Protein kinase MARK/PAR-1 is required for neurite outgrowth and establishment of neuronal polarity

Molecular Biology of the Cell

Volumn 13, Issue 11, 2002, Pages 4013-4028

  Biernat, Jacek ^a   Wu, Yong Zhong ^a   Timm, Thomas ^a   Zheng Fischhöfer, Qingyi ^a   Mandelkow, Eckhard ^a   Meijer, Laurent ^b   Mandelkow, Eva Maria ^a  

^a MAX PLANCK UNIT FOR STRUCTURAL MOLECULAR BIOLOGY   (Germany)

^b STATION BIOLOGIQUE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME INHIBITOR; HYMENIALDISINE; MARK2 INHIBITOR; MICROTUBULE AFFINITY REGULATING KINASE; PROTEIN KIN1; PROTEIN KINASE; PROTEIN MARK2; PROTEINASE ACTIVATED RECEPTOR 1; TAU PROTEIN; UNCLASSIFIED DRUG; AZEPINE DERIVATIVE; FLAVONOID; FLAVOPIRIDOL; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASE 3 BETA; HYBRID PROTEIN; MARK2 PROTEIN, RAT; PIPERIDINE DERIVATIVE; PROTEIN SERINE THREONINE KINASE; PYRROLE DERIVATIVE;

ALZHEIMER DISEASE; ARTICLE; BRAIN TISSUE; CELL DIFFERENTIATION; CELL POLARITY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME STRUCTURE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MEMBRANE BINDING; MEMBRANE STABILIZATION; MICROTUBULE ASSEMBLY; NERVE CELL PLASTICITY; NERVE FIBER GROWTH; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECT; GENETICS; METABOLISM; MOUSE; NERVE CELL; NEURITE; PHYSIOLOGY; SIGNAL TRANSDUCTION;

AMINO ACID MOTIFS; ANIMALS; AZEPINES; CELL LINE; CELL POLARITY; ENZYME INHIBITORS; FLAVONOIDS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; MICE; NEURITES; NEURONS; PIPERIDINES; PROTEIN-SERINE-THREONINE KINASES; PYRROLES; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TAU PROTEINS;

EID: 0036854327     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.02-03-0046     Document Type: Article

References (91)

1. Ackmann, M., Wiech, H., and Mandelkow, E. (2000). Non-saturable binding indicates clustering of tau on the microtubule surface in a paired helical filament-like conformation. J. Biol. Chem. 275, 30335-30343.
2. Baas, P., and Ahmad, F. (1993). The transport properties of axonal microtubules establish their polarity orientation. J. Cell Biol. 111, 495-509.
3. Baas, P.W., Pienkowski, T.P., and Kosik, K.S. (1991). Processes induced by tau expression in Sf9-cells have an axon-like microtubule organization. J. Cell Biol. 115, 1333-1344.
4. Barlow, S., Gonzalez-Garay, M.L., West, R., Olmsted, J.B., and Cabral, F. (1994). Stable expression of heterologous microtubule-associated proteins (MAPs) in Chinese hamster ovary cells: Evidence for differing roles of MAPs in microtubule organization. J. Cell Biol. 126, 1017-1029.
5. Biernat, J., Gustke, N., Drewes, G., Mandelkow, E.-M., and Mandelkow, E. (1993). Phosphorylation of serine 262 strongly reduces the binding of tau protein to microtubules: Distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11, 153-163.
6. Biernat, J., and Mandelkow, E.-M. (1999). The development of cell processes induced by tau protein requires phosphorylation of serine 262 and 356 in the repeat domain and is inhibited by phosphorylation in the proline-rich domains. Mol. Biol. Cell 10, 727-740.
7. Binder, L.I., Frankfurter, A., and Rebhun, L. (1985). The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101, 1371-1378.
