Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose)

Nature Communications

Volumn 6, Issue , 2015, Pages

  Altmeyer, Matthias ^a,b   Neelsen, Kai J ^a   Teloni, Federico ^b   Pozdnyakova, Irina ^a   Pellegrino, Stefania ^b   Grøfte, Merete ^a   Rask, Maj Britt Druedahl ^a   Streicher, Werner ^a,c   Jungmichel, Stephanie ^a   Nielsen, Michael Lund ^a   Lukas, Jiri ^a  

^a University of Copenhagen   (Denmark)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c NOVOZYMES A S   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCINE; INTRINSICALLY DISORDERED PROTEIN; NUCLEIC ACID; POLY(ADENOSINE DIPHOSPHATE RIBOSE); PROTEIN AGGREGATE; PROTEIN;

CELLS AND CELL COMPONENTS; CRYSTAL STRUCTURE; DNA; ELECTROKINESIS; MOLECULAR ANALYSIS; NUCLEIC ACID; PHASE TRANSITION; PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL COMPARTMENTALIZATION; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; LIQUID; PHASE SEPARATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEINOSIS; STATIC ELECTRICITY; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; PHYSIOLOGY; PROTEIN CONFORMATION; PROTEIN TERTIARY STRUCTURE; TUMOR CELL LINE;

CELL LINE, TUMOR; CLONING, MOLECULAR; DNA DAMAGE; GENE EXPRESSION REGULATION; HUMANS; POLY ADENOSINE DIPHOSPHATE RIBOSE; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; PROTEINS;

EID: 84939825873     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9088     Document Type: Article

References (51)

