Deregulated proteolysis by the F-box proteins SKP2 and β-TrCP: tipping the scales of cancer (original) (raw)
Hershko, A. The ubiquitin system for protein degradation and some of its roles in the control of the cell-division cycle (Nobel lecture). Angew. Chem. Int. Ed. Engl.44, 5932–5943 (2005). An historical perspective about the discovery of the ubiquitin system that describes how E1, E2 and E3 enzymes work together to promote ubiquitin ligation to substrates. ArticleCASPubMed Google Scholar
Petroski, M. D. & Deshaies, R. J. Function and regulation of cullin-RING ubiquitin ligases. Nature Rev. Mol. Cell Biol.6, 9–20 (2005). An excellent review of cullin RING ubiquitin ligases. ArticleCAS Google Scholar
Cardozo, T. & Pagano, M. The SCF ubiquitin ligase: insights into a molecular machine. Nature Rev. Mol. Cell Biol.5, 739–751 (2004). ArticleCAS Google Scholar
Cenciarelli, C. et al. Identification of a family of human F-box proteins. Curr. Biol.9, 1177–1179 (1999). ArticleCASPubMed Google Scholar
Winston, J. T., Koepp, D. M., Zhu, C., Elledge, S. J. & Harper, J. W. A family of mammalian F-box proteins. Curr. Biol.9, 1180–1182 (1999). References 4–6 classify the mammalian family of F-box proteins. ArticleCASPubMed Google Scholar
Welcker, M. & Clurman, B. E. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nature Rev. Cancer8, 83–93 (2007). An excellent and up-to-date review about FBXW7 and its role in cancer. ArticleCAS Google Scholar
Malumbres, M. & Barbacid, M. Cell cycle kinases in cancer. Curr. Opin. Genet. Dev.17, 60–65 (2007). ArticleCASPubMed Google Scholar
Guardavaccaro, D. & Pagano, M. Stabilizers and destabilizers controlling cell cycle oscillators. Mol. Cell22, 1–4 (2006). ArticleCASPubMed Google Scholar
Branzei, D. & Foiani, M. Regulation of DNA repair throughout the cell cycle. Nature Rev. Mol. Cell Biol.9, 297–308 (2008). ArticleCAS Google Scholar
Zhang, H., Kobayashi, R., Galaktionov, K. & Beach, D. p19Skp1 and p45Skp2 are essential elements of the cyclin A–CDK2 S phase kinase. Cell82, 915–925 (1995). ArticleCASPubMed Google Scholar
Carrano, A. C., Eytan, E., Hershko, A. & Pagano, M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nature Cell Biol.1, 193–199 (1999). ArticleCASPubMed Google Scholar
Sutterluty, H. et al. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nature Cell Biol.1, 207–214 (1999). ArticleCASPubMed Google Scholar
Tsvetkov, L. M., Yeh, K. H., Lee, S. J., Sun, H. & Zhang, H. p27Kip1 ubiquitination and degradation is regulated by the SCFSkp2 complex through phosphorylated Thr187 in p27. Curr. Biol.9, 661–664 (1999). References 12–14 characterize the function of SKP2 in cell cycle control and the ubiquitin-mediated degradation of the tumour suppressor p27. ArticleCASPubMed Google Scholar
Spruck, C. et al. A CDK-independent function of mammalian Cks1: targeting of SCFSkp2 to the CDK inhibitor p27Kip1. Mol. Cell7, 639–650 (2001). ArticleCASPubMed Google Scholar
Ganoth, D. et al. The cell-cycle regulatory protein Cks1 is required for SCFSkp2-mediated ubiquitinylation of p27. Nature Cell Biol.3, 321–324 (2001). ArticleCASPubMed Google Scholar
Bloom, J. & Pagano, M. Deregulated degradation of the cdk inhibitor p27 and malignant transformation. Semin. Cancer Biol.13, 41–47 (2003). ArticleCASPubMed Google Scholar
Nakayama, K. et al. Targeted disruption of Skp2 results in accumulation of cyclin E and p27Kip1, polyploidy and centrosome overduplication. EMBO J.19, 2069–2081 (2000). Shows that deletion ofSKP2results in accumulation of p27in vivo. ArticleCASPubMedPubMed Central Google Scholar
Nakayama, K. et al. Skp2-mediated degradation of p27 regulates progression into mitosis. Dev. Cell6, 661–672 (2004). Shows that p27 loss reverts most of the phenotypes that are due to SKP2-deficiency and that the SKP2–p27 axis functions not only at G1–S, but also at G2–M. ArticleCASPubMed Google Scholar
Bornstein, G. et al. Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S. phase. J. Biol. Chem.278, 25752–25757 (2003). ArticleCASPubMed Google Scholar
Yu, Z. K., Gervais, J. L. & Zhang, H. Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21CIP1/WAF1 and cyclin D proteins. Proc. Natl Acad. Sci. USA95, 11324–11329 (1998). The first evidence that SKP2 targets p21, a tumour suppressor protein, for degradation. ArticleCASPubMedPubMed Central Google Scholar
Kamura, T. et al. Degradation of p57Kip2 mediated by SCFSkp2-dependent ubiquitylation. Proc. Natl Acad. Sci. USA100, 10231–10236 (2003). ArticleCASPubMedPubMed Central Google Scholar
Hiramatsu, Y. et al. Degradation of Tob1 mediated by SCFSkp2-dependent ubiquitination. Cancer Res.66, 8477–8483 (2006). ArticleCASPubMed Google Scholar
Song, M. S. et al. Skp2 regulates the antiproliferative function of the tumor suppressor RASSF1A via ubiquitin-mediated degradation at the G(1)–S transition. Oncogene 10 Dec 2007 (doi:10.1038/sj.onc.1210971).
