Evolutionary aspects in intermediate filament proteins

Peter, Annette; Stick, Reimer

doi:10.1016/j.ceb.2014.12.009

Cited by 67 publications

(45 citation statements)

References 69 publications

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“…Certainly, the notion of IF proteins localizing in the nucleus is not unprecedented, because the A-, B-, and C-type lamins are bona fide nuclear proteins responsible for the formation of a dense meshwork of 10-nm filaments covering the inner surface of the nuclear envelope (Aebi et al, 1986), as well as a diffuse, less well-defined structure in the nucleoplasm (Bridger et al, 1993). In fact, IF proteins are believed to have initially appeared as nuclear-localized elements in more ‘‘primitive’’ organisms (Peter and Stick, 2015), as inferred from the notion that the two IF-encoding genes found in Drosophila melanogaster and the lone IF-encoding gene in Dictyostelium discoidum encode lamin-like proteins that localize to the nucleus (Erber et al, 1998; Krüger et al, 2012). The loss of a small exon coding for a classical nuclear localization signal (NLS) along with a membrane-targeting CAAX motif likely facilitated the appearance of lamin-like IFs in the cytoplasm at some point during metazoan evolution (Peter and Stick, 2015).…”

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confidence: 99%

“…In fact, IF proteins are believed to have initially appeared as nuclear-localized elements in more ‘‘primitive’’ organisms (Peter and Stick, 2015), as inferred from the notion that the two IF-encoding genes found in Drosophila melanogaster and the lone IF-encoding gene in Dictyostelium discoidum encode lamin-like proteins that localize to the nucleus (Erber et al, 1998; Krüger et al, 2012). The loss of a small exon coding for a classical nuclear localization signal (NLS) along with a membrane-targeting CAAX motif likely facilitated the appearance of lamin-like IFs in the cytoplasm at some point during metazoan evolution (Peter and Stick, 2015). The element of intrigue here is that at least some, and perhaps many, of the remaining 68 non-lamin polypeptides forming the modern IF superfamily may not exhibit an exclusively cytoplasmic localization in interphase cells, as previously thought.…”

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confidence: 99%

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Keratins Are Going Nuclear

2016

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Previously thought to reside exclusively in the cytoplasm, the cytoskeletal protein keratin 17 (K17) has been recently identified inside the nucleus of tumor epithelial cells with a direct impact on cell proliferation and gene expression. We comment on fundamental questions raised by this new finding and the associated significance. Everything should be made as simple as possible, but not simpler.Albert Einstein

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Keratins Are Going Nuclear

2016

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“…It was once thought that insects do not require IF proteins due to their stabilizing chitin‐based exoskeleton (Herrmann & Strelkov, ) and that the metazoan fresh‐water polyp Hydra attenuata represents the most basal branching eukaryote to possess IF proteins (Erber et al, ; Peter & Stick, ). Both views changed with the discovery of isomin, a cytoplasmic IF protein in the hexapod Isotomurus maculatus (Mencarelli, Ciolfi, Caroti, Lupetti, & Dallai, ) and the identification of the lamin homolog NE81 in the amoeba Dictyostelium discoideum (Kruger et al, ).…”

Section: When the Definitions Fail And Lamins Are No Longer A Metazoamentioning

confidence: 99%

“…The identification of IF proteins beyond metazoans is an onerous task. Metazoan IF proteins are primarily defined and identified through the tertiary structure they are predicted to form and their biochemical properties such as detergent‐resistance, but not primary amino acid sequence (Herrmann & Strelkov, ; Peter & Stick, ). IF protein families exhibit a strong heterogeneity, leading to uncertain assignments among the individual classes.…”

Section: The Challenges Of Intermediate Filament Protein Identificationmentioning

confidence: 99%

“…Crucial for their integration into the nucleus is a nucleus localization signal (NLS) and a CaaX-motif within the carboxy-terminal tail-domain. The presence of these two domains are one of the major structural differences that distinguish lamins from cytoplasmic IF proteins (Peter & Stick, 2015). Lamin is considered to represent the most primordial IF protein (Dodemont, Riemer, & Weber, 1990;Erber et al, 1999), which is why the identification of lamin homologs throughout eukaryotic diversity (Kollmar, 2015;Koreny & Field, 2016) was a game changer, as it demonstrated this nuclear IF protein not to be a metazoan invention.…”

