Foxo1 plays an important role in regulating β-cell compensation for insulin resistance in male mice

Endocrinology

Volumn 157, Issue 3, 2016, Pages 1055-1070

  Zhang, Ting ^a   Kim, Dae Hyun ^a,b   Xiao, Xiangwei ^a   Lee, Sojin ^a   Gong, Zhenwei ^a   Muzumdar, Radhika ^a   Calabuig Navarro, Virtu ^a   Yamauchi, Jun ^a,c   Harashima, Hideyoshi ^c   Wang, Rennian ^d   Bottino, Rita ^e   Alvarez Perez, Juan Carlos ^f   Garcia Ocaña, Adolfo ^f   Gittes, George ^a   Dong, H Henry ^a  

^a CHILDREN S HOSPITAL OF PITTSBURGH   (United States)

^b Pusan National University   (South Korea)

^c HOKKAIDO UNIVERSITY   (Japan)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

^e ALLEGHENY HEALTH NETWORK   (United States)

^f MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; FAT; GLUCOSE; GLUCOSE TRANSPORTER 2; INSULIN; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR PDX 1; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, HUMAN; FOXO1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; PANCREATIC AND DUODENAL HOMEOBOX 1 PROTEIN; SLC2A2 PROTEIN, MOUSE; TRANSACTIVATOR PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL GROWTH; CELL METABOLISM; CELL PROLIFERATION; CELL VOLUME; CONTROLLED STUDY; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HUMAN; HUMAN TISSUE; INSULIN RELEASE; INSULIN RESISTANCE; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; OVERNUTRITION; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; ADAPTATION; ANIMAL; C57BL MOUSE; CHROMATIN IMMUNOPRECIPITATION; ENERGY METABOLISM; FLUORESCENCE MICROSCOPY; GENETICS; GLUCOSE TOLERANCE TEST; IMMUNOBLOTTING; METABOLISM; ORGAN SIZE; PANCREAS; PANCREAS ISLET; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SECRETION (PROCESS); TRANSGENIC MOUSE; TUMOR CELL LINE;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DIET, HIGH-FAT; ENERGY METABOLISM; FORKHEAD BOX PROTEIN O1; FORKHEAD TRANSCRIPTION FACTORS; GLUCOSE TOLERANCE TEST; GLUCOSE TRANSPORTER TYPE 2; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOBLOTTING; INSULIN; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, FLUORESCENCE; ORGAN SIZE; PANCREAS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS;

EID: 84960471645     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1852     Document Type: Article

References (65)

