1932

Abstract

Proteins guide the flows of information, energy, and matter that make life possible by accelerating transport and chemical reactions, by allosterically modulating these reactions, and by forming dynamic supramolecular assemblies. In these roles, conformational change underlies functional transitions. Time-resolved X-ray diffraction methods characterize these transitions either by directly triggering sequences of functionally important motions or, more broadly, by capturing the motions of which proteins are capable. To date, most successful have been experiments in which conformational change is triggered in light-dependent proteins. In this review, I emphasize emerging techniques that probe the dynamic basis of function in proteins lacking natively light-dependent transitions and speculate about extensions and further possibilities. In addition, I review how the weaker and more distributed signals in these data push the limits of the capabilities of analytical methods. Taken together, these new methods are beginning to establish a powerful paradigm for the study of the physics of protein function.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-111622-091155
2023-05-09
2024-04-13
Loading full text...

Full text loading...

/deliver/fulltext/biophys/52/1/annurev-biophys-111622-091155.html?itemId=/content/journals/10.1146/annurev-biophys-111622-091155&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Adhikary R, Zimmermann J, Romesberg FE. 2017. Transparent window vibrational probes for the characterization of proteins with high structural and temporal resolution. Chem. Rev. 117:1927–69
    [Google Scholar]
  2. 2.
    Arnlund D, Johansson LC, Wickstrand C, Barty A, Williams GJ et al. 2014. Visualizing a protein quake with time-resolved X-ray scattering at a free-electron laser. Nat. Methods 11:923–26
    [Google Scholar]
  3. 3.
    Askerka M, Wang J, Brudvig GW, Batista VS. 2014. Structural changes in the oxygen-evolving complex of photosystem II induced by the S1 to S2 transition: a combined XRD and QM/MM study. Biochemistry 53:6860–62
    [Google Scholar]
  4. 4.
    Atakisi H, Moreau DW, Thorne RE. 2018. Effects of protein-crystal hydration and temperature on side-chain conformational heterogeneity in monoclinic lysozyme crystals. Acta Crystallogr. D 74:264–78
    [Google Scholar]
  5. 5.
    Austin RH, Beeson KW, Eisenstein L, Frauenfelder H, Gunsalus IC. 1975. Dynamics of ligand binding to myoglobin. Biochemistry 14:5355–73
    [Google Scholar]
  6. 6.
    Barends TR, Foucar L, Ardevol A, Nass K, Aquila A et al. 2015. Direct observation of ultrafast collective motions in CO myoglobin upon ligand dissociation. Science 350:445–50
    [Google Scholar]
  7. 7.
    Barstow B, Ando N, Kim CU, Gruner SM. 2008. Alteration of citrine structure by hydrostatic pressure explains the accompanying spectral shift. PNAS 105:13362–66
    [Google Scholar]
  8. 8.
    Ben-Chaim Y, Chanda B, Dascal N, Bezanilla F, Parnas I, Parnas H 2006. Movement of “gating charge” is coupled to ligand binding in a G-protein-coupled receptor. Nature 444:106–9
    [Google Scholar]
  9. 9.
    Ben-Chaim Y, Tour O, Dascal N, Parnas I, Parnas H. 2003. The M2 muscarinic G-protein-coupled receptor is voltage-sensitive. J. Biol. Chem. 278:22482–91
    [Google Scholar]
  10. 10.
    Bilderback DH, Moffat K, Szebenyi DME. 1984. Time-resolved Laue diffraction from protein crystals—instrumental considerations. Nuclear Instrum. Methods Phys. Res. A 222:245–51
    [Google Scholar]
  11. 11.
    Bock LV, Grubmuller H. 2022. Effects of cryo-EM cooling on structural ensembles. Nat. Commun. 13:1709
    [Google Scholar]
  12. 12.
    Boehr DD, McElheny D, Dyson HJ, Wright PE. 2006. The dynamic energy landscape of dihydrofolate reductase catalysis. Science 313:1638–42
    [Google Scholar]
  13. 13.
