Top-down proteomics in health and disease: Challenges and opportunities

Proteomics

Volumn 14, Issue 10, 2014, Pages 1195-1210

  Gregorich, Zachery R ^a,b   Ge, Ying ^a,b  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

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

Author keywords

Human disease; Mass spectrometry; Proteomics; PTMs; Systems biology

Indexed keywords

AMYLOIDOSIS; CARDIOVASCULAR DISEASE; DEGENERATIVE DISEASE; DIABETES MELLITUS; HEALTH; HUMAN; INFECTION; MASS SPECTROMETRY; MEDICAL RESEARCH; NEOPLASM; PHYSICAL DISEASE BY ANATOMICAL STRUCTURE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEOMICS; REVIEW; SICKLE CELL ANEMIA; DISEASES; CHEMISTRY; COMMUNICABLE DISEASE; METABOLISM; PROTEIN PROCESSING; SYSTEMS BIOLOGY;

BIOLOGICAL MARKER; PROTEOME;

BIOLOGICAL MARKERS; CARDIOVASCULAR DISEASES; COMMUNICABLE DISEASES; DIABETES MELLITUS; HUMANS; MASS SPECTROMETRY; NEOPLASMS; NEURODEGENERATIVE DISEASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME; PROTEOMICS; SYSTEMS BIOLOGY;

EID: 84899827440     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201300432     Document Type: Review

References (136)

