Epigenetic modifications of the neuroproteome

Proteomics

Volumn 12, Issue 15-16, 2012, Pages 2404-2420

  Brunner, Andrea M ^a   Tweedie Cullen, Ry Y ^b   Mansuy, Isabelle M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

Animal proteomics; Epigenetics; Histones; Neuroscience; Post translational modifications

Indexed keywords

BRAIN PROTEIN; DNA; HISTONE; NEUROPROTEOME; PROTEIN VARIANT; PROTEOME; STABLE ISOTOPE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CHEMICAL LABELING; DERIVATIZATION; DNA MODIFICATION; EPIGENETICS; GENE EXPRESSION REGULATION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HISTONE ACETYLATION; HISTONE CODE; HISTONE METHYLATION; HISTONE PHOSPHORYLATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; ISOTOPE LABELING; LEARNING; MASS SPECTROMETRY; MEMORY; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN DETERMINATION; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; PROTEIN PURIFICATION; PROTEOMICS; QUANTITATIVE ANALYSIS; REVIEW; VALIDATION STUDY;

AMINO ACID SEQUENCE; ANIMALS; EPIGENESIS, GENETIC; HISTONES; HUMANS; MOLECULAR SEQUENCE DATA; NERVOUS SYSTEM; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEOME;

EID: 84861689295     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100672     Document Type: Review

References (121)

1. Klose, R. J., Bird, A. P., Genomic DNA methylation: the mark and its mediators. Trends Biochem Sci. 2006, 31, 89-97.
2. Bannister, A. J., Kouzarides, T., Regulation of chromatin by histone modifications. Cell Res. 2011, 21, 381-395.
3. Ho, L., Crabtree, G. R., Chromatin remodelling during development. Nature 2010, 463, 474-484.
4. Graff, J., Mansuy, I. M., Epigenetic codes in cognition and behaviour. Behav. Brain Res. 2008, 192, 70-87.
5. Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. et al., Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389, 251-260.
6. Campos, E. I., Reinberg, D., Histones: annotating chromatin. Annu. Rev. Genet. 2009, 43, 559-599.
7. Tweedie-Cullen, R. Y., Park, C. S., Mansuy, I. M., in: Vidal, C. J. (Ed.), Posttranslational Modifications in Health and Diseases, Springer Verlag, Murcia, Spain 2009, pp. 233-257.
8. Tweedie-Cullen, R. Y., Reck, J. M., Mansuy, I. M., Comprehensive mapping of post-translational modifications on synaptic, nuclear, and histone proteins in the adult mouse brain. J. Proteome Res. 2009, 8, 4966-4982.
9. Brownell, J. E., Allis, C. D., Special HATs for special occasions: linking histone acetylation to chromatin assembly and gene activation. Curr. Opin. Genet. Dev. 1996, 6, 176-184.
10. Shogren-Knaak, M., Ishii, H., Sun, J. M., Pazin, M. J. et al., Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311, 844-847.
11. Latham, J. A., Dent, S. Y., Cross-regulation of histone modifications. Nat. Struct. Mol. Biol. 2007, 14, 1017-1024.
12. Feng, Y., Wang, J., Asher, S., Hoang, L. et al., Histone H4 acetylation differentially modulates arginine methylation by an in Cis mechanism. J. Biol. Chem. 2011, 286, 20323-20334.
13. Kim, J., Guermah, M., McGinty, R. K., Lee, J. S. et al., RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 2009, 137, 459-471.
14. Zhou, J., Fan, J. Y., Rangasamy, D., Tremethick, D. J., The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat. Struct. Mol. Biol. 2007, 14, 1070-1076.
15. Dodd, I. B., Micheelsen, M. A., Sneppen, K., Thon, G., Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 2007, 129, 813-822.
16. Levenson, J. M., Sweatt, J. D., Epigenetic mechanisms in memory formation. Nat. Rev. Neurosci. 2005, 6, 108-118.
17. Day, J. J., Sweatt, J. D., Epigenetic mechanisms in cognition. Neuron 2011, 70, 813-829.
18. Attia, M., Rachez, C., De Pauw, A., Avner, P. et al., Nap1l2 promotes histone acetylation activity during neuronal differentiation. Mol. Cell. Biol. 2007, 27, 6093-6102.
19. Chen, Y. L., Law, P. Y., Loh, H. H., NGF/PI3K signaling-mediated epigenetic regulation of delta opioid receptor gene expression. Biochem. Biophys. Res. Commun. 2008, 368, 755-760.
