Hostname: page-component-669899f699-ggqkh Total loading time: 0 Render date: 2025-04-25T10:02:28.615Z Has data issue: false hasContentIssue false
  • English
  • Français

Cumulus cell features and nuclear chromatin configuration of in vitro matured canine COCs and the influence of in vivo serum progesterone concentrations of ovary donors

Published online by Cambridge University Press:  01 February 2009

B. A. Rodrigues ,
A. E. F. Silva ,
P. Rodriguez ,
L. F. Cavalcante  and
J. L. Rodrigues
B. A. Rodrigues*
Affiliation:
Laboratory of Embryology and Biotechnics of Reproduction, Faculty of Veterinary Medicine, UFRGS; Cx Postal 15004, 91501-970 Porto Alegre, RS, Brazil. Laboratory of Embryology and Biotechnics of Reproduction, Faculty of Veterinary Medicine, UFRGS; Porto Alegre, RS, Brazil.
A. E. F. Silva
Affiliation:
Laboratory of Embryology and Biotechnics of Reproduction, Faculty of Veterinary Medicine, UFRGS; Porto Alegre, RS, Brazil.
P. Rodriguez
Affiliation:
Laboratory of Embryology and Biotechnics of Reproduction, Faculty of Veterinary Medicine, UFRGS; Porto Alegre, RS, Brazil.
L. F. Cavalcante
Affiliation:
Laboratory of Embryology and Biotechnics of Reproduction, Faculty of Veterinary Medicine, UFRGS; Porto Alegre, RS, Brazil.
J. L. Rodrigues
Affiliation:
Laboratory of Embryology and Biotechnics of Reproduction, Faculty of Veterinary Medicine, UFRGS; Porto Alegre, RS, Brazil.
*
All correspondence to Berenice de Ávila Rodrigues. Laboratory of Embryology and Biotechnics of Reproduction, Faculty of Veterinary Medicine, UFRGS; Cx Postal 15004, 91501-970 Porto Alegre, RS, Brazil. Tel: +55 51 33086126. e-mail: berenice@portoweb.com.br
Get access Rights & Permissions [Opens in a new window]

Summary

Phenotype integrity is viewed as an indicator of cumulus–oocyte complex (COC) viability. The objectives of this study were: (a) to observe the influence of cumulus investment expansion on the nuclear chromatin configuration of canine oocytes matured in vitro; (b) to examine the relationship between cumulus cell (CC) expansion and its morphology after in vitro maturation (IVM); (c) to ascertain the influence of in vivo serum progesterone (SP) concentrations of ovary donors on oocyte nuclear maturation, CC phenotypes and degrees of CC expansion of in vitro matured COCs. After 48 h of IVM in modified TCM 199, CCs from grade 1 and 2 COCs were stained with propidium iodide. Oocyte chromatin configuration was visualized by Hoechst 33342 stain. Results showed that oocyte IVM was not influenced by degree of CC expansion (D1, D2 and D3) in COCs. From the CC types (C1, C2 and C3), number of C1 types was higher at D1 expansion and differed from those observed at D2 and D3 expansions. Additionally, rates of apoptosis in D1 CCs were lower than those observed in D2 CCs (p < 0.05). Oocyte nuclear maturation was not influenced by in vivo SP concentrations of ovary donors. On the other hand, D3 expansion prevailed in COCs from bitches at SP > 2.5 ng/ml (p < 0.001). Moreover, in vitro CC apoptosis was associated both with low (0–1 ng/ml) and with high (>5 ng/ml) in vivo SP levels. These findings indicate that morphology of CCs from in vitro matured dog oocytes gives valuable information on viability of COCs and could possibly be used as a parameter in predicting the quality of oocytes destined for in vitro fertilization (IVF) and their outcomes.

