1887

Chapter 9 : Structure and Evolution of the 23S rRNA Binding Domain of Protein L2

Authors: Isao Tanaka1, Atsushi Nakagawa1, Takashi Nakashima1, Masae Taniguchi1, Harumi Hosaka1, Makoto Kimura2
VIEW AFFILIATIONS HIDE AFFILIATIONS
Affiliations: 1: Division of Biological Sciences, Graduate School of Science, Hokkaido University, Sapporo 060-0810, Japan; 2: Laboratory of Biochemistry, Faculty of Agriculture, Kyushu University, Fukuoka 812-8512, Japan
Content Type: Monograph
Publication Year: 2000

Category: Microbial Genetics and Molecular Biology

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555818142/9781555811846_Chap09-1.gif /docserver/preview/fulltext/10.1128/9781555818142/9781555811846_Chap09-2.gif

Abstract:

This chapter focuses on the crystal structure of the RNA binding domain of L2, and discusses its structure from functional and evolutionary points of view. Site-directed mutagenesis of Arg86 or Arg155 significantly diminished RNA binding affinity, and in addition, Arg68 and Lys70 mutations caused partial loss of RNA binding. To date, the three-dimensional structures of over a dozen ribosomal proteins have been determined. Comparison of their structures with those of other known proteins in the Protein Data Bank revealed that many ribosomal proteins share structural motifs, such as RNP, dsRNA binding domain, KH domain, and helix-turn-helix motifs, with RNA or DNA binding proteins. Recent studies of ribosomes, however, demonstrated that peptidyltransferase activity is never attributed solely to the 23S rRNA, and they reduce the number of possible essential macromolecular components of the peptidyltransferase center to 23S rRNA and ribosomal proteins L2 and L3.

Citation: Tanaka I, Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M. 2000. Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, p 85-92. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch9
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Structure and Evolution of the 23S rRNA Binding Domain of Protein L2
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818142.chap9-1,webId=/content/author/10.1128/9781555818142.chap9-1,properties={foaf_givenname=Isao, foaf_name=Isao Tanaka, foaf_surname=Tanaka, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818142.chap9-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818142.chap9-2,webId=/content/author/10.1128/9781555818142.chap9-2,properties={foaf_givenname=Atsushi, foaf_name=Atsushi Nakagawa, foaf_surname=Nakagawa, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818142.chap9-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818142.chap9-3,webId=/content/author/10.1128/9781555818142.chap9-3,properties={foaf_givenname=Takashi, foaf_name=Takashi Nakashima, foaf_surname=Nakashima, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818142.chap9-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818142.chap9-4,webId=/content/author/10.1128/9781555818142.chap9-4,properties={foaf_givenname=Masae, foaf_name=Masae Taniguchi, foaf_surname=Taniguchi, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818142.chap9-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818142.chap9-5,webId=/content/author/10.1128/9781555818142.chap9-5,properties={foaf_givenname=Harumi, foaf_name=Harumi Hosaka, foaf_surname=Hosaka, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818142.chap9-aff1]]}], com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781555818142.chap9-6,webId=/content/author/10.1128/9781555818142.chap9-6,properties={foaf_givenname=Makoto, foaf_name=Makoto Kimura, foaf_surname=Kimura, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781555818142.chap9-aff2]]}]]
Citation: Tanaka I, Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M. 2000. Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, p 85-92. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch9
/content/10.1128/9781555818142.chap9.fig9-1
Figure 1

Stereo view of L2-RBD. The molecule consists of two subdomains of approximately equal size. The N-terminal domain has an OB fold homologous to the S1 domain, and the C-terminal domain has an SH3-like-barrel motif. The fifth -strand and a 3 helix (H1) connect two subdomains.

10.1128/9781555818142/fig9-1_thmb.gif
10.1128/9781555818142/fig9-1.gif
Image of Figure 1
Figure 1

Stereo view of L2-RBD. The molecule consists of two subdomains of approximately equal size. The N-terminal domain has an OB fold homologous to the S1 domain, and the C-terminal domain has an SH3-like-barrel motif. The fifth -strand and a 3 helix (H1) connect two subdomains.

Citation: Tanaka I, Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M. 2000. Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, p 85-92. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555818142.chap9.fig9-2
Figure 2

Topological diagram showing secondary structure of L2-RBD. The molecule consists of 10 -strands (indicated by arrows) and a short 3 helix (indicated by a rectangle). Unlike in the ordinal OB fold, -strands 4 and 5 are linked by a crossover connection, leaving the fifth -strand at the interface between the N- and C-terminal domains. The C-terminal 10 makes a hydrogen bond to the 5, and thus all the -strands in the molecule are connected by hydrogen bonds.