    Boomsma W, Ferkinghoff-Borg J, Lindorff-Larsen K. 2014. Combining experiments and simulations using the maximum entropy principle. PLOS Comput. Biol. 10:1003406
    [Google Scholar]
  14. 14.
    Bourgeois D, Schotte F, Brunori M, Vallone B. 2007. Time-resolved methods in biophysics. 6. Time-resolved Laue crystallography as a tool to investigate photo-activated protein dynamics. Photochem. Photobiol. Sci. 6:1047–56
    [Google Scholar]
  15. 15.
    Bozovic O, Jankovic B, Hamm P. 2022. Using azobenzene photocontrol to set proteins in motion. Nat. Rev. Chem. 6:112–24
    [Google Scholar]
  16. 16.
    Branden G, Neutze R. 2021. Advances and challenges in time-resolved macromolecular crystallography. Science 373:6558eaba0954
    [Google Scholar]
  17. 17.
    Bricogne G. 1997. Bayesian statistical viewpoint on structure determination: basic concepts and examples. Methods Enzymol. 276:361–423
    [Google Scholar]
  18. 18.
    Burnley BT, Afonine PV, Adams PD, Gros P. 2012. Modelling dynamics in protein crystal structures by ensemble refinement. eLife 1:e00311
    [Google Scholar]
  19. 19.
    Butryn A, Simon PS, Aller P, Hinchliffe P, Massad RN et al. 2021. An on-demand, drop-on-drop method for studying enzyme catalysis by serial crystallography. Nat. Commun. 12:4461
    [Google Scholar]
  20. 20.
    Calvey GD, Katz AM, Zielinski KA, Dzikovski B, Pollack L. 2020. Characterizing enzyme reactions in microcrystals for effective mix-and-inject experiments using X-ray free-electron lasers. Anal. Chem. 92:13864–70
    [Google Scholar]
  21. 21.
    Cao H, Skolnick J. 2019. Time-resolved x-ray crystallography capture of a slow reaction tetrahydrofolate intermediate. Struct. Dyn. 6:024701
    [Google Scholar]
  22. 22.
    Carini GA, Boutet S, Chollet M, Dragone A, Haller G et al. 2014. Experience with the CSPAD during dedicated detector runs at LCLS. J. Phys. Conf. Ser. 493:012011
    [Google Scholar]
  23. 23.
    Casanas A, Warshamanage R, Finke AD, Panepucci E, Olieric V et al. 2016. EIGER detector: application in macromolecular crystallography. Acta Crystallogr. D 72:1036–48
    [Google Scholar]
  24. 24.
    Cerutti DS, Case DA. 2019. Molecular dynamics simulations of macromolecular crystals. Wiley Interdiscip. Rev. Comput. Mol. Sci. 9:e1402
    [Google Scholar]
  25. 25.
    Chapman HN, Fromme P, Barty A, White TA, Kirian RA et al. 2011. Femtosecond X-ray protein nanocrystallography. Nature 470:73–77
    [Google Scholar]
  26. 26.
    Claesson E, Wahlgren WY, Takala H, Pandey S, Castillon L et al. 2020. The primary structural photoresponse of phytochrome proteins captured by a femtosecond X-ray laser. eLife 9:e53514
    [Google Scholar]
  27. 27.
    Coquelle N, Sliwa M, Woodhouse J, Schiro G, Adam V et al. 2018. Chromophore twisting in the excited state of a photoswitchable fluorescent protein captured by time-resolved serial femtosecond crystallography. Nat. Chem. 10:31–37
    [Google Scholar]
  28. 28.
    Dailey BP. 1964. Chemical shifts, ring currents, and magnetic anisotropy in aromatic hydrocarbons. J. Chem. Phys. 41:2304
    [Google Scholar]
  29. 29.
    Dalton KM, Greisman JB, Hekstra DR. 2022. A unifying Bayesian framework for merging X-ray diffraction data. Nat. Commun. 13:7764
    [Google Scholar]
  30. 30.
    Davies DW. 1961. The relation between theoretical and experimental diamagnetic susceptibilities for aromatic hydrocarbons. Nature 190:1102–3
    [Google Scholar]
  31. 31.
