Interleukin-1β stimulates acute phase response and C-reactive protein synthesis by inducing an NFκB- and C/EBPβ-dependent autocrine interleukin-6 loop

Molecular Immunology

Volumn 45, Issue 9, 2008, Pages 2678-2689

  Kramer, Frank ^a   Torzewski, Jan ^b   Kamenz, Joachim ^b   Veit, Kerstin ^a   Hombach, Vinzenz ^b   Dedio, Jürgen ^a   Ivashchenko, Yuri ^a  

^a SANOFI AVENTIS DEUTSCHLAND GMBH   (Germany)

^b UNIVERSITY OF ULM   (Germany)

Author keywords

CRP; IL 1 ; IL 6; Primary human hepatocytes

Indexed keywords

C REACTIVE PROTEIN; CCAAT ENHANCER BINDING PROTEIN BETA; HEPCIDIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; LIPOPOLYSACCHARIDE BINDING PROTEIN; ACUTE PHASE PROTEIN; STAT3 PROTEIN; STAT3 PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; HEPATOMA CELL; HUMAN; HUMAN CELL; KUPFFER CELL; LIVER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; ACUTE PHASE RESPONSE; BIOSYNTHESIS; CELL CULTURE; CELL NUCLEUS; CYTOLOGY; GENE EXPRESSION PROFILING; GENETICS; IMMUNOLOGY; METABOLISM; PHOSPHORYLATION; TUMOR CELL LINE;

ACUTE-PHASE PROTEINS; ACUTE-PHASE REACTION; C-REACTIVE PROTEIN; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL LINE, TUMOR; CELL NUCLEUS; CELLS, CULTURED; GENE EXPRESSION PROFILING; HEPATOCYTES; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 40849135497     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2007.12.017     Document Type: Article

References (43)

