Cancerous inhibitor of protein phosphatase 2A (CIP2A) protein is involved in centrosome separation through the regulation of NIMA (never in mitosis gene A)-related kinase 2 (NEK2) protein activity

Journal of Biological Chemistry

Volumn 289, Issue 1, 2014, Pages 28-40

  Jeong, Ae Lee ^a   Lee, Sunyi ^a   Park, Jeong Su ^a   Han, Sora ^a   Jang, Chang Young ^a   Lim, Jong Seok ^a   Lee, Myung Sok ^a   Yang, Young ^a  

^a Sookmyung Women's University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROLIFERATION; CYTOLOGY; ENZYMES; GENES; PROTEINS;

BINDING PARTNERS; CELLULAR FUNCTION; CO-IMMUNOPRECIPITATION ASSAYS; HUMAN MALIGNANCIES; PROTEIN ACTIVITY; PROTEIN PHOSPHATASE 2A; SPINDLE-ASSEMBLY; YEAST TWO HYBRID;

SEPARATION;

CANCEROUS INHIBITOR OF PROTEIN PHOSPHATASE 2A; NEVER IN MITOSIS GENE A RELATED KINASE 2; ONCOPROTEIN; PROTEIN SERINE THREONINE KINASE; UNCLASSIFIED DRUG; AUTOANTIGEN; KIAA1524 PROTEIN, HUMAN; KIAA1524 PROTEIN, MOUSE; MEMBRANE PROTEIN; NEK2 PROTEIN, HUMAN; NEK2 PROTEIN, MOUSE; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2;

ARTICLE; CELL CYCLE CHECKPOINT; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL DIVISION; CELL SEPARATION; CENTROSOME; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME LOCALIZATION; IMMUNOPRECIPITATION; INTRACELLULAR SIGNALING; MITOSIS SPINDLE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; ANIMAL; CYTOPLASM; GENETICS; HEK293 CELL LINE; HELA CELL LINE; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; SIGNAL TRANSDUCTION; TWO HYBRID SYSTEM;

ANIMALS; AUTOANTIGENS; CELL CYCLE CHECKPOINTS; CELL DIVISION; CENTROSOME; CYTOPLASM; G2 PHASE; HEK293 CELLS; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; PROTEIN PHOSPHATASE 1; PROTEIN PHOSPHATASE 2; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84891676480     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.507954     Document Type: Article

References (66)

