Transcriptional regulation of human polo-like kinases and early mitotic inhibitor

Moe Tategu; Hiroki Nakagawa; Kaori Sasaki; Rieko Yamauchi; Sota Sekimachi; Yuka Suita; Naoko Watanabe; Kenichi Yoshid

doi:10.1016/S1673-8527(08)60030-2

Volume 35 Issue 4

Apr. 2008

Turn off MathJax

Article Contents

Article Navigation > Journal of Genetics and Genomics > 2008 > 35(4): 215-224

PDF( 2036 KB)

Transcriptional regulation of human polo-like kinases and early mitotic inhibitor

doi: 10.1016/S1673-8527(08)60030-2

Department of Life Sciences, Meiji University School of Agriculture, 1-1-1 Higashimita, Tama-ku, Kawasaki, Kanagawa 214-8571, Japan

More Information

Corresponding author: E-mail address: yoshida@isc.meiji.ac.jp (Kenichi Yoshid)
Received Date: 2007-12-12
Accepted Date: 2008-01-09
Rev Recd Date: 2008-01-08

Available Online: 2008-04-24

Publish Date: 2008-04-20

Abstract

Abstract

Human polo-like kinases (PLK1–PLK4) have been implicated in mitotic regulation and carcinogenesis. PLK1 phosphorylates early mitotic inhibitor 1 (Emi1) to ensure mitosis entry, whereas Emi2 plays a key role during the meiotic cell cycle. Transcription factor E2F is primarily considered to regulate the G₁/S transition of the cell cycle but its involvement in the regulation of mitosis has also been recently suggested. A gap still exists between the molecular basis of E2F and mitotic regulation. The present study was designed to characterize the transcriptional regulation of human PLK and Emi genes. Adenoviral overexpression of E2F1 increased PLK1 and PLK3 mRNA levels in A549 cells. A reporter gene assay revealed that the putative promoter regions of PLK1, PLK3, and PLK4 genes were responsive to activators E2F, E2F1–E2F3. We further characterized the putative promoter regions of Emi1 and Emi2 genes, and these could be regulated by activators E2F and E2F1–E2F4, respectively. Finally, PLK1–PLK4, Emi1, and Emi2 mRNA expression levels in human adult, fetal tissues, and several cell lines indicated that each gene has a unique expression pattern but is uniquely expressed in common tissues and cells such as the testes and thymus. Collectively, these results indicate that E2F can integrate G₁/S and G₂/M to oscillate the cell cycle by regulating mitotic genes PLK and Emi, leading to determination of the cell fate.
- polo-like kinase,
- early mitotic inhibitor,
- cell cycle,
- E2F,
- promoter,
- gene regulation

FullText(HTML)

References(49)