1. Malinovska, L., Kroschwald, S., Alberti, S. Protein disorder, prion propensities, and self-organizing macromolecular collectives. Biochim. Biophys. Acta. 1834, 918-931 (2013).
2. Li, Y. R., King, O. D., Shorter, J., Gitler, A. D. Stress granules as crucibles of ALS pathogenesis. J. Cell Biol. 201, 361-372 (2013).
3. Jucker, M., Walker, L. C. Self-propagation of pathogenic protein aggregates in neurodegenerative diseases. Nature 501, 45-51 (2013).
4. Han, T. W. et al. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 149, 768-779 (2012).
5. Kato, M. et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 149, 753-767 (2012).
6. Hyman, A. A., Simons, K. Cell biology. Beyond oil and water-phase transitions in cells. Science 337, 1047-1049 (2012).
7. Weber, S. C., Brangwynne, C. P. Getting RNA and protein in phase. Cell 149, 1188-1191 (2012).
8. Hyman, A. A., Weber, C. A., Julicher, F. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30, 39-58 (2014).
9. Schwartz, J. C., Wang, X., Podell, E. R., Cech, T. R. RNA seeds higher-order assembly of FUS protein. Cell Rep. 5, 918-925 (2013).
10. Altmeyer, M. et al. The chromatin scaffold protein SAFB1 renders chromatin permissive for DNA damage signalling. Mol. Cell 52, 206-220 (2013).
11. Zhang, Q. C., Petrey, D., Garzon, J. I., Deng, L., Honig, B. PrePPI: a structureinformed database of protein-protein interactions. Nucleic Acids Res. 41, D828-D833 (2013).
12. Isabelle, M., Gagne, J. P., Gallouzi, I. E., Poirier, G. G. Quantitative proteomics and dynamic imaging reveal that G3BP-mediated stress granule assembly is poly(ADP-ribose)-dependent following exposure to MNNG-induced DNA alkylation. J. Cell Sci. 125, 4555-4566 (2012).
13. Nomura, T. et al. Intranuclear aggregation of mutant FUS/TLS as a molecular pathomechanism of amyotrophic lateral sclerosis. J. Biol. Chem. 289, 1192-1202 (2014).
14. Deng, Q. et al. FUS is phosphorylated by DNA-PK and accumulates in the cytoplasm after DNA damage. J. Neurosci. 34, 7802-7813 (2014).
15. Rulten, S. L. et al. PARP-1 dependent recruitment of the amyotrophic lateral sclerosis-associated protein FUS/TLS to sites of oxidative DNA damage. Nucleic Acids Res. 42, 307-314 (2014).
16. Wang, W. Y. et al. Interaction of FUS and HDAC1 regulates DNA damage response and repair in neurons. Nat. Neurosci. 16, 1383-1391 (2013).
17. Mastrocola, A. S., Kim, S. H., Trinh, A. T., Rodenkirch, L. A., Tibbetts, R. S. The RNA-binding protein fused in sarcoma (FUS) functions downstream of poly(ADP-ribose) polymerase (PARP) in response to DNA damage. J. Biol. Chem. 288, 24731-24741 (2013).
18. Sama, R. R., Ward, C. L., Bosco, D. A. Functions of FUS/TLS from DNA repair to stress response: implications for ALS. ASN Neuro 6, doi:10.1177/1759091414544472 (2014).
19. Rouleau, M., Patel, A., Hendzel, M. J., Kaufmann, S. H., Poirier, G. G. PARP inhibition: PARP1 and beyond. Nat. Rev. Cancer. 10, 293-301 (2010).
20. Bekker-Jensen, S. et al. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J. Cell Biol. 173, 195-206 (2006).
21. Kwon, I. et al. Phosphorylation-regulated binding of RNA polymerase II to fibrous polymers of low-complexity domains. Cell 155, 1049-1060 (2013).
22. Banjade, S., Rosen, M. K. Phase transitions of multivalent proteins can promote clustering of membrane receptors. ELife 3, doi:10.7554/eLife.04123 (2014).
23. Hong, Z. et al. The role of hnRPUL1 involved in DNA damage response is related to PARP1. PLoS ONE 8, e60208 (2013).
24. Polo, S. E. et al. Regulation of DNA-end resection by hnRNPU-like proteins promotes DNA double-strand break signalling and repair. Mol. Cell 45, 505-516 (2012).
25. Lukas, C. et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13, 243-253 (2011).
26. Toretsky, J. A., Wright, P. E. Assemblages: functional units formed by cellular phase separation. J. Cell Biol. 206, 579-588 (2014).
27. Kim, H. J. et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 495, 467-473 (2013).
28. Leung, A. K. Poly(ADP-ribose): An organizer of cellular architecture. J. Cell Biol. 205, 613-619 (2014).
29. Leung, A. K. et al. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 42, 489-499 (2011).
30. Reijns, M. A., Alexander, R. D., Spiller, M. P., Beggs, J. D. A role for Q/N-rich aggregation-prone regions in P-body localization. J. Cell Sci. 121, 2463-2472 (2008).
31. Brangwynne, C. P. et al. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324, 1729-1732 (2009).
32. Ciryam, P., Tartaglia, G. G., Morimoto, R. I., Dobson, C. M., Vendruscolo, M. Widespread aggregation and neurodegenerative diseases are associated with supersaturated proteins. Cell Rep. 5, 781-790 (2013).
33. Altmeyer, M., Lukas, J. Guarding against collateral damage during chromatin transactions. Cell 153, 1431-1434 (2013).
34. Panier, S., Durocher, D. Push back to respond better: regulatory inhibition of the DNA double-strand break response. Nat. Rev. Mol. Cell Biol. 14, 661-672 (2013).
35. Kwon, I. et al. Poly-dipeptides encoded by the C9ORF72 repeats bind nucleoli, impede RNA biogenesis, and kill cells. Science 345, 1139-1145 (2014).
36. Li, P. et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 483, 336-340 (2012).
37. Wippich, F. et al. Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell 152, 791-805 (2013).
38. Beli, P. et al. Proteomic investigations reveal a role for RNA processing factor THRAP3 in the DNA damage response. Mol. Cell 46, 212-225 (2012).
39. Britton, S. et al. DNA damage triggers SAF-A and RNA biogenesis factors exclusion from chromatin coupled to R-loops removal. Nucleic Acids Res. 42, 9047-9062 (2014).
40. Shanbhag, N. M., Rafalska-Metcalf, I. U., Balane-Bolivar, C., Janicki, S. M., Greenberg, R. A. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970-981 (2010).
41. Khurana, S. et al. A macrohistone variant links dynamic chromatin compaction to BRCA1-dependent genome maintenance. Cell Rep. 8, 1049-1062 (2014).
42. Jungmichel, S. et al. Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses. Mol. Cell 52, 272-285 (2013).
43. Garnett, M. J. et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 483, 570-575 (2012).
44. Lee, H. J. et al. Combining PARP-1 inhibition and radiation in Ewing sarcoma results in lethal DNA damage. Mol. Cancer Ther. 12, 2591-2600 (2013).
45. Hicks, G. G. et al. Fus deficiency in mice results in defective B-lymphocyte development and activation, high levels of chromosomal instability and perinatal death. Nat. Genet. 24, 175-179 (2000).
46. Mandir, A. S. et al. Poly(ADP-ribose) polymerase activation mediates 1-methyl-4-phenyl-1, 2,3,6-tetrahydropyridine (MPTP)-induced parkinsonism. Proc. Natl Acad. Sci. USA 96, 5774-5779 (1999).
47. Outeiro, T. F. et al. Pharmacological inhibition of PARP-1 reduces alpha-synuclein-and MPP\+-induced cytotoxicity in Parkinson's disease in vitro models. Biochem. Biophys. Res. Commun. 357, 596-602 (2007).
48. Hanai, S. et al. Loss of poly(ADP-ribose) glycohydrolase causes progressive neurodegeneration in Drosophila melanogaster. Proc. Natl Acad. Sci. USA 101, 82-86 (2004).
49. Thandapani, P., O'Connor, T. R., Bailey, T. L., Richard, S. Defining the RGG/RG motif. Mol. Cell 50, 613-623 (2013).
50. Gudjonsson, T. et al. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150, 697-709 (2012).
51. Toledo, L. I. et al. ATR prohibits replication catastrophe by preventing global exhaustion of RPA. Cell 155, 1088-1103 (2013).