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RESEARCH |
Institute of Anatomy, University of Leipzig, Liebigstrasse 13, D-04103 Leipzig, Germany and 1 National Institute of Agrobiological Sciences, Tsukuba, Ibaraki 305-8602, Japan
Correspondence should be addressed to K Spanel-Borowski; Email: spanelb{at}medizin.uni-leipzig.de
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Abstract |
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-hydroxylase, a thecal cell-specific enzyme. The late secretory stage was defined by an advanced manifestation of the KIT+ network in the CL periphery. At the stage of regression, the KIT+ network was absent. The CL of pregnancy expressed high levels of KIT mRNA and KIT protein uniformly throughout pregnancy. The KIT+ immunolocalization revealed small fibroblast-like cells, luteal cells with granules, and clusters of large luteal cells with staining of the cell membrane. We conclude that a majority of KIT+ cells in the bovine CL are primarily theca-derived small luteal cells, and that a minority represent KIT+ leukocytes, in some cases KIT+ monocytes. |
Introduction |
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The fetal ovary is extremely sensitive to the KIT ligand complex. In gene-deficient mice, migration of germ cells into the genital ridge, oogenesis, and initiation of folliculogenesis fail or are impeded (Driancourt et al. 2000, Reynaud et al. 2001). The postnatal ovary appears to require the KIT ligand complex at particular steps of follicle growth and maturation. Blocking experiments in premature and mature mice with the anti-KIT antibody ACK2 indicate that the development of primordial follicles into preantral follicles is dependent on the KIT ligand complex (Yoshida et al. 1997). Preantral follicles continue to grow under KIT blockade, whereas antral follicles do not develop by lack of follicular fluid formation. Because superovulated mice develop CL despite the presence of blocking KIT antibody, it is said that the CL might be KIT independent. However, the KIT mRNA has been found in the ovine and porcine CL (Gentry et al. 1998, Brankin et al. 2004), which points to a possible KIT-dependent function. Hence, studies of the localization of the KIT protein in the CL are necessary. Because the CL encompasses diverse cell types, i.e., steroidogenic and vascular cells, fibroblasts, and leukocytes, it is of special interest to identify KIT expression to particular cell types. Small luteal cells are likely candidates, because they are known to be derived from the theca where KIT transcription takes place (Driancourt et al. 2000). In addition, isolated thecal cells secrete an increased amount of progesterone under KIT stimulation when compared with unstimulated controls (Parrott & Skinner 2000).
An important process of developing mammalian CL is the ingrowth of capillary sprouts from the vascular thecal layer into the avascular granulosa layer (Smith et al. 1994, Schams & Berisha 2004). Growing vessels are considered a vehicle for the dispersion of steroidogenic cells throughout the CL (Murphy et al. 2001). According to the classical concept, granulosa cells develop into large luteal cells, while thecal cells become small luteal cells (O’Shea 1987). During CL formation, the proliferation of both luteal cell types is low. Obviously, the amount of luteinizing granulosa and thecal cells is adequate to perform an endocrine function during the estrous cycle. In the case of pregnancy, the question of luteal cell renewal is unclear. Potentially, new luteal cells differentiate from CL precursor cells into luteal cells under the appropriate stimulus. Such a precursor concept was postulated years ago (Niswender et al. 1985, 2000), but the precursor cells have not yet been found. Because bone marrow precursor/progenitor cells are characterized by KIT expression (Li et al. 2003, Fazel et al. 2006), we undertook to determine the presence or absence of KIT+ cells in the bovine CL and whether changes in pattern are detectable during the estrous cycle and during pregnancy.
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Results |
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). Western blots of CL homogenates showed a band at 148 kDa, which was the characteristic size of the KIT protein. The KIT-signal seemed to be high in the CL of late secretory stage and low in the developing and regressing CL (Fig. 1B).
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). In addition, the outer thecal layer not included in the remodeling process displayed islands of KIT+ cells, most probably leukocytes (compare Figs 2B and 5B). The KIT+ islands were often found in the vicinity of venules. Both theca-derived venules and arterioles repeatedly showed a KIT+ endothelium (Fig. 2B and C). The specificity of immunostaining was demonstrated by a preabsorption control, which abolished the reaction (negative control), and by KIT+ oocytes in primary follicles as positive control (Fig. 2D, inset).
