Kinetic mechanism of nick sealing by T4 RNA ligase 2 and effects of 3′-OH base mispairs and damaged base lesions

RNA

Volumn 19, Issue 12, 2013, Pages 1840-1847

  Chauleau, Mathieu ^a   Shuman, Stewart ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

8 oxoguanine; Abasic lesions; RNA repair; Transient state kinetics

Indexed keywords

8 HYDROXYGUANINE; ADENINE DERIVATIVE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ESTER DERIVATIVE; RIBONUCLEOSIDE; RNA LIGASE; T4 RNA LIGASE 2; UNCLASSIFIED DRUG;

ADENYLATION; ARTICLE; BACTERIOPHAGE T4; BASE MISPAIRING; BASE PAIRING; CATALYSIS; CHEMICAL REACTION KINETICS; CONTROLLED STUDY; COVALENT BOND; DNA DAMAGE; NONHUMAN; PRIORITY JOURNAL; RNA ANALYSIS; RNA SEQUENCE; SINGLE TURNOVER NICK SEALING;

8-OXOGUANINE; ABASIC LESIONS; RNA REPAIR; TRANSIENT STATE KINETICS;

ADENINE; APURINIC ACID; BASE PAIRING; BASE SEQUENCE; ESCHERICHIA COLI; GUANINE; KINETICS; RNA LIGASE (ATP); RNA, DOUBLE-STRANDED; VIRAL PROTEINS;

EID: 84888402585     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.041731.113     Document Type: Article

References (45)

