Top-down Proteomics: Technology Advancements and Applications to Heart Diseases

Expert Review of Proteomics

Volumn 13, Issue 8, 2016, Pages 717-730

  Cai, Wenxuan ^a,b   Tucholski, Trisha M ^b   Gregorich, Zachery R ^a,b   Ge, Ying ^a,b  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

heart diseases; myofilaments; post translational modifications; quantitative analysis; Top down mass spectrometry

Indexed keywords

CONTRACTILE PROTEIN; ISOPROTEIN; BIOLOGICAL MARKER; PROTEOME;

AMINO ACID SEQUENCE; DATA ANALYSIS; HEART DISEASE; HUMAN; MASS SPECTROMETRY; MEDICAL TECHNOLOGY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEOMICS; REVIEW; GENETICS; PATHOLOGY; PROCEDURES;

BIOMARKERS; HEART DISEASES; HUMANS; MASS SPECTROMETRY; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS;

EID: 84980025306     PISSN: 14789450     EISSN: 17448387     Source Type: Journal    
DOI: 10.1080/14789450.2016.1209414     Document Type: Review

References (102)

1. D.Mozaffarian, E.J.Benjamin, A.S.Go, et al. Heart disease and stroke statistics–2015 update:a report from the American Heart Association. Circulation. 2015;131:e29–322.
2. A.L.Bui, T.B.Horwich, G.C.Fonarow Epidemiology and risk profile of heart failure. Nat Rev Cardiol. 2011;8:30–41.
3. J.J.McMurray, M.A.Pfeffer. Heart failure. Lancet. 2005;365:1877–1889.
4. J.O.Mudd, D.A.Kass. Tackling heart failure in the twenty-first century. Nature. 2008;451:919–928.
5. T.A.Drake, P.Ping. Thematic review series:systems biology approaches to metabolic and cardiovascular disorders. Proteomics approaches to the systems biology of cardiovascular diseases. J Lipid Res. 2007;48:1–8.
6. E.Sabidó, N.Selevsek, R.Aebersold. Mass spectrometry-based proteomics for systems biology. Curr Opin Biotechnol. 2012;23:591–597.
7. A.Pandey, M.Mann. Proteomics to study genes and genomes. Nature. 2000;405:837–846.
8. L.M.Smith, N.L.Kelleher, Proteomics CfTD. Proteoform:a single term describing protein complexity. Nat Methods. 2013;10:186–187.
9. Z.R.Gregorich, Y.Ge. Top-down proteomics in health and disease:challenges and opportunities. Proteomics. 2014;14:1195–1210.
10. M.Mann, O.N.Jensen. Proteomic analysis of post-translational modifications. Nat Biotechnol. 2003;21:255–261.
11. T.M.Karve, A.K.Cheema. Small changes huge impact:the role of protein posttranslational modifications in cellular homeostasis and disease. J Amino Acids. 2011;2011:207691.
12. P.Geraldes, G.L.King. Activation of protein kinase C isoforms and its impact on diabetic complications. Circ Res. 2010;106:1319–1331.
13. S.B.Marston, C.S.Redwood. Modulation of thin filament activation by breakdown or isoform switching of thin filament proteins:physiological and pathological implications. Circ Res. 2003;93:1170–1178.
14. A.Risco, A.Cuenda. New insights into the p38γ and p38δ MAPK pathways. J Signal Transduct. 2012;2012:520289.
15. Z.R.Gregorich, Y.H.Chang, Y.Ge. Proteomics in heart failure:top-down or bottom-up? Pflugers Arch. 2014;466:1199–1209.
16. B.T.Chait. Chemistry. Mass spectrometry:bottom-up or top-down? Science. 2006;314:65–66.
17. H.Zhang, Y.Ge. Comprehensive analysis of protein modifications by top-down mass spectrometry. Circ Cardiovasc Genet. 2011;4:711.
18. X.Dong, C.A.Sumandea, Y.C.Chen, et al. Augmented phosphorylation of cardiac troponin I in hypertensive heart failure. J Biol Chem. 2012;287:848–857.
19. J.Zhang, M.J.Guy, H.S.Norman, et al. Top-down quantitative proteomics identified phosphorylation of cardiac troponin I as a candidate biomarker for chronic heart failure. J Proteome Res. 2011;10:4054–4065.
20. Y.Ge, I.N.Rybakova, Q.Xu, et al. Top-down high-resolution mass spectrometry of cardiac myosin binding protein C revealed that truncation alters protein phosphorylation state. Proc Natl Acad Sci U S A. 2009;106:12658–12663.• Demonstrated alteration of protein phosphorylation caused by truncation using top-down MS.
