Phosphorylation acts positively and negatively to regulate MRTF-A subcellular localisation and activity

eLife

Volumn 5, Issue JUN2016, 2016, Pages

  Panayiotou, Richard ^a   Miralles, Francesc ^a,b   Pawlowski, Rafal ^a,c   Diring, Jessica ^a   Flynn, Helen R ^a   Skehel, Mark ^a,d   Treisman, Richard ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^c inVentiv Health ^*  (Switzerland)

^d MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; F ACTIN; G ACTIN; LATRUNCULIN B; MITOGEN ACTIVATED PROTEIN KINASE 1; MYOCARDIN RELATED TRANSCRIPTION FACTOR A; MYOSIN LIGHT CHAIN 2; PHALLOIDIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ACTIN; MKL1 PROTEIN, MOUSE; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSACTIVATOR PROTEIN;

3T3 CELL LINE; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE MUTATION; GENETIC TRANSFECTION; HUMAN; IMMUNOFLUORESCENCE TEST; LUCIFERASE ASSAY; MASS SPECTROMETRY; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; PROTEIN SYNTHESIS REGULATION; REAL TIME POLYMERASE CHAIN REACTION; TRANSCRIPTION INITIATION; ANIMAL; CELL LINE; GENETIC TRANSCRIPTION; METABOLISM; MOUSE; PHOSPHORYLATION; PROTEIN PROCESSING;

ACTINS; ANIMALS; CELL LINE; MICE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RHO GTP-BINDING PROTEINS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 84982730582     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.15460     Document Type: Article

References (47)

