Cyclin dependent kinase-5 (CDK-5) phosphorylates neurofilament heavy (NF-H) chain to generate epitopes for antibodies that label neurofilament accumulations in amyotrophic lateral sclerosis (ALS) and is present in affected motor neurones in ALS

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 23, Issue 5, 1999, Pages 833-850

  Bajaj, Narinder P S ^a   Al Sarraj, Saffa T ^a   Leigh, P Nigel ^a   Anderson, Valerie ^a   Miller, Christopher C J ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Amyotrophic lateral sclerosis (ALS); Apoptosis; Cyclin dependent kinase 5 (cdk 5); Lipofuscin; Neurofilament heavy chain (NF H)

Indexed keywords

CYCLIN DEPENDENT KINASE; NEUROFILAMENT PROTEIN;

ADULT; AGED; AMYOTROPHIC LATERAL SCLEROSIS; APOPTOSIS; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; EPITOPE MAPPING; FEMALE; HUMAN; HUMAN TISSUE; MALE; NEUROFILAMENT; PROTEIN PHOSPHORYLATION;

AGED; AGED, 80 AND OVER; AMINO ACID SEQUENCE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; BLOTTING, WESTERN; COS CELLS; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; DNA PRIMERS; EPITOPE MAPPING; EPITOPES; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; MOTOR NEURONS; NEUROFILAMENT PROTEINS; PEPTIDE FRAGMENTS; PHOSPHORYLATION;

EID: 0033167050     PISSN: 02785846     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0278-5846(99)00044-5     Document Type: Article

References (37)

