Abstract
This review describes the critical evidence that in eukaryotic cells polyribosomes, mRNAs and components of the protein synthetic machinery are associated with the cytoskeleton. The role of microtubules, intermediate filaments and microfilaments are discussed; at present most evidence suggests that polyribosomes interact with the actin filaments. The use of non-ionic detergent/deoxycholate treatment in the isolation of cytoskeletal-bound polysomes is described and the conclusion reached that at low salt concentrations this leads to mixed preparations of polysomes derived from both the cytoskeleton and the endoplasmic reticulum. At present the best approach for isolation of cytoskeletal-bound polysomes appears to involve extraction with salt concentrations greater than 130 mM after an initial non-ionic detergent treatment. Such polysomes appear to be enriched in certain mRNAs and thus it is suggested that they are involved in translation of a unique set of proteins. The evidence for mRNA localisation is presented and the role of the cytoskeleton in transport and localisation of RNA discussed. Recent data on the role of the 3′ untranslated region in the targeting of mRNAs both to particular regions of the cell and for translation on cytoskeletal-bound polysomes is described. The hypothesis is developed that the association of polysomes with the cytoskeleton is the basis of a mechanism for the targeting of mRNAs and the compartmentalization of protein synthesis.
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Abbreviations
- CBP:
-
cytoskeletal-bound polysomes
- FP:
-
free polysomes
- MBP:
-
membrane-bound polysomes
- ER:
-
endoplasmic reticulum
References
Silver PA (1991) Cell 64: 489–497
Blobel G & Dobberstein B (1975) J. Cell Biol. 67: 835–851
Hesketh JE & Pryme IF (1991) Biochem. J. 277: 1–10
Fulton AB (1993) J. Cell. Biochem. 52: 148–152
Luby-Phelps K (1993) J. Cell. Biochem. 52: 140–147
Osborn M & Weber K (1977) Exp. Cell Res. 106: 339–349
Lenk R, Ransom L, Kaufmann Y & Penman S (1977) Cell 10: 67–78
Cervera M, Dreyfuss G & Penman S (1981) Cell 23: 113–120
van Venrooij WJ, Sillekens PTG, van Eekelen CAG & Reinders RT (1981) Exp. Cell Res. 135: 79–91
Toh B, Lolait S, Mathy J & Baum R (1980) Cell Tissue Res. 211: 163–169
Hesketh JE, Campbell G & Horne Z (1990) Cell Biol. Int. Rep. 15: 141–150
Zumbe A, Stahli C & Trachsel H (1982) Proc. Natl. Acad. Sci. (USA) 79: 2927–2931
Heuijerjans JH, Pieper FR, Ramaekers FCS, Timmermans LJM, Kuijpers H, Bloemendal H & van Venrooij WJ (1989) Exp. Cell Res. 181: 317–330
Gavrilova LP, Rutkevitch NM, Gelfand VI, Motuz LP, Stahl J, Bommer U-A & Bielka H (1987) Cell Biol. Int. Rep. 11: 745–753
Shestakova EA, Motuz LP, Minin AA & Gavrilova LP (1993) Cell Biol. Int. Rep. 17: 409–416
Singer RH, Langevin GL & Lawrence JB (1989) J. Cell Biol. 108: 2343–2353
Dang CV, Yang DCH & Pollard TD (1983) J. Cell Biol. 96: 1138–1147
Vedeler A, Pryme IF & Hesketh JE (1991) Mol. Cell. Biochem. 100: 2397–2403
Zambetti G, Schmidt W, Stein G & Stein J (1985) J. Cell Physiol. 125: 345–353
Zambetti G, Stein J & Stein G (1990) J. Cell Physiol. 144: 175–182
Hesketh JE, Campbell GP & Whitelaw PF (1991) Biochem. J. 274: 607–609
Adams A, Fey EG, Pike SF, Taylorson CJ, White HA & Rabin BR (1983) Biochem. J. 216: 215–226
Pondel MD & King ML (1988) Proc. Natl. Acad. Sci. (USA) 85: 7612–7616
