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The Lebanese Baladi goat dairy production sector suffers from food availability problems due to the dependence on natural rangelands and the scarcity of crop residues and forage pastures, leading to lower production. Thus, the nutritional values of the pastures were evaluated in an observational study where 48 Baladi lactating goats were selected and kept within a farm in Qâa er Rîm located in the region of Zahleh, Lebanon. Animal responses in feeding behavior were measured on four different circuits of natural rangelands (NR1, NR2, NR3, and NR4) surrounding the farm site, during a period of ≈75 d (from April to mid-June). Observations and measures consisted of evaluating the rangeland’s botanical composition, selective feeding and analysis of forage nutritional values, recording of daily foraging dynamic, and estimation of daily intake. Natural rangelands revealed a large botanical diversity that changed according to season and altitude: From NR1 to NR4, as summer season advanced and animals were moved to higher altitudes, bushes increased, whereas grasses retreated. In parallel, mean diet nutritional value decreased; dry matter (DM) content increased, as well as acid detergent fiber and neutral detergent fiber contents, while crude protein levels decreased. The animals, however, adapted their feeding dynamics on the rangelands accordingly: With the advancement of summer time, total duration of grazing day was increased in order to compensate for longer resting periods at noon and longer walking periods in higher altitudes, without a decrease in total feeding duration. On the other hand, animals were able to adjust their feeding regimen to the available plant species by increasing their daily intake of 0.56 kg/d between NR1 and NR3 and by substituting grasses with shrubby species; a shift from 25% to 28% to 53% to 54% DM in the animals’ diet. These adaptive behavioral responses explain the capacity of Baladi goats to survive in their harsh environment and even tolerate feeding perturbations.
M. Kharrat; P. Hassoun; P.Y. Aad; E. Hajj; F. Bocquier. Surveillance of Baladi Goat Feeding Behavior in Response to a Mediterranean Natural Rangeland Evolution. Rangeland Ecology & Management 2020, 73, 403 -410.
AMA StyleM. Kharrat, P. Hassoun, P.Y. Aad, E. Hajj, F. Bocquier. Surveillance of Baladi Goat Feeding Behavior in Response to a Mediterranean Natural Rangeland Evolution. Rangeland Ecology & Management. 2020; 73 (3):403-410.
Chicago/Turabian StyleM. Kharrat; P. Hassoun; P.Y. Aad; E. Hajj; F. Bocquier. 2020. "Surveillance of Baladi Goat Feeding Behavior in Response to a Mediterranean Natural Rangeland Evolution." Rangeland Ecology & Management 73, no. 3: 403-410.
Advances in molecular genetics have allowed the identification of genes that can enhance livestock production. The aim of this study was to investigate possible relationships between the calpastatin (CAST) Hha1 gene polymorphisms and growth performance, carcass characteristics, and meat quality in Awassi sheep. A total of 87 blood samples were collected from two-week-old Awassi ram lambs. The amplification of the CAST Hha1 gene yielded a fragment of 622 bp. Three CAST genotypes were found in Awassi sheep: MM for two fragments (385 bp and 281 bp), MN for three fragments (622 bp, 385 bp, and 281 bp), and NN for only one fragment (622 bp). The M and N allele frequencies of the CAST Hha1 genotypes were 0.765 and 0.235, respectively, while the genotypic frequencies of MM, MN, and NN were 0.586, 0.356, and 0.057, respectively. Based on CASTHha1 gene polymorphisms, three groups of lambs (MM: n = 8; MN: n = 6; and NN: n = 3 genotypes) were subjected to a fattening period of 70 days to investigate growth performance and meat characteristics. Only the final body weight and longissimus muscle width were significantly different between the three genotypes, while no significant differences were detected in any other carcass characteristics and meat quality parameters. In this study, new variants were observed in CAST using the Hha1 restriction site, potentially assisting in Awassi sheep breeding and selection programs to improve final body weight and longissimus muscle width.
Khaleel I. Jawasreh; Ahmad H. Al-Amareen; Pauline Y. Aad. Relationships between Hha1 Calpastatin Gene Polymorphism, Growth Performance, and Meat Characteristics of Awassi Sheep. Animals 2019, 9, 667 .
AMA StyleKhaleel I. Jawasreh, Ahmad H. Al-Amareen, Pauline Y. Aad. Relationships between Hha1 Calpastatin Gene Polymorphism, Growth Performance, and Meat Characteristics of Awassi Sheep. Animals. 2019; 9 (9):667.
Chicago/Turabian StyleKhaleel I. Jawasreh; Ahmad H. Al-Amareen; Pauline Y. Aad. 2019. "Relationships between Hha1 Calpastatin Gene Polymorphism, Growth Performance, and Meat Characteristics of Awassi Sheep." Animals 9, no. 9: 667.
Mycotoxins are ubiquitous and unavoidable harmful fungal products with the ability to cause disease in both animals and humans, and are found in almost all types of foods, with a greater prevalence in hot humid environments. These mycotoxins vary greatly in structure and biochemical effects; therefore, by better understanding the toxicological and pathological aspects of mycotoxins, we can be better equipped to fight the diseases, as well as the biological and economic devastations, they induce. Multiple studies point to the association between a recent increase in male infertility and the increased occurrence of these mycotoxins in the environment. Furthermore, understanding how mycotoxins may induce an accumulation of epimutations during parental lifetimes can shed light on their implications with respect to fertility and reproductive efficiency. By acknowledging the diversity of mycotoxin molecular function and mode of action, this review aims to address the current limited knowledge on the effects of these chemicals on spermatogenesis and the various endocrine and epigenetics patterns associated with their disruptions.
Diala El. Khoury; Salma Fayjaloun; Marc Nassar; Joseph Sahakian; Pauline Y. Aad. Updates on the Effect of Mycotoxins on Male Reproductive Efficiency in Mammals. Toxins 2019, 11, 515 .
AMA StyleDiala El. Khoury, Salma Fayjaloun, Marc Nassar, Joseph Sahakian, Pauline Y. Aad. Updates on the Effect of Mycotoxins on Male Reproductive Efficiency in Mammals. Toxins. 2019; 11 (9):515.
Chicago/Turabian StyleDiala El. Khoury; Salma Fayjaloun; Marc Nassar; Joseph Sahakian; Pauline Y. Aad. 2019. "Updates on the Effect of Mycotoxins on Male Reproductive Efficiency in Mammals." Toxins 11, no. 9: 515.
