Overexpression of NSUN2 by DNA hypomethylation is associated with metastatic progression in human breast cancer

Oncotarget

Volumn 8, Issue 13, 2017, Pages 20751-20765

  Yi, Jie ^a   Gao, Ran ^a   Chen, Yu ^a   Yang, Zhuo ^a   Han, Pei ^c   Zhang, Hui ^a   Dou, Yaling ^a   Liu, Wenjing ^a   Wang, Wengong ^c   Du, Guanhua ^b   Xu, Yingchun ^a   Wang, Jinhua ^b  

^a PEKING UNION MEDICAL COLLEGE HOSPITAL   (China)

^b INSTITUTE OF MATERIA MEDICA   (China)

^c PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

Biomarker; Breast cancer; Methylation; NSUN2; Progression

Indexed keywords

ESTROGEN RECEPTOR; KI 67 ANTIGEN; MESSENGER RNA; NSUN2 PROTEIN; PROGESTERONE RECEPTOR; RNA METHYLTRANSFERASE; UNCLASSIFIED DRUG; METHYLTRANSFERASE; NSUN2 PROTEIN, HUMAN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST EPITHELIUM CELL; BREAST TISSUE; CANCER CELL; CANCER CLASSIFICATION; CANCER GROWTH; CANCER STAGING; CANCER TISSUE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; FEMALE; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; MAJOR CLINICAL STUDY; METASTASIS POTENTIAL; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; AGED; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BREAST TUMOR; DISEASE EXACERBATION; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; MIDDLE AGED; NUDE MOUSE; PATHOLOGY; POLYMERASE CHAIN REACTION; TUMOR INVASION; WESTERN BLOTTING; XENOGRAFT;

ADULT; AGED; ANIMALS; BLOTTING, WESTERN; BREAST NEOPLASMS; DISEASE PROGRESSION; DNA METHYLATION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HETEROGRAFTS; HUMANS; IMMUNOHISTOCHEMISTRY; METHYLTRANSFERASES; MICE; MICE, INBRED BALB C; MICE, NUDE; MIDDLE AGED; NEOPLASM INVASIVENESS; POLYMERASE CHAIN REACTION;

EID: 85016402330     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10612     Document Type: Article

References (39)

1. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet-Tieulent J, Jemal A. Global cancer statistics, 2012. CA Cancer J Clin. 2015; 65:87-108.
2. Lichtenstein P, Holm NV, Verkasalo PK, Iliadou A, Kaprio J, Koskenvuo M, Pukkala E, Skytthe A, Hemminki K. Environmental and heritable factors in the causation of cancer analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med. 2000; 343:78-85.
3. McPherson K, Steel CM, Dixon JM. ABC of breast diseases. Breast cancer-epidemiology, risk factors, and genetics. BMJ. 2000; 321:624-628.
4. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. C. W. Elston & I. O. Ellis. Histopathology 1991; 19; 403-410. Histopathology. 2002; 41:151-152, discussion 152-153.
5. Cheang MC, Voduc D, Bajdik C, Leung S, McKinney S, Chia SK, Perou CM, Nielsen TO. Basal-like breast cancer defined by five biomarkers has superior prognostic value than triple-negative phenotype. Clin Cancer Res. 2008; 14:1368-1376.
6. Taby R, Issa JP. Cancer epigenetics. CA Cancer J Clin. 2010; 60:376-392.
7. Herman JG, Baylin SB. Promoter-region hypermethylation and gene silencing in human cancer. Curr Top Microbiol Immunol. 2000; 249:35-54.
8. Ehrlich M. DNA methylation in cancer: too much, but also too little. Oncogene. 2002; 21:5400-5413.
9. Momparler RL. Cancer epigenetics. Oncogene. 2003; 22:6479-6483.
10. Belinsky SA. Gene-promoter hypermethylation as a biomarker in lung cancer. Nat Rev Cancer. 2004; 4:707-717.
11. Marra M, Sordelli IM, Lombardi A, Lamberti M, Tarantino L, Giudice A, Stiuso P, Abbruzzese A, Sperlongano R, Accardo M, Agresti M, Caraglia M, Sperlongano P. Molecular targets and oxidative stress biomarkers in hepatocellular carcinoma: an overview. J Transl Med. 2011; 9:171.
12. Ho E, Beaver LM, Williams DE, Dashwood RH. Dietary factors and epigenetic regulation for prostate cancer prevention. Adv Nutr. 2011; 2:497-510.
13. Rahmatpanah FB, Carstens S, Hooshmand SI, Welsh EC, Sjahputera O, Taylor KH, Bennett LB, Shi H, Davis JW, Arthur GL, Shanafelt TD, Kay NE, Wooldridge JE, Caldwell CW. Large-scale analysis of DNA methylation in chronic lymphocytic leukemia. Epigenomics. 2009; 1:39-61.
14. Frye M, Watt FM. The RNA methyltransferase Misu (NSUN2) mediates Myc-induced proliferation and is upregulated in tumors. Curr Biol. 2006; 16:971-981.
15. Hussain S, Benavente SB, Nascimento E, Dragoni I, Kurowski A, Gillich A, Humphreys P, Frye M. The nucleolar RNA methyltransferase Misu (NSUN2) is required for mitotic spindle stability. J Cell Biol. 2009; 186:27-40.
16. Blanco S, Kurowski A, Nichols J, Watt FM, Benitah SA, Frye M. The RNA-methyltransferase Misu (NSUN2) poises epidermal stem cells to differentiate. PLoS Genet. 2011; 7:e1002403.
17. Hussain S, Tuorto F, Menon S, Blanco S, Cox C, Flores JV, Watt S, Kudo NR, Lyko F, Frye M. The mouse cytosine-5 RNA methyltransferase NSUN2 is a component of the chromatoid body and required for testis differentiation. Mol Cell Biol. 2013; 33:1561-1570.
18. Okamoto M, Hirata S, Sato S, Koga S, Fujii M, Qi G, Ogawa I, Takata T, Shimamoto F, Tatsuka M. Frequent increased gene copy number and high protein expression of tRNA (cytosine-5-)-methyltransferase (NSUN2) in human cancers. DNA Cell Biol. 2012; 31:660-671.
19. Zhang X, Liu Z, Yi J, Tang H, Xing J, Yu M, Tong T, Shang Y, Gorospe M, Wang W. The tRNA methyltransferase NSUN2 stabilizes p16INK(4) mRNA by methylating the 3'-untranslated region of p16. Nat Commun. 2012; 3:712.
20. Yuan S, Tang H, Xing J, Fan X, Cai X, Li Q, Han P, Luo Y, Zhang Z, Jiang B, Dou Y, Gorospe M, Wang W. Methylation by NSUN2 represses the levels and function of microRNA 125b. Mol Cell Biol. 2014; 34:3630-3641.
21. Xing J, Yi J, Cai X, Tang H, Liu Z, Zhang X, Martindale JL, Yang X, Jiang B, Gorospe M, Wang W. NSUN2 Promotes Cell Growth via Elevating Cyclin-Dependent Kinase 1 Translation. Mol Cell Biol. 2015; 35:4043-4052.