10.1128/9781555818142/fig9-2_thmb.gif
10.1128/9781555818142/fig9-2.gif
Image of Figure 2
Figure 2

Topological diagram showing secondary structure of L2-RBD. The molecule consists of 10 -strands (indicated by arrows) and a short 3 helix (indicated by a rectangle). Unlike in the ordinal OB fold, -strands 4 and 5 are linked by a crossover connection, leaving the fifth -strand at the interface between the N- and C-terminal domains. The C-terminal 10 makes a hydrogen bond to the 5, and thus all the -strands in the molecule are connected by hydrogen bonds.

Citation: Tanaka I, Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M. 2000. Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, p 85-92. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555818142.chap9.fig9-3
Figure 3

Amino acid residues identified by mutagenesis experiments as essential for 23S rRNA binding. (Left) Positively charged residues important for 23S rRNA binding. Most of the residues that affect 23S rRNA binding are located in the Nterminal domain. The most important residues (Arg86 and Arg155) are located in the protruding loops of the N- and Cterminal domains, respectively. The side chains of these residues face the gate of the interface between two subdomains, a putative RNA binding site. (Right) Aromatic residues important for 23S rRNA binding. Phe66 and Tyr95 are at the interface between two subdomains, and Tyr102 is exposed to the molecular surface at the N-terminal extension of the molecule.

10.1128/9781555818142/fig9-3_thmb.gif
10.1128/9781555818142/fig9-3.gif
Image of Figure 3
Figure 3

Amino acid residues identified by mutagenesis experiments as essential for 23S rRNA binding. (Left) Positively charged residues important for 23S rRNA binding. Most of the residues that affect 23S rRNA binding are located in the Nterminal domain. The most important residues (Arg86 and Arg155) are located in the protruding loops of the N- and Cterminal domains, respectively. The side chains of these residues face the gate of the interface between two subdomains, a putative RNA binding site. (Right) Aromatic residues important for 23S rRNA binding. Phe66 and Tyr95 are at the interface between two subdomains, and Tyr102 is exposed to the molecular surface at the N-terminal extension of the molecule.

Citation: Tanaka I, Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M. 2000. Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, p 85-92. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555818142.chap9.fig9-4
Figure 4

Comparison of the fold of N- and C-terminal subdomains of L2-RBD with those of other proteins having similar motifs. (Left) The SH3-like-barrel domain of the biotin biosynthetic operon repressor, BirA, C-terminal domain (1BIA). (Middle) L2-RBD. The N-terminal half of L2-RBD is an OB fold, and the C-terminal half is an SH3-like barrel. The fifth strand (5) is at the linker region between the OB fold and the SH3-like barrel. (Right) The OB fold of the S1 domain of the polynucleotide phosphorylase of (1SRO).

10.1128/9781555818142/fig9-4_thmb.gif
10.1128/9781555818142/fig9-4.gif
Image of Figure 4
Figure 4

Comparison of the fold of N- and C-terminal subdomains of L2-RBD with those of other proteins having similar motifs. (Left) The SH3-like-barrel domain of the biotin biosynthetic operon repressor, BirA, C-terminal domain (1BIA). (Middle) L2-RBD. The N-terminal half of L2-RBD is an OB fold, and the C-terminal half is an SH3-like barrel. The fifth strand (5) is at the linker region between the OB fold and the SH3-like barrel. (Right) The OB fold of the S1 domain of the polynucleotide phosphorylase of (1SRO).

Citation: Tanaka I, Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M. 2000. Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, p 85-92. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781555818142.chap9.fig9-5
Figure 5

Comparison of molecules that have OB-fold and SH3-like-barrel domains. (Left) L2-RBD. (Right) Eukaryotic translation initiation factor IF-5A (2EIF). The N-terminal domain of IF-5A is an SH3-like barrel, and the C-terminal domain is an OB fold, the reverse of the situation in the L2-RBD. The molecules are drawn in rainbow colors to show the chain connectivity clearly.

10.1128/9781555818142/fig9-5_thmb.gif
10.1128/9781555818142/fig9-5.gif
Image of Figure 5
Figure 5

Comparison of molecules that have OB-fold and SH3-like-barrel domains. (Left) L2-RBD. (Right) Eukaryotic translation initiation factor IF-5A (2EIF). The N-terminal domain of IF-5A is an SH3-like barrel, and the C-terminal domain is an OB fold, the reverse of the situation in the L2-RBD. The molecules are drawn in rainbow colors to show the chain connectivity clearly.

