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The Changes in Adenine Nucleotides Measured in Glucose-stimulated Rodent Islets Occur in β Cells but Not in α Cells and Are Also Observed in Human Islets
Open accessAbstract
Glucose metabolism by pancreatic beta and alpha cells is essential for stimulation of insulin secretion and inhibition of glucagon secretion. Studies using rodent islets have suggested that the ATP/ADP ratio serves as second messenger in beta cells. This study compared the effects of glucose on glucose oxidation ([U-14C]glucose) and adenine nucleotides (luminometric method) in purified rat alpha and beta cells. The rate of glucose oxidation at 1 mM glucose was higher in beta than alpha cells (4.5-fold, i.e. approximately 2-fold after normalization for cell size). It was more strongly stimulated by 10 mM glucose in beta cells (9-fold) than in alpha cells (5-fold). At 1 mM glucose, ATP levels were similar in both cell types, which corresponds to an approximately 2-fold higher concentration in alpha cells ( approximately 6.5 mM) than in beta cells ( approximately 3 mM). In beta cells, glucose dose-dependently increased ATP and decreased ADP levels, causing a rise in the ATP/ADP ratio from 2.4 to 11.6 at 1 and 10 mM, respectively. In alpha cells, glucose did not affect ATP and ADP levels, and the ATP/ADP ratio remained stable around 7.5. In human islets, the ATP/ADP ratio progressively increased between 1 and 10 mM glucose. In duct cells, which often contaminate human islet preparations, an increase in the ATP/ADP ratio sometimes occurred between 1 and 3 mM glucose. In conclusion, the present observations establish that the regulation of glucagon secretion by glucose does not involve changes in alpha cell adenine nucleotides and further support the role of the ATP/ADP ratio in the control of insulin secretion.
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“These values are in broad agreement with biochemical measurements of [ATP]i in purified rat β-cells which suggest ATP is ~2 mM under basal conditions and rises to 4 mM when glucose is increased to 10 mM (142) (see v).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [142]
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BackgroundSelf-citationNucleotide Sensitivity of Pancreatic ATP-Sensitive Potassium Channels and Type 2 Diabetes
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Glucose-dependent docking and SNARE protein-mediated exocytosis in mouse pancreatic alpha-cell
Andersson, S. A., Pedersen, M. G., Vikman, J., & Eliasson, L. (2011) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-011-0979-5 · Cited by 46
“Escalating glucose concentrations results in a concentration-dependent acceleration of glucose metabolism in both alpha- and beta-cells [8].”
Modeling the pancreatic α-cell: dual mechanisms of glucose suppression of glucagon secretion
Watts, M., & Sherman, A. (2014) · Biophysical Journal · doi:10.1016/j.bpj.2013.11.4504 · Cited by 45
“Some studies report no change (23,36), but others show an increase in ATP with glucose (6,37,38).”
BackgroundA pathway model of glucose-stimulated insulin secretion in the pancreatic β-cell
Maheshvare, M. D., Raha, S., König, M., & Pal, D. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1185656 · Cited by 56
“Detimary, 1998 (55) 9852040 ATP, ADP, ATP+ADP, ATP/ADP Wistar rats”
Fast and cAMP-Sensitive Mode of Ca2+-Dependent Exocytosis in Pancreatic β-Cells
Kasai, H., Suzuki, T., Liu, T., Kishimoto, T. E., & Takahashi, N. K. (2002) · Diabetes · doi:10.2337/diabetes.51.2007.s19 · Cited by 44
Physiological characterization of the human EndoC-βH1 β-cell line
Gurgul-Convey, E., Kaminski, M. T., & Lenzen, S. (2015) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2015.05.072 · Cited by 39
Mitochondrial metabolism and dynamics in pancreatic beta cell glucose sensing
Rutter, G. A., Sidarala, V., Kaufman, B. A., & Soleimanpour, S. A. (2023) · Biochemical Journal · doi:10.1042/bcj20230167 · Cited by 41
Quantal ATP release in rat β-cells by exocytosis of insulin-containing LDCVs
Karanauskaite, J., Hoppa, M. B., Braun, M., Galvanovskis, J., & Rorsman, P. (2008) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-008-0610-6 · Cited by 37
“Pancreatic β-cells contain 4 fmol of ATP per cell [22] of which 30% is stored in the ∼10,000 insulincontaining secretory granules [14].”
