The Impact of dUTPase on Ribonucleotide Reductase-Induced Genome Instability in Cancer Cells

Cell Reports

Volumn 16, Issue 5, 2016, Pages 1287-1299

  Chen, Chih Wei ^a   Tsao, Ning ^b   Huang, Lin Yi ^a   Yen, Yun ^d,e   Liu, Xiyong ^e,f   Lehman, Christine ^g   Wang, Yuh Hwa ^h   Tseng, Mei Chun ⁱ   Chen, Yu Ju ^c,i   Ho, Yi Chi ⁱ   Chen, Chian Feng ^a   Chang, Zee Fen ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^d CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^e TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^f California Cancer Institute   (United States)

^g WAKE FOREST SCHOOL OF MEDICINE   (United States)

^h UNIVERSITY OF VIRGINIA   (United States)

ⁱ INSTITUTE OF CHEMISTRY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYURIDINE TRIPHOSPHATE PYROPHOSPHATASE; RIBONUCLEOTIDE REDUCTASE; URACIL; DUTP PYROPHOSPHATASE; INORGANIC PYROPHOSPHATASE;

ADULT; AGE DISTRIBUTION; AGED; ARTICLE; BREAST CANCER; CANCER CELL; CANCER PROGNOSIS; CANCER SURVIVAL; CELL TRANSFORMATION; COLORECTAL CANCER; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENE CONTROL; GENOME STRESS; GENOMIC INSTABILITY; HEREDITY; HUMAN; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; CHROMOSOME FRAGILE SITE; GENETICS; HT-29 CELL LINE; MCF-7 CELL LINE; MIDDLE AGED; NEOPLASM; PROGNOSIS; TUMOR CELL LINE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; CELL LINE, TUMOR; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOME FRAGILE SITES; FEMALE; GENOMIC INSTABILITY; HT29 CELLS; HUMANS; MALE; MCF-7 CELLS; MIDDLE AGED; NEOPLASMS; PROGNOSIS; PYROPHOSPHATASES; RIBONUCLEOTIDE REDUCTASES;

EID: 84989877205     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.06.094     Document Type: Article

References (51)

