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The Lieber Lab

Keck School of Medicine
University of Southern California

PI

Michael R. Lieber, M.D., Ph.D.

Affiliations Department of Pathology
Department of Biochemistry and Molecular Biology
Department of Molecular Microbiology and Immunology
Department of Biological Sciences
Address Norris Comprehensive Cancer Center
1441 Eastlake Avenue, Room 5428
Los Angeles, CA 90033
Telephone(323)865-0568
Fax (323)865-3019
e-Mail lieber@usc.edu
Mail Code9176 HSC
Students The Graduate School
Programs in Biomedical and Biological Sciences (PIBBS)
MD/PhD Program

Photo Album


Dr. Michael Lieber

 

Research Overview

The Lieber lab studies how chromosome breaks play key roles in human cancer, aging, and the immune system.

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 defective 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-independently, like TdT. Finally, DNA ligase IV, XRCC4, and XLF form the ligation complex that 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.

Immunoglobulin 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 cannot 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.

 

Photo Album

Click here for photos of the laboratory, holiday and publication parties, and graduation celebrations.

Selected Publications

Mechanisms of human lymphoid chromosomal translocations.. Lieber MR. Nature Reviews Cancer 16(6): 387-98, 2016. PMID: 27220482

Dissecting the Roles of Divergent and Convergent Transcription in Chromosome Instability.. Pannunzio NR, Lieber MR. Cell Reports 14(5): 1025-1031, 2016. PMID:26804908

The repetitive portion of the Xenopus IgH Mu switch region mediates orientation-dependent class switch recombination.. Zhang ZZ, Pannunzio NR, Lu Z, Hsu E, Yu K, Lieber MR. (2015) Mol Immunol. 67(2 Pt B):524-31. PMID:26277278

Convergent BCL6 and lncRNA promoters demarcate the major breakpoint region for BCL6 translocations.. Lu Z, Pannunzio NR, Greisman HA, Casero D, Parekh C, Lieber MR. (2015) Blood. 126(14):1730-1. PMID:26276666

Unifying the DNA End-processing Roles of the Artemis Nuclease: KU-DEPENDENT ARTEMIS RESECTION AT BLUNT DNA ENDS.. Chang HH, Watanabe G, Lieber MR. (2015) J Biol Chem. 290(40):24036-50. PMID:26276388

Mechanisms of clonal evolution in childhood acute lymphoblastic leukemia.. 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. Nat Immunol. 16(7): 766-74, 2015. PMID:25985233

Organization and dynamics of the nonhomologous end-joining machinery during DNA double-strand break repair. Reid DA, Keegan S, Leo-Macias A, Watanabe G, Strande NT, Chang HH, Oksuz BA, Fenyo D, Lieber MR, Ramsden DA, Rothenberg E. Proc Natl Acad Sci 112(20): E2575-84, 2015. PMID:25941401

Effect of CpG dinucleotides within IgH switch region repeats on immunoglobulin class switch recombination. Zhang ZZ, Hsieh CL, Okitsu CY, Han L, Yu K, Lieber MR. Mol Immunol. 66(2):284-9, 2015. PMID:25899867

Complexities due to single-stranded RNA during antibody detection of genomic rna:dna hybrids. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber MR BMC Res Notes 8;8:127,2015. PMID:25890199


Human lymphoid translocation fragile zones are hypomethylated and have accessible chromatin. Lu Z, Lieber MR, Tsai AG, Pardo CE, Müschen M, Kladde MP, Hsieh CL. Mol Cell Biol. 35(7): 1209-22, 2015. PMID: 25624348


The role of G-density in switch region repeats for immunoglobulin class switch recombination. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber MR. Nucleic Acids Res. 42(21): 13186-93, 2014. PMID: 25378327

