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Insect hormones: more than 50-years after the discovery of insect juvenile hormone analogues (JHA, juvenoids)

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This review describes the over half-centennial history of research on insect juvenile hormone (JH) as well as its natural and synthetic bioanalogues (JHA or juvenoids).The leading theories of insect hormone action in growth and metamorphosis were created more than 50 years ago by the pioneers of insect endocrinology, V. B. Wigglesworth, C. M. Williams, V. J. A. Novák, H. Piepho, H. A. Schneiderman and L. I. Gilbert. There are two principal categories of hormones released from the central neuroendocrine system (neurosecretory cells of the brain, corpora cardiaca, corpora allata) that regulate insect growth and metamorphosis. The first is a complex set of neurohormones (neuropeptides) originating in the neurosecretory cells of the insect brain, which are released from the neurohaemal organs, the corpora cardiaca. These neuropeptides are responsible for stimulation of various developmental events, such as the release of the activation hormone, AH. The second category of centrally produced hormones in insects is the morphogenesis inhibiting hormone, or juvenile hormone (JH), produced by the associated endocrine glands, the corpora allata. JH is responsible for induction of the somatic larval growth in young instar larvae and stimulation of reproduction in the feeding adult stages. Wigglesworth (1935) first described JH as an inhibitory hormone; Williams (1957) discovered its active extracts. Sláma (1961) discovered the hormonomimetic or pseudojuvenile effects of various lipid extracts and free fatty acids. In addition to lipid extracts with JH activity, a phenomenon found in various human organs, microorganisms and plants, JH-mimetic materials were found in American paper products in 1964. The source of the so-called “paper factor” was the wood of the Canadian balsam fir. The potential use of these and other analogues of JH as nontoxic, selectively acting “third generation pesticides” stimulated an enormous boom of activity among industrial and academic institutions all over the world, in the pursuit of synthetic JH analogues for replacement of toxic insecticides. For practical reasons, in this review the chemical structures of the synthetic juvenoids have been divided into three categories: a) natural and synthetic, predominantly terpenoid juvenoids known before 1970; b) terpenoid and nonterpenoid juvenoids synthesized and tested before 1980, and; c) predominantly nonterpenoid, polycyclic juvenoids with relatively high JH activity, found and selected for practical use after 1980. Chemical structures of several juvenoids of theoretical or practical importance, together with the essential structure-activity relationships, are outlined in several figures and tables. The total number of all juvenoids reported active in one or more insects species has been estimated to be more than 4000 compounds. A juvenoid molecule has, more or less, a similar molecular size, roughly equivalent to a chain of 15 to 17 carbon atoms, with the presence of some slightly polar functional groups and a more or less lipophilic physico-chemical properties. Beyond these similarities, there are many variations in the structural types of juvenoids, including, derivatives of acyclic terpenoids, arylterpenoids, peptides, heterocyclic and polycyclic juvenoids, phenoxyphenyl juvenoids, juvenoid carbamates, and pyridyl-derivatives. In addition to the generally known and intensively studied effects of juvenoids, such as inhibition of metamorphosis, inhibition of embryogenesis, and stimulation of ovarian growth, there are certain less remarkable and largely unexplored biological effects of juvenoids. Some of those phenomena, which are briefly described in this review, are: a) the effects of juvenoids on embryonic development (ovicidal effects); b) delayed effects of JH on metamorphosis from egg stage; c) sexually transmitted female sterility caused by juvenoid treatments of the males; d) the nonvolatile, biochemically activated juvenogen complexes, generating hormonally active juvenoids by enzymatic hydrolysis of the complex, and; e) antihormones with antijuvenile activity. There are two basic hormonal theories on the regulation of insect metamorphosis by JH that have been proposed during the past 50 years. The first is the theory of Gilbert-Riddiford, which has been widely disseminated at universities worldwide, through textbooks on insect physiology, biochemistry and endocrinology. The second, less renowned, hormonal theory of insect development is that of Novák-Sláma. Briefly, the Gilbert-Riddiford theory is based on several fundamental principles. These are: a) the brain hormone-prothoracic gland (PG) concept created more than 50 years ago and later disproved by Williams; b) the conclusions of Piepho, who suggested that a large concentration of JH would cause a single epidermal cell to develop larval patterns, pupal patterns at medium concentrations, and adult epidermal patterns at zero concentration; c) small amounts of JH are necessary in the last larval instars of endopterygote insects for preventing precocious proliferation of imaginal discs; d) metamorphosis is stimulated by PG through a small endogenous peak of ecdysteroid preceding the large prepupal one; e) ecdysteroids are released from the PG in response to superimposed prothoracicotropic hormone (PTTH) from the brain; f) the true juvenile hormone of the corpora allata is a sesquiterpenoid compound known as epoxy homofarnesoate (JH-I), isolated from the adult male abdomens of the Cecropia silkmoths, and; g) physiological functions of JH and other hormones are regulated at the peripheral level by enzymes (esterase) or genes (methoprene tolerant, Met or a Broad complex gene). The Novák-Sláma theory is based on completely different building blocks. Briefly, these are: a) the PG represent a peripheral organ which is not involved in the regulation of the moulting cycles, instead; b) the PG are a subordinated target of JH (not PTTH), they are inactive during the last larval instar and their removal does not abolish the cycles of moults; c) the PG are used to generate metabolic water during the growth of young larval instars by secreting of an adipokinetic superhormone, which stimulates total combustion of the dietary lipids; d) small, medium, or large concentrations of JH are unimportant, the hormone only needs to be present in the minimum, physiologically effective concentrations; e) an imperative condition for metamorphosis to occur is a virtual absence of JH starting from the second half of the penultimate larval instar; f) JH acts according to an “all-or-none” rule at the single cell level, and the temporal sensitivity to JH is strictly limited to a narrow period at the beginning of the moulting cycle, before the cells begin to divide; g) the corpus allatum never produces JH in a nonfeeding stage, and the sesquiterpenoid juvenoid JH-I cannot be the true JH of insects (it has very low JH activity, 100,000-fold smaller in comparison to human made peptidic juvenoids); h) the developmental cycles are stimulated exclusively by neuropeptides produced by the brain’s neurosecretory cells (AH); i) developmental stimulation by AH has nothing in common with the PTTH or PG; j) when environmental interventions in the hormonal system become obsolete, the regulation of moulting cycles becomes autonomic (hormone independent), supported by the stereotypic instructions coded on the genome; k) during the millions of years of insect evolution, the central neuroendocrine system acquired the superimposed, epigenetic ability to adapt gene functions and synchronize them with essential changes in the environment. A model based on the regulation of insect metamorphosis by simple combination of two hormones (AH, JH) of the central neuroendocrine system is outlined. A possibility that the 4000 known juvenoid molecules act as the feedback or homeostatic factors affecting permeability of the epidermal cell membranes has been suggested. Speculations about possible peptidic or proteinic nature of the corpus allatum hormone have been emphasized.

Affiliations: 1: Institute of Entomology, Czech Academy of Sciences, Drnovská 507, 16100 Praha 6, Czech Republic, e-mail: slama@entu.cas.cz

10.1163/18749836-06041073
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2013-03-31
2016-12-06

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