Middle-down proteomics: a still unexploited resource for chromatin biology

References

• Xu D, Bai J, Duan Q, et al. Covalent modifications of histones during mitosis and meiosis. Cell Cycle. 2009;8(22):3688–3694.
   PubMed Web of Science ®Google Scholar
• Weber CM, Henikoff S. Histone variants: dynamic punctuation in transcription. Genes Dev. 2014;28(7):672–682.
   PubMed Web of Science ®Google Scholar
• Kumar R, Horikoshi N, Singh M, et al. Chromatin modifications and the DNA damage response to ionizing radiation. Front Oncol. 2012;2:214.
   PubMedGoogle Scholar
• Greer EL, Shi Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nat Rev Genet. 2012;13(5):343–357.
   PubMed Web of Science ®Google Scholar
• Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol. 2010;28(10):1057–1068.
   PubMed Web of Science ®Google Scholar
• Chi P, Allis CD, Wang GG. Covalent histone modifications–miswritten, misinterpreted and mis-erased in human cancers. Nat Rev Cancer. 2010;10(7):457–469.
   PubMed Web of Science ®Google Scholar
• Jenuwein T, Allis CD. Translating the histone code. Science. 2001;293(5532):1074–1080.
   PubMed Web of Science ®Google Scholar
• Taverna SD, Li H, Ruthenburg AJ, et al. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nat Struct Mol Biol. 2007;14(11):1025–1040.
   PubMed Web of Science ®Google Scholar
• Yun MY, Wu J, Workman JL, et al. Readers of histone modifications. Cell Res. 2011;21(4):564–578.
   PubMed Web of Science ®Google Scholar
• Kouzarides T. Chromatin modifications and their function. Cell. 2007;128(4):693–705.
   PubMed Web of Science ®Google Scholar
• Fernandez-Capetillo O, Mahadevaiah SK, Celeste A, et al. H2AX is required for chromatin remodeling and inactivation of sex chromosomes in male mouse meiosis. Developmental Cell. 2003;4(4):497–508.
   PubMed Web of Science ®Google Scholar
• Sabari BR, Zhang D, Allis CD, et al. Metabolic regulation of gene expression through histone acylations. Nat Rev Mol Cell Biol. 2017;18(2):90–101.
   PubMed Web of Science ®Google Scholar
• Fischle W, Wang Y, Allis CD. Histone and chromatin cross-talk. Curr Opin Cell Biol. 2003;15(2):172–183.
   PubMed Web of Science ®Google Scholar
• Lee JS, Smith E, Shilatifard A. The language of histone crosstalk. Cell. 2010;142(5):682–685.
   PubMed Web of Science ®Google Scholar
• Creyghton MP, Cheng AW, Welstead GG, et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A. 2010;107(50):21931–21936.
   PubMed Web of Science ®Google Scholar
• Hirota T, Lipp JJ, Toh BH, et al. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature. 2005;438(7071):1176–1180.
   PubMed Web of Science ®Google Scholar
• Xhemalce B, Kouzarides T. A chromodomain switch mediated by histone H3 Lys 4 acetylation regulates heterochromatin assembly. Genes Dev. 2010;24(7):647–652.
   PubMed Web of Science ®Google Scholar
• Vermeulen M, Eberl HC, Matarese F, et al. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell. 2010;142(6):967–980.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Garcia BA. Comprehensive catalog of currently documented histone modifications. Cold Spring Harb Perspect Biol. 2015;7(9):a025064.
   PubMed Web of Science ®Google Scholar
• Yuan W, Xu M, Huang C, et al. H3K36 methylation antagonizes PRC2-mediated H3K27 methylation. J Biol Chem. 2011;286(10):7983–7989.
   PubMed Web of Science ®Google Scholar
• Chandra T, Kirschner K, Thuret JY, et al. Independence of repressive histone marks and chromatin compaction during senescent heterochromatic layer formation. Mol Cell. 2012;47(2):203–214.
   PubMed Web of Science ®Google Scholar
• Shema E, Jones D, Shoresh N, et al. Single-molecule decoding of combinatorially modified nucleosomes. Science. 2016;352(6286):717–721.
   PubMed Web of Science ®Google Scholar
• Egelhofer TA, Minoda A, Klugman S, et al. An assessment of histone-modification antibody quality. Nat Struct Mol Biol. 2011;18(1):91–93.
