Lafora disease E3 ubiquitin ligase malin is recruited to the processing bodies and regulates the microRNA-mediated gene silencing process via the decapping enzyme Dcp1a

RNA Biology

Volumn 9, Issue 12, 2012, Pages 1440-1449

  Singh, Sweta ^a   Singh, Pankaj Kumar ^a   Bhadauriya, Pratibha ^a   Ganesh, Subramaniam ^a  

^a INDIAN INSTITUTE OF TECHNOLOGY KANPUR   (India)

Author keywords

Epilepsy; mRNA dysregulation; Neurodegenerative disorder; Neuronal processing bodies; Post translational modification; RNA granules; Stress response

Indexed keywords

DCP1A PROTEIN; MALIN; MICRORNA; PROTEASOME; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; CELL ASSAY; CONTROLLED STUDY; ENZYME DEGRADATION; GENE ACTIVITY; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; IMMUNOPRECIPITATION; MYOCLONUS EPILEPSY; UBIQUITINATION;

EID: 84875128329     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.22708     Document Type: Article

References (73)

1. Renoux AJ, Todd PK. Neurodegeneration the RNA way. Prog Neurobiol 2012; 97:173-89; PMID:22079416; http://dx.doi.org/10.1016/j.pneurobio.2011.10.006.
2. Ranum L P, Cooper TA. RNA-mediated neuromuscu-lar disorders. Annu Rev Neurosci 2006; 29:259-77; PMID:16776586; http://dx.doi.org/10.1146/annurev. neuro.29.051605.113014.
3. Davis BM, McCurrach ME, Taneja KL, Singer RH, Housman DE. Expansion of a CUG trinucleotide repeat in the 3' untranslated region of myotonic dystrophy protein kinase transcripts results in nuclear retention of transcripts. Proc Natl Acad Sci USA 1997; 94:7388-93; PMID:9207101; http://dx.doi. org/10.1073/pnas.94.14.7388.
4. Tassone F, Hagerman RJ, Garcia-Arocena D, Khandjian EW, Greco CM, Hagerman PJ. Intranuclear inclusions in neural cells with premutation alleles in fragile X associated tremor/ataxia syndrome. J Med Genet 2004; 41:e43; PMID:15060119; http://dx.doi.org/10.1136/jmg.2003.012518.
5. Chen IC, Lin HY, Lee GC, Kao SH, Chen CM, Wu YR, et al. Spinocerebellar ataxia type 8 larger triplet expansion alters histone modification and induces RNA foci. BMC Mol Biol 2009; 10:9; PMID:19203395; http://dx.doi.org/10.1186/ 1471-2199-10-9.
6. Dahm R, Macchi P. Human pathologies associated with defective RNA transport and localization in the nervous system. Biol Cell 2007; 99:649-61; PMID:17939777; http://dx.doi.org/10.1042/BC20070045. (Pubitemid 350120984)
7. Doi H, Mitsui K, Kurosawa M, Machida Y, Kuroiwa Y, Nukina N. Identification of ubiquitin-interacting proteins in purified polyglutamine aggregates. FEBS Lett 2004; 571:171-6; PMID:15280037; http://dx.doi. org/10.1016/j.febslet.2004.06.077. (Pubitemid 38992943)
8. Doi H, Koyano S, Suzuki Y, Nukina N, Kuroiwa Y. The RNA-binding protein FUS/TLS is a common aggregate-interacting protein in polyglutamine diseases. Neurosci Res 2010; 66:131-3; PMID:19833157; http://dx.doi.org/10.1016/j.neures. 2009.10.004.
9. Schwab C, Arai T, Hasegawa M, Yu S, McGeer PL. Colocalization of transactivation-responsive DNA-binding protein 43 and huntingtin in inclusions of Huntington disease. J Neuropathol Exp Neurol 2008; 67:1159-65; PMID:19018245; http://dx.doi. org/10.1097/NEN.0b013e31818e8951.
