Generation and selection of ribozyme variants with potential application in protein engineering and synthetic biology

Applied Microbiology and Biotechnology

Volumn 98, Issue 8, 2014, Pages 3389-3399

  Balke, Darko ^a   Wichert, Claudia ^a   Appel, Bettina ^a   Müller, Sabine ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

DNAzyme; Gene expression; Peptide synthesis; Regulation; Ribozyme

Indexed keywords

BIOSYNTHESIS; CATALYSTS; GENE EXPRESSION; PROTEINS;

DNAZYME; FUNCTIONAL MECHANISMS; FUNCTIONAL NUCLEIC ACIDS; INTRACELLULAR CONTROL; NATURALLY OCCURRING; PEPTIDE SYNTHESIS; REGULATION; RIBOZYMES;

RNA;

APTAMER; DNAZYME; FLEXIZYME; HAMMERHEAD RIBOZYME; RIBOZYME; UNCLASSIFIED DRUG;

AMINOACYLATION; CATALYST; GENE EXPRESSION; GENETIC ANALYSIS; HUMAN; NONHUMAN; PEPTIDE SYNTHESIS; PROTEIN ENGINEERING; PROTEIN MODIFICATION; REPORTER GENE; REVIEW; SCREENING; SYNTHETIC BIOLOGY; BIOTECHNOLOGY; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; PROCEDURES;

BIOTECHNOLOGY; PROTEIN ENGINEERING; RNA, CATALYTIC; SYNTHETIC BIOLOGY;

EID: 84898874449     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-5528-7     Document Type: Review

References (88)

