Comparison of in vivo and in vitro preimplantation embryo development in OXYS and WAG rats

OXYS rats are the model of precocious senescence. Numerous studies addressed physiology and behavior in rats of this strain during a postnatal period of their life, however, preimplantation development in OXYS rats has not yet been investigated. This study is addressing preimplantation embryonic development in OXYS rats both in vivo and in vitro. Rats of the WAG strain were used as controls. For studying the in vivo development, the embryos were collected from OXYS and WAG rats on day 5 post coitum, the stages of embryo development were estimated, the percentage of embryos at blastocyst stage and the cell numbers in these blastocysts were counted. In a special experiment, for studying in vitro development, the embryos were collected from both rat strains on day 4 post coitum and were cultured in vitro in P1 medium for 48 hours with or without supplementation with IGF-1 (200 ng/mL). Thereafter the percentage of embryos at blastocyst stage and the cell numbers in these blastocysts were counted in the same manner as for the in vivo experiment. This study reports that in vivo derived blastocysts of OXYS rats contain fewer cells on day 5 of their development than in vivo derived blastocysts of WAG rats. In vitro culture of the early preimplantation embryos in P1 medium mitigated the difference in the rate of embryo development between these two strains, the addition of IGF-1 into culture medium exerts neither negative nor positive effect on the rate of in vitro embryo development in rats of both strains.

OXYS rats, WAG rats, in vivo preimplantation development, in vitro culture, embryos, IGF-1

1. Berryman D.E., Christiansen J.S., Johannsson G., Thorner M.O., Kop-chick J.J. Role of the GH/IGF-1 axis in lifespan and healthspan: Lessons from animal models. Growth Horm. IGF Res. 2008;18(6):455-471. DOI 10.1016/j.ghir.2008.05.005.

2. Brusentsev E.Yu., Igonina T.N., Amstislavsky S.Ya. Traditional and modern approaches to culture of preimplantation mammalian embryos in vitro. Ontogenez = Ontogenesis (Moscow). 2014;45(2):73-88. (in Russian)

3. Brusentsev E.Yu., Igonina T.N., Rozhkova I.N., Ragaeva D.S., Am-stislavsky S.Ya. Effects of growth factors during in vitro culture of mouse and rat embryos. Vavilovskii Zhurnal Genetiki i Selekt-sii = Vavilov Journal of Genetics and Breeding. 2015;19(4):372-377 DOI 10.18699/VJ15.046. (in Russian)

4. Green C.J., Day M.L. Insulin-like growth factor 1 acts as an autocrine factor to improve early embryogenesis in vitro. Int. J. Dev. Biol. 2013;57(11-12):837-44. DOI 10.1387/ijdb.130044md. PubMed PMID: 24623075.

5. Harlow G.M., Quinn P. Development of preimplantation mouse embryos in vivo and in vitro. Aust. J. Biol. Sci. 1982;35(2):187-193. Harvey M.B., Kaye P.L. Insulin-like growth factor-1 stimulates growth of mouse preimplantation embryos in vitro. Mol. Reprod. Dev. 1992; 31(3):195-199.

6. Heyner S., Shi C.Z., Garside W.T., Smith R.M. Functions of the IGFs in early mammalian development. Mol. Reprod. Dev. 1993;35(4): 421-425.

7. Ho Y., Wigglesworth K., Eppig J.J., Schultz R.M. Preimplantation development of mouse embryos in KSOM: augmentation by amino acids and analysis of gene expression. Mol. Reprod. Dev. 1995;41: 232-238.

8. Holzenberger M., Dupont J., Ducos B., Leneuve P., Geloen A., Even P.C., Cervera P., Le Bouc Y. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature. 2003;421(6919):182-187.

9. Horii T., Yanagisawa E., Kimura M., Morita S., Hatada I. Epigenetic differences between embryonic stem cells generated from blastocysts developed in vitro and in vivo. Cell Reprogram. 2010;12(5):551-563. DOI 10.1089/cell.2009.0104.

10. Igonina T.N., Ragaeva D.S., Tikhonova M.A., Petrova O.M., Her-beck Yu.E., Rozhkova I.N., Amstislavskaya T.G., Amstislavsky S. Ya. Neurodevelopment and behavior in neonatal OXYS rats with genetically determined accelerated senescence. Brain Res. 2017 (in press).

11. Kapur S., Tamada H., Dey S.K., Andrews G.K. Expression of insulinlike growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone. Biol. Reprod. 1992;46(2):208-219.

