Impairment of phosphatase 2A contributes to the prolonged MAP kinase phosphorylation in Alzheimer's disease fibroblasts

Neurobiology of Disease

Volumn 14, Issue 3, 2003, Pages 458-469

  Zhao, Wei Qin ^a   Feng, Christina ^a   Alkon, Daniel L ^a  

^a Blanchette Rockefeller Neurosci I   (United States)

Author keywords

Alzheimer's disease; FK506; Gene expression; Human skin fibroblasts; MAP kinase nuclear translocation; MAP kinase phosphorylation; Phosphatase 2A; Real time PCR

Indexed keywords

BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; OKADAIC ACID; PHOSPHATASE; PHOSPHATASE 2A; TACROLIMUS; UNCLASSIFIED DRUG;

ADULT; AGED; ALZHEIMER DISEASE; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVATION; ENZYME ACTIVITY; FIBROBLAST; HUMAN; HUMAN CELL; HYPOPHOSPHATASIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION;

EID: 0346848898     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-9961(03)00124-4     Document Type: Article

References (59)

1. Adachi M., Fukuda M., Nishida E. Two co-existing mechanisms for nuclear import of MAP kinase passive diffusion of a monomer and active transport of a dimmer . EMBO J. 18:1999;5347-5358.
2. Alessi D.R., Gomez N., Moorhead G., Lewis T., Keyse S.M., Cohen P. Inactivation of p42 MAP kinase by protein phosphatase 2A and a protein tyrosine phosphatase, but not CL100, in various cell lines. Curr. Biol. 5:1995;283-295.
3. Billingsley M.L., Kincaid R.L. Regulated phosphorylation and dephosphorylation of tau protein effects on microtubule interaction, intracellular trafficking and neurodegeneration . Biochem. J. 323:1997;577-591.
4. Braconi Quintaje S.B., Church D.J., Rebsamen M., Valloton M.B., Hemmings B.A., Lang U. Role of protein phosphatase 2A in the regulation of mitogen-activated protein kinase activity in ventricular cardiomyocytes. Biochem. Biophys. Res. Commun. 221:1996;539-547.
5. Brunet A., Roux D., Lenormand P., Dowd S., Keyse S., Pouyssegur J. Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 18:1999;664-674.
6. Connolly G.P. Fibroblast models of neurological disorders fluorescence measurement studies . Trends Pharmacol. Sci. 19:1998;171-177.
7. Chen R.H., Sarnecki C., Blenis J. Nuclear localization and regulation of Erk- and rsk encoded protein kinases. Mol. Cell. Biol. 12:1992;915-927.
8. Christner C., Herdegen T., Fischer G. FKBP ligands as novel therapeutics for neurological disorders. Mini-Rev. Med. Chem. 1:2001;377-397.
9. Chung H., Brautigan D.L. Protein phosphatase 2A suppresses MAP kinase signaling and ectopic protein expression. Cell Signal. 11:1999;575-580.
10. Cummings J.L., Vinters H.V., Cole G.M., Khachaturian Z.S. Alzheimer's disease etiologies, pathophysiology, cognitive reserve, and treatment opportunities . Neurology. 51:1998;S2-S17.
11. Dineley K.T., Westerman M., Bui D., Bell K., Ashe K.H., Sweatt J.D. Beta-amyloid activates the mitogen-activated protein kinase cascade via hippocampal alpha7 nicotinic acetylcholine receptors in vitro and in vivo mechanisms related to Alzheimer's disease . J. Neurosci. 21:2001;4125-4133.
12. Etcheberrigaray R., Hirashima N., Nee L., Prince J., Govoni S., Racchi M., Tanzi R.E., Alkon D.L. Calcium responses in fibroblasts from asymptomatic members of Alzheimer's disease families. Neurobiol. Dis. 5:1998;37-45.
13. Fernandez J.J., Candenas M.L., Souto M.L., Trujillo M.M., Norte M. Okadaic acid, useful tool for studying cellular processes. Curr. Med. Chem. 9:2002;229-262.
14. Ferrell J.E. Jr. How regulated protein translocation can produce switch-like responses. Trends Biochem. Sci. 23:1998;461-465.
15. Force T., Bonventre J.V. Growth factors and mitogen-activated protein kinases. Hypertension. 31:1998;152-161.
16. Goedert M., Spillantini M.G., Cairns N.J., Crowther R.A. Tau proteins of Alzheimer paired helical filaments abnormal phosphorylation of all six brain isoforms . Neuron. 8:1992;159-168.
17. Gold B.G. FK506 and the role of the immunophilin FKBP-52 in nerve regeneration. Drug Metab. Rev. 31:1999;649-663.
