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Biology of Reproduction 61, 1581-1585 (1999)
©Copyright 1999 Society for the Study of Reproduction, Inc.

Articles

Tumor Necrosis Factor {alpha} Regulates Collagenolytic Activity in Preovulatory Ovine Follicles: Relationship to Cytokine Secretion by the Oocyte-Cumulus Cell Complex1

Michelle L. Johnsona, Jenifer Murdocha, Edward A. Van Kirka, James E. Kaltenbacha, and William J. Murdoch2,a

a Department of Animal Science, University of Wyoming, Laramie, Wyoming 82071


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The pleiotropic cytokine tumor necrosis factor (TNF)-{alpha} has been implicated in the mechanism of ovulation. Experiments were designed to test the hypothesis that TNF-{alpha} secreted from the oocyte-cumulus cell complex stimulates follicular collagenase production and thereby contributes to ovarian wall degradation and ovulatory rupture. Proestrous ewes were treated with GnRH to synchronize the onset of the gonadotropin surge; ovulation occurs approximately 24 h later. There was an increase in TNF-{alpha} (immunoassay) in antral fluid of preovulatory follicles at 18 h after GnRH, which was related to tissue collagenolytic bioactivity (radiolabeled type I substrate digestion by enzymatic extract) and collagen (hydroxyproline) depletion. Intrafollicular injection of TNF-{alpha} antibodies at 12 h after GnRH negated the rise in follicular collagenolytic bioactivity (and is known to block ovulation in the sheep). Moreover, collagenase production was enhanced when follicular tissues (0 h GnRH) were incubated (6 h) with recombinant TNF-{alpha}; this effect was abolished by the transcriptional inhibitor actinomycin D. Secretion of TNF-{alpha} by oocyte-cumulus cell complexes isolated from preovulatory follicles simulated the in vivo circumstance. Immunostaining indicated that TNF-{alpha} was confined mainly to the oocyte before GnRH administration, accumulated in cumulus cells during the mid-to-late preovulatory period, and was expended with the imminent approach of ovulation. To our knowledge, this is the first report specifying that up-regulation of collagenase expression is a target mode of TNF-{alpha} action in preovulatory follicles. The oocyte-cumulus cell complex is an apparent source of soluble TNF-{alpha}.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Tumor necrosis factor (TNF)-{alpha} is generated by cells as an integral transmembrane precursor protein of 26 kDa [1]; the structure is well conserved (~80% homology at the amino acid level) among mammals [2]. The exodomain of TNF-{alpha} is truncated from the cell surface by a metalloproteinase disintegrin [3] or serine protease [4] to yield a soluble product of 17 kDa. Mature TNF-{alpha} is a noncovalent homotrimer. Common cell types that secrete TNF-{alpha} include leukocytes, smooth muscle, fibroblasts, and endothelium. Virtually all nucleated cells display receptors for TNF-{alpha} [1, 5]. In addition to its capacity to elicit cellular death [6–8], TNF-{alpha} can promote (nonlethal) transcriptional activities [1], such as collagenase gene expression [9–11].

A prospective role for TNF-{alpha} in the mechanism of ovulatory follicular rupture has recently emerged. Ovarian and circulatory concentrations of TNF-{alpha} were elevated in rats relative to the first pubertal ovulation and after treatment with gonadotropins [12]. Perfused rat ovaries released TNF-{alpha} into venous effluent during ovulation [13], and the addition of TNF-{alpha} to perfusates enhanced LH-induced ovulation rates [14]. Preovulatory bovine and human follicles also secrete bioactive TNF-{alpha} [15, 16]. Ovulation was blocked in ewes after injection of TNF-{alpha} antibodies into the follicular antrum [17]. The oocyte of rodent follicles was a conspicuous intrafollicular site of TNF-{alpha} production [18, 19].

