Skip to main content
SpringerLink
Log in

Conformational Preferences of Modified Nucleoside N2-methylguanosine (m2G) and Its Derivative N2, N2-dimethylguanosine (m 22 G) Occur at 26th Position (Hinge Region) in tRNA

  • Original Paper
  • Published:
Cell Biochemistry and Biophysics Aims and scope Submit manuscript

Abstract

Conformational preferences of the modified nucleosides N2-methylguanosine (m2G) and N2, N2-dimethylguanosine (m 22 G) have been studied theoretically by using quantum chemical perturbative configuration interaction with localized orbitals (PCILO) method. Automated complete geometry optimization using semiempirical quantum chemical RM1, along with ab initio molecular orbital Hartree–Fock (HF-SCF), and density functional theory (DFT) calculations has also been made to compare the salient features. Single-point energy calculation studies have been made on various models of m2G26:C/A/U44 and m 22 G26:C/A/U44. The glycosyl torsion angle prefers “syn” (χ = 286°) conformation for m2G and m 22 G molecules. These conformations are stabilized by N(3)–HC2′ and N(3)–HC3′ by replacing weak interaction between O5′–HC(8). The N2-methyl substituent of (m2G26) prefers “proximal” or s-trans conformation. It may also prefer “distal” or s-cis conformation that allows base pairing with A/U44 instead of C at the hinge region. Thus, N2-methyl group of m2G may have energetically two stable s-trans m2G:C/A/U or s-cis m2G:A/U rotamers. This could be because of free rotations around C–N bond. Similarly, N2, N2-dimethyl substituent of (m 22 G) prefers “distal” conformation that may allow base pairing with A/U instead of C at 44th position. Such orientations of m2G and m 22 G could play an important role in base-stacking interactions at the hinge region of tRNA during protein biosynthesis process.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16

Similar content being viewed by others

References

  1. Dunn, D. B. (1959). Additional components in ribonucleic acid of rat-liver fractions. Biochimica et Biophysica Acta, 34, 286–288.

    Article  PubMed  CAS  Google Scholar 

  2. Smith, J. D., & Dunn, D. B. (1959). The occurrence of methylated guanines in ribonucleic acids from several sources. The Biochemical Journal, 72, 294–301.

    PubMed  CAS  Google Scholar 

  3. Adamiak, R. W., & Gornicki, P. (1985). Hypermodified nucleosides of tRNA: Synthesis, chemistry, and structural features of biological interest. Progress in Nucleic Acid Research and Molecular Biology, 32, 27–74.

    Article  PubMed  CAS  Google Scholar 

  4. Motorin, Y., Bec, G., Tewari, R., & Grosjean, H. (1997). Transfer RNA recognition by the Escherichia coli delta2-isopentenyl-pyrophosphate: tRNA delta2-isopentenyl transferase: Dependence on the anticodon arm structure. RNA, 3, 721–733.

    PubMed  CAS  Google Scholar 

  5. Morin, A., Auxilien, S., Senger, B., Tewari, R., & Grosjean, H. (1998). Structural requirements for enzymatic formation of threonylcarbamoyladenosine (t6A) in tRNA: An in vivo study with Xenopus laevis oocytes. RNA, 4, 24–37.

    PubMed  CAS  Google Scholar 

  6. Limbach, P. A., Crain, P. F., & McClowskey, J. A. (1994). Summary: The modified nucleosides of RNA. Nucleic Acids Research, 22, 2183–2196.

    Article  PubMed  CAS  Google Scholar 

  7. Persson, B. C. (1993). Modification of tRNA as a regulatory device. Molecular Microbiology, 8, 1011–1016.

    Article  PubMed  CAS  Google Scholar 

  8. Agris, P. F. (1996). The importance of being modified: Roles of modified nucleosides and Mg2+ in RNA structure and function. Progress in Nucleic Acid Research and Molecular Biology, 53, 79–129.

    Article  PubMed  CAS  Google Scholar 

  9. Agris, P. F., Vendeix, F. A. P., & Graham, W. D. (2007). tRNA’s wobble decoding of the genome: 40 years of modification. Journal of Molecular Biology, 366, 1–13.

    Article  PubMed  CAS  Google Scholar 

  10. Bjork, G. R., & Hagervall, T. G. (2005). Transfer RNA modification, in Escherichia coli and Salmonella. In R. Curtiss III, A. Bock, J. L. Ingrahan, J. B. Kaper, S. Maloy, & F. C. Neidhardt (Eds.), Cellular and molecular biology. Washington, DC: ASM.

    Google Scholar 

  11. Giege, R. (2006). The early history of tRNA recognition by aminoacyl-tRNA synthetases. Journal of Biosciences, 31, 477–488.

