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Title: Formation of long and winding nuclear F-actin bundles by nuclear c-Abl tyrosine kinase

Abstract

The non-receptor-type tyrosine kinase c-Abl is involved in actin dynamics in the cytoplasm. Having three nuclear localization signals (NLSs) and one nuclear export signal, c-Abl shuttles between the nucleus and the cytoplasm. Although monomeric actin and filamentous actin (F-actin) are present in the nucleus, little is known about the relationship between c-Abl and nuclear actin dynamics. Here, we show that nuclear-localized c-Abl induces nuclear F-actin formation. Adriamycin-induced DNA damage together with leptomycin B treatment accumulates c-Abl into the nucleus and increases the levels of nuclear F-actin. Treatment of c-Abl-knockdown cells with Adriamycin and leptomycin B barely increases the nuclear F-actin levels. Expression of nuclear-targeted c-Abl (NLS-c-Abl) increases the levels of nuclear F-actin even without Adriamycin, and the increased levels of nuclear F-actin are not inhibited by inactivation of Abl kinase activity. Intriguingly, expression of NLS-c-Abl induces the formation of long and winding bundles of F-actin within the nucleus in a c-Abl kinase activity-dependent manner. Furthermore, NLS-c-AblΔC, which lacks the actin-binding domain but has the full tyrosine kinase activity, is incapable of forming nuclear F-actin and in particular long and winding nuclear F-actin bundles. These results suggest that nuclear c-Abl plays critical roles in actin dynamics within the nucleus. - Highlights:more » • We show the involvement of c-Abl tyrosine kinase in nuclear actin dynamics. • Nuclear F-actin is formed by nuclear-localized c-Abl and its kinase-dead version. • The c-Abl actin-binding domain is prerequisite for nuclear F-actin formation. • Formation of long nuclear F-actin bundles requires nuclear c-Abl kinase activity. • We discuss a role for nuclear F-actin bundle formation in chromatin regulation.« less

Authors:
; ; ; ; ; ; ;  [1]; ; ;  [2];  [1]
  1. Department of Molecular Cell Biology, Graduate School of Pharmaceutical Sciences, Chiba University, Inohana 1-8-1, Chuo-ku, Chiba 260-8675 (Japan)
  2. Laboratory of Proteome Research, National Institute of Biomedical Innovation, Ibaraki, Osaka 567-0085 (Japan)
Publication Date:
OSTI Identifier:
22278207
Resource Type:
Journal Article
Journal Name:
Experimental Cell Research
Additional Journal Information:
Journal Volume: 319; Journal Issue: 20; Other Information: Copyright (c) 2013 Elsevier Science B.V., Amsterdam, The Netherlands, All rights reserved.; Country of input: International Atomic Energy Agency (IAEA); Journal ID: ISSN 0014-4827
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES; ACTIN; CHROMATIN; CYTOPLASM; DNA DAMAGES; DOXORUBICIN; PHOSPHORYLATION; RECEPTORS; TYROSINE

Citation Formats

Aoyama, Kazumasa, Yuki, Ryuzaburo, Horiike, Yasuyoshi, Kubota, Sho, Yamaguchi, Noritaka, Morii, Mariko, Ishibashi, Kenichi, Nakayama, Yuji, Kuga, Takahisa, Hashimoto, Yuuki, Tomonaga, Takeshi, and Yamaguchi, Naoto. Formation of long and winding nuclear F-actin bundles by nuclear c-Abl tyrosine kinase. United States: N. p., 2013. Web. doi:10.1016/J.YEXCR.2013.09.003.
Aoyama, Kazumasa, Yuki, Ryuzaburo, Horiike, Yasuyoshi, Kubota, Sho, Yamaguchi, Noritaka, Morii, Mariko, Ishibashi, Kenichi, Nakayama, Yuji, Kuga, Takahisa, Hashimoto, Yuuki, Tomonaga, Takeshi, & Yamaguchi, Naoto. Formation of long and winding nuclear F-actin bundles by nuclear c-Abl tyrosine kinase. United States. https://doi.org/10.1016/J.YEXCR.2013.09.003
Aoyama, Kazumasa, Yuki, Ryuzaburo, Horiike, Yasuyoshi, Kubota, Sho, Yamaguchi, Noritaka, Morii, Mariko, Ishibashi, Kenichi, Nakayama, Yuji, Kuga, Takahisa, Hashimoto, Yuuki, Tomonaga, Takeshi, and Yamaguchi, Naoto. 2013. "Formation of long and winding nuclear F-actin bundles by nuclear c-Abl tyrosine kinase". United States. https://doi.org/10.1016/J.YEXCR.2013.09.003.
@article{osti_22278207,
title = {Formation of long and winding nuclear F-actin bundles by nuclear c-Abl tyrosine kinase},
author = {Aoyama, Kazumasa and Yuki, Ryuzaburo and Horiike, Yasuyoshi and Kubota, Sho and Yamaguchi, Noritaka and Morii, Mariko and Ishibashi, Kenichi and Nakayama, Yuji and Kuga, Takahisa and Hashimoto, Yuuki and Tomonaga, Takeshi and Yamaguchi, Naoto},
abstractNote = {The non-receptor-type tyrosine kinase c-Abl is involved in actin dynamics in the cytoplasm. Having three nuclear localization signals (NLSs) and one nuclear export signal, c-Abl shuttles between the nucleus and the cytoplasm. Although monomeric actin and filamentous actin (F-actin) are present in the nucleus, little is known about the relationship between c-Abl and nuclear actin dynamics. Here, we show that nuclear-localized c-Abl induces nuclear F-actin formation. Adriamycin-induced DNA damage together with leptomycin B treatment accumulates c-Abl into the nucleus and increases the levels of nuclear F-actin. Treatment of c-Abl-knockdown cells with Adriamycin and leptomycin B barely increases the nuclear F-actin levels. Expression of nuclear-targeted c-Abl (NLS-c-Abl) increases the levels of nuclear F-actin even without Adriamycin, and the increased levels of nuclear F-actin are not inhibited by inactivation of Abl kinase activity. Intriguingly, expression of NLS-c-Abl induces the formation of long and winding bundles of F-actin within the nucleus in a c-Abl kinase activity-dependent manner. Furthermore, NLS-c-AblΔC, which lacks the actin-binding domain but has the full tyrosine kinase activity, is incapable of forming nuclear F-actin and in particular long and winding nuclear F-actin bundles. These results suggest that nuclear c-Abl plays critical roles in actin dynamics within the nucleus. - Highlights: • We show the involvement of c-Abl tyrosine kinase in nuclear actin dynamics. • Nuclear F-actin is formed by nuclear-localized c-Abl and its kinase-dead version. • The c-Abl actin-binding domain is prerequisite for nuclear F-actin formation. • Formation of long nuclear F-actin bundles requires nuclear c-Abl kinase activity. • We discuss a role for nuclear F-actin bundle formation in chromatin regulation.},
doi = {10.1016/J.YEXCR.2013.09.003},
url = {https://www.osti.gov/biblio/22278207}, journal = {Experimental Cell Research},
issn = {0014-4827},
number = 20,
volume = 319,
place = {United States},
year = {Tue Dec 10 00:00:00 EST 2013},
month = {Tue Dec 10 00:00:00 EST 2013}
}