CYLD regulates spindle orientation by stabilizing astral microtubules and promoting dishevelled-NuMA-dynein/dynactin complex formation

Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic spindle. The molecular mechanisms underlying the regulation of spindle orientation remain largely unknown. Herein, we identify a critical role...

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Published in	Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 6; pp. 2158 - 2163
Main Authors	Yang, Yunfan, Liu, Min, Li, Dengwen, Ran, Jie, Gao, Jinmin, Suo, Shaojun, Sun, Shao-Cong, Zhou, Jun
Format	Journal Article
Language	English
Published	United States National Academy of Sciences 11.02.2014 National Acad Sciences
Subjects	Animals Antibodies Antigens, Nuclear - metabolism Biological Sciences Caco 2 cells Cell division Cellular immunity Deubiquitinating Enzyme CYLD Dynactin Complex dynein ATPase Dyneins - metabolism Epithelial cells Gender equity Gene expression HeLa Cells homeostasis Humans Mice Mice, Knockout Microscopy, Fluorescence Microtubule-Associated Proteins - metabolism Microtubules Microtubules - metabolism mitosis Mitotic spindle apparatus Nuclear Matrix-Associated Proteins - metabolism Proteins Small interfering RNA Spindle Apparatus - physiology Tissues Tumor Suppressor Proteins - physiology Tumors 3D cell culture cell cycle cell cortex knockout mouse ubiquitin
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Abstract	Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic spindle. The molecular mechanisms underlying the regulation of spindle orientation remain largely unknown. Herein, we identify a critical role for cylindromatosis (CYLD), a deubiquitinase and regulator of microtubule dynamics, in the control of spindle orientation. CYLD is highly expressed in mitosis and promotes spindle orientation by stabilizing astral microtubules and deubiquitinating the cortical polarity protein dishevelled. The deubiquitination of dishevelled enhances its interaction with nuclear mitotic apparatus, stimulating the cortical localization of nuclear mitotic apparatus and the dynein/dynactin motor complex, a requirement for generating pulling forces on astral microtubules. These findings uncover CYLD as an important player in the orientation of the mitotic spindle and cell division and have important implications in health and disease.
AbstractList	Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic spindle. The molecular mechanisms underlying the regulation of spindle orientation remain largely unknown. Herein, we identify a critical role for cylindromatosis (CYLD), a deubiquitinase and regulator of microtubule dynamics, in the control of spindle orientation. CYLD is highly expressed in mitosis and promotes spindle orientation by stabilizing astral microtubules and deubiquitinating the cortical polarity protein dishevelled. The deubiquitination of dishevelled enhances its interaction with nuclear mitotic apparatus, stimulating the cortical localization of nuclear mitotic apparatus and the dynein/dynactin motor complex, a requirement for generating pulling forces on astral microtubules. These findings uncover CYLD as an important player in the orientation of the mitotic spindle and cell division and have important implications in health and disease.Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic spindle. The molecular mechanisms underlying the regulation of spindle orientation remain largely unknown. Herein, we identify a critical role for cylindromatosis (CYLD), a deubiquitinase and regulator of microtubule dynamics, in the control of spindle orientation. CYLD is highly expressed in mitosis and promotes spindle orientation by stabilizing astral microtubules and deubiquitinating the cortical polarity protein dishevelled. The deubiquitination of dishevelled enhances its interaction with nuclear mitotic apparatus, stimulating the cortical localization of nuclear mitotic apparatus and the dynein/dynactin motor complex, a requirement for generating pulling forces on astral microtubules. These findings uncover CYLD as an important player in the orientation of the mitotic spindle and cell division and have important implications in health and disease. Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic spindle. The molecular mechanisms underlying the regulation of spindle orientation remain largely unknown. Herein, we identify a critical role for cylindromatosis (CYLD), a deubiquitinase and regulator of microtubule dynamics, in the control of spindle orientation. CYLD is highly expressed in mitosis and promotes spindle orientation by stabilizing astral microtubules and deubiquitinating the cortical polarity protein dishevelled. The deubiquitination of dishevelled enhances its interaction with nuclear mitotic apparatus, stimulating the cortical localization of nuclear mitotic apparatus and the dynein/dynactin motor complex, a requirement for generating pulling forces on astral microtubules. These findings uncover CYLD as an important player in the orientation of the mitotic