Small molecule therapeutics targeting F-box proteins in cancer

Seminars in Cancer Biology

Volumn 36, Issue , 2016, Pages 105-119

  Liu, Yuan ^a   Mallampalli, Rama K ^a,b  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Cancer; E3 ligase; F box protein; Small molecule inhibitor; Ubiquitin

Indexed keywords

BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; F BOX PROTEIN; FBXL2 PROTEIN; FBXL7 PROTEIN; FBXO1 PROTEIN; FBXO11 PROTEIN; FBXO31 PROTEIN; FBXW7 PROTEIN; FBXW8 PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; MULTIPROTEIN COMPLEX; PROTEASOME; PROTEIN BINDING; UBIQUITIN;

COMPLEX FORMATION; DNA REPAIR; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR RECOGNITION; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; REVIEW; UBIQUITINATION; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; NEOPLASMS; SIGNAL TRANSDUCTION;

ANTINEOPLASTIC AGENTS; F-BOX PROTEINS; HUMANS; MOLECULAR TARGETED THERAPY; MULTIPROTEIN COMPLEXES; NEOPLASMS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; SIGNAL TRANSDUCTION; UBIQUITINS;

EID: 84958125783     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2015.09.014     Document Type: Review

References (181)

1. Stockwell B. Outsmarting Cancer. A biologist talks about what makes disease-causing proteins so difficult to target with drugs. Sci. Am. 2011, 305:20.
2. Hershko A., Ciechanover A. The ubiquitin system. Ann. Rev. Biochem. 1998, 67:425-479.
3. Komander D., Rape M. The ubiquitin code. Ann. Rev. Biochem. 2012, 81:203-229.
4. Deshaies R.J., Joazeiro C.A.P. RING domain E3 ubiquitin ligases. Ann. Rev. Biochem. 2009, 78:399-434.
5. Petroski M.D., Deshaies R.J. Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 2005, 6:9-20.
6. Feldman R.M., Correll C.C., Kaplan K.B., Deshaies R.J. A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 1997, 91:221-230.
7. Skowyra D., Craig K.L., Tyers M., Elledge S.J., Harper J.W. F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 1997, 91:209-219.
8. Cardozo T., Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat. Rev. Mol. Cell Biol. 2004, 5:739-751.
9. Bai C., Sen P., Hofmann K., Ma L., Goebl M., Harper J.W., Elledge S.J. SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 1996, 86:263-274.
10. Cenciarelli C., Chiaur D.S., Guardavaccaro D., Parks W., Vidal M., Pagano M. Identification of a family of human F-box proteins. Curr. Biol.: CB 1999, 9:1177-1179.
11. Winston J.T., Koepp D.M., Zhu C., Elledge S.J., Harper J.W. A family of mammalian F-box proteins. Curr. Biol.: CB 1999, 9:1180-1182.
12. Jin J., Cardozo T., Lovering R.C., Elledge S.J., Pagano M., Harper J.W. Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev. 2004, 18:2573-2580.
13. Ravid T., Hochstrasser M. Diversity of degradation signals in the ubiquitin-proteasome system. Nat. Rev. Mol. Cell Biol. 2008, 9:679-690.
14. Lau A.W., Fukushima H., Wei W. The Fbw7 and betaTRCP E3 ubiquitin ligases and their roles in tumorigenesis. Front. Biosci. 2012, 17:2197-2212.
15. Frescas D., Pagano M. Deregulated proteolysis by the F-box proteins SKP2 and beta-TrCP: tipping the scales of cancer. Nat. Rev. Cancer 2008, 8:438-449.
16. Nash P., Tang X., Orlicky S., Chen Q., Gertler F.B., Mendenhall M.D., Sicheri F., Pawson T., Tyers M. Multisite phosphorylation of a CDK inhibitor sets a threshold for the onset of DNA replication. Nature 2001, 414:514-521.
17. Liu C., Li Y., Semenov M., Han C., Baeg G.H., Tan Y., Zhang Z., Lin X., He X. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 2002, 108:837-847.
18. Welcker M., Singer J., Loeb K.R., Grim J., Bloecher A., Gurien-West M., Clurman B.E., Roberts J.M. Multisite phosphorylation by Cdk2 and GSK3 controls cyclin E degradation. Mol. Cell 2003, 12:381-392.
19. Wei W., Jin J., Schlisio S., Harper J.W., Kaelin W.G. The v-Jun point mutation allows c-Jun to escape GSK3-dependent recognition and destruction by the Fbw7 ubiquitin ligase. Cancer Cell 2005, 8:25-33.
20. Abbas T., Mueller A.C., Shibata E., Keaton M., Rossi M., Dutta A. CRL1-FBXO11 promotes Cdt2 ubiquitylation and degradation and regulates Pr-Set7/Set8-mediated cellular migration. Mol. Cell 2013, 49:1147-1158.
21. Rossi M., Duan S., Jeong Y.T., Horn M., Saraf A., Florens L., Washburn M.P., Antebi A., Pagano M. Regulation of the CRL4(Cdt2) ubiquitin ligase and cell-cycle exit by the SCF(Fbxo11) ubiquitin ligase. Mol. Cell 2013, 49:1159-1166.
22. Skaar J.R., Pagan J.K., Pagano M. Mechanisms and function of substrate recruitment by F-box proteins. Nat. Rev. Mol. Cell Biol. 2013, 14:369-381.
23. D'Angiolella V., Donato V., Vijayakumar S., Saraf A., Florens L., Washburn M.P., Dynlacht B., Pagano M. SCF(Cyclin F) controls centrosome homeostasis and mitotic fidelity through CP110 degradation. Nature 2010, 466:138-142.
24. Chen B.B., Coon T.A., Glasser J.R., Mallampalli R.K. Calmodulin antagonizes a calcium-activated SCF ubiquitin E3 ligase subunit, FBXL2, to regulate surfactant homeostasis. Mol. Cell. Biol. 2011, 31:1905-1920.
25. Chen B.B., Glasser J.R., Coon T.A., Mallampalli R.K. F-box protein FBXL2 exerts human lung tumor suppressor-like activity by ubiquitin-mediated degradation of cyclin D3 resulting in cell cycle arrest. Oncogene 2012, 31:2566-2579.
