Purinergic signaling in glioma progression

Advances in Experimental Medicine and Biology

Volumn 986, Issue , 2013, Pages 81-102

  Braganhol, Elizandra ^a   Wink, Márcia Rosângela ^b   Lenz, Guido ^c   Battastini, Ana Maria Oliveira ^c  

^a FEDERAL UNIVERSITY OF PELOTAS   (Brazil)

^b UNIVERSIDADE FEDERAL DE CIÊNCIAS DA SAÚDE DE PORTO ALEGRE   (Brazil)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Adenosine; Animal models of gliomas; ATP; Cancer stem cells; E NPPs (ectonucleoside pyrophosphatase phosphodiesterase); E NTPDases (ectonucleoside triphosphate diphosphohydrolase); Ecto 5 nucleotidase CD73; Ectonucleotidases; Gliomas

Indexed keywords

ADENOSINE DEAMINASE; ALKALINE PHOSPHATASE; APYRASE; ECTONUCLEOSIDE TRIPHOSPHATE DIPHOSPHOHYDROLASE; ECTONUCLEOTIDE PYROPHOSPHATASE PHOSPHODIESTERASE; PHOSPHODIESTERASE; PURINERGIC P2X1 RECEPTOR; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2X3 RECEPTOR; PURINERGIC P2X4 RECEPTOR; PURINERGIC P2X5 RECEPTOR; PURINERGIC P2X6 RECEPTOR; PURINERGIC P2X7 RECEPTOR; PURINERGIC P2Y13 RECEPTOR; UNCLASSIFIED DRUG;

ARTICLE; CANCER GROWTH; CANCER INVASION; CANCER STEM CELL; ENZYME ACTIVITY; GLIOMA; HUMAN; MOLECULAR PATHOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

EID: 84867491570     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-94-007-4719-7_5     Document Type: Article

References (166)

1. Agresti C, Meomartini ME, Amadio S, Ambrosini E, Sera fi ni B, Franchini L, Volonte C, Aloisi F, Visentin S (2005) Metabotropic P2 receptor activation regulates oligodendrocyte progenitor migration and development. Glia 50:132-1444
2. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD, Rich JN (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756-7600
3. Baranska J, Czajkowski R, Sabala P (2004) Croos-talks between nucleotide receptor-induced signaling pathways in serum-deprived and non-starved glioma C6 cells. Adv Enzyme Regul 44:219-2322
4. Battastini AMO, da Rocha JBT, Kuplich CK, Dias RD, Sarkis JJF (1991) Characterization of an ATP diphosphohydrolase (EC 3.6.1.5) in synaptosomes from cerebral cortex of adult rats. Neurochem Res 16(12):1303-13100
5. Bavaresco L, Bernardi A, Braganhol E, Wink MR, Battastini AMO (2007) Dexamethasone inhibits proliferation and stimulates ecto-5′-nucleotidase/ CD73 activity in C6 rat glioma cell line. J Neurooncol 84:1-88
6. Bavaresco L, Bernardi A, Braganhol E, Cappellari AR, Rockenbach L, Farias PF, Wink MR, Delgado-Cañedo A, Battastini AMO (2008) The role of ecto-5′-nucleotidase/CD73 in glioma cell line proliferation. Mol Cell Biochem 319(1-2):61-688
7. Beier D, Rohrl S, Pillai DR, Schwarz S, Kunz-Schughart LA, Leukel P, Proescholdt M, Brawanski A, Bogdahn U, Trampe-Kieslich A, Giebel B, Wischhusen J, Reifenberger G, Hau P, Beier CP (2008) Temozolomide preferentially depletes cancer stem cells in glioblastoma. Cancer Res 68:5706-57155
8. Belcher SM, Zsarnovszky A, Crawford PA, Hemani H, Spurling L, Kirley TL (2006) Immunolocalization of ectonucleoside triphosphate diphosphohydrolase 3 in rat brain: implications for modulation of multiple homeostatic systems including feeding and sleep-wake behavior. Neuroscience 137:1331-13466
9. Beraudi A, Traversa U, Villani L, Sekino Y, Nagy JI, Poli A (2003) Distribution and expression of A 1 adenosine receptors, adenosine deaminase and adenosine deaminase-binding protein (CD26) in gold fish brain. Neurochem Int 42(6): 455-4644
10. Berens ME, Giese A (1999) "Those left behind." Biology and oncology of invasive glioma cells. Neoplasia 1:208-2199
11. Bernardi A, Bavaresco L, Wink MR, Jacques-Silva MC, Delgado-Cañedo A, Lenz G, Battastini AMO (2007) Indomethacin stimulates activity and expression of ecto-5′-nucleotidase/CD73 in glioma cell lines. Eur J Pharmacol 569:8-155
12. Bianchi V, Spychala J (2003) Mammalian 5′-nucleotidases. J Biol Chem 278(47):46195-461988
13. Biederbick A, Kosan C, Kunz J, Elsasser HP (2000) First apyrase splice variants have different enzymatic properties. J Biol Chem 275:19018-190244
