A review of the role of neurosecretion in the control of juvenile hormone synthesis: a tribute to Berta Scharrer

In the 1950s, Berta Scharrer predicted that neurosecretions from the brain regulated corpus allatum activity based upon the observation of the change in localization of neurosecretory material in the brain and change in gland activity after severance of nerves between the brain and corpus allatum. Isolation and characterization of neuropeptide regulators of juvenile hormone production by the corpora allata in the late 1980s has confirmed this prediction. Both a stimulatory allatotropin and an inhibitory allatostatin have been isolated from moth brains. Two families of allatostatins, both quite different from each other and that of moths, have been isolated from cockroaches and crickets.The wide distribution of these peptides in the nervous system, in nerves to visceral muscle, in endocrine cells of the midgut and in blood cells, indicate multifunctions in the insects in which they are allatoregulatory. Some of these other functions have been demonstrated in these insects and in insects in which these neuropeptides occur but do not act as corpus allatum regulators. For the latter group, the neuropeptide regulators of the corpora allata have yet to be isolated. The families of neurosecretory regulators will continue to grow.     

Ultrastructural localization of unique neurosecretory granules in the corpora cardiaca of the stable fly,Stomoxys calcitrans,and the Tsetse Fly,Glossina morsitans

Ultrastructural analysis of the corpora cardiaca of the stable fly, Stomoxys calcitrans, and the tsetse fly, Glossina morsitans, revealed the presence of elementary neurosecretory granules (ENG) unique to the intrinsic neurosecretory cells (INC) of these species. In addition to electron‐dense spheres, the INC of the corpus cardiacum of the stable fly contain electron‐dense angular granules, either square or rectangular in shape, while the INC of the tsetse fly contain electron‐dense spindle‐shaped ENG. The distinctive granules of these INC can be traced within nerves to their sites of storage and release, eliminating the need for labeling with artificial probes. Although the INC of the corpus cardiacum of most species have been found to be fuchsinophilic, neither the INC of the stable fly nor the tsetse fly are aldehyde‐fuchsinophilic. These peptigenic cells offer neuroendocrinologists a unique opportunity to study the physiology and biochemistry of neurosecretory cells. J. Morphol. 240:155–168, 1999. Published 1999 Wiley‐Liss, Inc.     

Early immunohistochemical detection of somatostatin-like and methionine-enkephablin-like neuropeptides in the brain of the migratory locust embryo

The two groups of neurosecretory cells producing neuropeptides related to somatostatin (SRIF) and methionine-enkephalin (met-enkephalin), previously high-lighted in the brain of adult migratory locusts, were detected by immunofluorescent techniques during the embryonic development of these insects. The earliest detection of these neurosecretory products occurred firstly in the terminal arborizations, then in the fibres, and finally in the perikarya. SRIF-like material is present in the corpora cardiaca already four days before hatching, i.e. at two-thirds of embryonic life, whereas immunoreactivity can be detected only after hatching in the perikarya located in the pars intercerebralis. The synthesis of met-enkephalin-like neuropeptide starts in the four cells of this system at least two days before hatching as shown by the immunofluorescence in the terminal arborizations along the tractus I to the corpora cardiaca. SRIF-like and met-enkephalin-like neurosecretory products are synthesized and carried to their release areas whilst the formation of brain structures and of the corpora cardiaca has not yet been completed.     

THE NEUROENDOCRINE SYSTEM AND STOMATOGASTRIC NERVOUS SYSTEM OF THE ADULT TSETSE FLY GLOSSINA MORSITANS

The brain of Glossina morsitans Westwood contains four groups of neurosecretory cells which are stainable with chrome haematozylin and phloxin. The axons of these cells form a pair of nervi corporis cardiaci which pass posteriorly from the brain and innervate the corpora cardiaca and corpus allatum before uniting with a small ganglion posterior to the corpora cardiaca. This ganglion is considered to represent the fusion of the fusion of the hypocerebral and ventricular ganglia which remain separate in other insects.
There is no frontal ganglion in the adult Glossina and the recurrent nerve fuses with one of the nervi corporis cardiaci immediately behind the brain. The oesophageal nerves arising from the fused hypocerebral and ventricular ganglia innervate the oesophagus in the anterior part of the thorax, the proventriculus and the posterior extension of the oesophagus close to the crop. These nerves possess both sensory and motor nerve endings. The differences which exist between Glossina and other cyclorrhaphous Diptera with respect to their neuroendocrine/stomatogastric system are noted and considered in terms of the control of neuroendocrine function.     

