1932

Abstract

RNA localization mechanisms have been intensively studied and include localized protection of mRNA from degradation, diffusion-coupled local entrapment of mRNA, and directed transport of mRNAs along the cytoskeleton. While it is well understood how cells utilize these three mechanisms to organize mRNAs within the cytoplasm, a newly appreciated mechanism of RNA localization has emerged in recent years in which mRNAs phase-separate and form liquid-like droplets. mRNAs both contribute to condensation of proteins into liquid-like structures and are themselves regulated by being incorporated into membraneless organelles. This ability to condense into droplets is in many instances contributing to previously appreciated mRNA localization phenomena. Here we review how phase separation enables mRNAs to selectively and efficiently colocalize and be coregulated, allowing control of gene expression in time and space.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090817-062814
2018-09-08
2024-06-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/72/1/annurev-micro-090817-062814.html?itemId=/content/journals/10.1146/annurev-micro-090817-062814&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Anderson CA, Eser U, Korndorf T, Borsuk ME, Skotheim JM, Gladfelter AS 2013. Nuclear repulsion enables division autonomy in a single cytoplasm. Curr. Biol. 23:201999–2010
    [Google Scholar]
  2. 2.  Ayad-Durieux Y, Knechtle P, Goff S, Dietrich F, Philippsen P 2000. A PAK-like protein kinase is required for maturation of young hyphae and septation in the filamentous ascomycete Ashbya gossypii.. J. Cell Sci1–13
    [Google Scholar]
  3. 3.  Banani SF, Lee HO, Hyman AA, Rosen MK 2017. Biomolecular condensates: organizers of cellular biochemistry. Nat. Rev. Mol. Cell Biol. 18:5285–98
    [Google Scholar]
  4. 4.  Baumann S, Pohlmann T, Jungbluth M, Brachmann A, Feldbrugge M 2012. Kinesin-3 and dynein mediate microtubule-dependent co-transport of mRNPs and endosomes. J. Cell Sci. 125:112740–52
    [Google Scholar]
  5. 5.  Berchowitz LE, Kabachinski G, Walker MR, Carlile TM, Gilbert WV et al. 2015. Regulated formation of an amyloid-like translational repressor governs gametogenesis. Cell 163:2406–18
    [Google Scholar]
  6. 6.  Bertrand E, Chartrand P, Schaefer M, Shenoy SM, Singer RH, Long RM 1998. Localization of ASH1 mRNA particles in living yeast. Mol. Cell 2:4437–45
    [Google Scholar]
  7. 7.  Bramham CR, Wells DG 2007. Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 8:10776–89
    [Google Scholar]
  8. 8.  Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C et al. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:59351729–32
    [Google Scholar]
  9. 9.  Brangwynne CP, Mitchison TJ, Hyman AA 2011. Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes. PNAS 108:114334–39
    [Google Scholar]
  10. 10.  Brangwynne CP, Tompa P, Pappu RV 2015. Polymer physics of intracellular phase transitions. Nat. Phys. 11:11899–904
    [Google Scholar]
  11. 11.  Buchan JR, Muhlrad D, Parker R 2008. P bodies promote stress granule assembly in Saccharomyces cerevisiae. J. . Cell Biol 183:3441–55
    [Google Scholar]
  12. 12.  Buchan JR, Parker R 2009. Eukaryotic stress granules: the ins and outs of translation. Mol. Cell 36:6932–41
    [Google Scholar]
  13. 13.  Buchan JR, Yoon JH, Parker R 2010. Stress-specific composition, assembly and kinetics of stress granules in Saccharomyces cerevisiae.. J. Cell Sci 124:2228–39
