A Counterintuitive Mg2+-dependent and Modification-assisted Functional Folding of Mitochondrial tRNAs

Journal of Molecular Biology

Volumn 362, Issue 4, 2006, Pages 771-786

  Jones, Christopher I ^a   Spencer, Angela C ^b   Hsu, Jennifer L ^c   Spremulli, Linda L ^b   Martinis, Susan A ^c   DeRider, Michele ^a   Agris, Paul F ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b University of North Carolina at Chapel Hill   (United States)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

aminoacylation; mitochondrial RNA folding; tRNALeu; tRNAMet

Indexed keywords

DIHYDROURIDINE; MAGNESIUM ION; MITOCHONDRIAL RNA; TRANSFER RNA; UNCLASSIFIED DRUG; URIDINE DERIVATIVE; MAGNESIUM; RNA; RNA, MITOCHONDRIAL;

AMINOACYLATION; ARTICLE; CIRCULAR DICHROISM; DNA MODIFICATION; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEIN TERTIARY STRUCTURE; RNA ANALYSIS; TRANSCRIPTION REGULATION; ULTRAVIOLET RADIATION; ANIMAL; CATTLE; CHEMISTRY; CONFORMATION; DNA DENATURATION; DRUG EFFECT; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; RNA STABILITY; TEMPERATURE; YEAST;

BOS TAURUS; ESCHERICHIA COLI;

AMINOACYLATION; ANIMALS; BASE SEQUENCE; CATTLE; CIRCULAR DICHROISM; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; MAGNESIUM; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; NUCLEIC ACID DENATURATION; RNA; RNA STABILITY; RNA, TRANSFER; TEMPERATURE; YEASTS;

EID: 33748313069     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.07.036     Document Type: Article

References (77)

