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
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We present the first comprehensive capillary electrophoresis electrospray ionization mass spectrometry (CESI-MS) analysis of post-translational modifications derived from H1 and core histones. Using a capillary electrophoresis system equipped with a sheathless high-sensitivity porous sprayer and nano-liquid chromatography electrospray ionization mass spectrometry (nano-LC-ESI-MS) as two complementary techniques, we characterized H1 histones isolated from rat testis. Without any pre-separation of the perchloric acid extraction, a total of 70 different modified peptides, including 50 phosphopeptides, were identified in the rat linker histones H1.0, H1a-H1e, and H1t. Out of the 70 modified H1 histone peptides, 27 peptides could be identified with CESI-MS only, and 11 solely with LC-ESI-MS. Immobilized metal-affinity chromatography enrichment prior to MS analysis yielded a total of 55 phosphopeptides; 22 of these peptides could be identified only by CESI-MS, and 19 only by LC-ESI-MS, showing the complementarity of the two techniques. We mapped 42 H1 modification sites, including 31 phosphorylation sites, of which 8 were novel sites. For the analysis of core histones, we chose a different strategy. In a first step, the sulfuric-acid-extracted core histones were pre-separated using reverse-phase high-performance liquid chromatography. Individual rat testis core histone fractions obtained in this way were digested and analyzed via bottom-up CESI-MS. This approach yielded the identification of 42 different modification sites including acetylation (lysine and N(α)-terminal); mono-, di-, and trimethylation; and phosphorylation. When we applied CESI-MS for the analysis of intact core histone subtypes from butyrate-treated mouse tumor cells, we were able to rapidly detect their degree of modification, and we found this method very useful for the separation of isobaric trimethyl and acetyl modifications. Taken together, our results highlight the need for additional techniques for the comprehensive analysis of post-translational modifications. CESI-MS is a promising new proteomics tool as demonstrated by this, the first comprehensive analysis of histone modifications, using rat testis as an example.
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Jenuwein, T., & Allis, C. D. (2001) · Science · doi:10.1126/science.1063127 · Cited by 9,756 · see citing works
Histone acetylation and an epigenetic code
Turner, B. M. (2000) · BioEssays · doi:10.1002/1521-1878(200009)22:9 · Cited by 1,214 · see citing works
Sugimoto, M., Wong, D. T., Hirayama, A., Soga, T., & Tomita, M. (2009) · Metabolomics · doi:10.1007/s11306-009-0178-y · Cited by 1,002 · see citing works
Hirayama, A., Kami, K., Sugimoto, M., Sugawara, M., Toki, N., Onozuka, H., Kinoshitá, T., Saito, N., Ochiai, A., Tomita, M., et al. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-4806 · Cited by 959 · see citing works
Schmidt, A., Karas, M., & Dülcks, T. (2003) · Journal of the American Society for Mass Spectrometry · doi:10.1016/s1044-0305(03)00128-4 · Cited by 535 · see citing works
Naturally Occurring Human Urinary Peptides for Use in Diagnosis of Chronic Kidney Disease
Good, D. M., Zürbig, P., Argilés, À., Bauer, H. W., Behrens, G., Coon, J. J., Dakna, M., Decramer, S., Delles, C., Dominiczak, A. F., et al. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.001917 · Cited by 525 · see citing works
Histone H1 and its isoforms: Contribution to chromatin structure and function
Happel, N., & Doenecke, D. (2008) · Gene · doi:10.1016/j.gene.2008.11.003 · Cited by 424 · see citing works
Chemical derivatization of histones for facilitated analysis by mass spectrometry
Garcia, B. A., Mollah, S., Ueberheide, B. M., Busby, S. A., Muratore‐Schroeder, T. L., Shabanowitz, J., & Hunt, D. F. (2007) · Nature Protocols · doi:10.1038/nprot.2007.106 · Cited by 389 · see citing works
Moini, M. (2007) · Analytical Chemistry · doi:10.1021/ac0704560 · Cited by 322 · see citing works
High Throughput Characterization of Combinatorial Histone Codes
Young, N. L., DiMaggio, P. A., Plazas-Mayorca, M. D., Baliban, R. C., Floudas, C. A., & Garcia, B. A. (2009) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m900238-mcp200 · Cited by 312 · see citing works
Recent advances in capillary electrophoresis/electrospray/mass spectrometry
Banks, J. F. (1997) · Electrophoresis · doi:10.1002/elps.1150181216 · Cited by 308 · see citing works
Sarg, B., Koutzamani, E., Helliger, W., Rundquist, I., & Lindner, H. H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205166200 · Cited by 252 · see citing works
Self-citationPervasive combinatorial modification of histone H3 in human cells
