Opposition between PKC isoforms regulates histone deimination and neutrophil extracellular chromatin release

Frontiers in Immunology

Volumn 4, Issue FRB, 2013, Pages

  Neeli, Indira ^a   Radic, Marko ^a  

^a UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

Deimination; Inflammation; NETosis; PAD4; Protein kinase C

Indexed keywords

CALCIMYCIN; CHELERYTHRINE; ISOENZYME; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN ARGININE DEIMINASE; PROTEIN KINASE B BETA; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C TAU; PROTEIN KINASE C ZETA; SANGUINARINE; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EXTRACELLULAR MATRIX; HISTONE DEIMINATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; INFLAMMATION; NEUTROPHIL; NEUTROPHIL EXTRACELLULAR TRAP; WESTERN BLOTTING;

EID: 84879689982     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00038     Document Type: Article

References (48)

1. Andrade, F., Darrah, E., Gucek, M., Cole, R. N., Rosen, A., and Zhu, X. (2010). Autocitrullination of human peptidyl arginine deiminase type 4 regulates protein citrullination during cell activation. Arthritis Rheum. 62, 1630-1640.
2. Bertram, A., Zhang, H., von Vietinghoff, S., de Pablo, C., Haller, H., Shushakova, N., et al. (2012). Protein kinase C-t is required for murine neutrophil recruitment and adhesion strengthening under flow. J. Immunol. 188, 4043-4051.
3. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., et al. (2004). Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535.
4. Brinkmann, V., and Zychlinsky, A. (2012). Neutrophil extracellular traps: is immunity the second function of chromatin? J. Cell Biol. 198, 773-783.
5. Cuthbert, G. L., Daujat, S., Snowden, A. W., Erdjument-Bromage, H., Hagiwara, T., Yamada, M., et al. (2004). Histone deimination antagonizes arginine methylation. Cell 118, 545-553.
6. Dang, P. M., Fontayne, A., Hakim, J., El Benna, J., and Perianin, A. (2001). Protein kinase C ζ phosphorylates a subset of selective sites of the NADPH oxidase component p47phox and participates in formyl peptide-mediated neutrophil respiratory burst. J. Immunol. 166, 1206-1213.
7. Darrah, E., Rosen, A., Giles, J. T., and Andrade, F. (2012). Peptidylarginine deiminase 2, 3 and 4 have distinct specificities against cellular substrates: novel insights into autoantigen selection in rheumatoid arthritis. Ann. Rheum. Dis. 71, 92-98.
8. Duran, A., Diaz-Meco, M. T., and Moscat, J. (2003). Essential role of RelA Ser311 phosphorylation by ζPKC in NF-κB transcriptional activation. EMBO J. 22, 3910-3918.
9. Erdahl, W. L., Chapman, C. J., Taylor, R. W., and Pfeiffer, D. R. (1994). Ca2+ transport properties of ionophores A23187, ionomycin, and 4-BrA23187 in a well defined model system. Biophys. J. 66, 1678-1693.
10. Feng, Y., and Longmore, G. D. (2005). The LIM protein Ajuba influences interleukin-1-induced NF-kappaB activation by affecting the assembly and activity of the protein kinase Cζ/p62/TRAF6 signaling complex. Mol. Cell. Biol. 25, 4010-4022.
11. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., et al. (2007). Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241.
12. Fuchs, T. A., Brill, A., Duerschmied, D., Schatzberg, D., Monestier, M., Myers, D. D. Jr., et al. (2010). Extracellular DNA traps promote thrombosis. Proc. Natl. Acad. Sci. U.S.A. 107, 15880-15885.
13. Hakkim, A., Fuchs, T. A., Martinez, N. E., Hess, S., Prinz, H., Zychlinsky, A., et al. (2011). Activation of the Raf-MEK-ERK pathway is required for neutrophil extracellular trap formation. Nat. Chem. Biol. 7, 75-77.
14. 4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection. PLoS ONE 6:e22043. doi: 10.1371/journal.pone.0022043
15. Kaplan, M. J., and Radic, M. (2012). Neutrophil extracellular traps: double-edged swords of innate immunity. J. Immunol. 189, 2689-2695.
16. Kennedy, A. D., and DeLeo, F. R. (2009). Neutrophil apoptosis and the resolution of infection. Immunol. Res. 43, 25-61.
17. Laudanna, C., Mochly-Rosen, D., Liron, T., Constantin, G., and Butcher, E. C. (1998). Evidence of ζ protein kinase C involvement in polymorphonuclear neutrophil integrin-dependent adhesion and chemotaxis. J. Biol. Chem. 273, 30306-30315.
18. 4 mediated histone hypercitrullination induces heterochromatin decondensation and chromatin unfolding to form neutrophil extracellular trap-like structures. Front. Immunol. 3:307. doi: 10.3389/fimmu.2012.00307
19. Levy, D., Kuo, A. J., Chang, Y., Schaefer, U., Kitson, C., Cheung, P., et al. (2011). Lysine methylation of the NF-kappaB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-kappaB signaling. Nat. Immunol. 12, 29-36.
20. 4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. J. Exp. Med. 207, 1853-1862.
21. Martiny-Baron, G., Kazanietz, M. G., Mischak, H., Blumberg, P. M., Kochs, G., Hug, H., et al. (1993). Selective inhibition of protein kinase C isozymes by the indolocarbazole Go 6976. J. Biol. Chem. 268, 9194-9197.
