Decrease in lymphoid specific helicase and 5-hydroxymethylcytosine is associated with metastasis and genome instability

Theranostics

Volumn 7, Issue 16, 2017, Pages 3920-3932

  Jia, Jiantao ^a,b,c   Shi, Ying ^a,c   Chen, Ling ^a,c   Lai, Weiwei ^a,c   Yan, Bin ^a,c   Jiang, Yiqun ^a,c   Xiao, Desheng ^a   Xi, Sichuan ^d   Cao, Ya ^a,c   Liu, Shuang ^a   Cheng, Yan ^c   Tao, Yongguang ^a,b,c  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CHANGZHI MEDICAL COLLEGE   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

5 hmC; Genome instability; LSH; Satellites; TET2

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; CELL PROTEIN; CISPLATIN; HELICASE; LYMPHOID SPECIFIC HELICASE; MICRORNA; MICRORNA 26B; MICRORNA 29C; TET2 PROTEIN; TET3 PROTEIN; UNCLASSIFIED DRUG; 5 METHYLCYTOSINE; 5-HYDROXYMETHYLCYTOSINE; DIOXYGENASE; DNA BINDING PROTEIN; DNA HELICASE; HELLS PROTEIN, HUMAN; ONCOPROTEIN; PROTEIN BINDING; TET2 PROTEIN, HUMAN; TET3 PROTEIN, HUMAN;

ARTICLE; BREAST CANCER; COLON CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA DAMAGE; GENE SILENCING; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; HUMAN TISSUE; METASTASIS; NASOPHARYNX CARCINOMA; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; TISSUE LEVEL; ANALOGS AND DERIVATIVES; ANIMAL; DRUG EFFECT; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENETICS; HETEROCHROMATIN; METABOLISM; NUDE MOUSE; TUMOR CELL LINE;

5-METHYLCYTOSINE; ANIMALS; CELL LINE, TUMOR; CISPLATIN; DIOXYGENASES; DNA HELICASES; DNA-BINDING PROTEINS; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; HETEROCHROMATIN; HUMANS; MICE, NUDE; MICRORNAS; NEOPLASM METASTASIS; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS;

EID: 85030655643     PISSN: None     EISSN: 18387640     Source Type: Journal    
DOI: 10.7150/thno.21389     Document Type: Article

References (63)

