1932

Abstract

My accidental encounter with protein hydrogen exchange (HX) at its very beginning and its continued development through my scientific career have led us to a series of advances in HX measurement, interpretation, and cutting edge biophysical applications. After some thoughts about how life brought me there, I take the opportunity to reflect on our early studies of allosteric structure and energy change in hemoglobin, the still-current protein folding problem, and our most recent forward-looking studies on protein machines.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-062122-093517
2023-05-09
2024-04-13
Loading full text...

Full text loading...

/deliver/fulltext/biophys/52/1/annurev-biophys-062122-093517.html?itemId=/content/journals/10.1146/annurev-biophys-062122-093517&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Bai Y. 2000. Kinetic evidence of an on-pathway intermediate in the folding of lysozyme. Protein Sci. 9:194–96
    [Google Scholar]
  2. 2.
    Bai Y, Englander JJ, Mayne L, Milne JS, Englander SW. 1995. Thermodynamic parameters from hydrogen exchange measurements. Methods Enzymol. 259:344–56
    [Google Scholar]
  3. 3.
    Bai Y, Milne JS, Mayne L, Englander SW. 1993. Primary structure effects on peptide group hydrogen exchange. Proteins Struct. Funct. Genet. 17:75–86
    [Google Scholar]
  4. 4.
    Bai Y, Milne JS, Mayne L, Englander SW. 1994. Protein stability parameters measured by hydrogen exchange. Proteins Struct. Funct. Genet. 20:4–14
    [Google Scholar]
  5. 5.
    Bai Y, Sosnick TR, Mayne L, Englander SW. 1995. Protein folding intermediates: native-state hydrogen exchange. Science 269:192–97
    [Google Scholar]
  6. 6.
    Baldwin RL. 2011. Early days of protein hydrogen exchange: 1954–1972. Proteins Struct. Funct. Bioinform. 79:2021–26
    [Google Scholar]
  7. 7.
    Bryngelson JD, Onuchic JN, Socci ND, Wolynes PG. 1995. Funnels, pathways, and the energy landscape of protein folding: a synthesis. Proteins 21:167–95
    [Google Scholar]
  8. 8.
    Bryngelson JD, Wolynes PG. 1987. Spin glasses and the statistical mechanics of protein folding. PNAS 84:7524–28
    [Google Scholar]
  9. 9.
    Calhoun DB, Vanderkooi JM, Englander SW. 1983. Penetration of small molecules into proteins studied by quenching of phosphorescence and fluorescence. Biochemistry 22:1533–39
    [Google Scholar]
  10. 10.
    Connelly GP, Bai Y, Jeng MF, Englander SW. 1993. Isotope effects in peptide group hydrogen exchange. Proteins Struct. Funct. Genet. 17:87–92
    [Google Scholar]
  11. 11.
    Eigen M. 1964. Proton transfer, acid-base catalysis, and enzymatic hydrolysis. Part I: elementary processes. Angew. Chem. Int. Ed. 3:1–19
    [Google Scholar]
  12. 12.
    Engen JR, Botzanowski T, Peterle D, Georgescauld F, Wales TE. 2021. Developments in hydrogen/deuterium exchange mass spectrometry. Anal. Chem. 93:567–82
    [Google Scholar]
  13. 13.
    Englander JJ, Calhoun DB, Englander SW. 1979. Measurement and calibration of peptide group hydrogen-deuterium exchange by ultraviolet spectrophotometry. Anal. Biochem. 92:517–24
    [Google Scholar]
  14. 14.
    Englander JJ, Louie G, McKinnie RE, Englander SW. 1998. Energetic components of the allosteric machinery in hemoglobin measured by hydrogen exchange. J. Mol. Biol. 284:1695–706
    [Google Scholar]
  15. 15.
    Englander JJ, Rogero JR, Englander SW. 1983. Identification of an allosterically sensitive unfolding unit in hemoglobin. J. Mol. Biol. 169:325–44
    [Google Scholar]
  16. 16.
    Englander JJ, Rogero JR, Englander SW. 1985. Protein hydrogen exchange studied by the fragment separation method. Anal. Biochem. 147:234–44
    [Google Scholar]
  17. 17.
    Englander JJ, Rumbley JN, Englander SW. 1998. Signal transmission between subunits in the hemoglobin T-state. J. Mol. Biol. 284:1707–16
    [Google Scholar]
  18. 18.
    Englander SW. 1963. A hydrogen method using tritium and sephadex. Application to ribonuclease. Biochemistry 2:798–807
    [Google Scholar]
  19. 19.
