Chromatin, microtubule and microfilament configurations in the canine oocyte
Yong-Xun Jin A , Hyo-Sang Lee B , Xi-Jun Yin B , Xiang-Shun Cui A , Il-Keun Kong B and Nam-Hyung Kim A C
+ Author Affiliations
- Author Affiliations
A Department of Animal Sciences, Chungbuk National University, Cheongju, Chungbuk 361-763, South Korea.
B Department of Animal Sciences and Technology, Sunchon National University, Sunchon, JeonNam, South Korea.
C Corresponding author. Email: nhkim@chungbuk.ac.kr
Reproduction, Fertility and Development 18(8) 849-856 https://doi.org/10.1071/RD06026
Submitted: 22 May 2006 Accepted: 8 August 2006 Published: 22 November 2006
Abstract
In the present study, we observed chromatin, microtubule and microfilament distribution in canine oocytes. The germinal vesicle (GV) chromatin of canine oocytes was classified into four configurations (GV-I, -II, -III and -IV) based on the degree of chromatin separation and condensation. Oocytes recovered from follicular phase ovaries had a greater amount (68%, P < 0.05) of GV-III or GV-IV chromatin than did those from non-follicular phase ovaries (35%). The majority (86.7%) of in vivo ovulated oocytes were at GV-IV. The rates of development to GV breakdown/metaphase I/metaphase II were higher in oocytes recovered from follicular ovaries than from non-follicular ovaries. Immunostaining results revealed cytoplasmic microtubules present in all GV-stage oocytes. Following GV breakdown, microtubular asters were produced from condensed chromatin. The asters appeared to be elongated, and encompassed condensed chromatin particles to form meiotic metaphase chromatin. Microfilaments were located in the cortex and around the GV. During meiotic maturation, a microfilament-rich area, in which the chromatin is allocated, was observed in the oocyte. Our results indicate that oocytes recovered from follicular ovaries were in an advanced stage of GV, and were more competent to complete maturation compared to those from non-follicular phase ovaries. Both microtubules and microfilaments are closely associated with reconstruction of chromatin during meiotic maturation in canine oocytes.
Acknowledgments
This work was supported by The Ministry of Science and Technology (Nano-Bio Program; M10525010001-05N2501-00110 and National Research Laboratory program to N.-H. Kim).
References
Albertini, D. F. (1987). Cytoplasmic reorganization during the resumption of meiosis in cultured preovulatory rat oocytes. Dev. Biol. 120, 121–131.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chohan, K. R. , and Hunter, A. G. (2003). Meiotic competence of bovine fetal oocytes following in vitro maturation. Anim. Reprod. Sci. 76, 43–51.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Crozet, N. , Motlik, J. , and Szollosi, D. (1981). Nucleolar fine structure and RNA synthesis in porcine oocytes during early stages of antrum formation. Biol. Cell. 41, 35–42.
Fair, T. , Hyttel, P. , Greve, T. , and Boland, M. (1996). Nucleus structure and transcriptional activiy in relation to oocyte diameter in cattle. Mol. Reprod. Dev. 43, 503–512.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Hinrichs, K. (1997). Cumulus expansion, chromatin configuration and meiotic competence in horse oocytes: a new hypothesis. Equine Vet. J. Suppl. 25, 43–46.
| PubMed |
Holst, P. A. , and Phemister, R. D. (1975). Temporal sequence of events in the estrous cycle of the bitch. Am. J. Vet. Res. 36, 705–706.
| PubMed |
Howlett, S. K. , Webb, M. , Maro, B. , and Johnson, M. H. (1985). Meiosis II, mitosis I and the linking interphase: A study of the cytoskeleton in the fertilized mouse oocyte. Cytobios 43, 295–305.
| PubMed |
Hyttel, P. , Callesen, H. , and Greve, T. (1989). A comparative ultrastructural study of in vivo versus in vitro fertilization of bovine oocytes. Anat. Embryol. 179, 435–442.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim, M. K. , Fibrianto, Y. H. , Oh, H. J. , Jang, G. , Kim, H. J. , Lee, K. S. , Kang, S. K. , Lee, B. C. , and Hwang, W. S. (2004). Effect of β-mercaptoethanol or epidermal growth factor supplementation on in vitro maturation of canine oocytes collected from dogs with different stages of the estrus cycle. J. Vet. Sci. 5, 253–258.