The Awassi breed is desirable due to its resilient traits, but shows poor lean meat content on the carcass; the callipyge mutation may enhance growth and meat characteristics. The first backcross of callipyge Awassi–Rambouillet (CRAW) lambs was generated by mating Awassi ewes with heterozygous F1 (50 % Awassi and 50 % Rambouillet) rams for the callipyge mutation. A fattening trial with carriers of CLPG (CRAW), non-carriers (RAW), and Awassi (AW) ram lambs was conducted for 94 days and growth and meat characteristic parameters were recorded. Final body weight, average daily gain (ADG), feed conversion ratio, and dry matter intake, but not initial body weight, were greater in CRAW and RAW lambs as compared to AW lambs; hot and cold carcass, dressing percentage, and shoulder, rack, and loin weights were greater in CRAW vs. AW but not RAW lambs. Leg cuts were heavier in CRAW vs. both RAW and AW lambs; intermuscular and subcutaneous fat percentages were greater in CRAW as compared to AW but not RAW lambs. Non-carcass components showed kidney fat, kidney, liver and testes weights higher in CRAW lambs as compared to AW lambs, but these parameters were similar to those of RAW lambs. There were no differences in fat tail weight. Further, CRAW lambs had higher shear force and water holding capacity than RAW and AW lambs, while cooking loss was the lowest in CRAW lambs. In conclusion, the callipyge mutation with 25% Rambouillet genes can provide efficient improvements in growth and meat characteristics, with the exception of tenderness in Awassi sheep.
Khaleel I. Jawasreh; Ahmad Hasen Alamareen; Mohammad Diya Obeidat; Pauline Y. Aad. Growth Performance and Meat Characteristics of the First Awassi–Rambouillet Callipyge Backcross. Animals 2019, 9, 517 .
AMA StyleKhaleel I. Jawasreh, Ahmad Hasen Alamareen, Mohammad Diya Obeidat, Pauline Y. Aad. Growth Performance and Meat Characteristics of the First Awassi–Rambouillet Callipyge Backcross. Animals. 2019; 9 (8):517.
Chicago/Turabian StyleKhaleel I. Jawasreh; Ahmad Hasen Alamareen; Mohammad Diya Obeidat; Pauline Y. Aad. 2019. "Growth Performance and Meat Characteristics of the First Awassi–Rambouillet Callipyge Backcross." Animals 9, no. 8: 517.
A participatory animal-breeding program was applied to 9 commercial Awassi sheep flocks in Jordan. This study aimed to assess the influence of Beta-lactoglobulin (β-LG), Prolactin (PRL), and Kappa casein (CSN3) genes, genotypes and their interaction on milk production and composition traits of 167 genotyped Awassi ewes via Polymerase Chain Reaction (PCR) followed by sequencing. Allele frequencies for the two variants were 0.42 and 0.58 for β-LG, 0.82 and 0.18 for PRL, and 0.92 and 0.08 for CSN3. No association was found among β-LG and CSN3 polymorphic genotypes with milk production traits. However, ewes with PRL AA genotype showed higher milk production, β-LG AB was associated with lowest fat%, high solid not fat (SNF)%, protein%, and lactose%. β-LG BB was associated with highest milk density. PRL, β-LG, and CSN3 polymorphic genotypes were differentially associated with milk production and component traits. Furthermore, β-LG × PRL interaction showed the highest milk production and fat%; β-LG × PRL recorded the highest SNF%, protein%, lactose%, and milk density, while the PRL × CSN3 had the highest fat% and SNF%. The enhancing effects of these gene interactions can be incorporated in Awassi breeding programs to improve milk production and composition.
Khaleel Jawasreh; Ahmad Al Amareen; Pauline Aad. Effect and Interaction of β-Lactoglobulin, Kappa Casein, and Prolactin Genes on Milk Production and Composition of Awassi Sheep. Animals 2019, 9, 382 .
AMA StyleKhaleel Jawasreh, Ahmad Al Amareen, Pauline Aad. Effect and Interaction of β-Lactoglobulin, Kappa Casein, and Prolactin Genes on Milk Production and Composition of Awassi Sheep. Animals. 2019; 9 (6):382.
Chicago/Turabian StyleKhaleel Jawasreh; Ahmad Al Amareen; Pauline Aad. 2019. "Effect and Interaction of β-Lactoglobulin, Kappa Casein, and Prolactin Genes on Milk Production and Composition of Awassi Sheep." Animals 9, no. 6: 382.
Aim: This study was designed to introduce the callipyge (CLPG) and 50% of Rambouillet sheep genes to improve meat quality and quantity of Awassi (AW) sheep. Materials and Methods: The CLPG mutation was introduced into the AW sheep through frozen semen of homozygous Rambouillet rams for the CLPG mutation. Four ram lambs from the first-generation Rambouillet callipyge Awassi (F1-RCA) and five from pure AW were recruited for a fattening trial conducted in individual pens using standard ration, following which ram lambs were slaughtered for carcass and meat evaluation. Results: Final body weight, dry matter intake, average daily gain, and feed conversion ratio were significantly higher in F1-RCA than AW. Hot and cold carcass weights and the other carcass cuts' weights, except for the fat tail, were heavier in F1-RCA than AW. There was no difference in dressing percentage between the two genetic groups (p>0.05). All non-carcass components' weights, except spleen, kidney, and testis, were higher in F1-RCA. Total lean, total bone, and intermuscular fat weight were greater in F1-RCA, but bone-to-lean ratio was lower in F1-RCA when compared with AW (p0.05) were observed in all meat quality parameters for muscle longissimus with the exception of pH, redness color, and tenderness that were lower (p
Khaleel I. Z. Jawasreh; A. H. Al-Amareen; P. Y. Aad. Growth performance and meat characteristics of the first filial Awassi Rambouillet callipyge ram lambs. Veterinary World 2019, 12, 783 -788.
AMA StyleKhaleel I. Z. Jawasreh, A. H. Al-Amareen, P. Y. Aad. Growth performance and meat characteristics of the first filial Awassi Rambouillet callipyge ram lambs. Veterinary World. 2019; 12 (6):783-788.
Chicago/Turabian StyleKhaleel I. Z. Jawasreh; A. H. Al-Amareen; P. Y. Aad. 2019. "Growth performance and meat characteristics of the first filial Awassi Rambouillet callipyge ram lambs." Veterinary World 12, no. 6: 783-788.
