Oxidative stress biology and cell injury during Type 1 and Type 2 diabetes mellitus

Current Neurovascular Research

Volumn 4, Issue 1, 2007, Pages 63-71

  Maiese, Kenneth ^a   Morhan, Simona Daniela ^a   Zhao, Zhong Chong ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Akt; Apoptosis; Diabetes; Endoplasmic reticulum stress; Erythropoietin; Exercise; Mitochondria; Oxidative stress; Uncoupling proteins

Indexed keywords

INSULIN; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN;

APOPTOSIS; ARTICLE; CELL DAMAGE; CELL STRESS; CYTOLOGY; CYTOPATHOLOGY; DISEASE COURSE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOPLASMIC RETICULUM; GLUCOSE INTOLERANCE; HUMAN; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN TARGETING; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; HUMANS; OXIDATIVE STRESS;

EID: 33847146814     PISSN: 15672026     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720207779940653     Document Type: Article

References (130)

1. Adams, S, Green, P, Claxton, R, Simcox, S, Williams, MV, Walsh, K, Leeuwenburgh, C. (2001) Reactive carbonyl formation by oxidative and non-oxidative pathways. Front Biosci 6: A17-24.
2. Awad, N, Gagnon, M, Messier, C. (2004) The relationship between impaired glucose tolerance, type 2 diabetes, and cognitive function. J Clin Exp Neuropsychol 26: 1044-80.
3. Awata, T, Kurihara, S, Kikuchi, C, Takei, S, Inoue, I, Ishii, C, Takahashi, K, Negishi, K, Yoshida, Y, Hagura, R, Kanazawa, Y, Katayama, S. (1997) Evidence for association between the class I subset of the insulin gene minisatellite (IDDM2 locus) and IDDM in the Japanese population. Diabetes 46: 1637-42.
4. Baisch, JM, Weeks, T, Giles, R, Hoover, M, Stastny, P, Capra, JD. (1990) Analysis of HLA-DQ genotypes and susceptibility in insulin-dependent diabetes mellitus. N Engl J Med 322: 1836-41.
5. Bernal-Mizrachi, C, Weng, S, Li, B, Nolte, LA, Feng, C, Coleman, T, Holloszy, JO, Semenkovich, CF. (2002) Respiratory uncoupling lowers blood pressure through a leptin-dependent mechanism in genetically obese mice. Arterioscler Thromb Vasc Biol 22: 961-8.
6. Bernal-Mizrachi, E, Fatrai, S, Johnson, JD, Ohsugi, M, Otani, K, Han, Z, Polonsky, KS, Permutt, MA. (2004) Defective insulin secretion and increased susceptibility to experimental diabetes are induced by reduced Akt activity in pancreatic islet beta cells. J Clin Invest 114: 928-36.
7. Bonner-Weir, S. (2000) Life and death of the pancreatic beta cells. Trends Endocrinol Metab 11: 375-8.
8. Bottino, R, Trucco, M. (2005) Multifaceted therapeutic approaches for a multigenic disease. Diabetes 54(Suppl 2): S79-86.
9. Brussee, V, Cunningham, FA, Zochodne, DW. (2004) Direct insulin signaling of neurons reverses diabetic neuropathy. Diabetes 53: 1824-30.
10. Cai, Z, Semenza, GL. (2004) Phosphatidylinositol-3-kinase signaling is required for erythropoietin-mediated acute protection against myocardial ischemia/reperfusion injury. Circulation 109: 2050-3.
11. Carvalho, E, Rondinone, C, Smith, U. (2000) Insulin resistance in fat cells from obese Zucker rats - evidence for an impaired activation and translocation of protein kinase B and glucose transporter 4. Mol Cell Biochem 206: 7-16.
12. Ceriello, A, dello Russo, P, Amstad, P, Cerutti, P. (1996) High glucose induces antioxidant enzymes in human endothelial cells in culture. Evidence linking hyperglycemia and oxidative stress. Diabetes 45: 471-7.
13. Chan, CB, De Leo, D, Joseph, JW, McQuaid, TS, Ha, XF, Xu, F, Tsushima, RG, Pennefather, PS, Salapatek, AM, Wheeler, MB. (2001) Increased uncoupling protein-2 levels in beta-cells are associated with impaired glucose-stimulated insulin secretion: mechanism of action. Diabetes 50: 1302-10.
