Sel’skokhozyaistvennaya Biologiya [Agricultural Biology], 2018, Vol. 53, № 6, p. 1202-1211.
(how to cite this article)

doi: 10.15389/agrobiology.2018.6.1202eng

UDC 636.2:591.39

Acknowledgements:
Supported financially by Russain Science Foundation (project 16-16-10069)

 

RESISTANCE OF BOVINE OOCYTES TO AGE-RELATED
CHANGES AFTER EXPOSURE TO LUTEOTROPIC FACTORS DURING
THE SECOND PHASE OF CULTURE TILL THE METAPHASE II STAGE

I.Yu. Lebedeva, G.N. Singina, E.N. Shedova,
A.V. Lopukhov, O.S. Mityashova

Ernst Federal Science Center for Animal Husbandry,60, pos. Dubrovitsy, Podolsk District, Moscow Province, 142132 Russia, e-mail irledv@mail.ru (✉ corresponding author), g_singina@mail.ru, shedvek@yandex.ru, vubi_myaso@mail.ru, mityashova_o@mail.ru

ORCID:
Lebedeva I.Yu. orcid.org/0000-0002-7815-7900
Singina G.N. orcid.org/0000-0003-0198-9757
Shedova E.N. orcid.org/0000-0002-9642-2384
Lopukhov A.V. orcid.org/0000-0002-1284-1486
Mityashova O.S. orcid.org/0000-0002-0401-5088
The authors declare no conflict of interests

Received September 17, 2018

 

After the completion of the first division of meiosis in oocytes of various mammalian species, including cattle, the aging processes are acutely activated, which adversely affects the quality of mature ova and their competence to embryonic development after fertilization. Endogenous progesterone (P4) is known to play an important role in maintaining the viability of bovine oocytes, with its production by surrounding cumulus cells increasing significantly in the course of the final maturation period of female gametes from metaphase I to metaphase II (MII). However, effects of P4 and its two main stimulators, prolactin (PRL) and luteinizing hormone (LH), during maturation of oocytes on their resistance to age-related transformations are still poorly studied. We performed for the first time a comparative investigation of abnormal changes of MII chromosomes and apoptotic degeneration of oocytes, ripened by exposure to P4, PRL, and LH in the absence and in the presence of granulosa cells, during the subsequent prolonged culture of the ova. The aim of the present work was to study effects of luteotropic factors, P4, PRL and LH, during the second phase of in vitro maturation of bovine oocytes on the resistance of these latter to age-related changes. Oocytes surrounded by cumulus matured for the first 12 hours in the medium TCM 199 containing 10 % fetal bovine serum (FBS), 10 μg/ml follicle-stimulating hormone (FSH) and 10 μg/ml LH. Then the oocytes were transferred to a new medium, i.e. TCM 199 containing 10 % FBS (control) or the same medium supplemented with 50 ng/ml P4, 50 ng/ml PRL or 5 μg/ml LH, and cultured for the next 12 h in the presence and in the absence of granulosa cells. After 24 h of maturation in the two-phase system, the oocytes were transferred to an aging medium (TCM 199 containing 10 % FBS) and further cultured for 24 h. In media collected after oocyte aging, the P4 content was determined by enzyme immunoassay. The state of the nuclear material in oocytes was assessed using cytogenetic analysis, the presence of apoptosis in oocytes was determined by the TUNEL method. The rate of oocytes being at the MII stage of meiosis after 24 h of aging was similar in all groups and amounted 78.2-88.4 %. In the absence of granulosa cells, the effect of P4 on oocytes during the second phase of maturation led to a subsequent decrease in the frequency of destructive changes in MII chromosomes, from 67.1±2.0 (control) to 51.2±2.9 % (p < 0.01), whereas the introduction of these cells into the culture system eliminated the positive effect of the hormone (p < 0.001). On the contrary, a similar effect of PRL, reducing the rate of aging ova with the abnormal morphology of MII chromosomes, from 67.7±1.6 (control) to 46.5±5.0 % (p < 0.001), we detected only in the presence of granulosa cells. In addition, after ripening in the system not containing granulosa cells, the frequency of the apoptotic degeneration is lowest in the group of aging oocytes exposed to P4 (17.6 % vs. 23.5-25.2 %, p < 0.05). In the presence of granulosa cells, this anti-apoptotic effect of P4 is less pronounced. Meanwhile, there is no difference between the compared groups in the content of P4 in the aging medium. The results of the study suggest that effects of P4 and PRL on bovine oocytes during the second phase of maturation may increase their resistance to subsequent age-related changes associated with a decline in the quality. Thus, these hormones can be used to optimize the maturation conditions of cattle oocytes in the two-phase system.

