Embryonic development in the primitive bilaterian Neochildia fusca: Normal morphogenesis and isolation of POU genes Brn-1 and Brn-3

Development Genes and Evolution

Volumn 212, Issue 2, 2002, Pages 55-69

  Ramachandra, Nallur B ^a   Gates, Ruth D ^a   Ladurner, Peter ^b   Jacobs, David K ^a   Hartenstein, Volker ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Acoel; Development; Neochildia; Nervous system; POU gene

Indexed keywords

PROTEIN BRN 1; PROTEIN BRN 2; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

BRAIN DEVELOPMENT; BRAIN NERVE CELL; CAENORHABDITIS ELEGANS; CELL DIVISION; CELL FATE; CELL SHAPE; CILIATED EPITHELIUM; CONTROLLED STUDY; CYTOARCHITECTURE; DROSOPHILA; EMBRYO DEVELOPMENT; ENDODERM; GENE EXPRESSION; GENE FUNCTION; GENE ISOLATION; GENE SEQUENCE; GENETIC CONSERVATION; MESODERM; MORPHOGENESIS; MUSCLE CELL; MYOBLAST; NEOCHILDIA FUSCA; NEUROPIL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLATYHELMINTH; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; REVIEW; SEQUENCE HOMOLOGY; STEM CELL; TAXON;

AMINO ACID SEQUENCE; ANIMALS; DNA-BINDING PROTEINS; HELMINTH PROTEINS; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEUROPEPTIDES; PLATYHELMINTHS; POU DOMAIN FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION FACTOR BRN-3; TRANSCRIPTION FACTORS;

ACOELA; BILATERIA; CAENORHABDITIS; CAENORHABDITIS ELEGANS; INVERTEBRATA; METAZOA; NEMATODA; NEOCHILDIA; NEOCHILDIA FUSCA; PLATYHELMINTHES; VERTEBRATA;

EID: 0036935183     PISSN: 0949944X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00427-001-0207-y     Document Type: Review

References (67)

