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

Experimental Cell Research

Volumn 319, Issue 20, 2013, Pages 3251-3268

  Aoyama, Kazumasa ^a   Yuki, Ryuzaburo ^a   Horiike, Yasuyoshi ^a   Kubota, Sho ^a   Yamaguchi, Noritaka ^a   Morii, Mariko ^a   Ishibashi, Kenichi ^a   Nakayama, Yuji ^a   Kuga, Takahisa ^b   Hashimoto, Yuuki ^b   Tomonaga, Takeshi ^b   Yamaguchi, Naoto ^a  

^a CHIBA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

Author keywords

Actin dynamics; Actin biding domain; C Abl tyrosine kinase; F actin; Nucleus; Tyrosine phosphorylation

Indexed keywords

ABELSON KINASE; ACTIN BINDING PROTEIN; BETA ACTIN; COMPLEMENTARY DNA; DOXORUBICIN; F ACTIN; LEPTOMYCIN B; MONOMER; PROTEIN TYROSINE KINASE;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DNA DAMAGE; ENZYME ACTIVITY; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; NUCLEAR EXPORT SIGNAL; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 84887140427     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2013.09.003     Document Type: Article

References (63)

1. Hantschel O., Superti-Furga G. Regulation of the c-Abl and Bcr-Abl tyrosine kinases. Nat. Rev. Mol. Cell Biol. 2004, 5:33-44.
2. Sirvent A., Benistant C., Roche S. Cytoplasmic signalling by the c-Abl tyrosine kinase in normal and cancer cells. Biol. Cell 2008, 100:617-631.
3. Van Etten R.A., Jackson P.K., Baltimore D., Sanders M.C., Matsudaira P.T., Janmey P.A. The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J. Cell Biol. 1994, 124:325-340.
4. Woodring P.J., Hunter T., Wang J.Y.J. Regulation of F-actin-dependent processes by the Abl family of tyrosine kinases. J. Cell Sci. 2003, 116:2613-2626.
5. Leng Y., Zhang J., Badour K., Arpaia E., Freeman S., Cheung P., Siu M., Siminovitch K. Abelson-interactor-1 promotes WAVE2 membrane translocation and Abelson-mediated tyrosine phosphorylation required for WAVE2 activation. Proc. Natl. Acad. Sci. USA 2005, 102:1098-1103.
6. Cans C., Mangano R., Barilá D., Neubauer G., Superti-Furga G. Nuclear tyrosine phosphorylation: the beginning of a map. Biochem. Pharmacol. 2000, 60:1203-1215.
7. Moorhead G.B.G., Trinkle-Mulcahy L., Ulke-Lemée A. Emerging roles of nuclear protein phosphatases. Nat. Rev. Mol. Cell Biol. 2007, 8:234-244.
8. Yamaguchi N., Nakayama Y., Urakami T., Suzuki S., Nakamura T., Suda T., Oku N. Overexpression of the Csk homologous kinase (Chk tyrosine kinase) induces multinucleation: a possible role for chromosome-associated Chk in chromosome dynamics. J. Cell. Sci. 2001, 114:1631-1641.
9. Ikeda K., Nakayama Y., Togashi Y., Obata Y., Kuga T., Kasahara K., Fukumoto Y., Yamaguchi N. Nuclear localization of Lyn tyrosine kinase mediated by inhibition of its kinase activity. Exp. Cell Res. 2008, 314:3392-3404.
10. Takahashi A., Obata Y., Fukumoto Y., Nakayama Y., Kasahara K., Kuga T., Higashiyama Y., Saito T., Yokoyama K.K., Yamaguchi N. Nuclear localization of Src-family tyrosine kinases is required for growth factor-induced euchromatinization. Exp. Cell Res. 2009, 315:1117-1141.
11. Taagepera S., McDonald D., Loeb J.E., Whitaker L.L., McElroy A.K., Wang J.Y.J., Hope T.J. Nuclear-cytoplasmic shuttling of c-Abl tyrosine kinase. Proc. Natl. Acad. Sci. USA 1998, 95:7457-7462.