10. Nakashima-Yasuda H, Uryu K, Robinson J, Xie SX, Hurtig H, Duda JE, et al. Co-morbidity of TDP-43 proteinopathy in Lewy body related diseases. Acta Neuropathol 2007; 114:221-9; PMID:17653732; http://dx.doi.org/10.1007/s00401- 007-0261-2. (Pubitemid 47226148)
11. Amador-Ortiz C, Lin WL, Ahmed Z, Personett D, Davies P, Duara R, et al. TDP-43 immunoreactivity in hippocampal sclerosis and Alzheimer's disease. Ann Neurol 2007; 61:435-45; PMID:17469117; http://dx.doi.org/10.1002/ana.21154. (Pubitemid 46878771)
12. Higashi S, Iseki E, Yamamoto R, Minegishi M, Hino H, Fujisawa K, et al. Concurrence of TDP-43, tau and alpha-synuclein pathology in brains of Alzheimer's disease and dementia with Lewy bodies. Brain Res 2007; 1184:284-94; PMID:17963732; http://dx.doi. org/10.1016/j.brainres.2007.09.048. (Pubitemid 350160566)
13. Lin WL, Dickson DW. Ultrastructural localization of TDP-43 in filamentous neuronal inclusions in various neurodegenerative diseases. Acta Neuropathol 2008; 116:205-13; PMID:18607609; http://dx.doi. org/10.1007/s00401-008-0408-9.
14. Neumann M, Sampathu DM, Kwong LK, Truax AC, Micsenyi MC, Chou T T, et al. Ubiquitinated TDP-43 in frontotemporal lobar degeneration and amyotrophic lateral sclerosis. Science 2006; 314:130-3; PMID:17023659; http://dx.doi.org/10. 1126/sci-ence.1134108. (Pubitemid 44547757)
15. Belzil VV, Valdmanis PN, Dion PA, Daoud H, Kabashi E, Noreau A, et al.; S2D team. Mutations in FUS cause FALS and SALS in French and French Canadian populations. Neurology 2009; 73:1176-9; PMID:19741216; http://dx.doi.org/10. 1212/WNL.0b013e3181bbfeef.
16. Corrado L, Del Bo R, Castellotti B, Ratti A, Cereda C, Penco S, et al. Mutations of FUS gene in sporadic amy-otrophic lateral sclerosis. J Med Genet 2010; 47:190-4; PMID:19861302; http://dx.doi.org/10.1136/jmg.2009.071027.
17. Kwiatkowski TJ Jr., Bosco DA, Leclerc AL, Tamrazian E, Vanderburg CR, Russ C, et al. Mutations in the FUS/TLS gene on chromosome 16 cause familial amyotrophic lateral sclerosis. Science 2009; 323:1205-8; PMID:19251627; http://dx.doi.org/10.1126/sci-ence.1166066.
18. Vance C, Rogelj B, Hortobágyi T, De Vos KJ, Nishimura AL, Sreedharan J, et al. Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009; 323:1208-11; PMID:19251628; http://dx.doi.org/10.1126/sci-ence.1165942.
19. Gal J, Zhang J, Kwinter DM, Zhai J, Jia H, Jia J, et al. Nuclear localization sequence of FUS and induction of stress granules by ALS mutants. Neurobiol Aging 2011; 32:2323, e27-40; PMID:20674093; http://dx.doi.org/10.1016/ j.neurobiolaging.2010.06.010.
20. Bosco DA, Lemay N, Ko HK, Zhou H, Burke C, Kwiatkowski TJ Jr., et al. Mutant FUS proteins that cause amyotrophic lateral sclerosis incorporate into stress granules. Hum Mol Genet 2010; 19:4160-75; PMID:20699327; http://dx.doi.org/10.1093/hmg/ddq335.
21. Moisse K, Volkening K, Leystra-Lantz C, Welch I, Hill T, Strong MJ. Divergent patterns of cytosolic TDP-43 and neuronal progranulin expression following axotomy: implications for TDP-43 in the physiological response to neuronal injury. Brain Res 2009; 1249:202-11; PMID:19046946; http://dx.doi.org/10.1016/j. brainres.2008.10.021.
