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Molecular and Cellular Biology Volume 25, 2005 - Issue 14
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Chromosome Structure and Dynamics

Double-Strand Break Formation by the RAG Complex at the Bcl-2 Major Breakpoint Region and at Other Non-B DNA Structures In Vitro

Sathees C. Raghavan1 Norris Comprehensive Cancer Center;2 Department of Pathology;3 Department of Biochemistry & Molecular Biology;4 Department of Biological Sciences;5 Department of Molecular Microbiology & Immunology, University of Southern California Keck School of Medicine, 1441 Eastlake Ave., Los Angeles, California90033
,
Patrick C. Swanson6 Department of Medical Microbiology and Immunology, Creighton University Medical Center, 2500 California Plaza, Omaha, Nebraska68178
,
Yunmei Ma1 Norris Comprehensive Cancer Center;2 Department of Pathology;3 Department of Biochemistry & Molecular Biology;4 Department of Biological Sciences;5 Department of Molecular Microbiology & Immunology, University of Southern California Keck School of Medicine, 1441 Eastlake Ave., Los Angeles, California90033
&
Michael R. Lieber1 Norris Comprehensive Cancer Center;2 Department of Pathology;3 Department of Biochemistry & Molecular Biology;4 Department of Biological Sciences;5 Department of Molecular Microbiology & Immunology, University of Southern California Keck School of Medicine, 1441 Eastlake Ave., Los Angeles, California90033Correspondence[email protected]
Pages 5904-5919 | Received 22 Nov 2004, Accepted 10 Apr 2005, Published online: 27 Mar 2023

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Di Liu & Michael R. Lieber. (2022) The mechanisms of human lymphoid chromosomal translocations and their medical relevance. Critical Reviews in Biochemistry and Molecular Biology 57:3, pages 227-243.
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Mridula Nambiar, Mrinal Srivastava, Vidya Gopalakrishnan, Sritha K. Sankaran & Sathees C. Raghavan. (2013) G-Quadruplex Structures Formed at the HOX11 Breakpoint Region Contribute to Its Fragility during t(10;14) Translocation in T-Cell Leukemia. Molecular and Cellular Biology 33:21, pages 4266-4281.
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Xiaoping Cui, Zhengfei Lu, Aya Kurosawa, Lars Klemm, Andrew T. Bagshaw, Albert G. Tsai, Neil Gemmell, Markus Müschen, Noritaka Adachi, Chih-Lin Hsieh & Michael R. Lieber. (2013) Both CpG Methylation and Activation-Induced Deaminase Are Required for the Fragility of the Human bcl-2 Major Breakpoint Region: Implications for the Timing of the Breaks in the t(14;18) Translocation. Molecular and Cellular Biology 33:5, pages 947-957.
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Mani Larijani, Alexander P. Petrov, Oxana Kolenchenko, Maribel Berru, Sergey N. Krylov & Alberto Martin. (2007) AID Associates with Single-Stranded DNA with High Affinity and a Long Complex Half-Life in a Sequence-Independent Manner. Molecular and Cellular Biology 27:1, pages 20-30.
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Sathees C. Raghavan, Chih-Lin Hsieh & Michael R. Lieber. (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. Molecular and Cellular Biology 25:15, pages 6475-6484.
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Articles from other publishers (51)

Guliang Wang & Karen M. Vasquez. (2022) Dynamic alternative DNA structures in biology and disease. Nature Reviews Genetics 24:4, pages 211-234.
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Sumedha Dahal, Humaira Siddiqua, Shivangi Sharma, Ravi K Babu, Diksha Rathore, Sheetal Sharma & Sathees C Raghavan. (2022) Unleashing a novel function of Endonuclease G in mitochondrial genome instability. eLife 11.
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Amita M. Paranjape, Sagar S. Desai, Mayilaadumveettil Nishana, Urbi Roy, Namrata M. Nilavar, Amrita Mondal, Rupa Kumari, Gudapureddy Radha, Vijeth Kumar Katapadi, Bibha Choudhary & Sathees C. Raghavan. (2022) Nonamer dependent RAG cleavage at CpGs can explain mechanism of chromosomal translocations associated to lymphoid cancers. PLOS Genetics 18:10, pages e1010421.
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Urbi Roy & Sathees C. Raghavan. (2021) Deleterious point mutations in T‐cell acute lymphoblastic leukemia: Mechanistic insights into leukemogenesis. International Journal of Cancer 149:6, pages 1210-1220.
