Molecular Human Reproduction, Vol. 5, No. 3, 240-245,
March 1999
© 1999 European Society of Human Reproduction and Embryology
Interleukin-1 receptor-ligand interactions modulate interstitial collagenase-1 production by human endometrial fibroblasts
1 Cell Biology Unit, Christian de Duve Institute of Cellular Pathology, Avenue Hippocrate 75 and 2 Department of Pathology, Saint-Luc University Clinics, Louvain University Medical School, Avenue Hippocrate 10, B-1200 Brussels, Belgium
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The expression of interstitial collagenase-1 in the cycling human endometrium is restricted to the perimenstrual phase and is a key event for matrix degradation that initiates menstruation. In the absence of ovarian steroids, collagenase production by endometrial fibroblasts is induced by epithelial cell-derived interleukin-1
. Media conditioned by endometrial epithelial cells were found to contain interleukin-1 but not interleukin-1ß, and their capacity to induce collagenase production by endometrial fibroblasts correlated with interleukin-1 concentration in a saturable manner. Collagenase induction by recombinant interleukin-1 was severely inhibited by interleukin-1 receptor antagonist alone and abolished by its combination with soluble interleukin-1 type-II receptor. By contrast, the association of the receptor antagonist with soluble type-I receptor was less effective than each factor alone. Induction of collagenase by epithelial cell-conditioned media was severely inhibited by neutralizing interleukin-1 antibodies, whereas the combination of receptor antagonist with soluble type-II receptor proved less effective. We conclude that the collagenase response of endometrial fibroblasts to epithelial cell-derived interleukin-1 is effectively blocked in vitro by soluble members of the interleukin-1 family and can thus be modulated in vivo by these or other local factors. endometrium/IL-1 receptor antagonist/interleukin-1/interstitial collagenase-1/soluble IL-1 receptor
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Introduction |
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Interleukins-1 (IL-1) are classical `multifunctional' cytokines: they are produced by, and affect, a wide variety of cell types. In vivo, IL-1 exert a wide range of systemic effects such as hypotension, fever, weight loss, and neutrophilia, but also a variety of local responses such as the controlled expression of growth factors, extracellular matrix components, and matrix metalloproteinases (for a review, see Dinarello, 1996
). Although IL-1 production in humans is generally considered to result from inflammation or tissue injury, evidence points to a transient upregulation in embryogenesis (Sheth et al., 1991) and during the menstrual cycle (Cannon and Dinarello, 1985; Polan et al., 1994).
The IL-1 family comprises IL-1, IL-1ß, as well as the IL-1 receptor antagonist (IL-1Ra). Two types of IL-1 receptor have been identified in humans. Although IL-1 and IL-1ß share little homology in primary sequence, the two cytokines exert their agonist effects through binding to the same type I receptor (IL-1RI). Type II receptor (IL-1RII) also binds IL-1 but does not transduce a signal (Stylianou et al., 1992; Sims et al., 1993). The receptor antagonist IL-1Ra binds to IL-1RI with an affinity comparable to that of IL-1 and IL-1ß, but does not elicit biological responses (Arend and Dayer, 1990; Hannum et al., 1990). Furthermore, extracellular fragments of both receptor types (IL-1sRI and IL-1sRII) circulate in the blood and function as natural `scavengers' by binding and neutralizing IL-1, IL-1ß, or IL-1Ra (Symons et al., 1993, 1994; Arend et al., 1994). This complex array of interacting factors could finely modulate IL-1 responses in vivo (Burger et al., 1995).
We have recently identified IL-1 as a major paracrine stimulator of the production of interstitial collagenase (matrix metalloproteinase-1; MMP-1) by human endometrial fibroblasts (Singer et al., 1997). Generally secreted as inactive proenzymes, MMPs are activated by limited proteolysis and degrade virtually all extracellular matrix proteins (for reviews, see Woessner, 1991; Murphy and Reynolds, 1993; Hulboy et al., 1997). A number of observations suggest that among MMPs, interstitial collagenase (MMP-1) is a key enzyme in the initiation of menstrual tissue degradation. In the normal eutopic endometrium, MMP-1 expression is restricted to the perimenstrual phase and confined to foci of fibroblast-like stromal cells in the functionalis layer of the human endometrium, that is destined to be shed (Marbaix et al., 1995, 1996a; Kokorine et al., 1996). Furthermore, inhibition of MMP-1 and related matrix metalloproteinases prevents tissue degradation in endometrial tissue explants (Marbaix, et al., 1996b).