We hypothesized that TNF-{alpha} derived from the oocyte-cumulus cell complex up-regulates preovulatory follicular collagenolysis. Degradation of collagen is a requisite of follicular wall weakening and rupture [20–24]. Fibrillar collagens comprise three polypeptide chains coiled into a helix; nascent {alpha}-chains consist of repeating sequences of glycine-X-Y, where X and Y are often proline or hydroxyproline [25]. Mammalian collagenases belong to a family of metalloproteinases that cleave each of the polypeptide chains of collagen at sites near the amino terminus [26]. The objectives of this investigation using sheep were to establish the temporal relationship (before and after in vivo gonadotropic stimulation) between antral fluid TNF-{alpha} accumulation and collagenolytic capacity of preovulatory follicles, determine the effects of TNF-{alpha} and antibodies against TNF-{alpha} on collagenase bioactivity in explanted follicular tissues, and consider the oocyte-cumulus cell complex as a source of TNF-{alpha}.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Experiments were conducted with the approval of the University of Wyoming Animal Care and Use Committee. Ovarian excisions were made when the animals were killed (by Beuthanasia-D i.v.; Schering-Plough Animal Health, Kenilworth, NJ). Reagents were purchased from Sigma Chemical Company (St. Louis, MO) unless stated otherwise.

Experimental Model

Mature Western-range ewes were penned with vasectomized rams and observed for estrous behavior. The first day of estrus was considered Day 0. Animals were treated on Day 14 with prostaglandin F2{alpha} (PGF2{alpha}; 10 mg i.m. dinoprost tromethamine; The Upjohn Co., Kalamazoo, MI) to synchronize luteal regression and 36 h later with an agonistic analog of GnRH (5 µg i.m. des Gly10-Ala6 ethylamide) to evoke a preovulatory surge of gonadotropins. Dominant antral follicles (>= 6 mm diameter) ovulate approximately 24 h after injection of GnRH [27].

Preovulatory TNF-{alpha}-Collagenase-Collagen Dynamics

Two preovulatory follicles were isolated from each of five ewes at 36 h after PGF2{alpha} injection (no exogenous GnRH stimulation; 0 h) or 18 h after GnRH injection. Follicular fluids for TNF-{alpha} analysis were aspirated into a 1-ml tuberculin syringe fitted with a 27-gauge hypodermic needle. Tissues were blotted on absorbent paper, weighed, and analyzed for collagenase bioactivity and hydroxyproline.

Effect of TNF-{alpha} Antibodies on Follicular Collagenase Bioactivity

Eight preovulatory follicles were obtained from five ewes at 12 h after GnRH injection. Five microliters of normal rabbit serum (control) or rabbit polyclonal anti-sheep TNF-{alpha} serum (AB1842; Chemicon International, Temecula, CA) were injected into the antral cavity (n = 4). Follicles were incubated in 1 ml RPMI-1640 medium (supplemented with 10% fetal calf serum and 10 µg/ml insulin) for 6 h at 37°C, lanced, blotted on absorbent paper, weighed, and assayed for collagenase bioactivity.

Effect of TNF-{alpha} on Follicular Collagenase Bioactivity: Transcriptional Control

Sixteen preovulatory follicles were isolated from seven ewes at 0 h after GnRH injection. Follicular fluids were aspirated and replaced with 0.1 ml RPMI-1640 in the absence or presence of recombinant human TNF-{alpha} (0.3 ng; R & D Systems Inc., Minneapolis, MN) and the transcriptional inhibitor actinomycin D (0.2 µg) (2 x 2 factorial arrangement of treatments; n = 4). Follicles were incubated (6 h, 37°C) and analyzed for tissue collagenase bioactivity.

Secretion of TNF-{alpha} by Oocyte-Cumulus Cell Complexes of Preovulatory Follicles

An oocyte-cumulus cell complex was recovered, using a 5-µl microdispenser (Drummond Scientific Co., Broomall, PA) and the aid of a dissection microscope (Bausch & Lomb, Rochester, NY), from a follicular aspirate of each of four ewes at 0, 12, and 18 h after GnRH and incubated in 0.1 ml RPMI-1640 (without phenol red) for 6 h at 37°C. Media were assayed for TNF-{alpha}.

