The N-terminus of the human RecQL4 helicase is a homeodomain-like DNA interaction motif

Nucleic Acids Research

Volumn 40, Issue 17, 2012, Pages 8309-8324

  Ohlenschläger, Oliver ^a   Kuhnert, Anja ^b   Schneider, Annerose ^a   Haumann, Sebastian ^a   Bellstedt, Peter ^a   Keller, Heidi ^a   Saluz, Hans Peter ^b,c   Hortschansky, Peter ^b   Hänel, Frank ^b   Grosse, Frank ^a,c   Görlach, Matthias ^a   Pospiech, Helmut ^a,d  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b HANS KNÖLL INSTITUTE   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d UNIVERSITY OF OULU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ARGININE; DNA; DNA BINDING PROTEIN; DOUBLE STRANDED DNA; HELICASE; PROTEIN; RECQL4 HELICASE; REPLICATION INITIATION FACTOR; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; Y SHAPED DNA;

AMINO TERMINAL SEQUENCE; ANIMAL; ARTICLE; CONTROLLED STUDY; HETERONUCLEAR NUCLEAR MAGNETIC RESONANCE; HOMEODOMAIN LIKE DNA INTERACTION MOTIF; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN MOTIF; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; SEQUENCE HOMOLOGY; YEAST;

AMINO ACID SEQUENCE; CARRIER PROTEINS; DNA; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HOMEODOMAIN PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; NUCLEAR PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECQ HELICASES; SEQUENCE ALIGNMENT;

METAZOA;

EID: 84866930447     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks591     Document Type: Article

References (67)

