Novel mechanisms of epithelial ion transport: insights from the cryptonephridial system of lepidopteran larvae

Kapoor, Damandeep; Khan, Aliyyah; O’Donnell, Michael J.; Kolosov, Dennis

doi:10.1016/j.cois.2021.04.001

Cited by 8 publications

(7 citation statements)

References 70 publications

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“…Because gut luminal alkalinity is established by an excess of potassium ions [10] and there is a correlation between gut alkalinity and larval growth [9], maintenance of high potassium ion concentration in the midgut is possibly involved in the acceleration of humus degradation, which is partly associated with the compost-mediated growth improvement of female larvae. The gut epithelium and Malpighian tubules regulate potassium ion concentration through transepithelial transport from the hemolymph to the gut lumen and vise versa [31][32][33]. The effects of compost on the function of potassium ion transport in the gut epithelium and Malpighian tubules remain to be elucidated.…”

Section: Discussionmentioning

confidence: 99%

A Thermophile-Fermented Compost Modulates Intestinal Cations and the Expression of a Juvenile Hormone-Binding Protein Gene in the Female Larvae of Hercules Beetle Dynastes hercules (Coleoptera: Scarabaeidae)

Asano,

Miyahara,

Miyamoto

et al. 2023

Insects

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The Hercules beetle larvae grow by feeding on humus, and adding a thermophile-fermented compost to the humus can upregulate the growth of female larvae. In this study, the effects of compost on the intestinal environment, including pH, cation concentrations, and organic acid concentrations of intestinal fluids, were investigated, and the RNA profile of the fat body was determined. Although the total intestinal potassium ions were similar between the larvae grown without compost (control larvae) and those with compost (compost larvae), the proportion of potassium ions in the midgut of the compost larvae drastically increased. In the midgut, an unidentified organic acid was the most abundant, and its concentration increased in the compost larvae. Transcriptome analysis showed that a gene encoding hemolymph juvenile-binding protein (JHBP) was expressed in the compost female larvae and not in the control female larvae. Expression of many genes involved in the defensive system was decreased in the compost female larvae. These results suggest that the female-specific enhancement of larval growth by compost was associated with the increased JHBP expression under conditions in which the availability of nutrition from the humus was improved by an increase in potassium ions in the midgut.

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Section: Discussionmentioning

confidence: 99%

A Thermophile-Fermented Compost Modulates Intestinal Cations and the Expression of a Juvenile Hormone-Binding Protein Gene in the Female Larvae of Hercules Beetle Dynastes hercules (Coleoptera: Scarabaeidae)

Asano,

Miyahara,

Miyamoto

et al. 2023

Insects

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“…Transcriptomic studies on osmoregulatory epithelia of lepidopterans and dipterans uncovered the presence of many more VGICs (e.g., H V , Cl V , BK, KCNA, KCNC, KCNS, TRP M, TRP V channels), expression of which has not been confirmed using direct molecular, protein-based, or pharmacological approaches to date ( 26 , 58 , 65 , 89 , 94 ). Whether these VGICs play a role in the regulation of ion transport in insect epithelia remains unexplored.…”

Section: Select Unstudied Vgics Detected In Osmoregulatory Epithelia ...mentioning

confidence: 99%

“…Interestingly, expression of many Ca V , K V , Na V , and non-selective cation permeable VGICs has been reported specifically in epithelia of animals ranging from early divergent Placozoans to vertebrates (e.g., 26 ) (See Table 1 ). The genesis of the study of how VGICs regulate ion transport in insect epithelia traces itself to a recent collection of studies that investigate the topic in the Malpighian tubules (MTs) of lepidopterans.…”

Section: Introductionmentioning

confidence: 99%

Voltage-gated ion channels as novel regulators of epithelial ion transport in the osmoregulatory organs of insects

Dates,

Kolosov

2024

Front. Insect Sci.

