Antiepileptic carbamazepine drug treatment induces alteration of membrane in red blood cells: Possible positive effects on metabolism and oxidative stress

Biochimie

Volumn 95, Issue 4, 2013, Pages 833-841

  Ficarra, Silvana ^a   Misiti, Francesco ^b   Russo, Annamaria ^a   Carelli Alinovi, Cristiana ^b   Bellocco, Ersilia ^a   Barreca, Davide ^a   Laganà, Giuseppina ^a   Leuzzi, Ugo ^a   Toscano, Giovanni ^a   Giardina, Bruno ^c,d   Galtieri, Antonio ^a   Tellone, Ester ^a  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF CASSINO AND SOUTHERN LAZIO   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d CNR   (Italy)

Author keywords

Acetylcholinesterase; Anionic transport; Carbamazepine; Nitric oxide; Red blood cell

Indexed keywords

ADENOSINE TRIPHOSPHATE; CARBAMAZEPINE; CARBON DIOXIDE; CASPASE 3; ERYTHROCYTE BAND 3 PROTEIN; FREE RADICAL; HEMOGLOBIN; LIPID; SCAVENGER; SUPEROXIDE;

ANION TRANSPORT; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; CYTOSOL; DRUG EFFECT; DRUG METABOLISM; DRUG TARGETING; ELIMINATION REACTION; ENZYME ACTIVITY; ERYTHROCYTE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; HUMAN TISSUE; LIPID PEROXIDATION; OXIDATIVE STRESS; PROTEIN SECRETION; VASCULARIZATION;

ADENOSINE TRIPHOSPHATE; ANION EXCHANGE PROTEIN 1, ERYTHROCYTE; ANTICONVULSANTS; BIOLOGICAL TRANSPORT; CARBAMAZEPINE; CARBON DIOXIDE; ERYTHROCYTE MEMBRANE; HUMANS; NITRIC OXIDE; OXIDATIVE STRESS;

EID: 84874645668     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2012.11.018     Document Type: Article

References (60)

