The transcriptional repressor Hes1 attenuates inflammation by regulating transcription elongation

Nature Immunology

Volumn 17, Issue 8, 2016, Pages 930-937

  Shang, Yingli ^a   Coppo, Maddalena ^b   He, Teng ^c   Ning, Fei ^a   Yu, Li ^a   Kang, Lan ^a   Zhang, Bin ^a   Ju, Chanyang ^b   Qiao, Yu ^b   Zhao, Baohong ^b,d   Gessler, Manfred ^e   Rogatsky, Inez ^b,d   Hu, Xiaoyu ^a,f  

^a Tsinghua University   (China)

^b HOSPITAL FOR SPECIAL SURGERY   (United States)

^c PEKING UNIVERSITY   (China)

^d WEILL CORNELL MEDICAL COLLEGE   (United States)

^e UNIVERSITY OF WÜRZBURG   (Germany)

^f TSINGHUA UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; INTERLEUKIN 12P40; INTERLEUKIN 6; MACROPHAGE DERIVED CHEMOKINE; RNA POLYMERASE II; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR HEY 1; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; CXCL1 PROTEIN, MOUSE; HES1 PROTEIN, MOUSE; HEY1 PROTEIN, MOUSE; POSITIVE TRANSCRIPTION ELONGATION FACTOR B;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; GENE DELETION; GENE EXPRESSION; GENE REPRESSION; IN VIVO STUDY; INFLAMMATION; MACROPHAGE; MOUSE; NEUTROPHIL; NONHUMAN; PERITONITIS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RHEUMATOID ARTHRITIS; TRANSCRIPTION ELONGATION; TRANSCRIPTION INITIATION; ANIMAL; ARTHRITIS; C57BL MOUSE; CELL CULTURE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MUTATION; NEUTROPHIL CHEMOTAXIS;

ANIMALS; ARTHRITIS; CELL CYCLE PROTEINS; CELLS, CULTURED; CHEMOKINE CXCL1; GENE EXPRESSION REGULATION; INFLAMMATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NEUTROPHIL INFILTRATION; POSITIVE TRANSCRIPTIONAL ELONGATION FACTOR B; RNA POLYMERASE II; TRANSCRIPTION ELONGATION, GENETIC; TRANSCRIPTION FACTOR HES-1;

EID: 84975215444     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3486     Document Type: Article

References (49)

