Local action of thyroxin on amphibian metamorphosis

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Local action of thyroxin on amphibian metamorphosis

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LOCAL ACTION OF THIROXIN ON AMPHIBIAN METAMORPHOSIS

by Jane Couffer Kaltenbach

A dissertation submitted in partial fulfi llment of the requirements for the degree of Doctor of Philosophy, in the Department of Zoology in the Graduate College of the State University of Iowa June, 19 £0

ProQ uest Number: 10583787

All rights reserved INFORMATION TO ALL USERS The quality o f this reproduction is d e p e n d e n t up on th e quality o f th e c o p y su b m itted . In th e unlikely e v e n t th a t th e author did not se n d a c o m p le t e m anuscript a n d th ere are missing p a g e s , t h e s e will b e n o te d . Also, if m aterial h a d to b e r e m o v e d , a n o te will in d ica te th e d e le tio n .

uest. ProQ uest 10583787 Published by ProQ uest LLC (2017). Copyright o f th e Dissertation is h eld by th e Author. All rights reserved. This work is p r o te c te d a g a in st unauthorized co p y in g under Title 17, United S tates C o d e Microform Edition © ProQ uest LLC. ProQ uest LLC. 789 East Eisenhower Parkway P.O. Box 1346 Ann Arbor, Ml 48106 - 1346

ACKNOWLEDGMENT The author wishes to express sincere appreciation to Dr* Jerry J. Kollros for the suggestion of this problem and for his invaluable advice and assistance throughout the progress of the investigation.

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TABLE OF CONTENTS

Page i n t r o d u c t i o n .........

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MATERIALS AND M E T H O D S ........................................

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........................................... . . . .

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RESULTS



Frelirainaiy S e r i e s .............. * ..................... Head Symmetry Group . • • ............. larval Mouth Furnishings Group ................... Tall Fin Group . . . Skin Pigmentation and DermalPlicae G r o u p ........... Hind Limb G r o u p ............... ...» Orbit Group ............................... Skin Window G r o u p ............. . . . . . . . . . . . Discussion and S u m ma r y.......................

IS l£ 17 19 21 29 36 10 11

Orbit S e r i e s ............................................ Normal Development of Extrinsic Ocular Muscles, Cornea, Eyelids, and Nictitating Membrane . . . . . Results: Premature Unilateral Development of Extrinsic Ocular Muscles, Cornea, Eyelids, and Nictitating M e m b r a n e ..................... Discussion............ .. .

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Skin Window Series ................................... Normal Formation and Perforation of the Skin Window. . Introduction • • • • • .......... • * • • . • • • • • Results: Premature Formation and Perforation of the Skin Window .......................... Discussion . . . . . . . ........

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GENERAL DISCUSSION............................................

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SUMMARY AND C O N C L U S I O N S .........................

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BIBLIOGRAPHY..................................................

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TABLE OF TABLES Table 1 II

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page Effects of Thyroxin—cholesterol Implants on Ossification and Growth inthe Hind Limbs• • « < . • • • • • . • • » « «

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Mat amorphic Changes Induced in the Eye and Adjacent Structures by Thyroxin—cholesterol Implants in the .................... Orbit Unilateral Formation and Perforation of the Skin Window Induced by Thyroxin—c holes terol Implants

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TABLE OF GRAPHS Graph

page

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Ossification and Growth of the Hind Limbs of Tadpole $9

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Effects of Thyroxin-c holestarol Implants Upon Local Metamorphosis (Skin Window Formation and Perforation) and Upon General Metamorphosis (Hind Limb Development)»

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TABLE OF PLATES Photographs and Photomicrographs of* Rana p ipiens Larvae in which Thyroxin-»chole sterol Pellets and Cholesterol Control Pellets had been Implanted in Corresponding Positions on Opposite Sides of the BodyPlate I IX III IV V VI VII m u

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x xx XIX XIII

page Ventral View of the Circumoral Area, Showing the Effect of Thyroxin Upon Larval Mouth Furnishings . . . . . . .

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Ventral View of the Hind Limbs, Showing the Effect of Thyroxin Upon Ossification and Growth of the Hind Limbs

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External Views of the Head, Showing the Effect of Thyroxin Upon the Eye and Adjacent Structures • . . . .

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Ventral View of the Extrinsic Ocular Muscles, Showing the Effect of Thyroxin Upon Extrinsic Ocular Muscles *

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Gross Sections of the Eye, Showing the Incipient Effect of Thyroxin Upon the Eye and Adjacent Structures •

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Gross Sections of the Eye, Showing the Effects of Thyroxin Upon the Eye and Adjacent Structures . . .

