Electrospray ionization–mass spectrometry for the investigation of protein– nucleic acid interactions

Mass Spectrometry of Nucleosides and Nucleic Acids

Volumn , Issue , 2009, Pages 303-328

  Fabris, Daniele ^a   Turner, Kevin B ^a   Hagan, Nathan A ^a  

^a UNIVERSITY OF MARYLAND BALTIMORE COUNTY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOMOLECULES; MASS SPECTROMETRY; NUCLEIC ACIDS; PROTEINS;

ACCESSIBLE INFORMATION; BIOPHYSICAL TECHNIQUES; ELECTROSPRAY IONIZATION (ESI); INTRINSIC CHARACTERISTICS; MASS SPECTROMETRIC ANALYSIS; NON-COVALENT COMPLEXES; PERSONAL EXPERIENCE; SPECIFIC INTERACTION;

ELECTROSPRAY IONIZATION;

EID: 84904042560     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1201/9781420044034     Document Type: Chapter

References (111)

1. Yamashita, M. and Fenn, J.B., Electrospray ion source. Another variation on the free-jet theme, J. Phys. Chem. 88, 4671-4675, 1984.
2. Aleksandrov, M.L., Gall, L.N., Krasnov, V.N., Nikolaev, V.I., Pavlenko, V.A., and Shkurov, V.A., Extraction of ions from solutions under atmospheric pressure: A method of mass spectrometric analysis of bioorganic compounds, Doklady Akademii Nauk. 277, 379-383, 1984.
3. Ganem, B., Li, Y.T., and Henion, J.D., Detection of non-covalent receptor-ligand complexes by mass spectrometry, J. Am. Chem. Soc. 113, 6294-6296, 1991.
4. Ganem, B., Li, Y.T., and Henion, J.D., Observation of noncovalent enzyme-substrate and enzyme- product complexes by ion-spray mass spectrometry, J. Am. Chem. Soc. 113, 7818-7819, 1991.
5. Ganguly, A.K., Pramanik, B.N., Tsarbopoulos, A., Covey, T.R., Huang, E., and Fuhrman, S.A., Mass spectrometric detection of the noncovalent GDP-bound conformational state of the human H-ras protein, J. Am. Chem. Soc. 114, 6559-6560, 1992.
6. Loo, J.A., Studying noncovalent protein complexes by electrospray ionization mass spectrometry, Mass Spectrom. Rev. 16, 1-23, 1997.
7. Pramanik, B.N., Bartner, P.L., Mirza, U.A., Liu, Y.H., and Ganguly, A.K., Electrospray ionization mass spectrometry for the study of non-covalent complexes: An emerging technology, J. Mass Spectrom. 33, 911-920, 1998.
8. Beck, J.L., Colgrave, M.L., Ralph, S.F., and Sheil, M.M., Electrospray ionization mass spectrometry of oligonucleotide complexes with drugs, metals, and proteins, Mass Spectrom. Rev. 20, 61-87, 2001.
9. Hofstadler, S.A., and Griffey, R.H., Analysis of noncovalent complexes of DNA and RNA by mass spectrometry, Chem. Rev. 101, 377-390, 2001.
10. Comisarow, M.B., and Marshall, A.G., Fourier transform ion cyclotron resonance, Chem. Phys. Lett. 25, 282-283, 1974.
11. Hendrickson, C.L., Emmett, M.R., and Marshall, A.G., Electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry, Annu. Rev. Phys. Chem. 50, 517-536, 1999.
12. Chen, R., Cheng, X., Mitchell, D.W., Hofstadler, S.A., Wu, Q., Rockwood, A.L., Sherman, M.G., and Smith, R.D., Trapping, detection, and mass determination of coliphage T4 DNA ions of 108 Da by electrospray ionization Fourier transform ion cyclotron resonance mass spectrometry, Anal. Chem. 67, 1159-1168, 1995.
13. Cheng, X., Camp, D.G., 2nd, Wu, Q., Bakhtiar, R., Springer, D.L., Morris, B.J., Bruce, J.E., Anderson, G.A., Edmonds, C.G., and Smith, R.D., Molecular weight determination of plasmid DNA using electrospray ionization mass spectrometry, Nucleic Acids Res. 24, 2183-2189, 1996.
