DNA and RNA ligases: structural variations and shared mechanisms

Current Opinion in Structural Biology

Volumn 18, Issue 1, 2008, Pages 96-105

  Pascal, John M ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; LIGAND; NICOTINAMIDE ADENINE DINUCLEOTIDE; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; RNA;

CHLORELLA; CRYSTAL STRUCTURE; ESCHERICHIA COLI; GENETIC VARIABILITY; LIGASE CHAIN REACTION; NONHUMAN; NUCLEIC ACID STRUCTURE; PRIORITY JOURNAL; REVIEW;

ADENOSINE MONOPHOSPHATE; ANIMALS; CRYSTALLOGRAPHY, X-RAY; DNA LIGASES; ESCHERICHIA COLI PROTEINS; HUMANS; RNA LIGASE (ATP); STRUCTURE-ACTIVITY RELATIONSHIP; SUBSTRATE SPECIFICITY;

EID: 39149142191     PISSN: 0959440X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.sbi.2007.12.008     Document Type: Review

References (36)

1. Lehman I.R. DNA ligase: structure, mechanism, and function. Science 186 (1974) 790-797
2. Shuman S., and Lima C.D. The polynucleotide ligase and RNA capping enzyme superfamily of covalent nucleotidyltransferases. Curr Opin Struct Biol 14 (2004) 757-764
3. Akey D., Martins A., Aniukwu J., Glickman M.S., Shuman S., and Berger J.M. Crystal structure and nonhomologous end-joining function of the ligase component of Mycobacterium DNA ligase D. J Biol Chem 281 (2006) 13412-13423
4. Nishida H., Kiyonari S., Ishino Y., and Morikawa K. The closed structure of an archaeal DNA ligase from Pyrococcus furiosus. J Mol Biol 360 (2006) 956-967
5. Pascal J.M., Tsodikov O.V., Hura G.L., Song W., Cotner E.A., Classen S., Tomkinson A.E., Tainer J.A., and Ellenberger T. A flexible interface between DNA ligase and PCNA supports conformational switching and efficient ligation of DNA. Mol Cell 24 (2006) 279-291
6. Deng J., Schnaufer A., Salavati R., Stuart K.D., and Hol W.G. High resolution crystal structure of a key editosome enzyme from Trypanosoma brucei: RNA editing ligase 1. J Mol Biol 343 (2004) 601-613
7. El Omari K., Ren J., Bird L.E., Bona M.K., Klarmann G., LeGrice S.F., and Stammers D.K. Molecular architecture and ligand recognition determinants for T4 RNA ligase. J Biol Chem 281 (2006) 1573-1579
8. Nandakumar J., Shuman S., and Lima C.D. RNA ligase structures reveal the basis for RNA specificity and conformational changes that drive ligation forward. Cell 127 (2006) 71-84. This paper describes the crystal structure of the ligase-AMP intermediate of bacteriophage T4 RNA ligase 2 (Rnl2) and Rnl2 bound to different RNA/DNA hybrid substrates. The structures reveal several stages of the ligation reaction in the context of one ligase active site, providing unparalleled insights into the subtlety of active site rearrangements that accompany AMP transfer and drive the ligation reaction in the forward direction. The structures demonstrate the physical basis for selecting RNA nucleotides on the 3′ end of the substrate. The structures also revealed the fold of a α-helical C-terminal domain conserved among RNA editing ligases.
9. Srivastava S.K., Tripathi R.P., and Ramachandran R. NAD+-dependent DNA Ligase (Rv3014c) from Mycobacterium tuberculosis. Crystal structure of the adenylation domain and identification of novel inhibitors. J Biol Chem 280 (2005) 30273-30281
10. Pascal J.M., O'Brien P.J., Tomkinson A.E., and Ellenberger T. Human DNA ligase I completely encircles and partially unwinds nicked DNA. Nature 432 (2004) 473-478. The crystal structure of human DNA ligase I provided the first view of a polynucleotide ligase engaging nucleic acid substrate, and the first example of a eukaryotic DNA ligase. The structure demonstrates that the NTase and OB domains, found in all DNA ligases, collaborate to distort the conformation of bound substrate to align the DNA ends for the joining reaction. Structural and biochemical analysis determine the function of the N-terminal DBD conserved among eukaryotic and archaeal DNA ligases. The structure reveals that the domains of LIG1 form a protein clamp that encircles DNA.
11. +-dependent DNA ligase. The structure demonstrates that bacterial ligases LigA form a protein clamp using the C-terminal HhH domain. Comparison to the unliganded crystal structure of T. filiformis ligase illustrates a large-scale re-organization of bacterial ligase domains upon binding to DNA breaks.
