When less is more: The forbidden fruits of gene repression in the adult β-cell

Diabetes, Obesity and Metabolism

Volumn 15, Issue 6, 2013, Pages 503-512

  Pullen, T J ^a   Rutter, G A ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Gene profile; Insulin secretion; Type 2 diabetes; cell

Indexed keywords

CYTOCHROME C OXIDASE; GLUTATHIONE TRANSFERASE; GLYCEROL 3 PHOSPHATE DEHYDROGENASE; GROWTH ARREST SPECIFIC PROTEIN 6; LACTATE DEHYDROGENASE; MONOCARBOXYLATE TRANSPORTER 1; NUCLEAR FACTOR I; ORNITHINE OXOACID AMINOTRANSFERASE; PALMITOYL COENZYME A HYDROLASE; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; PLECTIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; RIBOSOME PROTEIN; THIOSULFATE SULFURTRANSFERASE; UNTRANSLATED RNA; ZINC FINGER PROTEIN;

AEROBIC METABOLISM; ANAEROBIC METABOLISM; CELL EXPANSION; CELL PROLIFERATION; EPIGENETICS; GENE REPRESSION; GENE SILENCING; GLUCOSE METABOLISM; HISTONE MODIFICATION; HUMAN; HYPERINSULINISM; INSULIN LIKE ACTIVITY; INSULIN RELEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; REVIEW; STIMULUS SECRETION COUPLING;

EID: 84877601932     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12029     Document Type: Review

References (84)

