S-nitrosylation of Cdk5: Potential implications in amyloid-β-related neurotoxicity in Alzheimer disease

Prion

Volumn 6, Issue 4, 2012, Pages 364-370

  Qu, Jing ^a   Nakamura, Tomohiro ^a   Holland, Emily A ^a   McKercher, Scott R ^a   Lipton, Stuart A ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

Cyclindependent kinase 5; Neuronal NO synthase; Nitric oxide; Nitrosative stress; Transnitrosylation

Indexed keywords

AMYLOID BETA PROTEIN; CYCLIN DEPENDENT KINASE 5; CYSTEINE; MITOCHONDRIAL PROTEIN; MYC PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN DRP1; S NITROSYLASE; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; DENDRITIC SPINE; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HUMAN; NEGATIVE FEEDBACK; NERVE CELL NECROSIS; NEUROTOXICITY; NITROSYLATION; NONHUMAN; PROTEIN PROTEIN INTERACTION; REVIEW; SYNAPSE;

ALZHEIMER DISEASE; AMYLOID; ANIMALS; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE 5; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; NITROSO COMPOUNDS; RATS;

EID: 84866555095     PISSN: 19336896     EISSN: 1933690X     Source Type: Journal    
DOI: 10.4161/pri.21250     Document Type: Review

References (61)

