Chemical tagging and customizing of cellular chromatin states using ultrafast trans-splicing inteins

Nature Chemistry

Volumn 7, Issue 5, 2015, Pages 394-402

  David, Yael ^a   Vila Perelló, Miquel ^a   Verma, Shivam ^a   Muir, Tom W ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMATIN; INTEIN;

CELL LINE; CHEMISTRY; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; HUMAN; POLYMERASE CHAIN REACTION; RNA SPLICING;

CELL LINE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; HUMANS; INTEINS; POLYMERASE CHAIN REACTION; RNA SPLICING;

EID: 84928552345     PISSN: 17554330     EISSN: 17554349     Source Type: Journal    
DOI: 10.1038/nchem.2224     Document Type: Article

References (45)

1. Badeaux, A. I. & Shi, Y. Emerging roles for chromatin as a signal integration and storage platform. Nature Rev. Mol. Cell Biol. 14, 211-224 (2013).
2. Dawson, M. A. & Kouzarides, T. Cancer epigenetics: from mechanism to therapy. Cell 150, 12-27 (2012).
3. Sturm, D. et al. Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge. Nature Rev. Cancer 14, 92-107 (2014).
4. Rodriguez-Paredes, M. & Esteller, M. Cancer epigenetics reaches mainstream oncology. Nature Med. 17, 330-339 (2011).
5. Dunham, I. et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
6. Allis, C. D. & Muir, T. W. Spreading chromatin into chemical biology. ChemBioChem 12, 264-279 (2011).
7. Fierz, B. & Muir, T. W. Chromatin as an expansive canvas for chemical biology. Nature Chem. Biol. 8, 417-427 (2012).
8. Jiang, H. et al. Regulation of transcription by the MLL2 complex and MLL complex-associated AKAP95. Nature Struct. Mol. Biol. 20, 1156-1163 (2013).
9. Ernst, J. & Kellis, M. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nature Biotechnol. 28, 817-825 (2010).
10. Cole, P. A. Chemical probes for histone-modifying enzymes. Nature Chem. Biol. 4, 590-597 (2008).
11. Iwasaki, W. et al. Comprehensive structural analysis of mutant nucleosomes containing lysine to glutamine (KQ) substitutions in the H3 and H4 histone-fold domains. Biochemistry 50, 7822-7832 (2011).
12. Shah, N. H., Dann, G. P., Vila-Perello, M., Liu, Z. & Muir, T.W. Ultrafast protein splicing is common among cyanobacterial split inteins: implications for protein engineering. J. Am. Chem. Soc. 134, 11338-11341 (2012).
13. Wood, D. W. & Camarero, J. A. Intein applications: from protein purification and labeling to metabolic control methods. J. Biol. Chem. 289, 14512-14519 (2014).
14. Shah, N. H. & Muir, T.W. Inteins: nature's gift to protein chemists. Chem. Sci. 5, 446-461 (2014).
15. Vila-Perello, M. et al. Streamlined expressed protein ligation using split inteins. J. Am. Chem. Soc. 135, 286-292 (2013).
16. Wadia, J. S., Stan, R. V. & Dowdy, S. F. Transducible TAT-HA fusogenic peptide enhances escape of TAT-fusion proteins after lipid raft macropinocytosis. Nature Med. 10, 310-315 (2004).
17. Giriat, I. & Muir, T. W. Protein semi-synthesis in living cells. J. Am. Chem. Soc. 125, 7180-7181 (2003).
18. Wombacher, R. et al. Live-cell super-resolution imaging with trimethoprim conjugates. Nature Methods 7, 717-719 (2010).
19. Klein, T. et al. Live-cell dSTORM with SNAP-tag fusion proteins. Nature Methods 8, 7-9 (2011).
20. Pellois, J. P., Hahn, M. E. & Muir, T. W. Simultaneous triggering of protein activity and fluorescence. J. Am. Chem. Soc. 126, 7170-7171 (2004).
21. Borra, R., Dong, D., Elnagar, A. Y., Woldemariam, G. A. & Camarero, J. A. Incell fluorescence activation and labeling of proteins mediated by FRETquenched split inteins. J. Am. Chem. Soc. 134, 6344-6353 (2012).
