Age-dependent increases in tau phosphorylation in the brains of type 2 diabetic rats correlate with a reduced expression of p62

Experimental Neurology

Volumn 248, Issue , 2013, Pages 441-450

  Jung, Hyun Jung ^a   Kim, Yoon Jeong ^a   Eggert, Simone ^b   Chung, Kwang Chul ^c   Choi, Kyeong Sook ^d   Park, Sun Ah ^a  

^a Soonchunhyang University   (South Korea)

^b Rheinland Pfälzische Technische Universität Kaiserslautern Landau   (Germany)

^c Yonsei University   (South Korea)

^d Ajou University School of Medicine   (South Korea)

Author keywords

Aging; Alzheimer's disease; P62; Tau; Type 2 diabetes; Ubiquitin

Indexed keywords

MESSENGER RNA; PROTEASOME; PROTEIN P62; TAU PROTEIN;

AGE DISTRIBUTION; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CHRONIC DISEASE; COMORBIDITY; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE LOCATION; GENETIC CORRELATION; MOLECULAR PATHOLOGY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UBIQUITINATION;

AD; AGING; ALZHEIMER'S DISEASE; BCL-2-INTERACTING PROTEIN-1; BECLIN-1; BOVINE SERUM ALBUMIN; BSA; CALCIUM/CALMODULIN-DEPENDENT PROTEIN KINASE II; CAMKII; CDK5; CYCLIN DEPENDENT KINASE 5; CYCLOPHILIN A; CYPA; GLYCOGEN SYNTHASE KINASE-3Β; LC3B; LETO; LONG-EVANS TOKUSHIMA OTSUKA; MICROTUBULE-ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; NBR1; NEIGHBOR OF BRAC1 GENE 1; OLETF; OTSUKA LONG-EVANS TOKUSHIMA FATTY; P62; PBS CONTAINING 0.2% TRITON X-100; PBST; PGSK3Β; PPP2A; PROTEIN PHOSPHATASE 2; SDS; SODIUM DODECYL SULFATE; T2DM; TAU; TBS; TRIS-BUFFERED SALINE; TYPE 2 DIABETES; UBIQUITIN; UBIQUITIN-PROTEASOME SYSTEM; UPS;

AGE FACTORS; AGING; ANIMALS; BRAIN; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; EPITOPES; HEAT-SHOCK PROTEINS; NEURONS; OBESITY; PHOSPHORYLATION; RATS; SIGNAL TRANSDUCTION; TAU PROTEINS;

EID: 84882748923     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2013.07.013     Document Type: Article

References (48)

