The effect of secondary structure on cleavage of the phosphodiester bonds of RNA
Abstract
This review discusses the effects the secondary structure of an RNA molecule has on the inherent reactivity of its phosphodiester bonds, and on the catalytic activity of metal ion-based cleaving agents. The basic principles of the intramolecular transesterification of RNA phosphodiester bonds, particularly cleavage, are first briefly described. Studies of the structural effects on the cleavage, in the absence and in the presence of metal ion catalysts, are then reviewed, and the sources of the reactivity differences observed in different structures are discussed.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
We obtained single-nucleotide-resolution measurements of 3030 RNA fragments using In-line-seq.
“In particular, we obtained single-nucleotide-resolution measurements of 3030 RNA fragments using In-line-seq, a version of a low-bias ligation and reverse transcription protocol (MAP-seq)64 adapted here for in-line hydrolysis profiles65 (Fig. 3B).”
From Combinatorial optimization of mRNA structure, stability, and translation for RNA-based therapeutics (2022) · cites this paper as [64]
The base sequence and secondary structure of mRNA influence the rate of hydrolysis.
“In two publications on mRNA hydrolysis the authors state that the base sequence and secondary structure of mRNA influence the rate of hydrolysis (Kaukinen et al., 2002, Mikkola et al., 2001).”
From mRNA-lipid nanoparticle COVID-19 vaccines: structure and stability (2021) · cites this paper as Mikkola et al., 2001
Base-stacking may decrease the cleavage rate of phosphodiester bonds.
“Specifically, base-stacking may decrease the cleavage rate of phosphodiester bonds.”
From mRNA-lipid nanoparticle COVID-19 vaccines: structure and stability (2021) · cites this paper as Mikkola et al., 2001
Cites
The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme
Guerrier-Takada, C., Gardiner, K., Marsh, T., Pace, N., & Altman, S. (1983) · Cell · doi:10.1016/0092-8674(83)90117-4 · Cited by 2,684 · see citing works
Cech, T. R., Zaug, A. J., & Grabowski, P. J. (1981) · Cell · doi:10.1016/0092-8674(81)90390-1 · Cited by 879 · see citing works
Pseudo-rotation in the hydrolysis of phosphate esters
Westheimer, F. H. (1968) · Accounts of Chemical Research · doi:10.1021/ar50003a002 · Cited by 772 · see citing works
Structural Features that Give Rise to the Unusual Stability of RNA Hairpins Containing GNRA Loops
Heus, H. A., & Pardi, A. (1991) · Science · doi:10.1126/science.1712983 · Cited by 633 · see citing works
Li, Y., & Breaker, R. R. (1999) · Journal of the American Chemical Society · doi:10.1021/ja990592p · Cited by 587 · see citing works
Highly Efficient Synthesis of Covalently Cross-Linked Peptide Helices by Ring-Closing Metathesis
Blackwell, H. E., & Grubbs, R. H. (1998) · Angewandte Chemie International Edition · doi:10.1002/(sici)1521-3773(19981217)37:23 · Cited by 567 · see citing works
Williams, N. H., Takasaki, B. K., Wall, M., & Chin, J. (1999) · Accounts of Chemical Research · doi:10.1021/ar9500877 · Cited by 550 · see citing works
Relationship between internucleotide linkage geometry and the stability of RNA
Soukup, G. A., & Breaker, R. R. (1999) · RNA · doi:10.1017/s1355838299990891 · Cited by 549 · see citing works
The Intervening Sequence RNA of Tetrahymena Is an Enzyme
Zaug, A. J., & Cech, T. R. (1986) · Science · doi:10.1126/science.3941911 · Cited by 507 · see citing works
Oivanen, M., Kuusela, S., & Lönnberg, H. (1998) · Chemical Reviews · doi:10.1021/cr960425x · Cited by 438 · see citing works
Solution structure of an unusually stable RNA hairpin, 5GGAC(UUCG)GUCC
Cheong, C., Varani, G., & Tinoco, I. (1990) · Nature · doi:10.1038/346680a0 · Cited by 427 · see citing works
Structure of an unusually stable RNA hairpin
Varani, G., Cheong, C., & Tinoco, I. (1991) · Biochemistry · doi:10.1021/bi00227a016 · Cited by 369 · see citing works
Roles of zinc(II) ion in phosphatases. A model study with zinc(II)-macrocyclic polyamine complexes
Koike, T., & Kimura, E. (1991) · Journal of the American Chemical Society · doi:10.1021/ja00023a048 · Cited by 335 · see citing works
Sigman, D. S., Bruice, T. W., Mazumder, A., & Sutton, C. L. (1993) · Accounts of Chemical Research · doi:10.1021/ar00027a004 · Cited by 307 · see citing works
Trawick, B. N., Daniher, A. T., & Bashkin, J. K. (1998) · Chemical Reviews · doi:10.1021/cr960422k · Cited by 280 · see citing works
Unifying the Current Data on the Mechanism of Cleavage–Transesterification of RNA
Perreault, D. M., & Anslyn, E. V. (1997) · Angewandte Chemie International Edition in English · doi:10.1002/anie.199704321 · Cited by 277 · see citing works
Brown, R. S., Dewan, J. C., & Klug, A. (1985) · Biochemistry · doi:10.1021/bi00339a012 · Cited by 263 · see citing works
Loll, P. J., & Lattman, E. E. (1989) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340050302 · Cited by 261 · see citing works
Brown, R. S., Hingerty, B. E., Dewan, J. C., & Klug, A. (1983) · Nature · doi:10.1038/303543a0 · Cited by 226 · see citing works
A small metalloribozyme with a two-step mechanism
Pan, T., & Uhlenbeck, O. C. (1992) · Nature · doi:10.1038/358560a0 · Cited by 215 · see citing works
In vitro selection of RNAs that undergo autolytic cleavage with lead(2+)
Pan, T., & Uhlenbeck, O. C. (1992) · Biochemistry · doi:10.1021/bi00131a001 · Cited by 197 · see citing works
Zhou, D., & Taira, K. (1998) · Chemical Reviews · doi:10.1021/cr9604292 · Cited by 195 · see citing works
Järvinen, P., Oivanen, M., & Lönnberg, H. (1991) · The Journal of Organic Chemistry · doi:10.1021/jo00018a037 · Cited by 184 · see citing works
Hydrolytic stability of helical RNA: a selective advantage for the natural 3',5'-bond.
