Local anesthetics depolarize mitochondrial membrane potential by intracellular alkalization in rat dorsal root ganglion neurons

Anesthesia and Analgesia

Volumn 111, Issue 3, 2010, Pages 775-783

  Onizuka, Shin ^a   Tamura, Ryuji ^a   Hosokawa, Nobuko ^a   Kawasaki, Yuko ^a   Tsuneyoshi, Isao ^a  

^a UNIVERSITY OF MIYAZAKI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIUM CHLORIDE; BUPIVACAINE; LIDOCAINE; LIDOCAINE ETHOBROMIDE; LOCAL ANESTHETIC AGENT; MEPIVACAINE; PROCAINE; BENZOPYRAN DERIVATIVE; CARBOXY SEMINAPHTHORHODAMINEFLUORIDE; CARBOXY-SEMINAPHTHORHODAMINEFLUORIDE; FLUORESCENT DYE; NAPHTHOL DERIVATIVE; RHODAMINE;

ANIMAL CELL; ARTICLE; CELL PH; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; MEMBRANE DEPOLARIZATION; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; PH MEASUREMENT; PRIORITY JOURNAL; RAT; SPINAL GANGLION; ANIMAL; CALIBRATION; CYTOLOGY; DOSE RESPONSE; FEMALE; MALE; NERVE CELL; PH; WISTAR RAT;

ANESTHETICS, LOCAL; ANIMALS; BENZOPYRANS; CALIBRATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLUORESCENT DYES; GANGLIA, SPINAL; HYDROGEN-ION CONCENTRATION; MALE; MEMBRANE POTENTIAL, MITOCHONDRIAL; NAPHTHOLS; NEURONS; RATS; RATS, WISTAR; RHODAMINES;

EID: 77956414668     PISSN: 00032999     EISSN: None     Source Type: Journal    
DOI: 10.1213/ANE.0b013e3181e9f03b     Document Type: Article

References (39)