1. Bessho Y, Hodgson DR, Suga H (2002) A tRNA aminoacylation system for non-natural amino acids based on a programmable ribozyme. Nat Biotechnol 20(7):723-728. doi: 10.1038/nbt0702-723
2. Bramlage B, Luzi E, Eckstein F (1998) Designing ribozymes for the inhibition of gene expression. Trends Biotechnol 16(10):434-438
3. Brandsen BM, Hesser AR, Castner MA, Chandra M, Silverman SK (2013) DNA-catalyzed hydrolysis of esters and aromatic amides. J Am Chem Soc 135:16014-16017. doi: 10.1021/ja4077233
4. Breaker RR (2012) Riboswitches and the RNA world. Cold Spring Harbor Perspectives in Biology 4(2):a003566. doi: 10.1101/cshperspect.a003566
5. Breaker RR, Joyce GF (1994) A DNA enzyme that cleaves RNA. Chem Biol 1(4):223-229
6. Büttner L, Seikowski J, Wawrzyniak K, Ochmann A, Hobartner C (2013) Synthesis of spin-labeled riboswitch RNAs using convertible nucleosides and DNA-catalyzed RNA ligation. Bioorg Med Chem 21(20):6171-6180. doi: 10.1016/j.bmc.2013.04.007
7. Chandrasekar J, Silverman SK (2013) Catalytic DNA with phosphatase activity. Proc Natl Acad Sci U S A 110(14):5315-5320. doi: 10.1073/pnas. 1221946110
8. Chen YY, Jensen MC, Smolke CD (2010) Genetic control of mammalian T-cell proliferation with synthetic RNA regulatory systems. Proc Natl Acad Sci U S A 107(19):8531-8536. doi: 10.1073/pnas.1001721107
9. Cho EJ, Lee J-W, Rajendran M, Ellington AD (2008) Nucleic acids for reagentless biosensors. In: Ligler FS, Taitt CR (eds) Optical biosensors, 2nd edn. Elsevier, Amsterdam, pp 493-541. doi: 10.1016/B978-044453125-4.50015-2
10. Chumachenko NV, Novikov Y, Yarus M (2009) Rapid and simple ribozymic aminoacylation using three conserved nucleotides. J Am Chem Soc 131(14):5257-5263. doi: 10.1021/ja809419f
11. Coppins RL, Silverman SK (2004) A DNA enzyme that mimics the first step of RNA splicing. Nat Struct Mol Biol 11(3):270-274. doi: 10.1038/nsmb727
12. Drude I, Vauléon S, Müller S (2007) Twin ribozyme mediated removal of nucleotides from an internal RNA site. Biochem Biophys Res Commun 363(1):24-29. doi: 10.1016/j.bbrc.2007.08.135
13. Fujita Y, Ishikawa J, Furuta H, Ikawa Y (2010) Generation and development of RNA ligase ribozymes with modular architecture through "design and selection". Molecules 15(9):5850-5865. doi: 10.3390/molecules15095850
14. Fusz S, Eisenfuhr A, Srivatsan SG, Heckel A, Famulok M (2005) A ribozyme for the aldol reaction. Chem Biol 12(8):941-950. doi: 10.1016/j.chembiol.2005. 06.008
15. Goto Y, Suga H (2012) Flexizymes as a tRNA acylation tool facilitating genetic code reprogramming. Methods Mol Biol 848:465-478. doi: 10.1007/978-1-61779-545-9-29
16. Goto Y, Murakami H, Suga H (2008a) Initiating translation with D-amino acids. RNA 14(7):1390-1398. doi: 10.1261/rna.1020708
17. Goto Y, Ohta A, Sako Y, Yamagishi Y, Murakami H, Suga H (2008b) Reprogramming the translation initiation for the synthesis of physiologically stable cyclic peptides. ACS Chem Biol 3(2):120-129. doi: 10.1021/cb700233t
18. Gredell JA, Frei CS, Cirino PC (2012) Protein and RNA engineering to customize microbial molecular reporting. Biotechnol J 7(4):477-499. doi: 10.1002/biot.201100266
19. Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35(3 Pt 2):849-857
20. Harris ME (2008) Catalytic Modes in Natural Ribozymes. Wiley Encyclopedia of Chemical Biology. John Wiley & Sons, Inc., 1-11. doi: 10.1002/9780470048672.wecb640
21. Hartig JS, Najafi-Shoushtari SH, Grune I, Yan A, Ellington AD, Famulok M (2002) Protein-dependent ribozymes report molecular interactions in real time. Nat Biotechnol 20(7):717-722. doi: 10.1038/nbt0702-717
22. Hausch F, Jäschke A (1997) Libraries of multifunctional RNA conjugates for the selection of new RNA catalysts. Bioconjugate Chem 8(6):885-890. doi: 10.1021/bc9701151
23. Illangasekare M, Yarus M (1999) A tiny RNA that catalyzes both aminoacyl-RNA and peptidyl-RNA synthesis. RNA 5(11):1482-1489