1. Rutter GA. Nutrient-secretion coupling in the pancreatic islet β-cell: recent advances. Mol Aspects Med 2001; 22: 247-284.
2. Rorsman P, Renstrom E. Insulin granule dynamics in pancreatic beta cells. Diabetologia 2003; 46: 1029-1045.
3. Henquin JC. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 2000; 49: 1751-1760.
4. da Silva Xavier G, Leclerc I, Salt IP et al. Role of AMP-activated protein kinase in the regulation by glucose of islet beta-cell gene expression. Proc Natl Acad Sci USA 2000; 97: 4023-4028.
5. Ohlsson H, Karlsson K, Edlund T. IPF-1, a homeodomain-containing transactivator of the insulin gene. EMBO J 1993; 12: 4251-4259.
6. Melloul D, Ben-Neriah Y, Cerasi E. Glucose modulates the binding of an islet-specific factor to a conserved sequence within the rat I and the human insulin promoters. Proc Natl Acad Sci USA 1993; 90: 3865-3869.
7. Olbrot M, Rud J, Moss LG, Sharma A. Identification of beta-cell-specific insulin gene transcription factor RIPE3b1 as mammalian MafA. Proc Natl Acad Sci USA 2002; 99: 6737-6742.
8. Naya FJ, Huang HP, Qiu Y et al. Diabetes, defective pancreatic morphogenesis, and abnormal enteroendocrine differentiation in BETA2/neuroD-deficient mice. Genes Dev 1997; 11: 2323-2334.
9. Thorens B, Sarkar HK, Kaback HR, Lodish HF. Cloning and functional expression in bacteria of a novel glucose transporter present in liver, intestine, kidney, and beta-pancreatic islet cells. Cell 1988; 55: 281-290.
10. Iynedjian PB. Mammalian glucokinase and its gene. Biochem J 1993; 293: 1-13.
11. Hattersley AT, Ashcroft FM. Activating mutations in Kir6.2 and neonatal diabetes: new clinical syndromes, new scientific insights, and new therapy. Diabetes 2005; 54: 2503-2513.
12. Froguel P, Velho G. Molecular genetics of maturity-onset diabetes of the young. Trends Endocrinol Metab 1999; 10: 142-146.
13. Tarasov AI, Nicolson T, Riveline JP et al. A rare mutation in ABCC8/SUR1 leading to altered KATP channel activity and {beta}-cell glucose sensing is associated with type 2 diabetes mellitus in adults. Diabetes 2008; 57: 1595-1604.
14. Sekine N, Cirulli V, Regazzi R et al. Low lactate dehydrogenase and high mitochondrial glycerol phosphate dehydrogenase in pancreatic β-cell. Potential role in nutrient sensing. J Biol Chem 1994; 269: 4895-4902.
15. Schuit FC. Why expression of some genes is disallowed in beta-cells. Biochem Soc Trans 2008; 36: 300-305.
16. Otonkoski T, Kaminen N, Ustinov J et al. Physical exercise-induced hyperinsulinemic hypoglycemia is an autosomal-dominant trait characterized by abnormal pyruvate-induced insulin release. Diabetes 2003; 52: 199-204.
17. Otonkoski T, Jiao H, Kaminen-Ahola N et al. Physical exercise-induced hyperinsulinemic hypoglycemia caused by failure of monocarboxylate transporter 1 silencing in pancreatic beta cells. Am J Hum Genet 2007; 81: 467-474.
18. Schuit F, Van LL, Granvik M et al. Beta-cell-specific gene repression: a mechanism to protect against inappropriate or maladjusted insulin secretion? Diabetes 2012; 61: 969-975.
19. Zhao C, Wilson CM, Schuit F, Halestrap AP, Rutter GA. Expression and distribution of lactate/monocarboxylate transporter (MCT) isoforms in pancreatic islets and the exocrine pancreas. Diabetes 2001; 50: 361-366.
20. Hellman B, Idahl L-A, Sehlin J, Taljedal I-B. Influence of anoxia on glucose metabolism in pancreatic islets: lack of correlation between fructose-1, 6-diphosphate and apparent glycolytic flux. Diabetologia 1975; 11: 495-500.
21. Halestrap AP, Meredith D. The SLC16 gene family-from monocarboxylate transporters (MCTs) to aromatic amino acid transporters and beyond. Pflugers Arch 2004; 447: 619-628.
22. Brown LJ, MacDonald MJ, Lehn DA, Moran SM. Sequence of rat mitochondrial glycerol-3-phosphate dehydrogenase cDNA. Evidence for EF-hand calcium-binding domains. J Biol Chem 1994; 269: 14363-14366.
23. Hansford RG, Chappell JB. The effect of Ca2+ on the oxidation of glycerol phosphate by blowfly flight-muscle mitochondria. Biochem Biophys Res Commun 1967; 27: 686-692.
24. Spegel P, Malmgren S, Sharoyko VV, Newsholme P, Koeck T, Mulder H. Metabolomic analyses reveal profound differences in glycolytic and tricarboxylic acid cycle metabolism in glucose-responsive and -unresponsive clonal beta-cell lines. Biochem J 2011; 435: 277-284.
25. Liang Y, Bai G, Doliba N et al. Glucose metabolism and insulin release in mouse betaHC9 cells, as model for wild-type pancreatic beta-cells. Am J Physiol Endocrinol Metab 1996; 270: E846-E857.
26. Schuit F, DeVos A, Farfari S et al. Metabolic fate of glucose in purified islet cells - Glucose-regulated anaplerosis in beta cells. J Biol Chem 1997; 272: 18572-18579.
