Table of Contents Author Guidelines Submit a Manuscript
Table of Contents Alerts

To receive news and publication updates for Journal of Diabetes Research, enter your email address in the box below.

Experimental Diabetes Research
Volume 2012 (2012), Article ID 187018, 11 pages
http://dx.doi.org/10.1155/2012/187018
Review Article

The Role of Glucosamine-Induced ER Stress in Diabetic Atherogenesis

Daniel R. Beriault1,2 and Geoff H. Werstuck1,2,3

1Thrombosis and Atherosclerosis Research Institute, McMaster University, 237 Barton Street East, Hamilton, ON, Canada L8L 2X2
2Department of Biochemistry and Biomedical Sciences, McMaster University, Hamilton, ON, Canada L8N 3Z5
3Department of Medicine, McMaster University, Hamilton, ON, Canada L8N 3Z5

Received 29 July 2011; Accepted 27 November 2011

Academic Editor: Muthuswamy Balasubramanyam

Copyright © 2012 Daniel R. Beriault and Geoff H. Werstuck. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. S. Yusuf, S. Hawken, S. Ôunpuu et al., “Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study,” The Lancet, vol. 364, no. 9438, pp. 937–952, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Yusuf, S. Reddy, S. Ôunpuu, and S. Anand, “Global burden of cardiovascular diseases. Part I: general considerations, the epidemiologic transition, risk factors, and impact of urbanization,” Circulation, vol. 104, no. 22, pp. 2746–2753, 2001. View at Google Scholar · View at Scopus
  3. G. Danaei, M. M. Finucane, Y. Lu et al., “National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2·7 million participants,” The Lancet, vol. 378, no. 9785, pp. 31–40, 2011. View at Publisher · View at Google Scholar
  4. P. Hossain, B. Kawar, and M. El Nahas, “Obesity and diabetes in the developing world—a growing challenge,” The New England Journal of Medicine, vol. 356, no. 3, pp. 213–215, 2007. View at Publisher · View at Google Scholar · View at Scopus
  5. S. M. Haffner, S. Lehto, T. Ronnemaa, K. Pyorala, and M. Laakso, “Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction,” The New England Journal of Medicine, vol. 339, no. 4, pp. 229–234, 1998. View at Publisher · View at Google Scholar · View at Scopus
  6. H. C. Gerstein, K. Malmberg, S. Capes, and S. Yusuf, “Cardiovascular diseases,” in Evidence-Based Diabetes Care, H. C. Gerstein and R. B. Haynes, Eds., pp. 488–514, BC Decker, Ontario, Canada, 2001. View at Google Scholar
  7. S. Lehto, T. Ronnemaa, K. Pyorala, and M. Laakso, “Cardiovascular risk factors clustering with endogenous hyperinsulinemia predict death from coronary heart disease in patients with Type II diabetes,” Diabetologia, vol. 43, no. 2, pp. 148–155, 2000. View at Google Scholar
  8. R. J. W. Middelbeek and E. S. Horton, “The role of glucose as an independent cardiovascular risk factor,” Current Diabetes Reports, vol. 7, no. 1, pp. 43–49, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Selvin, J. Coresh, S. H. Golden, F. L. Brancati, A. R. Folsom, and M. W. Steffes, “Glycemic control and coronary heart disease risk in persons with and without diabetes: the atherosclerosis risk in communities study,” Archives of Internal Medicine, vol. 165, no. 16, pp. 1910–1916, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. H. C. Gerstein, M. E. Miller, R. P. Byington et al., “Effects of intensive glucose lowering in type 2 diabetes,” The New England Journal of Medicine, vol. 358, no. 24, pp. 2545–2559, 2008. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Patel, S. MacMahon, J. Chalmers et al., “Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes,” The New England Journal of Medicine, vol. 358, no. 24, pp. 2560–2572, 2008. View at Publisher · View at Google Scholar · View at Scopus
  12. R. R. Holman, S. K. Paul, M. A. Bethel, H. A. W. Neil, and D. R. Matthews, “Long-term follow-up after tight control of blood pressure in type 2 diabetes,” The New England Journal of Medicine, vol. 359, no. 15, pp. 1565–1576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. W. Duckworth, C. Abraira, T. Moritz et al., “Glucose control and vascular complications in veterans with type 2 diabetes,” The New England Journal of Medicine, vol. 360, no. 2, pp. 129–139, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. D. M. Nathan, J. Lachin, P. Cleary et al., “Intensive diabetes therapy and carotid intima-media thickness in type 1 diabetes mellitus,” The New England Journal of Medicine, vol. 348, no. 23, pp. 2294–2303, 2003. View at Publisher · View at Google Scholar
  15. R. Turner, “Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33),” The Lancet, vol. 352, no. 9131, pp. 837–853, 1998. View at Publisher · View at Google Scholar
