The Arkadia-ESRP2 axis suppresses tumor progression: Analyses in clear-cell renal cell carcinoma

Oncogene

Volumn 35, Issue 27, 2016, Pages 3514-3523

  Mizutani, A ^a,b   Koinuma, D ^a   Seimiya, H ^b   Miyazono, K ^a  

^a UNIVERSITY OF TOKYO   (Japan)

^b CANCER CHEMOTHERAPY CENTER   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARKADIA PROTEIN; COMPLEMENTARY DNA; EPITHELIAL SPLICING REGULATORY PROTEIN 1; EPITHELIAL SPLICING REGULATORY PROTEIN 2; MESSENGER RNA; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ESRP2 PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEIN BINDING; RNA BINDING PROTEIN; RNF111 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ALTERNATIVE RNA SPLICING; ARTICLE; CANCER INHIBITION; CANCER PROGNOSIS; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOSKELETON; EMBRYO; EPITHELIUM CELL; EXON; GENE EXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; KIDNEY CARCINOMA; MCF 7 CELL LINE; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA SEQUENCE; TUMOR GROWTH; UBIQUITINATION; WOUND HEALING; DISEASE COURSE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ONTOLOGY; GENETICS; KAPLAN MEIER METHOD; KIDNEY TUMOR; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; PROCEDURES; PROGNOSIS; RENAL CELL CARCINOMA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE; WESTERN BLOTTING;

ALTERNATIVE SPLICING; BLOTTING, WESTERN; CARCINOMA, RENAL CELL; CELL LINE, TUMOR; CELL PROLIFERATION; DISEASE PROGRESSION; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE ONTOLOGY; HEK293 CELLS; HUMANS; KAPLAN-MEIER ESTIMATE; KIDNEY NEOPLASMS; MCF-7 CELLS; NUCLEAR PROTEINS; PROGNOSIS; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA-BINDING PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84977621648     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2015.412     Document Type: Article

References (46)

