Regulation of myelin basic protein phosphorylation by mitogen-activated protein kinase during increased action potential firing in the hippocampus

Journal of Neurochemistry

Volumn 73, Issue 3, 1999, Pages 1090-1097

  Atkins, Coleen M ^a   Yon, M ^b   Groome, N P ^b   Sweatt, J David ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b OXFORD BROOKES UNIVERSITY   (United Kingdom)

Author keywords

Action potential; Alveus; Hippocampus; Mitogen activated protein kinase; Myelin basic protein; Phosphorylation; Reactive nitrogen species; Reactive oxygen species

Indexed keywords

CATALASE; MITOGEN ACTIVATED PROTEIN KINASE; MYELIN BASIC PROTEIN; N(G) NITROARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; SUPEROXIDE DISMUTASE; TETRODOTOXIN;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; EXTRACELLULAR CALCIUM; HIPPOCAMPUS; IMMUNOBLOTTING; INFORMATION PROCESSING; MULTIPLE SCLEROSIS; MYELIN SHEATH; MYELINATION; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM;

ACTION POTENTIALS; ANIMALS; ANTIBODIES; BLOTTING, WESTERN; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CELL COMMUNICATION; HIPPOCAMPUS; ISOENZYMES; KINETICS; MYELIN BASIC PROTEINS; NEUROGLIA; NEURONS; PHOSPHORYLATION; RATS; REACTIVE OXYGEN SPECIES; THREONINE;

EID: 0032840879     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0731090.x     Document Type: Article

References (51)