  16. S. M. Haffner, “The importance of hyperglycemia in the nonfasting state to the development of cardiovascular disease,” Endocrine Reviews, vol. 19, no. 5, pp. 583–592, 1998. View at Publisher · View at Google Scholar · View at Scopus
  17. E. Standl, B. Balletshofer, B. Dahl et al., “Predictors of 10-year macrovascular and overall mortality in patients with NIDDM: the Munich General Practitioner Project,” Diabetologia, vol. 39, no. 12, pp. 1540–1545, 1996. View at Publisher · View at Google Scholar · View at Scopus
  18. S. Lehto, T. Ronnemaa, S. M. Haffner, K. Pyorala, V. Kallio, and M. Laakso, “Dyslipidemia and hyperglycemia predict coronary heart disease events in middle-aged patients with NIDDM,” Diabetes, vol. 46, no. 8, pp. 1354–1359, 1997. View at Google Scholar · View at Scopus
  19. S. M. Santilli, V. D. Fiegel, D. E. Aldridge, and D. R. Knighton, “The effect of diabetes on the proliferation of aortic endothelial cells,” Annals of Vascular Surgery, vol. 6, no. 6, pp. 503–510, 1992. View at Publisher · View at Google Scholar · View at Scopus
  20. F. C. Huvers, P. W. De Leeuw, A. J. H. M. Houben et al., “Endothelium-dependent vasodilatation, plasma markers of endothelial function, and adrenergic vasoconstrictor responses in type 1 diabetes under near-normoglycemic conditions,” Diabetes, vol. 48, no. 6, pp. 1300–1307, 2000. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Quagliaro, L. Piconi, R. Assaloni, L. Martinelli, E. Motz, and A. Ceriello, “Intermittent high glucose enhances apoptosis related to oxidative stress in human umbilical vein endothelial cells: the role of protein kinase C and NAD(P)H-oxidase activation,” Diabetes, vol. 52, no. 11, pp. 2795–2804, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. S. M. Grundy, H. B. Brewer, J. I. Cleeman, S. C. Smith Jr., and C. Lenfant, “Definition of metabolic syndrome: report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition,” Circulation, vol. 109, no. 3, pp. 433–438, 2004. View at Publisher · View at Google Scholar · View at Scopus
  23. World Health Organization, “Obesity: preventing and managing the global epidemic,” WHO Technical Report Series, no. 894, 2003. View at Google Scholar
  24. S. M. Grundy, “Metabolic complications of obesity,” Endocrine, vol. 13, no. 2, pp. 155–165, 2000. View at Google Scholar · View at Scopus
  25. A. Y. W. Lee and S. S. M. Chung, “Contributions of polyol pathway to oxidative stress in diabetic cataract,” The FASEB Journal, vol. 13, no. 1, pp. 23–30, 1999. View at Google Scholar · View at Scopus
  26. C. A. Gleissner, J. M. Sanders, J. Nadler, and K. Ley, “Upregulation of aldose reductase during foam cell formation as possible link among diabetes, hyperlipidemia, and atherosclerosis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 28, no. 6, pp. 1137–1143, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. B. Tesfamariam, M. L. Brown, and R. A. Cohen, “Elevated glucose impairs endothelium-dependent relaxation by activating protein kinase C,” The Journal of Clinical Investigation, vol. 87, no. 5, pp. 1643–1648, 1991. View at Google Scholar · View at Scopus
  28. T. Inoguchi, P. Li, F. Umeda et al., “High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells,” Diabetes, vol. 49, no. 11, pp. 1939–1945, 2000. View at Google Scholar · View at Scopus
  29. K. J. Wells-Knecht, D. V. Zyzak, J. E. Litchfield, S. R. Thorpe, and J. W. Baynes, “Mechanism of autoxidative glycosylation: identification of glyoxal and arabinose as intermediates in the autoxidative modification of proteins by glucose,” Biochemistry, vol. 34, no. 11, pp. 3702–3709, 1995. View at Publisher · View at Google Scholar · View at Scopus
  30. T. P. Degenhardt, S. R. Thorpe, and J. W. Baynes, “Chemical modification of proteins by methylglyoxal,” Cellular and Molecular Biology, vol. 44, no. 7, pp. 1139–1145, 1998. View at Google Scholar · View at Scopus
  31. J. Liu, M. R. Masurekar, D. E. Vatner et al., “Glycation end-product cross-link breaker reduces collagen and improves cardiac function in aging diabetic heart,” American Journal of Physiology, vol. 285, no. 6, pp. H2587–H2591, 2003. View at Google Scholar · View at Scopus
  32. S. Tanaka, G. Avigad, B. Brodsky, and E. F. Eikenberry, “Glycation induces expansion of the molecular packing of collagen,” Journal of Molecular Biology, vol. 203, no. 2, pp. 495–505, 1988. View at Google Scholar · View at Scopus
  33. M. Neeper, A. M. Schmidt, J. Brett et al., “Cloning and expression of a cell surface receptor for advanced glycosylation end products of proteins,” The Journal of Biological Chemistry, vol. 267, no. 21, pp. 14998–15004, 1992. View at Google Scholar · View at Scopus
