Characterization of the Hydra Lamin and Its Gene: A Molecular Phylogeny of Metazoan Lamins

Abstract

We report sequences for nuclear lamins from the teleost fish Danio and six invertebrates. These include two cnidarians (Hydra and Tealia), one priapulid, two echinoderms, and the cephalochordate Branchiostoma. Combining these results with earlier data on Drosophila, Caenorhabditis elegans, and various vertebrates, the following conclusions on lamin evolution can be drawn. First, all invertebrate lamins resemble in size the vertebrate B-type lamin. Second, all lamins described previously for amphibia, birds and mammals as well as the first lamin of a fish, characterized here, show a cluster of 7 to 12 acidic residues in the tail domain. Since this acidic cluster is absent from all invertebrate lamins including that of the cephalochordate Branchiostoma, it was acquired with the vertebrate lineage. The larger A-type lamin of differentiated cells must have arisen subsequently by gene duplication and insertion of an extra exon. This extra exon of the vertebrate A-lamins is the only major change in domain organization in metazoan lamin evolution. Third, the three introns of the Hydra and Priapulus genes correspond in position to the last three introns of vertebrate B-type lamin genes. Thus the entirely different gene organization of the C. elegans and Drosophila Dmo genes seems to reflect evolutionary drift, which probably also accounts for the fact that C. elegans has the most diverse lamin sequence. Finally we discuss the possibility that two lamin types, a constitutively expressed one and a developmentally regulated one, arose independently on the arthropod and vertebrate lineages.

Flanking genes of an essential gene give information about the evolution of metazoa

“…The corresponding B3 (LIII) gene was first described by Doring and Stick (1990). It is also described for the fish Danio rerio (Erber et al, 1999). We now find that the gene is located on chromosome 10.…”

“…While the Hydra lamin has a nuclear location signal with only 3 basic amino acid residues (KRSR) and an unusual basic cluster RRIRKRR, cell biological experiments show that this cluster is not responsible for nuclear uptake (Erber et al, 1999). We now recognise in the Nematostella lamin also a nuclear location signal with only three basic residues (KRAR) and also a basic stretch close to the carboxy terminal end (RRGRGRR).…”

“…We were therefore surprised when we interpreted the Nematostella lamin gene and did not put our Hydra gene in the summary, but mentioned it only in the text with the note that we did not know whether our intron mapping procedure had been correct (Zimek and Weber, 2008). It was clearly not and this most likely concerns also the Priapulus caudatus lamin gene where we reported also only 3 introns (Erber et al, 1999). Chapman et al (2010) report that the sequence divergence between a Hydra peptide and its Nematostella orthologue is typically greater than the sequence divergence between the Nematostella and its human orthologue.…”

“…We had previously cloned the Hydra gene from Hydra attenuata (Erber et al, 1999). The deduced cDNA and protein sequences show 99% identity with the new data from Hydra magnipapillata.…”

Functions and dysfunctions of the nuclear lamin Ig-fold domain in nuclear assembly, growth, and Emery–Dreifuss muscular dystrophy

“…We determined the effects of a point mutation, R454W, in LB3T-Ig (LB3T-IgRW) on nuclear assembly. This site was chosen because it is one of the most highly conserved sites within lamin Ig-folds across invertebrate and vertebrate species [from hydra to human (47)] and corresponds to the human LA R453W mutant, which causes EDMD (48). This mutation removes a salt bridge between two ␤-strands, thereby destabilizing the structure of the Ig-fold (7).…”