Phosphorylation of Ago2 and subsequent inactivation of let-7a RNP-specific microRNAs control differentiation of mammalian sympathetic neurons

Molecular and Cellular Biology

Volumn 36, Issue 8, 2016, Pages 1260-1271

  Patranabis, Somi ^a   Bhattacharyya, Suvendra Nath ^a  

^a INDIAN INSTITUTE OF CHEMICAL BIOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ARGONAUTE 2 PROTEIN; LET 7A PROTEIN; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN AND STRESS ACTIVATED PROTEIN KINASE 1; RIBONUCLEOPROTEIN; UNCLASSIFIED DRUG; AGO2 PROTEIN, RAT; ARGONAUTE PROTEIN; KRAS PROTEIN, RAT; MIRNLET7 MICRORNA, RAT; PROTEIN P21;

ANIMAL CELL; ARTICLE; BASE PAIRING; CONTROLLED STUDY; DISSOCIATION; GENE EXPRESSION REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; MAMMAL CELL; NERVE CELL DIFFERENTIATION; NEWBORN; NONHUMAN; ONCOGENE K RAS; PC12 CELL LINE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SYMPATHETIC NERVE CELL; TRANSCRIPTION REGULATION; UPREGULATION; ANIMAL; CELL CULTURE; CELL LINE; CYTOLOGY; GENETICS; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; ARGONAUTE PROTEINS; CELL LINE; CELLS, CULTURED; MAP KINASE SIGNALING SYSTEM; MICRORNAS; NEUROGENESIS; NEURONS; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS P21(RAS); RATS; RATS, SPRAGUE-DAWLEY; UP-REGULATION;

EID: 84963805295     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00054-16     Document Type: Article

References (42)

