insect endocrinology

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ANNUAL REVIEWS

Further

Quick links to online contentAnn. Rev. Physiol. 1980. 42:511-28 Copyright 1980 by Annual Reviews Inc. All Rights reserved

INSECT ENDOCRINOLOGY: Action of HormonesAnnu. Rev. Physiol. 1980.42:511-528. Downloaded from www.annualreviews.org by Universidade Estadual de Feira de Santana on 11/19/12. For personal use only.

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at the Cellular LevelLynn M

Riddiford

Department of Zoology, University of Washington, Seattle, Washington 98195

The endocrine regulation of the life of the insect is based on the ecdysteroids (ecdysone, 20-hydroxyecdysone), juvenile hormone (JH), and a myriad of neurosecretory peptide hormones,most of which have yet to be purified and sequenced. Ecdysteroids and JH control both growth and development and later reproductive maturation. The neurohormones regulate the release of these two hormones and also a variety of homeostatic activities and behav ior. The preceding review in this volume (47) discusses the regulation of the endocrine glands and the chemistry and metabolism of the hormones. This review is concerned with the hormonal regulation of physiological pro cesses. Since there have been many recent reviews of various aspects of insect endocrinology and insect hormone action (13, 26, 36,48, 50-52, 60, 99, 111, 112, 120) I concentrate here on a few systems that promise to better our understanding of the action of ecdysteroids and juvenile hormone at the cellular level, in both morphogenesis and reproduction. I then discuss the actions of two identified peptide hormones.MORPHOGENETIC ACTIONS OF ECDYSONE AND JUVENILE HORMONE

Since an insect lives within a rigid exoskeleton or cuticle, growth necessitates the periodic shedding of this cuticle and the production of a larger one.

This process of molting is controlled by ecdysone from the prothoracic glands, which is converted to 20-hydroxyecdysone, the active hormone, by511

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the peripheral tissues (47). Since growth always occurs in the larval stages and is terminated at metamorphosis, a second hormone, juvenile hormone, from the corpora allata ensures larval molting. When the insect approaches its maximum size,the JH titer declines,allowing the ecdysteroids to initiate metamorphosis. The cellular changes associated with larval molting occur primarily in the epidermis; but at metamorphosis internal changes also occur.Epidermis and Cuticle Formation The insect epidermis is a single cell layer of electrically coupled cells (21) that produces the overlying cuticle, each cell molding the surface pattern of the cuticle lying above it (127). Although epidermal cells are regarded as differentiated cells that make the cuticle, they can further differentiate into specialized structures such as bristles or hairs at the time of the molt (128). Most insect epidermal cells can produce various kinds of cuticle i.e. larval, pupal, or adult, depending on the hormonal milieu. The cytological events occurring in the epidermis in preparation for the molt have been described in detail (reviewed in 73, 86, 133). The following sequence of events generally occurs: The cells detach from the overlying cuticle (apolysis); an ecdysial membrane is secreted that separates the old cuticle from the one to be made; the molting gel is secreted,followed by the new epicuticle, consisting primarily of proteins and lipids, and the new procuticle of chitin and protein (4). Usually late in this sequence the en zymes in the molting fluid, often including enzymes in the cuticle itself (7), are activated and digest the old procuticle leaving the epicuticle to be shed at ecdysis. After ecdysis the new cuticle is sclerotized by a cross-linking of the proteins with each other and with chitin (4), a process often accelerated by the hormone bursicon (86, 99). Thus the insect epidermal cell is primar ily a secretory unit that makes and releases various products in a defined sequence in response to a hormonal stimulus. The cell must also undergo any cell division and/or differentiation dictated by the hormonal milieu at the beginning of this sequence. Ecdysone, which initiates cuticle formation and directs its progress, is present in the insect through the beginning of procuticle deposition (35, 99). The hormonal control of this cuticular deposition is now being studied primarily in tissue culture. Irrespective of whether the epidermis is from embryos (16,17),body wall (20,39,78,82,83,101),or from imaginal discs or their derivatives (76, 78, 81, 85, 88, 129), cuticle formation complete with differentiated bristles requires exposure to about 10--6 to 10-7 M 20hydroxyecdysone (,B-ecdysone or ecdysterone) [similar to the titers being reported in the hemolymph (126)] for a defined length of time. In most systems a definite concentration-time relationship governs cuticle formation (20, 78,82, 85). Furthermore,ecdysone (a-ecdysone). the hormone secreted

Annu. Rev. Physiol. 1980.42:511-528. Downloaded from www.annualreviews.org by Universidade Estadual de Feira de Santana on 11/19/12. For personal use only.

