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

Journal of Neurochemistry

Volumn 72, Issue 2, 1999, Pages 491-499

  Sihag, Ram K ^a,b   Jaffe, Howard ^a   Nixon, Ralph A ^b   Rong, Xianhui ^b  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b MCLEAN HOSPITAL   (United States)

Author keywords

Mass spectrometry; Neurofilament protein; Phosphopeptides; Phosphorylation; Protein kinase A

Indexed keywords

CASEIN KINASE II; CHYMOTRYPSIN A; CYCLIC AMP DEPENDENT PROTEIN KINASE; NEUROFILAMENT PROTEIN; PHOSPHORUS 32; PROTEIN KINASE C; PROTEIN SUBUNIT; SERINE; SYNTHETIC PEPTIDE; THREONINE;

AMINO TERMINAL SEQUENCE; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MOLECULAR WEIGHT; MOUSE; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SPINAL CORD;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CYCLIC AMP-DEPENDENT PROTEIN KINASES; MASS SPECTROMETRY; MICE; MOLECULAR SEQUENCE DATA; NEUROFILAMENT PROTEINS; PHOSPHOPEPTIDES; PHOSPHORYLATION; PROTEIN KINASE C; SECOND MESSENGER SYSTEMS; SERINE; SPINAL CORD;

EID: 0032901910     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.0720491.x     Document Type: Article

References (32)

1. Betts J. C., Blackstock W. P., Ward M. A., and Anderton B. H. (1997) Identification of phosphorylation sites on neurofilament proteins by nanoelectrospray mass spectrometry. J. Biol. Chem. 272, 12922-12927.
2. Carden M. J., Schlaepfer W. W., and Lee V. M.-Y. (1985) The structure, biochemical properties, and immunogenicity of neurofilament peripheral regions are determined by phosphorylation state. J. Biol. Chem. 260, 9805-9817.
3. 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.
4. De Jongh K. S., Rotman E. I., and Murphy B. J. (1993) The identification of phosphorylation sites in large membrane proteins following their isolation by SDS-PAGE, in Techniques in Protein Chemistry IV (Angeletti R. H., ed), pp. 45-51. Academic Press, San Diego.
5. Geisler N., Vanderkerchove J., and Weber K. (1987) Location and sequence characterization of the major phosphorylation sites of the high molecular mass neurofilament proteins M and H. FEBS Lett. 221, 403-407.
6. 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.
7. 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.
8. Hisanaga S.-I., 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.
9. Jaffe H., Veerana V., Shetty K. T., and Pant H. C. (1998) Characterization of the phosphorylation sites of human high molecular weight neurofilament protein by electrospray ionization tandem mass spectrometry and database searching. Biochemistry 37, 3931-3946.
10. Julien J.-P. and Mushynski W. E. (1982) Multiple phosphorylation sites in mammalian neurofilament polypeptides. J. Biol. Chem. 257, 10467-10470.
11. Julien J.-P. and Mushynski W. E. (1983) The distribution of phosphorylation sites among identified proteolytic fragments of mammalian neurofilaments. J. Biol. Chem. 258, 4019-4025.
12. Lee V. M.-Y., Otvos L., Carden M. J., Hollosi M., Dietzschold B., and Lazzarini R. A. (1988) Identification of the major multiphosphorylation site in mammalian neurofilaments. Proc. Natl. Acad. Sci. USA 85, 1998-2002.
13. Levy E., Liem R. K. H., D'Eustachio P., and Cowan N. J. (1987) Structure and evolutionary origin of the gene encoding mouse NF-M, the middle-molecular-mass neurofilament protein. Eur. J. Biochem. 166, 71-77.
14. Meyer H. E., Hoffmann-Posorske E., Korte H., and Heilmeyer M. G. Jr. (1986) Sequence analysis of phosphoserine-containing peptides. Modification of picomolar sensitivity. FEBS Lett. 204, 61-66.
15. Nixon R. A. and Sihag R. K. (1991) Neurofilament phosphorylation: a new look at regulation and function. Trends Neurosci. 14, 501-506.
16. Pappin D. J. C., Coull J. M., and Koester H. (1990) Solid-phase sequence analysis of proteins electroblotted or spotted onto polyvinylidene difluoride membranes. Anal. Biochem. 187, 10-19.
17. Parten B. F., McDowell J. H., Nawrocki J. P., and Hargrave P. A. (1994) Characterization of phosphorylation sites in bovine rhodopsin using modified gas phase sequencing programs, in Techniques in Protein Chemistry V (Crabb J. W., ed), pp. 159-167. Academic Press, San Diego.
18. Pearson R. B. and Kemp B. E. (1991) Protein kinase phosphorylation sites sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200, 62-81.
19. 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.
20. Schägger H. and von Jagow G. (1987) Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range 1 to 100 kDa. Anal. Biochem. 166, 368-376.
21. Sihag R. K. (1996) Supramolecular organization of neuronal cytoskeleton is regulated by protein phosphorylation. (Abstr.) Mol. Biol. Cell 7, 384a.
22. Sihag R. K. (1998) Brain β-spectrin phosphorylation: phosphate analysis and identification of threonine-347 as a heparin-sensitive protein kinase phosphorylation site. J. Neurochem. 71, 2220-2228.
23. Sihag R. K. and Cataldo A. M. (1996) Brain β-spectrin is an integral component of senile plaques in Alzheimer's disease. Brain Res. 743, 249-257.
24. 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.
25. Sihag R. K. and Nixon R. A. (1990) Phosphorylation of the amino-terminal head domain of the middle molecular mass 145 kDa subunit of neurofilaments: evidence for regulation by second messenger-dependent protein kinases. J. Biol Chem. 265, 4166-4171.
26. 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.
27. Sihag R. K. and Nixon R. A. (1993) Site-specific rapid turnover of amino-terminal phosphate groups on the NF-M subunit of neurofilaments during axonal transport. (Abstr.) Mol. Biol. Cell 4, 174a.
28. Sihag R. K., Jeng A. Y., and Nixon R. A. (1988) Phosphorylation of neurofilament proteins by protein kinase. C. FEBS Lett. 233, 181-185.
29. Sihag R. K., Jaffe H., Nixon R. A., and Rong X. (1997) Serine-23 is a major protein kinase A phosphorylation site on the amino-terminal head domain of neurofilaments. (Abstr.) Mol. Biol. Cell 7, 384a.
30. Streifel T. D., Avalos R. T., and Cohlberg J. A. (1996) cAMP-dependent phosphorylation of neurofilament proteins NF-L and NF-M inhibits their coassembly into filaments in vitro. Biochem. Biophys. Res. Commun. 222, 646-651.
31. Xu Z., Liu W. S., and Willard M. B. (1992) Identification of six phosphorylation sites in the COOH-terminal tail region of the rat neurofilament protein M. J. Biol. Chem. 267, 4467-4471.
32. Yates J. R. III, Eng J. K., McCormack A. L., and Schieltz D. (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal. Chem. 67, 1426-1436.