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Open AccessOpen Access JUSTC Life Sciences 06 July 2023

Dynamics in the assembly of the 30S ribosomal subunit investigated by coarse-grained simulations

  • 1.

    School of Data Science, University of Science and Technology of China, Hefei 230027, China

  • 2.

    Department of Physics, University of Science and Technology of China, Hefei 230026, China

Cite this:
https://doi.org/10.52396/JUSTC-2023-0064
More Information
  • Author Bio:

    Xin Liu is currently a graduate student in the School of Data Science at the University of Science and Technology of China. She is under the supervision of Prof. Zhiyong Zhang. Her research mainly focuses on computer simulations of large biomolecular complex assemblies

    Zhiyong Zhang is currently a Professor in the Department of Physics at the University of Science and Technology of China (USTC). He received his Ph.D. degree in Biochemistry and Molecular Biology from USTC. His research interests include method development on multiscale modeling and integrative modeling of large biomolecular complexes

  • Corresponding author: E-mail: zzyzhang@ustc.edu.cn
  • Received Date: 18 April 2023
  • Accepted Date: 08 June 2023
    • Available Online: 06 July 2023
    Abstract

  • Abstract

    The ribosome is a large biomolecular complex responsible for protein synthesis. In Escherichia coli (E. coli), a complete ribosome is composed of a 30S small subunit and a 50S large subunit. For approximately half a century, the 30S subunit has been a key model system for studying the in vitro assembly of the ribosome, and an assembly map has been proposed. However, structural details in the assembly of this protein‒RNA complex remain elusive. In this paper, we conducted a series of coarse-grained simulations following the order of the assembly map to investigate conformational dynamics during the assembly process of the 30S subunit. It has been found that the tertiary structure of naked 16S rRNA is very unstable, which is the case after binding of early-assembly proteins. The mid-assembly proteins can significantly restrict the mobility of the 16S rRNA and make the latter close to the native structure. The final binding of the late-assembly proteins would fully obtain the collective motion of the 16S rRNA. In particular, proteins S9 and S3 may have more important contributions to the assembly of the 30S subunit than other S proteins. Our strategy of coarse-grained simulations can be generally used to study assembly dynamics of large biomolecular complexes as long as the assembly map is available.

    Graphical abstract

    As the ribosomal proteins are assembled sequentially at each stage, the 16S rRNA changes from an unfolded to a well-folded structure.

    Abstract

    The ribosome is a large biomolecular complex responsible for protein synthesis. In Escherichia coli (E. coli), a complete ribosome is composed of a 30S small subunit and a 50S large subunit. For approximately half a century, the 30S subunit has been a key model system for studying the in vitro assembly of the ribosome, and an assembly map has been proposed. However, structural details in the assembly of this protein‒RNA complex remain elusive. In this paper, we conducted a series of coarse-grained simulations following the order of the assembly map to investigate conformational dynamics during the assembly process of the 30S subunit. It has been found that the tertiary structure of naked 16S rRNA is very unstable, which is the case after binding of early-assembly proteins. The mid-assembly proteins can significantly restrict the mobility of the 16S rRNA and make the latter close to the native structure. The final binding of the late-assembly proteins would fully obtain the collective motion of the 16S rRNA. In particular, proteins S9 and S3 may have more important contributions to the assembly of the 30S subunit than other S proteins. Our strategy of coarse-grained simulations can be generally used to study assembly dynamics of large biomolecular complexes as long as the assembly map is available.

    • Public Summary

    • Our simulations provide some dynamic details during the assembly process of the 30S small subunit.
    • S9 and S3 may have more important contributions to the assembly of the 30S subunit than other ribosomal proteins.
    • Our strategy can be applied for studying the assembly dynamics of any large biomolecular complex as long as the assembly map is known.

