Comparative analysis of two murine CDC25B isoforms

Authors

  • Min Kook Kang Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834
  • Aera Bang Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834
  • Hwa Ok Choi Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834
  • Seung Jin Han Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834

Keywords:

Cdc25B, 14-3-3, localization, phosphatase activity, isoform

Abstract

CDC25B phosphatase plays a pivotal role in the cell cycle process by dephosphorylating and activating the CDC2 kinase of maturation-promoting factor (MPF). In mice, two transcripts of Cdc25B are generated by the alternative splicing of one gene. We compared the properties of these two forms of CDC25B. When the expression pattern of Cdc25B was examined using RT-PCR, both forms were detected in almost all mouse tissues tested. The expression of two forms of the CDC25B protein in various mouse tissues was confirmed using Western blotting with generated isoform specific antibodies. CDC25B1 tends to accumulate more in the cytosol than CDC25B2 does, and they have different binding capacity for 14-3-3 proteins. CDC25B1 was more effective in dephosphorylating in vitro substrate para-nitrophenyl phosphate and showed higher activity in the modified histone H1 kinase assay than CDC25B2. These results suggest that the two forms of CDC25B play different roles in cell cycle regulation.

DOI: 10.2298/ABS160315062K

Received: March 15, 2016; Revised: April 17, 2016; Accepted: April 19, 2016; Published online: July 28, 2016

How to cite this article: How to cite this article: Kang MK, Bang A, Choi HO, Han SJ. Comparative analysis of two murine CDC25B isoforms. Arch Biol Sci. 2017;69(1):35-44.

Downloads

Download data is not yet available.

Author Biographies

Min Kook Kang, Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834

Department of Biological Sciences

Aera Bang, Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834

Department of Biological Sciences

Hwa Ok Choi, Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834

Department of Biological Sciences

Seung Jin Han, Inje University, 197 Inje-ro, Gimhae, Gyeongnam, 50834

Department of Biological Sciences

References

Gabrielli BG, Lee MS, Walker DH, Piwnica-Worms H, Maller JL. Cdc25 regulates the phosphorylation and activity of the Xenopus cdk2 protein kinase complex. J Biol Chem. 1992;267(25):18040-6.

Lammer C, Wagerer S, Saffrich R, Mertens D, Ansorge W, Hoffmann I. The cdc25B phosphatase is essential for the G2/M phase transition in human cells. J Cell Sci. 1998;111(Pt16):2445-53.

Gabrielli BG, De Souza CP, Tonks ID, Clark JM, Hayward NK, Ellem KA. Cytoplasmic accumulation of cdc25B phosphatase in mitosis triggers centrosomal microtubule nucleation in HeLa cells. J Cell Sci. 1996;109 (Pt5):1081-93.

Sanchez Y, Wong C, Thoma RS, Richman R, Wu Z, Piwnica-Worms H, Elledge SJ. Conservation of the Chk1 checkpoint pathway in mammals: linkage of DNA damage to Cdk regulation through Cdc25. Science. 1997;277(5331):1497-501.

Zeng Y, Forbes KC, Wu Z, Moreno S, Piwnica-Worms H, Enoch T. Replication checkpoint requires phosphorylation of the phosphatase Cdc25 by Cds1 or Chk1. Nature. 1998;395(6701):507-10.

Wickramasinghe D, Becker S, Ernst MK, Resnick JL, Centanni JM, Tessarollo L, Grabel LB, Donovan PJ. Two CDC25 homologues are differentially expressed during mouse development. Development. 1995;121(7):2047-56.

Boutros R, Dozier C, Ducommun B. The when and wheres of CDC25 phosphatases. Curr Opin Cell Biol. 2006;18(2):185-91.

Ray D, Kiyokawa H. CDC25A levels determine the balance of proliferation and checkpoint response. Cell Cycle. 2007;6(24):3039-42.

