Phospholipids alter tau conformation, phosphorylation, proteolysis, and association with microtubules: Implication for tau function under normal and degenerative conditions

Journal of Neuroscience Research

Volumn 50, Issue 1, 1997, Pages 114-122

  Shea, Thomas B ^a  

^a UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

Author keywords

Alzheimer's disease; MAP kinase; Neurodegeneration; Paired helical filaments; Phosphatidyl serine

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; PHOSPHOLIPID; TAU PROTEIN;

ALZHEIMER DISEASE; ARTICLE; CATTLE; HUMAN; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; NONHUMAN; PAIRED HELICAL FILAMENT; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION;

ALZHEIMER DISEASE; ANIMALS; ANTIBODY SPECIFICITY; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALPAIN; CATTLE; CELL-FREE SYSTEM; HUMANS; MICROTUBULES; NERVE DEGENERATION; PHOSPHATIDYLSERINES; PHOSPHOLIPIDS; PHOSPHORYLATION; PROTEIN CONFORMATION; TAU PROTEINS;

EID: 0030766489     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19971001)50:1<114::AID-JNR12>3.0.CO;2-B     Document Type: Article

References (47)

1. Aizawa H, Kawasaki H, Murofushi S, Kotani K, Suzuki, Sakai H (1988): Microtubule-binding domain of tau proteins. J Biol Chem 263:7703-7707.
2. Baas PW, Pienkowski TP, Cimbalnik KA, Toyama K, Bakalis S, Ahmand FJ, Kosik KS (1994): Tau confers drug-stability but cold-stability to microtubules in living cells. J Cell Sci 107:135-143.
3. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Wiche G, Seiteberger F, Grundke-Iqbal I, Iqbal I, Wisniewski HM (1989): Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res 477:90-99.
4. Baudier J, Cole RD (1987) Phosphorylation of tau proteins to a state like that in Alzheimer's brain in catalyzed by a calcium/ calmodulin-dependent kinase and modulated by phospholipids. J Biol Chem 262:17577-17583.
5. Baudier J, Lee S-H, Cole RD (1987) Separation of the different microtubule-associated tau proteins from bovine brain and their mode II phosphorylation by Ca2+/phospholipid-dependent protein kinase C. J Biol Chem 262:17584-17590.
6. Binder LI, Wilson DW, Kuret J (1996): Lipid stimulation of tau polymerization into Alzheimer straight filament-like structures. J Neurochem 66 Supp: S95.
7. Black MM, Slaughter T, Moshiach M, Obrocka M, Fischer I (1996): Tau is enriched on dynamics microtubules in the distal region of growing axons. J Neurosci 16:3601-3619.
8. Brambett GT, Goedert M, Jakes R, Merrick SE, Trojanowski JQ, Lee VM-Y (1993): Abnormal tau phosphorylation at ser-396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10:1089-1099.
9. Brandt R, Leger J, Lee G (1995): Interaction of tau with the neural plasma membrane mediated by tau's amino-lerminal projection domain. J Cell Biol 131:1327-1340.
10. Burns RG, Surridge CD (1995): The phosphatidylinositol-binding site of microtubule-associated protein MAP2. Biochem Soc Trans 23:41-46.
11. Cleveland DW, Hwo SY, Kirschner MW (1977): Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol 116:227-247.
12. Cressman CM, Shea TB (1995): Hyperphosphorylation of tau and filopodial retraction following microinjection of protein kinase C catalytic subunits. J Neurosci Res 42:648-656.
13. Cressman CM, Mercken MM, Shea TB (1995a): Alteration in tau antigenicity and electrophoretic migration by PKCα under cell-free conditions. Neurosci Res Commun 17:61-64.
14. Cressman CM, Mohan PS, Nixon RA, Griffin WR, Shea TB (1995b): Proteolysis of protein kinase C: mM and μM calcium-requiring calpains have different abilities to generate, and degrade, the free catalytic subunit, protein kinase M. FEBS Lett 1995 367:223-227.
15. Dreschel DN, Hyman AA, Cobb MH, Kirschner MW (1992): Modulation of the dynamic instability of tubulin assembly by the microtubule-associated protein tau. Mol Biol Cell 3:1141-1154.
16. Drubin DG, Kirschner MW (1986): Tau protein function in living cells. J Cell Biol 103:2739-2746.
17. Garver TD, Harris KA, Lehman RAW, Lee Vm-Y, Trojanowski JQ, Billingsley ML (1994): Tau phosphorylation in human, primate and rat brain: Evidence that a pool of tau is highly phosphorylated in vivo and is rapidly dephosphorylated in vitro. J Neurochem 63:2279-2287.
18. Goedert M (1993): Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends Neurosci 16:460-465.
19. Goedert M, Jakes R, Crowther RA, Six J, Lubke U, Vandermeeren M, Cras P, Trojanowski JQ, Lee VM-Y (1993): The abnormal phosphorylation of tau proteins at ser-202 in Alzheimer's disease recapitulates phosphorylation during development. Proc Natl Acad Sci USA 90:5066-5070.
20. Gray EG, Paula-Barbosa M, Roher (1987): Alzheimer's disease: Paired helical filaments and cytomembranes. Neuropath Appl Neurobiol 13:91-110.
