Rabbit Development

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Introduction

Rabbit.jpg

As an embryological tool, the rabbit (Taxon- Oryctolagus cuniculus) along with human was a species which show birth defects with thalidomide (teratogenic effects not detected with prior testing on other species).

These animals are herbivores with a very high breeding rate and number of offspring produced. Rabbit ovulation is induced by mating allowing an accurate staging of embryonic age and pregnancy.


Rabbit Links: 2009 Student Project | Category:Rabbit | Animal Development
Historic Embryology - Rabbit: 1889 Uterus and Embryo | 1905 Normal Plates | 1908 Pancreas | 1908 Pharyngeal Pouches | 1909 Lymph glands | 1918 Pituitary | 1935 Oocyte | 1935 Somites

Some Recent Findings

  • Gonad differentiation in the rabbit: evidence of species-specific features[1] "The rabbit is an attractive species for the study of gonad differentiation because of its 31-day long gestation, the timing of female meiosis around birth and the 15-day delay between gonadal switch and the onset of meiosis in the female. ...Firstly, the peak of SRY gene expression that is observed in early differentiated XY gonads in numerous mammals was also seen in the rabbit, but this expression was maintained at a high level until the end of puberty. Secondly, a peak of aromatase gene expression was observed at two-thirds of the gestation in XX gonads as in many other species except in the mouse. Thirdly, the expression of STRA8 and DMC1 genes (which are known to be specifically expressed in germ cells during meiosis) was enhanced in XX gonads around birth but also slightly and significantly in XY gonads at the same time, even though no meiosis occurs in XY gonad at this stage."
  • Stability of the reproductive variables and fetal malformations from control animals and animals treated with thalidomide in Kbl:JW rabbits over two decades[2] "We retrospectively analyzed the reproductive variables and the spontaneous malformations in the historical control data from the embryo-fetal development studies conducted in our laboratories with Kbl:JW rabbits over two decades (1990-2010) and fetal malformations induced by thalidomide in 1988, 1995 and 2007. ...Therefore, it is concluded that Kbl:JW rabbit is one of the useful rabbit strains to evaluate the effects of test substances on embryo-fetal development, especially in view of the chronological stability of spontaneous or drug-induced malformations in the fetuses." Thalidomide
  • Rabbit whole embryo culture[3] "Although the rabbit is used extensively in developmental toxicity testing, relatively little is known about the fundamental developmental biology of this species let alone mechanisms underlying developmental toxicity. This paucity of information about the rabbit is partly due to the historic lack of whole embryo culture (WEC) methods for the rabbit, which have only been made available fairly recently. ... During this 48 h culture period, major phases of organogenesis can be studied including cardiac looping and segmentation, neural tube closure, and development of anlagen of the otic system, eyes and craniofacial structures, somites and early phases of limb development (up to bud stage), as well as expansion and closure of the visceral yolk sac around the embryo."
  • Ultrasonographic characterisation of prenatal development in European brown hares (Lepus europaeus PALLAS, 1778) [4] "In contrast with the European rabbit, a distant relative, European hares give birth to precocial young. A comparison of the prenatal growth rate of both species suggests that the precocial state of the hare neonate is a more recently derived evolutionary characteristic, whereas the altricial condition of rabbits represents the ancestral mode."
  • Promoter analysis of the rabbit POU5F1 gene and its expression in preimplantation stage embryos [5] "The POU5F1 gene encodes the octamer-binding transcription factor-4 (Oct4). It is crucial in the regulation of pluripotency during embryonic development and widely used as molecular marker of embryonic stem cells (ESCs). ...Notably, we are the first to report that the rabbit POU5F1 is not restricted to ICM cells only, but it is expressed in trophoblast cells as well."
More recent papers  
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This table shows an automated computer PubMed search using the listed sub-heading term.

  • Therefore the list of references do not reflect any editorial selection of material based on content or relevance.
  • References appear in this list based upon the date of the actual page viewing.

References listed on the rest of the content page and the associated discussion page (listed under the publication year sub-headings) do include some editorial selection based upon both relevance and availability.