  34. Y. M. Li, T. Mitsuhashi, D. Wojciechowicz et al., “Molecular identity and cellular distribution of advanced glycation endproduct receptors: relationship of p60 to OST-48 and p90 to 80K-H membrane proteins,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 20, pp. 11047–11052, 1996. View at Publisher · View at Google Scholar · View at Scopus
  35. B. Smedsrod, J. Melkko, N. Araki, H. Sano, and S. Horiuchi, “Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells,” Biochemical Journal, vol. 322, part 2, pp. 567–573, 1997. View at Google Scholar · View at Scopus
  36. M. A. Hofmann, E. Lalla, Y. Lu et al., “Hyperhomocysteinemia enhances vascular inflammation and accelerates atherosclerosis in a murine model,” The Journal of Clinical Investigation, vol. 107, no. 6, pp. 675–683, 2001. View at Google Scholar · View at Scopus
  37. M. Brownlee, “The pathobiology of diabetic complications: a unifying mechanism,” Diabetes, vol. 54, no. 6, pp. 1615–1625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. S. V. Brodsky, O. Gealekman, J. Chen et al., “Prevention and reversal of premature endothelial cell senescence and vasculopathy in obesity-induced diabetes by ebselen,” Circulation Research, vol. 94, no. 3, pp. 377–384, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. A. M. Schmidt, O. Hori, Jing Xian Chen et al., “Advanced glycation endproducts interacting with their endothelial receptor induce expression of vascular cell adhesion molecule-1 (VCAM-1) in cultured human endothelial cells and in mice: a potential mechanism for the accelerated vasculopathy of diabetes,” The Journal of Clinical Investigation, vol. 96, no. 3, pp. 1395–1403, 1995. View at Google Scholar · View at Scopus
  40. L. G. Bucciarelli, T. Wendt, W. Qu et al., “RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice,” Circulation, vol. 106, no. 22, pp. 2827–2835, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. A. Soro-Paavonen, A. M. D. Watson, J. Li et al., “Receptor for advanced glycation end products (RAGE) deficiency attenuates the development of atherosclerosis in diabetes,” Diabetes, vol. 57, no. 9, pp. 2461–2469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. H. C. Gerstein, S. Yusuf, J. F. E. Mann et al., “Effects of ramipril on cardiovascular and microvascular outcomes in people with diabetes mellitus: results of the HOPE study and MICRO-HOPE substudy,” The Lancet, vol. 355, no. 9200, pp. 253–259, 2000. View at Publisher · View at Google Scholar
  43. E. M. Lonn, S. Yusuf, V. Dzavik et al., “Effects of Ramipril and vitamin E on atherosclerosis: the Study to Evaluate Carotid Ultrasound changes in patients treated with Ramipril and vitamin E (SECURE),” Circulation, vol. 103, no. 7, pp. 919–925, 2001. View at Google Scholar · View at Scopus
  44. B. M. McQuillan, J. Hung, J. P. Beilby, M. Nidorf, and P. L. Thompson, “Antioxidant vitamins and the risk of carotid atherosclerosis: the perth carotid ultrasound disease assessment study (CUDAS),” Journal of the American College of Cardiology, vol. 38, no. 7, pp. 1788–1794, 2001. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Lonn, “Effects of long-term vitamin E supplementation on cardiovascular events and cancer: a randomized controlled trial,” JAMA, vol. 293, no. 11, pp. 1338–1347, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. M. J. Thomson, V. Puntmann, and J. C. Kaski, “Atherosclerosis and oxidant stress: the end of the road for antioxidant vitamin treatment?” Cardiovascular Drugs and Therapy, vol. 21, no. 3, pp. 195–210, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. S. Marshall, V. Bacote, and R. R. Traxinger, “Discovery of a metabolic pathway mediating glucose-induced desensitization of the glucose transport system: role of hexosamine in the induction of insulin resistance,” The Journal of Biological Chemistry, vol. 266, no. 8, pp. 4706–4712, 1991. View at Google Scholar · View at Scopus
  48. A. G. Nerlich, U. Sauer, V. Kolm-Litty, E. Wagner, M. Koch, and E. D. Schleicher, “Expression of glutamine:fructose-6-phosphate amidotransferase in human tissues: evidence for high variability and distinct regulation in diabetes,” Diabetes, vol. 47, no. 2, pp. 170–178, 1998. View at Google Scholar · View at Scopus
  49. G. H. Werstuck, M. I. Khan, G. Femia et al., “Glucosamine-induced endoplasmic reticulum dysfunction is associated with accelerated atherosclerosis in a hyperglycemic mouse model,” Diabetes, vol. 55, no. 1, pp. 93–101, 2006. View at Publisher · View at Google Scholar · View at Scopus