1. Kalichman MW, Powell HC, Myers RR. Quantitative histologic analysis of local anesthetic-induced injury to rat sciatic nerve. J Pharmacol Exp Ther 1989;250:406-13
2. Sakura S, Kirihara Y, Muguruma T, Kishimoto T, Saito Y. The comparative neurotoxicity of intrathecal lidocaine and bupivacaine in rats. Anesth Analg 2005;101:541-7
3. Onizuka S, Takasaki M, Syed NI. Long-term exposure to local but not inhalation anesthetics affects neurite regeneration and synapse formation between identified lymnaea neurons. Anesthesiology 2005;102:353-63
4. Werdehausen R, Braun S, Essmann F, Schulze-Osthoff K, Walczak H, Lipfert P, Stevens MF. Lidocaine induces apoptosis via the mitochondrial pathway independently of death receptor signaling. Anesthesiology 2007;107:136-43
5. Johnson ME, Uhl CB, Spittler KH, Wang H, Gores GJ. Mitochondrial injury and caspase activation by the local anesthetic lidocaine. Anesthesiology 2004;101:1184-94
6. Tembe V, Henderson BR. BARD1 translocation to mitochondria correlates with Bax oligomerization, loss of mitochondrial membrane potential, and apoptosis. J Biol Chem 2007;282:20,513-22
7. McGill A, Frank A, Emmett N, Turnbull DM, Birch-Machin MA, Reynolds NJ. The anti-psoriatic drug anthralin accumulates in keratinocyte mitochondria, dissipates mitochondrial membrane potential, and induces apoptosis through a pathway dependent on respiratory competent mitochondria. FASEB J 2005;19:1012-4
8. Andersson BS, A TY, Jones DP. Mitochondrial transmembrane potential and pH gradient during anoxia. Am J Physiol 1987;252:349-55
9. Kauppinen R. Proton electrochemical potential of the inner mitochondrial membrane in isolated perfused rat hearts, as measured by exogenous probes. Biochim Biophys Acta 1983;725:131-7
10. Broekemeier KM, Klocek CK, Pfeiffer DR. Proton selective substate of the mitochondrial permeability transition pore: regulation by the redox state of the electron transport chain. Biochemistry 1998;37:13,059-65
11. Marzulli D, La Piana G, Cafagno L, Fransvea E, Lofrumento NE. Proton translocation linked to the activity of the bi-transmembrane electron transport chain. Arch Biochem Biophys 1995;319:36-48
12. Yokota K, Tatebayashi H, Matsuo T, Shoge T, Motomura H, Matsuno T, Fukuda A, Tashiro N. The effects of neuroleptics on the GABA-induced Cl- current in rat dorsal root ganglion neurons: differences between some neuroleptics. Br J Pharmacol 2002;135:1547-55
13. Smiley ST, Reers M, Mottola-Hartshorn C, Lin M, Chen A, Smith TW, Steele GD Jr, Chen LB. Intracellular heterogeneity in mitochondrial membrane potentials revealed by a J-aggregateforming lipophilic cation JC-1. Proc Natl Acad Sci USA 1991;88:3671-5
14. Cossarizza A, Baccarani-Contri M, Kalashnikova G, Franceschi C. A new method for the cytofluorimetric analysis of mitochondrial membrane potential using the J-aggregate forming lipophilic cation 5,5',6,6'-tetrachloro-1,1',3,3'- tetraethylbenzimidazolcarbocyanine iodide (JC-1). Biochem Biophys Res Commun 1993;197:40-5
15. Willoughby D, Thomas RC, Schwiening CJ. Comparison of simultaneous pH measurements made with 8-hydroxypyrene- 1,3,6-trisulphonic acid (HPTS) and pH-sensitive microelectrodes in snail neurons. Pflugers Arch 1998;436:615-22
16. Overly CC, Lee KD, Berthiaume E, Hollenbeck PJ. Quantitative measurement of intraorganelle pH in the endosomal-lysosomal pathway in neurons by using ratiometric imaging with pyranine. Proc Natl Acad Sci USA 1995;92:3156-60
17. Takahashi A, Zhang Y, Centonze E, Herman B. Measurement of mitochondrial pH in situ. Biotechniques 2001;30:804-8
18. Balut C, vandeVen M, Despa S, Lambrichts I, Ameloot M, Steels P, Smets I. Measurement of cytosolic and mitochondrial pH in living cells during reversible metabolic inhibition. Kidney Int 2008;73:226-32
19. Baysal K, Brierley GP, Novgorodov S, Jung DW. Regulation of the mitochondrial Na+/Ca2+ antiport by matrix pH. Arch Biochem Biophys 1991;291:383-9
20. Sanchez V, Arthur GR, Strichartz GR. Fundamental properties of local anesthetics: I. The dependence of lidocaine's ionization and octanol: buffer partitioning on solvent and temperature. Anesth Analg 1987;66:159-65
21. De Jong RH. Local anesthetic pharmacology. In: Brown DL, ed. Regional Anesthesia and Analgesia. Philadelphia: WB Saunders, 1996: 125-42
22. Mitchell P. Coupling of phosphorylation to electron and hydrogen transfer by a chemi-osmotic type of mechanism. Nature 1961;191:144-8
23. Dzbek J, Korzeniewski B. Control over the contribution of the mitochondrial membrane potential and proton gradient to the protonmotive force. J Biol Chem 2008;283:33,232-9
24. Schoolwerth AC, Gesek FA, Culpepper RM. Proton compartmentation in rat renal cortical tubules. Am J Physiol 1989;256:986-93
25. Mollica MP, Iossa S, Liverini G, Soboll S. Steady state changes in mitochondrial electrical potential and proton gradient in perfused liver from rats fed a high fat diet. Mol Cell Biochem 1998;178:213-7
26. Bernardi P, Vassanelli S, Veronese P, Colonna R, Szabó I, Zoratti M. Modulation of the mitochondrial permeability transition pore. Effect of protons and divalent cations. J Biol Chem 1992;267:2934-9
27. Bernardi P. Modulation of the mitochondrial cyclosporine A-sensitive permeability transition pore by the proton electrochemical gradient. Evidence that the pore can be opened by membrane depolarization. J Biol Chem 1992;267:8834-9
28. Hamaguchi MS, Watanabe K, Hamaguchi Y. Regulation of intracellular pH in sea urchin eggs by medium containing both weak acid and base. Cell Struct Funct 1997;22:387-98
29. González-Méndez R, Hahn GM, Wade-Jardetzky NG, Jardetzky O. Comparison of intracellular pH measurements by 31P NMR and weak acid partitioning in Chinese hamster ovary fibroblasts. Magn Reson Med 1988;6:373-80
30. Irwin W, Fontaine E, Agnolucci L, Penzo D, Betto R, Bortolotto S, Reggiani C, Salviati G, Bernardi P. Bupivacaine myotoxicity is mediated by mitochondria. J Biol Chem 2002;277:12,221-7
31. Hoyt KR, McLaughlin BA, Higgins DS Jr, Reynolds IJ. Inhibition of glutamate-induced mitochondrial depolarization by tamoxifen in cultured neurons. J Pharmacol Exp Ther 2000;293:480-6
32. He L, Poblenz AT, Medrano CJ, Fox DA. Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. J Biol Chem 2000;275:12,175-84
33. Yodozawa S, Speake T, Elliott A. Intracellular alkalinization mobilizes calcium from agonist-sensitive pools in rat lacrimal acinar cells. J Physiol 1997;15:601-11
34. Potapenko E, Kostyuk E, Voitenko N, Kostyuk P. Alkalinization-induced changes in intracellular calcium in rat spinal cord neurons. Neurochem Res 2004;29:1659-65
35. Speake T, Elliott AC. Modulation of calcium signals by intracellular pH in isolated rat pancreatic acinar cells. J Physiol 1998;15:415-30 (Pubitemid 28048370)
36. Mironov SL, Lux HD. Cytoplasmic alkalinization increases high-threshold calcium current in chick dorsal root ganglion neurones. Pflugers Arch 1991;419:138-43
37. Bernardi P, Azzone GF. Delta pH induced calcium fluxes in rat liver mitochondria. Eur J Biochem 1979;102:555-62
38. Werdehausen R, Fazeli S, Braun S, Hermanns H, Essmann F, Hollmann MW, Bauer I, Stevens MF. Apoptosis induction by different local anaesthetics in a neuroblastoma cell line. Br J Anaesth 2009;103:711-8
39. Auroy Y, Benhamou D, Bargues L, Ecoffey C, Falissard B, Mercier FJ, Bouaziz H, Samii K. Major complications of regional anesthesia in France: the SOS Regional Anesthesia Hotline Service. Anesthesiology 2002;97:1274-80