Neuroinflammation after neonatal hypoxia–ischemia is associated with alterations in the purinergic system: adenosine deaminase 1 isoenzyme is the most predominant after insult

Molecular and Cellular Biochemistry

Volumn 403, Issue 1-2, 2015, Pages 169-177

  Pimentel, Victor Camera ^a   Moretto, Maria Beatriz ^a   Oliveira, Mariana Colino ^b   Zanini, Daniela ^a   Sebastião, Ana Maria ^b   Schetinger, Maria Rosa Chitolina ^a  

^a FEDERAL UNIVERSITY OF SANTA MARIA   (Brazil)

^b UNIVERSITY OF LISBON   (Portugal)

Author keywords

Adenosine deaminase; Adenosine receptors; Cerebral cortex; Hypoxia ischemia; Inflammation markers; Isoenzymes

Indexed keywords

9-(2-HYDROXY-3-NONYL)ADENINE; ACETYLGLUCOSAMINIDASE; ADENINE; ADENOSINE A1 RECEPTOR; ADENOSINE DEAMINASE; ADENOSINE KINASE; ISOENZYME; PEROXIDASE; PURINE DERIVATIVE;

ANALOGS AND DERIVATIVES; ANIMAL; BRAIN; BRAIN CORTEX; ENZYMOLOGY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INFLAMMATION; MALE; METABOLISM; NEWBORN; PATHOLOGY; WESTERN BLOTTING; WISTAR RAT;

ACETYLGLUCOSAMINIDASE; ADENINE; ADENOSINE DEAMINASE; ADENOSINE KINASE; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; BRAIN; CEREBRAL CORTEX; HYPOXIA-ISCHEMIA, BRAIN; INFLAMMATION; ISOENZYMES; MALE; PEROXIDASE; PURINES; RATS, WISTAR; RECEPTOR, ADENOSINE A1;

EID: 84940008587     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-015-2347-9     Document Type: Article

References (61)

