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PreprintCited by 13Microtubule and mitosis dynamicsTrypanosoma species research and implicationsGenomics and Chromatin Dynamics

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Kinetoplastid kinetochore proteins KKT14-KKT15 are divergent Bub1/BubR1-Bub3 proteins

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Ballmer, Daniel, Carter, William, van Hooff, Jolien J. E., Tromer, Eelco C., Ishii, Midori, Ludzia, Patryk, Akiyoshi, Bungo·2024·Open Biology
DOI 10.1101/2024.01.04.574194PMC PMC11286163

Preprint — published as 10.1098/rsob.240025 · Paper page

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Abstract

Faithful transmission of genetic material is crucial for the survival of all organisms. In many eukaryotes, a feedback control mechanism called the spindle checkpoint ensures chromosome segregation fidelity by delaying cell cycle progression until all chromosomes achieve proper attachment to the mitotic spindle. Kinetochores are the macromolecular complexes that act as the interface between chromosomes and spindle microtubules. While most eukaryotes have canonical kinetochore proteins that are widely conserved, kinetoplastids such as Trypanosoma brucei have a seemingly unique set of kinetochore proteins including KKT1–25. Available evidence suggests that T. brucei lacks components of the spindle checkpoint and is unable to delay cell cycle progression in response to spindle defects. It therefore remains poorly understood how kinetoplastids regulate cell cycle progression or ensure chromosome segregation fidelity. Here, we report a crystal structure of the C-terminal domain of KKT14 from Apiculatamorpha spiralis and uncover that it is a pseudokinase. Its structure is most similar to the kinase domain of Bub1, a key component of the spindle checkpoint in other eukaryotes. In addition, KKT14 in T. brucei and other trypanosomatids has a putative ABBA motif that is present in Bub1 and its paralog BubR1. We also find that the N-terminal part of KKT14 interacts with KKT15, whose WD40 repeat beta-propeller is phylogenetically closely related to a direct interactor of Bub1/BubR1 called Bub3. Our findings indicate that KKT14-KKT15 are divergent orthologs of Bub1/BubR1-Bub3, which promote accurate chromosome segregation in trypanosomes.

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Metadata

Authors
Ballmer, D., Carter, W., van Hooff, J. J. E., Tromer, E. C., Ishii, M., Ludzia, P., & Akiyoshi, B.
Affiliations
  • University of Oxford (GB)
  • Wageningen University & Research (NL)
  • University of Groningen (NL)
Corresponding author
Akiyoshi, Bungo
ORCID
Venue
Open Biology
Publisher
openRxiv
Published
2024-01-05
Volume
14
Issue
6
Pages
240025-240025
ISSN
2046-2441 (ISSN-L)
DOI
10.1101/2024.01.04.574194
PMC
PMC11286163
OpenAlex
W4399518174
Cited by
13
References
1
Citations by year
2026: 3 · 2025: 4 · 2024: 6
FWCI
2.91
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Open Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (acceptedVersion)
  • Socio-Environmental Systems Modeling (submittedVersion, cc-by)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
  • University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, cc-by)
Funders
  • Wellcome Trust (227243/Z/23/Z, 210622/A/18/Z, 210622, 203149, 210622/Z/18/Z)
  • University of Warwick
  • Boehringer Ingelheim Fonds
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (Veni.202.223, 202.223, VI.Veni.202.223, VI.Veni.212.099)
  • Wellcome / EPSRC Centre for Interventional and Surgical Sciences
  • Warwick Medical School
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Health Sciences › Medicine › Epidemiology › Trypanosoma species research and implications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Keywords
kinetochore proteins, BUB1, BubR1, Bub3, spindle assembly checkpoint, chromosome segregation, kinetoplastids, Trypanosoma brucei, pseudokinase, crystal structure, protein evolution, cell cycle regulation
MeSH terms
Amino Acid Sequence, Models, Molecular, Phylogeny, Protein Binding, Trypanosoma brucei brucei, Protozoan Proteins, Protein Serine-Threonine Kinases, Crystallography, X-Ray, Kinetochores, Cell Cycle Proteins, Chromosome Segregation

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