8. Black, M.M., Slaughter, T., Moshiach, S., Obrocka, M., and Fischer, I. (1996). Tau is enriched on dynamic microtubules in the distal region of growing axons. J. Neurosci. 16, 3601-3619.
9. Böhm, H., Brinkmann, V., Drab, M., Henske, A., and Kurzchalia, T.V. (1997). Mammalian homologues of C. elegans PAR-1 are asymmetrically localized in epithelial cells and may influence their polarity. Curr. Biol. 7, 603-606.
10. Borisy, G.G., and Svitkina, T.M. (2000). Actin machinery: Pushing the envelope. Curr. Opin. Cell Biol. 12, 104-112.
11. Boyle, W.J., van der Geer, P., and Hunter, T. (1991). Phosphopeptide mapping and phosphoamino acid analysis by two-dimensional separation on thin layer cellulose plates. Methods Enzymol. 201, 110-149.
12. Bradke, F., and Dotti, C.G. (1999). The role of local actin instability in axon formation. Science 283, 1931-1934.
13. Bradke, F., and Dotti, C.G. (2000). Establishment of neuronal polarity: Lessons from cultured hippocampal neurons. Curr. Opin. Neurobiol. 10, 574-581.
14. Brandt, R., Leger, J., and Lee, G. (1995). Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. J. Cell Biol. 131, 1327-1340.
15. Brown, A.J., Hutchings, C., Burke, J.F., and Mayne, L.V. (1999). Application of a rapid method (targeted display) for the identification of differentially expressed mRNAs following NGF-induced neuronal differentiation in PC12 cells. Mol. Cell. Neurosci. 13, 119-130.
16. Butner, K.A., and Kirschner, M.W. (1991). Tau-protein binds to microtubules through a flexible array of distributed weak sites. J. Cell Biol. 115, 717-730.
17. Caceres, A., and Kosik, K.S. (1990). Inhibition of neurite polarity by tau antisense oligonucleotide in primary cerebellar neurons. Nature 343, 461-463.
18. Chijiwa, T., Mishima, A., Hagiwara, M., Sano, M., Hayashi, K., Inoue, T., Naito, K., Toshioka, T., and Hidaka, H. (1990). Inhibition of forskolin-induced neurite outgrowth and protein phosphorylation by a newly synthesized selective inhibitor of cyclic AMP-dependent protein kinase, N-[2-(p-bromocinnamylamino)ethyl]-5-isoquinolinesulfonamide (H-89), of PC12D pheochromocytoma cells. J. Biol. Chem. 265, 5267-5272.
19. 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.
20. Cunningham, C., Leclerc, N., Flanagan, L., Lu, M., Janmey, P., and Kosik, K. (1997). Microtubule-associated protein 2c reorganizes both microtubules and microfilaments into distinct cytological structures in an actin-binding protein-280-deficient melanoma cell line. J. Cell Biol. 136, 845-857.
21. Dan, C., Nath, N., Liberto, M., and Minden, A. (2002). PAK5, a brain-specific kinase, promotes neurite outgrowth in N1E-115 cells. Mol. Cell. Biol. 22, 567-577.
22. Daub, H., Gevaert, K., Vandekerckhove, J., Sobel, A., and Hall, A. (2001). Rac/cdc42 and p65PAK regulated the microtubule-destablizing protein stathmin through phosphorylation at serine 16. J. Biol. Chem. 276, 1677-1680.
23. Delacourte, A., and Buee, L. (2000). Tau pathology: A marker of neurodegenerative disorders. Curr. Opin. Neurol. 13, 371-376.
24. DiTella, M.C., Feiguin, F., Carri, N., Kosik, K.S., and Caceres, A. (1996). MAP-1B/TAU functional redundancy during laminin-enhanced axonal growth. J. Cell Sci. 109, 467-477.
25. DiTella, M., Feiguin, F., Morfini, G., and Caceres, A. (1994). Microfilament-associated growth cone component depends upon Tau for its intracellular localization. Cell Motil. Cytoskeleton 29, 117-130.