Usher, D. A., & McHale, A. H. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.4.1149 · Cited by 179 · see citing works
Lead-catalyzed cleavage of yeast tRNAPhe mutants
Behlen, L. S., Sampson, J. R., DiRenzo, A. B., & Uhlenbeck, O. C. (1990) · Biochemistry · doi:10.1021/bi00462a013 · Cited by 155 · see citing works
Sequence-Specific Cleavage of HIV mRNA by a Ribozyme Mimic
Bashkin, J. K., Frolova, E. I., & Sampath, U. (1994) · Journal of the American Chemical Society · doi:10.1021/ja00092a064 · Cited by 149 · see citing works
Breslow, R., & Huang, D. L. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.10.4080 · Cited by 149 · see citing works
Blaskó, A., & Bruice, T. C. (1999) · Accounts of Chemical Research · doi:10.1021/ar980060y · Cited by 135 · see citing works
Sequence-Specific and Hydrolytic Scission of DNA and RNA by Lanthanide Complex-OligoDNA Hybrids1
Komiyama, M. (1995) · The Journal of Biochemistry · doi:10.1093/oxfordjournals.jbchem.a124961 · Cited by 130 · see citing works
Anslyn, E. V., & Breslow, R. (1989) · Journal of the American Chemical Society · doi:10.1021/ja00194a050 · Cited by 117 · see citing works
Stacking Free Energy Profiles for All 16 Natural Ribodinucleoside Monophosphates in Aqueous Solution
Norberg, J., & Nilsson, L. (1995) · Journal of the American Chemical Society · doi:10.1021/ja00149a006 · Cited by 110 · see citing works
Structure, Reactivity, and Biology of Double-Stranded RNA
Nicholson, A. W. (1996) · Progress in nucleic acid research and molecular biology · doi:10.1016/s0079-6603(08)60963-0 · Cited by 108 · see citing works
Selection of an RNA domain that binds Zn2+.
Ciesiołka, J., Górski, J., & Yarus, M. (1995) · PubMed · Cited by 108 · see citing works
Ciesiołka, J., Michałowski, D., Wrzesiński, J., Krajewski, J., & Krzyżosiak, W. J. (1998) · Journal of Molecular Biology · doi:10.1006/jmbi.1997.1462 · Cited by 106 · see citing works
Molinaro, M., & Tinoco, I. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.15.3056 · Cited by 100 · see citing works
Depolymerization of ribonucleic acid by plumbous ion
Farkas, W. R. (1968) · Biochimica et Biophysica Acta (BBA) - Nucleic Acids and Protein Synthesis · doi:10.1016/0005-2787(68)90184-6 · Cited by 100 · see citing works
Hall, J., Hüsken, D., Pieles, U., Moser, H. E., & Häner, R. (1994) · Chemistry & Biology · doi:10.1016/1074-5521(94)90008-6 · Cited by 99 · see citing works
Crystal structure of a lead-dependent ribozyme revealing metal binding sites relevant to catalysis.
Wedekind, J. E., & McKay, D. B. (1999) · Nature Structural Biology · doi:10.1038/6700 · Cited by 96 · see citing works
Vlassov, V. V., Zuber, G., Felden, B., Behr, J., & Giegé, R. (1995) · Nucleic Acids Research · doi:10.1093/nar/23.16.3161 · Cited by 93 · see citing works
Towards artificial ribonucleases: the sequence-specific cleavage of RNA in a duplex
Hall, J. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.18.3522 · Cited by 87 · see citing works
Transesterification of a phosphate diester by divalent and trivalent metal ions
Morrow, J. R., Buttrey, L. A., & Berback, K. A. (1992) · Inorganic Chemistry · doi:10.1021/ic00027a005 · Cited by 86 · see citing works
Imidazole Tethered Oligodeoxyribonucleotides: Synthesis and RNA Cleaving Activity
Hovinen, J., Guzaev, A. P., Azhayeva, E., Azhayev, A. V., & Lönnberg, H. (1995) · The Journal of Organic Chemistry · doi:10.1021/jo00112a047 · Cited by 85 · see citing works
Properties of an In vitro Selected Pb2+ Cleavage Motif
Pan, T., Dichtl, B., & Uhlenbeck, O. C. (1994) · Biochemistry · doi:10.1021/bi00198a023 · Cited by 82 · see citing works
Creating RNA Bulges: Cleavage of RNA in RNA/DNA Duplexes by Metal Ion Catalysis
Hüsken, D., Goodall, G. J., Blommers, M. J. J., Jahnke, W., Hall, J., Häner, R., & Moser, H. E. (1996) · Biochemistry · doi:10.1021/bi961700c · Cited by 80 · see citing works
Hoogstraten, C. G., Legault, P., & Pardi, A. (1998) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2182 · Cited by 78 · see citing works
Podyminogin, M. A., VIassov, V. V., & Giegé, R. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.25.5950 · Cited by 76 · see citing works
Nonenzymatic hydrolysis of oligoribonucleotides
Kierzek, R. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.19.5079 · Cited by 74 · see citing works
Butzow, J. J., & Eichhorn, G. L. (1971) · Biochemistry · doi:10.1021/bi00787a009 · Cited by 73 · see citing works
Portmann, S., Grimm, S., Workman, C. T., Usman, N., & Egli, M. (1996) · Chemistry & Biology · doi:10.1016/s1074-5521(96)90260-4 · Cited by 70 · see citing works
Cuchillo, C. M., Parés, X., Guasch, A., Barman, T., Travers, F., & Nogués, M. V. (1993) · FEBS Letters · doi:10.1016/0014-5793(93)80654-d · Cited by 70 · see citing works
