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Bechstedt, S.

Publications and source records attributed to Bechstedt, S..

9 recordsLinked to original sources

The microtubule-associated proteins CKAP2 and its paralog CKAP2-Like control ciliogenesis in human cells

Ciliogenesis is an evolutionarily conserved process that leads to the assembly of cilia. This process relies on microtubule-associated proteins (MAPs) to regulate axonemal microtubule dynamics. Misregulation of MAPs often leads to changes in ciliary homeostasis, contributing to numerous ciliopathies. Although CKAP2 and CKAP2-Like are best known for regulating microtubule dynamics during cell division, they are also components of ciliary organelles. Notably, CKAP2 overexpression promotes chromosomal instability and cancer, whereas CKAP2-Like deficiency causes Filippi syndrome, a developmental disorder with clinical features overlapping those of ciliopathies. How both MAPs operate at primary cilia remains poorly understood. Here, we identify both MAPs as axonemal components of motile and primary cilia in human cells. We find that CKAP2-positive cilia are linked to cell cycle progression and that the conserved intrinsically disordered microtubule-binding domain of CKAP2, which is essential for microtubule polymerization and stabilization, is required for its ciliary localization. Unexpectedly, CRISPR-mediated loss of either paralog results in elongated cilia without affecting ciliogenesis, accompanied by increased ciliary enrichment of the remaining paralog and impaired Gli2 accumulation at the ciliary tip. In contrast, simultaneous deletion of both MAPs suppresses ciliogenesis and has minimal effect on the ciliary length as compared to wild-type levels. These findings uncover that CKAP2 and CKAP2-Like are axonemal MAPs that contribute to ciliogenesis, partially compensating for each other in human cells.

cell biology↗

An Aurora Kinase A/TPX2 complex phosphorylates CKAP2 to control mitotic spindle growth

Faithful chromosome segregation requires the precise assembly of the mitotic spindle. Cytoskeleton-associated protein 2 (CKAP2) is a microtubule-associated protein with potent microtubule-polymerizing activity that localizes to spindle microtubules during mitosis. Loss or overexpression of CKAP2 causes chromosomal instability and aneuploidy, yet its regulation remains poorly understood. To identify CKAP2 interactors, we immunoprecipitated endogenous CKAP2 from mitotic RPE1 cells and analysed co-purifying proteins by mass spectrometry. This revealed a specific interaction between CKAP2 and the mitotic kinase Aurora A and its activator TPX2, but not with Aurora B, as previously suggested. We further show that CKAP2 co-localizes with Aurora A-TPX2 complexes throughout mitosis, and Aurora A directly phosphorylates CKAP2 in cells and in vitro. Phosphorylation of CKAP2 By Aurora kinase A decreases its microtubule affinity in cells and in vitro. These findings identify CKAP2 as a direct interactor of TPX2 and a substrate of Aurora kinase A and uncover a regulatory pathway controlling spindle growth and stability during mitosis.

biochemistry↗

Enzymatic Function of an Intrinsically Disordered Protein

Intrinsically disordered proteins (IDPs) challenge the traditional structure-function paradigm by lacking a stable three-dimensional structure 1. While their roles as dynamic effectors, scaffolds, and molecular switches are well-established, it has been widely accepted that enzymatic activity requires a stably folded catalytic center 2. Here, we challenge this dogma by demonstrating that a 284-amino acid intrinsically disordered domain of the cytoskeleton-associated protein 2 (CKAP2) is sufficient to catalyze both microtubule polymerization and depolymerization. CKAP2 promotes tubulin incorporation without high-affinity tubulin binding, suggesting a transition-state-based catalytic mechanism distinct from known microtubule polymerases. These findings establish, for the first time, that an intrinsically disordered domain can function as a bona fide enzyme, expanding our understanding of the functional repertoire of disordered proteins and their roles in cellular processes.

biochemistry↗

The microtubule-binding protein EML3 is required for mammalian embryonic growth and cerebral cortical development; Eml3 null mice are a model of cobblestone brain malformation

