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J. Biol. Chem., Vol. 277, Issue 19, 16391-16395, May 10, 2002
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From the
Received for publication, January 9, 2002, and in revised form, February 11, 2002
Transfer RNA molecules translate the genetic code
by recognizing cognate mRNA codons during protein synthesis. The
anticodon wobble at position 34 and the nucleotide immediately 3' to
the anticodon triplet at position 37 display a large diversity of modified nucleosides in the tRNAs of all organisms. We show that tRNA
species translating 2-fold degenerate codons require a modified U34 to enable recognition of their cognate codons
ending in A or G but restrict reading of noncognate or near-cognate
codons ending in U and C that specify a different amino acid. In
particular, the nucleoside modifications 2-thiouridine at position 34 (s2U34), 5-methylaminomethyluridine at position
34 (mnm5U34), and 6-threonylcarbamoyladenosine
at position 37 (t6A37) were essential for
Watson-Crick (AAA) and wobble (AAG) cognate codon recognition by
tRNA tRNA molecules play a significant role in the translation of the
genetic code into protein sequences. The ribosome-mediated interaction
of the mRNA codons with the anticodon of the tRNA results in the
discrimination of cognate versus near-cognate and noncognate codons (1, 2). Cytoplasmic tRNA molecules contain ~80
posttranscriptional nucleoside modifications (3) with the largest
diversity of these modifications located in the anticodon wobble at
position 34 or immediately 3' adjacent to the anticodon triplet at
position 37. Some of these nucleoside modifications appear to be
necessary for efficient protein synthesis as determinants for
aminoacylation (4, 5), which is important in maintaining reading frame
(6) and necessary for codon recognition on the ribosome (7-9). We had
previously reported that modified nucleosides in the anticodon loop of
tRNA Crick's wobble hypothesis for codon recognition (10) has been revised
(11-14) to include the influence of modified nucleosides. The wobble
rules proposed by Crick are that U recognizes A and G, C recognizes G,
A recognizes U, and G recognizes U and C. Lim and colleagues (11, 12)
and Yokoyama and colleagues (13, 14) proposed that unmodified
U34 could recognize U and C in addition to A and G. The
modifications of U34 would restrict wobble recognition to A
and G, but 5-oxyuridine modifications at position 34 such as
5-methoxyuridine (mo5U34) and
5-carboxymethoxyuridine (cmo5U34) would allow
recognition of U as well as A and G (12). However, we had previously
shown that the unmodified U34 in completely unmodified
tRNA To identify tRNA species that require a modified U34 for
codon recognition and restrict wobble specificity of the first
anticodon position, we assayed the ability of specific tRNAs to
recognize cognate and wobble codons in the absence of their naturally
occurring modifications at U34. The 17 nucleotides of the
anticodon stem and loop domain (ASL; Fig. 1) were used as a
mimic of the entire tRNA molecule to assess codon recognition at the
ribosomal A and P sites (7, 8, 15-17). The 30 S ribosomal P site has
the highest affinity of all ribosomal sites for entire tRNA molecules and for ASLs. Thus, the P site is first occupied in vitro
(18, 19), and binding to the A and P sites does not depend on the presence of initiation or elongation factors (16, 17). Here we provide
experimental evidence that the need for a modified wobble position,
U34, directly correlates to the need for some tRNAs to
discriminate at the third position of the codon. We also show that
modified nucleosides in tRNA anticodon domain modulate codon
recognition in the ribosomal A site similarly to the ribosomal P site.
RNA Synthesis--
Unmodified and variously modified ASLs and
30-mer mRNAs were purchased from Dharmacon (Lafayette, CO) and
Xeragon (Huntsville, AL) or synthesized using ribonucleoside
phosphoramidite chemistries and methods as described previously (7,
8).
Ribosomal P Site Filter Binding Assay--
ASLs were
3'-32P end-labeled as described previously (20). Small
ribosomal subunits (30 S) were prepared from Escherichia coli MRE600 cells (21) and activated by incubating at 37 °C for
30 min in CMN buffer (80 mM potassium cacodylate
acid, pH 7.5, 20 mM MgCl2, 100 mM
NH4Cl). Ribosomal subunits were 70-95% active in all
assays. ASLs were bound to the 30 S ribosomal P site as reported
previously (7, 8, 15) with the exception that mixtures of ASL, 30 S
subunit, and mRNA were incubated on ice for 1 h before being
passed through nitrocellulose membranes. Binding curves were analyzed
by one site nonlinear regression (GraphPad Prism) with yeast
tRNAPhe (Sigma) binding to poly(U) as the positive control.
Ribosomal A Site Filter Binding Assay--
ASLs were bound to 30 S ribosomal subunits with a procedure modified from that previously
reported for determining only programmed P site binding (7, 8, 15).
Small 30 S ribosomal subunits (10 pmol) and a 30-mer message consisting