26. Chen B.B., Glasser J.R., Coon T.A., Zou C., Miller H.L., Fenton M., McDyer J.F., Boyiadzis M., Mallampalli R.K. F-box protein FBXL2 targets cyclin D2 for ubiquitination and degradation to inhibit leukemic cell proliferation. Blood 2012, 119:3132-3141.
27. D'Angiolella V., Donato V., Forrester F.M., Jeong Y.T., Pellacani C., Kudo Y., Saraf A., Florens L., Washburn M.P., Pagano M. Cyclin F-mediated degradation of ribonucleotide reductase M2 controls genome integrity and DNA repair. Cell 2012, 149:1023-1034.
28. Chen B.B., Coon T.A., Glasser J.R., McVerry B.J., Zhao J., Zhao Y., Zou C., Ellis B., Sciurba F.C., Zhang Y., Mallampalli R.K. A combinatorial F box protein directed pathway controls TRAF adaptor stability to regulate inflammation. Nat. Immunol. 2013, 14:470-479.
29. Liu Y., Lear T., Zhao Y., Zhao J., Zou C., Chen B.B., Mallampalli R.K. F-box protein Fbxl18 mediates polyubiquitylation and proteasomal degradation of the pro-apoptotic SCF subunit Fbxl7. Cell Death Dis. 2015, 6:e1630.
30. Richardson P.G., Barlogie B., Berenson J., Singhal S., Jagannath S., Irwin D., Rajkumar S.V., Srkalovic G., Alsina M., Alexanian R., Siegel D., Orlowski R.Z., Kuter D., Limentani S.A., Lee S., Hideshima T., Esseltine D.L., Kauffman M., Adams J., Schenkein D.P., Anderson K.C. A phase 2 study of bortezomib in relapsed, refractory myeloma. N. Engl. J. Med. 2003, 348:2609-2617.
31. Richardson P.G., Briemberg H., Jagannath S., Wen P.Y., Barlogie B., Berenson J., Singhal S., Siegel D.S., Irwin D., Schuster M., Srkalovic G., Alexanian R., Rajkumar S.V., Limentani S., Alsina M., Orlowski R.Z., Najarian K., Esseltine D., Anderson K.C., Amato A.A. Frequency, characteristics, and reversibility of peripheral neuropathy during treatment of advanced multiple myeloma with bortezomib. J. Clin. Oncol.: Off. J. Am. Soc. Clin. Oncol. 2006, 24:3113-3120.
32. Kouroukis T.C., Baldassarre F.G., Haynes A.E., Imrie K., Reece D.E., Cheung M.C. Bortezomib in multiple myeloma: systematic review and clinical considerations. Curr. Oncol. 2014, 21:e573-e603.
33. Xie C.M., Wei W., Sun Y. Role of SKP1-CUL1-F-box-protein (SCF) E3 ubiquitin ligases in skin cancer. J. Genet. Genom. - Yi chuan xue bao 2013, 40:97-106.
34. Zhao Y., Sun Y. Cullin-RING Ligases as attractive anti-cancer targets. Curr. Pharm. Des. 2013, 19:3215-3225.
35. Weathington N.M., Mallampalli R.K. Emerging therapies targeting the ubiquitin proteasome system in cancer. J. Clin. Invest. 2014, 124:6-12.
36. Skaar J.R., Pagan J.K., Pagano M. SCF ubiquitin ligase-targeted therapies. Nat. Rev. Drug Discov. 2014, 13:889-903.
37. Wang Z., Liu P., Inuzuka H., Wei W. Roles of F-box proteins in cancer. Nat. Rev. Cancer 2014, 14:233-247.
38. Liu J., Shaik S., Dai X., Wu Q., Zhou X., Wang Z., Wei W. Targeting the ubiquitin pathway for cancer treatment. Biochim. Biophys. Acta 2015, 1855:50-60.
39. Yu Z.K., Gervais J.L., Zhang H. Human CUL-associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:11324-11329.
40. Tsvetkov L.M., Yeh K.H., Lee S.J., Sun H., Zhang H. p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr. Biol.: CB 1999, 9:661-664.
41. Sutterluty H., Chatelain E., Marti A., Wirbelauer C., Senften M., Muller U., Krek W. p45SKP2 promotes p27Kip1 degradation and induces S phase in quiescent cells. Nat. Cell Biol. 1999, 1:207-214.
42. Carrano A.C., Eytan E., Hershko A., Pagano M. SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27. Nat. Cell Biol. 1999, 1:193-199.
43. Ganoth D., Bornstein G., Ko T.K., Larsen B., Tyers M., Pagano M., Hershko A. The cell-cycle regulatory protein Cks1 is required for SCF(Skp2)-mediated ubiquitinylation of p27. Nat. Cell Biol. 2001, 3:321-324.
44. Spruck C., Strohmaier H., Watson M., Smith A.P., Ryan A., Krek T.W., Reed S.I. A CDK-independent function of mammalian Cks1: targeting of SCF(Skp2) to the CDK inhibitor p27Kip1. Mol. Cell 2001, 7:639-650.
45. Nakayama K., Nagahama H., Minamishima Y.A., Miyake S., Ishida N., Hatakeyama S., Kitagawa M., Iemura S.-i., Natsume T., Nakayama K.I. Skp2-mediated degradation of p27 regulates progression into mitosis. Dev. Cell 2004, 6:661-672.
46. Kossatz U., Dietrich N., Zender L., Buer J., Manns M.P., Malek N.P. Skp2-dependent degradation of p27kip1 is essential for cell cycle progression. Genes Dev. 2004, 18:2602-2607.
47. Chan C.H., Morrow J.K., Li C.F., Gao Y., Jin G., Moten A., Stagg L.J., Ladbury J.E., Cai Z., Xu D., Logothetis C.J., Hung M.C., Zhang S., Lin H.K. Pharmacological inactivation of Skp2 SCF ubiquitin ligase restricts cancer stem cell traits and cancer progression. Cell 2013, 154:556-568.
48. Chan C.H., Li C.F., Yang W.L., Gao Y., Lee S.W., Feng Z., Huang H.Y., Tsai K.K., Flores L.G., Shao Y., Hazle J.D., Yu D., Wei W., Sarbassov D., Hung M.C., Nakayama K.I., Lin H.K. The Skp2-SCF E3 ligase regulates Akt ubiquitination, glycolysis, herceptin sensitivity, and tumorigenesis. Cell 2012, 149:1098-1111.
