N-terminal truncation of Lats1 causes abnormal cell growth control and chromosomal instability

Journal of Cell Science

Volumn 126, Issue 2, 2013, Pages 508-519

  Yabuta, Norikazu ^a   Mukai, Satomi ^a   Okamoto, Ayumi ^a   Okuzaki, Daisuke ^a,b   Suzuki, Hirokazu ^a   Torigata, Kosuke ^a   Yoshida, Kaori ^a   Okada, Nobuhiro ^a,e   Miura, Daisaku ^c   Ito, Akihiko ^d   Ikawa, Masahito ^b   Okabe, Masaru ^b   Nojima, Hiroshi ^a,b  

^a OSAKA UNIVERSITY   (Japan)

^b OSAKA UNIVERSITY   (Japan)

^c HYOGO COLLEGE OF MEDICINE   (Japan)

^d KINKI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Chromosome instability; Hippo; Lats1; Lats2; YAP

Indexed keywords

LATS1 PROTEIN; LATS2 PROTEIN; MESSENGER RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL CONTACT; CELL DENSITY; CELL GROWTH; CENTROSOME; CHROMOSOMAL INSTABILITY; CYTOKINESIS; DOWN REGULATION; FIBROBLAST; GROWTH REGULATION; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARCINOGENESIS; CELL ADHESION; CELL GROWTH PROCESSES; CELL LINE, TUMOR; CHROMOSOMAL INSTABILITY; DOWN-REGULATION; FEMALE; HUMANS; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, NUDE; PHOSPHOPROTEINS; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

MUS; MUS MUSCULUS;

EID: 84876083320     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.113431     Document Type: Article

References (53)