Phosphate ester hydrolysis: calculation of gas-phase reaction paths and solvation effects
Dejaegere, A. P., Liang, X., & Karplus, M. (1994) · Journal of the Chemical Society Faraday Transactions · doi:10.1039/ft9949001763 · Cited by 69 · see citing works
The Liberation of Polynucleotides by the Alkaline Hydrolysis of Ribonucleic Acid from Yeast
Smith, K. C., & Allen, F. W. (1953) · Journal of the American Chemical Society · doi:10.1021/ja01105a031 · Cited by 69 · see citing works
Hegg, E. L., Deal, K. A., Kiessling, L. L., & Burstyn, J. N. (1997) · Inorganic Chemistry · doi:10.1021/ic960955b · Cited by 68 · see citing works
β-Thiopeptides: Synthesis, NMR Solution Structure, CD Spectra, and Photochemistry
Sifferlen, T., Rueping, M., Gademann, K., Jaun, B., & Seebàch, D. (1999) · Helvetica Chimica Acta · doi:10.1002/(sici)1522-2675(19991215)82:12 · Cited by 68 · see citing works
Hydrolysis of oligoribonucleotides: influence of sequence and length
Kierzek, R. (1992) · Nucleic Acids Research · doi:10.1093/nar/20.19.5073 · Cited by 65 · see citing works
Mikkola, S., Stenman, E., Nurmi, K., Yousefi-Salakdeh, E., Strömberg, R., & Lönnberg, H. (1999) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/a903691a · Cited by 65 · see citing works
Order, dynamics and metal-binding in the lead-dependent ribozyme 1 1Edited by I. Tinoco
Legault, P., Hoogstraten, C. G., Metlitzky, E., & Pardi, A. (1998) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.2181 · Cited by 65 · see citing works
Laing, L. G., & Hall, K. B. (1996) · Biochemistry · doi:10.1021/bi961310q · Cited by 65 · see citing works
Reynolds, M. A., Beck, T., Say, P. B., Schwartz, D. A., Dwyer, B. P., Daily, W. J., Vaghefi, M. M., Metzler, M. D., Klem, R. E., & Arnold, L. J. (1996) · Nucleic Acids Research · doi:10.1093/nar/24.4.760 · Cited by 62 · see citing works
A trinucleotide can promote metal ion-dependent specific cleavage of RNA.
祐二, 有., & 幹, 直. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.17.7939 · Cited by 60 · see citing works
Breslow, R., Dong, S. D., Webb, Y., & Xu, R. (1996) · Journal of the American Chemical Society · doi:10.1021/ja9526933 · Cited by 60 · see citing works
Dange, V., Atta, R. B. V., & Hecht, S. M. (1990) · Science · doi:10.1126/science.2185542 · Cited by 57 · see citing works
Ciesiołka, J., Marciniec, T., & Krzyżosiak, W. J. (1989) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1989.tb14851.x · Cited by 56 · see citing works
Magda, D. J., Crofts, S., Lin, A. V., Miles, D., Wright, M., & Sessler, J. L. (1997) · Journal of the American Chemical Society · doi:10.1021/ja9627149 · Cited by 54 · see citing works
The exceptional resistance of certain oligoribonucleotides to alkaline degradation
Lane, B. G., & Butler, G. C. (1959) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(59)90539-6 · Cited by 52 · see citing works
Effect of europium(III) on the thermal denaturation and cleavage of transfer ribonucleic acids
Rordorf, B. F., & Kearns, D. R. (1976) · Biopolymers · doi:10.1002/bip.1976.360150805 · Cited by 52 · see citing works
The Role of Metals in the Hydrolytic Cleavage of DNA and RNA
Bashkin, J. K., & Jenkins, L. A. (1994) · Comments on Inorganic Chemistry · doi:10.1080/02603599408035852 · Cited by 51 · see citing works
Kuusela, S., & Lönnberg, H. (1993) · Journal of Physical Organic Chemistry · doi:10.1002/poc.610060606 · Cited by 48 · see citing works
Site-selective hydrolysis of tRNA by lanthanide metal complexes
Hayashi, N., Takeda, N., Shiiba, T., Yashiro, M., Watanabe, K., & Komiyama, M. (1993) · Inorganic Chemistry · doi:10.1021/ic00078a002 · Cited by 47 · see citing works
Zagorowska, I., Kuusela, S., & Lönnberg, H. (1998) · Nucleic Acids Research · doi:10.1093/nar/26.14.3392 · Cited by 47 · see citing works
Role of Nd3+ and Pb2+ on the RNA Cleavage Reaction by a Small Ribozyme
Ohmichi, T., & Sugimoto, N. (1997) · Biochemistry · doi:10.1021/bi962030d · Cited by 45 · see citing works
Oivanen, M., Schnell, R., Pfleiderer, W., & Lönnberg, H. (1991) · The Journal of Organic Chemistry · doi:10.1021/jo00011a032 · Cited by 43 · see citing works
Aliphatic analogues of nucleotides: synthesis and affinity towards nucleases
Holý, A., & Gs, I. (1974) · Nucleic Acids Research · doi:10.1093/nar/1.1.19 · Cited by 42 · see citing works
Ciesiołka, J., Lorenz, S., & Erdmann, V. A. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16670.x · Cited by 42 · see citing works
Development of artificial ribonucleases
Häner, R., Hall, J., Pfützer, A., & Hüsken, D. (1998) · Pure and Applied Chemistry · doi:10.1351/pac199870010111 · Cited by 41 · see citing works
Role of metal ions in ribozymes.
