Metamorphosis Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells CELL BIOLOGY: A Series of Monographs EDITORS D. E. BUETOW I. L. CAMERON Department of Physiology Department of Cellular and and Biophysics Structural Biology University of Illinois The University of Texas Urbana, Illinois Health Science Center at San Antonio San Antonio, Texas G. M. PADILLA A.M. ZIMMERMAN Department of Cell Biology Department of Zoology Duke University Medical Center University of Toronto Durham, North Carolina Toronto, Ontario, Canada Volumes published since 1984 Gary S. Stein and Janet L. Stein (editors). RECOMBINANT DNA AND CELL PROLIFERA- TION, 1984 Prasad S. Sunkara (editor). NOVEL APPROACHES TO CANCER CHEMOTHERAPY, 1984 B. G. Atkinson and D. B. Walden (editors). CHANGES IN EUKARYOTIC GENE EXPRESSION IN RESPONSE TO ENVIRONMENTAL STRESS, 1985 Reginald M. Gorczynski (editor). RECEPTORS IN CELLULAR RECOGNITION AND DEVELOP- MENTAL PROCESSES, 1986 Govindjee, Jan Amesz, and David Charles Fork (editors). LIGHT EMISSION BY PLANTS AND BACTERIA, 1986 Peter B. Moens (editor). MEIOSIS, 1986 Robert A. Schlegel, Margaret S. Halleck, and Potu N. Rao (editors). MOLECULAR REGULATION OF NUCLEAR EVENTS IN MITOSIS AND MEIOSIS, 1987 Monique C. Braude and Arthur M. Zimmerman (editors). GENETIC AND PERINATAL EFFECTS OF ABUSED SUBSTANCES, 1987 E. J. Rauckman and George M. Padilla (editors). THE ISOLATED HEPATOCYTE: USE IN TOXI- COLOGY AND XENOBIOTIC BIOTRANSFORMATIONS, 1987 Heide Schatten and Gerald Schatten (editors). THE MOLECULAR BIOLOGY OF FERTILIZA- TION, 1989 Heide Schatten and Gerald Schatten (editors). THE CELL BIOLOGY OF FERTILIZATION, 1989 Anwar Nasim, Paul Young, and Byron F. Johnson (editors). MOLECULAR BIOLOGY OF THE FISSION YEAST, 1989 Mary P. Moyer and George Poste (editors). COLON CANCER CELLS, 1990 Gary S. Stein and Jane B. Lian (editors). MOLECULAR AND CELLULAR APPROACHES TO THE CONTROL OF PROLIFERATION AND DIFFERENTIATION, 1991 Victauts I. Kalnins (editor). THE CENTROSOME, 1992 Carl M. Feldherr (editor). NUCLEAR TRAFFICKING, 1992 Christer Sundqvist and Margareta Ryberg (editors). PIGMENT-PROTEIN COMPLEXES IN PLAS- TIDS: SYNTHESIS AND ASSEMBLY, 1993 David H. Rohrbach and Rupert Timpl (editors). MOLECULAR AND CELLULAR ASPECTS OF BASEMENT MEMBRANES, 1993 Danton H. O'Day (editor). SIGNAL TRANSDUCTION DURING BIOMEMBRANE FUSION, 1993 John K. Stevens, Linda R. Mills, and Judy E. Trogadis (editors). THREE-DIMENSIONAL CONFO- CAL MICROSCOPY: VOLUME INVESTIGATION OF BIOLOGICAL SPECIMENS, 1994 Lawrence I. Gilbert, Jamshed R. Tata, and Burr G. Atkinson (editors). METAMORPHOSIS: POST- EMBRYONIC REPROGRAMMING OF GENE EXPRESSION IN AMPHIBIAN AND IN- SECT CELLS, 1996 R. John Ellis (editor). THE CHAPERONINS, 1996 (in preparation) Metamorphosis Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells Edited by Lawrence I. Gilbert Department of Biology College of Arts and Sciences University of North Carolina at Chapel Hill Chapel Hill, North Carolina Jamshed R. Tata National Institute for Medical Research London, United Kingdom Burr G. Atkinson Department of Zoology University of Western Ontario London, Ontario, Canada ACADEMIC PRESS San Diego New York Boston London Sydney Tokyo Toronto Front cover illustration depicts the unified concept of insect and amphibian postembryonic development as illustrated by the major morphological changes that take place during metamorphosis, which are obligatorily regulated by the hormonal signals of ecdysteroids and thyroid hormones, respectively. Illustration courtesy of J. R. Tata and J. W. Brock, MRC National Institute for Medical Research, Mill Hill, London, United Kingdom. This book is printed on acid-free paper. (~ Copyright (cid:14)9 1996 by ACADEMIC PRESS, INC. All Rights Reserved. No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopy, recording, or any information storage and retrieval system, without permission in writing from the publisher. Academic Press, Inc. A Division of Harcourt Brace & Company 525 B Street, Suite 1900, San Diego, California 92101-4495 United Kingdom Edition published by Academic Press Limited 24-28 Oval Road, London NWI 7DX Library of Congress Cataloging-in-Publication Data Metamorphosis : postembryonic reprogramming of gene expression in amphibian and insect cells / edited by Lawrence I. Gilbert, Jamshed R. Tata, Burr G. Atkinson. p. cm.-- (Cell biology series) Includes index. ISBN 0-12-283245-0 (alk. paper) 1. Insects--Metamorphosis. 2. Amphibians--Metamorphosis. 3. Insects--Molecular genetics. 4. Amphibians--Molecular genetics. I. Gilbert, Lawrence I. (Lawrence Irwin), date. II. Tata, Jamshed R. (Jamshed Rustom) III. Atkinson, Burr G. IV. Series. QL494.5.M48 1996 595.7'0334--dc20 95-20630 CIP PRINTED IN THE UNITED STATES OF AMERICA 96 97 98 99 00 01 BB 9 8 7 6 5 4 3 2 1 Contents Contributors ........................................................................ xi Preface ............................................................................... xv I Insects 1 Evolution of Insect Metamorphosis Franti~ek Sehnal, Petr Svfcha, and Jan Zrzavf~ I. Introduction ........................................................................ 4 II. Metamorphosis in Insects ......................................................... 5 III. Insect Phylogeny and Types of Postembryonic Development ............... 12 IV. Role of Hormones in Development of Moder.n Insects ...................... 20 V. Evolution of Insect Metamorphosis ............................................. 