1. Gamazon ER, Stranger BE. Genomics of alternative splicing: evolution, development and pathophysiology. Hum Genet 2014; 133: 679-687.
2. Kalsotra A, Cooper TA. Functional consequences of developmentally regulated alternative splicing. Nat Rev Genet 2011; 12: 715-729.
3. Chen J, Weiss WA. Alternative splicing in cancer: implications for biology and therapy. Oncogene 2014; 34: 1-14.
4. Biamonti G, Catillo M, Pignataro D, Montecucco A, Ghigna C. The alternative splicing side of cancer. Semin Cell Dev Biol 2014; 32C: 30-36.
5. Turner N, Grose R. Fibroblast growth factor signalling: from development to cancer. Nat Rev Cancer 2010; 10: 116-129.
6. Shirakihara T, Horiguchi K, Miyazawa K, Ehata S, Shibata T, Morita I et al. TGF-? regulates isoform switching of FGF receptors and epithelial-mesenchymal transition. EMBO J 2011; 30: 783-795.
7. Zhao Q, Caballero OL, Davis ID, Jonasch E, Tamboli P, Yung WK et al. Tumorspecific isoform switch of the fibroblast growth factor receptor 2 underlies the mesenchymal and malignant phenotypes of clear cell renal cell carcinomas. Clin Cancer Res 2013; 19: 2460-2472.
8. Warzecha CC, Sato TK, Nabet B, Hogenesch JB, Carstens RP. ESRP1 and ESRP2 are epithelial cell-type-specific regulators of FGFR2 splicing. Mol Cell 2009; 33: 591-601.
9. Warzecha CC, Carstens RP. Complex changes in alternative pre-mRNA splicing play a central role in the epithelial-to-mesenchymal transition (EMT). Semin Cancer Biol 2012; 22: 417-427.
10. Warzecha CC, Jiang P, Amirikian K, Dittmar KA, Lu H, Shen S et al. An ESRPregulated splicing programme is abrogated during the epithelial-mesenchymal transition. EMBO J 2010; 29: 3286-3300.
11. Ikushima H, Miyazono K. TGFbeta signalling: A complex web in cancer progression. Nat Rev Cancer 2010; 10: 415-424.
12. Horiguchi K, Sakamoto K, Koinuma D, Semba K, Inoue A, Inoue S et al. TGF-? drives epithelial-mesenchymal transition through ?EF1-mediated downregulation of ESRP. Oncogene 2012; 31: 3190-3201.
13. Miyazono K, Koinuma D. Arkadia-beyond the TGF-? pathway. J Biochem 2011; 149: 1-3.
14. Koinuma D, Shinozaki M, Komuro A, Goto K, Saitoh M, Hanyu A et al. Arkadia amplifies TGF-beta superfamily signalling through degradation of Smad7. EMBO J 2003; 22: 6458-6470.
15. Nagano Y, Mavrakis KJ, Lee KL, Fujii T, Koinuma D, Sase H et al. Arkadia induces degradation of SnoN and c-Ski to enhance transforming growth factor-beta signaling. J Biol Chem 2007; 282: 20492-20501.
16. Briones-Orta MA, Levy L, Madsen CD, Das D, Erker Y, Sahai E et al. Arkadia regulates tumor metastasis by modulation of the TGF-? pathway. Cancer Res 2013; 73: 1800-1810.
17. Sharma V, Antonacopoulou AG, Tanaka S, Panoutsopoulos AA, Bravou V, Kalofonos HP et al. Enhancement of TGF-? signaling responses by the E3 ubiquitin ligase Arkadia provides tumor suppression in colorectal cancer. Cancer Res 2011; 71: 6438-6449.
18. Bierie B, Moses HL. Tumour microenvironment: TGFbeta: The molecular Jekyll and Hyde of cancer. Nat Rev Cancer 2006; 6: 506-520.
19. Mizutani A, Saitoh M, Imamura T, Miyazawa K, Miyazono K. Arkadia complexes with clathrin adaptor AP2 and regulates EGF signalling. J Biochem 2010; 148: 733-741.
20. Poulsen SL, Hansen RK, Wagner SA, van Cuijk L, van Belle GJ, Streicher W et al. RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J Cell Biol 2013; 201: 797-807.
21. Erker Y, Neyret-Kahn H, Seeler JS, Dejean A, Atfi A, Levy L. Arkadia, a novel SUMOtargeted ubiquitin ligase involved in PML degradation. Mol Cell Biol 2013; 33: 2163-2177.
22. Ishii H, Saitoh M, Sakamoto K, Kondo T, Katoh R, Tanaka S et al. Epithelial Splicing Regulatory Protein 1 (ESRP1) and 2 (ESRP2) suppress cancer cell motility via different mechanisms. J Biol Chem 2014; 289: 27386-27399.
23. Le Scolan E, Zhu Q, Wang L, Bandyopadhyay A, Javelaud D, Mauviel A et al. Transforming growth factor-beta suppresses the ability of Ski to inhibit tumor metastasis by inducing its degradation. Cancer Res 2008; 68: 3277-3285.
24. Levy L, Howell M, Das D, Harkin S, Episkopou V, Hill CS. Arkadia activates Smad3/ Smad4-dependent transcription by triggering signal-induced SnoN degradation. Mol Cell Biol 2007; 27: 6068-6083.
