Variable-Temperature Native Mass Spectrometry for Studies of Protein Folding, Stabilities, Assembly, and Molecular Interactions

Literature Cited

1. 1.

   Anderson DE, Becktel WJ, Dahlquist FW. 1990. pH-Induced denaturation of proteins: A single salt bridge contributes 3–5 kcal/mol to the free energy of folding of T4 lysozyme. Biochemistry 29:2403–8
   [Google Scholar]
2. 2.

   Åqvist J, Kamerlin SCL. 2016. Conserved motifs in different classes of GTPases dictate their specific modes of catalysis. ACS Catal 6:1737–43
   [Google Scholar]
3. 3.

   Baldwin RL. 2008. The search for folding intermediates and the mechanism of protein folding. Annu. Rev. Biophys. 37:1–21
   [Google Scholar]
4. 4.

   Barron LD, Hecht L, Wilson G. 1997. The lubricant of life: a proposal that solvent water promotes extremely fast conformational fluctuations in mobile heteropolypeptide structure. Biochemistry 36:13143–47
   [Google Scholar]
5. 5.

   Bohrer BC, Merenbloom SI, Koeniger SL, Hilderbrand AE, Clemmer DE. 2008. Biomolecule analysis by ion mobility spectrometry. Annu. Rev. Anal. Chem. 1:293–327
   [Google Scholar]
6. 6.

   Borgia A, Williams PM, Clarke J. 2008. Single-molecule studies of protein folding. Annu. Rev. Biochem. 77:101–25
   [Google Scholar]
7. 7.

   Brockwell DJ, Radford SE. 2007. Intermediates: ubiquitous species on folding energy landscapes?. Curr. Opin. Struct. Biol. 17:30–37
   [Google Scholar]
8. 8.

   Brown CJ, Woodall DW, El-Baba TJ, Clemmer DE. 2019. Characterizing thermal transitions of IgG with mass spectrometry. J. Am. Soc. Mass Spectrom. 30:2438–45
   [Google Scholar]
9. 9.

   Bustamante C, Alexander L, Maciuba K, Kaiser CM 2020. Single-molecule studies of protein folding with optical tweezers. Annu. Rev. Biochem. 89:443–70
   [Google Scholar]
10. 10.

    Caro JA, Harpole KW, Kasinath V, Lim J, Granja J et al. 2017. Entropy in molecular recognition by proteins. PNAS 114:6563–68
    [Google Scholar]
11. 11.

    Colicelli J. 2004. Human RAS superfamily proteins and related GTPases. Sci. STKE 2004 RE13
    [Google Scholar]
12. 12.

    Conant CR, Fuller DR, El-Baba TJ, Zhang Z, Russell DH, Clemmer DE 2019. Substance P in solution: trans-to-cis configurational changes of penultimate prolines initiate non-enzymatic peptide bond cleavages. J. Am. Soc. Mass Spectrom. 30:919–31
    [Google Scholar]
13. 13.

    Conant CR, Fuller DR, Zhang Z, Woodall DW, Russell DH, Clemmer DE 2019. Substance P in the gas phase: conformational changes and dissociations induced by collisional activation in a drift tube. J. Am. Soc. Mass Spectrom. 30:932–45
    [Google Scholar]
14. 14.

    Cong X, Liu Y, Liu W, Liang X, Laganowsky A. 2017. Allosteric modulation of protein-protein interactions by individual lipid binding events. Nat. Commun. 8:2203
    [Google Scholar]
15. 15.

    Cong X, Liu Y, Liu W, Liang X, Russell DH, Laganowsky A. 2016. Determining membrane protein-lipid binding thermodynamics using native mass spectrometry. J. Am. Chem. Soc. 138:4346–49
    [Google Scholar]
16. 16.

    Conroy MJ, Durand A, Lupo D, Li XD, Bullough PA et al. 2007. The crystal structure of the Escherichia coli AmtB-GlnK complex reveals how GlnK regulates the ammonia channel. PNAS 104:1213–18
    [Google Scholar]
17. 17.

    Daggett V, Fersht A. 2003. The present view of the mechanism of protein folding. Nat. Rev. Mol. Cell Biol. 4:497–502
    [Google Scholar]
18. 18.

    Daneshfar R, Kitova EN, Klassen JS. 2004. Determination of protein-ligand association thermochemistry using variable-temperature nanoelectrospray mass spectrometry. J. Am. Chem. Soc. 126:4786–87
    [Google Scholar]
19. 19.

    Dill KA, Chan HS. 1997. From Levinthal to pathways to funnels. Nat. Struct. Biol. 4:10–19
    [Google Scholar]
20. 20.

    Downward J. 2003. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 3:11–22
    [Google Scholar]
21. 21.