Keywords: cattle, oocyte, two-phase system of in vitro maturation, age-related changes of oocytes, progesterone, prolactin, luteinizing hormone, granulosa cells.

 

Full article (Rus)

Full article (Eng)

 

REFERENCES

  1. Moore S.G., Hasler J.F. A 100-year review: reproductive technologies in dairy science. J. Dairy Sci., 2017, 100(12): 10314-10331 CrossRef
  2. Conti M., Franciosi F. Acquisition of oocyte competence to develop as an embryo: integrated nuclear and cytoplasmic events. Hum. Reprod. Update, 2018, 24(3): 245-266 CrossRef
  3. Sutton M.L., Gilchrist R.B., Thompson J.G. Effects of in-vivo and in-vitro environments on the metabolism of the cumulus-oocyte complex and its influence on oocyte developmental capacity. Hum. Reprod. Update, 2003, 9(1): 35-48 CrossRef
  4. Hansen P.J., Block J., Loureiro B., Bonilla L., Hendricks K.E. Effects of gamete source and culture conditions on the competence of in vitro-produced embryos for post-transfer survival in cattle. Reprod. Fert. Develop., 2010, 22(1): 59-66 CrossRef
  5. Farin P.W., Piedrahita J.A., Farin C.E. Errors in development of fetuses and placentas from in vitro-produced bovine embryos. Theriogenology, 2006, 65(1): 178-191 CrossRef
  6. Wrenzycki C., Stinshoff H. Maturation environment and impact on subsequent developmental competence of bovine oocytes. Reprod. Domest. Anim., 2013, 48(Suppl. 1): 38-43 CrossRef
  7. Thompson J.G., Lane M., Gilchrist R.B. Metabolism of the bovine cumulus-oocyte complex and influence on subsequent developmental competence. Soc. Reprod. Fertil. Suppl., 2007, 64: 179-190.
  8. Sudiman J., Sutton-McDowall M.L., Ritter L.J., White M.A., Mottershead D.G., Thompson J.G., Gilchrist R.B. Bone morphogenetic protein 15 in the pro-mature complex form enhances bovine oocyte developmental competence. PLoS ONE, 2014, 9(7): e103563 CrossRef
  9. Takahashi T., Igarashi H., Amita M., Hara S., Kurachi H. Cellular and molecular mechanisms of various types of oocyte aging. Reproductive Medicine and Biology, 2011, 10(4): 239-249 CrossRef
  10. Lebedeva I.Yu., Singina G.N., Lopukhov A.V., Zinovieva N.A. Dynamics of morphofunctional changes in aging bovine ova during prolonged culture in vitro. Cell and Tissue Biology, 2014, 8(3): 258-266 CrossRef
  11. Kong Q.Q., Wang J., Xiao B., Lin F.H., Zhu J., Sun G.Y., Luo M.J., Tan J.H. Cumulus cell-released tumor necrosis factor (TNF)-a promotes post-ovulatory aging of mouse oocytes. Aging (Albany NY), 2018, 10(7): 1745-1757 CrossRef
  12. Liang X., Ma J., Schatten H., Sun Q. Epigenetic changes associated with oocyte aging. Science China Life Sciences, 2012, 55(8): 670-676 CrossRef
  13. Tarín J.J., Pérez-Albalá S., Pérez-Hoyos S., Cano A. Postovulatory aging of oocytes decreases reproductive fitness and longevity of offspring. Biol. Reprod., 2002, 66(2): 495-499 CrossRef
  14. Takahashi T., Igarashi H., Amita M., Hara S., Matsuo K., Kurachi H. Molecular mechanism of poor embryo development in postovulatory aged oocytes: mini review. J. Obstet. Gynaecol. Re., 2013, 39(10): 1431-1439 CrossRef
