Yeast phenylalanine transfer RNA: atomic coordinates and torsion angles. G.J.Quigley, N.C.Seeman, A.H.-J.Wang, F.L.Suddath* and Alexander Rich
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1 Volume number December Nucleic Acids Research Yeast henylalanine transfer RNA: atomic coordinates and torsion angles G.J.Quigley, N.C.Seeman, A.H.-J.Wang, F.L.Suddath* and Alexander Rich Deartment of Biology, Massachusetts Institute of Technology, Cambridge, MA, USA Received November ABSTRACT The atomic coordinates of yeast henylalanine transfer RNA (trna) as well as the torsion angles of the olynucleotide chain are resented as derived from an x-ray diffraction analysis of orthorhombic crystals. A comarison is made between the coordinates obtained from analysis of monoclinic crystals of the same material. It is concluded that the molecule has substantially the same form in the orthorhombic and the monoclinic lattices, excet for differences found between residues at the ' end of the olynucleotide chain. A number of observations are made concerning hydrogen bonding interactions which may account for many of the residues conserved in all trna sequences. INTRODUCTION Aroximately three years ago, the folding of the olynucleotide o chain of yeast henylalanine trna was described from a A x-ray diffraction analysis of orthorhombic crystals (). It was shown that the molecule was bent into an L-shae with the accetor and TdSC stems of the familiar trna cloverleaf forming one limb, while the D stem and the anticodon stem form the other limb. In this conformation, the ' accetor terminus is at one end of the L-shaed molecule A from the anticodon at the other end. Somewhat over a year ago, the tertiary interactions in this molecule were described in an analysis o at A resolution of the orthorhombic crystals (). At the same time, a similar A resolution analysis of the monoclinic crystal form was reorted in which most of the olynucleotide chain was traced with the excetion of the interactions between the T#C and D loos at the corner of the L-shaed molecule (). Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May,
2 -ray diffraction data from orthorhombic crystals have been obtained o o to. A resolution (). The. A data have been analyzed by two indeendent refinement methods to obtain reliminary atomic coordinates. The results of these analyses are resented here and in another aer (). These two indeendent refinements have roduced similar sets of atomic coordinates. Recently, atomic coordinates from the monoclinic crystal have been ublished (). The coordinates from these two crystal forms are comared here and it is shown that the structures are almost identical in the orthorhombic and monoclinic lattices with the excetion of the conformation near the ' end of the olynucleotide chain. RESULTS The atomic coordinates of yeast henylalanine trna are resented in Table. The general conformation of the molecule including the secondary and tertiary interactions has been described earlier (,,). Rough coordinates were measured in an otical comaritor and these coordinates were refined using a method similar to that described by Huber et al. (), couled with extensive idealization. At this stage o* o in the refinement, the R factor is. at A and. at. A. The ositions of most of the residues in the olynucleotide chain are well defined, with the excetion of residues,, and where the electron density is consistently weak and diffuse. Thus, it is ossible that these may change their conformation slightly uon further refinement. We do not anticiate substantial changes in the atomic ositions of the other residues. Most of the ribose residues in the molecule are in Table. Atomic Coordinates of Yeast henylalanine trna The Cartesian x, y, z coordinates, with distances in angstroms, corresond to the a, b_ and axes of the orthorhombic unit cell (J. The origin of the unit cell is taken as the origin of the coordinate system. These coordinates have been deosited in the rotein Data Bank at Brookhaven National Laboratories, Uton, Long Island, New York (). They can also be obtained uon request from the authors. The oxygen atoms attached to the hoshorus atom are labeled O and O, such that when the hoshate grou is viewed from the O' osition, the atoms O, O and O are organized in a clockwise arrangement. Methyl grous are designated as M, followed by the numbering of the atoms to which the methyl grous are attached. Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May,