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). There the KIT+ cells looked like small luteal cells, which often completely surrounded the pale, large luteal cells. Occasionally, KIT+ leukocytes were observed amid the luteal cells. At the late secretory stage, this KIT+ network conspicuously expanded towards the interior, yet stayed delimited from the inner CL. KIT+ cells were completely absent from the central region of the CL. The KIT+ fibroblast-like cells abundant in the septa of early secretory stage were replaced by a few scattered KIT+ cells in the late luteal CL (Fig. 3E). These changes in distribution of KIT+ cells were a reliable parameter to differentiate between the early and late secretory stages. Again, the endothelium of septal vessels exhibited KIT+ staining. All the described staining patterns disappeared by the use of preabsorbed KIT antiserum (not shown).
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). Instead, the now dominating cell type, the large luteal cells, acquired moderate KIT+ staining with pronounced cytoplasmic granules. The CL of regression also contained a few KIT+ leukocytes, which were scattered throughout the CL and often gathered in the vicinity of small blood vessels. The KIT+ staining including the ‘granules’ and the KIT+ leukocytes, disappeared by the use of preabsorption control (not shown).
At the secretory stage, large luteal cells were regularly surrounded by KIT+ small-sized cells (Fig. 3E). To identify their origin as steroidogenic thecal cells, double immunofluorescence localization was performed for KIT and CYP17. The results revealed a similar cell pattern at the early secretory stage (Fig. 4A and B). We observed some overlapping responses, which might be explained by KIT being primarily expressed at the cell membrane and CYP17 in the perinuclear zone (Fig. 4C). The specific staining for CYP17 was validated by CYP17-positive thecal cells in an antral follicle (Fig. 4D).
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). As already shown by single immunostaining (Fig. 2B and C), KIT+ endothelial cells of arterioles, capillaries, and venules were restricted only to the capsule and the septa (not shown). We concluded that the KIT+ network represented a separate identity apart from the capillary bed of the CL and that KIT+ cells, being small luteal cells, were derived from steroidogenic thecal cells.
Single immunostaining with the KIT antibody marked beside luteal cells also leukocytes recruited into the CL, as we had identified by their morphology. Double immunofluorescence for the pan leukocyte marker CD45 and KIT antigen was performed to identify a subpopulation of KIT+ leukocytes in the CL. At the developmental stage, the CD45 staining detected all the leukocytes, which were preferentially localized at high density within the septal region (Fig. 5B). A subpopulation of CD45+ cells also displayed KIT+ staining as revealed by the orange–yellow color of the overlapping fluorochromes (Fig. 5B and C). The KIT+/CD45– luteal cells preferentially localized to the already described band-like pattern of the former theca. Some of the KIT+ leukocytes were identified as monocytes by positive staining for CD14 (Fig. 5D). At the CL stage of regression, the CD45+ leukocyte population contained only a few KIT+/CD45+ leukocytes (not shown).
KIT message and protein in homogenates of the bovine CL of pregnancy, KIT immunolocalization
Comparing early, middle, and late trimester of pregnancy, both KIT mRNA signal of 465 bp and the protein band of 148 kDa were present. The signals seemed to persist at the same level of intensity at the time points examined before (Fig. 6).
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). We also found clusters of large cells depicted by a distinct KIT+ staining of the cell membrane. Neither small nor large KIT+ cells displayed the additional presence of CYP17 (results not shown). The pattern of immunostaining seemed comparable for early, middle, and late trimester. Preabsorption controls always displayed blank sections.
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summarizes location and identity of KIT+ cells in the bovine CL throughout the estrous cycle and pregnancy.
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Discussion |
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An immunohistochemical approach was used to identify the KIT-expressing cells and patterns in the bovine CL. The technique of Hoyer et al.(2005) was used, who carried out KIT antigen retrieval by microwave treatment at pH 9.0. It became evident that KIT+ cells exist in changing CL compartments. At the developmental stage, we found a strong KIT+ band-like pattern of expression in the former thecal layer. According to other groups, thecal cells of antral follicles express both KIT+ mRNA and KIT protein (Motro & Bernstein 1993, Parrott & Skinner 1997, Driancourt et al. 2000, Brankin et al. 2004). Obviously, the KIT expression persists after ovulation in the theca-derived capsule/septum in fibroblast-like cells and in small luteal cells. In situ hybridization studies in the ovine CL also detected KIT mRNA in small luteal cells (Gentry et al. 1998). During the secretory stage of the bovine CL, KIT+ fibroblast-like cells reside in the septum close to blood vessels and might also be recruited into the parenchyma, probably under KIT ligand stimulation. Recruitment of KIT+ stromal cells to primary follicles after KIT ligand stimulation has been found in the cortex of the adult bovine ovary (Parrott & Skinner 2000).