Garcia, B. A., Pesavento, J. J., Mizzen, C. A., & Kelleher, N. L. (2007) · Nature Methods · doi:10.1038/nmeth1052 · Cited by 242 · see citing works
Pesavento, J. J., Mizzen, C. A., & Kelleher, N. L. (2006) · Analytical Chemistry · doi:10.1021/ac0600050 · Cited by 240 · see citing works
Wojcik, R., Dada, O. O., Sadilek, M., & Dovichi, N. J. (2010) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.4672 · Cited by 234 · see citing works
Wiśniewski, J. R., Zougman, A., Krüger, S., & Mann, M. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600255-mcp200 · Cited by 233 · see citing works
Urinary Proteomic Biomarkers in Coronary Artery Disease
Zimmerli, L., Schiffer, E., Zürbig, P., Good, D. M., Kellmann, M., Mouls, L., Pitt, A. R., Coon, J. J., Schmieder, R. E., Peter, K., et al. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700394-mcp200 · Cited by 226 · see citing works
The histone H1 family: specific members, specific functions?
Izzo, A., Kamieniarz-Gdula, K., & Schneider, R. (2008) · Biological Chemistry · doi:10.1515/bc.2008.037 · Cited by 223 · see citing works
Maxwell, E. J., & Chen, D. D. Y. (2008) · Analytica Chimica Acta · doi:10.1016/j.aca.2008.06.034 · Cited by 197 · see citing works
Recent advances in capillary electrophoresis/electrospray-mass spectrometry
von Brocke, A., NICHOLSON, G. J., & Bayer, E. (2001) · Electrophoresis · doi:10.1002/1522-2683(200105)22:7 · Cited by 197 · see citing works
Mass Spectrometric Characterization of Human Histone H3: A Bird's Eye View
Thomas, C. E., Kelleher, N. L., & Mizzen, C. A. (2006) · Journal of Proteome Research · doi:10.1021/pr050266a · Cited by 190 · see citing works
博一, 長., Bullock, C. R., LeDuc, R. D., Mizzen, C. A., & Kelleher, N. L. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m709796200 · Cited by 185 · see citing works
Busnel, J., Schoenmaker, B., Ramautar, R., Carrasco‐Pancorbo, A., Ratnayake, C. K., Feitelson, J. S., Chapman, J. D., Deelder, A. M., & Mayboroda, O. A. (2010) · Analytical Chemistry · doi:10.1021/ac102159d · Cited by 165 · see citing works
Tweedie‐Cullen, R. Y., Brunner, A. M., Grossmann, J., Mohanna, S., Sichau, D., Nanni, P., Panse, C., & Mansuy, I. M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0036980 · Cited by 162 · see citing works
Precise Characterization of Human Histones in the H2A Gene Family by Top Down Mass Spectrometry
Boyne, M. T., Pesavento, J. J., Mizzen, C. A., & Kelleher, N. L. (2006) · Journal of Proteome Research · doi:10.1021/pr050269n · Cited by 157 · see citing works
Faserl, K., Sarg, B., Kremser, L., & Lindner, H. H. (2011) · Analytical Chemistry · doi:10.1021/ac2010372 · Cited by 153 · see citing works
Self-citationTweedie‐Cullen, R. Y., Reck, J. M., & Mansuy, I. M. (2009) · Journal of Proteome Research · doi:10.1021/pr9003739 · Cited by 150 · see citing works
Decoupling CE and ESI for a more robust interface with MS
Maxwell, E. J., Zhong, X., Zhang, H., van Zeijl, N., & Chen, D. D. Y. (2010) · Electrophoresis · doi:10.1002/elps.200900517 · Cited by 150 · see citing works
Wang, Y., Fonslow, B. R., Wong, C. C. L., Nakorchevsky, A., & Yates, J. R. (2012) · Analytical Chemistry · doi:10.1021/ac301091m · Cited by 144 · see citing works
Characterization of histones and their post-translational modifications by mass spectrometry
Garcia, B. A., Shabanowitz, J., & Hunt, D. F. (2006) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2006.11.022 · Cited by 143 · see citing works
Bonenfant, D., Coulot, M., Towbin, H., Schindler, P. A., & van Oostrum, J. (2005) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m500288-mcp200 · Cited by 142 · see citing works
Li, Y., Champion, M. M., Sun, L., Champion, P. A. D., Wojcik, R., & Dovichi, N. J. (2012) · Analytical Chemistry · doi:10.1021/ac202899p · Cited by 128 · see citing works
Talasz, H., Lindner, H. H., Sarg, B., & Helliger, W. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m505563200 · Cited by 120 · see citing works
Self-citationHistone H1 Phosphorylation Occurs Site-specifically during Interphase and Mitosis
Sarg, B., Helliger, W., Talasz, H., Förg, B., & Lindner, H. H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m508957200 · Cited by 117 · see citing works
Self-citationSeparation of acetylated core histones by hydrophilic-interaction liquid chromatography
Lindner, H. H., Sarg, B., Meraner, C., & Helliger, W. (1996) · Journal of Chromatography A · doi:10.1016/0021-9673(96)00131-8 · Cited by 111 · see citing works
Self-citationHaselberg, R., Ratnayake, C. K., de Jong, G. J., & Somsen, G. W. (2010) · Journal of Chromatography A · doi:10.1016/j.chroma.2010.10.006 · Cited by 109 · see citing works
Gene-specific characterization of human histone H2B by electron capture dissociation.
