Cytoplasmic retention of protein phosphatase 2A inhibitor 2 (I2PP2A) induces alzheimer-like abnormal hyperphosphorylation of Tau

Journal of Biological Chemistry

Volumn 289, Issue 40, 2014, Pages 27677-27691

  Arif, Mohammad ^a   Wei, Jianshe ^a   Zhang, Qi ^a   Liu, Fei ^a   Basurto Islas, Gustavo ^a   Grundke lqbal, Inge ^a   Iqbal, Khalid ^a  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN; CELLS; CYTOLOGY; NEURODEGENERATIVE DISEASES; NEURONS; PHOSPHORYLATION; PROTEINS;

ENDOGENOUS INHIBITOR; HYPERPHOSPHORYLATION; IMMUNOPRECIPITATIONS; MICROTUBULE NETWORKS; NEUROFIBRILLARY TANGLES; NUCLEAR LOCALIZATION; NUCLEAR LOCALIZATION SIGNAL; PROTEIN PHOSPHATASE 2A;

PHOSPHATASES;

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; GLYCOGEN SYNTHASE KINASE 3BETA; PHOSPHOPROTEIN PHOSPHATASE 2A; PHOSPHOPROTEIN PHOSPHATASE 2A INHIBITOR; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; TAU PROTEIN; UNCLASSIFIED DRUG; CHAPERONE; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; MAPT PROTEIN, HUMAN; NUCLEAR LOCALIZATION SIGNAL; PHOSPHOPROTEIN PHOSPHATASE 2; SET PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ALZHEIMER DISEASE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; DRUG PROTEIN BINDING; DRUG TARGETING; ENZYME INHIBITION; GENETIC CONSERVATION; IMMUNOPRECIPITATION; MICROTUBULE; MOLECULAR STABILITY; NERVE CELL NETWORK; NERVE FIBER GROWTH; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; BRAIN; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION;

ALZHEIMER DISEASE; BRAIN; CELL NUCLEUS; CYTOPLASM; GLYCOGEN SYNTHASE KINASE 3; HISTONE CHAPERONES; HUMANS; NUCLEAR LOCALIZATION SIGNALS; PHOSPHORYLATION; PROTEIN PHOSPHATASE 2; TAU PROTEINS; TRANSCRIPTION FACTORS;

EID: 84907495395     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.565358     Document Type: Article

References (73)

