Characterisation of neurotransmitter-induced electrolyte transport in cockroach salivary glands by intracellular Ca2+, Na+ and pH measurements in duct cells

Hille, Carsten

doi:10.1242/jeb.010207

Cited by 15 publications

(18 citation statements)

References 53 publications

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“…However, in the presence of HCO 3 Ϫ / CO 2 -buffered saline, NKCC activity can be at least partly compensated by paired NHE/AE activity keeping resting [Cl Ϫ ] i high, which is not the case in HCO 3 Ϫ -free saline as used in this study (47). The HCO 3 Ϫ -dependent NKCC and NHE/AE activity has been also demonstrated indirectly by pH i recordings in cockroach salivary duct cells (28). However, to our knowledge no data are available for NKCC regulation in insect salivary glands.…”

Section: Discussionmentioning

confidence: 60%

“…Bath application of bumetanide has been previously shown to reduce the dopamine-induced fluid secretion by 92% and the concentrations of Na ϩ , K ϩ , and Cl Ϫ in the final saliva (60). In addition, bumetanide also influenced the saliva modification in the duct cells, most likely indirectly because of missing primary saliva in the duct lumen (28,44). From these observations it was concluded that a basolateral NKCC in the acinar peripheral cells is activated for NaCl uptake during dopamine-induced NaCl-rich primary saliva secretion.…”

Section: Discussionmentioning

confidence: 99%

“…However, this remains speculative because so far only basolateral membrane potential recordings, but no intracellular ion recordings, could be successfully performed in living cockroach salivary acinar cells (65,66). Thus the presence of a Na ϩ -K ϩ -2Cl Ϫ cotransporter (NKCC), Cl Ϫ -HCO 3 Ϫ (AE), and Na ϩ -H ϩ exchangers (NHE) within the cockroach salivary acinar peripheral cells is still postulated only indirectly from microfluorometric ion measurements in duct cells and recordings of saliva secretion rates (28,60). The lack of data concerning acinar ion homeostasis exists mainly because of methodological problems.…”

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confidence: 99%

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Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na⁺ and Cl⁻ changes in cockroach salivary acinar cells

Lahn

Dosche

Hille

2011

American Journal of Physiology-Cell Physiology

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The intracellular ion homeostasis in cockroach salivary acinar cells during salivation is not satisfactorily understood. This is mainly due to technical problems regarding strong tissue autofluorescence and ineffective ion concentration quantification. For minimizing these problems, we describe the successful application of two-photon (2P) microscopy partly in combination with fluorescence lifetime imaging microscopy (FLIM) to record intracellular Na(+) and Cl(-) concentrations ([Na(+)](i), [Cl(-)](i)) in cockroach salivary acinar cells. Quantitative 2P-FLIM Cl(-) measurements with the dye N-(ethoxycarbonylmethyl)-6-methoxy-quinolinium bromide indicate that the resting [Cl(-)](i) is 1.6 times above the Cl(-) electrochemical equilibrium but is not influenced by pharmacological inhibition of the Na(+)-K(+)-2Cl(-) cotransporter (NKCC) and anion exchanger using bumetanide and 4,4'-diisothiocyanatodihydrostilbene-2,2'-disulfonic acid disodium salt. In contrast, rapid Cl(-) reuptake after extracellular Cl(-) removal is almost totally NKCC mediated both in the absence and presence of dopamine. However, in physiological saline [Cl(-)](i) does not change during dopamine stimulation although dopamine stimulates fluid secretion in these glands. On the other hand, dopamine causes a decrease in the sodium-binding benzofuran isophthalate tetra-ammonium salt (SBFI) fluorescence and an increase in the Sodium Green fluorescence after 2P excitation. This opposite behavior of both dyes suggests a dopamine-induced [Na(+)](i) rise in the acinar cells, which is supported by the determined 2P-action cross sections of SBFI. The [Na(+)](i) rise is Cl(-) dependent and inhibited by bumetanide. The Ca(2+)-ionophore ionomycin also causes a bumetanide-sensitive [Na(+)](i) rise. We propose that a Ca(2+)-mediated NKCC activity in acinar peripheral cells attributable to dopamine stimulation serves for basolateral Na(+) uptake during saliva secretion and that the concomitantly transported Cl(-) is recycled back to the bath.

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Section: Discussionmentioning

confidence: 60%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na⁺ and Cl⁻ changes in cockroach salivary acinar cells

Lahn

Dosche

Hille

2011

American Journal of Physiology-Cell Physiology

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“…We also report numerous transcripts predicting receptors for a Na+-transmitter symporter, molecules that transport cations into cells innervated by dopaminergic and/or serotoninergic neurons. In cockroaches, it is believed that these transporters are involved in the secretion of the NaCl-rich primary saliva [58], a finding import for ticks in which regulation of the salt composition of saliva is essential for control of body water balance (Table 5). …”

Section: Resultsmentioning

confidence: 99%

Transcriptome of the Female Synganglion of the Black-Legged Tick Ixodes scapularis (Acari: Ixodidae) with Comparison between Illumina and 454 Systems

