Advertisement

Molecular Biology

, Volume 52, Issue 6, pp 799–811 | Cite as

Intersubunit Mobility of the Ribosome

  • A. V. Finkelstein
  • S. V. Razin
  • A. S. SpirinEmail author
REVIEWS
  • 43 Downloads

Abstract

Ribosomes are ribonucleoprotein nanoparticles synthesizing all proteins in living cells. The function of the ribosome is to translate the genetic information encoded in a nucleotide sequence of mRNA into the amino acid sequence of a protein. Each translation step (occurring after the codon-dependent binding of the aminoacyl-tRNA with the ribosome and mRNA) includes (i) the transpeptidation reaction and (ii) the translocation that unidirectionally drives the mRNA chain and mRNA-bound tRNA molecules through the ribosomal intersubunit space; the latter process is driven by the free energy of the chemical reaction of transpeptidation. Thus, the translating ribosome can be considered a conveying protein-synthesizing molecular machine. In this review we analyze the role of ribosomal intersubunit mobility in the process of translocation.

Keywords:

ribosome molecular machines translocation free energy transpeptidation rectification of Brownian motion 

Notes

REFERENCES

  1. 1.
    Spirin A.S. 2002. Ribosome as a molecular machine. FEBS Lett. 514, 2‒10.CrossRefGoogle Scholar
  2. 2.
    Spirin A.S. 2004. The ribosome as an RNA-based molecular machine. RNA Biol. 1, 3‒9.CrossRefGoogle Scholar
  3. 3.
    Spirin A.S. 2009. The ribosome as a conveying thermal ratchet machine. J. Biol. Chem. 284, 21103‒21119.CrossRefGoogle Scholar
  4. 4.
    Frank J., Gonzalez R.L., Jr. 2010. Structure and dynamics of a processive Brownian motor: The translating ribosome. Annu. Rev. Biochem. 79, 381‒412.CrossRefGoogle Scholar
  5. 5.
    Spirin A.S., Finkelstein A.V. 2011. The ribosome as a Brownian ratchet machine. In: Molecular Machines in Biology. Ed. Frank J. Cambridge: Cambridge Univ. Press, pp. 158‒190.Google Scholar
  6. 6.
    Schmeing T.M., Voorhees R.M., Kelley A.C., Gao Y.G., Murphy F.V. 4th, Weir J.R., Ramakrishnan V. 2009. The crystal structure of the ribosome bound to EF-Tu and aminoacyl-tRNA. Science. 326, 688‒694.CrossRefGoogle Scholar
  7. 7.
    Gao Y.G., Selmer M., Dunham C.M., Weixlbaumer A., Kelley A.C., Ramakrishnan V. 2009. The structure of the ribosome with elongation factor G trapped in the posttranslocational state. Science. 326, 694‒699.CrossRefGoogle Scholar
  8. 8.
    Voorhees R.M., Weixlbaumer A., Loakes D., Kelley A.C., Ramakrishnan V. 2009. Insights into substrate stabilization from snapshots of the peptidyl transferase center of the intact 70S ribosome. Nat. Struct. Mol. Biol. 16, 528‒533.CrossRefGoogle Scholar
  9. 9.
    Spirin A.S. 1999. Ribosomes. New York: Kluwer.CrossRefGoogle Scholar
  10. 10.
    Gavrilova L.P., Spirin A.S. 1974. “Nonenzymatic” translation. Meth. Enzymol. 30, 452‒462.CrossRefGoogle Scholar
  11. 11.
    Gavrilova L.P., Kostiashkina O.E., Koteliansky V.E., Rutkevitch N.M., Spirin A.S. 1976. Factor-free (“non-enzymic”) and factor-dependent systems of translation of polyuridylic acid by Escherichia coli ribosomes. J. Mol. Biol. 101, 537‒552.CrossRefGoogle Scholar
  12. 12.
    Pestka S. 1968. Studies on the formation of transfer ribonucleic acid–ribosome complexes: 3. The formation of peptide bonds by ribosomes in the absence of supernatant enzymes. J. Biol. Chem. 243, 2810–2820.Google Scholar
  13. 13.
    Pestka S. 1969. Studies on the formation of transfer ribonucleic acid-ribosome complexes: 4. Oligopeptide synthesis and translocation on ribosomes in the presence and absence of soluble transfer factors. J. Biol. Chem. 244, 1533–1539.Google Scholar
  14. 14.
