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J Biol Chem, Vol. 274, Issue 20, 14112-14121, May 14, 1999
From the Section of Islet Transplantation and Cell Biology, Joslin
Diabetes Center, Boston, Massachusetts 02215
Differentiated pancreatic
Chronic Hyperglycemia Triggers Loss of Pancreatic
Cell
Differentiation in an Animal Model of Diabetes
cells are unique in
their ability to secrete insulin in response to a rise in plasma
glucose. We have proposed that the unique constellation of genes they
express may be lost in diabetes due to the deleterious effect of
chronic hyperglycemia. To test this hypothesis, Sprague-Dawley rats
were submitted to a 85-95% pancreatectomy or sham pancreatectomy. One week later, the animals developed mild to severe chronic hyperglycemia that was stable for the next 3 weeks, without significant alteration of
plasma nonesterified fatty acid levels. Expression of many genes
important for glucose-induced insulin release decreased progressively
with increasing hyperglycemia, in parallel with a reduction of several
islet transcription factors involved in cell development and
differentiation. In contrast, genes barely expressed in sham islets
(lactate dehydrogenase A and hexokinase I) were markedly increased, in
parallel with an increase in the transcription factor c-Myc, a
potent stimulator of cell growth. These abnormalities were accompanied
by cell hypertrophy. Changes in gene expression were fully
developed 2 weeks after pancreatectomy. Correction of blood glucose by
phlorizin for the next 2 weeks normalized islet gene expression and cell volume without affecting plasma nonesterified fatty acid levels,
strongly suggesting that hyperglycemia triggers these abnormalities. In
conclusion, chronic hyperglycemia leads to cell hypertrophy and
loss of cell differentiation that is correlated with changes in
c-Myc and other key transcription factors. A similar change in
cell differentiation could contribute to the profound derangement
of insulin secretion in human diabetes.
Copyright © 1999 by The American Society for Biochemistry and Molecular Biology, Inc.
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H. Y. Gaisano, C.-G. Ostenson, L. Sheu, M. B. Wheeler, and S. Efendic Abnormal Expression of Pancreatic Islet Exocytotic Soluble N-Ethylmaleimide-Sensitive Factor Attachment Protein Receptors in Goto-Kakizaki Rats Is Partially Restored by Phlorizin Treatment and Accentuated by High Glucose Treatment Endocrinology, November 1, 2002; 143(11): 4218 - 4226. [Abstract] [Full Text] [PDF]
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A. Arredouani, Y. Guiot, J.-C. Jonas, L. H. Liu, M. Nenquin, J. A. Pertusa, J. Rahier, J.-F. Rolland, G. E. Shull, M. Stevens, et al. SERCA3 Ablation Does Not Impair Insulin Secretion but Suggests Distinct Roles of Different Sarcoendoplasmic Reticulum Ca2+ Pumps for Ca2+ Homeostasis in Pancreatic {beta}-cells Diabetes, November 1, 2002; 51(11): 3245 - 3253. [Abstract] [Full Text] [PDF]
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S. Srinivasan, E. Bernal-Mizrachi, M. Ohsugi, and M. A. Permutt Glucose promotes pancreatic islet beta -cell survival through a PI 3-kinase/Akt-signaling pathway Am J Physiol Endocrinol Metab, October 1, 2002; 283(4): E784 - E793. [Abstract] [Full Text] [PDF]
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H. Kaneto, G. Xu, N. Fujii, S. Kim, S. Bonner-Weir, and G. C. Weir Involvement of c-Jun N-terminal Kinase in Oxidative Stress-mediated Suppression of Insulin Gene Expression J. Biol. Chem., August 9, 2002; 277(33): 30010 - 30018. [Abstract] [Full Text] [PDF]
