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    Michael R. Lieber, MD, PhD

    TitleProfessor of Pathology
    SchoolKeck School of Medicine of USC
    DepartmentPathology
    AddressNTT 1441 Eastlake Ave
    Health Sciences Campus
    Los Angeles California 90089-9176
    Phone+1 323 865 0568
    Emaillieber@usc.edu
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      Other Positions
      TitleRita and Edward Polusky Chair in Basic Cancer Research


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      The web page for the Lieber lab is: lieber.usc.edu

      The following overview of research at the Lieber lab is taken from lieber.usc.edu.

      DNA double-strand breaks occur as part of the physiologic development of the immune repertoire in B and T lymphocytes. We study the manner in which these breaks are generated in a process called V(D)J recombination. Defects in the normal enzymes that generate these breaks can result in inherited forms of human severe combined immune deficiency (SCID). We study the biochemistry of how these proteins function, and we study how mutations in them result in SCID. Once DNA breaks are generated, they must be repaired. All cells of the body possess the ability to repair double-strand DNA breaks because all cells must deal with pathologic breaks in DNA that arise due to external radiation or due to free radicals of oxidative metabolism. The major pathway for repairing double-strand breaks in mammalian cells is called nonhomologous DNA end joining (NHEJ). If this pathway is defective in lymphocytes, then the breaks generated can not be repaired. Such defects also result in SCID. If the NHEJ pathway is defectve in all cells of the body, not only is the immune system affected, but the entire body is extremely vulnerable to ionizing radiation. Our laboratory has made substantial progress in defining proteins important in the NHEJ pathway. The first protein in the NHEJ pathway, Ku, binds at the broken DNA ends. The Artemis:DNA-PKcs complex is recruited to the DNA end by Ku. This binding activates the protein kinase activity of DNA-PKcs, which then phosphorylates Artemis and makes the Artemis:DNA-PKcs complex a potent nuclease for trimming DNA ends. Polymerase mu and lambda fill-in gaps, and polymerase mu can add nucleotides template-indepenently, like TdT. Finally, DNA ligase IV, XRCC4, and XLF form the ligation complex which ligates the double-strand break. We are interested in how all of these proteins carry out their functions and how their structure is important for this, and we are interested in identifying any other proteins that might be in th is pathway. We are also interested in how chromatin structure affects these proteins as they repair DNA breaks. The process of NHEJ is intrinsically imprecise. We suspect that this imprecision may contribute to the aging of somatic cells over time as well as to cancer. We are currently investigating this possibility using cell culture models, animal models, and analysis of human cells. Identification of inhibitors of NHEJ would be useful in cancer therapy and in improving gene targeting in human stem cells, and hence, we are trying to identify inhibitors of the pathway and individual components.

      Mistakes of V(D)J recombination account for about 40% of nonHodgkin's lymphoma. We study how the normal V(D)J recombination process goes awry. Specifically, why do some ends fail to join properly, and why do some sites adjacent to oncogenes get cleaved inadvertently. The inadvertent cleavage of some sites may be due to an altered DNA structure at those sites. We are trying to understand the extent to which such DNA structural deviations contribute to the fragility of such common chromosomal translocation hotspots.

      Class switch recombination is a second developmentally programmed gene rearrangement process in the vertebrate immune system, and it occurs in B cells at the Ig heavy chain locus. Class switching is the process that results in IgM being converted to IgG, IgA, or IgE. Humans borne with defects in class switching die early in life because they can not make IgA for protection of their lungs. The enzyme that initiates the class switch gene rearrangement process is a cytidine deaminase, called AID, that only functions on single-stranded DNA. We have focused on how the class switch recombination regions become single-stranded. Upon transcription, the RNA remains associated with the template DNA strand, resulting in an R-loop structure. The R-loop structure provides a substantial amount of single-stranded DNA at which the AID enzyme can act. We are interested in determining the factors that favor R-loop formation. In some lymphomas, the class switch recombination process goes awry, just as in V(D)J recombination. We are also studying these events.

      In summary, the Lieber lab focuses on how physiologic and pathologic gene rearrangements function in the immune system and in cancer and aging.


