Hypoxic-ischemic injury in the developing brain: The role of reactive oxygen species originating in mitochondria

Neurology Research International

Volumn 2012, Issue , 2012, Pages

  Ten, Vadim S ^a,b,c   Starkov, Anatoly ^b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c NEW YORK PRESBYTERIAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84863842930     PISSN: 20901852     EISSN: 20901860     Source Type: Journal    
DOI: 10.1155/2012/542976     Document Type: Review

References (91)

1. CDC Morbidity and Mortality Weekly Report. 53, 57-59, 2004
2. Ferriero D. M., Neonatal brain injury. The New England Journal of Medicine 2004 351 1985 1995
3. Niermeyer S., Kattwinkel J., Van Reempts P., Nadkarni V., Phillips B., Zideman D., Azzopardi D., Berg R., Boyle D., Boyle R., Burchfield D., Carlo W., Chameides L., Denson S., Fallat M., Gerardi M., Gunn A., Hazinski M. F., Keenan W., Knaebel S., Milner A., Perlman J., Saugstad O. D., Schleien C., Solimano A., Speer M., Toce S., Wiswell T., Zaritsky A., International guidelines for neonatal resuscitation: an excerpt from the guidelines 2000 for cardiopulmonary resuscitation and emergency cardiovascular care: international consensus on science. Contributors and reviewers for the neonatal resuscitation guidelines. Pediatrics 2000 106 3 E29 2-s2.0-0034266005
4. Saugstad O. D., Rootwelt T., Aalen O., Resuscitation of asphyxiated newborn infants with room air or oxygen: an international controlled trial: the Resair 2 study. Pediatrics 1998 102 1, article e1 2-s2.0-0032111587
5. Tan A., Schulze A., O'Donnell C. P., Davis P. G., Air versus oxygen for resuscitation of infants at birth. Cochrane Database of Systematic Reviews 2005 3 CD002273 2-s2.0-16544366306
6. Vento M., Saugstad O. D., Oxygen supplementation in the delivery room: updated information. Journal of Pediatrics 2011 158 supplement 2 e5 e7
7. Vento M., Asensi M., Sastre J., Lloret A., García-Sala F., Via J., Oxidative stress in asphyxiated term infants resuscitated with 100 oxygen. Journal of Pediatrics 2003 142 3 240 246 2-s2.0-0037342239 10.1067/mpd.2003.91 (Pubitemid 36338004)
8. Koch J. D., Miles D. K., Gilley J. A., Yang C. P., Kernie S. G., Brief exposure to hyperoxia depletes the glial progenitor pool and impairs functional recovery after hypoxic-ischemic brain injury. Journal of Cerebral Blood Flow and Metabolism 2008 28 7 1294 1306 2-s2.0-46049091773 10.1038/jcbfm.2008.15 (Pubitemid 351896643)
9. Haase E., Bigam D. L., Nakonechny Q. B., Jewell L. D., Korbutt G., Cheung P. Y., Resuscitation with 100 oxygen causes intestinal glutathione oxidation and reoxygenation injury in asphyxiated newborn piglets. Annals of Surgery 2004 240 2 364 373 2-s2.0-3242663422 10.1097/01.sla.0000133348.58450.e4 (Pubitemid 38963030)
10. 2 increases cerebral injury in hypoxemic piglets. Pediatric Research 2004 56 5 783 790 2-s2.0-6344258467 10.1203/01.PDR.0000141988.89820.E3 (Pubitemid 39403406)
11. Van Meter K., Sheps S., Kriedt F., Moises J., Barratt D., Murphy-Lavoie H., Harch P. G., Bazan N., Hyperbaric oxygen improves rate of return of spontaneous circulation after prolonged normothermic porcine cardiopulmonary arrest. Resuscitation 2008 78 2 200 214 2-s2.0-46649087948 10.1016/j. resuscitation.2008.02.026
12. Linner R., Werner O., Perez-De-Sa V., Cunha-Goncalves D., Circulatory recovery is as fast with air ventilation as with 100 oxygen after asphyxia-induced cardiac arrest in piglets. Pediatric Research 2009 66 4 391 394 2-s2.0-70350442811 10.1203/PDR.0b013e3181b3b110
