Intermediate filaments

Intermediate filaments (IFs) make up one of three cytoskeletal systems in human cells. This family of proteins include cytoplasmic intermediate filaments, which form an extensive network through the cytosol, as well as nuclear intermediate filaments, which form the thin nuclear lamina underlying the nuclear membrane. The major role for the cytoplasmic filaments is in providing structural organization and mechanical support to the cell, contributing to cell shape, cell migration and cell adhesion (Leduc C et al. (2015)). Nuclear lamins are involved in organization of chromatin. In the Human Protein Atlas, staining of proteins that localize to nuclear lamins appear as a staining of the nuclear membrane and are therefore not included in the annotation of intermediate filaments. Example images of proteins localizing to cytoplasmic intermediate filaments can be seen in Figure 1.

In the Cell Atlas, 185 genes (1% of all protein-coding human genes) have been shown to encode proteins that localize to intermediate filaments (Figure 2). A Gene Ontology (GO)-based functional enrichment analysis of genes encoding proteins that localize to intermediate filaments shows enrichment of terms related to the organization, assembly and functions of the intermediate filament cytoskeleton. About 69% (n=128) of the proteins localized to intermediate filaments are also detected in additional cellular compartments, the most common ones being the cytosol and the nucleus.

GFAP - U-2 OS
GFAP - HEK 293
NES - U-2 OS

KRT13 - A-431
KRT19 - RT4
DES - RH-30

Figure 1. Examples of proteins localized to the intermediate filaments. GFAP (detected in U-2 OS and HEK 293 cells) and NES (detected in U-2 OS cells). KRT13 (detected in A-431cells), KRT19 (detected in RT-4 cells) and DES (detected in RH-30 cells).

Figure 2. 1% of all human protein-coding genes encode proteins localized to the intermediate filaments. Each bar is clickable and gives a search result of proteins that belong to the selected category.

Structure of intermediate filaments

Intermediate filaments are assembled from a diverse family of proteins, unified by a characteristic tripartite structure and an ability to self-assemble into homo- or heteropolymeric filaments with a diameter of approximately 10 nm. This diversity, and the fact that intermediate filaments are non-polar, clearly distinguish them from the other cytoskeletal filaments in human cells (microtubules and actin filaments). Moreover, intermediate filaments are characterized by a high degree of stability and mechanical strength, while yet remaining dynamic.

There are currently more than 70 genes known to encode proteins that form intermediate filaments (Lowery J et al. (2015)). These proteins are classified into five or six subgroups, mainly based on sequence homology. The acidic and basic keratins are categorized into the type I and type II groups, respectively. Figure 3 shows immunofluorescent staining of keratins in different cell types. The type III igroup include vimentin (VIM), desmin (DES), glial fibrillary acidic protein (GFAP) and peripherin (PRPH). Neurofilament (NF) triplet proteins and α-internexin are categorized as type IV intermediate filament proteins, while the nuclear lamins are categorized as type V (7979242)). The sixth subgroup would contain nestin (NES) and synemin (SYNM) (Leduc C et al. (2015)), but they are often also categorized as type IV (Robert A et al. (2016); Fuchs E et al. (1994)). A selection of proteins suitable as markers for intermediate filaments can be found in Table 1. A list of highly expressed proteins that localize to intermediate filaments can be found in Table 2.

While intermediate filament proteins have an intrinsic ability to self-assemble, their in vivo assembly is a regulated process. Moreover, it has been demonstrated that intermediate filaments are continually undergoing assembly and disassembly, as well as exchange of subunits within existing filaments. This enables dynamic remodeling of the intermediate filament network, which is necessary for to adjust to changing needs in terms of mechanical support, flexibility and attachment to the surrounding matrix during differentiation and cellular processes such as migration and cell division (Robert A et al. (2016)).

Table 1. Selection of proteins suitable as markers for the intermediate filaments or its substructures.

Table 2. Highly expressed single localizing intermediate filaments proteins across different cell lines.

