High-Dimensional Mutant and Modular Thermodynamic Cycles, Molecular Switching, and Free Energy Transduction

Literature Cited

1. Abrahams JP, Leslie AGW, Lutter R, Walker JE. 1.  1994. Structure at 2.8 Å resolution of F₁-ATPase from bovine heart mitochondria. Nature 370:621–28 [Google Scholar]
2. Adamczyk AJ, Warshel A. 2.  2011. Converting structural information into an allosteric-energy-based picture for elongation factor Tu activation by the ribosome. PNAS 108:9827–32 [Google Scholar]
3. Astumian RD. 3.  2007. Design principles for Brownian molecular machines: how to swim in molasses and walk in a hurricane. Phys. Chem. Chem. Phys. 9:5067–83 [Google Scholar]
4. Astumian RD. 4.  2010. Thermodynamics and kinetics of molecular motors. Biophys. J. 98:2401–9 [Google Scholar]
5. Astumian RD. 5.  2011. Stochastic conformational pumping: a mechanism for free-energy transduction by molecules. Annu. Rev. Biophys. 40:289–313 [Google Scholar]
6. Astumian RD, Mukherjee S, Warshel A. 6.  2016. The physics and physical chemistry of molecular machines. Chem. Phys. Chem. 17:1719–41 [Google Scholar]
7. Bahar I, Lezon TR, Yang L-W, Eyal E. 7.  2010. Global dynamics of proteins: bridging between structure and function. Annu. Rev. Biophys. 39:23–42 [Google Scholar]
8. Baldwin J, Chothia C. 8.  1979. Hemoglobin: the structural changes related to ligand binding and its allosteric mechanism. J. Mol. Biol. 129:175–200 [Google Scholar]
9. Ben-Abu Y, Zhou Y, Zilberberg N, Yifrach O. 9.  2009. Inverse coupling in leak and voltage-activated K⁺ channel gates underlies distinct roles in electrical signaling. Nat. Struct. Mol. Biol. 16:71–79 [Google Scholar]
10. Berezhkovskii A, Hummer G, Szabo A. 10.  2009. Reactive flux and folding pathways in network models of coarse-grained protein dynamics. J. Chem. Phys. 130:205102 [Google Scholar]
11. Box GEP, Hunter WG, Hunter JS. 11.  1978. Statistics for Experimenters New York: Wiley Interscience
12. Budiman M, Knaggs MH, Fetrow JS, Alexander RW. 12.  2007. Using molecular dynamics to map interaction networks in an aminoacyl-tRNA synthetase. Proteins 68:670–89 [Google Scholar]
13. Cammer S, Carter CW Jr.. 13.  2010. Six Rossmannoid folds, including the Class I aminoacyl-tRNA synthetases, share a partial core with the anticodon-binding domain of a Class II aminoacyl-tRNA synthetase. Bioinformatics 26:709–14 [Google Scholar]
14. Carter CW Jr.. 14.  2014. Urzymology: experimental access to a key transition in the appearance of enzymes. J. Biol. Chem. 289:30213–20 [Google Scholar]
15. Carter CW Jr., Ilyin V, Yin Y, Huang X, Retailleau P. 15.  2001. Three TrpRS conformations stabilize a dynamic, dissociative transition-state Presented at Using Crystallogr. Underst. Enzym. Mech. St. Paul, MN:
16. Carter CW Jr., LeFebvre B, Cammer SA, Tropsha A, Edgell MH. 16.  2001. Four-body potentials reveal protein-specific correlations to stability changes caused by hydrophobic core mutations. J. Mol. Biol. 311:625–38 [Google Scholar]
17. Carter CW Jr., Charles W, Chandrasekaran SN, Weinreb V, Li L, Williams T. 17.  2017. Combining multi-mutant and modular thermodynamic cycles to measure energetic coupling networks in enzyme catalysis. Struct. Dyn. 4:3032101 [Google Scholar]
18. Chandrasekaran SN, Carter CW Jr. 18.  2017. Augmenting the anisotropic network model with torsional potentials improves PATH performance, enabling detailed comparison with experimental rate data. Struct. Dyn. 4:3032103 [Google Scholar]
