Bridges between mitochondrial oxidative stress, ER stress and mTOR signaling in pancreatic β cells

Cellular Signalling

Volumn 28, Issue 8, 2016, Pages 1099-1104

  Wang, Jing ^a   Yang, Xin ^a   Zhang, Jingjing ^a  

^a CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

ER stress; Mitochondrial oxidative stress; MTOR; Pancreatic cells

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; PROTEIN KINASE B; TARGET OF RAPAMYCIN KINASE;

APOPTOSIS; CELL GROWTH; CELL LOSS; CELL MEMBRANE; CELL PROLIFERATION; CELL SURVIVAL; DISULFIDE BOND; ENDOPLASMIC RETICULUM STRESS; HUMAN; INSULIN RELEASE; INSULIN SYNTHESIS; LIPOTOXICITY; MITOCHONDRIAL DYNAMICS; NONHUMAN; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; METABOLISM; MITOCHONDRION; PATHOLOGY;

ANIMALS; ENDOPLASMIC RETICULUM STRESS; HUMANS; INSULIN-SECRETING CELLS; MITOCHONDRIA; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84969814814     PISSN: 08986568     EISSN: 18733913     Source Type: Journal    
DOI: 10.1016/j.cellsig.2016.05.007     Document Type: Review

References (111)

1. Xu G., et al. Exendin-4 stimulates both beta-cell replication and neogenesis, resulting in increased beta-cell mass and improved glucose tolerance in diabetic rats. Diabetes 1999, 48(12):2270-2276.
2. Liu Z., et al. Mice with beta cell overexpression of glycogen synthase kinase-3beta have reduced beta cell mass and proliferation. Diabetologia 2008, 51(4):623-631.
3. Ernesto Bernal-Mizrachi W.W., Stahlhut S., Welling C.M., Permutt M.A. Islet β cell expression of constitutively active Akt1/PKBα induces striking hypertrophy, hyperplasia, and hyperinsulinemia. J. Clin. Investig. 2002, 108(11):1631-1638.
4. Butler A.E., et al. Increased beta-cell apoptosis prevents adaptive increase in beta-cell mass in mouse model of type 2 diabetes: evidence for role of islet amyloid formation rather than direct action of amyloid. Diabetes 2003, 52(9):2304-2314.
5. Butler A.E., et al. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003, 52(1):102-110.
6. Ott M., et al. Mitochondria, oxidative stress and cell death. Apoptosis 2007, 12(5):913-922.
7. Harding H.P., Ron D. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 2002, 51(Suppl. 3):S455-S461.
8. Um S.H., D'Alessio D., Thomas G. Nutrient overload, insulin resistance, and ribosomal protein S6 kinase 1, S6K1. Cell Metab. 2006, 3(6):393-402.
9. Wullschleger S., Loewith R., Hall M.N. TOR signaling in growth and metabolism. Cell 2006, 124(3):471-484.
10. Estela J., et al. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat. Cell Biol. 2004, 6(11):1122-1128.
11. DH K., et al. GbetaL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 2003, 11(4):895-904.
12. Peterson T.R., et al. DEPTOR is an mTOR inhibitor frequently overexpressed in multiple myeloma cells and required for their survival. Cell 2009, 137(5):873-886.
13. Takeshi K., et al. Tti1 and Tel2 are critical factors in mammalian target of rapamycin complex assembly. J. Biol. Chem. 2010, 285(26):20109-20116.
14. Hara K., et al. Raptor, a binding partner of target of rapamycin (TOR), mediates TOR action. Cell 2002, 110(2):177-189.
15. Sancak Y., et al. PRAS40 is an insulin-regulated inhibitor of the mTORC1 protein kinase. Mol. Cell 2007, 25(6):903-915.
16. Frias M.A., et al. mSin1 is necessary for Akt/PKB phosphorylation, and its isoforms define three distinct mTORC2s. Curr. Biol. 2006, 16(18):1865-1870.