13. Solevåg A. L., Dannevig I., Nakstad B., Saugstad O. D., Resuscitation of severely asphyctic newborn pigs with cardiac arrest by using 21 or 100 oxygen. Neonatology 2010 98 1 64 72 2-s2.0-73649140007 10.1159/000275560
14. Matsiukevich D., Randis T. M., Utkina-Sosunova I., Polin R. A., Ten V. S., The state of systemic circulation, collapsed or preserved defines the need for hyperoxic or normoxic resuscitation in neonatal mice with hypoxia-ischemia. Resuscitation 2010 81 2 224 229 2-s2.0-74249105164 10.1016/j.resuscitation.2009. 11.024
15. Ditelberg J. S., Sheldon R. A., Epstein C. J., Ferriero D. M., Brain injury after perinatal hypoxia-ischemia is exacerbated in copper/zinc superoxide dismutase transgenic mice. Pediatric Research 1996 39 2 204 208 2-s2.0-0030045877 (Pubitemid 26039540)
16. Sheldon R. A., Christen S., Ferriero D. M., Genetic and pharmacologic manipulation of oxidative stress after neonatal hypoxia-ischemia. International Journal of Developmental Neuroscience 2008 26 1 87 92 2-s2.0-38849175410 10.1016/j.ijdevneu.2007.08.010 (Pubitemid 351192264)
17. Abramov A. Y., Scorziello A., Duchen M. R., Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. Journal of Neuroscience 2007 27 5 1129 1138 2-s2.0-33846818524 10.1523/JNEUROSCI.4468-06.2007 (Pubitemid 46203321)
18. Saugstad O. D., Gluck L., Plasma hypoxanthine levels in newborn infants: a specific indicator of hypoxia. Journal of Perinatal Medicine 1982 10 6 266 272 (Pubitemid 13177676)
19. Saugstad O. D., Hypoxanthine as an indicator of hypoxia: its role in health and disease through free radical production. Pediatric Research 1988 23 2 143 150 (Pubitemid 18095054)
20. Feng Y., Shi W., Huang M., LeBlanc M. H., Oxypurinol administration fails to prevent hypoxic-ischemic brain injury in neonatal rats. Brain Research Bulletin 2003 59 6 453 457 2-s2.0-0037441740 10.1016/S0361-9230(02)00963-2 (Pubitemid 36173600)
21. Chaudhari T., McGuire W., Allopurinol for preventing mortality and morbidity in newborn infants with suspected hypoxic-ischaemic encephalopathy. Cochrane Database of Systematic Reviews 2008 2 2-s2.0-44949172545 10.1002/14651858.CD006817.pub2 CD006817 (Pubitemid 351807226)
22. Doverhag C., Keller M., Karlsson A., Hedtjarn M., Nilsson U., Kapeller E., Sarkozy G., Klimaschewski L., Humpel C., Hagberg H., Simbruner G., Gressens P., Savman K., Pharmacological and genetic inhibition of NADPH oxidase does not reduce brain damage in different models of perinatal brain injury in newborn mice. Neurobiology of Disease 2008 31 1 133 144 2-s2.0-45149100248 10.1016/j.nbd.2008.04.003 (Pubitemid 351833142)
23. Loor G., Kondapalli J., Iwase H., Chandel N. S., Waypa G. B., Guzy R. D., Vanden Hoek T. L., Schumacker P. T., Mitochondrial oxidant stress triggers cell death in simulated ischemia-reperfusion. Biochimica et Biophysica Acta 2011 1813 7 1382 1394 2-s2.0-78650958994 10.1016/j.bbamcr.2010.12.008
24. Starkov A. A., Chinopoulos C., Fiskum G., Mitochondrial calcium and oxidative stress as mediators of ischemic brain injury. Cell Calcium 2004 36 3-4 257 264 2-s2.0-3342910554 10.1016/j.ceca.2004.02.012 (Pubitemid 38992351)
25. Ambrosio G., Zweier J. L., Duilio C., Kuppusamy P., Santoro G., Elia P. P., Tritto I., Cirillo P., Condorelli M., Chiariello M., Flaherty J. T., Evidence that mitochondrial respiration is a source of potentially toxic oxygen free radicals in intact rabbit hearts subjected to ischemia and reflow. Journal of Biological Chemistry 1993 268 25 18532 18541 2-s2.0-0027181186 (Pubitemid 23273786)
