Steric exclusion and wrapping of the excluded DNA strand occurs along discrete external binding paths during MCM helicase unwinding

Nucleic Acids Research

Volumn 39, Issue 15, 2011, Pages 6585-6595

  Graham, Brian W ^a   Schauer, Grant D ^b   Leuba, Sanford H ^b   Trakselis, Michael A ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MINICHROMOSOME MAINTENANCE PROTEIN; SINGLE STRANDED DNA; ARCHAEAL PROTEIN; DNA; HELICASE; MUNG BEAN NUCLEASE; NUCLEASE S1; VEGETABLE PROTEIN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; DNA DENATURATION; DNA FOOTPRINTING; DNA PROTEIN COMPLEX; ENZYME STABILITY; FLUORESCENCE ANALYSIS; GENE MUTATION; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; STATISTICAL MODEL; STERIC EXCLUSION AND WRAPPING MODEL; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; MUTATION; PROTEIN BINDING; SULFOLOBUS SOLFATARICUS;

ARCHAEA; EUKARYOTA; SULFOLOBUS SOLFATARICUS;

ARCHAEAL PROTEINS; DNA; DNA HELICASES; MUTATION; PLANT PROTEINS; PROTEIN BINDING; SINGLE-STRAND SPECIFIC DNA AND RNA ENDONUCLEASES; SULFOLOBUS SOLFATARICUS;

EID: 80053576584     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkr345     Document Type: Article

References (45)

