Dimethyl sulfoxide damages mitochondrial integrity and membrane potential in cultured astrocytes

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Yuan, Chan ^a   Gao, Junying ^a   Guo, Jichao ^a   Bai, Lei ^a   Marshall, Charles ^b   Cai, Zhiyou ^c   Wang, Linmei ^a   Xiao, Ming ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF KENTUCKY   (United States)

^c ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE 3; CYTOCHROME C; DIMETHYL SULFOXIDE; EXCITATORY AMINO ACID TRANSPORTER; REACTIVE OXYGEN METABOLITE; VESICULAR GLUTAMATE TRANSPORTER 1; EXCITATORY AMINO ACID TRANSPORTER 2;

ADULT; ANIMAL CELL; APOPTOSIS; ARTICLE; ASTROCYTE; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MITOCHONDRION SWELLING; MOUSE; NEUROTOXICITY; NONHUMAN; PROTEIN EXPRESSION; ANIMAL; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; MEMBRANE POTENTIAL; METABOLISM;

ANIMALS; APOPTOSIS; ASTROCYTES; CASPASE 3; CELL SURVIVAL; CELLS, CULTURED; CYTOCHROMES C; DIMETHYL SULFOXIDE; EXCITATORY AMINO ACID TRANSPORTER 2; MEMBRANE POTENTIALS; MICE; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 84907215674     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107447     Document Type: Article

References (52)