The Corpus Cardiacum Neurosecretory Cells of Schistocerca gregaria. Electron Microscopy of Resting and Secreting Cells

The corpora cardiaca of Schistocerca consist of a neurohaemal part containing mainly extrinsic neurosecretory axons coming from the brain, and of a glandular part consisting mainly of intrinsic neurosecretory cells. Some extrinsic axons penetrate into the glandular region, and innervate intrinsic corpus cardiacum neurosecretory cells. The fine structure of the latter has been examined and related to other neurosecretory cell types. Secretion occurs by exocytosis. Omega-profiles are more frequently observed in corpora cardiaca stimulated electrically or by acetylcholine than in the controls.     

Leucokinin and diuretic hormone immunoreactivity of neurons in the tobacco hornworm,Manduca sexta,and co-localization of this immunoreactivity in lateral neurosecretory cells of abdominal ganglia

Because leucokinins stimulate diuresis in some insects, we wished to identify the neurosecretory cells in Manduca sexta that might be a source of leucokinin-like neurohormones. Immunostaining was done at various stages of development, using an antiserum to leucokinin IV. Bilateral pairs of neurosecretory cells in abdominal ganglia 3–7 of larvae and adults are immunoreactive; these cells project via the ipsilateral ventral nerves to the neurohemal transverse nerves. The immunoreactivity and size of these lateral cells greatly increases in the pharate adult, and this change appears to be related to a period of intensive diuresis occurring a few days before adult eclosion. Relationships of these neurons to cells that are immunoreactive to a M. sexta diuretic hormone were also investigated. Diuretic hormone and leucokinin immunoreactivity are co-localized in the lateral neurosecretory cells and their neurohemal projections. A median pair of leucokinin-immunoreactive, and a lateral pair of diuretic hormone-immunoreactive neurons in the larval terminal abdominal ganglion project to neurohemal release sites within the cryptonephridium. The immunoreactivity of these cells is lost as the cryptonephridium is eliminated during metamorphosis. This loss appears to be related to the change from the larval to adult pattern of diuresis.     

Contribution à l'étude infrastructurale du système neurosécréteur rétrocérébral chez Locusta migratoria migratorioides (R. et F.)

Résumé L'étude infrastructurale des corpora cardiaca de Locusta révèle l'existence de 3 types de fibres neurosécrétrices (portion neurohémale) et d'un seul type de cellules glandulaires (portion endocrine intrinsèque). Elle permet également d'envisager les modalités du rejet des sécrétions exogènes et endogènes.

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Ultrastructural study of the retrocerebral neurosecretory system in Locusta migratoria migratorioides (R. et F.)I. The corpora cardiaca

Summary An ultrastructural study of the corpora cardiaca of Locusta migratoria migratorioides shows three neurosecretory fiber types in the neurohaemal part of these organs; only one cellular type constitutes the intrinsic glandular part of the corpora cardiaca. This study also shows sites of release of stored extrinsic neurosecretory material and of products elaborated by intrinsic glandular cells of the corpora cardiaca.

     

Methylxanthine inhibition of neurosecretion in the brain and corpus cardiacum of Cecropia

The fine-structure of the median neurosecretory cells and corpora cardiaca of the Cecropia silkmoth during the first 7 days after transfer from cold conditions to room temperature was compared to that of similar animals whose development was arrested with aminophylline. The major difference observed was the failure of the intrinsic secretory cells of the corpus cardiacum to degenerate in the arrested animals. This failure to degenerate coincides with the expected period of brain hormone release. After long periods of arrest, the medial neurosecretory cells and their axons became distended with neurosecretory granules. The significance of these observations in the initiation of adult development is discussed.     

