Insights into the regulation of neuronal viability by nucleophosmin/B23

Experimental Biology and Medicine

Volumn 240, Issue 6, 2015, Pages 774-786

  Pfister, Jason A ^a   D’Mello, Santosh R ^a,b  

^a UNIVERSITY OF TEXAS AT DALLAS   (United States)

^b SOUTHERN METHODIST UNIVERSITY   (United States)

Author keywords

cell cycle; Huntington's disease; neurodegeneration; neurons; nucleolus; Nucleophosmin

Indexed keywords

ARF PROTEIN; ATR PROTEIN; CASEIN KINASE II; CASPASE ACTIVATED DEOXYRIBONUCLEASE; CYCLIN DEPENDENT KINASE 1; CYCLIN E; DNA DIRECTED RNA POLYMERASE III; EXPORTIN 1; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; K RAS PROTEIN; MANGANESE SUPEROXIDE DISMUTASE; MITOGEN ACTIVATED PROTEIN KINASE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 2; NUCLEOPHOSMIN; PROTEIN BAX; PROTEIN KINASE B; PROTEIN KINASE B BETA; PROTEIN MDM2; PROTEIN P21; PROTEIN P53; REDOX EFFECTOR FACTOR 1; RIBOSOME DNA; RIBOSOME RNA; RNA 28S; RNA 5S; THYROID TRANSCRIPTION FACTOR 1; TRANSCRIPTION FACTOR E2F1; TRANSCRIPTION FACTOR RELA; UNINDEXED DRUG; NUCLEAR PROTEIN;

APOPTOSIS; ARTICLE; BIOGENESIS; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL STRESS; CELL VIABILITY; CELLULAR DISTRIBUTION; CENTROSOME; DNA DAMAGE; EXCITOTOXICITY; GENOMIC INSTABILITY; HUMAN; HUNTINGTON CHOREA; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SPINAL CORD INJURY; ANIMAL; CELL SURVIVAL; GENETICS; METABOLISM; MITOSIS; NEURODEGENERATIVE DISEASES; PATHOLOGY;

ANIMALS; CELL SURVIVAL; GENOMIC INSTABILITY; HUMANS; MITOSIS; NEURODEGENERATIVE DISEASES; NEURONS; NUCLEAR PROTEINS;

EID: 84930814601     PISSN: 15353702     EISSN: 15353699     Source Type: Journal    
DOI: 10.1177/1535370215579168     Document Type: Article

References (114)

