Proteinase-activated receptors induce interleukin-8 expression by intestinal epithelial cells through ERK/RSK90 activation and histone acetylation

FASEB Journal

Volumn 24, Issue 6, 2010, Pages 1971-1980

  Wang, Hongying ^a,b   Moreau, France ^a   Hirota, Christina L ^a   MacNaughton, Wallace K ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

Chemokine; Epithelium; Inflammation; NF B; Transcription

Indexed keywords

HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE 2; I KAPPA B; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN; PROTEIN P300; PROTEINASE ACTIVATED RECEPTOR 1; PROTEINASE ACTIVATED RECEPTOR 2; PROTIEN P50; S6 KINASE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ACETYLATION; ARTICLE; CELL STRAIN HT29; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION;

ACETYLATION; BLOTTING, WESTERN; CELLS, CULTURED; COLON; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; HISTONE ACETYLTRANSFERASES; HISTONES; HUMANS; I-KAPPA B PROTEINS; IMMUNOPRECIPITATION; INTERLEUKIN-8; LUCIFERASES; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NF-KAPPA B; P300-CBP TRANSCRIPTION FACTORS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RECEPTOR, PAR-1; RECEPTOR, PAR-2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; RNA, MESSENGER; TRANSFECTION;

EID: 77953494803     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-137646     Document Type: Article

References (48)

