Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-23T16:45:07.067Z Has data issue: false hasContentIssue false
  • English
  • Français

Somatic cell nuclear transfer using transported in vitro-matured oocytes in cynomolgus monkey

Published online by Cambridge University Press:  01 February 2007

N. Chen ,
S-L. Liow ,
R. Bin Abdullah ,
WK. Khadijah Wan Embong ,
W-Y. Yip ,
L-G. Tan ,
G-Q. Tong  and
S-C. Ng
N. Chen
Affiliation:
Embryonics International, Gleneagles Hospital, Singapore 258500, Singapore.
S-L. Liow
Affiliation:
Embryonics International, Gleneagles Hospital, Singapore 258500, Singapore.
R. Bin Abdullah
Affiliation:
Department of Biological Sciences, University of Malaya, Kuala Lumpur 50603, Malaysia.
WK. Khadijah Wan Embong
Affiliation:
Department of Biological Sciences, University of Malaya, Kuala Lumpur 50603, Malaysia.
W-Y. Yip
Affiliation:
Embryonics International, Gleneagles Hospital, Singapore 258500, Singapore.
L-G. Tan
Affiliation:
Department of Obstetrics & Gynaecology, National University of Singapore, Singapore 119074, Singapore.
G-Q. Tong
Affiliation:
Department of Obstetrics & Gynaecology, National University of Singapore, Singapore 119074, Singapore.
S-C. Ng*
Affiliation:
Embryonics International, Gleneagles Hospital, Singapore 258500, Singapore. Department of Obstetrics & Gynaecology, National University of Singapore, Singapore 119074, Singapore.
*
All correspondence to: S-C. Ng, Gleneagles Hospital, Annex Block, #01–38, 6A Napier Road, Singapore 258500, Singapore. Tel: +65 6479 7267. Fax: +65 6479 6536. e-mail: scng@embryonics.biz
Get access Rights & Permissions [Opens in a new window]

Summary

Somatic cell nuclear transfer (SCNT) is not successful so far in non-human primates. The objective of this study was to investigate the effects of stimulation cycles (first and repeat) on oocyte retrieval and in vitro maturation (IVM) and to evaluate the effects of stimulation cycles and donor cell type (cumulus and fetal skin fibroblasts) on efficiency of SCNT with transported IVM oocytes. In this study, 369 immature oocytes were collected laparoscopically at 24 h following human chorionic gonadotrophin (hCG) treatment from 12 cynomolgus macaque (Macaca fascicularis) in 24 stimulation cycles, and shipped in pre-equilibrated IVM medium for a 5 h journey, placed in a dry portable incubator (37 °C) without CO2 supplement. A total of 70.6% (247/350) of immature oocytes reached metaphase II (MII) stage at 36 h after hCG administration, MII spindle could be seen clearly in 80.6% (104/129) of matured IVM oocytes under polarized microscopy. A total of 50.0% (37/74) of reconstructive SCNT embryos cleaved after activation; after cleavage, 37.8% (14/37) developed to the 8-cell stage and 8.1% (3/37) developed to morula, but unfortunately none developed to the blastocyst stage. Many more oocytes could be retrieved per cycle from monkeys in the first cycle than in repeated cycles (19.1 vs. 11.7, p < 0.05). There were no significant differences in the maturation rate (70.0 vs. 71.4%, p > 0.05) and MII spindle rate under polarized microscopy (76.4 vs. 86.0%, p > 0.05) between the first and repeat cycles. There were also no significant differences in the cleavage rate, and the 4-cell, 8-cell and morula development rate of SCNT embryos between the first and repeat cycles. When fibroblast cells and cumulus cells were used as the donor cells for SCNT, first cleavage rate was not significantly different, but 4-cell (50.0 vs. 88.9%, p < 0.05) and 8-cell (0 vs. 51.9%, p < 0.01) development rate were significantly lower for the former. In conclusion, the number of stimulation cycles has a significant effect on oocyte retrieval, but has no effect on maturation and SCNT embryo development; however, different donor cell types (cumulus and fibroblast) resulted in different developmental potentials of SCNT embryos.

