A model of transcriptional and morphological changes during thyroid hormone-induced metamorphosis of the axolotl

General and Comparative Endocrinology

Volumn 162, Issue 2, 2009, Pages 219-232

  Page, Robert B ^a,b   Monaghan, James R ^a,b   Walker, John A ^a,b   Voss, S Randal ^a,b  

^a UNIVERSITY OF KENTUCKY   (United States)

^b UNIVERSITY OF KENTUCKY   (United States)

Author keywords

Ambystoma; Amphibian; Linear regression; Metamorphosis; Mexican axolotl; Morphometrics; Piecewise regression; Thyroid hormone; Transcription

Indexed keywords

THYROID HORMONE;

AMBYSTOMA MEXICANUM; AMPHIBIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; GENE EXPRESSION; HISTOLOGY; IN SITU HYBRIDIZATION; METAMORPHOSIS; MORPHOMETRICS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SKIN; STATISTICAL MODEL;

EID: 67349133771     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2009.03.001     Document Type: Article

References (79)

1. Alberch P., Lewbart G.A., and Gale E.A. The fate of larval chondrocytes during the metamorphosis of the epibranchial in the salamander, Eurycea bislineata. J. Embryol. Exp. Morphol. 88 (1985) 71-83
2. 3 in naturally metamorphosing Eurycea bislineata (amphibia; plethodontidae). Gen. Comp. Endocrinol. 61 (1986) 153-163
3. Anderson J.S., Reisz R.R., Scott D., Frobisch N.B., and Sumida S.S. A stem batrachian from the early Permian of Texas and the origin of frogs and salamanders. Nature 453 (2008) 515-518
4. Armstrong J.B., Duhon S.T., and Malacinski G.M. Raising the axolotl in captivity. In: Armstrong J.B., and Malacinski G.M. (Eds). Developmental Biology of the Axolotl (1989), Oxford University Press, New York 220-227
5. Armstrong J.B., and Duhon S.T. Induced spawnings, artificial insemination, and other genetic manipulations. In: Armstrong J.B., and Malacinski G.M. (Eds). Developmental Biology of the Axolotl (1989), Oxford University Press, New York 228-235
6. Ben-Porath I., and Benvenisty N. Characterization of a tumor-associated gene, a member of a novel family of genes encoding membrane glycoproteins. Gene 183 (1996) 69-75
7. Bolker J.A. Model systems in developmental biology. Bioessays 17 (1995) 451-455
8. Brown D.D. The role of thyroid hormone in zebrafish and axolotl development. Proc. Natl. Acad. Sci. USA 94 (1997) 13011-13016
9. Brown D.D. The role of deiodinases in amphibian metamorphosis. Thyroid 15 (2005) 815-821
10. Brown D.D., and Cai L. Amphibian metamorphosis. Dev. Biol. 306 (2007) 20-33
11. Buchholz D.R., and Hayes T.B. Variation in thyroid hormone action and tissue content underlies species differences in the timing of metamorphosis in desert frogs. Evol. Dev. 7 (2005) 458-467
12. Buchholz D.R., Paul B.D., Fu L., and Shi Y.B. Molecular and developmental analyses of thyroid hormone function in Xenopus laevis, the African clawed frog. Gen. Comp. Endocrinol. 145 (2006) 1-19
13. Bustin S.A., and Nolan T. Pitfalls of quantitative real-time reverse-transcription polymerase chain reaction. J. Biomol. Tech. 15 (2004) 155-166
14. Cano-Martinez A., Vargas-Gonzalez A., and Asai M. Metamorphic stages in Ambystoma mexicanum. Axolotl Newsletter 23 (1994) 64-71
15. 4 release in Ambystoma mexicanum. Gen. Comp. Endocrinol. 51 (1983) 286-291
16. Darras V.M., and Kuhn E.R. Difference of the in vivo responsiveness to thyrotropin stimulation between the neotenic and metamorphosed axolotl, Ambystoma mexicanum: failure of prolactin to block the thyrotropin-induced thyroxine release. Gen. Comp. Endocrinol. 56 (1984) 321-325
17. Denver R.J., Glennemeier K.A., and Boorse G.C. Endocrinology of complex life cycles: amphibians. In: Pfaff D., Arnold A., Etgen A., Fahrbach S., and Rubin R. (Eds). Hormones, Brains, and Behavior (2002), Academic Press, San Diego 469-513