1. Santos NC, Figueira-Coelho J, Martins-Silva J, Saldanha C (2003) Multidisciplinary utilization of dimethyl sulfoxide: pharmacological, cellular, and molecular aspects. Biochem Pharmacol 65: 1035-1041.
2. Balakin KV, Savchuk NP, Tetko IV (2006) In silico approaches to prediction of aqueous and DMSO solubility of drug-like compounds: trends, problems and solutions. Curr Med Chem 13: 223-241.
3. Jacob SW, de la Torre JC (2009) Pharmacology of dimethyl sulfoxide in cardiac and CNS damage. Pharmacol Rep 61: 225-235.
4. Cavaletti G, Oggioni N, Sala F, Pezzoni G, Cavalletti E, et al. (2000) Effect on the peripheral nervous system of systemically administered dimethylsulfoxide in the rat: a neurophysiological and pathological study. Toxicol Lett 118, 103-107.
5. Authier N, Dupuis E, Kwasiborski A, Eschalier A, Coudoré F (2002) Behavioural assessment of dimethylsulfoxide neurotoxicity in rats. Toxico Lett 132: 117-121.
6. Fossum EN, Lisowski MJ, Macey TA, Ingram SL, Morgan MM (2008) Microinjection of the vehicle dimethyl sulfoxide (DMSO) into the periaqueductal gray modulates morphine antinociception. Brain Res 1204: 53-58.
7. Turan NN, Akar F, Budak B, Seren M, Parlar AI, et al. (2008) How DMSO, a widely used solvent, affects spinal cord injury. Ann Vasc Surg 22: 98-105.
8. Budinich CS, Tucker LB, Lowe D, Rosenberger JG, McCabe JT (2013) Short and long-term motor and behavioral effects of diazoxide and dimethyl sulfoxide administration in the mouse after traumatic brain injury. Pharmacol Biochem Behav 108: 66-73.
9. Shimizu S, Simon RP, Graham SH (1997) Dimethylsulfoxide (DMSO) treatment reduces infarction volume after permanent focal cerebral ischemia in rats. Neurosci Lett 239: 125-127.
10. Phillis JW, Estevez AY, O'Regan MH (1998) Protective effects of the free radical scavengers, dimethyl sulfoxide and ethanol, in cerebral ischemia in gerbils. Neurosci Lett 244: 109-111.
11. Di Giorgio AM, Hou Y, Zhao X, Zhang B, Lyeth BG, et al. (2008) Dimethyl sulfoxide provides neuroprotection in a traumatic brain injury model. Restor Neurol Neurosci 26: 501-507.
12. Hanslick JL, Lau K, Noguchi KK, Olney JW, Zorumski CF, et al. (2009) Dimethyl sulfoxide (DMSO) produces widespread apoptosis in the developing central nervous system. Neurobiol Dis 34: 1-10.
13. Julien C, Marcouiller F, Bretteville A, El Khoury NB, Baillargeon J, et al. (2012) Dimethyl sulfoxide induces both direct and indirect Tau hyperphosphorylation. PLoS ONE 7:e40020.
14. Windrum P, Morris TC (2003) Severe neurotoxicity because of dimethyl sulphoxide following peripheral blood stem cell transplantation. Bone Marrow Transplant 31: 315.
15. Bauwens D, Hantson P, Laterre PF, Michaux L, Latinne D, et al. (2005) Recurrent seizure and sustained encephalopathy associated with dimethylsulfoxide-preserved stem cell infusion. Leuk Lymphoma 46: 1671-1674.
16. Mueller LP, Theurich S, Christopeit M, Grothe W, Muetherig A, et al. (2007) Neurotoxicity upon infusion of dimethylsulfoxide-cryopreserved peripheral blood stem cells in patients with and without pre-existing cerebral disease. Eur J Haematol 78: 527-531.
17. Júnior AM, Arrais CA, Saboya R, Velasques RD, Junqueira PL, et al. (2008) Neurotoxicity associated with dimethylsulfoxide-preserved hematopoietic progenitor cell infusion. Bone Marrow Transplant 41: 95-96.
18. Abdelkefi A, Lakhal A, Moojat N, Hamed LB, Fekih J, et al. (2009) Severe neurotoxicity associated with dimethyl sulphoxide following PBSCT. Bone Marrow Transplant 44: 323-324.
19. Dhodapkar M, Goldberg SL, Tefferi A, Gertz MA (1994) Reversible encephalopathy after cryopreserved peripheral blood stem cell infusion. Am J Hematol 45: 187-188.
20. Higman MA, Port JD, Bezuchamp NJ Jr, Chen AR (2000) Reversible leukoencephalopathy associated with re-infusion of DMSO preserved stem cells. Bone Marrow Transplant 26: 797-800.
21. Marcacci G, Corazzelli G, Becchimanzi C, Arcamone M, Capobianco G, et al. (2009) DMSO-associated encephalopathy during autologous peripheral stem cell infusion: a predisposing role of preconditioning exposure to CNS-penetrating agents? Bone Marrow Transplant 44: 133-135.
22. Otrock ZK, Beydoun A, Barada WM, Masroujeh R, Hourani R, et al. (2008) Transient global amnesia associated with the infusion of DMSO-cryopreserved autologous peripheral blood stem cells. Haematologica 93: e36-37.
23. Allen NJ, Barres BA (2009) Neuroscience: Glia - more than just brain glue. Nature 457: 675-677.
24. Volterra A, Meldolesi J (2005) Astrocytes, from brain glue to communication elements: the revolution continues. Nat Rev Neurosci 6: 626-640.