1. Vannucci SJ, Hagberg H (2004) Hypoxia-ischemia in the immature brain. J Exp Biol 207(18):3149–3154
2. Ferriero DM (2004) Neonatal brain injury. N Engl J Med 351:1985–1995. doi:10.1056/NEJMra041996
3. Nelson KB, Lynch JK (2004) Stroke in newborn infants. Lancet Neurol 3:150–158. doi:10.1016/S1474-4422(04)00679-9
4. Derrick M, Drobyshevsky A, Ji X, Tan S (2007) A model of cerebral palsy from fetal hypoxia-ischemia. Stroke 38:731–735. doi:10.1161/01STR.0000251445.94697.64
5. Berger R, Garnier Y (2000) Perinatal brain injury. J Perinat Med 28:261–285. doi:10.1515/JPM.2000.034
6. Moretto MB, Arteni NS, Lavinsky D, Netto CA, Rocha JB, Souza DO, Wofchuk S (2005) Hypoxic-ischemic insult decreases glutamate uptake by hippocampal slices from neonatal rats: prevention by guanosine. Exp Neurol 195:400–406. doi:10.1016/j.expneurol.2005.06.005
7. Richardson PJ, Brown SJ, Bailyes EM, Luzio JP (1987) Ectoenzymes control adenosine modulation of immunoisolated cholinergic synapses. Nature 327:232–234. doi:10.1038/327232a0
8. Latini S, Pedata F (2008) Adenosine in the central nervous system: release mechanisms and extracellular concentrations. J Neurochem 79:463–484. doi:10.1046/j.1471-4159.2001.00607.x
9. Dale N, Frenguelli BG (2009) Release of adenosine and ATP during ischemia and epilepsy. Curr Neuropharmacol 7:160–179. doi:10.2174/157015909789152146
10. Fredholm BB, Arslan G, Halldner L, Kull B, Schulte G, Wasserman W (2000) Structure and function of adenosine receptors and their genes. Naunyn Schmiedebergs Arch Pharmacol 362:364–374. doi:10.1007/s002100000313
11. Abbracchio MP, Ceruti S (2007) P1 receptors and cytokine secretion. Purinergic Signal 3:13–25. doi:10.1007/s11302-006-9033-z
12. Blackburn MR, Lee CG, Young HW, Zhu Z, Chunn JL, Kang MJ, Banerjee SK, Elias JA (2003) Adenosine mediates IL-13-induced inflammation and remodeling in the lung and interacts in an IL-13-adenosine amplification pathway. J Clin Invest 112:332–344. doi:10.1172/JCI200316815
13. Sharoyan S, Antonyan A, Mardanyan S, Lupidi G, Cristalli G (2006). Influence of dipeptidyl peptidase IV on enzymatic properties of adenosine deaminase. Acta Biochim Pol 53:539–546
14. Franco R, Pacheco R, Gatell JM, Gallart T, Lluis C (2007) Enzymatic and extraenzymatic role of adenosine deaminase 1 in T-cell-dendritic cell contacts and in alterations of the immune function. Crit Rev Immunol 27:495–509. doi:10.1615/CritRevImmunol.v27.i6.10
15. Saura CA, Mallol J, Canela EI, Lluis C, Franco R (1998) Adenosine deaminase and A1 adenosine receptors internalize together following agonist-induced receptor desensitization. J Biol Chem 273:17610–17617. doi:10.1074/jbc.273.28.17610
16. Herrera C, Casadó V, Ciruela F, Schofield P, Mallol J, Lluis C, Franco R (2001) Adenosine A2B receptors behave as an alternative anchoring protein for cell surface adenosine deaminase in lymphocytes and cultured cells. Mol Pharmacol 59:127–134. doi:10.1124/mol.59.1.127
17. Xavier DO, Amaral LS, Gomes MA, Rocha MA, Campos PR, Cota BD, Tafuri LS, Paiva AM, Silva JH, Andrade SP, Belo AV (2010) Metformin inhibits inflammatory angiogenesis in a murine sponge model. Biomed Pharmacother 64:220–225. doi:10.1016/j.biopha.2009.08.004
18. Bradley PP, Christensen RD, Rothstein G (1982) Cellular and extracellular myeloperoxidase in pyogenic inflammation. Blood 60:618–622
19. Nagra RM, Becher B, Tourtellotte WW, Antel JP, Gold D, Paladino T, Smith RA, Nelson JR, Reynolds WF (1997) Immunohistochemical and genetic evidence of myeloperoxidase involvement in multiple sclerosis. J Neuroimmunol 78:97–107. doi:10.1016/S0165-5728(97)00089-1
20. Klebanoff SJ (1970) Myeloperoxidase: contribution to the microbicidal activity of intact leukocytes. Science 169:1095–1097. doi:10.1126/science.169.3950.1095
21. Johansson MW, Patarroyo M, Oberg F, Siegbahn A, Nilsson K (1997) Myeloperoxidase mediates cell adhesion via the alpha M beta 2 integrin (Mac-1, CD11b/CD18). J Cell Sci 110:1133–1139
