Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-29T15:08:04.415Z Has data issue: false hasContentIssue false
  • English
  • Français

Bovine somatic cell nuclear transfer using mitomycin C-mediated chemical oocyte enucleation

Published online by Cambridge University Press:  30 April 2019

M.T. Moura Open the ORCID record for M.T. Moura [Opens in a new window] ,
R.V. Sousa ,
C.M. Lucci  and
R. Rumpf
M.T. Moura*
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia, 70770–917, Brasília-DF, Brazil Universidade de Brasília, 70910–900, Brasília-DF, Brazil
R.V. Sousa
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia, 70770–917, Brasília-DF, Brazil
C.M. Lucci
Affiliation:
Universidade de Brasília, 70910–900, Brasília-DF, Brazil
R. Rumpf
Affiliation:
Embrapa Recursos Genéticos e Biotecnologia, 70770–917, Brasília-DF, Brazil Universidade de Brasília, 70910–900, Brasília-DF, Brazil
*
Address for correspondence: Marcelo Tigre Moura. Federal University of São Paulo-UNIFESP, Diadema-SP, Brazil. Tel: +55 11 4044 0500 extension 3474. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Chemical oocyte enucleation holds the potential to ease somatic cell nuclear transfer (SCNT), although high enucleation rates remain limited to micromanipulation-based approaches. Therefore, this study aimed to test mitomycin C (MMC) for use in bovine functional chemical oocyte enucleation. Incubation of denuded eggs in 10 µg ml−1 MMC for different periods did not affect most maturation rates (0.5 h: 85.78%A, 1.0 h: 72.77%B, 1.5 h: 83.87%A, and 2.0 h: 82.05%A) in comparison with non-treated controls (CTL; 85.77%A). Parthenogenetic development arrest by MMC was efficient at cleavage (CTL: 72.93%A, 0.5 h: 64.92%A,B, 1.0 h: 60.39%B,C, 1.5 h: 66.35%A,B, and 2.0 h: 53.84%C) and blastocyst stages (CTL: 33.94%A, 0.5 h: 7.58%B, 1.0 h: 2.47%C, 1.5 h: 0.46%C, and 2.0 h: 0.51%C). Blastocysts were obtained after nuclear transfer (NT) using MMC enucleation [NT(MMC): 4.54%B] but at lower rates than for the SCNT control [NT(CTL): 26.31%A]. The removal of the meiotic spindle after MMC incubation fully restored SCNT blastocyst development [NT(MMC+SR): 24.74%A]. Early pregnancies were obtained by the transfer of NT(MMC) and NT(MMC+SR) blastocysts to synchronized recipients. In conclusion, MMC leads to functional chemical oocyte enucleation during SCNT and further suggests its potential for application towards technical improvements.

Keywords

CattleCytoplastDNA damageLivestockNuclear transplantation
Type
Research Article
Information
Zygote , Volume 27 , Issue 3 , June 2019 , pp. 137 - 142
Copyright
© Cambridge University Press 2019 

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.)

Footnotes

†

Current address: Federal University of São Paulo-UNIFESP, 09972–270, Diadema-SP, Brazil.

‡

Current address: Geneal Genética e Biotecnologia Animal, 38020-970, Uberaba-MG, Brazil.

