Genomic imprinting of Dopa decarboxylase in heart and reciprocal allelic expression with neighboring Grb10

Molecular and Cellular Biology

Volumn 28, Issue 1, 2008, Pages 386-396

  Menheniott, Trevelyan R ^a   Woodfine, Kathryn ^a   Schulz, Reiner ^a   Wood, Andrew J ^a   Monk, David ^b   Giraud, Andrew S ^d   Baldwin, H Scott ^c   Moore, Gudrun E ^b   Oakey, Rebecca J ^a,e  

^a GUY S HOSPITAL   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^d ROYAL CHILDREN'S HOSPITAL   (Australia)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC LEVO AMINO ACID DECARBOXYLASE;

ALLELE; ANIMAL TISSUE; ARTICLE; CHROMOSOME 11; CONTROLLED STUDY; EMBRYO; GENE; GENE DUPLICATION; GENE EXPRESSION; GENE OVEREXPRESSION; GENE SILENCING; GENETIC CONSERVATION; GENETIC LINKAGE; GENETIC TRANSCRIPTION; GENOME IMPRINTING; GRB10 GENE; HEART; HEART MUSCLE CELL; INTRON; METHYLATION; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION;

ADENOSINE TRIPHOSPHATASES; ALLELES; ANIMALS; BASE SEQUENCE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DOPA DECARBOXYLASE; EXONS; GENOMIC IMPRINTING; GRB10 ADAPTOR PROTEIN; HUMANS; MICE; MICE, TRANSGENIC; MYOCARDIUM; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; PROTEINS;

EID: 37549026512     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00862-07     Document Type: Article

References (71)