Apart from vascular cells, the thecal layer consists of steroidogenic cells and fibroblasts, both of which are candidate cells for the small KIT+ cells in the bovine CL. We here clearly show by double-immunostaining of KIT and the thecal cell-specific enzyme CYP17 that the KIT+ network in the peripheral zone of the CL was derived from the steroidogenic thecal cells. The presence of CYP17-positive cells in the CL’s periphery seems to be a ruminant-specific feature (Conley et al. 1995).
In the bovine CL of secretory stage, the small-sized KIT+ cells form a peripheral network surrounding the large luteal cells. Using double-immunostaining of the CL, we verified that the FVIIIr-positive microvascular bed is separate from the KIT+ network. Since neovascularization of the CL has its origin in the invading theca, the intimate vicinity of both networks would allow for a molecular crosstalk between small KIT+ luteal cells and sprouting endothelial cells. It is conceivable that this cellular arrangement is engaged in the replenishment of capillaries in the CL. Recent studies of induced angiogenesis identified perivascular fibroblasts and smooth muscle cells with stromal-derived factor 1 expression being responsible for the retention of recruited proangiogenic cells in peripheral tissues (Ruiz de Almodovar et al. 2006). Among other retention candidates, KIT and KIT ligand are also discussed (Quesenberry et al. 2005, Grunewald et al. 2006). In the inner CL zone, which is free of KIT+ cells, different factors might be necessary to stabilize the microvascular bed. For example, angiopoetin-1 and its specific receptor Tie-2, which control blood vessel stabilization and are abundant in the mid-luteal phase of the human CL, might be involved (Sugino et al. 2005).
The complete disappearance of the KIT+ network at the stage of regression, characterized by degradation of the capillaries, also indicates a KIT function in neovascularization of CL. Examination of the localization of the KIT+ network suggests that early in luteolysis, the KIT+ cells undergo programmed cell death, or luteolytic factors, e.g., prostaglandin F2, vasoactive peptides, etc. (Schams & Berisha 2004), influence KIT expression and processing.
In the CL of pregnancy, large luteal cells are dominant, which is indicative of a high steroidogenic output. Some of them display a KIT+ cell membrane, possibly indicating de novo induction of KIT. Alternatively, the KIT+ large cells have originated from small KIT+ cells, which reside close to the small septum. We could not confirm this transformation by the presence of CPY17 positivity in KIT+ cells (unpublished) and therefore deduce that the thecal cell-specific marker is missing in the CL of pregnancy. This is in line with the literature describing lack of CYP17 expression in the bovine CL (Rodgers et al. 1986, Conley et al. 1995). Our observation revisits the discussion of whether small thecal cells remain small cells or alternately transform into large luteal cells (Niswender et al. 1985, 2000). The small KIT+ cells with a rather diffuse immunostaining might represent theca-derived cells and contribute to cell renewal in pregnancy.
At present, a new concept is emerging that KIT+ cells from the bone marrow contribute to the self-healing potential of the body. These bone marrow-derived KIT+ cells migrate for angiogenic repair into a remote organ such as ischemic hindlimb, myocardium after infarction, and injured femoral artery, there secreting angiogenic cytokines (Li et al. 2003, Fazel et al. 2006, Wang et al. 2006). This regenerative mechanism may have a physiological counterpart in the vascularization of the CL. We have described that macrophage-like cells from bovine antral follicles proliferate in co-culture with granulosa cells (Spanel-Borowski & Ricken 1997). Others have isolated immature, hematopoietic cells from the ovarian murine stroma expressing high KIT levels. In culture, these cells retained long-term proliferative capacity and eventually differentiated into CD45+ monocytes/macrophages (Pascual et al. 2005). In the developing bovine CL, we have also reported on the correlation of microvessel sprouting and the recruitment of CD18-positive leukocytes into the capsule/septa area (Spanel-Borowski et al. 1997). Of note, 90% of all leukocytes have been defined as eosinophils, which do not colonize together with mast cells (Reibiger & Spanel-Borowski 2000). It can thus be deduced that <10% of the CL invading leukocytes are CD14+ monocytes containing a KIT+ subpopulation. It is assumed that these particular monocytes might be derived from the bone marrow, which contains KIT+ hematopoietic progenitor cells in the bovine system (Hikono et al. 2001). The KIT+ leukocytes might provide a local pool of progenitor cells, which could ensure recruitment of cells for angiogenesis, steroidogenesis, or production of CL-specific signals like growth factors, chemokines, etc.
