Molecular architecture of a multifunctional MCM complex

Nucleic Acids Research

Volumn 40, Issue 3, 2012, Pages 1366-1380

  Sanchez Berrondo, June ^a   Mesa, Pablo ^a   Ibarra, Arkaitz ^b,d   Martínez Jiménez, Maria I ^c   Blanco, Luis ^c   Méndez, Juan ^b   Boskovic, Jasminka ^a   Montoya, Guillermo ^a  

^a Macromolecular Crystallography Group   (Spain)

^b Centro Nacional de Investigaciones Oncológicas   (Spain)

^c CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

^d SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; DOUBLE STRANDED DNA; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN; PRIMASE; SINGLE STRANDED DNA; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS CEREUS; COMPLEX FORMATION; CONTROLLED STUDY; DNA REPLICATION; ELECTRON MICROSCOPY; ENZYME ACTIVITY; GEL MOBILITY SHIFT ASSAY; IMAGE ANALYSIS; IN VITRO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SITE DIRECTED MUTAGENESIS; ULTRACENTRIFUGATION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACILLUS CEREUS; BACTERIAL PROTEINS; DEOXYRIBONUCLEOTIDES; DNA; DNA HELICASES; DNA PRIMASE; DNA, SINGLE-STRANDED; DNA-DIRECTED DNA POLYMERASE; MODELS, MOLECULAR; MUTATION; PROTEIN STRUCTURE, TERTIARY;

BACILLUS CEREUS; PAPILLOMAVIRIDAE;

EID: 84856862677     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr831     Document Type: Article

References (51)