Tedesco, D., Lukas, J. & Reed, S. I. The pRb-related protein p130 is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCFSkp2. Genes Dev.16, 2946–2957 (2002). ArticleCASPubMedPubMed Central Google Scholar
Huang, H. et al. Skp2 inhibits FOXO1 in tumor suppression through ubiquitin-mediated degradation. Proc. Natl Acad. Sci. USA102, 1649–1654 (2005). Identifies FOXO1 as a substrate of SKP2 and suggests SKP2-promoted proteolysis might have a role in tumorigenesis. ArticleCASPubMedPubMed Central Google Scholar
Tokarz, S. et al. The ISG15 isopeptidase UBP43 is regulated by proteolysis via the SCFSkp2 ubiquitin ligase. J. Biol. Chem.279, 46424–46430 (2004). ArticleCASPubMed Google Scholar
Garriga, J. et al. CDK9 is constitutively expressed throughout the cell cycle, and its steady-state expression is independent of SKP2. Mol. Cell. Biol.23, 5165–5173 (2003). ArticleCASPubMedPubMed Central Google Scholar
Kiernan, R. E. et al. Interaction between cyclin T1 and SCFSKP2 targets CDK9 for ubiquitination and degradation by the proteasome. Mol. Cell. Biol.21, 7956–7970 (2001). ArticleCASPubMedPubMed Central Google Scholar
Carrano, A. C. & Pagano, M. Role of the F-box protein Skp2 in adhesion-dependent cell cycle progression. J. Cell Biol.153, 1381–1390 (2001). ArticleCASPubMedPubMed Central Google Scholar
Signoretti, S. et al. Oncogenic role of the ubiquitin ligase subunit Skp2 in human breast cancer. J. Clin. Invest.110, 633–641 (2002). ArticleCASPubMedPubMed Central Google Scholar
Waltregny, D. et al. Androgen-driven prostate epithelial cell proliferation and differentiation in vivo involve the regulation of p27. Mol. Endocrinol.15, 765–782 (2001). ArticleCASPubMed Google Scholar
Lu, L., Schulz, H. & Wolf, D. A. The F-box protein SKP2 mediates androgen control of p27 stability in LNCaP human prostate cancer cells. BMC Cell Biol.3, 22 (2002). ArticleCASPubMedPubMed Central Google Scholar
Kang-Decker, N. et al. Loss of CBP causes T cell lymphomagenesis in synergy with p27Kip1 insufficiency. Cancer Cell5, 177–189 (2004). ArticleCASPubMed Google Scholar
Shim, E. H. et al. Expression of the F-box protein SKP2 induces hyperplasia, dysplasia, and low-grade carcinoma in the mouse prostate. Cancer Res.63, 1583–1588 (2003). CASPubMed Google Scholar
Radke, S., Pirkmaier, A. & Germain, D. Differential expression of the F-box proteins Skp2 and Skp2B in breast cancer. Oncogene24, 3448–3458 (2005). ArticleCASPubMed Google Scholar
Timmerbeul, I. et al. Testing the importance of p27 degradation by the SCFskp2 pathway in murine models of lung and colon cancer. Proc. Natl Acad. Sci. USA103, 14009–14014 (2006). ArticleCASPubMedPubMed Central Google Scholar
Keller, U. B. et al. Myc targets Cks1 to provoke the suppression of p27Kip1, proliferation and lymphomagenesis. EMBO J.26, 2562–2574 (2007). ArticleCASPubMedPubMed Central Google Scholar
Philipp-Staheli, J., Payne, S. R. & Kemp, C. J. p27Kip1: regulation and function of a haploinsufficient tumor suppressor and its misregulation in cancer. Exp. Cell Res.264, 148–168 (2001). ArticleCASPubMed Google Scholar
Shapira, M. et al. The prognostic impact of the ubiquitin ligase subunits Skp2 and Cks1 in colorectal carcinoma. Cancer103, 1336–1346 (2005). ArticleCASPubMed Google Scholar
Shapira, M. et al. Alterations in the expression of the cell cycle regulatory protein cyclin kinase subunit 1 in colorectal carcinoma. Cancer100, 1615–1621 (2004). ArticleCASPubMed Google Scholar
Masuda, T. A. et al. Cyclin-dependent kinase 1 gene expression is associated with poor prognosis in gastric carcinoma. Clin. Cancer Res.9, 5693–5698 (2003). CASPubMed Google Scholar
Hershko, D. D. & Shapira, M. Prognostic role of p27Kip1 deregulation in colorectal cancer. Cancer107, 668–675 (2006). ArticleCASPubMed Google Scholar
Kamura, T. et al. Cytoplasmic ubiquitin ligase KPC regulates proteolysis of p27Kip1 at G1 phase. Nature Cell Biol.6, 1229–1235 (2004). ArticleCASPubMed Google Scholar
Hattori, T. et al. Pirh2 promotes ubiquitin-dependent degradation of the cyclin-dependent kinase inhibitor p27Kip1. Cancer Res.67, 10789–10795 (2007). ArticleCASPubMed Google Scholar
Goto, T. et al. Mechanism and functional consequences of loss of FOXO1 expression in endometrioid endometrial cancer cells. Oncogene27, 9–19 (2008). ArticleCASPubMed Google Scholar
