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RESEARCH |
Centre de recherche en reproduction animale et Département de biomédecine vétérinaire, Faculté de médecine vétérinaire, Université de Montréal, CP 5000, Saint-Hyacinthe, Québec, Canada J2S 7C6
Correspondence should be addressed to K Sayasith; Email: k.sayasith{at}umontreal.ca
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Abstract |
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 Top Abstract IntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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Introduction |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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-amidation of the same 176-amino acid precursor (Vaudry et al. 2000); and share identical N-terminal 27 amino acids of which expression of PACAP-38 predominates in most mammalian tissues (Miyata et al. 1989). To mediate its action, PACAP binds with marked affinity to three distinct G protein-coupled seven transmembrane receptors, referred to as PACAP receptor-1 (PAC-1), VIP/PACAP-1 (VPAC-1) and VPAC-2 (Vaudry et al. 2000). PAC-1 is highly selective for PACAP, and its binding is followed by activation of both adenylate cyclase and phospholipase C (Morrow et al. 1993, Pisegna & Wank 1993, Spengler et al. 1993). VPAC-1 and VPAC-2 bind equally PACAP and VIP, and are almost exclusively coupled to adenylate cyclase (Spengler et al. 1993, Rawling & Hezareh 1996, Jaworski & Proctor 2000). The expression of PACAP and its receptors can be found in many tissues, including hypothalamus, pituitary, testis and ovary (Vaudry et al. 2000), and the role of PACAP in reproduction has been suggested by studies showing its involvement in the synthesis and release of gonadotropins in pituitary cells in vivo and in vitro (Hart et al. 1992, Osuga et al. 1992, Perrin et al. 1993). Ovulation is a complex process triggered by luteinizing hormone (LH)/gonadotropin stimulation that ultimately leads to the rupture of follicles and the release of the germ cell. In rodent ovaries, this stimulation may induce the expression and secretion of PACAP, but its role during the ovulatory process is not clearly understood (Gras et al. 1999, Ko et al. 1999). It is suggested that PACAP may be involved in modulation of ovarian functions, including steroidogenesis, accumulation of cAMP, production of plasminogen activator, maturation of the oocyte, and survival of granulosa cells (Vaudry et al. 2000). Likewise, mice deficient in PACAP display a reduction of fertility (Shintani et al. 2002). Little is known about the regulation of PACAP in preovulatory follicles of monoovulatory species, and there is no evidence of PACAP-regulated genes involved in the ovulatory process. Thus, the objectives of the study were to characterize the PACAP cDNA and its gonadotropin-dependent regulation in bovine preovulatory follicles prior to ovulation, and to determine the effect of PACAP on the expression of genes known to be involved in ovulation.
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Materials and Methods |
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Cloning of VPAC-2 cDNA fragment
A fragment of bovine VPAC-2 receptor cDNA was isolated by RT-PCR using total RNA extracts (100 ng) obtained from primary granulosa cells 24 h after forskolin (FSK) treatment, a OneStep RT-PCR kit as directed by the manufacturer, and sense (5'-GCC TCT TCA GGA AGC TGC ACT GC-3') and antisense (5'- GCA ACA CCA TGT AGT GGA CGC C-3') primers designed from highly conserved regions identified after sequence alignments of human (GenBank Accession numbers: NM_003383
[GenBank]
) and rat (GenBank Accession numbers: NM_009511
[GenBank]
) VPAC-2 receptor. Reaction products were subcloned into pGEM-T Easy vector and sequenced.