3 Table ' ' ' C' ' C' C' ' N C N C C N C N ' ' ' C' ' C' C' ' C C N C N ' ' ' C' ' C' C' ' N C N C CS N C N A " ci- ' ". t..,,,...,,.,,,,,,,,,,,,,......,,,.,.,,,,,,,,,,,, ,,,,,,,,,.,,, ,,,,,,,.,,,,,,,,,...,,,..., t..,,,,,,,,,,,, C' " C' C' ' N C N C C N C N ' ' ' C' ' C' C' ' N C N C C N C N ' ' ' C' ' C' CS' ' C C C N ' ' ' C' ' C' C' ' B C C C N ' ci- ' ' C' ' C" C' ' C C C N ' ' ' C' ' C' C' OS' N C N C C N C N ' ' ' C' ' C' C' ' M N C N ,,,,.,,.....,..,.....,.,,,,, -,,,.,.,......,.,.....,,,,,,,.,,,,,,,., m-guansine ,.,,,, C C N C N ' ' ' C' ' C' C' ' C C N C N ' ' ' C' ' C' C' ' CA C C N ' ' ' C' ' C' C' ' C C N C N ' ' ',.,.,,,,,,..... IB ,.,,...,,,, ,, IS,,, IS ,,,.,,,,,,,.,,,,,,,,,, B,,,,,,,,.,,,,..,,,...., ,,,,,.&,,,,,,,,,,,,, B, >,. S at ennsylvania State University on May, Downloaded from htt://nar.oxfordjournals.org/
4 Table (continued) C' ' C' C- ' O N C N C C N C N IS ' " ' C' ' C' C' ' N C N C C N CB N ' ' ' C' ' C' C' ' C C C N ' ' ' C' ' C' C' '.... e.o..s , DIHYDRO DIHYDRO C C C N ' ' ' C' ' C' C' ' N C N C C N C N ' Cl ' ' ' C' ' C' C' ' N C N C C N C N ' ' ' C' ' C' C' ' N C O.B B N C C N C N ' Cl ' ' ' C' ' C' C' ' N C N C C N CO N ' ' - C' ' C' C' ' N C N C C N C N ' ' ' C' ' C' C" ' N C N C..... S C N C N ' ' ' C' ' C' CS' ' N C N C C N C N ' ' ' C' ' C- C' ' C C N C N ' ' ' C' ' C'. C' ' F" M M N C N C C N C,..... S..... IS (>m-guansine at ennsylvania State University on May, Downloaded from htt://nar.oxfordjournals.org/
5 Table (continued) N ' ' ' C' ' C' CS' OS' C CS N C N ' Cl ' ' ' C' ' C' CS' ' C CS N C N ' CJ ' ' ' C' ' C' C' ' N C N C C N C N ' ' ' C' ' Y S.... IB S S.S C" C' ' N C N C C N C N ' ' ' C' ' C' C' ' N C N C CS N C N ' ' ' M C' ' C' C- - C C N C N ' ' ' C' ' C" C' ' DI. Y. IS ,..., ,,.,,, URIDNE a , "m,, ,, C C C N M C' ' C' C' ' Ol N C N C C N C N - ' ' C' ' C' C' ' N C N C C N C N ' - ' C' ' C' C' ' N C... -" , ,,,.....,,, IS,.,, I ,, S m ,, i N C C N CB N ' ci- ' ' C' - C' C' ' N C C C C C C Cll N C N C C C N C N ' - ' C' ' C' C' ' N C N C C N C N ' ' '., Y.. Y NUCLEOSIDE S SEUDOURIOINE. at ennsylvania State University on May, Downloaded from htt://nar.oxfordjournals.org/
6 Table (continued) C' ' C' C' ' O O C N C C ' ' ' C' ' C' C' ' M C C N C N ' ' ' C' ' C' C' ' C C C N ' ' ' C' ' C' C' ' N. * *.....» * *.... IS *.. IS. Sm-..B.....a.. B IS C N C C N CB N ' ' ' C' ' C' C' OS' N C N C CS N C N ' ' ' C' ' C' C' ' N C N C C N CB N ' ' ' C' ' C' C' ' N C ,..V...,,..,,,,,.,..? i ,,,.,.,.,.,,..., S ,,.,,,,.,,,.,, ^ ,...,,,,, S ' S N C C N C N ' ' ' C' ' C' C' ' M N C N C C N C N ' ' ' C' ' C' CS' ' C C C N ' ' ' C' ' C' CS' ' C C N C N... H-GUANSINE..... IS,,,,,,...,.....,.,,,,,,,,,,,,, ,....,,,,.,,,,,, ,.....,..,., ' ' ' C' ' C- C' ' M C C N C N ' " ' C' ' C' C' ' C C C N ' ' ' C' ' C' C' ' N C N C C N C N ' ' ' C' ' IH "^~* - n *. « * ,.....» *.. *.. at ennsylvania State University on May, Downloaded from htt://nar.oxfordjournals.org/
7 Table C' CS' ' C C C N S ' ' ' C' ' C' C' ' N CA N C ' C N C N ' Cl" ' ' C' ' C' C' ' M C C C N ' ' L)' C' ' C' C' ' C.. (continued) Y..... ~ RIBOTHYMIDINE S. ^SEUDO N C C ' ' ' C' ' C' C' ' C C N C N ' ' ' C' ' C' C' ' N C N C C N CB N ' ' ' C' ' C' C' ' DI Ml N C N C C N C N. Y ,,,,., ,, -,,,,,...., ,.,,.,.,,,,, lm ,.,,,, ' ' ' C' ' C' C' ' C C C N ' ' ' C' ' C" C' ' C C N C N ' ' ' C' ' C' CE- OS' C C N C N ' ' ' C' ' C' C' ' Y * SO N C N C C N C N ' Cl ' ' ' C' ' C' C' ' C C N C N ' ' ' C' ' C' C' ' N C N C C N C N ' Cl ' ' ' C' ' C' C' ' DI N C N C.... Y..., : S..S..B... '... S. SO. at ennsylvania State University on May, Downloaded from htt://nar.oxfordjournals.org/
8 Table (continued) C N C. N ' ' ' C' ' C' C' ' N C N C C N C N - ' - C' ' C' C' ' N C N C C N C N ' ' ' C' ' C' C' '. S.. The base Y is numbered as follows: C C C N ' ' ' C' ' C' C' ' C C C N ' ' ' C' ' C' C' ' C CS N C N ' ' ' C' ' C' C". Y ,,......' J.... ' N C N C C N C N ' ' ' C- ' C' C' ' C C N C N ' ' ' C" ' C' C' ' N C N C C N CB N S S '. ' ' C' ' C' C' ' C C N C N ' ' ' C' ' C' C' ' C C N C N ' ' ' C' ' C' C' ' N C N C C N C N S &. O. O H n H n ii M C-O-C-C-N-C-O-CH ' I\ R= v Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May,