22. Li, B., Carey, M. & Workman, J. L. The role of chromatin during transcription. Cell 128, 707-719 (2007).
23. Woodcock, C. L. & Ghosh, R. P. Chromatin higher-order structure and dynamics. Cold Spring Harb. Perspect. Biol. 2, a000596 (2010).
24. Salina, D. et al. Cytoplasmic dynein as a facilitator of nuclear envelope breakdown. Cell 108, 97-107 (2002).
25. Voigt, P. & Reinberg, D. Histone tails: ideal motifs for probing epigenetics through chemical biology approaches. ChemBioChem 12, 236-252 (2011).
26. Fuchs, G. & Oren, M. Writing and reading H2B monoubiquitylation. Biochim. Biophys. Acta 1839, 694-701 (2014).
27. Hodgins, R. R., Ellison, K. S. & Ellison, M. J. Expression of a ubiquitin derivative that conjugates to protein irreversibly produces phenotypes consistent with a ubiquitin deficiency. J. Biol. Chem. 267, 8807-8812 (1992).
28. McGinty, R. K., Kim, J., Chatterjee, C., Roeder, R. G. & Muir, T. W. Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 453, 812-816 (2008).
29. McGinty, R. K. et al. Structure-activity analysis of semisynthetic nucleosomes: mechanistic insights into the stimulation of Dot1L by ubiquitylated histone H2B. ACS Chem. Biol. 4, 958-968 (2009).
30. Wilkins, B. J. et al. A cascade of histone modifications induces chromatin condensation in mitosis. Science 343, 77-80 (2014).
31. Matsushita, N. et al. A FancD2-monoubiquitin fusion reveals hidden functions of Fanconi anemia core complex in DNA repair. Mol. Cell 19, 841-847 (2005).
32. Vlaming, H. et al. Flexibility in crosstalk between H2B ubiquitination and H3 methylation in vivo. EMBO Rep. 15, 1220-1221 (2014).
33. Schwarze, S. R., Hruska, K. A. & Dowdy, S. F. Protein transduction: unrestricted delivery into all cells? Trends Cell Biol. 10, 290-295 (2000).
34. van den Berg, A. & Dowdy, S. F. Protein transduction domain delivery of therapeutic macromolecules. Curr. Opin. Biotechnol. 22, 888-893 (2011).
35. Erazo-Oliveras, A. et al. Protein delivery into live cells by incubation with an endosomolytic agent. Nature Methods 11, 861-867 (2014).
36. Zuris, J. A. et al. Cationic lipid-mediated delivery of proteins enables efficient protein-based genome editing in vitro and in vivo. Nature Biotechnol. 33, 73-80 (2015).
37. Musselman, C. A., Lalonde, M. E., Cote, J. & Kutateladze, T. G. Perceiving the epigenetic landscape through histone readers. Nature Struct. Mol. Biol. 19, 1218-1227 (2012).
38. Tan, M. et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146, 1016-1028 (2011).
39. Tsompana, M. & Buck, M. J. Chromatin accessibility: a window into the genome. Epigenetics Chromatin 7, 33 (2014).
40. Thurman, R. E. et al. The accessible chromatin landscape of the human genome. Nature 489, 75-82 (2012).
41. Crawford, G. E. et al. DNase-CHiP: a high-resolution method to identify DNase I hypersensitive sites using tiled microarrays. Nature Methods 3, 503-509 (2006).
42. Crawford, G. E. et al. Genome-wide mapping of DNase hypersensitive sites using massively parallel signature sequencing (MPSS). Genome Res. 16, 123-131 (2006).
43. Kanda, T., Sullivan, K. F. & Wahl, G. M. Histone-GFP fusion protein enables sensitive analysis of chromosome dynamics in living mammalian cells. Curr. Biol. 8, 377-385 (1998).
44. Sugita, T. et al. Improved cytosolic translocation and tumor-killing activity of Tat-shepherdin conjugates mediated by co-treatment with Tat-fused endosome-disruptive HA2 peptide. Biochem. Biophys. Res. Commun. 363, 1027-1032 (2007).
45. Goldberg, A. D. et al. Distinct factors control histone variant H3.3 localization at specific genomic regions. Cell 140, 678-691 (2010).