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Infection and Immunity, April 2006, p. 2482-2486, Vol. 74, No. 4
0019-9567/06/$08.00+0     doi:10.1128/IAI.74.4.2482-2486.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Chlamydiae Modulate Gamma Interferon, Interleukin-1ß, and Tumor Necrosis Factor Alpha Receptor Expression in HeLa Cells

Kari Ann Shirey and Joseph M. Carlin*

Department of Microbiology, Miami University, Oxford, Ohio

Received 17 November 2005/ Returned for modification 23 December 2005/ Accepted 30 January 2006


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ABSTRACT
 
Chlamydia psittaci was found to modulate receptor expression for the cytokine receptors that are involved in the synergistic induction of indoleamine dioxygenase in epithelial cells. Increases in receptor expression were seen even with inactivated Chlamydia, suggesting that chlamydial antigens and not products of infection are important for up-regulating cytokine receptor expression.


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TEXT
 
Although Chlamydia may be sheltered from antibody-mediated immune responses, it is still susceptible to cell-mediated immune responses. Gamma interferon (IFN-{gamma}) induces several antimicrobial mechanisms, including the production of nitrogen oxide synthase (1) and reactive oxygen species (19) and the breakdown of L-tryptophan by indoleamine 2,3-dioxygenase (IDO). IDO has been shown to restrict the growth of several pathogens, including Toxoplasma, group B Streptococcus, and Chlamydia species (3, 17, 21). The regulation of IDO can be influenced by other cytokines and immunomodulating agents, such as interleukin-1ß (IL-1ß), tumor necrosis factor alpha (TNF-{alpha}), and lipopolysaccharide (LPS), each of which increases the amount of IDO activity in IFN-{gamma}-induced cells (5, 6, 12). This increase in IDO activity enhances the antimicrobial effect of IFN-{gamma} in a dose-dependent manner (5, 26, 30), in which the amount of antichlamydial activity is proportional to the amount of IDO activity induced. Changes in cytokine receptor expression are also essential to synergistic IDO induction. IFN-{gamma}, TNF-{alpha}, and IL-1ß each increase the expression of receptors for the other cytokines (15, 27), rendering the cell more sensitive to their respective cytokines and thereby requiring less of each cytokine for IDO induction. Inasmuch as LPS can also up-regulate IFN-{gamma}-induced IDO activity (6, 12), the objective of this study was to characterize the effect that Chlamydia psittaci has on the expression of these cytokine receptors in epithelial cells. The modified LPS structure of various chlamydial species contributes to its weaker endotoxic activity (11, 13, 20). Furthermore, the structure possesses only minor variations between species, especially among different serotypes. This similarity, along with C. psittaci's ability to infect various cells, including the epithelial cell targets of Chlamydia trachomatis, may provide insight into how other Chlamydia may interact with the host (4, 18), particularly with the Toll-like receptor (TLR) system. While intact chlamydiae have been shown to interact predominantly with TLR2, chlamydial HSP60 and LPS may interact with both TLR2 and TLR4.

