Advanced search
Publication Cover
Expert Review of Proteomics Volume 8, 2011 - Issue 5
Submit an article Journal homepage
484
Views
96
CrossRef citations to date
0
Altmetric
Review

Breaking the histone code with quantitative mass spectrometry

Laura-Mae P Britton Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA; Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA
,
Michelle Gonzales-Cope Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA; Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA
,
Barry M Zee Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA; Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA
&
Benjamin A Garcia Department of Molecular Biology, Princeton University, Princeton, NJ 08544, USA; Department of Chemistry, Princeton University, Princeton, NJ 08544, USA; Quantitative and Computational Biology Program, Princeton University, Princeton, NJ 08544, USA;[email protected]
Pages 631-643 | Published online: 09 Jan 2014

References

  • Campos EI, Reinberg D. Histones: annotating chromatin. Annu. Rev. Genet.43, 559–599 (2009).
  • Jenuwein T, Allis CD. Translating the histone code. Science293(5532), 1074–1080 (2001).
  • Strahl BD, Allis CD. The language of covalent histone modifications. Nature403(6765), 41–45 (2000).
  • Magenis RE, Brown MG, Lacy DA, Budden S, LaFranchi S. Is Angelman syndrome an alternate result of del(15)(q11q13)? Am. J. Med. Genet.28(4), 829–838 (1987).
  • Nicholls RD, Knoll JH, Butler MG, Karam S, Lalande M. Genetic imprinting suggested by maternal heterodisomy in nondeletion Prader–Willi syndrome. Nature342(6247), 281–285 (1989).
  • Hasegawa T, Hara M, Ando M et al. Cytogenetic studies of familial Prader–Willi syndrome. Hum. Genet.65(4), 325–330 (1984).
  • Smeets DF, Hamel BC, Nelen MR et al. Prader–Willi syndrome and Angelman syndrome in cousins from a family with a translocation between chromosomes 6 and 15. N. Engl. J. Med.326(12), 807–811 (1992).
  • Weksberg R, Nishikawa J, Caluseriu O et al. Tumor development in the Beckwith–Wiedemann syndrome is associated with a variety of constitutional molecular 11p15 alterations including imprinting defects of KCNQ1OT1. Hum. Mol. Genet.10(26), 2989–3000 (2001).
  • DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am. J. Hum. Genet.72(1), 156–160 (2003).
  • Prawitt D, Enklaar T, Gartner-Rupprecht B et al. Microdeletion of target sites for insulator protein CTCF in a chromosome 11p15 imprinting center in Beckwith–Wiedemann syndrome and Wilms’ tumor. Proc. Natl. Acad. Sci. USA102(11), 4085–4090 (2005).
  • Amir RE, Van den Veyver IB et al. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet.23(2), 185–188 (1999).
  • Carney RM, Wolpert CM, Ravan SA et al. Identification of MeCP2 mutations in a series of females with autistic disorder. Pediatr. Neurol.28(3), 205–211 (2003).
  • Zhang L, Freitas MA, Wickham J et al. Differential expression of histone post-translational modifications in acute myeloid and chronic lymphocytic leukemia determined by high-pressure liquid chromatography and mass spectrometry. J. Am. Soc. Mass Spectrom.15(1), 77–86 (2004).
  • Linggi BE, Brandt SJ, Sun ZW, Hiebert SW. Translating the histone code into leukemia. J. Cell. Biochem.96(5), 938–950 (2005).
  • Fraga MF, Ballestar E, Villar-Garea A et al. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat. Genet.37(4), 391–400 (2005).
  • Seligson DB, Horvath S, Shi T et al. Global histone modification patterns predict risk of prostate cancer recurrence. Nature435(7046), 1262–1266 (2005).
  • Wang GG, Song J, Wang Z et al. Haematopoietic malignancies caused by dysregulation of a chromatin-binding. finger. Nature459(7248), 847–851 (2009).
  • Minucci S, Pelicci PG. Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat. Rev. Cancer6(1), 38–51 (2006).
  • Moving AHEAD with an international human epigenome project. Nature454(7205), 711–715 (2008).
  • Park PJ. ChIP-seq: advantages and challenges of a maturing technology. Nat. Rev. Genet.10(10), 669–680 (2009).