49. Chen Q., Xie W., Kuhn D.J., Voorhees P.M., Lopez-Girona A., Mendy D., Corral L.G., Krenitsky V.P., Xu W., Moutouh-de Parseval L., Webb D.R., Mercurio F., Nakayama K.I., Nakayama K., Orlowski R.Z. Targeting the p27 E3 ligase SCF(Skp2) results in p27- and Skp2-mediated cell-cycle arrest and activation of autophagy. Blood 2008, 111:4690-4699.
50. Nickeleit I., Zender S., Sasse F., Geffers R., Brandes G., Sorensen I., Steinmetz H., Kubicka S., Carlomagno T., Menche D., Gutgemann I., Buer J., Gossler A., Manns M.P., Kalesse M., Frank R., Malek N.P. Argyrin a reveals a critical role for the tumor suppressor protein p27(kip1) in mediating antitumor activities in response to proteasome inhibition. Cancer Cell 2008, 14:23-35.
51. Rico-Bautista E., Yang C.C., Lu L., Roth G.P., Wolf D.A. Chemical genetics approach to restoring p27Kip1 reveals novel compounds with antiproliferative activity in prostate cancer cells. BMC Biol. 2010, 8:153.
52. Wu L., Grigoryan A.V., Li Y., Hao B., Pagano M., Cardozo T.J. Specific small molecule inhibitors of Skp2-mediated p27 degradation. Chem. Biol. 2012, 19:1515-1524.
53. Yang G., Ayala G., De Marzo A., Tian W., Frolov A., Wheeler T.M., Thompson T.C., Harper J.W. 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.: Off. J. Am. Assoc. Cancer Res. 2002, 8:3419-3426.
54. Liu S., Yamauchi H. p27-Associated G1 arrest induced by hinokitiol in human malignant melanoma cells is mediated via down-regulation of pRb, Skp2 ubiquitin ligase, and impairment of Cdk2 function. Cancer Lett. 2009, 286:240-249.
55. Koga H., Harada M., Ohtsubo M., Shishido S., Kumemura H., Hanada S., Taniguchi E., Yamashita K., Kumashiro R., Ueno T., Sata M. Troglitazone induces p27Kip1-associated cell-cycle arrest through down-regulating Skp2 in human hepatoma cells. Hepatology 2003, 37:1086-1096.
56. Hsieh H.Y., Shieh J.J., Chen C.J., Pan M.Y., Yang S.Y., Lin S.C., Chang J.S., Lee A.Y., Chang C.C. Prodigiosin down-regulates SKP2 to induce p27(KIP1) stabilization and antiproliferation in human lung adenocarcinoma cells. Br. J. Pharmacol. 2012, 166:2095-2108.
57. Chung Y.K., Chi-Hung Or R., Lu C.H., Ouyang W.T., Yang S.Y., Chang C.C. Sulforaphane down-regulates SKP2 to stabilize p27(KIP1) for inducing antiproliferation in human colon adenocarcinoma cells. J. Biosci. Bioeng. 2015, 119:35-42.
58. Sumimoto H., Hirata K., Yamagata S., Miyoshi H., Miyagishi M., Taira K., Kawakami Y. Effective inhibition of cell growth and invasion of melanoma by combined suppression of BRAF (V599E) and Skp2 with lentiviral RNAi. Int. J. Cancer 2006, 118:472-476.
59. Wang Y., Dai D.L., Martinka M., Li G. Prognostic significance of nuclear ING3 expression in human cutaneous melanoma. Clin. Cancer Res.: Off. J. Am. Assoc. Cancer Res. 2007, 13:4111-4116.
60. Chen G., Wang Y., Garate M., Zhou J., Li G. The tumor suppressor ING3 is degraded by SCF(Skp2)-mediated ubiquitin-proteasome system. Oncogene 2010, 29:1498-1508.
61. Fuchs S.Y., Spiegelman V.S., Kumar K.G. The many faces of beta-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer. Oncogene 2004, 23:2028-2036.
62. Perkins N.D. Integrating cell-signalling pathways with NF-kappaB and IKK function. Nat. Rev. Mol. Cell Biol. 2007, 8:49-62.
63. Chen Z.J. Ubiquitin signalling in the NF-kappaB pathway. Nat. Cell Biol. 2005, 7:758-765.
64. Yaron A., Hatzubai A., Davis M., Lavon I., Amit S., Manning A.M., Andersen J.S., Mann M., Mercurio F., Ben-Neriah Y. Identification of the receptor component of the IkappaBalpha-ubiquitin ligase. Nature 1998, 396:590-594.
65. Nakajima H., Fujiwara H., Furuichi Y., Tanaka K., Shimbara N. A novel small-molecule inhibitor of NF-kappaB signaling. Biochem. Biophys. Res. Commun. 2008, 368:1007-1013.
66. Nakayama K., Hatakeyama S., Maruyama S.-i., Kikuchi A., Onoé K., Good R.A., Nakayama K.I. 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. 2003, 100:8752-8757.
67. Yang H.S., Jansen A.P., Komar A.A., Zheng X., Merrick W.C., Costes S., Lockett S.J., Sonenberg N., Colburn N.H. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol. Cell. Biol. 2003, 23:26-37.
68. Mudduluru G., Medved F., Grobholz R., Jost C., Gruber A., Leupold J.H., Post S., Jansen A., Colburn N.H., Allgayer H. 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. Cancer 2007, 110:1697-1707.
69. Wei N.A., Liu S.S., Leung T.H., Tam K.F., Liao X.Y., Cheung A.N., Chan K.K., Ngan H.Y. Loss of Programmed cell death 4 (Pdcd4) associates with the progression of ovarian cancer. Mol. Cancer 2009, 8:70.
70. Dorrello N.V., Peschiaroli A., Guardavaccaro D., Colburn N.H., Sherman N.E., Pagano M. S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science 2006, 314:467-471.
71. Blees J.S., Bokesch H.R., Rubsamen D., Schulz K., Milke L., Bajer M.M., Gustafson K.R., Henrich C.J., McMahon J.B., Colburn N.H., Schmid T., Brune B. Erioflorin stabilizes the tumor suppressor Pdcd4 by inhibiting its interaction with the E3-ligase beta-TrCP1. PloS ONE 2012, 7:e46567.
