RNA sequencing and differential expression reveals the effects of serial oestrus synchronisation on ovarian genes in dairy goats
Shuang Sun A , Cong Li A , Shimin Liu B , Jun Luo A C , Zhi Chen A , Changhui Zhang A , Tianying Zhang A , Jiangtao Huang A and Limeng Xi A
+ Author Affiliations
- Author Affiliations
A Shaanxi Key Laboratory of Molecular Biology for Agriculture, College of Animal Science and Technology, Northwest A&F University, Yangling, Shaanxi, 712100, PR China.
B School of Agriculture and Environment, The University of Western Australia, Crawley, WA 6009, Australia.
C Corresponding author. Email: luojun@nwafu.edu.cn
Reproduction, Fertility and Development 30(12) 1622-1633 https://doi.org/10.1071/RD17511
Submitted: 6 December 2017 Accepted: 5 May 2018 Published: 7 June 2018
Abstract
A total of 24 female Xinong Saanen dairy goats were used to examine differentially expressed genes (DEGs) in the ovaries of goats treated once or three times for oestrus synchronisation (ES). The goats were randomly divided into two groups: one group received three ES treatments at fortnightly intervals (repeated or triple ES group), whereas the other was only treated once on the same day as the third ES treatment for the triple group (control group) during the breeding season. Ovaries of three goats in oestrus from each group were collected for morphological examination and transcriptome sequencing, while the rest of the goats were artificially inseminated twice. Litter size and fecundity rate tended (P = 0.06) to be lower in the triple ES group. A total of 319 DEGs were identified, including carbohydrate sulphotransferase 8 (CHST8), corticosteroid-binding globulin (CBG), oestradiol 17-β-dehydrogenase 1 (DHB1), oestrogen receptor 1 (ESR1), progestin and adipoQ receptor family member 4 (PAQR4), PAQR9, prostacyclin synthase (PTGIS), contactin-associated protein (CNTNAP4), matrix metalloproteinase-2 (MMP-2), regulator of G-protein signalling 9-2 (RGS9-2) and sperm surface protein Sp17 (Sp17); these were the most promising novel candidate genes for reproductive performances in goats. Our study indicates that triple ES could cause DNA damage and alter gene expression in goat ovaries, potentially affecting ovary function, neural regulation and hormone secretion.
Additional keywords: ovary function, ovary morphology, reproductive performance, triple ES treatment.
References
Anders, S., Pyl, P. T., and Huber, W. (2015). HTSeq – a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169.| HTSeq – a Python framework to work with high-throughput sequencing data.Crossref | GoogleScholarGoogle Scholar |
Arrais, R. F., and Dib, S. A. (2006). The hypothalamus-pituitary-ovary axis and Type 1 diabetes mellitus: a mini review. Hum. Reprod. 21, 327–337.
| The hypothalamus-pituitary-ovary axis and Type 1 diabetes mellitus: a mini review.Crossref | GoogleScholarGoogle Scholar |
Baril, G., Remy, B., Vallet, J., and Beckers, J.-F. (1992). Effect of repeated use of progestagen‐PMSG treatment for estrus control in dairy goats out of breeding season. Reprod. Domest. Anim. 27, 161–168.
| Effect of repeated use of progestagen‐PMSG treatment for estrus control in dairy goats out of breeding season.Crossref | GoogleScholarGoogle Scholar |
Baril, G., Leboeuf, B., and Saumande, J. (1993). Synchronization of estrus in goats: the relationship between time of occurrence of estrus and fertility following artificial insemination. Theriogenology 40, 621–628.
| Synchronization of estrus in goats: the relationship between time of occurrence of estrus and fertility following artificial insemination.Crossref | GoogleScholarGoogle Scholar |
Baril, G., Remy, B., Leboeuf, B., Beckers, J. F., and Saumande, J. (1996). Synchronization of estrus in goats: the relationship between eCG binding in plasma time of occurrence of estrus and fertility following artificial insemination. Theriogenology 45, 1553–1559.
