Crystal structure of a near-full-length archaeal MCM: Functional insights for an AAA+ hexameric helicase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 105, Issue 51, 2008, Pages 20191-20196

  Brewster, Aaron S ^a   Wang, Ganggang ^a   Yu, Xian ^a   Greenleaf, William B ^a   Carazo, José María ^b   Tjajadi, Matthew ^a   Klein, Michael G ^a,c   Chen, Xiaojiang S ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^c DOE JOINT GENOME INSTITUTE   (United States)

Author keywords

hairpin; Cancer; DNA replication; Nucleic acid motor; Replicative helicase

Indexed keywords

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; DNA; HELICASE; MINICHROMOSOME MAINTENANCE PROTEIN;

AMINO TERMINAL SEQUENCE; ARCHAEBACTERIUM; ARTICLE; BIOCHEMISTRY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DNA REPLICATION; EUKARYOTE; EXTRACELLULAR MATRIX; METHANOTHERNOBACTER THERMAUTOTOPHICUS; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; SULFOLOBUS SOLFATARICUS;

ADENOSINE TRIPHOSPHATE; ARCHAEAL PROTEINS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA HELICASES; MUTAGENESIS, SITE-DIRECTED; PROTEIN CONFORMATION; PROTEIN SUBUNITS; SULFOLOBUS SOLFATARICUS;

ARCHAEA; EUKARYOTA; METHANOTHERMOBACTER THERMAUTOTROPHICUS; SULFOLOBUS SOLFATARICUS;

EID: 58149505656     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0808037105     Document Type: Article

References (36)

