Functional analysis of a potassium-chloride co-transporter 3 (SLC12A6) promoter polymorphism leading to an additional DNA methylation site

Neuropsychopharmacology

Volumn 34, Issue 2, 2009, Pages 458-467

  Moser, Dirk ^a   Ekawardhani, Savira ^a   Kumsta, Robert ^a   Palmason, Haukur ^a   Bock, Christoph ^b   Athanassiadou, Zoi ^c   Lesch, Klaus Peter ^c   Meyer, Jobst ^a  

^a UNIVERSITY OF TRIER   (Germany)

^b MAX PLANCK INSTITUTE FOR INFORMATICS   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Bipolar disorder; DNA methylation; Epigenetics; Gene x environment interaction; Periodic catatonia; SLC12A6

Indexed keywords

CYTOSINE; GUANINE;

ALLELE; ARTICLE; BIPOLAR DISORDER; DNA EXTRACTION; DNA METHYLATION; DNA SEQUENCE; EPIGENETICS; GENE; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENOTYPE ENVIRONMENT INTERACTION; HUMAN; HUMAN CELL; LYMPHOCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SLCI2A6 GENE;

BIPOLAR DISORDER; CELL LINE; CPG ISLANDS; DNA METHYLATION; EPIGENESIS, GENETIC; GENES, REPORTER; HUMANS; LYMPHOCYTES; MOLECULAR SEQUENCE DATA; PLASMIDS; POLYMERASE CHAIN REACTION; POLYMORPHISM, SINGLE NUCLEOTIDE; PROMOTER REGIONS, GENETIC; SEQUENCE ANALYSIS, PROTEIN; SYMPORTERS;

EID: 57849159039     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/npp.2008.77     Document Type: Article

References (68)

