Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers
Adhesion between cells and the extracellular matrix (ECM) is one of the prerequisites for multicellularity, motility, and tissue specialization. Focal adhesions (FAs) are defined as protein complexes that mediate signals from the ECM to major components of the cytoskeleton (microtubules, actin, and...
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MDPI AG
2022-05-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/23/10/5594 |
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| author | Tina Paradžik Iva I. Podgorski Tanja Vojvoda Zeljko Mladen Paradžik |
| author_facet | Tina Paradžik Iva I. Podgorski Tanja Vojvoda Zeljko Mladen Paradžik |
| author_sort | Tina Paradžik |
| collection | DOAJ |
| description | Adhesion between cells and the extracellular matrix (ECM) is one of the prerequisites for multicellularity, motility, and tissue specialization. Focal adhesions (FAs) are defined as protein complexes that mediate signals from the ECM to major components of the cytoskeleton (microtubules, actin, and intermediate filaments), and their mutual communication determines a variety of cellular processes. In this study, human cytoskeletal crosstalk proteins were identified by comparing datasets with experimentally determined cytoskeletal proteins. The spectraplakin dystonin was the only protein found in all datasets. Other proteins (FAK, RAC1, septin 9, MISP, and ezrin) were detected at the intersections of FAs, microtubules, and actin cytoskeleton. Homology searches for human crosstalk proteins as queries were performed against a predefined dataset of proteomes. This analysis highlighted the importance of FA communication with the actin and microtubule cytoskeleton, as these crosstalk proteins exhibit the highest degree of evolutionary conservation. Finally, phylogenetic analyses elucidated the early evolutionary history of spectraplakins and cortical microtubule stabilization complexes (CMSCs) as model representatives of the human cytoskeletal crosstalk. While spectraplakins probably arose at the onset of opisthokont evolution, the crosstalk between FAs and microtubules is associated with the emergence of metazoans. The multiprotein complexes contributing to cytoskeletal crosstalk in animals gradually gained in complexity from the onset of metazoan evolution. |
| first_indexed | 2024-03-10T03:43:46Z |
| format | Article |
| id | doaj.art-bc4d5d33713c4a6bb5e85349d9e8c1fb |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-10T03:43:46Z |
| publishDate | 2022-05-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-bc4d5d33713c4a6bb5e85349d9e8c1fb2023-11-23T11:25:15ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-05-012310559410.3390/ijms23105594Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as CrosslinkersTina Paradžik0Iva I. Podgorski1Tanja Vojvoda Zeljko2Mladen Paradžik3Laboratory for Biotechnology in Aquaculture, Division of Materials Chemistry, Ruđer Bošković Institute, 10000 Zagreb, CroatiaLaboratory for Metabolism and Aging, Division of Molecular Medicine, Ruđer Bošković Institute, 10000 Zagreb, CroatiaLaboratory for Precipitation Processes, Division of Materials Chemistry, Ruđer Bošković Institute, 10000 Zagreb, CroatiaLaboratory of Experimental Therapy, Division of Molecular Medicine, Ruđer Bošković Institute, 10000 Zagreb, CroatiaAdhesion between cells and the extracellular matrix (ECM) is one of the prerequisites for multicellularity, motility, and tissue specialization. Focal adhesions (FAs) are defined as protein complexes that mediate signals from the ECM to major components of the cytoskeleton (microtubules, actin, and intermediate filaments), and their mutual communication determines a variety of cellular processes. In this study, human cytoskeletal crosstalk proteins were identified by comparing datasets with experimentally determined cytoskeletal proteins. The spectraplakin dystonin was the only protein found in all datasets. Other proteins (FAK, RAC1, septin 9, MISP, and ezrin) were detected at the intersections of FAs, microtubules, and actin cytoskeleton. Homology searches for human crosstalk proteins as queries were performed against a predefined dataset of proteomes. This analysis highlighted the importance of FA communication with the actin and microtubule cytoskeleton, as these crosstalk proteins exhibit the highest degree of evolutionary conservation. Finally, phylogenetic analyses elucidated the early evolutionary history of spectraplakins and cortical microtubule stabilization complexes (CMSCs) as model representatives of the human cytoskeletal crosstalk. While spectraplakins probably arose at the onset of opisthokont evolution, the crosstalk between FAs and microtubules is associated with the emergence of metazoans. The multiprotein complexes contributing to cytoskeletal crosstalk in animals gradually gained in complexity from the onset of metazoan evolution.https://www.mdpi.com/1422-0067/23/10/5594cytoskeletal crosstalkspectraplakincortical microtubule stabilization complexfocal adhesionactinmicrotubule |
| spellingShingle | Tina Paradžik Iva I. Podgorski Tanja Vojvoda Zeljko Mladen Paradžik Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers International Journal of Molecular Sciences cytoskeletal crosstalk spectraplakin cortical microtubule stabilization complex focal adhesion actin microtubule |
| title | Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers |
| title_full | Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers |
| title_fullStr | Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers |
| title_full_unstemmed | Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers |
| title_short | Ancient Origins of Cytoskeletal Crosstalk: Spectraplakin-like Proteins Precede the Emergence of Cortical Microtubule Stabilization Complexes as Crosslinkers |
| title_sort | ancient origins of cytoskeletal crosstalk spectraplakin like proteins precede the emergence of cortical microtubule stabilization complexes as crosslinkers |
| topic | cytoskeletal crosstalk spectraplakin cortical microtubule stabilization complex focal adhesion actin microtubule |
| url | https://www.mdpi.com/1422-0067/23/10/5594 |
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