668
Views
80
CrossRef citations to date
0
Altmetric
Review

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

, , &
Pages 717-730 | Received 25 Apr 2016, Accepted 01 Jul 2016, Published online: 26 Jul 2016

References

  • Mozaffarian D, Benjamin EJ, Go AS, et al. Heart disease and stroke statistics–2015 update: a report from the American Heart Association. Circulation. 2015;131:e29–322.
  • Bui AL, Horwich TB, Fonarow GC. Epidemiology and risk profile of heart failure. Nat Rev Cardiol. 2011;8:30–41.
  • McMurray JJ, Pfeffer MA. Heart failure. Lancet. 2005;365:1877–1889.
  • Mudd JO, Kass DA. Tackling heart failure in the twenty-first century. Nature. 2008;451:919–928.
  • Drake TA, Ping P. 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.
  • Sabidó E, Selevsek N, Aebersold R. Mass spectrometry-based proteomics for systems biology. Curr Opin Biotechnol. 2012;23:591–597.
  • Pandey A, Mann M. Proteomics to study genes and genomes. Nature. 2000;405:837–846.
  • Smith LM, Kelleher NL, Proteomics CfTD. Proteoform: a single term describing protein complexity. Nat Methods. 2013;10:186–187.
  • Gregorich ZR, Ge Y. Top-down proteomics in health and disease: challenges and opportunities. Proteomics. 2014;14:1195–1210.
  • Mann M, Jensen ON. Proteomic analysis of post-translational modifications. Nat Biotechnol. 2003;21:255–261.
  • Karve TM, Cheema AK. Small changes huge impact: the role of protein posttranslational modifications in cellular homeostasis and disease. J Amino Acids. 2011;2011:207691.
  • Geraldes P, King GL. Activation of protein kinase C isoforms and its impact on diabetic complications. Circ Res. 2010;106:1319–1331.
  • Marston SB, Redwood CS. Modulation of thin filament activation by breakdown or isoform switching of thin filament proteins: physiological and pathological implications. Circ Res. 2003;93:1170–1178.
  • Risco A, Cuenda A. New insights into the p38γ and p38δ MAPK pathways. J Signal Transduct. 2012;2012:520289.
  • Gregorich ZR, Chang YH, Ge Y. Proteomics in heart failure: top-down or bottom-up? Pflugers Arch. 2014;466:1199–1209.
  • Chait BT. Chemistry. Mass spectrometry: bottom-up or top-down? Science. 2006;314:65–66.
  • Zhang H, Ge Y. Comprehensive analysis of protein modifications by top-down mass spectrometry. Circ Cardiovasc Genet. 2011;4:711.
  • Dong X, Sumandea CA, Chen YC, et al. Augmented phosphorylation of cardiac troponin I in hypertensive heart failure. J Biol Chem. 2012;287:848–857.
  • Zhang J, Guy MJ, Norman HS, 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.
  • Ge Y, Rybakova IN, Xu Q, 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.
  • Peng Y, Ayaz-Guner S, Yu D, et al. Top-down mass spectrometry of cardiac myofilament proteins in health and disease. Proteomics Clin Appl. 2014;8:554–568.
  • Gregorich ZR, Peng Y, Lane NM, 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.
  • Carroll J, Fearnley IM, Walker JE. Definition of the mitochondrial proteome by measurement of molecular masses of membrane proteins. Proc Natl Acad Sci U S A. 2006;103:16170–16175.
  • Catherman AD, Li M, Tran JC, et al. Top down proteomics of human membrane proteins from enriched mitochondrial fractions. Anal Chem. 2013;85:1880–1888.
  • Chang YH, Gregorich ZR, Chen AJ, et al. New mass-spectrometry-compatible degradable surfactant for tissue proteomics. J Proteome Res. 2015;14:1587–1599.
  • Ayaz-Guner S, Zhang J, Li L, 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.
