Tumor suppressor PTEN affects tau phosphorylation, aggregation, and binding to microtubules

FASEB Journal

Volumn 20, Issue 8, 2006, Pages

  Zhang, Xue ^a   Li, Feng ^a   Bulloj, Ayelen ^a,b   Zhang, Yun Wu ^a   Tong, Gang ^a   Zhang, Zhuohua ^a   Liao, Francesca Fang ^a   Xu, Huaxi ^a  

^a BURNHAM INSTITUTE   (United States)

^b FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

Alzheimer's disease; PIP3 Akt; Tauopathy

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; INOSITOL 1,4,5 TRISPHOSPHATE; PTEN PROTEIN, HUMAN; SERINE; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; CELL STRUCTURE; ENZYME ACTIVITY; MICROTUBULE; MONKEY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; ANIMAL; BRAIN; CELL STRAIN COS1; CERCOPITHECUS; CYTOLOGY; ENZYMOLOGY; GENETICS; HUMAN; METABOLISM; MOUSE; MUTATION; NERVE CELL; PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ALZHEIMER DISEASE; ANIMALS; BRAIN; CERCOPITHECUS AETHIOPS; COS CELLS; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE; MICE; MICROTUBULES; MUTATION; NEURONS; PHOSPHORYLATION; PTEN PHOSPHOHYDROLASE; RATS; RATS, SPRAGUE-DAWLEY; SERINE; SIGNAL TRANSDUCTION; TAU PROTEINS;

EID: 33845619414     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-5721fje     Document Type: Article

References (58)

