AKT1 inhibits epithelial-to-mesenchymal transition in breast cancer through phosphorylation-dependent twist1 degradation

Cancer Research

Volumn 76, Issue 6, 2016, Pages 1451-1462

  Li, Chia Wei ^a   Xia, Weiya ^a   Lim, Seung Oe ^a   Hsu, Jennifer L ^a,b,c   Huo, Longfei ^a   Wu, Yun ^a   Li, Long Yuan ^b,c   Lai, Chien Chen ^e   Chang, Shih Shin ^a   Hsu, Yi Hsin ^a   Sun, Hui Lung ^a   Kim, Jongchan ^a   Yamaguchi, Hirohito ^a   Lee, Dung Fang ^a   Wang, Hongmei ^a   Wang, Yan ^a   Chou, Chao Kai ^a,b,c   Hsu, Jung Mao ^a   Lai, Yun Ju ^a   LaBaff, Adam M ^a,f   Ding, Qingqing ^a   Ko, How Wen ^a,f   Tsai, Fuu Jen ^d   Tsai, Chang Hai ^c,d   Hortobagyi, Gabriel N ^a   Hung, Mien Chie ^a,b,c,f   more..

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b CHINA MEDICAL UNIVERSITY   (Taiwan)

^c ASIA UNIVERSITY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^e NATIONAL CHUNG HSING UNIVERSITY   (Taiwan)

^f UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; BETA TRANSDUCIN REPEAT CONTAINING PROTEIN; PROTEIN AKT1; PROTEIN KINASE B; RESVERATROL; TRANSCRIPTION FACTOR TWIST; TRANSCRIPTION FACTOR TWIST1; UNCLASSIFIED DRUG; UVOMORULIN; FUSED HETEROCYCLIC RINGS; STILBENE DERIVATIVE; TWIST RELATED PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER SURVIVAL; CONTROLLED STUDY; DRUG EFFICACY; ENZYME INHIBITOR INTERACTION; ENZYME SPECIFICITY; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LUNG METASTASIS; METASTASIS INHIBITION; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SURVIVAL TIME; UBIQUITINATION; ANIMAL; BAGG ALBINO MOUSE; BREAST TUMOR; CELL MOTION; DRUG EFFECTS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; BETA-TRANSDUCIN REPEAT-CONTAINING PROTEINS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; HETEROCYCLIC COMPOUNDS, 3-RING; HUMANS; MICE; MICE, INBRED BALB C; PHOSPHORYLATION; PROTEOLYSIS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; STILBENES; TWIST-RELATED PROTEIN 1;

EID: 84962205007     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-15-1941     Document Type: Article

References (38)