18. Ducibella T. The occurrence of biochemical metamorphic events without anatomical metamorphosis in the axolotl. Dev. Biol. 38 (1974) 175-186
19. Duellman W.E., and Trueb L. Biology of Amphibians (1994), Johns Hopkins University Press, Baltimore
20. Etkin W. Hormonal control of amphibian metamorphosis. In: Etkin W., and Gilbert L.I. (Eds). Metamorphosis: a Problem in Developmental Biology (1968), Appleton-Century-Crofts, New York 313-348
21. Fahrmann W. Morphodynamics of the epidermis of the axolotl (Siredon mexicanum Shaw) under the influence of exogenously administered thyroxine I. the epidermis of neotenic axolotls. Z. Mikrosk. Anat. Forsch. 83 (1971) 472-506
22. Fahrmann W. Morphodynamics of the epidermis of the axolotl (Siredon mexicanum Shaw) under the influence of exogenously administered thyroxine II. the epidermis during metamorphosis. Z. Mikrosk. Anat. Forsch. 83 (1971) 535-568
23. Fahrmann W. Morphodynamics of the epidermis of the axolotl (Siredon mexicanum Shaw) under the influence of exogenously administered thyroxine III. the epidermis of the metamorphosed axolotl. Z. Mikrosk. Anat. Forsch. 84 (1971) 1-25
24. Friedberg F., and Rhoads A.R. Evolutionary aspects of calmodulin. IUBMB Life 51 (2001) 215-221
25. Frost S.K., Neff A.W., and Malacinski G.M. Primary and long-term culture of axolotl cells. In: Armstrong J.B., and Malacinski G.M. (Eds). Developmental Biology of the Axolotl (1989), Oxford University Press, New York 244-254
26. Furlow J.D., Berry D.L., Wang Z., and Brown D.D. A set of novel tadpole specific genes expressed only in the epidermis are down-regulated by thyroid hormone during Xenopus laevis metamorphosis. Dev. Biol. 182 (1997) 284-298
27. Galton V.A. Thyroid hormone receptors and iodothyronine deiodinases in the developing Mexican axolotl, Ambystoma mexicanum. Gen. Comp. Endocrinol. 85 (1992) 62-70
28. Heady J.E., and Kollros J.J. Hormonal modification of the development of plical skin glands. Gen. Comp. Endocrinol. 4 (1964) 124-131
29. Holder N., and Glade R. Skin glands in the axolotl: the creation and maintenance of a spacing pattern. J. Embyol. Exp. Morhol. 79 (1984) 97-112
30. Ishizuya-Oka A., and Shi Y.B. Regulation of adult intestinal epithelial stem cell development by thyroid hormone during Xenopus laevis metamorphosis. Dev. Dyn. 236 (2007) 3358-3368
31. Kanamori A., and Brown D.D. The regulation of thyroid hormone receptor β genes by thyroid hormone in Xenopus laevis. J. Biol. Chem. 267 (1992) 739-745
32. Kardong K.V. Vertebrates: Comparative Anatomy, Function, Evolution. second ed. (1998), McGraw-Hill, New York
33. Kawahara A., Baker B.S., and Tata J.R. Developmental and regional expression of thyroid hormone receptor genes during Xenopus metamorphosis. Development 112 (1991) 933-943
34. Kumada Y., Benson D.R., Hillemann D., Hosted T.J., Rochefort D.A., Thompson C.J., Wohlleben W., and Tateno Y. Evolution of the glutamine synthetase gene, one of the oldest existing and functioning genes. Proc. Natl. Acad. Sci. USA 90 (1993) 3009-3013
35. 3 levels in Ambystoma tigrinum at various stages of metamorphosis. Gen. Comp. Endocrinol. 43 (1981) 443-450
36. Leloup J., and Buscaglia M. La triiodothyronine: hormone de la metamorphose des amphibiens. C.R. Acad. Sci. 284 (1977) 2261-2263
37. Marvin K.W., Fujimoto W., and Jetten A.M. Identification and characterization of a novel squamous cell-associated gene related to PMP22. J. Biol. Chem. 270 (1995) 28910-28916
38. Monaghan J.R., Walker J.A., Page R.B., Putta S., Beachy C.K., and Voss S.R. Early gene expression during natural spinal cord regeneration in the salamander Ambystoma mexicanum. J. Neurochem. 101 (2007) 27-40