Egekwu

Sonenshine

Bissinger³

et al. 2014

PLoS ONE

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Illumina and 454 pyrosequencing were used to characterize genes from the synganglion of female Ixodes scapularis. GO term searching success for biological processes was similar for samples sequenced by both methods. However, for molecular processes, it was more successful for the Illumina samples than for 454 samples. Functional assignments of transcripts predicting neuropeptides, neuropeptide receptors, neurotransmitter receptors and other genes of interest was done, supported by strong e-values (<−6), and high consensus sequence alignments. Transcripts predicting 15 putative neuropeptide prepropeptides ((allatostatin, allatotropin, bursicon α, corticotropin releasing factor (CRF), CRF-binding protein, eclosion hormone, FMRFamide, glycoprotein A, insulin-like peptide, ion transport peptide, myoinhibitory peptide, inotocin ( = neurophysin-oxytocin), Neuropeptide F, sulfakinin and SIFamide)) and transcripts predicting receptors for 14 neuropeptides (allatostatin, calcitonin, cardioacceleratory peptide, corazonin, CRF, eclosion hormone, gonadotropin-releasing hormone/AKH-like, insulin-like peptide, neuropeptide F, proctolin, pyrokinin, SIFamide, sulfakinin and tachykinin) are reported. Similar to Dermacentor variabilis, we found transcripts matching pro-protein convertase, essential for converting neuropeptide hormones to their mature form. Additionally, transcripts predicting 6 neurotransmitter/neuromodulator receptors (acetylcholine, GABA, dopamine, glutamate, octopamine and serotonin) and 3 neurotransmitter transporters (GABA transporter, noradrenalin-norepinephrine transporter and Na+-neurotransmitter/symporter) are described. Further, we found transcripts predicting genes for pheromone odorant receptor, gustatory receptor, novel GPCR messages, ecdysone nuclear receptor, JH esterase binding protein, steroidogenic activating protein, chitin synthase, chitinase, and other genes of interest. Also found were transcripts predicting genes for spermatogenesis-associated protein, major sperm protein, spermidine oxidase and spermidine synthase, genes not normally expressed in the female CNS of other invertebrates. The diversity of messages predicting important genes identified in this study offers a valuable resource useful for understanding how the tick synganglion regulates important physiological functions.

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“…Thus, a [Ca 2+ ] i rise accompanied by intracellular acidification could probably be detected with ACR at a higher [Ca 2+ ] i level than actually occurs. From the literature it is known that cockroach salivary gland duct cells acidify after dopamine stimulation, from about pH 7.3 to pH 6.9 [47]. This acidification would lead to an increase in the signal of the Ca 2+ -free ACR species of about 10%, which might cause a slight overestimation of the [Ca 2+ ] i rise.…”

Section: Resultsmentioning

confidence: 99%

Asante Calcium Green and Asante Calcium Red—Novel Calcium Indicators for Two-Photon Fluorescence Lifetime Imaging

Jahn

Hille

2014

PLoS ONE

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For a comprehensive understanding of cellular processes and potential dysfunctions therein, an analysis of the ubiquitous intracellular second messenger calcium is of particular interest. This study examined the suitability of the novel Ca2+-sensitive fluorescent dyes Asante Calcium Red (ACR) and Asante Calcium Green (ACG) for two-photon (2P)-excited time-resolved fluorescence measurements. Both dyes displayed sufficient 2P fluorescence excitation in a range of 720–900 nm. In vitro, ACR and ACG exhibited a biexponential fluorescence decay behavior and the two decay time components in the ns-range could be attributed to the Ca2+-free and Ca2+-bound dye species. The amplitude-weighted average fluorescence decay time changed in a Ca2+-dependent way, unraveling in vitro dissociation constants K D of 114 nM and 15 nM for ACR and ACG, respectively. In the presence of bovine serum albumin, the absorption and steady-state fluorescence behavior of ACR was altered and its biexponential fluorescence decay showed about 5-times longer decay time components indicating dye-protein interactions. Since no ester derivative of ACG was commercially available, only ACR was evaluated for 2P-excited fluorescence lifetime imaging microscopy (2P-FLIM) in living cells of American cockroach salivary glands. In living cells, ACR also exhibited a biexponential fluorescence decay with clearly resolvable short (0.56 ns) and long (2.44 ns) decay time components attributable to the Ca2+-free and Ca2+-bound ACR species. From the amplitude-weighted average fluorescence decay times, an in situ K D of 180 nM was determined. Thus, quantitative [Ca2+]i recordings were realized, unraveling a reversible dopamine-induced [Ca2+]i elevation from 21 nM to 590 nM in salivary duct cells. It was concluded that ACR is a promising new Ca2+ indicator dye for 2P-FLIM recordings applicable in diverse biological systems.

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Characterisation of neurotransmitter-induced electrolyte transport in cockroach salivary glands by intracellular Ca2+, Na+ and pH measurements in duct cells

Cited by 15 publications

References 53 publications

Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na⁺ and Cl⁻ changes in cockroach salivary acinar cells

Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na⁺ and Cl⁻ changes in cockroach salivary acinar cells

Transcriptome of the Female Synganglion of the Black-Legged Tick Ixodes scapularis (Acari: Ixodidae) with Comparison between Illumina and 454 Systems

Asante Calcium Green and Asante Calcium Red—Novel Calcium Indicators for Two-Photon Fluorescence Lifetime Imaging

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Characterisation of neurotransmitter-induced electrolyte transport in cockroach salivary glands by intracellular Ca2+, Na+ and pH measurements in duct cells

Cited by 15 publications

References 53 publications

Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na+ and Cl− changes in cockroach salivary acinar cells

Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na+ and Cl− changes in cockroach salivary acinar cells

Transcriptome of the Female Synganglion of the Black-Legged Tick Ixodes scapularis (Acari: Ixodidae) with Comparison between Illumina and 454 Systems

Asante Calcium Green and Asante Calcium Red—Novel Calcium Indicators for Two-Photon Fluorescence Lifetime Imaging

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Product

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Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na⁺ and Cl⁻ changes in cockroach salivary acinar cells

Two-photon microscopy and fluorescence lifetime imaging reveal stimulus-induced intracellular Na⁺ and Cl⁻ changes in cockroach salivary acinar cells