The tumor suppressor tuberin regulates mitotic onset through the cellular localization of cyclin B1

Cell Cycle

Volumn 10, Issue 18, 2011, Pages 3129-3139

  Da Silva, Elizabeth Fidalgo ^a   Ansari, Shora B ^b   Maimaiti, Jiamila ^a   Barnes, Elizabeth A ^c   Kong Beltran, Monica ^d   Donoghue, Daniel J ^b   Porter, Lisa A ^a  

^a UNIVERSITY OF WINDSOR   (Canada)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^d GENENTECH INC   (United States)

Author keywords

Cancer; Cdk1; Cell cycle; Hamartin; Hamartoma; TSC2

Indexed keywords

CYCLIN B1; RAPAMYCIN; TUBERIN;

ANIMAL CELL; ARTICLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE REGULATION; CELL DEATH; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MISSENSE MUTATION; MITOSIS; MOUSE; NONHUMAN; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; TUBEROUS SCLEROSIS;

EID: 80052878665     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.10.18.17296     Document Type: Article

References (38)

1. Cheadle JP, Reeve MP, Sampson JR, Kwiatkowski DJ. Molecular genetic advances in tuberous sclerosis. Hum Genet 2000; 107:97-114; PMID:11030407.
2. Dabora SL, Jozwiak S, Franz DN, Roberts PS, Nieto A, Chung J, et al. Mutational analysis in a cohort of 224 tuberous sclerosis patients indicates increased severity of TSC2, compared with TSC1, disease in multiple organs. Am J Hum Genet 2001; 68:64-80; PMID:11112665.
3. Jiang WG, Sampson J, Martin TA, Lee-Jones L, Watkins G, Douglas-Jones A, et al. Tuberin and hamartin are aberrantly expressed and linked to clinical outcome in human breast cancer: the role of promoter methylation of TSC genes. Eur J Cancer 2005; 41:1628-36; PMID:15951164.
4. Parry L, Maynard JH, Patel A, Clifford SC, Morrissey C, Maher ER, et al. Analysis of the TSC1 and TSC2 genes in sporadic renal cell carcinomas. Br J Cancer 2001; 85:1226-30; PMID:11710839.
5. Suzuki K, Ogura T, Yokose T, Nagai K, Mukai K, Kodama T, et al. Loss of heterozygosity in the tuberous sclerosis gene associated regions in adenocarcinoma of the lung accompanied by multiple atypical adenomatous hyperplasia. Int J Cancer 1998; 79:384-9; PMID:9699531.
6. Soucek T, Pusch O, Wienecke R, DeClue JE, Hengstschlager M. Role of the tuberous sclerosis gene-2 product in cell cycle control. Loss of the tuberous sclerosis gene-2 induces quiescent cells to enter S phase. J BiolChem 1997; 272:29301-8; PMID:9361010.
7. Tee AR, Manning BD, Roux PP, Cantley LC, Blenis J. Tuberous sclerosis complex gene products, tuberin and Hamartin, control mTOR signaling by acting as a GTPase-activating protein complex toward Rheb. Curr Biol 2003; 13:1259-68; PMID:12906785.
8. Soucek T, Holzl G, Bernaschek G, Hengstschlager M. A role of the tuberous sclerosis gene-2 product during neuronal differentiation. Oncogene 1998; 16:2197-204; PMID:9619828.
9. Astrinidis A, Senapedis W, Henske EP. Hamartin, the tuberous sclerosis complex 1 gene product, interacts with polo-like kinase 1 in a phosphorylation-dependent manner. Hum Mol Genet 2006; 15:287-97; PMID:16339216.
10. Astrinidis A, Senapedis W, Coleman TR, Henske EP. Cell cycle-regulated phosphorylation of hamartin, the product of the tuberous sclerosis complex 1 gene, by cyclin-dependent kinase 1/cyclin B. J Biol Chem 2003; 278:51372-9; PMID:14551205.
11. 2/M cyclin-dependent kinase CDK1 and its regulatory cyclins A and B. J Neuropathol Exp Neurol 2001; 60:711-23; PMID:11444800.
12. Petersen J, Nurse P. TOR signalling regulates mitotic commitment through the stress MAP kinase pathway and the Polo and Cdc2 kinases. Nat Cell Biol 2007; 9:1263-72; PMID:17952063.
13. cdc2. Cell 1989; 58:833-46; PMID:2570636.
14. Porter LA, Donoghue DJ. Cyclin B1 and CDK1: nuclear localization and upstream regulators. Prog Cell Cycle Res 2003; 5:335-47; PMID:14593728.
15. Jackman M, Lindon C, Nigg EA, Pines J. Active cyclin B1-Cdk1 first appears on centrosomes in prophase. Nat Cell Biol 2003; 5:143-8; PMID:12524548.
16. Gavet O, Pines J. Activation of cyclin B1-Cdk1 synchronizes events in the nucleus and the cytoplasm at mitosis. J Cell Biol 2010; 189:247-59; PMID:20404109.