| Synchronization of estrus in goats: the relationship between eCG binding in plasma time of occurrence of estrus and fertility following artificial insemination.Crossref | GoogleScholarGoogle Scholar |
Bavister, B. D., Dees, C., and Schultz, R. D. (1986). Refractoriness of rhesus monkeys to repeated ovarian stimulation by exogenous gonadotropins is caused by nonprecipitating antibodies. Am. J. Reprod. Immunol. Microbiol. 11, 11–16.
| Refractoriness of rhesus monkeys to repeated ovarian stimulation by exogenous gonadotropins is caused by nonprecipitating antibodies.Crossref | GoogleScholarGoogle Scholar |
Ben-Jonathan, N., and Hnasko, R. (2001). Dopamine as a prolactin (PRL) inhibitor. Endocr. Rev. 22, 724–763.
| Dopamine as a prolactin (PRL) inhibitor.Crossref | GoogleScholarGoogle Scholar |
Boiti, C., Castellini, C., Canali, C., Zampini, D., and Monaci, M. (1995). Long term effect of PMSG on rabbit does reproductive performance. World Rabbit Sci. 3, 51–56.
Cesana, A., Albani, E., Marras, A., Novara, P. V., Raucci, A., and Setti, P. E. L. (2007). SP17 and necrozoospermia. Fertil. Steril. 88, S367.
| SP17 and necrozoospermia.Crossref | GoogleScholarGoogle Scholar |
Chao, H. T., Lee, S. Y., Lee, H. M., Liao, T. L., Wei, Y. H., and Kao, S. H. (2005). Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries. Ann. N. Y. Acad. Sci. 1042, 148–156.
| Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries.Crossref | GoogleScholarGoogle Scholar |
Chiriva-Internati, M., Grizzi, F., Weidanz, J. A., Ferrari, R., Yu, Y. F., Velez, B., Shearer, M. H., Lowe, D. B., Frezza, E. E., Cobos, E., Kast, W. M., and Kennedy, R. C. (2007). A NOD/SCID tumor model for human ovarian cancer that allows tracking of tumor progression through the biomarker Sp17. J. Immunol. Methods 321, 86–93.
| A NOD/SCID tumor model for human ovarian cancer that allows tracking of tumor progression through the biomarker Sp17.Crossref | GoogleScholarGoogle Scholar |
Chou, C. S., Zhu, H., MacCalman, C. D., and Leung, P. C. K. (2003). Regulatory effects of gonadotropin-releasing hormone (GnRH) I and GnRH II on the levels of matrix metalloproteinase (MMP)-2, MMP-9, and tissue inhibitor of metalloproteinases-1 in primary cultures of human extravillous cytotrophoblasts. J. Clin. Endocrinol. Metab. 88, 4781–4790.
| Regulatory effects of gonadotropin-releasing hormone (GnRH) I and GnRH II on the levels of matrix metalloproteinase (MMP)-2, MMP-9, and tissue inhibitor of metalloproteinases-1 in primary cultures of human extravillous cytotrophoblasts.Crossref | GoogleScholarGoogle Scholar |
Combelles, C. M. H., and Albertini, D. F. (2003). Assessment of oocyte quality following repeated gonadotropin stimulation in the mouse. Biol. Reprod. 68, 812–821.
| Assessment of oocyte quality following repeated gonadotropin stimulation in the mouse.Crossref | GoogleScholarGoogle Scholar |
Comings, D. E., Muhleman, D., Johnson, P., and MacMurray, J. P. (1999). Potential role of the estrogen receptor gene (ESR1) in anxiety. Mol. Psychiatry 4, 374–377.
| Potential role of the estrogen receptor gene (ESR1) in anxiety.Crossref | GoogleScholarGoogle Scholar |
Crisà, A., Ferre, F., Chillemi, G., and Moioli, B. (2016). RNA-Sequencing for profiling goat milk transcriptome in colostrum and mature milk. BMC Vet. Res. 12, 264.