1. Aye, Y., Li, M., Long, M.J., Weiss, R.S., Ribonucleotide reductase and cancer: biological mechanisms and targeted therapies. Oncogene 34 (2015), 2011–2021.
2. Bakkenist, C.J., Kastan, M.B., DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421 (2003), 499–506.
3. Bedard, P.L., Hansen, A.R., Ratain, M.J., Siu, L.L., Tumour heterogeneity in the clinic. Nature 501 (2013), 355–364.
4. Bester, A.C., Roniger, M., Oren, Y.S., Im, M.M., Sarni, D., Chaoat, M., Bensimon, A., Zamir, G., Shewach, D.S., Kerem, B., Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145 (2011), 435–446.
5. Bryan, D.S., Ransom, M., Adane, B., York, K., Hesselberth, J.R., High resolution mapping of modified DNA nucleobases using excision repair enzymes. Genome Res. 24 (2014), 1534–1542.
6. Burrell, R.A., McClelland, S.E., Endesfelder, D., Groth, P., Weller, M.C., Shaikh, N., Domingo, E., Kanu, N., Dewhurst, S.M., Gronroos, E., et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 494 (2013), 492–496.
7. Burrell, R.A., McGranahan, N., Bartek, J., Swanton, C., The causes and consequences of genetic heterogeneity in cancer evolution. Nature 501 (2013), 338–345.
8. Canman, C.E., Lawrence, T.S., Shewach, D.S., Tang, H.Y., Maybaum, J., Resistance to fluorodeoxyuridine-induced DNA damage and cytotoxicity correlates with an elevation of deoxyuridine triphosphatase activity and failure to accumulate deoxyuridine triphosphate. Cancer Res. 53 (1993), 5219–5224.
9. Chabes, A., Stillman, B., Constitutively high dNTP concentration inhibits cell cycle progression and the DNA damage checkpoint in yeast Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 104 (2007), 1183–1188.
10. Chabes, A., Georgieva, B., Domkin, V., Zhao, X., Rothstein, R., Thelander, L., Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell 112 (2003), 391–401.
11. Chabes, A.L., Björklund, S., Thelander, L., S Phase-specific transcription of the mouse ribonucleotide reductase R2 gene requires both a proximal repressive E2F-binding site and an upstream promoter activating region. J. Biol. Chem. 279 (2004), 10796–10807.
12. Chan, K.L., Palmai-Pallag, T., Ying, S., Hickson, I.D., Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 11 (2009), 753–760.
13. Chang, D.J., Cimprich, K.A., DNA damage tolerance: when it's OK to make mistakes. Nat. Chem. Biol. 5 (2009), 82–90.
14. Chang, Z.F., Huang, D.Y., Hsue, N.C., Differential phosphorylation of human thymidine kinase in proliferating and M phase-arrested human cells. J. Biol. Chem. 269 (1994), 21249–21254.
15. Chen, J., Bozza, W., Zhuang, Z., Ubiquitination of PCNA and its essential role in eukaryotic translesion synthesis. Cell Biochem. Biophys. 60 (2011), 47–60.
16. D'Angiolella, V., Donato, V., Forrester, F.M., Jeong, Y.T., Pellacani, C., Kudo, Y., Saraf, A., Florens, L., Washburn, M.P., Pagano, M., Cyclin F-mediated degradation of ribonucleotide reductase M2 controls genome integrity and DNA repair. Cell 149 (2012), 1023–1034.
17. Davidson, M.B., Katou, Y., Keszthelyi, A., Sing, T.L., Xia, T., Ou, J., Vaisica, J.A., Thevakumaran, N., Marjavaara, L., Myers, C.L., et al. Endogenous DNA replication stress results in expansion of dNTP pools and a mutator phenotype. EMBO J. 31 (2012), 895–907.
18. Durkin, S.G., Glover, T.W., Chromosome fragile sites. Annu. Rev. Genet. 41 (2007), 169–192.
19. Ferraro, P., Franzolin, E., Pontarin, G., Reichard, P., Bianchi, V., Quantitation of cellular deoxynucleoside triphosphates. Nucleic Acids Res., 38, 2010, e85.
20. Friedberg, E.C., Lehmann, A.R., Fuchs, R.P., Trading places: how do DNA polymerases switch during translesion DNA synthesis?. Mol. Cell 18 (2005), 499–505.
21. Gandhi, M., Dillon, L.W., Pramanik, S., Nikiforov, Y.E., Wang, Y.H., DNA breaks at fragile sites generate oncogenic RET/PTC rearrangements in human thyroid cells. Oncogene 29 (2010), 2272–2280.
22. Hu, C.M., Yeh, M.T., Tsao, N., Chen, C.W., Gao, Q.Z., Chang, C.Y., Lee, M.H., Fang, J.M., Sheu, S.Y., Lin, C.J., et al. Tumor cells require thymidylate kinase to prevent dUTP incorporation during DNA repair. Cancer Cell 22 (2012), 36–50.
23. Jackson, D.A., Pombo, A., Replicon clusters are stable units of chromosome structure: evidence that nuclear organization contributes to the efficient activation and propagation of S phase in human cells. J. Cell Biol. 140 (1998), 1285–1295.
24. Jeggo, P.A., Pearl, L.H., Carr, A.M., DNA repair, genome stability and cancer: a historical perspective. Nat. Rev. Cancer 16 (2016), 35–42.
25. Kim, N., Jinks-Robertson, S., dUTP incorporation into genomic DNA is linked to transcription in yeast. Nature 459 (2009), 1150–1153.
26. Krokan, H.E., Bjørås, M., Base excision repair. Cold Spring Harb. Perspect. Biol., 5, 2013, a012583.
27. Kruiswijk, F., Labuschagne, C.F., Vousden, K.H., p53 in survival, death and metabolic health: a lifeguard with a licence to kill. Nat. Rev. Mol. Cell Biol. 16 (2015), 393–405.
