The protein phosphatase PP2A/Bα binds to the microtubule-associated proteins Tau and MAP2 at a motif also recognized by the kinase Fyn: Implications for tauopathies

Journal of Biological Chemistry

Volumn 287, Issue 18, 2012, Pages 14984-14993

  Sontag, Jean Marie ^a,b   Nunbhakdi Craig, Viyada ^b   White III, Charles L ^b   Halpain, Shelley ^c   Sontag, Estelle ^a,b  

^a UNIVERSITY OF NEWCASTLE   (Australia)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; CYTOSKELETAL ORGANIZATION; DEPHOSPHORYLATES; DEPHOSPHORYLATIONS; DOWN-REGULATION; GRAY MATTER; IN-VITRO; ISOFORMS; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE STABILITY; MICROTUBULE-BINDING DOMAINS; MICROTUBULES; MULTIFUNCTIONAL PROTEIN; NEURONAL CELL; NEURONAL PLASTICITY; PROTEIN INTERACTION; PROTEIN PHOSPHATASE; PROTEIN PHOSPHATASE 2A; PROTEIN-TYROSINE KINASE; TAUOPATHIES;

AMINO ACIDS; DEREGULATION; GROWTH KINETICS; NEURODEGENERATIVE DISEASES; PHOSPHATASES; PHOSPHORYLATION;

PROTEINS;

MICROTUBULE ASSOCIATED PROTEIN 2; PHOSPHOPROTEIN PHOSPHATASE 2A; PROLINE; PROTEIN KINASE FYN; TAU PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MATURATION; CONTROLLED STUDY; COW; DOWN REGULATION; GRAY MATTER; HUMAN; HUMAN TISSUE; IMMUNOPRECIPITATION; IN VITRO STUDY; INHIBITION KINETICS; MICROTUBULE; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; TAUOPATHY;

ALZHEIMER DISEASE; AMINO ACID MOTIFS; ANIMALS; CATTLE; CELL LINE; MICROTUBULE-ASSOCIATED PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PEPTIDES; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN PHOSPHATASE 2; PROTO-ONCOGENE PROTEINS C-FYN; SIGNAL TRANSDUCTION; TAU PROTEINS;

BOVINAE;

EID: 84860354271     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.338681     Document Type: Article

References (52)

