Evidence of reactive oxygen species-mediated damage to mitochondrial DNA in children with typical autism

Molecular Autism

Volumn 4, Issue 1, 2013, Pages

  Napoli, Eleonora ^a   Wong, Sarah ^a   Giulivi, Cecilia ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Autism; Bioenergetics; Mitochondria; Mitochondrial DNA; Oxidative damage

Indexed keywords

APURINIC ACID; DNA DIRECTED DNA POLYMERASE GAMMA; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE;

ARTICLE; AUTISM; CELL ISOLATION; CHILD; CHILD DEVELOPMENT; CONTROLLED STUDY; DNA DAMAGE; FATHER; FEMALE; GENE DELETION; GENE FREQUENCY; GENE SEQUENCE; HUMAN; INHERITANCE; MAJOR CLINICAL STUDY; MALE; MITOCHONDRIAL GENOME; MOTHER; NUCLEOTIDE SEQUENCE; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PERIPHERAL BLOOD MONONUCLEAR CELL; PRESCHOOL CHILD; PRIORITY JOURNAL; RISK FACTOR;

EID: 84873622303     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/2040-2392-4-2     Document Type: Article

References (68)

1. The role of mitochondrial glutathione in DNA base oxidation. Giulivi C, Cadenas E, Biochim Biophys Acta 1998 1366 265 274 10.1016/S0005-2728(98)00125-X 9814840 (Pubitemid 29164400)
2. The steady-state concentrations of oxygen radicals in mitochondria. Giulivi C, Boveris A, Cadenas E, Reactive Oxygen Species in Biological Systems: An Interdisciplinary Approach. Volume 77 Colton: Kluwer Academic/Plenum Publishers, Gilbert DL, 1997 77 102
3. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Lin MT, Beal MF, Nature 2006 443 787 795 10.1038/nature05292 17051205 (Pubitemid 44622683)
4. Nuclear genes in mitochondrial disorders. Zeviani M, Spinazzola A, Carelli V, Curr Opin Genet Dev 2003 13 262 270 10.1016/S0959-437X(03)00052-2 12787788 (Pubitemid 36645089)
5. Mitochondrial dysfunction and oxidative stress in aging and neurodegenerative disease. Albers DS, Beal MF, J Neural Transm Suppl 2000 59 133 154 10961426 (Pubitemid 30479414)
6. Mitochondrial DNA 4977 bp deletion and OH8dG levels correlate in the brain of aged subjects but not Alzheimer's disease patients. Lezza AMS, Mecocci P, Cormio A, Beal MF, Cherubini A, Cantatore P, Senin U, Gadaleta MN, FASEB J 1999 13 1083 1088 10336891 (Pubitemid 29249734)
7. Mutagenesis by metal-induced oxygen radicals. Reid TM, Feig DI, Loeb LA, Environ Health Perspect 1994 102 Suppl 3 57 61 10.1289/ehp.94102s357 7705307 (Pubitemid 24316360)
8. Oxidized, deaminated cytosines are a source of C -> T transitions in vivo. Kreutzer DA, Essigmann JM, Proc Natl Acad Sci USA 1998 95 3578 3582 10.1073/pnas.95.7.3578 9520408 (Pubitemid 28173170)
9. Mitochondrial mutational spectra in human cells and tissues. Khrapko K, Coller HA, Andre PC, Li XC, Hanekamp JS, Thilly WG, Proc Natl Acad Sci USA 1997 94 13798 13803 10.1073/pnas.94.25.13798 9391107 (Pubitemid 28009664)
10. Repair of oxidative damage to nuclear and mitochondrial DNA in mammalian cells. Croteau DL, Bohr VA, J Biol Chem 1997 272 25409 25412 10.1074/jbc.272.41.25409 9325246 (Pubitemid 27438839)
11. Oxidative decay of DNA. Beckman KB, Ames BN, J Biol Chem 1997 272 19633 19636 10.1074/jbc.272.32.19633 9289489 (Pubitemid 27340047)
