Reduction of calcineurin activity in brain by antisense oligonucleotides leads to persistent phosphorylation of τ protein at Thr181 and Thr231

Molecular Pharmacology

Volumn 55, Issue 4, 1999, Pages 632-641

  Garver, Timothy D ^a,c   Kincaid, Randall L ^b   Conn, Richard A ^a   Billingsley, Melvin L ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b Veritas Inc   (United States)

^c Lineberry Associates   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; ASCOMYCIN; CALCINEURIN; MONOCLONAL ANTIBODY; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE; PROTEIN KINASE; TAU PROTEIN; THREONINE;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; IMMUNOBLOTTING; MALE; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; BRAIN; CALCINEURIN; MALE; NEOCORTEX; OLIGONUCLEOTIDES, ANTISENSE; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; TAU PROTEINS; THREONINE;

EID: 0032917077     PISSN: 0026895X     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (39)

1. Albert PR and Morris SJ (1994) Antisense oligonucleotides: Molecular scapels for dissection of signal transduction pathways. Trends Pharmacol Sci 15:250-254.
2. Arias C, Sharma N, Davies P and Shafit-Zagardo B (1993) Okadaic acid induces early changes in microtubule-associated protein 2 and τ phosphorylation prior to neurodegeneration in cultured cortical neurons. J Neurochem 61:673-682.
3. Baumann K, Mandelkow E-M, Biernat J, Piwnica-Worms H and Mandelkow E (1993) Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases like cdk2 and cdk5. FEBS Lett 336:417-424.
4. 262 strongly reduces binding of tau to microtubules: Distinction between PHF-like immunoreactivity and microtubule binding. EMBO J 11:1593-1597.
5. Billingsley ML (1995) Biochemical and molecular characterization of calcineurin (protein phosphatase 2B) in nervous tissue. Neuroprotocols 6:20-28.
6. Billingsley ML and Kincaid RL (1997) Regulated phosphorylation and dephosporylation of tau protein: Effects on microtubule interaction intracellular trafficking and neurodegeneration. Biochem J 323:577-591.
7. Blumenthal D, Takio K, Hansen RS and Krebs E (1986) Dephosphorylation of cAMP-dependent protein kinase regulatiory subunit (type II) by calmodulin-dependent protein phosphatase. J Biol Chem 261:8140-8145.
8. 396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10:1089-1099.
9. mark). J Biol Chem 270:7679-7688.
10. Ferreira A, Kincaid RL and Kosik KS (1993) Localization of calcineurin in growth cones of neurons. Mol Biol Cell 4:1225-1238.
11. Garver TD, Harris KA, Lehman RAW, Lee VM-Y, Trojanowski JQ and Billingsley ML (1994) Evidence that a pool of τ is highly phosphorylated in vivo and is rapidly dephosphorylated in vitro. J Neurochem 63:2279-2287.
12. Garver TD, Oyler GA, Harris KA, Polavarapu RG, Damuni Z, Lehman RAW and Billingsley ML (1995) Tau phosphorylation in brain slices: Pharmacological evidence for convergent effects of protein phosphatases on tau and mitogen-activated protein kinase. Mol Pharmacol 47:745-756.
13. Giri PR, Marietta CA, Higuchi S and Kincaid RL (1992) Molecular and phylogenetic analysis of calmodulin-dependent protein phosphatase (calcineurin) catalytic sub-unit genes. DNA Cell Biol 11:415-424.
14. 1. FEBS Lett 312:95-99.
15. Goedert M and Jakes R (1990) Expression of separate isofonns of human tau protein: Correlation with the human tau pattern in brain and effects on tubulin polymerization. EMBO J 9:4225-4230.
16. Goedert M, Jakes R, Crowther RA, Cohen P, Vanmechelen E, Vandermeeren M and Cras P (1994) A preparation of Alzheimer paired helical filaments that display distinct tau proteins by polyacrylamide gel electrophoresis. Biochem J 301:871-877.
17. Goedert M, Spillantini MG, Cairns NJ and Crowther RA (1992a) Tau protein of Alzheimer paired helical filaments: Abnormal phosphorylation of all six brain isoforms. Neuron 8:159-168.
18. Goedert M, Spillantini MG, Jakes R, Rutherford D and Crowther RA (1989) Multiple isoforms of human microtubule associated protein tau: Sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3:519-526.
