Axolotl Development

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Introduction

Adult Axolotl

Axolotls (Ambystoma mexicanum) are the larval form of the Mexican Salamander amphibian and are an animal model used in limb regeneration studies. Axolotls take about 12 months to reach sexual maturity, males release spermatophore into the water and the female may take them up, eventually laying around 200-600 eggs on plants. Egg development takes two weeks, the tadpole-like young remain attached to the plants for a further two weeks. Loss or amputation of the axolotl limb leads to the regeneration of the lost limb from trunk tissue, thereby repeating a developmental sequence as a repair process.


The sequence of axolotl embryonic developmental stages was characterised in the late 1980's.[1]


Links: Category:Axolotl | Category:Salamander | Animal Development

Some Recent Findings

  • Dual embryonic origin and patterning of the pharyngeal skeleton in the axolotl (Ambystoma mexicanum)[2] "The impressive morphological diversification of vertebrates was achieved in part by innovation and modification of the pharyngeal skeleton. Extensive fate mapping in amniote models has revealed a primarily cranial neural crest derivation of the pharyngeal skeleton....Our fate map confirms a dual embryonic origin of the pharyngeal skeleton in urodeles, including derivation of basibranchial 2 from mesoderm closely associated with the second heart field. Additionally, heterotopic transplantation experiments reveal lineage restriction of mesodermal cells that contribute to pharyngeal cartilage. The mesoderm-derived component of the pharyngeal skeleton appears to be particularly sensitive to retinoic acid (RA): administration of exogenous RA leads to loss of the second basibranchial, but not the first. Neural crest was undoubtedly critical in the evolution of the vertebrate pharyngeal skeleton, but mesoderm may have played a central role in forming ventromedial elements, in particular. When and how many times during vertebrate phylogeny a mesodermal contribution to the pharyngeal skeleton evolved remain to be resolved."
  • Stochastic specification of primordial germ cells from mesoderm precursors in axolotl embryos[3] "A common feature of development in most vertebrate models is the early segregation of the germ line from the soma. For example, in Xenopus and zebrafish embryos primordial germ cells (PGCs) are specified by germ plasm that is inherited from the egg; in mice, Blimp1 expression in the epiblast mediates the commitment of cells to the germ line. How these disparate mechanisms of PGC specification evolved is unknown. Here, in order to identify the ancestral mechanism of PGC specification in vertebrates, we studied PGC specification in embryos from the axolotl (Mexican salamander), a model for the tetrapod ancestor. In the axolotl, PGCs develop within mesoderm, and classic studies have reported their induction from primitive ectoderm (animal cap). We used an axolotl animal cap system to demonstrate that signalling through FGF and BMP4 induces PGCs. The role of FGF was then confirmed in vivo. We also showed PGC induction by Brachyury, in the presence of BMP4. These conditions induced pluripotent mesodermal precursors that give rise to a variety of somatic cell types, in addition to PGCs. Irreversible restriction of the germ line did not occur until the mid-tailbud stage, days after the somatic germ layers are established. Before this, germline potential was maintained by MAP kinase signalling. We propose that this stochastic mechanism of PGC specification, from mesodermal precursors, is conserved in vertebrates."
  • Regeneration of Limb Joints in the Axolotl[4] "In spite of numerous investigations of regenerating salamander limbs, little attention has been paid to the details of how joints are reformed. An understanding of the process and mechanisms of joint regeneration in this model system for tetrapod limb regeneration would provide insights into developing novel therapies for inducing joint regeneration in humans. To this end, we have used the axolotl (Mexican Salamander) model of limb regeneration to describe the morphology and the expression patterns of marker genes during joint regeneration in response to limb amputation. These data are consistent with the hypothesis that the mechanisms of joint formation whether it be development or regeneration are conserved. We also have determined that defects in the epiphyseal region of both forelimbs and hind limbs in the axolotl are regenerated only when the defect is small. As is the case with defects in the diaphysis, there is a critical size above which the endogenous regenerative response is not sufficient to regenerate the joint. This non-regenerative response in an animal that has the ability to regenerate perfectly provides the opportunity to screen for the signaling pathways to induce regeneration of articular cartilage and joints."
  • Multiple sequences and factors are involved in stability/degradation of Awnt-1, Awnt-5A and Awnt-5B mRNAs during axolotl development.[5] "Following fertilization in amphibian, early cleavage stages are maternally controlled at a post-transcriptional level before initiation of zygotic transcriptions at the mid blastula transition (MBT). ...Altogether, these results show that oocyte maturation and late cleavages following MBT are two important periods when axolotl Wnt RNAs are highly regulated."
  • The axolotl limb: a model for bone development, regeneration and fracture healing.[6] "Among vertebrates, urodele amphibians (e.g., axolotls) have the unique ability to perfectly regenerate complex body parts after amputation."
  • Expression of heat-shock protein 70 during limb development and regeneration in the axolotl.[7] "Using molecular biology and biochemical techniques, we have characterized both the spatiotemporal and quantitative expression patterns of Hsp-70 in axolotl development and regeneration. Our results show that Hsp-70 is expressed and regulated during axolotl development as in other vertebrates. Our data also demonstrate an up-regulation of the RNA transcript for Hsp-70 during limb regeneration as early as 24 hr after amputation that is maintained up to early differentiation. We also demonstrate a similar pattern of expression for the protein during regeneration. Finally, we show that axolotl Hsp-70 is induced threefold after heat-shock as observed in other vertebrates."
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.
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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.

