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Structural evidence for the roles of divalent cations in actin polymerization and activation of ATP hydrolysis.

Scipion CPM, Ghoshdastider U, Ferrer FJ, Yuen TY, Wongsantichon J, Robinson RC
Proc Natl Acad Sci U S A 115 10345-10350 (2018)
Cited: 13 times
EuropePMC logo PMID: 30254171

Abstract

The structure of the actin filament is known at a resolution that has allowed the architecture of protein components to be unambiguously assigned. However, fully understanding the chemistry of the system requires higher resolution to identify the ions and water molecules involved in polymerization and ATP hydrolysis. Here, we find experimental evidence for the association of cations with the surfaces of G-actin in a 2.0-Å resolution X-ray structure of actin bound to a Cordon-Bleu WH2 motif and in previously determined high-resolution X-ray structures. Three of four reoccurring divalent cation sites were stable during molecular dynamics (MD) simulations of the filament, suggesting that these sites may play a functional role in stabilizing the filament. We modeled the water coordination at the ATP-bound Mg2+, which also proved to be stable during the MD simulations. Using this model of the filament with a hydrated ATP-bound Mg2+, we compared the cumulative probability of an activated hydrolytic water molecule approaching the γ-phosphorous of ATP, in comparison with G-actin, in the MD simulations. The cumulative probability increased in F-actin in line with the activation of actin's ATPase activity on polymerization. However, inclusion of the cations in the filament lowered cumulative probability, suggesting the rate of hydrolysis may be linked to filament flexibility. Together, these data extend the possible roles of Mg2+ in polymerization and the mechanism of polymerization-induced activation of actin's ATPase activity.

Articles - 5ypu mentioned but not cited (4)

  1. Structural evidence for the roles of divalent cations in actin polymerization and activation of ATP hydrolysis. Scipion CPM, Ghoshdastider U, Ferrer FJ, Yuen TY, Wongsantichon J, Robinson RC. Proc Natl Acad Sci U S A 115 10345-10350 (2018)
  2. Specialization of actin isoforms derived from the loss of key interactions with regulatory factors. Boiero Sanders M, Toret CP, Guillotin A, Antkowiak A, Vannier T, Robinson RC, Michelot A. EMBO J 41 e107982 (2022)
  3. Investigation into Early Steps of Actin Recognition by the Intrinsically Disordered N-WASP Domain V. Chan-Yao-Chong M, Durand D, Ha-Duong T. Int J Mol Sci 20 4493 (2019)
  4. Functional and structural insights into the multi-step activation and catalytic mechanism of bacterial ExoY nucleotidyl cyclase toxins bound to actin-profilin. Teixeira Nunes M, Retailleau P, Raoux-Barbot D, Comisso M, Missinou AA, Velours C, Plancqueel S, Ladant D, Mechold U, Renault L. PLoS Pathog 19 e1011654 (2023)


Reviews citing this publication (1)

  1. Human deafness-associated variants alter the dynamics of key molecules in hair cell stereocilia F-actin cores. Miyoshi T, Belyantseva IA, Kitajiri SI, Miyajima H, Nishio SY, Usami SI, Kim BJ, Choi BY, Omori K, Shroff H, Friedman TB. Hum Genet 141 363-382 (2022)

Articles citing this publication (8)

  1. Structural basis of actin filament assembly and aging. Oosterheert W, Klink BU, Belyy A, Pospich S, Raunser S. Nature 611 374-379 (2022)
  2. Atomic view into Plasmodium actin polymerization, ATP hydrolysis, and fragmentation. Kumpula EP, Lopez AJ, Tajedin L, Han H, Kursula I. PLoS Biol 17 e3000315 (2019)
  3. Actinosomes: Condensate-Templated Containers for Engineering Synthetic Cells. Ganar KA, Leijten L, Deshpande S. ACS Synth Biol 11 2869-2879 (2022)
  4. DnaJA4 is involved in responses to hyperthermia by regulating the expression of F-actin in HaCaT cells. Liu RJ, Niu XL, Yuan JP, Chen HD, Gao XH, Qi RQ. Chin Med J (Engl) 134 456-462 (2020)
  5. Effects of Nucleotide and End-Dependent Actin Conformations on Polymerization. Jepsen L, Sept D. Biophys J 119 1800-1810 (2020)
  6. Graphene Enhances Actin Filament Assembly Kinetics and Modulates NIH-3T3 Fibroblast Cell Spreading. Park J, Kravchuk P, Krishnaprasad A, Roy T, Kang EH. Int J Mol Sci 23 509 (2022)
  7. The structure of a 15-stranded actin-like filament from Clostridium botulinum. Koh F, Narita A, Lee LJ, Tanaka K, Tan YZ, Dandey VP, Popp D, Robinson RC. Nat Commun 10 2856 (2019)
  8. Bioinspired Membrane Interfaces: Controlling Actomyosin Architecture and Contractility. Liebe NL, Mey I, Vuong L, Shikho F, Geil B, Janshoff A, Steinem C. ACS Appl Mater Interfaces 15 11586-11598 (2023)


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