The cerebral cortex is a multi-layered structure generated through the migration of neural precursors from their birthplace in the ventricular zone to their destination within the cortical plate. Neuronal migration defects are responsible for many human pathologies collectively called neuronal migration disorders, which include subcortical band heterotopia and cobblestone brain (COB) malformation. One example of a protein involved in a neuronal migration disorder is the echinoderm microtubule-associated protein-like 1 (EML1) protein, one of six members of the mammalian EML family. Absence of EML1 protein results in subcortical band heterotopia in mice and humans. Here, we report that absence of the paralogous protein EML3 leads to delayed embryonic development and small size, and a COB-like phenotype with neuronal ectopias in the dorsal telencephalon. We found that EML3 is expressed in the neuroepithelium and meningeal mesenchyme when those tissues participate in pial basement membrane (PBM) formation. Transmission electron microscopy demonstrated that the extracellular matrix of the PBM is structurally abnormal in Eml3 null mice when the first radially migrating neurons arrive. The reduced structural integrity of the PBM leads to focal over-migration of neurons into the subarachnoid space. These findings strengthen the link between the EML protein family and cortical neuronal migration defects by identifying Eml3 as the first EML family member whose absence leads to over-migration of neuroblasts. Moreover, we report the first COB-like phenotype with PBM structural defects when a single microtubule-associated protein is deleted.

developmental biology↗

Maspin/SerpinB5 is a cytoskeleton-binding protein that regulates epithelial cell shape

Maspin/SerpinB5 is an abundant and pleiotropic protein mostly expressed by epithelia. Initially described as a tumor suppressor, it has been reported as a regulator of cell adhesion, migration, and invasion. How intracellular Maspin orchestrates these processes is poorly understood. In this study, we utilized Affinity purification-Mass spectrometry (AP/MS) alongside in vitro reconstitution assays to establish that Maspin directly interacts with microtubules and microfilaments. Additionally, CRISPR/Cas9-mediated GFP tagging of endogenous Maspin, combined with immunostaining, revealed its localization at the cortical cytoskeleton and the mitotic spindle. Depletion of Maspin by RNAi and CRISPR/Cas9 in three distinct epithelial cell lines disrupts cell-cell adhesion, reorganizes the cytoskeleton and results in upregulation of mesenchymal markers during interphase. In mitotic cells, loss of Maspin induces abnormal cell rounding and rearrangement of cortical F-actin. Moreover, Maspin suppresses microtubule growth in vitro and in cells. Collectively, these results demonstrate that Maspin acts at the interface between the cytoskeleton and adhesion sites, directly modulating cell shape and preventing epithelial-mesenchymal transition. SummaryDa Silva et al. report that the non-inhibitory serpin Maspin (SerpinB5), which has long been implicated in the regulation of cell adhesion, migration, invasion and metastasis, directly binds to microfilaments and microtubules in vitro and in cells, acting at the interface between the cytoskeleton and adhesion sites.

cell biology↗

The spindle protein CKAP2 regulates microtubule dynamics and ensures faithful chromosome segregation.

Regulation of microtubule dynamics by microtubule-associated proteins (MAPs) is essential for mitotic spindle assembly and chromosome segregation. Altered microtubule dynamics, particularly increased microtubule growth rates, were found to be a contributing factor for the development of chromosomal instability, which potentiates tumorigenesis. The MAP XMAP215/CKAP5 is the only known microtubule growth factor, and whether other MAPs regulate microtubule growth in cells is unclear. Our recent in vitro reconstitution experiments have demonstrated that Cytoskeleton-Associated Protein 2 (CKAP2) increases microtubule nucleation and growth rates, and here we find that CKAP2 is also an essential microtubule growth factor in cells. By applying CRISPR-Cas9 knock-in and knock-out as well as microtubule plus-end tracking live cell imaging, we show that CKAP2 is a mitotic spindle protein that ensures faithful chromosome segregation by regulating microtubule growth. Live cell imaging of endogenously-labelled CKAP2 showed that it localizes to the spindle during mitosis, and rapidly shifts its localization to the chromatin upon mitotic exit before being degraded. Cells lacking CKAP2 display reduced microtubule growth rates and an increased proportion of chromosome segregation errors and aneuploidy that may be a result of an accumulation of kinetochore-microtubule mis-attachments. Microtubule growth rates and chromosome segregation fidelity can be rescued upon CKAP2 expression in knock-out cells, revealing a direct link between CKAP2 expression and microtubule dynamics. Our results unveil a role of CKAP2 in regulating microtubule growth in cells and provide a mechanistic explanation for the oncogenic potential of CKAP2 misregulation. Significance statementCell division is accomplished by the assembly of a mitotic spindle composed of microtubules that segregate the chromosomes. Cells with altered microtubule dynamics frequently mis-segregate chromosomes and develop aneuploidy, which contributes to cancer development. However, how microtubule dynamics are regulated in cells is not entirely understood. Here, using CRISPR-Cas9 genome editing and live cell imaging, we find that the microtubule-associated protein CKAP2 tightly regulates microtubule growth and ensures the proper segregation of chromosomes. Cells lacking CKAP2 develop errors in chromosome segregation and aneuploidy due to a substantial decline in microtubule growth rates. The essential role of CKAP2 in the regulation of microtubule growth provides an explanation for the oncogenic potential of CKAP2 misregulation. ClassificationBiological Sciences - Cell Biology