    Article  PubMed  CAS  Google Scholar 

  12. Steinberg, S., & Cedergren, R. (1995). A correlation between N2-dimethylguanosine presence and alternate tRNA conformers. RNA, 1, 886–891.

    PubMed  CAS  Google Scholar 

  13. Noon, K. R., Guymon, R., Crain, P. F., McCloskey, J. A., Thomm, M., Lim, J., et al. (2003). Influence of temperature on tRNA modification in archaea: Methanococcoides burtonii (optimum growth temperature [T opt], 23°C) and Stetteria hydrogenophila (T opt, 95°C). Journal of Bacteriology, 185, 5483–5490.

    Article  PubMed  CAS  Google Scholar 

  14. Grosjean, H., Sprinzl, M., & Steinberg, S. (1995). Posttranscriptionally modified nucleosides in transfer RNA: Their locations and frequencies. Biochimie, 77, 139–141.

    Article  PubMed  CAS  Google Scholar 

  15. Sprinzl, M., & Vassilenko, K. S. (2005). Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Research, 33, 139–140.

    Article  Google Scholar 

  16. Johnson, G. D., Pirtle, I. L., & Pirtle, R. M. (1985). The nucleotide sequence of tyrosine tRNAQ*ΨA from bovine liver. Archives of Biochemistry and Biophysics, 236, 448–453.

    Article  PubMed  CAS  Google Scholar 

  17. Auffinger, P., & Westhof, E. (1998). In H. Grosjean & R. Benne (Eds.), Editing modification of RNA (pp. 569–576). Washington, DC: ASM.

    Google Scholar 

  18. Kowalak, J. A., Dalluge, J. J., McCloskey, J. A., & Stetter, K. O. (1994). The role of posttranscriptional modification in stabilization of transfer RNA from hyperthermophiles. Biochemistry, 33, 7869–7876.

    Article  PubMed  CAS  Google Scholar 

  19. Sprinzl, M., Horn, C., Brown, M., Ioudovitch, A., & Steinberg, S. (1998). Compilation of tRNA sequences and sequences of tRNA genes. Nucleic Acids Research, 26, 148–153.

    Article  PubMed  CAS  Google Scholar 

  20. Maden, B. E. H. (1990). The numerous modified nucleotides in eukaryotic ribosomal RNA. Progress in Nucleic Acid Research and Molecular Biology, 39, 241–303.

    Article  PubMed  CAS  Google Scholar 

  21. Rozenski, J., Crain, P. F., & McCloskey, J. A. (1999). The RNA modification database. Nucleic Acids Research, 27, 196–197.

    Article  PubMed  CAS  Google Scholar 

  22. Davis, D. R. (1998). Biophysical and conformational properties of modified nucleosides in RNA (nuclear magnetic resonance studies). In H. Grosjean & R. Benne (Eds.), Modification and editing of RNA (pp. 85–102). Washington, DC: ASM.

    Google Scholar 

  23. Sussman, J. L., Holbrook, S. R., Warrant, R. W., Church, G. M., & Kim, S. H. (1978). Crystal structure of yeast phenylalanine transfer RNA 1. Crystallographic refinement. Journal of Molecular Biology, 123, 607–630.

    Article  PubMed  CAS  Google Scholar 

  24. Edqvist, J., Straby, K. B., & Grosjean, H. (1995). Enzymatic formation of N2, N2 dimethylguanosine in eukaryotic tRNA: Importance of the tRNA architecture. Biochimie, 77, 54–61.

    Article  PubMed  CAS  Google Scholar 

  25. Edqvist, J., Blomqvist, K., & Straby, K. B. (1994). Structural elements in yeast tRNAs required for homologous modification of guanosine-26 into dimethylguanosine-26 by the yeast Trm1 tRNA-modifying enzyme. Biochemistry, 33, 9546–9551.

    Article  PubMed  CAS  Google Scholar 

  26. Boyle, J., Robillard, G. T., & Kim, S. H. (1980). Sequential folding of transfer RNA: A nuclear magnetic resonance study of successively longer tRNA fragments with a common 5′ end. Journal of Molecular Biology, 139, 601–625.

    Article  PubMed  CAS  Google Scholar 

  27. Ginell, S. L., & Parthasarathy, R. (1978). Conformation of N2-methylguanosine, a modified nucleoside of tRNA. Biochemical and Biophysical Research Communications, 84, 886–894.

    Article  PubMed  CAS  Google Scholar 

  28. Rife, J. P., Cheng, C. S., Moore, P. B., & Strobel, S. A. (1998). N2-methylguanosine is iso-energetic with guanosine in RNA duplexes and GNRA tetraloops. Nucleic Acids Research, 26, 3640–3644.

