Serum and glucocorticoid-regulated kinase 1 regulates neutrophil clearance during inflammation resolution

Journal of Immunology

Volumn 192, Issue 4, 2014, Pages 1796-1805

  Burgon, Joseph ^a   Robertson, Anne L ^a   Sadiku, Pranvera ^a   Wang, Xingang ^b   Hooper Greenhill, Edward ^c   Prince, Lynne R ^a   Walker, Paul ^d   Hoggett, Emily E ^a   Ward, Jonathan R ^a   Farrow, Stuart N ^c   Zuercher, William J ^e   Jeffrey, Philip ^c   Savage, Caroline O ^c   Ingham, Philip W ^b   Hurlstone, Adam F ^d   Whyte, Moira K B ^a   Renshaw, Stephen A ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c GLAXOSMITHKLINE   (United Kingdom)

^d UNIVERSITY OF MANCHESTER   (United Kingdom)

^e GLAXOSMITHKLINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; ANIMALS, GENETICALLY MODIFIED; APOPTOSIS; BENZOATES; BICYCLO COMPOUNDS, HETEROCYCLIC; CELL MOVEMENT; CELL SURVIVAL; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IMMEDIATE-EARLY PROTEINS; INFLAMMATION; MORPHOLINOS; NEUTROPHILS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; ZEBRAFISH;

EID: 84894273373     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300087     Document Type: Article

References (51)

