Rediscovering the Axolotl as a Model for Thyroid Hormone Dependent Development - PubMed (original) (raw)
Rediscovering the Axolotl as a Model for Thyroid Hormone Dependent Development
Anne Crowner et al. Front Endocrinol (Lausanne). 2019.
Abstract
The Mexican axolotl (Ambystoma mexicanum) is an important model organism in biomedical research. Much current attention is focused on the axolotl's amazing ability to regenerate tissues and whole organs after injury. However, not forgotten is the axolotl's equally amazing ability to thwart aspects of tissue maturation and retain juvenile morphology into the adult phase of life. Unlike close tiger salamander relatives that undergo a thyroid hormone regulated metamorphosis, the axolotl does not typically undergo a metamorphosis. Instead, the axolotl exhibits a paedomorphic mode of development that enables a completely aquatic life cycle. The evolution of paedomorphosis allowed axolotls to exploit relatively permanent habitats in Mexico, and preadapted axolotls for domestication and laboratory study. In this perspective, we first introduce the axolotl and the various meanings of paedomorphosis, and then stress the need to move beyond endocrinology-guided approaches to understand the axolotl's hypothyroid state. With the recent completion of the axolotl genome assembly and established methods to manipulate gene functions, the axolotl is poised to provide new insights about paedomorphosis and the role of thyroid hormone in development and evolution.
Keywords: ambystoma; axolotl; metamorphosis; paedomorphosis; thyroid hormone.
Figures
Figure 1
(A) The ancestral salamander mode of development is metamorphosis. Metamorphosis in the tiger salamander is regulated by the hypothalamus-pituitary-thyroid (HPT) axis. At a critical time during larval development, corticotrophin releasing hormone (CRH) from the hypothalamus stimulates thyrotrophic cells in the pituitary to release thyroid stimulating hormone (TSH), which in turn stimulates the thyroid gland to secrete thyroid hormone (TH). Increasing TH (+) triggers metamorphic changes in target cells. (B) The derived paedomorphic mode of development. Paedomorphosis in the axolotl results in the retention of ancestral larval characters into the adult phase of life. Although CRH-like and TSH-like activity are present in the axolotl hypothalamus and pituitary respectively, and TSH and TH treatment can induce metamorphosis, the HPT axis is not activated during larval development. Modified from Johnson and Voss (7).
Figure 2
(A) Map of genes from axolotl chromosome 2 (Chr2p) that associate with met1. (B) General structure of CCN family proteins showing insulin-like growth factor binding protein-like (IGFBP), a von Willebrand factor type C repeat (VWC), thrombospondin-homology type 1 repeat (TSP1), and a C-terminal cysteine-knot-containing (CT) domains. Human (Hs) ccn1 (GenBank: AAB84227.1) was used as a reference to compare domain-specific amino acid similarity among Xenopus tropicalis (Xp) ccn1 (GenBank: OCA36969.1), A. mexicanum ccn1 (AMEXTC_0340000257024_cysteine-rich), and A. mexicanum ccn1-like (AMEXTC_0340000025590_LOC102363594). The A. mexicanum ccn1-like sequence has a unique deletion of 30 amino acids between the VWC and TSP1 domains.
Similar articles
- Forever young: Endocrinology of paedomorphosis in the Mexican axolotl (Ambystoma mexicanum).
De Groef B, Grommen SVH, Darras VM. De Groef B, et al. Gen Comp Endocrinol. 2018 Sep 15;266:194-201. doi: 10.1016/j.ygcen.2018.05.016. Epub 2018 May 16. Gen Comp Endocrinol. 2018. PMID: 29777689 Review. - Microarray analysis of a salamander hopeful monster reveals transcriptional signatures of paedomorphic brain development.
Page RB, Boley MA, Smith JJ, Putta S, Voss SR. Page RB, et al. BMC Evol Biol. 2010 Jun 28;10:199. doi: 10.1186/1471-2148-10-199. BMC Evol Biol. 2010. PMID: 20584293 Free PMC article. - Geography is more important than life history in the recent diversification of the tiger salamander complex.
