MiR-26b, upregulated in Alzheimer's disease, activates cell cycle entry, Tau-phosphorylation, and apoptosis in postmitotic neurons

Journal of Neuroscience

Volumn 33, Issue 37, 2013, Pages 14645-14659

  Absalon, Sabrina ^a   Kochanek, Dawn M ^a   Raghavan, Venkatesan ^a   Krichevsky, Anna M ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOTIC PROTEASE ACTIVATING FACTOR 1; CASPASE 3; CASPASE 8; CYCLIN DEPENDENT KINASE 5; CYCLIN DEPENDENT KINASE INHIBITOR 1B; CYCLIN E; KI 67 ANTIGEN; MICRORNA; MICRORNA 26B; RETINOBLASTOMA PROTEIN; TAU PROTEIN; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ANIMAL CELL; APOPTOSIS; ARTICLE; CASE REPORT; CELL ACTIVATION; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; DNA REPLICATION; EMBRYO; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MALE; NERVE CELL; NEUROPATHOLOGY; NICK END LABELING; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

ALZHEIMER DISEASE; ANIMALS; APOPTOSIS; BRAIN; CELL CYCLE; CELL SURVIVAL; CELLS, CULTURED; CEREBRAL CORTEX; E2F1 TRANSCRIPTION FACTOR; EMBRYO, MAMMALIAN; FEMALE; FETUS; HUMANS; MALE; MICRORNAS; NERVE TISSUE PROTEINS; NEURONS; RATS; RNA, SMALL INTERFERING; TAU PROTEINS; UP-REGULATION;

EID: 84883732254     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1327-13.2013     Document Type: Article

References (84)

1. Akashiba H, Matsuki N, Nishiyama N (2006) p27 small interfering RNA induces cell death through elevating cell cycle activity in cultured cortical neurons: a proof-of-concept study. Cell Mol Life Sci 63:2397-2404. CrossRef Medline
2. Andorfer C, Acker CM, Kress Y, Hof PR, Duff K, Davies P (2005) Cell-cycle reentry and cell death in transgenic mice expressing nonmutant human tau isoforms. J Neurosci 25:5446-5454. CrossRef Medline
3. Andrusiak MG, Vandenbosch R, Park DS, Slack RS (2012) The retinoblastoma protein is essential for survival of postmitotic neurons. J Neurosci 32:14809-14814. CrossRef Medline
4. Arendt T, Holzer M, Gärtner U, Brückner MK (1998) Aberrancies in signal transduction and cell cycle related events in Alzheimer's disease. J Neural Transm Suppl 54:147-158. Medline
5. Bernocco S, Fondelli C, Matteoni S, Magnoni L, Gotta S, Terstappen GC, Raggiaschi R (2008) Sequential detergent fractionation of primary neurons for proteomics studies. Proteomics 8:930-938. CrossRef Medline
6. Bommer GT, Gerin I, Feng Y, Kaczorowski AJ, Kuick R, Love RE, Zhai Y, Giordano TJ, Qin ZS, Moore BB, MacDougald OA, Cho KR, Fearon ER (2007) p53-mediated activation of miRNA34 candidate tumorsuppressor genes. Curr Biol 17:1298-1307. CrossRef Medline
7. Bonda DJ, Evans TA, Santocanale C, Llosá JC, Vinã J, Bajic V, Castellani RJ, Siedlak SL, Perry G, Smith MA, Lee HG (2009) Evidence for the progression through S-phase in the ectopic cell cycle re-entry of neurons in Alzheimer disease. Aging 1:382-388. Medline
8. Bonda DJ, Lee HP, Kudo W, Zhu X, Smith MA, Lee HG (2010) Pathological implications of cell cycle re-entry in Alzheimer disease. Expert Rev Mol Med 12:e19. CrossRef Medline
9. 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. Medline
10. Byrnes KR, Stoica BA, Fricke S, Di Giovanni S, Faden AI (2007) Cell cycle activation contributes to post-mitotic cell death and secondary damage after spinal cord injury. Brain 130: 2977-2992. CrossRef Medline
11. Cogswell JP, Ward J, Taylor IA, Waters M, Shi Y, Cannon B, Kelnar K, Kemppainen J, Brown D, Chen C, Prinjha RK, Richardson JC, Saunders AM, Roses AD, Richards CA (2008) Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J Alzheimers Dis 14:27-41. Medline
