Lead neurotoxicity: Exploring the potential impact of lead substitution in zinc-finger proteins on mental health

Metallomics

Volumn 8, Issue 6, 2016, Pages 579-588

  Ordemann, Jacqueline Michelle ^a   Austin, Rachel Narehood ^a,b  

^a BATES COLLEGE   (United States)

^b Program on US Russia Relations at Columbia s Harriman Institute   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INDUSTRIAL POISONS; NEURODEGENERATIVE DISEASES; PROTEINS; ZINC;

ALZHEIMER'S DISEASE; DNA METHYLTRANSFERASES; INTELLECTUAL DISABILITY; MENTAL HEALTH; NMDA RECEPTOR; PARKINSON'S DISEASE; POTENTIAL IMPACTS; ZINC FINGER PROTEIN;

DISEASES;

AMYLOID BETA PROTEIN; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; DNA METHYLTRANSFERASE 1; DOPAMINE RECEPTOR; EARLY GROWTH RESPONSE FACTOR 1; LEAD; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PRESENILIN 1; PRESENILIN 2; TRANSCRIPTION FACTOR IIIA; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG; ZINC; ZINC FINGER PROTEIN; ZINC FINGER PROTEIN 804A; NERVE PROTEIN;

ALZHEIMER DISEASE; BINDING SITE; COGNITION; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; LEAD POISONING; MENTAL DISEASE; MENTAL HEALTH; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; REINFORCEMENT; REVIEW; SCHIZOPHRENIA; CHEMISTRY; METABOLISM; PATHOLOGY;

HUMANS; LEAD; MENTAL DISORDERS; MENTAL HEALTH; NERVE TISSUE PROTEINS; ZINC FINGERS;

EID: 84975267535     PISSN: 17565901     EISSN: 1756591X     Source Type: Journal    
DOI: 10.1039/c5mt00300h     Document Type: Review

References (121)

