Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Development of buffalo embryo derived from ICSI: effects of various somatic-cell co-culture

Ratree Jintana A , Kriengsak Tasripoo A , Kitiya Srisakwattana https://orcid.org/0000-0002-9184-0528 A * , Wisut Nualchuen A , Sungworn Usawang A and Sunpetch Sophon B
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Science, Chulalongkorn University, Henri Dunant Road, Phathumwan, Bangkok 10330, Thailand.

B 3 Ramkamhaeng 118 alley 11-1, Ramkamhaeng Road, Saphansoong, Bangkok 10240, Thailand.

* Correspondence to: skitiya@chula.ac.th

Handling Editor: Sathya Velmurugan

Animal Production Science 64, AN23177 https://doi.org/10.1071/AN23177
Submitted: 7 September 2022  Accepted: 13 October 2023  Published: 16 November 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

Somatic-cell co-culture of intracytoplasmic sperm injection (ICSI) buffalo embryos has not been reported earlier.

Aim

This study aimed to determine the effects of buffalo oviductal epithelial-cell, granulosa-cell, and cumulus-cell co-culture on in vitro culture of early embryo development as ICSI and post-activation.

Methods

Selected oocyte–cumulus complexes were cultured for 19–20 h in 50-μL drop of tissue culture medium (TCM199 + 10% buffalo follicular fluid, hCG 50 IU/mL, 0.02% arbitrary units (AU)/mL follicle-stimulating hormone and 1 μg/mL estradiol-17βE2). Oocytes reaching Metaphase II were subjected to ICSI with immobilised spermatozoa. All ICSI oocytes were activated with calcium ionophore for 5 min, followed by cycloheximide for 5 h. The embryos at 6–8-cell stages were co-cultured.

Key results

The morula, blastocyst, and hatched blastocyst rates when co-cultured with oviductal epithelial cells were 68.18%, 48.18%, and 30.00% respectively. The morula, blastocyst, and hatched blastocyst rates when co-cultured with cumulus cells were 51.49%, 34.33%, and 16.42% respectively. The morula, blastocyst, and hatched blastocyst rates when co-cultured with granulosa cells were 52.14%, 32.48%, and 13.68% respectively.

Conclusions

In vitro maturation buffalo oocytes can be fertilised in vitro with ICSI and co-cultured with different types of cells. Oviductal epithelial cell co-culture was shown to be superior in supporting in vitro embryo development in this study.

Implications

The oviductal epithelial cells are easy to prepare and may be used for co-culture to increase the efficiency of in vitro production of buffalo embryos.

Keywords: buffalo, co-culture, cumulus cells, granulosa cells, ICSI, intracytoplasmic sperm injection, oviductal epithelial cells, somatic cells.

References

Ajduk A, Yamauchi Y, Ward MA (2006) Sperm chromatin remodeling after intracytoplasmic sperm injection differs from that of in vitro fertilization. Biology of Reproduction 75, 442-451.
| Crossref | Google Scholar | PubMed |

Atabay EC, Atabay FP, de Vera RV, Mamuad FV, Cruz LC (2006) Chemical and electrical activation of swamp buffalo (Bubalus bubalis) oocytes with or without cycloheximide treatments. Buffalo Journal 22(2), 121-130.
| Google Scholar |

Chuangsoongneon U, Kamonpatana M (1991) Oocyte maturation, in vitro fertilization and culture system for developing preimplantation swamp buffalo embryos using frozen thawed semen. Buffalo Journal 7(2), 189-198.
| Google Scholar |

Chung JT, Keefer CL, Downey BR (2000) Activation of bovine oocytes following intracytoplasmic sperm injection (ICSI). Theriogenology 53, 1273.
| Crossref | Google Scholar | PubMed |

Cockrill WR (1987) The buffalo a world assessment. Buffalo Journal 3, 1-20.
| Google Scholar |

Dantas JK, Miranda MS, Santos SSD, Ohashi OM (2002) Co-culture of buffalo embryos with oviduct and granulose cells in different media. In ‘The proceeding of the 1st buffalo symposium of Americas’, 1–4 September, Brazil. pp. 425–428. (Associacao de Criadores de Bufalos do Para: Belem, Brazil)

Ellington JE, Carney EW, Farrell PB, Simkin ME, Foote RH (1990) Bovine 1–2 cell embryo development using a simple medium in three oviduct epithelial cell coculture systems. Biology of Reproduction 43, 97-104.
| Crossref | Google Scholar | PubMed |

Gasparrini B, Boccia L, Rosa AD, Palo RD, Campanile G, Zicarelli L (2004) Chemical activation of buffalo (Bubalus bubalis) oocytes by different methods: effects of aging on post-parthenogenetic development. Theriogenology 62, 1627-1637.
| Crossref | Google Scholar | PubMed |