Section: Wh E N T He D Ef I Ni T Ion S F a I L A N D La M I Ns Ar Ementioning

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Intermediate filament protein evolution and protists

et al. 2018

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Metazoans evolved from a single protist lineage. While all eukaryotes share a conserved actin and tubulin-based cytoskeleton, it is commonly perceived that intermediate filaments (IFs), including lamin, vimentin or keratin among many others, are restricted to metazoans. Actin and tubulin proteins are conserved enough to be detectable across all eukaryotic genomes using standard phylogenetic methods, but IF proteins, in contrast, are notoriously difficult to identify by such means. Since the 1950s, dozens of cytoskeletal proteins in protists have been identified that seemingly do not belong to any of the IF families described for metazoans, yet, from a structural and functional perspective fit criteria that define metazoan IF proteins. Here, we briefly review IF protein discovery in metazoans and the implications this had for the definition of this protein family. We argue that the many cytoskeletal and filament-forming proteins of protists should be incorporated into a more comprehensive picture of IF evolution by aligning it with the recent identification of lamins across the phylogenetic diversity of eukaryotic supergroups. This then brings forth the question of how the diversity of IF proteins has unfolded. The evolution of IF proteins likely represents an example of convergent evolution, which, in combination with the speed with which these cytoskeletal proteins are evolving, generated their current diversity. IF proteins did not first emerge in metazoa, but in protists. Only the emergence of cytosolic IF proteins that appear to stem from a nuclear lamin is unique to animals and coincided with the emergence of true animal multicellularity.

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Role of Intermediate Filaments in Cell Locomotion

Fujiwara

Mizuno

2017

Encyclopedia of Life Sciences

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Cell locomotion is essential for diverse pathophysiological processes, including embryogenesis, immune responses, wound healing and cancer metastasis. Intermediate filaments (IFs) are resilient cytoskeleton components that provide structural support and mechanical protection. Accumulating evidence suggests that IFs are dynamic structures that function as a scaffold for signalling networks, which regulate cell locomotion, shape change and mechanical responses. The dynamics of IFs are regulated by posttranslational modifications, crosstalk with other cytoskeletons and association with cell adhesion complexes. IFs differentially regulate cell locomotion, depending on the particular IF protein, the cell type, the cellular context and the mode of cell migration. In general, vimentin filaments promote and keratin filaments inhibit cell locomotion. These cytoplasmic IFs regulate cell locomotion by modulating the localisation and activity of signalling molecules and influencing the stability of cell–cell and cell–substrate adhesion complexes. Nuclear lamin‐A represses cell locomotion by stiffening the nucleus. Key Concepts Intermediate filaments (IFs) constitute the resilient cytoskeleton that provides structural support and protects cells from external forces. IFs function as a dynamic scaffold for signalling networks that regulate locomotion, shape change and mechanical responses. Cytoplasmic IFs are linked to desmosomes and hemidesmosomes at cell adhesion sites and linker of nucleoskeleton and cytoskeleton (LINC) complexes on the nuclear membrane. The reorganisation and dynamics of IFs are regulated by posttranslational modifications, crosstalk with other cytoskeletons and association with cell adhesion complexes. IFs differentially regulate cell locomotion, depending on the particular IF protein, the cell type, the cellular context and the mode of cell migration. Vimentin IFs generally promote cell locomotion by destabilising desmosomes, promoting focal adhesion maturation and affecting the activity of signalling molecules. Keratin IFs generally repress cell locomotion by stabilising desmosomes and hemidesmosomes and affecting the localisation and activity of signalling molecules. Nuclear lamin‐A represses cell locomotion by stiffening the nucleus. Keratin IFs and Rho signalling are mutually regulated, providing a feedback mechanism during mechanical responses.

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Evolutionary aspects in intermediate filament proteins

Cited by 67 publications

References 69 publications

Keratins Are Going Nuclear

Keratins Are Going Nuclear

Intermediate filament protein evolution and protists

Role of Intermediate Filaments in Cell Locomotion

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