18. Gong C.X., Lidsky T., Wegiel J., Zuck L., Grundke-Iqbal I., Iqbal K. Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer's disease. J. Biol. Chem. 275:2000;5535-5544.
19. Gong C.X., Shaikh S., Wang J.Z., Zaidi T., Grundke-Iqbal I., Iqbal K. Phosphatase activity toward abnormally phosphorylated tau decrease in Alzheimer disease brain . J. Neurochem. 65:1995;732-738.
20. Gonzalez F.A., Seth A., Raden D.L., Bowman D.S., Fay F.S., Davis R.J. Serum-induced translocation of mitogen-activated protein kinase to the cell surface ruffling membrane and the nucleus. J. Cell Biol. 122:1993;1089-10101.
21. Guise S., Braguer D., Carles G., Delacourte A., Briand C. Hyperphosphorylation of tau is mediated by ERK activation during anticancer drug-induced apoptosis in neuroblastoma cells. J. Neurosci. Res. 63:2001;257-267.
22. Heid C.A., Stevens J., Livak K.J., Williams P.M. Real time quantitative PCR. Genome Res. 6:1996;986-994.
23. Janssens V., Goris J. Protein phosphatase 2A a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling . Biochem. J. 353:2001;417-439.
24. Janssens V., Jordens J., Stevens I., Van Hoof C., Martens E., De Smedt H., Engelborghs Y.m, Waelkens E., Goris J. Identification and functional analysis of two Ca2+-binding EF-hand motifs in the B″/PR72 subunit of protein phosphatase 2A. J. Biol. Chem. 278:2003;10697-10706.
25. Jellinger K.A., Bancher C. Neuropathology of Alzheimer's disease a critical update . J. Neural Transm. Suppl. 54:1998;77-95.
26. Khokhlatchev A.V., Canagarajah B., Wilsbacher J., Robinson M., Atkinson M., Goldsmith E., Cobb M.H. Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell. 93:1998;605-615.
27. Kins S., Crameri A., Evans D.R., Hemmings B.A., Nitsch R.M., Gotz J. Reduced protein phosphatase 2A activity induces hyperphosphorylation and altered compartmentalization of tau in transgenic mice. J. Biol. Chem. 276:2001;38193-38200.
28. Klettner A., Baumgrass R., Zhang Y., Fischer G., Burger E., Herdegen T., Mielke K. The neuroprotective actions of FK506 binding protein ligands neuronal survival is triggered by de novo RNA synthesis, but is independent of inhibition of JNK and calcineurin . Brain Res. Mol. Brain Res. 97:2001;21-31.
29. Knowles R.B., Chin J., Ruff C.T., Hyman B.T. Demonstration by fluorescence resonance energy transfer of a close association between activated MAP kinase and neurofibrillary tangles implications for MAP kinase activation in Alzheimer disease . J. Neuropathol. Exp. Neurol. 58:1999;1090-1098.
30. Lee V.M. Disruption of the cytoskeleton in Alzheimer's disease. Curr. Opin. Neurobiol. 5:1995;663-668.
31. Lenormand P., Sardet C., Pages G., L'Allemain G., Brunet A., Pouyssegur J. Growth factors induce nuclear translocation of MAP kinases (p42mapk and p44mapk) but not of their activator MAP kinase kinase (p45mapkk) in fibroblasts. J. Cell Biol. 122:1993;1079-1088.
32. Lewis T.S., Shapiro P.S., Ahn N.G. Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74:1998;49-139.
33. Liebmann C. Bradykinin signalling to MAP kinase cell specific connections versus principle mitogenic pathways . Biol. Chem. 382:2001;49-55.
34. T method. Methods. 25:2001;402-408.
35. Mandelkow E., Song Y.H., Schweers O., Marx A., Mandelkow E.M. On thestructure of microtubules, tau, and paired helical filaments. Neurobiol. Aging. 16:1995;347-354.
36. Matsubayashi Y., Fukuda M., Nishida E. Evidence for existence of a nuclear pore complex-mediated, cytosol-independent pathway of nuclear translocation of ERK MAP kinase in permeabilized cells. J. Biol. Chem. 276:2001;41755-41760.
37. Mattson M., Chan S.L., Camandola S. Presenilin mutations and calcium signaling defects in the nervous and immune systems. BioEssays. 23.8:2001;733-744.
38. McMahon K.A., Wilson N.J., Marks D.C., Beecroft T.L., Whitty G.A., Hamilton J.A., Csar X.F. Colony-stimulating factor-1 (CSF-1) receptor-mediated macrophage differentiation in myeloid cells a role for tyrosine 559-dependent protein phosphatase 2A (PP2A) activity . Biochem. J. 358:2001;431-436.
