Aromatic L-Amino Acid Decarboxylase (AADC) Is Crucial for Brain Development and Motor Functions

PLoS ONE

Volumn 8, Issue 8, 2013, Pages

  Shih, De Fen ^a   Hsiao, Chung Der ^b   Min, Ming Yuan ^a   Lai, Wen Sung ^a   Yang, Chianne Wen ^c   Lee, Wang Tso ^a,c   Lee, Shyh Jye ^a  

^a NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^b CHUNG YUAN CHRISTIAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBENZYLHYDRAZINE; AROMATIC LEVO AMINO ACID DECARBOXYLASE; OLIGONUCLEOTIDE;

AADC GENE; AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY HEIGHT; BRAIN CELL; BRAIN DEVELOPMENT; BRAIN SIZE; CELL LOSS; CONTROLLED STUDY; DDC GENE; DIENCEPHALON; DOPAMINERGIC NERVE CELL; DOWN REGULATION; EMBRYO; EPIPHYSIS; EYE MOVEMENT; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE IDENTIFICATION; IN SITU HYBRIDIZATION; LOCUS CERULEUS; MOTOR PERFORMANCE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; RAPHE NUCLEUS; SEIZURE; SEQUENCE HOMOLOGY; SWIMMING; ZEBRA FISH;

AMINO ACID SEQUENCE; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AROMATIC-L-AMINO-ACID DECARBOXYLASES; BRAIN; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; MOLECULAR SEQUENCE DATA; MOTOR ACTIVITY; SEQUENCE HOMOLOGY, AMINO ACID; ZEBRAFISH;

EID: 84881115440     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0071741     Document Type: Article

References (79)

1. Pons R, Ford B, Chiriboga CA, Clayton PT, Hinton V, et al. (2004) Aromatic L-amino acid decarboxylase deficiency: clinical features, treatment, and prognosis. Neurology 62: 1058-1065. doi:10.1212/WNL.62.7.1058. PubMed: 15079002.
2. Swoboda KJ, Hyland K, Goldstein DS, Kuban KC, Arnold LA, et al. (1999) Clinical and therapeutic observations in aromatic L-amino acid decarboxylase deficiency. Neurology 53: 1205-1211. doi:10.1212/WNL.53.6.1205. PubMed: 10522874.
3. Swoboda KJ, Saul JP, McKenna CE, Speller NB, Hyland K, (2003) Aromatic L-amino acid decarboxylase deficiency: overview of clinical features and outcomes. Ann Neurol 54 (Suppl 6):: S49-S55. doi:10.1002/ana.10631. PubMed: 12891654.
4. Brun L, Ngu LH, Keng WT, Ch'ng GS, Choy YS, et al. (2010) Clinical and biochemical features of aromatic L-amino acid decarboxylase deficiency. Neurology 75: 64-71. doi:10.1212/WNL.0b013e3181e620ae. PubMed: 20505134.
5. Manegold C, Hoffmann GF, Degen I, Ikonomidou H, Knust A, et al. (2009) Aromatic L-amino acid decarboxylase deficiency: clinical features, drug therapy and follow-up. J Inherit Metab Dis 32: 371-380. doi:10.1007/s10545-009-1076-1. PubMed: 19172410.
6. Lee HF, Tsai CR, Chi CS, Chang TM, Lee HJ, (2009) Aromatic L-amino acid decarboxylase deficiency in Taiwan. Eur J Paediatr Neurol 13: 135-140. doi:10.1016/j.ejpn.2008.03.008. PubMed: 18567514.
7. Lee WT, Weng WC, Peng SF, Tzen KY, (2009) Neuroimaging findings in children with paediatric neurotransmitter diseases. J Inherit Metab Dis 32: 361-370. doi:10.1007/s10545-009-1106-z. PubMed: 19455403.
8. Hyland K, Clayton PT, (1990) Aromatic amino acid decarboxylase deficiency in twins. J Inherit Metab Dis 13: 301-304. doi:10.1007/BF01799380. PubMed: 1700191.