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Rupa Kumari, Urbi Roy, Sagar Desai, Namrata M. Nilavar, Annemarie Van Nieuwenhuijze, Amita Paranjape, Gudapureddy Radha, Pushpinder Bawa, Mrinal Srivastava, Mridula Nambiar, Kithiganahalli Narayanaswamy Balaji, Adrian Liston, Bibha Choudhary & Sathees C. Raghavan. (2021) MicroRNA miR-29c regulates RAG1 expression and modulates V(D)J recombination during B cell development. Cell Reports 36:2, pages 109390.
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Namrata M. Nilavar, Amita M. Paranjape & Sathees C. Raghavan. (2020) Biochemical activity of RAGs is impeded by Dolutegravir, an HIV integrase inhibitor. Cell Death Discovery 6:1.
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Vidya Gopalakrishnan, Sumedha Dahal, Gudapureddy Radha, Shivangi Sharma, Sathees C. Raghavan & Bibha Choudhary. (2019) Characterization of DNA double-strand break repair pathways in diffuse large B cell lymphoma. Molecular Carcinogenesis 58:2, pages 219-233.
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Anton G. Henssen & Alex Kentsis. (2018) Emerging functions of DNA transposases and oncogenic mutators in childhood cancer development. JCI Insight 3:20.
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Aditi Daga, Afzal Ansari, Medha Pandya, Krupa Shah, Shanaya Patel, Rakesh Rawal & Valentina Umrania. (2016) Significant Role of Segmental Duplications and SIDD Sites in Chromosomal Translocations of Hematological Malignancies: A Multi-parametric Bioinformatic Analysis. Interdisciplinary Sciences: Computational Life Sciences 10:3, pages 467-475.
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Saniya M. Javadekar, Rakhee Yadav & Sathees C. Raghavan. (2018) DNA structural basis for fragility at peak III of BCL2 major breakpoint region associated with t(14;18) translocation. Biochimica et Biophysica Acta (BBA) - General Subjects 1862:3, pages 649-659.
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Pallabi Sengupta, Samit Chattopadhyay & Subhrangsu Chatterjee. (2017) G-Quadruplex surveillance in BCL-2 gene: a promising therapeutic intervention in cancer treatment. Drug Discovery Today 22:8, pages 1165-1186.
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Mayilaadumveettil Nishana, Namrata M Nilavar, Rupa Kumari, Monica Pandey & Sathees C Raghavan. (2017) HIV integrase inhibitor, Elvitegravir, impairs RAG functions and inhibits V(D)J recombination. Cell Death & Disease 8:6, pages e2852-e2852.
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Satish Kumar Tadi, Robin Sebastian, Sumedha Dahal, Ravi K. Babu, Bibha Choudhary & Sathees C. Raghavan. (2016) Microhomology-mediated end joining is the principal mediator of double-strand break repair during mitochondrial DNA lesions. Molecular Biology of the Cell 27:2, pages 223-235.
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Deepthi Raveendran & Sathees C. Raghavan. (2016) Biochemical Characterization of Nonamer Binding Domain of RAG1 Reveals its Thymine Preference with Respect to Length and Position. Scientific Reports 6:1.
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Saniya M. Javadekar & Sathees C. Raghavan. (2015) Snaps and mends: DNA breaks and chromosomal translocations. FEBS Journal 282:14, pages 2627-2645.
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Aditi Daga, Afzal Ansari, Rakesh Rawal & Valentina Umrania. (2015) Characterization of Chromosomal Translocation Breakpoint Sequences in Solid Tumours: “An In Silico Analysis”. The Open Medical Informatics Journal 9:1, pages 1-8.
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Rupa Kumari, Mridula Nambiar, Shaika Shanbagh & Sathees C. Raghavan. (2015) Detection of G-Quadruplex DNA Using Primer Extension as a Tool. PLOS ONE 10:3, pages e0119722.
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Rupa Kumari & Sathees C. Raghavan. (2015) Structure-specific nuclease activity of RAGs is modulated by sequence, length and phase position of flanking double-stranded DNA. FEBS Journal 282:1, pages 4-18.
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Xiangjun Du, E. Michael Gertz, Damian Wojtowicz, Dina Zhabinskaya, David Levens, Craig J. Benham, Alejandro A. Schäffer & Teresa M. Przytycka. (2014) Potential non-B DNA regions in the human genome are associated with higher rates of nucleotide mutation and expression variation. Nucleic Acids Research 42:20, pages 12367-12379.
