Skip to main content Accessibility help
×
Home
Hostname: page-component-8bbf57454-jcfbx Total loading time: 0.197 Render date: 2022-01-22T09:48:45.518Z Has data issue: true Feature Flags: { "shouldUseShareProductTool": true, "shouldUseHypothesis": true, "isUnsiloEnabled": true, "metricsAbstractViews": false, "figures": true, "newCiteModal": false, "newCitedByModal": true, "newEcommerce": true, "newUsageEvents": true }

Article contents

Effect of nucleocytoplasmic ratio on the in vitro porcine embryo development after in vitro fertilization or parthenogenetic activation

Published online by Cambridge University Press:  06 October 2021

Nguyen Thi Men
Affiliation:
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8602, Japan
Thanh Quang Dang-Nguyen*
Affiliation:
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8602, Japan
Tamas Somfai
Affiliation:
Institute of Livestock and Grassland Science, NARO, Ibaraki 305-0901, Japan
Hiep Thi Nguyen
Affiliation:
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8602, Japan Institute of Biotechnology, Vietnam Academy of Science and Technology, Hanoi, Vietnam The United Graduate School of Veterinary Science, Yamaguchi University, Yamaguchi 753-8515 Japan
Junko Noguchi
Affiliation:
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8602, Japan
Hiroyuki Kaneko
Affiliation:
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8602, Japan
Kazuhiro Kikuchi
Affiliation:
Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305-8602, Japan The United Graduate School of Veterinary Science, Yamaguchi University, Yamaguchi 753-8515 Japan
*
Author for correspondence: T. Q. Dang-Nguyen. Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), Ibaraki 305–8602, Japan. E-mail: adipy36@affrc.go.jp

Summary

This study was conducted to examine whether the nuclear to cytoplasmic (N/C) ratio had any influence on the timing of embryo compaction and blastocoel formation, as well as formation rate and quality of blastocyst. First, we produced embryos with increased N/C ratio by removal of approximately one-third of the cytoplasm and with decreased N/C ratio by doubling the oocyte cytoplasm with an enucleated oocyte. The initiation of compaction and cavitation in reduced cytoplasm group was significantly earlier (P < 0.05) compared with the control and doubled cytoplasm groups. The rate of blastocysts in the reduced cytoplasm and doubled cytoplasm groups was significantly lower (P < 0.05) compared with the control group. Blastocyst quality in terms of total cell number in the reduced cytoplasm group was significantly lower (P < 0.05) compared with the doubled cytoplasm group, but not different from the control group. Next, we produced embryos with various N/C ratios by oocyte fusion combined with cytochalasin D treatment. The onset of compaction and cavitation in the 2N/2C group (decreased N/C ratio) was significantly delayed (P < 0.05) or had the tendency to be delayed (P = 0.064), respectively, compared with the control group (2N/1C). A significantly higher rate of blastocyst was observed in the 4N/2C group compared with the 1N/1C group (P < 0.05) but not different from the remaining groups. These results demonstrated that an increase in N/C ratio caused an earlier occurrence of morula compaction and blastocyst formation in both in vitro fertilization (IVF) and parthenogenetically activated pig embryos.

Type
Research Article
Copyright
© The Author(s), 2021. Published by Cambridge University Press

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.)