1. Abe, Y., Ohsugi, M., Haraguchi, K., Fujimoto, J. and Yamamoto, T. (2006). LATS2- Ajuba complex regulates gamma-tubulin recruitment to centrosomes and spindle organization during mitosis. FEBS Lett. 580, 782-788.
2. Akagi, T., Sasai, K. and Hanafusa, H. (2003). Refractory nature of normal human diploid fibroblasts with respect to oncogene-mediated transformation. Proc. Natl. Acad. Sci. USA 100, 13567-13572.
3. Aylon, Y., Michael, D., Shmueli, A., Yabuta, N., Nojima, H. and Oren, M. (2006). A positive feedback loop between the p53 and Lats2 tumor suppressors prevents tetraploidization. Genes Dev. 20, 2687-2700.
4. Aylon, Y., Ofir-Rosenfeld, Y., Yabuta, N., Lapi, E., Nojima, H., Lu, X. and Oren, M. (2010). The Lats2 tumor suppressor augments p53-mediated apoptosis by promoting the nuclear proapoptotic function of ASPP1. Genes Dev. 24, 2420-2429.
5. Boggiano, J. C. and Fehon, R. G. (2012). Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling. Dev. Cell 22, 695-702.
6. Bothos, J., Tuttle, R. L., Ottey, M., Luca, F. C. and Halazonetis, T. D. (2005). Human LATS1 is a mitotic exit network kinase. Cancer Res. 65, 6568-6575.
7. Chan, E. H., Nousiainen, M., Chalamalasetty, R. B., Schäfer, A., Nigg, E. A. and Silljé, H. H. (2005). The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 24, 2076-2086.
8. Feigin, M. E. and Muthuswamy, S. K. (2009). Polarity proteins regulate mammalian cell-cell junctions and cancer pathogenesis. Curr. Opin. Cell Biol. 21, 694-700.
9. Fujiwara, T., Bandi, M., Nitta, M., Ivanova, E. V., Bronson, R. T. and Pellman, D. (2005). Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437, 1043-1047.
10. Funato, Y., Terabayashi, T., Sakamoto, R., Okuzaki, D., Ichise, H., Nojima, H., Yoshida, N. and Miki, H. (2010). Nucleoredoxin sustains Wnt/β-catenin signaling by retaining a pool of inactive dishevelled protein. Curr. Biol. 20, 1945-1952.
11. Gordon, D. J., Resio, B. and Pellman, D. (2012). Causes and consequences of aneuploidy in cancer. Nat. Rev. Genet. 13, 189-203.
12. Hanahan, D. and Weinberg, R. A. (2011). Hallmarks of cancer: the next generation. Cell 144, 646-674.
13. Hergovich, A., Lamla, S., Nigg, E. A. and Hemmings, B. A. (2007). Centrosomeassociated NDR kinase regulates centrosome duplication. Mol. Cell 25, 625-634.
14. Hirota, T., Morisaki, T., Nishiyama, Y., Marumoto, T., Tada, K., Hara, T., Masuko, N., Inagaki, M., Hatakeyama, K. and Saya, H. (2000). Zyxin, a regulator of actin filament assembly, targets the mitotic apparatus by interacting with h-warts/LATS1 tumor suppressor. J. Cell Biol. 149, 1073-1086.
15. Humbert, N., Navaratnam, N., Augert, A., Da Costa, M., Martien, S., Wang, J., Martinez, D., Abbadie, C., Carling, D., de Launoit, Y. et al. (2010). Regulation of ploidy and senescence by the AMPK-related kinase NUAK1. EMBO J. 29, 376-386.
16. Iida, S., Hirota, T., Morisaki, T., Marumoto, T., Hara, T., Kuninaka, S., Honda, S., Kosai, K., Kawasuji, M., Pallas, D. C. et al. (2004). Tumor suppressor WARTS ensures genomic integrity by regulating both mitotic progression and G1 tetraploidy checkpoint function. Oncogene 23, 5266-5274.
17. Ishii, T., Onda, H., Tanigawa, A., Ohshima, S., Fujiwara, H., Mima, T., Katada, Y., Deguchi, H., Suemura, M., Miyake, T. et al. (2006). Isolation and expression profiling of genes upregulated in the peripheral blood cells of systemic lupus erythematosus patients. DNA Res. 12, 429-439.
18. Kamikubo, Y., Takaori-Kondo, A., Uchiyama, T. and Hori, T. (2003). Inhibition of cell growth by conditional expression of kpm, a human homologue of Drosophila warts/lats tumor suppressor. J. Biol. Chem. 278, 17609-17614.
19. Ke, H., Pei, J., Ni, Z., Xia, H., Qi, H., Woods, T., Kelekar, A. and Tao, W. (2004). Putative tumor suppressor Lats2 induces apoptosis through downregulation of Bcl-2 and Bcl-x(L). Exp. Cell Res. 298, 329-338.
20. Lei, Q. Y., Zhang, H., Zhao, B., Zha, Z. Y., Bai, F., Pei, X. H., Zhao, S., Xiong, Y. and Guan, K. L. (2008). TAZ promotes cell proliferation and epithelialmesenchymal transition and is inhibited by the hippo pathway. Mol. Cell. Biol. 28, 2426-2436.
21. Li, Y., Pei, J., Xia, H., Ke, H., Wang, H. and Tao, W. (2003). Lats2, a putative tumor suppressor, inhibits G1/S transition. Oncogene 22, 4398-4405.
22. Li, W., Wang, L., Katoh, H., Liu, R., Zheng, P. and Liu, Y. (2011). Identification of a tumor suppressor relay between the FOXP3 and the Hippo pathways in breast and prostate cancers. Cancer Res. 71, 2162-2171.
23. Liu, C. Y., Zha, Z. Y., Zhou, X., Zhang, H., Huang, W., Zhao, D., Li, T., Chan, S. W., Lim, C. J., Hong, W. et al. (2010). The hippo tumor pathway promotes TAZ degradation by phosphorylating a phosphodegron and recruiting the SCFbeta-TrCP E3 ligase. J. Biol. Chem. 285, 37159-37169.
24. Matallanas, D., Romano, D., Al-Mulla, F., O'Neill, E., Al-Ali, W., Crespo, P., Doyle, B., Nixon, C., Sansom, O., Drosten, M. et al. (2011). Mutant K-Ras activation of the proapoptotic MST2 pathway is antagonized by wild-type K-Ras. Mol. Cell 44, 893-906.
25. McPherson, J. P., Tamblyn, L., Elia, A., Migon, E., Shehabeldin, A., Matysiak-Zablocki, E., Lemmers, B., Salmena, L., Hakem, A., Fish, J. et al. (2004). Lats2/ Kpm is required for embryonic development, proliferation control and genomic integrity. EMBO J. 23, 3677-3688.
26. Mizushima, H., Wang, X., Miyamoto, S. and Mekada, E. (2009). Integrin signal masks growth-promotion activity of HB-EGF in monolayer cell cultures. J. Cell Sci. 122, 4277-4286.