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Elli Papaemmanuil, Inmaculada Rapado, Yilong Li, Nicola E Potter, David C Wedge, Jose Tubio, Ludmil B Alexandrov, Peter Van Loo, Susanna L Cooke, John Marshall, Inigo Martincorena, Jonathan Hinton, Gunes Gundem, Frederik W van Delft, Serena Nik-Zainal, David R Jones, Manasa Ramakrishna, Ian Titley, Lucy Stebbings, Catherine Leroy, Andrew Menzies, John Gamble, Ben Robinson, Laura Mudie, Keiran Raine, Sarah O'Meara, Jon W Teague, Adam P Butler, Giovanni Cazzaniga, Andrea Biondi, Jan Zuna, Helena Kempski, Markus Muschen, Anthony M Ford, Michael R Stratton, Mel Greaves & Peter J Campbell. (2014) RAG-mediated recombination is the predominant driver of oncogenic rearrangement in ETV6-RUNX1 acute lymphoblastic leukemia. Nature Genetics 46:2, pages 116-125.
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Christopher M. Kirkham, James N. Scott, Joan Boyes & Sarah Bevington. 2014. Transcriptional and Epigenetic Mechanisms Regulating Normal and Aberrant Blood Cell Development. Transcriptional and Epigenetic Mechanisms Regulating Normal and Aberrant Blood Cell Development 331 363 .
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Mayilaadumveettil Nishana & Sathees C. Raghavan. (2012) Role of recombination activating genes in the generation of antigen receptor diversity and beyond. Immunology 137:4, pages 271-281.
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Mayilaadumveettil Nishana & Sathees C. Raghavan. (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. Biochemical Journal 448:1, pages 115-125.
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Vijeth K. Katapadi, Mridula Nambiar & Sathees C. Raghavan. (2012) Potential G-quadruplex formation at breakpoint regions of chromosomal translocations in cancer may explain their fragility. Genomics 100:2, pages 72-80.
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Mridula Nambiar & Sathees C. Raghavan. (2012) Mechanism of Fragility at BCL2 Gene Minor Breakpoint Cluster Region during t(14;18) Chromosomal Translocation. Journal of Biological Chemistry 287:12, pages 8688-8701.
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Abani Kanta Naik & Sathees C. Raghavan. (2012) Differential Reaction Kinetics, Cleavage Complex Formation, and Nonamer Binding Domain Dependence Dictate the Structure-Specific and Sequence-Specific Nuclease Activity of RAGs. Journal of Molecular Biology 415:3, pages 475-488.
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Masashi Numata & Kyosuke Nagata. (2011) Synergistic requirement of orphan nonamer-like elements and DNA bending enhanced by HMGB1 for RAG-mediated nicking at cryptic 12-RSS but not authentic 12-RSS. Genes to Cells 16:8, pages 879-895.
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M. Nambiar & S. C. Raghavan. (2011) How does DNA break during chromosomal translocations?. Nucleic Acids Research 39:14, pages 5813-5825.
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Mridula Nambiar, G. Goldsmith, Balaji T. Moorthy, Michael R. Lieber, Mamata V. Joshi, Bibha Choudhary, Ramakrishna V. Hosur & Sathees C. Raghavan. (2011) Formation of a G-quadruplex at the BCL2 major breakpoint region of the t(14;18) translocation in follicular lymphoma. Nucleic Acids Research 39:3, pages 936-948.
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J Score, M J Calasanz, O Ottman, F Pane, R F Yeh, M A Sobrinho-Simões, S Kreil, D Ward, C Hidalgo-Curtis, J V Melo, J Wiemels, B Nadel, N C P Cross & F H Grand. (2010) Analysis of genomic breakpoints in p190 and p210 BCR–ABL indicate distinct mechanisms of formation. Leukemia 24:10, pages 1742-1750.
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Abani Kanta Naik, Michael R. Lieber & Sathees C. Raghavan. (2010) Cytosines, but Not Purines, Determine Recombination Activating Gene (RAG)-induced Breaks on Heteroduplex DNA Structures. Journal of Biological Chemistry 285:10, pages 7587-7597.
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Mridula Nambiar & Sathees C. Raghavan. (2009) Prevalence and analysis of t(14;18) and t(11;14) chromosomal translocations in healthy Indian population. Annals of Hematology 89:1, pages 35-43.