1. Grundke-Iqbal, I., Iqbal, K., Tung, Y. C., Quinlan, M., Wisniewski, H. M., and Binder, L. I. (1986) Abnormal phosphorylation of the microtubule-associated protein tau (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. USA 83, 4913-4917
2. Lee, V. M., Goedert, M., and Trojanowski, J. Q. (2001) Neurodegenerative tauopathies. Annu. Rev. Neurosci. 24, 1121-1159
3. Hutton, M., Lendon, C. L., Rizzu, P., Baker, M., Froelich, S., Houlden, H., Pickering-Brown, S., Chakraverty, S., Isaacs, A., Grover, A., et al. (1998) Association of missense and 5′-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393, 702-705
4. Poorkaj, P., Bird, T. D., Wijsman, E., Nemens, E., Garruto, R. M., Anderson, L., Andreadis, A., Wiederholt, W. C., Raskind, M., and Schellenberg, G. D. (1998) Tau is a candidate gene for chromosome 17 frontotemporal dementia. Ann Neurol 43, 815-825
5. Spillantini, M. G., Murrell, J. R., Goedert, M., Farlow, M. R., Klug, A., and Ghetti, B. (1998) Mutation in the tau gene in familial multiple system tauopathy with presenile dementia. Proc. Natl. Acad. Sci. USA 95, 7737-7741
6. Weingarten, M. D., Lockwood, A. H., Hwo, S. Y., and Kirschner, M. W. (1975) A protein factor essential for microtubule assembly. Proc. Natl. Acad. Sci. USA 72, 1858-1862
7. Cleveland, D. W., Hwo, S. Y., and Kirschner, M. W. (1977) Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J. Mol. Biol. 116, 207-225
8. Cleveland, D. W., Hwo, S. Y., and Kirschner, M. W. (1977) Physical and chemical properties of purified tau factor and the role of tau in microtubule assembly. J. Mol. Biol. 116, 227-247
9. Ksiezak-Reding, H., Pyo, H. K., Feinstein, B., and Pasinetti, G. M. (2003) Akt/PKB kinase phosphorylates separately Thr212 and Ser214 of tau protein in vitro. Biochim Biophys Acta 1639, 159-168
10. Kopke, 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
11. Kenessey, A., and Yen, S. H. (1993) The extent of phosphorylation of fetal tau is comparable to that of PHF-tau from Alzheimer paired helical filaments. Brain Res. 629, 40-46
12. 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. USA 91, 5562-5566
13. 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. USA 98, 6923-6928
14. Stokoe, D. (2001) Pten. Curr. Biol. 11, R502
15. Li, D. M., and Sun, H. (1997) TEP1, encoded by a candidate tumor suppressor locus, is a novel protein tyrosine phosphatase regulated by transforming growth factor beta. Cancer Res. 57, 2124-2129
16. Li, J., Yen, C., Liaw, D., Podsypanina, K., Bose, S., Wang, S. I., Puc, J., Miliaresis, C., Rodgers, L., McCombie, R., et al. (1997) PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275, 1943-1947
17. Steck, P. A., Pershouse, M. A., Jasser, S. A., Yung, W. K., Lin, H., Ligon, A. H., Langford, L. A., Baumgard, M. L., Hattier, T., Davis, T., et al. (1997) Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat. Genet. 15, 356-362
18. Maehama, T., and Dixon, J. E. (1998) The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273, 13375-13378
19. Stiles, B., Groszer, M., Wang, S., Jiao, J., and Wu, H. (2004) PTENless means more. Dev. Biol. 273, 175-184
20. Sulis, M. L., and Parsons, R. (2003) PTEN: from pathology to biology. Trends Cell Biol. 13, 478-483
21. Myers, M. P., Pass, I., Batty, I. H., Van der Kaay, J., Stolarov, J. P., Hemmings, B. A., Wigler, M. H., Downes, C. P., and Tonks, N. K. (1998) The lipid phosphatase activity of PTEN is critical for its tumor supressor function. Proc. Natl. Acad. Sci. USA 95, 13513-13518
22. Di Cristofano, A., Pesce, B., Cordon-Cardo, C., and Pandolfi, P. P. (1998) Pten is essential for embryonic development and tumour suppression. Nat. Genet. 19, 348-355
23. Podsypanina, K., Ellenson, L. H., Nemes, A., Gu, J., Tamura, M., Yamada, K. M., Cordon-Cardo, C., Catoretti, G., Fisher, P. E., and Parsons, R. (1999) Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc. Natl. Acad. Sci. USA 96, 1563-1568
24. Stambolic, V., Suzuki, A., de la Pompa, J. L., Brothers, G. M., Mirtsos, C., Sasaki, T., Ruland, J., Penninger, J. M., Siderovski, D. P., et al. (1998) Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95, 29-39
25. Suzuki, A., de la Pompa, J. L., Stambolic, V., Elia, A. J., Sasaki, T., del Barco Barrantes, I., Ho, A., Wakeham, A., Itie, A., Khoo, W., et al. (1998) High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice. Curr. Biol. 8, 1169-1178
26. Kwon, C. H., Zhu, X., Zhang, J., Knoop, L. L., Tharp, R., Smeyne, R. J., Eberhart, C. G., Burger, P. C., and Baker, S. J. (2001) Pten regulates neuronal soma size: a mouse model of Lhermitte-Duclos disease. Nat. Genet. 29, 404-411
27. Fraser, M. M., Zhu, X., Kwon, C. H., Uhlmann, E. J., Gutmann, D. H., and Baker, S. J. (2004) Pten loss causes hypertrophy and increased proliferation of astrocytes in vivo. Cancer Res. 64, 7773-7779
28. Griffin, R. J., Moloney, A., Kelliher, M., Johnston, J. A., Ravid, R., Dockery, P., O'Connor, R., and O'Neill, C. (2005) Activation of Akt/PKB, increased phosphorylation of Akt substrates and loss and altered distribution of Akt and PTEN are features of Alzheimer's disease pathology. J. Neurochem. 93, 105-117
29. Hanger, D. P., Hughes, K., Woodgett, J. R., Brion, J. P., and Anderton, B. H. (1992) Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci. Lett. 147, 58-62
30. Mandelkow, E. M., Drewes, G., Biernat, J., Gustke, N., Van Lint, J., Vandenheede, J. R., and Mandelkow, E. (1992) Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett. 314, 315-321
31. Lovestone, S., Reynolds, C. H., Latimer, D., Davis, D. R., Anderton, B. H., Gallo, J. M., Hanger, D., Mulot, S., Marquardt, B., Stabel, S., et al. (1994) Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol. 4, 1077-1086
