Expression Profiles of Mitochondrial Genes in the Frontal Cortex and the Caudate Nucleus of Developing Humans and Mice Selectively Bred for High and Low Fear

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Choi, Kwang H ^a   Le, Thien ^a   McGuire, Jennifer ^a   Coyner, Jennifer ^a   Higgs, Brandon W ^b   Diglisic, Suad ^c   Johnson, Luke R ^a   Benedek, David M ^a   Ursano, Robert J ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b Elashoff Consulting   (United States)

^c Stanley Medical Research Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME B; RNA;

ADOLESCENT; ADULT; AGE; ANIMAL EXPERIMENT; ARTICLE; BRAIN DEVELOPMENT; BRAIN TISSUE; CAUDATE NUCLEUS; CHILD; CONTROLLED STUDY; FEAR; GENE EXPRESSION; HUMAN; HUMAN TISSUE; INFANT; MICROARRAY ANALYSIS; MITOCHONDRIAL GENE; MITOCHONDRIAL UNCOUPLING PROTEIN 5 GENE; MONOAMINE OXIDASE B GENE; MOUSE; NADH DEHYDROGENASE FLAVOPROTEIN GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; POSTNATAL DEVELOPMENT; PREFRONTAL CORTEX; PRESCHOOL CHILD; RNA EXTRACTION; SCHOOL CHILD; TUBULIN BETA 3 CHAIN GENE;

ADOLESCENT; ADULT; AGING; ANIMALS; BREEDING; CAUDATE NUCLEUS; CHILD; CHILD, PRESCHOOL; FEAR; FRONTAL LOBE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, MITOCHONDRIAL; HUMANS; INFANT; INFANT, NEWBORN; MICE; MIDDLE AGED; POLYMERASE CHAIN REACTION; REPRODUCIBILITY OF RESULTS; SIGNAL TRANSDUCTION; YOUNG ADULT;

MUS;

EID: 84869073292     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0049183     Document Type: Article

References (89)