Bellan, C. et al. Missing expression of pRb2/p130 in human retinoblastomas is associated with reduced apoptosis and lesser differentiation. Invest. Ophthalmol. Vis. Sci.43, 3602–3608 (2002). PubMed Google Scholar
Caputi, M. et al. Loss of pRb2/p130 expression is associated with unfavorable clinical outcome in lung cancer. Clin. Cancer Res.8, 3850–3856 (2002). CASPubMed Google Scholar
D'Andrilli, G. et al. Frequent loss of pRb2/p130 in human ovarian carcinoma. Clin. Cancer Res.10, 3098–3103 (2004). ArticleCASPubMed Google Scholar
Helin, K. et al. Loss of the retinoblastoma protein-related p130 protein in small cell lung carcinoma. Proc. Natl Acad. Sci. USA94, 6933–6938 (1997). ArticleCASPubMedPubMed Central Google Scholar
Scambia, G., Lovergine, S. & Masciullo, V. RB family members as predictive and prognostic factors in human cancer. Oncogene25, 5302–5308 (2006). ArticleCASPubMed Google Scholar
Susini, T. et al. Expression of the retinoblastoma-related gene Rb2/p130 correlates with clinical outcome in endometrial cancer. J. Clin. Oncol.16, 1085–1093 (1998). ArticleCASPubMed Google Scholar
Zamparelli, A. et al. Expression of cell-cycle-associated proteins pRB2/p130 and p27kip in vulvar squamous cell carcinomas. Hum. Pathol.32, 4–9 (2001). ArticleCASPubMed Google Scholar
Soldatenkov, V. A., Dritschilo, A., Ronai, Z. & Fuchs, S. Y. Inhibition of homologue of Slimb (HOS) function sensitizes human melanoma cells for apoptosis. Cancer Res.59, 5085–5088 (1999). CASPubMed Google Scholar
Busino, L. et al. Degradation of Cdc25A by β-TrCP during S phase and in response to DNA damage. Nature426, 87–91 (2003). ArticleCASPubMed Google Scholar
Tang, W. et al. Targeting β-transducin repeat-containing protein E3 ubiquitin ligase augments the effects of antitumor drugs on breast cancer cells. Cancer Res.65, 1904–1908 (2005). ArticleCASPubMed Google Scholar
Guardavaccaro, D. et al. Control of meiotic and mitotic progression by the F box protein β-Trcp1 in vivo. Dev. Cell4, 799–812 (2003). ArticleCASPubMed Google Scholar
Nakayama, K. et al. Impaired degradation of inhibitory subunit of NF-κB (IκB) and β-catenin as a result of targeted disruption of the β-TrCP1 gene. Proc. Natl Acad. Sci. USA100, 8752–8757 (2003). ArticleCASPubMedPubMed Central Google Scholar
Mailand, N., Bekker-Jensen, S., Bartek, J. & Lukas, J. Destruction of Claspin by SCFβTrCP restrains Chk1 activation and facilitates recovery from genotoxic stress. Mol. Cell23, 307–318 (2006). ArticleCASPubMed Google Scholar
Peschiaroli, A. et al. SCFβTrCP-mediated degradation of Claspin regulates recovery from the DNA replication checkpoint response. Mol. Cell23, 319–329 (2006). ArticleCASPubMed Google Scholar
Watanabe, N. et al. M-phase kinases induce phospho-dependent ubiquitination of somatic Wee1 by SCFβ-TrCP. Proc. Natl Acad. Sci. USA101, 4419–4424 (2004). ArticleCASPubMedPubMed Central Google Scholar
Ougolkov, A. et al. Associations among β-TrCP, an E3 ubiquitin ligase receptor, β-catenin, and NF-κB in colorectal cancer. J. Natl Cancer Inst.96, 1161–1170 (2004). ArticleCASPubMed Google Scholar
Muerkoster, S. et al. Increased expression of the E3-ubiquitin ligase receptor subunit βTRCP1 relates to constitutive nuclear factor-κB activation and chemoresistance in pancreatic carcinoma cells. Cancer Res.65, 1316–1324 (2005). ArticlePubMed Google Scholar
Koch, A. et al. Elevated expression of Wnt antagonists is a common event in hepatoblastomas. Clin. Cancer Res.11, 4295–4304 (2005). ArticleCASPubMed Google Scholar
Spiegelman, V. S. et al. Induction of homologue of Slimb ubiquitin ligase receptor by mitogen signaling. J. Biol. Chem.277, 36624–36630 (2002). ArticleCASPubMed Google Scholar
Kudo, Y. et al. Role of F-box protein βTrcp1 in mammary gland development and tumorigenesis. Mol. Cell. Biol.24, 8184–8194 (2004). Shows that β-TrCP1 positively controls the proliferation of breast epithelium and its overexpression induces transformation in the breast epithelium. ArticleCASPubMedPubMed Central Google Scholar
Karin, M. & Greten, F. R. NF-κB: linking inflammation and immunity to cancer development and progression. Nature Rev. Immunol.5, 749–759 (2005). ArticleCAS Google Scholar
Wu, C. & Ghosh, S. β-TrCP mediates the signal-induced ubiquitination of IκBβ. J. Biol. Chem.274, 29591–29594 (1999). ArticleCASPubMed Google Scholar