20. Park, S. W., He, Y., Ha, S. G., Loh, H. H. et al., Epigenetic regulation of kappa opioid receptor gene in neuronal differentiation. Neuroscience 2008, 151, 1034-1041.
21. Siebzehnrubl, F. A., Buslei, R., Eyupoglu, I. Y., Seufert, S. et al., Histone deacetylase inhibitors increase neuronal differentiation in adult forebrain precursor cells. Exp. Brain Res. 2007, 176, 672-678.
22. Guan, Z., Giustetto, M., Lomvardas, S., Kim, J. H. et al., Integration of long-term-memory-related synaptic plasticity involves bidirectional regulation of gene expression and chromatin structure. Cell 2002, 111, 483-493.
23. Guan, J. S., Haggarty, S. J., Giacometti, E., Dannenberg, J. H. et al., HDAC2 negatively regulates memory formation and synaptic plasticity. Nature 2009, 459, 55-60.
24. Vecsey, C. G., Hawk, J. D., Lattal, K. M., Stein, J. M. et al., Histone deacetylase inhibitors enhance memory and synaptic plasticity via CREB:CBP-dependent transcriptional activation. J. Neurosci. 2007, 27, 6128-6140.
25. Graff, J., Rei, D., Guan, J.-S., Wang, W.-Y. et al., An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 2012, 483, 222-226.
26. Dash, P. K., Orsi, S. A., Moore, A. N., Histone deactylase inhibition combined with behavioral therapy enhances learning and memory following traumatic brain injury. Neuroscience 2009, 163, 1-8.
27. Fischer, A., Sananbenesi, F., Wang, X., Dobbin, M. et al., Recovery of learning and memory is associated with chromatin remodelling. Nature 2007, 447, 178-182.
28. Wood, M. A., Kaplan, M. P., Park, A., Blanchard, E. J. et al., Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn. Mem. 2005, 12, 111-119.
29. Zhao, Z., Fan, L., Frick, K. M., Epigenetic alterations regulate estradiol-induced enhancement of memory consolidation. Proc. Natl. Acad. Sci. USA 2010, 107, 5605-5610.
30. Fernandez, S. M., Lewis, M. C., Pechenino, A. S., Harburger, L. L. et al., Estradiol-induced enhancement of object memory consolidation involves hippocampal extracellular signal-regulated kinase activation and membrane-bound estrogen receptors. J. Neurosci. 2008, 28, 8660-8667.
31. Levenson, J. M., O'Riordan, K. J., Brown, K. D., Trinh, M. A. et al., Regulation of histone acetylation during memory formation in the hippocampus. J. Biol. Chem. 2004, 279, 40545-40559.
32. Korzus, E., Rosenfeld, M. G., Mayford, M., CBP histone acetyltransferase activity is a critical component of memory consolidation. Neuron 2004, 42, 961-972.
33. Alarcon, J. M., Malleret, G., Touzani, K., Vronskaya, S. et al., Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron 2004, 42, 947-959.
34. Oliveira, A. M., Wood, M. A., McDonough, C. B., Abel, T., Transgenic mice expressing an inhibitory truncated form of p300 exhibit long-term memory deficits. Learn. Mem. 2007, 14, 564-572.
35. Bredy, T. W., Wu, H., Crego, C., Zellhoefer, J. et al., Histone modifications around individual BDNF gene promoters in prefrontal cortex are associated with extinction of conditioned fear. Learn. Mem. 2007, 14, 268-276.
36. Chwang, W. B., O'Riordan, K. J., Levenson, J. M., Sweatt, J. D., ERK/MAPK regulates hippocampal histone phosphorylation following contextual fear conditioning. Learn. Mem. 2006, 13, 322-328.
37. Chwang, W. B., Arthur, J. S., Schumacher, A., Sweatt, J. D., The nuclear kinase mitogen- and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J. Neurosci. 2007, 27, 12732-12742.
38. Lubin, F. D., Sweatt, J. D., The IkappaB kinase regulates chromatin structure during reconsolidation of conditioned fear memories. Neuron 2007, 55, 942-957.
39. Koshibu, K., Graff, J., Mansuy, I. M., Nuclear protein phosphatase-1: an epigenetic regulator of fear memory and amygdala long-term potentiation. Neuroscience 2011, 173, 30-36.
