Mitochondrial superoxide contributes to hippocampal synaptic dysfunction and memory deficits in Angelman syndrome model mice

Journal of Neuroscience

Volumn 35, Issue 49, 2015, Pages 16213-16220

  Santini, Emanuela ^a   Turner, Kathryn L ^a   Ramaraj, Xakila B ^a   Murphy, Michael P ^b   Klann, Eric ^a   Kaphzan, Xhanoch ^a,c  

^a NEW YORK UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF HAIFA   (Israel)

Author keywords

Hippocampus; Memory; Mitochondria; Neurodevelopmental disorders; Oxidative stress; Synpatic plasticity

Indexed keywords

MESYLIC ACID; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; 10-(6'-UBIQUINONYL)DECYLTRIPHENYLPHOSPHONIUM BROMIDE; ORGANOPHOSPHORUS COMPOUND; UBIQUINONE;

ADULT; AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOCHEMICAL ANALYSIS; BRAIN ELECTROPHYSIOLOGY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; FEAR; FEMALE; HAPPY PUPPET SYNDROME; HIPPOCAMPAL CA1 REGION; MALE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; ROTAROD TEST; ANALOGS AND DERIVATIVES; ANALYSIS OF VARIANCE; ANIMAL; C57BL MOUSE; COMPLICATION; CONDITIONING; DISEASE MODEL; ELECTROSTIMULATION; HIPPOCAMPUS; IN VITRO STUDY; METABOLISM; MITOCHONDRION; MOTOR ACTIVITY; MOVEMENT DISORDERS; PATHOLOGY; PHYSIOLOGY; SYNAPSE; ULTRASTRUCTURE;

ANALYSIS OF VARIANCE; ANGELMAN SYNDROME; ANIMALS; CONDITIONING (PSYCHOLOGY); DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION; FEAR; HIPPOCAMPUS; IN VITRO TECHNIQUES; MICE; MICE, INBRED C57BL; MITOCHONDRIA; MOTOR ACTIVITY; MOVEMENT DISORDERS; ORGANOPHOSPHORUS COMPOUNDS; SUPEROXIDES; SYNAPSES; UBIQUINONE;

EID: 84949591430     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2246-15.2015     Document Type: Article

References (41)

