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Translation and the cytoskeleton: a mechanism for targeted protein synthesis

  • Special Issue: Protein Synthesis
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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

  1. Silver PA (1991) Cell 64: 489–497

    PubMed  Google Scholar 

  2. Blobel G & Dobberstein B (1975) J. Cell Biol. 67: 835–851

    PubMed  Google Scholar 

  3. Hesketh JE & Pryme IF (1991) Biochem. J. 277: 1–10

    PubMed  Google Scholar 

  4. Fulton AB (1993) J. Cell. Biochem. 52: 148–152

    PubMed  Google Scholar 

  5. Luby-Phelps K (1993) J. Cell. Biochem. 52: 140–147

    PubMed  Google Scholar 

  6. Osborn M & Weber K (1977) Exp. Cell Res. 106: 339–349

    PubMed  Google Scholar 

  7. Lenk R, Ransom L, Kaufmann Y & Penman S (1977) Cell 10: 67–78

    PubMed  Google Scholar 

  8. Cervera M, Dreyfuss G & Penman S (1981) Cell 23: 113–120

    PubMed  Google Scholar 

  9. van Venrooij WJ, Sillekens PTG, van Eekelen CAG & Reinders RT (1981) Exp. Cell Res. 135: 79–91

    PubMed  Google Scholar 

  10. Toh B, Lolait S, Mathy J & Baum R (1980) Cell Tissue Res. 211: 163–169

    PubMed  Google Scholar 

  11. Hesketh JE, Campbell G & Horne Z (1990) Cell Biol. Int. Rep. 15: 141–150

    Google Scholar 

  12. Zumbe A, Stahli C & Trachsel H (1982) Proc. Natl. Acad. Sci. (USA) 79: 2927–2931

    Google Scholar 

  13. Heuijerjans JH, Pieper FR, Ramaekers FCS, Timmermans LJM, Kuijpers H, Bloemendal H & van Venrooij WJ (1989) Exp. Cell Res. 181: 317–330

    PubMed  Google Scholar 

  14. Gavrilova LP, Rutkevitch NM, Gelfand VI, Motuz LP, Stahl J, Bommer U-A & Bielka H (1987) Cell Biol. Int. Rep. 11: 745–753

    PubMed  Google Scholar 

  15. Shestakova EA, Motuz LP, Minin AA & Gavrilova LP (1993) Cell Biol. Int. Rep. 17: 409–416

    Google Scholar 

  16. Singer RH, Langevin GL & Lawrence JB (1989) J. Cell Biol. 108: 2343–2353

    PubMed  Google Scholar 

  17. Dang CV, Yang DCH & Pollard TD (1983) J. Cell Biol. 96: 1138–1147

    PubMed  Google Scholar 

  18. Vedeler A, Pryme IF & Hesketh JE (1991) Mol. Cell. Biochem. 100: 2397–2403

    Google Scholar 

  19. Zambetti G, Schmidt W, Stein G & Stein J (1985) J. Cell Physiol. 125: 345–353

    PubMed  Google Scholar 

  20. Zambetti G, Stein J & Stein G (1990) J. Cell Physiol. 144: 175–182

    PubMed  Google Scholar 

  21. Hesketh JE, Campbell GP & Whitelaw PF (1991) Biochem. J. 274: 607–609

    PubMed  Google Scholar 

  22. Adams A, Fey EG, Pike SF, Taylorson CJ, White HA & Rabin BR (1983) Biochem. J. 216: 215–226

    PubMed  Google Scholar 

  23. Pondel MD & King ML (1988) Proc. Natl. Acad. Sci. (USA) 85: 7612–7616

    Google Scholar 

  24. Jeffery WR (1984) Dev. Biol. 103: 482–492

    PubMed  Google Scholar 

  25. Taneja KL, Lifshitz LM, Fay FS & Singer RH (1992) J. Cell Biol. 119: 1245–1260

    PubMed  Google Scholar 

  26. Wolosewick JJ & Porter KR (1979) J. Cell Biol. 82: 114–139

    PubMed  Google Scholar 

  27. Heuser J & Kirschner MW (1980) J. Cell Biol. 86: 212–234

    PubMed  Google Scholar 

  28. Ornelles DA, Fey EG & Penman S (1986) Mol. Cell. Biol. 6: 1650–1662

    PubMed  Google Scholar 

  29. Ramaekers F, Benedetti E, Dunia I, Vorstenbosch P & Bloemendal H (1983) Biochim. Biophys. Acta 740: 441–448

    PubMed  Google Scholar 

  30. Bird R & Sells B (1986) Biochim. Biophys. Acta 868: 215–225

    PubMed  Google Scholar 

  31. Hesketh JE & Pryme IF (1988) FEBS Lett. 231: 62–66

    PubMed  Google Scholar 

  32. Vedeler A, Pryme IF & Hesketh JE (1990) Cell. Biol. Int. Rep. 14: 211–218

    PubMed  Google Scholar 

  33. Biegel D & Pachter JS (1992) J. Cell. Biochem. 48: 98–106

    PubMed  Google Scholar 

  34. Schroder HC, Diehl-Seifert B, Rottmann M, Messer R, Bryson BA, Agutter PS & Muller WEG (1988) Arch. Biochem. Biophys. 261: 394–404

