The cholinergic gene locus in amphioxus: Molecular characterization and developmental expression patterns

Developmental Dynamics

Volumn 237, Issue 5, 2008, Pages 1399-1411

  Candiani, Simona ^a   Lacalli, Thurston C ^b   Parodi, Manuela ^a   Oliveri, Diana ^a   Pestarino, Mario ^a  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Amphioxus; ChAT; Cholinergic gene locus; Cholinergic motoneurons and interneurons; Development; Evolution; ISH; VAChT

Indexed keywords

CHOLINE ACETYLTRANSFERASE; MESSENGER RNA; VESICULAR ACETYLCHOLINE TRANSPORTER;

5' UNTRANSLATED REGION; ARTICLE; CELL DIFFERENTIATION; GENE EXPRESSION; GENE LOCUS; IN SITU HYBRIDIZATION; INTERNEURON; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOTONEURON; NERVE CORD; NEUROECTODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA SPLICING; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; CHOLINE O-ACETYLTRANSFERASE; CHORDATA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; IN SITU HYBRIDIZATION; MOLECULAR SEQUENCE DATA; NEURONS; PHYLOGENY; SEQUENCE ALIGNMENT; VESICULAR ACETYLCHOLINE TRANSPORT PROTEINS;

BRANCHIOSTOMA LANCEOLATUM; MAMMALIA;

EID: 43449095721     PISSN: 10588388     EISSN: 10970177     Source Type: Journal    
DOI: 10.1002/dvdy.21541     Document Type: Article

References (43)