14. Chen, H, Li, X, Epstein, PN. (2005) MnSOD and catalase transgenes demonstrate that protection of islets from oxidative stress does not alter cytokine toxicity. Diabetes 54: 1437-46.
15. Chong, ZZ, Kang, J, Li, F, Maiese, K. (2005a) mGluRI targets microglial activation and selectively prevents neuronal cell engulfment through Akt and caspase dependent pathways. Curr Neurovasc Res 2: 197-211.
16. Chong, ZZ, Kang, JQ, Maiese, K. (2004a) Akt1 drives endothelial cell membrane asymmetry and microglial activation through Bcl-x(L) and caspase 1, 3, and 9. Exp Cell Res 296: 196-207.
17. Chong, ZZ, Kang, JQ, Maiese, K. (2003a) Apaf-1, Bcl-xL, Cytochrome c, and Caspase-9 Form the Critical Elements for Cerebral Vascular Protection by Erythropoietin. J Cereb Blood Flow Metab 23: 320-30.
18. Chong, ZZ, Kang, JQ, Maiese, K. (2003b) Erythropoietin fosters both intrinsic and extrinsic neuronal protection through modulation of microglia, Akt1, Bad, and caspase-mediated pathways. Br J Pharmacol 138: 1107-1118.
19. Chong, ZZ, Kang, JQ, Maiese, K. (2002) Erythropoietin is a novel vascular protectant through activation of Akt1 and mitochondrial modulation of cysteine proteases. Circulation 106: 2973-9.
20. Chong, ZZ, Kang, JQ, Maiese, K. (2004b) Essential cellular regulatory elements of oxidative stress in early and late phases of apoptosis in the central nervous system. Antioxid Redox Signal 6: 277-87.
21. Chong, ZZ, Li, F, Maiese, K. (2005b) Activating Akt and the brain's resources to drive cellular survival and prevent inflammatory injury. Histol Histopathol 20: 299-315.
22. Chong, ZZ, Li, F, Maiese, K. (2006) Group I metabotropic receptor neuroprotection requires Akt and its substrates that govern FOXO3a, Bim, and beta-catenin during oxidative stress. Curr Neurovasc Res 3: 107-17.
23. Chong, ZZ, Li, F, Maiese, K. (2005c) Oxidative stress in the brain: Novel cellular targets that govern survival during neurodegenerative disease. Prog Neurobiol 75: 207-46.
24. Chong, ZZ, Li, F, Maiese, K. (2005d) Stress in the brain: novel cellular mechanisms of injury linked to Alzheimer's disease. Brain Res Brain Res Rev 49: 1-21.
25. Chong, ZZ, Lin, SH, Kang, JQ, Maiese, K. (2003c) Erythropoietin prevents early and late neuronal demise through modulation of Akt1 and induction of caspase 1, 3, and 8. J Neurosci Res 71: 659-69.
26. Chong, ZZ, Lin, SH, Li, F, Maiese, K. (2005e) The sirtuin inhibitor nicotinamide enhances neuronal cell survival during acute anoxic injury through Akt, Bad, PARP, and mitochondrial associated "anti-apoptotic" pathways. Curr Neurovasc Res 2: 271-85.
27. Choo, HJ, Kim, JH, Kwon, OB, Lee, CS, Mun, JY, Han, SS, Yoon, YS, Yoon, G, Choi, KM, Ko, YG. (2006) Mitochondria are impaired in the adipocytes of type 2 diabetic mice. Diabetologia 49: 784-91.
28. Criscuolo, F, Mozo, J, Hurtaud, C, Nubel, T, Bouillaud, F. (2006) UCP2, UCP3, avUCP, what do they do when proton transport is not stimulated? Possible relevance to pyruvate and glutamine metabolism. Biochim Biophys Acta 1757: 1284-91.
29. Daneman, D. (2006) Type 1 diabetes. Lancet 367: 847-58.
30. Datta, SR, Dudek, H, Tao, X, Masters, S, Fu, H, Gotoh, Y, Greenberg, ME. (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-41.