In vivo model of ovulation
Holstein heifers of 2–3 years of age exhibiting normal estrous cycles were used as a model of hCG-induced ovulation to study the regulation of PACAP during the ovulatory process in vivo, as previously described (Sirois 1994). Briefly, bovine preovulatory follicles were obtained after induction of luteolysis on day 7 of the estrous cycle, and i.v. administration of an ovulatory dose of hCG (3000 IU) 36 h after induction of luteolysis. The ovary bearing the preovulatory follicle was isolated by ovariectomy (via colpotomy) from individual heifers at 0 to 26 h after hCG (Sirois 1994). The interval of time from hCG administration to ovulation is 26–28 h in this animal model. The preovulatory follicles were dissected from the ovary with a scalpel, and pieces of follicle wall (i.e. theca interna with attached granulosa cells) were prepared and further dissected into isolated preparations of granulosa and theca cells (Sirois 1994). All tissue samples were stored at 70 °C. All animal procedures were approved by the Institutional Animal Care and Use Committee of the Université de Montréal and were consistent with the guidelines of the Canadian Council of Animal Care.
PACAP construct, granulosa cell cultures and DNA transfection
To produce the PACAP expression construct, full-length PACAP was amplified by RT-PCR using total RNA extracts (100 ng) obtained from preovulatory follicles, sense (5'-GTG AAT TCG CCG CCA CCA TGG CCA TGT GTA GCG GAG CG-3') and anti-sense (5'-ACC TCT AGA CTA CAA ATA CGG TAT TCG CCG-3') primers, and a OneStep RT-PCR kit. Reaction products were subcloned into the expression vector pcDNA 3.1(+) (Invitrogen Life Technologies), and sequenced.
Primary cultures of bovine granulosa cells were prepared as previously described (Liu et al. 1999, Sayasith et al. 2004). Briefly, pairs of bovine ovaries bearing a newly formed corpus luteum and a follicle of 8–12 mm in diameter (dominant follicle of the first wave of the estrous cycle) were obtained from a slaughterhouse. Granulosa cells were isolated from the largest follicle as previously described (Liu et al. 1997), seeded at a density of 2 x 106 in the 100 mm Petri-dish containing 10 ml of minimal essential medium (MEM; Invitrogen Life Technologies) supplemented with L-glutamine, nonessential amino acids, 2% fetal bovine serum, insulin (1 µg/ml), transferrin (5 µg/ml), and penicillin (100 units/ml)-streptomycin (100 µg/ml) and incubated at 37 °C in a humidified atmosphere of 5% CO2. To study the regulation of PACAP and its receptors, cells were serum-starved overnight in MEM and then incubated in serum-free MEM containing FSK (10 µM). After various times of incubation, cells were harvested, and total RNA extracts were isolated. In some experiments, granulosa cells were transfected with the vector expressing bovine PACAP, catalytic subunit of PKA (cPKA) or PKA inhibitor (PKI) polypeptide (4 µg/Petri-dish) using LipofectAMINE PLUS (Invitrogen Life Technologies) in accordance with the manufacturer’s protocol. cPKA and PKI polypeptide expression vectors, pRSVcPKA and pRSVPKI respectively, were generously provided by Dr Richard Maurer (Oregon Health Science University, Portland, Oregon, USA). After 3 h transfection, cells were incubated in serum-free MEM in the absence or presence of FSK (10 µM) or PKA inhibitor H89 (Calbiochem, La Jolla, CA, USA) for 24 h, from which total RNA were extracted.
RNA extraction and semiquantitative RT-PCR/Southern blot
All tissues were obtained from a slaughterhouse, and total RNA was isolated from bovine preovulatory follicles, granulosa cell cultures and tissues using the TRIzol reagent, and a Kinematica PT 1200C Polytron Homogenizer (Fisher Scientific, Montréal, Canada), according to manufacturer’s instructions. Levels of PACAP and glycer-aldehyde-3-phosphate dehydrogenase (GAPDH) mRNA were analyzed by semiquantitative RT-PCR/Southern blot using RNA extracts (100 ng), a OneStep RT-PCR kit and sense (5'-ATG ACC ATG TGT AGC GGA GCG-3') and antisense (5'-GCG TCC TTT GTT TTTAAC CC-3') primers specific for bovine PACAP, generating a 513-bp DNA fragment, and sense (5'-GTT TCC AGTAGATTC CAC CC-3') and antisense (5'-TCC ACC ACC CTG TTG CTG TA-3') primers specific for bovine GAPDH, producing an 850-bp DNA fragment. The reaction conditions were one cycle of 50 °C for 30 min and 95 °C for 15 min followed by 26 cycles for PACAP of 94 °C for 30 s, 53 °C for 1 min, and 72 °C for 2 min, or 13 cycles for GAPDH of 94 °C for 30 s, 59 °C for 1 min, and 72 °C for 2 min. The number of cycles used was optimized for each gene to fall within the linear range of PCR amplification. PCR products were electrophoresed on 2% agarose gels, transferred to nylon membrane and hybridized with corresponding 32P-labeled PACAP and GAPDH cDNA fragments using QuikHyb hybridization solution (Stratagene, La Jolla, CA, USA). Membranes were exposed to X-OMAT Kodak films with the intensification screen, and signals were quantified by densitometer using the ImageQuant software.