26. Chen Q., Moghaddas S., Hoppel C. L., Lesnefsky E. J., Ischemic defects in the electron transport chain increase the production of reactive oxygen species from isolated rat heart mitochondria. American Journal of PhysiologyCell Physiology 2008 294 2 C460 C466 2-s2.0-39549102405 10.1152/ajpcell.00211.2007 (Pubitemid 351276913)
27. Piantadosi C. A., Zhang J., Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke 1996 27 2 327 332 2-s2.0-0030060186 (Pubitemid 26045253)
28. Perrelli M. G., Pagliaro P., Penna C., Ischemia/reperfusion injury and cardioprotective mechanisms: role of mitochondria and reactive oxygen species. World Journal of Cardiology 2011 3 6 186 200
29. Simerabet M., Robin E., Aristi I., Adamczyk S., Tavernier B., Vallet B., Bordet R., Lebuffe G., Preconditioning by an in situ administration of hydrogen peroxide: involvement of reactive oxygen species and mitochondrial ATP-dependent potassium channel in a cerebral ischemia-reperfusion model. Brain Research 2008 1240 177 184 2-s2.0-54549085364 10.1016/j.brainres.2008.08.070
30. Cohen M. V., Yang X. M., Downey J. M., Acidosis, oxygen, and interference with mitochondrial permeability transition pore formation in the early minutes of reperfusion are critical to postconditioning's success. Basic Research in Cardiology 2008 103 5 464 471 2-s2.0-50249090955 10.1007/s00395-008-0737-9
31. Ten V. S., Yao J., Ratner V., Sosunov S., Fraser D. A., Botto M., Sivasankar B., Morgan B. P., Silverstein S., Stark R., Polin R., Vannucci S. J., Pinsky D., Starkov A. A., Complement component C1q mediates mitochondria-driven oxidative stress in neonatal hypoxic-ischemic brain injury. Journal of Neuroscience 2010 30 6 2077 2087 2-s2.0-76649108526 10.1523/JNEUROSCI.5249-09. 2010
32. Chen Q., Vazquez E. J., Moghaddas S., Hoppel C. L., Lesnefsky E. J., Production of reactive oxygen species by mitochondria: central role of complex III. Journal of Biological Chemistry 2003 278 38 36027 36031 2-s2.0-0141815741 10.1074/jbc.M304854200 (Pubitemid 37139922)
33. Skulachev M. V., Antonenko Y. N., Anisimov V. N., Mitochondrial-targeted plastoquinone derivatives. Effect on senescence and acute age-related pathologies. Current Drug Targets 2011 12 6 800 826
34. Szeto H. H., Liu S., Soong Y., Mitochondria-targeted peptide accelerates ATP recovery and reduces ischemic kidney injury. Journal of the American Society of Nephrology 2011 22 6 1041 1052
35. Rocha M., Hernandez-Mijares A., Garcia-Malpartida K., Bauls C., Bellod L., Victor V. M., Mitochondria-targeted antioxidant peptides. Current Pharmaceutical Design 2010 16 28 3124 3131 2-s2.0-78649897034 10.2174/138161210793292519
36. Choi K., Kim J., Kim G. W., Choi C., Oxidative stress-induced necrotic cell death via mitochondira-dependent burst of reactive oxygen species. Current Neurovascular Research 2009 6 4 213 222 2-s2.0-70350325187 10.2174/ 156720209789630375
37. Lesnefsky E. J., Chen Q., Moghaddas S., Hassan M. O., Tandler B., Hoppel C. L., Blockade of electron transport during ischemia protects cardiac mitochondria. Journal of Biological Chemistry 2004 279 46 47961 47967 2-s2.0-9144227549 10.1074/jbc.M409720200 (Pubitemid 39540947)
38. Tompkins A. J., Burwell L. S., Digerness S. B., Zaragoza C., Holman W. L., Brookes P. S., Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochimica et Biophysica Acta 2006 1762 2 223 231 2-s2.0-29344464774 10.1016/j.bbadis.2005.10.001 (Pubitemid 43006028)
