Skip to main content

Advertisement

Log in

Oocyte maturation-related gene expression in the canine oviduct, cumulus cells, and oocytes and effect of co-culture with oviduct cells on in vitro maturation of oocytes

  • Gamete Biology
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

In contrast to most other mammals, canine oocytes are ovulated in an immature state and undergo oocyte maturation within the oviduct during the estrus stage. The aim of the study was to investigate whether oviduct cells from the estrus stage affect the maturation of oocytes and show gene expression patterns related to oocyte maturation.

Methods

We analyzed MAPK1/3, SMAD2/3, and BMP6/15 expression in oviduct cells, cumulus cells, and oocytes from anestrus, estrus, and diestrus stages. Next, we investigated the effect of co-culture with oviduct cells derived from the estrus stage upon in vitro maturation (IVM) of canine oocytes.

Results

There was significantly higher MAPK1/3 (1.42 ± 0.02 and 2.23 ± 0.06), SMAD2/3 (0.77 ± 0.03 and 2.39 ± 0.07), and BMP15 (2.21 ± 0.16) expression in oviduct cells at the estrus stage (P < 0.05). In cumulus cells, MAPK1 (1.26 ± 0.07), SMAD2/3 (0.82 ± 0.01, 1.04 ± 0.01), and BMP6 (13.09 ± 0.11) expression was significantly higher in the estrus stage (P < 0.05). In oocytes, significant upregulation of MAPK1/3 (14,960 ± 3121 and 1668 ± 253.4), SMAD3 (774.6 ± 79.62), and BMP6 (8500 ± 895.4) expression was found in the estrus stage (P < 0.05). After 72 h of IVM culture, a significantly higher maturation rate was observed in oocytes co-cultured with oviduct cells (10.0 ± 1.5%) than in the control group (3.2 ± 1.4%).

Conclusions

We demonstrate that oviduct cells at the estrus stage highly expressed MAPK1/3, SMAD2/3, and BMP15. Furthermore, canine oviduct cells from the estrus stage enhance the culture environment for canine oocyte maturation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Hashimoto S. Application of in vitro maturation to assisted reproductive technology. J Reprod Dev. 2009;55(1):1–10.

    Article  CAS  PubMed  Google Scholar 

  2. Reynaud K, Fontbonne A, Saint-Dizier M, Thoumire S, Marnier C, Tahir MZ, et al. Folliculogenesis, ovulation and endocrine control of oocytes and embryos in the dog. Reprod Domest Anim. 2012;47(Suppl 6):66–9. doi:10.1111/rda.12055.

    Article  PubMed  Google Scholar 

  3. Chastant-Maillard S, Viaris de Lesegno C, Chebrout M, Thoumire S, Meylheuc T, Fontbonne A, et al. The canine oocyte: uncommon features of in vivo and in vitro maturation. Reprod Fertil Dev. 2011;23(3):391–402. doi:10.1071/RD10064.

    Article  CAS  PubMed  Google Scholar 

  4. Hewitt DA, England GC. Synthetic oviductal fluid and oviductal cell coculture for canine oocyte maturation in vitro. Anim Reprod Sci. 1999;55(1):63–75.

    Article  CAS  PubMed  Google Scholar 

  5. Lee HS, Seo YI, Yin XJ, Cho SG, Lee SS, Kim NH, et al. Effect of follicle stimulation hormone and luteinizing hormone on cumulus cell expansion and in vitro nuclear maturation of canine oocytes. Reprod Domest Anim. 2007;42(6):561–5. doi:10.1111/j.1439-0531.2006.00818.x.

    Article  CAS  PubMed  Google Scholar 

  6. Bolamba D, Russ KD, Harper SA, Sandler JL, Durrant BS. Effects of epidermal growth factor and hormones on granulosa expansion and nuclear maturation of dog oocytes in vitro. Theriogenology. 2006;65(6):1037–47. doi:10.1016/j.theriogenology.2005.06.017.

    Article  CAS  PubMed  Google Scholar 

  7. Cui XS, Jin YX, Shen XH, Lee JY, Lee HS, Yin XJ, et al. Epidermal growth factor enhances meiotic resumption of canine oocytes in the presence of BSA. Theriogenology. 2006;66(2):267–74. doi:10.1016/j.theriogenology.2005.11.011.

