Disruption of protein-tyrosine phosphatase 1B expression in the pancreas affects β-cell function

Endocrinology (United States)

Volumn 155, Issue 9, 2014, Pages 3329-3338

  Liu, Siming ^a   Xi, Yannan ^a   Bettaieb, Ahmed ^a   Matsuo, Kosuke ^a   Matsuo, Izumi ^a   Kulkarni, Rohit N ^b   Haj, Fawaz G ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN; PROTEIN TYROSINE PHOSPHATASE 1B; PANCRELIPASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CELL CULTURE; COMPARATIVE STUDY; CONTROLLED STUDY; ENERGY BALANCE; ENZYME PHOSPHORYLATION; EX VIVO STUDY; FAT INTAKE; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE; GLUCOSE TOLERANCE TEST; HUMAN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; INSULIN SENSITIVITY; LIPID DIET; MALE; MOUSE; NONHUMAN; PANCREAS ISLET CELL FUNCTION; PROTEIN EXPRESSION; ANIMAL; C57BL MOUSE; ENZYMOLOGY; GENE INACTIVATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; PANCREAS ISLET BETA CELL;

ANIMALS; FEMALE; GENE KNOCKOUT TECHNIQUES; GLUCOSE; GLUCOSE INTOLERANCE; INSULIN; INSULIN-SECRETING CELLS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PANCRELIPASE; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 1;

EID: 84907042723     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-2004     Document Type: Article

References (56)

1. Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest. 2000;106:473-481.
2. Biddinger SB, Kahn CR. From mice to men: insights into the insulin resistance syndromes. Annu Rev Physiol. 2006;68:123-158.
3. Bell GI, Polonsky KS. Diabetes mellitus and genetically programmed defects in beta-cell function. Nature. 2001;414:788-791.
4. Muoio DM, Newgard CB. Mechanisms of disease: molecular and metabolic mechanisms of insulin resistance and beta-cell failure in type 2 diabetes. Nat Rev Mol Cell Biol. 2008;9:193-205.
5. 2+and insulin oscillations, and basal insulin release. Diabetes. 2005;54:1798-1807.
6. Pasquale EB. Eph-ephrin bidirectional signaling in physiology and disease. Cell. 2008;133:38-52.
7. Konstantinova I, Nikolova G, Ohara-Imaizumi M, et al. EphA-Eph-rin-A-mediated beta cell communication regulates insulin secretion from pancreatic islets. Cell. 2007;129:359-370.
8. Frangioni JV, Beahm PH, Shifrin V, Jost CA, Neel BG. The non-transmembrane tyrosine phosphatase PTP-1B localizes to the endoplasmic reticulum via its 35 amino acid C-terminal sequence. Cell. 1992;68:545-560.
9. Woodford-Thomas TA, Rhodes JD, Dixon JE. Expression of a protein tyrosine phosphatase in normal and v-src-transformed mouse 3T3 fibroblasts. J Cell Biol. 1992;117:401-414.
10. Haj FG, Verveer PJ, Squire A, Neel BG, Bastiaens PI. Imaging sites of receptor dephosphorylation by PTP1B on the surface of the endoplasmic reticulum. Science. 2002;295:1708-1711.
11. Elchebly M, Payette P, Michaliszyn E, et al. Increased insulin sensitivity and obesity resistance in mice lacking the protein tyrosine phosphatase-1B gene. Science. 1999;283:1544-1548.
12. Klaman LD, Boss O, Peroni OD, et al. Increased energy expenditure, decreased adiposity, and tissue-specific insulin sensitivity in protein-tyrosine phosphatase 1B-deficient mice. Mol Cell Biol. 2000;20: 5479-5489.
13. Cheng A, Uetani N, Simoncic PD, et al. Attenuation of leptin action and regulation of obesity by protein tyrosine phosphatase 1B. Dev Cell. 2002;2:497-503.
14. Zabolotny JM, Bence-Hanulec KK, Stricker-Krongrad A, et al. PTP1B regulates leptin signal transduction in vivo. Dev Cell. 2002; 2:489-495.
15. Delibegovic M, Zimmer D, Kauffman C, et al. Liver-specific deletion of protein-tyrosine phosphatase 1B (PTP1B) improves metabolic syndrome and attenuates diet-induced endoplasmic reticulum stress. Diabetes. 2009;58:590-599.
16. -/-mice. J Biol Chem. 2005;280: 15038-15046.
17. Delibegovic M, Bence KK, Mody N, et al. Improved glucose homeostasis in mice with muscle-specific deletion of protein-tyrosine phosphatase 1B. Mol Cell Biol. 2007;27:7727-7734.
18. Bence KK, Delibegovic M, Xue B, et al. Neuronal PTP1B regulates body weight, adiposity and leptin action. Nat Med. 2006;12:917-924.
19. Owen C, Czopek A, Agouni A, et al. Adipocyte-specific protein tyrosine phosphatase 1B deletion increases lipogenesis, adipocyte cell size and is a minor regulator of glucose homeostasis. PloS One. 2012;7:e32700.
20. Kushner JA, Haj FG, Klaman LD, et al. Islet-sparing effects of protein tyrosine phosphatase-1b deficiency delays onset of diabetes in IRS2 knockout mice. Diabetes. 2004;53:61-66.
21. Bettaieb A, Liu S, Xi Y, et al. Differential regulation of endoplasmic reticulum stress by protein tyrosine phosphatase 1B and T cell protein tyrosine phosphatase. J Biol Chem. 2011;286:9225-9235.
22. Gu G, Dubauskaite J, Melton DA. Direct evidence for the pancreatic lineage: NGN3 + cells are islet progenitors and are distinct from duct progenitors. Development. 2002;129:2447-2457.
23. Kulkarni RN, Winnay JN, Daniels M, et al. Altered function of insulin receptor substrate-1-deficient mouse islets and cultured beta-cell lines. J Clin Invest. 1999;104:R69-75.
24. Bettaieb A, Matsuo K, Matsuo I, et al. Protein tyrosine phosphatase 1B deficiency potentiates PERK/eIF2alpha signaling in brown adipocytes. PloS One. 2012;7:e34412.
25. Bettaieb A, Bakke J, Nagata N, et al. Protein tyrosine phosphatase 1B regulates pyruvate kinase M2 tyrosine phosphorylation. J Biol Chem. 2013;288:17360-17371.
26. Bakke J, Bettaieb A, Nagata N, Matsuo K, Haj FG. Regulation of the SNARE-interacting protein Munc18c tyrosine phosphorylation in adipocytes by protein-tyrosine phosphatase 1B. Cell Commun Signal. 2013;11:57.
27. Tiganis T, Bennett AM. Protein tyrosine phosphatase function: the substrate perspective. Biochem J. 2007;402:1-15.
28. Zhang SS, Hao E, Yu J, et al. Coordinated regulation by Shp2 tyrosine phosphatase of signaling events controlling insulin biosynthesis in pancreatic beta-cells. Proc Natl Acad Sci USA. 2009;106: 7531-7536.
29. Bagdade JD, Bierman EL, Porte D Jr. The significance of basal insulin levels in the evaluation of the insulin response to glucose in diabetic and nondiabetic subjects. J Clin Invest. 1967;46:1549-1557.