14. Cotter, R.J., Time-of-Flight Mass Spectrometry. Instrumentation and Applications in Biological Research, ACS Professional Reference Books, ACS, Washington, DC, 1997.
15. Rostom, A.A., Fucini, P., Benjamin, D.R., Juenemann, R., Nierhaus, K.H., Hartl, F.U., Dobson, C.M., and Robinson, C.V., Detection and selective dissociation of intact ribosomes in a mass spectrometer, Proc. Nat. Acad. Sci. USA 97, 5185-5190, 2000.
16. McKay, A.R., Ruotolo, B.T., Ilag, L.L., and Robinson, C.V., Mass measurements of increased accuracy resolve heterogeneous populations of intact ribosomes, J. Am. Chem. Soc. 128, 11433-11442, 2006.
17. Greig, M.J., Gaus, H.J., and Griffey, R.H., Negative ionization micro electrospray mass spectrometry of oligonucleotides and their complexes, Rapid Commun. Mass Spectrom. 10, 47-50, 1996.
18. Kapur, A., Beck, J.L., Brown, S.E., Dixon, N.E., and Sheil, M.M., Use of electrospray mass spectrometry to study the binding interactions between a replication terminator protein and DNA, Protein Sci. 11, 147-157, 2002.
19. Valaskovic, G.A., Kelleher, N.L., and McLafferty, F.W., Attomole protein characterization by capillary electrophoresis-mass spectrometry, Science 273, 1199-1202, 1996.
20. Martin, S.E., Shabanowitz, J., Hunt, D.F., and Marto, J.A., Subfemtomole MS and MS/MS peptide sequence analysis using nano-HPLC micro-ESI Fourier transform ion cyclotron resonance mass spectrometry, Anal. Chem. 72, 4266-4274, 2000.
21. Wilm, M., and Mann, M., Analytical properties of the nanoelectrospray ion source, Anal. Chem. 68, 1-8, 1996.
22. McLafferty, F.W., Tandem mass spectrometry, Science 214, 280-287, 1981.
23. Hunt, D.F., Shabanowitz, J., Yates, J.R. R., Zhu, N.Z., Russell, D.H., and Castro, M.E., Tandem quadrupole Fourier transform mass spectrometry of oligopeptides and small proteins, Proc. Natl. Acad. Sci. USA 84, 60-63, 1987.
24. Biemann, K., and Scoble, H., Characterization by tandem mass spectrometry of structural modifications in proteins, Science 237, 992-998.
25. Papayannopoulos, I.A., 1995, The interpretation of collision-induced dissociation tandem mass spectra of peptides, Mass Spectrom. Rev. 15, 49-73, 1987.
26. Cerny, R.L., Tomer, K.B., Gross, M.L., and Grotjahn, L., Fast atom bombardment combined with tandem mass spectrometry for determining structures of small oligonucleotides, Anal. Biochem. 165, 175-182, 1987.
27. McLuckey, S.A., and Habibi-Goudarzi, S., Decompositions of multiply charged oligonucleotide anions, J. Am. Chem. Soc. 115, 12085-12095, 1993.
28. Little, D.P., Chorush, R.A., Spier, J.P., Senko, M.W., Kelleher, N.L., and McLafferty, F.W., Rapid sequencing of oligonucleotides by high-resolution mass spectrometry, J. Am. Chem. Soc. 116, 4893-4897, 1994.
29. Limbach, P.A., Crain, P.F., and McCloskey, J.A., Characterization of oligonucleotides and nucleic acids by mass spectrometry, Curr. Opin. Biotechnol. 6, 96-102, 1995.
30. Nordhoff, E., Kirpekar, F., and Roepstorff, P., Mass spectrometry of nucleic acids, Mass Spectrom. Rev. 15, 67-138, 1996.
31. Kowalak, J.A., Pomerantz, S.C., Crain, P.F., and McCloskey, J.A., A novel method for the determination of post-transcriptional modification in RNA by mass spectrometry, Nucleic Acids Res. 21, 4577-4585, 1993.
32. Barry, J.P., Vouros, P., Van Schepdael, A., and Law, S.-J., Mass and sequence verification of modified oligonucleotides using electrospray tandem mass spectrometry, J. Mass Spectrom. 30, 993-1006, 1995.