22. Akaogi K, Nakajima Y, Ito I, Kawasaki S, Oie SH, Murayama A, Kimura K, Yanagisawa J. KLF4 suppresses estrogen-dependent breast cancer growth by inhibiting the transcriptional activity of ERalpha. Oncogene. 2009; 28:2894-2902.
23. Frye M, Dragoni I, Chin SF, Spiteri I, Kurowski A, Provenzano E, Green A, Ellis IO, Grimmer D, Teschendorff A, Zouboulis CC, Caldas C, Watt FM. Genomic gain of 5p15 leads to over-expression of Misu (NSUN2) in breast cancer. Cancer Lett. 2010; 289:71-80.
24. Ponder BA. Cancer genetics. Nature. 2001; 411:336-341.
25. Bartek J. DNA damage response, genetic instability and cancer: from mechanistic insights to personalized treatment. Mol Oncol. 2011; 5:303-307.
26. Kim TW, Lee SJ, Oh BM, Lee H, Uhm TG, Min JK, Park YJ, Yoon SR, Kim BY, Kim JW, Choe YK, Lee HG. Epigenetic modification of TLR4 promotes activation of NF-κB by regulating methyl-CpG-binding domain protein 2 and Sp1 in gastric cancer. Oncotarget. 2016; 7:4195-209. doi: 10.18632/oncotarget.6549.
27. Evron E, Dooley WC, Umbricht CB, Rosenthal D, Sacchi N, Gabrielson E, Soito AB, Hung DT, Ljung B, Davidson NE, Sukumar S. Detection of breast cancer cells in ductal lavage fluid by methylation-specific PCR. Lancet. 2001; 357:1335-1336.
28. Fackler MJ, Malone K, Zhang Z, Schilling E, Garrett-Mayer E, Swift-Scanlan T, Lange J, Nayar R, Davidson NE, Khan SA, Sukumar S. Quantitative multiplex methylation-specific PCR analysis doubles detection of tumor cells in breast ductal fluid. Clin Cancer Res. 2006; 12:3306-3310.
29. Jackson K, Yu MC, Arakawa K, Fiala E, Youn B, Fiegl H, Muller-Holzner E, Widschwendter M, Ehrlich M. DNA hypomethylation is prevalent even in low-grade breast cancers. Cancer Biol Ther. 2004; 3:1225-1231.
30. Szyf M. DNA demethylation and cancer metastasis: therapeutic implications. Expert Opin Drug Discov. 2008; 3:519-531.
31. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MC, Nielsen TO, Moorman PG, Earp HS, Millikan RC. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006; 295:2492-2502.
32. Rakha EA, El-Sayed ME, Green AR, Paish EC, Powe DG, Gee J, Nicholson RI, Lee AH, Robertson JF, Ellis IO. Biologic and clinical characteristics of breast cancer with single hormone receptor positive phenotype. J Clin Oncol. 2007; 25:4772-4778.
33. Viale G, Regan MM, Mastropasqua MG, Maffini F, Maiorano E, Colleoni M, Price KN, Golouh R, Perin T, Brown RW, Kovács A, Pillay K, Ohlschlegel C, et al. Predictive value of tumor Ki-67 expression in two randomized trials of adjuvant chemoendocrine therapy for node-negative breast cancer. J Natl Cancer Inst. 2008; 100:207-212.
34. Campos M, DE Campos SG, Ribeiro GG, Eguchi FC, Silva SR, DE OCZ, DA CAM, Curcelli EC, Nunes MC, Penna V, Longatto-Filho A. Ki-67 and CD100 immunohistochemical expression is associated with local recurrence and poor prognosis in soft tissue sarcomas, respectively. Oncol Lett. 2013; 5:1527-1535.
35. Tabata K, Tanaka T, Hayashi T, Hori T, Nunomura S, Yonezawa S, Fukuoka J. Ki-67 is a strong prognostic marker of non-small cell lung cancer when tissue heterogeneity is considered. BMC Clin Pathol. 2014; 14:23.
36. Tang H, Fan X, Xing J, Liu Z, Jiang B, Dou Y, Gorospe M, Wang W. NSUN2 delays replicative senescence by repressing p27 (KIP1) translation and elevating CDK1 translation. Aging (Albany NY). 2015; 7:1143-1158. doi: 10.18632/aging.100860.
37. Li LC, Dahiya R. MethPrimer: designing primers for methylation PCRs. Bioinformatics. 2002; 18:1427-1431.
38. Fukuoka J, Fujii T, Shih JH, Dracheva T, Meerzaman D, Player A, Hong K, Settnek S, Gupta A, Buetow K, Hewitt S, Travis WD, Jen J. Chromatin remodeling factors and BRM/BRG1 expression as prognostic indicators in non-small cell lung cancer. Clin Cancer Res. 2004; 10:4314-4324.
39. Song LB, Liao WT, Mai HQ, Zhang HZ, Zhang L, Li MZ, Hou JH, Fu LW, Huang WL, Zeng YX, Zeng MS. The clinical significance of twist expression in nasopharyngeal carcinoma. Cancer Lett. 2006; 242:258-265.