The ubiquitin-proteasome system and signal transduction pathways regulating Epithelial Mesenchymal transition of cancer

Journal of Biomedical Science

Volumn 19, Issue 1, 2012, Pages

  Voutsadakis, Ioannis A ^a  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Carcinogenesis; Epithelial to mesenchymal transition; Signal transduction; Ubiquitin proteasome system; Ubiquitination

Indexed keywords

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3; PROTEASOME; UBIQUITIN; UBIQUITIN PROTEIN LIGASE E3;

CELLULAR DISTRIBUTION; ENDOCYTOSIS; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; LYSOSOME; NEOPLASM; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; APOPTOSIS; CELL PROLIFERATION; CELL TRANSFORMATION; GENETICS; METABOLISM; NEOVASCULARIZATION (PATHOLOGY);

APOPTOSIS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; PROTEASOME ENDOPEPTIDASE COMPLEX; SIGNAL TRANSDUCTION; UBIQUITIN;

EID: 84864996678     PISSN: 10217770     EISSN: 14230127     Source Type: Journal    
DOI: 10.1186/1423-0127-19-67     Document Type: Review

References (125)

1. Complex networks orchestrate epithelial-mesenchymal transitions. Thiery JP, Sleeman JP, Nature Rev Mol Cell Biol 2006 7 131 142 (Pubitemid 43278296)
2. Epithelial-mesenchymal transitions: the importance of changing cell state in development and disease. Acloque H, Adams MS, Fishwick K, Bronner-Fraser M, Nieto MA, J Clin Invest 2009 119 1438 1449
3. The basics of epithelial-mesenchymal transition. Kalluri R, Weinberg RA, J Clin Invest 2009 119 1420 1428
4. Biomarkers for epithelial-mesenchymal transitions. Zeisberg M, Neilson EG, J Clin Invest 2009 119 1429 1437
5. The epithelial-mesenchymal transition generates cells with properties of stem cells. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA, Cell 2008 133 704 715 (Pubitemid 351636299)
6. The fallacy of epithelial-mesenchymal transition in neoplasia. Tarin D, Cancer Res 2005 65 5996 6001
7. Hallmarks of cancer: The next generation. Hanahan D, Weinberg RA, Cell 2011 144 646 674
8. Epithelial-mesenchymal transition in cancer: parallels between normal development and tumor progression. Micalizzi DS, Farabaugh SM, Ford HL, J Mammary Gland Biol Neoplasia 2010 15 117 134
9. Ubiquitin, ubiquitination and the ubiquitin-proteasome system in cancer. Voutsadakis IA, Atlas Genet Cytogen Oncol Haematol 2010 14 1088 1099 http://AtlasGeneticsOncology.org/Deep/UbiquitinCancerID20083.httml
10. Polyubiquitin chains: functions, structures, and mechanisms. Li W, Ye Y, Cell Mol Life Sci 2008 65 2397 2406
11. Physiological functions of the HECT family of ubiquitin ligases. Rotin D, Kumar S, Nat Rev Mol Cell Biol 2009 10 398 409
12. Mechanism and function of deubiquitinating enzymes. Amerik AY, Hochstrasser M, Biochim Biophys Acta 2004 1695 189 207 (Pubitemid 39574973)
13. Pathogenesis of colorectal carcinoma and therapeutic implications: the roles of the ubiquitin-proteasome system and Cox-2. Voutsadakis IA, J Cell Mol Med 2007 11 252 285 (Pubitemid 46695694)
14. The proteasome: a proteolytic nanomachine of cell regulation and waste disposal. Wolf DH, Hilt W, Biochim Biophys Acta 2004 1695 19 31 (Pubitemid 39574965)
15. Targeting Wnt signaling: can we safely eradicate cancer stem cells? Takahashi-Yanaga F, Kahn M, Clin Cancer Res 2010 16 3153 3162
