Browse > Article
http://dx.doi.org/10.12749/RDB.2015.39.2.29

Factors Influencing the Efficiency of In Vitro Embryo Production in the Pig  

Lin, Tao (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University)
Lee, Jae Eun (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University)
Shin, Hyun Young (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University)
Oqani, Reza K. (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University)
Jin, Dong Il (Department of Animal Science & Biotechnology, Research Center for Transgenic Cloned Pigs, Chungnam National University)
Publication Information
Abstract
Pigs are considered an ideal source of human disease model due to their physiological similarities to humans. However, the low efficiency of in vitro embryo production (IVP) is still a major barrier in the production of pig offspring with gene manipulation. Despite ongoing advances in the associated technologies, the developmental capacity of IVP pig embryos is still lower than that of their in vivo counterparts, as well as IVP embryos of other species (e.g., cattle and mice). The efficiency of IVP can be influenced by many factors that affect various critical steps in the process. The previous relevant reviews have focused on the in vitro maturation system, in vitro culture conditions, in vitro fertilization medium, issues with polyspermy, the utilized technologies, etc. In this review, we concentrate on factors that have not been fully detailed in prior reviews, such as the oocyte morphology, oocyte recovery methods, denuding procedures, first polar body morphology and embryo quality.
Keywords
Oocyte recovery; In vitro maturation; In vitro fertilization; Somatic cell nuclear transfer; Pig;
Citations & Related Records
Times Cited By KSCI : 3  (Citation Analysis)
연도 인용수 순위
1 Somfai T, Ozawa M, Noguchi J, Kaneko H, Ohnuma K, Karja NW, Fahrudin M, Maedomari N, Dinnyes A, Nagai T, Kikuchi K (2006): Diploid porcine parthenotes produced by inhibition of first polar body extrusion during in vitro maturation of follicular oocytes. Reproduction 132:559-570.   DOI
2 Song BS, Kim JS, Yoon SB, Lee KS, Koo DB, Lee DS, Choo YK, Huh JW, Lee SR, Kim SU, Kim SH, Kim HM, Chang KT (2011): Inactivated Sendai-virus- mediated fusion improves early development of cloned bovine embryos by avoiding endoplasmicreticulum- stress-associated apoptosis. Reprod Fertil Dev 23:826-836.
3 Song BS, Yoon SB, Sim BW, Kim YH, Cha JJ, Choi SA, Jeong KJ, Kim JS, Huh JW, Lee SR, Kim SH, Kim SU, Chang KT (2014): Valproic acid enhances early development of bovine somatic cell nuclear transfer embryos by alleviating endoplasmic reticulum stress. Reprod Fertil Dev 26:432-440.   DOI
4 Tanghe S, Van Soom A, Nauwynck H, Coryn M, de Kruif A (2002): Minireview: Functions of the cumulus oophorus during oocyte maturation, ovulation, and fertilization. Mol Reprod Dev 61:414-424.   DOI
5 Tasaki H, Iwata H, Sato D, Monji Y, Kuwayama T (2013): Estradiol has a major role in antrum formation of porcine preantral follicles cultured in vitro. Theriogenology 79:809-814.   DOI
6 Ueno S, Kurome M, Ueda H, Tomii R, Hiruma K, Nagashima H (2005): Effects of maturation conditions on spindle morphology in porcine MII oocytes. J Reprod Develop 51:405-410.   DOI
7 Vajta G (2007): Handmade cloning: the future way of nuclear transfer? Trends in Biotechnology 25:250-253.   DOI
8 VanSoom A, Boerjan M, Ysebaert MT, DeKruif A (1996): Cell allocation to the inner cell mass and the trophectoderm in bovine embryos cultured in two different media. Mol Reprod Dev 45:171-182.   DOI
9 Wang ZG, Yu SD, Xu ZR (2007): Effects of collection methods on recovery efficiency, maturation rate and subsequent embryonic developmental competence of oocytes in holstein cow. Asian Austral J Anim 20:496-500.   DOI
10 Wongsrikeao P, Otoi T, Murakami M, Karja NW, Budiyanto A, Nii M, Suzuki T (2004): Relationship between DNA fragmentation and nuclear status of in vitro-matured porcine oocytes: role of cumulus cells. Reprod Fertil Dev 16:773-780.   DOI
11 Wu D, Cheung QCK, Wen LH, Li JL (2006): A growth-maturation system that enhances the meiotic and developmental competence of porcine oocytes isolated from small follicles. Biol Reprod 75: 547-554.   DOI
12 Wu GQ, Jia BY, Li JJ, Fu XW, Zhou GB, Hou YP, Zhu SE (2011): L-Carnitine enhances oocyte maturation and development of parthenogenetic embryos in pigs. Theriogenology 76:785-793.   DOI
13 Wu J, Emery BR, Carrell DT (2001): In vitro growth, maturation, fertilization, and embryonic development of oocytes from porcine preantral follicles. Biol Reprod 64:375-381.   DOI
14 Xia GL, Kikuchi K, Noguchi J, Izaike Y (2000): Short time priming of pig cumulus-oocyte complexes with FSH and forskolin in the presence of hypoxanthine stimulates cumulus cells to secrete a meiosis-activating substance. Theriogenology 53:1807- 1815.   DOI
15 Zhang P, Liu P, Dou HW, Chen L, Chen LX, Lin L, Tan P, Vajta G, Gao JF, Du YT, Ma RLZ (2013): Handmade cloned transgenic sheep rich in omega-3 fatty acids. Plos One 8.
