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An evolutionary perspective on the relationship between kinetochore size and CENP-E dependence for chromosome alignment

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Title: An evolutionary perspective on the relationship between kinetochore size and CENP-E dependence for chromosome alignment
Authors: Ana C. Almeida, Helder Rocha, Maximilian W. D. Raas, Hanh Witte, Ralf J. Sommer, Berend Snel, Geert J. P. L. Kops, Reto Gassmann, Helder Maiato
Contributors: Hubrecht Institute with UMC
Source: J Cell Sci
Publisher Information: The Company of Biologists, 2024.
Publication Year: 2024
Subject Terms: 0301 basic medicine, Evolution, Chromosomal Proteins, Non-Histone, Centromere, Short Report, Mitosis, Chromosome, Chromosomes, Evolution, Molecular, 03 medical and health sciences, Chromosome Segregation, Animals, Humans, Holocentric, Kinetochores, Caenorhabditis elegans, Phylogeny, Caenorhabditis elegans/metabolism, 0303 health sciences, Molecular, Cell Biology, Kinesin, Biological Evolution, Chromosomal Proteins, Kinetochore, Kinetochores/metabolism, Chromosomes/metabolism, Non-Histone/metabolism, Centromere/metabolism, CENP-E
Description: Chromosome alignment during mitosis can occur as a consequence of bi-orientation or is assisted by the CENP-E (kinesin-7) motor at kinetochores. We previously found that Indian muntjac chromosomes with larger kinetochores bi-orient more efficiently and are biased to align in a CENP-E-independent manner, suggesting that CENP-E dependence for chromosome alignment negatively correlates with kinetochore size. Here, we used targeted phylogenetic profiling of CENP-E in monocentric (localized centromeres) and holocentric (centromeres spanning the entire chromosome length) clades to test this hypothesis at an evolutionary scale. We found that, despite being present in common ancestors, CENP-E was lost more frequently in taxa with holocentric chromosomes, such as Hemiptera and Nematoda. Functional experiments in two nematodes with holocentric chromosomes in which a CENP-E ortholog is absent (Caenorhabditis elegans) or present (Pristionchus pacificus) revealed that targeted expression of human CENP-E to C. elegans kinetochores partially rescued chromosome alignment defects associated with attenuated polar-ejection forces, whereas CENP-E inactivation in P. pacificus had no detrimental effects on mitosis and viability. These data showcase the dispensability of CENP-E for mitotic chromosome alignment in species with larger kinetochores.
Document Type: Article
Other literature type
File Description: application/pdf
Language: English
ISSN: 1477-9137
0021-9533
DOI: 10.1242/jcs.263466
Access URL: https://pubmed.ncbi.nlm.nih.gov/39698944
https://pure.knaw.nl/portal/en/publications/48cdc60b-b220-4538-a415-dc117e5557bc
https://hdl.handle.net/20.500.11755/48cdc60b-b220-4538-a415-dc117e5557bc
https://doi.org/10.1242/jcs.263466
https://dspace.library.uu.nl/handle/1874/459910
Rights: CC BY
URL: http://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0 (http://creativecommons.org/licenses/by/4.0/) ), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
Accession Number: edsair.doi.dedup.....a4c61d43939beaa90e7c0cfcc47a7c90
Database: OpenAIRE
Description
Abstract:Chromosome alignment during mitosis can occur as a consequence of bi-orientation or is assisted by the CENP-E (kinesin-7) motor at kinetochores. We previously found that Indian muntjac chromosomes with larger kinetochores bi-orient more efficiently and are biased to align in a CENP-E-independent manner, suggesting that CENP-E dependence for chromosome alignment negatively correlates with kinetochore size. Here, we used targeted phylogenetic profiling of CENP-E in monocentric (localized centromeres) and holocentric (centromeres spanning the entire chromosome length) clades to test this hypothesis at an evolutionary scale. We found that, despite being present in common ancestors, CENP-E was lost more frequently in taxa with holocentric chromosomes, such as Hemiptera and Nematoda. Functional experiments in two nematodes with holocentric chromosomes in which a CENP-E ortholog is absent (Caenorhabditis elegans) or present (Pristionchus pacificus) revealed that targeted expression of human CENP-E to C. elegans kinetochores partially rescued chromosome alignment defects associated with attenuated polar-ejection forces, whereas CENP-E inactivation in P. pacificus had no detrimental effects on mitosis and viability. These data showcase the dispensability of CENP-E for mitotic chromosome alignment in species with larger kinetochores.
ISSN:14779137
00219533
DOI:10.1242/jcs.263466