1. E. Peisach C. O. Pabo Constraints for Zinc Finger Linker Design as Inferred from X-ray Crystal Structure of Tandem Zif268-DNA Complexes J. Mol. Biol. 2003 330 1 7
2. R. T. Nolte R. M. Conlin S. C. Harrison R. S. Brown Differing roles for zinc fingers in DNA recognition: structure of a six-finger transcription factor IIIA complex Proc. Natl. Acad. Sci. U. S. A. 1998 95 2938 2943
3. S. Oka Y. Shiraishi T. Yoshida T. Ohkubo Y. Sugiura Y. Kobayashi NMR Structure of Transcription Factor Sp1 DNA Binding Domain Biochemistry 2004 43 16027 16035
4. K. Takeshita I. Suetake E. Yamashita M. Suga H. Narita A. Nakagawa S. Tajima Structural insight into maintenance methylation by mouse DNA methyltransferase 1 (Dnmt1) Proc. Natl. Acad. Sci. U. S. A. 2011 108 9055 9059
5. A. N. Istrate P. O. Tsvetkov A. B. Mantzyzov A. A. Kulikova S. A. Kozin A. A. Makarov V. I. Polshakov NMR Solution Structure of Rat Aβ(1-16): Toward Understanding the Mechanism of Rats' Resistance to Alzheimer's Disease Biophys. J. 2012 102 136 143
6. M. T. Lai E. Chen M. Crouthamel J. Di-Muzio-Mower M. Xu Q. Huang E. Price R. B. Register X. Shi D. B. Donoviel A. Bernstein D. Hazuda S. J. Gardell Y. Li Presenilin-1 and Presenilin-2 Exhibit Distinct yet Overlapping-Secretase Activities J. Biol. Chem. 2003 278 22475 22481
7. J. A. Schetz D. R. Sibley Zinc allosterically modulates antagonist binding to cloned D1 and D2 dopamine receptors J. Neurochem. 1997 68 1990 1997
8. T. R. Guilarte R. C. Miceli D. A. Jett Biochemical evidence of an interaction of lead at the zinc allosteric sites of the NMDA receptor complex: effects of neuronal development Neurotoxicology 1995 16 63 71
9. T. Ikuta B. D. Peters S. Guha M. John K. H. Karlsgodt T. Lencz P. R. Szeszko A. K. Malhotra A schizophrenia risk gene, ZNF804A, is associated with brain white matter microstructure Schizophr. Res. 2014 155 15 20
10. S. Shimizu Y. Koyama T. Hattori T. Tachibana T. Yoshimi H. Emoto Y. Matsumoto S. Miyata T. Katayama A. Ito M. Tohyama DBZ, a CNS-specific DISC1 binding protein, positively regulates oligodendrocyte differentiation DBZ promotes oligodendrocyte differentiation Glia 2014 62 709 724
11. CDC, Blood Lead Levels in Children Aged 1-5 Years-United States, 1999-2010, Morbidity and Mortality Weekly Report, 2013, 62, 245-248
12. E. Goulde Childhood Lead Poisoning: Conservative Estimates of the Social and Economic Benefits of Lead Hazard Control Environ. Health Perspect. 2009 117 1162 1167
13. L. Patrick Lead toxicity, a review of the literature. Part 1: Exposure, evaluation, and treatment Altern. Med. Rev. 2006 11 2 22
14. American Association of Pediatrics Lead poisoning: from screening to primary prevention Pediatric 1993 92 176 183
15. K. M. Bakulski L. S. Rozek D. C. Dolinoy H. L. Paulson H. Hu Alzheimer's disease and environmental exposure to lead: the epidemiologic evidence and potential role of epigenetics Curr. Alzheimer Res. 2012 9 563 573
16. J. Lee J. L. Freeman Zebrafish as a model for investigating developmental lead (Pb) neurotoxicity as a risk factor in adult neurodegenerative disease: A mini-review Neurotoxicology 2014 43 57 64
17. M. G. Weisskopf J. Weuve M. H. Saint-Hilaire L. Sudarsky N. K. Simon B. Hersh J. Schwartz R. O. Wright H. Hu Association of Cumulative Lead Exposure with Parkinson's Disease Environ. Health Perspect. 2010 118 1609 1613
18. S. Coon A. Stark E. Peterson A. Gloi G. Kortsha J. Pounds D. Chettle J. Gorell Whole-Body Lifetime Occupational Lead Exposure and Risk of Parkinson's Disease Environ. Health Perspect. 2006 114 1872 1876
19. M. G. A. Opler A. S. Brown J. Graziano M. Desai W. Zheng C. Schaefer P. Factor-Litvak E. S. Susser Prenatal lead exposure, δ-aminolevulinic acid, and schizophrenia Environ. Health Perspect. 2004 112 548 552
