Abstract
Background
Interleukin (IL)-17 is a newly identified T-cell-specific cytokine. In this study, we investigated the effects of IL-17 on colony-stimulating factor (CSF) release in human colonic subepithelial myofibroblasts (SEMFs).
Methods
CSF release and mRNA expression were determined by enzyme-linked immunosorbent assay (ELISA) and Northern blotting, respectively. Nuclear factor (NF)-κB- and activating protein (AP-1)-DNA binding activities were evaluated by electrophoretic gel mobility shift assays (EMSAs).
Results
Unstimulated cells secreted a small amount of granulocyte G- and granulocyte/macrophage (GM)-CSF, and a considerable amount of M-CSF. IL-17 weakly enhanced G-CSF release, but did not affect GM- and M-CSF release. IL-17 selectively enhanced tumor necrosis factor (TNF)-α-induced G- and GM-CSF release. The combination of IL-17 plus TNF-α induced a marked increase in NF-κB- and AP-1-DNA binding activities. The adenovirus-mediated transfer of a stable form of IκBα and/or a dominant negative mutant of c-Jun markedly inhibited the IL-17 plus TNF-α-induced G- and GM-CSF mRNA expression. Furthermore, a stability study showed that IL-17 plus TNF-α markedly enhanced the stability of G- and GM-CSF mRNA.
Conclusions
IL-17 augments TNF-α-induced G- and GM-CSF release via transcriptional and posttranscriptional mechanisms.
Similar content being viewed by others
References
PS Crosier SC Clark (1992) ArticleTitleBasic biology of the hematopoietic growth factors Semin Oncol 19 349–61 Occurrence Handle1380728
F Fossiez J Banchereau R Murry C van Kooten P Garrone S Lebecque (1998) ArticleTitleInterleukin-17 Int Rev Immunol 16 541–51 Occurrence Handle9646176
Z Yao SL Painter WC Fanslow D Ulrich BM Macduff MK Spriggs RJ Armitage (1995) ArticleTitleHuman IL-17: a novel cytokine derived from T cells J Immunol 155 5483–6 Occurrence Handle7499828
J Kennedy DL Rossi SM Zurawski F Vega SuffixJr RA Kastelein JL Wagner et al. (1996) ArticleTitleMouse IL-17: a cytokine preferentially expressed by αβ TCR+ CD4−CD8− T cells J Interferon Cytokine Res 16 611–7 Occurrence Handle8877732
C Albanesi C Scarponi A Cavani M Federici F Nasorri G Girolomoni (2000) ArticleTitleInterleukin-17 is produced by both Th1 and Th2 lymphocytes, and modulates interferon-γ- and interleukin-4-induced activation of human keratinocytes J Invest Dermatol 115 81–7 Occurrence Handle10.1046/j.1523-1747.2000.00041.x Occurrence Handle10886512
HC Shin N Benbernou S Esnault M Guenounou (1999) ArticleTitleExpression of IL-17 in human memory CD45RO+ T lymphocytes and its regulation by protein kinase A pathway Cytokine 11 257–66 Occurrence Handle10.1006/cyto.1998.0433 Occurrence Handle10328864
M Chabaud F Fossiez JL Taupin P Miossec (1998) ArticleTitleEnhancing effects of IL-17 on IL-1-induced IL-6 and leukemia inhibitory factor production by rheumatoid arthritis synoviocytes and its regulation by Th2 cytokines J Immunol 161 409–14 Occurrence Handle9647250
DV Jovanovic JA Di Battista PJ Martel FC Jolicoeur Y He M Zhang et al. (1998) ArticleTitleIL-17 stimulates the production and expression of proinflammatory cytokines, IL-1 and TNF-α by human macrophages J Immunol 60 3513–21
C Albanesi A Cavani G Girolomoni (1999) ArticleTitleIL-17 is produced by Nickel-specific T lymphocytes and regulates ICAM-1 expression and chemokine production in human keratinocytes: synergistic or antagonistic effects with IFN-γ and TNF-α J Immunol 162 494–502 Occurrence Handle9886425
M Shimada A Andoh K Hata K Tasaki Y Araki Y Fujiyama et al. (2002) ArticleTitleIL-6 secretion by human pancreatic periacinar myofibroblasts in response to inflammatory mediators J Immunol 168 861–8 Occurrence Handle11777983
XY Cai J Gommol-CP L Justice SK Narula JS Fine (1998) ArticleTitleReglation of granulocyte colony-stimulating factor gene expression by interleukin-17 Immunol Lett 62 51–8 Occurrence Handle10.1016/S0165-2478(98)00027-3 Occurrence Handle9672148
CE Jones K Chan (2002) ArticleTitleInterleukin-17 stimulates the expression of interleukin-8, growth-related oncogene-, and granulocyte-colony-stimulating factor by human airway epithelial cells Am J Respir Cell Mol Biol 26 748–53 Occurrence Handle12034575
F Fossiez O Djossou P Chomarat L Flores-Romo S Ait-Yahia C Maat et al. (1996) ArticleTitleT cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines J Exp Med 183 2593–603 Occurrence Handle10.1084/jem.183.6.2593 Occurrence Handle8676080
