Novel origin of lamin-derived cytoplasmic intermediate filaments in tardigrades.

Lars Hering,Jamal-Eddine Bouameur,Julian Reichelt,Thomas M Magin,Georg Mayer

doi:10.7554/elife.11117

Lars Hering, Jamal-Eddine Bouameur + Show 3 more

Open Access

https://doi.org/10.7554/elife.11117

Copy DOI

Journal: eLife	Publication Date: Feb 3, 2016
Citations: 42	License type: CC BY 4.0

Affiliation: Leipzig University, University of Kassel

Abstract

Intermediate filament (IF) proteins, including nuclear lamins and cytoplasmic IF proteins, are essential cytoskeletal components of bilaterian cells. Despite their important role in protecting tissues against mechanical force, no cytoplasmic IF proteins have been convincingly identified in arthropods. Here we show that the ancestral cytoplasmic IF protein gene was lost in the entire panarthropod (onychophoran + tardigrade + arthropod) rather than arthropod lineage and that nuclear, lamin-derived proteins instead acquired new cytoplasmic roles at least three times independently in collembolans, copepods, and tardigrades. Transcriptomic and genomic data revealed three IF protein genes in the tardigrade Hypsibius dujardini, one of which (cytotardin) occurs exclusively in the cytoplasm of epidermal and foregut epithelia, where it forms belt-like filaments around each epithelial cell. These results suggest that a lamin derivative has been co-opted to enhance tissue stability in tardigrades, a function otherwise served by cytoplasmic IF proteins in all other bilaterians.

Highlights

Tardigrades, known as water bears, are microscopic invertebrates that live in marine, freshwater and semi-aquatic/limno-terrestrial environments (Kinchin, 1994; Nelson, 2002) (Figure 1)
The integrity and plasticity of tardigrade tissues might be achieved by specialised cytoskeletal components, such as Intermediate filament (IF) proteins, which are known to be essential for stress resilience of cells (Herrmann et al, 2009; Coulombe and Wong, 2004; Kim and Coulombe, 2007)
A group of IF proteins found in the nucleus, occur in most eukaryotes, including social amoebae (Kruger et al, 2012) and all metazoans (Dittmer and Misteli, 2011), cytoplasmic IF proteins are thought to have evolved from an ancestral lamin gene by duplication in the bilaterian lineage (Erber et al, 1999; Herrmann and Strelkov, 2011)

Summary

Introduction

Tardigrades, known as water bears, are microscopic invertebrates that live in marine, freshwater and semi-aquatic/limno-terrestrial environments (Kinchin, 1994; Nelson, 2002) (Figure 1). The apparent loss of cytoplasmic IF proteins in the arthropod lineage might correlate with the acquisition of an exoskeleton (Herrmann and Strelkov, 2011; Goldstein and Gunawardena, 2000; Erber et al, 1998), which provides mechanical support to the arthropod skin The fact that cytotardin is only found in the skin of the tardigrade and in those tissues that experience mechanical stress (for example, the mouth and legs) hints that it might help stabilize these cells This could mean that the protein helps these animals to resist extreme conditions.

Results and discussion

Materials and methods

Funding Funder