| RNA-Sequencing for profiling goat milk transcriptome in colostrum and mature milk.Crossref | GoogleScholarGoogle Scholar |
Dong, G., Guo, Y., Cao, H., Zhou, T., Zhou, Z., Sha, J., Guo, X., and Zhu, H. (2014). Long-term effects of repeated superovulation on ovarian structure and function in rhesus monkeys. Fertil. Steril. 102, 1452–1457.
| Long-term effects of repeated superovulation on ovarian structure and function in rhesus monkeys.Crossref | GoogleScholarGoogle Scholar |
Drion, P. V., Furtoss, V., Baril, G., Manfredi, E., Bouvier, F., Pougnard, J. L., Bernelas, D., Caugnon, P., McNamara, E. M., Remy, B., Sulon, J., Beckers, J. F., Bodin, L., and Lebceuf, B. (2001). Four years of induction/synchronization of estrus in dairy goats: effect on the evolution of eCG binding rate in relation with the parameters of reproduction. Reprod. Nutr. Dev. 41, 401–412.
| Four years of induction/synchronization of estrus in dairy goats: effect on the evolution of eCG binding rate in relation with the parameters of reproduction.Crossref | GoogleScholarGoogle Scholar |
Forcada, F., Abecia, J. A., Lozano, J. M., and Zúñiga, O. (2000). Repeated superovulation of high-prolificacy Rasa Aragonesa ewes before culling as an inexpensive way to obtain high-quality embryos. Livest. Prod. Sci. 66, 263–269.
| Repeated superovulation of high-prolificacy Rasa Aragonesa ewes before culling as an inexpensive way to obtain high-quality embryos.Crossref | GoogleScholarGoogle Scholar |
Forcada, F., Ait Am.-Meziane, M., Abecia, J. A., Maurel, M. C., Cebrian-Perez, J. A., Muino-Blanco, T., Asenjo, B., Vazquez, M. I., and Casao, A. (2011). Repeated superovulation using a simplified FSH/eCG treatment for in vivo embryo production in sheep. Theriogenology 75, 769–776.
| Repeated superovulation using a simplified FSH/eCG treatment for in vivo embryo production in sheep.Crossref | GoogleScholarGoogle Scholar |
Giesecke, K., Hamann, H., Stock, K. F., Klewitz, J., Martinsson, G., Distl, O., and Sieme, H. (2011). Evaluation of ACE, SP17, and FSHB as candidates for stallion fertility in Hanoverian warmblood horses. Anim. Reprod. Sci. 126, 200–206.
| Evaluation of ACE, SP17, and FSHB as candidates for stallion fertility in Hanoverian warmblood horses.Crossref | GoogleScholarGoogle Scholar |
Gunawan, A., Kaewmala, K., Uddin, M. J., Cinar, M. U., Tesfaye, D., Phatsara, C., Tholen, E., Looft, C., and Schellander, K. (2011). Association study and expression analysis of porcine ESR1 as a candidate gene for boar fertility and sperm quality. Anim. Reprod. Sci. 128, 11–21.
| Association study and expression analysis of porcine ESR1 as a candidate gene for boar fertility and sperm quality.Crossref | GoogleScholarGoogle Scholar |
Hakkarainen, J., Jokela, H., Pakarinen, P., Heikela, H., Katkanaho, L., Vandenput, L., Ohlsson, C., Zhang, F. P., and Poutanen, M. (2015). Hydroxysteroid (17beta)-dehydrogenase 1-deficient female mice present with normal puberty onset but are severely subfertile due to a defect in luteinization and progesterone production. FASEB J. 29, 3806–3816.
