Pathway-specific dopaminergic deficits in a mouse model of Angelman syndrome

Journal of Clinical Investigation

Volumn 122, Issue 12, 2012, Pages 4544-4554

  Riday, Thorfinn T ^a,b   Dankoski, Elyse C ^a   Krouse, Michael C ^b   Fish, Eric W ^b   Walsh, Paul L ^c   Han, Ji Eun ^b   Hodge, Clyde W ^a,b   Wightman, R Mark ^a,b,c   Philpot, Benjamin D ^a,b   Malanga, C J ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c University of North Carolina at Chapel Hill   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COCAINE; DOPAMINE; UBIQUITIN PROTEIN LIGASE E3; UBIQUITIN PROTEIN LIGASE E3A; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN DEPTH STIMULATION; CLINICAL FEATURE; CONTROLLED STUDY; CORPUS STRIATUM; CYCLIC POTENTIOMETRY; DISEASE MODEL; DOPAMINE METABOLISM; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DOPAMINERGIC TRANSMISSION; HAPPY PUPPET SYNDROME; LOCOMOTION; MALE; MESOLIMBIC DOPAMINERGIC SYSTEM; MOUSE; NEUROANATOMY; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; REWARD;

ANGELMAN SYNDROME; ANIMALS; BENZAZEPINES; COCAINE; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; DOPAMINERGIC NEURONS; ELECTRIC STIMULATION; FEMALE; INDOLES; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; PIPERIDINES; RACLOPRIDE; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; REWARD; SELF STIMULATION; SUBSTANTIA NIGRA; SYNAPTIC TRANSMISSION; UBIQUITIN-PROTEIN LIGASES; VENTRAL TEGMENTAL AREA;

EID: 84870575446     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI61888     Document Type: Article

References (61)