This study investigates the expression of the muscle growth factors Myostatin (MSTN) and Insulin-like growth hormone type I (IGF-I) and muscle marker genes MyoD and MyoG in relation to growth performance and meat characteristics in four different commercial broiler strains. Eight hundred, one-day-old chicks of Hubbard Classic (HC), Cobb500 (Cobb), Ross308 (Ross) and Indian River (IR) strains were randomly distributed in a completely randomised design into four groups for 28 days. At the end of the growth trial, 10 birds from each strain were weighed and slaughtered. A sample of Pectoral muscle was taken and kept in RNA solution for mRNA expression level measurements. Gene expression in the pectoral muscle at 20 days revealed that MSTN expression was higher for Ross than HC and IR. IGF-I expression was highest in IR and lowest in HC. MyoD expression was lowest in HC but higher in Ross and Cobb, while MyoG expression was similar. At the end of the experiment, IR gained the highest (p < .0001) body weight, while Ross the lowest, yet still with no significant differences in body weight gain among the four strains. HC scored the lowest (p = .01) efficiency in feed consumption (1.60 ± 0.03 kg/kg). Hot and cold carcase weights of IR were significantly heavier (p < .0001) than the other strains, with no significant difference in dressing percentages. Cooking loss was the highest (p = .058) for Cobb, IR, HC, and Ross, in decreasing order. The meat-tenderness value was highest for Ross, while differences in pH, colour and water holding capacities were insignificant among the strains.
Khaleel Jawasreh; Safwan Al Athamneh; Mohammad Borhan Al-Zghoul; Ahmad Al Amareen; Ibrahem AlSukhni; Pauline Aad. Evaluation of growth performance and muscle marker genes expression in four different broiler strains in Jordan. Italian Journal of Animal Science 2019, 18, 766 -776.
AMA StyleKhaleel Jawasreh, Safwan Al Athamneh, Mohammad Borhan Al-Zghoul, Ahmad Al Amareen, Ibrahem AlSukhni, Pauline Aad. Evaluation of growth performance and muscle marker genes expression in four different broiler strains in Jordan. Italian Journal of Animal Science. 2019; 18 (1):766-776.
Chicago/Turabian StyleKhaleel Jawasreh; Safwan Al Athamneh; Mohammad Borhan Al-Zghoul; Ahmad Al Amareen; Ibrahem AlSukhni; Pauline Aad. 2019. "Evaluation of growth performance and muscle marker genes expression in four different broiler strains in Jordan." Italian Journal of Animal Science 18, no. 1: 766-776.
Abundance of IGF-2 receptor (IGF2R), FSH receptor (FSHR), and LH receptor (LHCGR) mRNA in granulosa cells (GCs) or theca cells (TCs) or both cells as well as estradiol (E2), progesterone (P4), and androstenedione concentrations in follicular fluid were compared in cows genetically selected (Twinner) or not selected (control) for multiple ovulations and twin births. Cows were slaughtered at day 3 to 4 (day 3) and day 5 to 6 (day 5) of an estrous cycle, and ovaries, follicular fluid, GCs, and TCs were collected. The two largest (F1 and F2) E2-active (EA) and E2-inactive (EI) follicles were selected according to their E2-to-P4 ratio and diameter. Androstenedione levels in EA F1 and F2 follicles were 5-fold greater (P < 0.05) in Twinner cows than in control cows on day 3 but did not differ on day 5. Twinner cows also had greater (P < 0.05) E2 and P4 concentrations, whereas steroid levels in EI follicles did not differ (P > 0.10) between genotypes. In EA F2 follicles, IGF2R levels in GCs were greater (P < 0.05) in control cows than in Twinner cows on day 3 and day 5, whereas IGF2R mRNA in TCs did not differ (P > 0.10). On day 3, FSHR mRNA levels were greater (P < 0.05) in GCs of EA F1 and EI F2 follicles of control cows than of Twinner cows. LH receptor mRNA expression was less in GCs and greater in TCs of EA F2 follicles in control cows than in Twinner cows (P < 0.05). We hypothesize that reduced GC IGF2R expression in F2 follicles of Twinner cows may play a role in the development of 2 or more dominant follicles.
P.Y. Aad; S.E. Echternkamp; L.J. Spicer. Possible role of IGF2 receptors in regulating selection of 2 dominant follicles in cattle selected for twin ovulations and births. Domestic Animal Endocrinology 2013, 45, 187 -195.
AMA StyleP.Y. Aad, S.E. Echternkamp, L.J. Spicer. Possible role of IGF2 receptors in regulating selection of 2 dominant follicles in cattle selected for twin ovulations and births. Domestic Animal Endocrinology. 2013; 45 (4):187-195.
Chicago/Turabian StyleP.Y. Aad; S.E. Echternkamp; L.J. Spicer. 2013. "Possible role of IGF2 receptors in regulating selection of 2 dominant follicles in cattle selected for twin ovulations and births." Domestic Animal Endocrinology 45, no. 4: 187-195.
Cattle genetically selected for twin ovulations and births (Twinner) exhibit increased ovarian follicular development, increased ovulation rate, and greater blood and follicular fluid IGF-1 concentrations compared with contemporary cattle not selected for twins (Control). Experimental objectives were to 1) assess relationships among aromatase (CYP19A1), IGF-1 (IGF1), IGF-2 receptor (IGF2R), and FSH receptor (FSHR) mRNA expression in small (≤5 mm) antral follicles and 2) determine their association with increased numbers of developing follicles in ovaries of Twinner females. Ovaries were collected from mature, cyclic (d 3 to 6) Twinner (n = 11), and Control (n = 12) cows at slaughter and pieces of cortical tissue were fixed and embedded in paraffin. Expression of mRNA was evaluated by in situ hybridization using 35S-UTP-labeled antisense and sense probes for CYP19A1, FSHR, IGF1, and IGF2R mRNA. Silver grain density was quantified within the granulosa and theca cells of individual follicles (2 to 7 follicles/cow) by Bioquant image analysis. Follicles of Twinners tended to be smaller in diameter than Controls (1.9 ± 0.1 vs. 2.3 ± 0.1 mm; P = 0.08), but thickness of granulosa layer did not differ (P > 0.1) by genotype. Relative abundance of CYP19A1 (P < 0.01) and FSHR (P < 0.05) mRNA was greater in granulosa cells of Twinners vs. Controls, respectively, whereas IGF2R mRNA expression was less in both granulosa (P < 0.01) and theca (P < 0.05) cells in follicles of Twinners vs. Controls, respectively. Abundance of CYP19A1 mRNA in granulosa cells was correlated negatively with IGF2R mRNA expression in both granulosa (r = −0.33; P < 0.01) and theca (r = −0.21; P = 0.05) cells. Expression of IGF1 mRNA was primarily in granulosa cells, including cumulus cells, and its expression did not differ between Twinners vs. Controls (P > 0.10). Detected increases in CYP19A1 and FSHR, but not IGF1, mRNA expression along with decreases in IGF2R mRNA expression in individual follicles of Twinners support the hypothesis that increased follicular development and steroidogenesis in Twinner females result from increased extra-ovarian IGF-1 production. Furthermore, a reduction in follicular IGF2R mRNA expression accompanied by a reduction in receptor numbers would increase availability of free IGF-2 and its stimulation of follicular development in Twinners. Copyright © 2012. American Society of Animal Science.
