1932

Abstract

Hydroxyl radical footprinting (HRF) of proteins with mass spectrometry (MS) is a widespread approach for assessing protein structure. Hydroxyl radicals react with a wide variety of protein side chains, and the ease with which radicals can be generated (by radiolysis or photolysis) has made the approach popular with many laboratories. As some side chains are less reactive and thus cannot be probed, additional specific and nonspecific labeling reagents have been introduced to extend the approach. At the same time, advances in liquid chromatography and MS approaches permit an examination of the labeling of individual residues, transforming the approach to high resolution. Lastly, advances in understanding of the chemistry of the approach have led to the determination of absolute protein topologies from HRF data. Overall, the technology can provide precise and accurate measures of side-chain solvent accessibility in a wide range of interesting and useful contexts for the study of protein structure and dynamics in both academia and industry.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070317-033123
2018-05-20
2024-04-12
Loading full text...

Full text loading...

/deliver/fulltext/biophys/47/1/annurev-biophys-070317-033123.html?itemId=/content/journals/10.1146/annurev-biophys-070317-033123&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Angel TE, Chance MR, Palczewski K 2009. Conserved waters mediate structural and functional activation of family A (rhodopsin-like) G protein-coupled receptors. PNAS 106:8555–60First comprehensive footprinting of a membrane protein.
    [Google Scholar]
  2. 2.  Angel TE, Gupta S, Jastrzebska B, Palczewski K, Chance MR 2009. Structural waters define a functional channel mediating activation of the GPCR, rhodopsin. PNAS 106:14367–72First identification of dynamics of internal waters by radiolytic footprinting.
    [Google Scholar]
  3. 3.  Aye TT, Low TY, Sze SK 2005. Nanosecond laser-induced photochemical oxidation method for protein surface mapping with mass spectrometry. Anal. Chem. 77:5814–22Early paper on laser-induced hydroxyl radical footprinting of proteins.
    [Google Scholar]
  4. 4.  Bai Y, Milne JS, Mayne L, Englander SW 1993. Primary structure effects on peptide group hydrogen exchange. Proteins 17:75–86
    [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.  Bavro VN, Gupta S, Ralston C 2015. Oxidative footprinting in the study of structure and function of membrane proteins: current state and perspectives. Biochem. Soc. Trans. 43:983–94
    [Google Scholar]
  7. 7.  Borotto NB, Degraan-Weber N, Zhou Y, Vachet RW 2014. Label scrambling during CID of covalently labeled peptide ions. J. Am. Soc. Mass Spectrom. 25:1739–46
    [Google Scholar]
  8. 8.  Borotto NB, Zhou Y, Hollingsworth SR, Hale JE, Graban EM et al. 2015. Investigating therapeutic protein structure with diethylpyrocarbonate labeling and mass spectrometry. Anal. Chem. 87:10627–34
    [Google Scholar]
  9. 9.  Burley SK, Almo SC, Bonanno JB, Capel M, Chance MR et al. 1999. Structural genomics: beyond the human genome project. Nat. Genet. 23:151–57
    [Google Scholar]
  10. 10.  Calabrese AN, Ault JR, Radford SE, Ashcroft AE 2015. Using hydroxyl radical footprinting to explore the free energy landscape of protein folding. Methods 89:38–44
    [Google Scholar]
  11. 11.  Chance MR. 2001. Unfolding of apomyoglobin examined by synchrotron footprinting. Biochem. Biophys. Res. Commun. 287:614–21
    [Google Scholar]
  12. 12.  Chandonia JM, Brenner SE 2006. The impact of structural genomics: expectations and outcomes. Science 311:347–51
    [Google Scholar]
  13. 13.  Chen J, Rempel DL, Gau BC, Gross ML 2012. Fast photochemical oxidation of proteins and mass spectrometry follow submillisecond protein folding at the amino-acid level. J. Am. Chem. Soc. 134:18724–31
    [Google Scholar]
  14. 14.  Craig PO, Latzer J, Weinkam P, Hoffman RM, Ferreiro DU et al. 2011. Prediction of native-state hydrogen exchange from perfectly funneled energy landscapes. J. Am. Chem. Soc. 133:17463–72
    [Google Scholar]
  15. 15.  Deperalta G, Alvarez M, Bechtel C, Dong K, McDonald R, Ling V 2013. Structural analysis of a therapeutic monoclonal antibody dimer by hydroxyl radical footprinting. mAbs 5:86–101Comprehensive mapping of antibody structure and dimerization by HRF.