Our findings convincingly demonstrate KIT+ small luteal cells, which have originated from the former thecal layer and which persist in the CL periphery. In addition, a subpopulation of KIT+ monocytes are detectable in the septum/capsule area of the bovine CL of early development. Further studies are needed to corroborate whether, similar to the promotion of follicular development by the KIT–KIT ligand complex (Carlsson et al. 2006, Hutt et al. 2006), the CL life cycle also depends on KIT and KIT ligand-expressing cells.
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Materials and Methods |
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RNA isolation, cDNA synthesis, and RT-PCR analysis
Frozen CL were crushed into powder with a pestle and mortar in liquid nitrogen, and total RNA was isolated using the peqGOLD RNAPURE isolation kit (PEQLAB GmbH, Erlangen, Germany). Genomic DNA was digested with 0.02 U DNase/µg RNA (Roche Molecular Biochemicals). RNA of 5 µg was taken to synthesize cDNA using a first-strand cDNA synthesis kit from Amersham Pharmacia Biotech by use of oligo-dT primers in a 15 µl reaction volume. RT-PCR technique was used to amplify a KIT mRNA fragment from bovine CL cDNA (Table 2). KIT primers were designed using the GenBank deposited Bos taurus sequences (no. D16680
[GenBank]
). Primers did not match to the sequences of the platelet-derived growth factor receptor subfamily. Each 25 µl amplification reaction contained 2.5 µl 10x concentrated PCR buffer (15 mM MgCl2), 0.3 U Taq DNA polymerase (Roche Molecular Biochemicals), 100 µM dNTPs (Perkin–Elmer, Weiterstadt, Germany), 0.1 µM of each primer, and 1 µl sample cDNA. According to our standard laboratory protocol, the product was amplified by 40 cycles as 465 bp amplicons. Amplified fragments were cloned into pGEM-T (Promega). Clones harboring cDNA inserts of expected sizes were isolated and sequenced. Subsequent identification of the cDNA inserts was obtained by interrogation of GenBank (BLAST search). Glyceraldehyde-3-phosphate dehydrogenase (GAPDH), amplified as 566 bp fragments, was used for equal loading. RT-PCR analysis was carried out without sample cDNA as negative control (not shown).
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Immunohistochemistry for KIT localization
The technique of Hoyer et al.(2005) was performed with minor modifications using antigen retrieval and Envision method (DakoCytomation, Glostrup, Denmark). We selected the rabbit anti-human CD117 antiserum (A4502, DakoCytomation), because comparative evaluations attested this product’s high specificity and sensitivity (Lucas et al. 2003, Vakiani et al. 2005). Additionally, the antiserum was successfully applied to reveal KIT+ Cajal cells in the bovine gut (Marquez et al. 2006).
Paraffin sections (7 µm) were mounted on poly-L-lysin-coated glass slides, dewaxed, and washed 3x with TBS buffer (0.05 M Tris (pH 7.6), 0.15 M NaCl) containing 0.01% Nonidet P-40 (TBS/NP40). To unmask antigens, CL sections were pretreated with microwaves in 0.02 M Tris (pH 9.0) and 0.5 mM EDTA as follows: 800 W for 5 min, 100 W for 15 min, and then cooled to room temperature (RT). Endogenous peroxidase activity was quenched with 0.45% H202 in TBS/NP40 for 15 min at RT. Sections were washed 1x in TBS with 0.125% Tween (TBS/Tween), 2x in TBS, and incubated in 10% normal goat serum in TBS/NP40 at RT to block non-specific binding for 30 min. The primary antiserum was diluted (concentration 100 µg/ml) in PBS with 0.25% BSA (A-4378, Sigma–Aldrich) and applied at 4 °C overnight. To control the specificity of KIT staining, the antiserum was incubated with 100x molar excess of the antigenic peptide (PP-1518, LAB VISION Corp., Fremont, CA, USA) at 4 °C overnight, the immunoprecipitates were removed by repeated centrifugation, and the supernatants applied to sections. Next day, slides were successively washed 3x in TBS/Tween and TBS alone, and then incubated with DakoCytomation Envision System (Labelled Polymer-HRP Anti-rabbit, K4002; DakoCytomation) at RT for 30 min. Sections were washed and incubated with 0.025% 3',3'-diaminobenzidine (Sigma–Aldrich) in 0.05 M Tris (pH 7.6), 0.03% H202 for 6 min. Sections were counter-stained with hematoxylin, dehydrated, and mounted in Histokitt (Carl Roth GmbH, Karlsruhe, Germany).