1. Chu, W.K. and Hickson, I.D. (2009) RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer., 9, 644-654.
2. Kellermayer, R. (2006) The versatile RECQL4. Genet. Med., 8, 213-216.
3. Siitonen, H.A., Sotkasiira, J., Biervliet, M., Benmansour, A., Capri, Y., Cormier-Daire, V., Crandall, B., Hannula-Jouppi, K., Hennekam, R., Herzog, D. et al. (2009) The mutation spectrum in RECQL4 diseases. Eur. J. Hum. Genet., 17, 151-158.
4. Kitao, S., Lindor, N.M., Shiratori, M., Furuichi, Y. and Shimamoto, A. (1999) Rothmund-thomson syndrome responsible gene, RECQL4: genomic structure and products. Genomics, 61, 268-276.
5. Macris, M.A., Krejci, L., Bussen, W., Shimamoto, A. and Sung, P. (2006) Biochemical characterization of the RECQ4 protein, mutated in Rothmund-Thomson syndrome. DNA Repair, 5, 172-180. (Pubitemid 43069518)
6. Xu, X. and Liu, Y. (2009) Dual DNA unwinding activities of the Rothmund-Thomson syndrome protein, RECQ4. EMBO J., 28, 568-577.
7. Capp, C., Wu, J. and Hsieh, T.S. (2009) Drosophila RecQ4 has a 3'-5' DNA helicase activity that is essential for viability. J. Biol. Chem., 284, 30845-30852.
8. Suzuki, T., Kohno, T. and Ishimi, Y. (2009) DNA helicase activity in purified human RECQL4 protein. J. Biochem., 146, 327-335.
9. Ichikawa, K., Noda, T. and Furuichi, Y. (2002) [Preparation of the gene targeted knockout mice for human premature aging diseases, Werner syndrome, and Rothmund-Thomson syndrome caused by the mutation of DNA helicases]. Nippon Yakurigaku Zasshi, 119, 219-226. (Pubitemid 34456569)
10. Hoki, Y., Araki, R., Fujimori, A., Ohhata, T., Koseki, H., Fukumura, R., Nakamura, M., Takahashi, H., Noda, Y., Kito, S. et al. (2003) Growth retardation and skin abnormalities of the Recql4-deficient mouse. Hum. Mol. Genet., 12, 2293-2299. (Pubitemid 37160873)
11. Mann, M.B., Hodges, C.A., Barnes, E., Vogel, H., Hassold, T.J. and Luo, G. (2005) Defective sister-chromatid cohesion, aneuploidy and cancer predisposition in a mouse model of type II Rothmund-Thomson syndrome. Hum. Mol. Genet., 14, 813-825. (Pubitemid 40403277)
12. Sangrithi, M.N., Bernal, J.A., Madine, M., Philpott, A., Lee, J., Dunphy, W.G. and Venkitaraman, A.R. (2005) Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell, 121, 887-898. (Pubitemid 40806420)
13. Matsuno, K., Kumano, M., Kubota, Y., Hashimoto, Y. and Takisawa, H. (2006) The N-terminal noncatalytic region of Xenopus RecQ4 is required for chromatin binding of DNA polymerase alpha in the initiation of DNA replication. Mol. Cell Biol., 26, 4843-4852. (Pubitemid 43955802)
14. Tanaka, S., Umemori, T., Hirai, K., Muramatsu, S., Kamimura, Y. and Araki, H. (2007) CDK-dependent phosphorylation of Sld2 and Sld3 initiates DNA replication in budding yeast. Nature, 445, 328-332. (Pubitemid 46122821)
15. Xu, X., Rochette, P.J., Feyissa, E.A., Su, T.V. and Liu, Y. (2009) MCM10 mediates RECQ4 association with MCM2-7 helicase complex during DNA replication. EMBO J., 28, 3005-3014.
16. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
17. Bartels, C., Xia, T., Billeter, M., Guntert, P. and Wuthrich, K. (1995) The program XEASY for computer-supported NMR spectral analysis of biological macromolecules. J. Biomol. NMR, 6, 1-10.
18. Schlott, B., Wohnert, J., Icke, C., Hartmann, M., Ramachandran, R., Guhrs, K.H., Glusa, E., Flemming, J., Gorlach, M., Grosse, F. et al. (2002) Interaction of Kazal-type inhibitor domains with serine proteinases: biochemical and structural studies. J. Mol. Biol., 318, 533-546. (Pubitemid 34734845)
19. Ohlenschlager, O., Ramachandran, R., Flemming, J., Guhrs, K.H., Schlott, B. and Brown, L.R. (1997) NMR secondary structure of the plasminogen activator protein staphylokinase. J. Biomol. NMR, 9, 273-286. (Pubitemid 127505388)
20. Herrmann, T., Guntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE-identification in the NOESY spectra using the new software ATNOS. J. Biomol. NMR, 24, 171-189. (Pubitemid 36113646)
21. Herrmann, T., Guntert, P. and Wuthrich, K. (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J. Mol. Biol., 319, 209-227. (Pubitemid 34729497)
22. Vuister, G.W. and Bax, A. (1993) Quantitative J correlation: a new approach for measuring homonuclear three-bond J(HNHa) coupling constants in 15 N-enriched proteins. J. Am. Chem. Soc., 115, 7772-7777.
23. Guntert, P., Billeter, M., Ohlenschlager, O., Brown, L.R. and Wuthrich, K. (1998) Conformational analysis of protein and nucleic acid fragments with the new grid search algorithm FOUND. J. Biomol. NMR, 12, 543-548. (Pubitemid 128511326)
