Stress, the endoplasmic reticulum, and insulin resistance

Annals of the New York Academy of Sciences

Volumn 1083, Issue , 2006, Pages 63-76

  Tsiotra, Panayoula C ^a   Tsigos, Constantine ^a,b,c  

^a Hellenic National Center for the Research   (Greece)

^b UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^c NONE   (Greece)

Author keywords

Diabetes; Endoplasmic reticulum; Insulin resistance; Obesity; Stress

Indexed keywords

CATECHOLAMINE; GLUCOCORTICOID; INSULIN; PROTEIN;

APOPTOSIS; ATHEROSCLEROSIS; CHRONIC STRESS; CONFERENCE PAPER; ENDOPLASMIC RETICULUM; HEALTH HAZARD; HEAT SHOCK; HUMAN; INFLAMMATION; INSULIN RESISTANCE; LIPID STORAGE; METABOLIC SYNDROME X; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PATHOPHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN SYNTHESIS INHIBITION; TRANSCRIPTION INITIATION; VIRUS INFECTION;

EID: 33845722716     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1196/annals.1367.007     Document Type: Conference Paper

References (104)

1. CHROUSOS, G.P. & P.W. GOLD. 1992. The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis. JAMA 267: 1244-1252.
2. CHARMANDARI, E., C. TSIGOS & G. CHROUSOS. 2005. Endocrinology of the stress response. Annu. Rev. Physiol. 67: 259-284.
3. TSIGOS, C. & G.P. CHROUSOS. 1994. Physiology of the hypothalamic-pituitary-adrenal axis in health and in psychiatric and other disorders. Endocr. Metab. Clin. North Am. 23: 451-466.
4. TSIGOS, C. & G.P. CHROUSOS. 2002. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. J. Psychosom. Res. 53: 865-871.
5. BJORNTROP, P. & R. ROSMOND. 1999. Hypothalamic origin of the metabolic syndrome X. Ann. N. Y. Acad. Sci. 892: 297-307.
6. BJORNTROP, P. 1999. Neuroendocrine perturbations as a cause of insulin resistance. Diabetes Metab. Res. Rev. 15: 427-441.
7. ROSMOND, R & P. BJORNTROP. 2000. The hypothalamic-pituitary-adrenal axis activity as a predictor of cardiovascular disease, type 2 diabetes and stroke. J. Intern. Med. 247: 188-197.
8. STEPTOE, A. et al. 2001. Acute mental stress elicits delayed increases in circulating inflammatory cytokine levels. Clin. Sci. 101: 185-192.
9. BLACK, P.H. 2003. The inflammatory response is an integral part of the stress response: implications for atherosclerosis, insulin resistance, type II diabetes and metabolic syndrome X. Brain Behav. Immun. 17: 350-364.
10. SEEMATTER, G. et al. 2004. Relationship between stress, inflammation and metabolism. Curr. Opin. Clin. Nutr. Metab. Care 7: 169-173.
11. TRACEY, K.J. 2002. The inflammatory reflex. Nature 420: 853-859.
12. BIERHAUS, A. et al. 2003. A mechanism converting pychosocial stress into mononucler cell activation. Proc. Natl. Acad. Sci. USA 100: 1920-1925.
13. CLERK, A. et al. 1998. Stimulation of "stress-regulated" mitogen-activated protein kinases (stress-activated protein kinases/c-Jun N-terminal kinases and p38-mitogen-activated protein kinases) in perfused rat hearts by oxidative and other stresses. J. Biol. Chem. 273: 7228-7234.
14. BLAIR, A.S. et al. 1999. Regulation of glucose transport and glycogen synthesis in L6 muscle cells during oxidative stress. Evidence for cross-talk between the insulin and SAPK2/p38 mitogen-activated protein kinase signaling pathways. J. Biol. Chem. 274: 36293-36299.
15. MORIGI, M. et al. 1998. Leukocyte-endothelial interaction is augmented by high glucose concentrations and hyperglycemia in a NF-kB-dependent fashion. J. Clin. Invest. 101: 1905-1915.
16. PERALDI, P., M. XU, & B.M. SPIEGELMAN. 1997. Thiazolidinediones block tumor necrosis factor-α-induced inhibition of insulin signaling. J. Clin. Invest. 100: 1863-1869.
17. KHARROUBI, I. et al. 2004. Free fatty acids and cytokines induce pancreatic β-cell apoptosis by different mechanisms: role of nuclear factor-κB and endoplasmic reticulum stress. Endocrinology 145: 5087-5096.
18. EVANS, J.L. et al. 2002. Oxidative stress and stress-activated signaling pathways: a unifying hypothesis of type 2 diabetes. Endocr. Rev. 23: 599-622.