1. Adkins, N. L., T. A. Hagerman, and P. Georgel. 2006. GAGA protein: a multi-faceted transcription factor. Biochem. Cell Biol. 84:559-567.
2. Aguanno, A., R. Afar, and V. R. Albert. 1996. Tissue-specific expression of the nonneuronal promoter of the aromatic L-amino acid decarboxylase gene is regulated by hepatocyte nuclear factor 1. J. Biol. Chem. 271:4528-4538.
3. Aguanno, A., M. R. Lee, C. M. Marden, M. Rattray, A. Gault, and V. R. Albert. 1995. Analysis of the neuronal promoter of the rat aromatic L-amino acid decarboxylase gene. J. Neurochem. 65:1944-1954.
4. -/- females. Hum. Mol. Genet. 15:589-598.
5. Arnaud, P., D. Monk, M. Hitchins, E. Gordon, W. Dean, C. V. Beechey, J. Peters, W. Craigen, M. Preece, P. Stanier, G. E. Moore, and G. Kelsey. 2003. Conserved methylation imprints in the human and mouse GRB10 genes with divergent allelic expression suggests differential reading of the same mark. Hum. Mol. Genet. 12:1005-1019.
6. Beechey, C. V., S. T. Ball, K. M. Townsend, and J. Jones. 1997. The mouse chromosome 7 distal imprinting domain maps to G-bands F4/F5. Mamm. Genome 8:236-240.
7. Bell, A. C., and G. Felsenfeld. 2000. Methylation of a CTCF-dependent boundary controls imprinted expression of the Igf2 gene. Nature 405:482-485.
8. Bliek, J., P. Terhal, M. J. van den Bogaard, S. Maas, B. Hamel, G. Salieb- Beugelaar, M. Simon, T. Letteboer, J. van der Smagt, H. Kroes, and M. Mannens. 2006. Hypomethylation of the H19 gene causes not only Silver-Russell syndrome (SRS) but also isolated asymmetry or an SRS-like phenotype. Am. J. Hum. Genet. 78:604-614.
9. Borglum, A. D., T. G. Bruun, T. E. Kjeldsen, H. Ewald, O. Mors, G. Kirov, C. Russ, B. Freeman, D. A. Collier, and T. A. Kruse. 1999. Two novel variants in the DOPA decarboxylase gene: association with bipolar affective disorder. Mol. Psychiatry 4:545-551.
10. Borglum, A. D., G. Kirov, N. Craddock, O. Mors, W. Muir, V. Murray, I. McKee, D. A. Collier, H. Ewald, M. J. Owen, D. Blackwood, and T. A. Kruse. 2003. Possible parent-of-origin effect of Dopa decarboxylase in susceptibility to bipolar affective disorder. Am. J. Med. Genet. B 117:18-22.
11. Bourc'his, D., G. L. Xu, C. S. Lin, B. Bollman, and T. H. Bestor. 2001. Dnmt3L and the establishment of maternal genomic imprints. Science 294:2536-2539.
12. Charalambous, M., F. M. Smith, W. R. Bennett, T. E. Crew, F. Mackenzie, and A. Ward. 2003. Disruption of the imprinted Grb10 gene leads to disproportionate overgrowth by an Igf2-independent mechanism. Proc. Natl. Acad. Sci. USA 100:8292-8297.
13. Chatelin, S., R. Wehrle, P. Mercier, D. Morello, C. Sotelo, and M. J. Weber. 2001. Neuronal promoter of human aromatic L-amino acid decarboxylase gene directs transgene expression to the adult floor plate and aminergic nuclei induced by the isthmus. Brain Res. Mol. Brain Res. 97:149-160.
14. Choi, J. D., L. A. Underkoffler, A. J. Wood, J. N. Collins, P. T. Williams, J. A. Golden, E. F. Schuster, Jr., K. M. Loomes, and R. J. Oakey. 2005. A novel variant of Inpp5f is imprinted in brain, and its expression is correlated with differential methylation of an internal CpG island. Mol. Cell. Biol. 25:5514-5522.
15. Christenson, J. G., W. Dairman, and S. Udenfriend. 1972. On the identity of DOPA decarboxylase and 5-hydroxytryptophan decarboxylase (immunological titration-aromatic L-amino acid decarboxylase-serotonin-dopamine- norepinephrine). Proc. Natl. Acad. Sci. USA 69:343-347.
16. Cole, R. B., and S. E. Levin. 1973. Congenital heart disease associated with the Russell-Silver syndrome. S. Afr. Med. J. 47:989-990.
17. Constancia, M., W. Dean, S. Lopes, T. Moore, G. Kelsey, and W. Reik. 2000. Deletion of a silencer element in Igf2 results in loss of imprinting independent of H19. Nat. Genet. 26:203-206.