Considering the pivotal role of MMP-1 in initiating menstruation, interference with its IL-1-mediated stimulation should have profound effects on endometrial function and morphology in vivo. To investigate whether biological agents could modulate IL-1 receptor-mediated MMP-1 production in endometrial stromal cells, we analysed cultures of epithelial and of fibroblast cells isolated from human endometrial biopsies.
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Materials and methods |
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Cell cultures
The study was approved by the Ethical Committee of the University of Louvain, Belgium. Endometrial tissue samples, derived from patients who had undergone hysterectomies or biopsies for non-endometrial pathologies, were generally obtained during the secretory phase. Epithelial cells and fibroblasts were then isolated as previously described (Zhang et al., 1995
). In brief, fresh endometrial biopsies were washed with phosphate-buffered saline (PBS) and digested with 400 IU/ml of collagenase IA (Sigma-Aldrich, Bornem, Belgium) at 37°C for 45 min. Fibroblasts were then separated from endometrial glands by sequential filtration through nylon meshes with pore sizes of 300 and 35 µm respectively. Epithelial glands, collected on the second filter, were sedimented twice, then digested with trypsin. Immunolabelling for vimentin and cytokeratin of isolated cells shortly after plating confirmed that fibroblasts were essentially pure and that epithelial cells were highly enriched.
Fibroblasts were plated into culture flasks and propagated for 2–6 weeks (i.e. 3–5 passages) in Phenol Red-free Dulbecco's minimal essential medium (DMEM)/Ham's F12 medium containing 100 IU/ml penicillin, 100 IU/ml streptomycin, 0.25 mg/ml amphotericin B, and 10% fetal calf serum (FCS; all from Gibco Europe, Merelbeke, Belgium). All experiments were carried out on confluent fibroblastic monolayers after three washes with PBS and replacement by medium devoid of FCS. Freshly isolated epithelial cells were cultured in medium with FCS for 2–7 days, washed three times with PBS and further cultured for 24–48 h in medium without FCS. The latter medium, referred to as `conditioned by epithelial cells', was then added to fibroblast monolayers in the absence or presence of recombinant proteins, as indicated. Alternatively, conditioned media were incubated with monoclonal anti-IL-1 antibodies for 1 h at 20°C before addition to fibroblasts.
Recombinant proteins and antibodies
Recombinant human IL-1, IL-1ß, IL-1Ra, IL-1sRI, and IL-1sRII were purchased from R & D Systems (Abingdon, UK) and added at the indicated nominal concentrations (n.c.; due to adsorption on plastic at very low concentrations, effective values may fall very much below nominal values; for example, a 6 pM n.c. of rhIL-1 corresponded to a ~0.6 pM effective concentration, as measured by enzyme-linked immunosorbent assay (ELISA); this is close to maximal stimulating concentration in our assays, (Singer et al., 1997). The monoclonal mouse anti-human IL-1 antibody (clone IC12.1) was purchased from Calbiochem (Bierges, Belgium).
Collagenase assays
Total collagenase activity was determined at 25°C with [3H]-acetylated collagen in solution (Eeckhout et al., 1986). One unit of collagenase is defined as the amount of enzyme which degrades 1 µg of soluble collagen/min. Full collagenase activation was achieved by treating the conditioned media with 2 mM 4-aminophenylmercuric acetate (APMA; Sigma-Aldrich) for 2 h at 37°C. Antibodies directed against MMP-1 (a kind gift of Dr H.Nagase, Kansas University, Kansas City, KS, USA) abolished the collagenase activity in media conditioned by endometrial fibroblasts, indicating that other collagenases such as MMP-8 and MMP-13 did not contribute to the collagenolytic activity in this assay (data not shown).