1. Griffith J.W., Sokol C.L., & Luster A.D. Chemokines and chemokine receptors: positioning cells for host defense and immunity. Annu. Rev. Immunol. 32, 659-702 (2014).
2. Takeuchi O., & Akira S. Pattern recognition receptors and inflammation. Cell 140, 805-820 (2010).
3. Kondo T., Kawai T., & Akira S. Dissecting negative regulation of Toll-like receptor signaling. Trends Immunol. 33, 449-458 (2012).
4. Smale S.T. Selective transcription in response to an inflammatory stimulus. Cell 140, 833-844 (2010).
5. Ivashkiv L.B. Epigenetic regulation of macrophage polarization and function. Trends Immunol. 34, 216-223 (2013).
6. Rogatsky I., & Adelman K. Preparing the first responders: building the inflammatory transcriptome from the ground up. Mol. Cell 54, 245-254 (2014).
7. Kwak H., & Lis J.T. Control of transcriptional elongation. Annu. Rev. Genet. 47, 483-508 (2013).
8. Adelman K., & Lis J.T. Promoter-proximal pausing of RNA polymerase II: emerging roles in metazoans. Nat. Rev. Genet. 13, 720-731 (2012).
9. Zhou Q., Li T., & Price D.H. RNA polymerase II elongation control. Annu. Rev. Biochem. 81, 119-143 (2012).
10. Adelman K., et al. Immediate mediators of the inflammatory response are poised for gene activation through RNA polymerase II stalling. Proc. Natl. Acad. Sci. USA 106, 18207-18212 (2009).
11. Hargreaves D.C., Horng T., & Medzhitov R. Control of inducible gene expression by signal-dependent transcriptional elongation. Cell 138, 129-145 (2009).
12. Gupte R., Muse G.W., Chinenov Y., Adelman K., & Rogatsky I. Glucocorticoid receptor represses proinflammatory genes at distinct steps of the transcription cycle. Proc. Natl. Acad. Sci. USA 110, 14616-14621 (2013).
13. Kobayashi T., & Kageyama R. Expression dynamics and functions of Hes factors in development and diseases. Curr. Top. Dev. Biol. 110, 263-283 (2014).
14. Ishibashi M., et al. Targeted disruption of mammalian hairy and Enhancer of split homolog-1 (HES-1) leads to up-regulation of neural helix-loop-helix factors, premature neurogenesis, and severe neural tube defects. Genes Dev. 9, 3136-3148 (1995).
15. Hu X., et al. Integrated regulation of Toll-like receptor responses by Notch and interferon-gamma pathways. Immunity 29, 691-703 (2008).
16. Su X., et al. Interferon-γ regulates cellular metabolism and mRNA translation to potentiate macrophage activation. Nat. Immunol. 16, 838-849 (2015).
17. Alvarez Y., et al. Notch-And transducin-like enhancer of split (TLE)-dependent histone deacetylation explain interleukin 12 (IL-12) p70 inhibition by zymosan. J. Biol. Chem. 286, 16583-16595 (2011).
18. Shang Y., Smith S., & Hu X. Role of Notch signaling in regulating innate immunity and inflammation in health and disease. Protein Cell 7, 159-174 (2016).
19. Zhang W., Xu W., & Xiong S. Blockade of Notch1 signaling alleviates murine lupus via blunting macrophage activation and M2b polarization. J. Immunol. 184, 6465-6478 (2010).
20. Sodsai P., Hirankarn N., Avihingsanon Y., & Palaga T. Defects in Notch1 upregulation upon activation of T Cells from patients with systemic lupus erythematosus are related to lupus disease activity. Lupus 17, 645-653 (2008).
21. Antoniv T.T., & Ivashkiv L.B. Dysregulation of interleukin-10-dependent gene expression in rheumatoid arthritis synovial macrophages. Arthritis Rheum. 54, 2711-2721 (2006).
22. Teachey D.T., et al. Targeting Notch signaling in autoimmune and lymphoproliferative disease. Blood 111, 705-714 (2008).
23. Fischer A., Schumacher N., Maier M., Sendtner M., & Gessler M. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911 (2004).
24. Ström A., Castella P., Rockwood J., Wagner J., & Caudy M. Mediation of NGF signaling by post-Translational inhibition of HES-1, A basic helix-loop-helix repressor of neuronal differentiation. Genes Dev. 11, 3168-3181 (1997).
25. Kolaczkowska E., & Kubes P. Neutrophil recruitment and function in health and inflammation. Nat. Rev. Immunol. 13, 159-175 (2013).
26. Wipke B.T., & Allen P.M. Essential role of neutrophils in the initiation and progression of A murine model of rheumatoid arthritis. J. Immunol. 167, 1601-1608 (2001).
27. Richmond A. NF-κB, chemokine gene transcription and tumour growth. Nat. Rev. Immunol. 2, 664-674 (2002).
28. Stender J.D., & Glass C.K. Epigenomic control of the innate immune response. Curr. Opin. Pharmacol. 13, 582-587 (2013).
29. Barboric M., Nissen R.M., Kanazawa S., Jabrane-Ferrat N., & Peterlin B.M. NF-κB binds P-TEFb to stimulate transcriptional elongation by RNA polymerase II. Mol. Cell 8, 327-337 (2001).
30. Nicodeme E., et al. Suppression of inflammation by A synthetic histone mimic. Nature 468, 1119-1123 (2010).
31. Min I.M., et al. Regulating RNA polymerase pausing and transcription elongation in embryonic stem cells. Genes Dev. 25, 742-754 (2011).
32. Jonkers I., Kwak H., & Lis J.T. Genome-wide dynamics of Pol II elongation and its interplay with promoter proximal pausing, chromatin, and exons. eLife 3, e02407 (2014).
33. Saponaro M., et al. RECQL5 controls transcript elongation and suppresses genome instability associated with transcription stress. Cell 157, 1037-1049 (2014).
34. Nilson K.A., et al. THZ1 reveals roles for Cdk7 in co-Transcriptional capping and pausing. Mol. Cell 59, 576-587 (2015).
35. Williams L.H., et al. Pausing of RNA polymerase II regulates mammalian developmental potential through control of signaling networks. Mol. Cell 58, 311-322 (2015).
36. Imayoshi I., Shimogori T., Ohtsuka T., & Kageyama R. Hes genes and neurogenin regulate non-neural versus neural fate specification in the dorsal telencephalic midline. Development 135, 2531-2541 (2008).
37. Chinenov Y., et al. Role of transcriptional coregulator GRIP1 in the anti-inflammatory actions of glucocorticoids. Proc. Natl. Acad. Sci. USA 109, 11776-11781 (2012).
38. Xu H., et al. Notch-RBP-J signaling regulates the transcription factor IRF8 to promote inflammatory macrophage polarization. Nat. Immunol. 13, 642-650 (2012).
39. Swamydas M., & Lionakis M.S. Isolation, purification and labeling of mouse bone marrow neutrophils for functional studies and adoptive transfer experiments. J. Vis. Exp. 77, e50586 (2013).
40. Lima T.F., et al. Warifteine, an alkaloid purified from Cissampelos sympodialis, inhibits neutrophil migration in vitro and in vivo. J. Immunol. Res. 2014, 752923 (2014).
41. Zhang X., Goncalves R., & Mosser D.M. The isolation and characterization of murine macrophages. Curr. Protoc. Immunol. 14, 14.11 (2008).
42. De Filippo K., Henderson R.B., Laschinger M., & Hogg N. Neutrophil chemokines KC and macrophage-inflammatory protein-2 are newly synthesized by tissue macrophages using distinct TLR signaling pathways. J. Immunol. 180, 4308-4315 (2008).
43. Wongchana W., Lawlor R.G., Osborne B.A., & Palaga T. Impact of Notch1 deletion in macrophages on proinflammatory cytokine production and the outcome of experimental autoimmune encephalomyelitis. J. Immunol. 195, 5337-5346 (2015).
44. Monach P.A., Mathis D., & Benoist C. The K/BxN arthritis model. Curr. Protoc. Immunol. 15, 15.22 (2008).
45. Li S., et al. RBP-J imposes A requirement for ITAM-mediated costimulation of osteoclastogenesis. J. Clin. Invest. 124, 5057-5073 (2014).
46. Sadik C.D., Kim N.D., Iwakura Y., & Luster A.D. Neutrophils orchestrate their own recruitment in murine arthritis through C5aR and FcγR signaling. Proc. Natl. Acad. Sci. USA 109, E3177-E3185 (2012).
47. Son D.S., & Roby K.F. Interleukin-1α-induced chemokines in mouse granulosa cells: impact on keratinocyte chemoattractant chemokine A CXC subfamily. Mol. Endocrinol. 20, 2999-3013 (2006).
48. Giannopoulou E.G., & Elemento O. An integrated ChIP-seq analysis platform with customizable workflows. BMC Bioinformatics 12, 277 (2011).
49. Liao Y., Smyth G.K., & Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930 (2014).