Targeting the mitochondrial electron transport chain in autism, a systematic review and synthesis of a novel therapeutic approach

Mitochondrion

Volumn 13, Issue 5, 2013, Pages 515-519

  Ghanizadeh, Ahmad ^a,b   Berk, Michael ^c,d   Farrashbandi, Hassan ^a,b   Alavi shoushtari, Ali ^a,b   Villagonzalo, Kristi Ann ^c  

^a SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b SHIRAZ UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c DEAKIN UNIVERSITY   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Autism; Energy; Etiology; Mitochondria; Oxidative stress; Treatment

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ADENOSINE TRIPHOSPHATE; APYRASE; CREATINE KINASE; CYTOCHROME C; CYTOCHROME C OXIDASE; LACTIC ACID; METHYLENE BLUE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); SUPEROXIDE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANTIOXIDANT ACTIVITY; ARTICLE; AUTISM; CASE CONTROL STUDY; CLINICAL TRIAL (TOPIC); DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG TARGETING; ENZYME DEFICIENCY; HUMAN; MITOCHONDRIAL ENERGY TRANSFER; OXIDATIVE STRESS; PRIORITY JOURNAL; SYSTEMATIC REVIEW;

AUTISM; ENERGY; ETIOLOGY; MITOCHONDRIA; OXIDATIVE STRESS; TREATMENT;

ADENOSINE TRIPHOSPHATE; AUTISTIC DISORDER; ELECTRON TRANSPORT; HUMANS; MITOCHONDRIA; REACTIVE OXYGEN SPECIES;

EID: 84882830603     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.10.001     Document Type: Article

References (60)