| Hydroxysteroid (17beta)-dehydrogenase 1-deficient female mice present with normal puberty onset but are severely subfertile due to a defect in luteinization and progesterone production.Crossref | GoogleScholarGoogle Scholar |
He, W., Cowan, C. W., and Wensel, T. G. (1998). RGS9, a GTPase accelerator for phototransduction. Neuron 20, 95–102.
| RGS9, a GTPase accelerator for phototransduction.Crossref | GoogleScholarGoogle Scholar |
Helliwell, R. J., Adams, L. F., and Mitchell, M. D. (2004). Prostaglandin synthases: recent developments and a novel hypothesis. Prostaglandins Leukot. Essent. Fatty Acids 70, 101–113.
| Prostaglandin synthases: recent developments and a novel hypothesis.Crossref | GoogleScholarGoogle Scholar |
Karayannis, T., Au, E., Patel, J. C., Kruglikov, I., Markx, S., Delorme, R., Heron, D., Salomon, D., Glessner, J., Restituito, S., Gordon, A., Rodriguez-Murillo, L., Roy, N. C., Gogos, J. A., Rudy, B., Rice, M. E., Karayiorgou, M., Hakonarson, H., Keren, B., Huguet, G., Bourgeron, T., Hoeffer, C., Tsien, R. W., Peles, E., and Fishell, G. (2014). Cntnap4 differentially contributes to GABAergic and dopaminergic synaptic transmission. Nature 511, 236–240.
| Cntnap4 differentially contributes to GABAergic and dopaminergic synaptic transmission.Crossref | GoogleScholarGoogle Scholar |
Kato, R., and Ogawa, H. (1994). An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae. Nucleic Acids Res. 22, 3104–3112.
| An essential gene, ESR1, is required for mitotic cell growth, DNA repair and meiotic recombination in Saccharomyces cerevisiae.Crossref | GoogleScholarGoogle Scholar |
Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., and Salzberg, S. L. (2013). TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36.
| TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.Crossref | GoogleScholarGoogle Scholar |
Lamp, M., Peters, M., Reinmaa, E., Haller-Kikkatalo, K., Kaart, T., Kadastik, U., Karro, H., Metspalu, A., and Salumets, A. (2011). Polymorphisms in ESR1, ESR2 and HSD17B1 genes are associated with fertility status in endometriosis. Gynecol. Endocrinol. 27, 425–433.
| Polymorphisms in ESR1, ESR2 and HSD17B1 genes are associated with fertility status in endometriosis.Crossref | GoogleScholarGoogle Scholar |
Lee, S. H., and Mouradian, M. M. (1999). Up-regulation of D1A dopamine receptor gene transcription by estrogen. Mol. Cell. Endocrinol. 156, 151–157.
| Up-regulation of D1A dopamine receptor gene transcription by estrogen.Crossref | GoogleScholarGoogle Scholar |
Li, F. Q., Han, Y. L., Liu, Q., Wu, B., Huang, W. B., and Zeng, S. Y. (2009). Overexpression of human sperm protein 17 increases migration and decreases the chemosensitivity of human epithelial ovarian cancer cells. BMC Cancer 9, 323.
| Overexpression of human sperm protein 17 increases migration and decreases the chemosensitivity of human epithelial ovarian cancer cells.Crossref | GoogleScholarGoogle Scholar |
Ling, Y. H., Xiang, H., Li, Y. S., Liu, Y., Zhang, Y. H., Zhang, Z. J., Ding, J. P., and Zhang, X. R. (2014). Exploring differentially expressed genes in the ovaries of uniparous and multiparous goats using the RNA-Seq (quantification) method. Gene 550, 148–153.
| Exploring differentially expressed genes in the ovaries of uniparous and multiparous goats using the RNA-Seq (quantification) method.Crossref | GoogleScholarGoogle Scholar |
Liu, L. Q., Li, F. E., Deng, C. Y., Zuo, B., Zheng, R., and Xiong, Y. Z. (2009). Polymorphism of the pig 17beta-hydroxysteroid dehydrogenase type1 (HSD17B1) gene and its association with reproductive traits. Anim. Reprod. Sci. 114, 318–323.
