Dichloroacetate treatment improves mitochondrial metabolism and reduces brain injury in neonatal mice

Oncotarget

Volumn 7, Issue 22, 2016, Pages 31708-31722

  Sun, Yanyan ^a,b   Li, Tao ^a,b,c   Xie, Cuicui ^b   Zhang, Yaodong ^b,c   Zhou, Kai ^b,d   Wang, Xiaoyang ^a,b   Blomgren, Klas ^d   Zhu, Changlian ^a,b,e  

^a ZHENGZHOU UNIVERSITY   (China)

^b UNIVERSITY OF GOTHENBURG   (Sweden)

^c ZHENGZHOU CHILDREN S HOSPITAL   (China)

^d KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^e Henan Key Laboratory for Neonatal Brain Injury   (China)

Author keywords

Apoptosis; Autophagy; Brain ischemia; Mitochondria; Pathology Section; Pyruvate dehydrogenase

Indexed keywords

ACETYL COENZYME A; APOPTOSIS INDUCING FACTOR; CASPASE 3; DICHLOROACETIC ACID; MESSENGER RNA; MITOCHONDRIAL TRANSCRIPTION FACTOR A; MYELIN BASIC PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PYRUVATE DEHYDROGENASE; TRANSCRIPTION FACTOR NRF1; CASPASE; NEUROPROTECTIVE AGENT; PYRUVATE DEHYDROGENASE COMPLEX;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BRAIN INFARCTION SIZE; CONTROLLED STUDY; HYPOXIC ISCHEMIC ENCEPHALOPATHY; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; NEWBORN; NONHUMAN; WHITE MATTER INJURY; ANIMAL; BRAIN; BRAIN INJURY; C57BL MOUSE; CELL PROTECTION; DISEASE MODEL; DRUG EFFECTS; ENERGY METABOLISM; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; ORGANELLE BIOGENESIS; PATHOLOGY; TIME FACTOR;

ACETYL COENZYME A; ANIMALS; ANIMALS, NEWBORN; APOPTOSIS; AUTOPHAGY; BRAIN; BRAIN INJURIES; CASPASES; CYTOPROTECTION; DICHLOROACETIC ACID; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; HYPOXIA-ISCHEMIA, BRAIN; MALE; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; NEUROPROTECTIVE AGENTS; ORGANELLE BIOGENESIS; PYRUVATE DEHYDROGENASE COMPLEX; TIME FACTORS;

EID: 84973515357     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.9150     Document Type: Article

References (52)