22. Pimentel VC, Bellé LP, Pinheiro FV, De Bona KS, Da Luz SC, Moretto MB (2009) Adenosine deaminase activity, lipid peroxidation and astrocyte responses in the cerebral cortex of rats after neonatal hypoxia ischemia. Int J Dev Neurosci 27:857–862. doi:10.1016/j.ijdevneu.2009.06.003
23. Rice JE, Vannucci RC, Brierley JB (1981) The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann Neurol 9:131–141. doi:10.1002/ana.410090206
24. Mustafa SJ, Tewari CP (1970) Latent adenosine deaminase in mouse brain. I. Exposure in solubilization of the mitochondrial enzyme. Biochem Biophys Acta 198:93–100. doi:10.1016/0005-2744(70)90037-9
25. Bradford MM (1976) A rapid and sensitive method for quantification of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3
26. Giusti G (1974) Adenosine deaminase. In: Bergmeyer HU (ed) Methods of enzymatic analysis, 3rd edn. Academic Press, New York, pp 1092–1099
27. Lloret S, Moreno JJ (1995) Effects of an anti-inflammatory peptide (antiflammin 2) on cell influx, eicosanoid biosynthesis and oedema formation by arachidonic acid and tetradecanoyl phorbol dermal application. Biochem Pharmacol 50:347–353. doi:10.1016/0006-2952(95)00148-S
28. Suzuki K, Ota H, Sasagawa S, Sakatani T, Fujikura T (1983) Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Anal Biochem 132:345–352. doi:10.1016/0003-2697(83)90019-2
29. Burnstock G (2007) Purine and pyrimidine receptors. Cell Mol Life Sci 64:1471–1483. doi:10.1007/s00018-007-6497-0
30. Pearson T, Currie AJ, Etherington LA, Gadalla AE, Damian K, Llaudet E, Dale N, Frenguelli BG (2003) Plasticity of purine release during cerebral ischemia: clinical implications? J Cell Mol Med 7:362–375. doi:10.1111/j.1582-4934.2003.tb00239.x
31. Kobayashi T, Yamada T, Okada Y (1998) The levels of adenosine and its metabolites in the guinea pig and rat brain during complete ischemia—in vivo study. Brain Res 787:211–219. doi:10.1016/S0006-8993(97)01481-9
32. Ungerer JPJ, Oosthuizen HM, Bissbort SH, Vermaak WJH (1992) Serum adenosine deaminase: isoenzymes and diagnostic application. Clin Chem 38:1322–1326
33. Van Ede AE, Laan RF, De Abreu RA, Stegeman AB, van de Putte LB (2002) Purine enzymes in patients with rheumatoid arthritis treated with methotrexate. Ann Rheum Dis 6:1060–1064. doi:10.1136/ard.61.12.1060
34. Xia Y, Khatchikian G, Zweier JL (1996) Adenosine deaminase inhibition prevents free radical-mediated injury in the postischemic heart. J Biol Chem 271:10096–10102. doi:10.1074/jbc.271.17.10096
35. Gervitz LM, Lutherer LO, Davies DG, Pirch JH, Fowler JC (2001) Adenosine induces initial hypoxic-ischemic depression of synaptic transmission in the rat hippocampus in vivo. Am J Physiol Regul Integr Comp Physiol 280:639–645
36. Hovi T, Smyth JF, Allison AC, Williams SC (1976) Role of adenosine deaminase in lymphocyte proliferation. Clin Exp Immunol 23:395–403
37. Snyder FF, Hershfield MS, Seegmiller JE (1978) Cytotoxic and metabolic effects of adenosine and adenine on human lymphoblasts. Cancer Res 38:2357–2362
38. Conlon BA, Law WR (2004) Macrophages are a source of extracellular adenosine deaminase-2 during inflammatory responses. Clin Exp Immunol 138:14–20. doi:10.1111/j.1365-2249.2004.02591.x
39. Desrosiers MD, Cembrola KM, Fakir MJ, Stephens LA, Jama FM, Shameli A, Mehal WZ, Santamaria P, Shi Y (2007) Adenosine deamination sustains dendritic cell activation in inflammation. J Immunol 179:1884–1892. doi:10.4049/jimmunol.179.3.1884
40. Werner U, Szelenyi I (1992) Measurement of MPO activity as model for detection of granulocyte infiltration in different tissues. Agents Actions Spec 36(3–4):101–103. doi:10.1007/BF01991038
41. Barcelos LS, Talvani A, Teixeira AS, Cassali GD, Andrade SP, Teixeira MM (2004) Production and in vivo effects of chemokines CXCL1-3/KC and CCL2/JE in a model of inflammatory angiogenesis in mice. Inflamm Res 53:576–584. doi:10.1007/s00011-004-1299-4
42. Pimentel VC, Pinheiro FV, Kaefer M, Moresco RN, Moretto MB (2011) Assessment of uric acid and lipid peroxidation in serum and urine after hypoxia-ischemia neonatal in rats. Neurol Sci 32:59–65. doi:10.1007/s10072-010-0393-3
