Sex differences in mitochondrial (dys)function: Implications for neuroprotection
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  • 作者：Tyler G. Demarest (1) (2)
    Margaret M. McCarthy (1) (3)

    1. Program in Neuroscience     ; University of Maryland School of Medicine ; Baltimore ; MD ; USA
    2. Department of Anesthesiology     ; University of Maryland School of Medicine ; Baltimore ; MD ; USA
    3. Department of Pharmacology     ; University of Maryland School of Medicine ; Baltimore ; MD ; USA
  • 关键词：Sex differences ; Mitochondria ; Metabolism ; Neuroprotection ; Excitotoxicity ; Mitophagy ; Oxidative stress ; Cell death
  • 刊名：Journal of Bioenergetics and Biomembranes
  • 出版年：2015
  • 出版时间：April 2015
  • 年：2015
  • 卷：47
  • 期：1-2
  • 页码：173-188
  • 全文大小：1,204 KB
  • 参考文献：1. Alano CC, Ying W, Swanson RA (2004) Poly(ADP-ribose) polymerase-1-mediated cell death in astrocytes requires NAD鈥?鈥塪epletion and mitochondrial permeability transition. J Biol Chem 279:18895鈥?8902
    2. Alano CC, Garnier P, Ying W, Higashi Y, Kauppinen TM, Swanson RA (2010) NAD鈥?鈥塪epletion is necessary and sufficient for poly(ADP-ribose) polymerase-1-mediated neuronal death. J Neurosci 30:2967鈥?978
    3. Ali SS, Xiong C, Lucero J, Behrens MM, Dugan LL, Quick KL (2006) Gender differences in free radical homeostasis during aging: shorter-lived female C57BL6 mice have increased oxidative stress. Aging Cell 5:565鈥?74
    4. Andrabi SA, Dawson TM, Dawson VL (2008) Mitochondrial and nuclear cross talk in cell death: parthanatos. Ann N Y Acad Sci 1147:233鈥?41
    5. Anne SR, Leak RK, Gao Y, Chen J (2013) The dynamics of the mitochondrial organelle as a potential therapeutic target. J Cereb Blood Flow Metab 33:22鈥?2
    6. Arieli Y, Gursahani H, Eaton MM, Hernandez LA, Schaefer S (2004) Gender modulation of Ca(2+) uptake in cardiac mitochondria. J Mol Cell Cardiol 37:507鈥?13
    7. Arnold S, Beyer C (2009) Neuroprotection by estrogen in the brain: the mitochondrial compartment as presumed therapeutic target. J Neurochem 110:1鈥?1
    8. Arnold S, de Araujo GW, Beyer C (2008) Gender-specific regulation of mitochondrial fusion and fission gene transcription and viability of cortical astrocytes by steroid hormones. J Mol Endocrinol 41:289鈥?00
    9. Au AK, Bayir H, Kochanek PM, Clark RS (2010) Evaluation of autophagy using mouse models of brain injury. Biochim Biophys Acta 1802:918鈥?23
    10. Baek SH, Bae ON, Kim EK, Yu SW (2013) Induction of mitochondrial dysfunction by poly(ADP-ribose) polymer: implication for neuronal cell death. Mol Cell 36:258鈥?66
    11. Ballard JW, Melvin RG, Miller JT, Katewa SD (2007) Sex differences in survival and mitochondrial bioenergetics during aging in Drosophila. Aging Cell 6:699鈥?08
    12. Bates TE, Loesch A, Burnstock G, Clark JB (1995) Immunocytochemical evidence for a mitochondrially located nitric oxide synthase in brain and liver. Biochem Biophys Res Commun 213:896鈥?00
    13. Bayir H, Kagan VE, Tyurina YY, Tyurin V, Ruppel RA, Adelson PD, Graham SH, Janesko K, Clark RS, Kochanek PM (2002) Assessment of antioxidant reserves and oxidative stress in cerebrospinal fluid after severe traumatic brain injury in infants and children. Pediatr Res 51:571鈥?78
    14. Bayir H, Marion DW, Puccio AM, Wisniewski SR, Janesko KL, Clark RS, Kochanek PM (2004) Marked gender effect on lipid peroxidation after severe traumatic brain injury in adult patients. J Neurotrauma 21:1鈥?