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      Publications listed below are automatically derived from MEDLINE/PubMed and other sources, which might result in incorrect or missing publications. Researchers can login to make corrections and additions, or contact us for help.
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      1. Watanabe G, Lieber M, Williams D. Structural step forward for NHEJ. Cell Res. 2017 Sep 19. PMID: 28925388.
        View in: PubMed
      2. Conlin MP, Reid DA, Small GW, Chang HH, Watanabe G, Lieber M, Ramsden DA, Rothenberg E. DNA Ligase IV Guides End-Processing Choice during Nonhomologous End Joining. Cell Rep. 2017 Sep 19; 20(12):2810-2819. PMID: 28930678.
        View in: PubMed
      3. Duncan JR, Lieber M, Adachi N, Wahl RL. DNA Repair Following Exposure to Ionizing Radiation is Not Error-Free. J Nucl Med. 2017 Aug 03. PMID: 28775198.
        View in: PubMed
      4. Gerodimos CA, Chang HHY, Watanabe G, Lieber M. Effects of DNA end configuration on XRCC4-DNA ligase IV and its stimulation of Artemis activity. J Biol Chem. 2017 Aug 25; 292(34):13914-13924. PMID: 28696258.
        View in: PubMed
      5. Chang HHY, Pannunzio NR, Adachi N, Lieber M. Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat Rev Mol Cell Biol. 2017 Aug; 18(8):495-506. PMID: 28512351.
        View in: PubMed
      6. Reid DA, Conlin MP, Yin Y, Chang HH, Watanabe G, Lieber M, Ramsden DA, Rothenberg E. Bridging of double-stranded breaks by the nonhomologous end-joining ligation complex is modulated by DNA end chemistry. Nucleic Acids Res. 2017 Feb 28; 45(4):1872-1878. PMID: 27924007.
        View in: PubMed
      7. Zagelbaum J, Shimazaki N, Esguerra ZA, Watanabe G, Lieber M, Rothenberg E. Real-time analysis of RAG complex activity in V(D)J recombination. Proc Natl Acad Sci U S A. 2016 Oct 18; 113(42):11853-11858. PMID: 27702897.
        View in: PubMed
      8. Lieber M. Mechanisms of human lymphoid chromosomal translocations. Nat Rev Cancer. 2016 05 25; 16(6):387-98. PMID: 27220482.
        View in: PubMed
      9. Greco GE, Matsumoto Y, Brooks RC, Lu Z, Lieber M, Tomkinson AE. SCR7 is neither a selective nor a potent inhibitor of human DNA ligase IV. DNA Repair (Amst). 2016 Jul; 43:18-23. PMID: 27235626.
        View in: PubMed
      10. Pannunzio NR, Lieber M. RNA Polymerase Collision versus DNA Structural Distortion: Twists and Turns Can Cause Break Failure. Mol Cell. 2016 May 5; 62(3):327-34. PMID: 27153532.
        View in: PubMed
      11. Pannunzio NR, Lieber M. Dissecting the Roles of Divergent and Convergent Transcription in Chromosome Instability. Cell Rep. 2016 Feb 09; 14(5):1025-31. PMID: 26804908.
        View in: PubMed
      12. Lu Z, Pannunzio NR, Greisman HA, Casero D, Parekh C, Lieber M. Convergent BCL6 and lncRNA promoters demarcate the major breakpoint region for BCL6 translocations. Blood. 2015 Oct 01; 126(14):1730-1. PMID: 26276666; PMCID: PMC4591794 [Available on 10/01/16].
      13. Chang HH, Watanabe G, Lieber M. Unifying the DNA end-processing roles of the artemis nuclease: Ku-dependent artemis resection at blunt DNA ends. J Biol Chem. 2015 Oct 02; 290(40):24036-50. PMID: 26276388; PMCID: PMC4591795 [Available on 10/02/16].
      14. Zhang ZZ, Pannunzio NR, Lu Z, Hsu E, Yu K, Lieber M. The repetitive portion of the Xenopus IgH Mu switch region mediates orientation-dependent class switch recombination. Mol Immunol. 2015 Oct; 67(2 Pt B):524-31. PMID: 26277278; PMCID: PMC4615597.