  • Fuchs SM, Krajewski K, Baker RW, Miller VL, Strahl BD. Influence of combinatorial histone modifications on antibody and effector protein recognition. Curr. Biol.21(1), 53–58 (2011).
  • Brumbaugh J, Phanstiel D, Coon JJ. Unraveling the histone’s potential: a proteomics perspective. Epigenetics3(5), 254–257 (2008).
  • Trelle MB, Jensen ON. Functional proteomics in histone research and epigenetics. Expert Rev. Proteomics4(4), 491–503 (2007).
  • Evertts AG, Zee BM, Garcia BA. Modern approaches for investigating epigenetic signaling pathways. J. Appl. Physiol.109(3), 927–933 (2010).
  • Eberl HC, Mann M, Vermeulen M. Quantitative proteomics for epigenetics. ChemBioChem12(2), 224–234 (2010).
  • Strahl BD, Briggs SD, Brame CJ et al. Methylation of histone H4 at arginine 3 occurs in vivo and is mediated by the nuclear receptor coactivator PRMT1. Curr. Biol.11(12), 996–1000 (2001).
  • Weiss T, Hergeth S, Zeissler U et al. Histone H1 variant-specific lysine methylation by G9a/KMT1C and Glp1/KMT1D. Epigenetics Chromatin.3(1), 7 (2010).
  • Gardner KE, Zhou L, Parra MA, Chen X, Strahl BD. Identification of lysine 37 of histone H2B as a novel site of methylation. PLoS One6(1), e16244 (2011).
  • Xie W, Song C, Young NL et al. Histone h3 lysine 56 acetylation is linked to the core transcriptional network in human embryonic stem cells. Mol. Cell.33(4), 417–427 (2009).
  • Morris SA, Rao B, Garcia BA et al. Identification of histone H3 lysine 36 acetylation as a highly conserved histone modification. J. Biol. Chem.282(10), 7632–7640 (2007).
  • Baker SP, Phillips J, Anderson S et al. Histone H3 Thr 45 phosphorylation is a replication-associated post-translational modification in S. cerevisiae. Nat. Cell. Biol.12(3), 294–298 (2010).
  • Hurd PJ, Bannister AJ, Halls K et al. Phosphorylation of histone H3 Thr-45 is linked to apoptosis. J. Biol. Chem.284(24), 16575–16583 (2009).
  • Garske AL, Oliver SS, Wagner EK et al. Combinatorial profiling of chromatin binding modules reveals multisite discrimination. Nat. Chem. Biol.6(4), 283–290 (2010).
  • Fischle W, Tseng BS, Dormann HL et al. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature438(7071), 1116–1122 (2005).
  • Hirota T, Lipp JJ, Toh BH, Peters JM. Histone H3 serine 10 phosphorylation by Aurora B causes HP1 dissociation from heterochromatin. Nature438(7071), 1176–1180 (2005).
  • Sakabe K, Wang Z, Hart GW. β-N-acetylglucosamine (O-GlcNAc) is part of the histone code. Proc. Natl Acad. Sci. USA107(46), 19915–19920 (2010).
  • Wisniewski JR, 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.36(2), 570–577 (2008).
  • Messner S, Altmeyer M, Zhao H et al. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res.38(19), 6350–6362 (2010).
  • Chen Y, Sprung R, Tang Y et al. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol. Cell. Proteomics6(5), 812–819 (2007).
  • Wang Z, Zang C, Rosenfeld JA et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet.40(7), 897–903 (2008).
  • Cheng Z, Tang Y, Chen Y et al. Molecular characterization of propionyllysines in non-histone proteins. Mol. Cell. Proteomics8(1), 45–52 (2009).
  • Xiong L, Adhvaryu KK, Selker EU, Wang Y. Mapping of lysine methylation and acetylation in core histones of Neurospora crassa. Biochemistry49(25), 5236–5243 (2010).
  • Jufvas A, Stralfors P, Vener AV. Histone variants and their post-translational modifications in primary human fat cells. PLoS One6(1), e15960 (2011).
  • Tweedie-Cullen RY, Reck JM, Mansuy IM. Comprehensive mapping of post-translational modifications on synaptic, nuclear, and histone proteins in the adult mouse brain. J. Proteome Res.8(11), 4966–4982 (2009).
  • Garcia BA, Thomas CE, Kelleher NL, Mizzen CA. Tissue-specific expression and post-translational modification of histone H3 variants. J. Proteome Res.7(10), 4225–4236 (2008).
  • McKittrick E, Gafken PR, Ahmad K, Henikoff S. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl Acad. Sci. USA101(6), 1525–1530 (2004).