12. Baskaran R., Wood L.D., Whitaker L.L., Canman C.E., Morgan S.E., Xu Y., Barlow C., Baltimore D., Wynshaw-Boris A., Kastan M.B., Wang J.Y.J. Ataxia telangiectasia mutant protein activates c-Abl tyrosine kinase in response to ionizing radiation. Nature 1997, 387:516-519.
13. Shafman T., Khanna K.K., Kedar P., Spring K., Kozlov S., Yen T., Hobson K., Gatei M., Zhang N., Watters D., Egerton M., Shiloh Y., Kharbanda S., Kufe D., Lavin M.F. Interaction between ATM protein and c-Abl in response to DNA damage. Nature 1997, 387:520-523.
14. Shaul Y., Ben-Yehoyada M. Role of c-Abl in the DNA damage stress response. Cell Res. 2005, 15:33-35.
15. Maiani E., Diederich M., Gonfloni S. DNA damage response: the emerging role of c-Abl as a regulatory switch?. Biochem. Pharmacol. 2011, 82:1269-1276.
16. McDonald D., Carrero G., Andrin C., de Vries G., Hendzel M.J. Nucleoplasmic β-actin exists in a dynamic equilibrium between low-mobility polymeric species and rapidly diffusing populations. J. Cell Biol. 2006, 172:541-552.
17. Visa N., Percipalle P. Nuclear Functions of Actin. Cold Spring Harbor Perspect. Biol. 2010, 2:a000620.
18. de Lanerolle P., Serebryannyy L. Nuclear actin and myosins: life without filaments. Nat. Cell Biol. 2011, 13:1282-1288.
19. Simon D.N., Wilson K.L. The nucleoskeleton as a genome-associated dynamic 'network of net works'. Nat. Rev. Mol. Cell Biol. 2011, 12:695-708.
20. de Lanerolle P. Nuclear actin and myosins at a glance. J. Cell Sci. 2012, 125:4945-4949.
21. Belin B.J., Cimini B.A., Blackburn E.H., Mullins R.D. Visualization of actin filaments and monomers. Mol. Biol. Cell 2013, 24:982-994.
22. Wada A., Fukuda M., Mishima M., Nishida E. Nuclear export of actin: a novel mechanism regulating the subcellular localization of a major cytoskeletal protein. EMBO J. 1998, 17:1635-1641.
23. Stüven T., Hartmann E., Görlich D. Exportin 6: a novel nuclear export receptor that is specific for profilin.actin complexes. EMBO J. 2003, 22:5928-5940.
24. Huet G., Skarp K.P., Vartiainen M.K. Nuclear actin levels as an important transcriptional switch. Transcription 2012, 3:1-5.
25. Dopie J., Skarp K.P., Rajakylä E.K., Tanhuanpää K., Vartiainen M.K. Active maintenance of nuclear actin by importin 9 supports transcription. Proc. Natl. Acad. Sci. USA 2012, 109:E544-E552.
26. Shtivelman E., Lifshitz B., Gale R.P., Canaani E. Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature 1985, 315:550-554.
27. Kasahara K., Nakayama Y., Nakazato Y., Ikeda K., Kuga T., Yamaguchi N. Src signaling regulates completion of abscission in cytokinesis through ERK/MAPK activation at the midbody. J. Biol. Chem. 2007, 282:5327-5339.
28. Aoyama K., Fukumoto Y., Ishibashi K., Kubota S., Morinaga T., Horiike Y., Yuki R., Takahashi A., Nakayama Y., Yamaguchi N. Nuclear c-Abl-mediated tyrosine phosphorylation induces chromatin structural changes through histone modifications that include H4K16 hypoacetylation. Exp. Cell Res. 2011, 317:2874-2903.
29. lck. Mol. Cell. Biol. 1987, 7:237-243.