1. Kikuno, R., Nagase, T., Ishikawa, K., Hirosawa, M., Miyajima, N., Tanaka, A., Kotani, H., Nomura, N., and Ohara, O. (1999) Prediction of the coding sequences of unidentified human genes. XIV. The complete sequences of 100 new cDNA clones from brain which code for large proteins in vitro. DNA Res. 6, 197-205 (Pubitemid 129705079)
2. Wang, L., Gu, F., Ma, N., Zhang, L., Bian, J. M., and Cao, H. Y. (2013) CIP2A expression is associated with altered expression of epithelial-mesenchymal transition markers and predictive of poor prognosis in pancreatic ductal adenocarcinoma. Tumour Biol. 34, 2309-2313
3. Li, W., Ge, Z., Liu, C., Liu, Z., Björkholm, M., Jia, J., and Xu, D. (2008) CIP2A is overexpressed in gastric cancer and its depletion leads to impaired clonogenicity, senescence, or differentiation of tumor cells. Clin. Cancer Res. 14, 3722-3728
4. Khanna, A., Böckelman, C., Hemmes, A., Junttila, M. R., Wiksten, J. P., Lundin, M., Junnila, S., Murphy, D. J., Evan, G. I., Haglund, C., Westermarck, J., and Ristimäki, A. (2009) MYC-dependent regulation and prognostic role of CIP2A in gastric cancer. J. Natl. Cancer Inst. 101, 793-805
5. Côme, C., Laine, A., Chanrion, M., Edgren, H., Mattila, E., Liu, X., Jonkers, J., Ivaska, J., Isola, J., Darbon, J. M., Kallioniemi, O., Thézenas, S., and Westermarck, J. (2009) CIP2A is associated with human breast cancer aggressivity. Clin. Cancer Res. 15, 5092-5100
6. Niemelä, M., Kauko, O., Sihto, H., Mpindi, J. P., Nicorici, D., Pernilä, P., Kallioniemi, O. P., Joensuu, H., Hautaniemi, S., and Westermarck, J. (2012) CIP2A signature reveals the MYC dependency of CIP2A-regulated phenotypes and its clinical association with breast cancer subtypes. Oncogene 31, 4266-4278
7. Huang, L. P., Adelson, M. E., Mordechai, E., and Trama, J. P. (2010) CIP2A expression is elevated in cervical cancer. Cancer Biomark. 8, 309-317
8. Liu, J., Wang, X., Zhou, G., Wang, H., Xiang, L., Cheng, Y., Liu, W., Wang, Y., Jia, J., and Zhao, W. (2011) Cancerous inhibitor of protein phosphatase 2A is overexpressed in cervical cancer and upregulated by human papillomavirus 16 E7 oncoprotein. Gynecol. Oncol. 122, 430-436
9. Dong, Q. Z., Wang, Y., Dong, X. J., Li, Z. X., Tang, Z. P., Cui, Q. Z., and Wang, E. H. (2011) CIP2A is overexpressed in non-small cell lung cancer and correlates with poor prognosis. Ann. Surg. Oncol. 18, 857-865
10. Katz, J., Jakymiw, A., Ducksworth, M. K., Stewart, C. M., Bhattacharyya, I., Cha, S., and Chan, E. K. (2010) CIP2A expression and localization in oral carcinoma and dysplasia. Cancer Biol. Ther. 10, 694-699
11. Vaarala, M. H., Väisänen, M. R., and Ristimäki, A. (2010) CIP2A expression is increased in prostate cancer. J. Exp. Clin. Cancer Res. 29, 136
12. Qu, W., Li, W., Wei, L., Xing, L., Wang, X., and Yu, J. (2012) CIP2A is overexpressed in esophageal squamous cell carcinoma. Med. Oncol 29, 113-118
13. Coenen, E. A., Zwaan, C. M., Meyer, C., Marschalek, R., Pieters, R., Van Der Veken, L. T., Beverloo, H. B., and Van Den Heuvel-Eibrink, M. M. (2011) KIAA1524. Anovel MLL translocation partner inacute myeloid leukemia. Leuk. Res. 35, 133-135
14. Wang, J., Li, W., Li, L., Yu, X., Jia, J., and Chen, C. (2011) CIP2A is overexpressed in acute myeloid leukaemia and associated with HL60 cells proliferation and differentiation. Int. J. Lab. Hematol. 33, 290-298
15. Böckelman, C., Lassus, H., Hemmes, A., Leminen, A., Westermarck, J., Haglund, C., Bützow, R., and Ristimäki, A. (2011) Prognostic role of CIP2A expression in serous ovarian cancer. Br. J. Cancer 105, 989-995
16. Böckelman, C., Hagström, J., Mäkinen, L. K., Keski-Säntti, H., Häyry, V., Lundin, J., Atula, T., Ristimäki, A., and Haglund, C. (2011) High CIP2A immunoreactivity is an independent prognostic indicator in early-stage tongue cancer. Br. J. Cancer 104, 1890-1895
