scholarly journals Physiology, Development, and Disease Modeling in the Drosophila Excretory System

Genetics ◽  
2020 ◽  
Vol 214 (2) ◽  
pp. 235-264 ◽  
Author(s):  
Erez Cohen ◽  
Jessica K. Sawyer ◽  
Nora G. Peterson ◽  
Julian A. T. Dow ◽  
Donald T. Fox
Keyword(s):  
Human Disease ◽  
Fluid Transport ◽  
Disease Modeling ◽  
Malpighian Tubule ◽  
Malpighian Tubules ◽  
Excretory System ◽  
Anatomy And Physiology ◽  
Disease Biology ◽  
Organ Systems ◽  
And Function

The insect excretory system contains two organ systems acting in concert: the Malpighian tubules and the hindgut perform essential roles in excretion and ionic and osmotic homeostasis. For over 350 years, these two organs have fascinated biologists as a model of organ structure and function. As part of a recent surge in interest, research on the Malpighian tubules and hindgut of Drosophila have uncovered important paradigms of organ physiology and development. Further, many human disease processes can be modeled in these organs. Here, focusing on discoveries in the past 10 years, we provide an overview of the anatomy and physiology of the Drosophila excretory system. We describe the major developmental events that build these organs during embryogenesis, remodel them during metamorphosis, and repair them following injury. Finally, we highlight the use of the Malpighian tubules and hindgut as accessible models of human disease biology. The Malpighian tubule is a particularly excellent model to study rapid fluid transport, neuroendocrine control of renal function, and modeling of numerous human renal conditions such as kidney stones, while the hindgut provides an outstanding model for processes such as the role of cell chirality in development, nonstem cell–based injury repair, cancer-promoting processes, and communication between the intestine and nervous system.

NHE8 mediates amiloride-sensitive Na+/H+exchange across mosquito Malpighian tubules and catalyzes Na+and K+transport in reconstituted proteoliposomes

2007 ◽  
Vol 292 (5) ◽  
pp. F1501-F1512 ◽  
Author(s):  
Wanyoike Kang'ethe ◽  
Karlygash G. Aimanova ◽  
Ashok K. Pullikuth ◽  
Sarjeet S. Gill
Keyword(s):  
Fluid Transport ◽  
Ion Homeostasis ◽  
Malpighian Tubule ◽  
Malpighian Tubules ◽  
Yeast Cells ◽  
Kinetic Properties ◽  
Sodium Load ◽  
Electrophysiological Studies ◽  
Reconstituted Membranes ◽  
Apical Membranes

Following a blood meal, the mosquito Aedes aegypti will have acquired an enormous sodium load that must be rapidly excreted to restore ion homeostasis. It is a process that demands robust sodium and fluid transport capabilities. Even though the identities of the components involved in this ion transport across the mosquito Malpighian tubule epithelia have not been completely determined, electrophysiological studies suggest the contribution of a Na+/H+exchanger extruding cations into the lumen driven secondarily by the proton gradient created by the V-type H+-ATPase in the tubules' apical membrane. We have identified the putative exchanger and designated it AeNHE8. Immunolocalization studies demonstrated that AeNHE8 is expressed in the apical membranes of Malpighian tubules, gastric caecae, and rectum. When heterologously expressed in salt-sensitive yeast cells lacking Na+extrusion and Na+/H+exchange proteins, AeNHE8 rescues the salt-sensitive phenotype and restores the cells' ability to grow in high NaCl media. Furthermore, heterologous expression of AeNHE8 in NHE-deficient fibroblast cells results in an amiloride-sensitive22Na+uptake. To determine the exchanger's kinetic properties, we reconstituted membranes from yeast cells expressing the protein into lipid proteoliposomes and assayed for cation-dependent H+exchange by fluorimetric methods. Our results indicate that AeNHE8 mediates saturable exchange of Na+and K+for H+. We propose that AeNHE8 may be coupled to the inward H+gradient across the Malpighian tubules and plays a role in the extrusion of excess sodium and potassium while maintaining steady intracellular pH in the principal cells.