16. A Wnt-Axin2-GSK3 cascade regulates Snail1 activity in breast cancer cells. Yook JI, Li XY, Ota I, Hu C, Kim HS, Kim NH, Cha SY, Ryu JK, Choi YJ, Kim J, Fearon ER, Weiss SJ, Nat Cell Biol 2006 8 1398 1406 (Pubitemid 44835115)
17. A novel lung metastasis signature links Wnt signaling with cancer self-renewal and epithelial-mesenchymal transition in basal-like breast cancer. DiMeo TA, Anderson K, Phadke P, Fan C, Perou CM, Naber S, Kuperwasser C, Cancer Res 2009 69 5364 5373
18. Cross-talk of WNT and FGF signalling pathways at GSK3 to regulate -catenin and SNAIL signalling cascades. Katoh M, Katoh M, Cancer Biol Ther 2006 5 1059 1064 (Pubitemid 44772212)
19. A Mutant-p53/Smad complex opposes p63 to empower TGFbeta-induced metastasis. Adorno M, Cordenonsi M, Montagner M, Dupont S, Wong C, Hann B, Solari A, Bobisse S, Rondina MB, Guzzardo V, Parenti AR, Rosato A, Bicciato S, Balmain A, Piccolo S, Cell 2009 137 87 98
20. Sustained TGF exposure suppresses Smad and non-Smad signalling in mammary epithelial cells, leading to EMT and inhibition of growth arrest and apoptosis. Gal A, Sjöblom T, Fedorova L, Imreh S, Beug H, Moustakas A, Oncogene 2008 27 1218 1230 (Pubitemid 351294691)
21. Transforming growth factor-1 induces epithelial-to-mesenchymal transition and apoptosis via a cell cycle-dependent mechanism. Yang Y, Pan X, Lei W, Wang J, Song J, Oncogene 2006 25 7235 7244 (Pubitemid 44809089)
22. Latent TGF- structure and activation. Shi M, Zhu J, Wang R, Chen X, Mi L, Walz T, Springer TA, Nature 2011 474 343 349
23. TGF- activates Erk MAP kinase signalling through direct phosphorylation of ShcA. Lee MK, Pardoux C, Hall MC, Lee PS, Warburton D, Qing J, Smith SM, Derynck R, EMBO J 2007 26 3957 3967 (Pubitemid 47367487)
24. TGF induces SIK to negatively regulate type I receptor kinase signalling. Kowanetz M, Lönn P, Vanlandewijck M, Kowanetz K, Heldin CH, Moustakas A, J Cell Biol 2008 182 655 662
25. Regulation of TGF- family signalling by E3 ubiquitin ligases. Inoue Y, Imamura T, Cancer Sci 2008 99 2107 2112
26. Peroxisome proliferator-activated receptor- activation inhibits tumor metastasis by antagonizing Smad3-mediated epithelial-mesenchymal transition. Reka AK, Kurapati H, Narala VR, Bommer G, Chen J, Standiford TJ, Keshamouni VG, Mol Cancer Ther 2010 9 3221 3232
27. TGF - induced epithelial to mesenchymal transition. Xu J, Lamouille S, Derynck R, Cell Res 2009 19 156 172
28. Complete reversal of epithelial to mesenchymal transition requires inhibition of both ZEB expression and the Rho pathway. Das S, Becker BN, Hoffmann FM, Mertz JE, BMC Cell Biol 2009 10 94
29. Mesenchyme Forkhead 1 (FOXC2) plays a key role in metastasis and is associated with aggressive basal-like breast cancers. Mani SA, Yang J, Brooks M, Schwaninger G, Zhou A, Miura N, Kutok JL, Hartwell K, Richardson AL, Weinberg RA, Proc Natl Acad Sci U S A 2007 104 10069 10074 (Pubitemid 47175264)
30. Forkhead transcription factor Foxq1 promotes Epithelial-Mesenchymal transition and breast cancer metastasis. Zhang H, Meng F, Liu G, Zhang B, Zhu J, Wu F, Ethier SP, Miller F, Wu G, Cancer Res 2011 71 1292 1301
31. FOXQ1 regulates Epithelial-Mesenchymal Transition in human cancers. Qiao Y, Jiang X, Lee ST, Karuturi RK, Hooi SC, Yu Q, Cancer Res 2011 71 3076 3086