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Search term: Axolotl Development

Akira Tazaki, Elly M Tanaka, Jifeng Fei Salamander spinal cord regeneration: the ultimate positive control in vertebrate spinal cord regeneration. Dev. Biol.: 2017; PubMed 29030146

Rodrigo Montoro, Renee Dickie Comparison of tissue processing methods for microvascular visualization in axolotls. MethodsX: 2017, 4;265-273 PubMed 28913170

Thomas L Anderson, Freya E Rowland, Raymond D Semlitsch Variation in phenology and density differentially affects predator-prey interactions between salamanders. Oecologia: 2017; PubMed 28894959

Syed F Hassnain Waqas, Anna Noble, Anh C Hoang, Grace Ampem, Manuela Popp, Sarah Strauß, Matthew Guille, Tamás Röszer Adipose tissue macrophages develop from bone marrow-independent progenitors in Xenopus laevis and mouse. J. Leukoc. Biol.: 2017; PubMed 28642277

Éric Villiard, Jean-François Denis, Faranak Sadat Hashemi, Sebastian Igelmann, Gerardo Ferbeyre, Stéphane Roy Senescence gives insights into the morphogenetic evolution of anamniotes. Biol Open: 2017; PubMed 28500032

Developmental Stages

The following stage information is based upon published staging data.[1]