  • Darwanto A, Curtis MP, Schrag M et al. A modified ‘cross-talk’ between histone H2B Lys-120 ubiquitination and H3 Lys-79 methylation. J. Biol. Chem.285(28), 21868–21876 (2010).
  • Smith CM, Haimberger ZW, Johnson CO et al. Heritable chromatin structure: mapping ‘memory’ in histones H3 and H4. Proc. Natl Acad. Sci. USA99(Suppl. 4), 16454–16461 (2002).
  • Garcia BA, Mollah S, Ueberheide BM et al. Chemical derivatization of histones for facilitated analysis by mass spectrometry. Nat. Protoc.2(4), 933–938 (2007).
  • Bonaldi T, Imhof A, Regula JT. A combination of different mass spectroscopic techniques for the analysis of dynamic changes of histone modifications. Proteomics4(5), 1382–1396 (2004).
  • Plazas-Mayorca MD, Zee BM, Young NL et al. One-pot shotgun quantitative mass spectrometry characterization of histones. J. Proteome Res.8(11), 5367–5374 (2009).
  • Robin P, Fritsch L, Philipot O, Svinarchuk F, Ait-Si-Ali S. Post-translational modifications of histones H3 and H4 associated with the histone methyltransferases Suv39h1 and G9a. Genome Biol.8(12), R270 (2007).
  • Drogaris P, Wurtele H, Masumoto H, Verreault A, Thibault P. Comprehensive profiling of histone modifications using a label-free approach and its applications in determining structure–function relationships. Anal. Chem.80(17), 6698–6707 (2008).
  • Peters AH, Kubicek S, Mechtler K et al. Partitioning and plasticity of repressive histone methylation states in mammalian chromatin. Mol. Cell.12(6), 1577–1589 (2003).
  • Chen X, Xiong J, Xu M, Chen S, Zhu B. Symmetrical modification within a nucleosome is not required globally for histone lysine methylation. EMBO Rep.12(3), 244–251 (2011).
  • Mandava V, Fernandez JP, Deng H, Janzen CJ, Hake SB, Cross GA. Histone modifications in Trypanosoma brucei. Mol. Biochem. Parasitol.156(1), 41–50 (2007).
  • Kapoor A, Goldberg MS, Cumberland LK et al. The histone variant macroH2A suppresses melanoma progression through regulation of CDK8. Nature468(7327), 1105–1109 (2010).
  • Ouvry-Patat SA, Schey KL. Characterization of antimicrobial histone sequences and posttranslational modifications by mass spectrometry. J. Mass Spectrom.42(5), 664–674 (2007).
  • Plazas-Mayorca MD, Bloom JS, Zeissler U et al. Quantitative proteomics reveals direct and indirect alterations in the histone code following methyltransferase knockdown. Mol. Biosyst.6(9), 1719–1729 (2010).
  • Ong SE, Blagoev B, Kratchmarova I et al. Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics1(5), 376–386 (2002).
  • Pimienta G, Chaerkady R, Pandey A. SILAC for global phosphoproteomic analysis. Methods Mol. Biol.527, 107–116, x (2009).
  • Bonenfant D, Towbin H, Coulot M, Schindler P, Mueller DR, van Oostrum J. Analysis of dynamic changes in post-translational modifications of human histones during cell cycle by mass spectrometry. Mol. Cell. Proteomics6(11), 1917–1932 (2007).
  • Pesavento JJ, Yang H, Kelleher NL, Mizzen CA. Certain and progressive methylation of histone H4 at lysine 20 during the cell cycle. Mol. Cell. Biol.28(1), 468–486 (2008).
  • Jung HR, Pasini D, Helin K, Jensen ON. 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. Proteomics9(5), 838–850 (2010).
  • Cuomo A, Moretti S, Minucci S, Bonaldi T. SILAC-based proteomic analysis to dissect the ‘histone modification signature’ of human breast cancer cells. Amino Acids41(2), 387–399 (2011).
  • Zee BM, Levin RS, Dimaggio PA, Garcia BA. Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin.3(1), 22 (2010).
  • Scharf AN, Barth TK, Imhof A. Establishment of histone modifications after chromatin assembly. Nucleic Acids Res.37(15), 5032–5040 (2009).
  • Xu M, Long C, Chen X, Huang C, Chen S, Zhu B. Partitioning of histone H3–H4 tetramers during DNA replication-dependent chromatin assembly. Science328(5974), 94–98 (2010).
  • Ong SE, Mittler G, Mann M. Identifying and quantifying in vivo methylation sites by heavy methyl SILAC. Nat. Methods1(2), 119–126 (2004).
  • Fodor BD, Kubicek S, Yonezawa M et al. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev.20(12), 1557–1562 (2006).
