Proctolin in the antennal circulatory system of lower Neoptera: a comparative pharmacological and immunohistochemical study

Abstract

Neuropeptides are important with respect to almost all physiological processes and behavioural patterns in an organism. In the present study, muscle bioassays, immunohistochemistry and matrix-assisted laser desorption ionization timeof-flight (MALDI-TOF) mass spectrometry are used to investigate the distribution and efficacy of proctolin in the antennal heart of 36 species of lower Neoptera. In total, 20 species of Dictyoptera (cockroaches, termites, praying mantids), eight species of Saltatoria (crickets and grasshoppers) and eight species of Phasmatodea (stick insects) are investigated. The antennal heart of all tested Blattoidea, including the termite Mastotermes darwiniensis Froggatt, exhibit a strong proctolin-like immunoreactivity, as well as a high sensitivity to proctolin, whereas members of the second clade of cockroaches (Blaberoidea) are largely insensitive to proctolin and show only a weak proctolin-like immunoreactivity. The antennal heart of praying mantids (Mantodea) also contains only few proctolin-like immunoreactive fibres but is highly sensitive to proctolin. Such a high sensitivity is found also in Phasmatodea, although the antennal heart of these insects does not have proctolin-like immunoreactive fibres. These findings are supported by MALDI-TOF mass spectrometry; no trace of proctolin is detected in antennal heart preparations of Phasmatodea. In Saltatoria, only weak (or no) effects of proctolin are observed and, in most subtaxa, no proctolin-like immunoreactivity is visible in the antennal heart preparations. Only in Grylloidea is strong proctolin-like immunostaining found in processes of the antennal heart. In these species, weak or moderate effects of proctolin are observed in the antennal heart bioassay. In general, the differences in distribution of proctolin and effects on the antennal heart within the basal Neoptera cannot be deduced from their phylogenetic position, although they show conformity within each (sub)taxon.

Hemolymph circulation in insect flight appendages: physiology of the wing heart and circulatory flow in the wings of the mosquito,Anopheles gambiae

“…In both mosquitoes and cockroaches, there is no correlation between the contraction rate of the antennal hearts and the dorsal vessel, but different from what we observed for the wing heart, the antennal hearts contract at a significantly slower rate than the dorsal vessel (Hertel et al, 1985;Boppana and Hillyer, 2014;Suggs et al, 2016). Furthermore, some cardioacceleratory peptides, such as CCAP, FMRFamides and proctolin, are known to modulate the contraction dynamics of both the dorsal vessel and the antennal hearts of insects (Cuthbert and Evans, 1989;Predel et al, 2004;Ejaz and Lange, 2008;Hertel et al, 2012;Estevez-Lao et al, 2013;Suggs et al, 2016). Whether these same factors also modulate the rhythmicity of the wing heart remains to be determined.…”

CCAP and FMRFamide-like peptides accelerate the contraction rate of the antennal accessory pulsatile organs (auxiliary hearts) of mosquitoes

“…The structure of the antennal APOs has been elucidated in multiple insect orders, but the most comprehensive studies have focused on cockroaches (order Blattodea). Furthermore, until the present study, the hormonal modulation of antennal APO contraction had only been studied in cockroaches and other polyneopterans (Hertel et al, 2012), with no studies focusing on the largest group of insects: the Endopterygota (Holometabola). Thus, we assessed whether the neurohormones CCAP, FMRFamide and SALDKNFMRFamide affect the physiology of the antennal APOs of mosquitoes (holometabolous insects in the order Diptera), and demonstrate that these three neuropeptides increase the contraction rate of these pulsatile organs in a manner that is similar to how they accelerate the heart.…”

“…Furthermore, we show that these neuropeptides also increase the velocity and maximum acceleration of hemolymph in the antennal space. In cockroaches, two types of neuropeptides are known to accelerate the antennal APO contraction rate: proctolin and three FLPs (Hertel et al, 1985(Hertel et al, , 2012Hertel and Penzlin, 1992;Lange et al, 1993;Predel et al, 2004). Proctolin stimulates the contraction of visceral, skeletal and cardiac muscle, and modulates digestion, egg laying, and both sexual and feeding behaviors (Konopinska and Rosinski, 1999;Isaac et al, 2004;Ejaz and Lange, 2008).…”

“…Although the structure of the antennal APOs has been elucidated in multiple insect species, less is known about endogenous factors that control their contraction. In cockroaches and some polyneopterans (lower Neoptera), the neuropeptide proctolin and three FMRFamide-like peptides (FLPs) accelerate the contraction rate of the antennal APOs, whereas the neuropeptide allatostatin and another FLP do not (Hertel et al, 1985(Hertel et al, , 2012Hertel and Penzlin, 1992;Lange et al, 1993;Predel et al, 2004). Whether these or other factors accelerate the contraction rate of the antennal APOs of nonpolyneopteran insects remains unknown; however, proctolin and certain FLPs are cardioacceleratory in diverse insect species (Cuthbert and Evans, 1989;Robb and Evans, 1990;Zornik et al, 1999;Sliwowska et al, 2001;Nichols, 2006;Ejaz and Lange, 2008;Hillyer et al, 2014).…”

Hemolymph circulation in insect sensory appendages: functional mechanics of antennal accessory pulsatile organs (auxiliary hearts) in the mosquitoAnopheles gambiae

“…This is primarily because the circulation of hemolymph through the antennae has been inferred from structural analyses and not from active visualizations of flow. Nevertheless, several studies in Blattodea and other Polyneoptera (lower Neoptera) have described the contractile and neurohemal activity of antennal hearts, illustrating the physiological complexity of these APOs (Hertel et al, 1985;Pass et al, 1988;Lange et al, 1993;Richter and Hertel, 1997;Predel, 2001;Hertel et al, 2012).The goal of the present study was to characterize the functional mechanics of antennal accessory pulsatile organs in the African malaria mosquito Anopheles gambiae Giles 1902 sensu stricto (Diptera: Culicidae: Anophelinae). The structure of antennal APOs has been described for the yellow fever mosquito, Aedes aegypti (Diptera: Culicidae: Culicinae), but physiological data on these organs are lacking (Clements, 1956;Sun and Schmidt, 1997).…”