cell biology↗

TPPP Forms Liquid Condensates and Aggregates in Multiple System Atrophy

Oligodendrocytes have elaborate arbors of microtubules that extend toward axons and spiral around myelin sheaths. Oligodendrocytes rely on satellite organelles called Golgi outposts to nucleate new microtubules at sites far from the cell body. We now show that the Golgi outpost marker TPPP (tubulin polymerization promoting protein) forms liquid condensates that co-partition with tubulin in order to nucleate microtubules. In oligodendrocytes, TPPP forms either dynamic puncta or aberrant microtubule-associated aggregates. In Multiple System Atrophy (MSA), a sequela of histological events initiates with TPPP aggregation in myelin sheaths and terminates in perinuclear TPPP co-aggregation with alpha-synuclein (aSyn). Finally, recombinant TPPP aggregates are toxic to primary oligodendrocytes. Thus, while the liquid condensate property of TPPP facilitates microtubule nucleation, it also predisposes TPPP to aggregate in disease.

neuroscience↗

The mitotic spindle protein CKAP2 potently increases formation and stability of microtubules

Cells increase microtubule dynamics to make large rearrangements to their microtubule cytoskeleton during cell division. Changes in microtubule dynamics are essential for the formation and function of the mitotic spindle, and misregulation can lead to aneuploidy and cancer. Using in vitro reconstitution assays we show that the mitotic spindle protein Cytoskeleton-Associated Protein 2 (CKAP2) has a strong effect on nucleation of microtubules by lowering the critical tubulin concentration 100-fold. CKAP2 increases the apparent rate constant ka of microtubule growth by 50-fold and increases microtubule growth rates. In addition, CKAP2 strongly suppresses catastrophes. Our results identify CKAP2 as the most potent microtubule growth factor to date. These finding help explain CKAP2s role as an important spindle protein, proliferation marker, and oncogene.

biophysics↗

The inner junction complex of the cilia is an interaction hub that involves tubulin post-translational modifications

Microtubules are cytoskeletal structures involved in structural support, microtubule-based transport and the organization of organelles in the cells. The building blocks of the microtubule, the - and {beta}-tubulin heterodimers, polymerize into protofilaments, that associate laterally to form the hollow microtubule. There exists a specific type of microtubule structures in the cilia, termed doublet microtubules, where high stability is required for ciliary beating and function. The doublet microtubule, consisting of a complete A-tubule and a partial B-tubule maintains its stability through unique interactions at its outer and inner junctions, where the A- and B-tubules meet.\n\nUsing cryo-electron microscopy, we present the answer to the long-standing question regarding the identities, localizations and structures of the Chlamydomonas doublet microtubule inner junction proteins. Using a combination of sequence bioinformatics and mass spectrometry, we identified two new inner junction proteins, FAP276 and FAP106, and an inner junction associated protein FAP126. We show that inner junction proteins PACRG and FAP20, together with FAP52, previously unidentified FAP276, FAP106 and FAP126, form an interaction hub at the inner junction, which involves tubulin sites for post-translational modifications. We further compare the Chlamydomonas and Tetrahymena doublet microtubule structures to understand the common and species-specific features of the inner junction.

biophysics↗