1. Wittenhagen L.M., and Kelley S.O. Impact of disease-related mitochondrial mutations on tRNA structure and function. Trends Biochem. Sci. 28 (2003) 605-611
2. Asn gene associated with a lethal disease. Biochem. Biophys. Res. Commun. 329 (2005) 1152-1154
3. 2+ in RNA structure and function. In: Cohn W., and Moldave K. (Eds). Progress in Nucleic Acid Research and Molecular Biology vol. 53 (1996) 79
4. 2+-dependent tRNA folding. Nucl. Acids Res. 30 (2001) 4751-4760
5. Sprinzl M., and Vassilenko K.S. Compilation of tRNA sequences and sequences of tRNA genes. Nucl. Acids Res. 33 (2005) D139-D140
6. Barrell B.G., Seidman J.G., Guthrie C., and McClain W.H. Transfer RNA biosynthesis: the nucleotide sequence of a precursor to serine and proline transfer RNAs. Proc. Natl Acad. Sci. USA 71 (1974) 413-416
7. Helm M., Brule H., Degoul F., Cepanec C., Leroux J.P., Giege R., and Florentz C. The presence of modified nucleotides is required for cloverleaf folding of a human mitochondrial tRNA. Nucl. Acids Res. 26 (1998) 1636-1643
8. Lys. Biochemistry 38 (1999) 13338-13346
9. Rainaldi G., Volpicella M., Licciulli F., Liuni S., Gallerani R., and Ceci L.R. PLMItRNA, a database on the heterogeneous genetic origin of mitochondrial tRNA genes and tRNAs in photosynthetic eukaryotes. Nucl. Acids Res. 31 (2003) 436-438
10. Onoa B., and Tinoco Jr. I. RNA folding and unfolding. Curr. Opin. Struct. Biol. 14 (2004) 374-379
11. Thirumalai D., Lee N., Woodson S.A., and Klimov D.K. Early events in RNA Folding. Annu. Rev. Phys. Chem. 52 (2001) 751-762
12. Misra V.K., and Draper D.E. The linkage between magnesium binding and RNA folding. J. Mol. Biol. 317 (2002) 507-521
13. Shi H., and Moore P.B. The crystal structure of yeast phenylalanine tRNA at 1.93 A resolution: a classic structure revisited. RNA 6 (2000) 1091-1105
14. 2+ induced tRNA folding. Biochemistry 40 (2001) 6688-6698
15. Sakurai M., Ohtsuki T., and Watanabe K. Modification at position 9 with 1-methyladenosine is crucial for structure and function of nematode mitochondrial tRNAs lacking the entire T-arm. Nucl. Acids Res. 33 (2005) 1653-1661
16. Moriya J., Yokogawa T., Wakita K., Ueda T., Nishikawa K., Crain P.F., et al. A novel modified nucleoside found at the first position of the anticodon of methionine tRNA from bovine liver mitochondria. Biochemistry 33 (1994) 2234-2239
17. Leu aminoacylation and amino acid editing using minimalist RNA molecules. Nucl. Acids Res. 30 (2002) 2103-2113
18. Wittenhagen L.M., and Kelley S.O. Dimerization of a pathogenic human mitochondrial tRNA. Nature Struct. Biol. 9 (2002) 586-590
19. Phe. Nucl. Acids Res. 20 (1992) 4055-4059
20. 2+ transients that modulate secretion. Nature Cell Biol. 2 (2000) 57-61
21. Clark C.L., Cecil P.K., Singh D., and Gray D.M. CD, absorption and thermodynamic analysis of repeating dinucleotide DNA, RNA and hybrid duplexes [d/r(AC)]12·[d/r(GT/U)]12 and the influence of phosphorothioate substitution. Nucl. Acids Res. 25 (1997) 4098-4106
22. 2+ and 2′OH. Biospectroscopy 2 (1996) 205-217
23. Sosnick T.R., Fang X., and Shelton V.M. Application of circular dichroism to study RNA folding transitions. Methods Enzymol. 317 (2000) 393-409
24. Yarian C.S., Cain R., Basti M.M., Ansari G., Guenther R.H., Sochacka E., et al. Structural and functional roles of the N1- and N3-protons of Ψ at tRNA's position 39. Nucl. Acids Res. 27 (1999) 3543-3549
25. Agris P.F. Decoding the genome, a modified view. Nucl. Acids Res. 32 (2004) 223-238
26. Phe TΨC domain. Biochemistry 38 (1999) 8647-8656
27. 54-tRNA methyltransferases. Nucl. Acids Res. 28 (2000) 1374-1380
28. Gale A.J., Shi J.P., and Schimmel P. Evidence that specificity of microhelix charging by a class I tRNA synthetase occurs in the transition state of catalysis. Biochemistry 35 (1996) 608-615
29. Sugiura I., Nureki O., Ugaji-Yoshikawa Y., Kuwabara S., Shimada A., Tateno M., et al. The 2.0 A crystal structure of Thermus thermophilus methionyl-tRNA synthetase reveals two RNA-binding modules. Structure 8 (2000) 197-208
30. Senger B., and Fasiolo F. Yeast tRNA(Met) recognition by methionyl-tRNA synthetase requires determinants from the primary, secondary and tertiary structure: a review. Biochimie 78 (1996) 597-604
31. Spencer A.C., Heck A., Takeuchi N., Watanabe K., and Spremulli L.L. Characterization of the human mitochondrial methionyl-tRNA synthetase. Biochemistry 43 (2004) 9743-9754
32. Hsu J.L., Rho S.B., Vannella K.M., and Martinis S.A. Functional divergence of a unique C-terminal domain of leucyl-tRNA synthetase to accommodate its splicing and aminoacylation roles. J. Biol. Chem. 281 (2006) 23075-23082
33. Helm M., Brule H., Friede D., Giege R., Putz D., and Florentz C. Search for characteristic structural features of mammalian mito-tRNAs. RNA 6 (2000) 1356-1379
34. Phe with monovalent and divalent cations. Biochemistry 40 (2001) 3629-3638
35. Heilman-Miller S.L., Thirumalai D., and Woodson S.A. Role of counterion condensation in folding of the Tetrahymena ribozyme. I. Equilibrium stabilization by cations. J. Mol. Biol. 306 (2001) 1157-1166
36. Pyle A.M. Metal ions in the structure and function of RNA. J. Biol. Inorg. Chem. 7 (2002) 679-690
37. Russell R., Millett I.S., Doniach S., and Hershlag D. Small angle X-ray scattering reveals a compact intermediate in RNA folding. Nature Struct. Biol. 7 (2000) 367-370
38. Buchmueller K.L., Webb A.E., Richardson D.A., and Weeks K.M. A collapsed non-native RNA folding state. Nature Struct. Biol. 7 (2000) 362-366