Citation: Tanaka I, Nakagawa A, Nakashima T, Taniguchi M, Hosaka H, Kimura M. 2000. Structure and Evolution of the 23S rRNA Binding Domain of Protein L2, p 85-92. In Garett R, Douthwaite S, Liljas A, Matheson A, Moore P, Noller H (ed), The Ribosome. ASM Press, Washington, DC. doi: 10.1128/9781555818142.ch9
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555818142.chap9
1. Abola, E. E.,, J. L. Sussman,, J. Prilusky,, and N. O. Manning. 1997. Protein data bank archives of three-dimensional macromolecular structures. Methods Enzymol. 276: 556– 571.
2. Beauclerk, A. A.,, and E. Cundliffe. 1988. The binding site for ribosomal protein L2 within 23S ribosomal RNA for Escherichia coli. EMBO J. 7: 3589– 3594.
3. Bycroft, M.,, T. J. P. Hubbard,, M. Proctor,, S. M. Freund,, and A. G. Murzin. 1997. The solution structure of the S1 RNA binding domain: a member of an ancient nucleic acid-binding fold. Cell 88: 235– 242.
4. Capel, M. S.,, D. M. Engelman,, B. R. Freeborn,, M. Kjeldgaard,, J. A. Langer,, V. Ramakrishnan,, D. G. Schindler,, D. K. Schneider,, B. P. Schoenborn,, and I. Y. Sillers. 1987. A complete mapping of the proteins in the small ribosomal subunit of Escherichia coli. Science 238: 1403– 1406.
5. Cooperman, B. S.,, T. Wooten,, D. P. Romero,, and R. R. Traut. 1995. Histidine 229 in protein L2 is apparently essential for 50S peptidyl transferase activity. Biochem. Cell Biol. 73: 1087– 1094.
6. Draper, D. E.,, and L. P. Reynaldo. 1999. RNA binding strategies of ribosomal proteins. Nucleic Acids Res. 27: 381– 388.
7. Egebjerg, J.,, J. Christiansen,, and R. A. Garrett. 1991. Attachment sites of primary binding proteins L1, L2 and L23 on 23S ribosomal RNA of Escherichia coli. J. Mol. Biol. 222: 251– 264.
8. Golden, B. L.,, D. W. Hoffman,, V. Ramakrishnan,, and S. W. White. 1993. Ribosomal protein S17: characterization of the three-dimensional structure by 1H and 15N NMR. Biochemistry 32: 12812– 12820.
9. Harada, N.,, K. Maemura,, N. Yamasaki,, and M. Kimura. 1998. Identification by site-directed mutagenesis of amino acid residues in ribosomal protein L2 that are essential for binding to 23S ribosomal RNA. Biochim. Biophys. Acta 1429: 176– 186.
10. Holm, L.,, and C. Sander. 1993. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233: 123– 138.
11. Hosaka, H.,, A. Nakagawa,, I. Tanaka,, N. Harada,, K. Sano,, M. Kimura,, M. Yao,, and S. Wakatsuki. 1998. Ribosomal protein S7: a new RNA-binding motif with structural similarities to a DNA architectural factor. Structure 5: 1199– 1208.
12. Khaitovich, P.,, A. S. Mankin,, R. Green,, L. Lancaster,, and H. Noller. 1999. Characterization of functionally active subribosomal particles from Thermus aquaticus. Proc. Natl. Acad. Sci. USA 96: 85– 90.
13. Kim, K. K.,, L.-W. Hung,, H. Yokota,, R. Kim,, and S. H. Kim. 1998. Crystal structures of eukaryotic translation initiation factor 5A from Methanococcus jannaschii at 1.8 Å resolution. Proc. Natl. Acad. Sci. USA 95: 10419– 10424.
14. Kimura, M.,, M. Noda,, M. Nakashima,, and I. Tanaka. Unpublished data.
15. Lodi, P. J.,, J. A. Ernst,, J. Kuszewski,, A. B. Hickman,, A. Engelman,, R. Craigie,, G. M. Clore,, and A. M. Gronenborn. 1995. Solution structure of the DNA binding domain of HIV-1 integrase. Biochemistry 34: 9826– 9833.
16. Murzin, A. G. 1993. OB (oligonucleotide / oligosaccharide binding)- fold: common structural and functional solution for nonhomologous sequences. EMBO J. 12: 861– 867.
17. Murzin, A. G.,, S. E. Brenner,, T. Hubbard,, and C. Chothia. 1995. SCOP: a structural classification of proteins database for the investigation of sequences and structures. J. Mol. Biol. 247: 536– 540.
