Senescence may mediate conversion of tau phosphorylation-induced apoptotic escape to neurodegeneration

Experimental Gerontology

Volumn 68, Issue , 2015, Pages 82-86

  Wang, Jian Zhi ^a   Wang, Zhi Hao ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Alzheimer's disease; Apoptosis; Hyperphosphorylation; Neurodegeneration; Senescence; Tau

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; BETA CATENIN; BINDING PROTEIN; CASPASE 3; CYTOCHROME C; ELF2 PROTEIN; GLYCOGEN SYNTHASE KINASE 3BETA; IRON REGULATORY FACTOR; PERK PROTEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; TAU PROTEIN; UNCLASSIFIED DRUG; PROTEIN P53;

APOPTOSIS; ARTICLE; BIOACCUMULATION; DISEASE ACTIVITY; DISEASE ASSOCIATION; ENZYME ACTIVATION; HUMAN; MOLECULAR DYNAMICS; MOLECULAR PATHOLOGY; NERVE DEGENERATION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; SENESCENCE; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ALZHEIMER DISEASE; ANIMAL; CELL AGING; DISEASE MODEL; ENDOPLASMIC RETICULUM STRESS; GLIA; METABOLISM; MITOCHONDRION; NERVOUS SYSTEM DEVELOPMENT; NEUROFIBRILLARY TANGLE; PATHOPHYSIOLOGY; PHOSPHORYLATION; PHYSIOLOGY;

ALZHEIMER DISEASE; ANIMALS; APOPTOSIS; CELL AGING; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; HUMANS; MITOCHONDRIA; NEUROFIBRILLARY TANGLES; NEUROGENESIS; NEUROGLIA; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; TAU PROTEINS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84941316353     PISSN: 05315565     EISSN: 18736815     Source Type: Journal    
DOI: 10.1016/j.exger.2015.03.007     Document Type: Article

References (49)