12. Random mtDNA deletions and functional consequence in aged human skeletal muscle. Chabi B, Mousson de Camaret B, Chevrollier A, Boisgard S, Stepien G, Biochem Biophys Res Commun 2005 332 542 549 10.1016/j.bbrc.2005.04.153 15896715 (Pubitemid 40725010)
13. Double-strand breaks of mouse muscle mtDNA promote large deletions similar to multiple mtDNA deletions in humans. Srivastava S, Moraes CT, Hum Mol Genet 2005 14 893 902 10.1093/hmg/ddi082 15703189 (Pubitemid 40533100)
14. Instability and decay of the primary structure of DNA. Lindahl T, Nature 1993 362 709 715 10.1038/362709a0 8469282 (Pubitemid 23125973)
15. Mitochondrial dysfunction in autism. Giulivi C, Zhang YF, Omanska-Klusek A, Ross-Inta C, Wong S, Hertz-Picciotto I, Tassone F, Pessah IN, JAMA 2010 304 2389 2396 10.1001/jama.2010.1706 21119085
16. Brain region-specific glutathione redox imbalance in autism. Chauhan A, Audhya T, Chauhan V, Neurochem Res 2012 37 1681 1689 10.1007/s11064-012-0775-4 22528835
17. Evidence of oxidative stress in autism derived from animal models. Ming X, Cheh MA, Yochum CL, Halladay AK, Wagner GC, Am J Biochem Biotechnol 2008 4 218 225 (Pubitemid 351573655)
18. Mitochondrial dysfunction in Pten haplo-insufficient mice with social deficits and repetitive behavior: interplay between Pten and p53. Napoli E, Ross-Inta C, Wong S, Hung C, Fujisawa Y, Sakaguchi D, Angelastro J, Omanska-Klusek A, Schoenfeld R, Giulivi C, PLoS One 2012 7 42504 10.1371/journal.pone.0042504 22900024
19. Cellular and mitochondrial glutathione redox imbalance in lymphoblastoid cells derived from children with autism. James SJ, Rose S, Melnyk S, Jernigan S, Blossom S, Pavliv O, Gaylor DW, FASEB J 2009 23 2374 2383 10.1096/fj.08-128926 19307255
20. Efficacy of methylcobalamin and folinic acid treatment on glutathione redox status in children with autism. James SJ, Melnyk S, Fuchs G, Reid T, Jernigan S, Pavliv O, Hubanks A, Gaylor DW, Am J Clin Nutr 2009 89 425 430 19056591
21. Biomarkers of environmental toxicity and susceptibility in autism. Geier DA, Kern JK, Garver CR, Adams JB, Audhya T, Nataf R, Geier MR, J Neurol Sci 2009 280 101 108 10.1016/j.jns.2008.08.021 18817931
22. Genetic variant of glutathione peroxidase 1 in autism. Ming X, Johnson WG, Stenroos ES, Mars A, Lambert GH, Buyske S, Brain Dev 2010 32 105 109 10.1016/j.braindev.2008.12.017 19195803
23. The CHARGE study: an epidemiologic investigation of genetic and environmental factors contributing to autism. Hertz-Picciotto I, Croen LA, Hansen R, Jones CR, van de Water J, Pessah IN, Environ Health Perspect 2006 114 1119 1125 10.1289/ehp.8483 16835068 (Pubitemid 44018911)
24. Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Lord C, Rutter M, Le Couteur A, J Autism Dev Disord 1994 24 659 685 10.1007/BF02172145 7814313 (Pubitemid 24309810)
25. The autism diagnostic observation schedule-generic: a standard measure of social and communication deficits associated with the spectrum of autism. Lord C, Risi S, Lambrecht L, Cook EH Jr, Leventhal BL, DiLavore PC, Pickles A, Rutter M, J Autism Dev Disord 2000 30 205 223 10.1023/A:1005592401947 11055457
26. Association AP, Diagnostic and statistical manual of mental disorders DSM-IV-TR (text revision) Washington, DC: American Psychiatric Press 4 2000
27. Mullen EM, Mullen Scales of Early Learning Circle Pines, MN: American Guidance Service 1995
