Chemical tools for temporally and spatially resolved mass spectrometry-based proteomics

Annals of Biomedical Engineering

Volumn 42, Issue 2, 2014, Pages 299-311

  Yuet, Kai P ^a   Tirrell, David A ^a  

^a California Institute of Technology   (United States)

Author keywords

APEX; BONCAT; Protein synthesis; SILAC

Indexed keywords

BIOSYNTHESIS; CELLS; CYTOLOGY; DEGRADATION; MASS SPECTROMETRY; MOLECULAR BIOLOGY; TOOLS;

APEX; BONCAT; CHEMICAL AND BIOLOGICALS; COMPLEX MICROBIAL SYSTEMS; LOW-ABUNDANCE PROTEINS; PROTEIN SYNTHESIS; SILAC; TISSUE HETEROGENEITY;

PROTEINS;

ASCORBATE PEROXIDASE; INTERMEDIATE FILAMENT PROTEIN; METHIONINE; METHIONINE TRANSFER RNA LIGASE; MICRORNA;

BIOORTHOGONAL NON CANONICAL AMINO ACID TAGGING; CELL CULTURE; CELL TYPE; CONFERENCE PAPER; FLOW CYTOMETRY; HUMAN; INTRACELLULAR SPACE; ISOTOPE LABELING; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEOMICS; PULSED STABLE ISOTOPE LABELING WITH AMINO ACID IN CELL CULTURE; QUANTITATIVE NON CANONICAL AMINO ACID TAGGING;

MASS SPECTROMETRY; PROTEOMICS;

EID: 84899444682     PISSN: 00906964     EISSN: 15739686     Source Type: Journal    
DOI: 10.1007/s10439-013-0878-3     Document Type: Conference Paper

References (96)