    15. Bayir H, Kagan VE, Clark RS, Janesko-Feldman K, Rafikov R, Huang Z, Zhang X, Vagni V, Billiar TR, Kochanek PM (2007) Neuronal NOS-mediated nitration and inactivation of manganese superoxide dismutase in brain after experimental and human brain injury. J Neurochem 101:168鈥?81
    16. Bender C, de OS, Bueno A, de OJ, Lorenzo A (2010) Comparative analyses of the neurodegeneration induced by the non-competitive NMDA-receptor-antagonist drug MK801 in mice and rats. Neurotoxicol Teratol 32:542鈥?50
    17. Borras C, Sastre J, Garcia-Sala D, Lloret A, Pallardo FV, Vina J (2003) Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 34:546鈥?52
    18. Brown GC (1995) Nitric oxide regulates mitochondrial respiration and cell functions by inhibiting cytochrome oxidase. FEBS Lett 369:136鈥?39
    19. Brown GC (2001) Regulation of mitochondrial respiration by nitric oxide inhibition of cytochrome c oxidase. Biochim Biophys Acta 1504:46鈥?7
    20. Brown GC (2007) Nitric oxide and mitochondria. Front Biosci 12:1024鈥?033
    21. Brown GC, Cooper CE (1994) Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase. FEBS Lett 356:295鈥?98
    22. Cao Y, Lv G, Wang YS, Fan ZK, Bi YL, Zhao L, Guo ZP (2013) Mitochondrial fusion and fission after spinal sacord injury in rats. Brain Res 1522:59鈥?6
    23. Chen Q, Harris C, Brown CS, Howe A, Surmeier DJ, Reiner A (1995) Glutamate-mediated excitotoxic death of cultured striatal neurons is mediated by non-NMDA receptors. Exp Neurol 136:212鈥?24
    24. Chen TY, Tsai KL, Lee TY, Chiueh CC, Lee WS, Hsu C (2010) Sex-specific role of thioredoxin in neuroprotection against iron-induced brain injury conferred by estradiol. Stroke 41:160鈥?65
    25. Chen CW, Chen TY, Tsai KL, Lin CL, Yokoyama KK, Lee WS, Chiueh CC, Hsu C (2012) Inhibition of autophagy as a therapeutic strategy of iron-induced brain injury after hemorrhage. Autophagy 8:1510鈥?520
    26. Chen C, Hu LX, Dong T, Wang GQ, Wang LH, Zhou XP, Jiang Y, Murao K, Lu SQ, Chen JW, Zhang GX (2013) Apoptosis and autophagy contribute to gender difference in cardiac ischemia-reperfusion induced injury in rats. Life Sci 93:265鈥?70
    27. Choi DW (1985) Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci Lett 58:293鈥?97
    28. Choi DW (1994) Calcium and excitotoxic neuronal injury. Ann N Y Acad Sci 747:162鈥?71
    29. Chu CT, Ji J, Dagda RK, Jiang JF, Tyurina YY, Kapralov AA, Tyurin VA, Yanamala N, Shrivastava IH, Mohammadyani D, Qiang Wang KZ, Zhu J, Klein-Seetharaman J, Balasubramanian K, Amoscato AA, Borisenko G, Huang Z, Gusdon AM, Cheikhi A, Steer EK, Wang R, Baty C, Watkins S, Bahar I, Bayir H, Kagan VE (2013) Cardiolipin externalization to the outer mitochondrial membrane acts as an elimination signal for mitophagy in neuronal cells. Nat Cell Biol 15:1197鈥?205
    30. Chu CT, Bayir H, Kagan VE (2014) LC3 binds externalized cardiolipin on injured mitochondria to signal mitophagy in neurons: implications for Parkinson disease. Autophagy 10:376鈥?78
    31. Clark RS, Kochanek PM, Watkins SC, Chen M, Dixon CE, Seidberg NA, Melick J, Loeffert JE, Nathaniel PD, Jin KL, Graham SH (2000) Caspase-3 mediated neuronal death after traumatic brain injury in rats. J Neurochem 74:740鈥?53
    32. Clark RS, Vagni VA, Nathaniel PD, Jenkins LW, Dixon CE, Szabo C (2007) Local administration of the poly(ADP-ribose) polymerase inhibitor INO-1001 prevents NAD鈥?鈥塪epletion and improves water maze performance after traumatic brain injury in mice. J Neurotrauma 24:1399鈥?405
    33. Clayton JA, Collins FS (2014) Policy: NIH to balance sex in cell and animal studies. Nature 509:282鈥?83
    34. Costa LG, de Laat R, Dao K, Pellacani C, Cole TB, Furlong CE (2013) Paraoxonase-2 (PON2) in brain and its potential role in neuroprotection. Neurotoxicology 43:3鈥?