   PubMed Web of Science ®Google Scholar
• Walther TC, Mann M. Mass spectrometry-based proteomics in cell biology. J Cell Biol. 2010;190(4):491–500.
   PubMed Web of Science ®Google Scholar
• Sidoli S, Cheng L, Jensen ON. Proteomics in chromatin biology and epigenetics: elucidation of post-translational modifications of histone proteins by mass spectrometry. J Proteomics. 2012;75(12):3419–3433.
   PubMed Web of Science ®Google Scholar
• Sidoli S, Bhanu NV, Karch KR, et al. Complete workflow for analysis of histone post-translational modifications using bottom-up mass spectrometry: from histone extraction to data analysis. J Vis Exp. 2016;(111). doi: 10.3791/54112.
   PubMed Web of Science ®Google Scholar
• Bonaldi T, Imhof A, Regula JT. A combination of different mass spectroscopic techniques for the analysis of dynamic changes of histone modifications. Proteomics. 2004;4(5):1382–1396.
   PubMed Web of Science ®Google Scholar
• Garcia BA, Mollah S, Ueberheide BM, et al. Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nat Protoc. 2007;2(4):933–938.
   PubMed Web of Science ®Google Scholar
• Liao R, Wu H, Deng H, et al. Specific and efficient N-propionylation of histones with propionic acid N-hydroxysuccinimide ester for histone marks characterization by LC-MS. Anal Chem. 2013;85(4):2253–2259.
   PubMed Web of Science ®Google Scholar
• Maile TM, Izrael-Tomasevic A, Cheung T, et al. Mass spectrometric quantification of histone post-translational modifications by a hybrid chemical labeling method. Mol Cell Proteomics. 2015;14(4):1148–1158.
   PubMed Web of Science ®Google Scholar
• Kelleher NL. Top-down proteomics. Anal Chem. 2004;76(11):197A–203A.
   PubMed Web of Science ®Google Scholar
• Loo JA, Edmonds CG, Smith RD. Primary sequence information from intact proteins by electrospray ionization tandem mass spectrometry. Science. 1990;248(4952):201–204.
   PubMed Web of Science ®Google Scholar
• Zubarev RAK, McLafferty NL, Electron Capture FW. Dissociation of multiply charged protein cations. a nonergodic process. J Am Chem Soc. 1998;120:3265–3266.
   Web of Science ®Google Scholar
• Syka JE, 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(26):9528–9533.
   PubMed Web of Science ®Google Scholar
• Thomas CE, Kelleher NL, Mizzen CA. Mass spectrometric characterization of human histone H3: a bird’s eye view. J Proteome Res. 2006;5(2):240–247.
   PubMed Web of Science ®Google Scholar
• Boyne MT 2nd, Pesavento JJ, Mizzen CA, et al. Precise characterization of human histones in the H2A gene family by top down mass spectrometry. J Proteome Res. 2006;5(2):248–253.
   PubMed Web of Science ®Google Scholar
• Siuti N, Roth MJ, Mizzen CA, et al. Gene-specific characterization of human histone H2B by electron capture dissociation. J Proteome Res. 2006;5(2):233–239.
   PubMed Web of Science ®Google Scholar
• 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(13):4271–4280.
   PubMed Web of Science ®Google Scholar
• Banks GC, Deterding LJ, Tomer KB, et al. Hormone-mediated dephosphorylation of specific histone H1 isoforms. J Biol Chem. 2001;276(39):36467–36473.
   PubMed Web of Science ®Google Scholar
• Sarg B, Faserl K, Kremser L, et al. Comparing and combining capillary electrophoresis electrospray ionization mass spectrometry and nano-liquid chromatography electrospray ionization mass spectrometry for the characterization of post-translationally modified histones. Mol Cell Proteomics. 2013;12(9):2640–2656.
   PubMed Web of Science ®Google Scholar
• Onder O, Sidoli S, Carroll M, et al. Progress in epigenetic histone modification analysis by mass spectrometry for clinical investigations. Expert Rev Proteomics. 2015;12(5):499–517.
   PubMed Web of Science ®Google Scholar
• Taverna SD, Ueberheide BM, Liu Y, et al. Long-distance combinatorial linkage between methylation and acetylation on histone H3 N termini. Proc Natl Acad Sci U S A. 2007;104(7):2086–2091.
   PubMed Web of Science ®Google Scholar
• Mikesh LM, Ueberheide B, Chi A, et al. The utility of ETD mass spectrometry in proteomic analysis. Biochim Biophys Acta. 2006;1764(12):1811–1822.