    [Google Scholar]
  14. 14.  Burke KA, Janke AM, Rhine CL, Fawzi NL 2015. Residue-by-residue view of in vitro FUS granules that bind the C-terminal domain of RNA polymerase II. Mol. Cell 60:2231–41
    [Google Scholar]
  15. 15.  Buskila A-AA, Kannaiah S, Amster-Choder O 2014. RNA localization in bacteria. RNA Biol 11:81051–60
    [Google Scholar]
  16. 16.  Buxbaum AR, Haimovich G, Singer RH 2015. In the right place at the right time: visualizing and understanding mRNA localization. Nat. Rev. Mol. Cell Biol. 16:295–109
    [Google Scholar]
  17. 17.  Byrgazov K, Vesper O, Moll I 2013. Ribosome heterogeneity: another level of complexity in bacterial translation regulation. Curr. Opin. Microbiol. 16:2133–39
    [Google Scholar]
  18. 18.  Cajigas IJ, Tushev G, Will TJ, tom Dieck S, Fuerst N, Schuman EM 2012. The local transcriptome in the synaptic neuropil revealed by deep sequencing and high-resolution imaging. Neuron 74:3453–66
    [Google Scholar]
  19. 19.  Cereda M, Pozzoli U, Rot G, Juvan P, Schweitzer A et al. 2014. RNAmotifs: prediction of multivalent RNA motifs that control alternative splicing. Genome Biol 15:1R20
    [Google Scholar]
  20. 20.  Chandarlapaty S, Errede B 1998. Ash1, a daughter cell-specific protein, is required for pseudohyphal growth of Saccharomyces cerevisiae. Mol. Cell. . Biol 18:52884–91
    [Google Scholar]
  21. 21.  Chao JA, Yoon YJ, Singer RH 2012. Imaging translation in single cells using fluorescent microscopy. Cold Spring Harb. Perspect. Biol. 4:11a012310–10
    [Google Scholar]
  22. 22.  Cleveland DW, Lopata MA, Sherline P, Kirschner MW 1981. Unpolymerized tubulin modulates the level of tubulin mRNAs. Cell 25:2537–46
    [Google Scholar]
  23. 23.  Decker CJ, Parker R 2012. P-bodies and stress granules: possible roles in the control of translation and mRNA degradation. Cold Spring Harb. Perspect. Biol. 4:9a012286
    [Google Scholar]
  24. 24.  Decker CJ, Teixeira D, Parker R 2007. Edc3p and a glutamine/asparagine-rich domain of Lsm4p function in processing body assembly in Saccharomyces cerevisiae. J. . Cell Biol 179:3437–49
    [Google Scholar]
  25. 25.  Dictenberg JB, Swanger SA, Antar LN, Singer RH, Bassell GJ 2008. A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev. Cell 14:6926–39
    [Google Scholar]
  26. 26.  Dundon SER, Chang S-S, Kumar A, Occhipinti P, Shroff H et al. 2016. Clustered nuclei maintain autonomy and nucleocytoplasmic ratio control in a syncytium. Mol. Biol. Cell 27:132000–7
    [Google Scholar]
  27. 27.  Eddy EM 1975. Germ plasm and the differentiation of the germ cell line. Int. Rev. Cytol. 43:229–80
    [Google Scholar]
  28. 28.  Elbaum-Garfinkle S, Kim Y, Szczepaniak K, Chen CC-H, Eckmann CR et al. 2015. The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. PNAS 112:237189–94
    [Google Scholar]
  29. 29.  Elson SL, Noble SM, Solis NV, Filler SG, Johnson AD 2009. An RNA transport system in Candida albicans regulates hyphal morphology and invasive growth. PLOS Genet 5:9e1000664
    [Google Scholar]
  30. 30.  Erickson SL, Lykke-Andersen J 2011. Cytoplasmic mRNP granules at a glance. J. Cell Sci. 124:3293–97
    [Google Scholar]
  31. 31.  Falkenberg CV, Carson JH, Blinov ML 2017. Multivalent molecules as modulators of RNA granule size and composition. Biophys. J. 113:2245–55
    [Google Scholar]
  32. 32.  Feric M, Brangwynne CP 2013. A nuclear F-actin scaffold stabilizes ribonucleoprotein droplets against gravity in large cells. Nat Cell Biol 15:101253–59