scholarly journals A comparison of the effects of two putative diuretic hormones from Locusta migratoria on isolated locust malpighian tubules

1993 ◽  
Vol 175 (1) ◽  
pp. 1-14 ◽  
Author(s):  
G. M. Coast ◽  
R. C. Rayne ◽  
T. K. Hayes ◽  
A. I. Mallet ◽  
K. S. Thompson ◽  
...  
Keyword(s):  
Cyclic Amp ◽  
Arginine Vasopressin ◽  
Locusta Migratoria ◽  
Malpighian Tubule ◽  
Fluid Secretion ◽  
Enzymatic Digestion ◽  
Malpighian Tubules ◽  
Suboesophageal Ganglion ◽  
Anatomy And Physiology ◽  
Strong Stimulation

Previous work has shown that a peptide related to arginine vasopressin is present in the suboesophageal ganglion of the locust, Locusta migratoria. This peptide was determined to be an anti-parallel dimer of the nonapeptide Cys-Leu-Ile-Thr-Asn-Cys-Pro-Arg-Gly-NH2 and was reported to stimulate cyclic AMP production and fluid secretion in a combined Malpighian tubules and midgut preparation from locusts. For these reasons the peptide has been called the arginine-vasopressin-like insect diuretic hormone (AVP-like IDH). Recently, a second diuretic peptide (Locusta-DP), which is related to corticotropin releasing factor, has been identified: this is a potent stimulant of fluid secretion and cyclic AMP production by isolated locust tubules. Because water balance in insects is likely to be controlled by a cocktail of hormones acting on both Malpighian tubules and hindgut, this study directly compares the activity of these two peptides in fluid secretion and cyclic AMP production bioassays on one target organ, the isolated Malpighian tubule of Locusta migratoria. Locusta-DP was synthesised directly, whereas the dimeric AVP-like IDH was obtained by oxidation of a synthetic nonapeptide monomer. Products were separated by RP-HPLC and their structures unequivocally confirmed by enzymatic digestion, sequence analysis and electrospray mass spectrometry. We show that Locusta-DP causes strong stimulation of fluid secretion and cyclic AMP production, whereas the AVP-like IDH has no effect in either assay. These findings are discussed in the light of recent work on the anatomy and physiology of the vasopressin-like immunoreactive (VPLI) neurones in the suboesophageal ganglion of Locusta migratoria, the proposed source of the AVP-like peptide.

Stimulation of sodium transport and fluid secretion by ouabain in an insect malpighian tubule

1988 ◽  
Vol 137 (1) ◽  
pp. 265-276 ◽  
Author(s):  
S. H. Maddrell ◽  
J. A. Overton
Keyword(s):  
Fluid Flow ◽  
Sodium Transport ◽  
Fluid Transport ◽  
Electrical Potential ◽  
Malpighian Tubule ◽  
Fluid Secretion ◽  
Malpighian Tubules ◽  
Sodium Ions ◽  
Tubule Cells ◽  
Stimulation Of

Ouabain, at all concentrations higher than 2 × 10(−7) mol l-1, stimulates the rate at which the Malpighian tubules of the insect, Rhodnius, transport sodium ions and fluid into the lumen. An effect on paracellular movement of sodium ions is unlikely because ouabain makes the electrical potential of the lumen more positive, which would slow diffusion of sodium into the lumen. Radioactive ouabain binds to the haemolymph-facing sides of the tubule cells but not to the luminal face. This binding is reduced in the presence of elevated levels of potassium or of non-radioactive ouabain. Bound ouabain is only slowly released on washing in ouabain-free saline. The evidence suggests that there is a Na+/K+-ATPase on the outer (serosal) membranes of the tubules. Such a pump would transport sodium in a direction opposed to the flow of ions and water involved in fluid transport; poisoning it with ouabain would remove this brake, and fluid flow and sodium transport would increase, as observed.