BackgroundSaito, T., Okada, S., Yamada, E., Ohshima, K., Shimizu, H., Shimomura, K., Sato, M., Pessin, J. E., & Mori, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m305114200 · Cited by 37
Zaborska, K. E., Dadi, P. K., Dickerson, M. T., Nakhe, A. Y., Thorson, A. S., Schaub, C. M., Graff, S. M., Stanley, J. E., Kondapavuluru, R. S., Denton, J. S., et al. (2020) · Molecular Metabolism · doi:10.1016/j.molmet.2020.101056 · Cited by 33
“However, glucose-induced ATP production in a-cells is significantly lower than in b-cells [34,69] and the ATP/ADP ratio is much higher in a-cells compared to b-cells under low-glucose conditions [15].”
BackgroundDoliba, N. M., Wehrli, S. L., Vatamaniuk, M. Z., Qin, W. D., Buettger, C. W., Collins, H. W., & Matschinsky, F. M. (2007) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00282.2006 · Cited by 37
“Measurements of intracellular ATP concentration ([ATP]i) in purified rat -cells suggest that [ATP]i is 2 mmol/l (2 pmol/10(3) cells) in the absence of glucose and increases to 4 mmol/l cells ( 4 pmol/10(3) cells) when glucose is raised to 10 mmol/l (8).”
BackgroundRavier, M. A., Eto, K., Jonkers, F. C., Nenquin, M., Kadowaki, T., & Henquin, J. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.275.3.1587 · Cited by 35
Self-citationCharacterization of Islet Preparations
Colton, C. K., Papas, K. K., Pisania, A., Rappel, M. J., Powers, D. E., O’Neil, J. J., Omer, A., Weir, G. C., & Bonner‐Weir, S. (2007) · Elsevier eBooks · doi:10.1016/b978-012369415-7/50007-7 · Cited by 35
Leucine Culture Reveals That ATP Synthase Functions as a Fuel Sensor in Pancreatic β-Cells
Yang, J., Wong, R., Wang, X., Moibi, J. A., Hessner, M. J., Greene, S. R., Wu, J., Sukumvanich, S. S., Wolf, B. A., & Gao, Z. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405309200 · Cited by 35
Aggarwal, S., Giri, S., Ribnicky, D., Burk, D. H., Karki, N., & Wang, M. S. Q. (2015) · Journal of Ethnopharmacology · doi:10.1016/j.jep.2015.05.003 · Cited by 36
“Further, since β cells have glucose-sensing property, the glucose–induced changes in energy state of β cells and are associated with insulin release (Detimary et al., 1998; Detimary et al., 1995).”
The Shifting Landscape of KAtpChannelopathies and the Need for ‘Sharper’ Therapeutics
Kharade, S. V., Nichols, C. G., & Denton, J. S. (2016) · Future Medicinal Chemistry · doi:10.4155/fmc-2016-0005 · Cited by 34
Grubelnik, V., Markovič, R., Lipovšek, S., Leitinger, G., Gosak, M., Dolenšek, J., Valladolid-Acebes, I., Berggren, P.-O., Stožer, A., Perc, M., et al. (2020) · Royal Society Open Science · doi:10.1098/rsos.191171 · Cited by 32
“Additionally, the values of JGPDH are comparable with experimentally measured values at 1 and 10 mM glucose [34,36].”
BackgroundMethodContribution of Mitochondria to Insulin Secretion by Various Secretagogues
Ježek, P., Holendová, B., Jabůrek, M., Dlasková, A., & Plecitá‐Hlavatá, L. (2021) · Antioxidants and Redox Signaling · doi:10.1089/ars.2021.0113 · Cited by 33
“With isolated rat PIs, elevations from resting 2 mM up to insulin-stimulating 4 mM [ATP] (at 10 mM [glucose]) were found (43), while AC50 at *3 mM was reported for the total ATP rise and 50% KATP closure in mouse PIs, not correlating with AC50 of*12 mM for GSIS (210).”
MethodAn adenylate kinase is involved in KATP channel regulation of mouse pancreatic beta cells
Schulze, D., Düfer, M., Wieringa, B., Krippeit‐Drews, P., & Drews, G. (2007) · Diabetologia · doi:10.1007/s00125-007-0742-9 · Cited by 32
“The bulk ATP concentration in beta cells ranges between 3 and 5 mmol/l at high glucose concentration [1–3].”
BackgroundEffects of Glucose and Amino Acids on Free ADP in βHC9 Insulin-Secreting Cells
Ronner, P., Naumann, C. M., & Friel, E. (2001) · Diabetes · doi:10.2337/diabetes.50.2.291 · Cited by 32
Metabolic regulation of glucagon secretion
Armour, S. L., Stanley, J. E., Cantley, J., Dean, E. D., & Knudsen, J. G. (2023) · Journal of Endocrinology · doi:10.1530/joe-23-0081 · Cited by 41
Anello, M., Spampinato, D., Piro, S., Purrello, F., & Rabuazzo, A. M. (2004) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00320.2003 · Cited by 31
“In particular, the increase of the ATP-to-ADP (ATP/ADP) ratio tightly associates to glucose-induced insulin granules release (1, 6, 7).”