1. Sabido, E., Selevsek, N., Aebersold, R., Mass spectrometry-based proteomics for systems biology. Curr. Opin. Biotechnol. 2012, 23, 591-597.
2. Drake, T. A., Ping, P. P., Proteomics approaches to the systems biology of cardiovascular diseases. J. Lipid Res. 2007, 48, 1-8.
3. Altelaar, A. F. M. J., Heck, A. J., Next-generation proteomics: towards an integrative view of proteome dynamics. Nat. Rev. Genet. 2013, 14, 35-48.
4. Patterson, S. D., Aebersold, R. H., Proteomics: the first decade and beyond. Nat. Genet. 2003, 33(Suppl), 311-323.
5. Yates, J. R., Mass spectrometry as an emerging tool for systems biology. Biotechniques 2004, 36, 917-919.
6. Mann, M., Jensen, O. N., Proteomic analysis of post-translational modifications. Nat. Biotechnol. 2003, 21, 255-261.
7. Krueger, K. E., Srivastava, S., Posttranslational protein modifications-current implications for cancer detection, prevention, and therapeutics. Mol. Cell. Proteomics 2006, 5, 1799-1810.
8. Karve, T. M., Cheema, A. K., Small changes huge impact: the role of protein posttranslational modifications in cellular homeostasis and disease. J. Amino Acids 2011, 2011, 207691.
9. Futreal, P. A., Coin, L., Marshall, M., Down, T. et al., A census of human cancer genes. Nat. Rev. Cancer 2004, 4, 177-183.
10. Morita, H., Seidman, J., Seidman, C. E., Genetic causes of human heart failure. J. Clin. Invest. 2005, 115, 518-526.
11. Smith, L. M., Kelleher, N. L., Proteoform: a single term describing protein complexity. Nat. Methods 2013, 10, 186-187.
12. Nedelkov, D., Kiernan, U. A., Niederkofler, E. E., Tubbs, K. A., Nelson, R. W., Population proteomics: the concept, attributes, and potential for cancer biomarker research. Mol. Cell. Proteomics 2006, 5, 1811-1818.
13. Chait, B. T., Mass spectrometry: bottom-up or top-down? Science 2006, 314, 65-66.
14. Siuti, N., Kelleher, N. L., Decoding protein modifications using top-down mass spectrometry. Nat. Methods 2007, 4, 817-821.
15. Zhang, H., Ge, Y., Comprehensive analysis of protein modifications by top-down mass spectrometry. Circ. Cardiovasc. Genet. 2011, 4, 711.
16. Tipton, J. D., Tran, J. C., Catherman, A. D., Ahlf, D. R. et al., Analysis of intact protein isoforms by mass spectrometry. J. Biol. Chem. 2011, 286, 25451-25458.
17. Kelleher, N. L., Lin, H. Y., Valaskovic, G. A., Aaserud, D. J. et al., Top down versus bottom up protein characterization by tandem high-resolution mass spectrometry. J. Am. Chem. Soc. 1999, 121, 806-812.
18. Ge, Y., Lawhorn, B. G., ElNaggar, M., Strauss, E. et al., Top down characterization of larger proteins (45 kDa) by electron capture dissociation mass spectrometry. J. Am. Chem. Soc. 2002, 124, 672-678.
19. Ayaz-Guner, S., Zhang, J., Li, L., Walker, J. W., Ge, Y., 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.
20. Ge, Y., Rybakova, I. N., Xu, Q., Moss, R. L., Top-down high-resolution mass spectrometry of cardiac myosin binding protein C revealed that truncation alters protein phosphorylation state. Proc. Natl. Acad. Sci. USA 2009, 106, 12658-12663.
21. Sancho Solis, R., Ge, Y., Walker, J. W., 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.
22. Zabrouskov, V., Ge, Y., Schwartz, J., Walker, J. W., Unraveling molecular complexity of phosphorylated human cardiac troponin I by top down electron capture dissociation/electron transfer dissociation mass spectrometry. Mol. Cell. Proteomics 2008, 7, 1838-1849.
23. Zabrouskov, V., Han, X., Welker, E., Zhai, H. et al., Stepwise deamidation of ribonuclease A at five sites determined by top down mass spectrometry. Biochemistry 2006, 45, 987-992.
24. Zhang, J., Dong, X., Hacker, T. A., Ge, Y., Deciphering modifications in swine cardiac troponin I by top-down high-resolution tandem mass spectrometry. J. Am. Soc. Mass Spectrom. 2010, 21, 940-948.
25. Armirotti, A., Damonte, G., Achievements and perspectives of top-down proteomics. Proteomics 2010, 10, 3566-3576.
26. Zubarev, R. A., Horn, D. M., Fridriksson, E. K., Kelleher, N. L. et al., Electron capture dissociation for structural characterization of multiply charged protein cations. Anal. Chem. 2000, 72, 563-573.