    De Zitter E, Coquelle N, Oeser P, Barends TRM, Colletier JP. 2022. Xtrapol8 enables automatic elucidation of low-occupancy intermediate-states in crystallographic studies. Commun. Biol. 5:640
    [Google Scholar]
  32. 32.
    DePonte DP, Weierstall U, Schmidt K, Warner J, Starodub D et al. 2008. Gas dynamic virtual nozzle for generation of microscopic droplet streams. J. Phys. D 41:195505
    [Google Scholar]
  33. 33.
    Dods R, Bath P, Morozov D, Gagner VA, Arnlund D et al. 2021. Ultrafast structural changes within a photosynthetic reaction centre. Nature 589:310–14
    [Google Scholar]
  34. 34.
    Dogutan DK, Nocera DG. 2019. Artificial photosynthesis at efficiencies greatly exceeding that of natural photosynthesis. Acc. Chem. Res. 52:3143–48
    [Google Scholar]
  35. 35.
    Echelmeier A, Cruz Villarreal J, Messerschmidt M, Kim D, Coe JD et al. 2020. Segmented flow generator for serial crystallography at the European X-ray free electron laser. Nat. Commun. 11:4511
    [Google Scholar]
  36. 36.
    Fraser JS, Clarkson MW, Degnan SC, Erion R, Kern D, Alber T. 2009. Hidden alternative structures of proline isomerase essential for catalysis. Nature 462:669–73
    [Google Scholar]
  37. 37.
    Frauenfelder H, Petsko GA, Tsernoglou D. 1979. Temperature-dependent X-ray diffraction as a probe of protein structural dynamics. Nature 280:558–63
    [Google Scholar]
  38. 38.
    Fuller FD, Gul S, Chatterjee R, Burgie ES, Young ID et al. 2017. Drop-on-demand sample delivery for studying biocatalysts in action at X-ray free-electron lasers. Nat. Methods 14:443–49
    [Google Scholar]
  39. 39.
    Fulop JA, Tzortzakis S, Kampfrath T. 2020. Laser-driven strong-field terahertz sources. Adv. Opt. Mater. 8:1900681
    [Google Scholar]
  40. 40.
    Garcia-Bonete MJ, Katona G 2019. Bayesian machine learning improves single-wavelength anomalous diffraction phasing. Acta Crystallogr. A 75:851–60
    [Google Scholar]
  41. 41.
    Genick UK. 2007. Structure-factor extrapolation using the scalar approximation: theory, applications and limitations. Acta Crystallogr. D 63:1029–41
    [Google Scholar]
  42. 42.
    Genick UK, Borgstahl GEO, Ng K, Ren Z, Pradervand C et al. 1997. Structure of a protein photocycle intermediate by millisecond time-resolved crystallography. Science 275:1471–75
    [Google Scholar]
  43. 43.
    Gevorkov Y, Barty A, Brehm W, White TA, Tolstikova A et al. 2020. pinkIndexer—a universal indexer for pink-beam X-ray and electron diffraction snapshots. Acta Crystallogr. A 76:121–31
    [Google Scholar]
  44. 44.
    Ginn HM, Messerschmidt M, Ji X, Zhang H, Axford D et al. 2015. Structure of CPV17 polyhedrin determined by the improved analysis of serial femtosecond crystallographic data. Nat. Commun. 6:6435
    [Google Scholar]
  45. 45.
    Gudmundson M, Kim S, Wu M, Ishida T, Hadadd Momeni M et al. 2014. Structural and electronic snapshots during the transition from a Cu (II) to Cu (I) metal center of a lytic polysaccharide monooxygenase by X-ray photoreduction. J. Biol. Chem. 289:2718782–92
    [Google Scholar]
  46. 46.
    Gisriel C, Coe J, Letrun R, Yefanov OM, Luna-Chavez C et al. 2019. Membrane protein megahertz crystallography at the European XFEL. Nat. Commun. 10:5021
    [Google Scholar]
  47. 47.
