Formation and Maturation of Phase-Separated Liquid Droplets by RNA-Binding Proteins

Molecular Cell

Volumn 60, Issue 2, 2015, Pages 208-219

  Lin, Yuan ^a,b,d   Protter, David S W ^a,c,d   Rosen, Michael K ^a,b,d   Parker, Roy ^a,c,d  

^a MARINE BIOLOGICAL LABORATORY   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID; INTRINSICALLY DISORDERED PROTEIN; PROTEIN; PROTEIN HNRNPA1; RIBONUCLEOPROTEIN; RNA; RNA BINDING PROTEIN; SODIUM CHLORIDE; UNCLASSIFIED DRUG; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN GROUP A B; HNRNP A1; MACROGOL DERIVATIVE; PROTEIN BINDING; RECOMBINANT PROTEIN; SOLUTION AND SOLUBILITY;

ARTICLE; CELL FUNCTION; CELL GRANULE; CELL STRUCTURE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; IN VITRO STUDY; IN VIVO STUDY; LIQUID; MOLECULAR DYNAMICS; NONHUMAN; PHASE SEPARATION; PHYSICAL CHEMISTRY; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN RNA BINDING; CELL ORGANELLE; CHEMISTRY; ESCHERICHIA COLI; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; MOLECULAR MIMICRY; PATHOLOGY; PROTEIN TERTIARY STRUCTURE; PROTEINOSIS; SOLUTION AND SOLUBILITY;

AMYLOID; CYTOPLASMIC GRANULES; ESCHERICHIA COLI; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENE EXPRESSION; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEIN GROUP A-B; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR MIMICRY; ORGANELLES; POLYETHYLENE GLYCOLS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA; SODIUM CHLORIDE; SOLUTIONS;

EID: 84944884978     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.08.018     Document Type: Article

References (41)