1. Agrawal A., Samols D., and Kushner I. Transcription factor c-Rel enhances C-reactive protein expression by facilitating the binding of C/EBPbeta to the promoter. Mol. Immunol. 40 (2003) 373-380
2. Agrawal A., Cha-Molstad H., Samols D., and Kushner I. Overexpressed nuclear factor-kappaB can participate in endogenous C-reactive protein induction, and enhances the effects of C/EBPbeta and signal transducer and activator of transcription-3. Immunology 108 (2003) 539-547
3. Akira S., Isshiki H., Sugita T., Tanabe O., Kinoshita S., Nishio Y., Nakajima T., Hirano T., and Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. Embo J. 9 (1990) 1897-1906
4. Alam T., An M.R., and Papaconstantinou J. Differential expression of three C/EBP isoforms in multiple tissues during the acute phase response. J. Biol. Chem. 267 (1992) 5021-5024
5. Black S., Kushner I., and Samols D. C-reactive protein. J. Biol. Chem. 279 (2004) 48487-48490
6. Cha-Molstad H., Agrawal A., Zhang D., Samols D., and Kushner I. The Rel family member P50 mediates cytokine-induced C-reactive protein expression by a novel mechanism. J. Immunol. 165 (2000) 4592-4597
7. Chi M., Tridandapani S., Zhong W., Coggeshall K.M., and Mortensen R.F. C-reactive protein induces signaling through Fc gamma RIIa on HL-60 granulocytes. J. Immunol. 168 (2002) 1413-1418
8. De Martin R., Raidl M., Hofer E., and Binder B.R. Adenovirus-mediated expression of green fluorescent protein. Gene Ther. 4 (1997) 493-495
9. Didonato J., Mercurio F., Rosette C., Wu-Li W., Suyang H., Gosh S., and Karin M. Mapping of the inducible IκBα phosphorylation sites that signal its ubiquitination and degradation. Mol. Cell. Biol. 16 (1996) 1295-1304
10. Ganapathi M.K., Rzewnicki D., Samols D., Jiang S.L., and Kushner I. Effect of combinations of cytokines and hormones on synthesis of serum amyloid A and C-reactive protein in Hep3B cells. J. Immunol. 147 (1991) 1261-1265
11. Gomez-Lechon M.J., Donato M.T., Castell J.V., and Jover R. Human hepatocytes as a tool for studying toxicity and drug metabolism. Curr. Drug. Metab. 4 (2003) 292-312
12. Graham F.L., and Prevec L. Methods for construction of adenovirus vectors. Mol. Biotechnol. 3 (1995) 207-220
13. Ivashchenko Y., Kramer F., Schäfer S., Bucher A., Veit K., Hombach V., Busch A., and Torzewski J. Protein kinase C pathway is involved in transcriptional regulation of C-reactive protein synthesis in human hepatocytes. Arterioscler. Thromb. Vasc. Biol. 25 (2005) 1-7
14. Jialal I., Devaraj S., and Venugopal S.K. C-reactive protein: risk marker or mediator in atherothrombosis?. Hypertension 44 1 (2004) 6-11
15. Jobin C., Panja A., Hellerbrand C., Iimuro Y., Didonato J., Brenner D., and Balfour Sartor R. Inhibition of proinflammatory molecule production by adenovirus-mediated expression of a nuclear factor κB super-repressor in human intestinal epithelial cells. J. Immunol. 160 (1998) 410-418
16. Kleemann R., Gervois P.P., Verschuren L., Staels B., Princen H.M., and Kooistra T. Fibrates downregulate IL-1-stimulated C-reactive protein gene expression in hepatocytes by reducing nuclear p50-NFκB-C/EBPβ complex formation. Blood 101 (2003) 545-551
17. Lekstrom-Himes J., and Xanthopoulos K.G. Biological role of the CCAAT/enhancer-binding protein family of transcription factors. J. Biol. Chem. 273 (1998) 28545-28548
18. Li S.P., and Goldmann N.D. Regulation of human C-reactive protein gene expression by two synergistic IL-6 responsive elements. Biochemistry 35 (1996) 9060-9068
19. Lozanski G., Jiang S.L., Samols D., and Kushner I. C-reactive protein and serum amyloid A mRNA stability following induction by cytokines. Cytokine 8 (1996) 534-540
20. Majello B., Arcone R., Toniatti C., and Ciliberto G. Constitutive and IL-6 induced nuclear factors that interact with the human C-reactive protein promoter. Embo J. 9 (1990) 457-465
21. Manolov D.E., Röcker C., Hombach V., Nienhaus G.U., and Torzewski J. Ultrasensitive confocal fluorescence microscopy of C-reactive protein interacting with FcgammaRIIa. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 2372-2377
22. Mortensen R.F. C-reactive protein, inflammation, and innate immunity. Immunol. Res. 24 (2001) 163-176
23. Mortensen R.F., Osmand A.P., Lint T.F., and Gewurz H. Interaction of C-reactive protein with lymphocytes and monocytes: complement-dependent adherence and phagocytosis. J. Immunol. 117 (1976) 774-781
24. Moshage H.J., Roelofs H.M., van Pelt V.F., Hazenberg B.P., van Leeuwen M.A., Limburg P.C., Aarden L.A., and Yap S.H. The effect of interleukin-1, interleukin-6 and its interrelationship on the synthesis of serum amyloid A and C-reactive protein in primary cultures of adult human hepatocytes. Biochem. Biophys. Res. Commun. 155 (1988) 112-117
