Hyperglycemia magnifies bupivacaine-induced cell apoptosis triggered by mitochondria dysfunction and endoplasmic reticulum stress

Journal of Neuroscience Research

Volumn 91, Issue 6, 2013, Pages 786-798

  Li, Le ^a   Ye, Xiao Ping ^a   Lu, Ai Zhu ^a   Zhou, Shu Qin ^a   Liu, Hui ^a   Liu, Zhong Jie ^a   Jiang, Shan ^a   Xu, Shi Yuan ^a  

^a SOUTHERN MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Bupivacaine; Endoplasmic reticulum stress; Glucose; Mitochondrial dysfunction; Reactive oxygen species

Indexed keywords

BUPIVACAINE; CASPASE 12; CASPASE 3; CHOLECYSTOKININ OCTAPEPTIDE; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; MESSENGER RNA; PLACEBO; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SERINE PROTEINASE OMI; SUCCINATE DEHYDROGENASE (UBIQUINONE);

APOPTOSIS; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL PROLIFERATION; CELL STRUCTURE; CELL VIABILITY; CONCENTRATION (PARAMETERS); DIABETIC NEUROPATHY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG CYTOTOXICITY; ENDOPLASMIC RETICULUM STRESS; FLOW CYTOMETRY; GROWTH INHIBITION; HYPERGLYCEMIA; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION SWELLING; NEUROTOXICITY; PERIPHERAL NEUROPATHY; PREMEDICATION; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANESTHETICS, LOCAL; APOPTOSIS; BLOTTING, WESTERN; BUPIVACAINE; CELL SURVIVAL; ENDOPLASMIC RETICULUM STRESS; FLOW CYTOMETRY; HUMANS; HYPERGLYCEMIA; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICROSCOPY, ELECTRON, TRANSMISSION; MITOCHONDRIA; NEURONS; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84876474647     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.23216     Document Type: Article

References (49)