Am, P. (1996) · PubMed · Cited by 41 · see citing works
Ikenaga, H., & Inoue, Y. (1974) · Biochemistry · doi:10.1021/bi00700a027 · Cited by 40 · see citing works
Trivalent lanthanide ions do not cleave RNA in DNA-RNA hybrids
Kolasa, K. A., Morrow, J. R., & Sharma, A. P. (1993) · Inorganic Chemistry · doi:10.1021/ic00071a002 · Cited by 40 · see citing works
Kosonen, M., Yousefi-Salakdeh, E., Strömberg, R., & Lönnberg, H. (1997) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/a704636g · Cited by 37 · see citing works
Precise control of RNA cleavage by ribozyme mimics
Daniher, A. T., & Bashkin, J. K. (1998) · Chemical Communications · doi:10.1039/a800818c · Cited by 31 · see citing works
The Nonenzymic Hydrolysis of Nucleoside 2',3'-Phosphates*
Abrash, H. I., Cheung, C.-C. S., & Davis, J. C. (1967) · Biochemistry · doi:10.1021/bi00857a011 · Cited by 30 · see citing works
Specific RNA cleavages induced by manganese ions
Wrzesiński, J., Michałowski, D., Ciesiołka, J., & Krzyżosiak, W. J. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)01077-r · Cited by 29 · see citing works
Sreedhara, A., Patwardhan, A., & Cowan, J. A. (1999) · Chemical Communications · doi:10.1039/a901140d · Cited by 29 · see citing works
Cleavages Induced by Different Metal Ions in Yeast tRNAPhe U59C60 Mutants
Michałowski, D., Wrzesiński, J., & Krzyżosiak, W. J. (1996) · Biochemistry · doi:10.1021/bi9530393 · Cited by 29 · see citing works
Ciesiołka, J., Lorenz, S., & Erdmann, V. A. (1992) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1992.tb16671.x · Cited by 28 · see citing works
Mechanisms of catalysis by imidazole buffers of the hydrolysis and isomerisation of RNA models
Beckmann, C., Kirby, A. J., Kuusela, S., & Tickle, D. C. (1998) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/a707741f · Cited by 28 · see citing works
Metal-ion-promoted hydrolysis of polyuridylic acid
Kuusela, S., & Lönnberg, H. (1994) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/p29940002301 · Cited by 28 · see citing works
Sequence-Specific Hydrolysis of Yeast tRNAPhe Mediated by Metal-Free Bleomycin
Keck, M. V., & Hecht, S. M. (1995) · Biochemistry · doi:10.1021/bi00037a046 · Cited by 28 · see citing works
Kosonen, M., & Lönnberg, H. (1995) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/p29950001203 · Cited by 28 · see citing works
Haim, A. (1992) · Journal of the American Chemical Society · doi:10.1021/ja00048a006 · Cited by 27 · see citing works
Kosonen, M., Oivanen, M., & Lönnberg, H. (1994) · The Journal of Organic Chemistry · doi:10.1021/jo00092a037 · Cited by 27 · see citing works
Kuusela, S., & Lönnberg, H. (1992) · Journal of Physical Organic Chemistry · doi:10.1002/poc.610051205 · Cited by 26 · see citing works
Witzel, H. (1960) · Justus Liebig s Annalen der Chemie · doi:10.1002/jlac.19606350122 · Cited by 26 · see citing works
Kuusela, S., & Lönnberg, H. (1994) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/p29940002109 · Cited by 24 · see citing works
Kosonen, M., Yousefi-Salakdeh, E., Strömberg, R., & Lönnberg, H. (1998) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/a801670d · Cited by 24 · see citing works
Effect of Structural Modifications on the Activity of the Leadzyme
Chartrand, P., Usman, N., & Cedergren, R. (1997) · Biochemistry · doi:10.1021/bi962219p · Cited by 24 · see citing works
Sundaralingam, M., Rubin, J. R., & Cannon, J. F. (1984) · International Journal of Quantum Chemistry · doi:10.1002/qua.560260736 · Cited by 23 · see citing works
Hydrolytic cleavage of RNA catalyzed by metal ion complexes.
Morrow, J. R. (1996) · PubMed · Cited by 23 · see citing works
RNA Hydrolysis by the Cooperation of Carboxylate Ion and Ammonium Ion
Endo, M., Hirata, K., Ihara, T., Sueda, S., Takagi, M., & Komiyama, M. (1996) · Journal of the American Chemical Society · doi:10.1021/ja960009u · Cited by 22 · see citing works
Kosonen, M., Hakala, K., & Lönnberg, H. (1998) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/a707095k · Cited by 20 · see citing works
Kuusela, S., & Lönnberg, H. (1996) · Nucleosides and Nucleotides · doi:10.1080/07328319608002466 · Cited by 19 · see citing works
Inoue, H., Furukawa, T., Shimizu, M., Tamura, T., Matsui, M., & Ohtsuka, E. (1999) · Chemical Communications · doi:10.1039/a808522f · Cited by 19 · see citing works
Sequence-specific cleavage of oligoribonucleotide capable of forming a stem and loop structure.