Keywords

CloningIn vitro maturationMonkeyNuclear transferOocytesTransport
Type
Research Article
Information
Zygote , Volume 15 , Issue 1 , February 2007 , pp. 25 - 33
Copyright
Copyright © Cambridge University Press 2007

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

Arat, S., Rzucidlo, S.J., Gibbons, J., Miyoshi, K. & Stice, S.L. (2001). Production of transgenic bovine embryos by transfer of transfected granulosa cells into enucleated oocytes. Mol. Reprod. Dev. 60, 20–6.CrossRefGoogle ScholarPubMed
Baguisi, A. & Overstrom, E.W. (2000). Induced enucleation in nuclear transfer procedures to produce cloned animals. Theriogenology 53, 209.Google Scholar
Baguisi, A., Behboodi, E., Melican, D.T., Pollock, J.S., Destrempes, M.M., Cammuso, C., Williams, J.L., Nims, S.D., Porter, C.A., Midura, P., Palacios, M.J., Ayres, S.L., Denniston, R.S., Hayes, M.L., Ziomek, C.A., Meade, H.M., Godke, R.A., Gavin, W.G., Overstrom, E.W. & Echelard, Y. (1999). Production of goats by somatic cell nuclear transfer. Nat. Biotechnol. 17, 456–61.CrossRefGoogle ScholarPubMed
Bavister, B.D., Dees, C. & Schultz, R.D. (1986). Refractoriness of rhesus monkeys to repeated ovarian stimulation by exogenous gonadotropins is caused by onoprecipitating antibodies. Am. J. Reprod. Immunol. Microbiol. 11, 11–6.CrossRefGoogle ScholarPubMed
Betthauser, J., Forsberg, E., Augenstein, M., Childs, L., Eilertsen, K., Enos, J., Forsythe, T., Golueke, P., Jurgella, G., Koppang, R., Lesmeister, T., Mallon, K., Mell, G., Misica, P., Pace, M., Pfister-Genskow, M., Strelchenko, N., Voelker, G., Watt, S., Thompson, S. & Bishop, M. (2000). Production of cloned pigs from in vitro systems. Nat. Biotechnol. 18, 1055–9.CrossRefGoogle ScholarPubMed
Bordignon, V. & Smith, L.C. (1998). Telophase enucleation: an improved method to prepare recipient cytoplasts for use in bovine nuclear transfer. Mol. Reprod. Dev. 49, 29–36.3.0.CO;2-Q>CrossRefGoogle ScholarPubMed
Caligara, C., Navarro, J., Vargas, G., Simon, C., Pellicer, A. & Remohi, J. (2001). The effect of repeated controlled ovarian stimulation in donors. Hum. Reprod. 16, 2320–3.CrossRefGoogle ScholarPubMed
Campbell, K.H.S. (1999). Nuclear transfer in farm animal species. Semin. Cell Dev. Biol. 10, 245–52.CrossRefGoogle ScholarPubMed
Campbell, K.H.S., McWhir, J., Ritchie, W.A. & Wilmut, I. (1996). Sheep cloned by nuclear transfer from a cultured cell line. Nature 380, 64–6.CrossRefGoogle ScholarPubMed
Chen, N.Q., Liow, S.L., Yip, W.Y., Tan, L.G. & Ng, S.C. (2005). Influence of cysteamine supplementation and culture in portable dry-incubator on the IVM, fertilization and subsequent development of mouse oocytes. Theriogenology 63, 2300–10.CrossRefGoogle ScholarPubMed
Chen, N.Q., Liow, S.L., Abdullah, R.B., Wan Khadijah, W.E., Yip, W.Y., Tan, L.G., Tong, G.Q. & Ng, S.C. (2006). Developmental competence of transported in vitro-matured macaque oocytes. Reprod. BioMed. Online 12, 50–9.CrossRefGoogle ScholarPubMed
Cibelli, J.B., Stice, S.L., Golueke, P.J., Kane, J.J., Jerry, J., Blackwell, C., León, A.P. & Robl, J.M. (1998). Cloned transgenic calves produced from non-quiescent fetal fibroblasts. Science 280, 1256–8.CrossRefGoogle Scholar
Combelles, C.M. & Albertini, D.F. (2003). Assessment of oocyte quality following repeated gonadotropin stimulation in the mouse. Biol. Reprod. 68, 812–21.CrossRefGoogle ScholarPubMed
Dannyes, A., De Sousa, P., King, T. & Wilmut, I. (2002). Somatic cell nuclear transfer: Recent progress and challenges. Cloning Stem Cells 4, 81–90.CrossRefGoogle Scholar
