Protein phosphatase inhibitors induce modification of synapse structure and tau hyperphosphorylation in cultured rat hippocampal neurons

Journal of Neuroscience Research

Volumn 48, Issue 5, 1997, Pages 425-438

  Malchiodi Albedi, Fiorella ^a   Petrucci, Tamara C ^a   Picconi, Barbara ^a   Iosi, Francesca ^a   Falchi, Mario ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Alzheimer's disease; Caliculin A; cytoskeleton; okadaic acid; synaptic proteins

Indexed keywords

CALICULIN A; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE INHIBITOR; TAU PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME INHIBITION; HIPPOCAMPUS; NERVE FIBER TRANSPORT; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SYNAPSE;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CYTOSKELETON; ENZYME INHIBITORS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MICROSCOPY, ELECTRON, SCANNING; NEURITES; NEURONS; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHORYLATION; RATS; RATS, WISTAR; SYNAPSES; SYNAPTIC VESICLES; TAU PROTEINS;

EID: 0031004401     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-4547(19970601)48:5<425::AID-JNR4>3.0.CO;2-G     Document Type: Article

References (60)

1. Alonso A del C, Zaidi T, Grundke-Iqbal I, Iqbal K (1994): Role of abnormally phosphorylated tau in the breakdown of microtubules an Alzheimer's disease. Proc Natl Acad Sci USA 91:5562-5566.
2. Arendt T, Holzer M, Fruth R, Bruckner MK, Gartner U (1995): Paired helical filament-like phosphorylation of tau, deposition of b/A4-amyloid and memory impairment in rat induced by chronic inhibition of phosphatase 1 and 2A. Neuroscience 69:691-698.
3. Arias C, Sharma N, Davies P, Shafit-Zagardo B (1993): Okadaic acid induces early changes in microtubulc-associated protein 2 and tau phosphorylation prior to neurodegeneration in cultured cortical neurons. J Neurochem 61:673-782.
4. Bartlett WP, Banker GA (1984): An electron microscopic study of the development of axons and dendrites by hippocampal neurons in culture. II. Synaptic relationships. J Neurosci 4:1954-1965.
5. Basarsky TA, Parpura V, Haydon PG (1994): Hippocampal synaptogenesis in cell culture: developmental time course of synapse formation, calcium influx, and synaptic protein distribution. J Neurosci 14:6402-6411.
6. Betz WJ, Henkel AW (1994): Okadaic acid disrupts clusters of synaptic vesicles in frog motor nerve terminals. J Cell Biol 124:843-854.
7. Bialojan C, Takai A (1988): Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem J 256:283-290.
8. 262 strongly reduces binding of tau to microtubules: distinction between PHF-like immunoreactivity and microtubule binding. Neuron 11:153-163.
9. Bloom GS, Richards BW, Leopold PL, Ritchey DM, Brady ST (1993): GTP-γS inhibits organelle transport along axonal microtubules. J Cell Biol 120:467-476.
10. Bottenstein JE, Sato GH (1979): Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci USA 76:514-517.
11. 396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neuron 10:1089-1099.
12. Busciglio J, Lorenzo A, Yeh J, Yankner B (1995): B-amyloid fibrils induce tau phosphorylation and loss of microtubule binding. Neuron 14:879-888.
13. Chang MF, Liu W-K, Yen S-H (1993): Reversible heat stress-related loss of phosphorylated Alzheimer-type epitopes in tau proteins of human neuroblastoma cells. J Neurosci 13:4854-4860.
14. Choi DW (1988): Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623-634.
15. Choi DW, Maulucci-Gedde M, Kriegstein AR (1987): Glutamate neurotoxicity in cortical cell cultures. J Neurosci 7:357-368.
16. Cleveland DW, Hwo S, Kirschener MW (1977): Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J Mol Biol 116:207-225.
17. Churn BS, Limbrick D, Sombati S, DeLorenzo R (1995): Excitotoxic activation of the NMDA receptor results in inhibition of calcium/calmodulin kinase II activity, in cultured hippocampal neurons. J Neurosci 15:3200-3214.
