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Michael R. Lieber, MD, PhD

Title(s)Professor of Pathology
SchoolKeck School of Medicine of USC
Phone+1 323 865 0568
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    Other Positions
    Title(s)Rita 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.

    Collapse Research 
    Collapse Research Activities and Funding
    Mechanisms of Human Lymphoid Chromosomal Translocation
    NIH/NCI R01CA196671Sep 1, 2016 - Aug 31, 2022
    Role: Principal Investigator
    Site-Specific Recombination in Human Health & Disease
    NIH/NIGMS R35GM118009Jun 1, 2016 - May 31, 2021
    Role: Principal Investigator
    Selective Inhibitors of the Artemis Endonuclease
    NIH/NIMH R03MH095489Feb 6, 2012 - Dec 31, 2014
    Role: Principal Investigator
    Mechanism and Regulation of Human Nonhomologous DNA End Joining
    NIH/NCI R01CA100504Aug 1, 2003 - Jul 31, 2022
    Role: Principal Investigator
    Mechanism of R-loop Formation in CSR and SHM
    NIH/NIGMS R01GM056984Sep 1, 1998 - Aug 31, 2016
    Role: Principal Investigator
    Normal and Mutant Lymphoid V(D)J Recombinase
    NIH/NIGMS R01GM043236Jun 1, 1990 - Aug 31, 2019
    Role: Principal Investigator
    MECHANISMS OF HUMAN LYMPHOID CHROMOSOMAL TRANSLOCATION
    NIH/NCI R37CA051105Jan 1, 1990 - Aug 31, 2014
    Role: Principal Investigator
    HUMAN V(D)J RECOMBINASE IN NEOPLASTIC AND PRIMARY CELLS
    NIH/NCI R01CA051105Jan 1, 1990 - Aug 31, 2005
    Role: Principal Investigator
    PROGRAM IN MOLECULAR ONCOLOGY
    NIH/NCI T32CA009569Sep 1, 1987 - Jul 31, 2003
    Role: Principal Investigator
    Postdoctoral Training in Tumor Biology
    NIH/NCI T32CA009151Jul 1, 1975 - Apr 30, 2015
    Role: Co-Principal Investigator

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    Collapse Publications
    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. Pannunzio NR, Lieber MR. AID and Reactive Oxygen Species Can Induce DNA Breaks within Human Chromosomal Translocation Fragile Zones. Mol Cell. 2019 Feb 07; 73(3):639. PMID: 30735656.
      View in: PubMed
    2. Duncan JR, Lieber MR, Adachi N, Wahl RL. Reply: Radiation Dose Does Matter: Mechanistic Insights into DNA Damage and Repair Support the Linear No-Threshold Model of Low-Dose Radiation Health Risks. J Nucl Med. 2019 Jan 10. PMID: 30630943.
      View in: PubMed
    3. Duncan JR, Lieber MR, Adachi N, Wahl RL. Reply: Radiation Dose Does Matter: Mechanistic Insights into DNA Damage and Repair Support the Linear No-Threshold Model of Low-Dose Radiation Health Risks J Nucl Med. 2018 11; 59(11):1780-1781. PMID: 30262519.
      View in: PubMed
    4. Duncan JR, Lieber MR, Adachi N, Wahl RL. Radiation Dose Does Matter: Mechanistic Insights into DNA Damage and Repair Support the Linear No-Threshold Model of Low-Dose Radiation Health Risks. J Nucl Med. 2018 Jul; 59(7):1014-1016. PMID: 29853652.
      View in: PubMed
    5. Pannunzio NR, Lieber MR. Concept of DNA Lesion Longevity and Chromosomal Translocations. Trends Biochem Sci. 2018 07; 43(7):490-498. PMID: 29735400.
      View in: PubMed
    6. Pannunzio NR, Watanabe G, Lieber MR. Nonhomologous DNA end-joining for repair of DNA double-strand breaks. J Biol Chem. 2018 07 06; 293(27):10512-10523. PMID: 29247009.