1. Webster MJ, Elashoff M, Weickert CS, (2011) Molecular evidence that cortical synaptic growth predominates during the first decade of life in humans. Int J Dev Neurosci 29: 225-236.
2. Weickert CS, Elashoff M, Richards AB, Sinclair D, Bahn S, et al. (2009) Transcriptome analysis of male-female differences in prefrontal cortical development. Mol Psychiatry 14: 558-561.
3. Choi KH, Zepp ME, Higgs BW, Weickert CS, Webster MJ, (2009) Expression profiles of schizophrenia susceptibility genes during human prefrontal cortical development. J Psychiatry Neurosci 34: 450-458.
4. Wright LD, Muir KE, Perrot TS, (2012) Enhanced stress responses in adolescent versus adult rats exposed to cues of predation threat, and peer interaction as a predictor of adult defensiveness. Dev Psychobiol 54: 47-69.
5. Meaney MJ, Szyf M, (2005) Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin Neurosci 7: 103-123.
6. Wright LD, Hebert KE, Perrot-Sinal TS, (2008) Periadolescent stress exposure exerts long-term effects on adult stress responding and expression of prefrontal dopamine receptors in male and female rats. Psychoneuroendocrinology 33: 130-142.
7. Meaney MJ, Sapolsky RM, McEwen BS, (1985) The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Brain Res 350: 159-164.
8. McCormick CM, Mathews IZ, (2007) HPA function in adolescence: role of sex hormones in its regulation and the enduring consequences of exposure to stressors. Pharmacol Biochem Behav 86: 220-233.
9. Sullivan RM, Gratton A, (2002) Prefrontal cortical regulation of hypothalamic-pituitary-adrenal function in the rat and implications for psychopathology: side matters. Psychoneuroendocrinology 27: 99-114.
10. Woo TU, Crowell AL, (2005) Targeting synapses and myelin in the prevention of schizophrenia. Schizophr Res 73: 193-207.
11. Casey BJ, Giedd JN, Thomas KM, (2000) Structural and functional brain development and its relation to cognitive development. Biol Psychol 54: 241-257.
12. Miller EK, Cohen JD, (2001) An integrative theory of prefrontal cortex function. Annu Rev Neurosci 24: 167-202.
13. Savitz J, Drevets WC, (2009) Bipolar and major depressive disorder: neuroimaging the developmental-degenerative divide. Neurosci Biobehav Rev 33: 699-771.
14. Lewis DA, (1997) Development of the prefrontal cortex during adolescence: insights into vulnerable neural circuits in schizophrenia. Neuropsychopharmacology 16: 385-398.
15. Weinberger DR, Berman KF, Suddath R, Torrey EF, (1992) Evidence of dysfunction of a prefrontal-limbic network in schizophrenia: a magnetic resonance imaging and regional cerebral blood flow study of discordant monozygotic twins. Am J Psychiatry 149: 890-897.
16. Myers-Schulz B, Koenigs M (2011) Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders. Mol Psychiatry.
17. Lewis DA, Moghaddam B, (2006) Cognitive dysfunction in schizophrenia: convergence of gamma-aminobutyric acid and glutamate alterations. Arch Neurol 63: 1372-1376.
18. Weickert CS, Weinberger DR, (1998) A candidate molecule approach to defining developmental pathology in schizophrenia. Schizophr Bull 24: 303-316.
19. Graybiel AM, (2005) The basal ganglia: learning new tricks and loving it. Curr Opin Neurobiol 15: 638-644.
20. Hollerman JR, Tremblay L, Schultz W, (2000) Involvement of basal ganglia and orbitofrontal cortex in goal-directed behavior. Prog Brain Res 126: 193-215.
21. Selemon LD, Goldman-Rakic PS, (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5: 776-794.
22. Eblen F, Graybiel AM, (1995) Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J Neurosci 15: 5999-6013.
23. Murray GK, Corlett PR, Clark L, Pessiglione M, Blackwell AD, et al. (2008) Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol Psychiatry 13: 239, 267-276.
24. Mamah D, Wang L, Barch D, de Erausquin GA, Gado M, et al. (2007) Structural analysis of the basal ganglia in schizophrenia. Schizophr Res 89: 59-71.
25. 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.
26. Pieczenik SR, Neustadt J, (2007) Mitochondrial dysfunction and molecular pathways of disease. Exp Mol Pathol 83: 84-92.
27. Tranah GJ (2010) Mitochondrial-nuclear epistasis: Implications for human aging and longevity. Ageing Res Rev.
28. Santoro A, Salvioli S, Raule N, Capri M, Sevini F, et al. (2006) Mitochondrial DNA involvement in human longevity. Biochim Biophys Acta 1757: 1388-1399.
29. Jazin EE, Cavelier L, Eriksson I, Oreland L, Gyllensten U, (1996) Human brain contains high levels of heteroplasmy in the noncoding regions of mitochondrial DNA. Proc Natl Acad Sci U S A 93: 12382-12387.
30. Bowling AC, Mutisya EM, Walker LC, Price DL, Cork LC, et al. (1993) Age-dependent impairment of mitochondrial function in primate brain. J Neurochem 60: 1964-1967.
31. Cortopassi GA, Shibata D, Soong NW, Arnheim N, (1992) A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc Natl Acad Sci U S A 89: 7370-7374.