18. Cohen P, Holmes CFB, Tsukitani Y (1990): Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem Sci 15:98-102.
19. Davies CA, Mann DMA, Sumpter PQ, Yates PO (1987): A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J Neurol Sci 78:151-164.
20. DeKosky ST, Schaff SW (1990): Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 27:457-464.
21. Diaz-Nido J, Serrano L, Hernandez MA, Avila J (1990): Phosphorylation of microtubule proteins in rat brain at different developmental stages: comparison with that found in neuronal cultures. J Neurochem 54:211-222.
22. Dotti CG, Sullivan CA, Banker GA (1988): The establishment of polarity by hippocampal neurons in culture. J Neurosci 8:1454-1468.
23. Fletcher TL, Cameron P, De Camilli P, Banker G (1991): The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture. J Neurosci 11:1617-1626.
24. Fletcher TL, De Camilli P, Banker G (1994): Synaptogenesis in hippocampal cultures: evidence indicating that axons and dendrites become competent to form synapses at different stages of neuronal development. J Neurosci 14:6695-6706.
25. Geddes JW, Schwab C, Craddock S, Wilson JL, Pettigrew LC (1994): Alterations of tau immunostaining in the rat hippocampus following transient cerebral ischemia. J Cereb Blood Flow Metab 14:554-564.
26. Gong C-X, Shaikh S, Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K (1995): Phosphatase activity toward abnormally phosphorylated tau: decrease in Alzheimer's disease brain. J Neurochem 65:732-738.
27. Gonatas NK, Anderson WV, Evangelism I (1967): The contribution of altered synapses in senile plaque: an electron microscopic study in Alzheimer's disease. J Neuropathol Exp Neurol 26:25-39.
28. Goslin K, Banker G (1991): Rat hippocampal neurons in low density culture. In Banker G, Goslin K (eds.): "Culturing Nerve Cells." Cambridge. MA: MIT Press, pp 251-282.
29. Greenberg SG, Davies P (1990): A preparation of Alzheimer paired helical filaments that display distinct t proteins by polyacrylamide gel electrophoresis. Proc Natl Acad Sci USA 87:5827-5831.
30. Greengard P (1978): Phosphorylated proteins as physiological effectors. Science 199:146-152.
31. Greengard P, Valtorta F, Czernik AJ, Benfenati F (1993): Synaptic vesicle phosphoproteins and regulation of synaptic function. Science 259:780-785.
32. Grundke-Iqbal I, Iqbal K, Tung Y-C, Quinlan M, Wisniewsky HM, Binder LI (1986): Abnormal phosphorylation of the microtubule-associated protein t in Alzheimer cytoskeletal pathology. Proc Natl Acad Sci USA 83:4913-4917.
33. Gurland G, Gundersen GG (1993): Protein phosphatase inhibitors induce the selective breakdown of stable microtubules in fibroblasts and epithelial cells. Proc Natl Acad Sci USA 90:8827-8831.
34. Hajimohammadreza I, Probert AW, Coughenour LL, Borosky SA, Marcoux FW, Boxer PA, Wang KKW (1995): A specific inhibitor of calcium/calmodulin-dependent protein kinase-II provide neuroprotection against NMDA- and hypoxia/hypoglycemia-induced cell death. J Neurosci 15:4093-4101.
35. Heinonen O, Soininen H, Sorvari H, Kosunen O, Paljarvi L, Koivisto E, Riekkinen Sr PJ (1995): Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neuroscience 64:375-384.
36. Huganir RL, Greengard P (1990): Regulation of neurotransmitter receptor desensization by protein phosphorylation. Neuron 5:555-567.
37. Iqbal K, Grundke-Ikbal I, Smith AJ, George L, Tung Y-C, Zaidi T (1989): Identification and localization of a t peptide to paired helical filaments of Alzheimer's disease. Neurobiology 86:5646-5650.
38. Ishihara H, Martin BL, Brautigan DL, Karuki H, Ozaki H, Kato Y, Fusetani N, Watabe S, Hashimoto K, Uemura D, Hartshorne DJ (1989): Caliculin A and ocadaic acid: inhibitors of protein phosphatase activity. Biochem Biophys Res Commun 159:871-877.