1. Yung BYM.Oncogenic role of nucleophosmin/B23.Chang Gung Med J. 2007;30:285-93
2. Grisendi S,Mecucci C,Falini B,Pandolfi PP.Nucleophosmin and cancer.Nat Rev Cancer. 2006;6:493-5
3. Yu Y,Maggi LB,Brady SN,Apicelli AJ,Dai M-S,Lu H,Weber JD.Nucleophosmin is essential for ribosomal protein L5 nuclear export.Mol Cell Biol. 2006;26:3798-809
4. Wang W,Budhu A,Forgues M,Wang XW.Temporal and spatial control of nucleophosmin by the Ran-Crm1 complex in centrosome duplication.Nat Cell Biol. 2005;7:823-30
5. Frehlick LJ,Eirín-López JM,Ausió J.New insights into the nucleophosmin/nucleoplasmin family of nuclear chaperones.BioEssays. 2007;29:49-59
6. Sloan KE,Mattijssen S,Lebaron S,Tollervey D,Pruijn GJM,Watkins NJ.Both endonucleolytic and exonucleolytic cleavage mediate ITS1 removal during human ribosomal RNA processing.J Cell Biol. 2013;200:577-88
7. Savkur RS,Olson MOJ.Preferential cleavage in pre-ribosomal RNA by protein B23 endoribonuclease.Nucleic Acid Res. 1998;26:4508-15
8. Vascotto C,Fantini D,Romanello M,Cesaratto L,Deganuto M,Leonardi A,Radicella JP,Kelley MR,D’Ambrosio C,Scaloni A,Quadrifoglio F,Tell G.APE1/Ref-1 interacts with NPM1 within nucleoli and plays a role in the rRNA quality control process.Mol Cell Biol. 2009;29:1834-54
9. Meder VS,Boeglin M,de Murcia G,Schreiber V.PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli.J Cell Sci. 2005;118:211-22
10. Hernandez-Verdun D.Assembly and disassembly of the nucleolus during the cell cycle.Nucleus. 2014;2:189-94
11. Okuwaki M,Tsujimoto M,Nagata K.The RNA binding activity of a ribosome biogenesis factor, nucleophosmin/B23, is modulated by phosphorylation with a cell cycle-dependent kinase and by association with its subtype.Mol Biol Cell. 2002;13:2016-30
12. Negi SS,Olson MOJ.Effects of interphase and mitotic phosphorylation on the mobility and location of nucleolar protein B23.J Cell Sci. 2006;119:3676-85
13. Huang N,Negi S,Szebeni A,Olson MOJ.Protein NPM3 interacts with the multifunctional nucleolar protein B23/nucleophosmin and inhibits ribosome biogenesis.J Biol Chem. 2005;280:5496-502
14. Hingorani K,Szebeni A,Olson MO.Mapping the functional domains of nucleolar protein B23.J Biol Chem. 2000;275:24451-7
15. Szebeni A,Hingorani K,Negi S,Olson MOJ.Role of protein kinase CK2 phosphorylation in the molecular chaperone activity of nucleolar protein b23.J Biol Chem. 2003;278:9107-15
16. Maggi LB,Kuchenruether M,Dadey DYA,Schwope RM,Grisendi S,Townsend RR,Pandolfi PP,Weber JD.Nucleophosmin serves as a rate-limiting nuclear export chaperone for the Mammalian ribosome.Mol Cell Biol. 2008;28:7050-65
17. Okuwaki M,Matsumoto K,Tsujimoto M,Nagata K.Function of nucleophosmin/B23, a nucleolar acidic protein, as a histone chaperone.FEBS Lett. 2001;506:272-6
18. Kotsinas A,Papanagnou P,Evangelou K,Trigas GC,Kostourou V,Townsend P,Gorgoulis VG.ARF: a versatile DNA damage response ally at the crossroads of development and tumorigenesis.Front Genet. 2014;5:236-236
19. Ayrault O,Andrique L,Larsen C-J,Seite P.Human Arf tumor suppressor specifically interacts with chromatin containing the promoter of rRNA genes.Oncogene. 2004;23:8097-4
20. Apicelli AJ,Maggi LB,Hirbe AC,Miceli AP,Olanich ME,Schulte-Winkeler CL,Saporita AJ,Kuchenreuther M,Sanchez J,Weilbaecher K,Weber JD.A non-tumor suppressor role for basal p19ARF in maintaining nucleolar structure and function.Mol Cell Biol. 2008;28:1068-80
21. Lessard F,Morin F,Ivanchuk S,Langlois F,Stefanovsky V,Rutka J,Moss T.The ARF tumor suppressor controls ribosome biogenesis by regulating the RNA polymerase I transcription factor TTF-I.Mol Cell. 2010;38:539-50