    [Google Scholar]
  16. 16.  Espino JA, Mali VS, Jones LM 2015. In cell footprinting coupled with mass spectrometry for the structural analysis of proteins in live cells. Anal. Chem. 87:7971–78
    [Google Scholar]
  17. 17.  Fenton HJH. 1894. LXXIII.—Oxidation of tartaric acid in presence of iron. J. Am. Chem. Soc. Trans. 65:899–910
    [Google Scholar]
  18. 18.  Fitzgerald MC, West GM 2009. Painting proteins with covalent labels: What's in the picture?. J. Am. Soc. Mass Spectrom. 20:1193–206
    [Google Scholar]
  19. 19.  Galas DJ, Schmitz A 1978. DNAse footprinting: a simple method for the detection of protein-DNA binding specificity. Nucleic Acids Res 5:3157–70
    [Google Scholar]
  20. 20.  Gau BC, Sharp JS, Rempel DL, Gross ML 2009. Fast photochemical oxidation of protein footprints faster than protein unfolding. Anal. Chem. 81:6563–71
    [Google Scholar]
  21. 21.  Goldsmith SC, Guan J-Q, Almo S, Chance M 2001. Synchrotron protein footprinting: a technique to investigate protein-protein interactions. J. Biomol. Struct. Dyn. 19:405–18
    [Google Scholar]
  22. 22.  Gomez GE, Cauerhff A, Craig PO, Goldbaum FA, Delfino JM 2006. Exploring protein interfaces with a general photochemical reagent. Protein Sci 15:744–52
    [Google Scholar]
  23. 23.  Guan J-Q, Almo SC, Chance MR 2004. Synchrotron radiolysis and mass spectrometry: a new approach to research on the actin cytoskeleton. Acc. Chem. Res. 37:221–29Highly cited HRF review article highlighting applications of HRF to metal ion binding and protein–protein interactions in the actin cytoskeleton.
    [Google Scholar]
  24. 24.  Guan J-Q, Almo SC, Reisler E, Chance MR 2003. Structural reorganization of proteins revealed by radiolysis and mass spectrometry: G-actin solution structure is divalent cation dependent. Biochemistry 42:11992–2000
    [Google Scholar]
  25. 25.  Guan J-Q, Chance MR 2005. Structural proteomics of macromolecular assemblies using oxidative footprinting and mass spectrometry. Trends Biochem. Sci. 30:583–92
    [Google Scholar]
  26. 26.  Guan J-Q, Takamoto K, Almo SC, Reisler E, Chance MR 2005. Structure and dynamics of the actin filament. Biochemistry 44:3166–75
    [Google Scholar]
  27. 27.  Guan J-Q, Vorobiev S, Almo SC, Chance MR 2002. Mapping the G-actin binding surface of cofilin using synchrotron protein footprinting. Biochemistry 41:5765–75
    [Google Scholar]
  28. 28.  Gupta S, Bavro VN, D'Mello R, Tucker SJ, Venien-Bryan C, Chance MR 2010. Conformational changes during the gating of a potassium channel revealed by structural mass spectrometry. Structure 18:839–46
    [Google Scholar]
  29. 29.  Gupta S, Celestre R, Petzold CJ, Chance MR, Ralston C 2014. Development of a microsecond X-ray protein footprinting facility at the Advanced Light Source. J. Synchrotron Radiat. 21:690–99Capabilities of radiolytic footprinting facilities at Berkeley laboratories.
