Oxygen-glucose deprivation increases the enzymatic activity and the microvesicle-mediated release of ectonucleotidases in the cells composing the blood-brain barrier

Neurochemistry International

Volumn 59, Issue 2, 2011, Pages 259-271

  Ceruti, Stefania ^a   Colombo, Laura ^a   Magni, Giulia ^a   Viganó, Francesca ^a   Boccazzi, Marta ^a   Deli, Mária A ^b   Sperlágh, Beáta ^b   Abbracchio, Maria P ^a   Kittel, Ágnes ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Astrocytes; Brain endothelial cells; Hypoxia; NTPDases; Pericytes

Indexed keywords

NUCLEOSIDE TRIPHOSPHATE; NUCLEOTIDASE;

ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CELL; CELL DEATH; CONTROLLED STUDY; CYTOTOXICITY; ELECTRON MICROSCOPY; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME RELEASE; HUMAN; HUMAN CELL; HYPOXIC ISCHEMIC ENCEPHALOPATHY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; IN VITRO STUDY; NERVE CELL LESION; NEUROMODULATION; OUTCOME ASSESSMENT; PERICYTE; PRIORITY JOURNAL; QUANTITATIVE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; BASE SEQUENCE; BLOOD-BRAIN BARRIER; CELLS, CULTURED; DNA PRIMERS; GLUCOSE; IMMUNOHISTOCHEMISTRY; OXYGEN; POLYMERASE CHAIN REACTION; RATS;

EID: 79960364758     PISSN: 01970186     EISSN: 18729754     Source Type: Journal    
DOI: 10.1016/j.neuint.2011.05.013     Document Type: Article

References (58)