De Sousa, P.A., Dobrinsky, J.R., Zhu, J., Archibald, A.L., Ainslie, A., Bosma, W., Bowering, J., Bracken, J., Ferrier, P.W., Fletcher, J., Gasparrini, B., Harkness, L., Johnston, P., Ritchie, M., Ritchie, W.A., Travers, A., Albertini, D., Dinnyes, A., King, T.J. & Wilmut, I. (2002). Somatic cell nuclear transfer in pig: control of pronuclear formation and integration with improved methods for activation and maintenance of pregnancy. Biol. Reprod. 66, 642–50.CrossRefGoogle ScholarPubMed
Gao, S., Chung, Y.G., William, J.W., Riley, J., Moley, K. & Latham, K.E. (2003a). Somatic cell-like features of cloned mouse embryos prepared with cultured myoblast nuclei. Biol. Reprod. 69, 48–56.CrossRefGoogle ScholarPubMed
Gao, S.R., McGarry, M., Ferrier, T., Pallante, B., Gasparrini, B., Fletcher, J., Harkness, L., De Sousa, P., McWhir, J. & Wilmut, I. (2003b). Effect of cell confluence on production of cloned mice using an inbred embryonic stem cell line. Biol. Reprod. 68, 595–603.CrossRefGoogle ScholarPubMed
Hochedlinger, K. & Jaenisch, R. (2002). Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 415, 1035–8.CrossRefGoogle ScholarPubMed
Humpherys, D., Eggan, K., Akitsu, H., Hochedlinger, K., Rideout, W.M., Biniszkiewics, D., Yanagimachi, R. & Jaenish, R. (2001). Epignetic instability in ES cells and cloned mice. Science 293, 95–7.CrossRefGoogle Scholar
Hyun, S.H., Lee, G.S., Kim, D.Y., Kim, H.S., Lee, S.H., Kim, S., Lee, E.S., Lim, J.M., Kang, S.K., Lee, B.C. & Hwang, W.S. (2003). Effect of maturation media and oocytes derived from sows or gilts on the development of cloned pig embryos. Therigenology 59, 1641–9.CrossRefGoogle ScholarPubMed
Iliff, S.A., Molskness, T.A. & Stouffer, R.L. (1995). Anti-human gonadotropin antibodies generated during in vitro fertilization (IVF)-related cycles: effect on fertility of rhesus macaques. J. Med. Primatol. 24, 7–11.CrossRefGoogle ScholarPubMed
Inoue, K., Ogonuki, N., Mochida, K., Yamamoto, Y., Takano, K., Kohto, T., Ishino, F. & Ogura, A. (2003). Effects of donor cell type and genotype on the efficiency of mouse somatic cell cloning. Biol. Reprod. 69, 1394–400.CrossRefGoogle ScholarPubMed
Jain, A., Robins, J.C., Williams, D.B. & Thomas, M.A. (2005). The effect of multiple cycles in oocyte donors. Am. J. Obstet. Gynecol. 192, 1382–4.CrossRefGoogle ScholarPubMed
Kasinathan, P., Knott, J.G., Wang, Z., Jerry, D.J. & Robl, J.M. (2001). Production of calves from G1 fibroblasts. Nature Biotechnol. 19, 1176–8.CrossRefGoogle ScholarPubMed
Keefer, C.L., Baldassarre, H., Keyston, R., Wang, B., Bhatia, B., Bilodeau, A.S., Zhou, J.F., Leduc, M., Downey, B.R., Lazaris, A. & Karatzas, C.N. (2001). Generation of dwarf goat (Capra hircus) clones following nuclear transfer with transfected and nontransfected fetal fibroblasts and in vitro-matured oocytes. Biol. Reprod. 64, 849–56.CrossRefGoogle ScholarPubMed
Kühholzer, B., Hawley, T.J., Lai, L., Kolber-Simonds, D. & Prather, R.S. (2001). Clonal lines of transgenic fibroblast cells derived from the same fetus result in different development when used for nuclear transfer in pigs. Biol. Reprod. 64, 1695–8.CrossRefGoogle ScholarPubMed
Kurosaka, S., Nagao, Y., Minami, N., Yamada, M. & Imai, H. (2002). Dependence of DNA synthesis and in vitro development of bovine nuclear transfer embryos on the stage of the cell cycle of donor cells and recipient cytoplasts. Biol. Reprod. 67, 643–7.CrossRefGoogle ScholarPubMed
Lanzendorf, Z.E., Zelinski-Wooten, M.B., Stouffer, R.L. & Wolf, D.P. (1990). Maturity at collection and the developmental potential of rhesus monkey oocytes. Biol. Reprod. 42, 703–11.CrossRefGoogle ScholarPubMed
Li, L.Y., Connelly, M.C., Wetmore, C., Curran, T. & Morgan, J.I. (2003). Mouse embryos cloned from brain tumors. Cancer Research 63, 2733–6.Google ScholarPubMed