    Graber T, Anderson S, Brewer H, Chen YS, Cho HS et al. 2011. BioCARS: a synchrotron resource for time-resolved X-ray science. J. Synchrotron Radiat. 18:658–70
    [Google Scholar]
  48. 48.
    Grünbein ML, Gorel A, Foucar L, Carbajo S, Colocho W et al. 2021. Effect of X-ray free-electron laser-induced shockwaves on haemoglobin microcrystals delivered in a liquid jet. Nat. Commun. 12:1672
    [Google Scholar]
  49. 49.
    Hajdu J, Machin PA, Campbell JW, Greenhough TJ, Clifton IJ et al. 1987. Millisecond X-ray-diffraction and the first electron-density map from Laue photographs of a protein crystal. Nature 329:178–81
    [Google Scholar]
  50. 50.
    Heath GR, Scheuring S. 2019. Advances in high-speed atomic force microscopy (HS-AFM) reveal dynamics of transmembrane channels and transporters. Curr. Opin. Struct. Biol. 57:93–102
    [Google Scholar]
  51. 51.
    Hekstra DR, White KI, Socolich MA, Henning RW, Srajer V, Ranganathan R. 2016. Electric field-stimulated protein mechanics. Nature 540:400–5
    [Google Scholar]
  52. 52.
    Henry L, Panman MR, Isaksson L, Claesson E, Kosheleva I et al. 2020. Real-time tracking of protein unfolding with time-resolved x-ray solution scattering. Struct. Dyn. 7:054702
    [Google Scholar]
  53. 53.
    Hille B. 2001. Ion Channels of Excitable Membranes Sunderland, MA: Sinauer Assoc.
  54. 54.
    Ho BK, Agard DA. 2010. Conserved tertiary couplings stabilize elements in the PDZ fold, leading to characteristic patterns of domain conformational flexibility. Protein Sci. 19:398–411
    [Google Scholar]
  55. 55.
    Holton JM, Classen S, Frankel KA, Tainer JA. 2014. The R-factor gap in macromolecular crystallography: an untapped potential for insights on accurate structures. FEBS J. 281:4046–60
    [Google Scholar]
  56. 56.
    Hosseinizadeh A, Breckwoldt N, Fung R, Sepehr R, Schmidt M et al. 2021. Few-fs resolution of a photoactive protein traversing a conical intersection. Nature 599:697–701
    [Google Scholar]
  57. 57.
    Howell PL, Smith GD. 1992. Identification of heavy-atom derivatives by normal probability methods. J. Appl. Crystallogr. 25:81–86
    [Google Scholar]
  58. 58.
    Ibrahim M, Fransson T, Chatterjee R, Cheah MH, Hussein R et al. 2020. Untangling the sequence of events during the S2 → S3 transition in photosystem II and implications for the water oxidation mechanism. PNAS 117:12624–35
    [Google Scholar]
  59. 59.
    Ihee H, Rajagopal S, Srajer V, Pahl R, Anderson S et al. 2005. Visualizing reaction pathways in photoactive yellow protein from nanoseconds to seconds. PNAS 102:7145–50
    [Google Scholar]
  60. 60.
    Keedy DA, Fraser JS, van den Bedem H. 2015. Exposing hidden alternative backbone conformations in X-ray crystallography using qFit. PLOS Comput. Biol. 11:e1004507
    [Google Scholar]
  61. 61.
    Keedy DA, Hill ZB, Biel JT, Kang E, Rettenmaier TJ et al. 2018. An expanded allosteric network in PTP1B by multitemperature crystallography, fragment screening, and covalent tethering. eLife 7:e36307
    [Google Scholar]
  62. 62.
    Kern J, Chatterjee R, Young ID, Fuller FD, Lassalle L et al. 2018. Structures of the intermediates of Kok's photosynthetic water oxidation clock. Nature 563:421–25
    [Google Scholar]
  63. 63.
    Kim D, Echelmeier A, Cruz Villarreal J, Gandhi S, Quintana S et al. 2019. Electric triggering for enhanced control of droplet generation. Anal. Chem. 91:9792–99
    [Google Scholar]
  64. 64.