1. Abdolmaleky HM, Cheng KH, Faraone SV, Wilcox M, Glatt SJ, Gao F et al (2006). Hypomethylation of MB-COMT promoter is a major risk factor for schizophrenia and bipolar disorder. Hum Mol Genet 15: 3132-3145.
2. Abdolmaleky HM, Cheng KH, Russo A, Smith CL, Faraone SV, Wilcox M et al (2005). Hypermethylation of the reelin (RELN) promoter in the brain of schizophrenic patients: a preliminary report. Am J Med Genet B Neuropsychiatr Genet 134: 60-66.
3. Abdolmaleky HM, Smith CL, Faraone SV, Shafa R, Stone W, Glatt SJ et al (2004). Methylomics in psychiatry: modulation of gene-environment interactions may be through DNA methylation. Am J Med Genet B Neuropsychiatr Genet 127: 51-59.
4. Alonso-Aperte E, Ubeda N, Achon M, Perez-Miguelsanz J, Varela-Moreiras G (1999). Impaired methionine synthesis and hypomethylation in rats exposed to valproate during gestation. Neurology 52: 750-756.
5. Attwood JT, Yung RL, Richardson BC (2002). DNA methylation and the regulation of gene transcription. Cell Mol Life Sci 59: 241-257.
6. Bianchetti MG, Bettinelli A, Oetliker OH, Sereni F (1992). Calciuria in Bartter's and similar syndromes. Clin Nephrol 38: 338.
7. Bock C, Paulsen M, Tierling S, Mikeska T, Lengauer T, Walter J (2006). CpG island methylation in human lymphocytes is highly correlated with DNA sequence, repeats, and predicted DNA structure. PLoS Genet 2: e26.
8. Bock C, Walter J, Paulsen M, Lengauer T (2007). CpG island mapping by epigenome prediction. PLoS Comput Biol 3: e110.
9. Bock C, Walter J, Paulsen M, Lengauer T (2008). Inter-individual variation of DNA methylation and its implications for large-scale epigenome mapping. Nucleic Acids Res. doi: 10.1093/nar/gkn122.
10. Boettger T, Hubner CA, Maier H, Rust MB, Beck FX, Jentsch TJ (2002). Deafness and renal tubular acidosis in mice lacking the K-Cl co-transporter Kcc4. Nature 416: 874-878.
11. Boettger T, Rust MB, Maier H, Seidenbecher T, Schweizer M, Keating DJ et al (2003). Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. EMBO J 22: 5422-5434.
12. Cannon TD (2005). The inheritance of intermediate phenotypes for schizophrenia. Curr Opin Psychiatry 18: 135-140.
13. de Kloet ER, Joels M, Holsboer F (2005). Stress and the brain: from adaptation to disease. Nat Rev Neurosci 6: 463-475.
14. Delpire E, Mount DB (2002). Human and murine phenotypes associated with defects in cation-chloride cotransport. Annu Rev Physiol 64: 803-843.
15. Di Fulvio M, Lincoln TM, Lauf PK, Adragna NC (2001). Protein kinase G regulates potassium chloride cotransporter-4 [corrected] expression in primary cultures of rat vascular smooth muscle cells. J Biol Chem 276: 21046-21052.
16. Dupre N, Howard HC, Mathieu J, Karpati G, Vanasse M, Bouchard JP et al (2003). Hereditary motor and sensory neuropathy with agenesis of the corpus callosum. Ann Neurol 54: 9-18.
17. Eckhardt F, Lewin J, Cortese R, Rakyan VK, Attwood J, Burger M et al (2006). DNA methylation profiling of human chromosomes 6, 20 and 22. Nat Genet 38: 1378-1385.
18. Elmslie F (1997a). Gene table: epilepsy. Eur J Paediatr Neurol 1: 55-57.
19. Elmslie FV, Rees M, Williamson MP, Kerr M, Kjeldsen MJ, Pang KA et al (1997). Genetic mapping of a major susceptibility locus for juvenile myoclonic epilepsy on chromosome 15q. Hum Mol Genet 6: 1329-1334.
20. Elmslie KS (1997b). Identification of the single channels that underlie the N-type and L-type calcium currents in bullfrog sympathetic neurons. J Neurosci 17: 2658-2668.
21. Escher G, Hoang A, Georges S, Tchoua U, El-Osta A, Krozowski Z et al (2005). Demethylation using the epigenetic modifier, 5-azacytidine, increases the efficiency of transient transfection of macrophages. J Lipid Res 46: 356-365.
22. Filteau MJ, Pourcher E, Bouchard RH, Baruch P, Mathieu J, Bedard F et al (1991). Corpus callosum agenesis and psychosis in Andermann syndrome. Arch Neurol 48: 1275-1280.
23. Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML et al (2005). Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci USA 102: 10604-10609.
