Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells

Metamorphosis: Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. LAWRENCE I. GILBERT, JAMSHED R. TATA, AND BURR G. ATKINSON, eds. Academic Press. 1996. 687 pages. $125.00. ISBN 0-12-283245-0.

This is the third volume of Metamorphosis, a series of texts edited by Gilbert and various associates at 13 to 15 year intervals that provide eclectic but up-to-date reviews of the endocrine, cellular, and molecular biology of animal metamorphoses. We can't really call these volumes editions, because they are quite independent windows on the state of the art of our knowledge about postembryonic development. As such, they do not build on each other and overlap little in authorship and chapter topics, nor do they attempt to cover the breadth of the field. As a trio, these volumes do present an interesting perspective on the scientific and political preoccupations of the era when each was produced. The first volume (1968, by Etkin and Gilbert), deals primarily with the diversity of metamorphoses in a broad range of phyla, and with the cellular and biochemical changes that accompany metamorphosis. A clear, but clearly premature, desire to analyze metamorphosis at the genetic and biochemical level is evident. In the second volume (1981, by Gilbert and Frieden) the coverage of diversity is retained, but the focus is now on the biochemistry of hormones, their synthesis and degradation, and the molecular events (then defined as protein and nucleic acid synthesis) that follow when cells and tissues are exposed to a hormone. In keeping with its time, the tone of that volume reflected the enthusiasm of the late 1970's when early methods of macromolecular analysis had become widely used and enabled researchers to directly study gene expression during animal development. Important problems in biology were becoming defined as those that could be addressed by using molecular techniques.

The present volume, produced at a time when genetic determinism is the dominant doctrine in molecular and developmental biology, bears the timeappropriate subtitle Postembryonic Reprogramming of Gene Expression in Amphibian and Insect Cells. There are 19 chapters, of which four indeed deal with the problems that attend reprogramming of gene expression. These are the chapters by Willis (on reprogramming of protein expression in the insect cuticle), by Atkinson, Helbing and Chen (reprogramming of gene expression in amphibian liver), Weber (switching of globin genes in amphibians), and Miller (changes in keratin gene expression in amphibians). Diversity, so prominent in earlier volumes, has disappeared, and there is but a single chapter that deals with the morphological and structural consequences of metamorphosis, that by Truman on the metamorphosis of insect nervous systems. Four chapters provide general overviews of the evolution of insect metamorphosis (Sehnal, Svacha and Zrzavy), the endocrine control of insect metamorphosis (Gilbert, Rybczynski and Tobe), and the endocrine control of amphibian metamorphosis (by Kaltenbach and by Denver).

The real focus of this volume is on two aspects of the molecular events that attend metamorphosis. The first of these concerns the temporal and spatial patterns of gene expression that follow upon exposure to a hormone. These are discussed in chapters by Ashbumer and by Lezzi on salivary gland chromosome puffing; by Bayer, Von Kalm and Fristrom on the imaginal disks of Drosophila (highlighting the critical role played by the Broad-Complex gene); by Wilder and Perrimon on the genes associated with cell proliferation in Drosophila; and for amphibians in the chapters by Shi on thyroid hormone-regulated genes, and Yoshizato on hormone-induced and programmed cell death in amphibian metamorphosis.

The second focus concerns the molecular biology of hormone receptors, and this is clearly where the real advances in our understanding of the endocrine control of metamorphosis are being made at present. A nice review of the current state of our knowledge of the ecdysone receptors is given by Cherbas and Cherbas, and for the thyroid hormone receptors by Tata and by Shi. Both ecdysone and thyroid hormone receptors are members of the nuclear steroid hormone receptor superfamily and share interesting structural and functional features. Structurally they exhibit a permutation of heterodimeric pairings among a small set of peptides, which produces a diversity of molecular combinations that may be involved in controlling differential hormonal responses. Functionally they share the peculiarity that they are upregulated in response to their respective hormone, a phenomenon Tata calls autoinduction. Dimerization, heterodimerization, and autoinduction appear to be the shared primitive characters of this receptor system.

Juvenile hormone continues to pose problems, both conceptual and practical. On the conceptual level we find a few authors who still advocate the old view that tissues somehow respond differentially to different titers of JH in controlling the expression of larval, pupal and adult characters. This view arises from an attempt to reconcile in a single model a hodgepodge of fragmentary and incommensurate data from phylogenetically distant systems. When a single system is studied in detail, like Riddiford has done with the epidermis of Manduca, it is generally found that JH acts as a status quo agent that controls a binary developmental switch at a single discrete threshold of concentration characteristic of the tissue. On the practical level, the nuclear JH receptor continues to be elusive, and assays for JH continue to be technically demanding. Riddiford concludes her chapter on the role of JH in metamorphosis with the suggestion that JH may have multiple mechanisms of action: it may act indirectly on genes through interactions with transcription factors, and it may act via a membrane receptor pathway as well.