C. psittaci strain 6BC was propagated as described previously (10). To establish whether C. psittaci modulates the expression of various cytokine receptors, HeLa 229 cells (105 cells/ml) were cultivated in minimal essential medium containing 10% fetal bovine serum alone or infected with one 50% infective dose (multiplicity of infection [MOI], ~2) of C. psittaci for 24 h at 37°C in 5% CO2, at which time the cells were harvested by gentle scraping with rubber policemen. The amount of chlamydial infection and changes in cytokine receptor expression were detected by using a genus-specific antibody to chlamydial LPS (MAB8321; Chemicon, Temecula, CA) and anti-IFN-{gamma} receptor (IFN-{gamma}R; Fitzgerald Inc., Ireland), anti-IL-1 receptor I (IL-1R; Rockland Immunochemicals, Gillbertsville, PA), or anti-TNF receptor (TNFR; R&D Systems, Minneapolis, MN) antibodies by incubating for 1 h with primary antibody and 1 h with fluorescein isothiocyanate- or phycoerythrin-conjugated secondary antibodies (Sigma, St. Louis, MO). The percentage of infected cells that were detected by flow cytometry was in agreement with that determined by visual inspection of Giemsa-stained cells. All cells were analyzed by two-color flow cytometry on a FACScan flow cytometer (Becton Dickinson, San Jose, CA). Four-quadrant fluorescence-activated cytometric analysis revealed that, in cultures receiving viable or inactivated chlamydiae, all cell populations, infected and uninfected, increased IFN-{gamma}R{alpha} expression relative to cells that were cultivated in medium alone (Fig. 1A). Similar patterns were observed for the expression of IL-1R and TNFR (data not shown), in which all cells within cultures receiving chlamydiae (viable or inactivated) exhibited increased receptor expression. In another experiment, some cultures received cytokine (IFN-{gamma} from Biogen, Cambridge, MA, or IL-1ß from R&D Systems) at concentrations that had been previously determined to induce maximal cytokine receptor expression (15, 27); IL-1ß (100 ng/ml) was used to increase IFN-{gamma}R expression, while IFN-{gamma} (10 ng/ml) was used to increase IL-1R and TNFR expression. While treatment of cells with IL-1ß significantly increased the expression of IFN-{gamma}R{alpha}, the ligand binding chain, above the baseline that was obtained from cells cultivated in medium alone (P < 0.05, Dunnett's test), C. psittaci infection further increased (P < 0.01) IFN-{gamma}R{alpha} expression 2.9-fold over that induced by treatment with IL-1ß, resulting in an 11.2-fold increase over the baseline expression of IFN-{gamma}R{alpha} (Fig. 1B, top panel). The effect that Chlamydia had on the expression of IFN-{gamma}Rß was also examined because it is the signal-transducing chain. If Chlamydia increased the expression of the ligand binding chain with little or no effect on the signal-transducing chain, it could result in diminished IFN-{gamma}-induced responses. However, infection resulted in an increase in IFN-{gamma}Rß expression similar to that seen with IFN-{gamma}R{alpha} (data not shown). The same trend was observed with both the IL-1R and TNFR (Fig. 1B, middle and bottom panels, respectively). Treatment with IFN-{gamma} resulted in increased expression of both IL-1R and TNFR above baseline levels (P < 0.05). Furthermore, infection with C. psittaci significantly increased (P < 0.01) the expression of IL-1R and TNFR 2.6-fold and 2.1-fold, respectively, over expression by IFN-{gamma}-stimulated cells and 5.4- fold and 4.7-fold, respectively, over medium-treated cells.


Figure 1
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  		FIG. 1. Up-regulation of cytokine receptor expression by Chlamydia. (A) HeLa 229 cells were cultivated in medium or with C. psittaci (live, heat-inactivated [{Delta}H], or UV-inactivated [UV]) for 24 h and analyzed for IFN-{gamma}R{alpha} expression and chlamydiae by two-color flow cytometry. The numbers in each quadrant indicate the percentage of cells in that quadrant. (B) Cytokine receptor increase by Chlamydia is antigen and not infection dependent. HeLa 229 cells were cultivated with medium, cytokine (top panel, IL-1ß at 100 ng/ml; middle and bottom panels, IFN-{gamma} at 10 ng/ml), C. psittaci (live), heat-inactivated C. psittaci ({Delta}H), or UV-inactivated C. psittaci (UV). Some cultures were treated with chloramphenicol (CAM) before infection. After 24 h, IFN-{gamma}R{alpha}, IL-1R, and TNFR expression was assessed by indirect immunofluorescence with flow cytometry. The results in mean fluorescence intensity (MFI) ± standard deviations (SD) of three separate representative experiments are presented. Error bars indicate standard deviations.

To determine whether the increase in receptors required viable Chlamydia or the production of new chlamydial proteins, HeLa 229 cells were infected with viable C. psittaci (MOI, 2) that was cultivated with equivalent amounts of heat-inactivated (30 min at 60°C) or UV-inactivated (30 min) C. psittaci or infected in the presence of chloramphenicol (50 µg/ml) to inhibit chlamydial protein synthesis for 24 h. Chlamydia and changes in receptor expression were detected by anti-Chlamydia and antireceptor antibodies and analyzed by flow cytometry as described above. Nonviable and viable Chlamydia increased the expression of the IFN-{gamma}R{alpha} similarly (Fig. 1B, top panel). Furthermore, treatment with chloramphenicol to prevent synthesis of new chlamydial proteins failed to prevent the increase in IFN-{gamma}R{alpha} expression. Moreover, the same trend was observed for both the IL-1R and TNFR (Fig. 1B, middle and bottom panels, respectively), also suggesting that the increase is dependent on the presence of antigen and is independent of an active infection or the synthesis of new proteins.

