Implication of cyclin-dependent kinases and glycogen synthase kinase 3 in the phosphorylation of microtubule-associated protein 1B in developing neuronal cells

Journal of Neuroscience Research

Volumn 52, Issue 4, 1998, Pages 445-452

  García Pérez, Julia ^a,b   Avila, Jesús ^a   Díaz Nido, Javier ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b Centra Ing Genet y Biotecnologia   (Cuba)

Author keywords

Alzheimer's disease; Axonal growth; Cytoskeleton; Lithium

Indexed keywords

CYCLIN DEPENDENT KINASE; MICROTUBULE ASSOCIATED PROTEIN 1; PROTEIN KINASE;

ALZHEIMER DISEASE; ARTICLE; CANCER CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMAN; HUMAN CELL; NERVE CELL CULTURE; NEUROBLASTOMA CELL; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELLS, CULTURED; CEREBELLUM; CYCLIN-DEPENDENT KINASES; GLYCOGEN SYNTHASE KINASE 3; GLYCOGEN SYNTHASE KINASES; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; NEUROBLASTOMA; NEURONS; PHOSPHORYLATION; PROLINE; RATS; TUMOR CELLS, CULTURED;

EID: 1642440160     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19980515)52:4<445::AID-JNR8>3.0.CO;2-9     Document Type: Article

References (52)