1. Vaudry D, Stork PJ, Lazarovici P, Eiden LE. 2002. Signaling pathways for PC12 cell differentiation: making the right connections. Science 296:1648-1649. http://dx.doi.org/10.1126/science.1071552.
2. Greene LA, Tischler AS. 1976. Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci U S A 73:2424-2428. http://dx.doi.org/10.1073/pnas.73.7.2424.
3. Dichter MA, Tischler AS, Greene LA. 1977. Nerve growth factor-induced increase in electrical excitability and acetylcholine sensitivity of a rat pheochromocytoma cell line. Nature 268:501-504. http://dx.doi.org/10.1038/268501a0.
4. Jeon CY, Jin JK, Koh YH, Chun W, Choi IG, Kown HJ, Kim YS, Park JB. 2010. Neurites from PC12 cells are connected to each other by synapse-like structures. Synapse 64:765-772. http://dx.doi.org/10.1002/syn.20789.
5. D'Arcangelo G, Halegoua S. 1993. A branched signaling pathway for nerve growth factor is revealed by Src-, Ras-, and Raf-mediated gene inductions. Mol Cell Biol 13:3146-3155. http://dx.doi.org/10.1128/MCB.13.6.3146.
6. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W. 2006. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125:1111-1124. http://dx.doi.org/10.1016/j.cell.2006.04.031.
7. Jakymiw A, Lian S, Eystathioy T, Li S, Satoh M, Hamel JC, Fritzler MJ, Chan EK. 2005. Disruption of GW bodies impairs mammalian RNA interference. Nat Cell Biol 7:1267-1274. http://dx.doi.org/10.1038/ncb1334.
8. Pillai RS, Bhattacharyya SN, Artus CG, Zoller T, Cougot N, Basyuk E, Bertrand E, Filipowicz W. 2005. Inhibition of translational initiation by let-7 microRNA in human cells. Science 309:1573-1576. http://dx.doi.org/10.1126/science.1115079.
9. Vreugdenhil E, Berezikov E. 2010. Fine-tuning the brain: microRNAs. Front Neuroendocrinol 31:128-133. http://dx.doi.org/10.1016/j.yfrne.2009.08.001.
10. Miska EA, Alvarez-Saavedra E, Townsend M, Yoshii A, Sestan N, Rakic P, Constantine-Paton M, Horvitz HR. 2004. Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol 5:R68. http://dx.doi.org/10.1186/gb-2004-5-9-r68.
11. Krichevsky AM, Sonntag KC, Isacson O, Kosik KS. 2006. Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24:857-864. http://dx.doi.org/10.1634/stemcells.2005-0441.
12. Rajasethupathy P, Fiumara F, Sheridan R, Betel D, Puthanveettil SV, Russo JJ, Sander C, Tuschl T, Kandel E. 2009. Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63:803-817. http://dx.doi.org/10.1016/j.neuron.2009.05.029.
13. Yu JY, Chung KH, Deo M, Thompson RC, Turner DL. 2008. MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp Cell Res 314:2618-2633. http://dx.doi.org/10.1016/j.yexcr.2008.06.002.
14. Edbauer D, Neilson JR, Foster KA, Wang CF, Seeburg DP, Batterton MN, Tada T, Dolan BM, Sharp PA, Sheng M. 2010. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65:373-384. http://dx.doi.org/10.1016/j.neuron.2010.01.005.
15. Magill ST, Cambronne XA, Luikart BW, Lioy DT, Leighton BH, Westbrook GL, Mandel G, Goodman RH. 2010. microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc Natl Acad Sci U S A 107:20382-20387. http://dx.doi.org/10.1073/pnas.1015691107.
16. Bruno IG, Karam R, Huang L, Bhardwaj A, Lou CH, Shum EY, Song HW, Corbett MA, Gifford WD, Gecz J, Pfaff SL, Wilkinson MF. 2011. Identification of a microRNA that activates gene expression by repressing nonsense-mediated RNA decay. Mol Cell 42:500-510. http://dx.doi.org/10.1016/j.molcel.2011.04.018.
17. Friedman RC, Farh KK, Burge CB, Bartel DP. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92-105. http://dx.doi.org/10.1101/gr.082701.108.
18. Qi HH, Ongusaha PP, Myllyharju J, Cheng D, Pakkanen O, Shi Y, Lee SW, Peng J, Shi Y. 2008. Prolyl 4-hydroxylation regulates Argonaute 2 stability. Nature 455:421-424. http://dx.doi.org/10.1038/nature07186.
19. Kirino Y, Kim N, de Planell-Saguer M, Khandros E, Chiorean S, Klein PS, Rigoutsos I, Jongens TA, Mourelatos Z. 2009. Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat Cell Biol 11:652-658. http://dx.doi.org/10.1038/ncb1872.
20. Horman SR, Janas MM, Litterst C, Wang B, MacRae IJ, Sever MJ, Morrissey DV, Graves P, Luo B, Umesalma S, Qi HH, Miraglia LJ, Novina CD, Orth AP. 2013. Akt-mediated phosphorylation of Argonaute 2 downregulates cleavage and upregulates translational repression of microRNA targets. Mol Cell 50:356-367. http://dx.doi.org/10.1016/j.molcel.2013.03.015.
21. Rudel S, Wang Y, Lenobel R, Korner R, Hsiao HH, Urlaub H, Patel D, Meister G. 2011. Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic Acids Res 39:2330-2343. http://dx.doi.org/10.1093/nar/gkq1032.