Because Chlamydia has been shown to stimulate the production and secretion of cytokines by nonimmunological cells (8, 13, 23, 29) and increased receptor expression was observed in both infected and uninfected populations within infected cultures (Fig. 1), changes in receptor expression in response to chlamydial infection could be cytokine mediated (15, 24, 27, 28). In particular, IL-1{alpha} mRNA in epithelial cells has been detected following infection with C. trachomatis, (23) and increased IL-1ß mRNA has been detected by reverse transcription (RT)-PCR in C. psittaci-infected HeLa cell cultures (data not shown). To assess whether the observed increases from infection were mediated by IL-1ß, HeLa 229 cells were simultaneously infected with C. psittaci (MOI, 2) and treated with neutralizing anti-IL-1ß (R&D Systems) antibody (1 mg/ml) for 24 h. Changes in receptor expression were analyzed by flow cytometry. While anti-IL-1ß blocked the increase in IFN-{gamma}R{alpha} expression in IL-1ß-treated cells (P < 0.001), it had no effect on cultures that were infected with C. psittaci (Fig. 2). Increases in receptor expression in cells that were cultured with C. psittaci and anti-IL-1ß were similar to increases in cells that were cultured with C. psittaci alone, suggesting that the observed increases are not the result of secreted IL-1ß. To eliminate the possibility that other soluble products of infected cells triggered the increase in cytokine receptor expression, culture supernatants (conditioned medium) were collected at 8 h postinfection and placed on uninfected cells for 24 h. Parallel sets of infected cells were also infected for 24 h. Changes in receptor expression were detected by antireceptor antibodies and analyzed by flow cytometry. Cells treated with conditioned medium from infected cells did not increase their IFN-{gamma}R{alpha} expression (Fig. 3, top panel), suggesting that the up-regulation of cytokine receptor expression was due to Chlamydia and not the result of secreted cytokines. To ensure that sufficient time was allowed for the accumulation of cytokines in the medium of the infected cell cultures, the conditioning of medium was extended to 24 h, again with no effect on cytokine receptor expression (data not shown). Furthermore, the change in receptor expression over 36 h following infection corroborates this conclusion (Fig. 3, inset, top panel). Increases in receptor expression occurred 4 h earlier in infected cells than in cells stimulated with cytokine alone and by 8 h were greater than increases obtained with cytokine at any time point. Similar results were obtained for IL-1R and TNFR with conditioned medium from Chlamydia-infected cells (Fig. 3, middle and bottom panels, respectively), indicating that Chlamydia has a direct effect on changes in cytokine receptor expression.


Figure 2
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  		FIG. 2. Up-regulation of cytokine receptor expression by Chlamydia is independent of IL-1. HeLa 229 cells were cultivated with medium or IL-1ß (100 ng/ml) or infected with C. psittaci for 24 h. Some cultures also received neutralizing anti-IL-1ß antibody (>1 µg/ml). After 24 h, the cells were collected and receptor expression was assessed by indirect immunofluorescence with flow cytometry. Visual confirmation was assessed by fluorescent microscopy. The results of one of three similar experiments (MFI ± SD) are presented. Error bars indicate standard deviations.


Figure 3
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  		FIG. 3. Cytokine receptor expression is independent of secreted cytokines. HeLa 229 cells were infected with C. psittaci or cultivated with medium alone. After 8 h, culture supernatants (conditioned medium) were transferred to fresh HeLa cells and incubated for an additional 24 h. Parallel cultures were cultivated in triplicate with medium or cytokine (top panel, IL-1ß at 100 ng/ml; bottom panels, IFN-{gamma} at 10 ng/ml) or infected with C. psittaci for 24 h. Cytokine receptor expression was assessed by indirect immunofluorescence by flow cytometry. The results for three separate representative experiments (MFI ± SD) are presented. The insets show changes in receptor expression over time that were obtained in independent experiments. Changes in MFI ± SD over 36 h following treatment with medium ({blacksquare}) or cytokine (•) or infection with C. psittaci ({triangleup}) from one of three experiments with similar results are presented. Error bars indicate standard deviations.

Since heat-inactivated Chlamydia retained the ability to up-regulate cytokine receptor expression, the heat stability of the chlamydial component was assessed. A series of temperatures were chosen to discriminate between heat-labile and heat-stable proteins. HeLa cells (105 cells/ml) were infected with C. psittaci (MOI, 2) or cultivated with an equivalent amount of Chlamydia that had been heat inactivated for 30 min at 60°C, 80°C, or 100°C, for 24 h. Regardless of the temperature used to inactivate the chlamydiae, there were similar increases in IFN-{gamma}R{alpha} expression (data not shown), suggesting that the component is heat stable. Heat treatments yielded similar results for both IL-1R and TNFR (data not shown). The heat stability of the chlamydial component responsible for up-regulated cytokine receptor expression eliminated more heat-labile components, such as heat shock protein 60, from further consideration and suggested that LPS, major outer membrane protein, or another heat-stable component could mediate the increase in receptor expression.

