WEE1 murine deficiency induces hyper-activation of APC/C and results in genomic instability and carcinogenesis

Oncogene

Volumn 34, Issue 23, 2015, Pages 3023-3035

  Vassilopoulos, A ^a,b   Tominaga, Y ^a   Kim, H Seok ^a,c   Lahusen, T ^a   Li, B ^d   Yu, H ^d   Gius, D ^b   Deng, C X ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c Ewha Womans University   (South Korea)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; AURORA A KINASE; AURORA B KINASE; CYCLIN B1; POLO LIKE KINASE 1; SECURIN; UVOMORULIN; CELL CYCLE PROTEIN; NUCLEAR PROTEIN; PROTEIN TYROSINE KINASE; TAMOXIFEN; WEE1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CARCINOGENESIS; BREAST EPITHELIUM; BREAST EPITHELIUM CELL; CELL CYCLE REGULATION; CELL DIVISION; CELL MUTANT; CONTROLLED STUDY; DAUGHTER CELL; DNA DAMAGE; GENE ACTIVATION; GENE DELETION; GENOMIC INSTABILITY; HAPLOINSUFFICIENCY; HETEROZYGOTE; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MITOSIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE; WEE1 GENE; ANIMAL; CELL TRANSFORMATION; CYTOLOGY; EPITHELIUM CELL; FEMALE; GENETICS; METABOLISM; PATHOLOGY; UDDER;

EUKARYOTA; MURINAE; MUS;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; CELL CYCLE PROTEINS; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL CELLS; FEMALE; GENE DELETION; GENOMIC INSTABILITY; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; MITOSIS; NUCLEAR PROTEINS; PROTEIN-TYROSINE KINASES; TAMOXIFEN;

EID: 84930536727     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.239     Document Type: Article

References (60)

