scholarly journals Neurochemical fine tuning of a peripheral tissue: peptidergic and aminergic regulation of fluid secretion by Malpighian tubules in the tobacco hawkmoth M. sexta

2002 ◽  
Vol 205 (13) ◽  
pp. 1869-1880 ◽  
Author(s):  
N. J. V. Skaer ◽  
D. R. Nässel ◽  
S. H. P. Maddrell ◽  
N. J. Tublitz
Keyword(s):  
Extracellular Fluid ◽  
Malpighian Tubule ◽  
Fluid Secretion ◽  
The Body ◽  
Malpighian Tubules ◽  
Adult Brain ◽  
Fine Tuning ◽  
Small Subset ◽  
Larval Brain ◽  
Pharate Adult

SUMMARY The actions of various peptides and other compounds on fluid secretion by Malpighian tubules in the tobacco hawkmoth Manduca sexta sexta are investigated in this study. Using a newly developed pharate adult Malpighian tubule bioassay, we show that three tachykinin-related peptides (TRPs),leucokinin I, serotonin (5-HT), octopamine, the cardioacceleratory peptides 1a, 1b and 2c, cGMP and cAMP each cause an increase in the rate of fluid secretion in pharate adult tubules. Whereas the possible hormonal sources of biogenic amines and some of the peptides are known, the distribution of TRPs has not been investigated previously in M. sexta. Thus we performed immunocytochemistry using an anti-TRP antiserum. We show the presence of TRP-like material in a small subset of cells in the M. sexta central nervous system (CNS). The larval brain contains approximately 60 TRP-immunopositive cells and there are approximately 100 such cells in the adult brain including the optic lobes. Every ganglion of the ventral nerve cord also contains TRP-like immunoreactive cells. No TRP-containing neurosecretory cells were seen in the CNS, but endocrine cells of the midgut reacted with the antiserum. We propose the hypothesis that the control in insects of physiological systems by hormones may not always involve tissue-specific hormones that force stereotypical responses in their target systems. Instead, there may exist in the extracellular fluid a continuous broadcast of information in the form of a chemical language to which some or all parts of the body continuously respond on a moment-to-moment basis, and which ensures a more effective and efficient coordination of function than could be achieved otherwise.

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.

Intracellular ion activities in Malpighian tubule cells ofRhodnius prolixus: evaluation of Na+-K+-2Cl-cotransport across the basolateral membrane

2002 ◽  
Vol 205 (11) ◽  
pp. 1645-1655 ◽  
Author(s):  
Juan P. Ianowski ◽  
Robert J. Christensen ◽  
Michael J. O'Donnell
Keyword(s):  
Basolateral Membrane ◽  
Malpighian Tubule ◽  
Fluid Secretion ◽  
Rhodnius Prolixus ◽  
Passive Movement ◽  
Malpighian Tubules ◽  
Intracellular Ion Activities ◽  
Ion Activities ◽  
Tubule Cells ◽  
Electrochemical Potentials

SUMMARYIntracellular ion activities (aion) and basolateral membrane potential (Vbl) were measured in Malpighian tubule cells of Rhodnius prolixus using double-barrelled ion-selective microelectrodes. In saline containing 103mmoll-1Na+, 6mmoll-1 K+ and 93mmoll-1Cl-, intracellular ion activities in unstimulated upper Malpighian tubules were 21, 86 and 32mmoll-1, respectively. In serotonin-stimulated tubules, aCl was unchanged, whereas aNa increased to 33mmoll-1 and aK declined to 71mmoll-1. Vbl was -59mV and -63mV for unstimulated and stimulated tubules, respectively. Calculated electrochemical potentials(Δμ/F) favour passive movement of Na+ into the cell and passive movement of Cl- out of the cell in both unstimulated and serotonin-stimulated tubules. Passive movement of K+ out of the cell is favoured in unstimulated tubules. In stimulated tubules, Δμ/F for K+ is close to 0 mV.The thermodynamic feasibilities of Na+-K+-2Cl-, Na+-Cl-and K+-Cl- cotransporters were evaluated by calculating the net electrochemical potential (Δμnet/F) for each transporter. Our results show that a Na+-K+-2Cl- or a Na+-Cl- cotransporter but not a K+-Cl- cotransporter would permit the movement of ions into the cell in stimulated tubules. The effects of Ba2+ and ouabain on Vbl and rates of fluid and ion secretion show that net entry of K+ through ion channels or the Na+/K+-ATPase can be ruled out in stimulated tubules. Maintenance of intracellular Cl- activity was dependent upon the presence of both Na+ and K+ in the bathing saline. Bumetanide reduced the fluxes of both Na+ and K+. Taken together, the results support the involvement of a basolateral Na+-K+-2Cl- cotransporter in serotonin-stimulated fluid secretion by Rhodnius prolixus Malpighian tubules.