| Polymorphism of the pig 17beta-hydroxysteroid dehydrogenase type1 (HSD17B1) gene and its association with reproductive traits.Crossref | GoogleScholarGoogle Scholar |
Löseke, A., and Spanel-Borowski, K. (1996). Simple or repeated induction of superovulation: a study on ovulation rates and microvessel corrosion casts in ovaries of golden hamsters. Ann. Anat. 178, 5–14.
| Simple or repeated induction of superovulation: a study on ovulation rates and microvessel corrosion casts in ovaries of golden hamsters.Crossref | GoogleScholarGoogle Scholar |
Love, M. I., Huber, W., and Anders, S. (2014). Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550.
| Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.Crossref | GoogleScholarGoogle Scholar |
Melo, M. B., Nguyen, Q. P., Cordeiro, C., Hassan, M. A., Yang, N., McKell, R., Rosowski, E. E., Julien, L., Butty, V., Darde, M. L., Ajzenberg, D., Fitzgerald, K., Young, L. H., and Saeij, J. P. (2013). Transcriptional analysis of murine macrophages infected with different Toxoplasma strains identifies novel regulation of host signaling pathways. PLoS Pathog. 9, e1003779.
| Transcriptional analysis of murine macrophages infected with different Toxoplasma strains identifies novel regulation of host signaling pathways.Crossref | GoogleScholarGoogle Scholar |
Miao, X., Luo, Q., and Qin, X. (2016). Genome-wide transcriptome analysis in the ovaries of two goats identifies differentially expressed genes related to fecundity. Gene 582, 69–76.
| Genome-wide transcriptome analysis in the ovaries of two goats identifies differentially expressed genes related to fecundity.Crossref | GoogleScholarGoogle Scholar |
Minhas, V., Shrestha, A., Wadhwa, N., Singh, R., and Gupta, S. K. (2016). Novel sperm and gonadotropin-releasing hormone-based recombinant fusion protein: achievement of 100% contraceptive efficacy by co-immunization of male and female mice. Mol. Reprod. Dev. 83, 1048–1059.
| Novel sperm and gonadotropin-releasing hormone-based recombinant fusion protein: achievement of 100% contraceptive efficacy by co-immunization of male and female mice.Crossref | GoogleScholarGoogle Scholar |
Miyata, A., Hara, S., Yokoyama, C., Inoue, H., Ullrich, V., and Tanabe, T. (1994). Molecular cloning and expression of human prostacyclin synthase. Biochem. Biophys. Res. Commun. 200, 1728–1734.
| Molecular cloning and expression of human prostacyclin synthase.Crossref | GoogleScholarGoogle Scholar |
Moisan, M. P., Minni, A. M., Dominguez, G., Helbling, J. C., Foury, A., Henkous, N., Dorey, R., and Beracochea, D. (2014). Role of corticosteroid binding globulin in the fast actions of glucocorticoids on the brain. Steroids 81, 109–115.
| Role of corticosteroid binding globulin in the fast actions of glucocorticoids on the brain.Crossref | GoogleScholarGoogle Scholar |
Moretti, R. M., Montagnani Marelli, M., Mai, S., and Limonta, P. (2008). Gonadotropin-releasing hormone agonists suppress melanoma cell motility and invasiveness through the inhibition of alpha3 integrin and MMP-2 expression and activity. Int. J. Oncol. 33, 405–413.