    [Google Scholar]
  30. 30.  Gupta S, D'Mello R, Chance MR 2012. Structure and dynamics of protein waters revealed by radiolysis and mass spectrometry. PNAS 109:14882–87
    [Google Scholar]
  31. 31.  Gupta S, Feng J, Chance M, Ralston C 2016. Recent advances and applications in synchrotron X-ray protein footprinting for protein structure and dynamics elucidation. Protein Pept. Lett. 23:309–22
    [Google Scholar]
  32. 32.  Gupta S, Sullivan M, Toomey J, Kiselar J, Chance MR 2007. The Beamline X28C of the Center for Synchrotron Biosciences: a national resource for biomolecular structure and dynamics experiments using synchrotron footprinting. J. Synchrotron Radiat. 14:233–43
    [Google Scholar]
  33. 33.  Gustavsson M, Wang L, van Gils N, Stephens BS, Zhang P et al. 2017. Structural basis of ligand interaction with atypical chemokine receptor 3. Nat. Commun. 8:14135
    [Google Scholar]
  34. 34.  Hambly DM, Gross ML 2005. Laser flash photolysis of hydrogen peroxide to oxidize protein solvent-accessible residues on the microsecond timescale. J. Am. Soc. Mass Spectrom. 16:2057–63Seminal and highly cited paper that introduced nanosecond laser photolysis of peroxide as protein footprinting reagent.
    [Google Scholar]
  35. 35.  Heinkel F, Gsponer J 2016. Determination of protein folding intermediate structures consistent with data from oxidative footprinting mass spectrometry. J. Mol. Biol. 428:365–71
    [Google Scholar]
  36. 36.  Huang W, Ravikumar KM, Chance MR, Yang S 2015. Quantitative mapping of protein structure by hydroxyl radical footprinting-mediated structural mass spectrometry: a protection factor analysis. Biophys. J. 108:107–15This paper introduced protection factor analysis to provide absolute structure measures from HRF data of proteins.
    [Google Scholar]
  37. 37.  Huang W, Ravikumar KM, Parisien M, Yang S 2016. Theoretical modeling of multiprotein complexes by iSPOT: integration of small-angle X-ray scattering, hydroxyl radical footprinting, and computational docking. J. Struct. Biol. 196:340–49A paper highlighting integration of local (footprinting) and global (small-angle X-ray scattering) data for structure analysis.
    [Google Scholar]
  38. 38.  Jones LM, Sperry JB, Carroll JA, Gross ML 2011. Fast photochemical oxidation of proteins for epitope mapping. Anal. Chem. 83:7657–61
    [Google Scholar]
  39. 39.  Jumper CC, Bomgarden R, Rogers J, Etienne C, Schriemer DC 2012. High-resolution mapping of carbene-based protein footprints. Anal. Chem. 84:4411–18
    [Google Scholar]
  40. 40.  Jumper CC, Schriemer DC 2011. Mass spectrometry of laser-initiated carbene reactions for protein topographic analysis. Anal. Chem. 83:2913–20Important paper highlighting carbene footprinting approaches.
