Major phosphorylation site (Ser55) of neurofilament L by cyclic AMP- dependent protein kinase in rat primary neuronal culture

Journal of Neurochemistry

Volumn 74, Issue 3, 2000, Pages 949-959

  Nakamura, Yu ^a   Hashimoto, Ryota ^a   Kashiwagi, Yujiro ^a   Aimoto, Saburo ^b   Fukusho, Eriko ^a   Matsumoto, Naohiko ^a   Kudo, Takashi ^a   Takeda, Masatoshi ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Cyclic AMP dependent protein kinase; Matrix assisted laser desorption and ionization; Neurofilament; Neurofilament L; Neuronal culture; Okadaic acid; Phosphorylation

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; FORSKOLIN; MAGNESIUM CHLORIDE; OKADAIC ACID; SEROTONIN; TRYPSIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSKELETON; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; IONIZATION; MASS SPECTROMETRY; NERVE CELL CULTURE; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; STOICHIOMETRY;

AMINO ACID SEQUENCE; ANIMALS; CATTLE; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME INHIBITORS; FORSKOLIN; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; NEUROFILAMENT PROTEINS; NEURONS; OKADAIC ACID; PEPTIDE FRAGMENTS; PHOSPHATES; PHOSPHORYLATION; RATS;

ANIMALIA; BOVINAE;

EID: 0033951171     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2000.0740949.x     Document Type: Article

References (41)