1. Aksenov MY, Tucker HM, Nair P, Aksenova MV, Butterfield DA, Estus S, Markesbery WR (1998) The expression of key oxidative stress-handling genes in different brain regions in Alzheimer’s disease. J Mol Neurosci 11:151–164. CrossRef Medline
2. Anitha A, Nakamura K, Thanseem I, Matsuzaki H, Miyachi T, Tsujii M, Iwata Y, Suzuki K, Sugiyama T, Mori N (2013) Downregulation of the expression of mitochondrial electron transport complex genes in autism brains. Brain Pathol 23:294–302. CrossRef Medline
3. Boveris A, Chance B (1973) The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134:707–716. CrossRef Medline
4. Braam W, Didden R, Smits MG, Curfs LM (2008) Melatonin for chronic insomnia in Angelman syndrome: a randomized placebo-controlled trial. J Child Neurol 23:649–654. CrossRef Medline
5. Cadenas E, Boveris A, Ragan CI, Stoppani AO (1977) Production of superoxide radicals and hydrogen peroxide by NADH-ubiquinone reductase and ubiquinol-cytochrome c reductase from beef-heart mitochondria. Arch Biochem Biophys 180:248–257. CrossRef Medline
6. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morton AJ (1999) Characterization of progressive motor deficits in mice transgenic for the human Huntington’s disease mutation. J Neurosci 19:3248 –3257. Medline
7. Carter RJ, Morton J, Dunnett SB (2001) Motor coordination and balance in rodents. Curr Protoc Neurosci Chapter 8:Unit 8.12. CrossRef Medline
8. Chamberlain SJ, Lalande M (2010) Angelman syndrome, a genomic imprinting disorder of the brain. J Neurosci 30:9958 –9963. CrossRef Medline
9. Chandran K, Aggarwal D, Migrino RQ, Joseph J, McAllister D, Konorev EA, Antholine WE, Zielonka J, Srinivasan S, Avadhani NG, Kalyanaraman B (2009) Doxorubicin inactivates myocardial cytochrome c oxidase in rats: cardioprotection by Mito-Q. Biophys J 96:1388–1398. CrossRef Medline
10. Chauhan A, Chauhan V (2006) Oxidative stress in autism. Pathophysiology 13:171–181. CrossRef Medline
11. Dindot SV, Antalffy BA, Bhattacharjee MB, Beaudet AL (2008) The Angelman syndrome ubiquitin ligase localizes to the synapse and nucleus, and maternal deficiency results in abnormal dendritic spine morphology. Hum Mol Genet 17:111–118. CrossRef Medline
12. Ghosh A, Chandran K, Kalivendi SV, Joseph J, Antholine WE, Hillard CJ, Kanthasamy A, Kanthasamy A, Kalyanaraman B (2010) Neuroprotection by a mitochondria-targeted drug in a Parkinson’s disease model. Free Radic Biol Med 49:1674 –1684. CrossRef Medline
13. Gu F, Chauhan V, Kaur K, Brown WT, LaFauci G, Wegiel J, Chauhan A (2013) Alterations in mitochondrial DNA copy number and the activities of electron transport chain complexes and pyruvate dehydrogenase in the frontal cortex from subjects with autism. Transl Psychiatry 3:e299. CrossRef Medline
14. Gustin RM, Bichell TJ, Bubser M, Daily J, Filonova I, Mrelashvili D, Deutch AY, Colbran RJ, Weeber EJ, Haas KF (2010) Tissue-specific variation of Ube3a protein expression in rodents and in a mouse model of Angelman syndrome. Neurobiol Dis 39:283–291. CrossRef Medline
15. Hu D, Serrano F, Oury TD, Klann E (2006) Aging-dependent alterations in synaptic plasticity and memory in mice that overexpress extracellular superoxide dismutase. J Neurosci 26:3933–3941. CrossRef Medline
16. Hu D, Cao P, Thiels E, Chu CT, Wu GY, Oury TD, Klann E (2007) Hippocampal long-term potentiation, memory, and longevity in mice that overexpress mitochondrial superoxide dismutase. Neurobiol Learn Mem 87:372–384. CrossRef Medline
17. Jiang YH, Armstrong D, Albrecht U, Atkins CM, Noebels JL, Eichele G, Sweatt JD, Beaudet AL (1998) Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21:799–811. CrossRef Medline
18. Kaphzan H, Hernandez P, Jung JI, Cowansage KK, Deinhardt K, Chao MV, Abel T, Klann E (2012) Reversal of impaired hippocampal long-term potentiation and contextual fear memory deficits in Angelman syndrome model mice by ErbB inhibitors. Biol Psychiatry 72:182–190. CrossRef Medline
19. Kaphzan H, Buffington SA, Ramaraj AB, Lingrel JB, Rasband MN, Santini E, Klann E (2013) Genetic reduction of the _1 subunit of Na/K-ATPase corrects multiple hippocampal phenotypes in Angelman syndrome. Cell Rep 4:405–412. CrossRef Medline
20. Kern JK, Jones AM (2006) Evidence of toxicity, oxidative stress, and neuronal insult in autism. J Toxicol Environ Health B Crit Rev 9:485– 499. CrossRef Medline
21. Kishino T, Lalande M, Wagstaff J (1997) UBE3A/E6-AP mutations cause Angelman syndrome. Nat Genet 15:70 –73. CrossRef Medline