1. Aksenov V., Long J., Liu J., Szechtman H., Khanna P., Matravadia S., Rollo C.D. A complex dietary supplement augments spatial learning, brain mass, and mitochondrial electron transport chain activity in aging mice. Age (Dordr.) 2011, (Electronic publication ahead of print).
2. Al-Mosalem O.A., El-Ansary A., Attas O., Al-Ayadhi L. Metabolic biomarkers related to energy metabolism in Saudi autistic children. Clin. Biochem. 2009, 42:949-957.
3. Andreazza A.C., Shao L., Wang J.F., Young L.T. Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch. Gen. Psychiatry 2010, 67:360-368.
4. Atamna H., Nguyen A., Schultz C., Boyle K., Newberry J., Kato H., Ames B.N. Methylene blue delays cellular senescence and enhances key mitochondrial biochemical pathways. FASEB J. 2008, 22:703-712.
5. Berger G., Dell'Olio M., Amminger P., Cornblatt B., Phillips L., Yung A., Yan Y., Berk M., McGorry P. Neuroprotection in emerging psychotic disorders. Early Interv. Psychiatry 2007, 1:114-127.
6. Berk M. Neuroprogression: pathways to progressive brain changes in bipolar disorder. Int. J. Neuropsychopharmacol. 2009, 12:441-445.
7. Berk M., Hallam K., Lucas N., Hasty M., McNeil C.A., Conus P., Kader L., McGorry P.D. Early intervention in bipolar disorders: opportunities and pitfalls. Med. J. Aust. 2007, 187:S11-S14.
8. Blanchet L., Buydens M.C., Smeitink J.A., Willems P.H., Koopman W.J. Isolated mitochondrial complex I deficiency: explorative data analysis of patient cell parameters. Curr. Pharm. Des. 2011, 17:4023-4033.
9. Boveris A., Costa L.E., Poderoso J.J., Carreras M.C., Cadenas E. Regulation of mitochondrial respiration by oxygen and nitric oxide. Ann. N. Y. Acad. Sci. 2000, 899:121-135.
10. Callaway N.L., Riha P.D., Bruchey A.K., Munshi Z., Gonzalez-Lima F. Methylene blue improves brain oxidative metabolism and memory retention in rats. Pharmacol. Biochem. Behav. 2004, 77:175-181.
11. Chance B., Williams G.R. Respiratory enzymes in oxidative phosphorylation. IV. The respiratory chain. J. Biol. Chem. 1955, 217:429-438.
12. Chance B., Williams G.R. The respiratory chain and oxidative phosphorylation. Adv. Enzymol. Relat. Subj. Biochem. 1956, 17:65-134.
13. Chauhan A., Gu F., Essa M.M., Wegiel J., Kaur K., Brown W.T., Chauhan V. Brain region-specific deficit in mitochondrial electron transport chain complexes in children with autism. J. Neurochem. 2011, 117:209-220.
14. 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. J. Biol. Chem. 2003, 278:36027-36031.
15. Chugani D.C., Sundram B.S., Behen M., Lee M.L., Moore G.J. Evidence of altered energy metabolism in autistic children. Prog. Neuropsychopharmacol. Biol. Psychiatry 1999, 23:635-641.
16. Craig A.K., de Menezes M.S., Saneto R.P. Dravet syndrome: patients with co-morbid SCN1A gene mutations and mitochondrial electron transport chain defects. Seizure 2012, 21:17-20.
17. Dean O., Giorlando F., Berk M. N-Acetylcysteine in psychiatry: current therapeutic evidence and potential mechanisms of action. J. Psychiatry Neurosci. 2011, 36:78-86.
18. Ezugha H., Goldenthal M., Valencia I., Anderson C.E., Legido A., Marks H. 5q14.3 deletion manifesting as mitochondrial disease and autism: case report. J. Child Neurol. 2010, 25:1232-1235.
19. Filipek P.A., Juranek J., Smith M., Mays L.Z., Ramos E.R., Bocian M., Masser-Frye D., Laulhere T.M., Modahl C., Spence M.A., Gargus J.J. Mitochondrial dysfunction in autistic patients with 15q inverted duplication. Ann. Neurol. 2003, 53:801-804.
20. Frye R.E. Mitochondrial disease in 22q13 duplication syndrome. J. Child Neurol. 2012, 27(7):942-949.
21. Gandhi S., Wood N.W. Molecular pathogenesis of Parkinson's disease. Hum. Mol. Genet. 2005, 14:2749-2755.
22. Ghanizadeh, A., Derakhshan, N., under press. N-Acetylcysteine for treatment of autism, a case report. J. Res. Med. Sci.
23. Ghanizadeh A., Akhondzadeh S., Hormozi M., Makarem A., Abotorabi-Zarchi M., Firoozabadi A. Glutathione-related factors and oxidative stress in autism, a review. Curr. Med. Chem. 2012, 19:4000-4005.
24. Giulivi C., Zhang Y.F., Omanska-Klusek A., Ross-Inta C., Wong S., Hertz-Picciotto I., Tassone F., Pessah I.N. Mitochondrial dysfunction in autism. JAMA 2010, 304:2389-2396.
25. Giulivi C., Zhang Y.F., Omanska-Klusek A., Ross-Inta C., Wong S., Hertz-Picciotto I., Tassone F., Pessah I.N. Mitochondrial dysfunction in autism. JAMA 2012, 304:2389-2396.
26. Grivennikova V.G., Vinogradov A.D. Generation of superoxide by the mitochondrial complex I. Biochim. Biophys. Acta 2006, 1757:553-561.
27. Guevara-Campos J., Gonzalez-Guevara L., Briones P., Lopez-Gallardo E., Bulan N., Ruiz-Pesini E., Ramnarine D., Montoya J. Autism associated to a deficiency of complexes III and IV of the mitochondrial respiratory chain. Invest. Clin. 2010, 51:423-431.
28. Haas R.H. Autism and mitochondrial disease. Dev. Disabil. Res. Rev. 2010, 16:144-153.
29. Hardan A.Y., Fung L.K., Libove R.A., Obukhanych T.V., Nair S., Herzenberg L.A., Frazier T.W., Tirouvanziam R. A randomized controlled pilot trial of oral N-acetylcysteine in children with autism. Biol. Psychiatry 2012, 71:956-961.
30. Jastroch M., Divakaruni A.S., Mookerjee S., Treberg J.R., Brand M.D. Mitochondrial proton and electron leaks. Essays Biochem. 2010, 47:53-67.
31. Kelner M.J., Bagnell R., Hale B., Alexander N.M. Potential of methylene blue to block oxygen radical generation in reperfusion injury. Basic Life Sci. 1988, 49:895-898.
32. Kudin A.P., Malinska D., Kunz W.S. Sites of generation of reactive oxygen species in homogenates of brain tissue determined with the use of respiratory substrates and inhibitors. Biochim. Biophys. Acta 2008, 1777:689-695.
