Goldilocks and RNA: where Mg2+ concentration is just right.
Journal
Nucleic acids research
ISSN: 1362-4962
Titre abrégé: Nucleic Acids Res
Pays: England
ID NLM: 0411011
Informations de publication
Date de publication:
08 05 2023
08 05 2023
Historique:
accepted:
28
03
2023
revised:
08
02
2023
received:
28
09
2022
medline:
9
5
2023
pubmed:
30
3
2023
entrez:
29
3
2023
Statut:
ppublish
Résumé
Magnesium, the most abundant divalent cation in cells, catalyzes RNA cleavage but also promotes RNA folding. Because folding can protect RNA from cleavage, we predicted a 'Goldilocks landscape', with local maximum in RNA lifetime at Mg2+ concentrations required for folding. Here, we use simulation and experiment to discover an innate and sophisticated mechanism of control of RNA lifetime. By simulation we characterized RNA Goldilocks landscapes and their dependence on cleavage and folding parameters. Experiments with yeast tRNAPhe and the Tetrahymena ribozyme P4-P6 domain show that structured RNAs can inhabit Goldilocks peaks. The Goldilocks peaks are tunable by differences in folded and unfolded cleavage rate constants, Mg2+ binding cooperativity, and Mg2+ affinity. Different folding and cleavage parameters produce Goldilocks landscapes with a variety of features. Goldilocks behavior allows ultrafine control of RNA chemical lifetime, whereas non-folding RNAs do not display Goldilocks peaks of protection. In sum, the effects of Mg2+ on RNA persistence are expected to be pleomorphic, both protecting and degrading RNA. In evolutionary context, Goldilocks behavior may have been a selectable trait of RNA in an early Earth environment containing Mg2+ and other metals.
Identifiants
pubmed: 36987860
pii: 7092924
doi: 10.1093/nar/gkad124
pmc: PMC10164553
doi:
Substances chimiques
RNA
63231-63-0
Magnesium
I38ZP9992A
RNA, Catalytic
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3529-3539Informations de copyright
© The Author(s) 2023. Published by Oxford University Press on behalf of Nucleic Acids Research.
Références
Proc Natl Acad Sci U S A. 1991 May 15;88(10):4080-3
pubmed: 1709734
Nucleic Acids Res. 1981 May 25;9(10):2411-20
pubmed: 7019856
J Mol Biol. 2005 Nov 25;354(2):483-96
pubmed: 16242711
Nat Chem Biol. 2007 Nov;3(11):693-4
pubmed: 17948016
Biochemistry. 1972 Nov 7;11(23):4358-68
pubmed: 4562590
Biochemistry. 1976 Jan 13;15(1):141-6
pubmed: 1247501
Biophys Chem. 1976 Jul;4(4):383-94
pubmed: 953154
Nat Commun. 2020 Jun 19;11(1):3137
pubmed: 32561731
Ann N Y Acad Sci. 1969 Aug 15;162(2):717-26
pubmed: 4242156
Biochim Biophys Acta. 1997 Jan 31;1323(2):310-8
pubmed: 9042353
J Am Chem Soc. 1996 Apr 10;118(14):3340-4
pubmed: 11539268
Biochemistry. 2000 Oct 10;39(40):12465-75
pubmed: 11015228
Biochemistry. 1999 Dec 21;38(51):16831-9
pubmed: 10606516
Annu Rev Biophys Biomol Struct. 2005;34:221-43
pubmed: 15869389
PLoS One. 2012;7(5):e38024
pubmed: 22701543
RNA. 2005 Sep;11(9):1348-54
pubmed: 16043496
Biochemistry. 1972 Aug 15;11(17):3248-56
pubmed: 4558706
Biochemistry. 2001 Jun 5;40(22):6688-98
pubmed: 11380264
J Mol Biol. 1978 Jul 15;122(4):447-64
pubmed: 691049