The Strength of an Ig Switch Region Is Determined by Its Ability to Drive R Loop Formation and Its Number of WGCW Sites. Zhang ZZ, Pannunzio NR, Han L, Hsieh CL, Yu K, Lieber MR. Cell Rep. 2014 Jul 24;8(2):557-69. doi: 10.1016/j.celrep.2014.06.021. Epub 2014 Jul 10. PMID: 25017067

Modeling of the RAG Reaction Mechanism. Askary A, Shimazaki N, Bayat N, Lieber MR. Cell Rep. 2014 Apr 24;7(2):307-15. PMID: 24703851


BCL6 breaks occur at different AID sequence motifs in Ig-BCL6 and non-Ig-BCL6 rearrangements. Lu Z, Tsai AG, Akasaka T, Ohno H, Jiang Y, Melnick AM, Greisman HA, Lieber MR. Blood. 2013 May 30;121(22):4551-4. doi: 10.1182/blood-2012-10-464958. Epub 2013 Mar PMID: 23476051


Large chromosome deletions, duplications, and gene conversion events accumulate with age in normal human colon crypts. Hsieh JC, Van Den Berg D, Kang H, Hsieh CL, Lieber MR. Aging Cell. 2013 Apr;12(2):269-79. PMID: 23425690


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. Cui X, Lu Z, Kurosawa A, Klemm L, Bagshaw AT, Tsai AG, Gemmell N, Müschen M, Adachi N, Hsieh CL, Lieber MR. Mol Cell Biol. 2013 Mar;33(5):947-57. PMID: 23263985


Mechanistic basis for RAG discrimination between recombination sites and the off-target sites of human lymphomas. Shimazaki N, Askary A, Swanson PC, Lieber MR. Mol Cell Biol. 2012 Jan;32(2):365-75. doi: 10.1128/MCB.06187-11. Epub 2011 Nov 7. PMID 22064481


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. Roy D, Zhang Z, Lu Z, Hsieh CL, Lieber MR. 2010 Mol Cell Biol. 30(1):146-59.


H3K4me3 stimulates the V(D)J RAG complex for both nicking and hairpinning in trans in addition to tethering in cis: implications for translocations. Shimazaki N, Tsai AG, Lieber MR. 2009 Mol Cell. 34(5):535-44.


Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity. Tsai AG, Lu H, Raghavan SC, Muschen M, Hsieh CL, Lieber MR. 2008 Cell. 135(6):1130-42.


Mechanism of R-loop formation at immunoglobulin class switch sequences. Roy D, Yu K, Lieber MR. 2008 Mol Cell Biol. 28(1):50-60.

A biochemically defined system for coding joint formation in V(D)J recombination. Lu H, Shimazaki N, Raval P, Gu J, Watanabe G, Schwarz K, Swanson PC, Lieber MR. 2008 Mol Cell. 31(4):485-97.

XRCC4:DNA ligase IV can ligate incompatible DNA ends and can ligate across gaps. Gu J, Lu H, Tippin B, Shimazaki N, Goodman MF, Lieber MR. 2007 EMBO J. 26(4):1010-23.

Downstream boundary of chromosomal R-loops at murine switch regions: implications for the mechanism of class switch recombination. Huang FT, Yu K, Hsieh CL, Lieber MR. 2006 Proc Natl Acad Sci U S A. 103(13):5030-5.


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. Raghavan SC, Hsieh CL, Lieber MR. 2005 Mol Cell Biol. 25(15):6475-84.

A biochemically defined system for mammalian nonhomologous DNA end joining. Ma Y, Lu H, Tippin B, Goodman MF, Shimazaki N, Koiwai O, Hsieh CL, Schwarz K, Lieber MR. 2004 Mol Cell. 16(5):701-13.

A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex. Raghavan SC, Swanson PC, Wu X, Hsieh CL, Lieber MR. 2004 Nature. 428(6978):88-93.

R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Yu K, Chedin F, Hsieh CL, Wilson TE, Lieber MR. 2003 Nat Immunol. 4(5):442-51.

