journal article Jun 23, 2017

The LATS1 and LATS2 tumor suppressors: beyond the Hippo pathway

View at Publisher Save 10.1038/cdd.2017.99
Topics

No keywords indexed for this article. Browse by subject →

References
217
[1]
Visintin R, Amon A . Regulation of the mitotic exit protein kinases Cdc15 and Dbf2. Mol Biol Cell 2001; 12: 2961–2974. 10.1091/mbc.12.10.2961
[2]
Rock JM, Lim D, Stach L, Ogrodowicz RW, Keck JM, Jones MH et al. Activation of the yeast Hippo pathway by phosphorylation-dependent assembly of signaling complexes. Science 2013; 340: 871–875. 10.1126/science.1235822
[3]
Bardin AJ, Amon A . Men and sin: what’s the difference? Nat Rev Mol Cell Biol 2001; 2: 815–826. 10.1038/35099020
[4]
Chan EHY, Nousiainen M, Chalamalasetty RB, Schäfer A, Nigg EA, Silljé HHW . The Ste20-like kinase Mst2 activates the human large tumor suppressor kinase Lats1. Oncogene 2005; 24: 2076–2086. 10.1038/sj.onc.1208445
[5]
Cai Q, Wang W, Gao Y, Yang Y, Zhu Z, Fan Q . Ce-wts-1 plays important roles in Caenorhabditis elegans development. FEBS Lett 2009; 583: 3158–3164. 10.1016/j.febslet.2009.09.002
[6]
Hilman D, Gat U . The evolutionary history of YAP and the Hippo/YAP pathway. Mol Biol Evol 2011; 28: 2403–2417. 10.1093/molbev/msr065
[7]
Bryant PJ, Watson KL, Justice RW, Woods DF . Tumor suppressor genes encoding proteins required for cell interactions and signal transduction in Drosophila. Development 1993: 239–249. 10.1242/dev.119.supplement.239
[8]
Justice RW, Zilian O, Woods DF, Noll M, Bryant PJ . The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev 1995; 9: 534–546. 10.1101/gad.9.5.534
[9]
Zhao B, Li L, Lei Q, Guan K-L . The Hippo-YAP pathway in organ size control and tumorigenesis: an updated version. Genes Dev 2010; 24: 862–874. 10.1101/gad.1909210
[10]
Dewey EB, Sanchez D, Johnston CA . Warts phosphorylates mud to promote pins-mediated mitotic spindle orientation in Drosophila, independent of Yorkie. Curr Biol 2015; 25: 2751–2762. 10.1016/j.cub.2015.09.025
[11]
Staley BK, Irvine KD . Hippo signaling in Drosophila: recent advances and insights. Dev Dyn 2012; 241: 3–15. 10.1002/dvdy.22723
[12]
Tao W, Zhang S, Turenchalk GS, Stewart RA St, John MA, Chen W et al. Human homologue of the Drosophila melanogaster lats tumour suppressor modulates CDC2 activity. Nat Genet 1999; 21: 177–181. 10.1038/5960
[13]
McPherson JP, Tamblyn L, Elia A, Migon E, Shehabeldin A, Matysiak-Zablocki E et al. Lats2/Kpm is required for embryonic development, proliferation control and genomic integrity. EMBO J 2004; 23: 3677–3688. 10.1038/sj.emboj.7600371
[14]
Yabuta N, Okada N, Ito A, Hosomi T, Nishihara S, Sasayama Y et al. Lats2 is an essential mitotic regulator required for the coordination of cell division. J Biol Chem 2007; 282: 19259–19271. 10.1074/jbc.m608562200