Keywords

ApoptosisCumulus cellsDogOocyteProgesterone
Type
Research Article
Information
Zygote , Volume 17 , Issue 1 , February 2009 , pp. 79 - 91
Copyright
Copyright © Cambridge University Press 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

Abe, H. & Hoshi, H. (2003). Evaluation of bovine embryos produced in high performance serum-free media. J. Reprod. Dev. 49, 193–202.CrossRefGoogle ScholarPubMed
Ball, G.D., Ax, R.L. & First, N.L. (1980). Mucopolysaccharide synthesis accompanies expansion of bovine cumulus–oocytes complexes in vitro. In Functional Correlates of Hormone Receptors in Reproduction. (eds. Mahash, V.B., Muldoon, T.G., Saxana, B.B. & Sadler, W.A.), p. 561. North Holland, New York: Elsevier.Google Scholar
Bogliolo, L., Ariu, F., Fois, S., Rosati, I., Zedola, M.T., Leoni, G., Succu, S., Pau, S. & Ledda, S. (2007). Morphological and biochemical analysis of immature ovine oocytes vitrified with or without cumulus cells. Theriogenology 68, 1138–49.CrossRefGoogle ScholarPubMed
Bolamba, D., Russ, K.D., Harper, S.A., Sandler, J.L., & Durrant, B.S. (2006). Effects of epidermal growth factor and hormones on granulosa expansion and nuclear maturation of dog oocytes in vitro. Theriogenology 65, 1037–47.CrossRefGoogle ScholarPubMed
Brück, I., Bézard, J., Baltsen, M., Synnestvedt, B., Couty, I., Greve, T. & Duchamp, G. (2000). Effect of administering a crude gonadotrophin preparation to mares on follicular development, oocyte recovery rate and oocyte maturation in vivo.J. Reprod. Fertil. 118, 351–60.CrossRefGoogle ScholarPubMed
Calado, A.M., Rocha, E., Colaço, A. & Sousa, M. (2001). Stereologic characterization of bovine (Bos taurus) cumulus–oocyte complexes aspirated from small antral follicles during the diestrus phase. Biol. Reprod. 65, 1383–91.CrossRefGoogle Scholar
Calado, A.M., Rocha, E., Colaço, A. & Sousa, M. (2003). A stereological study of medium antral follicles during the bovine estrous cycle. Tissue & Cell 35, 313–23CrossRefGoogle ScholarPubMed
De Los Reyes, M., de Lange, J., Miranda, P., Palominos, J. & Barros, C. (2005). Effect of human chorionic gonadotrophin supplementation during different culture periods on in vitro maturation of canine oocytes. Theriogenology 64, 1–11.CrossRefGoogle ScholarPubMed
Dunning, K.R., Lane, M., Brown, H.M., Yeo, C., Robker, R.L. & Russell, D.L. (2007). Altered composition of the cumulus–oocyte complex matrix during in vitro maturation of oocytes Human Reprod. 22, 2842–50.CrossRefGoogle ScholarPubMed
Ebner, T., Moser, M. & Tews, G. (2006). Is oocyte morphology prognostic of embryo developmental potential after ICSI? Reprod. Biomed. Online 12, 507–12.CrossRefGoogle ScholarPubMed
Fabian, D., Koppel, J. & Maddox-Hyttel, P. (2005). Apoptotic processes during mammalian preimplantation development. Theriogenology 64, 221–31.CrossRefGoogle ScholarPubMed
Feldman, E.C. & Nelson, R.W. (1997). The Ovarian Cycle and Vaginal Cytology in the Bitch. Internal Medicine Proceedings 284, pp. 273–88. Post Graduate Foundation in Veterinary Science University of Sydney.Google Scholar
