Diabetes-induced central neuritic dystrophy and cognitive deficits are associated with the formation of oligomeric reticulon-3 via oxidative stress

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15590-15599

  Zhao, Bei ^a,d   Pan, Bai Shen ^b   Shen, Su Wen ^a,d   Sun, Xiao ^a,d   Hou, Zheng Zhou ^a,d   Yan, Riqiang ^c   Sun, Feng Yan ^a,d  

^a Institute of Pathogenic Biology   (China)

^b FUDAN UNIVERSITY   (China)

^c LERNER RESEARCH INSTITUTE   (United States)

^d FUDAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

COGNITIVE DEFICITS; COGNITIVE FUNCTIONS; HIGH MOLECULAR WEIGHT; IMMUNOPRECIPITATIONS; MOLECULAR MECHANISM; NEURAL MORPHOLOGY; PROTEIN CARBONYLS; THERAPEUTIC STRATEGY;

AGGREGATES; DAMAGE DETECTION; NEURODEGENERATIVE DISEASES; OLIGOMERS; OXIDATIVE STRESS; RATS; TISSUE;

PROTEINS;

BETA SECRETASE 1; HYDROGEN PEROXIDE; MEMBRANE PROTEIN; RETICULON 3; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DISEASE; CELL STRUCTURE; CENTRAL NEURITIC DYSTROPHY; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CORRELATION ANALYSIS; DEMENTIA; DIABETES MELLITUS; DISEASE ASSOCIATION; DYSTROPHY; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MALE; NERVE CELL; NEURITE; NEUROBLASTOMA; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; RNA SEQUENCE; SPATIAL LEARNING; SPATIAL MEMORY;

AGGREGATION; ALZHEIMER DISEASE; AXON; CENTRAL DYSTROPHIC NEURITE; DEMENTIA; DIABETES; DYSTROPHIN; OXIDATIVE STRESS; RETICULON;

AMYLOID BETA-PEPTIDES; ANIMALS; CARRIER PROTEINS; CELL LINE, TUMOR; CEREBRAL CORTEX; COGNITION DISORDERS; DEMENTIA; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC NEUROPATHIES; HYDROGEN PEROXIDE; MALE; NEURITES; OXIDANTS; OXIDATIVE STRESS; PROTEIN CARBONYLATION; PROTEIN MULTIMERIZATION; RATS; RATS, SPRAGUE-DAWLEY;

RATTUS;

EID: 84878388997     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.440784     Document Type: Article

References (54)

