p35/p25 is not essential for tau and cytoskeletal pathology or neuronal loss in Niemann-Pick type C disease

Journal of Neuroscience

Volumn 26, Issue 10, 2006, Pages 2738-2744

  Hallows, Janice L ^a   Iosif, Robert E ^a,c   Biasell, Rebecca D ^a   Vincent, Inez ^a,b  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c LUND UNIVERSITY   (Sweden)

Author keywords

ALS; Alzheimer's disease; cdk5; Hyperphosphorylation; Spheroid; Tauopathy

Indexed keywords

CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR; CYTOSKELETON PROTEIN; PROTEIN P25; PROTEIN P35; TAU PROTEIN;

ALZHEIMER DISEASE; AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INCLUSION; DISEASE COURSE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REGULATION; FEMALE; LOCOMOTION; MALE; MOUSE; NERVE DEGENERATION; NEUROPATHOLOGY; NIEMANN PICK DISEASE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION;

AGE FACTORS; ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN; CYCLIN-DEPENDENT KINASE 5; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; MOTOR ACTIVITY; NEUROFILAMENT PROTEINS; NEURONS; NIEMANN-PICK DISEASES; NUCLEAR PROTEINS; PHOSPHOPYRUVATE HYDRATASE; PHOSPHORYLATION; PHOSPHOTRANSFERASES; PROTEINS; TAU PROTEINS; WEIGHT LOSS;

EID: 33644827659     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4834-05.2006     Document Type: Article

References (41)