1. Fredriksson, R., and Schioth, H. B. (2005) The repertoire of G-protein-coupled receptors in fully sequenced genomes. Mol. Pharmacol. 67, 1414-1425
2. Macfarlane, S. R., Seatter, M. J., Kanke, T., Hunter, G. D., and Plevin, R. (2001) Proteinase-activated receptors. Pharmacol. Rev. 53, 245-282
3. Hollenberg, M. D., and Compton, S. J. (2002) International Union of Pharmacology. XXVIII. Proteinase-activated receptors. Pharmacol. Rev. 54, 203-217
4. MacNaughton, W. K. (2005) Epithelial effects of proteinase-activated receptors in the gastrointestinal tract. Mem. Inst. Oswaldo Cruz 100(Suppl. 1), 211-215 (Pubitemid 40685466)
5. Vergnolle, N., Cellars, L., Mencarelli, A., Rizzo, G., Swaminathan, S., Beck, P., Steinhoff, M., Andrade-Gordon, P., Bunnett, N. W., Hollenberg, M. D., Wallace, J. L., Cirino, G., and Fiorucci, S. (2004) A role for proteinase-activated receptor-1 in inflammatory bowel diseases. J. Clin. Invest. 114, 1444-1456
6. Kim, J. A., Choi, S. C., Yun, K. J., Kim, D. K., Han, M. K., Seo, G. S., Yeom, J. J., Kim, T. H., Nah, Y. H., and Lee, Y. M. (2003) Expression of protease-activated receptor 2 in ulcerative colitis. Inflamm. Bowel Dis. 9, 224-229
7. Le Berre, N., Heresbach, D., Kerbaol, M., Caulet, S., Bretagne, J. F., Chaperon, J., Gosselin, M., and Ramee, M. P. (1995) Histological discrimination of idiopathic inflammatory bowel disease from other types of colitis. J. Clin. Pathol. 48, 749-753
8. Izzo, R. S., Witkon, K., Chen, A. I., Hadjiyane, C., Weinstein, M. I., and Pellecchia, C. (1992) Interleukin-8 and neutrophil markers in colonic mucosa from patients with ulcerative colitis. Am. J. Gastroenterol. 87, 1447-1452
9. Mazzucchelli, L., Hauser, C., Zgraggen, K., Wagner, H., Hess, M., Laissue, J. A., and Mueller, C. (1994) Expression of interleukin-8 gene in inflammatory bowel disease is related to the histological grade of active inflammation. Am. J. Pathol. 144, 997-1007 (Pubitemid 24160640)
10. Hou, L., Kapas, S., Cruchley, A. T., Macey, M. G., Harriott, P., Chinni, C., Stone, S. R., and Howells, G. L. (1998) Immunolocalization of protease-activated receptor-2 in skin: receptor activation stimulates interleukin-8 secretion by keratinocytes in vitro. Immunology 94, 356-362
11. Asokananthan, N., Graham, P. T., Fink, J., Knight, D. A., Bakker, A. J., McWilliam, A. S., Thompson, P. J., and Stewart, G. A. (2002) Activation of protease-activated receptor (PAR)-1, PAR-2, and PAR-4 stimulates IL-6, IL-8, and prostaglandin E2 release from human respiratory epithelial cells. J. Immunol. 168, 3577-3585 (Pubitemid 34250428)
12. Zhao, D., Keates, A. C., Kuhnt-Moore, S., Moyer, M. P., Kelly, C. P., and Pothoulakis, C. (2001) Signal transduction pathways mediating neurotensin-stimulated interleukin-8 expression in human colonocytes. J. Biol. Chem. 276, 44464-44471
13. Boyes, J., Byfield, P., Nakatani, Y., and Ogryzko, V. (1998) Regulation of activity of the transcription factor GATA-1 by acetylation. Nature 396, 594-598 (Pubitemid 28563723)
14. Wang, H., Wen, S., Bunnett, N. W., Leduc, R., Hollenberg, M. D., and MacNaughton, W. K. (2008) Proteinase-activated receptor-2 induces cyclooxygenase-2 expression through catenin and cyclic AMP-response element-binding protein. J. Biol. Chem. 283, 809-815
15. Wang, H., and MacNaughton, W. K. (2005) Overexpressed beta-catenin blocks nitric oxide-induced apoptosis in colonic cancer cells. Cancer Res. 65, 8604-8607
16. Mukaida, N., Shiroo, M., and Matsushima, K. (1989) Genomic structure of the human monocyte-derived neutrophil chemotactic factor IL-8. J. Immunol. 143, 1366-1371 (Pubitemid 19211374)
17. Wang, H., Ubl, J. J., Stricker, R., and Reiser, G. (2002) Thrombin (PAR-1)-induced proliferation in astrocytes via MAPK involves multiple signaling pathways. Am. J. Physiol. Cell Physiol. 283, C1351-C1364 (Pubitemid 35178427)
18. Davies, S. P., Reddy, H., Caivano, M., and Cohen, P. (2000) Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351, 95-105
19. Chen, R. H., Sarnecki, C., and Blenis, J. (1992) Nuclear localization and regulation of erk- and rsk-encoded protein kinases. Mol. Cell. Biol. 12, 915-927
20. Zhang, L., Ma, Y., Zhang, J., Cheng, J., and Du, J. (2005) A new cellular signaling mechanism for angiotensin II activation of NF-κB: An IκB-independent, RSK-mediated phosphorylation of p65. Arterioscler. Thromb. Vasc. Biol. 25, 1148-1153
21. Rogler, G., and Andus, T. (1998) Cytokines in inflammatory bowel disease. World J. Surg. 22, 382-389
22. Brannigan, A. E., O'Connell, P. R., Hurley, H., O'Neill, A., Brady, H. R., Fitzpatrick, J. M., and Watson, R. W. (2000) Neutrophil apoptosis is delayed in patients with inflammatory bowel disease. Shock 13, 361-366
23. Koutroubakis, I. E., Tsiolakidou, G., Karmiris, K., and Kouroumalis, E. A. (2006) Role of angiogenesis in inflammatory bowel disease. Inflamm. Bowel. Dis. 12, 515-523
24. Danese, S., Scaldaferri, F., Vetrano, S., Stefanelli, T., Graziani, C., Repici, A., Ricci, R., Sgambato, A., Straface, G., Malesci, A., Fiocchi, C., and Rutella, S. (2007) Critical role of the CD40-CD40 ligand pathway in governing mucosal inflammation-driven angiogenesis in inflammatory bowel disease. Gut 14, 649-666