32. Role of Ras signalling in the induction of snail by transforming growth factor- Horiguchi K, Shirakihara T, Nakano A, Imamura T, Miyazono K, Saitoh M, J Biol Chem 2009 284 245 253
33. TGF-1-induced expression of human Mdm2 correlates with late-stage metastatic breast cancer. Araki S, Eitel JA, Batuello CN, Bijangi-Vishehsaraei K, Xie XJ, Danielpour D, Pollok KE, Boothman DA, Mayo LD, J Clin Invest 2010 120 290 302
34. Regulation of the polarity protein Par6 by TGF receptors controls epithelial cell plasticity. Ozdamar B, Bose R, Barrios-Rodiles M, Wang HR, Zhang Y, Wrana JL, Science 2005 307 1603 1609 (Pubitemid 40354739)
35. The canonical Notch signalling pathway: unfolding the activation mechanism. Kopan R, Ilagan MXG, Cell 2009 137 216 233
36. Non-canonical activation of Notch signaling/target genes in vertebrates. Sanalkumar R, Dhanesh SB, James J, Cell Mol Life Sci 2010 67 2957 2968
37. The multiple facets of ubiquitination in the regulation of Notch signaling pathway. Le Bras S, Loyer N, Le Borgne R, Traffic 2011 12 149 161
38. The Notch signaling pathway: transcriptional regulation at Notch target genes. Borggrefe T, Oswald F, Cell Mol Life Sci 2009 66 1631 1646
39. Hypoxia-induced Jagged2 promotes breast cancer metastasis and self-renewal of cancer stem-like cells. Xing F, Okuda H, Watabe M, Kobayashi A, Pai SK, Liu W, Pandey PR, Fukuda K, Hirota S, Sugai T, Wakabayshi G, Koeda K, Kashiwaba M, Suzuki K, Chiba T, Endo M, Mo YY, Watabe K, Oncogene 2011 30 4075 4086
40. Acquisition of epithelial-mesenchymal transition phenotype of gemcitabine-resistant pancreatic cancer cells is linked with activation of the Notch signalling pathway. Wang Z, Li Y, Kong D, Banerjee S, Ahmad A, Azmi AS, Ali S, Abbruzzese JL, Gallick GE, Sarkar FH, Cancer Res 2009 69 2400 2407
41. Notch activation induces Akt signalling via an autocrine loop to prevent apoptosis in breast epithelial cells. Meurette O, Stylianou S, Rock R, Collu GM, Gilmore AP, Brennan K, Cancer Res 2009 69 5015 5022
42. Notch1 mediates visfatin-induced FGF-2 up-regulation and endothelial angiogenesis. Bae YH, Park HJ, Kim SR, Kim JY, Kang Y, Kim JA, Wee HJ, Kageyama R, Jung JS, Bae MK, Bae SK, Cardiovasc Res 2011 89 436 445
43. Hypoxia potentiates Notch signalling in breast cancer leading to decreased E-cadherin expression and increased cell migration and invasion. Chen J, Imanaka N, Chen J, Griffin JD, Br J Cancer 2010 102 351 360
44. Integration of TGF-/Smad and Jagged1/Notch signalling in epithelial-to-mesenchymal transition. Zavadil J, Cermak L, Soto-Nieves N, Böttinger EP, EMBO J 2004 23 1155 1165 (Pubitemid 38436879)
45. Hedgehog signalling promotes the degradation of tumor suppressor Sufu through the ubiquitin-proteasome pathway. Yue S, Chen Y, Cheng SY, Oncogene 2009 28 492 499
46. Multiple ubiquitin-dependent processing pathways regulate Hedgehog/Gli signalling. Di Marcotullio L, Ferretti E, Greco A, De Smaele E, Screpanti I, Gulino A, Cell Cycle 2007 6 390 393
47. Hedgehog and epithelial-mesenchymal transition signalling in normal and malignant epithelial cells of the esophagus. Isohata N, Aoyagi K, Mabuchi T, Daiko H, Fukaya M, Ohta H, Ogawa K, Yoshida T, Sasaki H, Int J Cancer 2009 125 1212 1221