1. Iqbal, K., Liu, F., Gong, C. X., Alonso Adel, C., and Grundke-Iqbal, I. (2009) Mechanisms of tau-induced neurodegeneration. Acta Neuropathol. 118, 53-69
2. Goedert, M., Clavaguera, F., and Tolnay, M. (2010) The propagation of prion-like protein inclusions in neurodegenerative diseases. Trends Neurosci. 33, 317-325
3. Alonso, A. D., Di Clerico,J., Li, B., Corbo, C. P., Alaniz, M. E., Grundke-Iqbal, I., and Iqbal, K. (2010) Phosphorylation of Tau at Thr212, Thr231, and Ser262 combined causes neurodegeneration. J. Biol. Chem. 285, 30851-30860
4. Alonso, A. D., Grundke-Iqbal, I., Barra, H. S., and Iqbal, K. (1997) Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proc. Natl. Acad. Sci. U.S.A. 94, 298-303
5. Alonso, A. C., Grundke-Iqbal, I., and Iqbal, K. (1996) Alzheimer's disease hyperphosphorylated tau sequesters normal tau into tangles of filaments and disassembles microtubules. Nat. Med. 2, 783-787
6. Alonso, A. C., Zaidi, T., Grundke-Iqbal, I., and Iqbal, K. (1994) Role of abnormally phosphorylated tau in the breakdown of microtubules in Alzheimer disease. Proc. Natl. Acad. Sci. U.S.A. 91, 5562-5566
7. Li, B., Chohan, M. O., Grundke-Iqbal, I., and Iqbal, K. (2007) Disruption of microtubule network by Alzheimer abnormally hyperphosphorylated tau. Acta Neuropathol. 113, 501-511
8. Köpke, E., Tung, Y. C., Shaikh, S., Alonso, A. C., Iqbal, K., and Grundke-Iqbal, I. (1993) Microtubule-associated protein tau. Abnormal phosphorylation of a non-paired helical filament pool in Alzheimer disease. J. Biol. Chem. 268, 24374-24384
9. Alafuzoff, I., Iqbal, K., Friden, H., Adolfsson, R., and Winblad, B. (1987) Histopathological criteria for progressive dementia disorders: clinicalpathological correlation and classification by multivariate data analysis. Acta Neuropathol. 74, 209-225
10. Arriagada, P. V., Growdon, J. H., Hedley-Whyte, E. T., and Hyman, B. T. (1992) Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology 42, 631- 639
11. Polydoro, M., Acker, C. M., Duff, K., Castillo, P. E., and Davies, P. (2009) Age-dependent impairment of cognitive and synaptic function in the htau mouse model of tau pathology. J. Neurosci. 29, 10741-10749
12. Small, S. A., and Duff, K. (2008) Linking Aß and tau in late-onset Alzheimer's disease: a dual pathway hypothesis. Neuron 60, 534 -542
13. Liu, F., Grundke-Iqbal, I., Iqbal, K., and Gong, C. X. (2005) Contributions of protein phosphatases PP1, PP2A, PP2B and PP5 to the regulation of tau phosphorylation. Eur. J. Neurosci. 22, 1942-1950
14. Wang, J. Z., Grundke-Iqbal, I., and Iqbal, K. (2007) Kinases and phosphatases and tau sites involved in Alzheimer neurofibrillary degeneration. Eur. J. Neurosci. 25, 59-68
15. Gong, C. X., Shaikh, S., Wang, J. Z., Zaidi, T., Grundke-Iqbal, I., and Iqbal, K. (1995) Phosphatase activity toward abnormally phosphorylated tau: decrease in Alzheimer disease brain.J. Neurochem. 65, 732-738
16. Gong, C. X., Singh, T. J., Grundke-Iqbal, I., and Iqbal, K. (1993) Phosphoprotein phosphatase activities in Alzheimer disease brain. J. Neurochem. 61, 921-927
17. Li, M., Guo, H., and Damuni, Z. (1995) Purification and characterization of two potent heat-stable protein inhibitors of protein phosphatase 2A from bovine kidney. Biochemistry 34, 1988 -1996
18. Li, M., Makkinje, A., and Damuni, Z. (1996) The myeloid leukemia-associated protein SET is a potent inhibitor of protein phosphatase 2A.J. Biol. Chem. 271, 11059-11062
19. Chen, J., Martin, B. L., and Brautigan, D. L. (1992) Regulation of protein serine-threonine phosphatase type-2A by tyrosine phosphorylation. Science 257, 1261-1264
20. Favre, B., Zolnierowicz, S., Turowski, P., and Hemmings, B. A. (1994) The catalytic subunit of protein phosphatase 2A is carboxyl-methylated in vivo.J. Biol. Chem. 269, 16311-16317
21. Canela, N., Rodriguez-Vilarrupla, A., Estanyol, J. M., Diaz, C., Pujol, M. J., Ageli, N., and Bachs, O. (2003) The SET protein regulates G2/M transition by modulating cyclin B-cyclin-dependent kinase 1 activity.J. Biol. Chem. 278, 1158-1164
