Depletion of deoxyribonucleotide pools is an endogenous source of DNA damage in cells undergoing oncogene-induced senescence

American Journal of Pathology

Volumn 182, Issue 1, 2013, Pages 142-151

  Mannava, Sudha ^a   Moparthy, Kalyana C ^a   Wheeler, Linda J ^b   Natarajan, Venkatesh ^a   Zucker, Shoshanna N ^a   Fink, Emily E ^a   Im, Michael ^c   Flanagan, Sheryl ^c   Burhans, William C ^a   Zeitouni, Nathalie C ^a   Shewach, Donna S ^c   Mathews, Christopher K ^b   Nikiforov, Mikhail A ^a  

^a ROSWELL PARK CANCER INSTITUTE   (United States)

^b OREGON STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEOXYRIBONUCLEOTIDE; HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RETINOBLASTOMA PROTEIN; RIBONUCLEOTIDE REDUCTASE; SHORT HAIRPIN RNA; THYMIDYLATE SYNTHASE; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CELL CYCLE ARREST; CELL PROLIFERATION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DOWN REGULATION; FIBROBLAST; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; MELANOMA CELL; NUCLEOTIDE METABOLISM; ONCOGENE; ONCOGENE INDUCED SENESCENCE; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; QUANTITATIVE ANALYSIS; RETINOBLASTOMA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENESCENCE;

CELL AGING; CELL PROLIFERATION; CELLS, CULTURED; DEOXYRIBONUCLEOTIDES; DNA DAMAGE; DNA REPLICATION; FIBROBLASTS; HUMANS; ONCOGENES; PROTO-ONCOGENE PROTEINS P21(RAS); RIBONUCLEOTIDE REDUCTASES; THYMIDYLATE SYNTHASE;

EID: 84871297080     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.09.011     Document Type: Article

References (37)

