tRNA Modifying Enzymes, NSUN2 and METTL1, Determine Sensitivity to 5-Fluorouracil in HeLa Cells

PLoS Genetics

Volumn 10, Issue 9, 2014, Pages

  Okamoto, Mayumi ^a   Fujiwara, Mamoru ^a   Hori, Masato ^a   Okada, Kaoru ^a   Yazama, Futoshi ^a   Konishi, Hiroaki ^a   Xiao, Yegui ^a   Qi, Guangying ^a   Shimamoto, Fumio ^a   Ota, Takahide ^b   Temme, Achim ^c   Tatsuka, Masaaki ^a  

^a PREFECTURAL UNIVERSITY OF HIROSHIMA   (Japan)

^b KANAZAWA MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; FLUOROURACIL; METHYLTRANSFERASE LIKE 1; NOP2 SUN DOMAIN FAMILY MEMBER 2; PROTEIN KINASE B; TRANSFER RNA; TRANSFER RNA METHYLTRANSFERASE; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIMETABOLITE; CISPLATIN; METHYLTRANSFERASE; METTL1 PROTEIN, HUMAN; NSUN2 PROTEIN, HUMAN; PACLITAXEL;

ARTICLE; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; DRUG SENSITIVITY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FEMALE; HEAT STRESS; HELA CELL LINE; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RNA DEGRADATION; RNA METHYLATION; CELL PROLIFERATION; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; GENE EXPRESSION; GENE SILENCING; GENETICS; HEAT SHOCK RESPONSE; METABOLISM; PHOSPHORYLATION; RNA STABILITY;

ANTIMETABOLITES, ANTINEOPLASTIC; CELL PROLIFERATION; CISPLATIN; DRUG RESISTANCE, NEOPLASM; FLUOROURACIL; GENE EXPRESSION; GENE KNOCKDOWN TECHNIQUES; HEAT-SHOCK RESPONSE; HELA CELLS; HUMANS; METHYLTRANSFERASES; PACLITAXEL; PHOSPHORYLATION; RNA STABILITY; RNA, TRANSFER; TUMOR STEM CELL ASSAY;

EID: 84907572307     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1004639     Document Type: Article

References (52)

