Mechano-chemical kinetics of DNA replication: Identification of the translocation step of a replicative DNA polymerase

Nucleic Acids Research

Volumn 43, Issue 7, 2015, Pages 3643-3652

  Morin, José A ^a,f   Cao, Francisco J ^b   Lázaro, José M ^c   Arias Gonzalez, J Ricardo ^d   Valpuesta, José M ^e   Carrascosa, José L ^d,e   Salas, Margarita ^c   Ibarra, Borja ^d  

^a INSTITUTO MADRILEÑO DE ESTUDIOS AVANZADOS EN NANOCIENCIA IMDEA NANOCIENCIA   (Spain)

^b UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d CSIC   (Spain)

^e CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^f MAX PLANCK INSTITUT FÜR PHYSIK KOMPLEXER SYSTEME   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; NUCLEOTIDE; DNA DIRECTED DNA POLYMERASE;

ARTICLE; BACTERIOPHAGE; CATALYSIS; CONCENTRATION (PARAMETERS); DNA REPLICATION; ENZYME BINDING; ENZYME KINETICS; ENZYME MODIFICATION; ENZYME STABILITY; ENZYME TRANSLOCATION; OPTICAL TWEEZERS; PRIORITY JOURNAL; PROTEIN TRANSPORT; THERMAL DIFFUSION; KINETICS; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BACILLUS PHAGE PHI29;

BIOLOGICAL TRANSPORT; DNA REPLICATION; DNA-DIRECTED DNA POLYMERASE; KINETICS;

EID: 84930637595     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv204     Document Type: Article

References (75)