1. Nurse P. Genetic control of cell size at cell division in yeast. Nature 1975; 256: 547-551
2. Thuriaux P, Nurse P, Carter B. Mutants altered in the control co-ordinating cell division with cell growth in the fission yeast Schizosaccharomyces pombe. Mol Gen Genet 1978; 161: 215-220
3. Fantes PA, Nurse P. Control of the timing of cell division in fission yeast. Cell size mutants reveal a second control pathway. Exp Cell Res 1978; 115: 317-329
4. Squire CJ, Dickson JM, Ivanovic I, Baker EN. Structure and inhibition of the human cell cycle checkpoint kinase, Wee1A kinase: an atypical tyrosine kinase with a key role in CDK1 regulation. Structure 2005; 13: 541-550
5. Featherstone C, Russell P. Fission yeast p107wee1 mitotic inhibitor is a tyrosine/serine kinase. Nature 1991; 349: 808-811
6. Gould KL, Nurse P. Tyrosine phosphorylation of the fission yeast cdc2+ protein kinase regulates entry into mitosis. Nature 1989; 342: 39-45
7. Lundgren K, Walworth N, Booher R, Dembski M, Kirschner M, Beach D. mik1 and wee1 cooperate in the inhibitory tyrosine phosphorylation of cdc2. Cell 1991; 64: 1111-1122
8. Parker LL, Atherton-Fessler S, Piwnica-Worms H. p107wee1 is a dual-specificity kinase that phosphorylates p34cdc2 on tyrosine 15. Proc Natl Acad Sci USA 1992; 89: 2917-2921
9. Parker LL, Piwnica-Worms H. Inactivation of the p34cdc2-cyclin B complex by the human WEE1 tyrosine kinase. Science 1992; 257: 1955-1957
10. Parker LL, Sylvestre PJ, Byrnes MJ 3rd, Liu F, Piwnica-Worms H. Identification of a 95-kDa WEE1-like tyrosine kinase in HeLa cells. Proc Natl Acad Sci USA 1995; 92: 9638-9642
11. Dunphy WG, Kumagai A. The cdc25 protein contains an intrinsic phosphatase activity. Cell 1991; 67: 189-196
12. Gautier J, Solomon MJ, Booher RN, Bazan JF, Kirschner MW. cdc25 is a specific tyrosine phosphatase that directly activates p34cdc2. Cell 1991; 67: 197-211
13. Kumagai A, Dunphy WG. The cdc25 protein controls tyrosine dephosphorylation of the cdc2 protein in a cell-free system. Cell 1991; 64: 903-914
14. Millar JB, McGowan CH, Lenaers G, Jones R, Russell P. p80cdc25 mitotic inducer is the tyrosine phosphatase that activates p34cdc2 kinase in fission yeast. EMBO J 1991; 10: 4301-4309
15. Strausfeld U, Labbe JC, Fesquet D, Cavadore JC, Picard A, Sadhu K, et al. Dephosphorylation and activation of a p34cdc2/cyclin B complex in vitro by human CDC25 protein. Nature 1991; 351: 242-245
16. Stumpff J, Kellogg DR, Krohne KA, Su TT. Drosophila Wee1 interacts with members of the gammaTURC and is required for proper mitotic-spindle morphogenesis and positioning. Curr Biol 2005; 15: 1525-1534
17. Deng CX. BRCA1: cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res 2006; 34: 1416-1426
18. Negrini S, Gorgoulis VG, Halazonetis TD. Genomic instability-An evolving hallmark of cancer. Nat Rev Mol Cell Biol 2010; 11: 220-228
19. Bartkova J, Rezaei N, Liontos M, Karakaidos P, Kletsas D, Issaeva N, et al. Oncogeneinduced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints. Nature 2006; 444: 633-637
20. Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004; 432: 316-323
21. Lukas J, Lukas C, Bartek J. Mammalian cell cycle checkpoints: signalling pathways and their organization in space and time. DNA Repair (Amst) 2004; 3: 997-1007
22. Indovina P, Marcelli E, Di Marzo D, Casini N, Forte IM, Giorgi F, et al. Abrogating G/M checkpoint through WEE1 inhibition in combination with chemotherapy as a promising therapeutic approach for mesothelioma. Cancer Biol Ther 2013; 15: 380-388
23. Simanski S, Madoux F, Rahaim RJ, Chase P, Schurer S, Cameron M, et al. Identification of Small Molecule Inhibitors of Wee1 Degradation and Mitotic Entry. Probe Reports from the NIH Molecular Libraries Program: NIH, Bethesda, MD, USA, 2010
24. Towler WI, Zhang J, Ransburgh DJ, Toland AE, Ishioka C, Chiba N, et al. Analysis of BRCA1 variants in double-strand break repair by homologous recombination and single-strand annealing. Hum Mutat 2013; 34: 439-445
25. Hollstein M, Sidransky D, Vogelstein B, Harris CC. p53 mutations in human cancers. Science 1991; 253: 49-53
26. Michael D, Oren M. The p53 and Mdm2 families in cancer. Curr Opin Genet Dev 2002; 12: 53-59
27. Dixon H, Norbury CJ. Therapeutic exploitation of checkpoint defects in cancer cells lacking p53 function. Cell Cycle 2002; 1: 362-368
28. Bucher N, Britten CD. G2 checkpoint abrogation and checkpoint kinase-1 targeting in the treatment of cancer. Br J Cancer 2008; 98: 523-528
29. Kawabe T. G2 checkpoint abrogators as anticancer drugs. Mol Cancer Ther 2004; 3: 513-519
30. Peters JM. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol 2006; 7: 644-656
31. Pines J. The APC/C: a smorgasbord for proteolysis. Mol Cell 2009; 34: 135-136