27. Syka, J. E., Coon, J. J., Schroeder, M. J., Shabanowitz, J., Hunt, D. F., Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl. Acad. Sci. USA 2004, 101, 9528-9533.
28. Cooper, H. J., Hakansson, K., Marshall, A. G., The role of electron capture dissociation in biomolecular analysis. Mass Spectrom. Rev. 2005, 24, 201-222.
29. Eliuk, S. M., Maltby, D., Panning, B., Burlingame, A. L., High resolution electron transfer dissociation studies of unfractionated intact histones from murine embryonic stem cells using on-line capillary LC separation: determination of abundant histone isoforms and post-translational modifications. Mol. Cell. Proteomics 2010, 9, 824-837.
30. Tian, Z., Tolic, N., Zhao, R., Moore, R. J. et al., Enhanced top-down characterization of histone post-translational modifications. Genome Biol. 2012, 13, R86.
31. Mazur, M. T., Cardasis, H. L., Spellman, D. S., Liaw, A. et al., Quantitative analysis of intact apolipoproteins in human HDL by top-down differential mass spectrometry. Proc. Natl. Acad. Sci. USA 2010, 107, 7728-7733.
32. Edwards, R. L., Griffiths, P., Bunch, J., Cooper, H. J., Top-down proteomics and direct surface sampling of neonatal dried blood spots: diagnosis of unknown hemoglobin variants. J. Am. Soc. Mass. Spectrom 2012, 23, 1921-1930.
33. Coelho Graça, D., Lescuyer, P., Clerici, L., Tsybin, Y. O. et al., Electron transfer dissociation mass spectrometry of hemoglobin on clinical samples. J. Am. Soc. Mass. Spectrom. 2012, 23, 1750-1756.
34. Zhang, J., Guy, M. J., Norman, H. S., Chen, Y. C. 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.
35. Ansong, C., Wu, S., Meng, D., Liu, X. 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. USA 2013, 110, 10153-10158.
36. Auclair, J. R., Boggio, K. J., Petsko, G. A., Ringe, D., Agar, J. N., Strategies for stabilizing superoxide dismutase (SOD1), the protein destabilized in the most common form of familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 2010, 107, 21394-21399.
37. Borges, C. R., Oran, P. E., Buddi, S., Jarvis, J. W. et al., Building multidimensional biomarker views of type 2 diabetes on the basis of protein microheterogeneity. Clin. Chem. 2011, 57, 719-728.
38. Burnaevskiy, N., Fox, T. G., Plymire, D. A., Ertelt, J. M. et al., Proteolytic elimination of N-myristoyl modifications by the Shigella virulence factor Ipa. J. Nat. 2013, 496, 106-109.
39. Chamot-Rooke, J., Mikaty, G., Malosse, C., Soyer, M. et al., Posttranslational modification of pili upon cell contact triggers N. meningitidis dissemination. Science 2011, 331, 778-782.
40. Desiderio, C., D'Angelo, L., Rossetti, D. V., Iavarone, F. et al., Cerebrospinal fluid top-down proteomics evidenced the potential biomarker role of LVV- and VV-hemorphin-7 in posterior cranial fossa pediatric brain tumors. Proteomics 2012, 12, 2158-2166.
41. Dong, X., Sumandea, C. A., Chen, Y. C., Garcia-Cazarin, M. L. et al., Augmented phosphorylation of cardiac troponin I in hypertensive heart failure. J. Biol. Chem. 2012, 287, 848-857.
42. Molnar, K. S., Karabacak, N. M., Johnson, J. L., Wang, Q. et al., A common property of amyotrophic lateral sclerosis-associated variants: destabilization of the copper/zinc superoxide dismutase electrostatic loop. J. Biol. Chem. 2009, 284, 30965-30973.
43. Nepomuceno, A. I., Mason, C. J., Muddiman, D. C., Bergen, H. R., 3rd, Zeldenrust, S. R., Detection of genetic variants of transthyretin by liquid chromatography-dual electrospray ionization Fourier-transform ion-cyclotron-resonance mass spectrometry. Clin. Chem. 2004, 50, 1535-1543.
44. Pflieger, D., Przybylski, C., Gonnet, F., Le Caer, J. P. et al., Analysis of human C1q by combined bottom-up and top-down mass spectrometry: detailed mapping of post-translational modifications and insights into the C1r/C1s binding sites. Mol. Cell. Proteomics 2010, 9, 593-610.
45. Rauser, S., Marquardt, C., Balluff, B., Deininger, S. O. et al., Classification of HER2 receptor status in breast cancer tissues by MALDI imaging mass spectrometry. J. Proteome Res. 2010, 9, 1854-1863.
46. Theberge, R., Infusini, G., Tong, W., McComb, M. E., Costello, C. E., Top-down analysis of small plasma proteins using an LTQ-Orbitrap. Potential for mass spectrometry-based clinical assays for transthyretin and hemoglobin. Int. J. Mass Spectrom. 2011, 300, 130-142.
