Differential effects of the HESR/HEY transcription factor family on dopamine transporter reporter gene expression via variable number of tandem repeats

Journal of Neuroscience Research

Volumn 89, Issue 4, 2011, Pages 562-575

  Kanno, Kouta ^a   Ishiura, Shoichi ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

Dopamine; Genetic polymorphism; Luciferase reporter assay; VNTR

Indexed keywords

DOPAMINE TRANSPORTER; LUCIFERASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HESR1; TRANSCRIPTION FACTOR HESR2; TRANSCRIPTION FACTOR HESR3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DOPAMINERGIC NERVE CELL; ENZYME ACTIVITY; EXON; GENE EXPRESSION; HUMAN; MALE; MESENCEPHALON; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; VARIABLE NUMBER OF TANDEM REPEAT;

ANIMALS; BASE SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; DOPAMINE PLASMA MEMBRANE TRANSPORT PROTEINS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NEURONS; POLYMORPHISM, GENETIC; REPRESSOR PROTEINS; TANDEM REPEAT SEQUENCES; TRANSFECTION;

EID: 79751496861     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.22593     Document Type: Article

References (71)

1. Bannon MJ, Michelhaugh SK, Wang J, Sacchetti P. 2001. The human dopamine transporter gene: gene organization, transcriptional regulation, and potential involvement in neuropsychiatric disorders. Eur Neuropsychopharmacol 11: 449-455.
2. Belandia B, Powell SM, Garcia-Pedrero JM, Walker MM, Bevan CL, Parker MG. 2005. Hey1, a mediator of notch signaling, is an androgen receptor corepressor. Mol Cell Biol 25: 1425-1436.
3. Bjorklund A, Dunnett SB. 2007. Dopamine neuron systems in the brain: an update. Trends Neurosci 30: 194-202.
4. Brookes KJ, Neale BM, Sugden K, Khan N, Asherson P, D'souza UM. 2007. Relationship between VNTR Polymorphisms of the human dopamine transporter gene and expression in post-mortem midbrain tissue. Am J Med Genet B Neuropsychiatr Genet 144B: 1070-1078.
5. 99m TRODAT-1 SPECT imaging. Am J Psychiatry 160: 1836-1841.
6. Caine SB. 1998. Cocaine abuse: hard knocks for the dopamine hypothesis? Nat Neurosci 1: 90-92.
7. Cook EH, Stein MA, Krasowski MD, Cox NJ, Olkon DM, Kieffer JE, Leventhal BL. 1995. Association of attention-deficit disorder and dopamine transporter gene. Am J Hum Genet 56: 993-998.
8. D'souza UM, Craig IW. 2008. Functional genetic polymorphisms in serotonin and dopamine gene systems and their significance in behavioural disorders. Prog Brain Res 172: 73-98.
9. Dahlqvist C, Blokzijl A, Chapman G, Falk A, Dannaeus K, Ibanez CF, Lendahl U. 2003. Functional notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 130: 6089-6099.
10. Farkas LM, Dunker N, Roussa E, Unsicker K, Krieglstein K. 2003. Transforming growth factor-beta s are essential for the development of midbrain dopaminergic neurons in vitro and in vivo. J Neurosci 23: 5178-5186.
11. Fauchey V, Jaber M, Caron MG, Bloch B, Le Moine C. 2000. Differential regulation of the dopamine D1, D2 and D3 receptor gene expression and changes in the phenotype of the striatal neurons in mice lacking the dopamine transporter. Eur J Neurosci 12: 19-26.
12. Fischer A, Gessler M. 2007. Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res 35: 4583-4596.
13. Fischer A, Schumacher N, Maier M, Sendtner M, Gessler M. 2004. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Gene Dev 18: 901-911.
14. Franklin KBJ, Paxinos G. 2008. The mouse brain in stereotaxic coordinates. Amsterdam: Elsevier/Academic Press.
15. Fuke S, Suo S, Takahashi N, Koike H, Sasagawa N, Ishiura S. 2001. The VNTR polymorphism of the human dopamine transporter (DAT1) gene affects gene expression. Pharmacogenomics J 1: 152-156.