21. Y.Peng, S.Ayaz-Guner, D.Yu, et al. Top-down mass spectrometry of cardiac myofilament proteins in health and disease. Proteomics Clin Appl. 2014;8:554–568.
22. Z.R.Gregorich, Y.Peng, N.M.Lane, et al. Comprehensive assessment of chamber-specific and transmural heterogeneity in myofilament protein phosphorylation by top-down mass spectrometry. J Mol Cell Cardiol. 2015;87:102–112.• First comprehensive assessment of regional and transmural heterogeneity of contractile proteoforms using top-down proteomics.
23. J.Carroll, I.M.Fearnley, J.E.Walker. Definition of the mitochondrial proteome by measurement of molecular masses of membrane proteins. Proc Natl Acad Sci U S A. 2006;103:16170–16175.
24. A.D.Catherman, M.Li, J.C.Tran, et al. Top down proteomics of human membrane proteins from enriched mitochondrial fractions. Anal Chem. 2013;85:1880–1888.
25. Y.H.Chang, Z.R.Gregorich, A.J.Chen, et al. New mass-spectrometry-compatible degradable surfactant for tissue proteomics. J Proteome Res. 2015;14:1587–1599.
26. S.Ayaz-Guner, J.Zhang, L.Li, et al. In vivo phosphorylation site mapping in mouse cardiac troponin I by high resolution top-down electron capture dissociation mass spectrometry:Ser22/23 are the only sites basally phosphorylated. Biochemistry. 2009;48:8161–8170.
27. H.J.Sterling, J.D.Batchelor, D.E.Wemmer, et al. Effects of buffer loading for electrospray ionization mass spectrometry of a noncovalent protein complex that requires high concentrations of essential salts. J Am Soc Mass Spectrom. 2010;21:1045–1049.
28. A.Laganowsky, E.Reading, J.T.S.Hopper, et al. Mass spectrometry of intact membrane protein complexes. Nat Protoc. 2013;8:639–651.• Seminal work identified MS-compatible surfactants for the analysis of intact membrane proteins and protein complexes.
29. L.Xiu, S.G.Valeja, A.J.Alpert, et al. Effective protein separation by coupling hydrophobic interaction and reverse phase chromatography for top-down proteomics. Anal Chem. 2014;86:7899–7906.
30. J.C.Tran, A.A.Doucette. Gel-eluted liquid fraction entrapment electrophoresis:an electrophoretic method for broad molecular weight range proteome separation. Anal Chem. 2008;80:1568–1573.• Development of high-resolution gel-based separation and fractionation of proteins.
31. S.Mehmood, T.M.Allison, C.V.Robinson. Mass spectrometry of protein complexes:from origins to applications. Annu Rev Phys Chem. 2015;66:453–474.
32. J.T.S.Hopper, Y.T.Yu, D.Li, et al. Detergent-free mass spectrometry of membrane protein complexes. Nat Methods. 2013;10:1206–1208.• Development of detergent-free systems for the analysis of intact membrane proteins and protein complexes.
33. J.P.Whitelegge. HPLC and mass spectrometry of intrinsic membrane proteins. Methods Mol Biol. 2004;251:323–340.
34. J.Whitelegge. Intact protein mass spectrometry and top-down proteomics. Expert Rev Proteomics. 2013;10:127–129.
35. P.Souda, C.M.Ryan, W.A.Cramer, et al. Profiling of integral membrane proteins and their post translational modifications using high-resolution mass spectrometry. Methods. 2011;55:330–336.
36. A.A.Doucette, J.C.Tran, M.J.Wall, et al. Intact proteome fractionation strategies compatible with mass spectrometry. Expert Rev Proteomics. 2011;8:787–800.
37. J.Zhang, X.Dong, T.A.Hacker, et al. Deciphering modifications in swine cardiac troponin I by top-down high-resolution tandem mass spectrometry. J Am Soc Mass Spectrom. 2010;21:940–948.
38. Y.Wang, J.R.Pinto, R.S.Solis, et al. Generation and functional characterization of knock-in mice harboring the cardiac troponin I-R21C mutation associated with hypertrophic cardiomyopathy. J Biol Chem. 2012;287:2156–2167.
39. R.Sancho Solis, Y.Ge, J.W.Walker. Single amino acid sequence polymorphisms in rat cardiac troponin revealed by top-down tandem mass spectrometry. J Muscle Res Cell Motil. 2008;29:203–212.