IL-1 and IL-1ß ELISA
IL-1 and IL-1ß concentrations in media conditioned by epithelial cells for 24 or 48 h were determined in microtitre plates by an immunoassay (R & D Systems) according to the manufacturer's protocol. Optical densities were estimated using a Titertek Multiscan MCC 340 spectrophotometer (Flow Laboratories, Doornveld, Belgium).
Curvilinear fitting
The relationship between IL-1 concentration and MMP-1 production was adjusted by least-square curvilinear fitting based on equation 1:
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where MMP-1i and MMP-1max are actual and maximal total collagenase activities, expressed in IU/ml respectively; IL-1i is the actual concentration measured in conditioned medium applied to fibroblasts, expressed in fM; Ks is the calculated half-maximal stimulatory IL-1 concentration, expressed in fM.
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Results |
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Recombinant IL-1
- and IL-1ß-induced MMP-1 production by endometrial fibroblasts is suppressed by IL-1RaTo determine the respective ability of IL-1
and IL-1ß to stimulate MMP-1 production in the human endometrium, the recombinant cytokines were added at 6 pM n.c. to confluent fibroblast monolayers and MMP-1 production after 24 h of culture was measured by collagenase assays (Fig 1). When added at equimolar concentrations, both cytokines augmented MMP-1 production with comparable potency. Addition of ~1000-fold molar excess of the IL-1 receptor antagonist (rhIL-1Ra) severely inhibited the stimulatory effect of either cytokine.
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Induction of fibroblast-derived MMP-1 by epithelial cell-conditioned medium correlates with its IL-1
concentration in a saturable mannerTo analyse the natural release of IL-1
and IL-1ß by human endometrial cells, the concentration of both cytokines was measured in media conditioned by epithelial cells derived from endometrial biopsies obtained during the secretory phase, and cultured in the absence of ovarian steroids (Figure 2). Whereas IL-1ß in conditioned media was always below the level of detection (<60 fM; data not shown), IL-1 was found in all media but one, its maximum concentration being 1.8 pM.
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As previously reported (Singer et al., 1997
), epithelial-conditioned media strongly induced MMP-1 production. The capacity of these media to induce collagenase (MMP-1) production by fibroblasts showed an excellent curvilinear correlation (r = 0.97) with the IL-1 concentration, present in the media. Curvilinear least-square fitting indicates that the estimated half-stimulatory concentration was as low as 53 ± 35 fM (mean with 95% confidence intervals). In contrast to their inhibitory effect on explants (Singer et al., 1997), ovarian steroids failed to decrease IL-1 release by cultured epithelial cells in our experimental conditions (data not shown).
IL-1-induced MMP-1 production by endometrial fibroblasts is inhibited by IL-1Ra and IL-1-soluble receptors
To further explore the possibility of inhibiting endometrial MMP-1 expression by interfering with the binding of IL-1 to its receptor, the effects of a 1000-fold molar excess of rhIL-1Ra, rhIL-1sRI, and rhIL-1sRII, alone or in combination, on rhIL-1-induced MMP-1 production by endometrial fibroblasts was investigated (Figure 3). As shown in Figure 1
, endometrial fibroblasts produced only marginal amounts of MMP-1 in the absence of added IL-1 and this production increased considerably upon the addition of rhIL-1. When rhIL-1Ra was added together with rhIL-1, MMP-1 induction was greatly reduced, whereas rhIL-1sRI or rhIL-1sRII were weak inhibitors by themselves. Surprisingly, a combination of rhIL-1Ra with rhIL-1sRI resulted in a less potent inhibition of rhIL-1-induced MMP-1 expression than rhIL-1Ra alone. By contrast, the combination of rhIL-1Ra with rhIL-1sRII almost abolished MMP-1 induction. Again, the addition of rhIL-1sRI to this combination weakened its inhibition of rhIL-1-induced MMP-1 production.