    35. Demarest TG, Waddell J, Schuh RA, McKenna MC, Fiskum G (2013) Sexually dimorphic impairment of brain mitochondrial respiration following neonatal hypoxic-ischemia [abstract]. J Neurotrauma 30:A4
    36. Dewing P, Shi T, Horvath S, Vilain E (2003) Sexually dimorphic gene expression in mouse brain precedes gonadal differentiation. Brain Res Mol Brain Res 118:82鈥?0
    37. Di DF, Casalena G, Jia J, Sultana R, Barone E, Cai J, Pierce WM, Cini C, Mancuso C, Perluigi M, Davis CM, Alkayed NJ, Butterfield DA (2012) Sex differences in brain proteomes of neuron-specific STAT3-null mice after cerebral ischemia/reperfusion. J Neurochem 121:680鈥?92
    38. Diskin T, Tal-Or P, Erlich S, Mizrachy L, Alexandrovich A, Shohami E, Pinkas-Kramarski R (2005) Closed head injury induces upregulation of Beclin 1 at the cortical site of injury. J Neurotrauma 22:750鈥?62
    39. Diwakar L, Kenchappa RS, Annepu J, Ravindranath V (2007) Downregulation of glutaredoxin but not glutathione loss leads to mitochondrial dysfunction in female mice CNS: implications in excitotoxicity. Neurochem Int 51:37鈥?6
    40. Djebaili M, Guo Q, Pettus EH, Hoffman SW, Stein DG (2005) The neurosteroids progesterone and allopregnanolone reduce cell death, gliosis, and functional deficits after traumatic brain injury in rats. J Neurotrauma 22:106鈥?18
    41. Djouadi F, Weinheimer CJ, Saffitz JE, Pitchford C, Bastin J, Gonzalez FJ, Kelly DP (1998) A gender-related defect in lipid metabolism and glucose homeostasis in peroxisome proliferator- activated receptor alpha- deficient mice. J Clin Invest 102:1083鈥?091
    42. Dringen R, Kussmaul L, Gutterer JM, Hirrlinger J, Hamprecht B (1999) The glutathione system of peroxide detoxification is less efficient in neurons than in astroglial cells. J Neurochem 72:2523鈥?530
    43. Du L, Zhang X, Han YY, Burke NA, Kochanek PM, Watkins SC, Graham SH, Carcillo JA, Szabo C, Clark RS (2003) Intra-mitochondrial poly(ADP-ribosylation) contributes to NAD鈥?鈥塪epletion and cell death induced by oxidative stress. J Biol Chem 278:18426鈥?8433
    44. Du L, Bayir H, Lai Y, Zhang X, Kochanek PM, Watkins SC, Graham SH, Clark RS (2004) Innate gender-based proclivity in response to cytotoxicity and programmed cell death pathway. J Biol Chem 279:38563鈥?8570
    45. Du L, Hickey RW, Bayir H, Watkins SC, Tyurin VA, Guo F, Kochanek PM, Jenkins LW, Ren J, Gibson G, Chu CT, Kagan VE , Clark RS (2009) Starving neurons show sex difference in autophagy. J Biol Chem 284:2383鈥?396
    46. Duchen MR (2000a) Mitochondria and Ca(2+)in cell physiology and pathophysiology. Cell Calcium 28:339鈥?48
    47. Duchen MR (2000b) Mitochondria and calcium: from cell signalling to cell death. J Physiol 1:57鈥?8
    48. Enari M, Sakahira H, Yokoyama H, Okawa K, Iwamatsu A, Nagata S (1998) A caspase-activated DNase that degrades DNA during apoptosis, and its inhibitor ICAD. Nature 391:43鈥?0
    49. Erlich S, Alexandrovich A, Shohami E, Pinkas-Kramarski R (2007) Rapamycin is a neuroprotective treatment for traumatic brain injury. Neurobiol Dis 26:86鈥?3
    50. Fatokun AA, Dawson VL, Dawson TM (2014) Parthanatos: mitochondrial-linked mechanisms and therapeutic opportunities. Br J Pharmacol 171:2000鈥?016
    51. Fernandez-Gajardo R, Matamala JM, Carrasco R, Gutierrez R, Melo R, Rodrigo R (2014) Novel therapeutic strategies for traumatic brain injury: acute antioxidant reinforcement. CNS Drugs 28:229鈥?48
    52. Fink EL, Lai Y, Zhang X, Janesko-Feldman K, Adelson PD, Szabo C, Berger RP, Sarnaik AA, Kochanek PM, Clark RS (2008) Quantification of poly(ADP-ribose)-modified proteins in cerebrospinal fluid from infants and children after traumatic brain injury. J Cereb Blood Flow Metab 28:1523鈥?529
    53. Fiskum G (2000) Mitochondrial participation in ischemic and traumatic neural cell death. J Neurotrauma 17:843鈥?55
    54. Fonfria E, Marshall IC, Benham CD, Boyfield I, Brown JD, Hill K, Hughes JP, Skaper SD, McNulty S (2004) TRPM2 channel opening in response to oxidative stress is dependent on activation of poly(ADP-ribose) polymerase. Br J Pharmacol 143:186鈥?92
    55. Ford LM, Sanberg PR, Norman AB, Fogelson MH (1989) MK-801 prevents hippocampal neurodegeneration in neonatal hypoxic-ischemic rats. Arch Neurol 46:1090鈥?096
    56. Gaviria M, Privat A, d'Arbigny P, Kamenka J, Haton H, Ohanna F (2000) Neuroprotective effects of a novel NMDA antagonist, Gacyclidine, after experimental contusive spinal cord injury in adult rats. Brain Res 874:200鈥?09
    57. Ginet V, Spiehlmann A, Rummel C, Rudinskiy N, Grishchuk Y, Luthi-Carter R, Clarke PG, Truttmann AC, Puyal J (2014) Involvement of autophagy in hypoxic-excitotoxic neuronal death. Autophagy 10:846鈥?60
    58. Giordano G, Tait L, Furlong CE, Cole TB, Kavanagh TJ, Costa LG (2013) Gender differences in brain susceptibility to oxidative stress are mediated by levels of paraoxonase-2 expression. Free Radic Biol Med 58:98鈥?08
    59. Giulivi C (2007) Mitochondria as generators and targets of nitric oxide. Novartis Found Symp 287:92鈥?00
    60. Guo Z, Cao G, Yang H, Zhou H, Li L, Cao Z, Yu B, Kou J (2014) A combination of four active compounds alleviates cerebral ischemia-reperfusion injury in correlation with inhibition of autophagy and modulation of AMPK/mTOR and JNK pathways. J Neurosci Res 92(10):1295鈥?306
    61. Hagberg H, Mallard C, Rousset CI, Thornton C (2014) Mitochondria: hub of injury responses in the developing brain. Lancet Neurol 13:217鈥?32
    62. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, Lippincott-Schwartz J (2010) Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell 141:656鈥?67
    63. Han RZ, Hu JJ, Weng YC, Li DF, Huang Y (2009) NMDA receptor antagonist MK-801 reduces neuronal damage and preserves learning and memory in a rat model of traumatic brain injury. Neurosci Bull 25:367鈥?75
    64. Harman D (1956) Aging: a theory based on free radical and radiation chemistry. J Gerontol 11:298鈥?00
    65. Harman D (1972) The biologic clock: the mitochondria? J Am Geriatr Soc 20:145鈥?47
    66. Haynes V, Elfering S, Traaseth N, Giulivi C (2004) Mitochondrial nitric-oxide synthase: enzyme expression, characterization, and regulation. J Bioenerg Biomembr 36:341鈥?46
    67. Hill CA, Fitch RH (2012) Sex differences in mechanisms and outcome of neonatal hypoxia-ischemia in rodent models: implications for sex-specific neuroprotection in clinical neonatal practice. Neurol Res Int 2012:1鈥?