72. Peterson T.R., Laplante M., Thoreen C.C., Sancak Y., Kang S.A., Kuehl W.M., Gray N.S., Sabatini D.M. DEPTOR is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell 2009, 137:873-886.
73. Duan S., Skaar J.R., Kuchay S., Toschi A., Kanarek N., Ben-Neriah Y., Pagano M. mTOR generates an auto-amplification loop by triggering the betaTrCP- and CK1alpha-dependent degradation of DEPTOR. Mol. Cell 2011, 44:317-324.
74. Gao D., Inuzuka H., Tan M.K., Fukushima H., Locasale J.W., Liu P., Wan L., Zhai B., Chin Y.R., Shaik S., Lyssiotis C.A., Gygi S.P., Toker A., Cantley L.C., Asara J.M., Harper J.W., Wei W. mTOR drives its own activation via SCF(betaTrCP)-dependent degradation of the mTOR inhibitor DEPTOR. Mol. Cell 2011, 44:290-303.
75. Zhao Y., Xiong X., Sun Y. DEPTOR, an mTOR inhibitor, is a physiological substrate of SCF(betaTrCP) E3 ubiquitin ligase and regulates survival and autophagy. Mol. Cell 2011, 44:304-316.
76. Boyd K.D., Walker B.A., Wardell C.P., Ross F.M., Gregory W.M., Davies F.E., Morgan G.J. High expression levels of the mammalian target of rapamycin inhibitor DEPTOR are predictive of response to thalidomide in myeloma. Leuk. Lymphoma 2010, 51:2126-2129.
77. Sakamoto K.M., Kim K.B., Kumagai A., Mercurio F., Crews C.M., Deshaies R.J. Protacs: chimeric molecules that target proteins to the Skp1-Cullin-box complex for ubiquitination and degradation. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:8554-8559.
78. Sakamoto K.M., Kim K.B., Verma R., Ransick A., Stein B., Crews C.M., Deshaies R.J. Development of Protacs to target cancer-promoting proteins for ubiquitination and degradation. Mol. Cell. Proteomics: MCP 2003, 2:1350-1358.
79. Schneekloth A.R., Pucheault M., Tae H.S., Crews C.M. Targeted intracellular protein degradation induced by a small molecule: En route to chemical proteomics. Bioorgan. Med. Chem. Lett. 2008, 18:5904-5908.
80. O'Connor L., Strasser A., O'Reilly L.A., Hausmann G., Adams J.M., Cory S., Huang D.C. Bim: a novel member of the Bcl-family that promotes apoptosis. EMBO J. 1998, 17:384-395.
81. Fletcher J.I., Huang D.C. Controlling the cell death mediators Bax and Bak: puzzles and conundrums. Cell Cycle 2008, 7:39-44.
82. Dehan E., Bassermann F., Guardavaccaro D., Vasiliver-Shamis G., Cohen M., Lowes K.N., Dustin M., Huang D.C., Taunton J., Pagano M. betaTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol. Cell 2009, 33:109-116.
83. Rogers G.C., Rusan N.M., Roberts D.M., Peifer M., Rogers S.L. The SCF Slimb ubiquitin ligase regulates Plk4/Sak levels to block centriole reduplication. J. Cell Biol. 2009, 184:225-239.
84. Cunha-Ferreira I., Rodrigues-Martins A., Bento I., Riparbelli M., Zhang W., Laue E., Callaini G., Glover D.M., Bettencourt-Dias M. The SCF/Slimb ubiquitin ligase limits centrosome amplification through degradation of SAK/PLK4. Curr. Biol.: CB 2009, 19:43-49.
85. Akhoondi S., Sun D., von der Lehr N., Apostolidou S., Klotz K., Maljukova A., Cepeda D., Fiegl H., Dafou D., Marth C., Mueller-Holzner E., Corcoran M., Dagnell M., Nejad S.Z., Nayer B.N., Zali M.R., Hansson J., Egyhazi S., Petersson F., Sangfelt P., Nordgren H., Grander D., Reed S.I., Widschwendter M., Sangfelt O., Spruck C. FBXW7/hCDC4 is a general tumor suppressor in human cancer. Cancer Res. 2007, 67:9006-9012.
86. Spruck C. miR-27a regulation of SCF(Fbw7) in cell division control and cancer. Cell Cycle 2011, 10:3232-3233.
87. Ma J., Cheng L., Liu H., Zhang J., Shi Y., Zeng F., Miele L., Sarkar F.H., Xia J., Wang Z. Genistein down-regulates miR-223 expression in pancreatic cancer cells. Curr. Drug Targets 2013, 14:1150-1156.
88. Kimura T., Gotoh M., Nakamura Y., Arakawa H. hCDC4b, a regulator of cyclin E, as a direct transcriptional target of p53. Cancer Sci. 2003, 94:431-436.
89. Mao J.H., Perez-Losada J., Wu D., Delrosario R., Tsunematsu R., Nakayama K.I., Brown K., Bryson S., Balmain A. Fbxw7/Cdc4 is a p53-dependent, haploinsufficient tumour suppressor gene. Nature 2004, 432:775-779.
90. Balamurugan K., Wang J.M., Tsai H.H., Sharan S., Anver M., Leighty R., Sterneck E. The tumour suppressor C/EBPdelta inhibits FBXW7 expression and promotes mammary tumour metastasis. EMBO J. 2010, 29:4106-4117.
91. Welcker M., Orian A., Jin J., Grim J.E., Harper J.W., Eisenman R.N., Clurman B.E. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:9085-9090.
92. von der Lehr N., Johansson S., Wu S., Bahram F., Castell A., Cetinkaya C., Hydbring P., Weidung I., Nakayama K., Nakayama K.I., Soderberg O., Kerppola T.K., Larsson L.G. The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription. Mol. Cell 2003, 11:1189-1200.
93. Kim S.Y., Herbst A., Tworkowski K.A., Salghetti S.E., Tansey W.P. Skp2 regulates Myc protein stability and activity. Mol. Cell 2003, 11:1177-1188.
94. Yada M., Hatakeyama S., Kamura T., Nishiyama M., Tsunematsu R., Imaki H., Ishida N., Okumura F., Nakayama K., Nakayama K.I. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 2004, 23:2116-2125.