    Englander SW 1971. Oxygen changes hemoglobin's breathing. Probes of Structure and Function of Macromolecules and Membranes B Chance, C Lee, JK Blasie 389–92. New York: Academic
    [Google Scholar]
  20. 20.
    Englander SW. 2007. How do proteins fold and why? The Biomedical and Life Sciences Collection Henry Steward Talks London: https://hstalks.com/bs/636/
  21. 21.
    Englander SW, Crowe D. 1965. Rapid microdialysis and hydrogen exchange. Anal. Biochem. 12:579–84
    [Google Scholar]
  22. 22.
    Englander SW, Englander JJ, McKinnie RE, Ackers GK, Turner GJ et al. 1992. Hydrogen exchange measurement of the free energy of structural and allosteric change in hemoglobin. Science 256:1684–87
    [Google Scholar]
  23. 23.
    Englander SW, Kallenbach NR. 1983. Hydrogen exchange and structural dynamics of proteins and nucleic acids. Q. Rev. Biophys. 16:521–55
    [Google Scholar]
  24. 24.
    Englander SW, Mayne L. 2017. The case for defined protein folding pathways. PNAS 114:8253–58
    [Google Scholar]
  25. 25.
    Englander SW, Mayne L, Krishna MMG. 2007. Protein folding and misfolding: mechanism and principles. Q. Rev. Biophys. 40:287–326
    [Google Scholar]
  26. 26.
    Englander SW, Poulsen A. 1969. Hydrogen-tritium exchange of the random chain polypeptide. Biopolymers 7:329–39
    [Google Scholar]
  27. 27.
    Feng H, Zhou Z, Bai Y. 2005. A protein folding pathway with multiple folding intermediates at atomic resolution. PNAS 102:5026–31
    [Google Scholar]
  28. 28.
    Fenn JB, Mann M, Meng CK, Wong SF, Whitehouse CM. 1989. Electrospray ionization for mass spectrometry of large biomolecules. Science 246:64–71
    [Google Scholar]
  29. 29.
    Gellert MF, Englander SW. 1963. The molecular weight of rabbit myosin A by light scattering. Biochemistry 2:39–42
    [Google Scholar]
  30. 30.
    Georgescauld F, Popova K, Gupta AJ, Bracher A, Engen JR et al. 2014. GroEL/ES chaperonin modulates the mechanism and accelerates the rate of TIM-barrel domain folding. Cell 157:922–34
    [Google Scholar]
  31. 31.
    Henry ER, Mozzarelli A, Viappiani C, Abbruzzetti S, Bettati S et al. 2015. Experiments on hemoglobin in single crystals and silica gels distinguish among allosteric models. Biophys. J. 109:1264–72
    [Google Scholar]
  32. 32.
    Hoang L, Bédard S, Krishna MMG, Lin Y, Englander SW. 2002. Cytochrome c folding pathway: kinetic native-state hydrogen exchange. PNAS 99:12173–78
    [Google Scholar]
  33. 33.
    Hu W, Kan ZY, Mayne L, Englander SW. 2016. Cytochrome c folds through foldon-dependent native-like intermediates in an ordered pathway. PNAS 113:3809–14
    [Google Scholar]
  34. 34.
    Hu W, Walters BT, Kan ZY, Mayne L, Rosen LE et al. 2013. Stepwise protein folding at near amino acid resolution by hydrogen exchange and mass spectrometry. PNAS 110:7684–89
    [Google Scholar]
  35. 35.
    Hvidt A, Nielsen SO. 1966. Hydrogen exchange in proteins. Adv. Protein Chem. 21:287–386
    [Google Scholar]
  36. 36.
    Hwang W, Karplus M. 2019. Structural basis for power stroke vs. Brownian ratchet mechanisms of motor proteins. PNAS 116:19777–85
    [Google Scholar]
  37. 37.
    Jennings PA, Wright PE. 1993. Formation of a molten globule intermediate early in the kinetic folding pathway of apomyoglobin. Science 262:892–96
    [Google Scholar]
  38. 38.
    Kan ZY, Mayne L, Sevugan Chetty P, Englander SW 2011. ExMS: data analysis for HX MS experiments. J. Am. Soc. Mass. Spectrom. 22:1906–15
    [Google Scholar]
  39. 39.
    Kan ZY, Walters BT, Mayne L, Englander SW. 2013. Protein hydrogen exchange at residue resolution by proteolytic fragmentation mass spectrometry analysis. PNAS 110:16438–43
    [Google Scholar]
  40. 40.
    Kan ZY, Ye X, Skinner JJ, Mayne L, Englander SW. 2019. ExMS2: An integrated solution for hydrogen-deuterium exchange mass spectrometry data analysis. Anal. Chem. 91:7474–81
    [Google Scholar]
  41. 41.