    [Google Scholar]
  41. 41.  Kalkum M, Przybylski M, Glocker MO 1998. Structure characterization of functional histidine residues and carbethoxylated derivatives in peptides and proteins by mass spectrometry. Bioconjug. Chem. 9:226–35
    [Google Scholar]
  42. 42.  Kamal JK, Chance MR 2008. Modeling of protein binary complexes using structural mass spectrometry data. Protein Sci 17:79–94
    [Google Scholar]
  43. 43.  Kaur P, Kiselar J, Yang S, Chance MR 2015. Quantitative protein topography analysis and high-resolution structure prediction using hydroxyl radical labeling and tandem-ion mass spectrometry (MS). Mol. Cell. Proteom. 14:1159–68
    [Google Scholar]
  44. 44.  Kaur P, Kiselar JG, Shi W, Yang S, Chance MR 2015. Covalent labeling techniques for characterizing higher order of monoclonal antibodies. State-of-the-Art and Emerging Technologies for Therapeutic Monoclonal Antibody Characterization, Vol. 2: Biopharmaceutical Characterization: the NISTmAb Case Study JE Schiel, DL Davis, OV Borisov 45–73 Washington, DC: Am. Chem. Soc
    [Google Scholar]
  45. 45.  Kaur P, Tomechko SE, Kiselar J, Shi W, Deperalta G et al. 2015. Characterizing monoclonal antibody structure by carboxyl group footprinting. mAbs 7:540–52
    [Google Scholar]
  46. 46.  Kiselar JG, Chance MR 2010. Future directions of structural mass spectrometry using hydroxyl radical footprinting. J. Mass Spectrom. 45:1373–82
    [Google Scholar]
  47. 47.  Kiselar JG, Janmey PA, Almo SC, Chance MR 2003. Structural analysis of gelsolin using synchrotron protein footprinting. Mol. Cell. Proteom. 2:1120–32
    [Google Scholar]
  48. 48.  Kiselar JG, Janmey PA, Almo SC, Chance MR 2003. Visualizing the Ca2+-dependent activation of gelsolin by using synchrotron footprinting. PNAS 100:3942–47
    [Google Scholar]
  49. 49.  Kiselar JG, Mahaffy R, Pollard TD, Almo SC, Chance MR 2007. Visualizing Arp2/3 complex activation mediated by binding of ATP and WASp using structural mass spectrometry. PNAS 104:1552–57
    [Google Scholar]
  50. 50.  Kiselar JG, Maleknia SD, Sullivan M, Downard KM, Chance MR 2002. Hydroxyl radical probe of protein surfaces using synchrotron X-ray radiolysis and mass spectrometry. Int. J. Radiat. Biol. 78:101–14First HRF of a protein using mass spectrometry approaches.
    [Google Scholar]
  51. 51.  Klinger AL, Kiselar J, Ilchenko S, Komatsu H, Chance MR, Axelsen PH 2014. A synchrotron-based hydroxyl radical footprinting analysis of amyloid fibrils and prefibrillar intermediates with residue-specific resolution. Biochemistry 53:7724–34
    [Google Scholar]
  52. 52.  Konermann L, Tong X, Pan Y 2008. Protein structure and dynamics studied by mass spectrometry: H/D exchange, hydroxyl radical labeling, and related approaches. J. Mass Spectrom. 43:1021–36
    [Google Scholar]
  53. 53.  Li K, Chen G, Mo J, Huang RY, Deyanova EG, et al. 2017. Orthogonal mass spectrometry-based footprinting for epitope mapping and structural characterization: the IL-6 receptor upon binding of protein therapeutics. Anal. Chem. 89:7742–49
    [Google Scholar]
  54. 54.  Li X, Li Z, Xie B, Sharp JS 2013. Improved identification and relative quantification of sites of peptide and protein oxidation for hydroxyl radical footprinting. J. Am. Soc. Mass Spectrom. 24:1767–76
    [Google Scholar]
  55. 55.  Li Z, Moniz H, Wang S, Ramiah A, Zhang F et al. 2015. High structural resolution hydroxyl radical protein footprinting reveals an extended Robo1-heparin binding interface. J. Biol. Chem. 290:10729–40
    [Google Scholar]
  56. 56.  Liu R, Guan J-Q, Zak O, Aisen P, Chance MR 2003. Structural reorganization of the transferrin C-lobe and transferrin receptor upon complex formation: the C-lobe binds to the receptor helical domain. Biochemistry 42:12447–54
    [Google Scholar]
  57. 57.  Macgregor RB Jr 1992. Photogeneration of hydroxyl radicals for footprinting. Anal. Biochem. 204:324–27
    [Google Scholar]
  58. 58.  Maleknia SD, Brenowitz M, Chance MR 1999. Millisecond radiolytic modification of peptides by synchrotron X-rays identified by mass spectrometry. Anal. Chem. 71:3965–73
    [Google Scholar]
  59. 59.  Maleknia SD, Chance MR, Downard KM 1999. Electrospray-assisted modification of proteins: a radical probe of protein structure. Rapid Commun. Mass Spectrom 13:2352–58
    [Google Scholar]
  60. 60.  Manzi L, Barrow AS, Scott D, Layfield R, Wright TG et al. 2016. Carbene footprinting accurately maps binding sites in protein–ligand and protein–protein interactions. Nat. Commun. 7:13288
    [Google Scholar]
  61. 61.  Mendoza VL, Vachet RW 2008. Protein surface mapping using diethylpyrocarbonate with mass spectrometric detection. Anal. Chem. 80:2895–904Early paper highlighting protein surface mapping with diethyl-pyrocarbonate.