KRT17 - U-2 OS
KRT19 - MCF7
KRT14 - HaCaT

Figure 3. Examples of the morphology of intermediate filaments in different cell lines, represented by immunofluorescent staining of keratins: KRT17 in U-2 OS cells, KRT19 in MCF-7 cells and KRT14 in HaCaT cells.

Function of intermediate filaments

Intermediate filaments are essential for providing physical support and stability to cells and tissues, thereby enabling them to withstand mechanical stress and tension. A subgroup of intermediate filaments, VIM, has been shown to exhibit different properties when exposed to increasing levels of strain in vitro. When increasing the strain, the filaments were shown to stiffen and resist breakage (Janmey PA et al. (1991); Köster S et al. (2015)). Intermediate filaments have also been implicated in cell adhesion and mobility (Leduc C et al. (2015)). Indeed, there seems to be a dynamic rearrangement of intermediate filaments in response to changes in cell motility, as it has been shown that they are organized closer to the nuclear membrane in immobile cells, whereas in migrating cells they are aligned with lamella in the cell's leading edge. Both mutations in genes encoding cytoplasmic intermediate filaments, as well as genes coding for nuclear lamins, have been linked to a number of severe diseases (Herrmann H et al. (2007)).

A Gene Ontology (GO)-based analysis of genes encoding protein localized to intermediate filaments shows enrichment of terms for both biological processes (Figure 4a) and molecular functions (Figure 4b) that are well in-line with the known functions of the intermediate filaments, but also for cell differentiation during development of the placenta, which has been shown to involve differential expression of keratins (Gauster M et al. (2013)).

Figure 4a. Gene Ontology-based enrichment analysis for the intermediate filaments proteome showing the significantly enriched terms for the GO domain Biological Process. Each bar is clickable and gives a search result of proteins that belong to the selected category.

Figure 4b. Gene Ontology-based enrichment analysis for the intermediate filaments proteome showing the significantly enriched terms for the GO domain Molecular Function. Each bar is clickable and gives a search result of proteins that belong to the selected category.

Intermediate filament proteins with multiple locations

Approximately 69% (n=128) of the intermediate filament proteome detected in the Cell Atlas also localize to other compartments in the cell. The cytoscape network plot (Figure 5) shows that the most common location shared with intermediate filaments is cytosol and a hypergeometric test demonstrates that the number of proteins localizing to both of these compartments is significantly higher than expected. This could reflect cytosolic staining of soluble intermediate filament subunits, that have not assembled into filaments, or staining of proteins that interact with the soluble as well as the filamentous forms of intermediate filament proteins, or of proteins that connect intermediate filaments to other cellular structures.

Figure 5. Interactive network plot of intermediate filament proteins with multiple localizations. The numbers in the connecting nodes show the proteins that are localized to intermediate filaments and to one or more additional locations. Only connecting nodes containing more than one protein and at least 0.5% of proteins in the intermediate filament proteome are shown. The circle sizes are related to the number of proteins. The cyan colored nodes show combinations that are significantly overrepresented, while magenta colored nodes show combinations that are significantly underrepresented as compared to the probability of observing that combination based on the frequency of each annotation and a hypergeometric test (p≤0.05). Note that this calculation is only done for proteins with dual localizations. Each node is clickable and results in a list of all proteins that are found in the connected organelles.

Expression levels of intermediate filament proteins in tissue

Transcriptome analysis and classification of genes into tissue distribution categories (Figure 6) shows that a larger portion of genes encoding proteins that localize to intermediate filaments are detected in some tissues or in many tissues, while a smaller portion are detected in all tissues, compared to all genes presented in the Cell Atlas. This is well in-line with the known tissue type-dependent expression patterns of intermediate filament proteins (Herrmann H et al. (2007)).

Figure 6. Bar plot showing the percentage of genes in different tissue distribution categories for intermediate filament-associated protein-coding genes compared to all genes in the Cell Atlas. Asterisk marks a statistically significant deviation (p≤0.05) in the number of genes in a category based on a binomial statistical test. Each bar is clickable and gives a search result of proteins that belong to the selected category.

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