Mechanistic studies of the T4 DNA (gp41) replication helicase: Functional interactions of the C-terminal tails of the helicase subunits with the T4 (gp59) helicase loader protein

Journal of Molecular Biology

Volumn 347, Issue 2, 2005, Pages 257-275

  Delagoutte, Emmanuelle ^a,b   Von Hippel, Peter H ^a  

^a UNIVERSITY OF OREGON   (United States)

^b INSTITUT CURIE   (France)

Author keywords

ATPase; DNA replication complexes; dsDNA unwinding; Functional coupling; Helicases; ssDNA translocation

Indexed keywords

DIMER; DNA BINDING PROTEIN; GLYCOPROTEIN; GLYCOPROTEIN GP 32; GLYCOPROTEIN GP 41; GLYCOPROTEIN GP 59; GLYCOPROTEIN GP 61; HELICASE; MUTANT PROTEIN; PROTEIN SUBUNIT; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; VIRUS DNA;

ARTICLE; BACTERIOPHAGE T4; CARBOXY TERMINAL SEQUENCE; DNA REPLICATION; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME LOCALIZATION; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; WILD TYPE;

EID: 14644411671     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.01.036     Document Type: Article

References (77)

1. B. Alberts The cell as a collection of protein machines: preparing the next generation of molecular biologists Cell 92 1998 291 294
2. E. Delagoutte, and P.H. von Hippel Molecular mechanisms of the functional coupling of the helicase (gp41) and polymerase (gp43) of bacteriophage T4 within the DNA replication fork Biochemistry 40 2001 4459 4477
3. M.C. Young, M.K. Reddy, and P.H. von Hippel Structure and function of the bacteriophage T4 DNA polymerase holoenzyme Biochemistry 31 1992 8675 8690
4. N.G. Nossal Protein-protein interactions at a DNA replication fork: bacteriophage T4 as a model FASEB J. 6 1992 871 878
5. S.J. Benkovic, A.M. Valentine, and F. Salinas Replisome-mediated DNA replication Annu. Rev. Biochem. 70 2001 181 208
6. Newport, J., Kowalczykowski, S., Lonberg, N., Paul, L. & von Hippel, P. (1981). Molecular aspects of the interactions of T4-coded gene 32-protein and DNA polymerase (gene 43-protein) with nucleic acids. In "Mechanistic Studies of DNA Replication and Genetic Recombination". ICN-UCLA Symposia on Molecular and Cellular Biology. XIX, pp. 485-506.
7. K.J. Hacker, and B.M. Alberts The rapid dissociation of the T4 DNA polymerase holoenzyme when stopped by a DNA hairpin helix. A model for polymerase release following the termination of each Okazaki fragment J. Biol. Chem. 269 1994 24221 24228
8. S.C. Alley, V.K. Shier, E. Abel-Santos, D.J. Sexton, P. Soumillion, and S.J. Benkovic Sliding clamp of the bacteriophage T4 polymerase has open and closed subunit interfaces in solution Biochemistry 38 1999 7696 7709
9. M.K. Reddy, S.E. Weitzel, and P.H. von Hippel Assembly of a functional replication complex without ATP hydrolysis: a direct interaction of bacteriophage T4 gp45 with T4 DNA polymerase Proc. Natl Acad. Sci. USA 90 1993 3211 3215
10. B.F. Kaboord, and S.J. Benkovic Rapid assembly of the bacteriophage T4 core replication complex on a linear primer/template construct Proc. Natl Acad. Sci. USA 90 1993 10881 10885
11. T.C. Jarvis, L.S. Paul, and P.H. von Hippel Structural and enzymatic studies of the T4 DNA replication system. I. Physical characterization of the polymerase accessory protein complex J. Biol. Chem. 264 1989 12709 12716
