Upregulation of Coagulation Factor V by Glucocorticoid in the Preovulatory Follicles of Zebrafish

Overview

Journal J Steroid Biochem Mol Biol

Specialties Biochemistry
Molecular Biology

Date 2024 Apr 17

PMID 38631601

Authors

Jing Huang

Chao Sun

Zhuo Huang

Yong Zhu

Shi Xi Chen

Affiliations

Soon will be listed here.

Abstract

Increased cortisol levels in the preovulatory follicular fluid suggests a role of glucocorticoid in human ovulation. However, the mechanisms through which cortisol regulates the ovulatory process remain poorly understood. In this study, we examined the upregulation of f5 mRNA by glucocorticoid and its receptor (Gr) in the preovulatory follicles of zebrafish. Our findings demonstrate a significant increase in 11β-hydroxysteroid dehydrogenase type 2 (hsd11b2), a cortisol response gene, in preovulatory follicles. Additionally, hydrocortisone exerts a dose- and time-dependent upregulation of f5 mRNA in these follicles. Importantly, this stimulatory effect is Gr-dependent, as it was completely abolished in gr mutants. Furthermore, site-directed mutagenesis identified a glucocorticoid response element (GRE) in the promoter of zebrafish f5. Interestingly, successive incubation of hydrocortisone and the native ovulation-inducing steroid, progestin (17α,20β-dihydroxy-4-pregnen-3-one, DHP), further enhanced f5 expression in preovulatory follicles. Overall, our results indicate that the dramatic increase of f5 expression in preovulatory follicles is partially attributable to the regulation of glucocorticoid and Gr.

References

Tsai M, OMalley B . Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu Rev Biochem. 1994; 63:451-86. DOI: 10.1146/annurev.bi.63.070194.002315. View

Zhu Y, Liu D, Shaner Z, Chen S, Hong W, Stellwag E . Nuclear progestin receptor (pgr) knockouts in zebrafish demonstrate role for pgr in ovulation but not in rapid non-genomic steroid mediated meiosis resumption. Front Endocrinol (Lausanne). 2015; 6:37. PMC: 4365747. DOI: 10.3389/fendo.2015.00037. View

Thornton J . Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions. Proc Natl Acad Sci U S A. 2001; 98(10):5671-6. PMC: 33271. DOI: 10.1073/pnas.091553298. View

Tsilchorozidou T, Honour J, Conway G . Altered cortisol metabolism in polycystic ovary syndrome: insulin enhances 5alpha-reduction but not the elevated adrenal steroid production rates. J Clin Endocrinol Metab. 2003; 88(12):5907-13. DOI: 10.1210/jc.2003-030240. View

Johannsen M, Poulsen L, Mamsen L, Grondahl M, Englund A, Lauritsen N . The intrafollicular concentrations of biologically active cortisol in women rise abruptly shortly before ovulation and follicular rupture. Hum Reprod. 2024; 39(3):578-585. DOI: 10.1093/humrep/deae003. View

van der Pas R, de Bruin C, Leebeek F, De Maat M, Rijken D, Pereira A . The hypercoagulable state in Cushing's disease is associated with increased levels of procoagulant factors and impaired fibrinolysis, but is not reversible after short-term biochemical remission induced by medical therapy. J Clin Endocrinol Metab. 2012; 97(4):1303-10. DOI: 10.1210/jc.2011-2753. View

Huang J, Sun C, Teng Liu D, Zhao N, Shavit J, Zhu Y . Nuclear Progestin Receptor-mediated Linkage of Blood Coagulation and Ovulation. Endocrinology. 2022; 163(7). PMC: 9653010. DOI: 10.1210/endocr/bqac057. View

West D, Pan D, Tonsing-Carter E, Hernandez K, Pierce C, Styke S . GR and ER Coactivation Alters the Expression of Differentiation Genes and Associates with Improved ER+ Breast Cancer Outcome. Mol Cancer Res. 2016; 14(8):707-19. PMC: 5008962. DOI: 10.1158/1541-7786.MCR-15-0433. View

Lado-Abeal J, Rodriguez-Arnao J, Perry L, Grossman A, Besser G, Trainer P . Menstrual abnormalities in women with Cushing's disease are correlated with hypercortisolemia rather than raised circulating androgen levels. J Clin Endocrinol Metab. 1998; 83(9):3083-8. DOI: 10.1210/jcem.83.9.5084. View

10.

Duffy D, Ko C, Jo M, Brannstrom M, Curry T . Ovulation: Parallels With Inflammatory Processes. Endocr Rev. 2018; 40(2):369-416. PMC: 6405411. DOI: 10.1210/er.2018-00075. View

11.

Lee H, Schwab T, Sigafoos A, Gauerke J, Krug 2nd R, Serres M . Novel zebrafish behavioral assay to identify modifiers of the rapid, nongenomic stress response. Genes Brain Behav. 2018; 18(2):e12549. PMC: 6446827. DOI: 10.1111/gbb.12549. View

12.

Xiao H, Xu Z, Zhu X, Wang J, Zheng Q, Zhang Q . Cortisol safeguards oogenesis by promoting follicular cell survival. Sci China Life Sci. 2022; 65(8):1563-1577. DOI: 10.1007/s11427-021-2051-0. View

13.

van der Pas R, Leebeek F, Hofland L, de Herder W, Feelders R . Hypercoagulability in Cushing's syndrome: prevalence, pathogenesis and treatment. Clin Endocrinol (Oxf). 2012; 78(4):481-8. DOI: 10.1111/cen.12094. View

14.

Strahle U, Klock G, Schutz G . A DNA sequence of 15 base pairs is sufficient to mediate both glucocorticoid and progesterone induction of gene expression. Proc Natl Acad Sci U S A. 1987; 84(22):7871-5. PMC: 299431. DOI: 10.1073/pnas.84.22.7871. View

15.

Caimari F, Valassi E, Garbayo P, Steffensen C, Santos A, Corcoy R . Cushing's syndrome and pregnancy outcomes: a systematic review of published cases. Endocrine. 2016; 55(2):555-563. DOI: 10.1007/s12020-016-1117-0. View

16.

Barton B . Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol. 2011; 42(3):517-25. DOI: 10.1093/icb/42.3.517. View

17.

Dhiman V, Bolt M, White K . Nuclear receptors in cancer - uncovering new and evolving roles through genomic analysis. Nat Rev Genet. 2017; 19(3):160-174. DOI: 10.1038/nrg.2017.102. View

18.

Jeon H, Choi Y, Brannstrom M, Akin J, Curry T, Jo M . Cortisol/glucocorticoid receptor: a critical mediator of the ovulatory process and luteinization in human periovulatory follicles. Hum Reprod. 2023; 38(4):671-685. PMC: 10068287. DOI: 10.1093/humrep/dead017. View

19.

Wan Y, Nordeen S . Overlapping but distinct gene regulation profiles by glucocorticoids and progestins in human breast cancer cells. Mol Endocrinol. 2002; 16(6):1204-14. DOI: 10.1210/mend.16.6.0848. View

20.

Kastelan D, Dusek T, Kraljevic I, Polasek O, Giljevic Z, Solak M . Hypercoagulability in Cushing's syndrome: the role of specific haemostatic and fibrinolytic markers. Endocrine. 2009; 36(1):70-4. DOI: 10.1007/s12020-009-9186-y. View