Mortazavi, A., Williams, B. A., McCue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621–628.
| Mapping and quantifying mammalian transcriptomes by RNA-Seq.Crossref | GoogleScholarGoogle Scholar |
Pedersen, T., and Peters, H. (1968). Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17, 555–557.
| Proposal for a classification of oocytes and follicles in the mouse ovary.Crossref | GoogleScholarGoogle Scholar |
Perogamvros, I., Ray, D. W., and Trainer, P. J. (2012). Regulation of cortisol bioavailability – effects on hormone measurement and action. Nat. Rev. Endocrinol. 8, 717–727.
| Regulation of cortisol bioavailability – effects on hormone measurement and action.Crossref | GoogleScholarGoogle Scholar |
Rahman, Z., Schwarz, J., Gold, S. J., Zachariou, V., Wein, M. N., Choi, K. H., Kovoor, A., Chen, C. K., DiLeone, R. J., Schwarz, S. C., Selley, D. E., Sim-Selley, L. J., Barrot, M., Luedtke, R. R., Self, D., Neve, R. L., Lester, H. A., Simon, M. I., and Nestler, E. J. (2003). RGS9 modulates dopamine signaling in the basal ganglia. Neuron 38, 941–952.
| RGS9 modulates dopamine signaling in the basal ganglia.Crossref | GoogleScholarGoogle Scholar |
Rahman, A. N. M. A., Abdullah, R. B., and Wankhadijah, W. E. (2008). Estrus synchronization and superovulation in goats: a review. J. Biol. Sci. 8, 1129–1137.
| Estrus synchronization and superovulation in goats: a review.Crossref | GoogleScholarGoogle Scholar |
Remy, B., Baril, G., Vallet, J. C., Dufour, R., Chouvet, C., Saumande, J., Chupin, D., and Beckers, J. F. (1991). Are antibodies responsible for a decreased superovulatory response in goats which have been treated repeatedly with porcine follicle-stimulating hormone? Theriogenology 36, 389–399.
| Are antibodies responsible for a decreased superovulatory response in goats which have been treated repeatedly with porcine follicle-stimulating hormone?Crossref | GoogleScholarGoogle Scholar |
Roy, F., Maurel, M. C., Combes, B., Vaiman, D., Cribiu, E. P., Lantier, I., Pobel, T., Deletang, F., Combarnous, Y., and Guillou, F. (1999). The negative effect of repeated equine chorionic gonadotropin treatment on subsequent fertility in alpine goats is due to a humoral immune response involving the major histocompatibility complex. Biol. Reprod. 60, 805–813.
| The negative effect of repeated equine chorionic gonadotropin treatment on subsequent fertility in alpine goats is due to a humoral immune response involving the major histocompatibility complex.Crossref | GoogleScholarGoogle Scholar |
Skrzypczak, J., Wirstlein, P., Mikolajczyk, M., Ludwikowski, G., and Zak, T. (2007). TGF superfamily and MMP2, MMP9, TIMP1 genes expression in the endometrium of women with impaired reproduction. Folia Histochem. Cytobiol. 45, S143–S148.
Spencer, T. E., and Bazer, F. W. (2002). Biology of progesterone action during pregnancy recognition and maintenance of pregnancy. Front. Biosci. 7, d1879–d1898.
| Biology of progesterone action during pregnancy recognition and maintenance of pregnancy.Crossref | GoogleScholarGoogle Scholar |
Swanson, W. F., Roth, T. L., Graham, K., Horohov, D. W., and Godke, R. A. (1996). Kinetics of the humoral immune response to multiple treatments with exogenous gonadotropins and relation to ovarian responsiveness in domestic cats. Am. J. Vet. Res. 57, 302–307.
Tang, Y. T., Hu, T., Arterburn, M., Boyle, B., Bright, J. M., Emtage, P. C., and Funk, W. D. (2005). PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif. J. Mol. Evol. 61, 372–380.
| PAQR proteins: a novel membrane receptor family defined by an ancient 7-transmembrane pass motif.Crossref | GoogleScholarGoogle Scholar |
Trapnell, C., Roberts, A., Goff, L., Pertea, G., Kim, D., Kelley, D. R., Pimentel, H., Salzberg, S. L., Rinn, J. L., and Pachter, L. (2012). Differential gene and transcript expression analysis of RNA-Seq experiments with TopHat and Cufflinks. Nat. Protoc. 7, 562–578.
