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Identification of Four Engrailed Genes in the Japanese Lamprey

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Identification of Four Engrailed Genes in the Japanese Lamprey DEVELOPMENTAL DYNAMICS 237:1581–1589, 2008 RESEARCH ARTICLE Identification of Four Engrailed Genes in the Japanese Lamprey, Lethenteron japonicum Manami Matsuura,1 Hidenori Nishihara,2 Koh Onimaru,1 Nobuhiro Kokubo,1 Shigehiro Kuraku,3† Rie Kusakabe,3‡ Norihiro Okada,2 Shigeru Kuratani,3 and Mikiko Tanaka1* 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. © 2008 Wiley-Liss, Inc. Key words: Engrailed; lamprey; homeodomains; midbrain; hindbrain; epibranchial muscle; mandibular arch Accepted 24 March 2008 INTRODUCTION 1976). En homologs have been cloned teleosts produced four En homologs from several protochordates (Holland in zebrafish: eng1a (renamed eng1), The Engrailed (En) genes encode a et al., 1997; Imai et al., 2002) and eng1b, eng2a (renamed eng2), and highly conserved homeodomain-con- many vertebrate species (Joyner et eng2b (renamed eng3) (Ekker et al., taining transcription factor and play pivotal roles in morphogenesis in in- al., 1985). The cephalochordate Bran- 1992; Force et al., 1999). Four En vertebrate and vertebrate develop- chiostoma floridae and urochordate paralogues, En-1A, En-1B, En-2A, and ment (Gibert, 2002). In Drosophila, Ciona intestinalis are reported to have En-2B have also been identified in the engrailed is known as a selector gene, only a single En gene, whereas chick, tetraploid Xenopus laevis (Holland as it is involved in the development of mouse, and humans contain two mem- and Williams, 1990; Hemmati-Brivan- appendages and in the establishment bers of the En family, En-1 and En-2 lou et al., 1991). In cephalochordates of segments, whereby it specifies the (Joyner et al., 1985; Joyner and Mar- and vertebrates, segmentally reiter- posterior identity of each compart- tin, 1987; Poole et al., 1989; Holland et ated En expression has been observed ment (Garcia-Bellido and Santama- al., 1997; Imai et al., 2002). Whole ge- in the paraxial mesoderm (Davidson ria, 1972; Lawrence and Morata, nome duplication prior to the origin of et al., 1988; Ekker et al., 1992; Hol- 1Laboratory for Developmental Biology, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan 2Laboratory for Molecular Evolution, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, Yokohama, Japan 3Laboratory for Evolutionary Morphology, Center for Developmental Biology, RIKEN, Kobe, Japan Grant sponsor: Ministry of Education, Science, Sports and Culture of Japan; Grant sponsor: Hayashi Memorial Foundation of Female Natural Scientists. †Shigehiro Kuraku’s present address is Laboratory of Zoology and Evolutionary Biology, Department of Biology, University of Konstanz, Universitaetsstrasse 10, 78457 Konstanz, Germany. ‡Rie Kusakabe’s present address is Department of Biology, Graduate School of Science, Kobe University, 1-1 Rokkodaicho, Nadaku, Kobe 657-8501, Japan. *Correspondence to: Mikiko Tanaka, Graduate School of Bioscience and Biotechnology, Tokyo Institute of Technology, B-17, 4259 Nagatsuta-cho, Midori-ku, Yokohama 226-8501, Japan. E-mail: [email protected] DOI 10.1002/dvdy.21552 Published online 9 May 2008 in Wiley InterScience (www.interscience.wiley.com). © 2008 Wiley-Liss, Inc. 1582 MATSUURA ET AL. land et al., 1997). In amphioxus, midbrain and hindbrain of the neural they seem to have duplicated within metameric expression of AmphiEn in epithelium (Davis et al., 1991; Ekker the lineage (Holland and Williams, the forming somites was observed et al., 1992). Recent studies in mice 1990). En protein distribution has (Holland et al., 1997). Somitic En-1 showed that the development of the been studied in the lamprey using the expression was also observed in the tectum (midbrain) and cerebellum polyclonal antiserum aEnhb-1 raised muscle pioneer-like cells in the prim- (hindbrain) depends upon the dose of against mouse En protein (Holland et itive cartilaginous dogfish Scyliorhi- En proteins expressed in the mid- al., 1993). However, no En mRNA ex- nus canicula (Tanaka et al., 2002). In brain-hindbrain boundary (Sgaier et pression patterns have been described zebrafish, eng1a and eng2a expression al., 2007). In chick and mouse em- in lamprey during embryogenesis. was also observed in a subset of mus- bryos, ectodermal expression of En-1 In this study, we obtained 3 novel cle precursor cells in the myotomes, is seen in the ventral compartment of En sequences LjEnB, LjEnC, and such as muscle pioneers, during somi- the body epidermis at the pre-fin/limb LjEnD, in a Japanese lamprey, togenesis (Ekker et al., 1992). A