47. Zhang, L., Freitas, M. A., Wickham, J., Parthun, M. R. et al., Differential expression of histone post-translational modifications in acute myeloid and chronic lymphocytic leukemia determined by high-pressure liquid chromatography and mass spectrometry. J. Am. Soc. Mass Spectrom. 2004, 15, 77-86.
48. Cabras, T., Pisano, E., Montaldo, C., Giuca, M. R. et al., Significant modifications of the salivary proteome potentially associated with complications of Down syndrome revealed by top-down proteomics. Mol. Cell. Proteomics 2013, 12, 1844-1852.
49. Hardesty, W. M., Kelley, M. C., Mi, D., Low, R. L., Caprioli, R. M., Protein signatures for survival and recurrence in metastatic melanoma. J. Proteomics 2011, 74, 1002-1014.
50. Roger, V. L., Go, A. S., Lloyd-Jones, D. M., Benjamin, E. J. et al., Heart disease and stroke statistics-2012 update: a report from the American Heart Association. Circulation 2012, 125, e2-e220.
51. Messer, A. E., Jacques, A. M., Marston, S. B., Troponin phosphorylation and regulatory function in human heart muscle: dephosphorylation of Ser23/24 on troponin I could account for the contractile defect in end-stage heart failure. J. Mol. Cell. Cardiol. 2007, 42, 247-259.
52. van der Velden, J., Papp, Z., Zaremba, R., Boontje, N. M. et al., Increased Ca2+-sensitivity of the contractile apparatus in end-stage human heart failure results from altered phosphorylation of contractile proteins. Cardiovasc. Res. 2003, 57, 37-47.
53. Babuin, L., Jaffe, A. S., Troponin: the biomarker of choice for the detection of cardiac injury. Can. Med. Assoc. J. 2005, 173, 1191-1202.
54. Solaro, R. J., Rosevear, P., Kobayashi, T., The unique functions of cardiac troponin I in the control of cardiac muscle contraction and relaxation. Biochem. Biophys. Res. Commun. 2008, 369, 82-87.
55. Layland, J., Solaro, R. J., Shah, A. M., Regulation of cardiac contractile function by troponin I phosphorylation. Cardiovasc. Res. 2005, 66, 12-21.
56. Sumandea, M. P., Burkart, E. M., Kobayashi, T., De Tombe, P. P., Solaro, R. J., Molecular and integrated biology of thin filament protein phosphorylation in heart muscle. Ann. N. Y. Acad. Sci. 2004, 1015, 39-52.
57. Westfall, M. V., Borton, A. R., Role of troponin I phosphorylation in protein kinase C-mediated enhanced contractile performance of rat myocytes. J. Biol. Chem. 2003, 278, 33694-33700.
58. Kannel, W. B., Incidence and epidemiology of heart failure. Heart Fail Rev. 2000, 5, 167-173.
59. Pollin, T. I., Damcott, C. M., Shen, H., Ott, S. H. et al., A null mutation in human APOC3 confers a favorable plasma lipid profile and apparent cardioprotection. Science 2008, 322, 1702-1705.
60. Chen, L., Magliano, D. J., Zimmet, P. Z., The worldwide epidemiology of type 2 diabetes mellitus-present and future perspectives. Nat. Rev. Endocrinol. 2012, 8, 228-236.
61. Nissen, S. E., Wolski, K., Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N. Engl. J. Med. 2007, 356, 2457-2471.
62. Nissen, S. E., Wolski, K., Rosiglitazone revisited: an updated meta-analysis of risk for myocardial infarction and cardiovascular mortality. Arch. Intern. Med. 2010, 170, 1191-1201.
63. Reitz, C., Brayne, C., Mayeux, R., Epidemiology of Alzheimer disease. Nat. Rev. Neurol. 2011, 7, 137-152.
64. LaVoie, M. J., Ostaszewski, B. L., Weihofen, A., Schlossmacher, M. G., Selkoe, D. J., Dopamine covalently modifies and functionally inactivates parkin. Nat. Med. 2005, 11, 1214-1221.
65. Yan, S. D., Chen, X., Schmidt, A. M., Brett, J. et al., Glycated tau protein in Alzheimer disease: a mechanism for induction of oxidant stress. Proc. Natl. Acad. Sci. USA 1994, 91, 7787-7791.
66. Kabashi, E., Valdmanis, P. N., Dion, P., Rouleau, G. A., Oxidized/misfolded superoxide dismutase-1: the cause of all amyotrophic lateral sclerosis? Ann. Neurol. 2007, 62, 553-559.
67. Rakhit, R., Crow, J. P., Lepock, J. R., Kondejewski, L. H. et al., Monomeric Cu, Zn-superoxide dismutase is a common misfolding intermediate in the oxidation models of sporadic and familial amyotrophic lateral sclerosis. J. Biol. Chem. 2004, 279, 15499-15504.