P Schwarzenberger W Huang P Ye P Oliver M Manuel Z Zhang et al. (2000) ArticleTitleRequirement of endogenous stem cell factor and granulocyte-colony-stimulating factor for IL-17-mediated granulopoiesis J Immunol 164 4783–9 Occurrence Handle10779785
P Schwarzenberger JK Kolls (2002) ArticleTitleInterleukin-17: an example for gene therapy as a tool to study cytokine mediated regulation of hematopoiesis J Cell Biochem Suppl 38 88–95 Occurrence Handle10.1002/jcb.10054 Occurrence Handle12046855
P Schwarzenberger VR Russa A Miller P Ye W Huang A Zieske et al. (1998) ArticleTitleIL-17 stimulates granulopoiesis in mice: use of an alternate, novel gene therapy-derived method for in vivo evaluation of cytokines J Immunol 161 6368–89 Occurrence Handle9834127
P Schwarzenberger W Huang P Oliver P Byrne V La Russa Z Zhang et al. (2001) ArticleTitleIL-17 mobilizes peripheral stem cells with short- and long-term repopulating ability in mice J Immunol 167 2081–6 Occurrence Handle11489991
DW Powell RC Mifflin JD Valentich SE Crowe JI Saada AB West I Myofibroblasts (1999) ArticleTitleParacrine cells important in health and disease Am J Physiol 277 C1–C9 Occurrence Handle10409103
DW Powell RC Mifflin JD Valentich SE Crowe JI Saada AB West (1999) ArticleTitleII. Intestinal subepithelial myofibroblasts Am J Physiol 277 C183–C201 Occurrence Handle10444394
K Hata A Andoh M Shimada S Fujino S Bamba Y Araki et al. (2002) ArticleTitleIL-17 stimulates inflammatory responses via NF-kappaB and MAP kinase pathways in human colonic myofibroblasts Am J Physiol Gastrointest Liver Physiol 282 G1035–44 Occurrence Handle12016129
A Andoh S Fujino S Bamba Y Araki T Okuno T Bamba et al. (2002) ArticleTitleIL-17 selectively down-regulates TNF-α-induced RANTES gene expression in human colonic subepithelial myofibroblasts J Immunol 169 1683–7 Occurrence Handle12165487
S Bamba A Andoh H Yasui Y Araki T Bamba Y Fujiyama (2003) ArticleTitleMatrix metalloproteinase-3 secretion from human colonic subepithelial myofibroblasts: role of interleukin-17 J Gastroenterol 38 548–54 Occurrence Handle12825130
YR Mahida J Beltinger S Marh M Goke T Gray DK Podolsky et al. (1997) ArticleTitleAdult human colonic subepithelial myofibroblasts express extracellular matrix proteins and cyclooxygenase-1 and -2 Am J Physiol 273 G1341–8 Occurrence Handle9435560
S Nagata M Tsuchiya S Asano Y Kaziro T Yamazaki O Yamamoto et al. (1986) ArticleTitleMolecular cloning and expression of cDNA for human granulocyte colony-stimulating factor Nature 319 415–8 Occurrence Handle10.1038/319415a0 Occurrence Handle3484805
F Lee T Yokota T Otsuka L Gemmell N Larson J Luh et al. (1985) ArticleTitleIsolation of cDNA for human granulocyte-macrophage colony-stimulating factor by functional expression in mammalian cells Proc Natl Acad Sci USA 82 4360–4 Occurrence Handle3925454
M Takahashi T Hirato M Takano T Nishida K Nagamura T Kamogashira et al. (1989) ArticleTitleAmino-terminal region of human macrophage colony-stimulating factor (M-CSF) is sufficient for its in vitro biological activity: molecular cloning and expression of carboxyl-terminal deletion mutants of human M-CSF Biochem Biophys Res Commun 161 892–901 Occurrence Handle10.1016/0006-291X(89)92683-1 Occurrence Handle2660794
A Andoh H Takaya J Makino H Sato S Bamba Y Araki et al. (2001) ArticleTitleCooperation of interleukin-17 and interferon-gamma on chemokine secretion in human fetal intestinal epithelial cells Clin Exp Immunol 125 56–63 Occurrence Handle10.1046/j.1365-2249.2001.01588.x Occurrence Handle11472426
JD Dignam RM Lebovitz RG Roeder (1983) ArticleTitleAccurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei Nucleic Acids Res 11 1475–89 Occurrence Handle6828386
H Obara A Takayanagi J Hirahashi K Tanaka G Wakabayashi K Matsumoto et al. (2000) ArticleTitleOverexpression of truncated IκBα induces TNF-α-dependent apoptosis in human vascular smooth muscle cells Arterioscler Thromb Vasc Biol 20 2198–204 Occurrence Handle11031204
H Yasumoto S Kim Y Zhan H Miyazaki M Hoshiga Y Kaneda et al. (2001) ArticleTitleDominant negative c-jun gene transfer inhibits vascular smooth muscle cell proliferation and neointimal hyperplasia in rats Gene Ther 8 1682–9 Occurrence Handle10.1038/sj.gt.3301590 Occurrence Handle11892835
