Gelsolin interacts with LamR, hnRNP U, nestin, Arp3 and β-tubulin in human melanoma cells as demonstrated by immunoprecipitation and mass spectrometry (2023)

European Journal of Cell Biology

Volume 95, Issue 1,

January 2016

, pages 26-41

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Gelsolin, a multifunctional actin-binding protein, plays a role that is still not fully understood in tumorigenesis. Therefore, the aim of this study was to identify additional gelsolin molecular partners in human melanoma cells, separately in the cytoplasmic compartment and cell nuclei. To this end, we performed immunoprecipitation experiments based on a modified protocol followed by mass spectrometry. The obtained results were confirmed by Western blot analysis, proximity binding assays and confocal microscopy. As expected, gelsolin interacted with actin, in particular we demonstrated its interaction with cytoplasmic β and γ actins and a newly discovered actin isoform, actbl2. We have identified the ribosomal protein Rpsa, also known as the non-integrin laminin receptor (LamR), and the heterogeneous nuclear ribonucleoprotein hnRNP U as new interaction partners with gelsolin. Our data also indicate that gelsolin interacts with specific components of three cytoskeleton systems: nestin (intermediate filaments), Arp3 ( actin cytoskeleton) and β-tubulin (microtubules). We also report for the first time that gelsolin is a component of intermediate bodies, a tubulin-containing structure formed at the end of cytokinesis.


Gelsolin is a multifunctional actin binding protein and is involved in the dynamic reorganization of the actin cytoskeleton due to its capping, cleavage and, under certain circumstances, nucleation (Mannherz et al., 2010, Nag et al., 2013). Gelsolin is a member of the actin-binding protein (AbP) family of the gelsolin/villin family and is characterized by six homologous segments of approximately 14 kDa (Kwiatkowski et al., 1986). Gelsolin is found on the tips of lamellipodia or podosomes and invadopodia (Attanasio et al., 2011, Cervero et al., 2012, Mazur et al., 2010), i.e. on the structures responsible for the migration of macrophages and cancer cells. Gelsolin has also been localized in the cell nuclei of various types of cancer cells, including in astrocytoma (Ohnishi et al., 2009), in colorectal cancer cell subpopulations (Zhuo et al., 2012), and in melanoma cell lines (our unpublished observations), but its possible nuclear function is still not fully elucidated. Among members of the gelsolin family, only supervillin has a nuclear localization sequence (NLS), while gelsolin has neither an NLS nor a nuclear export signal (NES) (Li et al., 2012). Published data show that intracellular gelsolin exists in various states of activation, including free gelsolin and Ca2+bound gelsolin, but only free gelsolin can translocate to the nucleus (Van den Abbeele et al., 2010). On the other hand, it has been found that gelsolin can enter the cell nucleus in complex with a steroid hormone and its receptor (Ambrosino et al., 2010, Nishimura et al., 2003). Nishimura et al. (2003) postulated that the formation of the androgen:androgen-receptor:gelsolin complex is crucial for the interaction of the nuclear actin-activated receptor with RNA polymerase II. Although these data suggest that steroid hormones may be responsible for the nuclear localization of gelsolin in melanoma cells, we postulate that gelsolin may have additional functions in the cell nucleus. Indeed, recent data describes the interaction of gelsolin with FBXO25, an F-box protein that serves as a specificity factor for ubiquitin ligases found mainly in the nuclear domains associated with FBXO25 (FAND) (Teixeira et al., 2010).

Recent reports suggest that gelsolin plays a role in tumorigenesis as both a tumor suppressor and tumor promoter. These conflicting hypotheses are based on observations of a decrease in gelsolin levels (GSN)for example breast, bladder, colon, stomach, kidney, lung, oral, ovarian, pancreatic and prostate cancers (as reviewed by Li et al. (2012)) or upregulated in non-small cell lung cancer, urothelial carcinoma, pancreas and (Rao et al., 2002, Shieh et al., 2006, Thompson et al., 2007, Yang et al., 2004). Interestingly, biphasic gelsolin expression was observed during the transition from oral precancerous lesions to oral cancer (Shieh et al., 2006).GSNdownregulation was observed in precancerous lesions, whileGSNupregulation has been observed in oral cancer progression. In addition, gelsolin has been shown to positively stimulate the proliferation, migration and invasion of human oral squamous cell carcinoma cells (Deng et al., 2015).