S. E. Echternkamp; P. Y. Aad; D. R. Eborn; L. J. Spicer. Increased abundance of aromatase and follicle stimulating hormone receptor mRNA and decreased insulin-like growth factor-2 receptor mRNA in small ovarian follicles of cattle selected for twin births1,2. Journal of Animal Science 2012, 90, 2193 -2200.
AMA StyleS. E. Echternkamp, P. Y. Aad, D. R. Eborn, L. J. Spicer. Increased abundance of aromatase and follicle stimulating hormone receptor mRNA and decreased insulin-like growth factor-2 receptor mRNA in small ovarian follicles of cattle selected for twin births1,2. Journal of Animal Science. 2012; 90 (7):2193-2200.
Chicago/Turabian StyleS. E. Echternkamp; P. Y. Aad; D. R. Eborn; L. J. Spicer. 2012. "Increased abundance of aromatase and follicle stimulating hormone receptor mRNA and decreased insulin-like growth factor-2 receptor mRNA in small ovarian follicles of cattle selected for twin births1,2." Journal of Animal Science 90, no. 7: 2193-2200.
Ovarian follicular growth and development are regulated by extraovarian and intraovarian factors, which influence granulosa cell proliferation and differentiation. However, the molecular mechanisms that drive follicular growth are not completely understood. Ovarian follicular cysts are one of the most common causes of reproductive failure in dairy cattle. Nevertheless, the primary cause of cyst formation has not been clearly established. A gene expression comparison may aid in elucidating the causes of ovarian cyst disease. Our objective was to identify differentially expressed genes in ovarian granulosa cells between normal dominant and cystic follicles of cattle. Granulosa cells and follicular fluid were isolated from dominant and cystic follicles collected via either ultrasound-guided aspiration from dairy cows (n = 24) or slaughterhouse ovaries from beef cows (n = 23). Hormonal analysis for progesterone, estradiol, and androstenedione in follicular fluid was performed by RIA. Total RNA was extracted and hybridized to 6 Affymetrix GeneChip Bovine Genome Arrays (Affymetrix, Santa Clara, CA). Abundance of mRNA for differentially expressed selected genes was determined through quantitative real-time reverse-transcription PCR. Follicular cysts showed greater (P < 0.05) progesterone, lesser (P < 0.05) estradiol, and no differences (P > 0.10) in androstenedione concentrations compared with noncystic follicles. A total of 163 gene sequences were differentially expressed (P < 0.01), with 19 upregulated and 144 downregulated. From selected target genes, quantitative real-time reverse-transcription PCR confirmed angiogenin, PGE2 receptor 4, and G-protein coupled receptor 34 genes as upregulated in cystic follicles, and Indian hedgehog protein precursor and secreted frizzled-related protein 4 genes as downregulated in cystic follicles. Further research is required to elucidate the role of these factors in follicular development and cyst formation. Copyright © 2011. American Society of Animal Science.
J. A. Grado-Ahuir; P. Y. Aad; L. J. Spicer. New insights into the pathogenesis of cystic follicles in cattle: Microarray analysis of gene expression in granulosa cells1. Journal of Animal Science 2011, 89, 1769 -1786.
AMA StyleJ. A. Grado-Ahuir, P. Y. Aad, L. J. Spicer. New insights into the pathogenesis of cystic follicles in cattle: Microarray analysis of gene expression in granulosa cells1. Journal of Animal Science. 2011; 89 (6):1769-1786.
Chicago/Turabian StyleJ. A. Grado-Ahuir; P. Y. Aad; L. J. Spicer. 2011. "New insights into the pathogenesis of cystic follicles in cattle: Microarray analysis of gene expression in granulosa cells1." Journal of Animal Science 89, no. 6: 1769-1786.
Resistin is an adipokine that has not been extensively studied in cattle but is produced by adipocytes in greater amounts in lactating versus non-lactating cattle. Seven experiments were conducted to determine the effect of resistin on proliferation, steroidogenesis, and gene expression of theca and granulosa cells from small (1-5mm) and/or large (8-22 mm) cattle follicles. Resistin had no effect on IGF-I-induced proliferation of large-follicle theca cells or small-follicle granulosa cells, but decreased IGF-I-induced proliferation of large-follicle granulosa cells. Resistin weakly stimulated FSH plus IGF-I-induced estradiol production by large-follicle granulosa cells, but had no effect on IGF-I- or insulin-induced progesterone and androstenedione production by theca cells or progesterone production by granulosa cells of large follicles. In small-follicle granulosa cells, resistin attenuated the stimulatory effect of IGF-I on progesterone and estradiol production of small-follicle granulosa cells. RT-PCR measuring abundance of side-chain cleavage enzyme (CYP11A1), aromatase (CYP19A1), FSH receptor (FSHR) and LH receptor (LHCGR) mRNA in large- and small-follicle granulosa cells indicated that resistin reduced the stimulatory effect of IGF-I on CPY11A1 mRNA abundance in large-follicle granulosa cells but had no effect on CYP19A1, FSHR or LHCGR mRNA abundance in large- or small-follicle granulosa cells. Resistin had no effect on CYP11A1, CYP17A1 or LHCGR mRNA abundance in theca cells. These results indicate that resistin preferentially inhibits steroidogenesis of undifferentiated (small follicle) granulosa cells and inhibits proliferation of differentiated (large follicle) granulosa cells, indicating that the ovarian response to resistin is altered during follicular development.
