Protein kinase-C and calcium/calmodulin-dependent protein kinase II phosphorylate three-repeat and four-repeat tau isoforms at different rates

Molecular and Cellular Biochemistry

Volumn 168, Issue 1-2, 1997, Pages 141-148

  Singh, Toolsee J ^a   Grundke Iqbal, Inge ^a   Wu, Wu Qiongli ^a   Chauhan, Ved ^a   Novak, Michal ^b   Kontzekova, Eva ^b   Iqbal, Khalid ^a  

^a NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^b INSTITUTE OF NEUROIMMUNOLOGY   (Slovakia)

Author keywords

Alzheimer's disease; Microtubules; Protein kinase C; Protein kinases; Tau protein

Indexed keywords

ISOPROTEIN; PHOSPHOSERINE; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE C; TAU PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; NONHUMAN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION;

CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; KINETICS; PHOSPHORYLATION; PROTEIN KINASE C; SERINE;

ANIMALIA;

EID: 0031046463     PISSN: 03008177     EISSN: None     Source Type: Journal    
DOI: 10.1023/A:1006807105059     Document Type: Article

References (45)

1. Grudke-Iqbal I, Iqbal K, Quinlan M, Tung Y-C, Zaidi MS, Wisniewski HM: Microtubule-associated protein tau: a component of Alzheimer's paired helical filaments. J Biol Chem 261: 6084-6089, 1986
2. Grundke-Iqbal I, Iqbal K, Tung Y-C, Quinlan M, Wisniewski HM, Binder LI: Abnormal phosphorylation of the microtubule-associated protein tau in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83: 4913-4917, 1986
3. Iqbal K, Grundke-Iqbal I, Smith AJ, George L Tung Y-C, Zaidi T: Identification and localization of a tau peptide to paired helical filaments of Alzheimer disease. Proc Natl Acad Sci USA 86: 5646-5650, 1989
4. Brion JP, Hanger DP, Bruce MT, Couck AM, Flament-Durant J, Anderton BT: Tau in Alzheimer's neurofibrillary tangles. Biochem J 273: 127-133, 1991
5. Morishima-Kawashima M, Hasegawa M, Takio K, Suzuki M, Yoshida H, Titani K, Ihara Y: Proline-directed and non-proline-directed phosphorylation of PHF-tau. J Biol Chem 270: 823-829, 1995
6. Drewes G, Lichtenberg-Kraag B, Coring F, Mandelkow EM, Biernat J, Goris J, Doree M, Mandelkow E: Mitogen-activated protein (MAP) kinase transforms tau protein into an Alzheimer-like state. EMBO J 11: 2131-2138, 1992
7. Goedert M, Cohen ES, Jakes R, Cohen P: P42 map kinase phosphorylation sites in microtubule-associated protein tau are dephosphorylated by protein phosphatase 2A. FEBS Lett 312: 95-99, 1992
8. erk converts tau into a PHF-like form as found in Alzheimer's disease. Biochem Biophys Res Commun 193: 639-647, 1993
9. Vulliet R, Halloran SM, Braun RK, Smith AJ, Lee G: Proline-directed phosphorylation of human tau protein. J Biol Chem 267: 22570-22574, 1992
10. Baumann K, Mandelkow EM, Biernat J, Piwnica-Worms H, Mandelkow E: Abnormal Alzheimer-like phosphorylation of tau protein by cyclin dependent kinases cdk2 and cdk5. FEBS Lett 336: 417-424, 1993
11. Paudel HK, Lew J, Ali Z, Wang JH: Brain proline-directed protein kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments. J Biol Chem 268: 23512-23518, 1993
12. Mandelkow EM, Drewes G, Biernat J, Gustke N, Van Lint J, Vandenheede JR, Mandelkow E: Glycogen synthase kinase-3 and the Alzheimer-like state of microtubule-associated protein tau. FEBS Lett 314: 315-321, 1992
13. Ishiguro K, Shiratsuchi A, Sato S, Omori A, Arioka M, Kobayashi S, Uchida T, Imahori K: Glycogen synthase kinase 3β is identical to tau protein kinase I, generating several epitopes of paired helical filaments. FEBS Lett 325: 167-172, 1993
14. A/GSK-3 phosphorylates ρ on ser 235-pro and ser 404-pro that are abnormally phosphorylated in Alzheimer's disease brain. J Neurochem 61: 1742- 1747, 1993
15. Singh TJ, Haque N, Grandke-Iqbal I, Iqbal K: Rapid Alzheimer-like phosphorylation of tau by the synergistic actions of non-proline-dependent protein kinases and GSK-3. FEBS Lett 358: 267-272, 1995
16. Singh TJ, Zaidi T, Grandke-Iqbal I, Iqbal K: Modulation of GSK-3- catalyzed phosphorylation of microtubule-associated protein tau by non-proline-dependent protein kinases. FEBS Lett 358: 4-8, 1995
17. Singh TJ, Grundke-Iqbal I, Iqbal K: Differential phosphorylation of human tau 17 isoforms containing three repeats by several protein kinases. Arch Biochem Biophys 328: 43-50, 1996
18. Litersky JM, Johnson GVVV: Phosphorylation by cAMP-dependent protein kinase inhibits the degradation of tau by calpain. J Biol Chem 267: 1563-1568, 1992
19. Scott CW, Spreen RC, Herman JL, Chow FP, Davison MD, Young J, Caputo CB: Phosphorylation of recombinant tau by cAMP-dependent protein kinase. J Biol Chem 268: 1166-1173, 1993
20. Singh TJ, Grundke-Iqbal I, Iqbal K: Phosphorylation of tau protein by casein kinase-1 converts it to an abnormal Alzheimer-like state. J Neurochem 64: 1420-1423, 1995