   PubMed Web of Science ®Google Scholar
• Good DM, Wirtala M, McAlister GC, et al. Performance characteristics of electron transfer dissociation mass spectrometry. Mol Cell Proteomics. 2007;6(11):1942–1951.
   PubMed Web of Science ®Google Scholar
• Young NL, DiMaggio PA, Plazas-Mayorca MD, et al. High throughput characterization of combinatorial histone codes. Mol Cell Proteomics. 2009;8(10):2266–2284.
   PubMed Web of Science ®Google Scholar
• Tian Z, Tolic N, Zhao R, et al. Enhanced top-down characterization of histone post-translational modifications. Genome Biol. 2012;13(10):R86.
   PubMed Web of Science ®Google Scholar
• DiMaggio PA Jr., Young NL, Baliban RC, et al. A mixed integer linear optimization framework for the identification and quantification of targeted post-translational modifications of highly modified proteins using multiplexed electron transfer dissociation tandem mass spectrometry. Mol Cell Proteomics. 2009;8(11):2527–2543.
   PubMed Web of Science ®Google Scholar
• Sidoli S, Schwammle V, Ruminowicz C, et al. Middle-down hybrid chromatography/tandem mass spectrometry workflow for characterization of combinatorial post-translational modifications in histones. Proteomics. 2014;14(19):2200–2211.
   PubMed Web of Science ®Google Scholar
• LeDuc RD, Taylor GK, Kim YB, et al. ProSight PTM: an integrated environment for protein identification and characterization by top-down mass spectrometry. Nucleic Acids Res. 2004;32(Web Server issue):W340–345.
   PubMed Web of Science ®Google Scholar
• 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(Web Server issue):W701–706.
   PubMed Web of Science ®Google Scholar
• 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(4):846–856.
   PubMed Web of Science ®Google Scholar
• Frank AM, Pesavento JJ, Mizzen CA, et al. Interpreting top-down mass spectra using spectral alignment. Anal Chem. 2008;80(7):2499–2505.
   PubMed Web of Science ®Google Scholar
• Shechter D, Dormann HL, Allis CD, et al. Extraction, purification and analysis of histones. Nat Protoc. 2007;2(6):1445–1457.
   PubMed Web of Science ®Google Scholar
• Sidoli S, Garcia BA. Characterization of individual histone posttranslational modifications and their combinatorial patterns by mass spectrometry-based proteomics strategies. Methods Mol Biol. 2017;1528:121–148.
   PubMedGoogle Scholar
• Kalli A, Sweredoski MJ, Hess S. Data-dependent middle-down nano-liquid chromatography-electron capture dissociation-tandem mass spectrometry: an application for the analysis of unfractionated histones. Anal Chem. 2013;85(7):3501–3507.
   PubMed Web of Science ®Google Scholar
• Liao R, Zheng D, Nie A, et al. Sensitive and precise characterization of combinatorial histone modifications by selective derivatization coupled with RPLC-EThcD-MS/MS. J Proteome Res. 2017;16:780–787.
   PubMed Web of Science ®Google Scholar
• Sweredoski MJ, Moradian A, Raedle M, et al. High resolution parallel reaction monitoring with electron transfer dissociation for middle-down proteomics. Anal Chem. 2015;87(16):8360–8366.
   PubMed Web of Science ®Google Scholar
• 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(4):320–332.
   PubMed Web of Science ®Google Scholar
• 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(12):2772–2782.
   PubMed Web of Science ®Google Scholar
• Aggarwal S, Yadav AK. False discovery rate estimation in proteomics. Methods Mol Biol. 2016;1362:119–128.
   PubMedGoogle Scholar
• LeDuc RD, Fellers RT, Early BP, et al. The C-score: a Bayesian framework to sharply improve proteoform scoring in high-throughput top down proteomics. J Proteome Res. 2014;13(7):3231–3240.
   PubMed Web of Science ®Google Scholar
• Software for middle-down Proteomics [Internet]. Simone Sidoli; [cited 2017 June 19]. Available from: http://middle-down.github.io/Software/
   Google Scholar
• Jung HR, Sidoli S, Haldbo S, et al. Precision mapping of coexisting modifications in histone H3 tails from embryonic stem cells by ETD-MS/MS. Anal Chem. 2013;85(17):8232–8239.