1. Adams S.J., DeTure M.A., McBride M., Dickson D.W., Petrucelli L. Three repeat isoforms of tau inhibit assembly of four repeat tau filaments. PLoS One 2010, 5:e10810.
2. Al-Aubaidy H.A., Jelinek H.F. Oxidative DNA damage and obesity in type 2 diabetes mellitus. Eur. J. Endocrinol. 2011, 164:899-904.
3. Alonso A.D., Di Clerico J., Li B., Corbo C.P., Alaniz M.E., Grundke-Iqbal I., Iqbal K. Phosphorylation of tau at Thr212, Thr231, and Ser262 combined causes neurodegeneration. J. Biol. Chem. 2010, 285:30851-30860.
4. Baba M., Nakajo S., Tu P.H., Tomita T., Nakaya K., Lee V.M., Trojanowski J.Q., Iwatsubo T. Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 1998, 152:879-884.
5. Babu J.R., Geetha T., Wooten M.W. Sequestosome 1/p62 shuttles polyubiquitinated tau for proteasomal degradation. J. Neurochem. 2005, 94:192-203.
6. Bingol B., Sheng M. Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron 2011, 69:22-32.
7. Cowan C.M., Bossing T., Page A., Shepherd D., Mudher A. Soluble hyper-phosphorylated tau causes microtubule breakdown and functionally compromises normal tau in vivo. Acta Neuropathol. 2010, 120:593-604.
8. Craft S. The role of metabolic disorders in Alzheimer disease and vascular dementia: two roads converged. Arch. Neurol. 2009, 66:300-305.
9. Cripps D., Thomas S.N., Jeng Y., Yang F., Davies P., Yang A.J. Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. J. Biol. Chem. 2006, 281:10825-10838.
10. den Heijer T., Vermeer S.E., van Dijk E.J., Prins N.D., Koudstaal P.J., Hofman A., Breteler M.M. Type 2 diabetes and atrophy of medial temporal lobe structures on brain MRI. Diabetologia 2003, 46:1604-1610.
11. Deng Y., Li B., Liu Y., Iqbal K., Grundke-Iqbal I., Gong C.X. Dysregulation of insulin signaling, glucose transporters, O-GlcNAcylation, and phosphorylation of tau and neurofilaments in the brain: implication for Alzheimer's disease. Am. J. Pathol. 2009, 175:2089-2098.
12. Du Y., Wooten M.C., Gearing M., Wooten M.W. Age-associated oxidative damage to the p62 promoter: implications for Alzheimer disease. Free Radic. Biol. Med. 2009, 46:492-501.
13. Du Y., Wooten M.C., Wooten M.W. Oxidative damage to the promoter region of SQSTM1/p62 is common to neurodegenerative disease. Neurobiol. Dis. 2009, 35:302-310.
14. Gal J., Strom A.L., Kilty R., Zhang F., Zhu H. p62 accumulates and enhances aggregate formation in model systems of familial amyotrophic lateral sclerosis. J. Biol. Chem. 2007, 282:11068-11077.
15. Geetha T., Zheng C., Vishwaprakash N., Broderick T.L., Babu J.R. Sequestosome 1/p62, a scaffolding protein, is a newly identified partner of IRS-1 protein. J. Biol. Chem. 2012, 287:29672-29678.
16. Hanes J., Zilka N., Bartkova M., Caletkova M., Dobrota D., Novak M. Rat tau proteome consists of six tau isoforms: implication for animal models of human tauopathies. J. Neurochem. 2009, 108:1167-1176.
17. Hartley T., Brumell J., Volchuk A. Emerging roles for the ubiquitin-proteasome system and autophagy in pancreatic beta-cells. Am. J. Physiol. Endocrinol. Metab. 2009, 296:E1-E10.
18. Jung H.J., Park S.S., Mok J.O., Lee T.K., Park C.S., Park S.A. Increased expression of three-repeat isoforms of tau contributes to tau pathology in a rat model of chronic type 2 diabetes. Exp. Neurol. 2011, 228:232-241.
19. Kahn S.E. The relative contributions of insulin resistance and beta-cell dysfunction to the pathophysiology of type 2 diabetes. Diabetologia 2003, 46:3-19.
20. Kaniuk N.A., Kiraly M., Bates H., Vranic M., Volchuk A., Brumell J.H. Ubiquitinated-protein aggregates form in pancreatic beta-cells during diabetes-induced oxidative stress and are regulated by autophagy. Diabetes 2007, 56:930-939.
21. Kawano K., Hirashima T., Mori S., Saitoh Y., Kurosumi M., Natori T. Spontaneous long-term hyperglycemic rat with diabetic complications. Otsuka Long-Evans Tokushima Fatty (OLETF) strain. Diabetes 1992, 41:1422-1428.
22. Ke Y.D., Delerue F., Gladbach A., Gotz J., Ittner L.M. Experimental diabetes mellitus exacerbates tau pathology in a transgenic mouse model of Alzheimer's disease. PLoS One 2009, 4:e7917.
23. Kopeikina K.J., Hyman B.T., Spires-Jones T.L. Soluble forms of tau are toxic in Alzheimer's disease. Transl. Neurosci. 2012, 3:223-233.
24. Kosik K.S., Orecchio L.D., Bakalis S., Neve R.L. Developmentally regulated expression of specific tau sequences. Neuron 1989, 2:1389-1397.
25. Launer L.J. Diabetes and brain aging: epidemiologic evidence. Curr. Diab. Rep. 2005, 5:59-63.
26. Lee M.J., Lee J.H., Rubinsztein D.C. Tau degradation: the ubiquitin-proteasome system versus the autophagy-lysosome system. Prog. Neurobiol. 2013, 105:49-59.