    Eftink MR, Anusiem AC, Biltonen RL. 1983. Enthalpy-entropy compensation and heat capacity changes for protein-ligand interactions: general thermodynamic models and data for the binding of nucleotides to ribonuclease A. Biochemistry 22:3884–96
    [Google Scholar]
22. 22.

    Eisenberg DS, Crothers DM. 1979. Physical Chemistry: With Applications to the Life Sciences Menlo Park, CA: Benjamin/Cummings Publ.
23. 23.

    El-Baba TJ, Clemmer DE. 2019. Solution thermochemistry of concanavalin A tetramer conformers measured by variable-temperature ESI-IMS-MS. Int. J. Mass Spectrom. 443:93–100
    [Google Scholar]
24. 24.

    El-Baba TJ, Fuller DR, Woodall DW, Raab SA, Conant CR et al. 2018. Melting proteins confined in nanodroplets with 10.6 μm light provides clues about early steps of denaturation. Chem. Commun. 54:3270–73
    [Google Scholar]
25. 25.

    El-Baba TJ, Kim D, Rogers DB, Khan FA, Hales DA et al. 2016. Long-lived intermediates in a cooperative two-state folding transition. J. Phys. Chem. B 120:12040–46
    [Google Scholar]
26. 26.

    El-Baba TJ, Raab SA, Buckley RP, Brown CJ, Lutomski CA et al. 2021. Thermal analysis of a mixture of ribosomal proteins by vT-ESI-MS: toward a parallel approach for characterizing the stabilitome. Anal. Chem. 93:8484–92
    [Google Scholar]
27. 27.

    El-Baba TJ, Woodall DW, Raab SA, Fuller DR, Laganowsky A et al. 2017. Melting proteins: evidence for multiple stable structures upon thermal denaturation of native ubiquitin from ion mobility spectrometry-mass spectrometry measurements. J. Am. Chem. Soc. 139:6306–9
    [Google Scholar]
28. 28.

    Englander SW, Mayne L, Kan Z-Y, Hu W. 2016. Protein folding—how and why: by hydrogen exchange, fragment separation, and mass spectrometry. Annu. Rev. Biophys. 45:135–52
    [Google Scholar]
29. 29.

    Epstein CJ, Goldberger RF, Anfinsen CB. 1963. The genetic control of tertiary protein structure: studies with model systems. Cold Spring Harb. Symp. Quant. Biol. 28:439–49
    [Google Scholar]
30. 30.

    Eyring H. 1935. The activated complex in chemical reactions. J. Chem. Phys. 3:107–15
    [Google Scholar]
31. 31.

    Frederick KK, Marlow MS, Valentine KG, Wand AJ. 2007. Conformational entropy in molecular recognition by proteins. Nature 448:325–29
    [Google Scholar]
32. 32.

    Freire E. 2006. Overcoming HIV-1 resistance to protease inhibitors. Drug Discov. Today Dis. Mech. 3:281–86
    [Google Scholar]
33. 33.

    Fuller DR, Conant CR, El-Baba TJ, Brown CJ, Woodall DW et al. 2018. Conformationally regulated peptide bond cleavage in bradykinin. J. Am. Chem. Soc. 140:9357–60
    [Google Scholar]
34. 34.

    Gault J, Donlan JA, Liko I, Hopper JT, Gupta K et al. 2016. High-resolution mass spectrometry of small molecules bound to membrane proteins. Nat. Methods 13:333–36
    [Google Scholar]
35. 35.

    Goitre L, Trapani E, Trabalzini L, Retta SF 2014. The Ras superfamily of small GTPases: the unlocked secrets. Methods Mol. Biol. 1120:1–18
    [Google Scholar]
36. 36.

    Gruswitz F, O'Connell J 3rd, Stroud RM 2007. Inhibitory complex of the transmembrane ammonia channel, AmtB, and the cytosolic regulatory protein, GlnK. at 1.96 A. PNAS 104:42–47
    [Google Scholar]
37. 37.

    Houde D, Peng Y, Berkowitz SA, Engen JR. 2010. Post-translational modifications differentially affect IgG1 conformation and receptor binding. Mol. Cell. Proteom. 9:1716–28
    [Google Scholar]
38. 38.

    Jackson SE, Fersht AR 1991. Folding of chymotrypsin inhibitor 2. 1. Evidence for a two-state transition. Biochemistry 30:10428–35
    [Google Scholar]
39. 39.

    Karplus M, McCammon JA. 2002. Molecular dynamics simulations of biomolecules. Nat. Struct. Biol. 9:646–52
    [Google Scholar]
40. 40.

    Karplus M, Sali A. 1995. Theoretical studies of protein folding and unfolding. Curr. Opin. Struct. Biol. 5:58–73
    [Google Scholar]
41. 41.