    Khan YA, White KI, Brunger AT. 2021. The AAA+ superfamily: a review of the structural and mechanistic principles of these molecular machines. Crit. Rev. Biochem. Mol. Biol. 57:156–87
    [Google Scholar]
  42. 42.
    Krishna MMG, Englander SW. 2005. The N-terminal to C-terminal motif in protein folding and function. PNAS 102:1053–58
    [Google Scholar]
  43. 43.
    Krishna MMG, Englander SW. 2007. A unified mechanism for protein folding: predetermined pathways with optional errors. Protein Sci. 16:449–64
    [Google Scholar]
  44. 44.
    Krishna MMG, Lin Y, Englander SW. 2004. Protein misfolding: optional barriers, misfolded intermediates, and pathway heterogeneity. J. Mol. Biol. 343:1095–109
    [Google Scholar]
  45. 45.
    Krishna MMG, Maity H, Rumbley JN, Lin Y, Englander SW. 2006. Order of steps in the cytochrome c folding pathway: evidence for a sequential stabilization mechanism. J. Mol. Biol. 359:1411–20
    [Google Scholar]
  46. 46.
    Leopold PE, Montal M, Onuchic JN. 1992. Protein folding funnels: a kinetic approach to the sequence-structure relationship. PNAS 89:8721–25
    [Google Scholar]
  47. 47.
    Levinthal C. 1968. Are there pathways for protein folding. J. Chim. Phys. 65:44–45
    [Google Scholar]
  48. 48.
    Levinthal C. 1969. How to fold graciously. Univ. Illinois Bull. 67:4122–24
    [Google Scholar]
  49. 49.
    Linderstrøm-Lang K 1958. Deuterium exchange and protein structure. Symposium on Protein Structure A Neuberger London: Methuen
  50. 50.
    Linderstrøm-Lang KU, Schellman JA 1959. Protein structure and enzyme activity. The Enzymes PD Boyer, H Lardy, K Myrback 443–510. New York: Academic
    [Google Scholar]
  51. 51.
    Maity H, Maity M, Krishna MM, Mayne L, Englander SW. 2005. Protein folding: the stepwise assembly of foldon units. PNAS 102:4741–46
    [Google Scholar]
  52. 52.
    Mayne L, Kan ZY, Chetty PS, Ricciuti A, Walters BT, Englander SW. 2011. Many overlapping peptides for protein hydrogen exchange experiments by the fragment separation-mass spectrometry method. J. Am. Soc. Mass. Spectrom. 22:1898–905
    [Google Scholar]
  53. 53.
    Molday RS, Englander SW, Kallen RG. 1972. Primary structure effects on peptide group hydrogen exchange. Biochemistry 11:150–58
    [Google Scholar]
  54. 54.
    Monod J, Wyman J, Changeaux JP. 1965. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12:88–118
    [Google Scholar]
  55. 55.
    Nguyen D, Mayne L, Phillips MC, Englander SW. 2018. Reference parameters for protein hydrogen exchange rates. J. Am. Soc. Mass. Spectrom. 29:1936–39
    [Google Scholar]
  56. 56.
    Oliveberg M, Wolynes PG. 2005. The experimental survey of protein-folding energy landscapes. Q. Rev. Biophys. 38:245–88
    [Google Scholar]
  57. 57.
    Onuchic JN, Wolynes PG. 2004. Theory of protein folding. Curr. Opin. Struct. Biol. 14:70–75
    [Google Scholar]
  58. 58.
    Perutz MF. 1963. X-ray analysis of hemoglobin. Science 140:863–69
    [Google Scholar]
  59. 59.
    Perutz MF. 1970. Stereochemistry of cooperative effects in haemoglobin. Nature 228:726–39
    [Google Scholar]
  60. 60.
    Perutz MF. 1989. Mechanisms of cooperativity and allosteric regulation in proteins. Q. Rev. Biochem. 22:130–236
    [Google Scholar]
  61. 61.
    Perutz MF, Wilkinson AJ, Paoli M, Dodson GG. 1998. The stereochemical mechanism of the cooperative effects in hemoglobin revisited. Annu. Rev. Biophys. Biomol. Struct. 27:1–34
    [Google Scholar]
  62. 62.
    Petersen M, Barrick D. 2021. Analysis of tandem repeat protein folding using nearest-neighbor models. Annu. Rev. Biophys. 50:245–65
    [Google Scholar]
  63. 63.
    Puchades C, Sandate CR, Lander GC. 2020. The molecular principles governing the activity and functional diversity of AAA+ proteins. Nat. Rev. Mol. Cell Biol. 21:43–58
    [Google Scholar]
  64. 64.