19. SHOELSON, S.E., J. LEE, & M. YUAN. 2003. Inflammation and the IKKB/IκB/NF-κB axis in obesity- and diet-induced insulin resistance. Int. J. Obes. Relat. Metab. Disord. 27: S49-S52.
20. SCHMIDT, A.M. & D.M. STERN. 2000. Hyperinsulinemia and vascular dysfunction: the role of nuclear factor-κB, yet again. Circ. Res. 87: 722-724.
21. KOPP, E. & S. GHOSH. 1994. Inhibition of NF-kappa B by sodium salicylate and aspirin. Science 265: 956-959.
22. YUAN, M. et al. 2001. Reversal of obesity- and diet-induced insulin resistance with salicylates or targeted disruption of Ikkβ. Science 293: 1673-1677.
23. UYSAL, K.T. et al. 1997. Protection from obesity-induced insulin resistance in mice lacking TNFA-α function. Nature 389: 610-614.
24. GRIMBLE, R.F. 2002. Inflammatory status and insulin resistance. Curr. Opin. Clin. Nutr. Metab. Care 5: 551-559.
25. WEISBERG, S.P. et al. 2003. Obesity is associated with macrophage accumulation in adipose tissue. J. Clin. Invest. 112: 1796-1808.
26. XU, H. et al. 2003. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J. Clin. Invest. 112: 1821-1830.
27. LEHRKE, M. & M.A. LAZAR. 2004. Inflamed about obesity. Nat. Med. 10: 126-127.
28. WELLEN, K.P. & G.H. HOTAMISLIGIL. 2005. Inflammation, stress and diabetes. J. Clin. Invest. 115: 1111-1119.
29. MAEDA, K. et al. 2005. Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes. Cell Metab. 1: 107-119.
30. MAKOWSKI, L. & G.H. HOTAMISLIGIL.2004. Fatty acid binding proteins - the evolutionary crossroads of inflammatory and metabolic responses. J. Nutr. 134: 2464S-2468S.
31. CHROUSOS, G.P. 2000. The role of stress and the hypothalamic-pituitary- adrenal axis in the pathogenesis of the metabolic syndrome: neuro-endocrine and target tissue-related causes. Int. J. Obes. Relat. Metab. Disord. 24: S50-S55.
32. ROSMOND, R., M.F. DALLMAN & P. BJÖRNTORP. 1998. Stress-related cortisol secretion in men: relationships with abdominal obesity and endocrine, metabolic and hemodynamic abnormalities. J. Clin. Endocr. Metab. 83: 1853-1859.
33. TSIGOS, C. & G.P. CHROUSOS. 1996. Differential diagnosis and management of Cushing's syndrome. Annu. Rev. Med. 47: 443-61.
34. TSIGOS, C., J. KYROU & G.P. CHROUSOS. 2004. Stress, endocrine physiology and pathophysiology. In L. DeGroot Ed. Available at www.endotext.org (Section Adrenal Glands and Function).
35. RAIKKONEN, K., A. HAUTANEN & L. KELTIKANGAS-JARVINEN. 1994. Association of stress and depression with regional fat distribution in healthy middle-aged men. J. Behav. Med. 17: 605-616.
36. PASQUALI, R. et al. 1993. The hypothalamic-pituitary-adrenal axis in obese women with different patterns of body fat distribution. J. Clin. Endocr. Metab. 77: 341-346.
37. LISSAU, I. & T.I. SORENSEN. 1994. Parental neglect during childhood and increased risk of obesity in young adulthood. Lancet 343: 324-327.
38. BJORNTROP, P. 2001. Do stress reactions cause abdominal obesity and comorbidities? Obes. Rev. 2: 73-86.
39. KANAKA-GANTENBEIN, C., G. MASTORAKOS & G.P. CHROUSOS. 2003. Endocrine-related causes and consequences of intrauterine growth retardation. Ann. N. Y. Acad. Sci. 997: 150-157.
40. ORBAN, Z. et al. 1999. The differential effect of food intake and β-adrenergic stimulation on adipose-derived hormones and cytokines in man. J. Clin. Endocr. Metab. 84: 2126-2133.
41. TSIGOS, C. et al. 1999. Circulating tumor necrosis factor a levels are higher in abdominal than peripheral obesity. Metabolism 48: 1332-1335.
42. WU, G., P. BROUCKAERT & T. OLIVECRONA. 2004. Rapid downregulation of adipose tissue lipoprotein lipase activity on food deprivation: evidence that TNF-alpha is involved. Am. J. Physiol. Endocrinol. Metab. 286: E711-E717.
43. GREENBERG, A.S. et al. 1992. Interleukin 6 reduces lipoprotein lipase activity in adipose tissue of mice in vivo and in 3T3-L1 adipocytes: a possible role for interleukin 6 in cancer cachexia. Cancer Res. 52: 4113-4116.
44. YU, C. et al. 2002. Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J. Biol. Chem. 277: 50230-50236.