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    • References(43)
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    Klinge S, Woolford J L. Ribosome assembly coming into focus. Nat. Rev. Mol. Cell Biol., 2019, 20 (2): 116–131. doi: 10.1038/s41580-018-0078-y
    [2]
    Melnikov S, Ben-Shem A, de Loubresse N G, et al. One core, two shells: Bacterial and eukaryotic ribosomes. Nat. Struct. Mol. Biol., 2012, 19 (6): 560–567. doi: 10.1038/nsmb.2313
    [3]
    Levy E D, Erba E B, Robinson C V, et al. Assembly reflects evolution of protein complexes. Nature, 2008, 453 (7199): 1262–1265. doi: 10.1038/nature06942
    [4]
    Marsh J A, Teichmann S A. Parallel dynamics and evolution: Protein conformational fluctuations and assembly reflect evolutionary changes in sequence and structure. BioEssays, 2014, 36 (2): 209–218. doi: 10.1002/bies.201300134
    [5]
    Marsh J A, Hernández H, Hall Z, et al. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell, 2013, 153 (2): 461–470. doi: 10.1016/j.cell.2013.02.044
    [6]
    Friedman F K, Beychok S. Probes of subunit assembly and reconstitution pathways in multisubunit proteins. Annu. Rev. Biochem., 1979, 48: 217–250. doi: 10.1146/annurev.bi.48.070179.001245
    [7]
    Bunner A E, Nord S, Wikström M, et al. The effect of ribosome assembly cofactors on in vitro 30S subunit reconstitution. J. Mol. Biol., 2010, 398 (1): 1–7. doi: 10.1016/j.jmb.2010.02.036
    [8]
    Traub P, Nomura M. Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc. Natl. Acad. Sci. U.S.A., 1968, 59 (3): 777–784. doi: 10.1073/pnas.59.3.777
    [9]
    Nierhaus K H, Dohme F. Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 1974, 71 (12): 4713–4717. doi: 10.1073/pnas.71.12.4713
    [10]
    Green R, Noller H F. Reconstitution of functional 50S ribosomes from in vitro transcripts of Bacillus stearothermophilus 23S rRNA. Biochemistry, 1999, 38 (6): 1772–1779. doi: 10.1021/bi982246a
    [11]
    Agalarov S, Yusupov M, Yusupova G. Reconstitution of functionally active Thermus thermophilus 30S ribosomal subunit from ribosomal 16S RNA and ribosomal proteins. In: Ennifar E, editor. Nucleic Acid Crystallography: Methods and Protocols. New York: Humana Press, 2016: 303−314.
    [12]
    Londei P, Teuudò J, Acca M, et al. Total reconstitation of active large ribosomal subunlts of the tbermoaddophllk arcfaaebacterium Sulfolobus solfataricus. Nucleic Acids Res., 1986, 14 (5): 2269–2285. doi: 10.1093/nar/14.5.2269
    [13]
    Sanchez M E, Urena D, Amils R, et al. In vitro reassembly of active large ribosomal subunits of the halophilic archaebacterium Haloferax mediterranei. Biochemistry, 1990, 29 (39): 9256–9261. doi: 10.1021/bi00491a021
    [14]
    Fahnestock S R. Reconstitution of active 50 S ribosomal subunits from Bacillus lichenformis and Bacillus subtilis. Methods Enzymol., 1979, 59: 437–443. doi: 10.1016/0076-6879(79)59105-8
    [15]
    Cohlberg J A, Nomura M. Reconstitution of Bacillus stearothermophilus 50 S ribosomal subunits from purified molecular components. J. Biol. Chem., 1976, 251 (1): 209–221. doi: 10.1016/S0021-9258(17)33947-9
    [16]
    Weitzmann C J, Cunningham P R, Nurse K, et al. Chemical evidence for domain assembly of the Escherichia coli 30S ribosome. FASEB J., 1993, 7 (1): 177–180. doi: 10.1096/fasebj.7.1.7916699
    [17]
    Agalarov S C, Zheleznyakova E N, Selivanova O M, et al. In vitro assembly of a ribonucleoprotein particle corresponding to the platform domain of the 30S ribosomal subunit. Proc. Natl. Acad. Sci. U.S.A., 1998, 95 (3): 999–1003. doi: 10.1073/pnas.95.3.999
    [18]
    Samaha R R, O'Brien B, O'Brien T W, et al. Independent in vitro assembly of a ribonucleoprotein particle containing the 3′ domain of 16S rRNA. Proc. Natl. Acad. Sci. U.S.A., 1994, 91 (17): 7884–7888. doi: 10.1073/pnas.91.17.7884
    [19]
    Nierhaus K H. The assembly of prokaryotic ribosomes. Biochimie, 1991, 73 (6): 739–755. doi: 10.1016/0300-9084(91)90054-5
    [20]
    Mizushima S, Nomura M. Assembly mapping of 30S ribosomal proteins from E. coli. Nature, 1970, 226 (5252): 1214–1218. doi: 10.1038/2261214a0
    [21]
    Culver G M. Assembly of the 30S ribosomal subunit. Biopolymers, 2003, 68 (2): 234–249. doi: 10.1002/bip.10221
    [22]