1. Dehmelt, L., and Halpain, S. (2005) The MAP2/Tau family of microtubule-associated proteins. Genome Biol. 6, 204
2. Farah, C. A., and Leclerc, N. (2008) HMWMAP2: new perspectives on a pathway to dendritic identity. Cell Motil. Cytoskeleton 65, 515-527 (Pubitemid 351956380)
3. Lee, G., Newman, S. T., Gard, D. L., Band, H., and Panchamoorthy, G. (1998) Tau interacts with src-family non-receptor tyrosine kinases. J. Cell Sci. 111, 3167-3177 (Pubitemid 28532427)
4. Zamora-Leon, S. P., Lee, G., Davies, P., and Shafit-Zagardo, B. (2001) Binding of Fyn to MAP-2c through an SH3 binding domain. Regulation of the interaction by ERK2. J. Biol. Chem. 276, 39950-39958
5. Reynolds, C. H., Garwood, C. J., Wray, S., Price, C., Kellie, S., Perera, T., Zvelebil, M., Yang, A., Sheppard, P. W., Varndell, I. M., Hanger, D. P., and Anderton, B. H. (2008) Phosphorylation regulates tau interactions with Src homology 3 domains of phosphatidylinositol 3-kinase, phospholipase Cγ1, Grb2, and Src family kinases. J. Biol. Chem. 283, 18177-18186
6. Götz, J., Ittner, L. M., and Kins, S. (2006) Do axonal defects in tau and amyloid precursor protein transgenic animals model axonopathy in Alzheimer disease? J. Neurochem. 98, 993-1006 (Pubitemid 44127777)
7. Morris, M., Maeda, S., Vossel, K., and Mucke, L. (2011) The many faces of tau. Neuron 70, 410-426
8. Lee, G., Thangavel, R., Sharma, V. M., Litersky, J. M., Bhaskar, K., Fang, S. M., Do, L. H., Andreadis, A., Van Hoesen, G., and Ksiezak-Reding, H. (2004) Phosphorylation of tau by fyn: implications for Alzheimer disease. J. Neurosci. 24, 2304-2312 (Pubitemid 38314562)
9. Bhaskar, K., Yen, S. H., and Lee, G. (2005) Disease-related modifications in tau affect the interaction between Fyn and Tau. J. Biol. Chem. 280, 35119-35125 (Pubitemid 41532698)
10. Ittner, A., Ke, Y. D., Eersel, J., Gladbach, A., Götz, J., and Ittner, L. M. (2011) Brief update on different roles of tau in neurodegeneration. IUBMB. Life 63, 495-502
11. Iqbal, K., Liu, F., Gong, C. X., and Grundke-Iqbal, I. (2010) Tau in Alzheimer disease and related tauopathies. Curr. Alzheimer Res. 7, 656-664
12. Sánchez, C., Díaz-Nido, J., and Avila, J. (2000) Phosphorylation of microtubule- associated protein 2 (MAP2) and its relevance for the regulation of the neuronal cytoskeleton function. Prog. Neurobiol. 61, 133-168 (Pubitemid 30110476)
13. Ballatore, C., Lee, V. M., and Trojanowski, J. Q. (2007) Tau-mediated neurodegeneration in Alzheimer disease and related disorders. Nat. Rev. Neurosci. 8, 663-672 (Pubitemid 47283144)
14. Iqbal, K., Alonso Adel, C., and Grundke-Iqbal, I. (2008) Cytosolic abnormally hyperphosphorylated tau but not paired helical filaments sequester normal MAPs and inhibit microtubule assembly. J. Alzheimers. Dis. 14, 365-370
15. 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 (Pubitemid 41579384)
16. Virshup, D. M., and Shenolikar, S. (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol. Cell 33, 537-545
17. Sontag, E., Nunbhakdi-Craig, V., Lee, G., Bloom, G. S., and Mumby, M. C. (1996) Regulation of the phosphorylation state and microtubule-binding activity of Tau by protein phosphatase 2A. Neuron 17, 1201-1207 (Pubitemid 27021104)
18. Sontag, E., Nunbhakdi-Craig, V., Lee, G., Brandt, R., Kamibayashi, C., Kuret, J., White, C. L., 3rd, Mumby, M. C., and Bloom, G. S. (1999) Molecular interactions among protein phosphatase 2A, tau, and microtubules. Implications for the regulation of tau phosphorylation and the development of tauopathies. J. Biol. Chem. 274, 25490-25498
19. Xu, Y., Chen, Y., Zhang, P., Jeffrey, P. D., and Shi, Y. (2008) Structure of a protein phosphatase 2A holoenzyme: insights into B55-mediated Tau dephosphorylation. Mol. Cell 31, 873-885
20. Sontag, E., Nunbhakdi-Craig, V., Bloom, G. S., and Mumby, M. C. (1995) A novel pool of protein phosphatase 2A is associated with microtubules and is regulated during the cell cycle. J. Cell Biol. 128, 1131-1144