14. Bigonnesse F, Lévesque SA, Kukulski F, Lecka J, Robson SC, Fernandes MJ, Sévigny J (2004) Cloning and characterization of mouse nucleoside triphosphate diphosphohydrolase-8. Biochemistry 43(18):5511-55199
15. 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 48:95-1111
16. Blay J, White TD, Hoskin DW (1997) The extracellular fl uid of solid carcinomas contains immunosuppressive concentrations of adenosine. Cancer Res 57:2602-26055
17. Boeck CR, Sarkis JJF, Vendite D (2002) Kinetic characterization and immunodetection of ecto-ATP diphosphohydrolase (EC 3.6.1.5) in cultured hippocampal neurons. Neurochem Int 40:449-4533
18. Bollen M, Gijsbers R, Ceulemans H, Stalmans W, Stefan C (2000) Nucleotide pyrophosphatases/phosphodiesterases on the move. Crit Rev Biochem Mol Biol 35:393-4322
19. Braganhol E, Tamajusuku ASK, Bernardi A, Wink MR, Battastini AMO (2007) Ecto-5′-nucleotidase/CD73 inhibition by quercetin in the human U138MG glioma cell line. Biochim Biophys Acta 1770:1352-13599
20. Braganhol E, Huppes D, Bernardi A, Wink MR, Lenz G, Battastini AMO (2008) A comparative study of ectonucleotidase and P2 receptor mRNA pro fi les in C6 cell line cultures and C6 ex vivo glioma model. Cell Tissue Res 335(2):331-3400
21. Braganhol E, Morrone FB, Bernardi A, Huppes D, Meurer L, Edelweiss MI, Lenz G, Wink MR, Robson SC, Battastini AMO (2009) NTPDase2 expression modulates in vivo rat glioma growth. Cancer Sci 100(8):1434-14422
22. Braganhol E, Zanin RF, Bernardi A, Bergamin LS, Cappellari AR, Campesato LF, Morrone FB, Campos MM, Calixto JB, Edelweiss MI, Wink MR, Sévigny J, Robson SC, Battastini AM (2011) Overexpression of NTPDase2 in gliomas promotes systemic in fl ammation and pulmonary injury. Purinergic Signal. doi: 10.1007/s11302-011-9276-11
23. Braun N, Sevigny J, Robson SC, Enjyoji K, Guckelberger O, Hammer K, Di Virgilio F, Zimmermann H (2000) Assignment of ecto-nucleoside triphosphate diphosphohydrolase-1/CD39 expression to microglia and vasculature of the brain. Eur J Neurosci 12:4357-43666
24. Braun N, Sevigny J, Mishra SK, 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 17:1355-13644
25. Bruno AN, Bonan CD, Wofchuk ST, Sarkis JJ, Battastini AM (2002) ATP diphosphohydrolase (NTPDase 1) in rat hippocampal slices and effect of glutamate on the enzyme activity in different phases of development. Life Sci 71(2):215-2255
26. Buckingham SC, Campbell SL, Haas BR, Montana V, Robel S, Ogunrinu T, Sontheimer H (2011) Glutamate release by primary brain tumors induces epileptic activity. Nat Med 17(10):1269-12744
27. Burnstock G (2008) Purinergic signalling and disorders of the central nervous system. Nat Rev Drug Discov 7(7):575-5900
28. Calhau C, Martel F, Soares-da-Silva P, Hipólito-Reis C, Azevedo I (2002) Regulation of [(3)H]MPP(+) transport by phosphorylation/dephosphorylation pathways in RBE4 cells: role of ecto-alkaline phosphatase. Naunyn Schmierdebergs Arch Pharmacol 365(5):349-3566
29. Cappellari AR, Vasques GJ, Bavaresco L, Braganhol E, Battastini AMO (2011) Involvement of ecto-5′-nucleotidase/ CD73 in U138MG cell adhesion. Mol Cell Biochem 359:315-3222
30. Chadwick BP, Frischauf AM (1998) The CD39-like gene family: identi fication of three new human members (CD39L2, CD39L3, and CD39L4), their murine homologues, and a member of the gene family from Drosophila melanogaster. Genomics 50(3):357-3677
31. Ciruela F, Saura C, Canela EI, Mallol J, Lluis C, Franco R (1996) Adenosine deaminase affects ligand-induced signalling by interacting with cell surface adenosine receptors. FEBS Lett 380:219-2233
32. Cunha RA, Sebastião AM (1991) Extracellular metabolism of adenine nucleotides and adenosine in the innervated skeletal muscle of the frog. Eur J Pharmacol 197:83-922
33. Cunha RA, Almeida T, Ribeiro JA (2000) Modi fication by arachidonic acid of extracellular adenosine metabolism and neuromodulatory action in the rat hippocampus. J Biol Chem 275(48):37572-375811
