Evolution of the lamin protein family

Abstract

Lamins are the major components of the nuclear lamina, a filamentous layer found at the interphase between chromatin and the inner nuclear membrane. The lamina supports the nuclear envelope and provides anchorage sites for chromatin. Lamins and their associated proteins are required for most nuclear activities, mitosis, and for linking the nucleoskeleton to the network of cytoskeletal filaments. Mutations in lamins and their associated proteins give rise to a wide range of diseases, collectively called laminopathies. This review focuses on the evolution of the lamin protein family. Evolution from basal metazoans to man will be described on the basis of protein sequence comparisons and analyses of their gene structure. Lamins are the founding members of the family of intermediate filament proteins. How genes encoding cytoplasmic IF proteins could have arisen from the archetypal lamin gene progenitor, can be inferred from a comparison of the respective gene structures. The lamin/IF protein family seems to be restricted to the metazoans. In general, invertebrate genomes harbor only a single lamin gene encoding a B-type lamin. The archetypal lamin gene structure found in basal metazoans is conserved up to the vertebrate lineage. The completely different structure of lamin genes in Caenorhabditis and Drosophila are exceptions rather than the rule within their systematic groups. However, variation in the length of the coiled-coil forming central domain might be more common than previously anticipated. The increase in the number of lamin genes in vertebrates can be explained by two rounds of genome duplication. The origin of lamin A by exon shuffling might explain the processing of prelamin A to the mature non-isoprenylated form of lamin A. By alternative splicing the number of vertebrate lamin proteins has increased even further. Lamin C, an alternative splice form of the LMNA gene, is restricted to mammals. Amphibians and mammals express germline-specific lamins that differ in their protein structure from that of somatic lamins. Evidence is provided that there exist lamin-like proteins outside the metazoan lineage.

Phosphorylation of lamins determine their structural properties and signaling functions

“…9 Invertebrates have in general only one B-type lamin whereas A-type lamins only exist in vertebrates, indicating that lamin A is an evolutionary more recent protein. 10 The cytoplasmic IFs found in lower organisms are more closely related to lamins than to cytoplasmic IFs in higher organisms. 11 This indicates that a B-type lamin was the first IF to evolve and that this founder IF gradually gave rise to cytoplasmic IFs and later to A-type lamins.…”

Evolutionary history of the mammalian synaptonemal complex

“…Thus, the SC components are not the first case in which Drosophila and C. elegans hold a rather exceptional role. Evolutionary analysis of the lamin gene(s) in Metazoa for example revealed that just Drosophila and C. elegans exhibit an unusual gene organization most likely due to a strong genetic drift (Peter and Stick 2012).…”

Hydra meiosis reveals unexpected conservation of structural synaptonemal complex proteins across metazoans

“…An explanation for the strong differences in SC protein sequences between these two species and the other metazoans described here may be the evolutionary drift of ecdysozoans. This view is not without precedent in the literature as it has been already proposed for other structural proteins as is the case of lamins, the major components of the nuclear lamina (25,26), as well as for ribosomal DNA (27). In support of this, our bioinformatic analysis with C(3)G [the TF protein of D. melanogaster (28)] and SYP1-4 [the TF proteins of C. elegans (29)] in each case revealed only protein sequences from the respective genus, underscoring the proposal of a great sequence diversity and a rapid evolution within this clade (27).…”