Links: References | Discussion Page | Pubmed Most Recent | Journal Searches


Search term: Rabbit Embryology

Ibrahim Halil Ural, Kerem Alptekin, Aysegul Ketenci, Seyhun Solakoglu, Hasan Alpak, Süleyman Özyalçın Fibroblast Transplantation Results to the Degenerated Rabbit Lumbar Intervertebral Discs. Open Orthop J: 2017, 11;404-416 PubMed 28603572

Nikola Bijelić, Tatjana Belovari, Maja Tolušić Levak, Mirela Baus Lončar Localization of trefoil factor family peptide 3 in epithelial tissues originating from the three germ layers of developing mouse embryo. Bosn J Basic Med Sci: 2017; PubMed 28485250

Figen Sevil-Kilimci, Mutlu Cobanoglu, Mehmet K Ocal, Deniz Korkmaz, Emre Cullu Effects of Tibial Rotational-guided Growth on the Geometries of Tibial Plateaus and Menisci in Rabbits. J Pediatr Orthop: 2017; PubMed 28471817

Michal Kyllar, Barbora Putnová, Vladimír Jekl, Ladislav Stehlík, Marcela Buchtová, Jan Štembírek Diagnostic imaging modalities and surgical anatomy of the temporomandibular joint in rabbits. Lab. Anim.: 2017;23677217702178 PubMed 28443382

O Yoruk, A Tatar, O N Keles, A Cakir The value of Nigella sativa in the treatment of experimentally induced rhinosinusitis. [Potenziale della Nigella sativa nel trattamento della rinosinusite indotta in setting sperimentale.] Acta Otorhinolaryngol Ital: 2017, 37(1);32-37 PubMed 28374868

Taxon

Oryctolagus cuniculus

Taxonomy Id: 9986 Rank: species

Genetic code: Translation table 1 (Standard) Mitochondrial genetic code: Translation table 2 Other names: New Zealand rabbit[includes], rabbits[common name], European rabbit[common name], Japanese white rabbit[common name], domestic rabbit[common name], rabbit[common name], Lepus cuniculus[misnomer]

Lineage( abbreviated ): Eukaryota; Metazoa; Chordata; Craniata; Vertebrata; Mammalia; Eutheria; Lagomorpha; Leporidae; Oryctolagus

Genome

  • The Oryctolagus cuniculus haploid genome is estimated to be 3500 Mb.
  • The diploid genome is organized in 21 pairs of autosomes and two sex chromosomes.
  • Rabbit gene sequences are more similar to human sequences than rodent ones.
Links: Genome Project Report

Rabbit Reproductive Cycle

  • Rabbits are seasonal breeders with the peak of reproductive activity occurring in the spring and early summer.
  • The female is always in estrus and mating induces ovulation (reflex ovulators).
  • Following mating the ovarian follicles remain active for 12 to 16 days if the doe is not fertilized.
Rabbit-ovulation.jpg
 ‎‎Ovulation
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Developmental Timeline

Sizeswithscale.JPG
Early growth of the rabbit morula and blastocyst.[6]

Early development data from an in vitro development study.[7]

Fertilization - penetration of most ova during the first hour after ovulation.
  1. 0-16 h - pronuclei
  2. 16-22 h - 2 cell
  3. 22-29 h - 4 cell
  4. 29-32 h - 8 cell
  5. 32-77h - morula
  6. 77-98h - blastocyst
  7. 98h + - hatching blastocyst
  8. 6 Days - gastrulation starts.
Gastrulation planar cell move icon.jpg
 ‎‎Planar Movement
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Gastrulation

Gonad Development

Rabbit gonad timeline.jpg

Timeline of rabbit gonad development.[1]

Day post coïtum (dpc)

  • 9 - first germ cells are detected in both sexes.
  • 14 - gonad macroscopically evident, the mesonephros and gonads are still connected and interactions between tissues are probable.
  • 16 - most germ cells already entered the genital ridges (crests).
  • 16 to 25 - regression of the mesonephros.
  • 23 - gonadal and mesonephric tissues are separated by connective tissue. Thought to prevent the migration of cells and other substances.

Days post partum (dpp)

  • birth - XX gonads first signs of meiosis.
  • 50 - XY gonads first signs of meiosis.
  • 70 - blood-testis barrier is definitively complete.

(text modified from reference[1])


Links: Genital System Development

Historic Images

The following plates are from Normal Plates of the Development of Vertebrates Vol. 5. 1905 Rabbit (Lepus cuniculus) by Charles S. Minot and Edwing Taylor.

Keibel1905 plate01.jpg Keibel1905 plate02.jpg Keibel1905 plate03.jpg

Pincus G. and Enzmann EV. The Comparative Behavior of Mammalian Eggs in Vivo and in Vitro. (1935) J Exp Med. 62(5):665-75. PMID 19870440

The following drawings were compiled in the textbooks: Bailey, F.R. and Miller, A.M. (1921). Text-Book of Embryology. New York: William Wood and Co; Foster, M., Balfour, F. M., Sedgwick, A., & Heape, W. (1883). The Elements of Embryology. (2nd ed.). London: Macmillan and Co.