1. Steitz, T.A. and Steitz, J.A. (1993) A general two-metal-ion mechanism for catalytic RNA. Proc. Natl. Acad. Sci. U.S.A., 90, 6498-6502.
2. Nakamura, T., Zhao, Y, Yamagata, Y, Hua, Y-j. and Yang, W. (2012) Watching DNA polymerase r\ make a phosphodiester bond. Nature, 487, 196-201.
3. Kohlstaedt, L., Wang, J., Friedman, J., Rice, P. and Steitz, T. (1992) Crystal structure at 3.5 A resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science, 256, 1783-1790.
4. Steitz, T.A. (2006) Visualizing polynucleotide polymerase machines at work. EMBO J., 25, 3458-3468.
5. Zhang, H., Cao, W., Zakharova, E., Konigsberg, W. and De La Cruz, E.M. (2007) Fluorescence of 2-aminopurine reveals rapid conformational changes in the RB69 DNA polymerase-primer/template complexes upon binding and incorporation of matched deoxynucleoside triphosphates. Nucleic Acids Res., 35, 6052-6062.
6. Wang, W., Wu, EY, Hellinga, H.W. and Beese, L.S. (2012) Structural factors that determine selectivity of a high fdelity DNA polymerase for deoxy-, dideoxy-, and ribonucleotides. J. Biol. Chem., 287, 28215-28226.
7. Berezhna, S.Y, Gill, J.P., Lamichhane, R. and Millar, DP. (2012) Single-molecule Förster resonance energy transfer reveals an innate fdelity checkpoint in DNA polymerase I. J. Am. Chem. Soc. 134, 11261-11268.
8. Hariharan, C, Bloom, L.B., Helquist, S.A., Kool, E.T. and Reha-Krantz, L.J. (2006) Dynamics of nucleotide incorporation: snapshots revealed by 2-aminopurine fuorescence studies. Biochemistry, 45, 2836-2844.
9. Joyce, C.M., Potapova, O., DeLucia, A.M., Huang, X., Basu, V.P. and Grindley, NDF (2008) Fingers-closing and other rapid conformational changes in DNA polymerase I (Klenow fragment) and their role in nucleotide selectivity. Biochemistry, 47, 6103-6116.
10. Vande Berg, B.J., Beard, W.A. and Wilson, S.H. (2001) DNA structure and aspartate 276 infuence nucleotide binding to human DNA polymerase ß: implication for the identity of the rate-limiting conformational change. J. Biol. Chem., 276, 3408-3416.
11. Showalter, A.K. and Tsai, M.-D. (2002) A reexamination of the nucleotide incorporation fdelity of DNA polymerases. Biochemistry, 41, 10571-10576.
12. Shah, A.M., Li, S.-X., Anderson, K.S. and Sweasy, J.B. (2001) Y265H mutator mutant of DNA polymerase ß: proper geometric aligment is critical for fdelity. J. Biol. Chem., 276, 10824-10831.
13. Rothwell, PJ., MitaksovV. and Waksman, G. (2005) Motions of the fngers subdomain of Klentaq1 are fast and not rate limiting: implications for the molecular basis of fdelity in DNA polymerases. Mol. Cell, 19, 345-355.
14. Patel, S.S., Wong, I. and Johnson, K.A. (1991) Pre-steady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease-defcient mutant. Biochemistry, 30, 511-525.
15. Luo, G., Wang, M., Konigsberg, WH. andXie, X.S. (2007) Single-molecule and ensemble fuorescence assays for a functionally important conformational change in T7 DNA polymerase. Proc.Natl Acad. Sci. U.S.A., 104, 12610-12615.
16. Joyce, C.M. and Benkovic, S.J. (2004) DNA polymerase fdelity: kinetics, structure, and checkpointsf. Biochemistry, 43, 14317-14324.
17. Fiala, KA. and Suo, Z. (2004) Mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase IV. Biochemistry, 43, 2116-2125.
18. Cramer, J. andRestle, T. (2005) Pre-steady-state kinetic characterization of the DinB homologue DNA polymerase of Sulfolobus solfataricus. J. Biol. Chem., 280, 40552-40558.
19. Choi, J.-Y and Guengerich, FP (2005) Adduct size limits effcient and error-free bypass across bulky N2-guanine DNA lesions by human DNA polymerase r\. J. Mol. Biol, 352, 72-90.
20. Olsen, T.J., Choi, Y, Sims, PC, Gul, O.T., Corso, B.L., Dong, C, Brown, WA., Collins, PG and Weiss, GA. (2013) Electronic measurements of single-molecule processing by DNA polymerase I (Klenow fragment). J. Am. Chem. Soc, 135, 7855-7860.
21. Rothwell, PJ. and Waksman, G (2005) Structure and mechanism of DNA polymerases. Adv. Protein Chem., 71, 40.
22. Allen, WJ., Rothwell, PJ. and Waksman, G (2008) An intramolecular FRET system monitors fngers subdomain opening in Klentaq1. Protein Sci, 17, 401-408.
23. Johnson, S.J. and Beese, L.S. (2004) Structures of mismatch replication errors observed in a DNA polymerase. Cell, 116, 13.
24. Yin, YW and Steitz, T.A. (2004) The structural mechanism of translocation and helicase activity in T7 RNA polymerase. Cell, 116, 393-404.
25. Golosov, A.A., Warren, J.J., Beese, L.S. and Karplus, M. (2010) The mechanism of the translocation step in DNA replication by DNA polymerase I: a computer simulation analysis. Structure, 18, 83-93.