22. Shin, K. S., Shin, E. Y., Bae, S. C., Kim, S. R., Jeong, G. B., Kwak, S. J., Ballermann, B. J., and Kim, E. G. (1999) Expression of SET is modulated as a function of cell proliferation.J. Cell Biochem. 74, 119-126
23. ten Klooster, J. P., Leeuwen, I., Scheres, N., Anthony, E. C., and Hordijk, P. L. (2007) Racl-induced cell migration requires membrane recruitment of the nuclear oncogene SET. EMBO J. 26, 336-345
24. Compagnone, N. A., Zhang, P., Vigne,J. L., and Mellon, S. H. (2000) Novel role for the nuclear phosphoprotein SET in transcriptional activation of P450c17 and initiation of neurosteroidogenesis. Mol. Endocrinol. 14, 875-888
25. Seo, S. B., McNamara, P., Heo, S., Turner, A., Lane, W. S., and Chakravarti, D. (2001) Regulation of histone acetylation and transcription by INHAT, a human cellular complex containing the set oncoprotein. Cell 104, 119-130
26. Madeira, A., Pommet, J. M., Prochiantz, A., and Allinquant, B. (2005) SET protein (TAF1ß, I2PP2A) is involved in neuronal apoptosis induced by an amyloid precursor protein cytoplasmic subdomain. FASEB J. 19, 1905-1907
27. Tanimukai, H., Grundke-Iqbal, I., and Iqbal, K. (2005) Up-regulation of inhibitors of protein phosphatase-2A in Alzheimer's disease. Am. J. Pathol. 166, 1761-1771
28. Tsujio, I., Zaidi, T., Xu, J., Kotula, L., Grundke-Iqbal, I., and Iqbal, K. (2005) Inhibitors of protein phosphatase-2A from human brain structures, immunocytological localization and activities towards dephosphorylation of the Alzheimer type hyperphosphorylated tau. FEBS Lett. 579, 363-372
29. Basurto-Islas, G., Grundke-Iqbal, I., Tung, Y. C., Liu, F., and Iqbal, K. (2013) Activation of asparaginyl endopeptidase leads to Tau hyperphosphorylation in Alzheimer disease. J. Biol. Chem. 288, 17495-17507
30. Chohan, M. O., Khatoon, S., Iqbal, I. G., and Iqbal, K. (2006) Involvement of I2PP2A in the abnormal hyperphosphorylation of tau and its reversal by Memantine. FEBS Lett. 580, 3973-3979
31. Arnaud, L., Chen, S., Liu, F., Li, B., Khatoon, S., Grundke-Iqbal, I., and Iqbal, K. (2011) Mechanism of inhibition of PP2A activity and abnormal hyperphosphorylation of tau by I2PP2A/SET. FEBS Lett. 585, 2653-2659
32. Wang, X., Blanchard, J., Kohlbrenner, E., Clement, N., Linden, R. M., Radu, A., Grundke-Iqbal, I., and Iqbal, K. (2010) The carboxy-terminal fragment of inhibitor-2 of protein phosphatase-2A induces Alzheimer disease pathology and cognitive impairment. FASEB J. 24, 4420-4432
33. Qu, D., Zhang, Y., Ma, J., Guo, K., Li, R., Yin, Y., Cao, X., and Park, D. S. (2007) The nuclear localization of SET mediated by impα3/impß attenu- ates its cytosolic toxicity in neurons.J. Neurochem. 103, 408-422
34. Yu, X. X., Du, X., Moreno, C. S., Green, R. E., Ogris, E., Feng, Q., Chou, L., McQuoid, M. J., and Pallas, D. C. (2001) Methylation of the protein phosphatase 2A catalytic subunit is essential for association of Bα regulatory subunit but not SG2NA, striatin, or polyomavirus middle tumor antigen. Mol. Biol. Cell 12, 185-199
35. Tatebayashi, Y., Iqbal, K., and Grundke-Iqbal, I. (1999) Dynamic regulation of expression and phosphorylation of tau by fibroblast growth factor-2 in neural progenitor cells from adult rat hippocampus. J. Neurosci. 19, 5245-5254
36. Liu, F., Iqbal, K., Grundke-Iqbal, I., Hart, G. W., and Gong, C. X. (2004) O-GlcNAcylation regulates phosphorylation of tau: a mechanism involved in Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A. 101, 10804-10809
37. Shi, J., Zhang, T., Zhou, C., Chohan, M. O., Gu, X., Wegiel, J., Zhou, J., Hwang, Y. W., Iqbal, K., Grundke-Iqbal, I., Gong, C. X., and Liu, F. (2008) Increased dosage of DyrklA alters alternative splicing factor (ASF)-regulated alternative splicing of tau in Down syndrome. J. Biol. Chem. 283, 28660-28669