40. Koshibu, K., Graff, J., Beullens, M., Heitz, F. D. et al., Protein phosphatase 1 regulates the histone code for long-term memory. J. Neurosci. 2009, 29, 13079-13089.
41. Gupta, S., Kim, S. Y., Artis, S., Molfese, D. L. et al., Histone methylation regulates memory formation. J. Neurosci. 2010, 30, 3589-3599.
42. Graff, J., Koshibu, K., Jouvenceau, A., Dutar, P. et al., Protein phosphatase 1-dependent transcriptional programs for long-term memory and plasticity. Learn. Mem. 2010, 17, 355-363.
43. Putignano, E., Lonetti, G., Cancedda, L., Ratto, G. et al., Developmental downregulation of histone posttranslational modifications regulates visual cortical plasticity. Neuron 2007, 53, 747-759.
44. Graff, J., Mansuy, I. M., Epigenetic dysregulation in cognitive disorders. Eur. J. Neurosci. 2009, 30, 1-8.
45. Egelhofer, T. A., Minoda, A., Klugman, S., Lee, K. et al., An assessment of histone-modification antibody quality. Nat. Struct. Mol. Biol. 2011, 18, 91-93.
46. Fuchs, S. M., Krajewski, K., Baker, R. W., Miller, V. L., Influence of combinatorial histone modifications on antibody and effector protein recognition. Curr. Biol. 2011, 21, 53-58.
47. Tweedie-Cullen, R. Y., Mansuy, I. M., Towards a better understanding of nuclear processes based on proteomics. Amino Acids 2010, 39, 1117-1130.
48. Steen, H., Mann, M., The ABC's (and XYZ's) of peptide sequencing. Nat. Rev. Mol. Cell Biol 2004, 5, 699-711.
49. Perkins, D. N., Pappin, D. J., Creasy, D. M., Cottrell, J. S., Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 1999, 20, 3551-3567.
50. Eng, J. K., McCormack, A. L., Yates Iii, J. R., An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J. Am. Soc. Mass Spectrom. 1994, 5, 976-989.
51. Cox, J., Neuhauser, N., Michalski, A., Scheltema, R. A. et al., Andromeda: a peptide search engine integrated into the MaxQuant environment. J. Proteome Res. 2011, 10, 1794-1805.
52. Gstaiger, M., Aebersold, R., Applying mass spectrometry-based proteomics to genetics, genomics and network biology. Nat. Rev. Genet. 2009, 10, 617-627.
53. Evertts, A. G., Zee, B. M., Garcia, B. A., Modern approaches for investigating epigenetic signaling pathways. J. Appl. Physiol. 2010, 109, 927-933.
54. Udeshi, N. D., Compton, P. D., Shabanowitz, J., Hunt, D. F. et al., Methods for analyzing peptides and proteins on a chromatographic timescale by electron-transfer dissociation mass spectrometry. Nat. Protoc. 2008, 3, 1709-1717.
55. Bellet, M. M., Sassone-Corsi, P., Mammalian circadian clock and metabolism - the epigenetic link. J. Cell Sci. 2010, 123, 3837-3848.
56. Spellman, D. S., Deinhardt, K., Darie, C. C., Chao, M. V. et al., Stable isotopic labeling by amino acids in cultured primary neurons: application to brain-derived neurotrophic factor-dependent phosphotyrosine-associated signaling. Mol. Cell Proteomics 2008, 7, 1067-1076.
57. Tweedie-Cullen, R. Y., Wollscheid, B., Livingstone-Zatchej, M., Mansuy, I. M., Neuroproteomics and the detection of regulatory phosphosites. Cur. Proteomics 2007, 4, 209-222.
58. Shechter, D., Dormann, H. L., Allis, C. D., Hake, S. B., Extraction, purification and analysis of histones. Nat. Protoc. 2007, 2, 1445-1457.
59. Greyling, H. J., Schwager, S., Sewell, B. T., von Holt, C., The identity of conformational states of reconstituted and native histone octamers. Eur. J. Biochem. 1983, 137, 221-226.
60. McKittrick, E., Gafken, P. R., Ahmad, K., Henikoff, S., Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 2004, 101, 1525-1530.
61. Boersema, P. J., Mohammed, S., Heck, A. J., Hydrophilic interaction liquid chromatography (HILIC) in proteomics. Anal. Bioanal. Chem. 2008, 391, 151-159.
