Abstract
Rabbit is a valuable animal model in biomedical research due to many practical advantages, including reproductive ones. Assisted reproductive techniques (ARTs) are very useful tools to facilitate the progression of these studies in rabbit model. However, the majority of ARTs are not well developed in this species, and some problems remain unsolved. A brief overview of current ARTs for using rabbits as animal model for biomedical studies is addressed in this chapter.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Arias-Álvarez M (2009) Influencia de diferentes estrategias reproductivas y nutricionales sobre la fisiologia ovarica en conejas primíparas. PhD thesis. Universidad Complutense de Madrid, Madrid, Spain; 266 pp. ISBN: 978-84-693-2400-4
Arias-Álvarez M, García-García RM, Rebollar PG et al (2009) Effects of a lignin-rich fibre diet on productive, reproductive and endocrine parameters in nulliparous rabbit does. Livest Sci 123:107–115. https://doi.org/10.1016/j.livsci.2008.10.013
Arias-Álvarez M, García-García RM, Torres-Rovira L et al (2010a) Influence of hormonal and nonhormonal estrus synchronization methods on follicular and oocyte quality in primiparous lactating does at early postpartum period. Theriogenology 73:26–35. https://doi.org/10.1016/j.theriogenology.2009.07.017
Arias-Álvarez M, García-García RM, Torres-Rovira L et al (2010b) Influence of leptin on in vitro maturation and steroidogenic secretion of cumulus-oocyte complexes through JAK2/STAT3 and MEK 1/2 pathways in the rabbit model. Reproduction 139. https://doi.org/10.1530/REP-09-0309
Arias-Álvarez M, García-García RM, López-Tello J et al (2017) In vivo and in vitro maturation of rabbit oocytes differently affects the gene expression profile, mitochondrial distribution, apoptosis and early embryo development. Reprod Fertil Dev 29:1667–1679. https://doi.org/10.1071/RD15553
Arias-Álvarez M, Garciá-Garciá RM, López-Tello J et al (2018) α-Tocopherol modifies the expression of genes related to oxidative stress and apoptosis during in vitro maturation and enhances the developmental competence of rabbit oocytes. Reprod Fertil Dev 30:1728–1738. https://doi.org/10.1071/RD17525
Austin CR (1952) The ‘capacitation’ of the mammalian sperm. Nature 170:326–326. https://doi.org/10.1038/170326a0
Bank H, Maurer RR (1974) Survival of frozen rabbit embryos. Exp Cell Res 89:188–196. https://doi.org/10.1016/0014-4827(74)90201-8
Besenfelder U, Brem G (1993) Laparoscopic embryo transfer in rabbits. J Reprod Fertil 99:53–56. https://doi.org/10.1530/jrf.0.0990053
Biggers JD, Whitten WK, Whittingham DG (1971) The culture of mouse embryos in vitro. In: Daniel JC (ed) Methods in mammalian embryology. WH Freeman, San Francisco, pp 86–116
Brackett BG, Oliphant G (1975) Capacitation of rabbit spermatozoa in vitro. Biol Reprod 12:260–274
Brackett BG, Bousquet D, Dressel MA (1982) In vitro sperm capacitation and in vitro fertilization with normal development in the rabbit. J Androl 3:402–411. https://doi.org/10.1002/j.1939-4640.1982.tb00710.x
Bredderman PJ, Foote RH, Yassen AM (1964) An improved artificial vagina for collecting rabbit semen. J Reprod Fertil 7:401–403
Brunet-Simon A, Henrion G, Renard JP, Duranthon V (2001) Onset of zygotic transcription and maternal transcript legacy in the rabbit embryo. Mol Reprod Dev 58:127–136. https://doi.org/10.1002/1098-2795(200102)58:2<127::aid-mrd1>3.0.co;2-a
Bruyère P, Baudot A, Joly T et al (2013) A chemically defined medium for rabbit embryo cryopreservation. PLoS One 8. https://doi.org/10.1371/journal.pone.0071547
Campo H, García-Domínguez X, López-Martínez S et al (2019) Tissue-specific decellularized endometrial substratum mimicking different physiological conditions influences in vitro embryo development in a rabbit model. Acta Biomater 89:126–138. https://doi.org/10.1016/j.actbio.2019.03.004
Cao W, Zhao J, Qu P, Liu E (2022) Current progress and prospects in rabbit cloning. Cell Reprog 24:63–70