1. Wilson AS, Power BE, Molloy PL. DNA hypomethylation and human diseases. Biochim Biophys Acta. 2007; 1775: 138-62.
2. Esteller M. Epigenetics in cancer. N Engl J Med. 2008; 358: 1148-59.
3. Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, Nederlof PM, et al. BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature. 2011; 477: 179-84.
4. Hennig W. Heterochromatin. Chromosoma. 1999; 108: 1-9.
5. Cann KL, Dellaire G. Heterochromatin and the DNA damage response: the need to relax. Biochem Cell Biol. 2011; 89: 45-60.
6. Falk M, Lukasova E, Kozubek S. Chromatin structure influences the sensitivity of DNA to gamma-radiation. Biochim Biophys Acta. 2008; 1783: 2398-414.
7. Jiang Y, Liu S, Chen X, Cao Y, Tao Y. Genome-wide distribution of DNA methylation and DNA demethylation and related chromatin regulators in cancer. Biochimica et biophysica acta. 2013; 1835: 155-63.
8. Liu S, Tao Y. Interplay between chromatin modifications and paused RNA polymerase II in dynamic transition between stalled and activated genes. Biological reviews of the Cambridge Philosophical Society. 2013; 88: 40-8.
9. 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.
10. Delatte B, Deplus R, Fuks F. Playing TETris with DNA modifications. EMBO J. 2014; 33: 1198-211.
11. Shen L, Zhang Y. 5-Hydroxymethylcytosine: generation, fate, and genomic distribution. Curr Opin Cell Biol. 2013; 25: 289-96.
12. Solary E, Bernard OA, Tefferi A, Fuks F, Vainchenker W. The Ten-Eleven Translocation-2 (TET2) gene in hematopoiesis and hematopoietic diseases. Leukemia. 2014; 28: 485-96.
13. Ficz G, Gribben JG. Loss of 5-hydroxymethylcytosine in cancer: cause or consequence? Genomics. 2014; 104: 352-7.
14. 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.
15. 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.
16. 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 U S A. 2011; 108: 5626-31.
17. 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.
18. 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.
19. Burrage J, Termanis A, Geissner A, Myant K, Gordon K, Stancheva I. 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.
20. 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.
21. Liu S, Tao YG. Chromatin remodeling factor LSH affects fumarate hydratase as a cancer driver. Chin J Cancer. 2016; 35: 72.
22. 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.
23. 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.
24. 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 research. 2016; 76: 5743-55.
25. Jiang Y MC, Yang R, Yan B, Shi Y, Liu X, Lai W, Liu Y, Wang X, Xiao D, Zhou H, Cheng Y, Yu F, Cao Y, Liu S, Yan Q, Tao Y. EGLN1/c-Myc Induced Lymphoid-Specific Helicase Inhibits Ferroptosis through Lipid Metabolic Gene Expression Changes. Theranostics. 2017; 7: 3293-305.
26. Koh KP, Yabuuchi A, Rao S, Huang Y, Cunniff K, Nardone J, et al. Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell. 2011; 8: 200-13.
27. Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, Jansen PW, Bauer C, et al. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell. 2013; 152: 1146-59.
28. Suva ML, Riggi N, Bernstein BE. Epigenetic reprogramming in cancer. Science. 2013; 339: 1567-70.
29. Chen T, Dent SY. Chromatin modifiers and remodellers: regulators of cellular differentiation. Nat Rev Genet. 2014; 15: 93-106.
30. 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.
31. 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.
32. Xu Y, Shi Y, Yuan Q, Liu X, Yan B, Chen L, et al. Epstein-Barr Virus encoded LMP1 regulates cyclin D1 promoter activity by nuclear EGFR and STAT3 in CNE1 cells. Journal of experimental & clinical cancer research: CR. 2013; 32: 90.
33. Yang H, Liu Y, Bai F, Zhang JY, Ma SH, Liu J, et al. Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene. 2013; 32: 663-9.
34. Poh WJ, Wee CP, Gao Z. DNA Methyltransferase Activity Assays: Advances and Challenges. Theranostics. 2016; 6: 369-91.
35. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009; 324: 930-5.
36. Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Masse A, et al. Mutation in TET2 in myeloid cancers. N Engl J Med. 2009; 360: 2289-301.
37. Langemeijer SM, Kuiper RP, Berends M, Knops R, Aslanyan MG, Massop M, et al. Acquired mutations in TET2 are common in myelodysplastic syndromes. Nat Genet. 2009; 41: 838-42.
38. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature. 2010; 468: 839-43.