Siuti, N., Roth, M. J., Mizzen, C., Kelleher, N., & Pesavento, J. J. (2006) · Journal of Proteome Research · doi:10.1021/pr050268v · Cited by 101 · see citing works
Lindner, H. H., Sarg, B., & Helliger, W. (1997) · Journal of Chromatography A · doi:10.1016/s0021-9673(97)00468-8 · Cited by 95 · see citing works
Self-citationZamfir, A. D. (2007) · Journal of Chromatography A · doi:10.1016/j.chroma.2007.03.115 · Cited by 87 · see citing works
CE–MS for proteomics: Advances in interface development and application
Ramautar, R., Heemskerk, A. A. M., Hensbergen, P. J., Deelder, A. M., Busnel, J.-M., & Mayboroda, O. A. (2012) · Journal of Proteomics · doi:10.1016/j.jprot.2012.04.050 · Cited by 86 · see citing works
Kelly, R., Page, J. S., Zhao, R., Qian, W., Mottaz, H. M., Tang, K., & Smith, R. D. (2007) · Analytical Chemistry · doi:10.1021/ac701647s · Cited by 74 · see citing works
Issaq, H. J., Janini, G. M., Chan, K. C., & Veenstra, T. (2004) · Journal of Chromatography A · doi:10.1016/s0021-9673(04)01475-x · Cited by 68 · see citing works
Histone H4 Hyperacetylation Precludes Histone H4 Lysine 20 Trimethylation
Sarg, B., Helliger, W., Talasz, H., Koutzamani, E., & Lindner, H. H. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m409099200 · Cited by 67 · see citing works
Self-citationLindner, H. H., Helliger, W., Dirschlmayer, A., Jaquemar, M., & Puschendorf, B. (1992) · Biochemical Journal · doi:10.1042/bj2830467 · Cited by 67 · see citing works
Self-citationDahlin, A. P., Wetterhall, M., Liljegren, G., Bergström, S. K., Andrén, P. E., Nyholm, L., Markides, K. E., & Bergquist, J. (2005) · The Analyst · doi:10.1039/b414592e · Cited by 65 · see citing works
The Microheterogeneity of the Mammalian H10Histone
Lindner, H. H., Sarg, B., Hoertnagl, B., & Helliger, W. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.21.13324 · Cited by 63 · see citing works
Self-citationComprehensive Phosphoprotein Analysis of Linker Histone H1 from Tetrahymena thermophila
Garcia, B. A., Joshi, S. M., Thomas, C. E., Chitta, R. K., Diaz, R. L., Busby, S. A., Andrews, P., Loo, R. R. O., Shabanowitz, J., Kelleher, N. L., et al. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600086-mcp200 · Cited by 62 · see citing works
Pesavento, J. J., Garcia, B., Streeky, J. A., Kelleher, N., & Mizzen, C. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m600404-mcp200 · Cited by 61 · see citing works
The analysis of histone modifications
Villar‐Garea, A., & Imhof, A. (2006) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2006.08.009 · Cited by 60 · see citing works
Nguyen, A., & Moini, M. (2008) · Analytical Chemistry · doi:10.1021/ac801158q · Cited by 55 · see citing works
Recent advances in CE‐MS: Synergy of wet chemistry and instrumentation innovations
Pantůčková, P., Gebauer, P., Boček, P., & Křivánková, L. (2010) · Electrophoresis · doi:10.1002/elps.201000382 · Cited by 54 · see citing works
Analysis of Complex Protein Mixtures with Improved Sequence Coverage Using (CE−MS/MS)n
Garza, S., & Moini, M. (2006) · Analytical Chemistry · doi:10.1021/ac0612269 · Cited by 50 · see citing works
Effect of buffer composition on the migration order and separation of histone H1 subtypes
Lindner, H. H., Helliger, W., Sarg, B., & Meraner, C. (1995) · Electrophoresis · doi:10.1002/elps.1150160197 · Cited by 48 · see citing works
Self-citationAge-dependent deamidation of H1° histones in chromatin of mammalian tissues
Lindner, H. H., Sarg, B., Grunicke, H. H., & Helliger, W. (1999) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s004320050261 · Cited by 47 · see citing works