Carney EW, Foote RH (1990) Effects of superovulation, embryo recovery, culture system and embryo transfer on development of rabbit embryos in vivo and in vitro. J Reprod Fertil 89:543–551
Castellini C, Mattioli S, Dal Bosco A et al (2020) Nerve growth factor receptor role on rabbit sperm storage. Theriogenology 153:54–61. https://doi.org/10.1016/j.theriogenology.2020.04.042
Cervera RP, García-Ximénez F (2003) Oocyte age and nuclear donor cell type affect the technical efficiency of somatic cloning in rabbits. Zygote 11:151–158. https://doi.org/10.1017/S0967199403002181
Chang MC (1951) Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168:697–698. https://doi.org/10.1038/168697b0
Chang MC (1955) Development of fertilizing capacity of rabbit spermatozoa in the uterus. Nature 175:1036–1037. https://doi.org/10.1038/1751036a0
Chang MC (1959) Fertilization of rabbit ova in vitro. Nature 184:466–467. https://doi.org/10.1038/184466a0
Chesné P, Adenot PG, Viglietta C et al (2002) Cloned rabbits produced by nuclear transfer from adult somatic cells. Nat Biotechnol 20:366–369
Chung OS, Bae I, Cho WK (1974) The maturation in vitro of the rabbit oocytes. Yonsei Med J 15:11–16
Collas P, Robl JM (1990) Factors affecting the efficiency of nuclear transplantation in the rabbit embryo. Biol Reprod 43:877–884
Daniel N, Renard JP (2010) Artificial fertilization in rabbits by intracytoplasmic sperm injection (ICSI). Cold Spring Harb Protoc 5. https://doi.org/10.1101/pdb.prot5359
Deng M, Yang X (2001) Full term development of rabbit oocytes fertilized by intracytoplasmic sperm injection. Mol Reprod Dev 59:38–43. https://doi.org/10.1002/mrd.1005
Denker HW (2000) Structural dynamics and function of early embryonic coats. Cells Tissues Organs 166:180–207. https://doi.org/10.1159/000016732
Du F, Xu J, Zhang J et al (2009) Beneficial effect of young oocytes for rabbit somatic cell nuclear transfer. Cloning Stem Cells 11:131–140. https://doi.org/10.1089/clo.2008.0042
Esteves PJ, Abrantes J, Baldauf HM et al (2018) The wide utility of rabbits as models of human diseases. Exp Mol Med 50:1–10. https://doi.org/10.1038/s12276-018-0094-1
Fahy MM, Kane MT (1993) Incorporation of [3H]inositol into phosphoinositides and inositol phosphates by rabbit blastocysts. Mol Reprod Dev 34:391–395. https://doi.org/10.1002/mrd.1080340407
Fan J, Watanabe T (2003) Inflammatory reactions in the pathogenesis of atherosclerosis. J Atheroscler Thromb 10:63–71
Fischer B, Chavatte-Palmer P, Viebahn C et al (2012) Rabbit as a reproductive model for human health. Reproduction 144:1–10
Fraser LR (2010) The “switching on” of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation. Mol Reprod Dev 77:197–208. https://doi.org/10.1002/mrd.21124
Gadella BM, Harrison RAP (2000) The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development 127:2407–2420
Garcia-Dominguez X, Marco-Jimenez F, Viudes-de-Castro MP, Vicente JS (2019) Minimally invasive embryo transfer and embryo vitrification at the optimal embryo stage in rabbit model. J Vis Exp 2019:1–9. https://doi.org/10.3791/58055
Giojalas LC, Rovasio RA, Fabro G et al (2004) Timing of sperm capacitation appears to be programmed according to egg availability in the female genital tract. Fertil Steril 82:247–249. https://doi.org/10.1016/j.fertnstert.2003
Graur D, Duret L, Gouy M (1996) Phylogenetic position of the order Lagomorpha (rabbits, hares and allies). Nature 379:333–335
Guidobaldi HA, Teves ME, Uñates DR et al (2008) Progesterone from the cumulus cells is the sperm chemoattractant secreted by the rabbit oocyte cumulus complex. PLoS One 3. https://doi.org/10.1371/journal.pone.0003040
Hafez ES (1964) Effects of over-crowding in utero on implantation and fetal development in the rabbit. J Exp Zool 156:269–287. https://doi.org/10.1002/jez.1401560304
Harper MJK (1973) Relationship between sperm transport and penetration of eggs in the rabbit oviduct. Biol Reprod 8:441–450