1. Sachdeva MM, Stoffers DA. Minireview: meeting the demand for insulin: molecular mechanisms of adaptive postnatal β-cell mass expansion. MolEndocrinol. 2009;23:747-758.
2. Prentki M, Nolan CJ. Islet β cell failure in type 2 diabetes. J Clin Invest. 2006;116:1802-1812.
3. Stamateris RE, Sharma RB, Hollern DA, Alonso LC. Adaptive β-cell proliferation increases early in high-fat feeding in mice, concurrent with metabolic changes, with induction of islet cyclin D2 expression. Am J Physiol Endocrinol Metab. 2013;305:E149-E159.
4. Alonso LC, Yokoe T, Zhang P, et al. Glucose infusion in mice: a new model to induce β-cell replication. Diabetes. 2007;56:1792-1801.
5. Topp BG, Atkinson LL, Finegood DT. Dynamics of insulin sensitivity, -cell function, and -cell mass during the development of diabetes in fa/fa rats. Am J Physiol Endocrinol Metab. 2007;293:E1730-E1735.
6. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. β-Cell deficit and increased β-cell apoptosis in humans with type 2 diabetes. Diabetes. 2003;52:102-110.
7. Bonner-Weir S, Deery D, Leahy JL, Weir GC. Compensatory growth of pancreatic β-cells in adult rats after short-term glucose infusion. Diabetes. 1989;38:49-53.
8. Topp BG, McArthur MD, Finegood DT. Metabolic adaptations to chronic glucose infusion in rats. Diabetologia. 2004;47:1602-1610.
9. Pechhold K, Koczwara K, Zhu X, et al. Blood glucose levels regulate pancreatic β-cell proliferation during experimentally-induced and spontaneous autoimmune diabetes in mice. PLoS One. 2009;4:e4827.
10. Levitt HE, Cyphert TJ, Pascoe JL, et al. Glucose stimulates human β cell replication in vivo in islets transplanted into NOD-severe combined immunodeficiency (SCID) mice. Diabetologia. 2011;54:572-582.
11. Porat S, Weinberg-Corem N, Tornovsky-Babaey S, et al. Control of pancreatic β cell regeneration by glucose metabolism. Cell Metab. 2011;13:440-449.
12. Terauchi Y, Takamoto I, Kubota N, et al. Glucokinase and IRS-2 are required for compensatory β cell hyperplasia in response to high-fat diet-induced insulin resistance. J Clin Invest. 2007;117:246-257.
13. Withers DJ, Gutierrez JS, Towery H, et al. Disruption of IRS-2 causes type 2 diabetes in mice. Nature. 1998;391:900-904.
14. Kubota N, Tobe K, Terauchi Y, et al. Disruption of insulin receptor substrate 2 causes type 2 diabetes because of liver insulin resistance and lack of compensatory β-cell hyperplasia. Diabetes. 2000;49:1880-1889.
15. Accili D, Arden KC. FoxOs at the crossroads of cellular metabolism, differentiation, and transformation. Cell. 2004;117:421-426.
16. Kitamura T. Theroleof FOXO1 inβ-cell failure and type 2 diabetes mellitus. Nat Rev Endocrinol. 2013;9:615-623.
17. Müssig K, Staiger H, Machicao F, et al. Association of common genetic variation in the FOXO1 gene with β-cell dysfunction, impaired glucose tolerance, and type 2 diabetes. J Clin Endocrinol Metab. 2009;94:1353-1360.
18. Talchai SC, Accili D. Legacy effect of Foxo1 in pancreatic endocrine progenitors on adult β-cell mass and function. Diabetes. 2015;64:2868-2879.
19. Kim-Muller JY, Zhao S, Srivastava S, et al. Metabolic inflexibility impairs insulin secretion and results in MODY-like diabetes in triple FoxO-deficient mice. Cell Metab. 2014;20:593-602.
20. Talchai C, Xuan S, Lin HV, Sussel L, Accili D. Pancreatic β cell dedifferentiation as a mechanism of diabetic β cell failure. Cell. 2012;150:1223-1234.
21. Kitamura T, Nakae J, Kitamura Y, et al. The forkhead transcription factor Foxo1 links insulin signaling to Pdx1 regulation of pancreatic β cell growth. J Clin Invest. 2002;110:1839-1847.