19. Chandrasekaran SN, Das J, Dokholyan NV, Carter CW Jr. 19.  2016. A modified PATH algorithm rapidly generates transition states comparable to those found by other well established algorithms. Struct. Dyn. 3:012101 [Google Scholar]
20. Chen J, Stites WE. 20.  2001. Energetics of side chain packing in staphylococcal nuclease assessed by systematic double mutant cycles. Biochemistry 40:14004–11 [Google Scholar]
21. Chen J, Stites WE. 21.  2001. Higher-order packing interactions in triple and quadruple mutants of staphylococcal nuclease. Biochemistry 40:14012–19 [Google Scholar]
22. Chi C, Elfström L, Shi Y, Snäll T, Engström A, Jemth P. 22.  2008. Reassessing a sparse energetic network within a single protein domain. PNAS 105:4679–84 [Google Scholar]
23. Cleland WW, Northrup DB. 23.  1999. Energetics of substrate binding, catalysis, and product release. Methods Enzymol 308:3–48 [Google Scholar]
24. Das A, Gur M, Cheng MH, Jo S, Bahar I, Roux B. 24.  2014. Exploring the conformational transitions of biomolecular systems using a simple two-state anisotropic network model. PLOS Comput. Biol. 10:e1003521 [Google Scholar]
25. del Sol A, Fujihashi H, Amoros D, Nussinov R. 25.  2006. Residues crucial for maintaining short paths in network communication mediate signaling in proteins. Mol. Syst. Biol. 2:20060019 [Google Scholar]
26. Dill KA, Bromberg S. 26.  2012. Molecular Driving Forces New York: Garland
27. Dokholyan NV, Buldyrev SV, Stanley HE, Shakhnovich EI. 27.  1998. Discrete molecular dynamics studies of the folding of a protein-like model. Fold. Des. 3:577–87 [Google Scholar]
28. Doublié S, Bricogne G, Gilmore CJ, Carter CW Jr.. 28.  1995. Tryptophanyl-tRNA synthetase crystal structure reveals an unexpected homology to tyrosyl-tRNA synthetase. Structure 3:17–31 [Google Scholar]
29. Dürr D, Bach A. 29.  1978. The Onsager-Machlup function as a Lagrangian for the most probable path of a diffusion process. Commun. Math. Phys. 60:153–70 [Google Scholar]
30. Eisenberg E, Hill TL. 30.  1978. A cross-bridge model of muscle contraction. Prog. Biophys. Mol. Biol. 33:55–82 [Google Scholar]
31. Fersht AR. 31.  1987. Dissection of the structure and activity of the tyrosyl-tRNA synthetase by site-directed mutagenesis. Biochemistry 26:8031–37 [Google Scholar]
32. Fersht AR, Knill Jones JW, Bedouelle H, Winter G. 32.  1988. Reconstruction by site-directed mutagenesis of the transition state for the activation of tyrosine by the tyrosyl-tRNA synthetase: A mobile loop envelopes the transition state in an induced-fit mechanism. Biochemistry 27:1581–87 [Google Scholar]
33. First EA, Fersht AR. 33.  1993. Involvement of threonine 234 in catalysis of tyrosyl adenylate formation by tyrosyl-tRNA synthetase. Biochemistry 32:13644–50 [Google Scholar]
34. First EA, Fersht AR. 34.  1993. Mutation of lysine 233 to alanine introduces positive cooperativity into tyrosyl-tRNA synthetase. Biochemistry 32:13651–57 [Google Scholar]
35. First EA, Fersht AR. 35.  1993. Mutational and kinetic analysis of a mobile loop in tyrosyl-tRNA synthetase. Biochemistry 32:13658–63 [Google Scholar]
36. First EA, Fersht AR. 36.  1995. Analysis of the role of the KMSKS loop in the catalytic mechanism of the tyrosyl-tRNA synthetase using multimutant cycles. Biochemistry 34:5030–43 [Google Scholar]
37. Franklin J, Koehl P, Doniach S, Delarue M. 37.  2007. MinActionPath: maximum likelihood trajectory for large-scale structural transitions in a coarse-grained locally harmonic energy landscape. Nucleic Acids Res 35:W477–82 [Google Scholar]
