Ambystoma mexicanum, the axolotl: A versatile amphibian model for regeneration, development, and evolution studies

Cold Spring Harbor Protocols

Volumn 4, Issue 8, 2009, Pages

  Voss, S Randal ^a   Epperlein, Hans H ^b   Tanaka, Elly M ^b,c  

^a UNIVERSITY OF KENTUCKY   (United States)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 73349097865     PISSN: None     EISSN: 15596095     Source Type: Journal    
DOI: 10.1101/pdb.emo128     Document Type: Article

References (69)

1. Armstrong, JB and Malacinski, GM, eds. 1989. Developmental biology of the axolotl. Oxford University Press, NY.
2. Armstrong JB, Duhon ST, Malacinski GM. 1989. Raising the axolotl in captivity. In Developmental biology of the axolotl (eds. JB Armstrong and GM Malacinski), pp. 220-227. Oxford University Press, New York.
3. Bolker JA. 1995. Model systems in developmental biology. Bioessays 17: 451-455.
4. Brandon RA. 1989. Natural history of the axolotl and its relationship to other ambystomatid salamanders. In Developmental biology of the axolotl (eds. JB Armstrong and GM Malacinski), pp. 13-21. Oxford University Press, New York.
5. Cerny R, Lwigale P, Ericsson R, Meulemans D, Epperlein HH, Bronner-Fraser M. 2004. Developmental origins and evolution of jaws: New interpretation of 'maxillary' and 'mandibular.' Dev Biol 276: 225-236.
6. Collazo A, Fraser SE, Mabee PM. 1994. A dual embryonic origin for vertebrate mechanoreceptors. Science 264: 426-430.
7. Cotter JD, Storfer A, Page RB, Beachy CK, Voss SR. 2008. Transcriptional response of Mexican axolotis to Ambystoma tigrinum virus (ATV) infection. BMC Genomics 9: 493. doi: 10. 1186/ 1471-2164-9-493.
8. da Silva SM, Gates PB, Brockes JB. 2002. The newt ortholog of CD59 is implicated in proximodistal identity during amphibian limb regeneration. Dev Cell 3: 547-555.
9. Detwiler SR. 1937. Observations upon the migration of neural crest cells, and upon the development of the spinal ganglia and vertebral arches in Ambystoma. Am J Anat 61: 63-94.
10. Developmental Biology of Urodeles. 1996, Int J Dev Biol 40: 613-916.
11. DuShane GP. 1938. Neural fold derivatives in the amphibia: Pigment cells, spinal ganglia and Rohon-Beard cells. J Exp Zool 78: 485-503.
12. Echeverri K, Tanaka EM. 2002. Ectoderm to mesoderm lineage switching during axolotl tail regeneration. Science 298: 1993-1996.
13. Echeverri K, Tanaka EM. 2003. Electroporation as a tool to study in vivo spinal cord regeneration. Dev Dyn 226: 418-425.
14. Echeverri K, Tanaka EM. 2005. Proximodistal patterning during limb regeneration. Dev Biol 279: 391-401.
15. Endo T, Bryant SV, Gardiner DM. 2004. A stepwise model system for limb regeneration. Dev Biol 270: 135-145.
16. Epperlein HH, Meulemans D, Bronner-Fraser M, Steinbeisser H, Selleck MAJ. 2000. Analysis of cranial neural crest migratory pathways in axolotl using cell markers and transplantation. Development 127: 2751-2761.
17. Epperlein HH, Selleck MA, Meulemans D, Mchedlishvili L, Cerny R, Sobkow L, Bronner-Fraser M. 2007. Migratory patterns and developmental potential of trunk neural crest cells in the axolotl embryo. Dev Dyn 236: 389-403.
18. Fitzpatrick B3, Shaffer HB. 2007. Hybrid vigor between native and introduced salamanders raises new challenges for conservation. Proc Natl Acad Sci 104: 15793-15798.
19. Gollisch T, Meister M. 2008. Rapid neural coding in the retina with relative spike latencies. Science 319: 1108-1111.
20. Gould SJ. 1977. Ontogeny and phylogeny. Harvard University Press, Cambridge, MA.
21. Habermann B, Bebin AG, Herklotz S, Volkmer M, Eckelt K, Pehlke K, Epperlein HH, Schackert HK, Wiebe G, Tanaka EM. 2004. An Ambystoma mexicanum EST sequencing project: Analysis of 17,352 expressed sequence tags from embryonic and regenerating blastema cDNA libraries. Genome Biol 5: R67. doi: 10.1186/gb-2004-5-9-r67.
22. Harlow DE, Barlow LA. 2007. Embryonic origin of gustatory cranial sensory neurons. Dev Biol 310: 317-328.
23. Hess K, Steinbeisser H, Kurth T, Epperlein HH. 2008. Bone morphogenetic protein-4 and Noggin signaling regulates pigment cell distribution in the axolotl trunk. Differentiation 76: 206-218.
24. Humphrey RR. 1967. Albino axolotls from an albino tiger salamander through hybridization. J Hered 58: 95-101.