1. Lew J, Huang QQ, Qi Z, Winkfein RJ, Aebersold R, Hunt T, et al. A brain-specific activator of cyclin-dependent kinase 5. Nature 1994; 371:423-6; PMID:8090222; http://dx.doi.org/10.1038/371423a0.
2. Tang D, Yeung J, Lee KY, Matsushita M, Matsui H, Tomizawa K, et al. An isoform of the neuronal cyclin-dependent kinase 5 (Cdk5) activator. J Biol Chem 1995; 270:26897-903; PMID:7592934; http://dx.doi.org/10.1074/jbc.270.45.26897.
3. Tsai LH, Lee MS, Cruz J. Cdk5, a therapeutic target for Alzheimer's disease? Biochim Biophys Acta 2004; 1697:137-142.
4. Kim Y, Sung JY, Ceglia I, Lee KW, Ahn JH, Halford JM, et al. Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 2006; 442:814-7; PMID:16862120; http://dx.doi.org/10.1038/ nature04976.
5. Ohshima T, Ward JM, Huh CG, Longenecker G, Veeranna, Pant HC, et al. Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death. Proc Natl Acad Sci U S A 1996; 93:11173-8; PMID:8855328; http://dx.doi.org/10.1073/pnas.93.20.11173.
6. Xie Z, Sanada K, Samuels BA, Shih H, Tsai LH. Serine 732 phosphorylation of FAK by Cdk5 is important for microtubule organization, nuclear movement, and neuronal migration. Cell 2003; 114:469-82; PMID:12941275; http://dx.doi.org/10. 1016/S0092-8674(03)00605-6.
7. Patrick C, Crews L, Desplats P, Dumaop W, Rockenstein E, Achim CL, et al. Increased CDK5 expression in HIV encephalitis contributes to neurodegeneration via tau phosphorylation and is reversed with Roscovitine. Am J Pathol 2011; 178:1646-61; PMID:21435449; http://dx.doi.org/10.1016/j.ajpath.2010.12.033.
8. Nguyen MD, Larivière RC, Julien JP. Deregulation of Cdk5 in a mouse model of ALS: toxicity alleviated by perikaryal neurofilament inclusions. Neuron 2001; 30:135-47; PMID:11343650; http://dx.doi.org/10.1016/S0896-6273(01) 00268-9.
9. Paoletti P, Vila I, Rifé M, Lizcano JM, Alberch J, Ginés S. Dopaminergic and glutamatergic signaling crosstalk in Huntington's disease neurodegeneration: the role of p25/cyclin-dependent kinase 5. J Neurosci 2008; 28:10090-101; PMID:18829967; http://dx.doi.org/10.1523/JNEUROSCI.3237-08.2008.
10. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999; 402:615-22; PMID:10604467; http://dx.doi.org/10. 1038/45159.
11. Qu D, Rashidian J, Mount MP, Aleyasin H, Parsanejad M, Lira A, et al. Role of Cdk5-mediated phosphorylation of Prx2 in MPTP toxicity and Parkinson's disease. Neuron 2007; 55:37-52; PMID:17610816; http://dx.doi.org/10.1016/j. neuron.2007.05.033.
12. Smith PD, Crocker SJ, Jackson-Lewis V, Jordan-Sciutto KL, Hayley S, Mount MP, et al. Cyclindependent kinase 5 is a mediator of dopaminergic neuron loss in a mouse model of Parkinson's disease. Proc Natl Acad Sci U S A 2003; 100:13650-5; PMID:14595022; http://dx.doi.org/10.1073/pnas.2232515100.
13. Wang J, Liu S, Fu Y, Wang JH, Lu Y. Cdk5 activation induces hippocampal CA1 cell death by directly phosphorylating NMDA receptors. Nat Neurosci 2003; 6:1039-47; PMID:14502288; http://dx.doi.org/10.1038/nn1119.
14. Kitazawa M, Oddo S, Yamasaki TR, Green KN, LaFerla FM. Lipopolysaccharide-induced inflammation exacerbates tau pathology by a cyclin-dependent kinase 5-mediated pathway in a transgenic model of Alzheimer's disease. J Neurosci 2005; 25:8843-53; PMID:16192374; http://dx.doi.org/10.1523/ JNEUROSCI.2868-05.2005.
15. Lee MS, Kwon YT, Li M, Peng J, Friedlander RM, Tsai LH. Neurotoxicity induces cleavage of p35 to p25 by calpain. Nature 2000; 405:360-4; PMID:10830966; http://dx.doi.org/10.1038/35012636.
16. Sahlgren CM, Pallari HM, He T, Chou YH, Goldman RD, Eriksson JE. A nestin scaffold links Cdk5/p35 signaling to oxidant-induced cell death. EMBO J 2006; 25:4808-19; PMID:17036052; http://dx.doi.org/10.1038/sj.emboj.7601366.
17. Strocchi P, Pession A, Dozza B. Up-regulation of cDK5/p35 by oxidative stress in human neuroblastoma IMR-32 cells. J Cell Biochem 2003; 88:758-65; PMID:12577309; http://dx.doi.org/10.1002/jcb.10391.
18. Zambrano CA, Egaña JT, Núñez MT, Maccioni RB, González-Billault C. Oxidative stress promotes tau dephosphorylation in neuronal cells: the roles of cdk5 and PP1. Free Radic Biol Med 2004; 36:1393-402; PMID:15135175; http://dx.doi.org/10.1016/j.freeradbiomed.2004.03. 007.
19. Cruz JC, Kim D, Moy LY, Dobbin MM, Sun X, Bronson RT, et al. p25/cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloid beta in vivo. J Neurosci 2006; 26:10536-41; PMID:17035538; http://dx.doi.org/10.1523/JNEUROSCI.3133-06.2006.
20. Cruz JC, Tseng HC, Goldman JA, Shih H, Tsai LH. Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles. Neuron 2003; 40:471-83; PMID:14642273; http://dx.doi.org/10.1016/S0896-6273(03)00627-5.