Studies on the neurosecretory system and retrocerebral endocrine glands of Nezara viridula Linn. (Heteroptera: Pentatomidae)

The neurosecretory system and retrocerebral endocrine glands of Nezara viridula Linn. have been described on the basis of in situ preparations and histological sections employing the paraldehyde fuchsin (PF) and performic acid-victoria blue (PAVB) techniques. In the brain of N. viridula, there are two medial groups–each consisting of five neurosecretory cells which belong to A-type. The lateral neurosecretory cells are absent. The axons of the two groups of medial neurosecretory cells (MNC) compose the two bundles of neurosecretory pathways (NSP) that decussate in the anterodorsal part of the protocerebrum. The two pathways, after the cross-over, run deep into the protocerebrum and deutocerebrum and emerge as NCC-I from the tritocerebrum. The nervi corporis cardiaci-I (NCC-I) of each side which are heavily loaded with NSM terminate in the aorta wall. Thus, the neurosecretory material (NSM), elaborated in the medial neurosecretory cells of the brain, is stored in the aortic wall and nervi corporis cardiaci-I (NCC-I). The NCC-II are very short nerves that originate from the tritocerebrum and terminate in the corpora cardiaca (CC) of their side. Below the aorta, but dorsal to the oesophagus, lie two oval or spherical corpora cardiaca. A corpus allatum (CA) lies posterior to the corpora cardiaca (CC). The corpora cardiaca do not contain NSM; only the intrinsic secretion of their cells has been occasionally observed which stains orange or green with PF staining method. The corpus allatum sometimes exhibits PF positive granules of cerebral origin. A new connection between the corpus allatum and aorta has been recorded. The suboesophageal ganglion contains two neurosecretory cells of A-type which, in structure and staining behaviour, are similar to the medial neurosecretory cells of the brain. The course and termination of axons of suboesophageal ganglion neurosecretory cells, and the storage organ for the secretion of these cells have been reported. It is suggested that the aortic wall and NCC-I axons function as neurohaemal organ for cerebral and suboesophageal secretions.     

Ultrastructure of retrocerebral complex of the earwig, Euborellia annulipes, and rôle of aorta as a neurohaemal organ

The ultrastructure of the retrocerebral endocrine-aortal complex of the earwig, Euborellia annulipes has been studied. The space between the inner and outer stromal layers of the aorta is occupied by numerous axon terminals and pre-terminals containing large electron dense granules (NS-I) of approximately 100 to 220 nm and a few axon terminals having small granules (NS-II) of approximately 40 to 90 nm; the former appear to belong to medial neurosecretory A-cells, and the latter to the B-cells of the brain. The corpora cardiaca consist of intrinsic cells with mitochondria and multivesicular bodies. Granules of type NS-II and NS-III are observed in the axon terminals and pre-terminals in the corpora cardiaca. The NS-II are identical to those found in the aorta and are probably the secretions of the lateral B-cells. Granules of type NS-III are 40 to 120 nm and electron dense, and are intrinsic in origin. Similar granules occur in the intrinsic cells of the corpora cardiaca. E M studies have confirmed the rôle of the aorta as a neurohaemal organ for the medial neurosecretory cells, and the corpora cardiaca for the lateral neurosecretory cells of the brain. The corpora cardiaca also act as a reservoir for the intrinsic secretion. The corpus allatum is a solid body consisting of parenchymal cells with prominent nuclei, mitochondria, and endoplasmic reticulum. In between its cells are occasional glial cells and also neurosecretory as well as non-neurosecretory axons. The gland is devoid of A-cell NSM.     

Regulation of the corpora allata in the black mutant of Manduca sexta

Regulation of corpus allatum activity in the black mutant strain of Manduca sexta was studied in vivo and in vitro. Allatectomy, denervation, and implantation studies demonstrated that black mutant corpus allatum activity remains low in both wild-type and black mutant host larvae. Attempts to distinguish humoral control mechanisms versus mechanisms dependent on intact allatal nerves indicated that intact allatal nerves were not required for the reduced black mutant corpus allatum activity in vivo. Incubation of corpora allata, using [1-¹⁴C]propionate as a juvenile hormone biosynthetic precursor and haemolymph as culture medium, confirmed that black mutant corpora allata are suppressed by a factor(s) in the haemolymph. Under identical conditions wild-type corpora allata were unaffected. Finally, the lowered black mutant corpus allatum activity in haemolymph in vitro correlates with the lowered juvenile hormone titre in black mutant larvae.     

