Non-traditional Models: The Molecular Physiology of Sodium and Water Transport in Mosquito Malpighian Tubules

Piermarini, Peter M.; Gillen, Christopher M.

doi:10.1007/978-1-4939-3213-9_13

Cited by 4 publications

(3 citation statements)

References 77 publications

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“…The morphology and physiology of mosquito Malpighian tubules have been the focus of recent comprehensive reviews [ 8 , 9 , 10 ]. In brief, the five Malpighian tubules together with the hindgut (i.e., ileum and rectum) form the renal excretory system of mosquitoes ( Figure 1 A).…”

Section: Mosquito Malpighian Tubulesmentioning

confidence: 99%

Malpighian Tubules as Novel Targets for Mosquito Control

Piermarini

Esquivel

Denton

2017

IJERPH

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The Malpighian tubules and hindgut are the renal excretory tissues of mosquitoes; they are essential to maintaining hemolymph water and solute homeostasis. Moreover, they make important contributions to detoxifying metabolic wastes and xenobiotics in the hemolymph. We have focused on elucidating the molecular mechanisms of Malpighian tubule function in adult female mosquitoes and developing chemical tools as prototypes for next-generation mosquitocides that would act via a novel mechanism of action (i.e., renal failure). To date, we have targeted inward rectifier potassium (Kir) channels expressed in the Malpighian tubules of the yellow fever mosquito Aedes aegypti and malaria mosquito Anopheles gambiae. Inhibition of these channels with small molecules inhibits transepithelial K+ and fluid secretion in Malpighian tubules, leading to a disruption of hemolymph K+ and fluid homeostasis in adult female mosquitoes. In addition, we have used next-generation sequencing to characterize the transcriptome of Malpighian tubules in the Asian tiger mosquito Aedes albopictus, before and after blood meals, to reveal new molecular targets for potentially disrupting Malpighian tubule function. Within 24 h after a blood meal, the Malpighian tubules enhance the mRNA expression of genes encoding mechanisms involved with the detoxification of metabolic wastes produced during blood digestion (e.g., heme, NH3, reactive oxygen species). The development of chemical tools targeting these molecular mechanisms in Malpighian tubules may offer a promising avenue for the development of mosquitocides that are highly-selective against hematophagous females, which are the only life stage that transmits pathogens.

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Section: Mosquito Malpighian Tubulesmentioning

confidence: 99%

Malpighian Tubules as Novel Targets for Mosquito Control

Piermarini

Esquivel

Denton

2017

IJERPH

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“…Over the past 30 years, numerous physiological and molecular studies on mosquito Malpighian tubules have uncovered a variety of mechanisms that regulate and mediate the post-prandial diuresis (e.g., ion transporters, neuroendocrine factors) ( Beyenbach, 2003 ; Beyenbach, 2012 ; Beyenbach & Piermarini, 2011 ; Coast, 2009 ; Piermarini & Gillen, 2015 ). However, our understanding of how mosquito Malpighian tubules contribute to osmotic balance and blood meal processing after the post-prandial diuresis is limited.…”

Section: Introductionmentioning

confidence: 99%

Ade novotranscriptome of the Malpighian tubules in non-blood-fed and blood-fed Asian tiger mosquitoesAedes albopictus: insights into diuresis, detoxification, and blood meal processing