33. Iannitti, P., Sheil, M.M., and Wickham, G., High sensitivity and fragmentation specificity in the analysis of drug-DNA adducts by electrospray tandem mass spectrometry, J. Am. Chem. Soc. 119, 1490-1491, 1997.
34. McCloskey, J.A., Graham, D.E., Zhou, S., Crain, P.F., Ibba, M., Konisky, J., Soll, D., and Olsen, G.J., Post-transcriptional modification in archaeal tRNAs: Identities and phylogenetic relations of nucleotides from mesophilic and hyperthermophilic Methanococcales, Nucleic Acids Res. 29, 4699-4706, 2001.
35. Kellersberger, K.A., Yu, E., Kruppa, G.H., Young, M.M., and Fabris, D., Top-down characterization of nucleic acids modified by structural probes using high-resolution tandem mass spectrometry and automated data interpretation, Anal. Chem. 76, 2438-2445, 2004.
36. Gale, D.C. and Smith, R.D., Characterization of noncovalent complexes formed between minor groove binding molecules and duplex DNA by electrospray ionization-mass spectrometry, J. Am. Soc. Mass Spectrom. 6, 1154-1164, 1995.
37. Gabelica, V., Rosu, F., Houssier, C., and De Pauw, E., Gas phase thermal denaturation of an oligonucleotide duplex and its complexes with minor groove binders, Rapid Commun. Mass Spectrom. 14, 464-467, 2000.
38. Wan, K.X., Gross, M.L., and Shibue, T., Gas-phase stability of double-stranded oligodeoxynucleotides and their noncovalent complexes with DNA-binding drugs as revealed by collisional activation in an ion trap, J. Am. Soc. Mass Spectrom. 11, 450-457, 2000.
39. David, W.M., Brodbelt, J.S., Kerwin, S.M., and Thomas, P.W., Investigation of quadruplex oligonucleotide- drug interaction by electrospray ionization mass spectrometry, Anal. Chem. 74, 2029-2033, 2002.
40. Fenn, J.B., Mann, M., Meng, C.K., Wong, S.F., and Whitehouse, C.M., Electrospray ionization for mass spectrometry of large biomolecules, Science 246, 64-71, 1989.
41. Cech, N.B. and Enke, C.G., Practical implications of some recent studies in electrospray ionization fundamentals, Mass Spectrom. Rev. 20, 362-387, 2001.
42. Amad, M.H., Cech, N.B., Jackson, G.S., and Enke, C.G., Importance of gas-phase proton affinities in determining the electrospray ionization response for analytes and solvents, J. Mass Spectrom. 35, 784-789, 2000.
43. Stults, J.T. and Marsters, J.C., Improved electrospray ionization of synthetic oligodeoxynucleotides, Rapid Commun. Mass Spectrom. 5, 359, 1991.
44. Pieles, U., Zurcher, W., Schar, M., and Moser, H.E., Matrix-assisted laser desorption ionization time-offlight mass spectrometry: A powerful tool for the mass and sequence analysis of natural and modified oligonucleotides, Nucleic Acids Res. 21, 3191-3196, 1993.
45. Nordhoff, E., Ingendoh, A., Cramer, R., Overberg, A., Stahl, B., Karas, M., Hillenkamp, F., and Crain, P.F., Matrix-assisted laser desorption/ionization mass spectrometry of nucleic acids with wavelengths in the ultraviolet and infrared, Rapid Commun. Mass Spectrom. 6, 771-776, 1992.
46. Little, D.P., Thannhauser, T.W., and McLafferty, F.W., Verification of 50- to 100-mer DNA and RNA sequences with high-resolution mass spectrometry, Proc. Natl. Acad. Sci. USA 92, 2318-2322, 1995.
47. Limbach, P.A., Crain, P.F., and McCloskey, J.A., Molecular mass measurement of intact ribonucleic acids via electrospray ionization quadrupole mass spectrometry, J. Am. Soc. Mass Spectrom. 6, 27-39, 1995.
48. Muddiman, D.C., Cheng, X., Udseth, H.R., and Smith, R.D., Charge-state reduction with improved signal intensity of oligonucleotides in electrospray ionization mass spectrometry, J. Am. Soc. Mass Spectrom. 7, 697-706, 1996.