| Differential gene and transcript expression analysis of RNA-Seq experiments with TopHat and Cufflinks.Crossref | GoogleScholarGoogle Scholar |
Vallone, D., Picetti, R., and Borrelli, E. (2000). Structure and function of dopamine receptors. Neurosci. Biobehav. Rev. 24, 125–132.
| Structure and function of dopamine receptors.Crossref | GoogleScholarGoogle Scholar |
Vo, N. V., Sowa, G. A., Kang, J. D., Seidel, C., and Studer, R. K. (2010). Prostaglandin E2 and prostaglandin F2alpha differentially modulate matrix metabolism of human nucleus pulposus cells. J. Orthop. Res. 28, 1259–1266.
| Prostaglandin E2 and prostaglandin F2alpha differentially modulate matrix metabolism of human nucleus pulposus cells.Crossref | GoogleScholarGoogle Scholar |
Wood, R. I. (2007). Sex and drugs: comment on “Evidence for involvement of ER beta and RGS9-2 in 17 beta estradiol enhancement of amphetamine-induced place preference behavior” by Silverman and Koenig. Horm. Behav. 52, 143–145.
| Sex and drugs: comment on “Evidence for involvement of ER beta and RGS9-2 in 17 beta estradiol enhancement of amphetamine-induced place preference behavior” by Silverman and Koenig.Crossref | GoogleScholarGoogle Scholar |
Xia, G., Evers, M. R., Kang, H. G., Schachner, M., and Baenziger, J. U. (2000). Molecular cloning and expression of the pituitary glycoprotein hormone N-acetylgalactosamine-4-O-sulfotransferase. J. Biol. Chem. 275, 38402–38409.
| Molecular cloning and expression of the pituitary glycoprotein hormone N-acetylgalactosamine-4-O-sulfotransferase.Crossref | GoogleScholarGoogle Scholar |
Xie, C., Mao, X., Huang, J., Ding, Y., Wu, J., Dong, S., Kong, L., Gao, G., Li, C. Y., and Wei, L. (2011). KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39, W316–322.
Yin, H., Wan, Q., Tian, Y., Zhao, B., and Deng, Y. (2017). Female hormone 17β-estradiol downregulated MMP-2 expression and upregulated A1PI expression in human corneal stromal cells. Cell Biochem. Biophys. 76, 265–271.
| Female hormone 17β-estradiol downregulated MMP-2 expression and upregulated A1PI expression in human corneal stromal cells.Crossref | GoogleScholarGoogle Scholar |
Yokoyama, C., Yabuki, T., Inoue, H., Tone, Y., Hara, S., Hatae, T., Nagata, M., Takahashi, E. I., and Tanabe, T. (1996). Human gene encoding prostacyclin synthase (PTGIS): genomic organization, chromosomal localization, and promoter activity. Genomics 36, 296–304.
| Human gene encoding prostacyclin synthase (PTGIS): genomic organization, chromosomal localization, and promoter activity.Crossref | GoogleScholarGoogle Scholar |
Young, M. D., Wakefield, M. J., Smyth, G. K., and Oshlack, A. (2010). Gene ontology analysis for RNA-Seq: accounting for selection bias. Genome Biol. 11, R14.
| Gene ontology analysis for RNA-Seq: accounting for selection bias.Crossref | GoogleScholarGoogle Scholar |
Zhou, C. X., Elsheikha, H. M., Zhou, D. H., Liu, Q., Zhu, X. Q., and Suo, X. (2016). Dual identification and analysis of differentially expressed transcripts of porcine PK-15 cells and Toxoplasma gondii during in vitro infection. Front. Microbiol. 7, 721.
| Dual identification and analysis of differentially expressed transcripts of porcine PK-15 cells and Toxoplasma gondii during in vitro infection.Crossref | GoogleScholarGoogle Scholar |