    Article  CAS  PubMed  Google Scholar 

  8. Hatoya S, Sugiyama Y, Torii R, Wijewardana V, Kumagai D, Sugiura K, et al. Effect of co-culturing with embryonic fibroblasts on IVM, IVF and IVC of canine oocytes. Theriogenology. 2006;66(5):1083–90. doi:10.1016/j.theriogenology.2005.12.015.

    Article  CAS  PubMed  Google Scholar 

  9. Abdel-Ghani MA, Shimizu T, Asano T, Suzuki H. In vitro maturation of canine oocytes co-cultured with bovine and canine granulosa cell monolayers. Theriogenology. 2012;77(2):347–55. doi:10.1016/j.theriogenology.2011.08.007.

    Article  CAS  PubMed  Google Scholar 

  10. Boruszewska D, Sinderewicz E, Kowalczyk-Zieba I, Grycmacher K, Woclawek-Potocka I. The effect of lysophosphatidic acid during in vitro maturation of bovine cumulus-oocyte complexes: cumulus expansion, glucose metabolism and expression of genes involved in the ovulatory cascade, oocyte and blastocyst competence. Reprod Biol Endocrinol. 2015;13:44. doi:10.1186/s12958-015-0044-x.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Romero-Aguirregomezcorta J, Santa AP, Garcia-Vazquez FA, Coy P, Matas C. Nitric oxide synthase (NOS) inhibition during porcine in vitro maturation modifies oocyte protein S-nitrosylation and in vitro fertilization. PLoS One. 2014;9(12):e115044. doi:10.1371/journal.pone.0115044.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Zavareh S, Karimi I, Salehnia M, Rahnama A. Effect of in vitro maturation technique and alpha lipoic acid supplementation on oocyte maturation rate: focus on oxidative status of oocytes. Int J Fertil Steril. 2016;9(4):442–51.

    CAS  PubMed  Google Scholar 

  13. Motola S, Cao X, Popliker M, Tsafriri A. Involvement of mitogen-activated protein kinase (MAPK) pathway in LH- and meiosis-activating sterol (MAS)-induced maturation in rat and mouse oocytes. Mol Reprod Dev. 2008;75(10):1533–41. doi:10.1002/mrd.20899.

    Article  CAS  PubMed  Google Scholar 

  14. Zhang YL, Liu XM, Ji SY, Sha QQ, Zhang J, Fan HY. ERK1/2 activities are dispensable for oocyte growth but are required for meiotic maturation and pronuclear formation in mouse. J Genet Genomics. 2015;42(9):477–85. doi:10.1016/j.jgg.2015.07.004.

    Article  CAS  PubMed  Google Scholar 

  15. Yeo CX, Gilchrist RB, Lane M. Disruption of bidirectional oocyte-cumulus paracrine signaling during in vitro maturation reduces subsequent mouse oocyte developmental competence. Biol Reprod. 2009;80(5):1072–80. doi:10.1095/biolreprod.108.073908.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Hussein TS, Froiland DA, Amato F, Thompson JG, Gilchrist RB. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci. 2005;118(Pt 22):5257–68. doi:10.1242/jcs.02644.

    Article  CAS  PubMed  Google Scholar 

  17. Glister C, Kemp CF, Knight PG. Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin. Reproduction. 2004;127(2):239–54. doi:10.1530/rep.1.00090.

    Article  CAS  PubMed  Google Scholar 

  18. Seger R, Krebs EG. The MAPK signaling cascade. FASEB J. 1995;9(9):726–35.

    CAS  PubMed  Google Scholar 

  19. Concannon PW. Reproductive cycles of the domestic bitch. Anim Reprod Sci. 2011;124(3–4):200–10. doi:10.1016/j.anireprosci.2010.08.028.

    Article  CAS  PubMed  Google Scholar 

  20. Kim MJ, Oh HJ, Kim GA, Jo YK, Choi J, Lee BC. Application of chemiluminescence enzyme immunoassay method to collect in vivo matured oocyte in dog cloning. J Vet Clin. 2014a;31(4):267–71.