16. Fuke S, Sasagawa N, Ishiura S. 2005. Identification and characterization of the Hesr1/Hey1 as a candidate trans-acting factor on gene expression through the 3' non-coding polymorphic region of the human dopamine transporter (DAT1) gene. J Biochem 137: 205-216.
17. Fuke S, Minami N, Kokubo H, Yoshikawa A, Yasumatsu H, Sasagawa N, Saga Y, Tsukahara T, Ishiura S. 2006. Hesr1 knockout mice exhibit behavioral alterations through the dopaminergic nervous system. J Neurosci Res 84: 1555-1563.
18. Gainetdinov RR, Sotnikova TD, Caron MG. 2002. Monoamine transporter pharmacology and mutant mice. Trends Pharmacol Sci 23: 367-373.
19. Giros B, Caron MG. 1993. Molecular characterization of the dopamine transporter. Trends Pharmacol Sci 14: 43-49.
20. Giros B, Elmestikawy S, Bertrand L, Caron MG. 1991. Cloning and functional characterization of a cocaine-sensitive dopamine transporter. FEBS Lett 295: 149-154.
21. Giros B, Elmestikawy S, Godinot N, Zheng KQ, Han H, Yangfeng T, Caron MG. 1992. Cloning, pharmacological characterization, and chromosome assignment of the human dopamine transporter. Mol Pharmacol 42: 383-390.
22. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG. 1996. Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379: 606-612.
23. Greenwood TA, Kelsoe JR. 2003. Promoter and intronic variants affect the transcriptional regulation of the human dopamine transporter gene. Genomics 82: 511-520.
24. Heinz A, Goldman D, Jones DW, Palmour R, Hommer D, Gorey JG, Lee KS, Linnoila M, Winberger DR. 2000. Genotype influences in vivo dopamine transporter availability in human striatum. Neuropsychopharmacology 22: 133-139.
25. Henderson AM, Wang SJ, Taylor AC, Aitkenhead M, Hughes CCW. 2001. The basic helix-loop-helix transcription factor HESR1 regulates endothelial cell tube formation. J Biol Chem 276: 6169-6176.
26. Inoue-Murayama M, Adachi S, Mishima N, Mitani H, Takenaka O, Terao K, Hayasaka I, Ito S, Murayama Y. 2002. Variation of variable number of tandem repeat sequences in the 3'-untransiated region of primate dopamine transporter genes that affects reporter gene expression. Neurosci Lett 334: 206-210.
27. Iso T, Sartorelli V, Poizat C, Iezzi S, Wu HY, Chung G, Kedes L, Hamamori Y. 2001. HERP, a novel heterodimer partner of HES/E(spl) in notch signaling. Mol Cell Biol 21: 6080-6089.
28. Iso T, Kedes L, Hamamori Y. 2003. HES and HERP families: Multiple effectors of the Notch signaling pathway. J Cell Physiol 194: 237-255.
29. Jaber M, Dumartin B, Sagne C, Haycock JW, Roubert C, Giros B, Bloch B, Caron MG. 1999. Differential regulation of tyrosine hydroxylase in the basal ganglia of mice lacking the dopamine transporter. Eur J Neurosci 11: 3499-3511.
30. Jackson DM, Westlinddanielsson A. 1994. Dopamine receptors: molecular biology, biochemistory and behavioral aspects. Pharmacol Ther 64: 291-370.
31. Jacobsen LK, Staley JK, Zoghbi S, Seibyl JP, Kosten TR, Innis RB, Gelernter J. 2000. Prediction of dopamine transporter binding availability by genotype: a preliminary report. Am J Psychiatry 157: 1700-1703.
32. Kilty JE, Lorang D, Amara SG. 1991. Cloning and expression of a cocaine-sensitive rat dopamine transporter. Science 254: 578-579.
33. Klenova E, Scott AC, Roberts J, Shamsuddin S, Lovejoy EA, Bergmann S, Bubb VJ, Royer HD, Quinn JP. 2004. YB-1 and CTCF differentially regulate the 5-HTT polymorphic intron 2 enhancer which predisposes to a variety of neurological disorders. J Neurosci 24: 5966-5973.
34. Kokubo H, Lun Y, Johnson RL. 1999. Identification and expression of a novel family of bHLH cDNAs related to Drosophila hairy and enhancer of split. Biochem Biophys Res Commun 260: 459-465.
35. Kokubo H, Miyagawa-Tomita S, Tomimatsu H, Nakashima Y, Nakazawa M, Saga Y, Johnson RL. 2004. Targeted disruption of hesr2 results in atrioventricular valve anomalies that lead to heart dysfunction. Circ Res 95: 540-547.