32. Hutchin T, Cortopassi G, (1995) A mitochondrial DNA clone is associated with increased risk for Alzheimer disease. Proc Natl Acad Sci U S A 92: 6892-6895.
33. 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.
34. Kang HJ, Kawasawa YI, Cheng F, Zhu Y, Xu X, et al. (2011) Spatio-temporal transcriptome of the human brain. Nature 478: 483-489.
35. Somel M, Franz H, Yan Z, Lorenc A, Guo S, et al. (2009) Transcriptional neoteny in the human brain. Proc Natl Acad Sci U S A 106: 5743-5748.
36. Harris LW, Lockstone HE, Khaitovich P, Weickert CS, Webster MJ, et al. (2009) Gene expression in the prefrontal cortex during adolescence: implications for the onset of schizophrenia. BMC Med Genomics 2: 28.
37. Ben-Shachar D, Laifenfeld D, (2004) Mitochondria, synaptic plasticity, and schizophrenia. Int Rev Neurobiol 59: 273-296.
38. Konradi C, Eaton M, MacDonald ML, Walsh J, Benes FM, et al. (2004) Molecular evidence for mitochondrial dysfunction in bipolar disorder. Arch Gen Psychiatry 61: 300-308.
39. Shao L, Martin MV, Watson SJ, Schatzberg A, Akil H, et al. (2008) Mitochondrial involvement in psychiatric disorders. Ann Med 40: 281-295.
40. Einat H, Yuan P, Manji HK, (2005) Increased anxiety-like behaviors and mitochondrial dysfunction in mice with targeted mutation of the Bcl-2 gene: further support for the involvement of mitochondrial function in anxiety disorders. Behav Brain Res 165: 172-180.
41. Su YA, Wu J, Zhang L, Zhang Q, Su DM, et al. (2008) Dysregulated mitochondrial genes and networks with drug targets in postmortem brain of patients with posttraumatic stress disorder (PTSD) revealed by human mitochondria-focused cDNA microarrays. Int J Biol Sci 4: 223-235.
42. Gardner A, Johansson A, Wibom R, Nennesmo I, von Dobeln U, et al. (2003) Alterations of mitochondrial function and correlations with personality traits in selected major depressive disorder patients. J Affect Disord 76: 55-68.
43. Konradi C, Sillivan SE, Clay HB (2011) Mitochondria, oligodendrocytes and inflammation in bipolar disorder: Evidence from transcriptome studies points to intriguing parallels with multiple sclerosis. Neurobiol Dis.
44. 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.
45. Ryan MM, Lockstone HE, Huffaker SJ, Wayland MT, Webster MJ, et al. (2006) Gene expression analysis of bipolar disorder reveals downregulation of the ubiquitin cycle and alterations in synaptic genes. Mol Psychiatry 11: 965-978.
46. Shao L, Vawter MP, (2008) Shared gene expression alterations in schizophrenia and bipolar disorder. Biol Psychiatry 64: 89-97.
47. Rondi-Reig L, Lemaigre Dubreuil Y, Martinou JC, Delhaye-Bouchaud N, Caston J, et al. (1997) Fear decrease in transgenic mice overexpressing bcl-2 in neurons. Neuroreport 8: 2429-2432.
48. Koene S, Kozicz TL, Rodenburg RJ, Verhaak CM, de Vries MC, et al. (2009) Major depression in adolescent children consecutively diagnosed with mitochondrial disorder. J Affect Disord 114: 327-332.
49. Vawter MP, Tomita H, Meng F, Bolstad B, Li J, et al. (2006) Mitochondrial-related gene expression changes are sensitive to agonal-pH state: implications for brain disorders. Mol Psychiatry 11: 615, 663-679.
50. Gardner A, Boles RG, (2011) Beyond the serotonin hypothesis: mitochondria, inflammation and neurodegeneration in major depression and affective spectrum disorders. Prog Neuropsychopharmacol Biol Psychiatry 35: 730-743.
51. Duncan J, Johnson S, Ou XM, (2012) Monoamine oxidases in major depressive disorder and alcoholism. Drug Discov Ther 6: 112-122.
52. Carrera N, Sanjuan J, Molto MD, Carracedo A, Costas J, (2009) Recent adaptive selection at MAOB and ancestral susceptibility to schizophrenia. Am J Med Genet B Neuropsychiatr Genet 150B: 369-374.
53. Ben-Shachar D, Karry R, (2008) Neuroanatomical pattern of mitochondrial complex I pathology varies between schizophrenia, bipolar disorder and major depression. PLoS One 3: e3676.
54. Ben-Shachar D, Karry R, (2007) Sp1 expression is disrupted in schizophrenia; a possible mechanism for the abnormal expression of mitochondrial complex I genes, NDUFV1 and NDUFV2. PLoS One 2: e817.
55. Gigante AD, Andreazza AC, Lafer B, Yatham LN, Beasley CL, et al. (2011) Decreased mRNA expression of uncoupling protein 2, a mitochondrial proton transporter, in post-mortem prefrontal cortex from patients with bipolar disorder and schizophrenia. Neurosci Lett 505: 47-51.
56. Cocchi M, Tonello L, Rasenick MM, (2010) Human depression: a new approach in quantitative psychiatry. Ann Gen Psychiatry 9: 25.
57. Beasley CL, Pennington K, Behan A, Wait R, Dunn MJ, et al. (2006) Proteomic analysis of the anterior cingulate cortex in the major psychiatric disorders: Evidence for disease-associated changes. Proteomics 6: 3414-3425.
58. Li Z, Okamoto K, Hayashi Y, Sheng M, (2004) The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell 119: 873-887.
59. Lee CW, Peng HB, (2008) The function of mitochondria in presynaptic development at the neuromuscular junction. Mol Biol Cell 19: 150-158.