Hauser R, Homonnai G, Paz GF et al (1992) Migration sedimentation technique as a predictive test for the fertilizing capacity of spermatozoa in an in-vitro fertilization programme. Int J Androl 15:498–503. https://doi.org/10.1111/j.1365-2605.1992.tb01143.x
Henderson GRW, Brahmasani SR, Yelisetti UM et al (2014) Candidate gene expression patterns in rabbit preimplantation embryos developed in vivo and in vitro. J Assist Reprod Genet 31:899–911. https://doi.org/10.1007/s10815-014-0233-0
Hosoi Y, Niwa K, Hatanaka S, Iritani A (1981) Fertilization in vitro of rabbit eggs by epididymal spermatozoa capacitated in a chemically defined medium. Biol Reprod 24:637–642
Jelínkova L, Kubelka M, Motlfk J, Guerrier P (1994) Chromatin condensation and histone H1 kinase activity during growth and maturation of rabbit oocytes. Mol Reprod Dev 37:210–215
Jiménez-Trigos E, Vicente JS, Marco-Jiménez F (2014) First pregnancy and live birth from vitrified rabbit oocytes after intraoviductal transfer and in vivo fertilization. Theriogenology 82:599–604. https://doi.org/10.1016/j.theriogenology.2014.05.029
Joung SY, Kim HJ, Choi WS et al (2004) Effects of transferring in vitro-cultured rabbit embryos to recipient oviducts on mucin coat deposition, implantation and development. Zygote 12:215–219. https://doi.org/10.1017/S0967199404002795
Ju JC, Chen TH, Tseng JK et al (2002) Cytoskeletal patterns, in vitro maturation and parthenogenetic development of rabbit GV oocytes. Asian Aust J Anim Sci 15:1695–1701
Kane MT (1972) Energy substrates and culture of single cell rabbit ova to blastocysts. Nature 238:468–469
Kane MT (2019) Culture of preimplantation rabbit embryos. In: Herrick J (ed) Comparative embryo culture. Methods in molecular biology. Springer, New York, pp 63–91
Kasai M, Hamaguchi Y, Zhu SE et al (1992) High survival of rabbit morulae after vitrification in an ethylene glycol-based solution by a simple method. Biol Reprod 46(6):1042–1046
Keefer CL (1989) Fertilization by sperm injection in the rabbit. Gamete Res 22:59–69. https://doi.org/10.1002/mrd.1120220107
Kim CK, Im KS, Zheng X, Foote RH (1989) In vitro capacitation and fertilizing ability of ejaculated rabbit sperm treated with lysophosphatidylcholine. Gamete Res 22:131–141
Lan C, Xiaohui D, Qingzhao F et al (2008) Developmental potential of oocytes fertilized by conventional in vitro fertilization (IVF) or intracytoplasmic sperm injection (ICSI) after cryopreservation and mesometrial autotransplantation of rabbit ovarian tissue. Animal 2:1371–1376. https://doi.org/10.1017/S1751731108002528
Lavara R, Baselga M, Marco-Jiménez F, Vicente JS (2015) Embryo vitrification in rabbits: Consequences for progeny growth. Theriogenology 84:674–680. https://doi.org/10.1016/j.theriogenology.2015.04.025
Li W-H, Gouy M, Sharp PM et al (1990) Molecular phylogeny of Rodentia, Lagomorpha, Primates, Artiodactyla, and Carnivora and molecular clocks (mammalian phylogeny/DNA sequence trees/branching dates). Proc Natl Acad Sci USA 87:6703–6707
Li Q, Hou J, Wang S et al (2010a) Production of transgenic rabbit embryos through intracytoplasmic sperm injection. Zygote 18:301–307. https://doi.org/10.1017/S0967199410000250
Li QY, Hou J, Chen YF, An XR (2010b) Full-term development of rabbit embryos produced by ICSI with sperm frozen in liquid nitrogen without cryoprotectants. Reprod Domest Anim 45:717–722. https://doi.org/10.1111/j.1439-0531.2009.01340.x
Lin TA, Chen CH, Sung LY et al (2011) Open-pulled straw vitrification differentiates cryotolerance of in vitro cultured rabbit embryos at the eight-cell stage. Theriogenology 75:760–768. https://doi.org/10.1016/j.theriogenology.2010.10.018
López-Béjar M, López-Gatius F (2002) Nonequilibrium cryopreservation of rabbit embryos using a modified (sealed) open pulled straw procedure. Theriogenology 58:1541–1552. https://doi.org/10.1016/S0093-691X(02)01045-2
Lopez-Tello J, Arias-Alvarez M, Gonzalez-Bulnes A, Sferuzzi-Perri AN (2019) Models of Intrauterine growth restriction and fetal programming in rabbits. Mol Reprod Dev 86:1781–1809
