Cyclin-dependent kinase 5 increases perikaryal neurofilament phosphorylation and inhibits neurofilament axonal transport in response to oxidative stress

Journal of Neuroscience Research

Volumn 76, Issue 6, 2004, Pages 795-800

  Shea, Thomas B ^a   Zheng, Ya Li ^b   Ortiz, Daniela ^a   Pant, Harish C ^b  

^a University of Massachusetts Lowell   (United States)

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

Author keywords

Axonal transport; Cyclin dependent kinase 5; Neurodegeneration; Neurofilament; Oxidative stress; Phosphorylation

Indexed keywords

CYCLIN DEPENDENT KINASE 5; HYDROGEN PEROXIDE; NEUROFILAMENT PROTEIN; PROTEIN SERINE THREONINE KINASE; ROSCOVITINE;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENZYME PHOSPHORYLATION; IMMUNOREACTIVITY; MOTOR NEURON DISEASE; NERVE CELL CULTURE; NEUROFILAMENT; NEUROPATHOLOGY; NONHUMAN; OXIDATIVE STRESS; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPINAL GANGLION;

ANIMALS; AXONAL TRANSPORT; CELLS, CULTURED; CHICK EMBRYO; CYCLIN-DEPENDENT KINASE 5; CYCLIN-DEPENDENT KINASES; GANGLIA, SPINAL; HYDROGEN PEROXIDE; NEUROFILAMENT PROTEINS; NEURONS; OXIDANTS; OXIDATIVE STRESS; PHOSPHORYLATION;

EID: 2642524580     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.20099     Document Type: Article

References (60)