49. Liu, C., Wu, Q., Harms, A.C., and Smith, R.D., On-line microdialysis sample cleanup for electrospray ionization mass spectrometry of nucleic acid samples, Anal. Chem. 68, 3295-3299, 1996.
50. Xu, N., Lin, Y., Hofstadler, S.A., Matson, D., Call, C.J., and Smith, R.D., A microfabricated dialysis device for sample cleanup in electrospray ionization mass spectrometry, Anal. Chem. 70, 3553-3536, 1998.
51. Hannis, J.C. and Muddiman, D.C., Characterization of a microdialysis approach to prepare polymerase chain reaction products for electrospray ionization mass spectrometry using on-line ultraviolet absorbance measurements and inductively coupled plasma atomic emission spectroscopy, Rapid Commun. Mass Spectrom. 13, 323-330, 1999.
52. McLuckey, S.A. and Stephenson, J.L., Jr., Ion/ion chemistry of high-mass multiply charged ions, Mass Spectrom. Rev. 17, 369-407, 1998.
53. Newton, K.A., He, M., Amunugama, R., and McLuckey, S.A., Selective cation removal from gaseous polypeptide ions: Proton vs. sodium ion abstraction via ion/ion reaction, Phys. Chem. Chem. Phys. 6, 2710-2717, 2004.
54. Turner, K. B., Monti, S. and Fabris, D., Like polarity ion/ion reactions enable the investigation of specific metal interactions in nucleic acids and their non-covalent assemblies, J. Am. Chem. Soc. 30, 13353-13363, 2008.
55. McGhee, J.D. and von Hippel, P.H., Theoretical aspects of DNA-protein interactions: Co-operative and non-co-operative binding of large ligands to a one-dimensional homogeneous lattice, J. Mol. Biol. 86, 469-489, 1974.
56. Hagan, N. and Fabris, D., Direct mass spectrometric determination of the stoichiometry and binding affinity of the complexes between HIV-1 nucleocapsid protein and RNA stem-loops hairpins of the HIV-1 Y-recognition element, Biochemistry 42, 10736-10745, 2003.
57. Bruins, A.P., Covey, T.R., and Henion, J.D., Ion spray interface for combined liquid chromatographyatmospheric pressure ionization mass spectrometry, Anal. Chem. 59, 2642-2646, 1987.
58. Dole, M., Mack, L.L., Hines, R.C., Mobley, R.L., Ferguson, L.D., and Alice, M.B., Molecular Beams of Macroions, J. Chem. Phys. 49, 2240-2249, 1968.
59. Kebarle, P., A brief overview of the present status of the mechanisms involved in electrospray mass spectrometry, J. Mass Spectrom. 35, 804-817, 2000.
60. Iribarne, J.V. and Thomson, B.A., On the evaporation of small ions from charged droplets, J. Chem. Phys. 64, 2287-2294, 1976.
61. Mora, J.F., Van Berkel, G.J., Enke, C.G., Cole, R.B., Martinez-Sanchez, M., and Fenn, J.B., Electrochemical processes in electrospray ionization mass spectrometry, J. Mass Spectrom. 35, 939-952, 2000.
62. Verkerk, U.H., Peschke, M., and Kebarle, P., Effect of buffer cations and of H3O+ on the charge states of native proteins. Significance to determinations of stability constants of protein complexes, J. Mass Spectrom. 38, 618-631, 2003.
63. Peschke, M., Verkerk, U.H., and Kebarle, P., Features of the ESI mechanism that affect the observation of multiply charged noncovalent protein complexes and the determination of the association constants by the titration method, J. Am. Soc. Mass Spectrom. 15, 1424-1434, 2004.
64. Ding, J. and Anderegg, R.J., Specific and nonspecific dimer formation in the electrospray ionization mass spectrometry of oligonucleotides, J. Am. Soc. Mass Spectrom. 6, 159-164, 1994.
65. De Guzman, R.N., Wu, Z.R., Stalling, C.C., Pappalardo, L., Borer, P.N., and Summers, M.F., Structure of the HIV-1 nucleocapsid protein bound to the SL-3 Y-RNA recognition element, Science 279, 384-388, 1998.
66. Robinson, C.V., Chung, E.W., Kragelund, B.B., Knudsen, J., Aplin, R.T., Poulsen, F.M., and Dobson, C.M., Probing the nature of noncovalent interactions by mass spectrometry. A study of protein-CoA ligand binding and assembly, J. Am. Chem. Soc. 118, 8646-8653, 1996.