22. Shen J, Xia W, Khotskaya YB, Huo L, Nakanishi K, Lim SO, Du Y, Wang Y, Chang WC, Chen CH, Hsu JL, Wu Y, Lam YC, James BP, Liu X, Liu CG, Patel DJ, Hung MC. 2013. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 497:383-387. http://dx.doi.org/10.1038/nature12080.
23. Zeng Y, Sankala H, Zhang X, Graves PR. 2008. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem J 413:429-436. http://dx.doi.org/10.1042/BJ20080599.
24. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM, Song JJ, Hammond SM, Joshua-Tor L, Hannon GJ. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437-1441. http://dx.doi.org/10.1126/science.1102513.
25. Lopez-Orozco J, Pare JM, Holme AL, Chaulk SG, Fahlman RP, Hobman TC. 2015. Functional analyses of phosphorylation events in human Argonaute 2. RNA 21:2030-2038. http://dx.doi.org/10.1261/rna.053207.115.
26. Mazumder A, Bose M, Chakraborty A, Chakrabarti S, Bhattacharyya SN. 2013. A transient reversal of miRNA-mediated repression controls macrophage activation. EMBO Rep 14:1008-1016. http://dx.doi.org/10.1038/embor.2013.149.
27. Barancik M, Bohacova V, Kvackajova J, Hudecova S, Krizanova O, Breier A. 2001. SB203580, a specific inhibitor of p38-MAPK pathway, is a new reversal agent of P-glycoprotein-mediated multidrug resistance. Eur J Pharm Sci 14:29-36. http://dx.doi.org/10.1016/S0928-0987(01)00139-7.
28. Zareen N, Greene LA. 2009. Protocol for culturing sympathetic neurons from rat superior cervical ganglia (SCG). J Vis Exp 2009:988. http://dx.doi.org/10.3791/988.
29. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, Slack FJ. 2005. RAS is regulated by the let-7 microRNA family. Cell 120:635-647. http://dx.doi.org/10.1016/j.cell.2005.01.014.
30. Xing J, Kornhauser JM, Xia Z, Thiele EA, Greenberg ME. 1998. Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol Cell Biol 18:1946-1955. http://dx.doi.org/10.1128/MCB.18.4.1946.
31. Morooka T, Nishida E. 1998. Requirement of p38 mitogen-activated protein kinase for neuronal differentiation in PC12 cells. J Biol Chem 273:24285-24288. http://dx.doi.org/10.1074/jbc.273.38.24285.
32. Zheng WH, Quirion R. 2006. Insulin-like growth factor-1 (IGF-1) induces the activation/phosphorylation of Akt kinase and cAMP response element-binding protein (CREB) by activating different signaling pathways in PC12 cells. BMC Neurosci 7:51. http://dx.doi.org/10.1186/1471-2202-7-51.
33. Bussing I, Slack FJ, Grosshans H. 2008. let-7 microRNAs in development, stem cells and cancer. Trends Mol Med 14:400-409. http://dx.doi.org/10.1016/j.molmed.2008.07.001.
34. Reinhart BJ, Slack FJ, Basson M, Pasquinelli AE, Bettinger JC, Rougvie AE, Horvitz HR, Ruvkun G. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901-906. http://dx.doi.org/10.1038/35002607.
35. Krol J, Busskamp V, Markiewicz I, Stadler MB, Ribi S, Richter J, Duebel J, Bicker S, Fehling HJ, Schubeler D, Oertner TG, Schratt G, Bibel M, Roska B, Filipowicz W. 2010. Characterizing light-regulated retinal microRNAs reveals rapid turnover as a common property of neuronal microRNAs. Cell 141:618-631. http://dx.doi.org/10.1016/j.cell.2010.03.039.
36. Xue Y, Ouyang K, Huang J, Zhou Y, Ouyang H, Li H, Wang G, Wu Q, Wei C, Bi Y, Jiang L, Cai Z, Sun H, Zhang K, Zhang Y, Chen J, Fu XD. 2013. Direct conversion of fibroblasts to neurons by reprogramming PTBregulated microRNA circuits. Cell 152:82-96. http://dx.doi.org/10.1016/j.cell.2012.11.045.
37. Peng Y, Laser J, Shi G, Mittal K, Melamed J, Lee P, Wei JJ. 2008. Antiproliferative effects by let-7 repression of high-mobility group A2 in uterine leiomyoma. Mol Cancer Res 6:663-673. http://dx.doi.org/10.1158/1541-7786.MCR-07-0370.
38. Rybak A, Fuchs H, Smirnova L, Brandt C, Pohl EE, Nitsch R, Wulczyn FG. 2008. A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat Cell Biol 10:987-993. http://dx.doi.org/10.1038/ncb1759.
39. Schwamborn JC, Berezikov E, Knoblich JA. 2009. The TRIM-NHL protein TRIM32 activates microRNAs and prevents self-renewal in mouse neural progenitors. Cell 136:913-925. http://dx.doi.org/10.1016/j.cell.2008.12.024.
40. Nicklas S, Okawa S, Hillje AL, Gonzalez-Cano L, Del Sol A, Schwamborn JC. 2015. The RNA helicase DDX6 regulates cell-fate specification in neural stem cells via miRNAs. Nucleic Acids Res 43:2638-2654. http://dx.doi.org/10.1093/nar/gkv138.
41. Li S, Wang X, Gu Y, Chen C, Wang Y, Liu J, Hu W, Yu B, Ding F, Liu Y, Gu X. 2015. Let-7 microRNAs regenerate peripheral nerve regeneration by targeting nerve growth factor. Mol Ther 23:423-433. http://dx.doi.org/10.1038/mt.2014.220.
42. Huang YW, Ruiz CR, Eyler EC, Lin K, Meffert MK. 2012. Dual regulation of miRNA biogenesis generates target specificity in neurotrophin-induced protein synthesis. Cell 148:933-946. http://dx.doi.org/10.1016/j.cell.2012.01.036.