RT-PCR analysis
The expression of transcripts for prostaglandin (PG) G/H endoperoxide-2 (PGHS-2), PG synthase (PGES), PG E2 receptor (EP2), progesterone receptor (PR), disintegrin and metalloprotease with thrombospondin-like motifs-1 (ADAMTS-1), cytochrome P450-side chain cleavage (P450scc), cytochome P450 aromatase (P450arom), PAC-1, and VPAC-2 was analyzed by RT-PCR using RNA extracts (100 ng), a OneStep RT-PCR kit (Qiagen) and appropriate primers (see Table 1
). RNA extracts were isolated from untransfected and PACAP-transfected granulosa cells cultured in the absence or presence of FSK (10 µM) for 24 h. Each reaction was performed at one cycle of 50 °C for 30 min and 95 °C for 15 min followed by 35 cycles of 94 °C for 30 s, 59 °C for 1 min, and 72 °C for 2 min. PCR products were electrophoresed on 2% Tris-acetate/EDTA-agarose gels, and the intensity of the band was quantified by densitometer using the ImageQuant software.
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). Its predicted amino acid sequence encodes a 176-amino acid protein that is the same length as human and sheep, and one amino acid residue longer than mouse, rat, and chicken homologs (Fig. 1B). The nucleotide sequence of bovine PACAP was submitted to GenBank with Accession number AY924308
[GenBank]
. In comparison to other species, bovine PACAP deduced amino acid sequence is relatively similar to human (77%), mouse (79%), rat (76%), sheep (90%; GenBank Accession number NM_001009776) and chicken (76%; GenBank Accession number NM_001001291) homologs, and conserves putative elements for its functions, including the signal peptide, a PACAP-related peptide region, dibasic residues at positions 129–130, 159–160 and 170–171 involved in post-translational peptide cleavage to release PACAP-27 and PACAP-38 isoforms, and an amino acid residue at position 131 required for PACAP activity (Fig. 1B).
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). In contrast, expression of GAPDH mRNA (control gene) was relatively constant in these tissues (Fig. 2A).
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). Results from several follicles expressed as ratios of PACAP to GAPDH indicated that a significant increase in levels of PACAP mRNA was observed from 6 to 18 h post-hCG as compared to 0 h, with a maximum induction 6 and 12 h after hCG (P < 0.05; Fig. 2C).
Cellular localization of PACAP transcripts in preovulatory follicles prior to ovulation
To determine the cellular localization of bovine PACAP mRNA in preovulatory follicles, RT-PCR/Southern blot was performed using isolated preparations of granulosa and theca cells obtained from preovulatory follicles 0, 6, 12, 18 and 24 h after hCG treatment (n = 2 distinct follicles (each from a different animal) per time point). In granulosa cells, results showed that the expression of PACAP mRNA was undetectable at 0 h, markedly increased in levels from 6 to 12 h, and decreased between 18 and 24 h post-hCG (Fig. 3A). When results from several follicles were expressed as PACAP and GAPDH ratios, a significant increase of PACAP transcripts was observed at 6 and 12 h as compared to 0 h post-hCG, with a peak at 12 h post-hCG (Fig. 3B). In theca cells, results revealed that levels of PACAP mRNA were undetectable at 0 h, increased at 6 h, and declined between 12 and 24 h post-hCG (Fig. 3C). When results from multiple follicles were expressed as PACAP and GAPDH ratios, a marked increase in levels of PACAP mRNA was observed from 6 to 18 h as compared to 0 h post-hCG, with a peak at 6 h post-hCG (Fig. 3D).
