Chromatin-Associated Protein Kinase C-θ Regulates an Inducible Gene Expression Program and MicroRNAs in Human T Lymphocytes

Molecular Cell

Volumn 41, Issue 6, 2011, Pages 704-719

  Sutcliffe, Elissa L ^a   Bunting, Karen L ^b   He, Yi Qing ^a   Li, Jasmine ^a   Phetsouphanh, Chansavath ^e   Seddiki, Nabila ^e   Zafar, Anjum ^a   Hindmarsh, Elizabeth J ^a   Parish, Christopher R ^a   Kelleher, Anthony D ^e   McInnes, Russell L ^c   Taya, Toshiki ^d   Milburn, Peter J ^a   Rao, Sudha ^a,f  

^a Biology and Environment   (Australia)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c AGILENT TECHNOLOGIES   (Australia)

^d YOKOGAWA ANALYTICAL SYSTEMS INC   (Japan)

^e UNIVERSITY OF NEW SOUTH WALES   (Australia)

^f UNIVERSITY OF CANBERRA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; MICRORNA; PROTAMINE KINASE; PROTEIN 14 3 3; PROTEIN 14 3 3ZETA; PROTEIN KINASE C THETA; PROTEIN MSK 1; RNA POLYMERASE II; UNCLASSIFIED DRUG;

ARTICLE; CELL NUCLEUS; CHROMATIN; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; IMMUNE RESPONSE GENE; IMMUNOREGULATION; LYMPHOCYTE FUNCTION; NUCLEOTIDE SEQUENCE; PROMOTER REGION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION;

CELL LINE, TUMOR; CELL NUCLEUS; CHROMATIN; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-2; ISOENZYMES; JURKAT CELLS; MICRORNAS; PROMOTER REGIONS, GENETIC; PROTEIN KINASE C; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; RNA POLYMERASE II; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 79952632406     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.02.030     Document Type: Article

References (40)