28. Ladner, R.D., Lynch, F.J., Groshen, S., Xiong, Y.P., Sherrod, A., Caradonna, S.J., Stoehlmacher, J., Lenz, H.J., dUTP nucleotidohydrolase isoform expression in normal and neoplastic tissues: association with survival and response to 5-fluorouracil in colorectal cancer. Cancer Res. 60 (2000), 3493–3503.
29. Lis, E.T., O'Neill, B.M., Gil-Lamaignere, C., Chin, J.K., Romesberg, F.E., Identification of pathways controlling DNA damage induced mutation in Saccharomyces cerevisiae. DNA Repair (Amst.) 7 (2008), 801–810.
30. Liu, X., Lai, L., Wang, X., Xue, L., Leora, S., Wu, J., Hu, S., Zhang, K., Kuo, M.L., Zhou, L., et al. Ribonucleotide reductase small subunit M2B prognoses better survival in colorectal cancer. Cancer Res. 71 (2011), 3202–3213.
31. Liu, X., Zhang, H., Lai, L., Wang, X., Loera, S., Xue, L., He, H., Zhang, K., Hu, S., Huang, Y., et al. Ribonucleotide reductase small subunit M2 serves as a prognostic biomarker and predicts poor survival of colorectal cancers. Clin. Sci. 124 (2013), 567–578.
32. Lu, A.G., Feng, H., Wang, P.X., Han, D.P., Chen, X.H., Zheng, M.H., Emerging roles of the ribonucleotide reductase M2 in colorectal cancer and ultraviolet-induced DNA damage repair. World J. Gastroenterol. 18 (2012), 4704–4713.
33. Lukas, C., Savic, V., Bekker-Jensen, S., Doil, C., Neumann, B., Pedersen, R.S., Grøfte, M., Chan, K.L., Hickson, I.D., Bartek, J., Lukas, J., 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13 (2011), 243–253.
34. Marusyk, A., Polyak, K., Tumor heterogeneity: causes and consequences. Biochim. Biophys. Acta 1805 (2010), 105–117.
35. Mathews, C.K., Deoxyribonucleotide metabolism, mutagenesis and cancer. Nat. Rev. Cancer 15 (2015), 528–539.
36. Méndez, J., Stillman, B., Chromatin association of human origin recognition complex, cdc6, and minichromosome maintenance proteins during the cell cycle: assembly of prereplication complexes in late mitosis. Mol. Cell. Biol. 20 (2000), 8602–8612.
37. Minocherhomji, S., Ying, S., Bjerregaard, V.A., Bursomanno, S., Aleliunaite, A., Wu, W., Mankouri, H.W., Shen, H., Liu, Y., Hickson, I.D., Replication stress activates DNA repair synthesis in mitosis. Nature 528 (2015), 286–290.
38. Naim, V., Wilhelm, T., Debatisse, M., Rosselli, F., ERCC1 and MUS81-EME1 promote sister chromatid separation by processing late replication intermediates at common fragile sites during mitosis. Nat. Cell Biol. 15 (2013), 1008–1015.
39. Niida, H., Katsuno, Y., Sengoku, M., Shimada, M., Yukawa, M., Ikura, M., Ikura, T., Kohno, K., Shima, H., Suzuki, H., et al. Essential role of Tip60-dependent recruitment of ribonucleotide reductase at DNA damage sites in DNA repair during G1 phase. Genes Dev. 24 (2010), 333–338.
40. Nordlund, P., Reichard, P., Ribonucleotide reductases. Annu. Rev. Biochem. 75 (2006), 681–706.
41. Poli, J., Tsaponina, O., Crabbé, L., Keszthelyi, A., Pantesco, V., Chabes, A., Lengronne, A., Pasero, P., dNTP pools determine fork progression and origin usage under replication stress. EMBO J. 31 (2012), 883–894.
42. Prakash, S., Johnson, R.E., Prakash, L., Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74 (2005), 317–353.
43. Roos, W.P., Thomas, A.D., Kaina, B., DNA damage and the balance between survival and death in cancer biology. Nat. Rev. Cancer 16 (2016), 20–33.
44. Sabouri, N., Viberg, J., Goyal, D.K., Johansson, E., Chabes, A., Evidence for lesion bypass by yeast replicative DNA polymerases during DNA damage. Nucleic Acids Res. 36 (2008), 5660–5667.
45. Waters, L.S., Minesinger, B.K., Wiltrout, M.E., D'Souza, S., Woodruff, R.V., Walker, G.C., Eukaryotic translesion polymerases and their roles and regulation in DNA damage tolerance. Microbiol. Mol. Biol. Rev. 73 (2009), 134–154.
46. Wilson, P.M., Fazzone, W., LaBonte, M.J., Lenz, H.J., Ladner, R.D., Regulation of human dUTPase gene expression and p53-mediated transcriptional repression in response to oxaliplatin-induced DNA damage. Nucleic Acids Res. 37 (2009), 78–95.
47. Wilson, P.M., Danenberg, P.V., Johnston, P.G., Lenz, H.J., Ladner, R.D., Standing the test of time: targeting thymidylate biosynthesis in cancer therapy. Nat. Rev. Clin. Oncol. 11 (2014), 282–298.
48. Xu, X., Page, J.L., Surtees, J.A., Liu, H., Lagedrost, S., Lu, Y., Bronson, R., Alani, E., Nikitin, A.Y., Weiss, R.S., Broad overexpression of ribonucleotide reductase genes in mice specifically induces lung neoplasms. Cancer Res. 68 (2008), 2652–2660.
49. Ying, S., Minocherhomji, S., Chan, K.L., Palmai-Pallag, T., Chu, W.K., Wass, T., Mankouri, H.W., Liu, Y., Hickson, I.D., MUS81 promotes common fragile site expression. Nat. Cell Biol. 15 (2013), 1001–1007.
50. Zeman, M.K., Cimprich, K.A., Causes and consequences of replication stress. Nat. Cell Biol. 16 (2014), 2–9.
51. Zhang, W., Tan, S., Paintsil, E., Dutschman, G.E., Gullen, E.A., Chu, E., Cheng, Y.C., Analysis of deoxyribonucleotide pools in human cancer cell lines using a liquid chromatography coupled with tandem mass spectrometry technique. Biochem. Pharmacol. 82 (2011), 411–417.