    68. Hill CA, Alexander ML, McCullough LD, Fitch RH (2011) Inhibition of X-linked inhibitor of apoptosis with embelin differentially affects male versus female behavioral outcome following neonatal hypoxia-ischemia in rats. Dev Neurosci 33:494鈥?04
    69. Hilton GD, Nunez JL, Bambrick L, Thompson SM, McCarthy MM (2006) Glutamate-mediated excitotoxicity in neonatal hippocampal neurons is mediated by mGluR-induced release of Ca++ from intracellular stores and is prevented by estradiol. Eur J Neurosci 24:3008鈥?016
    70. Huang Q, Shen HM (2009) To die or to live: the dual role of poly(ADP-ribose) polymerase-1 in autophagy and necrosis under oxidative stress and DNA damage. Autophagy 5:273鈥?76
    71. Hutson CB, Lazo CR, Mortazavi F, Giza CC, Hovda D, Chesselet MF (2011) Traumatic brain injury in adult rats causes progressive nigrostriatal dopaminergic cell loss and enhanced vulnerability to the pesticide paraquat. J Neurotrauma 28:1783鈥?801
    72. Hyman BT, Yuan J (2012) Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci 13:395鈥?06
    73. Jahani-Asl A, Pilon-Larose K, Xu W, MacLaurin JG, Park DS, McBride HM, Slack RS (2011) The mitochondrial inner membrane GTPase, optic atrophy 1 (Opa1), restores mitochondrial morphology and promotes neuronal survival following excitotoxicity. J Biol Chem 286:4772鈥?782
    74. Jia J, Verma S, Nakayama S, Quillinan N, Grafe MR, Hurn PD, Herson PS (2011) Sex differences in neuroprotection provided by inhibition of TRPM2 channels following experimental stroke. J Cereb Blood Flow Metab 31:2160鈥?168
    75. Jikumaru M, Hiramoto K, Honma T, Sato EF, Sekiyama A, Inoue M (2007) Effect of starvation on the survival of male and female mice. Physiol Chem Phys Med NMR 39:247鈥?57
    76. Kashani IR, Rajabi Z, Akbari M, Hassanzadeh G, Mohseni A, Eramsadati MK, Rafiee K, Beyer C, Kipp M, Zendedel A (2014) Protective effects of melatonin against mitochondrial injury in a mouse model of multiple sclerosis. Exp Brain Res 232(9):2835鈥?846
    77. Keller JN, Kindy MS, Holtsberg FW, St Clair DK, Yen HC, Germeyer A, Steiner SM, Bruce-Keller AJ, Hutchins JB, Mattson MP (1998) Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J Neurosci 18:687鈥?97
    78. Kenchappa RS, Ravindranath V (2003) Glutaredoxin is essential for maintenance of brain mitochondrial complex I: studies with MPTP. FASEB J 17:717鈥?19
    79. Kenchappa RS, Diwakar L, Boyd MR, Ravindranath V (2002) Thioltransferase (glutaredoxin) mediates recovery of motor neurons from excitotoxic mitochondrial injury. J Neurosci 22:8402鈥?410
    80. Kenchappa RS, Diwakar L, Annepu J, Ravindranath V (2004) Estrogen and neuroprotection: higher constitutive expression of glutaredoxin in female mice offers protection against MPTP-mediated neurodegeneration. FASEB J 18:1102鈥?104
    81. Kim HJ, Magrane J, Starkov AA, Manfredi G (2012) The mitochondrial calcium regulator cyclophilin D is an essential component of oestrogen-mediated neuroprotection in amyotrophic lateral sclerosis. Brain 135:2865鈥?874
    82. Kirkland RA, Adibhatla RM, Hatcher JF, Franklin JL (2002) Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy. Neuroscience 115:587鈥?02
    83. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, Tanaka K, Uchiyama Y (2008) Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol 172:454鈥?69
    84. Lagranha CJ, Deschamps A, Aponte A, Steenbergen C, Murphy E (2010) Sex differences in the phosphorylation of mitochondrial proteins result in reduced production of reactive oxygen species and cardioprotection in females. Circ Res 106:1681鈥?691
    85. Lamont LS (2005) Gender differences in amino acid use during endurance exercise. Nutr Rev 63:419鈥?22
    86. Lapchak PA (2004) The neuroactive steroid 3-alpha-ol-5-beta-pregnan-20-one hemisuccinate, a selective NMDA receptor antagonist improves behavioral performance following spinal cord ischemia. Brain Res 997:152鈥?58
    87. Lee BI, Lee DJ, Cho KJ, Kim GW (2005) Early nuclear translocation of endonuclease G and subsequent DNA fragmentation after transient focal cerebral ischemia in mice. Neurosci Lett 386:23鈥?7
