Inhibition of protein kinase C βiI downregulates tristetraprolin expression in activated macrophages

Inflammation Research

Volumn 57, Issue 5, 2008, Pages 230-240

  Leppanen T ^a   Jalonen, U ^a   Kankaanranta, H ^a   Tuominen, R ^b   Moilanen, E ^a  

^a TAMPERE UNIVERSITY OF TECHNOLOGY   (Finland)

^b UNIVERSITY OF HELSINKI   (Finland)

Author keywords

AP 2; Macrophages; PKC; Tristetraprolin

Indexed keywords

12 (2 CYANOETHYL) 6,7,12,13 TETRAHYDRO 13 METHYL 5 OXOINDOLO[2,3 A]PYRROLO[3,4 C]CARBAZOLE; 2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; 4,5 BIS(4 FLUOROANILINO)PHTHALIMIDE; 5,6 BIS[(4 FLUOROPHENYL)AMINO] 2H ISOINDOLE 1,3 DIONE; EARLY GROWTH RESPONSE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LIPOPOLYSACCHARIDE; MESSENGER RNA; PHORBOL 13 ACETATE 12 MYRISTATE; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN KINASE C BETA INHIBITOR; PROTEIN KINASE C BETAI; PROTEIN KINASE C BETAII; RUBOXISTAURIN; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR SP1; TRISTETRAPROLIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE EXPRESSION REGULATION; MACROPHAGE ACTIVATION; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; CARCINOGENS; CELLS, CULTURED; EARLY GROWTH RESPONSE PROTEIN 1; ENZYME INHIBITORS; IMMUNOGLOBULINS; ISOENZYMES; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NF-KAPPA B; PHTHALIMIDES; PROTEIN KINASE C; RNA, MESSENGER; TETRADECANOYLPHORBOL ACETATE; TRANSCRIPTION FACTOR AP-2; TRISTETRAPROLIN;

EID: 46449108930     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-007-7122-2     Document Type: Article

References (62)