30. Xiao J, Gregersen S, Kruhøffer M, Pedersen SB, Ørntoft TF, Her-mansen K. The effect of chronic exposure to fatty acids on gene expression in clonal insulin-producing cells: studies using high density oligonucleotide microarray. Endocrinology. 2001;142:4777-4784.
31. Hennige AM, Ranta F, Heinzelmann I, et al. Overexpression of kinase-negative protein kinase Cdelta in pancreatic beta-cells protects mice from diet-induced glucose intolerance and beta-cell dysfunction. Diabetes. 2010;59:119-127.
32. Jain R, Jain D, Liu Q, et al. Pharmacological inhibition of Eph receptors enhances glucose-stimulated insulin secretion from mouse and human pancreatic islets. Diabetologia. 2013;56:1350-1355.
33. Nievergall E, Janes PW, Stegmayer C, et al. PTP1B regulates Eph receptor function and trafficking. J Cell Biol. 2010;191:1189-1203.
34. Haj FG, Sabet O, Kinkhabwala A, et al. Regulation of signaling at regions of cell-cell contact by endoplasmic reticulum-bound protein-tyrosine phosphatase 1B. PloS One. 2012;7:e36633.
35. Zhang ZY, Maclean D, McNamara DJ, Sawyer TK, Dixon JE. Protein tyrosine phosphatase substrate specificity: size and phosphoty-rosine positioning requirements in peptide substrates. Biochemistry. 1994;33:2285-2290.
36. Flint AJ, Tiganis T, Barford D, Tonks NK. Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. Proc Natl Acad Sci USA. 1997;94: 1680-1685.
37. Haj FG, Markova B, Klaman LD, Bohmer FD, Neel BG. Regulation of receptor tyrosine kinase signaling by protein tyrosine phospha-tase-1B. J Biol Chem. 2003;278:739-744.
38. Stuible M, Dubé N, Tremblay ML. PTP1B regulates cortactin tyrosine phosphorylation by targeting Tyr446. J Biol Chem. 2008; 283:15740-15746.
39. Huyer G, Liu S, Kelly J, et al. Mechanism of inhibition of protein-tyrosine phosphatases by vanadate and pervanadate. J Biol Chem. 1997;272:843-851.
40. Merrins MJ, Van Dyke AR, Mapp AK, Rizzo MA, Satin LS. Direct measurements of oscillatory glycolysis in pancreatic islet β-cells using novel fluorescence resonance energy transfer (FRET) biosensors for pyruvate kinase M2 Activity. J Biol Chem. 2013;288:33312-33322.
41. Wicksteed B, Brissova M, Yan W, et al. Conditional gene targeting in mouse pancreatic β-cells: analysis of ectopic Cre transgene expression in the brain. Diabetes. 2010;59:3090-3098.
42. Schwartz MW, Guyenet SJ, Cirulli V. The hypothalamus and β-cell connection in the gene-targeting era. Diabetes. 2010;59:2991-2993.
43. Banno R, Zimmer D, De Jonghe BC, et al. PTP1B and SHP2 in POMC neurons reciprocally regulate energy balance in mice. J Clin Invest. 2010;120:720-734.
44. Lu B, Wu H, Gu P, et al. Improved glucose-stimulated insulin secretion by intra-islet inhibition of protein-tyrosine phosphatase 1B expression in rats fed a high-fat diet. J Endocrinol Invest. 2012;35: 63-70.
45. Gunton JE, Kulkarni RN, Yim S, et al. Loss of ARNT/HIF1beta mediates altered gene expression and pancreatic-islet dysfunction in human type 2 diabetes. Cell. 2005;122:337-349.
46. Holst B, Egerod KL, Jin C, et al. G protein-coupled receptor 39 deficiency is associated with pancreatic islet dysfunction. Endocrinology. 2009;150:2577-2585.
47. Bjorge JD, Pang A, Fujita DJ. Identification of protein-tyrosine phosphatase 1B as the major tyrosine phosphatase activity capable of dephosphorylating and activating c-Src in several human breast cancer cell lines. J Biol Chem. 2000;275:41439-41446.
48. Kulkarni RN, Brüning JC, Winnay JN, Postic C, Magnuson MA, Kahn CR. Tissue-specific knockout of the insulin receptor in pancreatic beta cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell. 1999;96:329-339.
49. Okada T, Liew CW, Hu J, et al. Insulin receptors in beta-cells are critical for islet compensatory growth response to insulin resistance. Proc Natl Acad Sci USA. 2007;104:8977-8982.
50. Covey SD, Wideman RD, McDonald C, et al. The pancreatic beta cell is a key site for mediating the effects of leptin on glucose homeostasis. Cell Metab. 2006;4:291-302.
51. Morioka T, Asilmaz E, Hu J, et al. Disruption of leptin receptor expression in the pancreas directly affects beta cell growth and function in mice. J Clin Invest. 2007;117:2860-2868.
52. Tejedo JR, Cahuana GM, Ramírez R, et al. nitric oxide triggers the phosphatidylinositol 3-kinase/Akt survival pathway in insulin-producing RINm5F cells by arousing Src to activate insulin receptor substrate-1. Endocrinology. 2004;145:2319-2327.
53. Kominato R, Fujimoto S, Mukai E, et al. Src activation generates reactive oxygen species and impairs metabolism-secretion coupling in diabetic Goto-Kakizaki and ouabain-treated rat pancreatic islets. Diabetologia. 2008;51:1226-1235.
54. -/-mice reveals a role for transla-tional control in secretory cell survival. Molecular cell. 2001;7: 1153-1163.
55. Scheuner D, Song B, McEwen E, et al. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell. 2001;7:1165-1176.
56. Oh E, Thurmond DC. Munc18c depletion selectively impairs the sustained phase of insulin release. Diabetes. 2009;58:1165-1174.