    Tozzini V. Multiscale modeling of proteins. Accounts. Chem. Res., 2010, 43 (2): 220–230. doi: 10.1021/ar9001476
    [23]
    Zhang J, Li W, Wang J, et al. Protein folding simulations: From coarse-grained model to all-atom model. IUBMB Life, 2009, 61 (6): 627–643. doi: 10.1002/iub.223
    [24]
    Takada S. Coarse-grained molecular simulations of large biomolecules. Curr. Opin. Struc. Biol., 2012, 22 (2): 130–137. doi: 10.1016/j.sbi.2012.01.010
    [25]
    Tozzini V. Minimalist models for proteins: A comparative analysis. Q. Rev. Biophys., 2010, 43 (3): 333–371. doi: 10.1017/S0033583510000132
    [26]
    Li W F, Zhang J, Wang J, et al. Multiscale theory and computational method for biomolecule simulations. Acta Phys. Sin., 2015, 64 (9): 098701. doi: 10.7498/aps.64.098701
    [27]
    Yao X Q, Kenzaki H, Murakami S, et al. Drug export and allosteric coupling in a multidrug transporter revealed by molecular simulations. Nat. Commun., 2010, 1: 117. doi: 10.1038/ncomms1116
    [28]
    Yan A, Wang Y, Kloczkowski A, et al. Effects of protein subunits removal on the computed motions of partial 30S structures of the ribosome. J. Chem. Theory Comput., 2008, 4 (10): 1757–1767. doi: 10.1021/ct800223g
    [29]
    Wen B, Wang W, Zhang J, et al. Structural and dynamic properties of the C-terminal region of the Escherichia coli RNA chaperone Hfq: Integrative experimental and computational studies. Phys. Chem. Chem. Phys., 2017, 19 (31): 21152–21164. doi: 10.1039/C7CP01044C
    [30]
    Kenzaki H, Koga N, Hori N, et al. CafeMol: A coarse-grained biomolecular simulator for simulating proteins at work. J. Chem. Theory Comput., 2011, 7 (6): 1979–1989. doi: 10.1021/ct2001045
    [31]
    Izvekov S, Voth G A. A multiscale coarse-graining method for biomolecular systems. J. Phys. Chem. B, 2005, 109 (7): 2469–2473. doi: 10.1021/jp044629q
    [32]
    Marrink S J, Risselada H J, Yefimov S, et al. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B, 2007, 111 (27): 7812–7824. doi: 10.1021/jp071097f
    [33]
    Souza P C T, Alessandri R, Barnoud J, et al. Martini 3: A general purpose force field for coarse-grained molecular dynamics. Nat. Methods, 2021, 18 (4): 382–388. doi: 10.1038/s41592-021-01098-3
    [34]
    Avendaño C, Lafitte T, Galindo A, et al. SAFT-γ force field for the simulation of molecular fluids. 1. A single-site coarse grained model of carbon dioxide. J. Phys. Chem. B, 2011, 115 (38): 11154–11169. doi: 10.1021/jp204908d
    [35]
    Zhang Z, Sanbonmatsu K Y, Voth G A. Key intermolecular interactions in the E. coli 70S ribosome revealed by coarse-grained analysis. J. Am. Chem. Soc., 2011, 133 (42): 16828–16838. doi: 10.1021/ja2028487
    [36]
    Li W, Wang W, Takada S. Energy landscape views for interplays among folding, binding, and allostery of calmodulin domains. Proc. Natl. Acad. Sci. U.S.A., 2014, 111 (29): 10550–10555. doi: 10.1073/pnas.1402768111
    [37]
    Clementi C, Nymeyer H, Onuchic J N. Topological and energetic factors: What determines the structural details of the transition state ensemble and “en-route” intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol., 2000, 298 (5): 937–953. doi: 10.1006/jmbi.2000.3693
    [38]
    Amadei A, Linssen A B, Berendsen H J. Essential dynamics of proteins. Proteins, 1993, 17 (4): 412–425. doi: 10.1002/prot.340170408
    [39]
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    Powers T, Daubresse G, Noller H F. Dynamics of in vitro assembly of 16 S rRNA into 30 S ribosomal subunits. J. Mol. Biol., 1993, 232 (2): 362–374. doi: 10.1006/jmbi.1993.1396
    [42]
    Amann S J, Keihsler D, Bodrug T, et al. Frozen in time: Analyzing molecular dynamics with time-resolved cryo-EM. Structure, 2023, 31 (1): 4–19. doi: 10.1016/j.str.2022.11.014
    [43]
    Kurisaki I, Tanaka S. Computational prediction of heteromeric protein complex disassembly order using hybrid Monte Carlo/molecular dynamics simulation. Phys. Chem. Chem. Phys., 2022, 24 (17): 10575–10587. doi: 10.1039/D2CP00267A
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    Figure  1.  Structure of the 30S ribosomal subunit. (a) The front side (the interface with the 50S subunit) and (b) the back. The 16S rRNA is colored black, and the S proteins are colored differently according to the kinetic assembly map (Table 1). The body, platform, head, and beak are labeled.

