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Structural analysis of the inactive state of the Escherichia coli DNA polymerase clamp-loader complex.

Kazmirski SL, Podobnik M, Weitze TF, O'Donnell M, Kuriyan J
Proc Natl Acad Sci U S A 101 16750-5 (2004)
Cited: 44 times
EuropePMC logo PMID: 15556993

Abstract

Clamp-loader complexes are heteropentameric AAA+ ATPases that load sliding clamps onto DNA. The structure of the nucleotide-free Escherichia coli clamp loader had been determined previously and led to the proposal that the clamp-loader cycles between an inactive state, in which the ATPase domains form a closed ring, and an active state that opens up to form a "C" shape. The crystal structure was interpreted as being closer to the active state than the inactive state. The crystal structure of a nucleotide-bound eukaryotic clamp loader [replication factor C (RFC)] revealed a different and more tightly packed spiral organization of the ATPase domains, raising questions about the significance of the conformation seen earlier for the bacterial clamp loader. We describe crystal structures of the E. coli clamp-loader complex bound to the ATP analog ATPgammaS (at a resolution of 3.5 A) and ADP (at a resolution of 4.1 A). These structures are similar to that of the nucleotide-free clamp-loader complex. Only two of the three functional ATP-binding sites are occupied by ATPgammaS or ADP in these structures, and the bound nucleotides make no interfacial contacts in the complex. These results, along with data from isothermal titration calorimetry, molecular dynamics simulations, and comparison with the RFC structure, suggest that the more open form of the E. coli clamp loader described earlier and in the present work corresponds to a stable inactive state of the clamp loader in which the ATPase domains are prevented from engaging the clamp in the highly cooperative manner seen in the fully ATP-loaded RFC-clamp structure.

Articles - 1xxi mentioned but not cited (6)

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  3. Structural analysis of the inactive state of the Escherichia coli DNA polymerase clamp-loader complex. Kazmirski SL, Podobnik M, Weitze TF, O'Donnell M, Kuriyan J. Proc Natl Acad Sci U S A 101 16750-16755 (2004)
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Reviews citing this publication (11)

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  2. DNA replicases from a bacterial perspective. McHenry CS. Annu Rev Biochem 80 403-436 (2011)
  3. Replication clamps and clamp loaders. Hedglin M, Kumar R, Benkovic SJ. Cold Spring Harb Perspect Biol 5 a010165 (2013)
  4. Architecture and conservation of the bacterial DNA replication machinery, an underexploited drug target. Robinson A, Causer RJ, Dixon NE. Curr Drug Targets 13 352-372 (2012)
  5. Loading clamps for DNA replication and repair. Bloom LB. DNA Repair (Amst) 8 570-578 (2009)
  6. Review: The lord of the rings: Structure and mechanism of the sliding clamp loader. Kelch BA. Biopolymers 105 532-546 (2016)
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  9. Dynamics of loading the Escherichia coli DNA polymerase processivity clamp. Bloom LB. Crit Rev Biochem Mol Biol 41 179-208 (2006)
  10. A structural view of bacterial DNA replication. Oakley AJ. Protein Sci 28 990-1004 (2019)
  11. Assessing heterogeneity in oligomeric AAA+ machines. Sysoeva TA. Cell Mol Life Sci 74 1001-1018 (2017)

Articles citing this publication (27)