26. Drewes, G., Trinczek, B., Illenberger, S., Biernat, J., Schmitt-Ulms, G., Meyer, H.E., Mandelkow, E.-M., and Mandelkow, E. (1995). MAP/microtubule affinity regulating kinase (P110/mark): A novel protein kinase that regulates tau-microtubule interactions and dynamic instability by phosphorylation at the Alzheimer-specific site Serine 262. J. Biol. Chem. 270, 7679-7688.
27. Drewes, G., Ebneth, A., and Mandelkow, E.-M. (1998). MAPs, MARKs, and microtubule dynamics. Trends Biochem. Sci. 23, 307-311.
28. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E.-M., and Mandelkow, E. (1997). MARK: A novel family of protein kinases that phosphorylate microtubule-associated proteins and trigger microtubule disruption. Cell 89, 297-308.
29. Drubin, D., and Kirschner, M. (1986). Tau protein function in living cells. J. Cell Biol. 103, 2739-2746.
30. Ebneth, A., Drewes, G., Mandelkow, E.-M., and Mandelkow, E. (1999). Phosphorylation of MAP2c and MAP4 by MARK kinases leads to the destabilization of microtubules in cells. Cell Motil. Cytoskeleton 44, 209-224.
31. Ebneth, A., Godemann, R., Stamer, K., Illenberger, S., Trinczek, B., Mandelkow, E.-M., and Mandelkow, E. (1998). Overexpression of tau protein alters kinesin-dependent trafficking of vesicles, mitochondria, and endoplasmic reticulum: Implications for Alzheimer's disease. J. Cell Biol. 143, 777-794.
32. Edson, K., Weisshaar, B., and Matus, A. (1993). Actin depolymerization induces process formation on MAP2-transfected nonneuronal cells. Development 117, 689-700.
33. Esmaeli-Azad, B., Mccarty, J.H., and Feinstein, S.C. (1994). Sense and antisense transfection analysis of tau-function: Tau influences net microtubule assembly, neurite outgrowth and neuritic stability. J. Cell Sci. 107, 869-879.
34. Godemann, R., Biernat, J., Mandelkow, E., and Mandelkow, E.-M. (1999). Phosphorylation of tau protein by recombinant GSK-3β: Pronounced phosphorylation at select Ser/Thr-Pro motifs but no phosphorylation at Ser262 in the repeat domain. FEBS Lett. 454, 157-164.
35. Goedert, M., Spillantini, M., Jakes, R., Rutherford, D., and Crowther, R.A. (1989). Multiple isoforms of human microtubule-associated protein-tau: Sequences and localization in neurofibrillary tangles of Alzheimers-disease. Neuron 3, 519-526.
36. Goode, B.L., Drubin, D.G., and Barnes, G. (2000). Functional cooperation between the microtubule and actin cytoskeletons. Curr. Opin. Cell Biol. 12, 63-71.
37. Griffith, L.M., and Pollard, T.M. (1982). The interaction of actin filaments with microtubules and microtubule-associated proteins. J. Biol. Chem. 257, 9143-9151.
38. Guo, S., and Kemphues, K.J. (1995). par-1, a gene required for establishing polarity in C. elegans embryos, encodes a putative Ser/Thr kinase that is asymmetrically distributed. Cell 81, 611-620.
39. Gustke, N., Trinczek, B., Biernat, J., Mandelkow, E.-M., and Mandelkow, E. (1994). Domains of tau protein and interactions with microtubules. Biochemistry 33, 9511-9522.
40. Hanks, S.K., and Hunter, T. (1995). Protein kinases 6. The eukaryotic protein kinase superfamily: Kinase catalytic domain structure and classification. FASEB J. 9, 576-596.
41. Harada, A., Oguchi, K., Okabe, S., Kuno, J., Terada, S., Ohshima, T., Sato-Yoshitake, R., Takei, Y., Noda, T., and Hirokawa, N. (1994). Altered microtubule organization in small-caliber axons of mice lacking tau protein. Nature 369, 488-491.