12. de las Cuevas N, Urcelay E, Hermida OG, Saíz-Diaz RA, Bermejo F, Ayuso MS, Martín-Requero A (2003) Ca2+/calmodulin-dependent modulation of cell cycle elements pRb and p27kip1 involved in the enhanced proliferation of lymphoblasts from patients with Alzheimer dementia. Neurobiol Dis 13:254-263. CrossRef Medline
13. Dill H, Linder B, Fehr A, Fischer U (2012) Intronic miR-26b controls neuronal differentiation by repressing its host transcript, ctdsp2. Genes Dev 26:25-30. CrossRef Medline
14. Futatsugi A, Utreras E, Rudrabhatla P, Jaffe H, Pant HC, Kulkarni AB (2012) Cyclin-dependent kinase 5 regulates E2F transcription factor through phosphorylation of Rb protein in neurons. Cell Cycle 11: 1603-1610. CrossRef Medline
15. Fu AK, Hung KW, Wong HH, Fu WY, Ip NY (2013) Cdk5 phosphorylates a component of the HDAC complex and regulates histone acetylation during neuronal cell death. Neurosignals 21:55-60. CrossRef Medline
16. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28:5369-5380. CrossRef Medline
17. Galderisi U, Jori FP, Giordano A (2003) Cell cycle regulation and neural differentiation. Oncogene 22:5208-5219. CrossRef Medline
18. Giovanni A, Keramaris E, Morris EJ, Hou ST, O'Hare M, Dyson N, Robertson GS, Slack RS, Park DS (2000) E2F1 mediates death of B-amyloid-treated cortical neurons in a manner independent of p53 and dependent on Bax and caspase 3. J Biol Chem 275:11553-11560. CrossRef Medline
19. Gómez Ravetti M, Rosso OA, Berretta R, Moscato P (2010) Uncovering molecular biomarkers that correlate cognitive decline with the changes of hippocampus' gene expression profiles in Alzheimer's disease. PLoS One 5:e10153. CrossRef Medline
20. Greene LA, Biswas SC, Liu DX (2004) Cell cycle molecules and vertebrate neuron death: E2F at the hub. Cell Death Differ 11:49-60. CrossRef Medline
21. Hamdane M, Bretteville A, Sambo AV, Schindowski K, Bégard S, Delacourte A, Bertrand P, Buée L (2005) p25/Cdk5-mediated retinoblastoma phosphorylation is an early event in neuronal cell death. J Cell Sci 118: 1291-1298. CrossRef Medline
22. Hammond SM (2006) microRNA detection comes of age. Nat Methods 3:12-13. CrossRef Medline
23. Hébert SS, Horré K, Nicolaï L, Papadopoulou AS, Mandemakers W, Silahtaroglu AN, Kauppinen S, Delacourte A, De Strooper B (2008) Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/beta-secretase expression. Proc Natl Acad Sci U S A 105:6415-6420. CrossRef Medline
24. Hébert SS, Horré K, Nicolaï L, Bergmans B, Papadopoulou AS, Delacourte A, De Strooper B (2009) MicroRNA regulation of Alzheimer's amyloid precursor protein expression. Neurobiol Dis 33:422-428. CrossRef Medline
25. Hermeking H (2009) MiR-34a and p53. Cell Cycle 8:1308. CrossRef Medline
26. Hoozemans JJ, van Haastert ES, Veerhuis R, Arendt T, Scheper W, Eikelenboom P, Rozemuller AJ (2005) Maximal COX-2 and ppRb expression in neurons occurs during early Braak stages prior to the maximal activation of astrocytes and microglia in Alzheimer's disease. J Neuroinflammation 2:27. CrossRef Medline
27. Hou ST, Callaghan D, Fournier MC, Hill I, Kang L, Massie B, Morley P, Murray C, Rasquinha I, Slack R, MacManus JP (2000) The transcription factor E2F1 modulates apoptosis of neurons. J Neurochem 75:91-100. Medline
28. Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, Sohn-Lee C, le Sage C, Agami R, Tuschl T, Holland EC (2009) The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev 23:1327-1337. CrossRef Medline
29. Hwang HW, Mendell JT (2006) MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br J Cancer 94:776-780. CrossRef Medline