Leon J. Spicer; Nicole B. Schreiber; Dana V. Lagaly; Pauline Aad; Laura B. Douthit; Juan A. Grado-Ahuir. Effect of resistin on granulosa and theca cell function in cattle. Animal Reproduction Science 2011, 124, 19 -27.
AMA StyleLeon J. Spicer, Nicole B. Schreiber, Dana V. Lagaly, Pauline Aad, Laura B. Douthit, Juan A. Grado-Ahuir. Effect of resistin on granulosa and theca cell function in cattle. Animal Reproduction Science. 2011; 124 (1-2):19-27.
Chicago/Turabian StyleLeon J. Spicer; Nicole B. Schreiber; Dana V. Lagaly; Pauline Aad; Laura B. Douthit; Juan A. Grado-Ahuir. 2011. "Effect of resistin on granulosa and theca cell function in cattle." Animal Reproduction Science 124, no. 1-2: 19-27.
The expression of hedgehog (Hh) genes, their receptor, and the co-receptor in mice, rat, and bovine ovaries were investigated. RT-PCR of ovarian transcripts in mice showed amplification of transcripts for Indian (Ihh) and desert (Dhh) Hh, patched 1 (Ptch1), and smoothened (Smo) genes. Semi-quantitative RT-PCR and northern blot analyses showed that whole ovarianIhhandDhhtranscripts decreased 4–24 h after hCG versus 0–48 h after pregnant mares serum gonadotrophin treatment in mice, whereas mousePtch1andSmotranscripts were expressed throughout the gonadotropin treatments. Quantitative real-time RT-PCR (qRT-PCR) revealed that the expression of the Hh-patched signaling system withIhhmRNA abundance in granulosa cells was greater, whereasSmoandPtch1mRNA abundance was less in theca cells of small versus large follicles of cattle. In cultured rat and bovine theca-interstitial cells, qRT-PCR analyses revealed that the abundance ofGli1andPtch1mRNAs were increased (PIhhmRNA abundance in bovine granulosa cells. The expression and regulation ofIhhtranscripts in granulosa cells andPtch1mRNA in theca cells suggest a potential paracrine role of this system in bovine follicular development. This study illustrates for the first time Hh activation of Gli1 transcriptional factor in theca cells and its stimulation of theca cell proliferation and androgen biosynthesis.
Leon J Spicer; Satoko Sudo; Pauline Aad; Lora Shuo Wang; Sang-Young Chun; Izhar Ben-Shlomo; Cindy Klein; Aaron J W Hsueh. The hedgehog-patched signaling pathway and function in the mammalian ovary: a novel role for hedgehog proteins in stimulating proliferation and steroidogenesis of theca cells. REPRODUCTION 2009, 138, 329 -339.
AMA StyleLeon J Spicer, Satoko Sudo, Pauline Aad, Lora Shuo Wang, Sang-Young Chun, Izhar Ben-Shlomo, Cindy Klein, Aaron J W Hsueh. The hedgehog-patched signaling pathway and function in the mammalian ovary: a novel role for hedgehog proteins in stimulating proliferation and steroidogenesis of theca cells. REPRODUCTION. 2009; 138 (2):329-339.
Chicago/Turabian StyleLeon J Spicer; Satoko Sudo; Pauline Aad; Lora Shuo Wang; Sang-Young Chun; Izhar Ben-Shlomo; Cindy Klein; Aaron J W Hsueh. 2009. "The hedgehog-patched signaling pathway and function in the mammalian ovary: a novel role for hedgehog proteins in stimulating proliferation and steroidogenesis of theca cells." REPRODUCTION 138, no. 2: 329-339.
Insulin-like growth factor-I in conjunction with gonadotropins are important stimulators of mitosis and ovarian steroid production by granulosa and thecal cells, which are required for normal oocyte development and hormonal feedback signaling to the hypothalamus and pituitary. However, a comprehensive evaluation of the changes in gene expression induced by IGF-I has not been conducted. Our objective was to characterize granulosa cell gene expression in response to IGF-I treatment. Porcine granulosa cells were pooled in 4 biological replicates and treated with FSH (baseline) or FSH+IGF-I for 24 h in vitro. The RNA was collected and hybridized to 8 Affymetrix Porcine GeneChips (Affymetrix, Santa Clara, CA) in a paired design. Differentially regulated gene sequence element sets (P < 0.01) were used as queries in the UniGene database searching for annotated genes. Abundance of messenger RNA (mRNA) for genes differentially expressed in the microarray analysis was determined through multiplex assays of one-step real-time reverse transcription-PCR and further analyzed under a statistical model including the fixed effect of treatment. A total of 388 gene sequence element sets were differentially expressed, and 42 matched annotated genes in the UniGene database. Of the 3 upregulated target genes selected for further quantitative reverse transcription-PCR analysis, only FGF receptor 2 III c (FGFR2IIIc) mRNA abundance was significantly increased by IGF-I. Of the 3 downregulated target genes selected for further analysis, only thrombospondin-1 (THBS1) mRNA abundance was significantly decreased by IGF-I. Further study revealed that neither FSH nor estradiol affected the IGF-I-induced suppression of THBS1 mRNA abundance. These results provide the first comprehensive assessment of IGF-I-induced gene expression in granulosa cells and will contribute to a better understanding of the molecular mechanisms of IGF-I regulation of follicular development. Involvement of FGFR2IIIc and THBS1 in mediating IGF-I-induced granulosa cell steroidogenesis and proliferation during follicular development is novel, but their specific roles will require further elucidation. Copyright © 2009. . Copyright 2009 Journal of Animal Science
J. A. Grado-Ahuir; P. Y. Aad; G. Ranzenigo; F. Caloni; Fausto Cremonesi; L. J. Spicer. Microarray analysis of insulin-like growth factor-I-induced changes in messenger ribonucleic acid expression in cultured porcine granulosa cells: Possible role of insulin-like growth factor-I in angiogenesis1,2. Journal of Animal Science 2009, 87, 1921 -1933.
AMA StyleJ. A. Grado-Ahuir, P. Y. Aad, G. Ranzenigo, F. Caloni, Fausto Cremonesi, L. J. Spicer. Microarray analysis of insulin-like growth factor-I-induced changes in messenger ribonucleic acid expression in cultured porcine granulosa cells: Possible role of insulin-like growth factor-I in angiogenesis1,2. Journal of Animal Science. 2009; 87 (6):1921-1933.