1. Chong, J. P., Hayashi, M. K., Simon, M. N., Xu, R. M. and Stillman, B. (2000) A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc. Natl Acad. Sci. USA, 97, 1530-1535.
2. Shechter, D. F., Ying, C. Y. and Gautier, J. (2000) The intrinsic DNA helicase activity of Methanobacterium thermoautotrophicum delta H minichromosome maintenance protein. J. Biol. Chem., 275, 15049-15059.
3. Niedenzu, T., Roleke, D., Bains, G., Scherzinger, E. and Saenger, W. (2001) Crystal structure of the hexameric replicative helicase RepA of plasmid RSF1010. J. Mol. Biol., 306, 479-487.
4. Bochman, M. L. and Schwacha, A. (2008) The Mcm2-7 complex has in vitro helicase activity. Mol. Cell, 31, 287-293.
5. Gomez-Llorente, Y., Fletcher, R. J., Chen, X. S., Carazo, J. M. and San Martin, C. (2005) Polymorphism and double hexamer structure in the archaeal minichromosome maintenance (MCM) helicase from Methanobacterium thermoautotrophicum. J. Biol. Chem., 280, 40909-40915.
6. Remus, D., Beuron, F., Tolun, G., Griffith, J. D., Morris, E. P. and Diffley, J. F. (2009) Concerted loading of Mcm2-7 double hexamers around DNA during DNA replication origin licensing. Cell, 139, 719-730.
7. Kelman, Z., Lee, J. K. and Hurwitz, J. (1999) The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc. Natl Acad. Sci. USA, 96, 14783-14788.
8. Carpentieri, F., De Felice, M., De Falco, M., Rossi, M. and Pisani, F. M. (2002) Physical and functional interaction between the mini-chromosome maintenance-like DNA helicase and the single-stranded DNA binding protein from the crenarchaeon Sulfolobus solfataricus. J. Biol. Chem., 277, 12118-12127.
9. Forsburg, S. L. (2004) Eukaryotic MCM proteins: beyond replication initiation. Microbiol Mol. Biol. Rev., 68, 109-131.
10. Going, J. J., Keith, W. N., Neilson, L., Stoeber, K., Stuart, R. C. and Williams, G. H. (2002) Aberrant expression of minichromosome maintenance proteins 2 and 5, and Ki-67 in dysplastic squamous oesophageal epithelium and Barrett's mucosa. Gut, 50, 373-377.
11. Shetty, A., Loddo, M., Fanshawe, T., Prevost, A. T., Sainsbury, R., Williams, G. H. and Stoeber, K. (2005) DNA replication licensing and cell cycle kinetics of normal and neoplastic breast. Br. J. Cancer, 93, 1295-1300.
12. Honeycutt, K. A., Chen, Z., Koster, M. I., Miers, M., Nuchtern, J., Hicks, J., Roop, D. R. and Shohet, J. M. (2006) Deregulated minichromosomal maintenance protein MCM7 contributes to oncogene driven tumorigenesis. Oncogene, 25, 4027-4032.
13. Fletcher, R. J., Bishop, B. E., Leon, R. P., Sclafani, R. A., Ogata, C. M. and Chen, X. S. (2003) The structure and function of MCM from archaeal M. Thermoautotrophicum. Nat. Struct. Biol., 10, 160-167.
14. Liu, W., Pucci, B., Rossi, M., Pisani, F. M. and Ladenstein, R. (2008) Structural analysis of the Sulfolobus solfataricus MCM protein N-terminal domain. Nucleic Acids Res., 36, 3235-3243.
15. Bae, B., Chen, Y. H., Costa, A., Onesti, S., Brunzelle, J. S., Lin, Y., Cann, I. K. and Nair, S. K. (2009) Insights into the architecture of the replicative helicase from the structure of an archaeal MCM homolog. Structure, 17, 211-222.
16. Brewster, A. S., Wang, G., Yu, X., Greenleaf, W. B., Carazo, J. M., Tjajadia, M., Klein, M. G. and Chen, X. S. (2008) Crystal structure of a near-full-length archaeal MCM: functional insights for an AAA+hexameric helicase. Proc. Natl Acad. Sci. USA, 105, 20191-20196.
17. Pape, T., Meka, H., Chen, S., Vicentini, G., van Heel, M. and Onesti, S. (2003) Hexameric ring structure of the full-length archaeal MCM protein complex. EMBO Rep., 4, 1079-1083.
18. Chen, Y. J., Yu, X., Kasiviswanathan, R., Shin, J.-H., Kelman, Z. and Egelman, E. H. (2005) Structural polymorphism of Methanothermobacter thermautotrophicus MCM. J. Mol. Biol., 346, 389-394.
19. Costa, A., Pape, T., van Heel, M., Brick, P., Patwardhan, A. and Onesti, S. (2006) Structural basis of the Methanothermobacter thermautotrophicus MCM helicase activity. Nucleic Acids Res., 34, 5829-5838.
20. Costa, A., van Duinen, G., Medagli, B., Chong, J., Sakakibara, N., Kelman, Z., Nair, S. K., Patwardhan, A. and Onesti, S. (2008) Cryo-electron microscopy reveals a novel DNA-binding site on the MCM helicase. EMBO J., 27, 2250-2258.
21. Jenkinson, E. R., Costa, A., Leech, A. P., Patwardhan, A., Onesti, S. and Chong, J. P. (2009) Mutations in subdomain B of the minichromosome maintenance (MCM) helicase affect DNA binding and modulate conformational transitions. J. Biol. Chem., 284, 5654-5661.
22. 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.
23. McGeoch, A. T. and Bell, S. D. (2005) Eukaryotic/archaeal primase and MCM proteins encoded in a bacteriophage genome. Cell, 120, 167-168.
24. Iyer, L. M., Koonin, E. V., Leipe, D. D. and Aravind, L. (2005) Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucleic Acids Res., 33, 3875-3896.
25. McGeoch, A. T. and Bell, S. D. (2005) Eukaryotic/archaeal primase and MCM proteins encoded in a bacteriophage genome. Cell, 120, 167-168.