    [Google Scholar]
  33. 33.  Feric M, Vaidya N, Harmon TS, Mitrea DM, Zhu L et al. 2016. Coexisting liquid phases underlie nucleolar subcompartments. Cell 165:71686–97
    [Google Scholar]
  34. 34.  Ferrandon D, Koch I, Westhof E, Nusslein-Volhard C 1997. RNA-RNA interaction is required for the formation of specific bicoid mRNA. EMBO J 16:71751–58
    [Google Scholar]
  35. 35.  Franzmann TM, Jahnel M, Pozniakovsky A, Mahamid J, Holehouse AS et al. 2018. Phase separation of a yeast prion protein promotes cellular fitness. Science 359:6371eaao5654
    [Google Scholar]
  36. 36.  Gadir N, Haim-Vilmovsky L, Kraut-Cohen J, Gerst JE 2011. Localization of mRNAs coding for mitochondrial proteins in the yeast Saccharomyces cerevisiae. . RNA 17:81551–65
    [Google Scholar]
  37. 37.  Giustiniani A, Drenckhan W, Poulard C 2017. Interfacial tension of reactive, liquid interfaces and its consequences. Adv. Colloid Interface Sci. 247:185–97
    [Google Scholar]
  38. 38.  Gladfelter AS, Hungerbuehler AK, Philippsen P 2006. Asynchronous nuclear division cycles in multinucleated cells. J. Cell Biol. 172:3347–62
    [Google Scholar]
  39. 39.  Glock C, Heumüller M, Schuman EM 2017. mRNA transport and local translation in neurons. Curr. Opin. Neurobiol. 45:169–77
    [Google Scholar]
  40. 40.  Gonsalvez GB, Urbinati CR, Long RM 2005. RNA localization in yeast: moving towards a mechanism. Biol. Cell 97:175–86
    [Google Scholar]
  41. 41.  Govindarajan S, Nevo-Dinur K, Amster-Choder O 2012. Compartmentalization and spatiotemporal organization of macromolecules in bacteria. FEMS Microbiol. Rev. 36:51005–22
    [Google Scholar]
  42. 42.  Gumy LF, Yeo GSH, Tung YCL, Zivraj KH, Willis D et al. 2010. Transcriptome analysis of embryonic and adult sensory axons reveals changes in mRNA repertoire localization. RNA 17:185–98
    [Google Scholar]
  43. 43.  Harmon TS, Holehouse AS, Rosen MK, Pappu RV 2017. Intrinsically disordered linkers determine the interplay between phase separation and gelation in multivalent proteins. eLife 6:e30294
    [Google Scholar]
  44. 44.  Hegner RW 1911. The germ cell determinants in the eggs of chrysomelid beetles. Science 33:83771–72
    [Google Scholar]
  45. 45.  Hyman AA, Weber CA, Jülicher F 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:139–58
    [Google Scholar]
  46. 46.  Imai K, Nakai K 2010. Prediction of subcellular locations of proteins: where to proceed?. Proteomics 10:223970–83
    [Google Scholar]
  47. 47.  Jacobs WM, Frenkel D 2017. Phase transitions in biological systems with many components. Biophys. J. 112:4683–91
    [Google Scholar]
  48. 48.  Jain A, Vale RD 2017. RNA phase transitions in repeat expansion disorders. Nature 546:7657243–47
    [Google Scholar]
  49. 49.  Jain N, Lin H-C, Morgan CE, Harris ME, Tolbert BS 2017. Rules of RNA specificity of hnRNP A1 revealed by global and quantitative analysis of its affinity distribution. PNAS 114:92206–11
    [Google Scholar]
  50. 50.  Jain S, Wheeler JR, Walters RW, Agrawal A, Barsic A, Parker R 2016. ATPase-modulated stress granules contain a diverse proteome and substructure. Cell 164:3487–98
    [Google Scholar]
  51. 51.  Jiang H, Wang S, Huang Y, He X, Cui H et al. 2015. Phase transition of spindle-associated protein regulate spindle apparatus assembly. Cell 163:1108–22
    [Google Scholar]
