Expression and regulation of stromal cell-derived factor-1 (SDF1) and chemokine CXC motif receptor 4 (CXCR4) in equine and bovine preovulatory follicles.
Abstract: The interaction between stromal cell-derived factor-1 (SDF1) and chemokine CXC motif receptor 4 (CXCR4) has been implicated in leukocyte attraction, tissue remodeling and angiogenesis. The objective of the present study was to characterize the expression and regulation of SDF1 and CXCR4 in equine follicles during the ovulatory process. Equine preovulatory follicles were isolated during estrus 0-39h after hCG treatment. Follicle wall preparations (theca interna with attached granulosa cells) and isolated preparations of granulosa cells and theca interna were obtained, and total RNA extracts were analyzed by RT-PCR/Southern blot. Results showed that levels of CXCR4 transcripts were induced by hCG in follicles at 36 h post-hCG (P<0.05 vs 0 h), with the induction observed in both granulosa and theca cells. Immunoblotting and immunohistochemical analyses confirmed an increase in CXCR4 protein in follicles after hCG treatment. In contrast, levels of SDF1 transcripts were very low in granulosa cells but high in theca interna cells throughout most of the ovulatory period. Studies in vivo performed with bovine preovulatory follicles collected 0-24h post-hCG revealed a marked and significant up-regulation of CXCR4 transcripts after hCG (P<0.05), as observed in equine follicles. A similar pattern of CXCR4 mRNA up-regulation was observed in cultures of bovine granulosa cells treated with forskolin (P<0.05). This forskolin-dependent induction of CXCR4 mRNA was suppressed by co-treatment with inhibitors of PKA, ERK1/2 and EGFR, and by the progesterone receptor antagonist RU486 (P<0.05), underscoring the contribution of multiple signaling pathways. In complementary studies, treatment of bovine granulosa cells with EGF or the hypoxia mimetic cobalt chloride significantly increased CXCR4 transcript levels, whereas co-treatment with forskolin and a CXCR4 antagonist repressed the expression of several ovulation-related genes. Collectively, this study describes for the first time the gonadotropin-dependent up-regulation of CXCR4 transcript in ovarian follicles of large monoovulatory species, provides some insights into the regulation of CXCR4 gene expression in granulosa cells, and identifies a potential link between follicular SDF1/CXCR4 activation and the regulation of ovulation-related genes.
Copyright © 2014 Elsevier Ireland Ltd. All rights reserved.
Publication Date: 2014-04-28 PubMed ID: 24784705DOI: 10.1016/j.mce.2014.04.009Google Scholar: Lookup
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- Journal Article
- Research Support
- Non-U.S. Gov't
Summary
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The research focuses on studying the expression and regulation of stromal cell-derived factor-1 (SDF1) and chemokine CXC motif receptor 4 (CXCR4) in equine and bovine preovulatory follicles. The study suggests a link between follicular SDF1/CXCR4 activation and the regulation of ovulation-related genes, providing insight into the role of gonadotropin-dependent up-regulation of CXCR4 in ovarian follicles of large mono-ovulatory species.
Background and Objective of the Study
- The study aimed to understand the expression and regulation of two biological compounds, stromal cell-derived factor-1 (SDF1) and chemokine CXC motif receptor 4 (CXCR4), in the ovarian follicles of horses and cows during the process of ovulation.
- The interaction of SDF1 and CXCR4 has been observed to play a significant role in various biological processes such as attraction of leukocytes, remodeling of tissues, and the formation of new blood vessels (angiogenesis).
- The researchers set out with the purpose to elucidate the role these compounds might play in the ovulatory process.
Methodology and Procedures
- Equine preovulatory follicles were isolated at different time intervals (0-39 hours) after the administration of human Chorionic Gonadotropin (hCG).
- Both the follicle wall preparations and certain isolated cell types were obtained for study.
- Levels of CXCR4 and SDF1 were then analyzed using techniques such as RT-PCR/Southern blot.
- Immunoblotting and immunohistochemical analyses were carried out to confirm the levels of CXCR4 protein within the follicles post-hCG treatment.
- In vivo studies were also performed with bovine follicles that were collected at different time intervals post-hCG administration.
Research Findings and Conclusion
- Results indicated an increased level of CXCR4 after hCG treatment, as identified from both equine and bovine follicles.
- While the levels of SDF1 were notably low in certain cells (granulosa cells), they were found high in interna cells throughout most of the ovulatory period.
- Treatment of bovine granulosa cells with particular agents led to a significant increase in CXCR4 transcript levels.
- The study successfully highlighted a potential link between SDF1/CXCR4 activation within the follicles and the regulation of genes related to ovulation.
- This research marks the first occurrence of unveiling the gonadotropin-dependent up-regulation of CXCR4 transcript in ovarian follicles, mainly in larger mono-ovulatory species.
