Homeobox genes in axolotl lateral line placodes and neuromasts

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.

Evolution of electrosensory ampullary organs: conservation of Eya4 expression during lateral line development in jawed vertebrates

“…To our knowledge, the homeobox genes Msx2 and Dlx3 are the only previously described transcription factors expressed during neuromast and ampullary organ development in the axolotl: in the mature sense organs, both genes were reported to be expressed in the sensory receptor cells and support cells, though expression data were only shown for neuromasts (Metscher et al 1997). However, neither of these genes is expressed during neuromast or ampullary organ development in the paddlefish (M.S.M., unpublished data), suggesting they may not be conserved markers for lateral line sense organs in bony fishes.…”

Molecular analysis of neurogenic placode development in a basal ray‐finned fish

“…Only five molecular markers for vertebrate ampullary organs have previously been reported: in axolotl, Dlx3 and Msx2 (Metscher et al, 1997), and in sharks, Eya4 (O'Neill et al, 2007), Sox8, and ephrinB2 (Freitas et al, 2006). Hence, Sox3 is a novel molecular marker for vertebrate ampullary organs and also the first published molecular marker for actinopterygian ampullary organs.…”

Lateral Line Receptors: Where Do They Come from Developmentally and Where Is Our Research Going?

“…Metscher et al [1997] found that in axolotls homeobox genes Msx1 & 2 and Dlx3 are expressed in mature neuromast support cells, and Dlx3 is also expressed in mature hair cells. Interestingly, Msx2 and Dlx3 are expressed in differentiated primitive neuromasts but not in neuromast primordia [Metscher et al, 1997].…”

“…Dorsolateral placodes not only arise from the lateral walls of the hindbrain neural folds [Northcutt, 1996], but they do so in an anterior-posterior series. Metscher et al [1997] demonstrated Hox gene expression in at least one lateral line placode, and Northcutt [1996] suggested that each dorsolateral placode should have a unique pattern of Hox gene expression that could be altered by exposure to retinoic acid, which is involved with setting boundaries of Hox gene expression. Gibbs and Northcutt [2004b] have shown that when late gastrula -early neurula axolotl embryos were exposed to retinoic acid, embryos not only lost organization of their lateral line neuromasts in a dose dependent fashion, but also completely lost ampullary organs at the highest dose.…”