16 You J, Kim J, Lim J, Lee E (2010): Anthocyanin stimulates in vitro development of cloned pig embryos by increasing the intracellular glutathione level and inhibiting reactive oxygen species. Theriogenology 74:777-785.   DOI
17 Younis JS, Radin O, Izhaki I, Ben-Ami M (2009): Does first polar body morphology predict oocyte performance during ICSI treatment? J Assist Reprod Gen 26:561-567.   DOI
18 Zhang JY, Diao YF, Oqani RK, Han RX, Jin DI (2012a): Effect of endoplasmic reticulum stress on porcine oocyte maturation and parthenogenetic embryonic development in vitro. Biol Reprod 86.
19 Zhang P, Zhang YD, Dou HW, Yin JD, Chen Y, Pang XZ, Vajta G, Bolund L, Du YT, Ma RZ (2012b): Handmade cloned transgenic piglets expressing the nematode Fat-1 gene. Cell Reprogram 14: 258-266.   DOI
20 Zhang X, Miao Y, Zhao JG, Spate L, Bennett MW, Murphy CN, Schatten H, Prather RS (2010): Porcine oocytes denuded before maturation can develop to the blastocyst stage if provided a cumulous cell-derived coculture system. Journal of Animal Science 88:2604-2610.   DOI
21 Zhao J, Hao Y, Ross JW, Spate LD, Walters EM, Samuel MS, Rieke A, Murphy CN, Prather RS (2010): Histone deacetylase inhibitors improve in vitro and in vivo developmental competence of somatic cell nuclear transfer porcine embryos. Cell Reprogram 12:75-83.   DOI
22 Camargo L, Viana J, Sa W, Ferreira A, Ramos A, Vale Filho V (2006): Factors influencing in vitro embryo production. Animal Reproduction 3:19-28.
23 Zhao J, Ross JW, Hao Y, Spate LD, Walters EM, Samuel MS, Rieke A, Murphy CN, Prather RS (2009): Significant improvement in cloning efficiency of an inbred miniature pig by histone deacetylase inhibitor treatment after somatic cell nuclear transfer. Biol Reprod 81:525-530. (Received: April 30 2015/ Accepted: May 11 2015)   DOI
24 Ahn KS, Kim YJ, Kim M, Lee BH, Heo SY, Kang MJ, Kang YK, Lee JW, Lee KK, Kim JH, Nho WG, Hwang SS, Woo JS, Park JK, Park SB, Shim H (2011): Resurrection of an alpha-1,3-galactosyltransferase gene-targeted miniature pig by recloning using postmortem ear skin fibroblasts. Theriogenology 75:933-939.   DOI
25 Alvarez GM, Dalvit GC, Achi MV, Miguez MS, Cetica PD (2009): Immature oocyte quality and maturational competence of porcine cumulus-oocyte complexes subpopulations. Biocell 33:167-177.