48. Cross talk between hedgehog and epithelial-mesenchymal transition pathways in gastric pit cells and in diffuse-type gastric cancers. Ohta H, Aoyagi K, Fukaya M, Danjoh I, Ohta A, Isohata N, Saeki N, Taniguchi H, Sakamoto H, Shimoda T, Tani T, Yoshida T, Sasaki H, Br J Cancer 2009 100 389 398
49. Gli1 enhances migration and invasion via up-regulation of MMP-11 and promotes metastasis in ER negative breast cancer cell lines. Kwon Y-J, Hurst DR, Steg AD, Yuan K, Vaidya KS, Welch DR, Frost AR, Clin Exp Metastasis 2011 28 437 449
50. Wnt signalling stimulates transcriptional outcome of the Hedgehog pathway by stabilizing GLI1 mRNA. Noubissi FK, Goswami S, Sanek NA, Kawakami K, Minamoto T, Moser A, Grinblat Y, Spiegelman VS, Cancer Res 2009 69 8572 8578
51. Aberrant activation of hedgehog signalling pathway contributes to endometrial carcinogenesis through -catenin. Liao X, Siu MK, Au CW, Chan QK, Chan HY, Wong ES, Ip PP, Ngan HY, Cheung AN, Mod Pathol 2009 22 839 847
52. Gli1 acts through Snail and E-cadherin to promote nuclear signalling by -catenin. Li X, Deng W, Lobo-Ruppert SM, Ruppert JM, Oncogene 2007 26 4489 4498 (Pubitemid 47037042)
53. Human colon cancer epithelial cells harbour active HEDGEHOG-GLI signalling that is essential for tumour growth, recurrence, metastasis and stem cell survival and expansion. Varnat F, Duquet A, Malerba M, Zbinden M, Mas C, Gervaz P, Ruiz i Altaba A, EMBO Mol Med 2009 1 338 351
54. Gli1, downregulated in colorectal cancers, inhibits proliferation of colon cancer cells involving Wnt signalling activation. Akiyoshi T, Nakamura M, Koga K, Nakashima H, Yao T, Tsuneyoshi M, Tanaka M, Katano M, Gut 2006 55 991 999 (Pubitemid 43962612)
55. Hedgehog signalling overrides p53-mediated tumor suppression by activating Mdm2. Abe Y, Oda-Sato E, Tobiume K, Kawauchi K, Taya Y, Okamoto K, Oren M, Tanaka N, Proc Natl Acad Sci U S A 2008 105 4838 4843 (Pubitemid 351753833)
56. Up-regulation of Sonic Hedgehog contributes to TGF-1-induced epithelial to mesenchymal transition in NSCLC cells. Maitah M, Ali S, Ahmad A, Gadgeel S, Sarkar FH, PLoS One 2011 6 16068
57. Epithelial-mesenchymal transition in development and cancer: role of phosphatidylinositol 3 kinase/AKT pathways. Larue L, Bellacosa A, Oncogene 2005 24 7443 7454 (Pubitemid 41637984)
58. PI3K-dependent phosphorylation of Fbw7 modulates substrate degradation and activity. Schülein C, Eilers M, Popov N, FEBS Lett 2011 585 2151 2157
59. p70 S6 kinase promotes epithelial to mesenchymal transition through Snail induction in ovarian cancer cells. Pon YL, Zhou HY, Cheung ANY, Ngan HY, Wong AS, Cancer Res 2008 68 6524 6532
60. Epidermal Growth Factor Receptor cooperates with Signal Transducer and Activator of Transcription 3 to induce epithelial-mesenchymal transition in cancer cells via up-regulation of TWIST gene expression. Lo H-W, Hsu S-C, Xia W, Cao X, Shih JY, Wei Y, Abbruzzese JL, Hortobagyi GN, Hung MC, Cancer Res 2007 67 9066 9076 (Pubitemid 47535891)
61. Cell adhesion protects c-Raf-1 against ubiquitin-dependent degradation by the proteasome. Manenti S, Delmas C, Darbon JM, Biochem Biophys Res Commun 2002 294 976 980 (Pubitemid 34687145)