1. Amano M., Chihara K., Kimura K., Fukata Y., Nakamura N., Matsuura Y., and Kaibuchi K. (1997) Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275, 1308-1311.
2. Angelides K. J., Smith K. E., and Takeda M. (1989) Assembly and exchange of intermediate filament proteins of neurons: neurofilaments are dynamic structures. J. Cell Biol. 108, 1495-1506.
3. Brewer G. J., Torricelli J. R., Evege E. K., and Price P. J. (1993) Optimized survival of hippocampal neurons in B27-supplemented Neurobasal, a new serum-free medium combination. J. Neurosci. Res. 35, 567-576.
4. 2+ in cultured cortical neurons. Neuron 11, 751-757.
5. Chou Y. H., Bischoff J. R., Beach D., and Goldman R. D. (1990) Intermediate filament reorganization during mitosis is mediated by p34cdc2 phosphorylation of vimentin. Cell 62, 1063-1071.
6. Cleverley K. E., Betts J. C., Blackstock W. P., Gallo J. M., and Anderton B. H. (1998) Identification of novel in vitro PKA phosphorylation sites on the low and middle molecular mass neurofilament subunits by mass spectrometry. Biochemistry 37, 3917-3930.
7. Dosemeci A. and Pant H. C. (1992) Association of cyclic-AMP-dependent protein kinase with neurofilaments. Biochem. J. 282, 477-481.
8. Geisler N. and Weber K. (1988) Phosphorylation of desmin in vitro inhibits formation of intermediate filaments; identification of three kinase A sites in the aminoterminal head domain. EMBO J. 7, 15-20.
9. Giasson B. I. and Mushynski W. E. (1997) Okadaic acid reversibly inhibits neurite outgrowth in embryonic dorsal root ganglion neurons. J. Neurobiol. 32, 193-201.
10. Giasson B. I. and Mushynski W. E. (1998) Intermediate filament disassembly in cultured dorsal root ganglion neurons is associated with amino-terminal head domain phosphorylation of specific subunits. J. Neurochem. 70, 1869-1875.
11. 2 in the low-molecular-mass neurofilament subunit. J. Neurochem. 66, 1207-1213.
12. 55 mutants in transfected mammalian cells. J. Neurochem. 66, 1306-1311.
13. Gibb B. J. M., Brion J.-P., Brownlees J,. Anderton B. H., and Miller C. C. J. (1998) Neuropathological abnormalities in transgenic mice harbouring a phosphorylation mutant neurofilament transgene. J. Neurochem. 70, 492-500.
14. Gonda Y., Nishizawa K., Ando S., Kitamura S., Minoura Y., Nishi Y., and Inagaki M. (1990) Involvement of protein kinase C in the regulation of assembly-disassembly of neurofilaments in vitro. Biochem. Biophys. Res. Commun. 167, 1316-1325.
15. Hall G. F. and Kosik K. S. (1993) Axotomy-induced neurofilament phosphorylation is inhibited in situ by microinjection of PKA and PKC inhibitors into identified lamprey neurons. Neuron 10, 613-625.
16. Hashimoto R., Nakamura Y., Goto H., Wada Y., Sakoda S., Kaihuchi K., Inagaki M., and Takeda M. (1998) Domain- and site-specific phosphorylation of bovine NF-L by Rho-associated kinase. Biochem. Biophys. Res. Commun. 245, 407-411.
17. Heald R. and McKeon F. (1990) Mutations of phosphorylation sites in lamin A that prevent nuclear lamina disassembly in mitosis. Cell 61, 579-589.
18. Hisanaga S., Gonda Y., Inagaki M., Ikai A., and Hirokawa N. (1990) Effects of phosphorylation of the neurofilament L protein on filamentous structures. Cell Regul. 1, 237-248.
19. Hisanaga S., Matsuoka Y., Nishizawa K., Saito T., Inagaki M., and Hirokawa N. (1994) Phosphorylation of native and reassembled neurofilaments composed of NF-L, NF-M, and NF-H by the catalytic subunit of cAMP-dependent protein kinase. Mol. Biol. Cell 5, 161-172.
20. Inagaki M., Nishi Y., Nishizawa K., Matsuyama M., and Sato C. (1987) Site-specific phosphorylation induces disassembly of vimentin filaments in vitro. Nature 328, 649-652.
21. Inagaki M., Inagaki N., Takahashi T., and Takai Y. (1997) Phosphorylation-dependent control of structures of intermediate filaments: a novel approach using site- and phosphorylation state-specific antibodies. J. Biochem. (Tokyo) 121, 407-414.
22. Kashiwagi Y., Nakamura Y., Miyamae Y., Hashimoto R., and Takeda M. (1998) Pulse exposure of cultured rat neurons to aluminummaltol affected the axonal transport system. Neurosci. Lett. 252, 5-8.
23. Kato H., Gotoh H., Kajikawa M., and Suto K. (1998) Depolarization triggers intracellular magnesium surge in cultured dorsal root ganglion neurons. Brain Res. 779, 329-333.
24. Lelong I. H., Petegnief V., and Rebel G. (1992) Neuronal cells mature faster on polyethyleneimine coated plates than on polylysine coated plates. J. Neurosci. Res. 32, 562-568.
25. Nakamura Y., Takeda M., Angelides K. J., Tanaka T., Tada K., and Nishimura T. (1990) Effect of phosphorylation on 68 KDa neurofilament subunit protein assembly by the cyclic AMP dependent protein kinase in vitro. Biochem. Biophys. Res. Commun. 169, 744-750.
26. Nakamura Y., Takeda M., Angelides K. J., Tada K., Hariguchi S., and Nishimura T. (1991) Assembly, disassembly, and exchange of glial fibrillary acidic protein. Glia 4, 101-110.
27. Nakamura Y., Takeda M., Aimoto S., Hojo H., Takao T., Shimonishi Y., Hariguchi S., and Nishimura T. (1992) Assembly regulatory domain of glial fibrillary acidic protein. A single phosphorylation diminishes its assembly-accelerating property. J. Biol. Chem. 267, 23269-23274.
28. Nakamura Y., Takeda M., Aimoto S., Hariguchi S., Kitajima S., and Nishimura T. (1993) Acceleration of bovine neurofilament L assembly by deprivation of acidic tail domain. Eur. J. Biochem. 212, 565-571.
29. Nakamura Y., Takeda M., and Nishimura T. (1996) Dynamics of bovine glial fibrillary acidic protein phosphorylation. Neurosci. Lett. 205, 91-94.
30. Nakamura Y., Hashimoto R., Kashiwagi Y., Wada Y., Sakoda S., Miyamae Y., Kudo T., and Takeda M. (1999) Casein kinase II is responsible for phosphorylation of NF-L at Ser-473. FEBS Lett. 455, 83-86.
31. Newport J. and Spann T. (1987) Disassembly of the nucleus in mitotic extracts: membrane vesicularization, lamin disassembly, and chromosome condensation are independent processes. Cell 48, 219-230.
32. Nishizawa K., Yano T., Shibata M., Ando S., Saga S., Takahashi T., and Inagaki M. (1991) Specific localization of phosphoimermediate filament protein in the constricted area of dividing cells. J. Biol. Chem. 266, 3074-3079.
33. Peter M., Nakagawa I., Doree M., Labbe J. C., and Nigg E. A. (1990) In vitro disassembly of the nuclear lamina and M phase-specific phosphorylation of lamins by cdc2 kinase. Cell 61, 591-602.
34. Sacher M. G., Athlan E. S., and Mushynski W. E. (1992) Okadaic acid induces the rapid and reversible disruption of the neurofilament network in rat dorsal root ganglion neurons. Biochem. Biophys. Res. Commun. 186, 524-530.
35. Sacher M. G., Athlan E. S., and Mushynski W. E. (1994) Increased phosphorylation of the amino-terminal domain of the low molecular weight neurofilament subunit in okadaic acid-treated neurons. J. Biol. Chem. 269, 18480-18484.
36. Saito T., Shima H., Osawa Y., Nagao M., Hemmings B. A., Kishimoto T., and Hisanaga S. (1995) Neurofilament-associated protein phosphatase 2A: its possible role in preserving neurofilaments in filamentous states. Biochemistry 34, 7376-7384.
37. Shea T. B., Paskevich P. A., and Beermann M. L. (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.
38. Sihag R. K. and Nixon R. A. (1989) In vivo phosphorylation of distinct domains of the 70 kilodalton neurofilament subunit involves different protein kinases. J. Biol. Chem. 264, 457-464.
39. Sihag R. K. and Nixon R. A. (1991) Identification of Ser-55 as a major protein kinase A phosphorylation site on the 70 kDa subunit of neurofilaments. Early turnover during axonal transport. J. Biol. Chem. 266, 18861-18867.
40. Sihag R. K., Jaffe H., Nixon R. A., and Rong X. (1999) Serine-23 is a major protein kinase A phosphorylation site on the amino-terminal head domain of the middle molecular mass subunit of neurofilament proteins. J. Neurochem. 72, 491-499.
41. Tan Y., Rouse J., Zhang A., Cariati S., Cohen P., and Comb M. J. (1996) FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase 2. EMBO J. 15, 4629-4642.