Mitochondrial DNA (mtDNA) in brain samples from patients with major psychiatric disorders: Gene expression profiles, MtDNA content and presence of the MtDNA common deletion

American Journal of Medical Genetics, Part B: Neuropsychiatric Genetics

Volumn 162, Issue 2, 2013, Pages 213-223

  Torrell, Helena ^a   Montaña, Elena ^a   Abasolo, Nerea ^a   Roig, Bàrbara ^a   Gaviria, Ana M ^a   Vilella, Elisabet ^a   Martorell, Lourdes ^a  

^a IISPV   (Spain)

Author keywords

Bipolar disorder; Major depressive disorder; Mitochondrial genetics; Schizophrenia

Indexed keywords

MITOCHONDRIAL DNA;

ARTICLE; BIPOLAR DISORDER; BRAIN; BRAIN REGION; CONTROLLED STUDY; DIAGNOSIS RELATED GROUP; DISEASE DURATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA CONTENT; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN TISSUE; MAJOR DEPRESSION; MENTAL DISEASE; MITOCHONDRIAL DNA DEPLETION; MITOCHONDRIAL DNA REPLICATION; MITOCHONDRIAL GENE; MITOCHONDRIAL GENETICS; OCCIPITAL CORTEX; ONSET AGE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHIZOPHRENIA;

BIPOLAR DISORDER; BRAIN; CASE-CONTROL STUDIES; DEPRESSIVE DISORDER, MAJOR; DNA, MITOCHONDRIAL; GENE EXPRESSION REGULATION; GENOME, MITOCHONDRIAL; HUMANS; MENTAL DISORDERS; NADH DEHYDROGENASE; RNA, MESSENGER; SCHIZOPHRENIA; SEQUENCE DELETION; TRANSCRIPTOME;

EID: 84874134421     PISSN: 15524841     EISSN: 1552485X     Source Type: Journal    
DOI: 10.1002/ajmg.b.32134     Document Type: Article

References (77)