1. Black RE, Cousens S, Johnson HL, Lawn JE, Rudan I, Bassani DG, Jha P, Campbell H, Walker CF, Cibulskis R, Eisele T, Liu L, Mathers C. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet. 2010;375:1969-1987.
2. Liu L, Oza S, Hogan D, Perin J, Rudan I, Lawn JE, Cousens S, Mathers C and Black RE. Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet. 2015;385:430-440.
3. Douglas-Escobar M, Weiss MD. Hypoxic-ischemic encephalopathy: a review for the clinician. JAMA Pediatr. 2015;169:397-403.
4. Hagberg H, Mallard C, Rousset CI, Thornton C. Mitochondria: hub of injury responses in the developing brain. Lancet Neurol. 2014;13:217-232.
5. Rousset CI, Baburamani AA, Thornton C, Hagberg H. Mitochondria and perinatal brain injury. J Matern Fetal Neonatal Med. 2012;25 Suppl 1:35-38.
6. Azzopardi D, Strohm B, Marlow N, Brocklehurst P, Deierl A, Eddama O, Goodwin J, Halliday HL, Juszczak E, Kapellou O, Levene M, Linsell L, Omar O, et al. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med. 2014;371:140-149.
7. Zhou WH, Cheng GQ, Shao XM, Liu XZ, Shan RB, Zhuang DY, Zhou CL, Du LZ, Cao Y, Yang Q, Wang LS. Selective head cooling with mild systemic hypothermia after neonatal hypoxic-ischemic encephalopathy: a multicenter randomized controlled trial in China. J Pediatr. 2010;157:367-372.
8. Zhu C, Kang W, Xu F, Cheng X, Zhang Z, Jia L, Ji L, Guo X, Xiong H, Simbruner G, Blomgren K and Wang X. Erythropoietin improved neurologic outcomes in newborns with hypoxic-ischemic encephalopathy. Pediatrics. 2009;124(2):e218-26.
9. Wu YW, Bauer LA, Ballard RA, Ferriero DM, Glidden DV, Mayock DE, Chang T, Durand DJ, Song D, Bonifacio SL, Gonzalez FF, Glass HC and Juul SE. Erythropoietin for neuroprotection in neonatal encephalopathy: safety and pharmacokinetics. Pediatrics. 2012;130:683-691.
10. Johnston MV, Fatemi A, Wilson MA, Northington F. Treatment advances in neonatal neuroprotection and neurointensive care. Lancet Neurol. 2011;10:372-382.
11. Yager JY, Brucklacher RM, Vannucci RC. Cerebral energy metabolism during hypoxia-ischemia and early recovery in immature rats. Am J Physiol. 1992;262:H672-677.
12. Blomgren K, Zhu C, Wang X, Karlsson JO, Leverin AL, Bahr BA, Mallard C and Hagberg H. Synergistic activation of caspase-3 by m-calpain after neonatal hypoxia-ischemia: a mechanism of "pathological apoptosis"? J Biol Chem. 2001;276:10191-10198.
13. Marino G, Pietrocola F, Eisenberg T, Kong Y, Malik SA, Andryushkova A, Schroeder S, Pendl T, Harger A, Niso-Santano M, Zamzami N, Scoazec M, Durand S, et al. Regulation of autophagy by cytosolic acetyl-coenzyme A. Mol Cell. 2014;53:710-725.
14. Murray DM, Boylan GB, Fitzgerald AP, Ryan CA, Murphy BP, Connolly S. Persistent lactic acidosis in neonatal hypoxic-ischaemic encephalopathy correlates with EEG grade and electrographic seizure burden. Arch Dis Child Fetal Neonatal Ed. 2008;93:F183-186.
15. Williams PJ, Lane JR, Turkel CC, Capparelli EV, Dziewanowska Z, Fox AW. Dichloroacetate: population pharmacokinetics with a pharmacodynamic sequential link model. J Clin Pharmacol. 2001;41:259-267.
16. Berendzen K, Theriaque DW, Shuster J, Stacpoole PW. Therapeutic potential of dichloroacetate for pyruvate dehydrogenase complex deficiency. Mitochondrion. 2006;6:126-135.
17. Koga Y, Povalko N, Katayama K, Kakimoto N, Matsuishi T, Naito E and Tanaka M. Beneficial effect of pyruvate therapy on Leigh syndrome due to a novel mutation in PDH E1alpha gene. Brain Dev. 2012;34:87-91.