27. Morisaki, T., Hirota, T., Iida, S., Marumoto, T., Hara, T., Nishiyama, Y., Kawasuzi, M., Hiraoka, T., Mimori, T., Araki, N. et al. (2002). WARTS tumor suppressor is phosphorylated by Cdc2/cyclin B at spindle poles during mitosis. FEBS Lett. 529, 319-324.
28. Nigg, E. A. (2002). Centrosome aberrations: cause or consequence of cancer progression? Nat. Rev. Cancer 2, 815-825.
29. Nigg, E. A. and Raff, J. W. (2009). Centrioles, centrosomes, and cilia in health and disease. Cell 139, 663-678.
30. Nishioka, N., Inoue, K., Adachi, K., Kiyonari, H., Ota, M., Ralston, A., Yabuta, N., Hirahara, S., Stephenson, R. O., Ogonuki, N. et al. (2009). The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398-410.
31. Nishiyama, Y., Hirota, T., Morisaki, T., Hara, T., Marumoto, T., Iida, S., Makino, K., Yamamoto, H., Hiraoka, T., Kitamura, N. et al. (1999). A human homolog of Drosophila warts tumor suppressor, h-warts, localized to mitotic apparatus and specifically phosphorylated during mitosis. FEBS Lett. 459, 159-165.
32. Okada, N., Yabuta, N., Suzuki, H., Aylon, Y., Oren, M. and Nojima, H. (2011). A novel Chk1/2-Lats2-14-3-3 signaling pathway regulates P-body formation in response to UV damage. J. Cell Sci. 124, 57-67.
33. Ota, M. and Sasaki, H. (2008). Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 135, 4059-4069.
34. Pan, D. (2010). The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505.
35. Powzaniuk, M., McElwee-Witmer, S., Vogel, R. L., Hayami, T., Rutledge, S. J., Chen, F., Harada, S., Schmidt, A., Rodan, G. A., Freedman, L. P. et al. (2004). The LATS2/KPM tumor suppressor is a negative regulator of the androgen receptor. Mol. Endocrinol. 18, 2011-2023.
36. St John, M. A., Tao, W., Fei, X., Fukumoto, R., Carcangiu, M. L., Brownstein, D. G., Parlow, A. F., McGrath, J. and Xu, T. (1999). Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat. Genet. 21, 182-186.
37. Takahashi, Y., Miyoshi, Y., Takahata, C., Irahara, N., Taguchi, T., Tamaki, Y. and Noguchi, S. (2005). Down-regulation of LATS1 and LATS2 mRNA expression by promoter hypermethylation and its association with biologically aggressive phenotype in human breast cancers. Clin. Cancer Res. 11, 1380-1385.
38. Takahashi, A., Ohtani, N., Yamakoshi, K., Iida, S., Tahara, H., Nakayama, K., Nakayama, K. I., Ide, T., Saya, H. and Hara, E. (2006). Mitogenic signalling and the p16INK4a-Rb pathway cooperate to enforce irreversible cellular senescence. Nat. Cell Biol. 8, 1291-1297.
39. Toji, S., Yabuta, N., Hosomi, T., Nishihara, S., Kobayashi, T., Suzuki, S., Tamai, K. and Nojima, H. (2004). The centrosomal protein Lats2 is a phosphorylation target of Aurora-A kinase. Genes Cells 9, 383-397.
40. Vigneron, A. M. and Vousden, K. H. (2011). An indirect role for ASPP1 in limiting p53-dependent p21 expression and cellular senescence. EMBO J. 31, 471-480.
41. Visser, S. and Yang, X. (2010). LATS tumor suppressor: a new governor of cellular homeostasis. Cell Cycle 9, 3892-3903.
42. Xia, H., Qi, H., Li, Y., Pei, J., Barton, J., Blackstad, M., Xu, T. and Tao, W. (2002). LATS1 tumor suppressor regulates G2/M transition and apoptosis. Oncogene 21, 1233-1241.
43. Yabuta, N., Fujii, T., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Nishiguchi, H., Endo, Y., Toji, S., Tanaka, H., Nishimune, Y. et al. (2000). Structure, expression, and chromosome mapping of LATS2, a mammalian homologue of the Drosophila tumor suppressor gene lats/warts. Genomics 63, 263-270.
44. Yabuta, N., Okada, N., Ito, A., Hosomi, T., Nishihara, S., Sasayama, Y., Fujimori, A., Okuzaki, D., Zhao, H., Ikawa, M. et al. (2007). Lats2 is an essential mitotic regulator required for the coordination of cell division. J. Biol. Chem. 282, 19259-19271.
45. Yabuta, N., Mukai, S., Okada, N., Aylon, Y. and Nojima, H. (2011). The tumor suppressor Lats2 is pivotal in Aurora A and Aurora B signaling during mitosis. Cell Cycle 10, 2724-2736.
46. Yang, X., Li, D. M., Chen, W. and Xu, T. (2001). Human homologue of Drosophila lats, LATS1, negatively regulate growth by inducing G(2)/M arrest or apoptosis. Oncogene 20, 6516-6523.
47. Zhang, J., Smolen, G. A. and Haber, D. A. (2008). Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res. 68, 2789-2794.
48. Zhang, K., Rodriguez-Aznar, E., Yabuta, N., Owen, R. J., Mingot, J. M., Nojima, H., Nieto, M. A. and Longmore, G. D. (2011). Lats2 kinase potentiates Snail1 activity by promoting nuclear retention upon phosphorylation. EMBO J. 31, 29-43.
49. Zhao, B., Wei, X., Li, W., Udan, R. S., Yang, Q., Kim, J., Xie, J., Ikenoue, T., Yu, J., Li, L. et al. (2007). Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21, 2747-2761.
50. Zhao, B., Ye, X., Yu, J., Li, L., Li, W., Li, S., Yu, J., Lin, J. D., Wang, C. Y., Chinnaiyan, A. M. et al. (2008). TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22, 1962-1971.
51. Zhao, B., Li, L., Tumaneng, K., Wang, C. Y. and Guan, K. L. (2010). A coordinated phosphorylation by Lats and CK1 regulates YAP stability through SCF(beta-TRCP). Genes Dev. 24, 72-85.
52. Zhao, B., Tumaneng, K. and Guan, K. L. (2011). The Hippo pathway in organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13, 877-883.
53. Zhou, D., Conrad, C., Xia, F., Park, J. S., Payer, B., Yin, Y., Lauwers, G. Y., Thasler, W., Lee, J. T., Avruch, J. et al. (2009). Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 16, 425-438.