The Skp2-SCF E3 ligase regulates akt ubiquitination, glycolysis, herceptin sensitivity, and tumorigenesis

Cell

Volumn 149, Issue 5, 2012, Pages 1098-1111

  Chan, Chia Hsin ^a   Li, Chien Feng ^c,d,i   Yang, Wei Lei ^a,b   Gao, Yuan ^a,b   Lee, Szu Wei ^a,b   Feng, Zizhen ^a   Huang, Hsuan Ying ^e   Tsai, Kelvin K C ^d   Flores, Leo G ^a   Shao, Yiping ^a   Hazle, John D ^a   Yu, Dihua ^a,b   Wei, Wenyi ^f   Sarbassov, Dos ^a,b   Hung, Mien Chie ^a,b,h   Nakayama, Keiichi I ^g   Lin, Hui Kuan ^a,b  

^a UNIVERSITY OF TEXAS   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c Chi Mei Foundational Medical Center   (Taiwan)

^d NATIONAL HEALTH RESEARCH INSTITUTES   (Taiwan)

^e CHANG GUNG UNIVERSITY   (Taiwan)

^f HARVARD MEDICAL SCHOOL   (United States)

^g KYUSHU UNIVERSITY   (Japan)

^h CHINA MEDICAL UNIVERSITY   (Taiwan)

ⁱ SOUTHERN TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

EPIDERMAL GROWTH FACTOR; GLUCOSE; GLUCOSE TRANSPORTER 1; GROWTH FACTOR; PROTEIN KINASE B; RECEPTOR PROTEIN; TRASTUZUMAB; TUMOR MARKER; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UBIQUITIN PROTEIN LIGASE E3;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST TUMOR; CANCER CELL CULTURE; CANCER GROWTH; CARCINOGENESIS; CONTROLLED STUDY; DRUG SENSITIVITY; FEMALE; GENE SILENCING; GLYCOLYSIS; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UBIQUITINATION;

EID: 84861552793     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.02.065     Document Type: Article

References (46)