68. Shibata, N., Hirano, A., Kobayashi, M., Sasaki, S. et al., Cu/Zn superoxide dismutase-like immunoreactivity in Lewy body-like inclusions of sporadic amyotrophic lateral sclerosis. Neurosci. Lett. 1994, 179, 149-152.
69. Elam, J. S., Taylor, A. B., Strange, R., Antonyuk, S. et al., Amyloid-like filaments and water-filled nanotubes formed by SOD1 mutant proteins linked to familial ALS. Nat. Struct. Biol. 2003, 10, 461-467.
70. Auclair, J. R., Johnson, J. L., Liu, Q., Salisbury, J. P. et al., Post-translational modification by cysteine protects Cu/Zn-superoxide dismutase from oxidative damage. Biochemistry 2013, 52, 6137-6144.
71. Qin, W., Ho, L., Wang, J., Peskind, E., Pasinetti, G. M., S100A7, a novel Alzheimer's disease biomarker with non-amyloidogenic alpha-secretase activity acts via selective promotion of ADAM-10. PLoS One 2009, 4, e4183.
72. Dhillon, A. S., Hagan, S., Rath, O., Kolch, W., MAP kinase signalling pathways in cancer. Oncogene 2007, 26, 3279-3290.
73. Julien, S. G., Dube, N., Hardy, S., Tremblay, M. L., Inside the human cancer tyrosine phosphatome. Nat. Rev. Cancer 2011, 11, 35-49.
74. Marks, P., Rifkind, R. A., Richon, V. M., Breslow, R. et al., Histone deacetylases and cancer: causes and therapies. Nat. Rev. Cancer 2001, 1, 194-202.
75. Carroll, J., Fearnley, I. M., Walker, J. E., Definition of the mitochondrial proteome by measurement of molecular masses of membrane proteins. Proc. Natl. Acad. Sci. USA 2006, 103, 16170-16175.
76. Catherman, A. D., Li, M., Tran, J. C., Durbin, K. R. et al., Top down proteomics of human membrane proteins from enriched mitochondrial fractions. Anal. Chem. 2013, 85, 1880-1888.
77. Whitelegge, J., Halgand, F., Souda, P., Zabrouskov, V., Top-down mass spectrometry of integral membrane proteins. Expert Rev. Proteomics 2006, 3, 585-596.
78. Whitelegge, J. P., HPLC and mass spectrometry of intrinsic membrane proteins. Methods Mol. Biol. 2004, 251, 323-340.
79. Whitelegge, J. P., le Coutre, J., Lee, J. C., Engel, C. K. et al., Toward the bilayer proteome, electrospray ionization-mass spectrometry of large, intact transmembrane proteins. Proc. Natl. Acad. Sci. USA 1999, 96, 10695-10698.
80. Whitelegge, J. P., Zhang, H., Aguilera, R., Taylor, R. M., Cramer, W. A., Full subunit coverage liquid chromatography electrospray ionization mass spectrometry (LCMS+) of an oligomeric membrane protein: cytochrome b(6)f complex from spinach and the cyanobacterium Mastigocladus laminosus. Mol. Cell. Proteomics 2002, 1, 816-827.
81. Laganowsky, A., Reading, E., Hopper, J. T., Robinson, C. V., Mass spectrometry of intact membrane protein complexes. Nat. Protoc. 2013, 8, 639-651.
82. Catherman, A. D., Li, M., Tran, J. C., Durbin, K. R. et al., Top down proteomics of human membrane proteins from enriched mitochondrial fractions. Anal. Chem. 2013, 85, 1880-1888.
83. Doucette, A. A., Tran, J. C., Wall, M. J., Fitzsimmons, S., Intact proteome fractionation strategies compatible with mass spectrometry. Expert Rev. Proteomics 2011, 8, 787-800.
84. Kellie, J. F., Tran, J. C., Lee, J. E., Ahlf, D. R. et al., The emerging process of Top Down mass spectrometry for protein analysis: biomarkers, protein-therapeutics, and achieving high throughput. Mol. Biosyst. 2010, 6, 1532-1539.
85. Washburn, M. P., Wolters, D., Yates, J. R., 3rd, Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat. Biotechnol. 2001, 19, 242-247.
86. Wolters, D. A., Washburn, M. P., Yates, J. R., 3rd. An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 2001, 73, 5683-5690.
87. Tran, J. C., Zamdborg, L., Ahlf, D. R., Lee, J. E. et al., Mapping intact protein isoforms in discovery mode using top-down proteomics. Nature 2011, 480, 254-258.
88. Neverova, I., Van Eyk, J. E., Role of chromatographic techniques in proteomic analysis. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2005, 815, 51-63.
89. Hage, D. S., Affinity chromatography: a review of clinical applications. Clin. Chem. 1999, 45, 593-615.
90. de Frutos, M., Regnier, F. E., Tandem chromatographic-immunological analyses. Anal. Chem. 1993, 65, 17A-25A.
91. Nelson, R. W., Krone, J. R., Bieber, A. L., Williams, P., Mass spectrometric immunoassay. Anal. Chem. 1995, 67, 1153-1158.