Shirane, M., Hatakeyama, S., Hattori, K., Nakayama, K. & Nakayama, K. Common pathway for the ubiquitination of IκBα, IκBβ, and IκBε mediated by the F-box protein FWD1. J. Biol. Chem.274, 28169–28174 (1999). ArticleCASPubMed Google Scholar
Tan, P. et al. Recruitment of a ROC1-CUL1 ubiquitin ligase by Skp1 and HOS to catalyze the ubiquitination of IκBα. Mol. Cell3, 527–533 (1999). One of the first papers showing that the SCF contains the RING-finger protein RBX1 and that an SCF containing β-TrCP targets IκBα for degradation. ArticleCASPubMed Google Scholar
Kroll, M. et al. Inducible degradation of IkBa by the proteasome requires interaction with the F-box protein h-βTrCP. J. Biol. Chem.274, 7941–7945 (1999). ArticleCASPubMed Google Scholar
Spencer, E., Jiang, J. & Chen, Z. J. Signal-induced ubiquitination of IκBα by the F-box protein Slimb/β-TrCP. Genes Dev.13, 284–294 (1999). ArticleCASPubMedPubMed Central Google Scholar
Winston, J. T. et al. The SCFβ-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IκBα and β-catenin and stimulates IκBα ubiquitination in vitro. Genes Dev.13, 270–283 (1999). ArticleCASPubMedPubMed Central Google Scholar
Yaron, A. et al. Identification of the receptor component of the IκBα-ubiquitin ligase. Nature396, 590–594 (1998). ArticleCASPubMed Google Scholar
Hatakeyama, S. et al. Ubiquitin-dependent degradation of IκBα a is mediated by a ubiquitin ligase Skp1/Cul1/F-box protein FWD1. Proc. Natl Acad. Sci. USA96, 3859–3863 (1999). ArticleCASPubMedPubMed Central Google Scholar
Arsura, M. & Cavin, L. G. Nuclear factor-κB and liver carcinogenesis. Cancer Lett.229, 157–169 (2005). ArticleCASPubMed Google Scholar
Pikarsky, E. et al. NF-κB functions as a tumour promoter in inflammation-associated cancer. Nature431, 461–466 (2004). ArticleCASPubMed Google Scholar
Dhawan, P. & Richmond, A. A novel NF-κB-inducing kinase-MAPK signaling pathway up-regulates NF-κB activity in melanoma cells. J. Biol. Chem.277, 7920–7928 (2002). ArticleCASPubMed Google Scholar
Liu, J. et al. Oncogenic BRAF regulates β-Trcp expression and NF-κB activity in human melanoma cells. Oncogene26, 1954–1958 (2007). ArticleCASPubMed Google Scholar
Yang, H. S. et al. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol. Cell. Biol.23, 26–37 (2003). ArticlePubMedPubMed CentralCAS Google Scholar
Dorrello, N. V. et al. S6K1- and βTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science314, 467–471 (2006). ArticleCASPubMed Google Scholar
Afonja, O., Juste, D., Das, S., Matsuhashi, S. & Samuels, H. H. Induction of PDCD4 tumor suppressor gene expression by RAR agonists, antiestrogen and HER-2/neu antagonist in breast cancer cells. Evidence for a role in apoptosis. Oncogene23, 8135–8145 (2004). ArticleCASPubMed Google Scholar
Goke, R., Barth, P., Schmidt, A., Samans, B. & Lankat-Buttgereit, B. Programmed cell death protein 4 suppresses CDK1/cdc2 via induction of p21Waf1/Cip1. Am. J. Physiol. Cell Physiol.287, C1541–C1546 (2004). ArticleCASPubMed Google Scholar
Wen, Y. H. et al. Alterations in the expression of PDCD4 in ductal carcinoma of the breast. Oncol. Rep.18, 1387–1393 (2007). CASPubMed Google Scholar
Zhang, H. et al. Involvement of programmed cell death 4 in transforming growth factor-β1-induced apoptosis in human hepatocellular carcinoma. Oncogene25, 6101–6112 (2006). ArticleCASPubMed Google Scholar
Mudduluru, G. et al. Loss of programmed cell death 4 expression marks adenoma-carcinoma transition, correlates inversely with phosphorylated protein kinase B, and is an independent prognostic factor in resected colorectal cancer. Cancer110, 1697–1707 (2007). ArticleCASPubMed Google Scholar
Chen, Y. et al. Loss of PDCD4 expression in human lung cancer correlates with tumour progression and prognosis. J. Pathol.200, 640–646 (2003). ArticleCASPubMed Google Scholar
Majumder, S. REST in good times and bad: roles in tumor suppressor and oncogenic activities. Cell Cycle5, 1929–1935 (2006). ArticleCASPubMed Google Scholar
Westbrook, T. F. et al. A genetic screen for candidate tumor suppressors identifies REST. Cell121, 837–848 (2005). ArticleCASPubMed Google Scholar
Westbrook, T. F. et al. SCFβ-TRCP controls oncogenic transformation and neural differentiation through REST degradation. Nature452, 370–374 (2008). ArticleCASPubMedPubMed Central Google Scholar
Saitoh, T. & Katoh, M. Expression profiles of βTRCP1 and βTRCP2, and mutation analysis of βTRCP2 in gastric cancer. Int. J. Oncol.18, 959–964 (2001). CASPubMed Google Scholar