1. N.J. Abbott, L. Rönnbäck, and E. Hansson Astrocyte-endothelial interactions at the blood-brain barrier Nat. Rev. Neurosci. 7 2006 41 53 (Pubitemid 41828930)
2. M.P. Abbracchio, G. Burnstock, A. Verkhratsky, and H. Zimmermann Purinergic signalling in the nervous system: an overview Trends Neurosci. 32 2009 19 29
3. A. Al Ahmad, M. Gassmann, and O. Ogunshola Maintaining blood-brain barrier integrity: pericytes perform better than astrocytes during prolonged oxygen deprivation J. Cell. Physiol. 218 2009 612 622
4. A. Armulik, G. Genové, M. Mäe, M.H. Nisancioglu, E. Wallgard, C. Niaudet, L. He, J. Norlin, P. Lindblom, K. Strittmatter, B.R. Johansson, and C. Betsholtz Pericytes regulate the blood-brain barrier Nature 468 2010 557 561
5. Y. Banz, G. Beldi, Y. Wu, B. Atkinson, A. Usheva, and S.C. Robson CD39 is incorporated into plasma microparticles where it maintains functional properties and impacts endothelial activation Br. J. Haematol. 142 2008 627 637 (Pubitemid 352020213)
6. R.D. Bell, and B.V. Zlokovic Neurovascular mechanisms and blood-brain barrier disorder in Alzheimer's disease Acta Neuropathol. 118 2009 103 113
7. M. Bjarnegard, M. Enge, J. Norlin, S. Gustafsdottir, S. Fredriksson, A. Abramsson, M. Takemoto, E. Gustafsson, R. Fassler, and C. Betsholtz Endothelium-specific ablation of PDGFB leads to pericyte loss and glomerular, cardiac and placental abnormalities Development 131 2004 1847 1857 (Pubitemid 38559851)
8. N. Braun, J. Sevigny, S.C. Robson, K. Enjyoji, O. Guckelberger, K. Hammer, F. Di Virgilio, and H. Zimmermann Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/CD39 expression to microglia and vasculature of the brain Eur. J. Neurosci. 12 2000 4357 4366 (Pubitemid 32037844)
9. N. Braun, J. Sevigny, S.K. Mishra, S.C. Robson, S.W. Barth, R. Gerstberger, K. Hammer, and H. Zimmermann Expression of the ecto-ATPase NTPDase2 in the germinal zones of the developing and adult rat brain Eur. J. Neurosci. 17 2003 1355 1364 (Pubitemid 36560835)
10. G. Burnstock Purinergic signalling and disorders of the central nervous system Nat. Rev. Drug Discov. 7 2008 575 590 (Pubitemid 351927723)
11. F.L. Cardoso, D. Brites, and M.A. Brito Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches Brain Res. Rev. 64 2010 328 363
12. R. Cecchelli, V. Berezowski, S. Lundquist, M. Culot, Dehouck.M.-P. Renftel, and L. Fenart Modelling the blood-brain barrier in drug discovery and development Nat. Rev. Drug Discov. 6 2007 650 661 (Pubitemid 47202487)
13. E. Cocucci, G. Racchetti, and J. Meldolesi Shedding microvesicles: artefacts no more Trends Cell Biol. 19 2009 43 51
14. D. Crippa, U. Schenk, M. Francolini, P. Rosa, C. Verderio, M. Zonta, T. Pozzan, M. Matteoli, and G. Carmignoto Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis J. Physiol. 570 2006 567 582
15. R. Daneman, L. Zhou, A.A. Kebede, and B.A. Barres Pericytes are required for blood-brain barrier integrity during embryogenesis Nature 468 2010 562 566
16. M.A. Deli Potential use of tight junction modulators to reversibly open membranous barriers and improve drug delivery Biochem. Biophys. Acta 1788 2009 892 910
17. M.A. Deli, C.S. Abrahám, Y. Kataoka, and M. Niwa Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology Cell. Mol. Neurobiol. 25 2005 59 127 (Pubitemid 40558585)
18. V.L. Feigin Stroke epidemiology in the developing world Lancet 365 2005 2160 2161 (Pubitemid 40853896)
19. T. Fellin Communication between neurons and astrocytes: relevance to the modulation of synaptic and network activity J. Neurochem. 108 2009 533 544
20. M. Fumagalli, R. Brambilla, N. D'Ambrosi, C. Volonte, M. Matteoli, C. Verderio, and M.P. Abbracchio Nucleotide-mediated calcium signaling in rat cortical astrocytes: role of P2X and P2Y receptors Glia 43 2003 218 230 (Pubitemid 37047678)
21. B. Gómez-Gonzáles, and A. Escobar Altered functional development of the blood-brain barrier after early life stress in the rat Brain Res. Bull. 79 2009 376 387