Gasparrini B, Boccia L, Marchandise J, Di Palo R, George F, Donnay I, Zicarelli L (2006) Enrichment of in vitro maturation medium for buffalo (Bubalus bubalis) oocytes with thiol compounds: effects of cystine on glutathione synthesis and embryo development. Theriogenology 65, 275-287.
| Crossref | Google Scholar | PubMed |

Goto K (1993) Bovine microfertilization and embryo transfer. Molecular Reproduction and Development 36, 288-290.
| Crossref | Google Scholar | PubMed |

Goto K, Kinoshita A, Takuma Y, Ogawa K (1990) Fertilization of bovine oocytes by the injection of immobilised, killed spermatozoa. Veterinary Record 127, 517-520.
| Google Scholar | PubMed |

Hasler JF (2000) In vitro culture of bovine embryos in Ménézo’s B2 medium with or without coculture and serum: the normalcy of pregnancies and calves resulting from transferred embryos. Animal Reproduction Science 60-61, 81-91.
| Crossref | Google Scholar | PubMed |

Hawk HW, Wall RJ (1994) Improved yields of bovine blastocysts from in vitro-produced oocytes. II. Media and co-culture cells. Theriogenology 41, 1585-1594.
| Crossref | Google Scholar |

Heidari B, Shirazi A, Naderi M-M, Akhondi M-M, Hassanpour H, Sarvari A, Borjian S (2013) Effect of various co-culture systems on embryo development in ovine. Czech Journal of Animal Science 58(10), 443-452.
| Crossref | Google Scholar |

Horiuchi T, Emuta C, Yamauchi Y, Oikawa T, Numabe T, Yanagimachi R (2002) Birth of normal calves after intracytoplasmic sperm injection of bovine oocytes: a methodological approach. Theriogenology 57, 1013-1024.
| Crossref | Google Scholar |

Kalyanaraman B, Soundarapandian S, Gopal DR, Sivasankaran B, Manoharan P (2022) Expression profiling of candidate embryotrophic genes of buffalo oviduct during different stages of oestrous cycle. Buffalo Bulletin 41(2), 251-261.
| Crossref | Google Scholar |

Kamonpatana M (1994) IVM/IVF/IVC in buffaloes: procedure and points for research. Buffalo Journal, Suppl. 2, 181-210.
| Google Scholar |

Kharche SD, Goel AK, Jindal SK, Sinha NK, Yadav P (2008) Effect of somatic cells co-culture on cleavage and development of in-vitro fertilized caprine embryos. The Indian Journal of Animal Science 78(7), 686-692.
| Google Scholar |

Khatir H, Anouassi A, Tibary A (2004) Production of dromedary (Camelus dromedarius) embryos by IVM and IVF and co-culture with oviductal or granulosa cells. Theriogenology 62, 1175-1185.
| Crossref | Google Scholar | PubMed |

Khatir H, Anouassi A, Tibary A (2007) Effect of follicular size on in vitro developmental competence of oocytes and viability of embryos after transfer in the dromedary (Camelus dromedarius). Animal Reproduction Science 99, 413-420.
| Crossref | Google Scholar | PubMed |

Kumar D, Anand T (2012) In vitro embryo production in buffalo: basic concepts. Journal of Buffalo Science 1, 50-54.
| Crossref | Google Scholar |

Lakshmi Devi H, Shital Negargoje D, Pandey S, Yasotha T, Chandra V, Taru Sharma G (2022) Impact of uterine epithelial cells and its conditioned medium on the in vitro embryo production in buffalo (Bubalus bubalis). Theriogenology 183, 61-68.
| Crossref | Google Scholar |

Locatelli Y, Cognié Y, Vallet JC, Baril G, Verdier M, Poulin N, Legendre X, Mermillod P (2005) Successful use of oviduct epithelial cell coculture for in vitro production of viable red deer (Cervus elaphus) embryos. Theriogenology 64, 1729-1739.
| Crossref | Google Scholar | PubMed |

Mahmoud KGM, Puglisi R, Scholkamy TH (2007) Artificial meiotic arrest and parthenogenetic activation of buffalo oocytes using cycloheximide. Cytologia 72, 173-180.
| Crossref | Google Scholar |

Nandi S, Chauhan MS, Palta P (1998) Influence of cumulus cells and sperm concentration on cleavage rate and subsequent embryonic development of buffalo (Bubalus bubalis) oocytes matured and fertilized in vitro. Theriogenology 50, 1251-1262.
| Crossref | Google Scholar | PubMed |

Nandi S, Ravindranatha BM, Gupta PSP, Sarma PV (2001) Effect of somatic cells monolayer on maturation of buffalo oocytes in vitro. Indian Journal of Animal Science 71(10), 936-937.
| Google Scholar |

Oikawa T, Takada N, Kikuchi T, Numabe T, Takenaka M, Horiuchi T (2005) Evaluation of activation treatments for blastocyst production and birth of viable calves following bovine intracytoplasmic sperm injection. Animal Reproduction Science 86, 187-194.
| Crossref | Google Scholar | PubMed |