1. Ahlijanian MK, Barrezueta NX, Williams RD, Jakowski A, Kowsz KP, McCarthy S, Coskran T, Carlo A, Seymour PA, Burkhardt JE, Nelson RB, McNeish JD (2000) Hyperphosphorylated tau and neurofilament and cytoskeletal disruptions in mice overexpressing human p25, an activator of cdk5. Proc Natl Acad Sci USA 97:2910-2915.
2. Axelsson R, Roytta M, Sourander P, Akesson HO, Andersen O (1984) Hereditary diffuse leucoencephalopathy with spheroids. Acta Psychiatr Scand Suppl 314:1-65.
3. Bian F, Nath R, Sobocinski G, Booher RN, Lipinski WJ, Callahan MJ, Pack A, Wang KK, Walker LC (2002) Axonopathy, tau abnormalities, and dyskinesia, but no neurofibrillary tangles in p25-transgenic mice. J Comp Neurol 446:257-266.
4. Bu B, Li J, Davies P, Vincent I (2002a) Deregulation of cdk5, hyperphosphorylation, and cytoskeletal pathology in the Niemann-Pick type C murine model. J Neurosci 22:6515-6525.
5. Bu B, Klunemann H, Suzuki K, Li J, Bird T, Jin LW, Vincent I (2002b) Niemann-Pick disease type C yields possible clue for why cerebellar neurons do not form neurofibrillary tangles. Neurobiol Dis 11:285-297.
6. Busser J, Geldmacher DS, Herrup K (1998) Ectopic cell cycle proteins predict the sites of neuronal cell death in Alzheimer's disease brain. J Neurosci 18:2801-2807.
7. Cruz JC, Tsai LH (2004) A Jekyll and Hyde kinase: roles for Cdk5 in brain development and disease. Curr Opin Neurobiol 14:390-394.
8. Cruz JC, Tseng HC, Goldman JA, Shih H, Tsai LH (2003) Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 40:471-483.
9. Delisle MB, Carpenter S (1984) Neurofibrillary axonal swellings and amyotrophic lateral sclerosis. J Neurol Sci 63:241-250.
10. Erickson RP, Bernard O (2002) Studies on neuronal death in the mouse model of Niemann-Pick C disease. J Neurosci Res 68:738-744.
11. German DC, Quintero EM, Liang CL, Ng B, Punia S, Xie C, Dietschy JM (2001) Selective neurodegeneration, without neurofibrillary tangles, in a mouse model of Niemann-Pick C disease. J Comp Neurol 433:415-425.
12. Gotow T, Tanaka J (1994) Phosphorylation of neurofilament H subunit as related to arrangement of neurofilaments. J Neurosci Res 37:691-713.
13. Hallows JL, Chen K, DePinho RA, Vincent I (2003) Decreased cyclin-dependent kinase 5 (cdk5) activity is accompanied by redistribution of cdk5 and cytoskeletal proteins and increased cytoskeletal protein phosphorylation in p35 null mice. J Neurosci 23:10633-10644.
14. Henderson LP, Lin L, Prasad A, Paul CA, Chang TY, Maue RA (2000) Embryonic striatal neurons from niemann-pick type C mice exhibit defects in cholesterol metabolism and neurotrophin responsiveness. J Biol Chem 275:20179-20187.
15. Iqbal K, Alonso Adel C, Chen S, Chohan MO, El-Akkad E, Gong CX, Khatoon S, Li B, Liu F, Rahman A, Tanimukai H, Grundke-Iqbal I (2005) Tau pathology in Alzheimer disease and other tauopathies. Biochim Biophys Acta 1739:198-210.
16. Lau KF, Howlett DR, Kesavapany S, Standen CL, Dingwall C, McLoughlin DM, Miller CC (2002) Cyclin-dependent kinase-5/p35 phosphorylates presenilin 1 to regulate carboxy-terminal fragment stability. Mol Cell Neurosci 20:13-20.
17. Lee VM, Goedert M, Trojanowski JQ (2001) Neurodegenerative tauopathies. Annu Rev Neurosci 24:1121-1159.
18. Lew J, Huang QQ, Qi Z, Winkfein RJ, Aebersold R, Hunt T, Wang JH (1994) A brain-specific activator of cyclin-dependent kinase 5. Nature 371:423-426.
19. Loftus SK, Morris JA, Carstea ED, Gu JZ, Cummings C, Brown A, Ellison J, Ohno K, Rosenfeld MA, Tagle DA, Pentchev PG, Pavan WJ (1997) Murine model of Niemann-Pick C disease: mutation in a cholesterol homeostasis gene. Science 277:232-235.
20. Loftus SK, Erickson RP, Walkley SU, Bryant MA, Incao A, Heidenreich RA, Pavan WJ (2002) Rescue of neurodegeneration in Niemann-Pick C mice by a prion-promoter- driven Npc1 cDNA transgene. Hum Mol Genet 11:3107-3114.
21. Lucas JJ, Hernandez F, Gomez-Ramos P, Moran MA, Hen R, Avila J (2001) Decreased nuclear beta-catenin, tau hyperphosphorylation and neurodegeneration in GSK-3beta conditional transgenic mice. EMBO J 20:27-39.
22. 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.
23. Morfini G, Szebenyi G, Brown H, Pant HC, Pigino G, DeBoer S, Beffert U, Brady ST (2004) A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J 23:2235-2245.
24. 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.
25. Nguyen MD, Boudreau M, Kriz J, Couillard-Despres S, Kaplan DR, Julien JP (2003) Cell cycle regulators in the neuronal death pathway of amyotrophic lateral sclerosis caused by mutant superoxide dismutase 1. J Neurosci 23:2131-2140.
26. Noble W, Olm V, Takata K, Casey E, Mary O, Meyerson J, Gaynor K, LaFrancois J, Wang L, Kondo T, Davies P, Burns M, Veeranna, Nixon R, Dickson D, Matsuoka Y, Ahlijanian M, Lau LF, Duff K (2003) Cdk5 is a key factor in tau aggregation and tangle formation in vivo. Neuron 38:555-565.
27. Ohshima T, Ward JM, Huh CG, Longenecker G, Veeranna, Pant HC, Brady RO, Martin LJ, Kulkarni AB (1996) Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc Natl Acad Sci USA 93:11173-11178.
28. 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 402:615-622.
29. Rashidian J, Iyirhiaro G, Aleyasin H, Rios M, Vincent I, Callaghan S, Bland RJ, Slack RS, During MJ, Park DS (2005) Multiple cyclin-dependent kinases signals are critical mediators of ischemia/hypoxic neuronal death in vitro and in vivo. Proc Natl Acad Sci USA 102:14080-14085.
30. Sawamura N, Gong JS, Garver WS, Heidenreich RA, Ninomiya H, Ohno K, Yanagisawa K, Michikawa M (2001) Site-specific phosphorylation of tau accompanied by activation of mitogen-activated protein kinase (MAPK) in brains of Niemann-Pick type C mice. J Biol Chem 276:10314-10319.
31. Sharma P, Veeranna, Sharma M, Amin ND, Sihag RK, Grant P, Ahn N, Kulkarni AB, Pant HC (2002) Phosphorylation of MEK1 by cdk5/p35 down-regulates the mitogen-activated protein kinase pathway. J Biol Chem 277:528-534.
32. Smith PD, Mount MP, Shree R, Callaghan S, Slack RS, Anisman H, Vincent I, Mao X, Park DS (2006) Calpain regulated p35/cdk5 plays a central role in dopaminergic neuron death through modulation of the transcription factor myocyte enhancer factor 2. J Neurosci 26:440-557.
33. Takahashi S, Kulkarni AB (2004) Mutant superoxide dismutase 1 causes motor neuron degeneration independent of cyclin-dependent kinase 5 activation by p35 or p25. J Neurochem 88:1295-1304.
34. Takashima A, Murayama M, Yasutake K, Takahashi H, Yokoyama M, Ishiguro K (2001) Involvement of cyclin dependent kinase5 activator p25 on tau phosphorylation in mouse brain. Neurosci Lett 306:37-40.
35. 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.
36. Vesely J, Havlicek L, Strnad M, Blow JJ, Donella-Deana A, Pinna L, Letham DS, Kato J, Detivaud L, Leclerc S (1994) Inhibition of cyclin-dependent kinases by purine analogues. Eur J Biochem 224:771-786.
37. Vincent I, Jicha G, Rosado M, Dickson DW (1997) Aberrant expression of mitotic cdc2/cyclin B1 kinase in degenerating neurons of Alzheimer's disease brain. J Neurosci 17:3588-3598.
38. Walkley SU, Suzuki K (2004) Consequences of NPC1 and NPC2 loss of function in mammalian neurons. Biochim Biophys Acta 1685:48-62.
39. Yoo BC, Lubec G (2001) p25 protein in neurodegeneration. Nature 411:763-764, discussion 764-765.
40. Zhang M, Li J, Chakrabarty P, Bu B, Vincent I (2004) Cyclin-dependent kinase inhibitors attenuate protein hyperphosphorylation, cytoskeletal lesion formation, and motor defects in Niemann-Pick type C mice. Am J Pathol 165:843-853.
41. Zhou L, Miller BL, McDaniel CH, Kelly L, Kim OJ, Miller CA (1998) Frontotemporal dementia: neuropil spheroids and presynaptic terminal degeneration. Ann Neurol 44:99-109.