   PubMed Web of Science ®Google Scholar
• Schwammle V, Aspalter CM, Sidoli S, et al. Large scale analysis of co-existing post-translational modifications in histone tails reveals global fine structure of cross-talk. Mol Cell Proteomics. 2014;13(7):1855–1865.
   PubMed Web of Science ®Google Scholar
• Shortreed MR, Frey BL, Scalf M, et al. Elucidating proteoform families from proteoform intact-mass and lysine-count measurements. J Proteome Res. 2016;15(4):1213–1221.
   PubMed Web of Science ®Google Scholar
• Guan X, Rastogi N, Parthun MR, et al. Discovery of histone modification crosstalk networks by stable isotope labeling of amino acids in cell culture mass spectrometry (SILAC MS). Mol Cell Proteomics. 2013;12(8):2048–2059.
   PubMed Web of Science ®Google Scholar
• Zhang K, Williams KE, Huang L, et al. Histone acetylation and deacetylation: identification of acetylation and methylation sites of HeLa histone H4 by mass spectrometry. Mol Cell Proteomics. 2002;1(7):500–508.
   PubMed Web of Science ®Google Scholar
• Gonzales-Cope M, Sidoli S, Bhanu NV, et al. Histone H4 acetylation and the epigenetic reader Brd4 are critical regulators of pluripotency in embryonic stem cells. BMC Genomics. 2016;17:95.
   PubMed Web of Science ®Google Scholar
• Schwammle V, Sidoli S, Ruminowicz C, et al. Systems level analysis of histone H3 Post-translational modifications (PTMs) reveals features of PTM crosstalk in chromatin regulation. Mol Cell Proteomics. 2016;15(8):2715–2729.
   PubMed Web of Science ®Google Scholar
• Wang Z, Zang C, Rosenfeld JA, et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet. 2008;40(7):897–903.
   PubMed Web of Science ®Google Scholar
• Voigt P, LeRoy G, Drury WJ 3rd, et al. Asymmetrically modified nucleosomes. Cell. 2012;151(1):181–193.
   PubMed Web of Science ®Google Scholar
• Lex A, Gehlenborg N, Strobelt H, et al. UpSet: visualization of intersecting sets. IEEE Trans Vis Comput Graph. 2014;20(12):1983–1992.
   PubMed Web of Science ®Google Scholar
• Nardelli SC, Che FY, Silmon De Monerri NC, et al. The histone code of Toxoplasma gondii comprises conserved and unique posttranslational modifications. Mbio. 2013;4(6):e00922–00913.
   PubMed Web of Science ®Google Scholar
• Sidoli S, Vandamme J, Salcini AE, et al. Dynamic changes of histone H3 marks during Caenorhabditis elegans lifecycle revealed by middle-down proteomics. Proteomics. 2016;16(3):459–464.
   PubMed Web of Science ®Google Scholar
• Jamieson K, Wiles ET, McNaught KJ, et al. Loss of HP1 causes depletion of H3K27me3 from facultative heterochromatin and gain of H3K27me2 at constitutive heterochromatin. Genome Res. 2016;26(1):97–107.
   PubMed Web of Science ®Google Scholar
• Tvardovskiy A, Wrzesinski K, Sidoli S, et al. Top-down and middle-down protein analysis reveals that intact and clipped human histones differ in post-translational modification patterns. Mol Cell Proteomics. 2015;14(12):3142–3153.
   PubMed Web of Science ®Google Scholar
• Zheng Y, Huang X, Kelleher NL. Epiproteomics: quantitative analysis of histone marks and codes by mass spectrometry. Curr Opin Chem Biol. 2016;33:142–150.
   PubMed Web of Science ®Google Scholar
• Sidoli S, Lin S, Karch KR, et al. Bottom-up and middle-down proteomics have comparable accuracies in defining histone post-translational modification relative abundance and stoichiometry. Anal Chem. 2015;87(6):3129–3133.
   PubMed Web of Science ®Google Scholar
• Vandamme J, Sidoli S, Mariani L, et al. H3K23me2 is a new heterochromatic mark in Caenorhabditis elegans. Nucleic Acids Res. 2015;43(20):9694–9710.
   PubMed Web of Science ®Google Scholar
• Shvartsburg AA, Zheng Y, Smith RD, et al. Separation of variant methylated histone tails by differential ion mobility. Anal Chem. 2012;84(15):6317–6320.
   PubMed Web of Science ®Google Scholar