39. Monaghan J.R., Epp L.G., Putta S., Page R.B., Walker J.A., Beachy C.K., Zhu W., Pao G.M., Verma I.M., Hunter T., Bryant S.V., Gardiner D.M., Harkins T.T., and Voss S.R. Microarray and cDNA sequence analysis of transcription during nerve-dependent limb regeneration. BMC Biology 7 (2009) 1
40. Muggeo V.M.R. Segmented: an R package to fit regression models with broken-line relationships. R. News 8 (2008) 20-25
41. Nieuwkoop P.D., and Faber J. Normal Table of Xenopus laevis (Daudin): a Systematical and Chronological Survey of the Development From the Fertilized Egg till the End of Metamorphosis. second ed. (1967), North-Holland, Amsterdam
42. Norman M.F. A practical method for staging metamorphosis in the tiger salamander Ambystoma tigrinum. Anat. Rec. 211 (1985) 102-109
43. Ohmura H., and Wakahara M. Transformation of skin from larval to adult types in normally metamorphosing and metamorphosis-arrested salamander, Hynobius retardatus. Differentiation 62 (1998) 237-246
44. Oofusa K., and Yoshizato K. Biochemical and immunological characterization of collagenase in tissues of metamorphosing bullfrog tadpoles. Dev. Growth Differ. 33 (1991) 329-339
45. Oofusa K., and Yoshizato K. Thyroid hormone-dependent expression of bullfrog tadpole collagenase gene. Roux's Arch. Dev. Biol. 205 (1996) 243-251
46. Page R.B., Monaghan J.R., Samuels A.K., Smith J.J., Beachy C.K., and Voss S.R. Microarray analysis identifies keratin loci as sensitive biomarkers for thyroid hormone disruption in the salamander Ambystoma mexicanum. Comp. Biochem. Physiol. C, Pharmacol. Toxicol. 145 (2007) 15-27
47. Page R.B., Voss S.R., Samuels A.K., Smith J.J., Putta S., and Beachy C.K. Effect of thyroid hormone concentration on the transcriptional response underlying induced metamorphosis in the Mexican axolotl (Ambystoma). BMC Genomics 9 (2008) 78
48. Petranka J.W. Salamanders of the United States and Canada (1998), Smithsonian Institution Press, Washington
49. Pfaffl M. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29 (2001) e45
50. Prahlad K.V., and DeLanney L.E. A study of induced metamorphosis in the axolotl. J. Exp. Zool. 160 (1965) 137-146
51. Prahlad K.V. Induced metamorphosis: rectification of a genetic disability by thyroid hormone in the Mexican axolotl Siredon mexicanum. Gen. Comp. Endocrinol. 11 (1968) 21-30
52. Putta S., Smith J.J., Walker J.A., Rondet M., Weisrock D.W., Monaghan J.R., Samuels A.K., Kump K., King D.C., Maness N.J., Habermann B., Tanaka E., Bryant S.V., Gardiner D.M., Parichy D.M., and Voss S.R. From biomedicine to natural history research: EST resources for ambystomatid salamanders. BMC Genomics 5 (2004) 54
53. Ranjan M., Wong J., and Shi Y.B. Transcriptional repression of Xenopus TRβ gene is mediated by a thyroid hormone response element located near the start site. J. Biol. Chem. 269 (1994) 24699-24705
54. Rose C.S. Skeletal morphogenesis in the urodele skull: I. postembryonic development in the hemidactyliini (amphibia: plethodontidae). J. Morphol. 223 (1995) 125-148
55. Rose C.S. Skeletal morphogenesis in the urodele skull: II. Effect of developmental stage in thyroid hormone-induced remodeling. J. Morphol. 223 (1995) 149-166
56. Rose C.S. Skeletal morphogenesis in the urodele skull: III. Effect of hormone dosage in TH-induced remodeling. J. Morphol. 223 (1995) 243-261
57. Rosenkilde P., and Ussing A.P. What mechanisms control neoteny and regulate induced metamorphosis in urodeles. Int. J. Dev. Biol. 40 (1996) 665-673
58. Rozen S., and Skaletsky H. Primer3 on the www for general users and for biologist programmers. Methods Mol. Biol. 132 (2000) 365-386