1. Abbas W, Khan KA, Tripathy MK, Dichamp I, Keita M, Rohr O, Herbein G. 2012. Inhibition of ER stress-mediated apoptosis in macrophages by nuclear-cytoplasmic relocalization of eEF1A by the HIV-1 Nef protein. Cell Death Dis 3:e368.
2. Al-Nasser B. 2004. Toxic effects of epidural analgesia with ropivacaine 0.2% in a diabetic patient. J Clin Anesth 16:220-223.
3. Arai Y, Kondo T, Tanabe K, Zhao QL, Li FJ, Ogawa R, Li M, Kasuya M. 2002. Enhancement of hyperthermia-induced apoptosis by local anesthetics on human histiocytic lymphoma U937 cells. J Biol Chem 277:18986-18993.
4. Araki E, Oyadomari S, Mori M. 2003. Endoplasmic reticulum stress and diabetes mellitus. Intern Med 42:7-14.
5. Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F, Youle RJ. 2003. Mitochondrial release of AIF and EndoG requires caspase activation downstream of Bax/Bak-mediated permeabilization. EMBO J 22:4385-4399.
6. Auroy Y, Benhamou D, Bargues L, Ecoffey C, Falissard B, Mercier FJ, Bouaziz H, Samii K. 2002. Major complications of regional anesthesia in France: The SOS Regional Anesthesia Hotline Service. Anesthesiology 97:1274-1280.
7. Barateiro A, Vaz AR, Silva SL, Fernandes A, Brites D. 2012. ER stress, mitochondrial dysfunction and calpain/JNK activation are involved in oligodendrocyte precursor cell death by unconjugated bilirubin. Neuromol Med (in press).
8. Bernardi P, Krauskopf A, Basso E, Petronilli V, Blachly-Dyson E, Di Lisa F, Forte MA. 2006. The mitochondrial permeability transition from in vitro artifact to disease target. FEBS Lett 273:2077-2099.
9. 2+ antagonist nimodipine on functional deficits in the peripheral and central nervous system of streptozotocin-diabetic rats. Brain Res 1035:86-93.
10. Boyce M, Yuan J. 2006. Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ 13:363-373.
11. Brownlee M. 2001. Biochemistry and molecular cell biology of diabetic complications. Nature 414:813-820.
12. Cela O, Piccoli C, Scrima R, Quarato G, Marolla A, Cinnella G, Dambrosio M, Capitanio N. 2010. Bupivacaine uncouples the mitochondrial oxidative phosphorylation, inhibits respiratory chain complexes I and III and enhances ROS production: results of a study on cell cultures. Mitochondrion 10:487-496.
13. -/- mice on a Western diet. Mol Genet Metab (in press).
14. Drummond IA, Lee AS, Resendez E Jr, Steinhardt RA. 1987. Depletion of intracellular calcium stores by calcium ionophore A23187 induces the genes for glucose-regulated proteins in hamster fibroblasts. J Biol Chem 262:12801-12805.
15. Gaspar JM, Castilho A, Baptista FI, Liberal J, Ambrosio AF. 2010. Long-term exposure to high glucose induces changes in the content and distribution of some exocytotic proteins in cultured hippocampal neurons. Neuroscience 171:981-992.
16. Halangk W, Matthias R, Nedelev B, Schild L, Meyer F, Schulz HU, Lippert H. 1997. [Modification of energy supply by pancreatic mitochondria in acute experimental pancreatitis]. Zentralbl Chir 122:305-308.
17. Hampl KF, Schneider MC, Thorin D, Ummenhofer W, Drewe J. 1995. Hyperosmolarity does not contribute to transient radicular irritation after spinal anesthesia with hyperbaric 5% lidocaine. Reg Anesth 20:363-368.
18. Johnson ME, Uhl CB, Spittler KH, Wang H, Gores GJ. 2004. Mitochondrial injury and caspase activation by the local anesthetic lidocaine. Anesthesiology 101:1184-1194.
19. Kroin JS, Buvanendran A, Tuman KJ, Kerns JM. 2012. Safety of local anesthetics administered intrathecally in diabetic rats. Pain Med 13:802-807.
20. Lelkes E, Unsworth BR, Lelkes PI. 2001. Reactive oxygen species, apoptosis and altered NGF-induced signaling in PC12 pheochromocytoma cells cultured in elevated glucose: an in vitro cellular model for diabetic neuropathy. Neurotox Res 3:189-203.
21. Li M, Yu L, She T, Gan Y, Liu F, Hu Z, Chen Y, Li S, Xia H. 2012. Astragaloside IV attenuates Toll-like receptor 4 expression via NF-kappaB pathway under high glucose condition in mesenchymal stem cells. Eur J Pharmacol (in press).
22. Li ZG, Zhang W, Sima AA. 2003. C-peptide enhances insulin-mediated cell growth and protection against high glucose-induced apoptosis in SH-SY5Y cells. Diabetes Metab Res Rev 19:375-385.
23. Little AA, Edwards JL, Feldman EL. 2007. Diabetic neuropathies. Pract Neurol 7:82-92.
24. C(T) method. Methods 25:402-408.
25. Lu J, Xu SY, Zhang QG, Xu R, Lei HY. 2011. Bupivacaine induces apoptosis via mitochondria and p38 MAPK dependent pathways. Eur J Pharmacol 657:51-58.