1. D.B. Agus, R.W. Akita, W.D. Fox, G.D. Lewis, B. Higgins, P.I. Pisacane, J.A. Lofgren, C. Tindell, D.P. Evans, and K. Maiese Targeting ligand-activated ErbB2 signaling inhibits breast and prostate tumor growth Cancer Cell 2 2002 127 137
2. J. Aragonés, P. Fraisl, M. Baes, and P. Carmeliet Oxygen sensors at the crossroad of metabolism Cell Metab. 9 2009 11 22
3. A. Barthel, S.T. Okino, J. Liao, K. Nakatani, J. Li, J.P. Whitlock Jr.; R.A. Roth Regulation of GLUT1 gene transcription by the serine/threonine kinase Akt1 J. Biol. Chem. 274 1999 20281 20286
4. M.J. Birnbaum On the InterAktion between hexokinase and the mitochondrion Dev. Cell 7 2004 781 782
5. G. Bornstein, J. Bloom, D. Sitry-Shevah, K. Nakayama, M. Pagano, and A. Hershko Role of the SCFSkp2 ubiquitin ligase in the degradation of p21Cip1 in S phase J. Biol. Chem. 278 2003 25752 25757
6. D.P. Brazil, J. Park, and B.A. Hemmings PKB binding proteins. Getting in on the Akt Cell 111 2002 293 303
7. C.H. Chan, S.W. Lee, C.F. Li, J. Wang, W.L. Yang, C.Y. Wu, J. Wu, K.I. Nakayama, H.Y. Kang, and H.Y. Huang Deciphering the transcriptional complex critical for RhoA gene expression and cancer metastasis Nat. Cell Biol. 12 2010 457 467
8. C.H. Chan, S.W. Lee, J. Wang, and H.K. Lin Regulation of Skp2 expression and activity and its role in cancer progression ScientificWorldJournal 10 2010 1001 1015
9. C.H. Chan, Y. Gao, A. Moten, and H.K. Lin Novel ARF/p53-independent senescence pathways in cancer repression J. Mol. Med. (Berl.) 89 2011 857 867
10. K. Datta, T.F. Franke, T.O. Chan, A. Makris, S.I. Yang, D.R. Kaplan, D.K. Morrison, E.A. Golemis, and P.N. Tsichlis AH/PH domain-mediated interaction between Akt molecules and its potential role in Akt regulation Mol. Cell. Biol. 15 1995 2304 2310
11. R.J. DeBerardinis, J.J. Lum, G. Hatzivassiliou, and C.B. Thompson The biology of cancer: metabolic reprogramming fuels cell growth and proliferation Cell Metab. 7 2008 11 20
12. R.L. Elstrom, D.E. Bauer, M. Buzzai, R. Karnauskas, M.H. Harris, D.R. Plas, H. Zhuang, R.M. Cinalli, A. Alavi, C.M. Rudin, and C.B. Thompson Akt stimulates aerobic glycolysis in cancer cells Cancer Res. 64 2004 3892 3899
13. D. Gao, H. Inuzuka, A. Tseng, R.Y. Chin, A. Toker, and W. Wei Phosphorylation by Akt1 promotes cytoplasmic localization of Skp2 and impairs APCCdh1-mediated Skp2 destruction Nat. Cell Biol. 11 2009 397 408
14. H.Y. Huang, H.Y. Kang, C.F. Li, H.L. Eng, S.C. Chou, C.N. Lin, and C.Y. Hsiung Skp2 overexpression is highly representative of intrinsic biological aggressiveness and independently associated with poor prognosis in primary localized myxofibrosarcomas Clin. Cancer Res. 12 2006 487 498
15. N.E. Hynes, and G. MacDonald ErbB receptors and signaling pathways in cancer Curr. Opin. Cell Biol. 21 2009 177 184
16. B.H. Jiang, G. Jiang, J.Z. Zheng, Z. Lu, T. Hunter, and P.K. Vogt Phosphatidylinositol 3-kinase signaling controls levels of hypoxia-inducible factor 1 Cell Growth Differ. 12 2001 363 369
17. S.Y. Kim, A. Herbst, K.A. Tworkowski, S.E. Salghetti, and W.P. Tansey Skp2 regulates Myc protein stability and activity Mol. Cell 11 2003 1177 1188
18. G. Künstle, J. Laine, G. Pierron, S. Kagami Si, H. Nakajima, F. Hoh, C. Roumestand, M.H. Stern, and M. Noguchi Identification of Akt association and oligomerization domains of the Akt kinase coactivator TCL1 Mol. Cell. Biol. 22 2002 1513 1525
19. S.T. Lee-Hoeflich, L. Crocker, E. Yao, T. Pham, X. Munroe, K.P. Hoeflich, M.X. Sliwkowski, and H.M. Stern A central role for HER3 in HER2-amplified breast cancer: implications for targeted therapy Cancer Res. 68 2008 5878 5887
20. H.K. Lin, S. Bergmann, and P.P. Pandolfi Cytoplasmic PML function in TGF-beta signalling Nature 431 2004 205 211
21. H.K. Lin, G. Wang, Z. Chen, J. Teruya-Feldstein, Y. Liu, C.H. Chan, W.L. Yang, H. Erdjument-Bromage, K.I. Nakayama, and S. Nimer Phosphorylation- dependent regulation of cytosolic localization and oncogenic function of Skp2 by Akt/PKB Nat. Cell Biol. 11 2009 420 432
22. H.K. Lin, Z. Chen, G. Wang, C. Nardella, S.W. Lee, C.H. Chan, W.L. Yang, J. Wang, A. Egia, and K.I. Nakayama Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence Nature 464 2010 374 379
23. P. Liu, H. Cheng, T.M. Roberts, and J.J. Zhao Targeting the phosphoinositide 3-kinase pathway in cancer Nat. Rev. Drug Discov. 8 2009 627 644
