Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturation
Summary: The BRCA1-interacting protein Obg-like ATPase 1 (OLA1) functions in centriole duplication. In this study, we show the role of the mitotic kinase Aurora A in the reduction of centrosomal OLA1. Aurora A binds to and polyubiquitinates OLA1, targeting it for proteasomal degradation. NIMA-relate...
Main Authors: | , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Elsevier
2023-08-01
|
Series: | Cell Reports |
Subjects: | |
Online Access: | http://www.sciencedirect.com/science/article/pii/S2211124723008616 |
_version_ | 1797731113953656832 |
---|---|
author | Zhenzhou Fang Xingming Li Yuki Yoshino Moe Suzuki Huicheng Qi Hinari Murooka Riko Katakai Matsuyuki Shirota Thi Anh Mai Pham Ayako Matsuzawa Kei Otsuka Chikashi Ishioka Takahiro Mori Natsuko Chiba |
author_facet | Zhenzhou Fang Xingming Li Yuki Yoshino Moe Suzuki Huicheng Qi Hinari Murooka Riko Katakai Matsuyuki Shirota Thi Anh Mai Pham Ayako Matsuzawa Kei Otsuka Chikashi Ishioka Takahiro Mori Natsuko Chiba |
author_sort | Zhenzhou Fang |
collection | DOAJ |
description | Summary: The BRCA1-interacting protein Obg-like ATPase 1 (OLA1) functions in centriole duplication. In this study, we show the role of the mitotic kinase Aurora A in the reduction of centrosomal OLA1. Aurora A binds to and polyubiquitinates OLA1, targeting it for proteasomal degradation. NIMA-related kinase 2 (NEK2) phosphorylates the T124 residue of OLA1, increases binding of OLA1 to Aurora A and OLA1 polyubiquitination by Aurora A, and reduces centrosomal OLA1 in G2 phase. The kinase activity of Aurora A suppresses OLA1 polyubiquitination. The decrease in centrosomal OLA1 caused by Aurora A-mediated polyubiquitination promotes the recruitment of pericentriolar material proteins in G2 phase. The E3 ligase activity of Aurora A is critical for centrosome amplification induced by its overexpression. The results suggest a dual function of Aurora A as an E3 ubiquitin ligase and a kinase in the regulation of centrosomal OLA1, which is essential for proper centrosome maturation in G2 phase. |
first_indexed | 2024-03-12T11:54:04Z |
format | Article |
id | doaj.art-caf9765e3f364d1f80eb33fd713745a2 |
institution | Directory Open Access Journal |
issn | 2211-1247 |
language | English |
last_indexed | 2024-03-12T11:54:04Z |
publishDate | 2023-08-01 |
publisher | Elsevier |
record_format | Article |
series | Cell Reports |
spelling | doaj.art-caf9765e3f364d1f80eb33fd713745a22023-08-31T05:01:52ZengElsevierCell Reports2211-12472023-08-01428112850Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturationZhenzhou Fang0Xingming Li1Yuki Yoshino2Moe Suzuki3Huicheng Qi4Hinari Murooka5Riko Katakai6Matsuyuki Shirota7Thi Anh Mai Pham8Ayako Matsuzawa9Kei Otsuka10Chikashi Ishioka11Takahiro Mori12Natsuko Chiba13Department of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Department of Cancer Biology, Tohoku University Graduate School of Medicine, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Department of Cancer Biology, Tohoku University Graduate School of Medicine, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Department of Cancer Biology, Tohoku University Graduate School of Medicine, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDivision of Interdisciplinary Medical Science, Tohoku University Graduate School of Medicine, 2-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Molecular Immunology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Clinical Oncology, Tohoku University Graduate School of Medicine, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, JapanDepartment of Clinical Oncology, Tohoku University Graduate School of Medicine, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Departemt of Medical Oncology and Hematology, Okinawa Chubu Hospital, 281 Miyazato, Uruma, Okinawa 904-2293, Japan; Genome Medical Science Project, National Center for Global Health and Medicine, 1-21-1 Toyama, Shinjuku, Tokyo 162-8655, JapanDepartment of Cancer Biology, Institute of Development, Aging and Cancer (IDAC), Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Department of Cancer Biology, Tohoku University Graduate School of Medicine, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Laboratory of Cancer Biology, Graduate School of Life Sciences, Tohoku University, 4-1 Seiryomachi Aoba-ku, Sendai 980-8575, Japan; Corresponding authorSummary: The BRCA1-interacting protein Obg-like ATPase 1 (OLA1) functions in centriole duplication. In this study, we show the role of the mitotic kinase Aurora A in the reduction of centrosomal OLA1. Aurora A binds to and polyubiquitinates OLA1, targeting it for proteasomal degradation. NIMA-related kinase 2 (NEK2) phosphorylates the T124 residue of OLA1, increases binding of OLA1 to Aurora A and OLA1 polyubiquitination by Aurora A, and reduces centrosomal OLA1 in G2 phase. The kinase activity of Aurora A suppresses OLA1 polyubiquitination. The decrease in centrosomal OLA1 caused by Aurora A-mediated polyubiquitination promotes the recruitment of pericentriolar material proteins in G2 phase. The E3 ligase activity of Aurora A is critical for centrosome amplification induced by its overexpression. The results suggest a dual function of Aurora A as an E3 ubiquitin ligase and a kinase in the regulation of centrosomal OLA1, which is essential for proper centrosome maturation in G2 phase.http://www.sciencedirect.com/science/article/pii/S2211124723008616CP: Molecular biology |
spellingShingle | Zhenzhou Fang Xingming Li Yuki Yoshino Moe Suzuki Huicheng Qi Hinari Murooka Riko Katakai Matsuyuki Shirota Thi Anh Mai Pham Ayako Matsuzawa Kei Otsuka Chikashi Ishioka Takahiro Mori Natsuko Chiba Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturation Cell Reports CP: Molecular biology |
title | Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturation |
title_full | Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturation |
title_fullStr | Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturation |
title_full_unstemmed | Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturation |
title_short | Aurora A polyubiquitinates the BRCA1-interacting protein OLA1 to promote centrosome maturation |
title_sort | aurora a polyubiquitinates the brca1 interacting protein ola1 to promote centrosome maturation |
topic | CP: Molecular biology |
url | http://www.sciencedirect.com/science/article/pii/S2211124723008616 |
work_keys_str_mv | AT zhenzhoufang auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT xingmingli auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT yukiyoshino auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT moesuzuki auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT huichengqi auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT hinarimurooka auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT rikokatakai auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT matsuyukishirota auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT thianhmaipham auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT ayakomatsuzawa auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT keiotsuka auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT chikashiishioka auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT takahiromori auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration AT natsukochiba auroraapolyubiquitinatesthebrca1interactingproteinola1topromotecentrosomematuration |