The blood vessels development, morphogenesis and blood circulation are three ontologic groups highly up-regulated in porcine oocytes before in vitro maturation

Open access

Abstract

The mammalian oocytes undergo significant biochemical and structural modifications during maturation both in vitro and in vivo. These changes involve chromatin reorganization and modification within metabolic status of cytoplasmic organelles. After oocytes’ successful maturation the substantially increased storage of RNA was observed. Moreover, the early embryo interaction with maternal endometrial tissue after fertilization is up to now considered as the main marker of proper embryo implantation and early growth. In this study, we first investigated the expression profile of genes involved in blood vessel formation and blood circulation in porcine oocytes before and after in vitro maturation.

The cumulus-oocyte complexes were collected from pubertal Landrace gilts and classified as before in vitro maturation (in Vivo) or after in vitro maturation (in Vitro). The RNA was isolated from these two experimental groups and analyzed using Affymetrix microarrays.

We found an increased expression of genes involved in ontological groups such as “blood circulation” (TPM1, ECE1, ACTA2, EPHX2, EDNRA, NPR2, MYOF, TACR3, VEGFA, GUCY1B3), “blood vessel development” (ANGPTL4, CYR61, SEMA5A, ID1, RHOB, RTN4, IHH, ANGPT2, EDNRA, TGFBR3, MYO1E, MMP14), and “blood vessels morphogenesis” (ANGPT2, as well as other common transcripts) in in Vivo group as compared to decreased expression of these genes in in Vitro group of oocytes.

It has been suggested that investigated genes undergo significant expression before in vitro maturation, when enhanced storage of large amount of RNA takes place. Creating templates for synthesis of proteins is required for formation of fully mature gametes and early embryo growth. Therefore we hypothesized that the processes of vascularization and/or angiogenesis reach a high activity in immature oocytes and are distinct from achievement of maturational stage by oocytes in pigs.

1. Budna J, Celichowski P, Karimi P, Kranc W, Bryja A, Ciesiółka S, Rybska M, Borys S, Jeseta M, Bukowska D, Antosik P, Brüssow KP, Bruska M, Nowicki M, Zabel M, Kempisty B. Does Porcine oocytes maturation in vitro is regulated by genes involved in transforming growth factor beta receptor signaling pathway? Adv Cell Biol. 2017;5(1):1-14.

2. Kranc W, Budna J, Chachuła A, Borys S, Bryja A, Rybska M, Ciesiółka S, Sumelka E, Jeseta M, Brüssow KP, Bukowska D, Antosik P, Bruska M, Nowicki M, Zabel M, Kempisty B. “Cell Migration” Is the Ontology Group Differentially Expressed in Porcine Oocytes Before and After In Vitro Maturation: A Microarray Approach. DNA Cell Biol. 2017;36(4):273-282.

3. Kranc W, Celichowski P, Budna J, Khozmi R, Bryja A, Ciesiółka S, Rybska M, Borys S, Jeseta M, Bukowska D, Antosik P, Brüssow KP, Bruska M, Nowicki M, Zabel M, Kempisty B. Positive regulation of macromolecule metabolic process belongs to the main mechanisms crucial for porcine oocytes maturation. Adv Cell Biol. 2017;5(1):15-32.

4. Ciesiółka S, Bryja A, Budna J, Kranc W, Chachuła A, Bukowska D, Piotrowska H, Porowski L, Antosik P, Bruska M, Brüssow KP, Nowicki M, Zabel M, Kempisty B. Epithelialization and stromalization of porcine follicular granulosa cells during real-time proliferation – a primary cell culture approach. J Biol Regul Homeost Agents. 2016;30(3):693-702.

5. Ciesiółka S, Budna J, Jopek K, Bryja A, Kranc W, Borys S, Jeseta M, Chachuła A, Ziółkowska A, Antosik P, Bukowska D, Brüssow KP, Bruska M, Nowicki M, Zabel M, Kempisty B. Time- and Dose-Dependent Effects of 17 Beta-Estradiol on Short-Term, Real-Time Proliferation and Gene Expression in Porcine Granulosa Cells. Biomed Res Int. 2017;2017:9738640.

6. Hazzard TM, Xu F, Stouffer RL. Injection of soluble vascular endothelial growth factor receptor 1 into the preovulatory follicle disrupts ovulation and subsequent luteal function in rhesus monkeys. Biol Reprod. 2002;67:1305-1312.