27. Matschinsky FM, Meglasson M, Ghosh A et al. Biochemical design features of the pancreatic islet cell glucose-sensory system. Adv Exp Med Biol 1986; 211: 459-469.
28. Ishihara H, Wang H, Drewes LR, Wollheim CB. Overexpression of monocarboxylate transporter and lactate dehydrogenase alters insulin secretory responses to pyruvate and lactate in beta cells. J Clin Invest 1999; 104: 1621-1629.
29. Pullen TJ, Sylow L, Sun G, Halestrap AP, Richter EA, Rutter GA. Over-expression of Monocarboxylate Transporter-1 (Slc16a1) in the pancreatic beta-cell leads to relative hyperinsulinism during exercise. Diabetes 2012; 61: 1719-1725.
30. Zhao C, Rutter GA. Overexpression of lactate dehydrogenase A attenuates glucose-induced insulin secretion in stable MIN-6 beta-cell lines. FEBS Lett 1998; 430: 213-216.
31. Ainscow EK, Zhao C, Rutter GA. Acute overexpression of lactate dehydrogenase-A perturbs beta-cell mitochondrial metabolism and insulin secretion. Diabetes 2000; 49: 1149-1155.
32. Meissner T, Otonkoski T, Feneberg R et al. Exercise induced hypoglycaemic hyperinsulinism. Arch Dis Child 2001; 84: 254-257.
33. Pullen TJ, Khan AM, Barton G, Butcher SA, Sun G, Rutter GA. Identification of genes selectively disallowed in the pancreatic islet. Islets 2010; 2: 89-95.
34. Thorrez L, Laudadio I, Van DK et al. Tissue-specific disallowance of housekeeping genes: the other face of cell differentiation. Genome Res 2011; 21: 95-105.
35. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009; 25: 1105-1111.
36. Zhang M, Yao C, Guo Z et al. Apparently low reproducibility of true differential expression discoveries in microarray studies. Bioinformatics 2008; 24: 2057-2063.
37. Bensellam M, Van LL, Overbergh L, Schuit FC, Jonas JC. Cluster analysis of rat pancreatic islet gene mRNA levels after culture in low-, intermediate- and high-glucose concentrations. Diabetologia 2009; 52: 463-476.
38. Ishihara H, Maechler P, Gjinovci A, Herrera PL, Wollheim CB. Islet beta-cell secretion determines glucagon release from neighbouring alpha-cells. Nat Cell Biol 2003; 5: 330-335.
39. Lenzen S, Drinkgern J, Tiedge M. Low antioxidant enzyme gene expression in pancreatic islets compared with various other mouse tissues. Free Radic Biol Med 1996; 20: 463-466.
40. Leloup C, Tourrel-Cuzin C, Magnan C et al. Mitochondrial reactive oxygen species are obligatory signals for glucose-induced insulin secretion. Diabetes 2009; 58: 673-681.
41. Pi J, Zhang Q, Fu J et al. ROS signaling, oxidative stress and Nrf2 in pancreatic beta-cell function. Toxicol Appl Pharmacol 2010; 244: 77-83.
42. Arata AK, Shah R, Rhodes CJ. Hydrogen peroxide is a nutrient-activated secondary signal in beta cells. Diabetologia 2011; 54: S49.
43. Chen H, Gu X, Liu Y et al. PDGF signalling controls age-dependent proliferation in pancreatic beta-cells. Nature 2011; 478: 349-355.
44. Ueno K, Hirata H, Majid S et al. IGFBP-4 activates the Wnt/beta-catenin signaling pathway and induces M-CAM expression in human renal cell carcinoma. Int J Cancer 2011; 129: 2360-2369.
45. Durai R, Davies M, Yang W et al. Biology of insulin-like growth factor binding protein-4 and its role in cancer (review). Int J Oncol 2006; 28: 1317-1325.
46. Rulifson IC, Karnik SK, Heiser PW et al. Wnt signaling regulates pancreatic beta cell proliferation. Proc Natl Acad Sci USA 2007; 104: 6247-6252.
47. Zhu W, Shiojima I, Ito Y et al. IGFBP-4 is an inhibitor of canonical Wnt signalling required for cardiogenesis. Nature 2008; 454: 345-349.
48. Singh RK, Lokeshwar BL. The IL-8-regulated chemokine receptor CXCR7 stimulates EGFR signaling to promote prostate cancer growth. Cancer Res 2011; 71: 3268-3277.
49. Cnop M, Hughes SJ, Igoillo-Esteve M et al. The long lifespan and low turnover of human islet beta cells estimated by mathematical modelling of lipofuscin accumulation. Diabetologia 2010; 53: 321-330.
50. Krishnamurthy J, Ramsey MR, Ligon KL et al. p16INK4a induces an age-dependent decline in islet regenerative potential. Nature 2006; 443: 453-457.
51. Schraenen A, Lemaire K. de FG et al. Placental lactogens induce serotonin biosynthesis in a subset of mouse beta cells during pregnancy. Diabetologia 2010; 53: 2589-2599.
52. Kim H, Toyofuku Y, Lynn FC et al. Serotonin regulates pancreatic beta cell mass during pregnancy. Nat Med 2010; 16: 804-808.
53. Kibbey RG, Pongratz RL, Romanelli AJ, Wollheim CB, Cline GW, Shulman GI. Mitochondrial GTP regulates glucose-stimulated insulin secretion. Cell Metab 2007; 5: 253-264.
54. Maechler P, Wollheim CB. Mitochondrial glutamate acts as a messenger in glucose-induced insulin exocytosis. Nature 1999; 402: 685-689.
55. Prentki M, Vischer S, Glennon MC, Regazzi R, Deeney JT, Corkey BE. Malonyl-CoA and long chain acyl-CoA esters as metabolic coupling factors in nutrient-induced insulin secretion. J Biol Chem 1992; 267: 5802-5810.