TNF-{alpha} Immunoassay

TNF-{alpha} was quantified using a competitive enzyme immunoassay kit according to the instructions of the manufacturer (Chemicon). Biotinylated and standard ligands were recombinant human. Binding values representing different dilutions of sheep follicular fluid or tissue-conditioned incubation medium were parallel to the standard curve. Assay coefficients of variation were < 10%. The assay was sensitive to 0.02 ng.

Collagenase Bioassay

In vitro degradation of a radioactive collagen substrate was used as an index of follicular collagenolytic bioactivity [22, 24]. Tissues were homogenized in 0.25 ml assay buffer (20 mM Tris·HCl, 5 mM CaCl2; pH 7.6) and heated (60°C for 6 min to dissociate enzyme from collagen fibrils). Substrate tubes were prepared by mixing 10 µl (0.25 µCi) of tritiated interstitial (type I) collagen (New England Nuclear, Boston, MA) in 10 mM acetic acid solution with 90 µl of assay buffer. Formation of fibrils was allowed to proceed by incubating the substrate solution for 2 h at 4°C. Substrate and tissue homogenates were coincubated with shaking for 2 h at 37°C. Supernatants (containing solubilized radiolabeled peptide fragments) were harvested after centrifugation and counted by liquid scintillation spectroscopy. Data are expressed as a percentage of substrate digested per mg follicular tissue.

Hydroxyproline Determinations

Concentrations of hydroxyproline, an imino acid distinctively abundant in collagen, were measured in tissue acid hydrolyzates (20 x 6 N HCl, 110°C, 16 h) using a standard colorimetric assay [28].

Immunostaining of TNF-{alpha} in Oocyte-Cumulus Cell Complexes

An ovary containing a preovulatory follicle was obtained from each of three ewes at 0, 12, 18, and 24 (ovulatory stigma stage) h after GnRH, fixed in 10% buffered formalin, paraffin-embedded, serially sectioned at 5-µm thickness, and transferred onto microscope slides. Sections through preovulatory follicles were deparaffinized in xylene, rehydrated, and examined under a dissection microscope to locate oocyte-cumulus cell complexes. Samples were incubated for 30 min in 10% normal goat serum and for 30 min with TNF-{alpha} antiserum (1:200 dilution), washed in two changes of PBS, incubated for 30 min with secondary goat anti-rabbit immunoglobulin G-fluorescein isothiocyanate (F0382; 1:40), washed in two changes of PBS, coverslipped, and examined using an Olympus BH-2 microscope equipped with a reflected light fluorescence attachment and photography (Tokyo, Japan). Negative control reactions were performed in the absence of primary antibody and with antiserum preabsorbed with TNF-{alpha} (1 µg/ml).

Fluorescence intensities generated by gray-scale images of oocytes, cumulus oophorus, and mural granulosa captured (x200; two randomly selected areas/cellular parameter/follicle) by digital photography (1.2 million pixel; Pixera, Los Gatos, CA) were determined by computer-assisted analysis (Optimas, Bothell, WA). Data are expressed as a percentage above (black) background.

Statistics

Assignments to treatments were made at random. Subsample data were averaged. Percentage values were transformed (arc sine) for the purpose of analysis. Mean comparisons were made by Student's t-test or ANOVA and protected least-significant difference. Contrasts were considered significantly different at P < 0.05.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Between 0 and 18 h after treatment of proestrous ewes with GnRH, there was an increase in concentrations of TNF-{alpha} in antral fluid of preovulatory follicles. Degradation in vitro of type I collagen substrate by extracts of follicular wall also was elevated at 18 h post-GnRH. The net increase in follicular enzymatic bioactivity was inversely related to tissue concentrations of hydroxyproline (i.e., depletion of interstitial collagen matrix; Fig. 1).