9. Verbeek MM, Geurtz PB, Willemsen MA, Wevers RA, (2007) Aromatic L-amino acid decarboxylase enzyme activity in deficient patients and heterozygotes. Mol Genet Metab 90: 363-369. doi:10.1016/j.ymgme.2006.12.001. PubMed: 17240182.
10. Ito S, Nakayama T, Ide S, Ito Y, Oguni H, et al. (2008) Aromatic L-amino acid decarboxylase deficiency associated with epilepsy mimicking non-epileptic involuntary movements. Dev Med Child Neurol 50: 876-878. doi:10.1111/j.1469-8749.2008.03094.x. PubMed: 18754761.
11. Crisp KM, Mesce KA, (2004) A cephalic projection neuron involved in locomotion is dye coupled to the dopaminergic neural network in the medicinal leech. J Exp Biol 207: 4535-4542. doi:10.1242/jeb.01315. PubMed: 15579549.
12. Kiehn O, Kjaerulff O, (1996) Spatiotemporal characteristics of 5-HT and dopamine-induced rhythmic hindlimb activity in the in vitro neonatal rat. J Neurophysiol 75: 1472-1482. PubMed: 8727391.
13. Marder E, Eisen JS, (1984) Electrically coupled pacemaker neurons respond differently to same physiological inputs and neurotransmitters. J Neurophysiol 51: 1362-1374. PubMed: 6145758.
14. Schotland J, Shupliakov O, Wikström M, Brodin L, Srinivasan M, et al. (1995) Control of lamprey locomotor neurons by colocalized monoamine transmitters. Nature 374: 266-268. doi:10.1038/374266a0. PubMed: 7885446.
15. Verney C, Lebrand C, Gaspar P, (2002) Changing distribution of monoaminergic markers in the developing human cerebral cortex with special emphasis on the serotonin transporter. Anat Rec 267: 87-93. doi:10.1002/ar.10089. PubMed: 11997877.
16. Gaspar P, Cases O, Maroteaux L, (2003) The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 4: 1002-1012. doi:10.1038/nrn1256. PubMed: 14618156.
17. Neff NH, Hadjiconstantinou M, (1995) Aromatic L-amino acid decarboxylase modulation and Parkinson's disease. Prog Brain Res 106: 91-97. doi:10.1016/S0079-6123(08)61206-6. PubMed: 8584678.
18. King JM, Muthian G, Mackey V, Smith M, Charlton C, (2011) L-Dihydroxyphenylalanine modulates the steady-state expression of mouse striatal tyrosine hydroxylase, aromatic L-amino acid decarboxylase, dopamine and its metabolites in an MPTP mouse model of Parkinson's disease. Life Sci 89: 638-643. doi:10.1016/j.lfs.2011.08.008. PubMed: 21871902.
19. Kitahama K, Ikemoto K, Jouvet A, Araneda S, Nagatsu I, et al. (2009) Aromatic L-amino acid decarboxylase-immunoreactive structures in human midbrain, pons, and medulla. J Chem Neuroanat 38: 130-140. doi:10.1016/j.jchemneu.2009.06.010. PubMed: 19589383.
20. Moreira-Rodrigues M, Sampaio-Maia B, Pestana M, (2009) Renal dopaminergic system activity in rat remnant kidney up to twenty-six weeks after surgery. Life Sci 84: 409-414. doi:10.1016/j.lfs.2008.12.018. PubMed: 19167406.
21. Yang S, Yao B, Zhou Y, Yin H, Zhang MZ, et al. (2012) Intrarenal dopamine modulates progressive angiotensin II-mediated renal injury. Am J Physiol Renal Physiol 302: F742-F749. doi:10.1152/ajprenal.00583.2011. PubMed: 22169008.
22. Blechingberg J, Holm IE, Johansen MG, Børglum AD, Nielsen AL, (2010) Aromatic l-amino acid decarboxylase expression profiling and isoform detection in the developing porcine brain. Brain Res 1308: 1-13. doi:10.1016/j.brainres.2009.10.051. PubMed: 19857468.