Chen MS, Hurov J, White LS, Woodford-Thomas T, Piwnica-Worms H. Absence of apparent phenotype in mice lacking Cdc25C protein phosphatase. Mol Cell Biol. 2001;21(12):3853-61.

Lincoln AJ, Wickramasinghe D, Stein P, Schultz RM, Palko ME, De Miguel MP, Tessarollo L, Donovan PJ. Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet. 2002;30(4):446-9.

De Souza CP, Ellem KA, Gabrielli BG. Centrosomal and cytoplasmic Cdc2/cyclin B1 activation precedes nuclear mitotic events. Exp Cell Res. 2000;257(1):11-21.

Boutros R, Lobjois V, Ducommun B. CDC25B involvement in the centrosome duplication cycle and in microtubule nucleation. Cancer Res. 2007;67(24):11557-64.

Forrest AR, McCormack AK, DeSouza CP, Sinnamon JM, Tonks ID, Hayward NK, Ellem KA, Gabrielli BG. Multiple splicing variants of cdc25B regulate G2/M progression. Biochem Biophys Res Commun. 1999;260(2):510-5.

Baldin V, Cans C, Superti-Furga G, Ducommun B. Alternative splicing of the human CDC25B tyrosine phosphatase. Possible implications for growth control? Oncogene. 1997;14(20):2485-95.

Gabrielli BG, Clark JM, McCormack AK, Ellem KA. Hyperphosphorylation of the N-terminal domain of Cdc25 regulates activity toward cyclin B1/Cdc2 but not cyclin A/Cdk2. J Biol Chem. 1997;272(45):28607-14.

Lindqvist A, Kallstrom H, Karlsson Rosenthal C. Characterisation of Cdc25B localisation and nuclear export during the cell cycle and in response to stress. J Cell Sci. 2004;117(Pt 21):4979-90.

Woo ES, Rice RL, Lazo JS. Cell cycle dependent subcellular distribution of Cdc25B subtypes. Oncogene. 1999;18(17):2770-6.

Dutertre S, Cazales M, Quaranta M, Froment C, Trabut V, Dozier C, Mirey G, Bouche JP, Theis-Febvre N, Schmitt E, Monsarrat B, Prigent C, Ducommun B. Phosphorylation of CDC25B by Aurora-A at the centrosome contributes to the G2-M transition. J Cell Sci. 2004;117(Pt 12):2523-31.

Baldin V, Theis-Febvre N, Benne C, Froment C, Cazales M, Burlet-Schiltz O, Ducommun B. PKB/Akt phosphorylates the CDC25B phosphatase and regulates its intracellular localisation. Biol Cell. 2003;95(8):547-54.

Uchida S, Kuma A, Ohtsubo M, Shimura M, Hirata M, Nakagama H, Matsunaga T, Ishizaka Y, Yamashita K. Binding of 14-3-3beta but not 14-3-3sigma controls the cytoplasmic localization of CDC25B: binding site preferences of 14-3-3 subtypes and the subcellular localization of CDC25B. J Cell Sci. 2004;117(Pt 14):3011-20.

Giles N, Forrest A, Gabrielli B. 14-3-3 acts as an intramolecular bridge to regulate cdc25B localization and activity. J Biol Chem. 2003;278(31):28580-7.

Kumagai A, Yakowec PS, Dunphy WG. 14-3-3 proteins act as negative regulators of the mitotic inducer Cdc25 in Xenopus egg extracts. Mol Biol Cell. 1998;9(2):345-54.

Conklin DS, Galaktionov K, Beach D. 14-3-3 proteins associate with cdc25 phosphatases. Proc Natl Acad Sci U S A. 1995;92(17):7892-6.

Cui C, Ren X, Liu D, Deng X, Qin X, Zhao X, Wang E, Yu B. 14-3-3 epsilon prevents G2/M transition of fertilized mouse eggs by binding with CDC25B. BMC Dev Biol. 2014;14:33.