Self-citationWood, C., Snijders, A. P., Williamson, J. C., Reynolds, C. D., Baldwin, J., & Dickman, M. J. (2009) · FEBS Journal · doi:10.1111/j.1742-4658.2009.07079.x · Cited by 46 · see citing works
Elhamili, A., Wetterhall, M., Arvidsson, B., Sebastiano, R., Righetti, P. G., & Bergquist, J. (2008) · Electrophoresis · doi:10.1002/elps.200700737 · Cited by 44 · see citing works
Self-citationSu, X., Ren, C., & Freitas, M. A. (2007) · Expert Review of Proteomics · doi:10.1586/14789450.4.2.211 · Cited by 43 · see citing works
Zamfir, A. D., Dincă, N., Şişu, E., & Peter‐Katalinić, J. (2006) · Journal of Separation Science · doi:10.1002/jssc.200500374 · Cited by 41 · see citing works
Separation of phosphorylated histone H1 variants by high-performance capillary electrophoresis
Lindner, H. H., Helliger, W., Dirschlmayer, A., Talasz, H., Wurm, M., Sarg, B., Jaquemar, M., & Puschendorf, B. (1992) · Journal of Chromatography A · doi:10.1016/0021-9673(92)87126-s · Cited by 38 · see citing works
Self-citationApplication of high‐performance capillary electrophoresis to the analysis of H1 histones
Lindner, H. H., Wurm, M., Dirschlmayer, A., Sarg, B., & Helliger, W. (1993) · Electrophoresis · doi:10.1002/elps.1150140174 · Cited by 36 · see citing works
Self-citationTestis-specific Linker Histone H1t Is Multiply Phosphorylated during Spermatogenesis
Sarg, B., Chwatal, S., Talasz, H., & Lindner, H. H. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m805925200 · Cited by 35 · see citing works
Self-citationAnalysis of histones, histone variants, and their post‐translationally modified forms
Lindner, H. H. (2008) · Electrophoresis · doi:10.1002/elps.200800094 · Cited by 33 · see citing works
Self-citationLindner, H. H., Helliger, W., & Puschendorf, B. (1990) · Biochemical Journal · doi:10.1042/bj2690359 · Cited by 33 · see citing works
Self-citationLiquid chromatography mass spectrometry profiling of histones
Su, X., Jacob, N. K., Amunugama, R., Lucas, D. M., Knapp, A. R., Ren, C., Davis, M. E., Marcucci, G., Parthun, M. R., Byrd, J. C., et al. (2007) · Journal of Chromatography B · doi:10.1016/j.jchromb.2006.12.037 · Cited by 31 · see citing works
ω-Iodoalkylammonium salts as permanent capillary silica wall modifiers
Sebastiano, R., Gelfi, C., Righetti, P. G., & Citterio, A. (2001) · Journal of Chromatography A · doi:10.1016/s0021-9673(01)00804-4 · Cited by 29 · see citing works
Self-citationKele, Z., Ferenc, G., Klement, É., Tóth, G. K., & Janáky, T. (2005) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.1866 · Cited by 28 · see citing works
Sarg, B., Helliger, W., Hoertnagl, B., Puschendorf, B., & Lindner, H. H. (1999) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1999.1503 · Cited by 25 · see citing works
Self-citationLindner, H. H., Wesierska-Gadek, J., Helliger, W., Pushendorf, B., & Sauermann, G. (1989) · Journal of Chromatography A · doi:10.1016/s0021-9673(00)94110-4 · Cited by 15 · see citing works
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Phosphoproteomics in the Age of Rapid and Deep Proteome Profiling
Riley, N. M., & Coon, J. J. (2016) · Analytical Chemistry · doi:10.1021/acs.analchem.5b04123 · Cited by 265 · see citing works
Sun, L., Zhu, G., Zhang, Z., Mou, S., & Dovichi, N. J. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00100 · Cited by 216 · see citing works
Recent advances in column coatings for capillary electrophoresis of proteins
