Blocking GSK3β-mediated dynamin1 phosphorylation enhances BDNF-dependent TrkB endocytosis and the protective effects of BDNF in neuronal and mouse models of Alzheimer's disease

Neurobiology of Disease

Volumn 74, Issue 1, 2015, Pages 377-391

  Liu, Xiang Hua ^a   Geng, Zhao ^a   Yan, Jing ^a   Li, Ting ^a   Chen, Qun ^a   Zhang, Qun Ye ^a   Chen, Zhe Yu ^a  

^a SHANDONG UNIVERSITY   (China)

Author keywords

Alzheimer's disease; BDNF; Beta amyloid; Dynamin1; Endocytosis; GSK3

Indexed keywords

AMYLOID BETA PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; CASPASE 3; DYNAMIN I; DYNAMIN II; GLYCOGEN SYNTHASE KINASE 3BETA; OLIGOMER; PEPTIDE; PEPTIDE TAT DYN1SPS; PROTEIN KINASE B; SERINE; UNCLASSIFIED DRUG; AMYLOID PRECURSOR PROTEIN; APP PROTEIN, HUMAN; PRESENILIN 1; PSEN1 PROTEIN, HUMAN;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BRAIN NERVE CELL; CELL SURVIVAL; CONTROLLED STUDY; EMBRYO; ENDOCYTOSIS; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; HUMAN; IN VITRO STUDY; MALE; MOUSE; NEUROPROTECTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; RAT; RECOGNITION; SIGNAL TRANSDUCTION; SPATIAL LEARNING; TRANSGENIC MOUSE; ANIMAL; COGNITION; DISEASE MODEL; DRUG EFFECTS; GENETICS; HEK293 CELL LINE; METABOLISM; NERVE CELL; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; PSYCHOLOGY; SPRAGUE DAWLEY RAT;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL SURVIVAL; COGNITION; DISEASE MODELS, ANIMAL; DYNAMIN I; ENDOCYTOSIS; FEMALE; HEK293 CELLS; HUMANS; MALE; MICE, TRANSGENIC; NEURONS; PHOSPHORYLATION; PRESENILIN-1; PROTO-ONCOGENE PROTEINS C-AKT; RATS, SPRAGUE-DAWLEY; RECEPTOR, TRKB;

EID: 84937132551     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2014.11.020     Document Type: Article

References (50)