1. Steffenburg S, Gillberg CL, Steffenburg U, Kyllerman M. Autism in Angelman syndrome: a population- based study. Pediatr Neurol. 1996;14(2):131-136. (Pubitemid 26104417)
2. Peters SU, Beaudet AL, Madduri N, Bacino CA. Autism in Angelman syndrome: implications for autism research. Clin Genet. 2004;66(6):530-536. (Pubitemid 39562016)
3. Williams CA, et al. Angelman syndrome 2005: updated consensus for diagnostic criteria. Am J Med Genet A. 2006;140(5):413-418. (Pubitemid 43376311)
4. Kishino T, Lalande M, Wagstaff J. UBE3A/E6-AP mutations cause Angelman syndrome. Nat Genet. 1997;15(1):70-73. (Pubitemid 27014952)
5. Mabb AM, Judson MC, Zylka MJ, Philpot BD. Angelman syndrome: insights into genomic imprinting and neurodevelopmental phenotypes. Trends Neurosci. 2011;34(6):293-303.
6. Knoll JH, Nicholls RD, Magenis RE, Graham JM Jr, Lalande M, Latt SA. Angelman and Prader-Willi syndromes share a common chromosome 15 deletion but differ in parental origin of the deletion. Am J Med Genet. 1989;32(2):285-290.
7. Williams CA, Zori RT, Stone JW, Gray BA, Cantu ES, Ostrer H. Maternal origin of 15q11-13 deletions in Angelman syndrome suggests a role for genomic imprinting. Am J Med Genet. 1990;35(3):350-353. (Pubitemid 20068464)
8. Rougeulle C, Glatt H, Lalande M. The Angelman syndrome candidate gene, UBE3A/E6-AP, is imprinted in brain. Nat Genet. 1997;17(1):14-15.
9. Vu TH, Hoffman AR. Imprinting of the Angelman syndrome gene, UBE3A, is restricted to brain. Nat Genet. 1997;17(1):12-13.
10. Sutcliffe JS, et al. The E6-AP ubiquitin-protein ligase (UBE3A) gene is localized within a narrowed angelman syndrome critical region. Genome Research. 1997;7(4):368-377. (Pubitemid 27183005)
11. Pelc K, Boyd SG, Cheron G, Dan B. Epilepsy in Angelman syndrome. Seizure. 2008;17(3):211-217. (Pubitemid 351324161)
12. Harbord M. Levodopa responsive Parkinsonism in adults with Angelman Syndrome. J Clin Neurosci. 2001;8(5):421-422. (Pubitemid 32843694)
13. Tan W-H. A Trial of Levodopa in Angelman Syndrome. NIH Web site. http://clinicaltrials.gov/ct2/ show/NCT01281475. Updated March 16, 2012. Accessed October 1, 2012.
14. Mulherkar SA, Jana NR. Loss of dopaminergic neurons and resulting behavioural deficits in mouse model of Angelman syndrome. Neurobiol Dis. 2010; 40(3):586-592.
15. Ferdousy F, et al. Drosophila Ube3a regulates monoamine synthesis by increasing GTP cyclohydrolase I activity via a non-ubiquitin ligase mechanism. Neurobiol Dis. 2011;41(3):669-677.
16. Philpot BD, Thompson CE, Franco L, Williams CA. Angelman syndrome: advancing the research frontier of neurodevelopmental disorders. J Neurodev Disord. 2011;3(1):50-56.
17. Cooper BR, Breese GR. A role for dopamine in the psychopharmacology of electrical self-stimulation. Natl Inst Drug Abuse Res Monogr Ser. 1975;(3):63-70.
18. Wise RA. Brain reward circuitry: insights from unsensed incentives. Neuron. 2002;36(2):229-240. (Pubitemid 35217889)
19. Benuck M, Lajtha A, Reith ME. Pharmacokinetics of systemically administered cocaine and locomotor stimulation in mice. J Pharmacol Exp Ther. 1987; 243(1):144-149. (Pubitemid 17162710)
20. Allensworth M, Saha A, Reiter LT, Heck DH. Normal social seeking behavior, hypoactivity and reduced exploratory range in a mouse model of Angelman syndrome. BMC Genet. 2011;12:7.
21. Wise RA, Rompre PP. Brain dopamine and reward. Annu Rev Psychol. 1989;40:191-225.
22. Walz NC, Baranek GT. Sensory processing patterns in persons with Angelman syndrome. Am J Occup Ther. 2006;60(4):472-479. (Pubitemid 44859806)
23. Chausmer AL, Elmer GI, Rubinstein M, Low MJ, Grandy DK, Katz JL. Cocaine-induced locomotor activity and cocaine discrimination in dopamine D2 receptor mutant mice. Psychopharmacology (Berl). 2002;163(1):54-61. (Pubitemid 34985312)
24. Welter M, Vallone D, Samad TA, Meziane H, Usiello A, Borrelli E. Absence of dopamine D2 receptors unmasks an inhibitory control over the brain circuitries activated by cocaine. Proc Natl Acad Sci U S A. 2007;104(16):6840- 6845. (Pubitemid 47175588)
25. Rouge-Pont F, Usiello A, Benoit-Marand M, Gonon F, Piazza PV, Borrelli E. Changes in extracellular dopamine induced by morphine and cocaine: crucial control by D2 receptors. J Neurosci. 2002; 22(8):3293-3301. (Pubitemid 35379217)
26. Bello EP, et al. Cocaine supersensitivity and enhanced motivation for reward in mice lacking dopamine D2 autoreceptors. Nat Neurosci. 2011; 14(8):1033-1038.
27. Elmer GI, et al. Brain stimulation and morphine reward deficits in dopamine D2 receptor-deficient mice. Psychopharmacology (Berl). 2005;182(1):33-44. (Pubitemid 41400859)
28. Kitada T, et al. Impaired dopamine release and synaptic plasticity in the striatum of PINK1-deficient mice. Proc Natl Acad Sci U S A. 2007;104(27):11441-11446. (Pubitemid 47175159)
29. Lee JY, et al. Human DJ-1 and its homologs are novel glyoxalases. Hum Mol Genet. 2012;21(14):3215-3225.
30. Goldberg MS, et al. Nigrostriatal dopaminergic deficits and hypokinesia caused by inactivation of the familial Parkinsonism-linked gene DJ-1. Neuron. 2005;45(4):489-496. (Pubitemid 40249861)
31. Gispert S, et al. Parkinson phenotype in aged PINK1-deficient mice is accompanied by progressive mitochondrial dysfunction in absence of neurodegeneration. PLoS One. 2009;4(6):e5777.