1. Adoutte A, Balavoine G, Lartillot N, de Rosa R (1999) Animal evolution: the end of the intermediate taxa? Trends Genet 15:104-108
2. Agata K, Soejima Y, Kato K, Kobayashi C, Umesono Y, Watanabe K (1998) Structure of the planarian central nervous system (CNS) revealed by neuronal cell markers. Zool Sci 15:433-440
3. Alvarez-Bolado G, Rosenfeld MG, Swanson LW (1995) Model of forebrain regionalization based on spatiotemporal patterns of POU-III homeobox gene expression, birthdates, and morphological features. J Comp Neurol 355:237-295
4. Anderson MG, Perkins GL, Chittick P, Shrigley RJ, Johnson WA (1995) drifter, a Drosophila POU-domain transcription factor, is required for correct differentiation and migration of tracheal cells and midline glia. Genes Dev 9:123-137
5. Artinger KB, Fedtsova N, Rhee JM, Bronner-Fraser M, Turner E (1998) Placodal origin of Brn-3-expressing cranial sensory neurons. J Neurobiol 36:572-585
6. Ashburner M (1989) Drosophila. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 214-217
7. Ax P (1963) Relationships and phylogeny of the turbellaria. In: Dougherty EC (ed) The lower Metazoa. University of California Press, Berkeley, pp 191-224
8. Ax P (1996) Multicellular animals, vol I. Fischer, Stuttgart
9. Baguna J (1981) Planarian neoblasts. Nature 290:14-15
10. Bedini F, Lanfranchi A (1991) The central and peripheral nervous system of Acoela (Plathelminthes). An electron microscopic study. Acta Zool (Stockh) 72:101-106
11. Berney C, Pawlowski J, Zaninetti L (2000) Elongation factor 1-alpha sequences do not support an early divergence of the Acoela. Mol Biol Evol 17:1032-1039
12. Billin AN, Poole SJ (1995) Expression domains of the Cf1a POU domain protein during Drosophila development. Roux's Arch Dev Biol 204:502-508
13. Boyer BC, Henry JJ, Martindale MQ (1998) The cell lineage of a polyclad turbellarian embryo reveals close similarity to coelomate spiralians. Dev Biol 204:111-123
14. Bresslau E (1909) Die Entwicklung der Acoelen. Verh Dtsch Zool Ges 48:414-324
15. Certel SJ, Clyne PJ, Carlson JR, Johnson WA (2000) Regulation of central neuron synaptic targeting by the Drosophila POU protein, Acj6. Development. 127:2395-2405
16. Chavez M, Landry C, Loret S, Muller M, Figueroa J, Peers B, Rentier-Delrue F, Rousseau GG, Krauskopf M, Martial JA (1999) APH-1, a POU homeobox gene expressed in the salt gland of the crustacean Artemia franciscana. Mech Dev 87:207-312
17. Clark CG (1992) In: Lee JJ, Soldo A (eds) Protocols in protozoology. Allen Press, Lawrence, Kan. pp D3.1-D3.2
18. DeCelis JF, Llimargas M, Casanova J (1995) Ventral veinless, the gene encoding the Cf1a transcription factor, links positional information and cell differentiation during embryonic and imaginal development in Drosophila melanogaster. Development 121:3405-3416
19. Ehlers U (1985) Das phylogenetische System der Plathelminthes. Fischer, Stuttgart
20. Finney M, Ruvkin G (1990) The unc-86 gene product couples cell lineage and cell identity in Caenorhabditis elegans. Cell 63:895-906
21. Gan L, Xiang M, Zhou L, Wagner DS, Klein WH, Nathans J (1996) POU domain factor Brn-3b is required for the development of a large set of retinal ganglion cells. Proc Natl Acad Sci USA 93:3920-3925
22. Gan L, Wang SW, Huang Z, Klein WH (1999) POU domain factor Brn-3b is essential for retinal ganglion cell differentiation and survival but not for initial cell fate specification. Dev Biol 210:469-480
23. Giribet G, Distel DL, Polz M, Sterrer W, Wheeler WC (2000) Triploblastic relationships with emphasis on the acoelomates and the position of Gnathostomulida, Cycliophora, Plathelminthes, and Chaetognatha: a combined approach of 18S rDNA sequences and morphology. Syst Biol 49:539-562
24. Gschwentner R, Ladurner P, Nimeth K, Rieger R (2001) Stem cells in a basal bilaterian: S-phase and mitotic cells in Convolutriloba longifissura (Acoela, Platyhelminthes). Cell Tissue Res 304:401-408