      15. Swaminathan S, Klemm L, Park E, Papaemmanuil E, Ford A, Kweon SM, Trageser D, Hasselfeld B, Henke N, Mooster J, Geng H, Schwarz K, Kogan SC, Casellas R, Schatz DG, Lieber M, Greaves MF, Müschen M. Mechanisms of clonal evolution in childhood acute lymphoblastic leukemia. Nat Immunol. 2015 Jul; 16(7):766-774. PMID: 25985233; PMCID: PMC4475638.
      16. Reid DA, Keegan S, Leo-Macias A, Watanabe G, Strande NT, Chang HH, Oksuz BA, Fenyo D, Lieber M, Ramsden DA, Rothenberg E. Organization and dynamics of the nonhomologous end-joining machinery during DNA double-strand break repair. Proc Natl Acad Sci U S A. 2015 May 19; 112(20):E2575-84. PMID: 25941401; PMCID: PMC4443322.
      17. Zhang ZZ, Hsieh CL, Okitsu CY, Han L, Yu K, Lieber M. Effect of CpG dinucleotides within IgH switch region repeats on immunoglobulin class switch recombination. Mol Immunol. 2015 Aug; 66(2):284-9. PMID: 25899867; PMCID: PMC4461542.
      18. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber M. Complexities due to single-stranded RNA during antibody detection of genomic rna:dna hybrids. BMC Res Notes. 2015 Apr 08; 8:127. PMID: 25890199; PMCID: PMC4393563.
      19. Lu Z, Lieber M, Tsai AG, Pardo CE, Müschen M, Kladde MP, Hsieh CL. Human lymphoid translocation fragile zones are hypomethylated and have accessible chromatin. Mol Cell Biol. 2015 Apr; 35(7):1209-22. PMID: 25624348; PMCID: PMC4355534.
      20. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber M. The role of G-density in switch region repeats for immunoglobulin class switch recombination. Nucleic Acids Res. 2014 Dec 01; 42(21):13186-93. PMID: 25378327; PMCID: PMC4245955.
      21. Shimazaki N, Lieber M. Histone methylation and V(D)J recombination. Int J Hematol. 2014 Sep; 100(3):230-7. PMID: 25060705.
        View in: PubMed
      22. Zhang ZZ, Pannunzio NR, Han L, Hsieh CL, Yu K, Lieber M. The strength of an Ig switch region is determined by its ability to drive R loop formation and its number of WGCW sites. Cell Rep. 2014 Jul 24; 8(2):557-69. PMID: 25017067; PMCID: PMC4118936.
      23. Askary A, Shimazaki N, Bayat N, Lieber M. Modeling of the RAG reaction mechanism. Cell Rep. 2014 Apr 24; 7(2):307-15. PMID: 24703851; PMCID: PMC4010234.
      24. Pannunzio NR, Li S, Watanabe G, Lieber M. Non-homologous end joining often uses microhomology: implications for alternative end joining. DNA Repair (Amst). 2014 May; 17:74-80. PMID: 24613510; PMCID: PMC4440676.
      25. Li S, Chang HH, Niewolik D, Hedrick MP, Pinkerton AB, Hassig CA, Schwarz K, Lieber M. Evidence that the DNA endonuclease ARTEMIS also has intrinsic 5'-exonuclease activity. J Biol Chem. 2014 Mar 14; 289(11):7825-34. PMID: 24500713; PMCID: PMC3953294.
      26. Okitsu CY, Van Den Berg DJ, Lieber M, Hsieh CL. Reproducibility and reliability of SNP analysis using human cellular DNA at or near nanogram levels. BMC Res Notes. 2013 Dec 06; 6:515. PMID: 24314330; PMCID: PMC4029319.
      27. Hsieh JC, Van Den Berg D, Kang H, Hsieh CL, Lieber M. Large chromosome deletions, duplications, and gene conversion events accumulate with age in normal human colon crypts. Aging Cell. 2013 Apr; 12(2):269-79. PMID: 23425690.
        View in: PubMed
      28. Lu Z, Tsai AG, Akasaka T, Ohno H, Jiang Y, Melnick AM, Greisman HA, Lieber M. BCL6 breaks occur at different AID sequence motifs in Ig-BCL6 and non-Ig-BCL6 rearrangements. Blood. 2013 May 30; 121(22):4551-4. PMID: 23476051; PMCID: PMC3668488.