18. Constancia, M., M. Hemberger, J. Hughes, W. Dean, A. Ferguson-Smith, R. Fundele, F. Stewart, G. Kelsey, A. Fowden, C. Sibley, and W. Reik. 2002. Placental-specific IGF-II is a major modulator of placental and fetal growth. Nature 417:945-948.
19. DeChiara, T. M., E. J. Robertson, and A. Efstratiadis. 1991. Parental imprinting of the mouse insulin-like growth factor II gene. Cell 64:849-859.
20. Dugast-Darzacq, C., S. Egloff, and M. J. Weber. 2004. Cooperative dimerization of the POU domain protein Brn-2 on a new motif activates the neuronal promoter of the human aromatic L-amino acid decarboxylase gene. Brain Res. Mol. Brain Res. 120:151-163.
21. Kitzpatrick, G. V., P. D. Soloway, and M. J. Higgins. 2002. Regional loss of imprinting and growth deficiency in mice with a targeted deletion of KvDMR1. Nat. Genet. 32:426-431.
22. Gicquel, C., S. Rossignol, S. Cabrol, M. Houang, V. Steunou, V. Barbu, F. Danton, N. Thibaud, M. Le Merrer, L. Burglen, A. M. Bertrand, I. Netchine, and Y. Le Bouc. 2005. Epimutation of the telomeric imprinting center region on chromosome 11p15 in Silver-Russell syndrome. Nat. Genet. 37:1003-1007.
23. Hark, A. T., C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman. 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486-489.
24. Hawi, Z., D. Foley, A. Kirley, M. McCarron, M. Fitzgerald, and M. Gill. 2001. Dopa decarboxylase gene polymorphisms and attention deficit hyperactivity disorder (ADHD): no evidence for association in the Irish population. Mol. Psychiatry 6:420-424.
25. Hikichi, T., T. Kohda, T. Kaneko-Ishino, and F. Ishino. 2003. Imprinting regulation of the murine Meg1/Grb10 and human GRB10 genes: roles of brain-specific promoters and mouse-specific CTCF-binding sites. Nucleic Acids Res. 31:1398-1406.
26. Hitchins, M. P., L. Bentley, D. Monk, C. Beechey, J. Peters, G. Kelsey, F. Ishino, M. A. Preece, P. Stanier, and G. E. Moore. 2002. DDC and COBL, flanking the imprinted GRB10 gene on 7p12, are biallelically expressed. Mamm. Genome 13:686-691.
27. Hitchins, M. P., D. Monk, G. M. Bell, Z. Ali, M. A. Preece, P. Stanier, and G. E. Moore. 2001. Maternal repression of the human GRB10 gene in the developing central nervous system: evaluation of the role for GRB10 in Silver-Russell syndrome. Eur. J. Hum. Genet. 9:82-90.
28. Hitchins, M. P., P. Stanier, M. A. Preece, and G. E. Moore. 2001. Silver-Russell syndrome: a dissection of the genetic aetiology and candidate chromosomal regions. J. Med. Genet. 38:810-819.
29. Ichinose, H., and T. Nagatsu. 1993. Molecular genetics of aromatic L-amino acid decarboxylase. Yakubutsu Seishin Kodo 13:251-256. (In Japanese.)
30. Ichinose, H., T. Ohye, K. Fujita, F. Pantucek, K. Lange, P. Riederer, and T. Nagatsu. 1994. Quantification of mRNA of tyrosine hydroxylase and aromatic L-amino acid decarboxylase in the substantia nigra in Parkinson's disease and schizophrenia. J. Neural Transm. Park. Dis. Dement. Sect. 8:149-158.
31. Ichinose, H., C. Sumi-Ichinose, T. Ohye, Y. Hagino, K. Fujita, and T. Nagatsu. 1992. Tissue-specific alternative splicing of the first exon generates two types of mRNAs in human aromatic L-amino acid decarboxylase. Biochemistry 31:11546-11550.
32. Jahnes, E., D. J. Muller, T. G. Schulze, C. Windemuth, S. Cichon, S. Ohlraun, H. Fangerau, T. Held, W. Maier, P. Propping, M. M. Nothen, and M. Rietschel. 2002. Association study between two variants in the DOPA decarboxylase gene in bipolar and unipolar affective disorder. Am. J. Med. Genet. 114:519-522.
33. Kirley, A., Z. Hawi, G. Daly, M. McCarron, C. Mullins, N. Millar, I. Waldman, M. Fitzgerald, and M. Gill. 2002. Dopaminergic system genes in ADHD: toward a biological hypothesis. Neuropsychopharmacology 27:607-619.