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MMP-1 induction in fibroblasts by epithelial cell-conditioned media is partially repressed by a combination of IL-1Ra and IL-1sRII
The effectiveness of the combination of rhIL-1Ra with rhIL-1sRII to inhibit MMP-1 production by fibroblasts upon stimulation by epithelial cell-conditioned medium was next examined (Figure 4
). Conditioned medium did not contain detectable MMP-1, and only little collagenase activity was spontaneously produced by endometrial fibroblasts cultured without conditioned medium. As shown in Figure 2, addition of epithelial cell-conditioned medium to endometrial fibroblasts greatly increased MMP-1 production. Whereas this induction could be almost abolished following incubation of conditioned medium with a monoclonal anti-human IL-1, incubation of conditioned medium with a precombination of rhIL-1Ra and rhIL-1sRII was much less effective.
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Discussion |
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Both IL-1
and IL-1ß are strong stimulators of MMP-1 production by fibroblasts of various tissues (Burger et al., 1995). Probably due to the presence of an IL-1 receptor accessory protein (IL-1R-AcP), which increases IL-1 binding affinity to IL-1RI (Greenfeder et al., 1995), and especially because of powerful post-receptor amplification through multiple phosphorylations by protein kinases (Croston et al., 1995), occupancy of only a few receptors per cell may suffice to elicit maximal biological responses (O'Neill, 1995). In agreement with this concept, we found a half-maximal stimulation of MMP-1 production at a concentration of ~50 fM IL-1, i.e. several orders of magnitude below the KD of the ligand-receptor interaction.
When the concentrations of IL-1 and IL-1ß were determined in media conditioned by endometrial epithelial cells, only IL-1 was measurable in concentrations capable of stimulating MMP-1 production by endometrial fibroblasts (Singer et al., 1997); the concentration of IL-1ß was always below the level of detection (<60 fM). These findings are in agreement with previous studies which detected IL-1 in the epithelial cells of the human endometrium, while reports on IL-1ß immunostaining were not consistent (Tabibzadeh and Sun, 1992; Simón et al., 1993).
Whereas explants from endometrial biopsies obtained during the proliferative or the secretory phases of the menstrual cycle and cultured for 24 h in the absence of ovarian steroids do not release measurable IL-1 into the culture medium, explants from biopsies obtained during the perimenstrual phase release considerable amounts of this cytokine over the same period (Singer et al., 1997). Upon longer culture times of non-menstrual explants in the absence of ovarian steroids, an appreciable release of IL-1 becomes apparent, a phenomenon that can be partially suppressed by the addition of physiological concentrations of 17ß-oestradiol and progesterone (Singer et al., 1997). In contrast, purified epithelial cells cultured in the absence of ovarian steroids also released IL-1, but this release was not inhibited by the addition of 17ß-oestradiol and progesterone (data not shown). Further studies are clearly needed to determine whether the unresponsiveness of isolated epithelial cells to ovarian steroids is due to the absence of stromal–epithelial interactions (Cooke et al., 1997) and/or to the loss of ovarian steroid receptors upon culture.
The interaction of IL-1 and IL-1ß with IL-1RI on target cells can be modulated by receptor expression on the cell surface and counterbalanced by the soluble inhibitory factors IL-1Ra, IL-1sRI, and IL-1sRII. Although IL-1Ra has nearly the same binding affinity to IL-1RI as IL-1 and IL-1ß at equilibrium, its rate of association with IL-1RI is slower, so that, when IL-1Ra dissociates from its cell surface receptor, IL-1 will preferentially bind to the empty receptor (Arend, 1993). This kinetic peculiarity might explain why IL-1 activity is inhibited only by a high molar excess of IL-1Ra (Arend et al., 1990). In our experiments, the presence of a 1000-fold molar excess of IL-1Ra largely inhibited the stimulatory effects of both IL-1 and IL-1ß on MMP-1 production in human endometrial fibroblasts.