67. Gabelica, V. and De Pauw, E., Comparison between solution-phase stability and gas-phase kinetic stability of oligodeoxynucleotide duplexes, J. Mass Spectrom. 36, 397-402, 2001.
68. Schwartz, B.L., Bruce, J.F., Anderson, G.A., Hofstadler, S.A., Rockwood, A.L., Smith, R.D., Chilkoti, A., and Stayton, P.S., Dissociation of tetrameric ions of non-covalent streptavidin complexes by electrospray ionization, J. Am. Soc. Mass Spectrom. 6, 459-465, 1995.
69. Potier, N., Donald, L.J., Chernushevich, I., Ayed, A., Ens, W., Arrowsmith, C.H., Standing, K., and Duckworth, H.W., Study of a noncovalent trp repressor: DNA operator complex by electrospray ionization time-of-flight mass spectrometry, Protein Sci. 7, 1388-1395, 1998.
70. Benjamin, D.R., Robinson, C.V., Hendrick, J.P., Hartl, F.U., and Dobson, C.M., Mass spectrometry of ribosomes and ribosomal subunits, Proc. Natl. Acad. Sci. USA 95, 7391-7395, 1998.
71. Cheng, X., Harms, A.C., Goudreau, P.N., Terwilliger, T.C., and Smith, R.D., Direct measurement of oligonucleotide binding stoichiometry of gene V protein by mass spectrometry, Proc. Natl. Acad. Sci. USA 93, 7022-7027, 1996.
72. Griffey, R.H., Sannes-Lowery, K.A., Drader, J.J., Mohan, V., Swayze, E.E., and Hofstadler, S.A., Characterization of low-affinity complexes between RNA and small molecules using electrospray ionization mass spectrometry, J. Am. Chem. Soc. 122, 9933-9938, 2000.
73. Turner, K.B., Hagan, N.A., and Fabris, D., Inhibitory effects of archetypical nucleic acid ligands on the interactions of HIV-1 nucleocapsid protein with elements of Y-RNA, Nucleic Acids Res. 34, 1305-1316, 2006.
74. Cheng, X., Morin, P.E., Harms, A.C., Bruce, J.E., Ben-David, Y., and Smith, R.D., Mass spectrometric characterization of sequence-specific complexes of DNA and transcription factor PU.1 DNA binding domain, Anal. Biochem. 239, 35-40, 1996.
75. Veenstra, T.D., Johnson, K.L., Tomlinson, A.J., Craig, T.A., Kumar, R., and Naylor, S., Zinc-induced conformational changes in the DNA-binding domain of the vitamin D receptor determined by electrospray ionization mass spectrometry, J. Am. Soc. Mass Spectrom. 9, 8-14, 1998.
76. Craig, T.A., Benson, L.M., Tomlinson, A.J., Veenstra, T.D., Naylor, S., and Kumar, R., Analysis of transcription complexes and effects of ligands by microspray ionization mass spectrometry, Nat. Biotechnol. 17, 1214-1218, 1999.
77. Deterding, L.J., Kast, J., Przybylski, M., and Tomer, K.B., Molecular characterization of a tetramolecular complex between dsDNA and a DNA-binding leucine zipper peptide dimer by mass spectrometry, Bioconj. Chem. 11, 335-344, 2000.
78. Sannes-Lowery, K.A., Hu, P., Mack, D.P., Mei, H.Y., and Loo, J.A., HIV-1 Tat peptide binding to TAR RNA by electrospray ionization mass spectrometry, Anal. Chem. 69, 5130-5135, 1997.
79. Mei, H.Y., Mack, D., Galan, A.A., Halim, N.S., Heldsinger, A., Loo, J.A., Moreland, D.W., Sannes- Lowery, K.A., Sharmeen, L., Truong, H.N., and Czarnik, A.W., Discovery of selective, small-molecule inhibitors of RNA complexes-I. The Tat protein/TAR RNA complexes required for HIV-1 transcription, Bioorg. Med. Chem. 5, 1173-1184, 1997.
80. Loo, J.A., Holler, T.P., Foltin, S.K., McConnell, P., Banotal, C.A., Horne, N.M., Mueller, W.T., Stevenson, T.I., and Mack, D.P., Application of electrospray ionization mass spectrometry for studying human immunodeficiency virus protein complexes, Proteins 2(Suppl.), 28-37, 1998.
