Structure-function relationships in the hammerhead ribozyme probed by base rescue

RNA

Volumn 4, Issue 11, 1998, Pages 1332-1346

  Peracchi, Alessio ^a,b   Matulic Adamic, Jasenka ^c   Wang, Shenglong ^a   Beigelman, Leonid ^c   Herschlag, Daniel ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITY OF PARMA   (Italy)

^c Sirna Therapeutics Inc   (United States)

Author keywords

Abasic sites; Binding; Catalysis; Chemical rescue; Enzyme; Functional groups; Mutagenesis; Ribozyme; RNA

Indexed keywords

ADENOSINE DERIVATIVE; RIBOZYME;

ARTICLE; CATALYSIS; KINETICS; MOLECULAR INTERACTION; MUTAGENESIS; NUCLEIC ACID BASE SUBSTITUTION; PRIORITY JOURNAL; RNA STRUCTURE; STRUCTURE ACTIVITY RELATION;

ADENINE; BASE SEQUENCE; BINDING SITES; CATALYTIC DOMAIN; CRYSTALLIZATION; GUANINE; HYDROGEN BONDING; KINETICS; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; NUCLEIC ACID CONFORMATION; RNA, CATALYTIC; STRUCTURE-ACTIVITY RELATIONSHIP; THERMODYNAMICS;

EID: 0031758565     PISSN: 13558382     EISSN: None     Source Type: Journal    
DOI: 10.1017/S1355838298980979     Document Type: Article

References (78)