95. Zhou G.B., Chen S.J., Wang Z.Y., Chen Z. Back to the future of oridonin: again, compound from medicinal herb shows potent antileukemia efficacies in vitro and in vivo. Cell Res. 2007, 17:274-276.
96. Huang H.L., Weng H.Y., Wang L.Q., Yu C.H., Huang Q.J., Zhao P.P., Wen J.Z., Zhou H., Qu L.H. Triggering Fbw7-mediated proteasomal degradation of c-Myc by oridonin induces cell growth inhibition and apoptosis. Mol. Cancer Ther. 2012, 11:1155-1165.
97. Xia J., Duan Q., Ahmad A., Bao B., Banerjee S., Shi Y., Ma J., Geng J., Chen Z., Rahman K.M., Miele L., Sarkar F.H., Wang Z. Genistein inhibits cell growth and induces apoptosis through up-regulation of miR-34a in pancreatic cancer cells. Curr. Drug Targets 2012, 13:1750-1756.
98. Reavie L., Buckley S.M., Loizou E., Takeishi S., Aranda-Orgilles B., Ndiaye-Lobry D., Abdel-Wahab O., Ibrahim S., Nakayama K.I., Aifantis I. Regulation of c-Myc ubiquitination controls chronic myelogenous leukemia initiation and progression. Cancer Cell 2013, 23:362-375.
99. Gregory M.A., Hann S.R. c-Myc proteolysis by the ubiquitin-proteasome pathway: stabilization of c-Myc in Burkitt's lymphoma cells. Mol. Cell. Biol. 2000, 20:2423-2435.
100. Busino L., Millman S.E., Scotto L., Kyratsous C.A., Basrur V., O'Connor O., Hoffmann A., Elenitoba-Johnson K.S., Pagano M. Fbxw7alpha- and GSK3-mediated degradation of p100 is a pro-survival mechanism in multiple myeloma. Nat. Cell Biol. 2012, 14:375-385.
101. Inoue J., Ishida T., Tsukamoto N., Kobayashi N., Naito A., Azuma S., Yamamoto T. Tumor necrosis factor receptor-associated factor (TRAF) family: adapter proteins that mediate cytokine signaling. Exp. Cell Res. 2000, 254:14-24.
102. Mallampalli R.K., Coon T.A., Glasser J.R., Wang C., Dunn S.R., Weathington N.M., Zhao J., Zou C., Zhao Y., Chen B.B. Targeting F box protein Fbxo3 to control cytokine-driven inflammation. J. Immunol. 2013, 191:5247-5255.
103. Chen B.B., Glasser J.R., Coon T.A., Mallampalli R.K. Skp-cullin-box E3 ligase component FBXL2 ubiquitinates Aurora B to inhibit tumorigenesis. Cell Death Dis. 2013, 4:e759.
104. Margolis R.L. Tetraploidy and tumor development. Cancer Cell 2005, 8:353-354.
105. Fujiwara T., Bandi M., Nitta M., Ivanova E.V., Bronson R.T., Pellman D. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 2005, 437:1043-1047.
106. Cimini D., Wan X., Hirel C.B., Salmon E.D. Aurora kinase promotes turnover of kinetochore microtubules to reduce chromosome segregation errors. Curr. Biol.: CB 2006, 16:1711-1718.
107. Coon T.A., Glasser J.R., Mallampalli R.K., Chen B.B. Novel E3 ligase component FBXL7 ubiquitinates and degrades Aurora A, causing mitotic arrest. Cell Cycle 2012, 11:721-729.
108. Liu Y., Lear T., Iannone O., Shiva S., Corey C., Rajbhandari S., Jerome J., Chen B.B., Mallampalli R.K. The proapoptotic F-box protein Fbxl7 regulates mitochondrial function by mediating the ubiquitylation and proteasomal degradation of survivin. J. Biol. Chem. 2015, 290:11843-11852.
109. Johansson P., Jeffery J., Al-Ejeh F., Schulz R.B., Callen D.F., Kumar R., Khanna K.K. SCF-FBXO31 E3 ligase targets DNA replication factor Cdt1 for proteolysis in the G2 phase of cell cycle to prevent re-replication. J. Biol. Chem. 2014, 289:18514-18525.
110. Santra M.K., Wajapeyee N., Green M.R. F-box protein FBXO31 mediates cyclin D1 degradation to induce G1 arrest after DNA damage. Nature 2009, 459:722-725.
111. Lin D.I., Barbash O., Kumar K.G., Weber J.D., Harper J.W., Klein-Szanto A.J., Rustgi A., Fuchs S.Y., Diehl J.A. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF (FBX4-alphaB crystallin) complex. Mol. Cell 2006, 24:355-366.
112. Wade M., Li Y.C., Wahl G.M. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat. Rev. Cancer 2013, 13:83-96.
113. Malonia S.K., Dutta P., Santra M.K., Green M.R. F-box protein FBXO31 directs degradation of MDM2 to facilitate p53-mediated growth arrest following genotoxic stress. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:8632-8637.
114. Huang H.L., Jiang Y., Wang Y.H., Chen T., He H.J., Liu T., Yang T., Yang L.W., Chen J., Song Z.Q., Yao W., Wu B., Liu G. FBXO31 promotes cell proliferation, metastasis and invasion in lung cancer. Am. J. Cancer Res. 2015, 5:1814-1822.
115. Liu J., Han L., Li B., Yang J., Huen M.S., Pan X., Tsao S.W., Cheung A.L. F-box only protein 31 (FBXO31) negatively regulates p38 mitogen-activated protein kinase (MAPK) signaling by mediating lysine 48-linked ubiquitination and degradation of mitogen-activated protein kinase kinase 6 (MKK6). J. Biol. Chem. 2014, 289:21508-21518.
116. Fung T.K., Siu W.Y., Yam C.H., Lau A., Poon R.Y. Cyclin F is degraded during G2-by mechanisms fundamentally different from other cyclins. J. Biol. Chem. 2002, 277:35140-35149.
117. Nordlund P., Reichard P. Ribonucleotide reductases. Ann. Rev. Biochem. 2006, 75:681-706.
118. Fu J., Qiu H., Cai M., Pan Y., Cao Y., Liu L., Yun J., Zhang C.Z. Low cyclin F expression in hepatocellular carcinoma associates with poor differentiation and unfavorable prognosis. Cancer Sci. 2013, 104:508-515.