62. Lindner, H., Sarg, B., Meraner, C., Helliger, W., Separation of acetylated core histones by hydrophilic-interaction liquid chromatography. J. Chromatogr. A 1996, 743, 137-144.
63. Lindner, H., Sarg, B., Helliger, W., Application of hydrophilic-interaction liquid chromatography to the separation of phosphorylated H1 histones. J. Chromatogr. A 1997, 782, 55-62.
64. Darwanto, A., Curtis, M. P., Schrag, M., Kirsch, W. et al., A modified "cross-talk" between histone H2B Lys-120 ubiquitination and H3 Lys-79 methylation. J. Biol. Chem. 2010, 285, 21868-21876.
65. Jung, S. Y., Li, Y., Wang, Y., Chen, Y. et al., Complications in the assignment of 14 and 28 Da mass shift detected by mass spectrometry as in vivo methylation from endogenous proteins. Anal. Chem. 2008, 80, 1721-1729.
66. Jung, H. R., Pasini, D., Helin, K., Jensen, O. N., Quantitative mass spectrometry of histones H3.2 and H3.3 in Suz12-deficient mouse embryonic stem cells reveals distinct, dynamic post-translational modifications at Lys-27 and Lys-36. Mol. Cell. Proteomics 2010, 9, 838-850.
67. Garcia, B. A., Mollah, S., Ueberheide, B. M., Busby, S. A., et al., Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nat. Protoc. 2007, 2, 933-938.
68. Phanstiel, D., Brumbaugh, J., Berggren, W. T., Conard, K., et al., Mass spectrometry identifies and quantifies 74 unique histone H4 isoforms in differentiating human embryonic stem cells. Proc. Natl. Acad. Sci. USA 2008, 105, 4093-4098.
69. Taverna, S. D., Ueberheide, B. M., Liu, Y., Tackett, A. J. et al., Long-distance combinatorial linkage between methylation and acetylation on histone H3 N termini. Proc. Natl. Acad. Sci. USA 2007, 104, 2086-2091.
70. Young, N. L., DiMaggio, P. A., Plazas-Mayorca, M. D., Baliban, R. C. et al., High throughput characterization of combinatorial histone codes. Mol. Cell. Proteomics 2009, 8, 2266-2284.
71. Sarg, B., Helliger, W., Talasz, H., Koutzamani, E. et al., Histone H4 hyperacetylation precludes histone H4 lysine 20 trimethylation. J. Biol. Chem. 2004, 279, 53458-53464.
72. Liu, B., Lin, Y., Darwanto, A., Song, X. et al., Identification and characterization of propionylation at histone H3 lysine 23 in mammalian cells. J. Biol. Chem. 2009, 284, 32288-32295.
73. Ahmed, M. M., Gardiner, K. J., Preserving protein profiles in tissue samples: differing outcomes with and without heat stabilization. J. Neurosci. Methods 2011, 196, 99-106.
74. O'Callaghan, J. P., Sriram, K., Focused microwave irradiation of the brain preserves in vivo protein phosphorylation: comparison with other methods of sacrifice and analysis of multiple phosphoproteins. J. Neurosci. Methods 2004, 135, 159-168.
75. Skold, K., Svensson, M., Norrman, M., Sjogren, B. et al., The significance of biochemical and molecular sample integrity in brain proteomics and peptidomics: stathmin 2-20 and peptides as sample quality indicators. Proteomics 2007, 7, 4445-4456.
76. Nielsen, K. J., Callaway, E. M., More than a feeling: sensation from cortical stimulation. Nat. Neurosci. 2008, 11, 10-11.
77. Wisniewski, J. R., Zougman, A., Mann, M., Nepsilon-formylation of lysine is a widespread post-translational modification of nuclear proteins occurring at residues involved in regulation of chromatin function. Nucleic Acids Res. 2008, 36, 570-577.
78. Zhao, Y., Jensen, O. N., Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques. Proteomics 2009, 9, 4632-4641.
79. Andersson, L., Porath, J., Isolation of phosphoproteins by immobilized metal (Fe3+) affinity chromatography. Anal. Biochem. 1986, 154, 250-254.
80. Munton, R. P., Tweedie-Cullen, R., Livingstone-Zatchej, M., Weinandy, F. et al., Qualitative and quantitative analyses of protein phosphorylation in naive and stimulated mouse synaptosomal preparations. Mol. Cell. Proteomics 2007, 6, 283-293.