24. Luginbuhl, P., Guntert, P., Billeter, M. and Wuthrich, K. (1996) The new program OPAL for molecular dynamics simulations and energy refinements of biological macromolecules. J. Biomol. NMR, 8, 136-146. (Pubitemid 126706783)
25. Koradi, R., Billeter, M. and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph, 14, 51-55. (Pubitemid 26152976)
26. Laskowski, R.A., Rullmannn, J.A., MacArthur, M.W., Kaptein, R. and Thornton, J.M. (1996) AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486. (Pubitemid 126706801)
27. Herold, S., Wanzel, M., Beuger, V., Frohme, C., Beul, D., Hillukkala, T., Syvaoja, J., Saluz, H.P., Haenel, F. and Eilers, M. (2002) Negative regulation of the mammalian UV response by Myc through association with Miz-1. Mol. Cell, 10, 509-521. (Pubitemid 35284171)
28. Borth, N., Massier, J., Franke, C., Sachse, K., Saluz, H.P. and Hanel, F. (2010) Chlamydial protease CT441 interacts with SRAP1 co-activator of estrogen receptor alpha and partially alleviates its co-activation activity. J. Steroid Biochem. Mol. Biol., 119, 89-95.
29. Wollmann, Y., Schmidt, U., Wieland, G.D., Zipfel, P.F., Saluz, H.P. and Hanel, F. (2007) The DNA topoisomerase IIbeta binding protein 1 (TopBP1) interacts with poly (ADP-ribose) polymerase (PARP-1). J. Cell Biochem., 102, 171-182. (Pubitemid 47378920)
30. Leung, C.C., Gong, Z., Chen, J. and Glover, J.N. (2011) Molecular basis of BACH1/FANCJ recognition by TopBP1 in DNA replication checkpoint control. J. Biol. Chem., 286, 4292-4301.
31. Wishart, D.S. and Sykes, B.D. (1994) The 13C chemical-shift index: a simple method for the identification of protein secondary structure using 13C chemical-shift data. J. Biomol. NMR, 4, 171-180.
32. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-W549.
33. Billeter, M., Qian, Y.Q., Otting, G., Muller, M., Gehring, W. and Wuthrich, K. (1993) Determination of the nuclear magnetic resonance solution structure of an Antennapedia homeodomain-DNA complex. J. Mol. Biol., 234, 1084-1093. (Pubitemid 24027238)
34. Clarke, N.D., Kissinger, C.R., Desjarlais, J., Gilliland, G.L. and Pabo, C.O. (1994) Structural studies of the engrailed homeodomain. Protein Sci., 3, 1779-1787. (Pubitemid 24356602)
35. Li, T., Stark, M.R., Johnson, A.D. and Wolberger, C. (1995) Crystal structure of the MATa1/MAT alpha 2 homeodomain heterodimer bound to DNA. Science, 270, 262-269.
36. Joshi, R., Passner, J.M., Rohs, R., Jain, R., Sosinsky, A., Crickmore, M.A., Jacob, V., Aggarwal, A.K., Honig, B. and Mann, R.S. (2007) Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell, 131, 530-543. (Pubitemid 350007697)
37. Gehring, W.J., Qian, Y.Q., Billeter, M., Furukubo-Tokunaga, K., Schier, A.F., Resendez-Perez, D., Affolter, M., Otting, G. and Wuthrich, K. (1994) Homeodomain-DNA recognition. Cell, 78, 211-223. (Pubitemid 24241090)
38. Billeter, M., Guntert, P., Luginbuhl, P. and Wuthrich, K. (1996) Hydration and DNA recognition by homeodomains. Cell, 85, 1057-1065. (Pubitemid 26231172)
39. Thangavel, S., Mendoza-Maldonado, R., Tissino, E., Sidorova, J.M., Yin, J., Wang, W., Monnat, R.J. Jr, Falaschi, A. and Vindigni, A. (2010) Human RECQ1 and RECQ4 helicases play distinct roles in DNA replication initiation. Mol. Cell Biol., 30, 1382-1396.
40. Biamonti, G., Giacca, M., Perini, G., Contreas, G., Zentilin, L., Weighardt, F., Guerra, M., Della Valle, G., Saccone, S., Riva, S. et al. (1992) The gene for a novel human lamin maps at a highly transcribed locus of chromosome 19 which replicates at the onset of S-phase. Mol. Cell Biol., 12, 3499-3506.
41. Connelly, M.A., Zhang, H., Kieleczawa, J. and Anderson, C.W. (1998) The promoters for human DNA-PKcs (PRKDC) and MCM4: divergently transcribed genes located at chromosome 8 band q11. Genomics, 47, 71-83. (Pubitemid 28080083)
42. Keller, C., Ladenburger, E.M., Kremer, M. and Knippers, R. (2002) The origin recognition complex marks a replication origin in the human TOP1 gene promoter. J. Biol. Chem., 277, 31430-31440. (Pubitemid 34968943)
43. Gorlach, M., Wittekind, M., Beckman, R.A., Mueller, L. and Dreyfuss, G. (1992) Interaction of the RNA-binding domain of the hnRNP C proteins with RNA. EMBO J., 11, 3289-3295.
44. Williamson, R.A., Carr, M.D., Frenkiel, T.A., Feeney, J. and Freedman, R.B. (1997) Mapping the binding site for matrix metalloproteinase on the N-terminal domain of the tissue inhibitor of metalloproteinases-2 by NMR chemical shift perturbation. Biochemistry, 36, 13882-13889. (Pubitemid 27494895)