40. J.C.Tran, A.A.Doucette. Multiplexed size separation of intact proteins in solution phase for mass spectrometry. Anal Chem. 2009;81:6201–6209.• Novel gel-based, multiplexed separation method for application in top-down proteomics.
41. J.C.Tran, L.Zamdborg, D.R.Ahlf, et al. Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature. 2011;480:254–258.• First study utilizing multidimensional separation coupling GELFrEE, isoelectric focusing and RPC to top-down MS, and allows for identification of over 3000 proteoforms.
42. A.D.Catherman, K.R.Durbin, D.R.Ahlf, et al. Large-scale top-down proteomics of the human proteome:membrane proteins, mitochondria, and senescence. Mol Cell Proteomics. 2013;12:3465–3473.
43. I.Neverova, J.E.Van Eyk. Role of chromatographic techniques in proteomic analysis. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;815:51–63.
44. C.Ansong, S.Wu, D.Meng, et al. Top-down proteomics reveals a unique protein S-thiolation switch in Salmonella Typhimurium in response to infection-like conditions. Proc Natl Acad Sci U S A. 2013;110:10153–10158.
45. B.Chen, Y.Peng, S.G.Valeja, et al. Online hydrophobic interaction chromatography-mass spectrometry for top-down proteomics. Anal Chem. 2016;88:1885–1891.• Development of novel column materials for HIC that allows for direct coupling to top-down MS.
46. S.G.Valeja, L.Xiu, Z.R.Gregorich, et al. Three dimensional liquid chromatography coupling ion exchange chromatography/hydrophobic interaction chromatography/reverse phase chromatography for effective protein separation in top-down proteomics. Anal Chem. 2015;87:5363–5371.• Demonstrated unprecendented separation power of multidimensional liquid chromatography platform for the analysis of intact proteins by top-down MS.
47. K.Muneeruddin, M.Nazzaro, I.A.Kaltashov. Characterization of intact protein conjugates and biopharmaceuticals using ion-exchange chromatography with online detection by native electrospray ionization mass spectrometry and top-down tandem mass spectrometry. Anal Chem. 2015;87:10138–10145.
48. P.D.Compton, L.Zamdborg, P.M.Thomas, et al. On the scalability and requirements of whole protein mass spectrometry. Anal Chem. 2011;83:6868–6874.
49. A.J.Alpert. Size exclusion high-performance liquid chromatography of small solutes. In:Chi-san Wu, editor. Column handbook for size exclusion chromatography. San Diego (CA):Academic Press; 1999. p. 49–66.
50. X.Chen, Y.Ge. Ultrahigh pressure fast size exclusion chromatography for top-down proteomics. Proteomics. 2013;13:2563–2566.
51. S.Sharma, D.C.Simpson, N.Tolić, et al. Proteomic profiling of intact proteins using WAX-RPLC 2-D separations and FTICR mass spectrometry. J Proteome Res. 2007;6:602–610.
52. M.Karas, R.Krüger. Ion formation in MALDI:the cluster ionization mechanism. Chem Rev. 2003;103:427–440.
53. J.B.Fenn, M.Mann, C.K.Meng, et al. Electrospray ionization for mass spectrometry of large biomolecules. Science. 1989;246:64–71.
54. G.Scherperel, G.E.Reid. Emerging methods in proteomics:top-down protein characterization by multistage tandem mass spectrometry. Analyst. 2007;132:500–506.
55. M.Mann, N.L.Kelleher. Precision proteomics:the case for high resolution and high mass accuracy. Proc Natl Acad Sci U S A. 2008;105:18132–18138.
56. N.L.Kelleher, M.W.Senko, M.M.Siegel, et al. Unit resolution mass spectra of 112 kDa molecules with 3 Da accuracy. J Am Soc Mass Spectrom. 1997;8:380–383.
57. Y.Ge, B.G.Lawhorn, M.ElNaggar, et al. Top down characterization of larger proteins (45 kDa) by electron capture dissociation mass spectrometry. J Am Chem Soc. 2002;124:672–678.
58. X.Han, M.Jin, K.Breuker, et al. Extending top-down mass spectrometry to proteins with masses greater than 200 kilodaltons. Science. 2006;314:109–112.• Novel pre- and post-skimmer dissociation, and capillary additives for the characterization of proteins up to 200 kDa.
