CHFR protein regulates mitotic checkpoint by targeting PARP-1 protein for ubiquitination and degradation

Journal of Biological Chemistry

Volumn 287, Issue 16, 2012, Pages 12975-12984

  Kashima, Lisa ^a,c   Idogawa, Masashi ^a   Mita, Hiroaki ^a   Shitashige, Miki ^b   Yamada, Tesshi ^b   Ogi, Kazuhiro ^a   Suzuki, Hiromu ^a   Toyota, Minoru ^a   Ariga, Hiroyoshi ^c   Sasaki, Yasushi ^a   Tokino, Takashi ^a  

^a SAPPORO MEDICAL UNIVERSITY   (Japan)

^b NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AFFINITY PURIFICATION; CANCER CELLS; CELL CYCLE REGULATION; CELL-CYCLE ARREST; CELL-CYCLE PROGRESSION; GASTRIC CANCERS; HUMAN CANCER; HYPERMETHYLATION; KNOCKOUT MICE; MICROTUBULES; PARP-INHIBITOR; POLY POLYMERASE; POLYUBIQUITINATION; PROTEIN LEVEL; RING FINGER; STRESS-INDUCED; TARGET PROTEINS; THERAPEUTIC STRATEGY; TUMOR SUPPRESSORS; TUMORIGENESIS; UBIQUITIN LIGASES; UBIQUITINATION;

CELLS; CHEMOTHERAPY; CYTOLOGY; DEGRADATION; DISEASES; GENES; MASS SPECTROMETRY; TISSUE;

PROTEINS;

CHFR PROTEIN; MICROTUBULE INHIBITOR; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; PROTEIN INHIBITOR; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CYCLE ARREST; CELL STRESS; CONTROLLED STUDY; DRUG RESISTANCE; EMBRYO; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; M PHASE CELL CYCLE CHECKPOINT; MASS SPECTROMETRY; MICROTUBULE; MITOTIC STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROPHASE; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STOMACH CANCER; UBIQUITINATION;

ANIMALS; BREAST NEOPLASMS; CARCINOMA, NON-SMALL-CELL LUNG; CELL CYCLE CHECKPOINTS; DRUG DESIGN; FEMALE; GENES, TUMOR SUPPRESSOR; HEK293 CELLS; HELA CELLS; HUMANS; LUNG NEOPLASMS; M PHASE CELL CYCLE CHECKPOINTS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULES; MOUTH NEOPLASMS; NEOPLASMS; NEOPLASMS, SQUAMOUS CELL; POLY(ADP-RIBOSE) POLYMERASES; STOMACH NEOPLASMS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

MUS;

EID: 84859766576     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.321828     Document Type: Article

References (33)