Cite This Article
APA
Sayasith K, Sirois J.
(2014).
Expression and regulation of stromal cell-derived factor-1 (SDF1) and chemokine CXC motif receptor 4 (CXCR4) in equine and bovine preovulatory follicles.
Mol Cell Endocrinol, 391(1-2), 10-21.
https://doi.org/10.1016/j.mce.2014.04.009 Publication
Researcher Affiliations
- Centre de Recherche en Reproduction Animale, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada; Département de Biomédecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada; Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada. Electronic address: k.sayasith@umontreal.ca.
- Centre de Recherche en Reproduction Animale, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada; Département de Biomédecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada; Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada.
MeSH Terms
- Amino Acid Sequence
- Animals
- Cattle
- Cells, Cultured
- Chemokine CXCL12 / genetics
- Chemokine CXCL12 / metabolism
- Chorionic Gonadotropin / administration & dosage
- Cobalt / pharmacology
- Colforsin / pharmacology
- Epidermal Growth Factor / pharmacology
- Estrus / physiology
- Female
- Gene Expression Regulation
- Granulosa Cells / cytology
- Granulosa Cells / drug effects
- Granulosa Cells / metabolism
- Horses
- Humans
- Mifepristone / pharmacology
- Molecular Sequence Data
- Ovulation / physiology
- Protein Kinase Inhibitors / pharmacology
- RNA, Messenger / agonists
- RNA, Messenger / antagonists & inhibitors
- RNA, Messenger / genetics
- RNA, Messenger / metabolism
- Receptors, CXCR4 / agonists
- Receptors, CXCR4 / antagonists & inhibitors
- Receptors, CXCR4 / genetics
- Receptors, CXCR4 / metabolism
- Signal Transduction
- Theca Cells / cytology
- Theca Cells / drug effects
- Theca Cells / metabolism
Citations
This article has been cited 10 times.- McIntosh SZ, Quinn KE, Ashley RL. CXCL12 May Drive Inflammatory Potential in the Ovine Corpus Luteum During Implantation. Reprod Sci 2022 Jan;29(1):122-132.
- Martinez CA, Alvarez-Rodriguez M, Casado-Bedmar M, Rodriguez-Martinez H. In Vitro Maturation of Cumulus-Oocyte Complexes and In Vitro Sperm Capacitation Significantly Increase the Expression and Enhance the Location of the CXCL12 and CXCR4 Anchoring Attractant Complex in Pigs. Animals (Basel) 2021 Jan 11;11(1).
- Ruszkowska M, Sadowska A, Nynca A, Orlowska K, Swigonska S, Molcan T, Paukszto L, Jastrzebski JP, Ciereszko RE. The effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on the transcriptome of aryl hydrocarbon receptor (AhR) knock-down porcine granulosa cells. PeerJ 2020;8:e8371.
- Duffy DM, Ko C, Jo M, Brannstrom M, Curry TE. Ovulation: Parallels With Inflammatory Processes. Endocr Rev 2019 Apr 1;40(2):369-416.
- Schuermann Y, Rovani MT, Gasperin B, Ferreira R, Ferst J, Madogwe E, Gonçalves PB, Bordignon V, Duggavathi R. ERK1/2-dependent gene expression in the bovine ovulating follicle. Sci Rep 2018 Nov 1;8(1):16170.
- Rojo JL, Linari M, Young KA, Peluffo MC. Stromal-derived factor 1 directly promotes genes expressed within the ovulatory cascade in feline cumulus oocyte complexes. J Assist Reprod Genet 2018 May;35(5):785-792.
- Sanchez NS, Quinn KE, Ashley AK, Ashley RL. In the ovine pituitary, CXCR4 is localized in gonadotropes and somatotropes and increases with elevated serum progesterone. Domest Anim Endocrinol 2018 Jan;62:88-97.
- Choi Y, Park JY, Wilson K, Rosewell KL, Brännström M, Akin JW, Curry TE Jr, Jo M. The expression of CXCR4 is induced by the luteinizing hormone surge and mediated by progesterone receptors in human preovulatory granulosa cells. Biol Reprod 2017 Jun 1;96(6):1256-1266.
- Guo Y, Xue L, Tang W, Xiong J, Chen D, Dai Y, Wu C, Wei S, Dai J, Wu M, Wang S. Ovarian microenvironment: challenges and opportunities in protecting against chemotherapy-associated ovarian damage. Hum Reprod Update 2024 Oct 1;30(5):614-647.
- Forutan M, Engle BN, Chamberlain AJ, Ross EM, Nguyen LT, D'Occhio MJ, Snr AC, Kho EA, Fordyce G, Speight S, Goddard ME, Hayes BJ. Genome-wide association and expression quantitative trait loci in cattle reveals common genes regulating mammalian fertility. Commun Biol 2024 Jun 12;7(1):724.
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