    Kim KH, Muniyappan S, Oang KY, Kim JG, Nozawa S et al. 2012. Direct observation of cooperative protein structural dynamics of homodimeric hemoglobin from 100 ps to 10 ms with pump-probe X-ray solution scattering. J. Am. Chem. Soc. 134:7001–8
    [Google Scholar]
  65. 65.
    Knapp JE, Pahl R, Srajer V, Royer WE. 2006. Allosteric action in real time: time-resolved crystallographic studies of a cooperative dimeric hemoglobin. PNAS 103:7649–54
    [Google Scholar]
  66. 66.
    Kroon-Batenburg LM, Schreurs AM, Ravelli RB, Gros P. 2015. Accounting for partiality in serial crystallography using ray-tracing principles. Acta Crystallogr. D 71:1799–811
    [Google Scholar]
  67. 67.
    Kupitz C, Basu S, Grotjohann I, Fromme R, Zatsepin NA et al. 2014. Serial time-resolved crystallography of photosystem II using a femtosecond X-ray laser. Nature 513:261–65
    [Google Scholar]
  68. 68.
    Lee SJ, Kim TW, Kim JG, Yang C, Yun SR et al. 2022. Light-induced protein structural dynamics in bacteriophytochrome revealed by time-resolved x-ray solution scattering. Sci. Adv. 8:eabm6278
    [Google Scholar]
  69. 69.
    Levantino M, Schiro G, Lemke HT, Cottone G, Glownia JM et al. 2015. Ultrafast myoglobin structural dynamics observed with an X-ray free-electron laser. Nat. Commun. 6:6772
    [Google Scholar]
  70. 70.
    Lundholm IV, Rodilla H, Wahlgren WY, Duelli A, Bourenkov G et al. 2015. Terahertz radiation induces non-thermal structural changes associated with Frohlich condensation in a protein crystal. Struct. Dyn. 2:054702
    [Google Scholar]
  71. 71.
    Matthews BW, Czerwinski EW. 1975. Local scaling: a method to reduce systematic errors in isomorphous replacement and anomalous scattering measurements. Acta Crystallogr. A 31:480–87
    [Google Scholar]
  72. 72.
    Meents A, Wiedorn MO, Srajer V, Henning R, Sarrou I et al. 2017. Pink-beam serial crystallography. Nat. Commun. 8:1281
    [Google Scholar]
  73. 73.
    Meisburger SP, Case DA, Ando N. 2020. Diffuse X-ray scattering from correlated motions in a protein crystal. Nat. Commun. 11:1271
    [Google Scholar]
  74. 74.
    Mendez D, Bolotovsky R, Bhowmick A, Brewster AS, Kern J et al. 2020. Beyond integration: modeling every pixel to obtain better structure factors from stills. IUCrJ 7:1151–67
    [Google Scholar]
  75. 75.
    Moffat K, Szebenyi D, Bilderback D. 1984. X-ray Laue diffraction from protein crystals. Science 223:1423–25
    [Google Scholar]
  76. 76.
    Monteiro DCF, Amoah E, Rogers C, Pearson AR. 2021. Using photocaging for fast time-resolved structural biology studies. Acta Crystallogr. D 77:1218–32
    [Google Scholar]
  77. 77.
    Mozzanica A, Bergamaschi A, Brueckner M, Cartier S, Dinapoli R et al. 2016. Characterization results of the JUNGFRAU full scale readout ASIC. J. Instrum. 11:C02047
    [Google Scholar]
  78. 78.
    Nakamura T, Zhao Y, Yamagata Y, Hua Y-j, Yang W 2012. Watching DNA polymerase η make a phosphodiester bond. Nature 487:196–201
    [Google Scholar]
  79. 79.
    Nass K, Bacellar C, Cirelli C, Dworkowski F, Gevorkov Y et al. 2021. Pink-beam serial femtosecond crystallography for accurate structure-factor determination at an X-ray free-electron laser. IUCrJ 8:905–20
    [Google Scholar]
  80. 80.