1. Atkins C. M., Chen S.-J., Klann E., and Sweatt J. D. (1997) Increased phosphorylation of myelin basic protein during hippocampal long-term potentiation. J. Neurochem. 68, 1960-1967.
2. - in vascular smooth muscle cells. Circ. Res. 77, 29-36.
3. Beniac D. R., Luckevich M. D., Czarnota G. J., Tompkins T. A., Ridsdale R. A., Ottensmeyer F. P., Moscarello M. A., and Harauz G. (1997) Three-dimensional structure of myelin basic protein. I. Reconstruction via angular reconstitution of randomly oriented single particles. J. Biol. Chem. 272, 4261-4268.
4. Böhme G. A., Bon C., Stutzmann J.-M., Doble A., and Blanchard J.-C. (1991) Possible involvement of nitric oxide in long-term potentiation. Eur. J. Pharmacol. 199, 379-381.
5. Brady G. W., Fein D. B., Wood D. D., and Moscarello M. A. (1985) The role of charge microheterogeneity of human myelin basic protein in the formation of phosphatidylglycerol multilayers. Biochem. Biophys. Res. Commun. 126, 1161-1165.
6. Campagnoni A. T. and Magno C. S. (1974) Molecular weight estimation of mouse and guinea-pig myelin basic proteins by polyacrylamide gel electrophoresis in the presence of sodium dodecyl sulphate: influence of ionic strength. J. Neurochem. 23, 887-890.
7. Cheifetz S. and Moscarello M. A. (1985) Effect of bovine basic protein charge microheterogeneity on protein-induced aggregation of unilamellar vesicles containing a mixture of acidic and neutral phospholipids. Biochemistry 24, 1909-1914.
8. Cheifetz S., Boggs J. M., and Moscarello M. A. (1985) Increase in vesicle permeability mediated by myelin basic protein: effect of phosphorylation of basic protein. Biochemistry 24, 5170-5175.
9. Chetkovich D. M., Klann E., and Sweatt J. D. (1993) Nitric oxide synthase-independent long-term potentiation in area CA1 of hippocampus. Neuroreport 4, 919-922.
10. De Vente J., Hopkins D. A., Markerink-Van Ittersum M., Emson P. C., Schmidt H. H., and Steinbusch H. W. (1998) Distribution of nitric oxide synthase and nitric oxide-receptive, cyclic GMP-producing structures in the rat brain. Neuroscience 87, 207-241.
11. Dinerman J. L., Dawson T. M., Schell M. J., Snowman A., and Snyder S. H. (1994) Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc. Natl. Acad. Sci. USA 91, 4214-4218.
12. Edwards A. M., Ross N. W., Ulmer J. B., and Braun P. E. (1989) Interaction of myelin basic protein and proteolipid protein. J. Neurosci. Res. 22, 97-102.
13. Erickson A. K., Payne D. M., Martino P. A., Rossomando A. J., Shabanowitz J., Weber M. J., Hunt D. F., and Sturgill T. W. (1990) Identification by mass spectrometry of threonine 97 in bovine myelin basic protein as a specific phosphorylation site for mitogen-activated protein kinase. J. Biol. Chem. 265, 19728-19735.
14. Fialkow L., Chan C. K., Rotin D., Grinstein S., and Downey G. P. (1994) Activation of the mitogen-activated protein kinase signaling pathway in neutrophils. Role of oxidants. J. Biol. Chem. 269, 31234-31242.
15. 2. Role in cell survival following oxidant injury. J. Biol. Chem. 271, 4138-4142.
16. Haley J. E., Wilcox G. L., and Chapman P. F. (1992) The role of nitric oxide in hippocampal long-term potentiation. Neuron 8, 211-216.
17. Halliwell B. and Gutteridge J. M. C. (1989) Free Radicals in Biology and Medicine, 2nd edit. Oxford University Press, New York.
18. Kanterewicz B. I., Knapp L. T., and Klann E. (1998) Stimulation of p42 and p44 mitogen-activated protein kinases by reactive oxygen species and nitric oxide in hippocampus. J. Neurochem. 70, 1009-1016.
19. Kim Y. S. and Kim S. U. (1991) Oligodendroglial cell death induced by oxygen radicals and its protection by catalase. J. Neurosci. Res. 29, 100-106.
20. Klann E., Roberson E. D., Knapp L. T., and Sweatt J. D. (1998) A role for superoxide in protein kinase C activation and induction of long-term potentiation. J. Biol. Chem. 273, 4516-4522.
21. Knapp L. T. and Klann E. (1997) Regulation of PKC and LTP by reactive oxygen species. Soc. Neurosci. Abstr. 23, 1394.
22. Mackenzie-Graham A. J., Mitrovic B., Smoll A., and Merrill J. E. (1994) Differential sensitivity to nitric oxide in immortalized, cloned murine oligodendrocyte cell lines. Dev. Neurosci. 16, 162-171.
23. Mendelson K. G., Contois L. R., Tevosian S. G., Davis R. J., and Paulson K. E. (1996) Independent regulation of JNK/p38 mitogen-activated protein kinases by metabolic oxidative stress in the liver. Proc. Natl. Acad. Sci. USA 93, 12908-12913.
24. Milner B., Squire L. R., and Kandel E. R. (1998) Cognitive neuroscience and the study of memory. Neuron 20, 445-468.
