An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action

Nature Medicine

Volumn 20, Issue 8, 2014, Pages 919-926

  Gibbs, Julie ^a   Ince, Louise ^b   Matthews, Laura ^a   Mei, Junjie ^c   Bell, Thomas ^b   Yang, Nan ^a   Saer, Ben ^b   Begley, Nicola ^b   Poolman, Toryn ^a   Pariollaud, Marie ^a   Farrow, Stuart ^a,d   Demayo, Francesco ^e   Hussell, Tracy ^b   Worthen, G Scott ^c   Ray, David ^a   Loudon, Andrew ^b  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d GLAXOSMITHKLINE   (United Kingdom)

^e BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CELLS, CULTURED; CHEMOKINE CXCL5; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; DEXAMETHASONE; EPITHELIAL CELLS; GLUCOCORTICOIDS; HUMANS; LIPOPOLYSACCHARIDES; LUNG; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NEUTROPHIL INFILTRATION; NEUTROPHILS; PERIOD CIRCADIAN PROTEINS; PNEUMONIA, PNEUMOCOCCAL; RECEPTORS, GLUCOCORTICOID; STREPTOCOCCUS PNEUMONIAE; UTEROGLOBIN;

EID: 84905727517     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3599     Document Type: Article

References (50)

1. Martinez, F.J., Donohue, J.F. & Rennard, S.I. The future of chronic obstructive pulmonary disease treatment-difficulties of and barriers to drug development. Lancet 378, 1027-1037 (2011).
2. Scheiermann, C. et al. Adrenergic nerves govern circadian leukocyte recruitment to tissues. Immunity 37, 290-301 (2012).
3. Scheiermann, C., Kunisaki, Y. & Frenette, P.S. Circadian control of the immune system. Nat. Rev. Immunol. 13, 190-198 (2013).
4. Keller, M. et al. A circadian clock in macrophages controls inflammatory immune responses. Proc. Natl. Acad. Sci. USA 106, 21407-21412 (2009).
5. Gibbs, J.E. et al. The nuclear receptor REV-ERBα mediates circadian regulation of innate immunity through selective regulation of inflammatory cytokines. Proc. Natl. Acad. Sci. USA 109, 582-587 (2012).
6. Wang, X., Reece, S.P., Van Scott, M.R. & Brown, J.M. A circadian clock in murine bone marrow-derived mast cells modulates IgE-dependent activation in vitro. Brain Behav. Immun. 25, 127-134 (2011).
7. Shackelford, P.G. & Feigin, R.D. Periodicity of susceptibility to pneumococcal infection: Influence of light and adrenocortical secretions. Science 182, 285-287 (1973).
8. Silver, A.C., Arjona, A., Walker, W.E. & Fikrig, E. The circadian clock controls Toll-like receptor 9-mediated innate and adaptive immunity. Immunity 36, 251-261 (2012).
9. Halberg, F., Johnson, N.E.A., Brown, B.W. & Bittner, J.J. Susceptibility rhythm to E. coli endotoxin and bioassay. Proc. Soc. Exp. Biol. Med. 103, 142-144 (1960).
10. Castanon-Cervantes, O. et al. Dysregulation of inflammatory responses by chronic circadian disruption. J. Immunol. 185, 5796-5805 (2010).
11. Bellet, M.M. et al. Circadian clock regulates the host response to Salmonella. Proc. Natl. Acad. Sci. USA 110, 9897-9902 (2013).
12. Witko-Sarsat, V., Rieu, P., Descamps-Latscha, B., Lesavre, P. & Halbwachs-Mecarelli, L. Neutrophils: Molecules, functions and pathophysiological aspects. Lab. Invest. 80, 617-653 (2000).
13. Perkins, N.D. Integrating cell-signalling pathways with NF-κB and IKK function. Nat. Rev. Mol. Cell Biol. 8, 49-62 (2007). (Pubitemid 46012014)
14. Ota, T., Fustin, J.M., Yamada, H., Doi, M. & Okamura, H. Circadian clock signals in the adrenal cortex. Mol. Cell. Endocrinol. 349, 30-37 (2012).
15. Dickmeis, T. Glucocorticoids and the circadian clock. J. Endocrinol. 200, 3-22 (2009).
16. Nader, N., Chrousos, G.P. & Kino, T. Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: Potential physiological implications. FASEB J. 23, 1572-1583 (2009).
17. Lamia, K.A. et al. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 480, 552-556 (2011).
18. Han, D.H., Lee, Y.J., Kim, K., Kim, C.J. & Cho, S. Modulation of glucocorticoid receptor induction properties by core circadian clock proteins. Mol. Cell. Endocrinol. 383, 170-180 (2014).
19. Aschoff, J. in Circadian Clocks (ed. Aschoff, J.) 95-111 (Amsterdam, North-Holland, 1965).
20. Paladino, N., Leone, M.J., Plano, S.A. & Golombek, D.A. Paying the circadian toll: The circadian response to LPS injection is dependent on the Toll-like receptor 4. J. Neuroimmunol. 225, 62-67 (2010).
21. Kadioglu, A. et al. Host cellular immune response to pneumococcal lung infection in mice. Infect. Immun. 68, 492-501 (2000). (Pubitemid 30056499)
22. Yoo, S.H. et al. PERIOD2:LUCIFERASE real-time reporting of circadian dynamics reveals persistent circadian oscillations in mouse peripheral tissues. Proc. Natl. Acad. Sci. USA 101, 5339-5346 (2004).