1. Lee JK, 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.
2. Ishimi Y (1997) A DNA helicase activity is associated with an MCM4, -6, and -7 protein complex. J Biol Chem 272:24508-24513.
3. You Z, Komamura Y, Ishimi Y (1999) Biochemical analysis of the intrinsic Mcm4-Mcm6-mcm7 DNA helicase activity. Mol Cell Biol 19:8003-8015.
4. Mendez J, Stillman B (2003) Perpetuating the double helix: Molecular machines at eukaryotic DNA replication origins. Bioessays 25:1158-1167.
5. Bell SP, Dutta A (2002) DNA replication in eukaryotic cells. Annu Rev Biochem 71:333-374.
6. Bowers JL, Randell JC, Chen S, Bell SP (2004) ATP hydrolysis by ORC catalyzes reiterative Mcm2-7 assembly at a defined origin of replication. Mol Cell 16:967-978.
7. Neuwald AF, Aravind L, Spouge JL, Koonin EV (1999) AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 9:27-43.
8. Tye BK (1999) MCM proteins in DNA replication. Annu Rev Biochem 68:649-686.
9. Kelman Z, Lee JK, Hurwitz J (1999) The single minichromosome maintenance protein of Methanobacterium thermoautotrophicum DeltaH contains DNA helicase activity. Proc Natl Acad Sci USA 96:14783-14788.
10. Chong JP, Hayashi MK, Simon MN, Xu RM, Stillman B (2000) A double-hexamer archaeal minichromosome maintenance protein is an ATP-dependent DNA helicase. Proc Natl Acad Sci USA 97:1530-1535.
11. Fletcher RJ, et al. (2003) The structure and function of MCM from archaeal M. Thermoautotrophicum. Nat Struct Biol 10:160-167.
12. Kelman Z, White MF (2005) Archaeal DNA replication and repair. Curr Opin Microbiol 8:669-676.
13. Liu W, Pucci B, Rossi M, Pisani FM, Ladenstein R (2008) Structural analysis of the Sulfolobus solfataricus MCM protein N-terminal domain. Nucleic Acids Res 36:3235-3243.
14. McGeoch AT, Trakselis MA, Laskey RA, Bell SD (2005) Organization of the archaeal MCM complex on DNA and implications for the helicase mechanism. Nat Struct Mol Biol 12:756-762.
15. Iyer LM, Leipe DD, Koonin EV, Aravind L (2004) Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 146:11-31.
16. Li D, et al. (2003) Structure of the replicative helicase of the oncoprotein SV40 large tumour antigen. Nature 423:512-518.
17. Gai D, Zhao R, Li D, Finkielstein CV, Chen XS (2004) Mechanisms of conformational change for a replicative hexameric helicase of SV40 large tumor antigen. Cell 119:47-60.
18. Ingleston SM, Sharples GJ, Lloyd RG (2000) The acidic pin of RuvA modulates Holliday junction binding and processing by the RuvABC resolvasome. EMBO J 19:6266-6274.
19. Jenkinson ER, Chong JPJ (2006) Minichromosome maintenance helicase activity is controlled by N- and C-terminal motifs and requires the ATPase domain helix-2 insert. Proc Natl Acad Sci USA 103:7613-7618.
20. Gómez-Llorente Y, Fletcher RJ, Chen XS, Carazo JM, San Martín C (2005) Polymorphism and double hexamer structure in the archaeal minichromosome maintenance (MCM) helicase from Methanobacterium thermoautotrophicum. J Biol Chem 280:40909-40915.
21. Costa A, et al. (2006) Structural basis of the Methanothermobacter thermautotrophicus MCM helicase activity. Nucleic Acids Res 34:5829-5838.
22. Barry ER, McGeoch AT, Kelman Z, Bell SD (2007) Archaeal MCM has separable processivity, substrate choice and helicase domains. Nucleic Acids Res 35:988-998.
23. Yamada K, et al. (2002) Crystal structure of the RuvA-RuvB complex: A structural basis for the Holliday junction migrating motor machinery. Mol Cell 10:671-681.
24. Ohnishi T, Hishida T, Harada Y, Iwasaki H, Shinagawa H (2005) Structure-function analysis of the three domains of RuvB DNA motor protein. J Biol Chem 280:30504-30510.
25. Sakakibara N, et al. (2008) Coupling of DNA binding and helicase activity is mediated by a conserved loop in the MCM protein. Nucleic Acids Res 36:1309-1320.
26. Carpentieri F, De Felice M, De Falco M, Rossi M, Pisani FM (2002) Physical and functional interaction between the minichromosome maintenance-like DNA helicase and the single-stranded DNA-binding protein from the crenarchaeon Sulfolobus solfataricus. J Biol Chem 277:12118-12127.
27. Moreau MJ, McGeoch AT, Lowe AR, Itzhaki LS, Bell SD (2007) ATPase site architecture and helicase mechanism of an archaeal MCM. Mol Cell 28:304-314.
28. Pucci B, De Felice M, Rossi M, Onesti S, Pisani FM (2004) Amino acids of the Sulfolobus solfataricus minichromosome maintenance-like DNA helicase involved in DNA binding/remodeling. J Biol Chem 279:49222-49228.
29. Pucci B, et al. (2007) Modular organization of the Sulfolobus solfataricus minichromosome maintenance protein. J Biol Chem 282:12574-12582.
30. Shen J, Gai D, Patrick A, Greenleaf WB, Chen XS (2005) The roles of the residues on the channel β-hairpin and loop structures of simian virus 40 hexameric helicase. Proc Natl Acad Sci USA 102:11248-11253.
31. Takahashi TS, Wigley DB, Walter JC (2005) Pumps, paradoxes and ploughshares: Mechanism of the MCM2-7 DNA helicase. Trends Biochem Sci 30:437-444.
32. Chong JP (2005) Learning to unwind. Nat Struct Mol Biol 12:734-736.
33. Kaplan DL, Davey MJ, 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.
34. Rothenberg E, Trakselis MA, Bell SD, Ha T (2007) MCM forked substrate specificity involves dynamic interaction with the 5′-tail. J Biol Chem 282:34229-34234.
35. Fodje MN, et al. (2001) Interplay between an AAA module and an integrin I domain may regulate the function of magnesium chelatase. J Mol Biol 311:111-122.
36. Liu J, et al. (2000) Structure and function of Cdc6/Cdc18: Implications for origin recognition and checkpoint control. Mol Cell 6:637-648.