      View in: PubMed
    7. Conlin MP, Reid DA, Small GW, Chang HH, Watanabe G, Lieber MR, 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
    8. Watanabe G, Lieber MR, Williams D. Structural step forward for NHEJ. Cell Res. 2017 Nov; 27(11):1304-1306. PMID: 28925388.
      View in: PubMed
    9. Duncan JR, Lieber MR, Adachi N, Wahl RL. DNA Repair After Exposure to Ionizing Radiation Is Not Error-Free. J Nucl Med. 2018 Feb; 59(2):348. PMID: 28775198.
      View in: PubMed
    10. Gerodimos CA, Chang HHY, Watanabe G, Lieber MR. Effects of DNA end configuration on XRCC4-DNA ligase IV and its stimulation of Artemis activity. J Biol Chem. 2017 08 25; 292(34):13914-13924. PMID: 28696258.
      View in: PubMed
    11. Chang HHY, Pannunzio NR, Adachi N, Lieber MR. Non-homologous DNA end joining and alternative pathways to double-strand break repair. Nat Rev Mol Cell Biol. 2017 08; 18(8):495-506. PMID: 28512351.
      View in: PubMed
    12. Reid DA, Conlin MP, Yin Y, Chang HH, Watanabe G, Lieber MR, 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 02 28; 45(4):1872-1878. PMID: 27924007.
      View in: PubMed
    13. Chang HH, Watanabe G, Gerodimos CA, Ochi T, Blundell TL, Jackson SP, Lieber MR. Different DNA End Configurations Dictate Which NHEJ Components Are Most Important for Joining Efficiency. J Biol Chem. 2016 Nov 18; 291(47):24377-24389. PMID: 27703001.
      View in: PubMed
    14. Zagelbaum J, Shimazaki N, Esguerra ZA, Watanabe G, Lieber MR, Rothenberg E. Real-time analysis of RAG complex activity in V(D)J recombination. Proc Natl Acad Sci U S A. 2016 10 18; 113(42):11853-11858. PMID: 27702897.
      View in: PubMed
    15. Rand KA, Song C, Dean E, Serie DJ, Curtin K, Sheng X, Hu D, Huff CA, Bernal-Mizrachi L, Tomasson MH, Ailawadhi S, Singhal S, Pawlish K, Peters ES, Bock CH, Stram A, Van Den Berg DJ, Edlund CK, Conti DV, Zimmerman T, Hwang AE, Huntsman S, Graff J, Nooka A, Kong Y, Pregja SL, Berndt SI, Blot WJ, Carpten J, Casey G, Chu L, Diver WR, Stevens VL, Lieber MR, Goodman PJ, Hennis AJ, Hsing AW, Mehta J, Kittles RA, Kolb S, Klein EA, Leske C, Murphy AB, Nemesure B, Neslund-Dudas C, Strom SS, Vij R, Rybicki BA, Stanford JL, Signorello LB, Witte JS, Ambrosone CB, Bhatti P, John EM, Bernstein L, Zheng W, Olshan AF, Hu JJ, Ziegler RG, Nyante SJ, Bandera EV, Birmann BM, Ingles SA, Press MF, Atanackovic D, Glenn MJ, Cannon-Albright LA, Jones B, Tricot G, Martin TG, Kumar SK, Wolf JL, Deming Halverson SL, Rothman N, Brooks-Wilson AR, Rajkumar SV, Kolonel LN, Chanock SJ, Slager SL, Severson RK, Janakiraman N, Terebelo HR, Brown EE, De Roos AJ, Mohrbacher AF, Colditz GA, Giles GG, Spinelli JJ, Chiu BC, Munshi NC, Anderson KC, Levy J, Zonder JA, Orlowski RZ, Lonial S, Camp NJ, Vachon CM, Ziv E, Stram DO, Hazelett DJ, Haiman CA, Cozen W. A Meta-analysis of Multiple Myeloma Risk Regions in African and European Ancestry Populations Identifies Putatively Functional Loci. Cancer Epidemiol Biomarkers Prev. 2016 12; 25(12):1609-1618. PMID: 27587788.
