Spd2 assists Spd1 in the modulation of ribonucleotide reductase architecture but does not regulate deoxynucleotide pools

Journal of Cell Science

Volumn 127, Issue 11, 2014, Pages 2460-2470

  Vejrup Hansen, Rasmus ^a   Fleck, Oliver ^a,b   Landvad, Katrine ^a   Fahnøe, Ulrik ^a   Broendum, Sebastian S ^a   Ann Schreurs, Sofie ^c   Kragelund, Birthe B ^a   Carr, Antony M ^c   Holmberg, Christian ^a   Nielsen, Olaf ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b BANGOR UNIVERSITY   (United Kingdom)

^c UNIVERSITY OF SUSSEX   (United Kingdom)

Author keywords

Cancer model; Genome stability; Intrinsically disordered proteins; Ribonucleotide reductase; S. pombe

Indexed keywords

CHECKPOINT KINASE RAD3; DEOXYRIBONUCLEOTIDE; FUNGAL PROTEIN; RIBONUCLEOTIDE REDUCTASE; SPD1 PROTEIN; SPD2 PROTEIN; UNCLASSIFIED DRUG; CDT2 PROTEIN, S POMBE; CELL CYCLE PROTEIN; CHECKPOINT KINASE 2; DEOXYNUCLEOTIDE 3'-PHOSPHATASE; INTRINSICALLY DISORDERED PROTEIN; NUCLEOTIDASE; RAD3 PROTEIN, S POMBE; SCHIZOSACCHAROMYCES POMBE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SPD1 PROTEIN, S POMBE; SPD2 PROTEIN, S POMBE;

ARTICLE; CELL ACTIVATION; CELL ELONGATION; CELL GROWTH; CELL MUTANT; CELL SHAPE; CELL VIABILITY; CIRCULAR DICHROISM; CYTOARCHITECTURE; DNA DAMAGE; DNA REPLICATION; ENZYME REGULATION; GENE DELETION; GENETIC ANALYSIS; HETERONUCLEAR SINGLE QUANTUM COHERENCE; MEIOSIS; NEGATIVE FEEDBACK; NONHUMAN; NUCLEAR IMPORT; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECONDARY STRUCTURE; SCHIZOSACCHAROMYCES POMBE; WESTERN BLOTTING; ALLOSTERISM; AMINO ACID SEQUENCE; CELL CYCLE; DNA REPAIR; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN CONFORMATION; SCHIZOSACCHAROMYCES; SEQUENCE HOMOLOGY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALLOSTERIC REGULATION; AMINO ACID SEQUENCE; CELL CYCLE; CELL CYCLE PROTEINS; CHECKPOINT KINASE 2; DNA REPAIR; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEOTIDASES; PROTEIN CONFORMATION; RIBONUCLEOTIDE REDUCTASES; SCHIZOSACCHAROMYCES; SCHIZOSACCHAROMYCES POMBE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84901793114     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.139816     Document Type: Article

References (38)