1. Abasolo N, Torrell H, Roig B, Moyano S, Vilella E, Martorell L. 2011. RT-qPCR study on post-mortem brain samples from patients with major psychiatric disorders: Reference genes and specimen characteristics. J Psychiatr Res 45:1411-1418.
2. Altar CA, Jurata LW, Charles V, Lemire A, Liu P, Bukhman Y, Young TA, Bullard J, Yokoe H, Webster MJ, Knable MB, Brockman JA. 2005. Deficient hippocampal neuron expression of proteasome, ubiquitin, and mitochondrial genes in multiple schizophrenia cohorts. Biol Psychiatry 58:85-96.
3. Andreazza AC, Shao L, Wang JF, Young LT. 2010. Mitochondrial complex I activity and oxidative damage to mitochondrial proteins in the prefrontal cortex of patients with bipolar disorder. Arch Gen Psychiatry 67:360-368.
4. Anglin RE, Garside SL, Tarnopolsky MA, Mazurek MF, Rosebush PI. 2012. The psychiatric manifestations of mitochondrial disorders: A case and review of the literature. J Clin Psychiatry 73:506-512.
5. Bataillard M, Chatzoglou E, Rumbach L, Sternberg D, Tournade A, Laforet P, Jardel C, Maisonobe T, Lombes A. 2001. Atypical MELAS syndrome associated with a new mitochondrial tRNA glutamine point mutation. Neurology 56:405-407.
6. Beech RD, Lowthert L, Leffert JJ, Mason PN, Taylor MM, Umlauf S, Lin A, Lee JY, Maloney K, Muralidharan A, Lorberg B, Zhao H, Newton SS, Mane S, Epperson CN, Sinha R, Blumberg H, Bhagwagar Z. 2010. Increased peripheral blood expression of electron transport chain genes in bipolar depression. Bipolar Disord 12:813-824.
7. Ben-Shachar D. 2009. The interplay between mitochondrial complex I, dopamine and Sp1 in schizophrenia. J Neural Transm 116:1383-1396.
8. Bergemann ER, Boles RG. 2010. Maternal inheritance in recurrent early-onset depression. Psychiatr Genet 20:31-34.
9. Bogenhagen DF. 2012. Mitochondrial DNA nucleoid structure. Biochim Biophys Acta 1819:914-920.
10. Bustin SA, Beaulieu JF, Huggett J, Jaggi R, Kibenge FS, Olsvik PA, Penning LC, Toegel S. 2010. MIQE precis: Practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments. BMC Mol Biol 11:74.
11. Castagna AE, Addis J, McInnes RR, Clarke JT, Ashby P, Blaser S, Robinson BH. 2007. Late onset leigh syndrome and ataxia due to a T to C mutation at bp 9, 185 of mitochondrial DNA. Am J Med Genet Part A 143A:808-816.
12. Cataldo AM, McPhie DL, Lange NT, Punzell S, Elmiligy S, Ye NZ, Froimowitz MP, Hassinger LC, Menesale EB, Sargent LW, Logan DJ, Carpenter AE, Cohen BM. 2010. Abnormalities in mitochondrial structure in cells from patients with bipolar disorder. Am J Pathol 177:575-585.
13. Chinnery PF, Elliott HR, Hudson G, Samuels DC, Relton CL. 2012. Epigenetics, epidemiology and mitochondrial DNA diseases. Int J Epidemiol 41:177-187.
14. Falkenberg M, Gaspari M, Rantanen A, Trifunovic A, Larsson NG, Gustafsson CM. 2002. Mitochondrial transcription factors B1 and B2 activate transcription of human mtDNA. Nat Genet 31:289-294.
15. Fattal O, Budur K, Vaughan AJ, Franco K. 2006. Review of the literature on major mental disorders in adult patients with mitochondrial diseases. Psychosomatics 47:1-7.
16. Fattal O, Link J, Quinn K, Cohen BH, Franco K. 2007. Psychiatric comorbidity in 36 adults with mitochondrial cytopathies. CNS Spectr 12:429-438.
17. Finsterer J, Mahjoub SZ. 2012. Primary mitochondrial arteriopathy. Nutr Metab Cardiovasc Dis 22:393-399.
18. Fuke S, Kametani M, Kato T. 2008. Quantitative analysis of the 4977-bp common deletion of mitochondrial DNA in postmortem frontal cortex from patients with bipolar disorder and schizophrenia. Neurosci Lett 439:173-177.
19. Gardner A, Johansson A, Wibom R, Nennesmo I, von Dobeln U, Hagenfeldt L, Hallstrom T. 2003. Alterations of mitochondrial function and correlations with personality traits in selected major depressive disorder patients. J Affect Disord 76:55-68.
20. Gejman PV, Sanders AR, Kendler KS. 2011. Genetics of schizophrenia: New findings and challenges. Annu Rev Genomics Hum Genet 12:121-144.