17. Pearce L., et al. Identification of Protor as a novel Rictor-binding component of mTOR complex-2. Biochem. J. 2007, 405(Part 3):513-522.
18. Loewith R., et al. Two TOR complexes, only one of which is rapamycin sensitive, have distinct roles in cell growth control. Mol. Cell 2002, 10(3):457-468.
19. Barlow A.D., et al. Rapamycin toxicity in MIN6 cells and rat and human islets is mediated by the inhibition of mTOR complex 2 (mTORC2). Diabetologia 2012, 55(5):1355-1365.
20. Sarbassov D.D., et al. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 2006, 22(2):159-168.
21. Yecies J.L., Manning B.D. Transcriptional control of cellular metabolism by mTOR signaling. Cancer Res. 2011, 71(8):2815-2820.
22. Kim D.-H., et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 2002, 110(2):163-175.
23. Cunningham J.T., et al. mTOR controls mitochondrial oxidative function through a YY1-PGC-1alpha transcriptional complex. Nature 2007, 450(7170):736-740.
24. Norman B., et al. mTORC1 activation regulates beta-cell mass and proliferation by modulation of cyclin D2 synthesis and stability. J. Biol. Chem. 2009, 284(12):7832-7842.
25. Fraenkel M., et al. mTOR inhibition by rapamycin prevents beta-cell adaptation to hyperglycemia and exacerbates the metabolic state in type 2 diabetes. Diabetes 2008, 57(4):945-957.
26. Reiling J.H., Sabatini D.M. Stress and mTORture signaling. Oncogene 2006, 25(48):6373-6383.
27. Alberto B., et al. Pancreatic β-cell failure mediated by mTORC1 hyperactivity and autophagic impairment. Diabetes 2014, 63(9):2996-3008.
28. Shigeyama Y., et al. Biphasic response of pancreatic beta-cell mass to ablation of tuberous sclerosis complex 2 in mice. Mol. Cell. Biol. 2008, 28(9):2971-2979.
29. Rachdi L., et al. Disruption of Tsc2 in pancreatic beta cells induces beta cell mass expansion and improved glucose tolerance in a TORC1-dependent manner. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(27):9250-9255.
30. Lynda E., et al. Decreased IRS signaling impairs beta-cell cycle progression and survival in transgenic mice overexpressing S6K in beta-cells. Diabetes 2010, 59(10):2390-2399.
31. Yanyun G., et al. Rictor/mTORC2 is essential for maintaining a balance between beta-cell proliferation and cell size. Diabetes 2011, 60(3):827-837.
32. Le Bacquer O., et al. mTORC1 and mTORC2 regulate insulin secretion through Akt in INS-1 cells. J. Endocrinol. 2013, 216(1):21-29.
33. Pelicano H., Carney D., Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. 2004, 7(2):97-110.
34. Houstis N., Rosen E.D., Lander E.S. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 2006, 440(7086):944-948.
35. Aleksandra T., et al. Somatic mtDNA mutations cause aging phenotypes without affecting reactive oxygen species production. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(50):17993-17998.
36. Wulf D.G. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82(1):47-95.
37. Granger D.N., Kvietys P.R. Reperfusion injury and reactive oxygen species: the evolution of a concept. Redox Biol. 2015, 6:524-551.
38. Maechler P., et al. Role of mitochondria in beta-cell function and dysfunction. Adv. Exp. Med. Biol. 2010, 654:193-216.
39. Panfoli I., et al. Extramitochondrial tricarboxylic acid cycle in retinal rod outer segments. Biochimie 2011, 93(9):1565-1575.
40. Murphy M.P. How mitochondria produce reactive oxygen species. Biochem. J. 2009, 417(1):1-13.
41. Nishikawa T., et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404(6779):787-790.