22. Liu-Yesucevitz L, Bilgutay A, Zhang YJ, Vanderweyde T, Citro A, Mehta T, et al. Tar DNA binding pro-tein-43 (TDP-43) associates with stress granules: analysis of cultured cells and pathological brain tissue. PLoS One 2010; 5:e13250; PMID:20948999; http://dx.doi. org/10.1371/journal.pone.0013250.
23. Nonhoff U, Ralser M, Welzel F, Piccini I, Balzereit D, Yaspo ML, et al. Ataxin-2 interacts with the DEAD/H-box RNA helicase DDX6 and interferes with P-bodies and stress granules. Mol Biol Cell 2007; 18:1385-96; PMID:17392519; http://dx.doi.org/10.1091/mbc. E06-12-1120. (Pubitemid 46626633)
24. Savas JN, Makusky A, Ottosen S, Baillat D, Then F, Krainc D, et al. Huntington's disease protein contributes to RNA-mediated gene silencing through association with Argonaute and P bodies. Proc Natl Acad Sci USA 2008; 105:10820-5; PMID:18669659; http://dx.doi.org/10.1073/pnas.0800658105.
25. Sheth U, Parker R. Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 2003; 300:805-8; PMID:12730603; http://dx.doi. org/10.1126/science.1082320. (Pubitemid 36532117)
26. Cougot N, Babajko S, Séraphin B. Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 2004; 165:31-40; PMID:15067023; http://dx.doi. org/10.1083/jcb.200309008. (Pubitemid 38649174)
27. Eulalio A, Behm-Ansmant I, Izaurralde E. P bodies: at the crossroads of post-transcriptional pathways. Nat Rev Mol Cell Biol 2007; 8:9-22; PMID:17183357; http://dx.doi.org/10.1038/nrm2080. (Pubitemid 46012011)
28. Teixeira D, Sheth U, Valencia-Sanchez MA, Brengues M, Parker R. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 2005; 11:371-82; PMID:15703442; http://dx.doi. org/10.1261/rna.7258505. (Pubitemid 40397171)
29. Zeitelhofer M, Karra D, Macchi P, Tolino M, Thomas S, Schwarz M, et al. Dynamic interaction between P-bodies and transport ribonucleoprotein particles in dendrites of mature hippocampal neurons. J Neurosci 2008; 28:7555-62; PMID:18650333; http://dx.doi. org/10.1523/JNEUROSCI.0104-08.2008.
30. Ganesh S, Puri R, Singh S, Mittal S, Dubey D. Recent advances in the molecular basis of Lafora's progressive myoclonus epilepsy. J Hum Genet 2006; 51:1-8; PMID:16311711; http://dx.doi.org/10.1007/s10038-005-0321-1. (Pubitemid 43162244)
31. Singh S, Ganesh S. Lafora progressive myoclonus epilepsy: a meta-analysis of reported mutations in the first decade following the discovery of the EPM2A and NHLRC1 genes. Hum Mutat 2009; 30:715-23; PMID:19267391; http://dx.doi.org/ 10.1002/humu.20954.
32. Ramachandran N, Girard JM, Turnbull J, Minassian BA. The autosomal recessively inherited progressive myoclonus epilepsies and their genes. Epilepsia 2009; 50(Suppl 5):29-36; PMID:19469843; http://dx.doi. org/10.1111/j.1528-1167.2009.02117.x.
33. Fernández-Sánchez ME, Criado-García O, Heath KE, García-Fojeda B, Medraño-Fernández I, Gomez-Garre P, et al. Laforin, the dual-phosphatase responsible for Lafora disease, interacts with R5 (PTG), a regulatory subunit of protein phosphatase-1 that enhances glyco-gen accumulation. Hum Mol Genet 2003; 12:3161-71; PMID:14532330; http://dx.doi.org/10.1093/hmg/ddg340. (Pubitemid 37508887)