  • Sterling HJ, Batchelor JD, Wemmer DE, 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.
  • Laganowsky A, Reading E, Hopper JTS, et al. Mass spectrometry of intact membrane protein complexes. Nat Protoc. 2013;8:639–651.
  • Xiu L, Valeja SG, Alpert AJ, et al. Effective protein separation by coupling hydrophobic interaction and reverse phase chromatography for top-down proteomics. Anal Chem. 2014;86:7899–7906.
  • Tran JC, Doucette AA. Gel-eluted liquid fraction entrapment electrophoresis: an electrophoretic method for broad molecular weight range proteome separation. Anal Chem. 2008;80:1568–1573.
  • Mehmood S, Allison TM, Robinson CV. Mass spectrometry of protein complexes: from origins to applications. Annu Rev Phys Chem. 2015;66:453–474.
  • Hopper JTS, Yu YT, Li D, et al. Detergent-free mass spectrometry of membrane protein complexes. Nat Methods. 2013;10:1206–1208.
  • Whitelegge JP. HPLC and mass spectrometry of intrinsic membrane proteins. Methods Mol Biol. 2004;251:323–340.
  • Whitelegge J. Intact protein mass spectrometry and top-down proteomics. Expert Rev Proteomics. 2013;10:127–129.
  • Souda P, Ryan CM, Cramer WA, et al. Profiling of integral membrane proteins and their post translational modifications using high-resolution mass spectrometry. Methods. 2011;55:330–336.
  • Doucette AA, Tran JC, Wall MJ, et al. Intact proteome fractionation strategies compatible with mass spectrometry. Expert Rev Proteomics. 2011;8:787–800.
  • Zhang J, Dong X, Hacker TA, 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.
  • Wang Y, Pinto JR, Solis RS, 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.
  • Sancho Solis R, Ge Y, Walker JW. 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.
  • Tran JC, Doucette AA. Multiplexed size separation of intact proteins in solution phase for mass spectrometry. Anal Chem. 2009;81:6201–6209.
  • Tran JC, Zamdborg L, Ahlf DR, et al. Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature. 2011;480:254–258.
  • Catherman AD, Durbin KR, Ahlf DR, et al. Large-scale top-down proteomics of the human proteome: membrane proteins, mitochondria, and senescence. Mol Cell Proteomics. 2013;12:3465–3473.
  • Neverova I, Van Eyk JE. Role of chromatographic techniques in proteomic analysis. J Chromatogr B Analyt Technol Biomed Life Sci. 2005;815:51–63.
  • Ansong C, Wu S, Meng D, 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.
  • Chen B, Peng Y, Valeja SG, et al. Online hydrophobic interaction chromatography-mass spectrometry for top-down proteomics. Anal Chem. 2016;88:1885–1891.
  • Valeja SG, Xiu L, Gregorich ZR, 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.
  • Muneeruddin K, Nazzaro M, Kaltashov IA. 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.
  • Compton PD, Zamdborg L, Thomas PM, et al. On the scalability and requirements of whole protein mass spectrometry. Anal Chem. 2011;83:6868–6874.
  • Alpert AJ. 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.
  • Chen X, Ge Y. Ultrahigh pressure fast size exclusion chromatography for top-down proteomics. Proteomics. 2013;13:2563–2566.
  • Sharma S, Simpson DC, Tolić N, et al. Proteomic profiling of intact proteins using WAX-RPLC 2-D separations and FTICR mass spectrometry. J Proteome Res. 2007;6:602–610.
  • Karas M, Krüger R. Ion formation in MALDI: the cluster ionization mechanism. Chem Rev. 2003;103:427–440.
  • Fenn JB, Mann M, Meng CK, et al. Electrospray ionization for mass spectrometry of large biomolecules. Science. 1989;246:64–71.
  • Scherperel G, Reid GE. Emerging methods in proteomics: top-down protein characterization by multistage tandem mass spectrometry. Analyst. 2007;132:500–506.