30. Law C.L., Sidorenko S.P., Chandran K.A., Draves K.E., Chan A.C., Weiss A., Edelhoff S., Disteche C.M., Clark E.A. Molecular cloning of human Syk. A B cell protein-tyrosine kinase associated with the surface immunoglobulin M-B cell receptor complex. J. Biol. Chem. 1994, 269:12310-12319.
31. 2+ channels. Proc. Natl. Acad. Sci. USA 2002, 99:14458-14463.
32. Kuga T., Hoshino M., Nakayama Y., Kasahara K., Ikeda K., Obata Y., Takahashi A., Higashiyama Y., Fukumoto Y., Yamaguchi N. Role of Src-family kinases in formation of the cortical actin cap at the dorsal cell surface. Exp. Cell Res. 2008, 314:2040-2054.
33. Tamura T., Kunimatsu T., Yee S.T., Igarashi O., Utsuyama M., Tanaka S., Miyazaki S., Hirokawa K., Nariuchi H. Molecular mechanism of the impairment in activation signal transduction in CD4 T cells from old mice. Int. Immunol. 2000, 12:1205-1215.
34. Kamath R., Jiang Z., Sun G., Yalowich J.C., Baskaran R. c-Abl kinase regulates curcumin-induced cell death through activation of c-Jun N-terminal kinase. Mol. Pharmacol. 2007, 71:61-72.
35. Fukumoto Y., Obata Y., Ishibashi K., Tamura N., Kikuchi I., Aoyama K., Hattori Y., Tsuda K., Nakayama Y., Yamaguchi N. Cost-effective gene transfection by DNA compaction at pH 4.0 using acidified, long shelf-life polyethylenimine. Cytotechnology 2010, 62:73-82.
36. Nakayama Y., Yamaguchi N. Multi-lobulation of the nucleus in prolonged S phase by nuclear expression of Chk tyrosine kinase. Exp. Cell Res. 2005, 304:570-581.
37. Kasahara K., Nakayama Y., Kihara A., Matsuda D., Ikeda K., Kuga T., Fukumoto Y., Igarashi Y., Yamaguchi N. Rapid trafficking of c-Src, a non-palmitoylated Src-family kinase, between the plasma membrane and late endosomes/lysosomes. Exp. Cell Res. 2007, 313:2651-2666.
38. Sato I., Obata Y., Kasahara K., Nakayama Y., Fukumoto Y., Yamasaki T., Yokoyama K.K., Saito T., Yamaguchi N. Differential trafficking of Src, Lyn, Yes and Fyn is specified by the state of palmitoylation in the SH4 domain. J. Cell. Sci. 2009, 122:965-975.
39. Obata Y., Fukumoto Y., Nakayama Y., Kuga T., Dohmae N., Yamaguchi N. The Lyn kinase C-lobe mediates Golgi export of Lyn through conformation-dependent ACSL3 association. J. Cell Sci. 2010, 123:2649-2662.
40. Yamaguchi N., Fukuda M.N. Golgi retention mechanism of ß-1,4-galactosyltransferase: membrane-spanning domain-dependent homodimerization and association with α- and β-tubulins. J. Biol. Chem. 1995, 270:12170-12176.
41. Tada J., Omine M., Suda T., Yamaguchi N. A common signaling pathway via Syk and Lyn tyrosine kinases generated from capping of the sialomucins CD34 and CD43 in immature hematopoietic cells. Blood 1999, 93:3723-3735.
42. Kasahara K., Nakayama Y., Ikeda K., Fukushima Y., Matsuda D., Horimoto S., Yamaguchi N. Trafficking of Lyn through the Golgi caveolin involves the charged residues on αE and αI helices in the kinase domain. J. Cell Biol. 2004, 165:641-652.
43. Matsuda D., Nakayama Y., Horimoto S., Kuga T., Ikeda K., Kasahara K., Yamaguchi N. Involvement of Golgi-associated Lyn tyrosine kinase in the translocation of annexin II to the endoplasmic reticulum under oxidative stress. Exp. Cell Res. 2006, 312:1205-1217.
