Deregulation of Cdk5 in a mouse model of ALS: Toxicity alleviated by perikaryal neurofilament inclusions

Neuron

Volumn 30, Issue 1, 2001, Pages 135-148

  Nguyen, Minh Dang ^a   Larivière, Roxanne C ^a   Julien, Jean Pierre ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN DEPENDENT KINASE 5; NEUROFILAMENT PROTEIN; SUPEROXIDE DISMUTASE;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CYTOSKELETON; ENZYME ACTIVITY; ENZYME REGULATION; MOUSE; NERVE CELL NECROSIS; NEUROFILAMENT; NEUROTOXICITY; NONHUMAN; PHOSPHORYLATION; PRIORITY JOURNAL;

EID: 17744368458     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(01)00268-9     Document Type: Article

References (63)

1. Ahlijanian M.K., Barrezueta N.X., Williams R.D., Jakowski A., Kowsz K.P., McCarthy S., Coskran T., Carlo A., Seymour P.A., Burkhardt J.E.et al. Hyperphosphorylation of tau and neurofilaments and cytoskeletal disruptions in mice overexpressing human p25, an activator of Cdk5. Proc. Natl. Acad. Sci. USA. 97:2000;2910-2915.
2. Bajaj N.P., Miller C.C.J. Phosphorylation of neurofilament heavy-chain side-arm fragments by cyclin-dependent kinase-5 and glycogen synthase kinase-3α in transfected cells. J. Neurochem. 69:1997;737-743.
3. Bajaj N.P., Al-Sarraj S.T., Anderson V., Kibble M., Leigh P.N., Miller C.C.J. Cyclin-dependent kinase-5 is associated with lipofuscin in motor neurons in amyotrophic lateral sclerosis. Neurosci. Lett. 245:1998;45-48.
4. Bajaj N.P., Al-Sarraj S.T., Leigh P.N., Anderson V., Miller C.C.J. 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 neurons in ALS. Prog. Neuropsychopharmacol. Biol. Psychiatry. 23:1999;833-850.
5. Baumann K., Mandelkow E.M., Biernat J., Piwnica-Worms H., Mandelkow E. Abnormal Alzheimer-like phosphorylation of tau-protein by cyclin-dependent kinases cdk2 and cdk5. FEBS Lett. 336:1993;417-424.
6. Beaulieu J.-M., Nguyen M.D., Julien J.-P. Late onset death of motor neurons in mice overexpressing wild-type peripherin. J. Cell. Biol. 147:1999;531-544.
7. Beaulieu J.-M., Jacomy H., Julien J.P. Formation of intermediate filament protein aggregates with disparate effects in two transgenic mouse models lacking the neurofilament light subunit. J. Neurosci. 20:2000;5321-5328.
8. Beckman J.S., Carson M., Smith C.D., Koppenol W.H. ALS, SOD and peroxynitrite. Nature. 364:1993;584.
9. Brion J.P., Couck A.M. Cortical and brainstem-type lewy bodies are immunoreactive for the cyclin-dependent kinase 5. Am. J. Pathol. 147:1995;1465-1476.
10. Bruijn L.I., Becher M.W., Lee M.K., Anderson L.L., Jenkins N.A., Copeland N.G., Sisodia S.S., Rothstein J.D., Borchelt D.R., Price D.L., Cleveland D.W. ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron. 18:1997;327-338.
11. Bruijn L.I., Houseweart M.K., Kato S., Anderson K.L., Anderson S.D., Ohama E., Reaume A.G., Scott R.W., Cleveland D.W. Aggregation and motor neuron toxicity of an ALS-linked SOD1 mutant independent from wild-type SOD1. Science. 281:1998;1851-1854.