39. Starkov A. A., The role of mitochondria in reactive oxygen species metabolism and signaling. Annals of the New York Academy of Sciences 2008 1147 37 52 2-s2.0-57649233079 10.1196/annals.1427.015
40. Andreyev A. Y., Kushnareva Y. E., Starkov A. A., Mitochondrial metabolism of reactive oxygen species. Biochemistry 2005 70 2 200 214 2-s2.0-17144422877 10.1007/s10541-005-0102-7 (Pubitemid 40512329)
41. Starkov A. A., Fiskum G., Chinopoulos C., Lorenzo B. J., Browne S. E., Patel M. S., Beal M. F., Mitochondrial α -ketoglutarate dehydrogenase complex generates reactive oxygen species. Journal of Neuroscience 2004 24 36 7779 7788 2-s2.0-4544359913 10.1523/JNEUROSCI.1899-04.2004 (Pubitemid 39215681)
42. Tretter L., Adam-Vizi V., Generation of reactive oxygen species in the reaction catalyzed by α -ketoglutarate dehydrogenase. Journal of Neuroscience 2004 24 36 7771 7778 2-s2.0-4544226082 10.1523/JNEUROSCI.1842-04. 2004 (Pubitemid 39215680)
43. Tahara E. B., Navarete F. D. T., Kowaltowski A. J., Tissue-, substrate-, and site-specific characteristics of mitochondrial reactive oxygen species generation. Free Radical Biology and Medicine 2009 46 9 1283 1297 2-s2.0-63349087445 10.1016/j.freeradbiomed.2009.02.008
44. Almeida A., Allen K. L., Bates T. E., Clark J. B., Effect of reperfusion following cerebral ischaemia on the activity of the mitochondrial respiratory chain in the gerbil brain. Journal of Neurochemistry 1995 65 4 1698 1703 2-s2.0-0029097980
45. Allen K. L., Almeida A., Bates T. E., Clark J. B., Changes of respiratory chain activity in mitochondrial and synaptosomal fractions isolated from the gerbil brain after graded ischaemia. Journal of Neurochemistry 1995 64 5 2222 2229 2-s2.0-0028961896
46. Gilland E., Puka-Sundvall M., Hillered L., Hagberg H., Mitochondrial function and energy metabolism after hypoxia-ischemia in the immature rat brain: involvement of NMDA-receptors. Journal of Cerebral Blood Flow and Metabolism 1998 18 3 297 304 2-s2.0-0031916208 (Pubitemid 28103637)
47. Sims N. R., Selective impairment of respiration in mitochondria isolated from brain subregions following transient forebrain ischemia in the rat. Journal of Neurochemistry 1991 56 6 1836 1844 2-s2.0-0026010158 10.1111/j.1471-4159. 1991.tb03438.x
48. Folbergrova J., Ljunggren B., Norberg K., Siesjo B. K., Influence of complete ischemia on glycolytic metabolites, citric acid cycle intermediates, and associated amino acids in the rat cerebral cortex. Brain Research 1974 80 2 265 279 2-s2.0-0016302480 10.1016/0006-8993(74)90690-8
49. Benzi G., Arrigoni E., Marzatico F., Villa R. F., Influence of some biological pyrimidines on the succinate cycle during and after cerebral ischemia. Biochemical Pharmacology 1979 28 17 2545 2550 2-s2.0-0018664824 10.1016/0006-2952(79)90024-8 (Pubitemid 10229266)
50. Khazanov V. A., Poborsky A. N., Kondrashova M. N., Air saturation of the medium reduces the rate of phosphorylating oxidation of succinate in isolated mitochondria. FEBS Letters 1992 314 3 264 266 2-s2.0-0026619302 10.1016/0014-5793(92)81485-5 (Pubitemid 23005669)
51. Poborskii A. N., Effect of research conditions on succinate oxidation in brain mitochondria in circulatory hypoxia. Patologicheskaia Fiziologiia i Eksperimental'naia Terapiia's 1997 1 10 12 2-s2.0-0030632660
52. König T., Nicholls D. G., Garland P. B., The inhibition of pyruvate and Ls(+)-isocitrate oxidation by succinate oxidation in rat liver mitochondria. Biochemical Journal 1969 114 3 589 596 2-s2.0-0014572763