24. Frommer M, McDonald LE, Millar DS, Collis CM, Watt F, Grigg GW et al (1992). A genomic sequencing protocol that yields a positive display of 5-methylcytosine residues in individual DNA strands. Proc Natl Acad Sci USA 89: 1827-1831.
25. Gamba G (2005). Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol Rev 85: 423-493.
26. Gitelman HJ, Graham JB, Welt LG (1966). A new familial disorder characterized by hypokalemia and hypomagnesemia. Trans Assoc Am Physicians 79: 221-235.
27. Gordon RD (1986). Syndrome of hypertension and hyperkalemia with normal glomerular filtration rate. Hypertension 8: 93-102.
28. Grayson DR, Chen Y, Costa E, Dong E, Guidotti A, Kundakovic M et al (2006). The human reelin gene: transcription factors (+), repressors (-) and the methylation switch (+/-) in schizophrenia. Pharmacol Ther 111: 272-286.
29. Grayson DR, Jia X, Chen Y, Sharma RP, Mitchell CP, Guidotti A et al (2005). Reelin promoter hypermethylation in schizophrenia. Proc Natl Acad Sci USA 102: 9341-9346.
30. Grunau C, Clark SJ, Rosenthal A (2001). Bisulfite genomic sequencing: systematic investigation of critical experimental parameters. Nucleic Acids Res 29: E65-E65.
31. Hiki K, D'Andrea RJ, Furze J, Crawford J, Woollatt E, Sutherland GR et al (1999). Cloning, characterization, and chromosomal location of a novel human K+-Cl- cotransporter. J Biol Chem 274: 10661-10667.
32. Howard HC, Dube MP, Prevost C, Bouchard JP, Mathieu J, Rouleau GA (2002a). Fine mapping the candidate region for peripheral neuropathy with or without agenesis of the corpus callosum in the French Canadian population. Eur J Hum Genet 10: 406-412.
33. Howard HC, Dupre N, Mathieu J, Bouchard JP, Rouleau GA (2003). Severe neuropathy with agenesis of the corpus callosum. Med Sci (Paris) 19: 414-416.
34. Howard HC, Mount DB, Rochefort D, Byun N, Dupre N, Lu J et al (2002b). The K-Cl cotransporter KCC3 is mutant in a severe peripheral neuropathy associated with agenesis of the corpus callosum. Nat Genet 32: 384-392.
35. Hubner CA, Stein V, Hermans-Borgmeyer I, Meyer T, Ballanyi K, Jentsch TJ (2001). Disruption of KCC2 reveals an essential role of K-Cl cotransport already in early synaptic inhibition. Neuron 30: 515-524.
36. Isohanni M, Jones PB, Moilanen K, Rantakallio P, Veijola J, Oja H et al (2001). Early developmental milestones in adult schizophrenia and other psychoses. A 31-year follow-up of the Northern Finland 1966 Birth Cohort. Schizophr Res 52: 1-19.
37. Jaenisch R, Bird A (2003). Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 33(Suppl): 245-254.
38. Jentsch TJ (2005). Chloride transport in the kidney: lessons from human disease and knockout mice. J Am Soc Nephrol 16: 1549-1561.
39. Jones P, Rodgers B, Murray R, Marmot M (1994). Child development risk factors for adult schizophrenia in the British 1946 birth cohort. Lancet 344: 1398-1402.
40. Kohn Y (2005). Focus on rare genetic variants in bipolar disorder: how outliers help understand complex disorders. Int J Neuropsychopharmacol 8: 491-493.
41. Liu X, Jorgenson E, Witte JS (2005). Hierarchical modeling in association studies of multiple phenotypes. BMC Genet 6(Suppl 1): S104.
42. Mercado A, Mount DB, Gamba G (2004). Electroneutral cation-chloride cotransporters in the central nervous system. Neurochem Res 29: 17-25.
43. Mercado A, Vazquez N, Song L, Cortes R, Enck AH, Welch R et al (2005). NH2-terminal heterogeneity in the KCC3 K+-Cl-cotransporter. Am J Physiol Renal Physiol 289: F1246-F1261.
44. Meyer J, Johannssen K, Freitag CM, Schraut K, Teuber I, Hahner A et al (2005). Rare variants of the gene encoding the potassium chloride co-transporter 3 are associated with bipolar disorder. Int J Neuropsychopharmacol 8: 495-504.
45. Miller SA, Dykes DD, Polesky HF (1988). A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16: 1215.
46. Moser D, Molitor A, Kumsta R, Tatschner T, Riederer P, Meyer J (2007). The glucocorticoid receptor gene exon 1-F promoter is not methylated at the NGFI-A binding site in human hippocampus. World J Biol Psychiatry 8: 262-268.
47. Mount DB, Mercado A, Song L, Xu J, George Jr AL, Delpire E et al (1999). Cloning and characterization of KCC3 and KCC4, new members of the cation-chloride cotransporter gene family. J Biol Chem 274: 16355-16362.