1. Alfonso A, Grundahl K, Duerr JS, Han HP, Rand JB. 1993. The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 261:617-619.
2. Alfonso A, Grundahl K, McManus JR, Asbury JM, Rand JB. 1994. Alternative splicing leads to two cholinergic proteins in Caenorhabditis elegans. J Mol Biol 241:627-630.
3. Bardet PL, Schubert M, Horard B, Holland LZ, Laudet V, Holland ND, Vanacker JM. 2005. Expression of estrogen-receptor related receptors in amphioxus and zebrafish: implications for the evolution of posterior brain segmentation at the invertebrate-to-vertebrate transition. Evol Dev 7:223-233.
4. Berrard S, Brice A, Lottspeich F, Braun A, Barde YA, Mallet J. 1987. cDNA cloning and complete sequence of porcine choline acetyltransferase: in vitro translation of the corresponding RNA yields an active protein. Proc Natl Acad Sci U S A 84:9280-9284.
5. Berrard S, Varoqui H, Cervini R, Israël M, Mallet J, Diebler MF. 1995. Coregulation of two embedded gene products, choline acetyltransferase and the vesicular acetylcholine transporter. J Neurochem 65:939-942.
6. Berse B, Blusztajn JK. 1997. Modulation of cholinergic locus expression by glucocorticoids and retinoic acid is cell-type specific. FEBS Lett 410:175-179.
7. Castro LFC, Rasmussen SLK, Holland PWH, Holland ND, Holland LZ. 2006. A Gbx homeobox gene in amphioxus: insights into ancestry of the ANTP class and evolution of the midbrain/hindbrain boundary. Dev Biol 295:40-51.
8. Cervini R, Houhou L, Pradat PF, Bejanin S, Mallet J, Berrard S. 1995. Specific vesicular acetylcholine transporter promoters lie within the first intron of the rat choline acetyltransferase gene. J Biol Chem 270:24654-24657.
9. Delsuc F, Brinkmann H, Chourrout D, Philippe H. 2006. Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439:965-968.
10. Denes AS, Jekely G, Steinmetz PR, Raible F, Snyman H, Prud'homme B, Ferrier DE, Balavoine G, Arendt D. 2007. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 129:277-288.
11. Duerr JS, Han HP, Fields SD, Rand JB. 2008. Identification of major classes of cholinergic neurons in the nematode Caenorhabditis elegans. J Comp Neurol 506:398-408.
12. Eiden LE. 1998. The cholinergic gene locus. J Neurochem 70:2227-2240.
13. Flood PR. 1974. Histochemistry of Cholinesterase in amphioxus (Branchiostoma lanceolatum, Pallas). J Comp Neurol 157:407-437.
14. Gilland E, Baker R. 1993. Conservation of neuroepithelial and mesodermal segments in the embryonic head. Acta Anat 148:110-123.
15. Holland LZ, Holland ND. 1999. Chordate origins of the vertebrate central nervous system. Curr Opin Neurobiol 9:596-602.
16. Holland ND, Holland LZ. 2006. Stage- and tissue-specific patterns of cell division in embryonic and larval tissues of amphioxus during normal development. Evol Dev 8:142-149.
17. Holland LZ, Holland PWH, Holland ND. 1996. Revealing homologies between body parts of distantly related animals by in situ hybridization to developmental genes: amphioxus versus vertebrates. In: Ferraris JD, Palumbi SR, editors. Molecular zoology: advances, strategies, and protocols. New York: Wiley-Liss. p 267-282.
18. Jackman WR, Kimmel CB. 2002. Coincident iterated gene expression in the amphioxus neural tube. Evol Dev 4:366-374.
19. Jackman WR, Langeland JA, Kimmel CB. 2000. islet reveals segmentation in the Amphioxus hindbrain homolog. Dev Biol 220:16-26.
20. Kengaku M, Misawa H, Deguchi T. 1993. Multiple mRNA species of choline acetyltransferase from rat spinal cord. Brain Res Mol Brain Res 18:71-76.
21. Kim MH, Lu M, Lim EJ, Chai YG, Hersh LB. 1999. Mutational analysis of aspartate residues in the transmembrane regions and cytoplasmic loops of rat vesicular acetylcholine transporter. J Biol Chem 274:673-680.
22. Kitamoto T, Wang W, Salvaterra PM. 1998. Structure and organization of the Drosophila cholinergic locus. J Biol Chem 273:2706-2713.
23. Kumar S, Tamura K, Nei M. 2004. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150-163.
24. Lacalli TC. 2002. The dorsal compartment locomotory control system in amphioxus larvae. J Morphol 252:227-237.
25. Lacalli TC. 2003. Ventral neurons in the anterior nerve cord of amphioxus larvae II. Further data on the pacemaker circuit. J Morphol 257:212-218.
26. Lacalli TC. 2008. Basic features of the ancestral chordate brain: a protochodate perspective. Brain Res Bull 75:319-323.
27. Lacalli TC, Kelly SJ. 1999. Somatic motoneurons in the anterior nerve cord of Amphioxus larvae: cell types, cell position and innervation patterns. Acta Zool 80:113-124.
28. Lacalli TC, Kelly SJ. 2003. Ventral neurons in the anterior nerve cord of amphioxus larvae. I. An inventory of cell types and synaptic patterns. J Morphol 257:190-211.
29. Levey AI, Wainer BH, Mufson EJ, Mesulam MM. 1983. Co-localization of acetylcholinesterase and choline acetyltransferase in the rat cerebrum. Neuroscience 9:9-22.
30. Mazet F, Shimeld SM. 2002. The evolution of chordate neural segmentation. Dev Biol 251:258-270.
31. Misawa H, Ishii K, Deguchi T. 1992. Gene expression of mouse choline acetyltransferase. Alternative splicing and identification of a highly active promoter region. J Biol Chem 267:20392-20399.
32. Misawa H, Takahashi R, Deguchi T. 1995. Coordinate expression of vesicular acetylcholine transporter and choline acetyltransferase in sympathetic superior cervical neurones. Neuroreport 6:965-968.
33. Oda Y. 1999. Choline acetyltransferase: the structure, distribution and pathologic changes in the central nervous system. Pathol Int 49:921-937.
34. Saitou N, Nei M. 1987. The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406-425.
35. Schutz B, Weihe E, Eiden LE. 2001. Independent patterns of transcription for the products of the rat cholinergic gene locus. Neuroscience 104:633-642.
36. Søviknes AM, Chourrout D, Glover JC. 2007. Development of the caudal nerve cord, motoneurons, and muscle innervation in the appendicularian urochordate Oikopleura dioica. J Comp Neurol 503:224-243.
37. Takamura K, Egawa T, Ohnishi S, Okada T, Fukuoka T. 2002. Developmental expression of ascidian neurotransmitter synthesis genes. I. Choline acetyltransferase and acetylcholine transporter genes. Dev Genes Evol 212:50-53.
38. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673-4680.
39. Wada H, Saiga H, Satoh N, Holland PWH. 1998. Tripartite organisation of the ancestral chordate brain and the antiquity of placodes: insights from ascidian Pax-2/5/8/, Hox and Otx genes. Development 125:1113-1122.
40. Wicht H, Lacalli TC. 2005. The nervous system of amphioxus: structure, development, and evolutionary significance. Can J Zool 83:122-150.
41. Woolf NJ. 1991. Cholinergic systems in mammalian brain and spinal cord. Prog Neurobiol 37:475-524.
42. Wu D, Hersh LB. 1994. Choline acetyltransferase: celebrating its fiftieth year. J Neurochem 62:1653-1663.
43. Yoshida R, Sakurai D, Horie T, Kawakami I, Tsuda M, Kusakabe T. 2004. Identification of neuron-specific promoters in Ciona intestinalis. Genesis 39:130-140.