Stage Time (hours) Description
1 0 Freshly laid egg in jellycoat.
2 First appearance of the first cleavage furrow and the animal pole.
3 2.5 Four cells.
4 4 Eight cells.
5-6 5.5 16 cells.
6 6.5 - 7 32 cells
7 8 - 9 64 cells
8 16 Early blastula (fall of mitotic index in animal blastomeres).
9 21 Late blastula, surface is smooth.
10 26 Early gastrula I, first sign of dorsal blastopore lip.
11 38 Middle gastrula II, Blastopore covers three quadrants. Lateral lips are formed; ventral lip is marked only by pigment accumulation. Yolk plug reaches its maximum diameter.
12 47 Late gastrula II, Blastopore has an oval or circular shape.
14 58 Early neurula II: Neural plate is broad. Neural folds are outlined and begin to rise above the surface in the head region. Embryo is slightly elongated.
15-16 59 - 63 Early neurula III and middle neurula: Neural plate is shield-shaped and becomes sunken; neural folds are raised and bound all regions of the neural plate.
17 64 Late Neurula I: Neural folds are higher; especially in the head region. Further narrowing and deepening of the neural plate occur both in the head and in the spinal regions. Hyomandibular furrow limiting the mandibular arch is slightly outlined. The segmentation of the mesodermal material begins. There are two pairs of somites.
18 66 Late neurula II: Neural plate is deeply sunken. Neural folds are closing and are especially high in the head region where three slight bulges corresponding to fore-, mid- and hindbrain vesicles are outlined. The neural folds of the spinal region are almost in contact. Hyomandibular furrow is more marked. There are two pairs of somites.
19 69 Late neurula III: Neural folds are in contact throughout, but are not yet fused. Brain curvature is quite distinct in profile; fore-, mid- and hindbrain vesicles are also distinct. The swelling of optic vesicles is outlined (barely visible in these pictures because of unfortunate perspective). Hymandibular furrows are deeper. There are three pairs of somites.
20 70 Late Neurula IV: Späte Neurulation IV: Neural folds are fused in spinal region (or are starting this process in these pictures); in brain region, they are only in contact. Optical vesicles are destinct and becoming larger. Grooves in ectoderm appear at the level of the hindbrain. A very slight swelling marks the future gill region. Mandibular arch becomes prominent and four pairs of somites are present.
22-23 73-74 Neural folds are completely fused. The gill region and the pronephros are distinct; the tailbud is slightly outlined. Five to six pairs of somites are present. Primordium of the ear is outlined as a shallow depression in the ectoderm in the region above the future hyoid arch. The hyobranchial furrow appears, outlining the boundary between the hyoid arch and the first branchial arch.
24 80 Ear pit is outlined and becomes more distinct. The hyobranchial furrow lengthens ventrally. The prophenic swelling is clearly outlined, and both the pronephros itself and the beginning of the pronephric duct are clearly visible Eight or nine pairs of somites are visible.
29 Since first cleavage, up to 97 hours have passed (sorry, I missed some hours here... ;-) ). Ear pit becomes quite distinct. The gill region is clearly outlined. The pronephric duct is clearly visible along six somites at least. The primordium of the olfactory organ appears as a tubercle on the anterior part of the head; the tailbud is gradually enlarging in all stages. Up to 16 pairs of somites are present.
30-31 110 The body of the embryo continues to straighten; the tailbud enlarges. Dorsal finfold begins at somite 14-12. A groove appears in the region of the lens primordium (visual system - i.e. eyes) The third branchial furrow becomes apparent in the dorsal part of the gill region.
32-34 115 The dorsal fin develops until it begins at somite 10.
35 122 From this stage on, the body axis from the hindbrain to the tail base are quite straight. Three external gills show ad nodules on the surface of the gill swelling. The lateral line reaches to the sixth somite. The dorsal fin begins at the fifth somite. The first chromatophores appear; heart pulsation begins.
36-37 177 Gills elongate and push venventroposteriorly. No limb buds are yet visible.
38 Filament sprouts appear as two nodules on each gill. The primordium of the operculum is visible as a fold upon the hyoid arch. Neither of the two rudiments of the perculum reaches the midline. The limb buds are slightly outlined.
39 220 The first gills have two pairs of filament sprouts; the second and third have three pairs each. The gills cover the limb buds. Both rudiments of the operculum approach the midline. The angle of the mouth begins to show.
40 240 The gills are longer and the number of filaments increases (four pairs in the first gills, six or seven pairs on the second or third gills). The rudiments of the operculum join at the middline. The angles of the mouth are marked more distinctly and limb buds protrude slightly.
41 265 The gills contunie to elongate, the number of filaments increases and they become longer. The mouth is distinctly outlined. The second lateral line runs along the flank toward the limb bud and bypasses it on the ventral side. Hatching begins.
42 296 The gills extend far beyond the forelimb buds. The mouth is completely outlined, but is not broken through.
43 With galvanic and convulsive movements the larva breaks free of the jelly coat. The mouth either is already opened or will open within the next 24 - 72 hours.


Thyroid Hormone Effects

Axolotl - thyroxine effects.jpg
The effect of thyroxine on the early larval development of the axolotl. The same control and 30 nM T4-treated (TH) sibling animals were photographed at the days postfertilization noted. T4 was added from day 14. (Bar = 1 cm.)[8]

Limb Development

Axolotl developing limb Bmp2 and Sox9.jpg

Axolotl developing limb Bmp2 and Sox9 expression and cartilage staining.[9]


Teeth Development

A study has used the axolotl as a model for tooth development.[10] Using transgenic axolotls and fate-mapping approaches they found "evidence of oral teeth derived from both the ectoderm and endoderm and, moreover, demonstrate teeth with a mixed ecto/endodermal origin. Despite the enamel epithelia having a different embryonic source, oral teeth in the axolotl display striking developmental uniformities and are otherwise identical. This suggests a dominant role for the neural crest mesenchyme over epithelia in tooth initiation and, from an evolutionary point of view, that an essential factor in teeth evolution was the odontogenic capacity of neural crest cells, regardless of possible 'outside-in' or 'inside-out' influx of the epithelium."