    Kazmirski SL, Wong KB, Freund SM, Tan YJ, Fersht AR, Daggett V. 2001. Protein folding from a highly disordered denatured state: the folding pathway of chymotrypsin inhibitor 2 at atomic resolution. PNAS 98:4349–54
    [Google Scholar]
42. 42.

    Keserü G, Swinney DC, Mannhold R, Kubinyi H, Folkers G. 2015. Thermodynamics and Kinetics of Drug Binding Hoboken, NJ: Wiley
43. 43.

    Klebe G. 2015. Applying thermodynamic profiling in lead finding and optimization. Nat. Rev. Drug Discov. 14:95–110
    [Google Scholar]
44. 44.

    Kötting C, Gerwert K. 2004. Time-resolved FTIR studies provide activation free energy, activation enthalpy and activation entropy for GTPase reactions. Chem. Phys. 307:227–32
    [Google Scholar]
45. 45.

    Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–85
    [Google Scholar]
46. 46.

    Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT et al. 2014. Membrane proteins bind lipids selectively to modulate their structure and function. Nature 510:172–75
    [Google Scholar]
47. 47.

    Lazaridis T, Karplus M. 1997.. “ New view” of protein folding reconciled with the old through multiple unfolding simulations. Science 278:1928–31
    [Google Scholar]
48. 48.

    Lin CW, McCabe JW, Russell DH, Barondeau DP 2020. Molecular mechanism of ISC iron-sulfur cluster biogenesis revealed by high-resolution native mass spectrometry. J. Am. Chem. Soc. 142:6018–29
    [Google Scholar]
49. 49.

    Lumry R, Eyring H. 1954. Conformation changes of proteins. J. Phys. Chem. 58:110–20
    [Google Scholar]
50. 50.

    Makhatadze GI, Privalov PL. 1990. Heat capacity of proteins. I. Partial molar heat capacity of individual amino acid residues in aqueous solution: hydration effect. J. Mol. Biol. 213:375–84
    [Google Scholar]
51. 51.

    Maple HJ, Scheibner O, Baumert M, Allen M, Taylor RJ et al. 2014. Application of the Exactive Plus EMR for automated protein-ligand screening by non-covalent mass spectrometry. Rapid Commun. Mass Spectrom. 28:1561–68
    [Google Scholar]
52. 52.

    Mirza UA, Cohen SL, Chait BT. 1993. Heat-induced conformational changes in proteins studied by electrospray ionization mass spectrometry. Anal. Chem. 65:1–6
    [Google Scholar]
53. 53.

    Moghadamchargari Z, Huddleston J, Shirzadeh M, Zheng X, Clemmer DE et al. 2019. Intrinsic GTPase activity of K-RAS monitored by native mass spectrometry. Biochemistry 58:3396–405
    [Google Scholar]
54. 54.

    Naghibi H, Tamura A, Sturtevant JM. 1995. Significant discrepancies between van't Hoff and calorimetric enthalpies. PNAS 92:5597–99
    [Google Scholar]
55. 55.

    Pierson NA, Clemmer DE. 2015. An IMS–IMS threshold method for semi-quantitative determination of activation barriers: interconversion of proline cis↔trans forms in triply protonated bradykinin. Int. J. Mass Spectrom. 377:646–54
    [Google Scholar]
56. 56.

    Poltash ML, McCabe JW, Shirzadeh M, Laganowsky A, Russell DH. 2020. Native IM-Orbitrap MS: resolving what was hidden. Trends Anal. Chem. 124:115533
    [Google Scholar]
57. 57.

    Poltash ML, Shirzadeh M, McCabe JW, Moghadamchargari Z, Laganowsky A, Russell DH 2019. New insights into the metal-induced oxidative degradation pathways of transthyretin. Chem. Commun. 55:4091–94
    [Google Scholar]
58. 58.

    Prabhu NV, Sharp KA. 2005. Heat capacity in proteins. Annu. Rev. Phys. Chem. 56:521–48
    [Google Scholar]
59. 59.

    Raab SA, El-Baba TJ, Laganowsky A, Russell DH, Valentine SJ, Clemmer DE. 2021. Protons are fast and smart; proteins are slow and dumb: on the relationship of electrospray ionization charge states and conformations. J. Am. Soc. Mass Spectrom. 32:1553–61
    [Google Scholar]
60. 60.

    Raab SA, El-Baba TJ, Woodall DW, Liu W, Liu Y et al. 2020. Evidence for many unique solution structures for chymotrypsin inhibitor 2: a thermodynamic perspective derived from vT-ESI-IMS-MS measurements. J. Am. Chem. Soc. 142:17372–83
    [Google Scholar]
61. 61.