62. The PHD domain of MEKK1 acts as an E3 ubiquitin ligase and mediates ubiquitination and degradation of ERK1/2. Lu Z, Xu S, Joazeiro C, Cobb MH, Hunter T, Mol Cell 2002 9 945 956 (Pubitemid 34626666)
63. Rapid turnover of Extracellular Signal-Regulated kinase 3 by the Ubiquitin-Proteasome Pathway defines a novel paradigm of Mitogen-Activated Protein Kinase regulation during cellular differentiation. Coulombe P, Rodier G, Pelletier S, Pellerin J, Meloche S, Mol Cell Biol 2003 23 4542 4558 (Pubitemid 36734745)
64. Down-regulation of ubiquitin ligase Cbl induced by twist haploinsufficiency in Saethre-Chotzen syndrome results in increased PI3K/Akt signalling and osteoblast proliferation. Guenou H, Kaabeche K, Dufour C, Miraoui H, Marie PJ, Am J Pathol 2006 169 1303 1311 (Pubitemid 351194365)
65. Proteasome-dependent decrease in Akt by growth factors in vascular smooth muscle cells. Adachi M, Katsumura KR, Fujii K, Kobayashi S, Aoki H, Matsuzaki M, FEBS Lett 2003 554 77 80 (Pubitemid 37324818)
66. ERK and the F-box protein TRCP target STAT1 for degradation. Soond SM, Townsend PA, Barry SP, Knight RA, Latchman DS, Stephanou A, J Biol Chem 2008 283 16077 16083
67. Endocytosis and signalling: intertwining molecular networks. Sorkin A, von Zastrow M, Nature Rev Mol Cell Biol 2009 10 609 622
68. A direct role for Met endocytosis in tumorigenesis. Joffre C, Barrow R, Ménard L, Calleja V, Hart IR, Kermorgant S, Nature Cell Biol 2011 13 827 837
69. A Twist-Snail axis critical for TrkB-induced epithelial-mesenchymal transition-like transformation, anoikis resistance, and metastasis. Smit MA, Geiger TR, Song J-Y, Gitelman I, Peeper DS, Mol Cell Biol 2009 29 3722 3737
70. Zeb1 is required for TrkB-induced epithelial-mesenchymal transition, anoikis resistance and metastasis. Smit MA, Peeper DS, Oncogene 2011 30 3735 3744
71. TrkB induces EMT and has a key role in invasion of head and neck squamous cell carcinoma. Kupferman ME, Jiffar T, El-Naggar A, Yilmaz T, Zhou G, Xie T, Feng L, Wang J, Holsinger FC, Yu D, Myers JN, Oncogene 2010 29 2047 2059
72. PTEN loss induces epithelial-mesenchymal transition in human colon cancer cells. Bowen KA, Doan HQ, Zhou BP, Wang Q, Zhou Y, Rychahou PG, Evers BM, Anticancer Res 2009 29 4439 4450
73. mTORC1 and mTORC2 regulate EMT, motility, and metastasis of colorectal cancer via RhoA and Rac1 signaling pathways. Gulhati P, Bowen KA, Liu J, Liu J, Stevens PD, Rychahou PG, Chen M, Lee EY, Weiss HL, OConnor KL, Gao T, Evers BM, Cancer Res 2011 71 3246 3256
74. Epithelial-mesenchymal-transition induced by EGFR activation interferes with cell migration and response to irradiation and cetuximab in head and neck cancer cells. Holz C, Niehr F, Boyko M, Hristozova T, Distel L, Budach V, Tinhofer I, Radiother Oncol 2011 101 158 64
75. Met induces mammary tumors with diverse histologies and is associated with poor outcome and human basal breast cancer. Ponzo MG, Lesurf R, Petkiewicz S, OMalley FP, Pinnaduwage D, Andrulis IL, Bull SB, Chughtai N, Zuo N, Souleimanova M, Germain D, Omeroglu A, Cardiff RD, Hallett M, Park M, Proc Natl Acad Sci U S A 2009 106 12903 12908
76. Rack1 promotes epithelial cell-cell adhesion by regulating E-cadherin endocytosis. Swaminathan G, Cartwright CA, Oncogene 2012 31 376 389