31. Davies, JL, Kawaguchi, Y, Bennett, ST, Copeman, JB, Cordell, HJ, Pritchard, LE, Reed, PW, Gough, SC, Jenkins, SC, Palmer, SM, et al. (1994) A genome-wide search for human type 1 diabetes susceptibility genes. Nature 371: 130-6.
32. Del Prato, S, Marchetti, P. (2004) Beta- and alpha-cell dysfunction in type 2 diabetes. Horm Metab Res 36: 775-81.
33. Deng, Y, Lin, Y, Wu, X. (2002) TRAIL-induced apoptosis requires Bax-dependent mitochondrial release of Smac/DIABLO. Genes Dev 16: 33-45.
34. Di Noia, MA, Van Driesche, S, Palmieri, F, Yang, LM, Quan, S, Goodman, AI, Abraham, NG. (2006) Heme oxygenase-1 enhances renal mitochondrial transport carriers and cytochrome C oxidase activity in experimental diabetes. J Biol Chem 281: 15687-93.
35. Douette, P, Sluse, FE. (2006) Mitochondrial uncoupling proteins: new insights from functional and proteomic studies. Free Radic Biol Med 40: 1097-107.
36. Dzietko, M, Felderhoff-Mueser, U, Sifringer, M, Krutz, B, Bittigau, P, Thor, F, Heumann, R, Buhrer, C, Ikonomidou, C, Hansen, HH. (2004) Erythropoietin protects the developing brain against N-methyl-D-aspartate receptor antagonist neurotoxicity. Neurobiol Dis 15: 177-87.
37. Farese, RV, Sajan, MP, Standaert, ML. (2005) Insulin-sensitive protein kinases (atypical protein kinase C and protein kinase B/Akt): actions and defects in obesity and type II diabetes. Exp Biol Med (Maywood) 230: 593-605.
38. Floyd, RA, Hensley, K. (2002) Oxidative stress in brain aging. Implications for therapeutics of neurodegenerative diseases. Neurobiol Aging 23: 795-807.
39. Fubini, B, Hubbard, A. (2003) Reactive oxygen species (ROS) and reactive nitrogen species (RNS) generation by silica in inflammation and fibrosis. Free Radic Biol Med 34: 1507-16.
40. George, S, Rochford, JJ, Wolfrum, C, Gray, SL, Schinner, S, Wilson, JC, Soos, MA, Murgatroyd, PR, Williams, RM, Acerini, CL, Dunger, DB, Barford, D, Umpleby, AM, Wareham, NJ, Davies, HA, Schafer, AJ, Stoffel, M, O'Rahilly, S, Barroso, I. (2004) A family with severe insulin resistance and diabetes due to a mutation in AKT2. Science 304: 1325-8.
41. Gerozissis, K. (2003) Brain insulin: regulation, mechanisms of action and functions. Cell Mol Neurobiol 23: 1-25.
42. Greco, A, Minghetti, L. (2004) Isoprostanes as biomarkers and mediators of oxidative injury in infant and adult central nervous system diseases. Curr Neurovasc Res 1: 341-354.
43. Grimm, C, Wenzel, A, Groszer, M, Mayser, H, Seeliger, M, Samardzija, M, Bauer, C, Gassmann, M, Reme, CE. (2002) HIF-1-induced erythropoietin in the hypoxic retina protects against light-induced retinal degeneration. Nat Med 8: 718-24.
44. Haber, CA, Lam, TK, Yu, Z, Gupta, N, Goh, T, Bogdanovic, E, Giacca, A, Fantus, IG. (2003) N-acetylcysteine and taurine prevent hyperglycemia-induced insulin resistance in vivo: possible role of oxidative stress. Am J Physiol Endocrinol Metab 285: E744-53.
45. Hampton, RY. (2000) ER stress response: getting the UPR hand on misfolded proteins. Curr Biol 10: R518-21.
46. Han, HS, Suk, K. (2005) The function and integrity of the neurovascular unit rests upon the integration of the vascular and inflammatory cell systems. Curr Neurovasc Res 2: 409-23.
47. Harris, MI, Eastman, RC. (2000) Early detection of undiagnosed diabetes mellitus: a US perspective. Diabetes Metab Res Rev 16: 230-6.
48. Henry, DH, Bowers, P, Romano, MT, Provenzano, R. (2004) Epoetin alfa. Clinical evolution of a pleiotropic cytokine. Arch Intern Med 164: 262-76.