    [Google Scholar]
  62. 62.  Mendoza VL, Vachet RW 2009. Probing protein structure by amino acid-specific covalent labeling and mass spectrometry. Mass Spectrom. Rev. 28:785–815
    [Google Scholar]
  63. 63.  Niu B, Mackness BC, Rempel DL, Zhang H, Cui W et al. 2017. Incorporation of a reporter peptide in FPOP compensates for adventitious scavengers and permits time-dependent measurements. J. Am. Soc. Mass Spectrom. 28:389–92
    [Google Scholar]
  64. 64.  Oztug Durer ZA, Kamal JK, Benchaar S, Chance MR, Reisler E 2011. Myosin binding surface on actin probed by hydroxyl radical footprinting and site-directed labels. J. Mol. Biol. 414:204–16
    [Google Scholar]
  65. 65.  Pacholarz KJ, Garlish RA, Taylor RJ, Barran PE 2012. Mass spectrometry based tools to investigate protein–ligand interactions for drug discovery. Chem. Soc. Rev. 41:4335–55
    [Google Scholar]
  66. 66.  Padayatti PS, Wang L, Gupta S, Orban T, Sun W et al. 2013. A hybrid structural approach to analyze ligand binding by the serotonin type 4 receptor (5-HT4). Mol. Cell. Proteom. 12:1259–71
    [Google Scholar]
  67. 67.  Rashidzadeh H, Khrapunov S, Chance MR, Brenowitz M 2003. Solution structure and interdomain interactions of the Saccharomyces cerevisiae “TATA binding protein” (TBP) probed by radiolytic protein footprinting. Biochemistry 42:3655–65
    [Google Scholar]
  68. 68.  Richards FM, Lamed R, Wynn R, Patel D, Olack G 2000. Methylene as a possible universal footprinting reagent that will include hydrophobic surface areas: overview and feasibility: properties of diazirine as a precursor. Protein Sci 9:2506–17
    [Google Scholar]
  69. 69.  Sandercock CG, Storz U 2012. Antibody specification beyond the target: claiming a later-generation therapeutic antibody by its target epitope. Nat. Biotechnol. 30:615–18
    [Google Scholar]
  70. 70.  Sangodkar J, Perl A, Tohme R, Kiselar J, Kastrinsky DB et al. 2017. Activation of tumor suppressor protein PP2A inhibits KRAS-driven tumor growth. J. Clin. Invest. 127:2081–90
    [Google Scholar]
  71. 71.  Schmitz A, Galas DJ 1979. The interaction of RNA polymerase and lac repressor with the lac control region. Nucleic Acids Res 6:111–37
    [Google Scholar]
  72. 72.  Sharp JS, Becker JM, Hettich RL 2003. Protein surface mapping by chemical oxidation: structural analysis by mass spectrometry. Anal. Biochem. 313:216–25Early, highly cited paper laying out HRF of proteins using photolysis of peroxide.
    [Google Scholar]
  73. 73.  Sharp JS, Becker JM, Hettich RL 2004. Analysis of protein solvent accessible surfaces by photochemical oxidation and mass spectrometry. Anal. Chem. 76:672–83Early, highly cited paper laying out HRF of proteins using photolysis of peroxide.