    PubMed  Google Scholar 

  35. Hirokawa N, Takemura R & Hisanaga S-I (1985) J. Cell Biol. 101: 1858–1870

    PubMed  Google Scholar 

  36. Suprenant KA (1993) Cell Motil. Cytoskel. 25: 1–9

    Google Scholar 

  37. Papasozomenos S Ch & Binder LI (1987) Cell Motil. Cytoskel. 8: 210–226

    Google Scholar 

  38. MacGregor HC & Stebbings H (1970) J. Cell Sci. 6: 431–449

    PubMed  Google Scholar 

  39. Yisraeli JK, Sokol S & Melton DA (1990) Development 108: 289–298

    PubMed  Google Scholar 

  40. Pokrywka NJ & Stephenson EC (1991) Development 113: 55–666

    PubMed  Google Scholar 

  41. Raff GW, Whitfield WGF & Glover DM (1990) Development 110: 1249–1261

    PubMed  Google Scholar 

  42. 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

    PubMed  Google Scholar 

  43. Katze MG, Lara J & Wambach M (1989) Virology 169: 312–322

    PubMed  Google Scholar 

  44. Bagchi T, Larson DE & Sells BH (1987) Exp. Cell Res. 168: 160–172

    PubMed  Google Scholar 

  45. Lequang H & Gauthier D (1989) Neurochem. Res. 14: 239–243

    PubMed  Google Scholar 

  46. Hesketh JE, Campbell GP, Piechacyzk M & Blanchard J-M (1994) Biochem. J. 298: 143–148

    PubMed  Google Scholar 

  47. Moon RT, Nicosia RF, Olsen C, Hille MB & Jeffery WR (1983) Dev. Biol. 95: 447–458

    PubMed  Google Scholar 

  48. Hesketh JE, Campbell GP & Reeds PJ (1986) Biosci. Rpts 6: 797–804

    Google Scholar 

  49. Lenk R & Penman S (1979) Cell 16: 289–301

    PubMed  Google Scholar 

  50. Kirkeide E-K, Pryme IF & Vedeler A (1992) Mol. Cell Biochem 118: 131–140

    PubMed  Google Scholar 

  51. Horne Z & Hesketh JE (1990) Biochem. J. 268: 231–236

    PubMed  Google Scholar 

  52. Horne Z & Hesketh JE (1990) Biochem. J. 272: 831–833

    PubMed  Google Scholar 

  53. Meadus WJ, Pramanik S & Bag J (1990) Exp. Cell Res. 187: 25–32

    PubMed  Google Scholar 

  54. Sundell CL & Singer RH (1990) J. Cell Biol. 111: 2397–2403

    PubMed  Google Scholar 

  55. Hill MA & Gunning P (1993) J. Cell Biol. 122: 825–832

    PubMed  Google Scholar 

  56. Aigner S & Pette D (1990) Histochemistry 95: 11–18

    PubMed  Google Scholar 

  57. Hesketh JE, Campbell GP & Loveridge N (1991) Biochem. J. 279: 309–310

    PubMed  Google Scholar 

  58. Russell BR & Dix D (1992) Amer. J. Physiol. 2662: C1–8

    Google Scholar 

  59. Steward O & Banker GA (1992) Trends Neurosci. 15: 180–186

    PubMed  Google Scholar 

  60. Weeks DL & Melton D (1987) Cell 51: 861–867

    PubMed  Google Scholar 

  61. Sundell CL & Singer RH (1991) Science 253: 1275–1277

    PubMed  Google Scholar 

  62. MacDonald PM & Struhl G (1988) Nature 336: 595–598

    PubMed  Google Scholar 

  63. Gottlieb E (1992) Proc. Natl. Acad. Sci. USA 89: 7164–71668

    PubMed  Google Scholar 

  64. Davis I & Ish-Horowicz D (1991) Cell 67: 927–940

    PubMed  Google Scholar 

  65. Kislauskis EH, Li Z, Taneja KL & Singer RH (1993) J. Cell Biol. 123: 165–172

    PubMed  Google Scholar 

  66. Bag J & Pramanik S (1987) Biochem. Cell Biol. 65: 565–575

    PubMed  Google Scholar 

  67. Howe JG & Hershey JWB (1984) Cell 37: 85–93

    PubMed  Google Scholar 

  68. Savitz AJ & Meyer DI (1990) Nature 346: 540–544

    PubMed  Google Scholar 

  69. Yang F, Domma M, Warren V, Dharmawardhane S & Condeelis J (1990) Nature 347: 494–496

    PubMed  Google Scholar 

  70. Sharpless K, Biegel D, Yang T & Pachter JS (1993) Eur. J. Biochem. 212: 217–225

    PubMed  Google Scholar 

Download references

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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

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