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Liver glucose-6-phosphatase proteins in suckling and weaned grey seal pups: structural similarities to other mammals and relationship to nutrition, insulin signalling and metabolite levels

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Abstract

Phocid seals have been proposed as models for diabetes because they exhibit limited insulin response to glucose, high blood glucose and increasing insulin resistance when fasting. Liver glucose-6-phosphatase (G6Pase) catalyses the final step in glucose production and is central to glucose regulation in other animals. G6Pase comprises a translocase (SLC37A4) and a catalytic subunit (G6PC). G6PC and SLC37A4 expression and activity are normally regulated by nutritional state and glucostatic hormones, particularly insulin, and are elevated in diabetes. We tested the hypotheses that (1) grey seal G6PC and SLC37A4 cDNA and predicted protein sequences differ from other species’ at functional sites, (2) relative G6Pase protein abundances are lower during feeding than fasting and (3) relative G6Pase protein abundances are related to insulin, insulin receptor phosphorylation and key metabolite levels. We show that G6PC and partial SLC37A4 cDNA sequences encode proteins sharing 82–95 % identity with other mammals. Seal G6PC contained no differences in sites responsible for activity, stability or subcellular location. Several substitutions in seal SLC37A4 were predicted to be tolerated with low probability, which could affect glucose production. Suckling pups had higher relative abundance of both subunits than healthy, postweaned fasting pups. Furthermore, relative G6PC abundance was negatively related to glucose levels. These findings contrast markedly with the response of relative hepatic G6Pase abundance to feeding, fasting, insulin, insulin sensitivity and key metabolites in other animals, and highlight the need to understand the regulation of enzymes involved in glucose control in phocids if these animals are to be informative models of diabetes.

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Abbreviations

BUN:

Blood urea nitrogen

EGP:

Endogenous glucose production

ER:

Endoplasmic reticulum

FFA:

Free fatty acids

G6P:

Glucose-6-phosphate

G6Pase:

Glucose-6-phosphatase enzyme complex

G6PC:

Catalytic subunit of glucose-6-phosphatase

GC:

Glucocorticoid

INS-R:

Insulin receptor

pINS-R:

Phosphorylated insulin receptor

SLC37A4:

Translocase subunit of glucose-6-phosphatase

SIFT:

Sorting intolerant from tolerant

TM:

Transmembrane domain

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Acknowledgments

Logistical support was provided by the Sea Mammal Research Unit (SMRU), UK, Department of Fisheries and Oceans (DFO), Canada and the Canadian Coastguard. We would specifically like to thank Simon Moss at SMRU, Sam Turgeon at DFO and Sacha LeBlanc and Ian MacMillan at Mount Allison University. Scottish Natural Heritage granted SMRU the permit to collect samples on the Isle of May, Scotland. We would also like to thank Debbie Smith, Dr. David Lee, Natalie Donaher, Dr. John Hammond and Dr. Amanda Cockshutt for technical advice, Prof. Ann Burchell for access to facilities and consumables and Dr. Tyson MacCormack for helpful comments on the manuscript. This work was funded by a McCain postdoctoral fellowship at Mount Allison University, Canada (KAB), Marine Biology and Ecology Research Centre pump priming (KAB), a Natural Sciences and Engineering Research Council Discovery Grant (SC) and the Harold Crabtree Foundation (SC). We would like to thank the anonymous reviewers for their helpful input.

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This study was performed in accordance with the laws of the countries in which the work was conducted.

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The authors declare no conflicts of interest.

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Authors and Affiliations

  1. Marine Biology and Ecology Research Centre, School of Marine Science and Engineering, Plymouth University, Portland Square, Drake Circus, Plymouth, Devon, PL4 8AA, UK

    K. A. Bennett

  2. Department of Fisheries and Oceans, Maurice Lamontagne Institute, Mont Joli, QC, Canada

    M. Hammill

  3. Biology Department, Mount Allison University, 63B York St, Sackville, NB, Canada

    S. Currie

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  1. K. A. Bennett
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  2. M. Hammill
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  3. S. Currie
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Correspondence to K. A. Bennett.

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Communicated by H.V. Carey.

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Bennett, K.A., Hammill, M. & Currie, S. Liver glucose-6-phosphatase proteins in suckling and weaned grey seal pups: structural similarities to other mammals and relationship to nutrition, insulin signalling and metabolite levels. J Comp Physiol B 183, 1075–1088 (2013). https://doi.org/10.1007/s00360-013-0768-x

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