotides stimulate proliferation of chick astrocytes and human astrocytoma cells , 1992, Neuroscience Research.

[39]  N. Tolbert,et al.  A modification of the Lowry procedure to simplify protein determination in membrane and lipoprotein samples. , 1978, Analytical biochemistry.

[40]  M. Stojiljkovic,et al.  Ecto-ATPase and ecto-ATP-diphosphohydrolase are co-localized in rat hippocampal and caudate nucleus synaptic plasma membranes. , 2003, Physiological research.

[41]  M. Yacoub,et al.  Regulation of ecto-5'-nucleotidase by TNF-alpha in human endothelial cells. , 2002, Molecular and cellular biochemistry.

[42]  Y. Nakata,et al.  Extracellular ATP triggers tumor necrosis factor-alpha release from rat microglia. , 2000, Journal of neurochemistry.

[43]  R. Penniall.  An improved method for the determination of inorganic phosphate by the isobutanol-benzene extraction procedure☆ , 1966 .

[44]  V. P. Whittaker,et al.  The isolation of nerve endings from brain: an electron-microscopic study of cell fragments derived by homogenization and centrifugation. , 1962, Journal of anatomy.