34. Deissler H, Blass-Kampmann S, Bruyneel E, Mareel M, Rajewsky MF (1995a) Neural cell surface differentiation antigen gp130RB13-6induces fibroblasts and glioma cells to express astroglial proteins and invasive properties. FASEB J 13:657-6666
35. Deissler H, Lottspeich F, Rajewsky MF (1995b) Affinity purification and cDNA cloning of rat neural differentiation and tumor cell surface antigen gp130RB13-6 reveals relationship to human and murine PC-1. J Biol Chem 270:9849-98555
36. Delarasse C, Gonnord P, Galante M, Auger R, Daniel H, Motta I, Kanellopoulos JM (2009) Neural progenitor cell death is induced by extracellular ATP via ligation of P2X7 receptor. J Neurochem 109:846-8577
37. Demuth T, Berens ME (2004) Molecular mechanisms of glioma cell migration and invasion. J Neurooncol 70:217-2288
38. Dornand J, Bonnafous JC, Mani JC (1978) Purification and properties of 5′-nucleotidase from lymphocyte plasma membranes. Eur J Biochem 87:459-4655
39. Ehrlich YH, Hogan MV, Pawlowska Z, Naik U, Kornecki E (1990) Ectoprotein kinase in the regulation of cellular responsiveness to extracellular ATP. Ann N Y Acad Sci 603:401-4166
40. 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 14:595-6099
41. 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(2):179-1966
42. Franco R, Casado V, Ciruela F, Saura C, Mallol J, Canela EI, Lluis C (1997) Cell surface adenosine deaminase: much more than an ecto-enzyme. Prog Neurobiol 52:283-2944
43. Franco R, Valenzuela A, Lluis C, Blanco J (1998) Enzymatic and extraenzymatic role of ecto-adenosine deaminase in lymphocytes. Immunol Rev 161:27-422
44. Fumagalli M, Brambilla R, D'Ambrosi N, Volonte C, Matteoli M, Verderio C, Abbracchio MP (2003) Nucleotidemediated calcium signaling in rat cortical astrocytes: role of P2X and P2Y receptors. Glia 43:218-3033
45. 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 17:9095-91033
46. Ganzella MG, Faraco RB, Almeida RF, Fernandes VF, Souza DO (2011) Intracerebroventricular administration of inosine is anticonvulsant against quinolinic acid-induced seizures in mice: an effect independent of benzodiazepine and adenosine receptors. Pharmacol Biochem Behav 100:271-2744
47. Gessi S, Sacchetto V, Fogli E, Merighi S, Varani K, Baraldi PG, Tabrizi MA, Leung E, MacLennan S, Borea PA (2010) Modulation of metalloproteinase-9 in U87MG glioblastoma cells by A3 adenosine receptors. Biochem Pharmacol 79:1483-14955
48. Gessi S, Merighi S, Sacchetto V, Simioni C, Borea PA (2011) Adenosine receptors and cancer. Biochim Biophys Acta 1808:1400-14122
49. Gines S, Ciruela F, Burgueño J, Casado V, Canela EI, Mallol J, Lluis C, Franco R (2001) Involvement of caveolin in ligand-induced recruitment and internalization of A1 adenosine receptor and adenosine deaminase in an epithelial cell line. Mol Pharmacol 59:1314-13233
50. Goding JW, Grobben B, Slegers H (2003) Physiological and pathophysiological functions of the ecto-nucleotide pyrophosphatase/ phosphodiesterase family. Biochim Biophys Acta 1638:1-199
51. Goldman N, Chen M, Fujita T, Xu Q, Peng W, Liu W, Jensen TK, Pei Y, Wang F, Han X, Chen JF, Schnermann J, Takano T, Bekar L, Tieu K, Nedergaard M (2010) Nat Neurosci 13(7):883-8888
52. Grobben B, Anciaux K, Roymans D, Stefan C, Bollen M, Esmans EL, Slegers H (1999) An ecto-nucleotide pyrophosphatase is one of the main enzymes involved in the extracellular metabolism of ATP in rat C6 glioma. J Neurochem 72:826-8344
53. Hansen KR, Resta R, Webb CF, Thompson LF (1995) Isolation and characterization of the promoter of the human 5′-nucleotidase 9CD730-encoding gene. Gene 167:307-3122
54. Haskó G, Sitkovsky MV, Szabó C (2004) Immunomodulatory and neuroprotective effects of inosine. Trends Pharmacol Sci 25(3):152-1577
55. Heine P, Braun N, Heilbronn A, Zimmermann H (1999) Functional characterization of rat ecto-ATPase and ecto-ATP diphosphohydrolase after heterologous expression in CHO cells. Eur J Biochem 262:102-1077