To determine whether the heat-stable component responsible for receptor increase could be chlamydial LPS, HeLa 229 cells (105 cells/ml) were infected with C. psittaci (MOI, 2) and treated with increasing concentrations of a competitive inhibitor of LPS, diphosphoryl lipid A (DPLA) (16) from Escherichia coli F583 (Sigma), for 24 h. Parallel sets of cells were treated with minimal essential medium, IL-1ß (100 ng/ml), IFN-{gamma} (10 ng/ml), or E. coli 026:B6 LPS (1 µg/ml, Sigma) and increasing concentrations of DPLA for 24 h as controls for the competitive inhibitor. The cells were then harvested and analyzed for changes in cytokine receptor expression by using flow cytometry. DPLA did not affect IFN-{gamma}R expression of cells treated with medium or cytokine; however, a dose-dependent decrease in receptor expression was observed with increasing concentrations of DPLA for cells treated with LPS or infected with C. psittaci (Fig. 4). The same trends were observed with both the IL-1R and TNFR (data not shown).


Figure 4
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  		FIG. 4. Chlamydial LPS may mediate gamma interferon receptor increase. HeLa 229 cells were cultivated in triplicate with medium ({blacksquare}), IL-1ß (•) (100 ng/ml), or E. coli LPS ({blacktriangleup}) (1 µg/ml) or infected with C. psittaci ({triangleup}). Cultures also received increasing concentrations of DPLA. After 24 h, the cells were collected and receptor expression was assessed by indirect immunofluorescence with flow cytometry. The results from one of three experiments with similar results (MFI ± SD) are shown.

The increases in cytokine receptor expression by Chlamydia may be due to stimulation of TLRs, resulting in the activation of NF-{kappa}B. IL-1ß up-regulation of IFN-{gamma}R expression has been shown to be NF-{kappa}B-mediated, and binding of chlamydial antigens to specific TLRs could stimulate a similar response. Although intact chlamydiae have been shown to predominantly activate TLR2 (22), purified chlamydial components interact with TLR differentially; chlamydial LPS activates TLR4 (11), whereas chlamydial HSP60 may activate both TLR2 and TLR4 (7, 25). Results presented here suggest that more than one TLR may be involved in the up-regulation of receptor expression. Although DPLA, a TLR4 antagonist, completely inhibited cytokine receptor up-regulation by E. coli LPS, it was only partially effective against chlamydiae-mediated upregulation, resulting in a 67% reduction in cytokine receptor up-regulation. While the heat stability of the chlamydial antigen and the ability to inhibit its effect with a TLR4 antagonist are consistent with chlamydial LPS as the stimulus, other heat-stable components could also induce this response, perhaps through TLR2.

Cytokine production by epithelial cells in response to infection is thought to play a critical role in both the immune response and the clearance of the pathogen. Rasmussen et al. reported that Chlamydia-infected cells secreted increased levels of IL-1{alpha}, IL-8, granulocyte-macrophage colony-stimulating factor, and IL-6 (23). Several of these are potent chemoattractants and activators for T cells, monocytes, and neutrophils, or they are pleiotropic regarding inflammation and induction of other proinflammatory cytokines by macrophages and other cells that are important in the clearance of pathogens (2, 9, 14). This study shows that Chlamydia also increases cytokine receptor expression for the cytokines involved in synergistic IDO induction in epithelial cells. These changes in receptor expression could modulate the responsiveness to cytokines produced during infection and might lead to an increase in IDO induction (27).


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ACKNOWLEDGMENTS
 
This work was supported by Public Health Service grant no. AI45836 from the National Institute of Allergy and Infection Diseases (J.M.C.).

We would like to thank Michael Hughes in the Department of Mathematics and Statistics at Miami University for his help with all statistical data analysis.


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FOOTNOTES
 
* Corresponding author. Mailing address: Department of Microbiology, 32 Pearson Hall, Miami University, Oxford, OH 45056. Phone: (513) 529-5422. Fax: (513) 529-2431. E-mail: carlinjm{at}muohio.edu. Back

Editor: J. D. Clements


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Infection and Immunity, April 2006, p. 2482-2486, Vol. 74, No. 4
0019-9567/06/$08.00+0     doi:10.1128/IAI.74.4.2482-2486.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



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  • Shirey, K. A., Jung, J.-Y., Carlin, J. M. (2006). Up-Regulation of Gamma Interferon Receptor Expression Due to Chlamydia-Toll-Like Receptor Interaction Does Not Enhance Signal Transducer and Activator of Transcription 1 Signaling. Infect. Immun. 74: 6877-6884 [Abstract] [Full Text]  

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