GIAT4RA functions as a tumor suppressor in non-small cell lung cancer by counteracting Uchl3–mediated deubiquitination of LSH

Oncogene

Volumn 38, Issue 46, 2019, Pages 7133-7145

  Yang, Rui ^a,b   Liu, Na ^a,b   Chen, Ling ^a,b   Jiang, Yiqun ^a,b   Shi, Ying ^a,b   Mao, Chao ^a,b   Liu, Yating ^a,b   Wang, Min ^a,b   Lai, Weiwei ^a,b   Tang, Haosheng ^a,b   Gao, Menghui ^a,b   Xiao, Desheng ^b   Wang, Xiang ^b   Zhou, Hu ^c   Tang, Can e ^b   Liu, Wenliang ^b   Yu, Fenglei ^b   Cao, Ya ^a,b   Yan, Qin ^d   Liu, Shuang ^b   Tao, Yongguang ^a,b   more..

^a BEIJING UNIVERSITY OF POSTS AND TELECOMMUNICATIONS   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

^c SHANGHAI INSTITUTE OF MATERIA MEDICA   (China)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; LONG UNTRANSLATED RNA; LONG UNTRANSLATED RNA GIAT4RA; LYMPHOID SPECIFIC HELICASE; PROTEASOME; UNCLASSIFIED DRUG; DNA HELICASE; UBIQUITIN THIOLESTERASE; UCHL3 PROTEIN, HUMAN;

ARTICLE; CANCER STAGING; CANCER TISSUE; CARCINOGENESIS; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; DEUBIQUITINATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION; GENE KNOCKDOWN; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; LUNG CANCER CELL LINE; MAJOR CLINICAL STUDY; MALE; NON SMALL CELL LUNG CANCER; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; RNA DEGRADATION; SIGNAL TRANSDUCTION; TUMOR GROWTH; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; LUNG ADENOCARCINOMA; LUNG TUMOR; METABOLISM; MOUSE; NUDE MOUSE; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE; TUMOR SUPPRESSOR GENE; UBIQUITINATION; XENOGRAFT;

ADENOCARCINOMA OF LUNG; ANIMALS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DNA HELICASES; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, TUMOR SUPPRESSOR; HETEROGRAFTS; HUMANS; LUNG NEOPLASMS; MICE; MICE, NUDE; RNA, LONG NONCODING; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 85070806914     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/s41388-019-0909-0     Document Type: Article

References (51)

1. Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, et al. Cancer statistics in China, 2015. CA Cancer J Clin. 2016;66:115–32.
2. Reck M, Heigener DF, Mok T, Soria JC, Rabe KF. Management of non-small-cell lung cancer: recent developments. Lancet. 2013;382:709–19.
3. Forde PM, Brahmer JR, Kelly RJ. New strategies in lung cancer: epigenetic therapy for non-small cell lung cancer. Clin Cancer Res. 2014;20:2244–8.
4. Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, et al. Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature. 2009;458:223–7.
5. Huarte M. The emerging role of lncRNAs in cancer. Nat Med. 2015;21:1253–61.
6. Brunner AL, Beck AH, Edris B, Sweeney RT, Zhu SX, Li R, et al. Transcriptional profiling of long non-coding RNAs and novel transcribed regions across a diverse panel of archived human cancers. Genome Biol. 2012;13:R75.
7. Feinberg AP, Koldobskiy MA, Gondor A. Epigenetic modulators, modifiers and mediators in cancer aetiology and progression. Nat Rev Genet. 2016;17:284–99.
8. Bhan A, Soleimani M, Mandal SS. Long noncoding RNA and cancer: a new paradigm. Cancer Res. 2017;77:3965–81.
9. Batista PJ, Chang HY. Long noncoding RNAs: cellular address codes in development and disease. Cell. 2013;152:1298–307.
10. Schmitt AM, Chang HY. Long noncoding RNAs in cancer pathways. Cancer Cell. 2016;29:452–63.
11. Zemach A, Kim MY, Hsieh PH, Coleman-Derr D, Eshed-Williams L, Thao K, et al. The Arabidopsis nucleosome remodeler DDM1 allows DNA methyltransferases to access H1-containing heterochromatin. Cell. 2013;153:193–205.
12. Yu W, McIntosh C, Lister R, Zhu I, Han Y, Ren J, et al. Genome-wide DNA methylation patterns in LSH mutant reveals de-repression of repeat elements and redundant epigenetic silencing pathways. Genome Res. 2014;24:1613–23.
13. Tao Y, Xi S, Shan J, Maunakea A, Che A, Briones V, et al. Lsh, chromatin remodeling family member, modulates genome-wide cytosine methylation patterns at nonrepeat sequences. Proc Natl Acad Sci USA. 2011;108:5626–31.
14. Myant K, Termanis A, Sundaram AY, Boe T, Li C, Merusi C, et al. LSH and G9a/GLP complex are required for developmentally programmed DNA methylation. Genome Res. 2011;21:83–94.
15. Fan T, Yan Q, Huang J, Austin S, Cho E, Ferris D, et al. Lsh-deficient murine embryonal fibroblasts show reduced proliferation with signs of abnormal mitosis. Cancer Res. 2003;63:4677–83.
16. Burrage J, Termanis A, Geissner A, Myant K, Gordon K, et al. The SNF2 family ATPase LSH promotes phosphorylation of H2AX and efficient repair of DNA double-strand breaks in mammalian cells. J Cell Sci. 2012;125:5524–34.
17. Jia JSY, Chen L, Lai W, Yan B, Jiang Y, Xiao D, et al. Decrease in lymphoid specific helicase and 5-hydroxymethylcytosine is associated with metastasis and genome instability. Theranostics. 2017;7:3920–32.
18. von Eyss B, Maaskola J, Memczak S, Mollmann K, Schuetz A, Loddenkemper C, et al. The SNF2-like helicase HELLS mediates E2F3-dependent transcription and cellular transformation. EMBO J. 2012;31:972–85.
19. Xiao D, Huang J, Pan Y, Li H, Fu C, Mao C, et al. Chromatin remodeling factor LSH is upregulated by the LRP6-GSK3beta-E2F1 axis linking reversely with survival in gliomas. Theranostics. 2017;7:132–43.
20. Keyes WM, Pecoraro M, Aranda V, Vernersson-Lindahl E, Li W, Vogel H, et al. DeltaNp63alpha is an oncogene that targets chromatin remodeler Lsh to drive skin stem cell proliferation and tumorigenesis. Cell Stem Cell. 2011;8:164–76.
21. He X, Yan B, Liu S, Jia J, Lai W, Xin X, et al. Chromatin remodeling factor LSH drives cancer progression by suppressing the activity of fumarate hydratase. Cancer Res. 2016;76:5743–55.
22. Kong L, Ueno M, Itoh M, Yoshioka K, Takakura N. Identification and characterization of mouse PSF1-binding protein, SLD5. Biochem Biophys Res Commun. 2006;339:1204–7.
23. Kamada K, Kubota Y, Arata T, Shindo Y, Hanaoka F. Structure of the human GINS complex and its assembly and functional interface in replication initiation. Nat Struct Mol Biol. 2007;14:388–96.
24. Labib K, Gambus A. A key role for the GINS complex at DNA replication forks. Trends Cell Biol. 2007;17:271–8.
25. Jiang Y, Mao C, Yang R, Yan B, Shi Y, Liu X, et al. EGLN1/c-Myc induced lymphoid-specific helicase inhibits ferroptosis through lipid metabolic gene expression changes. Theranostics. 2017;7:3293–305.
26. Liu S, Tao YG. Chromatin remodeling factor LSH affects fumarate hydratase as a cancer driver. Chin J Cancer. 2016;35:72.
