Fez1/Lzts1 Absence Impairs Cdk1/Cdc25C Interaction during Mitosis and Predisposes Mice to Cancer Development

Cancer Cell

Volumn 11, Issue 3, 2007, Pages 275-289

  Vecchione, Andrea ^a,b   Baldassarre, Gustavo ^c   Ishii, Hideshi ^d   Nicoloso, Milena S ^a,c   Belletti, Barbara ^c   Petrocca, Fabio ^a   Zanesi, Nicola ^a   Fong, Louise Y Y ^a   Battista, Sabrina ^f   Guarnieri, Daniela ^e   Baffa, Raffaele ^g   Alder, Hansjuerg ^a   Farber, John L ^g   Donovan, Peter J ^h   Croce, Carlo M ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c CENTRO DI RIFERIMENTO ONCOLOGICO   (Italy)

^d JICHI MEDICAL UNIVERSITY   (Japan)

^e UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^f CNR   (Italy)

^g THOMAS JEFFERSON UNIVERSITY   (United States)

^h JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cdc2; CdC25C; Fez1 Lzts1; Knockout mice; NMBA

Indexed keywords

CARCINOGEN; CELL CYCLE PROTEIN; CELL DIVISION CYCLE PROTEIN 25 C; CYCLIN DEPENDENT KINASE 1; FASCICULATION AND ELONGATION PROTEIN ZETA 1; LEUCINE ZIPPER PROTEIN; LEUCINE ZIPPER TUMOR SUPPRESSOR PROTEIN; NOCODAZOLE; PACLITAXEL; PROTEIN DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CHROMOSOME SEGREGATION; EMBRYO; ENZYME ACTIVITY; FIBROBLAST; INCIDENCE; KNOCKOUT MOUSE; MALE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN INTERACTION; TUMOR GROWTH;

MUS;

EID: 33847408725     PISSN: 15356108     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ccr.2007.01.014     Document Type: Article

References (48)