9 the standard '-endo conformation; however, several are found which adot the '-endo conformation:,,,,, and. All of the urines and yrimidines aear to be in the anti-conformation with the excetion of residue A. A is resented in the syn-conformation in Table although it is ossible to lace the residue in the anticonformation using the same electron density. Either conformation could form two hydrogen bonds to m G. Further refinement should clarify this ambiguity. The torsion angles in the olynucleotide chains are resented in Table, together with the angle which describes the conformation of the glycosyl linkage. The major torsional variations are in the two hoshoester linkages (,) as had been suggested reviously (). Table. Torsion Angles in the olyiyucleotide Chain LINK ALHA BETA GAMMA DELTA ESILON CHI LINK ALHA BETA GAMMA DELTA ESILON CHI S B ALHA BETA GAHMA DELTA LINK ALHA BETA GAMMA DELTA ESILON CHI ISO IS - Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May, The system defining the torsion angles of the internucleotide linkage is described elsewhere (). a refers to the torsion angle defined by C\ C, O', ; is defined by C\ O\, O ; is defined by O\, O\ C ; g is defined by, O, C', C'; is defined by O, C\ C, C'. The angle describes the torsion angle about the glycosyl linkage. The internucleotide linkage has the same number as the nucleotide on the O side of the hoshorus atom.
10 Recent ublication of the atomic coordinates for yeast henylalanine trna in the monoclinic crystal () has made it ossible to comare the conformation in these two crystal forms. In the initial descrition of the conformation in the monoclinic crystal, Robertus et al. () were unable to define the vital interactions between the D loo and the T\JlC loo at the corner of the molecule. Insection of the atomic coordinates in the monoclinic cell shows that they have confirm'ed the assignments which we made of the tertiary interactions in the orthorhombic unit cell somewhat over a year ago (). Their coordinates' indicate the interaction between and G as well as the stacking interactions of the other bases in the comlex intertwining of these two loos (, ). In addition, they aear to have reinterreted the conformation of the molecule in the segment lying between the accetor stem and the D stem. In their initial descrition, m G was described as artially intercalated between the bases A and G (). In their revised interretation (), they have adoted a geometry very similar to that which we described earlier, including aroriate modifications in the stacking interactions in this art of the molecule (, ). Thus the similarities in the conformation of the molecule in these two different crystal forms is greater than was initially aarent. A comarison of the conformation of yeast henylalanine trna in the two different crystal forms is shown in Figure. A rojection is shown in which lines connect the grou coordinates in the molecule as described in the figure legend. It can be seen that the conformation of the two molecules is quite similar with the excetion of the two terminal residues at the end of the accetor stem. Leaving out these two residues, the mean deviation in the ositions of the atomic coordinates is. A while the mean difference in the ositions of the grou coordinates is o. A. The residues for which there is a significant difference in conformation include D, U and the side chain of Y. Using an indeendent refinement analysis on the orthorhombic data, another set of coordinates has been obtained (). The grou coordinates of the two different refinement analyses of the orthorhombic crystal form have a mean deviation of. A. This comarison makes Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May,
11 TijkC Stem A Accetor Stem Variable Loo Anticodon Stem Anticodon Figure. Comarison of the conformation of yeast henylalanine trna in two crystal forms. The two molecules from the orthorhombic and monoclinic unit cells have been fitted by a least squares rocedure (). Three grou coordinates are lotted: the osition of the hoshorus atom, the centroid of the five atoms in the furanose ring of ribose, and the centroid of the six atoms which make u the six-membered ring in either yrimidines or urines. The solid line connecting the grou coordinates reresents the conformation of the molecule in the orthorhombic unit cell, while the dashed line shows its conformation in the monoclinic unit cell. In the schematic diagram at the right, secondary and tertiary hydrogen bonds between bases are shown with different shading (). The numbers refer to the residues in the olynucleotide chain. it very clear that the conformations of the molecule in the monoclinic and the orthorhombic unit cells are essentially indistinguishable at this resolution excet for the nucleotides at the end of the molecule. Several features of the hydrogen bonding interactions of yeast henylalanine trna have been described recently (). However, some additional observations can be made. It is interesting, for examle, that both the orthorhombic and monoclinic analyses aear to show a GU base air held together by two hydrogen bonds. osition is always a urine (). In the structure, there is a hydrogen bond between ribose O' and N of G, a bond which can be reserved even if osition is adenine. In the resent structure, G also has two other otential hydrogen bonds between the amino grou N and O' of Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May,