21. Otth C, Concha II, Arendt T, Stieler J, Schliebs R, González- Billault C, et al. AbetaPP induces cdk5-dependent tau hyperphosphorylation in transgenic mice Tg2576. J Alzheimers Dis 2002; 4:417-30; PMID:12446973.
22. Iijima K, Ando K, Takeda S, Satoh Y, Seki T, Itohara S, et al. Neuron-specific phosphorylation of Alzheimer's beta-amyloid precursor protein by cyclindependent kinase 5. J Neurochem 2000; 75:1085-91; PMID:10936190; http://dx.doi.org/10.1046/j.1471-4159.2000.0751085.x.
23. Fischer A, Sananbenesi F, Pang PT, Lu B, Tsai LH. Opposing roles of transient and prolonged expression of p25 in synaptic plasticity and hippocampus-dependent memory. Neuron 2005; 48:825-38; PMID:16337919; http://dx.doi.org/10.1016/j.neuron.2005.10.033.
24. Nakamura T, Lipton SA. S-Nitrosylation and uncompetitive/fast off-rate (UFO) drug therapy in neurodegenerative disorders of protein misfolding. Cell Death Differ 2007; 14:1305-14; PMID:17431424; http://dx.doi.org/10.1038/sj.cdd. 4402138.
25. Abu-Soud HM, Stuehr DJ. Nitric oxide synthases reveal a role for calmodulin in controlling electron transfer. Proc Natl Acad Sci U S A 1993; 90:10769-72; PMID:7504282; http://dx.doi.org/10.1073/pnas.90.22.10769.
26. Bredt DS, Hwang PM, Glatt CE, Lowenstein C, Reed RR, Snyder SH. Cloned and expressed nitric oxide synthase structurally resembles cytochrome P-450 reductase. Nature 1991; 351:714-8; PMID:1712077; http://dx.doi.org/10.1038/ 351714a0.
27. Sattler R, Xiong Z, Lu WY, Hafner M, MacDonald JF, Tymianski M. Specific coupling of NMDA receptor activation to nitric oxide neurotoxicity by PSD-95 protein. Science 1999; 284:1845-8; PMID:10364559; http://dx.doi.org/10.1126/ science.284.5421.1845.
28. Kim E, Sheng M. PDZ domain proteins of synapses. Nat Rev Neurosci 2004; 5:771-81; PMID:15378037; http://dx.doi.org/10.1038/nrn1517.
29. Lipton SA, Choi YB, Pan ZH, Lei SZ, Chen HS, Sucher NJ, et al. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature 1993; 364:626-32; PMID:8394509; http://dx.doi.org/10.1038/364626a0.
30. Cho DH, Nakamura T, Fang J, Cieplak P, Godzik A, Gu Z, et al. S-nitrosylation of Drp1 mediates beta-amyloid-related mitochondrial fission and neuronal injury. Science 2009; 324:102-5; PMID:19342591; http://dx.doi.org/10. 1126/science.1171091.
31. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, et al. S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 2004; 304:1328-31; PMID:15105460; http://dx.doi.org/10.1126/science.1093891.
32. Uehara T, Nakamura T, Yao D, Shi ZQ, Gu Z, Ma Y, et al. S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 2006; 441:513-7; PMID:16724068; http://dx.doi.org/10.1038/nature04782.
33. Yao D, Gu Z, Nakamura T, Shi ZQ, Ma Y, Gaston B, et al. Nitrosative stress linked to sporadic Parkinson's disease: S-nitrosylation of parkin regulates its E3 ubiquitin ligase activity. Proc Natl Acad Sci U S A 2004; 101:10810-4; PMID:15252205; http://dx.doi.org/10.1073/pnas.0404161101.
34. Qu J, Nakamura T, Cao G, Holland EA, McKercher SR, Lipton SA. S-Nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by β-amyloid peptide. Proc Natl Acad Sci U S A 2011; 108:14330-5; PMID:21844361; http://dx.doi.org/10.1073/pnas.1105172108.
35. Tian B, Yang Q, Mao Z. Phosphorylation of ATM by Cdk5 mediates DNA damage signalling and regulates neuronal death. Nat Cell Biol 2009; 11:211-8; PMID:19151707; http://dx.doi.org/10.1038/ncb1829.
36. Ho GP, Selvakumar B, Mukai J, Hester LD, Wang Y, Gogos JA, et al. S-nitrosylation and S-palmitoylation reciprocally regulate synaptic targeting of PSD-95. Neuron 2011; 71:131-41; PMID:21745643; http://dx.doi.org/10.1016/j. neuron.2011.05.033.
37. Asada A, Yamamoto N, Gohda M, Saito T, Hayashi N, Hisanaga S. Myristoylation of p39 and p35 is a determinant of cytoplasmic or nuclear localization of active cyclin-dependent kinase 5 complexes. J Neurochem 2008; 106:1325-36; PMID:18507738; http://dx.doi.org/10.1111/j.1471-4159.2008.05500.x.
38. Morabito MA, Sheng M, Tsai LH. Cyclin-dependent kinase 5 phosphorylates the N-terminal domain of the postsynaptic density protein PSD-95 in neurons. J Neurosci 2004; 24:865-76; PMID:14749431; http://dx.doi.org/10.1523/JNEUROSCI. 4582-03.2004.
39. Zheng YL, Li BS, Amin ND, Albers W, Pant HC. A peptide derived from cyclin-dependent kinase activator (p35) specifically inhibits Cdk5 activity and phosphorylation of tau protein in transfected cells. Eur J Biochem 2002; 269:4427-34; PMID:12230554; http://dx.doi.org/10.1046/j.1432-1033.2002.03133.x.
40. Huang YZ, Won S, Ali DW, Wang Q, Tanowitz M, Du QS, et al. Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 2000; 26:443-55; PMID:10839362; http://dx.doi.org/10.1016/S0896-6273(00)81176-9.