[15]
St John MA, Tao W, Fei X, Fukumoto R, Carcangiu ML, Brownstein DG et al. Mice deficient of Lats1 develop soft-tissue sarcomas, ovarian tumours and pituitary dysfunction. Nat Genet 1999; 21: 182–186. 10.1038/5965
[16]
Zanconato F, Cordenonsi M, Piccolo S . YAP/TAZ at the roots of cancer. Cancer Cell 2016; 29: 783–803. 10.1016/j.ccell.2016.05.005
[17]
Meng Z, Moroishi T, Guan K-L . Mechanisms of Hippo pathway regulation. Genes Dev 2016; 30: 1–17. 10.1101/gad.274027.115
[18]
Avruch J, Zhou D, Fitamant J, Bardeesy N, Mou F, Barrufet LR . Protein kinases of the Hippo pathway: regulation and substrates. Semin Cell Dev Biol 2012; 23: 770–784. 10.1016/j.semcdb.2012.07.002
[19]
Hori T, Takaori-Kondo A, Kamikubo Y, Uchiyama T . Molecular cloning of a novel human protein kinase, kpm, that is homologous to warts/lats, a Drosophila tumor suppressor. Oncogene 2000; 19: 3101–3109. 10.1038/sj.onc.1203659
[20]
Yabuta N, Fujii T, Copeland NG, Gilbert DJ, Jenkins NA, Nishiguchi H et al. Structure, expression, and chromosome mapping of LATS2, a mammalian homologue of the Drosophila tumor suppressor gene lats/warts. Genomics 2000; 63: 263–270. 10.1006/geno.1999.6065
[21]
Li Y, Pei J, Xia H, Ke H, Wang H, Tao W . Lats2, a putative tumor suppressor, inhibits G1/S transition. Oncogene 2003; 22: 4398–4405. 10.1038/sj.onc.1206603
[22]
Yabuta N, Mukai S, Okamoto A, Okuzaki D, Suzuki H, Torigata K et al. N-terminal truncation of Lats1 causes abnormal cell growth control and chromosomal instability. J Cell Sci 2013; 126: 508–520. 10.1242/jcs.113431
[23]
Kim M, Kim M, Park S-J, Lee C, Lim D-S . Role of Angiomotin-like 2 mono-ubiquitination on YAP inhibition. EMBO Rep 2016; 17: 64–78. 10.15252/embr.201540809
[24]
Nishiyama Y, Hirota T, Morisaki T, Hara T, Marumoto T, Iida S et al. A human homolog of Drosophila warts tumor suppressor, h-warts, localized to mitotic apparatus and specifically phosphorylated during mitosis. FEBS Lett 1999; 459: 159–165. 10.1016/s0014-5793(99)01224-7
[25]
Sudol M . Newcomers to the WW domain-mediated network of the Hippo tumor suppressor pathway. Genes Cancer 2010; 1: 1115–1118. 10.1177/1947601911401911
[26]
Pearce LR, Komander D, Alessi DR . The nuts and bolts of AGC protein kinases. Nat Rev Mol Cell Biol 2010; 11: 9–22. 10.1038/nrm2822
[27]
Hoa L, Kulaberoglu Y, Gundogdu R, Cook D, Mavis M, Gomez M et al. The characterisation of LATS2 kinase regulation in Hippo-YAP signalling. Cell Signal 2016; 28: 488–497. 10.1016/j.cellsig.2016.02.012
[28]
Hergovich A, Schmitz D, Hemmings BA . The human tumour suppressor LATS1 is activated by human MOB1 at the membrane. Biochem Biophys Res Commun 2006; 345: 50–58. 10.1016/j.bbrc.2006.03.244
[29]
Spatial Organization of Hippo Signaling at the Plasma Membrane Mediated by the Tumor Suppressor Merlin/NF2