36. Kokubo H, Miyagawa-Tomita S, Nakazawa M, Saga Y, Johnson RL. 2005. Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev Biol 278: 301-309.
37. Kokubo H, Tomita-Miyagawa S, Hamada Y, Saga Y. 2007. Hesr1 and Hesr2 regulate atrioventricular boundary formation in the developing heart through the repression of Tbx2. Development 134: 747-755.
38. Kouzmenko AP, Pereira AM, Singh BS. 1997. Intronic sequences are involved in neural targeting of human dopamine transporter gene expression. Biochem Biophys Res Commun 240: 807-811.
39. Krause KH, Dresel SH, Krause J, la Fougere C, Ackenheil M. 2003. The dopamine transporter and neuroimaging in attention deficit hyperactivity disorder. Neurosci Biobehav Rev 27: 605-613.
40. Leimeister C, Externbrink A, Klamt B, Gessler M. 1999. Hey genes: a novel subfamily of hairy- and Enhancer of split related genes specifically expressed during mouse embryogenesis. Mech Dev 85: 173-177.
41. Madras BK, Gracz LM, Fahey MA, Elmaleh D, Meltzer PC, Liang AY, Stopa EG, Babich J, Fischman AJ. 1998. Altropane, a SPECT or PET imaging probe for dopamine neurons: III. Human dopamine transporter in postmortem normal and Parkinson's diseased brain. Synapse 29: 116-127.
42. Martinez D, Gelernter J, Abi-Dargham A, van Dyck CH, Kegeles L, Innis RB, Laruelle M. 2001. The variable number of tandem repeats polymorphism of the dopamine transporter gene is not associated with significant change in dopamine transporter phenotype in humans. Neuropsychopharmacology 24: 553-560.
43. Michelhaugh SK, Fiskerstrand C, Lovejoy E, Bannon MJ, Quinn JP. 2001. The dopamine transporter gene (SLC6A3) variable number of tandem repeats domain enhances transcription in dopamine neurons. J Neurochem 79: 1033-1038.
44. Mill J, Asherson P, Browes C, D'souza U, Craig I. 2002. Expression of the dopamine transporter gene is regulated by the 3' UTR VNTR: evidence from brain and lymphocytes using quantitative RT-PCR. Am J Med Genet B Neuropsychiatr Genet 114B: 975-979.
45. Mill J, Asherson P, Craig I, D'souza UM. 2005. Transient expression analysis of allelic variants of a VNTR in the dopamine transporter gene (DAT1). BMC Genet 6.
46. Miller GM, Madras BK. 2002. Polymorphisms in the 3'-untranslated region of human and monkey dopamine transporter genes affect reporter gene expression. Mol Psychiatry 7: 44-55.
47. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG. 1998. Dopamine receptors: From structure to function. Physiol Rev 78: 189-225.
48. Muller-Vahl KR, Berding G, Brucke T, Kolbe H, Meyer GJ, Hundeshagen H, Dengler R, Knapp WH, Emrich HM. 2000. Dopamine transporter binding in Gilles de la Tourette syndrome. JNeurol 247: 514-520.
49. Nakagawa O, Nakagawa M, Richardson JA, Olson EN, Srivastava D. 1999. HRT1, HRT2, and HRT3: a new subclass of bHLH transcription factors marking specific cardiac, somitic, and pharyngeal arch segments. Dev Biol 216: 72-84.
50. Nakagawa O, McFadden DG, Nakagawa M, Yanagisawa H, Hu TH, Srivastava D, Olson EN. 2000. Members of the HRT family of basic helix-loop-helix proteins act as transcriptional repressors downstream of Notch signaling. Proc Natl Acad Sci U S A 97: 13655-13660.
51. Nakamura Y, Koyama K, Matsushima M. 1998. VNTR (variable number of tandem repeat) sequences as transcriptional, translational, or functional regulators. J Hum Genet 43: 149-152.
52. Ohadi M, Shirazi E, Tehranidoosti M, Moghimi N, Keikhaee MR, Ehssani S, Aghajani A, Najrnabadi H. 2006. Attention-deficit/hyperactivity disorder (ADHD) association with the DAT1 core promoter-67 T allele. Brain Res 1101: 1-4.
53. Ohadi M, Keikhaee MR, Javanbakht A, Sargolzaee MR, Robabeh M, Najmabadi H. 2007. Gender dimorphism in the DAT1-67 T-allele homozygosity and predisposition to bipolar disorder. Brain Res 1144: 142-145.