45. GAO, Z. et al. 2004. Inhibition of insulin sensitivity by free fatty acids requires activation of multiple serine kinases in 3T3-L1 adipocytes. Mol. Endocrinol. 18: 2024-2034.
46. TRIPATHY, D. et al. 2003. Elevation of free fatty acids induces inflammation and impairs vascular reactivity in healthy subjects. Diabetes 52: 2882-2887.
47. GHANIM, H. et al. 2004. Circulating mononuclear cells in the obese are in a proinflammatory state. Circulation 110: 1564-1571.
48. AJUWON, K.M. & M.E. SPURLOCK. 2005. Palmitate activates the NF-kappaB transcription factor and induces IL-6 and TNFalpha expression in 3T3-L1 adipocytes. J. Nutr. 135: 1841-1846.
49. KIM, J.K. et al. 2001. Prevention of fat-induced insulin resistance by salicylate. J. Clin. Invest. 108: 437-446.
50. PASQUALI, R. & V. VINCENNATI. 2000. Activity of the hypothalamic-pituitary-adrenal axis in different obesity phenotypes. Int. J. Obes. Relat. Metab. Disord. 24: S47-S49.
51. MOHAMED-ALI, V., J.H. PINKNEY & S.W. COPPACK. 1998. Adipose tissue as an endocrine and paracrine organ. Int. J. Obes. Relat. Metab. Disord. 22: 1145-1158.
52. MOHAMED-ALI, V. et al. 2000. β-adrenergic regulation of proinflammatory cytokines in humans. Int. J. Obes. Relat. Metab. Disord. 24(Suppl 2): S154-S155.
53. MYERS, M.G., Jr. & M.F. WHITE. 1993. The new elements of insulin signaling. Insulin receptor substrate-1 and proteins with SH2 domains. Diabetes 42: 643-650.
54. HOTAMISLIGIL, G.S. 1999. The role of TNFalpha and TNF receptors in obesity and insulin resistance. J. Intern. Med. 245: 621-625.
55. AGUIRRE, V. et al. 2002. Phosphorylation of Ser307 in insulin receptor substrate-1 blocks interactions with the insulin receptor and inhibits insulin action. J. Biol. Chem. 277: 1531-1537.
56. GUAL, P., Y. LE MARCHAND-BRUSTEL & J.F. TANTI. 2005. Positive and negative regulation of insulin signaling through IRS-1 phosphorylation. Biochimie 87: 99-109.
57. HOTAMISLIGIL, G.S. et al. 1996. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-alpha- and obesity-induced insulin resistance. Science 271: 665-668.
58. SESTI, G. et al. 2001. Defects of the insulin receptor substrate (IRS) system in human metabolic disorders. FASEB J. 15: 2099-2111.
59. KYRIAKIS, J.M. & J. AVRUCH. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81: 807-869.
60. KYRIAKIS, J.M. et al. 1994. The stress-activated protein kinase subfamily of c-Jun kinases. Nature 369: 156-160.
61. HIROSUMI, J. et al. 2002. A central role for JNK in obesity and insulin resistance. Nature 420: 333-336.
62. URANO, F. et al. 2000. Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1. Science 287: 664-666.
63. KAUFMAN, R.J. 1999. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Gene Dev. 13: 1211-1233.
64. KAUFMAN, R.J. 2002. Orchestrating the unfolded protein response in health and disease. J. Clin. Invest. 110: 1389-1398.
65. HARDING, H.P. et al. 2002. Transcriptional and translational control in the mammalian unfolded protein response. Annu. Rev. Cell Dev. Biol. 18: 575-599.
66. RUTKOWSKI, D.T. & R.J. KAUFMAN. 2004. A trip to the ER: coping with stress. Trends Cell Biol. 14: 20-28.
67. SCHRODER, M. & R.J. KAUFMAN. 2005. ER stress and the unfolded protein response. Mutat. Res. 569: 29-63.
68. XU, C., B. BAILLY-MAITRE & J.C. REED. 2005. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 115: 2656-2664.
69. RON, D. 2002. Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110: 1383-1388.
70. SIDRAUSKI, C. & P. WALTER. 1997. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90: 1031-1039.
71. YOSHIDA, H. et al. 2000. ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol. Cell Biol. 20: 6755-6767.
72. HORWICH, A. et al. 2002. Protein aggregation in disease: a role for folding intermediates forming specific multimeric interactions. J. Clin. Invest. 110: 1221-1232.
73. WANG, X.Z. et al. 1996. Signals from the stressed endoplasmic reticulum induce C/EBP-homologous protein (CHOP/GADD153). Mol. Cell Biol. 16: 4273-4280.
74. YOSHIDA, H. et al. 2001. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107: 881-891.