  52. 52.  Jin L, Zhang K, Xu Y, Sternglanz R, Neiman AM 2015. Sequestration of mRNAs modulates the timing of translation during meiosis in budding yeast. Mol. Cell. Biol. 35:203448–58
    [Google Scholar]
  53. 53.  Jung H, Gkogkas CG, Sonenberg N, Holt CE 2014. Remote control of gene function by local translation. Cell 157:126–40
    [Google Scholar]
  54. 54.  Jung H, Yoon BC, Holt CE 2012. Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair. Nat. Rev. Neurosci. 13:5308–24
    [Google Scholar]
  55. 55.  Kedersha N, Stoecklin G, Ayodele M, Yacono P, Lykke-Andersen J et al. 2005. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169:6871–84
    [Google Scholar]
  56. 56.  Keene JD, Tenenbaum SA 2002. Eukaryotic mRNPs may represent posttranscriptional operons. Mol. Cell 9:61161–67
    [Google Scholar]
  57. 57.  Khong A, Matheny T, Jain S, Mitchell SF, Wheeler JR, Parker R 2017. The stress granule transcriptome reveals principles of mRNA accumulation in stress granules. Mol. Cell 68:4808–20.e5
    [Google Scholar]
  58. 58.  Kim H-L, Shin E-K, Kim H-M, Ryou S-M, Kim S et al. 2007. Heterogeneous rRNAs are differentially expressed during the morphological development of Streptomyces coelicolor.FEMS Microbiol. . Lett 275:1146–52
    [Google Scholar]
  59. 59.  Knechtle P, Dietrich F, Philippsen P 2003. Maximal polar growth potential depends on the polarisome component AgSpa2 in the filamentous fungus Ashbya gossypii. Mol. Biol. . Cell 14:104140–54
    [Google Scholar]
  60. 60.  Komili S, Farny NG, Roth FP, Silver PA 2007. Functional specificity among ribosomal proteins regulates gene expression. Cell 131:3557–71
    [Google Scholar]
  61. 61.  Krichevsky AM, Kosik KS 2001. Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32:4683–96
    [Google Scholar]
  62. 62.  Kroschwald S, Maharana S, Mateju D, Malinovska L, Nuske E et al. 2015. Promiscuous interactions and protein disaggregases determine the material state of stress-inducible RNP granules. eLife 4:e068071–32
    [Google Scholar]
  63. 63.  Kwon S, Zhang Y, Matthias P 2007. The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response. Genes Dev 21:243381–94
    [Google Scholar]
  64. 64.  Langdon EM, Qiu Y, Ghanbari Niaki A, McLaughlin GA, Weidmann CA et al. 2018. mRNA structure determines specificity of a polyQ-driven phase separation. Science 157:eaar7432–13
    [Google Scholar]
  65. 65.  Lawrence J 1986. Intracellular localization of messenger RNAs for cytoskeletal proteins. Cell 45:3407–15
    [Google Scholar]
  66. 66.  Lécuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T et al. 2007. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131:1174–87
    [Google Scholar]
  67. 67.  Lee C, Occhipinti P, Gladfelter AS 2015. PolyQ-dependent RNA-protein assemblies control symmetry breaking. J. Cell Biol. 208:5533–44
    [Google Scholar]
  68. 68.  Lee C, Zhang H, Baker AE, Occhipinti P, Borsuk ME, Gladfelter AS 2013. Protein aggregation behavior regulates cyclin transcript localization and cell-cycle control. Dev. Cell 25:6572–84
    [Google Scholar]
  69. 69.  Lenz P, Søgaard-Andersen L 2011. Temporal and spatial oscillations in bacteria. Nat. Rev. Microbiol. 9:8565–77
    [Google Scholar]
  70. 70.  Lewis PJ, Thaker SD, Errington J 2000. Compartmentalization of transcription and translation in Bacillus subtilis. . EMBO J 19:4710–18
    [Google Scholar]
  71. 71.  Li P, Banjade S, Cheng H-C, Kim S, Chen B et al. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:7389336–40