    88. Li H, Pin S, Zeng Z, Wang MM, Andreasson KA, McCullough LD (2005) Sex differences in cell death. Ann Neurol 58:317鈥?21
    89. Lieb K, Andrae J, Reisert I, Pilgrim C (1995) Neurotoxicity of dopamine and protective effects of the NMDA receptor antagonist AP-5 differ between male and female dopaminergic neurons. Exp Neurol 134:222鈥?29
    90. Lin CJ, Chen TH, Yang LY, Shih CM (2014) Resveratrol protects astrocytes against traumatic brain injury through inhibiting apoptotic and autophagic cell death. Cell Death Differ 5:e1147
    91. Lubomski M, Louise RR, Lee W, Bertram KL, Williams DR (2014) Sex differences in Parkinson鈥檚 disease. J Clin Neurosci 21(9):1503鈥?506
    92. Martin LJ (2011) An approach to experimental synaptic pathology using green fluorescent protein-transgenic mice and gene knockout mice to show mitochondrial permeability transition pore-driven excitotoxicity in interneurons and motoneurons. Toxicol Pathol 39:220鈥?33
    93. Masmoudi A, Mandel P (1987) ADP-ribosyl transferase and NAD glycohydrolase activities in rat liver mitochondria. Biochemistry 26:1965鈥?969
    94. Masmoudi A, Islam F, Mandel P (1988) ADP-ribosylation of highly purified rat brain mitochondria. J Neurochem 51:188鈥?93
    95. McCarthy MM (2008) Estradiol and the developing brain. Physiol Rev 88:91鈥?24
    96. McCarthy MM, Arnold AP (2011) Reframing sexual differentiation of the brain. Nat Neurosci 14:677鈥?83
    97. McCarthy MM, Arnold AP, Ball GF, Blaustein JD, De Vries GJ (2012) Sex differences in the brain: the not so inconvenient truth. J Neurosci 32:2241鈥?247
    98. McCullough LD, Zeng Z, Blizzard KK, Debchoudhury I, Hurn PD (2005) Ischemic nitric oxide and poly (ADP-ribose) polymerase-1 in cerebral ischemia: male toxicity, female protection. J Cereb Blood Flow Metab 25:502鈥?12
    99. Mecocci P, MacGarvey U, Kaufman AE, Koontz D, Shoffner JM, Wallace DC, Beal MF (1993) Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol 34:609鈥?16
    100. Mehta SL, Kumari S, Mendelev N, Li PA (2012) Selenium preserves mitochondrial function, stimulates mitochondrial biogenesis, and reduces infarct volume after focal cerebral ischemia. BMC Neurosci 13:79
    101. Michel S, Wanet A, De PA, Rommelaere G, Arnould T, Renard P (2012) Crosstalk between mitochondrial (dys)function and mitochondrial abundance. J Cell Physiol 227:2297鈥?310
    102. Minano A, Cerbon MA, Xifro X, Malagelada C, Aguilera J, Rodriguez-Alvarez J (2007) 17beta-estradiol does not protect cerebellar granule cells from excitotoxicity or apoptosis. J Neurochem 102:354鈥?64
    103. Minghetti L, Greco A, Zanardo V, Suppiej A (2013) Early-life sex-dependent vulnerability to oxidative stress: the natural twining model. J Matern Fetal Neonatal Med 26:259鈥?62
    104. Misiak M, Beyer C, Arnold S (2010) Gender-specific role of mitochondria in the vulnerability of 6-hydroxydopamine-treated mesencephalic neurons. Biochim Biophys Acta 1797:1178鈥?188
    105. Mohagheghi F, Ahmadiani A, Rahmani B, Moradi F, Romond N, Khalaj L (2013a) Gemfibrozil pretreatment resulted in a sexually dimorphic outcome in the rat models of global cerebral ischemia-reperfusion via modulation of mitochondrial pro-survival and apoptotic cell death factors as well as MAPKs. J Mol Neurosci 50:379鈥?93
    106. Mohagheghi F, Khalaj L, Ahmadiani A, Rahmani B (2013b) Gemfibrozil pretreatment affecting antioxidant defense system and inflammatory, but not Nrf-2 signaling pathways resulted in female neuroprotection and male neurotoxicity in the rat models of global cerebral ischemia-reperfusion. Neurotox Res 23:225鈥?37
    107. Murakami K, Kondo T, Kawase M, Li Y, Sato S, Chen SF, Chan PH (1998) Mitochondrial susceptibility to oxidative stress exacerbates cerebral infarction that follows permanent focal cerebral ischemia in mutant mice with manganese superoxide dismutase deficiency. J Neurosci 18:205鈥?13
    108. Nicholls DG (2004) Mitochondrial dysfunction and glutamate excitotoxicity studied in primary neuronal cultures. Curr Mol Med 4:149鈥?77
    109. Nilsen J, Brinton RD (2004) Mitochondria as therapeutic targets of estrogen action in the central nervous system. Curr Drug Targets CNS Neurol Disord 3:297鈥?13