20. T. R. Guilarte M. Opler M. Pletnikov Is lead exposure in early life an environmental risk factor for Schizophrenia? Neurobiological connections and testable hypotheses Neurotoxicology 2012 33 560 574
21. J.-H. Yoon Y.-S. Ahn The association between blood lead level and clinical mental disorders in fifty thousand lead-exposed male workers J. Affective Disord. 2016 190 41 46
22. S. Nolen-Hoeksema, Abnormal Psychology, McGraw Hill, New York, NY, 6th edn, 2013
23. S. Sadiq Z. Ghazala A. Chowdhury D. Busselberg Metal Toxicity at the Synapse: Presynaptic, Postsynaptic, and Long-term Effects J. Toxicol. 2012 110 1 42
24. J. T. Coyle G. Tsai D. Goff Converging Evidence of NMDA Receptor Hypofunction in the Pathophysiology of Schizophrenia Ann. N. Y. Acad. Sci. 2003 1003 318 327
25. H. A. Robertson Dopamine receptor interactions: some implications for the treatment of Parkinson's disease Trends Neurosci. 1992 15 201 206
26. M. D. Garrick K. G. Dolan C. Horbinski A. J. Ghio D. Higgins M. Porubcin E. G. Moore L. N. Hainsworth J. N. Umbreit M. E. Conrad L. Feng A. Lis J. A. Roth S. Singleton L. M. Garrick DMT1: a mammalian transporter for multiple metals BioMetals 2003 16 41 54
27. D. I. Bannon R. Abounader P. S. Lees J. P. Bressler Effect of DMT1 knockdown on iron, cadmium, and lead uptake in Caco-2 cells Am. J. Physiol.: Cell Physiol. 2003 284 C44 C50
28. Q. Wang W. Luo W. Zhang M. Liu H. Song J. Chen Involvement of DMT1 IRE in the transport of lead in an in vitro BBB model Toxicol. In Vitro 2011 25 991 998
29. M. R. Basha W. Wei M. Brydie M. Razmiafshari N. H. Zawia Lead-induced developmental perturbations in hippocampal Sp1 DNA-binding are prevented by zinc supplementation: in vivo evidence for Pb and Zn competition Int. J. Dev. Neurosci. 2003 21 1 12
30. M. Razmiafshari J. Kao A. d'Avignon N. Zawia NMR Identification of Heavy Metal-Binding Sites in a Synthetic Zinc Finger Peptide: Toxicological Implications for the Interactions of Xenobiotic Metals with Zinc Finger Proteins Toxicol. Appl. Pharmacol. 2001 172 1 10
31. M. Razmiafshari N. Zawia Utilization of a Synthetic Peptide as a Tool to Study the Interaction of Heavy Metals with the Zinc Finger Domain of Proteins Critical for Gene Expression in the Developing Brain Toxicol. Appl. Pharmacol. 2000 166 1 12
32. G. R. Reddy N. Zawia Lead exposure alters Egr-1 DNA-binding in the neonatal rat brain Int. J. Dev. Neurosci. 2000 18 791 795
33. M. Huang D. Krepkiy D. H. Petering Zn-, Cd-, and Pb-transcription factor IIIA: properties, DNA binding, and comparison with TFIIIA-finger 3 metal complexes J. Inorg. Biochem. 2004 98 775 785
34. B. S. Sekhon Zinc finger proteins: an overview Natl. Acad. Sci. Lett. 2006 29 387 398
35. A. J. Courey R. Tijan Analysis of Sp1 in vivo reveals mutiple transcriptional domains, including a novel glutamine-rich activation motif Cell 1988 55 887 898
36. G. Suske The Sp-family of transcription factors Gene 1999 238 291 300
37. V. A. Narayan R. W. Kriwacki J. P. Caradonna Structures of Zinc Finger Domains from Transcription Factor Sp1: Insights into Sequence-Specific Protein-DNA Recognition J. Biol. Chem. 1997 272 7801 7809
38. J. M. Berg Sp1 and the subfamily of zinc finger proteins with guanine-rich binding sites Proc. Natl. Acad. Sci. U. S. A. 1992 89 11109 11110
39. J. D. Saffer S. P. Jackson M. B. Annarella Developmental expression of Sp1 in the mouse Mol. Cell. Biol. 1991 11 2189 2199
40. O. G. Opitz A. K. Rustgi Interaction between Sp1 and cell cycle regulatory proteins is important in transactivation of a differentiation-related gene Cancer Res. 2000 60 2825 2830
41. J. Kaczynski T. Cook R. Urrutia Sp1- and Krüppel-like transcription factors Genome Biol. 2003 4 206
42. S. Chu T. J. Ferro Sp1: regulation of gene expression by phosphorylation Gene 2005 348 1 11