1. Abola JE, Abraham DJ. 1976. The crystal structure of 3-methylguaine, a potentially miscoding base. Tetrahedron Lett 39:3483-3486.
2. Abramovitz DL, Friedman RA, Pyle AM. 1996. Catalytic role of 2′-hydroxyl groups within a group II intron active site. Science 277:1410-1413.
3. 2+ in RNA structure and function. Prog Nucleic Acid Res Mol Biol 53:79-129.
4. Baidya N, Ammons GE, Matulic-Adamic J, Karpeisky AM, Beigelman L, Uhlenbeck OC. 1997. Functional groups on the cleavage site pyrimidine nucleotide are required for stabilization of the hammerhead transition state. RNA 3:1135-1142.
5. Barrick D. 1994. Replacement of the proxymal ligand of sperm whale myoglobin with free imidazole in the mutant His-93-→Gly. Biochemistry 33:6546-6554.
6. Barrick D, Ho NT, Simplaceanu V, Dahlquist FW, Ho C. 1997. A test of the role of the proximal histidines in the Perutz model for cooperativity in haemoglobin. Nature Struct Biol 4:78-83.
7. Beigelman L, Karpeisky A, Matulic-Adamic C, Gonzales C, Usman N. 1995. New structural motifs for hammerhead ribozymes. Catalytic activity of abasic nucleotide substituted ribozymes. Nucleosides & Nucleotides 74:907-910.
8. Beigelman L, Karpeisky A, Usman N. 1994. Synthesis of 1-deoxy-D-ribofuranose phosphoramidite and the incorporation of abasic nucleotides in stem-loop II of a hammerhead ribozyme. Bioorg Med Chem Lett 4:1715-1720.
9. 3-nitrogens for efficient cleavage by a hammerhead ribozyme. Biochemistry 35:6483-6490.
10. Birikh KR, Heaton PA, Eckstein F. 1997. The structure, function and application of the hammerhead ribozyme. Eur J Biochem 245: 1-16.
11. Boehlein SK, Walworth ES, Richards NG, Schuster SM. 1997. Mutagenesis and chemical rescue indicate residues involved in β-aspartyl-AMP formation by Escherichia coli asparagine synthetase B. J Biol Chem 272:12384-12392
12. Bratty J, Chartrand P, Ferbeyre G, Cedergren R. 1993. The hammerhead RNA domain, a model ribozyme. Biochim Biophys Acta 1216:345-359.
13. Brown DJ. 1962. The chemistry of heterocyclic compounds, vol. 16: Pyrimidines. New York: Wiley.
14. Carlow DC, Smith AA, Yang CC, Short SA, Wolfenden R. 1995. Major contribution of a carboxymethyl group to transition-state stabilization by cytidine deaminase: Mutation and rescue. Biochemistry 34:4220-4224
15. Carter P, Abrahmsen L, Wells JA. 1991. Probing the mechanism and improving the rate of substrate-assisted catalysis in subtilisin BPN′. Biochemistry 30:6142-6148.
16. Cernà J. 1975. Effect of cytidine-5′-monophosphate on peptidyl transferase activity. FEBS Lett 56:94-98.
17. Cernà J, Holy A, Rychlìk I. 1978. The stimulation of ribosomal peptidyl transferase by cytosine and its derivatives. Collection Czechoslov Chem Commun 43:3279-3291.
18. Chartrand P, Usman N, Cedergren R. 1997. Effect of structural modifications on the activity of the leadzyme. Biochemistry 36:3145-3150.
19. Dahm SC, Derrick WB, Uhlenbeck OC. 1993. Evidence for the role of solvated metal hydroxide in the hammerhead cleavage mechanism. Biochemistry 32:13040-13045.
20. Dhalla AM, Li B, Alibhai MF, Yost KJ, Hemmingsen JM, Atkins WM, Schineller J, Villafranca JJ. 1994. Regeneration of catalytic activity of glutamine synthetase mutants by chemical activation: Exploration of the role of arginines 339 and 359 in activity. Protein Sci 3:476-481.
21. Eriksson AE, Baase WA, Wozniak JA, Matthews BW. 1992. A cavity-containing mutant of T4 lysozyme is stabilized by buried benzene. Nature 355:371-373.
22. Fasman GD. 1975. Handbook of biochemistry and molecular biology, 3rd ed., vol. I, Nucleic acids. Cleveland: CRC Press.
23. Fersht A. 1985. Enzyme structure and mechanism. New York: Freeman & Co.
24. Fitzgerald MM, Churchill MJ, McRee DE, Goodin DB. 1994. Small molecule binding to an artificially created cavity at the active site of cytochrome C peroxidase. Biochemistry 33:3807-3818.
25. Forster AC, Symons RH. 1987. Self-cleavage of plus and minus RNAs of a virusoid and a structural model for the active sites. Cell 49:211-220.
26. Frillingos S, Kaback HR. 1996. Chemical rescue of Asp237 → Ala and Lys358 → Ala mutants in the lactose permease of Escherichia Coli. Biochemistry 35:13363-13367.
27. Fu D-J, McLaughlin LW. 1992a. Importance of specific adenosine N′-nitrogens for efficient cleavage by a hammerhead ribozyme. A model for magnesium binding. Biochemistry 37:10941-10949.
