Identification of a Novel Chromosomal Passenger Complex and Its Unique Localization during Cytokinesis in Trypanosoma brucei

Li, Ziyin; Lee, Ju Huck; Chu, Feixia; Burlingame, Alma L.; Günzl, Arthur; Wang, Ching C.

doi:10.1371/journal.pone.0002354

Cited by 94 publications

(211 citation statements)

References 53 publications

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“…3 A and B) for the latter to initiate cytokinesis from the anterior tip of the new FAZ filament. Moreover, our results also uncovered the mechanism underlying the recruitment of TbAUK1 to the new FAZ tip at late anaphase, which has been a mystery since we first discovered that TbAUK1 emerges at the new FAZ tip at late anaphase (12). It should be noted that CIF1 also localizes to the cleavage furrow during cytokinesis (Fig.…”

Section: Discussionsupporting

confidence: 56%

“…Selection of transfectants, cloning, and RNAi induction were carried out as described previously (14). TbPLK RNAi cell line and TbAUK1 RNAi cell line have been reported previously (12,17).…”

Section: Methodsmentioning

confidence: 99%

“…The complex is located in kinetochores from S phase to metaphase and on the central spindle during anaphase, but finally is degraded at the central spindle after late anaphase. However, starting from late anaphase, newly synthesized CPC proteins emerge at the new FAZ tip and then transfer to the cleavage furrow during cytokinesis (12). Localization of TbAUK1 to the new FAZ tip at late anaphase is crucial for cytokinesis initiation (13), but how it is recruited remains mysterious.…”

Section: Trypanosoma Bruceimentioning

confidence: 99%

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Two distinct cytokinesis pathways drive trypanosome cell division initiation from opposite cell ends

Zhou¹,

Zhao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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160

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Cytokinesis in Trypanosoma brucei, an early branching protozoan, occurs along its longitudinal axis uni-directionally from the anterior tip of the new flagellum attachment zone filament toward the cell's posterior end. However, the underlying mechanisms remain elusive. Here we report that cytokinesis in T. brucei is regulated by a concerted action of Polo-like kinase, Aurora B kinase, and a trypanosome-specific protein CIF1. Phosphorylation of CIF1 by Polo-like kinase targets it to the anterior tip of the new flagellum attachment zone filament, where it subsequently recruits Aurora B kinase to initiate cytokinesis. Consistent with its role, CIF1 depletion inhibits cytokinesis initiation from the anterior end of the cell, but, surprisingly, triggers cytokinesis initiation from the posterior end of the cell, suggesting the activation of an alternative cytokinesis from the opposite cell end. Our results reveal the mechanistic roles of CIF1 and Polo-like kinase in cytokinesis initiation and elucidate the mechanism underlying the recruitment of Aurora B kinase to the cytokinesis initiation site at late anaphase. These findings also delineate a signaling cascade controlling cytokinesis initiation from the anterior end of the cell and uncover a backup cytokinesis that is initiated from the posterior end of the cell when the typical anterior-to-posterior cytokinesis is compromised.cytokinesis | Polo-like kinase | Aurora B kinase | backup cytokinesis |

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Section: Discussionsupporting

confidence: 56%

Section: Methodsmentioning

confidence: 99%

Section: Trypanosoma Bruceimentioning

confidence: 99%

See 1 more Smart Citation

Two distinct cytokinesis pathways drive trypanosome cell division initiation from opposite cell ends

Zhou¹,

Zhao

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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160

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“…5, D, F, G, I, and J and data not shown), this suggests that there are two distinct TbSAS-4-containing complexes at the FAZ tip. The complex with FAZ12 is present only in G 1 cells, and following cell cycle progression to S-phase and later cell cycle stages, the complex without FAZ12 emerges at (43,44) and the chromosomal passenger complex (CPC) consisting of the Aurora B kinase TbAUK1 and two trypanosome-specific chromosomal passengers TbCPC1 and TbCPC2 (19,20). All of these proteins are concentrated only at the new FAZ tip, and are required for cytokinesis initiation, without any involvement in life cycle transitions.…”

Section: Discussionmentioning

confidence: 99%

SAS-4 Protein in Trypanosoma brucei Controls Life Cycle Transitions by Modulating the Length of the Flagellum Attachment Zone Filament