Kim, C. J. et al. Somatic mutations of the β-TrCP gene in gastric cancer. Apmis115, 127–133 (2007). ArticleCASPubMed Google Scholar
Gerstein, A. V. et al. APC/CTNNB1 (β-catenin) pathway alterations in human prostate cancers. Genes Chromosomes Cancer34, 9–16 (2002). ArticleCASPubMed Google Scholar
Wood, L. D. et al. The genomic landscapes of human breast and colorectal cancers. Science318, 1108–1113 (2007). ArticleCASPubMed Google Scholar
Liu, C. et al. β-Trcp couples β-catenin phosphorylation-degradation and regulates Xenopus axis formation. Proc. Natl Acad. Sci. USA96, 6273–6278 (1999). ArticleCASPubMedPubMed Central Google Scholar
Lagna, G., Carnevali, F., Marchioni, M. & Hemmati-Brivanlou, A. Negative regulation of axis formation and Wnt signaling in Xenopus embryos by the F-box/WD40 protein βTrCP. Mech. Dev.80, 101–106 (1999). ArticleCASPubMed Google Scholar
Hart, M. et al. The F-box protein β-TrCP associates with phosphorylated β-catenin and regulates its activity in the cell. Curr. Biol.9, 207–210 (1999). ArticleCASPubMed Google Scholar
Latres, E., Chiaur, D. S. & Pagano, M. The human F box protein β-Trcp associates with the Cul1/Skp1 complex and regulates the stability of β-catenin. Oncogene18, 849–854 (1999). ArticleCASPubMed Google Scholar
Marikawa, Y. & Elinson, R. P. β-TrCP is a negative regulator of Wnt/β-catenin signaling pathway and dorsal axis formation in Xenopus embryos. Mech. Dev.77, 75–80 (1998). ArticleCASPubMed Google Scholar
Li, Y. et al. Stabilization of prolactin receptor in breast cancer cells. Oncogene25, 1896–1902 (2006). ArticleCASPubMed Google Scholar
Fuller, G. N. et al. Many human medulloblastoma tumors overexpress repressor element-1 silencing transcription (REST)/neuron-restrictive silencer factor, which can be functionally countered by REST-VP16. Mol. Cancer Ther.4, 343–349 (2005). CASPubMed Google Scholar
Su, X., Kameoka, S., Lentz, S. & Majumder, S. Activation of REST/NRSF target genes in neural stem cells is sufficient to cause neuronal differentiation. Mol. Cell. Biol.24, 8018–8025 (2004). ArticleCASPubMedPubMed Central Google Scholar
Lawinger, P. et al. The neuronal repressor REST/NRSF is an essential regulator in medulloblastoma cells. Nature Med.6, 826–831 (2000). ArticleCASPubMed Google Scholar
Kanemori, Y., Uto, K. & Sagata, N. β-TrCP recognizes a previously undescribed nonphosphorylated destruction motif in Cdc25A and Cdc25B phosphatases. Proc. Natl Acad. Sci. USA102, 6279–6284 (2005). ArticleCASPubMedPubMed Central Google Scholar
Boutros, R., Lobjois, V. & Ducommun, B. CDC25 phosphatases in cancer cells: key players? Good targets? Nature Rev. Cancer7, 495–507 (2007). ArticleCAS Google Scholar
Cangi, M. G. et al. Role of the Cdc25A phosphatase in human breast cancer. J. Clin. Invest.106, 753–761 (2000). ArticleCAS Google Scholar
Kristjansdottir, K. & Rudolph, J. Cdc25 phosphatases and cancer. Chem. Biol.11, 1043–1051 (2004). ArticleCASPubMed Google Scholar
Hernandez, S. et al. Cdc25 cell cycle-activating phosphatases and c-myc expression in human non-Hodgkin's lymphomas. Cancer Res.58, 1762–1767 (1998). CASPubMed Google Scholar
Hernandez, S. et al. Cdc25a and the splicing variant cdc25b2, but not cdc25B1, -B3 or -C, are over-expressed in aggressive human non-Hodgkin's lymphomas. Int. J. Cancer89, 148–152 (2000). ArticleCASPubMed Google Scholar
Ito, Y. et al. Cdc25A and cdc25B expression in malignant lymphoma of the thyroid: correlation with histological subtypes and cell proliferation. Int. J. Mol. Med.13, 431–435 (2004). CASPubMed Google Scholar
Loffler, H. et al. Distinct modes of deregulation of the proto-oncogenic Cdc25A phosphatase in human breast cancer cell lines. Oncogene22, 8063–8071 (2003). ArticlePubMedCAS Google Scholar
Hsu, J. Y., Reimann, J. D., Sorensen, C. S., Lukas, J. & Jackson, P. K. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APCCdh1. Nature Cell Biol.4, 358–366 (2002). ArticleCASPubMed Google Scholar
Gutgemann, I., Lehman, N. L., Jackson, P. K. & Longacre, T. A. Emi1 protein accumulation implicates misregulation of the anaphase promoting complex/cyclosome pathway in ovarian clear cell carcinoma. Mod. Pathol.21, 445–454 (2008). ArticlePubMedCAS Google Scholar