49. Henry, MK, Lynch, JT, Eapen, AK, Quelle, FW. (2001) DNA damage-induced cell-cycle arrest of hematopoietic cells is overridden by activation of the PI-3 kinase/Akt signaling pathway. Blood 98: 834-41.
50. Howlett, KF, Sakamoto, K, Yu, H, Goodyear, LJ, Hargreaves, M. (2006) Insulin-stimulated insulin receptor substrate-2-associated phosphatidylinositol 3-kinase activity is enhanced in human skeletal muscle after exercise. Metabolism 55: 1046-52.
51. Huang, TJ, Verkhratsky, A, Fernyhough, P. (2005) Insulin enhances mitochondrial inner membrane potential and increases ATP levels through phosphoinositide 3-kinase in adult sensory neurons. Mol Cell Neurosci 28: 42-54.
52. Hyoda, K, Hosoi, T, Horie, N, Okuma, Y, Ozawa, K, Nomura, Y. (2006) PI3K-Akt inactivation induced CHOP expression in endoplasmic reticulum-stressed cells. Biochem Biophys Res Commun 340: 286-90.
53. Ieraci, A, Herrera, DG. (2006) Nicotinamide Protects against Ethanol-Induced Apoptotic Neurodegeneration in the Developing Mouse Brain. PLoS Med 3: e101.
54. Ihara, Y, Toyokuni, S, Uchida, K, Odaka, H, Tanaka, T, Ikeda, H, Hiai, H, Seino, Y, Yamada, Y. (1999) Hyperglycemia causes oxidative stress in pancreatic beta-cells of GK rats, a model of type 2 diabetes. Diabetes 48: 927-32.
55. Kang, JQ, Chong, ZZ, Maiese, K. (2003a) Akt1 protects against inflammatory microglial activation through maintenance of membrane asymmetry and modulation of cysteine protease activity. J Neurosci Res 74: 37-51.
56. Kang, JQ, Chong, ZZ, Maiese, K. (2003b) Critical role for Akt1 in the modulation of apoptotic phosphatidylserine exposure and microglial activation. Mol Pharmacol 64: 557-69.
57. Kelley, DE, He, J, Menshikova, EV, Ritov, VB. (2002) Dysfunction of mitochondria in human skeletal muscle in type 2 diabetes. Diabetes 51: 2944-50.
58. Kernan, WN, Inzucchi, SE, Viscoli, CM, Brass, LM, Bravata, DM, Horwitz, RI. (2002) Insulin resistance and risk for stroke. Neurology 59: 809-15.
59. Kohn, AD, Summers, SA, Birnbaum, MJ, Roth, RA. (1996) Expression of a constitutively active Akt Ser/Thr kinase in 3T3-L1 adipocytes stimulates glucose uptake and glucose transporter 4 translocation. J Biol Chem 271: 31372-8.
60. Kopecky, J, Clarke, G, Enerback, S, Spiegelman, B, Kozak, LP. (1995) Expression of the mitochondrial uncoupling protein gene from the aP2 gene promoter prevents genetic obesity. J Clin Invest 96: 2914-23.
61. Krook, A, Roth, RA, Jiang, XJ, Zierath, JR, Wallberg-Henriksson, H. (1998) Insulin-stimulated Akt kinase activity is reduced in skeletal muscle from NIDDM subjects. Diabetes 47: 1281-6.
62. Kyvik, KO, Green, A, Beck-Nielsen, H. (1995) Concordance rates of insulin dependent diabetes mellitus: a population based study of young Danish twins. BMJ 311: 913-7.
63. Laakso, M. (2001) Cardiovascular disease in type 2 diabetes: challenge for treatment and prevention. J Intern Med 249: 225-35.
64. Lee, DH, O'Connor, TR, Pfeifer, GP. (2002) Oxidative DNA damage induced by copper and hydrogen peroxide promotes CG - >TT tandem mutations at methylated CpG dinucleotides in nucleotide excision repair-deficient cells. Nucleic Acids Res 30: 3566-73.
65. Lepore, DA, Shinkel, TA, Fisicaro, N, Mysore, TB, Johnson, LE, d'Apice, AJ, Cowan, PJ. (2004) Enhanced expression of glutathione peroxidase protects islet beta cells from hypoxia-reoxygenation. Xenotransplantation 11: 53-9.