26. Zhang, C. and Burton, Z.F (2004) Transcription factors IIF and IIS and nucleoside triphosphate substrates as dynamic probes of the human RNA polymerase II mechanism. J. Mol. Biol., 342, 1085-1099.
27. Nedialkov, YA., Gong, X.Q., Hovde, S.L., Yamaguchi, Y, Handa, H., Geiger, J.H., Yan, H. and Burton, Z.F (2003) NTP-driven translocation by human RNA polymerase II. J. Biol. Chem., 278, 18303-18312.
28. Gong, X.Q., Zhang, C, Feig, M. and Burton, Z.F (2005) Dynamic error correction and regulation of downstream bubble opening by human RNA polymerase II. Mol. Cell, 18, 461-470.
29. Guajardo, R. and Sousa, R. (1997) A model for the mechanism of polymerase translocation. J. Mol. Biol, 265, 8-19.
30. Thomen, P, Lopez, PJ. and Heslot, F (2005) Unravelling the mechanism of RNA-polymerase forward motion by using mechanical force. Phys. Rev. Lett., 94, 128102.
31. Larson, M.H., Zhou, J., Kaplan, C.D, Palangat, M., Kornberg, R.D, Landick, R. and Block, S.M. (2012) Trigger loop dynamics mediate the balance between the transcriptional fdelity and speed of RNA polymerase II. Proc. Natl. Acad. Sci. U.S.A., 109, 6555-6560.
32. Bar-Nahum, G, Epshtein, V, Ruckenstein, A.E., Rafkov, R., Mustaev, A. and Nudler, E. (2005) A ratchet mechanism of transcription elongation and its control. Cell, 120, 183-193.
33. Bai, L., Fulbright, R.M. and Wang, M.D (2007) Mechanochemical kinetics of transcription elongation. Phys. Rev. Lett., 98, 068103.
34. Abbondanzieri, E.A., Greenleaf, WJ., Shaevitz, J.W, Landick, R. and Block, S.M. (2005) Direct observation of base-pair stepping by RNA polymerase. Nature, 438, 460-465.
35. Dangkulwanich, M., Ishibashi, T, Liu, S., Kreeva, M.L., Lubkowska, L., Kashlev, M. and Bustamante, C.J. (2013) Complete dissection of transcription elongation reveals slow translocation of RNA polymerase II in a linear ratchet mechanism. eLife, 2, 22.
36. Lieberman, KR., Dahl, J.M., Mai, A.H., Cox, A., Akeson, M. and Wang, H. (2013) Kinetic mechanism of translocation and dNTP binding in individual DNA polymerase complexes. J. Am.Chem. Soc, 135, 9149-9155.
37. Lieberman, KR., Dahl, J.M., Mai, A.H., Akeson, M. and Wang, H. (2012) Dynamics of the translocation step measured in individual DNA polymerase complexes. J. Am. Chem. Soc, 134, 18816-18823.
38. Dahl, J.M., Mai, A.H., Cherf, GM., Jetha, NN, Garalde, DR., Marziali, A., Akeson, M., Wang, H. and Lieberman, KR. (2012) Direct observation of translocation in individual DNA polymerase complexes. J. Biol. Chem., 287, 13407-13421.
39. Blanco, L., Bernad, A., Lazaro, J.M., Martín, G, Garmendia, C. and Salas, M. (1989) Highly effcient DNA synthesis by the phage phi 29 DNA polymerase. Symmetrical mode of DNA replication. J. Biol Chem., 264, 8935-8940.
40. Rodríguez, I., Lazaro, J.M., Blanco, L., Kamtekar, S., Berman, A.J., Wang, J., Steitz, TA., Salas, M. and de Vega, M. (2005) A specifc subdomain in tp29 DNA polymerase confers both processivity and strand-displacement capacity. Proc. Natl. Acad. Sci. U.S.A., 102, 6407-6412.
41. Morin, J.A., Cao, FJ., Valpuesta, J.M., Carrascosa, J.L., Salas, M. and Ibarra, B. (2012) Manipulation of single polymerase-DNA complexes: a mechanical view of DNA unwinding during replication. Cell Cycle, 11, 2967-2968.
42. Morin, J.A., Cao, FJ., Lazaro, J.M., Arias-Gonzalez, J.R., Valpuesta, J.M., Carrascosa, J.L., Salas, M. and Ibarra, B. (2012) Active DNA unwinding dynamics during processive DNA replication. Proc. Natl. Acad. U.S.A., 109, 8115-8120.
43. Ibarra, B., Chemla, YR., Plyasunov, S., Smith, S.B., Lazaro, J.M., Salas, M. and Bustamante, C. (2009) Proofreading dynamics of a processive DNA polymerase. EMBO J., 28, 2794-2802.
44. Bustamante, C, Chemla, YR., Forde, NR. andIzhaky, D. (2004) Mechanical processes in biochemistry. Annu. Rev. Biochem., 73, 705-748.
45. Smith, S.B., Cui, Y and Bustamante, C. (2003) Methods in Enzymology. 361, 134-162.
46. Jahnel, M., Behrndt, M., Jannasch, A., Schäffer, E. and Grill, S.W. (2011) Measuring the complete force feld of an optical trap. Opt. Lett., 36, 1260-1262.
47. Soengas, M.S., Esteban, J.A., Lazaro, J.M., Bernad, A., Blasco, M.A., Salas, M. and Blanco, L. (1992) Site directed mutagenesis at the Exo III motif of $29 DNA polymerase. Overlapping structural domains for the 3'-5' exonuclease and strand displacement activities. EMBO J., 11, 4227-4237.
48. Soengas, M.A.S., Gutierrez, C. and Salas, M. (1995) Helix-destabilizing activity of tp29 single-stranded DNA binding protein: effect on the elongation rate during strand displacement DNA replication. J. Mol Biol, 253, 517-529.
49. De Vega, M., Lázaro, J.M., Salas, M. and Blanco, L. (1996) Primer terminus stabilization at the 3'-5' exonuclease active site of $29 DNA polymerase. EMBO J. 15, 1182-1192.