    Gavrilova L.P., Smolyaninov V.V. 1971. Analysis of translocation mechanism in the ribosome: 1. Polyphenylalanine synthesis in E. coli ribosomes without the involvement of GTP and protein translation factors. Mol. Biol. (Moscow). 5, 883‒891.Google Scholar
  15. 15.
    Gavrilova L.P., Spirin A.S. 1971. Stimulation of “non-enzymic” translocation in ribosomes by p-chloromercuribenzoate. FEBS Lett. 17, 324–326.CrossRefGoogle Scholar
  16. 16.
    Lucas-Lenard J., Lipmann F. 1971. Protein biosynthesis. Annu. Rev. Biochem., 40, 409‒448.CrossRefGoogle Scholar
  17. 17.
    Gavrilova L.P., Spirin A.S. 1972. A modification of the 30S ribosomal subparticle is responsible for stimulation of “non-enzymatic” translocation by p-chloromercuribenzoate. FEBS Lett. 22, 91–92.CrossRefGoogle Scholar
  18. 18.
    Kaji A., Kaji H. 1963. Specific interaction of soluble RNA and polyribonucleic acid induced polysomes, Biochem. Biophys. Res. Commun. 13, 186–192.CrossRefGoogle Scholar
  19. 19.
    Nakamot T., Conway T.W., Allende J.E., Spyrides G.I., Lipmann F. 1963. Formation of peptide bonds: 1. Peptide formation from aminoacyl-sRNA. Cold Spring Harb. Symp. Quant. Biol. 28, 227–231.CrossRefGoogle Scholar
  20. 20.
    Gottesman M.E. 1967. Reaction of ribosome-bound peptidyl transfer ribonucleic acid with aminoacyl transfer ribonucleic acid or puromycin. J. Biol. Chem. 242, 5564–5571.Google Scholar
  21. 21.
    Spirin A.S. 1978. Energetics of the ribosome. In: Progress in Nucleic Acid Research and Molecular Biology, vol. 21. Ed. Cohn W.E. New York: Academic, pp. 39–62.Google Scholar
  22. 22.
    Belitsina N.V., Spirin A.S. 1979. Ribosomal translocation assayed by the matrix-bound poly(uridylic acid) column technique. Eur. J. Biochem. 94, 315–320.CrossRefGoogle Scholar
  23. 23.
    Gavrilova L.P., Perminova I.N., Spirin A.S. 1981. Elongation factor Tu can reduce translation errors in poly(U)-directed cell-free systems. J. Mol. Biol. 149, 69–78.CrossRefGoogle Scholar
  24. 24.
    Southworth D.R., Brunelle J.L, Green R. 2002. EFG-independent translocation of the mRNA:tRNA complex is promoted by modification of the ribosome with thiol-specific reagents. J. Mol. Biol. 324, 611–623.CrossRefGoogle Scholar
  25. 25.
    Kakhniashvili D.G., Spirin A.S. 1977. Temperature dependence of factor-free and factor-promoted translation systems. The absence of an effect of elongation factors and GTP on activation. Dokl. Akad. Nauk SSSR. 234, 958‒963.Google Scholar
  26. 26.
    Blanchard S.C., Kim H.D., Gonzalez R.L. Jr., Puglisi J.D., Chu S. 2004. tRNA dynamics on the ribosome during translation. Proc. Natl. Acad. Sci. U. S. A. 101, 12893‒12898.CrossRefGoogle Scholar
  27. 27.
    Kim H.D., Puglisi J.D., Chu S. 2007. Fluctuations of transfer RNAs between classical and hybrid states. Biophys. J. 93, 3575‒3582.CrossRefGoogle Scholar
  28. 28.
    Munro J.B., Altman R.B., O’Connor N., Blanchard S.C. 2007. Identification of two distinct hybrid state intermediates on the ribosome. Mol. Cell. 25, 505‒517.CrossRefGoogle Scholar
  29. 29.
    Cornish P.V., Ermolenko D.N., Noller H.F., Ha T. 2008. Spontaneous intersubunit rotation in single ribosomes. Mol. Cell. 30, 578‒588.CrossRefGoogle Scholar
  30. 30.
    Moazed D., Noller H.F. 1989. Intermediate states in the movement of transfer RNA in the ribosome. Nature. 342, 142‒148.CrossRefGoogle Scholar
  31. 31.
    Bretscher M.S. 1968. Translocation in protein synthesis: A hybrid structure model. Nature. 218, 675‒677.CrossRefGoogle Scholar
  32. 32.
    Moazed D., Noller H.F. 1986. Transfer RNA shields specific nucleotides in 16S ribosomal RNA from attack by chemical probes. Cell. 47, 985‒994.CrossRefGoogle Scholar
  33. 33.
    Moazed D., Noller H.F. 1989. Interaction of tRNA with 23S rRNA in the ribosomal A, P, and E sites. Cell. 57, 585‒597.CrossRefGoogle Scholar
  34. 34.