32. Moreno, F. J., Medina, M., Perez, M., Montejo de Garcini, E., and Avila, J. (1995) Glycogen synthase kinase 3 phosphorylates recombinant human tau protein at serine-262 in the presence of heparin (or tubulin). FEBS Lett. 372, 65-68
33. Sperber, B. R., Leight, S., Goedert, M., and Lee, V. M. (1995) Glycogen synthase kinase-3 beta phosphorylates tau protein at multiple sites in intact cells. Neurosci. Lett. 197, 149-153
34. Gouras, G. K., Xu, H., Jovanovic, J. N., Buxbaum, J. D., Wang, R., Greengard, P., Relkin, N. R., and Gandy, S. (1998) Generation and regulation of beta-amyloid peptide variants by neurons. J. Neurochem. 71, 1920-1925
35. Dou, F., Netzer, W. J., Tanemura, K., Li, F., Hartl, F. U., Takashima, A., Gouras, G. K., Greengard, P., and Xu, H. (2003) Chaperones increase association of tau protein with microtubules. Proc. Natl. Acad. Sci. U. S. A. 100, 721-726
36. 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
37. Kyoung Pyo, H., Lovati, E., Pasinetti, G. M., and Ksiezak-Reding, H. (2004) Phosphorylation of tau at THR212 and SER214 in human neuronal and glial cultures: the role of AKT. Neuroscience 127, 649-658
38. Mahimainathan, L., and Choudhury, G. G. (2004) Inactivation of platelet-derived growth factor receptor by the tumor suppressor PTEN provides a novel mechanism of action of the phosphatase. J. Biol. Chem. 279, 15258-15268
39. Imahori, K., Hoshi, M., Ishiguro, K., Sato, K., Takahashi, M., Shiurba, R., Yamaguchi, H., Takashima, A., and Uchida, T. (1998) Possible role of tau protein kinases in pathogenesis of Alzheimer's disease. Neurobiol. Aging 19, S93-98
40. Sun, H., Lesche, R., Li, D. M., Liliental, J., Zhang, H., Gao, J., Gavrilova, N., Mueller, B., Liu, X., and Wu, H. (1999) PTEN modulates cell cycle progression and cell survival by regulating phosphatidylinositol 3,4,5,-trisphosphate and Akt/protein kinase B signaling pathway. Proc. Natl. Acad. Sci. USA 96, 6199-6204
41. Bondy, C. A., and Cheng, C. M. (2004) Signaling by insulin-like growth factor 1 in brain. Eur. J. Pharmacol. 490, 25-31
42. Gasparini, L., and Xu, H. (2003) Potential roles of insulin and IGF-1 in Alzheimer's disease. Trends Neurosci. 26, 404-406
43. Carro, E., and Torres-Aleman, I. (2004) The role of insulin and insulin-like growth factor I in the molecular and cellular mechanisms underlying the pathology of Alzheimer's disease. Eur. J. Pharmacol. 490, 127-133
44. Hong, M., and Lee, V. M. (1997) Insulin and insulin-like growth factor-1 regulate tau phosphorylation in cultured human neurons. J. Biol. Chem. 272, 19547-19553
45. Schubert, M., Brazil, D. P., Burks, D. J., Kushner, J. A., Ye, J., Flint, C. L., Farhang-Fallah, J., Dikkes, P., Warot, X. M., Rio, C., et al. (2003) Insulin receptor substrate-2 deficiency impairs brain growth and promotes tau phosphorylation. J. Neurosci. 23, 7084-7092
46. Lesort, M., Jope, R. S., and Johnson, G. V. (1999) Insulin transiently increases tau phosphorylation: involvement of glycogen synthase kinase-3beta and Fyn tyrosine kinase. J. Neurochem. 72, 576-584
47. Lesort, M., and Johnson, G. V. (2000) Insulin-like growth factor-1 and insulin mediate transient site-selective increases in tau phosphorylation in primary cortical neurons. Neuroscience 99, 305-316
48. Illenberger, S., Zheng-Fischhofer, Q., Preuss, U., Stamer, K., Baumann, K., Trinczek, B., Biernat, J., Godemann, R., Mandelkow, E. M., et al. (1998) The endogenous and cell cycledependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol. Biol. Cell 9, 1495-1512
49. Weng, L. P., Brown, J. L., Baker, K. M., Ostrowski, M. C., and Eng, C. (2002) PTEN blocks insulin-mediated ETS-2 phosphorylation through MAP kinase, independently of the phosphoinositide 3-kinase pathway. Hum. Mol. Genet. 11, 1687-1696
50. Michikawa, M. (2003) The role of cholesterol in pathogenesis of Alzheimer's disease: dual metabolic interaction between amyloid beta-protein and cholesterol. Mol. Neurobiol. 27, 1-12
51. Tanzi, R. E., and Bertram, L. (2001) New frontiers in Alzheimer's disease genetics. Neuron 32, 181-184
52. Kehoe, P., Wavrant-De Vrieze, F., Crook, R., Wu, W. S., Holmans, P., Fenton, I., Spurlock, G., Norton, N., Williams, H., Williams, N., et al. (1999) A full genome scan for late onset Alzheimer's disease. Hum. Mol. Genet. 8, 237-245
53. Bertram, L., Blacker, D., Mullin, K., Keeney, D., Jones, J., Basu, S., Yhu, S., McInnis, M. G., Go, R. C., Vekrellis, K., et al. (2000) Evidence for genetic linkage of Alzheimer's disease to chromosome 10q. Science 290, 2302-2303
54. Myers, M. P., Stolarov, J. P., Eng, C., Li, J., Wang, S. I., Wigler, M. H., Parsons, R., and Tonks, N. K. (1997) P-TEN, the tumor suppressor from human chromosome 10q23, is a dual-specificity phosphatase. Proc. Natl. Acad. Sci. USA 94, 9052-9057
55. Derkinderen, P., Scales, T. M., Hanger, D. P., Leung, K. Y., Byers, H. L., Ward, M. A., Lenz, C., Price, C., Bird, I. N., Perera, T., et al. (2005) Tyrosine 394 is phosphorylated in Alzheimer's paired helical filament tau and in fetal tau with c-Abl as the candidate tyrosine kinase. J. Neurosci. 25, 6584-6593
56. Ducruet, A. P., Vogt, A., Wipf, P., and Lazo, J. S. (2005) Dual specificity protein phosphatases: therapeutic targets for cancer and Alzheimer's disease. Annu. Rev. Pharmacol. Toxicol. 45, 725-750
57. Pei, J. J., Khatoon, S., An, W. L., Nordlinder, M., Tanaka, T., Braak, H., Tsujio, I., Takeda, M., Alafuzoff, I., Winblad, B., et al. (2003) Role of protein kinase B in Alzheimer's neurofibrillary pathology. Acta Neuropathol. (Berl) 105, 381-392
58. Rickle, A., Bogdanovic, N., Volkman, I., Winblad, B., Ravid, R., and Cowburn, R. F. (2004) Akt activity in Alzheimer's disease and other neurodegenerative disorders. Neuroreport 15, 955-959