25. Natsuka S., Isshiki H., Akira S., and Kishimoto T. Augmentation of haptoglobin production in Hep3B cell line by a nuclear factor NF-IL6. FEBS Lett. 291 (1991) 58-62
26. Ng P.M., Le Saux A., Lee C.M., Tan N.S., Lu J., Thiel S., Ho B., and Ding J.L. C-reactive protein collaborates with plasma lectins to boost immune response against bacteria. Embo J. 25 (2007) 3431-3440
27. Patel D.N., King C.A., Bailey S.R., Holt J.W., Venkatachalam K., Agrawal A., Valente A.J., and Chandrasekar B. Interleukin-17 stimulates C-reactive protein expression in hepatocytes and smooth muscle cells via p38 MAPK and ERK1/2-dependent NF-kappaB and C/EBPbeta activation. J. Biol. Chem. 282 37 (2007) 27229-27238
28. Pearson T.A., Mensah G.A., Alexander R.W., Anderson J.L., Cannon R.O., Criqui M., Fadl Y.Y., Fortmann S.P., Hong Y., Myers G.L., Rifai N., Smith S.C., Taubert K., Tracy R.P., and Vinicor F. Markers of inflammation and cardiovascular disease. Application to clinical and public health practice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 107 (2003) 499-511
29. Pepys M.B., Hirschfield G.M., Tennent G.A., Gallimore J.R., Kahan M.C., Bellotti V., Hawkins P.N., Myers R.M., Smith M.D., Polara A., Cobb A.J., Ley S.V., Aquilina J.A., Robinson C.V., Sharif I., Gray G.A., Sabin C.A., Jenvey M.C., Kolstoe S.E., Thompson D., and Wood S.P. Targeting C-reactive protein for the treatment of cardiovascular disease. Nature 440 (2006) 1217-1221
30. Poli V., and Cortese R. Interleukin 6 induces a liver-specific nuclear protein that binds to the promoter of acute-phase genes. Proc. Natl. Acad. Sci. U.S.A. 86 (1989) 8202-8206
31. Rattazzi M., Puato M., Faggin E., Bertipaglia B., Zambon A., and Pauletto P. C-reactive protein and interleukin-6 in vascular disease: culprits or passive bystanders?. J. Hypertens. 10 (2003) 1787-1803
32. Röcker C., Manolov D.E., Kuzmenkina E.V., Tron K., Slatosch H., Torzewski J., and Nienhaus G.U. Affinity of C-reactive protein towards FcγRI is strongly enhanced by the γ-chain. Am. J. Pathol. 170 (2007) 755-763
33. Sabatine M.S., Morrow D.A., Jablonski K.A., Rice M.M., Warnica J.W., Domanski M.J., Hsia J., Gersh B.J., Rifai N., Ridker P.M., Pfeffer M.A., and Braunwald E. PEACE investigators. Prognostic significance of the Centers for Disease Control/American Heart Association high-sensitivity C-reactive protein cut points for cardiovascular and other outcomes in patients with stable coronary artery disease. Circulation 115 (2007) 1528-1536
34. Scirica B.M., and Morrow D.A. Is C-reactive protein an innocent bystander or proatherogenic culprit? The verdict is still out. Circulation 113 (2006) 2128-2134
35. Stahl N., Boulton T.G., Farrugella T., Ip N.Y., Davis S., Witthuhn B.A., Quelle F.W., Silvennoinen O., Barbieri G., and Pellegrini S. Association and activation of Jak-Tyk kinases by CNTF-LIF-OSM-IL-6β receptor components. Science 263 (1994) 92-95
36. Thompson J.E., Cubbon R.M., Cummings R.T., Wicker L.S., Frankshun R., Cunningham B.R., Cameron P.M., Meinke P.T., Liverton N., Weng Y., and DeMartino J.A. Photochemical preparation of a pyridone containing tetracycle: a JAK protein kinase inhibitor. Bioorg. Med. Chem. Lett. 12 (2002) 1219-1223
37. Toniatti C., Demartis A., Monaci P., Nicosia A., and Ciliberto G. Synergistic transactivation of the human C-reactive protein promoter by transcription factor HNF-1 binding at two distinct sites. Embo J. 9 (1990) 4467-4475
38. Torzewski J. C-reactive protein and atherogenesis: new insights from established animal models. Am. J. Pathol. 167 (2005) 923-925
39. Venugopal S.K., Devaraj S., and Jialal I. Effect of C-reactive protein on vascular cells: evidence for a proinflammatory, proatherogenic role. Curr. Opin. Nephrol. Hypertens. 14 1 (2005) 33-37
40. Volanakis J.E. Complement activation by C-reactive protein complexes. Ann. NY Acad. Sci. 389 (1982) 235-250
41. Yamazaki S., Muta T., Matsuo S., and Takeshige K. Stimulus-specific induction of a novel nuclear factor-κB regulator, Iκ-B-zeta, via Toll/Interleukin-1 receptor is mediated by mRNA stabilization. J. Biol. Chem. 280 (2005) 1678-1687
42. Zhang D., Jiang S.L., Rzewnicki D., Samols D., and Kushner I. The effect of interleukin-1 on C-reactive protein expression in Hep3B cells is exerted at the transcriptional level. Biochem. J. 310 (1995) 143-148
43. Zhang D., Sun M., Samols D., and Kushner I. STAT3 participates in transcriptional activation of the C-reactive protein gene by interleukin-6. J. Biol. Chem. 27 (1996) 9503-9509