Histone serotonylation is a permissive modification that enhances TFIID binding to H3K4me3

Nature

Volumn 567, Issue 7749, 2019, Pages 535-539

  Farrelly, Lorna A ^a   Thompson, Robert E ^b   Zhao, Shuai ^c,d   Lepack, Ashley E ^a   Lyu, Yang ^a   Bhanu, Natarajan V ^e   Zhang, Baichao ^c,d   Loh, Yong Hwee E ^a   Ramakrishnan, Aarthi ^a   Vadodaria, Krishna C ^f   Heard, Kelly J ^f   Erikson, Galina ^f   Nakadai, Tomoyoshi ^g   Bastle, Ryan M ^a   Lukasak, Bradley J ^b   Zebroski, Henry ^g   Alenina, Natalia ^h   Bader, Michael ^h   Berton, Olivier ^a   Roeder, Robert G ^g   Molina, Henrik ^g   Gage, Fred H ^f   Shen, Li ^a   Garcia, Benjamin A ^e   Li, Haitao ^c,d   Muir, Tom W ^b   Maze, Ian ^a   more..

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b PRINCETON UNIVERSITY   (United States)

^c Tsinghua University   (China)

^d TSINGHUA UNIVERSITY   (China)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^g ROCKEFELLER UNIVERSITY   (United States)

^h MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMINE; HISTONE H3; HISTONE H3 TRI METHYLATED LYSINE 4; LYSINE; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; SEROTONIN; TRANSCRIPTION FACTOR IID; UNCLASSIFIED DRUG; GUANINE NUCLEOTIDE BINDING PROTEIN; HISTONE; HISTONE H3 TRIMETHYL LYS4; PROTEIN BINDING; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; BRAIN; CELL CULTURE; CHEMICAL MODIFICATION; CONTROLLED STUDY; CORRELATIONAL STUDY; EMBRYO; EUCHROMATIN; FEMALE; GENE EXPRESSION; GENOME-WIDE ASSOCIATION STUDY; HUMAN; HUMAN CELL; IN VIVO STUDY; INTESTINE; LETTER; MALE; MAMMAL; NERVE CELL DIFFERENTIATION; NEUROTRANSMISSION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SEROTONINERGIC NERVE CELL; SEROTONYLATION; YOUNG ADULT; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL LINE; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; METABOLISM; METHYLATION; MOUSE;

MAMMALIA;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; FEMALE; GENE EXPRESSION REGULATION; GLUTAMINE; GTP-BINDING PROTEINS; HISTONES; HUMANS; LYSINE; METHYLATION; MICE; MICE, INBRED C57BL; PROTEIN BINDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEROTONERGIC NEURONS; SEROTONIN; TRANSCRIPTION FACTOR TFIID; TRANSGLUTAMINASES;

EID: 85063402494     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/s41586-019-1024-7     Document Type: Article

References (49)

1. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693–705 (2007).
2. Jenuwein, T. & Allis, C. D. Translating the histone code. Science 293, 1074–1080 (2001).
3. Strahl, B. D. & Allis, C. D. The language of covalent histone modifications. Nature 403, 41–45 (2000).
4. Lauberth, S. M. et al. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 152, 1021–1036 (2013).
5. Vermeulen, M. et al. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131, 58–69 (2007).
6. van Ingen, H. et al. Structural insight into the recognition of the H3K4me3 mark by the TFIID subunit TAF3. Structure 16, 1245–1256 (2008).
7. Colgan, L. A., Putzier, I. & Levitan, E. S. Activity-dependent vesicular monoamine transporter-mediated depletion of the nucleus supports somatic release by serotonin neurons. J. Neurosci. 29, 15878–15887 (2009).
8. Young, A. B., Pert, C. D., Brown, D. G., Taylor, K. M. & Snyder, S. H. Nuclear localization of histamine in neonatal rat brain. Science 173, 247–249 (1971).
9. Walther, D. J. et al. Serotonylation of small GTPases is a signal transduction pathway that triggers platelet α-granule release. Cell 115, 851–862 (2003).
10. Watts, S. W., Priestley, J. R. & Thompson, J. M. Serotonylation of vascular proteins important to contraction. PLoS ONE 4, e5682 (2009).
11. Hummerich, R., Thumfart, J. O., Findeisen, P., Bartsch, D. & Schloss, P. Transglutaminase-mediated transamidation of serotonin, dopamine and noradrenaline to fibronectin: evidence for a general mechanism of monoaminylation. FEBS Lett. 586, 3421–3428 (2012).
12. Ballestar, E., Abad, C. & Franco, L. Core histones are glutaminyl substrates for tissue transglutaminase. J. Biol. Chem. 271, 18817–18824 (1996).
13. Kim, J. H. et al. Histone cross-linking by transglutaminase. Biochem. Biophys. Res. Commun. 293, 1453–1457 (2002).
14. Sileno, S. et al. A possible role of transglutaminase 2 in the nucleus of INS-1E and of cells of human pancreatic islets. J. Proteomics 96, 314–327 (2014).
15. Lin, J. C. et al. Characterization of protein serotonylation via bioorthogonal labeling and enrichment. J. Proteome Res. 13, 3523–3529 (2014).
16. Nurminskaya, M. V. & Belkin, A. M. Cellular functions of tissue transglutaminase. Int. Rev. Cell Mol. Biol. 294, 1–97 (2012).
17. Hummerich, R., Costina, V., Findeisen, P. & Schloss, P. Monoaminylation of fibrinogen and glia-derived proteins: indication for similar mechanisms in posttranslational protein modification in blood and brain. ACS Chem. Neurosci. 6, 1130–1136 (2015).
18. Lu, J. et al. Generation of serotonin neurons from human pluripotent stem cells. Nat. Biotechnol. 34, 89–94 (2016).
19. Shen, L. et al. diffReps: detecting differential chromatin modification sites from ChIP-seq data with biological replicates. PLoS ONE 8, e65598 (2013).
20. Chen, E. Y. et al. Enrichr: interactive and collaborative HTML5 gene list enrichment analysis tool. BMC Bioinformatics 14, 128 (2013).
21. Kuleshov, M. V. et al. Enrichr: a comprehensive gene set enrichment analysis web server 2016 update. Nucleic Acids Res. 44 (W1), 90–97 (2016).
22. Daubert, E. A. & Condron, B. G. Serotonin: a regulator of neuronal morphology and circuitry. Trends Neurosci. 33, 424–434 (2010).
23. White, L. A. et al. Distinct regulatory pathways control neurofilament expression and neurotransmitter synthesis in immortalized serotonergic neurons. J. Neurosci. 14, 6744–6753 (1994).
24. Maze, I. et al. Critical role of histone turnover in neuronal transcription and plasticity. Neuron 87, 77–94 (2015).
25. Tessarz, P. et al. Glutamine methylation in histone H2A is an RNA-polymerase-I-dedicated modification. Nature 505, 564–568 (2014).
26. Eaton, M. J. & Whittemore, S. R. Autocrine BDNF secretion enhances the survival and serotonergic differentiation of raphe neuronal precursor cells grafted into the adult rat CNS. Exp. Neurol. 140, 105–114 (1996).
27. Ollivier, N. et al. Tidbits for the synthesis of bis(2-sulfanylethyl)amido (SEA) polystyrene resin, SEA peptides and peptide thioesters. J. Pept. Sci. 20, 92–97 (2014).
28. Dann, G. P. et al. ISWI chromatin remodellers sense nucleosome modifications to determine substrate preference. Nature 548, 607–611 (2017).
29. Nguyen, U. T. et al. Accelerated chromatin biochemistry using DNA-barcoded nucleosome libraries. Nat. Methods 11, 834–840 (2014).
30. Simon, M. D. & Shokat, K. M. A method to site-specifically incorporate methyl-lysine analogues into recombinant proteins. Methods Enzymol. 512, 57–69 (2012).
31. Debelouchina, G. T., Gerecht, K. & Muir, T. W. Ubiquitin utilizes an acidic surface patch to alter chromatin structure. Nat. Chem. Biol. 13, 105–110 (2017).
32. Lowary, P. T. & Widom, J. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276, 19–42 (1998).
33. Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23–44 (2004).
34. Wojcik, F. et al. Functional crosstalk between histone H2B ubiquitylation and H2A modifications and variants. Nat. Commun. 9, 1394 (2018).
35. Peterson, A. C., Russell, J. D., Bailey, D. J., Westphall, M. S. & Coon, J. J. Parallel reaction monitoring for high resolution and high mass accuracy quantitative, targeted proteomics. Mol. Cell. Proteomics 11, 1475–1488 (2012).
36. Dignam, J. D., Lebovitz, R. M. & Roeder, R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475–1489 (1983).
37. Rappsilber, J., Mann, M. & Ishihama, Y. Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips. Nat. Protoc. 2, 1896–1906 (2007).
38. Cox, J. et al. Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ. Mol. Cell. Proteomics 13, 2513–2526 (2014).
39. Käll, L., Canterbury, J. D., Weston, J., Noble, W. S. & MacCoss, M. J. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 4, 923–925 (2007).
40. Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).
41. Schwanhäusser, B. et al. Global quantification of mammalian gene expression control. Nature 473, 337–342 (2011).
42. Sidoli, S., Bhanu, N. V., Karch, K. R., Wang, X. & Garcia, B. A. Complete workflow for analysis of histone post-translational modifications using bottom-up mass spectrometry: from histone extraction to data analysis. J. Vis. Exp. 17, e54112 (2016).
43. Tsankova, N. M. et al. Sustained hippocampal chromatin regulation in a mouse model of depression and antidepressant action. Nat. Neurosci. 9, 519–525 (2006).
44. Zhang, Y. et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9, R137 (2008).
45. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105–1111 (2009).
46. Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
47. Gundemir, S. & Johnson, G. V. Intracellular localization and conformational state of transglutaminase 2: implications for cell death. PLoS ONE 4, e6123 (2009).
48. Vizcaíno, J. A. et al. A guide to the Proteomics Identifications Database proteomics data repository. Proteomics 9, 4276–4283 (2009).
49. Vizcaíno, J. A. et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 44 (D1), D447–D456 (2016).