Foster096.jpg Rabbit's ovum between 70-90 hours after impregnation, after E. van Beneden.
Bailey066.jpg Historic drawing of a Transverse sections of embryonic disks of rabbit, (a) Kolliker, (b) Rabl.
a, section through primitive streak of embryo of 6 days and 18 hours; b, section through Hensen's node of embryo of 7 days and 3 hours.
Bailey078.jpg Transverse section through primitive groove of rabbit embryo, van Beneden.
Bailey079.jpg Transverse section through primitive groove of rabbit embryo, van Beneden.
Foster106.jpg Embryo rabbits of about nine days from the dorsal side, Kolliker.
Foster107.jpg Embryo rabbit of about nine days transverse section through the head, Kolliker. B. is a more highly magnified representation of part of A.
Bailey161.jpg Surface view of area vasculosa of a rabbit embryo of 11 days, van Beneden and Julin.
Foster108.jpg Advanced embryo of a rabbit (about twelve days), by Mr Weldon.


Limb Vasculature (veins)
Bailey203.jpg Bailey204.jpg Bailey205.jpg
Rabbit embryo of 14 days (11 mm), modified from Lewis. Rabbit embryo of 14 days and 18 hours (14.5 mm), modified from Lewis. Rabbit embryo of 17 days (21 mm), modified from Lewis.

Rabbit Placentation

Rabbit implantation and placentation is a centric (or fusion) type, where the blastocyst adheres only to the epithelial cells (apical region) by trophectoderm forming projections.[8]

Neural Development

The data below is summarised from an excellent study of early neural development in the rabbit.[9] The same authors have studied neural development in the pig.

  • 6 - 8 somite stage - the flat neural plate transforms into a V-shaped neural groove (beginning at rhombo-cervical level)
  • 8 and 9 somite stage - multiple closure sites occur simultaneously at three levels
  1. incipient pros-mesencephalic transition
  2. incipient mes-rhombencephalic transition
  3. level of the first pairs of somites

results in four transient neuropores

anterior neuropore

  • 9-11 somite stages - anterior and rhombencephalic neuropores close
  • mesencephalic neuropore is very briefly present

posterior neuropore

  • largest and remains open longest
  • 9-10 somite stages - tapered (cranial) portion closes fast within
  • wide (caudal) portion closes up to a narrow slit
  • further closure slows
  • 22 somite stage - full closure occurs

compared with chick and mouse - sequence of multiple site closure resembles that of the mouse embryo, but other important aspects of neurulation resemble those of the chick embryo. In contrast to mouse and chick, no time lag between closure at the three closure sites in the rabbit was seen

Ultrasound

Ultrasound day16 rabbit.jpg
 ‎‎Rabbit Embryo
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Ultrasound of a 16 day rabbit embryo.

Rabbit Immune Development

Rabbits generate their antibody repertoire in three stages.[10]

  1. Neonatal repertoire is generated by B lymphopoiesis in fetal liver and bone marrow (limited by preferential V(H) gene segment usage).
  2. Between 4 and 8 weeks after birth gut-associated lymphoid tissue (GALT) a complex primary antibody repertoire.
  3. The primary antibody repertoire is subsequently modified during antigen-dependent immune responses (the secondary repertoire).

Rabbits uniquely develop a primary antibody repertoire through somatic diversification of Ig genes (dependent on intestinal microbial flora).

The esacculus rotundus is located at the ileocaecal junction as an enlargement of the large intestine and contains lymphoid tissue.

Postnatal Rabbit Growth

Postnatal growth data from 2 to 34 weeks of age at biweekly intervals for New Zealand white rabbit.[11]

  • 17 male and 12 female rabbits, with the data tabulated separately.
  • Skeletal growth was complete at 28 weeks, with the 34 week values mature adult lengths.

Mean body weight

  • 2 weeks of age was 6% that at 34 weeks
  • 16 weeks was 72% of the weight at 34 weeks
  • weight continued to increase in the adult.

