Global SUMOylation on active chromatin is an acute heat stress response restricting transcription

Genome Biology

Volumn 16, Issue 1, 2015, Pages

  Niskanen, Einari A ^a   Malinen, Marjo ^a   Sutinen, Päivi ^a   Toropainen, Sari ^a   Paakinaho, Ville ^a,d   Vihervaara, Anniina ^b,c   Joutsen, Jenny ^b,c   Kaikkonen, Minna U ^a   Sistonen, Lea ^b,c   Palvimo, Jorma J ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b ÅBO AKADEMI UNIVERSITY   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; HEAT SHOCK TRANSCRIPTION FACTOR 1; PIAS1 PROTEIN; PROTEIN INHIBITOR OF ACTIVATED STAT; PROTEIN UBC9; RNA POLYMERASE II; SUMO 2 PROTEIN; SUMO 3 PROTEIN; TRANSCRIPTION FACTOR CTCF; UNCLASSIFIED DRUG; CHROMATIN; DNA BINDING PROTEIN; HEAT SHOCK TRANSCRIPTION FACTOR; SUMO PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; BINDING SITE; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; ENHANCER REGION; GENE EXPRESSION; HEAT SHOCK RESPONSE; HEAT STRESS; HUMAN; HUMAN CELL; K562 CELL LINE; PROMOTER REGION; PROSTATE CANCER CELL LINE; SUMOYLATION; TRANSCRIPTION REGULATION; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; K-562 CELL LINE; METABOLISM; PHYSIOLOGY;

CHROMATIN; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HEAT-SHOCK RESPONSE; HUMANS; K562 CELLS; PROMOTER REGIONS, GENETIC; PROTEIN INHIBITORS OF ACTIVATED STAT; RNA POLYMERASE II; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS; SUMOYLATION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 84938749969     PISSN: 14747596     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/s13059-015-0717-y     Document Type: Article

References (53)