1. Varnum BC, Lim RW, Sukhatme VP, Herschman HR. Nucleotide sequence of a cDNA encoding TIS11, a message induced in Swiss 3T3 cells by the tumor promoter tetradecanoyl phorbol acetate. Oncogene 1989; 4: 119-20.
2. DuBois RN, McLane MW, Ryder K, Lau LF, Nathans D. A growth factor-inducible nuclear protein with a novel cysteine/histidine repetitive sequence. J Biol Chem 1990; 265: 19185-91.
3. Lai WS, Stumpo DJ, Blackshear PJ. Rapid insulin-stimulated accumulation of an mRNA encoding a proline-rich protein. J Biol Chem 1990; 265: 16556-63.
4. Carballo E, Lai WS, Blackshear PJ. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 1998; 281: 1001-5.
5. Lai WS, Carballo E, Strum JR, Kennington EA, Phillips RS, Blackshear PJ. Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 1999; 19: 4311-23.
6. Carballo E, Lai WS, Blackshear PJ. Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 2000; 95: 1891-9.
7. Stoecklin G, Ming XF, Looser R, Moroni C. Somatic mRNA turnover mutants implicate tristetraprolin in the interleukin-3 mRNA degradation pathway. Mol Cell Biol 2000; 20: 3753-63.
8. Sawaoka H, Dixon DA, Oates JA, Boutaud O. Tristetraprolin binds to the 3′-untranslated region of cyclooxygenase-2 mRNA. A polyadenylation variant in a cancer cell line lacks the binding site. J Biol Chem 2003; 278: 13928-35.
9. Ogilvie RL, Abelson M, Hau HH, Vlasova I, Blackshear PJ, Bohjanen PR. Tristetraprolin down-regulates IL-2 gene expression through AU-rich element-mediated mRNA decay. J Immunol 2005; 174: 953-61.
10. Fechir M, Linker K, Pautz A, Hubrich T, Förstermann U, Rodriguez-Pascual F, et al. Tristetraprolin regulates the expression of the human inducible nitric-oxide synthase gene. Mol Pharmacol 2005; 67: 2148-61.
11. Taylor GA, Carballo E, Lee DM, Lai WS, Thompson MJ, Patel DD, et al. A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 1996; 4: 445-54.
12. Carballo E, Cao H, Lai WS, Kennington EA, Campbell D, Blackshear PJ. Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway. J Biol Chem 2001; 276: 42580-7.
13. Mahtani KR, Brook M, Dean JL, Sully G, Saklatvala J, Clark AR. Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol Cell Biol 2001; 21: 6461-9.
14. Cao H, Dzineku F, Blackshear PJ. Expression and purification of recombinant tristetraprolin that can bind to tumor necrosis factor-alpha mRNA and serve as a substrate for mitogen-activated protein kinases. Arch Biochem Biophys 2003; 412: 106-20.
15. Jalonen U, Lahti A, Korhonen R, Kankaanranta H, Moilanen E. Inhibition of tristetraprolin expression by dexamethasone in activated macrophages. Biochem Pharmacol 2005; 69: 733-40.
16. Brook M, Tchen CR, Santalucia T, McIlrath J, Arthur JS, Saklatvala J, et al. Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol Cell Biol 2006; 26: 2408-18.
17. Hitti E, Iakovleva T, Brook M, Deppenmeier S, Gruber AD, Radzioch D, et al. Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenine/uridine-rich element. Mol Cell Biol 2006; 26: 2399-407.
18. Brooks SA, Connolly JE, Rigby WF. The role of mRNA turnover in the regulation of tristetraprolin expression: evidence for an extracellular signal-regulated kinase-specific, AU-rich element-dependent, autoregulatory pathway. J Immunol 2004; 172: 7263-71.
19. Tchen CR, Brook M, Saklatvala J, Clark AR. The stability of tristetraprolin mRNA is regulated by mitogen-activated protein kinase p38 and by tristetraprolin itself. J Biol Chem 2004; 279: 32393-400.
20. 2Y-purinoceptors on astrocytes results in immediate early gene expression and potentiation of neuropeptide action. Neuroscience 1998; 85: 521-5.
21. Murata T, Niimi Y, Kaneda N. Characterization of the 5′-flanking region of the rat TIS11 gene. Mol Cell Biochem 2000; 214: 1-6.
22. Tan SL, Parker PJ. Emerging and diverse roles of protein kinase C in immune cell signalling. Biochem J 2003; 376: 545-52.