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). When results from three independent experiments were expressed as ratios of PACAP to GAPDH, a significant increase in levels of PACAP mRNA was observed after FSK treatment (P < 0.05; Fig. 4B).
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, lanes 2 and 5 vs 1), whereas levels of FSK-inducible PACAP mRNA were significantly reduced by H89 and PKI (Fig. 4C and D, lanes 3 and 4 vs 2).
Effect of PACAP overexpression on PGHS-2, PGES, EP2, ADAMTS-1, PR, P450scc and P450arom mRNA in bovine granulosa cells
To investigate if PACAP induction may have an effect on the expression of PGHS-2, PGES, EP2, ADAMTS-1, PR, P450scc and P450arom mRNA, granulosa cells, either mock transfected or transfected with the PACAP expression vector, were cultured in the absence or presence of FSK for 24 h. In untransfected cells, results from RT-PCR analyses showed that basal expression of mRNA for PGHS-2, PGES, EP2, ADAMTS-1, PR and P450arom was low or undetectable, but markedly increased by FSK (Fig. 5, lanes 2 vs 1). In PACAP-transfected cells, overexpression of PACAP stimulated basal expression of mRNA for each gene, except for P450scc and P450arom, initially observed in untransfected cells (Fig. 5, lane 3 vs lane 1), whereas the treatment with FSK enhanced the latter PACAP-dependent stimulation (Fig. 5, lane 4 vs lane 3). In contrast, expression of GAPDH mRNA (control gene) was relatively constant for each samples tested (Fig. 5H).
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), and encodes for a 196 amino acid peptide, corresponding to the human VPAC-2 region of 149–344 amino acid residues. The predicted amino acid sequence of bovine VPAC-2 is highly similar to human (87%), rat (84%) and mouse (85%) homologs (Fig. 6B).
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), whereas levels of VPAC-2 mRNA were low at 0 h, highly increased at 6, and returned to basal levels from 12 to 24 h post-FSK (Fig. 6C and E). A fragment of 684 bp for bovine VPAC-1 cDNA was also isolated (data not shown) using RNA extracts from intestine, and primers designed from highly conserved regions identified after sequence alignment of human, mouse and rat VPAC-1 homologs. However, RT-PCR analyses did not reveal the presence of VPAC-1 mRNA expression in bovine granulosa cells (data not shown). |
Discussion |
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Ovulation is a complex process triggered by LH surge, during which there is increased expression of several genes thought to be involved in a rupture of the follicle and the release of the oocyte, including PGHS-2, mPGES, membrane type 1-metalloproteinase, early growth factor-1, and PACAP (Richards et al. 2002, Sirois et al. 2004, Sayasith et al. 2006). Many studies have suggested the role of PACAP as a regulator of ovarian functions in the rodent ovary (Lee et al. 1999, Park et al. 2000, Cecconi et al. 2004). Indeed, it has been reported that incubation of preovulatory follicles or granulosa cells with PACAP markedly stimulates cAMP production and amplifies FSH stimulation of cAMP, suggesting that PACAP may act as a mediator for LH during ovulation (Tornell et al. 1988, Heindel et al. 1996, Cecconi et al. 2004). It is known that the preovulatory LH surge induces follicular cAMP production, causing a transient increase of several enzymes and receptors, such as PGHS-2, PR and ADAMTS-1, and production of PGE2 (Richards et al. 2002, Sirois et al. 2004). Furthermore, previous studies have shown that PACAP increases the production of progesterone and PGE2 in the ovary of crested newt, Triturus carnifex (Zhong & Kasson 1994, Gobbetti et al. 1997, Gras et al. 1999, Ko et al. 1999). In the present work, we used primary granulosa cell cultures that have been previously established as a valuable in vitro model to study the regulation of several bovine genes, including PGHS-2 and cPLA2, and the production of PGE2 recapitulating results observed in vivo (Liu et al. 1999, Sayasith et al. 2004, Diouf et al. 2006). A similar in vitro model was employed in rodents to study the gonadotropin-dependent regulation of PACAP and its role in the