1. H. Jokeit, M. Okujava, and F.G. Woermann Carbamazepine reduces memory induced activation of mesial temporal lobe structures: a pharmacological fMRI-study BMC Neurol. 1 2001 1 6
2. J.C. Ballenger, and R.M. Post Therapeutic effects of carbamazepine in affective illness: a preliminary report Commun. Psychopharmacol. 2 2 1978 159 175
3. A. Lenzi, F. Lazzerini, E. Grossi, G. Massimetti, and G.F. Placidi Use of carbamazepine in acute psychosis: a controlled study J. Int. Med. Res. 14 2 1986 78 84
4. Y.Y. Yang, H.C. Deng, and B.H. Wang The increasing use of anticonvulsants in prophylactic treatment of bipolar disorder Psychiatry Clin. Neurosci. 52 4 1998 429 431
5. U.K. Misra, J. Kalita, and C. Rathore Phenytoin and carbamazepine cross reactivity: report of a case and review of literature Postgrad. Med. J. 79 2003 703 704
6. N. Coxhead, T. Silverstone, and J. Cookson Carbamazepine versus lithium in the prophylaxis of bipolar affective disorder Acta Psychiatr. Scand. 85 2 1992 114 118
7. C.C. Kuo A common anticonvulsant binding site for phenytoin, carbamazepine, and lamotrigine in neuronal Na+ channels Mol. Pharmacol. 54 1998 712 721
8. R. Yoshimura, N. Yanagihara, T. Terao, K. Minami, Y. Toyohira, S. Ueno, Y. Uezono, K. Abe, and F. Izumi An active metabolite of carbamazepine, carbamazepine-10,11-epoxide, inhibits ion channel-mediated catecholamine secretion in cultured bovine adrenal medullary cells Psychopharmacology 135 4 1998 368 373
9. R. Yoshimura, N. Yanagihara, T. Terao, K. Minami, K. Abe, and F. Izumi Inhibition by carbamazepine of various ion channels-mediated catecholamine secretion in cultured bovine adrenal medullary cells Naunyn Schmiedebergs Arch. Pharmacol. 352 3 1995 297 303
10. F.J. Barrantes Structural basis for lipid modulation of nicotine acetylcholine receptor function Brain Res. Brain Res. Rev. 47 2004 71 95
11. J.A. Lundbaek, P. Birn, J. Girshman, A.J. Hansen, and O.S. Andersen Membrane stiffness and channel function Biochemistry 35 1996 3825 3830
12. J.O. McNamara Drugs effective in the therapy of the epilepsies J.G. Hardman, L.E. Limbird, Goodman and Gilman's The Pharmacological Basis of Therapeutics 10th ed. 2001 McGraw-Hill New York (chapter 21)
13. T. Loftsson, M.E. Brewster, and M. Masson Role of cyclodextrins in improving oral drug delivery Am. J. Drug Delivery 2 2004 261 275
14. M. Suwalsky, S. Mennickent, B. Norris, F. Villena, and C.P. Sotomayor Effects of the antiepileptic drug carbamazepine on human erythrocytes Toxicol. in Vitro 20 8 2006 1363 1369
15. P. Wong The behavior of the human erythrocyte as an imperfect osmometer: a hypothesis J. Theor. Biol. 238 2006 167 171
16. P. Wong A basis of echinocytosis and stomatocytosis in the disc-sphere transformation of the erythrocyte J. Theor. Biol. 196 1999 343 361
17. V. Bennett, and P.J. Stenbuck Association between ankyrin and the cytoplasmic domain of band 3 isolated from the human erythrocyte membrane J. Biol. Chem. 255 13 1980 6424 6432
18. S.J. Harris, and D.J. Winzor Interactions of glycolytic enzymes with erythrocyte membranes Biochim. Biophys. Acta 1038 3 1990 306 314
19. J.D. Jenkins, F.J. Kezdy, and T.L. Steck Mode of interaction of phospho-fructokinase with the erythrocyte membrane J. Biol. Chem. 260 1985 10426 10433
20. M.L. Harrison, C.C. Isaacson, D.L. Burg, R.L. Geahlen, and P.S. Low Phosphorylation of human erythrocyte band 3 by endogenous p72syk J. Biol. Chem. 269 2 1994 955 959
21. J.A. Walder, R. Chatterjee, T.L. Steck, P.S. Low, G.F. Musso, E.T. Kaiser, P.H. Rogers, and A. Arnone The interaction of hemoglobin with the cytoplasmic domain of band 3 of the human erythrocyte membrane J. Biol. Chem. 259 16 1984 10238 10246