12. Nair P.A., Nandakumar J., Smith P., Odell M., Lima C.D., and Shuman S. Structural basis for nick recognition by a minimal pluripotent DNA ligase. Nat Struct Mol Biol 14 (2007) 770-778. This paper describes the crystal structure of the Chlorella ligase-AMP intermediate bound to a phosphorylated DNA substrate, providing the first view of a ligase active site before transferring AMP to DNA. The structure and biochemical analysis reveal that a 'latch' module that protrudes from the OB domain provides DNA-binding affinity and a novel mechanism for forming a protein clamp to encircle DNA breaks.
13. Subramanya H.S., Doherty A.J., Ashford S.R., and Wigley D.B. Crystal structure of an ATP-dependent DNA ligase from bacteriophage T7. Cell 85 (1996) 607-615
14. Odell M., Sriskanda V., Shuman S., and Nikolov D.B. Crystal structure of eukaryotic DNA ligase-adenylate illuminates the mechanism of nick sensing and strand joining. Mol Cell 6 (2000) 1183-1193
15. Lee J.Y., Chang C., Song H.K., Moon J., Yang J.K., Kim H.K., Kwon S.T., and Suh S.W. Crystal structure of NAD(+)-dependent DNA ligase: modular architecture and functional implications. EMBO J 19 (2000) 1119-1129
16. Sriskanda V., and Shuman S. Mutational analysis of Chlorella virus DNA ligase: catalytic roles of domain I and motif VI. Nucleic Acids Res 26 (1998) 4618-4625
17. Mackey Z.B., Niedergang C., Murcia J.M., Leppard J., Au K., Chen J., de Murcia G., and Tomkinson A.E. DNA ligase III is recruited to DNA strand breaks by a zinc finger motif homologous to that of poly(ADP-ribose) polymerase. Identification of two functionally distinct DNA binding regions within DNA ligase III. J Biol Chem 274 (1999) 21679-21687
18. Hakansson K., Doherty A.J., Shuman S., and Wigley D.B. X-ray crystallography reveals a large conformational change during guanyl transfer by mRNA capping enzymes. Cell 89 (1997) 545-553
19. Sriskanda V., and Shuman S. Conserved residues in domain Ia are required for the reaction of Escherichia coli DNA ligase with NAD+. J Biol Chem 277 (2002) 9695-9700
20. Gajiwala K.S., and Pinko C. Structural rearrangement accompanying NAD+ synthesis within a bacterial DNA ligase crystal. Structure 12 (2004) 1449-1459
21. Tomkinson A.E., Vijayakumar S., Pascal J.M., and Ellenberger T. DNA ligases: structure, reaction mechanism, and function. Chem Rev 106 (2006) 687-699
22. Ho C.K., Wang L.K., Lima C.D., and Shuman S. Structure and mechanism of RNA ligase. Structure 12 (2004) 327-339
23. Wang L.K., Nandakumar J., Schwer B., and Shuman S. The C-terminal domain of T4 RNA ligase 1 confers specificity for tRNA repair. RNA 13 (2007) 1235-1244
24. Kodama K., Barnes D.E., and Lindahl T. In vitro mutagenesis and functional expression in Escherichia coli of a cDNA encoding the catalytic domain of human DNA ligase I. Nucleic Acids Res 19 (1991) 6093-6099
25. Tomkinson A.E., Tappe N.J., and Friedberg E.C. DNA ligase I from Saccharomyces cerevisiae: physical and biochemical characterization of the CDC9 gene product. Biochemistry 31 (1992) 11762-11771
26. Grawunder U., Zimmer D., and Leiber M.R. DNA ligase IV binds to XRCC4 via a motif located between rather than within its BRCT domains. Curr Biol 8 (1998) 873-876
27. Kiyonari S., Takayama K., Nishida H., and Ishino Y. Identification of a novel binding motif in Pyrococcus furiosus DNA ligase for the functional interaction with proliferating cell nuclear antigen. J Biol Chem 281 (2006) 28023-28032
28. Jeon H.J., Shin H.J., Choi J.J., Hoe H.S., Kim H.K., Suh S.W., and Kwon S.T. Mutational analyses of the thermostable NAD+-dependent DNA ligase from Thermus filiformis. FEMS Microbiol Lett 237 (2004) 111-118
29. Ho C.K., Van Etten J.L., and Shuman S. Characterization of an ATP-dependent DNA ligase encoded by Chlorella virus PBCV-1. J Virol 71 (1997) 1931-1937
30. Sriskanda V., and Shuman S. Chlorella virus DNA ligase: nick recognition and mutational analysis. Nucleic Acids Res 26 (1998) 525-531
31. Odell M., and Shuman S. Footprinting of Chlorella virus DNA ligase bound at a nick in duplex DNA. J Biol Chem 274 (1999) 14032-14039
32. Sriskanda V., and Shuman S. Specificity and fidelity of strand joining by Chlorella virus DNA ligase. Nucleic Acids Res 26 (1998) 3536-3541
33. Sriskanda V., and Shuman S. Role of nucleotidyltransferase motifs I, III and IV in the catalysis of phosphodiester bond formation by Chlorella virus DNA ligase. Nucleic Acids Res 30 (2002) 903-911
34. Sriskanda V., and Shuman S. Role of nucleotidyl transferase motif V in strand joining by chlorella virus DNA ligase. J Biol Chem 277 (2002) 9661-9667
35. Nandakumar J., and Shuman S. How an RNA ligase discriminates RNA versus DNA damage. Mol Cell 16 (2004) 211-221
36. Pascal J.M., and Ellenberger T. RNA ligase does the AMP shuffle. Nat Struct Mol Biol 13 (2006) 950-951