1. Bähler, J., Wu, J. Q., Longtine, M. S., Shah, N. G., McKenzie, A., III, Steever, A. B., Wach, A., Philippsen, P. and Pringle, J. R. (1998). Heterologous modules for efficient and versatile PCR-based gene targeting in Schizosaccharomyces pombe. Yeast 14, 943-951.
2. Basrai, M. A., Velculescu, V. E., Kinzler, K. W. and Hieter, P. (1999). NORF5/ HUG1 is a component of the MEC1-mediated checkpoint response to DNA damage and replication arrest in Saccharomyces cerevisiae. Mol. Cell. Biol. 19, 7041-7049.
3. Beck, H., Nähse-Kumpf, V., Larsen, M. S., O'Hanlon, K. A., Patzke, S., Holmberg, C., Mejlvang, J., Groth, A., Nielsen, O., Syljuåsen, R. G. et al. (2012). Cyclin-dependent kinase suppression by WEE1 kinase protects the genome through control of replication initiation and nucleotide consumption. Mol. Cell. Biol. 32, 4226-4236.
4. Bester, A. C., Roniger, M., Oren, Y. S., Im, M. M., Sarni, D., Chaoat, M., Bensimon, A., Zamir, G., Shewach, D. S. and Kerem, B. (2011). Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 145, 435-446.
5. Chabes, A., Georgieva, B., Domkin, V., Zhao, X., Rothstein, R. and Thelander, L. (2003). Survival of DNA damage in yeast directly depends on increased dNTP levels allowed by relaxed feedback inhibition of ribonucleotide reductase. Cell 112, 391-401.
6. Danielsson, J., Liljedahl, L., Bárány-Wallje, E., Sønderby, P., Kristensen, L. H., Martinez-Yamout, M. A., Dyson, H. J., Wright, P. E., Poulsen, F. M., Mäler, L. et al. (2008). The intrinsically disordered RNR inhibitor Sml1 is a dynamic dimer. Biochemistry 47, 13428-13437.
7. Elledge, S. J., Zhou, Z., Allen, J. B. and Navas, T. A. (1993). DNA damage and cell cycle regulation of ribonucleotide reductase. Bioessays 15, 333-339.
8. Fairman, J. W., Wijerathna, S. R., Ahmad, M. F., Xu, H., Nakano, R., Jha, S., Prendergast, J., Welin, R. M., Flodin, S., Roos, A. et al. (2011). Structural basis for allosteric regulation of human ribonucleotide reductase by nucleotideinduced oligomerization. Nat. Struct. Mol. Biol. 18, 316-322.
9. Fleck, O., Vejrup-Hansen, R., Watson, A., Carr, A. M., Nielsen, O. and Holmberg, C. (2013). Spd1 accumulation causes genome instability independently of ribonucleotide reductase activity but functions to protect the genome when deoxynucleotide pools are elevated. J. Cell Sci. 126, 4985-4994.
10. Håkansson, P., Dahl, L., Chilkova, O., Domkin, V. and Thelander, L. (2006). The Schizosaccharomyces pombe replication inhibitor Spd1 regulates ribonucleotide reductase activity and dNTPs by binding to the large Cdc22 subunit. J. Biol. Chem. 281, 1778-1783.
11. Halazonetis, T. D., Gorgoulis, V. G. and Bartek, J. (2008). An oncogene-induced DNA damage model for cancer development. Science 319, 1352-1355.
12. Hofer, A., Crona, M., Logan, D. T. and Sjöberg, B. M. (2012). DNA building blocks: keeping control of manufacture. Crit. Rev. Biochem. Mol. Biol. 47, 50-63.
13. Holmberg, C. and Nielsen, O. (2012). Replication: DNA building block synthesis on demand. Curr. Biol. 22, R271-R272.
14. Holmberg, C., Fleck, O., Hansen, H. A., Liu, C., Slaaby, R., Carr, A. M. and Nielsen, O. (2005). Ddb1 controls genome stability and meiosis in fission yeast. Genes Dev. 19, 853-862.
15. Kjaerulff, S., Lautrup-Larsen, I., Truelsen, S., Pedersen, M. and Nielsen, O. (2005). Constitutive activation of the fission yeast pheromone-responsive pathway induces ectopic meiosis and reveals ste11 as a mitogen-activated protein kinase target. Mol. Cell. Biol. 25, 2045-2059.
16. Knutsen, J. H., Rein, I. D., Rothe, C., Stokke, T., Grallert, B. and Boye, E. (2011). Cell-cycle analysis of fission yeast cells by flow cytometry. PLoS ONE 6, e17175.
17. Lee, Y. D., Wang, J., Stubbe, J. and Elledge, S. J. (2008). Dif1 is a DNAdamage-regulated facilitator of nuclear import for ribonucleotide reductase. Mol. Cell 32, 70-80.
18. Liu, C., Powell, K. A., Mundt, K., Wu, L., Carr, A. M. and Caspari, T. (2003). Cop9/signalosome subunits and Pcu4 regulate ribonucleotide reductase by both checkpoint-dependent and-independent mechanisms. Genes Dev. 17, 1130-1140.
