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Establishment of a Pancreatic β Cell Line That Retains Glucose-Inducible Insulin Secretion: Special Reference to Expression of Glucose Transporter Isoforms^*

Institute for Medical Genetics (J.-I.M., K.A., K.-I.Y.), Kumamoto University Medical School Kumamoto 862, Japan
Department of Geriatric Medicine (E. Y., H.I.), Osaka University Medical School Osaka 553, Japan
The Third Department of Internal Medicine (T.A., Y.S., Y.O.), Faculty of Medicine, University of Tokyo Tokyo 113, Japan

Address all correspondence to: Dr. Jun-ichi Miyazaki, Institute for Medical Genetics, Kumamoto University Medical School, Kuhonji 4-24-1, Kumamoto City, Kumamoto 862, Japan.

Abstract

Two cell lines have been established from insulinomas obtained by targeted expression of the simian virus 40 T antigen gene in transgenic mice. These cell lines, designated MIN6 and MIN7, produce insulin and T antigen and have morphological characteristics of pancreatic β cells. MIN6 cells exhibit glucose-inducible insulin secretion comparable with cultured normal mouse islet cells, whereas MIN7 cells do not. Both cell lines produce liver-type glucose transporter (GT) mRNA at high level. Brain-type GT mRNA is also present at considerable level in MIN7 cells, but is barely detectable in MIN6 cells, suggesting that exclusive expression of the liver-type GT is related to glucose-inducible insulin secretion. MIN6 cells do not express either major histocompatibility (MHC) class I or class II antigens on the cell surface. However, treatment with interferon- induces high levels of MHC class I antigens, and a combination of interferon- and tumor necrosis factor-β induces a MHC class II antigen on the cell surface. These results emphasize that the MIN6 cell line retains physiological characteristics of normal β cells. The MIN6 cell line will be especially useful to analyze the molecular mechanisms by which β cells regulate insulin secretion in response to extracellular glucose concentrations. We discuss a possible role of GT isoforms in glucose sensing by β cells. (Endocrinology 127: 126–132,1990)

Footnotes

^* This work was supported by Special Coordination Funds of the Science and Technology Agency of the Japanese Government and by Grants-in-Aid for Cancer Research from the Japanese Ministry of Education, Science and Culture, and from the Sagawa Foundation.

Received January 17, 1990.

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				K. Masur, E. C. Tibaduiza, C. Chen, B. Ligon, and M. Beinborn Basal Receptor Activation by Locally Produced Glucagon-Like Peptide-1 Contributes to Maintaining {beta}-Cell Function Mol. Endocrinol., May 1, 2005; 19(5): 1373 - 1382. [Abstract] [Full Text] [PDF]

				T. Iype, J. Francis, J. C. Garmey, J. C. Schisler, R. Nesher, G. C. Weir, T. C. Becker, C. B. Newgard, S. C. Griffen, and R. G. Mirmira Mechanism of insulin Gene Regulation by the Pancreatic Transcription Factor Pdx-1: APPLICATION OF PRE-mRNA ANALYSIS AND CHROMATIN IMMUNOPRECIPITATION TO ASSESS FORMATION OF FUNCTIONAL TRANSCRIPTIONAL COMPLEXES J. Biol. Chem., April 29, 2005; 280(17): 16798 - 16807. [Abstract] [Full Text] [PDF]

				K. Kitiphongspattana, C. E. Mathews, E. H. Leiter, and H. R. Gaskins Proteasome Inhibition Alters Glucose-stimulated (Pro)insulin Secretion and Turnover in Pancreatic {beta}-Cells J. Biol. Chem., April 22, 2005; 280(16): 15727 - 15734. [Abstract] [Full Text] [PDF]

				S. Srinivasan, M. Ohsugi, Z. Liu, S. Fatrai, E. Bernal-Mizrachi, and M. A. Permutt Endoplasmic Reticulum Stress-Induced Apoptosis Is Partly Mediated by Reduced Insulin Signaling Through Phosphatidylinositol 3-Kinase/Akt and Increased Glycogen Synthase Kinase-3{beta} in Mouse Insulinoma Cells Diabetes, April 1, 2005; 54(4): 968 - 975. [Abstract] [Full Text] [PDF]

				B. Ritz-Laser, A. Mamin, T. Brun, I. Avril, V. M. Schwitzgebel, and J. Philippe The Zinc Finger-Containing Transcription Factor Gata-4 Is Expressed in the Developing Endocrine Pancreas and Activates Glucagon Gene Expression Mol. Endocrinol., March 1, 2005; 19(3): 759 - 770. [Abstract] [Full Text] [PDF]