21. Hiraga, A., and Tamura, S. (2000) Protein phosphatase 2A is associated in an inactive state with microtubules through 2A1-specific interaction with tubulin. Biochem. J. 346, 433-439 (Pubitemid 30148130)
22. Nunbhakdi-Craig, V., Schuechner, S., Sontag, J. M., Montgomery, L., Pallas, D. C., Juno, C., Mudrak, I., Ogris, E., and Sontag, E. (2007) Expression of protein phosphatase 2A mutants and silencing of the regulatory B αsubunit induce a selective loss of acetylated and detyrosinated microtubules. J. Neurochem. 101, 959-971 (Pubitemid 46683881)
23. Sontag, E., Luangpirom, A., Hladik, C., Mudrak, I., Ogris, E., Speciale, S., and White, C. L., 3rd (2004) Altered expression levels of the protein phosphatase 2A ABαC enzyme are associated with Alzheimer disease pathology. J. Neuropathol. Exp. Neurol. 63, 287-301 (Pubitemid 38429026)
24. Sánchez, C., Tompa, P., Szücs, K., Friedrich, P., and Avila, J. (1996) Phosphorylation and dephosphorylation in the proline-rich C-terminal domain of microtubule-associated protein 2. Eur. J. Biochem. 241, 765-771 (Pubitemid 26379378)
25. Alexa, A., Schmidt, G., Tompa, P., Ogueta, S., Vázquez, J., Kulcsár, P., Kovács, J., Dombrádi, V., and Friedrich, P. (2002) The phosphorylation state of threonine-220, a uniquely phosphatase-sensitive protein kinase A site in microtubule-associated protein MAP2c, regulates microtubule binding and stability. Biochemistry 41, 12427-12435
26. Sánchez, M. C., Díaz-Nido, J., and Avila, J. (1998) Regulation of a site-specific phosphorylation of the microtubule-associated protein 2 during the development of cultured neurons. Neuroscience 87, 861-870 (Pubitemid 28400357)
27. Fan, Q. W., Yu, W., Gong, J. S., Zou, K., Sawamura, N., Senda, T., Yanagisawa, K., and Michikawa, M. (2002) Cholesterol-dependent modulation of dendrite outgrowth and microtubule stability in cultured neurons. J. Neurochem. 80, 178-190 (Pubitemid 34614590)
28. Gong, C. X., Wegiel, J., Lidsky, T., Zuck, L., Avila, J., Wisniewski, H. M., Grundke-Iqbal, I., and Iqbal, K. (2000) Regulation of phosphorylation of neuronal microtubule-associated proteins MAP1b and MAP2 by protein phosphatase-2A and -2B in rat brain. Brain Res. 853, 299-309 (Pubitemid 30035229)
29. Goedert, M., Satumtira, S., Jakes, R., Smith, M. J., Kamibayashi, C., White, C. L., 3rd, and Sontag, E. (2000) Reduced binding of protein phosphatase 2A to tau protein with frontotemporal dementia and parkinsonism linked to chromosome 17 mutations. J. Neurochem. 75, 2155-2162
30. Lim, R. W., and Halpain, S. (2000) Regulated association of microtubule-associated protein 2 (MAP2) with Src and Grb2: evidence for MAP2 as a scaffolding protein. J. Biol. Chem. 275, 20578-20587 (Pubitemid 30457642)
31. Roger, B., Al-Bassam, J., Dehmelt, L., Milligan, R. A., and Halpain, S. (2004) MAP2c, but not tau, binds and bundles F-actin via its microtubule binding domain. Curr. Biol. 14, 363-371 (Pubitemid 38431169)
32. Kim, H., Binder, L. I., and Rosenbaum, J. L. (1979) The periodic association of MAP2 with brain microtubules in vitro. J. Cell Biol. 80, 266-276 (Pubitemid 9091503)
33. Joly, J. C., Flynn, G., and Purich, D. L. (1989) The microtubule-binding fragment of microtubule-associated protein-2: location of the protease-accessible site and identification of an assembly-promoting peptide. J. Cell Biol. 109, 2289-2294 (Pubitemid 19282616)
34. Vallee, R. B. (1982) A taxol-dependent procedure for the isolation of microtubules and microtubule-associated proteins (MAPs). J. Cell Biol. 92, 435-442
35. Mumby, M. C., Russell, K. L., Garrard, L. J., and Green, D. D. (1987) Cardiac contractile protein phosphatases. Purification of two enzyme forms and their characterization with subunit-specific antibodies. J. Biol. Chem. 262, 6257-6265