38. Seubert, P., Mawal-Dewan, M., Barbour, R., Jakes, R., Goedert, M., Johnson, G. V., Litersky, J. M., Schenk, D., Lieberburg, I., Trojanowski, J. Q., and Lee, V. M.-Y. (1995) Detection of phosphorylated Ser262 in fetal tau, adult tau, and paired helical filament Tau. J. Biol. Chem. 270, 18917-18922
39. Blanchard, J., Wanlca, L., Tung, Y. C., Cárdenas-Aguayo Mdel, C., LaFerla, F. M., Iqbal, K., and Grundke-Iqbal, I. (2010) Pharmacologic reversal of neurogenic and neuroplastic abnormalities and cognitive impairments without affecting Aß and Tau pathologies in 3xTg-AD mice. Acta Neuropathol. 120, 605-621
40. Bolognin, S., Blanchard, J., Wang, X., Basurto-Islas, G., Tung, Y. C., Kohlbrenner, E., Grundke-Iqbal, I., and Iqbal, K. (2012) An experimental rat model of sporadic Alzheimer's disease and rescue of cognitive impairment with a neurotrophic peptide. Acta Neuropathol. 123, 133-151
41. Chen, S., Li, B., Grundke-Iqbal, I., and Iqbal, K. (2008) I1PP2A affects Tau phosphorylation via association with the catalytic subunit of protein phosphatase 2A.J. Biol. Chem. 283, 10513-10521
42. Grundke-Iqbal, I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M., and Binder, L. I. (1986) Abnormal phosphorylation of the microtubuleassociated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. U.S.A. 83, 4913-4917
43. Alonso, A., Zaidi, T., Novak, M., Grundke-Iqbal, I., and Iqbal, K. (2001) Hyperphosphorylation induces self-assembly of tau into tangles of paired helical filaments/straight filaments. Proc. Natl. Acad. Sci. U.S.A. 98, 6923-6928
44. Gong, C. X., Shaikh, S., Grundke-Iqbal, I., and Iqbal, K. (1996) Inhibition of protein phosphatase-2B (calcineurin) activity towards Alzheimer abnormally phosphorylated tau by neuroleptics. Brain Res. 741, 95-102
45. 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., and Wang, J. Z. (2012) Synaptic released zinc promotes Tau hyperphosphorylation by inhibition of protein phosphatase 2A (PP2A).J. Biol. Chem. 287, 11174-11182
46. Wang, X., Blanchard, J., Grundke-Iqbal, I., Wegiel, J., Deng, H. X., Siddique, T., and Iqbal, K. (2014) Alzheimer disease and amyotrophic lateral sclerosis: an etiopathogenie connection. Acta Neuropathol. 127, 243-256
47. Iqbal, K., and Grundke-Iqbal, I. (2005) Metabolic/signal transduction hypothesis of Alzheimer's disease and other tauopathies. Acta Neuropathol. 109, 25-31
48. Qian, W., Shi, J., Yin, X., Iqbal, K., Grundke-Iqbal, I., Gong, C. X., and Liu, F. (2010) PP2A regulates tau phosphorylation directly and also indirectly via activating GSK-3ß.J. Alzheimers Dis. 19, 1221-1229
49. Hernández, F., Langa, E., Cuadros, R., Avila, J., and Villanueva, N. (2010) Regulation of GSK3 isoforms by phosphatases PP1 and PP2A. Mol. Cell Biochem. 344, 211-215
50. Facchinetti, P., Dorard, E., Contremoulins, V., Gaillard, M. C., Déglon, N., Sazdovitch, V., Guihenneuc-Jouyaux, C., Brouillet, E., Duyckaerts, C., and Allinquant, B. (2014) SET translocation is associated with increase in caspase cleaved amyloid precursor protein in CA1 of Alzheimer and Down syndrome patients. Neurobiol. Aging 35, 958 -968
51. Yu, G., Yan, T., Feng, Y., Liu, X., Xia, Y., Luo, H., Wang, J. Z., and Wang, X. (2013) Ser9 phosphorylation causes cytoplasmic detention of I2PP2A/ SET in Alzheimer disease. Neurobiol. Aging 34, 1748-1758
52. Luo, M., Pang, C. W., Gerken, A. E., and Brock, T. G. (2004) Multiple nuclear localization sequences allow modulation of 5-lipoxygenase nuclear import. Traffic 5, 847-854
53. Pei, J. J., Gong, C. X., An, W. L., Winblad, B., Cowburn, R. F., Grundke-Iqbal, I., and Iqbal, K. (2003) Okadaic-acid-induced inhibition of protein phosphatase 2A produces activation of mitogen-activated protein kinases ERK1/2, MEK1/2, and p70 S6, similar to that in Alzheimer's disease. Am.J. Pathol. 163, 845-858
54. Singh, T. J., Wang, J. Z., Novak, M., Kontzekova, E., Grundke-Iqbal, I., and Iqbal, K. (1996) Calcium/calmodulin-dependent protein kinase II phosphorylates tau at Ser-262 but only partially inhibits its binding to microtubules. FEBS Lett. 387, 145-148