24. P.K. Majumder, P.G. Febbo, R. Bikoff, R. Berger, Q. Xue, L.M. McMahon, J. Manola, J. Brugarolas, T.J. McDonnell, and T.R. Golub mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways Nat. Med. 10 2004 594 601
25. B.D. Manning, and L.C. Cantley AKT/PKB signaling: navigating downstream Cell 129 2007 1261 1274
26. K.I. Nakayama, and K. Nakayama Ubiquitin ligases: cell-cycle control and cancer Nat. Rev. Cancer 6 2006 369 381
27. K. Nakayama, H. Nagahama, Y.A. Minamishima, M. Matsumoto, I. Nakamichi, K. Kitagawa, M. Shirane, R. Tsunematsu, T. Tsukiyama, and N. Ishida Targeted disruption of Skp2 results in accumulation of cyclin E and p27(Kip1), polyploidy and centrosome overduplication EMBO J. 19 2000 2069 2081
28. M. Noguchi, V. Ropars, C. Roumestand, and F. Suizu Proto-oncogene TCL1: more than just a coactivator for Akt FASEB J. 21 2007 2273 2284
29. R.G. Oshima, J. Lesperance, V. Munoz, L. Hebbard, B. Ranscht, N. Sharan, W.J. Muller, C.A. Hauser, and R.D. Cardiff Angiogenic acceleration of Neu induced mammary tumor progression and metastasis Cancer Res. 64 2004 169 179
30. R.C. Osthus, H. Shim, S. Kim, Q. Li, R. Reddy, M. Mukherjee, Y. Xu, D. Wonsey, L.A. Lee, and C.V. Dang Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc J. Biol. Chem. 275 2000 21797 21800
31. H. Pelicano, D.S. Martin, R.H. Xu, and P. Huang Glycolysis inhibition for anticancer treatment Oncogene 25 2006 4633 4646
32. D.R. Plas, and C.B. Thompson Akt-dependent transformation: there is more to growth than just surviving Oncogene 24 2005 7435 7442
33. R.B. Robey, and N. Hay Is Akt the "Warburg kinase"?-Akt-energy metabolism interactions and oncogenesis Semin. Cancer Biol. 19 2009 25 31
34. H. Shim, C. Dolde, B.C. Lewis, C.S. Wu, G. Dang, R.A. Jungmann, R. Dalla-Favera, and C.V. Dang c-Myc transactivation of LDH-A: implications for tumor metabolism and growth Proc. Natl. Acad. Sci. USA 94 1997 6658 6663
35. M.J. van de Vijver, Y.D. He, L.J. van't Veer, H. Dai, A.A. Hart, D.W. Voskuil, G.J. Schreiber, J.L. Peterse, C. Roberts, and M.J. Marton A gene-expression signature as a predictor of survival in breast cancer N. Engl. J. Med. 347 2002 1999 2009
36. M.G. Vander Heiden, L.C. Cantley, and C.B. Thompson Understanding the Warburg effect: the metabolic requirements of cell proliferation Science 324 2009 1029 1033
37. N. von der Lehr, S. Johansson, S. Wu, F. Bahram, A. Castell, C. Cetinkaya, P. Hydbring, I. Weidung, K. Nakayama, and K.I. Nakayama The F-box protein Skp2 participates in c-Myc proteosomal degradation and acts as a cofactor for c-Myc-regulated transcription Mol. Cell 11 2003 1189 1200
38. H. Wang, F. Bauzon, P. Ji, X. Xu, D. Sun, J. Locker, R.S. Sellers, K. Nakayama, K.I. Nakayama, D. Cobrinik, and L. Zhu Skp2 is required for survival of aberrantly proliferating Rb1-deficient cells and for tumorigenesis in Rb1+/- mice Nat. Genet. 42 2010 83 88
39. O. Warburg On the origin of cancer cells Science 123 1956 309 314
40. H.L. Wieman, J.A. Wofford, and J.C. Rathmell Cytokine stimulation promotes glucose uptake via phosphatidylinositol-3 kinase/Akt regulation of Glut1 activity and trafficking Mol. Biol. Cell 18 2007 1437 1446
41. Z.P. Xia, L. Sun, X. Chen, G. Pineda, X. Jiang, A. Adhikari, W. Zeng, and Z.J. Chen Direct activation of protein kinases by unanchored polyubiquitin chains Nature 461 2009 114 119
42. W.L. Yang, J. Wang, C.H. Chan, S.W. Lee, A.D. Campos, B. Lamothe, L. Hur, B.C. Grabiner, X. Lin, B.G. Darnay, and H.K. Lin The E3 ligase TRAF6 regulates Akt ubiquitination and activation Science 325 2009 1134 1138
43. W.L. Yang, C.Y. Wu, J. Wu, and H.K. Lin Regulation of Akt signaling activation by ubiquitination Cell Cycle 9 2010 487 497
44. W.L. Yang, X. Zhang, and H.K. Lin Emerging role of Lys-63 ubiquitination in protein kinase and phosphatase activation and cancer development Oncogene 29 2010 4493 4503
45. W. Zeng, L. Sun, X. Jiang, X. Chen, F. Hou, A. Adhikari, M. Xu, and Z.J. Chen Reconstitution of the RIG-I pathway reveals a signaling role of unanchored polyubiquitin chains in innate immunity Cell 141 2010 315 330
46. A. Zhu, D. Lee, and H. Shim Metabolic positron emission tomography imaging in cancer detection and therapy response Semin. Oncol. 38 2011 55 69