119. Ci W., Polo J.M., Melnick A. B-cell lymphoma 6 and the molecular pathogenesis of diffuse large B-cell lymphoma. Curr. Opin. Hematol. 2008, 15:381-390.
120. Staudt L.M., Dave S. The biology of human lymphoid malignancies revealed by gene expression profiling. Adv. Immunol. 2005, 87:163-208.
121. Duan S., Cermak L., Pagan J.K., Rossi M., Martinengo C., di Celle P.F., Chapuy B., Shipp M., Chiarle R., Pagano M. FBXO11 targets BCL6 for degradation and is inactivated in diffuse large B-cell lymphomas. Nature 2012, 481:90-93.
122. Higa L.A., Banks D., Wu M., Kobayashi R., Sun H., Zhang H. L2DTL/CDT2 interacts with the CUL4/DDB1 complex and PCNA and regulates CDT1 proteolysis in response to DNA damage. Cell Cycle 2006, 5:1675-1680.
123. Abbas T., Shibata E., Park J., Jha S., Karnani N., Dutta A. CRL4(Cdt2) regulates cell proliferation and histone gene expression by targeting PR-Set7/Set8 for degradation. Mol. Cell 2010, 40:9-21.
124. Centore R.C., Havens C.G., Manning A.L., Li J.M., Flynn R.L., Tse A., Jin J., Dyson N.J., Walter J.C., Zou L. CRL4(Cdt2)-mediated destruction of the histone methyltransferase Set8 prevents premature chromatin compaction in S phase. Mol. Cell 2010, 40:22-33.
125. Oda H., Hubner M.R., Beck D.B., Vermeulen M., Hurwitz J., Spector D.L., Reinberg D. Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 2010, 40:364-376.
126. Havens C.G., Walter J.C. Mechanism of CRL4(Cdt2), a PCNA-dependent E3 ubiquitin ligase. Genes Dev. 2011, 25:1568-1582.
127. Jorgensen S., Eskildsen M., Fugger K., Hansen L., Larsen M.S., Kousholt A.N., Syljuasen R.G., Trelle M.B., Jensen O.N., Helin K., Sorensen C.S. SET8 is degraded via PCNA-coupled CRL4(CDT2) ubiquitylation in S phase and after UV irradiation. J. Cell Biol. 2011, 192:43-54.
128. Hall J.R., Bereman M.S., Nepomuceno A.I., Thompson E.A., Muddiman D.C., Smart R.C. C/EBPalpha regulates CRL4(Cdt2)-mediated degradation of p21 in response to UVB-induced DNA damage to control the G1/S checkpoint. Cell Cycle 2014, 13:3602-3610.
129. Pan H.W., Chou H.Y., Liu S.H., Peng S.Y., Liu C.L., Hsu H.C. Role of L2DTL, cell cycle-regulated nuclear and centrosome protein, in aggressive hepatocellular carcinoma. Cell Cycle 2006, 5:2676-2687.
130. Ueki T., Nishidate T., Park J.H., Lin M.L., Shimo A., Hirata K., Nakamura Y., Katagiri T. Involvement of elevated expression of multiple cell-cycle regulator DTL/RAMP (denticleless/RA-regulated nuclear matrix associated protein), in the growth of breast cancer cells. Oncogene 2008, 27:5672-5683.
131. Yang C.H., Pfeffer S.R., Sims M., Yue J., Wang Y., Linga V.G., Paulus E., Davidoff A.M., Pfeffer L.M. The oncogenic microRNA-21 inhibits the tumor suppressive activity of FBXO11 to promote tumorigenesis. J. Biol. Chem. 2015, 290:6037-6046.
132. Xue J., Chi Y., Chen Y., Huang S., Ye X., Niu J., Wang W., Pfeffer L.M., Shao Z., Wu m., Wu Z.H.J. MiRNA-621 sensitizes breast cancer to chemotherapy by suppressing FBXO11 and enhancing p53 activity. Oncogene 2015.
133. Dias D.C., Dolios G., Wang R., Pan Z.-Q. CUL7: A DOC domain-containing cullin selectively binds Skp1 Fbx29 to form an SCF-like complex. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:16601-16606.
134. Tsunematsu R., Nishiyama M., Kotoshiba S., Saiga T., Kamura T., Nakayama K.I. Fbxw8 is essential for Cul1-Cul7 complex formation and for placental development. Mol. Cell. Biol. 2006, 26:6157-6169.
135. Okabe H., Lee S.-H., Phuchareon J., Albertson D.G., McCormick F., Tetsu O. A critical role for FBXW8 and MAPK in cyclin D1 degradation and cancer cell proliferation. PloS ONE 2006, 1:e128.
136. Kong C., Samovski D., Srikanth P., Wainszelbaum M.J., Charron A.J., Liu J., Lange J.J., Chen P.-I., Pan Z.-Q., Su X., Stahl P.D. Ubiquitination and degradation of the hominoid-specific oncoprotein TBC1D3 is mediated by CUL7 E3 ligase. PloS ONE 2012, 7:e46485.
137. Wang H., Chen Y., Lin P., Li L., Zhou G., Liu G., Logsdon C., Jin J., Abbruzzese J.L., Tan T.-H., Wang H. The CUL7/F-box and WD repeat domain containing 8 (CUL7/Fbxw8) ubiquitin ligase promotes degradation of hematopoietic progenitor kinase 1. J. Biol. Chem. 2014, 289:4009-4017.
138. Takai H., Wang R.C., Takai K.K., Yang H., de Lange T. Tel2 regulates the stability of PI3K-related protein kinases. Cell 2007, 131:1248-1259.
139. Horejsi Z., Takai H., Adelman C.A., Collis S.J., Flynn H., Maslen S., Skehel J.M., de Lange T., Boulton S.J. CK2 phospho-dependent binding of R2TP complex to TEL2 is essential for mTOR and SMG1 stability. Mol. Cell 2010, 39:839-850.
140. Takai H., Xie Y., de Lange T., Pavletich N.P. Tel2 structure and function in the Hsp90-dependent maturation of mTOR and ATR complexes. Genes Dev. 2010, 24:2019-2030.