75. HARDING, H.P., Y. ZHANG & D. RON. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
76. HARDING, H.P. et al. 2000. Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5: 897-904.
77. HARDING, H.P. et al. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell. 6: 1099-1108.
78. MA, Y. & L.M. HENDERSHOT. 2001. The unfolding tale of the unfolded protein response. Cell 107: 827-830.
79. MA, Y. et al. 2002. Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318: 1351-1365.
80. HARDING, H.P. et al. 2001. Diabetes mellitus and exocrine pancreatic dysfunction in perk-/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7: 1153-1163.
81. WOLCOTT, C.D. & M.L. RALLISON. 1972. Infancy-onset diabetes mellitus and multiple epiphyseal dysplasia. J. Pediatr. 80: 292-297.
82. SCHEUNER, D. et al. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7: 1165-1176.
83. SONENBERG, N. & C.B. NEWGARD. 2001. Protein synthesis. The perks of balancing glucose. Science 293: 818-819.
84. WANG, J. et al. 1999. A mutation in the insulin 2 gene induces diabetes with severe pancreatic β-cell dysfunction in the Mody mouse. J. Clin. Invest. 103: 27-37.
85. ALLEN, J.R. et al. 2004. High ER stress in β-cells stimulates intracellular degradation of misfolded insulin. Biochem. Biophys. Res. Commun. 324: 166-170.
86. NOZAKI, J. et al. 2004. 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 9: 261-270.
87. OYADOMARI, S. et al. 2002. Targeted disruption of the Chop gene delays endoplasmic reticulum stress-mediated diabetes. J. Clin. Invest. 109: 525-532.
88. ARAKI, E., S. OYADOMARI & M. MORI. 2003. Impact of endoplasmic reticulum stress pathway on pancreatic beta-cells and diabetes mellitus. Exp. Biol. Med. (Maywood). 228: 1213-1217.
89. OZAWA, K. et al. 2005. The endoplasmic reticulum chaperone improves insulin resistance in type 2 diabetes. Diabetes 54: 657-663.
90. LADIGES, W.K. et al. 2005. Pancreatic beta-cell failure and diabetes in mice with a deletion mutation of the endoplasmic reticulum molecular chaperone gene P58IPK. Diabetes 54: 1074-1081.
91. OYADOMARI, S., E. ARAKI & M. MORI. 2002. Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells. Apoptosis 7: 335-345.
92. KHARROUBI, I. et al. 2004. Free fatty acids and cytokines induce pancreatic beta-cell apoptosis by different mechanisms: role of nuclear factor-kappaB and endoplasmic reticulum stress. Endocrinology 145: 5087-5096.
93. CARDOZO, A.K. et al. 2005. Cytokines downregulate the sarcoendoplasmic reticulum pump Ca2+ ATPase 2b and deplete endoplasmic reticulum Ca2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 54: 452-461.
94. KANETO, H. et al. 2005. Oxidative stress, ER stress, and the INK pathway in type 2 diabetes. J. Mol. Med. 83: 429-439.
95. WANG, H., G. KOURI & C.B. WOLLHEIM. 2005. ER stress and SREBP-1 activation are implicated in {beta}-cell glucolipotoxicity. J. Cell. Sci. 118: 3905-3915.
96. MUOIO, D.M. & C.B. NEWGARD. 2004. Biomedicine. Insulin resistance takes a trip through the ER. Science 306: 425-426.
97. OZCAN, U. et al. 2004. Endoplasmic reticulum stress links obesity, insulin action, and Type 2 diabetes. Science 306: 457-461.
98. HARDING, H.P. & D. RON. 2002. Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51(Suppl 3): S455-S461.
99. OYADOMARI, S. & M. MORI. 2004. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11: 381-389.
100. KANETO, H. et al. 2005. Role of oxidative stress, endoplasmic reticulum stress, and c-Jun N-terminal kinase in pancreatic beta-cell dysfunction and insulin resistance. Int. J. Biochem. Cell Biol. 37: 1595-1608.
101. KANETO, H. et al. 2004. Possible novel therapy for diabetes with cell-permeable JNK-inhibitory peptide. Nat. Med. 10: 1128-1132.
102. WISEMAN, R.L. & W.E. BALCH. 2005. A new pharmacology-drugging stressed folding pathways. Trends Mol. Med. 11: 347-350.
103. BOYCE, M. et al. 2005. A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307: 935-939.
104. NAKATANI, Y. et al. 2005. Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J. Biol. Chem. 280: 847-851.