43. K. A. Jones J. T. Kadonaga P. A. Luciw R. Tijan Activation of the AIDS retrovirus promoter by the cellular transcription factor, Sp1 Science 1986 232 755 759
44. Y. Bu Y. Suenaga S. Ono T. Koda F. Song A. Nakagawara T. Ozaki Sp1-mediated transcriptional regulation of NFBD1/MDC1 plays a critical role in DNA damage response pathway Sp1-mediated transactivation of NFBD1/MDC1 Genes Cells 2008 13 53 66
45. B. I. Milavetz SP1 and AP-1 Elements Direct Chromatin Remodeling in SV40 Chromosomes during the First 6 Hours of Infection Virology 2002 294 170 179
46. N. H. Zawia R. Sharan M. Brydie T. Oyama T. Crumpton Sp1 as a target site for metal-induced perturbations of transcriptional regulation of developmental brain gene expression Dev. Brain Res. 1998 107 291 298
47. J. S. Magyar T.-C. Weng C. M. Stern D. F. Dye B. W. Rous J. D. Payne B. M. Bridgewater A. Mijovilovish G. Parkin J. M. Zaleski J. E. Penner-Hahn H. A. Godwin Reexamination of Lead(ii) Coordination Preferences in Sulfur-Rich Sites: Implications for a Critical Mechanism of Lead Poisoning J. Am. Chem. Soc. 2005 127 9495 9505
48. N. Zawia G. J. Harry Developmental Exposure to Lead Interferes with Glial and Neuronal Differential Gene Expression in the Rat Cerebellum Toxicol. Appl. Pharmacol. 1996 138 43 47
49. D. Ben-Shachar R. Karry Sp1 Expression is Disrupted in Schizophrenia: A Possible Mechanism for the Abnormal Expression of Mitochondrial Complex I Genes, NDUFV1 and NDU FV2 PLoS One 2007 e871
50. L. Li J. Carter X. Gao J. Whitehead W. G. Tourtellotte The Neuroplasticity-Associated Arc Gene is a Direct Transcriptional Target of Early Growth Response (Egr) Transcription Factors Mol. Cell. Biol. 2005 25 10286 10300
51. M. W. Jones M. L. Errington A. Fine T. V. Bliss S. Garel P. Charnay B. Bozon S. Laroche S. Davis A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories Nat. Neurosci. 2001 4 289 296
52. J. S. Hanas J. S. Rodgers J. A. Bantle Y. G. Cheng Lead inhibition of DNA-binding mechanism of Cys2His2 zinc finger proteins Mol. Physiol. 1999 56 982 988
53. J. S. Hanas C. G. Gunn Inhibition of transcription factor IIIA-DNA interactions by xenobiotic metal ions Nucleic Acids Res. 1996 24 924 930
54. NIH, Alzheimer's Disease: Fact Sheet, National Institute on Aging, 2001
55. A. S. Association, 2014 Alzheimer's Disease Facts and Figures, 2014
56. C. M. Karch A. M. Goate Alzheimer's Disease Risk Genes and Mechanisms of Disease Pathogenesis Biol. Psychiatry 2015 77 43 51
57. D. M. Holtzman J. C. Morris A. M. Goate Alzheimer's Disease: The Challenge of the Second Century Sci. Transl. Med. 2011 3 77sr71
58. J. Hardy D. J. Selkoe The Amyloid Hypothesis of Alzheimer's Disease: Progress and Problems on the Road to Therapeutics Science 2002 297 353 356
59. M. Gatz N. L. Pedersen S. Berg B. Johansson K. Johansson J. A. Mortimer S. F. Posner M. Viitanen B. Winblad A. Ahlbom Heritability for Alzheimer's Disease: The Study of Dementia in Swedish Twins J. Gerontol., Ser. A 1997 52A M117 M125
60. J. S. Saczynski A. Beiser S. Seshadri S. Auerbach P. A. Wolf R. Au Depressive symptoms and risk of dementia: The Framingham Heart Study Neurology 2010 75 35 41
61. J. A. Luchsinger M.-X. Tang Y. Stern S. Shea R. Mayeux Diabetes Mellitus and Risk of Alzheimer's Disease and Dementia with Stroke in a Multiethnic Cohort Am. J. Epidemiol. 2001 154 635 641
62. B. L. Plassman R. J. Havlik D. C. Steffens M. J. Helms T. N. Newman D. Drosdick C. Phillips B. A. Gau K. A. Welsh-Bohmer J. R. Burke J. M. Guralnik J. C. Breitner Documented head injury in early adulthood and risk of Alzheimer's disease and other dementias Neurology 2000 55 1158 1166
63. M. G. Weisskopf R. O. Wright J. Schwartz A. Spiro D. Sparrow A. Aro H. Hu Cumulative Lead Exposure and Prospective Change in Cognition among Elderly Men: The VA Normative Aging Study Am. J. Epidemiol. 2004 160 1184 1193