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  		FIG. 1. Concomitant preovulatory follicular alterations in TNF-{alpha}, collagenolytic bioactivity, and hydroxyproline. Means ± standard errors are plotted; each contrast is different (P < 0.05)

Preovulatory follicles that were explanted at 12 h after administration of GnRH, that received injections of TNF-{alpha} antibodies into the antrum, and that were then incubated for 6 h exhibited less tissue collagenolytic bioactivity than did sham-operated control follicles that had received an equivalent dose of normal rabbit serum (Fig. 2A). There was an increase in the collagenolytic bioactivity of follicles that were isolated at 0 h and incubated for 6 h with a dose of TNF-{alpha} (Fig. 2B) similar to the (endogenous) level detected in follicular fluid at 18 h after GnRH (Fig. 1). The TNF-{alpha}-induced rise in follicular collagenolytic bioactivity was negated by the transcriptional suppressor actinomycin D. Actinomycin D alone had no effect on basal (i.e., compared to control follicle) collagenolysis (Fig. 2B).



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  		FIG. 2. In vitro effects of intrafollicular injection of (A) TNF-{alpha} antibodies (Ab; follicles were explanted at 12 h after in vivo GnRH administration and incubated for 6 h) or (B) TNF-{alpha} ± actinomycin D (AD; 0 h collection, 6 h incubation) on tissue collagenolytic bioactivities. C, Controls. An asterisk indicates an elevation (P < 0.01)

TNF-{alpha} was secreted by oocyte-cumulus cell complexes that were isolated from follicles at 0, 12, and 18 h after injection of GnRH and incubated for 6 h. Concentrations of TNF-{alpha} in conditioned media were higher after in vivo gonadotropic stimulation. The TNF-{alpha} secretory response was greatest at 12 h (Fig. 3).



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  		FIG. 3. Secretion in vitro (after 6-h incubations) of TNF-{alpha} by oocyte-cumulus cell complexes isolated at 0, 12, or 18 h after GnRH injection. *Increase compared to 0 (P < 0.01) and 18 (P < 0.05) h

Modalities of TNF-{alpha} immunostaining among oocyte-cumulus cell complexes were consistent within each time of ovarian collection after GnRH. An intense reaction toward TNF-{alpha} in oocytes was observed at 0 and 12 h. Immunostaining of the cytoplasm of oocytes at 18 and 24 h was relatively weak (similar to that of negative controls); there was an indication of positive reactions along the periphery (presumptive plasma membrane). At 24 h, oocytes were detached from the mural granulosa and were virtually depleted of surrounding epithelium. Cumulus cell immunostaining was most conspicuous (and comparatively greater than that of basal cells) at 12 h after administration of GnRH (Fig. 4).



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  		FIG. 4. Representative light photomicrographs of sections of preovulatory oocyte-cumulus cell complexes immunostained for TNF-{alpha}: 0 (A), 12 (B–D [negative control]), 18 (E), and 24 (F) h after injection of GnRH. Quantifications of response variables are shown in G. *Difference (P < 0.05) from 0 h. No attempt was made to assess (dispersed/often absent) cumulus cells at 24 h


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
That TNF-{alpha} is an intermediary of the ovulatory process is becoming evident [29–31]. Novel results of this research indicate a causal preovulatory relationship between secretion of TNF-{alpha} by the oocyte-cumulus cell complex and enhanced collagenase production within the ovine follicular wall; antral fluid apparently serves as the diffusion medium for cytokine delivery. Type I collagen, the principal supportive fabric of the theca and tunica albuginea, must be degraded so that follicular distension and ovulatory rupture can occur [20–24].

Target tissue actions of TNF-{alpha} are receptor subtype- and concentration-dependent. Transmembrane glycoprotein receptors (TNFRI, TNFRII) bind trimeric ligand through a homologous extracellular N-terminal motif [5, 32, 33]. The cytoplasmic segment of TNFRI contains a death domain that, upon receptor aggregation, can evoke a proteolytic cascade leading to apoptotic DNA fragmentation and cellular dissolution [34–37]. Nonlethal transcriptional events also can be activated by TNFRI or TNFRII ligation. It remains unclear what mechanisms dictate the pathway of signal transduction outcome (i.e., toward genomic stimulation with or without programmed death) [38]. At high tissue concentrations, TNF-{alpha} initiates microvascular coagulation associated with necrotic cellular death and acute inflammation [6, 31].