Lorenzo PL, Illera JC, Silván G et al (1997) Steroid-level response to insulin-like growth factor-1 in oocytes matured in vitro. J Reprod Immunol 35(1):11–29
Marco-Jiménez F, Lavara R, Jiménez-Trigos E, Vicente JS (2013) In vivo development of vitrified rabbit embryos: Effects of vitrification device, recipient genotype, and asynchrony. Theriogenology 79:1124–1129. https://doi.org/10.1016/j.theriogenology.2013.02.008
Marco-Jiménez F, Jiménez-Trigos E, Almela-Miralles V, Vicente JS (2016) Development of cheaper embryo vitrification device using the minimum volume method. PLoS One 11:1–9. https://doi.org/10.1371/journal.pone.0148661
Mehaisen GMK, Vicente JS, Lavara R (2004) In vivo embryo recovery rate by laparoscopic technique from rabbit does selected for growth rate. Reprod Domest Anim 39:347–351. https://doi.org/10.1111/j.1439-0531.2004.00526.x
Mehaisen GMK, Viudes-De-Castro MP, Vicente JS, Lavara R (2006) In vitro and in vivo viability of vitrified and non-vitrified embryos derived from eCG and FSH treatment in rabbit does. Theriogenology 65:1279–1291. https://doi.org/10.1016/j.theriogenology.2005.08.007
Meng Q, Polgar Z, Tancos Z et al (2013) Cloning of rabbits. In: Cibelli J, Wilmut I, Jaenisch R, Gurdon J, Lanza R, West M, Campbell KHS (eds) Principles of cloning, 2nd edn. Academic, New York, pp 227–244. https://doi.org/10.1016/B978-0-12-386541-0.00018-7
Murakami H, Imai H (1996) Successful implantation of in vitro cultured rabbit embryos after uterine transfer: A role for mucin. Mol Reprod Dev 43:167–170. https://doi.org/10.1002/(SICI)1098-2795(199602)43:2<167::AID-MRD5>3.0.CO;2-P
Naresh S, Atreja SK (2015) The protein tyrosine phosphorylation during in vitro capacitation and cryopreservation of mammalian spermatozoa. Cryobiology 70:211–216. https://doi.org/10.1016/j.cryobiol.2015.03.008
Niwa K, Hosoi Y, Ohara K, Iritani A (1983) Fertilization in vitro of rabbit eggs with or without follicular cells by epididymal spermatozoa capacitated in a chemically defined medium. Anim Reprod Sci 6:143–149
Ogonuki N, Inoue K, Miki H et al (2005) Differential development of rabbit embryos following microinsemination with sperm and spermatids. Mol Reprod Dev 72:411–417. https://doi.org/10.1002/mrd.20363
Püschel B, Daniel N, Bitzer E et al (2010) The rabbit (Oryctolagus cuniculus): A model for mammalian reproduction and early embryology. Cold Spring Harb Protoc 5. https://doi.org/10.1101/pdb.emo139
Rebollar PG, Bonanno A, Di Grigoli A et al (2008) Endocrine and ovarian response after a 2-day controlled suckling and eCG treatment in lactating rabbit does. Anim Reprod Sci 104:316–328. https://doi.org/10.1016/j.anireprosci.2007.02.018
Saenz-de-Juano M, Marco-Jimenez F, Viudes-de-Castro M et al (2014) Direct comparison of the effects of slow freezing and vitrification on late blastocyst gene expression, development, implantation and offspring of rabbit morulae. Reprod Domest Anim 49:505–511. https://doi.org/10.1111/rda.12320
Saez Lancellotti TE, Boarelli PV, Monclus MA et al (2010) Hypercholesterolemia impaired sperm functionality in rabbits. PLoS One 5. https://doi.org/10.1371/journal.pone.0013457
Saez Lancellotti TE, Boarelli PV, Romero AA et al (2013) Semen quality and sperm function loss by hypercholesterolemic diet was recovered by addition of olive oil to diet in rabbit. PLoS One 8. https://doi.org/10.1371/journal.pone.0052386
Seidel GE, Bowen RA, Kane MT (1976) In vitro fertilization, culture, and transfer of rabbit ova. Fertil Steril 27(7):861–870
Shiomi M (2020) The history of the WHHL rabbit, an animal model of familial hypercholesterolemia (II)-Contribution to the development and validation of the therapeutics for hypercholesterolemia and atherosclerosis. J Atheroscler Thromb 27:119–131. https://doi.org/10.5551/jat.RV17038-2
Stice SL, Robl JM (1988) Nuclear reprogramming in nuclear transplant rabbit embryos. Biol Reprod 39:657–664