1. Alepuz P.M., Jovanovic A., Reiser V., Ammerer G. Stress-induced map kinase Hog1 is part of transcription activation complexes. Mol. Cell 2001, 7:767-777.
2. Alepuz P.M., de Nadal E., Zapater M., Ammerer G., Posas F. Osmostress-induced transcription by Hot1 depends on a Hog1-mediated recruitment of the RNA Pol II. EMBO J. 2003, 22:2433-2442.
3. Anest V., Hanson J.L., Cogswell P.C., Steinbrecher K.A., Strahl B.D., Baldwin A.S. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 2003, 423:659-663.
4. Araki Y., Fann M., Wersto R., Weng N.P. Histone acetylation facilitates rapid and robust memory CD8 T cell response through differential expression of effector molecules (eomesodermin and its targets: perforin and granzyme B). J. Immunol. 2008, 180:8102-8108.
5. Birbach A., Gold P., Binder B.R., Hofer E., de Martin R., Schmid J.A. Signaling molecules of the NF-kappa B pathway shuttle constitutively between cytoplasm and nucleus. J. Biol. Chem. 2002, 277:10842-10851.
6. Burkhart B.A., Kennett S.B., Archer T.K. Osmotic stress-dependent repression is mediated by histone H3 phosphorylation and chromatin structure. J. Biol. Chem. 2007, 282:4400-4407.
7. de Nadal E., Posas F. Multilayered control of gene expression by stress-activated protein kinases. EMBO J. 2010, 29:4-13.
8. Doehn U., Hauge C., Frank S.R., Jensen C.J., Duda K., Nielsen J.V., Cohen M.S., Johansen J.V., Winther B.R., Lund L.R., et al. RSK is a principal effector of the RAS-ERK pathway for eliciting a coordinate promotile/invasive gene program and phenotype in epithelial cells. Mol. Cell 2009, 35:511-522.
9. Edmunds J.W., Mahadevan L.C. Cell signaling. Protein kinases seek close encounters with active genes. Science 2006, 313:449-451.
10. Ford J.W., McVicar D.W. TREM and TREM-like receptors in inflammation and disease. Curr. Opin. Immunol. 2009, 21:38-46.
11. Furuno K., Ikeda K., Hamano S., Fukuyama K., Sonoda M., Hara T., Sasazuki T., Yamamoto K. Onecut transcription factor OC2 is a direct target of T-bet in type-1 T-helper cells. Genes Immun. 2008, 9:302-308.
12. Gregory P.A., Bert A.G., Paterson E.L., Barry S.C., Tsykin A., Farshid G., Vadas M.A., Khew-Goodall Y., Goodall G.J. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 2008, 10:593-601.
13. Griner E.M., Kazanietz M.G. Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 2007, 7:281-294.
14. Hayashi K., Altman A. Protein kinase C theta (PKCtheta): a key player in T cell life and death. Pharmacol. Res. 2007, 55:537-544.
15. Inoue M., Kishimoto A., Takai Y., Nishizuka Y. Studies on a cyclic nucleotide-independent protein kinase and its proenzyme in mammalian tissues. II. Proenzyme and its activation by calcium-dependent protease from rat brain. J. Biol. Chem. 1977, 252:7610-7616.
16. Isakov N., Altman A. Protein kinase C(theta) in T cell activation. Annu. Rev. Immunol. 2002, 20:761-794.
17. Lawrence M.C., McGlynn K., Shao C., Duan L., Naziruddin B., Levy M.F., Cobb M.H. Chromatin-bound mitogen-activated protein kinases transmit dynamic signals in transcription complexes in beta-cells. Proc. Natl. Acad. Sci. USA 2008, 105:13315-13320.
18. Liu Y., Graham C., Li A., Fisher R.J., Shaw S. Phosphorylation of the protein kinase C-theta activation loop and hydrophobic motif regulates its kinase activity, but only activation loop phosphorylation is critical to in vivo nuclear-factor-kappaB induction. Biochem. J. 2002, 361:255-265.
19. Marsland B.J., Nembrini C., Schmitz N., Abel B., Krautwald S., Bachmann M.F., Kopf M. Innate signals compensate for the absence of PKC-theta during in vivo CD8(+) T cell effector and memory responses. Proc. Natl. Acad. Sci. USA 2005, 102:14374-14379.
20. Martelli A.M., Sang N., Borgatti P., Capitani S., Neri L.M. Multiple biological responses activated by nuclear protein kinase C. J. Cell. Biochem. 1999, 74:499-521.
21. Martiny-Baron G., Fabbro D. Classical PKC isoforms in cancer. Pharmacol. Res. 2007, 55:477-486.
22. Meller N., Altman A., Isakov N. New perspectives on PKCtheta, a member of the novel subfamily of protein kinase C. Stem Cells 1998, 16:178-192.
23. Metzger E., Imhof A., Patel D., Kahl P., Hoffmeyer K., Friedrichs N., Müller J.M., Greschik H., Kirfel J., Ji S., et al. Phosphorylation of histone H3T6 by PKCbeta(I) controls demethylation at histone H3K4. Nature 2010, 464:792-796.
24. Pascual-Ahuir A., Struhl K., Proft M. Genome-wide location analysis of the stress-activated MAP kinase Hog1 in yeast. Methods 2006, 40:272-278.
25. Passalacqua M., Patrone M., Sparatore B., Melloni E., Pontremoli S. Protein kinase C-theta is specifically localized on centrosomes and kinetochores in mitotic cells. Biochem. J. 1999, 337:113-118.
26. Plaisance V., Abderrahmani A., Perret-Menoud V., Jacquemin P., Lemaigre F., Regazzi R. MicroRNA-9 controls the expression of Granuphilin/Slp4 and the secretory response of insulin-producing cells. J. Biol. Chem. 2006, 281:26932-26942.
27. Pokholok D.K., Zeitlinger J., Hannett N.M., Reynolds D.B., Young R.A. Activated signal transduction kinases frequently occupy target genes. Science 2006, 313:533-536.
28. Proft M., Mas G., de Nadal E., Vendrell A., Noriega N., Struhl K., Posas F. The stress-activated Hog1 kinase is a selective transcriptional elongation factor for genes responding to osmotic stress. Mol. Cell 2006, 23:241-250.
29. Rao S., Procko E., Shannon M.F. Chromatin remodeling, measured by a novel real-time polymerase chain reaction assay, across the proximal promoter region of the IL-2 gene. J. Immunol. 2001, 167:4494-4503.
30. Saccani S., Pantano S., Natoli G. p38-Dependent marking of inflammatory genes for increased NF-kappa B recruitment. Nat. Immunol. 2002, 3:69-75.
31. Simone C., Forcales S.V., Hill D.A., Imbalzano A.N., Latella L., Puri P.L. p38 pathway targets SWI-SNF chromatin-remodeling complex to muscle-specific loci. Nat. Genet. 2004, 36:738-743.
32. Springael C., Thomas S., Rahmouni S., Vandamme A., Goldman M., Willems F., Vosters O. Rottlerin inhibits human T cell responses. Biochem. Pharmacol. 2007, 73:515-525.
33. Sutcliffe E.L., Parish I.A., He Y.Q., Juelich T., Tierney M.L., Rangasamy D., Milburn P.J., Parish C.R., Tremethick D.J., Rao S. Dynamic histone variant exchange accompanies gene induction in T cells. Mol. Cell. Biol. 2009, 29:1972-1986.
34. Thomson S., Clayton A.L., Hazzalin C.A., Rose S., Barratt M.J., Mahadevan L.C. The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. EMBO J. 1999, 18:4779-4793.
35. Visnjic D., Banfic H. Nuclear phospholipid signaling: phosphatidylinositol-specific phospholipase C and phosphoinositide 3-kinase. Pflugers Arch. 2007, 455:19-30.
36. Winter S., Simboeck E., Fischle W., Zupkovitz G., Dohnal I., Mechtler K., Ammerer G., Seiser C. 14-3-3 proteins recognize a histone code at histone H3 and are required for transcriptional activation. EMBO J. 2008, 27:88-99.
37. Yamamoto Y., Verma U.N., Prajapati S., Kwak Y.T., Gaynor R.B. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 2003, 423:655-659.
38. Yin Y., Chen X., Shu Y. Gene expression of the invasive phenotype of TNF-alpha-treated MCF-7 cells. Biomed. Pharmacother. 2009, 63:421-428.
39. Yu H., Fukami K., Watanabe Y., Ozaki C., Takenawa T. Phosphatidylinositol 4,5-bisphosphate reverses the inhibition of RNA transcription caused by histone H1. Eur. J. Biochem. 1998, 251:281-287.
40. Yu M., Schreek S., Cerni C., Schamberger C., Lesniewicz K., Poreba E., Vervoorts J., Walsemann G., Grötzinger J., Kremmer E., et al. PARP-10, a novel Myc-interacting protein with poly(ADP-ribose) polymerase activity, inhibits transformation. Oncogene 2005, 24:1982-1993.