    Figure  2.  Time evolution of RMSD during the CG simulations. Black: the naked 16S rRNA, magenta: the 16S rRNA with the early-assembly proteins, orange: the 16S rRNA with the early- and mid-assembly proteins, blue: the 16S rRNA with early-, mid-, and mid-late-assembly proteins, and red: the 30S subunit.

    Figure  3.  Stability of the 16S rRNA after assembling the S proteins at each stage sequentially. (a) Naked 16S rRNA. (b) The 16S rRNA with only the early-assembly proteins. (c) The 16S rRNA with the early- and mid-assembly proteins. (d) The 16S rRNA with the early-, mid- and mid-late-assembly proteins. (e) The 30S subunit. At each stage, the final structure of the CG simulation is shown.

    Figure  4.  An assembly path of the 30S subunit shown on a subspace defined by the PCA modes. PCA was conducted on the CG trajectory of the 30S subunit, and only P particles were used to construct the covariance matrix. The first two PCA modes with the largest eigenvalues (PC1 and PC2) were chosen to define the 2D subspace. (a) Projections of the different CG trajectories onto the subspace. (b) Collective motion along PC1. (c) Collective motion along PC2.

    Figure  5.  The role of individual S proteins in the assembly of the 30S subunit. (a) Equilibriumed (from 80 to 100 million steps of the CG simulations) RMSD values of all the simulated systems. Starting from the naked 16S rRNA, then adding the S proteins one by one following the order shown in Table 1, and finally ending with the 30S subunit. The RMSD curves at the four stages are colored differently. In the color bar on the right side, the two dividing proteins (S9 and S3) are labeled by *. The two corresponding RMSD curves are shown by solid lines, while other curves are shown by dashed lines. (b) The position of S9. (c) The position of S3.