33. Looney J.M., Childs H.M. The lactic acid and glutathione content of the blood of schizophrenic patients. J. Clin. Invest. 1934, 13:963-968.
34. Malinska D., Kulawiak B., Kudin A.P., Kovacs R., Huchzermeyer C., Kann O., Szewczyk A., Kunz W.S. Complex III-dependent superoxide production of brain mitochondria contributes to seizure-related ROS formation. Biochim. Biophys. Acta 2010, 1797:1163-1170.
35. Mimaki M., Wang X., McKenzie M., Thorburn D.R., Ryan M.T. Understanding mitochondrial complex I assembly in health and disease. Biochim. Biophys. Acta 2012, 1817(6):851-862.
36. Naylor G.J., Martin B., Hopwood S.E., Watson Y. A two-year double-blind crossover trial of the prophylactic effect of methylene blue in manic-depressive psychosis. Biol. Psychiatry 1986, 21:915-920.
37. Nierenberg A.A., Kansky C., Brennan B.P., Shelton R.C., Perlis R., Iosifescu D.V. Mitochondrial modulators for bipolar disorder: a pathophysiologically informed paradigm for new drug development. Aust. N. Z. J. Psychiatry 2013, 47(1):26-42.
38. Oliveira G., Diogo L., Grazina M., Garcia P., Ataide A., Marques C., Miguel T., Borges L., Vicente A.M., Oliveira C.R. Mitochondrial dysfunction in autism spectrum disorders: a population-based study. Dev. Med. Child Neurol. 2005, 47:185-189.
39. Oz M., Lorke D.E., Petroianu G.A. Methylene blue and Alzheimer's disease. Biochem. Pharmacol. 2009, 78:927-932.
40. Peter C., Hongwan D., Kupfer A., Lauterburg B.H. Pharmacokinetics and organ distribution of intravenous and oral methylene blue. Eur. J. Clin. Pharmacol. 2000, 56:247-250.
41. Poling J.S., Frye R.E., Shoffner J., Zimmerman A.W. Developmental regression and mitochondrial dysfunction in a child with autism. J. Child Neurol. 2006, 21:170-172.
42. Riha P.D., Bruchey A.K., Echevarria D.J., Gonzalez-Lima F. Memory facilitation by methylene blue: dose-dependent effect on behavior and brain oxygen consumption. Eur. J. Pharmacol. 2005, 511:151-158.
43. Rojas J.C., Bruchey A.K., Gonzalez-Lima F. Neurometabolic mechanisms for memory enhancement and neuroprotection of methylene blue. Prog. Neurobiol. 2011, 96:32-45.
44. Rossignol D.A., Frye R.E. A review of research trends in physiological abnormalities in autism spectrum disorders: immune dysregulation, inflammation, oxidative stress, mitochondrial dysfunction and environmental toxicant exposures. Mol. Psychiatry 2012, 17(4):389-401.
45. Salaris S.C., Babbs C.F., Voorhees W.D. Methylene blue as an inhibitor of superoxide generation by xanthine oxidase. A potential new drug for the attenuation of ischemia/reperfusion injury. Biochem. Pharmacol. 1991, 42:499-506.
46. Sandhir R., Sood A., Mehrotra A., Kamboj S.S. N-Acetylcysteine reverses mitochondrial dysfunctions and behavioral abnormalities in 3-nitropropionic acid-induced Huntington's disease. Neurodegener Dis 2012, 9:145-157.
47. Schonfeld P., Wojtczak L. Fatty acids decrease mitochondrial generation of reactive oxygen species at the reverse electron transport but increase it at the forward transport. Biochim. Biophys. Acta 2007, 1767:1032-1040.
48. Selivanov V.A., Votyakova T.V., Pivtoraiko V.N., Zeak J., Sukhomlin T., Trucco M., Roca J., Cascante M. Reactive oxygen species production by forward and reverse electron fluxes in the mitochondrial respiratory chain. PLoS Comput. Biol. 2011, 7:e1001115.
49. Sills M.R., Zinkham W.H. Methylene blue-induced Heinz body hemolytic anemia. Arch. Pediatr. Adolesc. Med. 1994, 148:306-310.
50. Skulachev V.P. A biochemical approach to the problem of aging: "megaproject" on membrane-penetrating ions. The first results and prospects. Biochemistry (Mosc.) 2007, 72:1385-1396.
51. - generation in reduction and oxidation cycle of ubiquinones in a model of mitochondrial electron transport systems. Biochim. Biophys. Acta 1988, 936:377-385.
52. Taurines R., Thome J., Duvigneau J.C., Forbes-Robertson S., Yang L., Klampfl K., Romanos J., Muller S., Gerlach M., Mehler-Wex C. Expression analyses of the mitochondrial complex I 75-kDa subunit in early onset schizophrenia and autism spectrum disorder: increased levels as a potential biomarker for early onset schizophrenia. Eur. Child Adolesc. Psychiatry 2010, 19:441-448.
53. Turrens J.F. Superoxide production by the mitochondrial respiratory chain. Biosci. Rep. 1997, 17:3-8.
54. Turrens J.F. Mitochondrial formation of reactive oxygen species. J. Physiol. 2003, 552:335-344.
55. Villagonzalo K.A., Dodd S., Dean O., Gray K., Tonge B., Berk M. Oxidative pathways as a drug target for the treatment of autism. Expert Opin. Ther. Targets 2010, 14:1301-1310.
56. Vinogradov A.D., Grivennikova V.G. Generation of superoxide-radical by the NADH:ubiquinone oxidoreductase of heart mitochondria. Biochemistry (Mosc.) 2005, 70:120-127.
57. Visarius T.M., Stucki J.W., Lauterburg B.H. Stimulation of respiration by methylene blue in rat liver mitochondria. FEBS Lett. 1997, 412:157-160.
58. Weissman J.R., Kelley R.I., Bauman M.L., Cohen B.H., Murray K.F., Mitchell R.L., Kern R.L., Natowicz M.R. Mitochondrial disease in autism spectrum disorder patients: a cohort analysis. PLoS One 2008, 3:e3815.
59. Wen Y., Li W., Poteet E.C., Xie L., Tan C., Yan L.J., Ju X., Liu R., Qian H., Marvin M.A., Goldberg M.S., She H., Mao Z., Simpkins J.W., Yang S.H. Alternative mitochondrial electron transfer as a novel strategy for neuroprotection. J. Biol. Chem. 2011, 286:16504-16515.
60. Zoroglu S.S., Armutcu F., Ozen S., Gurel A., Sivasli E., Yetkin O., Meram I. Increased oxidative stress and altered activities of erythrocyte free radical scavenging enzymes in autism. Eur. Arch. Psychiatry Clin. Neurosci. 2004, 254:143-147.