17. Fang, Y., Li, Z., Wang, X., and Zhang, S. (2012) CIP2A is overexpressed in human ovarian cancer and regulates cell proliferation and apoptosis. Tumour. Biol. 33, 2299-2306
18. Ren, J., Li, W., Yan, L., Jiao, W., Tian, S., Li, D., Tang, Y., Gu, G., Liu, H., and Xu, Z. (2011) Expression of CIP2A in renal cell carcinomas correlates with tumour invasion, metastasis and patients' survival. Br. J. Cancer 105, 1905-1911
19. Lin, Y. C., Chen, K. C., Chen, C. C., Cheng, A. L., and Chen, K. F. (2012) CIP2A-mediated Akt activation plays a role in bortezomib-induced apoptosis in head and neck squamous cell carcinoma cells. Oral Oncol. 48, 585-593
20. Teng, H. W., Yang, S. H., Lin, J. K., Chen, W. S., Lin, T. C., Jiang, J. K., Yen, C. C., Li, A. F., Chen, P. C., Lan, Y. T., Lin, C. C., Hsu, Y. N., Wang, H. W., and Chen, K. F. (2012) CIP2A is a predictor of poor prognosis in colon cancer. J. Gastrointest. Surg. 16, 1037-1047
21. He, H., Wu, G., Li, W., Cao, Y., and Liu, Y. (2012) CIP2A is highly expressed in hepatocellular carcinoma and predicts poor prognosis. Diagn. Mol. Pathol. 21, 143-149
22. Huang, L. P., Savoly, D., Sidi, A. A., Adelson, M. E., Mordechai, E., and Trama, J. P. (2012) CIP2A protein expression in high-grade, high-stage bladder cancer. Cancer Med. 1, 76-81
23. Huang, P., Qiu, J., You, J., Hong, J., Li, B., Zhou, K., Chen, G., Yuan, Y., and Zou, R. (2012) Expression and prognostic significance of CIP2A mRNA in hepatocellular carcinoma and nontumoral liver tissues. Biomarkers 17, 422-429
24. Xue, Y., Wu, G., Wang, X., Zou, X., Zhang, G., Xiao, R., Yuan, Y., Long, D., Yang, J., Wu, Y., Xu, H., Liu, F., and Liu, M. (2013) CIP2A is a predictor of survival and a novel therapeutic target in bladder urothelial cell carcinoma. Med. Oncol. 30, 406
25. Yi, F., Ni, W., Liu, W., Bai, J., and Li, W. (2013) Expression and biological role of CIP2A in human astrocytoma. Mol. Med. Rep. 7, 1376-1380
26. Khanna, A., Okkeri, J., Bilgen, T., Tiirikka, T., Vihinen, M., Visakorpi, T., and Westermarck, J. (2011) ETS1 mediates MEK1/2-dependent overexpression of cancerous inhibitor of protein phosphatase 2A (CIP2A) in human cancer cells. PLoS ONE 6, e17979
27. Laine, A., Sihto, H., Come, C., Rosenfeldt, M. T., Zwolinska, A., Niemela, M., Khanna, A., Chan, E. K., Kahari, V. M., Kellokumpu-Lehtinen, P. L., Sansom, O. J., Evan, G. I., Junttila, M. R., Ryan, K. M., Marine, J. C., Joensuu, H., and Westermarck, J. (2013) Senescence Sensitivity of Breast Cancer Cells Is Defined by Positive Feedback Loop between CIP2A and E2F1. Cancer Discov. 3, 182-197
28. Junttila, M. R., Puustinen, P., Niemelä, M., Ahola, R., Arnold, H., Böttzauw, T., Ala-aho, R., Nielsen, C., Ivaska, J., Taya, Y., Lu, S. L., Lin, S., Chan, E. K., Wang, X. J., Grènman, R., Kast, J., Kallunki, T., Sears, R., Kähäri, V. M., and Westermarck, J. (2007) CIP2A inhibits PP2A in human malignancies. Cell 130, 51-62 (Pubitemid 47039258)
29. Ma, L., Wen, Z. S., Liu, Z., Hu, Z., Ma, J., Chen, X. Q., Liu, Y. Q., Pu, J. X., Xiao, W. L., Sun, H. D., and Zhou, G. B. (2011) Overexpression and small molecule-triggered downregulation of CIP2A in lung cancer. PLoS ONE 6, e20159
30. Mathiasen, D. P., Egebjerg, C., Andersen, S. H., Rafn, B., Puustinen, P., Khanna, A., Daugaard, M., Valo, E., Tuomela, S., Bøttzauw, T., Nielsen, C. F., Willumsen, B. M., Hautaniemi, S., Lahesmaa, R., Westermarck, J., Jäättelä, M., and Kallunki, T. (2012) Identification of a c-Jun. N-terminal kinase-2-dependent signal amplification cascade that regulates c-Myc levels in ras transformation. Oncogene 31, 390-401
31. Böckelman, C., Koskensalo, S., Hagström, J., Lundin, M., Ristimäki, A., and Haglund, C. (2012) CIP2A overexpression is associated with c-Myc expression in colorectal cancer. Cancer Biol. Ther. 13, 289-295