1. Aebersold, R., and M. Mann. Mass spectrometry-based proteomics. Nature 422:198-207, 2003.
2. Agard, N., J. Prescher, and C. Bertozzi. A strain-promoted [3+2] azide-alkyne cycloaddition for covalent modification of biomolecules in living systems. J. Am. Chem. Soc. 126:15046-15047, 2004.
3. Ahrens, C. H., E. Brunner, E. Qeli, K. Basler, and R. Aebersold. Generating and navigating proteome maps using mass spectrometry. Nat. Rev. Mol. Cell Biol. 11:789-801, 2010.
4. Bantscheff, M., M. Schirle, G. Sweetman, J. Rick, and B. Kuster. Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 389:1017-1031, 2007.
5. Bantscheff, M., S. Lemeer, M. H. Savitski, and B. Kuster. Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal. Bioanal. Chem. 404:939-965, 2012.
6. Beatty, K., F. Xie, Q. Wang, and D. Tirrell. Selective dyelabeling of newly synthesized proteins in bacterial cells. J. Am. Chem. Soc. 127:14150-14151, 2005.
7. Beatty, K., J. Liu, F. Xie, D. Dieterich, E. Schuman, Q. Wang, and D. Tirrell. Fluorescence visualization of newly synthesized proteins in mammalian cells. Angew. Chem. Int. Ed. 45:7364-7367, 2006.
8. Black, D. L. Protein diversity from alternative splicing: a challenge for bioinformatics and post-genome biology. Cell 103:367-370, 2000.
9. Boisvert, F. M., Y. W. Lam, D. Lamont, and A. I. Lamond. A quantitative proteomics analysis of subcellular proteome localization and changes induced by DNA damage. Mol. Cell. Proteomics 9:457-470, 2010.
10. Brunet, I., C. Weinl, M. Piper, A. Trembleau, M. Volovitch, W. Harris, A. Prochiantz, and C. Holt. The transcription factor Engrailed-2 guides retinal axons. Nature 438:94-98, 2005.
11. Corthals, G. L., V. C. Wasinger, D. F. Hochstrasser, and J. C. Sanchez. The dynamic range of protein expression: a challenge for proteomic research. Electrophoresis 21:1104-1115, 2000.
12. Cox, J., N. Neuhauser, A. Michalski, R. A. Scheltema, J. V. Olsen, and M. Mann. Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 10:1794-1805, 2011.
13. Deal, R. B., and S. Henikoff. A simple method for gene expression and chromatin profiling of individual cell types within a tissue. Dev. Cell 18:1030-1040, 2010.
14. Deal, R. B., J. G. Henikoff, and S. Henikoff. Genome-wide kinetics of nucleosome turnover determined by metabolic labeling of histones. Science 328:1161-1164, 2010.
15. De Godoy, L. M. F., J. V. Olsen, J. Cox, M. L. Nielsen, N. C. Hubner, F. Frohlich, T. C. Walther, and M. Mann. Comprehensive mass spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455:1251-1254, 2008.
16. De Sousa Abreu, R., L. O. Penalva, E. M. Marcotte, and C. Vogel. Global signatures of protein and mRNA expression levels. Mol. Biosyst. 5:1512-1526, 2009.
17. Dieterich, D. C., A. J. Link, J. Graumann, D. A. Tirrell, and E. M. Schuman. Selective identification of newly synthesized proteins in mammalian cells using bioorthogonal noncanonical amino acid tagging (BONCAT). Proc. Natl. Acad. Sci. USA 103:9482-9487, 2006.
18. Dieterich, D. C., J. Hodas, G. Gouzer, I. Shadrin, J. Ngo, A. Triller, D. Tirrell, and E. Schuman. In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons. Nat. Neurosci. 13:897-905, 2010.
19. Eichelbaum, K., M. Winter, M. B. Diaz, S. Herzig, and J. Krijgsveld. Selective enrichment of newly synthesized proteins for quantitative secretome analysis. Nat. Biotechnol. 30:984-990, 2012.
20. Essader, A. S., B. J. Cargile, J. L. Bundy, and J. L. Stephenson. A comparison of immobilized pH gradient isoelectric focusing and strong cation-exchange chromatography as a first dimension in shotgun proteomics. Proteomics 5:24-34, 2005.
21. Fredens, J., K. Engholm-Keller, A. Giessing, D. Pultz, M. R. Larsen, P. Højrup, J. Møller-Jensen, and N. J. Færgeman. Quantitative proteomics by amino acid labeling in C. elegans. Nat. Methods 8:845-847, 2011.