of 10 consecutive copies of the appropriate triplet codon either in the
absence of tetracycline or in the presence of 250 µM
tetracycline (Sigma) were incubated with 200 pmol 3'-32P
end-labeled ASL in 40 µl of CMN buffer plus 3 mM
Chemical Protection of 16 S rRNA Nucleotides--
E.
coli 30 S ribosomal subunits (10 pmol) were programmed with an
appropriate message in CMN buffer either in the absence of tetracycline
or in the presence of 250 µM tetracycline in the absence
of tRNA or in the presence of 200 pmol of ASL. The mixtures (40 µl) were incubated on ice for 1 h before chemical probing. Chemical modification of 16 S rRNA nucleosides was conducted by adding
2 µl of one-third dimethyl sulfate (Sigma) solution in 100%
ethanol as described previously (7, 8). The dimethyl sulfate-modified
16 S rRNA was reverse-transcribed with a 5'-32P end-labeled
DNA primer complimentary to bases 1509-1530 to probe A1492 and A1493
and bases 824-845 to probe A794 and C795 in 16 S rRNA as described
previously (7, 8). The reverse transcription products were
electrophoresed by 6% PAGE/7 M urea.
Codon Recognition in the Ribosomal P Site--
Unmodified ASLs
corresponding to the sequences of LysUUU,
GluUUC, GlnUUG, ArgUCU,
AlaUGC, SerUGA, ValUAC, and
ProUGG tRNAs were chemically synthesized and assayed for
their ability to bind to 30 S ribosomal subunits programmed with the
respective cognate codons. The naturally occurring modifications in the
anticodon domains of each of these tRNA species are listed in Table
I. The unmodified
LysUUU, GluUUC, GlnUUG,
ArgUCU, and AlaUGC ASLs did not recognize their
cognate codons in the ribosomal P site (Table I). However, the
unmodified SerUGA, ValUAC, and
ProUGG ASLs recognized their cognate codons
(Kd = 600 ± 270 nM, 300 ± 100 nM, and 180 ± 60 nM, respectively)
(Table I). The inability of an ASL to recognize its cognate codon on
the ribosome was not a result of using only the isolated anticodon
domain as a tRNA mimic. The completely unmodified transcripts of human
tRNA Codon Recognition in the Ribosomal A Site--
To determine
whether modified nucleosides have a contribution in the ribosomal A
site, we assessed the ability of modifications previously shown to
restore programmed ribosomal P site binding (7, 8) to restore
programmed A site binding. The binding affinity of the ribosomal A site
is ~100 times lower than that for the P site (18). Thus, to achieve A
site binding to the 30 S subunit in vitro as described here,
it is necessary to saturate the P site. An additional tRNA exit site on
the ribosome, the E site, has also been identified for deacylated tRNAs
(22), but the majority of the binding energy for this site appears to be in the 3'-terminal adenosine base of the entire tRNA molecule and
the 50 S ribosomal subunit (23).
The binding of various modified
ASL Chemical Protection of 16 S rRNA Nucleotides--
To confirm that
we were observing A site binding in the absence of tetracycline but not
in the presence of tetracycline, we monitored the altered chemical
reactivity of 16 S rRNA bases A1492, A1493, A794, and C795 in the
presence of the variously modified ASL The work reported here provides experimental evidence for the role
of tRNA modified nucleosides in maintaining accurate recognition of the
genetic code. Many tRNAs can recognize more than one codon because of
the ability of the anticodon wobble at position 34 to wobble to
recognize the third position of the codon. These data indicate
that modification of U34 is the biochemical mechanism by
which tRNA molecules accurately differentiate codons from multiple amino acid codon boxes. Multiple amino acid or mixed codon boxes refer
to 2- and 3-fold degenerate codons that specify more than one amino
acid by only a difference in the third base (Table
III). We have found that the tRNAs
that have a U34 and translate codons from mixed codon boxes
rely on the U34 modification to enable recognition of A or
G in the third position of the codon.
tRNA If a modified U34 is necessary for tRNAs that translate
codons from mixed codon boxes to recognize A and G, the modification may also restrict the recognition to A and G. Previously, we reported that the incorporation of the s2U34
modification into the otherwise completely unmodified
ASL The cmo5U34 modification is present only in
tRNAs that read 4-fold degenerate codons. There is no requirement for
these tRNAs to discriminate at the third position of the codon, and we
have found that these tRNAs do not require a modified U34
for cognate codon recognition. For example, unmodified
ASL tRNA Although contributions of anticodon tRNA-modified nucleosides have been
established (6-8, 13), we had not previously compared the ability of
the anticodon stem and loop constructs to recognize their cognate
codons at the ribosomal P and A sites. The ribosomal position that
first discriminates cognate from near-cognate and noncognate tRNAs
during protein elongation is the ribosomal A site. Previous work has
reported contributions of modified nucleosides in the ribosomal A site
