Extrabranchial mechanisms of systemic pH recovery in hagfish (Eptatretus stoutii)

Clifford, Alexander M.; Guffey, Samuel C.; Goss, Greg G.

doi:10.1016/j.cbpa.2013.11.009

Cited by 21 publications

(19 citation statements)

References 32 publications

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“…Specially constructed hagfish compartmentalizing flux chambers (58×6.3×6.1 cm L×W×H; schematic diagram available in Fig. S1 and photos available in Clifford et al, 2014) were used to partition anterior and posterior contributions to ṀO 2 and J Amm . Anterior (20 cm) and posterior (32 cm) chambers were separated by a collar assembly made from two square Plexiglas plates with 2.5 cm diameter central holes sandwiching a latex sheath (finger from nonpowdered latex glove; 7 cm long×2 cm unstretched diameter) and bolted together.…”

Section: Introductionmentioning

confidence: 99%

It's all in the gills: Evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin

Clifford

Zimmer

Wood

et al. 2016

Journal of Experimental Biology

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Hagfish skin has been reported as an important site for ammonia excretion and as the major site of systemic oxygen acquisition. However, whether cutaneous O 2 uptake is the dominant route of uptake remains under debate; all evidence supporting this hypothesis has been derived using indirect measurements. Here, we used partitioned chambers and direct measurements of oxygen consumption and ammonia excretion to quantify cutaneous and branchial exchanges in Pacific hagfish (Eptatretus stoutii) at rest and following exhaustive exercise. Hagfish primarily relied on the gills for both O 2 uptake (81.0%) and ammonia excretion (70.7%). Following exercise, both O 2 uptake and ammonia excretion increased, but only across the gill; cutaneous exchange was not increased. When branchial O 2 availability was reduced by exposure to anteriorly localized hypoxia (∼4.6 kPa O 2 ), cutaneous O 2 consumption was only slightly elevated on an absolute basis. These results refute a major role for cutaneous O 2 acquisition in the Pacific hagfish.

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Section: Introductionmentioning

confidence: 99%

It's all in the gills: Evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin

Clifford

Zimmer

Wood

et al. 2016

Journal of Experimental Biology

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“…This suggestion was further supported by the demonstration of a significant increase in hagfish gill NHE mRNA expression following the induction of metabolic acidosis (6). An alternate role for the NHE would be to act as a Na ϩ /NH 4 ϩ exchanger; however, Evans (7) found no evidence for the presence of Na ϩ /NH 4 ϩ exchange in the Atlantic hagfish. This finding, along with recent evidence presented for Pacific hagfish, suggests the hagfish's ability to excrete ammonia following a perturbation may be via Rh glycoproteins (1).…”

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“…In a review, Weihrauch et al (38) presented two working models for ammonia excretion across the branchial epithelium of marine fishes, one associated with pavement cells and the other with MRCs. The pavement cell model involves basolaterally located Rhbg and apically located Rhcg2, as proposed by Nakada et al (19), but adds that significant diffusion of NH 3 and NH 4 ϩ likely occurs across the shallow paracellular junction of gill epithelial cells in marine fishes. Weihrauch et al (38) suggested that as pavement cells comprise the majority (greater than 90%) of the surface area of the marine fish gill, they most likely provide the dominant route of branchial ammonia excretion.…”

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“…Weihrauch et al (38) suggested that as pavement cells comprise the majority (greater than 90%) of the surface area of the marine fish gill, they most likely provide the dominant route of branchial ammonia excretion. Alternatively, the proposed MRC model is primarily focused on the transport of NH 4 ϩ into the MRCs via basolaterally located NKA and NKCC and excreted as NH 4 ϩ substituted for H ϩ as the substrate of apically located Na ϩ / H ϩ -exchanger (NHE-2) or as NH 3 by Rhcg1 (38). The localization of Rhcg variants 1 and 2 to the apical membrane of branchial epithelial cells suggests their possible involvement in facilitating the outward diffusion of NH 3 from the branchial epithelium to the water.…”

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Ammonia excretion in the Atlantic hagfish (Myxine glutinosa) and responses of an Rhc glycoprotein