77. Autocrine PDGFR signalling promotes mammary cancer metastasis. Jechlinger M, Sommer A, Moriggl R, Seither P, Kraut N, Capodiecci P, Donovan M, Cordon-Cardo C, Beug H, Grünert S, J Clin Invest 2006 116 1561 1570
78. Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition. Acevedo VD, Gangula RD, Freeman KW, Li R, Zhang Y, Wang F, Ayala GE, Peterson LE, Ittmann M, Spencer DM, Cancer Cell 2007 12 559 571 (Pubitemid 350199071)
79. Epithelial-mesenchymal transition in ovarian cancer progression: a crucial role for the endothelin axis. Bagnato A, Rosan L, Cells Tissues Organs 2007 185 85 94 (Pubitemid 46956847)
80. The Ubiquitin- Proteasome system in prostate cancer and its transition to castration resistance. Voutsadakis IA, Papandreou CN, Urologic Oncology; seminars and original investigations 2010 [e-pub ahead of print] PMID: 20580272
81. What are the bona fide GSK3 substrates? Sutherland C, Int J Alzheimers Dis 2011 2011 Article ID 505607
82. Axin and GSK3- control Smad3 protein stability and modulate TGF- signaling. Guo X, Ramirez A, Waddell DS, Li Z, Liu X, Wang XF, Genes Dev 2008 22 106 120
83. Integrating patterning signals: Wnt/GSK3 regulates the duration of the BMP/Smad1 signal. Fuentealba LC, Eivers E, Ikeda A, Hurtado C, Kuroda H, Pera EM, De Robertis EM, Cell 2007 131 980 993 (Pubitemid 350138081)
84. Glycogen synthase kinase-3 beta regulates NFkappa B1/p105 stability. Demarchi F, Bertoli C, Sandy P, Schneider C, J Biol Chem 2003 278 39583 39590 (Pubitemid 37258323)
85. Maintenance of constitutive IB kinase activity by Glycogen Synthase Kinase-3/ in pancreatic cancer. Wilson W, Baldwin AS, Cancer Res 2008 68 8156 8163
86. Glycogen Synthase Kinase 3-mediated apoptosis of primary cortical astrocytes involves inhibition of Nuclear Factor B signaling. Sanchez JF, Sniderhan LF, Williamson AL, Fan S, Chakraborty-Sett S, Maggirwar SB, Mol Cell Biol 2003 23 4649 4662 (Pubitemid 36734753)
87. Raf kinase inhibitor protein RKIP enhances signaling by Glycogen Synthase Kinase-3 Al-Mulla F, Bitar MS, Al-Maghrebi M, Behbehani AI, Al-Ali W, Rath O, Doyle B, Tan KY, Pitt A, Kolch W, Cancer Res 2011 71 1334 1343
88. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. Gregory MA, Qi Y, Hann SR, J Biol Chem 2003 278 51606 51612 (Pubitemid 38020405)
89. Multiple Ras-dependent phosphorylation pathways regulate Myc protein stability. Sears R, Nuckolls F, Haura E, Taya Y, Tamai K, Nevins JR, Genes Dev 2000 14 2501 2514
90. Glycogen Synthase Kinase 3 phosphorylates Hypoxia-Inducible Factor 1 and mediates its destabilization in a VHL-independent manner. Flügel D, Görlach A, Michiels C, Kietzmann T, Mol Cell Biol 2007 27 3253 3265 (Pubitemid 46685205)
91. Regulation of Hypoxia-inducible Factor-1 protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/Glycogen Synthase Kinase 3 pathway in HepG2 cells. Mottet D, Dumont V, Deccache Y, Demazy C, Ninane N, Raes M, Michiels C, J Biol Chem 2003 278 31277 31285 (Pubitemid 36994645)
92. Glycogen Synthase Kinase 3-dependent phosphorylation of Mdm2 regulates p53 abundance. Kulikov R, Boehme KA, Blattner C, Mol Cell Biol 2005 25 7170 7180 (Pubitemid 41105913)
93. Cooperative phosphorylation of the tumor suppressor Phosphatase and Tensin Homologue (PTEN) by Casein Kinases and Glycogen Synthase Kinase 3 Al-Khouri AM, Ma Y, Togo SH, Williams S, Mustelin T, J Biol Chem 2005 280 35195 35202 (Pubitemid 41532706)