Funahashy, H. & Day, B.N. (1993). Effects of the duration of exposure to hormone supplements on cytoplasmic maturation of pig oocytes in vitro. J. Reprod. Fertil. 98, 179–85.CrossRefGoogle Scholar
Gandolfi, F., Brevini, T.A.L., Cillo, F. & Antonini, S. (2005). Cellular and molecular mechanisms regulating oocyte quality and the relevance for animal reproductive efficiency. Rev. Sci. Tech. Int. Epiz. 24, 413–23.CrossRefGoogle ScholarPubMed
Greenwald, G.S. (1989). Temporal and topographic changes in DNA synthesis after induced follicular atresia. Biol. Reprod. 40, 175–81.CrossRefGoogle Scholar
Hewitt, D.A., Watson, P.F. & England, G.C.W. (1998). Nuclear staining and culture requirements for in vitro maturation of domestic bitch oocytes. Theriogenology 49, 1083–101.CrossRefGoogle ScholarPubMed
Hossein, M.S., Kim, M.K., Jang, G., Oh, H. J., Koo, O., Kim, J.J., Kang, S.K., Lee, B.C. & Hwang, W.S. (2007). Effects of thiol compounds on in vitro maturation of canine oocytes collected from different reproductive stages. Mol. Reprod. Dev. 74, 1213–20.CrossRefGoogle ScholarPubMed
Hussein, T.S., Froiland, D.A., Amato, F., Thompson, J.G. & Gilchrist, R.B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257–68.CrossRefGoogle ScholarPubMed
Ikeda, S., Imai, H. & Yamada, M. (2003). Apoptosis in cumulus cells during in vitro maturation of bovine cumulus-enclosed oocytes. Reproduction 125, 369–76.CrossRefGoogle ScholarPubMed
Kerr, J.F., Wyllie, A.H. & Currie, A.R. (1972). Apoptosis: a basic biological phenomenon with wide-ranging implication in tissue kinetics. Br. J. Cancer 26, 239–57.CrossRefGoogle ScholarPubMed
Köhle, S., Woehl-Wenigerkind, A., Sinowatz, F. & Braun, J. (2005). Regulation of cumulus cell numbers in the course of the canine estrous cycle. Anat. Histol. Embryol. (Suppl.) 34, 26–7.CrossRefGoogle Scholar
Lee, H-S., Seo, Y-I., Yin, X-J., Cho, S-G., Lee, S-S., Kim, N-H., Cho, S-K. & Kon, I.K. (2007). Effect of follicle stimulation hormone and luteinizing hormone on cumulus cell expansion and in vitro nuclear maturation of canine oocytes. Reprod. Dom. Anim. 42, 561–5.CrossRefGoogle ScholarPubMed
Lopes, G., Sousa, M., Luvoni, G. & Rocha, A. (2007). Recovery rate, morphological quality and nuclear maturity of canine cumulus–oocyte complexes collected from anestrus or diestrus bitches of different ages. Theriogenology 68, 821–5.CrossRefGoogle ScholarPubMed
McNatty, K.P., Heath, D.A., Henderson, K.M., Lun, S., Hurst, P.R., Ellis, L.M., Montgomery, G.W., Morrison, L. & Thurley, D.C. (1984). Some aspects of thecal and granulosa cell function during follicular development in the bovine ovary. J. Reprod. Fertil. 72, 39–53.CrossRefGoogle ScholarPubMed
Mrazek, M. & FulkaJ., Jr. J., Jr. (2003). Failure of oocyte maturation: possible mechanisms for oocyte maturation arrest. Human Reprod. 18, 2249–52.CrossRefGoogle ScholarPubMed
Nickson, D.A., Boyd, J.S., Eckersall, P.D., Ferguson, J.M., Harvey, M.J.A. & Renton, J.P. (1993). Molecular biological methods for monitoring oocyte maturation and in vitro fertilization in bitches.J. Reprod. Fertil. (Suppl.) 47, 231–40.Google ScholarPubMed
