Ring Finger Protein 14 is a New Regulator of TCF/β-catenin-mediated Transcription and Colon Cancer Cell Survival

Overview

Journal EMBO Rep

Specialty Molecular Biology

Date 2013 Mar 2

PMID 23449499

Citations 17

Authors

Beibei Wu

Sarah Piloto

Weihua Zeng

Nate P Hoverter

Thomas F Schilling

Marian L Waterman

Affiliations

Soon will be listed here.

Abstract

T-cell factor/lymphoid enhancer factor (TCF/LEF) proteins regulate transcription by recruiting β-catenin and its associated co-regulators. Whether TCF/LEFs also recruit more factors through independent, direct interactions is not well understood. Here we discover Ring Finger Protein 14 (RNF14) as a new binding partner for all TCF/LEF transcription factors. We show that RNF14 positively regulates Wnt signalling in human cancer cells and in an in vivo zebrafish model by binding to target promoters with TCF and stabilizing β-catenin recruitment. RNF14 depletion experiments demonstrate that it is crucial for colon cancer cell survival. Therefore, we have identified a key interacting factor of TCF/β-catenin complexes to regulate Wnt gene transcription.

Citing Articles

The cross talk of ubiquitination and chemotherapy tolerance in colorectal cancer.

Rong Z, Zheng K, Chen J, Jin X J Cancer Res Clin Oncol. 2024; 150(3):154.

PMID: 38521878 PMC: 10960765. DOI: 10.1007/s00432-024-05659-9.

The involvement of E3 ubiquitin ligases in the development and progression of colorectal cancer.

Chen J, Feng H, Wang Y, Bai X, Sheng S, Li H Cell Death Discov. 2023; 9(1):458.

PMID: 38104139 PMC: 10725464. DOI: 10.1038/s41420-023-01760-z.

Long non-coding RNA SNHG4 enhances RNF14 mRNA stability to promote the progression of colorectal cancer by recruiting TAF15 protein.

Lv L, Huang B, Yi L, Zhang L Apoptosis. 2022; 28(3-4):414-431.

PMID: 36482019 DOI: 10.1007/s10495-022-01781-6.

Counteractive and cooperative actions of muscle β-catenin and Ca1.1 during early neuromuscular synapse formation.

Kaplan M, Flucher B iScience. 2022; 25(4):104025.

PMID: 35340430 PMC: 8941212. DOI: 10.1016/j.isci.2022.104025.

Detection of genomic structure variants associated with wrinkled skin in Xiang pig by next generation sequencing.

Xiaoli L, Fengbin H, Shihui H, Xi N, Sheng L, Zhou W Aging (Albany NY). 2021; 13(22):24710-24739.

PMID: 34837693 PMC: 8660620. DOI: 10.18632/aging.203711.

References

Dorsky R, Sheldahl L, Moon R . A transgenic Lef1/beta-catenin-dependent reporter is expressed in spatially restricted domains throughout zebrafish development. Dev Biol. 2002; 241(2):229-37. DOI: 10.1006/dbio.2001.0515. View

Ito K, Adachi S, Iwakami R, Yasuda H, Muto Y, Seki N . N-Terminally extended human ubiquitin-conjugating enzymes (E2s) mediate the ubiquitination of RING-finger proteins, ARA54 and RNF8. Eur J Biochem. 2001; 268(9):2725-32. DOI: 10.1046/j.1432-1327.2001.02169.x. View

Hovanes K, Li T, Munguia J, Truong T, Milovanovic T, Marsh J . Beta-catenin-sensitive isoforms of lymphoid enhancer factor-1 are selectively expressed in colon cancer. Nat Genet. 2001; 28(1):53-7. DOI: 10.1038/ng0501-53. View

Love J, Li X, Case D, Giese K, Grosschedl R, Wright P . Structural basis for DNA bending by the architectural transcription factor LEF-1. Nature. 1995; 376(6543):791-5. DOI: 10.1038/376791a0. View

Kang H, Yeh S, Fujimoto N, Chang C . Cloning and characterization of human prostate coactivator ARA54, a novel protein that associates with the androgen receptor. J Biol Chem. 1999; 274(13):8570-6. DOI: 10.1074/jbc.274.13.8570. View