30. Illenberger S, Zheng-Fischhöfer Q, Preuss U, Stamer K, Baumann K, Trinczek B, Biernat J, Godemann R, Mandelkow EM, Mandelkow E (1998) The endogenous and cell cycle-dependent phosphorylation of tau protein in living cells: implications for Alzheimer's disease. Mol Biol Cell 9:1495-1512. CrossRef Medline
31. Janicki SM, Monteiro MJ (1999) Presenilin overexpression arrests cells in the G1 phase of the cell cycle. Arrest potentiated by the Alzheimer's disease PS2(N141I)mutant. Am J Pathol 155:135-144. CrossRef Medline
32. Jaworski T, Dewachter I, Lechat B, Croes S, Termont A, Demedts D, Borghgraef P, Devijver H, Filipkowski RK, Kaczmarek L, Kügler S, Van Leuven F (2009) AAV-tau mediates pyramidal neurodegeneration by cell-cycle re-entry without neurofibrillary tangle formation in wild-type mice. PLoS One 4:e7280. CrossRef Medline
33. Jordan-Sciutto KL, Malaiyandi LM, Bowser R (2002) Altered distribution of cell cycle transcriptional regulators during Alzheimer disease. J Neuropathol Exp Neurol 61:358-367. Medline
34. Jordan-Sciutto KL, Dorsey R, Chalovich EM, Hammond RR, Achim CL (2003) Expression patterns of retinoblastoma protein in Parkinson disease. J Neuropathol Exp Neurol 62:68-74. Medline
35. Keeney JT, Swomley AM, Harris JL, Fiorini A, Mitov MI, Perluigi M, Sultana R, Butterfield DA (2012) Cell cycle proteins in brain in mild cognitive impairment: insights into progression to Alzheimer disease. Neurotox Res 22:220-230. CrossRef Medline
36. Kim H, Huang W, Jiang X, Pennicooke B, Park PJ, Johnson MD (2010) Integrative genome analysis reveals an oncomir/oncogene cluster regulating glioblastoma survivorship. Proc Natl Acad Sci U S A 107: 2183-2188. CrossRef Medline
37. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, Chang TC, Vivekanandan P, Torbenson M, Clark KR, Mendell JR, Mendell JT (2009) Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137:1005-1017. CrossRef Medline
38. Krichevsky AM, Kosik KS (2001) Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32: 683-696. CrossRef Medline
39. Lau P, de Strooper B (2010) Dysregulated microRNAs in neurodegenerative disorders. Semin Cell Dev Biol 21:768-773. CrossRef Medline
40. Lee MS, Tsai LH (2003) Cdk5: one of the links between senile plaques and neurofibrillary tangles? J Alzheimers Dis 5:127-137. Medline
41. Liu N, Landreh M, Cao K, Abe M, Hendriks GJ, Kennerdell JR, Zhu Y, Wang LS, Bonini NM (2012) The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 482:519-523. CrossRef Medline
42. Lopes JP, Blurton-Jones M, Yamasaki TR, Agostinho P, LaFerla FM (2009) Activation of cell cycle proteins in transgenic mice in response to neuronal loss but not amyloid-beta and tau pathology. J Alzheimers Dis 16:541-549. Medline
43. Lu J, He ML, Wang L, Chen Y, Liu X, Dong Q, Chen YC, Peng Y, Yao KT, Kung HF, Li XP (2011) MiR-26a inhibits cell growth and tumorigenesis of nasopharyngeal carcinoma through repression of EZH2. Cancer Res 71:225-233. CrossRef Medline
44. Manning AL, Dyson NJ (2011) pRB, a tumor suppressor with a stabilizing presence. Trends Cell Biol 21:433-441. CrossRef Medline
45. Mazanetz MP, Fischer PM (2007) Untangling tau hyperphosphorylation in drug design for neurodegenerative diseases. Nat Rev Drug Discov 6:464-479. CrossRef Medline
46. McShea A, Lee HG, Petersen RB, Casadesus G, Vincent I, Linford NJ, Funk JO, Shapiro RA, Smith MA (2007) Neuronal cell cycle re-entry mediates Alzheimer disease-type changes. Biochim Biophys Acta 1772: 467-472. CrossRef Medline
47. Moh C, Kubiak JZ, Bajic VP, Zhu X, Smith MA, Lee HG (2011) Cell cycle deregulation in the neurons of Alzheimer's disease. Results Probl Cell Differ 53:565-576. CrossRef Medline
