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©The Author(s) 2024. Published by Baishideng Publishing Group Inc. All rights reserved.
Amylase intrapancreatic infusion delays insulin release during an intravenous glucose tolerance test, proof of acini–islet–acinar interactions
Kateryna Pierzynowska, Piotr Wychowański, Kamil Zaworski, Jarosław Woliński, Janine Donaldson, Dominika Szkopek, Katarzyna Roszkowicz-Ostrowska, Agata Kondej, Stefan G Pierzynowski
Kateryna Pierzynowska, Stefan G Pierzynowski, Department of Biology, Lund University, Lund 22362, Sweden
Kateryna Pierzynowska, Kamil Zaworski, Katarzyna Roszkowicz-Ostrowska, Department of Animal Physiology, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jabłonna 05110, Poland
Kateryna Pierzynowska, Janine Donaldson, Stefan G Pierzynowski, Anara AB, Trelleborg 23132, Sweden
Piotr Wychowański, Department of Head and Neck and Sensory Organs, Division of Oral Surgery and Implantology, Institute of Clinical Dentistry, Gemelli Foundation for the University Policlinic, Catholic University of the “Sacred Heart”, Rome 00168, Italy
Piotr Wychowański, Department of Oral Surgery, Medical University of Gdańsk, Gdańsk 80211, Poland
Jarosław Woliński, Dominika Szkopek, Agata Kondej, Laboratory of Large Animal Models, The Kielanowski Institute of Animal Physiology and Nutrition, Polish Academy of Sciences, Jabłonna 05110, Poland
Janine Donaldson, School of Physiology, Faculty of Health Sciences, University of the Witwatersrand (WITS), Johannesburg 2050, South Africa
Stefan G Pierzynowski, Department of Medical Biology, Institute of Rural Health, Lublin 20090, Poland
Co-corresponding authors: Kateryna Pierzynowska and Piotr Wychowański.
Author contributions: Wychowanski P, Pierzynowska K, and Pierzynowski S for conceptualization; Pierzynowska K and Zaworski K for data curation, formal analysis; Wychowanski P, Pierzynowski SG, and Pierzynowska K for funding acquisition; Pierzynowska K, Wychowanski P, Zaworski K, Woliński J, Szkopek D, Roszkowicz K, Kondej A, and Pierzynowski S for investigation; Pierzynowska K, Zaworski K and Wychowanski P for methodology; Woliński J for project administration; Donaldson J, Roszkowicz-Ostrowska K for resource.
Institutional review board statement: The National Science Centre (Poland) has approved the protocol of current study.
Institutional animal care and use committee statement: The animal study protocol was approved by the Second Local Ethics Committee for Animal Experimentation in Warsaw, Poland (approval No. WAW2/025/2022). The protocol was designed to minimize pain or discomfort to the animals.
Conflict-of-interest statement: The authors of this manuscript have the following competing interests: Stefan Pierzynowski and Kateryna Pierzynowska are the owners of Anara AB, Sweden. Piotr Wychowański is the owner of MED Sp. z o.o., Poland. Stefan Pierzynowski is the owner of Vitanano Sp. z o.o., Poland. Kamil Zaworski received funding from National Science Centre, Poland (Preludium, 2021/41/N/NZ9/01722). All other authors declare no competing interests.
Data sharing statement: Data is contained within the article. No additional data are available.
ARRIVE guidelines statement: The authors have read the ARRIVE guidelines, and the manuscript was prepared and revised according to the ARRIVE guidelines.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See:
https://creativecommons.org/Licenses/by-nc/4.0/ Corresponding author: Kateryna Pierzynowska, DSc, PhD, Associate Professor, Senior Research Fellow, Department of Biology, Lund University, Sölvegatan 35, Lund 22362, Sweden.
kateryna.pierzynowska@biol.lu.se
Received: January 31, 2024
Revised: June 19, 2024
Accepted: July 10, 2024
Published online: September 20, 2024
Processing time: 210 Days and 14.6 Hours
BACKGROUND
The possible existence of an acini–islet–acinar (AIA) reflex, involving mutual amylase and insulin interactions, was investigated in the current acute experiment on pigs.
AIM
To confirm the existence of an AIA reflex and justify the placement of the exocrine and endocrine pancreatic components within the same organ.
METHODS
The study was performed on six pigs under general anesthesia. An intravenous glucose tolerance test was performed, with a bolus infusion of 50% glucose to the jugular vein, while amylase (5000 U/kg) or vehicle intrapancreatic infusions were administered via the pancreaticoduodenalis cranialis artery during 30 min with a 1 mL/min flow rate.
RESULTS
The amylase infusion to pancreatic arterial circulation inhibited and delayed the insulin release peak which is usually associated with the highest value of blood glucose and is typically observed at 15 min after glucose infusion, for > 1 h. The intrapancreatic infusion of the vehicle (saline) did not have any effect on the time frame of insulin release. Infusion of 1% bovine serum albumin changed the insulin release curve dramatically and prolonged the high range of insulin secretion, far beyond the glucose peak.
CONCLUSION
Intrapancreatic arterial infusion of amylase interrupted the integrated glucose–insulin interactions. This confirms an AIA reflex and justifies placement of the exocrine and endocrine pancreatic components within the same organ.
Core tip: The acini–islet–acinar axis involves the inhibition of insulin production by amylase and the stimulation of amylase release by insulin, which is of particular importance with regards to glucose regulation. There is increasing evidence that amylase levels correspond to overall metabolic health, with low amylase levels being significantly associated with the development of metabolic syndrome, diabetes, and obesity. Disruption of the integrated glucose–insulin interactions by intrapancreatic arterial amylase infusion in the present study confirms the existence of an AIA reflex and justifies placement of the exocrine and endocrine pancreatic components within the same organ.