1. Anbazhagan R., Fujii H., and Gabrielson E. Allelic loss of chromosomal arm 8p in breast cancer progression. Am. J. Pathol. 152 (1998) 815-819
2. INK4c sensitizes mice to carcinogen-induced tumorigenesis. Mol. Cell. Biol. 23 (2003) 1269-1277
3. Baldassarre G., Belletti B., Nicoloso M.S., Schiappacassi M., Vecchione A., Spessotto P., Morrione A., Canzonieri V., and Colombatti A. p27(Kip1)-stathmin interaction influences sarcoma cell migration and invasion. Cancer Cell 7 (2005) 51-63
4. Blajeski A.L., Phan V.A., Kottke T.J., and Kaufmann S.H. G1 and G2 cell-cycle arrest following microtubule depolymerization in human breast cancer cells. J. Clin. Invest. 110 (2002) 91-99
5. Cabeza-Arvelaiz Y., Sepulveda J.L., Lebovitz R.M., Thompson T.C., and Chinault A.C. Functional identification of LZTS1 as a candidate prostate tumor suppressor gene on human chromosome 8p22. Oncogene 20 (2001) 4169-4179
6. Carnero A. Targeting the cell cycle for cancer therapy. Br. J. Cancer 87 (2002) 129-133
7. Chao J.I., Kuo P.C., and Hsu T.S. Down-regulation of survivin in nitric oxide-induced cell growth inhibition and apoptosis of the human lung carcinoma cells. J. Biol. Chem. 279 (2004) 20267-20276
8. Chang D.C., Xu N., and Luo K.Q. Degradation of cyclin B is required for the onset of anaphase in mammalian cells. J. Biol. Chem. 278 (2003) 37865-37873
9. Chen F., Zhang Z., Bower J., Lu Y., Leonard S.S., Ding M., Castranova V., Piwnica-Worms H., and Shi X. Arsenite-induced Cdc25C degradation is through the KEN-box and ubiquitin-proteasome pathway. Proc. Natl. Acad. Sci. USA 99 (2002) 1990-1995
10. Cimini D., Moree B., Canman J.C., and Salmon E.D. Merotelic kinetochore orientation occurs frequently during early mitosis in mammalian tissue cells and error correction is achieved by two different mechanisms. J. Cell Sci. 116 (2003) 4213-4225
11. Clute P., and Pines J. Temporal and spatial control of cyclin B1 destruction in metaphase. Nat. Cell Biol. 1 (1999) 82-87
12. Cross F.R., Schroeder L., Kruse M., and Chen K.C. Quantitative characterization of a mitotic cyclin threshold regulating exit from mitosis. Mol. Biol. Cell 16 (2005) 2129-2138
13. El-Naggar A.K., Coombes M.M., Batsakis J.G., Hong W.K., Goepfert H., and Kagan J. Localization of chromosome 8p regions involved in early tumorigenesis of oral and laryngeal squamous carcinoma. Oncogene 16 (1998) 2983-2987
14. Kip1 is haplo-insufficient for tumor suppression. Nature 396 (1998) 177-180
15. Han Y., Shen H., Carr B.I., Wipf P., Lazo J.S., and Pan S. NAD(P)H:quinone oxidoreductase-1-dependent and -independent cytotoxicity of potent quinone Cdc25 phosphatase inhibitors. J. Pharmacol. Exp. Ther. 309 (2004) 64-70
16. Ichikawa T., Nihei N., Suzuki H., Oshimura M., Emi M., Nakamura Y., Hayata I., Isaacs J.T., and Shimazaki J. Suppression of metastasis of rat prostatic cancer by introducing human chromosome 8. Cancer Res. 54 (1994) 2299-2302
17. Ishii H., Baffa R., Numata S., Murakumo Y., Rattan S., Inoue H., Mori M., Fidanza V., Alder H., and Croce C.M. The FEZ1 gene at chromosome 8p22 encodes a leucine-zipper protein, and its expression is altered in multiple human tumors. Proc. Natl. Acad. Sci. USA 96 (1999) 3928-3933
18. Ishii H., Vecchione A., Murakumo Y., Baldassarre G., Numata S., Trapasso F., Alder H., Baffa R., and Croce C.M. FEZ1/LZTS1 gene at 8p22 suppresses cancer cell growth and regulates mitosis. Proc. Natl. Acad. Sci. USA 98 (2001) 10374-10379
19. Jackson P.K. Climbing the Greatwall to mitosis. Mol. Cell 22 (2006) 156-157
20. Kwabi-Addo B., Giri D., Schimdt K., Podsypanina K., Parson R., Greenberg N., and Ittmann M. Haploinsufficiency of Pten tumor suppressor gene promotes prostate cancer progression. Proc. Natl. Acad. Sci. USA 98 (2001) 11563-11568
21. Lindqvist A., Kallstrom H., Lundgren A., Barsoum E., and Rosenthal C.K. Cdc25B cooperates with Cdc25A to induce mitosis but has a unique role in activating cyclin B1-Cdk1 at the centrosome. J. Cell Biol. 171 (2005) 35-45
22. Magee P.N. The experimental basis for the role of nitroso compounds in human cancer. Cancer Surv. 8 (1989) 207-239
23. McCurrach M.E., and Lowe S.W. Methods for studying pro- and antiapoptotic genes in nonimmortal cells. Methods Cell Biol. 66 (2001) 197-227
24. McGarry T.J., and Kirschner M.W. Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell 93 (1998) 1043-1053
25. Nigg E.A. Mitotic kinases as regulators of cell division and its checkpoints. Nat. Rev. Mol. Cell Biol. 2 (2001) 21-32
26. Niiya F., Xie X., Lee K.S., Inoue H., and Miki T. Inhibition of cyclin-dependent kinase 1 induces cytokinesis without chromosome segregation in an ECT2 and MgcRacGAP-dependent manner. J. Biol. Chem. 280 (2005) 36502-36509