42. Koopman W.J., Willems P.H., Smeitink J.A. Monogenic mitochondrial disorders. N. Engl. J. Med. 2012, 366(12):1132-1141.
43. Niemann A., et al. The Gdap1 knockout mouse mechanistically links redox control to Charcot-Marie-Tooth disease. Brain 2014, 137(Pt 3):668-682.
44. Koopman W.J., et al. Mammalian mitochondrial complex I: biogenesis, regulation, and reactive oxygen species generation. Antioxid. Redox Signal. 2010, 12(12):1431-1470.
45. Brown G.C., Borutaite V. There is no evidence that mitochondria are the main source of reactive oxygen species in mammalian cells. Mitochondrion 2012, 12(1):1-4.
46. Mailloux R.J., McBride S.L., Harper M.E. Unearthing the secrets of mitochondrial ROS and glutathione in bioenergetics. Trends Biochem. Sci. 2013, 38(12):592-602.
47. Quinlan C.L., et al. Sites of reactive oxygen species generation by mitochondria oxidizing different substrates. Redox Biol. 2013, 1:304-312.
48. Woolley J.F., Stanicka J., Cotter T.G. Recent advances in reactive oxygen species measurement in biological systems. Trends Biochem. Sci. 2013, 38(11):556-565.
49. Iynedjian P.B. Molecular physiology of mammalian glucokinase. Cell. Mol. Life Sci. 2009, 66(1):27-42.
50. Ashcroft F.M. K(ATP) channels and insulin secretion: a key role in health and disease. Biochem. Soc. Trans. 2006, 34(2):243-246.
51. Eliasson L., et al. Novel aspects of the molecular mechanisms controlling insulin secretion. J. Physiol. 2008, 586(14):3313-3324.
52. Silva J.P., et al. Impaired insulin secretion and beta-cell loss in tissue-specific knockout mice with mitochondrial diabetes. Nat. Genet. 2000, 26(3):336-340.
53. Brändle M., et al. Diminished insulin secretory response to glucose but normal insulin and glucagon secretory responses to arginine in a family with maternally inherited diabetes and deafness caused by mitochondrial tRNA(LEU(UUR)) gene mutation. Diabetes Care 2001, 24(7):1253-1258.
54. Maassen J.A., et al. Mitochondrial diabetes: molecular mechanisms and clinical presentation. Diabetes 2004, 53(Suppl. 1):S103-S109.
55. Circu M.L., Aw T.Y. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic. Biol. Med. 2010, 48(6):749-762.
56. Mehmeti I., et al. Induction of the intrinsic apoptosis pathway in insulin-secreting cells is dependent on oxidative damage of mitochondria but independent of caspase-12 activation. Biochim. Biophys. Acta 2011, 1813(10):1827-1835.
57. Pi J., et al. ROS signaling, oxidative stress and Nrf2 in pancreatic beta-cell function. Toxicol. Appl. Pharmacol. 2010, 244(1):77-83.
58. Maechler P., Jornot L., Wollheim C.B. Hydrogen peroxide alters mitochondrial activation and insulin secretion in pancreatic beta cells. J. Biol. Chem. 1999, 274(39):27905-27913.
59. Newsholme P., Haber E.P., Hirabara S.M., Rebelato E.L.O., Procopio J., Morgan D., et al. Diabetes associated cell stress and dysfunction: role of mitochondrial and non-mitochondrial ROS production and activity. J. Physiol. 2007, 583(Pt 1):9-24.
60. Rabinovitch A. An update on cytokines in the pathogenesis of insulin-dependent diabetes mellitus. Diabetes Metab. Rev. 1998, 14(2):129-151.
61. Evans J.L., et al. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr. Rev. 2002, 23(5):599-622.
62. Mandrup-Poulsen T. Beta-cell apoptosis: stimuli and signaling. Diabetes 2001, 50(Suppl. 1):S58-S63.
63. Robertson R.P., et al. Glucose toxicity in beta-cells: type 2 diabetes, good radicals gone bad, and the glutathione connection. Diabetes 2003, 52(3):581-587.