Edwards

Arnold

Blair

et al. 2015

American Journal of Physiology-Regulatory, Integrative and Comp

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Hagfishes, the most ancient of the extant craniates, demonstrate a high tolerance for a number of unfavorable environmental conditions, including elevated ammonia. Proposed mechanisms of ammonia excretion in aquatic organisms include vesicular NH4+ transport and release by exocytosis in marine crabs, and passive NH3 diffusion, active NH4+ transport, and paracellular leakage of NH3 or NH4+ across the gills of fishes. Recently, an emerging paradigm suggests that Rhesus glycoproteins play a vital role in ammonia transport in both aquatic invertebrates and vertebrates. This study has identified an Rh glycoprotein ortholog from the gills of Atlantic hagfish. The hagfish Rhcg shares a 56–60% amino acid identity to other vertebrate Rhcg cDNAs. Sequence information was used to produce an anti-hagfish Rhcg (hRhcg) antibody. We have used hRhcg to localize protein expression to epithelial cells of the gill and the skin. In addition, we have quantified hRhcg expression following exposure to elevated plasma ammonia levels. Animals exposed to a 3 mmol/kg NH4Cl load resulted in significantly elevated plasma ammonia concentrations compared with controls for up to 4 h postinjection. This correlated with net ammonia excretion rates that were also significantly elevated for up to 4 h postinjection. Rhcg mRNA expression in both the gill and skin was significantly elevated by 15 min and 1 h, respectively, and hRhcg protein expression in gills was significantly elevated at 2, 4, and 8 h postinjection. These results demonstrate a potential role for Rhcg in the excretion of ammonia in the Atlantic hagfish.

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“…This efficient countercurrent exchange system provides hagfish with a favorable surface for exchange of ions, gases, and waste products between the blood and water (26). The gills are, therefore, suggested to play an important role in gas transport, ionoregulation, acid-base balance, and nitrogenous waste excretion (7,9,10,40).…”

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Phosphate absorption across multiple epithelia in the Pacific hagfish (Eptatretus stoutii)

Schultz

Guffey

Clifford

et al. 2014

American Journal of Physiology-Regulatory, Integrative and Comp

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Inorganic phosphate (Pi) is an essential nutrient for all organisms, but in seawater, Pi is a limiting nutrient. This study investigated the primary mechanisms of Pi uptake in Pacific hagfish ( Eptatretus stoutii) using ex vivo physiological and molecular techniques. Hagfish were observed to have the capacity to absorb Pi from the environment into at least three epithelial surfaces: the intestine, skin, and gill. Pi uptake in all tissues was concentration dependent, and saturable Pi transport was observed in the skin and gill at <2.0 mmol/l Pi. Gill and intestinal Pi uptake was sodium dependent, but Pi uptake into the skin increased under low sodium conditions. Gill Pi transport exhibited an apparent affinity constant ∼0.23–0.6 mmol/l Pi. A complete sequence of a type II sodium phosphate cotransporter (Slc34a) was obtained from the hagfish gill. Phylogenetic analysis of the hagfish Slc34a transporter indicates that it is earlier diverging than, and/or ancestral to, the other identified vertebrate Slc34a transporters (Slc34a1, Slc34a2, and Slc34a3). With the use of RT-PCR, the hagfish Slc34a transcript was detected in the intestine, skin, gill, and kidney, suggesting that this may be the transporter involved in Pi uptake into multiple epithelia in the hagfish. This is the first measurement of Pi uptake across the gill or skin of any vertebrate animal and first sodium phosphate cotransporter identified in hagfish.

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Extrabranchial mechanisms of systemic pH recovery in hagfish (Eptatretus stoutii)

Cited by 21 publications

References 32 publications

It's all in the gills: Evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin

It's all in the gills: Evaluation of O2 uptake in Pacific hagfish refutes a major respiratory role for the skin

Ammonia excretion in the Atlantic hagfish (Myxine glutinosa) and responses of an Rhc glycoprotein

Phosphate absorption across multiple epithelia in the Pacific hagfish (Eptatretus stoutii)

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