1. Amaro RE, Schnaufer A, Interthal H, Hol W, Stuart KD, McCammon JA. 2008. Discovery of drug-like inhibitors of an essential RNA-editing ligase in Trypanosoma brucei. Proc Natl Acad Sci 105: 17278-17283.
2. Amitsur M, Levitz R, Kaufman G. 1987. Bacteriophage T4 anticodon nuclease, polynucleotide kinase, and RNA ligase reprocess the host lysine tRNA. EMBO J 6: 2499-2503.
3. Barany F. 1991. Genetic disease detection and DNA amplification using cloned thermostable ligase. Proc Natl Acad Sci 88: 189-193.
4. Bhagwat AA, Sanderson RJ, Lindahl T. 1999. Delayed DNA joining at 3′ mismatches by human DNA ligases. Nucleic Acids Res 27: 4028-4033.
5. Blanc V, Alfonzo JD, Aphasizhev R, Simpson L. 1999. The mitochondrial RNA ligase from Leishmania tarentolae can join RNA molecules bridged by a complementary RNA. J Biol Chem 274: 24289-24296.
6. Bullard DR, Bowater RP. 2006. Direct comparison of nick-joining activity of the nucleic acid ligases from bacteriophage T4. Biochem J 398: 135-144.
7. Deng J, Schnaufer A, Salavati R, Stuart KD, Hol WG. 2004. High resolution crystal structure of a key editosome enzyme from Trypanosoma brucei : RNA editing ligase 1. J Mol Biol 343: 601-613.
8. Durrant JD, Hall L, Swift RV, Landon M, Schnaufer A, Amaro RE. 2010. Novel napththalene-based inhibitors of Trypanosoma brucei RNA editing ligase I. PLoS Negl Trop Dis 4: e803.
9. England TE, Uhlenbeck OC. 1978. 3′-Terminal labelling of RNA with T4 RNA ligase. Nature 275: 560-561.
10. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, Terns RM, Terns MP. 2009. RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139: 945-956.
11. Hale CR, Majumdar S, Elmore J, Pfister N, Compton M, Olson S, Resch AM, Glover CVC, Graveley BR, Terns RM, et al. 2012. Essential features and rational design of CRISPR RNAs that function with the Cas RAMP module complex to cleave RNAs. Mol Cell 45: 292-302.
12. Hashimoto K, Tominaga Y, Nakabeppu Y, Moriya M. 2004. Futile short-patch DNA base excision repair of adenine:8-oxoguanine mispair. Nucleic Acids Res 32: 5928-5934.
13. Ho CK, Shuman S. 2002. Bacteriophage T4 RNA ligase 2 (gp24.1) exemplifies a family of RNA ligases found in all phylogenetic domains. Proc Natl Acad Sci 99: 12709-12714.
14. Ho CK, Wang LK, Lima CD, Shuman S. 2004. Structure and mechanism of RNA ligase. Structure 12: 327-339.
15. Husain I, Tomkinson AE, Burkhart WA, Moyer MB, Ramos W, Mackey ZB, Besterman JM, Chen J. 1995. Purification and characterization of DNA ligase III from bovine testes: Homology with DNA ligase II and vaccinia DNA ligase. J Biol Chem 270: 9683-9690.
16. Lamarche BJ, Showalter AK, Tsai MD. 2005. An error-prone viral DNA ligase. Biochemistry 44: 8408-8417.
17. Li J, Chu X, Liu Y, Jiang JH, He Z, Zhang Z, Shen G, Yu RQ. 2005. A colorimetric method for point mutation detection using high-fidelity DNA ligase. Nucleic Acids Res 33: e168.
18. Lohman GS, Chen L, Evans TC. 2011. Kinetic characterization of single strand break ligation in duplex DNA by T4 DNA ligase. J Biol Chem 286: 44187-44196.
19. Luo J, Bergstrom DE, Barany F. 1996. Improving the fidelity of Thermus thermophilus DNA ligase. Nucleic Acids Res 24: 3071-3078.
20. Moshiri H, Acoca S, Kala S, Najafabadi HS, Hogues H, Purisma E, Salavati R. 2011. Naphthalene-based RNA editing inhibitor blocks RNA editing activities and editosome assembly in Trypanosoma brucei. J Biol Chem 286: 14178-14189.
21. Nakatani M, Ezaki S, Atomi H, Imanaka T. 2002. Substrate recognition and fidelity of strand joining by an archaeal DNA ligase. Eur J Biochem 269: 650-656.
22. Nandakumar J, Shuman S. 2004. How an RNA ligase discriminates RNA versus DNA damage. Mol Cell 16: 211-221.
23. Nandakumar J, Shuman S. 2005. Dual mechanisms whereby a broken RNA end assists the catalysis of its repair by T4 RNA ligase 2. J Biol Chem 280: 23484-23489.
24. Nandakumar J, Ho CK, Lima CD, Shuman S. 2004. RNA substrate specificity and structure-guided mutational analysis of bacteriophage T4 RNA ligase 2. J Biol Chem 279: 31337-31347.
25. Nandakumar J, Shuman S, Lima CD. 2006. RNA ligase structures reveal the basis for RNA specificity and conformational changes that drive ligation forward. Cell 127: 71-84.
26. Palazzo SS, PanigrahiAK, IgoRP, Salavati R, Stuart K. 2003. Kinetoplastid RNA editing ligases: Complex association, characterization, and substrate requirements. Mol Biochem Parasitol 127: 161-167.
27. Pfeffer S, Sewer A, Lagos-Quintana M, Sheridan R, Sander C, Grässer FA, van Dyck LF, Ho CK, Shuman S, Chien M, et al. 2005. Identification of microRNAs of the herpesvirus family. Nat Methods 2: 269-276.
28. Samai P, Shuman S. 2011a. Functional dissection of the DNA interface of the nucleotidyl transferase domain of Chlorella virus DNA ligase. J Biol Chem 286: 13314-13326.
29. Samai P, Shuman S. 2011b. Structure-function analysis of the OB and latch domains of Chlorella virus DNA ligase. J Biol Chem 286: 22642-22652.
30. Samai P, Shuman S. 2012. Kinetic analysis of DNA strand joining by Chlorella virus DNA ligase and the role of nucleotidyltransferase motif VI in ligase adenylylation. J Biol Chem 287: 28609-28618.
31. Schnaufer A, Panigrahi AK, Panicucci B, Igo RP, Salavati R, Stuart K. 2001. An RNA ligase essential for RNA editing and survival of the bloodstream form of Tryanosoma brucei. Science 291: 2159-2162.
32. Shuman S. 1995. Vaccinia virus DNA ligase: Specificity, fidelity, and inhibition. Biochemistry 34: 16138-16147.
33. Silber R, Malathi VG, Hurwitz J. 1972. Purification and properties of bacteriophage T4-induced RNA ligase. Proc Natl Acad Sci 69: 3009-3013.
34. Sriskanda V, Shuman S. 1998. Specificity and fidelity of strand joining by Chlorella virus DNA ligase. Nucleic Acids Res 26: 3536-3541.
35. Taylor MR, Conrad JA, Wahl D, O'Brien PJ. 2011. Kinetic mechanism of human DNA ligase I reveals magnesium-dependent changes in the rate-limiting step that compromise ligation efficiency. J Biol Chem 286: 23054-23062.
36. Tomkinson AE, Tappe NJ, Friedberg EC. 1992. DNA ligase I from Saccharomyces cerevisiae: Physical and biochemical characterization of the CDC9 gene product. Biochemistry 31: 11762-11771.
37. +-dependent DNA ligase from the hypethermophile Aquifex aeolicus. Nucleic Acids Res 28: 1447-1454.
38. Viollet S, Fuchs RT, Munafo DB, Zhuang F, Robb G. 2011. T4 RNA ligase 2 truncated active site mutants: Improved tools for RNA analysis. BMC Biotechnol 11: 72.
39. Wang Y, Lamarche BJ, Tsai MD. 2007a. Human DNA ligase IV and the ligase IV/XRCC4 complex: Analysis of nick ligation fidelity. Biochemistry 46: 4962-4976.
40. Wang LK, Nandakumar J, Schwer B, Shuman S. 2007b. The C-terminal domain of T4 RNA ligase 1 confers specificity for tRNA repair. RNA 13: 1235-1244.
41. Wang Y, Juranek S, Li H, Sheng G, Tuschl T, Patel DJ. 2008. Structure of an Argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456: 921-926.
42. Wurtmann EJ, Wolin SL. 2009. RNA under attack: Cellular handling of RNA damage. Crit Rev Biochem Mol Biol 44: 34-49.
43. Yin S, Ho CK, Shuman S. 2003. Structure-function analysis of T4 RNA ligase 2. J Biol Chem 278: 17601-17608.
44. Yuan YR, Pei Y, Ma JB, Kuryavyi V, Zhadina M, Meister G, Chen HY, Dauter Z, Tuschl T, Patel DJ. 2005. Crystal structure of A. aeolicus Argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol Cell 19: 405-419.
45. Zhao X, Muller JG, Halasyam M, David SS, Burrows CJ. 2007. In vitro ligation of oligodeoxynucleotide containing C8-oxidized purine lesions using bacteriophage T4 DNA ligase. Biochemistry 46: 3734-3744.