21. Guillausseau PJ, Dubois-Laforgue D, Massin P, Laloi-Michelin M, Bellanne-Chantelot C, Gin H, Bertin E, Blickle JF, Bauduceau B, Bouhanick B, Cahen-Varsaux J, Casanova S, Charpentier G, Chedin P, Derrien C, Grimaldi A, Guerci B, Kaloustian E, Lorenzini F, Murat A, Olivier F, Paques M, Paquis-Flucklinger V, Tielmans A, Vincenot M, Vialettes B, Timsit J, GEDIAM, Mitochondrial Diabetes French Study Group. 2004. Heterogeneity of diabetes phenotype in patients with 3243bp mutation of mitochondrial DNA (maternally inherited diabetes and deafness or MIDD). Diabetes Metab 30:181-186.
22. He L, Chinnery PF, Durham SE, Blakely EL, Wardell TM, Borthwick GM, Taylor RW, Turnbull DM. 2002. Detection and quantification of mitochondrial DNA deletions in individual cells by real-time PCR. Nucleic Acids Res 30:e68.
23. Horvath R, Kley RA, Lochmuller H, Vorgerd M. 2007. Parkinson syndrome, neuropathy, and myopathy caused by the mutation A8344G (MERRF) in tRNALys. Neurology 68:56-58.
24. Huang J, Perlis RH, Lee PH, Rush AJ, Fava M, Sachs GS, Lieberman J, Hamilton SP, Sullivan P, Sklar P, Purcell S, Smoller JW. 2010. Cross-disorder genomewide analysis of schizophrenia, bipolar disorder, and depression. Am J Psychiatry 167:1254-1263.
25. Iwamoto K, Bundo M, Kato T. 2005. Altered expression of mitochondria-related genes in postmortem brains of patients with bipolar disorder or schizophrenia, as revealed by large-scale DNA microarray analysis. Hum Mol Genet 14:241-253.
26. Kakiuchi C, Ishiwata M, Kametani M, Nelson C, Iwamoto K, Kato T. 2005. Quantitative analysis of mitochondrial DNA deletions in the brains of patients with bipolar disorder and schizophrenia. Int J Neuropsychopharmacol 8:515-522.
27. Kato T, Kato N. 2000. Mitochondrial dysfunction in bipolar disorder. Bipolar Disord 2:180-190.
28. Kato T, Stine OC, McMahon FJ, Crowe RR. 1997. Increased levels of a mitochondrial DNA deletion in the brain of patients with bipolar disorder. Biol Psychiatry 42:871-875.
29. Kato M, Nakamura M, Ichiba M, Tomiyasu A, Shimo H, Higuchi I, Ueno S, Sano A. 2011. Mitochondrial DNA deletion mutations in patients with neuropsychiatric symptoms. Neurosci Res 69:331-336.
30. Katsel P, Davis KL, Gorman JM, Haroutunian V. 2005. Variations in differential gene expression patterns across multiple brain regions in schizophrenia. Schizophr Res 77:241-252.
31. Koene S, Kozicz TL, Rodenburg RJ, Verhaak CM, de Vries MC, Wortmann S, van de Heuvel L, Smeitink JA, Morava E. 2009. Major depression in adolescent children consecutively diagnosed with mitochondrial disorder. J Affect Disord 114:327-332.
32. Konradi C, Eaton M, MacDonald ML, Walsh J, Benes FM, Heckers S. 2004. Molecular evidence for mitochondrial dysfunction in bipolar disorder. Arch Gen Psychiatry 61:300-308.
33. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandoski M, Barsh GS, Clayton DA. 1998. Mitochondrial transcription factor A is necessary for mtDNA maintenance and embryogenesis in mice. Nat Genet 18:231-236.
34. Malik AN, Czajka A. 2012. Is mitochondrial DNA content a potential biomarker of mitochondrial dysfunction? Mitochondrion S1567-7249:00232-00232.
35. Mancuso M, Ricci G, Choub A, Filosto M, DiMauro S, Davidzon G, Tessa A, Santorelli FM, Murri L, Siciliano G. 2008. Autosomal dominant psychiatric disorders and mitochondrial DNA multiple deletions: Report of a family. J Affect Disord 106:173-177.
36. Manji H, Kato T, Di Prospero NA, Ness S, Beal MF, Krams M, Chen G. 2012. Impaired mitochondrial function in psychiatric disorders. Nat Rev Neurosci 13:293-307.
37. McGuffin P, Rijsdijk F, Andrew M, Sham P, Katz R, Cardno A. 2003. The heritability of bipolar affective disorder and the genetic relationship to unipolar depression. Arch Gen Psychiatry 60:497-502.
38. McMahon FJ, Stine OC, Meyers DA, Simpson SG, DePaulo JR. 1995. Patterns of maternal transmission in bipolar affective disorder. Am J Hum Genet 56:1277-1286.
39. Meissner C, Bruse P, Oehmichen M. 2006. Tissue-specific deletion patterns of the mitochondrial genome with advancing age. Exp Gerontol 41:518-524.
