Structure-specific nuclease activity of RAGs is modulated by sequence, length and phase position of flanking double-stranded DNA

FEBS Journal

Volumn 282, Issue 1, 2015, Pages 4-18

  Kumari, Rupa ^a   Raghavan, Sathees C ^a  

^a INDIAN INSTITUTE OF SCIENCE   (India)

Author keywords

chromosomal translocation; double strand break repair; genomic instability; heteroduplex DNA; non B DNA structure; RAG cleavage

Indexed keywords

DOUBLE STRANDED DNA; HETERODUPLEX; RAG1 PROTEIN; RAG2 PROTEIN; DEOXYRIBONUCLEASE; DNA BINDING PROTEIN; HOMEODOMAIN PROTEIN; NUCLEAR PROTEIN; RAG-1 PROTEIN; RAG2 PROTEIN, HUMAN; RECOMBINANT PROTEIN;

CONTROLLED STUDY; DNA FLANKING REGION; DNA SEQUENCE; DOWN REGULATION; EMBRYO; HUMAN; HUMAN CELL; INCUBATION TIME; MOLECULAR WEIGHT; PROTEIN CLEAVAGE; PROTEIN DNA BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; REVIEW; STRUCTURE ANALYSIS; UPREGULATION; BINDING SITE; CHEMISTRY; CONFORMATION; GENE; GENETICS; HEK293 CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE; VDJ RECOMBINATION;

5' FLANKING REGION; BASE SEQUENCE; BINDING SITES; DEOXYRIBONUCLEASES; DNA-BINDING PROTEINS; GENES, RAG-1; HEK293 CELLS; HOMEODOMAIN PROTEINS; HUMANS; NUCLEAR PROTEINS; NUCLEIC ACID CONFORMATION; NUCLEIC ACID HETERODUPLEXES; RECOMBINANT PROTEINS; V(D)J RECOMBINATION;

EID: 84920815147     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13121     Document Type: Review

References (34)