12. T.C. Jarvis, L.S. Paul, J.W. Hockensmith, and P.H. von Hippel Structural and enzymatic studies of the T4 DNA replication system. II. ATPase properties of the polymerase accessory protein complex J. Biol. Chem. 264 1989 12717 12729
13. T.C. Jarvis, J.W. Newport, and P.H. von Hippel Stimulation of the processivity of the DNA polymerase of bacteriophage T4 by the polymerase accessory proteins. The role of ATP hydrolysis J. Biol. Chem. 266 1991 1830 1840
14. G.J. Latham, P. Pietroni, F. Dong, M.C. Young, and P.H. von Hippel Fluorescence monitoring of T4 polymerase holoenzyme accessory protein interactions during loading of the sliding clamp onto the template-primer junction J. Mol. Biol. 264 1996 426 439
15. G.J. Latham, F. Dong, P. Pietroni, J.M. Dozono, D.J. Bacheller, and P.H. von Hippel Opening of a monomer-monomer interface of the trimeric bacteriophage T4- coded GP45 sliding clamp is required for clamp loading onto DNA Proc. Natl Acad. Sci. USA 96 1999 12448 12453
16. P. Pietroni, M.C. Young, G.J. Latham, and P.H. von Hippel Structural analyses of gp45 sliding clamp interactions during assembly of the bacteriophage T4 DNA polymerase holoenzyme. I. Conformational changes within the gp44/62-gp45-ATP complex during clamp loading J. Biol. Chem. 272 1997 31666 31676
17. D.J. Sexton, T.E. Carver, A.J. Berdis, and S.J. Benkovic Protein-protein and protein-DNA interactions at the bacteriophage T4 DNA replication fork. Characterization of a fluorescently labeled DNA polymerase sliding clamp J. Biol. Chem. 271 1996 28045 28051
18. P. Pietroni, M.C. Young, G.J. Latham, and P.H. von Hippel Dissection of the ATP-driven reaction cycle of the bacteriophage T4 DNA replication processivity clamp loading system J. Mol. Biol. 309 2001 869 891
19. M.A. Trakselis, R.M. Roccasecca, J. Yang, A.M. Valentine, and S.J. Benkovic Dissociative properties of the proteins within the bacteriophage T4 replisome J. Biol. Chem. 278 2003 49839 49849
20. F.A. Kadyrov, and J.W. Drake Conditional coupling of leading-strand and lagging-strand dna synthesis at bacteriophage t4 replication forks J. Biol. Chem. 276 2001 29559 29566
21. J. Yang, Z. Zhuang, R.M. Roccasecca, M.A. Trakselis, and S.J. Benkovic From the cover: the dynamic processivity of the T4 DNA polymerase during replication Proc. Natl Acad. Sci. USA 101 2004 8289 8294
22. M. Venkatesan, L.L. Silver, and N.G. Nossal Bacteriophage T4 gene 41 protein, required for the synthesis of RNA primers, is also a DNA helicase J. Biol. Chem. 257 1982 12426 12434
23. R.W. Richardson, and N.G. Nossal Characterization of the bacteriophage T4 gene 41 DNA helicase J. Biol. Chem. 264 1989 4725 4731
24. C.C. Liu, and B.M. Alberts Characterization of the DNA-dependent GTPase activity of T4 gene 41 protein, an essential component of the T4 bacteriophage DNA replication apparatus J. Biol. Chem. 256 1981 2813 2820
25. F. Dong, E.P. Gogol, and P.H. von Hippel The phage T4-coded DNA replication helicase (gp41) forms a hexamer upon activation by nucleoside triphosphate J. Biol. Chem. 270 1995 7462 7473
26. M.C. Young, D.E. Schultz, D. Ring, and P.H. von Hippel Kinetic parameters of the translocation of bacteriophage T4 gene 41 protein helicase on single-stranded DNA J. Mol. Biol. 235 1994 1447 1458