Otoi, T., Ooka, A.N., Muramaki, M., Karja, N.W.K. & Suzuki, T. (2001). Size distribution and meiotic competence of oocytes obtained from bitches ovaries at various stages of the estrous cycle. Reprod. Fertil. Dev. 13, 151–5.CrossRefGoogle Scholar
Perez, G.I., Tao, X-J. & Tilly, J.L. (1999). Fragmentation and death (aka apoptosis) of ovulated oocytes Mol. Human. Reprod. 5, 414–20.CrossRefGoogle ScholarPubMed
Rattanachaiyanont, M., Leader, A., & Leveille, M.C. (1999). Lack of correlation between oocyte corona–cumulus complex morphology and nuclear maturity of oocytes collected in stimulated cycles for intracytoplasmic sperm injection. Fertil. Steril. 71, 937–40.CrossRefGoogle ScholarPubMed
Roberts, R., Frank, S. & Hardy, K. (2002). Culture environment modulates maturation and metabolism of human oocytes. Human Reprod. 17, 2950–6.CrossRefGoogle ScholarPubMed
Rodrigues, B.A. & Rodrigues, J.L. (2003). Influence of reproductive status on in vitro oocyte maturation in dogs Theriogenology 60, 59–66.CrossRefGoogle Scholar
Rodrigues, B.A., dos Santos, L.C. & Rodrigues, J.L. (2004). Embryonic development of in vitro matured and in vitro fertilized dog oocytes. Mol. Reprod. Dev. 67, 215–23.CrossRefGoogle ScholarPubMed
Rodrigues, B.A. & Rodrigues, J.L. (2006). Responses of canine oocytes to in vitro maturation and in vitro fertilization outcome. Theriogenology 66, 1667–72.CrossRefGoogle ScholarPubMed
Rodrigues, B.A., dos Santos, L.C. & Rodrigues, J.L. (2006). The effect of hyaluronan concentrations in hST-supplemented TCM 199 on in vitro nuclear maturation of bitch cumulus oocyte complexes Theriogenology 66, 1673–6.CrossRefGoogle ScholarPubMed
Rodrigues, B.A., dos Santos, L.C. & Rodrigues, J.L. (2007). Effect of maturation medium on in vitro cleavage of canine oocytes fertilized with fresh and cooled homologous semen. Zygote 15, 43–53.CrossRefGoogle ScholarPubMed
Rodriguez, P., Arruda, N.Cavalcante, L.F.Silva, A.E.F., Rodrigues, B.A. & Rodrigues, J.L. (2008). Cumulus cells viability and the relationship with nuclear morphology in oocytes from pre-pubertal and adult bitches at 0,24,48 and 72 hours after in vitro maturation. Proceedings of the 6th ISCFR (International Symposium on Canine and Feline Reproduction) & 6th Biannual EVSSAR Congress. (eds. England, G., Concannon, P., Schäfer-Somi, S.), pp. 201, 202. Vienna, Austria.Google Scholar
Santos, L.C., Rodrigues, B.A. & Rodrigues, J.L. (2006). In vitro nuclear maturation of bitch oocytes in the presence of polyvinyl-pyrrolidone. Anim. Reprod. 3, 70–5.Google Scholar
Silva, A.E.F., Rodriguez, P.Cavalcante, L.F.Rodrigues, B.A. & Rodrigues, J.L. (2008). The influence of oxygen tension on cumulus cell viability of canine COCs matured in high glucose medium. Proceedings of the 6th ISCFR (International Symposium on Canine and Feline Reproduction) & 6th Biannual EVSSAR Congress. (eds. England, G., Concannon, P., Schäfer-Somi, S.), pp. 226–8. Vienna, Austria.Google Scholar
Songsasen, N., Yu, I. & Leibo, S.P. (2002). Nuclear maturation of canine oocytes cultured in protein free-media. Mol. Reprod. Dev. 62, 407–15.CrossRefGoogle ScholarPubMed
Songsasen, N., Spindler, R. & Wildt, D. (2005). Impact of nuclear status and maturation period on energy substrate use by in vitro-cultured dog oocytes. Proceedings of the 38th SSR (The Society for the Study of Reproduction) Annual Meeting. Quebec, Canada.Google Scholar