  50. M. I. Khan, B. A. Pichna, Y. Shi, A. J. Bowes, and G. H. Werstuck, “Evidence supporting a role for endoplasmic reticulum stress in the development of atherosclerosis in a hyperglycaemic mouse model,” Antioxidants and Redox Signaling, vol. 11, no. 9, pp. 2289–2298, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. N. Fülöp, M. M. Mason, K. Dutta et al., “Impact of Type 2 diabetes and aging on cardiomyocyte function and O-linked N-acetylglucosamine levels in the heart,” American Journal of Physiology, vol. 292, no. 4, pp. C1370–C1378, 2007. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Wu, T. E. Haynes, W. Yan, and C. J. Meininger, “Presence of glutamine:fructose-6-phosphate amidotransferase for glucosamine-6-phosphate synthesis in endothelial cells: effects of hyperglycaemia and glutamine,” Diabetologia, vol. 44, no. 2, pp. 196–202, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. G. Veerababu, J. Tang, R. T. Hoffman et al., “Overexpression of glutamine:fructose-6-phosphate amidotransferase in the liver of transgenic mice results in enhanced glycogen storage, hyperlipidemia, obesity, and impaired glucose tolerance,” Diabetes, vol. 49, no. 12, pp. 2070–2078, 2000. View at Google Scholar · View at Scopus
  54. K. Liu, A. J. Paterson, E. Chin, and J. E. Kudlow, “Glucose stimulates protein modification by O-linked GlcNAc in pancreatic β cells: linkage of O-linked GlcNAc to β cell death,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 6, pp. 2820–2825, 2000. View at Google Scholar · View at Scopus
  55. S. Stender and P. Astrup, “Glucosamine and experimental atherosclerosis. Increased wet weight and changed composition of cholesterol fatty acids in aorta of rabbits fed a cholesterol enriched diet with added glucosamine,” Atherosclerosis, vol. 26, no. 2, pp. 205–213, 1977. View at Google Scholar · View at Scopus
  56. G. Majumdar, A. Harmon, R. Candelaria, A. Martinez-Hernandez, R. Raghow, and S. S. Solomon, “O-glycosylation of Sp1 and transcriptional regulation of the calmodulin gene by insulin and glucagon,” American Journal of Physiology, vol. 285, no. 3, pp. E584–E591, 2003. View at Google Scholar
  57. I. Han, E. S. Oh, and J. E. Kudlow, “Responsiveness of the state of O-linked N-acetylglucosamine modification of nuclear pore protein p62 to the extracellular glucose concentration,” Biochemical Journal, vol. 350, no. 1, pp. 109–114, 2000. View at Publisher · View at Google Scholar · View at Scopus
  58. X. L. Du, D. Edelstein, S. Dimmeler, Q. Ju, C. Sui, and M. Brownlee, “Hyperglycemia inhibits endothelial nitric oxide synthase activity by posttranslational modification at the Akt site,” The Journal of Clinical Investigation, vol. 108, no. 9, pp. 1341–1348, 2001. View at Publisher · View at Google Scholar · View at Scopus
  59. S. P. Jackson and R. Tjian, “O-glycosylation of eukaryotic transcription factors: implications for mechanisms of transcriptional regulation,” Cell, vol. 55, no. 1, pp. 125–133, 1988. View at Google Scholar · View at Scopus
  60. K. T. B. G. Schjoldager, M. B. Vester-Christensen, E. P. Bennett et al., “O-glycosylation modulates proprotein convertase activation of angiopoietin-like protein 3: possible role of polypeptide GalNAc-transferase-2 in regulation of concentrations of plasma lipids,” The Journal of Biological Chemistry, vol. 285, no. 47, pp. 36293–36303, 2010. View at Publisher · View at Google Scholar · View at Scopus
  61. M. Kuo, V. Zilberfarb, N. Gangneux, N. Christeff, and T. Issad, “O-glycosylation of FoxO1 increases its transcriptional activity towards the glucose 6-phosphatase gene,” FEBS Letters, vol. 582, no. 5, pp. 829–834, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. R. Dentin, S. Hedrick, J. Xie, J. Yates, and M. Montminy, “Hepatic glucose sensing via the CREB coactivator CRTC2,” Science, vol. 319, no. 5868, pp. 1402–1405, 2008. View at Publisher · View at Google Scholar · View at Scopus
  63. G. A. Ngoh, H. T. Facundo, A. Zafir, and S. P. Jones, “O-GlcNAc signaling in the cardiovascular system,” Circulation Research, vol. 107, no. 2, pp. 171–185, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. R. C. Cooksey and D. A. McClain, “Transgenic mice overexpressing the rate-limiting enzyme for hexosamine synthesis in skeletal muscle or adipose tissue exhibit total body insulin resistance,” Annals of the New York Academy of Sciences, vol. 967, pp. 102–111, 2002. View at Google Scholar · View at Scopus
  65. A. D. Baron, J. S. Zhu, J. H. Zhu, H. Weldon, L. Maianu, and W. T. Garvey, “Glucosamine induces insulin resistance in vivo by affecting GLUT 4 translocation in skeletal muscle. Implications for glucose toxicity,” The Journal of Clinical Investigation, vol. 96, no. 6, pp. 2792–2801, 1995. View at Google Scholar · View at Scopus