22. Okamoto H, Hribal ML, Lin HV, Bennett WR, Ward A, Accili D. Role of the forkhead protein FoxO1 in β cell compensation to insulin resistance. J Clin Invest. 2006;116:775-782.
23. Kitamura T, Kitamura YI, Kobayashi M, et al. Regulation of pancreatic juxtaductal endocrine cell formation by FoxO1. Mol Cell Biol. 2009;29:4417-4430.
24. Buteau J, Shlien A, Foisy S, Accili D. Metabolic diapause in pancreatic β-cells expressing a gain-of-function mutant of the forkhead protein Foxo1. J Biol Chem. 2007;282:287-293.
25. Kawamori D, Kaneto H, Nakatani Y, et al. The forkhead transcription factor Foxo1 bridges the JNK pathway and the transcription factor PDX-1 through its intracellular translocation. J Biol Chem. 2006;281:1091-1098.
26. Al-Masri M, Krishnamurthy M, Li J, et al. Effect of forkhead box O1 (FOXO1) on β cell development in the human fetal pancreas. Diabetologia. 2010;53:699-711.
27. Kitamura YI, Kitamura T, Kruse JP, et al. FoxO1 protects against pancreatic β cell failure through NeuroD and MafA induction. Cell Metab. 2005;2:153-163.
28. Kamagate A, Kim DH, Zhang T, et al. FoxO1 links hepatic insulin action to endoplasmic reticulum stress. Endocrinology. 2010;151:3521-3535.
29. Martinez SC, Tanabe K, Cras-Méneur C, Abumrad NA, Bernal-Mizrachi E, Permutt MA. Inhibition of Foxo1 protects pancreatic islet β-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis. Diabetes. 2008;57:846-859.
30. Kim DH, Perdomo G, Zhang T, et al. FoxO6 integrates insulin signaling with gluconeogenesis in the liver. Diabetes. 2011;60:2763-2774.
31. Qu S, Altomonte J, Perdomo G, He J, et al. Aberrant Forkhead box O1 function is associated with impaired hepatic metabolism. Endocrinology. 2006;147:5641-5652.
32. Su D, Zhang N, He J, et al. Angiopoietin-1 production in islets improves islet engraftment and protects islets from cytokine-induced apoptosis. Diabetes. 2007;56:2274-2283.
33. Sklavos MM, Bertera S, Tse HM, et al. Redox modulation protects islets from transplant-related injury. Diabetes. 2010;59:1731-1738.
34. Kamagate A, Qu S, Perdomo G, et al. FoxO1 mediates insulindependent regulation of hepatic VLDL production in mice. J Clin Invest. 2008;118:2347-2364.
35. Schisler JC, Jensen PB, Taylor DG, et al. The Nkx6.1 homeodomain transcription factor suppresses glucagon expression and regulates glucose-stimulated insulin secretion in islet β cells. Proc Natl Acad Sci USA. 2005;102:7297-7302.
36. Fiaschi-Taesch NM, Kleinberger JW, Salim FG, et al. Human pancreatic β-cell G1/S molecule cell cycle atlas. Diabetes. 2013;62:2450-2459.
37. Puig O, Tjian R. Transcriptional feedback control of insulin receptor by dFOXO/FOXO1. Genes Dev. 2005;19:2435-2446.
38. Meier JJ, Butler AE, Saisho Y, et al. β-Cell replication is the primary mechanism subserving the postnatal expansion of β-cell mass in humans. Diabetes. 2008;57:1584-1594.
39. Georgia S, Hinault C, Kawamori D, et al. Cyclin D2 is essential for the compensatory β-cell hyperplastic response to insulin resistance in rodents. Diabetes. 2010;59:987-996.
40. Balcazar N, Sathyamurthy A, Elghazi L, et al. mTORC1 activation regulates β-cell mass and proliferation by modulation of cyclin D2 synthesis and stability. J Biol Chem. 2009;284:7832-7842.
41. Del Guerra S, Lupi R, Marselli L, et al. Functional and molecular defects ofpancreatic islets in human type 2 diabetes. Diabetes. 2005;54:727-735.
42. Thorens B, Wu YJ, Leahy JL, Weir GC. The loss of GLUT2 expression by glucose-unresponsive β cells of db/db mice is reversible and is induced by the diabetic environment. J Clin Invest. 1992;90:77-85.
43. Guo S, Dai C, Guo M, et al. Inactivation of specific β cell transcription factors in type 2 diabetes. J Clin Invest. 2013;123:3305-3316.
