C-Abl induces stabilization of histone deacetylase 1 (HDAC1) in a kinase activity-dependent manner

Cell Biology International

Volumn 39, Issue 4, 2015, Pages 446-456

  Aoyama, Kazumasa ^a   Yamaguchi, Noritaka ^a   Yuki, Ryuzaburo ^a   Morii, Mariko ^a   Kubota, Sho ^a   Hirata, Kensuke ^a   Abe, Kohei ^a   Honda, Takuya ^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

C Abl tyrosine kinase; Histone deacetylase; Protein stability

Indexed keywords

ABELSON KINASE; HISTONE DEACETYLASE 1; IMATINIB; NUCLEAR PROTEIN; BENZYLOXYCARBONYLLEUCYL-LEUCYL-LEUCINE ALDEHYDE; HDAC1 PROTEIN, HUMAN; LEUPEPTIN; MESSENGER RNA; PROTEASOME;

ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL FRACTIONATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME STABILITY; GENE OVEREXPRESSION; GENE SILENCING; GENETIC TRANSFECTION; HELA CELL LINE; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; UPREGULATION; CELL NUCLEUS; DRUG EFFECTS; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MCF 7 CELL LINE; METABOLISM; PHOSPHORYLATION; PROTEIN STABILITY;

CELL NUCLEUS; GENE EXPRESSION REGULATION; HELA CELLS; HISTONE DEACETYLASE 1; HUMANS; LEUPEPTINS; MCF-7 CELLS; MICROSCOPY, FLUORESCENCE; PHOSPHORYLATION; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN STABILITY; PROTO-ONCOGENE PROTEINS C-ABL; RNA, MESSENGER;

EID: 84925329288     PISSN: 10656995     EISSN: 10958355     Source Type: Journal    
DOI: 10.1002/cbin.10413     Document Type: Article

References (36)