    [Google Scholar]
  72. 72.  Lin Y, Protter DSW, Rosen MK, Parker R 2015. Formation and maturation of phase-separated liquid droplets by RNA-binding proteins. Mol. Cell 60:2208–19
    [Google Scholar]
  73. 73.  Long RM, Singer RH, Meng X, Gonzalez I, Nasmyth K, Jansen RP 1997. Mating type switching in yeast controlled by asymmetric localization of ASH1 mRNA. Science 277:5324383–87
    [Google Scholar]
  74. 74.  Maharana S, Wang J, Papadopoulos DK, Richter D, Pozniakovsky A et al. 2018. RNA buffers the phase separation behavior of prion-like RNA binding proteins. Science 157:eaar7366–10
    [Google Scholar]
  75. 75.  Maris C, Dominguez C, Allain FHT 2005. The RNA recognition motif, a plastic RNA-binding platform to regulate post-transcriptional gene expression. FEBS J 272:92118–31
    [Google Scholar]
  76. 76.  Mayr C 2016. Evolution and biological roles of alternative 3′UTRs. Trends Cell Biol 26:3227–37
    [Google Scholar]
  77. 77.  McBride AE 2017. Messenger RNA transport in the opportunistic fungal pathogen Candida albicans.Curr. . Genet 63:6989–95
    [Google Scholar]
  78. 78.  Mili S, Moissoglu K, Macara IG 2008. Genome-wide screen reveals APC-associated RNAs enriched in cell protrusions. Nature 453:7191115–19
    [Google Scholar]
  79. 79.  Mingle LA, Okuhama NN, Shi J, Singer RH, Condeelis J, Liu G 2005. Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J. Cell Sci. 118:Part 112425–33
    [Google Scholar]
  80. 80.  Molliex A, Temirov J, Lee J, Coughlin M, Kanagaraj AP et al. 2015. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization. Cell 163:1123–33
    [Google Scholar]
  81. 81.  Monahan Z, Ryan VH, Janke AM, Burke KA, Rhoads SN et al. 2017. Phosphorylation of the FUS low-complexity domain disrupts phase separation, aggregation, and toxicity. EMBO J 36:202951–67
    [Google Scholar]
  82. 82.  Monterroso B, Zorrilla S, Sobrinos-Sanguino M, Keating CD, Rivas G 2016. Microenvironments created by liquid-liquid phase transition control the dynamic distribution of bacterial division FtsZ protein. Sci. Rep. 6:35140
    [Google Scholar]
  83. 83.  Nevo-Dinur K, Nussbaum-Shochat A, Ben-Yehuda S, Amster-Choder O 2011. Translation-independent localization of mRNA in E. coli. . Science 331:60201081–84
    [Google Scholar]
  84. 84.  Ohn T, Kedersha N, Hickman T, Tisdale S, Anderson P 2008. A functional RNAi screen links O-GlcNAc modification of ribosomal proteins to stress granule and processing body assembly. Nat. Cell Biol. 10:101224–31
    [Google Scholar]
  85. 85.  Protter DSW, Parker R 2016. Principles and properties of stress granules. Trends Cell Biol 26:9668–79
    [Google Scholar]
  86. 86.  Rao BS, Parker R 2017. Numerous interactions act redundantly to assemble a tunable size of P bodies in Saccharomyces cerevisiae. . PNAS 114:45E9569–78
    [Google Scholar]
  87. 87.  Riback JA, Katanski CA, Kear-Scott JL, Pilipenko EV, Sosnick TR, Drummond DA 2017. How evolution tunes stress-triggered protein phase separation to promote cell fitness during stress. Biophys. J. 112:35a
    [Google Scholar]
  88. 88.  Riback JA, Katanski CD, Kear-Scott JL, Pilipenko EV, Rojek AE et al. 2017. Stress-triggered phase separation is an adaptive, evolutionarily tuned response. Cell 168:61028–40.e19
    [Google Scholar]
  89. 89.  Riquelme M 2013. Tip growth in filamentous fungi: a road trip to the apex. Annu. Rev. Microbiol. 67:1587–609
    [Google Scholar]