Jeffery WR (1984) Dev. Biol. 103: 482–492
Taneja KL, Lifshitz LM, Fay FS & Singer RH (1992) J. Cell Biol. 119: 1245–1260
Wolosewick JJ & Porter KR (1979) J. Cell Biol. 82: 114–139
Heuser J & Kirschner MW (1980) J. Cell Biol. 86: 212–234
Ornelles DA, Fey EG & Penman S (1986) Mol. Cell. Biol. 6: 1650–1662
Ramaekers F, Benedetti E, Dunia I, Vorstenbosch P & Bloemendal H (1983) Biochim. Biophys. Acta 740: 441–448
Bird R & Sells B (1986) Biochim. Biophys. Acta 868: 215–225
Hesketh JE & Pryme IF (1988) FEBS Lett. 231: 62–66
Vedeler A, Pryme IF & Hesketh JE (1990) Cell. Biol. Int. Rep. 14: 211–218
Biegel D & Pachter JS (1992) J. Cell. Biochem. 48: 98–106
Schroder HC, Diehl-Seifert B, Rottmann M, Messer R, Bryson BA, Agutter PS & Muller WEG (1988) Arch. Biochem. Biophys. 261: 394–404
Hirokawa N, Takemura R & Hisanaga S-I (1985) J. Cell Biol. 101: 1858–1870
Suprenant KA (1993) Cell Motil. Cytoskel. 25: 1–9
Papasozomenos S Ch & Binder LI (1987) Cell Motil. Cytoskel. 8: 210–226
MacGregor HC & Stebbings H (1970) J. Cell Sci. 6: 431–449
Yisraeli JK, Sokol S & Melton DA (1990) Development 108: 289–298
Pokrywka NJ & Stephenson EC (1991) Development 113: 55–666
Raff GW, Whitfield WGF & Glover DM (1990) Development 110: 1249–1261
Grossi de Sa M-F, Martins de Sa C, Harper F, Olink-Coux M, Huesca M & Scherrer K (1988) J. Cell Biol. 107: 1517–1530
Katze MG, Lara J & Wambach M (1989) Virology 169: 312–322
Bagchi T, Larson DE & Sells BH (1987) Exp. Cell Res. 168: 160–172
Lequang H & Gauthier D (1989) Neurochem. Res. 14: 239–243
Hesketh JE, Campbell GP, Piechacyzk M & Blanchard J-M (1994) Biochem. J. 298: 143–148
Moon RT, Nicosia RF, Olsen C, Hille MB & Jeffery WR (1983) Dev. Biol. 95: 447–458
Hesketh JE, Campbell GP & Reeds PJ (1986) Biosci. Rpts 6: 797–804
Lenk R & Penman S (1979) Cell 16: 289–301
Kirkeide E-K, Pryme IF & Vedeler A (1992) Mol. Cell Biochem 118: 131–140
Horne Z & Hesketh JE (1990) Biochem. J. 268: 231–236
Horne Z & Hesketh JE (1990) Biochem. J. 272: 831–833
Meadus WJ, Pramanik S & Bag J (1990) Exp. Cell Res. 187: 25–32
Sundell CL & Singer RH (1990) J. Cell Biol. 111: 2397–2403
Hill MA & Gunning P (1993) J. Cell Biol. 122: 825–832
Aigner S & Pette D (1990) Histochemistry 95: 11–18
Hesketh JE, Campbell GP & Loveridge N (1991) Biochem. J. 279: 309–310
Russell BR & Dix D (1992) Amer. J. Physiol. 2662: C1–8
Steward O & Banker GA (1992) Trends Neurosci. 15: 180–186
Weeks DL & Melton D (1987) Cell 51: 861–867
Sundell CL & Singer RH (1991) Science 253: 1275–1277
MacDonald PM & Struhl G (1988) Nature 336: 595–598
Gottlieb E (1992) Proc. Natl. Acad. Sci. USA 89: 7164–71668
Davis I & Ish-Horowicz D (1991) Cell 67: 927–940
Kislauskis EH, Li Z, Taneja KL & Singer RH (1993) J. Cell Biol. 123: 165–172
Bag J & Pramanik S (1987) Biochem. Cell Biol. 65: 565–575
Howe JG & Hershey JWB (1984) Cell 37: 85–93
Savitz AJ & Meyer DI (1990) Nature 346: 540–544
Yang F, Domma M, Warren V, Dharmawardhane S & Condeelis J (1990) Nature 347: 494–496
Sharpless K, Biegel D, Yang T & Pachter JS (1993) Eur. J. Biochem. 212: 217–225
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Hesketh, J. Translation and the cytoskeleton: a mechanism for targeted protein synthesis. Mol Biol Rep 19, 233–243 (1994). https://doi.org/10.1007/BF00986965
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DOI: https://doi.org/10.1007/BF00986965