23. Eberling JL, Roberts JA, Taylor SE, VanBrocklin HF, O'Neil JP, et al. (2002) No effect of age and estrogen on aromatic L- amino acid decarboxylase activity in rhesus monkey brain. Neurobiol Aging 23: 479-483. doi:10.1016/S0197-4580(01)00323-2. PubMed: 11959410.
24. Waymire JC, Gilmer-Waymire K, (1978) Adrenergic enzymes in cultured mouse neuroblastoma: absence of detectable aromatic-L-amino-acid decarboxylase. J Neurochem 31: 693-698. doi:10.1111/j.1471-4159.1978.tb07842.x. PubMed: 28384.
25. Chatelin S, Wehrlé R, Mercier P, Morello D, Sotelo C, et al. (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 Molecular Brain Res 97: 149-160. doi:10.1016/S0169-328X(01)00318-7. PubMed: 11750071.
26. Takezako T, Noda K, Tsuji E, Koga M, Sasaguri M, et al. (2001) Adenosine activates aromatic L-amino acid decarboxylase activity in the kidney and increases dopamine. J Am Soc Nephrol 12: 29-36. PubMed: 11134247.
27. Costa M, Furness JB, McLean JR, (1976) The presence of aromatic L-amino acid decarboxylase in certain intestinal nerve cells. Histochemistry 48: 129-143. doi:10.1007/BF00494551. PubMed: 955982.
28. Hayashi H, Mizuguchi H, Kagamiyama H, (1993) Rat liver aromatic L-amino acid decarboxylase: spectroscopic and kinetic analysis of the coenzyme and reaction intermediates. Biochemistry 32: 812-818. doi:10.1021/bi00054a011. PubMed: 8422386.
29. Gilbert JA, Frederick LM, Ames MM, (2000) The aromatic-L-amino acid decarboxylase inhibitor carbidopa is selectively cytotoxic to human pulmonary carcinoid and small cell lung carcinoma cells. Clin Cancer Res Off J Am Assoc Cancer Res 6: 4365-4372. PubMed: 11106255.
30. Eberle ED, Eiduson S, (1968) Effect of pyridoxine deficiency on aromatic L-amino acid decarboxylase in the developing rat liver and brain. J Neurochem 15: 1071-1083. doi:10.1111/j.1471-4159.1968.tb06825.x. PubMed: 5711122.
31. DeJesus OT, Flores LG, Roberts AD, Dick DW, Bartlett RM, et al. (2005) Aromatic L-amino acid decarboxylase (AAAD) activity in rhesus macaque striatum after MAO-B inhibition by Ro 16-6491. Synapse 56: 54-56. doi:10.1002/syn.20119. PubMed: 15700282.
32. Eaton MJ, Gudehithlu KP, Quach T, Silvia CP, Hadjiconstantinou M, et al. (1993) Distribution of aromatic L-amino acid decarboxylase mRNA in mouse brain by in situ hybridization histology. J Comp Neurol 337: 640-654. doi:10.1002/cne.903370409. PubMed: 7904615.
33. Cañestro C, Yokoi H, Postlethwait JH, (2007) Evolutionary developmental biology and genomics. Nat Rev Genet 8: 932-942. doi:10.1038/nrg2226. PubMed: 18007650.
34. Whitlock KE, (2004) Development of the nervus terminalis: origin and migration. Microsc Res Tech 65: 2-12. doi:10.1002/jemt.20094. PubMed: 15570589.
35. Rinkwitz S, Mourrain P, Becker TS, (2011) Zebrafish: an integrative system for neurogenomics and neurosciences. Prog Neurobiol 93: 231-243. doi:10.1016/j.pneurobio.2010.11.003. PubMed: 21130139.
36. Barinaga M, (1990) Zebrafish: swimming into the development mainstream. Science 250: 34-35. doi:10.1126/science.2218513. PubMed: 2218513.