Curr Opin Struct Biol. 2012 Jun;22(3):262-72
pubmed: 22595008
J Biol Chem. 1966 Dec 25;241(24):5936-40
pubmed: 5954370
Eur J Cell Biol. 1997 Nov;74(3):281-8
pubmed: 9402476
Biophys J. 2012 Feb 8;102(3):L11-3
pubmed: 22325296
Mol Syst Biol. 2015 Jan 12;11(1):781
pubmed: 25583150
Cell. 2014 Feb 13;156(4):812-24
pubmed: 24529382
Nat Struct Biol. 1997 Jul;4(7):553-8
pubmed: 9228948
Proc Natl Acad Sci U S A. 2018 Nov 27;115(48):12164-12169
pubmed: 30413624
J Mol Biol. 1998 Jan 16;275(2):211-20
pubmed: 9466904
J Mol Evol. 2018 Dec;86(9):598-610
pubmed: 30456440
J Bacteriol. 1980 Nov;144(2):661-5
pubmed: 7430066
Biochemistry. 2000 Sep 12;39(36):11107-13
pubmed: 10998249
Mol Cell Biol. 1999 Jun;19(6):3989-97
pubmed: 10330139
Proc Natl Acad Sci U S A. 2022 Jun 21;119(25):e2201237119
pubmed: 35696576
Nucleic Acids Res. 2020 Sep 4;48(15):8663-8674
pubmed: 32663277
Biochemistry. 1986 Oct 21;25(21):6365-71
pubmed: 3539189
Proc Natl Acad Sci U S A. 1999 May 25;96(11):6149-54
pubmed: 10339556
Science. 1974 Aug 2;185(4149):435-40
pubmed: 4601792
FEBS Lett. 1995 Jan 9;357(3):287-9
pubmed: 7835429
RNA. 1996 Jun;2(6):564-73
pubmed: 8718685
Biochemistry. 2001 Mar 27;40(12):3629-38
pubmed: 11297430
Biochemistry. 1982 Jan 5;21(1):49-53
pubmed: 6916606
Proc Natl Acad Sci U S A. 2005 Jul 26;102(30):10505-10
pubmed: 16024731
Mol Cell. 2012 Nov 9;48(3):409-21
pubmed: 23000176
Q Rev Biophys. 2016 Jan;49:e10
pubmed: 27658939
Cell. 2014 Dec 18;159(7):1698-710
pubmed: 25497548
Biochemistry. 2010 Mar 9;49(9):1843-53
pubmed: 20112919
Eur J Biochem. 1988 Apr 5;173(1):233-9
pubmed: 3281833
Biochemistry. 1990 Mar 13;29(10):2515-23
pubmed: 2334679
Proc Natl Acad Sci U S A. 2016 Aug 23;113(34):E4956-65
pubmed: 27493222
Methods Enzymol. 2009;468:91-106
pubmed: 20946766
Biochemistry. 1998 Nov 17;37(46):16349-59
pubmed: 9819227
Biophys J. 2006 Jan 1;90(1):250-60
pubmed: 16214869
J Mol Biol. 2001 May 25;309(1):57-68
pubmed: 11491301
J Mol Biol. 1976 Apr 5;102(2):193-203
pubmed: 775102
RNA. 2001 Feb;7(2):161-6
pubmed: 11233973
Int J Biochem. 1992 Mar;24(3):493-7
pubmed: 1551462
Biochemistry. 1984 Nov 6;23(23):5414-20
pubmed: 6210103
J Biol Chem. 1967 Apr 25;242(8):1970-3
pubmed: 6024784
Biochemistry. 1999 Oct 26;38(43):14224-37
pubmed: 10571996
Biochemistry. 1982 Apr 27;21(9):2118-27
pubmed: 7046795
Res Microbiol. 2006 Sep;157(7):625-8
pubmed: 16814992
Cell. 1975 Jan;4(1):69-75
pubmed: 1078787
Mol Biosyst. 2016 Jan;12(1):12-7
pubmed: 26549858
RNA. 1999 Oct;5(10):1308-25
pubmed: 10573122
Arch Biochem Biophys. 2011 Aug 1;512(1):1-23
pubmed: 21640700
J Mol Biol. 2007 Sep 28;372(4):942-957
pubmed: 17707400
Annu Rev Biophys Biomol Struct. 1997;26:113-37
pubmed: 9241415
Elife. 2018 Sep 07;7:
pubmed: 30192227
Mol Genet Genomics. 2003 Aug;269(5):706-14
pubmed: 12884008
Science. 1998 Mar 20;279(5358):1940-3
pubmed: 9506944
Biochemistry. 1997 May 20;36(20):6090-9
pubmed: 9166779
Curr Protoc Nucleic Acid Chem. 2001 May;Chapter 11:Unit 11.5
pubmed: 18428831
J Biol Chem. 1971 Jan 10;246(1):110-7
pubmed: 5100278
Nature. 1993 Apr 22;362(6422):709-15
pubmed: 8469282
J Mol Biol. 2018 Feb 16;430(4):509-523
pubmed: 29128594