Serine/arginine protein-specific kinase 2 promotes leukemia cell proliferation by phosphorylating acinus and regulating cyclin A1

Cancer Research

Volumn 68, Issue 12, 2008, Pages 4559-4570

  Jang, Sung Wuk ^a   Yang, Seung Ju ^a   Ehlén, Åsa ^b   Dong, Shaozhong ^a   Khoury, Hanna ^a   Chen, Jing ^a   Persson, Jenny L ^b   Ye, Keqiang ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LUND UNIVERSITY   (Sweden)

^c EMORY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A1; MESSENGER RNA; NUCLEOPLASMIN; PROTEIN SERINE KINASE; SERINE ARGININE PROTEIN SPECIFIC KINASE 2; UNCLASSIFIED DRUG; ACIN1 PROTEIN, HUMAN; CCNA1 PROTEIN, HUMAN; CYCLIN A; NUCLEAR PROTEIN; PROTEIN KINASE B; PROTEIN SERINE THREONINE KINASE; SERINE; SRPK2 PROTEIN, HUMAN;

ACINAR CELL; ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; CARCINOGENESIS; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CELL STRAIN HEK293; CONTROLLED STUDY; HUMAN; HUMAN CELL; LEUKEMIA CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RNA SPLICING; BONE MARROW; CELL CULTURE; CELL CYCLE; CELL NUCLEUS; CHEMISTRY; ENZYMOLOGY; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LEUKEMIA; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; TWO HYBRID SYSTEM;

BONE MARROW; CELL CYCLE; CELL NUCLEUS; CELL PROLIFERATION; CYCLIN A; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LEUKEMIA; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SACCHAROMYCES CEREVISIAE; SERINE; TUMOR CELLS, CULTURED; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 49649101933     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-08-0021     Document Type: Article

References (40)