  90. 90.  Rodriguez AJ, Shenoy SM, Singer RH, Condeelis J 2006. Visualization of mRNA translation in living cells. J. Cell Biol. 175:167–76
    [Google Scholar]
  91. 91.  Rog O, Kohler S, Dernburg AF 2017. The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors. eLife 6:e214551
    [Google Scholar]
  92. 92.  Rudner DZ, Pan Q, Losick RM 2002. Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. PNAS 99:138701–6
    [Google Scholar]
  93. 93.  Russell JH, Keiler KC 2009. Subcellular localization of a bacterial regulatory RNA. PNAS 106:38164051–59
    [Google Scholar]
  94. 94.  Saha S, Weber CA, Nousch M, Adame-Arana O, Hoege C et al. 2016. Polar positioning of phase-separated liquid compartments in cells regulated by an mRNA competition mechanism. Cell 166:61572–84.e16
    [Google Scholar]
  95. 95.  Schwartz JC, Wang X, Podell ER, Cech TR 2013. RNA seeds higher order assembly of FUS protein. Cell Rep 5:4918–25
    [Google Scholar]
  96. 96.  Shapiro L, McAdams HH, Losick R 2009. Why and how bacteria localize proteins. Science 326:59571225–28
    [Google Scholar]
  97. 97.  Shepard KA, Gerber AP, Jambhekar A, Takizawa PA, Brown PO et al. 2011. Widespread cytoplasmic mRNA transport in yeast: identification of 22 bud-localized transcripts using DNA microarray analysis. PNAS 100:2011429–34
    [Google Scholar]
  98. 98.  Shi Z, Fujii K, Kovary KM, Genuth NR, Röst HL et al. 2017. Heterogeneous ribosomes preferentially translate distinct subpools of mRNAs genome-wide. Mol. Cell 67:171–83.e77
    [Google Scholar]
  99. 99.  Shin Y, Brangwynne CP 2017. Liquid phase condensation in cell physiology and disease. Science 357:6357eaaf4382
    [Google Scholar]
  100. 100.  Simsek D, Tiu GC, Flynn RA, Byeon GW, Leppek K et al. 2017. The mammalian ribo-interactome reveals ribosome functional diversity and heterogeneity. Cell 169:61051–57.e18
    [Google Scholar]
  101. 101.  Smith J, Calidas D, Schmidt H, Lu T, Rasoloson D, Seydoux G 2016. Spatial patterning of P granules by RNA-induced phase separation of the intrinsically-disordered protein MEG-3. eLife 5:e21337
    [Google Scholar]
  102. 102.  Strom AR, Emelyanov AV, Mir M, Fyodorov DV, Darzacq X, Karpen GH 2017. Phase separation drives heterochromatin domain formation. Nature 547:7662241–45
    [Google Scholar]
  103. 103.  Strulson CA, Molden RC, Keating CD, Bevilacqua PC 2012. RNA catalysis through compartmentalization. Nat. Chem. 4:11941–46
    [Google Scholar]
  104. 104.  Su X, Ditlev JA, Hui E, Xing W, Banjade S et al. 2016. Phase separation of signaling molecules promotes T cell receptor signal transduction. Science 352:6285595–99
    [Google Scholar]
  105. 105.  Sutton MA, Schuman EM 2006. Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127:149–58
    [Google Scholar]
  106. 106.  Taliaferro JM, Lambert NJ, Sudmant PH, Dominguez D, Merkin JJ et al. 2016. RNA sequence context effects measured in vitro predict in vivo protein binding and regulation. Mol. Cell 64:2294–306
    [Google Scholar]
  107. 107.  Tamayo JV, Teramoto T, Chatterjee S, Hall TMT, Gavis ER 2017. The Drosophila hnRNP F/H homolog Glorund uses two distinct RNA-binding modes to diversify target recognition. Cell Rep 19:1150–61
    [Google Scholar]
  108. 108.  Taylor AM, Berchtold NC, Perreau VM, Tu CH, Li Jeon N, Cotman CW 2009. Axonal mRNA in uninjured and regenerating cortical mammalian axons. J. Neurosci. 29:154697–707
    [Google Scholar]