64. Evans J.L., et al. Are oxidative stress-activated signaling pathways mediators of insulin resistance and beta-cell dysfunction?. Diabetes 2003, 52(1):1-8.
65. Sangbin L., et al. Mitochondria-targeted antioxidants protect pancreatic β-cells against oxidative stress and improve insulin secretion in glucotoxicity and glucolipotoxicity. Cell. Physiol. Biochem. 2011, 28(5):873-886.
66. Lin N., et al. Mitochondrial reactive oxygen species (ROS) inhibition ameliorates palmitate-induced INS-1 beta cell death. Endocrine 2012, 42(1):107-117.
67. Shoshani T., et al. Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol. Cell. Biol. 2002, 22(7):2283-2293.
68. Jin H., et al. Hypoxic condition- and high cell density-induced expression of Redd1 is regulated by activation of hypoxia-inducible factor-1 alpha and Sp1 through the phosphatidylinositol 3-kinase/Akt signaling pathway. Cell. Signal. 2007, 19(7):1393-1403.
69. Liu L., et al. Hypoxia-induced energy stress regulates mRNA translation and cell growth: molecular cell. Mol. Cell 2006, 21(21):521-531.
70. Kimball S.R., Abbas A., Jefferson L.S. Melatonin represses oxidative stress-induced activation of the MAP kinase and mTOR signaling pathways in H4IIE hepatoma cells through inhibition of Ras. J. Pineal Res. 2008, 44(4):379-386.
71. Koyanagi M., et al. Ablation of TSC2 enhances insulin secretion by increasing the number of mitochondria through activation of mTORC1. PLoS One 2011, 6(8).
72. Etty B.W., et al. Improvement of ER stress-induced diabetes by stimulating autophagy. Autophagy 2013, 9(4):626-628.
73. Swati A., et al. Activation of autophagic flux against xenoestrogen bisphenol-A-induced hippocampal neurodegeneration via AMP kinase (AMPK)/mammalian target of rapamycin (mTOR) pathways. J. Biol. Chem. 2015, 290(34):21163-21184.
74. McDaniel M.L., et al. Metabolic and autocrine regulation of the mammalian target of rapamycin by pancreatic beta-cells. Diabetes 2002, 51(10):2877-2885.
75. Zhang X., et al. Hypothalamic IKKbeta/NF-kappaB and ER stress link overnutrition to energy imbalance and obesity. Cell 2008, 135(1):61-73.
76. Yang L., et al. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 2010, 11(6):467-478.
77. Ozcan U., et al. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006, 313(5790):1137-1140.
78. Thomas S.E., et al. Diabetes as a disease of endoplasmic reticulum stress. Diabetes Metab. Res. Rev. 2010, 26(8):611-621.
79. Araki E., Oyadomari S., Mori M. Impact of endoplasmic reticulum stress pathway on pancreatic beta-cells and diabetes mellitus. Exp. Biol. Med. (Maywood) 2003, 228(10):1213-1217.
80. Laybutt D.R., et al. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 2007, 50(4):752-763.
81. Knowlton A.A. Life, death, the unfolded protein response and apoptosis. Cardiovasc. Res. 2007, 73(1):1-2.
82. Cao S.S., Kaufman R.J. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid. Redox Signal. 2014, 21(3):396-413.
83. Thon M., et al. Leptin induced GRP78 expression through the PI3K-mTOR pathway in neuronal cells. Sci. Rep. 2013, 4:7096.
84. Eizirik D.L., Cardozo A.K., Cnop M. The role for endoplasmic reticulum stress in diabetes mellitus. Endocr. Rev. 2008, 29(1):42-61.
85. Fonseca S.G., Lipson K.L., Urano F. Endoplasmic reticulum stress signaling in pancreatic beta-cells. Antioxid. Redox Signal. 2007, 9(12):2335-2344.
86. Ortsater H., Sjoholm A. A busy cell-endoplasmic reticulum stress in the pancreatic beta-cell. Mol. Cell. Endocrinol. 2007, 277(1-2):1-5.