Hajba, L., & Guttman, A. (2017) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2017.02.013 · Cited by 151 · see citing works
Recent developments in capillary and microchip electroseparations of peptides (2011–2013)
Kašička, V. (2013) · Electrophoresis · doi:10.1002/elps.201300331 · Cited by 130 · see citing works
McCool, E. N., Lubeckyj, R. A., Shen, X., Chen, D., Kou, Q., Liu, X., & Sun, L. (2018) · Analytical Chemistry · doi:10.1021/acs.analchem.8b00693 · Cited by 117 · see citing works
The coordinated action of the MVB pathway and autophagy ensures cell survival during starvation
Müller, M., Schmidt, O., Angelova, M., Faserl, K., Weys, S., Kremser, L., Pfaffenwimmer, T., Dalik, T., Kraft, C., Trajanoski, Z., et al. (2015) · eLife · doi:10.7554/elife.07736 · Cited by 117 · see citing works
Self-citationRecent applications of capillary electromigration methods to separation and analysis of proteins
Štěpánová, S., & Kašička, V. (2016) · Analytica Chimica Acta · doi:10.1016/j.aca.2016.06.006 · Cited by 114 · see citing works
Recent trends of capillary electrophoresis‐mass spectrometry in proteomics research
Gomes, F. P., & Yates, J. R. (2019) · Mass Spectrometry Reviews · doi:10.1002/mas.21599 · Cited by 112 · see citing works
Lubeckyj, R. A., McCool, E. N., Shen, X., Kou, Q., Liu, X., & Sun, L. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.7b02532 · Cited by 96 · see citing works
Middle-down proteomics: a still unexploited resource for chromatin biology
Sidoli, S., & Garcia, B. A. (2017) · Expert Review of Proteomics · doi:10.1080/14789450.2017.1345632 · Cited by 90 · see citing works
Current Trends in the Analysis of Post-translational Modifications
Virág, D., Kiss, B. D., Vékey, K., Drahos, L., Klebovich, I., Antal, I., & Ludányi, K. (2019) · Chromatographia · doi:10.1007/s10337-019-03796-9 · Cited by 92 · see citing works
Histone H1 Post-Translational Modifications: Update and Future Perspectives
Andrés, M., García-Gomis, D., Ponte, I., Suau, P., & Roque, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21165941 · Cited by 89 · see citing works
Histone N-alpha terminal modifications: genome regulation at the tip of the tail
Demetriadou, C., Koufaris, C., & Kirmizis, A. (2020) · Epigenetics & Chromatin · doi:10.1186/s13072-020-00352-w · Cited by 79 · see citing works
Kammeijer, G. S. M., Kohler, I., Jansen, B. C., Hensbergen, P. J., Mayboroda, O. A., Falck, D., & Wuhrer, M. (2016) · Analytical Chemistry · doi:10.1021/acs.analchem.6b00479 · Cited by 74 · see citing works
Zhong, X., Zhang, Z., Jiang, S., & Li, L. (2013) · Electrophoresis · doi:10.1002/elps.201300451 · Cited by 74 · see citing works
Lubeckyj, R. A., Basharat, A. R., Shen, X., Liu, X., & Sun, L. (2019) · Journal of the American Society for Mass Spectrometry · doi:10.1007/s13361-019-02167-w · Cited by 72 · see citing works
Štěpánová, S., & Kašička, V. (2015) · Journal of Separation Science · doi:10.1002/jssc.201500973 · Cited by 70 · see citing works
Gahoual, R., Biacchi, M., Chicher, J., Kühn, L., Hammann, P., Beck, A., Leize‐Wagner, E., & François, Y. (2014) · mAbs · doi:10.4161/mabs.36305 · Cited by 68 · see citing works
Recent developments in capillary and microchip electroseparations of peptides (2013–middle 2015)
Kašička, V. (2015) · Electrophoresis · doi:10.1002/elps.201500329 · Cited by 68 · see citing works
Önder, Ö., Sidoli, S., Carroll, M. P., & Garcia, B. A. (2015) · Expert Review of Proteomics · doi:10.1586/14789450.2015.1084231 · Cited by 65 · see citing works
CE–ESI‐MS for bottom‐up proteomics: Advances in separation, interfacing and applications