Double immunofluorescence localization of KIT and FVIIIr, or cytochrome P450 17-hydroxylase (CYP17), or CD45, or CD14
KIT was co-localized by use of the monoclonal anti-KIT antibody bk-1 (Hikono et al. 1999) and (a) the polyclonal antibody against the cytochrome P450 17-hydroxylase (CYP17), which is a selective key enzyme of steroidogenic thecal cells; the anti-CYP17 antibody was a kind gift from Prof. M R Waterman, Vanderbilt University, Nashville, TN, USA (Rodgers et al. 1986). There are reports that CYP17 is not highly expressed or absent in the bovine CL (Rodgers et al. 1986, Conley et al. 1995). In our hands, the anti-CYP17 antibody gave a positive signal in the former thecal cells of the developing CL and at the early stage of secretion. This CYP17 signal decreased thereafter. The monoclonal anti-KIT antibody was also applied with b) FVIIIr using the polyclonal anti-FVIIIr antiserum (DakoCytomation). KIT was finally c) co-localized with leukocyte markers; the polyclonal anti-KIT antiserum (DakoCytomation) was combined with the monoclonal anti-bovine CD45 antibody (VMRD Inc., Pullman, WA, USA), which localizes all leukocytes, and also with the monoclonal anti-bovine CD 14 antibody, clone BAQ151 (VMRD Inc.), for monocytes respectively.
Cryosections (10 µm) of CL samples were mounted on coated glass slides, postfixed in ice-cold methanol/ethanol, 1:1, air-dried and rehydrated in PBS buffer. Sections were incubated with the monoclonal anti-KIT antibody (20 µg/ml) or the polyclonal anti-KIT antiserum (100 µg/ml) diluted in antibody buffer (10 mg BSA/PBS) at 4 °C overnight. Thereafter, the Cy3-conjugated secondary antibody (7.5 µg/ml; Dianova) was applied at RT in the dark for 1 h. The secondary antibody was chosen in such a way that it corresponded to the species, in which the primary anti-KITantibody had been generated. In the second round staining, sections, labeled before with the monoclonal antibody bk-1, were incubated with the polyclonal anti-CYP17 (diluted 1:1000) or with the polyclonal anti-FVIIIr antiserum (concentration: 3.1 µg/ml), whereas sections treated with the polyclonal anti-KIT antiserum were treated with the monoclonal anti-CD45 antibody or the anti-CD14 antibody (both diluted 10 µg/ml). Incubation with secondary antibodies conjugated with Cy2 (7.5 µg/ml; Dianova) was conducted as described above. Finally, nuclei were stained with 1 µg/ml 4'-6-diamidino-2-phenylindole (Serva, Heidelberg, Germany) in PBS for 1 min. Between each incubation step, thorough rinsing with washing buffer (0.1 mg BSA/ml PBS) was performed. Air-dried sections were finally mounted in Entellan (Merck). Non-specific staining was judged by the use of nonspecific IgG instead of the primary antibody.
Photodocumentation
Pictures were taken by a light microscope (Axioplan 2, Zeiss, Jena, Germany) equipped either with a digital camera and the Image Access Software (Image, Glattburg, Switzerland) or with an epifluorescence illumination together with an axiovision camera. For double immunofluorescence localization, pictures were documented with a laser scanning microscope LSM 510 Meta (Zeiss). It allowed the reduction of nonspecific staining by minimizing crossover interference during scanning.
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Footnotes |
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References |
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