40. Meissner C, Bruse P, Mohamed SA, Schulz A, Warnk H, Storm T, Oehmichen M. 2008. The 4977bp deletion of mitochondrial DNA in human skeletal muscle, heart and different areas of the brain: A useful biomarker or more? Exp Gerontol 43:645-652.
41. Munakata K, Tanaka M, Mori K, Washizuka S, Yoneda M, Tajima O, Akiyama T, Nanko S, Kunugi H, Tadokoro K, Ozaki N, Inada T, Sakamoto K, Fukunaga T, Iijima Y, Iwata N, Tatsumi M, Yamada K, Yoshikawa T, Kato T. 2004. Mitochondrial DNA 3644T->C mutation associated with bipolar disorder. Genomics 84:1041-1050.
42. Munakata K, Iwamoto K, Bundo M, Kato T. 2005. Mitochondrial DNA 3243A>G mutation and increased expression of LARS2 gene in the brains of patients with bipolar disorder and schizophrenia. Biol Psychiatry 57:525-532.
43. Munakata K, Fujii K, Nanko S, Kunugi H, Kato T. 2007. Sequence and functional analyses of mtDNA in a maternally inherited family with bipolar disorder and depression. Mutat Res 617:119-124.
44. Prabakaran S, Swatton JE, Ryan MM, Huffaker SJ, Huang JTJ, Griffin JL, Wayland M, Freeman T, Dudbridge F, Lilley KS, Karp NA, Hester S, Trachev D, Mimmack ML, Yolken RH, Webster MJ, Torrey EF, Bahn S. 2004. Mitochondrial dysfunction in schizophrenia: Evidence for compromised brain metabolism and oxidative stress. Mol Psychiatry 9:684-697.
45. Raspall-Chaure M, Solano A, Vazquez E, Macaya-Ruiz A, del Toro-Riera M, Cabezuelo-Briones A, Montoya J, Andreu A, Roig-Quilis M. 2004. A patient with bilateral lesion in the striatum and slowly progressive dystonia secondary to T14487C mutation in the ND6 gene of complex I of the mitochondrial respiratory chain. Rev Neurol 39:1129-1132.
46. Regenold WT, Phatak P, Marano CM, Gearhart L, Viens CH, Hisley KC. 2007. Myelin staining of deep white matter in the dorsolateral prefrontal cortex in schizophrenia, bipolar disorder, and unipolar major depression. Psychiatry Res 151:179-188.
47. Reinecke F, Smeitink JA, van der Westhuizen FH. 2009. OXPHOS gene expression and control in mitochondrial disorders. Biochim Biophys Acta 1792:1113-1121.
48. Rezin GT, Amboni G, Zugno AI, Quevedo J, Streck EL. 2009. Mitochondrial dysfunction and psychiatric disorders. Neurochem Res 34:1021-1029.
49. Roig B, Franco-Pons N, Martorell L, Tomàs J, Vogel WF, Vilella E. 2010. Expression of the tyrosine kinase discoidin domain receptor 1 (DDR1) in human central nervous system myelin. Brain Res 1336:22-29.
50. Rollins B, Martin MV, Sequeira PA, Moon EA, Morgan LZ, Watson SJ, Schatzberg A, Akil H, Myers RM, Jones EG, Wallace DC, Bunney WE, Vawter MP. 2009. Mitochondrial variants in schizophrenia, bipolar disorder, and major depressive disorder. PLoS ONE 4:e4913.
51. Roubertoux PL, Sluyter F, Carlier M, Marcet B, Maarouf-Veray F, Cherif C, Marican C, Arrechi P, Godin F, Jamon M, Verrier B, Cohen-Salmon C. 2003. Mitochondrial DNA modifies cognition in interaction with the nuclear genome and age in mice. Nat Genet 35:65-69.
52. Ryu JS, Lee SJ, Sung IY, Ko TS, Yoo HI. 2009. Depressive episode with catatonic features in a case of mitochondrial myopathy, encephalopathy, lactic acidosis, and stroke-like episodes (MELAS). J Child Neurol 24:1307-1309.
53. Sabunciyan S, Kirches E, Krause G, Bogerts B, Mawrin C, Llenos IC, Weis S. 2007. Quantification of total mitochondrial DNA and mitochondrial common deletion in the frontal cortex of patients with schizophrenia and bipolar disorder. J Neural Transm 114:665-674.
54. Sacconi S, Salviati L, Gooch C, Bonilla E, Shanske S, DiMauro S. 2002. Complex neurologic syndrome associated with the G1606A mutation of mitochondrial DNA. Arch Neurol 59:1013-1015.
55. Salpietro CD, Briuglia S, Merlino MV, Di Bella C, Rigoli L. 2003. A mitochondrial DNA mutation (A3243G mtDNA) in a family with cyclic vomiting. Eur J Pediatr 162:727-728.
56. Scaglia F. 2010. The role of mitochondrial dysfunction in psychiatric disease. Dev Disabil Res Rev 16:136-143.
57. Schapira AH. 2006. Mitochondrial disease. Lancet 368:70-82.