Ultrastructural organization of the basal lamina in insect Malpighian tubules

1984 ◽  
Vol 42 ◽  
pp. 314-315
Author(s):  
J.S. Ryerse
Keyword(s):  
Basal Lamina ◽  
Insect Cells ◽  
Malpighian Tubule ◽  
Body Cavity ◽  
Malpighian Tubules ◽  
Ultrastructural Organization ◽  
En Bloc ◽  
Tubule Cells ◽  
Yellow Region ◽  
And Function

Relatively little is known about the structure or function of the basal lamina in insect cells. I report here the ultrastructural organization of the basal lamina in Malpighian tubule yellow region primary cells of larval stage skipper butterflies (Calpodes ethlius). The Malpighian tubules selectively filter the blood and produce a primary urine which flows down the tubule lumen into the alimentary canal for excretion. The basal lamina provides the only barrier between the Malpighian tubule cells and the blood which freely circulates within the open body cavity and it may therefore regulate which molecules and ions gain access to the tubule cells. As a first step in these studies on the structure, composition and function of the basal lamina in insect cells the ultrastructure of the basal lamina in Calpodes Malpighian tubules after conventional TEM tissue processing and poststaining has been compared with that observed following en bloc staining with a variety of electron dense stains and probes with specificity for basal lamina components.

Metamorphosis of the perirectal Malpighian tubules in the mealworm Tenebrio molitor L. (Coleoptera, Tenebrionidae). II. Ultrastructure and role of autophagic vacuoles

1971 ◽  
Vol 49 (8) ◽  
pp. 1185-1191 ◽  
Author(s):  
J. R. Byers
Keyword(s):  
Brush Border ◽  
Fluid Transport ◽  
Membrane Lipid ◽  
Structure And Function ◽  
Malpighian Tubules ◽  
Autophagic Vacuoles ◽  
Tubule Cells ◽  
And Function ◽  
Coleoptera Tenebrionidae

The perirectal Malpighian tubules of T. molitor are highly specialized for ion and fluid transport. Although they survive metamorphosis, being similar in structure and function in both larva and adult, they undergo a sequence of dramatic alterations in subcellular organization. In the early stages of metamorphosis there is a phase of dedifferentiation during which the perirectal tubule cells undergo degenerative changes. The highly specialized brush border, which in the larva is formed of closely packed microvilli containing mitochondria, is partially broken down and a large number of mitochondria undergo autophagic isolation and digestion. A conspicuous result of the autophagic processes is the accumulation of membrane lipid within autophagic vacuoles which are eventually transformed into 'osmiophilic bodies.' During the later stages of metamorphosis the cells progressively redifferentiate and the brush border is reconstituted. The number of osmiophilic bodies declines markedly, concomitant with an apparent increase in the number of mitochondria.

scholarly journals Functional Plasticity of the gut and the Malpighian tubules underlies cold acclimation and mitigates cold-induced hyperkalemia in Drosophila melanogaster

2017 ◽  
Author(s):  
Gil Y. Yerushalmi ◽  
Lidiya Misyura ◽  
Heath A. MacMillan ◽  
Andrew Donini
Keyword(s):  
Water Balance ◽  
Cold Acclimation ◽  
Low Temperatures ◽  
Fluid Transport ◽  
Epithelial Transport ◽  
Ion Homeostasis ◽  
Malpighian Tubule ◽  
Adult Emergence ◽  
Fluid Secretion ◽  
Malpighian Tubules