1. Arancibia S., et al. Protective effect of BDNF against beta-amyloid induced neurotoxicity in vitro and in vivo in rats. Neurobiol. Dis. 2008, 31:316-326.
2. Atwal J.K., et al. The TrkB-Shc site signals neuronal survival and local axon growth via MEK and P13-kinase. Neuron 2000, 27:265-277.
3. Beattie E.C., et al. NGF signals through TrkA to increase clathrin at the plasma membrane and enhance clathrin-mediated membrane trafficking. J. Neurosci. 2000, 20:7325-7333.
4. Bevins R.A., Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nat. Protoc. 2006, 1:1306-1311.
5. Bodmer D., et al. Isoform-specific dephosphorylation of dynamin1 by calcineurin couples neurotrophin receptor endocytosis to axonal growth. Neuron 2011, 70:1085-1099.
6. Chao M.V. Neurotrophins and their receptors: a convergence point for many signalling pathways. Nat. Rev. Neurosci. 2003, 4:299-309.
7. Chen Z.Y., et al. Identification of a maize kernel stress-related protein and its effect on aflatoxin accumulation. Phytopathology 2004, 94:938-945.
8. Chen Z.Y., et al. A novel endocytic recycling signal distinguishes biological responses of Trk neurotrophin receptors. Mol. Biol. Cell 2005, 16:5761-5772.
9. Chen P., et al. Glycogen synthase kinase 3 regulates N-methyl-d-aspartate receptor channel trafficking and function in cortical neurons. Mol. Pharmacol. 2007, 72:40-51.
10. Clayton E.L., et al. Dynamin I phosphorylation by GSK3 controls activity-dependent bulk endocytosis of synaptic vesicles. Nat. Neurosci. 2010, 13:845-851.
11. Du J., et al. A kinesin signaling complex mediates the ability of GSK-3beta to affect mood-associated behaviors. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:11573-11578.
12. Ferguson S.M., De Camilli P. Dynamin, a membrane-remodelling GTPase. Nat. Rev. Mol. Cell Biol. 2012, 13:75-88.
13. Ferguson S.M., et al. A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 2007, 316:570-574.
14. Frame S., Cohen P. GSK3 takes centre stage more than 20years after its discovery. Biochem. J. 2001, 359:1-16.
15. Ginty D.D., Segal R.A. Retrograde neurotrophin signaling: Trk-ing along the axon. Curr. Opin. Neurobiol. 2002, 12:268-274.
16. Grimes M.L., et al. Endocytosis of activated TrkA: evidence that nerve growth factor induces formation of signaling endosomes. J. Neurosci. 1996, 16:7950-7964.
17. Hernandez F., et al. The role of GSK3 in Alzheimer disease. Brain Res. Bull. 2009, 80:248-250.
18. Hernandez F., et al. GSK3: a possible link between beta amyloid peptide and tau protein. Exp. Neurol. 2010, 223:322-325.
19. Hu S., et al. GSK3 inhibitors show benefits in an Alzheimer's disease (AD) model of neurodegeneration but adverse effects in control animals. Neurobiol. Dis. 2009, 33:193-206.
20. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 2001, 24:677-736.
21. Huang E.J., Reichardt L.F. Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 2003, 72:609-642.
22. Huang S.H., et al. Essential role of Hrs in endocytic recycling of full-length TrkB receptor but not its isoform TrkB.T1. J. Biol. Chem. 2009, 284:15126-15136.
23. Huang S.H., et al. BDNF-dependent recycling facilitates TrkB translocation to postsynaptic density during LTP via a Rab11-dependent pathway. J. Neurosci. 2013, 33:9214-9230.
24. Ip N.Y., et al. Cultured hippocampal neurons show responses to BDNF, NT-3, and NT-4, but not NGF. J. Neurosci. 1993, 13:3394-3405.
25. Jo J., et al. Abeta(1-42) inhibition of LTP is mediated by a signaling pathway involving caspase-3, Akt1 and GSK-3beta. Nat. Neurosci. 2011, 14:545-547.
26. Kim W.Y., et al. Essential roles for GSK-3s and GSK-3-primed substrates in neurotrophin-induced and hippocampal axon growth. Neuron 2006, 52:981-996.
27. Kim J.H., et al. Nonmuscle myosin II is required for internalization of the epidermal growth factor receptor and modulation of downstream signaling. J. Biol. Chem. 2012, 287:27345-27358.
28. Klein W.L. Abeta toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem. Int. 2002, 41:345-352.
29. Klein W.L. Abeta toxicity in Alzheimer's disease: globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem. Int. 2002, 41:345-352.
30. Lu B., et al. BDNF-based synaptic repair as a disease-modifying strategy for neurodegenerative diseases. Nat. Rev. Neurosci. 2013, 14:401-416.
31. Mettlen M., et al. Dissecting dynamin's role in clathrin-mediated endocytosis. Biochem. Soc. Trans. 2009, 37:1022-1026.
32. Morris R. Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 1984, 11:47-60.
33. Nagahara A.H., Tuszynski M.H. Potential therapeutic uses of BDNF in neurological and psychiatric disorders. Nat. Rev. Drug Discov. 2011, 10:209-219.
34. Nagahara A.H., et al. Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat. Med. 2009, 15:331-337.
35. Poon W.W., et al. Beta-amyloid impairs axonal BDNF retrograde trafficking. Neurobiol. Aging 2011, 32:821-833.
36. Querfurth H.W., LaFerla F.M. Alzheimer's disease. N. Engl. J. Med. 2010, 362:329-344.
37. Smillie K.J., Cousin M.A. Akt/PKB controls the activity-dependent bulk endocytosis of synaptic vesicles. Traffic 2012, 13:1004-1011.
38. Sofola O., et al. Inhibition of GSK-3 ameliorates Abeta pathology in an adult-onset Drosophila model of Alzheimer's disease. PLoS Genet. 2010, 6:e1001087.
39. Stambolic V., et al. Lithium inhibits glycogen synthase kinase-3 activity and mimics wingless signalling in intact cells. Curr. Biol. 1996, 6:1664-1668.
40. Su Y., et al. Lithium, a common drug for bipolar disorder treatment, regulates amyloid-beta precursor protein processing. Biochemistry 2004, 43:6899-6908.
41. Tessarollo L. Pleiotropic functions of neurotrophins in development. Cytokine Growth Factor Rev. 1998, 9:125-137.
42. Tong L., et al. Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J. Neurosci. 2004, 24:6799-6809.
43. Townsend M., et al. Soluble Abeta inhibits specific signal transduction cascades common to the insulin receptor pathway. J. Biol. Chem. 2007, 282:33305-33312.
44. Valdez G., et al. Trk-signaling endosomes are generated by Rac-dependent macroendocytosis. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12270-12275.
45. Wirths O., Bayer T.A. Neuron loss in transgenic mouse models of Alzheimer's disease. Int. J. Alzheimers Dis. 2010, 2010.
46. Yu H., et al. Variant BDNF Val66Met polymorphism affects extinction of conditioned aversive memory. J. Neurosci. 2009, 29:4056-4064.
47. Yu H., et al. Variant brain-derived neurotrophic factor Val66Met polymorphism alters vulnerability to stress and response to antidepressants. J. Neurosci. 2012, 32:4092-4101.
48. Yuan J., Yankner B.A. Apoptosis in the nervous system. Nature 2000, 407:802-809.
49. Zhang Y., et al. Cell surface Trk receptors mediate NGF-induced survival while internalized receptors regulate NGF-induced differentiation. J. Neurosci. 2000, 20:5671-5678.
50. Zheng J., et al. Clathrin-dependent endocytosis is required for TrkB-dependent Akt-mediated neuronal protection and dendritic growth. J. Biol. Chem. 2008, 283:13280-13288.