28. Fu D-J, McLaughlin LW. 1992b. Importance of specific purine amino and hydroxyl groups for efficient cleavage by a hammerhead ribozyme. Proc Natl Acad Sci USA 89:3985-3989.
29. Fu D-J, Rajur SB, McLaughlin LW. 1993. Importance of specific guanosine N7 nitrogens and purine amino groups for efficient cleavage by a hammerhead ribozyme. Biochemistry 32:10629-10637.
30. Hall KB, Sampson JR, Uhlenbeck OC, Redfield AG. 1989. Structure of an unmodified tRNA molecule. Biochemistry 28:5794-5801.
31. Harpel MR, Hartman FC. 1994. Chemical rescue by exogenous amines of a site-directed mutant of ribulose 1,5-bisphosphate carboxylase/oxygenase that lacks a key lysyl residue. Biochemistry 33:5553-5561.
32. Herschlag D. 1995. RNA chaperones and the RNA folding problem. J Biol Chem 270:20871-20874.
33. Hertel KJ, Herschlag D, Uhlenbeck OC. 1994. A kinetic and thermodynamic framework for the hammerhead ribozyme reaction. Biochemistry 33:3374-3385.
34. Hertel KJ, Pardi A, Uhlenbeck OC, Koizumi M, Ohtsuka E, Uesugi S, Cedergren R, Eckstein F, Gerlach WL, Hodgson R, Symons RH. 1992. A numbering system for the hammerhead ribozyme. Nucleic Acids Res 20:3252.
35. Hertel KJ, Peracchi A, Uhlenbeck OC, Herschlag D. 1997. Use of intrinsic binding energy for catalysis by an RNA enzyme. Proc Natl Acad Sci USA 94:8947-8952.
36. 2 is required for the assembly of the binuclear metal center of phosphotriesterase. J Am Chem Soc 117:7580-7581.
37. Huang S, Tu SC. 1997. Identification and characterization of a catalytic base in bacterial luciferase by chemical rescue of a dark mutant. Biochemistry 36:14609-14615.
38. Kim S, Liang J, Barry BA. 1997. Chemical complementation identifies a proton acceptor for redox-active tyrosine D in photosystem II. Proc Natl Acad Sci USA 94:14406-14411.
39. Kim J, Ruzicka F, Frey P. 1990. Remodeling hexose-1-phosphate uridyltransferase: Mechanism-inspired mutation into a new enzyme, UDP-hexose synthase. Biochemistry 29:10590-10593.
40. Kintanar A, Yue D, Horowitz J. 1994. Effect of nucleoside modifications on the structure and thermal stability of Escherichia coli valine tRNA. Biochimie 76:1192-1204.
41. Kwiatkowski JS, Pullman B. 1975. Tautomerism and electronic structure of biological pyrimidines. In: Katritzky AR. Boulton AJ, eds. Advances in heterocyclic chemistry, vol. 18. New York: Academic Press. pp 199-327.
42. Lawley PD. 1971. Ionization and ultraviolet spectra of purines. In: Lister JH, ed. The chemistry of heterocyclic compounds, vol. 24: Fused pyrimidines. Part II, Purines. New York: Wiley. pp 439-496.
43. Lu Z, Nagata S, McPhie P, Miles EW. 1993. Lysine 87 in the β subunit of tryptophan synthase that forms an internal aldimine with pyridoxal phosphate serves critical roles in transimination, catalysis, and product release. J Biol Chem 268:8727-8734.
44. Matulic-Adamic J, Beigelman L, Potman S, Egli M, Usman N. 1996. Synthesis and structure of 1-deoxy-1-phenyl-β-D-ribofuranose and its incorporation into oligonucleotides. J Org Chem 67:3909-3911.
45. McKay D. 1996. Structure and function of the hammerhead ribozyme: An unfinished story. RNA 2:395-403.
46. Morton A, Baase WA, Matthews BW. 1995. Energetic origins of specificity of ligand binding in an interior nonpolar cavity of T4 lysozyme. Biochemistry 34:8564-8575.
47. Morton A, Matthews BW. 1995. Specificity of ligand binding in a buried nonpolar cavity of T4 lysozyme: Linkage of dynamics and structural plasticity. Biochemistry 34:8576-8588.
48. Murray JB, Adams CJ, Arnold JRP, Stockley PG. 1995. The roles of the conserved pyrimidine bases in hammerhead ribozyme catalysis: Evidence for a magnesium ion binding site. Biochem J 311:487-494.
49. Murray JB, Terwey DP, Maloney L, Karpeisky A, Usman N, Beigelman L, Scott WG. 1998. The structural basis of hammerhead ribozyme self-cleavage. Cell 92:665-673.
50. Narlikar GJ, Khosla M, Usman N, Herschlag D. 1997. Quantitating tertiary binding energies of 2′-OH groups on the P1 duplex of the tetrahymena ribozyme: Intrinsic binding energy in an RNA enzyme. Biochemistry 36:2465-2477.
51. Newmyer SL, Ortiz de Montellano PR. 1996. Rescue of the catalytic activity of an H42A mutant of horseradish peroxidase by exogenous imidazoles. J Biol Chem 271:14891-14896.
52. Ng MM, Benseler F, Tuschl T, Eckstein F. 1994. Isoguanosine substitution of conserved adenosines in the hammerhead ribozyme. Biochemistry 33:12119-12126.