References

Adriens, I, Smitz, J and Jacquet, P (2009) The current knowledge on radiosensitivity of ovarian follicle development stages. Hum Reprod Update 15, 359–377.Google Scholar
Brewen, JG and Payne, HS (1979) X-ray stage sensitivity of mouse oocytes and its bearing on dose–response curves. Genetics 91, 149–161.Google Scholar
Briggs, R and King, TJ (1952) Transplantation of living nuclei from blastula cells into enucleated frogs’ eggs. Proc Natl Acad Sci USA 38, 455–463.Google Scholar
Collins, JK and Jones, KT (2016) DNA damage responses in mammalian oocytes. Reproduction 152, R15–22.Google Scholar
Costa-Borges, N, Paramio, MT, Calderón, G, Santaló, J and Ibáñez, E (2009) Antimitotic treatments for chemically assisted oocyte enucleation in nuclear transfer procedures. Cloning Stem Cells 11, 153–166.Google Scholar
Elsheikh, AS, Takahashi, Y, Hishinuma, M and Kanagawa, H (1997) Developmental ability of mouse late 2-cell stage blastomeres fused to chemically enucleated oocytes in vitro . J Vet Med Sci 59, 107–113.Google Scholar
Finkielstein, CV, Lewellyn, AL and Maller, JL (2001) The midblastula transition in Xenopus embryos activates multiple pathways to prevent apoptosis in response to DNA damage. Proc Natl Acad Sci USA 98, 1006–1011.Google Scholar
Fulka, JJr, Loi, P, Fulka, H, Ptak, G and Nagai, T (2004) Nucleus transfer in mammals: noninvasive approaches for the preparation of cytoplasts. Trends Biotechnol 22, 279–283.Google Scholar
Gjørret, JO, Knijn, HM, Dieleman, SJ, Avery, B, Larsson, LI and Maddox-Hyttel, P (2003) Chronology of apoptosis in bovine embryos produced in vivo and in vitro . Biol Reprod 69, 1193–1200.Google Scholar
Goldberg, IH, Rabinowitz, M and Reich, E (1962) Basis of actinomycin action I DNA binding and inhibition of RNA–polymerase synthetic reactions by actinomycin. Proc Natl Acad Sci USA 48, 2094–2101.Google Scholar
Gurdon, JB (2006) From nuclear transfer to nuclear reprogramming: the reversal of cell differentiation. Annu Rev Cell Dev Biol 22, 1–22.Google Scholar
Gurdon, JB and Melton, DA (2008) Nuclear reprogramming in cells. Science 322, 1811–1815.Google Scholar
Hosseini, SM, Hajian, M, Forouzanfar, M, Ostadhosseini, S, Moulavi, F, Ghanaei, HR, Gourbai, H, Shahverdi, AH, Vosough, AD and Nasr-Esfahani, MH (2015) Chemically assisted somatic cell nuclear transfer without micromanipulator in the goat: effects of demecolcine, cytochalasin-B, and MG-132 on the efficiency of a manual method of oocyte enucleation using a pulled Pasteur pipette. Anim Reprod Sci 158, 11–18.Google Scholar
Iuso, D, Czernik, M, Zacchini, F, Ptak, G and Loi, P (2013) A simplified approach for oocyte enucleation in mammalian cloning. Cell Reprogram 15, 490–494.Google Scholar
Keefer, CL (2015) Artificial cloning of domestic animals. Proc Natl Acad Sci USA 112, 8874–8878.Google Scholar
Kim, TM, Hwang, WS, Shin, JH, Park, HJ, Han, JY and Lim, JM (2004) Development of a nonmechanical enucleation method using X-ray irradiation in somatic cell nuclear transfer. Fert Steril 82, 963–965.Google Scholar
Kishigami, S, Wakayama, S, Van Thuan, N, Ohta, H, Mizutani, E, Hikichi, T, Hong-Thuy Bui Balbach, S, Ogura, A, Boiani, M and Wakayama, T (2006) Production of cloned mice by somatic cell nuclear transfer. Nat Protoc 1, 125–138.Google Scholar
Kuetemeyer, K, Lucas-Hahn, A, Petersen, B, Lemme, E, Hassel, P, Niemann, H and Heisterkamp, A (2010) Combined multiphoton imaging and automated functional enucleation of porcine oocytes using femtosecond laser pulses. J Biomed Opt 15, 046006.Google Scholar
Kujjo, LL, Ronningen, R, Ross, P, Pereira, RJ, Rodriguez, R, Beyhan, Z, Goissis, MD, Baumann, T, Kagawa, W, Camsari, C, Smith, GW, Kurumizaka, H, Yokoyama, S, Cibelli, JB and Perez, GI (2012) RAD51 plays a crucial role in halting cell death program induced by ionizing radiation in bovine oocytes. Biol Reprod 86, 76.Google Scholar
Kyogoku, H, Yoshida, S and Kitajima, TS (2018) Cytoplasmic removal, enucleation, and cell fusion of mouse oocytes. Methods Cell Biol 144, 459–474.Google Scholar
Lan, GC, Wu, YG, Han, D, Ge, L, Liu, Y, Wang, HL, Wang, JZ and Tan, JH (2008) Demecolcine-assisted enucleation of goat oocytes: protocol optimization, mechanism investigation, and application to improve the developmental potential of cloned embryos. Cloning Stem Cells 10, 189–202.Google Scholar
