DNA binding properties of human Cdc45 suggest a function as molecular wedge for DNA unwinding

Nucleic Acids Research

Volumn 42, Issue 4, 2014, Pages 2308-2319

  Szambowska, Anna ^a,b   Tessmer, Ingrid ^c   Kursula, Petri ^d,e   Usskilat, Christian ^a   Prus, Piotr ^d   Pospiech, Helmut ^a,d   Grosse, Frank ^a,f  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b UNIVERSITY OF GDA SK   (Poland)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d UNIVERSITY OF OULU   (Finland)

^e UNIVERSITY OF HAMBURG   (Germany)

^f FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL CYCLE PROTEIN; DNA FRAGMENT; DOUBLE STRANDED DNA; MONOMER; PROTEIN CDC45; RECJ PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

AB INITIO CALCULATION; ALPHA HELIX; ARTICLE; ATOMIC FORCE MICROSCOPY; BINDING AFFINITY; BIOPHYSICS; CIRCULAR DICHROISM; COMPLEX FORMATION; CONTROLLED STUDY; DNA BINDING; DNA DENATURATION; DNA REPLICATION; DNA STRUCTURE; LIGHT SCATTERING; MOLECULAR WEDGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN STRUCTURE; RNA TRANSLATION; STRUCTURE ANALYSIS; SYNCHROTRON RADIATION; X RAY CRYSTALLOGRAPHY;

CELL CYCLE PROTEINS; DNA; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HUMANS; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY;

EID: 84895827561     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1217     Document Type: Article

References (55)