66. Li, B, Nolte, LA, Ju, JS, Han, DH, Coleman, T, Holloszy, JO, Semenkovich, CF. (2000) Skeletal muscle respiratory uncoupling prevents diet-induced obesity and insulin resistance in mice. Nat Med 6: 1115-20.
67. Li, F, Chong, ZZ, Maiese, K. (2006a) Cell life versus cell longevity: the mysteries surrounding the NAD(+) precursor nicotinamide. Curr Med Chem 13: 883-95.
68. Li, F, Chong, ZZ, Maiese, K. (2004) Erythropoietin on a tightrope: balancing neuronal and vascular protection between intrinsic and extrinsic pathways. Neurosignals 13: 265-89.
69. Li, F, Chong, ZZ, Maiese, K. (2006b) Microglial integrity is maintained by erythropoietin through integration of Akt and its substrates of glycogen synthase kinase-3beta, beta-catenin, and nuclear factor-kappaB. Curr Neurovasc Res 3: 187-201.
70. Li, LX, Skorpen, F, Egeberg, K, Jorgensen, IH, Grill, V. (2001) Uncoupling protein-2 participates in cellular defense against oxidative stress in clonal beta-cells. Biochem Biophys Res Commun 282: 273-7.
71. Lin, SH, Vincent, A, Shaw, T, Maynard, KI, Maiese, K. (2000) Prevention of nitric oxide-induced neuronal injury through the modulation of independent pathways of programmed cell death. J Cereb Blood Flow Metab 20: 1380-91.
72. Ling, PR, Mueller, C, Smith, RJ, Bistrian, BR. (2003) Hyperglycemia induced by glucose infusion causes hepatic oxidative stress and systemic inflammation, but not STAT3 or MAP kinase activation in liver in rats. Metabolism 52: 868-74.
73. Lund, T, O'Reilly, L, Hutchings, P, Kanagawa, O, Simpson, E, Gravely, R, Chandler, P, Dyson, J, Picard, JK, Edwards, A, et al. (1990) Prevention of insulin-dependent diabetes mellitus in non-obese diabetic mice by transgenes encoding modified I-A beta-chain or normal I-E alpha-chain. Nature 345: 727-9.
74. Luppi, P, Rossiello, MR, Faas, S, Trucco, M. (1995) Genetic background and environment contribute synergistically to the onset of autoimmune diseases. J Mol Med 73: 381-93.
75. Maciejewski, ML, Maynard, C. (2004) Diabetes-related utilization and costs for inpatient and outpatient services in the Veterans Administration. Diabetes Care 27 Suppl 2: B69-73.
76. MacLellan, JD, Gerrits, MF, Gowing, A, Smith, PJ, Wheeler, MB, Harper, ME. (2005) Physiological increases in uncoupling protein 3 augment fatty acid oxidation and decrease reactive oxygen species production without uncoupling respiration in muscle cells. Diabetes 54: 2343-50.
77. Maiese, K, Chong, ZZ. (2004) Insights into oxidative stress and potential novel therapeutic targets for Alzheimer disease. Restor Neurol Neurosci 22: 87-104.
78. Maiese, K, Chong, ZZ. (2003) Nicotinamide: necessary nutrient emerges as a novel cytoprotectant for the brain. Trends Pharmacol Sci 24: 228-32.
79. Maiese, K, Chong, ZZ, Li, F. (2005a) Driving cellular plasticity and survival through the signal transduction pathways of metabotropic glutamate receptors. Curr Neurovasc Res 2: 425-46.
80. Maiese, K, Li, F, Chong, ZZ. (2005b) Erythropoietin and cancer. JAMA 293: 1858-1859.
81. Maiese, K, Li, F, Chong, ZZ. (2004) Erythropoietin in the brain: can the promise to protect be fulfilled? Trends Pharmacol Sci 25: 577-583.
82. Maiese, K, Li, F, Chong, ZZ. (2005c) New avenues of exploration for erythropoietin. JAMA 293: 90-5.
83. Maiorana, A, O'Driscoll, G, Goodman, C, Taylor, R, Green, D. (2002) Combined aerobic and resistance exercise improves glycemic control and fitness in type 2 diabetes. Diabetes Res Clin Pract 56: 115-23.