Esquivel

Cassone

Piermarini

2016

PeerJ

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Background. In adult female mosquitoes, the renal (Malpighian) tubules play an important role in the post-prandial diuresis, which removes excess ions and water from the hemolymph of mosquitoes following a blood meal. After the post-prandial diuresis, the roles that Malpighian tubules play in the processing of blood meals are not well described.Methods. We used a combination of next-generation sequencing (paired-end RNA sequencing) and physiological/biochemical assays in adult female Asian tiger mosquitoes (Aedes albopictus) to generate molecular and functional insights into the Malpighian tubules and how they may contribute to blood meal processing (3–24 h after blood ingestion).Results/Discussion. Using RNA sequencing, we sequenced and assembled the first de novo transcriptome of Malpighian tubules from non-blood-fed (NBF) and blood-fed (BF) mosquitoes. We identified a total of 8,232 non-redundant transcripts. The Malpighian tubules of NBF mosquitoes were characterized by the expression of transcripts associated with active transepithelial fluid secretion/diuresis (e.g., ion transporters, water channels, V-type H+-ATPase subunits), xenobiotic detoxification (e.g., cytochrome P450 monoxygenases, glutathione S-transferases, ATP-binding cassette transporters), and purine metabolism (e.g., xanthine dehydrogenase). We also detected the expression of transcripts encoding sodium calcium exchangers, G protein coupled-receptors, and septate junctional proteins not previously described in mosquito Malpighian tubules. Within 24 h after a blood meal, transcripts associated with active transepithelial fluid secretion/diuresis exhibited a general downregulation, whereas those associated with xenobiotic detoxification and purine catabolism exhibited a general upregulation, suggesting a reinvestment of the Malpighian tubules’ molecular resources from diuresis to detoxification. Physiological and biochemical assays were conducted in mosquitoes and isolated Malpighian tubules, respectively, to confirm that the transcriptomic changes were associated with functional consequences. In particular, in vivo diuresis assays demonstrated that adult female mosquitoes have a reduced diuretic capacity within 24 h after a blood meal. Moreover, biochemical assays in isolated Malpighian tubules showed an increase in glutathione S-transferase activity and the accumulation of uric acid (an end product of purine catabolism) within 24 h after a blood meal. Our data provide new insights into the molecular physiology of Malpighian tubules in culicine mosquitoes and reveal potentially important molecular targets for the development of chemical and/or gene-silencing insecticides that would disrupt renal function in mosquitoes.

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“…Malpighian tubules (MTs) are typical arthropod organs, specialized in the osmoregulation and excretion of protein-derived and xenobiotic wastes [ 1 , 2 ]. The MTs are composed of only two types of cells that collaborate in ion exchange regulation: principal cells primarily regulating potassium fluxes and stellate cells specialized in chloride transport to maintain the electrolyte and water balance [ 3 ]. Maintaining a simple histological organization, principal and stellate cells further differentiate along the segments of the MTs [ 4 ], while different insect species vary significantly in the number, shape and specialized MT functions that encompass a wide range of roles, including bioluminescence, the processing of proteinaceous products and inorganic salts for adhesive or protective purposes and participation in the immune response [ 1 , 5 ].…”

Section: Introductionmentioning

confidence: 99%

Developmental and Nutritional Dynamics of Malpighian Tubule Autofluorescence in the Asian Tiger Mosquito Aedes albopictus

Croce,

Garbelli,

Moyano

et al. 2023

IJMS

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Malpighian tubules (MTs) are arthropod excretory organs crucial for the osmoregulation, detoxification and excretion of xenobiotics and metabolic wastes, which include tryptophan degradation products along the kynurenine (KYN) pathway. Specifically, the toxic intermediate 3-hydroxy kynurenine (3-HK) is metabolized through transamination to xanthurenic acid or in the synthesis of ommochrome pigments. Early investigations in Drosophila larval fat bodies revealed an intracellular autofluorescence (AF) that depended on tryptophan administration. Subsequent observations documented AF changes in the MTs of Drosophila eye-color mutants genetically affecting the conversion of tryptophan to KYN or 3-HK and the intracellular availability of zinc ions. In the present study, the AF properties of the MTs in the Asian tiger mosquito, Aedes albopictus, were characterized in different stages of the insect’s life cycle, tryptophan-administered larvae and blood-fed adult females. Confocal imaging and microspectroscopy showed AF changes in the distribution of intracellular, brilliant granules and in the emission spectral shape and amplitude between the proximal and distal segments of MTs across the different samples. The findings suggest AF can serve as a promising marker for investigating the functional status of MTs in response to metabolic alterations, contributing to the use of MTs as a potential research model in biomedicine.

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Non-traditional Models: The Molecular Physiology of Sodium and Water Transport in Mosquito Malpighian Tubules

Cited by 4 publications

References 77 publications

Malpighian Tubules as Novel Targets for Mosquito Control

Malpighian Tubules as Novel Targets for Mosquito Control

Ade novotranscriptome of the Malpighian tubules in non-blood-fed and blood-fed Asian tiger mosquitoesAedes albopictus: insights into diuresis, detoxification, and blood meal processing

Developmental and Nutritional Dynamics of Malpighian Tubule Autofluorescence in the Asian Tiger Mosquito Aedes albopictus

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