Mechanisms of acid secretion in pseudobranch cells of rainbow trout(<i>Oncorhynchus mykiss</i>)

Kern, Georg; Bösch, Simone T.; Unterhuber, E; Pelster, Bernd

doi:10.1242/jeb.205.18.2943

Cited by 18 publications

(2 citation statements)

References 35 publications

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“…However, the specific mechanisms responsible for acidifying the blood reaching the eye has remained largely elusive. While the pseudobranch slightly acidifies the blood before it reaches the eye, this acidification is not sufficient to activate the Root effect (Bridges et al, 1998;Kern et al, 2002;Waser and Heisler, 2005;Waser and Heisler, 2004), as otherwise, this would lead to a maladaptive loss of O 2 to the surrounding water. Thus, an additional source of H + -secretion of the blood draining the pseudobranch is required to activate the Root effect and induce retinal O 2 secretion.…”

Section: Introductionmentioning

confidence: 99%

“…This multi-subunit enzyme uses the energy from ATP hydrolysis to transport H + across biological membranes (Tresguerres, 2016). VHA is expressed in cells within the pseudobranch and the swimbladder gas-gland (Boesch et al, 2003;Kern et al, 2002). However, H + s do not rapidly cross the red blood cell membrane and must be combined with HCO 3 À to form CO 2 (HCO 3 À dehydration) that readily diffuses across the RBC membrane (Brauner et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Active Blood Acidification Greatly Enhances Oxygen Supply to the Teleost Retina

et al. 2021

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Most ray‐finned fishes possess a unique system for retinal oxygen delivery, where intracellular acidification of red blood cells (RBCs) in the retinal capillaries induces oxygen offloading from pH‐sensitive hemoglobin. A countercurrent vascular network, the choroid rete mirabile, posterior to the retina augments this “oxygen‐secretory” mechanism and confers retinal PO2 values that can exceed 1300 mmHg in some species. We hypothesized that the choroid rete mirabile exerts an active role in intracellular RBC acidification to facilitate retinal oxygen secretion. We show the presence and enzymatic activities of extracellular carbonic anhydrase (CA) and vacuolar‐type H+‐ATPase (VHA) in the lumen of the choroid rete mirabile. These data are consistent with a pathway, where VHA secretes H+ into the choroid rete mirabile lumen, which combines with HCO3– to form CO2 (catalyzed by extracellular CA) that rapidly diffuses into the RBC facilitating hemoglobin oxygen offloading. Next, we validated the model in vivo by injecting an extracellular CA inhibitor (C18) into the dorsal aorta of anesthetized rainbow trout with a PO2 electrode implanted into the retina. Here, the inhibition of extracellular CA resulted in a rapid reduction in retinal PO2 from 517 to 226 mmHg within minutes. These data strongly support the proposed model for RBC acidification in the choroid rete mirabile. Further, in vivo data show that this mechanism primarily augments oxygen diffusion to the inner retinal segments involved in signal‐processing and that the evolution of this pathway was tightly associated with the morphological expansion of this part of the retina. Together, these data suggest that the evolutionary origin of retinal oxygen secretion in the early history of the ray‐finned fishes was associated with a greatly enhanced capacity for visual processing, potentially permitting improved visual prey detection and the colonization of novel environments.

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Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Active Blood Acidification Greatly Enhances Oxygen Supply to the Teleost Retina

et al. 2021

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Epithelial mitochondria-rich cells and associated innervation in adult and developing zebrafish