spindle and cell division and have important implications in health and disease. Orientation of the mitotic spindle relative to the cell cortex is known to control the orientation of the cell division plane, thereby contributing to cell fate specification and tissue organization. The molecular mechanisms of how spindle orientation is regulated during mitosis remain poorly defined. In this paper, we demonstrate that cylindromatosis (CYLD) regulates spindle orientation via its dual functions as a microtubule-associated protein and deubiquitinase. CYLD stabilizes astral microtubules, hence ensuring microtubule extension to the cell cortex and interaction with cortical sites. The deubiquitinase activity of CYLD, however, catalyzes the removal of the polyubiquitin chain from dishevelled and thereby promotes the dishevelled-NuMA-dynein/dynactin complex formation at the cell cortex, a requirement for generating pulling forces on astral microtubules. Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic spindle. The molecular mechanisms underlying the regulation of spindle orientation remain largely unknown. Herein, we identify a critical role for cylindromatosis (CYLD), a deubiquitinase and regulator of microtubule dynamics, in the control of spindle orientation. CYLD is highly expressed in mitosis and promotes spindle orientation by stabilizing astral microtubules and deubiquitinating the cortical polarity protein dishevelled. The deubiquitination of dishevelled enhances its interaction with nuclear mitotic apparatus, stimulating the cortical localization of nuclear mitotic apparatus and the dynein/dynactin motor complex, a requirement for generating pulling forces on astral microtubules. These findings uncover CYLD as an important player in the orientation of the mitotic spindle and cell division and have important implications in health and disease. Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic spindle. The molecular mechanisms underlying the regulation of spindle orientation remain largely unknown. Herein, we identify a critical role for cylindromatosis (CYLD), a deubiquitinase and regulator of microtubule dynamics, in the control of spindle orientation. CYLD is highly expressed in mitosis and promotes spindle orientation by stabilizing astral microtubules and deubiquitinating the cortical polarity protein dishevelled. The deubiquitination of dishevelled enhances its interaction with nuclear mitotic apparatus, stimulating the cortical localization of nuclear mitotic apparatus and the dynein/dynactin motor complex, a requirement for generating pulling forces on astral microtubules. These findings uncover CYLD as an important player in the orientation of the mitotic spindle and cell division and have important implications in health and disease. [PUBLICATION ABSTRACT]
Author	Zhou, Jun Yang, Yunfan Gao, Jinmin Li, Dengwen Suo, Shaojun Sun, Shao-Cong Liu, Min Ran, Jie
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Notes	http://dx.doi.org/10.1073/pnas.1319341111 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 ObjectType-Article-1 ObjectType-Feature-2 content type line 23 Author contributions: Y.Y. and J.Z. designed research; Y.Y., M.L., D.L., J.R., J.G., and S.S. performed research; S.-C.S. contributed new reagents/analytic tools; Y.Y. analyzed data; and J.Z. wrote the paper. Edited* by Vishva M. Dixit, Genentech, San Francisco, CA, and approved January 3, 2014 (received for review October 12, 2013) 1Y.Y., M.L., and D.L. contributed equally to this work.
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Snippet	Oriented cell division is critical for cell fate specification, tissue organization, and tissue homeostasis, and relies on proper orientation of the mitotic... Orientation of the mitotic spindle relative to the cell cortex is known to control the orientation of the cell division plane, thereby contributing to cell...
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SubjectTerms	Animals Antibodies Antigens, Nuclear - metabolism Biological Sciences Caco 2 cells Cell division Cellular immunity Deubiquitinating Enzyme CYLD Dynactin Complex dynein ATPase Dyneins - metabolism Epithelial cells Gender equity Gene expression HeLa Cells homeostasis Humans Mice Mice, Knockout Microscopy, Fluorescence Microtubule-Associated Proteins - metabolism Microtubules Microtubules - metabolism mitosis Mitotic spindle apparatus Nuclear Matrix-Associated Proteins - metabolism Proteins Small interfering RNA Spindle Apparatus - physiology Tissues Tumor Suppressor Proteins - physiology Tumors
Title	CYLD regulates spindle orientation by stabilizing astral microtubules and promoting dishevelled-NuMA-dynein/dynactin complex formation
URI	https://www.jstor.org/stable/23768833 http://www.pnas.org/content/111/6/2158.abstract https://www.ncbi.nlm.nih.gov/pubmed/24469800 https://www.proquest.com/docview/1499055829 https://www.proquest.com/docview/1499142753 https://www.proquest.com/docview/1803090246 https://pubmed.ncbi.nlm.nih.gov/PMC3926035
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