1. Ackerley S, Thornhill P, Grierson AJ, Brownlees J, Anderton BH, Leigh PN, Shaw CE, Miller CC. 2003. Neurofilament heavy chain side arm phosphorylation regulates axonal transport of neurofilaments. J Cell Biol 161:489-495.
2. Al-Chalabi A, Andersen PM, Nilsson P, Chioza B, Andersson JL, Russ C, Shaw CE, Powell JF, Leigh PN. 1999. Deletions of the heavy neurofilament subunit tail in amyotrophic lateral sclerosis. Hum Mol Genet 8:157-164.
3. Anderton BH, Breinburg D, Downes MJ, Green PJ, Tomlinson BE, Ulrich J, Wood JN, Kahn J. 1982. Monoclonal antibodies show that neurofibrillary tangles and neurofilaments share antigenic determinants. Nature 298:84-86.
4. Bajaj NP, Al-Sarraj ST, Leigh PN, Anderson V, Miller CC. 1999. Cyclin dependent kinase 5 (cdk5) 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 neurons in ALS. Prog Neuropsychopharmacol Biol Psychiatry 23:833-850.
5. Brownlees J, Ackerley S, Grierson AJ, Jacobsen NJ, Shea K, Anderton BH, Leigh PN, Shaw CE, Miller CC. 2002. Charcot-Marie-Tooth disease neurofilament mutations disrupt neurofilament assembly and axonal transport. Hum Mol Genet 11:2837-2844.
6. Bu B, Li J, Davies P, Vincent I. 2002. Deregulation of cdkS, hyperphosphorylation and cytoskeletal pathology in the Niemann-Pick type C murine model. J Neurosci 22:6515-6525.
7. Cookson MR, Shaw PJ, 1999. Oxidative stress and motor neurone disease. Brain Pathol 9:165-186.
8. Cote F, Collard JF, Julien JP. 1993. Progressive neuropathy in transgenic mice expressing the human neurofilament heavy gene: a mouse model of amyotrophic lateral sclerosis. Cell 73:35-46.
9. De Jonghe P, Mersivanova I, Nelis E, Del Favero J, Martin JJ, Van Broeckhoven C, Evgrafov O, Timmerman V. 2001. Further evidence that neurofilament light chain gene mutations can cause Charcot-Marie-Tooth disease type 2E. Ann Neurol 49:245-249.
10. de la Monte SM, Ganju N, Feroz N, Luong T, Banerjee K, Cannon J, Wands JR. 2002. Oxygen free radical injury is sufficient to cause some Alzheimer-type molecular abnormalities in human CNS neuronal cells. J Alzheimers Dis 2:261-281.
11. Dhavan R, Tsai LH. 2001. A decade of cdk5. Nat Rev Mol Cell Biol 2:749-759.
12. Ekinci FJ, Malik KM, Shea TB. 1999. β-Amyloid induces calcium influx and neurodegeneration by MAP kinase-mediated activation of the L voltage-sensitive calcium channel. J Biol Chem 274:30322-30327.
13. Figlewicz DA, Krizus A, Martinoli MG, Meininger V, Dib M, Rouleau GA, Julien JP. 1994. Variants of the heavy neurofilament subunit are associated with the development of amyotrophic lateral sclerosis. Mol Genet 3:1757-1761.
14. Gelinas S, Chapados C, Beauregard M, Gosselin I, Martinoli MG. 2000. Effect of oxidative stress on stability and structure of neurofilament proteins. Biochem Cell Biol 78:667-674.
15. Gou JP, Gotow T, Janmey PA, Leterrier JF. 1998. Regulation of neurofilament interactions in vitro by natural and synthetic polypeptides sharing Lys-Ser-Pro sequences with the heavy neurofilanient subunit NF-H: neurofilament crossbridging by antiparallel sidearm overlapping. Med Biol Eng Comput 36:371-387.
16. Grant P, Sharma P, Pant HC. 2001. Cyclin-dependent protein kinase 5 (Cdk5) and the regulation of neurofilament metabolism. Eur J Biochem 268:1534-1546.
17. Hashiguchi M, Saito T, Hisanaga S, Hashiguchi T. 2002. Truncation of CDK5 activator p35 induces intensive phosphorylation of Ser202/ Thr205 of human tau. J Biol Chem 277:44525-44530.
18. Hirokawa N, Glicksman MA, Willard MB. 1984. Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J Cell Biol 98:1523-1536.
19. Julien JP, Mushynski WE. 1998. Neurofilaments in health and disease. Prog Nucleic Acid Res Mol Biol 61:1-20.
20. Jung C, Shea TB. 1999. Regulation of neurofilament axonal transport by phosphorylation in optic axons in situ. Cell Motil Cytoskeleton 43:230-240.
21. Jung C, Yabe J, Wang FS, Shea TB. 1998. Neurofilaments are present within axonal neurites before incorporation into Triton-insoluble structures. Cell Motil Cytoskeleton 40:44-58
22. Jung C, Yabe JT, Shea TB. 2000. C-terminal phosphorylation of the heavy molecular weight neurofilament subunit is inversely correlated with neurofilament axonal transport velocity. Brain Res 856:12-19.
23. Kerokoski P, Suuronen T, Salminen A, Soininen H, Pirttila T. 2002. Cleavage of the cyclin-dependent kinase 5 activator p35 to p25 does not induce tau hyperphosphorylation. Biochem Biophys Res Commun 298:693-698.
24. Kusakawa G, Saito T, Onuki R, Ishiguro K, Kishimoto T, Hisanaga S. 2000. Calpain-dependent proteolytic cleavage of the p35 cyclin-dependent kinase 5 activator to p25. J Biol Chem 275:17166-17172.
25. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH. 1996. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 405:360-364.
26. Lee KY, Rosales JL, Tang D, Wang JH. 2000. Interaction of cyclin-dependent kinase 5 (Cdk5) and neuronal Cdk5 activator in bovine brain. J Biol Chem 271:1538-11543.
27. Lee MS, Tsai LH. 2003. Cdk5: one of the links between senile plaques and neurofibrillary tangles? J Alzheimers Dis 5:127-137.
28. Leterrier JF, Käs J, Hartwig J, Vegners R, Janmey P. 1996. Mechanical effects of neurofilament cross-bridges. J Biol Chem 271:15687-15694.
29. Lew J, Winkfein RJ, Paudel HK, Wang JH. 1992. Brain proline-directed protein kinase is a neurofilament kinase which displays high sequence homology to p34cdc2. J Biol Chem 267:25922-25926.
30. Lewis SE, Nixon RA. 1988. Multiple phosphorylated variants of the high molecular mass subunit of neurofilaments in axons of retinal cell neurons: characterization and evidence for their differential association with stationary and moving neurofilaments. J Cell Biol 107:2689-2701.