25. Mitrovic B., Ignarro L. J., Montestruque S., Smell A., and Merrill J. E. (1994) Nitric oxide as a potential pathological mechanism in demyelination: its differential effects on primary glial cells in vitro. Neuroscience 61, 575-585.
26. Monuki E. S. and Lemke G. (1995) Molecular biology of myelination, in The Axon (Waxman S. G., Kocsis J. D., and Stys P. K., eds), pp. 144-163. Oxford University Press, New York.
27. Murray N. and Steck A. J. (1983) Depolarizing agents regulate the phosphorylation of myelin basic protein in rat optic nerves. J. Neurochem. 41, 543-548.
28. Murray N. and Steck A. J. (1984) Impulse conduction regulates myelin basic protein phosphorylation in rat optic nerve. J. Neurochem. 43, 243-248.
29. O'Dell T. J., Hawkins R. D., Kandel E. R., and Arancio O. (1991) Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc. Natl. Acad. Sci. USA 88, 11285-11289.
30. Pou S., Pou W. S., Bredt D. S., Snyder S. H., and Rosen G. M. (1992) Generation of superoxide by purified brain nitric oxide synthase. J. Biol. Chem. 267, 24173-24176.
31. Redford E. J., Kapoor R., and Smith K. J. (1997) Nitric oxide donors reversibly block axonal conduction: demyelinated axons are especially susceptible. Brain 120, 2149-2157.
32. Ridsdale R. A., Beniac D. R., Tompkins T. A., Moscarello M. A., and Harauz G. (1997) Three-dimensional structure of myelin basic protein. II. Molecular modeling and considerations of predicted structures in multiple sclerosis. J. Biol. Chem. 272, 4269-4275.
33. Roach A., Boylan K., Horvath S., Prusiner S. B., and Hood L. E. (1983) Characterization of cloned cDNA representing rat myelin basic protein: absence of expression in brain of shiverer mutant mice. Cell 34, 799-806.
34. Roberson E. D. and Sweatt J. D. (1996) Transient activation of cyclic AMP-dependent protein kinase during long-term potentiation. J. Biol. Chem. 271, 30436-30441.
35. mpk. FEBS Lett. 273, 223-226.
36. Schuman E. M. and Madison D. V. (1994) Locally distributed synaptic potentiation in the hippocampus. Science 263, 532-536.
37. Shine H. D., Readhead C., Popko B., Hood L., and Sidman R. L. (1992) Morphometric analysis of normal, mutant, and transgenic CNS: correlation of myelin basic protein expression to myelinogenesis. J. Neurochem. 58, 342-349.
38. Smith R. (1982) Self-association of myelin basic protein: enhancement by detergents and lipids. Biochemistry 21, 2697-2701.
39. Sontheimer H. (1994) Voltage-dependent ion channels in glial cells. Glia 11, 156-172.
40. Stariha R. L., Kikuchi S., Siow Y. L., Pelech S. L., Kim M., and Kim S. U. (1997) Role of extracellular signal-regulated protein kinases 1 and 2 in oligodendroglial process extension. J. Neurochem. 68, 945-953.
41. 2 stimulate mitogen-activated protein kinase activity in NIH-3T3 cells through the formation of reactive oxygen intermediates. Cancer Res. 54, 12-15.
42. Ulmer J. B. (1988) The phosphorylation of myelin proteins. Prog. Neurobiol. 31, 241-259.
43. Ulmer J. B. and Braun P. E. (1983) In vivo phosphorylation of myelin basic proteins in developing mouse brain: evidence that phosphorylation is an early event in myelin formation. Dev. Neurosci. 6, 345-355.
44. Vartanian T., Szuchet S., Dawson G., and Campagnoni A. T. (1986) Oligodendrocyte adhesion activates protein kinase C-mediated phosphorylation of myelin basic protein. Science 234, 1395-1398.
45. Villegas J. (1972) Axon-Schwann cell interaction in the squid nerve fibre. J. Physiol. (Lond.) 225, 275-296.
46. Waxman S. G. and Ritchie J. M. (1993) Molecular dissection of the myelinated axon. Ann. Neurol. 33, 121-136.
47. Wendland B., Schweizer F. E., Ryan T. A., Nakane M., Murad F., Scheller R. H., and Tsien R. W. (1994) Existence of nitric oxide synthase in rat hippocampal pyramidal cells. Proc. Natl. Acad. Sci. USA 91, 2151-2155.
48. Xia Y., Dawson V. L., Dawson T. M., Snyder S. H., and Zweier J. L. (1996) Nitric oxide synthase generates superoxide and nitric oxide in arginine-depleted cells leading to peroxynitrite-mediated cellular injury. Proc. Natl. Acad. Sci. USA 93, 6770-6774.
49. 98. J. Neuroimmunol. 58, 121-129.
50. Yon M., Ackerley C. A., Mastronardi F. G., Groome N., and Moscarello M. A. (1996) Identification of a mitogen-activated protein kinase site in human myelin basic protein in situ. J. Neuroimmunol. 65, 55-59.
51. 97-Pro in brain myelin basic protein: evidence for Thr-Pro and Ser-Arg-X-X-Ser as consensus sequence motifs. J. Neurochem. 62, 1596-1603.