    [Google Scholar]
  74. 74.  Sharp JS, Guo J-t, Uchiki T, Xu Y, Dealwis C, Hettich RL 2005. Photochemical surface mapping of C14S-Sml1p for constrained computational modeling of protein structure. Anal. Biochem. 340:201–12
    [Google Scholar]
  75. 75.  Stanford SM, Aleshin AE, Zhang V, Ardecky RJ, Hedrick MP et al. 2017. Diabetes reversal by inhibition of the low-molecular-weight tyrosine phosphatase. Nat. Chem. Biol. 13:624–32
    [Google Scholar]
  76. 76.  Stocks BB, Konermann L 2009. Structural characterization of short-lived protein unfolding intermediates by laser-induced oxidative labeling and mass spectrometry. Anal. Chem. 81:20–27
    [Google Scholar]
  77. 77.  Takamoto K, Chance MR 2006. Radiolytic protein footprinting with mass spectrometry to probe the structure of macromolecular complexes. Annu. Rev. Biophys. Biomol. Struct. 35:251–76Higly cited HRF review article outlining LC-MS methods and applications.
    [Google Scholar]
  78. 78.  Vahidi S, Konermann L 2016. Probing the time scale of FPOP (fast photochemical oxidation of proteins): Radical reactions extend over tens of milliseconds. J. Am. Soc. Mass Spectrom. 27:1156–64
    [Google Scholar]
  79. 79.  Vahidi S, Stocks BB, Liaghati-Mobarhan Y, Konermann L 2013. Submillisecond protein folding events monitored by rapid mixing and mass spectrometry-based oxidative labeling. Anal. Chem. 85:8618–25
    [Google Scholar]
  80. 80.  Volman DH, Chen JC 1959. The photochemical decomposition of hydrogen peroxide in aqueous solutions of allyl alcohol at 2537 Å. J. Am. Chem. Soc. 81:4141–44
    [Google Scholar]
  81. 81.  Wang L, Chance MR 2017. Protein footprinting comes of age: mass spectrometry for biophysical structure assessment. Mol. Cell. Proteom. 16:706–16
    [Google Scholar]
  82. 82.  Watson C, Sharp JS 2012. Conformational analysis of therapeutic proteins by hydroxyl radical protein footprinting. AAPS J 14:206–17
    [Google Scholar]
  83. 83.  Wecksler AT, Kalo MS, Deperalta G 2015. Mapping of Fab-1:VEGF interface using carboxyl group footprinting mass spectrometry. J. Am. Soc. Mass Spectrom 26:2077–80
    [Google Scholar]
  84. 84.  Wen J, Zhang H, Gross ML, Blankenship RE 2009. Membrane orientation of the FMO antenna protein from Chlorobaculum tepidum as determined by mass spectrometry-based footprinting. PNAS 106:6134–39
    [Google Scholar]
  85. 85.  Wong JWH, Maleknia SD, Downard KM 2005. Hydroxyl radical probe of the calmodulin-melittin complex interface by electrospray ionization mass spectrometry. J. Am. Soc. Mass Spectrom. 16:225–33
    [Google Scholar]
  86. 86.  Xie B, Sharp JS 2015. Hydroxyl radical dosimetry for high flux hydroxyl radical protein footprinting applications using a simple optical detection method. Anal. Chem. 87:10719–23
    [Google Scholar]
  87. 87.  Xie B, Sood A, Woods RJ, Sharp JS 2017. Quantitative protein topography measurements by high resolution hydroxyl radical protein footprinting enable accurate molecular model selection. Sci. Rep. 7:4552
    [Google Scholar]
  88. 88.  Xu G, Chance MR 2005. Radiolytic modification and reactivity of amino acid residues serving as structural probes for protein footprinting. Anal. Chem. 77:4549–55
    [Google Scholar]
  89. 89.  Xu G, Chance MR 2005. Radiolytic modification of sulfur-containing amino acid residues in model peptides: fundamental studies for protein footprinting. Anal. Chem. 77:2437–49
    [Google Scholar]
  90. 90.  Xu G, Chance MR 2007. Hydroxyl radical-mediated modification of proteins as probes for structural proteomics. Chem. Rev. 107:3514–43Most highly cited HRF of proteins article published to date; outlines overall chemistry and mass spectrometry detection of modified species.