    Article  PubMed  CAS  Google Scholar 

  29. Kumbhar, N. M., & Sonawane, K. D. (2011). Iso-energetic multiple conformations of hypermodified nucleic acid base Wybutine (yW) which occur at 37th position in anticodon loop of tRNAPhe. Journal of Molecular Graphics and Modelling, 29, 935–946.

    Article  PubMed  CAS  Google Scholar 

  30. Nandel, F. S., & Saini, A. (2011). Peptoids with aliphatic side chains as helical structures without hydrogen bonds and collagen/inverse-collagen type structures. Journal of Biophysical Chemistry, 2, 37–48.

    Article  CAS  Google Scholar 

  31. Sonawane, K. D., & Tewari, R. (2008). Conformational preferences of hypermodified nucleoside lysidine (k2C) occurring at “wobble” position in anticodon loop of tRNAIle. Nucleosides, Nucleotides and Nucleic Acids, 27, 1158–1174.

    Article  CAS  Google Scholar 

  32. Sonawane, K. D., Sonavane, U. B., & Tewari, R. (2002). Conformational preferences of anticodon 3′-adjacent hypermodified nucleic acid base cis- or trans-zeatin and its 2-methylthio derivative, cis- or trans-ms2zeatin. Journal of Biomolecular Structure and Dynamics, 19, 637–648.

    PubMed  CAS  Google Scholar 

  33. Sonavane, U. B., Sonawane, K. D., & Tewari, R. (2002). Conformational preferences of the base substituent in hypermodified nucleotide queuosine 5′-monophosphate ‘pQ’ and protonated variant ‘pQH+’. Journal of Biomolecular Structure and Dynamics, 20, 473–485.

    PubMed  CAS  Google Scholar 

  34. Tewari, R. (1987). Theoretical studies on conformational preference of modified nucleic acid base N6-(N-threonylcarbonyl) adenine. Indian Journal of Biochemistry and Biophysics, 24, 170–176.

    CAS  Google Scholar 

  35. Tewari, R. (1990). Conformational preferences of modified nucleic acid bases N6-methyl-N6-(N-threonylcarbonyl) adenine and 2-methylthion-N6-(N-threonylcarbonyl) adenine by quantum chemical PCILO calculations. Journal of Biomolecular Structure and Dynamics, 8, 675–686.

    PubMed  CAS  Google Scholar 

  36. Sonavane, U. B., Sonawane, K. D., Morin, A., Grosjean, H., & Tewari, R. (1999). N (7) protonation induced conformational flipping in hypermodified nucleic acid bases N6 (N-threonylcarbonyl) adenine and its 2-methylthio- or N(6)-methyl-derivatives. International Journal of Quantum Chemistry, 75, 223–229.

    Article  CAS  Google Scholar 

  37. Tewari, R. (1995). N(7)-protonation-induced conformational flipping in hypermodified nucleic acid base N6-(N-glycylcarbonyl) adenine. Chemical Physics Letters, 238, 365–370.

    Article  Google Scholar 

  38. Tewari, R. (1988). Conformational preferences of modified nucleic acid bases N 6-(Δ2-isopentenyl) adenine and 2-methylthio-N 6-(Δ2-isopentenyl) adenine by the quantum chemical PCILO calculations. International Journal of Quantum Chemistry, 34, 133–142.

    Article  CAS  Google Scholar 

  39. Tewari, R. (1992). Conformational preferences of 6-furfuryl amino purine and 6-benzyl amino purine. International Journal of Quantum Chemistry, 41, 709–718.

    Article  CAS  Google Scholar 

  40. Sonawane, K. D., Sonavane, U. B., & Tewari, R. (2000). Conformational flipping of the N(6) substituent in diprotonated N6-(N-glycylcarbonyl)adenines: The role of N(6)H in purine-ring-protonated ureido adenines. International Journal of Quantum Chemistry, 78, 398–405.

    Article  CAS  Google Scholar 

  41. Tewari, R. (1997). Influence of N(1) protonation on the orientation of the N(6) substituent in hypermodified nucleic acid base N6-(N-glycylcarbonyl) adenine. International Journal of Quantum Chemistry, 62, 551–556.

    Article  CAS  Google Scholar 

  42. Tewari, R. (1994). Protonation-induced conformational flipping in hypermodified nucleic acid base N6-(N-glycylcarbonyl) adenine. International Journal of Quantum Chemistry, 51, 105–112.

    Article  CAS  Google Scholar 

  43. Holbrook, S. R., Sussman, J. L., Warrant, R. W., & Kim, S. H. (1978). Crystal structure of yeast phenylalanine transfer RNA: II. Structural features and functional implications. Journal of Molecular Biology, 123, 631–660.

