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Sustained endocrine and exocrine function in the pancreas of the Pacific spiny dogfish post-feeding

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Abstract

Secretions of the exocrine pancreas contain digestive enzymes integral to the digestive process. The Pacific spiny dogfish (Squalus suckleyi) has a discrete pancreas, divided into two lobes termed the dorsal and ventral lobes. These lobes drain into the anterior intestine via a common duct to enable digestion. Previous studies have identified that the exocrine pancreas produces (co)lipases, chymotrypsin, carboxypeptidase, and low levels of chitinases; however, investigations into other digestive enzymes are limited. We detect the presence of lipase, trypsin, and carbohydrase and show that activities are equivalent between both lobes of the pancreas. Additionally, we sought to investigate the influence of a single feeding event (2% body weight ration of herring by gavage) on enzyme activities over an extended time course (0, 20, 48, 72, 168 h) post-feeding. The results indicate that there are no differences in pancreatic tissue digestive enzyme activities between fed or fasted states. Analysis of acinar cell circumference post-feeding demonstrates a significant increase at 20 and 48 h, that returns to fasting levels by 72 h. No significant changes were observed regarding whole-tissue insulin or glucagon mRNA abundance or with glucose transporter (glut) 1 or 3. Yet, a significant and transient decrease in glut4 and sodium glucose-linked transporter mRNA abundance was found at 48 h post-feeding. We propose that the constant enzyme activity across this relatively large organ, in combination with a relatively slow rate of digestion leads to an evenly distributed, sustained release of digestive enzymes regardless of digestive state.

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Data availability

The datasets generated for the current study are available in Mendeley data repository. https://doi.org/10.17632/8d6wvt6cnc.1

Code availability

Not applicable.

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Acknowledgements

The authors thank the Bamfield Marine Science Centre staff for helpful assistance with particular thanks to Dr. Eric Clelland and Tao Eastham. Additional thanks to Jess MacPherson, Alexandra Schoen, and Dr. Ikechukwu Isinguzo for dogfish collection and/or technical assistance. This work was supported by an NSERC Discovery Grant (05348-15) to WGA. AMW is supported by a NSERC PDF. The authors acknowledge that the Bamfield Marine Sciences Centre sits within the traditional territory of the Huu-ay-aht First Nations and the University of Manitoba campuses are located on the original lands of the Anishinaabeg, Cree, Oji-Cree, Dakota, and Dene peoples, and on the homeland of the Métis Nation.

Funding

Funding was provided by the University of Manitoba Faculty of Science Fieldwork support program and a Natural Science and Engineering Research Council of Canada (NSERC), discovery grant (#05348–15) to WGA. AMW holds a NSERC-PDF.

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Authors and Affiliations

  1. Department of Biological Sciences, University of Manitoba, Winnipeg, MB, R3T 2N2, Canada

    Alyssa M. Weinrauch, Frauke Fehrmann & W. Gary Anderson

  2. Bamfield Marine Sciences Centre, Bamfield, BC, V0R 1B0, Canada

    Alyssa M. Weinrauch & W. Gary Anderson

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  1. Alyssa M. Weinrauch
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  2. Frauke Fehrmann
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  3. W. Gary Anderson
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Contributions

AMW and WGA contributed to the study conception and design. AMW performed the feedings and tissue collection, conducted the enzymatic assays, qPCR, microscopy, analyzed the data, and wrote the first draft of the manuscript. FF performed the RACE experiment to obtain the full-length dogfish pre-proinsulin. WGA supervised and funded the project. All authors edited, read, and approved the final manuscript.

Corresponding author

Correspondence to Alyssa M. Weinrauch.

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Collection permits were granted by the Department of Fisheries and Oceans Canada (XR99 2019) while all experiments were approved by the BMSC animal care committee (RS-19–03) under the guidelines of the Canadian Council for Animal Care.

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Weinrauch, A.M., Fehrmann, F. & Anderson, W.G. Sustained endocrine and exocrine function in the pancreas of the Pacific spiny dogfish post-feeding. Fish Physiol Biochem 48, 645–657 (2022). https://doi.org/10.1007/s10695-022-01070-8

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