    110. Nu帽ez JL, McCarthy MM (2008) Androgens predispose males to GABAA-mediated excitotoxicity in the developing hippocampus. Exp Neurol 210:699鈥?08
    111. Nu帽ez JL, Alt JJ, McCarthy MM (2003) A new model for prenatal brain damage I GABAA receptor activation induces cell death in developing rat hippocampus. Exp Neurol 181:258鈥?69
    112. Owens K, Park JH, Schuh R, Kristian T (2013) Mitochondrial dysfunction and NAD(+) metabolism alterations in the pathophysiology of acute brain injury. Transl Stroke Res 4:618鈥?34
    113. Pankotai E, Lacza Z, Muranyi M, Szabo C (2009) Intra-mitochondrial poly(ADP-ribosyl)ation: potential role for alpha-ketoglutarate dehydrogenase. Mitochondrion 9:159鈥?64
    114. Peng TI, Jou MJ (2010) Oxidative stress caused by mitochondrial calcium overload. Ann N Y Acad Sci 1201:183鈥?88
    115. Perez-Pinzon MA, Stetler RA, Fiskum G (2012) Novel mitochondrial targets for neuroprotection. J Cereb Blood Flow Metab 32:1362鈥?376
    116. Perrella J, Bhavnani BR (2005) Protection of cortical cells by equine estrogens against glutamate-induced excitotoxicity is mediated through a calcium independent mechanism. BMC Neurosci 6:34
    117. Pinto RE, Bartley W (1969) The nature of the sex-linked differences in glutathione peroxidase activity and aerobic oxidation of glutathione in male and female rat liver. Biochem J 115:449鈥?56
    118. Portera-Cailliau C, Price DL, Martin LJ (1997) Non-NMDA and NMDA receptor-mediated excitotoxic neuronal deaths in adult brain are morphologically distinct: further evidence for an apoptosis-necrosis continuum. J Comp Neurol 378:88鈥?04
    119. Pringsheim T, Jette N, Frolkis A, Steeves TD (2014) The prevalence of Parkinson鈥檚 disease: A systematic review and meta-analysis. Mov Disord. doi:10.1002/mds.25945
    120. Purnell PR, Fox HS (2013) Autophagy-mediated turnover of dynamin-related protein 1. BMC Neurosci 14:86
    121. Quillinan N, Deng G, Grewal H, Herson PS (2014) Androgens and stroke: Good, bad or indifferent? Exp Neurol
    122. Rambold AS, Kostelecky B, Elia N, Lippincott-Schwartz J (2011) Tubular network formation protects mitochondria from autophagosomal degradation during nutrient starvation. Proc Natl Acad Sci U S A 108:10190鈥?0195
    123. Rao VL, Dogan A, Todd KG, Bowen KK, Dempsey RJ (2001) Neuroprotection by memantine, a non-competitive NMDA receptor antagonist after traumatic brain injury in rats. Brain Res 911:96鈥?00
    124. Robertson CL, Soane L, Siegel ZT, Fiskum G (2006) The potential role of mitochondria in pediatric traumatic brain injury. Dev Neurosci 28:432鈥?46
    125. Rossi MN, Carbone M, Mostocotto C, Mancone C, Tripodi M, Maione R, Amati P (2009) Mitochondrial localization of PARP-1 requires interaction with mitofilin and is involved in the maintenance of mitochondrial DNA integrity. J Biol Chem 284:31616鈥?1624
    126. Saeed U, Karunakaran S, Meka DP, Koumar RC, Ramakrishnan S, Joshi SD, Nidadavolu P, Ravindranath V (2009) Redox activated MAP kinase death signaling cascade initiated by ASK1 is not activated in female mice following MPTP: novel mechanism of neuroprotection. Neurotox Res 16:116鈥?26
    127. Scarpulla RC (2002) Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576:1鈥?4
    128. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26:1749鈥?760
    129. Semenas E, Nozari A, Sharma HS, Basu S, Rubertsson S, Wiklund L (2010) Sex differences in cerebral injury after severe haemorrhage and ventricular fibrillation in pigs. Acta Anaesthesiol Scand 54:343鈥?53
    130. Sharma J, Johnston MV, Hossain MA (2014) Sex differences in mitochondrial biogenesis determine neuronal death and survival in response to oxygen glucose deprivation and reoxygenation. BMC Neurosci 15:9
    131. Shin SS, Bray ER, Dixon CE (2012) Effects of nicotine administration on striatal dopamine signaling after traumatic brain injury in rats. J Neurotrauma 29:843鈥?50
    132. Siegel CS, McCullough LD (2013) NAD鈥?鈥塧nd nicotinamide: sex differences in cerebral ischemia. Neuroscience 237:223鈥?31
    133. Siegel C, Li J, Liu F, Benashski SE, McCullough LD (2011) miR-23a regulation of X-linked inhibitor of apoptosis (XIAP) contributes to sex differences in the response to cerebral ischemia. Proc Natl Acad Sci U S A 108:11662鈥?1667