41. Ehlers MD, Zhang S, Bernhadt JP, Huganir RL. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell 1996; 84:745-55; PMID:8625412; http://dx.doi.org/10.1016/S0092-8674(00)81052-1.
42. Vulliet R, Halloran SM, Braun RK, Smith AJ, Lee G. Proline-directed phosphorylation of human Tau protein. J Biol Chem 1992; 267:22570-4; PMID:1429606.
43. Zhang P, Yu PC, Tsang AH, Chen Y, Fu AK, Fu WY, et al. S-nitrosylation of cyclin-dependent kinase 5 (cdk5) regulates its kinase activity and dendrite growth during neuronal development. J Neurosci 2010; 30:14366-70; PMID:20980593; http://dx.doi.org/10.1523/JNEUROSCI.3899-10.2010.
44. Cho DH, Seo J, Park JH, Jo C, Choi YJ, Soh JW, et al. Cyclin-dependent kinase 5 phosphorylates endothelial nitric oxide synthase at serine 116. Hypertension 2010; 55:345-52; PMID:20048197; http://dx.doi.org/10.1161/ HYPERTENSIONAHA.109.140210.
45. Lue LF, Kuo YM, Roher AE, Brachova L, Shen Y, Sue L, et al. Soluble amyloid beta peptide concentration as a predictor of synaptic change in Alzheimer's disease. Am J Pathol 1999; 155:853-62; PMID:10487842; http://dx.doi.org/10.1016/S0002-9440(10)65184-X.
46. McLean CA, Cherny RA, Fraser FW, Fuller SJ, Smith MJ, Beyreuther K, et al. Soluble pool of Abeta amyloid as a determinant of severity of neurodegeneration in Alzheimer's disease. Ann Neurol 1999; 46:860-6; PMID:10589538; http://dx.doi.org/10.1002/1531-8249(199912)46:6〈860:: AIDANA8〉3.0.CO;2-M.
47. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, et al. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991; 30:572-80; PMID:1789684; http://dx.doi.org/10.1002/ana.410300410.
48. Penzes P, Cahill ME, Jones KA, VanLeeuwen JE, Woolfrey KM. Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 2011; 14:285-93; PMID:21346746; http://dx.doi.org/10.1038/nn.2741.
49. Meuer K, Suppanz IE, Lingor P, Planchamp V, Göricke B, Fichtner L, et al. Cyclin-dependent kinase 5 is an upstream regulator of mitochondrial fission during neuronal apoptosis. Cell Death Differ 2007; 14:651-61; PMID:17218957; http://dx.doi.org/10.1038/sj.cdd.4402087.
50. Cartoni R, Martinou JC. Role of mitofusin 2 mutations in the physiopathology of Charcot-Marie-Tooth disease type 2A. Exp Neurol 2009; 218:268-73; PMID:19427854; http://dx.doi.org/10.1016/j.expneurol.2009.05.003.
51. Lawson VH, Graham BV, Flanigan KM. Clinical and electrophysiologic features of CMT2A with mutations in the mitofusin 2 gene. Neurology 2005; 65:197-204; PMID:16043786; http://dx.doi.org/10.1212/01.wnl.0000168898.76071.70.
52. Züchner S, Mersiyanova IV, Muglia M, Bissar-Tadmouri N, Rochelle J, Dadali EL, et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat Genet 2004; 36:449-51; PMID:15064763; http://dx.doi.org/10.1038/ng1341.
53. Alexander C, Votruba M, Pesch UE, Thiselton DL, Mayer S, Moore A, et al. OPA1, encoding a dynamin-related GTPase, is mutated in autosomal dominant optic atrophy linked to chromosome 3q28. Nat Genet 2000; 26:211-5; PMID:11017080; http://dx.doi.org/10.1038/79944.
54. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, et al. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet 2000; 26:207-10; PMID:11017079; http://dx.doi.org/10.1038/79936.
55. Olichon A, Guillou E, Delettre C, Landes T, Arnaune-Pelloquin L, Emorine LJ, et al. Mitochondrial dynamics and disease, OPA1. Biochim Biophys Acta 2006; 1763:500-509.
56. Waterham HR, Koster J, van Roermund CW, Mooyer PA, Wanders RJ, Leonard JV. A lethal defect of mitochondrial and peroxisomal fission. N Engl J Med 2007; 356:1736-41; PMID:17460227; http://dx.doi.org/10.1056/NEJMoa064436.
57. Wang X, Su B, Lee HG, Li X, Perry G, Smith MA, et al. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J Neurosci 2009; 29:9090-103; PMID:19605646; http://dx.doi.org/10.1523/JNEUROSCI.1357-09.2009.
58. Su SC, Tsai LH. Cyclin-dependent kinases in brain development and disease. Annu Rev Cell Dev Biol 2011; 27:465-91; PMID:21740229; http://dx.doi.org/10.1146/annurev-cellbio-092910-154023.
59. Patrick GN, Zukerberg L, Nikolic M, de la Monte S, Dikkes P, Tsai LH. Conversion of p35 to p25 deregulates Cdk5 activity and promotes neurodegeneration. Nature 1999; 402:615-22; PMID:10604467; http://dx.doi.org/10. 1038/45159.
60. Paoletti P, Vila I, Rifé M, Lizcano JM, Alberch J, Ginés S. Dopaminergic and glutamatergic signaling crosstalk in Huntington's disease neurodegeneration: the role of p25/cyclin-dependent kinase 5. J Neurosci 2008; 28:10090-101; PMID:18829967; http://dx.doi.org/10.1523/JNEUROSCI.3237-08.2008.
61. Schmidt HHW, Kelm M. Determination of nitrite and nitrate by the Griess reaction. In: Feelisch M, Stamler JS, eds. Methods in Nitric Oxide Research New York, NY John Wiley and Sons 1996:491-497.