    Nass K, Gorel A, Abdullah MM, Martin AV, Kloos M et al. 2020. Structural dynamics in proteins induced by and probed with X-ray free-electron laser pulses. Nat. Commun. 11:1814
    [Google Scholar]
  81. 81.
    Neuman KC, Nagy A. 2008. Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods 5:491–505
    [Google Scholar]
  82. 82.
    Neutze R, Wouts R, van der Spoel D, Weckert E, Hajdu J 2000. Potential for biomolecular imaging with femtosecond X-ray pulses. Nature 406:752–57
    [Google Scholar]
  83. 83.
    Nogly P, Weinert T, James D, Carbajo S, Ozerov D et al. 2018. Retinal isomerization in bacteriorhodopsin captured by a femtosecond x-ray laser. Science 361:eaat0094
    [Google Scholar]
  84. 84.
    Noji H, Yasuda R, Yoshida M, Kinosita K. 1997. Direct observation of the rotation of F1-ATPase. Nature 386:299–302
    [Google Scholar]
  85. 85.
    Oda K, Nomura T, Nakane T, Yamashita K, Inoue K et al. 2021. Time-resolved serial femtosecond crystallography reveals early structural changes in channelrhodopsin. eLife 10:e62389
    [Google Scholar]
  86. 86.
    Olmos JL Jr., Pandey S, Martin-Garcia JM, Calvey G, Katz A et al. 2018. Enzyme intermediates captured “on the fly” by mix-and-inject serial crystallography. BMC Biol. 16:59
    [Google Scholar]
  87. 87.
    Pande K, Hutchison CD, Groenhof G, Aquila A, Robinson JS et al. 2016. Femtosecond structural dynamics drives the trans/cis isomerization in photoactive yellow protein. Science 352:725–29
    [Google Scholar]
  88. 88.
    Pande VS, Beauchamp K, Bowman GR. 2010. Everything you wanted to know about Markov State Models but were afraid to ask. Methods 52:99–105
    [Google Scholar]
  89. 89.
    Pandey S, Bean R, Sato T, Poudyal I, Bielecki J et al. 2020. Time-resolved serial femtosecond crystallography at the European XFEL. Nat. Methods 17:73–78
    [Google Scholar]
  90. 90.
    Pandey S, Calvey G, Katz AM, Malla TN, Koua FHM et al. 2021. Observation of substrate diffusion and ligand binding in enzyme crystals using high-repetition-rate mix-and-inject serial crystallography. IUCrJ 8:878–95
    [Google Scholar]
  91. 91.
    Pearlman SM, Serber Z, Ferrell JE Jr. 2011. A mechanism for the evolution of phosphorylation sites. Cell 147:934–46
    [Google Scholar]
  92. 92.
    Read RJ. 1990. Structure-factor probabilities for related structures. Acta Crystallogr. A 46:900–12
    [Google Scholar]
  93. 93.
    Ren Z, Moffat K. 1995. Quantitative analysis of synchrotron Laue diffraction patterns in macromolecular crystallography. J. Appl. Crystallogr. 28:461–81
    [Google Scholar]
  94. 94.
    Ren Z, Perman B, Srajer V, Teng TY, Pradervand C et al. 2001. A molecular movie at 1.8 A resolution displays the photocycle of photoactive yellow protein, a eubacterial blue-light receptor, from nanoseconds to seconds. Biochemistry 40:13788–801
    [Google Scholar]
  95. 95.
    Roedig P, Ginn HM, Pakendorf T, Sutton G, Harlos K et al. 2017. High-speed fixed-target serial virus crystallography. Nat. Methods 14:805–10
    [Google Scholar]
  96. 96.
    Roessler CG, Agarwal R, Allaire M, Alonso-Mori R, Andi B et al. 2016. Acoustic injectors for drop-on-demand serial femtosecond crystallography. Structure 24:631–40
    [Google Scholar]
  97. 97.
    Sanishvili R, Yoder DW, Pothineni SB, Rosenbaum G, Xu SL et al. 2011. Radiation damage in protein crystals is reduced with a micron-sized X-ray beam. PNAS 108:6127–32
    [Google Scholar]
  98. 98.