56. Heymann D, Reddington M, Kreutzberg GW (1984) Subcellular localization of 5′-nucleotidase in rat brain. J Neurochem 43(4):971-9788
57. Hicks-Berger CA, Chadwick BP, Frischauf AM, Kirley TL (2000) Expression and characterization of soluble and membrane-bound human nucleoside triphosphate diphosphohydrolase 6 (CD39L2). J Biol Chem 275: 34041-340455
58. Jacques-Silva MC, Bernardi A, Rodnight R, Lenz G (2004a) ERK, PKC and PI3K/Akt pathways mediate extracellular ATP and adenosine-induced proliferation of U138-MG human glioma cell line. Oncology 67:450-4599
59. Jacques-Silva MC, Rodnight R, Lenz G, Liao Z, Kong Q, Tran M, Kang Y, Gonzalez FA, Weisman GA, Neary JT (2004b) P2X7 receptors stimulate AKT phosphorylation in astrocytes. Br J Pharmacol 141:1106-11177
60. Joseph SM, Pifer MA, Przybylski RJ, Dubyak GR (2004) Methylene ATP analogs as modulators of extracellular ATP metabolism and accumulation. Br J Pharmacol 142:1002-10144
61. Kaczmarek E, Koziak K, Sevigny J, Siegel JB, Anrather J, Beaudoin AR, Bach FH, Robson SC (1996) Identification and characterization of CD39/vascular ATP diphosphohydrolase. J Biol Chem 271:33116-331222
62. Kegel B, Braun N, Heine P, Maliszewski CR, Zimmermann H (1997) An ecto-ATPase and an ecto-ATP diphosphohydrolase are expressed in rat brain. Neuropharmacology 36(9):1189-12000
63. Kiss DS, Zsarnovszky A, Horvath K, Gyorffy A, Bartha T, Hazai D, Sotonyi P, Somogyi V, Frenyo LV, Diano S (2009) Ecto-nucleoside triphosphate diphosphohydrolase 3 in the ventral and lateral hypothalamic area of female rats: morphological characterization and functional implications. Reprod Biol Endocrinol 7:31-433
64. Knowles AF (2011) The GDA1-CD39 superfamily: NTPDases with diverse functions. Purinergic Signal 7:21-455
65. Komoszynski M, Wojtczak A (1996) Apyrases (ATP diphosphohydrolases, EC 3.6.1.5): function and relationship to ATPases. Biochim Biophys Acta 1310:233-2411
66. Koshiba M, Kojima H, Huang S, Apasov S, Sitkovsky MV (1997) Memory of extracellular adenosine A2A purinergic receptor-mediated signalling in murine T cells. J Biol Chem 272:25881-258899
67. Kubler D, Pyerin W, Bill O, Hotz A, Sonka J, Kinzel V (1989) Evidence for ecto-protein kinase activity that phosphorylates kemptide in a cyclic AMP-dependent model. J Biol Chem 264(24):14549-145555
68. Ledur PF, Villodre ES, Paulus R, Cruz LA, Flores DG, Lenz G (2011) Extracellular ATP reduces tumorsphere growth and cancer stem cell population in U87 human glioblastoma cells. J Cell Biochem. doi: 10.1007/s11302-011-9252-99
69. Lemoli RM, Ferrari D, Fogli M, Rossi L, Pizzirani C, Forchap S, Chiozzi P, Vaselli D, Bertoli F, Foutz T, Aluigi M, Baccarani M, Di Virgilio F (2004) Extracellular nucleotides are potent stimulators of human hematopoietic stem cells in vitro and in vivo. Blood 104:1662-16700
70. Lenz G, Gottfried C, Luo Z, Avruch J, Rodnight R, Nie WJ, Kang Y, Neary JT (2000) P2Y purinergic receptor subunits recruit different Mek activators in astrocytes. Br J Pharmacol 129:927-9366
71. Lenz G, Goncalves D, Luo Z, Avruch J, Rodnight R, Neary JT (2001) Extracellular ATP stimulates an inhibitory pathway towards growth factor-induced cRaf-1 and MEKK activation in astrocyte cultures. J Neurochem 77: 1001-10099
72. Lie AA, Blümcke I, Beck H, Wiestler OD, Elger CE, Schoen SW (1999) 5′-Nucleotidase activity indicates sites of synaptic plasticity and reactive synaptogenesis in the human brain. J Neuropathol Exp Neurol 58(5):451-4588
73. Liu C, Sage JC, Miller MR, Verhaak RG, Hippenmeyer S, Vogel H, Foreman O, Bronson RT, Nishiyama A, Luo L, Zong H (2011) Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146:209-2211
74. Lohmann K (1928) The isolation of various natural phosphoric acid compounds and their identity. Biochem Z 194: 306-3277
75. Louis DN (1994) The p53 gene and protein in human brain tumors. J Neuropathol Exp Neurol 53:11-211
76. Ludwig HC, Rausch S, Schallock K, Markakis E (1999) Expression of CD73 (ecto-5′-nucleotidase) in 165 glioblastomas by immunohistochemistry and electromicroscopic histochemistry. Anticancer Res 19:1747-17522