28. Diagnostic uses of the vineland adaptive behavior scales. Sparrow SS, Cicchetti DV, J Pediatr Psychol 1985 10 215 225 10.1093/jpepsy/10.2.215 4020603
29. Declaration of Helsinki: ethical principles for medical research involving human subjects. World Medical Association, J Postgrad Med [serial online] 2002 48 3 206 208 http://www.jpgmonline.com/text.asp?2002/48/3/206/103 [cited 2013 Jan 22]
30. Co-amplification of nuclear pseudogenes and assessment of heteroplasmy of mitochondrial DNA mutations. Parfait B, Rustin P, Munnich A, Rotig A, Biochem Biophys Res Commun 1998 247 57 59 10.1006/bbrc.1998.8666 9636653 (Pubitemid 28412524)
31. MITOMAP: a human mitochondrial genome database-2004 update. Brandon MC, Lott MT, Nguyen KC, Spolim S, Navathe SB, Baldi P, Wallace DC, Nucleic Acids Res 2005 33 611 D613 10.1093/nar/gki399 15608272 (Pubitemid 44529995)
32. mtDB: Human Mitochondrial Genome Database, a resource for population genetics and medical sciences. Ingman M, Gyllensten U, Nucleic Acids Res 2006 34 749 D751 10.1093/nar/gkj010 16381973
33. The determination of complete human mitochondrial DNA sequences in single cells: implications for the study of somatic mitochondrial DNA point mutations. Taylor RW, Taylor GA, Durham SE, Turnbull DM, Nucleic Acids Res 2001 29 74 74 10.1093/nar/29.15.e74 11470889
34. Detection and quantification of mitochondrial DNA deletions in individual cells by real-time PCR. He L, Chinnery PF, Durham SE, Blakely EL, Wardell TM, Borthwick GM, Taylor RW, Turnbull DM, Nucleic Acids Res 2002 30 68 10.1093/nar/gnf067 12136116
35. Quantitation of age-related mitochondrial DNA deletions in rat tissues shows that their pattern of accumulation differs from that of humans. Yowe DL, Ames BN, Gene 1998 209 23 30 10.1016/S0378-1119(97)00628-8 9524209 (Pubitemid 28149615)
36. Variation in mutation dynamics across the maize genome as a function of regional and flanking base composition. Morton BR, Bi IV, McMullen MD, Gaut BS, Genetics 2006 172 569 577 16219784 (Pubitemid 43345516)
37. The influence of neighboring-nucleotide composition on single nucleotide polymorphisms (SNPs) in the mouse genome and its comparison with human SNPs. Zhang F, Zhao Z, Genomics 2004 84 785 795 10.1016/j.ygeno.2004.06.015 15475257 (Pubitemid 39314438)
38. Hydroxyl radical generation during mitochondrial electron transfer and the formation of 8-hydroxydesoxyguanosine in mitochondrial DNA. Giulivi C, Boveris A, Cadenas E, Arch Biochem Biophys 1995 316 909 916 10.1006/abbi.1995. 1122 7864650
39. Markers of oxidative damage to DNA: antioxidants and molecular damage. Loft S, Poulsen HE, Methods Enzymol 1999 300 166 184 9919520
40. Physical and functional interactions between human mitochondrial single-stranded DNA-binding protein and tumour suppressor p53. Wong TS, Rajagopalan S, Townsley FM, Freund SM, Petrovich M, Loakes D, Fersht AR, Nucleic Acids Res 2009 37 568 581 19066201
41. Repair and mutagenic potency of 8-oxoG:A and 8-oxoG:C base pairs in mammalian cells. Le Page F, Guy A, Cadet J, Sarasin A, Gentil A, Nucleic Acids Res 1998 26 1276 1281 10.1093/nar/26.5.1276 9469837 (Pubitemid 28291701)
42. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Shibutani S, Takeshita M, Grollman AP, Nature 1991 349 431 434 10.1038/349431a0 1992344 (Pubitemid 21926107)
43. Mechanistic studies of ionizing radiation and oxidative mutagenesis: genetic effects of a single 8-hydroxyguanine (7-hydro-8-oxoguanine) residue inserted at a unique site in a viral genome. Wood ML, Dizdaroglu M, Gajewski E, Essigmann JM, Biochemistry 1990 29 7024 7032 10.1021/bi00482a011 2223758 (Pubitemid 20241148)
44. Action of mitochondrial DNA polymerase gamma at sites of base loss or oxidative damage. Pinz KG, Shibutani S, Bogenhagen DF, J Biol Chem 1995 270 9202 9206 10.1074/jbc.270.16.9202 7721837
45. Mitochondrial mutagenesis in human cells and tissues. Marcelino LA, Thilly WG, Mutat Res 1999 434 177 203 10.1016/S0921-8777(99)00028-2 10486591 (Pubitemid 29352255)
46. Chemically induced mutations in mitochondrial DNA of human cells: mutational spectrum of N-methyl-N'-nitro-N-nitrosoguanidine. Marcelino LA, Andre PC, Khrapko K, Coller HA, Griffith J, Thilly WG, Cancer Res 1998 58 2857 2862 9661902 (Pubitemid 28311919)
47. Mitochondrial myopathies: clinical and biochemical features of 30 patients with major deletions of muscle mitochondrial DNA. Holt IJ, Harding AE, Cooper JM, Schapira AH, Toscano A, Clark JB, Morgan-Hughes JA, Ann Neurol 1989 26 699 708 10.1002/ana.410260603 2604380 (Pubitemid 20011001)
48. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Cortopassi GA, Shibata D, Soong NW, Arnheim N, Proc Natl Acad Sci USA 1992 89 7370 7374 10.1073/pnas.89.16.7370 1502147
49. Tipping the balance of autism risk: potential mechanisms linking pesticides and autism. Shelton JF, Hertz-Picciotto I, Pessah IN, Environ Health Perspect 2012 120 944 951 10.1289/ehp.1104553 22534084
50. Functional impact of global rare copy number variation in autism spectrum disorders. Pinto D, Pagnamenta AT, Klei L, Anney R, Merico D, Regan R, Conroy J, Magalhaes TR, Correia C, Abrahams BS, et al. Nature 2010 466 368 372 10.1038/nature09146 20531469
51. Early-life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation. Shanks N, Windle RJ, Perks PA, Harbuz MS, Jessop DS, Ingram CD, Lightman SL, Proc Natl Acad Sci USA 2000 97 5645 5650 10.1073/pnas.090571897 10779563 (Pubitemid 30313772)
52. Long-term alterations in neuroimmune responses after neonatal exposure to lipopolysaccharide. Boisse L, Mouihate A, Ellis S, Pittman QJ, J Neurosci 2004 24 4928 4934 10.1523/JNEUROSCI.1077-04.2004 15163684 (Pubitemid 38697825)
53. Early life immune challenge alters innate immune responses to lipopolysaccharide: implications for host defense as adults. Ellis S, Mouihate A, Pittman QJ, FASEB J 2005 19 1519 1521 15972802 (Pubitemid 41279017)
54. Early life immune challenge-effects on behavioural indices of adult rat fear and anxiety. Spencer SJ, Heida JG, Pittman QJ, Behav Brain Res 2005 164 231 238 10.1016/j.bbr.2005.06.032 16125259 (Pubitemid 41337878)
55. Suppression of a mitochondrial tRNA gene mutation phenotype associated with changes in the nuclear background. Hao H, Morrison LE, Moraes CT, Hum Mol Genet 1999 8 1117 1124 10.1093/hmg/8.6.1117 10332045 (Pubitemid 29250901)