Additional Images

Historic Images

References

  1. 1.0 1.1 Bordzilovskaya NP, Dettlaf TA, Duhan ST, Malacinski GM: Developmental-stage series of axolotl embryos. In Developmental Biology of the Axolotl. Edited by: Armstrong JB, Malacinski GM. New York: Oxford University Press; 1989:201-219.
  2. Elizabeth M Sefton, Nadine Piekarski, James Hanken Dual embryonic origin and patterning of the pharyngeal skeleton in the axolotl (Ambystoma mexicanum). Evol. Dev.: 2015, 17(3);175-84 PubMed 25963195
  3. Jodie Chatfield, Marie-Anne O'Reilly, Rosemary F Bachvarova, Zoltan Ferjentsik, Catherine Redwood, Maggie Walmsley, Roger Patient, Mathew Loose, Andrew D Johnson Stochastic specification of primordial germ cells from mesoderm precursors in axolotl embryos. Development: 2014, 141(12);2429-40 PubMed 24917499
  4. Jangwoo Lee, David M Gardiner Regeneration of limb joints in the axolotl (Ambystoma mexicanum). PLoS ONE: 2012, 7(11);e50615 PubMed 23185640
  5. Stéphane Caulet, Hélène Pelczar, Yannick Andéol Multiple sequences and factors are involved in stability/degradation of Awnt-1, Awnt-5A and Awnt-5B mRNAs during axolotl development. Dev. Growth Differ.: 2010, 52(2);209-22 PubMed 20151991
  6. Cara Hutchison, Mireille Pilote, Stéphane Roy The axolotl limb: a model for bone development, regeneration and fracture healing. Bone: 2007, 40(1);45-56 PubMed 16920050
  7. Mathieu Lévesque, Jean-Charles Guimond, Mireille Pilote, Séverine Leclerc, Florina Moldovan, Stéphane Roy Expression of heat-shock protein 70 during limb development and regeneration in the axolotl. Dev. Dyn.: 2005, 233(4);1525-34 PubMed 15965983
  8. D D Brown The role of thyroid hormone in zebrafish and axolotl development. Proc. Natl. Acad. Sci. U.S.A.: 1997, 94(24);13011-6 PubMed 9371791 | PubMed Central | PNAS
  9. Jean-Charles Guimond, Mathieu Lévesque, Pierre-Luc Michaud, Jérémie Berdugo, Kenneth Finnson, Anie Philip, Stéphane Roy BMP-2 functions independently of SHH signaling and triggers cell condensation and apoptosis in regenerating axolotl limbs. BMC Dev. Biol.: 2010, 10;15 PubMed 20152028 | BMC Dev Biol.
  10. Vladimír Soukup, Hans-Henning Epperlein, Ivan Horácek, Robert Cerny Dual epithelial origin of vertebrate oral teeth. Nature: 2008, 455(7214);795-8 PubMed 18794902

Reviews

Malcolm Maden Axolotl/newt. Methods Mol. Biol.: 2008, 461;467-80 PubMed 19030817

Stéphane Roy, Samuel Gatien Regeneration in axolotls: a model to aim for! Exp. Gerontol.: 2008, 43(11);968-73 PubMed 18814845

S K Frost-Mason, K A Mason What insights into vertebrate pigmentation has the axolotl model system provided? Int. J. Dev. Biol.: 1996, 40(4);685-93 PubMed 8877441

H H Epperlein, J Löfberg, L Olsson Neural crest cell migration and pigment pattern formation in urodele amphibians. Int. J. Dev. Biol.: 1996, 40(1);229-38 PubMed 8735933


Articles

Hans-Georg Simon Salamanders and fish can regenerate lost structures--why can't we? BMC Biol.: 2012, 10;15 PubMed 22369645

Stéphane Caulet, Hélène Pelczar, Yannick Andéol Multiple sequences and factors are involved in stability/degradation of Awnt-1, Awnt-5A and Awnt-5B mRNAs during axolotl development. Dev. Growth Differ.: 2010, 52(2);209-22 PubMed 20151991

Cara Hutchison, Mireille Pilote, Stéphane Roy The axolotl limb: a model for bone development, regeneration and fracture healing. Bone: 2007, 40(1);45-56 PubMed 16920050

Mathieu Lévesque, Jean-Charles Guimond, Mireille Pilote, Séverine Leclerc, Florina Moldovan, Stéphane Roy Expression of heat-shock protein 70 during limb development and regeneration in the axolotl. Dev. Dyn.: 2005, 233(4);1525-34 PubMed 15965983

Holly L D Nye, Jo Ann Cameron, Ellen A G Chernoff, David L Stocum Extending the table of stages of normal development of the axolotl: limb development. Dev. Dyn.: 2003, 226(3);555-60 PubMed 12619140

D C Meuler, G M Malacinski An analysis of protein synthesis patterns during early embryogenesis of the urodele--Ambystoma mexicanum. J Embryol Exp Morphol: 1985, 89;71-92 PubMed 4093754

J Signoret Evidence of the first genetic activity required in axolotl development. Results Probl Cell Differ: 1980, 11;71-4 PubMed 7444204


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Cite this page: Hill, M.A. 2017 Embryology Axolotl Development. Retrieved October 23, 2017, from https://embryology.med.unsw.edu.au/embryology/index.php/Axolotl_Development

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