23. Elizur, A. et al. Clara cells impact the pulmonary innate immune response to LPS. Am. J. Physiol. Lung Cell. Mol. Physiol. 293, L383-L392 (2007). (Pubitemid 47205019)
24. Hirota, T. et al. Identification of small molecule activators of cryptochrome. Science 337, 1094-1097 (2012).
25. Gibbs, J.E. et al. Circadian timing in the lung; a specific role for bronchiolar epithelial cells. Endocrinology 150, 268-276 (2009).
26. Li, S. et al. Foxp1/4 control epithelial cell fate during lung development and regeneration through regulation of anterior gradient 2. Development 139, 2500-2509 (2012).
27. Guilding, C. et al. Suppressed cellular oscillations in after-hours mutant mice are associated with enhanced circadian phase-resetting. J. Physiol. (Lond.) 591, 1063-1080 (2013).
28. Jeyaseelan, S. et al. Induction of CXCL5 during inflammation in the rodent lung involves activation of alveolar epithelium. Am. J. Respir. Cell Mol. Biol. 32, 531-539 (2005). (Pubitemid 40770131)
29. Mei, J. et al. CXCL5 regulates chemokine scavenging and pulmonary host defense to bacterial infection. Immunity 33, 106-117 (2010).
30. John, S. et al. Interaction of the glucocorticoid receptor with the chromatin landscape. Mol. Cell 29, 611-624 (2008). (Pubitemid 351374691)
31. Dalm, S., Brinks, V., van der Mark, M.H., de Kloet, E.R. & Oitzl, M.S. Non-invasive stress-free application of glucocorticoid ligands in mice. J. Neurosci. Methods 170, 77-84 (2008).
32. The ENCODE Project Consortium. et al. An integrated encyclopedia of DNA elements in the human genome. Nature 489, 57-74 (2012).
33. Vyas, S. et al. Insights into negative regulation by the glucocorticoid receptor from genome-wide profiling of inflammatory cistromes. Mol. Cell 49, 1-3 (2013).
34. Grommes, J. & Soehnlein, O. Contribution of neutrophils to acute lung injury. Mol. Med. 17, 293-307 (2011).
35. Nakagome, K., Matsushita, S. & Nagata, M. Neutrophilic inflammation in severe asthma. Int. Arch. Allergy Immunol. 158 (suppl. 1) 96-102 (2012).
36. Quint, J.K. & Wedzicha, J.A. The neutrophil in chronic obstructive pulmonary disease. J. Allergy Clin. Immunol. 119, 1065-1071 (2007). (Pubitemid 46654162)
37. Eash, K.J., Greenbaum, A.M., Gopalan, P.K. & Link, D.C. CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J. Clin. Invest. 120, 2423-2431 (2010).
38. Suratt, B.T. et al. Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood 104, 565-571 (2004). (Pubitemid 38900043)
39. Kobayashi, Y. Neutrophil infiltration and chemokines. Crit. Rev. Immunol. 26, 307-316 (2006).
40. Mei, J. et al. Cxcr2 and Cxcl5 regulate the IL-17/G-CSF axis and neutrophil homeostasis in mice. J. Clin. Invest. 122, 974-986 (2012).
41. Tuller, T., Atar, S., Ruppin, E., Gurevich, M. & Achiron, A. Common and specific signatures of gene expression and protein-protein interactions in autoimmune diseases. Genes Immun. 14, 67-82 (2013).
42. Heit, B., Tavener, S., Raharjo, E. & Kubes, P. An intracellular signaling hierarchy determines direction of migration in opposing chemotactic gradients. J. Cell Biol. 159, 91-102 (2002). (Pubitemid 35191521)
43. Hwang, J.W., Sundar, I.K., Yao, H., Sellix, M.T. & Rahman, I. Circadian clock function is disrupted by environmental tobacco/cigarette smoke, leading to lung inflammation and injury via a SIRT1-BMAL1 pathway. FASEB J. 28, 176-194 (2014).
44. Vasu, V.T., Cross, C.E. & Gohil, K. Nr1d1, an important circadian pathway regulatory gene, is suppressed by cigarette smoke in murine lungs. Integr. Cancer Ther. 8, 321-328 (2009).
45. Smith, J.B. & Herschman, H.R. Glucocorticoid-attenuated response genes encode intercellular mediators, including a new C-X-C chemokine. J. Biol. Chem. 270, 16756-16765 (1995).
46. Li, H. et al. Cre-mediated recombination in mouse Clara cells. Genesis 46, 300-307 (2008). (Pubitemid 352008878)
47. McGrath, E.E. et al. TNF-related apoptosis-inducing ligand (TRAIL) regulates inflammatory neutrophil apoptosis and enhances resolution of inflammation. J. Leukoc. Biol. 90, 855-865 (2011).
48. Meng, Q.J. et al. Ligand modulation of REV-ERBα function resets the peripheral circadian clock in a phasic manner. J. Cell Sci. 121, 3629-3635 (2008).
49. Lee, T.I., Johnstone, S.E. & Young, R.A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 1, 729-748 (2006).
50. Okamoto, K., Onai, K. & Ishiura, M. RAP, an integrated program for monitoring bioluminescence and analyzing circadian rhythms in real time. Anal. Biochem. 340, 193-200 (2005). (Pubitemid 40544857)