64. R. O. Wright S. W. Tsaih J. Schwartz A. Spiro K. McDonald S. T. Weiss H. Hu Lead Exposure Biomarkers and Mini-Mental Status Exam Scores in Older Men Epidemiology 2003 14 713 718
65. R. A. Shih H. Hu M. G. Weisskopf B. S. Schwartz Cumulative Lead Dose and Cognitive Function in Adults: A Review of Studies That Measured Both Blood Lead and Bone Lead Environ. Health Perspect. 2006 115 483 492
66. M. Payton K. M. Riggs A. Spiro S. T. Weiss H. Hu Relations of Bone and Blood Lead to Cognitive Function: The VA Normative Aging Study Neurotoxicol. Teratol. 1998 20 19 27
67. M. G. Weisskopf H. Hu D. Sparrow R. E. Lenkinski R. O. Wright Proton Magnetic Resonance Spectroscopic Evidence of Glial Effects of Cumulative Lead Exposure in the Adult Human Hippocampus Environ. Health Perspect. 2007 115 519 523
68. S. W. Bihaqi A. Bahmani G. M. Subaiea N. H. Zawia Infantile exposure to lead and late-age cognitive decline: Relevance to AD Alzheimer's Dementia 2014 10 187 195
69. D. J. Selkoe Cell biology of the amyloid β-protein precursor and the mechanism of Alzheimer's disease Annu. Rev. Cell Biol. 1994 10 373 403
70. R. Izumi T. Yamada S. Yoshikai H. Sasaki M. Hattori Y. Sakaki Positive and negative regulatory elements for the expression of the Alzheimer's disease amyloid precursor-encoding gene in mouse Gene 1992 112 189 195
71. H. W. Querfurth J. Jiang W. Xia D. J. Selkoe Enhancer function and novel DNA binding protein activity in the near upstream βAPP gene promoter Gene 1999 232 125 141
72. W. J. Lukiw E. L. Rogaev L. Wong G. Vaula D. R. McLachlan P. St. George Hyslop Protein-DNA interactions in the promoter region of the amyloid precursor protein (APP) gene in human neocortex Mol. Brain Res. 1994 22 121 131
73. H. Gu X. Wei A. D. Monnot C. V. Fontanilla M. Behl M. R. Farlow W. Zheng Y. Du Lead exposure increases levels of β-amyloid in the brain and CSF and inhibits LRP1 expression in APP transgenic mice Neurosci. Lett. 2011 490 16 20
74. J. Wu M. R. Basha B. Brock D. P. Cox F. Cardozo-Pelaez C. A. McPherson J. Harry D. C. Rice B. Maloney D. Chen D. K. Lahiri N. Zawia Alzheimer's Disease (AD)-Like Pathology in Aged Monkeys after Infantile Exposure to Environmental Metal Lead (Pb): Evidence for a Developmental Origin and Environmental Link for AD J. Neurosci. 2008 28 3 9
75. R.-K. Lin Y. Wang Dysregulated transcriptional and post-translational control of DNA methyltransferases in cancer Cell Biosci. 2014 4 46
76. M. S. Wolfe W. Xia B. L. Ostaszewski T. S. Diehl W. T. Kimberly D. J. Selkoe Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and γ-secretase activity Nature 1999 398 513 517
77. K. Shirotani M. Tomioka E. Kremmer C. Haass H. Steiner Pathological activity of familial Alzheimer's disease-associated mutant presenilin can be executed by six different γ-secretase complexes Neurobiol. Dis. 2007 27 102 107
78. P. Renbaum R. Beeri E. Gabai M. Amiel M. Gai M. U. Ehrengruber E. Levy-Lahad Egr-1 upregulates the Alzheimer's disease presenilin-2 gene in neuronal cells Gene 2003 318 113 124
79. X.-F. Chen Y. Zhang H. Xu G. Bu Transcriptional regulation and its misregulation in Alzheimer's disease Mol. Brain 2013 6 44
80. A. E. Guttmacher F. S. Collins Alzheimer's Disease and Parkinson's Disease N. Engl. J. Med. 2003 348 1356 1364
81. J. Jankovic Parkinson's disease: clinical features and diagnosis J. Neurol., Neurosurg. Psychiatry 2008 79 368 376
82. C. Missale S. R. Nash S. W. Robinson M. Jaber M. G. Caron Dopamine receptors: from structure to function Physiol. Rev. 1998 78 189 225
83. K. H. Stansfield K. N. Ruby B. D. Soares J. L. McGlothan X. Liu T. R. Guilarte Early-life lead exposure recapitulates the selective loss of parvalbumin-positive GABAergic interneurons and subcortical dopamine system hyperactivity present in schizophrenia Transl. Psychiatry 2015 5 e522