      29. Cottarel J, Frit P, Bombarde O, Salles B, Négrel A, Bernard S, Jeggo PA, Lieber M, Modesti M, Calsou P. A noncatalytic function of the ligation complex during nonhomologous end joining. J Cell Biol. 2013 Jan 21; 200(2):173-86. PMID: 23337116; PMCID: PMC3549972.
      30. Kao YP, Hsieh WC, Hung ST, Huang CW, Lieber M, Huang FT. Detection and characterization of R-loops at the murine immunoglobulin Sa region. Mol Immunol. 2013 Jun; 54(2):208-16. PMID: 23287599.
        View in: PubMed
      31. Cui X, Lu Z, Kurosawa A, Klemm L, Bagshaw AT, Tsai AG, Gemmell N, Müschen M, Adachi N, Hsieh CL, Lieber M. 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. Mol Cell Biol. 2013 Mar; 33(5):947-57. PMID: 23263985; PMCID: PMC3623081.
      32. Greisman HA, Lu Z, Tsai AG, Greiner TC, Yi HS, Lieber M. IgH partner breakpoint sequences provide evidence that AID initiates t(11;14) and t(8;14) chromosomal breaks in mantle cell and Burkitt lymphomas. Blood. 2012 Oct 04; 120(14):2864-7. PMID: 22915650; PMCID: PMC3466967.
      33. Shimazaki N, Askary A, Swanson PC, Lieber M. Mechanistic basis for RAG discrimination between recombination sites and the off-target sites of human lymphomas. Mol Cell Biol. 2012 Jan; 32(2):365-75. PMID: 22064481; PMCID: PMC3255787.
      34. Li S, Kanno S, Watanabe R, Ogiwara H, Kohno T, Watanabe G, Yasui A, Lieber M. Polynucleotide kinase and aprataxin-like forkhead-associated protein (PALF) acts as both a single-stranded DNA endonuclease and a single-stranded DNA 3' exonuclease and can participate in DNA end joining in a biochemical system. J Biol Chem. 2011 Oct 21; 286(42):36368-77. PMID: 21885877; PMCID: PMC3196146.
      35. Nambiar M, Goldsmith G, Moorthy BT, Lieber M, Joshi MV, Choudhary B, Hosur RV, Raghavan SC. Formation of a G-quadruplex at the BCL2 major breakpoint region of the t(14;18) translocation in follicular lymphoma. Nucleic Acids Res. 2011 Feb; 39(3):936-48. PMID: 20880994; PMCID: PMC3035451.
      36. Tsai AG, Yoda A, Weinstock DM, Lieber M. t(X;14)(p22;q32)/t(Y;14)(p11;q32) CRLF2-IGH translocations from human B-lineage ALLs involve CpG-type breaks at CRLF2, but CRLF2/P2RY8 intrachromosomal deletions do not. Blood. 2010 Sep 16; 116(11):1993-4. PMID: 20847213.
        View in: PubMed
      37. Lieber M, Wilson TE. SnapShot: Nonhomologous DNA end joining (NHEJ). Cell. 2010 Aug 06; 142(3):496-496.e1. PMID: 20691907.
        View in: PubMed
      38. Shibata D, Lieber M. Is there any genetic instability in human cancer? DNA Repair (Amst). 2010 Aug 05; 9(8):858; discussion 859-60. PMID: 20605538; PMCID: PMC2914198.
      39. Tsai AG, Lu Z, Lieber M. The t(14;18)(q32;q21)/IGH-MALT1 translocation in MALT lymphomas is a CpG-type translocation, but the t(11;18)(q21;q21)/API2-MALT1 translocation in MALT lymphomas is not. Blood. 2010 Apr 29; 115(17):3640-1; author reply 3641-2. PMID: 20430965; PMCID: PMC2867271.
      40. Lieber M. NHEJ and its backup pathways in chromosomal translocations. Nat Struct Mol Biol. 2010 Apr; 17(4):393-5. PMID: 20368722; PMCID: PMC3074614.