38. Fuentes EJ, Gilmore SA, Mauldin RV, Lee AL. 38.  2006. Evaluation of energetic and dynamic coupling networks in a PDZ domain protein. J. Mol. Biol. 364:337–51 [Google Scholar]
39. Gao R, Mack TR, Stock AM. 39.  Bacterial response regulators: versatile regulatory strategies from common domains. TRENDS Biochem. Sci. 32:225–34 [Google Scholar]
40. Ge H, Pressé S, Ghosh K, Dill KA. 40.  2012. Markov processes follow from the principle of maximum caliber. J. Chem. Phys. 136:064108 [Google Scholar]
41. Goldenfield N. 41.  2015. Indivi-duality. This Idea Must Die: Scientific Theories That Are Blocking Progress J Brockman 25–28 New York: Harper Perennial [Google Scholar]
42. Greed SM, Shortle D. 42.  1993. Patterns of nonadditivity between pairs of stability mutations in staphylococcal nuclease?. Biochemistry 32:10131–39 [Google Scholar]
43. Gunasekaran K, Buyong M, Nussinov R. 43.  2004. Is allostery an intrinsic property of all dynamic proteins?. Proteins 57:433–43 [Google Scholar]
44. Hernandez JV, Kay ER, Leigh DA. 44.  2004. A reversible synthetic rotary molecular motor. Science 306:1532–37 [Google Scholar]
45. Hidalgo P, MacKinnon R. 45.  1995. Revealing the architecture of a K⁺ channel pore through mutant cycles with a peptide inhibitor. Science 268:307–10 [Google Scholar]
46. Hill TL. 46.  1983. Some general principles in free energy transduction. PNAS 80:2922–25 [Google Scholar]
47. Hill TL, Eisenberg E. 47.  1981. Can free energy transduction be localized at some crucial part of the enzymatic cycle?. Q. Rev. Biophys. 14:463–511 [Google Scholar]
48. Holt JM, Ackers GK. 48.  1995. The pathway of allosteric control as revealed by hemoglobin intermediate states. FASEB J 9:210–18 [Google Scholar]
49. Horovitz A, Fersht AR. 49.  1990. Strategy for analyzing the co-operativity of intramolecular interactions in peptides and proteins. J. Mol. Biol. 214:613–17 [Google Scholar]
50. Howard J. 50.  2001. Mechanics of Motor Proteins and the Cytoskeleton Sunderland, MA: Sinauer
51. Ilyin VA, Temple B, Hu M, Li G, Yin Y. 51.  et al. 2000. 2.9 Å Crystal structure of ligand-free tryptophanyl-tRNA synthetase: Domain movements fragment the adenine nucleotide binding site. Protein Sci 9:218–31 [Google Scholar]
52. Jaffe R. 52.  1995. Where does the proton really get its spin?. Phys. Today 48:24–30 [Google Scholar]
53. Jencks WP. 53.  1975. Binding energy, specificity, and enzymatic catalysis: the Circe effect. Adv. Enzymol. Relat. Areas Mol. Biol. 43:219–410 [Google Scholar]
54. Jencks WP. 54.  1980. The utilization of binding energy in coupled vectorial processes. Adv. Enzymol. Relat. Areas Mol. Biol. 51:75–106 [Google Scholar]
55. Jencks WP. 55.  1981. On the attribution and additivity of binding energies. PNAS 78:4046–50 [Google Scholar]
56. Jencks WP. 56.  1987. Catalysis in Chemistry and Enzymology New York: Dover
57. Jencks WP. 57.  1989. Utilization of binding energy and coupling rules for active transport and other coupled vectorial processes. Methods Enzymol 171:145–64 [Google Scholar]
58. Jencks WP. 58.  1994. Reaction mechanisms, catalysis, and movement. Protein Sci 3:2459–64 [Google Scholar]
59. Kapustina M, Carter CW Jr.. 59.  2006. Computational studies of tryptophanyl-tRNA synthetase ligand binding and conformational stability. J. Mol. Biol. 362:1159–80 [Google Scholar]