55. Sengupta, A., Kabat, J., Novak, M., Wu, Q., Grundke-Iqba, I., and Iqbal, K. (1998) Maximal inhibition of tau binding to microtubules requires the phosphorylation of tau at both Thr 231 and Ser 262. Neurobiol. Aging 19, S124-S524
56. Iijima, K., Gatt, A., and Iijima-Ando, K. (2010) Tau Ser262 phosphorylation is critical for Aß42-induced tau toxicity in a transgenic Drosophila model of Alzheimer's disease. Hum. Mol. Genet. 19, 2947-2957
57. Singh, T. J., Zaidi, T., Grundke-Iqbal, I., and Iqbal, K. (1995) Modulation of GSK-3-catalyzed phosphorylation of microtubule-associated protein tau by non-proline-dependent protein kinases. FEBS Lett. 358, 4-8
58. Gong, C. X., Liu, F., Grundke-Iqbal, I., and Iqbal, K. (2005) Post-translational modifications of tau protein in Alzheimer's disease. J. Neural Transm. 112, 813-838
59. Mandelkow, E., von Bergen, M., Biernat, J., and Mandelkow, E. M. (2007) Structural principles of tau and the paired helical filaments of Alzheimer's disease. Brain Pathol. 17, 83-90
60. Jeganathan, S., Hascher, A., Chinnathambi, S., Biernat, J., Mandelkow, E. M., and Mandelkow, E. (2008) Proline-directed pseudo-phosphorylation at AT8 and PHF1 epitopes induces a compaction of the paperclip folding of Tau and generates a pathological (MC-1) conformation.J. Biol. Chem. 283, 32066-32076
61. Alonso Adel, C., Li, B., Grundke-Iqbal, I., and Iqbal, K. (2006) Polymerization of hyperphosphorylated tau into filaments eliminates its inhibitory activity. Proc. Natl. Acad. Sci. U.S.A. 103, 8864-8869
62. Sayas, C. L., Avila, J., and Wandoseil, F. (2002) Regulation of neuronal cytoskeleton by lysophosphatidic acid: role of GSR-3. Biochim. Biophys. Acta 1582, 144-153
63. Zhu, L. Q., Zheng, H. Y., Peng, C.X., Liu, D., Li, H. L., Wang, Q., and Wang, J. Z. (2010) Protein phosphatase 2A facilitates axonogenesis by dephosphorylating CRMP2.J. Neurosci. 30, 3839-3848
64. Virshup, D. M., and Shenolikar, S. (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol. Cell 33, 537-545
65. Sontag, J. M., and Sontag, E. (2014) Protein phosphatase 2A dysfunction in Alzheimer's disease. Front. Mol. Neurosci. 7, 16
66. Drewes, G., Lichtenberg-Kraag, B., Döring, F., Mandelkow, E. M., Biernat, J., Goris, J., Dorée, M., and Mandelkow, E. (1992) Mitogen activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBOJ. 11, 2131-2138
67. Sironi, J. J., Yen, S. H., Gondal, J. A., Wu, Q., Grundke-Iqbal, I., and Iqbal, K. (1998) Ser-262 in human recombinant tau protein is a markedly more favorable site for phosphorylation by CaMKII than PICA or PhK. FEBS Lett. 436, 471-475
68. Bennecib, M., Gong, C. X., Grundke-Iqbal, I., and Iqbal, K. (2001) Inhibition of PP-2A upregulates CaMKII in rat forebrain and induces hyperphosphorylation of tau at Ser 262/356. FEBS Lett. 490, 15-22
69. Lam, B. D., Anthony, E. C., and Hordijk, P.L. (2013) Cytoplasmic targeting of the proto-oncogene SET promotes cell spreading and migration. FEBS Lett. 587, 111-119
70. Fukukawa, C., Shima, H., Tanuma, N., Oleada, T., Kato, N., Adachi, Y., and Kikuchi, K. (2005) The oncoprotein I-2PP2A/SET negatively regulates the MEK/ERK pathway and cell proliferation. Int. J. Oncol. 26, 751-756
71. Sobral, L. M., Sousa, L. O., Coletta, R. D., Cabral, H., Greene, L. J., Tajara, E. H., Gutkind, J. S., Curti, C., and Leopoldino, A. M. (2014) Stable SET knockdown in head and neck squamous cell carcinoma promotes cell invasion and the mesenchymal-like phenotype in vitro, as well as necrosis, cisplatin sensitivity and lymph node metastasis in xenograft tumor models. Mol. Cancer 13, 32
72. Liu, G. P., Zhang, Y., Yao, X. Q., Zhang, C. E., Fang, J., Wang, Q., and Wang, J. Z. (2008) Activation of glycogen synthase kinase-3 inhibits pro- tein phosphatase-2A and the underlying mechanisms. Neurohiol. Aging 29, 1348-1358
73. Katayose, Y., Li, M., Al-Murrani, S. W., Shenolikar, S., and Damuni, Z. (2000) Protein phosphatase 2A inhibitors, and I2PP2A, associate with and modify the substrate specificity of protein phosphatase 1. J. Biol. Chem. 275, 9209-9214