84. Martin, D, Salinas, M, Lopez-Valdaliso, R, Serrano, E, Recuero, M, Cuadrado, A. (2001) Effect of the Alzheimer amyloid fragment Abeta(25-35) on Akt/PKB kinase and survival of PC12 cells. J Neurochem 78: 1000-8.
85. Matsuzaki, H, Tamatani, M, Mitsuda, N, Namikawa, K, Kiyama, H, Miyake, S, Tohyama, M. (1999) Activation of Akt kinase inhibits apoptosis and changes in Bcl-2 and Bax expression induced by nitric oxide in primary hippocampal neurons. J Neurochem 73: 2037-46.
86. McCormick, WC, Hardy, J, Kukull, WA, Bowen, JD, Teri, L, Zitzer, S, Larson, EB. (2001) Healthcare utilization and costs in managed care patients with Alzheimer's disease during the last few years of life. J Am Geriatr Soc 49: 1156-60.
87. Melanitou, E. (2005) The autoimmune contrivance: genetics in the mouse model. Clin Immunol 117: 195-206.
88. Mendiondo, MS, Kryscio, RJ, Schmitt, FA. (2001) Models of progression in AD: predicting disability and costs. Neurology 57: 943-4.
89. Mojiminiyi, OA, Abdella, NA, Zaki, MY, El Gebely, SA, Mohamedi, HM, Aldhahi, WA. (2006) Prevalence and associations of low plasma erythropoietin in patients with Type 2 diabetes mellitus. Diabet Med 23: 839-44.
90. Monnier, L, Mas, E, Ginet, C, Michel, F, Villon, L, Cristol, JP, Colette, C. (2006) Activation of oxidative stress by acute glucose fluctuations compared with sustained chronic hyperglycemia in patients with type 2 diabetes. JAMA 295: 1681-7.
91. Nakatani, Y, Kaneto, H, Kawamori, D, Yoshiuchi, K, Hatazaki, M, Matsuoka, TA, Ozawa, K, Ogawa, S, Hori, M, Yamasaki, Y, Matsuhisa, M. (2005) Involvement of endoplasmic reticulum stress in insulin resistance and diabetes. J Biol Chem 280: 847-51.
92. Namikawa, K, Honma, M, Abe, K, Takeda, M, Mansur, K, Obata, T, Miwa, A, Okado, H, Kiyama, H. (2000) Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration. J Neurosci 20: 2875-86.
93. Okouchi, M, Okayama, N, Alexander, JS, Aw, TY. (2006) NRF2-dependent glutamate-L-cysteine ligase catalytic subunit expression mediates insulin protection against hyperglycemia- induced brain endothelial cell apoptosis. Curr Neurovasc Res 3: 249-61.
94. Orchard, TJ, Olson, JC, Erbey, JR, Williams, K, Forrest, KY, Smithline Kinder, L, Ellis, D, Becker, DJ. (2003) Insulin resistance-related factors, but not glycemia, predict coronary artery disease in type 1 diabetes: 10-year follow-up data from the Pittsburgh Epidemiology of Diabetes Complications Study. Diabetes Care 26: 1374-9.
95. Ozcan, U, Cao, Q, Yilmaz, E, Lee, AH, Iwakoshi, NN, Ozdelen, E, Tuncman, G, Gorgun, C, Glimcher, LH, Hotamisligil, GS. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-61.
96. Parsa, CJ, Matsumoto, A, Kim, J, Riel, RU, Pascal, LS, Walton, GB, Thompson, RB, Petrofski, JA, Annex, BH, Stamler, JS, Koch, WJ. (2003) A novel protective effect of erythropoietin in the infarcted heart. J Clin Invest 112: 999-1007.
97. Perkins, BA, Bril, V. (2002) Diagnosis and management of diabetic neuropathy. Curr Diab Rep 2: 495-500.
98. Permutt, MA, Wasson, J, Cox, N. (2005) Genetic epidemiology of diabetes. J Clin Invest 115: 1431-9.
99. Petersen, KF, Befroy, D, Dufour, S, Dziura, J, Ariyan, C, Rothman, DL, DiPietro, L, Cline, GW, Shulman, GI. (2003) Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 300: 1140-2.