1. Schleimer, R. P., H. S. Freeland, S. P. Peters, K. E. Brown, and C. P. Derse. 1989. An assessment of the effects of glucocorticoids on degranulation, chemotaxis, binding to vascular endothelium and formation of leukotriene B4 by purified human neutrophils. J. Pharmacol. Exp. Ther. 250: 598-605.
2. Liu, H., and R. M. Pope. 2004. Phagocytes: mechanisms of inflammation and tissue destruction. Rheum. Dis. Clin. North Am. 30: 19-39, v.
3. Brinkmann, V., U. Reichard, C. Goosmann, B. Fauler, Y. Uhlemann, D. S. Weiss, Y. Weinrauch, and A. Zychlinsky. 2004. Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
4. Dahlgren, C., and A. Karlsson. 1999. Respiratory burst in human neutrophils. J. Immunol. Methods 232: 3-14.
5. Serhan, C. N., and J. Savill. 2005. Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6: 1191-1197.
6. Fox, S., A. E. Leitch, R. Duffin, C. Haslett, and A. G. Rossi. 2010. Neutrophil apoptosis: relevance to the innate immune response and inflammatory disease. J. Innate Immun. 2: 216-227.
7. Vaughan, K. R., L. Stokes, L. R. Prince, H. M. Marriott, S. Meis, M. U. Kassack, C. D. Bingle, I. Sabroe, A. Surprenant, and M. K. Whyte. 2007. Inhibition of neutrophil apoptosis by ATP is mediated by the P2Y11 receptor. J. Immunol. 179: 8544-8553.
8. Lee, A., M. K. Whyte, and C. Haslett. 1993. Inhibition of apoptosis and prolongation of neutrophil functional longevity by inflammatory mediators. J. Leukoc. Biol. 54: 283-288.
9. Parker, L. C., M. K. Whyte, S. K. Dower, and I. Sabroe. 2005. The expression and roles of Toll-like receptors in the biology of the human neutrophil. J. Leukoc. Biol. 77: 886-892.
10. Hannah, S., K. Mecklenburgh, I. Rahman, G. J. Bellingan, A. Greening, C. Haslett, and E. R. Chilvers. 1995. Hypoxia prolongs neutrophil survival in vitro. FEBS Lett. 372: 233-237.
11. Brannigan, A. E., P. R. O'Connell, H. Hurley, A. O'Neill, H. R. Brady, J. M. Fitzpatrick, and R. W. Watson. 2000. Neutrophil apoptosis is delayed in patients with inflammatory bowel disease. Shock 13: 361-366.
12. Matute-Bello, G., W. C. Liles, F. Radella, II, K. P. Steinberg, J. T. Ruzinski, M. Jonas, E. Y. Chi, L. D. Hudson, and T. R. Martin. 1997. Neutrophil apoptosis in the acute respiratory distress syndrome. Am. J. Respir. Crit. Care Med. 156: 1969-1977.
13. Klein, J. B., M. J. Rane, J. A. Scherzer, P. Y. Coxon, R. Kettritz, J. M. Mathiesen, A. Buridi, and K. R. McLeish. 2000. Granulocyte-macrophage colonystimulating factor delays neutrophil constitutive apoptosis through phosphoinositide 3-kinase and extracellular signal-regulated kinase pathways. J. Immunol. 164: 4286-4291.
14. Watanabe, S., T. Itoh, and K. Arai. 1996. JAK2 is essential for activation of c-fos and c-myc promoters and cell proliferation through the human granulocytemacrophage colony-stimulating factor receptor in BA/F3 cells. J. Biol. Chem. 271: 12681-12686.
15. Nicholson, K. M., and N. G. Anderson. 2002. The protein kinase B/Akt signalling pathway in human malignancy. Cell. Signal. 14: 381-395.
16. Alessi, D. R., M. Andjelkovic, B. Caudwell, P. Cron, N. Morrice, P. Cohen, and B. A. Hemmings. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J. 15: 6541-6551.
17. Hannigan, M. O., C. K. Huang, and D. Q. Wu. 2004. Roles of PI3K in neutrophil function. Curr. Top. Microbiol. Immunol. 282: 165-175.
18. Zhu, D., H. Hattori, H. Jo, Y. Jia, K. K. Subramanian, F. Loison, J. You, Y. Le, M. Honczarenko, L. Silberstein, and H. R. Luo. 2006. Deactivation of phosphatidylinositol 3,4,5-trisphosphate/Akt signaling mediates neutrophil spontaneous death. Proc. Natl. Acad. Sci. USA 103: 14836-14841.
19. Tilton, B., M. Andjelkovic, S. A. Didichenko, B. A. Hemmings, and M. Thelen. 1997. G-protein-coupled receptors and Fcγ-receptors mediate activation of Akt/protein kinase B in human phagocytes. J. Biol. Chem. 272: 28096-28101.
20. Brach, M. A., S. deVos, H. J. Gruss, and F. Herrmann. 1992. Prolongation of survival of human polymorphonuclear neutrophils by granulocyte-macrophage colony-stimulating factor is caused by inhibition of programmed cell death. Blood 80: 2920-2924.
21. Kobayashi, S. D., J. M. Voyich, A. R. Whitney, and F. R. DeLeo. 2005. Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage-colony stimulating factor. J. Leukoc. Biol. 78: 1408-1418.
22. Ward, J. R., P. R. Heath, J. W. Catto, M. K. B. Whyte, M. Milo, and S. A. Renshaw. 2011. Regulation of neutrophil senescence by microRNAs. PLoS One 6: e15810.
23. Cowling, R. T., and H. C. Birnboim. 2000. Expression of serum- and glucocorticoid-regulated kinase (sgk) mRNA is up-regulated by GM-CSF and other proinflammatory mediators in human granulocytes. J. Leukoc. Biol. 67: 240-248.
24. Mikosz, C. A., D. R. Brickley, M. S. Sharkey, T. W. Moran, and S. D. Conzen. 2001. Glucocorticoid receptor-mediated protection from apoptosis is associated with induction of the serine/threonine survival kinase gene, sgk-1. J. Biol. Chem. 276: 16649-16654.
25. Kobayashi, T., and P. Cohen. 1999. Activation of serum- and glucocorticoidregulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem. J. 339: 319-328.
26. Wardle, D. J., J. Burgon, I. Sabroe, C. D. Bingle, M. K. Whyte, and S. A. Renshaw. 2011. Effective caspase inhibition blocks neutrophil apoptosis and reveals Mcl-1 as both a regulator and a target of neutrophil caspase activation. PLoS One 6: e15768.
27. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
28. Renshaw, S. A., C. A. Loynes, D. M. Trushell, S. Elworthy, P. W. Ingham, and M. K. Whyte. 2006. A transgenic zebrafish model of neutrophilic inflammation. Blood 108: 3976-3978.
29. Xingang Wang, A. L. R., J. Li, R. J. Chai, W. Haishan, P. Sadiku, N. V. Ogryzko, M. Everett, K. Yoganathan, H. R. Luo, S. A. Renshaw, and P. W. Ingham. Novel natural product inhibitors of neutrophil recruitment identified through a transgenic zebrafish screen. Dis. Model. Mech. DOI: 10.1242/dmm.012047.
30. Nusslein-Volhard, C., and R. Dahm. 2002. Zebrafish: A Practical Approach. Oxford University Press, Oxford, U.K.
31. Elks, P. M., F. J. van Eeden, G. Dixon, X. Wang, C. C. Reyes-Aldasoro, P. W. Ingham, M. K. Whyte, S. R. Walmsley, and S. A. Renshaw. 2011. Activation of hypoxia-inducible factor-1α (Hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model. Blood 118: 712-722.
32. van Rooijen, E., E. E. Voest, I. Logister, J. Korving, T. Schwerte, S. Schulte-Merker, R. H. Giles, and F. J. van Eeden. 2009. Zebrafish mutants in the von Hippel-Lindau tumor suppressor display a hypoxic response and recapitulate key aspects of Chuvash polycythemia. Blood 113: 6449-6460.
33. Berghmans, S., P. Butler, P. Goldsmith, G. Waldron, I. Gardner, Z. Golder, F. M. Richards, G. Kimber, A. Roach, W. Alderton, and A. Fleming. 2008. Zebrafish based assays for the assessment of cardiac, visual and gut function - potential safety screens for early drug discovery. J. Pharmacol. Toxicol. Methods 58: 59-68.
34. Kobayashi, T., M. Deak, N. Morrice, and P. Cohen. 1999. Characterization of the structure and regulation of two novel isoforms of serum- and glucocorticoidinduced protein kinase. Biochem. J. 344: 189-197.
35. Prince, L. R., L. Allen, E. C. Jones, P. G. Hellewell, S. K. Dower, M. K. Whyte, and I. Sabroe. 2004. The role of interleukin-1b in direct and Toll-like receptor 4-mediated neutrophil activation and survival. Am. J. Pathol. 165: 1819-1826.
36. Brickley, D. R., C. A. Mikosz, C. R. Hagan, and S. D. Conzen. 2002. Ubiquitin modification of serum and glucocorticoid-induced protein kinase-1 (SGK-1). J. Biol. Chem. 277: 43064-43070.
37. Sabroe, I., L. R. Prince, E. C. Jones, M. J. Horsburgh, S. J. Foster, S. N. Vogel, S. K. Dower, and M. K. Whyte. 2003. Selective roles for Toll-like receptor (TLR)2 and TLR4 in the regulation of neutrophil activation and life span. J. Immunol. 170: 5268-5275.
38. Ellett, F., L. Pase, J. W. Hayman, A. Andrianopoulos, and G. J. Lieschke. 2011. mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117: e49-e56.
39. Murray, J. T., L. A. Cummings, G. B. Bloomberg, and P. Cohen. 2005. Identification of different specificity requirements between SGK1 and PKBα. FEBS Lett. 579: 991-994.
40. Nasevicius, A., and S. C. Ekker. 2000. Effective targeted gene 'knockdown' in zebrafish. Nat. Genet. 26: 216-220.
41. Park, J., M. L. Leong, P. Buse, A. C. Maiyar, G. L. Firestone, and B. A. Hemmings. 1999. Serum and glucocorticoid-inducible kinase (SGK) is a target of the PI 3-kinase-stimulated signaling pathway. EMBO J. 18: 3024-3033.
42. You, H., Y. Jang, A. I. You-Ten, H. Okada, J. Liepa, A. Wakeham, K. Zaugg, and T. W. Mak. 2004. p53-dependent inhibition of FKHRL1 in response to DNA damage through protein kinase SGK1. Proc. Natl. Acad. Sci. USA 101: 14057-14062.
43. Zhang, L., R. Cui, X. Cheng, and J. Du. 2005. Antiapoptotic effect of serum and glucocorticoid-inducible protein kinase is mediated by novel mechanism activating IκB kinase. Cancer Res. 65: 457-464.
44. Ward, C., A. Walker, I. Dransfield, C. Haslett, and A. G. Rossi. 2004. Regulation of granulocyte apoptosis by NF-κB. Biochem. Soc. Trans. 32: 465-467.
45. Jonsson, H., P. Allen, and S. L. Peng. 2005. Inflammatory arthritis requires Foxo3a to prevent Fas ligand-induced neutrophil apoptosis. Nat. Med. 11: 666-671.
46. Maurer, U., C. Charvet, A. S. Wagman, E. Dejardin, and D. R. Green. 2006. Glycogen synthase kinase-3 regulates mitochondrial outer membrane permeabilization and apoptosis by destabilization of MCL-1. Mol. Cell 21: 749-760.
47. Chen, J., H. Tang, N. Hay, J. Xu, and R. D. Ye. 2010. Akt isoforms differentially regulate neutrophil functions. Blood 115: 4237-4246.
48. Hannigan, M., L. Zhan, Z. Li, Y. Ai, D. Wu, and C. K. Huang. 2002. Neutrophils lacking phosphoinositide 3-kinaseg show loss of directionality during N-formyl-Met-Leu-Phe-induced chemotaxis. Proc. Natl. Acad. Sci. USA 99: 3603-3608.
49. Lang, F., C. Böhmer, M. Palmada, G. Seebohm, N. Strutz-Seebohm, and V. Vallon. 2006. (Patho)physiological significance of the serum- and glucocorticoidinducible kinase isoforms. Physiol. Rev. 86: 1151-1178.
50. Waldegger, S., K. Klingel, P. Barth, M. Sauter, M. L. Rfer, R. Kandolf, and F. Lang. 1999. h-sgk serine-threonine protein kinase gene as transcriptional target of transforming growth factor β in human intestine. Gastroenterology 116: 1081-1088.
51. Friedrich, B., S. Wärntges, K. Klingel, M. Sauter, R. Kandolf, T. Risler, G. A. Müller, R. Witzgall, W. Kriz, H. J. Gröne, and F. Lang. 2002. Upregulation of the human serum and glucocorticoid-dependent kinase 1 in glomerulonephritis. Kidney Blood Press. Res. 25: 303-307.