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J. A.G. Pertusa, R. Nesher, N. Kaiser, E. Cerasi, J.-C. Henquin, and J.-C. Jonas Increased Glucose Sensitivity of Stimulus-Secretion Coupling in Islets From Psammomys obesus After Diet Induction of Diabetes Diabetes, August 1, 2002; 51(8): 2552 - 2560. [Abstract] [Full Text] [PDF]
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I. Quesada, J. M. Rovira, F. Martin, E. Roche, A. Nadal, and B. Soria Nuclear KATP channels trigger nuclear Ca2+ transients that modulate nuclear function PNAS, July 9, 2002; 99(14): 9544 - 9549. [Abstract] [Full Text] [PDF]
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 C. Demeterco, P. Itkin-Ansari, B. Tyrberg, L. P. Ford, R. A. Jarvis, and F. Levine c-Myc Controls Proliferation Versus Differentiation in Human Pancreatic Endocrine Cells J. Clin. Endocrinol. Metab., July 1, 2002; 87(7): 3475 - 3485. [Abstract] [Full Text] [PDF]
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D. R. Laybutt, G. C. Weir, H. Kaneto, J. Lebet, R. D. Palmiter, A. Sharma, and S. Bonner-Weir Overexpression of c-Myc in {beta}-Cells of Transgenic Mice Causes Proliferation and Apoptosis, Downregulation of Insulin Gene Expression, and Diabetes Diabetes, June 1, 2002; 51(6): 1793 - 1804. [Abstract] [Full Text] [PDF]
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M. Olbrot, J. Rud, L. G. Moss, and A. Sharma Identification of beta -cell-specific insulin gene transcription factor RIPE3b1 as mammalian MafA PNAS, May 14, 2002; 99(10): 6737 - 6742. [Abstract] [Full Text] [PDF]
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 D. S. Ludwig The Glycemic Index: Physiological Mechanisms Relating to Obesity, Diabetes, and Cardiovascular Disease JAMA, May 8, 2002; 287(18): 2414 - 2423. [Abstract] [Full Text] [PDF]
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J. Boloker, S. J. Gertz, and R. A. Simmons Gestational Diabetes Leads to the Development of Diabetes in Adulthood in the Rat Diabetes, May 1, 2002; 51(5): 1499 - 1506. [Abstract] [Full Text] [PDF]
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H. Kaneto, A. Sharma, K. Suzuma, D. R. Laybutt, G. Xu, S. Bonner-Weir, and G. C. Weir Induction of c-Myc Expression Suppresses Insulin Gene Transcription by Inhibiting NeuroD/BETA2-mediated Transcriptional Activation J. Biol. Chem., April 5, 2002; 277(15): 12998 - 13006. [Abstract] [Full Text] [PDF]
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A. K. Busch, D. Cordery, G. S. Denyer, and T. J. Biden Expression Profiling of Palmitate- and Oleate-Regulated Genes Provides Novel Insights Into the Effects of Chronic Lipid Exposure on Pancreatic {beta}-Cell Function Diabetes, April 1, 2002; 51(4): 977 - 987. [Abstract] [Full Text] [PDF]
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D. R. Laybutt, A. Sharma, D. C. Sgroi, J. Gaudet, S. Bonner-Weir, and G. C. Weir Genetic Regulation of Metabolic Pathways in beta -Cells Disrupted by Hyperglycemia J. Biol. Chem., March 22, 2002; 277(13): 10912 - 10921. [Abstract] [Full Text] [PDF]
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V. Poitout and R. P. Robertson Minireview: Secondary {beta}-Cell Failure in Type 2 Diabetes--A Convergence of Glucotoxicity and Lipotoxicity Endocrinology, February 1, 2002; 143(2): 339 - 342. [Abstract] [Full Text] [PDF]