Mean body length

  • 2 weeks was 40% that at 34 weeks
  • 16 weeks was 91% of mature adult

Mean femoral length

  • 2 weeks was 38% of adult
  • 16 weeks was 95% of adult

Mean tibial length

  • 2 weeks was 38% of adult
  • 16 weeks was 94% of adult

References

  1. 1.0 1.1 1.2 Nathalie Daniel-Carlier, Erwana Harscoët, Dominique Thépot, Aurélie Auguste, Eric Pailhoux, Geneviève Jolivet Gonad differentiation in the rabbit: evidence of species-specific features. PLoS ONE: 2013, 8(4);e60451 PubMed 23593221 Cite error: Invalid <ref> tag; name "PMID23593221" defined multiple times with different content Cite error: Invalid <ref> tag; name "PMID23593221" defined multiple times with different content
  2. Yoshinori Kawamura, Kiyoshi Matsumoto, Keiichiro Sato Stability of the reproductive variables and fetal malformations from control animals and animals treated with thalidomide in Kbl:JW rabbits over two decades. Congenit Anom (Kyoto): 2012, 52(4);191-202 PubMed 23181494
  3. Valerie A Marshall, Edward W Carney Rabbit whole embryo culture. Methods Mol. Biol.: 2012, 889;239-52 PubMed 22669668
  4. Kathleen Roellig, Frank Goeritz, Thomas B Hildebrandt Ultrasonographic characterisation of prenatal development in European brown hares (Lepus europaeus PALLAS, 1778): an evolutionary approach. Reprod. Fertil. Dev.: 2010, 22(2);448-58 PubMed 20047730
  5. Julianna Kobolak, Katalin Kiss, Zsuzsanna Polgar, Solomon Mamo, Claire Rogel-Gaillard, Zsuzsanna Tancos, Istvan Bock, Arpad G Baji, Krisztina Tar, Melinda K Pirity, Andras Dinnyes Promoter analysis of the rabbit POU5F1 gene and its expression in preimplantation stage embryos. BMC Mol. Biol.: 2009, 10;88 PubMed 19732419
  6. S M Warner, F V Conlon, M T Kane Inositol transport in preimplantation rabbit embryos: effects of embryo stage, sodium, osmolality and metabolic inhibitors. Reproduction: 2003, 125(4);479-93 PubMed 12683919
  7. Fowzia Sultana, Masanori Hatori, Nobuhiro Shimozawa, Takashi Ebisawa, Tadashi Sankai Continuous observation of rabbit preimplantation embryos in vitro by using a culture device connected to a microscope. J. Am. Assoc. Lab. Anim. Sci.: 2009, 48(1);52-6 PubMed 19245751
  8. Kevin Y Lee, Francesco J DeMayo Animal models of implantation. Reproduction: 2004, 128(6);679-95 PubMed 15579585
  9. M C Peeters, C Viebahn, J W Hekking, H W van Straaten Neurulation in the rabbit embryo. Anat. Embryol.: 1998, 197(3);167-75 PubMed 9543335
  10. D Lanning, X Zhu, S K Zhai, K L Knight Development of the antibody repertoire in rabbit: gut-associated lymphoid tissue, microbes, and selection. Immunol. Rev.: 2000, 175;214-28 PubMed 10933605
  11. I Masoud, F Shapiro, R Kent, A Moses A longitudinal study of the growth of the New Zealand white rabbit: cumulative and biweekly incremental growth rates for body length, body weight, femoral length, and tibial length. J. Orthop. Res.: 1986, 4(2);221-31 PubMed 3712130


Reviews

Bernd Fischer, Pascale Chavatte-Palmer, Christoph Viebahn, Anne Navarrete Santos, Veronique Duranthon Rabbit as a reproductive model for human health. Reproduction: 2012, 144(1);1-10 PubMed 22580370

| Reproduction Bernd Püschel, Eva Bitzer, Martin Blum, Christoph Viebahn Mounting, embedding, and sectioning of early rabbit embryos. Cold Spring Harb Protoc: 2010, 2010(1);pdb.prot5356 PubMed 20150115

Bernd Püschel, Nathalie Daniel, Eva Bitzer, Martin Blum, Jean-Paul Renard, Christoph Viebahn The rabbit (Oryctolagus cuniculus): a model for mammalian reproduction and early embryology. Cold Spring Harb Protoc: 2010, 2010(1);pdb.emo139 PubMed 20150104


Articles

Romia Hassoun, Peter Schwartz, Detlef Rath, Christoph Viebahn, Jörg Männer Germ layer differentiation during early hindgut and cloaca formation in rabbit and pig embryos. J. Anat.: 2010, 217(6);665-78 PubMed 20874819

Jan Idkowiak, Gunnar Weisheit, Christoph Viebahn Polarity in the rabbit embryo. Semin. Cell Dev. Biol.: 2004, 15(5);607-17 PubMed 15271306


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Cite this page: Hill, M.A. 2017 Embryology Rabbit Development. Retrieved June 24, 2017, from https://embryology.med.unsw.edu.au/embryology/index.php/Rabbit_Development

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