12. Carpenter S. Proximal axonal enlargement in motor neuron disease. Neurology. 18:1968;841-851.
13. Cleveland D.W. From Charcot to SOD1. mechanisms of selective motor neuron death in ALS Neuron. 24:1999;515-520.
14. Corson L.B., Strain J.J., Culotta V.C., Cleveland D.W. Chaperone-facilitated copper binding is a property common to several classes of familial amyotrophic lateral sclerosis-linked superoxide dismutase mutants. Proc. Natl. Acad. Sci. USA. 95:1998;6361-6366.
15. Côté F., Collard J.F., Julien J.-P. Progressive neuropathy in transgenic mice expressing the human neurofilament heavy gene. a mouse model of amyotrophic lateral sclerosis Cell. 73:1993;35-46.
16. Couillard-Després J.-S., Zhu Q., Wong P.C., Price D.L., Cleveland D.W., Julien J.-P. Protective effect of neurofilament NF-H overexpression in motor neuron disease induced by mutant superoxide dismutase. Proc. Natl. Acad. Sci. USA. 95:1998;9626-9630.
17. Cudkowicz M.E., McKenna-Yasek D., Sapp P.E., Chin W., Geller B., Hayden D.L., Schoenfeld D.A., Hosler B.A., Horvitz H.R., Brown R.H. Epidemiology of mutations in superoxide dismutase in amyotrophic lateral sclerosis. Ann. Neurol. 41:1997;210-221.
18. Dal Canto M.C., Gurney M.E. Neuropathological changes in two lines of mice carrying a transgene for mutant human Cu,Zn SOD, and in mice overexpressing wild type human SOD. a model of familial amyotrophic lateral sclerosis (FALS) Brain Res. 676:1995;25-40.
19. Elliot J.L., Snider W.D. Parvalbumin is a marker of ALS-resistant motor neurons. Neuroreport. 6:1995;449-452.
20. Estevez A.G., Crow J.P., Sampson J.B., Reiter C., Zhuang Y., Richardson G.J., Tarpey M.M., Barbeito L., Beckman J.S. Induction of nitric oxide-dependent apoptosis in motor neurons by zinc-deficient superoxide dismutase. Science. 286:1999;2498-2500.
21. Eyer J., Cleveland D.W., Wong P.C., Peterson A.C. Pathogenesis of two axonopathies does not require axonal neurofilaments. Nature. 391:1998;584-587.
22. Fridovich I. Superoxide dismutases. Adv. Enzymol. Relat. Areas Mol. Biol. 58:1986;61-97.
23. Ghadge J.D., Lee J.P., Bindokas V.P., Jordan J., Ma L., Miller R.J., Roos R. Mutant superoxide dismutase-1-linked familial amyotrophic lateral sclerosis. molecular mechanisms of neuronal death and protection J. Neurosci. 17:1997;8756-8766.
24. Giasson B.I., Mushynski W.E. Aberrant stress-induced phosphorylation of perikaryal neurofilaments. J. Biol. Chem. 271:1996;30404-30409.
25. Green S.L., Vulliet P.R., Pinter M.J., Cork L.C. Alterations in cyclin-dependent kinase 5 (CDK5) protein levels, activity and immunocytochemistry in canine motor neuron disease. J. Neuropathol. Exp. Neurol. 57:1998;1070-1077.
26. Guidato S., Tsai L.H., Woodgett J., Miller C.C.J. Differential cellular phosphorylation of neurofilament heavy side-arms by glycogen synthase kinase-3 and cyclin-dependent kinase-5. J. Neurochem. 66:1996;1698-1706.
27. Hirano A., Nakano I., Kurland L.T., Mulder D.W., Holley P.W., Saccomanno G. Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 43:1984;471-480.
28. Ince P., Stout N., Shaw P., Slade J., Hunziker W., Heizmann C.W., Baimbridge K.G. Parvalbumin and calbindin D-28K in the human motor system and in motor neuron disease. Neuropathol. Appl. Neurobiol. 19:1993;291-299.
29. Iqbal K., Grundke-Iqbal I. Alzheimer abnormally phosphorylated tau is more hyperphosphorylated than the fetal tau and causes the disruption of microtubules. Neurobiol. Aging. 16:1995;375-379.