42. Hirokawa, N., Funakoshi, T., Satoharada, R., and Kanai, Y. (1996). Selective stabilization of tau in axons and microtubule-associated protein 2c in cell-bodies and dendrites contributes to polarized localization of cytoskeletal proteins in mature neurons. J. Cell Biol. 132, 667-679.
43. Illenberger, S., Drewes, G., Trinczek B., Biernat, J., Meyer, H.E., Olmsted, J.B., Mandelkow, E.-M., and Mandelkow, E. (1996). Phosphorylation of microtubule-associated proteins MAP2 and MAP4 by the protein kinase p110-MARK: Phosphorylation sites and regulation of microtubule dynamics. J. Biol. Chem. 271, 10834-10843.
44. Illenberger, S., Zheng-Fischhofer, Q., Preuss, U., Stamer, K., Baumann, K., Trinczek, B., Biernat, J., Godemann, R., Mandelkow, E.-M., and Mandelkow, E. (1998). The endogenous and cell-cycle dependent phosphorylation of tau protein in living cells: Implications for Alzheimer's disease. Mol. Biol. Cell, 9, 1495-1512.
45. Imahori, K., and Uchida, T. (1997). Physiology and pathology of tau protein kinases in relation to Alzheimer's disease. J. Biochem. 121, 179-188.
46. Jenkins, S.M., and Johnson, G.V.W. (1997). Phosphorylation of microtubule-associated protein tau on Ser 262 by an embryonic 100 kDa protein kinase. Brain Res. 767, 305-313.
47. Jordan, M.A., and Wilson, L. (1998). Use of drugs to study role of microtubule assembly dynamics in living cells. Methods Enzymol. 298, 252-76.
48. Kabir, N., Schaefer, A.W., Nakhost, A., Sossin, W.S., and Forscher, P. (2001). Protein kinase C activation promotes microtubule advance in neuronal growth cones by increasing average microtubule growth lifetimes. J. Cell Biol. 152, 1033-1044.
49. Kanai, Y., Takemura, R., Oshima, T., Mori, H., Ihara, Y., Yanagisawa, M., Masaki, T., and Hirokawa, N. (1989). Expression of multiple tau isoforms and microtubule bundle formation in fibroblasts transfected with a single tau cDNA. J. Cell Biol. 109, 1173-1184.
50. Kaverina, I., Rottner, K., and Small, J.V. (1998). Targeting, capture, and stabilization of microtubules in early focal adhesions. J. Cell Biol. 142, 181-190.
51. Kemphues, K. (2000). PARsing embryonic polarity. Cell 101, 345-348.
52. Knops, J., Kosik, K., Lee, G., Pardee, J., Cohen-Gould, L., and McConlogue, L. (1991). Overexpression of tau in a nonneuronal cell induces long cellular processes. J. Cell Biol. 114, 725-733.
53. Knowles, R., Leclerc, N., and Kosik, K.S. (1994). Organization of actin and microtubules during process formation in tau-expressing Sf9 cells. Cell Motil. Cytoskeleton 28, 256-264.
54. Leclerc, S., et al. (2001). Indirubins inhibit glycogen synthase kinase-3b and CDK5/p25, two protein kinases involved in abnormal tau phosphorylation in Alzheimer's disease: A property common to most CDK inhibitors? J. Biol. Chem. 276, 251-260.
55. Lee, V.M.Y., Balin, B.J., Otvos, L., and Trojanowski, J.Q. (1991). A68: A major subunit of paired helical filaments and derivatized forms of normal tau. Science 251, 675-678.
56. Lee, G., Cowan, N., and Kirschner, M. (1988). The primary structure and heterogeneity of tau protein from mouse brain. Science 239, 285-288.
57. 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.
58. Leger, J.G., Brandt, R., and Lee, G. (1994). Identification of tau protein regions required for process formation in PC12 cells. J. Cell Sci. 107, 3403-3412.