60. Kapustina M, Hermans J, Carter CW Jr.. 60.  2006. Potential of mean force estimation of the relative magnitude of the effect of errors in molecular mechanics approximations. J. Mol. Biol. 362:1177–80 [Google Scholar]
61. Kapustina M, Weinreb V, Li L, Kuhlman B, Carter CW Jr.. 61.  2007. A conformational transition state accompanies tryptophan activation by B.stearothermophilus tryptophanyl-tRNA synthetase. Structure 15:1272–84 [Google Scholar]
62. Laowanapiban P, Kapustina M, Vonrhein C, Delarue M, Koehl P, Carter CW Jr.. 62.  2009. Independent saturation of three TrpRS subsites generates a partially-assembled state similar to those observed in molecular simulations. PNAS 106:1790–95 [Google Scholar]
63. Laowanapiban P, Kapustina M, Vonrhein C, Delarue M, Koehl P, Carter CW Jr.. 63.  2009. Independent saturation of three TrpRS subsites generates a partially-assembled state similar to those observed in molecular simulations. PNAS 106:1790–95 [Google Scholar]
64. Li L, Carter CW Jr.. 64.  2013. Full implementation of the genetic code by tryptophanyl-tRNA synthetase requires intermodular coupling. J. Biol. Chem. 288:34736–45 [Google Scholar]
65. Li L, Francklyn C, Carter CW Jr.. 65.  2013. Aminoacylating Urzymes challenge the RNA World hypothesis. J. Biol. Chem. 288:26856–63 [Google Scholar]
66. Li L, Weinreb V, Francklyn C, Carter CW Jr.. 66.  2011. Histidyl-tRNA synthetase Urzymes: Class I and II aminoacyl-tRNA synthetase Urzymes have comparable catalytic activities for cognate amino acid activation. J. Biol. Chem. 286:10387–95 [Google Scholar]
67. Liao J-C, Sun S, Chandler D, Oster G. 67.  2004. The conformational states of Mg•ATP in water. Eur. Biophys. J. 33:29–37 [Google Scholar]
68. Lockless SW, Ranganathan R. 68.  1999. Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286:295–99 [Google Scholar]
69. Long SB, Campbell EB, MacKinnon R. 69.  2005. Crystal structure of a mammalian voltage-dependent Shaker family K⁺ channel. Science 309:897–903 [Google Scholar]
70. Lymn RW. 70.  1979. Kinetic analysis of myosin and actomyosin ATPase. Annu. Rev. Biophys. Bioeng. 8:145–63 [Google Scholar]
71. Lymn RW, Taylor EW. 71.  1970. Transient state phosphate production in the hydrolysis of nucleoside triphosphates by myosin. Biochemistry 9:2975–83 [Google Scholar]
72. Lymn RW, Taylor EW. 72.  1971. Mechanism of adenosine triphosphate hydrolysis by actomyosin. Biochemistry 10:4617–24 [Google Scholar]
73. Martinez L, Jimenez-Rodriguez M, Gonzalez-Rivera K, Williams T, Li L. 73.  et al. 2015. Functional Class I and II amino acid activating enzymes can be coded by opposite strands of the same gene. J. Biol. Chem. 290:19710–25 [Google Scholar]
74. Matouschek A, Fersht AR. 74.  1991. Protein engineering in analysis of protein folding pathways and stability. Methods Enzymol 202:82–112 [Google Scholar]
75. Monod J, Changeux J-P, Jacob F. 75.  1963. Allosteric proteins and cellular control systems. J. Mol. Biol. 6:306–29 [Google Scholar]
76. Monod J, Wyman J, Changeux J-P. 76.  1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88–118 [Google Scholar]
77. Motlagh HN, Wrabl JO, Li J, Hilser VJ. 77.  2014. The ensemble nature of allostery. Nature 508:331–39 [Google Scholar]
78. Onsager L, Machlup S. 78.  1953. Fluctuations and irreversible processes. Phys. Rev. 91:1505–12 [Google Scholar]
79. Ovchinnikov V, Karplus M, Vanden-Eijnden E. 79.  2011. Free energy of conformational transition paths in biomolecules: the string method and its application to myosin VI. J. Chem. Phys. 134:085103 [Google Scholar]