AbstractAt low temperatures, Drosophila, like most insects, lose the ability to regulate ion and water balance across the gut epithelia, which can lead to a lethal increase of [K+] in the hemolymph (hyperkalemia). Cold-acclimation, the physiological response to low temperature exposure, can mitigate or entirely prevent these ion imbalances, but the physiological mechanisms that facilitate this process are not well understood. Here, we test whether plasticity in the ionoregulatory physiology of the gut and Malpighian tubules of Drosophila may aid in preserving ion homeostasis in the cold. Upon adult emergence, D. melanogaster females were subjected to seven days at warm (25°C) or cold (10°C) acclimation conditions. The cold acclimated flies had a lower critical thermal minimum (CTmin), recovered from chill coma more quickly, and better maintained hemolymph K+ balance in the cold. The improvements in chill tolerance coincided with increased Malpighian tubule fluid secretion and better maintenance of K+ secretion rates in the cold, as well as reduced rectal K+ reabsorption in cold-acclimated flies. To test whether modulation of ion-motive ATPases, the main drivers of epithelial transport in the alimentary canal, mediate these changes, we measured the activities of Na+-K+-ATPase and V-type H+-ATPase at the Malpighian tubules, midgut, and hindgut. Na+/K+-ATPase and V-type H+-ATPase activities were lower in the midgut and the Malpighian tubules of cold-acclimated flies, but unchanged in the hindgut of cold acclimated flies, and were not predictive of the observed alterations in K+ transport. Our results suggest that modification of Malpighian tubule and gut ion and water transport likely prevents cold-induced hyperkalemia in cold-acclimated flies and that this process is not directly related to the activities of the main drivers of ion transport in these organs, Na+/K+- and V-type H+-ATPases.Summary StatementAt low temperatures, insects lose the ability to regulate ion and water balance and can experience a lethal increase in hemolymph [K+]. Previous exposure to low temperatures can mitigate this effect and improve chill tolerance. Here, we show that plasticity of ion and fluid transport across the Malpighian tubule and rectal epithelia likely drive this response.

Fine Structure of the Malpighian Tubules of the Mosquito, Culex pipiens

1971 ◽  
Vol 29 ◽  
pp. 402-403
Author(s):  
Brendan Clifford
Keyword(s):  
Fine Structure ◽  
Culex Pipiens ◽  
Stellate Cell ◽  
Malpighian Tubule ◽  
Cell Types ◽  
Instar Larva ◽  
Malpighian Tubules ◽  
Calliphora Erythrocephala ◽  
Distinct Cell ◽  
Basal Plasma

An ultrastructural investigation of the Malpighian tubules of the fourth instar larva of Culex pipiens was undertaken as part of a continuing study of the fine structure of transport epithelia.Each of the five Malpighian tubules was found to be morphologically identical and regionally undifferentiated. Two distinct cell types, the primary and stellate, were found intermingled along the length of each tubule. The ultrastructure of the stellate cell was previously described in the Malpighian tubule of the blowfly, Calliphora erythrocephala by Berridge and Oschman.The basal plasma membrane of the primary cell is extremely irregular, giving rise to a complex interconnecting network of basal channels. The compartments of cytoplasm entrapped within this system of basal infoldings contain mitochondria, free ribosomes, and small amounts of rough endoplasmic reticulum. The mitochondria are distinctive in that the cristae run parallel to the long axis of the organelle.

A Study of the Malpighian Tubules of the Pill Millipede, Glomeris marginata (Villers)

1974 ◽  
Vol 60 (1) ◽  
pp. 41-51
Author(s):  
PATRICIA ANNE FARQUHARSON
Keyword(s):  
Size Distribution ◽  
Fluid Transport ◽  
Molecular Size ◽  
Malpighian Tubules ◽  
Inverse Relation ◽  
Fluid Production ◽  
Molecular Size Distribution ◽  
Molecular Sieving ◽  
Tubule Fluid ◽  
Tubule Wall

1. Tubule fluid:medium ratios (TF/M) have been measured for inulin, glucose, LMWD and HMWD. These TF/M ratios were surprisingly high. 2. The tubule appears to act as a molecular filter; that is to say, molecules move through the tubule wall in inverse relation to their size. This is best illustrated using polyvinyl pyrrolidone as a tracer. The molecular size distribution of PVP fractions present in tubule fluid differs markedly from the molecular size distribution of PVP in the bathing Ringer. 3. No correlation can be made between the inulin and glucose TF/M and the rate of fluid production. However, the inverse relationship between TF/M and rate of fluid production for dextrans indicates a molecular sieving effect. 4. The significance of these results is discussed with reference to models of fluid transport.