53. Pisarenko O., Studneva I., Khlopkov V., Metabolism of the tricarboxylic acid cycle intermediates and related amino acids in ischemic guinea pig heart. Biomedica Biochimica Acta 1987 46 8-9 S568 S571 2-s2.0-17944397598
54. Kato K., Matsubara T., Sakamoto N., Correlation between myocardial blood flow and tissue succinate during acute ischemia. Nagoya Journal of Medical Science 1994 57 14 43 50 2-s2.0-0028403569
55. Niatsetskaya Z. V., Sosunov S. A., Matsiukevich D., Utkina-Sosunova I. V., Ratner V. I., Starkov A. A., Ten V. S., The oxygen free radicals originating from mitochondrial complex I contribute to oxidative brain injury following hypoxia-ischemia in neonatal mice. Journal of Neuroscience 2012 32 9 3235 3244
56. Han F., Da T., Riobo N. A., Becker L. B., Early mitochondrial dysfunction in electron transfer activity and reactive oxygen species generation after cardiac arrest. Critical Care Medicine 2008 36 supplement 11 S447 S453 2-s2.0-77953397093
57. Guzy R. D., Mack M. M., Schumacker P. T., Mitochondrial complex III is required for hypoxia-induced ROS production and gene transcription in yeast. Antioxidants and Redox Signaling 2007 9 9 1317 1328 2-s2.0-34547911818 10.1089/ars.2007.1708 (Pubitemid 47255011)
58. Sipos I., Tretter L., Adam-Vizi V., The production of reactive oxygen species in intact isolated nerve terminals is independent of the mitochondrial membrane potential. Neurochemical Research 2003 28 10 1575 1581 2-s2.0-0141482026 10.1023/A:1025634728227 (Pubitemid 37193540)
59. McDonald J. W., Johnston M. V., Physiological and pathophysiological roles of excitatory amino acids during cental nervous system development. Brain Research Reviews 1990 15 1 41 70 2-s2.0-0025257513 10.1016/0165-0173(90)90011-C (Pubitemid 20158154)
60. Tahraoui S. L., Marret S., Bodénant C., Leroux P., Dommergues M. A., Evrard P., Gressens P., Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathology 2001 11 1 56 71 2-s2.0-0035198556
61. Starkov A. A., The molecular identity of the mitochondrial Ca2+ sequestration system: minireview. FEBS Journal 2010 277 18 3652 3663 2-s2.0-77956322223 10.1111/j.1742-4658.2010.07756.x
62. Matsumoto S., Friberg H., Ferrand-Drake M., Wieloch T., Blockade of the mitochondrial permeability transition pore diminishes infarct size in the rat after transient middle cerebral artery occlusion. Journal of Cerebral Blood Flow and Metabolism 1999 19 7 736 741 2-s2.0-0033495895 (Pubitemid 30159798)
63. Khaspekov L., Friberg H., Halestrap A., Viktorov I., Wieloch T., Cyclosporin A and its nonimmunosuppressive analogue N-Me-Val-4-cyclosporin A mitigate glucose/oxygen deprivation-induced damage to rat cultured hippocampal neurons. European Journal of Neuroscience 1999 11 9 3194 3198 2-s2.0-0032860116 10.1046/j.1460-9568.1999.00743.x (Pubitemid 29431654)
64. Leung A. W. C., Halestrap A. P., Recent progress in elucidating the molecular mechanism of the mitochondrial permeability transition pore. Biochimica et Biophysica Acta 2008 1777 7-8 946 952 2-s2.0-46349097952 10.1016/j.bbabio.2008.03.009
65. Di Lisa F., Kaludercic N., Carpi A., Menabò R., Giorgio M., Mitochondrial pathways for ROS formation and myocardial injury: the relevance of p66Shc and monoamine oxidase. Basic Research in Cardiology 2009 104 2 131 139 2-s2.0-62249115660 10.1007/s00395-009-0008-4
66. Lemasters J. J., Theruvath T. P., Zhong Z., Nieminen A. L., Mitochondrial calcium and the permeability transition in cell death. Biochimica et Biophysica Acta 2009 1787 11 1395 1401 2-s2.0-68649095201 10.1016/j.bbabio.2009.06.009