18. Nakagawa, A.,, T. Nakashima,, M. Taniguchi,, H. Hosaka,, M. Kimura,, and I. Tanaka. 1999. The three-dimensional structure of the RNA-binding domain of ribosomal protein L2: a protein at the peptidyl transferase center of the ribosome. EMBO J. 18: 1459– 1467.
19. Nakashima, T.,, M. Kimura,, A. Nakagawa,, and I. Tanaka. 1998. Crystallization and preliminary X-ray crystallographic study of a 23S rRNA binding domain of the ribosomal protein L2 from Bacillus stearothermophilus. J. Struct. Biol. 124: 99– 101.
20. Nakashima, T.,, I. Tanaka,, and M. Kimura. Unpublished data.
21. Narayana, N.,, D. A. Matthews,, E. E. Howell,, and X. Nguyenhuu. 1995. A plasmid-encoded dihydrofolate reductase from trimethoprim- resistant bacteria has a novel D2-symmetric active site. Nat. Struct. Biol. 2: 1018– 1025.
22. Noller, H. F.,, V. Hoffarth,, and L. Zimniak. 1992. Unusual resistance of peptidyl transferase to protein extraction procedures . Science 256: 1416– 1419.
23. Peat, T. S.,, J. Newman,, G. S. Waldo,, J. Berendzen,, and T. C. Terwilliger. 1998. Structure of translation initiation factor 5A from Pyrobaculum aerophilum at 1.75Å resolution. Structure 6: 1207– 1214.
24. Ramakrishnan, V.,, and W. S. White. 1998. Ribosomal protein structures: insights into the architecture, machinery and evolution of the ribosome. Trends Biochem. Sci. 23: 208– 212.
25. Schulze, H.,, and K. H. Nierhaus. 1982. Minimal set of ribosomal components for reconstitution of the peptidyl transferase activity. EMBO J. 1: 609– 613.
26. Subramanian, A. R. 1983. Structure and functions of ribosomal protein S1. Prog. Nucleic Acid Res. Mol. Biol. 28: 101– 142.
27. Tanaka, I.,, A. Nakagawa,, H. Hosaka,, S. Wakatsuki,, F. Mueller,, and R. Brimacombe. 1998. Matching the crystallographic structure of ribosomal protein S7 to a three-dimensional model of the 16S ribosomal RNA. RNA 4: 542– 550.
28. Watanabe, K.Unpublished results.
29. Watanabe, K.,, and M. Kimura. 1985. Location of the binding region for 23S ribosomal RNA on ribosomal protein L2 from Bacillus stearothermophilus. Eur. J. Biochem. 153: 299– 304.
30. Wilson, K. P.,, L. M. Shewchuk,, R. G. Brennan,, A. J. Otsuka,, and B. W. Matthews. 1992. Escherichia coli biotin holoenzyme synthetase / bio repressor crystal structure delineates the biotinand DNA-binding domains. Proc. Natl. Acad. Sci. USA 89: 9257– 9261.
31. Wimberly, B. T.,, S. W. White,, and V. Ramakrishnan. 1998. The structure of ribosomal protein S7 at 1.9 Å resolution reveals a ?-hairpin motif that binds double-stranded nucleic acids. Structure 5: 1187– 1198.
32. Wimberly, B. T.,, R. Guymon,, J. P. McCutcheon,, S. W. White,, and V. Ramakrishnan. 1999. A detailed view of a ribosomal active site: the structure of the L11-RNA complex. Cell 97: 491– 502.
33. Wittmann-Liebold, B.,, A. K. E. Kopke,, E. Arndt,, W. Kromer,, T. Hatakeyama,, and H.G. Wittmann,. 1990. Sequence comparison and evolution of ribosomal proteins and their genes , p. 598– 616. In W. E. Hill, , A. Dahlberg, , R. A. Garrett, P. B. Moore, D. Schlessinger, and J. R. Warner (ed.), The Ribosome: Structure, Function, and Evolution. American Society for Microbiology, Washington, D.C.
34. Wu, X.,, B. Knudsen,, S. M. Feller,, J. Zheng,, A. Sali,, D. Cowburn,, H. Hanafusa,, and J. Kuriyan. 1995. Structural basis for the specific interaction of lysine-containing proline-rich peptides with the N-terminal SH3 domain of c-Crk. Structure 3: 215– 226.

Back to top
This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error