94. Mutant K-Ras increases GSK-3 gene expression via an ETS-p300 transcriptional complex in pancreatic cancer. Zhang JS, Koenig A, Harrison A, Ugolkov AV, Fernandez-Zapico ME, Couch FJ, Billadeau DD, Oncogene 2011 30 3705 3715
95. Role of Glycogen Synthase Kinase-3 in cell fate and Epithelial- Mesenchymal transitions. Doble BW, Woodgett JR, Cells Tissues Organs 2007 185 73 84 (Pubitemid 46956846)
96. Regulation of protein stability by GSK3 mediated phosphorylation. Xu C, Kim N-G, Gumbiner BM, Cell Cycle 2009 8 4032 4039
97. RINGs of good and evil: RING finger ubiquitin ligases at the crossroads of tumour suppression and oncogenesis. Lipkowitz S, Weissman AM, Nat Rev Cancer 2011 11 629 643
98. H-Ras is degraded by Wnt/-catenin signaling via -TrCP-mediated polyubiquitination. Kim S-E, Yoon J-Y, Jeong W-J, Jeon SH, Park Y, Yoon JB, Park YN, Kim H, Choi KY, J Cell Sci 2009 122 842 848
99. Deregulated proteolysis by the F-box proteins SKP2 and -TrCP: tipping the scales of cancer. Frescas D, Pagano M, Nat Rev Cancer 2008 8 438 449 (Pubitemid 351744963)
100. Ubiquitination and proteolysis of cancer-derived Smad4 mutants by SCFSkp2. Liang M, Liang YY, Wrighton K, Ungermannova D, Wang XP, Brunicardi FC, Liu X, Feng XH, Lin X, Mol Cell Biol 2004 24 7524 7537 (Pubitemid 39121480)
101. Nuclear translocation of Skp2 facilitates its destruction in response to TGF signaling. Hu D, Liu W, Wu G, Wan Y, Cell Cycle 2011 10 285 292
102. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to -secretase inhibitors. ONeal J, Grim J, Strack P, Rao S, Tibbitts D, Winter C, Hardwick J, Welcker M, Meijerink JP, Pieters R, Draetta G, Sears R, Clurman BE, Look AT, J Exp Med 2007 204 1813 1824 (Pubitemid 47236319)
103. Ras activity regulates cyclin E degradation by the Fbw7 pathway. Minella AC, Welcker M, Clurman BE, Proc Natl Acad Sci U S A 2005 102 9649 9654 (Pubitemid 40981735)
104. The cullin7 E3 ligase: a novel player in growth control. Sarikas A, Xu X, Field LJ, Pan Z-Q, Cell Cycle 2008 7 3154 3161
105. The CUL7 E3 ubiquitin ligase targets insulin receptor substrate 1 for ubiquitin-dependent degradation. Xu X, Sarikas A, Dias-Santagata DC, Dolios G, Lafontant PJ, Tsai SC, Zhu W, Nakajima HO, Field LJ, Wang R, Pan ZQ, Mol Cell 2008 30 403 414 (Pubitemid 351672370)
106. Induction of cullin 7 by DNA damage attenuates p53 function. Jung P, Verdoodt B, Bailey A, Yates JR, Menssen A, Hermeking H, Proc Natl Acad Sci U S A 2007 104 11388 11393 (Pubitemid 47175150)
107. The Nedd4-like family of E3 ubiquitin ligases and cancer. Chen C, Matesic LE, Cancer Metastasis Rev 2007 26 587 604 (Pubitemid 350119775)
108. Negative regulation of the E3 ubiquitin ligase itch via Fyn-mediated tyrosine phosphorylation. Yang C, Zhou W, Jeon MS, Demydenco D, Harada Y, Zhou H, Liu YC, Mol Cell 2006 21 135 141 (Pubitemid 43017855)
109. Activation of the E3 ubiquitin ligase Itch through a phosphorylation- induced conformational change. Gallagher E, Gao M, Liu YC, Karin M, Proc Natl Acad Sci U S A 2006 103 1717 1722 (Pubitemid 43228759)
110. Jun turnover is controlled through JNK-dependent phosphorylation of thr E3 ligase Itch. Gao M, Labuda T, Xia Y, Gallagher E, Fang D, Liu YC, Karin M, Science 2004 306 271 275 (Pubitemid 39336871)