67. Basso E., Fante L., Fowlkes J., Petronilli V., Forte M. A., Bernardi P., Properties of the permeability transition pore in mitochondria devoid of cyclophilin D. Journal of Biological Chemistry 2005 280 19 18558 18561 2-s2.0-21244446551 10.1074/jbc.C500089200 (Pubitemid 41379552)
68. Kim J. S., Jin Y., Lemasters J. J., Reactive oxygen species, but not Ca2+ overloading, trigger pH- and mitochondrial permeability transition-dependent death of adult rat myocytes after ischemia-reperfusion. American Journal of PhysiologyHeart and Circulatory Physiology 2006 290 5 H2024 H2034 2-s2.0-33646421637 10.1152/ajpheart.00683.2005
69. Liang H. L., Sedlic F., Bosnjak Z., Nilakantan V., SOD1 and MitoTEMPO partially prevent mitochondrial permeability transition pore opening, necrosis, and mitochondrial apoptosis after ATP depletion recovery. Free Radical Biology and Medicine 2010 49 10 1550 1560 2-s2.0-77957751549 10.1016/j.freeradbiomed. 2010.08.018
70. Puka-Sundvall M., Wallin C., Gilland E., Hallin U., Wang X., Sandberg M., Karlsson J. O., Blomgren K., Hagberg H., Impairment of mitochondrial respiration after cerebral hypoxia-ischemia in immature rats: relationship to activation of caspase-3 and neuronal injury. Developmental Brain Research 2000 125 1-2 43 50 2-s2.0-0034731336 10.1016/S0165-3806(00)00111-5 (Pubitemid 32057180)
71. Caspersen C. S., Sosunov A., Utkina-Sosunova I., Ratner V. I., Starkov A. A., Ten V. S., An isolation method for assessment of brain mitochondria function in neonatal mice with hypoxic-ischemic brain injury. Developmental Neuroscience 2008 30 5 319 324 2-s2.0-52949153648 10.1159/000121416
72. Vinogradov A., Scarpa A., Chance B., Calcium and pyridine nucleotide interaction in mitochondrial membranes. Archives of Biochemistry and Biophysics 1972 152 2 646 654 2-s2.0-0015408790
73. Baines C. P., Kaiser R. A., Purcell N. H., Blair N. S., Osinska H., Hambleton M. A., Brunskill E. W., Sayen M. R., Gottlieb R. A., Dorn G. W., Bobbins J., Molkentin J. D., Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005 434 7033 658 662 2-s2.0-15844375853 10.1038/nature03434 (Pubitemid 40488559)
74. Nakagawa T., Shimizu S., Watanabe T., Yamaguchi O., Otsu K., Yamagata H., Inohara H., Kubo T., Tsujimoto Y., Cyclophilin D-dependent mitochondrial permeability transition regulates some necrotic but not apoptotic cell death. Nature 2005 434 7033 652 658 2-s2.0-15844407874 10.1038/nature03317 (Pubitemid 40488558)
75. Puka-Sundvall M., Gajkowska B., Cholewinski M., Blomgren K., Lazarewicz J. W., Hagberg H., Subcellular distribution of calcium and ultrastructural changes after cerebral hypoxia-ischemia in immature rats. Developmental Brain Research 2000 125 1-2 31 41 2-s2.0-0034731384 10.1016/S0165-3806(00)00110-3 (Pubitemid 32057179)
76. Wang X., Carlsson Y., Basso E., Zhu C., Rousset C. I., Rasola A., Johansson B. R., Blomgren K., Mallard C., Bernardi P., Forte M. A., Hagberg H., Developmental shift of cyclophilin D contribution to hypoxic-ischemic brain injury. Journal of Neuroscience 2009 29 8 2588 2596 2-s2.0-61449100405 10.1523/JNEUROSCI.5832-08.2009
77. Puka-Sundvall M., Gilland E., Hagberg H., Cerebral hypoxia-ischemia in immature rats: involvement of mitochondrial permeability transition? Developmental Neuroscience 2001 23 3 192 197 2-s2.0-0035742481 10.1159/000046142 (Pubitemid 34701671)
78. Hwang J. H., Lee J. H., Lee K. H., Bae E. J., Sung D. K., Chang Y. S., Park W. S., Cyclosporine A attenuates hypoxic-ischemic brain injury in newborn rats. Brain Research 2010 1359 208 215 2-s2.0-77957979880 10.1016/j.brainres. 2010.08.047