39. Quivoron C, Couronne L, Della Valle V, Lopez CK, Plo I, Wagner-Ballon O, et al. TET2 Inactivation Results in Pleiotropic Hematopoietic Abnormalities in Mouse and Is a Recurrent Event during Human Lymphomagenesis. Cancer Cell. 2011; 20: 25-38.
40. Lian CG, Xu Y, Ceol C, Wu F, Larson A, Dresser K, et al. Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell. 2012; 150: 1135-46.
41. Moran-Crusio K, Reavie L, Shih A, Abdel-Wahab O, Ndiaye-Lobry D, Lobry C, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer cell. 2011; 20: 11-24.
42. Bertoli G, Cava C, Castiglioni I. MicroRNAs: New Biomarkers for Diagnosis, Prognosis, Therapy Prediction and Therapeutic Tools for Breast Cancer. Theranostics. 2015; 5: 1122-43.
43. James AM, Baker MB, Bao G, Searles CD. MicroRNA Detection Using a Double Molecular Beacon Approach: Distinguishing Between miRNA and Pre-miRNA. Theranostics. 2017; 7: 634-46.
44. Wang J, Ye H, Zhang D, Cheng K, Hu Y, Yu X, et al. Cancer-derived Circulating MicroRNAs Promote Tumor Angiogenesis by Entering Dendritic Cells to Degrade Highly Complementary MicroRNAs. Theranostics. 2017; 7: 1407-21.
45. Tu J, Ng SH, Luk AC, Liao J, Jiang X, Feng B, et al. MicroRNA-29b/Tet1 regulatory axis epigenetically modulates mesendoderm differentiation in mouse embryonic stem cells. Nucleic Acids Res. 2015; 43: 7805-22.
46. Song SJ, Ito K, Ala U, Kats L, Webster K, Sun SM, et al. The oncogenic microRNA miR-22 targets the TET2 tumor suppressor to promote hematopoietic stem cell self-renewal and transformation. Cell Stem Cell. 2013; 13: 87-101.
47. Fu X, Jin L, Wang X, Luo A, Hu J, Zheng X, et al. MicroRNA-26a targets ten eleven translocation enzymes and is regulated during pancreatic cell differentiation. Proc Natl Acad Sci U S A. 2013; 110: 17892-7.
48. Haffner MC, Chaux A, Meeker AK, Esopi DM, Gerber J, Pellakuru LG, et al. Global 5-hydroxymethylcytosine content is significantly reduced in tissue stem/progenitor cell compartments and in human cancers. Oncotarget. 2011; 2: 627-37.
49. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer cell. 2011; 19: 17-30.
50. Kraus TF, Globisch D, Wagner M, Eigenbrod S, Widmann D, Munzel M, et al. Low values of 5-hydroxymethylcytosine (5hmC), the "sixth base," are associated with anaplasia in human brain tumors. Int J Cancer. 2012; 131: 1577-90.
51. Zhang Y, Wu K, Shao Y, Sui F, Yang Q, Shi B, et al. Decreased 5-Hydroxymethylcytosine (5-hmC) predicts poor prognosis in early-stage laryngeal squamous cell carcinoma. Am J Cancer Res. 2016; 6: 1089-98.
52. Gao F, Xia Y, Wang J, Lin Z, Ou Y, Liu X, et al. Integrated analyses of DNA methylation and hydroxymethylation reveal tumor suppressive roles of ECM1, ATF5, and EOMES in human hepatocellular carcinoma. Genome Biol. 2014; 15: 533.
53. Larson AR, Dresser KA, Zhan Q, Lezcano C, Woda BA, Yosufi B, et al. Loss of 5-hydroxymethylcytosine correlates with increasing morphologic dysplasia in melanocytic tumors. Mod Pathol. 2014; 27: 936-44.
54. Ryu B, Kim DS, Deluca AM, Alani RM. Comprehensive expression profiling of tumor cell lines identifies molecular signatures of melanoma progression. PLoS One. 2007; 2: e594.
55. Waseem A, Ali M, Odell EW, Fortune F, Teh MT. Downstream targets of FOXM1: CEP55 and HELLS are cancer progression markers of head and neck squamous cell carcinoma. Oral Oncol. 2010; 46: 536-42.
56. 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. Proceedings of the National Academy of Sciences of the United States of America. 2014; 111: 5890-5.
57. 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.
58. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer cell. 2010; 18: 553-67.
59. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, et al. Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer cell. 2010; 17: 510-22.
60. Huang J, Fan T, Yan Q, Zhu H, Fox S, Issaq HJ, et al. Lsh, an epigenetic guardian of repetitive elements. Nucleic Acids Res. 2004; 32: 5019-28.
61. Yan Q, Cho E, Lockett S, Muegge K. Association of Lsh, a regulator of DNA methylation, with pericentromeric heterochromatin is dependent on intact heterochromatin. Mol Cell Biol. 2003; 23: 8416-28.
62. Murata A, Baba Y, Ishimoto T, Miyake K, Kosumi K, Harada K, et al. TET family proteins and 5-hydroxymethylcytosine in esophageal squamous cell carcinoma. Oncotarget. 2015; 6: 23372-82.
63. Lai W, Li H, Liu S, Tao Y. Connecting chromatin modifying factors to DNA damage response. International journal of molecular sciences. 2013; 14: 2355-69.