References

[1]	Adams, P.D., Kaelin, W.G.J. The cellular effects of E2F overexpression Curr. Top. Microbiol. Immunol., 208 (1996),pp. 79-93
[2]	Agger, K., Santoni-Rugiu, E., Holmberg, C. et al. Conditional E2F1 activation in transgenic mice causes testicular atrophy and dysplasia mimicking human CIS Oncogene, 24 (2005),pp. 780-789
[3]	Barr, F.A., Silljé, H.H., Nigg, E.A. Polo-like kinases and the orchestration of cell division Nat. Rev. Mol. Cell Biol., 5 (2004),pp. 429-440
[4]	Bettencourt-Dias, M., Rodrigues-Martins, A., Carpenter, L. et al. SAK/PLK4 is required for centriole duplication and flagella development Curr. Biol., 15 (2005),pp. 2199-2207
[5]	Bräuninger, A., Strebhardt, K., Rübsamen-Waigmann, H. Identification and functional characterization of the human and murine polo-like kinase (Plk) promoter Oncogene, 11 (1995),pp. 1793-1800
[6]	Bracken, A.P., Ciro, M., Cocito, A. et al. E2F target genes: unraveling the biology Trends Biochem. Sci., 29 (2004),pp. 409-417
[7]	Eckerdt, F., Strebhardt, K. Polo-like kinase 1: target and regulator of anaphase-promoting complex/cyclosome-dependent proteolysis Cancer Res., 66 (2006),pp. 6895-6898
[8]	Field, S.J., Tsai, F.Y., Kuo, F. et al. E2F-1 functions in mice to promote apoptosis and suppress proliferation Cell, 85 (1996),pp. 549-561
[9]	Glover, D.M., Hagan, I.M., Tavares, A.A. Polo-like kinases: a team that plays throughout mitosis Genes Dev., 12 (1998),pp. 3777-3787
[10]	Golsteyn, R.M., Schultz, S.J., Bartek, J. et al. J. Cell Sci., 107 (1994),pp. 1509-1517
[11]	Goto, Y., Hayashi, R., Muramatsu, T. et al. JPO1/CDCA7, a novel transcription factor E2F1-induced protein, possesses intrinsic transcriptional regulator activity Biochim. Biophys. Acta, 1759 (2006),pp. 60-68
[12]	Gunawardena, R.W., Siddiqui, H., Solomon, D.A. et al. Hierarchical requirement of SWI/SNF in retinoblastoma tumor suppressor-mediated repression of Plk1 J. Biol. Chem., 279 (2004),pp. 29278-29285
[13]	Habedanck, R., Stierhof, Y.D., Wilkinson, C.J. et al. The Polo kinase Plk4 functions in centriole duplication Nat. Cell Biol., 7 (2005),pp. 1140-1146
[14]	Hansen, D.V., Loktev, A.V., Ban, K.H. et al. Plk1 regulates activation of the anaphase promoting complex by phosphorylating and triggering SCFbetaTrCP-dependent destruction of the APC Inhibitor Emi1 Mol. Biol. Cell, 15 (2004),pp. 5623-5634
[15]	Hsu, J.Y., Reimann, J.D., Sørensen, C.S. et al. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APC(Cdh1) Nat. Cell Biol., 4 (2002),pp. 358-366
[16]	Incassati, A., Patel, D., McCance, D.J. Induction of tetraploidy through loss of p53 and upregulation of Plk1 by human papillomavirus type-16 E6 Oncogene, 25 (2006),pp. 2444-2451
[17]	Kimura, M., Uchida, C., Takano, Y. et al. Cell cycle-dependent regulation of the human aurora B promoter Biochem. Biophys. Res. Commun., 316 (2004),pp. 930-936
[18]	Ko, M.A., Rosario, C.O., Hudson, J.W. et al. Plk4 haploinsufficiency causes mitotic infidelity and carcinogenesis Nat. Genet., 37 (2005),pp. 883-888
[19]	Liu, J., Grimison, B., Lewellyn, A.L. et al. The anaphase-promoting complex/cyclosome inhibitor Emi2 is essential for meiotic but not mitotic cell cycles J. Biol. Chem., 281 (2006),pp. 34736-34741
[20]	Llamazares, S., Moreira, A., Tavares, A. et al. Genes Dev., 5 (1991),pp. 2153-2165
[21]	Lukas, C., Sørensen, C.S., Kramer, E. et al. Accumulation of cyclin B1 requires E2F and cyclin-A-dependent rearrangement of the anaphase-promoting complex Nature, 401 (1999),pp. 815-818
[22]	Macaluso, M., Montanari, M., Cinti, C. et al. Modulation of cell cycle components by epigenetic and genetic events Semin. Oncol., 32 (2005),pp. 452-457
[23]	Martin, B.T., Strebhardt, K. Polo-like kinase 1: target and regulator of transcriptional control Cell Cycle, 5 (2006),pp. 2881-2885
[24]	Ohsumi, K., Koyanagi, A., Yamamoto, T.M. et al. Proc. Natl. Acad. Sci. USA, 101 (2004),pp. 12531-12536
