Lipid acquisition and tissue storage in hagfish: new insights from an ancient vertebrate

Weinrauch, Alyssa M.; Glover, Chris N.; Goss, Greg G.

doi:10.1007/s00360-018-1196-8

Cited by 9 publications

(7 citation statements)

References 58 publications

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“…This action could signal a switch towards lipids as a fuel source and is consistent with a move from carbohydrate to lipid metabolism during fasting in this group (Emdin, 1982). This switch is supported by large and diffuse tissue lipid deposits that could accommodate lengthy periods without feeding (Weinrauch et al, 2019). Additionally, it has been observed that serotonin is produced by, and has biological effects in, hagfishes (Bernier and Perry, 1996).…”

Section: Critical Knowledge Gapssupporting

confidence: 66%

The good, the bad and the slimy: experimental studies of hagfish digestive and nutritional physiology

Glover

Weinrauch

2019

Journal of Experimental Biology

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The hagfishes provide valuable insight into the physiology of feeding, digestion and nutrient absorption by virtue of unusual and unique features of their biology. For example, members of this group undergo long periods of fasting, and are the only vertebrates known to absorb organic nutrients across their epidermal surface. Such properties engender significant attention from researchers interested in feeding and feeding-related processes; however, the practical realities of employing the hagfish as an experimental organism can be challenging. Many of the key tools of the experimental biologist are compromised by a species that does not readily feed in captivity, is difficult to instrument and which produces copious quantities of slime. This Commentary provides critical insight into the key aspects of hagfish feeding and digestive processes, and highlights the pitfalls of this group as experimental organisms. We also suggest key research gaps that, if filled, will lead to better understanding of hagfishes, and we consider how this group may advance our knowledge of feeding, digestion and nutrient absorption processes.

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Section: Critical Knowledge Gapssupporting

confidence: 66%

The good, the bad and the slimy: experimental studies of hagfish digestive and nutritional physiology

Glover

Weinrauch

2019

Journal of Experimental Biology

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“…Lipids are an invaluable energetic source for hagfish, particularly during extended periods of starvation, which can persist at least 11 months in captivity [32,46]. Recent evidence has suggested that hagfish have a regulated and specific mechanism by which lipids can be acquired in the hindgut [47] and lipases are essential for the digestion and assimilation of dietary lipids. There were significantly elevated lipase activities in the anterior tract (B and PCD) in comparison to all regions of the hindgut (Fig 3).…”

Section: Discussionmentioning

confidence: 99%

Activity and post-prandial regulation of digestive enzyme activity along the Pacific hagfish (Eptatretus stoutii) alimentary canal

2019

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Hagfishes are living representatives of the earliest-diverging vertebrates and are thus useful for the study of early vertebrate physiology. It has been previously postulated that digestive enzymes account for the majority of digestion because hagfish are agastric with notable zymogen granules in specialized cells of the hindgut. While the presence of some digestive enzymes (amylase, lipase and leucinaminopeptidase) have been confirmed with histochemistry, quantification of enzymatic activity is limited. This study sought to biochemically quantify the tissue activity of six digestive enzymes (α-amylase, maltase, lipase, trypsin, aminopeptidase and alkaline phosphatase) along the length of the Pacific hagfish ( Eptatretus stoutii ) alimentary canal. In addition, the effect of feeding on the rate of enzyme activity was examined. Overall, maltase and trypsin activities were unchanging with respect to location or feeding status, while the activities of α-amylase and alkaline phosphatase decreased substantially following feeding, but were consistent along the length. Lipase and aminopeptidase activities were elevated in the anterior region of the alimentary canal in comparison to the more posterior regions, but were not altered with feeding. This study indicates hagfish have an assortment of digestive enzymes that likely are the result of a varied diet. The differential expression of these enzymes along the tract and in regards to feeding may be indications of early compartmentalization of digestive function.

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“…A sigmoidal relationship (Equation (1)) was the best fit ( R 2 = 0.9163), but a similar fit was obtained when modelled using Michaelis–Menten kinetics (Equation (2); R 2 = 0.9159). The sigmoidal uptake pattern is characteristic of other nutrient transport processes in hagfishes and has been explained by the presence of allosteric modulators ( e.g ., sodium, or protons) affecting transporter function (Glover et al ., ; Weinrauch et al ., ). Alternatively, the sigmoidal curve could reflect the effects of mucous binding, wherein at low dipeptide concentrations, the mucous layer covering the gut binds to and effectively limits the bioavailability of the substrate.…”

Section: Discussionmentioning

confidence: 97%

“…The straight, uncoiled hindgut is quite distinct with zig‐zag folds that are retained during intestinal distention. Digestion is accomplished using zymogen granules, released from distinct cells of the hindgut and absorption occurs across the apical brush border of the columnar cells (Adam, ; Weinrauch et al ., , ,c). The morphological data suggest hagfishes have a hindgut lacking regional functional specialisation, that would permit maximal nutrient uptake following a binge.…”

Section: Discussionmentioning

confidence: 99%

“…The rate of L ‐ala‐ala uptake was unaltered along the length of the hindgut. This feature is characteristic of hagfish intestinal nutrient uptake (Glover et al ., ; Schultz et al ., ; Weinrauch et al ., , ) and could conceivably be the result of both feeding behaviour and intestinal morphology. Hagfishes obtain food episodically through both active predation (Zintzen et al ., ) and opportunistic scavenging (Martini, ).…”

Section: Discussionmentioning

confidence: 99%

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Acquisition of alanyl‐alanine in an Agnathan: Characteristics of dipeptide transport across the hindgut of the Pacific hagfish Eptatretus stoutii

Weinrauch

Blewett

Glover

et al. 2019

Journal of Fish Biology

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This study used 3 H-L -alanyl-L -alanine to demonstrate dipeptide uptake using in vitro gut sacs prepared from the hindgut of the Pacific hagfish Eptatretus stoutii.Concentration-dependent kinetic analysis resulted in a sigmoidal distribution with a maximal (± SE) uptake rate (J max -like) of 70 ± 3 nmol cm −2 h −1 and an affinity constant (K m -like) of 1072 ± 81 μM. Addition of high alanine concentrations to transport assays did not change dipeptide transport rates, indicating that hydrolysis of the dipeptide in mucosal solutions and subsequent uptake via apical amino acid transporters was not occurring, which was further supported by a K m distinct from that of amino acid transport. Transport occurred independent of mucosal pH, but uptake was reduced by 42% in low mucosal sodium. This may implicate cooperation between peptide transporters and sodium-proton exchangers, previously demonstrated in several mammalian and teleost species. Finally, apical L -alanyl-L -alanine uptake rates (i.e., mucosal disappearance) were significantly increased following a meal, demonstrating regulation of uptake. Overall, this examination of dipeptide acquisition in the earliest extant Agnathan suggests evolutionarily conserved mechanisms of transport between hagfish and later-diverging vertebrates such as teleosts and mammals.

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Lipid acquisition and tissue storage in hagfish: new insights from an ancient vertebrate

Cited by 9 publications

References 58 publications

The good, the bad and the slimy: experimental studies of hagfish digestive and nutritional physiology

The good, the bad and the slimy: experimental studies of hagfish digestive and nutritional physiology

Activity and post-prandial regulation of digestive enzyme activity along the Pacific hagfish (Eptatretus stoutii) alimentary canal

Acquisition of alanyl‐alanine in an Agnathan: Characteristics of dipeptide transport across the hindgut of the Pacific hagfish Eptatretus stoutii

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