25. Seifert G, Schilling K, Steinhäuser C (2006) Astrocyte dysfunction in neurological disorders: a molecular perspective. Nat Rev Neurosci 7: 194-206.
26. Notman R, Noro M, O'Malley B, Anwar J (2006) Molecular basis for dimethylsulfoxide (DMSO) action on lipid membranes. J Am Chem Soc 128: 13982-13983.
27. Gurtovenko AA, Anwar J (2007) Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide. J Phys Chem B 111: 10453-10460.
28. Sesso A, Belizário JE, Marques MM, Higuchi ML, Schumacher RI, et al. (2012) Mitochondrial swelling and incipient outer membrane rupture in preapoptotic and apoptotic cells. Anat Rec (Hoboken) 295: 1647-1659.
29. Gogvadze V, Orrenius S (2006)Mitochondrial regulation of apoptotic cell death. Chem Biol Interact 163: 4-14.
30. Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, et al. (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13: 1423-1433.
31. Murphy MP (2009) How mitochondria produce reactive oxygen species. Biochem J 417: 1-13.
32. Suski JM, Lebiedzinska M, Bonora M, Pinton P, Duszynski J, et al. (2012) Relation between mitochondrial membrane potential and ROS formation. Methods Mol Biol 810: 183-205.
33. Chandra J, Samali A, Orrenius S (2000) Triggering and modulation of apoptosis by oxidative stress. Free Radic Biol Med 29: 323-333.
34. Ott M, Robertson JD, Gogvadze V, Zhivotovsky B, Orrenius S (2002) Cytochrome c release from mitochondria proceeds by a two-step process. Proc Natl Acad Sci USA 99: 1259-1263.
35. Gogvadze V, Orrenius S, Zhivotovsky B (2006) Multiple pathways of cytochrome c release from mitochondria in apoptosis. Biochim Biophys Acta 57: 639-647.
36. Tsujimoto Y, Shimizu S (2007) Role of the mitochondrial membrane permeability transition in cell death. Apoptosis 12: 835-840.
37. Trotti D, Danbolt NC, Volterra A (1998) Glutamate transporters are oxidantvulnerable: a molecular link between oxidative and excitotoxic neurodegeneration? Trends Pharmacol Sci 19: 328-334.
38. Lu C, Mattson MP (2001) Dimethyl sulfoxide suppresses NMDA-and AMPAinduced ion currents and calcium influx and protects against excitotoxic death in hippocampal neurons. Exp Neurol 170: 180-185.
39. Yu ZW, Quinn PJ (1998) Solvation effects of dimethyl sulphoxide on the structure of phospholipid bilayers. Biophys Chem 70: 35-39.
40. Capriotti K, Capriotti JA (2012) Dimethyl sulfoxide: history, chemistry, and clinical utility in dermatology. J Clin Aesthet Dermatol 5: 24-26.
41. Borutaite V (2010) Mitochondria as decision-makers in cell death. Environ Mol Mutagen 51: 406-416.
42. Tapia R (1996) Release and uptake of glutamate as related to excitotoxicity. Rev Bras Biol 56: 165-174.
43. An SJ, Kang TC, Park SK, Hwang IK, Cho SS, et al. (2002) Oxidative DNA damage and alteration of glutamate transporter expressions in the hippocampal Ca1 area immediately after ischemic insult. Mol Cells 13: 476-480.
44. Zhao B, Chen Y, Sun X, Zhou M, Ding J, et al. (2012) Phenolic alkaloids from Menispermum dauricum rhizome protect against brain ischemia injury via regulation of GLT-1, EAAC1 and ROS generation. Molecules 17: 2725-2737.
45. Rao VL, Başkaya MK, Doʇan A, Rothstein JD, Dempsey RJ (1998) Traumatic brain injury down-regulates glial glutamate transporter (GLT-1 and GLAST) proteins in rat brain. J Neurochem 70: 2020-2027.
46. Gorter JA, Van Vliet EA, Proper EA, De Graan PN, Ghijsen WE, et al. (2002) Glutamate transporters alterations in the reorganizing dentate gyrus are associated with progressive seizure activity in chronic epileptic rats. J Comp Neurol 442: 365-377.
47. Sheldon AL, Robinson MB (2007) The role of glutamate transporters in neurodegenerative diseases and potential opportunities for intervention. Neurochem Int 51: 333-355.
48. Kim K, Lee SG, Kegelman TP, Su ZZ, Das SK, et al. (2011) Role of excitatory amino acid transporter-2 (EAAT2) and glutamate in neurodegeneration: opportunities for developing novel therapeutics. J Cell Physiol 226: 2484-2493.
49. Kovács Z, Czurkó A, Kékesi KA, Juhász G (2011) The effect of intraperitoneally administered dimethyl sulfoxide on absence-like epileptic activity of freely moving WAG/Rij rats. J. Neurosci. Methods 197: 133-136.
50. Zeng XN, Sun XL, Gao L, Fan Y, Ding JH, et al. (2007) Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol. Cell. Neurosci. 34, 34-39.
51. Chazotte B (2011) Labeling mitochondria with TMRM or TMRE. Cold Spring Harb Protoc 2011: 895-897.
52. Eruslanov E, Kusmartsev S (2010) Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol Biol 594: 57-72.