Orsi NM, Reischl JB (2007) Mammalian embryo co-culture: trials and tribulations of a misunderstood method. Theriogenology 67, 441-458.
| Crossref | Google Scholar | PubMed |

Purohit GN, Duggal GP, Dadarwal D, Kumar D, Yadav RC, Vyas S (2003) Reproductive biotechnologies for improvement of buffalo: the current status. Asian–Australasian Journal of Animal Sciences 16(7), 1071-1086.
| Crossref | Google Scholar |

Ramesh HS, Gupta PSP, Nandi S, Manjunath BM, Kumar VG, Ravindra JP (2007) Co-culture of buffalo large preantral follicles with ovarian somatic cells. Advances in Biological Research 1(1-2), 29-33.
| Google Scholar |

Ramesh HS, Gupta PSP, Nandi S, Manjunatha BM, Kumar VG, Ravindra JP (2008) Co-culture of buffalo preantral follicles with different somatic cells. Reproduction in Domestic Animals 43, 520-524.
| Crossref | Google Scholar | PubMed |

Rexroad CE, Jr., Powell AM (1988) Co-culture of ovine ova with oviductal cells in medium 199. Journal of Animal Science 66, 947-953.
| Crossref | Google Scholar | PubMed |

Rosati I, Berlinguer F, Bogliolo L, Leoni G, Ledda S, Naitana S (2002) The effect of co-culture on the development of in vitro matured equine oocytes after intracytoplastic sperm injection. Equine Veterinary Journal 34(7), 673-678.
| Crossref | Google Scholar | PubMed |

Satheshkumar S, Brindha K, Nithya S, Palanisamy A, Kumanan K (2012) Morphological characterization of bubaline oviductal cells maintained under short-term culture. Buffalo Bulletin 31(3), 148-152.
| Google Scholar |

Suresh KP, Nandi S, Mondal S (2009) Factors affecting laboratory production of buffalo embryos: a meta-analysis. Theriogenology 72, 978-985.
| Crossref | Google Scholar | PubMed |

Suttner R, Zakhartchenko V, Stojkovic P, Muller S, Alberio R, Medjugorac I, Brem G, Wolf E, Stojkovic M (2000) Intracytoplasmic sperm injection in bovine: effects of oocyte activation, sperm pretreatment and injection technique. Theriogenology 54, 935-948.
| Crossref | Google Scholar | PubMed |

Tasripoo K, Srisakwattana K, Suthikrai W, Chethasing S, Kamonpatana M (2005) Potential uses of buffalo oocytes from ovaries with CL and without CL for in vitro maturation and fertilization. Buffalo Journal 21(3), 221-228.
| Google Scholar |

Tasripoo K, Srisakwattana K, Suthikrai W, Chethasing S, Kamonpatana M (2006) Potential use of buffalo follicular fluid for in vitro maturation supplementation of buffalo oocytes. In ‘Poster presentation at the 5th Asian Buffalo Congress Nanning, China’, pp. 610–615.

Tasripoo K, Srisakwattana K, Sophon S, Nualchuen W, Usawang S (2007) Cloning of buffalo from fibroblast cell of donor various ages. Buffalo Journal 23(2), 141-152.
| Google Scholar |

Tasripoo K, Srisakwattana K, Nualchuen W, Sophon S (2012) Effects of various activations on bovine embryonic development following intracytoplasmic sperm injection. Italian Journal of Applied Animal Science 2(2), 167-173.
| Google Scholar |

Tasripoo K, Suthikrai W, Sophon S, Jintana R, Nualchuen W, Usawang S, Bintvihok A, Techakumphu M, Srisakwattana K (2014) First cloned swamp buffalo produced from adult ear fibroblast cell. Animal 8(7), 1139-1145.
| Crossref | Google Scholar | PubMed |

Tasripoo K, Srisakwattana K, Nualchuen W, Sophon S (2015) In vitro production of buffalo embryos by injection of immobilized and dead spermatozoa. Buffalo Bulletin 34(2), 245-256.
| Google Scholar |

Tian J-H, Wu Z-H, Liu L, Cai Y, Zeng S-M, Zhu S-E, Liu G-S, Li Y, Wu C-X (2006) Effects of oocyte activation and sperm preparation on the development of porcine embryos derived from in vitro-matured oocytes and intracytoplasmic sperm injection. Theriogenology 66, 439-448.
| Crossref | Google Scholar | PubMed |

Yadav PS, Saini A, Kumar A, Jain GC (1998) Effect of oviductal cell co-culture on cleavage and development of goat IVF embryos. Animal Reproduction Science 51(4), 301-306.
| Crossref | Google Scholar | PubMed |

Yadav PS, Khanna S, Hooda OK, Sethi RK (2000) Effect of oviductal cell co-culture on cleavage and development of buffalo IVF embryos. Asian–Australasian Journal of Animal Sciences 13(7), 894-896.
| Crossref | Google Scholar |