1. Aoki K, Kumagai Y, Sakurai A, Komatsu N, Fujita Y, Shionyu C, Matsuda M. 2013. Stochastic ERK activation induced by noise and cell-to-cell propagation regulates cell density-dependent proliferation. Molecular Cell 52: 529-540. doi: 10.1016/j.molcel.2013.09.015
2. Arsenian S, Weinhold B, Oelgeschläger M, Rüther U, Nordheim A. 1998. Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO Journal 17: 6289-6299. doi: 10.1093/emboj/17.21.6289
3. Baarlink C, Wang H, Grosse R. 2013. Nuclear actin network assembly by formins regulates the SRF coactivator MAL. Science 340: 864-867. doi: 10.1126/science.1235038
4. Badorff C, Seeger FH, Zeiher AM, Dimmeler S. 2005. Glycogen synthase kinase 3beta inhibits myocardin-dependent transcription and hypertrophy induction through site-specific phosphorylation. Circulation Research 97: 645-654. doi: 10.1161/01.RES.0000184684.88750.FE
5. Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P. 2007. The selectivity of protein kinase inhibitors: a further update. Biochemical Journal 408: 297-315. doi: 10.1042/BJ20070797
6. Charbonney E, Speight P, Masszi A, Nakano H, Kapus A. 2011. b-catenin and Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblast transition. Molecular Biology of the Cell 22: 4472-4485. doi: 10.1091/mbc.E11-04-0335
7. Copeland JW, Treisman R. 2002. The diaphanous-related formin mDia1 controls serum response factor activity through its effects on actin polymerization. Molecular Biology of the Cell 13: 4088-4099. doi: 10.1091/mbc.02-06-0092
8. Cox J, Mann M. 2008. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nature Biotechnology 26: 1367-1372. doi: 10.1038/nbt.1511
9. Esnault C, Stewart A, Gualdrini F, East P, Horswell S, Matthews N, Treisman R. 2014. Rho-actin signaling to the MRTF coactivators dominates the immediate transcriptional response to serum in fibroblasts. Genes & Development 28: 943-958. doi: 10.1101/gad.239327.114
10. Fu SC, Huang HC, Horton P, Juan HF. 2013. ValidNESs: a database of validated leucine-rich nuclear export signals. Nucleic Acids Research 41: D338-343. doi: 10.1093/nar/gks936
11. Gineitis D, Treisman R. 2001. Differential usage of signal transduction pathways defines two types of serum response factor target gene. Journal of Biological Chemistry 276: 24531-24539. doi: 10.1074/jbc.M102678200
12. Gnad F, Gunawardena J, Mann M. 2011. PHOSIDA 2011: the posttranslational modification database. Nucleic Acids Research 39: D253-260. doi: 10.1093/nar/gkq1159
13. Gnad F, Ren S, Cox J, Olsen JV, Macek B, Oroshi M, Mann M. 2007. PHOSIDA (phosphorylation site database): management, structural and evolutionary investigation, and prediction of phosphosites. Genome Biology 8: R250. doi: 10.1186/gb-2007-8-11-r250
14. Griner EM, Kazanietz MG. 2007. Protein kinase C and other diacylglycerol effectors in cancer. Nature Reviews Cancer 7: 281-294. doi: 10.1038/nrc2110
15. Guettler S, Vartiainen MK, Miralles F, Larijani B, Treisman R. 2008. RPEL motifs link the serum response factor cofactor MAL but not myocardin to Rho signaling via actin binding. Molecular and Cellular Biology 28: 732-742. doi: 10.1128/MCB.01623-07
16. Güttler T, Madl T, Neumann P, Deichsel D, Corsini L, Monecke T, Ficner R, Sattler M, Görlich D. 2010. NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nature Structural & Molecular Biology 17: 1367-1376. doi: 10.1038/nsmb.1931
17. Güttler T, Görlich D. 2011. Ran-dependent nuclear export mediators: a structural perspective. EMBO Journal 30: 3457-3474. doi: 10.1038/emboj.2011.287
18. Hayashi K, Morita T. 2013. Differences in the nuclear export mechanism between myocardin and myocardin-related transcription factor A. Journal of Biological Chemistry 288: 5743-5755. doi: 10.1074/jbc.M112.408120
19. Henderson BR, Eleftheriou A. 2000. A comparison of the activity, sequence specificity, and CRM1-dependence of different nuclear export signals. Experimental Cell Research 256: 213-224. doi: 10.1006/excr.2000.4825
20. Hirano H, Matsuura Y. 2011. Sensing actin dynamics: structural basis for G-actin-sensitive nuclear import of MAL. Biochemical and Biophysical Research Communications 414: 373-378. doi: 10.1016/j.bbrc.2011.09.079
21. Hsu PP, Kang SA, Rameseder J, Zhang Y, Ottina KA, Lim D, Peterson TR, Choi Y, Gray NS, Yaffe MB, Marto JA, Sabatini DM. 2011. The mTOR-regulated phosphoproteome reveals a mechanism of mTORC1-mediated inhibition of growth factor signaling. Science 332: 1317-1322. doi: 10.1126/science.1199498
22. Ishikawa M, Shiota J, Ishibashi Y, Hakamata T, Shoji S, Fukuchi M, Tsuda M, Shirao T, Sekino Y, Ohtsuka T, Baraban JM, Tabuchi A. 2013. Identification, expression and characterization of rat isoforms of the serum response factor (SRF) coactivator MKL1. FEBS Open Bio 3: 387-393. doi: 10.1016/j.fob.2013.09.001
23. Kalita K, Kharebava G, Zheng JJ, Hetman M. 2006. Role of megakaryoblastic acute leukemia-1 in ERK1/2-dependent stimulation of serum response factor-driven transcription by BDNF or increased synaptic activity. Journal of Neuroscience 26: 10020-10032. doi: 10.1523/JNEUROSCI.2644-06.2006
24. Kosugi S, Yanagawa H, Terauchi R, Tabata S. 2014. NESmapper: accurate prediction of leucine-rich nuclear export signals using activity-based profiles. PLOS Computational Biology 10: e1003841. doi: 10.1371/journal.pcbi.1003841