27. X. Yu, M.M. Hingorani, S.S. Patel, and E.H. Egelman DNA is bound within the central hole to one or two of the six subunits of the T7 DNA helicase [letter] Nature Struct. Biol. 3 1996 740 743
28. D.L. Kaplan The 3′-tail of a forked-duplex sterically determines whether one or two DNA strands pass through the central channel of a replication-fork helicase J. Mol. Biol. 301 2000 285 299
29. C.C. Liu, and B.M. Alberts Pentaribonucleotides of mixed sequence are synthesized and efficiently prime de novo DNA chain starts in the T4 bacteriophage DNA replication system Proc. Natl Acad. Sci. USA 77 1980 5698 5702
30. C.C. Liu, and B.M. Alberts Characterization of RNA primer synthesis in the T4 bacteriophage in vitro DNA replication system J. Biol. Chem. 256 1981 2821 2829
31. T.A. Cha, and B.M. Alberts Studies of the DNA helicase-RNA primase unit from bacteriophage T4. A trinucleotide sequence on the DNA template starts RNA primer synthesis J. Biol. Chem. 261 1986 7001 7010
32. D.M. Hinton, and N.G. Nossal Bacteriophage T4 DNA primase-helicase. Characterization of oligomer synthesis by T4 61 protein alone and in conjunction with T4 41 protein J. Biol. Chem. 262 1987 10873 10878
33. N.G. Nossal, and D.M. Hinton Bacteriophage T4 DNA primase-helicase. Characterization of the DNA synthesis primed by T4 61 protein in the absence of T4 41 protein J. Biol. Chem. 262 1987 10879 10885
34. F. Dong, and P.H. von Hippel The ATP-activated hexameric helicase of bacteriophage T4 (gp41) forms a stable primosome with a single subunit of T4-coded primase (gp61) J. Biol. Chem. 271 1996 19625 19631
35. D.H. Jing, F. Dong, G.J. Latham, and P.H. von Hippel Interactions of bacteriophage T4-coded primase (gp61) with the T4 replication helicase (gp41) and DNA in primosome formation J. Biol. Chem. 274 1999 27287 27298
36. S.C. Kowalczykowski, N. Lonberg, J.W. Newport, and P.H. von Hippel Interactions of bacteriophage T4-coded gene 32 protein with nucleic acids. I. Characterization of the binding interactions J. Mol. Biol. 145 1981 75 104
37. J.A. Huberman, A. Kornberg, and B.M. Alberts Stimulation of T4 bacteriophage DNA polymerase by the protein product of T4 gene 32 J. Mol. Biol. 62 1971 39 52
38. T.A. Cha, and B.M. Alberts Effects of the bacteriophage T4 gene 41 and gene 32 proteins on RNA primer synthesis: coupling of leading- and lagging-strand DNA synthesis at a replication fork Biochemistry 29 1990 1791 1798
39. D.P. Giedroc, R. Khan, and K. Barnhart Overexpression, purification, and characterization of recombinant T4 gene 32 protein22-301 (g32P-B) J. Biol. Chem. 265 1990 11444 11455
40. Y. Shamoo, A.M. Friedman, M.R. Parsons, W.H. Konigsberg, and T.A. Steitz Crystal structure of a replication fork single-stranded DNA binding protein (T4 gp32) complexed to DNA [published erratum appears in Nature 1995 Aug 17;376(6541):616] Nature 376 1995 362 366
41. R.L. Burke, B.M. Alberts, and J. Hosoda Proteolytic removal of the COOH terminus of the T4 gene 32 helix-destabilizing protein alters the T4 in vitro replication complex J. Biol. Chem. 255 1980 11484 11493
42. K.N. Kreuzer Recombination-dependent DNA replication in phage T4 Trends Biochem. Sci. 25 2000 165 173