100. Petersen, KF, Dufour, S, Befroy, D, Garcia, R, Shulman, GI. (2004) Impaired mitochondrial activity in the insulin-resistant offspring of patients with type 2 diabetes. N Engl J Med 350: 664-71.
101. Pfeiffer, S, Lass, A, Schmidt, K, Mayer, B. (2001) Protein tyrosine nitration in mouse peritoneal macrophages activated in vitro and in vivo: evidence against an essential role of peroxynitrite. FASEB J 15: 2355-64.
102. Pietropaolo, M, Barinas-Mitchell, E, Pietropaolo, SL, Kuller, LH, Trucco, M. (2000) Evidence of islet cell autoimmunity in elderly patients with type 2 diabetes. Diabetes 49: 32-8.
103. Quinn, L. (2001) Type 2 diabetes: epidemiology, pathophysiology, and diagnosis. Nurs Clin North Am 36: 175-92, v.
104. Rachek, LI, Thornley, NP, Grishko, VI, LeDoux, SP, Wilson, GL. (2006) Protection of INS-1 cells from free fatty acid-induced apoptosis by targeting hOGG1 to mitochondria. Diabetes 55: 1022-8.
105. Redondo, MJ, Yu, L, Hawa, M, Mackenzie, T, Pyke, DA, Eisenbarth, GS, Leslie, RD. (2001) Heterogeneity of type I diabetes: analysis of monozygotic twins in Great Britain and the United States. Diabetologia 44: 354-62.
106. Robertson, LA, Kim, AJ, Werstuck, GH. (2006) Mechanisms linking diabetes mellitus to the development of atherosclerosis: a role for endoplasmic reticulum stress and glycogen synthase kinase-3. Can J Physiol Pharmacol 84: 39-48.
107. Ropelle, ER, Pauli, JR, Prada, PO, de Souza, CT, Picardi, PK, Faria, MC, Cintra, DE, Fernandes, MF, Flores, MB, Velloso, LA, Saad, MJ, Carvalheira, J. (2006) Reversal of diet-induced insulin resistance with a single bout of exercise: The role of PTP1B and IRS-1 serine phosphorylation. J Physiol 577: 997-1007.
108. Rytomaa, M, Lehmann, K, Downward, J. (2000) Matrix detachment induces caspase-dependent cytochrome c release from mitochondria: inhibition by PKB/Akt but not Raf signalling. Oncogene 19: 4461-8.
109. Schrauwen, P, Hesselink, MK, Blaak, EE, Borghouts, LB, Schaart, G, Saris, WH, Keizer, HA. (2001) Uncoupling protein 3 content is decreased in skeletal muscle of patients with type 2 diabetes. Diabetes 50: 2870-3.
110. Shah, DI, Singh, M. (2006) Possible role of Akt to improve vascular endothelial dysfunction in diabetic and hyperhomocysteinemic rats. Mol Cell Biochem Jul 14; [Epub ahead of print].
111. Silverberg, DS, Wexler, D, Blum, M, Tchebiner, JZ, Sheps, D, Keren, G, Schwartz, D, Baruch, R, Yachnin, T, Shaked, M, Schwartz, I, Steinbruch, S, Iaina, A. (2003) The effect of correction of anaemia in diabetics and non-diabetics with severe resistant congestive heart failure and chronic renal failure by subcutaneous erythropoietin and intravenous iron. Nephrol Dial Transplant 18: 141-6.
112. Siu, AW, To, CH. (2002) Nitric oxide and hydroxyl radical-induced retinal lipid peroxidation in vitro. Clin Exp Optom 85: 378-82.
113. Smeitink, JAM, van den Heuvel, L, Koopman, WJH, Nijtmans, LGJ, Ugalde, C, Willems, P. (2004) Cell biological consequences of mitochondrial NADH: Ubiquinone oxidoreductase deficiency. Curr Neurovasc Res 1: 29-40.
114. Staal, SP. (1987) Molecular cloning of the akt oncogene and its human homologues AKT1 and AKT2: amplification of AKT1 in a primary human gastric adenocarcinoma. Proc Natl Acad Sci USA 84: 5034-7.
115. Staal, SP, Huebner, K, Croce, CM, Parsa, NZ, Testa, JR. (1988) The AKT1 proto-oncogene maps to human chromosome 14, band q32. Genomics 2: 96-8.