19. Liu, C., Poitelea, M., Watson, A., Yoshida, S. H., Shimoda, C., Holmberg, C., Nielsen, O. and Carr, A. M. (2005). Transactivation of Schizosaccharomyces pombe cdt2+ stimulates a Pcu4-Ddb1-CSN ubiquitin ligase. EMBO J. 24, 3940-3951.
20. Marguerat, S., Schmidt, A., Codlin, S., Chen, W., Aebersold, R. and Bähler, J. (2012). Quantitative analysis of fission yeast transcriptomes and proteomes in proliferating and quiescent cells. Cell 151, 671-683.
21. Maundrell, K. (1990). nmt1 of fission yeast. A highly transcribed gene completely repressed by thiamine. J. Biol. Chem. 265, 10857-10864.
22. Moreno, S., Klar, A. and Nurse, P. (1991). Molecular genetic analysis of fission yeast Schizosaccharomyces pombe. Methods Enzymol. 194, 795-823.
23. Moss, J., Tinline-Purvis, H., Walker, C. A., Folkes, L. K., Stratford, M. R., Hayles, J., Hoe, K. L., Kim, D. U., Park, H. O., Kearsey, S. E. et al. (2010). Break-induced ATR and Ddb1-Cul4(Cdt)2 ubiquitin ligase-dependent nucleotide synthesis promotes homologous recombination repair in fission yeast. Genes Dev. 24, 2705-2716.
24. Nestoras, K., Mohammed, A. H., Schreurs, A. S., Fleck, O., Watson, A. T., Poitelea, M., O'Shea, C., Chahwan, C., Holmberg, C., Kragelund, B. B. et al. (2010). Regulation of ribonucleotide reductase by Spd1 involves multiple mechanisms. Genes Dev. 24, 1145-1159.
25. Nielsen, O. (2003). COP9 signalosome: a provider of DNA building blocks. Curr. Biol. 13, R565-R567.
26. Nordlund, P. and Reichard, P. (2006). Ribonucleotide reductases. Annu. Rev. Biochem. 75, 681-706.
27. Reichard, P. (2010). Ribonucleotide reductases: substrate specificity by allostery. Biochem. Biophys. Res. Commun. 396, 19-23.
28. Rhind, N., Chen, Z., Yassour, M., Thompson, D. A., Haas, B. J., Habib, N., Wapinski, I., Roy, S., Lin, M. F., Heiman, D. I. et al. (2011). Comparative functional genomics of the fission yeasts. Science 332, 930-936.
29. Salguero, I., Guarino, E., Shepherd, M. E., Deegan, T. D., Havens, C. G., MacNeill, S. A., Walter, J. C. and Kearsey, S. E. (2012). Ribonucleotide reductase activity is coupled to DNA synthesis via proliferating cell nuclear antigen. Curr. Biol. 22, 720-726.
30. Tompa, P. (2002). Intrinsically unstructured proteins. Trends Biochem. Sci. 27, 527-533.
31. Uchiki, T., Dice, L. T., Hettich, R. L. and Dealwis, C. (2004). Identification of phosphorylation sites on the yeast ribonucleotide reductase inhibitor Sml1. J. Biol. Chem. 279, 11293-11303.
32. Weinberg, G., Ullman, B. and Martin, D. W., Jr (1981). Mutator phenotypes in mammalian cell mutants with distinct biochemical defects and abnormal deoxyribonucleoside triphosphate pools. Proc. Natl. Acad. Sci. USA 78, 2447-2451.
33. Woollard, A., Basi, G. and Nurse, P. (1996). A novel S phase inhibitor in fission yeast. EMBO J. 15, 4603-4612.
34. Wu, X. and Huang, M. (2008). Dif1 controls subcellular localization of ribonucleotide reductase bymediating nuclear import of the R2 subunit.Mol. Cell. Biol. 28, 7156-7167.
35. Yoshida, S. H., Al-Amodi, H., Nakamura, T., McInerny, C. J. and Shimoda, C. (2003). The Schizosaccharomyces pombe cdt2(+) gene, a target of G1-S phase-specific transcription factor complex DSC1, is required for mitotic and premeiotic DNA replication. Genetics 164, 881-893.
36. Zhao, X. and Rothstein, R. (2002). The Dun1 checkpoint kinase phosphorylates and regulates the ribonucleotide reductase inhibitor Sml1. Proc. Natl. Acad. Sci. USA 99, 3746-3751.
37. Zhao, X., Georgieva, B., Chabes, A., Domkin, V., Ippel, J. H., Schleucher, J., Wijmenga, S., Thelander, L. and Rothstein, R. (2000). Mutational and structural analyses of the ribonucleotide reductase inhibitor Sml1 define its Rnr1 interaction domain whose inactivation allows suppression of mec1 and rad53 lethality. Mol. Cell. Biol. 20, 9076-9083.
38. Zolezzi, F., Fuss, J., Uzawa, S. and Linn, S. (2002). Characterization of a Schizosaccharomyces pombe strain deleted for a sequence homologue of the human damaged DNA binding 1 (DDB1) gene. J. Biol. Chem. 277, 41183-41191.