32. Li M, Zhang P. The function of APC/CCdh1 in cell cycle and beyond. Cell Div 2009; 4: 2
33. Pines J. Mitosis: a matter of getting rid of the right protein at the right time. Trends Cell Biol 2006; 16: 55-63
34. Garcia-Higuera I, Manchado E, Dubus P, Canamero M, Mendez J, Moreno S, et al. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat Cell Biol 2008; 10: 802-811
35. Kim HS, Vassilopoulos A, Wang RH, Lahusen T, Xiao Z, Xu X, et al. SIRT2 maintains genome integrity and suppresses tumorigenesis through regulating APC/C activity. Cancer Cell 2011; 20: 487-499
36. Saeki T, Ouchi M, Ouchi T. Physiological and oncogenic Aurora-A pathway. Int J Biol Sci 2009; 5: 758-762
37. Schmit TL, Zhong W, Nihal M, Ahmad N. Polo-like kinase 1 (Plk1) in nonmelanoma skin cancers. Cell Cycle 2009; 8: 2697-2702
38. Tominaga Y, Li C, Wang RH, Deng CX. Murine Wee1 plays a critical role in cell cycle regulation and pre-implantation stages of embryonic development. Int J Biol Sci 2006; 2: 161-170
39. Heald R, McLoughlin M, McKeon F. Human wee1 maintains mitotic timing by protecting the nucleus from cytoplasmically activated Cdc2 kinase. Cell 1993; 74: 463-474
40. Timofeev O, Cizmecioglu O, Settele F, Kempf T, Hoffmann I. Cdc25 phosphatases are required for timely assembly of CDK1-cyclin B at the G2/M transition. J Biol Chem 2010; 285: 16978-16990
41. Trovesi C, Falcettoni M, Lucchini G, Clerici M, Longhese MP. Distinct Cdk1 requirements during single-strand annealing, noncrossover, and crossover recombination. PLoS Genet 2011; 7: e1002263
42. Engelbert D, Schnerch D, Baumgarten A, Wasch R. The ubiquitin ligase APC(Cdh1) is required to maintain genome integrity in primary human cells. Oncogene 2008; 27: 907-917
43. DePinho RA. The age of cancer. Nature 2000; 408: 248-254
44. Murray AW, Solomon MJ, Kirschner MW. The role of cyclin synthesis and degradation in the control of maturation promoting factor activity. Nature 1989; 339: 280-286
45. Lianga N, Williams EC, Kennedy EK, Dore C, Pilon S, Girard SL, et al. A Wee1 checkpoint inhibits anaphase onset. J Cell Biol 2013; 201: 843-862
46. Harvey SL, Charlet A, Haas W, Gygi SP, Kellogg DR. Cdk1-dependent regulation of the mitotic inhibitor Wee1. Cell 2005; 122: 407-420
47. Simpson-Lavy KJ, Brandeis M. Clb2 and the APC/C(Cdh1) regulate Swe1 stability. Cell Cycle 2010; 9: 3046-3053
48. van Vugt MA, Bras A, Medema RH. Polo-like kinase-1 controls recovery from a G2 DNA damage-induced arrest in mammalian cells. Mol Cell 2004; 15: 799-811
49. Rajeshkumar NV, De Oliveira E, Ottenhof N, Watters J, Brooks D, Demuth T, et al. MK-1775, a potent Wee1 inhibitor, synergizes with gemcitabine to achieve tumor regressions, selectively in p53-deficient pancreatic cancer xenografts. Clin Cancer Res 2011; 17: 2799-2806
50. Hirai H, Arai T, Okada M, Nishibata T, Kobayashi M, Sakai N, et al. MK-1775, a small molecule Wee1 inhibitor, enhances anti-Tumor efficacy of various DNA-damaging agents, including 5-fluorouracil. Cancer Biol Ther 2010; 9: 514-522
51. Hirai H, Iwasawa Y, Okada M, Arai T, Nishibata T, Kobayashi M, et al. Small-molecule inhibition of Wee1 kinase by MK-1775 selectively sensitizes p53-deficient tumor cells to DNA-damaging agents. Mol Cancer Ther 2009; 8: 2992-3000
52. Wang Y, Decker SJ, Sebolt-Leopold J. Knockdown of Chk1, Wee1 and Myt1 by RNA interference abrogates G2 checkpoint and induces apoptosis. Cancer Biol Ther 2004; 3: 305-313
53. Posthumadeboer J, Wurdinger T, Graat HC, van Beusechem VW, Helder MN, van Royen BJ, et al. WEE1 inhibition sensitizes osteosarcoma to radiotherapy. BMC Cancer 2011; 11: 156
54. Wang Y, Li J, Booher RN, Kraker A, Lawrence T, Leopold WR, et al. Radiosensitization of p53 mutant cells by PD0166285, a novel G(2) checkpoint abrogator. Cancer Res 2001; 61: 8211-8217
55. Iorns E, Lord CJ, Grigoriadis A, McDonald S, Fenwick K, Mackay A, et al. Integrated functional, gene expression and genomic analysis for the identification of cancer targets. PLoS ONE 2009; 4: e5120
56. Mir SE, De Witt Hamer PC, Krawczyk PM, Balaj L, Claes A, Niers JM, et al. In silico analysis of kinase expression identifies WEE1 as a gatekeeper against mitotic catastrophe in glioblastoma. Cancer Cell 2010; 18: 244-257
57. Dine J, Deng CX. Mouse models of BRCA1 and their application to breast cancer research. Cancer Metastasis Rev 2013; 32: 25-37
58. Robinson GW, Hennighausen L. MMTV-Cre transgenes can adversely affect lactation: considerations for conditional gene deletion in mammary tissue. Anal Biochem 2011; 412: 92-95
59. Wagner KU, Wall RJ, St-Onge L, Gruss P, Wynshaw-Boris A, Garrett L, et al. Cre-mediated gene deletion in the mammary gland. Nucleic Acids Res 1997; 25: 4323-4330
60. Hayashi S, McMahon AP. Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 2002; 244: 305-318