27. Nonaka D., Fabbri A., Roz L., Mariani L., Vecchione A., Moore G.W., Tavecchio L., Croce C.M., and Sozzi G. Reduced FEZ1/LZTS1 expression and outcome prediction in lung cancer. Cancer Res. 65 (2005) 1207-1212
28. Ono K., Uzawa K., Nakatsuru M., Shiiba M., Mochida Y., Tada A., Bukawa H., Miyakawa A., Yokoe H., and Tanzawa H. Down-regulation of FEZ1/LZTS1 gene with frequent loss of heterozigosity in oral squamous cell carcinomas. Int. J. Oncol. 23 (2003) 297-302
29. Parry D.H., and O'Farrell P.H. The schedule of destruction of three mitotic cyclins can dictate the timing of events during exit from mitosis. Curr. Biol. 11 (2001) 671-683
30. Potapova T.A., Daum J.R., Pittman B.D., Hudson J.R., Jones T.N., Satinover D.L., Stukenberg P.T., and Gorbsky G.J. The reversibility of mitotic exit in vertebrate cells. Nature 440 (2006) 954-958
31. Seong Y.S., Min C., Li L., Yang J.Y., Kim S.-Y., Cao X., Kim K., Yuspa S.H., Chung H.H., and Lee K.S. Characterization of a novel cyclin-dependent kinase 1 inhibitor, BMI-1026. Cancer Res. 63 (2003) 7384-7391
32. Sha W., Moore J., Chen K., Lassaletta A.D., Yi C.-S., Tyson J.J., and Sible J.C. Hysteresis drives cell-cycle transitions in Xenopus laevis egg extracts. Proc. Natl. Acad. Sci. USA 100 (2003) 975-980
33. Shuji K., Gerburg W., Masafumi N., and Kun Ping L. Telomeric protein Pin2/TRF1 induces mitotic entry and apoptosis in cells with short telomers and is down-regulated in human breast tumors. Oncogene 20 (2001) 1497-1508
34. Sigrist S., Jacobs H., Stratmann R., and Lehner C.F. Exit from mitosis is regulated by Drosophila fizzy and the sequential destruction of cyclins A, B and B3. EMBO J. 14 (1995) 4827-4838
35. Smits V.A.J., and Medema R.H. Checking out the G2/M transition. Biochim. Biophys. Acta 1519 (2001) 1-12
36. Song M.S., Song S.J., Ayad N.G., Chang J.S., Lee J.H., Hong H.K., Lee H., Choi N., Kim J., Kim H., et al. The tumour suppressor RASSF1A regulates mitosis by inhibiting the APC-Cdc20 complex. Nat. Cell Biol. 6 (2004) 129-137
37. Tobey R.A., Oishi N., and Crissman H.A. Cell cycle synchronization: reversible induction of G2 synchrony in cultured rodent and human diploid fibroblasts. Proc. Natl. Acad. Sci. USA 87 (1990) 5104-5108
38. Toyooka S., Fukuyama Y., Wistuba I.I., Tockman M.S., Minna J.D., and Gazdar A.F. Differential expression of FEZ1/LZTS1 gene in lung cancers and their cell cultures. Clin. Cancer Res. 8 (2002) 2292-2297
39. Vassilev L.T., Tovar C., Chen S., Knezevic D., Zhao X., Sun H., Heimbrook D.C., and Chen L. Selective small-molecule inhibitor reveals critical mitotic functions of human CDK1. Proc. Natl. Acad. Sci. USA 103 (2006) 10660-10665
40. Vecchione A., Ishii H., Shiao Y.-H., Trapasso F., Rugge M., Alder H., Croce C.M., and Baffa R. Altered expression of Fez1 protein in gastric carcinoma. Clin. Cancer Res. 7 (2001) 1546-1552
41. Vecchione A., Ishii H., Baldassarre G., Bassi P., Trapasso F., Alder H., Pagano F., Gomella L.G., Croce C.M., and Baffa R. FEZ1/LZTS1 is down-regulated in high-grade bladder cancer, and its restoration suppresses tumorigenicity in transitional cell carcinoma cells. Am. J. Pathol. 160 (2002) 1345-1352
42. Venkatachalam S., Shi Y.P., Jones S.N., Vogel H., Bradley A., Pinkel D., and Donehower L.A. Retention of wild-type p53 in tumors from p53 heterozygous mice: reduction of p53 dosage can promote cancer formation. EMBO J. 17 (1998) 4657-4667
43. Vocke C.D., Pozzatti R.O., Bostwick D.G., Florence C.D., Jennings S.B., Strup S.E., Duray P.H., Liotta L.A., Emmert-Buck M.R., and Linehan W.M. Analysis of 99 microdissected prostate carcinomas reveals a high frequency of allelic loss on chromosome 8p12-21. Cancer Res. 56 (1996) 2411-2416
44. Wagner U., Bubendorf L., Gasser T.C., Moch H., Gorog J.P., Richter J., Mihatsch M.J., Waldman F.M., and Sauter G. Chromosome 8p deletions are associated with invasive tumor growth in urinary bladder cancer. Am. J. Pathol. 151 (1997) 753-759
45. Weaver B.A.A., and Cleveland D.W. Decoding the links between mitosis, cancer and chemotherapy. The mitotic checkpoint, adaptation and cell death. Cancer Cell 8 (2005) 7-12
46. Westendorf J.M., Rao P.N., and Gerace L. Cloning of cDNAs for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated epitope. Proc. Natl. Acad. Sci. USA 91 (1994) 714-718
47. Yang C.S. Research on esophageal cancer in China: a review. Cancer Res. 40 (1980) 2633-2644
48. Yu J., Zhao Y., Li Z., Galas S., and Goldberg M.L. Greatwall kinase participates in the CDC2 autoregulatory loop in Xenopus egg extracts. Mol. Cell 22 (2006) 83-91