44. Sansbury FH, Flanagan SE, Houghton JA, et al. SLC2A2 mutations can cause neonatal diabetes, suggesting GLUT2 may have a role in human insulin secretion. Diabetologia. 2012;55:2381-2385.
45. Hughes KJ, Meares GP, Hansen PA, Corbett JA. FoxO1 and SIRT1 regulate β-cell responses to nitric oxide. J Biol Chem. 2011;286:8338-8348.
46. Kibbe C, Chen J, Xu G, Jing G, Shalev A. FOXO1 competes with carbohydrate response element-binding protein (ChREBP) and inhibits thioredoxin-interacting protein (TXNIP) transcription in pancreatic β cells. J Biol Chem. 2013;288:23194-23202.
47. Essers MA, de Vries-Smits LM, Barker N, Polderman PE, Burgering BM, Korswagen HC. Functional interaction between β-catenin and FOXO in oxidative stress signaling. Science. 2005;308:1181-1184.
48. Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet β cells in diabetes. J Biol Chem. 2004;279:42351-42354.
49. Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal. 2007;9:2277-2293.
50. Poitout V, Robertson RP. Glucolipotoxicity: fuel excess and β-cell dysfunction. Endocr Rev. 2008;29:351-366.
51. Meares GP, Fontanilla D, Broniowska KA, Andreone T, Lancaster JR Jr, Corbett JA. Differential responses ofpancreatic β-cells to ROS and RNS. Am J Physiol Endocrinol Metab. 2013;304:E614-E622.
52. Zhao Z, Choi J, Zhao C, Ma ZA. FTY720 normalizes hyperglycemia by stimulating β-cell in vivo regeneration in db/db mice through regulation of cyclin D3 and p57 (KIP2). J Biol Chem. 2012;287:5562-5573.
53. Köhler CU, Olewinski M, Tannapfel A, Schmidt WE, Fritsch H, Meier JJ. Cell cycle control of β-cell replication in the prenatal and postnatal human pancreas. Am J Physiol Endocrinol Metab. 2011;300:E221-E230.
54. Ai J, Duan J, Lv X, et al. Overexpression of FoxO1 causes proliferation of cultured pancreatic β cells exposed to low nutrition. Biochemistry. 2010;49:218-225.
55. Sharma RB, O'Donnell AC, Stamateris RE, et al. Insulin demand regulates β cell number via the unfolded protein response. J Clin Invest. 2015;125:3831-3846.
56. Dowell P, Otto TC, Adi S, Lane MD. Convergence of peroxisome proliferator-activated receptor y and Foxo1 signaling pathways. J Biol Chem. 2003;278:45485-45491.
57. Qu S, Su D, Altomonte J, Kamagate A, et al. PPARα mediates the hypolipidemic action of fibrates by antagonizing FoxO1. Am J Physiol Endocrinol Metab. 2007;292:E421-E434.
58. Tsunekawa S, Demozay D, Briaud I, et al. FoxO feedback control of basal IRS-2 expression in pancreatic β-cells is distinct from that in hepatocytes. Diabetes. 2011;60:2883-2891.
59. Nakae J, Biggs WH 3rd, Kitamura T, et al. Regulation of insulin action and pancreatic β-cell function by mutated alleles of the gene encoding forkhead transcription factor Foxo1. Nat Genet. 2002;32:245-253.
60. Kikuchi O, Kobayashi M, Amano K, et al. FoxO1 gain of function in the pancreas causes glucose intolerance, polycystic pancreas, and islet hypervascularization. PLoS One. 2012;7:e32249.
61. Kim HJ, Kobayashi M, Sasaki T, et al. Overexpression of FoxO1 in the hypothalamus and pancreas causes obesity and glucose intolerance. Endocrinology. 2012;153:659-671.
62. Talchai C, Xuan S, Kitamura T, De Pinho RA, Accili D. Generation of functional insulin-producing cells in the gut by Foxo1 ablation. Nat Genet. 2012;44:406-412, S1.
63. Bouchi R, Foo KS, Hua H, et al. FOXO1 inhibition yields functional insulin-producing cells in human gut organoid cultures. Nat Commun. 2014;5:4242.
64. Kim MS, Pak YK, Jang PG, et al. Role of hypothalamic Foxo1 in the regulation of food intake and energy homeostasis. Nat Neurosci. 2006;9:901-906.
65. Ren H, Orozco IJ, Su Y, et al. FoxO1 target Gpr17 activates AgRP neurons to regulate food intake. Cell. 2012;149:1314-1326.