Fluid secretion by the Malpighian tubules of insects

1971 ◽  
Vol 262 (842) ◽  
pp. 197-208 ◽  
Keyword(s):  
Extracellular Fluid ◽  
Fluid Secretion ◽  
Malpighian Tubules ◽  
Potassium Ions ◽  
Osmotic Gradient ◽  
Facilitated Diffusion ◽  
Phosphate Ions ◽  
Large Size ◽  
Efficient Coupling ◽  
Tubule Cells

Malpighian tubules of insects typically secrete an iso-osmotic fluid by a process which is thought to involve the following: (1) Potassium ions enter the tubule cells by a process which is sodium dependent and which may be active; they are then actively pumped into the lumen by an electrogenic pump. (2) Sodium ions cross the wall in a similar fashion to potassium ions but their entry into the cells is very restricted so that they are transported only slowly. (3) These active cation movements create a trans-wall potential favouring the passive movements of anions from the haemolymph into the lumen. (4) With one exception, smaller anions appear to cross the wall faster than do larger ones. The exception is that phosphate ions cross faster than any other anion in spite of their large size. The evidence suggests that this is more likely to be achieved by facilitated diffusion but active movements are not excluded. (5) The apical and basal membranes of the tubule cells are elaborately folded. It is suggested that these foldings act to couple movement of water to the movements of ions by allowing the development of standing osmotic gradients. (6) Such gradients will be small because the channels in which they occur are short. However, as the cell membranes probably have a high osmotic permeability water is likely to be able osmotically to equilibrate with the channel contents to produce an iso-somotic secretion. (7) The folds in the cell membrane are such that a parallel array of channels alternately opening to the cytoplasm and to the extracellular fluid is produced. Such an arrangement leads to a steeper osmotic gradient across the cell wall and this will promote a more efficient coupling of solute and water movements.

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.

scholarly journals A SLC4-like anion exchanger from renal tubules of the mosquito (Aedes aegypti): evidence for a novel role of stellate cells in diuretic fluid secretion

2010 ◽  
Vol 298 (3) ◽  
pp. R642-R660 ◽  
Author(s):  
Peter M. Piermarini ◽  
Laura F. Grogan ◽  
Kenneth Lau ◽  
Li Wang ◽  
Klaus W. Beyenbach
Keyword(s):  
Aedes Aegypti ◽  
Anion Exchanger ◽  
Xenopus Oocytes ◽  
Malpighian Tubule ◽  
Stellate Cells ◽  
Fluid Secretion ◽  
Malpighian Tubules ◽  
Renal Tubules ◽  
Basal Region ◽  
Principal Cells

Transepithelial fluid secretion across the renal (Malpighian) tubule epithelium of the mosquito ( Aedes aegypti ) is energized by the vacuolar-type (V-type) H+-ATPase and not the Na+-K+-ATPase. Located at the apical membrane of principal cells, the V-type H+-ATPase translocates protons from the cytoplasm to the tubule lumen. Secreted protons are likely to derive from metabolic H2CO3, which raises questions about the handling of HCO3−by principal cells. Accordingly, we tested the hypothesis that a Cl/HCO3anion exchanger (AE) related to the solute-linked carrier 4 (SLC4) superfamily mediates the extrusion of HCO3−across the basal membrane of principal cells. We began by cloning from Aedes Malpighian tubules a full-length cDNA encoding an SLC4-like AE, termed AeAE. When expressed heterologously in Xenopus oocytes, AeAE is both N- and O-glycosylated and mediates Na+-independent intracellular pH changes that are sensitive to extracellular Cl−concentration and to DIDS. In Aedes Malpighian tubules, AeAE is expressed as two distinct forms: one is O-glycosylated, and the other is N-glycosylated. Significantly, AeAE immunoreactivity localizes to the basal regions of stellate cells but not principal cells. Concentrations of DIDS that inhibit AeAE activity in Xenopus oocytes have no effects on the unstimulated rates of fluid secretion mediated by Malpighian tubules as measured by the Ramsay assay. However, in Malpighian tubules stimulated with kinin or calcitonin-like diuretic peptides, DIDS reduces the diuretic rates of fluid secretion to basal levels. In conclusion, Aedes Malpighian tubules express AeAE in the basal region of stellate cells, where this transporter may participate in producing diuretic rates of transepithelial fluid secretion.