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Cross Sections of the Eye, showing the Effects of Thyroxin Upon the Eye and Adjacent Structures • •

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External View of the Opercular Region, Showing the Effects of Thyroxin Upon Opercular Perforation and Forelimb Emergence . . . . . . . . ............
hastens metamorphosis in amphibian larva© (Kendall, 1919$ Swingle, @t al., 192U).

Conversely, dinitrophenol

(1 -2 -U) causes an increase in the metabolic rate of mammals, but proves ineffective in stimulating amphibian metamorphosis (Cutter and fainter, 1933)* Th© degree of metamorphic response induced in amphibians by thyroid hormone varies with the species and stage of development of the larvae, with the concentration of hormone, and with the length of th© administration period (Allen, 1938)*

The first external

effects of thyroid preparations do not appear until after the gills are covered by th© operculum (Rom©is, 1923)* Activity of the thyroid gland is dependent upon thyrotropic hormone secreted by th© pars anterior of th© pituitary gland, and th© thyrotropic activity of th© pars anterior is inhibited by thyroid hormone (review articles, Allen, 1929, 1938).

The interrelationship

between these glands has been demonstrated in experiments involving extirpation of either or both glands and administration of hormones* After thyroidectomy, th© pituitary gland increases in size, but metamorphic changes do not occur (Allen, 1916, 1917©$ Hoskins and Morse, 1917$ Hoskins and Hoskins, 1918, 1919$ Rogers, 1918$ Larson,

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1919J Smith, 1920).

After hypophysectomy, growth of the thyroid gland

is retarded, and me tamo rphie changes are inhibited (Adler, 1911*1 Allen, 1916, 1917®, 1917b* Smith, 1916a, 1916b, 1920)*

Growth of the

hind limbs was retarded to the same extent in tadpoles in which either or both glands had been ablated, suggesting that metamorphosis is similarly effected in th© absence of either the hypophysis or the thyroid gland (Allen, 1925)*

Metamorphosis is accelerated after the

implantation of the anterior lobe of th© pituitary gland into normal tadpoles, but remains inhibited after similar implantation into thyroidless tadpoles, indicating that the pars anterior affects metamorphosis indirectly through its effect upon th© thyroid gland (Allen, 1920, 1921, 1927). The synthesis or release of thyroid hormone and hence amphibian metamorphosis is also inhibited by the administration of goitrogenic drugs, such as thiourea (Gordon, Goldsmith, and Gh&ripper, 191*3, 191*5) or thiouracil (Hughe® and Astwood, 191*1*). Administration of elemental iodine and various inorganic and organic compounds containing iodine results in stimulation of amphibian metamorphosis.

The effectiveness of such compounds depends

in part upon their chemical nature and the method and duration of their administration (Allen, 1929, 1936)*

Metamorphosis was induced by

feeding elemental iodine to normal and thyroidectomised tadpole® (Swingle, 1918a, 1918b, 1919a, 1919b), and also to hypophysactoniized tadpoles and to tadpoles from which both th© thyroid gland and the

it

hypophysis had been removed (Allen* 1919)*

Such results suggest that

although th© thyroid gland Is needed for utilisation of lodina present in very small quantities* it is not essential for th© utilization of iodine present In large amounts *

On the other hand* metamorphic

changes did not occur in tadpoles reared in distilled water and given food deficient in iodine* I*©** metamorphosis does not occur in the virtually complete absence of iodine (Lynn and Brambel* 193$) •

In*

organic compounds such as Iodoform and potassium iodide* and organic compounds such as

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-$-diiodotyrosine* acetylated thyroxin* the glycine

homologu© of thyroxin* and a benzoic acid analogue of thyroxin vary in their effectiveness in promoting metamorphosis (review article* Allen* 1938f Frieden and Winzler* 19US)• This suggests that the effective constituent is iodine and that its efficacy is modified by the type of chemical combination in which it occurs (Allen* 1936)* f The developmental progress of anuran tadpoles has been related by Btkin (1932) and by Taylor and Kollros (191*6)*

In the

pram© tamorp hie period prior to stage 3 OTII* th© following changes occurs ' rapid growth of the forelimbs (within the peribranehi&l cavity) and of the hind limbs* formation of cutaneous glands* and gradual development of th© adult skin pigment pattern*

In the metamorphic

stages (X1TIII—XXV), the following changes are evident:

regression

of the oloacal tail-piece* development of th© nictitating membrane and corneal reflex* formation and perforation of the skin window (disc­ shaped clearing in th© operculum)* emergence of the forelimb©, resorp­ tion of larval mouth furnishings* formation of th© adult mouth* changes

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in body shape from the broad, rounded tadpole type to the narrow, more pointed adult type, and resorption of the tail and of th© gills, Since thyroid administration to amphibian larvae accelerates general metamorphosis, it is of interest to determine which metamorphic changes are caused by the direct, and which by the indirect action of thyroid hormone.

For example, evidence of Helff (l