43. C.E. Jones, T.C. Mueser, K.C. Dudas, K.N. Kreuzer, and N.G. Nossal Bacteriophage T4 gene 41 helicase and gene 59 helicase-loading protein: a versatile couple with roles in replication and recombination Proc. Natl Acad. Sci. USA 98 2001 8312 8318
44. C.E. Jones, T.C. Mueser, and N.G. Nossal Bacteriophage T4 32 protein is required for helicase-dependent leading strand synthesis when the helicase is loaded by the T4 59 helicase-loading protein J. Biol. Chem. 279 2004 12067 12075
45. P.D. Chastain II, A.M. Makhov, N.G. Nossal, and J. Griffith Architecture of the replication complex and DNA loops at the fork generated by the bacteriophage t4 proteins J. Biol. Chem. 278 2003 21276 21285
46. Y. Ma, T. Wang, J.L. Villemain, D.P. Giedroc, and S.W. Morrical Dual functions of single-stranded DNA-binding protein in helicase loading at the bacteriophage T4 DNA replication fork J. Biol. Chem. 279 2004 19035 19045
47. K.D. Raney, T.E. Carver, and S.J. Benkovic Stoichiometry and DNA unwinding by the bacteriophage T4 41: 59 helicase J. Biol. Chem. 271 1996 14074 14081
48. F.T. Ishmael, S.C. Alley, and S.J. Benkovic Assembly of the bacteriophage T4 helicase. Architecture and stoichiometry of the gp41-gp59 complex J. Biol. Chem. 277 2002 20555 20562
49. C.E. Jones, T.C. Mueser, and N.G. Nossal Interaction of the bacteriophage T4 gene 59 helicase loading protein and gene 41 helicase with each other and with fork, flap, and cruciform DNA J. Biol. Chem. 275 2000 27145 27154
50. S.W. Morrical, H.T.H. Beernink, A. Dash, and K. Hempstead The gene 59 protein of bacteriophage T4. Characterization of protein-protein interactions with gene 32 protein, the T4 single-stranded DNA binding protein J. Biol. Chem. 271 1996 20198 20207
51. S.W. Morrical, K. Hempstead, and M.D. Morrical The gene 59 protein of bacteriophage T4 modulates the intrinsic and single-stranded DNA-stimulated ATPase activities of gene 41 protein, the T4 replicative DNA helicase J. Biol. Chem. 269 1994 33069 33081
52. J. Barry, and B. Alberts Purification and characterization of bacteriophage T4 gene 59 protein. A DNA helicase assembly protein involved in DNA replication J. Biol. Chem. 269 1994 33049 33062
53. T.C. Mueser, C.E. Jones, N.G. Nossal, and C.C. Hyde Bacteriophage T4 gene 59 helicase assembly protein binds replication fork DNA. The 1.45 A resolution crystal structure reveals a novel alpha- helical two-domain fold [In Process Citation] J. Mol. Biol. 296 2000 597 612
54. Lakowicz, J. R. (1999). Principles of fluorescence spectroscopy. Second Edition. Fluorescence anisotropy; Chapter 10, 291-319.
55. Cantor, C. R. & Schimmel, P. R. (1980). Biophysical chemistry. Part II: Techniques for the study of biological structure and function. Chapter 8: Other optical techniques, 409-480.
56. D.E. Jensen, R.C. Kelly, and P.H. von Hippel DNA "melting" proteins. II. Effects of bacteriophage T4 gene 32-protein binding on the conformation and stability of nucleic acid structures J. Biol. Chem. 251 1976 7215 7228
57. M.R. Singleton, M.R. Sawaya, T. Ellenberger, and D.B. Wigley Crystal structure of T7 gene 4 ring helicase indicates a mechanism for sequential hydrolysis of nucleotides Cell 101 2000 589 600
58. E. Delagoutte, and P.H. von Hippel Helicase mechanism and the coupling of helicases within macromolecular machines. Part II: integration of helicases into cellular processes Quat. Rev. Biophys. 36 2003 1 69
