The involvement of autophagy pathway in exaggerated ischemic brain damage in diabetic mice

CNS Neuroscience and Therapeutics

Volumn 19, Issue 10, 2013, Pages 753-763

  Wei, Ning ^a,b   Yu, Shan Ping ^b   Gu, Xiao Huan ^b   Chen, Dong Dong ^b   Whalin, Matthew K ^b   Xu, Ge Lin ^a   Liu, Xin Feng ^a   Wei, Ling ^b  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Autophagy; Blood brain barrier; Cell death; Diabetes; Ischemic stroke

Indexed keywords

3 METHYLADENINE; BECLIN 1; MICROTUBULE ASSOCIATED PROTEIN 2; NICOTINAMIDE; PROTEIN P62; STREPTOZOCIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ATTENUATION; AUTOPHAGOSOME; AUTOPHAGY; BLOOD BRAIN BARRIER; BRAIN DAMAGE; BRAIN ISCHEMIA; CELL ACTIVITY; CELL DEATH; CONTROLLED STUDY; MALE; MOTOR DYSFUNCTION; MOUSE; NEUROPROTECTION; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOPHYSIOLOGY; SENSORIMOTOR FUNCTION; SENSORY DYSFUNCTION;

AUTOPHAGY; BLOOD-BRAIN BARRIER; CELL DEATH; DIABETES; ISCHEMIC STROKE;

ANIMALS; AUTOPHAGY; BRAIN ISCHEMIA; DIABETES MELLITUS, EXPERIMENTAL; MALE; MICE; MICE, INBRED C57BL; SIGNAL TRANSDUCTION;

EID: 84884821329     PISSN: 17555930     EISSN: 17555949     Source Type: Journal    
DOI: 10.1111/cns.12123     Document Type: Article

References (54)