1. Allen B., Ingram E., Takao M., Smith M.J., Jakes R., Virdee K., Yoshida H., Holzer M., Craxton M., Emson P.C., Atzori C., Migheli A., Crowther R.A., Ghetti B., Spillantini M.G., Goedert M. Abundant tau filaments and nonapoptotic neurodegeneration in transgenic mice expressing human P301S tau protein. J. Neurosci. 2002, 22(21):9340-9351. (Nov 1).
2. Arendt T., Stieler J., Strijkstra A.M., Hut R.A., Rüdiger J., Van der Zee E.A., Harkany T., Holzer M., Härtig W. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J. Neurosci. 2003, 23(18):6972-6981. (Aug 6).
3. Chai G.S., Jiang X., Ni Z.F., Ma Z.W., Xie A.J., Cheng X.S., Wang Q., Wang J.Z., Liu G.P. Betaine attenuates Alzheimer-like pathological changes and memory deficits induced by homocysteine. J. Neurochem. 2013, 124(3):388-396. (Feb). 10.1111/jnc.12094.
4. Cheng X.S., Zhao K.P., Jiang X., Du L.L., Li X.H., Ma Z.W., Yao J., Luo Y., Duan D.X., Wang J.Z., Zhou X.W. Nmnat2 attenuates tau phosphorylation through activation of PP2A. J. Alzheimers Dis. 2013, 36(1):185-195. 10.3233/JAD-122173.
5. Duan D.X., Chai G.S., Ni Z.F., Hu Y., Luo Y., Cheng X.S., Chen N.N., Wang J.Z., Liu G.P. Phosphorylation of tau by death-associated protein kinase 1 antagonizes the kinase-induced cell apoptosis. J. Alzheimers Dis. 2013, 37(4):795-808. 10.3233/JAD-130377.
6. Grundke-Iqbal I., Iqbal K., Quinlan M., Tung Y.C., Zaidi M.S., Wisniewski H.M. Microtubule-associated protein tau. A component of Alzheimer paired helical filaments. J. Biol. Chem. 1986, 261:6084-6089.
7. Gu X.M., Huang H.C., Jiang Z.F. Mitochondrial dysfunction and cellular metabolic deficiency in Alzheimer's disease. Neurosci. Bull. 2012, 28(5):631-640. (Oct). 10.1007/s12264-012-1270-2.
8. Hong X.P., Peng C.X., Wei W., Tian Q., Liu Y.H., Yao X.Q., Zhang Y., Cao F.Y., Wang Q., Wang J.Z. Essential role of tau phosphorylation in adult hippocampal neurogenesis. Hippocampus 2010, 20(12):1339-1349.
9. Li H.L., Wang H.H., Liu S.J., Deng Y.Q., Zhang Y.J., Tian Q., Wang X.C., Chen X.Q., Yang Y., Zhang J.Y., Wang Q., Xu H., Liao F.F., Wang J.Z. Phosphorylation of tau antagonizes apoptosis by stabilizing beta-catenin, a mechanism involved in Alzheimer's neurodegeneration. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(9):3591-3596. (Feb 27, Epub 2007 Feb 21).
10. Li X.H., Zhou X.W., Wang J.Z. AGEs induce Alzheimer-like tau pathology and memory deficit via RAGE-mediated GSK-3 activation. Neurobiol. Aging 2012, 33(7):1400-1410. (Jul).
11. Lin L., Yang S.S., Chu J., Wang L., Ning L.N., Zhang T., Jiang Q., Tian Q., Wang J.Z. Region-specific expression of tau, amyloid-β protein precursor, and synaptic proteins at physiological condition or under endoplasmic reticulum stress in rats. J. Alzheimers Dis. 2014, 41(4):1149-1163. (Jan 1). 10.3233/JAD-140207.
12. Liu S.J., Zhang J.Y., Li H.J., Fang Z.Y., Wang Q., Deng H.M., Gong C., Iqbal K., Wang J.Z. Tau becomes a more favorable substrate for GSK-3 when it is prephosphorylated by PKA in rat brain. J. Biol. Chem. 2004, 279(48):50078-50088.
13. Liu G.P., Zhang Y., Yao X.Q., Zhang C.E., Fang J., Wang Q., Wang J.Z. Activation of glycogen synthase kinase-3 inhibits protein phosphatase-2A and the underlying mechanisms. Neurobiol. Aging 2008, 29(9):1348-1358. (Sep).
14. Liu Y.H., Wei W., Yin J., Liu G.P., Wang Q., Cao F.Y., Wang J.Z. Proteasome inhibition increases tau accumulation independent of phosphorylation. Neurobiol. Aging 2009, 30(12):1949-1961. (Dec).
15. Liu X.A., Liao K., Liu R., Wang H.H., Zhang Y., Zhang Q., Wang Q., Li H.L., Tian Q., Wang J.Z. Tau dephosphorylation potentiates apoptosis by mechanisms involving a failed dephosphorylation/activation of Bcl-2. J. Alzheimers Dis. 2010, 19(3):953-962. 10.3233/JAD-2010-1294.
16. Liu X.A., Song J., Jiang Q., Wang Q., Tian Q., Wang J.Z. Expression of the hyperphosphorylated tau attenuates ER stress-induced apoptosis with upregulation of unfolded protein response. Apoptosis 2012, 17(10):1039-1049. (Oct). 10.1007/s10495-012-0744-z.