  • Zee BM, Levin RS, Xu B, LeRoy G, Wingreen NS, Garcia BA. In vivo residue-specific histone methylation dynamics. J. Biol. Chem.285(5), 3341–3350 (2010).
  • Sweet SM, Li M, Thomas PM, Durbin KR, Kelleher NL. Kinetics of re-establishing H3K79 methylation marks in global human chromatin. J. Biol. Chem.285(43), 32778–32786 (2010).
  • Young NL, Plazas-Mayorca MD, Garcia BA. Systems-wide proteomic characterization of combinatorial post-translational modification patterns. Expert Rev. Proteomics7(1), 79–92 (2010).
  • Pesavento JJ, Kim YB, Taylor GK, Kelleher NL. Shotgun annotation of histone modifications: a new approach for streamlined characterization of proteins by top down mass spectrometry. J. Am. Chem. Soc.126(11), 3386–3387 (2004).
  • Medzihradszky KF, Zhang X, Chalkley RJ et al. Characterization of Tetrahymena histone H2B variants and posttranslational populations by electron capture dissociation (ECD) Fourier transform ion cyclotron mass spectrometry (FT-ICR MS). Mol. Cell. Proteomics3(9), 872–886 (2004).
  • Syka JE, Coon JJ, Schroeder MJ, Shabanowitz J, Hunt DF. Peptide and protein sequence analysis by electron transfer dissociation mass spectrometry. Proc. Natl Acad. Sci. USA101(26), 9528–9533 (2004).
  • Coon JJ, Ueberheide B, Syka JE et al. Protein identification using sequential ion/ion reactions and tandem mass spectrometry. Proc. Natl Acad. Sci. USA102(27), 9463–9468 (2005).
  • Pesavento JJ, Bullock CR, LeDuc RD, Mizzen CA, Kelleher NL. Combinatorial modification of human histone H4 quantitated by two-dimensional liquid chromatography coupled with top down mass spectrometry. J. Biol. Chem.283(22), 14927–14937 (2008).
  • Phanstiel D, Brumbaugh J, Berggren WT et al. Mass spectrometry identifies and quantifies 74 unique histone H4 isoforms in differentiating human embryonic stem cells. Proc. Natl Acad. Sci. USA105(11), 4093–4098 (2008).
  • Garcia BA. What does the future hold for top down mass spectrometry? J. Am. Soc. Mass Spectrom.21(2), 193–202 (2010).
  • Garcia BA, Pesavento JJ, Mizzen CA, Kelleher NL. Pervasive combinatorial modification of histone H3 in human cells. Nat. Methods4(6), 487–489 (2007).
  • 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. Proteomics1(7), 500–508 (2002).
  • Zhang K, Siino JS, Jones PR, Yau PM, Bradbury EM. A mass spectrometric ‘Western blot’ to evaluate the correlations between histone methylation and histone acetylation. Proteomics4(12), 3765–3775 (2004).
  • Young NL, DiMaggio PA, Plazas-Mayorca MD, Baliban RC, Floudas CA, Garcia BA. High throughput characterization of combinatorial histone codes. Mol. Cell. Proteomics8(10), 2266–2284 (2009).
  • 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. USA104(7), 2086–2091 (2007).
  • Garcia BA, Joshi S, Thomas CE et al. Comprehensive phosphoprotein analysis of linker histone H1 from Tetrahymena thermophila. Mol. Cell. Proteomics5(9), 1593–1609 (2006).
  • DiMaggio PA Jr, Young NL, Baliban RC, Garcia BA, Floudas CA. 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. Proteomics8(11), 2527–2543 (2009).
  • Guan S, Burlingame AL. Data processing algorithms for analysis of high resolution MSMS spectra of peptides with complex patterns of posttranslational modifications. Mol. Cell. Proteomics9(5), 804–810 (2010).
  • Frank AM, Pesavento JJ, Mizzen CA, Kelleher NL, Pevzner PA. Interpreting top-down mass spectra using spectral alignment. Anal. Chem.80(7), 2499–2505 (2008).
  • Talbert PB, Henikoff S. Histone variants – ancient wrap artists of the epigenome. Nat. Rev. Mol. Cell Biol.11(4), 264–275 (2010).
  • Bergmuller E, Gehrig PM, Gruissem W. Characterization of post-translational modifications of histone H2B-variants isolated from Arabidopsis thaliana. J. Proteome Res.6(9), 3655–3668 (2007).
  • Wiedemann SM, Mildner SN, Bonisch C et al. Identification and characterization of two novel primate-specific histone H3 variants, H3.X and H3.Y. J. Cell. Biol.190(5), 777–791 (2010).