  1. Stoichiometry and architecture of active DNA replication machinery in Escherichia coli. Reyes-Lamothe R, Sherratt DJ, Leake MC. Science 328 498-501 (2010)
  2. The mechanism of ATP-dependent primer-template recognition by a clamp loader complex. Simonetta KR, Kazmirski SL, Goedken ER, Cantor AJ, Kelch BA, McNally R, Seyedin SN, Makino DL, O'Donnell M, Kuriyan J. Cell 137 659-671 (2009)
  3. Open clamp structure in the clamp-loading complex visualized by electron microscopic image analysis. Miyata T, Suzuki H, Oyama T, Mayanagi K, Ishino Y, Morikawa K. Proc Natl Acad Sci U S A 102 13795-13800 (2005)
  4. Analysis of the role of PCNA-DNA contacts during clamp loading. McNally R, Bowman GD, Goedken ER, O'Donnell M, Kuriyan J. BMC Struct Biol 10 3 (2010)
  5. Clamp loader ATPases and the evolution of DNA replication machinery. Kelch BA, Makino DL, O'Donnell M, Kuriyan J. BMC Biol 10 34 (2012)
  6. The replication factor C clamp loader requires arginine finger sensors to drive DNA binding and proliferating cell nuclear antigen loading. Johnson A, Yao NY, Bowman GD, Kuriyan J, O'Donnell M. J Biol Chem 281 35531-35543 (2006)
  7. Out-of-plane motions in open sliding clamps: molecular dynamics simulations of eukaryotic and archaeal proliferating cell nuclear antigen. Kazmirski SL, Zhao Y, Bowman GD, O'donnell M, Kuriyan J. Proc Natl Acad Sci U S A 102 13801-13806 (2005)
  8. Human mitochondrial mTERF wraps around DNA through a left-handed superhelical tandem repeat. Jiménez-Menéndez N, Fernández-Millán P, Rubio-Cosials A, Arnan C, Montoya J, Jacobs HT, Bernadó P, Coll M, Usón I, Solà M. Nat Struct Mol Biol 17 891-893 (2010)
  9. Structure of the active form of human origin recognition complex and its ATPase motor module. Tocilj A, On KF, Yuan Z, Sun J, Elkayam E, Li H, Stillman B, Joshua-Tor L. Elife 6 e20818 (2017)
  10. Mapping the interaction of DNA with the Escherichia coli DNA polymerase clamp loader complex. Goedken ER, Kazmirski SL, Bowman GD, O'Donnell M, Kuriyan J. Nat Struct Mol Biol 12 183-190 (2005)
  11. Isomeric control of protein recognition with amino acid- and dipeptide-functionalized gold nanoparticles. You CC, Agasti SS, Rotello VM. Chemistry 14 143-150 (2008)
  12. A slow ATP-induced conformational change limits the rate of DNA binding but not the rate of beta clamp binding by the escherichia coli gamma complex clamp loader. Thompson JA, Paschall CO, O'Donnell M, Bloom LB. J Biol Chem 284 32147-32157 (2009)
  13. Solution structure of Domains IVa and V of the tau subunit of Escherichia coli DNA polymerase III and interaction with the alpha subunit. Su XC, Jergic S, Keniry MA, Dixon NE, Otting G. Nucleic Acids Res 35 2825-2832 (2007)
  14. Structure of the human clamp loader reveals an autoinhibited conformation of a substrate-bound AAA+ switch. Gaubitz C, Liu X, Magrino J, Stone NP, Landeck J, Hedglin M, Kelch BA. Proc Natl Acad Sci U S A 117 23571-23580 (2020)
  15. Structure and biochemical activities of Escherichia coli MgsA. Page AN, George NP, Marceau AH, Cox MM, Keck JL. J Biol Chem 286 12075-12085 (2011)
  16. Studying protein complexes by the yeast two-hybrid system. Rajagopala SV, Sikorski P, Caufield JH, Tovchigrechko A, Uetz P. Methods 58 392-399 (2012)
  17. Structure of the 12-subunit RNA polymerase II refined with the aid of anomalous diffraction data. Meyer PA, Ye P, Suh MH, Zhang M, Fu J. J Biol Chem 284 12933-12939 (2009)
  18. The CHAIN program: forging evolutionary links to underlying mechanisms. Neuwald AF. Trends Biochem Sci 32 487-493 (2007)
  19. Dynamics of Open DNA Sliding Clamps. Oakley AJ. PLoS One 11 e0154899 (2016)
  20. Insights into the structure and assembly of the Bacillus subtilis clamp-loader complex and its interaction with the replicative helicase. Afonso JP, Chintakayala K, Suwannachart C, Sedelnikova S, Giles K, Hoyes JB, Soultanas P, Rafferty JB, Oldham NJ. Nucleic Acids Res 41 5115-5126 (2013)
  21. Structure of the large terminase from a hyperthermophilic virus reveals a unique mechanism for oligomerization and ATP hydrolysis. Xu RG, Jenkins HT, Antson AA, Greive SJ. Nucleic Acids Res 45 13029-13042 (2017)
  22. Dynamics of the E. coli β-Clamp Dimer Interface and Its Influence on DNA Loading. Koleva BN, Gokcan H, Rizzo AA, Lim S, Jeanne Dit Fouque K, Choy A, Liriano ML, Fernandez-Lima F, Korzhnev DM, Cisneros GA, Beuning PJ. Biophys J 117 587-601 (2019)
  23. Comment Low-resolution crystallography is coming of age. Brunger AT. Structure 13 171-172 (2005)
  24. Hypothesis: bacterial clamp loader ATPase activation through DNA-dependent repositioning of the catalytic base and of a trans-acting catalytic threonine. Neuwald AF. Nucleic Acids Res 34 5280-5290 (2006)
  25. Solution study of the Escherichia coli DNA polymerase III clamp loader reveals the location of the dynamic ψχ heterodimer. Tondnevis F, Gillilan RE, Bloom LB, McKenna R. Struct Dyn 2 054701 (2015)
  26. Solution structure of an "open" E. coli Pol III clamp loader sliding clamp complex. Tondnevis F, Weiss TM, Matsui T, Bloom LB, McKenna R. J Struct Biol 194 272-281 (2016)
  27. Bacteriophage Twort protein Gp168 is a β-clamp inhibitor by occupying the DNA sliding channel. Liu B, Li S, Liu Y, Chen H, Hu Z, Wang Z, Zhao Y, Zhang L, Ma B, Wang H, Matthews S, Wang Y, Zhang K. Nucleic Acids Res 49 11367-11378 (2021)


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