Homeobox genes in axolotl lateral line placodes and neuromasts

B D Metscher,Susan V Bryant,David M Gardiner,R Glenn Northcutt

doi:10.1007/s004270050116

B D Metscher, Susan V Bryant + Show 2 more

Open Access

https://doi.org/10.1007/s004270050116

Copy DOI

Abstract

Gene expression has been studied in considerable detail in the developing vertebrate brain, neural crest, and some placode-derived organs. As a further investigation of vertebrate head morphogenesis, expression patterns of several homeobox-containing genes were examined using whole-mount in situ hybridization in a sensory system primitive for the vertebrate subphylum: the axolotl lateral lines and the placodes from which they develop. Axolotl Msx-2 and Dlx-3 are expressed in all of the lateral line placodes. Both genes are expressed throughout development of the lateral line system and their expression continues in the fully developed neuromasts. Expression within support cells is highly polarized. In contrast to most other observations of Msx genes in vertebrate organogenesis, expression of Msx-2 in developing lateral line organs is exclusively epithelial and is not associated with epithelial-mesenchymal interactions. A Hox-complex gene, Hoxb-3, is shown to be expressed in the embryonic hindbrain and in a lateral line placode at the same rostrocaudal level, but not in other placodes nor in mature lateral line organs. A Hox gene of a separate paralog group, Hoxa-4, is expressed in a more posterior hindbrain domain in the embryo, but is not expressed in the lateral line placode at that rostrocaudal level. These data provide the first test of the hypothesis that the neurogenic placodes develop in two rostrocaudal series aligned with the rhombomeric segments and patterned by combinations of Hox genes in parallel with the central nervous system.

Highlights

&p.1:Abstract Gene expression has been studied in considerable detail in the developing vertebrate brain, neural crest, and some placode-derived organs
The embryonic central nervous system, neural crest mesenchyme, and tissues in later organogenesis are known to express genes of the Hox, Msx and Dlx families during morphogenesis, and genes of all of these groups have been characterized in a number of animal lineages (Akimenko et al 1994, 1995; Holland 1992; Krumlauf 1994; Ma et al 1996; Robinson and Mahon 1994)
Hoxb-3 is expressed in the hindbrain and middle lateral line placode, which lies adjacent to the region of hindbrain expression; Hoxa-4 is expressed in a more posterior hindbrain domain, but not in the lateral line placode at that axial level

Summary

Introduction

&p.1:Abstract Gene expression has been studied in considerable detail in the developing vertebrate brain, neural crest, and some placode-derived organs. The phylogenetic distribution of conserved sequences within and outside of the homeobox suggests that these genes may have functions important in animal development generally, and the similarities of expression patterns in various vertebrates may be indicative of some developmental roles retained in the different lineages from their common chordate ancestor (Holland et al 1994; Sharman and Holland 1996) These same genes might be expected to be associated with the development of a sensory system primitive for the vertebrates, such as lateral lines (Northcutt 1989). We describe the expression of two non-Hox homeobox genes, Msx-2 and Dlx-3, in the placodes, and their continued expression in mature lateral line sensory organs

Methods

Results

Conclusion