    Article  Google Scholar 

  21. Schutte AP. Canine vaginal cytology. I. Technique and cytological morphology. J Small Anim Pract. 1967;8(6):301–6.

    Article  CAS  PubMed  Google Scholar 

  22. van Goethem B, Schaefers-Okkens A, Kirpensteijn J. Making a rational choice between ovariectomy and ovariohysterectomy in the dog: a discussion of the benefits of either technique. Vet Surg. 2006;35(2):136–43. doi:10.1111/j.1532-950X.2006.00124.x.

    Article  PubMed  Google Scholar 

  23. Oh HJ, Fibrianto YH, Kim MK, Jang G, Hossein MS, Kim HJ, et al. Effects of canine serum collected from dogs at different estrous cycle stages on in vitro nuclear maturation of canine oocytes. Zygote. 2005;13(3):227–32.

    Article  PubMed  Google Scholar 

  24. Kim MK, Fibrianto YH, Oh HJ, Jang G, Kim HJ, Lee KS, et al. Effects of estradiol-17beta and progesterone supplementation on in vitro nuclear maturation of canine oocytes. Theriogenology. 2005;63(5):1342–53. doi:10.1016/j.theriogenology.2004.07.019.

    Article  CAS  PubMed  Google Scholar 

  25. Kim GA, Oh HJ, Lee TH, Lee JH, Oh SH, Lee JH, et al. Effect of culture medium type on canine adipose-derived mesenchymal stem cells and developmental competence of interspecies cloned embryos. Theriogenology. 2014b;81(2):243–9. doi:10.1016/j.theriogenology.2013.09.018.

    Article  CAS  PubMed  Google Scholar 

  26. Lee BC, Kim MK, Jang G, Oh HJ, Yuda F, Kim HJ, et al. Dogs cloned from adult somatic cells. Nature. 2005;436(7051):641. doi:10.1038/436641a.

    Article  CAS  PubMed  Google Scholar 

  27. Hong SG, Oh HJ, Park JE, Kim MJ, Kim GA, Park EJ, et al. Production of offspring from cloned transgenic RFP female dogs and stable generational transmission of the RFP gene. Genesis. 2011;49(11):835–40. doi:10.1002/dvg.20772.

    Article  CAS  PubMed  Google Scholar 

  28. Kim MJ, Oh HJ, Park JE, Kim GA, Hong SG, Jang G, et al. Generation of transgenic dogs that conditionally express green fluorescent protein. Genesis. 2011;49(6):472–8. doi:10.1002/dvg.20737.

    Article  CAS  PubMed  Google Scholar 

  29. Saadeldin IM, Elsayed A, Kim SJ, Moon JH, Lee BC. A spatial model showing differences between juxtacrine and paracrine mutual oocyte-granulosa cells interactions. Indian J Exp Biol. 2015;53(2):75–81.

    PubMed  Google Scholar 

  30. de Avila Rodrigues B, Rodrigues JL. Influence of reproductive status on in vitro oocyte maturation in dogs. Theriogenology. 2003;60(1):59–66.

    Article  PubMed  Google Scholar 

  31. Kimura N, Hoshino Y, Totsukawa K, Sato E. Cellular and molecular events during oocyte maturation in mammals: molecules of cumulus-oocyte complex matrix and signalling pathways regulating meiotic progression. Soc Reprod Fertil Suppl. 2007;63:327–42.

    CAS  PubMed  Google Scholar 

  32. Luvoni GC, Chigioni S, Allievi E, Macis D. Factors involved in vivo and in vitro maturation of canine oocytes. Theriogenology. 2005;63(1):41–59. doi:10.1016/j.theriogenology.2004.03.004.

    Article  CAS  PubMed  Google Scholar 

  33. Liang CG, Su YQ, Fan HY, Schatten H, Sun QY. Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase. Mol Endocrinol. 2007;21(9):2037–55. doi:10.1210/me.2006-0408.

    Article  CAS  PubMed  Google Scholar 

  34. Ebeling S, Schuon C, Meinecke B. Mitogen-activated protein kinase phosphorylation patterns in pig oocytes and cumulus cells during gonadotrophin-induced resumption of meiosis in vitro. Zygote. 2007;15(2):139–47. doi:10.1017/S0967199406004011.

    Article  CAS  PubMed  Google Scholar 

  35. Fan HY, Huo LJ, Chen DY, Schatten H, Sun QY. Protein kinase C and mitogen-activated protein kinase cascade in mouse cumulus cells: cross talk and effect on meiotic resumption of oocyte. Biol Reprod. 2004;70(4):1178–87. doi:10.1095/biolreprod.103.024737.