Zhou

2015

Journal of Biological Chemistry

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The centrosome in animals constitutes the cell's microtubule-organizing center that nucleates spindle assembly, and is characterized by a symmetrical array of nine microtubule triplets emanating from a cartwheel structure in the very proximal region of the centriole. Biogenesis of centrioles requires many regulatory proteins, including SAS-6, SAS-4/CPAP, and BLD10/CEP135, which are thought to constitute the core ancestral module involved in centriole assembly (1). The three proteins have distinct functions in centriole biogenesis. SAS-6 assembles to the cartwheel (2, 3) and BLD10/CEP135 forms the pinhead that connects the cartwheel spokes to the A-microtubules of the microtubule triplets (4, 5), whereas SAS-4/CPAP controls the elongation of centriolar microtubules (6 -9).Trypanosoma brucei, a flagellated protozoan and the causative agent of human sleeping sickness, does not have centrosomes, but it possesses the basal body as its microtubule-organizing center to nucleate the assembly of a motile flagellum. The basal body is characterized by an array of nine microtubule triplets, with the conserved SAS-6 protein forming the cartwheel structure (10), similar to that of the centrosome in metazoa. The flagellum is attached, along most of its length, to the cell body via a specialized cytoskeletal structure termed the flagellum attachment zone (FAZ), 2 which consists of three main domains: the structure connecting the paraflagellar rod (PFR) to the flagellar membrane, the structure connecting the flagellar membrane and the cell body membrane, and a cytoplasmic filament (often referred to as the FAZ filament) and its associated microtubule quartet (11)(12)(13)(14)(15)(16)(17). In addition to mediating flagellum-cell body attachment, the FAZ filament also defines the cytokinesis cleavage plane (11,12), with the distal tip of the new FAZ filament marking the site of cytokinesis initiation (18 -20). Moreover, during the cell cycle in the procyclic form, the elongation of the FAZ filament positions the newly assembled basal body toward the cell posterior (21), which is crucial for organelle segregation and cell division (10,(22)(23)(24)(25).Trypanosomatids, a group of kinetoplastid parasites consisting of T. brucei, Trypanosoma cruzi, and Leishmania spp., appear in a variety of different morphological forms during their life cycle and are distinguished by the relative position of the kinetoplast (mitochondrial DNA) and the nucleus and by the position, length, and cell body attachment of the flagellum (26). In the tsetse fly vector, T. brucei differentiates from the trypomastigote form to the epimastigote form, which undergoes asymmetrical cell division to produce a long epimastigote cell and a short epimastigote cell (26). How life cycle transitions in T. brucei are regulated is largely unknown, but recent work has begun to uncover the regulators involved in this process. ALBA3 and ALBA4, two closed related RNA-binding proteins, are the first factors found to be involved in life cycle transitions in T. brucei (27). Anothe...

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“…However, the absence of these mitotic kinesins could be compensated by trypanosome-specific kinesins and orphan kinesins. Previously, we identified two orphan kinesins, TbKIN-A and TbKIN-B, that are essential for spindle assembly in trypanosomes (Li et al, 2008b). Inspired by the discovery of TbKIN-A and TbKIN-B as essential mitotic kinesins, we further explored the potential roles of other orphan kinesins in cellular morphogenesis, cell proliferation and cell cycle regulation in trypanosomes.…”

Section: Introductionmentioning

confidence: 99%

An orphan kinesin in trypanosomes cooperates with a kinetoplastid-specific kinesin to maintain cell morphology through regulating subpellicular microtubules

Hu¹,

Hu²,

Yu³

et al. 2012

Journal of Cell Science

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SummaryMicrotubules are a vital part of the cytoskeleton of eukaryotic cells and are involved in various cellular processes. The cytoskeleton of Trypanosoma brucei is characterized by an array of subpellicular microtubules and is essential for maintenance of cell shape and polarity, but little is known about the regulation of the assembly and organization of the subpellicular microtubule corset. Here, we report that the orphan kinesin TbKIN-D regulates the organization of subpellicular microtubules and is required for maintaining cell morphology. TbKIN-D possesses in vitro ATPase activity, associates with cytoskeletal microtubules and is distributed throughout the cytoskeleton at all cell cycle stages. RNAi of TbKIN-D disrupts the organization of the subpellicular microtubule corset and distorts cell morphology, resulting in round cells with an elongated posterior filled with newly assembled microtubules. Depletion of TbKIN-D also abolishes the segregation of organelles and cytoskeletal structures, suggesting that cellular morphogenesis is essential for proper organelle segregation. Moreover, TbKIN-D deficiency impairs the attachment of the new flagellum without compromising the formation of the flagellum attachment zone. Finally, we identified TbKIN-C, a kinetoplastid-specific kinesin known to regulate subpellicular microtubules and cell morphogenesis in T. brucei, as a partner of TbKIN-D. Further, we demonstrate that interaction between TbKIN-C and TbKIN-D requires the coiled-coil motifs in the C-termini of both proteins. Altogether, our results suggest that TbKIN-D cooperates with TbKIN-C to maintain cell morphology by regulating the organization of the subpellicular microtubule corset.

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Identification of a Novel Chromosomal Passenger Complex and Its Unique Localization during Cytokinesis in Trypanosoma brucei

Cited by 94 publications

References 53 publications

Two distinct cytokinesis pathways drive trypanosome cell division initiation from opposite cell ends

Two distinct cytokinesis pathways drive trypanosome cell division initiation from opposite cell ends

SAS-4 Protein in Trypanosoma brucei Controls Life Cycle Transitions by Modulating the Length of the Flagellum Attachment Zone Filament

An orphan kinesin in trypanosomes cooperates with a kinetoplastid-specific kinesin to maintain cell morphology through regulating subpellicular microtubules

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