34. Vilchez D, Ros S, Cifuentes D, Pujadas L, Vallès J, García-Fojeda B, et al. Mechanism suppressing glyco-gen synthesis in neurons and its demise in progressive myoclonus epilepsy. Nat Neurosci 2007; 10:1407-13; PMID:17952067; http://dx.doi.org/10.1038/nn1998. (Pubitemid 350014686)
35. Vernia S, Solaz-Fuster MC, Gimeno-Alcañiz JV, Rubio T, García-Haro L, Foretz M, et al. AMP-activated protein kinase phosphorylates R5/PTG, the glycogen targeting subunit of the R5/PTG-protein phosphatase 1 holoenzyme, and accelerates its down-regulation by the laforin-malin complex. J Biol Chem 2009; 284:8247-55; PMID:19171932; http://dx.doi.org/10.1074/jbc. M808492200.
36. Worby CA, Gentry MS, Dixon JE. Malin decreases glycogen accumulation by promoting the degradation of protein targeting to glycogen (PTG). J Biol Chem 2008; 283:4069-76; PMID:18070875; http://dx.doi. org/10.1074/jbc.M708712200.
37. Solaz-Fuster MC, Gimeno-Alcañiz J V, Ros S, Fernandez-Sanchez ME, Garcia-Fojeda B, Criado Garcia O, et al. Regulation of glycogen synthesis by the laforin-malin complex is modulated by the AMP-activated protein kinase pathway. Hum Mol Genet 2008; 17:667-78; PMID:18029386; http://dx.doi. org/10.1093/hmg/ddm339. (Pubitemid 351292256)
38. Sengupta S, Badhwar I, Upadhyay M, Singh S, Ganesh S. Malin and laforin are essential components of a protein complex that protects cells from thermal stress. J Cell Sci 2011; 124:2277-86; PMID:21652633; http://dx.doi.org/10.1242/ jcs.082800.
39. Vernia S, Rubio T, Heredia M, Rodríguez de Córdoba S, Sanz P. Increased endoplasmic reticulum stress and decreased proteasomal function in lafora disease models lacking the phosphatase laforin. PLoS One 2009; 4:e5907; PMID:19529779; http://dx.doi. org/10.1371/journal.pone.0005907.
40. Garyali P, Siwach P, Singh PK, Puri R, Mittal S, Sengupta S, et al. The malin-laforin complex suppresses the cellular toxicity of misfolded proteins by promoting their degradation through the ubiquitin-proteasome system. Hum Mol Genet 2009; 18:688-700; PMID:19036738; http://dx.doi.org/10.1093/hmg/ddn398.
41. Mittal S, Dubey D, Yamakawa K, Ganesh S. Lafora disease proteins malin and laforin are recruited to aggresomes in response to proteasomal impairment. Hum Mol Genet 2007; 16:753-62; PMID:17337485; http://dx.doi.org/10.1093/hmg/ ddm006. (Pubitemid 47061622)
42. Ganesh S, Agarwala KL, Ueda K, Akagi T, Shoda K, Usui T, et al. Laforin, defective in the progressive myoclonus epilepsy of Lafora type, is a dual-specificity phosphatase associated with polyribosomes. Hum Mol Genet 2000; 9:2251-61; PMID:11001928; http://dx.doi.org/10.1093/oxfordjournals.hmg.a018916.
43. Minassian BA, Andrade DM, Ianzano L, Young EJ, Chan E, Ackerley CA, et al. Laforin is a cell membrane and endoplasmic reticulum-associated protein tyrosine phosphatase. Ann Neurol 2001; 49:271-5; PMID:11220751; http://dx.doi.org/10.1002/1531-8249(20010201)49:23.0.CO;2-D. (Pubitemid 32158008)
44. Singh PK, Singh S, Ganesh S. The laforin-malin complex negatively regulates glycogen synthesis by modulating cellular glucose uptake via glucose transporters. Mol Cell Biol 2012; 32:652-63; PMID:22124153; http://dx.doi.org/ 10.1128/MCB.06353-11.