[25]	Ohtani, K., Iwanaga, R., Nakamura, M. et al. Oncogene, 18 (1999),pp. 2299-2309
[26]	Olsson, A.Y., Feber, A., Edwards, S. et al. Role of E2F3 expression in modulating cellular proliferation rate in human bladder and prostate cancer cells Oncogene, 26 (2007),pp. 1028-1037
[27]	Reimann, J.D., Jackson, P.K. Emi1 is required for cytostatic factor arrest in vertebrate eggs Nature, 416 (2002),pp. 850-854
[28]	Reimann, J.D., Gardner, B.E., Margottin-Goguet, F. et al. Emi1 regulates the anaphase-promoting complex by a different mechanism than Mad2 proteins Genes Dev., 15 (2001),pp. 3278-3285
[29]	Reimann, J.D., Freed, E., Hsu, J.Y. et al. Emi1 is a mitotic regulator that interacts with Cdc20 and inhibits the anaphase promoting complex Cell, 105 (2001),pp. 645-655
[30]	Schmidt, A., Rauh, N.R., Nigg, E.A. et al. Cytostatic factor: an activity that puts the cell cycle on hold J. Cell Sci., 119 (2006),pp. 1213-1218
[31]	Shibuya, E.K., Masui, Y. Stabilization and enhancement of primary cytostatic factor (CSF) by ATP and NaF in amphibian egg cytosols Dev. Biol., 129 (1988),pp. 253-264
[32]	Smith, P., Syed, N., Crook, T. Epigenetic inactivation implies a tumor suppressor function in hematologic malignancies for Polo-like kinase 2 but not Polo-like kinase 3 Cell Cycle, 5 (2006),pp. 1262-1264
[33]	Suzuki, S., Adachi, A., Hiraiwa, A. et al. Gene, 216 (1998),pp. 85-91
[34]	Takai, N., Hamanaka, R., Yoshimatsu, J. et al. Polo-like kinases (Plks) and cancer Oncogene, 24 (2005),pp. 287-291
[35]	Toyoshima-Morimoto, F., Taniguchi, E., Shinya, N. et al. Polo-like kinase 1 phosphorylates cyclin B1 and targets it to the nucleus during prophase Nature, 410 (2001),pp. 215-220
[36]	Tsvetkov, L., Stern, D.F. Interaction of chromatin-associated Plk1 and Mcm7 J. Biol. Chem., 280 (2005),pp. 11943-11947
[37]	Tung, J.J., Hansen, D.V., Ban, K.H. et al. Proc. Natl. Acad. Sci. USA, 102 (2005),pp. 4318-4323
[38]	Uchiumi, T., Longo, D.L., Ferris, D.K. Cell cycle regulation of the human polo-like kinase (PLK) promoter J. Biol. Chem., 272 (1997),pp. 9166-9174
[39]	van de Weerdt, B.C., Medema, R.H. Polo-like kinases: a team in control of the division Cell Cycle, 5 (2006),pp. 853-864
[40]	Verschuren, E.W., Ban, K.H., Masek, M.A. et al. Loss of Emi1-dependent APC/C inhibition deregulates E2F target expression and elicits DNA damage-induced senescence Mol. Cell. Biol., 27 (2007),pp. 7955-7965
[41]	Wang, Q., Xie, S., Chen, J. et al. Cell cycle arrest and apoptosis induced by human Polo-like kinase 3 is mediated through perturbation of microtubule integrity Mol. Cell. Biol., 22 (2002),pp. 3450-3459
[42]	Warnke, S., Kemmler, S., Hames, R.S. et al. Polo-like kinase-2 is required for centriole duplication in mammalian cells Curr. Biol., 14 (2004),pp. 1200-1207
[43]	Winkles, J.A., Alberts, G.F. Differential regulation of polo-like kinase 1, 2, 3, and 4 gene expression in mammalian cells and tissues Oncogene, 24 (2005),pp. 260-266
[44]	Yamasaki, L., Jacks, T., Bronson, R. et al. Tumor induction and tissue atrophy in mice lacking E2F-1 Cell, 85 (1996),pp. 537-548
[45]	Yoshida, K., Inoue, I. Regulation of Geminin and Cdt1 expression by E2F transcription factors Oncogene, 23 (2004),pp. 3802-3812
[46]	Zhu, H., Chang, B.D., Uchiumi, T. et al. Identification of promoter elements responsible for transcriptional inhibition of polo-like kinase 1 and topoisomerase II alpha genes by p21(WAF1/CIP1/SDI1) Cell Cycle, 1 (2002),pp. 59-66
[47]	Zhu, W., Giangrande, P.H., Nevins, J.R. E2Fs link the control of G1/S and G2/M transcription EMBO J., 23 (2004),pp. 4615-4626
[48]	Zimmerman, W.C., Erikson, R.L. Polo-like kinase 3 is required for entry into S phase Proc. Natl. Acad. Sci. USA, 104 (2007),pp. 1847-1852
[49]	Zuber, J., Tchernitsa, O.I., Hinzmann, B. et al. A genome-wide survey of RAS transformation targets Nat. Genet., 24 (2000),pp. 144-152