Liow, S.L., Martelli, B., Chen, N.Q., Yip, W.Y., Tan, L.G., Martelli, P., Oh, S.H., Oh, S. & Ng, S.C. (2002). Ovarian response to gonadotropin stimulation in the cynomolgus monkey, Macaca fascicularis. The Second International Symposium on Assisted Reproductive Technology (ART) for the Conservation and Genetic Management of Wildlife, 28–29 September, Omaha, Nebraska, USA.Google Scholar
Mitalipov, S.M., Yeoman, R.R., Nusser, K.D. & Wolf, D.P. (2002). Rhesus monkey embryos produced by nuclear transfer from embryonic blastomeres or somatic cells. Biol. Reprod. 66, 1367–73.CrossRefGoogle ScholarPubMed
Miyoshi, K., Rzucidlo, S.J., Gibbons, J.R., Arat, S. & Stice, S.L. (2001). Development of porcine embryos reconstituted with somatic cells and enucleated metaphase I and II oocytes matured in a protein-free medium. BMC Dev. Biol. 1, 12.CrossRefGoogle Scholar
Miyoshi, K., Rzucidlo, S.J., Pratt, S.L. & Stice, S.L. (2003). Improvements in cloning efficiencies may be possible by increasing uniformity in recipient oocytes and donor cells. Biol. Reprod. 68, 1079–86.CrossRefGoogle ScholarPubMed
Ng, S.C., Martelli, P., Liow, S.L., Herbert, S. & Oh, S.H. (2002). Intracytoplasmic injection of frozen-thawed epididymal spermatozoa in a nonhuman primate model, the cynomolgus monkey (Macaca fascicularis). Theriogenology 58, 1385–97.CrossRefGoogle Scholar
Ng, S.C., Chen, N.Q., Yip, W.Y., Liow, S.L., Tong, G.Q., Martelli, B., Tan, L.G. & Martelli, P. (2004). The first cell cycle after transfer of somatic cell nuclei in a non-human primate. Development 131, 2475–84.CrossRefGoogle Scholar
Oback, B. & Wells, D. (2002). Donor cells for cloning: many are called but few are chosen. Cloning Stem Cells 4, 147–69.CrossRefGoogle ScholarPubMed
Ono, Y., Shimozawa, N., Ito, M. & Kono, T. (2001). Cloned mice from fetal fibroblast cells arrested at metaphase by a serial nuclear transfer. Biol. Reprod. 64, 44–50.CrossRefGoogle ScholarPubMed
Ottobre, J.S. & Stouffer, R.L. (1985). Antibody production in rhesus monkeys following prolonged administration of human chorionic gonadotropins. Fertil. Steril. 33, 151–7.Google Scholar
Powell, A.M., Talbot, N.C., Wells, K.D., Kerr, D.E., Pursel, V.G. & Wall, R.J. (2004). Cell donor influences success of producing cattle by somatic cell nuclear transfer. Biol. Reprod. 71, 210–6.CrossRefGoogle ScholarPubMed
Renard, J.P., Zhou, Q., LeBourhis, D., Chavatte-Palmer, P., Hue, I., Heyman, Y. & Vignon, X. (2002). Nuclear transfer technologies: between successes and doubts. Theriogenology 57, 203–22.CrossRefGoogle ScholarPubMed
Schramm, R.D. & Bavister, B.D. (1999). A macaque model for studying mechanisms controlling oocyte development and maturation in human and non-human primates. Hum. Reprod. 14, 2544–55.CrossRefGoogle ScholarPubMed
Schuetz, A.W., Whittingham, D.G. & Snowden, R. (1996). Alteration in the cell cycle of mouse cumulus granulusa cells during expansion and magnification in vivo and in vitro. Reprod. Fertil. Dev. 8, 935–43.CrossRefGoogle Scholar
VandeVoort, C.A., Baughman, W.L. & Stouffer, R.L. (1989). Comparison of different regimens of human gonadotropins for superovulation of rhesus monkeys: ovulatory response and subsequent luteal function. J. In Vitro Fertil. Embryo Transfer 6, 85–91.CrossRefGoogle ScholarPubMed
VandeVoort, C.A., Leibo, S.P. & Tarantal, A.F. (2003). Improved collection and developmental competence of immature macaque oocytes. Theriogenology 59, 699–707.CrossRefGoogle ScholarPubMed
Vignon, X., Chesne, P., Le Bourhis, D., Flechon, J.E., Heyman, Y. & Renard, J.P. (1998). Developmental potential of bovine embryos reconstructed from enucleated matured oocytes fused with cultured somatic cells. C R Acad. Sci. III 321, 735–45.CrossRefGoogle ScholarPubMed