80. Ovchinnikov V, Trouta BL, Karplus M. 80.  2010. Mechanical coupling in myosin V: a simulation study. J. Mol. Biol. 395:815–35 [Google Scholar]
81. Perutz MF. 81.  1970. Stereochemistry of cooperative effects of hemoglobin. Nature 228:726–39 [Google Scholar]
82. Petit CM, Zhang J, Fuentes EJ, Lee AL. 82.  2009. Hidden dynamic allostery in a PDZ domain. PNAS 46:18249–54 [Google Scholar]
83. Pham Y, Kuhlman B, Butterfoss GL, Hu H, Weinreb V, Carter CW Jr.. 83.  2010. Tryptophanyl-tRNA synthetase Urzyme: a model to recapitulate molecular evolution and investigate intramolecular complementation. J. Biol. Chem. 285:38590–601 [Google Scholar]
84. Pham Y, Li L, Kim A, Weinreb V, Butterfoss G. 84.  et al. 2007. A minimal TrpRS catalytic domain supports sense/antisense ancestry of Class I and II aminoacyl-tRNA synthetases. Mol. Cell 25:851–62 [Google Scholar]
85. Prasad BR, Warshel A. 85.  2011. Prechemistry versus preorganization in DNA replication fidelity. Proteins 79:2900–19 [Google Scholar]
86. Pressé S, Ghosh K, Dill KA. 86.  2011. Modeling stochastic dynamics in biochemical systems with feedback using maximum caliber. J. Phys. Chem. B115:6202–12 [Google Scholar]
87. Rees DC, Howard JB. 87.  1999. Structural bioenergetics and energy transduction mechanisms. J. Mol. Biol. 293:343–50 [Google Scholar]
88. Retailleau P, Huang X, Yin Y, Hu M, Weinreb V. 88.  et al. 2003. Interconversion of ATP binding and conformational free energies by tryptophanyl-tRNA synthetase: structures of ATP bound to open and closed, pre-transition conformations. J. Mol. Biol. 325:39–63 [Google Scholar]
89. Retailleau P, Weinreb V, Hu M, Carter CW Jr.. 89.  2007. Crystal structure of tryptophanyl-tRNA synthetase complexed with adenosine-5′ tetraphosphate: evidence for distributed use of catalytic binding energy in amino acid activation by Class I aminoacyl-tRNA synthetases. J. Mol. Biol. 369:108–28 [Google Scholar]
90. Retailleau P, Yin Y, Hu M, Roach JM, Bricogne G. 90.  et al. 2001. High resolution experimental phases for tryptophanyl-tRNA synthetase (TrpRS) complexed with tryptophanyl-5′AMP. Acta Crystallogr. D 57:1595–608 [Google Scholar]
91. Rosenfeld SS, Houdusse A, Sweeney HL. 91.  2005. Magnesium regulates ADP dissociation from myosin V. J. Biol. Chem. 280:6072–79 [Google Scholar]
92. Roup AV, Bernstein DS, Neresov SG, Hadda WM, Chellaboina V. 92.  2003. Limit cycle analysis of the verge and Foliot clock escapement using impulsive differential equations and Poincaré maps. Int. J. Control 76:1685–98 [Google Scholar]
93. Sadovsky E, Yifrach O. 93.  2007. Principles underlying energetic coupling along an allosteric communication trajectory of a voltage-activated K channel. PNAS 104:19813–18 [Google Scholar]
94. Shirvanyants D, Ding F, Tsao D, Ramachandran S, Dokholyan NV. 94.  2012. Discrete molecular dynamics: an efficient and versatile simulation method for fine protein characterization. J. Phys. Chem. B 116:8375–82 [Google Scholar]
95. Smith FR, Ackers GK. 95.  1985. Experimental resolution of cooperative free energies for the ten ligation states of human hemoglobin. PNAS 82:5347–51 [Google Scholar]
96. Stockbridge RB, Wolfenden R. 96.  2009. The intrinsic reactivity of ATP and the catalytic proficiencies of kinases acting on glucose, N-acetylglucosamine, and homoserine. J. Biol. Chem. 284:22747–57 [Google Scholar]
97. Suel GM, Lockless SW, Wall MA, Ranganathan R. 97.  2003. Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat. Struct. Biol. 10:59–69 [Google Scholar]