79. Leger P. L., De Paulis D., Branco S., Bonnin P., Couture-Lepetit E., Baud O., Renolleau S., Ovize M., Gharib A., Charriaut-Marlangue C., Evaluation of cyclosporine A in a stroke model in the immature rat brain. Experimental Neurology 2011 230 1 58 66 2-s2.0-77954324290 10.1016/j.expneurol.2010.06.009
80. Liu X. D., Pan G. Y., Xie L., Hou Y. Y., Lan W., Su Q., Liu G. Q., Cyclosporin A enhanced protection of nimodipine against brain damage induced by hypoxia-ischemia in mice and rats. Acta Pharmacologica Sinica 2002 23 3 225 229 2-s2.0-0036189023 (Pubitemid 34194388)
81. Marzo I., Brenner C., Zamzami N., Jürgensmeier J. M., Susin S. A., Vieira H. L. A., Prévost M. C., Xie Z., Matsuyama S., Reed J. C., Kroemer G., Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 1998 281 5385 2027 2031 2-s2.0-0032566649 10.1126/science.281.5385.2027 (Pubitemid 28475490)
82. Eskes R., Antonsson B., Osen-Sand A., Montessuit S., Richter C., Sadoul R., Mazzei G., Nichols A., Martinou J. C., Bax-induced cytochrome C release from mitochondria is independent of the permeability transition pore but highly dependent on Mg2+ ions. Journal of Cell Biology 1998 143 1 217 224 2-s2.0-0032487583 10.1083/jcb.143.1.217 (Pubitemid 28480530)
83. Korytowski W., Basova L. V., Pilat A., Kernstock R. M., Girotti A. W., Permeabilization of the mitochondrial outer membrane by Bax/truncated Bid (tBid) proteins as sensitized by cardiolipin hydroperoxide translocation: mechanistic implications for the intrinsic pathway of oxidative apoptosis. The Journal of Biological Chemistry 2011 286 30 26334 26343
84. Jacotot E., Costantini P., Laboureau E., Zamzami N., Susin S. A., Kroemer G., Mitochondrial membrane permeabilization during the apoptotic process. Annals of the New York Academy of Sciences 1999 887 18 30 2-s2.0-0033386851 (Pubitemid 30040216)
85. Hagberg H., Mallard C., Rousset Catherine C. I., Wang X., Apoptotic mechanisms in the immature brain: involvement of mitochondria. Journal of Child Neurology 2009 24 9 1141 1146 2-s2.0-70349315125 10.1177/0883073809338212
86. Wang X., Han W., Du X., Zhu C., Carlsson Y., Mallard C., Jacotot E., Hagberg H., Neuroprotective effect of Bax-inhibiting peptide on neonatal brain injury. Stroke 2010 41 9 2050 2055 2-s2.0-77956410991 10.1161/STROKEAHA.110. 589051
87. Pasdois P., Parker J. E., Griffiths E. J., Halestrap A. P., The role of oxidized cytochrome c in regulating mitochondrial reactive oxygen species production and its perturbation in ischaemia. Biochemical Journal 2011 436 2 493 505
88. Vela L., Contel M., Palomera L., Azaceta G., Marzo I., Iminophosphorane-organogold (III) complexes induce cell death through mitochondrial ROS production. Journal of Inorganic Biochemistry 2011 105 10 1306 1313
89. Hahm E. R., Moura M. B., Kelley E. E., Van Houten B., Shiva S., Singh S. V., Withaferin a-induced apoptosis in human breast cancer cells is mediated by reactive oxygen species. PLoS One 2011 6 8, article e23354
90. Ma Q., Fang H., Shang W., Superoxide flashes: early mitochondrial signals for oxidative stress-induced apoptosis. The Journal of Biological Chemistry 2011 286 31 27573 27581
91. Narita M., Shimizu S., Ito T., Chittenden T., Lutz R. J., Matsuda H., Tsujimoto Y., Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proceedings of the National Academy of Sciences of the United States of America 1998 95 25 14681 14686 2-s2.0-0032422488 10.1073/pnas.95.25.14681 (Pubitemid 29003690)