  66. V. Kolm-Litty, U. Sauer, A. Nerlich, R. Lehmann, and E. D. Schleicher, “High glucose-induced transforming growth factor β1 production is mediated by the hexosamine pathway in porcine glomerular mesangial cells,” The Journal of Clinical Investigation, vol. 101, no. 1, pp. 160–169, 1998. View at Google Scholar · View at Scopus
  67. M. C. Daniels, P. Kansal, T. M. Smith, A. J. Paterson, J. E. Kudlow, and D. A. McClain, “Glucose regulation of transforming growth factor-α expression is mediated by products of the hexosamine biosynthesis pathway,” Molecular Endocrinology, vol. 7, no. 8, pp. 1041–1048, 1993. View at Publisher · View at Google Scholar · View at Scopus
  68. I. Gabriely, X. M. Yang, J. A. Cases, X. H. Ma, L. Rossetti, and N. Barzilai, “Hyperglycemia induces PAI-1 gene expression in adipose tissue by activation of the hexosamine biosynthetic pathway,” Atherosclerosis, vol. 160, no. 1, pp. 115–122, 2002. View at Publisher · View at Google Scholar · View at Scopus
  69. A. Helenius, “How N-linked oligosaccharides affect glycoprotein folding in the endoplasmic reticulum,” Molecular Biology of the Cell, vol. 5, no. 3, pp. 253–265, 1994. View at Google Scholar · View at Scopus
  70. M. Bence and M. Sahin-Tõth, “Asparagine-linked glycosylation of human chymotrypsin C is required for folding and secretion but not for enzyme activity,” The FEBS Journal, vol. 278, no. 22, pp. 4338–4350, 2011. View at Publisher · View at Google Scholar
  71. N. Branza-Nichita, G. Negroiu, A. J. Petrescu et al., “Mutations at critical N-glycosylation sites reduce tyrosinase activity by altering folding and quality control,” The Journal of Biological Chemistry, vol. 275, no. 11, pp. 8169–8175, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. P. Wujek, E. Kida, M. Walus, K. E. Wisniewski, and A. A. Golabek, “N-glycosylation is crucial for folding, trafficking, and stability of human tripeptidyl-peptidase I,” The Journal of Biological Chemistry, vol. 279, no. 13, pp. 12827–12839, 2004. View at Publisher · View at Google Scholar · View at Scopus
  73. H. P. Harding, Y. Zhang, and D. Ron, “Protein translation and folding are coupled by an endoplasmic- reticulum-resident kinase,” Nature, vol. 397, no. 6716, pp. 271–274, 1999. View at Publisher · View at Google Scholar · View at Scopus
  74. R. J. Kaufman, “Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls,” Genes and Development, vol. 13, no. 10, pp. 1211–1233, 1999. View at Google Scholar · View at Scopus
  75. M. J. Morin, C. W. Porter, P. McKernan, and R. J. Bernacki, “The biochemical and ultrastructural effects of tunicamycin and D-glucosamine in L1210 leukemic cells,” Journal of Cellular Physiology, vol. 114, no. 2, pp. 162–172, 1983. View at Google Scholar · View at Scopus
  76. H. Y. Lin, P. Masso-Welch, Y. P. Di, J. W. Cai, J. W. Shen, and J. R. Subjeck, “The 170-kDa glucose-regulated stress protein is an endoplasmic reticulum protein that binds immunoglobulin,” Molecular Biology of the Cell, vol. 4, no. 11, pp. 1109–1119, 1993. View at Google Scholar · View at Scopus
  77. D. Miskovic, L. Salter-Cid, N. Ohan, M. Flajnik, and J. J. Heikkila, “Isolation and characterization of a cDNA encoding a Xenopus immunoglobulin binding protein, BiP (Grp78),” Comparative Biochemistry and Physiology, vol. 116, no. 2, pp. 227–234, 1997. View at Publisher · View at Google Scholar · View at Scopus
  78. A. S. Lee, “The glucose-regulated proteins: stress induction and clinical applications,” Trends in Biochemical Sciences, vol. 26, no. 8, pp. 504–510, 2001. View at Publisher · View at Google Scholar · View at Scopus
  79. E. Lai, T. Teodoro, and A. Volchuk, “Endoplasmic reticulum stress: signaling the unfolded protein response,” Physiology, vol. 22, no. 3, pp. 193–201, 2007. View at Publisher · View at Google Scholar · View at Scopus
  80. E. Jamsa, M. Simonen, and M. Makarow, “Selective retention of secretory proteins in the yeast endoplasmic reticulum by treatment of cells with a reducing agent,” Yeast, vol. 10, no. 3, pp. 355–370, 1994. View at Google Scholar · View at Scopus
  81. W. W. Li, S. Alexandre, X. Cao, and A. S. Lee, “Transactivation of the grp78 promoter by Ca2+ depletion. A comparative analysis with A23187 and the endoplasmic reticulum Ca2+-ATPase inhibitor thapsigargin,” The Journal of Biological Chemistry, vol. 268, no. 16, pp. 12003–12009, 1993. View at Google Scholar
  82. N. M. Borradaile, X. Han, J. D. Harp, S. E. Gale, D. S. Ory, and J. E. Schaffer, “Disruption of endoplasmic reticulum structure and integrity in lipotoxic cell death,” Journal of Lipid Research, vol. 47, no. 12, pp. 2726–2737, 2006. View at Publisher · View at Google Scholar · View at Scopus