Hosaka, H., Sakabe, I., Sakamoto, K., Yokoyama, S., & TAKAKU, H. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32131-2 · Cited by 18 · see citing works
Kuusela, S., Azhayev, A. V., Guzaev, A. P., & Lönnberg, H. (1995) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/p29950001197 · Cited by 18 · see citing works
Ribozyme mimics as catalytic antisense reagents
Bashkin, J. K., Sampath, U., & Frolova, E. I. (1995) · Applied Biochemistry and Biotechnology · doi:10.1007/bf02787910 · Cited by 18 · see citing works
On the Mechanism of Buffer-Catalyzed Hydrolysis of RNA Models
Perrin, C. L. (1995) · The Journal of Organic Chemistry · doi:10.1021/jo00110a030 · Cited by 16 · see citing works
The negative rate constants of Breslow and Huang
Menger, F. M. (1991) · The Journal of Organic Chemistry · doi:10.1021/jo00022a001 · Cited by 16 · see citing works
Michao̵wski, D., Wrzesiński, J., Ciesiok̵a, J., & Krzyżosiak, W. J. (1996) · Biochimie · doi:10.1016/0300-9084(96)82645-9 · Cited by 13 · see citing works
Kuusela, S., Guzaev, A. P., & Lönnberg, H. (1996) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/p29960001895 · Cited by 13 · see citing works
Effect of metal ions on the hydrolytic reactions of nucleosides and their phosphoesters.
Kuusela, S., & Lönnberg, H. (1996) · PubMed · Cited by 13 · see citing works
RNA hydrolysis by cobalt(III) complexes 1
Komiyama, M., Matsumoto, Y., Takahashi, H., Shiiba, T., Tsuzuki, H., Yajima, H., Yashiro, M., & Sumaoka, J. (1998) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/a706624d · Cited by 12 · see citing works
Structural analysis of two plant 5S rRNA species and fragments thereof by lead‐induced hydrolysis
Ciesiołka, J., & Krzyżosiak, W. J. (1996) · IUBMB Life · doi:10.1080/15216549600201341 · Cited by 11 · see citing works
Kuusela, S., Rantanen, M., & Lönnberg, H. (1995) · Journal of the Chemical Society Perkin Transactions 2 · doi:10.1039/p29950002269 · Cited by 10 · see citing works
Duarte, V., Doisneau-Sixou, S. F., Favre, G., Pratviel, G., & Meunier, B. (1997) · Journal of the Chemical Society Dalton Transactions · doi:10.1039/a704743f · Cited by 10 · see citing works
Kuusela, S., & Lönnberg, H. (1998) · Nucleosides and Nucleotides · doi:10.1080/07328319808004328 · Cited by 8 · see citing works
Oivanen, M., Mikhailov, S. N., Florentiev, V. L., Vihanto, P., Lönnberg, H., Led, J. J., MIlanova, R. K., Nakata, H., Nasiri, A., & Tsuda, T. (1993) · Acta chemica Scandinavica/Acta chemica Scandinavica. B, Organic chemistry and biochemistry/Acta chemica Scandinavica. A, Physical and inorganic chemistry/Acta chemica Scandinavica. Series B. Organic chemistry and biochemistry/Acta chemica Scandinavica. Series A, Physical and inorganic chemistry · doi:10.3891/acta.chem.scand.47-0622 · Cited by 7 · see citing works
Oivanen, M., & Lönnberg, H. (1994) · ChemInform · doi:10.1002/chin.199425289 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
mRNA-lipid nanoparticle COVID-19 vaccines: structure and stability
Schoenmaker, L., Witzigmann, D., Kulkarni, J. A., Verbeke, R., Kersten, G., Jiskoot, W., & Crommelin, D. J. A. (2021) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2021.120586 · Cited by 1,566 · see citing works
Addressing the Cold Reality of mRNA Vaccine Stability
Crommelin, D. J. A., Anchordoquy, T. J., Volkin, D. B., Jiskoot, W., & Mastrobattista, E. (2021) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2020.12.006 · Cited by 517 · see citing works
Combinatorial optimization of mRNA structure, stability, and translation for RNA-based therapeutics
Leppek, K., Byeon, G. W., Kladwang, W., Wayment-Steele, H. K., Kerr, C. H., Xu, A. F., Kim, D. S., Topkar, V. V., Choe, C., Rothschild, D., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28776-w · Cited by 399 · see citing works
Combinatorial optimization of mRNA structure, stability, and translation for RNA-based therapeutics
Leppek, K., Byeon, G. W., Kladwang, W., Wayment-Steele, H. K., Kerr, C. H., Xu, A. F., Kim, D. S., Topkar, V. V., Choe, C., Rothschild, D., et al. (2021) · doi:10.1101/2021.03.29.437587 · Cited by 399 · see citing works
Synthetic metallonucleases for RNA cleavage
Morrow, J. R., & Iranzo, O. (2004) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2004.02.006 · Cited by 223 · see citing works
The Storage and In-Use Stability of mRNA Vaccines and Therapeutics: Not A Cold Case