Meng J, Cui C, Liu Y, Jin M, Wu D, Liu C, Wang E, Yu B. The role of 14-3-3epsilon interaction with phosphorylated Cdc25B at its Ser321 in the release of the mouse oocyte from prophase I arrest. PLoS One. 2013;8(1):e53633.

Bulavin DV, Higashimoto Y, Popoff IJ, Gaarde WA, Basrur V, Potapova O, Appella E, Fornace AJ, Jr. Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature. 2001;411(6833):102-7.

Pirino G, Wescott MP, Donovan PJ. Protein kinase A regulates resumption of meiosis by phosphorylation of Cdc25B in mammalian oocytes. Cell Cycle. 2009;8(4):665-70.

Kjarland E, Keen TJ, Kleppe R. Does isoform diversity explain functional differences in the 14-3-3 protein family? Curr Pharm Biotechnol. 2006;7(3):217-23.

Lee KH, Tsutsui T, Honda K, Ohtake H, Omasa T. Overexpression of mutant cell division cycle 25 homolog B (CDC25B) enhances the efficiency of selection in Chinese hamster ovary cells. Cytotechnology. 2013;65(6):1017-26.

Parks JM, Hu H, Rudolph J, Yang W. Mechanism of Cdc25B phosphatase with the small molecule substrate p-nitrophenyl phosphate from QM/MM-MFEP calculations. J Phys Chem B. 2009;113(15):5217-24.

Teng YN, Chung CL, Lin YM, Pan HA, Liao RW, Kuo PL. Expression of various CDC25B isoforms in human spermatozoa. Fertil Steril. 2007;88(2):379-82.

de Sousa Abreu R, Penalva LO, Marcotte EM, Vogel C. Global signatures of protein and mRNA expression levels. Mol Biosyst. 2009;5(12):1512-26.

Vogel C, Marcotte EM. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat Rev Genet. 2012;13(4):227-32.

Jullien D, Bugler B, Dozier C, Cazales M, Ducommun B. Identification of N-terminally truncated stable nuclear isoforms of CDC25B that are specifically involved in G2/M checkpoint recovery. Cancer Res. 2011;71(5):1968-77.

Fantes PA. Isolation of cell size mutants of a fission yeast by a new selective method: characterization of mutants and implications for division control mechanisms. J Bacteriol. 1981;146(2):746-54.

Alphey L, Jimenez J, White-Cooper H, Dawson I, Nurse P, Glover DM. twine, a cdc25 homolog that functions in the male and female germline of Drosophila. Cell. 1992;69(6):977-88.

Gottlin EB, Xu X, Epstein DM, Burke SP, Eckstein JW, Ballou DP, Dixon JE. Kinetic analysis of the catalytic domain of human cdc25B. J Biol Chem. 1996;271(44):27445-9.

Reynolds RA, Yem AW, Wolfe CL, Deibel MR, Jr., Chidester CG, Watenpaugh KD. Crystal structure of the catalytic subunit of Cdc25B required for G2/M phase transition of the cell cycle. J Mol Biol. 1999;293(3):559-68.

Bonnet J, Mayonove P, Morris MC. Differential phosphorylation of Cdc25C phosphatase in mitosis. Biochem Biophys Res Commun. 2008;370(3):483-8.

Baldin V, Cans C, Knibiehler M, Ducommun B. Phosphorylation of human CDC25B phosphatase by CDK1-cyclin A triggers its proteasome-dependent degradation. J Biol Chem. 1997;272(52):32731-4.

Pfleger CM, Kirschner MW. The KEN box: an APC recognition signal distinct from the D box targeted by Cdh1. Genes Dev. 2000;14(6):655-65.

Downloads

Published

2016-08-19

How to Cite

1.
Kang MK, Bang A, Choi HO, Han SJ. Comparative analysis of two murine CDC25B isoforms. Arch Biol Sci [Internet]. 2016Aug.19 [cited 2024Dec.22];69(1):35-44. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/340

Issue

Section

Articles