21. Hagestedt T, Lichtenberg B, Wille H, Mandelkow E-M, Mandelkow E (1989): Tau protein becomes long and stiff upon phosphorylation: Correlation between paracrystalline structure and degree of phosphorylation. J Cell Biol 109:1643-1651.
22. Himmler A, Dreschel D, Kirschner MW, Martin DW (1989): Tau consists of a set of proteins with repeated C-terminal microtubule-binding domains and variable N-terminal domains. Mol Cell Biol 9:1381-1388.
23. Hwang SC, Jhon DY, Bae YS, Kim JH, Rhee SG (1996): Activation of phospholipase C-gamma by the concerted action of tau proteins and arachidonic acid. J Biol Chem 27:18342-18349.
24. Johnson GVW, Jope RS, Binder LI (1989): Proteolysis of tau by calpain. Biochem Biophys Res Commun 163:1505-1511.
25. Kempf M, Clement A, Faissner A, Lee G, Brandt R (1996): Tau binds to the distal axon early in development of polarity in a microtubule-and microfilament-dependent manner. J Neurosci 16:5583-5592.
26. Kosik KS (1993): The molecular and cellular biology of tau. Brain Pathol 3:39-43.
27. Kosik KS, Finch EA (1987): MAP2 and tau segregate into dendritic and axonal domains after the elaboration of morphologically distinct neurites: An immunochemical study of cultured rat cerebellum. J Neurosci 7:3142-3153.
28. Kuret J, Hantash B, Cha D, Wilson DM, Binder LI (1996): Morphological and structural characterization of lipid-induced tau polymers. Mol Biol Cell 7:569a.
29. Lang D, Beermann ML, Hauser G, Cressman CM, Shea TB (1995): Phospholipids inhibit proteolysis of protein kinase Cα by mM calcium-requiring calpain. Neurochem Res 20:1361-1364.
30. Lee G, Neve RL, Kosik KS (1989): The microtubule binding domain of tau protein. Neuron 2:1615-1624.
31. Lee G, Kwei SL, Newman ST, Lu M, Yiu Y (1996a): A new molecular interactor for tau protein. Trans Am Soc Neurosci 22:975.
32. Lee G, Kwei SL, Newman ST, Olmstead J, Yiu Y (1996b): A new molecular interactor for tau protein. Mol Biol Cell 7:570a.
33. Litersky JM, Scott CW, Johnson GVW (1993): Phosphorylation, calpain proteolysis and tubulin binding of recombinant tau isoforms. Brain Res 604:32-40.
34. Mandelkow EM, Mandelkow E (1993): Tau as a marker for Alzheimer's disease. Trends Biochem Sci 18:480-483.
35. Mandell JW, Banker GA (1996): A spatial gradient of tau protein phosphorylation in nascent axons. J Neurosci 16:5727-5740.
36. Matsuo ES, Shin RW, Billingsley ML, Van deVoorde A, O'Connor M, Trojanowski JQ, Lee VM-Y (1994): Biopsy-derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13:989-1002.
37. Pope WB, Enam SA, Bawa N, Miller BE, Ghanbari HA, Klein WL (1993): Phosphorylated tau epitope of Alzheimer's disease is coupled to axon development in the avian central nervous system. Exp Neurol 120:106-113.
38. Pope WB, Lambert MP, Leypold B, Seupaul R, Sletten L, Krafft G, Klein WL (1994): Microtubule-associated protein tau is hyperphosphorylated during mitosis in the human neuroblastoma cell line SH-SY-5Y. Exp Neurol 126:185-194.
39. Rebhan M, Vacun G, Rösner H (1995): Complementary distribution of tau proteins in different phosphorylation states within growing axons. NeuroReport 6:429-432.
40. Shea TB, Beermann ML (1994): Respective roles of neurofilaments, microtubules, MAP1B and tau in the outgrowth and stabilization of axonal neuntes. Mol Biol Cell 5:863-875.
41. Shea TB, Fischer I (1996): Phosphatase inhibition in human neuroblastoma cells alters tau antigenicity and renders it incompetent to associate with exogenous microtubules. FEBS Lett 380:63-67.
42. Shea TB, Spencer MJ, Beermann ML, Cressman CM, Nixon RA (1996a): Calcium influx into human neuroblastoma cells induces ALZ-50 immunoreactivity: Involvement of calpain-mediated hydrolysis of protein kinase C. J Neurochem 66:1539-1549.
43. Shea TB, Cressman CM, Fischer I (1996b): Preferential translocation of HMW tau isoforms into newly-elaborated neurites in human neuroblastoma. J Neurochem 66 Supp: S62.
44. Surridge CD, Burns RG (1994): The difference in the binding of phosphatidylinositol distinguishes MAP2 from MAP2C and tau. Biochem 33:8051-8057.
45. Takemura R, Okabe S, Umeyama T, Kanai Y, Cowan NI, Hirokawa N (1992): Increased microtubule stability and alpha-tubulin acetylation in cells transfected with microtubule-associated proteins MAP1B, MAP2 or tau. J Cell Sci 103:953-964.
46. Willis KJ (1994): Interaction with model membrane system induces secondary structure in amino-terminal fragments of parathyroid hormone-related protein. Int J Peptide Protein Res 43:23-28.
47. Yang L-S, Ksiezak-Reding H (1995): Calpain-induced proteolysis of normal human tau and tau associated with paired helical filaments. Eur J Biochem 233:9-17.