98. Sunden F, Peck A, Salzman J, Ressl S, Herschlag D. 98.  2015. Extensive site-directed mutagenesis reveals interconnected functional units in the alkaline phosphatase active site. eLife 4:e06181 [Google Scholar]
99. Sweeney HL, Houdusse A. 99.  2010. Myosin VI rewrites the rules for myosin motors. Cell 141:573–82 [Google Scholar]
100. Sweeney HL, Houdusse A. 100.  2010. Structural and functional insights into the myosin motor mechanism. Annu. Rev. Biophys. 39:539–57 [Google Scholar]
101. Thomas PD, Dill KA. 101.  1996. Statistical potentials extracted from protein structures: How accurate are they?. J. Mol. Biol. 257:457–69 [Google Scholar]
102. Tsai C-J, Nussinov R. 102.  2014. A unified view of “how allostery works.”. PLOS Comput. Biol. 10:e1003394 [Google Scholar]
103. Vanden-Eijnden E, Venturolib M. 103.  2009. Revisiting the finite temperature string method for the calculation of reaction tubes and free energies. J. Chem. Phys. 130:194103 [Google Scholar]
104. Warshel A, Bora RP. 104.  2016. Perspective: defining and quantifying the role of dynamics in enzyme catalysis. J. Chem. Phys. 144:180901 [Google Scholar]
105. Weinkam P, Ponsb J, Sali A. 105.  2012. Structure-based model of allostery predicts coupling between distant sites. PNAS 109:4875–80 [Google Scholar]
106. Weinreb V, Carter CW Jr.. 106.  2008. Mg²⁺-free B.stearothermophilus tryptophanyl-tRNA synthetase activates tryptophan with a major fraction of the overall rate enhancement. J. Am. Chem. Soc. 130:1488–94 [Google Scholar]
107. Weinreb V, Li L, Carter CW Jr.. 107.  2012. A master switch couples Mg²⁺-assisted catalysis to domain motion in B.stearothermophilus tryptophanyl-tRNA synthetase. Structure 20:128–38 [Google Scholar]
108. Weinreb V, Li L, Chandrasekaran SN, Koehl P, Delarue M, Carter CW Jr.. 108.  2014. Enhanced amino acid selection in fully-evolved tryptophanyl-tRNA synthetase, relative to its Urzyme, requires domain movement sensed by the D1 Switch, a remote, dynamic packing motif. J. Biol. Chem. 289:4367–76 [Google Scholar]
109. Weinreb V, Li L, Kaguni LS, Campbell CL, Carter CW Jr.. 109.  2009. Mg2+-assisted catalysis by B.stearothermophilus TrpRS is promoted by allosteric effects. Structure 17:1–13 [Google Scholar]
110. Wolfenden R, Williams R. 110.  1983. Affinities of phosphoric acids, esters and amides for solvent water. J. Am. Chem. Soc. 105:1028–31 [Google Scholar]
111. Yifrach O. 111.  2004. Hill coefficient for estimating the magnitude of cooperativity in gating transitions of voltage-dependent ion channels. Biophys. J. 87:822–30 [Google Scholar]
112. Yifrach O, MacKinnon R. 112.  2002. Energetics of pore opening in a voltage-gated K channel. Cell 111:231–39 [Google Scholar]
113. Yin Y. 113.  1995. Crystallographic study of Bacillus stearothermophilus tryptophanyl-tRNA synthetase in the catalytic reaction PhD Thesis Univ. N.C. Chapel Hill: [Google Scholar]
114. Yin Y, Carter CW Jr.. 114.  1994. Quantitative analysis in the characterization and optimization of protein crystal growth. Acta Crystallogr. D 50:572–90 [Google Scholar]
115. Zandany N, Ovadia M, Orr I, Yifrach O. 115.  2008. Direct analysis of cooperativity in multisubunit allosteric proteins. PNAS 105:11697–702 [Google Scholar]
116. Zheng W, Brooks BR, Doniach S, Thirumalai D. 116.  2005. Network of dynamically important residues in the open/closed transition in polymerases is strongly conserved. Structure 13:565–77 [Google Scholar]