22. Lessard F,Stefanovsky V,Tremblay MG,Moss T.The cellular abundance of the essential transcription termination factor TTF-I regulates ribosome biogenesis and is determined by MDM2 ubiquitinylation.Nucleic Acid Res. 2012;40:5357-67
23. Liu X,Liu Z,Jang S-W,Ma Z,Shinmura K,Kang S,Dong S,Chen J,Fukasawa K,Ye K.Sumoylation of nucleophosmin/B23 regulates its subcellular localization, mediating cell proliferation and survival.Proc Natl Acad Sci U S A. 2007;104:9679-84
24. Haindl M,Harasim T,Eick D,Muller S.The nucleolar SUMO-specific protease SENP3 reverses SUMO modification of nucleophosmin and is required for rRNA processing.EMBO Rep. 2008;9:273-9
25. Kuo M-L,den Besten W,Thomas MC,Sherr CJ.Arf-induced turnover of the nucleolar nucleophosmin-associated SUMO-2/3 protease Senp3.Cell Cycle. 2014;7:3378-87
26. Okuda M,Horn HF,Tarapore P,Tokuyama Y,Smulian AG,Chan PK,Knudsen ES,Hofmann IA,Snyder JD,Bove KE,Fukasawa K.Nucleophosmin/B23 is a target of CDK2/cyclin E in centrosome duplication.Cell. 2000;103:127-40
27. Tokuyama Y,Horn HF,Kawamura K,Tarapore P,Fukasawa K.Specific Phosphorylation of nucleophosmin on Thr199 by cyclin-dependent kinase 2-cyclin e and its role in centrosome duplication.J Biol Chem. 2001;276:21529-37
28. Ma Z,Kanai M,Kawamura K,Kaibuchi K,Ye K,Fukasawa K.Interaction between ROCK II and nucleophosmin/B23 in the regulation of centrosome duplication.Mol Cell Biol. 2006;26:9016-34
29. Kanai M,Crowe MS,Zheng Y,Vande Woude GF,Fukasawa K.RhoA and RhoC are both required for the ROCK II-dependent promotion of centrosome duplication.Oncogene. 2010;29:6040-50
30. Shinmura K,Tarapore P,Tokuyama Y,George KR,Fukasawa K.Characterization of centrosomal association of nucleophosmin/B23 linked to Crm1 activity.FEBS Lett. 2005;579:6621-34
31. Fornerod M,Ohno M,Yoshida M,Mattaj IW.CRM1 is an export receptor for leucine-rich nuclear export signals.Cell. 1997;90:1051-60
32. Forgues M,Difilippantonio MJ,Linke SP,Ried T,Nagashima K,Feden J,Valerie K,Fukasawa K,Wang XW.Involvement of Crm1 in hepatitis B virus X protein-induced aberrant centriole replication and abnormal mitotic spindles.Mol Cell Biol. 2003;23:5282-92
33. Zhang H,Shi X,Paddon H,Hampong M,Dai W,Pelech S.B23/nucleophosmin serine 4 phosphorylation mediates mitotic functions of Polo-like kinase 1.J Biol Chem. 2004;279:35726-34
34. Krause A,Hoffmann I.Polo-like kinase 2-dependent phosphorylation of NPM/ B23 on serine 4 triggers centriole duplication.PLoS ONE. 2010;5 (3): e9849-e9849
35. Li J,Zhang X,Sejas DP,Pang Q.Negative regulation of p53 by nucleophosmin antagonizes stress-induced apoptosis in human normal and malignant hematopoietic cells.Leuk Res. 2005;29:1415-23
36. Brady SN,Yu Y,Maggi LB,Weber JD.ARF impedes NPM/B23 shuttling in an Mdm2-sensitive tumor suppressor pathway.Mol Cell Biol. 2004;24:9327-38
37. Kurki S,Peltonen K,Latonen L,Kiviharju TM,Ojala PM,Meek D,Laiho M.Nucleolar protein NPM interacts with HDM2 and protects tumor suppressor protein p53 from HDM2-mediated degradation.Cancer Cell. 2004;5:465-75
38. Colombo E,Marine J-C,Danovi D,Falini B,Pelicci PG.Nucleophosmin regulates the stability and transcriptional activity of p53.Nat Cell Biol. 2002;4:529-33
39. Maiguel DA,Jones L,Chakravarty D,Yang C,Carrier F.Nucleophosmin sets a threshold for p53 response to UV radiation.Mol Cell Biol. 2004;24:3703-11
40. Xiao J,Zhang Z,Chen GG,Zhang M,Ding Y,Fu J,Li M,Yun JP.Nucleophosmin/B23 interacts with p21WAF1/CIP1 and contributes to its stability.Cell Cycle. 2009;8:889-95