BackgroundDiderichsen, P. M., & Göpel, S. (2006) · Journal of Biological Physics · doi:10.1007/s10867-006-9013-0 · Cited by 30
“Studies on dispersed α-cells indicate that the ATP/ADP ratio remains unaffected by glucose [9].”
Piro, S., Rabuazzo, A. M., Renis, M., & Purrello, F. (2012) · PubMed · doi:10.3275/7866 · Cited by 29
Phosphocreatine as a determinant of KATP channel activity in pancreatic β-cells
Krippeit‐Drews, P., Bäcker, M., Düfer, M., & Drews, G. (2003) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-002-0975-x · Cited by 29
“The ATP concentration in the b-cell is estimated to be high in the range of 3 to 5 mM [3, 9].”
BackgroundLu, Y., Xu, J., Li, Y., Wang, R., Dai, C., Zhang, B., Zhang, X., Xu, L., Tao, Y., Han, M., et al. (2024) · Science Translational Medicine · doi:10.1126/scitranslmed.ade8647 · Cited by 29
Intercellular Communication in the Islet of Langerhans in Health and Disease
Ng, X. W., Chung, Y. H., & Piston, D. W. (2021) · Comprehensive physiology · doi:10.1002/cphy.c200026 · Cited by 39
“Another study indicates that not only is [ATP] twofold higher (6.5 mM) in α -cells than in β -cells but also that the [ATP]/[ADP] ratio in α -cells does not change following increase in glucose from 1 to 10 mM (85).”
InfluentialSpégel, P., Andersson, L. E., Storm, P., Sharoyko, V. V., Göhring, I., Rosengren, A. H., & Mulder, H. (2015) · Endocrinology · doi:10.1210/en.2014-1391 · Cited by 25
“Notably, the coupling of cytosolic and mitochondrial metabolism has been shown to be much less efficient in the than in the -cell (35, 36).”
BackgroundAnello, M., Ucciardello, V., Piro, S., Patanè, G., Frittitta, L., Calabrese, V., Stella, A. M. G., Vigneri, R., Purrello, F., & Rabuazzo, A. M. (2001) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.2001.281.5.e1082 · Cited by 25
“Because ADP may antagonize the effect of ATP on KATP 1 channels (24), and the ATP-to-ADP ratio plays a critical role and tightly regulates glucose-induced insulin release in both rodent (8) and human islets (7), these alterations may be the cause of the reduced insulin secretion in islets chronically exposed to high l…”
BackgroundChapter 17 Glucose, Regulator of Survival and Phenotype of Pancreatic Beta Cells
Martens, G. A., & PIPELEERS, D. G. (2009) · Vitamins and hormones · doi:10.1016/s0083-6729(08)00617-1 · Cited by 25
Self-citation
Metadata
- Authors
- Detimary, P., Dejonghe, S., Ling, Z., Pipeleers, D., Schuit, F., & Henquin, J.-C.
- Affiliations
- UCLouvain (BE)
- Vrije Universiteit Brussel (BE)
- Corresponding author
- Henquin, Jean-Claude
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 1998-12
- Volume
- 273
- Issue
- 51
- Pages
- 33905-33908
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2023149007
- Cited by
- 159
- References
- 38
- Citations by year
- 2026: 1 · 2024: 4 · 2023: 8 · 2022: 2 · 2021: 7 · 2020: 3 · 2019: 4 · 2018: 3 · 2017: 1 · 2016: 3 · 2015: 9 · 2014: 13 · 2013: 8 · 2012: 6
- FWCI
- 4.45
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DIAL (Catholic University of Leuven) (submittedVersion)
- Funders
- Fédération Wallonie-Bruxelles
- Vlaamse regering
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Keywords
- adenine nucleotides, ATP/ADP ratio, pancreatic beta cells, alpha cells, glucose oxidation, insulin secretion, glucagon secretion, second messengers, human islets, duct cells
- MeSH terms
- Adenosine Diphosphate, Adenosine Triphosphate, Adult, Animals, Cells, Cultured, Glucose, Glycolysis, Humans, Islets of Langerhans, Kinetics, Male, Middle Aged, Species Specificity, Rats, Wistar, Rats
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