Molecular modeling and functional characterization of the monomeric primase-polymerase domain from the Sulfolobus solfataricus plasmid pIT3

FEBS Journal

Volumn 275, Issue 17, 2008, Pages 4389-4402

  Prato, Santina ^a   Vitale, Rosa Maria ^b   Contursi, Patrizia ^a   Lipps, Georg ^c   Saviano, Michele ^d   Rossi, Mosé ^a,e   Bartolucci, Simonetta ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CNR Consiglio Nazionale delle Ricerche   (Italy)

^c UNIVERSITY OF BAYREUTH   (Germany)

^d CNR   (Italy)

^e INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

DNA replication; pIT3 plasmid; Primase polymerase domain; Sulfolobus; Terminal transferase

Indexed keywords

BACTERIAL ENZYME; DEOXYRIBONUCLEOTIDE; DIVALENT CATION; DNA; NUCLEIC ACID; NUCLEOTIDYLTRANSFERASE; OLIGONUCLEOTIDE; POLYMERASE; PRIMASE; RIBONUCLEOTIDE; RNA; TRANSFERASE;

ARTICLE; BACTERIAL STRAIN; BIOCHEMISTRY; COMPARATIVE STUDY; CONTROLLED STUDY; CRYSTALLOGRAPHY; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME STRUCTURE; ESCHERICHIA COLI; KNOWLEDGE; MOLECULAR DYNAMICS; MOLECULAR MODEL; NONHUMAN; NUCLEIC ACID SYNTHESIS; PH; PLASMID; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; RNA SYNTHESIS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; SULFOLOBUS SOLFATARICUS; TEMPERATURE;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA PRIMASE; DNA PRIMERS; DNA-DIRECTED DNA POLYMERASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLASMIDS; SEQUENCE HOMOLOGY, AMINO ACID; SULFOLOBUS SOLFATARICUS;

ARCHAEA; CRENARCHAEOTA; ESCHERICHIA COLI; SULFOLOBUS; SULFOLOBUS SOLFATARICUS;

EID: 49349086610     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2008.06585.x     Document Type: Article

References (44)