1. Spector DL, Fu XD, Maniatis T. Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J 1991;10:3467-81.
2. Gui JF, Lane WS, Fu XD. A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 1994;369:678-82.
3. Wang HY, Lin W, Dyck JA, et al. SRPK2: a differentially expressed SR protein-specific kinase involved in mediating the interaction and localization of pre-mRNA splicing factors in mammalian cells. J Cell Biol 1998;140:737-50.
4. Johnson KW, Smith KA. Molecular cloning of a novel human cdc2/CDC28-like protein kinase. J Biol Chem 1991;266:3402-7.
5. Ben-David Y, Letwin K, Tannock L, Bernstein A, Pawson T. A mammalian protein kinase with potential for serine/threonine and tyrosine phosphorylation is related to cell cycle regulators. EMBO J 1991;10:317-25.
6. Howell BW, Afar DE, Lew J, et al. STY, a tyrosine-phosphorylating enzyme with sequence homology to serine/threonine kinases. Mol Cell Biol 1991;11:568-72.
7. Colwill K, Pawson T, Andrews B, et al. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution. EMBO J 1996;15:265-75.
8. Colwill K, Feng LL, Yeakley JM, et al. SRPK1 and Clk/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J Biol Chem 1996;271:24569-75.
9. Fukuhara T, Hosoya T, Shimizu S, et al. Utilization of host SR protein kinases and RNA-splicing machinery during viral replication. Proc Natl Acad Sci U S A 2006;103:11329-33.
10. Ding JH, Zhong XY, Hagopian JC, et al. Regulated cellular partitioning of SR protein-specific kinases in mammalian cells. Mol Biol Cell 2006;17:876-85.
11. Okamoto Y, Onogi H, Honda R, et al. Cdc2 kinase-mediated phosphorylation of splicing factor SF2/ASF. Biochem Biophys Res Commun 1998;249:872-8.
12. Sahara S, Aoto M, Eguchi Y, Imamoto N, Yoneda Y, Tsujimoto Y. Acinus is a caspase-3-activated protein required for apoptotic chromatin condensation. Nature 1999;401:168-73.
13. Rappsilber J, Ryder U, Lamond AI, Mann M. Large-scale proteomic analysis of the human spliceosome. Genome Res 2002;12:1231-45.
14. Schwerk C, Prasad J, Degenhardt K, et al. ASAP, a novel protein complex involved in RNA processing and apoptosis. Mol Cell Biol 2003;23:2981-90.
15. Joselin AP, Schulze-Osthoff K, Schwerk C. Loss of Acinus inhibits oligonucleosomal DNA fragmentation but not chromatin condensation during apoptosis. J Biol Chem 2006;281:12475-84.
16. Tange TO, Shibuya T, Jurica MS, Moore MJ. Biochemical analysis of the EJC reveals two new factors and a stable tetrameric protein core. RNA 2005;11:1869-83.
17. Hu Y, Yao J, Liu Z, Liu X, Fu H, Ye K. Akt phosphorylates acinus and inhibits its proteolytic cleavage, preventing chromatin condensation. EMBO J 2005;24:3543-54.
18. Hu Y, Liu Z, Yang SJ, Ye K. Acinus-provoked protein kinase C δ isoform activation is essential for apoptotic chromatin condensation. Cell Death Differ 2007;14:2035-46.
19. Chan CB, Liu X, Tang X, Fu H, Ye K. Akt phosphorylation of zyxin mediates its interaction with acinus-S and prevents acinus-triggered chromatin condensation. Cell Death Differ 2007;14:2035-46.
20. Furukawa Y. Cell cycle regulation of hematopoietic stem cells. Hum Cell 1998;11:81-92.
21. Wolgemuth DJ, Lele KM, Jobanputra V, Salazar G. The A-type cyclins and the meiotic cell cycle in mammalian male germ cells. Int J Androl 2004;27:192-9.
22. Yang R, Morosetti R, Koeffler HP. Characterization of a second human cyclin A that is highly expressed in testis and in several leukemic cell lines. Cancer Res 1997;57:913-20.
23. Yang R, Nakamaki T, Lubbert M, et al. Cyclin A1 expression in leukemia and normal hematopoietic cells. Blood 1999;93:2067-74.
24. Kramer A, Hochhaus A, Saussele S, Reichert A, Willer A, Hehlmann R. Cyclin A1 is predominantly expressed in hematological malignancies with myeloid differentiation. Leukemia 1998;12:893-8.
25. Liao C, Wang XY, Wei HQ, et al. Altered myelopoiesis and the development of acute myeloid leukemia in transgenic mice overexpressing cyclin A1. Proc Natl Acad Sci U S A 2001;98:6853-58.
26. Muller C, Yang R, Idos G, et al. c-myb transactivates the human cyclin A1 promoter and induces cyclin A1 gene expression. Blood 1999;94:4255-62.
27. Ye K, Compton DA, Lai MM, Walensky LD, Snyder SH. Protein 4.1N binding to nuclear mitotic apparatus protein in PC12 cells mediates the antiproliferative actions of nerve growth factor. J Neurosci 1999;19:10747-56.
28. Ye K, Ke Y, Keshava N, et al. Opium alkaloid noscapine is an antitumor agent that arrests metaphase and induces apoptosis in dividing cells. Proc Natl Acad Sci U S A 1998;95:1601-6.
29. Kuroyanagi N, Onogi H, Wakabayashi T, Hagiwara M. Novel SR-protein-specific kinase, SRPK2, disassembles nuclear speckles. Biochem Biophys Res Commun 1998;242:357-64.
30. Wu JY, Tang H, Havlioglu N. Alternative pre-mRNA splicing and regulation of programmed cell death. Prog Mol Subcell Biol 2003;31:153-85.
31. Kamachi M, Le TM, Kim SJ, Geiger ME, Anderson P, Utz PJ. Human autoimmune sera as molecular probes for the identification of an autoantigen kinase signaling pathway. J Exp Med 2002;196:1213-25.
32. Liu D, Matzuk MM, Sung WK, Guo Q, Wang P, Wolgemuth DJ. Cyclin A1 is required for meiosis in the male mouse. Nat Genet 1998;20:377-80.
33. Xiao SH, Manley JL. Phosphorylation of the ASF/SF2 RS domain affects both protein-protein and protein-RNA interactions and is necessary for splicing. Genes Dev 1997;11:334-44.
34. Xiao SH, Manley JL. Phosphorylation-dephosphorylation differentially affects activities of splicing factor ASF/SF2. EMBO J 1998;17:6359-67.
35. Blaustein M, Pelisch F, Tanos T, et al. Concerted regulation of nuclear and cytoplasmic activities of SR proteins by AKT. Nat Struct Mol Biol 2005;12:1037-44.
36. Patel NA, Kaneko S, Apostolatos HS, et al. Molecular and genetic studies imply Akt-mediated signaling promotes protein kinase CβII alternative splicing via phosphorylation of serine/arginine-rich splicing factor SRp40. J Biol Chem 2005;280:14302-9.
37. Caceres JF, Screaton GR, Krainer AR. A specific subset of SR proteins shuttles continuously between the nucleus and the cytoplasm. Genes Dev 1998;12:55-66.
38. Papoutsopoulou S, Nikolakaki E, Chalepakis G, Kruft V, Chevaillier P, Giannakouros T. SR protein-specific kinase 1 is highly expressed in testis and phosphorylates protamine 1. Nucleic Acids Res 1999;27:2972-80.
39. Chapman DL, Wolgemuth DJ. Expression of proliferating cell nuclear antigen in the mouse germ line and surrounding somatic cells suggests both proliferation-dependent and -independent modes of function. Int J Dev Biol 1994;38:491-7.
40. Lemaire R, Prasad J, Kashima T, Gustafson J, Manley JL, Lafyatis R. Stability of a PKCI-1-related mRNA is controlled by the splicing factor ASF/SF2: a novel function for SR proteins. Genes Dev 2002;16:594-7.