Sugimoto H, Kida Y, Miyamoto Y et al (2012) Growth and development of rabbit oocytes in vitro: Effect of fetal bovine serum concentration on culture medium. Theriogenology 78:1040–1047. https://doi.org/10.1016/j.theriogenology.2012.04.007
Tancos Z, Nemes C, Polgar Z et al (2012) Generation of rabbit pluripotent stem cell lines. Theriogenology 78:1774–1786
Teixeira M, Commin L, Gavin-Plagne L et al (2018) Rapid cooling of rabbit embryos in a synthetic medium. Cryobiology 85:113–119. https://doi.org/10.1016/j.cryobiol.2018.07.006
Telford NA, Watson AJ, Schultz GA (1990) Transition from maternal to embryonic control in early mammalian development: a comparison of several species. Mol Reprod Dev 26:90
Vicente JS, Garciá-Ximénez F (1993) Effect of recipient doe genotype on survival rate at birth of frozen rabbit embryos. Reprod Nutr Dev 33:229–234
Vicente JS, Marco-Jiménez F, Pérez-García M et al (2022) Oocyte quality and in vivo embryo survival after ovarian stimulation in nulliparous and multiparous rabbit does. Theriogenology 189:53–58. https://doi.org/10.1016/j.theriogenology.2022.06.003
Visconti PE, Krapf D, De La Vega-Beltrán JL et al (2011) Ion channels, phosphorylation and mammalian sperm capacitation. Asian J Androl 13:395–405
Viudes-De-Castro MP, Mocé E, Vicente JS et al (2005) In vitro Evaluation of in vivo Fertilizing Ability of Frozen Rabbit Semen. Reprod Domest Anim 40:136–140
Viudes-de-Castro MP, Marco-Jiménez F, Más Pellicer A et al (2019) A single injection of corifollitropin alfa supplemented with human chorionic gonadotropin increases follicular recruitment and transferable embryos in the rabbit. Reprod Domest Anim 54:696–701. https://doi.org/10.1111/rda.13411
Wang HJ, Lin AX, Zhang ZC, Chen YF (2001) Expression of porcine growth hormone gene in transgenic rabbits as reported by green fluorescent protein. Anim Biotechnol 12:101–110. https://doi.org/10.1081/ABIO-100108336
Wang HL, Sui HS, Liu Y et al (2009) Dynamic changes of germinal vesicle chromatin configuration and transcriptional activity during maturation of rabbit follicles. Fertil Steril 91:1589–1594. https://doi.org/10.1016/j.fertnstert.2008.10.071
Wilmut I, Bai Y, Taylor J (2015) Somatic cell nuclear transfer: Origins, the present position and future opportunities. Philos Trans Roy Soc B Biol Sci 370. https://doi.org/10.1098/rstb.2014.0366
Xu J, Zhang J, Yang D et al (2021) Gene editing in rabbits: unique opportunities for translational biomedical research. Front Genet 12:1–12. https://doi.org/10.3389/fgene.2021.642444
Yanagimachi R, Chang MC (1963) Fertilization of hamster eggs in vitro. Nature 200:281–282. https://doi.org/10.1038/200281b0
Yang D, Xu J, Zhu T et al (2014) Effective gene targeting in rabbits using RNA-guided Cas9 nucleases. J Mol Cell Biol 6:97–99. https://doi.org/10.1093/jmcb/mjt047
Zeng SM, Zhu SE, Wang YS et al (1999) An efficient method for in vitro fertilization in rabbits. Anim Biotechnol 10:15–23. https://doi.org/10.1080/10495399909525918
Zheng Y-L, Jiang M-X, Zhang Y-L et al (2004) Effects of oocyte age, cumulus cells and injection methods on in vitro development of intracytoplasmic sperm injection rabbit embryos. Zygote 12:75–80. https://doi.org/10.1017/S0967199404002643
Zhou X, Yin M, Jiang W et al (2013) Electrical activation of rabbit oocytes increases fertilization and embryo development by intracytoplasmic sperm injection using sperm from deceased male. J Assist Reprod Genet 30:1605–1610. https://doi.org/10.1007/s10815-013-0113-z
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2024 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Garcia-Garcia, R.M., Jordán-Rodríguez, D., Gimeno-Martos, S., Rebollar, P.G., Lorenzo, P.L., Arias-Alvarez, M. (2024). Assisted Reproductive Technologies. In: Simões, J., Monteiro, J.M. (eds) Veterinary Care of Farm Rabbits. Springer, Cham. https://doi.org/10.1007/978-3-031-44542-2_13
Download citation
DOI: https://doi.org/10.1007/978-3-031-44542-2_13
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-44541-5
Online ISBN: 978-3-031-44542-2
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)