141. Kaizuka T., Hara T., Oshiro N., Kikkawa U., Yonezawa K., Takehana K., Iemura S., Natsume T., Mizushima N. Tti1 and Tel2 are critical factors in mammalian target of rapamycin complex assembly. J. Biol. Chem. 2010, 285:20109-20116.
142. Fernandez-Saiz V., Targosz B.S., Lemeer S., Eichner R., Langer C., Bullinger L., Reiter C., Slotta-Huspenina J., Schroeder S., Knorn A.M., Kurutz J., Peschel C., Pagano M., Kuster B., Bassermann F. SCFFbxo9 and CK2 direct the cellular response to growth factor withdrawal via Tel2/Tti1 degradation and promote survival in multiple myeloma. Nat. Cell Biol. 2013, 15:72-81.
143. Kim T.Y., Jackson S., Xiong Y., Whitsett T.G., Lobello J.R., Weiss G.J., Tran N.L., Bang Y.J., Der C.J. CRL4A-FBXW5-mediated degradation of DLC1 Rho GTPase-activating protein tumor suppressor promotes non-small cell lung cancer cell growth. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:16868-16873.
144. Hsu J.Y., Reimann J.D.R., Sorensen C.S., Lukas J., Jackson P.K. E2F-dependent accumulation of hEmi1 regulates S phase entry by inhibiting APCCdh1. Nat. Cell Biol. 2002, 4:358-366.
145. 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. 2008, 21:445-454.
146. Huang H.C., Lin C.L., Lin J.K. 1,2,3,4,6-penta-O-galloyl-beta-d-glucose, quercetin, curcumin and lycopene induce cell-cycle arrest in MDA-MB-231 and BT474 cells through downregulation of Skp2 protein. J. Agric. Food Chem. 2011, 59:6765-6775.
147. Huang H.C., Way T.D., Lin C.L., Lin J.K. EGCG stabilizes p27kip1 in E2-stimulated MCF-cells through down-regulation of the Skp2 protein. Endocrinology 2008, 149:5972-5983.
148. Yang E.S., Burnstein K.L. Vitamin D inhibits G1 to S progression in LNCaP prostate cancer cells through p27Kip1 stabilization and Cdk2 mislocalization to the cytoplasm. J. Biol. Chem. 2003, 278:46862-46868.
149. Gao J., Azmi A.S., Aboukameel A., Kauffman M., Shacham S., Abou-Samra A.B., Mohammad R.M. Nuclear retention of Fbw7 by specific inhibitors of nuclear export leads to Notch1 degradation in pancreatic cancer. Oncotarget 2014, 5:3444-3454.
150. Huang H.-L., Weng H.-Y., Wang L.-Q., Yu C.-H., Huang Q.-J., Zhao P.-P., Wen J.-Z., Zhou H., Qu L.-H. Triggering Fbw7-mediated proteasomal degradation of c-Myc by oridonin induces cell growth inhibition and apoptosis. Mol. Cancer Ther. 2012, 11:1155-1165.
151. Nangle S., Xing W., Zheng N. Crystal structure of mammalian cryptochrome in complex with a small molecule competitor of its ubiquitin ligase. Cell Res. 2013, 23:1417-1419.
152. Hirota T., Lee J.W., John St., Sawa P.C., Iwaisako M., Noguchi K., Pongsawakul T., Sonntag P.Y., Welsh T., Brenner D.K., Doyle D.A., Schultz F.J., Kay P.G.S.A. Identification of small molecule activators of cryptochrome. Science 2012, 337:1094-1097.
153. Lagarou A., Mohd-Sarip A., Moshkin Y.M., Chalkley G.E., Bezstarosti K., Demmers J.A., Verrijzer C.P. dKDM2 couples histone H2A ubiquitylation to histone H3 demethylation during Polycomb group silencing. Genes Dev. 2008, 22:2799-2810.
154. Tzatsos A., Paskaleva P., Ferrari F., Deshpande V., Stoykova S., Contino G., Wong K.-K., Lan F., Trojer P., Park P.J., Bardeesy N. KDM2B promotes pancreatic cancer via Polycomb-dependent and -independent transcriptional programs. J. Clin. Invest. 2013, 123:727-739.
155. Xiao J., Zhang T., Xu D., Wang H., Cai Y., Jin T., Liu M., Jin M., Wu K., Yuan J. FBXL20-mediated Vps34 ubiquitination as a p53 controlled checkpoint in regulating autophagy and receptor degradation. Genes Dev. 2015, 29:184-196.
156. Takagi H., Setou M., Ito S., Yao I. SCRAPPER Regulates the Thresholds of Long-Term Potentiation/Depression, the Bidirectional Synaptic Plasticity in Hippocampal CA3-CA1 Synapses. Neural Plast. 2012, 2012:7.
157. Dobie F., Craig A.M. A fight for neurotransmission: SCRAPPER trashes RIM. Cell 2007, 130:775-777.
158. Yao I., Takagi H., Ageta H., Kahyo T., Sato S., Hatanaka K., Fukuda Y., Chiba T., Morone N., Yuasa S., Inokuchi K., Ohtsuka T., MacGregor G.R., Tanaka K., Setou M. SCRAPPER-dependent ubiquitination of active zone protein RIM1 regulates synaptic vesicle release. Cell 2007, 130:943-957.
159. Zhu J., Li K., Dong L., Chen Y. Role of FBXL20 in human colorectal adenocarcinoma. Oncol. Rep. 2012, 28:2290-2298.
160. Zhu J., Deng S., Duan J.I.E., Xie X., Xu S., Ran M., Dai X., Pu Y.U., Zhang X. FBXL20 acts as an invasion inducer and mediates E-cadherin in colorectal adenocarcinoma. Oncol. Lett. 2014, 7:2185-2191.
161. Huber C., Dias-Santagata D., Glaser A., O'Sullivan J., Brauner R., Wu K., Xu X., Pearce K., Wang R., Uzielli M.L.G., Dagoneau N., Chemaitilly W., Superti-Furga A., Santos H.D., Megarbane A., Morin G., Gillessen-Kaesbach G., Hennekam R., Burgt I.V., Black d., Clayton G.C.M., Read P.E., Merrer A., Scambler M.L., Munnich P.J., Pan A., Winter Z.-Q., Cormier-Daire R.V. Identification of mutations in CUL7 in 3-syndrome. Nat. Genet. 2005, 37:1119-1124.