81. Larsen, M. R., Thingholm, T. E., Jensen, O. N., Roepstorff, P. et al., Highly selective enrichment of phosphorylated peptides from peptide mixtures using titanium dioxide microcolumns. Mol. Cell. Proteomics 2005, 4, 873-886.
82. Thingholm, T. E., Jensen, O. N., Robinson, P. J., Larsen, M. R., SIMAC (sequential elution from IMAC), a phosphoproteomics strategy for the rapid separation of monophosphorylated from multiply phosphorylated peptides. Mol. Cell. Proteomics 2008, 7, 661-671.
83. Kim, S. C., Sprung, R., Chen, Y., Xu, Y. et al., Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 2006, 23, 607-618.
84. Gronborg, M., Kristiansen, T. Z., Stensballe, A., Andersen, J. S. et al., A mass spectrometry-based proteomic approach for identification of serine/threonine-phosphorylated proteins by enrichment with phospho-specific antibodies: identification of a novel protein, Frigg, as a protein kinase A substrate. Mol. Cell. Proteomics 2002, 1, 517-527.
85. Rush, J., Moritz, A., Lee, K. A., Guo, A. et al., Immunoaffinity profiling of tyrosine phosphorylation in cancer cells. Nat. Biotechnol. 2005, 23, 94-101.
86. Beausoleil, S. A., Jedrychowski, M., Schwartz, D., Elias, J. E. et al., Large-scale characterization of HeLa cell nuclear phosphoproteins. Proc. Natl. Acad. Sci. USA 2004, 101, 12130-12135.
87. McNulty, D. E., Annan, R. S., Hydrophilic interaction chromatography reduces the complexity of the phosphoproteome and improves global phosphopeptide isolation and detection. Mol. Cell. Proteomics 2008, 7, 971-980.
88. Dunn, J. D., Reid, G. E., Bruening, M. L., Techniques for phosphopeptide enrichment prior to analysis by mass spectrometry. Mass Spectrom. Rev. 2010, 29, 29-54.
89. Steen, H., Jebanathirajah, J. A., Rush, J., Morrice, N. et al., Phosphorylation analysis by mass spectrometry: myths, facts, and the consequences for qualitative and quantitative measurements. Mol. Cell. Proteomics 2006, 5, 172-181.
90. Mikesh, L. M., Ueberheide, B., Chi, A., Coon, J. J. et al., The utility of ETD mass spectrometry in proteomic analysis. Biochim. Biophys. Acta 2006, 1764, 1811-1822.
91. Tholey, A., Reed, J., Lehmann, W. D., Electrospray tandem mass spectrometric studies of phosphopeptides and phosphopeptide analogues. J. Mass Spectrom. 1999, 34, 117-123.
92. Frese, C. K., Altelaar, A. F., Hennrich, M. L., Nolting, D. et al., Improved peptide identification by targeted fragmentation using CID, HCD and ETD on an LTQ-Orbitrap Velos. J. Proteome Res. 2011, 10, 2377-2388.
93. Frank, A., Pevzner, P., PepNovo: de novo peptide sequencing via probabilistic network modeling. Anal. Chem. 2005, 77, 964-973.
94. Olsen, J. V., Blagoev, B., Gnad, F., Macek, B. et al., Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 2006, 127, 635-648.
95. Beausoleil, S. A., Villen, J., Gerber, S. A., Rush, J. et al., A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat. Biotechnol. 2006, 24, 1285-1292.
96. Trelle, M. B., Jensen, O. N., Utility of immonium ions for assignment of epsilon-N-acetyllysine-containing peptides by tandem mass spectrometry. Anal. Chem. 2008, 80, 3422-3430.
97. Garcia, B. A., Siuti, N., Thomas, C. E., Mizzen, C. A. et al., Characterization of neurohistone variants and post-translational modifications by electron capture dissociation mass spectrometry. Int. J. Mass Spectrom. 2007, 259, 184-196.
98. Han, J., Borchers, C. H., Top-down analysis of recombinant histone H3 and its methylated analogs by ESI/FT-ICR mass spectrometry. Proteomics 2010, 10, 3621-3630.
99. 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.
100. Tsur, D., Tanner, S., Zandi, E., Bafna, V. et al., Identification of post-translational modifications by blind search of mass spectra. Nat. Biotechnol. 2005, 23, 1562-1567.
101. Arnaudo, A. M., Molden, R. C., Garcia, B. A., Revealing histone variant induced changes via quantitative proteomics. Crit. Rev. Biochem. Mol. Biol. 2011, 46, 284-294.