25. Johnson AD, Crother B, White ME, Patient R, Bachvarova RF, Drum M, Masi T. 2003. Regulative germ cell specification in axolotl embryos: A primitive trait conserved in the mammalian lineage. Philos Trans R Soc Lond B Biol Sci 358: 1371-1379.
26. Kawakami Y, Rodriguez Esteban C. Raya M, Kawakami H, Martí M, Dubova I, Izpisúa Belmonte JC. 2006. Wnt/β-catenin signaling regulates vertebrate limb regeneration. Genes & Dev 20: 3232-3237.
27. Khattak S, Tanaka EM. 2009. Axolotl (Ambystoma mexicanum) in vitro fertilization. Cold Spring Harb Protoc (this issue). doi: 10.1101/ pdb.prot5263.
28. Khattak S, Richter T, Tanaka EM. 2009. Generation of transgenic axolotis (Ambystoma mexicanum). Cold Spring Harb Protoc (this issue). doi: 10.1101/pdb.prot5264.
29. Kragl M, Tanaka EM. 2009a. Grafting axolotl (Ambystoma mexicanum) limb skin and cartilage from GFP+ donors to normal hosts. Cold Spring Harb Protoc (this issue). doi: 10.1101/pdb.prot5266.
30. Kragi M, Tanaka EM. 2009b. Axolotl (Ambystoma mexicanum) limb and tail amputation. Cold Spring Harb Protoc (this issue). doi: 10.1101/pdb.prot5267.
31. Kragi M, Knapp D, Nacu E, Khattak S, Maden M, Epperlein HH, Tanaka EM. 2009. Cells keep a memory of their tissue origin during axolotl limb regeneration. Nature 460: 60-65.
32. Kumar A, Brockes JP. 2007. Preparation of cultured myofibers from larval salamander limbs for cellular plasticity studies. Nat Protoc 2: 939-947.
33. Lawson KA, Dunn NR, Roelen BA, Zeinstra LM, Davis AM, Wright CV, Korving JP, Hogan BL. 1999. Bmp4 is required for the generation of primordial germ cells in the mouse embryo. Genes & Dev 13: 424-436.
34. Löfberg JA, Nynäs-McCoy A, Olsson C, Jönsson L, Perris R. 1985. Stimulation of initial neural crest cell migration in the axolotl embryo by tissue grafts and extracellular matrix transplanted on microcarriers. Dev Biol 107: 442-459.
35. Malacinski GM. 1989. Developmental genetics. In Developmental biology of the axolotl (eds. 313 Armstrong and GM Malacinski), pp. 102-109. Oxford University Press, New York.
36. Mchedlishvili L, Epperlein HH, Telzerow A, Tanaka EM. 2007. A clonal analysis of neural progenitors during axolotl spinal cord regeneration reveals evidence for both spatially restricted and multipotent progenitors. Development 134: 2083-2093.
37. Mercader N, Tanaka EM, Torres M. 2005. Proximodistal identity during vertebrate limb regeneration is regulated by Meis homeodomain proteins. Development 132: 41-31-4142.
38. Mescher AL, Neff AW. 2006. Limb regeneration in amphibians: Immunological considerations. ScientificlWorldJournal Suppl. 1 6: 1-11.
39. Monaghan JR, Walker JA, Page RB, Putta S, Beachy CK, Voss SA. 1007. Early gene expression during natural spinal cord regeneration in the salamander Ambystoma mexicanum. J Neurochem 101: 27-40.
40. Monaghan JR, Epp L, Putta S, Page RB, Walker JA, Zhu W, Pao GM, Verma IM, Hunter T, Bryant SV, et al. 2009. Microarray and DNA sequence analysis of transcription during nerve-dependent limb regeneration. BMC Biology 7: 1. doi: 10.1186/1741-7007-7-1.
41. Nacu E, Knapp D, Tanaka EM, Epperlein HH. 2009. Axolotl (Ambystoma mexicanum) embryonic transplantation methods. Cold Spring Harb Protoc (this issue). doi: 10.1101/pdb.prot5265.
42. Nieuwkoop PD. 1996. What are the key advantages and disadvantages of urodele species compared to anurans as a model system for experimental analysis of early development? Int J Dev Biol 40: 617-619.
43. Northcutt RG, Catania KC, Criley BB. 1994. Development of lateral line organs in the axolotl. J Comp Neurol 340: 480-514.
44. Page RB, Voss SR. 2009. Induction of metamorphosis in axolotis (Ambystoma mexicanum). Cold Spring Harb Protoc (this issue). doi: 10.1101/pd1b.prot5268.
45. Page RB, Monaghan JR, Samuels AK, Smith JJ, Beachy CK, Voss SR. 2007. Microarray analysis identities keratin loci as sensitive biomarkers for thyroid hormone disruption in salamanders (Ambystoma). Comp Biochem Physiol Part C 145, 15-27.
46. Page RB, Voss SR, Samuels AK, Smith JJ, Putta, S, Beachy CK. 2008. Effect of thyroid hormone concentration on the transcriptional response underlying induced metamorphosis in the Mexican axolotl (Ambystoma). BMC Genomics 9: doi: 10.1186/1471-2164-9-78.
47. Page RB, Monaghan JR, Walker JA, Voss SR. 2009. An integrative model of transcriptional and morphological changes during TH-induced metamorphosis of the Mexican axolotl. Gen Comp Endo 162: 219-232.
