A quantitative autoradiographic study of [3H]cAMP binding to cytosolic and particulate protein kinase A in post-mortem brain staged for Alzheimer's disease neurofibrillary changes and amyloid deposits

Brain Research

Volumn 818, Issue 2, 1999, Pages 383-396

  Bonkale, W L ^a   Cowburn, R F ^a   Ohm, T G ^b   Bogdanovic, N ^a   Fastbom, J ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Alzheimer's disease; Amyloid deposit; Autoradiography; cAMP dependent protein kinase; Entorhinal cortex; Hippocampus; Human brain; Neuropathological change; Staging

Indexed keywords

AMYLOID; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE;

AGED; ALZHEIMER DISEASE; ARTICLE; AUTORADIOGRAPHY; CLINICAL ARTICLE; CYTOSOL; ENTORHINAL CORTEX; ENZYME BINDING; FEMALE; HIPPOCAMPUS; HUMAN; MALE; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; PRIORITY JOURNAL; STAGING;

AGING; ALZHEIMER DISEASE; AMYLOID; AUTORADIOGRAPHY; BRAIN; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOSOL; DISEASE PROGRESSION; ENTORHINAL CORTEX; HIPPOCAMPUS; HUMANS; NEUROFIBRILLARY TANGLES; PARTICLE SIZE; RADIOLIGAND ASSAY; TRITIUM;

EID: 0033550704     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-8993(98)01307-9     Document Type: Article

References (62)