1. Forsburg, S.L. (2004) Eukaryotic MCM proteins: beyond replication initiation. Microbiol. Mol. Biol. Rev., 68, 109-131. (Pubitemid 38339657)
2. Bell, S.P. and Dutta, A. (2002) DNA replication in eukaryotic cells. Ann. Rev. Biochem., 71, 333-374. (Pubitemid 34800224)
3. Madine, M.A., Khoo, C.-Y., Mills, A.D., Musahl, C. and Laskey, R.A. (1995) The nuclear envelope prevents reinitiation of replication by regulating the binding of MCM3 to chromatin in Xenopus egg extracts. Curr. Biol., 5, 1270-1279. (Pubitemid 3000036)
4. Bochman, M.L. and Schwacha, A. (2008) The Mcm2-7 complex has in vitro helicase activity. Mol. Cell, 31, 287-293. (Pubitemid 352001397)
5. 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.
6. Iyer, L.M., Leipe, D.D., Koonin, E.V. and Aravind, L. (2004) Evolutionary history and higher order classification of AAA+ ATPases. J. Struct. Biol., 146, 11-31. (Pubitemid 38369015)
7. Brewster, A.S., Wang, G., Yu, X., Greenleaf, W.B., Carazo, J.M., Tjajadi, 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.
8. Duderstadt, K.E. and Berger, J.M. (2008) AAA+ATPases in the initiation of DNA replication. Crit. Rev. Biochem. Mol. Biol., 43, 163-187.
9. Neuwald, A.F., Aravind, L., Spouge, J.L. and Koonin, E.V. (1999) AAA+: a class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res., 9, 27-43. (Pubitemid 29095146)
10. 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. (Pubitemid 44941162)
11. 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. Mol. Biol., 10, 160-167. (Pubitemid 36297984)
12. McGeoch, A.T., Trakselis, M.A., Laskey, R.A. and Bell, S.D. (2005) Organization of the archaeal MCM complex on DNA and implication for the helicase mechanism. Nat. Struct. Mol. Biol., 12, 756-762. (Pubitemid 43086249)
13. Barry, E.R., McGeoch, A.T., Kelman, Z. and Bell, S.D. (2007) Archaeal MCM has separable processivity, substrate choice and helicase domains. Nucleic Acids Res., 35, 988-998. (Pubitemid 46344723)
14. Moreau, M.J., McGeoch, A.T., Lowe, A.R., Itzhaki, L.S. and Bell, S.D. (2007) ATPase site architecture and helicase mechanism of an archaeal MCM. Mol. Cell, 28, 304-314. (Pubitemid 47599994)
15. Barry, E.R., Lovett, J.E., Costa, A., Lea, S.M. and Bell, S.D. (2009) Intersubunit allosteric communication mediated by a conserved loop in the MCM helicase. Proc. Natl Acad. Sci., 106, 1051-1056.
16. Sakakibara, N., Kasiviswanathan, R., Melamud, E., Han, M., Schwarz, F.P. and Kelman, Z. (2008) Coupling of DNA binding and helicase activity is mediated by a conserved loop in the MCM protein. Nucleic Acids Res., 36, 1309-1320. (Pubitemid 351330946)
17. Li, D., Zhao, R., Lilyestrom, W., Gai, D., Zhang, R., DeCaprio, J.A., Fanning, E., Jochimiak, A., Szakonyi, G. and Chen, X.S. (2003) Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature, 423, 512-518. (Pubitemid 36648571)
18. Gomez-Llorente, Y., Fletcher, R.J., Chen, X.S., Carazo, J.M. and Martin, C.S. (2005) Polymorphism and double hexamer structure in the Archaeal minichromosome maintenance (MCM) helicase from Methanobacterium thermoautotrophicum. J. Biol. Chem., 280, 40909-40915. (Pubitemid 41780584)
19. Shin, J.-H., Heo, G.-Y. and Kelman, Z. (2009) The Methanothermobacter thermautotrophicus MCM helicase is active as a hexameric ring. J. Biol. Chem., 284, 540-546.
20. Patel, S.S. and Picha, K.M. (2000) Structure and function of hexameric helicases. Ann. Rev. Biochem., 69, 651-697.
21. Takahashi, T.S., Wigley, D.B. and Walter, J.C. (2005) Pumps, paradoxes and ploughshares: mechanism of the MCM2-7 DNA helicase. Trends Biochem. Sci., 30, 437-444. (Pubitemid 41033239)
22. Rothenberg, E., Trakselis, M.A., Bell, S.D. and Ha, T. (2007) MCM forked substrate specificity involves dynamic interaction with the 50-tail. J. Biol. Chem., 282, 34229-34234. (Pubitemid 350159423)
23. Sambrook, J. and Russell, D.W. (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Spring Harbor Press, Cold Spring Harbor, NY.
24. Morris, P.D. and Raney, K.D. (1999) DNA helicases displace streptavidin from biotin-labeled oligonucleotides. Biochemistry, 38, 5164-5171.
25. Mikheikin, A.L., Lin, H.-K., Mehta, P., Jen-Jacobson, L. and Trakselis, M.A. (2009) A trimeric DNA polymerase complex increases the native replication processivity. Nucleic Acids Res., 37, 7194-7205.
26. Roy, R., Hohng, S. and Ha, T. (2008) A practical guide to single-molecule FRET. Nat. Methods, 5, 507-516. (Pubitemid 351761757)
27. Axelrod, D. (2008) In John, J.C. and William Detrich, H. III (eds), Methods in Cell Biology, Vol. 89. Academic Press, Burlington, MA, pp. 169-221.
28. Fagerburg, M.V. and Leuba, S.H. (2011) Optimal Practices for Surface-tethered Single Molecule Total Internal Reflection Fluorescence Resonance Energy Transfer Analysis, 1st edn. Humana Press, New York, NY.
29. Li, K. (2008) The image stabilizer plugin for ImageJ, http://www.cs.cmu.edu/-kangli/code/Image-Stabilizer.html (1 August 2010, date last accessed), February, 2008.
30. Rasband, W.S. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA, http://imagej.nih.gov/ij/ (1 August 2010, date last accessed), 1997-2011.
31. 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. (Pubitemid 34952776)
32. 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.
33. Brewster, A., Slaymaker, I., Afif, S. and Chen, X. (2010) Mutational analysis of an archaeal minichromosome maintenance protein exterior hairpin reveals critical residues for helicase activity and DNA binding. BMC Mol. Biol., 11, 62.
34. Barry, E.R. and Bell, S.D. (2006) DNA replication in the Archaea. Microbiol. Mol. Biol. Rev., 70, 876-887. (Pubitemid 44958259)
35. Singleton, M.R., Dillingham, M.S. and Wigley, D.B. (2007) Structure and mechanism of helicases and nucleic acid translocases. Ann. Rev. Biochem., 76, 23-50.
36. 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. (Pubitemid 36305373)
37. Kaplan, D.L. and O'Donnell, M. (2004) Twin DNA pumps of a hexameric helicase provide power to simultaneously melt two duplexes. Mol. Cell, 15, 453-465. (Pubitemid 39092760)
38. Gai, D., Zhao, R., Li, D., Finkielstein, C.V. and Chen, X.S. (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell, 119, 47-60. (Pubitemid 39349319)
39. Wessel, R., Schweizer, J. and Stahl, H. (1992) Simian virus 40 T-antigen DNA helicase is a hexamer which forms a binary complex during bidirectional unwinding from the viral origin of DNA replication. J. Virol., 66, 804-815.
40. Brewster, A.S. and Chen, X.S. (2010) Insights into the MCM functional mechanism: lessons learned from the archaeal MCM complex. Crit. Rev. Biochem. Mol. Biol., 45, 243-256.
41. Matlock, D.L., Yeruva, L., Byrd, A.K., Mackintosh, S.G., Langston, C., Brown, C., Cameron, C.E., Fischer, C.J. and Raney, K.D. (2010) Investigation of translocation, DNA unwinding, and protein displacement by NS3h, the helicase domain from the hepatitis C virus helicase. Biochemistry, 49, 2097-2109.
42. Byrd, A.K. and Raney, K.D. (2006) Displacement of a DNA binding protein by Dda helicase. Nucleic Acids Res., 34, 3020-3029. (Pubitemid 44540429)
43. Pape, T., Meka, H., Chen, S., Vicentini, G., Heel, M.V. and Onesti, S. (2003) Hexameric ring structure of the full-length archaeal MCM protein complex. EMBO Rep., 4, 1079-1083. (Pubitemid 37527427)
44. Enemark, E.J. and Joshua-Tor, L. (2006) Mechanism of DNA translocation in a replicative hexameric helicase. Nature, 442, 270-275. (Pubitemid 44114897)
45. 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.