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Michael R. Lieber, Jiafeng Gu, Haihui Lu, Noriko Shimazaki & Albert G. Tsai. 2010. Genome Stability and Human Diseases. Genome Stability and Human Diseases 279 296 .
Albert G. Tsai, Aaron E. Engelhart, Ma'mon M. Hatmal, Sabrina I. Houston, Nicholas V. Hud, Ian S. Haworth & Michael R. Lieber. (2009) Conformational Variants of Duplex DNA Correlated with Cytosine-rich Chromosomal Fragile Sites. Journal of Biological Chemistry 284:11, pages 7157-7164.
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Albert G. Tsai, Haihui Lu, Sathees C. Raghavan, Markus Muschen, Chih-Lin Hsieh & Michael R. Lieber. (2008) Human Chromosomal Translocations at CpG Sites and a Theoretical Basis for Their Lineage and Stage Specificity. Cell 135:6, pages 1130-1142.
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Mridula Nambiar, Vijayalakshmi Kari & Sathees C. Raghavan. (2008) Chromosomal translocations in cancer. Biochimica et Biophysica Acta (BBA) - Reviews on Cancer 1786:2, pages 139-152.
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Hyun-Min Kim, Vidhya Narayanan, Piotr A Mieczkowski, Thomas D Petes, Maria M Krasilnikova, Sergei M Mirkin & Kirill S Lobachev. (2008) Chromosome fragility at GAA tracts in yeast depends on repeat orientation and requires mismatch repair. The EMBO Journal 27:21, pages 2896-2906.
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Jeffrey W. Pavlicek, Yuri L. Lyubchenko & Yung Chang. (2008) Quantitative Analyses of RAG−RSS Interactions and Conformations Revealed by Atomic Force Microscopy. Biochemistry 47:43, pages 11204-11211.
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Mridula Nambiar, Bibha Choudhary, Clementina R Rao & Sathees C Raghavan. (2008) Amplification of chromosomal translocation junctions from paraffin-embedded tissues of follicular lymphoma patients. Biomedical Materials 3:3, pages 034103.
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M. R. Lieber, S. C. Raghavan & K. Yu. (2008) Mechanistic Aspects of Lymphoid Chromosomal Translocations. JNCI Monographs 2008:39, pages 8-11.
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Han Li, James R. Mitchell & Paul Hasty. (2008) DNA double-strand breaks: A potential causative factor for mammalian aging?. Mechanisms of Ageing and Development 129:7-8, pages 416-424.
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K Busch, T Keller, U Fuchs, R-F Yeh, J Harbott, I Klose, J Wiemels, A Novosel, A Reiter & A Borkhardt. (2007) Identification of two distinct MYC breakpoint clusters and their association with various IGH breakpoint regions in the t(8;14) translocations in sporadic Burkitt-lymphoma. Leukemia 21:8, pages 1739-1751.
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Sathees C. Raghavan, Jiafeng Gu, Patrick C. Swanson & Michael R. Lieber. (2007) The structure-specific nicking of small heteroduplexes by the RAG complex: Implications for lymphoid chromosomal translocations. DNA Repair 6:6, pages 751-759.
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V B Holcomb, H Vogel, T Marple, R W Kornegay & P Hasty. (2006) Ku80 and p53 suppress medulloblastoma that arise independent of Rag-1-induced DSBs. Oncogene 25:54, pages 7159-7165.
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Michael R. Lieber, Kefei Yu & Sathees C. Raghavan. (2006) Roles of nonhomologous DNA end joining, V(D)J recombination, and class switch recombination in chromosomal translocations. DNA Repair 5:9-10, pages 1234-1245.
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Negar S. Rahman, LeAnn J. Godderz, Stephen J. Stray, J. Donald Capra & Karla K. Rodgers. (2006) DNA Cleavage of a Cryptic Recombination Signal Sequence by RAG1 and RAG2. Journal of Biological Chemistry 281:18, pages 12370-12380.
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Sathees C. Raghavan & Michael R. Lieber. (2006) DNA structures at chromosomal translocation sites. BioEssays 28:5, pages 480-494.
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Yang Xu. (2006) DNA damage: a trigger of innate immunity but a requirement for adaptive immune homeostasis. Nature Reviews Immunology 6:4, pages 261-270.
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Sathees C. Raghavan, Albert Tsai, Chih‐Lin Hsieh & Michael R. Lieber. 2006. DNA Repair, Part B. DNA Repair, Part B 301 316 .
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