    Article  PubMed  CAS  Google Scholar 

  44. Diner, S., Malrieu, J. P., & Claverie, P. (1969). Localized bond orbitals and the correlation problem. Theoretical Chemistry Accounts, 13, 1–17.

    CAS  Google Scholar 

  45. Diner, S., Malrieu, J. P., Jordan, F., & Gilbert, M. (1969). Localized bond orbitals and the correlation problem III. Energy up to third order in the zero differential overlap approximation. Application to σ electron systems. Theoretical Chemistry Accounts, 15, 100–110.

    CAS  Google Scholar 

  46. Masson, A., Levy, B., & Malrieu, J. P. (1970). Formaldehyde calculation of energy in the ground state by a perturbation method. Theoretical Chemistry Accounts, 18, 193–207.

    CAS  Google Scholar 

  47. Pullman, B., & Pullman, A. (1974). Molecular orbital calculations on the conformation of amino acid residues of proteins. Advances in Protein Chemistry, 16, 347–526.

    Article  Google Scholar 

  48. Pullman, B., & Saran, A. (1976). Quantum-mechanical studies on the conformation of nucleic acids and their constituents. Progress in Nucleic Acid Research and Molecular Biology, 18, 215–326.

    Article  PubMed  CAS  Google Scholar 

  49. Tewari, R. (1987). Theoretical studies on conformational preferences of modified nucleic acid base N6-(N-glycylcarbonyl) adenine. International Journal of Quantum Chemistry, 31, 611–624.

    Article  CAS  Google Scholar 

  50. Stewart, J. J. P. (1991). Optimization of parameters for semiempirical methods. III Extension of PM3 to Be, Mg, Zn, Ga, Ge, As, Se, Cd, In, Sn, Sb, Te, Hg, Tl, Pb, and Bi. Journal of Computational Chemistry, 12, 320–341.

    Article  CAS  Google Scholar 

  51. Rocha, G. B., Freire, R. O., Simas, A. M., & Stewart, J. P. (2006). RM1: A reparameterization of AM1 for H, C, N, O, P, S, F, Cl, Br, and I. Journal of Computational Chemistry, 27, 1101–1111.

    Article  PubMed  CAS  Google Scholar 

  52. Becke, A. D. (1992). Density-functional thermochemistry. III. The role of exact exchange. The Journal of Chemical Physics, 98, 5648–5652.

    Article  Google Scholar 

  53. Francl, M. M., Pietro, W. J., & Hehre, W. J. (1982). Self-consistent molecular orbital methods. XXIII. A polarization-type basis set for second-row elements. The Journal of Chemical Physics, 77, 3654–3665.

    Article  CAS  Google Scholar 

  54. Hehre, W. J., Radom, L., Schleyer, P. V. R., & Pople, J. A. (1986). In ab initio molecular orbital theory. New York: Wiley.

    Google Scholar 

  55. Shi, H., & Moore, P. B. (2000). The crystal structure of yeast phenylalanine tRNA at 1.93 A resolution: A classic structure revisited. RNA, 6, 1091–1105.

    Article  PubMed  CAS  Google Scholar 

  56. Pallan, P. S., Kreutz, C., & Bosio, S. (2008). Effects of N2, N2-dimethylguanosine on RNA structure and stability: Crystal structure of an RNA duplex with tandem m 22 G: A pairs. RNA, 14, 2125–2135.

    Article  PubMed  CAS  Google Scholar 

  57. Parmeggiani, A., Krab, I. M., Watanabe, T., Nielsen, R. C., Dahlberg, C., Nyborg, J., et al. (2006). Enacyloxin IIa pinpoints a binding pocket of elongation factor Tu for development of novel antibiotics. Journal of Biological Chemistry, 281, 2893–2900.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, Shivaji University, Kolhapur, 416 004, M.S, India

    Rohit S. Bavi, Asmita D. Kamble, Bajarang V. Kumbhar & Kailas D. Sonawane

  2. Department of Biotechnology, Shivaji University, Kolhapur, 416 004, M.S, India

    Navanath M. Kumbhar

  3. Department of Microbiology, Shivaji University, Kolhapur, 416 004, M.S, India

    Kailas D. Sonawane

Authors
  1. Rohit S. Bavi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Asmita D. Kamble
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Navanath M. Kumbhar
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Bajarang V. Kumbhar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kailas D. Sonawane
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kailas D. Sonawane.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 84 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bavi, R.S., Kamble, A.D., Kumbhar, N.M. et al. Conformational Preferences of Modified Nucleoside N2-methylguanosine (m2G) and Its Derivative N2, N2-dimethylguanosine (m 22 G) Occur at 26th Position (Hinge Region) in tRNA. Cell Biochem Biophys 61, 507–521 (2011). https://doi.org/10.1007/s12013-011-9233-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12013-011-9233-1

Keywords

Search

Navigation