77. Maeda T, Nishiyama F, Ogashiwa M, Takeuchi K, Hirano H (1985) Phosphatase activities in human glioma cells as revealed by light and electron microscopy-a preliminary study. J Neurooncol 3(3):211-2166
78. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, Cavenee WK, DePinho RA (2001) Malignant glioma: genetics and biology of a grave matter. Genes Dev 15:1311-13333
79. Marcus HJ, Carpenter KL, Price SJ, Hutchinson PJ (2010) In vivo assessment of high-grade glioma biochemistry using microdialysis: a study of energy-related molecules, growth factors and cytokines. J Neurooncol 97:11-233
80. Martins MJ, Negrão MR, Hipólito-Reis C (2001) Alkaline phosphatase from rat liver and kidney is differentially modulated. Clin Biochem 34:463-4688
81. Matsuoka I, Ohkubo S (2004) ATP-and adenosine-mediated signaling in the central nervous system: adenosine receptor activation by ATP through rapid and localized generation of adenosine by ecto-nucleotidases. J Pharmacol Sci 94:95-999
82. Matute C (2008) P2X7 receptors in oligodendrocytes: a novel target for neuroprotection. Mol Neurobiol 38:123-1288
83. Melani A, De Micheli E, Pinna G, Al fi eri A, Corte LD, Pedata F (2003) Adenosine extracellular levels in human brain gliomas: an intraoperative microdialysis study. Neurosci Lett 346(1-2):93-966
84. Merighi S, Mirandola P, Varani K, Gessi S, Leung E, Baraldi PG, Tabrizi MA, Borea PA (2003) A glance at adenosine receptors: novel target for antitumor therapy. Pharmacol Ther 100:31-488
85. Meyerhof O (1945) The origin of reaction of Harden and Young in cell-free alcoholic fermentation. J Biol Chem 157:105-1099
86. Morrone FB, Jacques-Silva MC, Horn AP, Bernardi A, Schwartsmann G, Rodnight R, Lenz G (2003) Extracellular nucleotides and nucleosides induce proliferation and increase nucleoside transport in human glioma cell line. J Neurooncol 64:211-2188
87. Morrone FB, Horn AP, Stella J, Spiller F, Sarkis JJ, Salbego CG, Lenz G, Battastini AM (2005) Increased resistance of glioma cell lines to extracellular ATP cytotoxicity. J Neurooncol 71:135-1400
88. Morrone FB, Oliveira DL, Gamermann P, Stella J, Wofchuk S, Wink MR, Meurer L, Edelweiss MIA, Lenz G, Battastini AMO (2006) In vivo glioblastoma growth is reduced by apyrase activity in a rat glioma model. BMC Cancer 23:2266
89. Mulero JJ, Yeung G, Nelken ST, Ford JE (1999) CD39-L4 is a secreted human apyrase, specific for the hydrolysis of nucleoside diphosphates. J Biol Chem 274:20064-200677
90. Mulero JJ, Yeung G, Nelken ST, Bright JM, McGowan DW, Ford JE (2000) Biochemical characterization of CD39L4. Biochemistry 39(42):12924-129288
91. Murphy-Piedmonte DM, Crawford PA, Kirley TL (2005) Bacterial expression, folding, purification and characterization of soluble NTPDase5 (CD39L4) ecto-nucleotidase. Biochim Biophys Acta 1747:251-2599
92. Nagy AK, Shuster TA, Delgado-Escueta AV (1986) Ecto-ATPase of mammalian synaptosomes:identi fication and enzymic characterization. J Neurochem 47:976-9866
93. Nagy A, Shuster TA, Delgado-Escueta AV (1989) Rat brain synaptosomal ATP:AMP-phosphotransferase acitvity. J Neurochem 53:1166-11722
94. Narisawa S, Hasegawa H, Watanabe K, Millán JL (1994) Stage-specific expression of alkaline phosphatase during neural development of the mouse. Dev Dyn 201:227-2355
95. Navaro JM, Olmo N, Turnay J, López-Conejo MT, Lizarbe MA (1998) Ecto-5′-nucleotidase from a human colon adenocarcinoma cell line. Correlation between enzyme activity and levels in intact cells. Mol Cell Biochem 187:121-1311
96. Neary JT, Kang Y, Willoughby KA, Ellis EF (2003) Activation of extracellular signal-regulated kinase by stretchinduced injury in astrocytes involves extracellular ATP and P2 purinergic receptors. J Neurosci 23:2348-23566
97. 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(8):1667-16722
98. Oses JP, Cardoso CM, Germano RA, Kirst IB, Rücker B, Fürstenau CR, Wink MR, Bonan CD, Battastini AM, Sarkis JJ (2004) Soluble NTPDase: an additional system of nucleotide hydrolysis in rat blood serum. Life Sci 74(26): 3275-32844