34. Kobayashi, K., S. Merita, H. Sawada, T. Mizuguchi, K. Yamada, I. Nagatsu, T. Hata, Y. Watanabe, K. Fujita, and T. Nagatsu. 1995. Targeted disruption of the tyrosine hydroxylase locus results in severe catecholamine depletion and perinatal lethality in mice. J. Biol. Chem. 270:27235- 27243.
35. Kramer, H. H., H. J. Trampisch, S. Rammos, and A. Giese. 1990. Birth weight of children with congenital heart disease. Eur. J. Pediatr. 149:752-757.
36. Leighton, P. A., J. R. Saam, R. S. Ingram, C. L. Stewart, and S. M. Tilghman. 1995. An enhancer deletion affects both H19 and Igf2 expression. Genes Dev. 9:2079-2089.
37. Le Van Thai, A., E. Coste, J. M. Allen, R. D. Palmiter, and M. J. Weber. 1993. Identification of a neuron-specific promoter of human aromatic L-amino acid decarboxylase gene. Brain Res. Mol. Brain Res. 17:227-238.
38. Li, E., C. Beard, and R. Jaenisch. 1993. Role for DNA methylation in genomic imprinting. Nature 366:302-303.
39. Lin, S. P., N. Youngson, S. Takada, H. Seitz, W. Reik, M. Paulsen, J. Cavaille, and A. C. Ferguson-Smith. 2003. Asymmetric regulation of imprinting on the maternal and paternal chromosomes at the Dlk1-Gtl2 imprinted cluster on mouse chromosome 12. Nat. Genet. 35:97-102.
40. Mager, J., N. D. Montgomery, F. P. de Villena, and T. Magnuson. 2003. Genome imprinting regulated by the mouse Polycomb group protein Eed. Nat. Genet. 33:502-507.
41. Malik, S., M. A. Cleves, W. Zhao, A. Correa, and C. A. Hobbs. 2007. Association between congenital heart defects and small for gestational age. Pediatrics 119:e976-e982.
42. Mancini-Dinardo, D., S. J. Steele, J. M. Levorse, R. S. Ingram, and S. M. Tilghman. 2006. Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev. 20:1268-1282.
43. Monk, D., L. Bentley, M. Hitchins, R. A. Myler, J. Clayton-Smith, S. Ismail, S. M. Price, M. A. Preece, P. Stanier, and G. E. Moore. 2002. Chromosome 7p disruptions in Silver Russell syndrome: delineating an imprinted candidate gene region. Hum. Genet. 111:376-387.
44. Monk, D., E. L. Wakeling, V. Proud, M. Hitchins, S. N. Abu-Amero, P. Stanier, M. A. Preece, and G. E. Moore. 2000. Duplication of 7p11.2-p13, including GRB10, in Silver-Russell syndrome. Am. J. Hum. Genet. 66:36-46.
45. Moon, Y. S., C. M. Smas, K. Lee, J. A. Villena, K. H. Kim, E. J. Yun, and H. S. Sul. 2002. Mice lacking paternally expressed Pref-1/Dlk1 display growth retardation and accelerated adiposity. Mol. Cell. Biol. 22:5585-5592.
46. Moore, T., M. Constancia, M. Zubair, B. Bailleul, R. Feil, H. Sasaki, and W. Reik. 1997. Multiple imprinted sense and antisense transcripts, differential methylation and tandem repeats in a putative imprinting control region upstream of mouse Igf2. Proc. Natl. Acad. Sci. USA 94:12509-12514.
47. Mostoslavsky, R., N. Singh, T. Tenzen, M. Goldmit, C. Gabay, S. Elizur, P. Qi, B. E. Reubinoff, A. Chess, H. Cedar, and Y. Bergman. 2001. Asynchronous replication and allelic exclusion in the immune system. Nature 414:221-225.
48. Murrell, A., S. Heeson, L. Bowden, M. Constancia, W. Dean, G. Kelsey, and W. Reik. 2001. An intragenic methylated region in the imprinted Igf2 gene augments transcription. EMBO Rep. 2:1101-1106.
49. Nebigil, C. G., D. S. Choi, A. Dierich, P. Hickel, M. Le Meur, N. Messaddeq, J. M. Launay, and L. Maroteaux. 2000. Serotonin 2B receptor is required for heart development. Proc. Natl. Acad. Sci. USA 97:9508-9513.
50. Nebigil, C. G., and L. Maroteaux. 2001. A novel role for serotonin in heart. Trends Cardiovasc. Med. 11:329-335.
51. Omichinski, J. G., P. V. Pedone, G. Felsenfeld, A. M. Gronenborn, and G. M. Clore. 1997. The solution structure of a specific GAGA factor-DNA complex reveals a modular binding mode. Nat. Struct. Biol. 4:122-132.
52. Ono, R., K. Nakamura, K. Inoue, M. Naruse, T. Usami, N. Wakisaka-Saito, T. Hino, R. Suzuki-Migishima, N. Ogonuki, H. Miki, T. Kohda, A. Ogura, M. Yokoyama, T. Kaneko-Ishino, and F. Ishino. 2006. Deletion of Peg10, an imprinted gene acquired from a retrotransposon, causes early embryonic lethality. Nat. Genet. 38:101-106.
53. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
54. Plagge, A., and G. Kelsey. 2006. Imprinting the Gnas locus. Cytogenet. Genome Res. 113:178-187.
55. Portbury, A. L., R. Chandra, M. Groelle, M. K. McMillian, A. Elias, J. R. Herlong, M. Rios, S. Roffler-Tarlov, and D. M. Chikaraishi. 2003. Catecholamines act via a beta-adrenergic receptor to maintain fetal heart rate and survival. Am. J. Physiol. Heart Circ. Physiol. 284:H2069-H2077.
56. Rosenthal, G. L., P. D. Wilson, T. Permutt, J. A. Boughman, and C. Ferencz. 1991. Birth weight and cardiovascular malformations: a population-based study. The Baltimore-Washington Infant Study. Am. J. Epidemiol. 133:1273-1281.
57. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
58. Schmidt, J. V., P. G. Matteson, B. K. Jones, X. J. Guan, and S. M. Tilghman. 2000. The Dlk1 and Gtl2 genes are linked and reciprocally imprinted. Genes Dev. 14:1997-2002.
59. Schoenherr, C. J., J. M. Levorse, and S. M. Tilghman. 2003. CTCF maintains differential methylation at the Igf2/H19 locus. Nat. Genet. 33:66-69.
60. Schulz, R., T. R. Menheniott, K. Woodfine, A. J. Wood, J. D. Choi, and R. J. Oakey. 2006. Chromosome-wide identification of novel imprinted genes using microarrays and uniparental disomies. Nucleic Acids Res. 34:e88.
61. Sleutels, F., G. Tjon, T. Ludwig, and D. P. Barlow. 2003. Imprinted silencing of Slc22a2 and Slc22a3 does not need transcriptional overlap between Igf2r and Air. EMBO J. 22:3696-3704.
62. Sleutels, F., R. Zwart, and D. P. Barlow. 2002. The non-coding Air RNA is required for silencing autosomal imprinted genes. Nature 415:810-813.
63. Sumi-Ichinose, C., S. Hasegawa, H. Ichinose, H. Sawada, K. Kobayashi, M. Sakai, T. Fujii, H. Nomura, T. Nomura, I. Nagatsu, et al. 1995. Analysis of the alternative promoters that regulate tissue-specific expression of human aromatic L-amino acid decarboxylase. J. Neurochem. 64:514-524.
64. Sumi-Ichinose, C., H. Ichinose, E. Takahashi, T. Hori, and T. Nagatsu. 1992. Molecular cloning of genomic DNA and chromosomal assignment of the gene for human aromatic L-amino acid decarboxylase, the enzyme for catecholamine and serotonin biosynthesis. Biochemistry 31:2229-2238.
65. Surani, M. A., S. C. Barton, and M. L. Norris. 1986. Nuclear transplantation in the mouse: heritable differences between parental genomes after activation of the embryonic genome. Cell 45:127-136.
66. Thorvaldsen, J. L., K. L. Duran, and M. S. Bartolomei. 1998. Deletion of the H19 differentially methylated domain results in loss of imprinted expression of H19 and Igf2. Genes Dev. 12:3693-3702.
67. Wakeling, E. L., S. Abu-Amero, S. M. Price, P. Stanier, R. C. Trembath, G. E. Moore, and M. A. Preece. 1998. Genetics of Silver-Russell syndrome. Horm. Res. 49(Suppl. 2):32-36.
68. Wang, Z. Q., M. R. Fung, D. P. Barlow, and E. F. Wagner. 1994. Regulation of embryonic growth and lysosomal targeting by the imprinted Igf2/Mpr gene. Nature 372:464-467.
69. Wilkins, R. C., and J. T. Lis. 1998. GAGA factor binding to DNA via a single trinucleotide sequence element. Nucleic Acids Res. 26:2672-2678.
70. Yamasaki-Ishizaki, Y., T. Kayashima, C. K. Mapendano, H. Soejima, T. Ohta, H. Masuzaki, A. Kinoshita, T. Urano, K. Yoshiura, N. Matsumoto, T. Ishimaru, T. Mukai, N. Niikawa, and T. Kishino. 2007. Role of DNA methylation and histone H3 lysine 27 methylation in tissue-specific imprinting of mouse Grb10. Mol. Cell. Biol. 27:732-742.
71. Yang, T., T. E. Adamson, J. L. Resnick, S. Leff, R. Wevrick, U. Francke, N. A. Jenkins, N. G. Copeland, and C. I. Brannan. 1998. A mouse model for Prader-Willi syndrome imprinting-centre mutations. Nat. Genet. 19:25-31.