17. Hagting A, Karlsson C, Clute P, Jackman M, Pines J. MPF localization is controlled by nuclear export. EMBO J 1998; 17:4127-38; PMID:9670027.
18. Toyoshima-Morimoto F, Taniguchi E, Shinya N, Iwamatsu A, Nishida E. Polo-like kinase 1 phosphorylates cyclin B1 and targets it to the nucleus during prophase. Nature 2001; 410:215-20; PMID:11242082.
19. Jones AC, Shyamsundar MM, Thomas MW, Maynard J, Idziaszczyk S, Tomkins S, et al. Comprehensive mutation analysis of TSC1 and TSC2-and phenotypic correlations in 150 families with tuberous sclerosis. Am J Hum Genet 1999; 64:1305-15; PMID:10205261.
20. Li J, Meyer AN, Donoghue DJ. Nuclear localization of cyclin B1 mediates its biological activity and is regulated by phosphorylation. Proc Natl Acad Sci USA 1997; 94:502-7; PMID:9012813.
21. Hodges AK, Li S, Maynard J, Parry L, Braverman R, Cheadle JP, et al. Pathological mutations in TSC1 and TSC2 disrupt the interaction between hamartin and tuberin. Hum Mol Genet 2001; 10:2899-905; PMID:11741833.
22. van Slegtenhorst M, Nellist M, Nagelkerken B, Cheadle J, Snell R, van den Ouweland A, et al. Interaction between hamartin and tuberin, the TSC1 and TSC2 gene products. Hum Mol Genet 1998; 7:1053-7; PMID:9580671.
23. Xiao GH, Shoarinejad F, Jin F, Golemis EA, Yeung RS. The tuberous sclerosis 2 gene product, tuberin, functions as a Rab5 GTPase activating protein (GAP) in modulating endocytosis. J BiolChem 1997; 272:6097-100; PMID:9045618.
24. Aicher LD, Campbell JS, Yeung RS. Tuberin phosphorylation regulates its interaction with hamartin. Two proteins involved in tuberous sclerosis. J Biol Chem 2001; 276:21017-21; PMID:11290735.
25. Nellist M, Verhaaf B, Goedbloed MA, Reuser AJ, van den Ouweland AM, Halley DJ. TSC2 missense mutations inhibit tuberin phosphorylation and prevent formation of the tuberin-hamartin complex. Hum Mol Genet 2001; 10:2889-98; PMID:11741832.
26. Hagting A, Jackman M, Simpson K, Pines J. Translocation of cyclin B1 to the nucleus at prophase requires a phosphorylation-dependent nuclear import signal. Curr Biol 1999; 9:680-9; PMID:10395539.
27. Yang J, Bardes ES, Moore JD, Brennan J, Powers MA, Kornbluth S. Control of cyclin B1 localization through regulated binding of the nuclear export factor CRM1. Genes Dev 1998; 12:2131-43; PMID:9679058.
28. Govindarajan B, Brat DJ, Csete M, Martin WD, Murad E, Litani K, et al. Transgenic expression of dominant negative tuberin through a strong constitutive promoter results in a tissue-specific tuberous sclerosis phenotype in the skin and brain. J Biol Chem 2005; 280:5870-4; PMID:15576369.
29. Kip1 localization. Cancer Res 2009; 69:7224-34; PMID:19738049.
30. Porter LA, Singh G, Lee JM. Abundance of cyclin B1 regulates gamma-radiation-induced apoptosis. Blood 2000; 95:2645-50; PMID:10753846.
31. Yuan J, Eckerdt F, Bereiter-Hahn J, Kurunci-Csacsko E, Kaufmann M, Strebhardt K. Cooperative phosphorylation including the activity of polo-like kinase 1 regulates the subcellular localization of cyclin B1. Oncogene 2002; 21:8282-92; PMID:12447691.
32. Gómez-Baldo L, Schmidt S, Maxwell CA, Bonifaci N, Gabaldon T, Vidalain PO, et al. TACC3-TSC2 maintains nuclear envelope structure and controls cell division. Cell Cycle 2010; 9:1143-55; PMID:20237422.
33. Ertych N, Bastians H. Interaction of TACC3 and TSC2 at the nuclear envelope and mitotic structures. Cell Cycle 2010; 9:1233; PMID:20404524.
34. Ito N, Rubin GM. gigas, a Drosophila homolog of tuberous sclerosis gene product-2, regulates the cell cycle. Cell 1999; 96:529-39; PMID:10052455.
35. Castedo M, Perfettini JL, Roumier T, Andreau K, Medema R, Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene 2004; 23:2825-37; PMID:15077146.
36. Kong M, Barnes EA, Ollendorff V, Donoghue DJ. Cyclin F regulates the nuclear localization of cyclin B1 through a cyclin-cyclin interaction. EMBO J 2000; 19:1378-88; PMID:10716937.
37. Vojtek AB, Hollenberg SM. Ras-Raf interaction: two-hybrid analysis. Methods Enzymol 1995; 255:331-42; PMID:8524119.
38. Vojtek AB, Hollenberg SM, Cooper JA. Mammalian Ras interacts directly with the serine/threonine kinase Raf. Cell 1993; 74:205-14; PMID:8334704.