59. Safi R., Bertrand S., Marchand O., Duffraisse M., de Luze A., Vanacker J.M., Maraninchi M., Margotat A., Demeneix B., and Laudet V. The axolotl (Ambystoma mexicanum), a neotenic amphibian, expresses functional thyroid hormone receptors. Endocrinology 145 (2004) 760-772
60. Sawada T., Oofusa K., and Yoshizato K. Thyroid hormone response element-like sequence in anuran metalloproteinase 1 gene is responsive to in vivo thyroid hormone administration. J. Endocrinol. 169 (2001) 477-486
61. Shaffer H.B. Phylogenetics of model organisms: the laboratory axolotl, Ambystoma mexicanum. Syst. Biol. 42 (1993) 508-522
62. Shaffer H.B., and McKnight M.L. The polytypic species revisited: genetic differentiation and molecular phylogenetics of the tiger salamander Ambystoma tigrinum (amphibia: caudata) complex. Evolution 50 (1996) 417-433
63. Shaffer H.B., and Voss S.R. Phylogenetic and mechanistic analysis of a developmentally integrated character complex: alternate life history modes in ambystomatid salamanders. Am. Zool. 36 (1996) 24-35
64. Shi Y.B. Amphibian Metamorphosis: From Morphology to Molecular Biology (2000), Wiley-Liss, New York
65. Smith H.M. Discovery of the axolotl and its early history in biological research. In: Armstrong J.B., and Malacinski G.M. (Eds). Developmental Biology of the Axolotl (1989), Oxford University Press, New York 3-12
66. Smith J.J., Kump D.K., Walker J.A., Parichy D.M., and Voss S.R. A comprehensive expressed sequence tag linkage map for tiger salamander and Mexican axolotl: enabling gene mapping and comparative genomics in Ambystoma. Genetics 171 (2005) 1161-1171
67. Smith J.J., Putta S., Walker J.A., Kump D.K., Samuels A.K., Monaghan J.R., Weisrock D.W., Staben C., and Voss S.R. Sal-site: integrating new and existing ambystomatid research and informational resources. BMC Genomics 6 (2005) 181
68. Taylor C.A., and Kollros J.J. Stages in the normal development of Rana pipiens larvae. Anat. Rec. 94 (1946) 7-23
69. Toms J.D., and Lesperance M.L. Piecewise regression: a tool for identifying ecological thresholds. Ecology 84 (2003) 2034-2041
70. Venables W.N., and Ripley B.D. Modern Applied Statistics with S. fourth ed. (2002), Springer, New York
71. Voss S.R., and Smith J.J. Evolution of salamander life cycles: a major-effect quantitative trait locus contributes to discrete and continuous variation for metamorphic timing. Genetics 170 (2005) 275-281
72. Weisrock D.W., Shaffer H.B., Storz B.L., Storz S.R., and Voss S.R. Multiple nuclear gene sequences identify phylogenetic species boundaries in the rapidly radiating clade of Mexican ambystomatid salamanders. Mol. Ecol. 15 (2006) 2489-2503
73. Wilbur H.M., and Collins J.P. Ecological aspects of amphibian metamorphosis. Science 182 (1973) 1305-1314
74. Wilder I.W. The Morphology of Amphibian Metamorphosis (1925), Smith College, Northampton, Massachusetts
75. Wong J., and Shi Y.B. Coordinated regulation of and transcriptional activation by Xenopus thyroid hormone and retinoid X receptors. J. Biol. Chem. 270 (1995) 18479-18483
76. Yaoita Y., and Brown D.D. A correlation of thyroid hormone receptor gene expression with amphibian metamorphosis. Genes Dev. 4 (1990) 1917-1924
77. Yoshizato K., and Frieden E. Increase in binding capacity for triiodothyronine in tadpole tail nuclei during metamorphosis. Nature 254 (1975) 705-707
78. Yoshizato K. Molecular mechanism and evolutional significance of epithelial-mesenchymal interactions in the body and tail-dependent metamorphic transformation of anuran larval skin. Int. Rev. Cytol. 260 (2007) 213-260
79. Zar J.H. Biostatistical Analysis. fourth ed. (1999), Prentice Hall, Upper Saddle River, New Jersey