Identification of Ser-Pro and Thr-Pro phosphorylation sites in chicken neurofilament-M tail domain

Journal of Neurochemistry

Volumn 68, Issue 2, 1997, Pages 534-543

  Bennett, Gudrun S ^a,b   Quintana, Ricardo ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF FLORIDA HEALTH   (United States)

Author keywords

Intermediate filaments; Neurofilaments; Phosphorylation; Protein kinase

Indexed keywords

NEUROFILAMENT PROTEIN;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CHICKEN; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SENSORY NERVE CELL;

EID: 0031030438     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1997.68020534.x     Document Type: Article

References (50)

1. Beaudette K. N., Lew J., and Wang J. H. (1993) Substrate specificity characterization of a cdc2-like protein kinase purified from bovine brain. J. Biol. Chem. 268, 20825-20830.
2. Bennett G. S. and DiLullo C. (1985) Slow posttranslational modification of a neurofilament protein. J. Cell Biol. 100, 1799-1804.
3. Bennett G. S., Laskowska D., and DiLullo C. (1991) Lithium chloride inhibits the phosphorylation of newly synthesized neurofilament protein, NF-M, in cultured chick sensory neurons. J. Neurochem. 57, 120-129.
4. Bennett G. S., Basu U., Hollander B. A., Quintana R., and Rodriguez R. (1994) Differential sensitivity to inhibitors discriminates between two types of kinases responsible for in vivo phosphorylation of different sites in the carboxy-terminal tail of chicken neurofilament-M. Mol. Cell. Neurosci. 5, 358-368.
5. 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.
6. Chertoff R., Soussan L., Roder H., and Michaelson D. M. (1995) Phosphorylation and dephosphorylation of distinct isoforms of the heavy neurofilament protein NF-H. Cell. Mol. Neurobiol. 15, 269-280.
7. mPk, the meiosis-activated myelin basic protein kinase. J. Biol. Chem. 266, 15180-15184.
8. deWaegh S. M., Lee V. M.-Y., and Brady S. T. (1992) Local modulation of neurofilament phosphorylation, axonal Caliber, and slow axonal transport by myelinating Schwann cells. Cell 68, 451-463.
9. Elhanany E., Jaffe H., Link W. T., Sheeley D. M., Gainer H., and Pant H. C. (1994) Identification of endogenously phosphorylated KSP sites in the high-molecular-weight rat neurofilament protein J. Neurochem. 63, 2324-2335.
10. Fliegner K. H. and Liem R. K. H. (1991) Cellular and molecular biology of neuronal intermediate filaments. Int. Rev. Cytol. 131, 109-167.
11. cdc2-like kinases. Biochem. Biophys. Res. Commun. 184, 80-85.
12. Geisler N., Vandekerckhove 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.
13. Gonzalez F. A., Raden D. L., and Davis R. J. (1991) Identification of substrate recognition determinants for human ERK1 and ERK2 protein kinases. J. Biol. Chem. 266, 22159-22163.
14. A (glycogen synthase kinase 3). J. Biol. Chem. 266, 8262-8267.
15. cyclin A) phosphorylates bovine neurofilaments. J. Neurochem. 58, 1365-1371.
16. Hisanaga S. and Hirokawa N. (1990) Dephosphorylation-induced interaction of neurofilaments with microtubules. J. Biol. Chem. 265, 21852-21858.
17. Hisanaga S., Kusubata M., Okumura E., and Kishimoto T. (1991) Phosphorylation of neurofilament H subunit at the tail domain by CDC2 kinase dissociates the association of microtubules. J. Biol. Chem. 266, 21798-21803.
18. Hollander B. A., Ayyub C., Shaw G., and Bennett G. S. (1993) A neurofilament-associated kinase phosphorylates only a subset of sites in the tail of chicken midsize neurofilament protein. J. Neurochem. 61, 2115-2123.
19. Hollander B. A., Bennett G. S., and Shaw G. (1996) Localization of sites in the tail domain of the middle molecular mass neurofilament subunit phosphorylated by a neurofilament-associated kinase and by casein kinase I. J. Neurochem. 66, 412-420.
20. Jones S. M. and Williams R. C. Jr. (1982) Phosphate content of mammalian neurofilaments. J. Biol. Chem. 257, 9902-9905.
21. Julien J.-P. and Mushynski W. E. (1982) Multiple phosphorylation sites in mammalian neurofilament polypeptides. J. Biol. Chem. 257, 10467-10470.
22. Klein P. S. and Melton D. A. (1996) A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA 93, 8455-8459.
23. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
24. Lee M. K. and Cleveland D. W. (1996) Neuronal intermediate filaments Annu. Rev. Neurosci. 19, 187-217.
25. 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.
26. cdc2. J. Biol. Chem. 276, 25922-25926.