99. Paas Y, Bohana-Kashtan O, Fishelson Z (1999) Phophorylation of the complement component, C9, by an ecto-protein kinase of human leukemic cells. Immunopharmacology 42:175-1855
100. Paez JG, Recio JÁ, Rouzaut A, Notario V (2001) Identity between the PCPH proto-oncogene and the CD39L4 (NTPDase5) ectonucleoside triphosphate diphosphohydrolase gene. Int J Oncol 19:1249-12544
101. Picher M, Burch LH, Hirsh AJ, Spychala J, Boucher RC (2003) Ecto 5′-nucleotidase and nonspecific alkaline phosphatase. Two AMP-hydrolyzing ecto-enzymes with distinct roles in human airways. J Biol Chem 278:13468-134799
102. Pinsky DJ, Broekman MJ, Peschon JJ, Stocking KL, Fujita T, Ramasamy R, Connolly ES Jr, Huang J, Kiss S, Zhang Y, Choudhri TF, McTaggart RA, Liao H, Drosopoulos JH, Price VL, Marcus AJ, Maliszewski CR (2002) Elucidation of the thromboregulatory role of CD39/ectoapyrase in the ischemic brain. J Clin Invest 109:1031-10400
103. Plesner L (1995) Ecto-ATPases: identities and functions. Int Rev Cytol 158:141-2144
104. Ravera S, Aluigi MG, Calzia D, Ramoino P, Morelli A, Panfoli I (2011) Evidence for ectopic aerobic ATP production on C6 glioma cell plasma membrane. Cell Mol Neurobiol 31:313-3211
105. Recio JA, Paez JG, Maskeri B, Loveland M, Velasco JA, Notario V (2000) Both normal and transforming PCPH proteins have guanosine diphosphatase activity but only the oncoprotein cooperates with Ras in activating extracellular signal-regulated kinase ERK1. Cancer Res 60:1720-17288
106. Recio JA, Paez JG, Sanders S, Kawakami T, Notario V (2002) Partial depletion of intracellular ATP mediates the stresssurvival function of the PCPH oncoprotein. Cancer Res 62:2690-26944
107. Redegeld FA, Caldwell CC, Sitkovsky MV (1999) Ecto-protein kinases: ecto-domain phosphorylation as a novel target for pharmacological manipulation? Trends Pharmacol Sci 20:453-4599
108. Resta R, Yamashita Y, Thompson LF (1998) Ectoenzyme and signaling functions of lymphocyte. Immunol Rev 161:95-1099
109. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, Invernici G, Cenci T, Maira G, Parati EA, Stassi G, Larocca LM, De Maria R (2010) Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 468:824-8288
110. Robson SC, Sévigny J, Zimmermann H (2006) The E-NTPDase family of ectonucleotidases: structure function relationship and pathophysiological signi ficance. Purinergic Signal 2:409-4300
111. Rouzaut A, Recio JA, Notario V (2001) Expression of the protein product of the PCHP proto-conogene in human tumor cell lines. Radiat Res 155:181-1877
112. Ryu JK, Choi HB, Hatori K, Heisel RL, Pelech SL, McLarnon JG, Kim SU (2003) Adenosine triphosphate induces proliferation of human neural stem cells: role of calcium and p70 ribosomal protein S6 kinase. J Neurosci Res 72: 352-3622
113. Ryu JK, Jantaratnotai N, Serrano-Perez MC, McGeer PL, McLarnon JG (2010) Block of purinergic P2X7R inhibits tumor growth in a C6 glioma brain tumor animal model. J Neuropathol Exp Neurol 70:13-222
114. Ryu JK, Jantaratnotai N, Serrano-Perez MC, McGeer PL, McLarnon JG (2011) Block of purinergic P2X7R inhibits tumor growth in a C6 glioma brain tumor animal model. J Neuropathol Exp Neurol 70(1):13-222
115. Sadej R, Spychala J, Skladanowski AC (2006) Expression of ecto-5′-nucleotidase (eN, CD73) in cell lines from various stages of human melanoma. Melanoma Res 16(3):213-2222
116. Saura C, Mallol J, Canela E, Lluis C, Franco R (1998) Adenosine deaminase and A1 adenosine receptors internalize together followingagonist-induced receptor desensitization. J Biol Chem 273:17610-176177
117. Seehafer J, Longenecker BM, Shaw AR (1984) Biochemical characterization of human carcinoma surface antigen associated with protein kinase activity. Int J Cancer 34(6):821-8299
118. Shapiro JR (2001) Genetics of brain neoplasms. Curr Neurol Neurosci Rep 1:217-2244