39. Murthy V.L., and Rose G.D. Is counterion delocalization responsible for collapse in RNA folding?. Biochemistry 39 (2000) 14365-14370
40. Woodson S.A. Compact but disordered states of RNA. Nature Struct. Biol. 7 (2000) 349-352
41. Wilson T.J., Zhao Z.Y., Maxwell K., Kontogiannis L., and Lilley D.M. Importance of specific nucleotides in the folding of the natural form of the hairpin ribozyme. Biochemistry 40 (2001) 2291-2302
42. Woodson S.A. Folding mechanisms of group I ribozymes: role of stability and contact order. Biochem. Soc. Trans. 30 (2001) 1166-1169
43. Trieber D.K., and Williamson J.R. Beyond kinetic traps in RNA folding. Curr. Opin. Struct. Biol. 11 (2001) 309-314
44. Tinoco Jr. I., and Bustamante B. How RNA folds. J. Mol. Biol. 293 (1999) 271-281
45. Russell R., Zhuang X., Babcock H.P., Millett I.S., Doniach S., Chu S., and Herschlag D. Exploring the folding landscape of a structured RNA. Proc. Natl Acad. Sci. USA 99 (2002) 155-160
46. Schultes E.A., Spasic A., Mohanty U., and Bartel D.P. Compact and ordered collapse of randomly generated RNA sequences. Nature Struct. Mol. Biol. 12 (2005) 1130-1136
47. Phe. J. Mol. Biol. 334 (2003) 901-918
48. Phe. J. Mol. Biol. 319 (2002) 1015-1034
49. Buchmueller K.L., Webb A.E., Richardson D.A., and Weeks K.M. A collapsed non-native RNA folding state. Nature Struct. Biol. 7 (2000) 362-366
50. Schroeder R., Grossberger R., Pichler A., and Waldsich C. RNA folding in vivo. Curr. Opin. Struct. Biol. 12 (2002) 296-300
51. Kramer F.R., and Mills D.R. Secondary structure formation during RNA synthesis. Nucl. Acids Res. 9 (1981) 5109-5124
52. Pan T., and Sosnick T. RNA folding during transcription. Annu. Rev.Biophys. Biomol. Struct. 35 (2006) 161-175
53. Boyle J., Robillard G.T., and Kim S.H. Sequential folding of transfer RNA. A nuclear magnetic resonance study of successively longer tRNA fragments with a common 5′ end. J. Mol. Biol. 139 (1980) 601-625
54. Adilakshmi T., Ramaswamy P., and Woodson S.A. Protein-independent folding pathway of the 16 S rRNA 5′ domain. J. Mol. Biol. 351 (2005) 508-519
55. Sosnick T.R., and Pan T. RNA folding: models and perspectives. Curr. Opin. Struct. Biol. 13 (2003) 309-316
56. Newby M.I., and Greenbaum N.L. A conserved pseudouridine modification in eukaryotic U2 snRNA induces a change in branch-site architecture. RNA 7 (2001) 833-845
57. Björk G.R. Biosynthesis and function of modified nucleosides. In: Söll D., and RajBhandary U.L. (Eds). tRNA: Structure, Biosynthesis and Function (1995), ASM, Washington DC 165-205
58. Schroeder R., Grossberger R., Pichler A., and Waldsich C. RNA folding in vivo. Curr. Opin. Struct. Biol. 12 (2002) 296-300
59. Zheng M., Wu M., and Tinoco Jr. I. Formation of a GNRA tetraloop in P5abc can disrupt an interdomain interaction in the Tetrahymena group I ribozyme. Proc. Natl Acad. Sci. USA 98 (2001) 3695-3700
60. Silverman S.K., Zheng M., Wu M., Tinoco Jr. I., and Cech T.R. Quantifying the energetic interplay of RNA tertiary and secondary structure interactions. RNA 5 (1999) 1555-1674
61. +-C base-pair and by pseudouridine. J. Mol. Biol. 285 (1999) 115-131
62. Phe. Nucl. Acids Res. 33 (2005) 6961-6971
63. Meroueh M., Grohar P.J., Qiu J., SantaLucia Jr. J., Scaringe S.A., and Chow C.S. Unique structural and stabilizing roles for the individual pseudouridine residues in the 1920 region of Escherichia coli 23S rRNA. Nucl. Acids Res. 28 (2000) 2075-2083
64. Sumita M., Desaulniers J.P., Chang Y.C., Chui H.M., Clos II L., and Chow C.S. Effects of nucleotide substitution and modification on the stability and structure of helix 69 from 28S rRNA. RNA 11 (2005) 1420-1429
65. UUU species. Biochemistry 39 (2000) 13390-13395
66. Guenther R.H., Gopal D.H., and Agris P.F. Purification of transfer RNA species by single-step ion-exchange HPLC. J. Chromatog. 444 (1988) 79-87
67. Sampson J.R., and Uhlenbeck O.C. Biochemical and physical characterization of an unmodified yeast phenylalanine transfer RNA transcribed in vitro. Proc. Natl Acad. Sci. USA 85 (1988) 1033-1037
68. Milligan J.F., Groebe D.R., Witherell G.W., and Uhlenbeck O.C. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucl. Acids Res. 15 (1987) 8783-8798
69. Puglisi J.D., and Tinoco Jr. I. Absorbance melting curves of RNA. Methods Enzymol. 180 (1989) 304-325
70. McDowell J.A., and Turner D.H. Investigation of the structural basis for thermodynamic stabilities of tandem GU mismatches: solution structure of (rGAGGUCUC)2 by two-dimensional NMR and simulated annealing. Biochemistry 35 (1996) 14077-14089
71. Phe anticodon stem-loop. Biochemistry 31 (1992) 11004-11011
72. 2+ binding and coupled conformational transition in DNA analogs. Biochemistry 31 (1992) 11012-11019
73. Piotto M., Saudek V., and Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2 (1992) 661-665
74. Rho S.B., and Martinis S.A. The bI4 group I intron binds directly to both its protein splicing partners, a tRNA synthetase and maturase, to facilitate RNA splicing activity. RNA 6 (2000) 1882-1894
75. Martinis S.A., and Fox G.E. Non-standard amino acid recognition by Escherichia coli leucyl-tRNA synthetase. Nucl. Acids Symp. Ser. 26 (1977) 125-128
76. Lincecum Jr. T.L., Tukalo M., Yaremchuk A., Mursinna R.S., Williams A.M., Sproat B.S., et al. Structural and mechanistic basis of pre- and posttransfer editing by leucyl-tRNA synthetase. Mol. Cell. 11 (2003) 951-963
77. Leu. Biochemistry 40 (2001) 5376-5381