Lehman, N. L. et al. Oncogenic regulators and substrates of the anaphase promoting complex/cyclosome are frequently overexpressed in malignant tumors. Am. J. Pathol.170, 1793–1805 (2007). ArticleCASPubMedPubMed Central Google Scholar
Adams, J. & Kauffman, M. Development of the proteasome inhibitor Velcade (Bortezomib). Cancer Invest.22, 304–311 (2004). ArticleCASPubMed Google Scholar
Busino, L. et al. SCFFbxl3 controls the oscillation of the circadian clock by directing the degradation of cryptochrome proteins. Science316, 900–904 (2007). ArticleCASPubMed Google Scholar
Gallego, M. & Virshup, D. M. Post-translational modifications regulate the ticking of the circadian clock. Nature Rev. Mol. Cell Biol.8, 139–148 (2007). ArticleCAS Google Scholar
Frescas, D., Guardavaccaro, D., Bassermann, F., Koyama-Nasu, R. & Pagano, M. JHDM1B/FBXL10 is a nucleolar protein that represses transcription of ribosomal RNA genes. Nature450, 309–313 (2007). ArticleCASPubMed Google Scholar
Bassermann, F. et al. NIPA defines an SCF-type mammalian E3 ligase that regulates mitotic entry. Cell122, 45–57 (2005). ArticleCASPubMed Google Scholar
Amador, V., Ge, S., Santamaria, P. G., Guardavaccaro, D. & Pagano, M. APC/CCdc20 controls the ubiquitin-mediated degradation of p21 in prometaphase. Mol. Cell27, 462–473 (2007). ArticleCASPubMedPubMed Central Google Scholar
Li, X., Zhao, Q., Liao, R., Sun, P. & Wu, X. The SCFSkp2 ubiquitin ligase complex interacts with the human replication licensing factor Cdt1 and regulates Cdt1 degradation. J. Biol. Chem.278, 30854–30858 (2003). ArticleCASPubMed Google Scholar
Mendez, J. et al. Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol. Cell9, 481–491 (2002). ArticleCASPubMed Google Scholar
Moro, L., Arbini, A. A., Marra, E. & Greco, M. Up-regulation of Skp2 after prostate cancer cell adhesion to basement membranes results in BRCA2 degradation and cell proliferation. J. Biol. Chem.281, 22100–22107 (2006). ArticleCASPubMed Google Scholar
Jiang, H. et al. Ubiquitylation of RAG-2 by Skp2-SCF links destruction of the V(D)J. recombinase to the cell cycle. Mol. Cell18, 699–709 (2005). ArticleCASPubMed Google Scholar
Liu, Y. et al. The ETS protein MEF is regulated by phosphorylation-dependent proteolysis via the protein-ubiquitin ligase SCFSkp2. Mol. Cell. Biol.26, 3114–3123 (2006). ArticleCASPubMedPubMed Central Google Scholar
Liu, H., Cheng, E. H. & Hsieh, J. J. Bimodal degradation of MLL by SCFSkp2 and APCCdc20 assures cell cycle execution: a critical regulatory circuit lost in leukemogenic MLL fusions. Genes Dev.21, 2385–2398 (2007). ArticleCASPubMedPubMed Central Google Scholar
Charrasse, S., Carena, I., Brondani, V., Klempnauer, K. H. & Ferrari, S. Degradation of B-Myb by ubiquitin-mediated proteolysis: involvement of the Cdc34-SCFp45Skp2 pathway. Oncogene19, 2986–2995 (2000). ArticleCASPubMed Google Scholar
von der Lehr, N., Johansson, S. & Larsson, L. G. Implication of the ubiquitin/proteasome system in Myc-regulated transcription. Cell Cycle2, 403–407 (2003). CASPubMed Google Scholar
von der Lehr, N. et al. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol. Cell11, 1189–1200 (2003). ArticleCASPubMed Google Scholar
Marti, A., Wirbelauer, C., Scheffner, M. & Krek, W. Interaction between ubiquitin-protein ligase SCFSKP2 and E2F-1 underlies the regulation of E2F-1 degradation. Nature Cell Biol.1, 14–19 (1999). ArticleCASPubMed Google Scholar
Oh, K. J. et al. The papillomavirus E7 oncoprotein is ubiquitinated by UbcH7 and Cullin 1- and Skp2-containing E3 ligase. J. Virol.78, 5338–5346 (2004). ArticleCASPubMedPubMed Central Google Scholar
Lin, Y. W. & Yang, J. L. Cooperation of ERK and SCFSkp2 for MKP-1 destruction provides a positive feedback regulation of proliferating signaling. J. Biol. Chem.281, 915–926 (2006). ArticleCASPubMed Google Scholar
Huang, Z., Nie, L., Xu, M. & Sun, X. H. Notch-induced E2A degradation requires CHIP and Hsc70 as novel facilitators of ubiquitination. Mol. Cell. Biol.24, 8951–8962 (2004). ArticleCASPubMedPubMed Central Google Scholar
Nie, L., Xu, M., Vladimirova, A. & Sun, X. H. Notch-induced E2A ubiquitination and degradation are controlled by MAP kinase activities. EMBO J.22, 5780–5792 (2003). ArticleCASPubMedPubMed Central Google Scholar
Nie, L., Wu, H. & Sun, X. H. Ubiquitination and degradation of Tal1/SCL is induced by Notch signaling and depends on Skp2 and CHIP. J. Biol. Chem. (2007).