39. Nagao M., Shima H., Nakayasu M., Sugimura T. Protein serine/threonine phosphatases as binding proteins for okadaic acid. Mutat. Res. 333:1995;173-179.
40. Planel E., Yasutake K., Fujita S.C., Ishiguro K. Inhibition of protein phosphatase 2A overrides tau protein kinase I/glycogen synthase kinase 3β and cyclin-dependent kinase 5 inhibition and results in tau hyperphosphorylation in the hippocampus of starved mouse. J. Biol. Chem. 276:2001;34289-34306.
41. Putney J.W. Jr. Presenilins, Alzheimer's disease, and capacitative calcium entry. Neuron. 27:2000;411-412.
42. Rapoport M., Ferreira A. PD98059 prevents neurite degeneration induced by fibrillar beta-amyloid in mature hippocampal neurons. J. Neurochem. 74:2000;125-133.
43. Roovers K., Assoian R.K. Integrating the MAP kinase signal into the G1 phase cell cycle machinery. Bioessays. 22:2000;818-826.
44. Saito T., Ishiguro K., Uchida T., Miyamoto E., Kishimoto T., Hisanaga S. In situ dephosphorylation of tau by protein phosphatase 2A and 2B in fetal rat primary cultured neurons. FEBS Lett. 376:1995;238-242.
45. Sheehan J.P., Swerdlow R.H., Miller S.W., Davis R.E., Parks J.K., Parker W.D., Tuttle J.B. Calcium homeostasis and reactive oxygen species production in cells transformed by mitochondria from individuals with sporadic Alzheimer's disease. J. Neurosci. 17:1997;4612-4622.
46. Sheppeck J.E., Gauss C.M., Chamberlin A.R. Inhibition of the Ser-Thr phosphatases PP1 and PP2A by naturally occurring toxins. Bioorg. Med. Chem. 5:1997;1739-1750.
47. Silverstein A.M., Barrow C.A., Davis A.J., Mumby M.C. Actions of PP2A on the MAP kinase pathway and apoptosis are mediated by distinct regulatory subunits. Proc. Natl. Acad. Sci. USA. 99:2002;4221-4226.
48. Sweatt J.D. The neuronal MAP kinase cascade a biochemical signal integration system subserving synaptic plasticity and memory . J. Neurochem. 76:2001;1-10.
49. Treisman R. Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8:1996;205-215.
50. Valjent E., Caboche J., Vanhoutte P. Mitogen-activated protein kinase/extracellular signal-regulated kinase induced gene regulation in brain a molecular substrate for learning and memory . Mol. Neurobiol. 23:2001;83-99.
51. Vogelsberg-Ragaglia V., Schuck T., Trojanowski J.Q., Lee V.M. PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus. Exp. Neurol. 168:2001;402-412.
52. Volmat V., Camps M., Arkinstall S., Pouyssegur J., Lenormand P. The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAP kinases. J. Cell Sci. 114:2001;3433-3443.
53. Wang J.Z., Gong C.X., Zaidi T., Grundke-Iqbal I., Iqbal K. Dephosphorylation of Alzheimer paired helical filaments by protein phosphatase-2A and -2B. J. Biol. Chem. 270:1995;4854-4860.
54. Winer J., Jung C.K., Shackel I., Williams P.M. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal. Biochem. 270:1999;41-49.
55. Winter C., Schenkel J., Zimmermann M., Herdegen T. MAP kinase phosphatase 1 is expressed and enhanced by FK506 in surviving mamillary, but not degenerating nigral neurons following axotomy. Brain Res. 801:1998;198-205.
56. Yoo A.S., Cheng I., Chung S., Grenfell T.Z., Lee H., Pack-Chung E., Handler M., Shen J., Xia W., Tesco G., Saunders A.J., Ding K., Frosch M.P., Tanzi R.E., Kim T.W. Presenilin-mediated modulation of capacitative calcium entry. Neuron. 27:2000;561-572.
57. Zawadzka M., Kaminska B. Immunosuppressant FK506 affects multiple signaling pathways and modulates gene expression in astrocytes. Mol. Cell. Neurosci. 22:2003;202-209.
58. Zhao W.Q., Chen H., Xu H., Moore E., Meiri N., Quon M.J., Alkon D.L. Brain insulin receptors and spatial memory. Correlated changes in gene expression, tyrosine phosphorylation, and signaling molecules in the hippocampus of water maze trained rats. J. Biol. Chem. 274:1999;34893-34902.
59. Zhao W.Q., Ravindranath L., Mohamed A.S., Zohar O., Chen G.H., Lyketsos C.G., Etcheberrigaray R., Alkon D.L. MAP kinase signaling cascade dysfunction specific to Alzheimer's disease in fibroblasts. Neurobiol. Dis. 11:2002;166-183.