    Roder H, Elove GA, Englander SW. 1988. Structural characterization of folding intermediates in cytochrome c by H-exchange labelling and proton NMR. Nature 335:700–4
    [Google Scholar]
  65. 65.
    Rogero JR, Englander JJ, Englander SW. 1986. Individual breathing reactions measured by functional labeling and hydrogen exchange methods. Methods Enzymol. 131:508–17
    [Google Scholar]
  66. 66.
    Rose GD. 2021. Protein folding—seeing is deceiving. Protein Sci. 30:1606–16
    [Google Scholar]
  67. 67.
    Rose GD. 2021. Reframing the protein folding problem: entropy as organizer. Biochemistry 60:3753–61
    [Google Scholar]
  68. 68.
    Sharp KA, Honig B. 1990. Electrostatic interactions in macromolecules: theory and applications. Annu. Rev. Biophys. Biophys. Chem. 19:301–32
    [Google Scholar]
  69. 69.
    Silverman JA, Harbury PB. 2002. The equilibrium unfolding pathway of a (β/α)8 barrel. J. Mol. Biol. 324:1031–40
    [Google Scholar]
  70. 70.
    Skinner JJ, Lim WK, Bedard S, Black BE, Englander SW. 2012. Protein dynamics viewed by hydrogen exchange. Protein Sci. 21:996–1005
    [Google Scholar]
  71. 71.
    Stigler J, Ziegler F, Gieseke A, Gebhardt JC, Rief M. 2011. The complex folding network of single calmodulin molecules. Science 334:512–16
    [Google Scholar]
  72. 72.
    Takei J, Pei W, Vu D, Bai Y. 2002. Populating partially unfolded forms by hydrogen exchange-directed protein engineering. Biochemistry 41:12308–12
    [Google Scholar]
  73. 73.
    Turner GJ, Galacteros F, Doyle ML, Hedlund B, Pettigrew DW et al. 1992. Mutagenic dissection of hemoglobin cooperativity: effects of amino acid alteration on subunit assembly of oxy and deoxy tetramers. Proteins 14:333–50
    [Google Scholar]
  74. 74.
    Walters BT, Ricciuti A, Mayne L, Englander SW. 2012. Minimizing back exchange in the hydrogen exchange-mass spectrometry experiment. J. Am. Soc. Mass. Spectrom. 23:2132–39
    [Google Scholar]
  75. 75.
    Wand AJ, Englander SW. 1985. Two-dimensional proton NMR studies of cytochrome c: assignment of the N-terminal helix. Biochemistry 25:5290–94
    [Google Scholar]
  76. 76.
    Wyman J Jr. 1964. Linked functions and reciprocal effects in hemoglobin: a second look. Adv. Protein Chem. 19:223–86
    [Google Scholar]
  77. 77.
    Xu Y, Mayne LC, Englander SW. 1998. Evidence for an unfolding and refolding pathway in cytochrome c. Nat. Struct. Biol 5:774–78
    [Google Scholar]
  78. 78.
    Yan S, Kennedy SD, Koide S. 2002. Thermodynamic and kinetic exploration of the energy landscape of B.burgdorferi OspA by native-state hydrogen exchange. J. Mol. Biol. 323:363–75
    [Google Scholar]
  79. 79.
    Ye X, Lin J, Mayne L, Shorter J, Englander SW. 2019. Hydrogen exchange reveals Hsp104 architecture, structural dynamics, and energetics in physiological solution. PNAS 116:7333–42
    [Google Scholar]
  80. 80.
    Ye X, Lin J, Mayne L, Shorter J, Englander SW. 2020. Structural and kinetic basis for the regulation and potentiation of Hsp104 function. PNAS 117:9384–92
    [Google Scholar]
  81. 81.
    Ye X, Mayne L, Englander SW. 2021. A conserved strategy for structure change and energy transduction in Hsp104 and other AAA+ protein motors. J. Biol. Chem. 297:101066
    [Google Scholar]
  82. 82.
    Ye X, Mayne L, Kan ZY, Englander SW. 2018. Folding of maltose binding protein outside of and in GroEL. PNAS 115:519–24
    [Google Scholar]
  83. 83.
    Yonetani T, Park SI, Tsuneshige A, Imai K, Kanaori K. 2002. Global allostery model of hemoglobin: modulation of O2 affinity, cooperativity, and Bohr effect by heterotropic allosteric effectors. J. Biol. Chem. 277:34508–20
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-062122-093517
Loading
/content/journals/10.1146/annurev-biophys-062122-093517
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