1. Aoyama K, Fukumoto Y, Ishibashi K, Kubota S, Morinaga T, Horiike Y, Yuki R, Takahashi A, Nakayama Y, Yamaguchi N ( 2011) Nuclear c-Abl-mediated tyrosine phosphorylation induces chromatin structural changes through histone modifications that include H4K16 hypoacetylation. Exp Cell Res 317: 2874-903.
2. Aoyama K, Yuki R, Horiike Y, Kubota S, Yamaguchi N, Morii M, Ishibashi K, Nakayama Y, Kuga T, Hashimoto Y, Tomonaga T, Yamaguchi N ( 2013) Formation of long and winding nuclear F-actin bundles by nuclear c-Abl tyrosine kinase. Exp Cell Res 319: 3251-68.
3. Ben-Neriah Y, Daley GQ, Mes-Masson AM, Witte ON, Baltimore D ( 1986) The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science 233: 212-4.
4. Cans C, Mangano R, Barila D, Neubauer G Superti-Furga G ( 2000) Nuclear tyrosine phosphorylation: the beginning of a map. Biochem Pharmacol 60: 1203-15.
5. Choi JH, Kwon HJ, Yoon BI, Kim JH, Han SU, Joo HJ, Kim DY ( 2001) Expression profile of histone deacetylase 1 in gastric cancer tissues. Jpn J Cancer Res 92: 1300-4.
6. Citro S, Jaffray E, Hay RT, Seiser C, Chiocca S ( 2013) A role for paralog-specific sumoylation in histone deacetylase 1 stability. J Mol Cell Biol 5: 416-27.
7. Clayton AL, Hazzalin CA, Mahadevan LC ( 2006) Enhanced histone acetylation and transcription: a dynamic perspective. Mol Cell 23: 289-96.
8. Fritzsche FR, Weichert W, Roske A, Gekeler V, Beckers T, Stephan C, Jung K, Scholman K, Denkert C, Dietel M, Kristiansen G ( 2008) Class I histone deacetylases 1, 2 and 3 are highly expressed in renal cell cancer. BMC Cancer 8: 381.
9. Fukumoto Y, Obata Y, Ishibashi K, Tamura N, Kikuchi I, Aoyama K, Hattori Y, Tsuda K, Nakayama Y, Yamaguchi N ( 2010) Cost-effective gene transfection by DNA compaction at pH 4.0 using acidified, long shelf-life polyethylenimine. Cytotechnology 62: 73-82.
10. Fukumoto Y, Morii M, Miura T, Kubota S, Ishibashi K, Honda T, Okamoto A, Yamaguchi N, Iwama A, Nakayama Y, Yamaguchi N ( 2014) Src family kinases promote silencing of ATR-Chk1 signaling in termination of DNA damage checkpoint. J Biol Chem 289: 12313-29.
11. Greuber EK, Smith-Pearson P, Wang J, Pendergast AM ( 2013) Role of ABL family kinases in cancer: from leukaemia to solid tumours. Nat Rev Cancer 13: 559-71.
12. Haberland M, Montgomery RL, Olson EN ( 2009) The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 10: 32-4.
13. Hantschel O, Nagar B, Guettler S, Kretzschmar J, Dorey K, Kuriyan J Superti-Furga G ( 2003) A myristoyl/phosphotyrosine switch regulates c-Abl. Cell 112: 845-57.
14. Ikeda K, Nakayama Y, Togashi Y, Obata Y, Kuga T, Kasahara K, Fukumoto Y, Yamaguchi N ( 2008) Nuclear localization of Lyn tyrosine kinase mediated by inhibition of its kinase activity. Exp Cell Res 314: 3392-404.
15. Ishibashi K, Fukumoto Y, Hasegawa H, Abe K, Kubota S, Aoyama K, Nakayama Y, Yamaguchi N ( 2013) Nuclear ErbB4 signaling through H3K9me3 is antagonized by EGFR-activated c-Src. J Cell Sci 126: 625-37.
16. Kaidi A, Jackson SP ( 2013) KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling. Nature 498: 70-4.
17. Kim LC, Song L, Haura EB ( 2009) Src kinases as therapeutic targets for cancer. Nat Rev Clin Oncol 6: 587-95.
18. Kramer OH, Zhu P, Ostendorff HP, Golebiewski M, Tiefenbach J, Peters MA, Brill B, Groner B, Bach I, Heinzel T, Gottlicher M ( 2003) The histone deacetylase inhibitor valproic acid selectively induces proteasomal degradation of HDAC2. EMBO J 22: 3411-20.
19. Kubota S, Fukumoto Y, Aoyama K, Ishibashi K, Yuki R, Morinaga T, Honda T, Yamaguchi N, Kuga T, Tomonaga T ( 2013) 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 288: 17871-83.
20. Levy D, Adamovich Y, Reuven N, Shaul Y ( 2008) Yap1 phosphorylation by c-Abl is a critical step in selective activation of proapoptotic genes in response to DNA damage. Mol Cell 29: 350-61.
21. Liberatore RA, Goff SP, Nunes I ( 2009) NF-κB activity is constitutively elevated in c-Abl null fibroblasts. Proc Natl Acad Sci U S A 106: 17823-8.
22. Marks PA ( 2010) The clinical development of histone deacetylase inhibitors as targeted anticancer drugs. Expert Opin Investig Drugs 19: 1049-66.
23. Miyake K, Yoshizumi T, Imura S, Sugimoto K, Batmunkh E, Kanemura H, Morine Y, Shimada M ( 2008) Expression of hypoxia-inducible factor-1alpha, histone deacetylase 1, and metastasis-associated protein 1 in pancreatic carcinoma: correlation with poor prognosis with possible regulation. Pancreas 36: e1-9.
24. Oh YM, Kwon YE, Kim JM, Bae SJ, Lee BK, Yoo SJ, Chung CH, Deshaies RJ, Seol JH ( 2009) Chfr is linked to tumour metastasis through the downregulation of HDAC1. Nat Cell Biol 11: 295-302.
25. Rikimaru T, Taketomi A, Yamashita Y, Shirabe K, Hamatsu T, Shimada M, Maehara Y ( 2007) Clinical significance of histone deacetylase 1 expression in patients with hepatocellular carcinoma. Oncology 72: 69-74.
26. Shaul Y, Ben-Yehoyada M ( 2005) Role of c-Abl in the DNA damage stress response. Cell Res 15: 33-5.
27. Shtivelman E, Lifshitz B, Gale RP, Canaani E ( 1985) Fused transcript of abl and bcr genes in chronic myelogenous leukaemia. Nature 315: 550-4.
28. Spiegel S, Milstien S, Grant S ( 2012) Endogenous modulators and pharmacological inhibitors of histone deacetylases in cancer therapy. Oncogene 31: 537-51.
29. Taagepera S, McDonald D, Loeb JE, Whitaker LL, McElroy AK, Wang JY, Hope TJ ( 1998) Nuclear-cytoplasmic shuttling of C-ABL tyrosine kinase. Proc Natl Acad Sci U S A 95: 7457-62.
30. Takahashi A, Obata Y, Fukumoto Y, Nakayama Y, Kasahara K, Kuga T, Higashiyama Y, Saito T, Yokoyama KK, Yamaguchi N ( 2009) Nuclear localization of Src-family tyrosine kinases is required for growth factor-induced euchromatinization. Exp Cell Res 315: 1117-41.
31. Tamura T, Kunimatsu T, Yee ST, Igarashi O, Utsuyama M, Tanaka S, Miyazaki S, Hirokawa K, Nariuchi H ( 2000) Molecular mechanism of the impairment in activation signal transduction in CD4(+) T cells from old mice. Int Immunol 12: 1205-1.
32. Weichert W, Roske A, Gekeler V, Beckers T, Stephan C, Jung K, Fritzsche FR, Niesporek S, Denkert C, Dietel M, Kristiansen G ( 2008) Histone deacetylases 1, 2 and 3 are highly expressed in prostate cancer and HDAC2 expression is associated with shorter PSA relapse time after radical prostatectomy. Br J Cancer 98: 604-10.
33. Yamaguchi N, Nakayama Y, Urakami T, Suzuki S, Nakamura T, Suda T, Oku N ( 2001) Overexpression of the Csk homologous kinase (Chk tyrosine kinase) induces multinucleation: a possible role for chromosome-associated Chk in chromosome dynamics. J Cell Sci 114: 1631-4.
34. Yamaguchi N, Yokota M, Taguchi Y, Gohda J, Inoue J ( 2012) CIAP1/2 negatively regulate RANKL-induced osteoclastogenesis through the inhibition of NFATc1 expression. Genes Cells 17: 971-8.
35. Zhang Z, Yamashita H, Toyama T, Sugiura H, Ando Y, Mita K, Hamaguchi M, Hara Y, Kobayashi S, Iwase H ( 2005) Quantitation of HDAC1 mRNA expression in invasive carcinoma of the breast*. Breast Cancer Res Treat 94: 11-6.
36. Zhang J, Kan S, Huang B, Hao Z, Mak TW, Zhong Q ( 2011) Mule determines the apoptotic response to HDAC inhibitors by targeted ubiquitination and destruction of HDAC2. Genes Dev 25: 2610-8.