12 ribose and Ol of ribose. These may further stabilize the structure. osition is always $ while osition is always uracil in trnas involved in olyetide chain elongation (). There may be structural reasons for these constancies. Both of these residues occur in a osition where the olynucleotide chain turns a corner. As described reviously (), # has on to of the base while the N of # forms a hydrogen bond to the hoshate grou of. In a similar way, U is near the bend in the anticodon loo and it has on to of the base U, while N of U forms a hydrogen bond with hoshate. Thus the bases of both # and U stabilize the corner in analogous ways. The geometry suggests a ossible additional hydrogen bond from of # to hoshate, although the distance is too long at the resent stage of refinement. It is of interest that the anticodon loo is likely to be further stabilized by a hydrogen bond between N of A and O of. Since osition is always occuied by a yrimidine containing O and osition usually has an aroriately ositioned roton donor, it is ossible that this interaction is of a general nature. The resent coordinates show a hydrogen bonding distance between N of C and a hoshate oxygen of C. If this distance remains after further refinement, it may rovide an exlanation for the constant GC air found at the base of the T#C stem. Finally, there is limited sace around the constant yrimidine site C and this may revent insertion of a urine at this osition in those trnas involved in the elongation of olyetide chains. With these observations, we can now give structural reasons for almost all of the base conservation in trna sequences. ACKNOWLEDGMENTS Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May, This research was suorted by grants from the National Institutes of Health, the National Science Foundation, the National Aeronautics and Sace Administration and the American Cancer Society. N. C. S. is a fellow of the National Institutes of Health, and A. H. -J. W. is suorted by Grant CA from the National Cancer Institute. ^resent address: Det. of Biochemistry, Institute of Dental Research Univ. of Alabama Medical Center, Birmingham, Alabama
13 REFERENCES. Kim, S. H., Quigley, G. J., Suddath, F. L., Mcherson, A., Sneden, D., Kim, J. J., Weinzierl, J. and Rich, A. () Science, -.. Kim, S. H., Suddath, F. L., Quigley, G. J., Mcherson, A., Sussman, J. L., Wang, A. H. -J., Seeman, N. C. and Rich, A. () Science, -.. Robertus, J. D., Ladner, J. E., Finch, J. T., Rhodes, D., Brown, R. D., Clark, B. F. C. and Klug, A. () Nature, -.. Quigley, G. J., Wang, A. H. -J., Seeman, N. C, Suddath, F. L., Rich, A., Sussman, J. L. and Kim, S. H., roc. Nat. A cad. Sci., Wash, (in ress).. Sussman, J. L. and Kim, S. H., Biochem. Biohys. Res. Comm. (in ress).. Ladner, J. E., Jack, A., Robertus, J. D., Brown, R. S., Rhodes, D., Clark, B. F. C. and Klug, A. () Nucleic Acid Res., -.. Kim, S. H., Sussman, J. L., Suddath, F. L., Quigley, G. J., Mcherson, A., Wang, A. H. -J., Seeman, N. C. and Rich, A. () roc. Nat. Acad. Sci., -.. Huber, R., Kukla, D., Bode, W., Schwager,., Bartels, K., Diesenhofer, J. and Steigemann, W. () J. Mol. Biol., -.. Seeman, N. C., Sussman, J. L., Berman, H. M. and Kim, S. H. () Nature New Biol., -.. Nyburg, S. C. () Acta Cryst. B, -.. Koetzle, T. F. () Acta Cryst. B,.. Seeman, N. C, Rosenberg, J. M., Suddath, F. L., Kim, J. J. and Rich, A., J. Mol. Biol. (in ress). Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May,
14 Downloaded from htt://nar.oxfordjournals.org/ at ennsylvania State University on May,
Figs. 1 and 2 show views of the ac and bc planes of both the. axes are shown, and inspection of the figure suggests that the
Proc. Nat. Acad. Sci. USA Vol. 71, No. 5, pp. 2146-2150, May 1974 The Molecular Structure of Yeast Phenylalanine Transfer RNA in Monoclinic Crystals (molecular replacement method/x-ray diffraction/orthorhombic
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