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Voltage-gated ion channels (VGICs) respond to changes in membrane potential (Vm) and typically exhibit fast kinetic properties. They play an important role in signal detection and propagation in excitable tissues. In contrast, the role of VGICs in non-excitable tissues like epithelia is less studied and less clear. Studies in epithelia of vertebrates and invertebrates demonstrate wide expression of VGICs in epithelia of animals. Recently, VGICs have emerged as regulators of ion transport in the Malpighian tubules (MTs) and other osmoregulatory organs of insects. This mini-review aims to concisely summarize which VGICs have been implicated in the regulation of ion transport in the osmoregulatory epithelia of insects to date, and highlight select groups for further study. We have also speculated on the roles VGICs may potentially play in regulating processes connected directly to ion transport in insects (e.g., acid-base balance, desiccation, thermal tolerance). This review is not meant to be exhaustive but should rather serve as a thought-provoking collection of select existing highlights on VGICs, and to emphasize how understudied this mechanism of ion transport regulation is in insect epithelia.

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“…Voltage-gated, ligand-gated and mechanosensitive ion channels have been detected in epithelia of several vertebrates and invertebrates using publicly available RNAseq datasets (Kapoor et al, 2021). Studies on vertebrate (and most often mammalian) epithelia have reported expression of voltage-gated ion channels in epithelia of the lung, intestine (Barshack et al, 2008), kidney (Siroky et al, 2017) and skin (Pitt et al, 2021).…”

Section: Functions Of Voltage-gated Ligand-gated and Mechanosensitive...mentioning

confidence: 99%

Blending physiology and RNAseq to provide new insights into regulation of epithelial transport: switching between ion secretion and reabsorption

Kolosov

O’Donnell

2022

Journal of Experimental Biology

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This Review addresses the means by which epithelia change the direction of vectorial ion transport. Recent studies have revealed that insect Malpighian (renal) tubules can switch from secreting to reabsorbing K+. When the gut of larval lepidopterans is empty (during the moult cycle) or when the larvae are reared on K+-deficient diet, the distal ileac plexus segment of the tubule secretes K+ from the haemolymph into the tubule lumen. By contrast, in larvae reared on K+-rich diet, ions and fluid are reabsorbed from the rectal lumen into the perinephric space surrounding the cryptonephridial tubules of the rectal complex. Ions and fluid are then transported from the perinephric space into the lumen of the cryptonephridial tubules, thus supplying the free segments of the tubule downstream. Under these conditions, some of the K+ and water in the tubule lumen is reabsorbed across the cells of the distal ileac plexus, allowing for expansion of haemolymph volume in the rapidly growing larvae, as well as recycling of K+ and base equivalents. RNA sequencing data reveal large-scale changes in gene transcription that are associated with the switch between ion secretion and ion reabsorption by the distal ileac plexus. An unexpected finding is the presence of voltage-gated, ligand-gated and mechanosensitive ion channels, normally seen in excitable cells, in Malpighian tubules. Transcriptomic surveys indicate that these types of channels are also present in multiple other types of vertebrate and invertebrate epithelia, suggesting that they may play novel roles in epithelial cell signalling and regulation of epithelial ion transport.

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Novel mechanisms of epithelial ion transport: insights from the cryptonephridial system of lepidopteran larvae

Cited by 8 publications

References 70 publications

A Thermophile-Fermented Compost Modulates Intestinal Cations and the Expression of a Juvenile Hormone-Binding Protein Gene in the Female Larvae of Hercules Beetle Dynastes hercules (Coleoptera: Scarabaeidae)

A Thermophile-Fermented Compost Modulates Intestinal Cations and the Expression of a Juvenile Hormone-Binding Protein Gene in the Female Larvae of Hercules Beetle Dynastes hercules (Coleoptera: Scarabaeidae)

Voltage-gated ion channels as novel regulators of epithelial ion transport in the osmoregulatory organs of insects

Blending physiology and RNAseq to provide new insights into regulation of epithelial transport: switching between ion secretion and reabsorption

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