1. Yu, X., Minter-Dykhouse, K., Malureanu, L., Zhao, W. M., Zhang, D., Merkle, C. J., Ward, I. M., Saya, H., Fang, G., van Deursen, J., and Chen, J. (2005) CHFR is required for tumor suppression and Aurora A regulation. Nat. Genet. 37, 401-406
2. Toyota, M., Sasaki, Y., Satoh, A., Ogi, K., Kikuchi, T., Suzuki, H., Mita, H., Tanaka, N., Itoh, F., Issa, J. P., Jair, K. W., Schuebel, K. E., Imai, K., and Tokino, T. (2003) Epigenetic inactivation of CHFR in human tumors. Proc. Natl. Acad. Sci. U.S.A. 100, 7818-7823 (Pubitemid 36760053)
3. Privette, L. M., and Petty, E. M. (2008) CHFR. A novel mitotic checkpoint protein and regulator of tumorigenesis. Transl. Oncol. 1, 57-64
4. Scolnick, D. M., and Halazonetis, T. D. (2000) CHFR defines a mitotic stress checkpoint that delays entry into metaphase. Nature 406, 430-435 (Pubitemid 30625565)
5. Kashima, L., Toyota, M., Mita, H., Suzuki, H., Idogawa, M., Ogi, K., Sasaki, Y., and Tokino, T. (2009) CHFR, a potential tumor suppressor, downregulates interleukin-8 through the inhibition of NF-κB. Oncogene 28, 2643-2653
6. Chaturvedi, P., Sudakin, V., Bobiak, M. L., Fisher, P. W., Mattern, M. R., Jablonski, S. A., Hurle, M. R., Zhu, Y., Yen, T. J., and Zhou, B. B. (2002) CHFR regulates a mitotic stress pathway through its RING finger domain with ubiquitin ligase activity. Cancer Res. 62, 1797-1801 (Pubitemid 34408505)
7. Kang, D., Chen, J., Wong, J., and Fang, G. (2002) The checkpoint protein CHFR is a ligase that ubiquitinates Plk1 and inhibits Cdc2 at the G2 to M transition. J. Cell Biol. 156, 249-259 (Pubitemid 34839907)
8. Bothos, J., Summers, M. K., Venere, M., Scolnick, D. M., and Halazonetis, T. D. (2003) The CHFR mitotic checkpoint protein functions with Ubc13-Mms2 to form Lys-63-linked polyubiquitin chains. Oncogene 22, 7101-7107 (Pubitemid 37378542)
9. Ahel, I., Ahel, D., Matsusaka, T., Clark, A. J., Pines, J., Boulton, S. J., and West, S. C. (2008) Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451, 81-85
10. Schreiber, V., Dantzer, F., Ame, J. C., and de Murcia, G. (2006) Poly(ADP-ribose). Novel functions for an old molecule. Nat. Rev. Mol. Cell Biol. 7, 517-528 (Pubitemid 44036457)
11. Bièche, I., de Murcia, G., and Lidereau, R. (1996) Poly(ADP-ribose) polymerase gene expression status and genomic instability in human breast cancer. Clin. Cancer Res. 2, 1163-1167 (Pubitemid 26238447)
12. Soldatenkov, V. A., Albor, A., Patel, B. K., Dreszer, R., Dritschilo, A., and Notario, V. (1999) Regulation of the human poly(ADP-ribose) polymerase promoter by the ETS transcription factor. Oncogene 18, 3954-3962 (Pubitemid 29361333)
13. Tomoda, T., Kurashige, T., Moriki, T., Yamamoto, H., Fujimoto, S., and Taniguchi, T. (1991) Enhanced expression of poly(ADP-ribose) synthetase gene in malignant lymphoma. Am. J. Hematol. 37, 223-227
14. Idogawa, M., Masutani, M., Shitashige, M., Honda, K., Tokino, T., Shinomura, Y., Imai, K., Hirohashi, S., and Yamada, T. (2007) Ku70 and poly- (ADP-ribose) polymerase-1 competitively regulate β-catenin and T-cell factor 4-mediated gene transactivation. Possible linkage of DNA damage recognition and Wnt signaling. Cancer Res. 67, 911-918
15. Shimizu, S., Nomura, F., Tomonaga, T., Sunaga, M., Noda, M., Ebara, M., and Saisho, H. (2004) Expression of poly(ADP-ribose) polymerase in human hepatocellular carcinoma and analysis of biopsy specimens obtained under sonographic guidance. Oncol. Rep. 12, 821-825
16. Rouleau, M., Patel, A., Hendzel, M. J., Kaufmann, S. H., and Poirier, G. G. (2010) PARP inhibitor: PARP1 and beyond. Nat. Rev. Cancer 10, 293-301
17. Idogawa, M., Yamada, T., Honda, K., Sato, S., Imai, K., and Hirohashi, S. (2005) Poly(ADP-ribose) polymerase-1 is a component of the oncogenic T-cell factor-4/β-catenin complex. Gastroenterology 128, 1919-1936 (Pubitemid 40824703)
18. Kawasaki, T., Ohnishi, M., Nosho, K., Suemoto, Y., Kirkner, G. J., Meyerhardt, J. A., Fuchs, C. S., and Ogino, S. (2008) CpG island methylator phenotype-low (CIMP-low) colorectal cancer shows not only few methylated CIMP-high-specific CpG islands, but also low-level methylation at individual loci. Mod. Pathol. 21, 245-255 (Pubitemid 351304277)