59. Levin, D.E., and Bishop, J.M. (1990). A putative protein-kinase gene (kinl+) is important for growth polarity in Schizosaccharomyces pombe. Proc. Natl. Acad. Sci. USA 87, 8272-8276.
60. Liao, H., Li, Y., Brautigan, D.L., and Gundersen, G.G. (1998). Protein phosphatase 1 is targeted to microtubules by the microtubule-associated protein tau. J. Biol. Chem. 273, 21901-21908.
61. Liao, G., Nagasaki, T., and Gundersen, G.G. (1995). Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: Implications for the role of dynamic microtubules in cell locomotion. J. Cell Sci. 108, 3473-3483.
62. Litersky, J.M., and Johnson, G.V.W. (1995). Phosphorylation of tau in-situ: Inhibition of calcium-dependent proteolysis. J. Neurochem. 65, 903-911.
63. Lopez, L.A., and Sheetz, M.P. (1995). A microtubule-associated protein (MAP2) kinase restores microtubule motility in embryonic brain. J. Biol. Chem. 270, 12511-12517.
64. Lucas, F., Goold, R., Gordon-Weeks, P., and Salinas, P. (1998). Inhibition of GSK-3β leading to the loss of phosphorylated MAP-1B is an early event in axonal remodelling induced by WNT-7a or lithium. J. Cell Sci. 111, 1351-1361.
65. Mandell, J.W., and Banker, G.A. (1996). A spatial gradient of tauprotein phosphorylation in nascent axons. J. Neurosci. 16, 5727-5740.
66. Mandelkow, E.-M., and Mandelkow, E. (1998). Tau in Alzheimer's disease. Trends Cell Biol. 8, 425-427.
67. Meijer, L., et al. (2000). Inhibition of cyclin-dependent kinases, G.S.K-3b and casein kinase I by hymenialdisine, a marine sponge constituent. Chem. Biol. 7, 51-63.
68. Moreno, F.J., Medina, M., Perez, M., Degarcini, E.M., 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.
69. Morishima-Kawashima, M., Hasegawa, M., Takio, K., Suzuki, M., Yoshida, H., Titani, K., and Ihara, Y. (1995). Proline-directed and non-proline-directed phosphorylation of PHF-tau. J. Biol. Chem. 270, 823-829.
70. Nelson, W.J., and Grindstaff, K.K. (1997). Cell polarity: Par for the polar course. Curr. Biol. 7, R562-R564.
71. Obar, R.A., Dingus, J., Bayley, H., and Vallee, R.B. (1989). The RII subunit of cAMP-dependent protein-kinase binds to a common amino-terminal domain in microtubule-associated proteins 2a, 2b, and 2c. Neuron 3, 639-645.
72. Ookata, K., Hisanaga, S., Sugita, M., Okuyama, A., Murofushi, H., Kitazawa, H., Chari, S., Bulinski, J.C., and Kishimoto, T. (1997). MAP4 is the in-vivo substrate for cdc2 kinase in HeLa cells: Identification of an M-phase specific and a cell cycle-independent phosphorylation site in MAP4. Biochemistry 36, 15873-15883.
73. Ozer, R., and Halpain, S. (2000). Phosphorylation-dependent localization of microtubule-associated protein MAP2c to the actin cytoskeleton. Mol. Biol. Cell 11, 3573-3587.
74. Palazzo, A., Cook, T., Alberts, A., and Gundersen, G.G. (2001). m-Dia mediates Rho-regulated formation, and orientation of stable microtubules. Nat. Cell Biol. 3, 723-729.
75. Panda, D., Miller, H.P., and Wilson, L. (1999). Rapid treadmilling of brain microtubules free of microtubule-associated proteins in vitro and its suppression by tau. Proc. Natl. Acad. Sci. USA 96, 12459-12464.