Wakayama, T., Rodriguez, I., Perry, A.C., Yanagimachi, R. & Mombaerts, P. (1999). Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 14984–9.CrossRefGoogle ScholarPubMed
Wells, D.N., Misica, P.M., Day, T.A. & Tervit, H.R. (1997). Production of cloned lambs from an established embryonic cell line: a comparison between in vivo- and in vitro-matured cytoplasts. Biol. Reprod. 57, 385–93.CrossRefGoogle ScholarPubMed
Wells, D.N., Pavla, P.M., Tervit, H.R. & Vivanco, W.H. (1998a). Adult somatic cell nuclear transfer is used to preserve the last surviving cow of the Enderby Island cattle breed. Reprod. Fertil. Dev. 10, 369–78.CrossRefGoogle ScholarPubMed
Wells, D.N., Misica, P.M., Day, A.M., Peterson, A.J. & Tervit, H.R. (1998b). Cloning sheep from cultured embryonic cells. Reprod. Fertil. Dev. 10, 615–26.CrossRefGoogle ScholarPubMed
Wells, D., Oliver, J., Miller, A., Forsyth, J., Berg, M. & Cockrem, K. (2001). Bovine cells selected in G1 of the cell cycle are totipotent following somatic cell nuclear transfer. In Proc. 32nd Ann. Conf. Soc. Reprod. Biol. Abstract No. 25.Google Scholar
Wells, D.N., Laible, G., Tucker, F.C., Miller, A.L., Oliver, J.E., Xiang, T., Forsyth, J.T., Berg, M.C., Cockrem, K., L'Huillier, P.J., Tervit, H.R. & Oback, B. (2003). Coordination between donor cell type and cell cycle stage improves nuclear cloning efficiency in cattle. Theriogenology 59, 45–59.CrossRefGoogle ScholarPubMed
Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J. & Campbell, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810–3.CrossRefGoogle ScholarPubMed
Wolf, D.P., Vandevoort, C.A., Meyer-Haas, G.R., Zelinski-Wooten, M.B., Hess, D.L., Baughman, W.L. & Stouffer, R.L. (1989). In vitro fertilization and embryo transfer in rhesus monkeys. Biol. Reprod. 41, 335–46.CrossRefGoogle Scholar
Wolf, D.P., Alexander, M., Zelinski-Wooten, M. & Stouffer, R.L. (1996). Maturity and fertility of rhesus monkey oocytes collected at different intervals after an ovulatory stimulus (human chorionic gonadotrophin) in in vitro fertilized cycles. Mol. Reprod. Dev. 43, 76–81.3.0.CO;2-2>CrossRefGoogle ScholarPubMed
Wolf, D.P., Meng, L., Ouhibi, O. & Zelinski-Wooten, M. (1999). Nuclear transfer in the rhesus monkey: practical and basic implications. Biol. Reprod. 60, 199–204.CrossRefGoogle ScholarPubMed
Wakayama, T., Rodriguez, I., Perry, A.C.F., Yanagimachi, R. & Mombaerts, P. (1999). Mice cloned from embryonic stem cells. Proc. Natl. Acad. Sci. USA 96, 14984–9.CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (2001a). Mouse cloning with nucleus donor cells of different age and type. Mol. Reprod. Dev. 58, 376–83.3.0.CO;2-L>CrossRefGoogle ScholarPubMed
Wakayama, T. & Yanagimachi, R. (2001b). Effect of cytokinesis inhibitors, DMSO and the timing of oocyte activation on mouse cloning using cumulus cell nuclei. Reproduction 122, 49–60.CrossRefGoogle ScholarPubMed
Zawada, W.M., Cibelli, J.B., Choi, P.K., Clarkson, E.D., Golueke, P.J., Witta, S.E., Bell, K.P., Kane, J., Ponce de Leon, F.A., Jerry, D.J. & Robl, J.M. (1998). Somatic cell cloned transgenic bovine neurons for transplantation in parkinsonian rats. Nat. Med. 4, 569–74.CrossRefGoogle ScholarPubMed
Zelinski-Wooten, M.B., Alexander, M., Molskness, T.A., Stouffer, R.L. & Wolf, D.P. (1996). Use of recombinant human gonadotropins for repeated follicular stimulation in rhesus monkeys. In Proceedings of the XIXth conference Am. Soc. Primate. Abstract No. 133.Google Scholar
Zhou, Q., Jouneau, A., Brochard, V., Adenot, P. & Renard, J.P. (2001). Developmental potential of mouse embryos reconstructed from metaphase embryonic stem cell nuclei. Biol. Reprod. 65, 412–9.CrossRefGoogle ScholarPubMed