30. Ishihara T., Hong M., Zhang B., Nakagawa Y., Lee M.K., Trojanowski J.Q., Lee V.M. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron. 24:1999;751-762.
31. Julien J.-P. Neurofilament functions in health and disease. Curr. Opin. Neurobiol. 9:1999;554-560.
32. Julien J.-P. Amyotrophic lateral sclerosis. unfolding the toxicity of the misfolded Cell. 104:2001;571-591.
33. Kong J., Xu Z. Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J. Neurosci. 18:1998;3241-3250.
34. Kusakawa G.I., Saito T., Onuki R., Ishiguro K., Kishimoto T., Hisanaga S. Calpain-dependent proteolytic cleavage of the p35 Cdk5 activator to p25. J. Biol. Chem. 275:2000;166-172.
35. Kwon Y.T., Tsai L.H. A novel disruption of cortical development in p35 (-/-) mice distinct from reeler. J. Comp. Neurol. 395:1998;510-522.
36. Lee M.K., Cleveland D.W. Neuronal intermediate filaments. Annu. Rev. Neurosci. 19:1996;187-217.
37. Lee M.-S., Kwon Y.T., Li M., Peng J., Friedlander R.M., Tsai L.-H. Neurotoxicity induces cleavage of p35 into p25. Nature. 405:2000;360-364.
38. Lew J., QI Z., Huang Q.-Q., Paudel H., Matsuura I., Matsushita M., Zhu X., Wang J.H. Structure, function, and regulation of neuronal Cdc2-like protein kinase. Neurobiol. Aging. 16:1995;263-270.
39. Li M., Ona V.O., Guégan C., Chen M., Jackson-Lewis V., Andrews L.J., Olzewski A.J., Stieg P.E., Lee J.P., Przedborski S., Friendlander R.M. Functional role of caspase-1 and caspase-3 in an ALS transgenic mouse model. Science. 288:2000;335-339.
40. Mandelkow E. The tangled tale of tau. Nature. 402:1999;588-599.
41. Morrison B.M., Gordon J.W., Ripps M.E., Morrison J.H. Quantitative immunocytochemical analysis of the spinal cord in G86R superoxide dismutase transgenic mice. neurochemical correlates of selective vulnerability J. Neurol. Comp. 373:1996;619-631.
42. Nikolic M., Dudek H., Kwon Y.T., Ramos Y.F., Tsai L.H. The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation. Genes Dev. 10:1996;816-825.
43. Oshima T., Ward J.M., Huh C.G., Longenecker G., Veeranna G.J., Pant H.C., Brady R.O., Martin L.J., Kulkarni A.B. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc. Acad. Natl. Sci. USA. 93:1996;11173-11178.
44. Pasinelli P., Borchelt D.R., Houseweart M.K., Cleveland D.W., Brown R.H. Jr. Caspase-1 is activated in neural cells and tissue with amyotrophic lateral sclerosis-associated mutations in copper-zinc superoxide dismutase. Proc. Natl. Acad. Sci. USA. 95:1998;15763-15768.
45. Patrick G.N., Zukerberg L., Nikolic M., de la Monte S., Dikkes P., Tsai L.H. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature. 402:1999;615-622.
46. Pei J.J., Grundke-Iqbal I., Iqbal K., Bogdanovic N., Winblad B., Cowburn R.F. Accumulation of cyclin-dependent kinase 5 (cdk5) in neurons with early stages of Alzheimer's disease neurofibrillary degeneration. Brain Res. 797:1998;267-277.
47. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Reagan J.P., Deng H.-X.et al. Mutation in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature. 362:1993;59-62.
48. Rouleau G.A., Clarke A.W., Rooke K., Pramatarova A., Krizus A., Suchowersky O., Julien J.-P., Figlewicz D.A. SOD1 mutation is associated with accumulations of neurofilaments in amyotrophic lateral sclerosis. Ann. Neurol. 39:1996;128-131.