26 Arav A (2001): Transillumination increases oocyte recovery from ovaries collected at slaughter. A new technique report. Theriogenology 55:1561-1565.   DOI
27 Bagg MA, Nottle MB, Armstrong DT, Grupen CG (2007): Relationship between follicle size and oocyte developmental competence in prepubertal and adult pigs. Reprod Fertil Dev 19:797-803.   DOI
28 Biswas D, Hyun SH (2011): Supplementation with vascular endothelial growth factor during in vitro maturation of porcine cumulus oocyte complexes and subsequent developmental competence after in vitro fertilization. Theriogenology 76:153-160.   DOI
29 Biswas D, Jeon YB, Kim GH, Jeung EB, Hyun SH (2011): Supplementation of vascular endothelial growth factor during in vitro maturation of porcine immature cumulus-oocyte complexes and subsequent developmental competence after parthenogenesis and somatic cell nuclear transfer. Reprod Fert Develop 23:165-165.
30 Campbell KH, Fisher P, Chen WC, Choi I, Kelly RD, Lee JH, Xhu J (2007a): Somatic cell nuclear transfer: Past, present and future perspectives. Theriogenology 68 Suppl 1:S214-231.   DOI
31 Campbell KH, McWhir J, Ritchie WA, Wilmut I (1996a): Implications of cloning. Nature 380:383.
32 Campbell KH, McWhir J, Ritchie WA, Wilmut I (1996b): Sheep cloned by nuclear transfer from a cultured cell line. Nature 380:64-66.   DOI
33 Campbell KHS, Fisher P, Chen WC, Choi I, Kelly RDW, Lee JH, Xhu J (2007b): Somatic cell nuclear transfer: Past, present and future perspectives. Theriogenology 68:S214-S231.   DOI
34 Dadashpour Davachi N, Kohram H, Zainoaldini S(2012): Cumulus cell layers as a critical factor in meiotic competence and cumulus expansion of ovine oocytes. Small Ruminant Res 102:37-42.   DOI
35 Diao YF, Kenji N, Han RX, Lin T, Oqani RZ, Kang JW, Jin DI (2013): Effects of trichostatin a on in vitro development of porcine parthenogenetic and nuclear transfer embryos. Reprod Devel Biol 37:57-64.   DOI
36 Dang-Nguyen TQ, Somfai T, Haraguchi S, Kikuchi K, Tajima A, Kanai Y, Nagai T (2011): In vitro production of porcine embryos: current status, future perspectives and alternative applications. Anim Sci J 82:374-382.   DOI
37 Davachi ND, Zeinoaldini S, Kohram H (2012): A novel ovine oocyte recovery method from slaughterhouse material. Small Ruminant Res 106:168-172.   DOI
38 Dey SR, Deb GK, Ha AN, Lee JI, Bang JI, Lee KL, Kong IK (2012): Coculturing denuded oocytes during the in vitro maturation of bovine cumulus oocyte complexes exerts a synergistic effect on embryo development. Theriogenology 77:1064-1077.   DOI
39 Fabian D, Koppel J, Maddox-Hyttel P (2005): Apoptotic processes during mammalian preimplantation development. Theriogenology 64:221-231.   DOI
40 Fatehi AN, Zeinstra EC, Kooij RV, Colenbrander B, Bevers MM (2002): Effect of cumulus cell removal of in vitro matured bovine oocytes prior to in vitro fertilization on subsequent cleavage rate. Theriogenology 57:1347-1355.   DOI
41 Funahashi H, Fujiwara T, Nagai T (2000): Modulation of the function of boar spermatozoa via adenosine and fertilization promoting peptide receptors reduce the incidence of polyspermic penetration into porcine oocytes. Biol Reprod 63:1157-1163.   DOI
42 Gupta MK, Uhm SJ, Lee SH, Lee HT (2008): Role of nonessential amino acids on porcine embryos produced by parthenogenesis or somatic cell nuclear transfer. Mol Reprod Dev 75:588-597.   DOI
43 Hao YH, Lai LX, Mao JD, Im GS, Bonk A, Prather RS (2004): Apoptosis in parthenogenetic preimplantation porcine embryos. Biol Reprod 70:1644-1649.   DOI
44 Gupta PS, Nandi S (2012): Isolation and culture of preantral follicles for retrieving oocytes for the embryo production: present status in domestic animals. Reprod Domest Anim 47:513-519.   DOI
45 Hao YH, Lai LX, Liu ZH, Im GS, Wax D, Samuel M, Murphy CN, Sutovsky P, Prather RS (2006): Developmental competence of porcine parthenogenetic embryos relative to embryonic chromosomal abnormalities. Mol Reprod Dev 73:77-82.   DOI
46 Hao YH, Lai LX, Mao JD, Im GS, Bonk A, Prather RS (2003): Apoptosis and in vitro development of preimplantation porcine embryos derived in vitro or by nuclear transfer. Biol Reprod 69:501-507.   DOI
47 Hashimoto N, Kishimoto T (1988): Regulation of meiotic metaphase by a cytoplasmic maturation-promoting factor during mouse oocyte maturation. Dev Biol 126:242-252.   DOI
48 Hazeleger W, Bouwman EG, Noordhuizen JPTM, Kemp B (2000): Effect of superovulation induction on embryonic development on day 5 and subsequent development and survival after nonsurgical embryo transfer in pigs. Theriogenology 53:1063- 1070.   DOI
49 Hirao Y, Naruse K, Kaneda M, Somfai T, Iga K, Shimizu M, Akagi S, Cao F, Kono T, Nagai T, Takenouchi N (2013): Production of fertile offspring from oocytes grown in vitro by nuclear transfer in cattle. Biol Reprod 89:57.   DOI
50 Hwang IS, Park MR, Moon HJ, Shim JH, Kim DH, Yang BC, Ko YG, Yang SS, Cheong HT, Im GS (2007): Effect of osmolarity of culture medium on the preimplantation development of porcine NT and IVF embryos. Reprod Devel Biol 31:91-96.