87. Jiang Y., et al. Metformin plays a dual role in MIN6 pancreatic beta cell function through AMPK-dependent autophagy. Int. J. Biol. Sci. 2014, 10(3):268-277.
88. Yang Z., Klionsky D.J. Eaten alive: a history of macroautophagy. Nat. Cell Biol. 2010, 12(9):814-822.
89. Noboru M., et al. Autophagy fights disease through cellular self-digestion. Nature 2008, 451(7182):1069-1075.
90. Debnath J., Baehrecke E.H., Kroemer G. Does autophagy contribute to cell death?. Autophagy 2014, 1(2):66-74.
91. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 2008, 9(12):1004-1010.
92. Gump J.M., Thorburn A. Autophagy and apoptosis: what is the connection?. Trends Cell Biol. 2011, 21(7):387-392.
93. Axe E.L., et al. Autophagosome formation from membrane compartments enriched in phosphatidylinositol 3-phosphate and dynamically connected to the endoplasmic reticulum. J. Cell Biol. 2008, 182(4):685-701.
94. Appenzeller-Herzog C., Hall M.N. Bidirectional crosstalk between endoplasmic reticulum stress and mTOR signaling. Trends Cell Biol. 2012, 22(5):274-282.
95. Wang X., Proud C.G. The mTOR pathway in the control of protein synthesis. Physiology 2006, 21(4):362-369.
96. Bachar E., et al. Glucose amplifies fatty acid-induced endoplasmic reticulum stress in pancreatic beta-cells via activation of mTORC1. PLoS One 2009, 4(3).
97. Kato H., et al. mTORC1 serves ER stress-triggered apoptosis via selective activation of the IRE1-JNK pathway. Cell Death Differ. 2012, 19(2):310-320.
98. Ozcan U., et al. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol. Cell 2008, 29(5):541-551.
99. Ito N., et al. mTORC1 activation triggers the unfolded protein response in podocytes and leads to nephrotic syndrome. Lab. Investig. 2011, 91(11):1584-1595.
100. Nakajima S., et al. Selective abrogation of BiP/GRP78 blunts activation of NF-kappaB through the ATF6 branch of the UPR: involvement of C/EBPbeta and mTOR-dependent dephosphorylation of Akt. Mol. Cell. Biol. 2011, 31(8):1710-1718.
101. Qin L., et al. ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 2010, 6(2):239-247.
102. Manning B.D., et al. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/Akt pathway. Mol. Cell 2002, 10(1):151-162.
103. Di Nardo A., et al. Tuberous sclerosis complex activity is required to control neuronal stress responses in an mTOR-dependent manner. J. Neurosci. 2009, 29(18):5926-5937.
104. Malhotra J.D., Kaufman R.J. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword?. Antioxid. Redox Signal. 2007, 9(12):2277-2293.
105. Cao S.S., Kaufman R.J. Unfolded protein response. Curr. Biol. 2012, 22(16):R622-R626.
106. Santos C.X.C., et al. Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid. Redox Signal. 2009, 11(10):2409-2427.
107. Brand M.D. The sites and topology of mitochondrial superoxide production. Exp. Gerontol. 2010, 45(7-8):466-472.
108. Pollard M.G., Travers K.J., Weissman J.S. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell 1998, 1(2):171-182.
109. Han J., et al. ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 2013, 15(5):481-490.
110. Hasnain S.Z., Prins J.B., McGuckin M.A. Oxidative and endoplasmic reticulum stress in beta-cell dysfunction in diabetes. J. Mol. Endocrinol. 2016, 56(2):R33-R54.
111. Gilkerson R.W., et al. Mitochondrial autophagy in cells with mtDNA mutations results from synergistic loss of transmembrane potential and mTORC1 inhibition. Hum. Mol. Genet. 2012, 21(5):978-990.