84. C. Zuch D. J. O'Mara D. A. Cory-Slechta Low-Level Lead Exposure Selectively Enhances Dopamine Overflow in Nucleus Accumbens: An In Vivo Electrochemistry Time Course Assessment Toxicol. Appl. Pharmacol. 1998 150 174 185
85. C. Mehler-Wex P. Riederer M. Gerlach Dopaminergic dysbalance in distinct basal ganglia neurocircuits: implications for the pathophysiology of parkinson's disease, schizophrenia and attention deficit hyperactivity disorder Neurotoxic. Res. 2006 10 167 179
86. S. Yajima S. H. Lee T. Minowa M. M. Mouradian Sp family transcription factors regulate expression of rat D2 dopamine receptor gene DNA Cell Biol. 1998 17 471 479
87. C. K. Hwang U. M. D'Souza A. J. Eisch S. Yajima C.-H. Lammers Y. Yang S.-H. Lee Y.-M. Kim E. J. Nestler M. M. Mouradian Dopamine receptor regulating factor, DRRF: a zinc finger transcription factor Proc. Natl. Acad. Sci. U. S. A. 2001 98 7558 7563
88. S.-H. Lee M.-K. Jang O. H. Lee O. S. Kim Y.-M. Kim S. Yajima Y.-C. Lee M. M. Mouradian Transcriptional auto-regulation of the dopamine receptor regulating factor (DRRF) gene Mol. Cell. Endocrinol. 2008 289 23 28
89. K.-H. Lee Y.-D. Kwak D.-H. Kim M.-Y. Chang Y.-S. Lee Y.-S. Lee Human zinc finger protein 161, a novel transcriptional activator of the dopamine transporter Biochem. Biophys. Res. Commun. 2004 313 969 976
90. E. J. Bromet S. Fennig Epidemiology and natural history of schizophrenia Biol. Psychiatry 1999 46 871 881
91. E. Kringlen Twin studies in schizophrenia with special emphasis on concordance figures Am. J. Med. Genet. 2000 97 4 11
92. B. Abazyan J. Nomura G. Kannan K. Ishizuka K. L. Tamashiro F. Nucifora V. Pogorelov B. Ladenheim C. Yang I. N. Krasnova J. L. Cadet C. Pardo S. Mori A. Kamiya M. W. Vogel A. Sawa C. A. Ross M. V. Pletnikov Prenatal Interaction of Mutant DISC1 and Immune Activation Produces Adult Psychopathology Biol. Psychiatry 2010 68 1172 1181
93. E. S. Susser C. Schaefer A. S. Brown M. D. Begg R. J. Wyatt The design of the prenatal determinants of schizophrenia study Schizophr Bull. 2000 26 257 273
94. M. G. A. Opler S. Buka J. Groeger I. McKeague C. Wei P. Factor-Litvak M. Bresnahan J. Graziano J. M. Goldstein L. J. Seidman A. S. Brown E. S. Susser Prenatal exposure to lead, δ-aminolevulinic acid, and schizophrenia: further evidence Environ. Health Perspect. 2008 116 1586 1590
95. I. Pérez-Otaño M. D. Ehlers Homeostatic plasticity and NMDA receptor trafficking Trends Neurosci. 2005 28 229 238
96. C. Chen S. Tonegawa Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning, and memory in the mammalian brain. Annu. Rev. Neurosci. 1997 20 157 184
97. A. P. Neal T. R. Guilarte Mechanisms of lead and manganese neurotoxicity Toxicol. Res. 2013 2 99 114
98. A. P. Neal T. R. Guilarte Journal 2010 42 151 160
99. C. D. Toscano T. R. Guilarte Lead neurotoxicity: from exposure to molecular effects Brain Res. Rev. 2005 49 529 554
100. L. Adwan G. M. Subaiea N. H. Zawia Tolfenamic acid downregulates BACE1 and protects against lead-induced upregulation of Alzheimer's disease related biomarkers Neuropharmacology 2014 79 596 602
101. E. Karakas N. Simorowski H. Furukawa Structure of the zinc-bound amino-terminal domain of the NMDA receptor NR2B subunit EMBO J. 2009 28 3910 3920
102. T.-U. W. Woo J. P. Walsh F. M. Benes Density of Glutamic Acid Decarboxylase 67 Messenger RNA-Containing Neurons that Express the N -Methyl-d-Aspartate Receptor Subunit NR2A in the Anterior Cingulate Cortex in Schizophrenia and Bipolar Disorder Arch. Gen. Psychiatry 2004 61 649 657
103. G. Rosenbaum B. D. Cohen E. D. Luby J. S. Gottlieb Comparison of sernyl with other drugs: simulation of schizophrenic performance with sernyl, LSD-25, and amobarbital (amytal) sodium; I. Attention, motor function, and proprioception Arch. Gen. Psychiatry 1959 1 651 656
