The single kinin receptor signals to separate and independent physiological pathways in Malpighian tubules of the yellow fever mosquito

In the past, we have used the kinins of the cockroach Leucophaea (the leucokinins) to evaluate the mechanism of diuretic action of kinin peptides in Malpighian tubules of the yellow fever mosquito Aedes aegypti . Now using the kinins of Aedes (the aedeskinins), we have found that in isolated Aedes Malpighian tubules all three aedeskinins (1 μM) significantly 1) increased the rate of fluid secretion (V̇S), 2) hyperpolarized the basolateral membrane voltage (Vbl), and 3) decreased the input resistance (Rin) of principal cells, consistent with the known increase in the Cl− conductance of the paracellular pathway in Aedes Malpighian tubules. Aedeskinin-III, studied in further detail, significantly increased V̇S with an EC50 of 1.5 × 10−8 M. In parallel, the Na+ concentration in secreted fluid significantly decreased, and the K+ concentration significantly increased. The concentration of Cl− remained unchanged. While the three aedeskinins triggered effects on Vbl, Rin, and V̇S, synthetic kinin analogs, which contain modifications of the COOH-terminal amide pentapeptide core sequence critical for biological activity, displayed variable effects. For example, kinin analog 1578 significantly stimulated V̇S but had no effect on Vbl and Rin, whereas kinin analog 1708 had no effect on V̇S but significantly affected Vbl and Rin. These observations suggest separate signaling pathways activated by kinins. One triggers the electrophysiological response, and the other triggers fluid secretion. It remains to be determined whether the two signaling pathways emanate from a single kinin receptor via agonist-directed signaling or from a differentially glycosylated receptor. Occasionally, Malpighian tubules did not exhibit a detectable response to natural and synthetic kinins. Hypothetically, the expression of the kinin receptor may depend on developmental, nutritional, and/or reproductive signals.

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Hormone-controlled cAMP-mediated fluid secretion in yellow-fever mosquito

AJP Regulatory Integrative and Comparative Physiology ◽

10.1152/ajpregu.1987.253.5.r701 ◽

1987 ◽

Vol 253 (5) ◽

pp. R701-R711 ◽

Cited By ~ 10

Author(s):

D. H. Petzel ◽

M. M. Berg ◽

K. W. Beyenbach

Keyword(s):

Yellow Fever ◽

Natriuretic Peptides ◽

Basolateral Membrane ◽

Fluid Secretion ◽

Malpighian Tubules ◽

In Vivo Studies ◽

Intracellular Camp ◽

Yellow Fever Mosquito ◽

Water Fraction

Evidence is presented for hormone-controlled adenosine 3',5'-cyclic monophosphate (cAMP)-mediated NaCl diuresis in Malpighian tubules of the blood-feeding yellow-fever mosquito Aedes aegypti. Studies in isolated Malpighian tubules reveal that cAMP added to the peritubular bath selectively stimulates NaCl secretion and not KCl secretion by increasing the Na conductance of the basolateral membrane of primary cells. These effects are duplicated by forskolin and theophylline in parallel with increased intracellular concentrations of endogenous cAMP. Two natriuretic peptides that we have isolated by high-pressure liquid chromatography (HPLC) methods from mosquito heads also increase NaCl and fluid secretion in isolated Malpighian tubules together with increased intracellular levels of cAMP. These results are consistent with a mechanism of NaCl diuresis in which the natriuretic peptides and cAMP are respectively the primary and secondary messengers that couple the ingestion of a blood meal to the excretion of the unwanted salt and water fraction of the meal. This hypothesis is supported by in vivo studies that reveal elevated intracellular cAMP levels in Malpighian tubules at the time of maximum NaCl diuresis.

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Dibutyryl cAMP activates bumetanide-sensitive electrolyte transport in Malpighian tubules

AJP Cell Physiology ◽

10.1152/ajpcell.1991.261.3.c521 ◽

1991 ◽

Vol 261 (3) ◽

pp. C521-C529 ◽

Cited By ~ 66

Author(s):

J. L. Hegarty ◽

B. Zhang ◽

T. L. Pannabecker ◽

D. H. Petzel ◽

M. D. Baustian ◽

...

Keyword(s):

Yellow Fever ◽

Apical Membrane ◽

Basolateral Membrane ◽

Fluid Secretion ◽

Ringer Solution ◽

Malpighian Tubules ◽

Membrane Voltage ◽

Dibutyryl Camp ◽

K Secretion ◽

Transepithelial Voltage

The effects of dibutyryl adenosine 3',5'-cyclic monophosphate (DBcAMP) and bumetanide (both 10(-4) M) on transepithelial Na+, K+, Cl-, and fluid secretion and on tubule electrophysiology were studied in isolated Malpighian tubules of the yellow fever mosquito Aedes aegypti. Peritubular DBcAMP significantly increased Na+, Cl-, and fluid secretion but decreased K+ secretion. In DBcAMP-stimulated tubules, bumetanide caused Na+, Cl-, and fluid secretion to return to pre-cAMP control rates and K+ secretion to decrease further. Peritubular bumetanide significantly increased Na+ secretion and decreased K+ secretion so that Cl- and fluid secretion did not change. In bumetanide-treated tubules, the secretagogue effects of DBcAMP are blocked. In isolated Malpighian tubules perfused with symmetrical Ringer solution, DBcAMP significantly hyperpolarized the transepithelial voltage (VT) and depolarized the basolateral membrane voltage (Vbl) with no effect on apical membrane voltage (Va). Total transepithelial resistance (RT) and the fractional resistance of the basolateral membrane (fRbl) significantly decreased. Bumetanide also hyperpolarized VT and depolarized Vbl, however without significantly affecting RT and fRbl. Together these results suggest that, in addition to stimulating electroconductive transport, DBcAMP also activates a nonconductive bumetanide-sensitive transport system in Aedes Malpighian tubules.