References

Barton, SH and Surani, MAH (1983). Microdissection of mouse egg. Exp. Cell Res 146, 187–91.CrossRefGoogle ScholarPubMed
Dang-Nguyen, TQ, Hiep, NT, Somfai, T, David, W, Men, NT, Viet-Linh, N, Noguchi, J, Kaneko, H, Kikuchi, K and Nagai, T (2018). Sucrose assists selection of high-quality oocytes in pigs. Anim Sci J 89, 880–7.CrossRefGoogle ScholarPubMed
Evsikov, SV, Morozoval, M and Solomko, AP (1990). The role of the nucleocytoplasmic ratio in development regulation of the early mouse embryo. Development 109, 323–8.CrossRefGoogle ScholarPubMed
Han, YM, Wang, WH, Abeydeera, LR, Petersen, AL, Kim, JH, Murphy, C, Day, BN and Prather, RS (1999). Pronuclear location before the first cell division determines ploidy of polyspermic pig embryos. Biol Reprod 61, 1340–6.CrossRefGoogle ScholarPubMed
Hardarson, T, Hanson, C, Sjögren, A and Lundin, K (2001). Human embryos with unevenly sized blastomeres have lower pregnancy and implantation rates: indications for aneuploidy and multinucleation. Hum Reprod 16, 313–8.CrossRefGoogle ScholarPubMed
He, W, Kong, Q, Shi, Y, Xie, B, Jiao, M, Huang, T, Guo, S, Hu, K and Liu, Z (2013). Generation and developmental characteristics of porcine tetraploid embryos and tetraploid/diploid chimeric embryos. Genomics Proteomics Bioinformatics 11, 327–33.CrossRefGoogle ScholarPubMed
Iwasaki, S, Kono, T, Fukatsu, H and Nakahara, T (1989). Production of bovine tetraploid embryos by electrofusion and their developmental capability in vitro . Gamete Res 24, 261–7.CrossRefGoogle ScholarPubMed
Kaufman, MH and Sachs, L (1976). Complete preimplantation development in culture of parthenogenetic mouse embryos. J Embryol Exp Morphol 35, 179–90.Google ScholarPubMed
Kaufman, MH and Webb, S (1990). Postimplantation development of tetraploid mouse embryos produced by electrofusion. Development 110, 1121–32.CrossRefGoogle ScholarPubMed
Kikuchi, K, Onishi, A, Kashiwazaki, N, Iwamoto, M, Noguchi, J, Kaneko, H, Akita, T and Nagai, T (2002). Successful piglet production after transfer of blastocysts produced by a modified in vitro system. Biol Reprod 66, 1033–41.CrossRefGoogle ScholarPubMed
Kim, J, Kim, SH and Jun, JH (2017). Prediction of blastocyst development and implantation potential in utero based on the third cleavage and compaction times in mouse pre-implantation embryos. J Reprod Dev 63, 117–25.CrossRefGoogle ScholarPubMed
Koizumi, N and Fukuta, K (1995). Preimplantation development of tetraploid mouse embryos produced by cytochalasin B. Exp Anim 44, 105–9.CrossRefGoogle ScholarPubMed
Kubiak, JZ and Tarkowski, AK (1985). Electrofusion of mouse blastomeres. Exp Cell Res 157, 561–6.CrossRefGoogle ScholarPubMed
Marcos, J, Pérez-Albalá, S, Mifsud, A, Molla, M, Landeras, J and Meseguer, M (2015). Collapse of blastocysts is strongly related to lower implantation success: a time-lapse study. Hum Reprod 30, 2501–8.CrossRefGoogle ScholarPubMed
Men, NT, Kikuchi, K, Nakai, M, Fukuda, A, Tanihara, F, Noguchi, J, Kaneko, H, Linh, NV, Nguyen, BX, Nagai, T and Tajima, A (2013). Effect of trehalose on DNA integrity of freeze-dried boar sperm, fertilization, and embryo development after intracytoplasmic sperm injection. Theriogenology 80, 1033–44.CrossRefGoogle ScholarPubMed
Mita, I (1983). Studies on factors affecting the timing of early morphogenetic events during starfish embryogenesis. J Exp Zool 225, 293–9.CrossRefGoogle Scholar
Nakai, M, Kashiwazaski, N, Takizawa, A, Hayashi, Y, Nakatsukasa, E, Fuchimoto, D, Noguchi, Kaneko, Shino, M and Kikuchi, K(2003). Viable piglets generated from porcine oocytes matured in vitro and fertilized by intracytoplasmic sperm head injection. Biol Reprod 68, 1003–8.CrossRefGoogle ScholarPubMed
Novakova, L, Kovacovicova, K, Dang Nguyen, TQ, Sodek, M, Skuultety, M and Anger, M (2016). A balance between nuclear and cytoplasmic volumes controls spindle length. PLoS One 11, e0149535.CrossRefGoogle ScholarPubMed
Petters, RM and Wells, KD (1993). Culture of pig embryos. J Reprod Fertil Suppl 48, 6173.Google ScholarPubMed
Sembon, S, Fuchimoto, D, Iwamoto, M, Suzuki, S, Yoshioka, K and Onishi, A (2011). A simple method for producing tetraploid porcine parthenogenetic embryos. Theriogenology 76, 598606.CrossRefGoogle Scholar
Skiadas, CC, Jackson, KV and Racowsky, C (2006). Early compaction on day 3 may be associated with increased implantation potential. Fertil Steril 86, 1386–91.CrossRefGoogle ScholarPubMed