  109. 109.  Terasaki M, Okumura E-I, Hinkle B, Kishimoto T 2003. Localization and dynamics of Cdc2-Cyclin B during meiotic reinitiation in starfish oocytes. Mol. Biol. Cell 14:4685–94
    [Google Scholar]
  110. 110.  Thandapani P, O'Connor TR, Bailey TL, Richard S 2013. Defining the RGG/RG motif. Mol. Cell 50:5613–23
    [Google Scholar]
  111. 111.  Trcek T, Grosch M, York A, Shroff H, Lionnet T, Lehmann R 2015. Drosophila germ granules are structured and contain homotypic mRNA clusters. Nat. Commun. 6:17962
    [Google Scholar]
  112. 112.  Valencia-Burton M, Shah A, Sutin J, Borogovac A, McCullough RM et al. 2009. Spatiotemporal patterns and transcription kinetics of induced RNA in single bacterial cells. PNAS 106:3816399–404
    [Google Scholar]
  113. 113.  Van Treeck B, Protter DSW, Matheny T, Khong A, Link CD, Parker R 2018. RNA self-assembly contributes to stress granule formation and defining the stress granule transcriptome. PNAS 115:112734–39
    [Google Scholar]
  114. 114.  Vollmeister E, Schipper K, Baumann S, Haag C, Pohlmann T et al. 2012. Fungal development of the plant pathogen Ustilago maydis.FEMS Microbiol. . Rev 36:159–77
    [Google Scholar]
  115. 115.  Wall FT 1954. Principles of Polymer Chemistry Paul J. Flory. Cornell Univ. Press, Ithaca New York: 1953. Science 119:3095555–56
    [Google Scholar]
  116. 116.  Weatheritt RJ, Gibson TJ, Babu MM 2014. Asymmetric mRNA localization contributes to fidelity and sensitivity of spatially localized systems. Nat. Struct. Mol. Biol. 21:9833–39
    [Google Scholar]
  117. 117.  Weber SC, Brangwynne CP 2015. Inverse size scaling of the nucleolus by a concentration-dependent phase transition. Curr. Biol. 25:5641–46
    [Google Scholar]
  118. 118.  Wheeler JR, Matheny T, Jain S, Abrisch R, Parker R 2016. Distinct stages in stress granule assembly and disassembly. eLife 5:e18413
    [Google Scholar]
  119. 119.  Willis DE, van Niekerk EA, Sasaki Y, Mesngon M, Merianda TT et al. 2007. Extracellular stimuli specifically regulate localized levels of individual neuronal mRNAs. J. Cell Biol. 178:6965–80
    [Google Scholar]
  120. 120.  Wippich F, Bodenmiller B, Trajkovska MG, Wanka S, Aebersold R, Pelkmans L 2013. Dual specificity kinase DYRK3 couples stress granule condensation/dissolution to mTORC1 signaling. Cell 152:4791–805
    [Google Scholar]
  121. 121.  Wu B, Eliscovich C, Yoon YJ, Singer RH 2016. Translation dynamics of single mRNAs in live cells and neurons. Science 352:62921430–35
    [Google Scholar]
  122. 122.  Xue S, Tian S, Fujii K, Kladwang W, Das R, Barna M 2015. RNA regulons in Hox 5′ UTRs confer ribosome specificity to gene regulation. Nature 517:753233–38
    [Google Scholar]
  123. 123.  Zander S, Baumann S, Weidtkamp-Peters S, Feldbrügge M 2016. Endosomal assembly and transport of heteromeric septin complexes promote septin cytoskeleton formation. J. Cell Sci. 129:142778–92
    [Google Scholar]
  124. 124.  Zhang H, Elbaum-Garfinkle S, Langdon EM, Taylor N, Occhipinti P et al. 2015. RNA controls polyQ protein phase transitions. Mol. Cell 60:2220–30
    [Google Scholar]
  125. 125.  Zivraj KH, Tung YCL, Piper M, Gumy L, Fawcett JW et al. 2010. Subcellular profiling reveals distinct and developmentally regulated repertoire of growth cone mRNAs. J. Neurosci. 30:4615464–78
    [Google Scholar]
/content/journals/10.1146/annurev-micro-090817-062814
Loading
/content/journals/10.1146/annurev-micro-090817-062814
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error