Feng Yin, Jianzhong Yu, Yonggang Zheng et al.

Cell 2013 10.1016/j.cell.2013.08.025
[30]
Praskova M, Xia F, Avruch J . MOBKL1A/MOBKL1B phosphorylation by MST1 and MST2 inhibits cell proliferation. Curr Biol 2008; 18: 311–321. 10.1016/j.cub.2008.02.006
[31]
Zhou D, Conrad C, Xia F, Park J-S, Payer B, Yin Y et al. Mst1 and Mst2 maintain hepatocyte quiescence and suppress hepatocellular carcinoma development through inactivation of the Yap1 oncogene. Cancer Cell 2009; 16: 425–438. 10.1016/j.ccr.2009.09.026
[32]
Meng Z, Moroishi T, Mottier-Pavie V, Plouffe SW, Hansen CG, Hong AW et al. MAP4K family kinases act in parallel to MST1/2 to activate LATS1/2 in the Hippo pathway. Nat Commun 2015; 6: 8357. 10.1038/ncomms9357
[33]
Kim M, Kim M, Lee S, Kuninaka S, Saya H, Lee H et al. cAMP/PKA signalling reinforces the LATS-YAP pathway to fully suppress YAP in response to actin cytoskeletal changes. EMBO J 2013; 32: 1543–1555. 10.1038/emboj.2013.102
[34]
Okada N, Yabuta N, Suzuki H, Aylon Y, Oren M, Nojima H . A novel Chk1/2-Lats2-14-3-3 signaling pathway regulates P-body formation in response to UV damage. J Cell Sci 2011; 124: 57–67. 10.1242/jcs.072918
[35]
Aylon Y, Yabuta N, Besserglick H, Buganim Y, Rotter V, Nojima H et al. Silencing of the Lats2 tumor suppressor overrides a p53-dependent oncogenic stress checkpoint and enables mutant H-Ras-driven cell transformation. Oncogene 2009; 28: 4469–4479. 10.1038/onc.2009.270
[36]
Aylon Y, Ofir-Rosenfeld Y, Yabuta N, Lapi E, Nojima H, Lu X et al. The Lats2 tumor suppressor augments p53-mediated apoptosis by promoting the nuclear proapoptotic function of ASPP1. Genes Dev 2010; 24: 2420–2429. 10.1101/gad.1954410
[37]
Wang G, Jiang Q, Zhang C . The role of mitotic kinases in coupling the centrosome cycle with the assembly of the mitotic spindle. J Cell Sci 2014; 127: 4111–4122. 10.1242/jcs.151753
[38]
Toji S, Yabuta N, Hosomi T, Nishihara S, Kobayashi T, Suzuki S et al. The centrosomal protein Lats2 is a phosphorylation target of Aurora-A kinase. Genes Cells 2004; 9: 383–397. 10.1111/j.1356-9597.2004.00732.x
[39]
Yabuta N, Mukai S, Okada N, Aylon Y, Nojima H . The tumor suppressor Lats2 is pivotal in Aurora A and Aurora B signaling during mitosis. Cell Cycle 2011; 10: 2724–2736. 10.4161/cc.10.16.16873
[40]
Zhang L, Iyer J, Chowdhury A, Ji M, Xiao L, Yang S et al. KIBRA regulates aurora kinase activity and is required for precise chromosome alignment during mitosis. J Biol Chem 2012; 287: 34069–34077. 10.1074/jbc.m112.385518
[41]
Humbert N, Navaratnam N, Augert A, Da Costa M, Martien S, Wang J et al. Regulation of ploidy and senescence by the AMPK-related kinase NUAK1. EMBO J 2010; 29: 376–386. 10.1038/emboj.2009.342
[42]
Xiao L, Chen Y, Ji M, Dong J . KIBRA regulates Hippo signaling activity via interactions with large tumor suppressor kinases. J Biol Chem 2011; 286: 7788–7796. 10.1074/jbc.m110.173468
[43]
Huntoon CJ, Nye MD, Geng L, Peterson KL, Flatten KS, Haluska P et al. Heat shock protein 90 inhibition depletes LATS1 and LATS2, two regulators of the mammalian Hippo tumor suppressor pathway. Cancer Res 2010; 70: 8642–8650. 10.1158/0008-5472.can-10-1345
[44]
Das Thakur M, Feng Y, Jagannathan R, Seppa MJ, Skeath JB, Longmore GD . Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr Biol 2010; 20: 657–662. 10.1016/j.cub.2010.02.035
[45]
Rauskolb C, Pan G, Reddy BVVG, Oh H, Irvine KD . Zyxin links fat signaling to the Hippo pathway. PLoS Biol 2011; 9: e1000624. 10.1371/journal.pbio.1000624
[46]
Bae SJ, Kim M, Kim S-H, Kwon YE, Lee J-H, Kim J et al. NEDD4 controls intestinal stem cell homeostasis by regulating the Hippo signalling pathway. Nat Commun 2015; 6: 6314. 10.1038/ncomms7314
[47]
Salah Z, Cohen S, Itzhaki E, Aqeilan RI . NEDD4 E3 ligase inhibits the activity of the Hippo pathway by targeting LATS1 for degradation. Cell Cycle 2013; 12: 3817–3823. 10.4161/cc.26672
[48]
Ho KC, Zhou Z, She Y-M, Chun A, Cyr TD, Yang X . Itch E3 ubiquitin ligase regulates large tumor suppressor 1 stability [corrected]. Proc Natl Acad Sci USA 2011; 108: 4870–4875. 10.1073/pnas.1101273108
[49]
Salah Z, Melino G, Aqeilan RI . Negative regulation of the Hippo pathway by E3 ubiquitin ligase ITCH is sufficient to promote tumorigenicity. Cancer Res 2011; 71: 2010–2020. 10.1158/0008-5472.can-10-3516
[50]
Yeung B, Ho K-C, Yang X . WWP1 E3 ligase targets LATS1 for ubiquitin-mediated degradation in breast cancer cells. PLoS ONE 2013; 8: e61027. 10.1371/journal.pone.0061027

Showing 50 of 217 references

Metrics
220
Citations
217
References
Details
Published
Jun 23, 2017
Vol/Issue
24(9)
Pages
1488-1501
License
View
Cite This Article
Noa Furth, Yael Aylon (2017). The LATS1 and LATS2 tumor suppressors: beyond the Hippo pathway. Cell Death & Differentiation, 24(9), 1488-1501. https://doi.org/10.1038/cdd.2017.99
Related

You May Also Like

Ferroptosis: process and function

Y Xie, W Hou · 2016

3,266 citations

Emerging roles of caspase-3 in apoptosis

Alan G Porter, Reiner U Jänicke · 1999

3,250 citations

Roles of CHOP/GADD153 in endoplasmic reticulum stress

S Oyadomari, M Mori · 2003

2,417 citations