102. Picotti, P., Bodenmiller, B., Mueller, L. N., Domon, B. et al., Full dynamic range proteome analysis of S. cerevisiae by targeted proteomics. Cell 2009, 138, 795-806.
103. Liu, H., Sadygov, R. G., Yates, J. R., 3rd, A model for random sampling and estimation of relative protein abundance in shotgun proteomics. Anal. Chem. 2004, 76, 4193-4201.
104. Lee, A. Y., Paweletz, C. P., Pollock, R. M., Settlage, R. E. et al., Quantitative analysis of histone deacetylase-1 selective histone modifications by differential mass spectrometry. J. Proteome Res. 2008, 7, 5177-5186.
105. Beck, H. C., Nielsen, E. C., Matthiesen, R., Jensen, L. H. et al., Quantitative proteomic analysis of post-translational modifications of human histones. Mol. Cell. Proteomics 2006, 5, 1314-1325.
106. Drogaris, P., Wurtele, H., Masumoto, H., Verreault, A. et al., Comprehensive profiling of histone modifications using a label-free approach and its applications in determining structure-function relationships. Anal. Chem. 2008, 80, 6698-6707.
107. Schmidt, A., Claassen, M., Aebersold, R., Directed mass spectrometry: towards hypothesis-driven proteomics. Curr. Opin. Chem. Biol. 2009, 13, 510-517.
108. Gygi, S. P., Rist, B., Gerber, S. A., Turecek, F. et al., Quantitative analysis of complex protein mixtures using isotope-coded affinity tags. Nat. Biotechnol. 1999, 17, 994-999.
109. Pierce, A., Unwin, R. D., Evans, C. A., Griffiths, S. et al., Eight-channel iTRAQ enables comparison of the activity of six leukemogenic tyrosine kinases. Mol. Cell. Proteomics 2008, 7, 853-863.
110. Thompson, A., Schafer, J., Kuhn, K., Kienle, S. et al., Tandem mass tags: a novel quantification strategy for comparative analysis of complex protein mixtures by MS/MS. Anal. Chem. 2003, 75, 1895-1904.
111. Plazas-Mayorca, M. D., Bloom, J. S., Zeissler, U., Leroy, G. et al., Quantitative proteomics reveals direct and indirect alterations in the histone code following methyltransferase knockdown. Mol. Biosyst. 2010, 6, 1719-1729.
112. Ong, S. E., Mann, M., A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC). Nat. Protoc. 2006, 1, 2650-2660.
113. McClatchy, D. B., Liao, L., Park, S. K., Venable, J. D. et al., Quantification of the synaptosomal proteome of the rat cerebellum during post-natal development. Genome Res. 2007, 17, 1378-1388.
114. Monetti, M., Nagaraj, N., Sharma, K., Mann, M., Large-scale phosphosite quantification in tissues by a spike-in SILAC method. Nat. Methods 2011, 8, 655-658.
115. Ishihama, Y., Sato, T., Tabata, T., Miyamoto, N. et al., Quantitative mouse brain proteomics using culture-derived isotope tags as internal standards. Nat. Biotechnol. 2005, 23, 617-621.
116. Kettenbach, A. N., Rush, J., Gerber, S. A., Absolute quantification of protein and post-translational modification abundance with stable isotope-labeled synthetic peptides. Nat. Protoc. 2011, 6, 175-186.
117. Singh, S., Springer, M., Steen, J., Kirschner, M. W. et al., FLEXIQuant: a novel tool for the absolute quantification of proteins, and the simultaneous identification and quantification of potentially modified peptides. J. Proteome Res. 2009, 8, 2201-2210.
118. Picotti, P., Rinner, O., Stallmach, R., Dautel, F. et al., High-throughput generation of selected reaction-monitoring assays for proteins and proteomes. Nat. Methods 2010, 7, 43-46.
119. Fraga, M. F., Ballestar, E., Villar-Garea, A., Boix-Chornet, M. et al., Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet. 2005, 37, 391-400.
120. Bonenfant, D., Towbin, H., Coulot, M., Schindler, P. et al., Analysis of dynamic changes in post-translational modifications of human histones during cell cycle by mass spectrometry. Mol. Cell. Proteomics 2007, 6, 1917-1932.
121. Zee, B. M., Levin, R. S., Xu, B., LeRoy, G. et al., In vivo residue-specific histone methylation dynamics. J. Biol. Chem. 2010, 285, 3341-3350.