37. Müller UK, van Leeuwen JL, (2004) Swimming of larval zebrafish: ontogeny of body waves and implications for locomotory development. J Exp Biol 207: 853-868. doi:10.1242/jeb.00821. PubMed: 14747416.
38. Yamamoto K, Ruuskanen JO, Wullimann MF, Vernier P, (2010) Two tyrosine hydroxylase genes in vertebrates New dopaminergic territories revealed in the zebrafish brain. Mol Cell Neurosci 43: 394-402. doi:10.1016/j.mcn.2010.01.006. PubMed: 20123022.
39. Yamamoto K, Ruuskanen JO, Wullimann MF, Vernier P, (2011) Differential expression of dopaminergic cell markers in the adult zebrafish forebrain. J Comp Neurol 519: 576-598. doi:10.1002/cne.22535. PubMed: 21192085.
40. Schweitzer J, Driever W, (2009) Development of the dopamine systems in zebrafish. Adv Exp Med Biol 651: 1-14. doi:10.1007/978-1-4419-0322-8_1. PubMed: 19731546.
41. Rink E, Wullimann MF, (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889: 316-330. doi:10.1016/S0006-8993(00)03174-7. PubMed: 11166725.
42. Schweitzer J, Lohr H, Filippi A, Driever W, (2012) Dopaminergic and noradrenergic circuit development in zebrafish. Dev Neurobiol 72: 256-268. doi:10.1002/dneu.20911. PubMed: 21567980.
43. Lin YL, Gao J, (2010) Internal proton transfer in the external pyridoxal 5'-phosphate Schiff base in dopa decarboxylase. Biochemistry 49: 84-94. doi:10.1021/bi901790e. PubMed: 19938875.
44. Miñano FJ, McMillen BA, Myers RD, (1990) Central action of an inhibitor of brain dopa-decarboxylase, NSD-1015, on cyanamide-induced alcohol drinking in rats. Pharmacol Biochem Behav 35: 465-468. doi:10.1016/0091-3057(90)90186-L. PubMed: 2320657.
45. Hosseini-Sharifabad M, Nyengaard JR, (2007) Design-based estimation of neuronal number and individual neuronal volume in the rat hippocampus. J Neurosci Methods 162: 206-214. doi:10.1016/j.jneumeth.2007.01.009. PubMed: 17368561.
46. Chen Q, Huang NN, Huang JT, Chen S, Fan J, et al. (2009) Sodium benzoate exposure downregulates the expression of tyrosine hydroxylase and dopamine transporter in dopaminergic neurons in developing zebrafish. Birth Defects Res B Dev Reprod Toxicol 86: 85-91. doi:10.1002/bdrb.20187. PubMed: 19294673.
47. McLean DL, Fetcho JR, (2004) Relationship of tyrosine hydroxylase and serotonin immunoreactivity to sensorimotor circuitry in larval zebrafish. J Comp Neurol 480: 57-71. doi:10.1002/cne.20281. PubMed: 15514919.
48. Korenke GC, Christen HJ, Hyland K, Hunneman DH, Hanefeld F, (1997) Aromatic L-amino acid decarboxylase deficiency: an extrapyramidal movement disorder with oculogyric crises. Eur J Paediatr Neurol 1: 67-71. doi:10.1016/S1090-3798(97)80065-7. PubMed: 10728198.
49. Yang S, Lee YJ, Kim JM, Park S, Peris J, et al. (2006) A murine model for human sepiapterin-reductase deficiency. Am J Hum Genet 78: 575-587. doi:10.1086/501372. PubMed: 16532389.
50. Alenina N, Kikic D, Todiras M, Mosienko V, Qadri F, et al. (2009) Growth retardation and altered autonomic control in mice lacking brain serotonin. Proc Natl Acad Sci U S A 106: 10332-10337. doi:10.1073/pnas.0810793106. PubMed: 19520831.