51 Kazuhiro Kikuchi, Michiko Nakai, Arata Shimada, Kashiwazaki N (2006): Production of viable porcine embryos by in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI). Journal of Mammalian Ova Research 23:96-106.   DOI
52 Jeon BG, Betts DH, King WA, Rho GJ (2011): In vitro developmental potential of nuclear transfer embryos cloned with enucleation methods using predenuded bovine oocytes. Reprod Domest Anim 46: 1035-1042.   DOI
53 Jin DI, Lee SH, Choi JH, Lee JS, Lee JE, Park KW, Seo JS (2003): Targeting efficiency of a-1,3-galactosyl transferase gene in pig fetal fibroblast cells. Experimental & molecular medicine 35:572-577.   DOI
54 Juhi Pathak, Kharche SD, Goel AK, Jindal SK (2013): A comparative study on parthenogenetic activation and embryo production from in vitro matured caprine oocytes. Small Ruminant Res 113:136-140.   DOI
55 Keefer CL (2008): Lessons learned from nuclear transfer (cloning). Theriogenology 69:48-54.   DOI
56 Kidson A, Rubio-Pomar FJ, Van Knegsel A, Van Tol HTA, Hazeleger W, Ducro-Steverink DWB, Colenbrander B, Dieleman SJ, Bevers MM (2004): Quality of porcine blastocysts produced in vitro in the presence or absence of GH. Reproduction 127: 165-177.   DOI
57 Kikuchi K, Nagai T, Motlik J, Shioya Y, Izaike Y (1993): Effect of follicle cells on in vitro fertilization of pig follicular oocytes. Theriogenology 39:593-599.   DOI
58 Kobayashi M, Lee ES, Fukui Y (2006): Cysteamine or beta-mercaptoethanol added to a defined maturation medium improves blastocyst formation of porcine oocytes after intracytoplasn-fic sperm injection. Theriogenology 65:1191-1199.   DOI
59 Kwak SS, Jeung SH, Biswas D, Jeon YB, Hyun SH (2012b): Effects of porcine granulocyte-macrophage colony-stimulating factor on porcine in vitro-fertilized embryos. Theriogenology 77:1186-1197.   DOI
60 Kwak SS, Cheong SA, Jeon Y, Lee E, Choi KC, Jeung EB, Hyun SH (2012a): The effects of resveratrol on porcine oocyte in vitro maturation and subsequent embryonic development after parthenogenetic activation and in vitro fertilization. Theriogenology 78:86-101.   DOI
61 Kwak SS, Yoon JD, Cheong SA, Jeon Y, Lee E, Hyun SH (2014): The new system of shorter porcine oocyte in vitro maturation (18 hours) using >/=8 mm follicles derived from cumulus-oocyte complexes. Theriogenology 81:291-301.   DOI
62 Lai LX, Prather RS (2004): A method for producing cloned pigs by using somatic cells as donors. Methods Mol Biol.:149-164.