119. Shi JD, Kukar T, Wang CY, Li QZ, Cruz PE, Davoodi-Semiromi A, Yang P, Gu Y, Lian W, Wu DH, She JX (2001) Molecular cloning and characterization of a novel mammalian endo-apyrase (LALP1). J Biol Chem 276: 17474-174788
120. Shukla V, Zimmermann H, Wanf L, 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. Neurosci Res 80(5):600-6100
121. Sierko E, Wojtukiewicz MZ (2007) Inhibition of platelet function: does it offer a chance of better cancer progression control? Semin Thromb Hemost 33:712-7211
122. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821-58288
123. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, Hide T, Henkelman RM, Cusimano MD, Dirks PB (2004) Identification of human brain tumour initiating cells. Nature 432:396-4011
124. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT Jr, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10:1470-14766
125. Smith TM, Carl SA, Kirley TL (1998) Immunological detection of ecto-ATPase in chicken and rat tissues: characterization, distribution, and a cautionary note. Biochem Mol Biol Int 45(5):1057-10666
126. Spychala J (2000) Tumor-promoting functions of adenosine. Pharmacol Ther 87(2-3):161-1733
127. Spychala J, Zimmermann AG, Mitchell BS (1999) Tissue-specific regulation of the Ecto-5′-nucleotidase promoter. J Biol Chem 274:22705-227122
128. Stanojevi I, Bjelobaba I, Nedeljkovi N, Drakuli D, Petrovi S, Stojiljkovi M, Horvat A (2011) Ontogenetic pro fi le of ecto-5′-nucleotidase in rat brain synaptic plasma membranes. Int J Dev Neurosci 29(4):397-4033
129. Stefan C, Jansen S, Bollen M (2006) Modulation of purinergic signaling by NPP-type ectophosphodiesterases. Purinergic Signal 2:361-3700
130. Stochaj U, Dieckhoff J, Mollenhauer J, Cramer M, Mannherz HG (1989) Evidence for the direct interaction of chicken gizzard 5′-nucleotidase with laminin and fi bronectin. Biochim Biophys Acta 992(3):385-3922
131. Stracke ML, Krutzsch HC, Unsworth EJ, Arestad A, Cioce V, Schiffmann E, Liotta LA (1992) Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulation protein. J Biol Chem 267:2524-25299
132. Su AI, Welsh JB, Sapinoso LM, Kern SG, Dimitrov P, Lapp H, Schultz PG, Powell SM, Moskaluk CA, Frierson HF Jr, Hampton GM (2001) Molecular classi fication of human carcinomas by use of gene expression signatures. Cancer Res 61(20):7388-73933
133. Takahashi T, Old LJ, Boyse EA (1970) Surface alloantigens of plasma cells. J Exp Med 131:1325-13411
134. Takano T, Lin JH, Arcuino G, Gao K, Yang J, Nedergaard M (2001) Glutamato release promotes growth of malignant gliomas. Nat Med 7:1010-10155
135. Tamajusuku AS, Villodre ES, Paulus R, Coutinho-Silva R, Battasstini AM, Wink MR, Lenz G (2010) Characterization of ATP-induced cell death in the GL261 mouse glioma. J Cell Biochem 109:983-9911
136. Taylor SR, Gonzalez-Begne M, Dewhurst S, Chimini G, Higgins CF, Melvin JE, Elliott JI (2008) Sequential shrinkage and swelling underlie P2X7-stimulated lymphocyte phosphatidylserine exposure and death. J Immunol 180: 300-3088
137. TCGA (2008) Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455:1061-10688
138. Tombetta ES, Helenius Q (1999) Glycoprotein reglucosylation and nucleotide sugar utilization in the secretory pathway: identi fication of a nucleoside diphosphatase in the endoplasmic reticulum. EMBO J 18:3282-32922
139. Tsukimoto M, Harada H, Ikari A, Takagi K (2005) Involvement of chloride in apoptotic cell death induced by activation of ATP-sensitive P2X7 purinoceptor. J Biol Chem 280:2653-26588
140. Turnay J, Olmo N, Reence G, Von der Mark K, Lizarbe MA (1989) 5′-Nucleotidase activity in cultured cell lines: effect of different assay conditions and correlation with cell proliferation. In Vitro Cell Dev Biol 25:1055-10611
141. Velasco JA, Avila MA, Notario V (1999) The product of the cph oncogene is a truncated, nucleotide-binding protein that enhances cellular survival to stress. Oncogene 18:689-7011
142. Verkhratsky A, Krishtal OA, Burnstock G (2009) Purinoceptors on neuroglia. Mol Neurobiol 39:190-2088