81. Fisher, R.J., Fivash, M.J., Stephen, A.G., Hagan, N.A., Shenoy, S.R., Medaglia, M.V., Smith, L.R., Worthy, K.M., Simpson, J.T., Shoemaker, R., McNitt, K.L., Johnson, D.J., Hixson, C.V., Gorelick, R.J., Fabris, D., Henderson, L.E., and Rein, A., Complex interactions of HIV-1 nucleocapsid protein with oligonucleotides, Nucleic Acids Res. 34, 472-484, 2006.
82. Stephen, A.G., Datta, S.A. K., Worthy, K.M., Bindu, L., Fivash, M.J., Turner, K.B., Fabris, D., Rein, A., and Fisher, R.J., Measuring the binding stoichiometry of HIV1 Gag to very low density oligonucleotide surfaces using surface plasmon resonance spectroscopy, J. Biomol. Technol. 18, 259-266, 2007.
83. Fabris, D., Chaudhari, P., Hagan, N.A., and Turner, K.B., Functional investigations of retroviral proteinribonucleic acid complexes by nanospray Fourier transform ion cyclotron resonance mass spectrometry, Eur. J. Mass Spectrom. 13, 29-33, 2007.
84. Yuan, Y., Kerwood, D.J., Paoletti, A.C., Shubsda, M.F., and Borer, P.N., Stem of SL1 RNA in HIV-1: Structure and nucleocapsid protein binding for a 1 × 3 internal loop, Biochemistry 42, 5259-5269, 2003.
85. Shubsda, M.F., Paoletti, A.C., Hudson, B.S., and Borer, P.N., Affinities of packaging domain loops in HIV-1 RNA for the nucleocapsid protein, Biochemistry 41, 5276-5282, 2002.
86. Lawrence, D.C., Stover, C.C., Noznitsky, J., Wu, Z., and Summers, M.F., Structure of the intact stem and bulge of HIV-1 Psi-RNA stem-loop SL1, J. Mol. Biol. 326, 529-542, 2003.
87. Hagan, N.A. and Fabris, D., Dissecting the protein-RNA and RNA-RNA interactions in the nucleocapsidmediated dimerization and isomerization of HIV-1 stemloop 1, J. Mol. Biol. 365, 396-410, 2007.
88. Turner, K.B., Hagan, N.A., Kohlway, A., and Fabris, D., Mapping noncovalent ligand binding to stemloop domains of the HIV-1 packaging signal by tandem mass spectrometry, J. Am. Soc. Mass Spectrom. 17, 1401-1411, 2006.
89. Daniel, J.M., Friess, S.D., Rajagopalan, S., Wendt, S., and Zenobi, R., Quantitative determination of noncovalent binding interactions using soft ionization mass spectrometry, Int. J. Mass Spectrom. Ion Processes 216, 1-27, 2002.
90. Millard, B.J., Quantitative Mass Spectrometry, Heyden & Son Ltd., London, 1978.
91. Goodner, K.L., Milgram, K.E., Williams, K.R., Watson, C.H., and Eyler, J.R., Quantitation of ion abundances in Fourier-transform ion cyclotron resonance mass spectrometry, J. Am. Soc. Mass Spectrom. 9, 1204-1212, 1998.
92. Amarasinghe, G.K., De Guzman, R.N., Turner, R.B., Chancellor, K.J., Wu, Z.R., and Summers, M.F., NMR structure of the HIV-1 nucleocapsid protein bound to stem-loop SL2 of the Y-RNA packaging signal. Implications for genome recognition, J. Mol. Biol. 301, 491-511, 2000.
93. Liu, C., Pasa-Tolic, L., Hofstadler, S.A., Harms, A.C., Smith, R.D., Kang, C., and Sinha, N., Probing RegA/RNA interactions using electrospray ionization-Fourier transform ion cyclotron resonance-mass spectrometry, Anal. Biochem. 262, 67-76, 1998.
94. Gabelica, V. and De Pauw, E., Comparison of the collision-induced dissociation of duplex DNA at different collision regimes: Evidence for a multistep dissociation mechanism, J. Am. Soc. Mass Spectrom. 13, 91-98, 2002.