26. Lucchinetti E, Awad AE, Rahman M, Feng J, Lou PH, Zhang L, Ionescu L, Lemieux H, Thebaud B, Zaugg M. 2012. Antiproliferative effects of local anesthetics on mesenchymal stem cells: potential implications for tumor spreading and wound healing. Anesthesiology 116:841-856.
27. Nagy G, Koncz A, Fernandez D, Perl A. 2007. Nitric oxide, mitochondrial hyperpolarization, and T cell activation. Free Radic Biol Med 42:1625-1631.
28. Nonaka I, Takagi A, Ishiura S, Nakase H, Sugita H. 1983. Pathophysiology of muscle fiber necrosis induced by bupivacaine hydrochloride (Marcaine). Acta Neuropathol 60:167-174.
29. Park CJ, Park SA, Yoon TG, Lee SJ, Yum KW, Kim HJ. 2005. Bupivacaine induces apoptosis via ROS in the Schwann cell line. J Dent Res 84:852-857.
30. Perez-Castro R, Patel S, Garavito-Aguilar ZV, Rosenberg A, Recio-Pinto E, Zhang J, Blanck TJ, Xu F. 2009. Cytotoxicity of local anesthetics in human neuronal cells. Anesth Analg 108:997-1007.
31. Riezzo I, Cerretani D, Fiore C, Bello S, Centini F, D'Errico S, Fiaschi AI, Giorgi G, Neri M, Pomara C, Turillazzi E, Fineschi V. 2010. Enzymatic-nonenzymatic cellular antioxidant defense systems response and immunohistochemical detection of MDMA, VMAT2, HSP70, and apoptosis as biomarkers for MDMA (ecstasy) neurotoxicity. J Neurosci Res 88:905-916.
32. Russell JW, Sullivan KA, Windebank AJ, Herrmann DN, Feldman EL. 1999. Neurons undergo apoptosis in animal and cell culture models of diabetes. Neurobiol Dis 6:347-363.
33. T method. Nat Protoc 3:1101-1108.
34. Schroder M, Kaufman RJ. 2005. The mammalian unfolded protein response. Annu Rev Biochem 74:739-789.
35. Takada A, Miki T, Kuno A, Kouzu H, Sunaga D, Itoh T, Tanno M, Yano T, Sato T, Ishikawa S, Miura T. 2012. Role of ER stress in ventricular contractile dysfunction in type 2 diabetes. PLoS One 7:e39893.
36. Takahashi S, Izawa Y, Suzuki N. 2012. Astroglial pentose phosphate pathway rates in response to high-glucose environments. ASN Neuro 4(2).
37. Tan Z, Dohi S, Chen J, Banno Y, Nozawa Y. 2002. Involvement of the mitogen-activated protein kinase family in tetracaine-induced PC12 cell death. Anesthesiology 96:1191-1201.
38. Ullman E, Fan Y, Stawowczyk M, Chen HM, Yue Z, Zong WX. 2008. Autophagy promotes necrosis in apoptosis-deficient cells in response to ER stress. Cell Death Differ 15:422-425.
39. Vincent AM, Brownlee M, Russell JW. 2002. Oxidative stress and programmed cell death in diabetic neuropathy. Ann N Y Acad Sci 959:368-383.
40. Vincent AM, Russell JW, Low P, Feldman EL. 2004. Oxidative stress in the pathogenesis of diabetic neuropathy. Endocr Rev 25:612-628.
41. Waterhouse NJ, Sedelies KA, Sutton VR, Pinkoski MJ, Thia KY, Johnstone R, Bird PI, Green DR, Trapani JA. 2006. Functional dissociation of DeltaPsim and cytochrome c release defines the contribution of mitochondria upstream of caspase activation during granzyme B-induced apoptosis. Cell Death Differ 13:607-618.
42. Werdehausen R, Fazeli S, Braun S, Hermanns H, Essmann F, Hollmann MW, Bauer I, Stevens MF. 2009. Apoptosis induction by different local anaesthetics in a neuroblastoma cell line. Br J Anaesth 103:711-718.
43. Xu DW, Shi L, Jia XG, Qian XY, Tang LL, Zhang YH, Wang Y, Wang WT. 2010. [Involvement of metallothionein in the protection of lung ischemic preconditioning]. Sheng Li Xue Bao 62:465-468.
44. Young TA, Cunningham CC, Bailey SM. 2002. Reactive oxygen species production by the mitochondrial respiratory chain in isolated rat hepatocytes and liver mitochondria: studies using myxothiazol. Arch Biochem Biophys 405:65-72.
45. Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G. 1995. Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 182:367-377.
46. Zeng YM, Cai KJ, Chen XY, Wu MX, Lin X. 2009. Effect of chronic intermittent hypoxia on the expression of Nip3, cell apoptosis, beta-amyloid protein deposit in mice brain cortex. Chin Med J (Engl) 122:68-73.
47. Zhang S, Fu J, Zhou Z. 2004. In vitro effect of manganese chloride exposure on reactive oxygen species generation and respiratory chain complexes activities of mitochondria isolated from rat brain. Toxicol In Vitro 18:71-77.
48. Zoratti M, Szabo I, De Marchi U. 2005. Mitochondrial permeability transitions: how many doors to the house? Biochim Biophys Acta 1706:40-52.
49. Zorov DB, Filburn CR, Klotz LO, Zweier JL, Sollott SJ. 2000. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med 192:1001-1014.