23. Aksoy E, Goldman M, Willems F. Protein kinase C epsilon: a new target to control inflammation and immune-mediated disorders. Int J Biochem Cell Biol 2004; 36: 183-8.
24. Hofmann J. Protein kinase C isozymes as potential targets for anticancer therapy. Curr Cancer Drug Targets 2004; 4: 125-46.
25. Spitaler M, Cantrell DA. Protein kinase C and beyond. Nat Immunol 2004; 5: 785-90.
26. Chen CC, Wang JK, Lin SB. Antisense oligonucleotides targeting protein kinase C-α, -βI, or -δ but not -η inhibit lipopolysaccharide-induced nitric oxide synthase expression in RAW 264.7 macrophages: involvement of a nuclear factor κB-dependent mechanism. J Immunol 1998; 161: 6206-14.
27. Ramana KV, Srivastava SK. Mediation of aldose reductase in lipopolysaccharide-induced inflammatory signals in mouse peritoneal macrophages. Cytokine 2006; 36: 115-22.
28. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-54.
29. Salonen T, Sareila O, Jalonen U, Kankaanranta H, Tuominen R, Moilanen E. Inhibition of classical PKC isoenzymes downregulates STAT1 activation and iNOS expression in LPS-treated murine J774 macrophages. Br J Pharmacol 2006; 147: 790-9.
30. Lahti A, Jalonen U, Kankaanranta H, Moilanen E. c-Jun NH2-terminal kinase inhibitor anthra(1,9-cd)pyrazol-6(2H)-one reduces inducible nitric-oxide synthase expression by destabilizing mRNA in activated macrophages. Mol Pharmacol 2003; 64: 308-15.
31. Huang FL, Yoshida Y, Cunha-Melo JR, Beaven MA, Huang KP. Differential down-regulation of protein kinase C isozymes. J Biol Chem 1989; 264: 4238-43.
32. Liu WS, Heckman CA. The sevenfold way of PKC regulation. Cell Signal 1998; 10: 529-42.
33. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, et al. Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J Biol Chem 1993; 268: 9194-7.
34. Wilkinson SE, Parker PJ, Nixon JS. Isoenzyme specificity of bisindolylmaleimides, selective inhibitors of protein kinase C. Biochem J 1993; 294: 335-7.
35. Kashiwada Y, Huang L, Ballas LM, Jiang JB, Janzen WP, Lee KH. New hexahydroxybiphenyl derivatives as inhibitors of protein kinase C. J Med Chem 1994; 37: 195-200.
36. Jirousek MR, Gillig JR, Gonzalez CM, Heath WF, McDonald JH,3rd, Neel DA, et al. (S)-13-[(dimethylamino)methyl]-10,11,14,15-tetrahydro-4,9:16, 21-dimetheno-1H, 13H-dibenzo[e,k]pyrrolo[3,4-h][1,4, 13]oxadiazacyclohexadecene-1,3(2H)-dione (LY333531) and related analogues: isozyme selective inhibitors of protein kinase C beta. J Med Chem 1996; 39: 2664-71.
37. Chalfant CE, Ohno S, Konno Y, Fisher AA, Bisnauth LD, Watson JE, et al. A carboxy-terminal deletion mutant of protein kinase C β II inhibits insulin-stimulated 2-deoxyglucose uptake in L6 rat skeletal muscle cells. Mol Endocrinol 1996; 10: 1273-81.
38. Lai WS, Thompson MJ, Taylor GA, Liu Y, Blackshear PJ. Promoter analysis of Zfp-36, the mitogen-inducible gene encoding the zinc finger protein tristetraprolin. J Biol Chem 1995; 270: 25266-72.
39. Lai WS, Thompson MJ, Blackshear PJ. Characteristics of the intron involvement in the mitogen-induced expression of Zfp-36. J Biol Chem 1998; 273: 506-17.
40. Kawakami T, Kawakami Y, Kitaura J. Protein kinase C β (PKC β): normal functions and diseases. J Biochem (Tokyo) 2002; 132: 677-82.
41. Bevilacqua A, Ceriani MC, Capaccioli S, Nicolin A. Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J Cell Physiol 2003; 195: 356-72.
42. Zhang W, Wagner BJ, Ehrenman K, Schaefer AW, DeMaria CT, Crater D, et al. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol Cell Biol 1993; 13: 7652-65.
43. Brennan CM, Steitz JA. HuR and mRNA stability. Cell Mol Life Sci 2001; 58: 266-77.
44. Blackshear PJ. Tristetraprolin and other CCCH tandem zinc-finger proteins in the regulation of mRNA turnover. Biochem Soc Trans 2002; 30: 945-52.