59. X.Chen, M.S.Westphall, L.M.Smith. Mass spectrometric analysis of DNA mixtures:instrumental effects responsible for decreased sensitivity with increasing mass. Anal Chem. 2003;75:5944–5952.
60. J.Park, H.Qin, M.Scalf, et al. A mechanical nanomembrane detector for time-of-flight mass spectrometry. Nano Lett. 2011;11:3681–3684.
61. S.Beck, A.Michalski, O.Raether, et al. The impact II, a very high-resolution quadrupole time-of-flight instrument (QTOF) for deep shotgun proteomics. Mol Cell Proteomics. 2015;14:2014–2029.
62. A.Makarov. Electrostatic axially harmonic orbital trapping:a high-performance technique of mass analysis. Anal Chem. 2000;72:1156–1162.
63. R.H.Perry, R.G.Cooks, R.J.Noll. Orbitrap mass spectrometry:instrumentation, ion motion and applications. Mass Spectrom Rev. 2008;27:661–699.
64. K.R.Durbin, L.Fornelli, R.T.Fellers, et al. Quantitation and identification of thousands of human proteoforms below 30 kDa. J Proteome Res. 2016;15:976–982.• Large-scale quantification of protein expression level using label-free top-down MS.
65. S.G.Valeja, N.K.Kaiser, F.Xian, et al. Unit mass baseline resolution for an intact 148 kDa therapeutic monoclonal antibody by Fourier transform ion cyclotron resonance mass spectrometry. Anal Chem. 2011;83:8391–8395.
66. Y.I.Kostyukevich, G.N.Vladimirov, E.N.Nikolaev. Dynamically harmonized FT-ICR cell with specially shaped electrodes for compensation of inhomogeneity of the magnetic field. Computer simulations of the electric field and ion motion dynamics. J Am Soc Mass Spectrom. 2012;23:2198–2207.
67. F.W.McLafferty, K.Breuker, M.Jin, et al. Top-down MS, a powerful complement to the high capabilities of proteolysis proteomics. FEBS J. 2007;274:6256–6268.
68. N.Siuti, N.L.Kelleher. Decoding protein modifications using top-down mass spectrometry. Nat Methods. 2007;4:817–821.
69. R.A.Zubarev, D.M.Horn, E.K.Fridriksson, et al. Electron capture dissociation for structural characterization of multiply charged protein cations. Anal Chem. 2000;72:563–573.
70. J.E.P.Syka, J.J.Coon, M.J.Schroeder, et al. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc Natl Acad Sci U S A. 2004;101:9528–9533.
71. S.M.Miladinović, L.Fornelli, Y.Lu, et al. In-spray supercharging of peptides and proteins in electrospray ionization mass spectrometry. Anal Chem. 2012;84:4647–4651.
72. S.A.McLuckey, G.E.Reid, J.M.Wells. Ion parking during ion/ion reactions in electrodynamic ion traps. Anal Chem. 2002;74:336–346.
73. T.Y.Huang, S.A.McLuckey. Top-down protein characterization facilitated by ion/ion reactions on a quadrupole/time of flight platform. Proteomics. 2010;10:3577–3588.
74. J.B.Shaw, W.Li, D.D.Holden, et al. Complete protein characterization using top-down mass spectrometry and ultraviolet photodissociation. J Am Chem Soc. 2013;135:12646–12651.• Demonstrated extensive fragmentation of UVPD for intact protein characterization.
75. J.J.Pesavento, C.A.Mizzen, N.L.Kelleher. Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry:human histone H4. Anal Chem. 2006;78:4271–4280.
76. Y.Peng, Z.R.Gregorich, S.G.Valeja, et al. Top-down proteomics reveals concerted reductions in myofilament and Z-disc protein phosphorylation after acute myocardial infarction. Mol Cell Proteomics. 2014;13:2752–2764.• Demonstrated concerted reduction of phosphorylation in myofilament and Z-disk proteins in a novel swine model of AMI.
77. J.Chamot-Rooke, G.Mikaty, C.Malosse, et al. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science. 2011;331:778–782.
78. Y.Du, B.A.Parks, S.Sohn, et al. Top-down approaches for measuring expression ratios of intact yeast proteins using Fourier transform mass spectrometry. Anal Chem. 2006;78:686–694.
79. L.F.Waanders, S.Hanke, M.Mann. Top-down quantitation and characterization of SILAC-labeled proteins. J Am Soc Mass Spectrom. 2007;18:2058–2064.
80. U.Bergmann, R.Ahrends, B.Neumann, et al. Application of metal-coded affinity tags (MeCAT):absolute protein quantification with top-down and bottom-up workflows by metal-coded tagging. Anal Chem. 2012;84:5268–5275.