1. Kornberg A Baker TA (1992) DNA Replication. Freeman, New York.
2. Frick DN Richardson CC (2001) DNA primases. Annu Rev Biochem 70, 39 80.
3. Myllykallio H, Lopez P, Lopez-Garcia P, Heilig R, Saurin W, Zivanovic Y, Philippe H Forterre P (2000) Bacterial mode of replication with eukaryotic-like machinery in a hyperthermophilic archaeon. Science 288, 2212 2215.
4. Kelman Z White MF (2005) Archaeal DNA replication and repair. Curr Opin Microbiol 8, 669 676.
5. Dionne I, Robinson NP, McGeoch AT, Marsh VL, Reddish A Bell SD (2003) DNA replication in the hyperthermophilic archaeon Sulfolobus solfataricus. Biochem Soc Trans 3, 674 676.
6. Barry ER Bell SD (2006) DNA replication in the Archaea. Microbiol Mol Biol Rev 4, 876 887.
7. De Falco M, Fusco A, De Felice M, Rossi M Pisani FM (2004) The DNA primase of Sulfolobus solfataricus is activated by substrates containing a thymine-rich bubble and has a 3′-terminal nucleotidyl-transferase activity. Nucleic Acids Res 32, 5223 5230.
8. Lao-Sirieix SH Bell SD (2004) The heterodimeric primase of the hyperthermophilic archaeon Sulfolobus solfataricus possesses DNA and RNA primase, polymerase and 3′-terminal nucleotidyl transferase activities. J Mol Biol 344, 1251 1263.
9. Bocquier AA, Liu L, Cann IK, Komori K, Kodha D Ishino Y (2001) Archaeal primase: bridging the gap between RNA and DNA polymerases. Curr Biol 11, 452 456.
10. Liu L, Komori K, Ishino S, Bocquier AA, Cann IK, Kodha D Ishino Y (2001) The archaeal DNA primase: biochemical characterisation of the p41-p46 complex from Pyrococcus furiosus. J Biol Chem 276, 45484 45490.
11. Iyer LM, Koonin EV, Leipe DD 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.
12. Lipps G, Rother S, Hartl C Krauss GA (2003) A novel type of replicative enzyme harbouring ATPase, primase and DNA polymerase activity. EMBO J 22, 2516 2535.
13. Lipps G, Weinzierl AO, von Scheven G, Buchen C Cramer P (2004) Structure of a bifunctional DNA primase-polymerase. Nat Struct Mol Biol 11, 157 162.
14. Augustin MA, Huber R Kaiser JT (2001) Crystal structure of a DNA-dependent RNA polymerase (DNA primase). Nat Struct Biol 8, 57 61.
15. Lao-Sirieix SH, Nookala RK, Roversi P, Bell SD Pellegrini L (2005) Structure of the heterodimeric core primase. Nat Struct Mol Biol 12, 1137 1144.
16. Ito N, Matsui I Matsui E (2007) Molecular basis for the subunit assembly of the primase from an archaeon Pyrococcus horikoshii. FEBS J 274, 1340 1351.
17. Steitz TA, Smerdon SJ, Jager J Joyce CM (1994) A unified polymerase mechanism for nonhomologous DNA and RNA polymerases. Science 266, 2022 2025.
18. Prato S, Cannio R, Klenk H-P, Contursi P, Rossi M Bartolucci S (2006) pIT3, a cryptic plasmid isolated from the hyperthermophilic crenarchaeon Sulfolobus solfataricus IT3. Plasmid 56, 35 45.
19. Delarue M, Pock V, Tordo N, Moras D Argos P (1990) An attempt to unify the structure of polymerase. Protein Eng 3, 461 467.
20. Braithwaite DK Ito J (1993) Compilation, alignment, and phylogenetic relationships of DNA polymerases. Nucleic Acids Res 21, 787 802.
21. Delarue M, Boulé JB, Lescar J, Expert-Benzaçon N, Jourdan N, Sukumar N, Rougeon F Papanicolaou C (2002) Crystal structures of a template-independent DNA polymerase: murine terminal deoxynucleotidyltransferase. EMBO J 21, 427 439.
22. Yang B, Gathy KN Coleman MS (1994) Mutational analysis of residues in the nucleotide binding domain of human terminal deoxynucleotidyl transferase. J Biol Chem 269, 11859 11868.
23. Lao-Sirieix SH, Pellegrini L Bell SD (2005) The promiscuous primase. Trends Genet 21, 568 572.
24. Pan H Wigley DB (2000) Structure of the zinc-binding domain of Bacillus stearothermophilus DNA primase. Structure 3, 231 239.
25. 2+ and deoxynucleoside monophosphate incorporation into transcripts. Biochemistry 44, 13718 13728.
26. Gabbara S Peliska JA (1996) Catalytic activities associated with retroviral and viral polymerases. Methods Enzymol 275, 276 310.
27. Trent JD, Gabrielsen M, Jensen B, Neuhard J Olsen J (1994) Acquired thermotolerance and heat shock proteins in thermophiles from the three phylogenetic domains. J Bacteriol 176, 6148 6152.
28. Arezi B Kuchta RD (2000) Eukaryotic DNA primase. Trends Biochem Sci 25, 572 576.
29. Garcia-Diaz M, Dominguez O, Lopez-Fernandez LA, de Lera LT, Saniger ML, Ruiz JF, Parraga M, Garcïa-Ortiz MJ, Kirchhoff T, del Mazo J et al. (2000) DNA polymerase lambda (Pol lambda), a novel eukaryotic DNA polymerase with a potential role in meiosis. J Mol Biol 301, 851 867.
30. Dominguez O, Ruiz JF, Lain de Lera T, Garcia-Diaz M, Gonzalez MA, Kirchhoff T, Martinez AC, Bernad A 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.
31. Ramadan K, Maga G, Shevelev IV, Villani G, Blanco L Hubscher U (2003) Human DNA polymerase lambda possesses terminal deoxyribonucleotidyl transferase activity and can elongate RNA primers: implications for novel functions. J Mol Biol 328, 63 72.
32. Ramadan K, Shevelev IV, Maga G Hubscher U (2004) De novo DNA synthesis by human DNA polymerase λ, DNA polymerase λ and terminal deoxyribonucleotidyl transferase. J Mol Biol 339, 395 404.
33. Ruiz JF, Juárez R, García-Díaz M, Terrados G, Picher AJ, González-Barrera S, Fernández de Henestrosa AR Blanco L (2003) Lack of sugar discrimination by human Pol mu requires a single glycine residue. Nucleic Acids Res 31, 4441 4449.
34. Boule' J-B, Rougeon F Papanicolaou C (2001) Terminal deoxynucleotidyl transferase indiscriminately incorporates ribonucleotides and deoxyribonucleotides. J Biol Chem 276, 31388 31393.
35. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25, 3389 3402.
36. Shi J, Blundell TL Mizuguchi K (2001) FUGUE: sequence-structure homology recognition using environment-specific substitution tables and structure-dependent gap penalties. J Mol Biol 310, 243 257.
37. Thompson JD, Higgins DG Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22, 4673 4680.
38. Rost B, Yachdav G Liu J (2003) In the Predict Protein: the Predict Protein Server. Nucleic Acids Res 32 (Web Server issue W321 W326.
39. Sali A Blundell TJ (1993) Comparative protein modeling by satisfaction of spatial restraints. J Mol Biol 234, 779 815.
40. Laskowski RA, MacArthur MW, Moss DS Thornton JM (1993) PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr 26, 283 291.
41. Case DA, Darden TA, Cheatham TE, Simmerling CL, Wang J, Duke RE, Luo R, Merz KM, Wang B, Pearlman DA et al. (2004) AMBER 8. University of California, San Francisco.
42. Wang J, Cieplak P Kollman PA (2000) How well does a restrained electrostatic potential (RESP) model perform in calculating conformational energies of organic and biological molecules? J Omput Chem 21, 1049 1074.
43. Ryckaert J-P, Ciccotti G Berendsen HJC (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Computat Phys 23, 327 341.
44. Koradi R, Billeter M Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. Mol Graphics 14, 51 55.