24. Illangasekare M, Sanchez G, Nickles T, Yarus M (1995) Aminoacyl-RNA synthesis catalyzed by an RNA. Science 267(5198):643-647
25. Jenne A, Famulok M (1998) A novel ribozyme with ester transferase activity. Chem Biol 5(1):23-34
26. Kawakami T, Aimoto S (2007) Peptide ligation using a building block having a cysteinyl prolyl ester (CPE) autoactivating unit at the carboxy terminus. Chem Lett 36(1):76-77. doi: 10.1246/Cl.2007.76
27. Kawakami T, Murakami H, Suga H (2008a) Messenger RNA-programmed incorporation of multiple N-methyl-amino acids into linear and cyclic peptides. Chem Biol 15(1):32-42. doi: 10.1016/j.chembiol.2007.12.008
28. Kawakami T, Murakami H, Suga H (2008b) Ribosomal synthesis of polypeptoids and peptoid-peptide hybrids. J Am Chem Soc 130(50):16861-16863. doi: 10.1021/ja806998v
29. Kawakami T, Ohta A, Ohuchi M, Ashigai H, Murakami H, Suga H (2009) Diverse backbone-cyclized peptides via codon reprogramming. Nat Chem Biol 5(12):888-890. doi: 10.1038/nchembio.259
30. Ketzer P, Haas SF, Engelhardt S, Hartig JS, Nettelbeck DM (2012) Synthetic riboswitches for external regulation of genes transferred by replication-deficient and oncolytic adenoviruses. Nucleic Acids Res 40(21):e167. doi: 10.1093/nar/gks734
31. Khvorova A, Lescoute A, Westhof E, Jayasena SD (2003) Sequence elements outside the hammerhead ribozyme catalytic core enable intracellular activity. Nat Struct Biol 10(9):708-712. doi: 10.1038/nsb959
32. Klauser B, Hartig JS (2013) An engineered small RNA-mediated genetic switch based on a ribozyme expression platform. Nucleic Acids Res 41(10):5542-5552. doi: 10.1093/nar/gkt253
33. Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR (1982) Self-splicing RNA: autoexcision and autocyclization of the ribosomal RNA intervening sequence of Tetrahymena. Cell 31(1):147-157
34. Lad C, Williams NH, Wolfenden R (2003) The rate of hydrolysis of phosphomonoester dianions and the exceptional catalytic proficiencies of protein and inositol phosphatases. Proc Natl Acad Sci U S A 100(10):5607-5610. doi: 10.1073/pnas.0631607100
35. Lee N, Suga H (2001) A minihelix-loop RNA acts as a trans-aminoacylation catalyst. RNA 7(7):1043-1051
36. Lee N, Bessho Y, Wei K, Szostak JW, Suga H (2000) Ribozyme-catalyzed tRNA aminoacylation. Nat Struct Biol 7(1):28-33. doi: 10.1038/71225
37. Lee J, Lin L, Li Y (2011) Functional nucleic acids for fluorescence-based biosensing applications. In: Demchenko AP (ed) Advanced fluorescence reporters in chemistry and biology III, vol 113. Springer Series on Fluorescence, 221, p 201. doi: 10.1007/978-3-642-18035-4-6
38. Lewin AS (2010) Regulatory RNA in gene therapy. In: Herzog RW, Zolotukhin S (ed) A guide to human gene therapy. World Scientific Publishing Co Pte Ltd, Singapore, pp 103-122
39. Link KH, Breaker RR (2009) In vitro selection of glmS ribozymes. Methods Mol Biol 540:349-364. doi: 10.1007/978-1-59745-558-9-25
40. Lohse PA, Szostak JW (1996) Ribozyme-catalysed amino-acid transfer reactions. Nature 381(6581):442-444. doi: 10.1038/381442a0
41. Meyer AJ, Ellefson JW, Ellington AD (2012) Abiotic self-replication. Acc Chem Res 45(12):2097-2105. doi: 10.1021/ar200325v
42. Michener JK, Smolke CD (2012) High-throughput enzyme evolution in Saccharomyces cerevisiae using a synthetic RNA switch. Metab Eng 14(4):306-316. doi: 10.1016/j.ymben.2012.04.004
43. Min D-H, Kim D-E (2012) Suppression of hepatitis C viral genome replication with RNA-cleaving deoxyribozyme. In: Erdmann VA, Barciszewski J (eds) From nucleic acids sequences to molecular medicine. RNA Technologies, Springer Berlin Heidelberg, pp 429-452. doi: 10.1007/978-3-642-27426-8-17
44. Morimoto J, Hayashi Y, Iwasaki K, Suga H (2011) Flexizymes: their evolutionary history and the origin of catalytic function. Acc Chem Res 44(12):1359-1368. doi: 10.1021/ar2000953