33 VI. Conclusions ......................................................................... 50 References .......................................................................... 52 2 Endocrine Cascade in Insect Metamorphosis Lawrence I. Gilbert, Robert Rybczynski, and Stephen S. Tobe I. Introduction ........................................................................ 60 II. Prothoracicotropic Hormone ..................................................... 63 III. Ecdysteroids ........................................................................ 76 IV. Juvenile Hormones ................................................................ 87 V. Epilogue ............................................................................ 97 References .......................................................................... 98 vi Contents 3 Ecdysone-Regulated Chromosome Puffing in Drosophila melanogaster Steven Russell and Michael Ashburner I. Introduction ........................................................................ 109 II. Puffs and Development ........................................................... 111 III. Physiology of Puffs ................................................................ 113 IV. Molecular Biology of Puffs ....................................................... 120 V. Molecular View of Ecdysone-Regulated Gene Expression .................. 136 References .......................................................................... 138 4 Chromosome Puffing: Supramolecular Aspects of Ecdysone Action Markus Lezzi I. Introduction ........................................................................ 146 II. Polytenic State of Interphase Chromatin ....................................... 146 III. Polytene Chromosome Puffs ..................................................... 147 IV. Control of Gene Activities in Ecdysone-Inducible Puff Sites ................ 157 V. Chromosomal Distribution of Proteins Involved in Gene Regulation by Ecdysone ........................................................................... 162 VI. New Look at Gene Regulation by Ecdysone .................................. 168 References .......................................................................... 170 5 Molecular Aspects of Ecdysteroid Hormone Action Peter Cherbas and Lucy Cherbas I. Introduction ........................................................................ 175 II. Vertebrate Precedents ............................................................ 177 III. Ecdysteroid Response Apparatus ............................................... 184 IV. Overview of Ecdysteroid Action ................................................ 207 References .......................................................................... 211 6 Molecular Aspects of Juvenile Hormone Action in Insect Metamorphosis Lynn M. Riddiford I. Introduction ........................................................................ 223 II. Overview: "Status Quo" Action of Juvenile Hormone ....................... 225 III. Modulation of Ecdysteroid Action by Juvenile Hormone .................... 228 IV. Juvenile Hormone Delivery System ............................................. 237 V. Theories of Molecular Action of Juvenile Hormone .......................... 240 References .......................................................................... 243 Contents vii 7 Metamorphosis of the Cuticle, Its Proteins, and Their Genes Judith H. Willis I. Introduction ........................................................................ 254 II. Background ........................................................................ 254 III. Proteins of the Cuticle ............................................................ 258 IV. Messages and Genes That Code for Cuticular Proteins ...................... 265 V. Perspective Gained from Analysis of Cuticular Proteins ..................... 274 References .......................................................................... 277 8 Metamorphosis of the Insect Nervous System James W. Truman I. Introduction ........................................................................ 283 II. Patterns of Development of the Insect Central Nervous System ............ 285 III. Cellular Changes during Metamorphosis of the Central Nervous System .............................................................................. 292 IV. Sex-Specific Differentiation within the Central Nervous System ............ 304 V. Hormonal Regulation of Metamorphic Changes .............................. 307 VI. Relationship of Ecdysone Receptor to Metamorphic Changes in the Central Nervous System .......................................................... 311 References .......................................................................... 315 9 Gene Regulation in Imaginal Disc and Salivary Gland Development during Drosophila Metamorphosis Cynthia Bayer, Laurence von Kalm, and James W. Fristrom I. Metamorphic Development of Imaginal Discs ................................. 322 II. Development of Larval Salivary Glands ........................................ 327 III. 20-Hyroxyecdysone-Regulated Gene Expression .............................. 329 IV. Role of Pattern in Imaginal Disc Morphogenesis ............................. 338 V. The Broad-Complex: A Key Regulator of Drosophila Metamorphosis .... 339 References .......................................................................... 355 10 Genes Involved in Postembryonic Cell Proliferation in Drosophila Elizabeth L. Wilder and Norbert Perrimon I. Introduction ........................................................................ 