Sanada, T. et al. Skp2 overexpression is a p27Kip1-independent predictor of poor prognosis in patients with biliary tract cancers. Cancer Sci.95, 969–976 (2004). ArticleCASPubMed Google Scholar
Traub, F., Mengel, M., Luck, H. J., Kreipe, H. H. & von Wasielewski, R. Prognostic impact of Skp2 and p27 in human breast cancer. Breast Cancer Res. Treat99, 185–191 (2006). ArticleCASPubMed Google Scholar
Sonoda, H. et al. Significance of skp2 expression in primary breast cancer. Clin. Cancer Res.12, 1215–1220 (2006). ArticleCASPubMed Google Scholar
Narayan, G. et al. Gene dosage alterations revealed by cDNA microarray analysis in cervical cancer: identification of candidate amplified and overexpressed genes. Genes Chromosomes Cancer46, 373–384 (2007). ArticleCASPubMed Google Scholar
Nishida, N., Nagasaka, T., Kashiwagi, K., Boland, C. R. & Goel, A. High copy amplification of the Aurora-A gene is associated with chromosomal instability phenotype in human colorectal cancers. Cancer Biol. Ther.6, 525–533 (2007). ArticleCASPubMed Google Scholar
Kamata, Y. et al. High expression of skp2 correlates with poor prognosis in endometrial endometrioid adenocarcinoma. J. Cancer Res. Clin. Oncol.131, 591–596 (2005). ArticleCASPubMed Google Scholar
Lahav-Baratz, S. et al. Decreased level of the cell cycle regulator p27 and increased level of its ubiquitin ligase Skp2 in endometrial carcinoma but not in normal secretory or in hyperstimulated endometrium. Mol. Hum. Reprod.10, 567–572 (2004). ArticleCASPubMed Google Scholar
Ma, X. M., Liu, J. H., Guo, J. W., Liu, Y. & Zuo, L. F. Correlation of Skp2 expression in gastric carcinoma to expression of P27 and PTEN. Ai Zheng25, 56–61 (2006). CASPubMed Google Scholar
Ma, X. M., Liu, Y., Guo, J. W., Liu, J. H. & Zuo, L. F. Relation of overexpression of S phase kinase-associated protein 2 with reduced expression of p27 and PTEN in human gastric carcinoma. World J. Gastroenterol.11, 6716–6721 (2005). ArticlePubMedPubMed Central Google Scholar
Schiffer, D., Cavalla, P., Fiano, V., Ghimenti, C. & Piva, R. Inverse relationship between p27/Kip1 and the F-box protein Skp2 in human astrocytic gliomas by immunohistochemistry and western blot. Neurosci. Lett.328, 125–128 (2002). ArticleCASPubMed Google Scholar
Saigusa, K. et al. Overexpressed Skp2 within 5p amplification detected by array-based comparative genomic hybridization is associated with poor prognosis of glioblastomas. Cancer Sci.96, 676–683 (2005). ArticleCASPubMed Google Scholar
Penin, R. M. et al. Over-expression of p45SKP2 in Kaposi's sarcoma correlates with higher tumor stage and extracutaneous involvement but is not directly related to p27KIP1 down-regulation. Mod. Pathol.15, 1227–1235 (2002). ArticleCASPubMed Google Scholar
Inui, N. et al. High expression of Cks1 in human non-small cell lung carcinomas. Biochem. Biophys. Res. Commun.303, 978–984 (2003). ArticleCASPubMed Google Scholar
Yokoi, S. et al. Amplification and overexpression of SKP2 are associated with metastasis of non-small-cell lung cancers to lymph nodes. Am. J. Pathol.165, 175–180 (2004). ArticleCASPubMedPubMed Central Google Scholar
Zhu, C. Q. et al. Skp2 gene copy number aberrations are common in non-small cell lung carcinoma, and its overexpression in tumors with ras mutation is a poor prognostic marker. Clin. Cancer Res.10, 1984–1991 (2004). ArticleCASPubMed Google Scholar
Coe, B. P. et al. High-resolution chromosome arm 5p array CGH analysis of small cell lung carcinoma cell lines. Genes Chromosomes Cancer42, 308–313 (2005). ArticleCASPubMed Google Scholar
Zhan, F. et al. CKS1B, overexpressed in aggressive disease, regulates multiple myeloma growth and survival through SKP2- and p27Kip1-dependent and -independent mechanisms. Blood109, 4995–5001 (2007). ArticleCASPubMedPubMed Central Google Scholar
Shaughnessy, J. Amplification and overexpression of CKS1B at chromosome band 1q21 is associated with reduced levels of p27Kip1 and an aggressive clinical course in multiple myeloma. Hematology10, S117–S126 (2005). ArticleCAS Google Scholar
Woenckhaus, C. et al. Expression of Skp2 and p27KIP1 in naevi and malignant melanoma of the skin and its relation to clinical outcome. Histol. Histopathol20, 501–508 (2005). CASPubMed Google Scholar
Li, Q., Murphy, M., Ross, J., Sheehan, C. & Carlson, J. A. Skp2 and p27kip1 expression in melanocytic nevi and melanoma: an inverse relationship. J. Cutan Pathol.31, 633–642 (2004). ArticlePubMed Google Scholar
Katagiri, Y., Hozumi, Y. & Kondo, S. Knockdown of Skp2 by siRNA inhibits melanoma cell growth in vitro and in vivo. J. Dermatol. Sci.42, 215–224 (2006). ArticleCASPubMed Google Scholar
Bhatt, K. V., Hu, R., Spofford, L. S. & Aplin, A. E. Mutant B-RAF signaling and cyclin D1 regulate Cks1/S-phase kinase-associated protein 2-mediated degradation of p27Kip1 in human melanoma cells. Oncogene26, 1056–1066 (2007). ArticleCASPubMed Google Scholar
Fukuchi, M. et al. Inverse correlation between expression levels of p27 and the ubiquitin ligase subunit Skp2 in early esophageal squamous cell carcinoma. Anticancer Res.24, 777–783 (2004). CASPubMed Google Scholar