Chicago/Turabian StyleJ. A. Grado-Ahuir; P. Y. Aad; G. Ranzenigo; F. Caloni; Fausto Cremonesi; L. J. Spicer. 2009. "Microarray analysis of insulin-like growth factor-I-induced changes in messenger ribonucleic acid expression in cultured porcine granulosa cells: Possible role of insulin-like growth factor-I in angiogenesis1,2." Journal of Animal Science 87, no. 6: 1921-1933.
To determine if tumor necrosis factor α (TNF-α) and interleukin-6 (IL-6). IL-6 gene expression is influenced by amount and source of dietary fat, 30 weanling female rats were randomly assigned to a moderate-fat soybean oil (MFS; 22% of total energy fed as fat), high-fat (HF) soybean oil (HFS; 39% of total energy fed as fat), or HF tallow (HFT; 39% of total energy fed as fat) diet treatments. Oral glucose tolerance tests (OGTT) were conducted serially over 10 weeks of treatment. HFT and HFS rats gained more weight and had greater body fat than the MFS rats fed similar amounts of energy. Both groups of HF-fed rats had greater (P<.05) insulin resistance (homeostasis model assessment) than MFS-fed rats. TNF-α mRNA abundance quantified by real-time reverse transcriptase-polymerase chain reaction was greater (P<.05) in liver and lower (P<.05) in adipose tissue in HFT compared to HFS and MFS rats. There were positive correlations (P<.05) between hepatic TNF-α mRNA and insulin resistance, and negative correlations between insulin sensitivity and hepatic TNF-α mRNA and hepatic IL-6 mRNA. During Week 3 and Week 6 OGTTs, hyperinsulinemic responses were observed in the HFT group, after which, on Week 9, insulin secretion was diminished in response to the OGTT, suggesting impaired pancreatic insulin secretion. HFS rats exhibited insulin resistance on Week 9 OGTT. In summary, an HFT diet fed to growing female rats caused insulin resistance associated with increased hepatic TNF-α mRNA leading to pancreatic insufficiency. Early-onset insulin resistance related to the inflammatory process in obesity is influenced by the amount and type of fat in the diet.
Anne M. Flanagan; Jackie L. Brown; Consuelo A. Santiago; Pauline Y. Aad; Leon J. Spicer; Maria T. Spicer. High-fat diets promote insulin resistance through cytokine gene expression in growing female rats. The Journal of Nutritional Biochemistry 2008, 19, 505 -513.
AMA StyleAnne M. Flanagan, Jackie L. Brown, Consuelo A. Santiago, Pauline Y. Aad, Leon J. Spicer, Maria T. Spicer. High-fat diets promote insulin resistance through cytokine gene expression in growing female rats. The Journal of Nutritional Biochemistry. 2008; 19 (8):505-513.
Chicago/Turabian StyleAnne M. Flanagan; Jackie L. Brown; Consuelo A. Santiago; Pauline Y. Aad; Leon J. Spicer; Maria T. Spicer. 2008. "High-fat diets promote insulin resistance through cytokine gene expression in growing female rats." The Journal of Nutritional Biochemistry 19, no. 8: 505-513.
Fusarium mycotoxins, such as trichothecenes and zearalenone, are common grain and foodstuffs contaminants. Some of these like deoxynivalenol (DON) can negatively impact pregnancy success in swine, but evidence for direct ovarian effects of DON, zearalenone, and its major metabolite, alpha-zearalenol (ZEA) is meager. To evaluate the effects of two mycotoxins, DON and ZEA on porcine granulosa cell(s) (GC) proliferation, steroidogenesis and gene expression, pig GC from small follicles (1-5mm) were cultured for 2 days in 5% fetal bovine serum and 5% porcine serum-containing medium followed by 2 days in serum-free medium containing control (no mycotoxins) or mycotoxins (at various doses/combinations). Both DON and ZEA had biphasic effects on IGF-I-induced estradiol production, increasing estradiol production at smaller doses and inhibiting at larger doses. ZEA at 3,000 ng/mL (9.37 microM) increased IGF-I-induced progesterone production and at 30 ng/mL (0.0937 microM) and 300 ng/mL (0.937 microM) were without effect, but these doses of ZEA increased FSH-induced progesterone production. ZEA at 3,000 ng/mL inhibited FSH plus IGF-I-induced CYP19A1 and CYP11A1 mRNA abundance. DON inhibited progesterone production at 100 ng/mL (0.337 microM) and 1,000 ng/mL (3.37 microM) but at 10 ng/mL (0.0337 microM) was without effect. DON at 1,000 ng/mL (but not at 10 ng/mL) completely inhibited FSH plus IGF-I-induced CYP19A1 and CYP11A1 mRNA abundance. The concomitant treatment of ZEA had little effect on the dose response to DON. DON increased IGF-I-induced cell numbers at 10 and 100 ng/mL and inhibited cell numbers at 1,000 ng/mL, whereas ZEA had no effect on GC numbers. Only a combined treatment of DON and ZEA increased serum-induced cell proliferation. In conclusion, mycotoxins have direct dose-dependent effects on GC proliferation, steroidogenesis and gene expression. These direct ovarian effects could be one mechanism whereby contaminating Fusarium mycotoxins in feedstuffs could impact reproductive performance in swine.
Giovanni Ranzenigo; Francesca Caloni; Fausto Cremonesi; Pauline Y. Aad; Leon J. Spicer. Effects of Fusarium mycotoxins on steroid production by porcine granulosa cells. Animal Reproduction Science 2008, 107, 115 -130.
AMA StyleGiovanni Ranzenigo, Francesca Caloni, Fausto Cremonesi, Pauline Y. Aad, Leon J. Spicer. Effects of Fusarium mycotoxins on steroid production by porcine granulosa cells. Animal Reproduction Science. 2008; 107 (1-2):115-130.
Chicago/Turabian StyleGiovanni Ranzenigo; Francesca Caloni; Fausto Cremonesi; Pauline Y. Aad; Leon J. Spicer. 2008. "Effects of Fusarium mycotoxins on steroid production by porcine granulosa cells." Animal Reproduction Science 107, no. 1-2: 115-130.