25. Yuzawa H, Koinuma D, Maeda S, Yamamoto K, Miyazawa K, Imamura T. Arkadia represses the expression of myoblast differentiation markers through degradation of Ski and the Ski-bound Smad complex in C2C12 myoblasts. Bone 2009; 44: 53-60.
26. Kulathu Y, Komander D. Atypical ubiquitylation-the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat Rev Mol Cell Biol 2012; 13: 508-523.
27. Shapiro IM, Cheng AW, Flytzanis NC, Balsamo M, Condeelis JS, Oktay MH et al. An EMT-driven alternative splicing program occurs in human breast cancer and modulates cellular phenotype. PLoS Genet 2011; 7: e1002218.
28. Ueda J, Matsuda Y, Yamahatsu K, Uchida E, Naito Z, Korc M et al. Epithelial splicing regulatory protein 1 is a favorable prognostic factor in pancreatic cancer that attenuates pancreatic metastases. Oncogene 2013; 33: 4485-4495.
29. Yae T, Tsuchihashi K, Ishimoto T, Motohara T, Yoshikawa M, Yoshida GJ et al. Alternative splicing of CD44 mRNA by ESRP1 enhances lung colonization of metastatic cancer cell. Nat Commun 2012; 3: 883.
30. Rini BI, Campbell SC, Escudier B. Renal cell carcinoma. Lancet 2009; 373: 1119-1132.
31. Di Modugno F, DeMonte L, Balsamo M, Bronzi G, Nicotra MR, Alessio M et al. Molecular cloning of hMena (ENAH) and its splice variant hMena+11a: epidermal growth factor increases their expression and stimulates hMena+11a phosphorylation in breast cancer cell lines. Cancer Res 2007; 67: 2657-2665.
32. Barzik M, Kotova TI, Higgs HN, Hazelwood L, Hanein D, Gertler FB et al. Ena/VASP proteins enhance actin polymerization in the presence of barbed end capping proteins. J Biol Chem 2005; 280: 28653-28662.
33. Cybulsky AV, Takano T, Guillemette J, Papillon J, Volpini RA, Di Battista JA. The Ste20-like kinase SLK promotes p53 transactivation and apoptosis. Am J Physiol Renal Physiol 2009; 297: F971-F980.
34. Peng DJ, Zeng M, Muromoto R, Matsuda T, Shimoda K, Subramaniam M et al. Noncanonical K27-linked polyubiquitination of TIEG1 regulates Foxp3 expression and tumor growth. J Immunol 2011; 186: 5638-5647.
35. Geisler S, Holmström KM, Skujat D, Fiesel FC, Rothfuss OC, Kahle PJ et al. PINK1/ Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12: 119-131.
36. Horvath A, Pakala SB, Mudvari P, Reddy SD, Ohshiro K, Casimiro S et al. Novel insights into breast cancer genetic variance through RNA sequencing. Sci Rep 2013; 3: 2256.
37. Hsu RJ, Ho JY, Cha TL, Yu DS, Wu CL, Huang WP et al. WNT10A plays an oncogenic role in renal cell carcinoma by activating WNT/?-catenin pathway. PLoS One 2012; 7: e47649.
38. Wild JR, Staton CA, Chapple K, Corfe BM. Neuropilins: expression and roles in the epithelium. Int J Exp Pathol 2012; 93: 81-103.
39. Harris IS, Treloar AE, Inoue S, Sasaki M, Gorrini C, Lee KC et al. Glutathione and thioredoxin antioxidant pathways synergize to drive cancer initiation and progression. Cancer Cell 2015; 27: 211-222.
40. Zhou ZN, Sharma VP, Beaty BT, Roh-Johnson M, Peterson EA, Van Rooijen N et al. Autocrine HBEGF expression promotes breast cancer intravasation, metastasis and macrophage-independent invasion in vivo. Oncogene 2014; 33: 3784-3793.
41. Ray KC, Moss ME, Franklin JL, Weaver CJ, Higginbotham J, Song Y et al. Heparin-binding epidermal growth factor-like growth factor eliminates constraints on activated Kras to promote rapid onset of pancreatic neoplasia. Oncogene 2014; 33: 823-831.
42. Park JH, Smith RJ, Shieh SY, Roeder RG. The GAS41-PP2Cbeta complex dephosphorylates p53 at serine 366 and regulates its stability. J Biol Chem 2011; 286: 10911-10917.
43. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA et al. The cBio cancer genomics portal: An open platform for exploring multidimensional cancer genomics data. Cancer Discov 2012; 2: 401-404.
44. Mizutani A, Koinuma D, Tsutsumi S, Kamimura N, Morikawa M, Suzuki HI et al. Cell type-specific target selection by combinatorial binding of Smad2/3 proteins and hepatocyte nuclear factor 4alpha in HepG2 cells. J Biol Chem 2011; 286: 29848-29860.
45. Isogaya K, Koinuma D, Tsutsumi S, Saito RA, Miyazawa K, Aburatani H et al. A Smad3 and TTF-1/NKX2-1 complex regulates Smad4-independent gene expression. Cell Res 2014; 24: 994-1008.
46. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 2013; 14: R36.