small bud stage and then in the ventral ec- Lethenteron japonicum. Moreover, the cluster of mesodermal cells in the toderm and ventral apical ridge of nucleotide sequence of the previously mandibular arch also express eng2a limb buds where it positions limbs at reported partial LjEnA gene (Takio et and eng2b during zebrafish embryo- the dorso-ventral boundary (Loomis et al., 2007) was extended and its expres- genesis (Ekker et al., 1992). These al., 1996; Laufer et al., 1997; Rodri- sion was analayzed throughout em- cells seem to be the jaw muscle pre- guez-Esteban et al., 1997; Tanaka et bryogenesis. Phylogenetic and expres- cursor cells derived from the paraxial al., 1998). This limb-positioning mech- sion analyses provided valuable mesoderm (Hatta et al., 1990) and anism of En-1 appears to be also con- insights into the evolution of verte- similar mandibular En expression is served in the primitive cartilaginous brate novel morphologies, as well as a observed in Xenopus laevis (Hemmati- dogfish (Tanaka et al., 2002). possible model of duplication events Brivanlou et al., 1991), chick (Gardner Because the above-mentioned re- whereby En genes have undergone and Barald, 1992), and mouse (Logan gions of En expression, including mus- subfunctionalization of their roles. et al., 1993). En-expression has been cle of the oral apparatus, tectum, and observed in the somites of chick and cerebellum, and function are major mice specifically in the dermis precur- morphological innovations along the RESULTS sor cells (Davis et al., 1991; Gardner chordate lineage, examination of En Identification of En and Barald, 1992). expression in agnathan lampreys Sequences in the Lamprey En expression is also observed in should provide further understanding neurons of hemichordates and various of vertebrate evolution. As Verte- L. japonicum chordates (Davis et al., 1991; Holland brates acquired the jaw after the ori- To identify En genes in the lamprey et al., 1997; Imai et al., 2002; Lowe et gin of agnathan vertebrates, expres- L. japonicum, we used an RT-PCR al., 2003). In the hemichordate Sacco- sion pattern of lamprey En genes in approach with stage-21 to -30 em- glossus kowalevski, which lacks a cen- the pharyngeal regions should provide bryos using degenerate primers. tralized nervous system, En is significant insights into the acquisi- This strategy led to amplification of strongly expressed in the anterior me- tion of the jaw in vertebrate evolution. several fragments of En genes. sosome of the neurogenic ectoderm as The optic tectum and cerebellum are Three of them, which we named a narrow single band (Lowe et al., the novel morphological innovations LjEngrailedA (LjEnA; Takio et al., 2003). In chordates, the ectoderm be- in vertebrate evolution; thus delineat- 2007), LjEngrailedB (LjEnB), LjEn- comes partitioned into the neuroecto- ing the expression patterns of the lam- grailedC (LjEnC), were closely re- derm and the non-neural ectoderm prey En genes should provide further lated to gnathostome En genes and (also named general ectoderm; Hol- understanding for the evolution of the were further characterized. We ex- land, 2005), both of which appear to be subdivisions of the brain. Although tended their sequences using a combi- patterned along the anterior-posterior the lamprey lacks paired fins, some nation of 5Ј and 3Ј RACE to yield 873-, axis by a common mechanism (Hol- agnathan fossils seem to have one set 784-, and 167-bp fragments, corre- land, 2005). In amphioxus, AmphiEn of paired fins, and these ancestral ag- sponding, respectively, to each gene. is expressed in a small cluster of cells nathan fish might have already had The ortholog of LjEnC was then ex- in the dorsal nerve cord and the cere- dorso-ventral compartmentalization. tended 264 bp using primers against bral vesicle, and it is transiently ex- Thus, examination of En gene expres- the EnC sequences from sea lamprey pressed in a band of cells of the gen- sion patterns in the body ectoderm of (Petromyzon marinus) retrieved from eral ectoderm (Holland et al., 1997; lamprey embryos could provide in- the NCBI Trace Archive database Holland, 2005). In Ciona intestinalis, sight into the evolutionary process of (http://www.ncbi.nlm.nih.gov/Traces/). Ci-En is restricted to two domains of these appendages (Tanaka et al., The sequence of LjEnC was further the central nervous system during 2002). extended using 3Ј RACE to yield embryogenesis: the midbrain and the In lampreys, only a single En se- 661-bp fragments. An additional En midbrain-hindbrain boundary (Imai quence has been identified in Lam- gene, P. marinus EnD (PmEnD), was et al., 2002).
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