22. Friedel, C. C., L. Dolken, Z. Ruzsics, U. H. Koszinowski, and R. Zimmer. Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res. 37:e115, 2009.
23. Gay, L., M. R. Miller, P. B. Ventura, V. Devasthali, Z. Vue, H. L. Thompson, S. Temple, H. Zong, M. D. Cleary, K. Stankunas, and C. Q. Doe. Mouse TU tagging: a chemical/genetic intersectional method for purifying cell type-specific nascent RNA. Genes Dev. 27:98-115, 2013.
24. Golebiowski, F., I. Matic, M. H. Tatham, C. Cole, Y. Yin, A. Nakamura, J. Cox, G. J. Barton, M. Mann, and R. T. Hay. System-wide changes to SUMO modifications in response to heat shock. Sci. Signal. 2: ra24, 2009.
25. Grammel, M., M. M. Zhang, and H. C. Hang. Orthogonal alkynyl-amino acid reporter for selective labeling of bacterial proteomes during infection. Angew. Chem. Int. Ed. 49:5970-5974, 2010.
26. Gresham, D., M. J. Dunham, and D. Botstein. Comparing whole genomes using DNA microarrays. Nat. Rev. Genet. 9:291-302, 2008.
27. Gygi, S. P., B. Rist, S. A. Gerber, F. Turecek, M. H. Gelb, and R. Aebersold. Quantitative analysis of complex protein mixtures using isotope coded affinity tags. Nat. Biotechnol. 17:994-999, 1999.
28. Henry, G. L., F. P. Davis, S. Picard, and S. R. Eddy. Cell type-specific genomics of Drosophila neurons. Nucleic Acids Res. 40:9691-9704, 2012.
29. Hinz, F. I., D. C. Dieterich, D. A. Tirrell, and E. M. Schuman. Noncanonical amino acid labeling in vivo to visualize and affinity purify newly synthesized proteins in larval zebrafish. ACS Chem. Neurosci. 3:40-49, 2012.
30. Hodas, J. J. L., A. Nehring, N. Hoche, M. J. Sweredoski, R. Pieolt, S. Hess, D. A. Tirrell, D. C. Dieterich, and E. M. Schuman. Dopaminergic modulation of the hippocampal neuropil proteome identified by bioorthogonal noncanonical amino acid tagging (BONCAT). Proteomics 12:2464-2476, 2012.
31. Howden, A. J. M., V. Geoghegan, K. Katsch, G. Efstathiou, B. Bhushan, O. Boutureira, B. Thomas, D. C. Trudgian, B. M. Kessler, D. C. Deiterich, B. G. Davis, and O. Acuto. QuaNCAT: quantitating proteome dynamics in primary cells. Nat. Methods 10:343-346, 2013.
32. Hughes, C., and J. Krijgsveld. Developments in quantitative mass spectrometry for the analysis of proteome dynamics. Trends Biotechnol. 30:668-676, 2012.
33. Huo, Y., V. Iadevaia, Z. Yao, I. Kelly, S. Cosulich, S. Guichard, L. J. Foster, and C. G. Proud. Stable isotopelabelling analysis of the impact of inhibition of the mammalian target of rapamycin on protein synthesis. Biochem. J. 444:141-151, 2012.
34. Kaller, M., S. T. Liffers, S. Oeljeklaus, K. Kuhlmann, S. Roh, R. Hoffmann, B. Warscheid, and H. Hermeking. Genome-wide characterization of miR-34a induced changes in protein and mRNA expression by a combined pulsed SILAC and microarray analysis. Mol. Cell. Proteomics 10:M111.010462, 2011.
35. Khidekel, N., S. B. Ficarro, E. C. Peters, and L. C. Hsieh-Wilson. Exploring the O-GlcNAc proteome: direct identification of O-GlcNAc-modified proteins. Proc. Natl. Acad. Sci. USA 101:13132-13137, 2004.
36. Kiick, K. L., E. Saxon, D. A. Tirrell, and C. R. Bertozzi. Incorporation of azides into recombinant proteins for chemoselective modification by the Staudinger ligation. Proc. Natl. Acad. Sci. USA 99:19-24, 2002.
37. Kraft-Terry, S. D., and H. E. Gendelman. Proteomic biosignatures for monocyte-macrophage differentiation. Cell. Immunol. 271:239-255, 2011.
38. Kramer, G., R. R. Sprenger, M. A. Nessen, W. Roseboom, D. Speijer, L. De Jong, M. J. De Mattos, J. Back, and C. G. De Koster. Proteome-wide alterations in Escherichia coli translation rates upon anaerobiosis. Mol. Cell. Proteomics 9:2508-2516, 2010.