48. Murrell A, Heeson S, Cooper WN, Douglas E, Apostolidou S, Moore GE et al (2004). An association between variants in the IGF2 gene and Beckwith-Wiedemann syndrome: interaction between genotype and epigenotype. Hum Mol Genet 13: 247-255.
49. Peaston AE, Whitelaw E (2006). Epigenetics and phenotypic variation in mammals. Mamm Genome 17: 365-374.
50. Race JE, Makhlouf FN, Logue PJ, Wilson FH, Dunham PB, Holtzman EJ (1999). Molecular cloning and functional characterization of KCC3, a new K-Cl cotransporter. Am J Physiol 277: C1210-C1219.
51. Rakyan VK, Beck S (2006). Epigenetic variation and inheritance in mammals. Curr Opin Genet Dev 16: 573-577.
52. Reif A, Herterich S, Strobel A, Ehlis AC, Saur D, Jacob CP et al (2006). A neuronal nitric oxide synthase (NOS-I) haplotype associated with schizophrenia modifies prefrontal cortex function. Mol Psychiatry 11: 286-300.
53. Rust MB, Faulhaber J, Budack MK, Pfeffer C, Maritzen T, Didie M et al (2006). Neurogenic mechanisms contribute to hypertension in mice with disruption of the K-Cl cotransporter KCC3. Circ Res 98: 549-556.
54. Sander T, Kretz R, Williamson MP, Elmslie FV, Rees M, Hildmann T et al (1997). Linkage analysis between idiopathic generalized epilepsies and the GABA(A) receptor alpha5, beta3 and gamma3 subunit gene cluster on chromosome 15. Acta Neurol Scand 96: 1-7.
55. Saur D, Vanderwinden JM, Seidler B, Schmid RM, De Laet MH, Allescher HD (2004). Single-nucleotide promoter polymorphism alters transcription of neuronal nitric oxide synthase exon 1c in infantile hypertrophic pyloric stenosis. Proc Natl Acad Sci USA 101: 1662-1667.
56. Shen MR, Chou CY, Hsu KF, Liu HS, Dunham PB, Holtzman EJ et al (2001). The KCl cotransporter isoform KCC3 can play an important role in cell growth regulation. Proc Natl Acad Sci USA 98: 14714-14719.
57. Shen MR, Lin AC, Hsu YM, Chang TJ, Tang MJ, Alper SL et al (2004). Insulin-like growth factor 1 stimulates KCl cotransport, which is necessary for invasion and proliferation of cervical cancer and ovarian cancer cells. J Biol Chem 279: 40017-40025.
58. Shimabukuro M, Jinno Y, Fuke C, Okazaki Y (2006). Haloperidol treatment induces tissue- and sex-specific changes in DNA methylation: a control study using rats. Behav Brain Funct 2: 37.
59. Song F, Smith JF, Kimura MT, Morrow AD, Matsuyama T, Nagase H et al (2005). Association of tissue-specific differentially methylated regions (TDMs) with differential gene expression. Proc Natl Acad Sci USA 102: 3336-3341.
60. Stober G, Pfuhlmann B, Nurnberg G, Schmidtke A, Reis A, Franzek E et al (2001). Towards the genetic basis of periodic catatonia: pedigree sample for genome scan I and II. Eur Arch Psychiatry Clin Neurosci 251(Suppl 1): I25-I30.
61. Stober G, Saar K, Ruschendorf F, Meyer J, Nurnberg G, Jatzke S et al (2000). Splitting schizophrenia: periodic catatonia-susceptibility locus on chromosome 15q15. Am J Hum Genet 67: 1201-1207.
62. Tsankova N, Renthal W, Kumar A, Nestler EJ (2007). Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 8: 355-367.
63. Uyanik G, Elcioglu N, Penzien J, Gross C, Yilmaz Y, Olmez A et al (2006). Novel truncating and missense mutations of the KCC3 gene associated with Andermann syndrome. Neurology 66: 1044-1048.
64. Vinogradov AE (2005). Dualism of gene GC content and CpG pattern in regard to expression in the human genome: magnitude versus breadth. Trends Genet 21: 639-643.
65. Weaver IC, Cervoni N, Champagne FA, D'Alessio AC, Sharma S, Seckl JR et al (2004). Epigenetic programming by maternal behavior. Nat Neurosci 7: 847-854.
66. Weaver IC, Champagne FA, Brown SE, Dymov S, Sharma S, Meaney MJ et al (2005). Reversal of maternal programming of stress responses in adult offspring through methyl supplementation: altering epigenetic marking later in life. J Neurosci 25: 11045-11054.
67. Weinberger DR (1995). From neuropathology to neurodevelopment. Lancet 346: 552-557.
68. Wolff GL, Kodell RL, Moore SR, Cooney CA (1998). Maternal epigenetics and methyl supplements affect agouti gene expression in Avy/a mice. FASEB J 12: 949-957.