60. Chan DC, (2006) Mitochondria: dynamic organelles in disease, aging, and development. Cell 125: 1241-1252.
61. Turnbull HE, Lax NZ, Diodato D, Ansorge O, Turnbull DM, (2010) The mitochondrial brain: From mitochondrial genome to neurodegeneration. Biochim Biophys Acta 1802: 111-121.
62. Mattson MP (1991) Activities in cellular signalling pathways: a two-edged sword? Neurobiol Aging 12: 343-346; discussion 352-345.
63. Levitt P, Harvey JA, Friedman E, Simansky K, Murphy EH, (1997) New evidence for neurotransmitter influences on brain development. Trends Neurosci 20: 269-274.
64. Meier E, Hertz L, Schousboe A, (1991) Neurotransmitters as developmental signals. Neurochem Int 19: 1-15.
65. Bortolato M, Chen K, Shih JC, (2008) Monoamine oxidase inactivation: from pathophysiology to therapeutics. Adv Drug Deliv Rev 60: 1527-1533.
66. Sokolov BP, Jiang L, Trivedi NS, Aston C, (2003) Transcription profiling reveals mitochondrial, ubiquitin and signaling systems abnormalities in postmortem brains from subjects with a history of alcohol abuse or dependence. J Neurosci Res 72: 756-767.
67. Rollins B, Martin MV, Sequeira PA, Moon EA, Morgan LZ, et al. (2009) Mitochondrial variants in schizophrenia, bipolar disorder, and major depressive disorder. PLoS One 4: e4913.
68. Davey GP, Peuchen S, Clark JB, (1998) Energy thresholds in brain mitochondria. Potential involvement in neurodegeneration. J Biol Chem 273: 12753-12757.
69. Katyare SS, Rajan RR, (1995) Effect of long-term in vivo treatment with imipramine on the oxidative energy metabolism in rat brain mitochondria. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 112: 353-357.
70. Nahon E, Israelson A, Abu-Hamad S, Varda SB, (2005) Fluoxetine (Prozac) interaction with the mitochondrial voltage-dependent anion channel and protection against apoptotic cell death. FEBS Lett 579: 5105-5110.
71. Souza ME, Polizello AC, Uyemura SA, Castro-Silva O, Curti C, (1994) Effect of fluoxetine on rat liver mitochondria. Biochem Pharmacol 48: 535-541.
72. Finsterer J, Segall L, (2010) Drugs interfering with mitochondrial disorders. Drug Chem Toxicol 33: 138-151.
73. LeDoux JE, (2000) Emotion circuits in the brain. Annu Rev Neurosci 23: 155-184.
74. Ameli R, Ip C, Grillon C, (2001) Contextual fear-potentiated startle conditioning in humans: replication and extension. Psychophysiology 38: 383-390.
75. Norrholm SD, Jovanovic T, Olin IW, Sands LA, Karapanou I, et al. (2011) Fear extinction in traumatized civilians with posttraumatic stress disorder: relation to symptom severity. Biol Psychiatry 69: 556-563.
76. Ehlers MD, (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6: 231-242.
77. Nicholls DG, Budd SL, (2000) Mitochondria and neuronal survival. Physiol Rev 80: 315-360.
78. Zielke HR, Wisniewski S, Stein SA, (1996) Brief report: the role of National Brain and Tissue Banks in research on autism and developmental disorders. J Autism Dev Disord 26: 227-230.
79. Choi KH, Zepp ME, Higgs BW, Weickert CS, Webster MJ, (2009) Expression profiles of schizophrenia susceptibility genes during human prefrontal cortical development. J Psych Neurosci 34: 450-458.
80. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, et al. (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5: R80.
81. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, et al. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4: 249-264.
82. Choi KH, Higgs BW, Wendland JR, Song J, McMahon FJ, et al. (2011) Gene expression and genetic variation data implicate PCLO in bipolar disorder. Biol Psychiatry 69: 353-359.
83. Sherman BT, Huang da W, Tan Q, Guo Y, Bour S, et al. (2007) DAVID Knowledgebase: a gene-centered database integrating heterogeneous gene annotation resources to facilitate high-throughput gene functional analysis. BMC Bioinformatics 8: 426.
84. Benjamini Y, Hochberg Y, (1995) Controlling the false discovery rate:A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 57: 289-300.
85. Parker CC, Palmer AA, (2011) Dark matter: Are mice the solution to missing heritability? Frontiers in Genetics 2: 32.
86. Ponder CA, Huded CP, Munoz MB, Gulden FO, Gilliam TC, et al. (2008) Rapid selection response for contextual fear conditioning in a cross between C57BL/6J and A/J: behavioral, QTL and gene expression analysis. Behav Genet 38: 277-291.
87. Ponder CA, Kliethermes CL, Drew MR, Muller J, Das K, et al. (2007) Selection for contextual fear conditioning affects anxiety-like behaviors and gene expression. Genes Brain Behav 6: 736-749.
88. Parker CC, Sokoloff G, Cheng R, Palmer AA (2012) Genome-Wide Association for Fear Conditioning in an Advanced Intercross Mouse Line. Behav Genet.
89. Choi K, Le T, McGuire J, Xing G, Zhang L, et al. (2012) Expression pattern of the cannabinoid receptor genes in the frontal cortex of mood disorder patients and mice selectively bred for high and low fear. J Psychiatr Res.