54. Roberts J, Scott AC, Howard MR, Breen G, Bubb VJ, Klenova E, Quinn JP. 2007. Differential regulation of the serotonin transporter gene by lithium is mediated by transcription factors, CCCTC binding protein and Y-box binding protein 1, through the polymorphic intron 2 variable number tandem repeat. J Neurosci 27: 2793-2801.
55. Sacchetti P, Brownschidle LA, Granneman GJ, Bannon MJ. 1999. Characterization of the 5'-flanking region of the human dopamine transporter gene. Brain Res Mol Brain Res 74: 167-174.
56. Sakamoto M, Hirata H, Ohtsuka T, Bessho Y, Kageyama R. 2003. The basic helix-loop-helix genes Hesr1/Hey1 and Hesr2/Hey2 regulate maintenance of neural precursor cells in the brain. J Biol Chem 278: 44808-44815.
57. Sanchez-Capelo A, Colin P, Guibert B, Biguet NF, Mallet J. 2003. Transforming growth factor beta 1 overexpression in the nigrostriatal system increases the dopaminergic deficit of MPTP mice. Mol Cell Neurosci 23: 614-625.
58. Shibuya N, Kamata M, Suzuki A, Matsumoto Y, Goto K, Otani K. 2009. The-67 A/T promoter polymorphism in the dopamine transporter gene affects personality traits of Japanese healthy females. Behav Brain Res 203: 23-26.
59. Shimada S, Kitayama S, Lin CL, Patel A, Nanthakumar E, Gregor P, Kuhar M, Uhl G. 1991. Cloning and expression of a cocaine-sensitive dopamine transporter complementary DNA. Science 254: 576-578.
60. Steidl C, Leimeister C, Klamt B, Maier M, Nanda I, Dixon M, Clarke R, Schmid M, Gessler M. 2000. Characterization of the human and mouse HEY1, HEY2, and HEYL genes: Cloning, mapping, and mutation screening of a new bHLH gene family. Genomics 66: 195-203.
61. Stull ND, Jung JW, Iacovitti L. 2001. Induction of a dopaminergic phenotype in cultured striatal neurons by bone morphogenetic proteins. Brain Res Dev Brain Res 130: 91-98.
62. Takizawa T, Ochiai W, Nakashima K, Taga T. 2003. Enhanced gene activation by Notch and BMP signaling cross-talk. Nucleic Acids Res 31: 5723-5731.
63. Ueno S. 2003. Genetic polymorphisms of serotonin and dopamine transporters in mental disorders. J Med Invest 50: 25-31.
64. Ueno S, Nakamura M, Mikami M, Kondoh K, Ishiguro H, Arinami T, Komiyama T, Mitsushio H, Sano A, Tanabe H. 1999. Identification of a novel polymorphism of the human dopamine transporter (DAT1) gene and the significant association with alcoholism. Mol Psychiatry 4: 552-557.
65. Uhl GR. 2003. Dopamine transporter: Basic science and human variation of a key molecule for dopaminergic function, locomotion, and parkinsonism. Mov Disord 18: S71-S80.
66. Vandenbergh DJ, Persico AM, Hawkins AL, Griffin CA, Li X, Jabs EW, Uhl GR. 1992. Human dopamine transporter gene (DAT1) maps to chromosome 5p15.3 and displays a VNTR. Genomics 14: 1104-1106.
67. Vandenbergh DJ, Thompson MD, Cook EH, Bendahhou E, Nguyen T, Krasowski MD, Zarrabian D, Comings D, Sellers EM, Tyndale RF, George SR, O'Dowd BF, Uhl GR. 2000. Human dopamine transporter gene: coding region conservation among normal, Tourette's disorder, alcohol dependence and attention-deficit hyperactivity disorder populations. Mol Psychiatry 5: 283-292.
68. VanNess SH, Owens MJ, Kilts CD. 2005. The variable number of tandem repeats element in DATI regulates in vitro dopamine transporter density. BMC Genet 6.
69. Villaronga MA, Lavery DN, Bevan CL, Llanos S, Belandia B. 2010. HEY1 Leu94Met gene polymorphism dramatically modifies its biological functions. Oncogene 29: 411-420.
70. Wang WL, Campos AH, Prince CZ, Mou YS, Pollman MJ. 2002. Coordinate Notch3-hairy-related transcription factor pathway regulation in response to arterial injury-mediator role of platelet-derived growth factor and ERK. J Biol Chem 277: 23165-23171.
71. Zavadil J, Cermak L, Soto-Nieves N, Bottinger EP. 2004. Integration of TGF-beta/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. EMBO J 23: 1155-1165.