39. Kramer, G., R. R. Sprenger, J. Back, H. L. Dekker, M. A. Nessen, J. H. Van Maarseveen, L. J. De Koning, K. J. Hellingwerf, D. De Jong, and C. G. De Koster. Identification and quantitation of newly synthesized proteins in Escherichia coli by enrichment of azidohomoalanine-labeled peptides with diagonal chromatography. Mol. Cell. Proteomics 8:1599-1611, 2009.
40. Krijgsveld, J., R. F. Ketting, T. Mahmoudi, J. Johansen, M. Artal-Sanz, C. P. Verrijzer, R. H. A. Plasterk, and A. J. R. Heck. Metabolic labeling of C. elegans and D. melanogaster for quantitative proteomics. Nat. Biotechnol. 21:927-931, 2003.
41. Kruger, M., M. Moser, S. Ussar, I. Thievessen, C. A. Luber, F. Forner, S. Schmidt, S. Zanivan, R. Fassler, and M. Mann. SILAC mouse for quantitative proteomics uncovers Kindlin-3 as an essential factor for red blood cell function. Cell 134:353-364, 2008.
42. Lam, Y. W., A. I. Lamond, M. Mann, and J. S. Andersen. Analysis of nucleolar protein dynamics reveals the nuclear degradation of ribosomal proteins. Curr. Biol. 17:749-760, 2007.
43. Larance, M., A. P. Bailly, E. Pourkarimi, R. T. Hay, G. Buchanan, S. Coulthurst, D. P. Xirodimas, A. Gartner, and A. I. Lamond. Stable isotope labeling with amino acids in nematodes. Nat. Methods 8:849-851, 2011.
44. Larrabee, K. L., J. O. Phillips, G. J. Williams, and A. R. Larrabee. The relative rates of protein synthesis and degradation in a growing culture of Escherichia coli. J. Biol. Chem. 255:4125-4130, 1980.
45. Link, A. J., M. K. S. Vink, N. J. Agard, J. A. Prescher, C. R. Bertozzi, and D. A. Tirrell. Discovery of aminoacyltRNA synthetase activity through cell-surface display of noncanonical amino acids. Proc. Natl. Acad. Sci. USA 103:10180-10185, 2006.
46. Liu, J., Y. Xu, D. Stoleru, and A. Salic. Imaging protein synthesis in cells and tissues with an alkyne analog of puromycin. Proc. Natl. Acad. Sci. USA 109:413-418, 2012.
47. Liu, K., P. Y. Yang, Z. Na, and S. Q. Yao. Dynamic monitoring of newly synthesized proteomes: up-regulation of myristoylated protein kinase A during butyric acid induced apoptosis. Angew. Chem. Int. Ed. 50:6776-6781, 2001.
48. Mahdavi, A., T. H. Segall-Shaprio, S. Kou, G. A. Jindal, K. G. Hoff, S. Liu, M. Chitsaz, R. F. Ismagilov, J. J. Silberg, and D. A. Tirrell. A genetically encoded AND gate for cell-targeted metabolic labeling of proteins. J. Am. Chem. Soc. 135:2979-2982, 2013.
49. Maier, T., M. Guell, and L. Serrano. Correlation of mRNA and protein in complex biological samples. FEBS Lett. 583:3966-3973, 2009.
50. Mann, M. Functional and quantitative proteomics using SILAC. Nat. Rev. Mol. Cell Biol. 7:952-958, 2006.
51. Martell, J. D., T. J. Deerinck, Y. Sancak, T. L. Poulos, V. K. Mootha, G. E. Sosinsky, M. H. Ellisman, and A. Y. Ting. Engineered ascorbate peroxidase as a genetically encoded reporter for electron microscopy. Nat. Biotechnol. 30:1143-1148, 2012.
52. Miller, M. R., K. J. Robinson, M. D. Cleary, and C. Q. Doe. TU-tagging: cell type-specific RNA isolation from intact complex tissues. Nat. Methods 6:439-441, 2009.
53. Milner, E., E. Barnea, I. Beer, and A. Admon. The turnover kinetics of major histocompatibility complex peptides of human cancer cells. Mol. Cell. Proteomics 5:357-365, 2006.
54. Mitulovíc, G., and K. Mechtler. HPLC techniques for proteomics analysis-a short overview of latest developments. Brief. Funct. Genomics Proteomics 5:249-260, 2006.
55. Mosteller, R., R. Goldstein, and K. Nishimoto. Metabolism of individual proteins in exponentially growing Escherichia coli. J. Biol. Chem. 255:2524-2532, 1980.
56. Nessen, M. A., G. Kramer, J. Back, J. M. Baskin, L. E. J. Smeenk, L. J. De Koning, J. H. Van Maarseveen, L. De Jong, C. R. Bertozzi, H. Hiemstra, and C. G. De Koster. Selective enrichment of azide-containing peptides from complex mixtures. J. Proteome Res. 8:3702-3711, 2009.
