Electrophysiological investigation of the antennal heart of Periplaneta americana and its reactions to proctolin

Hertel, Wieland; Pass, Günther; Penzlin, Heinz

doi:10.1016/0022-1910(85)90113-1

Cited by 43 publications

(25 citation statements)

References 27 publications

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“…This independence is reminiscent of the independence between the dorsal vessel and another type of accessory pulsatile organ: the antennal heart. 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).…”

Section: Discussioncontrasting

confidence: 50%

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

Chintapalli

Hillyer

2016

Journal of Experimental Biology

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The wings of insects are composed of membranes supported by interconnected veins. Within these veins are epithelial cells, nerves and tracheae, and their maintenance requires the flow of hemolymph. For this purpose, insects employ accessory pulsatile organs (auxiliary hearts) that circulate hemolymph throughout the wings. Here, we used correlative approaches to determine the functional mechanics of hemolymph circulation in the wings of the malaria mosquito Anopheles gambiae. Examination of sectioned tissues and intravital videos showed that the wing heart is located underneath the scutellum and is separate from the dorsal vessel. It is composed of a single pulsatile diaphragm (indicating that it is unpaired) that contracts at 3 Hz and circulates hemolymph throughout both wings. The wing heart contracts significantly faster than the dorsal vessel, and there is no correlation between the contractions of these two pulsatile organs. The wing heart functions by aspirating hemolymph out of the posterior wing veins, which forces hemolymph into the wings via anterior veins. By tracking the movement of fluorescent microspheres, we show that the flow diameter of the wing circulatory circuit is less than 1 µm, and we present a spatial map detailing the flow of hemolymph across all the wing veins, including the costa, sub-costa, ambient costa, radius, media, cubitus anterior, anal vein and crossveins. We also quantified the movement of hemolymph within the radius and within the ambient costa, and show that hemolymph velocity and maximum acceleration are higher when hemolymph is exiting the wing.

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Section: Discussioncontrasting

confidence: 50%

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

Chintapalli

Hillyer

2016

Journal of Experimental Biology

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“…However, the approach used in the present study diverged from that of previous studies, as we performed our analyses in intact insects, thus maintaining their normal hemocoel pressure and hemolymph components, whereas earlier studies were conducted on dissected specimens that had been immersed in buffer solutions. Furthermore, the basal antennal APO contraction rate of mosquitoes, at approximately 1 Hz, is twice the rate of the antennal APO of dissected cockroaches (Hertel et al, 1985). Crustacean cardioactive peptide is a cyclic amidated nonapeptide that is produced in a broad range of arthropods, including all sequenced insect lineages.…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

Section: Introductionmentioning

confidence: 99%

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

Suggs

Jones

Murphree

et al. 2016

Journal of Experimental Biology

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Insects rely on specialized accessory pulsatile organs (APOs), also known as auxiliary hearts, to propel hemolymph into their antennae. In most insects, this is accomplished via the pulsations of a pair of ampulla located in the head, each of which propels hemolymph across an antenna via an antennal vessel. Once at the distal end of the appendage, hemolymph returns to the head via the antennal hemocoel. Although the structure of the antennal hearts has been elucidated in various insect orders, their hormonal modulation has only been studied in cockroaches and other hemimetabolous insects within the superorder Polyneoptera, where proctolin and FMRFamide-like peptides accelerate the contraction rate of these auxiliary hearts. Here, we assessed the hormonal modulation of the antennal APOs of mosquitoes, a group of holometabolous (Endopterygota) insects within the order Diptera. We show that crustacean cardioactive peptide (CCAP), FMRFamide and SALDKNFMRFamide increase the contraction rate of the antennal APOs and the heart of Anopheles gambiae. Both antennal hearts are synchronously responsive to these neuropeptides, but their contractions are asynchronous with the contraction of the heart. Furthermore, we show that these neuropeptides increase the velocity and maximum acceleration of hemolymph within the antennal space, suggesting that each contraction is also more forceful. To our knowledge, this is the first report demonstrating that hormones of a holometabolous insect modulate the contraction dynamics of an auxiliary heart, and the first report that shows that the hormones of any insect accelerate the velocity of hemolymph in the antennal space.

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“…The amplitude of neurally evoked contractions is enhanced by pre-and/or postsynaptic action of the peptide (crustacean skeletal muscle: Schwarz et al, 1980;Bishop et al, 1984;Mercier and Wilkens, 1985;Pasztor and Golas, 1993;insect hyponeural, skeletal, andvisceral muscle: Cook andHolman, 1980, 1985;Evans, 1984;Hertel et al, 1985;Hertel and Penzlin, 1986;Baines et al, 1990;Bauer, 1991; Limulus heart and skeletal muscle: Benson et al, 1981;Watson et al, 1983;Rane et al, 1984;Watson and Hoshi, 1985).…”

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confidence: 99%

Effects of proctolin on contractions, membrane resistance, and non- voltage-dependent sarcolemmal ion channels in crustacean muscle fibers

1995

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The neuropeptide proctolin in nanomolar concentrations enhances the contraction of crustacean muscle fibers manyfold. The cellular mechanisms underlying this potentiation were investigated in single, isolated, fast-contracting abdominal extensor muscle fibers of a small crustacean, the marine isopod Idotea baltica. Force measurements and current-clamp experiments revealed two actions of proctolin on the muscle fibers. In half of the preparations, proctolin (10(-9)-10(-6) M) increased the fiber's input resistance by up to 25%. In about one- fourth of the preparations, proctolin induced all-or-none action potentials in response to depolarizing current pulses in muscle fibers that showed graded electric responses under control conditions. In both cases, proctolin potentiated the peak force of muscle contractions (between 1.5- and 18-fold for 5 x 10(-9) M proctolin). Proctolin affected neither the membrane resting potential nor the threshold for excitation-contraction coupling. Using cell-attached patches on the sarcolemmal membrane, we identified non-voltage-dependent ion channels which contribute to the passive membrane properties of the muscle fibers. A 53 +/- 6 pS channel had its reversal potential near rest and carried outward current at depolarized potentials with physiological saline in the recording pipette. With isotonic K+ saline in the patch pipette, the reversal potential was +85 +/- 12 mV depolarized from the resting potential and single-channel conductances ranged from 36 to 166 pS. Proctolin modulated the activity of all these putative K+ channels by reducing the number of functionally active channels. The effects of proctolin on force of contraction, input resistance, and single-channel activity were mimicked by a membrane-permeating analog of cAMP. Conversely, a monothio analog of cAMP (Rp-cAMPS), a blocker of protein kinase A activity, substantially decreased the membrane input resistance of the muscle fibers. The results suggest that activation of the cAMP signal pathway and phosphorylation of non-voltage-dependent K+ channels by protein kinase A are involved in the potentiation of contractions by proctolin in the muscle fibers of this crustacean.

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Electrophysiological investigation of the antennal heart of Periplaneta americana and its reactions to proctolin

Cited by 43 publications

References 27 publications

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

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

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

Effects of proctolin on contractions, membrane resistance, and non- voltage-dependent sarcolemmal ion channels in crustacean muscle fibers

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