1. Longley DB, Harkin DP, Johnston PG, (2003) 5-fluorouracil: mechanisms of action and clinical strategies. Nat Rev Cancer 3: 330–338.
2. Benz C, Tillis T, Tattelman E, Cadman E, (1982) Optimal schedule of methotrexate and 5-fluorouracil in human breast cancer. Cancer Res 42: 2081–2086.
3. Bertino JR, Mini E, Fernandes DJ, (1983) Sequential methotrexate and 5-fluorouracil: mechanisms of synergy. Semin Oncol 10: 2–5.
4. Bonnefoi H, Smith IE, O'Brien ME, Seymour MT, Powles TJ, et al. (1996) Phase II study of continuous infusional 5-fluorouracil with epirubicin and carboplatin (instead of cisplatin) in patients with metastatic/locally advanced breast cancer (infusional ECarboF): a very active and well-tolerated outpatient regimen. Br J Cancer 73: 391–396.
5. Greco FA, Figlin R, York M, Einhorn L, Schilsky R, et al. (1996) Phase III randomized study to compare interferon alfa-2a in combination with fluorouracil versus fluorouracil alone in patients with advanced colorectal cancer. J Clin Oncol 14: 2674–2681.
6. Jones DV, JrWinn RJ, Brown BW, Levy LB, Pugh RP, et al. (1995) Randomized phase III study of 5-fluorouracil plus high dose folinic acid versus 5-fluorouracil plus folinic acid plus methyl-lomustine for patients with advanced colorectal cancer. Cancer 76: 1709–1714.
7. Marsoni S, (1995) Fluorouracil and folinic acid in colon cancer. IMPACT Investigators. Lancet 345: 1582–1583.
8. Nadal JC, Van Groeningen CJ, Pinedo HM, Peters GJ, (1988) In vivo potentiation of 5-fluorouracil by leucovorin in murine colon carcinoma. Biomed Pharmacother 42: 387–393.
9. Wolmark N, Bryant J, Smith R, Grem J, Allegra C, et al. (1998) Adjuvant 5-fluorouracil and leucovorin with or without interferon alfa-2a in colon carcinoma: National Surgical Adjuvant Breast and Bowel Project protocol C-05. J Natl Cancer Inst 90: 1810–1816.
10. Hung SW, Mody HR, Govindarajan R, (2012) Overcoming nucleoside analog chemoresistance of pancreatic cancer: a therapeutic challenge. Cancer Lett 320: 138–149.
11. Shi S, Yao W, Xu J, Long J, Liu C, et al. (2012) Combinational therapy: new hope for pancreatic cancer? Cancer Lett 317: 127–135.
12. de la Cruz-Morcillo MA, Valero ML, Callejas-Valera JL, Arias-Gonzalez L, Melgar-Rojas P, et al. (2012) P38MAPK is a major determinant of the balance between apoptosis and autophagy triggered by 5-fluorouracil: implication in resistance. Oncogene 31: 1073–1085.
13. Cartlidge RA, Knebel A, Peggie M, Alexandrov A, Phizicky EM, et al. (2005) The tRNA methylase METTL1 is phosphorylated and inactivated by PKB and RSK in vitro and in cells. EMBO J 24: 1696–1705.
14. Frye M, Dragoni I, Chin SF, Spiteri I, Kurowski A, et al. (2010) Genomic gain of 5p15 leads to over-expression of Misu (NSUN2) in breast cancer. Cancer Lett 289: 71–80.
15. Okamoto M, Hirata S, Sato S, Koga S, Fujii M, et al. (2012) Frequent increased gene copy number and high protein expression of tRNA (cytosine-5-)-methyltransferase (NSUN2) in human cancers. DNA Cell Biol 31: 660–671.
16. Wikman H, Nymark P, Vayrynen A, Jarmalaite S, Kallioniemi A, et al. (2005) CDK4 is a probable target gene in a novel amplicon at 12q13.3-q14.1 in lung cancer. Genes Chromosomes Cancer 42: 193–199.
17. Sakita-Suto S, Kanda A, Suzuki F, Sato S, Takata T, et al. (2007) Aurora-B regulates RNA methyltransferase NSUN2. Mol Biol Cell 18: 1107–1117.
18. Motorin Y, Grosjean H, (1999) Multisite-specific tRNA:m5C-methyltransferase (Trm4) in yeast Saccharomyces cerevisiae: identification of the gene and substrate specificity of the enzyme. RNA 5: 1105–1118.
19. Wu P, Brockenbrough JS, Paddy MR, Aris JP, (1998) NCL1, a novel gene for a non-essential nuclear protein in Saccharomyces cerevisiae. Gene 220: 109–117.
20. Alexandrov A, Martzen MR, Phizicky EM, (2002) Two proteins that form a complex are required for 7-methylguanosine modification of yeast tRNA. RNA 8: 1253–1266.
21. Alexandrov A, Chernyakov I, Gu W, Hiley SL, Hughes TR, et al. (2006) Rapid tRNA decay can result from lack of nonessential modifications. Mol Cell 21: 87–96.
22. Chernyakov I, Whipple JM, Kotelawala L, Grayhack EJ, Phizicky EM, (2008) Degradation of several hypomodified mature tRNA species in Saccharomyces cerevisiae is mediated by Met22 and the 5′-3′ exonucleases Rat1 and Xrn1. Genes Dev 22: 1369–1380.
23. Whipple JM, Lane EA, Chernyakov I, D'Silva S, Phizicky EM, (2011) The yeast rapid tRNA decay pathway primarily monitors the structural integrity of the acceptor and T-stems of mature tRNA. Genes Dev 25: 1173–1184.
24. Bahr A, Hankeln T, Fiedler T, Hegemann J, Schmidt ER, (1999) Molecular analysis of METTL1, a novel human methyltransferase-like gene with a high degree of phylogenetic conservation. Genomics 57: 424–428.