58. Schoenfeld R, Wong A, Silva J, Li M, Itoh A, Horiuchi M, Itoh T, Pleasure D, Cortopassi G. 2010. Oligodendroglial differentiation induces mitochondrial genes and inhibition of mitochondrial function represses oligodendroglial differentiation. Mitochondrion 10:143-150.
59. Schroeder A, Mueller O, Stocker S, Salowsky R, Leiber M, Gassmann M, Lightfoot S, Menzel W, Granzow M, Ragg T. 2006. The RIN: An RNA integrity number for assigning integrity values to RNA measurements. BMC Mol Biol 7:3.
60. Sequeira A, Martin MV, Rollins B, Moon EA, Bunney WE, Macciardi F, Lupoli S, Smith EN, Kelsoe J, Magnan CN, van Oven M, Baldi P, Wallace DC, Vawter MP. 2012. Mitochondrial mutations and polymorphisms in psychiatric disorders. Front Genet 3:103.
61. Shao L, Martin MV, Watson SJ, Schatzberg A, Akil H, Myers RM, Jones EG, Bunney WE, Vawter MP. 2008. Mitochondrial involvement in psychiatric disorders. Ann Med 40:281-295.
62. Smoller JW, Finn CT. 2003. Family, twin, and adoption studies of bipolar disorder. Am J Med Genet Part C Semin Med Genet 123C:48-58.
63. Soong NW, Arnheim N. 1996. Detection and quantification of mitochondrial DNA deletions. Methods Enzymol 264:421-431.
64. Soong NW, Hinton DR, Cortopassi G, Arnheim N. 1992. Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain. Nat Genet 2:318-323.
65. Tanhauser SM, Laipis PJ. 1995. Multiple deletions are detectable in mitochondrial DNA of aging mice. J Biol Chem 270:24769-24775.
66. Taylor RW, Turnbull DM. 2005. Mitochondrial DNA mutations in human disease. Nat Rev Genet 6:389-402.
67. Taylor MA, Berenbaum SA, Jampala VC, Cloninger CR. 1993. Are schizophrenia and affective disorder related? Preliminary data from a family study. Am J Psychiatry 150:278-285.
68. Torrey EF, Webster M, Knable M, Johnston N, Yolken RH. 2000. The stanley foundation brain collection and neuropathology consortium. Schizophr Res 44:151-155.
69. Tsuang MT, Winokur G, Crowe RR. 1980. Morbidity risks of schizophrenia and affective disorders among first degree relatives of patients with schizophrenia, mania, depression and surgical conditions. Br J Psychiatry 137:497-504.
70. Vawter MP, Tomita H, Meng F, Bolstad B, Li J, Evans S, Choudary P, Atz M, Shao L, Neal C, Walsh DM, Burmeister M, Speed T, Myers R, Jones EG, Watson SJ, Akil H, Bunney WE. 2006. Mitochondrial-related gene expression changes are sensitive to agonal-pH state: Implications for brain disorders. Mol Psychiatry 11:663-679.
71. Venegas V, Wang J, Dimmock D, Wong LJ. 2011. Real-time quantitative PCR analysis of mitochondrial DNA content. Curr Protoc Hum Genet Chapter 19:Unit 19.7.
72. Verge B, Alonso Y, Valero J, Miralles C, Vilella E, Martorell L. 2011. Mitochondrial DNA (mtDNA) and schizophrenia. Eur Psychiatry 26:45-56.
73. Verge B, Alonso Y, Miralles C, Valero J, Vilella E, Boles RG, Martorell L. 2012. New evidence for the involvement of mitochondrial inheritance in schizophrenia: Results from a cross-sectional study evaluating the risk of illness in relatives of schizophrenia patients. J Clin Psychiatry 73:684-690.
74. Wallace DC, Lott MT, Shoffner JM, Brown MD. 1992. Diseases resulting from mitochondrial DNA point mutations. J Inherit Metab Dis 15:472-479.
75. Wang JF. 2007. Defects of mitochondrial electron transport chain in bipolar disorder: Implications for mood-stabilizing treatment. Can J Psychiatry 52:753-762.
76. Washizuka S, Ikeda A, Kato N, Kato T. 2003. Possible relationship between mitochondrial DNA polymorphisms and lithium response in bipolar disorder. Int J Neuropsychopharmacol 6:421-424.
77. Wray NR, Pergadia ML, Blackwood DH, Penninx BW, Gordon SD, Nyholt DR, Ripke S, Macintyre DJ, McGhee KA, Maclean AW, Smit JH, Hottenga JJ, Willemsen G, Middeldorp CM, de Geus EJ, Lewis CM, McGuffin P, Hickie IB, van den Oord EJ, Liu JZ, Macgregor S, McEvoy BP, Byrne EM, Medland SE, Statham DJ, Henders AK, Heath AC, Montgomery GW, Martin NG, Boomsma DI, Madden PA, Sullivan PF. 2012. Genome-wide association study of major depressive disorder: New results, meta-analysis, and lessons learned. Mol Psychiatry 17:36-48.