    [Google Scholar]
  91. 91.  Xu G, Kiselar J, He Q, Chance MR 2005. Secondary reactions and strategies to improve quantitative protein footprinting. Anal. Chem. 77:3029–37
    [Google Scholar]
  92. 92.  Xu G, Liu R, Zak O, Aisen P, Chance MR 2005. Structural allostery and binding of the transferrin receptor complex. Mol. Cell. Proteom. 4:1959–67
    [Google Scholar]
  93. 93.  Xu G, Takamoto K, Chance MR 2003. Radiolytic modification of basic amino acid residues in peptides: probes for examining protein–protein interactions. Anal. Chem. 75:6995–7007
    [Google Scholar]
  94. 94.  Yan Y, Chen G, Wei H, Huang RY, Mo J et al. 2014. Fast photochemical oxidation of proteins (FPOP) maps the epitope of EGFR binding to adnectin. J. Am. Soc. Mass Spectrom. 25:2084–92
    [Google Scholar]
  95. 95.  Zhang B, Rempel DL, Gross ML 2016. Protein footprinting by carbenes on a fast photochemical oxidation of proteins (FPOP) platform. J. Am. Soc. Mass Spectrom. 27:552–55
    [Google Scholar]
  96. 96.  Zhang H, Shen W, Rempel D, Monsey J, Vidavsky I et al. 2011. Carboxyl-group footprinting maps the dimerization interface and phosphorylation-induced conformational changes of a membrane-associated tyrosine kinase. Mol. Cell. Proteom. 10:M110.005678
    [Google Scholar]
  97. 97.  Zhang H, Tang X, Munske GR, Tolic N, Anderson GA, Bruce JE 2009. Identification of protein-protein interactions and topologies in living cells with chemical cross-linking and mass spectrometry. Mol. Cell. Proteom. 8:409–20
    [Google Scholar]
  98. 98.  Zhang Y, Wecksler AT, Molina P, Deperalta G, Gross ML 2017. Mapping the binding interface of VEGF and a monoclonal antibody Fab-1 fragment with fast photochemical oxidation of proteins (FPOP) and mass spectrometry. J. Am. Soc. Mass Spectrom. 28:850–58
    [Google Scholar]
  99. 99.  Zheng C, Yang L, Hoopmann MR, Eng JK, Tang X et al. 2011. Cross-linking measurements of in vivo protein complex topologies. Mol. Cell. Proteom. 10:M110.006841
    [Google Scholar]
  100. 100.  Zhou Y, Vachet RW 2012. Increased protein structural resolution from diethylpyrocarbonate-based covalent labeling and mass spectrometric detection. J. Am. Soc. Mass Spectrom. 23:708–17
    [Google Scholar]
  101. 101.  Zhu Y, Serra A, Guo T, Park JE, Zhong Q, Sze SK 2017. Application of nanosecond laser photolysis protein footprinting to study EGFR activation by EGF in cells. J. Proteome Res. 16:2282–93
    [Google Scholar]
  102. 102.  Ziemianowicz DS, Bomgarden R, Etienne C, Schriemer DC 2017. Amino acid insertion frequencies arising from photoproducts generated using aliphatic diazirines. J. Am. Soc. Mass Spectrom. 28:2011–21
    [Google Scholar]
/content/journals/10.1146/annurev-biophys-070317-033123
Loading
/content/journals/10.1146/annurev-biophys-070317-033123
Loading

Data & Media loading...

Supplemental Material

Supplementary Data

  • 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