    Figure  6.  Evolution of RMSIP in the assembly process of the 30S subunit. The x-axis represents the assembly order of the S proteins shown in Table 1. For each system, the RMSIP was calculated between the PCA modes of the system and those of the 30S subunit. The RMSIP ends at 1.0 because the system is the 30S subunit after S21 is assembled.

    Figure  7.  The role of individual S proteins in a switched assembly order of the 30S subunit. (a) Equilibriumed (from 80 to 100 million steps of the CG simulations) RMSD values of all the simulated systems. Starting from the naked 16S rRNA, then adding the S proteins one by one in descending order of their molecular weights, and finally ending with the 30S subunit. The RMSD curves are colored according to the stages to which the corresponding S proteins belong, as shown in Fig. 5a. In the color bar on the right side, the two dividing proteins (S5 and S11) are labeled by *. The two corresponding RMSD curves are shown by solid lines, while other curves are shown by dashed lines. (b) The position of S5. (c) The position of S11.

    [1]
    Klinge S, Woolford J L. Ribosome assembly coming into focus. Nat. Rev. Mol. Cell Biol., 2019, 20 (2): 116–131. doi: 10.1038/s41580-018-0078-y
    [2]
    Melnikov S, Ben-Shem A, de Loubresse N G, et al. One core, two shells: Bacterial and eukaryotic ribosomes. Nat. Struct. Mol. Biol., 2012, 19 (6): 560–567. doi: 10.1038/nsmb.2313
    [3]
    Levy E D, Erba E B, Robinson C V, et al. Assembly reflects evolution of protein complexes. Nature, 2008, 453 (7199): 1262–1265. doi: 10.1038/nature06942
    [4]
    Marsh J A, Teichmann S A. Parallel dynamics and evolution: Protein conformational fluctuations and assembly reflect evolutionary changes in sequence and structure. BioEssays, 2014, 36 (2): 209–218. doi: 10.1002/bies.201300134
    [5]
    Marsh J A, Hernández H, Hall Z, et al. Protein complexes are under evolutionary selection to assemble via ordered pathways. Cell, 2013, 153 (2): 461–470. doi: 10.1016/j.cell.2013.02.044
    [6]
    Friedman F K, Beychok S. Probes of subunit assembly and reconstitution pathways in multisubunit proteins. Annu. Rev. Biochem., 1979, 48: 217–250. doi: 10.1146/annurev.bi.48.070179.001245
    [7]
    Bunner A E, Nord S, Wikström M, et al. The effect of ribosome assembly cofactors on in vitro 30S subunit reconstitution. J. Mol. Biol., 2010, 398 (1): 1–7. doi: 10.1016/j.jmb.2010.02.036
    [8]
    Traub P, Nomura M. Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc. Natl. Acad. Sci. U.S.A., 1968, 59 (3): 777–784. doi: 10.1073/pnas.59.3.777
    [9]
    Nierhaus K H, Dohme F. Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc. Natl. Acad. Sci. U.S.A., 1974, 71 (12): 4713–4717. doi: 10.1073/pnas.71.12.4713
    [10]
    Green R, Noller H F. Reconstitution of functional 50S ribosomes from in vitro transcripts of Bacillus stearothermophilus 23S rRNA. Biochemistry, 1999, 38 (6): 1772–1779. doi: 10.1021/bi982246a
    [11]
    Agalarov S, Yusupov M, Yusupova G. Reconstitution of functionally active Thermus thermophilus 30S ribosomal subunit from ribosomal 16S RNA and ribosomal proteins. In: Ennifar E, editor. Nucleic Acid Crystallography: Methods and Protocols. New York: Humana Press, 2016: 303−314.
    [12]