63 Lee K, Redel BK, Spate L, Teson J, Brown AN, Park KW, Walters E, Samuel M, Murphy CN, Prather RS (2013): Piglets produced from cloned blastocysts cultured in vitro with GM-CSF. Mol Reprod Dev 80:145-154.   DOI
64 Li GP, Bunch TD, White KL, Rickords L, Liu Y, Sessions BR (2006): Denuding and centrifugation of maturing bovine oocytes alters oocyte spindle integrity and the ability of cytoplasm to support parthenogenetic and nuclear transfer embryo development. Mol Reprod Dev 73:446-451.   DOI
65 Li GP, White KL, Bunch TD (2004): Review of enucleation methods and procedures used in animal cloning: State of the art. Cloning Stem Cells 6:5-13.   DOI
66 Lin J, Shi L, Zhang M, Yang H, Qin Y, Zhang J, Gong D, Zhang X, Li D, Li J (2011): Defects in trophoblast cell lineage account for the impaired in vivo development of cloned embryos generated by somatic nuclear transfer. Cell Stem Cell 8:371-375.   DOI
67 Miao YL, Kikuchi K, Sun QY, Schatten H (2009): Oocyte aging: cellular and molecular changes, developmental potential and reversal possibility. Human Reproduction Update 15:573-585.   DOI
68 Lin T, Diao YF, Choi HS, Oqani RK, Kang JW, Lee JE, Jin DI (2015): Procedure used for denuding pig oocytes influences oocyte damage, and development of in vitro and nuclear transfer embryos. Anim Reprod Sci 152:65-76.   DOI
69 Lin T, Diao YF, Kang JW, Lee JE, Kim DK, Jin DI (2013): Chromosomes in the porcine first polar body possess competence of second meiotic division within enucleated MII stage oocytes. Plos One 8:e82766.   DOI
70 Lin T, Zhang JY, Diao YF, Kang JW, Jin DI (2014): Effects of sorbitol on porcine oocyte maturation and embryo development in vitro. Zygote:1-10.
71 Mochida N, Akatani-Hasegawa A, Saka K, Ogino M, Hosoda Y, Wada R, Sawai H, Shibahara H (2013): Live births from isolated primary/early secondary follicles following a multistep culture without organ culture in mice. Reproduction 146:37-47.   DOI
72 Naruse K, Kim HR, Shin YM, Chang SM, Lee HR, Park CS, Jin DI (2007a): Low concentrations of MEM vitamins during in vitro maturation of porcine oocytes improves subsequent parthenogenetic development. Theriogenology 67:407-412.   DOI
73 Naruse K, Quan YS, Choi SM, Park CS, Jin DI (2007b): Treatment of porcine oocytes with MEM vitamins during in vitro maturation improves subsequent blastocyst development following nuclear transfer. J Reprod Dev 53:679-684.   DOI
74 Onishi A, Iwamoto M, Akita T, Mikawa S, Takeda K, Awata T, Hanada H, Perry AC (2000): Pig cloning by microinjection of fetal fibroblast nuclei. Science 289:1188-1190.   DOI
75 Navarro PA, de Araujo MM, de Araujo CM, Rocha M, dos Reis R, Martins W (2009): Relationship between first polar body morphology before intracytoplasmic sperm injection and fertilization rate, cleavage rate, and embryo quality. Int J Gynecol Obstet 104:226-229.   DOI
76 Nguyen NT, Lo NW, Chuang SP, Jian YL, Ju JC (2011): Sonic hedgehog supplementation of oocyte and embryo culture media enhances development of IVF porcine embryos. Reproduction 142:87-97.   DOI
77 Ogura A, Inoue K, Wakayama T (2013): Recent advancements in cloning by somatic cell nuclear transfer. Philos Trans R Soc Lond B Biol Sci 368: 20110329.
78 Orsi NM, Leese HJ (2004): Amino acid metabolism of preimplantation bovine embryos cultured with bovine serum albumin or polyvinyl alcohol. Theriogenology 61:561-572.   DOI
79 Polejaeva IA, Chen SH, Vaught TD, Page RL, Mullins J, Ball S, Dai Y, Boone J, Walker S, Ayares DL, Colman A, Campbell KH (2000): Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407:86-90.   DOI
80 Sato C, Shimada M, Mori T, Kumasako Y, Otsu E, Watanabe H, Utsunomiya T (2007): Assessment of human oocyte developmental competence by cumulus cell morphology and circulating hormone profile. Reprod Biomed Online 14:49-56.   DOI
81 Sedmikova M, Burdova J, Petr J, Etrych M, Rozinek J, Jilek F (2003): Induction and activation of meiosis and subsequent parthenogenetic development of growing pig oocytes using calcium ionophore A23187. Theriogenology 60:1609-1620.   DOI