      View in: PubMed
    16. Lieber MR. Mechanisms of human lymphoid chromosomal translocations. Nat Rev Cancer. 2016 05 25; 16(6):387-98. PMID: 27220482.
      View in: PubMed
    17. Chang HH, Lieber MR. Structure-Specific nuclease activities of Artemis and the Artemis: DNA-PKcs complex. Nucleic Acids Res. 2016 06 20; 44(11):4991-7. PMID: 27198222.
      View in: PubMed
    18. Greco GE, Matsumoto Y, Brooks RC, Lu Z, Lieber MR, Tomkinson AE. SCR7 is neither a selective nor a potent inhibitor of human DNA ligase IV. DNA Repair (Amst). 2016 07; 43:18-23. PMID: 27235626.
      View in: PubMed
    19. Pannunzio NR, Lieber MR. RNA Polymerase Collision versus DNA Structural Distortion: Twists and Turns Can Cause Break Failure. Mol Cell. 2016 05 05; 62(3):327-334. PMID: 27153532.
      View in: PubMed
    20. Pannunzio NR, Lieber MR. Dissecting the Roles of Divergent and Convergent Transcription in Chromosome Instability. Cell Rep. 2016 Feb 09; 14(5):1025-1031. PMID: 26804908.
      View in: PubMed
    21. Chang HH, Watanabe G, Lieber MR. 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].
    22. Lu Z, Pannunzio NR, Greisman HA, Casero D, Parekh C, Lieber MR. 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].
    23. Zhang ZZ, Pannunzio NR, Lu Z, Hsu E, Yu K, Lieber MR. 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.
    24. 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 MR, Greaves MF, Müschen M. Mechanisms of clonal evolution in childhood acute lymphoblastic leukemia. Nat Immunol. 2015 Jul; 16(7):766-774. PMID: 25985233.
      View in: PubMed
    25. Reid DA, Keegan S, Leo-Macias A, Watanabe G, Strande NT, Chang HH, Oksuz BA, Fenyo D, Lieber MR, 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.
    26. Zhang ZZ, Hsieh CL, Okitsu CY, Han L, Yu K, Lieber MR. 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.
    27. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber MR. 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.
    28. Lu Z, Lieber MR, 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.
      View in: PubMed
    29. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber MR. 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.
    30. Shimazaki N, Lieber MR. Histone methylation and V(D)J recombination. Int J Hematol. 2014 Sep; 100(3):230-7. PMID: 25060705.
      View in: PubMed
    31. Zhang ZZ, Pannunzio NR, Han L, Hsieh CL, Yu K, Lieber MR. 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.
    32. Askary A, Shimazaki N, Bayat N, Lieber MR. Modeling of the RAG reaction mechanism. Cell Rep. 2014 Apr 24; 7(2):307-15. PMID: 24703851; PMCID: PMC4010234.
    33. Pannunzio NR, Li S, Watanabe G, Lieber MR. Non-homologous end joining often uses microhomology: implications for alternative end joining. DNA Repair (Amst). 2014 May; 17:74-80. PMID: 24613510; PMCID: PMC4440676.
    34. Li S, Chang HH, Niewolik D, Hedrick MP, Pinkerton AB, Hassig CA, Schwarz K, Lieber MR. 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.
    35. Okitsu CY, Van Den Berg DJ, Lieber MR, 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.
    36. Hsieh JC, Van Den Berg D, Kang H, Hsieh CL, Lieber MR. 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
    37. Lu Z, Tsai AG, Akasaka T, Ohno H, Jiang Y, Melnick AM, Greisman HA, Lieber MR. 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.
    38. Cottarel J, Frit P, Bombarde O, Salles B, Négrel A, Bernard S, Jeggo PA, Lieber MR, 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.
    39. Kao YP, Hsieh WC, Hung ST, Huang CW, Lieber MR, 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
    40. Cui X, Lu Z, Kurosawa A, Klemm L, Bagshaw AT, Tsai AG, Gemmell N, Müschen M, Adachi N, Hsieh CL, Lieber MR. 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.