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Ludwig, K. R., Sun, L., Zhu, G., Dovichi, N. J., & Hummon, A. B. (2015) · Analytical Chemistry · doi:10.1021/acs.analchem.5b02457 · Cited by 56 · see citing works
Quantitative Proteomics Using Ultralow Flow Capillary Electrophoresis–Mass Spectrometry
Faserl, K., Kremser, L., Müller, M., Teis, D., & Lindner, H. H. (2015) · Analytical Chemistry · doi:10.1021/acs.analchem.5b00312 · Cited by 57 · see citing works
Self-citationRobledo, V. R., & Smyth, W. F. (2014) · Electrophoresis · doi:10.1002/elps.201300561 · Cited by 55 · see citing works
Guo, X., Fillmore, T. L., Gao, Y., & Tang, K. (2016) · Analytical Chemistry · doi:10.1021/acs.analchem.5b04912 · Cited by 54 · see citing works
Yang, C., Zhong, X., & Li, L. (2014) · Electrophoresis · doi:10.1002/elps.201400017 · Cited by 47 · see citing works
Faserl, K., Sarg, B., Maurer, V., & Lindner, H. H. (2017) · Journal of Chromatography A · doi:10.1016/j.chroma.2017.01.086 · Cited by 43 · see citing works
Self-citationYang, Z., Shen, X., Chen, D., & Sun, L. (2018) · Analytical Chemistry · doi:10.1021/acs.analchem.8b02466 · Cited by 43 · see citing works
Capillary zone electrophoresis for bottom‐up analysis of complex proteomes
Sun, L., Zhu, G., Yan, X., Zhang, Z., Wojcik, R., Champion, M. M., & Dovichi, N. J. (2016) · PROTEOMICS · doi:10.1002/pmic.201500339 · Cited by 41 · see citing works
Faserl, K., Sarg, B., Gruber, P., & Lindner, H. H. (2018) · ELECTROPHORESIS · doi:10.1002/elps.201700437 · Cited by 38 · see citing works
Self-citationGahoual, R., Beck, A., François, Y., & Leize‐Wagner, E. (2016) · Journal of Mass Spectrometry · doi:10.1002/jms.3735 · Cited by 36 · see citing works
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Chen, D., Yang, Z., Shen, X., & Sun, L. (2021) · Analytical Chemistry · doi:10.1021/acs.analchem.0c04237 · Cited by 35 · see citing works
Chen, D., Ludwig, K. R., Krokhin, O. V., Spicer, V., Yang, Z., Shen, X., Hummon, A. B., & Sun, L. (2019) · Analytical Chemistry · doi:10.1021/acs.analchem.8b04770 · Cited by 34 · see citing works
Nguyen, T. T. T. N., Petersen, N. J., & Rand, K. D. (2016) · Analytica Chimica Acta · doi:10.1016/j.aca.2016.07.002 · Cited by 33 · see citing works
Sarg, B., López, R., Lindner, H. H., Ponte, I., Suau, P., & Roque, A. (2014) · Journal of Proteomics · doi:10.1016/j.jprot.2014.10.004 · Cited by 33 · see citing works
Self-citationRevealing the potential of capillary electrophoresis/mass spectrometry: the tipping point
Gahoual, R., Leize‐Wagner, E., Houzé, P., & François, Y. (2018) · Rapid Communications in Mass Spectrometry · doi:10.1002/rcm.8238 · Cited by 32 · see citing works
Sun, L., Zhu, G., Mou, S., Zhao, Y., Champion, M. M., & Dovic̀hi, N. J. (2014) · Journal of Chromatography A · doi:10.1016/j.chroma.2014.07.024 · Cited by 31 · see citing works
Zhu, G., Sun, L., Linkous, T., Kernaghan, D., McGivney, J. B., & Dovic̀hi, N. J. (2014) · Electrophoresis · doi:10.1002/elps.201300545 · Cited by 28 · see citing works
Plasma Proteomic Analysis Distinguishes Severity Outcomes of Human Ebola Virus Disease
Viodé, A., Smolen, K. K., Fatou, B., Wurie, Z., van Zalm, P., Kondé, M. K., Kéita, B. M., Ablam, R. A., Fish, E. N., & Steen, H. (2022) · mBio · doi:10.1128/mbio.00567-22 · Cited by 27 · see citing works
Morbioli, G. G., Mazzu-Nascimento, T., Aquino, A., Cervantes, C. A. C., & Carrilho, E. (2016) · Analytica Chimica Acta · doi:10.1016/j.aca.2016.06.019 · Cited by 21 · see citing works