56. Molecular neuropathology of MELAS: Level of heteroplasmy in individual neurones and evidence of extensive vascular involvement. Betts J, Jaros E, Perry RH, Schaefer AM, Taylor RW, Abdel-All Z, Lightowlers RN, Turnbull DM, Neuropathol Appl Neurobiol 2006 32 359 373 10.1111/j.1365-2990.2006.00731.x 16866982 (Pubitemid 44015578)
57. Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. Davey GP, Peuchen S, Clark JB, J Biol Chem 1998 273 12753 12757 10.1074/jbc.273.21.12753 9582300 (Pubitemid 28246828)
58. Effects of chronic lead exposure on 1H MRS of hippocampus and frontal lobes in children. Meng XM, Zhu DM, Ruan DY, She JQ, Luo L, Neurology 2005 64 1644 1647 10.1212/01.WNL.0000160391.58004.D4 15883337 (Pubitemid 40617712)
59. Muscle-specific mutations accumulate with aging in critical human mtDNA control sites for replication. Wang Y, Michikawa Y, Mallidis C, Bai Y, Woodhouse L, Yarasheski KE, Miller CA, Askanas V, Engel WK, Bhasin S, Attardi G, Proc Natl Acad Sci USA 2001 98 4022 4027 10.1073/pnas.061013598 11274426 (Pubitemid 32249891)
60. Differential accumulations of 4,977 bp deletion in mitochondrial DNA of various tissues in human ageing. Lee HC, Pang CY, Hsu HS, Wei YH, Biochim Biophys Acta 1994 1226 37 43 10.1016/0925-4439(94)90056-6 8155737 (Pubitemid 24123053)
61. Mitochondrial DNA deletions in human brain: regional variability and increase with advanced age. Corral-Debrinski M, Horton T, Lott MT, Shoffner JM, Beal MF, Wallace DC, Nat Genet 1992 2 324 329 10.1038/ng1292-324 1303288
62. Alzheimer pathology associated with POLG1 mutation, multiple mtDNA deletions, and APOE4/4: premature ageing or just coincidence? Melberg A, Nennesmo I, Moslemi AR, Kollberg G, Luoma P, Suomalainen A, Holme E, Oldfors A, Acta Neuropathol 2005 110 315 316 10.1007/s00401-005-1047-z 15981013 (Pubitemid 41430662)
63. POLG1 p.R722H mutation associated with multiple mtDNA deletions and a neurological phenotype. Komulainen T, Hinttala R, Karppa M, Pajunen L, Finnila S, Tuominen H, Rantala H, Hassinen I, Majamaa K, Uusimaa J, BMC Neurol 2010 10 29 10.1186/1471-2377-10-29 20438629
64. Defective mitochondrial disulfide relay system, altered mitochondrial morphology and function in Huntington's disease. Napoli E, Wong S, Hung C, Ross-Inta C, Bomdica P, Giulivi C, Hum Mol Genet 2012 epub 11/29/2012 10.1093/hmg/dds503
65. Alteration of the copy number and deletion of mitochondrial DNA in human hepatocellular carcinoma. Yin PH, Lee HC, Chau GY, Wu YT, Li SH, Lui WY, Wei YH, Liu TY, Chi CW, Br J Cancer 2004 90 2390 2396 15150555 (Pubitemid 38961905)
66. Prevalence and progression of diabetes in mitochondrial disease. Whittaker RG, Schaefer AM, McFarland R, Taylor RW, Walker M, Turnbull DM, Diabetologia 2007 50 2085 2089 10.1007/s00125-007-0779-9 17653689 (Pubitemid 47373861)
67. Association of mitochondrial antioxidant enzymes with mitochondrial DNA as integral nucleoid constituents. Kienhofer J, Haussler DJ, Ruckelshausen F, Muessig E, Weber K, Pimentel D, Ullrich V, Burkle A, Bachschmid MM, FASEB J 2009 23 2034 2044 10.1096/fj.08-113571 19228881
68. Prenatal vitamins, one-carbon metabolism gene variants, and risk for autism. Schmidt RJ, Hansen RL, Hartiala J, Allayee H, Schmidt LC, Tancredi DJ, Tassone F, Hertz-Picciotto I, Epidemiology 2011 22 476 485 10.1097/EDE. 0b013e31821d0e30 21610500