57. Ngo, J. T., B. M. Babin, J. A. Champion, E. M. Schuman, and D. A. Tirrell. State-selective metabolic labeling of cellular proteins. ACS Chem. Biol. 7:1326-1330, 2012.
58. Ngo, J. T., E. M. Schuman, and D. A. Tirrell. Mutant methionyl-tRNA synthetase from bacteria enables siteselective N-terminal labeling of proteins expressed in mammalian cells. Proc. Natl. Acad. Sci. USA 110:4992-4997, 2013.
59. Ngo, J. T., J. A. Champion, A. Mahdavi, I. C. Tanrikulu, K. E. Beatty, R. E. Conner, T. H. Yoo, D. C. Dieterich, E. M. Schuman, and D. A. Tirrell. Cell-selective metabolic labeling of proteins. Nat. Chem. Biol. 5:715-717, 2009.
60. Olsen, J. V., S.-E. Ong, and M. Mann. Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 3:608-614, 2004.
61. Ong, S.-E., and M. Mann. A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 1:2650-2660, 2007.
62. Patron, J. P., A. Fendler, M. Bild, U. Jung, H. Muller, M. Ø. Arntzen, C. Piso, C. Stephan, B. Thiede, H.-J. Mollenkopf, K. Jung, S. H. E. Kaufmann, and J. Schreiber. MiR-133b targets antiapoptotic genes and enhances death receptor-induced apoptosis. PLOS ONE 7:e35, 345, 2012.
63. Picotti, P., B. Bodenmiller, L. N. Mueller, B. Domon, and R. Aebersold. Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 138:795-806, 2009.
64. Picotti, P., M. Clement-Ziza, H. Lam, D. S. Campbell, A. Schmidt, E. W. Deutsch, H. Rost, Z. Sun, O. Rinner, L. Reiter, Q. Shen, J. J. Michaelson, A. Frei, S. Alberti, U. Kusebauch, B. Wollscheid, R. L. Moritz, A. Beyer, and R. Aebersold. A complete mass-spectrometric map of the yeast proteome applied to quantitative trait analysis. Nature 494:266-270, 2013.
65. Pratt, J. M., J. Petty, I. Riba-Garcia, D. H. Robertson, S. J. Gaskell, S. G. Oliver, and R. J. Beynon. Dynamics of protein turnover, a missing dimension in proteomics. Mol. Cell. Proteomics 1:579-591, 2002.
66. Prescher, J., and C. Bertozzi. Chemistry in living systems. Nat. Chem. Biol. 1:13-21, 2005.
67. Rabani, M., J. Z. Levin, L. Fan, X. Adiconis, R. Raychowdhury, M. Garber, A. Gnirke, C. Nusbaum, N. Hacohen, N. Friedman, I. Amit, and A. Regev. Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat. Biotechnol. 29:436-442, 2011.
68. Ramskold, D., S. Luo, Y. C. Wang, R. Li, Q. Deng, O. R. Faridani, G. A. Daniels, I. Khrebtukova, J. F. Loring, L. C. Laurent, G. P. Schroth, and R. Sandberg. Full-length mRNA-Seq from single-cell levels of RNA and individual circulating tumor cells. Nat. Biotechnol. 30:777-782, 2012.
69. Rappsilber, J., and M. Mann. What doesitmeantoidentify a protein in proteomics? Trends Biochem. Sci. 27:74-78, 2002.
70. Rechavi, O., M. Kalman, Y. Fang, H. Vernitsky, J. Jacob-Hirsch, L. J. Foster, Y. Kloog, and I. Goldstein. Trans-SILAC: sorting out the non-cell-autonomous proteome. Nat. Methods 7:923-927, 2010.
71. Rhee, H.-W., P. Zou, N. D. Udeshi, J. D. Martell, V. K. Mootha, S. A. Carr, and A. Y. Ting. Proteomic mapping of mitochondria in living cells via spatially restricted enzymatic tagging. Science 339:1328-1331, 2013.
72. Rostovtsev, V., L. Green, V. Fokin, and K. Sharpless. A stepwise Huisgen cycloaddition process: copper (I)-catalyzed regioselective ligation of azides and terminal alkynes. Angew. Chem. Int. Ed. 41:2596-2599, 2002.
73. Sadygov, R. G., D. Cociorva, and J. R. Yates, III. Largescale database searching using tandem mass spectra: looking up the answer in the back of the book. Nat. Methods 1:195-202, 2004.
74. Saxon, E., and C. Bertozzi. Cell surface engineering by a modified Staudinger reaction. Science 287:2007-2010, 2000.
75. Schwanhausser, B., M. Gossen, G. Dittmar, and M. Selbach. Global analysis of cellular protein translation by pulsed SILAC. Proteomics 9:205-209, 2009.