Blenke, E. O., Örnskov, E., Schöneich, C., Nilsson, G. Å., Volkin, D. B., Mastrobattista, E., Almarsson, Ö., & Crommelin, D. J. A. (2022) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2022.11.001 · Cited by 214 · see citing works
Self-selection of dissipative assemblies driven by primitive chemical reaction networks
Tena‐Solsona, M., Wanzke, C., Rieß, B., Bausch, A. R., & Boekhoven, J. (2018) · Nature Communications · doi:10.1038/s41467-018-04488-y · Cited by 197 · see citing works
Theoretical basis for stabilizing messenger RNA through secondary structure design
Wayment-Steele, H. K., Kim, D. S., Choe, C. A., Nicol, J. J., Wellington-Oguri, R., Watkins, A. M., Parra Sperberg, R. A., Huang, P.-S., Participants, E., & Das, R. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab764 · Cited by 197 · see citing works
Mancin, F., & Tecilla, P. (2007) · New Journal of Chemistry · doi:10.1039/b703556j · Cited by 184 · see citing works
Research Advances on the Stability of mRNA Vaccines
Cheng, F., Wang, Y., Bai, Y., Liang, Z., Mao, Q., Liu, D., Wu, X., & Xu, M. (2023) · Viruses · doi:10.3390/v15030668 · Cited by 171 · see citing works
Cleavage of RNA phosphodiester bonds by small molecular entities: a mechanistic insight
Lönnberg, H. (2011) · Organic & Biomolecular Chemistry · doi:10.1039/c0ob00486c · Cited by 111 · see citing works
Current landscape of mRNA technologies and delivery systems for new modality therapeutics
Lu, R., Hsu, H.-E., Perez, S. J. L. P., Kumari, M., Chen, G., Hong, M.-H., Lin, Y.-S., Liu, C.-H., Ko, S.-H., Concio, C. A. P., et al. (2024) · Journal of Biomedical Science · doi:10.1186/s12929-024-01080-z · Cited by 113 · see citing works
Role of an Active Site Adenine in Hairpin Ribozyme Catalysis
Kuzmin, Y. I., Costa, C. P. D., Cottrell, J. W., & Fedor, M. J. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.04.005 · Cited by 105 · see citing works
A Biopharmaceutical Perspective on Higher-Order Structure and Thermal Stability of mRNA Vaccines
Kloczewiak, M. A., Banks, J. M., Jin, L., & Brader, M. L. (2022) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.2c00092 · Cited by 89 · see citing works
Salter, J. D., Krucinska, J., Alam, S., Grum-Tokars, V. L., & Wedekind, J. E. (2005) · Biochemistry · doi:10.1021/bi051887k · Cited by 87 · see citing works
Ripoll, M., Bernard, M., Vaure, C., Bazin, E., Commandeur, S., Perkov, V., Lemdani, K., Nicolaï, M., Bonifassi, P., Kichler, A., et al. (2022) · Biomaterials · doi:10.1016/j.biomaterials.2022.121570 · Cited by 85 · see citing works
Metal Ion-Based RNA Cleavage as a Structural Probe
Forconi, M., & Herschlag, D. (2009) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(09)68005-8 · Cited by 70 · see citing works
Review of machine learning for lipid nanoparticle formulation and process development
Dorsey, P. J., Lau, C. L., Chang, T., Doerschuk, P. C., & D’Addio, S. M. (2024) · Journal of Pharmaceutical Sciences · doi:10.1016/j.xphs.2024.09.015 · Cited by 73 · see citing works
Synthesis of new OBAN's and further studies on positioning of the catalytic group
Åström, H., & Strömberg, R. (2004) · Organic & Biomolecular Chemistry · doi:10.1039/b403652b · Cited by 48 · see citing works
Åström, H., Williams, N. H., & Strömberg, R. (2003) · Organic & Biomolecular Chemistry · doi:10.1039/b212216b · Cited by 47 · see citing works
Noll, B. O., Seiffert, S., Vornlocher, H., & Roehl, I. (2011) · Journal of Chromatography A · doi:10.1016/j.chroma.2011.06.057 · Cited by 46 · see citing works
Murtola, M., & Strömberg, R. (2008) · Organic & Biomolecular Chemistry · doi:10.1039/b810106j · Cited by 40 · see citing works
mRNA Synthesis and Encapsulation in Ionizable Lipid Nanoparticles
McKenzie, R. E., Minnell, J. J., Ganley, M., Painter, G. F., & Draper, S. L. (2023) · Current Protocols · doi:10.1002/cpz1.898 · Cited by 35 · see citing works
Template-based copying in chemically fuelled dynamic combinatorial libraries
Kriebisch, C. M. E., Burger, L., Zozulia, O., Stasi, M., Floroni, A., Braun, D., Gerland, U., & Boekhoven, J. (2024) · Nature Chemistry · doi:10.1038/s41557-024-01570-5 · Cited by 32 · see citing works
Effect of Ribose Conformation on RNA Cleavage via Internal Transesterification
Guo, F., Yue, Z.-K., Trajkovski, M., Zhou, X., Cao, D., Li, Q., Wang, B., Wen, X., Plavec, J., Peng, Q., et al. (2018) · Journal of the American Chemical Society · doi:10.1021/jacs.8b06313 · Cited by 29 · see citing works
Razkin, J., Lindgren, J., Nilsson, H., & Baltzer, L. (2008) · ChemBioChem · doi:10.1002/cbic.200800057 · Cited by 26 · see citing works