  • Mann M, Kelleher NL. Precision proteomics: the case for high resolution and high mass accuracy. Proc Natl Acad Sci U S A. 2008;105:18132–18138.
  • Kelleher NL, Senko MW, Siegel MM, et al. Unit resolution mass spectra of 112 kDa molecules with 3 Da accuracy. J Am Soc Mass Spectrom. 1997;8:380–383.
  • Ge Y, Lawhorn BG, ElNaggar M, et al. Top down characterization of larger proteins (45 kDa) by electron capture dissociation mass spectrometry. J Am Chem Soc. 2002;124:672–678.
  • Han X, Jin M, Breuker K, et al. Extending top-down mass spectrometry to proteins with masses greater than 200 kilodaltons. Science. 2006;314:109–112.
  • Chen X, Westphall MS, Smith LM. Mass spectrometric analysis of DNA mixtures: instrumental effects responsible for decreased sensitivity with increasing mass. Anal Chem. 2003;75:5944–5952.
  • Park J, Qin H, Scalf M, et al. A mechanical nanomembrane detector for time-of-flight mass spectrometry. Nano Lett. 2011;11:3681–3684.
  • Beck S, Michalski A, Raether O, 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.
  • Makarov A. Electrostatic axially harmonic orbital trapping: a high-performance technique of mass analysis. Anal Chem. 2000;72:1156–1162.
  • Perry RH, Cooks RG, Noll RJ. Orbitrap mass spectrometry: instrumentation, ion motion and applications. Mass Spectrom Rev. 2008;27:661–699.
  • Durbin KR, Fornelli L, Fellers RT, et al. Quantitation and identification of thousands of human proteoforms below 30 kDa. J Proteome Res. 2016;15:976–982.
  • Valeja SG, Kaiser NK, Xian F, 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.
  • Kostyukevich YI, Vladimirov GN, Nikolaev EN. 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.
  • McLafferty FW, Breuker K, Jin M, et al. Top-down MS, a powerful complement to the high capabilities of proteolysis proteomics. FEBS J. 2007;274:6256–6268.
  • Siuti N, Kelleher NL. Decoding protein modifications using top-down mass spectrometry. Nat Methods. 2007;4:817–821.
  • Zubarev RA, Horn DM, Fridriksson EK, et al. Electron capture dissociation for structural characterization of multiply charged protein cations. Anal Chem. 2000;72:563–573.
  • Syka JEP, Coon JJ, Schroeder MJ, et al. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc Natl Acad Sci U S A. 2004;101:9528–9533.
  • Miladinović SM, Fornelli L, Lu Y, et al. In-spray supercharging of peptides and proteins in electrospray ionization mass spectrometry. Anal Chem. 2012;84:4647–4651.
  • McLuckey SA, Reid GE, Wells JM. Ion parking during ion/ion reactions in electrodynamic ion traps. Anal Chem. 2002;74:336–346.
  • Huang TY, McLuckey SA. Top-down protein characterization facilitated by ion/ion reactions on a quadrupole/time of flight platform. Proteomics. 2010;10:3577–3588.
  • Shaw JB, Li W, Holden DD, et al. Complete protein characterization using top-down mass spectrometry and ultraviolet photodissociation. J Am Chem Soc. 2013;135:12646–12651.
  • Pesavento JJ, Mizzen CA, Kelleher NL. Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: human histone H4. Anal Chem. 2006;78:4271–4280.
  • Peng Y, Gregorich ZR, Valeja SG, 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.
  • Chamot-Rooke J, Mikaty G, Malosse C, et al. Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science. 2011;331:778–782.
  • Du Y, Parks BA, Sohn S, et al. Top-down approaches for measuring expression ratios of intact yeast proteins using Fourier transform mass spectrometry. Anal Chem. 2006;78:686–694.