44. Kasahara K., Nakayama Y., Sato I., Ikeda K., Hoshino M., Endo T., Yamaguchi N. Role of Src-family kinases in formation and trafficking of macropinosomes. J. Cell. Physiol. 2007, 211:220-232.
45. Huyer G., Liu S., Kelly J., Moffat J., Payette P., Kennedy B., Tsaprailis G., Gresser M.J., Ramachandran C. Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J. Biol. Chem. 1997, 272:843-851.
46. Spector I., Shochet N.R., Kashman Y., Groweiss A. Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 1983, 219:493-495.
47. Wakatsuki T., Schwab B., Thompson N.C., Elson E.L. Effects of cytochalasin D and latrunculin B on mechanical properties of cells. J. Cell Sci. 2001, 114:1025-1036.
48. Zhou F., Hu J., Ma H., Harrison M.L., Geahlen R.L. Nucleocytoplasmic trafficking of the syk protein tyrosine kinase. Mol. Cell. Biol. 2006, 26:3478-3491.
49. Ishibashi K., Fukumoto Y., Hasegawa H., Kubota S., Aoyama K., Kubota S., Nakayama Y., Yamaguchi N. Nuclear ErbB4 signaling through H3K9me3 is antagonized by EGFR-activated c-Src. J. Cell Sci. 2013, 126:625-637.
50. Kubota S., Fukumoto Y., Aoyama K., Ishibashi K., Yuki R., Morinaga T., Honda T., Yamaguchi N.-t., Kuga T., Tomonaga T., Yamaguchi N. Phosphorylation of KRAB-associated protein 1 (KAP1) at Tyr-449, Tyr-458, and Tyr-517 by nuclear tyrosine kinases inhibits the association of KAP1 and heterochromatin protein 1α (HP1α) with heterochromatin. J. Biol. Chem. 2013, 288:17871-17883.
51. Preyer M., Vigneri P., Wang J.Y.J. Interplay between kinase domain autophosphorylation and F-actin binding domain in regulating imatinib sensitivity and nuclear import of BCR-ABL. PLoS One 2011, 6:e17020.
52. Grunstein M. Histone acetylation in chromatin structure and transcription. Nature 1997, 389:349-352.
53. Lamond A.I., Earnshaw W.C. Structure and function in the nucleus. Science 1998, 280:547-553.
54. Strahl B.D., Allis C.D. The language of covalent histone modifications. Nature 2000, 403:41-45.
55. Jenuwein T., Allis C.D. Translating the histone code. Science 2001, 293:1074-1080.
56. Andrin C., Hendzel M.J. F-actin-dependent insolubility of chromatin-modifying components. J. Biol. Chem. 2004, 279:25017-25023.
57. Andrin C., McDonald D., Attwood K.M., Rodrigue A., Ghosh S., Mirzayans R., Masson J.Y., Dellaire G., Hendzel M.J. A requirement for polymerized actin in DNA double-strand break repair. Nucleus 2012, 3:384-395.
58. Obrdlik A., Percipalle P. The F-actin severing protein cofilin-1 is required for RNA polymerase II transcription elongation. Nucleus 2011, 2:72-79.
59. Söderberg E., Hessle V., von Euler A., Visa N. Profilin is associated with transcriptionally active genes. Nucleus 2012, 3:290-299.
60. Percipalle P. Co-transcriptional nuclear actin dynamics. Nucleus 2013, 4:43-52.
61. Zuchero J.B., Coutts A.S., Quinlan M.E., La Thangue N.B., Mullins R.D. p53-cofactor JMY is a multifunctional actin nucleation factor. Nat. Cell Biol. 2009, 11:451-459.
62. Zuchero J.B., Belin B., Mullins R.D. Actin binding to WH2 domains regulates nuclear import of the multifunctional actin regulator JMY. Mol. Biol. Cell 2012, 23:853-863.
63. Baarlink C., Wang H., Grosse R. Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 2013, 340:864-867.