suppression of follicle apoptosis (Lee et al. 1999, Park et al. 2000). As the increase in cAMP by LH or FSK leads to the activation of several signaling mechanisms, including PKA and guanine nucleotide-exchange factors (also known as exchange protein directly activated by cAMP or EPAC) signaling pathways (Gonzalez-Robayna et al. 2000, Chin & Abayasekara 2004, Li et al. 2006), the present study indicates that PKA activation in granulosa cells by FSK changes the expression of PACAP, with a transient increase in the transcript at 12 h post-hCG as observed in vivo after hCG. Interestingly, we provide new findings to demonstrate that overexpression of PACAP increases the abundance of PGHS-2, mPGES and EP2 mRNA’s in bovine granulosa cell cultures, and these responses were amplified by FSK. As the expression of PGHS-2 and EP2 is required for ovulation, our data suggest the involvement of PACAP in ovulatory process with an important role in the prostaglandin biosynthesis pathway, including PGE2 production. In addition, the follicular induction of PGHS-2 (Sirois 1994) and PGES (Filion et al. 2001) occurs much later (18–24 h post-hCG) than that of PACAP (6–12 h post-hCG), thereby supporting the concept that PACAP may be involved in the increase of PGHS-2 and mPGES mRNA in bovine preovulatory follicles.
It has been reported that LH/gonadotropin stimulation selectively induces PR, ADAMTS-1 and progesterone production in granulosa cells of preovulatory follicles; and there is evidence to indicate that progesterone, acting through its nuclear receptor (PR), plays an essential role in the regulation of ovulation (Tsafriri et al. 1987, Espey et al. 1990). Furthermore, mice deficient for PR not only fail to undergo the expected induction of ADAMTS-1 but also fail to ovulate (Lydon et al. 1995, Conneely et al. 2000, Robker et al. 2000). Reduction in ADAMTS-1 expression was also observed when the preovulatory synthesis of progesterone was inhibited with epostane (Espey et al. 2000), suggesting that ADAMTS-1 is a downstream target for LH-induced expression of progesterone and PR, and may be involved in proteolytic cascades culminating in the rupture of the follicle. Of note, mice deficient for ADAMTS-1 display impaired ovulation with morphologically abnormal in ovaries (Shindo et al. 2000). The present study reports for the first time that overexpression of PACAP causes a marked increase of PR and ADAMTS-1 mRNA in granulosa cells. This increase was supported by an induction of PR in granulosa cell cultures after treatment with FSK, in which the levels of PR mRNA were greatly increased from 12 and 24 h post-FSK (data not shown) as compared to those of PACAP (Fig. 4A and B).
Luteinization is a differentiation process of granulosa cells characterized by a high and constitutive expression of P450scc, changes of transcriptional regulation of PGHS-2 gene from being PKA dependent to PKC dependent, and an increase in cell volume with an appearance of lipid droplets (Morris & Richards 1995, Wu & Wiltbank 2002). The present study indicates that expression of several genes was increased in PACAP-transfected cells. As the transfected cells did not display luteinized cell phenotypes, but weakly express P450arom mRNA (a marker of non-luteinized state of granulosa cells), the observed increase in gene expression would appear to be a direct effect of PACAP expression as opposed to a change in differentiation status of the granulosa cells. Further supporting this conclusion, levels of the transcript for P450arom, P450scc and other genes, including PGHS-2, were markedly increased after treatment with FSK (PKA activator), which is also observed in differentiating follicles in vivo and in cultures of non-luteinized granulosa cells isolated from small follicles (Xu et al. 1995, Bao et al. 1997, Sahmi et al. 2004). Additionally, levels of P450arom and P450scc mRNA were not affected by PACAP transfection as compared to untransfected cells. Together, these suggest that granulosa cells were maintained in a non-luteinized state in cultures, and represent a valuable in vitro model to study the regulation of genes involved in the ovulatory process in vivo.