25. Hadzi J (1963) The evolution of the Metazoa. Macmillan, New York
26. Hanson ED (1977) The origin and early evolution of animals. Wesleyan University Press, Middletown, Conn.
27. Hartenstein V, Ehlers U (2000) The embryonic development of the rhabdocoel flatworm Mesostoma lingua. Dev Genes Evol 210:399-415
28. Hartenstein V, Reh T (in press) Homologies between vertebrate and invertebrate eyes. In: Moses K (ed) Drosophila eye development. Springer, Berlin Heidelberg New York
29. Hauptmann G, Gerster T (2000) Combinatorial expression of Zebrafish Brn-1- and Brn-2-related POU genes in the embryonic brain, pronephric primordium, and pharyngeal arches. Dev Dyn 218:345-358
30. He X, Treacy MN, Simmons DM, Ingraham HA, Swanson LW, Rosenfeld MG (1989) Expression of a large family of POU-domain regulatory genes in mammalian brain development. Nature 340:35-41
31. Hendzel MJ, Wei Y, Mancini MA, VanHooser A, Ranalli T, Brinkley BR, Bazett-Jones DP, Allis CD (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:348-360
32. Henry JQ, Martindale MQ, Boyer BC (2000) The unique developmental program of the acoel flatworm, Neochildia fusca. Dev Biol 220:285-295
33. Herr W, Sturm RA, Clerc RG, Corcoran LM, Baltimore D, Sharp PA, Ingraham HA, Rosenfeld MG, Finney M (1988) The POU domain, a large conserved region in the mammalian Pit-1 Oct-1 Oct-2 and Caenorhabditis elegans unc-86 gene products. Genes Dev 12A:1513-1516
34. Hyman LH (1940) The invertebrates: the Protozoa through Ctenophora. McGraw Hill, New York
35. Hyman LH (1951) The invertebrates: Platyhelminthes and Rhynchocoela. McGraw Hill, New York
36. Jacobs DK, Lee SE, Dawson MN, Staton JL, Raskoff KA (1998) The history of development through the evolution of molecules: gene trees, hearts, eyes, and dorsoventral inversion. In: DeSalle R, Schierwater B (eds) Molecular approaches to ecology and evolution. Birkhauser, Basel, pp 323-357
37. Johnson WA, Hirsh J (1990) Binding of a Drosophila POU-domain protein to a sequence element regulating gene expression in specific dopaminergic neurons. Nature 343:467-470
38. Josephson R, Muller T, Pickel J, Okabe S, Reynolds K, Turner PA, Zimmer A, McKay RD (1998) POU transcription factors control expression of CNS stem cell-specific genes. Development 125:3087-3100
39. Kotikova EA (1986) Comparative characterization of the nervous system of the Turbellaria. Hydrobiologia 132:89-92
40. Ladurner P, Rieger R, Baguna J (2000) Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine platyhelminth Macrostomum sp.: a bromodeoxyuridine analysis. Dev Biol 226:231-224
41. Latchman DS (1999) POU family transcription factors in the nervous system. J Cell Physiol 179:126-133
42. Littlewood DTJ, Rohde K, Clough KA (1999) The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biol J Linn Soc 66:75-114
43. Littlewood DTJ, Olson PD, Telford MJ, Herniou EA, Riutort M (2001) Elongation factor 1-alpha sequences alone do not assist in resolving the position of the Acoela within the Metazoa. Mol Biol Evol 18:437-442
44. Munoz-Marmol AM, Casali A, Miralles A, Bueno D, Bayascas JR, Romero R, Salo E (1998) Characterization of platyhelminth POU domain genes: ubiquitous and specific anterior nerve cell expression of different epitopes of GtPOU-1. Mech Dev 76:127-140
45. Newmark PA, Sanchez-Alvarado A (2000) Bromodeoxyuridine specifically labels the regenerative stem cells of planarians. Dev Biol 220:142-153
46. Raikova OI, Reuter M, Jondelius U, Gustafsson MKS (2000) The brain of the Nemertodermatida (Platyhelminthes) as revealed by anti-5HT and anti-FMRFamide immunostainings. Tissue Cell 32:358-365
47. Remane A (1963) The enterocoelic origin of the coelom. In: Dougherty EC (ed)The lower Metazoa. University of California Press, Berkeley
48. Reuter M, Gustafsson MKS (1995) The flatworm nervous system: pattern and phylogeny. In: Breidbach O, Kutsch W (eds) The nervous system of invertebrates. Birkhäuser, Basel