363 II. Background on Drosophila Development ...................................... 366 III. Cell Proliferation in Larval Tissues ............................................. 367 IV. Mutual Control of Pattern and Proliferation ................................... 378 V. Additional Role for wingless ..................................................... 390 viii Contents VI. Concluding Remarks .............................................................. 393 References .......................................................................... 393 II Amphibians 11 Endocrinology of Amphibian Metamorphosis Jane C. Kaltenbach I. Introduction ........................................................................ 403 II. Thyroid Hormone ................................................................. 405 III. Hypothalamus-Pituitary-Thyroid Hormone Interactions .................... 409 IV. Hormonal Fine-Tuning ........................................................... 414 V. Environmental Influence ......................................................... 420 VI. Concluding Remarks .............................................................. 421 References .......................................................................... 423 12 Neuroendocrine Control of Amphibian Metamorphosis Robert J. Denver I. Introduction ........................................................................ 434 II. Development of the Hypothalamohypophyseal System ...................... 436 III. Roles of Pituitary Hormones in Metamorphosis .............................. 441 IV. Role of Hypothalamus in Controlling Pituitary Secretion during Metamorphosis ..................................................................... 445 V. Neurohormones Controlling Pituitary Secretion during Metamorphosis ... 446 VI. Negative Feedback on the Hypothalamohypophyseal Axis .................. 454 VII. Summary and Future Directions for Research ................................. 455 References .......................................................................... 457 13 Hormonal Interplay and Thyroid Hormone Receptor Expression during Amphibian Metamorphosis Jamshed R. Tata I. Introduction ........................................................................ 466 II. Morphological and Biochemical Responses of Amphibian Larvae to Thyroid Hormones ". ............................................................... 467 III. Thyroid Hormone Receptors .................................................... 479 IV. Expression of Thyroid Hormone Receptor Genes during Metamorphosis 483 V. Wider Implications of Thyroid Hormonal Regulation of Amphibian Metamorphosis ..................................................................... 494 References .......................................................................... 497 Contents ix 14 Thyroid Hormone-Regulated Early and Late Genes during Amphibian Metamorphosis Yun-Bo Shi I. Introduction ........................................................................ 505 II. Thyroid Hormone Receptors .................................................... 507 III. Gene Regulation by Thyroid Hormone during Metamorphosis ............. 509 IV. Correlation of Gene Expression with Tissue Remodeling and Function of Early Response Genes ............................................................ 524 V. Comparison with Insect Metamorphosis ........................................ 530 VI. Conclusion .......................................................................... 531 References .......................................................................... 533 15 Reprogramming of Genes Expressed in Amphibian Liver during Metamorphosis Burr G. Atkinson, Caren Helbing, and Yuqing Chen I. Introduction ........................................................................ 539 II. Expression of Proteins Characteristic of the Adult Liver Phenotype ....... 540 III. Expression of Thyroid Hormone Receptor mRNAs Characteristic of the Adult Liver Phenotype ........................................................... 543 IV. Accumulation of mRNAs Encoding Factors Implicated in Terminal Differentiation and Liver-Specific Gene Expression .......................... 551 V. Summary ............................................................................ 560 References .......................................................................... 562 16 Switching of Globin Genes during Anuran Metamorphosis Rudolph Weber I. Introduction ........................................................................ 567 II. Early Studies on Hemoglobin Transition in Anuran Development ......... 568 III. Molecular and Cellular Analysis of Hemoglobin Transition in Xenopus laevis ................................................................................ 571 IV. Cellular Basis of Hemoglobin Transition in Xenopus laevis ................. 584 V. Concluding Comments ............................................................ 592 References .......................................................................... 593 17 Hormone-Induced Changes in Keratin Gene Expression during Amphibian Skin Metamorphosis Leo Miller I. Introduction ........................................................................ 599 II. Morphogenesis and Differentiation of Skin .................................... 600 III. Changes in Epidermal Keratins during Metamorphosis ...................... 603