  • Bonenfant D, Coulot M, Towbin H, Schindler P, van Oostrum J. Characterization of histone H2A and H2B variants and their post-translational modifications by mass spectrometry. Mol. Cell. Proteomics5(3), 541–552 (2006).
  • Chu F, Nusinow DA, Chalkley RJ, Plath K, Panning B, Burlingame AL. Mapping post-translational modifications of the histone variant macroH2A1 using tandem mass spectrometry. Mol. Cell. Proteomics5(1), 194–203 (2006).
  • Wisniewski JR, Zougman A, Kruger S, Mann M. Mass spectrometric mapping of linker histone H1 variants reveals multiple acetylations, methylations, and phosphorylation as well as differences between cell culture and tissue. Mol. Cell. Proteomics6(1), 72–87 (2007).
  • Su X, Lucas DM, Zhang L et al. Validation of an LC-MS based approach for profiling histones in chronic lymphocytic leukemia. Proteomics9(5), 1197–1206 (2009).
  • Siuti N, Roth MJ, Mizzen CA, Kelleher NL, Pesavento JJ. Gene-specific characterization of human histone H2B by electron capture dissociation. J. Proteome Res.5(2), 233–239 (2006).
  • Thomas CE, Kelleher NL, Mizzen CA. Mass spectrometric characterization of human histone H3: a bird’s eye view. J. Proteome Res.5(2), 240–247 (2006).
  • Boyne MT, 2nd, Pesavento JJ, Mizzen CA, Kelleher NL. Precise characterization of human histones in the H2A gene family by top down mass spectrometry. J. Proteome Res.5(2), 248–253 (2006).
  • Jiang L, Smith JN, Anderson SL, Ma P, Mizzen CA, Kelleher NL. Global assessment of combinatorial post-translational modification of core histones in yeast using contemporary mass spectrometry. Lys4 trimethylation correlates with degree of acetylation on the same H3 tail. J. Biol. Chem.282(38), 27923–27934 (2007).
  • Tackett AJ, Dilworth DJ, Davey MJ et al. Proteomic and genomic characterization of chromatin complexes at a boundary. J. Cell Biol.169(1), 35–47 (2005).
  • Mittler G, Butter F, Mann M. A SILAC-based DNA protein interaction screen that identifies candidate binding proteins to functional DNA elements. Genome Res.19(2), 284–293 (2009).
  • Dejardin J, Kingston RE. Purification of proteins associated with specific genomic loci. Cell136(1), 175–186 (2009).
  • Brownell JE, Zhou J, Ranalli T et al. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell84(6), 843–851 (1996).
  • Daniel JA, Pray-Grant MG, Grant PA. Effector proteins for methylated histones: an expanding family. Cell Cycle4(7), 919–926 (2005).
  • Lachner M, O’Carroll D, Rea S, Mechtler K, Jenuwein T. Methylation of histone H3 lysine 9 creates a binding site for HP1 proteins. Nature410(6824), 116–120 (2001).
  • LeRoy G, Rickards B, Flint SJ. The double bromodomain proteins Brd2 and Brd3 couple histone acetylation to transcription. Mol. Cell.30(1), 51–60 (2008).
  • Wysocka J, Swigut T, Milne TA et al. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell121(6), 859–872 (2005).
  • Vermeulen M, Mulder KW, Denissov S et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell131(1), 58–69 (2007).
  • Vermeulen M, Eberl HC, Matarese F et al. Quantitative interaction proteomics and genome-wide profiling of epigenetic histone marks and their readers. Cell142(6), 967–980 (2010).
  • Chan DW, Wang Y, Wu M, Wong J, Qin J, Zhao Y. Unbiased proteomic screen for binding proteins to modified lysines on histone H3. Proteomics9(9), 2343–2354 (2009).
  • Bua DJ, Kuo AJ, Cheung P et al. Epigenome microarray platform for proteome-wide dissection of chromatin-signaling networks. PLoS One4(8), e6789 (2009).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Order Reprints Request Corporate Permissions

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

Request Academic Permissions

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.

Related research

People also read lists articles that other readers of this article have read.

Recommended articles lists articles that we recommend and is powered by our AI driven recommendation engine.

Cited by lists all citing articles based on Crossref citations.
Articles with the Crossref icon will open in a new tab.