56. Roduit R, Nolan C, Alarcon C et al. A role for the malonyl-CoA/long-chain acyl-CoA pathway of lipid signaling in the regulation of insulin secretion in response to both fuel and nonfuel stimuli. Diabetes 2004; 53: 1007-1019.
57. Nolan CJ, Madiraju MS, Delghingaro-Augusto V, Peyot ML, Prentki M. Fatty acid signaling in the beta-cell and insulin secretion. Diabetes 2006; 55: S16-S23.
58. Park I, Han C, Jin S et al. Myosin regulatory light chains are required to maintain the stability of myosin II and cellular integrity. Biochem J 2011; 434: 171-180.
59. Kobayashi H, Inoue A, Mikawa T et al. Isolation of cDNA for bovine stomach 155kDa protein exhibiting myosin light chain kinase activity. J Biochem 1992; 112: 786-791.
60. Massa O, Iafusco D, D'Amato E et al. KCNJ11 activating mutations in Italian patients with permanent neonatal diabetes. Hum Mutat 2004; 25: 22-27.
61. Kato M, Khan S, d'Aniello E, McDonald KJ, Hart DN. The novel endocytic and phagocytic C-Type lectin receptor DCL-1/CD302 on macrophages is colocalized with F-actin, suggesting a role in cell adhesion and migration. J Immunol 2007; 179: 6052-6063.
62. Rudel D, Sommer RJ. The evolution of developmental mechanisms. Dev Biol 2003; 264: 15-37.
63. Martin D, Allagnat F, Chaffard G et al. Functional significance of repressor element 1 silencing transcription factor (REST) target genes in pancreatic beta cells. Diabetologia 2008; 51: 1429-1439.
64. Chong JA, Tapia-Ramirez J, Kim S et al. REST: a mammalian silencer protein that restricts sodium channel gene expression to neurons. Cell 1995; 80: 949-957.
65. Prezioso C, Orlando V. Polycomb proteins in mammalian cell differentiation and plasticity. FEBS Lett 2011; 585: 2067-2077.
66. Shamovsky I, Nudler E. Gene control by large noncoding RNAs. Sci STKE 2006; 2006: e40.
67. Lynn FC. Meta-regulation: microRNA regulation of glucose and lipid metabolism. Trends Endocrinol Metab 2009; 20: 452-459.
68. Moran VA, Perera RJ, Khalil AM. Emerging functional and mechanistic paradigms of mammalian long non-coding RNAs. Nucleic Acids Res 2012; 40: 6391-6400.
69. Pullen TJ, da Silva Xavier G, Kelsey G, Rutter GA. miR-29a and miR-29b contribute to pancreatic {beta}-cell specific silencing of Monocarboxylate Transporter 1 (Mct1/slc16a1). Mol Cell Biol 2011; 31: 3182-3194.
70. van Arensbergen J, Garcia-Hurtado J, Moran I et al. Derepression of Polycomb targets during pancreatic organogenesis allows insulin-producing beta-cells to adopt a neural gene activity program. Genome Res 2010; 20: 722-732.
71. Margueron R, Reinberg D. The Polycomb complex PRC2 and its mark in life. Nature 2011; 469: 343-349.
72. Li KK, Pang JC, Ching AK et al. miR-124 is frequently down-regulated in medulloblastoma and is a negative regulator of SLC16A1. Hum Pathol 2009; 40: 1234-1243.
73. Avnit-Sagi T, Kantorovich L, Kredo-Russo S, Hornstein E, Walker MD. The promoter of the pri-miR-375 gene directs expression selectively to the endocrine pancreas. PLoS One 2009; 4: e5033.
74. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11: 597-610.
75. Barash Y, Calarco JA, Gao W et al. Deciphering the splicing code. Nature 2010; 465: 53-59.
76. Zehetner J, Danzer C, Collins S et al. PVHL is a regulator of glucose metabolism and insulin secretion in pancreatic beta cells. Genes Dev 2008; 22: 3135-3146.
77. Puri S, Cano DA, Hebrok M. A role for von Hippel-Lindau protein in pancreatic beta-cell function. Diabetes 2009; 58: 433-441.
78. Nicolson TJ, Bellomo EA, Wijesekara N et al. Insulin storage and glucose homeostasis in mice null for the granule zinc transporter ZnT8 and studies of the type 2 diabetes-associated variants. Diabetes 2009; 58: 2070-2083.
79. Cantley J, Grey ST, Maxwell PH, Withers DJ. The hypoxia response pathway and beta-cell function. Diabetes Obes Metab 2010; 12: 159-167.
80. Marselli L, Thorne J, Dahiya S et al. Gene expression profiles of Beta-cell enriched tissue obtained by laser capture microdissection from subjects with type 2 diabetes. PLoS One 2010; 5: e11499.
81. Parton LE, McMillen PJ, Shen Y et al. Limited role for SREBP-1c in defective glucose-induced insulin secretion from Zucker Diabetic Fatty rat islets: a functional and gene profiling analysis. Am J Physiol Endocrinol Metab 2006; 291: E982-E994.
82. Jonas JC, Sharma A, Hasenkamp W et al. Chronic hyperglycemia triggers loss of pancreatic beta cell differentiation in an animal model of diabetes. J Biol Chem 1999; 274: 14112-14121.
83. McCarthy MI. Genomics, type 2 diabetes, and obesity. N Engl J Med 2010; 363: 2339-2350.
84. Ravassard P, Hazhouz Y, Pechberty S et al. A genetically engineered human pancreatic beta cell line exhibiting glucose-inducible insulin secretion. J Clin Invest 2011; 121: 3589-3597.