Evaluation of Gel-Pad Oligonucleotide Microarray Technology by Using Artificial Neural Networks
Pozhitkov, A. E., CHERNOV, B. K., Yershov, G., & Noble, P. A. (2005) · Applied and Environmental Microbiology · doi:10.1128/aem.71.12.8663-8676.2005 · Cited by 26 · see citing works
Characterization of side reactions during the annealing of small interfering RNAs
Seiffert, S., Debelak, H., Hadwiger, P., Jahn‐Hofmann, K., Roehl, I., Vornlocher, H., & Noll, B. O. (2011) · Analytical Biochemistry · doi:10.1016/j.ab.2011.02.040 · Cited by 24 · see citing works
Jancsó, A., Mikkola, S., Lönnberg, H., Hegetschweiler, Κ., & Gajda, T. (2003) · Chemistry - A European Journal · doi:10.1002/chem.200305149 · Cited by 24 · see citing works
Enhanced RNA cleavage within bulge-loops by an artificial ribonuclease
Kuznetsova, I. L. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki264 · Cited by 22 · see citing works
Hu, Q., Jayasinghe‐Arachchige, V. M., Zuchniarz, J., & Prabhakar, R. S. (2019) · Frontiers in Chemistry · doi:10.3389/fchem.2019.00195 · Cited by 21 · see citing works
Kaukinen, U., Venäläinen, T., Lönnberg, H., & Peräkylä, M. (2003) · Organic & Biomolecular Chemistry · doi:10.1039/b302751a · Cited by 21 · see citing works
Laine, M., Ketomäki, K., Poijärvi-Virta, P., & Lönnberg, H. (2009) · Organic & Biomolecular Chemistry · doi:10.1039/b904828f · Cited by 20 · see citing works
Cleavage of a RNA analog containing uridine by a bifunctional dinuclear Zn(II) catalyst
Rossiter, C. S., Mathews, R. A., DELMUNDO, I., & MORROW, J. (2008) · Journal of Inorganic Biochemistry · doi:10.1016/j.jinorgbio.2008.09.004 · Cited by 20 · see citing works
Not so cold! Improving the thermostability of mRNA vaccines
Haensler, J., Even, L., Wils, P., Bensaid, F., Dias, A., Deng, H., Karve, S., & DeRosa, F. (2025) · Expert Review of Vaccines · doi:10.1080/14760584.2025.2596674 · Cited by 21 · see citing works
Takeuchi, N., Salazar, L., Poole, A. M., & Hogeweg, P. (2008) · Biology Direct · doi:10.1186/1745-6150-3-33 · Cited by 18 · see citing works
Murtola, M., Ghidini, A., Virta, P., & Strömberg, R. (2017) · Molecules · doi:10.3390/molecules22111856 · Cited by 17 · see citing works
Bernhardt, H. S., & Sandwick, R. K. (2014) · Journal of Molecular Evolution · doi:10.1007/s00239-014-9640-1 · Cited by 14 · see citing works
Zhang, Z., Mikkola, S., & Lönnberg, H. (2003) · Organic & Biomolecular Chemistry · doi:10.1039/b210663a · Cited by 13 · see citing works
Kaukinen, U., Lönnberg, H., & Peräkylä, M. (2003) · Organic & Biomolecular Chemistry · doi:10.1039/b309828a · Cited by 13 · see citing works
Process and analytical strategies for the safe production of mRNA vaccines and therapeutics
Nowak, C. J. A., Liu, S., Falconer, R. J., & Gerstweiler, L. (2026) · Molecular Biology Reports · doi:10.1007/s11033-026-11455-0 · Cited by 14 · see citing works
Led-Seq: ligation-enhanced double-end sequence-based structure analysis of RNA
Kolberg, T., von Löhneysen, S., Ozerova, I., Wellner, K., Hartmann, R. K., Stadler, P. F., & Mörl, M. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad312 · Cited by 11 · see citing works
Lönnberg, T., Kiiski, J., & Mikkola, S. (2005) · Organic & Biomolecular Chemistry · doi:10.1039/b500054h · Cited by 11 · see citing works
Duplex Formation and the Origins of Homochirality
Ross, D. S., & Deamer, D. W. (2022) · Astrobiology · doi:10.1089/ast.2021.0018 · Cited by 10 · see citing works
Natural deep eutectic solvents protect RNA from thermal-induced degradation
Mattioli, R., Maggiore, A., Risola, D. D., Federico, R., D’Erme, M., Francioso, A., & Mosca, L. (2023) · Archives of Biochemistry and Biophysics · doi:10.1016/j.abb.2023.109714 · Cited by 10 · see citing works
Ren, M., Cheng, Y., Duan, Q., & Zhou, C. (2019) · Chemical Research in Toxicology · doi:10.1021/acs.chemrestox.9b00059 · Cited by 10 · see citing works
Kirsebom, L. A., & Ciesiołka, J. (2014) · doi:10.1002/9783527647064.ch13 · Cited by 10 · see citing works
Regulatory perspective for quality evaluation of lipid nanoparticle-based mRNA vaccines in China
Lu, J., Wei, W., & He, W. (2023) · Biologicals · doi:10.1016/j.biologicals.2023.101700 · Cited by 9 · see citing works
Pb 2+ ‐induced Cleavage of RNA
Kirsebom, L. A., & Ciesiołka, J. (2005) · doi:10.1002/9783527619504.ch13 · Cited by 8 · see citing works
Lönnberg, H. (2022) · The Chemical Record · doi:10.1002/tcr.202200141 · Cited by 7 · see citing works
Beloglazova, N. G., Fabani, M. M., Polushin, N. N., Silnikov, V., Vlassov, V. V., Bichenkova, E. V., & Аркадьевна, З. М. (2011) · Journal of Nucleic Acids · doi:10.4061/2011/748632 · Cited by 7 · see citing works