12. Kenyon C. A conserved regulatory system for aging. Cell. 2001;105(2): 165-168.

13. Khatir H., Anouassi A., Tibary A. In vitro and in vivo developmental competence of dromedary (Camelus dromedarius) embryos produced in vitro using two culture systems (mKSOMaa and oviductal cells). Reprod. Domest. Anim. 2005;40(3):245-249.

14. Kito S., Kaneko Y., Yano H., Tateno S., Ohta Y. Developmental responses of 2-cell embryos to oxygen tension and bovine serum albumin in Wistar rats. Exp. Anim. 2008;57(2):123-128.

15. Krisher R.L. In vivo and in vitro environmental effects on mammalian oocyte quality. Annu. Rev. Anim. Biosci. 2013;1:393-417. DOI 10.1146/annurev-animal-031412-103647.

16. Lighten A.D., Moore G.E., Winston R.M., Hardy K. Routine addition of human insulin-like growth factor-I ligand could benefit clinical in vitro fertilization culture. Hum. Reprod. 1998;13(11):3144-3150.

17. Lin T.-C., Yen J.-M., Gong K.-B., Hsu T.-T., Chen L.-R. IGF-1/ IGFBP-1 increases blastocyst formation and total blastocyst cell number in mouse embryo culture and facilitates the establishment of a stem-cell line. BMC Cell Biol. 2003;4:14. DOI 10.1186/1471-21214-14.

18. Manabe Y., Tochigi M., Moriwaki A., Takeuchi S., Takahashi S. Insulin-like growth factor 1 mRNA expression in the uterus of strepto-zotocin-treated diabetic mice. J. Reprod. Dev. 2013;59(4):398-404. DOI 10.1262/jrd.2012-169.

19. Miyoshi K., Kono T., Niwa K. Stage-dependent development of rat 1-cell embryos in a chemically defined medium after fertilization in vivo and in vitro. Biol. Reprod. 1997;56(1):180-185.

20. Popova E., Bader M., Krivokharchenko A. Effect of culture conditions on viability of mouse and rat embryos developed in vitro. Genes. 2011;2(2):332-344. DOI 10.3390/genes2020332.

21. Renzini M., Dal Canto M., Coticchio G., Comi R., Brigante C., Ca-liari I., Brambillasca F., Merola M., Lain M., Turchi D. Clinical efficiency and perinatal outcome of ART cycles following embryo culture in the presence of GM-CSF in patients with miscarriage or early pregnancy loss history. Hum. Reprod. 2013;28(1):160-202.

22. Robertson S.A. GM-CSF regulation of embryo development and pregnancy. Cytokine Growth Factor Rev. 2007;18(3-4):287-298. Roth T.L., Swanson W.F., Wildt D.E. Developmental competence of domestic cat embryos fertilized in vivo versus in vitro. Biol. Re-prod. 1994;51(3):441-451.

23. Schiffner J., Spielmann H. Fluorometric assay of the protein content of mouse and rat embryos during preimplantation development. J. Reprod. Fertil. 1976;47(1):145-147.

24. Schultz G.A., Heyner S. Growth factors in preimplantation mammalian embryos. Oxf. Rev. Reprod. Biol. 1993;15:43-81.

25. Scott L., Whittingham D.G. Influence of genetic background and media components on the development of mouse embryos in vitro. Mol. Reprod. Dev. 1996;3(3):336-346.

26. Summers M.C., Biggers J.D. Chemically defined media and the culture of mammalian preimplantation embryos: historical perspective and current issues. Hum. Reprod. Update. 2003;9(6):557-582.

27. Thongkittidilok C., Tharasanit T., Sananmuang T. Insulin-like growth factor-1 (IGF-1) enhances developmental competence of cat embryos cultured singly by modulating the expression of its receptor (IGF-1R) and reducing developmental block. Growth Horm. IGF Res. 2014;24(2-3):76-82.

28. Velazquez M.A., Hermann D., Kues W.A., Niemann H. Increased apoptosis in bovine blastocysts exposed to high levels of IGF1 is not associated with downregulation of the IGF1 receptor. Reproduction. 2011:41(1):91-103. DOI 10.1530/REP-10-0336.

29. Xia P., Han V.K., Viuff D., Armstrong D.T., Watson A.J. Expression of insulin-like growth factors in two bovine oviductal cultures employed for embryo co-culture. J. Endocrinol. 1996;149:41-53.

30. Zhang X., Kidder G.M., Watson A.J., Schultz G.A., Armstrong D.T. Possible roles of insulin and insulin-like growth factors in rat preimplantation development: investigation of gene expression by reverse transcription-polymerase chain reaction. J. Reprod. Fertil. 1994; 100(2):375-380.