7. Trau HA, Brannstrom M, Curry TE, JR, Duffy DM. Prostaglandin E2 and vascular endothelial growth factor A mediate angiogenesis of human ovarian follicular endothelial cells. Hum Reprod. 2016;31:436-444.

8. Li S-H, Hwu Y-M, Lu C-H, Chang H-H, Hsieh C-E, Lee RK-K. VEGF and FGF2 Improve Revascularization, Survival, and Oocyte Quality of Cryopreserved, Subcutaneously-Transplanted Mouse Ovarian Tissues. Int J Mol Sci. 2016;17(8):1-13.

9. Anchordoquy JM, Anchordoquy JP, Testa JA, Sirini MA, Furnus CC. Influence of vascular endothelial growth factor and Cysteamine on in vitro bovine oocyte maturation and subsequent embryo development. Cell Biol Int. 2015;39:1090-1098.

10. Masaki T. Endothelins: Homeostatic and Compensatory Actions in the Circulatory and Endocrine Systems. Endocrine Reviews. 1993;14(3):256-268.

11. Ko C, Gieske MC, Al-Alem L, Hahn Y, Su W, Gong MC, Iglarz M, Koo Y. Endothelin-2 in ovarian follicle rupture. Endocrinology. 2006;147(4):1770-9.

12. Bridges PJ, Jo M, Al Alem L, Na G, Su W, Gong MC, Jeoung M, Ko C. Production and binding of endothelin-2 (EDN2) in the rat ovary: endothelin receptor subtype A (EDNRA)-mediated contraction. Reproduction, fertility, and development. 2010;22(5):780-7.

13. Thomas M, Augustin HG. The role of the Angiopoietins in vascular morphogenesis. Angiogenesis. 2009;12(2):125-37.

14. Holash J, Maisonpierre PC, Compton D, Boland P, Alexander CR, Zagzag D, Yancopoulos GD, Wiegand SJ. Vessel cooption, regression, and growth in tumors mediated by angiopoietins and VEGF. Science. 1999;284(5422):1994-8.

15. Hu B, Cheng SY. Angiopoietin-2: development of inhibitors for cancer therapy. Current oncology reports. 2009;11(2):111-6.

16. Hata K, Udagawa J, Fujiwaki R, Nakayama K, Otani H, Miyazaki K. Expression of angiopoietin-1, angiopoietin-2, and Tie2 genes in normal ovary with corpus luteum and in ovarian cancer. Oncology. 2002;62(4):340-8.

17. Santulli G. Angiopoietin-like proteins: a comprehensive look. Frontiers in endocrinology. 2014;5:4

18. Zhu P, Goh YY, Chin HF, Kersten S, Tan NS. Angiopoietin-like 4: a decade of research. Biosci Rep. 2012;32(3):211-9.

19. Mandard S, Zandbergen F, van Straten E, Wahli W, Kuipers F, Müller M, Kersten S. The fasting-induced adipose factor/angiopoietin-like protein 4 is physically associated with lipoproteins and governs plasma lipid levels and adiposity. J Biol Chem. 2006;281:934-944.

20. Liu Z, Liu C, Hao C, Xue Q, Huang X, Zhang N, Bao H, Qu Q. Aberrant expression of angiopoietin-like proteins 1 and 2 in cumulus cells is potentially associated with impaired oocyte developmental competence in polycystic ovary syndrome. Gynecol Endocrinol. 2016;32(7):557-61.

21. Sato H, Takino T, Okada Y, Cao J, Shinagawa A, Yamamoto E, Seiki M. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature. 1994;370(6484):61-5.

22. Perbal B. NOV (nephroblastoma overexpressed) and the CCN family of genes: structural and functional issues. Mol Pathol. 2001;54(2):57-79.

23. Azoury J, Lee KW, Georget V, Hikal P, Verlhac MH. Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development. 2011;138:2903-8.

24. Chaigne A, Campillo C, Gov NS, Voituriez R, Sykes C, Verlhac MH, Terret ME. A narrow window of cortical tension guides asymmetric spindle positioning in the mouse oocyte. Nat Commun. 2015;6:6027.

25. Valdenaire O, Lepailleur-Enouf D, Egidy G, Thouard A, Barret A, et al. A fourth isoform of endothelin-converting enzyme (ECE-1) is generated from an additional promoter molecular cloning and characterization. Eur J Biochem. 1999; 264: 341-349.

Medical Journal of Cell Biology

The Journal of Foundation for Cell Biology and Molecular Biology

Journal Information

Cited By

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 213 201 13
PDF Downloads 94 90 6