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D. R. Laybutt, H. Kaneto, W. Hasenkamp, S. Grey, J.-C. Jonas, D. C. Sgroi, A. Groff, C. Ferran, S. Bonner-Weir, A. Sharma, et al. Increased Expression of Antioxidant and Antiapoptotic Genes in Islets That May Contribute to {beta}-Cell Survival During Chronic Hyperglycemia Diabetes, February 1, 2002; 51(2): 413 - 423. [Abstract] [Full Text] [PDF]
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J. S. Harmon, C. E. Gleason, Y. Tanaka, V. Poitout, and R. P. Robertson Antecedent Hyperglycemia, Not Hyperlipidemia, Is Associated With Increased Islet Triacylglycerol Content and Decreased Insulin Gene mRNA Level in Zucker Diabetic Fatty Rats Diabetes, November 1, 2001; 50(11): 2481 - 2486. [Abstract] [Full Text] [PDF]
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C. Tourrel, D. Bailbe, M.-J. Meile, M. Kergoat, and B. Portha Glucagon-Like Peptide-1 and Exendin-4 Stimulate {beta}-Cell Neogenesis in Streptozotocin-Treated Newborn Rats Resulting in Persistently Improved Glucose Homeostasis at Adult Age Diabetes, July 1, 2001; 50(7): 1562 - 1570. [Abstract] [Full Text] [PDF]
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N. Spravchikov, G. Sizyakov, M. Gartsbein, D. Accili, T. Tennenbaum, and E. Wertheimer Glucose Effects on Skin Keratinocytes: Implications for Diabetes Skin Complications Diabetes, July 1, 2001; 50(7): 1627 - 1635. [Abstract] [Full Text] [PDF]
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M. Federici, M. Hribal, L. Perego, M. Ranalli, Z. Caradonna, C. Perego, L. Usellini, R. Nano, P. Bonini, F. Bertuzzi, et al. High Glucose Causes Apoptosis in Cultured Human Pancreatic Islets of Langerhans: A Potential Role for Regulation of Specific Bcl Family Genes Toward an Apoptotic Cell Death Program Diabetes, June 1, 2001; 50(6): 1290 - 1301. [Abstract] [Full Text]
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N. Trivedi, J. Hollister-Lock, M. D. Lopez-Avalos, J. J. O’Neil, M. Keegan, S. Bonner-Weir, and G. C. Weir Increase in {beta}-Cell Mass in Transplanted Porcine Neonatal Pancreatic Cell Clusters Is Due to Proliferation of {beta}-Cells and Differentiation of Duct Cells Endocrinology, May 1, 2001; 142(5): 2115 - 2122. [Abstract] [Full Text]
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G. M. Steil, N. Trivedi, J.-C. Jonas, W. M. Hasenkamp, A. Sharma, S. Bonner-Weir, and G. C. Weir Adaptation of {beta}-cell mass to substrate oversupply: enhanced function with normal gene expression Am J Physiol Endocrinol Metab, May 1, 2001; 280(5): E788 - E796. [Abstract] [Full Text] [PDF]
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H. Hui, C. Wright, and R. Perfetti Glucagon-Like Peptide 1 Induces Differentiation of Islet Duodenal Homeobox-1-Positive Pancreatic Ductal Cells Into Insulin-Secreting Cells Diabetes, April 1, 2001; 50(4): 785 - 796. [Abstract] [Full Text]
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C. Zhao, M. C. Wilson, F. Schuit, A. P. Halestrap, and G. A. Rutter Expression and Distribution of Lactate/Monocarboxylate Transporter Isoforms in Pancreatic Islets and the Exocrine Pancreas Diabetes, February 1, 2001; 50(2): 361 - 366. [Abstract] [Full Text]
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I. Suzuma, Y. Hata, A. Clermont, F. Pokras, S. L. Rook, K. Suzuma, E. P. Feener, and L. P. Aiello Cyclic Stretch and Hypertension Induce Retinal Expression of Vascular Endothelial Growth Factor and Vascular Endothelial Growth Factor Receptor--2: Potential Mechanisms for Exacerbation of Diabetic Retinopathy by Hypertension Diabetes, February 1, 2001; 50(2): 444 - 454. [Abstract] [Full Text]