Collectively, our results suggest an important role of PACAP as an autocrine/paracrine regulator in preovulatory follicles. To mediate its biological action, PACAP must be processed and secreted from cells to bind cell surface PACAP receptors. There are at least three types of PACAP receptors, referred to as PAC-1, VPAC-1 and VPAC-2. However, the distribution of PACAP receptor types in the ovary among species is variable. Some reports have suggested that either VPAC-1 or PAC-1 alone is found in the rat ovary (Gottschall et al. 1990, Scaldaferri et al. 1996), whereas others have indicated that PAC-1 and VPAC-2 mRNA, alone or together, are present in rodent granulosa cells (Gras et al. 2000, Ko & Park-Sarge 2000, Koh et al. 2000, Park et al. 2000, Apa et al. 2002). Our data indicate that PAC-1 and VPAC-2 were found in bovine granulosa cells and that these are modulated during the ovulatory process. Indeed, treatment with FSK regulated the expression of both receptors in these cells and elevated levels of transcripts for both receptors concurred with an elevated PACAP expression at 6–12 h post-FSK. However, it is not known whether VPAC-2 or PAC-1 acts alone or together, or to which receptor PACAP binds to exert its biological effects in granulosa cells. More studies are needed for the better understanding of the relative function of the two PACAP receptors.
Information on molecular control of PACAP expression is limited. Previous studies and the present work identified high/ovulatory levels of gonadotropins as a physiological regulator of PACAP in preovulatory follicles (Gras et al. 1996, Lee et al. 1999, Park et al. 2000, 2001). Results from granulosa cell cultures also indicated that the expression of PACAP transcripts is increased by the treatment with LH, FSH, GnRH, FSK and cAMP analogs (Lee et al. 1999, Park et al. 2001, Wang et al. 2003). The present study confirms that the expression of PACAP was significantly stimulated by FSK treatment or cPKA overexpression, but inhibited by PKA inhibitor H89 treatment or PKI overexpression, suggesting that activation of adenylyl cyclase/cAMP/PKA induces PACAP expression in bovine granulosa cells. In rodents, PR activation is required for PACAP expression in granulosa cells, since treatment with PR antagonist ZK98299 inhibits the effect of hCG on PACAP expression (Ko et al. 1999). Significantly, a potential consensus PR response element has been reported for PACAP promoter (Park et al. 2000), therefore, it will be of interest to understand the importance of the latter element in the regulation of PACAP by PR during the ovulatory process.
In summary, this study is the first to report the molecular cloning of bovine PACAP and describes the induction of PACAP mRNA in the bovine follicle during the ovulatory process. This induction occurred in both granulosa and theca cells after hCG, and a similar induction pattern was obtained in primary granulosa cells cultured with FSK. Moreover, FSK treatment also induced a concomitant increase of PAC-1 and VPAC-2, as observed with PACAP. Interestingly, overexpression of PACAP in granulosa cells stimulated the transcript expression of genes known to be involved in ovulation, such as PGHS-2, mPGES, EP2, PR and ADAMTS-1, suggesting its potential involvement in the ovulatory process. Further, studies are needed to elucidate the molecular mechanisms of the involvement of PACAP in the regulation of genes implicated in ovulation. As the regulation of these genes occurred in preovulatory follicles can be reproduced in primary granulosa cell cultures, these cultures represent a valuable model to address these issues.
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and pRSVPKI, respectively. The nucleotide sequence reported in this paper has been submitted to the GenBank/EBI Data Bank with Accession numbers AY924308
[GenBank]
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Footnotes |
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References |
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TopAbstractIntroductionMaterials and MethodsResultsDiscussionAcknowledgementsReferences |
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