Summary
We examined the role of thyroid hormone (TH) in mediating cranial ossification during metamorphosis in the Oriental fire-bellied toad, Bombina orientalis. Exogenous T3 (3,3′,5-triiodo-L-thyronine) was administered in three treatment dosages (0.025, 0.25, and 2.5 μg) plus a control dosage via plastic micropellets implanted within the dermis of tadpoles of three Gosner developmental stages: 28/29, 30/31, 32/33. Tadpoles were recovered after 2, 4, 6, and 8 d, and scored for the presence of three bones —median parasphenoid and paired frontoparietals and exoccipitals—as seen in cleared-and-stained, whole-mount preparations. T3 induced precocious ossification in both a stage-dependent and a dosage-dependent manner; stage dependence corresponded precisely with the degree of osteogenic differentiation at the time of hormone administration. Precocious ossification thus was due to the T3-promoted growth and calcified matrix deposition of these centers. Differential TH sensitivity among osteogenic sites may underlie both the temporal cranial ossification sequences characteristic of metamorphosing amphibians as well as sequence differences commonly observed among taxa.
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References
Burch WM, Lebovitz HE (1982a) Triiodothyronine stimulation of in vitro growth and maturation of embryonic chick cartilage. Endocrinology 111: 462–468
Burch WM, Lebovitz HE (1982b) Triiodothyronine stimulates maturation of porcine growth-plate cartilage in vitro. J Clin Invest 70:496–504
Buscaglia M, Leloup J, De Luze A (1985) The role and regulation of monoiodination of thyroxine to 3,5,3′-triiodothyronine during amphibian metamorphosis. In: Balls M, Bownes M (eds) Metamorphosis. Clarendon Press, Oxford
Carlson JT, Ellinger MS (1980) The reproductive biology of Bombina orientalis, with notes on care. Herpetol Rev 11:11–12
Chou HI, Kollros JJ (1974) Stage-modified responses to thyroid hormones in anurans. Gen Comp Endocrinol 22:255–260
Dent JN, Kirby-Smith JS (1963) Metamorphic physiology and morphology of the cave salamander Gyrinophilus palleucus. Copeia 1963:119–130
Dent JN, Kirby-Smith JS, Craig DL (1955) Induction of metamorphosis in Gyrinophilus palleucus. Anat Rec 121:429
Dodd MHI, Dodd JM (1976) The biology of metamorphosis. In: Lofts B (ed) Physiology of the Amphibia, vol. 3. Academic Press, New York
Dundee HA (1957) Partial metamorphosis induced in Typhlomolge rathbuni. Copeia 1957:52–53
Dundee HA (1961) Response of the neotenic salamander, Haideotriton wallacei to a metamorphic agent. Science 135:1060–1061
Etkin W (1968) Hormonal control of amphibian metamorphosis. In: Etkin W, Gilbert LI (eds) Metamorphosis, a problem in developmental biology. Appleton-Century-Crofts, New York
Fell H, Mellanby E (1955) The biological action of thyroxine on embryonic bones grown in tissue culture. J Physiol (Lond) 127:427–447
Fell H, Mellanby E (1956) The effect of L-triiodothyronine on the growth and development of embryonic chick limb-bones in tissue culture. J Physiol (Lond)133:89–100
Fox E, Irving JT (1950) The effect of thyroid hormone on the ossification of the femur in Xenopus laevis tadpoles. S Afr J Med Sci 15: 11–14
Frost JS (1982) A time efficient, low cost method for the laboratory rearing of frogs. Herpetol Rev 13:75–77
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190
Hall BK (1982) The role of tissue interactions in the growth of bone. In: Dixon AD, Sarnat BG (eds) Factors and mechanisms influencing bone growth. Alan R Liss, New York
Hall BK (1985) Critical periods during development as assessed by thallium-induced inhibition of growth of embryonic chick tibiae in vitro. Teratology 31:353–361
Hamburger V (1960) A manual of experimental embryology. University of Chicago Press, Chicago
Hanken J, Hall BK (1984) Variation and timing of the cranial ossification sequence of the Oriental fire-bellied toad, Bombina orientalis (Amphibia, Discoglossidae). J Morphol 182:245–255
Hanken J, Hall BK (1988) Skull development during anuran metamorphosis: I. Early development of the first three bones to form—the exoccipital, the parasphenoid, and the frontoparietal. J Morphol, in press
Hanken J, Summers CH (1988) Skull development during anuran metamorphosis: III. Role of thyroid hormone in chondrogenesis. J Exp Zool, in press
Hanken J, Wassersug RJ (1981) The visible skeleton. Funct Photog 16:22–26, 44
Heuberger B, Fitzka I, Wasner G, Kratochwil K (1982) Induction of androgen receptor formation by epithelium-mesenchyme interaction in embryonic mouse mammary gland. Proc Natl Acad Sci 79:2957–2961