| PubMed |
Kim, N.-H. , Funahashi, H. , Prather, R. S. , Schatten, G. , and Day, B. N. (1996a). Microtubule and microfilament dynamics in porcine oocytes during meiotic maturation. Mol. Reprod. Dev. 43, 248–255.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim, N.-H. , Moon, S. J. , Prather, R. S. , and Day, B. N. (1996b). Cytoskeletal alteration in aged oocytes and parthenogenesis. Mol. Reprod. Dev. 43, 513–518.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim, N.-H. , Simerly, C. , Funahashi, H. , Schatten, G. , and Day, B. N. (1996c). Microtubule organization in porcine oocytes during fertilization and parthenogenesis. Biol. Reprod. 54, 1397–1404.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kim, N.-H. , Chung, K. S. , and Day, B. N. (1997). The role and distribution of microtubule and microfilaments during fertilization and parthenogenesis. J. Reprod. Fertil. 111, 143–149.
| PubMed |
Kim, N.-H. , Chung, H. M. , Cha, K. Y. , and Chung, K. S. (1998). Microtubule and microfilament organization in maturing human oocytes. Hum. Reprod. 13, 2217–2222.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Kubiac, J. Z. , Weber, M. , Geraud, G. , and Maro, B. (1992). Cell cycle modification during the transition between meiotic M phase in mouse oocytes. J. Cell Sci. 102, 457–467.
| PubMed |
Lee, B. C. , Kim, M. K. , Jang, G. , Oh, H. J. , and Yuda, F. , et al. (2005). Dogs cloned from adult somatic cells. Nature 436, 641.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Li, G. P. , Liu, Y. , Bunch, T. D. , White, K. L. , and Aston, K. I. (2005). Asymmetric division of spindle microtubules and microfilaments during bovine meiosis from metaphase I to metaphase III. Mol. Reprod. Dev. 71, 220–226.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Long, C. R. , Pinto-Correia, C. , Duby, R. T. , Ponce de Leon, F. A. , Boland, M. P. , Roche, J. F. , and Robl, J. M. (1993). Chromatin and microtubule morphology during the first cell cycle in bovine zygotes. Mol. Reprod. Dev. 36, 23–32.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Long, C. R. , Damiani, P. , Pinto-Correia, C. , MacLean, R. A. , Duby, R. T. , and Robl, J. M. (1994). Morphology and subsequent development in culture of bovine oocytes matured in vitro under various conditions of fertilization. J. Reprod. Fertil. 102, 361–369.
| PubMed |
Longo, F. J. , and Chen, D. Y. (1985). Development of cortical polarity in mouse eggs: Involvement of the meiotic apparatus. Dev. Biol. 107, 382–394.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ma, W. , Hou, Y. , Sun, Q. Y. , Sun, X. F. , and Wang, W. H. (2003). Localization of centromere proteins and their association with chromosomes and microtubules during meiotic maturation in pig oocytes. Reproduction 126, 731–738.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maro, B. , Howlett, S. K. , and Webb, M. (1985). Non-spindle microtubule organizing centers in metaphase II-arrested mouse oocytes. J. Cell Biol. 101, 1665–1672.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Maro, B. , Johnson, M. H. , Webb, M. , and Flach, G. (1986). Mechanism of polar body formation in the mouse oocyte: an interaction between the centrosomes, the cytoskeleton and plasma membrane. J. Embryol. Exp. Morphol. 92, 11–32.
| PubMed |
Mattson, B. A. , and Albertini, D. F. (1990). Oogenesis: chromatin and microtubule dynamics during meiotic prophase. Mol. Reprod. Dev. 25, 374–383.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
McGaughey, R. W. , Montgomery, D. H. , and Richter, J. D. (1979). Germinal vesicle configurations and patterns of polypeptide synthesis of porcine oocytes from antral follicles of different size, as related to their competency for spontaneous maturation. J. Exp. Zool. 209, 239–254.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Messinger, S. M. , and Albertini, D. F. (1991). Centrosome and microtubule dynamics during meiotic prophase. Mol. Reprod. Dev. 25, 374–383.