116. Suhara, T, Mano, T, Oliveira, BE, Walsh, K. (2001) Phosphatidylinositol 3-kinase/Akt signaling controls endothelial cell sensitivity to Fas-mediated apoptosis via regulation of FLICE- inhibitory protein (FLIP). Circ Res 89: 13-9.
117. Symeonidis, A, Kouraklis-Symeonidis, A, Psiroyiannis, A, Leotsinidis, M, Kyriazopoulou, V, Vassilakos, P, Vagenakis, A, Zoumbos, N. (2006) Inappropriately low erythropoietin response for the degree of anemia in patients with noninsulin-dependent diabetes mellitus. Ann Hematol 85: 79-85.
118. Thomas, MC, Cooper, ME, Tsalamandris, C, MacIsaac, R, Jerums, G. (2005) Anemia with impaired erythropoietin response in diabetic patients. Arch Intern Med 165: 466-9.
119. Todd, JA, Bell, JI, McDevitt, HO. (1987) HLA-DQ beta gene contributes to susceptibility and resistance to insulin-dependent diabetes mellitus. Nature 329: 599-604.
120. van der Meer, P, Voors, AA, Lipsic, E, Smilde, TD, van Gilst, WH, van Veldhuisen, DJ. (2004) Prognostic value of plasma erythropoietin on mortality in patients with chronic heart failure. J Am Coll Cardiol 44: 63-7.
121. Varma, S, Lal, BK, Zheng, R, Breslin, JW, Saito, S, Pappas, PJ, Hobson, RW, 2nd, Duran, WN. (2005) Hyperglycemia alters PI3k and Akt signaling and leads to endothelial cell proliferative dysfunction. Am J Physiol Heart Circ Physiol 289: H1744-51.
122. Vincent, AM, Maiese, K. (1999) Nitric oxide induction of neuronal endonuclease activity in programmed cell death. Exp Cell Res 246: 290-300.
123. 2 and NO on apoptosis involving activation of p38 mitogen-activated protein kinase and caspase-3. J Neurosci Res 72: 508-19.
124. Wick, A, Wick, W, Waltenberger, J, Weller, M, Dichgans, J, Schulz, JB. (2002) Neuroprotection by hypoxic preconditioning requires sequential activation of vascular endothelial growth factor receptor and Akt. J Neurosci 22: 6401-7.
125. Wild, S, Roglic, G, Green, A, Sicree, R, King, H. (2004) Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care 27: 1047-53.
126. Wilson, FH, Hariri, A, Farhi, A, Zhao, H, Petersen, KF, Toka, HR, Nelson-Williams, C, Raja, KM, Kashgarian, M, Shulman, GI, Scheinman, SJ, Lifton, RP. (2004) A cluster of metabolic defects caused by mutation in a mitochondrial tRNA. Science 306: 1190-4.
127. Yamaguchi, H, Wang, HG. (2001) The protein kinase PKB/Akt regulates cell survival and apoptosis by inhibiting Bax conformational change. Oncogene 20: 7779-86.
128. Yamamoto, T, Maruyama, W, Kato, Y, Yi, H, Shamoto-Nagai, M, Tanaka, M, Sato, Y, Naoi, M. (2002) Selective nitration of mitochondrial complex I by peroxynitrite: involvement in mitochondria dysfunction and cell death of dopaminergic SH-SY5Y cells. J Neural Transm 109: 1-13.
129. Yano, M, Hasegawa, G, Ishii, M, Yamasaki, M, Fukui, M, Nakamura, N, Yoshikawa, T. (2004) Short-term exposure of high glucose concentration induces generation of reactive oxygen species in endothelial cells: implication for the oxidative stress associated with postprandial hyperglycemia. Redox Rep 9: 111-6.
130. Zhang, CY, Baffy, G, Perret, P, Krauss, S, Peroni, O, Grujic, D, Hagen, T, Vidal-Puig, AJ, Boss, O, Kim, YB, Zheng, XX, Wheeler, MB, Shulman, GI, Chan, CB, Lowell, BB. (2001) Uncoupling protein-2 negatively regulates insulin secretion and is a major link between obesity, beta cell dysfunction, and type 2 diabetes. Cell 105: 745-55.