Neurosecretory system of the earwig Labedura riparia, and the rôle of the aorta as a neurohaemal organ

The neurosecretory system of Labedura riparia has been described from sections and whole mounts using a variety of techniques. The pars intercerebralis contains two clusters of medial neurosecretory cells (MNC), each cluster consisting of 8 to 10 A-cells and occasional B-cells. The lateral sides of the brain have a few B-cells. The axons of the median neurosecretory cells terminate in the cephalic aorta (AO), whereas the axons of the lateral neurosecretory cells (LNC) terminate in the corpora cardiaca (CC). It appears that the neurosecretory material (NSM) elaborated in the MNC is stored in the cephalic aorta and that elaborated in the LNC is stored in the corpora cardiaca, which are two oval or elongate bodies composed of large chromophobe and small chromophil cells. Posteriorly there is the oval or elongate corpus allatum (CA) attached to the CC by thick nerves. The CA consists of one cell type only. Both CC and CA contain no A-cell neurosecretory material. It has been suggested that the neurosecretory system of L. riparia is composed of two complexes. One is formed by the medial neurosecretory cells for which the aorta functions as a neurohaemal organ, and the other is formed by lateral neurosecretory cells-lateral neurosecretory pathways-nervi corporis cardiaci-II in which the corpora cardiaca function as a neurohaemal organ.     

Extracerebral caphalic neuroendocine complex of the blattids,Periplaneta americana (L.) and Neostylopyga rhombifolia (Stoll): An in situ study

A cardiaca-allatal commissural plexus (CACP) lies between and partly overlapping the postcommissural lobes of the corpora cardiaca (CC), the nervi corpori allati I (NCA I) and the corpora allata (CA). CACP, which is often continuous posteriorly with a complicated postallatal plexus (PAP), comprises a variable number of connectives with neurosecretory processes linking the cardiaca-commissural organ or dorsal cardiac commissure (containig tritocerebral fibres) to the NCA I. the allatal commissure and the CA. Neurosecretory processes are exchanged between the two halves of the cephalic neuroendocrine complex (CNC) both intracerebrally at different locales, possibly to ensure functional synchrony of CNC components. NCA I and CACP are drawn out with their stroma to varying extents over the CA. Histophysiological evidence suggests that part of the stainable secretion stored in, and or in axonal transit through CA may be released through CA surface; NCA I, the nervi cardiostomatogastrici, CACP, perhaps also NCA II may function as neurohaemal areas. A “directed” neurosecretory pathway could be distinguished from PAP to the foregut and the fat body. The degree of spatial intimacy detected between neurosecretory and stomatogastric components of CNC suggests that the two systems may function in an integrated fashion. The recurrent-oesophageal nerve complex serves not only for a direct transport of neurosecretion, but also as one of the sites of its release.     

Diversity of neurohormonal release sites in insects: Neurohemal areas associated with peripheral neurosecretory cells in Periplaneta americana L. (Dictyoptera: Blattidae) and Locusta migratoria R. & F. (Orthoptera : Locustidae)

Neurohemal areas are located on the distal region of the transverse nerve and on the link nerve of the cockroach, Periplaneta americana (Dictyoptera : Blattidae) and the locust, Locusta migratoria (Orthoptera : Locustidae). They constitute the sites at which the peripheral neurosecretory cells on these nerves discharge their products. Histological and ultrastructural studies suggest that, at least in Periplaneta, these areas also serve to release neurosecretory products different from those found in the perisympathetic organs (POs). These products come from the ganglion cells, some of them via the transverse nerve, and others, via the somatic nerves. The existence of these neurohemal areas broadens the problem of the release zones and shows that the POs are not the only neurohemal structures associated with ventral ganglion cells. An attempt is made to explain the reason for the existence of these different release sites, as well as the role of the peripheral cells.     

CAPA-gene products in the haematophagous sandfly Phlebotomus papatasi (Scopoli) – vector for leishmaniasis disease

Sandflies (Phlebotominae, Nematocera, Diptera) are responsible for transmission of leishmaniasis and other protozoan-borne diseases in humans, and these insects depend on the regulation of water balance to cope with the sudden and enormous intake of blood over a very short time period. The sandfly inventory of neuropeptides, including those that regulate diuretic processes, is completely unknown. Direct MALDI-TOF/TOF mass spectrometric analysis of dissected ganglia of Phlebotomus papatasi, combined with a data-mining of sandfly genome ‘contigs’, was used to identify native CAPA-peptides, a peptide class associated with the regulation of diuresis in other hematophagous insects. The CAPA-peptides identified in this study include two CAPA-PVKs, differentially processed CAPA-PK, and an additional CAPA precursor peptide. The mass spectrometric analysis of different parts of the neuroendocrine system of the sandfly indicate that it represents the first insect which accumulates CAPA-PVKs exclusively in hormone release sites of abdominal ganglia and CAPA-PK (nearly) exclusively in the corpora cardiaca. Additionally, sandflies feature the smallest abdominal ganglia (∼35 μm) where CAPA-peptides could be detected so far. The small size of the abdominal ganglia does not appear to affect the development of the median neurosecretory system as it obviously does in another comparably small insect species, Nasonia vitripennis, in which no capa-gene expression was found. Rather, immunocytochemical analyses confirm that the general architecture in sandflies appears identical to that of much larger mosquitoes.     