    134. Simpkins JW, Dykens JA (2008) Mitochondrial mechanisms of estrogen neuroprotection. Brain Res Rev 57:421鈥?30
    135. Simpkins JW, Wang J, Wang X, Perez E, Prokai L, Dykens JA (2005) Mitochondria play a central role in estrogen-induced neuroprotection. Curr Drug Targets CNS Neurol Disord 4:69鈥?3
    136. Slupe AM, Merrill RA, Flippo KH, Lobas MA, Houtman JC, Strack S (2013) A calcineurin docking motif (LXVP) in dynamin-related protein 1 contributes to mitochondrial fragmentation and ischemic neuronal injury. J Biol Chem 288:12353鈥?2365
    137. Smith CM, Chen Y, Sullivan ML, Kochanek PM, Clark RS (2011) Autophagy in acute brain injury: feast, famine, or folly? Neurobiol Dis 43:52鈥?9
    138. Starkov AA (2013) An update on the role of mitochondrial alpha-ketoglutarate dehydrogenase in oxidative stress. Mol Cell Neurosci 55:13鈥?6
    139. Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, Beal MF (2004) Mitochondrial alpha-ketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci 24:7779鈥?788
    140. Stoica BA, Loane DJ, Zhao Z, Kabadi SV, Hanscom M, Byrnes KR, Faden AI (2014) PARP-1 inhibition attenuates neuronal loss, microglia activation and neurological deficits after traumatic brain injury. J Neurotrauma 31:758鈥?72
    141. Sundar BS, Barbara VM, Roemgens A, Beyer C, Arnold S (2011) Sex- and brain region-specific role of cytochrome c oxidase in 1-methyl-4-phenylpyridinium-mediated astrocyte vulnerability. J Neurosci Res 89:2068鈥?082
    142. Turtzo LC, McCullough LD (2010) Sex-specific responses to stroke. Future Neurol 5:47鈥?9
    143. van Bregt DR, Thomas TC, Hinzman JM, Cao T, Liu M, Bing G, Gerhardt GA, Pauly JR, Lifshitz J (2012) Substantia nigra vulnerability after a single moderate diffuse brain injury in the rat. Exp Neurol 234:8鈥?9
    144. van der Bliek AM, Shen Q, Kawajiri S (2013) Mechanisms of mitochondrial fission and fusion. Cold Spring Harb Perspect Biol. doi:10.1101/cshperspect.a011072
    145. Varma S, Janesko KL, Wisniewski SR, Bayir H, Adelson PD, Thomas NJ, Kochanek PM (2003) F2-isoprostane and neuron-specific enolase in cerebrospinal fluid after severe traumatic brain injury in infants and children. J Neurotrauma 20:781鈥?86
    146. Verma S, Quillinan N, Yang YF, Nakayama S, Cheng J, Kelley MH, Herson PS (2012) TRPM2 channel activation following in vitro ischemia contributes to male hippocampal cell death. Neurosci Lett 530:41鈥?6
    147. Virbasius JV, Virbasius CA, Scarpulla RC (1993) Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev 7:380鈥?92
    148. Wagner AK, Fabio A, Puccio AM, Hirschberg R, Li W, Zafonte RD, Marion DW (2005) Gender associations with cerebrospinal fluid glutamate and lactate/pyruvate levels after severe traumatic brain injury. Crit Care Med 33:407鈥?13
    149. Wang L, Cherednichenko G, Hernandez L, Halow J, Camacho SA, Figueredo V, Schaefer S (2001) Preconditioning limits mitochondrial Ca(2+) during ischemia in rat hearts: role of K(ATP) channels. Am J Physiol Heart Circ Physiol 280:H2321鈥揌2328
    150. Wang Y, Dawson VL, Dawson TM (2009) Poly(ADP-ribose) signals to mitochondrial AIF: a key event in parthanatos. Exp Neurol 218:193鈥?02
    151. Wang Y, Kim NS, Haince JF, Kang HC, David KK, Andrabi SA, Poirier GG, Dawson VL, Dawson TM (2011) Poly(ADP-ribose) (PAR) binding to apoptosis-inducing factor is critical for PAR polymerase-1-dependent cell death (parthanatos). Sci Signal 4:20
    152. Wang T, Huang XJ, Van KC, Went GT, Nguyen JT, Lyeth BG (2014) Amantadine improves cognitive outcome and increases neuronal survival after fluid percussion traumatic brain injury in rats. J Neurotrauma 31:370鈥?77
    153. Weaver CE Jr, Park-Chung M, Gibbs TT, Farb DH (1997) 17beta-Estradiol protects against NMDA-induced excitotoxicity by direct inhibition of NMDA receptors. Brain Res 761:338鈥?41
    154. Weis SN, Pettenuzzo LF, Krolow R, Valentim LM, Mota CS, Dalmaz C, Wyse AT, Netto CA (2012) Neonatal hypoxia-ischemia induces sex-related changes in rat brain mitochondria. Mitochondrion 12:271鈥?79