  15. Lebedeva I.Y., Singina G.N., Shedova E.N., Taradajnic T.E., Zinovieva N.A. Progesterone is involved in anti-aging effects of prolactin on bovine cumulus-enclosed oocytes matured in vitro. Anim. Reprod., 2016, 13(3): 652.
  16. Bachelot A., Carré N., Mialon O., Matelot M., Servel N., Monget P., Ahtiainen P., Huhtaniemi I., Binart N. The permissive role of prolactin as a regulator of luteinizing hormone action in the female mouse ovary and extragonadal tumorigenesis. Am. J. Physiol.-Endoc. M., 2013, 305(7): E845-E852 CrossRef
  17. Fair T., Lonergan P. The role of progesterone in oocyte acquisition of developmental competence. Reprod. Domest. Anim., 2012, 47(Suppl. 4): 142-147 CrossRef
  18. Tosca L., Uzbekova S., Chabrolle C., Dupont J. Possible role of 5´AMP-activated protein kinase in the metformin-mediated arrest of bovine oocytes at the germinal vesicle stage during in vitro maturation. Biol. Reprod., 2007, 77(3): 452-465 CrossRef
  19. Nuttinck F., Marquant-Le Guienne B., Clément L., Reinaud P., Charpigny G., Grimard B. Expression of genes involved in prostaglandin E2 and progesterone production in bovine cumulus-oocyte complexes during in vitro maturation and fertilization. Reproduction, 2008, 135(5): 593-603 CrossRef
  20. Singina G.N., Lebedeva I.Yu., Shedova E.N., Taradajnic T.E., Mityashova O.S., Tsyndrina E.V., Danch S.S. Bovine oocyte ability to embryonic development when maturing in different two-phase culture systems. Agricultural Biology, 2017, 52(4): 776-784 CrossRef
  21. Homa S.T. Effects of cyclic AMP on the spontaneous meiotic maturation of cumulus-free bovine oocytes cultured in chemically defined medium. J. Exp. Zool., 1988, 248(2): 222-231 CrossRef
  22. Lebedeva I.Yu., Singina G.N., Lopukhov A.V. Tsitologiya, 2013, 55(9): 643-644 (in Russ.).
  23. Aparicio I.M., Garcia-Herreros M., O'Shea L.C., Hensey C., Lonergan P., Fair T. Expression, regulation, and function of progesterone receptors in bovine cumulus oocyte complexes during in vitro maturation. Biol. Reprod., 2011, 84(5): 910-921 CrossRef
  24. Sirard M.A. Somatic environment and germinal differentiation in antral follicle: the effect of FSH withdrawal and basal LH on oocyte competence acquisition in cattle. Theriogenology, 2016, 86(1): 54-61 CrossRef
  25. Xiao X., Zi X.D., Niu H.R., Xiong X.R., Zhong J.C., Li J., Wang L., Wang Y. Effect of addition of FSH, LH and proteasome inhibitor MG132 to in vitro maturation medium on the developmental competence of yak (Bos grunniens) oocytes. Reprod. Biol. Endocrinol., 2014, 12: 30 CrossRef
  26. Kim Y., Kim E.Y., Seo Y.M., Yoon T.K., Lee W.S., Lee K.A. Function of the pentose phosphate pathway and its key enzyme, transketolase, in the regulation of the meiotic cell cycle in oocytes. Clin. Exp. Reprod. Med., 2012, 39(2): 58-67 CrossRef
  27. Zhang Z., Chen C., Ma L., Yu Q., Li S., Abbasi B., Yang J., Rui R., Ju S. Plk1 is essential for proper chromosome segregation during meiosis I/meiosis II transition in pig oocytes. Reprod. Biol. Endocrinol., 2017, 15(1): 69 CrossRef

back