Srsen, V., Kalous, J., Nagyova, E., Sutovsky, P., King, W.A. & Motlik, J. (1998). Effects of follicle-stimulating hormone, bovine somatotrophin and okadaic acid on cumulus expansion and nuclear maturation of blue fox (Alopex lagopus) oocytes in vitro. Zygote 6, 299–309.CrossRefGoogle ScholarPubMed
St John, J.C. (2002). The transmission of mitochondrial DNA following assisted reproductive techniques. Theriogenology 57, 109–23.CrossRefGoogle ScholarPubMed
Suzuki, H., Jeong, B-S. & Yang, X. (2000). Dynamic changes of cumulus–oocyte cell communication during in vitro maturation of porcine oocytes. Biol. Reprod. 63, 723–9.CrossRefGoogle ScholarPubMed
Trumpan, M. (2001). Experimentelle Untersuchungen zur In vitro maturation von Kumulus–Oozyten–Komplexen von Sus scrofa f.d. in modifizierten Whitten's Medium, p. 155. Thesis. Tierärztlichen Hochschule Hannover, Germany.Google Scholar
Tsafriri, A. & Braw, R.H. (1984). Experimental approaches to atresia in mammals. Oxf. Rev. Reprod. Biol. 6, 226–65.Google ScholarPubMed
Van Cruchten, S., Van den Broeck, W., Duchateau, L. & Simoens, P. (2003). Apoptosis in the canine endometrium during the estrous cycle. Theriogenology 60, 1595–608.CrossRefGoogle ScholarPubMed
Van Soom, A., Tanghe, S., de Pauw, I., Maes, D. & de Kruif, A. (2002). Function of cumulus otophorus before and during mammalian fertilization. Reprod. Dom. Anim. 37, 144–51.CrossRefGoogle ScholarPubMed
Van Soom, A., Vandaele, L., Goossens, K., de Kruif, A. & Peelman, L. (2007). Gamete origin in relation to early embryo development. Theriogenology (Suppl.) 68, 131–7.CrossRefGoogle ScholarPubMed
Warriach, H.M. & Chohan, K.R. (2004). Thickness of cumulus cell layer is a significant factor in meiotic competence of buffalo oocytes J. Vet. Sci. 5, 247–51.CrossRefGoogle ScholarPubMed
Willingham-Rocky, L.A., Hinrichs, K., Westhusin, M.E. & Kraemer, D.C. (2003). Effects of stage of oestrus cycle and progesterone supplementation during culture on maturation of canine oocytes in vitro. Reproduction 126, 501–8.CrossRefGoogle ScholarPubMed
Yang, M.Y. & Rajamahendran, R. (2000). Morphological and biochemical identification of apoptosis in small, medium and large bovine follicles and the effects of follicle-stimulating hormone and insulin-like growth factor-i on spontaneous apoptosis in cultured bovine granulosa cells. Biol. Reprod. 62, 1209–17.CrossRefGoogle ScholarPubMed
Yokoo, M., Miyahayashi, Y., Nagamura, T., Kimura, N., Sasada, H. & Sato, E. (2002). Identification of hyaluronic acid-binding proteins and their expressions in porcine cumulus–oocyte complexes during in vitro maturation. Biol.Reprod. 67, 1165–71.CrossRefGoogle Scholar
Yuan, Y.Q., Van Soom, A., Leroy, J.L.M.R., Dewulf, J., Van Zeveren, A., de Kruif, A. & Peelman, L.J. (2005). Apoptosis in cumulus cells but not in oocytes, may influence bovine embryonic developmental competence Theriogenology 63, 2147–63.CrossRefGoogle Scholar
Zong, W-X. & Thompson, C.B. (2006). Necrotic death as a cell fate. Genes Dev. 20, 1–15.CrossRefGoogle ScholarPubMed