92. Niederkofler, E. E., Tubbs, K. A., Kiernan, U. A., Nedelkov, D., Nelson, R. W., Novel mass spectrometric immunoassays for the rapid structural characterization of plasma apolipoproteins. J. Lipid Res. 2003, 44, 630-639.
93. Compton, P. D., Zamdborg, L., Thomas, P. M., Kelleher, N. L., On the scalability and requirements of whole protein mass spectrometry. Anal. Chem. 2011, 83, 6868-6874.
94. Alpert, A. J., Size exclusion high-performance liquid chromatography of small solutes, in: Wu, C.-S. (Ed.), Column Handbook for Size Exclusion Chromatography, Academic Press, San Diego, CA 1999, pp. 249-266.
95. Doucette, A. A., Tran, J. C., Wall, M. J., Fitzsimmons, S., Intact proteome fractionation strategies compatible with mass spectrometry. Expert Rev. Proteomics 2011, 8, 787-800.
96. Chen, X., Ge, Y., Ultrahigh pressure fast size exclusion chromatography for top-down proteomics. Proteomics 2013, 13, 2563-2566.
97. Sharma, S., Simpson, D. C., Tolic, N., Jaitly, 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.
98. Simpson, D. C., Ahn, S., Pasa-Tolic, L., Bogdanov, B. et al., Using size exclusion chromatography-RPLC and RPLC-CIEF as two-dimensional separation strategies for protein profiling. Electrophoresis 2006, 27, 2722-2733.
99. Neverova, I., Van Eyk, J. E., Role of chromatographic techniques in proteomic analysis. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2005, 815, 51-63.
100. Gundry, R. L., Fu, Q., Jelinek, C. A., Van Eyk, J. E., Cotter, R. J., Investigation of an albumin-enriched fraction of human serum and its albuminome. Proteomics Clin. Appl. 2007, 1, 73-88.
101. Iavarone, A. T., Williams, E. R., Mechanism of charging and supercharging molecules in electrospray ionization. J. Am. Chem. Soc. 2003, 125, 2319-2327.
102. Lomeli, S. H., Yin, S., Ogorzalek Loo, R. R., Loo, J. A., Increasing charge while preserving noncovalent protein complexes for ESI-MS. J. Am. Soc. Mass Spectrom. 2009, 20, 593-596.
103. Valeja, S. G., Tipton, J. D., Emmett, M. R., Marshall, A. G., New reagents for enhanced liquid chromatographic separation and charging of intact protein ions for electrospray ionization mass spectrometry. Anal. Chem. 2010, 82, 7515-7519.
104. Miladinovic, S. M., Fornelli, L., Lu, Y., Piech, K. M. et al., In-spray supercharging of peptides and proteins in electrospray ionization mass spectrometry. Anal. Chem. 2012, 84, 4647-4651.
105. Park, J., Qin, H., Scalf, M., Hilger, R. T. et al., A mechanical nanomembrane detector for time-of-flight mass spectrometry. Nano Lett. 2011, 11, 3681-3684.
106. Chen, X., Westphall, M. S., Smith, L. M., Mass spectrometric analysis of DNA mixtures: instrumental effects responsible for decreased sensitivity with increasing mass. Anal. Chem. 2003, 75, 5944-5952.
107. Kelleher, N. L., Senko, M. W., Siegel, M. M., McLafferty, F. W., Unit resolution mass spectra of 112 kDa molecules with 3 Da accuracy. J. Am. Soc. Mass Spectrom. 1997, 8, 380-383.
108. Valeja, S. G., Kaiser, N. K., Xian, F., Hendrickson, C. L. 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.
109. Kostyukevich, Y. I., Vladimirov, G. N., Nikolaev, E. N., 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.
110. Turecek, F., N[bond]C(alpha) bond dissociation energies and kinetics in amide and peptide radicals. Is the dissociation a non-ergodic process? J. Am. Chem. Soc. 2003, 125, 5954-5963.
111. Breuker, K., McLafferty, F. W., Stepwise evolution of protein native structure with electrospray into the gas phase, 10(-12) to 10(2) s. Proc. Natl. Acad. Sci. USA 2008, 105, 18145-18152.
112. Breuker, K., Oh, H., Horn, D. M., Cerda, B. A., McLafferty, F. W., Detailed unfolding and folding of gaseous ubiquitin ions characterized by electron capture dissociation. J. Am. Chem. Soc. 2002, 124, 6407-6420.
113. Peng, Y., Chen, X., Zhang, H., Xu, Q. et al., Top-down targeted proteomics for deep sequencing of tropomyosin isoforms. J. Proteome Res. 2013, 12, 187-198.
114. Han, X., Jin, M., Breuker, K., McLafferty, F. W., Extending top-down mass spectrometry to proteins with masses greater than 200 kilodaltons. Science 2006, 314, 109-112.