				M. J. Luther, E. Davies, D. Muller, M. Harrison, A. J. Bone, S. J. Persaud, and P. M. Jones Cell-to-cell contact influences proliferative marker expression and apoptosis in MIN6 cells grown in islet-like structures Am J Physiol Endocrinol Metab, March 1, 2005; 288(3): E502 - E509. [Abstract] [Full Text] [PDF]

				M. Ohsugi, C. Cras-Meneur, Y. Zhou, E. Bernal-Mizrachi, J. D. Johnson, D. S. Luciani, K. S. Polonsky, and M. A. Permutt Reduced Expression of the Insulin Receptor in Mouse Insulinoma (MIN6) Cells Reveals Multiple Roles of Insulin Signaling in Gene Expression, Proliferation, Insulin Content, and Secretion J. Biol. Chem., February 11, 2005; 280(6): 4992 - 5003. [Abstract] [Full Text] [PDF]

				S. J. Micallef, M. E. Janes, K. Knezevic, R. P. Davis, A. G. Elefanty, and E. G. Stanley Retinoic Acid Induces Pdx1-Positive Endoderm in Differentiating Mouse Embryonic Stem Cells Diabetes, February 1, 2005; 54(2): 301 - 305. [Abstract] [Full Text] [PDF]

				A. L. Mosley and S. Ozcan The Pancreatic Duodenal Homeobox-1 Protein (Pdx-1) Interacts with Histone Deacetylases Hdac-1 and Hdac-2 on Low Levels of Glucose J. Biol. Chem., December 24, 2004; 279(52): 54241 - 54247. [Abstract] [Full Text] [PDF]

				T. Tsuboi, H. T. McMahon, and G. A. Rutter Mechanisms of Dense Core Vesicle Recapture following "Kiss and Run" ("Cavicapture") Exocytosis in Insulin-secreting Cells J. Biol. Chem., November 5, 2004; 279(45): 47115 - 47124. [Abstract] [Full Text] [PDF]

				A. Varadi and G. A. Rutter Ca2+-Induced Ca2+ Release in Pancreatic Islet {beta}-Cells: Critical Evaluation of the Use of Endoplasmic Reticulum-Targeted "Cameleons" Endocrinology, October 1, 2004; 145(10): 4540 - 4549. [Abstract] [Full Text] [PDF]

				S. Iino, K. Abeyama, K.-i. Kawahara, M. Yamakuchi, T. Hashiguchi, S. Matsukita, S. Yonezawa, S. Taniguchi, M. Nakata, S. Takao, et al. The Antimetastatic Role of Thrombomodulin Expression in Islet Cell-Derived Tumors and Its Diagnostic Value Clin. Cancer Res., September 15, 2004; 10(18): 6179 - 6188. [Abstract] [Full Text] [PDF]

				A. L. Mosley, J. A. Corbett, and S. Ozcan Glucose Regulation of Insulin Gene Expression Requires the Recruitment of p300 by the {beta}-Cell-Specific Transcription Factor Pdx-1 Mol. Endocrinol., September 1, 2004; 18(9): 2279 - 2290. [Abstract] [Full Text] [PDF]

				C. Arden, A. Harbottle, S. Baltrusch, M. Tiedge, and L. Agius Glucokinase Is an Integral Component of the Insulin Granules in Glucose-Responsive Insulin Secretory Cells and Does Not Translocate During Glucose Stimulation Diabetes, September 1, 2004; 53(9): 2346 - 2352. [Abstract] [Full Text] [PDF]

				W. E. Hughes, Z. Elgundi, P. Huang, M. A. Frohman, and T. J. Biden Phospholipase D1 Regulates Secretagogue-stimulated Insulin Release in Pancreatic {beta}-Cells J. Biol. Chem., June 25, 2004; 279(26): 27534 - 27541. [Abstract] [Full Text] [PDF]

				L. Ma, V. P. Bindokas, A. Kuznetsov, C. Rhodes, L. Hays, J. M. Edwardson, K. Ueda, D. F. Steiner, and L. H. Philipson Direct imaging shows that insulin granule exocytosis occurs by complete vesicle fusion PNAS, June 22, 2004; 101(25): 9266 - 9271. [Abstract] [Full Text] [PDF]

				G. Vigliotta, C. Miele, S. Santopietro, G. Portella, A. Perfetti, M. A. Maitan, A. Cassese, F. Oriente, A. Trencia, F. Fiory, et al. Overexpression of the ped/pea-15 Gene Causes Diabetes by Impairing Glucose-Stimulated Insulin Secretion in Addition to Insulin Action Mol. Cell. Biol., June 1, 2004; 24(11): 5005 - 5015. [Abstract] [Full Text] [PDF]