    Spirin A.S. 1968. On the mechanism of ribosome function. The hypothesis of locking-unlocking of subparticles. Dokl. Akad. Nauk SSSR. 179, 1467‒1470.Google Scholar
  35. 35.
    Spirin A.S. 1969. A model of the functioning ribosome: Locking and unlocking of the ribosome subparticles. Cold Spring Harb. Symp. Quant. Biol. 34, 197‒207CrossRefGoogle Scholar
  36. 36.
    Spirin A.S., Baranov V.I., Polubesov G.S., Serdyuk I.N., May R.P. 1987. Translocation makes the ribosome less compact. J. Mol. Biol. 194, 119‒126.CrossRefGoogle Scholar
  37. 37.
    Baranov V.I., Belitsina N.V., Spirin A.S. 1979. The use of columns with matrix-bound polyuridylic acid for isolation of translating ribosomes. Meth. Enzymol. 59, 382‒397.CrossRefGoogle Scholar
  38. 38.
    Aitken C.E., Puglisi J.D. 2010. Following the intersubunit conformation of the ribosome during translation in real time. Nat. Struct. Mol. Biol. 17, 793‒800.CrossRefGoogle Scholar
  39. 39.
    Berk V., Zhang W., Pai R.D., Cate J.H.D. 2006. Structural basis for mRNA and tRNA positioning on the ribosome. Proc. Natl. Acad. Sci. U. S. A. 103, 15830‒15834.CrossRefGoogle Scholar
  40. 40.
    Zhang W., Dunkle J.A., Cate J.H. 2009. Structures of the ribosome in intermediate states of ratcheting. Science. 325, 1014‒1017.CrossRefGoogle Scholar
  41. 41.
    Lodish H.F., Jacobsen M. 1972. Regulation of hemoglobin synthesis. Equal rates of translation and termination of α- and β-globin chains. J. Biol. Chem. 247, 3622‒3629.Google Scholar
  42. 42.
    Finkelstein A.V., Ptitsyn O.B. 2016. Protein Physics. A Course of Lectures, 2nd ed. New York: Academic, lectures 8, 24, 25.Google Scholar
  43. 43.
    Frenkel J. 1984. Kinetic Theory of Liquids. Glocester, MA: Peter Smith Publ., Inc.Google Scholar
  44. 44.
    Frank J., Agrawal R.K. 2000. A ratchet-like inter-subunit reorganization of the ribosome during translocation. Nature. 406, 318‒322.CrossRefGoogle Scholar
  45. 45.
    Korostelev A., Noller H.F. 2007. Analysis of structural dynamics in the ribosome by TLS crystallographic refinement. J. Mol. Biol. 373, 1058‒1070.CrossRefGoogle Scholar
  46. 46.
    Ermolenko D.N., Majumdar Z.K., Hickerson R.P., Spiegel P.C., Clegg R.M., Noller H.F. 2007. Observation of intersubunit movement of the ribosome in solution using FRET. J. Mol. Biol. 370, 530‒540.CrossRefGoogle Scholar
  47. 47.
    Ermolenko D.N., Spiegel P.C., Majumdar Z.K., Hickerson R.P., Clegg R.M., Noller H.F. 2007. The antibiotic viomycin traps the ribosome in an intermediate state of translocation. Nat. Struct. Mol. Biol. 14, 493‒497.CrossRefGoogle Scholar
  48. 48.
    Horan L.H., Noller H.F. 2007. Intersubunit movement is required for ribosomal translocation. Proc. Natl. Acad. Sci. U. S. A. 104, 4881‒4885.CrossRefGoogle Scholar
  49. 49.
    Valle M., Zavialov A.V., Sengupta J., Rawat U., Ehrenberg M., Frank J. 2003. Locking and unlocking of ribosomal motions. Cell. 114, 123‒134.CrossRefGoogle Scholar
  50. 50.
    Korostelev A., Trakhanov S., Laurberg M., Noller H.F. 2006. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell. 126, 1065‒1077.CrossRefGoogle Scholar
  51. 51.
    Selmer M., Dunham C.M., Murphy F.V. 4th, Weixlbaumer A., Petry S., Kelley A.C., Weir J.R., Ramakrishnan V. 2006. Structure of the 70S ribosome complexed with mRNA and tRNA. Science. 313, 1935‒1942.CrossRefGoogle Scholar
  52. 52.
    Fei J., Kosuri P., MacDougall D.D., Gonzalez R.L. Jr. 2008. Coupling of ribosomal L1 stalk and tRNA dynamics during translation elongation. Mol. Cell. 30, 348‒359.CrossRefGoogle Scholar
  53. 53.
    Cornish P.V., Ermolenko D.N., Staple D.W., Hoang L., Hickerson R.P., Noller H.F., Ha T. 2009. Following movement of the L1 stalk between three functional states in single ribosomes. Proc. Natl. Acad. Sci. U. S. A. 106, 2571‒2576.CrossRefGoogle Scholar