Adiponectin is an adipokine that has been implicated in insulin resistance, a condition associated with polycystic ovarian syndrome in humans, but whether adiponectin can directly affect ovarian theca or granulosa cell function is unknown. Therefore, to determine the effects of adiponectin on proliferation, steroidogenesis and gene expression of large-follicle theca and granulosa cells, experiments were conducted using bovine ovarian cell cultures. RT-PCR was used to elucidate the effects of adiponectin on gene expression of CYP11A1 and LH receptor (LHR) in large-follicle theca and granulosa cells, as well as expression of CYP17A1 in theca cells and CYP19A1 in granulosa cells. Adiponectin decreased (P < 0.05) insulin-induced progesterone and androstenedione production as well as attenuated IGF-I-induced LHR, CYP11A1, and CYP17A1 gene expression in theca cells. In contrast, adiponectin decreased (P < 0.05) LHR mRNA abundance in granulosa cells but did not affect steroidogenic enzyme gene expression in granulosa cells. Adiponectin had no effect (P > 0.10) on proliferation of large-follicle theca cells. RT-PCR also revealed that abundance of mRNA for the adiponectin receptor (ADIPOR2) was greater (P < 0.05) in large-follicle than in small-follicle theca cells and did not significantly differ between small- and large-follicle granulosa cells. In cultured theca cells, LH increased (P < 0.05) and IGF-I decreased (P < 0.05) ADIPOR2 mRNA abundance. These results indicate that the inhibitory effects of adiponectin on steroidogenesis are primarily localized to theca cells and that the response of theca cells to adiponectin (i.e., ADIPOR2) may be regulated by LH and IGF-I.
Dana V. Lagaly; Pauline Aad; Juan A. Grado-Ahuir; Laura B. Hulsey; Leon J. Spicer. Role of adiponectin in regulating ovarian theca and granulosa cell function. Molecular and Cellular Endocrinology 2008, 284, 38 -45.
AMA StyleDana V. Lagaly, Pauline Aad, Juan A. Grado-Ahuir, Laura B. Hulsey, Leon J. Spicer. Role of adiponectin in regulating ovarian theca and granulosa cell function. Molecular and Cellular Endocrinology. 2008; 284 (1):38-45.
Chicago/Turabian StyleDana V. Lagaly; Pauline Aad; Juan A. Grado-Ahuir; Laura B. Hulsey; Leon J. Spicer. 2008. "Role of adiponectin in regulating ovarian theca and granulosa cell function." Molecular and Cellular Endocrinology 284, no. 1: 38-45.
Ovarian follicular development is controlled by numerous paracrine and endocrine regulators, including oocyte-derived growth differentiation factor 9 (GDF9), and a localized increase in bioavailable insulin-like growth factor 1 (IGF1). The effects of GDF9 on function of theca cells collected from small (3–6 mm) and large (8–22 mm) ovarian follicles were investigated. In small-follicle theca cells cultured in the presence of both LH and IGF1, GDF9 increased cell numbers and DNA synthesis, as measured by a 3H-thymidine incorporation assay, and dose-dependently decreased both progesterone and androstenedione production. Theca cells from large follicles had little or no response to GDF9 in terms of cell proliferation or steroid production induced by IGF1. Small-follicle theca cell studies indicated that GDF9 decreased the abundance of LHR and CYP11A1 mRNA in theca cells, but had no effect on IGF1R, STAR, or CYP17A1 mRNA abundance or the percentage of cells staining for CYP17A1 proteins. GDF9 activated similar to mothers against decapentaplegics (SMAD) 2/3-induced CAGA promoter activity in transfected theca cells. Small-follicle theca cells had more ALK5 mRNA than large-follicle theca cells. Small-follicle granulosa cells appeared to have greater GDF9 mRNA abundance than large-follicle granulosa cells, but theca cells had no detectable GDF9 mRNA. We conclude that theca cells from small follicles are more responsive to GDF9 than those from large follicles and that GDF9 mRNA may be produced by granulosa cells in cattle. Because GDF9 increased theca cell proliferation and decreased theca cell steroidogenesis, oocyte- and granulosa cell-derived GDF9 may simultaneously promote theca cell proliferation and prevent premature differentiation of the theca interna during early follicle development.
Leon J. Spicer; Pauline Y. Aad; Dustin T. Allen; Sabine Mazerbourg; Anita H. Payne; Aaron J. Hsueh. Growth Differentiation Factor 9 (GDF9) Stimulates Proliferation and Inhibits Steroidogenesis by Bovine Theca Cells: Influence of Follicle Size on Responses to GDF91. Biology of Reproduction 2008, 78, 243 -253.
AMA StyleLeon J. Spicer, Pauline Y. Aad, Dustin T. Allen, Sabine Mazerbourg, Anita H. Payne, Aaron J. Hsueh. Growth Differentiation Factor 9 (GDF9) Stimulates Proliferation and Inhibits Steroidogenesis by Bovine Theca Cells: Influence of Follicle Size on Responses to GDF91. Biology of Reproduction. 2008; 78 (2):243-253.
Chicago/Turabian StyleLeon J. Spicer; Pauline Y. Aad; Dustin T. Allen; Sabine Mazerbourg; Anita H. Payne; Aaron J. Hsueh. 2008. "Growth Differentiation Factor 9 (GDF9) Stimulates Proliferation and Inhibits Steroidogenesis by Bovine Theca Cells: Influence of Follicle Size on Responses to GDF91." Biology of Reproduction 78, no. 2: 243-253.
Little is known regarding the role of insulin-like growth factor 2 (IGF2) and the regulation of the IGF2 receptor (IGF2R) during follicular development. Granulosa cells were collected from small (1–5 mm) and large (8–22 mm) bovine follicles and were treated with IGF2 for 1–2 days in serum-free medium, and steroid production, cell proliferation, specific 125I-IGF2 binding, and gene expression were quantified. IGF2 increased both estradiol and progesterone production by granulosa cells, and cells from large follicles were more responsive to the effects of IGF2 than those from small follicles. Abundance of aromatase (CYP19A1) mRNA was stimulated by IGF2 and IGF1. The effective dose (ED50) of IGF2 stimulating 50% of the maximal estradiol production was 63 ng/ml for small follicles and 12 ng/ml for large follicles, and these values were not affected by FSH. The ED50 of IGF2 for progesterone production was 20 ng/ml for both small and large follicles. IGF2 also increased proliferation of granulosa cells by 2- to 3-fold, as determined by increased cell numbers and 3H-thymidine incorporation into DNA. Treatment with IGF1R antibodies reduced the stimulatory effect of IGF2 and IGF1 on estradiol production and cell proliferation. Specific receptors for 125I-IGF2 existed in granulosa cells, and 2-day treatment with estradiol, FSH, or cortisol had no significant effect on specific 125I-IGF2 binding. Also, FSH treatment of small- and large-follicle granulosa cells had no effect on IGF2R mRNA levels, whereas IGF1 decreased IGF2R mRNA and specific 125I-IGF2 binding. Granulosa cell IGF2R mRNA abundance was 3-fold greater in small than in large follicles. These findings support the hypothesis that both IGF2 and its receptor may play a role in granulosa cell function during follicular development. In particular, increased free IGF1 in developing follicles may decrease synthesis of IGF2R, thereby allowing for more IGF2 to be bioavailable (free) for induction of steroidogenesis and mitogenesis via the IGF1R.
