Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma brucei
Cytokinesis in eukaryotes is regulated by a Polo-like kinase-mediated and Aurora B kinase-mediated signalling pathway that promotes the assembly of the actomyosin contractile ring, a cytokinesis machinery conserved across evolution from yeast to humans. Trypanosoma brucei, an early divergent parasit...
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| Format: | Article |
| Language: | English |
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The Royal Society
2022-10-01
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| Series: | Open Biology |
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| Online Access: | https://royalsocietypublishing.org/doi/10.1098/rsob.220197 |
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| author | Yasuhiro Kurasawa Kyu Joon Lee Huiqing Hu Kieu T. M. Pham Ziyin Li |
| author_facet | Yasuhiro Kurasawa Kyu Joon Lee Huiqing Hu Kieu T. M. Pham Ziyin Li |
| author_sort | Yasuhiro Kurasawa |
| collection | DOAJ |
| description | Cytokinesis in eukaryotes is regulated by a Polo-like kinase-mediated and Aurora B kinase-mediated signalling pathway that promotes the assembly of the actomyosin contractile ring, a cytokinesis machinery conserved across evolution from yeast to humans. Trypanosoma brucei, an early divergent parasitic protozoan, employs an actomyosin-independent mechanism for its unusual cytokinesis that is controlled by a regulatory pathway comprising the Polo-like kinase TbPLK, the Aurora B kinase TbAUK1 and multiple trypanosomatid-specific regulators. However, whether any of these trypanosomatid-specific regulators function as substrates of TbPLK and/or TbAUK1 and how they cooperate with TbPLK and TbAUK1 to promote cytokinesis remain unknown. Here, we demonstrate that TbPLK and TbAUK1 phosphorylate the cytokinesis regulators CIF1 and CIF2 on multiple sites within their intrinsically disordered regions. We further show that TbPLK localization depends on its interaction with CIF1 from S/G2 phases, that TbPLK maintains CIF1 and CIF2 localization from G2 phase until early mitosis, and that TbAUK1 maintains CIF1 and CIF2 localization from late mitosis. Finally, we demonstrate that the cytokinesis regulators CIF4 and FPRC are not substrates of TbPLK and TbAUK1, and that they function upstream of TbPLK and TbAUK1 in the cytokinesis regulatory pathway. Together, these results provide insights into the functional interplay and the order of actions between the two protein kinases and the trypanosomatid-specific cytokinesis regulators in T. brucei. |
| first_indexed | 2024-04-09T17:37:00Z |
| format | Article |
| id | doaj.art-0ad8cbdda1274614887318af16cdeeab |
| institution | Directory Open Access Journal |
| issn | 2046-2441 |
| language | English |
| last_indexed | 2024-04-09T17:37:00Z |
| publishDate | 2022-10-01 |
| publisher | The Royal Society |
| record_format | Article |
| series | Open Biology |
| spelling | doaj.art-0ad8cbdda1274614887318af16cdeeab2023-04-17T10:59:39ZengThe Royal SocietyOpen Biology2046-24412022-10-01121010.1098/rsob.220197Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma bruceiYasuhiro Kurasawa0Kyu Joon Lee1Huiqing Hu2Kieu T. M. Pham3Ziyin Li4Department of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston, Houston, TX 77030, USADepartment of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston, Houston, TX 77030, USADepartment of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston, Houston, TX 77030, USADepartment of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston, Houston, TX 77030, USADepartment of Microbiology and Molecular Genetics, University of Texas Health Science Center at Houston, Houston, TX 77030, USACytokinesis in eukaryotes is regulated by a Polo-like kinase-mediated and Aurora B kinase-mediated signalling pathway that promotes the assembly of the actomyosin contractile ring, a cytokinesis machinery conserved across evolution from yeast to humans. Trypanosoma brucei, an early divergent parasitic protozoan, employs an actomyosin-independent mechanism for its unusual cytokinesis that is controlled by a regulatory pathway comprising the Polo-like kinase TbPLK, the Aurora B kinase TbAUK1 and multiple trypanosomatid-specific regulators. However, whether any of these trypanosomatid-specific regulators function as substrates of TbPLK and/or TbAUK1 and how they cooperate with TbPLK and TbAUK1 to promote cytokinesis remain unknown. Here, we demonstrate that TbPLK and TbAUK1 phosphorylate the cytokinesis regulators CIF1 and CIF2 on multiple sites within their intrinsically disordered regions. We further show that TbPLK localization depends on its interaction with CIF1 from S/G2 phases, that TbPLK maintains CIF1 and CIF2 localization from G2 phase until early mitosis, and that TbAUK1 maintains CIF1 and CIF2 localization from late mitosis. Finally, we demonstrate that the cytokinesis regulators CIF4 and FPRC are not substrates of TbPLK and TbAUK1, and that they function upstream of TbPLK and TbAUK1 in the cytokinesis regulatory pathway. Together, these results provide insights into the functional interplay and the order of actions between the two protein kinases and the trypanosomatid-specific cytokinesis regulators in T. brucei.https://royalsocietypublishing.org/doi/10.1098/rsob.220197Trypanosoma bruceicytokinesisPolo-like kinaseAurora B kinaseCIF1CIF2 |
| spellingShingle | Yasuhiro Kurasawa Kyu Joon Lee Huiqing Hu Kieu T. M. Pham Ziyin Li Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma brucei Open Biology Trypanosoma brucei cytokinesis Polo-like kinase Aurora B kinase CIF1 CIF2 |
| title | Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma brucei |
| title_full | Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma brucei |
| title_fullStr | Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma brucei |
| title_full_unstemmed | Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma brucei |
| title_short | Polo-like kinase and Aurora B kinase phosphorylate and cooperate with the CIF1-CIF2 complex to promote cytokinesis initiation in Trypanosoma brucei |
| title_sort | polo like kinase and aurora b kinase phosphorylate and cooperate with the cif1 cif2 complex to promote cytokinesis initiation in trypanosoma brucei |
| topic | Trypanosoma brucei cytokinesis Polo-like kinase Aurora B kinase CIF1 CIF2 |
| url | https://royalsocietypublishing.org/doi/10.1098/rsob.220197 |
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