  83. T. DeVries-Seimon, Y. Li, M. Y. Pin et al., “Cholesterol-induced macrophage apoptosis requires ER stress pathways and engagement of the type A scavenger receptor,” Journal of Cell Biology, vol. 171, no. 1, pp. 61–73, 2005. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Feige and I. E. Scheffler, “Analysis of the protein glycosylation defect of a temperature-sensitive cell cycle mutant by the use of mutant cells overexpressing the human epidermal growth factor receptor after transfection of the gene,” Journal of Cellular Physiology, vol. 133, no. 3, pp. 461–470, 1987. View at Google Scholar · View at Scopus
  85. J. Wu and R. J. Kaufman, “From acute ER stress to physiological roles of the unfolded protein response,” Cell Death and Differentiation, vol. 13, no. 3, pp. 374–384, 2006. View at Publisher · View at Google Scholar · View at Scopus
  86. A. T. Sage, L. A. Walter, Y. Shi et al., “Hexosamine biosynthesis pathway flux promotes endoplasmic reticulum stress, lipid accumulation, and inflammatory gene expression in hepatic cells,” American Journal of Physiology, vol. 298, no. 3, pp. E499–E511, 2010. View at Publisher · View at Google Scholar
  87. J. N. Lee and J. Ye, “Proteolytic activation of sterol regulatory element-binding protein induced by cellular stress through depletion of Insig-1,” The Journal of Biological Chemistry, vol. 279, no. 43, pp. 45257–45265, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. G. H. Werstuck, S. R. Lentz, S. Dayal et al., “Homocysteine-induced endoplasmic reticulum stress causes dysregulation of the cholesterol and triglyceride biosynthetic pathways,” The Journal of Clinical Investigation, vol. 107, no. 10, pp. 1263–1273, 2001. View at Google Scholar · View at Scopus
  89. I. Tabas and D. Ron, “Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress,” Nature Cell Biology, vol. 13, no. 3, pp. 184–190, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. U. Özcan, Q. Cao, E. Yilmaz et al., “Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes,” Science, vol. 306, no. 5695, pp. 457–461, 2004. View at Publisher · View at Google Scholar · View at Scopus
  91. D. A. Cunha, P. Hekerman, L. Ladrière et al., “Initiation and execution of lipotoxic ER stress in pancreatic β-cells,” Journal of Cell Science, vol. 121, no. 14, pp. 2308–2318, 2008. View at Publisher · View at Google Scholar · View at Scopus
  92. Y. Li, R. F. Schwabe, T. DeVries-Seimon et al., “Free cholesterol-loaded macrophages are an abundant source of tumor necrosis factor-α and interleukin-6: model of NF-κB- and map kinase-dependent inflammation in advanced atherosclerosis,” The Journal of Biological Chemistry, vol. 280, no. 23, pp. 21763–21772, 2005. View at Publisher · View at Google Scholar · View at Scopus
  93. F. Ursini, K. J. A. Davies, M. Maiorino, T. Parasassi, and A. Sevanian, “Atherosclerosis: another protein misfolding disease?” Trends in Molecular Medicine, vol. 8, no. 8, pp. 370–374, 2002. View at Publisher · View at Google Scholar · View at Scopus
  94. M. Vasa-Nicotera, “The new kid on the block: the unfolded protein response in the pathogenesis of atherosclerosis,” Cell Death and Differentiation, vol. 11, no. 1, pp. S10–S11, 2004. View at Publisher · View at Google Scholar · View at Scopus
  95. J. Zhou, S. Lhotak, B. A. Hilditch, and R. C. Austin, “Activation of the unfolded protein response occurs at all stages of atherosclerotic lesion development in apolipoprotein E-deficient mice,” Circulation, vol. 111, no. 14, pp. 1814–1821, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. S. M. Colgan, D. Tang, G. H. Werstuck, and R. C. Austin, “Endoplasmic reticulum stress causes the activation of sterol regulatory element binding protein-2,” International Journal of Biochemistry and Cell Biology, vol. 39, no. 10, pp. 1843–1851, 2007. View at Publisher · View at Google Scholar · View at Scopus
  97. H. Shimano, J. D. Horton, R. E. Hammer, I. Shimomura, M. S. Brown, and J. L. Goldstein, “Overproduction of cholesterol and fatty acids causes massive liver enlargement in transgenic mice expressing truncated SREBP-1a,” The Journal of Clinical Investigation, vol. 98, no. 7, pp. 1575–1584, 1996. View at Google Scholar · View at Scopus
  98. H. L. Pahl and P. A. Baeurle, “A novel signal transduction pathway from the endoplasmic reticulum to the nucleus is mediated by transcription factor NF-κB,” The EMBO Journal, vol. 14, no. 11, pp. 2580–2588, 1995. View at Google Scholar · View at Scopus
  99. H. Y. Jiang, S. A. Wek, B. C. McGrath et al., “Phosphorylation of the α subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses,” Molecular and Cellular Biology, vol. 23, no. 16, pp. 5651–5663, 2003. View at Publisher · View at Google Scholar · View at Scopus