  54. 54.
    Fei J., Bronson J.E., Hofman J.M., Srinivas R.L., Wiggins C.H., Gonzalez R.L., Jr. 2009. Allosteric collaboration between elongation factor G and the ribosomal L1 stalk directs tRNA movements during translation. Proc. Natl. Acad. Sci. U. S. A. 106, 15702‒15707.CrossRefGoogle Scholar
  55. 55.
    Guajardo R., Sousa R. 1997. A model for the mechanism of polymerase translocation. J. Mol. Biol. 265, 8–19.CrossRefGoogle Scholar
  56. 56.
    Spirin A.S. 2002. RNA polymerase as a molecular machine. Mol. Biol. (Moscow). 36 (2), 153–159.CrossRefGoogle Scholar
  57. 57.
    Komissarova N., Kashlev M. 1997. RNA polymerase switches between inactivated and activated states by translocating back and forth along the DNA and the RNA. J. Biol. Chem. 272, 15329‒15338.CrossRefGoogle Scholar
  58. 58.
    Bar-Nahum G., Epshtein V., Ruckenstein A.E., Rafikov R., Mustaev A., Nudler E. 2005. A ratchet mechanism of transcription elongation and its control. Cell. 120, 183‒193.CrossRefGoogle Scholar
  59. 59.
    Bai L., Fulbright R.M., Wang M.D. 2007. Mechanochemical kinetics of transcription elongation. Phys. Rev. Lett. 98, 068103.CrossRefGoogle Scholar
  60. 60.
    Dangkulwanich M., Ishibashi T., Liu S., Kireeva M.L., Lubkowska L., Kashlev M., Bustamante C.J. 2013. Complete dissection of transcription elongation reveals slow translocation of RNA polymerase II in a linear ratchet mechanism. eLife. doi 10.7554/eLife.00971Google Scholar
  61. 61.
    Xie P. 2011. A nucleotide binding rectification Brownian ratchet model for translocation of Y-family DNA polymerases. Theor. Biol. Med. Model. 8, 22.CrossRefGoogle Scholar
  62. 62.
    Pyle A.M. 2008. Translocation and unwinding mechanisms of RNA and DNA helicases. Annu. Rev. Biophys. 37, 317‒336.CrossRefGoogle Scholar
  63. 63.
    Levin M.K., Gurjar M., Patel S.S. 2005. A Brownian motor mechanism of translocation and strand separation by hepatitis C virus helicase. Nat. Struct. Mol. Biol. 12, 429‒435.CrossRefGoogle Scholar
  64. 64.
    Rasnik I., Jeong Y.J., McKinney S.A., Rajagopal V., Patel S.S., Ha T. 2008. Branch migration enzyme as a Brownian ratchet. EMBO J. 27, 1727‒1735.CrossRefGoogle Scholar
  65. 65.
    Li G., Cui Q. 2004. Analysis of functional motions in Brownian molecular machines with an efficient block normal mode approach: Myosin-II and Ca2+-ATPase. Biophys. J. 86, 743‒763.CrossRefGoogle Scholar
  66. 66.
    Takano M., Terada T.P., Sasai M. 2010. Unidirectional Brownian motion observed in an insilico single molecule experiment of an actomyosin motor. Proc. Natl. Acad. Sci. U. S. A. 107, 7769‒7774.CrossRefGoogle Scholar
  67. 67.
    Fujii T., Namba K. 2017. Structure of actomyosin rigour complex at 5.2  Å resolution and insights into the ATPase cycle mechanism. Nat. Commun. 8, 13969.CrossRefGoogle Scholar
  68. 68.
    Marshall W.F. 2002. Order and disorder in the nucleus. Curr. Biol. 12, 185‒192.CrossRefGoogle Scholar
  69. 69.
    Levi V., Ruan Q., Plutz M., Belmont A.S., Gratton E. 2005. Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys. J. 89, 4275‒4285.CrossRefGoogle Scholar
  70. 70.
    Razin S.V., Gavrilov A.A., Ioudinkova E.S., Iarovaia O.V. 2013. Communication of genome regulatory elements in a folded chromosome. FEBS Lett. 587, 1840–1847.CrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Inc. 2018

Authors and Affiliations

  • A. V. Finkelstein
    • 1
    • 2
  • S. V. Razin
    • 2
    • 3
  • A. S. Spirin
    • 1
    • 2
    Email author
  1. 1.Institute of Protein Research, Russian Academy of SciencesPushchinoRussia
  2. 2.Biological Faculty, Moscow State UniversityMoscowRussia
  3. 3.Institute of Gene Biology, Russian Academy of SciencesMoscowRussia

Personalised recommendations