Matrix-degrading effects of metalloproteinases are dependent upon de novo synthesis, secretion, proteolytic activation (e.g., by plasmin), and endogenous tissue inhibitor concentrations [26, 39–41]. The overall increase in this study of preovulatory follicular collagenolysis induced by TNF-{alpha} was apparently not the primary result of latent (preformed) enzyme activation. In fact, type I collagenolysis mediated by follicular extracts that were incubated with TNF-{alpha} was blocked by the transcriptional inhibitor actinomycin D. In dermal fibroblasts and chondrocytes, the gene encoding interstitial collagenase was up-regulated by TNF-{alpha} [9–11]. There was an increase in expression of an inhibitor of metalloproteinases-1 within granulosal cells of preovulatory ovine follicles following the gonadotropin surge [42]; regardless, this was not prohibitive of the stimulatory TNF-{alpha} effect on collagenolysis in our assay system (enzymatic inhibitors probably limit the extent of preovulatory follicular tissue damage, assuring that a viable corpus luteum can be formed). Follicular steroidogenic cells and fibroblasts are potential sources of collagenases [43, 44].

Immunolocalization of TNF-{alpha} to the oocyte and surrounding cumulus/corona cells of preovulatory follicles of ewes is in agreement with previous observations in mouse and rat complexes [18, 19]. Preliminary morphological observations (unpublished) indicate that oocytes associated with most classes of sheep follicles (beyond the primordial stage) immunostain for TNF-{alpha} (which is generally the case in rodents). It has been inferred that TNF-{alpha} synthesized within the oocyte is transferred to cohort granulosal cells [45] through coronal cytoplasmic extensions that traverse the zona pellucida and form gap junctions with the vitelline membrane [46]. Stores of TNF-{alpha} within preovulatory ovine oocytes are notably dissipated before cumulus expansion and impending ovarian rupture. Perhaps oocytic TNF-{alpha} is processed for secretion (i.e., mobilized to contiguous plasma membranes) as a reciprocal corollary of surge gonadotropic exposure of the follicular epithelium (antral fluid presumably contains TNF-{alpha}-cleaving enzymes). Biosynthesis of TNF-{alpha} can evidently rebound after ovulation and fertilization insomuch as secretion by human embryos was elevated during early development [47]; indeed, there is an apparent role for TNF-{alpha}, via activation of matrix metalloproteinase-9 (gelatinolysis), in implantation [48].

Thecal endothelial cells are an auxiliary source of (interstitial) TNF-{alpha} in preovulatory ovine follicles [17]. The exodomain of TNF-{alpha} is cleaved by plasmin from endothelium along the apical ovarian-follicular interface [49] as a consequence of urokinase secretion by juxtaposed ovarian surface epithelial cells [50]. Thus, a focal point of collagen degradation and cellular death occurs within the formative ovulatory stigma [51].

To our knowledge, this is the first empirical report indicating that a secretory product of the oocyte-cumulus cell complex could be involved in the biomechanics of follicular rupture. We suggest that TNF-{alpha} emanating from the oocyte-cumulus cell complex aids in the ovulatory process by induction of follicular collagenase gene expression. Diverse spatial attributes of ovarian TNF-{alpha} tissue effects (collagenase production ± apoptosis/necrosis) are contingent upon extent of soluble cytokine accretion, patterns of receptor expression, intracellular transduction properties, and relative concentrations of endogenous apoptotic inhibitors [52].

Finally, not all experimental findings are consistent with the concept that TNF-{alpha} is an ovulatory mediator. Hales et al. [53] observed that in perfused rat ovaries steroidogenesis and follicular rupture were inhibited by TNF-{alpha}.


   FOOTNOTES
 
1 Supported by USDA-NRI grant 95–37203–2131. Back

2 Correspondence: W.J. Murdoch, Department of Animal Science, P.O. Box 3684, University of Wyoming, Laramie, WY 82071. FAX: 307 766 2355; wmurdoch{at}uwyo.edu Back

Accepted: August 10, 1999.

Received: June 7, 1999.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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