27. Zhang K, Shi H, Xi H, Wu X, Cui J, Gao Y, et al. Genome-wide lncRNA microarray profiling identifies novel circulating lncRNAs for detection of gastric cancer. Theranostics. 2017;7:213–27.
28. Wang KC, Chang HY. Molecular mechanisms of long noncoding RNAs. Mol Cell. 2011;43:904–14.
29. Rinn JL, Chang HY. Genome regulation by long noncoding RNAs. Annu Rev Biochem. 2012;81:145–66.
30. Leveille N, Melo CA, Rooijers K, Diaz-Lagares A, Melo SA, Korkmaz G, et al. Genome-wide profiling of p53-regulated enhancer RNAs uncovers a subset of enhancers controlled by a lncRNA. Nat Commun. 2015;6:6520.
31. Yoon JH, Abdelmohsen K, Kim J, Yang X, Martindale JL, Tominaga-Yamanaka K, et al. Scaffold function of long non-coding RNA HOTAIR in protein ubiquitination. Nat Commun. 2013;4:2939.
32. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell. 2010;142:409–19.
33. Zhang H, Diab A, Fan H, Mani SK, Hullinger R, Merle P, et al. PLK1 and HOTAIR accelerate proteasomal degradation of SUZ12 and ZNF198 during hepatitis B virus-induced liver carcinogenesis. Cancer Res. 2015;75:2363–74.
34. Taniue K, Kurimoto A, Sugimasa H, Nasu E, Takeda Y, Iwasaki K, et al. Long noncoding RNA UPAT promotes colon tumorigenesis by inhibiting degradation of UHRF1. PNAS. 2016;113:1273–8.
35. Zheng J, Huang X, Tan W, Yu D, Du Z, Chang J, et al. Pancreatic cancer risk variant in LINC00673 creates a miR-1231 binding site and interferes with PTPN11 degradation. Nat Genet. 2016;48:747–57.
36. Zhang P, Cao L, Fan P, Mei Y, Wu M. LncRNA-MIF, a c-Myc-activated long non-coding RNA, suppresses glycolysis by promoting Fbxw7-mediated c-Myc degradation. EMBO Rep. 2016;17:1204–20.
37. Materne P, Vazquez E, Sanchez M, Yague-Sanz C, Anandhakumar J, Migeot V, et al. Histone H2B ubiquitylation represses gametogenesis by opposing RSC-dependent chromatin remodeling at the ste11 master regulator locus. elife. 2016;5:e13500.
38. Zhao D, Lu X, Wang G, Lan Z, Liao W, Li J, et al. Synthetic essentiality of chromatin remodelling factor CHD1 in PTEN-deficient cancer. Nature. 2017;542:484–8.
39. Keren I, Citovsky V. Activation of gene expression by histone deubiquitinase OTLD1. Epigenetics. 2017;12:584–90.
40. Yu W, Briones V, Lister R, McIntosh C, Han Y, Lee EY, et al. CG hypomethylation in Lsh-/- mouse embryonic fibroblasts is associated with de novo H3K4me1 formation and altered cellular plasticity. Proc Natl Acad Sci USA. 2014;111:5890–5.
41. Ren J, Briones V, Barbour S, Yu W, Han Y, Terashima M, et al. The ATP binding site of the chromatin remodeling homolog Lsh is required for nucleosome density and de novo DNA methylation at repeat sequences. Nucleic Acids Res. 2015;43:1444–55.
42. Tao Y, Liu S, Briones V, Geiman TM, Muegge K. Treatment of breast cancer cells with DNA demethylating agents leads to a release of Pol II stalling at genes with DNA-hypermethylated regions upstream of TSS. Nucleic Acids Res. 2011;39:9508–20.
43. Tao Y, Xi S, Briones V, Muegge K. Lsh mediated RNA polymerase II stalling at HoxC6 and HoxC8 involves DNA methylation. PLoS ONE. 2010;5:e9163.
44. Kim JY, Lee JM, Cho JY. Ubiquitin C-terminal hydrolase-L3 regulates Smad1 ubiquitination and osteoblast differentiation. FEBS Lett. 2011;585:1121–6.
45. Liao C, Beveridge R, Hudson JJR, Parker JD, Chiang SC, Ray S, et al. UCHL3 regulates topoisomerase-induced chromosomal break repair by controlling TDP1 proteostasis. Cell Rep. 2018;23:3352–65.
46. Luo K, Li L, Li Y, Wu C, Yin Y, Chen Y, et al. A phosphorylation-deubiquitination cascade regulates the BRCA2-RAD51 axis in homologous recombination. Genes Dev. 2016;30:2581–95.
47. Shi Y, Tao Y, Jiang Y, Xu Y, Yan B, Chen X, et al. Nuclear epidermal growth factor receptor interacts with transcriptional intermediary factor 2 to activate cyclin D1 gene expression triggered by the oncoprotein latent membrane protein 1. Carcinogenesis. 2012;33:1468–78.
48. Jiang Y, Yan B, Lai W, Shi Y, Xiao D, Jia J, et al. Repression of Hox genes by LMP1 in nasopharyngeal carcinoma and modulation of glycolytic pathway genes by HoxC8. Oncogene. 2015;34:6079–91.
49. Mao C, Wang X, Liu Y, Wang M, Yan B, Jiang Y, et al. A G3BP1-interacting lncRNA promotes ferroptosis and apoptosis in cancer via nuclear sequestration tof p53. Cancer Res. 2018;78:3484–96.
50. Yan B, Liu S, Shi Y, Liu N, Chen L, Wang X, et al. Activation of AhR with nuclear IKKalpha regulates cancer stem-like properties in the occurrence of radioresistance. Cell Death Dis. 2018;9:490.
51. Shi Y, Liu N, Lai W, Yan B, Chen L, Liu S, et al. Nuclear EGFR-PKM2 axis induces cancer stem cell-like characteristics in irradiation-resistant cells. Cancer Lett. 2018;422:81–93.