22. R.F. Haseloff, I.E. Blasig, H.C. Bauer, and H. Bauer In search of the astrocytic factor(s) modulating blood-brain barrier functions in brain capillary endothelial cells in vitro Cell. Mol. Neurobiol. 25 2005 25 39 (Pubitemid 40558583)
23. B.T. Hawkins, and T.P. Davis The blood-brain barrier/neurovascular unit in health and disease Pharmacol. Rev. 57 2005 173 185 (Pubitemid 41043883)
24. + channels in cerebral ischemic preconditioning Proc. Natl. Acad. Sci. USA 92 1995 4666 4670
25. M. Imai, C. Goepfert, E. Kaczmarek, and S.C. Robson CD39 modulates IL-1 release from activated endothelial cells Biochem. Biophys. Res. Commun. 270 1 2000 272 278 (Pubitemid 30440427)
26. C. Jiang, J. Wang, X. Li, C. Liu, N. Chen, and Y. Hao Progesterone exerts neuroprotective effects by inhibiting inflammatory response after stroke Inflamm. Res. 58 2009 619 624
27. F. Joó Endothelial cells of the brain and other organ systems: some similarities and differences Prog. Neurobiol. 48 1996 255 273 (Pubitemid 26160461)
28. 3H]purine outflow evoked by short-term hypoxia and hypoglycemia in rat hippocampal slices Brain Res. 823 1999 183 190 (Pubitemid 29225507)
29. J.A. Kim, N.D. Tran, Z. Li, F. Yang, W. Zhou, and M.J. Fisher Brain endothelial hemostasis regulation by pericytes J. Cereb. Blood Flow Metab. 26 2006 209 217 (Pubitemid 43151577)
30. A. Kittel Lipopolysaccharide treatment modifies pH- and cation-dependent ecto-ATPase activity of endothelial cells J. Histochem. Cytochem. 47 1999 393 400
31. A. Kittel, M. Garrido, and G. Varga Localization of NTPDase1/CD39 in normal and transformed human pancreas J. Histochem. Cytochem. 50 2002 549 556
32. A. Kittel, B. Sperlagh, J. Pelletier, J. Sevigny, and T.L. Kirley Transient changes in the localization and activity of ecto-nucleotidases in rat hippocampus following lipopolysaccharide treatment Int. J. Dev. Neurosci. 25 2007 275 282 (Pubitemid 47058897)
33. K. Koziak, E. Kaczmarek, A. Kittel, J. Sevigny, J.K. Blusztajn, J. Schulte Am Esch 2nd, M. Imai, O. Guckelberger, C. Goepfert, and I. Qawi Palmitoylation targets CD39/endothelial ATP diphosphohydrolase to caveolae J. Biol. Chem. 275 2000 2057 2062 (Pubitemid 30060833)
34. M. Krueger, and I. Bechmann CNS pericytes: concepts, misconceptions, and a way out Glia 58 2010 1 10
35. M. McIlroy, M. O'Rourke, S.R. McKeown, D.G. Hirst, and T. Robson Pericytes influence endothelial cell growth characteristics: role of plasminogen activator inhibitor type 1 (PAI-1) Cardiovasc. Res. 69 2006 207 217 (Pubitemid 41818972)
36. A. Melani, D. Turchi, M.G. Vannucchi, S. Cipriani, M. Gianfriddo, and F. Pedata ATP extracellular concentrations are increased in the rat striatum during in vivo ischemia Neurochem. Int. 47 2005 442 448 (Pubitemid 41242625)
37. N.I. Moldovan, A.N. Radu, and N. Simionescu Endothelial cell plasma membrane obtained by chemically induced vesiculation Exp. Cell Res. 170 1987 499 510 (Pubitemid 17093697)
38. S. Nakagawa, M.A. Deli, S. Nakao, M. Honda, K. Hayashi, R. Nakaoke, Y. Kataoka, and M. Niwa Pericytes from brain microvessels strengthen the barrier integrity in primary cultures of rat brain endothelial cells Cell. Mol. Neurobiol. 27 2007 687 694 (Pubitemid 47476613)
39. S. Nakagawa, M.A. Deli, H. Kawaguchi, T. Shimizudani, T. Shimono, A. Kittel, K. Tanaka, and M. Niwa A new blood-brain barrier model using primary rat brain endothelial cells, pericytes and astrocytes Neurochem. Int. 54 2009 253 263
40. N. Nedeljkovic, I. Bjelobaba, S. Subasic, I. Lavrnja, S. Pekovic, D. Stojkov, A. Vjestica, L. Rakic, and M. Stojiljkovic Up-regulation of ectonucleotidase activity after cortical stab injury in rats Cell Biol. Int. 30 2006 541 546 (Pubitemid 43825746)
41. A. Papanikolaou, A. Papafotika, C. Murphy, T. Papamarcaki, O. Tsolas, M. Drab, T.V. Kurzchalia, M. Kasper, and S. Christoforidis Cholesterol-dependent lipid assemblies regulate the activity of the ecto-nucleotidase CD39 J. Biol. Chem. 280 2005 26406 26414 (Pubitemid 41022237)