Jonz

Nurse

2006

J. Comp. Neurol.

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Studies of ion regulation by mitochondria-rich cells (MRCs) of transport epithelia in fish have revealed many processes by which ion homeostasis is achieved. However, the control of these mechanisms and, particularly, the extent of nervous system involvement are not completely understood. We characterized the potential innervation of MRCs in various gill and extrabranchial tissues involved in ion transport in the model vertebrate the zebrafish. Confocal and conventional microscopy of whole-mount preparations were combined with immunofluorescence techniques to label MRCs with antibodies against a subunit of the enzyme Na(+)/K(+)-ATPase and nerve fibers with a zebrafish neuronal marker, zn-12. MRCs of the gill filaments were identified by their morphology and migration out to the lamellae in response to ion-poor water acclimation. Gill MRCs were intimately associated with nerve fibers originating from outside the filaments. MRCs of the opercular epithelium resembled those of the gill and were also located adjacent to nerve fibers. Mitochondria-rich "pseudobranch cells" were identified in the pseudobranch by immunofluorescence and labeling of dissociated cells with the mitochondrial marker DASPEI. Pseudobranch MRCs resembled gill MRCs and received innervation from a dense network of nerve fibers. In larvae, MRCs were distributed across the surface of the skin. These cells were situated among a dense network of varicose nerve fibers, and some MRCs of the skin displayed extensive cytoplasmic processes. Evidence is presented suggestive of widespread association of MRCs with the nervous system in transport epithelia and the neural control of MRC-mediated ion regulation in teleost fish.

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The ultrastructural characterization of mitochondria-rich cells as a response to variations in salinity in two types of teleostean pseudobranch: milkfish (Chanos chanos) and Mozambique tilapia (Oreochromis mossambicus)

Shan

Tsai

Kang

et al. 2017

Journal of Morphology

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The pseudobranchs of two euryhaline teleost species, the milkfish (Chanos chanos) and the Mozambique tilapia (Oreochromis mossambicus), were studied after acclimization to different salinities using optical and electron microscopy. The milkfish pseudobranch was the lamellae-free type, with separate lamellae along the filaments containing two groups of mitochondria (Mt)-rich cells: chloride cells (CCs) and pseudobranch type cells (PSCs). Conversely, the tilapia pseudobranch was the embedded type, covered with connective tissues and with only one group of Mt-rich PSCs. Chloride cells were identified according to the apical openings and branched tubular networks around randomly distributed and diversely shaped Mt. Pseudobranchs type cells, however, were characterized according to the orderly arrangement of parallel tubules around closely packed Mt; both the tubules and the Mt were distributed in the vascular side of the cell, but were absent from the apical region. Compared with those of seawater (SW)-acclimated milkfish, the pseudobranchial lamellae of freshwater (FW) specimens were longer on average, and the Mt of the CCs had fewer cristae, were less electron-dense, and were often vacuolated. The Mt in the PSCs of FW-acclimated milkfish and tilapia were larger and more electron-dense than those of their SW-acclimated counterparts; in addition, more tubules were found to aggregately surround the Mt and basolateral membranes in the PSCs of fish from the hypo-osmotic environment. Conversely, the PSCs of tilapia were periodic acid-Schiff (PAS)-positive, and Mt in PSCs were concentrated with more parallel arrays of the tubule system than those of milkfish. Therefore, salinity-dependent changes in the ultrastructures of PSCs suggest their potential role in energy metabolism of both lamellae-free and embedded pseudobranchs, whereas the PAS-positive staining characteristics suggest a role in releasing or storaging polysaccharides in the embedded pseudobranch. J. Morphol. 278:390-402, 2017. © 2017 Wiley Periodicals, Inc.

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Mechanisms of acid secretion in pseudobranch cells of rainbow trout(Oncorhynchus mykiss)

Cited by 18 publications

References 35 publications

Active Blood Acidification Greatly Enhances Oxygen Supply to the Teleost Retina

Active Blood Acidification Greatly Enhances Oxygen Supply to the Teleost Retina

Epithelial mitochondria-rich cells and associated innervation in adult and developing zebrafish

The ultrastructural characterization of mitochondria-rich cells as a response to variations in salinity in two types of teleostean pseudobranch: milkfish (Chanos chanos) and Mozambique tilapia (Oreochromis mossambicus)

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