    Raffa RB. 2001. Drug-Receptor Thermodynamics: Introduction and Applications Hoboken, NJ: Wiley
62. 62.

    Rose RJ, Damoc E, Denisov E, Makarov A, Heck AJR 2012. High-sensitivity Orbitrap mass analysis of intact macromolecular assemblies. Nat. Methods 9:1084
    [Google Scholar]
63. 63.

    Shi H, Clemmer DE. 2014. Evidence for two new solution states of ubiquitin by IMS-MS analysis. J. Phys. Chem. B 118:3498–506
    [Google Scholar]
64. 64.

    Shi L, Holliday AE, Glover MS, Ewing MA, Russell DH, Clemmer DE 2016. Ion mobility-mass spectrometry reveals the energetics of intermediates that guide polyproline folding. J. Am. Soc. Mass Spectrom. 27:22–30
    [Google Scholar]
65. 65.

    Shi L, Holliday AE, Khanal N, Russell DH, Clemmer DE 2015. Configurationally-coupled protonation of polyproline-7. J. Am. Chem. Soc. 137:8680–83
    [Google Scholar]
66. 66.

    Shirzadeh M, Boone CD, Laganowsky A, Russell DH 2019. Topological analysis of transthyretin disassembly mechanism: Surface-induced dissociation reveals hidden reaction pathways. Anal. Chem. 91:2345–51
    [Google Scholar]
67. 67.

    Telmer PG, Shilton BH. 2003. Insights into the conformational equilibria of maltose-binding protein by analysis of high affinity mutants. J. Biol. Chem. 278:34555–67
    [Google Scholar]
68. 68.

    Tzeng S-R, Kalodimos CG. 2009. Dynamic activation of an allosteric regulatory protein. Nature 462:368–72
    [Google Scholar]
69. 69.

    Tzeng S-R, Kalodimos CG. 2012. Protein activity regulation by conformational entropy. Nature 488:236–40
    [Google Scholar]
70. 70.

    van't Hoff MJH. 1884. Etudes de dynamique chimique. Recl. Trav. Chim. Pays-Bas 3:333–36
    [Google Scholar]
71. 71.

    Velazquez-Campoy A, Freire E. 2006. Isothermal titration calorimetry to determine association constants for high-affinity ligands. Nat. Protoc. 1:186–91
    [Google Scholar]
72. 72.

    Villà J, Štrajbl M, Glennon TM, Sham YY, Chu ZT, Warshel A 2000. How important are entropic contributions to enzyme catalysis?. PNAS 97:11899–904
    [Google Scholar]
73. 73.

    Vouret-Craviari V, Grall D, Chambard J-C, Rasmussen UB, Pouysségur J, Van Obberghen-Schilling E. 1995. Post-translational and activation-dependent modifications of the G protein-coupled thrombin receptor. J. Biol. Chem. 270:8367–72
    [Google Scholar]
74. 74.

    Walsh G, Jefferis R 2006. Post-translational modifications in the context of therapeutic proteins. Nat. Biotechnol. 24:1241–52
    [Google Scholar]
75. 75.

    Warshel A. 1998. Electrostatic origin of the catalytic power of enzymes and the role of preorganized active sites. J. Biol. Chem. 273:27035–38
    [Google Scholar]
76. 76.

    Woodall DW, Brown CJ, Raab SA, El-Baba TJ, Laganowsky A et al. 2020. Melting of hemoglobin in native solutions as measured by IMS-MS. Anal. Chem. 92:3440–46
    [Google Scholar]
77. 77.

    Woodall DW, El-Baba TJ, Fuller DR, Liu W, Brown CJ et al. 2019. Variable-temperature ESI-IMS-MS analysis of myohemerythrin reveals ligand losses, unfolding, and a non-native disulfide bond. Anal. Chem. 91:6808–14
    [Google Scholar]
78. 78.

    Woodall DW, Henderson LW, Raab SA, Honma K, Clemmer DE. 2021. Understanding the thermal denaturation of myoglobin with IMS-MS: evidence for multiple stable structures and trapped pre-equilibrium states. J. Am. Soc. Mass Spectrom. 32:64–72
    [Google Scholar]
79. 79.

    Wyttenbach T, Bowers MT. 2011. Structural stability from solution to the gas phase: Native solution structure of ubiquitin survives analysis in a solvent-free ion mobility–mass spectrometry environment. J. Phys. Chem. B 115:12266–75
    [Google Scholar]
80. 80.

    Xie Y, Zhang J, Yin S, Loo JA. 2006. Top-down ESI-ECD-FT-ICR mass spectrometry localizes noncovalent protein-ligand binding sites. J. Am. Chem. Soc. 128:14432–33
    [Google Scholar]