41. Jackson JG,Pereira-Smith OM.p53 is preferentially recruited to the promoters of growth arrest genes p21 and GADD45 during replicative senescence of normal human fibroblasts.Cancer Res. 2006;66:8356-60
42. Zhao H,Jin S,Antinore MJ,Lung FD,Fan F,Blanck P,Roller P,Fornace AJ,Zhan Q.The central region of Gadd45 is required for its interaction with p21/WAF1.Exp Cell Res. 2000;258:92-100
43. Gao H,Jin S,Song Y,Fu M,Wang M,Liu Z,Wu M,Zhan Q.B23 regulates GADD45a nuclear translocation and contributes to GADD45a-induced cell cycle G2-M arrest.J Biol Chem. 2005;280:10988-96
44. Korgaonkar C,Hagen J,Tompkins V,Frazier AA,Allamargot C,Quelle FW,Quelle DE.Nucleophosmin (B23) targets ARF to nucleoli and inhibits its function.Mol Cell Biol. 2005;25:1258-71
45. Colombo E,Bonetti P,Lazzerini Denchi E,Martinelli P,Zamponi R,Marine J-C,Helin K,Falini B,Pelicci PG.Nucleophosmin is required for DNA integrity and p19Arf protein stability.Mol Cell Biol. 2005;25:8874-86
46. Kuo ML,Den Besten W,Bertwistle D,Roussel MF,Sherr CJ.N-terminal polyubiquitination and degradation of the Arf tumor suppressor.Genes Dev. 2004;18:1862-74
47. Colombo E,Martinelli P,Zamponi R,Shing DC,Bonetti P,Luzi L,Volorio S,Bernard L,Pruneri G,Alcalay M,Pelicci PG.Delocalization and destabilization of the Arf tumor suppressor by the leukemia-associated NPM mutant.Cancer Res. 2006;66:3044-50
48. Itahana K,Bhat KP,Jin A,Itahana Y,Hawke D,Kobayashi R,Zhang Y.Tumor suppressor ARF degrades B23, a nucleolar protein involved in ribosome biogenesis and cell proliferation.Mol Cell. 2003;12:1151-64
49. Hamilton G,Abraham AG,Morton J,Sampson O,Pefani DE,Khoronenkova S,Grawenda A,Papaspyropoulos A,Jamieson N,McKay C,Sansom O,Dianov GL,O’Neill E.AKT regulates NPM dependent ARF localization and p53mut stability in tumors.Oncotarget. 2014;:
50. Lee C,Smith BA,Bandyopadhyay K,Gjerset RA.DNA damage disrupts the p14ARF-B23(nucleophosmin) interaction and triggers a transient subnuclear redistribution of p14ARF.Cancer Res. 2005;65:9834-42
51. Yogev O,Saadon K,Anzi S,Inoue K,Shaulian E.DNA damage-dependent translocation of B23 and p19ARF is regulated by the Jun N-terminal kinase pathway.Cancer Res. 2008;68:1398-406
52. Vietri M,Bianchi M,Ludlow JW,Mittnacht S,Villa-Moruzzi E.Direct interaction between the catalytic subunit of protein phosphatase 1 and pRb.Cancer Cell Int. 2006;6:3-3
53. Cicchillitti L,Fasanaro P,Biglioli P,Capogrossi MC,Martelli F.Oxidative stress induces protein phosphatase 2A-dependent dephosphorylation of the pocket proteins pRb, p107, and p130.J Biol Chem. 2003;278:19509-17
54. Takemura M,Ohoka F,Perpelescu M,Ogawa M,Matsushita H,Takaba T,Akiyama T,Umekawa H,Furuichi Y,Cook PR,Yoshida S.Phosphorylation-dependent migration of retinoblastoma protein into the nucleolus triggered by binding to nucleophosmin/B23.Exp Cell Res. 2002;276:233-41
55. Lin CY,Tan BC-M,Liu H,Shih C-J,Chien K-Y,Lin C-L,Yung BY-M.Dephosphorylation of nucleophosmin by PP1β facilitates pRB binding and consequent E2F1-dependent DNA repair.Mol Biol Cell. 2010;21:4409-17
56. Ahn JY,Liu X,Cheng D,Peng J,Chan PK,Wade PA,Ye K.Nucleophosmin/B23, a nuclear PI(3,4,5)P3 receptor, mediates the antiapoptotic actions of NGF by inhibiting CAD.Mol Cell. 2005;18:435-45
57. Choi JW,Lee SB,Kim CK,Lee K-H,Cho S-W,Ahn J-Y.Lysine 263 residue of NPM/B23 is essential for regulating ATP binding and B23 stability.FEBS Lett. 2008;582:1073-80
58. Choi JW,Lee SB,Ahn J-Y,Lee K-H.Disruption of ATP binding destabilizes NPM/B23 and inhibits anti-apoptotic function.BMB Rep. 2008;41:840-5