17. Liu G.P., Wei W., Zhou X., Zhang Y., Shi H.H., Yin J., Yao X.Q., Peng C.X., Hu J., Wang Q., Li H.L., Wang J.Z. I(2)(PP2A) regulates p53 and Akt correlatively and leads the neurons to abort apoptosis. Neurobiol. Aging 2012, 33(2):254-264. (Feb). 10.1016/j.neurobiolaging.2010.01.016.
18. Liu X.P., Zheng H.Y., Qu M., Zhang Y., Cao F.Y., Wang Q., Ke D., Liu G.P., Wang J.Z. Upregulation of astrocytes protein phosphatase-2A stimulates astrocytes migration via inhibiting p38 MAPK in tg2576 mice. Glia 2012, 60(9):1279-1288. (Sep). 10.1002/glia.22347.
19. Liu G.P., Wei W., Zhou X., Shi H.R., Liu X.H., Chai G.S., Yao X.Q., Zhang J.Y., Peng C.X., Hu J., Li X.C., Wang Q., Wang J.Z. Silencing PP2A inhibitor by Lenti-shRNA interference ameliorates neuropathologies and memory deficits in tg2576 mice. Mol. Ther. 2013, 21(12):2247-2257. (Dec).
20. Liu D., Wei N., Man H.Y., Lu Y., Zhu L.Q., Wang J.Z. The MT2 receptor stimulates axonogenesis and enhances synaptic transmission by activating Akt signaling. Cell Death Differ. 2014, (Dec 12, Epub ahead of print). 10.1038/cdd.2014.195.
21. Luo D.J., Feng Q., Wang Z.H., Sun D.S., Wang Q., Wang J.Z., Liu G.P. Knockdown of phosphotyrosyl phosphatase activator induces apoptosis via mitochondrial pathway and the attenuation by simultaneous tau hyperphosphorylation. J. Neurochem. 2014, (May 12). 10.1111/jnc.12761.
22. Luo H.B., Xia Y.Y., Shu X.J., Liu Z.C., Feng Y., Liu X.H., Yu G., Yin G., Xiong Y.S., Zeng K., Jiang J., Ye K., Wang X.C., Wang J.Z. SUMOylation at K340 inhibits tau degradation through deregulating its phosphorylation and ubiquitination. Proc. Natl. Acad. Sci. U. S. A. 2014, 111(46):16586-16591. (Nov 18).
23. Morsch R., Simon W., Coleman P.D. Neurons may live for decades with neurofibrillary tangles. J. Neuropathol. Exp. Neurol. 1999, 58(2):188-197. (Feb).
24. Peng C.X., Hu J., Liu D., Hong X.P., Wu Y.Y., Zhu L.Q., Wang J.Z. Disease-modified glycogen synthase kinase-3β intervention by melatonin arrests the pathology and memory deficits in an Alzheimer's animal model. Neurobiol. Aging 2013, 34(6):1555-1563. (Jun). 10.1016/j.neurobiolaging.2012.12.010.
25. Ren Q.G., Liao X.M., Wang Z.F., Qu Z.S., Wang J.Z. The involvement of glycogen synthase kinase-3 and protein phosphatase-2A in lactacystin-induced tau accumulation. FEBS Lett. 2006, 580(10):2503-2511. (May 1).
26. Ren Q.G., Liao X.M., Chen X.Q., Liu G.P., Wang J.Z. Effects of tau phosphorylation on proteasome activity. FEBS Lett. 2007, 581(7):1521-1528. (Apr 3).
27. Spires T.L., Orne J.D., SantaCruz K., Pitstick R., Carlson G.A., Ashe K.H., Hyman B.T. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am. J. Pathol. 2006, 168(5):1598-1607. (May).
28. Sun X.Y., Wei Y.P., Xiong Y., Wang X.C., Xie A.J., Wang X.L., Yang Y., Wang Q., Lu Y.M., Liu R., Wang J.Z. Synaptic released zinc promotes tau hyperphosphorylation by inhibition of protein phosphatase 2A (PP2A). J. Biol. Chem. 2012, 287(14):11174-11182. (Mar 30).
29. Wang J.Z., Liu F. Microtubule-associated protein tau in development, degeneration and protection of neurons. Prog. Neurobiol. 2008, 85(2):148-175. (Jun, Epub 2008 Mar 22). 10.1016/j.pneurobio.2008.03.002.
30. Wang J.Z., Gong C.X., Zaidi T., Grundke-Iqbal I., Iqbal K. Dephosphorylation of Alzheimer paired helical filaments by protein phosphatase-2A and -2B. J. Biol. Chem. 1995, 270(9):4854-4860. (Mar 3).
31. Wang J.Z., Wu Q., Smith A., Grundke-Iqbal I., Iqbal K. Tau is phosphorylated by GSK-3 at several sites found in Alzheimer disease and its biological activity markedly inhibited only after it is prephosphorylated by A-kinase. FEBS Lett. 1998, 436(1):28-34. (Sep 25).
32. Wang Z.F., Li H.L., Li X.C., Zhang Q., Tian Q., Wang Q., Xu H., Wang J.Z. Effects of endogenous beta-amyloid overproduction on tau phosphorylation in cell culture. J. Neurochem. 2006, 98(4):1167-1175. (Aug, Epub 2006 Jun 6).