39. Laemmli UK (1970): Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
40. Lee VM-Y, Balin BJ, Otvos L, Jr, Trojanowski JQ (1991): A68: a major subunit of paired helical filaments and derivatized forms of normal tau. Science 251:675-679.
41. Lindwall G, Cole RD (1984): The purification of tau protein and the occurrence of two phosphorylation states of tau in brain. J Biol Chem 259:12241-12245.
42. Liu W-K, Dickson DW, Yen S-H (1992): Heterogeneity of tau proteins in Alzheimer's disease: evidence for increased expression of an isoform and preferential distribution of a phosphorylated isoform in neurites. Am J Pathol 142:387-394.
43. Lorenzo A, Yankner BA (1994): Beta amyloid neurotoxicity requires fibril formation and is inhibited by Congo red. Proc Natl Acad Sci USA 91:12243-12247.
44. Masliah E, Hansen L, Albright T, Mallory M, Terry RD (1991): Immunoelectron microscopic study of synaptic pathology in Alzheimer's disease. Acta Neuropathol 81:428-433.
45. Mattson MP, Dou P, Kater SB (1988): Outgrowth-regulating actions of glutamate in isolated hippocampal pyramidal neurons. J Neurosci 8:2087-2100.
46. Mattson MP, Rychlik B, You JS, Sisken JE (1991): Sensitivity of cultured human embryonic cerebral cortical neurons to excitatory amino acid-induced calcium influx and neurotoxicity. Brain Res 542:97-106.
47. Matus A (1988): Microtubule-associated proteins: their potential role in the developing brain. Annu Rev Neurosci 11:29-14.
48. Okada Y, Sato-Yoshitabe R, Hirokawa N (1995): The activation of protein kinase A selectively inhibits anterograde axonal transport of vesicles but not mitochondria transport or retrograde transport in vivo. J Neurosci 15:3053-3064.
49. Papasozomenos SC, Su Y (1995): Rapid dephosphorylation of t in heat-shocked fetal rat cerebral explants: prevention and hyperphosphorylation by inhibitors of protein phosphatases PP1 and PP2A. J Neurochem 65:396-406.
50. Petrucci TC, Morrow JS (1987): Synapsin I: an actin-bundling protein under phosphorylation control. J Cell Biol 105:1355-1363.
51. Pieribone VA, Shupliakov O, Bridin L, Hilfiker-Rothenfluh S, Czernik AJ, Greengard P (1995): Distinct pool of synaptic vesicles in neurotransmitter release. Nature 375:493-497.
52. Robinson PJ, Liu JP, Powell KA, Fykse EM, Südhof TC (1994): Phosphorylation of dynamin and synaptic-vesicle recycling. Trends Neurosci 17:348-352.
53. Sacher MG, Athlan ES, Mushynsky WE (1992): Okadaic acid induces the rapid and reversible disruption of the neurofilament network in dorsal root ganglion neurons. Biochem Biophys Res Commun 186:524-530.
54. Shea TB, Paskevich PA, Beerman ML (1993): The protein phosphatase inhibitor okadaic acid increases axonal neurofilaments and neurite caliber, and decreases axonal microtubules in NB2a/d1 cells. J Neurosci Res 35:507-521.
55. Takei K, McPerson PS, Schimid SL, De Camilli P (1995): Tubular membrane invaginations coated by dynamin rings are induced by GTP-γS in nerve terminals. Nature 374:186-190.
56. Terry RD, Masliah E, Salmon D, Butters N, DeTeresa R, Hill R, Hansen L, Katzman R (1990): Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 30:572-580.
57. Towbin M, Staehelin T, Gordon J (1979): Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedures and some applications. Proc Natl Acad Sci USA 76:4350-4354.
58. Whitson JS, Selkoe DJ, Cotman CW (1989): Amyloid β protein enhances the survival of hippocampal neurons in vitro. Science 243:1488-1490.
59. 2+, calmodulin-dependent regulation of microtubule formation via phosphorylation of microtubule-associated protein 2, tau factor, and tubulin, and comparison with the cyclic AMP dependent phosphorylation. J Neurochem 44:759-768.
60. Yankner BA (1996): Mechanismis of neuronal degeneration in Alzheimer's disease. Neuron 16:921-932.