Miyara, F. , Migne, C. , Dumont-Hassan, M. , Le Meur, A. , and Cohen-Bacrie, P. , et al. (2003). Chromatin configuration and transcriptional control in human and mouse oocytes. Mol. Reprod. Dev. 64, 458–470.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Otoi, T. , Fujii, M. , Tanaka, M. , Ooka, A. , and Suzuki, T. (1999). Effect of serum on the in vitro maturation of canine oocytes. Reprod. Fertil. Dev. 11, 387–390.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Otoi, T. , Ooka, A. , Murakami, M. , Karja, N. W. , and Suzuki, T. (2001). Size distribution and meiotic competence of oocytes obtained from bitch ovaries at various stages of the oestrous cycle. Reprod. Fertil. Dev. 13, 151–155.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Petters, R. M. , and Wells, K. D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 61–73.
| PubMed |
Plancha, C. E. , and Albertini, D. F. (1992). Protein synthesis requirements during resumption of meiosis in the hamster oocyte: early nuclear and microtubule configurations. Mol. Reprod. Dev. 33, 324–332.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Reynaud, K. , Fontbonne, A. , Marseloo, N. , Thoumire, S. , Chebrout, M. , de Lesegno, C. V. , and Chastant-Maillard, S. (2005). In vivo meiotic resumption, fertilization and early embryonic development in the bitch. Reproduction 130, 193–201.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Rime, H. , Jessus, C. , and Ozon, R. (1987). Distribution of microtubules during the first meiotic cell division in the mouse oocyte: Effect of taxol. Gamete Res. 17, 1–13.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Saint-Dizier, M. , Renard, J. P. , and Chastant-Maillard, S. (2001). Induction of final maturation by sperm penetration in canine oocytes. Reproduction 121, 97–105.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Simerly, C. , and Schatten, G. (1993). Techniques for localization of specific molecules in oocytes and embryos. Method. Emzymol. 225, 516–552.
Sirard, M. A. , Coenan, K. , and Bilodeau, S. (1992). Effects of fresh or cultured follicular fractions on meiotic resumption in bovine oocytes. Theriogenology 37, 39–57.
| Crossref | GoogleScholarGoogle Scholar |
Sun, Q. Y. , and Schatten, H. (2006). Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 131, 193–205.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Sun, Q. Y. , Lai, L. , Park, K. W. , Kuhholzer, B. , Prather, R. S. , and Schatten, H. (2001). Dynamic events are differently mediated by microfilaments, microtubules, and mitogen-activated protein kinase during porcine oocyte maturation and fertilization in vitro. Biol. Reprod. 64, 879–889.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Verlhac, M. H. , Kubiac, J. Z. , Clarke, H. J. , and Maro, B. (1994). Microtubules and chromatin behavior follow MAP kinase activity but not MPF activity during meiosis in mouse oocytes. Development 120, 1017–1025.
| PubMed |
Webb, M. , Howletts, K. , and Maro, B. (1986). Parthenogenesis and cytoskeleton organization in aging mouse eggs. J. Embryol. Exp. Morphol. 95, 131–145.
| PubMed |
Yamada, S. , Shimiza, Y. , Kawano, Y. , Nakazawa, M. , Naito, K. , and Toyoda, Y. (1993). In vitro maturation and fertilization of preovulatory dog oocytes. J. Reprod. Fertil. Suppl. 47, 227–229.
| PubMed |
Ye, J. , Flint, A. P. , Campbell, K. H. , and Luck, M. R. (2002). Synchronization of porcine oocyte meiosis using cycloheximide and its application to the study of regulation by cumulus cells. Reprod. Fertil. Dev. 14, 433–442.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zernicka-Goetz, M. , Kubiak, J. Z. , Antony, C. , and Maro, B. (1993). Cytoskeletal organization of rat oocytes during metaphase II arrest and following abortive activation: a study by confocal laser scanning microscopy. Mol. Reprod. Dev. 35, 165–175.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Zuccotti, M. , Piccinelli, A. , Giorgi, R. P. , Garagna, S. , and Redi, C. A. (1995). Chromatin organization during mouse oocyte growth. Mol. Reprod. Dev. 41, 479–485.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