THE EFFECTS OF MANDUCA SEXTA DIURETIC HORMONE ON FLUID TRANSPORT BY THE MALPIGHIAN TUBULES AND CRYPTONEPHRIC COMPLEX OF MANDUCA SEXTA

1993 ◽  
Vol 178 (1) ◽  
pp. 231-243 ◽  
Author(s):  
N. Audsley ◽  
G. M. Coast ◽  
D. A. Schooley
Keyword(s):  
Cyclic Amp ◽  
Manduca Sexta ◽  
Fluid Transport ◽  
Basal Membrane ◽  
Fluid Secretion ◽  
Hormonal Control ◽  
Malpighian Tubules ◽  
Proximal Tubules ◽  
Fluid Absorption ◽  
Diuretic Hormone

1. Manduca sexta diuretic hormone (Mas-DH) stimulates fluid secretion by adult Malpighian tubules of M. sexta, demonstrating its site of diuretic action in M. sexta for the first time. It was not possible to develop a suitable bioassay to measure fluid secretion in larval proximal tubules. 2. Mas-DH has an antidiuretic action on the cryptonephric complex of larval M. sexta because it increases fluid absorption from the rectum. It appears that in this complex Mas-DH is acting on a Na+/K+/2Cl- co-transporter, presumably on the basal membrane of the cryptonephric Malpighian tubules, because Mas-DH-stimulated fluid absorption by the cryptonephric complex is inhibited by bumetanide or the removal of Cl-, Na+ or K+ from the haemolymph side of the tissue. This is the first demonstration of hormonal control of fluid absorption by the cryptonephric complex. 3. Concomitant with the stimulation of fluid transport, Mas-DH increases the amount of cyclic AMP secreted by adult Malpighian tubules and the cryptonephric complex. In addition, Mas-DH promotes cyclic AMP production by the larval proximal tubules.

Anti-diuresis in the blood-feeding insect Rhodnius prolixus Stål: the peptide CAP2b and cyclic GMP inhibit Malpighian tubule fluid secretion.

1997 ◽  
Vol 200 (17) ◽  
pp. 2363-2367 ◽  
Author(s):  
M C Quinlan ◽  
N J Tublitz ◽  
M J O'Donnell
Keyword(s):  
Cyclic Gmp ◽  
Physiological Role ◽  
Malpighian Tubule ◽  
Fluid Secretion ◽  
Blood Feeding ◽  
Rhodnius Prolixus ◽  
Malpighian Tubules ◽  
Tubule Fluid ◽  
Secretion Rates

Rhodnius prolixus eliminates NaCl-rich urine at high rates following its infrequent but massive blood meals. This diuresis involves stimulation of Malpighian tubule fluid secretion by diuretic hormones released in response to distention of the abdomen during feeding. The precipitous decline in urine flow that occurs several hours after feeding has been thought until now to result from a decline in diuretic hormone release. We suggest here that insect cardioacceleratory peptide 2b (CAP2b) and cyclic GMP are part of a novel mechanism of anti-diuresis. Secretion rates of 5-hydroxytryptamine-stimulated Malpighian tubules are reduced by low doses of CAP2b or cyclic GMP. Maximal secretion rates are restored by exposing tubules to 1 mmol l-1 cyclic AMP. Levels of cyclic GMP in isolated tubules increase in response to CAP2b, consistent with a role for cyclic GMP as an intracellular second messenger. Levels of cyclic GMP in tubules also increase as urine output rates decline in vivo, suggesting a physiological role for this nucleotide in the termination of diuresis.

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