    41. Greisman HA, Lu Z, Tsai AG, Greiner TC, Yi HS, Lieber MR. 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.
    42. Shimazaki N, Askary A, Swanson PC, Lieber MR. 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.
    43. Li S, Kanno S, Watanabe R, Ogiwara H, Kohno T, Watanabe G, Yasui A, Lieber MR. 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.
    44. Nambiar M, Goldsmith G, Moorthy BT, Lieber MR, 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.
    45. Tsai AG, Yoda A, Weinstock DM, Lieber MR. 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
    46. Lieber MR, Wilson TE. SnapShot: Nonhomologous DNA end joining (NHEJ). Cell. 2010 Aug 06; 142(3):496-496.e1. PMID: 20691907.
      View in: PubMed
    47. Shibata D, Lieber MR. Is there any genetic instability in human cancer? DNA Repair (Amst). 2010 Aug 05; 9(8):858; discussion 859-60. PMID: 20605538; PMCID: PMC2914198.
    48. Tsai AG, Lu Z, Lieber MR. 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.
    49. Lieber MR. NHEJ and its backup pathways in chromosomal translocations. Nat Struct Mol Biol. 2010 Apr; 17(4):393-5. PMID: 20368722; PMCID: PMC3074614.
    50. Tsai AG, Lieber MR. Mechanisms of chromosomal rearrangement in the human genome. BMC Genomics. 2010 Feb 10; 11 Suppl 1:S1. PMID: 20158866; PMCID: PMC2822523.
    51. Gu J, Li S, Zhang X, Wang LC, Niewolik D, Schwarz K, Legerski RJ, Zandi E, Lieber MR. 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.
    52. Naik AK, Lieber MR, 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.
    53. Lieber MR. 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.
    54. Lieber MR, 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.
    55. Roy D, Zhang Z, Lu Z, Hsieh CL, Lieber MR. 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.
    56. 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.
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    57. 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 MR, 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.
      View in: PubMed
    58. Shimazaki N, Tsai AG, Lieber MR. 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.
    59. Roy D, Lieber MR. 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.
    60. Tsai AG, Engelhart AE, Hatmal MM, Houston SI, Hud NV, Haworth IS, Lieber MR. 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.
    61. Tsai AG, Lu H, Raghavan SC, Muschen M, Hsieh CL, Lieber MR. 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.
    62. de Villartay JP, Shimazaki N, Charbonnier JB, Fischer A, Mornon JP, Lieber MR, 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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    63. Longo VD, Lieber MR, 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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    64. Gajecka M, Gentles AJ, Tsai A, Chitayat D, Mackay KL, Glotzbach CD, Lieber MR, 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.
    65. Lu H, Shimazaki N, Raval P, Gu J, Watanabe G, Schwarz K, Swanson PC, Lieber MR. 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.
    66. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber MR, 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.
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    67. Shimazaki N, Lieber MR. DNA-PKcs at 7 angstrom: insights for DNA repair. Structure. 2008 Mar; 16(3):334-6. PMID: 18334206.
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    68. Tsai AG, Lieber MR. RAGs found "not guilty": cleared by DNA evidence. Blood. 2008 Feb 15; 111(4):1750. PMID: 19048671.
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    69. Gu J, Lieber MR. 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.
    70. Lieber MR, Raghavan SC, Yu K. Mechanistic aspects of lymphoid chromosomal translocations. J Natl Cancer Inst Monogr. 2008; (39):8-11. PMID: 18647994.
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    71. Lieber MR, 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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    72. Lieber MR. The mechanism of human nonhomologous DNA end joining. J Biol Chem. 2008 Jan 04; 283(1):1-5. PMID: 17999957.
      View in: PubMed
    73. Roy D, Yu K, Lieber MR. Mechanism of R-loop formation at immunoglobulin class switch sequences. Mol Cell Biol. 2008 Jan; 28(1):50-60. PMID: 17954560; PMCID: PMC2223306.
    74. Lu H, Schwarz K, Lieber MR. 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.
    75. Gu J, Lu H, Tsai AG, Schwarz K, Lieber MR. 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.
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