Everson KM, Gray LN, Jones AG, Lawrence NM, Foley ME, Sovacool KL, Kratovil JD, Hotaling S, Hime PM, Storfer A, Parra-Olea G, Percino-Daniel R, Aguilar-Miguel X, O'Neill EM, Zambrano L, Shaffer HB, Weisrock DW. Everson KM, et al. Proc Natl Acad Sci U S A. 2021 Apr 27;118(17):e2014719118. doi: 10.1073/pnas.2014719118. Proc Natl Acad Sci U S A. 2021. PMID: 33888580 Free PMC article. - Experimentally induced metamorphosis in highly regenerative axolotl (ambystoma mexicanum) under constant diet restructures microbiota.
Demircan T, Ovezmyradov G, Yıldırım B, Keskin İ, İlhan AE, Fesçioğlu EC, Öztürk G, Yıldırım S. Demircan T, et al. Sci Rep. 2018 Jul 20;8(1):10974. doi: 10.1038/s41598-018-29373-y. Sci Rep. 2018. PMID: 30030457 Free PMC article. - Salamander paedomorphosis: linking thyroid hormone to life history and life cycle evolution.
Johnson CK, Voss SR. Johnson CK, et al. Curr Top Dev Biol. 2013;103:229-58. doi: 10.1016/B978-0-12-385979-2.00008-3. Curr Top Dev Biol. 2013. PMID: 23347521 Review.
Cited by
- Insights into the Evolution of Neoteny from the Genome of the Asian Icefish Protosalanx chinensis.
Zhang J, Qi J, Shi F, Pan H, Liu M, Tian R, Geng Y, Li H, Qu Y, Chen J, Seim I, Li M. Zhang J, et al. iScience. 2020 Jul 24;23(7):101267. doi: 10.1016/j.isci.2020.101267. Epub 2020 Jun 14. iScience. 2020. PMID: 32593955 Free PMC article. - The rax homeobox gene is mutated in the eyeless axolotl, Ambystoma mexicanum.
Davis ES, Voss G, Miesfeld JB, Zarate-Sanchez J, Voss SR, Glaser T. Davis ES, et al. Dev Dyn. 2021 Jun;250(6):807-821. doi: 10.1002/dvdy.246. Epub 2020 Sep 17. Dev Dyn. 2021. PMID: 32864847 Free PMC article.
References
- Cuvier G. Recherches anatomique sur les reptiles regardes encore comme douteux par les naturalistes; faites a l'occasion de l'axolotl, rapport_e par M. de Humboldt du Mexique. In: Humboldt A, von, Bonpl A. editors. Voyage de Humboldt & Bonpland. Voyage aux regions equinoxiales du nouveau continent. Deuxieme partie. Tome 1. Recueil d'observations de zoologie et d'anatomie comparee. vol. 1 Paris: Schoell et Dufour; (1811). p. 93–126.
- Dumeril A. Reproduction, dans la menagerie des reptiles au Museum d'Histoire naturelle, des axolotls, batraciens, urodeles a branchies persistantes de Mexico (Siredon mexicanus, vel Humboldtii), qui n'avient encore jamais ete vus vivante en Europe. Compt Rend Hebd Seances Acad Sci. (1865a) 60:765–7.
- Dumeril A. Nouvelles observations sur les axolotls, batraciens urodeles de Mexico (Siredon mexicanus vel Humboldtii) nes dans la menagerie des reptiles au Mus_eum d'Histoire naturelle, et qui y subissent des metamorphose. Compt Rend Hebd Seances Acad Sci. (1865b) 61:775–8.
- Kollman J. Das Ueberwintern von europäis-chen Frosch und Triton Iarven und die Umwand-lung des mexikanischen Axolotl. Verh Naturforsch Ges Basel. (1885) 7:387–98.
LinkOut - more resources
Full Text Sources