33. Wang H.H., Li H.L., Liu R., Zhang Y., Liao K., Wang Q., Wang J.Z., Liu S.J. Tau overexpression inhibits cell apoptosis with the mechanisms involving multiple viability-related factors. J. Alzheimers Dis. 2010, 21(1):167-179. 10.3233/JAD-2010-091279.
34. Wang Z.F., Yin J., Zhang Y., Zhu L.Q., Tian Q., Wang X.C., Li H.L., Wang J.Z. Overexpression of tau proteins antagonizes amyloid-beta-potentiated apoptosis through mitochondria-caspase-3 pathway in N2a cells. J. Alzheimers Dis. 2010, 20(1):145-157. 10.3233/JAD-2010-1351.
35. Wang L., Jiang Q., Chu J., Lin L., Li X.G., Chai G.S., Wang Q., Wang J.Z., Tian Q. Expression of Tau40 induces activation of cultured rat microglial cells. PLoS One 2013, 8(10):e76057. (Oct 11, eCollection 2013). 10.1371/journal.pone.0076057.
36. Wang J.Z., Wang Z.H., Tian Q. Tau hyperphosphorylation induces apoptotic escape and triggers neurodegeneration in Alzheimer's disease. Neurosci. Bull. 2014, 30(2):359-366. (Apr, Epub 2014 Mar 14). 10.1007/s12264-013-1415-y.
37. Xia Y., Liu R., Chen R., Tian Q., Zeng K., Hu J., Liu X., Wang Q., Wang P., Wang X.C., Wang J.Z. Novel multipotent AChEI-CCB attenuates hyperhomocysteinemia-induced memory deficits and neuropathologies in rats. J. Alzheimers Dis. 2014, (Jul 2).
38. Xiong Y., Jing X.P., Zhou X.W., Wang X.L., Yang Y., Sun X.Y., Qiu M., Cao F.Y., Lu Y.M., Liu R., Wang J.Z. Zinc induces protein phosphatase 2A inactivation and tau hyperphosphorylation through Src dependent PP2A (tyrosine 307) phosphorylation. Neurobiol. Aging 2013, 34(3):745-756. (Mar). 10.1016/j.neurobiolaging.2012.07.003.
39. Yin G., Li L.Y., Qu M., Luo H.B., Wang J.Z., Zhou X.W. Upregulation of AKT attenuates amyloid-β-induced cell apoptosis. J. Alzheimers Dis. 2011, 25(2):337-345. 10.3233/JAD-2011-110104.
40. Zhang J.Y., Liu S.J., Li H.L., Wang J.Z. Microtubule-associated protein tau is a substrate of ATP/Mg(2+)-dependent proteasome protease system. J. Neural Transm. 2005, 112(4):547-555. (Apr).
41. Zhang Y.J., Xu Y.F., Liu Y.H., Yin J., Li H.L., Wang Q., Wang J.Z. Peroxynitrite induces Alzheimer-like tau modifications and accumulation in rat brain and its underlying mechanisms. FASEB J. 2006, 20(9):1431-1442.
42. Zhang C.E., Tian Q., Wei W., Peng J.H., Liu G.P., Zhou X.W., Wang Q., Wang D.W., Wang J.Z. Homocysteine induces tau phosphorylation by inactivating protein phosphatase 2A in rat hippocampus. Neurobiol. Aging 2008, 29(11):1654-1665. (Nov).
43. Zhang D.L., Chen Y.Q., Jiang X., Ji T.T., Mei B. Oxidative damage increased in presenilin1/presenilin2 conditional double knockout mice. Neurosci. Bull. 2009, 25:131-137.
44. Zhang C.E., Wei W., Liu Y.H., Peng J.H., Tian Q., Liu G.P., Zhang Y., Wang J.Z. Hyperhomocysteinemia increases beta-amyloid by enhancing expression of gamma-secretase and phosphorylation of amyloid precursor protein in rat brain. Am. J. Pathol. 2009, 74(4):1481-1491.
45. Zhang Y., Ma R.H., Li X.C., Zhang J.Y., Shi H.R., Wei W., Luo D.J., Wang Q., Wang J.Z., Liu G.P. Silencing [formula: see text] rescues tau pathologies and memory deficits through rescuing PP2A and inhibiting GSK-3β signaling in human tau transgenic mice. Front. Aging Neurosci. 2014, 6:123. (Jun 17). 10.3389/fnagi.2014.00123.
46. Zhou F., Zhu X., Castellani R.J., Stimmelmayr R., Perry G., Smith M.A., Drew K.L. Hibernation, a model of neuroprotection. Am. J. Pathol. 2001, 158(6):2145-2151. (Jun).
47. Zhu L.Q., Wang S.H., Yin Y.Y., Liu D., Zheng H.Y., Shi H.R., Tian Q., Wang X.C., Wang Q., Chen J.G., Wang J.Z. Activation of glycogen synthase kinase-3 inhibits long term potentiation with synapse-associated impairments. J. Neurosci. 2007, 27:12211-12220.
48. Zhu L.Q., Liu D., Hu J., Cheng J., Wang S.H., Wang Q., Wang F., Chen J.G., Wang J.Z. GSK-3β inhibits presynaptic vesicle exocytosis by phosphorylating P/Q-type calcium channel and interrupting SNARE complex formation. J. Neurosci. 2010, 30:3824-3833.
49. Zhu L.Q., Zheng H.Y., Peng C.X., Liu D., Li H.L., Wang Q., Wang J.Z. Protein phosphatase 2A facilitates axonogenesis by dephosphorylating CRMP2. J. Neurosci. 2010, 30:3839-3848.