59. Kwon I,Lee K-H,Choi J-W,Ahn J-Y.PI(3,4,5)P3 regulates the interaction between Akt and B23 in the nucleus.BMB Rep. 2010;43:127-32
60. Lee SB,Xuan Nguyen TL,Choi JW,Lee K-H,Cho S-W,Liu Z,Ye K,Bae SS,Ahn J-Y.Nuclear Akt interacts with B23/NPM and protects it from proteolytic cleavage, enhancing cell survival.Proc Natl Acad Sci U S A. 2008;105:16584-9
61. Kim CK,Nguyen TLX,Lee SB,Park SB,Lee KH,Cho SW,Ahn JY.Akt2 and nucleophosmin/B23 function as an oncogenic unit in human lung cancer cells.Exp Cell Res. 2011;317:966-75
62. Hsu CY,Yung BY.Down-regulation of nucleophosmin/B23 during retinoic acid-induced differentiation of human promyelocytic leukemia HL-60 cells.Oncogene. 1998;16:915-23
63. Hsu CY,Yung BY.Over-expression of nucleophosmin/B23 decreases the susceptibility of human leukemia HL-60 cells to retinoic acid-induced differentiation and apoptosis.Int J Cancer. 2000;88:392-400.
64. Liu WH,Yung BY.Mortalization of human promyelocytic leukemia HL-60 cells to be more susceptible to sodium butyrate-induced apoptosis and inhibition of telomerase activity by down-regulation of nucleophosmin/B23.Oncogene. 1998;17:3055-64
65. Chou CC,Yung BYM,Hsu CY.Involvement of nPKC-MAPK pathway in the decrease of nucleophosmin/B23 during megakaryocytic differentiation of human myelogenous leukemia K562 cells.Life Sci. 2007;80:2051-9
66. Liu H,Tan BC-M,Tseng KH,Chuang CP,Yeh C-W,Chen K-D,Lee S-C,Yung BY-M.Nucleophosmin acts as a novel AP2alpha-binding transcriptional corepressor during cell differentiation.EMBO Rep. 2007;8:394-400
67. Inder KL,Lau C,Loo D,Chaudhary N,Goodall A,Martin S,Jones A,Van der Hoeven D,Parton RG,Hill MM,Hancock JF.Nucleophosmin and nucleolin regulate K-ras plasma membrane interactions and MAPK signal transduction.J Biol Chem. 2009;284:28410-9
68. Falini B,Nicoletti I,Martelli MF,Mecucci C.Acute myeloid leukemia carrying cytoplasmic/mutated nucleophosmin (NPMc + AML): Biologic and clinical features.Blood. 2007;109:874-85
69. Huang M,Thomas D,Li MX,Feng W,Chan SM,Majeti R,Mitchell BS.Role of cysteine 288 in nucleophosmin cytoplasmic mutations: sensitization to toxicity induced by arsenic trioxide and bortezomib.Leukemia. 2013;27:1970-80
70. Stark LA,Dunlop MG.Nucleolar sequestration of RelA (p65) regulates NF-kappaB-driven transcription and apoptosis.Mol Cell Biol. 2005;25:5985-6004
71. Thoms HC,Dunlop MG,Stark LA.p38-mediated inactivation of cyclin D1/cyclin-dependent kinase 4 stimulates nucleolar translocation of RelA and apoptosis in colorectal cancer cells.Cancer Res. 2007;67:1660-9
72. Thoms HC,Dunlop MG,Stark LA.CDK4 inhibitors and apoptosis: A novel mechanism requiring nucleolar targeting of RelA.Cell Cycle. 2007;6:1293-7
73. Khandelwal N,Simpson J,Taylor G,Rafique S,Whitehouse A,Hiscox J,Stark LA.Nucleolar NF-κB/RelA mediates apoptosis by causing cytoplasmic relocalization of nucleophosmin.Cell Death Differ. 2011;18:1889-903
74. Ryan KM,Ernst MK,Rice NR,Vousden KH.Role of NF-kappaB in p53-mediated programmed cell death.Nature. 2000;404:892-7
75. Din FVN,Stark LA,Dunlop MG.Aspirin-induced nuclear translocation of NFkappaB and apoptosis in colorectal cancer is independent of p53 status and DNA mismatch repair proficiency.Br J Cancer. 2005;92:1137-43
76. Geng Y,Walls KC,Ghosh AP,Akhtar RS,Klocke BJ,Roth KA.Cytoplasmic p53 and activated Bax regulate p53-dependent, transcription-independent neural precursor cell apoptosis.J Histochem Cytochem. 2010;58:265-75