27. Liu F., Grundke-Iqbal I., Iqbal K., Gong C.X. Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur. J. Neurosci. 2005, 22:1942-1950.
28. Liu Y., Liu F., Grundke-Iqbal I., Iqbal K., Gong C.X. Deficient brain insulin signalling pathway in Alzheimer's disease and diabetes. J. Pathol. 2011, 225:54-62.
29. Nakaso K., Yoshimoto Y., Nakano T., Takeshima T., Fukuhara Y., Yasui K., Araga S., Yanagawa T., Ishii T., Nakashima K. Transcriptional activation of p62/A170/ZIP during the formation of the aggregates: possible mechanisms and the role in Lewy body formation in Parkinson's disease. Brain Res. 2004, 1012:42-51.
30. Neumann M., Sampathu D.M., Kwong L.K., Truax A.C., Micsenyi M.C., Chou T.T., Bruce J., Schuck T., Grossman M., Clark C.M., McCluskey L.F., Miller B.L., Masliah E., Mackenzie I.R., Feldman H., Feiden W., Kretzschmar H.A., Trojanowski J.Q., Lee V.M. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006, 314:130-133.
31. Oddo S. The ubiquitin-proteasome system in Alzheimer's disease. J. Cell. Mol. Med. 2008, 12:363-373.
32. Pankiv S., Clausen T.H., Lamark T., Brech A., Bruun J.A., Outzen H., Overvatn A., Bjorkoy G., Johansen T. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J. Biol. Chem. 2007, 282:24131-24145.
33. Park S.A. A common pathogenic mechanism linking type-2 diabetes and Alzheimer's disease: evidence from animal models. J. Clin. Neurol. 2011, 7:10-18.
34. Park S.S., Jung H.J., Kim Y.J., Park T.K., Kim C., Choi H., Mook-Jung I.H., Koo E.H., Park S.A. Asp664 cleavage of amyloid precursor protein induces tau phosphorylation by decreasing protein phosphatase 2A activity. J. Neurochem. 2012, 123:856-865.
35. Planel E., Tatebayashi Y., Miyasaka T., Liu L., Wang L., Herman M., Yu W.H., Luchsinger J.A., Wadzinski B., Duff K.E., Takashima A. Insulin dysfunction induces in vivo tau hyperphosphorylation through distinct mechanisms. J. Neurosci. 2007, 27:13635-13648.
36. Puissant A., Fenouille N., Auberger P. When autophagy meets cancer through p62/SQSTM1. Am. J. Cancer Res. 2012, 2:397-413.
37. Qian W., Shi J., Yin X., Iqbal K., Grundke-Iqbal I., Gong C.X., Liu F. PP2A regulates tau phosphorylation directly and also indirectly via activating GSK-3beta. J. Alzheimers Dis. 2010, 19:1221-1229.
38. Ramesh Babu J., Lamar Seibenhener M., Peng J., Strom A.L., Kemppainen R., Cox N., Zhu H., Wooten M.C., Diaz-Meco M.T., Moscat J., Wooten M.W. Genetic inactivation of p62 leads to accumulation of hyperphosphorylated tau and neurodegeneration. J. Neurochem. 2008, 106:107-120.
39. Rodriguez A., Duran A., Selloum M., Champy M.F., Diez-Guerra F.J., Flores J.M., Serrano M., Auwerx J., Diaz-Meco M.T., Moscat J. Mature-onset obesity and insulin resistance in mice deficient in the signaling adapter p62. Cell Metab. 2006, 3:211-222.
40. Salminen A., Kaarniranta K., Haapasalo A., Hiltunen M., Soininen H., Alafuzoff I. Emerging role of p62/sequestosome-1 in the pathogenesis of Alzheimer's disease. Prog. Neurobiol. 2012, 96:87-95.
41. Santacruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McGowan E., Forster C., Yue M., Orne J., Janus C., Mariash A., Kuskowski M., Hyman B., Hutton M., Ashe K.H. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309:476-481.
42. Seibenhener M.L., Babu J.R., Geetha T., Wong H.C., Krishna N.R., Wooten M.W. Sequestosome 1/p62 is a polyubiquitin chain binding protein involved in ubiquitin proteasome degradation. Mol. Cell. Biol. 2004, 24:8055-8068.
43. Spires-Jones T.L., Stoothoff W.H., de Calignon A., Jones P.B., Hyman B.T. Tau pathophysiology in neurodegeneration: a tangled issue. Trends Neurosci. 2009, 32:150-159.
44. Tai H.C., Serrano-Pozo A., Hashimoto T., Frosch M.P., Spires-Jones T.L., Hyman B.T. The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system. Am. J. Pathol. 2012, 181:1426-1435.
45. van den Berg E., Reijmer Y.D., de Bresser J., Kessels R.P., Kappelle L.J., Biessels G.J. A 4year follow-up study of cognitive functioning in patients with type 2 diabetes mellitus. Diabetologia 2010, 53:58-65.
46. Vigouroux S., Briand M., Briand Y. Linkage between the proteasome pathway and neurodegenerative diseases and aging. Mol. Neurobiol. 2004, 30:201-221.
47. Wang Y., Mandelkow E. Degradation of tau protein by autophagy and proteasomal pathways. Biochem. Soc. Trans. 2012, 40:644-652.
48. Wei N., Yu S.P., Gu X.H., Chen D.D., Whalin M.K., Xu G.L., Liu X.F., Wei L. The involvement of autophagy pathway in exaggerated ischemic brain damage in diabetic mice. CNS Neurosci. Ther 2013, (Jun. 3, Epub ahead of print). 10.1111/cns.12123.