1. Fugmann SD, Lee AI, Shockett PE, Villey IJ, &, Schatz DG, (2000) The RAG proteins and V(D)J recombination: complexes, ends, and transposition. Annu Rev Immunol 18, 495-527.
2. Lewis SM, (1994) The mechanism of V(D)J joining: lessons from molecular, immunological, and comparative analyses. Adv Immunol 56, 27-150.
3. Nishana M, &, Raghavan SC, (2012) Role of recombination activating genes in the generation of antigen receptor diversity and beyond. Immunology 137, 271-281.
4. Swanson PC, (2004) The bounty of RAGs: recombination signal complexes and reaction outcomes. Immunol Rev 200, 90-114.
5. Gellert M, (1992) Molecular analysis of V(D)J recombination. Annu Rev Genet 26, 425-446.
6. Nambiar M, Kari V, &, Raghavan SC, (2008) Chromosomal translocations in cancer. Biochim Biophys Acta 1786, 139-152.
7. Lieber MR, Raghavan SC, &, Yu K, (2008) Mechanistic aspects of lymphoid chromosomal translocations. J Natl Cancer Inst Monogr, 39, 8-11.
8. Lu CP, Posey JE, &, Roth DB, (2008) Understanding how the V(D)J recombinase catalyzes transesterification: distinctions between DNA cleavage and transposition. Nucleic Acids Res 36, 2864-2873.
9. Nambiar M, &, Raghavan SC, (2011) How does DNA break during chromosomal translocations? Nucleic Acids Res 39, 5813-5825.
10. Raghavan SC, Swanson PC, Wu X, Hsieh CL, &, Lieber MR, (2004) A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex. Nature 428, 88-93.
11. Raghavan SC, Swanson PC, Ma Y, &, Lieber MR, (2005) Double-strand break formation by the RAG complex at the bcl-2 major breakpoint region and at other non-B DNA structures in vitro. Mol Cell Biol 25, 5904-5919.
12. Naik AK, Lieber MR, &, Raghavan SC, (2010) Cytosines, but not purines, determine recombination activating gene (RAG)-induced Breaks on heteroduplex DNA structures: implications for genomic instability. J Biol Chem 285, 7587-7597.
13. Naik AK, &, Raghavan SC, (2012) Differential reaction kinetics, cleavage complex formation, and nonamer binding domain dependence dictate the structure-specific and sequence-specific nuclease activity of RAGs. J Mol Biol 415, 475-488.
14. Raghavan SC, Gu J, Swanson PC, &, Lieber MR, (2007) The structure-specific nicking of small heteroduplexes by the RAG complex: implications for lymphoid chromosomal translocations. DNA Repair (Amst) 6, 751-759.
15. Santagata S, Besmer E, Villa A, Bozzi F, Allingham JS, Sobacchi C, Haniford DB, Vezzoni P, Nussenzweig MC, Pan ZQ, et al,. (1999) The RAG1/RAG2 complex constitutes a 3′ flap endonuclease: implications for junctional diversity in V(D)J and transpositional recombination. Mol Cell 4, 935-947.
16. Arbuckle JL, Fauss LA, Simpson R, Ptaszek LM, &, Rodgers KK, (2001) Identification of two topologically independent domains in RAG1 and their role in macromolecular interactions relevant to V(D)J recombination. J Biol Chem 276, 37093-37101.
17. Rahman NS, Godderz LJ, Stray SJ, Capra JD, &, Rodgers KK, (2006) DNA cleavage of a cryptic recombination signal sequence by RAG1 and RAG2. Implications for partial V(H) gene replacement. J Biol Chem 281, 12370-12380.
18. Besmer E, Mansilla-Soto J, Cassard S, Sawchuk DJ, Brown G, Sadofsky M, Lewis SM, Nussenzweig MC, &, Cortes P, (1998) Hairpin coding end opening is mediated by RAG1 and RAG2 proteins. Mol Cell 2, 817-828.
19. Shockett PE, &, Schatz DG, (1999) DNA hairpin opening mediated by the RAG1 and RAG2 proteins. Mol Cell Biol 19, 4159-4166.
20. Gopalakrishnan V, &, Raghavan SC, (2012) Sequence and structural basis for chromosomal fragility during translocations in cancer. Future Oncol 8, 1121-1134.
21. Nambiar M, Goldsmith G, Moorthy BT, Lieber MR, Joshi MV, Choudhary B, Hosur RV, &, Raghavan SC, (2011) Formation of a G-quadruplex at the BCL2 major breakpoint region of the t(14;18) translocation in follicular lymphoma. Nucleic Acids Res 39, 936-948.
22. Raghavan SC, Hsieh CL, &, Lieber MR, (2005) Both V(D)J coding ends but neither signal end can recombine at the bcl-2 major breakpoint region, and the rejoining is ligase IV dependent. Mol Cell Biol 25, 6475-6484.
23. De P, Peak MM, &, Rodgers KK, (2004) DNA cleavage activity of the V(D)J recombination protein RAG1 is autoregulated. Mol Cell Biol 24, 6850-6860.
24. Nishana M, &, Raghavan SC, (2012) A non-B DNA can replace heptamer of V(D)J recombination when present along with a nonamer: implications in chromosomal translocations and cancer. Biochem J 448, 115-125.
25. Raghavan SC, Chastain P, Lee JS, Hegde BG, Houston S, Langen R, Hsieh CL, Haworth IS, &, Lieber MR, (2005) Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation. J Biol Chem 280, 22749-22760.
26. Tsai AG, Engelhart AE, Hatmal MM, Houston SI, Hud NV, Haworth IS, &, Lieber MR, (2009) Conformational variants of duplex DNA correlated with cytosine-rich chromosomal fragile sites. J Biol Chem 284, 7157-7164.
27. Feng JA, Johnson RC, &, Dickerson RE, (1994) Hin recombinase bound to DNA: the origin of specificity in major and minor groove interactions. Science 263, 348-355.
28. Alt FW, Zhang Y, Meng FL, Guo C, &, Schwer B, (2013) Mechanisms of programmed DNA lesions and genomic instability in the immune system. Cell 152, 417-429.
29. Nambiar M, &, Raghavan SC, (2013) Chromosomal translocations among the healthy human population: implications in oncogenesis. Cell Mol Life Sci 70, 1381-1392.
30. Sinden RR, (1994) DNA Structure and Function, Ist edn. Academic Press, San Diego, CA.
31. Srivastava M, Nambiar M, Sharma S, Karki SS, Goldsmith G, Hegde M, Kumar S, Pandey M, Singh RK, Ray P, et al,. (2012) An inhibitor of nonhomologous end-joining abrogates double-strand break repair and impedes cancer progression. Cell 151, 1474-1487.
32. Nambiar M, &, Raghavan SC, (2012) Mechanism of fragility at BCL2 gene minor breakpoint cluster region during t(14;18) chromosomal translocation. J Biol Chem 287, 8688-8701.
33. Sharma S, Choudhary B, &, Raghavan SC, (2011) Efficiency of nonhomologous DNA end joining varies among somatic tissues, despite similarity in mechanism. Cell Mol Life Sci 68, 661-676.
34. Raval P, Kriatchko AN, Kumar S, &, Swanson PC, (2008) Evidence for Ku70/Ku80 association with full-length RAG1. Nucleic Acids Res 36, 2060-2072.