    Sauter NK, Echols N, Adams PD, Zwart PH, Kern J et al. 2016. No observable conformational changes in PSII. Nature 533:E1–E2
    [Google Scholar]
  99. 99.
    Schlichting I, Almo SC, Rapp G, Wilson K, Petratos K et al. 1990. Time-resolved X-ray crystallographic study of the conformational change in Ha-Ras p21 protein on GTP hydrolysis. Nature 345:309–15
    [Google Scholar]
  100. 100.
    Schmidt M. 2013. Mix and inject: reaction initiation by diffusion for time-resolved macromolecular crystallography. Adv. Condens. Matter Phys. 2013:167276
    [Google Scholar]
  101. 101.
    Schmidt M. 2019. Time-resolved macromolecular crystallography at pulsed X-ray sources. Int. J. Mol. Sci. 20:1401
    [Google Scholar]
  102. 102.
    Schmidt M, Rajagopal S, Ren Z, Moffat K. 2003. Application of singular value decomposition to the analysis of time-resolved macromolecular x-ray data. Biophys. J. 84:2112–29
    [Google Scholar]
  103. 103.
    Sekhar A, Kay LE. 2013. NMR paves the way for atomic level descriptions of sparsely populated, transiently formed biomolecular conformers. PNAS 110:12867–74
    [Google Scholar]
  104. 104.
    Sharp K, Skinner JJ. 2006. Pump-probe molecular dynamics as a tool for studying protein motion and long range coupling. Proteins 65:347–61
    [Google Scholar]
  105. 105.
    Sierra RG, Laksmono H, Kern J, Tran R, Hattne J et al. 2012. Nanoflow electrospinning serial femtosecond crystallography. Acta Crystallogr. D 68:1584–87
    [Google Scholar]
  106. 106.
    Srajer V, Ren Z, Teng TY, Schmidt M, Ursby T et al. 2001. Protein conformational relaxation and ligand migration in myoglobin: a nanosecond to millisecond molecular movie from time-resolved Laue X-ray diffraction. Biochemistry 40:13802–15
    [Google Scholar]
  107. 107.
    Srajer V, Teng T, Ursby T, Pradervand C, Ren Z et al. 1996. Photolysis of the carbon monoxide complex of myoglobin: nanosecond time-resolved crystallography. Science 274:1726–29
    [Google Scholar]
  108. 108.
    Stauch B, Cherezov V. 2018. Serial femtosecond crystallography of G protein-coupled receptors. Annu. Rev. Biophys. 47:377–97
    [Google Scholar]
  109. 109.
    Stiller JB, Otten R, Haussinger D, Rieder PS, Theobald DL, Kern D. 2022. Structure determination of high-energy states in a dynamic protein ensemble. Nature 603:528–35
    [Google Scholar]
  110. 110.
    Suga M, Akita F, Sugahara M, Kubo M, Nakajima Y et al. 2017. Light-induced structural changes and the site of O=O bond formation in PSII caught by XFEL. Nature 543:131–35
    [Google Scholar]
  111. 111.
    Suga M, Akita F, Yamashita K, Nakajima Y, Ueno G et al. 2019. An oxyl/oxo mechanism for oxygen-oxygen coupling in PSII revealed by an x-ray free-electron laser. Science 366:334–38
    [Google Scholar]
  112. 112.
    Sui S, Wang YX, Dimitrakopoulos C, Perry SL. 2018. A graphene-based microfluidic platform for electrocrystallization and in situ X-ray diffraction. Crystals 8:76
    [Google Scholar]
  113. 113.
    Tao X, Lee A, Limapichat W, Dougherty DA, MacKinnon R. 2010. A gating charge transfer center in voltage sensors. Science 328:67–73
    [Google Scholar]
  114. 114.
    Tenboer J, Basu S, Zatsepin N, Pande K, Milathianaki D et al. 2014. Time-resolved serial crystallography captures high-resolution intermediates of photoactive yellow protein. Science 346:1242–46
    [Google Scholar]
  115. 115.