22. Klann E (1998) Cell-permeable scavengers of superoxide prevent long-term potentiation in hippocampal area CA1. J Neurophysiol 80:452– 457. Medline
23. Klann E, Roberson ED, Knapp LT, Sweatt JD (1998) Arole for superoxide in protein kinase C activation and induction of long-term potentiation. J Biol Chem 273:4516–4522. CrossRef Medline
24. Knoll JH, Nicholls RD, Magenis RE, Graham JM Jr, Lalande M, Latt SA (1989) Angelman and Prader-Willi syndromes share a common chromosome 15 deletion but differ in parental origin of the deletion. Am J Med Genet 32:285–290. CrossRef Medline
25. Lossie AC, Whitney MM, Amidon D, Dong HJ, Chen P, Theriaque D, Hutson A, Nicholls RD, Zori RT, Williams CA, Driscoll DJ (2001) Distinct phenotypes distinguish the molecular classes of Angelman syndrome. J Med Genet 38:834–845. CrossRef Medline
26. Ma T, Hoeffer CA, Wong H, Massaad CA, Zhou P, Iadecola C, Murphy MP, Pautler RG, Klann E (2011) Amyloid _-induced impairments in hippocampal synaptic plasticity are rescued by decreasing mitochondrial superoxide. J Neurosci 31:5589 –5595. CrossRef Medline
27. Massaad CA, Pautler RG, Klann E (2009) Mitochondrial superoxide: a key player in Alzheimer’s disease. Aging (Albany NY) 1:758 –761. Medline
28. Matsuura T, Sutcliffe JS, Fang P, Galjaard RJ, Jiang YH, Benton CS, Rommens JM, Beaudet AL (1997) De novo truncating mutations in E6-AP ubiquitin-protein ligase gene (UBE3A) in Angelman syndrome. Nat Genet 15:74 –77. CrossRef Medline
29. McManus MJ, Murphy MP, Franklin JL (2011) The mitochondria-targeted antioxidant MitoQ prevents loss of spatial memory retention and early neuropathology in a transgenic mouse model of Alzheimer’s disease. J Neurosci 31:15703–15715. CrossRef Medline
30. Schlanger S, Shinitzky M, Yam D (2002) Diet enriched with omega-3 fatty acids alleviates convulsion symptoms in epilepsy patients. Epilepsia 43: 103–104. CrossRef Medline
31. Silva-Santos S, van Woerden GM, Bruinsma CF, Mientjes E, Jolfaei MA, Distel B, Kushner SA, Elgersma Y (2015) Ube3a reinstatement identifies distinct developmental windows in a murine Angelman syndrome model. J Clin Invest 125:2069 –2076. CrossRef Medline
32. Smith RAJ, Murphy MP (2010) Animal and human studies with the mitochondria-targeted antioxidant MitoQ. Ann N Y Acad Sci 1201:96– 103. CrossRef Medline
33. Smith RA, Porteous CM, Gane AM, Murphy MP (2003) Delivery of bioactive molecules to mitochondria in vivo. Proc Natl Acad Sci U S A 100: 5407–5412. CrossRef Medline
34. Snow BJ, Rolfe FL, Lockhart MM, Frampton CM, O’Sullivan JD, Fung V, Smith RA, Murphy MP, Taylor KM, Protect Study Group (2010) A double-blind, placebo-controlled study to assess the mitochondriatargeted antioxidant MitoQ as a disease-modifying therapy in Parkinson’s disease. Mov Disord 25:1670 –1674. CrossRef Medline
35. Su H, Fan W, Coskun PE, Vesa J, Gold JA, Jiang YH, Potluri P, Procaccio V, Acab A, Weiss JH, Wallace DC, Kimonis VE (2011) Mitochondrial dysfunction in CA1 hippocampal neurons of the UBE3A deficient mouse model for Angelman syndrome. Neurosci Lett 487:129 –133. CrossRef Medline
36. Sutcliffe JS, Jiang YH, Galijaard RJ, Matsuura T, Fang P, Kubota T, Christian SL, Bressler J, Cattanach B, Ledbetter DH, Beaudet AL (1997) TheE6-Ap ubiquitin-protein ligase (UBE3A) gene is localized within a narrowed Angelman syndrome critical region. Genome Res 7:368–377. Medline
37. Thiels E, Urban NN, Gonzalez-Burgos GR, Kanterewicz BI, Barrionuevo G, Chu CT, Oury TD, Klann E (2000) Impairment of long-term potentiation and associative memory in mice that overexpress extracellular superoxide dismutase. J Neurosci 20:7631–7639. Medline
38. Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552:335–344. CrossRef Medline
39. van Woerden GM, Harris KD, Hojjati MR, Gustin RM, Qiu S, de Avila Freire R, Jiang YH, Elgersma Y, Weeber EJ (2007) Rescue of neurological deficits in a mouse model for Angelman syndrome by reduction of alphaCaMKII inhibitory phosphorylation. Nat Neurosci 10:280 –282. CrossRef Medline
40. Williams CA, Beaudet AL, Clayton-Smith J, Knoll JH, Kyllerman M, Laan LA, Magenis RE, Moncla A, Schinzel AA, Summers JA, Wagstaff J (2006) Angelman syndrome 2005: updated consensus for diagnostic criteria. Am J Med Genet 140:413– 418. CrossRef Medline
41. Zhdanova IV, Wurtman RJ, Wagstaff J (1999) Effects of a low dose of melatonin on sleep in children with Angelman syndrome. J Pediatr Endocrinol Metab 12:57– 67. Medline