104. J. W. Olney J. W. Newcomer N. B. Farber NMDA receptor hypofunction model of schizophrenia J. Psychiat. Res. 1999 33 523 533
105. B. Riley D. Thiselton B. S. Maher T. Bigdeli B. Wormley G. O. McMichael A. H. Fanous V. Vladimirov F. A. O'Neill D. Walsh K. S. Kendler Replication of association between schizophrenia and ZNF804A in the Irish Case-Control Study of Schizophrenia sample Mol. Psychiatry 2010 15 29 37
106. M. J. Girgenti J. J. LoTurco B. J. Maher ZNF804a Regulates Expression of the Schizophrenia-Associated Genes PRSS16, COMT, PDE4B, and DRD2 PLoS One 2012 7 e32404
107. Y. Loe-Mie A. M. Lepagnol-Bestel G. Maussion A. Doron-Faigenboim S. Imbeaud H. Delacroix L. Aggerbeck T. Pupko P. Gorwood M. Simonneau J. M. Moalic SMARCA2 and other genome-wide supported schizophrenia-associated genes: regulation by REST/NRSF, network organization and primate-specific evolution Hum. Mol. Genet. 2010 19 2841 2857
108. M. C. O'Donovan Identification of loci associated with schizophrenia by genome-wide association and follow-up Nat. Genet. 2008 40 1053 1055
109. Y. Yang W. Li G. Yang B. Xiao X. Wang M. Ding J. Zhao X. Song W. Yue D. Zhang H. Zhang L. Lv Evaluation of the Relationship between the ZNF804A Single Nucleotide Polymorphism rs1344706 A/C Variant and Schizophrenia Subtype in Han Chinese Patients Int. J. Psychiatry Med. 2013 45 269 278
110. J. L. Hess T. P. Quinn S. Akbarian S. J. Glatt Bioinformatic analyses and conceptual synthesis of evidence linking to risk for schizophrenia and bipolar disorder Am. J. Med. Genet., Part B 2015 168 14 35
111. T. Hattori K. Baba S. Matsuzaki A. Honda K. Miyoshi K. Inoue M. Taniguchi H. Hashimoto N. Shintani A. Baba S. Shimizu F. Yukioka N. Kumamoto A. Yamaguchi M. Tohyama T. Katayama A novel DISC1-interacting partner DISC1-Binding Zinc-finger protein: implication in the modulation of DISC1-dependent neurite outgrowth Mol. Psychiatry 2007 12 398 407
112. J. K. Millar J. C. Wilson-Annan S. Anderson S. Christie M. S. Taylor C. A. Semple R. S. Devon D. M. St. Clair W. J. Muir D. H. Blackwood D. J. Porteous Disruption of two novel genes by a translocation co-segregating with schizophrenia Hum. Mol. Genet. 2000 9 1415 1423
113. N. A. Sachs A. Sawa S. E. Holmes C. A. Ross L. E. DeLisi R. L. Margolis A frameshift mutation in disrupted in Schizophrenia 1 in an American family with schizophrenia and schizoaffective disorder Mol. Psychiatry 2005 10 758 764
114. F. Du A. J. Cooper T. Thida A. K. Shinn B. M. Cohen D. Ongur Myelin and Axon Abnormalities in Schizophrenia Measured with Magnetic Resonance Imaging Techniques Biol. Psychiatry 2013 74 451 457
115. N. C. Papanikolaou E. G. Hatzidaki S. Belivanis G. N. Tzanakakis A. M. Tsatsakis Lead toxicity update, a brief review Med. Sci. Monit. 2005 11 RA329 RA336
116. M. A. Verity Comparative Observations on Inorganic and Organic Lead Neurotoxicity Environ. Health Perspect. 1990 89 43 48
117. E. Habibi A. Masoudi-Nejad H. M. Abdolmaleky S. J. Haggarty Emerging roles of epigenetic mechanisms in Parkinson's disease Funct. Integr. Genomics 2011 11 523 537
118. B. L. Vallee D. D. Ulmer Biochemical Effects of Mercury, Cadmium, and Lead Annu. Rev. Biochem. 1972 41 91 128
119. G. Flora D. Gupta A. Tiwari Toxicity of lead: a review with recent updates Interdiscipl. Toxicol. 2012 5 47
120. H.-Y. Wang E. Friedman Enhanced protein kinase C activity and translocation in bipolar affective disorder brains Biol. Psychiatry 1996 40 568 575
121. K. M. Chitty J. Lagopoulos I. B. Hickie D. F. Hermens Investigating the role of glutathione in mismatch negativity: an insight into NMDA receptor disturbances in bipolar disorder Clin. Neurophysiol. 2014 126 1178 1184