22. H. Chu, and P.S. Low Mapping of glycolytic enzyme-binding sites on human erythrocyte band 3 Biochem. J. 400 2006 143 151
23. P.S. Low, B.M. Willardson, N. Mohandas, M. Ross, and S. Shohet Contribution of the band 3-ankyrin interaction to erythrocyte membrane mechanical stability Blood 77 7 1991 1581 1586
24. B. Giardina, I. Messana, R. Scatena, and M. Castagnola The multiple functions of hemoglobin Crit. Rev. Biochem. Mol. Biol. 30 1995 165 196
25. T. Tagawa, K. Sumi, R. Uno, Y. Itagaki, F. Fujii, and H. Yamaguchi Pure red cell aplasia during carbamazepine monotherapy Brain Dev. 19 1997 300 302
26. W.G. Zijlstra, A. Buursma, and W.P. Meeuwsen-Van Der Roest Absorption spectra of human fetal and adult oxyhemoglobin, de-oxyhemoglobin, carboxyhemoglobin and methemoglobin Clin. Chem. 37 1991 1633 1638
27. R.J. Labotka Measurement of intracellular pH and deoxyhemoglobin concentration in deoxygenated erythrocytes by phosphorus-31 nuclear magnetic resonance Biochemistry 23 1984 5549 5555
28. L. Romano, D. Peritore, E. Simone, A. Sidoti, F. Trischitta, and P. Romano Chloride-sulphate exchange chemically measured in human erythrocyte ghosts Cell. Mol. Biol. 44 1998 351 355
29. B. Giardina, and G. Amiconi Measurement of binding of gaseous and nongaseous ligands to hemoglobin by conventional spectrophotometric procedures Methods Enzymol. 76 1981 417 427
30. G.R. Bergfeld, and T. Forrester Release of ATP from human erythrocytes in response to a brief period hypoxia and hypercapnia Cardiovasc. Res. 26 1992 40 47
31. H.H. Dietrich, M.L. Ellsworth, R.S. Sprague, and R.G. Dacey Red blood cell regulation of microvascular tone through adenosine triphosphate Am. J. Physiol. 278 2000 H1294 H1298
32. A. Maccaglia, C. Mallozzi, and M. Minetti Differential effects of quercetin and resveratrol on band 3 tyrosine phosphorylation signalling of red blood cells Biochem. Biophys. Res. Commun. 305 3 2003 541 547
33. S. Ficarra, E. Tellone, B. Giardina, R. Scatena, A. Russo, F. Misiti, M.E. Clementi, D. Colucci, E. Bellocco, G. Laganà, D. Barreca, and A. Galtieri Derangement of erythrocytic AE1 in beta-thalassemia by caspase 3: pathogenic mechanisms and implications in red blood cell senescence J. Membr. Biol. 228 1 2009 43 49
34. S. Ficarra, A. Russo, F. Stefanizzi, M. Mileto, D. Barreca, E. Bellocco, G. Laganà, U. Leuzzi, B. Giardina, A. Galtieri, and E. Tellone Palytoxin induces functional changes of anion transport in red blood cells: metabolic impact J. Membr. Biol. 242 2011 31 39
35. K. Yagi, and R. Rastogi Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction Annu. Rev. Biochem. 95 1979 351 358
36. G.L. Ellman, K.D. Courtney, V. Anders, and R.M. Featherstone A new and rapid colorimetric determination of acetylcholinesterase activity Biochem. Pharmacol. 7 1961 88 95
37. P. Kleinbongard, A. Dejam, T. Lauer, T. Rassaf, A. Schindler, O. Picker, T. Scheeren, A. Gödecke, J. Schrader, R. Schulz, G. Heusch, G.A. Schaub, N.S. Bryan, M. Feelisch, and M. Kelm Plasma nitrite reflects constitutive nitric oxide synthase activity in mammals Free Radic. Biol. Med. 35 7 2003 790 796
38. R. Yoshimura, N. Yanagihara, T. Terao, Y. Uezono, Y. Toyohira, S. Ueno, K. Abe, and F. Izumi Carbamazepine-induced up-regulation of voltage-dependent Na+ channels in bovine adrenal medullary cells in culture J. Pharmacol. Exp. Ther. 287 2 1998 441 447
39. Y.M. Kim, R.V. Talanian, and T.R. Billiar Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms J. Biol. Chem. 272 1997 31138 31148
40. L. Rossig, B. Fichtlscherer, and K. Breitschopf Nitric oxide inhibits caspase-3 by S-nitrosation in vivo J. Biol. Chem. 274 1999 6823 6826
41. B. Aloin, and A. Livine Acetylcholinesterase as probe for erythrocyte membrane intactness Biochim. Biophys. Acta 339 1974 359 366