25. Heidemann, J., Ogawa, H., Dwinell, M. B., Rafiee, P., Maaser, C., Gockel, H. R., Otterson, M. F., Ota, D. M., Lugering, N., Domschke, W., and Binion, D. G. (2003) Angiogenic effects of interleukin 8 (CXCL8) in human intestinal microvascular endothelial cells are mediated by CXCR2. J. Biol. Chem. 278, 8508-8515
26. Gunter, M. J., Canzian, F., Landi, S., Chanock, S. J., Sinha, R., and Rothman, N. (2006) Inflammation-related gene polymorphisms and colorectal adenoma. Cancer Epidemiol. Biomarkers Prev. 15, 1126-1131
27. Eckmann, L., Jung, H. C., Schurer-Maly, C., Panja, A., Morzycka-Wroblewska, E., and Kagnoff, M. F. (1993) Differential cytokine expression by human intestinal epithelial cell lines: regulated expression of interleukin 8. Gastroenterology 105, 1689-1697 (Pubitemid 24002784)
28. Grimm, M. C., Elsbury, S. K., Pavli, P., and Doe, W. F. (1996) Interleukin 8: cells of origin in inflammatory bowel disease. Gut 38, 90-98 (Pubitemid 26022524)
29. Tantivejkul, K., Loberg, R. D., Mawocha, S. C., Day, L. L., John, L. S., Pienta, B. A., Rubin, M. A., and Pienta, K. J. (2005) PAR1-mediated NFκB activation promotes survival of prostate cancer cells through a Bcl-xL-dependent mechanism. J. Cell. Biochem. 96, 641-652
30. Page, K., Hughes, V. S., Odoms, K. K., Dunsmore, K. E., and Hershenson, M. B. (2005) German cockroach proteases regulate interleukin-8 expression via nuclear factor for interleukin-6 in human bronchial epithelial cells. Am. J. Respir. Cell Mol. Biol. 32, 225-231
31. Rothwarf, D. M., and Karin, M. (1999) The NF-κB activation pathway: a paradigm in information transfer from membrane to nucleus. Sci. STKE. 1999, RE1
32. Yoza, B. K., Hu, J. Y., and McCall, C. E. (1996) Protein-tyrosine kinase activation is required for lipopolysaccharide induction of interleukin 1β and NFκB activation, but not NFκB nuclear translocation. J. Biol. Chem. 271, 18306-18309
33. Beyaert, R., Cuenda, A., Vanden Berghe, W., Plaisance, S., Lee, J. C., Haegeman, G., Cohen, P., and Fiers, W. (1996) The p38/RK mitogen-activated protein kinase pathway regulates interleukin-6 synthesis response to tumor necrosis factor. EMBO J. 15, 1914-1923 (Pubitemid 26119694)
34. Finco, T. S., Westwick, J. K., Norris, J. L., Beg, A. A., Der, C. J., and Baldwin, A. S., Jr. (1997) Oncogenic Ha-Ras-induced signaling activates NF-κB transcriptional activity, which is required for cellular transformation. J. Biol. Chem. 272, 24113-24116
35. Schmitz, M. L., Bacher, S., and Kracht, M. (2001) I κB-independent control of NF-κB activity by modulatory phosphorylations. Trends Biochem. Sci. 26, 186-190
36. Merika, M., Williams, A. J., Chen, G., Collins, T., and Thanos, D. (1998) Recruitment of CBP/p300 by the IFN β enhanceosome is required for synergistic activation of transcription. Mol. Cell 1, 277-287 (Pubitemid 128378668)
37. Vanden Berghe, W., De Bosscher, K., Boone, E., Plaisance, S., and Haegeman, G. (1999) The nuclear factor-κB engages CBP/p300 and histone acetyltransferase activity for transcriptional activation of the interleukin-6 gene promoter. J. Biol. Chem. 274, 32091-32098 (Pubitemid 129503803)
38. Jamaluddin, M., Wang, S., Boldogh, I., Tian, B., and Brasier, A. R. (2007) TNF-α-induced NF-κB/RelA Ser(276) phosphorylation and enhanceosome formation is mediated by an ROS-dependent PKAc pathway. Cell. Signal. 19, 1419-1433
39. Nicholas, C., Batra, S., Vargo, M. A., Voss, O. H., Gavrilin, M. A., Wewers, M. D., Guttridge, D. C., Grotewold, E., and Doseff, A. I. (2007) Apigenin blocks lipopolysaccharide-induced lethality in vivo and proinflammatory cytokines expression by inactivating NF-κB through the suppression of p65 phosphorylation. J. Immunol. 179, 7121-7127
40. Kefaloyianni, E., Gaitanaki, C., and Beis, I. (2006) ERK1/2 and p38-MAPK signalling pathways, through MSK1, are involved in NF-κB transactivation during oxidative stress in skeletal myoblasts. Cell. Signal. 18, 2238-2251
41. Bohuslav, J., Chen, L. F., Kwon, H., Mu, Y., and Greene, W. C. (2004) p53 induces NF-κB activation by an IκB kinase-independent mechanism involving phosphorylation of p65 by ribosomal S6 kinase 1. J. Biol. Chem. 279, 26115-26125
42. Chen, L. F., and Greene, W. C. (2004) Shaping the nuclear action of NF-κB. Nat. Rev. Mol. Cell. Biol. 5, 392-401
43. Ashburner, B. P., Westerheide, S. D., and Baldwin, A. S., Jr. (2001) The p65 (RelA) subunit of NF-κB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol. Cell. Biol. 21, 7065-7077
44. Tomita, K., Barnes, P. J., and Adcock, I. M. (2003) The effect of oxidative stress on histone acetylation and IL-8 release. Biochem. Biophys. Res. Commun. 301, 572-577
45. Taplick, J., Kurtev, V., Kroboth, K., Posch, M., Lechner, T., and Seiser, C. (2001) Homo-oligomerisation and nuclear localisation of mouse histone deacetylase 1. J. Mol. Biol. 308, 27-38
46. Mariadason, J. M. (2008) HDACs and HDAC inhibitors in colon Cancer. Epigenetics 3, 28-37
47. Rahman, I., Marwick, J., and Kirkham, P. (2004) Redox modulation of chromatin remodeling: impact on histone acetylation and deacetylation, NF-κB and pro-inflammatory gene expression. Biochem. Pharmacol. 68, 1255-1267
48. Chiu, Y. C., Fong, Y. C., Lai, C. H., Hung, C. H., Hsu, H. C., Lee, T. S., Yang, R. S., Fu, W. M., and Tang, C. H. (2008) Thrombin-induced IL-6 production in human synovial fibroblasts is mediated by PAR1, phospholipase C, protein kinase C alpha, c-Src, NF-κB and p300 pathway. Mol. Immunol. 45, 1587-1599