Abstract
TWIST1 encodes a transcription factor that contains a highly conserved basic helix–loop–helix DNA-binding domain and a WR motif. We have isolated a full-length complementary DNA of the zebrafish ortholog of TWIST1 and determined its genomic organization. Inter-species comparisons reveal a remarkable degree of conservation at the gene structure, nucleotide, and predicted peptide levels across large evolutionary distances. Using reverse-transcription polymerase chain reaction analysis and in situ hybridization analyses of whole mount and cryosectioned zebrafish embryos, we detected maternal twist1 transcript in the zygote. During somitogenesis, twist1 transcripts were detected in the intermediate mesoderm from the 2-somite to 18-somite stages, followed by expression in the somites from the 5-somite stage to the 24-somite stage. Also, beginning at the two-somite stage, twist1 expression was observed in head mesenchyme and, subsequently, in neural crest-derived pharyngeal arches as the embryo developed. At the 24-hpf stage, twist1 transcripts were also observed in the ventral tail-bud region. These observations are consistent with a role for twist1 in craniofacial, vertebral, and early renal development.
References
Akimenko MA, Ekker M, Wegner J, Lin W, Westerfield M (1994) Combinatorial expression of three zebrafish genes related to distal-less: part of a homeobox gene code for the head. J Neurosci 14:3475–3486
Baylies MK, Bate M (1996) Twist: a myogenic switch in Drosophila. Science 272:1481–1484
Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G (2004) A twist code determines the onset of osteoblast differentiation. Dev Cell 6:423–435
Fuchtbauer EM (1995) Expression of M-twist during postimplantation development of the mouse. Dev Dyn 204:316–322
Germanguz I, Lev D, Waisman T, Kim CH, Gitelman I (2007) Four twist genes in zebrafish, four expression patterns. Dev Dyn 236:2615–2626
Hopwood ND, Pluck A, Gurdon JB (1989) A Xenopus mRNA related to Drosophila twist is expressed in response to induction in the mesoderm and the neural crest. Cell 59:893–903
Jan YN, Jan LY (1993) HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell 75:827–830
Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF (1995) Stages of embryonic development of the zebrafish. Dev Dyn 203:253–310
Majumdar A, Lun K, Brand M, Drummond IA (2000) Zebrafish no isthmus reveals a role for pax2.1 in tubule differentiation and patterning events in the pronephric primordia. Development 127:2089–2098
Oktenli C, Saglam M, Zafer E, Gul D (2002) Saethre–Chotzen syndrome presenting with incomplete renal Fanconi syndrome. Nephron 92:463–465
Rauch GJ, Lyons DA, Middendorf I., Friedlander B, Arana N, Reyes T, Talbot WS (2003) Submission and curation of gene expression data. ZFIN direct data submission
Renn J, Schaedel M, Volff JN, Goerlich R, Schartl M, Winkler C (2006) Dynamic expression of sparc precedes formation of skeletal elements in the Medaka (Oryzias latipes). Gene 372:208–218
Russo R, D’Armiento M, Vecchione R (1991) Renal tubular dysgenesis and very large cranial fontanels in a family with acrocephalosyndactyly S.C. type. Am J Med Genet 39:482–485
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Solnica-Krezel L (2002) Pattern formation in zebrafish. Springer, Heidelberg
Soo K, O’Rourke MP, Khoo PL, Steiner KA, Wong N, Behringer RR, Tam PP (2002) Twist function is required for the morphogenesis of the cephalic neural tube and the differentiation of the cranial neural crest cells in the mouse embryo. Dev Biol 247:251–270
Spring J, Yanze N, Middel AM, Stierwald M, Groger H, Schmid V (2000) The mesoderm specification factor twist in the life cycle of jellyfish. Dev Biol 228:363–375
Stoetzel C, Bolcato-Bellemin AL, Bourgeois P, Perrin-Schmitt F, Meyer D, Wolff M, Remy P (1998) X-twi is expressed prior to gastrulation in presumptive neurectodermal and mesodermal cells in dorsalized and ventralized Xenopus laevis embryos. Int J Dev Biol 42:747–756
Tavares AT, Izpisuja-Belmonte JC, Rodriguez-Leon J (2001) Developmental expression of chick twist and its regulation during limb patterning. Int J Dev Biol 45:707–713
Thisse B, el Messal M, Perrin-Schmitt F (1987) The twist gene: isolation of a Drosophila zygotic gene necessary for the establishment of dorsoventral pattern. Nucleic Acids Res 15:3439–3453
Thisse B, Stoetzel C, Gorostiza-Thisse C, Perrin-Schmitt F (1988) Sequence of the twist gene and nuclear localization of its protein in endomesodermal cells of early Drosophila embryos. EMBO J 7:2175–2183
Westerfield M (2000) The zebrafish book: a guide for the laboratory use of zebrafish (Danio rerio). University of Oregon Press, Eugene, OR
Wolf C, Thisse C, Stoetzel C, Thisse B, Gerlinger P, Perrin-Schmitt F (1991) The M-twist gene of Mus is expressed in subsets of mesodermal cells and is closely related to the Xenopus X-twi and the Drosophila twist genes. Dev Biol 143:363–373
Yasutake J, Inohaya K, Kudo A (2004) Twist functions in vertebral column formation in medaka, Oryzias latipes. Mech Dev 121:883–894
Acknowledgment
We thank Vladimir Korzh (Institute of Molecular and Cell Biology, Singapore) and Karuna Sampath (Temasek Life Science Laboratories, Singapore) for invaluable advice, Shangwei Chong, Nick Qiu (IMCB), and Jin Ben for technical assistance. This work was supported by a grant from the National University of Singapore Academic Research Fund (R178-000-104-112) to SSC.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Hammerschmidt
At the time of acceptance of this manuscript, a publication entitled “Four twist genes in zebrafish, four expression patterns” by Germanguz et al. appeared in the August 2007 issue of Developmental Dynamics.
Rights and permissions
About this article
Cite this article
Yeo, GH., Cheah, F.S.H., Jabs, E.W. et al. Zebrafish twist1 is expressed in craniofacial, vertebral, and renal precursors. Dev Genes Evol 217, 783–789 (2007). https://doi.org/10.1007/s00427-007-0187-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-007-0187-7