  100. A. J. Kim, Y. Shi, R. C. Austin, and G. H. Werstuck, “Valproate protects cells fom ER stress-induced lipid accumulation and apoptosis by inhibiting glycogen synthase kinase-3,” Journal of Cell Science, vol. 118, no. 1, pp. 89–99, 2005. View at Publisher · View at Google Scholar
  101. G. S. Hossain, J. V. Van Thienen, G. H. Werstuck et al., “TDAG51 is induced by homocysteine, promotes detachment-mediated programmed cell death, and contributes to the development of atherosclerosis in hyperhomocysteinemia,” The Journal of Biological Chemistry, vol. 278, no. 32, pp. 30317–30327, 2003. View at Publisher · View at Google Scholar · View at Scopus
  102. R. Ross, “Atherosclerosis—an inflammatory disease,” The New England Journal of Medicine, vol. 340, no. 2, pp. 115–126, 1999. View at Publisher · View at Google Scholar · View at Scopus
  103. A. J. Lusis, “Atherosclerosis,” Nature, vol. 407, no. 6801, pp. 233–241, 2000. View at Publisher · View at Google Scholar · View at Scopus
  104. W. Qiu, R. Kohen-Avramoglu, S. Mhapsekar, J. Tsai, R. C. Austin, and K. Adeli, “Glucósamine-induced endoplasmic reticulum stress promotes apoB100 degradation: evidence for Grp78-mediated targeting to proteasomal degradation,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 25, no. 3, pp. 571–577, 2005. View at Publisher · View at Google Scholar
  105. L. Rossetti, M. Hawkins, W. Chen, J. Gindi, and N. Barzilai, “In vivo glucosamine infusion induces insulin resistance in normoglycemic but not in hyperglycemic conscious rats,” The Journal of Clinical Investigation, vol. 96, no. 1, pp. 132–140, 1995. View at Google Scholar · View at Scopus
  106. G. A. Raciti, C. Iadicicco, L. Ulianich et al., “Glucosamine-induced endoplasmic reticulum stress affects GLUT4 expression via activating transcription factor 6 in rat and human skeletal muscle cells,” Diabetologia, vol. 53, no. 5, pp. 955–965, 2010. View at Publisher · View at Google Scholar · View at Scopus
  107. T. P. Ciaraldi, L. Carter, S. Nikoulina, S. Mudaliar, D. A. McClain, and R. R. Henry, “Glucosamine regulation of glucose metabolism in cultured human skeletal muscle cells: divergent effects on glucose transport/phosphorylation and glycogen synthase in non-diabetic and type 2 diabetic subjects,” Endocrinology, vol. 140, no. 9, pp. 3971–3980, 1999. View at Google Scholar · View at Scopus
  108. H. Chen, B. L. Ing, K. A. Robinson, A. C. Feagin, M. G. Buse, and M. J. Quon, “Effects of overexpression of glutamine:fructose-6-phosphate amidotransferase (GFAT) and glucosamine treatment on translocation of GLUT4 in rat adipose cells,” Molecular and Cellular Endocrinology, vol. 135, no. 1, pp. 67–77, 1997. View at Publisher · View at Google Scholar · View at Scopus
  109. M. Federici, R. Menghini, A. Mauriello et al., “Insulin-dependent activation of endothelial nitric oxide synthase is impaired by O-linked glycosylation modification of signaling proteins in human coronary endothelial cells,” Circulation, vol. 106, no. 4, pp. 466–472, 2002. View at Publisher · View at Google Scholar · View at Scopus
  110. M. G. Wallis, M. E. Smith, C. M. Kolka et al., “Acute glucosamine-induced insulin resistance in muscle in vivo is associated with impaired capillary recruitment,” Diabetologia, vol. 48, no. 10, pp. 2131–2139, 2005. View at Publisher · View at Google Scholar · View at Scopus
  111. T. Monauni, M. G. Zenti, A. Cretti et al., “Effects of glucosamine infusion on insulin secretion and insulin action in humans,” Diabetes, vol. 49, no. 6, pp. 926–935, 2000. View at Google Scholar · View at Scopus
  112. R. Muniyappa, R. J. Karne, G. Hall et al., “Oral glucosamine for 6 weeks at standard doses does not cause or worsen insulin resistance or endothelial dysfunction in lean or obese subjects,” Diabetes, vol. 55, no. 11, pp. 3142–3150, 2006. View at Publisher · View at Google Scholar · View at Scopus
  113. R. R. Simon, V. Marks, A. R. Leeds, and J. W. Anderson, “A comprehensive review of oral glucosamine use and effects on glucose metabolism in normal and diabetic individuals,” Diabetes/Metabolism Research and Reviews, vol. 27, no. 1, pp. 14–27, 2011. View at Publisher · View at Google Scholar · View at Scopus
  114. A. J. Bowes, M. I. Khan, Y. Shi, L. Robertson, and G. H. Werstuck, “Valproate attenuates accelerated atherosclerosis in hyperglycemic ApoE-deficient mice: evidence in support of a role for endoplasmic reticulum stress and glycogen synthase kinase-3 in lesion development and hepatic steatosis,” American Journal of Pathology, vol. 174, no. 1, pp. 330–342, 2009. View at Publisher · View at Google Scholar · View at Scopus