				M. Ohsugi, C. Cras-Meneur, Y. Zhou, W. Warren, E. Bernal-Mizrachi, and M. A. Permutt Glucose and Insulin Treatment of Insulinoma Cells Results in Transcriptional Regulation of a Common Set of Genes Diabetes, June 1, 2004; 53(6): 1496 - 1508. [Abstract] [Full Text] [PDF]

				G. da Silva Xavier, J. Rutter, and G. A. Rutter Involvement of Per-Arnt-Sim (PAS) kinase in the stimulation of preproinsulin and pancreatic duodenum homeobox 1 gene expression by glucose PNAS, June 1, 2004; 101(22): 8319 - 8324. [Abstract] [Full Text] [PDF]

				I. Leclerc, W. W. Woltersdorf, G. da Silva Xavier, R. L. Rowe, S. E. Cross, G. S. Korbutt, R. V. Rajotte, R. Smith, and G. A. Rutter Metformin, but not leptin, regulates AMP-activated protein kinase in pancreatic islets: impact on glucose-stimulated insulin secretion Am J Physiol Endocrinol Metab, June 1, 2004; 286(6): E1023 - E1031. [Abstract] [Full Text] [PDF]

				S. Miyazaki, E. Yamato, and J.-i. Miyazaki Regulated Expression of pdx-1 Promotes In Vitro Differentiation of Insulin-Producing Cells From Embryonic Stem Cells Diabetes, April 1, 2004; 53(4): 1030 - 1037. [Abstract] [Full Text] [PDF]

				Y. Qiu, M. Guo, S. Huang, and R. Stein Acetylation of the BETA2 Transcription Factor by p300-associated Factor Is Important in Insulin Gene Expression J. Biol. Chem., March 12, 2004; 279(11): 9796 - 9802. [Abstract] [Full Text] [PDF]

				J. i. Nozaki, H. Kubota, H. Yoshida, M. Naitoh, J. Goji, T. Yoshinaga, K. Mori, A. Koizumi, and K. Nagata The endoplasmic reticulum stress response is stimulated through the continuous activation of transcription factors ATF6 and XBP1 in Ins2+/Akita pancreatic {beta} cells Genes Cells, March 1, 2004; 9(3): 261 - 270. [Abstract] [Full Text] [PDF]

				K. J. Mitchell, T. Tsuboi, and G. A. Rutter Role for Plasma Membrane-Related Ca2+-ATPase-1 (ATP2C1) in Pancreatic {beta}-Cell Ca2+ Homeostasis Revealed by RNA Silencing Diabetes, February 1, 2004; 53(2): 393 - 400. [Abstract] [Full Text]

				A. Merglen, S. Theander, B. Rubi, G. Chaffard, C. B. Wollheim, and P. Maechler Glucose Sensitivity and Metabolism-Secretion Coupling Studied during Two-Year Continuous Culture in INS-1E Insulinoma Cells Endocrinology, February 1, 2004; 145(2): 667 - 678. [Abstract] [Full Text] [PDF]

				K.-H. Park and T. Akaike Visualization of the Specific Interaction of Sulfonylurea-Incorporated Polymer with Insulinoma Cell Line MIN6 J. Biochem., February 1, 2004; 135(2): 179 - 183. [Abstract] [Full Text] [PDF]

				T. Anno, S. Uehara, H. Katagiri, Y. Ohta, K. Ueda, H. Mizuguchi, Y. Moriyama, Y. Oka, and Y. Tanizawa Overexpression of constitutively activated glutamate dehydrogenase induces insulin secretion through enhanced glutamate oxidation Am J Physiol Endocrinol Metab, February 1, 2004; 286(2): E280 - E285. [Abstract] [Full Text] [PDF]

				T. J. Biden, D. Robinson, D. Cordery, W. E. Hughes, and A. K. Busch Chronic Effects of Fatty Acids on Pancreatic {beta}-Cell Function: New Insights From Functional Genomics Diabetes, February 1, 2004; 53(90001): S159 - 165. [Abstract] [Full Text]

				T. Tsuboi, G. da Silva Xavier, I. Leclerc, and G. A. Rutter 5'-AMP-activated Protein Kinase Controls Insulin-containing Secretory Vesicle Dynamics J. Biol. Chem., December 26, 2003; 278(52): 52042 - 52051. [Abstract] [Full Text] [PDF]

				D. Martin, T. Tawadros, L. Meylan, A. Abderrahmani, D. F. Condorelli, G. Waeber, and J.-A. Haefliger Critical Role of the Transcriptional Repressor Neuron-restrictive Silencer Factor in the Specific Control of Connexin36 in Insulin-producing Cell Lines J. Biol. Chem., December 26, 2003; 278(52): 53082 - 53089. [Abstract] [Full Text] [PDF]