Investigation of potential RNA bulge stabilizing elements
Sandbrink, J., Ossipov, D. A., Åström, H., & Strömberg, R. (2005) · Journal of Molecular Recognition · doi:10.1002/jmr.736 · Cited by 7 · see citing works
Oligonucleotide Based Artificial Ribonucleases (OBANs)
Ghidini, A., Murtola, M., & Strömberg, R. (2014) · doi:10.1002/9781118696880.ch3.2 · Cited by 7 · see citing works
Baccolini, G., & Micheletti, G. (2014) · Phosphorus, sulfur, and silicon and the related elements · doi:10.1080/10426507.2014.883625 · Cited by 6 · see citing works
Patutina, O., Chiglintseva, D., Amirloo, B., Clarke, D. J., Gaponova, S., Vlassov, V. V., Bichenkova, E. V., & Аркадьевна, З. М. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126562 · Cited by 6 · see citing works
The Role of Microemulsions in Enhancing the Stability of Biopharmaceuticals
Yu, X., Jin, Y., Sun, J., Jin, M., Bai, S., Zhu, R., Zhang, Y., Lu, Y., Song, J.-Y., & Ma, Y. (2026) · Drug Design Development and Therapy · doi:10.2147/dddt.s551864 · Cited by 5 · see citing works
Computational prediction of nonenzymatic RNA degradation patterns
Rybarczyk, A., Jackowiak, P., Figlerowicz, M., & Błażewicz, J. (2016) · Acta Biochimica Polonica · doi:10.18388/abp.2016_1331 · Cited by 5 · see citing works
Oligonucleotide‐Linked Lipid Nanoparticles as a Versatile mRNA Nanovaccine Platform
Im, S. H., Chung, Y., Duskunovic, N., Choi, H., Park, S., & Chung, H. J. (2024) · Advanced Healthcare Materials · doi:10.1002/adhm.202401868 · Cited by 4 · see citing works
Lönnberg, T. (2006) · Nucleosides Nucleotides & Nucleic Acids · doi:10.1080/15257770500544537 · Cited by 3 · see citing works
The Juxtaposition of Ribose Hydroxyl Groups: The Root of Biological Catalysis and the RNA World?
Bernhardt, H. S. (2015) · Origins of Life and Evolution of Biospheres · doi:10.1007/s11084-015-9403-z · Cited by 3 · see citing works
Vlassov, V. V., & Vlassov, A. V. (2004) · Nucleic acids and molecular biology · doi:10.1007/978-3-642-18510-6_5 · Cited by 3 · see citing works
Site-Specific Artificial Ribonucleases: Conjugates of Oligonucleotides with Catalytic Groups
Аркадьевна, З. М., & Beloglazova, N. G. (2004) · Nucleic acids and molecular biology · doi:10.1007/978-3-642-18510-6_12 · Cited by 2 · see citing works
Nonenzymatic and Metal-Ion-Dependent RNA Cleavage, and RNase Models
Lönnberg, H. (2011) · Nucleic acids and molecular biology · doi:10.1007/978-3-642-21078-5_14 · Cited by 2 · see citing works
Oligonucleotides in Sensing and Diagnostic Applications
Radecka, H., Radecki, J., Ghidini, A., Murtola, M., Strömberg, R., D’Urso, A., Petrovic, A. G., Fragalà, M. E., Tamargo, M. A., Ellestad, G. A., et al. (2015) · Wiley eBooks · doi:10.1002/9781118696880.ch3
Development of oligonucleotide based artificial ribonucleases 2'-O-MeOBAN´s and PNAzymes
Murtola, M. (2009) · Figshare
Jackson, N. A. C. (2022) · RNA technologies · doi:10.1007/978-3-031-08415-7_2
Iqbal, M. O., Bhutta, K. K., Khan, I. A., Rehman, I. U., Khan, M. K., Gu, Y., Chen, J., & Wu, X. (2026) · Drug Design Development and Therapy · doi:10.2147/dddt.s554673
Fine-scale structural information substantially improves mRNA therapeutic stability prediction
Yi, S., Ali, S. E., Jadeja, Y., Davis, J. W., & Metkar, M. (2026) · Molecular Therapy — Nucleic Acids · doi:10.1016/j.omtn.2026.102960
- Authors
- Mikkola, S., Kaukinen, U., & Lönnberg, H.
- Affiliations
- University of Turku (FI)
- Venue
- Cell Biochemistry and Biophysics
- Published
- 2001
- Volume
- 34
- Issue
- 1
- Pages
- 95-119
- ISSN
- 1085-9195 (ISSN-L)
- OpenAlex
- W1980553137
- Cited by
- 67
- References
- 117
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 4 · 2023: 5 · 2022: 8 · 2021: 2 · 2020: 1 · 2019: 2 · 2018: 2 · 2017: 1 · 2016: 1 · 2015: 2 · 2014: 4
- FWCI
- 1.04
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cell Biochemistry and Biophysics (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › DNA and Nucleic Acid Chemistry
- Physical Sciences › Chemistry › Organic Chemistry › Chemical Reaction Mechanisms
- Keywords
- RNA secondary structure, phosphodiester bond cleavage, metal ion catalysis
- MeSH terms
- Base Sequence, Catalysis, Chemistry, Physical, Esterification, Hydrogen-Ion Concentration, Metals, Nucleic Acid Conformation, RNA, RNA, Double-Stranded, RNA, Transfer, RNA, Catalytic, Chemical Phenomena
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review