Snow, MH (1975). Embryonic development of tetraploid mice during the second half of gestation. J Embryol Exp Morph 34, 707–21.Google ScholarPubMed
Somfai, T, Ozawa, M, Noguchi, J, Kaneko, H, Ohnuma, K, Karja, NW, Fahrudin, M, Maedomari, N, Dinnyés, A, Nagai, T and Kikuchi, K (2006). Diploid porcine parthenotes produced by inhibition of first polar body extrusion during in vitro maturation of follicular oocytes. Reproduction 132, 559–70.CrossRefGoogle ScholarPubMed
Somfai, T, Inaba, Y, Aikawa, Y, Ohtake, M, Kobayashi, S, Konishi, K and Imai, K (2010). Relationship between the length of cell cycles, cleavage pattern and developmental competence in bovine embryos generated by in vitro fertilization or parthenogenesis. J Reprod Dev 56, 200–7.CrossRefGoogle ScholarPubMed
Somfai, T, Yoshioka, K, Tanihara, F, Kaneko, H, Noguchi, J, Kashiwazaki, N, Nagai, T and Kikuchi, K (2014). Generation of live piglets from cryopreserved oocytes for the first time using a defined system for in vitro embryo production. PLoS One 9, e97731.CrossRefGoogle ScholarPubMed
Sugimura, S, Akai, T, Somfai, T, Hirayama, M, Aikawa, Y, Ohtake, M, Hattori, H, Kobayashi, S, Hashiyada, Y, Konishi, K and Imai, K (2010). Time-lapse cinematography-compatible polystyrene-based microwell culture system: a novel tool for tracking the development of individual bovine embryos. Biol Reprod 83, 970–8.CrossRefGoogle ScholarPubMed
Sugimura, S, Akai, T and Imai, K (2017). Selection of viable in vitro-fertilized bovine embryos using time-lapse monitoring in micro-well culture dishes. J Reprod Dev 63, 353–7.CrossRefGoogle Scholar
Suzuki, K, Asano, A, Eriksson, B, Niwa, K, Nagai, T and Rodriguez-Martinez, H (2002). Capacitation status and in vitro fertility of boar spermatozoa: effects of seminal plasma, cumulus–oocyte-complexes-conditioned medium and hyaluronan. Int J Androl 25, 8493.CrossRefGoogle ScholarPubMed
Tao, J, Tamis, R, Fink, K, Williams, B, Nelson-White, T and Craig, R (2002). The neglected morula/compact stage embryo transfer. Hum Reprod 17, 1513–8.CrossRefGoogle ScholarPubMed
Tsichlaki, E and FitzHarris, G (2016). Nucleus downscaling in mouse embryos is regulated by cooperative developmental and geometric programs. Sci Rep 6, 28040.CrossRefGoogle ScholarPubMed
Wakayama, T and Yanagimachi, R (1998). Fertilisability and developmental ability of mouse oocytes with reduced amounts of cytoplasm. Zygote 6, 341–6.CrossRefGoogle ScholarPubMed
Wakayama, S, Kishigami, S, Nguyen, VT, Ohta, H, Hikichi, T, Mizutani, E, Bui, HT, Miyake, M and Wakayama, T (2008). Effect of volume of oocyte cytoplasm on embryo development after parthenogenetic activation, intracytoplasmic sperm injection, or somatic cell nuclear transfer. Zygote 16, 211–22.Google Scholar
Wu, GM, Lai, L, Mao, J, McCauley, TC, Caamaño, JN, Cantley, T, Rieke, A, Murphy, CN, Prather, RS, Didion, BA and Day, BN (2004). Birth of piglets by in vitro fertilization of zona-free porcine oocytes. Theriogenology 62, 1544–56.CrossRefGoogle ScholarPubMed

Send article to Kindle

To send this article to your Kindle, first ensure no-reply@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about sending to your Kindle. Find out more about sending to your Kindle.

Note you can select to send to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be sent to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Effect of nucleocytoplasmic ratio on the in vitro porcine embryo development after in vitro fertilization or parthenogenetic activation
Available formats
×

Send article to Dropbox

To send this article to your Dropbox account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Dropbox.

Effect of nucleocytoplasmic ratio on the in vitro porcine embryo development after in vitro fertilization or parthenogenetic activation
Available formats
×

Send article to Google Drive

To send this article to your Google Drive account, please select one or more formats and confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your <service> account. Find out more about sending content to Google Drive.

Effect of nucleocytoplasmic ratio on the in vitro porcine embryo development after in vitro fertilization or parthenogenetic activation
Available formats
×
×

Reply to: Submit a response

Please enter your response.

Your details

Please enter a valid email address.

Conflicting interests

Do you have any conflicting interests? *