1. Abel T., Martin K.C., Bartsch D., Kandel E.R. Memory suppressor genes: inhibitory constraints on the storage of long-term memory. Science. 279:1998;338-341.
2. American Psychiatric Association, Committee on Nomenclature and Statistics, Diagnostic and Statistical Manual of Mental Disorders, 3rd edn., revised, American Psychiatric Association, Washington, DC (1987).
3. Arriagada P.V., Growdon J.H., Hedley-Whyte E.T., Hyman B.T. Neurofibrillary tangles but not senile plaques parallel duration and severity of Alzheimer's disease. Neurology. 42:1992;631-639.
4. erk beyond phosphorylation by cAMP-dependent PKA: relation to Alzheimer's disease. Biochem. Biophys. Res. Commun. 200:1994;187-194.
5. Bonkale W.L., Fastbom J., Wiehager B., Ravid R., Winblad B., Cowburn R.F. Impaired G-protein-stimulated adenylyl cyclase activity in Alzheimer's disease is not accompanied by reduced cyclic AMP-dependent protein kinase A activity. Brain Res. 737:1996;155-161.
6. 3H ]cGMP binding sites in the rat brain Brain Res. 763:1997;1-13.
7. Bourbonnière M., Shekarabi M., Nalbantoglu J. Enhanced expression of amyloid precursor protein in response to dibutyryl cyclic AMP is not mediated by the transcription factor AP-2. J. Neurochem. 68:1997;909-916.
8. Bourtchuladze R., Frenguelli B., Blendy J., Cioffi D., Schutz G., Silva A.J. Deficient long-term memory in mice with a targeted mutation of the cAMP-responsive element-binding protein. Cell. 79:1994;59-68.
9. Braak H., Braak E., Grundke-Iqbal I., Iqbal K. Occurrence of neuropil threads in the senile human brain and in Alzheimer's disease: a third location of paired helical filaments outside of neurofibrillary tangles and neuritic plaques. Neurosci. Lett. 65:1986;351-355.
10. Braak H., Braak E. Neuropathological stageing of Alzheimer's-related changes. Acta Neuropathol. 82:1991;239-259.
11. Braak H., Braak E. Evolution of the neuropathology of Alzheimer's disease. Acta Neurol. Scand. 165:1996;3-12.
12. Braak H., Braak E., Yilmazer D., de Vos R.A.I., Jansen E.N.H., Bohl J. Pattern of brain destruction in Parkinson's and Alzheimer's diseases. J. Neural Transm. 103:1996;455-490.
13. 396 in Alzheimer's disease recapitulates development and contributes to reduced microtubule binding. Neurone. 10:1993;1089-1099.
14. Brandon E.P., Zhuo M., Huang Y.-Y., Qi M., Gerhold K.A., Burton K.A., Kandel E.R., McKnight G.S., Idzerda R.L. Hippocampal long-term depression and depotentiation are defective in mice carrying a targeted disruption of the gene encoding the RIβ subunit of cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 92:1995;8851-8855.
15. Challis R.A.J., Willcocks A.L., Mulloy B., Potter B.V.L., Nahorski S.R. Characterization of inositol 1,4,5-triphosphate and 1,3,4,5-tetrakisphosphate-binding sites in rat cerebellum. Biochem. J. 274:1991;861-867.
16. Checler F. Processing of the β-amyloid precursor protein and its regulation in Alzheimer's disease. J. Neurochem. 65:1995;1431-1444.
17. Cleveland D.W., Hwo S.Y., Kirschner M.W. Purification of tau, a microtubule-associated protein that induces assembly of microtubules from purified tubulin. J. Mol. Biol. 116:1977;207-225.
18. Cowburn R.F., O'Neill C., Ravid R., Winblad B., Fowler C.J. Adenylyl cyclase activity in postmortem human brain: evidence of altered G-protein mediation in Alzheimer's disease. J. Neurochem. 58:1992;1409-1419.
19. Cowburn R.F., Fowler C.J., O'Neill C. Neurotransmitters, signal transduction and second messengers in Alzheimer's disease. Acta Neurol. Scand. 165:1996;25-32.
20. Efthimiopoulos S., Punj S., Manolopoulos V., Pangalos M., Wang G.P., Refolo L.M., Robakis N.K. Intracellular cyclic AMP inhibits constitutive and phorbol ester-stimulated secretory cleavage of amyloid precursor protein. J. Neurochem. 67:1996;872-875.
21. Frank D.A., Greenberg M.E. CREB: a mediator of long-term memory from mollusks to mammals. Cell. 79:1994;5-8.
22. Gegelashvili G., Bock E., Schousboe A., Linnemann D. Two types of amyloid precursor protein (APP) mRNA in rat glioma cell lines: upregulation via a cyclic AMP-dependent pathway. Mol. Brain Res. 37:1996;151-156.
23. Goedert M., Crowther R.A., Garner C.C. Molecular characterization of microtubule-associated proteins tau and MAP2. TINS. 14:1991;193-199.
24. Goldenring J.R., Vallano M.L., Delorenzo R.J. Phosphorylation of microtubule-associated protein 2 at distinct sites by calmodulin-dependent and cyclic AMP-dependent kinases. J. Neurochem. 45:1985;900-905.
25. Gómez-Isla T., Price J.L., McKeel D.W., Morris J.C., Growdon J.H., Hyman B.T. Profound loss of layer II entorhinal cortex neurons occurs in very mild Alzheimer's disease. J. Neurosci. 16:1996;4491-4500.
26. Greenberg S.M., Castelluci V.F., Bayley H., Schwartz J.H.A. A molecular mechanism for long-term sensitization in Aplysia. Nature. 329:1987;62-65.
27. Grundke-Iqbal I., Iqbal K., Tung Y.C., Quinlan M., Wisniewski H.M., Binder L.I. Abnormal phosphorylation of the microtubule-associated protein τ (tau) in Alzheimer cytoskeletal pathology. Proc. Natl. Acad. Sci. U.S.A. 83:1986;4913-4917.
28. 3H ]cAMP cyclic AMP: Implications for organization of second messenger systems Neuroscience. 29:1989;695-714.
29. Hardy J.A., Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science. 256:1992;184-185.
30. Hyman B.T., Van Hoesen G.W., Kromer L.J., Damasio A.R. Perforant pathway changes and the memory impairment of Alzheimer's disease. Ann. Neurol. 20:1986;472-481.
31. Hyman B.T., Van Hoesen G.W., Damasio A.R. Memory-related neural systems in Alzheimer's disease. Neurology. 40:1990;1721-1730.
32. Ikezu T., Okamoto T., Komatsuzaki K., Matsui T., Martyn J.J.A., Nishimoto I. Negative transactivation of cAMP response element by familial Alzheimer mutants of APP. EMBO J. 15:1996;2468-2475.