59. C.A. Gross, C. Chan, A. Dombroski, T. Gruber, M. Sharp, J. Tupy, and B. Young The functional and regulatory roles of sigma factors in transcription Cold Spring Harb. Symp. Quant. Biol. 63 1998 141 155
60. B.A. Young, T.M. Gruber, and C.A. Gross Views of transcription initiation Cell 109 2002 417 420
61. S. Callaci, E. Heyduk, and T. Heyduk Core RNA polymerase from E. coli induces a major change in the domain arrangement of the sigma 70 subunit Mol. Cell 3 1999 229 238
62. T.M. Gruber, D. Markov, M.M. Sharp, B.A. Young, C.Z. Lu, and H.J. Zhong Binding of the initiation factor sigma(70) to core RNA polymerase is a multistep process Mol. Cell 8 2001 21 31
63. B.A. Young, L.C. Anthony, T.M. Gruber, T.M. Arthur, E. Heyduk, and C.Z. Lu A coiled-coil from the RNA polymerase beta′ subunit allosterically induces selective nontemplate strand binding by sigma(70) Cell 105 2001 935 944
64. E.A. Campbell, O. Muzzin, M. Chlenov, J.L. Sun, C.A. Olson, and O. Weinman Structure of the bacterial RNA polymerase promoter specificity sigma subunit Mol. Cell 9 2002 527 539
65. K. Kuznedelov, L. Minakhin, A. Niedziela-Majka, S.L. Dove, D. Rogulja, and B.E. Nickels A role for interaction of the RNA polymerase flap domain with the sigma subunit in promoter recognition Science 295 2002 855 857
66. K.S. Murakami, S. Masuda, E.A. Campbell, O. Muzzin, and S.A. Darst Structural basis of transcription initiation: an RNA polymerase holoenzyme-DNA complex Science 296 2002 1285 1290
67. K.S. Murakami, S. Masuda, and S.A. Darst Structural basis of transcription initiation: RNA polymerase holoenzyme at 4 A resolution Science 296 2002 1280 1284
68. K. Geszvain, T.M. Gruber, R.A. Mooney, C.A. Gross, and R. Landick A hydrophobic patch on the flap-tip helix of E.coli RNA polymerase mediates sigma(70) region 4 function J. Mol. Biol. 343 2004 569 587
69. E. Skordalakes, and J.M. Berger Structure of the Rho transcription terminator: mechanism of mRNA recognition and helicase loading Cell 114 2003 135 146
70. J.P. Richardson Loading rho to terminate transcription Cell 114 2003 157 159
71. C.F. Morris, H. Hama-Inaba, D. Mace, N.K. Sinha, and B. Alberts Purification of the gene 43, 44, 45, and 62 proteins of the bacteriophage T4 DNA replication apparatus J. Biol. Chem. 254 1979 6787 6796
72. D.M. Hinton, L.L. Silver, and N.G. Nossal Bacteriophage T4 DNA replication protein 41. Cloning of the gene and purification of the expressed protein J. Biol. Chem. 260 1985 12851 12857
73. R.W. Richardson, and N.G. Nossal Trypsin cleavage in the COOH terminus of the bacteriophage T4 gene 41 DNA helicase alters the primase-helicase activities of the T4 replication complex in vitro J. Biol. Chem. 264 1989 4732 4739
74. T. Maniatis, E.F. Fritsch, and J. Sambrook Molecular Cloning: A Laboratory Manual; Kinase Reaction 1989 Book 1, chapt. 5, 5.68-5.71
75. T. Maniatis, E.F. Fritsch, and J. Sambrook Molecular Cloning: A Laboratory Manual; M13mp18 Propagation 1989 Book 1, chapt. 4, 4.21-4.32
76. K.E. van Holde, and W.O. Weischet Boundary analysis of sedimentationvelocity experiments with monodisperse and paucidisperse solutes Biopolymers 17 1978 1387 1403
77. P. Schuck Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling Biophys. J. 78 2000 1606 1619