      41. Tsai AG, Lieber M. Mechanisms of chromosomal rearrangement in the human genome. BMC Genomics. 2010 Feb 10; 11 Suppl 1:S1. PMID: 20158866; PMCID: PMC2822523.
      42. Gu J, Li S, Zhang X, Wang LC, Niewolik D, Schwarz K, Legerski RJ, Zandi E, Lieber M. DNA-PKcs regulates a single-stranded DNA endonuclease activity of Artemis. DNA Repair (Amst). 2010 Apr 04; 9(4):429-37. PMID: 20117966; PMCID: PMC2847011.
      43. Naik AK, Lieber M, Raghavan SC. Cytosines, but not purines, determine recombination activating gene (RAG)-induced breaks on heteroduplex DNA structures: implications for genomic instability. J Biol Chem. 2010 Mar 05; 285(10):7587-97. PMID: 20051517; PMCID: PMC2844206.
      44. Lieber M. The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem. 2010; 79:181-211. PMID: 20192759; PMCID: PMC3079308.
      45. Lieber M, Gu J, Lu H, Shimazaki N, Tsai AG. Nonhomologous DNA end joining (NHEJ) and chromosomal translocations in humans. Subcell Biochem. 2010; 50:279-96. PMID: 20012587; PMCID: PMC3079314.
      46. Roy D, Zhang Z, Lu Z, Hsieh CL, Lieber M. Competition between the RNA transcript and the nontemplate DNA strand during R-loop formation in vitro: a nick can serve as a strong R-loop initiation site. Mol Cell Biol. 2010 Jan; 30(1):146-59. PMID: 19841062; PMCID: PMC2798282.
      47. Amin N, Gonzalez E, Lieber M, Salusky IB, Zaritsky JJ. Successful treatment of calcific uremic arteriolopathy in a pediatric dialysis patient. Pediatr Nephrol. 2010 Feb; 25(2):357-62. PMID: 19885686.
        View in: PubMed
      48. Klemm L, Duy C, Iacobucci I, Kuchen S, von Levetzow G, Feldhahn N, Henke N, Li Z, Hoffmann TK, Kim YM, Hofmann WK, Jumaa H, Groffen J, Heisterkamp N, Martinelli G, Lieber M, Casellas R, Müschen M. The B cell mutator AID promotes B lymphoid blast crisis and drug resistance in chronic myeloid leukemia. Cancer Cell. 2009 Sep 08; 16(3):232-45. PMID: 19732723; PMCID: PMC2931825.
      49. Shimazaki N, Tsai AG, Lieber M. H3K4me3 stimulates the V(D)J RAG complex for both nicking and hairpinning in trans in addition to tethering in cis: implications for translocations. Mol Cell. 2009 Jun 12; 34(5):535-44. PMID: 19524534; PMCID: PMC2920491.
      50. Roy D, Lieber M. G clustering is important for the initiation of transcription-induced R-loops in vitro, whereas high G density without clustering is sufficient thereafter. Mol Cell Biol. 2009 Jun; 29(11):3124-33. PMID: 19307304; PMCID: PMC2682002.
      51. Tsai AG, Engelhart AE, Hatmal MM, Houston SI, Hud NV, Haworth IS, Lieber M. Conformational variants of duplex DNA correlated with cytosine-rich chromosomal fragile sites. J Biol Chem. 2009 Mar 13; 284(11):7157-64. PMID: 19106104; PMCID: PMC2652318.
      52. Tsai AG, Lu H, Raghavan SC, Muschen M, Hsieh CL, Lieber M. Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity. Cell. 2008 Dec 12; 135(6):1130-42. PMID: 19070581; PMCID: PMC2642632.
      53. de Villartay JP, Shimazaki N, Charbonnier JB, Fischer A, Mornon JP, Lieber M, Callebaut I. A histidine in the beta-CASP domain of Artemis is critical for its full in vitro and in vivo functions. DNA Repair (Amst). 2009 Feb 01; 8(2):202-8. PMID: 19022407.
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      54. Longo VD, Lieber M, Vijg J. Turning anti-ageing genes against cancer. Nat Rev Mol Cell Biol. 2008 11; 9(11):903-10. PMID: 18946478.