scholarly journals Sugar transporters enable a leaf beetle to accumulate plant defense compounds

2021 ◽  
Author(s):  
Zhi-Ling Yang ◽  
Hussam Hassan Nour-Eldin ◽  
Sabine Hänniger ◽  
Michael Reichelt ◽  
Christoph Crocoll ◽  
...  
Keyword(s):  
Plant Defense ◽  
Flea Beetle ◽  
Malpighian Tubule ◽  
Transport Processes ◽  
The Body ◽  
Malpighian Tubules ◽  
Major Facilitator Superfamily ◽  
Herbivorous Insects ◽  
Specialist Herbivore ◽  
Defense Compounds

AbstractMany herbivorous insects selectively accumulate plant toxins for defense against predators; however, little is known about the transport processes that enable insects to absorb and store defense compounds in the body. Here, we investigate how a specialist herbivore, the horseradish flea beetle, accumulates high amounts of glucosinolate defense compounds in the hemolymph. Using phylogenetic analyses of coleopteran membrane transporters of the major facilitator superfamily, we identified a clade of glucosinolate-specific transporters (PaGTRs) belonging to the sugar porter family.PaGTRexpression was predominantly detected in the excretory system, the Malpighian tubules. Silencing ofPaGTRs led to elevated glucosinolate excretion, significantly reducing the levels of sequestered glucosinolates in beetles. This suggests thatPaGTRs reabsorb glucosinolates from the Malpighian tubule lumen to prevent their loss by excretion. Ramsay assays performed with dissected Malpighian tubules confirmed a selective retention of glucosinolates. Thus, the selective accumulation of plant defense compounds in herbivorous insects can depend on the ability to prevent excretion.

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.

Analysis of epithelial transport by measurement of K+, Cl- and pH gradients in extracellular unstirred layers: ion secretion and reabsorption by Malpighian tubules of Rhodnius prolixus

1997 ◽  
Vol 200 (11) ◽  
pp. 1627-1638 ◽  
Author(s):  
KA Collier ◽  
MJ O'Donnell
Keyword(s):  
Epithelial Transport ◽  
Malpighian Tubule ◽  
Fluid Secretion ◽  
Rhodnius Prolixus ◽  
Malpighian Tubules ◽  
Unstirred Layer ◽  
Ph Gradients ◽  
In Situ Preparation

Summary The pH and concentrations of K+ and Cl- in the unstirred layer (USL) associated with the basolateral surfaces of the upper and lower Malpighian tubules of Rhodnius prolixus were measured using extracellular ion-selective microelectrodes. When stimulated with 5-hydroxytryptamine (5-HT) in vitro, the upper Malpighian tubule secretes Na+, K+, Cl- and water at high rates; the lower Malpighian tubule reabsorbs K+ and Cl- but not water. Concentrations of K+ and Cl- in the unstirred layer of the lower Malpighian tubule ([K+]USL, [Cl-]USL) were greater than those in the bathing saline, consistent with the accumulation of K+ and Cl- in the USL during 5-HT-stimulated KCl reabsorption. [K+]USL exceeded [K+]Bath by as much as 5.3-fold. Calculations of K+ flux based on measurements of [K+]USL at various distances from the tubule surface agreed well with flux calculated from the rate of fluid secretion and the change in K+ concentration of the secreted fluid during passage through the lower tubule. Concentrations of K+ in the unstirred layer of the upper Malpighian tubule were reduced relative to those in the bathing saline, consistent with depletion of K+ from the USL during 5-HT-stimulated secretion of K+ from bath to lumen. Changes in [K+]USL during 5-HT-stimulated K+ secretion from single upper Malpighian tubule cells could be resolved. Although differences between [K+]USL and [K+]Bath were apparent for upper and lower tubules in an in situ preparation, they were reduced relative to the differences measured using isolated tubules. We suggest that convective mixing of the fluids around the tubules by contractions of the midgut and hindgut reduces, but does not eliminate, differences between [K+]USL and [K+]Bath in situ. The USL was slightly acidic relative to the bath in 5-HT-stimulated upper and lower tubules; contributions to USL acidification are discussed. The results also show that the techniques described in this paper can resolve rapid and localized changes in ion transport across different regions of Malpighian tubules in response to stimulants or inhibitors of specific membrane transporters.

scholarly journals When two cells are better than one: specialized stellate cells provide a privileged route for uniquely rapid water flux in Drosophila renal tubule