1. Avila J, Domínguez J, Díaz-Nido J (1994): Regulation of microtubule dynamics by microtubule-associated protein expression and phosphorylation during neuronal development. Int J Dev Biol 38:13-25.
2. Baas PW, Slaughter T, Brown A, Black MM (1991): Microtubule dynamics in axons and dendrites. J Neurosci Res 30:134-153.
3. Belmont LD, Hyman AA, Sawin KE, Mitchison TJ (1990): Real-time visualization of cell cycle-dependent changes in microtubule dynamics in cytoplasmic extracts. Cell 62:579-589.
4. Benson DL, Mandell JW, Shaw G, Banker G (1996): Compartmentation of alpha-internexin and neurofilament triplet proteins in cultured hippocampal neurons. J Neurocytol 25:181-196.
5. Biedler JL, Roffler-Tarlov S, Schachner M, Freedman LS (1978): Multiple neurotransmitter synthesis by human neuroblastoma cell lines and clones. Cancer Res 38:3751-3757.
6. Bush MS, Tonge DA, Woolf C, Gordon-Weeks PR (1996): Expression of a developmentally regulated, phosphorylated isoform of microtubule-associated protein 1B in regenerating axons of the sciatic nerve. Neuroscience 73:553-563.
7. Challacombe JF, Snow DM, Letourneau PC (1997): Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J Neurosci 17:3085-3095.
8. Davis PK, Dudek SM, Johnson GVW (1997): Select alterations in protein kinases and phosphatases during apoptosis of differentiated PC12 cells. J Neurochem 68:2338-2347.
9. Díaz-Nido J, Serrano L, Méndez E, Avila J (1988): A casein kinase II-related activity is involved in phosphorylation of microtubule-associated protein MAP1B during neuroblastoma cell differentiation. J Cell Biol 106:2057-2065.
10. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR (1995): A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci USA 92:7686-7689.
11. Edelmann W, Zervas M, Costello P, Robaek L, Fischer I, Hamumarback JA, Cowan N, Davies P, Wainer B, Kucherlapati R (1996): Neuronal abnormalities in microtubule-associated protein 1B mutant mice. Proc Natl Acad Sci USA 93:1270-1275.
12. Fischer I, Romano-Clarke G (1990): Changes in microtubule-associated protein MAP1B phosphorylation during rat brain development. J Neurochem 55:328-333.
13. Gordon-Weeks PR, Mansfield SG, Alberto C, Johnstone M, Moya F (1993): A phosphorylation epitope on MAP1B that is transiently expressed in growing axons in the developing rat nervous system. Eur J Neurosci 5:1302-1311.
14. Grundke-Iqbal I, Iqbal K, Tung Y-C, Quinlan M, Wisniewski HM, Binder LI (1986): Abnormal phosphorylation of the microtubule-associated protein Tau in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83:4913-4917.
15. Grunsven LA, Billon, N, Savatier P, Thomas A, Urdiales JL, Rudkin BB (1996): Effect of nerve growth factor on the expression of cell cycle regulatory proteins in PC12 cells: Dissection of the neurotrophic response from the anti-mitogenic response. Oncogene 12:1347-1356.
16. Hasegawa M, Arai T, Ihara Y (1990): Immunochemical evidence that fragments of phosphorylated MAP5 (MAP1B) are bound to neurofibrillary tangles in Alzheimer's disease. Neuron 4:909-918.
17. Kallunki T, Su B, Tsigelny I, Sluss HK, Derijard B, Moore, G, Davis R, Karin M (1994): JNK2 contains a specificity-determining region responsible for efficient C-Jun binding and phosphorylation. Genes Dev 8:2996-3007.
18. Klein PS, Melton DA (1996): A molecular mechanism for the effect of lithium on development. Proc Natl Acad Sci USA 93:8455-8459.
19. Kondratick CM, Vandré DD (1997): Alzheimer's disease neurofibrillary tangles contain mitosis-specific phosphoepitopes. J Neurochem 67:2405-2416.
20. Kranenburg O, Scharnhorst V, Van del Eb AJ, Zantema A (1995): Inhibition of cyclin-dependent kinase activity triggers neuronal differentiation of mouse neuroblastoma cells. J Cell Biol 131:227-234.
21. Ledesma MD, Correas I, Avila J, Díaz-Nido J (1992): Implication of brain cdc2 and MAP kinases in the phosphorylation of Tau protein in Alzheimer's disease. FEBS Lett 308:218-224.
22. Levi G, Aloisi F, Ciotti MT, Gallo V (1984): Autoradiographic localization and depolarization-induced release of acidic amino acids in differentiating granule cell culture. Brain Res 290:77-86.
23. Levi G, Aloisi F, Ciotti MT, Thangnipon W, Kingsbury A, Balazs R (1989): Preparation of 98% pure cerebellar granule cell cultures. In Shahar A, de Vellis J, Vernadakis A, Haber B (eds): "A Dissection and Tissue culture Manual of the Nervous System." New York: Alan R. Liss, pp 211-214.
24. Lovestone S, Reynolds CH (1997): The phosphorylation of Tau: A critical stage in neurodevelopment and neurodegenerative processes. Neuroscience 78:309-324.
25. Mansfield SG, Díaz Nido J, Gordon-Weeks PR, Avila J (1992): The distribution and phosphorylation of MAP1B in growth cones. J Neurocytol 21:1007-1022.