1. Barnes, D. E., and Yaffe, K. (2011) The projected effect of risk factor reduction on Alzheimer's disease prevalence. Lancet Neurol 10, 819-828
2. Grundke-Iqbal, I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M., and Binder, L. I. (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. U.S.A. 83, 4913-4917
3. Murrell, J., Farlow, M., Ghetti, B., and Benson, M. D. (1991) A mutation in the amyloid precursor protein associated with hereditary Alzheimer's disease. Science 254, 97-99 (Pubitemid 21917324)
4. Selkoe, D. J. (1986) Altered structural proteins in plaques and tangles. What do they tell us about the biology of Alzheimer's disease? Neurobiol. Aging 7, 425-432
5. Spillantini, M. G., Goedert, M., Jakes, R., and Klug, A. (1990) Topographical relationship between β-amyloid and tau protein epitopes in tangle-bearing cells in Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 87, 3952-3956
6. Yankner, B. A. (1996) New clues to Alzheimer's disease. Unraveling the roles of amyloid and tau. Nat. Med. 2, 850-852
7. O'Brien, J. T., and Burns, A. (2011) Clinical practice with anti-dementia drugs. A revised (second) consensus statement from the British Association for Psychopharmacology. J. Psychopharmacol. 25, 997-1019
8. Daviglus, M. L., Bell, C. C., Berrettini, W., Bowen, P. E., Connolly, E. S., Jr., Cox, N. J., Dunbar-Jacob, J. M., Granieri, E. C., Hunt, G., McGarry, K., Patel, D., Potosky, A. L., Sanders-Bush, E., Silberberg, D., and Trevisan, M. (2010) National Institutes of Health State-of-the-Science Conference statement. Preventing alzheimer disease and cognitive decline. Ann. Intern. Med. 153, 176-181
9. Shaw, J. E., Sicree, R. A., and Zimmet, P. Z. (2010) Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res. Clin. Pract. 87, 4-14
10. Xu, W. L., von Strauss, E., Qiu, C. X., Winblad, B., and Fratiglioni, L. (2009) Uncontrolled diabetes increases the risk of Alzheimer's disease. A population-based cohort study. Diabetologia 52, 1031-1039
11. Schrijvers, E. M., Witteman, J. C., Sijbrands, E. J., Hofman, A., Koudstaal, P. J., and Breteler, M. M. (2010) Insulin metabolism and the risk of Alzheimer disease. The Rotterdam Study. Neurology 75, 1982-1987
12. Janson, J., Laedtke, T., Parisi, J. E., O'Brien, P., Petersen, R. C., and Butler, P. C. (2004) Increased risk of type 2 diabetes in Alzheimer disease. Diabetes 53, 474-481 (Pubitemid 38174565)
13. Murray, I. V., Proza, J. F., Sohrabji, F., and Lawler, J. M. (2011) Vascular and metabolic dysfunction in Alzheimer's disease. A review. Exp. Biol. Med. (Maywood) 236, 772-782
14. Li, Z. G., Zhang, W., and Sima, A. A. (2007) Alzheimer-like changes in rat models of spontaneous diabetes. Diabetes 56, 1817-1824 (Pubitemid 47025451)
15. Zhang, T., Pan, B. S., Zhao, B., Zhang, L. M., Huang, Y. L., and Sun, F. Y. (2009) Exacerbation of poststroke dementia by type 2 diabetes is associated with synergistic increases of β-secretase activation and β-amyloid generation in rat brains. Neuroscience 161, 1045-1056
16. Zhang, T., Pan, B. S., Sun, G. C., Sun, X., and Sun, F. Y. (2010) Diabetes synergistically exacerbates poststroke dementia and tau abnormality in brain. Neurochem. Int. 56, 955-961
17. Xiong, M., Zhang, T., Zhang, L. M., Lu, S. D., Huang, Y. L., and Sun, F. Y. (2008) Caspase inhibition attenuates accumulation of β-amyloid by reducing β-secretase production and activity in rat brains after stroke. Neurobiol. Dis. 32, 433-441
18. Tesco, G., Koh, Y. H., Kang, E. L., Cameron, A. N., Das, S., Sena-Esteves, M., Hiltunen, M., Yang, S. H., Zhong, Z., Shen, Y., Simpkins, J. W., and Tanzi, R. E. (2007) Depletion of GGA3 stabilizes BACE and enhances β-secretase activity. Neuron 54, 721-737 (Pubitemid 46843521)