27. Link W. T., Dosemici A., Floyd C. C., and Pant H. C. (1993) Bovine neurofilament-enriched preparations contain kinase activity similar to casein kinase I - neurofilament phosphorylation by casein kinase I (CKI). Neurosci. Lett. 151, 89-93.
28. McDowell J. H., Nawrocki J. P., and Hargrave P. A. (1993) Phosphorylation sites in bovine rhodopsin. Biochemistry 32, 4968-4974.
29. Meegio F., Donella Deana A., Ruzzene M., Brunati A. M., Cesaro L., Guerra B., Meyer T., Mett H., Fabbro D., Furet P., Dobrowolska G., and Pinna L. A. (1995) Different susceptibility of protein kinases to staurosporine inhibition: kinetic studies and molecular bases for the resistance of protein kinase CK2. Eur. J. Biochem. 234, 317-322.
30. Meyer H. E., Hoffmann-Posorske E., and Heilmeyer L. M. G. Jr. (1991) Determination and location of phosphoserine in proteins and peptides by conversion to S-ethylcysteine. Methods Enzymol. 201, 169-185.
31. Nakagawa T., Chen J., Zhang Z., Kanai Y., and Hirokawa N. (1995) Two distinct functions of the carboxyl-terminal tail domain of NF-M upon neurofilament assembly: cross-bridge formation and longitudinal elongation of filaments. J. Cell Biol. 129, 411-429
32. Napolitano E. W., Chin S. S., Colman D. R., and Liem R. K. H. (1987) Complete amino acid sequence and in vitro expression of rat NF-M, the middle molecular weight neurofilament protein J. Neurosci. 7, 2590-2599.
33. Nixon R. A. and Sihag R. K. (1991) Neurofilament phosphorylation: a new look at regulation and function. Trends Neurosci. 14, 501-506.
34. Pant H. C. and Veeranna (1995) Neurofilament phosphorylation. Biochem. Cell Biol. 73, 575-592.
35. Paudel H. K., Lew J., Zenobia A., and Wang J. H. (1993) Brain proline-directed protein kinase phosphorylates tau on sites that are abnormally phosphorylated in tau associated with Alzheimer's paired helical filaments. J. Biol. Chem. 268, 23512-23518.
36. Roder H. M. and Ingram V. M. (1991) Two novel kinases phosphorylate tau and the KSP site of heavy neurofilament subunits in high stoichiometric ratios. J. Neurosci. 11, 3325-3343.
37. Shaw G. (1989.) Identification of previously unrecognized sequence motifs at the extreme carboxy terminus of the neurofilament subunit NF-M. Biochem. Biophys. Res. Commun. 162, 294-299.
38. Shaw G. (1991) Neurofilament proteins, in The Neuronal Cytoskeleton (Burgoyne R. D., ed), pp. 185-214. Alan R. Liss, New York.
39. Shetty K. T., Link W. T., and Pant H. C. (1993) cdc2-like kinase from rat spinal cord specifically phosphorylates KSPXK motifs in neurofilament proteins: isolation and characterization. Proc. Natl. Acad. Sci. USA 90, 6844-6848.
40. Sullivan S. and Wong T. W. (1991) A manual sequencing method for identification of phosphorylated amino acids in phosphopeptides. Anal. Biochem. 197, 65-68.
41. Sun D., Leung C. L., and Liem R. K. H. (1996) Phosphorylation of the high molecular weight neurofilament protein (NF-H) by Cdk5 and p35. J. Biol. Chem. 271, 14245-14251.
42. Tanasijevic M. J., Myers M. G. Jr., Thoma R. S., Crimmins D. L., White M. F., and Sacks D. B. (1993) Phosphorylation of the insulin receptor substrate IRS-1 by casein kinase II. J. Biol. Chem. 268, 18157-18166.
43. Veeranna, Shetty K. T., Amin N., Grant P., Albers R. W., and Pant H. C. (1996) Inhibition of neuronal cyclin-dependent kinase-5 by staurosporine and purine analogs is independent of activation by Munc-18. Neurochem. Res. 21, 629-636.
44. Vulliet R., Halloran S. M., Braun R. K., Smith A. J., and Lee G. (1992) Proline-directed phosphorylation of human tau protein. J. Biol. Chem. 267, 22570-22574.
45. Woodgett J. R. (1991) A common denominator linking glycogen metabolism, nuclear oncogenes and development. Trends Biochem. Sci. 16, 177-181.
46. Xu Z.-S., 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.
47. Xu Z., Marszalek J. R., Lee M. K., Wong P. C., Folmer J., Crawford T. O., Hsieh S.-T., Griffin J. W., and Cleveland D. W. (1996) Subunit composition of neurofilaments specifies axonal diameter J. Cell Biol. 133, 1061-1069.
48. 404-Pro that are abnormally phosphorylated in Alzheimer's disease brain. J. Neurochem. 61, 1742-1747.
49. 666 in neurofilament. J. Neurochem. 64, 1848-1854.
50. Zopf D., Dineva B., Betz H., and Gundelfinger E. D. (1990) Isolation of the chicken middle-molecular weight neurofilament (NF-M) gene and characterization of its promoter. Nucleic Acids Res. 18, 521-529.