42. A. Kleinhorst, A. Oslender, C.W. Haest, and B. Deuticke Band 3-mediated flip-flop and phosphatase-catalyzed cleavage of a long-chain alkyl phosphate anion in the human erythrocyte membrane J. Membr. Biol. 165 2 1998 111 124
43. R. Ortwein, A. Oslender-Kohnen, and B. Deuticke Band 3, the anion exchanger of the erythrocyte membrane, is also a flippase Biochim. Biophys. Acta 1191 2 1994 317 323
44. M.V. Serra, D. Kamp, and C.W.M. Haest Pathways for flip-flop of mono- and di-anionic phospholipids in the erythrocyte membrane Biochim. Biophys. Acta 128 1996 263 273
45. M.L. Jennings, and M.F. Adams Modifications by papain of the structure and function of band 3, the erythrocyte anion transport protein Biochemistry 20 1981 7118 7123
46. N. Romero, A. Denicola, J.M. Souza, and R. Radi Diffusion of peroxynitrite in the presence of carbon dioxide Arch. Biochem. Biophys. 368 1 1999 23 30
47. C. Szabò, H. Ischiropoulos, and R. Radi Peroxynitrite: biochemistry, pathophysiology and development of therapeutics Nat. Rev. Drug Discov. 6 2007 662 680
48. E. Tellone, S. Ficarra, A. Russo, E. Bellocco, D. Barreca, G. Laganà, U. Leuzzi, D. Pirrolli, M.C. De Rosa, B. Giardina, and A. Galtieri Caffeine inhibits erythrocyte membrane derangement by antioxidant activity and by blocking caspase 3 activation Biochimie 94 2 2012 393 402
49. A. Galtieri, E. Tellone, L. Romano, F. Misiti, E. Bellocco, S. Ficarra, A. Russo, D. Di Rosa, M. Castagnola, B. Giardina, and I. Messana Band-3 protein function in human erythrocytes: effect of oxygenation-deoxygenation Biochim. Biophys. Acta 1564 2002 214 218
50. 2-linked transition of hemoglobin FEBS Lett. 390 1 1996 25 28
51. R.S. Sprague, M.L. Ellsworth, A.H. Stephenson, M.E. Kleinhenz, and A.J. Lonigro Deformation-induced ATP release from red blood cells requires CFTR activity Am. J. Physiol. 275 1998 1726 1732
52. J.F. Hoffman ATP compartmentation in human erythrocytes Curr. Opin. Hematol. 4 2 1997 112 115
53. 2 delivery mediated by hemoglobin oxygenation Am. J. Physiol. Heart Circ. Physiol. 280 6 2001 2833 2839
54. F. Misiti, F. Orsini, M.E. Clementi, D. Masala, E. Tellone, A. Galtieri, and B. Giardina Amyloid peptide inhibits ATP release from human erythrocytes Biochem. Cell. Biol. 86 6 2008 501 508
55. Z. Cao, J.B. Bell, J.G. Mohanty, E. Nagababu, and J.M. Rifkind Nitrite enhances RBC hypoxic ATP synthesis and the release of ATP into the vasculature: a new mechanism for nitrite-induced vasodilation Am. J. Physiol. Heart Circ. Physiol. 297 2009 1494 1503
56. P. Kleinbongard, R. Schulz, T. Rassaf, T. Lauer, A. Dejam, T. Jax, I. Kumara, P. Gharini, S. Kabanova, B. Ozuyaman, H.G. Schnurch, A. Godecke, A.A. Weber, M. Robenek, H. Robenek, W. Bloch, P. Rosen, and M. Kelm Red blood cells express a functional endothelial nitric oxide synthase Blood 107 7 2006 2943 2951
57. A.L. Jones, and A.T. Proudfoot Features and management of poisoning with modern drugs used to treat epilepsy QJM 91 5 1998 325 332 (Review)
58. I.M. Araújo, A.F. Ambrósio, E.C. Leal, M.J. Verdasca, J.O. Malva, P. Soares-da-Silva, A.P. Carvalho, and C.M. Carvalho Neurotoxicity induced by antiepileptic drugs in cultured hippocampal neurons: a comparative study between carbamazepine, oxcarbazepine, and two new putative antiepileptic drugs, BIA 2-024 and BIA 2-093 Epilepsia 45 12 2004 1498 1505
59. A. Spinedi, L. Pacini, C. Limatola, P. Luly, and R.N. Farias A study of human erythrocyte acetylcholinesterase inhibition by chlorpromazine Biochem. J. 1 278 1991 461 463
60. M. Chetty, P. Sarkar, A. Aggarwal, and V. Sakhuja Carbamazepine poisoning: treatment with haemodialysis Nephrol. Dial. Transplant. 18 1 2003 220 221