2019 ◽  
Author(s):  
Pablo Cabrero ◽  
Selim Terhzaz ◽  
Anthony J. Dornan ◽  
Saurav Ghimire ◽  
Heather L. Holmes ◽  
...  
Keyword(s):  
Water Permeability ◽  
Plasma Membranes ◽  
Water Flux ◽  
Malpighian Tubule ◽  
Stellate Cells ◽  
Fluid Secretion ◽  
Malpighian Tubules ◽  
Principal Cells ◽  
Very High

AbstractInsects are highly successful, in part through an excellent ability to osmoregulate. The renal (Malpighian) tubules can secrete fluid faster on a per-cell basis than any other epithelium, but the route for these remarkable water fluxes has not been established. In Drosophila melanogaster, we show that 4 members of the Major Intrinsic Protein family are expressed at very high level in the fly renal tissue; the aquaporins Drip and Prip, and the aquaglyceroporins Eglp2 and Eglp4. As predicted from their structure and by their transport function by expressing these proteins in Xenopus oocytes, Drip, Prip and Eglp2 show significant and specific water permeability, whereas Eglp2 and Eglp4 show very high permeability to glycerol and urea. Knockdowns of any of these genes impacts tubule performance resulting in impaired hormone-induced fluid secretion. The Drosophila tubule has two main secretory cell types: active cation-transporting principal cells with the aquaglyceroporins localize to opposite plasma membranes and small stellate cells, the site of the chloride shunt conductance, with these aquaporins localising to opposite plasma membranes. This suggests a model in which cations are pumped by the principal cells, causing chloride to follow through the stellate cells in order to balance the charge. As a consequence, osmotically obliged water follows through the stellate cells. Consistent with this model, fluorescently labelled dextran, an in vivo marker of membrane water permeability, is trapped in the basal infoldings of the stellate cells after kinin diuretic peptide stimulation, confirming that these cells provide the major route for transepithelial water flux. The spatial segregation of these components of epithelial water transport may help to explain the unique success of the higher insects.Significance statementThe tiny insect renal (Malpighian) tubule can transport fluid at unparalleled speed, suggesting unique specialisations. Here we show that strategic allocation of Major Intrinsic Proteins (MIPs) to specific cells within the polarized tubule allow the separation of metabolically intense active cation transport from chloride and water conductance. This body plan is general to at least many higher insects, providing a clue to the unique success of the class Insecta.

scholarly journals A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles

2021 ◽  
Vol 118 (14) ◽  
pp. e2023314118
Author(s):  
Takashi Koyama ◽  
Muhammad Tayyib Naseem ◽  
Dennis Kolosov ◽  
Camilla Trang Vo ◽  
Duncan Mahon ◽  
...  
Keyword(s):  
Water Balance ◽  
Tribolium Castaneum ◽  
High Surface ◽  
Malpighian Tubule ◽  
Volume Ratio ◽  
Fluid Secretion ◽  
Fluorescent Labeling ◽  
Malpighian Tubules ◽  
Fluid Loss ◽  
Last Common Ancestor

Maintaining internal salt and water balance in response to fluctuating external conditions is essential for animal survival. This is particularly true for insects as their high surface-to-volume ratio makes them highly susceptible to osmotic stress. However, the cellular and hormonal mechanisms that mediate the systemic control of osmotic homeostasis in beetles (Coleoptera), the largest group of insects, remain largely unidentified. Here, we demonstrate that eight neurons in the brain of the red flour beetle Tribolium castaneum respond to internal changes in osmolality by releasing diuretic hormone (DH) 37 and DH47—homologs of vertebrate corticotropin-releasing factor (CRF) hormones—to control systemic water balance. Knockdown of the gene encoding the two hormones (Urinate, Urn8) reduces Malpighian tubule secretion and restricts organismal fluid loss, whereas injection of DH37 or DH47 reverses these phenotypes. We further identify a CRF-like receptor, Urinate receptor (Urn8R), which is exclusively expressed in a functionally unique secondary cell in the beetle tubules, as underlying this response. Activation of Urn8R increases K+ secretion, creating a lumen-positive transepithelial potential that drives fluid secretion. Together, these data show that beetle Malpighian tubules operate by a fundamentally different mechanism than those of other insects. Finally, we adopt a fluorescent labeling strategy to identify the evolutionary origin of this unusual tubule architecture, revealing that it evolved in the last common ancestor of the higher beetle families. Our work thus uncovers an important homeostatic program that is key to maintaining osmotic control in beetles, which evolved parallel to the radiation of the “advanced” beetle lineages.

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