but not with the site-specific modified ASL constructs. It has been
proposed that a hypomodified tRNA may decrease the rate by which
the tRNA is recruited to the A site (6), that a position 37 modification enhances proofreading in the ribosomal A site (29), and
that position 37 modifications influence the in vivo
aminacylated tRNA selection in a tRNA-dependent manner (9).
We determined that modified nucleosides have a contribution in the
ribosomal A site similar to our previous observations of codon binding
in the ribosomal P site. The modifications previously shown to restore
programmed ribosomal P site binding (7, 8) restored the programmed A
site binding.
The x-ray crystallographic structures of the 30 S ribosomal subunit (1)
demonstrate that in forming the codon/anticodon duplex in the ribosomal
A site, ribosomal nucleotides A1492 and A1493 flip out of the internal
loop of ribosomal helix 44. In addition, the ribosomal nucleotide G530
switches from the syn-conformation to
anti-conformation. In these new conformations, A1492 and
A1493 interact with the first and second base pair in the minor groove of the codon/anticodon helix, and G530 interacts with the second position of the anticodon and the third position of the codon (1).
Thus, the ribosome discriminates cognate from near-cognate and
noncognate tRNA at two positions of the anticodon/codon duplex corresponding to the first and second positions of the codon base pairing with the third and second positions of the anticodon. The
wobble position of tRNA (position 34) appears to be more suited to
accommodate other geometries (1). Because the unmodified base sequences
of some tRNA molecules do not bind their cognate codons in the
ribosomal A site, we postulate that A1492 and A1493 are unable to
interact with the minor groove of the codon/anticodon helix, and
therefore, these tRNAs do not remain on the ribosome.
Studies on the human tRNA The modified nucleosides in the anticodon loop of some tRNAs modulate
codon recognition in the ribosomal A and P sites. We have shown that
the need for a modified U34 directly correlates to the need
for the tRNA to discriminate at the third position of the codon. Lim
and Curran (12) have suggested that the requirement for modifications
at position 34 may have arisen from evolutionary pressure to prevent
errors in codon recognition (12). Primitive codes may have specified
fewer amino acids, and the mixed codon boxes may have originally
specified single amino acids. Restricting wobble at tRNA position 34 would have functionally split some of the codon boxes, allowing the
incorporation of more amino acids into protein sequences (12). We have
also found some ASL sequences that have an unmodified G or C at
position 34, and a modification at position 37 also appear to require
modified nucleosides (data not shown). Position 37 modifications may be
involved in preventing frame-shifting (13) and probably have
arisen from an evolutionary pressure to maintain correct translation of
the genetic code. Modified nucleosides in the anticodon domain of tRNAs
appear to be a means of expanding the complexity of mRNA molecules
that interact with this region of the tRNA. The diversity of modified nucleosides at positions 34 and 37 may create an anticodon triplet unique enough to be specifically identified by the cognate
aminoacyl-tRNA synthetase while maintaining an anticodon loop structure
that allows a ribosome-mediated anticodon/codon discrimination during protein synthesis.
We acknowledge Winnell Newman (North Carolina
State University Nucleic Acids Facility) for expertise in RNA synthesis
and Dr. Paul Wollenzien, his laboratory, and Dr. Stanislov Kirillov for assistance in ribosomal binding assays. We thank Drs. James Curran,
James Brown, and Venki Ramakrishnan for editorial comments.
*
This research was supported by National Science Foundation
Grant MCB9986011 and National Institutes of Health Grant GM23037 (to
P. F. A.) and the Polish Committee for Scientific Research Grant
7T09A01721 (to A. J. M.).The costs of publication of this article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
§
Present address: Dept. of Biochemistry and Molecular
Biophysics, Washington University St. Louis, Box 8231, 660 S. Euclid Ave., St. Louis, MO 63110.
Published, JBC Papers in Press, February 22, 2002, DOI 10.1074/jbc.M200253200
The abbreviations used are:
mnm5U34, 5-methylaminomethyluridine at
position 34;
s2U34, 2-thiouridine at position
34;
t6A37, 6-threonylcarbamoyladenosine at
position 37;
mo5U34, 5-methoxyuridine;
cmo5U34, 5-carboxymethoxyuridine;
P, peptidyl;
ASL, anticodon stem and loop.
Accurate Translation of the Genetic Code Depends on tRNA Modified
Nucleosides*
§,
,
,
Department of Biochemistry, North Carolina
State University, Raleigh, North Carolina 27695-7622 and the
¶ Institute of Organic Chemistry, Technical University, 90-924 Lodz, Poland
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ABSTRACT
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES

![]()
INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES





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EXPERIMENTAL PROCEDURES
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
-mercaptoethanol. Reaction mixtures were incubated on ice for 1 h before being passed through nitrocellulose filters as described
previously (7, 8). The total number of ASLs bound to 30 S ribosomal
subunits was determined in the experiments without tetracycline. The
number of ASLs sensitive to tetracycline was determined by subtracting the number of ASLs bound in the presence of tetracycline from the total
number bound in the absence of tetracycline. The standard deviations
for A site binding were determined by taking the square root of the sum
of the squares of the standard deviations for the values in the absence
of tetracycline and the presence of tetracycline. All values are
averages and standard deviations of at least duplicate experiments.
![]()
RESULTS
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES






Sequences, naturally occurring modified nucleosides, and relative
ribosomal P site binding constants for ASL constructs




Ribosomal A and P-site relative binding efficiencies of unmodified and
variously modified ASL

View larger version (18K):
[in a new window]
Fig. 1.
Secondary structure of unmodified and
variously modified ASL 












View larger version (79K):
[in a new window]
Fig. 2.
Protection of 16 S rRNA bases from chemical
modification. The 30 S ribosomal subunits programmed with poly(A)
were incubated with no tRNA (lanes 1 and 2),
ASL 


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DISCUSSION
TOP
ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES









The genetic code
















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ACKNOWLEDGEMENTS
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FOOTNOTES
To whom correspondence should be addressed: Dept. of Molecular
and Structural Biochemistry, North Carolina State University, 128 Polk
Hall, Box 7622, Raleigh, NC 27695-7622. Tel.: 919-515-6188; Fax:
919-515-2047; E-mail: paul_agris@ncsu.edu.
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ABBREVIATIONS
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REFERENCES
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ABSTRACT
INTRODUCTION
EXPERIMENTAL PROCEDURES
RESULTS
DISCUSSION
REFERENCES
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P. F. Agris Decoding the genome: a modified view Nucleic Acids Res., January 9, 2004; 32(1): 223 - 238. [Abstract] [Full Text] [PDF] |
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A. L. KONEVEGA, N. G. SOBOLEVA, V. I. MAKHNO, Y. P. SEMENKOV, W. WINTERMEYER, M. V. RODNINA, and V. I. KATUNIN Purine bases at position 37 of tRNA stabilize codon-anticodon interaction in the ribosomal A site by stacking and Mg2+-dependent interactions RNA, January 1, 2004; 10(1): 90 - 101. [Abstract] [Full Text] [PDF] |
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H. R. Kalhor and S. Clarke Novel Methyltransferase for Modified Uridine Residues at the Wobble Position of tRNA Mol. Cell. Biol., December 15, 2003; 23(24): 9283 - 9292. [Abstract] [Full Text] |