143. Villar J, Arenas MI, MacCarthy CM, Blanquez MJ, Tirado OM, Notario V (2007) PCPH/ENTPD5 expression enhances the invasiveness of human prostate cancer cells by a protein kinase CD-dependent mechanism. Cancer Res 67(22):10859-108688
144. Visvader JE (2011) Cells of origin in cancer. Nature 469:314-3222
145. Vlashi E, Kim K, Lagadec C, Donna LD, McDonald JT, Eghbali M, Sayre JW, Stefani E, McBride W, Pajonk F (2009) In vivo imaging, tracking, and targeting of cancer stem cells. J Natl Cancer Inst 101:350-3599
146. Vogel M, Kowalewski HJ, Zimmermann H, Janetzko A, Margolis RU, Wollny HE (1991) Association of the HNK-1 epitope with 5′-nucleotidase from Torpedo marmorata. Biochem J 278:199-2022
147. Vollmayer P, Koch M, Braun N, Heine P, Servos J, Israr E, Kegel B, Zimmermann H (2001) Multiple ecto-nucleotidase in PC12 cells: identi fication and cellular distribution after heterologous expression. J Neurochem 78:1019-10288
148. Von Deimling A, Louis DN, Wiestler OD (1995) Molecular pathways in the formation of gliomas. Glia 15:328-3388
149. Wang T-F, Guidotti G (1999) Widespread expression of ecto-apyrase (CD39) in the central nervous system. Brain Res 790:318-3222
150. Wang R, Chadalavada K, Wilshire J, Kowalik U, Hovinga KE, Geber A, Fligelman B, Leversha M, Brennan C, Tabar V (2010) Glioblastoma stem-like cells give rise to tumour endothelium. Nature 468:829-8333
151. White N, Burnstock G (2006) P2 receptors and cancer. Trends Pharmacol Sci 27:211-2177
152. Wink MR, Lenz G, Braganhol E, Tamajusuku AS, Schwartsmann G, Sarkis JJ, Battastini AM (2003) Altered extracellular ATP, ADP and AMP catabolism in glioma cell lines. Cancer Lett 198(2):211-2188
153. Wink MR, Braganhol E, Tamajusuku ASK, Lenz G, Zerbini LF, Libermann TA, Sévigny J, Battastini AM, Robson SC (2006) Nucleoside triphosphate diphosphohydrolase-(NTPDase2/CD39L1) is the dominant ectonucleotidase expressed by rat astrocytes. Neuroscience 138:421-4322
154. Yamamoto T, Geiger JD, Daddona PE, Nagy JI (1987) Subcellular, regional and immunohistochemical localization of adenosine deaminase in various species. Brain Res Bull 19:473-4844
155. Ye ZC, Sontheimer H (1999) Glioma cells release excitotoxic concentrations of glutamate. Cancer Res 59:4383-43911
156. Yegutkin GG (2008) Nucleotide-and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783(5):673-6944
157. Yegutkin GG, Henttinen T, Samburski SS, Spychala J, Jalkanen S (2002) The evidence for two opposite, ATP-generating and ATP-consuming, extracellular pathways on endothelial and lymphoid cells. Biochem J 367:121-1288
158. Yeung G, Mulero JJ, McGowan DW, Bajwa SS, Ford JE (2000) CD39L2, a gene encoding a human nucleoside diphosphatase, predominantly expressed in the heart. Biochemistry 39(42):12916-129233
159. Zhi X, Chen S, Zhou P, Shao Z, Wang L, Ou Z, Yin L (2007) RNA interference of ecto-5′-nucleotidase (CD73) inhibits human breast cancer cell growth and invasion. Clin Exp Metastasis 24(6):439-4488
160. Zhou P, Zhi X, Zhou T, Chen S, Li X, Wang L, Yin L, Shao Z, Ou Z (2007) Overexpression of Ecto-5′-nucleotidase (CD73) promotes T-47D human breast cancer cells invasion and adhesion to extracellular matrix. Cancer Biol Ther 6(3):426-4311
161. Zimmermann H (1992) 5′-Nucleotidase: molecular structure and functional aspects. Biochem J 285:345-3655
162. Zimmermann H (1996) Biochemistry, localization and functional roles of ecto-5′-nucleotidase in the nervous system. Prog Neurobiol 49(6):589-6188
163. Zimmermann H (2001) Ectonucleotidases: some recent developments and a note on nomenclature. Drug Dev Res 52:44-566
164. Zimmermann H (2006) Purinergic signalling in neuron-glia interactions. In: Novartis foundation symposium 276, Wiley, Chichester, p 113-1300
165. Zimmermann H (2006) Ectonucleotidases in the nervous system. Novartis Found Symp 276:113-1288
166. Zimmermann H, Braun N, Kegel B, Heine P (1998) New insights into molecular structure and function of ectonucleotidases in the nervous system. Neurochem Res 32:421-4255