Jowsey J, Detenbeck LC (1969) Importance of thyroid hormones in bone metabolism and calcium homeostasis. Endocrinology 85:87–95
Kaltenbach JC (1953a) Local action of thyroxin on amphibian metamorphosis. I. Local metamorphosis in Rana pipiens larvae effected by thyroxin-cholesterol implants. J Exp Zool 122:21–39
Kaltenbach JC (1953b) Local action of thyroxin on amphibian metamorphosis. II. Development of the eyelids, nictitating membrane, cornea and extrinsic ocular muscles in Rana pipiens larvae effected by thyroxin-cholesterol implants. J Exp Zool 122:41–51
Kaltenbach JC (1953c) Local action of thyroxin on amphibian metamorphosis. III. Formation and perforation of the skin window in Rana pipiens larvae effected by thyroxin-cholesterol implants. J Exp Zool 122:449–467
Kemp NE, Hoyt JA (1965a) Influence of thyroxine on ossification of the femur in Rana pipiens. J Cell Biol 27:51A
Kemp NE, Hoyt JA (1965b) Influence of thyroxine on ossification of the parasphenoid bone in the skull of Rana pipiens. Am Zool 5:710
Kemp NE, Hoyt JA (1965c) Influence of thyroxine on order of ossification of bones of the skull of Rana pipiens. Am Zool 5:719
Kemp NE, Hoyt JA (1969a) Sequence of ossification in the skeleton of growing and metamorphosing tadpoles of Rana pipiens. J Morphol 129:415–444
Kemp NE, Hoyt JA (1969b) Ossification of the femur in thyroxine-treated tadpoles of Rana pipiens. Dev Biol 20: 387–410
Kollros JJ (1981) Transitions in the nervous system during amphibian metamorphosis. In: Gilbert LI, Frieden E (eds) Metamorphosis, a problem in developmental biology, 2nd edn. Plenum Press, New York
Kühn O, Hammer HO (1956) Über die Einwirkung des Schilddrüsenhormons auf die Ossifikation. Experientia 12:231–233
Lynn WG (1942) The embryology of Eleutherodactylus rubicola, an anuran which has no tadpole stage. Contrib Embryol Carnegie Inst Washington Publ 541:27–62
Nijweide PJ, Burger EH, Feyen JHM (1986) Cells of bone: proliferation, differentiation, and hormonal regulation. Physiol Rev 66:855–886
Orbai P, Gozariu L (1982) Effect of thyroid hormones on osteolysis “in vitro”. Endocrinology 20:181–185
Raisz LG, Canalis EM, Dietrich JW, Kream BE, Gworek SC (1978) Hormonal regulation of bone formation. Recent Prog Horm Res 34:335–356
Reddi AH (1982) Local and systemic mechanisms regulating bone formation and remodeling: an overview. In: Silberman M, Slavkin HC (eds) Current advances in skeletogenesis: development biomineralization mediators, and metabolic bone disease. Excerpta Medica, Amsterdam
Robinson ME, Scadding SR (1983) The effect of pH on tricaine methanesulfonate induced anaesthesia of the newt Notophthalmus viridescens. Can J Zool 61:531–533
Scott JP (1986) Critical periods in organizational processes. In: Falkner F, Tanner JM (eds) Human growth: a comprehensive treatise, vol. 1, 2nd edn. Plenum Press, New York
Silberberg M, Silberberg R (1938) The effects of thyroid feeding on growth processes and retrogressive changes in bone and cartilage of the immature guinea pig. Growth 2:327–333
Silberberg M, Silberberg R (1940) Changes in the skeletal tissues of mice following the administration of thyroxin. Growth 4:305–314
Silbermann M (1983) Hormones and cartilage. In: Hall BK (ed) Cartilage, vol. 2. Academic Press, New York
Silberstein GB, Daniel CW (1982) Elvax 40P implants: sustained, local release of bioactive molecules influencing mammary ductal development. Dev Biol 93:272–278
Takakubo F, Ikeda Y, Eto K (1986) Stage-specific response of the mesenchyme to excess vitamin A in developing rat facial processes. J Craniofac Genet Dev Biol 6:41–51
Terry GS (1918) Effects of the extirpation of the thyroid gland upon ossification in Rana pipiens. J Exp Zool 24:567–581
Turley EA, Hollenberg MD, Pratt RM (1985) Effect of epidermal growth factor/urogastrone on glycosaminoglycan synthesis and accumulation in vitro in the developing mouse palate. Differentiation 28:279–285
Wassersug RJ (1976) A procedure for differential staining of cartilage and bone in whole formalin-fixed vertebrates. Stain Technol 51:131–134
White BA, Nicoll CS (1981) Hormonal control of amphibian metamorphosis. In: Gilbert LI, Frieden E (eds). Metamorphosis, a problem in developmental biology, 2nd edn. Plenum Press, New York
Yeatman HC (1967) Artifically metamorphosed neotenic cave salamanders. J Tenn Acad Sci 42:16–22
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Hanken, J., Hall, B.K. Skull development during anuran metamorphosis. Anat Embryol 178, 219–227 (1988). https://doi.org/10.1007/BF00318225
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DOI: https://doi.org/10.1007/BF00318225