Various combinations of IL-1Ra, IL-1sRI, and/or IL-1sRII, had distinct inhibitory effects on IL-1-stimulated fibroblasts. Whereas the addition of IL-1 strongly induced MMP-1 production, this response was largely reversed by a 1000-fold molar excess of IL-1Ra and its combination with IL-1sRII proved most effective. By contrast, the combination of IL-1Ra with IL-1sRI produced a considerably less potent inhibition. It might seem paradoxical that the combination of two inhibitory proteins, one neutralizing the ligand and the other competing with the receptor, is less powerful than each factor alone. However, since IL-1Ra binds to IL-1sRI with an ~200-fold higher affinity than to IL-1RI (McMahan et al., 1991), addition of IL-1sRI will neutralize the majority of the IL-1Ra (which rather binds to the soluble than to the membrane-attached receptor), and therefore decrease its capacity to compete with IL-1 for binding to IL-1RI (Burger et al., 1995).
The ability of the combination of IL-1Ra with IL-1sRII to inhibit MMP-1 production by fibroblasts was almost complete when induction was by recombinant IL-1, but proved much less able to antagonize the induction caused by the more complex epithelial cell-conditioned media. This weaker inhibition cannot be ascribed to a high concentration of IL-1 in conditioned media (which was never >2 pM). Since a neutralizing monoclonal anti-IL-1 antibody almost abolished MMP-1 induction by conditioned media, the observation rather suggests that additional factors are released by endometrial cells and interfere with the inhibitory effect of IL-1Ra and IL-1sRII. One such factor might be IL-1sRI, known to circulate in the blood of healthy humans at concentrations of 10–20 pM (Dinarello, 1996). However, the degree of IL-1sRI production and its local concentration in the human endometrium are unknown. Alternatively, neutralizing anti-human IL-1 autoantibodies, which function as natural buffers of IL-1, have been found in up to 25% of healthy subjects. It is thus conceivable that autoantibodies similarly exist for IL-1Ra and IL-1sRII (Bendtzen et al., 1990; Svenson et al., 1990).
To what extent interactions such as those analysed in this report actually modulate IL-1 signalling in the human endometrium, so as to affect production of other cytokines, e.g. tumour necrosis factor (Laird et al., 1996), to finely tune tissue differentiation in the functionalis layer, and possibly to regulate implantation efficiency (Simón et al., 1996) and trophoblast invasion (Burrows et al., 1996) will await further investigations. From a practical point of view, however, inhibition of MMP-1-induced matrix breakdown may emerge as an interesting therapeutical possibility to control dysfunctional endometrial bleeding (C.Galant et al., unpublished results), or to prevent endometriotic tissue remodelling and scarring (Kokorine et al., 1997). Indeed, prevention of MMP-1-induced breakdown can be achieved at the level of ovarian steroids, their IL-1 relay, or by direct inhibition of MMP-1 by pharmacological inhibitors (Marbaix et al., 1996b). Since high levels of IL-1Ra and IL-1sRII can be administered to humans without noticeable side-effects (Granowitz et al., 1992; Dower et al., 1994), they appear to be interesting candidates for MMP-1 suppression. If this intervention is envisaged, attempts to interfere with IL-1-induced MMP-1 production in the human endometrium should however consider the multiple and complex interactions that may modulate the powerful effects of IL-1 on this tissue.
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Acknowledgments |
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The authors wish to thank Professor J.Donnez and his co-workers for providing endometrial tissues and Dr H.Nagase for the kind gift of anti-MMP-1 antiserum. C.F.S was a recipient of the Haas-Teichen Postdoctoral Fellowship of the Christian de Duve Institute of Cellular Pathology, Brussels, Belgium. This work was supported by the Belgian Fonds de la Recherche Scientifique Médicale, and by the Fonds de Développement Scientifique of the University of Louvain. This paper represents research results of the Belgian Programme on Interuniversity Poles of Attraction and of Concerted Research Actions of the `Communauté Franciaise de Belgique'.
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3 Present address: Division of Special Gynaecology, Department of Obstetrics and Gynaecology, University of Vienna Medical Center, Waehringer Guertel 18–20, A-1090 Vienna, Austria
4 To whom correspondence should be addressed
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Submitted on June 15, 1998; accepted on November 25, 1998.
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