M Nishizawa M Tsuchiya R Watanabe-Fukunaga S Nagata (1990) ArticleTitleMultiple elements in the promoter of granulocyte colony-stimulating factor gene regulate its constitutive expression in human carcinoma cells J Biol Chem 265 5897–902 Occurrence Handle1690717
SM Dunn LS Coles RK Lang S Gerondakis MA Vadas MF Shannon (1994) ArticleTitleRequirement for nuclear factor (NF)-κB p65 and NF-interleukin-6 binding elements in the tumor necrosis factor response region of the granulocyte colony-stimulating factor promoter Blood 83 2469–79 Occurrence Handle7513199
M Musso P Ghiorzo P Fiorentini R Giuffrida P Ciotti C Garre et al. (1996) ArticleTitleAn upstream positive regulatory element in human GM-CSF promoter is recognized by NF-κB/Rel family members Biochem Biophys Res Commun 223 64–72 Occurrence Handle10.1006/bbrc.1996.0847 Occurrence Handle8660380
F Jenkins PN Cockerill D Bohmann MF Shannon (1995) ArticleTitleMultiple signals are required for function of the human granulocyte-macrophage colony-stimulating factor gene promoter in T cells J Immunol 155 1240–51 Occurrence Handle7636192
R Schreck PA Baeuerle (1990) ArticleTitleNF-κB as inducible transcriptional activator of the granulocyte-macrophage colony-stimulating factor gene Mol Cell Biol 10 1281–6 Occurrence Handle2406568
J Ye X Zhang Z Dong (1996) ArticleTitleCharacterization of the human granulocyte-macrophage colony-stimulating factor gene promoter: an AP1 complex and an Sp1-related complex transactivate the promoter activity that is suppressed by a YY1 complex Mol Cell Biol 16 157–67 Occurrence Handle8524292
CY Wang AG Bassuk LH Boise CB Thompson R Bravo JM Leiden (1994) ArticleTitleActivation of the granulocyte-macrophage colony-stimulating factor promoter in T cells requires cooperative binding of Elf-1 and AP-1 transcription factors Mol Cell Biol 14 1153–9 Occurrence Handle8289796
GQ Yao BH Sun KL Insogna EC Weir (2000) ArticleTitleNuclear factor-kappaB p50 is required for tumor necrosis factor-alpha-induced colony-stimulating factor-1 gene expression in osteoblasts Endocrinology 141 2914–22 Occurrence Handle10.1210/en.141.8.2914 Occurrence Handle10919279
PJ Kamthong FM Wu MC Wu (2000) ArticleTitlecAMP attenuates interleukin-1-stimulated macrophage colony-stimulating factor (M-CSF) expression Biochem J 350 115–22 Occurrence Handle10.1042/0264-6021:3500115 Occurrence Handle10926834
BW Konicek X Xia T Rajavashisth MA Harrington (1998) ArticleTitleRegulation of mouse colony-stimulating factor-1 gene promoter activity by AP1 and cellular nucleic acid-binding protein DNA Cell Biol 17 799–809 Occurrence Handle9778039
A Cuenda J Rouse YN Doza R Meier P Cohen TF Gallagher et al. (1995) ArticleTitleSB203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1 FEBS Lett 364 229–33 Occurrence Handle10.1016/0014-5793(95)00357-F Occurrence Handle7750577
G Shaw R Kamen (1986) ArticleTitleA conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation Cell 46 659–67 Occurrence Handle10.1016/0092-8674(86)90341-7 Occurrence Handle3488815
CY Chen AB Shyu (1995) ArticleTitleAU-rich elements: characterization and importance in mRNA degradation Trends Biochem Sci 20 465–70 Occurrence Handle10.1016/S0968-0004(00)89102-1 Occurrence Handle8578590
R Winzen G Gowrishankar F Bollig N Redich K Resch H Holtmann (2004) ArticleTitleDistinct domains of AU-rich elements exert different functions in mRNA destabilization and stabilization by p38 mitogen-activated protein kinase or HuR Mol Cell Biol 24 4835–47 Occurrence Handle10.1128/MCB.24.11.4835-4847.2004 Occurrence Handle15143177
M Nishizawa N Wakabayashi-Ito S Nagata (1991) ArticleTitleMolecular cloning of cDNA and a chromosomal gene encoding GPE1-BP, a nuclear protein which binds to granulocyte colony-stimulating factor promoter element 1 FEBS Lett 282 95–7 Occurrence Handle10.1016/0014-5793(91)80452-9 Occurrence Handle1709121
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Andoh, A., Yasui, H., Inatomi, O. et al. Interleukin-17 augments tumor necrosis factor-α-induced granulocyte and granulocyte/macrophage colony-stimulating factor release from human colonic myofibroblasts. J Gastroenterol 40, 802–810 (2005). https://doi.org/10.1007/s00535-005-1632-x
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/s00535-005-1632-x