111. Grb10 prevents Nedd4-mediated vascular endothelial growth factor receptor-2 degradation. Murdaca J, Treins C, Monthoul-Kartmann MN, Pontier-Bres R, Kumar S, Van Obberghen E, Giorgetti-Peraldi S, J Biol Chem 2004 279 26754 26761 (Pubitemid 38798833)
112. The Grb10/Nedd4 complex regulates ligand-induced ubiquitination and stability of the insulin-like growth factor I receptor. Vecchione A, Marchese A, Henry P, Rotin D, Morrione A, Mol Cell Biol 2003 23 3363 3372 (Pubitemid 36459247)
113. Cell survival through Trk neurotrophin receptors is differentially regulated by ubiquitination. Arevalo JC, Waite J, Rajagopal R, Beyna M, Chen ZY, Lee FS, Chao MV, Neuron 2006 50 549 559
114. WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. Magnifico A, Ettenberg S, Yang C, Mariano J, Tiwari S, Fang S, Lipkowitz S, Weissman AM, J Biol Chem 2003 278 43169 43177 (Pubitemid 37345936)
115. Interaction between two ubiquitin-protein isopeptide ligases of different classes, CBLC and AIP4/ITCH. Courbard JR, Fiore F, Adélaide J, Borg JP, Birnbaum D, Ollendorff V, J Biol Chem 2002 277 45267 45275 (Pubitemid 36159132)
116. Ubiquitination regulates PTEN nuclear import and tumor suppression. Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, Yang H, Pavletich NP, Carver BS, Cordon-Cardo C, Erdjument-Bromage H, Tempst P, Chi SG, Kim HJ, Misteli T, Jiang X, Pandolfi PP, Cell 2007 128 141 156 (Pubitemid 46048885)
117. NEDD4-1 is a proto-oncogenic ubiquitin ligase for PTEN. Wang X, Trotman LC, Koppie T, Alimonti A, Chen Z, Gao Z, Wang J, Erdjument-Bromage H, Tempst P, Cordon-Cardo C, Pandolfi PP, Jiang X, Cell 2007 128 129 139 (Pubitemid 46048884)
118. Oncogenic role of the E3 ubiquitin ligase NEDD4-1, a PTEN negative regulator, in Non-Small-Cell Lung Carcinomas. Amodio N, Scrima M, Palaia L, Palaia L, Salman AN, Quintiero A, Franco R, Botti G, Pirozzi P, Rocco G, De Rosa N, Viglietto G, Am J Pathol 2010 177 2622 2634
119. Regulation of actin cytoskeleton by mDab1 through N-WASP and ubiquitination of mDab1. Suetsugu S, Tezuka T, Morimura T, Hattori M, Mikoshiba K, Yamamoto T, Takenawa T, Biochem J 2004 384 1 8 (Pubitemid 39564155)
120. Wasp and wave family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. Takenawa T, Miki H, J Cell Sci 2001 114 1801 1809 (Pubitemid 32530035)
121. The tumor suppressor p53 regulates polarity of self-renewing divisions in mammary stem cells. Cicalese A, Bonizzi G, Pasi CE, Faretta M, Ronzoni S, Giulini B, Brisken C, Minucci S, Di Fiore PP, Pelicci PG, Cell 2009 138 1083 1095
122. Downregulation of Par-3 expression and disruption of Par complex integrity by TGF-beta during the process of epithelial to mesenchymal transition in rat proximal epithelial cells. Wang X, Nie J, Zhou Q, Liu W, Zhu F, Chen W, Mao H, Luo N, Dong X, Yu X, Biochim Biophys Acta 2008 1782 51 59
123. Transcriptional regulation of cell polarity in EMT and cancer. Moreno-Bueno G, Portillo F, Cano A, Oncogene 2008 27 6958 6969
124. NUMB-ing down cancer by more than just a NOTCH. Pece S, Confalonieri S, Romano PR, Di Fiore PP, Biochim Biophys Acta 2011 1815 26 43
125. NUMB controls p53 tumour suppressor activity. Colaluca IN, Tosoni D, Nuciforo P, Senic-Matuglia F, Galimberti V, Viale G, Pece S, Di Fiore PP, Nature 2008 451 76 80