45. Müller S, Strohbach D, Wolf J (2006) Sensors made of RNA: tailored ribozymes for detection of small organic molecules, metals, nucleic acids and proteins. IEE Proc Nanobiotechnology 153(2):31-40. doi: 10.1049/ip-nbt:20050047
46. Murakami H, Kourouklis D, Suga H (2003a) Using a solid-phase ribozyme aminoacylation system to reprogram the genetic code. Chem Biol 10(11):1077-1084
47. Murakami H, Saito H, Suga H (2003b) A versatile tRNA aminoacylation catalyst based on RNA. Chem Biol 10(7):655-662
48. Murakami H, Ohta A, Ashigai H, Suga H (2006) A highly flexible tRNA acylation method for non-natural polypeptide synthesis. Nat Methods 3(5):357-359. doi: 10.1038/nmeth877
49. Nagraj N, Lu Y (2011) Catalytic nucleic acid biosensors for environmental monitoring. In: Mascini M, Palchetti I (eds) Nucleic acid biosensors for environmental pollution monitoring. The Royal Society of Chemistry, Cambridge, pp 82-98
50. Niwa N, Yamagishi Y, Murakami H, Suga H (2009) A flexizyme that selectively charges amino acids activated by a water-friendly leaving group. Bioorg Med Chem Lett 19(14):3892-3894. doi: 10.1016/j.bmcl.2009.03.114
51. Nomura Y, Zhou L, Miu A, Yokobayashi Y (2013) Controlling mammalian gene expression by allosteric hepatitis delta virus ribozymes. ACS Synth Biol 2(12):684-689. doi: 10.1021/sb400037a
52. Ohta A, Murakami H, Higashimura E, Suga H (2007) Synthesis of polyester by means of genetic code reprogramming. Chem Biol 14(12):1315-1322. doi: 10.1016/j.chembiol.2007.10.015
53. Piganeau N, Jenne A, Thuillier V, Famulok M (2000) An allosteric ribozyme regulated by doxycyline. Angew Chem, Int Ed 39(23):4369-4373. doi: 10.1002/1521-3773(20001201)39:23<4369::aid-anie4369>3.0.co;2-n
54. Pradeepkumar PI, Höbartner C, Baum DA, Silverman SK (2008) DNA-catalyzed formation of nucleopeptide linkages. Angew Chem, Int Ed 47(9):1753-1757. doi: 10.1002/anie.200703676
55. Prudent JR, Uno T, Schultz PG (1994) Expanding the scope of RNA catalysis. Science 264(5167):1924-1927
56. Puttaraju M, Jamison SF, Mansfield SG, Garcia-Blanco MA, Mitchell LG (1999) Spliceosome-mediated RNA trans-splicing as a tool for gene therapy. Nat Biotechnol 17(3):246-252. doi: 10.1038/6986
57. Ramaswamy K, Saito H, Murakami H, Shiba K, Suga H (2004) Designer ribozymes: programming the tRNA specificity into flexizyme. J Am Chem Soc 126(37):11454-11455. doi: 10.1021/ja046843y
58. Sachdeva A, Chandra M, Chandrasekar J, Silverman SK (2012) Covalent tagging of phosphorylated peptides by phosphate-specific deoxyribozymes. ChemBioChem 13(5):654-657. doi: 10.1002/cbic.201200048
59. Saito H, Suga H (2001) A ribozyme exclusively aminoacylates the 3'-hydroxyl group of the tRNA terminal adenosine. J Am Chem Soc 123(29):7178-7179
60. Saito H, Suga H (2002) Outersphere and innersphere coordinated metal ions in an aminoacyl-tRNA synthetase ribozyme. Nucleic Acids Res 30(23):5151-5159
61. Saito H, Kourouklis D, Suga H (2001a) An in vitro evolved precursor tRNA with aminoacylation activity. EMBO J 20(7):1797-1806. doi: 10.1093/emboj/20.7. 1797
62. Saito H, Watanabe K, Suga H (2001b) Concurrent molecular recognition of the amino acid and tRNA by a ribozyme. RNA 7(12):1867-1878
63. Santoro SW, Joyce GF (1997) A general purpose RNA-cleaving DNA enzyme. Proc Natl Acad Sci U S A 94(9):4262-4266
64. Saragliadis A, Hartig JS (2013) Ribozyme-based transfer RNA switches for post-transcriptional control of amino acid identity in protein synthesis. J Am Chem Soc 135(22):8222-8226. doi: 10.1021/Ja311107p
65. Schlosser K, Li YF (2010) A versatile endoribonuclease mimic made of DNA: characteristics and applications of the 8-17 RNA-cleaving DNAzyme. ChemBioChem 11(7):866-879. doi: 10.1002/Cbic.200900786
66. Schroeder GK, Lad C, Wyman P, Williams NH, Wolfenden R (2006) The time required for water attack at the phosphorus atom of simple phosphodiesters and of DNA. Proc Natl Acad Sci U S A 103(11):4052-4055. doi: 10.1073/pnas.0510879103
