Identification of four Engrailed genes in the Japanese lamprey, Lethenteron japonicum

Abstract

We have isolated four homologs of Engrailed genes from the Japanese lamprey, Lethenteron japonicum, an agnathan that occupies a critical phylogenic position between cephalochordates and gnathostomes. We named these four genes LjEngrailedA, LjEngrailedB, LjEngrailedC, and LjEngrailedD. LjEngrailedA, LjEngrailedB, and LjEngrailedD share a major expression domain in the presumptive midbrain-hindbrain boundary region of the central nervous system, although their levels and timing of expression differed. On the other hand, LjEngrailedC transcripts were in the pharyngeal ectoderm and the ventral ectoderm of the body wall. In addition, LjEngrailedA was expressed in the ventral side of the epibranchial muscle precursors. LjEngrailedD transcripts were seen in the mesodermal cells of the mandibular arch and later in a group of cells responsible for the formation of the upper lip, lower lip, and velum. Our results provide clues to the evolution of these structures as well as a possible scenario for duplication events of Engrailed genes. Developmental Dynamics 237:1581-1589, 2008.

Cephalochordata

“…3.12 ; Hatta et al 1990 ;Holland et al 1993 ;Matsuura et al 2008 ;reviewed in Holland et al 2008b ;Sambasivan et al 2011 ). Moreover, one of the four lamprey Engrailed genes is expressed in the ectoderm of the pharyngeal arches (Matsuura et al 2008 ), similar to expression of amphioxus Engrailed in a stripe in the ectoderm ventral to the fi rst somite .…”

“…For example, Engrailed is expressed in the posterior wall of the anterior somites in amphioxus embryos; in the velar and upper lip muscles of the lamprey, which develop from the mandibular head cavity; in the mandibular arch in the shark; and in the jaw muscles of gnathostomes ( Fig. 3.12 ; Hatta et al 1990 ;Holland et al 1993 ;Matsuura et al 2008 ;reviewed in Holland et al 2008b ;Sambasivan et al 2011 ). Moreover, one of the four lamprey Engrailed genes is expressed in the ectoderm of the pharyngeal arches (Matsuura et al 2008 ), similar to expression of amphioxus Engrailed in a stripe in the ectoderm ventral to the fi rst somite .…”

Engrailed controls epaxial-hypaxial muscle innervation and the establishment of vertebrate three-dimensional mobility

“…Recent studies showed that the lamprey harbours four En genes that were multiplied independently in the agnathan lineage and may have assumed novel roles (Matsuura et al, 2008). Remarkably, one of these genes is initially expressed in the centre of the somite before adopting a more widespread pattern (Hammond et al, 2009).…”

“…Yet distinct dorsal and ventral rami of the spinal nerves that can trigger localised dorsal or ventral muscle contraction (Wallen et al, 1985) as well as centralised embryonic Engrailed expression are already present (Hammond et al, 2009;Matsuura et al, 2008). In crown group gnathostomes, epaxial-hypaxial muscle segregation and innervation is well established (reviewed in (Fetcho, 1987).…”

Development of the head and trunk mesoderm in the dogfish, Scyliorhinus torazame: II. Comparison of gene expression between the head mesoderm and somites with reference to the origin of the vertebrate head

“…7. Gene expressions of cyclostome are based both on lamprey and hagfish data (Engrailed: Matsuura et al 2008;Pax3/7: MaCauley andBronner-Fraser 2002, Kusakabe et al 2010;MRF-A: Kusakabe et al 2010;Pax1/9: Ota et al 2011;Bapx: Cerny et al 2010;PitxA: Boorman andShimeld 2002a, Uchida et al 2003;Tbx1/10: Sauka-Spengler et al 2002, andTiecke et al 2007). Embryonic expression of orthologous genes in the mesodermal components are compared between amphioxus, cyclostomes, S. torazame, and amniotes.…”