  • Waanders LF, Hanke S, Mann M. Top-down quantitation and characterization of SILAC-labeled proteins. J Am Soc Mass Spectrom. 2007;18:2058–2064.
  • Bergmann U, Ahrends R, Neumann B, 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.
  • Mazur MT, Cardasis HL, Spellman DS, 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.
  • Horn DM, Zubarev RA, McLafferty FW. Automated reduction and interpretation of high resolution electrospray mass spectra of large molecules. J Am Soc Mass Spectrom. 2000;11:320–332.
  • Senko MW, Beu SC, McLafferty FW. Determination of monoisotopic masses and ion populations for large biomolecules from resolved isotopic distributions. J Am Soc Mass Spectrom. 1995;6:229–233.
  • Liu X, Inbar Y, Dorrestein PC, et al. Deconvolution and database search of complex tandem mass spectra of intact proteins: a combinatorial approach. Mol Cell Proteomics. 2010;9:2772–2782.
  • Marty MT, Baldwin AJ, Marklund EG, et al. Bayesian deconvolution of mass and ion mobility spectra: from binary interactions to polydisperse ensembles. Anal Chem. 2015;87:4370–4376.
  • Jaitly N, Mayampurath A, Littlefield K, et al. Decon2LS: an open-source software package for automated processing and visualization of high resolution mass spectrometry data. BMC Bioinformatics. 2009;10:87.
  • Zamdborg L, LeDuc RD, Glowacz KJ, et al. ProSight PTM 2.0: improved protein identification and characterization for top down mass spectrometry. Nucleic Acids Res. 2007;35:W701–W706.
  • Karabacak NM, Li L, Tiwari A, 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.
  • Frank AM, Pesavento JJ, Mizzen CA, et al. Interpreting top-down mass spectra using spectral alignment. Anal Chem. 2008;80:2499–2505.
  • Liu X, Sirotkin Y, Shen Y, et al. Protein identification using top-down spectra. Mol Cell Proteomics. 2012;11:M111.008524.
  • Cai W, Guner H, Gregorich ZR, et al. MASH suite pro: a comprehensive software tool for top-down proteomics. Mol Cell Proteomics. 2016;15:703–714.
  • de Tombe PP, Solaro RJ. Integration of cardiac myofilament activity and regulation with pathways signaling hypertrophy and failure. Ann Biomed Eng. 2000;28:991–1001.
  • Yin Z, Ren J, Guo W. Sarcomeric protein isoform transitions in cardiac muscle: a journey to heart failure. Biochim Biophys Acta. 2015;1852:47–52.
  • Peng Y, Yu D, Gregorich Z, et al. In-depth proteomic analysis of human tropomyosin by top-down mass spectrometry. J Muscle Res Cell Motil. 2013;34:199–210.
  • Peng Y, Chen X, Zhang H, et al. Top-down targeted proteomics for deep sequencing of tropomyosin isoforms. J Proteome Res. 2013;12:187–198.
  • Copeland O, Nowak KJ, Laing NG, 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.
  • Chen YC, Ayaz-Guner S, Peng Y, et al. Effective top-down LC/MS+ method for assessing actin isoforms as a potential cardiac disease marker. Anal Chem. 2015;87:8399–8406.
  • Gry M, Rimini R, Strömberg S, et al. Correlations between RNA and protein expression profiles in 23 human cell lines. BMC Genomics. 2009;10:365.
  • Solaro RJ, van der Velden J. Why does troponin I have so many phosphorylation sites? Fact and fancy. J Mol Cell Cardiol. 2010;48:810–816.
  • Hunter T. The age of crosstalk: phosphorylation, ubiquitination, and beyond. Mol Cell. 2007;28:730–738.
  • de Tombe PP. Myosin binding protein C in the heart. Circ Res. 2006;98:1234–1236.
  • Flashman E, Redwood C, Moolman-Smook J, et al. Cardiac myosin binding protein C: its role in physiology and disease. Circ Res. 2004;94:1279–1289.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.