1. Araki, H. (2010) Cyclin-dependent kinase-dependent initiation of chromosomal DNA replication. Curr. Opin. Cell. Biol., 22, 766-771.
2. Diffley, J.F. (2011) Quality control in the initiation of eukaryotic DNA replication. Philos. Trans. R. Soc. Lond. B Biol. Sci., 366, 3545-3553.
3. Labib, K. (2010) How do Cdc7 and cyclin-dependent kinases trigger the initiation of chromosome replication in eukaryotic cells? Genes Dev., 24, 1208-1219.
4. MacNeill, S.A. (2010) Structure and function of the GINS complex, a key component of the eukaryotic replisome. Biochem. J., 425, 489-500.
5. Pospiech, H., Grosse, F. and Pisani, F.M. (2010) The initiation step of eukaryotic DNA replication. Subcell Biochem., 50, 79-104.
6. Aparicio, O.M., Weinstein, D.M. and Bell, S.P. (1997) Components and dynamics of DNA replication complexes in S. cerevisiae: redistribution of MCM proteins and Cdc45p during S phase. Cell, 91, 59-69.
7. Aparicio, T., Ibarra, A. and Mendez, J. (2006) Cdc45-MCM-GINS, a new power player for DNA replication. Cell Div., 1, 18-18.
8. Hardy, C.F. (1997) Identification of Cdc45p, an essential factor required for DNA replication. Gene, 187, 239-246.
9. Bauerschmidt, C., Pollok, S., Kremmer, E., Nasheuer, H.-P. and Grosse, F. (2007) Interactions of human Cdc45 with the Mcm2-7 complex, the GINS complex, and DNA polymerases delta and epsilon during S phase. Genes Cells, 12, 745-758.
10. Pacek, M., Tutter, A.V., Kubota, Y., Takisawa, H. and Walter, J.C. (2006) Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol. Cell, 21, 581-587.
11. Pacek, M. and Walter, J.C. (2004) A requirement for MCM7 and Cdc45 in chromosome unwinding during eukaryotic DNA replication. EMBO J., 23, 3667-3676.
12. Kang, Y.H., Galal, W.C., Farina, A., Tappin, I. and Hurwitz, J. (2012) Properties of the human Cdc45/Mcm2-7/GINS helicase complex and its action with DNA polymerase epsilon in rolling circle DNA synthesis. Proc. Natl Acad. Sci. USA, 109, 6042-6047.
13. Onesti, S. and Macneill, S.A. (2013) Structure and evolutionary origins of the CMG complex. Chromosoma, 122, 47-53.
14. Sclafani, R.A. and Holzen, T.M. (2007) Cell cycle regulation of DNA replication. Annu. Rev. Genet., 41, 237-280.
15. Ilves, I., Petojevic, T., Pesavento, J.J. and Botchan, M.R. (2010) Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol. Cell, 37, 247-258.
16. Costa, A., Ilves, I., Tamberg, N., Petojevic, T., Nogales, E., Botchan, M.R. and Berger, J.M. (2011) The structural basis for MCM2-7 helicase activation by GINS and Cdc45. Nat. Struct. Mol. Biol., 18, 471-477.
17. Schmidt, U., Wollmann, Y., Franke, C., Grosse, F., Saluz, H.-P. and Hanel, F. (2008) Characterization of the interaction between the human DNA topoisomerase IIbeta-binding protein 1 (TopBP1) and the cell division cycle 45 (Cdc45) protein. Biochem. J., 409, 169-177.
18. Takaya, J., Kusunoki, S. and Ishimi, Y. (2013) Protein interaction and cellular localization of human CDC45. J. Biochem., 153, 381-388.
19. Zou, L. and Stillman, B. (2000) Assembly of a complex containing Cdc45p, replication protein A, and Mcm2p at replication origins controlled by S-phase cyclin-dependent kinases and Cdc7p-Dbf4p kinase. Mol. Cell Biol., 20, 3086-3096.
20. Krastanova, I., Sannino, V., Amenitsch, H., Gileadi, O., Pisani, F.M. and Onesti, S. (2012) Structural and functional insights into the DNA replication factor Cdc45 reveal an evolutionary relationship to the DHH family of phosphoesterases. J. Biol. Chem., 287, 4121-4128.
21. Aravind, L. and Koonin, E.V. (1998) The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci., 23, 469-472.
22. Sanchez-Pulido, L. and Ponting, C.P. (2011) Cdc45: the missing RecJ ortholog in eukaryotes? Bioinformatics, 27, 1885-1888.
23. Yamagata, A., Kakuta, Y., Masui, R. and Fukuyama, K. (2002) The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proc. Natl Acad. Sci. USA, 99, 5908-5912.
24. Kajander, T., Kellosalo, J. and Goldman, A. (2013) Inorganic pyrophosphatases: one substrate, three mechanisms. FEBS Lett., 587, 1863-1869.
25. Ugochukwu, E., Lovering, A.L., Mather, O.C., Young, T.W. and White, S.A. (2007) The crystal structure of the cytosolic exopolyphosphatase from Saccharomyces cerevisiae reveals the basis for substrate specificity. J. Mol. Biol., 371, 1007-1021.
26. Lovett, S.T. and Kolodner, R.D. (1989) Identification and purification of a single-stranded-DNA-specific exonuclease encoded by the recJ gene of Escherichia coli. Proc. Natl Acad. Sci. USA, 86, 2627-2631.
27. Han, E.S., Cooper, D.L., Persky, N.S., Sutera, V.A. Jr, Whitaker, R.D., Montello, M.L. and Lovett, S.T. (2006) RecJ exonuclease: substrates, products and interaction with SSB. Nucleic Acids Res., 34, 1084-1091.