51. Sumi-Ichinose C, Urano F, Shimomura A, Sato T, Ikemoto K, et al. (2005) Genetically rescued tetrahydrobiopterin-depleted mice survive with hyperphenylalaninemia and region-specific monoaminergic abnormalities. J Neurochem 95: 703-714. doi:10.1111/j.1471-4159.2005.03402.x. PubMed: 16135092.
52. Kwak SS, Suk J, Choi JH, Yang S, Kim JW, et al. (2011) Autophagy induction by tetrahydrobiopterin deficiency. Autophagy 7: 1323-1334. doi:10.4161/auto.7.11.16627. PubMed: 21795851.
53. Airhart MJ, Lee DH, Wilson TD, Miller BE, Miller MN, et al. (2012) Adverse effects of serotonin depletion in developing zebrafish. Neurotoxicol Teratol 34: 152-160. doi:10.1016/j.ntt.2011.08.008. PubMed: 21893190.
54. Flinn L, Mortiboys H, Volkmann K, Köster RW, Ingham PW, et al. (2009) Complex I deficiency and dopaminergic neuronal cell loss in parkin-deficient zebrafish (Danio rerio). Brain J Neurol 132: 1613-1623. doi:10.1093/brain/awp108. PubMed: 19439422.
55. Russek-Blum N, Gutnick A, Nabel-Rosen H, Blechman J, Staudt N, et al. (2008) Dopaminergic neuronal cluster size is determined during early forebrain patterning. Development 135: 3401-3413. doi:10.1242/dev.024232. PubMed: 18799544.
56. Crandall JE, McCarthy DM, Araki KY, Sims JR, Ren JQ, et al. (2007) Dopamine receptor activation modulates GABA neuron migration from the basal forebrain to the cerebral cortex. J Neurosci Off J Soc Neurosci 27: 3813-3822. doi:10.1523/JNEUROSCI.5124-06.2007. PubMed: 17409246.
57. Araki KY, Sims JR, Bhide PG, (2007) Dopamine receptor mRNA and protein expression in the mouse corpus striatum and cerebral cortex during pre- and postnatal development. Brain Res 1156: 31-45. doi:10.1016/j.brainres.2007.04.043. PubMed: 17509542.
58. Previc FH, (1999) Dopamine and the origins of human intelligence. Brain Cogn 41: 299-350. doi:10.1006/brcg.1999.1129. PubMed: 10585240.
59. Swanson JM, Kinsbourne M, Nigg J, Lanphear B, Stefanatos GA, et al. (2007) Etiologic subtypes of attention-deficit/hyperactivity disorder: brain imaging, molecular genetic and environmental factors and the dopamine hypothesis. Neuropsychol Rev 17: 39-59. doi:10.1007/s11065-007-9019-9. PubMed: 17318414.
60. Ide S, Sasaki M, Kato M, Shiihara T, Kinoshita S, et al. (2010) Abnormal glucose metabolism in aromatic L-amino acid decarboxylase deficiency. Brain Dev 32: 506-510. doi:10.1016/j.braindev.2009.05.004. PubMed: 19520530.
61. Betten A, Dahlgren C, Hermodsson S, Hellstrand K, (2001) Serotonin protects NK cells against oxidatively induced functional inhibition and apoptosis. J Leukoc Biol 70: 65-72. PubMed: 11435487.
62. Zhang M, Lee HJ, Park KH, Park HJ, Choi HS, et al. (2012) Modulatory effects of sesamin on dopamine biosynthesis and L-DOPA-induced cytotoxicity in PC12 cells. Neuropharmacology 62: 2219-2226. doi:10.1016/j.neuropharm.2012.01.012. PubMed: 22293035.
63. Saint-Amant L, Drapeau P, (1998) Time course of the development of motor behaviors in the zebrafish embryo. J Neurobiol 37: 622-632. doi:10.1002/(SICI)1097-4695(199812)37:4. PubMed: 9858263.
64. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid JR, et al. (2002) Development of the locomotor network in zebrafish. Prog Neurobiol 68: 85-111. doi:10.1016/S0301-0082(02)00075-8. PubMed: 12450489.
65. Brustein E, Saint-Amant L, Buss RR, Chong M, McDearmid JR, et al. (2003) Steps during the development of the zebrafish locomotor network. J Physiol Paris 97: 77-86. doi:10.1016/j.jphysparis.2003.10.009. PubMed: 14706693.
66. Buss RR, Drapeau P, (2001) Synaptic drive to motoneurons during fictive swimming in the developing zebrafish. J Neurophysiol 86: 197-210. PubMed: 11431502.
67. Thirumalai V, Cline HT, (2008) Endogenous dopamine suppresses initiation of swimming in prefeeding zebrafish larvae. J Neurophysiol 100: 1635-1648. doi:10.1152/jn.90568.2008. PubMed: 18562547.
68. Xi Y, Ryan J, Noble S, Yu M, Yilbas AE, et al. (2010) Impaired dopaminergic neuron development and locomotor function in zebrafish with loss of pink1 function. Eur J Neurosci 31: 623-633. doi:10.1111/j.1460-9568.2010.07091.x. PubMed: 20141529.
69. Brustein E, Chong M, Holmqvist B, Drapeau P, (2003) Serotonin patterns locomotor network activity in the developing zebrafish by modulating quiescent periods. J Neurobiol 57: 303-322. doi:10.1002/neu.10292. PubMed: 14608665.
70. Brustein E, Drapeau P, (2005) Serotoninergic modulation of chloride homeostasis during maturation of the locomotor network in zebrafish. J Neurosci Off J Soc Neurosci 25: 10607-10616. doi:10.1523/JNEUROSCI.2017-05.2005. PubMed: 16291933.
71. Missale C, Nash SR, Robinson SW, Jaber M, Caron MG, (1998) Dopamine receptors: from structure to function. Physiol Rev 78: 189-225. PubMed: 9457173.
72. Boehmler W, Carr T, Thisse C, Thisse B, Canfield VA, et al. (2007) D4 Dopamine receptor genes of zebrafish and effects of the antipsychotic clozapine on larval swimming behaviour. Genes Brain Behav 6: 155-166. doi:10.1111/j.1601-183X.2006.00243.x. PubMed: 16764679.
73. Boehmler W, Obrecht-Pflumio S, Canfield V, Thisse C, Thisse B, et al. (2004) Evolution and expression of D2 and D3 dopamine receptor genes in zebrafish. Dev Dynam Off Publ American Association Of Anatomists 230: 481-493. doi:10.1002/dvdy.20075. PubMed: 15188433.
74. Bundschuh ST, Zhu P, Schärer YP, Friedrich RW, (2012) Dopaminergic modulation of mitral cells and odor responses in the zebrafish olfactory bulb. J Neurosci Off J Soc Neurosci 32: 6830-6840. doi:10.1523/JNEUROSCI.6026-11.2012. PubMed: 22593052.
75. Easter SS Jr., Nicola GN, (1996) The development of vision in the zebrafish (Danio rerio). Dev Biol 180: 646-663. doi:10.1006/dbio.1996.0335. PubMed: 8954734.
76. Easter SS Jr., Nicola GN, (1997) The development of eye movements in the zebrafish (Danio rerio). Dev Psychobiol 31: 267-276. doi:10.1002/(SICI)1098-2302(199712)31:4. PubMed: 9413674.
77. Whitlock KE, Westerfield M, (2000) The olfactory placodes of the zebrafish form by convergence of cellular fields at the edge of the neural plate. Development 127: 3645-3653. PubMed: 10934010.
78. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF, (1995) Stages of embryonic development of the zebrafish. Dev Dynam Off Publ American Association Of Anatomists 203: 253-310. doi:10.1002/aja.1002030302.
79. Thisse C, Thisse B, (2008) High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat Protoc 3: 59-69. doi:10.1038/nnano.2008.25. PubMed: 18193022.