43. Blackburn MR, Datta SK, Kellems RE (1998) Adenosine-deficient mice generated using a two-stage genetic engineering strategy exhibit a combined immunodeficiency. J Biol Chem 273:5093–5100. doi:10.1074/jbc.273.9.5093
44. Winterbourn CC, Vissers MC, Kettle AJ (2000) Myeloperoxidase. Curr Opin Hematol 7:53–58. doi:10.1097/00062752-200001000-00010
45. Fröde TS, Medeiros YS (2001) Myeloperoxidase and adenosine-deaminase levels in the pleural fluid leakage induced by carrageenan in the mouse model of pleurisy. Mediat Inflamm 10:223–227. doi:10.1080/09629350123332
46. Iqbal MP, Sharif HM, Mehboobali N, Yousuf FA, Khan AH, Sellke FW (2008) N-acetyl-B-d-glucosaminidase and inflammatory response after cardiopulmonary bypass. J Coll Physicians Surg Pak 18:74–77
47. Østerholt HC, Dannevig I, Wyckoff MH, Liao J, Akgul Y, Ramgopal M, Mija DS, Cheong N, Longoria C, Mahendroo M, Nakstad B, Saugstad OD, Savani RC (2012) Antioxidant protects against increases in low molecular weight hyaluronan and inflammation in asphyxiated newborn pigs resuscitated with 100% oxygen. PLoS One 7:38839. doi:10.1371/journal.pone.0038839
48. Shen H, Chen GJ, Harvey BK, Bickford PC, Wang Y (2005) Inosine reduces ischemic brain injury in rats. Stroke 36:654–659. doi:10.1161/01.STR.0000155747.15679.04
49. Spitsin S, Hooper DC, Leist T, Streletz LJ, Mikheeva T, Koprowskil H (2001) Inactivation of peroxynitrite in multiple sclerosis patients after oral administration of inosine may suggest possible approaches to therapy of the disease. Mult Scler 7:313–319. doi:10.1191/135245801681138013
50. Johansson B, Halldner L, Dunwiddie TV, Masino SA, Poelchen W, Gimenez-Llort L, Escorihuela RM, Fernandez-Teruel A, Wiesenfeld-Hallin Z, Xu XJ, Hardemark A, Betsholtz C, Herlenius E, Fredholm BB (2001) Hyperalgesia, anxiety, and decreased hypoxic neuroprotection in mice lacking the adenosine A1 receptor. Proc Natl Acad Sci USA 98:9407–9412. doi:10.1073/pnas.161292398
51. Sebastiao AM, de Mendonça A, Moreira T, Ribeiro JA (2001). Activation of synaptic NMDA receptors by action potential-dependent release of transmitter during hypoxia impairs recovery of synaptic transmission on reoxygenation. J Neurosci 21:8564–8571
52. Wardas J (2002). Neuroprotective role of adenosine in the CNS. Pol J Pharmacol 54:313-326
53. De Mendonça A, Sebastião AM, Ribeiro JA (2000) Adenosine: does it have a neuroprotective role after all? Brain Res Rev 33:258–274. doi:10.1016/S0165-0173(00)00033-3
54. Ciccarelli R, Di Iorio P, Ballerini P, Ambrosini G, Giuliani P, Tiboni GM, Caciagli F (1994) Effects of exogenous ATP and related analogues on the proliferation rate of dissociated primary cultures of rat astrocytes. J Neurosci Res 39:556–566. doi:10.1002/jnr.490390507
55. Ciccarelli R, Ballerini P, Sabatino G, Rathbone MP, D’Onofrio M, Caciagli F, Di Iorio P (2001) Involvement of astrocytes in purine-mediated reparative processes in the brain. Int J Dev Neurosci 19:395–414. doi:10.1016/S0736-5748(00)00084-8
56. Rudolphi KA, Schubert P, Parkinson FE, Fredholm BB (1992) Adenosine and brain ischemia. Cerebrovasc Brain Metab Rev 4:346–369
57. Turner CP, Yan H, Schwartz M, Othman T, Rivkees SA (2002) A1 adenosine receptor activation induces ventriculomegaly and white matter loss. Neuroreport 13:1199–1204. doi:10.1097/00001756-200207020-00026
58. Dunwiddie TV, Masino SA (2001) The role and regulation of adenosine in the central nervous system. Annu Rev Neurosci 24:31–55. doi:10.1146/annurev.neuro.24.1.31
59. Lewin E, Bleck V (1981) Electroshock seizures in mice: effect on brain adenosine and its metabolites. Epilepsia 22:577–581. doi:10.1111/j.1528-1157.1981.tb04129.x
60. Kobayashi S, Millhorn DE (1999) Stimulation of expression for the adenosine A2A receptor gene by hypoxia in PC12 cells. A potential role in cell protection. J Biol Chem 274:20358–20365. doi:10.1074/jbc.274.29.20358
61. Cunha RA (2005) Neuroprotection by adenosine in the brain: from A(1) receptor activation to A (2A) receptor blockade. Purinergic Signal 1:111–134. doi:10.1007/s11302-005-0649-1