19. Goto S, Yamamoto H, Fukunaga K, Iwasa T, Matsukado Y and Miyamoto E (1985) Dephosphorylation of microtubule-associated protein 2, τ factor and tubulin by calcineurin. J Neurochem 45:276-283.
20. Greenberg SG and Davies P (1987) A preparation of Alzheimer paired helical filaments that display distinct tau proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 87:5827-5831.
21. Grunke-Iqbal I, Iqbal K, Tung Y-C, Quinlan M, Wisniewski HM and Binder LI (1986) Abnormal phosphorylation of the microtubule-associated protein tau in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83:4913-4917.
22. Harris KA, Oyler GA, Doolittle GM, Vincent I, Lehman RAW, Kincaid RL and Billingsley ML (1993) Okadaic acid induces hyperphosphorylated forms of tau protein in human brain slices. Ann Neurol 33:77-87.
23. Hasegawa M, Morishima-Kakashima M, Takio K, Suzuki M, Titani K and Ihara Y (1993) Protein sequence and mass spectrophotometric analysis of tau in Alzheimer's disease brain. J Biol Chem 267:17047-17054.
24. Ikegami S, Kato A, Kudo Y, Kuno T, Ozawa F and Inokuchi K (1996) A facilitory effect on the induction of long-term potentiation in vivo by chronic administration of antisense oligodeoxynucleotides against catalytic subunits of calcineurin. Mol Brain Res 42:183-191.
25. Ishiguro K, Takamatsu M, Tomizawa K, Omori A, Takahashi M, Arioka M, Uchida T and Imahori K (1992) Tau protein kinase I converts normal tau protein into A68-like component of paired helical filaments. J Biol Chem 267:10897-10901.
26. Kayyali US, Zhang W, Yee AG, Seidman JG and Potter H (1997) Cytoskeletal changes in the brains of mice lacking calcineurin Aa. J Neurochem 68:1668-1678.
27. Kincaid RL, Giri RP, Higuchi S, Tamura J, Dixon SC, Marietta CA, Amorese DA and Martin BA (1990) Cloning and characterization of molecular isoforms of the catalytic subunit of calcineurin using nonisotopic methods. J Biol Chem 265: 11312-11319.
28. Kosik KS, Orecchio LD, Binder L, Trojanowski JQ, Lee VM-Y and Lee G (1988) Epitopes that span the tau molecule are shared with paired helical filaments. Neuron 1:817-825.
29. Kuno T, Mukai H, Ito A, Chang CD, Kishima K, Saito N and Tanaka C (1992) Evidence for a second isoform of the catalytic subunit of calmodulin-dendent protein phosphatase (calcineurin A). J Neurochem 58:1643-1651.
30. cdc2. J Biol Chem 267:25922-25926.
31. Matsuo ES, Shin R-Y, Billingsley ML, Van de Voorde A, O'Connor M and Lee VM-Y (1994) Freshly extracted biopsy derived adult human brain tau is phosphorylation at many of the same sites as paired helical filament tau in Alzheimer's disease. Neuron 13:989-1002.
32. Milligan JF, Matteucci MD and Martin JC (1993) Current concepts in antisense drug design. J Med Chem 36:1923-1937.
33. Parsons JN, Wiederrecht GJ, Salowe S, Burbaum JJ, Rokosz LL, Kincaid RL and O'Keefe SJ (1994) Regulation of calcineurin phosphatase activity and interaction with the FK-506:FK-506 binding protein complex. J Biol Chem 269:19610-19616.
34. Payne D, Rossomando A, Martino P, Erickson A, Her J-H, Sbanowitz J, Hunt D, Weber M and Sturgill T (1991) Identification of the regulatory phosphorylation sites in p42/mitogen-activated protein kinase (MAP kinase). EMBO J 10:885-892.
35. Polli JW, Billingsley ML and Kincaid RL (1991) Expression of the calmodulin-dependent protein phosphatase calcineurin in rat brain: Developmental patterns and the role of nigrostriatal innervation. Dev Brain Res 63:105-119.
36. Spencer SA, Schuh SM, Liu W-S and Willard M (1992) Identification of phosphorylation sites in GAP-43. J Biol Chem 267:9059-9064.
37. 2+-calmodulin-dependent protein kinase and relationship with tau phosphorylation in Alzheimer's tangles. EMBO J 9:3539-3544.
38. Vulliet R, Halloran SM, Braun RK, Smith AJ and Lee G (1992) Proline-directed phosphorylation of human tau protein. J Biol Chem 267:22570-22574.
39. Wagner RW (1994) Gene inhibition using antisense oligonucleotides. Nature (London) 371:333-335.