    Article  CAS  PubMed  Google Scholar 

  36. Fatehi AN, van den Hurk R, Colenbrander B, Daemen AJ, van Tol HT, Monteiro RM, et al. Expression of bone morphogenetic protein2 (BMP2), BMP4 and BMP receptors in the bovine ovary but absence of effects of BMP2 and BMP4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology. 2005;63(3):872–89. doi:10.1016/j.theriogenology.2004.05.013.

    Article  CAS  PubMed  Google Scholar 

  37. Knight PG, Glister C. TGF-beta superfamily members and ovarian follicle development. Reproduction. 2006;132(2):191–206. doi:10.1530/rep.1.01074.

    Article  CAS  PubMed  Google Scholar 

  38. Buccione R, Schroeder AC, Eppig JJ. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod. 1990;43(4):543–7.

    Article  CAS  PubMed  Google Scholar 

  39. Pan Y, He H, Cui Y, Baloch AR, Li Q, Fan J, et al. Recombinant human bone morphogenetic protein 6 enhances oocyte reprogramming potential and subsequent development of the cloned yak embryos. Cell Reprogram. 2015;17(6):484–93. doi:10.1089/cell.2015.0049.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Su YQ, Sugiura K, Wigglesworth K, O’Brien MJ, Affourtit JP, Pangas SA, et al. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development. 2008;135(1):111–21. doi:10.1242/dev.009068.

    Article  CAS  PubMed  Google Scholar 

  41. Dube JL, Wang P, Elvin J, Lyons KM, Celeste AJ, Matzuk MM. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol. 1998;12(12):1809–17. doi:10.1210/mend.12.12.0206.

    Article  CAS  PubMed  Google Scholar 

  42. Paradis F, Novak S, Murdoch GK, Dyck MK, Dixon WT, Foxcroft GR. Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction. 2009;138(1):115–29. doi:10.1530/REP-08-0538.

    Article  CAS  PubMed  Google Scholar 

  43. Kuo FT, Fan K, Ambartsumyan G, Menon P, Ketefian A, Bentsi-Barnes IK, et al. Relative expression of genes encoding SMAD signal transduction factors in human granulosa cells is correlated with oocyte quality. J Assist Reprod Genet. 2011;28(10):931–8. doi:10.1007/s10815-011-9609-6.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Shimasaki S, Moore RK, Otsuka F, Erickson GF. The bone morphogenetic protein system in mammalian reproduction. Endocr Rev. 2004;25(1):72–101. doi:10.1210/er.2003-0007.

    Article  CAS  PubMed  Google Scholar 

  45. Li Q, Pangas SA, Jorgez CJ, Graff JM, Weinstein M, Matzuk MM. Redundant roles of SMAD2 and SMAD3 in ovarian granulosa cells in vivo. Mol Cell Biol. 2008;28(23):7001–11. doi:10.1128/MCB.00732-08.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Thompson JG, Armstrong DT, et al. Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod. 2007;76(5):848–57. doi:10.1095/biolreprod.106.057471.

    Article  CAS  PubMed  Google Scholar 

  47. Kidson A, Schoevers E, Langendijk P, Verheijden J, Colenbrander B, Bevers M. The effect of oviductal epithelial cell co-culture during in vitro maturation on sow oocyte morphology, fertilization and embryo development. Theriogenology. 2003;59(9):1889–903.

    Article  PubMed  Google Scholar 

  48. Bureau M, Bailey JL, Sirard MA. Influence of oviductal cells and conditioned medium on porcine gametes. Zygote. 2000;8(2):139–44.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by RDA (#PJ010928032017), Korea IPET (#316002-05-2-SB010), Research Institute for Veterinary Science, the BK21 plus program, and global Ph.D. Fellowship Program through the National Research Foundation of Korea (NRF-20142A1021187).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Byeong Chun Lee.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, S.H., Oh, H.J., Kim, M.J. et al. Oocyte maturation-related gene expression in the canine oviduct, cumulus cells, and oocytes and effect of co-culture with oviduct cells on in vitro maturation of oocytes. J Assist Reprod Genet 34, 929–938 (2017). https://doi.org/10.1007/s10815-017-0910-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10815-017-0910-x

Keywords

Navigation