    Tripathi S, Srajer V, Purwar N, Henning R, Schmidt M. 2012. pH dependence of the photoactive yellow protein photocycle investigated by time-resolved crystallography. Biophys. J. 102:325–32
    [Google Scholar]
  116. 116.
    Uervirojnangkoorn M, Zeldin OB, Lyubimov AY, Hattne J, Brewster AS et al. 2015. Enabling X-ray free electron laser crystallography for challenging biological systems from a limited number of crystals. eLife 4:e05421
    [Google Scholar]
  117. 117.
    van den Bedem H, Bhabha G, Yang K, Wright PE, Fraser JS et al. 2013. Automated identification of functional dynamic networks from X-ray crystallography. Nat. Methods 10:896–902
    [Google Scholar]
  118. 118.
    van Driel TB, Nelson S, Armenta R, Blaj G, Boo S et al. 2020. The ePix10k 2-megapixel hard X-ray detector at LCLS. J. Synchrotron. Radiat. 27:608–15
    [Google Scholar]
  119. 119.
    van Thor JJ, Warren MR, Lincoln CN. 2014. Signal to noise considerations for single crystal femtosecond time resolved crystallography of Photoactive Yellow Protein. Faraday Discuss. 171:439–55
    [Google Scholar]
  120. 120.
    Wan Q, Bennett BC, Wymore T, Li Z, Wilson MA et al. 2021. Capturing the catalytic proton of dihydrofolate reductase: implications for general acid-base catalysis. ACS Catal. 11:5873–84
    [Google Scholar]
  121. 121.
    White TA, Mariani V, Brehm W, Yefanov O, Barty A et al. 2016. Recent developments in CrystFEL. J. Appl. Crystallogr. 49:680–89
    [Google Scholar]
  122. 122.
    Winter G, Waterman DG, Parkhurst JM, Brewster AS, Gildea RJ et al. 2018. DIALS: implementation and evaluation of a new integration package. Acta Crystallogr. D 74:85–97
    [Google Scholar]
  123. 123.
    Wohri AB, Katona G, Johansson LC, Fritz E, Malmerberg E et al. 2010. Light-induced structural changes in a photosynthetic reaction center caught by Laue diffraction. Science 328:630–33
    [Google Scholar]
  124. 124.
    Wolff AM, Nango E, Young ID, Brewster AS, Kubo M et al. 2022. Mapping protein dynamics at high-resolution with temperature-jump X-ray crystallography. bioRxiv 2022.06.10.495662. https://doi.org/10.1101/2022.06.10.495662
  125. 125.
    Woodhouse J, Nass Kovacs G, Coquelle N, Uriarte LM, Adam V et al. 2020. Photoswitching mechanism of a fluorescent protein revealed by time-resolved crystallography and transient absorption spectroscopy. Nat. Commun. 11:741
    [Google Scholar]
  126. 126.
    Yun JH, Li X, Yue J, Park JH, Jin Z et al. 2021. Early-stage dynamics of chloride ion-pumping rhodopsin revealed by a femtosecond X-ray laser. PNAS 118:e2020486118
    [Google Scholar]
  127. 127.
    Zeldin OB, Brockhauser S, Bremridge J, Holton JM, Garman EF. 2013. Predicting the X-ray lifetime of protein crystals. PNAS 110:20551–56
    [Google Scholar]
  128. 128.
    Zhang XC, Shkurinov A, Zhang Y. 2017. Extreme terahertz science. Nat. Photonics 11:16–18
    [Google Scholar]
  129. 129.
    Zhu DL, Sun YW, Schafer DW, Shi HL, James JH et al. 2017. Development of a hard X-ray split-delay system at the Linac Coherent Light Source. Proceedings of SPIE Optics + Optoelectronics: Advances in X-Ray Free-Electron Lasers Instrumentation IV, Prague, 24–27 April art. 10237OR Bellingham, WA: SPIE
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-111622-091155
Loading
/content/journals/10.1146/annurev-biophys-111622-091155
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error