42. Y. Persidsky, S.H. Ramirez, J. Haorah, and G.D. Kanmogne Blood-brain barrier: structural components and function under physiologic and pathologic conditions J. Neuroimmune Pharmacol. 1 2006 223 236 (Pubitemid 44244128)
43. D.J. Pinsky, M.J. Broekman, J.J. Peschon, K.L. Stocking, T. Fujita, R. Ramasamy, E.S. Connolly Jr, J. Huang, S. Kiss, Y. Zhang, T.F. Choudhri, R.A. McTaggart, H. Liao, J.H. Drosopoulos, V.L. Price, A.J. Marcus, and C.R. Maliszewski Elucidation of the thromboregulatory role of CD39/ectoapyrase in the ischemic brain J. Clin. Invest. 109 2002 1031 1040 (Pubitemid 34408578)
44. M. Potokar, M. Kreft, L. Li, J. Daniel Andersson, T. Pangrsic, H.H. Chowdhury, M. Pekny, and R. Zorec Cytoskeleton and vesicle mobility in astrocytes Traffic 8 1 2007 12 20 (Pubitemid 44921879)
45. S.C. Robson, Y. Wu, X. Sun, C. Knosalla, K. Dwyer, and K. Enjyoji Ectonucleotidases of CD39 family modulate vascular inflammation and thrombosis in transplantation Semin. Thromb. Hemost. 31 2005 217 233 (Pubitemid 40605196)
46. S.C. Robson, J. Sévigny, and H. Zimmermann The E-NTPDase family of ectonucleotidases: structure-function relationships and pathophysiological significance Purinergic Signalling 2 2006 409 430
47. J. Sevigny, C. Sundberg, N. Braun, O. Guckelberger, E. Csizmadia, I. Qawi, M. Imai, H. Zimmermann, and S.C. Robson Differential catalytic properties and vascular topography of murine nucleoside triphosphate diphosphohydrolase 1 (NTPDase1) and NTPDase2 have implications for thromboregulation Blood 99 2002 2801 2809 (Pubitemid 34525368)
48. S.C. Shih, M. Ju, N. Liu, J.R. Mo, J.J. Ney, and L.E. Smith Transforming growth factor beta1 induction of vascular endothelial growth factor receptor 1: mechanism of pericyte-induced vascular survival in vivo Proc. Natl. Acad. Sci. USA 100 2003 15859 15864 (Pubitemid 38021080)
49. V. Shukla, H. Zimmermann, L. Wang, H. Kettenmann, S. Raab, K. Hammer, J. Sevigny, S.C. Robson, and N. Braun Functional expression of the ecto-ATPase NTPDase2 and of nucleotide receptors by neuronal progenitor cells in the adult murine hippocampus J. Neurosci. Res. 80 2005 600 610 (Pubitemid 40896181)
50. M. Simard, G. Arcuino, T. Takano, Q.S. Liu, and M. Nedergaard Signaling at the gliovascular interface J. Neurosci. 23 2003 9254 9262 (Pubitemid 37243827)
51. M. Spatz Past and recent BBB studies with particular emphasis on changes in ischemic brain edema: dedicated to the memory of Dr. Igor Klatzo Acta Neurochir. Suppl. 106 2010 21 27
52. G. Taraboletti, S. D'Ascenzo, P. Borsotti, R. Giavazzi, A. Pavan, and V. Dolo Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells Am. J. Pathol. 160 2002 673 680 (Pubitemid 34160345)
53. S. Veszelka, M. Pasztoi, A.E. Farkas, I. Krizbai, N.T.K. Dung, M. Niwa, C.S. Abraham, and M.A. Deli Pentosan polysulfate protects brain endothelial cells against bacterial lipopolysaccharide-induced damages Neurochem. Int. 50 2007 219 228 (Pubitemid 44879678)
54. N. Weiss, F. Miller, S. Cazaubon, and P.O. Couraud The blood-brain barrier in brain homeostasis and neurological diseases Biochim. Biophys. Acta 1788 2009 842 857
55. M.R. Wink, E. Braganhol, A.S. Tamajusuku, G. Lenz, L.F. Zerbini, T.A. Libermann, J. Sevigny, A.M. Battastini, and S.C. Robson Nucleoside triphosphate diphosphohydrolase-2 (NTPDase2/CD39L1) is the dominant ectonucleotidase expressed by rat astrocytes Neuroscience 138 2006 421 432 (Pubitemid 43255555)
56. H. Wolburg, S. Noell, A. Mack, K. Wolburg-Buchholz, and P. Fallier-Becker Brain endothelial cells and the glio-vascular complex Cell Tissue Res. 335 2009 75 96
57. G. Yegutkin Nucleotide- and nucleoside-converting ectoenzymes: Important modulators of purinergic signalling cascade Biochim. Biophys. Acta 1783 2008 673 694
58. B.V. Zlokovic The blood-brain barrier in health and chronic neurodegenerative disorders Neuron 57 2008 178 201