45. Eulalio A, Behm-Ansmant I, Schweizer D, Izaurralde E. P-body formation is a consequence, not the cause, of RNA-mediated gene silencing. Mol Cell Biol 2007; 27:3970-81; PMID:17403906; http://dx.doi. org/10.1128/MCB.00128-07. (Pubitemid 47010995)
46. Blumenthal J, Ginzburg I. Zinc as a translation regulator in neurons: implications for P-body aggregation. J Cell Sci 2008; 121:3253-60; PMID:18799791; http://dx.doi.org/10.1242/jcs.033266.
47. rd, Parker R, Hannon GJ. A role for the P-body component GW182 in microRNA function. Nat Cell Biol 2005; 7:1261-6; PMID:16284623; http://dx.doi.org/10.1038/ncb1333.
48. Eystathioy T, Jakymiw A, Chan EK, Séraphin B, Cougot N, Fritzler MJ. The GW182 protein colo-calizes with mRNA degradation associated proteins hDcp1 and hLSm4 in cytoplasmic GW bodies. RNA 2003; 9:1171-3; PMID:13130130; http://dx.doi. org/10.1261/rna.5810203. (Pubitemid 37151671)
49. Coller J, Parker R. Eukaryotic mRNA decap-ping. Annu Rev Biochem 2004; 73:861-90; PMID:15189161; http://dx.doi.org/10.1146/annurev. biochem.73.011303.074032.
50. Franks TM, Lykke-Andersen J. The control of mRNA decapping and P-body formation. Mol Cell 2008; 32:605-15; PMID:19061636; http://dx.doi. org/10.1016/j.molcel.2008.11.001.
51. Lykke-Andersen J. Identification of a human decap-ping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 2002; 22:8114-21; PMID:12417715; http://dx.doi.org/10.1128/MCB.22.23.8114-8121.2002. (Pubitemid 35304045)
52. Turnbull J, Wang P, Girard JM, Ruggieri A, Wang TJ, Draginov AG, et al. Glycogen hyperphosphoryla-tion underlies lafora body formation. Ann Neurol 2010; 68:925-33; PMID:21077101; http://dx.doi. org/10.1002/ana.22156.
53. Rehwinkel J, Behm-Ansmant I, Gatfield D, Izaurralde E. A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 2005; 11:1640-7; PMID:16177138; http://dx.doi.org/10.1261/rna.2191905. (Pubitemid 41505538)
54. Fierro-Monti I, Mathews MB. Proteins binding to duplexed RNA: one motif, multiple functions. Trends Biochem Sci 2000; 25:241-6; PMID:10782096; http://dx.doi.org/10.1016/S0968-0004(00)01580-2. (Pubitemid 30236222)
55. Bernstein E, Caudy AA, Hammond SM, Hannon GJ. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001; 409:363-6; PMID:11201747; http://dx.doi. org/10.1038/35053110. (Pubitemid 32151243)
56. Tokumaru S, Suzuki M, Yamada H, Nagino M, Takahashi T. let-7 regulates Dicer expression and constitutes a negative feedback loop. Carcinogenesis 2008; 29:2073-7; PMID:18700235; http://dx.doi. org/10.1093/carcin/bgn187.
57. Forman JJ, Legesse-Miller A, Coller HA. A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc Natl Acad Sci USA 2008; 105:14879-84; PMID:18812516; http://dx.doi.org/10.1073/pnas.0803230105.
58. Liu J, Valencia-Sanchez MA, Hannon GJ, Parker R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat Cell Biol 2005; 7:719-23; PMID:15937477; http://dx.doi.org/10.1038/ncb1274. (Pubitemid 40975754)
59. Behm-Ansmant I, Rehwinkel J, Doerks T, Stark A, Bork P, Izaurralde E. mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 2006; 20:1885-98; PMID:16815998; http://dx.doi. org/10.1101/gad.1424106. (Pubitemid 44079326)
60. Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J, Fritzler MJ, et al. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J Cell Biol 2005; 169:871-84; PMID:15967811; http://dx.doi.org/10.1083/jcb.200502088. (Pubitemid 41002864)