32. Müller, D., Bouchard, C., Rudolph, B., Steiner, P., Stuckmann, I., Saffrich, R., Ansorge, W., Huttner, W., and Eilers, M. (1997) Cdk2-dependent phosphorylation of p27 facilitates its Myc-induced release from cyclin E/cdk2 complexes. Oncogene 15, 2561-2576 (Pubitemid 27507248)
33. Pérez-Roger, I., Solomon, D. L., Sewing, A., and Land, H. (1997) Myc activation of cyclin E/Cdk2 kinase involves induction of cyclin E gene transcription and inhibition of p27 (Kip1) binding to newly formed complexes. Oncogene 14, 2373-2381 (Pubitemid 27268156)
34. Ha Kim, Y., Yeol Choi, J., Jeong, Y., Wolgemuth, D. J., and Rhee, K. (2002) Nek2 localizes to multiple sites in mitotic cells, suggesting its involvement in multiple cellular functions during the cell cycle. Biochem. Biophys. Res. Commun. 290, 730-736 (Pubitemid 34687501)
35. Fry, A. M., Meraldi, P., and Nigg, E. A. (1998) A centrosomal function for the human Nek2 protein kinase, a member of the NIMA family of cell cycle regulators. EMBOJ. 17, 470-481 (Pubitemid 28045488)
36. Andersen, J. S., Wilkinson, C. J., Mayor, T., Mortensen, P., Nigg, E. A., and Mann, M. (2003) Proteomic characterization of the human centrosome by protein correlation profiling. Nature 426, 570-574 (Pubitemid 37522644)
37. Fry, A. M., Mayor, T., Meraldi, P., Stierhof, Y. D., Tanaka, K., and Nigg, E. A. (1998) C-Nap1, a novel centrosomal coiled-coil protein and candidate substrate of the cell cycle-regulated protein kinase Nek2. J. Cell Biol. 141, 1563-1574 (Pubitemid 28309171)
38. Faragher, A. J., and Fry, A. M. (2003) Nek2A kinase stimulates centrosome disjunction and is required for formation of bipolar mitotic spindles. Mol. Biol. Cell 14, 2876-2889 (Pubitemid 36871528)
39. Mayor, T., Hacker, U., Stierhof, Y. D., and Nigg, E. A. (2002) The mechanism regulating the dissociation of the centrosomal protein C-Nap1 from mitotic spindle poles. J. Cell Sci. 115, 3275-3284 (Pubitemid 34960180)
40. Bahe, S., Stierhof, Y. D., Wilkinson, C. J., Leiss, F., and Nigg, E. A. (2005) Rootletin forms centriole-associated filaments and functions in centrosome cohesion. J. Cell Biol. 171, 27-33 (Pubitemid 41434599)
41. Bahmanyar, S., Kaplan, D. D., Deluca, J. G., Giddings, T. H., Jr., O'Toole, E. T., Winey, M., Salmon, E. D., Casey, P. J., Nelson, W. J., and Barth, A. I. (2008) β-Catenin is a Nek2 substrate involved in centrosome separation. Genes Dev. 22, 91-105
42. Rhee, K., and Wolgemuth, D. J. (1997) The NIMA-related kinase 2, Nek2, is expressed in specific stages of the meiotic cell cycle and associates with meiotic chromosomes. Development 124, 2167-2177 (Pubitemid 27283238)
43. Sonn, S., Khang, I., Kim, K., and Rhee, K. (2004) Suppression of Nek2A in mouse early embryos confirms its requirement for chromosome segregation. J. Cell Sci. 117, 5557-5566 (Pubitemid 40012202)
44. Jeong, Y., Lee, J., Kim, K., Yoo, J. C, and Rhee, K. (2007) Characterization of NIP2/centrobin, a novel substrate of Nek2, and its potential role in microtubule stabilization. J. Cell Sci. 120, 2106-2116 (Pubitemid 47010005)
45. Park, J., and Rhee, K. (2013) NEK2 phosphorylation antagonizes the microtubule stabilizing activity of centrobin. Biochem. Biophys. Res. Commun. 431, 302-308
46. Wei, R., Ngo, B., Wu, G., and Lee, W. H. (2011) Phosphorylation of the Ndc80 complex protein, HEC1, by Nek2 kinase modulates chromosome alignment and signaling of the spindle assembly checkpoint. Mol. Biol. Cell 22, 3584-3594
47. Chen, Y., Riley, D. J., Zheng, L., Chen, P. L., and Lee, W. H. (2002) Phosphorylation of the mitotic regulator protein Hec1 by Nek2 kinase is essential for faithful chromosome segregation. J. Biol. Chem. 277, 49408-49416 (Pubitemid 36014374)
48. Du, J., Cai, X., Yao, J., Ding, X., Wu, Q., Pei, S., Jiang, K., Zhang, Y., Wang, W., Shi, Y., Lai, Y., Shen, J., Teng, M., Huang, H., Fei, Q., Reddy, E. S., Zhu, J., Jin, C, and Yao, X. (2008) The mitotic checkpoint kinase NEK2A regulates kinetochore microtubule attachment stability. Oncogene 27, 4107-4114 (Pubitemid 351931984)