36. Eidenmüller, J., Fath, T., Hellwig, A., Reed, J., Sontag, E., and Brandt, R. (2000) Structural and functional implications of tau hyperphosphorylation: information from phosphorylation-mimicking mutated tau proteins. Biochemistry 39, 13166-13175
37. Nunbhakdi-Craig, V., Machleidt, T., Ogris, E., Bellotto, D., White, C. L., 3rd, and Sontag, E. (2002) Protein phosphatase 2A associates with and regulates atypical PKC and the epithelial tight junction complex. J. Cell Biol. 158, 967-978 (Pubitemid 35001086)
38. Sontag, J. M., Nunbhakdi-Craig, V., Montgomery, L., Arning, E., Bottiglieri, T., and Sontag, E. (2008) Folate deficiency induces in vitro and mouse brain region-specific down-regulation of leucine carboxyl methyl-transferase- 1 and protein phosphatase 2A B(α) subunit expression that correlate with enhanced tau phosphorylation. J. Neurosci. 28, 11477-11487
39. Sontag, E., Hladik, C., Montgomery, L., Luangpirom, A., Mudrak, I., Ogris, E., and White, C. L., 3rd (2004) Down-regulation of protein phosphatase 2A carboxyl methylation and methyltransferase may contribute to Alzheimer disease pathogenesis. J. Neuropathol. Exp. Neurol. 63, 1080-1091
40. Sontag, J. M., Nunbhakdi-Craig, V., Mitterhuber, M., Ogris, E., and Sontag, E. (2010) Regulation of protein phosphatase 2A methylation by LCMT1 and PME-1 plays a critical role in differentiation of neuroblastoma cells. J. Neurochem. 115, 1455-1465
41. Honkanen, R. E., and Golden, T. (2002) Regulators of serine/threonine protein phosphatases at the dawn of a clinical era? Curr. Med. Chem. 9, 2055-2075 (Pubitemid 35256504)
42. de Ancos, J. G., and Avila, J. (1993) Differential distribution in white and grey matter of tau phosphoisoforms containing four tubulin-binding motifs. Biochem. J. 296, 351-354
43. Binder, L. I., Frankfurter, A., and Rebhun, L. I. (1985) The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378 (Pubitemid 16203754)
44. Ogris, E., Gibson, D. M., and Pallas, D. C. (1997) Protein phosphatase 2A subunit assembly: the catalytic subunit carboxy terminus is important for binding cellular B subunit but not polyomavirus middle tumor antigen. Oncogene 15, 911-917 (Pubitemid 27399552)
45. Surridge, C. D., and Burns, R. G. (1994) The difference in the binding of phosphatidylinositol distinguishes MAP2 from MAP2C and Tau. Biochemistry 33, 8051-8057 (Pubitemid 24223826)
46. Goedert, M., and Spillantini, M. G. (2006) A century of Alzheimer disease. Science 314, 777-781
47. Turowski, P., Favre, B., Campbell, K. S., Lamb, N. J., and Hemmings, B. A. (1997) Modulation of the enzymatic properties of protein phosphatase 2A catalytic subunit by the recombinant 65-kDa regulatory subunit PR65α. Eur. J. Biochem. 248, 200-208 (Pubitemid 27356989)
48. Evans, B. J., Wang, Z., Mobley, L., Khosravi, D., Fujii, N., Navenot, J. M., and Peiper, S. C. (2008) Physical association of GPR54 C-terminal with protein phosphatase 2A. Biochem. Biophys. Res. Commun. 377, 1067-1071
49. Eidenmüller, J., Fath, T., Maas, T., Pool, M., Sontag, E., and Brandt, R. (2001) Phosphorylation-mimicking glutamate clusters in the proline-rich region are sufficient to simulate the functional deficiencies of hyperphosphorylated tau protein. Biochem. J. 357, 759-767 (Pubitemid 32735156)
50. Landrieu, I., Smet-Nocca, C., Amniai, L., Louis, J. V., Wieruszeski, J. M., Goris, J., Janssens, V., and Lippens, G. (2011) Molecular implication of PP2A and Pin1 in the Alzheimer disease specific hyperphosphorylation of Tau. PLoS. ONE. 6, e21521
51. Goedert, M., Jakes, R., Qi, Z., Wang, J. H., and Cohen, P. (1995) Protein phosphatase 2A is the major enzyme in brain that dephosphorylates tau protein phosphorylated by proline-directed protein kinases or cyclic AMP-dependent protein kinase. J. Neurochem. 65, 2804-2807
52. Arendt, T. (2001) Alzheimer disease as a disorder of mechanisms underlying structural brain self-organization. Neuroscience 102, 723-765