61. Kedersha N, Anderson P. Mammalian stress granules and processing bodies. Methods Enzymol 2007; 431:61-81; PMID:17923231; http://dx.doi. org/10.1016/S0076-6879(07)31005-7.
62. Franks TM, Lykke-Andersen J. The control of mRNA decapping and P-body formation. Mol Cell 2008; 32:605-15; PMID:19061636; http://dx.doi. org/10.1016/j.molcel.2008.11.001.
63. Zeng Y, Sankala H, Zhang X, Graves PR. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem J 2008; 413:429-36; PMID:18476811; http://dx.doi. org/10.1042/BJ20080599.
64. Rzeczkowski K, Beuerlein K, Müller H, Dittrich-Breiholz O, Schneider H, Kettner-Buhrow D, et al. c-Jun N-terminal kinase phosphorylates DCP1a to control formation of P bodies. J Cell Biol 2011; 194:581-96; PMID:21859862; http://dx.doi. org/10.1083/jcb.201006089.
65. Rybak A, Fuchs H, Hadian K, Smirnova L, Wulczyn EA, Michel G, et al. The let-7 target gene mouse lin-41 is a stem cell specific E3 ubiquitin ligase for the miRNA pathway protein Ago2. Nat Cell Biol 2009; 11:1411-20; PMID:19898466; http://dx.doi.org/10.1038/ncb1987.
66. Romá-Mateo C, Moreno D, Vernia S, Rubio T, Bridges TM, Gentry MS, et al. Lafora disease E3-ubiquitin ligase malin is related to TRIM32 at both the phylogenetic and functional level. BMC Evol Biol 2011; 11:225; PMID:21798009; http://dx.doi. org/10.1186/1471-2148-11-225.
67. Schwamborn JC, Berezikov E, Knoblich JA. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 2009; 136:913-25; PMID:19269368; http://dx.doi.org/10.1016/j.cell.2008.12.024.
68. Schaefer A, O'Carroll D, Tan CL, Hillman D, Sugimori M, Llinas R, et al. Cerebellar neurodegen-eration in the absence of microRNAs. J Exp Med 2007; 204:1553-8; PMID:17606634; http://dx.doi. org/10.1084/jem.20070823.
69. Hébert SS, Papadopoulou AS, Smith P, Galas MC, Planel E, Silahtaroglu AN, et al. Genetic ablation of Dicer in adult forebrain neurons results in abnormal tau hyperphosphorylation and neurodegeneration. Hum Mol Genet 2010; 19:3959-69; PMID:20660113; http://dx.doi.org/10.1093/hmg/ddq311.
70. Tao J, Wu H, Lin Q, Wei W, Lu XH, Cantle J P, et al. Deletion of astroglial Dicer causes non-cell-autonomous neuronal dysfunction and degeneration. J Neurosci 2011; 31:8306-19; PMID:21632951; http://dx.doi.org/10. 1523/JNEUROSCI.0567-11.2011.
71. Cuellar TL, Davis TH, Nelson PT, Loeb GB, Harfe BD, Ullian E, et al. Dicer loss in striatal neurons produces behavioral and neuroanatomical phenotypes in the absence of neurodegeneration. Proc Natl Acad Sci USA 2008; 105:5614-9; PMID:18385371; http://dx.doi.org/10.1073/pnas.0801689105. (Pubitemid 351753911)
72. Puri R, Suzuki T, Yamakawa K, Ganesh S. Hyperphosphorylation and aggregation of Tau in lafo-rin-deficient mice, an animal model for Lafora disease. J Biol Chem 2009; 284:22657-63; PMID:19542233; http://dx.doi.org/10. 1074/jbc.M109.009688.
73. Cougot N, Bhattacharyya SN, Tapia-Arancibia L, Bordonné R, Filipowicz W, Bertrand E, et al. Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation. J Neurosci 2008; 28:13793-804; PMID:19091970; http://dx.doi. org/10.1523/ JNEUROSCI.4155-08.2008.