31. Li BS, Zhang L, Gu J, Amin ND, Pant HC. 2000. Integrin alpha(1) beta(l)-mediated activation of cyclin-dependent kinase 5 activity is involved in neurite outgrowth and human neurofilament protein H Lys-Ser-Pro tail domain phosphorylation. J Neurosci 20:6055-6062.
32. Meijer L, Borgne A, Mulner O, Chong JP, Blow JJ, Inagaki N, Inagaki M, Delcros JG, Moulinoux JP. 1997. Biochemical and cellular effects of roscovitine, a potent and selective inhibitor of the cyclin-dependent kinases cdc2, cdk2 and cdk5. Eur J Biochem 243:527-536.
33. Meyerson M, Enders GH, Wu CL, Su LK, Gorka C, Nelson C, Harlow E, Tsai LH. 1992. A family of human cdc2-related protein kinases. EMBO J 11:2909-2917.
34. Nguyen MD, Lariviere RC, Julien JP. 2001. Deregulation of Cdk5 in a mouse model of ALS: toxicity alleviated by perikaryal neurofilament inclusions. Neuron 30:135-147.
35. Nixon RA, Paskevich PA, Sihag RK, Thayer CY. 1994. Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: influences on regional neurofilament accumulation, interneurofilament spacing, and axonal caliber. J Cell Biol 126:1031-1046.
36. Pant HC, Veeranna. 1995. Neurofilament phosphorylation. Biochem Cell Biol 73:575-592.
37. Pant AC, Veeranna, Pant HC, Amin N. 1997. Phosphorylation of human high molecular weight neurofilament protein (hNF-H) by neuronal cyclin-dependent kinase 5 (cdk5). Brain Res 765:259-266.
38. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. 1999. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 9:615-622.
39. Patzke H, Tsai LH. 2002. Cdk5 sinks into ALS. Trends Neurosci 25:8-10.
40. Perry G, Roder H, Nunomura A, Takeda A, Friedlich AL, Zhu X, Raina AK, Holbrook N, Siedlak SL, Harris PL, Smith MA. 1999. Activation of neuronal extracellular receptor kinase (ERK) in Alzheimer disease links oxidative stress to abnormal phosphorylation. Neuroreport 10:2411-2415.
41. Rao M, Nixon RA. 2003. Defective neurofilament transport in mouse models of amyotrophic lateral sclerosis: a review. Neurochem Res 28:1041-1047.
42. Robertson J, Beaulieu JM, Doroudchi MM, Durham HD, Julien JP, Mushynski WE. 2001. Apoptotic death of neurons exhibiting peripherin aggregates is mediated by the proinflammatory cytokine tumor necrosis factor-alpha. J Cell Biol 155:217-226.
43. Sanchez I, Hassinger L, Sihag RK, Cleveland DW, Mohan P, Nixon RA. 2000. Local control of neurofilament accumulation during radial growth of myelinating axons in vivo: selective role of site-specific phosphorylation. J Cell Biol 151:1013-1024.
44. Sharma M, Sharma P, Pant HC. 1999. CDK-5-mediated neurofilament phosphorylation in SHSY5Y human neuroblastoma cells. J Neurochem 73:79-86.
45. Sharma P, Veeranna, Sharma M, Amin ND, Sihag RK, Grant P, Ahn N, Kulkami AB, Pant HC. 2002. Phosphorylation of MEK1 by cdk5/p35 downregulates the mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 277:528-534.
46. Shea TB. 2001. Phosphorylation and neurofilament axonal transport. J Neurocytol 29:877-891.
47. Shea TB, Flanagan L. 2001. Kinesin, dynein and neurofilament transport. Trends Neurosci 24:644-648.
48. Shea TB, Wheeler E, Jung C. 1997. Aluminum inhibits neurofilament assembly, cytoskeletal incorporation, and axonal transport. Dynamic nature of aluminum-induced perikaryal neurofilament accumulations as revealed by subunit turnover. Mol Chem Neuropathol 32:17-39.
49. Shea TB, Yabe JT, Ortiz D, Pimenta A, Loomis P, Goldman RD, Amin N, Pant HC. 2004. CDK5 regulates axonal transport and phosphorylation of neurofilaments in cultured neurons. J Cell Sci 117:933-941.
50. Smith DS, Tsai LH. 2002. Cdk5 behind the wheel: a role in trafficking and transport? Cell Biol 12:28-36.
51. Straube-West K, Loomis PA, Opal P, Goldman RD. 1996. Alterations in neuronal intermediate filament organization, functional implications and the induction of pathological changes related to motor neuron disease. J Cell Sci 109:2319-2329.
52. Strong M. 2003. The basics of therapeutics in amyotrophic lateral sclerosis. Pharmacol Ther 5542:1-36.
53. Strong MJ, Strong WL, Jaffe H, Traggert B, Sopper MM, Pant HC. 2001. Phosphorylation state of the native high-molecular-weight neurofilament subunit protein from cervical spinal cord in sporadic amyotrophic lateral sclerosis. J Neurochem 76:1315-1325.
54. Tandon A, Yu H, Wang L, Rogaeva E, Sato C, Chishti MA, Kawarai T, Hasegawa H, Chen F, Davies P, Fraser PE, Westaway D, St George-Hyslop PH. 2003. Brain levels of CDK5 activator p25 are not increased in Alzheimer's or other neurodegenerative diseases with neurofibrillary tangles. J Neurochem 86:572-581.
55. Tomkins J, Usher P, Slade JY, Ince PG, Curtis A, Bushby K, Shaw PJ. 1998. Novel insertion in the KSP region of the neurofilament heavy gene in amyotrophic lateral sclerosis (ALS). Neuroreport 9:3967-3970.
56. Tseng HC, Zhou Y, Shen Y, Tsai LH. 2002. A survey of Cdk5 activator p35 and p25 levels in Alzheimer's disease brains. FEBS Lett 523:58-62.
57. Yabe JT, Chan WK, Chylinski TM, Lee S, Pimenta AF, Shea TB. 2001. The predominant form in which neurofilament subunits undergo axonal transport varies during axonal initiation, elongation, and maturation. Cell Motil Cytoskeleton 48:61-83.
58. Yabe JT, Pimenta A, Shea TB. 1999. Kinesin-mediated transport of neurofilament protein oligomers in growing axons. J Cell Sci 112:3799-3814.
59. Zheng YL, Li BS, Amin ND, Albers W, Pant HC. 2002. A peptide derived from cyclin-dependent kinase activator (p35) specifically inhibits Cdk5 activity and phosphorylation of tau protein in transfected cells. Eur J Biochem 269:4427-4434.
60. Zhu Q, Lindenbaum M, Levavasseur F, Jacomy H, Julien JP. 1998. Disruption of the NF-H gene increases axonal microtubule content and velocity of neurofilament transport: relief of axonopathy resulting from the toxin beta, betaprime;-iminodiproprionitrile. J Cell Biol 143:183-193.