48. Parichy DM, Stigson M, Voss SR. 1999. Genetic analysis of steel and the PG-M/Versican-encoding gene AxPG as candidates for the white (d) pigmentation mutant in the salamander Ambystoma mexicanum. Dev Genes Evol 209: 349-356.
49. Petranka JW. 1998. Salamanders of the United States and Canada. Smithsonian Institution Press, Washington, DC.
50. Putta S, Smith JJ, Walker JA, Rondet M, Weisrock D, Monaghan JR, Samuels AK, Kump K, King DC, Maness NJ, et al. 2004. From biomedicine to natural history research: Expressed sequence tag resources for ambystomatid salamanders. BMC Genomics 5: 54. doi: 10.1186/ 1471-2164-5-54.
51. Robertson AV, Ramsden C, Niedzwiecki J, Fu J, Bogart JP. 2006. An unexpected recent ancestor of unisexual Ambystoma. Mol Ecol 15: 3339-3351.
52. Roy S, Gardiner DM, Bryant SV. 2000. Vaccinia as a tool for functional analysis in regenerating limbs: Ectopic expression of Shh. Dev Biol 218: 199-205.
53. Schroeder, BC, Cheng T, Jan YN, Jan LY. 2008. Expression cloning of TMEM16A as a calcium-activated chloride channel subunit. Cell 134: 1019-1029.
54. Shook DR, Majer C, Keller R. 2002. Urodeles remove mesoderm from the superficial layer by subduction through a bilateral primitive streak. Dev Biol 248: 220-239.
55. Smith HM. 1989. Discovery of the axolotl and its early history in biological research. In Developmental biology of the axolotl (eds. JB Armstrong and GM Malacinski), pp. 3-12. Oxford University Press, New York.
56. Smith JJ, Voss SR. 2007. Bird and mammal sex-chromosome orthologs map to the same autosomal region in a salamander (ambystoma). Genetics 177: 607-613.
57. Smith JJ, Kump K, Walker JA, Parichy DM, Voss SR. 2005a. A comprehensive expressed sequence tag linkage map for tiger. salamander and Mexican axolotl: Enabling gene mapping, comparative genomics, and PCR marker development in Ambystoma. Genetics 171: 1161-1171.
58. Smith JJ, Putta S, Walker JA, Kump DK, Samuels AK, Monaghan JR, Weisrock DW, Staben C. Voss SR. 2005b. Sal-Site: Integrating new and existing ambystomatid research and information resources. BMC Genomics 6: 181. doi: 10.1186/1471-2164-6-181.
59. Smith JJ, Putta S, Zhu W, Pao GM, Verma IM, Hunter T, Bryant SV, Gardiner DM, Harkins TT, Voss SR. 2009. Genic regions of a large salamander genome contain long introns and novel genes. BMC Genomics 10: 19. doi: 10.1186/1471-2164-10-19.
60. Sobkow L, Epperlein HH, Herklotz S, Straube WL, Tanaka EM. 2006. A germline GFP transgenic axolotl and its use to track cell fate: Dual origin of the fin mesenchyme during development and the fate of blood cells during regeneration. Dev Biol 290: 386-397.
61. Soukup V, Epperlein HH, Horácek I, Cerny R. 2008. Dual epithelial origin of vertebrate oral teeth. Nature 455: 795-798.
62. Spemann H, Mangold H. 1924. Über induktion von embryonalanlagen durch, implantation artfremder organisatoren. Arch mikrosk Anat EntwMech 100: 599-638.
63. Stocum DL. 1984. The urodele limb regeneration blastema. Determination and organization of the morphogenetic field. Differentiation 27: 13-28.
64. Umanski EE. 1938. The regeneration potencies of axolotl skin studied by means of exclusion of the regeneration capacity of tissues through exposure to X-rays. Bull Biol Med Exp USSR 6: 141-145.
65. Voss SR, Shaffer HB. 1996. What insights into the developmental traits of urodeles does the study of interspecific hybrids provide? Int J Dev Biol 40: 885-893.
66. Voss SR, Smith JJ. 2005. Evolution of salamander life cycles: A major-effect quantitative trait locus contributes to discrete and continuous variation for metamorphic timing. Genetics 170: 275-281.
67. Ying Y, Zhao GQ. 2001. Cooperation of endoderm-derived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev Biol 232: 484-492.
68. Ying Y, Qi X, Zhao GQ. 2001. Induction of primordial germ cells from murine epiblasts by synergistic action of BMP4 and BMP8B signaling pathways. Proc Natl Acad Sci 98: 7858-7862.
69. Zhang C, Pietras KM, Sferrazza GF, Jia P, Athauda G, Rueda-de-Leon E, Maier JA, Dube DK, Lemanski SL, Lemanski LF, 2006. Molecular and immunohistochemical analyses of cardiac troponin T during cardiac development in the Mexican axolotl, Ambystoma mexicanum. J Cell Biochem 100: 1-15.