Kikuchi H, Uchida C, Hattori T, Isobe T, Hiramatsu Y, Kitagawa K . ARA54 is involved in transcriptional regulation of the cyclin D1 gene in human cancer cells. Carcinogenesis. 2007; 28(8):1752-8. DOI: 10.1093/carcin/bgm120. View

Miyamoto H, Rahman M, Takatera H, Kang H, Yeh S, Chang H . A dominant-negative mutant of androgen receptor coregulator ARA54 inhibits androgen receptor-mediated prostate cancer growth. J Biol Chem. 2001; 277(7):4609-17. DOI: 10.1074/jbc.M108312200. View

Hanson A, Wallace H, Freeman T, Beauchamp R, Lee L, Lee E . XIAP monoubiquitylates Groucho/TLE to promote canonical Wnt signaling. Mol Cell. 2012; 45(5):619-28. PMC: 3299836. DOI: 10.1016/j.molcel.2011.12.032. View

Tran H, Hamada F, Schwarz-Romond T, Bienz M . Trabid, a new positive regulator of Wnt-induced transcription with preference for binding and cleaving K63-linked ubiquitin chains. Genes Dev. 2008; 22(4):528-42. PMC: 2238673. DOI: 10.1101/gad.463208. View

10.

Skehan P, Storeng R, Scudiero D, Monks A, McMahon J, Vistica D . New colorimetric cytotoxicity assay for anticancer-drug screening. J Natl Cancer Inst. 1990; 82(13):1107-12. DOI: 10.1093/jnci/82.13.1107. View

11.

Zeng W, de Greef J, Chen Y, Chien R, Kong X, Gregson H . Specific loss of histone H3 lysine 9 trimethylation and HP1gamma/cohesin binding at D4Z4 repeats is associated with facioscapulohumeral dystrophy (FSHD). PLoS Genet. 2009; 5(7):e1000559. PMC: 2700282. DOI: 10.1371/journal.pgen.1000559. View

12.

Spaulding C, Reschly E, Zagort D, Yashiro-Ohtani Y, Beverly L, Capobianco A . Notch1 co-opts lymphoid enhancer factor 1 for survival of murine T-cell lymphomas. Blood. 2007; 110(7):2650-8. DOI: 10.1182/blood-2007-04-084202. View

13.

Cadigan K, Waterman M . TCF/LEFs and Wnt signaling in the nucleus. Cold Spring Harb Perspect Biol. 2012; 4(11). PMC: 3536346. DOI: 10.1101/cshperspect.a007906. View

14.

Sansom O, Reed K, van de Wetering M, Muncan V, Winton D, Clevers H . Cyclin D1 is not an immediate target of beta-catenin following Apc loss in the intestine. J Biol Chem. 2005; 280(31):28463-7. DOI: 10.1074/jbc.M500191200. View

15.

Mosimann C, Hausmann G, Basler K . Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol. 2009; 10(4):276-86. DOI: 10.1038/nrm2654. View

16.

Mohan M, Herz H, Takahashi Y, Lin C, Lai K, Zhang Y . Linking H3K79 trimethylation to Wnt signaling through a novel Dot1-containing complex (DotCom). Genes Dev. 2010; 24(6):574-89. PMC: 2841335. DOI: 10.1101/gad.1898410. View

17.

Thisse C, Thisse B, Schilling T, Postlethwait J . Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos. Development. 1993; 119(4):1203-15. DOI: 10.1242/dev.119.4.1203. View

18.

Sierra J, Yoshida T, Joazeiro C, Jones K . The APC tumor suppressor counteracts beta-catenin activation and H3K4 methylation at Wnt target genes. Genes Dev. 2006; 20(5):586-600. PMC: 1410807. DOI: 10.1101/gad.1385806. View

19.

Arce L, Pate K, Waterman M . Groucho binds two conserved regions of LEF-1 for HDAC-dependent repression. BMC Cancer. 2009; 9:159. PMC: 2701438. DOI: 10.1186/1471-2407-9-159. View

20.

Bienz M, Clevers H . Linking colorectal cancer to Wnt signaling. Cell. 2000; 103(2):311-20. DOI: 10.1016/s0092-8674(00)00122-7. View