49. Reuter M, Raikova OI, Gustafsson MKS (1998) An endocrine brain? The pattern of FMRF-amide immunoreactivity in Acoela (Plathelminthes). Tissue Cell 30:57-63
50. Rieger R (1985) The phylogenetic status of the acoelomate organization within the bilateria. In: Morris SC, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. (The Systematics Association special vol 28) Clarendon Press, Oxford, pp 101-122
51. Ruiz-Trillo I, Riutort M, Littlewood DTJ, Herniou EA, Baguna J (1999) Acoel flatworms: earliest extant bilaterian metazoans, not members of Platyhelminthes. Science 283:1919-1923
52. Ryan AK, Rosenfeld MG (1997) POU domain family values: flexibility, partnerships, and developmental codes. Genes Dev 11:1207-1225
53. Salvini-Plawen L von (1978) On the origin and evolution of the lower Metazoa. Z Zool Syst Evol Forsch 16:40-88
54. Schubert M, Holland LZ, Holland ND, Jacobs DK (2000) A phylogenetic tree of the Wnt genes based on all available full-length sequences, including five from the cephalochordate Amphioxus. Mol Biol Evol 17:1896-1903
55. Smith JPS, Tyler S (1985) The acoel turbellarians: kingpins of metazoan evolution or a specialized offshoot? In: Morris SC, George JD, Gibson R, Platt HM (eds) The origins and relationships of lower invertebrates. (The Systematics Association special vol 28) Clarendon Press, Oxford, pp 123-145
56. Tautz D, Pfeifle C (1989) A non-radioactive in situ hybridization method for the localization of specific RNA in Drosophila embryos reveals translational control of the segmentation gene hunchback. Chromosoma 98:81-85
57. Theil T, Zechner U, Klett C, Adolph S, Möröy T (1994) Chromosomal localization and sequences of the murine Brn-3 family of developmental control genes. Cytogenet Cell Genet 66:267-271
58. Vahava O, Morell R, Lynch ED, Weiss S, Kagan ME, Ahituv N, Morrow JE, Lee MK, Skvorak AB, Morton CC, Blumenfeld A, Frydman M, Friedman TB, King MC, Avraham KB (1998) Mutation in transcription factor POU4F3 associated with inherited progressive hearing loss in humans. Science 279:1950-1954
59. Wegner M, Drolet DW, Rosenfeld MG (1993) POU-domain proteins: structure and function of developmental regulators. Curr Opin Cell Biol 5:488-498
60. Xiang M, Gan L, Zhou L, Klein WH, Nathans J (1996) Targeted deletion of the mouse POU domain gene Brn-3a causes selective loss of neurons in the brainstem and trigeminal ganglion, uncoordinated limb movement, and impaired suckling. Proc Natl Acad Sci USA 93:1950-1955
61. Xiang M, Gan L, Li D, Chen ZY, Zhou L, O'Malley BW Jr, Klein W, Nathans J (1997a) Essential role of POU-domain factor Brn-3c in auditory and vestibular hair cell development. Proc Natl Acad Sci USA 94:9445-9450
62. Xiang M, Gan L, Li D, Zhou L, Chen ZY, Wagner D, O'Malley BW Jr, Klein W, Nathans J (1997b) Role of the Brn-3 family of POU-domain genes in the development of the auditory/vestibular, somatosensory, and visual systems. Cold Spring Harb Symp 62:325-336
63. Yeo SL, Lloyd A, Kozak K, Dinh A, Dick T, Yang X, Sakonju S, Chia W (1995) On the functional overlap between two Drosophila POU homeo domain genes and the cell fate specification of a CNS neural precursor. Genes Dev 9:1223-1236
64. Younossi-Hartenstein A, Hartenstein V (2000a) Comparative approach to developmental analysis: the case of the dalyellid flatworm, Gieysztoria superba. Int J Dev Biol 44:499-506
65. Younossi-Hartenstein A, Hartenstein V (2000b) The embryonic development of the polyclad flatworm Imgogine mcgrathi. Dev Genes Evol 210:383-398
66. Younossi-Hartenstein A, Ehlers U, Hartenstein V (2000) Embryonic development of the nervous system of the rhabdocoel flatworm Mesostoma lingua (Abildgaard, 1789). J Comp Neurol 416:461-476
67. Younossi-Hartenstein A, Jones M, Hartenstein V (2001) The embryonic development of the nervous system of the temnocephalid flatworm Craspedella pedum. J Comp Neurol 434:56-68