    Londei P, Teuudò J, Acca M, et al. Total reconstitation of active large ribosomal subunlts of the tbermoaddophllk arcfaaebacterium Sulfolobus solfataricus. Nucleic Acids Res., 1986, 14 (5): 2269–2285. doi: 10.1093/nar/14.5.2269
    [13]
    Sanchez M E, Urena D, Amils R, et al. In vitro reassembly of active large ribosomal subunits of the halophilic archaebacterium Haloferax mediterranei. Biochemistry, 1990, 29 (39): 9256–9261. doi: 10.1021/bi00491a021
    [14]
    Fahnestock S R. Reconstitution of active 50 S ribosomal subunits from Bacillus lichenformis and Bacillus subtilis. Methods Enzymol., 1979, 59: 437–443. doi: 10.1016/0076-6879(79)59105-8
    [15]
    Cohlberg J A, Nomura M. Reconstitution of Bacillus stearothermophilus 50 S ribosomal subunits from purified molecular components. J. Biol. Chem., 1976, 251 (1): 209–221. doi: 10.1016/S0021-9258(17)33947-9
    [16]
    Weitzmann C J, Cunningham P R, Nurse K, et al. Chemical evidence for domain assembly of the Escherichia coli 30S ribosome. FASEB J., 1993, 7 (1): 177–180. doi: 10.1096/fasebj.7.1.7916699
    [17]
    Agalarov S C, Zheleznyakova E N, Selivanova O M, et al. In vitro assembly of a ribonucleoprotein particle corresponding to the platform domain of the 30S ribosomal subunit. Proc. Natl. Acad. Sci. U.S.A., 1998, 95 (3): 999–1003. doi: 10.1073/pnas.95.3.999
    [18]
    Samaha R R, O'Brien B, O'Brien T W, et al. Independent in vitro assembly of a ribonucleoprotein particle containing the 3′ domain of 16S rRNA. Proc. Natl. Acad. Sci. U.S.A., 1994, 91 (17): 7884–7888. doi: 10.1073/pnas.91.17.7884
    [19]
    Nierhaus K H. The assembly of prokaryotic ribosomes. Biochimie, 1991, 73 (6): 739–755. doi: 10.1016/0300-9084(91)90054-5
    [20]
    Mizushima S, Nomura M. Assembly mapping of 30S ribosomal proteins from E. coli. Nature, 1970, 226 (5252): 1214–1218. doi: 10.1038/2261214a0
    [21]
    Culver G M. Assembly of the 30S ribosomal subunit. Biopolymers, 2003, 68 (2): 234–249. doi: 10.1002/bip.10221
    [22]
    Tozzini V. Multiscale modeling of proteins. Accounts. Chem. Res., 2010, 43 (2): 220–230. doi: 10.1021/ar9001476
    [23]
    Zhang J, Li W, Wang J, et al. Protein folding simulations: From coarse-grained model to all-atom model. IUBMB Life, 2009, 61 (6): 627–643. doi: 10.1002/iub.223
    [24]
    Takada S. Coarse-grained molecular simulations of large biomolecules. Curr. Opin. Struc. Biol., 2012, 22 (2): 130–137. doi: 10.1016/j.sbi.2012.01.010
    [25]
    Tozzini V. Minimalist models for proteins: A comparative analysis. Q. Rev. Biophys., 2010, 43 (3): 333–371. doi: 10.1017/S0033583510000132
    [26]
    Li W F, Zhang J, Wang J, et al. Multiscale theory and computational method for biomolecule simulations. Acta Phys. Sin., 2015, 64 (9): 098701. doi: 10.7498/aps.64.098701
    [27]
    Yao X Q, Kenzaki H, Murakami S, et al. Drug export and allosteric coupling in a multidrug transporter revealed by molecular simulations. Nat. Commun., 2010, 1: 117. doi: 10.1038/ncomms1116
    [28]
    Yan A, Wang Y, Kloczkowski A, et al. Effects of protein subunits removal on the computed motions of partial 30S structures of the ribosome. J. Chem. Theory Comput., 2008, 4 (10): 1757–1767. doi: 10.1021/ct800223g
    [29]