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      55. Gajecka M, Gentles AJ, Tsai A, Chitayat D, Mackay KL, Glotzbach CD, Lieber M, Shaffer LG. Unexpected complexity at breakpoint junctions in phenotypically normal individuals and mechanisms involved in generating balanced translocations t(1;22)(p36;q13). Genome Res. 2008 Nov; 18(11):1733-42. PMID: 18765821; PMCID: PMC2577863.
      56. Lu H, Shimazaki N, Raval P, Gu J, Watanabe G, Schwarz K, Swanson PC, Lieber M. A biochemically defined system for coding joint formation in V(D)J recombination. Mol Cell. 2008 Aug 22; 31(4):485-97. PMID: 18722175; PMCID: PMC2564285.
      57. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber M, Yang AS, An W. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell. 2008 Apr 11; 30(1):86-97. PMID: 18406329.
        View in: PubMed
      58. Shimazaki N, Lieber M. DNA-PKcs at 7 angstrom: insights for DNA repair. Structure. 2008 Mar; 16(3):334-6. PMID: 18334206.
        View in: PubMed
      59. Tsai AG, Lieber M. RAGs found "not guilty": cleared by DNA evidence. Blood. 2008 Feb 15; 111(4):1750. PMID: 19048671.
        View in: PubMed
      60. Gu J, Lieber M. Mechanistic flexibility as a conserved theme across 3 billion years of nonhomologous DNA end-joining. Genes Dev. 2008 Feb 15; 22(4):411-5. PMID: 18281457; PMCID: PMC2731650.
      61. Lieber M, Raghavan SC, Yu K. Mechanistic aspects of lymphoid chromosomal translocations. J Natl Cancer Inst Monogr. 2008; (39):8-11. PMID: 18647994.
        View in: PubMed
      62. Lieber M, Lu H, Gu J, Schwarz K. Flexibility in the order of action and in the enzymology of the nuclease, polymerases, and ligase of vertebrate non-homologous DNA end joining: relevance to cancer, aging, and the immune system. Cell Res. 2008 Jan; 18(1):125-33. PMID: 18087292.
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      63. Lieber M. The mechanism of human nonhomologous DNA end joining. J Biol Chem. 2008 Jan 04; 283(1):1-5. PMID: 17999957.
        View in: PubMed
      64. Roy D, Yu K, Lieber M. Mechanism of R-loop formation at immunoglobulin class switch sequences. Mol Cell Biol. 2008 Jan; 28(1):50-60. PMID: 17954560; PMCID: PMC2223306.
      65. Lu H, Schwarz K, Lieber M. Extent to which hairpin opening by the Artemis:DNA-PKcs complex can contribute to junctional diversity in V(D)J recombination. Nucleic Acids Res. 2007; 35(20):6917-23. PMID: 17932067; PMCID: PMC2175297.
      66. Gu J, Lu H, Tsai AG, Schwarz K, Lieber M. Single-stranded DNA ligation and XLF-stimulated incompatible DNA end ligation by the XRCC4-DNA ligase IV complex: influence of terminal DNA sequence. Nucleic Acids Res. 2007; 35(17):5755-62. PMID: 17717001; PMCID: PMC2034460.
      67. Huang FT, Yu K, Balter BB, Selsing E, Oruc Z, Khamlichi AA, Hsieh CL, Lieber M. Sequence dependence of chromosomal R-loops at the immunoglobulin heavy-chain Smu class switch region. Mol Cell Biol. 2007 Aug; 27(16):5921-32. PMID: 17562862; PMCID: PMC1952116.
      68. Raghavan SC, Lieber M. DNA structure and human diseases. Front Biosci. 2007 May 01; 12:4402-8. PMID: 17485384.
        View in: PubMed
      69. Lu H, Pannicke U, Schwarz K, Lieber M. Length-dependent binding of human XLF to DNA and stimulation of XRCC4.DNA ligase IV activity. J Biol Chem. 2007 Apr 13; 282(15):11155-62. PMID: 17317666.
        View in: PubMed
      70. Raghavan SC, Gu J, Swanson PC, Lieber M. The structure-specific nicking of small heteroduplexes by the RAG complex: implications for lymphoid chromosomal translocations. DNA Repair (Amst). 2007 Jun 01; 6(6):751-9. PMID: 17307402; PMCID: PMC2692700.