Dada, O. O., Zhao, Y., Jaya, N., & Salas-Solano, O. (2017) · Analytical Chemistry · doi:10.1021/acs.analchem.7b03405 · Cited by 20 · see citing works
Zhu, G., Sun, L., Yan, X., & Dovic̀hi, N. J. (2013) · Analytica Chimica Acta · doi:10.1016/j.aca.2013.11.057 · Cited by 20 · see citing works
Interphase H1 phosphorylation: Regulation and functions in chromatin
Liao, R., & Mizzen, C. A. (2015) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2015.11.012 · Cited by 19 · see citing works
Dominguez-Vega, E., De Vijlder, T., Romijn, E. P., & Somsen, G. W. (2017) · Analytica Chimica Acta · doi:10.1016/j.aca.2017.06.021 · Cited by 19 · see citing works
Application of CE-MS for the analysis of histones and histone modifications
Faserl, K., Sarg, B., & Lindner, H. H. (2020) · Methods · doi:10.1016/j.ymeth.2020.01.017 · Cited by 18 · see citing works
Self-citationGuzman, N., & Guzman, D. E. (2021) · Biomolecules · doi:10.3390/biom11101443 · Cited by 17 · see citing works
Fang, F., Xu, T., Hagar, H. C., Hovde, S., Kuo, M., & Sun, L. (2024) · Journal of Proteome Research · doi:10.1021/acs.jproteome.4c00587 · Cited by 17 · see citing works
Sarg, B., Faserl, K., & Lindner, H. H. (2017) · PROTEOMICS · doi:10.1002/pmic.201700269 · Cited by 17 · see citing works
Self-citationIbrahim, M., Gahoual, R., Enkler, L., Becker, H. D., Chicher, J., Hammann, P., François, Y., Kühn, L., & Leize‐Wagner, E. (2016) · Journal of Chromatographic Science · doi:10.1093/chromsci/bmw005 · Cited by 16 · see citing works
Cheng, J., Morin, G. B., & Chen, D. D. Y. (2020) · Electrophoresis · doi:10.1002/elps.201900452 · Cited by 15 · see citing works
Nath, S., Roy, R., & Mukherjee, S. (2012) · PubMed · Cited by 15 · see citing works
Liu, J., Zhang, Y., Yuan, F., Chen, H., & Zhang, X. (2014) · Electrophoresis · doi:10.1002/elps.201400334 · Cited by 12 · see citing works
Moreno‐González, D., Haselberg, R., Gámiz‐Gracia, L., García-Campaña, A. M., de Jong, G. J., & Somsen, G. W. (2017) · Journal of Chromatography A · doi:10.1016/j.chroma.2017.09.075 · Cited by 11 · see citing works
SPE-CZE-MS Quantifies Zeptomole Amounts of Phosphorylated Peptides
Serrano, L. R., Mellors, J. S., Thompson, J. W., Lancaster, N. M., Robinson, M. L., Overmyer, K. A., Quarmby, S. T., & Coon, J. J. (2025) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5c00194 · Cited by 8 · see citing works
Profiling post-translational modifications of histones in human monocyte-derived macrophages
Olszowy, P., Donnelly, M. R., Lee, C., & Ciborowski, P. S. (2015) · Proteome Science · doi:10.1186/s12953-015-0080-7 · Cited by 7 · see citing works
Rinas, A., Jenkins, C., & Orsburn, B. C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/559591 · Cited by 6 · see citing works
Electrospray Ionization Interface Development for Capillary Electrophoresis-Mass Spectrometry
Risley, J. M., Jong, C. A. G. D., & Chen, D. D. Y. (2016) · Wiley-VCH eBooks · doi:10.1002/9783527693801.ch2 · Cited by 6 · see citing works
Einfinger, K., Badrnya, S., Furtmüller, M., Handschuh, D., Lindner, H. H., & Geiger, M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0143137 · Cited by 6 · see citing works
Self-citationZhang, W., Tang, X., Ding, M., & Zhong, H. (2014) · Analytica Chimica Acta · doi:10.1016/j.aca.2014.08.038 · Cited by 5 · see citing works
Capillary Electrophoresis-Mass Spectrometry for Proteomics
Martelli, C., & Desiderio, C. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809375-7.00014-9 · Cited by 5 · see citing works
Analyzing Posttranslational Modifications in Single Cells