    Wen B, Wang W, Zhang J, et al. Structural and dynamic properties of the C-terminal region of the Escherichia coli RNA chaperone Hfq: Integrative experimental and computational studies. Phys. Chem. Chem. Phys., 2017, 19 (31): 21152–21164. doi: 10.1039/C7CP01044C
    [30]
    Kenzaki H, Koga N, Hori N, et al. CafeMol: A coarse-grained biomolecular simulator for simulating proteins at work. J. Chem. Theory Comput., 2011, 7 (6): 1979–1989. doi: 10.1021/ct2001045
    [31]
    Izvekov S, Voth G A. A multiscale coarse-graining method for biomolecular systems. J. Phys. Chem. B, 2005, 109 (7): 2469–2473. doi: 10.1021/jp044629q
    [32]
    Marrink S J, Risselada H J, Yefimov S, et al. The MARTINI force field: coarse grained model for biomolecular simulations. J. Phys. Chem. B, 2007, 111 (27): 7812–7824. doi: 10.1021/jp071097f
    [33]
    Souza P C T, Alessandri R, Barnoud J, et al. Martini 3: A general purpose force field for coarse-grained molecular dynamics. Nat. Methods, 2021, 18 (4): 382–388. doi: 10.1038/s41592-021-01098-3
    [34]
    Avendaño C, Lafitte T, Galindo A, et al. SAFT-γ force field for the simulation of molecular fluids. 1. A single-site coarse grained model of carbon dioxide. J. Phys. Chem. B, 2011, 115 (38): 11154–11169. doi: 10.1021/jp204908d
    [35]
    Zhang Z, Sanbonmatsu K Y, Voth G A. Key intermolecular interactions in the E. coli 70S ribosome revealed by coarse-grained analysis. J. Am. Chem. Soc., 2011, 133 (42): 16828–16838. doi: 10.1021/ja2028487
    [36]
    Li W, Wang W, Takada S. Energy landscape views for interplays among folding, binding, and allostery of calmodulin domains. Proc. Natl. Acad. Sci. U.S.A., 2014, 111 (29): 10550–10555. doi: 10.1073/pnas.1402768111
    [37]
    Clementi C, Nymeyer H, Onuchic J N. Topological and energetic factors: What determines the structural details of the transition state ensemble and “en-route” intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol., 2000, 298 (5): 937–953. doi: 10.1006/jmbi.2000.3693
    [38]
    Amadei A, Linssen A B, Berendsen H J. Essential dynamics of proteins. Proteins, 1993, 17 (4): 412–425. doi: 10.1002/prot.340170408
    [39]
    de Groot B L, van Aalten D M, Amadei A, et al. The consistency of large concerted motions in proteins in molecular dynamics simulations. Biophys. J., 1996, 71 (4): 1707–1713. doi: 10.1016/S0006-3495(96)79372-4
    [40]
    Amadei A, Ceruso M A, Di Nola A. On the convergence of the conformational coordinates basis set obtained by the essential dynamics analysis of proteins’ molecular dynamics simulations. Proteins, 1999, 36 (4): 419–424. doi: 10.1002/(SICI)1097-0134(19990901)36:4<419::AID-PROT5>3.0.CO;2-U
    [41]
    Powers T, Daubresse G, Noller H F. Dynamics of in vitro assembly of 16 S rRNA into 30 S ribosomal subunits. J. Mol. Biol., 1993, 232 (2): 362–374. doi: 10.1006/jmbi.1993.1396
    [42]
    Amann S J, Keihsler D, Bodrug T, et al. Frozen in time: Analyzing molecular dynamics with time-resolved cryo-EM. Structure, 2023, 31 (1): 4–19. doi: 10.1016/j.str.2022.11.014
    [43]
    Kurisaki I, Tanaka S. Computational prediction of heteromeric protein complex disassembly order using hybrid Monte Carlo/molecular dynamics simulation. Phys. Chem. Chem. Phys., 2022, 24 (17): 10575–10587. doi: 10.1039/D2CP00267A
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