21. Baudier J, Lee S-H, Cole RD: Separation of the different microtubule- associated tau protein species from bovine brain and their mode II phosphorylation by calcium/phospholipid-dependent protein kinase. J Biol Chem 262: 17584-17590, 1987
22. Correas I, Diaz-Nido J, Avila J: Microtubule-associated protein tau is phosphorylated by protein kinase C on its tubulin-binding domain. J Biol Chem 267: 15721-15728, 1992
23. Singh, TJ, Zaidi T, Grundke-Iqbal I, Iqbal K: Non-proline-dependent protein kinases phosphorylate several sites found in tau from Alzheimer disease brain. Mol Cell Biochem 154: 143-151, 1996
24. Baudier J, Cole RD: Phosphorylation of tau proteins to a state like that in Alzheimer's brain is catalyzed by calcium/calmodulin-dependent protein kinase and modulated by phospholipids. J Biol Chem 262: 17577-17583, 1991
25. Singh TJ, Grundke-Iqbal I, McDonald B, Iqbal K: Comparison of the phosphorylation of microtubule-associated protein tau by non-proline- dependent protein kinases. Mol Cell Biochem 131: 181-189, 1994
26. Greenwood JA, Scott CW, Spreen RC, Caputo CB, Johnson GVW: Casein kinase II preferentially phosphorylates human tau isoforms containing an amino-terminal insert. J Biol Chem 269: 4373-4380, 1994
27. erk2: Regulation by prior phosphorylation with cAMP dependent protein kinase. Biochem Biophys Res Commun 215: 1056-1066, 1995
28. Sengupta A, Wu Q, Grundke-Iqbal I, Iqbal K, Singh TJ: Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by cdk5. Mol Cell Biochem, 167: 99-105, 1997
29. Goedert M, Spillantini MG, Jakes R, Rutherford D, Crowther RA: Multiple isoforms of human microtubule-associated protein tau: Sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron 3: 519-526, 1989
30. Köpke E, Tung Y-C, Shaikh S, Alonso AC, Iqbal K, Grundke-Iqbal I: Microtubule associated protein tau: Abnormal phosphorylation of a non-paired helical fflament pool in Alzheimer's disease. J Biol Chem 268: 24374-24384, 1993
31. Goedert M, Spillantini MG, Cairns NJ, Crowther RA: Tau proteins of Alzheimer paired helical filaments: Abnormal phosphorylation of all six brain isoforms. Neuron 8: 159-168, 1992
32. Singh TJ: Polyamines stimulate the activity of glycogen synthase (casein) kinase-1 from bovine kidney and different rat tissues. Arch Biochem Biophys 267: 167-175, 1988
33. Tung HYL, Reed LJ: Purification and characterization of protein phosphatase 1 activating kinase from bovine brain cytosol and particulate fractions. J Biol Chem 264: 2985-2990, 1989
34. 21/calmodulin-dependent protein kinase enriched in cerebellar granule cells. J Biol Chem 264: 5866-5875, 1989
35. 2+-activated and phospholipid- dependent protein kinase. J Biol Chem 261: 12134-12140, 1986
36. Greenberg SG, Davies P: A preparation of Alzheimer's paired helical filaments that displays distinct T proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 87: 5827-5831, 1990
37. Otvos L, Feiner L, Lang E, Szendrei GI, Goedert M, Lee VM-Y: Phosphorylated serine residues 396 and 404 in paired helical filaments define the epitope for the monoclonal antibody PHF-1. J Neurosci Res 39: 669-673, 1995
38. Hasegawa M, Watanabe A, Takio K, Suzuki M, Arai T, Titani K, Ihara Y: Characterization of two distinct monoclonal antibodies to paired helical filaments: Further evidence for fetal-type phosphorylation of the tau in paired helical filaments. J Neurochem 60: 2068-2077, 1993
39. 262 in fetal tau, adult tau, and paired helical filament tau. J Biol Chem 270: 18917-18922, 1995
40. Huang K-P, Robinson JC: A rapid and sensitive assay method for protein kinase. Anal Biochem 72: 593-599, 1976
41. Fellous F, Francon J, Lennon AM, Nunez J: Microtubule assembly in vitro: Purification of assembly-promoting factors. Eur J Biochem 78: 167-174, 1977
42. Singh TJ, Wang J-Z, Novak M, Kontzekova E, Grundke-Iqbal I, Iqbal K: Calcium/calmodulin-dependent protein kinase II phosphorylates tau at ser 262 but only partially inhibits its binding to microtubules. FEBS Lett 387: 145-148, 1996
43. 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, 1995
44. Steiner B, Mandelkow E-M, Biernat J, Gustke N, Meyer HE, Schmidt B, Mieskes G, Soling HD, Drechsel D, Kirschner MW, Goedert M, Mandelkow E: Phosphorylation of microtubule-associated protein tau: Identification of the site for calcium/calmodulin-dependent kinase and relationship with tau phosphorylation in Alzheimer tangles. EMBO J 9: 3539-3544, 1990
45. Hasegawa M, Jakes R, Crowther RA, Lee VM-Y, Ihara Y, Goedert M: Characterization of mAb AP422, a novel phosphorylation-dependent monoclonal antibody against tau protein. FEBS Lett 384: 25-30, 1996