48. Munõz U, de Las Cuevas N, Bartolomé F, Hermida OG, Bermejo F, Martín-Requero A (2005) The cyclopentenone 15-deoxy-delta(12,14)-prostaglandin J2 inhibits G1/S transition and retinoblastoma protein phosphorylation in immortalized lymphocytes from Alzheimer's disease patients. Exp Neurol 195:508-517. CrossRef Medline
49. Nagy Z, Esiri MM, Cato AM, Smith AD (1997) Cell cycle markers in the hippocampus in Alzheimer's disease. Acta Neuropathol 94:6-15. CrossRef Medline
50. Neve RL, McPhie DL (2006) The cell cycle as a therapeutic target for Alzheimer's disease. Pharmacol Ther 111:99-113. CrossRef Medline
51. Park DS, Morris EJ, Bremner R, Keramaris E, Padmanabhan J, Rosenbaum M, Shelanski ML, Geller HM, Greene LA (2000) Involvement of retinoblastoma family members and E2F/DP complexes in the death of neurons evoked by DNA damage. J Neurosci 20:3104-3114. Medline
52. Park KH, Hallows JL, Chakrabarty P, Davies P, Vincent I (2007) Conditional neuronal simian virus 40 T antigen expression induces Alzheimerlike tau and amyloid pathology in mice. J Neurosci 27:2969-2978. CrossRef Medline
53. Preuss U, Döring F, Illenberger S, Mandelkow EM (1995) Cell cycledependent phosphorylation and microtubule binding of tau protein stably transfected into Chinese hamster ovary cells. Mol Biol Cell 6:1397-1410. Medline
54. Provost P (2010) Interpretation and applicability of microRNA data to the context of Alzheimer's and age-related diseases. Aging 2:166-169. Medline
55. Ranganathan S, Scudiere S, Bowser R (2001) Hyperphosphorylation of the retinoblastoma gene product and altered subcellular distribution of E2F-1 during Alzheimer's disease and amyotrophic lateral sclerosis. J Alzheimers Dis 3:377-385. Medline
56. 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 U S A 102:14080-14085. CrossRef Medline
57. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858-5868. CrossRef Medline
58. Satoh J (2012) Molecular network of microRNA targets in Alzheimer's disease brains. Exp Neurol 235:436-446. CrossRef Medline
59. Schindowski K, Belarbi K, Bretteville A, Ando K, Buée L (2008) Neurogenesis and cell cycle-reactivated neuronal death during pathogenic tau aggregation. Genes Brain Behav 7 [Suppl]1:92-100. CrossRef Medline
60. Schwartz EI, Smilenov LB, Price MA, Osredkar T, Baker RA, Ghosh S, Shi FD, Vollmer TL, Lencinas A, Stearns DM, Gorospe M, Kruman II (2007) Cell cycle activation in postmitotic neurons is essential for DNA repair. Cell Cycle 6:318-329. CrossRef Medline
61. Sellers WR, Rodgers JW, Kaelin WG Jr (1995) A potent transrepression domain in the retinoblastoma protein induces a cell cycle arrest when bound to E2F sites. Proc Natl Acad SciU S A92: 11544-11548. CrossRef Medline
62. Seward ME, Swanson E, Norambuena A, Reimann A, Cochran JN, Li R, Roberson ED, Bloom GS (2013) Amyloid-beta signals through tau to drive ectopic neuronal cell cycle re-entry in Alzheimer's Disease. J Cell Sci 126:1278-1286. CrossRef Medline
63. Sheaff RJ, Groudine M, Gordon M, Roberts JM, Clurman BE (1997) Cyclin E-CDK2 is a regulator of p27Kip1. Genes Dev 11:1464-1478. CrossRef Medline
64. Smith DS, Leone G, DeGregori J, Ahmed MN, Qumsiyeh MB, Nevins JR (2000) Induction of DNA replication in adult rat neurons by deregulation of the retinoblastoma/E2F G1 cell cycle pathway. Cell Growth Differ 11:625-633. Medline
65. Smith MZ, Nagy Z, Esiri MM (1999) Cell cycle-related protein expression in vascular dementia and Alzheimer's disease. Neurosci Lett 271: 45-48. CrossRef Medline
66. Smith PY, Delay C, Girard J, Papon MA, Planel E, Sergeant N, Buée L, Hébert SS (2011) MicroRNA-132 loss is associated with tau exon 10 inclusion in progressive supranuclear palsy. Hum Mol Genet 20: 4016-4024. CrossRef Medline