1. Gonzalez E, McGraw TE. The Akt kinases: isoform specificity in metabolism and cancer. Cell Cycle 2009;8:2502-8.
2. Testa JR, Bellacosa A. AKT plays a central role in tumorigenesis. Proc Natl Acad Sci U S A 2001;98:10983-5.
3. Phung TL, Du W, Xue Q, Ayyaswamy S, Gerald D, Antonello Z, et al. Akt1 and akt3 exert opposing roles in the regulation of vascular tumor growth. Cancer Res 2015;75:40-50.
4. Irie HY, Pearline RV, Grueneberg D, Hsia M, Ravichandran P, Kothari N, et al. Distinct roles of Akt1 and Akt2 in regulating cell migration and epithelial-mesenchymal transition. J Cell Biol 2005;171:1023-34.
5. Yoeli-Lerner M, Yiu GK, Rabinovitz I, Erhardt P, Jauliac S, Toker A. Akt blocks breast cancer cell motility and invasion through the transcription factor NFAT. Mol Cell 2005;20:539-50.
6. Iliopoulos D, Polytarchou C, Hatziapostolou M, Kottakis F, Maroulakou IG, Struhl K, et al. MicroRNAs differentially regulated by Akt isoforms control EMT and stem cell renewal in cancer cells. Sci Signal 2009;2:ra62.
7. Hutchinson JN, Jin J, Cardiff RD, Woodgett JR, Muller WJ.Activation of Akt- 1 (PKB-alpha) can accelerate ErbB-2-mediated mammary tumorigenesis but suppresses tumor invasion. Cancer Res 2004;64:3171-8.
8. Thiery JP. Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2002;2:442-54.
9. Huber MA, Kraut N, Beug H. Molecular requirements for epithelial-mesenchymal transition during tumor progression. Curr Opin Cell Biol 2005; 17:548-58.
10. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, et al. Twist, amaster regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004;117:927-39.
11. Lo HW, Hsu SC, XiaW, Cao X, Shih JY, Wei Y, et al. 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. Cancer Res 2007;67:9066-76.
12. Cheng GZ, Zhang WZ, Sun M, Wang Q, Coppola D, Mansour M, et al. Twist is transcriptionally induced by activation of STAT3 and mediates STAT3 oncogenic function. J Biol Chem 2008;283:14665-73.
13. Li CW, Xia W, Huo L, Lim SO, Wu Y, Hsu JL, et al. Epithelial-mesenchyme transition induced by TNF-a requires NF-kB mediated transcriptional upregulation of Twist1. Cancer Res 2012;72:1290-300.
14. Lee DF, Kuo HP, Chen CT, Hsu JM, Chou CK, Wei Y, et al. IKK beta suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 2007;130:440-55.
15. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature 2012;483:603-7.
16. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, et al. A gene-expression signature as a predictor of survival in breast cancer. NEngl J Med 2002;347:1999-2009.
17. Hu Z, Fan C, Oh DS, Marron JS, He X, Qaqish BF, et al. The molecular portraits of breast tumors are conserved across microarray platforms. BMC Genomics 2006;7:96.
18. Parker JS, Mullins M, Cheang MC, Leung S, Voduc D, Vickery T, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol 2009;27:1160-7.
19. Chang CJ, Yang JY, Xia W, Chen CT, Xie X, Chao CH, et al. EZH2 promotes expansion of breast tumor initiating cells through activation of RAF1-betacatenin signaling. Cancer Cell 2010;19:86-100.
20. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, et al. A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 2006;10:515-27.
21. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 1995;378:785-9.
22. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, et al. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 1996;15:6541-51.
23. Vichalkovski A, Gresko E, Hess D, Restuccia DF, Hemmings BA. PKB/AKT phosphorylation of the transcription factor Twist-1 at Ser42 inhibits p53 activity in response to DNA damage. Oncogene 2010;29: 3554-65.
24. Guardavaccaro D, Kudo Y, Boulaire J, Barchi M, Busino L, Donzelli M, et al. Control ofmeiotic andmitotic progression by the F box protein beta-Trcp1 in vivo. Dev Cell 2003;4:799-812.
25. Margottin-Goguet F, Hsu JY, Loktev A, Hsieh HM, Reimann JD, Jackson PK. Prophase destruction of Emi1 by the SCF(betaTrCP/Slimb) ubiquitin ligase activates the anaphase promoting complex to allow progression beyond prometaphase. Dev Cell 2003;4:813-26.
26. Wei S, Lin LF, Yang CC, Wang YC, Chang GD, Chen H, et al. Thiazolidinediones modulate the expression of beta-catenin and other cellcycle regulatory proteins by targeting the F-box proteins of Skp1-Cul1- F-box protein E3 ubiquitin ligase independently of peroxisome proliferator- Activated receptor gamma. Mol Pharmacol 2007;72:725-33.
27. Wei S, Chuang HC, Tsai WC, Yang HC, Ho SR, Paterson AJ, et al. Thiazolidinediones mimic glucose starvation in facilitating Sp1 degradation through the up-regulation of beta-transducin repeat-containing protein. Mol Pharmacol 2009;76:47-57.
28. Xue G, Restuccia DF, Lan Q, Hynx D, Dirnhofer S, Hess D, et al. Akt/PKBmediated phosphorylation of Twist1 promotes tumor metastasis via mediating cross-talk between PI3K/Akt and TGF-beta signaling axes. Cancer Discov 2012;2:248-59.
29. Pal SK, Reckamp K, Yu H, Figlin RA. Akt inhibitors in clinical development for the treatment of cancer. Expert Opin Investig Drugs 2010;19: 1355-66.
30. Yap TA, Yan L, Patnaik A, Fearen I, Olmos D, Papadopoulos K, et al. First-inman clinical trial of the oral pan-AKT inhibitor MK-2206 in patients with advanced solid tumors. J Clin Oncol 2011;29:4688-95.
31. Sangai T, Akcakanat A, Chen H, Tarco E, Wu Y, Do KA, et al. Biomarkers of response to Akt inhibitor MK-2206 in breast cancer. Clin Cancer Res 2012;18:5816-28.
32. Ju X, Katiyar S, Wang C, LiuM, Jiao X, Li S, et al. Akt1 governs breast cancer progression in vivo. Proc Natl Acad Sci U S A 2007;104:7438-43.
33. Maroulakou IG, Oemler W, Naber SP, Tsichlis PN. Akt1 ablation inhibits, whereas Akt2 ablation accelerates, the development of mammary adenocarcinomas in mouse mammary tumor virus (MMTV)-ErbB2/neu and MMTV-polyoma middle T transgenic mice. Cancer Res 2007;67:167-77.
34. Dillon RL, Muller WJ. Distinct biological roles for the akt family in mammary tumor progression. Cancer Res 2010;70:4260-4.
35. Hong KO, Kim JH, Hong JS, Yoon HJ, Lee JI, Hong SP, et al. Inhibition of Akt activity induces the mesenchymal-to-epithelial reverting transition with restoring E-cadherin expression inKB andKOSCC-25B oral squamous cell carcinoma cells. J Exp Clin Cancer Res 2009;28:28.
36. Grille SJ, Bellacosa A, Upson J, Klein-Szanto AJ, van Roy F, Lee-Kwon W, et al. The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 2003;63:2172-8.
37. Julien S, Puig I, Caretti E, Bonaventure J, Nelles L, van Roy F, et al. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 2007;26:7445-56.
38. Zhu QS, Rosenblatt K, Huang KL, Lahat G, Brobey R, Bolshakov S, et al. Vimentin is a novel AKT1 target mediating motility and invasion. Oncogene 2011;30:457-70.