49. Mardin, B. R., Lange, C., Baxter, J. E., Hardy, T., Scholz, S. R., Fry, A. M., and Schiebel, E. (2010) Components of the Hippo pathway cooperate with Nek2 kinase to regulate centrosome disjunction. Nat. CellBiol. 12, 1166-1176
50. Mardin, B. R., Isokane, M., Cosenza, M. R., Krämer, A., Ellenberg, J., Fry, A. M., and Schiebel, E. (2013) EGF-induced centrosome separation promotes mitotic progression and cell survival. Dev. Cell 25, 229-240
51. Choi, Y. A., Park, J. S., Park, M. Y., Oh, K. S., Lee, M. S., Lim, J. S., Kim, K. I., Kim, K. Y., Kwon, J., Yoon Do, Y., Moon, E. Y., and Yang, Y. (2011) Increase in CIP2A expression is associated with doxorubicin resistance. FEBS Lett. 585, 755-760
52. Fry, A. M., Arnaud, L., and Nigg, E. A. (1999) Activity of the human centrosomal kinase, Nek2, depends on an unusual leucine zipper dimerization motif. J. Biol. Chem. 274, 16304-16310
53. Helps, N. R., Luo, X., Barker, H. M., and Cohen, P. T. (2000) NIMA-related kinase 2 (Nek2), a cell-cycle-regulated protein kinase localized to centrosomes, is complexed to protein phosphatase 1. Biochem. J. 349, 509-518 (Pubitemid 30465786)
54. Meraldi, P., and Nigg, E. A. (2001) Centrosome cohesion is regulated by a balance of kinase and phosphatase activities. J. Cell Sci. 114, 3749-3757 (Pubitemid 33041056)
55. Mi, J., Guo, C., Brautigan, D. L., and Larner, J. M. (2007) Protein phosphatase-1 α regulates centrosome splitting through Nek2. Cancer Res. 67, 1082-1089
56. Rellos, P., Ivins, F. J., Baxter, J. E., Pike, A., Nott, T. J., Parkinson, D. M., Das, S., Howell, S., Fedorov, O., Shen, Q. Y., Fry, A. M., Knapp, S., and Smerdon, S. J. (2007) Structure and regulation of the human Nek2 centrosomal kinase. J. Biol. Chem. 282, 6833-6842 (Pubitemid 47100894)
57. Westwood, I., Cheary, D. M., Baxter, J. E., Richards, M. W., Van Montfort, R. L., Fry, A. M., and Bayliss, R. (2009) Insights into the conformational variability and regulation of human Nek2 kinase. J. Mol. Biol. 386, 476-485
58. Hames, R. S., and Fry, A. M. (2002) Alternative splice variants of the human centrosome kinase Nek2 exhibit distinct patterns of expression in mitosis. Biochem. J. 361, 77-85 (Pubitemid 34171411)
59. Fletcher, L., Cerniglia, G. J., Yen, T. J., and Muschel, R. J. (2005) Live cell imaging reveals distinct roles in cell cycle regulation for Nek2A and Nek2B. Biochim. Biophys. Acta 1744, 89-92 (Pubitemid 40798919)
60. Silkworth, W. T., Nardi, I. K., Paul, R., Mogilner, A., and Cimini, D. (2012) Timing of centrosome separation is important for accurate chromosome segregation. Mol. Biol. Cell 23, 401-411
61. Zhou, W., Yang, Y., Xia, J., Wang, H., Salama, M. E., Xiong, W., Xu, H., Shetty, S., Chen, T., Zeng, Z., Shi, L., Zangari, M., Miles, R., Bearss, D., Tricot, G., and Zhan, F. (2013) NEK2 induces drug resistance mainly through activation of efflux drug pumps and is associated with poor prognosis in myeloma and other cancers. Cancer Cell 23, 48-62
62. Haering, C. H., and Nasmyth, K. (2003) Building and breaking bridges between sister chromatids. BioEssays 25, 1178-1191 (Pubitemid 37499318)
63. Hirano, T. (2006) At the heart of the chromosome: SMC proteins in action. Nat Rev. Mol. CellBiol. 7, 311-322
64. Thadani, R., Uhlmann, F., and Heeger, S. (2012) Condensin, chromatin crossbarring and chromosome condensation. Curr. Biol. 22, R1012-1021
65. Flory, M. R., Carson, A. R., Muller, E. G., and Aebersold, R. (2004) An SMC-domain protein in fission yeast links telomeres to the meiotic centrosome. Mol. Cell 16, 619-630 (Pubitemid 39531884)
66. Ventelä, S., Côme, C., Mäkelä, J. A., Hobbs, R. M., Mannermaa, L., Kallajoki, M., Chan, E. K., Pandolfi, P. P., Toppari, J., and Westermarck, J. (2012) CIP2A promotes proliferation of spermatogonial progenitor cells and spermatogenesis in mice. PLoS ONE 7, e33209