1. G.I. Evan, and F. d' Adda di Fagagna Cellular senescence: hot or what? Curr Opin Genet Dev 19 2009 25 31
2. V.G. Gorgoulis, and T.D. Halazonetis Oncogene-induced senescence: The bright and dark side of the response Curr Opin Cell Biol 22 2010 816 827
3. L.G. Larsson Oncogene- and tumor suppressor gene-mediated suppression of cellular senescence Semin Cancer Biol 21 2011 367 376
4. J. Bartkova, Z. Horejsí, K. Koed, A. Krämer, F. Tort, K. Zieger, P. Guldberg, M. Sehested, J.M. Nesland, C. Lukas, T. Orntoft, J. Lukas, and J. Bartek DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis Nature 434 2005 864 870 (Pubitemid 40558993)
5. J. Bartkova, N. Rezaei, M. Liontos, P. Karakaidos, D. Kletsas, N. Issaeva, L.V. Vassiliou, E. Kolettas, K. Niforou, V.C. Zoumpourlis, M. Takaoka, H. Nakagawa, F. Tort, K. Fugger, F. Johansson, M. Sehested, C.L. Andersen, L. Dyrskjot, T. Orntoft, J. Lukas, C. Kittas, T. Helleday, T.D. Halazonetis, J. Bartek, and V.G. Gorgoulis Oncogene-induced senescence is part of the tumorigenesis barrier imposed by DNA damage checkpoints Nature 444 2006 633 637 (Pubitemid 44864442)
6. R. Di Micco, M. Fumagalli, A. Cicalese, S. Piccinin, P. Gasparini, C. Luise, C. Schurra, M. Garre', P.G. Nuciforo, A. Bensimon, R. Maestro, P.G. Pelicci, and F. d'Adda di Fagagna Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication Nature 444 2006 638 642 (Pubitemid 44864443)
7. F.A. Mallette, and G. Ferbeyre The DNA damage signaling pathway connects oncogenic stress to cellular senescence Cell Cycle 6 2007 1831 1836 (Pubitemid 47327900)
8. D. Branzei, and M. Foiani Regulation of DNA repair throughout the cell cycle Nat Rev Mol Cell Biol 9 2008 297 308 (Pubitemid 351430844)
9. D. Branzei, and M. Foiani The checkpoint response to replication stress DNA Repair 8 2009 1038 1046
10. S. Burma, B.P. Chen, M. Murphy, A. Kurimasa, and D.J. Chen ATM phosphorylates histone H2AX in response to DNA double-strand breaks J Biol Chem 276 2001 42462 42467
11. S. Banin, L. Moyal, S. Shieh, Y. Taya, C.W. Anderson, L. Chessa, N.I. Smorodinsky, C. Prives, Y. Reiss, Y. Shiloh, and Y. Ziv Enhanced phosphorylation of p53 by ATM in response to DNA damage Science 281 1998 1674 1677
12. C.E. Canman, D.S. Lim, K.A. Cimprich, Y. Taya, K. Tamai, K. Sakaguchi, E. Appella, M.B. Kastan, and J.D. Siliciano Activation of the ATM kinase by ionizing radiation and phosphorylation of p53 Science 281 1998 1677 1679 (Pubitemid 28435584)
13. S. Matsuoka, M. Huang, and S.J. Elledge Linkage of ATM to cell cycle regulation by the Chk2 protein kinase Science 282 1998 1893 1897 (Pubitemid 28555269)
14. J.W. Yarbro Mechanism of action of hydroxyurea Semin Oncol 19 1992 1 10
15. B. Van Triest, H.M. Pinedo, G. Giaccone, and G.J. Peters Downstream molecular determinants of response to 5-fluorouracil and antifolatethymidylate synthase inhibitors Ann Oncol 11 2000 385 391 (Pubitemid 30333539)
16. S. Mannava, A.R. Omilian, J.A. Wawrzyniak, E.E. Fink, D. Zhuang, J.C. Miecznikowski, J.R. Marshall, M.S. Soengas, R.C. Sears, C.D. Morrison, and M.A. Nikiforov PP2A-B56α controls oncogene-induced senescence in normal and tumor human melanocytic cells Oncogene 31 2012 1484 1492
17. S. Mannava, V. Grachtchouk, L.J. Wheeler, M. Im, D. Zhuang, E.G. Slavina, C.K. Mathews, D.S. Shewach, and M.A. Nikiforov Direct role of nucleotide metabolism in C-MYC-dependent proliferation of melanoma cells Cell Cycle 7 2008 2392 2400
18. C.K. Mathews, and L.J. Wheeler Measuring DNA precursor pools in mitochondria Methods Mol Biol 554 2009 371 381
19. S. Eriksson, and L. Thelander Allosteric regulation of calf thymus ribonucleotidereductase Ciba Found Symp 68 1978 165 175
20. M. Friedkin Thymidylatesynthetase Adv Enzymol Relat Areas Mol Biol 38 1973 235 292
21. E.S. Arner, and S. Eriksson Mammalian deoxyribonucleoside kinases Pharmacol Ther 67 1995 155 186
22. S. Björklund, S. Skog, B. Tribukait, and L. Thelander S-phase-specific expression of mammalian ribonucleotidereductase R1 and R2 subunit mRNAs Biochemistry 29 1990 5452 5458 (Pubitemid 20202268)
23. L.G. Navalgund, C. Rossana, A.J. Muench, and L.F. Johnson Cell cycle regulation of thymidylatesynthetase gene expression in cultured mouse fibroblasts J Biol Chem 255 1980 7386 7390
24. O.V. Leontieva, and M.V. Blagosklonny DNA damaging agents and p53 do not cause senescence in quiescent cells, while consecutive re-activation of mTOR is associated with conversion to senescence Aging 2 2010 924 935
25. A.B. Pardee, C.J. Li, and G.P. Reddy Regulation in S phase by E2F Cell Cycle 3 2004 1091 1094 (Pubitemid 40268618)
26. M. Narita, S. Ñunez, E. Heard, M. Narita, A.W. Lin, S.A. Hearn, D.L. Spector, G.J. Hannon, and S.W. Lowe Rb-mediated heterochromatin formation and silencing of E2F target genes during cellular senescence Cell 113 2003 703 716 (Pubitemid 36724935)
27. B.D. Strahl, and C.D. Allis The language of covalent histone modifications Nature 403 2000 41 45 (Pubitemid 30038513)
28. R.D. Ladner The role of dUTPase and uracil-DNA repair in cancer chemotherapy Curr Protein Pept Sci 2 2001 361 370 (Pubitemid 33150476)
29. P.D. Boucher, L.J. Ostruszka, P.J. Murphy, and D.S. Shewach Hydroxyurea significantly enhances tumor growth delay in vivo with herpes simplex virus thymidine kinase/ganciclovir gene therapy Gene Therapy 9 2002 1023 1030
30. J.J. O'Konek, P.D. Boucher, A.A. Iacco, T.E. Wilson, and D.S. Shewach MLH1 deficiency enhances tumor cell sensitivity to ganciclovir Cancer Gene Ther 16 2009 683 692
31. T.J. Kinsella Coordination of DNA mismatch repair and base excision repair processing of chemotherapy and radiation damage for targeting resistant cancers Clin Cancer Res 15 2009 1853 1859
32. M.F. Arlt, A.C. Ozdemir, S.R. Birkeland, T.E. Wilson, and T.W. Glover Hydroxyurea induces de novo copy number variants in human cells Proc Natl Acad Sci U S A 108 2011 17360 17365
33. S.G. Durkin, and T.W. Glover Chromosome fragile sites Annu Rev Genet 41 2007 169 192
34. R. Holzerlandt, C. Orengo, P. Kellam, and M.M. Albà Identification of new herpesvirus gene homologs in the human genome Genome Res 12 2002 1739 1748 (Pubitemid 35363678)
35. O. Warburg On respiratory impairment in cancer cells Science 124 1956 269 270
36. M.G. Vander Heiden, L.C. Cantley, and C.B. Thompson Understanding the Warburg effect: The metabolic requirements of cell proliferation Science 324 2009 1029 1033
37. X. Tong, F. Zhao, and C.B. Thompson The molecular determinants of de novo nucleotide biosynthesis in cancer cells Curr Opin Genet Dev 19 2009 32 37