49. Roy J., Minotti S., Dong L., Figlewicz D.A., Durham H.D. Glutamate potentiates the toxicity of mutant Cu/Zn-superoxide dismutase in motor neurons by postsynaptic calcium-dependent mechanisms. J. Neurosci. 18:1998;9673-9684.
50. Schmidt M.L., Carden M.J., Lee V.M., Trojanowski J.Q. Phosphate dependent and independent neurofilament epitopes in the axonal swellings of patients with motor neuron disease and controls. Lab. Invest. 56:1997;282-294.
51. Trotti D., Rolfs A., Danbolt N.C., Brown R.H. Jr., Hediger M.A. SOD1 mutants linked to amyotrophic lateral sclerosis selectively inactivate a glial glutamate transporter. Nat. Neurosci. 2:1998;427-433.
52. Tsai L.H., Takahashi T., Caviness V.S. Jr., Harlow E. Activity and expression pattern of cyclin-dependent kinase 5 in the embryonic mouse nervous system. Development. 119:1993;1029-1040.
53. Tsai L.H., Delalle I., Caviness V.S. Jr., Chae T., Harlow E. P35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5. Nature. 371:1994;419-423.
54. Veeranna G.J., Amin N.D., Ahn N.G., Jaffe H., Winters C.A., Grant P., Pant H.C. Mitogen-activated protein kinases (Erk1, 2) phosphorylate Lys-Ser-Pro (KSP) repeats in neurofilament proteins NF-H and NF-M. J. Neurosci. 18:1998;4008-4021.
55. Veeranna G.J., Shetty K.T., Takahashi M., Grant P., Pant H.C. Cdk5 and MAPK are associated with complexes of cytoskeletal proteins in rat brain. Mol. Brain Res. 76:2000;229-236.
56. Wideau-Pazos M., Goto J.J., Rabizadeh S., Gralla E.B., Roe J.A., Lee M.K., Valentine J.S., Bredesen D.E. Altered reactivity of superoxide dismutase in familial amyotrophic lateral sclerosis. Science. 271:1996;515-518.
57. Williamson T.L., Cleveland D.W. Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat. Neurosci. 2:1999;50-56.
58. Williamson T.L., Bruijn L.I., Zhu Q., Anderson K.L., Anderson S.D., Julien J.P., Cleveland D.W. Absence of neurofilaments reduces the selective vulnerability of motor neurons and slows disease caused by a amyotrophic lateral sclerosis-linked superoxide dismutase 1 mutant. Proc. Natl. Acad. Sci. USA. 95:1998;9631-9636.
59. Wong P.C., Pardo C.A., Borchelt D.R., Lee M.K., Copeland N.G., Jenkins N.A., Sisodia S.S., Cleveland D.W., Price D.L. An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron. 14:1995;1105-1116.
60. Yamaguchi H., Ishiguro K., Uchida T., Takashima A., Lemere C.A., Imahori K. Preferential labeling of Alzheimer neurofibrillary tangles with antisera for tau protein kinase (TPK)I/glycogen synthase kinase-3 and cyclin-dependent kinase 5, a component of TPK II. Acta Neuropathol. 92:1996;232-241.
61. Zhang B., Tu P., Abtahian F., Trojanowski J.Q., Lee V.M. Neurofilaments and orthograde transport are reduced in ventral root axons of transgenic mice that express human SOD1 with a G93A mutation. J. Cell. Biol. 139:1997;1307-1315.
62. Zhu Q., Couillard-Després S.-D., Julien J.-P. Delayed maturation of regenerating myelinated axons in mice lacking neurofilaments. Exp. Neurol. 148:1997;299-316.
63. Zhu Q., Lindenbaum M., Levavasseur F., Jacomy H., Julien J.-P. Disruption of the NF-H gene increases axonal microtubule content and velocity of neurofilament transport. relief of axonopathy resulting from the beta, beta′-iminodiproprionitrile J. Cell Biol. 143:1998;183-193.