67. Stone JG, Siedlak SL, Tabaton M, Hirano A, Castellani RJ, Santocanale C, Perry G, Smith MA, Zhu X, Lee HG (2011) The cell cycle regulator phosphorylated retinoblastoma protein is associated with tau pathology in several tauopathies. J Neuropathol Exp Neurol 70:578-587. CrossRef Medline
68. Swerdlow RH (2012) Alzheimer's disease pathologic cascades: who comes first, what drives what. Neurotox Res 22:182-194. CrossRef Medline
69. Thakur A, Siedlak SL, James SL, Bonda DJ, Rao A, Webber KM, Camins A, Pallàs M, Casadesus G, Lee HG, Bowser R, Raina AK, Perry G, Smith MA, Zhu X (2008) Retinoblastoma protein phosphorylation at multiple sites is associated with neurofibrillary pathology in Alzheimer disease. Int J Clin Exp Pathol 1:134-146. Medline
70. Vilardo E, Barbato C, Ciotti M, Cogoni C, Ruberti F (2010) MicroRNA-101 regulates amyloid precursor protein expression in hippocampal neurons. J Biol Chem 285:18344-18351. CrossRef Medline
71. 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. Medline
72. Vlach J, Hennecke S, Amati B (1997) Phosphorylation-dependent degradation of the cyclin-dependent kinase inhibitor p27. EMBO J 16: 5334-5344. CrossRef Medline
73. Wang WX, Huang Q, Hu Y, Stromberg AJ, Nelson PT (2011) Patterns of microRNA expression in normal and early Alzheimer's disease human temporal cortex: white matter versus gray matter. Acta Neuropathol 121: 193-205. CrossRef Medline
74. Wong HK, Veremeyko T, Patel N, Lemere CA, Walsh DM, Esau C, Vanderburg C, Krichevsky AM (2013) De-repression of FOXO3a death axis by microRNA-132 and -212 causes neuronal apoptosis in Alzheimer's disease. Hum Mol Genet 22:3077-3092. CrossRef Medline
75. Yang Y, Geldmacher DS, Herrup K (2001) DNA replication precedes neuronal cell death in Alzheimer's disease. J Neurosci 21:2661-2668. Medline
76. Ye W, Blain SW (2010) S phase entry causes homocysteine-induced death while ataxia telangiectasia and Rad3 related protein functions antiapoptotically to protect neurons. Brain 133: 2295-2312. CrossRef Medline
77. Yoshida A, Yoneda-Kato N, Kato JY (2013) CSN5 specifically interacts with CDK2 and controls senescence in a cytoplasmic cyclin E-mediated manner. Sci Rep 3:1054. Medline
78. Yurov YB, Vorsanova SG, Iourov IY (2011) The DNA replication stress hypothesis of Alzheimer's disease. ScientificWorldJournal 11:2602-2612. CrossRef Medline
79. Zhang J, Li H, Herrup K (2010) Cdk5 nuclear localization is p27-dependent in nerve cells: implications for cell cycle suppression and caspase-3 activation. J Biol Chem 285:14052-14061. CrossRef Medline
80. Zhang J, Herrup K (2008) Cdk5 and the non-catalytic arrest of the neuronal cell cycle. Cell Cycle 7:3487-3490. CrossRef Medline
81. Zhang J, Cicero SA, Wang L, Romito-Digiacomo RR, Yang Y, Herrup K (2008) Nuclear localization of Cdk5 is a key determinant in the postmitotic state of neurons. Proc Natl Acad SciU S A 105:8772-8777. CrossRef Medline
82. Zhu Y, Lu Y, Zhang Q, Liu JJ, Li TJ, Yang JR, Zeng C, Zhuang SM (2012a) MicroRNA-26a/b and their host genes cooperate to inhibit the G1/S transition by activating thepRbprotein. Nucleic Acids Res 40:4615-4625. CrossRef Medline
83. Zhu HC, Wang LM, Wang M, Song B, Tan S, Teng JF, Duan DX (2012b) MicroRNA-195 downregulates Alzheimer's disease amyloid-beta production by targeting BACE1. Brain Res Bull 88:596-601. CrossRef Medline
84. Zovoilis A, Agbemenyah HY, Agis-Balboa RC, Stilling RM, Edbauer D, Rao P, Farinelli L, Delalle I, Schmitt A, Falkai P, Bahari-Javan S, Burkhardt S, Sananbenesi F, Fischer A (2011) microRNA-34c is a novel target to treat dementias. EMBO J 30:4299-4308. CrossRef Medline