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W. Moritz, C. A. Leech, J. Ferrer, and J. F. Habener Regulated Expression of Adenosine Triphosphate-Sensitive Potassium Channel Subunits in Pancreatic {beta}-Cells Endocrinology, January 1, 2001; 142(1): 129 - 138. [Abstract] [Full Text] [PDF]
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F. C. Schuit, P. Huypens, H. Heimberg, and D. G. Pipeleers Glucose Sensing in Pancreatic {beta}-Cells: A Model for the Study of Other Glucose-Regulated Cells in Gut, Pancreas, and Hypothalamus Diabetes, January 1, 2001; 50(1): 1 - 11. [Abstract] [Full Text]
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 I. Mountian, F. Baba-Aissa, J.-C. Jonas, Humbert De Smedt, F. Wuytack, and J. B. Parys Expression of Ca2+ Transport Genes in Platelets and Endothelial Cells in Hypertension Hypertension, January 1, 2001; 37(1): 135 - 141. [Abstract] [Full Text] [PDF]
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S. Bonner-Weir Perspective: Postnatal Pancreatic {beta} Cell Growth Endocrinology, June 1, 2000; 141(6): 1926 - 1929. [Full Text] [PDF]
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S. SUSINI, G. VAN HAASTEREN, S. LI, M. PRENTKI, and W. SCHLEGEL Essentiality of intron control in the induction of c-fos by glucose and glucoincretin peptides in INS-1 {beta}-cells FASEB J, January 1, 2000; 14(1): 128 - 136. [Abstract] [Full Text]
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F. Schuit, K. Moens, H. Heimberg, and D. Pipeleers Cellular Origin of Hexokinase in Pancreatic Islets J. Biol. Chem., November 12, 1999; 274(46): 32803 - 32809. [Abstract] [Full Text] [PDF]
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R. Roduit, J. Morin, F. Masse, L. Segall, E. Roche, C. B. Newgard, F. Assimacopoulos-Jeannet, and M. Prentki Glucose Down-regulates the Expression of the Peroxisome Proliferator-activated Receptor-alpha Gene in the Pancreatic beta -Cell J. Biol. Chem., November 10, 2000; 275(46): 35799 - 35806. [Abstract] [Full Text] [PDF]
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A. E. Allen-Jennings, M. G. Hartman, G. J. Kociba, and T. Hai The Roles of ATF3 in Glucose Homeostasis. A TRANSGENIC MOUSE MODEL WITH LIVER DYSFUNCTION AND DEFECTS IN ENDOCRINE PANCREAS J. Biol. Chem., July 27, 2001; 276(31): 29507 - 29514. [Abstract] [Full Text] [PDF]
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H. Kaneto, G. Xu, K.-H. Song, K. Suzuma, S. Bonner-Weir, A. Sharma, and G. C. Weir Activation of the Hexosamine Pathway Leads to Deterioration of Pancreatic beta -Cell Function through the Induction of Oxidative Stress J. Biol. Chem., August 10, 2001; 276(33): 31099 - 31104. [Abstract] [Full Text] [PDF]
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J.-C. Jonas, D. R. Laybutt, G. M. Steil, N. Trivedi, J. G. Pertusa, M. Van de Casteele, G. C. Weir, and J.-C. Henquin High Glucose Stimulates Early Response Gene c-Myc Expression in Rat Pancreatic beta Cells J. Biol. Chem., September 14, 2001; 276(38): 35375 - 35381. [Abstract] [Full Text] [PDF]
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H. Kaneto, K. Suzuma, A. Sharma, S. Bonner-Weir, G. L. King, and G. C. Weir Involvement of Protein Kinase C beta 2 in c-myc Induction by High Glucose in Pancreatic beta -Cells J. Biol. Chem., January 25, 2002; 277(5): 3680 - 3685. [Abstract] [Full Text] [PDF]
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