      71. Gu J, Lu H, Tippin B, Shimazaki N, Goodman MF, Lieber M. XRCC4:DNA ligase IV can ligate incompatible DNA ends and can ligate across gaps. EMBO J. 2007 Feb 21; 26(4):1010-23. PMID: 17290226; PMCID: PMC1852838.
      72. Niewolik D, Pannicke U, Lu H, Ma Y, Wang LC, Kulesza P, Zandi E, Lieber M, Schwarz K. DNA-PKcs dependence of Artemis endonucleolytic activity, differences between hairpins and 5' or 3' overhangs. J Biol Chem. 2006 Nov 10; 281(45):33900-9. PMID: 16914548.
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      73. Lieber M. The polymerases for V(D)J recombination. Immunity. 2006 Jul; 25(1):7-9. PMID: 16860749.
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      74. Lieber M, Yu K, Raghavan SC. Roles of nonhomologous DNA end joining, V(D)J recombination, and class switch recombination in chromosomal translocations. DNA Repair (Amst). 2006 Sep 08; 5(9-10):1234-45. PMID: 16793349.
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      75. Raghavan SC, Lieber M. DNA structures at chromosomal translocation sites. Bioessays. 2006 May; 28(5):480-94. PMID: 16615081.
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      76. Huang FT, Yu K, Hsieh CL, Lieber M. Downstream boundary of chromosomal R-loops at murine switch regions: implications for the mechanism of class switch recombination. Proc Natl Acad Sci U S A. 2006 Mar 28; 103(13):5030-5. PMID: 16547142; PMCID: PMC1458789.
      77. Buck D, Moshous D, de Chasseval R, Ma Y, le Deist F, Cavazzana-Calvo M, Fischer A, Casanova JL, Lieber M, de Villartay JP. Severe combined immunodeficiency and microcephaly in siblings with hypomorphic mutations in DNA ligase IV. Eur J Immunol. 2006 Jan; 36(1):224-35. PMID: 16358361.
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      78. Raghavan SC, Tsai A, Hsieh CL, Lieber M. Analysis of non-B DNA structure at chromosomal sites in the mammalian genome. Methods Enzymol. 2006; 409:301-16. PMID: 16793408.
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      79. Ma Y, Lieber M. In vitro nonhomologous DNA end joining system. Methods Enzymol. 2006; 408:502-10. PMID: 16793389.
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      80. Yu K, Roy D, Huang FT, Lieber M. Detection and structural analysis of R-loops. Methods Enzymol. 2006; 409:316-29. PMID: 16793409.
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      81. Raghavan SC, Tong J, Lieber M. Hybrid joint formation in human V(D)J recombination requires nonhomologous DNA end joining. DNA Repair (Amst). 2006 Feb 03; 5(2):278-85. PMID: 16275127.
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      82. Ma Y, Lu H, Schwarz K, Lieber M. Repair of double-strand DNA breaks by the human nonhomologous DNA end joining pathway: the iterative processing model. Cell Cycle. 2005 Sep; 4(9):1193-200. PMID: 16082219.
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      83. Ma Y, Pannicke U, Lu H, Niewolik D, Schwarz K, Lieber M. The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. J Biol Chem. 2005 Oct 07; 280(40):33839-46. PMID: 16093244.
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      84. Raghavan SC, Hsieh CL, Lieber M. 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. 2005 Aug; 25(15):6475-84. PMID: 16024785; PMCID: PMC1190333.
      85. Ma Y, Schwarz K, Lieber M. The Artemis:DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps. DNA Repair (Amst). 2005 Jul 12; 4(7):845-51. PMID: 15936993.
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      86. Raghavan SC, Swanson PC, Ma Y, Lieber M. 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. 2005 Jul; 25(14):5904-19. PMID: 15988007; PMCID: PMC1168826.
      87. Raghavan SC, Chastain P, Lee JS, Hegde BG, Houston S, Langen R, Hsieh CL, Haworth IS, Lieber M. Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation. J Biol Chem. 2005 Jun 17; 280(24):22749-60. PMID: 15840562.
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