26. Lipps, G., Weinzierl, A. O., Scheven, von, G., Buchen, C. and Cramer, P. (2004) Structure of a bifunctional DNA primase-polymerase. Nat. Struct. Mol. Biol., 11, 157-162.
27. Frick, D. N. and Richardson, C. C. (2001) DNA primases. Annu. Rev. Biochem., 70, 39-80.
28. Panuska, J. R. and Goldthwait, D. A. (1980) A DNA-dependent ATPase from T4-infected Escherichia coli. Purification and properties of a 63, 000-dalton enzyme and its conversion to a 22, 000-dalton form. J. Biol. Chem., 255, 5208-5214.
29. Ludtke, S. J., Baldwin, P. R. and Chiu, W. (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol., 128, 82-97.
30. Sorzano, C. O., Marabini, R., Velazquez-Muriel, J., Bilbao-Castro, J. R., Scheres, S. H., Carazo, J. M. and Pascual-Montano, A. (2004) XMIPP: a new generation of an open-source image processing package for electron microscopy. J. Struct. Biol., 148, 194-204.
31. Samuels, M., Gulati, G., Shin, J.-H., Opara, R., Mcsweeney, E., Sekedat, M., Long, S., Kelman, Z. and Jeruzalmi, D. (2009) A biochemically active MCM-like helicase in Bacillus cereus. Nucleic Acids Res., 37, 4441-4452.
32. Hanson, P. I. and Whiteheart, S. W. (2005) AAA+proteins: have engine, will work. Nat. Rev. Mol. Cell. Biol., 6, 519-529.
33. Cavanaugh, N. A. and Kuchta, R. D. (2009) Initiation of new DNA strands by the herpes simplex virus-1 primase-helicase complex and either herpes DNA polymerase or human DNA polymerase alpha. J. Biol. Chem., 284, 1523-1532.
34. Holmes, A. M., Cheriathundam, E., Bollum, F. J. and Chang, L. M. (1985) Initiation of DNA synthesis by the calf thymus DNA polymerase-primase complex. J. Biol. Chem., 260, 10840-10846.
35. Parker, W. B. and Cheng, Y. C. (1987) Inhibition of DNA primase by nucleoside triphosphates and their arabinofuranosyl analogs. Mol. Pharmacol., 31, 146-151.
36. Evrin, C., Clarke, P., Zech, J., Lurz, R., Sun, J., Uhle, S., Li, H., Stillman, B. and Speck, C. (2009) A double-hexameric MCM2-7 complex is loaded onto origin DNA during licensing of eukaryotic DNA replication. Proc. Natl Acad. Sci. USA, 106.
37. Forsburg, S. L. (2004) Eukaryotic MCM proteins: beyond replication initiation. Microbiol Mol. Biol. Rev., 68, 109-131.
38. Toth, E. A., Li, Y., Sawaya, M. R., Cheng, Y. and Ellenberger, T. (2003) The crystal structure of the bifunctional primase-helicase of bacteriophage T7. Mol. Cell, 12, 1113-1123.
39. Brewster, A. S., Slaymaker, I. M., Afif, S. A. and Chen, X. S. Mutational analysis of an archaeal minichromosome maintenance protein exterior hairpin reveals critical residues for helicase activity and DNA binding. BMC Mol. Biol., 11, 62.
40. McGeoch, A. T., Trakselis, M. A., Laskey, R. A. and Bell, S. D. (2005) Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat. Struct. Mol. Biol., 12, 756-762.
41. Frank, E. G. and Woodgate, R. (2007) Increased catalytic activity and altered fidelity of human DNA polymerase iota in the presence of manganese. J. Biol. Chem., 282, 24689-24696.
42. Domíguez, O., Ruiz, J. F., Laión de Lera, T., Garcí-Dióz, M., Gonzaílez, M. A., Kirchhoff, T., Martez-A, C., Bernad, A. and Blanco, L. (2000) DNA polymerase mu (Pol mu), homologous to TdT, could act as a DNA mutator in eukaryotic cells. EMBO J., 19, 1731-1742.
43. Pitcher, R. S., Brissett, N. C., Picher, A. J., Andrade, P., Juarez, R., Thompson, D., Fox, G. C., Blanco, L. and Doherty, A. J. (2007) Structure and function of a mycobacterial NHEJ DNA repair polymerase. J. Mol. Biol., 366, 391-405.
44. Gabbai, C. B. and Marians, K. J. (2010) Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival. DNA Repair, 9, 202-209.
45. Lee, J. K. and Hurwitz, J. (2001) Processive DNA helicase activity of the minichromosome maintenance proteins 4, 6, and 7 complex requires forked DNA structures. Proc. Natl Acad. Sci. USA, 98, 54-59.
46. Kaplan, D. L., Davey, M. J. and O'Donnell, M. (2003) Mcm4, 6, 7 uses a "pump in ring" mechanism to unwind DNA by steric exclusion and actively translocate along a duplex. J. Biol. Chem., 278, 49171-49182.
47. Laskey, R. A. and Madine, M. A. (2003) A rotary pumping model for helicase function of MCM proteins at a distance from replication forks. EMBO Rep., 4, 26-30.
48. Méndez, J. and Stillman, B. (2003) Perpetuating the double helix: molecular machines at eukaryotic DNA replication origins. Bioessays, 25, 1158-1167.
49. Enemark, E. J. and Joshua-Tor, L. (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature, 442, 270-275.
50. Hingorani, M. M. and Patel, S. S. (1996) Cooperative interactions of nucleotide ligands are linked to oligomerization and DNA binding in bacteriophage T7 gene 4 helicases. Biochemistry, 35, 2218-2228.
51. Dean, F. B., Borowiec, J. A., Eki, T. and Hurwitz, J. (1992) The simian virus 40 T antigen double hexamer assembles around the DNA at the replication origin. J. Biol. Chem., 267, 14129-14137.