Harada, K. et al. High expression of S-phase kinase-associated protein 2 (Skp2) is a strong prognostic marker in oral squamous cell carcinoma patients treated by UFT in combination with radiation. Anticancer Res.25, 2471–2475 (2005). CASPubMed Google Scholar
Kudo, Y. et al. High expression of S-phase kinase-interacting protein 2, human F-box protein, correlates with poor prognosis in oral squamous cell carcinomas. Cancer Res.61, 7044–7047 (2001). CASPubMed Google Scholar
Kitajima, S. et al. Role of Cks1 overexpression in oral squamous cell carcinomas: cooperation with Skp2 in promoting p27 degradation. Am. J. Pathol.165, 2147–2155 (2004). ArticleCASPubMedPubMed Central Google Scholar
Shigemasa, K., Gu, L., O'Brien, T. J. & Ohama, K. Skp2 overexpression is a prognostic factor in patients with ovarian adenocarcinoma. Clin. Cancer Res.9, 1756–1763 (2003). CASPubMed Google Scholar
Sui, L. et al. Clinical significance of Skp2 expression, alone and combined with Jab1 and p27 in epithelial ovarian tumors. Oncol. Rep.15, 765–771 (2006). CASPubMed Google Scholar
Drobnjak, M. et al. Altered expression of p27 and Skp2 proteins in prostate cancer of African-American patients. Clin. Cancer Res.9, 2613–2619 (2003). CASPubMed Google Scholar
Yang, G. et al. Elevated Skp2 protein expression in human prostate cancer: association with loss of the cyclin-dependent kinase inhibitor p27 and PTEN and with reduced recurrence-free survival. Clin. Cancer Res.8, 3419–3426 (2002). CASPubMed Google Scholar
Amir, R. E., Haecker, H., Karin, M. & Ciechanover, A. Mechanism of processing of the NF-κB2 p100 precursor: identification of the specific polyubiquitin chain-anchoring lysine residue and analysis of the role of NEDD8-modification on the SCFβ-TrCP ubiquitin ligase. Oncogene23, 2540–2547 (2004). ArticleCASPubMed Google Scholar
Fong, A. & Sun, S. C. Genetic evidence for the essential role of β-transducin repeat-containing protein in the inducible processing of NF-κB2/p100. J. Biol. Chem.277, 22111–22114 (2002). ArticleCASPubMed Google Scholar
Lang, V. et al. βTrCP-mediated proteolysis of NF-κB1 p105 requires phosphorylation of p105 serines 927 and 932. Mol. Cell. Biol.23, 402–413 (2003). ArticleCASPubMedPubMed Central Google Scholar
Orian, A. et al. SCFβ-TrCP ubiquitin ligase-mediated processing of NF-κB p105 requires phosphorylation of its C-terminus by IκB kinase. EMBO J.19, 2580–2591 (2000). ArticleCASPubMedPubMed Central Google Scholar
Lassot, I. et al. ATF4 degradation relies on a phosphorylation-dependent interaction with the SCFβTrCP ubiquitin ligase. Mol. Cell. Biol.21, 2192–2202 (2001). ArticleCASPubMedPubMed Central Google Scholar
Li, Y., Kumar, K. G., Tang, W., Spiegelman, V. S. & Fuchs, S. Y. Negative regulation of prolactin receptor stability and signaling mediated by SCFβ-TrC E3 ubiquitin ligase. Mol. Cell. Biol.24, 4038–4048 (2004). ArticleCASPubMedPubMed Central Google Scholar
Besnard-Guerin, C. et al. HIV-1 Vpu sequesters β-transducin repeat-containing protein (βTrCP) in the cytoplasm and provokes the accumulation of β-catenin and other SCFβTrCP substrates. J. Biol. Chem.279, 788–795 (2004). ArticleCASPubMed Google Scholar
Kumar, K. G., Krolewski, J. J. & Fuchs, S. Y. Phosphorylation and specific ubiquitin acceptor sites are required for ubiquitination and degradation of the IFNAR1 subunit of type I interferon receptor. J. Biol. Chem.279, 46614–46620 (2004). ArticleCASPubMed Google Scholar
Mantovani, F. & Banks, L. Regulation of the discs large tumor suppressor by a phosphorylation-dependent interaction with the β-TrCP ubiquitin ligase receptor. J. Biol. Chem.278, 42477–42486 (2003). ArticleCASPubMed Google Scholar
Reischl, S. et al. β-TrCP1-mediated degradation of PERIOD2 is essential for circadian dynamics. J. Biol. Rhythms22, 375–386 (2007). ArticleCASPubMed Google Scholar
Shirogane, T., Jin, J., Ang, X. L. & Harper, J. W. SCFβ-TRCP controls clock-dependent transcription via casein kinase 1-dependent degradation of the mammalian period-1 (Per1) protein. J. Biol. Chem.280, 26863–26872 (2005). ArticleCASPubMed Google Scholar
Eide, E. J. et al. Control of mammalian circadian rhythm by CKIε-regulated proteasome-mediated PER2 degradation. Mol. Cell. Biol.25, 2795–2807 (2005). ArticleCASPubMedPubMed Central Google Scholar
Ding, Q. et al. Degradation of Mcl-1 by β-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol. Cell. Biol.27, 4006–4017 (2007). ArticleCASPubMed Google Scholar
Tan, P. et al. Recruitment of a ROC1-CUL1 ubiquitin ligase by Skp1 and HOS to catalyze the ubiquitination of IκBα. Mol. Cell3, 527–533 (1999). ArticleCASPubMed Google Scholar
Gallegos, J. R. et al. SCF TrCP1 activates and ubiquitylates TAp63γ. J. Biol. Chem.283, 66–75 (2008). ArticleCASPubMed Google Scholar
van Kerkhof, P., Putters, J. & Strous, G. J. The ubiquitin ligase SCFβTrCP regulates the degradation of the growth hormone receptor. J. Biol. Chem.282, 20475–20483 (2007). ArticleCASPubMed Google Scholar