1. Moskowitz MA, Lo EH, Iadecola C. The science of stroke: mechanisms in search of treatments. Neuron 2010;67:181-198.
2. Lawes CM, Parag V, Bennett DA, et al. Blood glucose and risk of cardiovascular disease in the Asia Pacific region. Diabetes Care 2004;27:2836-2842.
3. Gisselsson L, Smith ML, Siesjo BK. Hyperglycemia and focal brain ischemia. J Cereb Blood Flow Metab 1999;19:288-297.
4. Muranyi M, Fujioka M, He Q, et al. Diabetes activates cell death pathway after transient focal cerebral ischemia. Diabetes 2003;52:481-486.
5. Arboix A, Rivas A, Garcia-Eroles L, et al. Cerebral infarction in diabetes: clinical pattern, stroke subtypes, and predictors of in-hospital mortality. BMC Neurol 2005;5:9.
6. Bruno A, Liebeskind D, Hao Q, et al. Diabetes mellitus, acute hyperglycemia, and ischemic stroke. Curr Treat Options Neurol 2010;12:492-503.
7. Wei L, Ying DJ, Cui L, et al. Necrosis, apoptosis and hybrid death in the cortex and thalamus after barrel cortex ischemia in rats. Brain Res 2004;1022:54-61.
8. Biessels GJ, van der Heide LP, Kamal A, et al. Ageing and diabetes: implications for brain function. Eur J Pharmacol 2002;441:1-14.
9. Eisenberg-Lerner A, Bialik S, Simon HU, et al. Life and death partners: apoptosis, autophagy and the cross-talk between them. Cell Death Differ 2009;16:966-975.
10. Puyal J, Vaslin A, Mottier V, et al. Postischemic treatment of neonatal cerebral ischemia should target autophagy. Ann Neurol 2009;66:378-389.
11. Wang P, Miao CY. Autophagy in the disorders of central nervous system: vital and/or fatal? CNS Neurosci Ther 2012;18:955-956.
12. Wei K, Wang P, Miao CY. A double-edged sword with therapeutic potential: an updated role of autophagy in ischemic cerebral injury. CNS Neurosci Ther 2012;18:879-886.
13. Chen ZF, Li YB, Han JY, et al. The double-edged effect of autophagy in pancreatic beta cells and diabetes. Autophagy 2011;7:12-16.
14. Kaniuk NA, Kiraly M, Bates H, et al. Ubiquitinated-protein aggregates form in pancreatic beta-cells during diabetes-induced oxidative stress and are regulated by autophagy. Diabetes 2007;56:930-939.
15. Tanaka Y, Kume S, Kitada M, et al. Autophagy as a therapeutic target in diabetic nephropathy. Exp Diabetes Res 2012;2012:628978.
16. Gonzalez CD, Lee MS, Marchetti P, et al. The emerging role of autophagy in the pathophysiology of diabetes mellitus. Autophagy 2011;7:2-11.
17. Zhang T, Yan W, Li Q, et al. 3-n-Butylphthalide (NBP) attenuated neuronal autophagy and amyloid-beta expression in diabetic mice subjected to brain ischemia. Neurol Res 2011;33:396-404.
18. Bouet V, Boulouard M, Toutain J, et al. The adhesive removal test: a sensitive method to assess sensorimotor deficits in mice. Nat Protoc 2009;4:1560-1564.
19. He S, Wang C, Dong H, et al. Immune-related GTPase M (IRGM1) regulates neuronal autophagy in a mouse model of stroke. Autophagy 2012;8:1621-1627.
20. Liu C, Gao Y, Barrett J, et al. Autophagy and protein aggregation after brain ischemia. J Neurochem 2010;115:68-78.
21. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell 2010;140:313-326.
22. Wen YD, Sheng R, Zhang LS, et al. Neuronal injury in rat model of permanent focal cerebral ischemia is associated with activation of autophagic and lysosomal pathways. Autophagy 2008;4:762-769.
23. Grishchuk Y, Ginet V, Truttmann AC, et al. Beclin 1-independent autophagy contributes to apoptosis in cortical neurons. Autophagy 2011;7:1115-1131.
24. Zhang T, Liu X, Li Q, et al. Exacerbation of ischemia-induced amyloid-beta generation by diabetes is associated with autophagy activation in mice brain. Neurosci Lett 2010;479:215-220.
25. Masiello P, Broca C, Gross R, et al. Experimental NIDDM: development of a new model in adult rats administered streptozotocin and nicotinamide. Diabetes 1998;47:224-229.
26. Novelli M, D'Aleo V, Lupi R, et al. Reduction of oxidative stress by a new low-molecular-weight antioxidant improves metabolic alterations in a nonobese mouse diabetes model. Pancreas 2007;35:e10-e17.
27. Whitaker VR, Cui L, Miller S, et al. Whisker stimulation enhances angiogenesis in the barrel cortex following focal ischemia in mice. J Cereb Blood Flow Metab 2007;27:57-68.
28. Xiao AY, Wei L, Xia S, et al. Ionic mechanism of ouabain-induced concurrent apoptosis and necrosis in individual cultured cortical neurons. J Neurosci 2002;22:1350-1362.
29. Kihara A, Kabeya Y, Ohsumi Y, et al. Beclin-phosphatidylinositol 3-kinase complex functions at the trans-Golgi network. EMBO Rep 2001;2:330-335.
30. Rangaraju S, Verrier JD, Madorsky I, et al. Rapamycin activates autophagy and improves myelination in explant cultures from neuropathic mice. J Neurosci 2010;30:11388-11397.
31. Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000;19:5720-5728.
32. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007;3:542-545.
33. Tanida I, Ueno T, Kominami E. LC3 and Autophagy. Methods Mol Biol 2008;445:77-88.
34. Bjorkoy G, Lamark T, Brech A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol 2005;171:603-614.
35. Liu W, Hendren J, Qin XJ, et al. Normobaric hyperoxia attenuates early blood-brain barrier disruption by inhibiting MMP-9-mediated occludin degradation in focal cerebral ischemia. J Neurochem 2009;108:811-820.
36. Tavelin S, Hashimoto K, Malkinson J, et al. A new principle for tight junction modulation based on occludin peptides. Mol Pharmacol 2003;64:1530-1540.
37. Wei L, Han BH, Li Y, et al. Cell death mechanism and protective effect of erythropoietin after focal ischemia in the whisker-barrel cortex of neonatal rats. J Pharmacol Exp Ther 2006;317:109-116.
38. Nakamura T, Terajima T, Ogata T, et al. Establishment and pathophysiological characterization of type 2 diabetic mouse model produced by streptozotocin and nicotinamide. Biol Pharm Bull 2006;29:1167-1174.
39. Harada S, Fujita-Hamabe W, Tokuyama S. Ischemic stroke and glucose intolerance: a review of the evidence and exploration of novel therapeutic targets. J Pharmacol Sci 2012;118:1-13.
40. Folbergrova J, Memezawa H, Smith ML, et al. Focal and perifocal changes in tissue energy state during middle cerebral artery occlusion in normo- and hyperglycemic rats. J Cereb Blood Flow Metab 1992;12:25-33.
41. Widmer H, Abiko H, Faden AI, et al. Effects of hyperglycemia on the time course of changes in energy metabolism and pH during global cerebral ischemia and reperfusion in rats: correlation of 1H and 31P NMR spectroscopy with fatty acid and excitatory amino acid levels. J Cereb Blood Flow Metab 1992;12:456-468.
42. Yan J, Feng Z, Liu J, et al. Enhanced autophagy plays a cardinal role in mitochondrial dysfunction in type 2 diabetic Goto-Kakizaki (GK) rats: ameliorating effects of (-)-epigallocatechin-3-gallate. J Nutr Biochem 2012;23:716-724.
43. Shintani T, Klionsky DJ. Autophagy in health and disease: a double-edged sword. Science 2004;306:990-995.
44. Levine B, Klionsky DJ. Development by self-digestion: molecular mechanisms and biological functions of autophagy. Devel Cell 2004;6:463-477.
45. Wang P, Guan YF, Du H, et al. Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy 2012;8:77-87.
46. Sheng R, Liu XQ, Zhang LS, et al. Autophagy regulates endoplasmic reticulum stress in ischemic preconditioning. Autophagy 2012;8:310-325.
47. Petiot A, Ogier-Denis E, Blommaart EF, et al. Distinct classes of phosphatidylinositol 3'-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J Biol Chem 2000;275:992-998.
48. Yu L, Alva A, Su H, et al. Regulation of an ATG7-beclin 1 program of autophagic cell death by caspase-8. Science 2004;304:1500-1502.
49. Shimizu S, Kanaseki T, Mizushima N, et al. Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 2004;6:1221-1228.
50. Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005;122:927-939.
51. Zhang T, Jia W. Sun X 3-n-Butylphthalide (NBP) reduces apoptosis and enhances vascular endothelial growth factor (VEGF) up-regulation in diabetic rats. Neurol Res 2010;32:390-396.
52. Levine B, Sinha S, Kroemer G. Bcl-2 family members: dual regulators of apoptosis and autophagy. Autophagy 2008;4:600-606.
53. Denton D, Nicolson S, Kumar S. Cell death by autophagy: facts and apparent artefacts. Cell Death Differ 2012;19:87-95.
54. Galluzzi L, Vitale I, Abrams JM, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 2012;19:107-120.