32. Itier JM, et al. Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum Mol Genet. 2003;12(18):2277-2291.
33. Goldberg MS, et al. Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J Biol Chem. 2003;278(44):43628-43635. (Pubitemid 37345989)
34. Khan NL, et al. Clinical and subclinical dopaminergic dysfunction in PARK6-linked parkinsonism: an 18F-dopa PET study. Ann Neurol. 2002;52(6):849-853. (Pubitemid 35403199)
35. Dekker M, et al. Clinical features and neuroimaging of PARK7-linked parkinsonism. Mov Disord. 2003;18(7):751-757. (Pubitemid 36939969)
36. Scherfler C, et al. Striatal and cortical pre- and postsynaptic dopaminergic dysfunction in sporadic parkin-linked parkinsonism. Brain. 2004; 127(pt 6):1332-1342. (Pubitemid 38745511)
37. Ross CA, Pickart CM. The ubiquitin-proteasome pathway in Parkinson's disease and other neurodegenerative diseases. Trends Cell Biol. 2004; 14(12):703-711. (Pubitemid 39572556)
38. Xiong H, et al. Parkin, PINK1, and DJ-1 form a ubiquitin E3 ligase complex promoting unfolded protein degradation. J Clin Invest. 2009;119(3):650-660.
39. Shimura H, et al. Ubiquitination of a new form of alpha-synuclein by parkin from human brain: implications for Parkinson's disease. Science. 2001; 293(5528):263-269. (Pubitemid 32694735)
40. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, Dawson TM. Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc Natl Acad Sci U S A. 2000; 97(24):13354-13359.
41. Choi P, et al. SEPT5-v2 is a parkin-binding protein. Brain Res Mol Brain Res. 2003;117(2):179-189. (Pubitemid 38366031)
42. Wang HQ, et al. Pael-R transgenic mice crossed with parkin deficient mice displayed progressive and selective catecholaminergic neuronal loss. J Neurochem. 2008;107(1):171-185.
43. Imai Y, Soda M, Inoue H, Hattori N, Mizuno Y, Takahashi R. An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell. 2001; 105(7):891-902. (Pubitemid 32635090)
44. Ko HS, et al. Accumulation of the authentic parkin substrate aminoacyl-tRNA synthetase cofactor, p38/JTV-1, leads to catecholaminergic cell death. J Neurosci. 2005;25(35):7968-7978. (Pubitemid 41254399)
45. Snyder H, Mensah K, Theisler C, Lee J, Matouschek A, Wolozin B. Aggregated and monomeric alpha-synuclein bind to the S6' proteasomal protein and inhibit proteasomal function. J Biol Chem. 2003;278(14):11753-11759. (Pubitemid 36800143)
46. Tanaka Y, et al. Inducible expression of mutant alpha-synuclein decreases proteasome activity and increases sensitivity to mitochondria-dependent apoptosis. Hum Mol Genet. 2001;10(9):919-926. (Pubitemid 32401408)
47. Mulherkar SA, Sharma J, Jana NR. The ubiquitin ligase E6-AP promotes degradation of alpha-synuclein. J Neurochem. 2009;110(6):1955-1964.
48. Nemani VM, et al. Increased expression of alphasynuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron. 2010;65(1):66-79.
49. Maingay M, Romero-Ramos M, Carta M, Kirik D. Ventral tegmental area dopamine neurons are resistant to human mutant alpha-synuclein overexpression. Neurobiol Dis. 2006;23(3):522-532. (Pubitemid 44251282)
50. Shenoy SK, Lefkowitz RJ. Multifaceted roles of beta-arrestins in the regulation of seven-membrane- spanning receptor trafficking and signalling. Biochem J. 2003;375(pt 3):503-515. (Pubitemid 37433499)
51. Hislop JN, von Zastrow M. Role of ubiquitination in endocytic trafficking of G-protein-coupled receptors. Traffic. 2011;12(2):137-148.
52. Khan NL, et al. Parkin disease: a phenotypic study of a large case series. Brain. 2003;126(pt 6):1279-1292. (Pubitemid 36644375)
53. Macdonald PA, Monchi O. Differential effects of dopaminergic therapies on dorsal and ventral striatum in Parkinson's disease: implications for cognitive function. Parkinsons Dis. 2011;2011:572743.
54. Fish EW, Riday TT, McGuigan MM, Faccidomo S, Hodge CW, Malanga CJ. Alcohol, cocaine, and brain stimulation-reward in C57Bl6/J and DBA2/J mice. Alcohol Clin Exp Res. 2010;34(1):81-89.
55. Paxinos G, Franklin KBJ. The Mouse Brain In Stereotaxic Coordinates. 2nd ed. San Diego, California, USA: Academic Press; 2001.
56. West MJ. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci. 1999;22(2):51-61. (Pubitemid 29125550)
57. Gundersen HJ, Jensen EB. The efficiency of systematic sampling in stereology and its prediction. J Microsc. 1987;147(pt 3):229-263.
58. Baquet ZC, Williams D, Brody J, Smeyne RJ. A comparison of model-based (2D) and designbased (3D) stereological methods for estimating cell number in the substantia nigra pars compacta (SNpc) of the C57BL/6J mouse. Neuroscience. 2009; 161(4):1082-1090.
59. Mefford IN. Application of high performance liquid chromatography with electrochemical detection to neurochemical analysis: measurement of catecholamines, serotonin and metabolites in rat brain. J Neurosci Methods. 1981;3(3):207-224. (Pubitemid 11149054)
60. Cahill PS, Walker QD, Finnegan JM, Mickelson GE, Travis ER, Wightman RM. Microelectrodes for the measurement of catecholamines in biological systems. Anal Chem. 1996;68(18):3180-3186.
61. Heien ML, Phillips PE, Stuber GD, Seipel AT, Wightman RM. Overoxidation of carbon-fiber microelectrodes enhances dopamine adsorption and increases sensitivity. Analyst. 2003;128(12):1413-1419. (Pubitemid 38082985)