We have previously shown that gelsolin is critical for the migration and invasion of colon adenocarcinoma and melanoma cell lines (Litwin et al., 2012, Litwin et al., 2009). In colon adenocarcinoma cells, overexpression of gelsolin resulted in an increase, while downregulationGSNexpression in melanoma cells resulted in reduced migration potential. In both cases, we observed dramatic changes in the organization of the actin cytoskeleton, i.e. a reduced polymerization state in gelsolin overexpressing cells and an increase in cytoplasmic stress fibers in gelsolin suppressed cells, reflecting the well-known actin cleavage activity. actin from gelsolin. However, gelsolin was present in A375 cell nuclei even 72h after downregulation was startedGSNexpression, although the amount of gelsolin clearly decreased in the cytoplasmic compartment (Litwin et al., 2012). These intriguing observations inspired us to investigate nuclear gelsolin and its possible interaction partners in more detail. For this study, we selected established cell lines derived from human melanoma and aimed to identify gelsolin's molecular partners, with particular emphasis on possible gelsolin nuclear interaction partners.

To this end, we optimized the procedure for immunoprecipitation of endogenous gelsolin from whole cell lysates (WCL) and nuclear fractions (NF) of melanoma cells. Since our aim was to focus on downstream interactions of endogenous gelsolin, we did not use cells transfected with overexpressed tagged gelsolin. Liquid chromatography/mass spectrometry (LC/MS) analysis of co-immunoprecipitated complexes (Co-IP) led to the identification of novel protein partners interacting with endogenous gelsolin. The specificity of these partners was further confirmed by Western blotting (WB), proximity binding assay (PLA) and colocalization microscopic analyses. We believe that our data may have interesting implications for human melanoma biology and may initiate further research into the role of gelsolin in cancer cells.

section excerpts

Antibodies and dyes

Rabbit anti-emerin (FL-254), mouse anti-GAPDH (H-12), goat anti-gelsolin (C-20), mouse anti-hnRPU U (3G6), rabbit anti-laminin-R (H-141) , goat anti-Laminin-R (F-18), mouse anti-nestin (10c2), rabbit anti-Arp3 (H-110), goat anti-HA (Y-11) and normal goat IgG were obtained from Santa Cruz Biotechnology®Inc. (Heidelberg, Germany). Mouse anti-β-actin (AC-15), mouse anti-γ-actin (2-, mouse anti-all isoactin (AC40), rabbit anti-all isoactin (C-11), mouse anti-β- tubulin (TUB 2.1) and

Identification of gelsolin in melanoma cell nuclei

We first compared the quality of goat polyclonal and mouse anti-gelsolin monoclonal antibodies by Western blotting (WB) and confocal microscopy, as goat IgG was used for immunoprecipitation and immunostaining experiments, and mouse antibodies were used for Co-IP Western blotting and immunostaining. Evaluation of the results showed that both types of antibodies were specific for gelsolin and recognized a single band of 82 kDa (Supplementary Fig. 1A, B). We also observed


To identify novel molecular partners of gelsolin, we co-immunoprecipitated endogenous gelsolin from whole cell lysates (WCL) and nuclear fractions (NF) of melanoma cells using a modified immunoprecipitation protocol. The identification of actin, SERBP1 (SERPINE1 mRNA-binding protein) (Supplementary Table 3) and drabrin (Supplementary Table 5) as gelsolin interaction partners in the LC/MS analysis of coimmunoprecipitates provided a proof of principle for our approach, as there was a seance

Conflict of interest

The authors declare no competing financial interest.


AJM, TR and AM thank youFoundation for Polish Sciencefor financial support under the HOMING Plus Program (HOMING Plus/2010-2/8) under the Innovative Economy Program of the European Union. Special thanks go to Ilona Styczeń for her important administrative contribution to this work. The costs of publication were financed from the program of the Wrocław Center for Biotechnology "National Center for Leading Research (KNOW)" for the years 2014-2018.


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