67. Sengle G, Eisenfuhr A, Arora PS, Nowick JS, Famulok M (2001) Novel RNA catalysts for the Michael reaction. Chem Biol 8(5):459-473
68. Shimizu Y, Inoue A, Tomari Y, Suzuki T, Yokogawa T, Nishikawa K, Ueda T (2001) Cell-free translation reconstituted with purified components. Nat Biotechnol 19(8):751-755. doi: 10.1038/90802
69. Soukup GA, Breaker RR (1999) Engineering precision RNA molecular switches. Proc Natl Acad Sci U S A 96(7):3584-3589
70. Soukup GA, Breaker RR (2000) Allosteric nucleic acid catalysts. Curr Opin Struct Biol 10(3):318-325. doi: 10.1016/S0959-440X(00)00090-7
71. Suga H, Hayashi G, Terasaka N (2011) The RNA origin of transfer RNA aminoacylation and beyond. Philosophical transactions of the Royal Society of London Series B. Biol Sci 366(1580):2959-2964. doi: 10.1098/rstb.2011.0137
72. Sullenger BA (2003) Targeted genetic repair: an emerging approach to genetic therapy. J Clin Invest 112(3):310-311. doi: 10.1172/JCI19419
73. Sullenger BA, Cech TR (1994) Ribozyme-mediated repair of defective mRNA by targeted, trans-splicing. Nature 371(6498):619-622. doi: 10.1038/371619a0
74. Szostak J (2012) The eightfold path to non-enzymatic RNA replication. J Syst Chem 3(1):2. doi: 10.1186/1759-2208-3-2
75. Turk RM, Chumachenko NV, Yarus M (2010) Multiple translational products from a five-nucleotide ribozyme. Proc Natl Acad Sci U S A 107(10):4585-4589. doi: 10.1073/pnas.0912895107
76. Turk RM, Illangasekare M, Yarus M (2011) Catalyzed and spontaneous reactions on ribozyme ribose. J Am Chem Soc 133(15):6044-6050. doi: 10.1021/ja200275h
77. Vauléon S, Ivanov SA, Gwiazda S, Müller S (2005) Site-specific fluorescent and affinity labelling of RNA by using a small engineered twin ribozyme. ChemBioChem 6(12):2158-2162. doi: 10.1002/cbic. 200500215
78. Walsh SM, Sachdeva A, Silverman SK (2013) DNA catalysts with tyrosine kinase activity. J Am Chem Soc 135(40):14928-14931. doi: 10.1021/ja407586u
79. Welz R, Bossmann K, Klug C, Schmidt C, Fritz HJ, Müller S (2003) Site-directed alteration of RNA sequence mediated by an engineered twin ribozyme. Angew Chem, Int Ed 42(21):2424-2427. doi: 10.1002/anie.200250611
80. Wiegand TW, Janssen RC, Eaton BE (1997) Selection of RNA amide synthases. Chem Biol 4(9):675-683
81. Wieland M, Hartig JS (2008) Improved aptazyme design and in vivo screening enable riboswitching in bacteria. Angew Chem, Int Ed 47(14):2604-2607. doi: 10.1002/anie.200703700
82. Wilson C, Szostak JW (1995) In vitro evolution of a self-alkylating ribozyme. Nature 374(6525):777-782. doi: 10.1038/374777a0
83. Win MN, Smolke CD (2007) A modular and extensible RNA-based gene-regulatory platform for engineering cellular function. Proc Natl Acad Sci U S A 104(36):14283-14288. doi: 10.1073/pnas.0703961104
84. Win MN, Smolke CD (2008) Higher-order cellular information processing with synthetic RNA devices. Science 322(5900):456-460. doi: 10.1126/science. 1160311
85. Wittmann A, Suess B (2011) Selection of tetracycline inducible self-cleaving ribozymes as synthetic devices for gene regulation in yeast. Mol Biosyst 7(8):2419-2427. doi: 10.1039/c1mb05070b
86. Wong OY, Pradeepkumar PI, Silverman SK (2011) DNA-catalyzed covalent modification of amino acid side chains in tethered and free peptide substrates. Biochemistry 50(21):4741-4749. doi: 10.1021/bi200585n
87. Yamagishi Y, Shoji I, Miyagawa S, Kawakami T, Katoh T, Goto Y, Suga H (2011) Natural product-like macrocyclic N-methyl-peptide inhibitors against a ubiquitin ligase uncovered from a ribosome-expressed de novo library. Chem Biol 18(12):1562-1570. doi: 10.1016/j.chembiol.2011.09.013
88. Yen L, Svendsen J, Lee JS, Gray JT, Magnier M, Baba T, D'Amato RJ, Mulligan RC (2004) Exogenous control of mammalian gene expression through modulation of RNA self-cleavage. Nature 431(7007):471-476. doi: 10.1038/nature02844