CELLULAR ACTIONS OF INSECT HORMONES

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Annu. Rev. Physiol. 1980.42:511-528. Downloaded from www.annualreviews.org by Universidade Estadual de Feira de Santana on 11/19/12. For personal use only.

by the prothoracic glands (47, 48), appears to be about 1 % as effective as 20-hydroxyecdysone on epidermis (20, 39, 76, 78, 98), which indicates that it is a prohormone (47, 48). Whether ecdysone has any role itself in activat ing the epidermis is still an open question; several workers have suggested that it may be important in stimulating very early cellular changes-e.g. DNA synthesis (18, 67), appearance of rough endoplasmic reticulum, and increased mitochondrial number (20). Low concentrations of 20-hydroxy ecdysone can also cause these changes. (20). Thus before any definite conclusions can be drawn the role of the epidermis in the metabolism of ecdysone to 20-hydroxyecdysone must be clarified. The biochemistry of 20-hydroxyecdysone-stimulated cellular events lead ing up to cuticle production is being pursued profitably in the imaginal disc system (discussed below). The hormonal regulation of the type of cuticle deposited can be studied best in other kinds of epidermis. Thus far, two lepidopteran systems seem ideal for studying the morphogenetic role of JH in cuticle deposition: pupal wing epidermis (129) and larval abdominal epidermis (83, 101). In response to 20-hydroxyecdysone the former forms either adult cuticle with scales and hairs in the absence of JH or pupal cuticle in its presence. Similarly, the larval epidermis forms either new larval cuticle in the presence of JH or pupal cuticle in its absence. In both cases, the pattern of proteins synthesized in the presence of JH and 20hydroxyecdysone differs from that synthesized in the presence of 20hydroxyecdysone alone (100, 129). What these differences mean remains unclear, especially since some do not seem to be cuticular proteins (129).Sclerotization and Tanning of the Cuticle

After ecdysis the newly formed cuticle hardens and often darkens in a process called sclerotization (3, 4). This process is governed usually by neurosecretory hormones, though the ecdysteroids may also be involved in some instances (59, 99). At the time of metamorphosis in flies, the last stage larval cuticle hardens and darkens to form the puparium within which the pupa develops. At first the ecdysteroids were thought to initiate this process by turning on the gene for dopa decarboxylase (59), a key enzyme in quinone tanning (3). Yet dopa decarboxylase activity increases before the release of ecdysone to initiate puparium formation (109). This apparent paradox is resolved by the finding that 20-hydroxyecdysone serves mainly to increase the rate of synthesis of this enzyme (42) in the epidermis, probably by increasing the rate of mRNA synthesis. &dysone then later causes the release into the hemolymph of a neurosecretory hormone, "puparium tanning factor" (PTF), which initiates the tanning process (109). PTF appears to act via cAMP (41, 109), which can substitute for the factor in the presence of an RNA synthesis inhibitor (actinomycin) but not in the presence of protein synthesis inhibitors. Since

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Annu. Rev. Physiol. 1980.42:511-528. Downloaded from www.annualreviews.org by Universidade Estadual de Feira de Santana on 11/19/12. For personal use only.

the addition of dopa or dopamine but not of tyrosine has the same effect, Fraenkel et al (41) have speculated that PTF acts somehow on the initial step in the pathway to convert tyrosine to dopa. In most insects, the tanning of the Dew cuticle after ecdysis is controlled by another neurosecretory hormone, bursicon (86, 99). In the tobacco homworm, Manduca sexta, bursicon is released from two identified neu rons in each abdominal ganglion (P. Taghert, personal communication) into the hemolymph immediately after adult eclosion (95). It causes the in creased plasticization of the wings that allows full wing expansion (93). This plasticization is then followed by tanning of the wings. Bursicon from M. sexta has now been purified to near homogeneity and appears to be a peptide of about 9000 daltons (P. Taghert, personal communication). The precise mode of action of bursicon is not known, but it is thought to affect transport of tanning precursors into the hemocytes and/or the epidermal cells (86). It appears to increase cAMP levels in both of these cells (34, 86), though in the epidermal cells the evidence is only correlative. The critical experiments await a pure hormone preparation whose action on isolated cells can be defined.

Cellular Reprogramming of the EpidermisThe larval epidermis of Lepidoptera and probably also Coleoptera seems id