76. Schwanhausser, B., D. Busse, N. Li, G. Dittmar, J. Schuchhardt, J. Wolf, W. Chen, and M. Selbach. Global quantification of mammalian gene expression control. Nature 473:337-342, 2011.
77. Selbach, M., B. Schwanhausser, N. Thierfelder, Z. Fang, R. Khanin, and N. Rajewsky. Widespread changes in protein synthesis induced by microRNAs. Nature 455:58-63, 2008.
78. Steen, H., and M. Mann. The abc's (and xyz's) of peptide sequencing. Nat. Rev. Mol. Cell Biol. 5:699-711, 2004.
79. Steiner, F. A., P. B. Talbert, S. Kasinathan, R. B. Deal, and S. Henikoff. Cell-type-specific nuclei purification from whole animals for genome-wide expression and chromatin profiling. Genome Res. 22:766-777, 2012.
80. Sury, M. D., J. X. Chen, and M. Selbach. The SILAC fly allows for accurate protein quantification in vivo. Mol. Cell. Proteomics 9:2173-2183, 2010.
81. Szychowski, J., A. Mahdavi, J. J. L. Hodas, J. D. Bagert, J. T. Ngo, P. Landgraf, D. C. Dieterich, E. M. Schuman, and D. A. Tirrell. Cleavable biotin probes for labeling of biomolecules via azide-alkyne cycloaddition. J. Am. Chem. Soc. 132:18351-18360, 2010.
82. Taniguchi, Y., P. J. Choi, G. W. Li, H. Chen, M. Babu, J. Hearn, A. Emili, and X. S. Xie. Quantifying E. coli proteome and transcriptome with single-molecule sensitivity in single cells. Science 329:533-538, 2010.
83. Tanrikulu, I. C., E. Schmitt, Y. Mechulam, W. A. Goddard, III, and D. A. Tirrell. Discovery of Escherichia coli methionyl-tRNA synthetase mutants for efficient labeling of proteins with azidonorleucine in vivo. Proc. Natl. Acad. Sci. USA 106:15285-15290, 2009.
84. Tcherkezian, J., P. A. Brittis, F. Thomas, P. P. Roux, and J. G. Flanagan. Transmembrane receptor DCC associates with protein synthesis machinery and regulates translation. Cell 141:632-644, 2010.
85. Thingholm, T. E., O. N. Jensen, and M. R. Larsen. Analytical strategies for phosphoproteomics. Proteomics 9:1451-1468, 2009.
86. Tomlinson, E., N. Palaniyappan, D. Tooth, and R. Layfield. Methods for the purification of ubiquitinated proteins. Proteomics 7:1016-1022, 2007.
87. Tornoe, C. W., C. Christensen, and M. Meldal. Peptidotriazoles on solid phase: [1, 2, 3]-triazoles by regiospecific copper (I)-catalyzed 1, 3-dipolar cycloadditions of terminal alkynes to azides. J. Org. Chem. 67:3057-3064, 2002.
88. Truong, F., T. H. Yoo, T. J. Lampo, and D. A. Tirrell. Two-strain, cell-selective protein labeling in mixed bacterial cultures. J. Am. Chem. Soc. 134:8551-8556, 2012.
89. Vogel, C., and E. M. Marcotte. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13:227-232, 2012.
90. Vogel, C., S. Abreu Rde, D. Ko, S. Y. Le, B. A. Shaprio, S. C. Burns, D. Sandhu, D. R. Boutz, E. M. Marcotte, and L. O. Penalva. Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line. Mol. Syst. Biol. 6:400, 2010.
91. Wang, Z., M. Gerstein, and M. Snyder. RNA-Seq: a revolutionary tool for transcriptomics. Nat. Rev. Genet. 10:57-63, 2009.
92. Wiese, S., K. A. Reidegeld, H. E. Meyer, and B. Warscheid. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics 7:340-350, 2006.
93. Yates, J. R., C. I. Ruse, and A. Nakorchevsky. Proteomics by mass spectrometry: approaches, advances, and applications. Annu. Rev. Biomed. Eng. 11:49-79, 2009.
94. Yoon, B. C., H. Jung, A. Dwivedy, C. M. O'Hare, K. Zivraj, and C. E. Holt. Local translation of extranuclear lamin B promotes axon maintenance. Cell 148:752-764, 2012.
95. Zhang, L., H. Zhao, B. S. Blagg, and R. T. Dobrowsky. C-terminal heat shock protein 90 inhibitor decreases hyperglycemia-induced oxidative stress and improves mitochondrial bioenergetics in sensory neurons. J. Proteome Res. 11:2581-2593, 2012.
96. Zhang, M. M., L. K. Tsou, G. Charron, A. S. Raghavan, and H. C. Hang. Tandem fluorescence imaging of dynamic S-acylation and protein turnover. Proc. Natl. Acad. Sci. USA 107:8627-8632, 2010.