26. Meijer L, Borgne A, Mulner O, Chong JPJ, Blow JJ, Inagaki N, Inagaki M, Delcros J-G, Moulinoux J-P (1997): Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243:527-536.
27. Muñoz-Montaño JR, Moreno FJ, Avila J, Díaz-Nido J (1997): Lithium inhibits Alzheimer's disease-like Tau protein phosphorylation in neurons. FEBS Lett 411:183-188.
28. Pang L, Sawada T, Decker SJ, Saltiel AR (1995): Inhibition of MAP kinase blocks the differentiation of PC 12 cells induced by Nerve Growth Factor. J Biol Chem 270:13585-13588.
29. Park DS, Farinelli SE, Greene LA (1996): Inhibitors of cyclin-dependent kinases promote survival of post-mitotic neuronally differentiated PC12 cells and sympathetic neurons. J Biol Chem 271:8161-8169.
30. Pei J-J, Tanaka T, Tung Y-C, Braak E, Iqbal K, Grundke-Iqbal I (1997): Distribution, levels and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J Neuropathol Exp Neurol 56:70-78.
31. Pigino G, Paglini G, Ulloa L, Avila J, Caceres A (1997): Analysis of the expression, distribution and function of cyclin dependent kinase (cdk5) in developing cerebellar macroneurons. J Cell Sci 110:257-270.
32. Poluha W, Poluha DK, Chang B, Crosbie NE, Schonhoff CM, Kilpatrick DL, Ross AH (1996): The cyclin-dependent kinase inhibitor p21 WAF1 is required for survival of differentiating neuroblastoma cells. Mol Cell Biol 16:1335-1341.
33. Ramón-Cueto A, Avila J (1997): Differential expression of microtubule-associated protein 1B phosphorylated isoforms in the adult rat nervous system. Neuroscience 77:485-501.
34. Riederer BM, Moya F, Calvert R (1993): Phoshorylated MAP1B, alias MAP5 and MAP1X, is involved in axonal growth and neuronal mitosis. Neuroreport 4:771-774.
35. Shiurba RA, Ishiguro K, Takahashi M, Sato K, Spooner ET, Mercken M, Yoshida R, Wheelock TR, Yanagawa H, Imahori K, Nixon RA (1996): Immunocytochemistry of tau phosphoserine 413 and tau protein kinase I in Alzheimer pathology. Brain Res 737:119-132.
36. Stambolic V, Ruel L, Woodgett JR (1996): Lithium inhibits glycogen synthase kinase-3 activity and mimics Wingless signalling in intact cells. Curr Biol 6:1664-1668.
37. Sternberger LA, Sternberger NH (1983): Monoclonal antibodies distinguish phosphorylated and nonphosphorylated forms of neurofilaments in situ. Proc Natl Acad Sci USA 80:6126-6130.
38. Su JH, Anderson AJ, Cummings BJ, Cotman CW (1994): Immunohistochemical evidence for apoptosis in Alzheimer's disease. Neuroreport 5:2529-2533.
39. Takahashi M, Tomizawa K, Sato K, Uchida T, Fujita SC, Imahori K (1994): Localization and developmental changes of Tau protein kinase I/glycogen synthase kinase-3b in rat brain. J Neurochem 63:245-255.
40. Tanaka EM, Ho T, Kirschner MW (1995): The role of microtubule dynamics in growth cone motility and axonal growth. J Cell Biol 128:139-155.
41. Tombes RM, Peloquin JG, Borisy GG (1991): Specific association of an M-phase kinase with isolated mitotic spindles and identification of two of its substrates as MAP4 and MAP1B. Cell Regul 2:861-874.
42. Tsai L, Takahashi T, Caviness V, Harlow E (1993): Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development 119:1029-1040.
43. Tucker RP, Binder LI, Matus AI (1988): Neuronal microtubule-associated proteins in the embryonic avian spinal cord. J Comp Neurol 271:44-55.
44. Tucker RP, Garner CG, Matus AI (1989): In situ localization of microtubule-associated protein mRNA in the developing and adult rat brain. Neuron 2:1245-1246.
45. Ulloa L, Avila J, Díaz-Nido J (1993a): Heterogeneity in the phosphorylation of microtubule-associated protein MAP1B during rat brain development. J Neurochem 61:961-972.
46. Ulloa L, Díaz-Nido J, Avila J (1993b): Depletion of casein kinase II by antisense oligonucleotide prevents neuritogenesis in neuroblastoma cells. EMBOJ 12:1633-1640.
47. Ulloa L, Díez-Guerra J, Avila J, Díaz-Nido J (1994a): Localization of differentially phosphorylated isoforms of microtubule associated protein 1B (MAP1B) into axons and dendrites of cultured rat hippocampal neurons. Neuroscience 61:211-223.
48. Ulloa L, Montejo E, Gómez-Ramos P, Morán MA, Avila J (1994b): Microtubule-associated protein MAP1B showing a fetal phosphorylation pattern is present in sites of neurofibrillary degeneration in brain of Alzheimer's disease patients. Mol Brain Res 26:113-122.
49. Vesely J, Haulicek L, Strnad M, Blow JJ, Donella-Deana A, Pinna L, Letham DS, Kato J-Y, Detivaud L, Leclerc S, Meijer L (1994): Inhibition of cyclin-dependent kinases by purine analogues. Eur J Biochem 224:771-786.
50. Vincent I, Rosado M, Davies P (1996): Mitotic mechanisms in Alzheimer's disease. J Cell Biol 132:413-425.
51. Vincent I, Jicha G, Rosado M, Dickson DW (1997): Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J Neurosci 17:3588-3598.
52. Yan G-Z, Ziff EB (1995): NGF regulates the PC 12 cell cycle machinery through specific inhbition of the CDK kinases. J Neurosci 15:6200-6212.