L.J. Spicer; Pauline Aad. Insulin-Like Growth Factor (IGF) 2 Stimulates Steroidogenesis and Mitosis of Bovine Granulosa Cells Through the IGF1 Receptor: Role of Follicle-Stimulating Hormone and IGF2 Receptor1. Biology of Reproduction 2007, 77, 18 -27.
AMA StyleL.J. Spicer, Pauline Aad. Insulin-Like Growth Factor (IGF) 2 Stimulates Steroidogenesis and Mitosis of Bovine Granulosa Cells Through the IGF1 Receptor: Role of Follicle-Stimulating Hormone and IGF2 Receptor1. Biology of Reproduction. 2007; 77 (1):18-27.
Chicago/Turabian StyleL.J. Spicer; Pauline Aad. 2007. "Insulin-Like Growth Factor (IGF) 2 Stimulates Steroidogenesis and Mitosis of Bovine Granulosa Cells Through the IGF1 Receptor: Role of Follicle-Stimulating Hormone and IGF2 Receptor1." Biology of Reproduction 77, no. 1: 18-27.
Ovarian follicular growth and dominance are controlled by a series of hormonal and intraovarian events including a decrease in intrafollicular IGF-binding proteins -2, -4 and -5 levels. Proteolytic enzymes such as pregnancy-associated plasma protein-A (PAPP-A) degrade IGFBPs and increase bioavailability of IGF-I and -II during follicular development. The objective of this study was to determine the effect of IGF-I, IGF-II, insulin (INS), LH, FSH, estradiol (E2), leptin or cortisol on ovarian PAPP-A mRNA levels. Granulosa (GC) from small (SM) (1-5 mm) and large (LG) (8-22 mm) follicles as well as theca cells (TC) from LG follicles were collected from bovine ovaries and cultured for 48 h in medium containing 10% FCS and then treated with various hormones in serum-free medium for an additional 24 h. Cells were treated with various concentrations (3-500 ng/ml) and combinations of IGF-I, IGF-II, FSH, LH, E2, INS, leptin and (or) cortisol for 24 h (Experiments 1-10). PAPP-A mRNA levels were measured using quantitative real-time RT-PCR. In SM-GC and LG-GC, none of the treatments significantly affected (P>0.10) PAPP-A mRNA abundance. In LG-TC, IGF-I, LH or cortisol did not affect (P>0.10) PAPP-A mRNA levels, whereas INS with or without LH decreased (P<0.05) PAPP-A mRNA. E2 alone decreased PAPP-A mRNA levels in LG-TC, and E2 amplified the insulin-induced inhibition of PAPP-A mRNA abundance in LG-TC. We conclude that control of PAPP-A mRNA abundance in granulosa and theca cells differs, and that E2 may be part of an intraovarian negative feedback system which may reduce the bioavailable IGFs in the theca layer during growth and selection of follicles.
Pauline Y. Aad; Justin L. Voge; Consuelo A. Santiago; Jerry R. Malayer; Leon J. Spicer. Real-time RT-PCR quantification of pregnancy-associated plasma protein-A mRNA abundance in bovine granulosa and theca cells: Effects of hormones in vitro. Domestic Animal Endocrinology 2006, 31, 357 -372.
AMA StylePauline Y. Aad, Justin L. Voge, Consuelo A. Santiago, Jerry R. Malayer, Leon J. Spicer. Real-time RT-PCR quantification of pregnancy-associated plasma protein-A mRNA abundance in bovine granulosa and theca cells: Effects of hormones in vitro. Domestic Animal Endocrinology. 2006; 31 (4):357-372.
Chicago/Turabian StylePauline Y. Aad; Justin L. Voge; Consuelo A. Santiago; Jerry R. Malayer; Leon J. Spicer. 2006. "Real-time RT-PCR quantification of pregnancy-associated plasma protein-A mRNA abundance in bovine granulosa and theca cells: Effects of hormones in vitro." Domestic Animal Endocrinology 31, no. 4: 357-372.
In addition to gonadotropins, steroidogenesis and proliferation of granulosa cells during follicular development are controlled by a number of intraovarian factors including growth differentiation factor-9 (GDF-9), bone morphogenetic protein-4 (BMP-4), and IGF-I. The objective of this study was to determine the effect of GDF-9 and BMP-4 and their interaction with IGF-I and FSH on ovarian granulosa cell function in cattle. Granulosa cells from small (1–5 mm) and large (8–22 mm) follicles were collected from bovine ovaries and cultured for 48 h in medium containing 10% fetal calf serum and then treated with various hormones in serum-free medium for an additional 48 h. We evaluated the effects of GDF-9 (150–600 ng/ml) and BMP-4 (30 ng/ml) during a 2-day exposure on hormone-induced steroidogenesis and cell proliferation. In FSH plus IGF-I-treated granulosa cells obtained from small follicles, 300 ng/ml GDF-9 reduced (PPPP>0.10). Treatment with 600 ng/ml GDF-9 increased (PPPP>0.10) on estradiol production. In FSH plus IGF-I-treated granulosa cells obtained from large follicles, GDF-9 caused a dose-dependent decrease (PP
Leon Spicer; Pauline Aad; D Allen; S Mazerbourg; A J Hsueh. Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells. Journal of Endocrinology 2006, 189, 329 -339.
AMA StyleLeon Spicer, Pauline Aad, D Allen, S Mazerbourg, A J Hsueh. Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells. Journal of Endocrinology. 2006; 189 (2):329-339.
Chicago/Turabian StyleLeon Spicer; Pauline Aad; D Allen; S Mazerbourg; A J Hsueh. 2006. "Growth differentiation factor-9 has divergent effects on proliferation and steroidogenesis of bovine granulosa cells." Journal of Endocrinology 189, no. 2: 329-339.