Drosophila Ube3a regulates monoamine synthesis by increasing GTP cyclohydrolase I activity via a non-ubiquitin ligase mechanism

Neurobiology of Disease

Volumn 41, Issue 3, 2011, Pages 669-677

  Ferdousy, Faiza ^a   Bodeen, William ^b   Summers, Kyle ^b   Doherty, Olugbenga ^a   Wright, O'Neil ^a   Elsisi, Nahed ^b   Hilliard, George ^b   O'Donnell, Janis M ^a   Reiter, Lawrence T ^b  

^a UNIVERSITY OF ALABAMA   (United States)

^b UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Angelman syndrome; Autism; Dopamine; GTPCH1; Transcriptional co activation; UBE3A; Ubiquitin ligase activity

Indexed keywords

DOPAMINE; DROSOPHILA PROTEIN; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; PROTEIN DUBE3A; TETRAHYDROBIOPTERIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BRAIN; CONTROLLED STUDY; DOPAMINE METABOLISM; DROSOPHILA; ENZYME ACTIVE SITE; ENZYME ACTIVITY; FEMALE; GENE CONTROL; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; UBIQUITINATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DOPAMINE; DROSOPHILA; DROSOPHILA PROTEINS; ENZYME ACTIVATION; FEMALE; GTP CYCLOHYDROLASE; HUMANS; MALE; MUTATION; SEROTONIN; UBIQUITIN-PROTEIN LIGASES; UP-REGULATION;

EID: 79151474498     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2010.12.001     Document Type: Article

References (51)