77. Dhar SK,Clair DK.Nucleophosmin blocks mitochondrial localization of p53 and apoptosis.J Biol Chem. 2009;284:16409-18
78. Li Y,Bhuiyan M,Mohammad RM,Sarkar FH.Induction of apoptosis in breast cancer cells by TPA.Oncogene. 1998;17:2915-20
79. Grisendi S,Bernardi R,Rossi M,Cheng K,Khandker L,Manova K,Pandolfi PP.Role of nucleophosmin in embryonic development and tumorigenesis.Nature. 2005;437:147-53
80. Qing Y,Yingmao G,Lujun B,shaoling L.Role of Npm1 in proliferation, apoptosis and differentiation of neural stem cells.J Neurol Sci. 2008;266:131-7
81. Nishio Y,Koda M,Kamada T,Someya Y,Kadota R,Mannoji C,Miyashita T,Okada S,Okawa A,Moriya H,Yamazaki M.Granulocyte colony-stimulating factor attenuates neuronal death and promotes functional recovery after spinal cord injury in mice.J Neuropathol Exp Neurol. 2007;66:724-31
82. Guo Y,Liu S,Wang P,Zhang H,Wang F,Bing L,Gao J,Yang J,Hao A.Granulocyte colony-stimulating factor improves neuron survival in experimental spinal cord injury by regulating nucleophosmin-1 expression.J Neurosci Res. 2014;92:751-60
83. Qi W,Shakalya K,Stejskal a,Goldman a,Beeck S,Cooke L,Mahadevan D.NSC348884, a nucleophosmin inhibitor disrupts oligomer formation and induces apoptosis in human cancer cells.Oncogene. 2008;27:4210-20
84. Maezawa I,Wang B,Hu Q,Martin GM,Jin LW,Oshima J.Alterations of chaperone protein expression in presenilin mutant neurons in response to glutamate excitotoxicity.Pathol Int. 2002;52:551-4
85. Lee SB,Kim CK,Lee KH,Ahn JY.S-nitrosylation of B23/nucleophosmin by GAPDH protects cells from the SIAH1-GAPDH death cascade.J Cell Biol. 2012;199:65-76
86. Marquez-Lona EM,Tan Z,Schreiber SS.Nucleolar stress characterized by downregulation of nucleophosmin: A novel cause of neuronal degeneration.Biochem Biophys Res Commun. 2012;417:514-20
87. Folch J,Junyent F,Verdaguer E,Auladell C,Pizarro JG,Beas-Zarate C,Pallàs M,Camins A.Role of cell cycle re-entry in neurons: A common apoptotic mechanism of neuronal cell death.Neurotox Res. 2012;22:195-207
88. Lim ACB,Qi RZ.Cyclin-dependent kinases in neural development and degeneration.J Alzheimers Dis. 2003;5:329-35
89. Ranganathan S,Bowser R.Alterations in G(1) to S phase cell-cycle regulators during amyotrophic lateral sclerosis.Am J Pathol. 2003;162:823-35
90. Neve RL,McPhie DL.The cell cycle as a therapeutic target for Alzheimer’s disease.Pharmacol Ther. 2006;111:99-113
91. Pelegrí C,Duran-Vilaregut J,del Valle J,Crespo-Biel N,Ferrer I,Pallàs M,Camins A,Vilaplana J.Cell cycle activation in striatal neurons from Huntington’s disease patients and rats treated with 3-nitropropionic acid.Int J Dev Neurosci. 2008;26:665-71
92. Uttara B,Singh AV,Zamboni P,Mahajan RT.Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options.Curr Neuropharmacol. 2009;7:65-74
93. Flynn JM,Melovn S.SOD2 in mitochondrial dysfunction and neurodegeneration.Free Radic Biol Med. 2013;62:4-12
94. Dhar SK,Lynn BC,Daosukho C,Clair DK.Identification of nucleophosmin as an NF-κB co-activator for the induction of the human SOD2 gene.J Biol Chem. 2004;279:28209-19
95. Hou ST,Cowan E,Walker T,Ohan N,Dove M,Rasqinha I,MacManus JP.The transcription factor E2F1 promotes dopamine-evoked neuronal apoptosis by a mechanism independent of transcriptional activation.J Neurochem. 2001;78:287-97
96. Verdaguer E,Jiménez A,Canudas AM,Jordà EG,Sureda FX,Pallàs M,Camins A.Inhibition of cell cycle pathway by flavopiridol promotes survival of cerebellar granule cells after an excitotoxic treatment.J Pharmacol Exp Ther. 2004;308:609-16