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Inhibition of eicosanoid biosynthesis modulates basal fluid secretion in the Malpighian tubules of the yellow fever mosquito (Aedes aegypti)

Journal of Insect Physiology ◽

10.1016/0022-1910(92)90016-7 ◽

1992 ◽

Vol 38 (1) ◽

pp. 1-8 ◽

Cited By ~ 45

Author(s):

David H. Petzel ◽

David W. Stanley-Samuelson

Keyword(s):

Aedes Aegypti ◽

Yellow Fever ◽

Fluid Secretion ◽

Malpighian Tubules ◽

Yellow Fever Mosquito

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Roles of PKC and phospho‑adducin in transepithelial fluid secretion by Malpighian tubules of the yellow fever mosquito

Tissue Barriers ◽

10.4161/tisb.23120 ◽

2013 ◽

Vol 1 (1) ◽

pp. e23120 ◽

Cited By ~ 4

Author(s):

Jeremy T. Miyauchi ◽

Peter M. Piermarini ◽

Jason D. Yang ◽

Diana M. Gilligan ◽

Klaus W. Beyenbach

Keyword(s):

Yellow Fever ◽

Fluid Secretion ◽

Malpighian Tubules ◽

Yellow Fever Mosquito

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Corrigendum: RNA-Seq Comparison of Larval and Adult Malpighian Tubules of the Yellow Fever Mosquito Aedes aegypti Reveals Life Stage-Specific Changes in Renal Function

Frontiers in Physiology ◽

10.3389/fphys.2017.00843 ◽

2017 ◽

Vol 8 ◽

Author(s):

Yiyi Li ◽

Peter M. Piermarini ◽

Carlos J. Esquivel ◽

David P. Price ◽

Hannah E. Drumm ◽

...

Keyword(s):

Renal Function ◽

Aedes Aegypti ◽

Yellow Fever ◽

Life Stage ◽

Malpighian Tubules ◽

Rna Seq ◽

Yellow Fever Mosquito

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Voltage clamping single cells in intact Malpighian tubules of mosquitoes

AJP Renal Physiology ◽

10.1152/ajprenal.2000.279.4.f747 ◽

2000 ◽

Vol 279 (4) ◽

pp. F747-F754 ◽

Cited By ~ 19

Author(s):

R. Masia ◽

D. Aneshansley ◽

W. Nagel ◽

R. J. Nachman ◽

K. W. Beyenbach

Keyword(s):

Apical Membrane ◽

Single Cells ◽

Basolateral Membrane ◽

Malpighian Tubule ◽

Input Resistance ◽

Membrane Resistance ◽

Malpighian Tubules ◽

Shunt Resistance ◽

Transport Pathways ◽

Principal Cells

Principal cells of the Malpighian tubule of the yellow fever mosquito were studied with the methods of two-electrode voltage clamp (TEVC). Intracellular voltage ( V pc) was −86.7 mV, and input resistance ( R pc) was 388.5 kΩ ( n = 49 cells). In six cells, Ba2+ (15 mM) had negligible effects on V pc, but it increased R pc from 325.3 to 684.5 kΩ ( P< 0.001). In the presence of Ba2+, leucokinin-VIII (1 μM) increased V pc to −101.8 mV ( P < 0.001) and reduced R pc to 340.2 kΩ ( P < 0.002). Circuit analysis yields the following: basolateral membrane resistance, 652.0 kΩ; apical membrane resistance, 340.2 kΩ; shunt resistance ( R sh), 344.3 kΩ; transcellular resistance, 992.2 kΩ. The fractional resistance of the apical membrane (0.35) and the ratio of transcellular resistance and R sh (3.53) agree closely with values obtained by cable analysis in isolated perfused tubules and confirm the usefulness of TEVC methods in single principal cells of the intact Malpighian tubule. Dinitrophenol (0.1 mM) reversibly depolarized V pc from −94.3 to −10.7 mV ( P< 0.001) and reversibly increased R pc from 412 to 2,879 kΩ ( P < 0.001), effects that were duplicated by cyanide (0.3 mM). Significant effects of metabolic inhibition on voltage and resistance suggest a role of ATP in electrogenesis and the maintenance of conductive transport pathways.

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

Journal of Experimental Biology ◽

10.1242/jeb.205.11.1645 ◽

2002 ◽

Vol 205 (11) ◽

pp. 1645-1655 ◽

Cited By ~ 7

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.

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