Li, GP, White, KL and Bunch, TD (2004) Review of enucleation methods and procedures used in animal cloning: state of the art. Cloning Stem Cells 6, 5–13.Google Scholar
Li, S, Kang, JD, Jin, JX, Hong, Y, Zhu, HY, Jin, L, Gao, QS, Yan, CG, Cui, CD, Li, WX and Yin, XJ (2014) Effect of demecolcine-assisted enucleation on the MPF level and cyclin B1 distribution in porcine oocytes. PLoS One 9, e91483.Google Scholar
Llames, S, García-Pérez, E, Meana, Á, Larcher, F and del Río, M (2015) Feeder layer cell actions and applications Tissue Eng Part B Rev 21, 345–353.Google Scholar
Matoba, S and Zhang, Y (2018) Somatic cell nuclear transfer reprogramming: mechanisms and applications. Cell Stem Cell 23, 471–485.Google Scholar
Melo, EO, Canavessi, AM, Franco, MM and Rumpf, R (2007) Animal transgenesis: state of the art and applications. J Appl Genet 48, 47–61.Google Scholar
Moura, MT (2012) Pluripotency and cellular reprogramming. An Acad Pernamb Ciênc Agron 8, 138–168.Google Scholar
Moura, MT, Sousa, RV, Leme, LO and Rumpf, R (2008) Analysis of actinomycin D treated cattle oocytes and their use for somatic cell nuclear transfer. Anim Reprod Sci 109, 40–49.Google Scholar
Moura, MT, Badaraco, J, Sousa, RV, Lucci, CM and Rumpf, R (2019) Improving functional oocyte enucleation by actinomycin D for bovine somatic cell nuclear transfer. Reprod Fert Dev acceptedGoogle Scholar
Ogura, A (2017) Cloning mice. Cold Spring Harbor Protocols Cold Spring Harbor Laboratory Press. doi:10.1101/pdb.prot094425Google Scholar
Russell, LB and Russell, WL (1992) Frequency and nature of specific-locus induced in female mice by radiations and chemicals: a review. Mutat Res 296, 107–127.Google Scholar
Saraiva, NZ, Oliveira, CS, Leal, CLV, de Lima, MR, Del Collado, M, Vantini, R, Monteiro, FM, Niciura, SC and Garcia, JM (2015) Chemically induced enucleation of activated bovine oocytes: chromatin and microtubule organization and production of viable cytoplasts. Zygote 23, 852–862.Google Scholar
Savard, C, Novak, S, Saint-Cyr, A, Moreau, M, Pothier, F and Sirard, MA (2004) Comparison of bulk enucleation methods for porcine oocytes. Mol Reprod Dev 67, 70–76.Google Scholar
Scott, BR, Walker, DM, Tesfaigzi, Y, Schollnberger, H and Walker, V (2003) Mechanistic basis for nonlinear dose–response relationships for low-dose radiation-induced stochastic effects. Nonlinearity Biol Toxicol Med 1, 93–122.Google Scholar
Shimura, T, Inoue, M, Taga, M, Shiraishi, K, Uematsu, N, Takei, N, Yuan, ZM, Shinohara, T and Niwa, O (2007) p53-dependent S-phase damage checkpoint and pronuclear cross talk in mouse zygotes with X-irradiated sperm. Mol Cell Biol 22, 2220–2228.Google Scholar
Solter, D (2000) Mammalian cloning: advances and limitations Nat Rev Genet 1, 199–207.Google Scholar
Sun, MH, Zheng, J, Xie, FY, Shen, W, Yin, S and Ma, JY (2015) Cumulus cells block oocyte meiotic resumption via gap junctions in cumulus oocyte complexes subjected to DNA double-strand breaks. PLoS One 10, e0143223.Google Scholar
Tomasz, M and Palom, Y (1997) The mitomycin bioreductive antitumor agents: cross-linking and alkylation of DNA as the molecular basis of their activity. Pharmacol Ther 76, 73–87.Google Scholar
Vajta, G (2007) Handmade cloning: the future way of nuclear transfer? Trends Biotechnol 25, 250–253.Google Scholar
Wakamatsu, Y, Ju, B, Pristyaznhyuk, I, Niwa, K, Ladygina, T, Kinoshita, M, Araki, K and Ozato, K (2001) Fertile and diploid nuclear transplants derived from embryonic cells of a small laboratory fish, medaka (Oryzias latipes). Proc Natl Acad Sci USA 98, 1071–1076.Google Scholar
Yang, X, Smith, SL, Tian, XC, Lewin, HA, Renard, JP and Wakayama, T (2007) Nuclear reprogramming of cloned embryos and its implications for therapeutic cloning. Nat Genet 39, 295–302.Google Scholar
You, Z, Bailis, JM, Johnson, SA, Dilworth, SM and Hunter, T (2007) Rapid activation of ATM on DNA flanking double-stranded breaks. Nat Cell Biol 9, 1311–1318.Google Scholar
Yuen, WS, Merriman, JA, O’Bryan, MK and Jones, KT (2012) DNA double strand breaks but not interstrand crosslinks prevent progress through meiosis in fully grown mouse oocytes. PLoS One 7, e43875.Google Scholar