1. Lindquist S. The heat-shock response. Annu Rev Biochem. 1986;55:1151-91.
2. Sonna LA, Fujita J, Gaffin SL, Lilly CM. Invited review: effects of heat and cold stress on mammalian gene expression. J Appl Physiol (1985). 2002;92:1725-42.
3. Morimoto RI. Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev. 1998;12:3788-96.
4. Åkerfelt M, Morimoto RI, Sistonen L. Heat shock factors: integrators of cell stress, development and lifespan. Nat Rev Mol Cell Biol. 2010;11:545-55.
5. Flotho A, Melchior F. Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem. 2013;82:357-85.
6. Zhang FP, Mikkonen L, Toppari J, Palvimo JJ, Thesleff I, Jänne OA. Sumo-1 function is dispensable in normal mouse development. Mol Cell Biol. 2008;28:5381-90.
7. Wang L, Wansleeben C, Zhao S, Miao P, Paschen W, Yang W. SUMO2 is essential while SUMO3 is dispensable for mouse embryonic development. EMBO Rep. 2014;15:878-85.
8. Golebiowski F, Matic I, Tatham MH, Cole C, Yin Y, Nakamura A, et al. System-wide changes to SUMO modifications in response to heat shock. Sci Signal. 2009;2:ra24.
9. Hendriks IA, D'Souza RC, Yang B, Verlaan-de Vries M, Mann M, Vertegaal AC. Uncovering global SUMOylation signaling networks in a site-specific manner. Nat Struct Mol Biol. 2014;21:927-36.
10. Tammsalu T, Matic I, Jaffray EG, Ibrahim AF, Tatham MH, Hay RT. Proteome-wide identification of SUMO2 modification sites. Sci Signal. 2014;7:rs2.
11. Anckar J, Sistonen L. Heat shock factor 1 as a coordinator of stress and developmental pathways. Adv Exp Med Biol. 2007;594:78-88.
12. Rytinki M, Kaikkonen S, Sutinen P, Paakinaho V, Rahkama V, Palvimo JJ. Dynamic SUMOylation is linked to the activity cycles of androgen receptor in the cell nucleus. Mol Cell Biol. 2012;32:4195-205.
13. Paakinaho V, Kaikkonen S, Makkonen H, Benes V, Palvimo JJ. SUMOylation regulates the chromatin occupancy and anti-proliferative gene programs of glucocorticoid receptor. Nucleic Acids Res. 2014;42:1575-92.
14. Neyret-Kahn H, Benhamed M, Ye T, Le Gras S, Cossec JC, Lapaquette P, et al. Sumoylation at chromatin governs coordinated repression of a transcriptional program essential for cell growth and proliferation. Genome Res. 2013;23:1563-79.
15. Toropainen S, Malinen M, Kaikkonen S, Rytinki M, Jääskeläinen T, Sahu B, et al. SUMO ligase PIAS1 functions as a target gene selective androgen receptor coregulator on prostate cancer cell chromatin. Nucleic Acids Res. 2015;43:848-61.
16. ENCODE Project Consortium. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
17. Zhou VW, Goren A, Bernstein BE. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet. 2011;12:7-18.
18. Gerstein MB, Kundaje A, Hariharan M, Landt SG, Yan KK, Cheng C, et al. Architecture of the human regulatory network derived from ENCODE data. Nature. 2012;489:91-100.
19. Vihervaara A, Sergelius C, Vasara J, Blom MA, Elsing AN, Roos-Mattjus P, et al. Transcriptional response to stress in the dynamic chromatin environment of cycling and mitotic cells. Proc Natl Acad Sci U S A. 2013;110:E3388-97.
20. Ong CT, Corces VG. CTCF: an architectural protein bridging genome topology and function. Nat Rev Genet. 2014;15:234-46.
21. Xie D, Boyle AP, Wu L, Zhai J, Kawli T, Snyder M. Dynamic trans-acting factor colocalization in human cells. Cell. 2013;155:713-24.
22. Frietze S, O'Geen H, Blahnik KR, Jin VX, Farnham PJ. ZNF274 recruits the histone methyltransferase SETDB1 to the 3' ends of ZNF genes. PLoS One. 2010;5, e15082.
23. Heidari N, Phanstiel DH, He C, Grubert F, Jahanbani F, Kasowski M, et al. Genome-wide map of regulatory interactions in the human genome. Genome Res. 2014;24:1905-17.
24. Ivanov AV, Peng H, Yurchenko V, Yap KL, Negorev DG, Schultz DC, et al. PHD domain-mediated E3 ligase activity directs intramolecular sumoylation of an adjacent bromodomain required for gene silencing. Mol Cell. 2007;28:823-37.
25. Core LJ, Waterfall JJ, Lis JT. Nascent RNA sequencing reveals widespread pausing and divergent initiation at human promoters. Science. 2008;322:1845-8.
26. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, et al. Widespread transcription at neuronal activity-regulated enhancers. Nature. 2010;465:182-7.
27. De Santa F, Barozzi I, Mietton F, Ghisletti S, Polletti S, Tusi BK, et al. A large fraction of extragenic RNA pol II transcription sites overlap enhancers. PLoS Biol. 2010;8, e1000384.
28. Gilmour DS, Lis JT. RNA polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells. Mol Cell Biol. 1986;6:3984-9.
29. Adelman K, Lis JT. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat Rev Genet. 2012;13:720-31.
30. Bensaude O. Inhibiting eukaryotic transcription: Which compound to choose? How to evaluate its activity? Transcription. 2011;2:103-8.
31. Elsing AN, Aspelin C, Björk JK, Bergman HA, Himanen SV, Kallio MJ, et al. Expression of HSF2 decreases in mitosis to enable stress-inducible transcription and cell survival. J Cell Biol. 2014;206:735-49.
32. Siersbaek R, Rabiee A, Nielsen R, Sidoli S, Traynor S, Loft A, et al. Transcription factor cooperativity in early adipogenic hotspots and super-enhancers. Cell Rep. 2014;7:1443-55.
33. Wang J, Wang Y, Lu L. De-SUMOylation of CCCTC binding factor (CTCF) in hypoxic stress-induced human corneal epithelial cells. J Biol Chem. 2012;287:12469-79.
34. Li L, Lyu X, Hou C, Takenaka N, Nguyen HQ, Ong CT, et al. Widespread rearrangement of 3D chromatin organization underlies polycomb-mediated stress-induced silencing. Mol Cell. 2015;58:216-31.
35. Rosonina E, Duncan SM, Manley JL. SUMO functions in constitutive transcription and during activation of inducible genes in yeast. Genes Dev. 2010;24:1242-52.
36. Rosonina E, Duncan SM, Manley JL. Sumoylation of transcription factor Gcn4 facilitates its Srb10-mediated clearance from promoters in yeast. Genes Dev. 2012;26:350-5.
37. Fuda NJ, Ardehali MB, Lis JT. Defining mechanisms that regulate RNA polymerase II transcription in vivo. Nature. 2009;461:186-92.
38. Lewicki MC, Srikumar T, Johnson E, Raught B. The S. cerevisiae SUMO stress response is a conjugation-deconjugation cycle that targets the transcription machinery. J Proteomics. 2014;118:39.
39. Nayak A, Muller S. SUMO-specific proteases/isopeptidases: SENPs and beyond. Genome Biol. 2014;15:422.
40. Kaikkonen MU, Niskanen H, Romanoski CE, Kansanen E, Kivelä AM, Laitalainen J, et al. Control of VEGF-A transcriptional programs by pausing and genomic compartmentalization. Nucleic Acids Res. 2014;42:12570-84.
41. Ingolia NT, Ghaemmaghami S, Newman JR, Weissman JS. Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science. 2009;324:218-23.
42. Andrews, S. FastQC A quality control tool for high throughput sequence data. Available at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc/ .
43. Hannon Lab: FASTX Toolkit. Available at: http://hannonlab.cshl.edu/fastx_toolkit/index.html .
44. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25.
45. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576-89.
46. Schneider CA, Rasband WS, Eliceiri KW. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 2012;9:671-5.
47. Development Core Team R. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2012. Available at: http://www.R-project.org .
48. Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, et al. Integrative genomics viewer. Nat Biotechnol. 2011;29:24-6.
49. McLean CY, Bristor D, Hiller M, Clarke SL, Schaar BT, Lowe CB, et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol. 2010;28:495-501.
50. Littlefield K, Monroe M. Venn diagram plotter. Available at: http://omics.pnl.gov/software/venn-diagram-plotter .
51. Oliveros JC. VENNY. An interactive tool for comparing lists with Venn diagrams. Available at: http://bioinfogp.cnb.csic.es/tools/venny/index.html .
52. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
53. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139-40.