    155. Weis SN, Toniazzo AP, Ander BP, Zhan X, Careaga M, Ashwood P, Wyse AT, Netto CA, Sharp FR (2014) Autophagy in the brain of neonates following hypoxia-ischemia shows sex- and region-specific effects. Neuroscience 256:201鈥?09
    156. Widdowson EM (1976) The response of the sexes to nutritional stress. Proc Nutr Soc 35:175鈥?80
    157. Xie Y, Li J, Fan G, Qi S, Li B (2014) Reperfusion promotes mitochondrial biogenesis following focal cerebral ischemia in rats. PLoS One 9:e92443
    158. Xiong Y, Peterson PL, Lee CP (1999) Effect of N-acetylcysteine on mitochondrial function following traumatic brain injury in rats. J Neurotrauma 16:1067鈥?082
    159. Yan HQ, Ma X, Chen X, Li Y, Shao L, Dixon CE (2007) Delayed increase of tyrosine hydroxylase expression in rat nigrostriatal system after traumatic brain injury. Brain Res 1134:171鈥?79
    160. Yin W, Signore AP, Iwai M, Cao G, Gao Y, Chen J (2008) Rapidly increased neuronal mitochondrial biogenesis after hypoxic-ischemic brain injury. Stroke 39:3057鈥?063
    161. Yuan M, Siegel C, Zeng Z, Li J, Liu F, McCullough LD (2009) Sex differences in the response to activation of the poly (ADP-ribose) polymerase pathway after experimental stroke. Exp Neurol 217:210鈥?18
    162. Zhang C, Wong-Riley MT (2000) Depolarizing stimulation upregulates GA-binding protein in neurons: a transcription factor involved in the bigenomic expression of cytochrome oxidase subunits. Eur J Neurosci 12:1013鈥?023
    163. Zhang C, Yuan XR, Li HY, Zhao ZJ, Liao YW, Wang XY, Su J, Sang SS, Liu Q (2014) Downregualtion of dynamin-related protein 1 attenuates glutamate-induced excitotoxicity via regulating mitochondrial function in a calcium dependent manner in HT22 cells. Biochem Biophys Res Commun 443:138鈥?43
    164. Zheng Y, Hou J, Liu J, Yao M, Li L, Zhang B, Zhu H, Wang Z (2014) Inhibition of autophagy contributes to melatonin-mediated neuroprotection against transient focal cerebral ischemia in rats. J Pharmacol Sci 124:354鈥?64
    165. Zhou H, Wang J, Jiang J, Stavrovskaya IG, Li M, Li W, Wu Q, Zhang X, Luo C, Zhou S, Sirianni AC, Sarkar S, Kristal BS, Friedlander RM, Wang X (2014) N-acetyl-serotonin offers neuroprotection through inhibiting mitochondrial death pathways and autophagic activation in experimental models of ischemic injury. J Neurosci 34:2967鈥?978
    166. Zhu JH, Horbinski C, Guo F, Watkins S, Uchiyama Y, Chu CT (2007) Regulation of autophagy by extracellular signal-regulated protein kinases during 1-methyl-4-phenylpyridinium-induced cell death. Am J Pathol 170:75鈥?6
    167. Zuo W, Zhang W, Chen NH (2013) Sexual dimorphism in cerebral ischemia injury. Eur J Pharmacol 711:73鈥?9
  • 刊物类别：Chemistry and Materials Science
  • 刊物主题：Chemistry
    Bioorganic Chemistry
    Biochemistry
    Animal Anatomy, Morphology and Histology
    Animal Biochemistry
    Organic Chemistry
  • 出版者：Springer New York
  • ISSN：1573-6881
文摘
Decades of research have revealed numerous differences in brain structure size, connectivity and metabolism between males and females. Sex differences in neurobehavioral and cognitive function after various forms of central nervous system (CNS) injury are observed in clinical practice and animal research studies. Sources of sex differences include early life exposure to gonadal hormones, chromosome compliment and adult hormonal modulation. It is becoming increasingly apparent that mitochondrial metabolism and cell death signaling are also sexually dimorphic. Mitochondrial metabolic dysfunction is a common feature of CNS injury. Evidence suggests males predominantly utilize proteins while females predominantly use lipids as a fuel source within mitochondria and that these differences may significantly affect cellular survival following injury. These fundamental biochemical differences have a profound impact on energy production and many cellular processes in health and disease. This review will focus on the accumulated evidence revealing sex differences in mitochondrial function and cellular signaling pathways in the context of CNS injury mechanisms and the potential implications for neuroprotective therapy development.

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