115. Shaw, J. B., Li, W., Holden, D. D., Zhang, Y. et al., Complete protein characterization using top-down mass spectrometry and ultraviolet photodissociation. J. Am. Chem. Soc. 2013, 135, 12646-12651.
116. Bantscheff, M., Schirle, M., Sweetman, G., Rick, J., Kuster, B., Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 2007, 389, 1017-1031.
117. Ong, S. E., Mann, M., Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 2005, 1, 252-262.
118. Pesavento, J. J., Mizzen, C. A., Kelleher, N. L., Quantitative analysis of modified proteins and their positional isomers by tandem mass spectrometry: human histone H4. Anal. Chem. 2006, 78, 4271-4280.
119. Jiang, L., Smith, J. N., Anderson, S. L., Ma, P. et al., Global assessment of combinatorial post-translational modification of core histones in yeast using contemporary mass spectrometry. LYS4 trimethylation correlates with degree of acetylation on the same H3 tail. J. Biol. Chem. 2007, 282, 27923-27934.
120. Pesavento, J. J., Bullock, C. R., LeDuc, R. D., Mizzen, C. A., Kelleher, N. L., Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J. Biol. Chem. 2008, 283, 14927-14937.
121. Du, Y., Parks, B. A., Sohn, S., Kwast, K. E., Kelleher, N. L., Top-down approaches for measuring expression ratios of intact yeast proteins using Fourier transform mass spectrometry. Anal. Chem. 2006, 78, 686-694.
122. Waanders, L. F., Hanke, S., Mann, M., Top-down quantitation and characterization of SILAC-labeled proteins. J. Am. Soc. Mass. Spectrom. 2007, 18, 2058-2064.
123. Collier, T. S., Hawkridge, A. M., Georgianna, D. R., Payne, G. A., Muddiman, D. C., Top-down identification and quantification of stable isotope labeled proteins from Aspergillus flavus using online nano-flow reversed-phase liquid chromatography coupled to a LTQ-FTICR mass spectrometer. Anal. Chem. 2008, 80, 4994-5001.
124. Collier, T. S., Sarkar, P., Rao, B., Muddiman, D. C., Quantitative top-down proteomics of SILAC labeled human embryonic stem cells. J. Am. Soc. Mass. Spectrom. 2010, 21, 879-889.
125. Bergmann, U., Ahrends, R., Neumann, B., Scheler, C., Linscheid, M. W., 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.
126. Tsur, D., Tanner, S., Zandi, E., Bafna, V., Pevzner, P. A., Identification of post-translational modifications by blind search of mass spectra. Nat. Biotechnol. 2005, 23, 1562-1567.
127. Horn, D. M., Zubarev, R. A., McLafferty, F. W., Automated reduction and interpretation of high resolution electrospray mass spectra of large molecules. J. Am. Soc. Mass. Spectrom. 2000, 11, 320-332.
128. Jaitly, N., Mayampurath, A., Littlefield, K., Adkins, J. N. et al., Decon2LS: an open-source software package for automated processing and visualization of high resolution mass spectrometry data. BMC Bioinform. 2009, 10, 87.
129. Guner, H., Close, P. L., Cai, W., Zhang, H. et al., MASH suite: a user-friendly and versatile software interface for high-resolution mass spectrometry data interpretation and visualization. J. Am. Soc. Mass Spectrom. 2014, 25, 464-470.
130. Liu, X., Inbar, Y., Dorrestein, P. C., Wynne, C. et al., Deconvolution and database search of complex tandem mass spectra of intact proteins: a combinatorial approach. Mol. Cell. Proteomics 2010, 9, 2772-2782.
131. Perkel, J. M., Tearing the top off "Top-Down" Proteomics. Biotechniques 2012, 53, 75-78.
132. Zamdborg, L., LeDuc, R. D., Glowacz, K. J., Kim, Y. B. et al., ProSight PTM 2.0: improved protein identification and characterization for top down mass spectrometry. Nucleic Acids Res. 2007, 35, W701-W706.
133. Tsai, Y. S., Scherl, A., Shaw, J. L., MacKay, C. L. et al., Precursor ion independent algorithm for top-down shotgun proteomics. J. Am. Soc. Mass. Spectrom. 2009, 20, 2154-2166.
134. Liu, X., Sirotkin, Y., Shen, Y., Anderson, G. et al., Protein identification using top-down. Mol. Cell. Proteomics 2012, 11, M111 008524.
135. Brower, V., Proteomics: biology in the post-genomic era. Companies all over the world rush to lead the way in the new post-genomics race. EMBO Rep. 2001, 2, 558-560.
136. Savaryn, J. P., Catherman, A. D., Thomas, P. M., Abecassis, M. M., Kelleher, N. L., The emergence of top-down proteomics in clinical research. Genome Med. 2013, 5, 53.