Morphology of neurones associated with the antennal heart of Periplaneta americana (Blattodea,Insecta)

Summary Innervation of the antennal heart, an independent accessory circulatory motor in the head of insects, was investigated in the cockroach Periplaneta americana by use of axonal cobalt filling and transmission electron microscopy. The muscles associated with this organ are innervated by neurones located in a part of the suboesophageal ganglion, generally considered to be formed by the mandibular neuromere. Dorsal unpaired median (DUM) and paired contralateral neurones were stained. The axons of all these neurones run along the circumoesophageal connectives and through the paired nervus corporis cardiaci III into the corpora cardiaca. They pass through these organs forming fine arborizations there and exit anteriorly as a small pair of nerves which terminate at the antennal heart-dilator muscles. Numerous branches of these nerves extend beyond the lateral borders of the large transverse dilator muscle and terminate in the ampullar walls of the antennal heart. These neurosecretory fibres form neurohaemal areas which obviously release their products into the haemolymph, which is pumped into the antennae. The possible functions of the neurones associated with the antennal heart are discussed with respect to both, their role as a modulatory input for the circulatory motor and as a neurohormonal release site.     

Farnesoid secretions of dipteran ring glands: what we do know and what we can know

Harnessing of the Drosophila genetic system toward ascertaining the molecular endocrinology of higher dipteran (cyclorrhaphan) larval development has been a goal for over 70 years, beginning with the data left to us by pioneer researchers from the classical endocrine era. The results of their experiments evidence numerous ring gland activities that are parsimoniously explained as arising from secretions of the larval corpora allatal cells. Utilization of those data toward an understanding of molecular endocrinology of cyclorrhaphan metamorphosis has not yet achieved its hoped for fruition, in part due to a perceived difficulty in identifying larval targets of the molecule "methyl epoxyfarnesoate" (=juvenile hormone III). However, as is reviewed here, it is important to maintain a conceptual distinction between "the target of JH III"Versus "the target(s) of products secreted by the larval corpora allatal cells of ring glands." Recent advances have been made on the identity, regulation and reception of ring gland farnesoid products. When these advances are evaluated together with the above data from the classical endocrine era, there is a new opportunity to frame experimental hypotheses so as to discern underlying mechanisms on cyclorrhaphan larval-pupal metamorphosis that have been heretofore intractable. This paper reconsiders a number of evidenced physiological targets of secretions of corpora allatal cells of the larval ring gland, and places them in the context of more recent biochemical and molecular advances in the field.     

An electron microscopic study of the corpus cardiacum of adult Drosophila melanogaster and its afferent nerves

The left and right afferent nerves to the corpus cardiacum contain approximately 50 and 90 axons, respectively, when they enter the gland. Both bifurcate within the gland, so that four nerves leave the corpus cardiacum. These, however, contain a total of 90 axons. Of the 50 axons unaccounted for 30 are believed to terminate in the corpus cardiacum and 20 in the corpus allatum. The corpus cardiacum contains 12 intrinsic neurosecretory cells which are disposed laterally with respect to the extrinsic axons. Many of these contain neurosecretory spheres and presumably originate in the brain. The intrinsic corpus cardiacum cells also contain neurosecretory granules, and they produce short cytoplasmic processes which interdigitate with the extrinsic axons.     

Neurosecretory cells in Dysdercus similis (Hemiptera)

The neurosecretory cells of Dysdercus similis have been described. "A", "B", "C" and "D" types of neurosecretory cells are present. The "A" type of cells of the pars-intercerebralis show cyclical secretion. When these cells show secretory activity during one to three days of emergence, they have scattered granules. The cells are seen packed with clumps of neurosecretory material when they are not secreting, and this is interpreted as a storage stage. The axons of these cells supply the corpora cardiaca and some neurosecretory material also reaches the corpus allatum. The release of this neurosecretory material can be correlated both with moulting in the young stages and later with reproduction in the adults.