45. Jalonen U, Nieminen R, Vuolteenaho K, Kankaanranta H, Moilanen E. Down-regulation of tristetraprolin expression results in enhanced IL-12 and MIP-2 production and reduced MIP-3α synthesis in activated macrophages. Mediators Inflamm 2006; article ID 40691, doi: 10.1155/MI/2006/40691.
46. Carballo E, Gilkeson GS, Blackshear PJ. Bone marrow transplantation reproduces the tristetraprolin-deficiency syndrome in recombination activating gene-2 (-/-) mice. Evidence that monocyte/macrophage progenitors may be responsible for TNFα overproduction. J Clin Invest 1997; 100: 986-95.
47. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000; 351: 95-105.
48. Kaneda N, Murata T, Niimi Y, Minamiyama M. Cloning and characterization of the rat TIS11 gene. Mol Cell Biochem 2000; 213: 119-26.
49. Suyama K, Kabuyama Y, Suzuki S, Kawasaki Y, Suzuki J, Suzuki H, et al. Induction of transcription factor AP-2 by cytokines and prostaglandins in cultured mesangial cells. Am J Nephrol 2001; 21: 307-14.
50. Williams T, Admon A, Lüscher B, Tjian R. Cloning and expression of AP-2, a cell-type-specific transcription factor that activates inducible enhancer elements. Genes Dev 1988; 2: 1557-69.
51. Oyama N, Iwatsuki K, Homma Y, Kaneko F. Induction of transcription factor AP-2 by inflammatory cytokines in human keratinocytes. J Invest Dermatol 1999; 113: 600-6.
52. Imagawa M, Chiu R, Karin M. Transcription factor AP-2 mediates induction by two different signal-transduction pathways: protein kinase C and cAMP. Cell 1987; 51: 251-60.
53. Medcalf RL, Rüegg M, Schleuning WD. A DNA motif related to the cAMP-responsive element and an exon-located activator protein-2 binding site in the human tissue-type plasminogen activator gene promoter cooperate in basal expression and convey activation by phorbol ester and cAMP. J Biol Chem 1990; 265: 14618-26.
54. D'Angelo DD, Davis MG, Houser WA, Eubank JJ, Ritchie ME, Dorn GW,2nd. Characterization of 5′ end of human thromboxane receptor gene. Organizational analysis and mapping of protein kinase C-responsive elements regulating expression in platelets. Circ Res 1995; 77: 466-74.
55. Geimonen E, Jiang W, Ali M, Fishman GI, Garfield RE, Andersen J. Activation of protein kinase C in human uterine smooth muscle induces connexin-43 gene transcription through an AP-1 site in the promoter sequence. J Biol Chem 1996; 271: 23667-74.
56. Ries S, Büchler C, Langmann T, Fehringer P, Aslanidis C, Schmitz G. Transcriptional regulation of lysosomal acid lipase in differentiating monocytes is mediated by transcription factors Sp1 and AP-2. J Lipid Res 1998; 39: 2125-34.
57. Ishimitsu T, Tsukada K, Minami J, Ono H, Matsuoka H. Variations of human adrenomedullin gene and its relation to cardiovascular diseases. Hypertens Res 2003; 26: S129-34.
58. Inuzuka H, Nanbu-Wakao R, Masuho Y, Muramatsu M, Tojo H, Wakao H. Differential regulation of immediate early gene expression in preadipocyte cells through multiple signaling pathways. Biochem Biophys Res Commun 1999; 265: 664-8.
59. Jalonen U, Leppänen T, Kankaanranta H, Moilanen E. Salbutamol increases tristetraprolin expression in macrophages. Life Sci 2007; doi:10.1016/j.lfs.2007.09.022.
60. Korhonen R, Linker K, Pautz A, Förstermann U, Moilanen E, Kleinert H. Post-transcriptional regulation of human inducible nitric-oxide synthase expression by the Jun N-terminal kinase. Mol Pharmacol 2007; 71:1427-34.
61. Cao H, Kelly MA, Kari F, Dawson HD, Urban JF,Jr, Coves S, et al. Green tea increases anti-inflammatory tristetraprolin and decreases pro-inflammatory tumor necrosis factor mRNA levels in rats. J Inflamm 2007; 4: 1, doi:10.1186/1476-9255-4-1.
62. Cao H, Polansky MM, Anderson RA. Cinnamon extract and polyphenols affect the expression of tristetraprolin, insulin receptor, and glucose transporter 4 in mouse 3T3-L1 adipocytes. Arch Biochem Biophys 2007; 459: 214-22.