19. Zhang, Y., Xiong, M., Yan, R. Q., and Sun, F. Y. (2010) Mutant ubiquitin-mediated β-secretase stability via activation of caspase-3 is related to β-amyloid accumulation in ischemic striatum in rats. J. Cereb. Blood Flow Metab. 30, 566-575
20. Oertle, T., and Schwab, M. E. (2003) Nogo and its paRTNers. Trends Cell Biol. 13, 187-194 (Pubitemid 36351534)
21. Iwahashi, J., Kawasaki, I., Kohara, Y., Gengyo-Ando, K., Mitani, S., Ohshima, Y., Hamada, N., Hara, K., Kashiwagi, T., and Toyoda, T. (2002) Caenorhabditis elegans reticulon interacts with RME-1 during embryogenesis. Biochem. Biophys. Res. Commun. 293, 698-704 (Pubitemid 34687243)
22. Steiner, P., Kulangara, K., Sarria, J. C., Glauser, L., Regazzi, R., and Hirling, H. (2004) Reticulon 1-C/neuroendocrine-specific protein-C interacts with SNARE proteins. J. Neurochem. 89, 569-580 (Pubitemid 38534143)
23. Karnezis, T., Mandemakers, W., McQualter, J. L., Zheng, B., Ho, P. P., Jordan, K. A., Murray, B. M., Barres, B., Tessier-Lavigne, M., and Bernard, C. C. (2004) The neurite outgrowth inhibitor Nogo A is involved in autoimmune-mediated demyelination. Nat. Neurosci. 7, 736-744 (Pubitemid 38859058)
24. Yang, Y. S., and Strittmatter, S. M. (2007) The reticulons. A family of proteins with diverse functions. Genome Biol. 8, 234
25. Parodi, J., Sepúlveda, F. J., Roa, J., Opazo, C., Inestrosa, N. C., and Aguayo, L. G. (2010) β-Amyloid causes depletion of synaptic vesicles leading to neurotransmission failure. J. Biol. Chem. 285, 2506-2514
26. Yan, R., Shi, Q., Hu, X., and Zhou, X. (2006) Reticulon proteins. Emerging players in neurodegenerative diseases. Cell. Mol. Life Sci. 63, 877-889 (Pubitemid 43724076)
27. Tang, B. L., and Liou, Y. C. (2007) Novel modulators of amyloid-β precursor protein processing. J. Neurochem. 100, 314-323 (Pubitemid 46010993)
28. Murayama, K. S., Kametani, F., Saito, S., Kume, H., Akiyama, H., and Araki, W. (2006) Reticulons RTN3 and RTN4-B/C interact with BACE1 and inhibit its ability to produce amyloid β-protein. Eur. J. Neurosci. 24, 1237-1244 (Pubitemid 44401647)
29. Hu, X., Shi, Q., Zhou, X., He, W., Yi, H., Yin, X., Gearing, M., Levey, A., and Yan, R. (2007) Transgenic mice overexpressing reticulon 3 develop neuritic abnormalities. EMBO J. 26, 2755-2767 (Pubitemid 46884276)
30. Shi, Q., Prior, M., He, W., Tang, X., Hu, X., and Yan, R. (2009) Reduced amyloid deposition in mice overexpressing RTN3 is adversely affected by preformed dystrophic neurites. J. Neurosci. 29, 9163-9173
31. Nelson, P. T., Smith, C. D., Abner, E. A., Schmitt, F. A., Scheff, S. W., Davis, G. J., Keller, J. N., Jicha, G. A., Davis, D., Wang-Xia, W., Hartman, A., Katz, D. G., and Markesbery, W. R. (2009) Human cerebral neuropathology of type 2 diabetes mellitus. Biochim. Biophys. Acta 1792, 454-469
32. Zhang, F., Ye, C., Li, G., Ding, W., Zhou, W., Zhu, H., Chen, G., Luo, T., Guang, M., Liu, Y., Zhang, D., Zheng, S., Yang, J., Gu, Y., Xie, X., and Luo, M. (2003) The rat model of type 2 diabetic mellitus and its glycometabolism characters. Exp. Anim. 52, 401-407 (Pubitemid 41349948)
33. Morris, R. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60
34. Liu, H. M., Yang, S. Z., and Sun, F. Y. (2010) 1-Methyl-4-phenyl- pyridinium time-dependently alters expressions of oxoguanine glycosylase 1 and xeroderma pigmentosum group F protein in PC12 cells. Neurosci. Bull. 26, 1-7
35. Lortz, S., Tiedge, M., Nachtwey, T., Karlsen, A. E., Nerup, J., and Lenzen, S. (2000) Protection of insulin-producing RINm5F cells against cytokine-mediated toxicity through overexpression of antioxidant enzymes. Diabetes 49, 1123-1130 (Pubitemid 30439085)
36. He, W., Lu, Y., Qahwash, I., Hu, X. Y., Chang, A., and Yan, R. (2004) Reticulon family members modulate BACE1 activity and amyloid-β peptide generation. Nat. Med. 10, 959-965 (Pubitemid 39273737)