162. Ponyeam W., Hagen T. Characterization of the Cullin7 E3 ubiquitin ligase - heterodimerization of cullin substrate receptors as a novel mechanism to regulate cullin E3 ligase activity. Cell. Signal. 2012, 24:290-295.
163. Okabe H., Lee S.H., Phuchareon J., Albertson D.G., McCormick F., Tetsu O. A critical role for FBXW8 and MAPK in cyclin D1 degradation and cancer cell proliferation. PloS ONE 2006, 1:e128.
164. Xu X., Sarikas A., Dias-Santagata D.C., Dolios G., Lafontant P.J., Tsai S.-C., Zhu W., Nakajima H., Nakajima H.O., Field L.J., Wang R., Pan Z.-Q. The CUL7 E3 ubiquitin ligase targets insulin receptor substrate 1 for ubiquitin-dependent degradation. Mol. Cell 2008, 30:403-414.
165. Litterman N., Ikeuchi Y., Gallardo G., O'Connell B.C., Sowa M.E., Gygi S.P., Harper J.W., Bonni A. An OBSL1-Cul7Fbxw8 ubiquitin ligase signaling mechanism regulates golgi morphology and dendrite patterning. PLoS Biol. 2011, 9:e1001060.
166. Barbash O., Zamfirova P., Lin D.I., Chen X., Yang K., Nakagawa H., Lu F., Rustgi A.K., Diehl J.A. Mutations in Fbx4 inhibit dimerization of the SCFFbx4 ligase and contribute to cyclin D1 overexpression in human cancer. Cancer Cell 2008, 14:68-78.
167. Lin D.I., Barbash O., Kumar K.G.S., Weber J.D., Harper J.W., Klein-Szanto A.P., Rustgi A., Fuchs S., Diehl J.A. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCFFBX4-αB crystallin complex. Mol. Cell 2006, 24:355-366.
168. Koepp D.M., Schaefer L.K., Ye X., Keyomarsi K., Chu C., Harper J.W., Elledge S.J. Phosphorylation-dependent ubiquitination of cyctin E by the SCFFbw7 ubiquitin ligase. Science 2001, 294:173-177.
169. Lee T.H., Perrem K., Harper J.W., Lu K.P., Zhou X.Z. The F-box protein FBX4 targets PIN2/TRF1 for ubiquitin-mediated degradation and regulates telomere maintenance. J. Biol. Chem. 2006, 281:759-768.
170. Chen J.-Y., Wang M.-C., Hung W.-C. Bcr-Abl-induced tyrosine phosphorylation of Emi1 to stabilize Skp2 protein via inhibition of ubiquitination in chronic myeloid leukemia cells. J. Cell. Physiol. 2011, 226:407-413.
171. Lehman N.L., Tibshirani R., Hsu J.Y., Natkunam Y., Harris B.T., West R.B., Masek M.A., Montgomery K., van de Rijn M., Jackson P.K. Oncogenic regulators and substrates of the anaphase promoting complex/cyclosome are frequently overexpressed in malignant tumors. Am. J. Pathol. 2007, 170:1793-1805.
172. Fernández-Sáiz V., Targosz B.-S., Lemeer S., Eichner R., Langer C., Bullinger L., Reiter C., Slotta-Huspenina J., Schroeder S., Knorn A.-M., Kurutz J., Peschel C., Pagano M., Kuster B., Bassermann F. SCFFbxo9 and CK2 direct the cellular response to growth factor withdrawal via Tel2/Tti1 degradation and promote survival in multiple myeloma. Nat. Cell Biol. 2013, 15:72-81.
173. Smits B.M.G., Traun B.D., Devries T.L., Tran A., Samuelson D., Haag J.D., Gould M. An insulator loop resides between the synthetically interacting elements of the human/rat conserved breast cancer susceptibility locus MCS5A/Mcs5a. Nucleic Acids Res. 2012, 40:132-147.
174. Xu X., Powell D.W., Lambring C.J., Puckett A.H., Deschenes L., Prough R.A., Poeschla E.M., Samuelson D.J. Human MCS5A1 candidate breast cancer susceptibility gene FBXO10 is induced by cellular stress and correlated with lens epithelium-derived growth factor (LEDGF). Mol. Carcinog. 2014, 53:300-313.
175. Samuelson D.J., Hesselson S.E., Aperavich B.A., Zan Y., Haag J.D., Trentham-Dietz A., Hampton J.M., Mau B., Chen K.-S., Baynes C., Khaw K.-T., Luben R., Perkins B., Shah M., Pharoah P.D., Dunning A.M., Easton D.F., Ponder B.A., Gould M.N. Rat Mcs5a is a compound quantitative trait locus with orthologous human loci that associate with breast cancer risk. Proc. Natl. Acad. Sci. 2007, 104:6299-6304.
176. Zheng H., Shen M., Zha Y.-L., Li W., Wei Y., Blanco Mario A., Ren G., Zhou T., Storz P., Wang H.-Y., Kang Y. PKD1 phosphorylation-dependent degradation of SNAIL by SCF-FBXO11 regulates epithelial-mesenchymal transition and metastasis. Cancer Cell 2014, 26:358-373.
177. Jeong Y.-T., Cermak L., Guijarro M., Hernando E., Pagano M. FBH1 protects melanocytes from transformation and is deregulated in melanomas. Cell Cycle 2013, 12:1128-1132.
178. Jeong Y.-T., Rossi M., Cermak L., Saraf A., Florens L., Washburn M.P., Sung P., Schildkraut C.L., Pagano M. FBH1 promotes DNA double-strand breakage and apoptosis in response to DNA replication stress. J. Cell Biol. 2013, 200:141-149.
179. Fugger K., Mistrik M., Danielsen J.R., Dinant C., Falck J., Bartek J., Lukas J., Mailand N. Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. J. Cell Biol. 2009, 186:655-663.
180. Huang H.-L., Zheng W.-L., Zhao R., Zhang B., Ma W.-L. FBXO31 is down-regulated and may function as a tumor suppressor in hepatocellular carcinoma. Oncol. Rep. 2010, 24:715-720.
181. Kogo R., Mimori K., Tanaka F., Komune S., Mori M. FBXO31 determines poor prognosis in esophageal squamous cell carcinoma. Int. J. Oncol. 2011, 39:155-159.