25. Gustavsson M, Ronne H, (2008) Evidence that tRNA modifying enzymes are important in vivo targets for 5-fluorouracil in yeast. RNA 14: 666–674.
26. Frye M, Watt FM, (2006) The RNA methyltransferase Misu (NSun2) mediates Myc-induced proliferation and is upregulated in tumors. Curr Biol 16: 971–981.
27. Blanco S, Kurowski A, Nichols J, Watt FM, Benitah SA, et al. (2011) The RNA-methyltransferase Misu (NSun2) poises epidermal stem cells to differentiate. PLoS Genet 7: e1002403.
28. Kuchino Y, Borek E, (1976) Changes in transfer RNA's in human malignant trophoblastic cells (BeWo line). Cancer Res 36: 2932–2936.
29. Pavon-Eternod M, Gomes S, Geslain R, Dai Q, Rosner MR, et al. (2009) tRNA over-expression in breast cancer and functional consequences. Nucleic Acids Res 37: 7268–7280.
30. Auxilien S, Guerineau V, Szweykowska-Kulinska Z, Golinelli-Pimpaneau B, (2012) The human tRNA m (5) C methyltransferase Misu is multisite-specific. RNA Biol 9: 1331–1338.
31. Squires JE, Patel HR, Nousch M, Sibbritt T, Humphreys DT, et al. (2012) Widespread occurrence of 5-methylcytosine in human coding and non-coding RNA. Nucleic Acids Res 40: 5023–5033.
32. Khoddami V, Cairns BR, (2013) Identification of direct targets and modified bases of RNA cytosine methyltransferases. Nat Biotechnol 31: 458–464.
33. Hussain S, Sajini AA, Blanco S, Dietmann S, Lombard P, et al. (2013) NSun2-mediated cytosine-5 methylation of vault noncoding RNA determines its processing into regulatory small RNAs. Cell Rep 4: 255–261.
34. Zhang X, Liu Z, Yi J, Tang H, Xing J, et al. (2012) The tRNA methyltransferase NSun2 stabilizes p16INK(4) mRNA by methylating the 3′-untranslated region of p16. Nat Commun 3: 712.
35. Martinez FJ, Lee JH, Lee JE, Blanco S, Nickerson E, et al. (2012) Whole exome sequencing identifies a splicing mutation in NSUN2 as a cause of a Dubowitz-like syndrome. J Med Genet 49: 380–385.
36. Khan MA, Rafiq MA, Noor A, Hussain S, Flores JV, et al. (2012) Mutation in NSUN2, which encodes an RNA methyltransferase, causes autosomal-recessive intellectual disability. Am J Hum Genet 90: 856–863.
37. Abbasi-Moheb L, Mertel S, Gonsior M, Nouri-Vahid L, Kahrizi K, et al. (2012) Mutations in NSUN2 cause autosomal-recessive intellectual disability. Am J Hum Genet 90: 847–855.
38. Hussain S, Benavente SB, Nascimento E, Dragoni I, Kurowski A, et al. (2009) The nucleolar RNA methyltransferase Misu (NSun2) is required for mitotic spindle stability. J Cell Biol 186: 27–40.
39. Towns WL, Begley TJ, (2012) Transfer RNA methytransferases and their corresponding modifications in budding yeast and humans: activities, predications, and potential roles in human health. DNA Cell Biol 31: 434–454.
40. Watanabe K, Miyagawa R, Tomikawa C, Mizuno R, Takahashi A, et al. (2013) Degradation of initiator tRNAMet by Xrn1/2 via its accumulation in the nucleus of heat-treated HeLa cells. Nucleic Acids Res 41: 4671–4685.
41. Ruggero D, Pandolfi PP, (2003) Does the ribosome translate cancer? Nat Rev Cancer 3: 179–192.
42. Pandolfi PP, (2004) Aberrant mRNA translation in cancer pathogenesis: an old concept revisited comes finally of age. Oncogene 23: 3134–3137.
43. Lazaris-Karatzas A, Montine KS, Sonenberg N, (1990) Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature 345: 544–547.
44. Tatsuka M, Mitsui H, Wada M, Nagata A, Nojima H, et al. (1992) Elongation factor-1 alpha gene determines susceptibility to transformation. Nature 359: 333–336.
45. Borek E, Kerr SJ, (1972) Atypical transfer RNA's and their origin in neoplastic cells. Adv Cancer Res 15: 163–190.
46. Pavon-Eternod M, Gomes S, Rosner MR, Pan T, (2013) Overexpression of initiator methionine tRNA leads to global reprogramming of tRNA expression and increased proliferation in human epithelial cells. RNA 19: 461–466.
47. Suzuki F, Horikawa M, (1973) A replica plating method of cultured mammalian cells. Methods Cell Biol 6: 127–142.
48. Kakunaga T (1981) Approaches toward developing a human transformation assay system. In: Myron AM, Nawin CM, editors. Mammalian Cell Transformation by Chemical Carcinogens. Washington, DC, U.S.A.: Senate Press. pp. 355–382.
49. Suzuki F, Suzuki K, Nikaido O, (1984) An improved soft agar method for determining neoplastic transformation in vitro. J Tissue Cult Methods 8: 109–113.
50. Franken NA, Rodermond HM, Stap J, Haveman J, van Bree C, (2006) Clonogenic assay of cells in vitro. Nat Protoc 1: 2315–2319.
51. Tatsuka M, Sato S, Kitajima S, Suto S, Kawai H, et al. (2005) Overexpression of Aurora-A potentiates HRAS-mediated oncogenic transformation and is implicated in oral carcinogenesis. Oncogene 24: 1122–1127.
52. Kanda A, Kawai H, Suto S, Kitajima S, Sato S, et al. (2005) Aurora-B/AIM-1 kinase activity is involved in Ras-mediated cell transformation. Oncogene 24: 7266–7272.