45. Brennan, R.G. and Matthews, B.W. (1989) The helix-turn-helix DNA binding motif. J. Biol. Chem., 264, 1903-1906. (Pubitemid 19057656)
46. Wolberger, C. (1996) Homeodomain interactions. Curr. Opin. Struct. Biol., 6, 62-68. (Pubitemid 26073945)
47. Gehring, W.J., Muller, M., Affolter, M., Percival-Smith, A., Billeter, M., Qian, Y.Q., Otting, G. and Wuthrich, K. (1990) The structure of the homeodomain and its functional implications. Trends Genet., 6, 323-329.
48. Gehring, W.J. (1992) The homeobox in perspective. Trends Biochem. Sci., 17, 277-280.
49. Hanes, S.D. and Brent, R. (1989) DNA specificity of the bicoid activator protein is determined by homeodomain recognition helix residue 9. Cell, 57, 1275-1283. (Pubitemid 19169822)
50. Treisman, J., Gonczy, P., Vashishtha, M., Harris, E. and Desplan, C. (1989) A single amino acid can determine the DNA binding specificity of homeodomain proteins. Cell, 59, 553-562. (Pubitemid 19284468)
51. Falaschi, A., Abdurashidova, G. and Biamonti, G. (2010) DNA replication, development and cancer: a homeotic connection? Crit. Rev. Biochem. Mol. Biol., 45, 14-22.
52. Comelli, L., Marchetti, L., Arosio, D., Riva, S., Abdurashidova, G., Beltram, F. and Falaschi, A. (2009) The homeotic protein HOXC13 is a member of human DNA replication complexes. Cell Cycle, 8, 454-459.
53. de Stanchina, E., Gabellini, D., Norio, P., Giacca, M., Peverali, F.A., Riva, S., Falaschi, A. and Biamonti, G. (2000) Selection of homeotic proteins for binding to a human DNA replication origin. J. Mol. Biol., 299, 667-680.
54. Salsi, V., Ferrari, S., Ferraresi, R., Cossarizza, A., Grande, A. and Zappavigna, V. (2009) HOXD13 binds DNA replication origins to promote origin licensing and is inhibited by geminin. Mol. Cell Biol., 29, 5775-5788.
55. Marchetti, L., Comelli, L., D'Innocenzo, B., Puzzi, L., Luin, S., Arosio, D., Calvello, M., Mendoza-Maldonado, R., Peverali, F., Trovato, F. et al. (2010) Homeotic proteins participate in the function of human-DNA replication origins. Nucleic Acids Res., 38, 8105-8119.
56. Miotto, B. and Graba, Y. (2010) Control of DNA replication: a new facet of Hox proteins? Bioessays, 32, 800-807.
57. Otting, G., Qian, Y.Q., Billeter, M., Muller, M., Affolter, M., Gehring, W.J. and Wuthrich, K. (1990) Protein-DNA contacts in the structure of a homeodomain-DNA complex determined by nuclear magnetic resonance spectroscopy in solution. EMBO J., 9, 3085-3092.
58. Billeter, M., Qian, Y., Otting, G., Muller, M., Gehring, W.J. and Wuthrich, K. (1990) Determination of the three-dimensional structure of the Antennapedia homeodomain from Drosophila in solution by 1H nuclear magnetic resonance spectroscopy. J. Mol. Biol., 214, 183-197. (Pubitemid 20231218)
59. Nanda, V. and Brand, L. (2000) Aromatic interactions in homeodomains contribute to the low quantum yield of a conserved, buried tryptophan. Proteins, 40, 112-125. (Pubitemid 30368587)
60. Noyes, M.B., Christensen, R.G., Wakabayashi, A., Stormo, G.D., Brodsky, M.H. and Wolfe, S.A. (2008) Analysis of homeodomain specificities allows the family-wide prediction of preferred recognition sites. Cell, 133, 1277-1289. (Pubitemid 351852912)
61. Berger, M.F., Badis, G., Gehrke, A.R., Talukder, S., Philippakis, A.A., Pena-Castillo, L., Alleyne, T.M., Mnaimneh, S., Botvinnik, O.B., Chan, E.T. et al. (2008) Variation in homeodomain DNA binding revealed by high-resolution analysis of sequence preferences. Cell, 133, 1266-1276. (Pubitemid 351852913)
62. Im, J.S., Ki, S.H., Farina, A., Jung, D.S., Hurwitz, J. and Lee, J.K. (2009) Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc. Natl. Acad. Sci. USA, 106, 15628-15632.
63. Kanter, D.M. and Kaplan, D.L. (2010) Sld2 binds to origin single-stranded DNA and stimulates DNA annealing. Nucleic Acids Res., 39, 2580-2592.
64. Bruck, I., Kanter, D.M. and Kaplan, D.L. (2011) Enabling association of the GINS protein tetramer with the mini chromosome maintenance (Mcm)2-7 protein complex by phosphorylated Sld2 protein and single-stranded origin DNA. J Biol. Chem., 286, 36414-36426.
65. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402. (Pubitemid 27359211)
66. Nicholas, K.B., Nicholas, H.B. Jr and Deerfield, D.W. II (1997) GeneDoc: analysis and visualization of genetic variation. EMBNEW News, 4, 1-4.
67. Rost, B., Yachdav, G. and Liu, J. (2004) The PredictProtein server. Nucleic Acids Res., 32, W321-W326. (Pubitemid 39004075)