97. Höglinger GU,Breunig JJ,Depboylu C,Rouaux C,Michel PP,Alvarez-Fischer D,Boutillier A-L,Degregori J,Oertel WH,Rakic P,Hirsch EC,Hunot S.The pRb/E2F cell-cycle pathway mediates cell death in Parkinson’s disease.Proc Natl Acad Sci U S A. 2007;104:3585-90
98. Jordan-Sciutto KL,Dorsey R,Chalovich EM,Hammond RR,Achim CL.Expression patterns of retinoblastoma protein in Parkinson disease.J Neuropathol Exp Neurol. 2003;62:68-74
99. Saal K-A,Koch JC,Tatenhorst L,Szegő EM,Ribas VT,Michel U,Bähr M,Tönges L,Lingor P.AAV.shRNA-mediated downregulation of ROCK2 attenuates degeneration of dopaminergic neurons in toxin-induced models of Parkinson’s disease in vitro and in vivo.Neurobiol Dis. 2014;73:150-162
100. Herskowitz JH,Feng Y,Mattheyses AL,Hales CM,Higginbotham La,Duong DM,Montine TJ,Troncoso JC,Thambisetty M,Seyfried NT,Levey AI,Lah JJ.Pharmacologic inhibition of ROCK2 suppresses amyloid-β production in an Alzheimer’s disease mouse model.J Neurosci. 2013;33:19086-98
101. Song B,Davis K,Liu XS,Lee H,Smith M,Liu X.Inhibition of Polo ‐ like kinase 1 reduces beta ‐ amyloid ‐ induced neuronal cell death in Alzheimer’s disease. 2011;3:846-51
102. Bergeron M,Motter R,Tanaka P,Fauss D,Babcock M,Chiou Ss,Nelson S,San Pablo F,Anderson JP.In vivo modulation of polo-like kinases supports a key role for PLK2 in Ser129 α-synuclein phosphorylation in mouse brain.Neuroscience. 2014;256:72-82
103. Choi HJ,Kang KS,Fukui M,Zhu BT.Critical role of the JNK-p53-GADD45alpha apoptotic cascade in mediating oxidative cytotoxicity in hippocampal neurons.Br J Pharmacol. 2011;162:175-92
104. Lin CR,Yang CH,Huang CE,Wu CH,Chen YS,Sheen-Chen SM,Huang HW,Chen KH.GADD45A protects against cell death in dorsal root ganglion neurons following peripheral nerve injury.J Neurosci Res. 2011;89:689-99
105. Hetman M,Pietrzak M.Emerging roles of the neuronal nucleolus.Trends Neurosci. 2012;35:305-14
106. Ding Q,Markesbery WR,Chen Q,Li F,Keller JN.Ribosome dysfunction is an early event in Alzheimer’s disease.J Neurosci. 2005;25:9171-5
107. Ding Q,Markesbery WR,Cecarini V,Keller JN.Decreased RNA, and increased RNA oxidation, in ribosomes from early Alzheimer’s disease.Neurochem Res. 2006;31:705-10
108. Pietrzak M,Rempala G,Nelson PT,Zheng JJ,Hetman M.Epigenetic silencing of nucleolar rRNA genes in Alzheimer’s disease.PLoS ONE. 2011;6 (7): e22585-e22585
109. Tsoi H, Chan HYE. Expression of expanded CAG transcripts triggers nucleolar stress in huntington s disease. Cerebellum 2013;12:310–312.
110. Lee J,Hwang YJ,Ryu H,Kowall NW,Ryu H.Nucleolar dysfunction in Huntington’s disease.Biochim Biophys Acta Mol Basis Dis. 2014;1842:785-90
111. Kalita K,Makonchuk D,Gomes C,Zheng JJ,Hetman M.Inhibition of nucleolar transcription as a trigger for neuronal apoptosis.J Neurochem. 2008;105:2286-99
112. Parlato R,Kreiner G,Erdmann G,Rieker C,Stotz S,Savenkova E,Berger S,Grummt I,Schütz G.Activation of an endogenous suicide response after perturbation of rRNA synthesis leads to neurodegeneration in mice.J Neurosci. 2008;28:12759-64
113. Rieker C,Engblom D,Kreiner G,Domanskyi A,Schober A,Stotz S,Neumann M,Yuan X,Grummt I,Schütz G,Parlato R.Nucleolar disruption in dopaminergic neurons leads to oxidative damage and parkinsonism through repression of mammalian target of rapamycin signaling.J Neurosci. 2011;31:453-60
114. Kreiner G,Bierhoff H,Armentano M,Rodriguez-Parkitna J,Sowodniok K,Naranjo JR,Bonfanti L,Liss B,Schutz G,Grummt I,Parlato R.A neuroprotective phase precedes striatal degeneration upon nucleolar stress.Cell Death Differ. 2013;20:1455-64