25. la Cour T, Kiemer L, Mølgaard A, Gupta R, Skriver K, Brunak S. 2004. Analysis and prediction of leucine-rich nuclear export signals. Protein Engineering Design and Selection 17: 527-536. doi: 10.1093/protein/gzh062
26. Mansour SJ, Matten WT, Hermann AS, Candia JM, Rong S, Fukasawa K, Vande Woude GF, Ahn NG. 1994. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265: 966-970. doi: 10.1126/science.8052857
27. Martiny-Baron G, Kazanietz MG, Mischak H, Blumberg PM, Kochs G, Hug H, Marmé D, Schächtele C. 1993. Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. Journal of Biological Chemistry 268: 9194-9197.
28. Medjkane S, Perez-Sanchez C, Gaggioli C, Sahai E, Treisman R. 2009. Myocardin-related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nature Cell Biology 11: 257-268. doi: 10.1038/ncb1833
29. Miralles F, Posern G, Zaromytidou AI, Treisman R. 2003. Actin dynamics control SRF activity by regulation of its coactivator MAL. Cell 113: 329-342. doi: 10.1016/s0092-8674(03)00278-2
30. Mouilleron S, Guettler S, Langer CA, Treisman R, McDonald NQ. 2008. Molecular basis for G-actin binding to RPEL motifs from the serum response factor coactivator MAL. EMBO Journal 27: 3198-3208. doi: 10.1038/emboj.2008.235
31. Mouilleron S, Langer CA, Guettler S, McDonald NQ, Treisman R. 2011. Structure of a pentavalent G-actin*MRTF-A complex reveals how G-actin controls nucleocytoplasmic shuttling of a transcriptional coactivator. Science Signaling 4: ra40. doi: 10.1126/scisignal.2001750
32. Muehlich S, Wang R, Lee SM, Lewis TC, Dai C, Prywes R. 2008. Serum-induced phosphorylation of the serum response factor coactivator MKL1 by the extracellular signal-regulated kinase 1/2 pathway inhibits its nuclear localization. Molecular and Cellular Biology 28: 6302-6313. doi: 10.1128/MCB.00427-08
33. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, Mann M. 2006. Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127: 635-648. doi: 10.1016/j.cell.2006.09.026
34. Olson EN, Nordheim A. 2010. Linking actin dynamics and gene transcription to drive cellular motile functions. Nature Reviews Molecular Cell Biology 11: 353-365. doi: 10.1038/nrm2890
35. Pawłowski R, Rajakylä EK, Vartiainen MK, Treisman R. 2010. An actin-regulated importin a/b-dependent extended bipartite NLS directs nuclear import of MRTF-A. The EMBO Journal 29: 3448-3458. doi: 10.1038/emboj.2010.216
36. Posern G, Treisman R. 2006. Actin’ together: serum response factor, its cofactors and the link to signal transduction. Trends in Cell Biology 16: 588-596. doi: 10.1016/j.tcb.2006.09.008
37. Rajakylä EK, Viita T, Kyheröinen S, Huet G, Treisman R, Vartiainen MK. 2015. RNA export factor Ddx19 is required for nuclear import of the SRF coactivator MKL1. Nature Communications 6: 5978. doi: 10.1038/ncomms6978
38. Schratt G, Philippar U, Berger J, Schwarz H, Heidenreich O, Nordheim A. 2002. Serum response factor is crucial for actin cytoskeletal organization and focal adhesion assembly in embryonic stem cells. Journal of Cell Biology 156: 737-750. doi: 10.1083/jcb.200106008
39. Tanoue T, Nishida E. 2003. Molecular recognitions in the MAP kinase cascades. Cellular Signalling 15: 455-462. doi: 10.1016/s0898-6568(02)00112-2
40. Taurin S, Sandbo N, Yau DM, Sethakorn N, Kach J, Dulin NO. 2009. Phosphorylation of myocardin by extracellular signal-regulated kinase. Journal of Biological Chemistry 284: 33789-33794. doi: 10.1074/jbc.M109.048983
41. Torres E, Rosen MK. 2003. Contingent phosphorylation/dephosphorylation provides a mechanism of molecular memory in WASP. Molecular Cell 11: 1215-1227. doi: 10.1016/s1097-2765(03)00139-4
42. Vartiainen MK, Guettler S, Larijani B, Treisman R. 2007. Nuclear actin regulates dynamic subcellular localization and activity of the SRF cofactor MAL. Science 316: 1749-1752. doi: 10.1126/science.1141084
43. Wang D, Chang PS, Wang Z, Sutherland L, Richardson JA, Small E, Krieg PA, Olson EN. 2001. Activation of cardiac gene expression by myocardin, a transcriptional cofactor for serum response factor. Cell 105: 851-862. doi: 10.1016/S0092-8674(01)00404-4
44. Wiezlak M, Diring J, Abella J, Mouilleron S, Way M, McDonald NQ, Treisman R. 2012. G-actin regulates the shuttling and PP1 binding of the RPEL protein Phactr1 to control actomyosin assembly. Journal of Cell Science 125: 5860-5872. doi: 10.1242/jcs.112078
45. Wu X, Tian L, Li J, Zhang Y, Han V, Li Y, Xu X, Li H, Chen X, Chen J, Jin W, Xie Y, Han J, Zhong CQ. 2012. Investigation of receptor interacting protein (RIP3)-dependent protein phosphorylation by quantitative phosphoproteomics. Molecular & Cellular Proteomics 11: 1640-1651. doi: 10.1074/mcp.M112.019091
46. Xie P, Fan Y, Zhang H, Zhang Y, She M, Gu D, Patterson C, Li H. 2009. CHIP represses myocardin-induced smooth muscle cell differentiation via ubiquitin-mediated proteasomal degradation. Molecular and Cellular Biology 29: 2398-2408. doi: 10.1128/MCB.01737-08
47. Yu Y, Yoon SO, Poulogiannis G, Yang Q, Ma XM, Villén J, Kubica N, Hoffman GR, Cantley LC, Gygi SP, Blenis J. 2011. Phosphoproteomic analysis identifies Grb10 as an mTORC1 substrate that negatively regulates insulin signaling. Science 332: 1322-1326. doi: 10.1126/science.1199484