1. Asherie N., Pande J., Lomakin A., Ogun O., Hanson S.R., Smith J.B., Benedek G.B. Oligomerization and phase separation in globular protein solutions. Biophys. Chem. 1998, 75:213-227.
2. Banjade S., Rosen M.K. Phase transitions of multivalent proteins can promote clustering of membrane receptors. eLife 2014, 3:04123.
3. Beck M., Schmidt A., Malmstroem J., Claassen M., Ori A., Szymborska A., Herzog F., Rinner O., Ellenberg J., Aebersold R. The quantitative proteome of a human cell line. Mol. Syst. Biol. 2011, 7:549.
4. Brangwynne C.P., Eckmann C.R., Courson D.S., Rybarska A., Hoege C., Gharakhani J., Jülicher F., Hyman A.A. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 2009, 324:1729-1732.
5. Brangwynne C.P., Mitchison T.J., Hyman A.A. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. Proc. Natl. Acad. Sci. USA 2011, 108:4334-4339.
6. Buchan J.R., Parker R. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 2009, 36:932-941.
7. Buchan J.R., Muhlrad D., Parker R. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. Cell Biol. 2008, 183:441-455.
8. Buchan J.R., Kolaitis R.M., Taylor J.P., Parker R. Eukaryotic stress granules are cleared by autophagy and Cdc48/VCP function. Cell 2013, 153:1461-1474.
9. Decker C.J., Teixeira D., Parker R. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. Cell Biol. 2007, 179:437-449.
10. Eisenberg D., Jucker M. The amyloid state of proteins in human diseases. Cell 2012, 148:1188-1203.
11. Elbaum-Garfinkle S., Kim Y., Szczepaniak K., Chen C.C.H., Eckmann C.R., Myong S., Brangwynne C.P. The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. Proc. Natl. Acad. Sci. USA 2015, 112:7189-7194.
12. Flory P.J. Principles of polymer Chemistry 1953, Cornell University Press.
13. Fromm S.A., Kamenz J., Nöldeke E.R., Neu A., Zocher G., Sprangers R. In vitro reconstitution of a cellular phase-transition process that involves the mRNA decapping machinery. Angew. Chem. Int. Ed. Engl. 2014, 53:7354-7359.
14. Gilks N., Kedersha N., Ayodele M., Shen L., Stoecklin G., Dember L.M., Anderson P. Stress granule assembly is mediated by prion-like aggregation of TIA-1. Mol. Biol. Cell 2004, 15:5383-5398.
15. Guil S., Long J.C., Cáceres J.F. hnRNP A1 relocalization to the stress granules reflects a role in the stress response. Mol. Cell. Biol. 2006, 26:5744-5758.
16. Han T.W., Kato M., Xie S., Wu L.C., Mirzaei H., Pei J., Chen M., Xie Y., Allen J., Xiao G., McKnight S.L. Cell-free formation of RNA granules: bound RNAs identify features and components of cellular assemblies. Cell 2012, 149:768-779.
17. Handwerger K.E., Cordero J.A., Gall J.G. Cajal bodies, nucleoli, and speckles in the Xenopus oocyte nucleus have a low-density, sponge-like structure. Mol. Biol. Cell 2005, 16:202-211.
18. Jonas S., Izaurralde E. The role of disordered protein regions in the assembly of decapping complexes and RNP granules. Genes Dev. 2013, 27:2628-2641.
19. Kato M., Han T.W., Xie S., Shi K., Du X., Wu L.C., Mirzaei H., Goldsmith E.J., Longgood J., Pei J., et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 2012, 149:753-767.
20. Kim H.J., Kim N.C., Wang Y.D., Scarborough E.A., Moore J., Diaz Z., MacLea K.S., Freibaum B., Li S., Molliex A., et al. Mutations in prion-like domains in hnRNPA2B1 and hnRNPA1 cause multisystem proteinopathy and ALS. Nature 2013, 495:467-473.
21. King O.D., Gitler A.D., Shorter J. The tip of the iceberg: RNA-binding proteins with prion-like domains in neurodegenerative disease. Brain Res. 2012, 1462:61-80.
22. Lee C., Zhang H., Baker A.E., Occhipinti P., Borsuk M.E., Gladfelter A.S. Protein aggregation behavior regulates cyclin transcript localization and cell-cycle control. Dev. Cell 2013, 25:572-584.
23. Li P., Banjade S., Cheng H.C., Kim S., Chen B., Guo L., Llaguno M., Hollingsworth J.V., King D.S., Banani S.F., et al. Phase transitions in the assembly of multivalent signalling proteins. Nature 2012, 483:336-340.
24. Li Y.R., King O.D., Shorter J., Gitler A.D. Stress granules as crucibles of ALS pathogenesis. J. Cell Biol. 2013, 201:361-372.
25. Ling S.H., Decker C.J., Walsh M.A., She M., Parker R., Song H. Crystal structure of human Edc3 and its functional implications. Mol. Cell. Biol. 2008, 28:5965-5976.
26. Molliex A., Temirov J., Lee J., Coughlin M., Kanagaraj A.P., Kim H.J., Mittag T., Taylor J.P. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 2015, 163:123-133.
27. Nott T.J., Petsalaki E., Farber P., Jervis D., Fussner E., Plochowietz A., Craggs T.D., Bazett-Jones D.P., Pawson T., Forman-Kay J.D., Baldwin A.J. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol. Cell 2015, 57:936-947.
28. Pande J., Lomakin A., Fine B., Ogun O., Sokolinski I., Benedek G. Oxidation of gamma II-crystallin solutions yields dimers with a high phase separation temperature. Proc. Natl. Acad. Sci. USA 1995, 92:1067-1071.
29. Ramaswami M., Taylor J.P., Parker R. Altered ribostasis: RNA-protein granules in degenerative disorders. Cell 2013, 154:727-736.
30. Reijns M.A., Alexander R.D., Spiller M.P., Beggs J.D. A role for Q/N-rich aggregation-prone regions in P-body localization. J. Cell Sci. 2008, 121:2463-2472.
31. Schwartz J.C., Podell E.R., Han S.S., Berry J.D., Eggan K.C., Cech T.R. FUS is sequestered in nuclear aggregates in ALS patient fibroblasts. Mol. Biol. Cell 2014, 25:2571-2578.
32. Souquere S., Mollet S., Kress M., Dautry F., Pierron G., Weil D. Unravelling the ultrastructure of stress granules and associated P-bodies in human cells. J. Cell Sci. 2009, 122:3619-3626.
33. Spector D.L. SnapShot: Cellular bodies. Cell 2006, 127:1071.
34. Sun Z., Diaz Z., Fang X., Hart M.P., Chesi A., Shorter J., Gitler A.D. Molecular determinants and genetic modifiers of aggregation and toxicity for the ALS disease protein FUS/TLS. PLoS Biol. 2011, 9:e1000614.
35. Teixeira D., Sheth U., Valencia-Sanchez M.A., Brengues M., Parker R. Processing bodies require RNA for assembly and contain nontranslating mRNAs. RNA 2005, 11:371-382.
36. Updike D.L., Hachey S.J., Kreher J., Strome S. P granules extend the nuclear pore complex environment in the C. elegans germ line. J. Cell Biol. 2011, 192:939-948.
37. Walters R.W., Muhlrad D., Garcia J., Parker R. Differential effects of Ydj1 and Sis1 on Hsp70-mediated clearance of stress granules in Saccharomyces cerevisiae. RNA 2015, 21:1660-1671.
38. Wang J.T., Smith J., Chen B.C., Schmidt H., Rasoloson D., Paix A., Lambrus B.G., Calidas D., Betzig E., Seydoux G. Regulation of RNA granule dynamics by phosphorylation of serine-rich, intrinsically disordered proteins in C. elegans. eLife 2014, 3:e04591.
39. Weber S.C., Brangwynne C.P. Inverse size scaling of the nucleolus by a concentration-dependent phase transition. Curr. Biol. 2015, 25:641-646.
40. Yang Z., Jakymiw A., Wood M.R., Eystathioy T., Rubin R.L., Fritzler M.J., Chan E.K. GW182 is critical for the stability of GW bodies expressed during the cell cycle and cell proliferation. J. Cell Sci. 2004, 117:5567-5578.
41. Yeo G.C., Keeley F.W., Weiss A.S. Coacervation of tropoelastin. Adv. Colloid Interface Sci. 2011, 167:94-103.