37. Prior, M., Shi, Q., Hu, X., He, W., Levey, A., and Yan, R. (2010) RTN/Nogo in forming Alzheimer's neuritic plaques. Neurosci. Biobehav. Rev. 34, 1201-1206
38. Squier, T. C. (2001) Oxidative stress and protein aggregation during biological aging. Exp. Gerontol. 36, 1539-1550
39. Hashimoto, M., Rockenstein, E., Crews, L., and Masliah, E. (2003) Role of protein aggregation in mitochondrial dysfunction and neurodegeneration in Alzheimer's and Parkinson's diseases. Neuromolecular Med. 4, 21-36
40. Powell, S. R., Wang, P., Divald, A., Teichberg, S., Haridas, V., McCloskey, T. W., Davies, K. J., and Katzeff, H. (2005) Aggregates of oxidized proteins (lipofuscin) induce apoptosis through proteasome inhibition and dysregulation of proapoptotic proteins. Free Radic. Biol. Med. 38, 1093-1101 (Pubitemid 40386555)
41. Lee, M. H., Hyun, D. H., Jenner, P., and Halliwell, B. (2001) Effect of proteasome inhibition on cellular oxidative damage, antioxidant defenses, and nitric oxide production. J. Neurochem. 78, 32-41 (Pubitemid 32622586)
42. Dalle-Donne, I., Aldini, G., Carini, M., Colombo, R., Rossi, R., and Milzani, A. (2006) Protein carbonylation, cellular dysfunction, and disease progression. J. Cell. Mol. Med. 10, 389-406 (Pubitemid 44870187)
43. Cheng, K. C., Cahill, D. S., Kasai, H., Nishimura, S., and Loeb, L. A. (1992) 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G-T and A-C substitutions. J. Biol. Chem. 267, 166-172
44. Dalle-Donne, I., Rossi, R., Colombo, R., Giustarini, D., and Milzani, A. (2006) Biomarkers of oxidative damage in human disease. Clin. Chem. 52, 601-623
45. Dalle-Donne, I., Giustarini, D., Colombo, R., Rossi, R., and Milzani, A. (2003) Protein carbonylation in human diseases. Trends Mol. Med. 9, 169-176 (Pubitemid 36626706)
46. Wang, W., Sun, F., An, Y., Ai, H., Zhang, L., Huang, W., and Li, L. (2009) Morroniside protects human neuroblastoma SH-SY5Y cells against hydrogen peroxide-induced cytotoxicity. Eur. J. Pharmacol. 613, 19-23
47. Vincent, A. M., Brownlee, M., and Russell, J. W. (2002) Oxidative stress and programmed cell death in diabetic neuropathy. Ann. N.Y. Acad. Sci. 959, 368-383 (Pubitemid 34457577)
48. Greene, D. A., Stevens, M. J., Obrosova, I., and Feldman, E. L. (1999) Glucose-induced oxidative stress and programmed cell death in diabetic neuropathy. Eur. J. Pharmacol. 375, 217-223 (Pubitemid 29317606)
49. Selkoe, D. J. (2002) Alzheimer's disease is a synaptic failure. Science 298, 789-791
50. Glabe, C. G., and Kayed, R. (2006) Common structure and toxic function of amyloid oligomers implies a common mechanism of pathogenesis. Neurology 66, S74-S78 (Pubitemid 43739989)
51. Sponne, I., Fifre, A., Drouet, B., Klein, C., Koziel, V., Pinçon-Raymond, M., Olivier, J. L., Chambaz, J., and Pillot, T. (2003) Apoptotic neuronal cell death induced by the non-fibrillar amyloid-β peptide proceeds through an early reactive oxygen species-dependent cytoskeleton perturbation. J. Biol. Chem. 278, 3437-3445 (Pubitemid 36801260)
52. De Felice, F. G., Velasco, P. T., Lambert, M. P., Viola, K., Fernandez, S. J., Ferreira, S. T., and Klein, W. L. (2007) Aβ oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J. Biol. Chem. 282, 11590-11601 (Pubitemid 47100810)
53. Ewers, M., Sperling, R. A., Klunk, W. E., Weiner, M. W., and Hampel, H. (2011) Neuroimaging markers for the prediction and early diagnosis of Alzheimer's disease dementia. Trends Neurosci. 34, 430-442
54. Threlkeld, Z. D., Jicha, G. A., Smith, C. D., and Gold, B. T. (2011) Task deactivation reductions and atrophy within parietal default mode regions are overlapping but only weakly correlated in mild cognitive impairment. J. Alzheimers Dis. 27, 415-427