81. M.T.Mazur, H.L.Cardasis, D.S.Spellman, et al. Quantitative analysis of intact apolipoproteins in human HDL by top-down differential mass spectrometry. Proc Natl Acad Sci U S A. 2010;107:7728–7733.
82. D.M.Horn, R.A.Zubarev, F.W.McLafferty. Automated reduction and interpretation of high resolution electrospray mass spectra of large molecules. J Am Soc Mass Spectrom. 2000;11:320–332.
83. M.W.Senko, S.C.Beu, F.W.McLafferty. Determination of monoisotopic masses and ion populations for large biomolecules from resolved isotopic distributions. J Am Soc Mass Spectrom. 1995;6:229–233.
84. X.Liu, Y.Inbar, P.C.Dorrestein, et al. Deconvolution and database search of complex tandem mass spectra of intact proteins:a combinatorial approach. Mol Cell Proteomics. 2010;9:2772–2782.
85. M.T.Marty, A.J.Baldwin, E.G.Marklund, et al. Bayesian deconvolution of mass and ion mobility spectra:from binary interactions to polydisperse ensembles. Anal Chem. 2015;87:4370–4376.
86. N.Jaitly, A.Mayampurath, K.Littlefield, et al. Decon2LS:an open-source software package for automated processing and visualization of high resolution mass spectrometry data. BMC Bioinformatics. 2009;10:87.
87. L.Zamdborg, R.D.LeDuc, K.J.Glowacz, et al. ProSight PTM 2.0:improved protein identification and characterization for top down mass spectrometry. Nucleic Acids Res. 2007;35:W701–W706.
88. N.M.Karabacak, L.Li, A.Tiwari, et al. Sensitive and specific identification of wild type and variant proteins from 8 to 669 kDa using top-down mass spectrometry. Mol Cell Proteomics. 2009;8:846–856.
89. A.M.Frank, J.J.Pesavento, C.A.Mizzen, et al. Interpreting top-down mass spectra using spectral alignment. Anal Chem. 2008;80:2499–2505.
90. X.Liu, Y.Sirotkin, Y.Shen, et al. Protein identification using top-down spectra. Mol Cell Proteomics. 2012;11:M111.008524.
91. W.Cai, H.Guner, Z.R.Gregorich, et al. MASH suite pro:a comprehensive software tool for top-down proteomics. Mol Cell Proteomics. 2016;15:703–714.• First software interface integrating spectral deconvolution, protein identification, quantification, and characterization in a suite with visual components for data validation.
92. P.P.de Tombe, R.J.Solaro. Integration of cardiac myofilament activity and regulation with pathways signaling hypertrophy and failure. Ann Biomed Eng. 2000;28:991–1001.
93. Z.Yin, J.Ren, W.Guo. Sarcomeric protein isoform transitions in cardiac muscle:a journey to heart failure. Biochim Biophys Acta. 2015;1852:47–52.
94. Y.Peng, D.Yu, Z.Gregorich, et al. In-depth proteomic analysis of human tropomyosin by top-down mass spectrometry. J Muscle Res Cell Motil. 2013;34:199–210.
95. Y.Peng, X.Chen, H.Zhang, et al. Top-down targeted proteomics for deep sequencing of tropomyosin isoforms. J Proteome Res. 2013;12:187–198.
96. O.Copeland, K.J.Nowak, N.G.Laing, et al. Investigation of changes in skeletal muscle alpha-actin expression in normal and pathological human and mouse hearts. J Muscle Res Cell Motil. 2010;31:207–214.
97. Y.C.Chen, S.Ayaz-Guner, Y.Peng, et al. Effective top-down LC/MS+ method for assessing actin isoforms as a potential cardiac disease marker. Anal Chem. 2015;87:8399–8406.
98. M.Gry, R.Rimini, S.Strömberg, et al. Correlations between RNA and protein expression profiles in 23 human cell lines. BMC Genomics. 2009;10:365.
99. R.J.Solaro, J.van der Velden. Why does troponin I have so many phosphorylation sites? Fact and fancy. J Mol Cell Cardiol. 2010;48:810–816.
100. T.Hunter. The age of crosstalk:phosphorylation, ubiquitination, and beyond. Mol Cell. 2007;28:730–738.
101. P.P.de Tombe. Myosin binding protein C in the heart. Circ Res. 2006;98:1234–1236.
102. E.Flashman, C.Redwood, J.Moolman-Smook, et al. Cardiac myosin binding protein C:its role in physiology and disease. Circ Res. 2004;94:1279–1289.