50. Visscher, K., Schnitzer, M.J. and Block, S.M. (1999) Single kinesin molecules studied with a molecular force clamp. Nature, 400, 184-189.
51. Pandey, M. and Patel, S.S. (2014) Helicase and polymerase move together close to the fork junction and copy DNA in one-nucleotide steps. Cell Rep., 6, 1129-1138.
52. Truniger, V, Lazaro, J.M., Esteban, F.J., Blanco, L. and Salas, M. (2002) A positively charged residue of f29 DNA polymerase, highly conserved in DNA polymerases from families A and B, is involved in binding the incoming nucleotide. Nucleic Acids Res., 30, 1483-1492.
53. Blasco, M.A., Bernad, A., Blanco, L. and Salas, M. (1991) Characterization and mapping of the pyrophosphorolytic activity of the phage phi 29 DNA polymerase. Involvement of amino acid motifs highly conserved in alpha-like DNA polymerases. J. Biol. Chem., 266, 7904-7909.
54. Berman, A.J., Kamtekar, S., Goodman, J.L., Lázaro, J.M., de Vega, M., Blanco, L., Salas, M. and Steitz, T.A. (2007) Structures of phi29 DNA polymerase complexed with substrate: the mechanism of translocation in B family polymerases. EMBO J., 26, 3494-3505.
55. Thomen, P, Lopez, PJ., Bockelmann, U., Guillerez, J., Dreyfus, M. and Heslot, F. (2008) T7 RNA polymerase studied by force measurements varying cofactor concentration. Biophys. J., 95, 2423-2433.
56. Keller, D. and Bustamante, C. (2000) The mechanochemistry of molecular motors. Biophys. J., 78, 541-556.
57. Herbert, K.M., Greenleaf, W.J. and Block, S.M. (2008) Single-molecule studies of RNA polymerase: motoring along. Annu. Rev. Biochem., 77, 149-176.
58. Wong, I., Patel, S.S. and Johnson, K.A. (1991) An induced-ft kinetic mechanism for DNA replication fdelity: direct measurement by single-turnover kinetics. Biochemistry, 30, 526-537.
59. Lowe, L.G and Guengerich, F.P (1996) Steady-state and pre-steady-state kinetic analysis of dNTP insertion opposite 8-oxo-7, 8-dihydroguanine by Escherichia coli polymerases I exo-and II exo-f. Biochemistry, 35, 9840-9849.
60. Kirmizialtin, S., Nguyen, V, Johnson, K.A. and Elber, R. (2012) How conformational dynamics of DNA polymerase select correct substrates: experiments and simulations. Structure, 20, 618-627.
61. Donlin, M.J., Patel, S.S. and Johnson, K.A. (1991) Kinetic partitioning between the exonuclease and polymerase sites in DNA error correction. Biochemistry, 30, 538-546.
62. Li, Y, Korolev, S. and Waksman, G. (1998) Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J., 17, 7514-7525.
63. Lieberman, K.R., Dahl, J.M. andWang, H. (2014) Kinetic mechanism at the branchpoint between the DNA synthesis and editing pathways in individual DNA polymerase complexes. J. Am. Chem. Soc, 136, 7117-7131.
64. Subuddhi, U., Hogg, M. and Reha-Krantz, L.J. (2008) Use of 2-aminopurine fuorescence to study the role of the ß hairpin in the proofreading pathway catalyzed by the Phage T4 and RB69 DNA polymerases. Biochemistry, 47, 6130-6137.
65. Shamoo, Y. and Steitz, T.A. (1999) Building a replisome from interacting pieces: sliding clamp complexed to a peptide from DNA polymerase and a polymerase editing complex. Cell, 99, 155-166.
66. Lamichhane, R., Berezhna, S.Y, Gill, J.P, Van der Schans, E. and Millar, DP (2013) Dynamics of site switching in DNA polymerase. J. Am. Chem. Soc, 135, 4735-4742.
67. Kamtekar, S., Berman, A.J., Wang, J., Lázaro, J.M., de Vega, M., Blanco, L., Salas, M. and Steitz, T.A. (2004) Insights into strand displacement and processivity from the crystal structure of the protein-primed DNA polymerase of bacteriophage tp29. Mol Cell, 16, 609-618.
68. Hogg, M., Wallace, S.S. and Doublié, S. (2004) Crystallographic snapshots of a replicative DNA polymerase encountering an abasic site. EMBO J., 23, 1483-1493.
69. Udo, S. (2012) Stochastic thermodynamics, fuctuation theorems and molecular machines. Rep. Prog. Phys, 75, 126001.
70. Cao, F.J. and Feito, M. (2009) Thermodynamics of feedback controlled systems. Phys. Rev. E, 79, 041118.
71. Cao, F.J., Dinis, L. and Parrondo, J.M.R. (2004) Feedback control in a collective fashing ratchet. Phys. Rev. Lett., 93, 040603.
72. Bier, M. (2007) The stepping motor protein as a feedback control ratchet. Biosystems, 88, 301-307.
73. Astumian, R.D. (1997) Thermodynamics and kinetics of a Brownian motor. Science, 276, 917-922.
74. Komissarova, N and Kashlev, M. (1997) Transcriptional arrest: Escherichia coli RNA polymerase translocates backward, leaving the 3' end of the RNA intact and extruded. Proc. Natl. Acad. Sci. U.S.A., 94, 1755-1760.
75. Brueckner, F. and Cramer, P (2008) Structural basis of transcription inhibition by [alpha]-amanitin and implications for RNA polymerase II translocation. Nat. Struct. Mol Biol, 15, 811-818.