  115. D. R. Beriault, S. Sharma, Y. Shi, M. I. Khan, and G. H. Werstuck, “Glucosamine-supplementation promotes endoplasmic reticulum stress, hepatic steatosis and accelerated atherogenesis in apoE-/- mice,” Atherosclerosis, vol. 219, no. 1, pp. 134–140, 2011. View at Publisher · View at Google Scholar
  116. L. R. Tannock, E. A. Kirk, V. L. King, R. LeBoeuf, T. N. Wight, and A. Chait, “Glucosamine supplementation accelerates early but not late atherosclerosis in LDL receptor-deficient mice,” Journal of Nutrition, vol. 136, no. 11, pp. 2856–2861, 2006. View at Google Scholar · View at Scopus
  117. P. Prasad, A. K. Tiwari, K. M. P. Kumar et al., “Association analysis of ADPRT1, AKR1B1, RAGE, GFPT2 and PAI-1 gene polymorphisms with chronic renal insufficiency among Asian Indians with type-2 diabetes,” BMC Medical Genetics, vol. 11, no. 1, article 52, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. D. R. Laybutt, A. M. Preston, M. C. Akerfeldt et al., “Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes,” Diabetologia, vol. 50, no. 4, pp. 752–763, 2007. View at Publisher · View at Google Scholar · View at Scopus
  119. P. Marchetti, M. Bugliani, R. Lupi et al., “The endoplasmic reticulum in pancreatic beta cells of type 2 diabetes patients,” Diabetologia, vol. 50, no. 12, pp. 2486–2494, 2007. View at Publisher · View at Google Scholar · View at Scopus
  120. M. Igoillo-Esteve, L. Marselli, D. A. Cunha et al., “Palmitate induces a pro-inflammatory response in human pancreatic islets that mimics CCL2 expression by beta cells in type 2 diabetes,” Diabetologia, vol. 53, no. 7, pp. 1395–1405, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. U. Özcan, E. Yilmaz, L. Özcan et al., “Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes,” Science, vol. 313, no. 5790, pp. 1137–1140, 2006. View at Publisher · View at Google Scholar · View at Scopus
  122. W. J. Welch and C. R. Brown, “Influence of molecular and chemical chaperones on protein folding,” Cell Stress and Chaperones, vol. 1, no. 2, pp. 109–115, 1996. View at Google Scholar · View at Scopus
  123. Q. Xie, V. I. Khaoustov, C. C. Chung et al., “Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation,” Hepatology, vol. 36, no. 3, pp. 592–601, 2002. View at Publisher · View at Google Scholar · View at Scopus
  124. E. Erbay, V. R. Babaev, J. R. Mayers et al., “Reducing endoplasmic reticulum stress through a macrophage lipid chaperone alleviates atherosclerosis,” Nature Medicine, vol. 15, no. 12, pp. 1383–1391, 2009. View at Publisher · View at Google Scholar · View at Scopus
  125. H. Tsukano, T. Gotoh, M. Endo et al., “The endoplasmic reticulum stress-C/EBP homologous protein pathway-mediated apoptosis in macrophages contributes to the instability of atherosclerotic plaques,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 30, no. 10, pp. 1925–1932, 2010. View at Publisher · View at Google Scholar
  126. E. Thorp, G. Li, T. A. Seimon, G. Kuriakose, D. Ron, and I. Tabas, “Reduced apoptosis and plaque necrosis in advanced atherosclerotic lesions of Apoe-/- and Ldlr-/- mice lacking CHOP,” Cell Metabolism, vol. 9, no. 5, pp. 474–481, 2009. View at Publisher · View at Google Scholar · View at Scopus
  127. M. G. Buse, “Hexosamines, insulin resistance, and the complications of diabetes: current status,” American Journal of Physiology, vol. 290, no. 1, pp. E1–E8, 2006. View at Publisher · View at Google Scholar
  128. P. Durand, B. Golinelli-Pimpaneau, S. Mouilleron, B. Badet, and M.-A. Badet-Denisot, “Highlights of glucosamine-6P synthase catalysis,” Archives of Biochemistry and Biophysics, vol. 474, no. 2, pp. 302–317, 2008. View at Publisher · View at Google Scholar
  129. B. W. Doble and J. R. Woodgett, “GSK-3: tricks of the trade for a multi-tasking kinase,” Journal of Cell Science, vol. 116, no. 7, pp. 1175–1186, 2003. View at Publisher · View at Google Scholar · View at Scopus
  130. G. H. Werstuck, A. J. Kim, T. Brenstrum, S. A. Ohnmacht, E. Panna, and A. Capretta, “Examining the correlations between GSK-3 inhibitory properties and anti-convulsant efficacy of valproate and valproate-related compounds,” Bioorganic and Medicinal Chemistry Letters, vol. 14, no. 22, pp. 5465–5467, 2004. View at Publisher · View at Google Scholar · View at Scopus
  131. Y. Shi, D. Gerritsma, A. J. Bowes, A. Capretta, and G. H. Werstuck, “Induction of GRP78 by valproate is dependent upon histone deactylase inhibition,” Bioorganic & Medicinal Chemistry Letters, vol. 17, no. 16, pp. 4491–4494, 2007. View at Google Scholar
  132. I. Partserniak, G. Werstuck, A. Capretta, and J. D. Brennan, “An ESI-MS/MS method for screening of small-molecule mixtures against glycogen synthase kinase-3β (GSK-3β),” ChemBioChem, vol. 9, no. 7, pp. 1065–1073, 2008. View at Publisher · View at Google Scholar · View at Scopus