28. Sutera, V.A. Jr, Han, E.S., Rajman, L.A. and Lovett, S.T. (1999) Mutational analysis of the RecJ exonuclease of Escherichia coli: identification of phosphoesterase motifs. J. Bacteriol., 181, 6098-6102.
29. Courcelle, C.T., Chow, K.H., Casey, A. and Courcelle, J. (2006) Nascent DNA processing by RecJ favors lesion repair over translesion synthesis at arrested replication forks in Escherichia coli. Proc. Natl Acad. Sci. USA, 103, 9154-9159.
30. Chow, K.H. and Courcelle, J. (2007) RecBCD and RecJ/RecQ initiate DNA degradation on distinct substrates in UV-irradiated Escherichia coli. Radiat. Res., 168, 499-506.
31. Cooper, D.L., Lahue, R.S. and Modrich, P. (1993) Methyl-directed mismatch repair is bidirectional. J. Biol. Chem., 268, 11823-11829.
32. Wurst, H. and Kornberg, A. (1994) A soluble exopolyphosphatase of Saccharomyces cerevisiae. Purification and characterization. J. Biol. Chem., 269, 10996-11001.
33. Wakamatsu, T., Kitamura, Y., Kotera, Y., Nakagawa, N., Kuramitsu, S. and Masui, R. (2010) Structure of RecJ exonuclease defines its specificity for single-stranded DNA. J. Biol. Chem., 285, 9762-9769.
34. Winzer, A.T., Kraft, C., Bhushan, S., Stepanenko, V. and Tessmer, I. (2012) Correcting for AFM tip induced topography convolutions in protein-DNA samples. Ultramicroscopy, 121, 8-15.
35. van Stokkum, I.H., Spoelder, H.J., Bloemendal, M., van Grondelle, R. and Groen, F.C. (1990) Estimation of protein secondary structure and error analysis from circular dichroism spectra. Anal. Biochem., 191, 110-118.
36. Manavalan, P. and Johnson, W.C. Jr (1987) Variable selection method improves the prediction of protein secondary structure from circular dichroism spectra. Anal. Biochem., 167, 76-85.
37. Sreerama, N. and Woody, R.W. (1993) A self-consistent method for the analysis of protein secondary structure from circular dichroism. Anal. Biochem., 209, 32-44.
38. Whitmore, L. and Wallace, B.A. (2004) DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data. Nucleic Acids Res., 32, W668-W673.
39. Sreerama, N. and Woody, R.W. (2000) Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set. Anal. Biochem., 287, 252-260.
40. Petoukhov, M.V., Franke, D., Shkumatov, A.V., Tria, G., Kikhney, A.G., Gajda, M., Gorba, C., Mertens, H.D.T., Konarev, P.V. and Svergun, D.I. (2012) New developments in the ATSAS program package for small-angle scattering data analysis. J. Appl. Crystallogr., 45, 342-350.
41. Konarev, P.V., Volkov, V.V., Sokolova, A.V., Koch, M.H.J. and Svergun, D.I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr., 36, 1277-1282.
42. Svergun, D.I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr., 25, 495-503.
43. Svergun, D.I., Petoukhov, M.V. and Koch, M.H. (2001) Determination of domain structure of proteins from X-ray solution scattering. Biophys. J., 80, 2946-2953.
44. Franke, D. and Svergun, D.I. (2009) DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J. Appl. Crystallogr., 42, 342-346.
45. Kozin, M.B. and Svergun, D.I. (2001) Automated matching of high-and low-resolution structural models. J. Appl. Crystallogr., 34, 33-41.
46. Volkov, V.V. and Svergun, D.I. (2003) Uniqueness of ab initio shape determination in small-angle scattering. J. Appl. Crystallogr., 36, 860-864.
47. Svergun, D., Barberato, C. and Koch, M.H.J. (1995) CRYSOL-a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr., 28, 768-773.
48. Petoukhov, M.V. and Svergun, D.I. (2005) Global rigid body modeling of macromolecular complexes against small-angle scattering data. Biophys. J., 89, 1237-1250.
49. Bernado, P., Mylonas, E., Petoukhov, M.V., Blackledge, M. and Svergun, D.I. (2007) Structural characterization of flexible proteins using small-angle X-ray scattering. J. Am. Chem. Soc., 129, 5656-5664.
50. Rambo, R.P. and Tainer, J.A. (2013) Accurate assessment of mass, models and resolution by small-angle scattering. Nature, 496, 477-481.
51. Hirose, S., Shimizu, K. and Noguchi, T. (2010) POODLE-I:disordered region prediction by integrating POODLE series and structural information predictors based on a workflow approach. In Silico Biol., 10, 185-191.
52. Blanchet, C.E. and Svergun, D.I. (2012) Small-angle X-ray scattering on biological macromolecules and nanocomposites in solution. Annu. Rev. Phys. Chem., 64, 37-54.
53. Durand, D., Vives, C., Cannella, D., Perez, J., Pebay-Peyroula, E., Vachette, P. and Fieschi, F. (2010) NADPH oxidase activator p67(phox) behaves in solution as a multidomain protein with semi-flexible linkers. J. Struct. Biol., 169, 45-53.
54. Receveur-Brechot, V. and Durand, D. (2012) How random are intrinsically disordered proteins? A small angle scattering perspective. Curr. Protein Pept. Sci., 13, 55-75.
55. Bruck, I. and Kaplan, D.L. (2013) Cdc45 protein-single-stranded DNA interaction is important for stalling the helicase during replication stress. J. Biol. Chem., 288, 7550-7563.