1. Albrecht U., et al. Imprinted expression of the murine Angelman syndrome gene, Ube3a, in hippocampal and Purkinje neurons. Nat. Genet. 1997, 17:75-78.
2. Axelrod J. Noradrenaline: fate and control of its biosynthesis. Science 1971, 173:598-606.
3. Baron C.A., et al. Genomic and functional profiling of duplicated chromosome 15 cell lines reveal regulatory alterations in UBE3A-associated ubiquitin-proteasome pathway processes. Hum. Mol. Genet. 2006, 15:853-869.
4. Brand A.H., Perrimon N. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 1993, 118:401-415.
5. Canitano R., Scandurra V. Risperidone in the treatment of behavioral disorders associated with autism in children and adolescents. Neuropsychiatr. Dis. Treat. 2008, 4:723-730.
6. Carbone M.A., et al. Phenotypic variation and natural selection at catsup, a pleiotropic quantitative trait gene in Drosophila. Curr. Biol. 2006, 16:912-919.
7. Chaudhuri A., et al. Interaction of genetic and environmental factors in a Drosophila parkinsonism model. J. Neurosci. 2007, 27:2457-2467.
8. Colas J.F., et al. Maternal and zygotic control of serotonin biosynthesis are both necessary for Drosophila germband extension. Mech. Dev. 1999, 87:67-76.
9. Cummings E.D., et al. High-throughput proteomics processing of proteins in polyacrylamide in a multiwell format. J. Proteome Res. 2007, 6:1603-1608.
10. Descheemaeker M.J., et al. Pervasive developmental disorders in Prader-Willi syndrome: the Leuven experience in 59 subjects and controls. Am. J. Med. Genet. A 2006, 140:1136-1142.
11. Dindot S.V., et al. The Angelman syndrome ubiquitin ligase localizes to the synapse and nucleus, and maternal deficiency results in abnormal dendritic spine morphology. Hum. Mol. Genet. 2008, 17:111-118.
12. Duffy J.B. GAL4 system in Drosophila: a fly geneticist's Swiss army knife. Genesis 2002, 34:1-15.
13. Funderburk C.D., et al. A typical N-terminal extensions confer novel regulatory properties on GTP cyclohydrolase isoforms in Drosophila melanogaster. J. Biol. Chem. 2006, 281:33302-33312.
14. Haas K.F., Broadie K. Roles of ubiquitination at the synapse. Biochim. Biophys. Acta 2008, 1779:495-506.
15. Hettinger J.A., et al. A DRD1 haplotype is associated with risk for autism spectrum disorders in male-only affected sib-pair families. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2008, 147B:628-636.
16. Hicke L. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2001, 2:195-201.
17. Hogart A., et al. The comorbidity of autism with the genomic disorders of chromosome 15q11.2-q13. Neurobiol. Dis. 2010, 38:181-191.
18. Hsouna A., et al. Drosophila dopamine synthesis pathway genes regulate tracheal morphogenesis. Dev. Biol. 2007, 308:30-43.
19. Huibregtse J.M., et al. Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol. Cell. Biol. 1993, 13:4918-4927.
20. Jiang Y., et al. Genetics of Angelman syndrome. Am. J. Hum. Genet. 1999, 65:1-6.
21. Kishino T., et al. UBE3A/E6-AP mutations cause Angelman syndrome. Nat. Genet. 1997, 15:70-73.
22. Kolevzon A., et al. Selective serotonin reuptake inhibitors in autism: a review of efficacy and tolerability. J. Clin. Psychiatry 2006, 67:407-414.
23. Krishnakumar S., et al. Functional interactions between GTP cyclohydrolase I and tyrosine hydroxylase in Drosophila. J. Neurogenet. 2000, 14:1-23.
24. Lalande M., Calciano M.A. Molecular epigenetics of Angelman syndrome. Cell. Mol. Life Sci. 2007, 64:947-960.
25. Liu T., et al. Increased dopamine level enhances male-male courtship in Drosophila. J. Neurosci. 2008, 28:5539-5546.
26. Low D., Chen K.S. Genome-wide gene expression profiling of the Angelman syndrome mice with Ube3a mutation. Eur. J. Hum. Genet. 2010, 18:1228-1235.
27. Mackay W.J., O'Donnell J.M. A genetic analysis of the pteridine biosynthetic enzyme, guanosine triphosphate cyclohydrolase, in Drosophila melanogaster. Genetics 1983, 105:35-53.
28. Mackay W.J., et al. Tissue-specific and complex complementation patterns in the Punch locus of Drosophila melanogaster. Genetics 1985, 111:885-904.
29. Makkonen I., et al. Serotonin and dopamine transporter binding in children with autism determined by SPECT. Dev. Med. Child Neurol. 2008, 50:593-597.
30. McClung C., Hirsh J. The trace amine tyramine is essential for sensitization to cocaine in Drosophila. Curr. Biol. 1999, 9:853-860.
31. McLean J.R., et al. Multiple mRNAs from the Punch locus of Drosophila melanogaster encode isoforms of GTP cyclohydrolase I with distinct N-terminal domains. J. Biol. Chem. 1993, 268:27191-27197.
32. Milani D., et al. Another patient with MECP2 mutation without classic Rett syndrome phenotype. Pediatr. Neurol. 2005, 32:355-357.
33. Mulherkar S.A., Jana N.R. Loss of dopaminergic neurons and resulting behavioural deficits in mouse model of Angelman syndrome. Neurobiol. Dis. 2010, 40:586-592.
34. Nagatsu T., et al. Tyrosine hydroxylase. The initial step in norepinephrine biosynthesis. J. Biol. Chem. 1964, 239:2910-2917.
35. Neckameyer W.S., et al. Biochemical conservation of recombinant Drosophila tyrosine hydroxylase with its mammalian cognates. Biochem. Genet. 2005, 43:425-443.
36. Neckameyer W.S., White K. Drosophila tyrosine hydroxylase is encoded by the pale locus. J. Neurogenet. 1993, 8:189-199.
37. Pelc K., et al. Behavior and neuropsychiatric manifestations in Angelman syndrome. Neuropsychiatr. Dis. Treat. 2008, 4:577-584.
38. Pendleton R.G., et al. Effects of tyrosine hydroxylase mutants on locomotor activity in Drosophila: a study in functional genomics. Behav. Genet. 2002, 32:89-94.
39. Peterson A., Reiter L. Genetic screen for potential protein substrates of the Drosophila E3 ubiquitin ligase gene (dube3a). 47th Annual Drosophila Research Conference, Houston, TX 2006.
40. Ramamoorthy S., Nawaz Z. E6-associated protein (E6-AP) is a dual function coactivator of steroid hormone receptors. Nucl. Recept. Signal. 2008, 6:e006.
41. Reiter L.T., et al. Expression of the Rho-GEF Pbl/ECT2 is regulated by the UBE3A E3 ubiquitin ligase. Hum. Mol. Genet. 2006, 15:2825-2835.
42. Rougeulle C., et al. The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brain. Nat. Genet. 1997, 17:14-15. [letter].
43. Schroer R.J., et al. Autism and maternally derived aberrations of chromosome 15q. Am. J. Med. Genet. 1998, 76:327-336.
44. Takano K., et al. Two percent of patients suspected of having Angelman syndrome have TCF4 mutations. Clin Genet 2010, 78:282-288.
45. Tani Y., et al. Decrease in 6R-5,6,7,8-tetrahydrobiopterin content in cerebrospinal fluid of autistic patients. Neurosci. Lett. 1994, 181:169-172.
46. Thony B., et al. Tetrahydrobiopterin biosynthesis, regeneration and functions. Biochem. J. 2000, 347(Pt 1):1-16.
47. Veltman M.W., et al. Autism spectrum disorders in Prader-Willi and Angelman syndromes: a systematic review. Psychiatr. Genet. 2005, 15:243-254.
48. Watson P., et al. Angelman syndrome phenotype associated with mutations in MECP2, a gene encoding a methyl CpG binding protein. J. Med. Genet. 2001, 38:224-228.
49. Weisberg E.P., O'Donnell J.M. Purification and characterization of GTP cyclohydrolase I from Drosophila melanogaster. J. Biol. Chem. 1986, 261:1453-1458.
50. Wu Y., et al. A Drosophila model for Angelman syndrome. Proc. Natl Acad. Sci. USA 2008, 105:12399-12404.
51. Yashiro K., et al. Ube3a is required for experience-dependent maturation of the neocortex. Nat. Neurosci. 2009, 12:777-783.