53. Peracchi A, Beigelman L, Scott E, Uhlenbeck OC, Herschlag D. 1997. Involvement of a specific metal ion in the transition of the hammerhead ribozyme to its catalytic conformation. J Biol Chem 272:26822-26826.
54. Peracchi A, Beigelman L, Usman N, Herschlag D. 1996. Rescue of abasic hammerhead ribozymes by exogenous addition of specific bases. Proc Natl Acad Sci USA 93:11522-11527.
55. Perona JJ, Hedstrom L, Wagner RL, Rutter WJ, Craik CS, Fletterick RJ. 1994. Exogenous acetate reconstitutes the enzymatic activity of trypsin Asp189Ser. Biochemistry 33:3252-3259.
56. Asp transcripts deprived of modified nucleotides. Biochimie 72:735-744.
57. Phillips MA, Hedstrom L, Rutter WJ. 1992. Guanidine derivatives restore activity to carboxypeptidase lacking arginine-127. Protein Sci 1:517-521.
58. Pley HW, Flaherty KM, McKay DB. 1994. Three-dimensional structure of a hammerhead ribozyme. Nature 372:68-74.
59. Pullman B, Pullman A. 1972. Electronic aspects of purine tautomerism. In: Katritzky AR, Boulton AJ, eds. Advances in heterocyclic chemistry, vol. 13. New York: Academic Press, pp 77-160.
60. Ruffner DE, Stormo GD, Uhlenbeck OC. 1990. Sequence requirements of the hammerhead RNA self-cleavage reaction. Biochemistry 29:10695-10702.
61. Rynkiewicz MJ, Seaton BA. 1996. Chemical rescue by guanidine derivatives of an arginine-substituted site-directed mutant of Escherichia coli ornithine transcarbamylase. Biochemistry 35:16174-16179.
62. Schmidt S, Beigelman L, Karpeisky A, Usman N, Sorensen US, Gait MJ. 1996. Base and sugar requirements for RNA cleavage of essential nucleoside residues in internal loop B of the hairpin ribozyme: Implications for secondary structure. Nucleic Acids Res 24:573-581.
63. Scott AI. 1964. Interpretation of the ultraviolet spectra of natural products. New York: Pergamon Press.
64. Scott WG, Finch JT, Klug A. 1995. The crystal structure of an all-RNA hammerhead ribozyme: A proposed mechanism for RNA catalytic cleavage. Cell 81:991-1002.
65. Scott WG, Murray JB, Arnold JRP, Stoddard BL, Klug A. 1996. Capturing the structure of a catalytic RNA intermediate: The hammer-head ribozyme. Science 274:2065-2069.
66. Seela F, Debelak H, Usman N, Burgin A, Beigelman L. 1998. 1-Deazaadenosine: Synthesis and activity of base-modified hammerhead ribozymes. Nucleic Acids Res 26:1010-1018.
67. Seela F, Mersmann K, Grasby J, Gait MJ. 1993. 7-Deazaadenosine: Oligoribonucleotide building block synthesis and autocatalytic hydrolysis of base-modified hammerhead ribozymes. Helv Chim Acta 76:1809-1820.
68. Sekimoto T, Matsuyama T, Fukui T, Tanizawa K. 1993. Evidence for lysine 80 as general base catalyst of leucine dehydrogenase. J Biol Chem 265:27039-27045.
69. Sigler PB. 1975. An analysis of the structure of tRNA. Annu Rev Biophys Bioeng 4:477-527
70. Slim G, Gait MJ. 1992. The role of hexocyclic amino groups of conserved purines in hammerhead ribozyme cleavage. Biochem Biophys Res Commun 183:605-609.
71. Smith HB, Hartman FC. 1991. Demonstration of a functional requirement for the carbamate nitrogen of ribulosebisphosphate carboxylase/oxygenase by chemical rescue. Biochemistry 30:5172-5177.
72. Toney MD, Kirsch JF. 1989. Direct Brønsted analysis of the restoration of activity to a mutant enzyme by exogenous amines. Science 243:1485-1488.
73. Toney MD, Kirsch JF. 1992. Bronsted analysis of aspartate aminotransferase via exogenous catalysis of reactions of an inactive mutant. Protein Sci 1:107-119.
74. Tu CK, Silverman DN, Forsman C, Jonsson B-H, Lindskog S. 1989. Role of histidine 64 in the catalytic mechanism of human carbonic anhydrase II studied with a site-specific mutant. Biochemistry 23:7913-7918.
75. Ushida C, Muramatsu T, Mizushima H, Ueda T, Watanabe K, Stetter KO, Crain PF, McCloskey JA, Kuchino Y. 1996. Structural feature of the initiator tRNA gene from pyrodictium occultum and the thermal stability of its gene product tRNA(imet). Biochimie 78:847-855.
76. Wincott F, DiRenzo A, Shaffer C, Tracz D, Workman C, Sweedler D, Gonzales C, Scaringe S, Usman N. 1995. Synthesis, deprotection, analysis and purification of RNA and ribozymes. Nucleic Acids Res 23:2677-2684.
77. Val: An imino proton NMR investigation. Biochemistry 33:8905-8911.
78. Zhukovsky EA, Robinson PR, Oprian DD. 1991. Transducin activation by rhodopsin without a covalent bond to the 11-cis-retinal chromophore. Science 251:558-560. RNA (1998), 4:1347-1356.