18. Stacpoole PW, Kerr DS, Barnes C, Bunch ST, Carney PR, Fennell EM, Felitsyn NM, Gilmore RL, Greer M, Henderson GN, Hutson AD, Neiberger RE, O'Brien RG, et al. Controlled clinical trial of dichloroacetate for treatment of congenital lactic acidosis in children. Pediatrics. 2006;117:1519-1531.
19. Abdelmalak M, Lew A, Ramezani R, Shroads AL, Coats BS, Langaee T, Shankar MN, Neiberger RE, Subramony SH and Stacpoole PW. Long-term safety of dichloroacetate in congenital lactic acidosis. Mol Genet Metab. 2013;109:139-143.
20. Stacpoole PW, Gilbert LR, Neiberger RE, Carney PR, Valenstein E, Theriaque DW and Shuster JJ. Evaluation of long-term treatment of children with congenital lactic acidosis with dichloroacetate. Pediatrics. 2008;121:e1223-228.
21. Katayama Y, Welsh FA. Effect of dichloroacetate on regional energy metabolites and pyruvate dehydrogenase activity during ischemia and reperfusion in gerbil brain. J Neurochem. 1989;52:1817-1822.
22. Corbett R, Laptook A, Gee J, Garcia D, Silmon S, Tollefsbol G. Age-related differences in the effect of dichloroacetate on postischemic lactate and acid clearance measured in vivo using magnetic resonance spectroscopy and microdialysis. J Neurochem. 1998;71:1205-1214.
23. Madeo F, Pietrocola F, Eisenberg T, Kroemer G. Caloric restriction mimetics: towards a molecular definition. Nat Rev Drug Discov. 2014;13:727-740.
24. Ginet V, Spiehlmann A, Rummel C, Rudinskiy N, Grishchuk Y, Luthi-Carter R, Clarke PG, Truttmann AC and Puyal J. Involvement of autophagy in hypoxicexcitotoxic neuronal death. Autophagy. 2014;10:846-860.
25. Xie C, Ginet V, Sun Y, Koike M, Zhou K, Li T, Li H, Li Q, Wang X, Yasuo U, Truttmann A, Kroemer G, Puyal J, et al. Neuroprotection by selective neuronal deletion of autophagy-related gene 7 in neonatal brain injury. Autophagy. 2016; 12:410-423.
26. Zhu C, Wang X, Xu F, Bahr BA, Shibata M, Uchiyama Y, Hagberg H and Blomgren K. The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia. Cell Death Differ. 2005;12:162-176.
27. Wang X, Karlsson JO, Zhu C, Bahr BA, Hagberg H, Blomgren K. Caspase-3 activation after neonatal rat cerebral hypoxia-ischemia. Biol Neonate. 2001;79:172-179.
28. Chang LH, Shimizu H, Abiko H, Swanson RA, Faden AI, James TL and Weinstein PR. Effect of dichloroacetate on recovery of brain lactate, phosphorus energy metabolites, and glutamate during reperfusion after complete cerebral ischemia in rats. J Cereb Blood Flow Metab. 1992;12:1030-1038.
29. Peeling J, Sutherland G, Brown RA, Curry S. Protective effect of dichloroacetate in a rat model of forebrain ischemia. Neurosci Lett. 1996;208:21-24.
30. Iwata O, Iwata S, Bainbridge A, De Vita E, Matsuishi T, Cady EB and Robertson NJ. Supra-and sub-baseline phosphocreatine recovery in developing brain after transient hypoxia-ischaemia: relation to baseline energetics, insult severity and outcome. Brain. 2008;131:2220-2226.
31. Medeiros DM. Assessing mitochondria biogenesis. Methods. 2008;46:288-294.
32. Yin W, Signore AP, Iwai M, Cao G, Gao Y, Chen J. Rapidly increased neuronal mitochondrial biogenesis after hypoxic-ischemic brain injury. Stroke. 2008;39:3057-3063.
33. Correa F, Ljunggren E, Patil J, Wang X, Hagberg H, Mallard C, Sandberg M. Time-dependent effects of systemic lipopolysaccharide injection on regulators of antioxidant defence Nrf2 and PGC-1alpha in the neonatal rat brain. Neuroimmunomodulation. 2013;20:185-193.
34. Liesa M, Shirihai OS. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013;17:491-506.
35. Sheridan C, Martin SJ. Mitochondrial fission/fusion dynamics and apoptosis. Mitochondrion. 2010;10:640-648.
36. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD, Walzer G, Stiles L, Haigh SE, Katz S, Las G, Alroy J, Wu M, Py BF, et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008;27:433-446.
37. Baburamani AA, Hurling C, Stolp H, Sobotka K, Gressens P, Hagberg H, Thornton C. Mitochondrial optic atrophy (OPA) 1 processing is altered in response to neonatal hypoxicischemic brain injury. Int J Mol Sci. 2015;16:22509-22526.
38. Sanderson TH, Raghunayakula S, Kumar R. Neuronal hypoxia disrupts mitochondrial fusion. Neuroscience. 2015;301:71-8.
39. Sharp WW, Fang YH, Han M, Zhang HJ, Hong Z, Banathy A, Morrow E, Eyan JJ, Archer SL. Dynamin-related protein 1 (Drp1)-mediated diastolic dysfunction in myocardial ischemia-reperfusion injury: therapeutic benefits of Drp1 inhibition to reduce mitochondrial fission. FASEB J. 2014;28:316-326.
40. Oppenheim RW, Blomgren K, Ethell DW, Koike M, Komatsu M, Prevette D, Roth KA, Uchiyama Y, Vinsant S and Zhu C. Developing postmitotic mammalian neurons in vivo lacking Apaf-1 undergo programmed cell death by a caspase-independent, nonapoptotic pathway involving autophagy. J Neurosci. 2008;28:1490-1497.
41. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E and Tanaka K. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature. 2006;441:880-884.
42. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S, Massey DC, Menzies FM, Moreau K, et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol Rev. 2010;90:1383-1435.
43. Li Q, Li H, Roughton K, Wang X, Kroemer G, Blomgren K, Zhu C. Lithium reduces apoptosis and autophagy after neonatal hypoxia-ischemia. Cell Death Dis. 2010;1:e56.
44. Marino G, Pietrocola F, Madeo F, Kroemer G. Caloric restriction mimetics: natural/physiological pharmacological autophagy inducers. Autophagy. 2014;10:1879-1882.
45. Koike M, Shibata M, Tadakoshi M, Gotoh K, Komatsu M, Waguri S, Kawahara N, Kuida K, Nagata S, Kominami E, Tanaka K and Uchiyama Y. Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury. Am J Pathol. 2008;172:454-469.
46. Zhu C, Wang X, Huang Z, Qiu L, Xu F, Vahsen N, Nilsson M, Eriksson PS, Hagberg H, Culmsee C, Plesnila N, Kroemer G, Blomgren K. Apoptosis-inducing factor is a major contributor to neuronal loss induced by neonatal cerebral hypoxia-ischemia. Cell Death Differ. 2007;14:775-784.
47. Galluzzi L, Blomgren K, Kroemer G. Mitochondrial membrane permeabilization in neuronal injury. Nat Rev Neurosci. 2009;10:481-494.
48. Dimlich RV, Kaplan J, Timerding BL, Van Ligten PF. Effects of various doses of sodium dichloroacetate on hyperlactatemia in fed ischemic rats. Ann Emerg Med. 1989;18:1162-1171.
49. Kaufmann P, Engelstad K, Wei Y, Jhung S, Sano MC, Shungu DC, Millar WS, Hong X, Gooch CL, Mao X, Pascual JM, Hirano M, Stacpoole PW, et al. Dichloroacetate causes toxic neuropathy in MELAS: a randomized, controlled clinical trial. Neurology. 2006;66:324-330.
50. Han W, Sun Y, Wang X, Zhu C, Blomgren K. Delayed, long-term administration of the caspase inhibitor Q-VDOPh reduced brain injury induced by neonatal hypoxiaischemia. Dev Neurosci. 2014;36:64-72.
51. Li H, Li Q, Du X, Sun Y, Wang X, Kroemer G, Blomgren K, Zhu C. Lithium-mediated long-term neuroprotection in neonatal rat hypoxia-ischemia is associated with antiinflammatory effects and enhanced proliferation and survival of neural stem/progenitor cells. J Cereb Blood Flow Metab. 2011;31:2106-15.
52. Gubern C, Hurtado O, Rodriguez R, Morales JR, Romera VG, Moro MA, Lizasoain I, Serena J and Mallolas J. Validation of housekeeping genes for quantitative real-time PCR in in-vivo and in-vitro models of cerebral ischaemia. BMC Mol Biol. 2009;10:57.