19. Igarashi, S., Suzuki, H., Niinuma, T., Shimizu, H., Nojima, M., Iwaki, H., Nobuoka, T., Nishida, T., Miyazaki, Y., Takamaru, H., Yamamoto, E., Yamamoto, H., Tokino, T., Hasegawa, T., Hirata, K., Imai, K., Toyota, M., and Shinomura, Y. (2010) A novel correlation between LINE-1 hypomethylation and the malignancy of gastrointestinal stromal tumors. Clin. Cancer Res. 16, 5114-5123
20. Weisenberger, D. J., Siegmund, K. D., Campan, M., Young, J., Long, T. I., Faasse, M. A., Kang, G. H., Widschwendter, M., Weener, D., Buchanan, D., Koh, H., Simms, L., Barker, M., Leggett, B., Levine, J., Kim, M., French, A. J., Thibodeau, S. N., Jass, J., Haile, R., and Laird, P. W. (2006) CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat. Genet. 38, 787-793 (Pubitemid 43980599)
21. Ogi, K., Toyota, M., Mita, H., Satoh, A., Kashima, L., Sasaki, Y., Suzuki, H., Akino, K., Nishikawa, N., Noguchi, M., Shinomura, Y., Imai, K., Hiratsuka, H., and Tokino, T. (2005) Small interfering RNA-induced CHFR silencing sensitizes oral squamous cell cancer cells to microtubule inhibitors. Cancer Biol. Ther. 4, 773-780 (Pubitemid 41351179)
22. Martin, N., Schwamborn, K., Schreiber, V., Werner, A., Guillier, C., Zhang, X. D., Bischof, O., Seeler, J. S., and Dejean, A. (2009) PARP-1 transcriptional activity is regulated by sumoylation upon heat shock. EMBO J. 28, 3534-3548
23. Wang, T., Simbulan-Rosenthal, C. M., Smulson, M. E., Chock, P. B., and Yang, D. C. (2008) Polyubiquitylation of PARP-1 through ubiquitin K48 is modulated by activated DNA, NAD+, and dipeptides. J. Cell. Biochem. 104, 318-328
24. Bunz, F., Hwang, P. M., Torrance, C., Waldman, T., Zhang, Y., Dillehay, L., Williams, J., Lengauer, C., Kinzler, K. W., and Vogelstein, B. (1999) Disruption of p53 in human cancer cells alters the responses to therapeutic agents. J. Clin. Invest. 104, 263-269
25. Suzuki, H., Itoh, F., Toyota, M., Kikuchi, T., Kakiuchi, H., and Imai, K. (2000) Inactivation of the 14-3-3 sigma gene is associated with 5′ CpG island hypermethylation in human cancers. Cancer Res. 60, 4353-4357 (Pubitemid 32103610)
26. Satoh, A., Toyota, M., Itoh, F., Sasaki, Y., Suzuki, H., Ogi, K., Kikuchi, T., Mita, H., Yamashita, T., Kojima, T., Kusano, M., Fujita, M., Hosokawa, M., Endo, T., Tokino, T., and Imai, K. (2003) Epigenetic inactivation of CHFR and sensitivity to microtubule inhibitors in gastric cancer. Cancer Res. 63, 8606-8613 (Pubitemid 38064034)
27. Tentori, L., Muzi, A., Dorio, A. S., Scarsella, M., Leonetti, C., Shah, G. M., Xu, W., Camaioni, E., Gold, B., Pellicciari, R., Dantzer, F., Zhang, J., and Graziani, G. (2010) Pharmacological inhibition of poly(ADP-ribose) polymerase (PARP) activity in PARP-1 silenced tumour cells increases chemosensitivity to temozolomide and to a N3-adenine selective methylating agent. Curr. Cancer Drug Targets 10, 368-383
28. Wesierska-Gadek, J., Schloffer, D., Gueorguieva, M., Uhl, M., and Skladanowski, A. (2004) Increased susceptibility of poly(ADP-ribose) polymerase- 1 knockout cells to antitumor triazoloacridone C-1305 is associated with permanent G2 cell cycle arrest. Cancer Res. 64, 4487-4497 (Pubitemid 38856920)
29. Tanuma, S., and Kanai, Y. (1982) Poly(ADP-ribosyl)ation of chromosomal proteins in the HeLa S3 cell cycle. J. Biol. Chem. 257, 6565-6570
30. Saxena, A., Saffery, R., Wong, L. H., Kalitsis, P., and Choo, K. H. (2002) Centromere proteins Cenpa, Cenpb, and Bub3 interact with poly(ADP-ribose) polymerase-1 protein and are poly(ADP-ribosyl)ated. J. Biol. Chem. 277, 26921-26926 (Pubitemid 34951701)
31. Chang, P., Jacobson, M. K., and Mitchison, T. J. (2004) Poly(ADP-ribose) is required for spindle assembly and structure. Nature 432, 645-649 (Pubitemid 39626273)
32. Miwa, M., and Masutani, M. (2007) PolyADP-ribosylation and cancer. Cancer Sci. 98, 1528-1535 (Pubitemid 47308446)
33. Annunziata, C. M., and O'Shaughnessy, J. (2010) Poly (ADP-ribose) polymerase as a novel therapeutic target in cancer. Clin. Cancer Res. 16, 4517-4526