95. Heck, A.J. R. and van den Heuvel, R.H. H., Investigation of intact protein complexes by mass spectrometry, Mass Spectrom. Rev. 23, 368-389, 2004.
96. Schnier, P.D., Klassen, J.S., Strittmatter, E.F., and Williams, E.R., Activation energies for dissociation of double strand oligonucleotide anions: Evidence for Watson-Crick base pairing in vacuo, J. Am. Chem. Soc. 120, 9605-9613, 1998.
97. Turner, K.B., Hagan, N.A., and Fabris, D., Understanding the isomerization of the HIV-1 dimerization initiation domain by the nucleocapsid protein, J. Mol. Biol. 369, 812-828, 2007.
98. Gauthier, J.W., Trautman, T.R., and Jacobson, D.B., Sustained off-resonance irradiation for collisionactivated dissociation involving Fourier transform mass spectrometry. Collision-activated dissociation technique that emulates infrared multiphoton dissociation, Anal. Chim. Acta 246, 211-225, 1991.
99. de Koning, L.J., Nibbering, N.M.M., van Orden, S.L., and Laukien, F.H., Mass selection of ions in a Fourier transform ion cyclotron resonance trap using correlated harmonic excitation fields (CHEF), Int. J. Mass Spectrom. Ion Processes 165/166, 209-219, 1997.
100. Takáts, Z., Wiseman, J.M., and Cooks, R.G., Ambient mass spectrometry using desorption electrospray ionization (DESI): Instrumentation, mechanisms and applications in forensics, chemistry, and biology, J. Mass Spectrom. 40, 1261-1275, 2005.
101. Shiea, J., Huang, M.-Z., Hsu, H.-J., Lee, C.-Y., Yuan, C.-H., Beech, I., and Sunner, J., Electrosprayassisted laser desorption/ionization mass spectrometry for direct ambient analysis of solids, Rapid Commun. Mass Spectrom. 19, 3701-3704, 2005.
102. Sampson, J.S., Hawkridge, A.M., and Muddiman, D.C., Generation and detection of multiply-charged peptides and proteins by matrix-assisted laser desorption electrospray ionization (MALDESI) Fourier transform ion cyclotron resonance mass spectrometry, J. Am. Soc. Mass Spectrom. 17, 1712-1716, 2006.
103. Stoeckli, M., Chaurand, P., Hallahan, D.E., and Caprioli, R.M., Imaging mass spectrometry: A new technology for the analysis of protein expression in mammalian tissues, Nat. Med. 7, 493-496, 2001.
104. McDonnell, L.A., and Heeren, R.M.A., Imaging mass spectrometry, Mass Spectrom. Rev. 26, 606-643, 2007.
105. Woodin, R.L., Bomse, D.S., and Beauchamp, J.L., Multiphoton dissociation of molecules with low power continuous wave infrared laser radiation, J. Am. Chem. Soc. 100, 3248-3250, 1978.
106. Little, D.P., Speir, J.P., Senko, M.W., O’Connor, P.B., and McLafferty, F.W., Infrared multiphoton dissociation of large multiply charged ions for biomolecule sequencing, Anal. Chem. 66, 2809-2815, 1994.
107. Zubarev, R.A., Kelleher, N.L., and McLafferty, F.W., Electron capture dissociation of multiply charged protein cations: A nonergodic process, J. Am. Chem. Soc. 120, 3265-3266, 1998.
108. Zubarev, R.A., Horn, D.M., Fridriksson, E.K., Kelleher, N.L., Kruger, N.A., Lewis, M.A., Carpenter, B.K., and McLafferty, F.W., Electron capture dissociation for structural characterization of multiply charged protein cations, Anal. Chem. 72, 563-573, 2000.
109. Syka, J.E. P., Coon, J.J., Schroeder, M.J., Shabanowitz, J., and Hunt, D.F., Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry, Proc. Natl. Acad. Sci. USA 101, 9528-9533, 2000.
110. Kaneko, Y., Megill, L.R., and Hasted, J.B., Study of inelastic collisions by drifting ions, J. Chem. Phys. 45, 3741, 1966.
111. Clemmer, D.E. and Jarrold, M.F., Ion mobility measurements and their applications to cluster biomolecules, J. Mass Spectrom. 32, 577-592, 1967.