76. Rochlin, M.W., Wickline, K., and Bridgman, P. (1996). Microtubule stability decreases axon elongation but not axoplasm production. J. Neurosci. 16, 3236-3246.
77. Schneider, A., Biernat, J., von Bergen, M., Mandelkow, E., and Mandelkow, E.-M. (1999). Phosphorylation that detaches tau protein from microtubules (Ser262, Ser214) also protects it against aggregation into Alzheimer paired helical filaments. Biochemistry 38, 3549-3558.
78. Seubert, P., et al. (1995). Detection of phosphorylated Ser(262) in fetal tau, adult tau, and paired helical filament tau. J. Biol. Chem. 270, 18917-18922.
79. Shulman, J., Benton, R., and St. Johnston, D. (2000). The Drosophila homolog of C. elegans PAR-1 organizes the oocyte cytoskeleton and directs oskar mRNA localization to the posterior pole. Cell 101, 377-388.
80. Sontag, E., Nunbhakdi-Craig, V., Lee, G., Brandt, R., Kamibayashi, C., Kuret, J., White, C., Mumby, M., and Bloom, G. (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.
81. Stambolic, V., Ruel, L., and Woodgett, J.R. (1996). Lithium inhibits glycogen-synthase kinase-3 activity and mimics wingless signaling in intact cells. Curr. Biol. 6, 1664-1668.
82. Stamer, K., Vogel, R., Thies, E., Mandelkow, E., and Mandelkow, E.-M. (2002). Tau blocks traffic of organelles, neurofilaments, and APP-vesicles in neurons and enhances oxidative stress. J. Cell Biol. 156, 1051-1063.
83. Tanaka, E., Ho, T., and Kirschner, M.W. (1995). Microtubule behavior in the growth cones of living neurons during axon elongation. J. Cell Biol. 115, 345-363.
84. Tomancak, P., Piano, F., Riechmann, V., Gunsalus, K.C., Kemphues, K.J., and Ephrussi, A. (2000). A Drosophila melanogaster homologue of Caenorhabditis elegans par-1 acts at an early step in embryonic-axis formation. Nat. Cell Biol. 2, 458-460.
85. Takei, Y., Teng, J., Harada, A., and Hirokawa, N. (2000). Defects in axonal elongation and neuronal migration in mice with disrupted tau and MAPlb genes. J. Cell Biol. 150, 989-1000.
86. Ulloa, L., Montejo de Garcini, E., Gomez-Ramos, P., Moran, M.A., and Avila, J. (1994). Microtubule-associated protein MAPIB showing a fetal phosphorylation pattern is present in sites of neurofibrillary degeneration in brains of Alzheimer's disease patients. Brain Res. Mol. Brain Res. 26, 113-122.
87. Waterman-Storer, C.M., and Salmon, E.D. (1997). Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J. Cell Biol. 139, 417-434.
88. Waterman-Storer, C., and Salmon, E.D. (1999). Positive feedback interactions between microtubule and actin dynamics during cell motility. Curr. Opin. Cell Biol. 11, 61-67.
89. Watanabe, A., Hasegawa, M., Suzuki, M., Takio, K., Morishima-Kawashima, M., Titani, K., Arai, T., Kosik, K.S., and Ihara, Y. (1993). In vivo phosphorylation sites in fetal and adult rat tau. J. Biol. Chem. 268, 25712-25717.
90. Woodring, P.J., Litwack, E.D., O'Leary, D.D., Lucero, G.R., Wang, J.Y., and Hunter, T. (2002). Modulation of the F-actin cytoskeleton by c-Abl tyrosine kinase in cell spreading and neurite extension. J. Cell Biol. 156, 879-892.
91. Zheng-Fischhofer, Q., Biernat, J., Mandelkow, E.-M., Illenberger, S., Godemann, R., and Mandelkow, E. (1998). Sequential phosphorylation of tau-protein by GSK-3b and protein kinase A at Thr212 and Ser214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired helical filament-like conformation. Eur. J. Biochem. 252, 542-552.