22. Nakashima, K., Hagiwara, T., and Yamada, M. (2002). Nuclear localization of peptidylarginine deiminase V and histone deimination in granulocytes. J. Biol. Chem. 277, 49562-49568.
23. Nathan, C. (2006). Neutrophils and immunity: challenges and opportunities. Nat. Rev. Immunol. 6, 173-182.
24. Neeli, I., Dwivedi, N., Khan, S., and Radic, M. (2009). Regulation of extracellular chromatin release from neutrophils. J. Innate Immun. 1, 194-201.
25. Neeli, I., Khan, S. N., and Radic, M. (2008). Histone deimination as a response to inflammatory stimuli in neutrophils. J. Immunol. 180, 1895-1902.
26. Nishimura, T., Yamaguchi, T., Kato, K., Yoshizawa, M., Nabeshima, Y., Ohno, S., et al. (2005). PAR-6-PAR-3 mediates Cdc42-induced Rac activation through the Rac GEFs STEF/Tiam1. Nat. Cell Biol. 7, 270-277.
27. Nixon, J. B., and McPhail, L. C. (1999). Protein kinase C (PKC) isoforms translocate to Triton-insoluble fractions in stimulated human neutrophils: correlation of conventional PKC with activation of NADPH oxidase. J. Immunol. 163, 4574-4582.
28. Parker, H., Albrett, A. M., Kettle, A. J., and Winterbourn, C. C. (2012a). Myeloperoxidase associated with neutrophil extracellular traps is active and mediates bacterial killing in the presence of hydrogen peroxide. J. Leukoc. Biol. 91, 369-376.
29. Parker, H., Dragunow, M., Hampton, M. B., Kettle, A. J., and Winterbourn, C. C. (2012b). Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J. Leukoc. Biol. 92, 841-849.
30. Phillipson, M., Heit, B., Colarusso, P., Liu, L., Ballantyne, C. M., and Kubes, P. (2006). Intraluminal crawling of neutrophils to emigration sites: a molecularly distinct process from adhesion in the recruitment cascade. J. Exp. Med. 203, 2569-2575.
31. Powell, C. E., and Chen, K. K. (1955). The pharmacological action of chelerythrine. J. Am. Pharm. Assoc. Am. Pharm. Assoc. (Baltim.) 44, 196-199.
32. Raad, H., Paclet, M. H., Boussetta, T., Kroviarski, Y., Morel, F., Quinn, M. T., et al. (2009). Regulation of the phagocyte NADPH oxidase activity: phosphorylation of gp91phox/NOX2 by protein kinase C enhances its diaphorase activity and binding to Rac2, p67phox, and p47phox. FASEB J. 23, 1011-1022.
33. 4 in NET formation. Front. Immunol. 3:360. doi: 10.3389/fimmu.2012.00360
34. 3 integrin in osteoclasts and in Chinese hamster ovary (CHO) cells. J. Cell Sci. 118, 3263-3275.
35. Schenck, G., and Hannse, H. (1954). Separation of sanguinarine and chelerythrine and additional plant bases of Sanguinaria canadensis. Arch. Pharm. Ber. Dtsch. Pharm. Ges. 287, 544-548.
36. Steinberg, B. E., and Grinstein, S. (2007). Unconventional roles of the NADPH oxidase: signaling, ion homeostasis, and cell death. Sci. STKE 2007, pe11.
37. Steinberg, S. F. (2008). Structural basis of protein kinase C isoform function. Physiol. Rev. 88, 1341-1378.
38. Suzuki, K., and Namiki, H. (1998). Phorbol 12-myristate 13-acetate induced cell death of porcine peripheral blood polymorphonuclear leucocytes. Cell Struct. Funct. 23, 367-372.
39. Takei, H., Araki, A., Watanabe, H., Ichinose, A., and Sendo, F. (1996). Rapid killing of human neutrophils by the potent activator phorbol 12-myristate 13-acetate (PMA) accompanied by changes different from typical apoptosis or necrosis. J. Leukoc. Biol. 59, 229-240.
40. Tauber, A. I. (1987). Protein kinase C and the activation of the human neutrophil NADPH-oxidase. Blood 69, 711-720.
41. Wang, J., Weaver, I. C., Gauthier-Fisher, A., Wang, H., He, L., Yeomans, J., et al. (2010). CBP histone acetyltransferase activity regulates embryonic neural differentiation in the normal and Rubinstein-Taybi syndrome brain. Dev. Cell 18, 114-125.
42. Wang, Y., Li, M., Stadler, S., Correll, S., Li, P., Wang, D., et al. (2009). Histone hypercitrullination mediates chromatin decondensation and neutrophil extracellular trap formation. J. Cell Biol. 184, 205-213.
43. 4 regulates histone arginine methylation levels via demethylimination. Science 306, 279-283.
44. Xie, Z., Dong, Y., Zhang, J., Scholz, R., Neumann, D., and Zou, M. H. (2009). Identification of the serine 307 of LKB1 as a novel phosphorylation site essential for its nucleocytoplasmic transport and endothelial cell angiogenesis. Mol. Cell. Biol. 29, 3582-3596.
45. Xu, J., and Clark, R. A. (1997). A three-dimensional collagen lattice induces protein kinase C-ζ activity: role in α2 integrin and collagenase mRNA expression. J. Cell Biol. 136, 473-483.
46. 3 ubiquitin ligase CHIP facilitates Toll-like receptor signaling by recruiting and polyubiquitinating Src and atypical PKC ζ. J. Exp. Med. 208, 2099-2112.
47. Yipp, B. G., Petri, B., Salina, D., Jenne, C. N., Scott, B. N., Zbytnuik, L. D., et al. (2012). Infection-induced NETosis is a dynamic process involving neutrophil multitasking in vivo. Nat. Med. 18, 1386-1393.
48. Yousefi, S., Mihalache, C., Kozlowski, E., Schmid, I., and Simon, H. U. (2009). Viable neutrophils release mitochondrial DNA to form neutrophil extracellular traps. Cell Death Differ. 16, 1438-1444.