33. Insausti R., Belichenko P.V., Frotscher M., Matus A., Monyer H., Palm G., Steinhäuser C. Plasticity in the entorhinal-hippocampal system. Hippocampus. 3:1993;289-292.
34. 2+/calmodulin-dependent protein kinase II: metabolic and functional consequences. J. Neurochem. 59:1992;2056-2062.
35. Kurumatani T., Fastbom J., Bonkale W.L., Bogdanovic N., Winblad B., Ohm T.G., Cowburn R.F. Loss of inositol 1,4,5-trisphosphate receptor sites and decreased PKC levels correlate with staging of Alzheimer's disease neurofibrillary pathology. Brain Res. 796:1998;209-221.
36. Licameli V., Mattiace L.A., Erlichman J., Davies J., Dickson D., Shafit-Zagardo B. Regional localization of the regulatory subunit (RIIβ) of the type II cAMP-dependent protein kinase in human brain. Brain Res. 578:1992;61-68.
37. Litersky J.M., Johnson G.V.W. Phosphorylation by cAMP-dependent protein kinase inhibits the degradation of tau by calpain. J. Bio. Chem. 267:1992;1563-1568.
38. Litersky J.M., Johnson G.V.W., Jakes R., Goedert M., Lee M., Seubert P. Tau protein is phosphorylated by cyclic AMP-dependent protein kinase and calcium/calmodulin-dependent protein kinase II within its microtubule-binding domains at Ser-262 and Ser-356. Biochem. J. 316:1996;655-660.
39. Lovestone S., Reynolds C.H. The phosphorylation of tau: a critical stage in neurodevelopment and neurodegenerative processes. Neuroscience. 78:1997;309-324.
40. Marambaud P., Wilk S., Checler F. Protein kinase A phosphorylation of the proteasome: a contribution to the α-secretase pathway in human cells. J. Neurochem. 67:1996;2616-2619.
41. McKahn G., Drachman D., Folstein M., Katzman R., Price D., Stadlan E.M. Clinical diagnosis of Alzheimer's disease: report of the NINCDS-ADRA work group under the auspices of Department of Health and Human Services Task Force on Alzheimer's Disease. Neurology. 34:1984;939-944.
42. Meier-Ruge W., Iwangoff P., Reichlmeier K. Neurochemical enzyme changes in Alzheimer's and Pick's disease. Arch. Gerontol. Geriatr. 3:1984;161-165.
43. Ohm T.G., Bohl J., Lemmer B. Reduced basal and stimulated (isoprenaline, Gpp(NH)p, forskolin) adenylate cyclase activity in Alzheimer's disease correlated with histopathological changes. Brain Res. 540:1991;229-236.
44. Ohm T.G. Alterations of signal transduction in the lesioned entorhinal-hippocampal system: a mini-review on Alzheimer's disease-related changes and experimental data. Hippocampus. 3:1993;131-138.
45. Ohm T.G., Braak E., Bohl J., Braak H. A competition between silver-stain and immunocytochemistry. J. Neural Transm. 1:1989;111. P-D section.
46. Ohm T.G., Müller H., Braak H., Bohl J. Close-meshed prevalence rates of different stages as a tool to uncover the rate of Alzheimer's disease-related neurofibrillary changes. Neuroscience. 64:1995;209-217.
47. Ohm T.G., Schmitt M., Bohl J., Lemmer B. Decrease in adenylate cyclase activity antecedes neurofibrillary tangle formation. Neurobiol. Aging. 18:1997;275-279.
48. Qi M., Zhuo M., Skålhegg B.S., Brandon E.P., Kandel E.R., McKnight G.S., Izerda R.L. Impaired hippocampal plasticity in mice lacking the Cβ1 catalytic subunit of cAMP-dependent protein kinase. Proc. Natl. Acad. Sci. U.S.A. 93:1996;1571-1576.
49. M. Rössler, R. Zarski, J. Bohl, T.G. Ohm, Stage-dependent and sector-specific neuronal loss in hippocampi classified for Alzheimer's disease-related neurofibrillary changes, submitted.
50. Rubin C.S., Rangel-Aldao R., Sarkar D., Erlichman J., Fleischer N. Characterization and comparison of membrane-associated and cytosolic cAMP-dependent protein kinases. J. Biol. Chem. 254:1980;3797-3805.
51. Scott C.W., Spreen R.C., Herman J.L., Chow F.P., Davison M.D., Young J., Caputo C.B. Phosphorylation of recombinant tau by cAMP-dependent protein kinase. J. Biol. Chem. 268:1993;1166-1173.
52. Sengupta A., Wu Q., Grundke-Iqbal I., Iqbal K., Singh T.J. Potentiation of GSK-3-catalyzed Alzheimer-like phosphorylation of human tau by Cdk-5. Mol. Cell. Biochem. 167:1997;99-105.
53. Shekarabi M., Bourbonnière M., Dagenais A., Nalbantoglu J. Transcriptional regulation of amyloid precursor protein during dibutyryl cyclic AMP-induced differentiation of NG108-15 cells. J. Neurochem. 68:1997;970-978.
54. Singh T.J., Zaidi T., Grundke-Iqbal I., Iqbal K. Non-proline-dependent protein kinases phosphorylate several sites found in tau from Alzheimer's disease brain. Mol. Cell. Biochem. 154:1996;143-151.
55. Stein J.C., Farooq M., Norton W.T., Rubin C.S. Differential expression of isoforms of the regulatory subunit of the type II cAMP-dependent protein kinase in rat neurons, astrocytes, and oligodendrocytes. J. Biol. Chem. 262:1987;3002-3006.
56. Trinczek B., Schwoch G. Immunoelectron microscopical localization of the catalytic subunit of cAMP-dependent protein kinases in brain microtubules and neurofilaments. FEBS. 277:1990;167-170.
57. van Hoesen G.W., Hyman B.T., Damasio A.R. Entorhinal cortex pathology in Alzheimer's disease. Hippocampus. 1:1991;1-8.
58. Ventra C., Porcellini A., Feliciello A., Gallo A., Paolillo M., Mele E., Avvedimento V.E., Schettini G. The differential response of protein kinase A to cyclic AMP in discrete brain areas correlates with the abundance of regulatory subunit II. J. Neurochem. 66:1996;1752-1761.
59. West M.J., Coleman P.D., Flood D.G., Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet. 344:1994;769-772.
60. West M.J., Slomianka L. Total number of neurons in the layers of human entorhinal cortex. Hippocampus. 8:1998;69-82.
61. Yamamoto M., Ozawa H., Saito T., Frölich L., Riederer P., Takahata N. Reduced immunoreactivity of adenylyl cyclase in dementia of the Alzheimer type. NeuroReport. 7:1996;2965-2970.
62. 214 generates the Alzheimer-specific epitope of antibody AT100 and requires a paired-helical filament-like conformation. Eur. J. Biochem. 252:1998;542-552.