1. Bajaj, N. P. S. and Miller, C. C. J. (1997) Phosphorylation of neurofilament heavy-chain side-arm fragments by cyclin-dependent kinase-5 and glycogen synthase kinase-3α in transfected cells. J. Neurochem. 69: 737-743.
2. Beaudette, K. N., Lew, J. and Wang, J. H. (1993) Substrate specificity and characterisation of a cdc2-like protein kinase purified from bovine brain. J. Biol. Chem. 268: 20825-20830.
3. Brion, J. P. and Couck, A. M. (1995) Cortical and brain stem-type Lewy bodies are immunoreactive for cyclin-dependent kinase 5. Am. J. Path. 147: 1465-1476.
4. Brunk, U. T., Jone, G. B. and Sohal, R. S. (1992) A novel hypothesis of lipofuscinogenesis and cellular ageing based upon interactions between oxidative stress and autophagocytosis. Mutation Res. 275: 395-403.
5. 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.
6. Giasson, B. I. and Mushynski, W. E. (1996) Aberrant stress-induced phosphorylation of perikaryal neurofilaments. J. Biol. Chem. 271: 30404-30409.
7. Greenlund, L. J. S., Deckwerth, T. L. and Johnson, E. M. (1995) Superoxide dismutase delays neuronal apoptosis: a role for reactive oxygen species in programmed neuronal death. Neuron 14: 303-315.
8. Guidato, S., Bajaj, N. P. S. and Miller, C. C. J. (1996a) Cellular phosphorylation of neurofilament heavy-chain by cyclin dependent kinase-5 masks the epitope for monoclonal antibody N52. Neurosci. Lett. 217: 157-160.
9. Guidato, S., Tsai, L. H., Woodgett, J. and Miller, C. C. J. (1996b) Differential cellular phosphorylation of neurofilament heavy side-arms by glycogen synthase kinase-3 and cyclin-dependent kinase-5. J. Neurochem. 66: 1698-1706.
10. Henchcliffe, C. and Burke, R. E. (1997) Increased expression of cyclin-dependent kinase 5 in induced apoptotic neuron death in rat substantia nigra. Neurosci. Lett. 230: 41-44.
11. Hirokawa, N. (1982) The crosslinker system between neurofilaments, microtubules and membranous organelles revealed by quick freeze, freeze fracture, deep-etching method. J. Cell Biol. 94: 129-142.
12. Hirokawa, N., Glicksman, M. A. and Willard, M. B. (1984) Organisation of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J. Cell Biol. 98: 1523-1536.
13. Hisinaga, S., Ishiguro, K., Uchida, T., Okamura, E., Okano, T. and Kishimoto, T. (1993) Tau protein kinase II has a similar characteristic to cdc2 kinase for phosphorylating neurofilament proteins. J. Biol. Chem. 268: 15056-15060.
14. Julien, J. P., Cote, F., Beaudet, L., Sidky, M. and Flavell, D. (1988) Sequence and structure of the mouse gene coding for the largest neurofilament subunit. Gene 68: 307-314.
15. Lee, M. K. and Cleveland, D. W. (1996) Neuronal intermediate filaments. Ann. Rev. Neurosci. 19: 187-217.
16. Lee, V. M. -Y., Carden, M. J., Schlaepfer, W. W. and Trojanowski, J. Q. (1987) Monoclonal-antibodies distinguish several differentially phosphorylated states of the 2 largest rat neurofilament subunits (NF-H and NF-M) and demonstrate their existence in the normal nervous-system of adult-rats. J. Neurosci. 7: 3474-3488.
17. Leigh, P. N. and Garafolo, O. (1995) The molecular pathology of motor neurone disease. In: Motor Neurone Disease, M. Swash and P.N. Leigh, (Eds.), Springer Verlag, London.
18. Lew, J., Winkfein, R. J., Paudel, H. E. and Wang, J. H. (1992) Brain proline-directed kinase is a neurofilament kinase which displays high sequence homology to p34cdc2. J. Biol. Chem. 36: 25922-25926.
19. Lovestone, S., Reynolds, C. H., Latimer, D., Davis, D. R., Anderton, B. H., Gallo, J. -M., Hanger, D., Mulot, S., Marquardt, B., Stabel, S., Woodgett, J. R. and Miller, C. C. J. (1994) Alzheimer's disease-like phosphorylation of the microtubule-associated protein tau by glycogen synthase kinase-3 in transfected mammalian cells. Curr. Biol. 4: 1077-1086.
20. Migheli, A., Cavalla, P., Piva, R., Giordana, M. T. and Schiffer, D. (1994) bcl-2 protein expression in aged brain and neurodegenerative disease. Neuroreport 5: 1906-1908.
21. Miller, C. C. J., Brion, J. P., Calvert, R., Chin, T. K., Eagles, P. A. M., Downes, M. J., Haugh, M., Kahn, J., Probst, A., Ulrich, J. and Anderton, B. H. (1986) Alzheimer's paired helical filaments share epitopes with neurofilament side arms. EMBO J. 5: 269-276.
22. Miyasaka, H., Okabe, S., Ishiguro, K., Uchida, T. and Hirokawa, N. (1993) Interaction of the tail domain of high molecular weight subunits of neurofilaments with the COOH-terminal region of tubulin and its regulation by tau protein kinase II. J. Biol. Chem. 268: 22695-22702.
23. Mu, X., He, J., Anderson, D. W., Trojanowski, J. Q. and Springer, J. E. (1996) Altered expression of bcl-2 and bax mRNA in amyotrophic lateral sclerosis spinal cord motor neurons. Ann. Neurol. 40: 379-386.
24. Nakamura, S., Kawamoto, Y., Nakano, S., Akiguchi, I. and Kimura, J. (1997a) p35 (nck5a) and cyclin-dependent kinase 5 colocalize in Lewy bodies of brains with Parkinson's disease. Acta Neuropathol. 94: 153-157.
25. Nakamura, S., Kawamoto, Y., Nakano, S., Ikemoto, A., Akiguchi, I. and Kimura, J. (1997b) Cyclin-dependent kinase 5 in Lewy body-like inclusions in anterior horn cells of a patient with sporadic amyotrophic lateral sclerosis. Neurology 48:267-270.
26. Rabizadeh, S., Gralla, E. B., Borchelt, D. R., Gwinn, R., Valentine, J. S., Sisodia, S., Wong, P., Lee, M., Hahn, H. and Bredesen, D. E. (1995) Mutations associated with amyotrophic lateral sclerosis convert superoxide dismutase from an antiapoptotic gene to a proapoptotic gene:studies in yeast and neural cells. Proc. Natl. Acad. Sci. USA 92: 3024-3028.
27. Rosen, D. R., Siddique, T., Patterson, D., Figlewicz, D. A., Sapp, P., Hentati, A., Donaldson, D., Goto, J., Oregan, J. P., Deng, H. X., Rahmani, Z., Krizus, A., Mckennayasek, D., Cayabyab, A., Gaston, S. M., Berger, R., Tanzi, R. E., Halperin, J. J., Herzfeldt, B. Vandenbergh, R., Hung, W. Y., Bird, T., Deng, G., Mulder, D. W., Smyth, C., Laing, N.G., Soriano, E., Pericakvance, M. A., Haines, J., Rouleau, G. A., Gusella, J. S., Horvitz, H. R. and Brown, R. H. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362: 59-62.
28. Shaw, G. (1991) Neurofilament proteins. In: The Neuronal Cytoskeleton, R.D. Burgoyne, (Ed.), pp 185-214, Wiley-Liss, New-York.
29. 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 characterisation. Proc. Natl. Acad. Sci. USA 90: 6844-6848.
30. 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.
31. Trojanowski, J. Q., Schmidt, M. L., Shin, R. W., Bramblett, G. T., Rao, D. and Lee, V. M. -Y. (1993) Altered tau and neurofilament proteins in neurodegenerative diseases: Diagnostic implications for Alzheimer's disease and Lewy body dementias. Brain Pathol. 3: 45-54.
32. Tsai, L. H., Takahashi, T., Caviness, V. S. and Harlow, E. (1993) Activity and expression pattern of cyclin dependent kinase-5 in the embryonic mouse nervous system. Development 119: 1029-1040.
33. Tsai, L. H., Delalle, I., Caviness, V. S., Chae, T. and Harlow, E. (1994) P35 is a neural specific regulatory subunit of cdk-5. Nature 371: 419-423.
34. Tu, P.H., Gurney, M. E., Julien, J. P., Lee, V. M. -Y. and Trojanowski, J. Q. (1997) Oxidative stress, mutant SOD1 and neurofilament pathology in transgenic mouse models of human motor neuron disease. Lab. Invest. 76:441-456.
35. Veeranna, Amin, N. D., Ahn, N. G., Jaffe, H., Winters, C. A., Grant, P. and Pant, H. C. (1998) Mitogen-activated protein kinases (Erk1, 2) phosphorylate lys-ser-pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J. Neurosci. 18: 4008-4021.
36. Xu, Z., Cork, L. C, Griffin, J. W. and Cleveland, D. W. (1993) Involvement of neurofilaments in motor neurone disease. J. Cell Sci. S17: 101-108.
37. Zhang, Q., Ahuja, H. S., Zakeri, Z. F. and Wolgemuth, D. J. (1997) Cyclin-dependent kinase 5 is associated with apoptotic cell death during development and tissue remodeling. Dev. Biol. 183: 222-233.