Orsburn, B. C. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-3934-4_12 · Cited by 4 · see citing works
Liu, R., Lü, G., Hu, X., Li, J., Zhang, Z., & Tang, K. (2024) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-024-05502-7 · Cited by 4 · see citing works
Peptidomics and Capillary Electrophoresis
Štěpánová, S., & Kašička, V. (2021) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-77252-9_5 · Cited by 3 · see citing works
And Yet it is Modified—Holding a Candle to the Dark Matter of White Matter
Harauz, G. (2017) · PROTEOMICS · doi:10.1002/pmic.201700299 · Cited by 2 · see citing works
Segl, M., & Stutz, H. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2493-7_7 · Cited by 2 · see citing works
CE-MS for Clinical Proteomics and Metabolomics: Strategies and Applications
Ramautar, R., & Britz‐McKibbin, P. (2016) · Wiley-VCH eBooks · doi:10.1002/9783527693801.ch11 · Cited by 1 · see citing works
Gahoual, R., François, Y., Mignet, N., & Houzé, P. (2020) · Elsevier eBooks · doi:10.1016/b978-0-08-102906-0.00017-9 · Cited by 1 · see citing works
SPE-CZE-MS quantifies zeptomole concentrations of phosphorylated peptidesPreprint
Serrano, L. R., Mellors, J. S., Thompson, J. W., Lancaster, N. M., Robinson, M. L., Overmyer, K. A., Quarmby, S. T., & Coon, J. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.07.627347 · Cited by 1 · see citing works
Trends in CE ‐ MS and Applications
Týčová, A., & Foret, F. (2015) · doi:10.1002/9783527678129.assep039
Yuan, F., Ma, Y., Zhou, Y., & Zhang, X. (2021) · Springer protocols handbooks/Springer protocols · doi:10.1007/978-1-0716-1229-3_3
Woolfork, A. G., & Hage, D. S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-85486-3.00014-7
Identifying post-translational modifications with single cell proteomicsPreprint
Orsburn, B. C. (2023) · doi:10.31219/osf.io/465er
- Authors
- Sarg, B., Faserl, K., Kremser, L., Halfinger, B., Sebastiano, R., & Lindner, H. H.
- Affiliations
- Innsbruck Medical University (AT)
- Politecnico di Milano (IT)
- Corresponding author
- Lindner, Herbert H.
- Venue
- Molecular & Cellular Proteomics
- Publisher
- Elsevier BV
- Published
- 2013-09
- Volume
- 12
- Issue
- 9
- Pages
- 2640-2656
- ISSN
- 1535-9476 (ISSN-L)
- PMC
- PMC3769336
- OpenAlex
- W2103023204
- Cited by
- 76
- References
- 68
- Citations by year
- 2025: 1 · 2024: 4 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 5 · 2019: 5 · 2018: 7 · 2017: 11 · 2016: 9 · 2015: 13 · 2014: 9 · 2013: 3 · 2012: 1
- FWCI
- 5.09
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Molecular & Cellular Proteomics (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Virtual Community of Pathological Anatomy (University of Castilla La Mancha) (submittedVersion)
- Topics
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Physical Sciences › Chemistry › Spectroscopy › Mass Spectrometry Techniques and Applications
- Physical Sciences › Engineering › Biomedical Engineering › Microfluidic and Capillary Electrophoresis Applications
- Keywords
- histone modifications, core histones, histone phosphorylation, histone acetylation, histone methylation, phosphopeptides, rat testis, shotgun proteomics
- MeSH terms
- Acetylation, Animals, Arginase, Cell Line, Chromatography, Affinity, Chromatography, Liquid, Histones, Male, Methylation, Molecular Weight, Phosphopeptides, Protein Processing, Post-Translational, Testis, Rats, Sprague-Dawley, Electrophoresis, Capillary, Spectrometry, Mass, Electrospray Ionization, Nanotechnology, Mice, Rats
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