Bidirectional gene organization: a common architectural feature of the human genome. Adachi N, Lieber MR. 2002 Cell. 109(7):807-9.


Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Ma Y, Pannicke U, Schwarz K, Lieber MR. 2002 Cell. 108(6):781-94.

Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Karanjawala ZE, Murphy N, Hinton DR, Hsieh CL, Lieber MR. 2002 Curr Biol. 12(5):397-402.

The nonhomologous DNA end joining pathway is important for chromosome stability in primary fibroblasts. Karanjawala ZE, Grawunder U, Hsieh CL, Lieber MR. 1999 Curr Biol. 9(24):1501-4.

A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Wu X, Wilson TE, Lieber MR. 1999 Proc Natl Acad Sci U S A. 96(4):1303-8.

DNA ligase IV is essential for V(D)J recombination and DNA double-strand break repair in human precursor lymphocytes. Grawunder U, Zimmer D, Fugmann S, Schwarz K, Lieber MR. 1998 Mol Cell. 2(4):477-84.

Interaction of DNA-dependent protein kinase with DNA and with Ku: biochemical and atomic-force microscopy studies. Yaneva M, Kowalewski T, Lieber MR. 1997 EMBO J. 16(16):5098-112.

Yeast DNA ligase IV mediates non-homologous DNA end joining. Wilson TE, Grawunder U, Lieber MR. 1997 Nature. 388(6641):495-8.

Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Grawunder U, Wilm M, Wu X, Kulesza P, Wilson TE, Mann M, Lieber MR. 1997 Nature. 388(6641):492-5.

Strand specificity in the transcriptional targeting of recombination at immunoglobulin switch sequences. Daniels GA, Lieber MR. 1995 Proc Natl Acad Sci U S A. 92(12):5625-9.

Functional domains within FEN-1 and RAD2 define a family of structure-specific endonucleases: implications for nucleotide excision repair. Harrington JJ, Lieber MR. 1994 Genes Dev. 8(11):1344-55.

The characterization of a mammalian DNA structure-specific endonuclease. Harrington JJ, Lieber MR. 1994 EMBO J. 13(5):1235-46.

Coding end sequence can markedly affect the initiation of V(D)J recombination. Gerstein RM, Lieber MR. 1993 Genes Dev. 7(7B):1459-69.

Extent to which homology can constrain coding exon junctional diversity in V(D)J recombination. Gerstein RM, Lieber MR. 1993 Nature. 363(6430):625-7.

The basis for the mechanistic bias for deletional over inversional V(D)J recombination. Gauss GH, Lieber MR. 1992 Genes Dev. 6(8):1553-61.

CpG methylated minichromosomes become inaccessible for V(D)J recombination after undergoing replication. Hsieh CL, Lieber MR. 1992 EMBO J. 11(1):315-25.

 

All Publications

Mechanisms of human lymphoid chromosomal translocations. Lieber MR. Nature Reviews Cancer 16(6): 387-98, 2016. PMID: 27220482

Structure-Specific nuclease activities of Artemis and the Artemis: DNA-PKcs complex.
Chang HH, Lieber MR. Nucleic Acids Res. 2016 May 19 (in press) PMID: 27198222

RNA Polymerase Collision versus DNA Structural Distortion: Twists and Turns Can Cause Break Failure.
Pannunzio NR,Lieber MR. Molecular Cell 62: 327-34. PMID: 27153532

SCR7 is neither a selective nor a potent inhibitor of human DNA ligase IV. Greco GE, Matsumoto Y, Brooks RC, Lu Z, Lieber MR, Tomkinson AE. DNA Repair (Amst) 43: 18-23, 2016. PMID: 27235626

Dissecting the Roles of Divergent and Convergent Transcription in Chromosome Instability.. Pannunzio NR, Lieber MR. Cell Reports 14(5): 1025-1031, 2016. PMID:26804908

The repetitive portion of the Xenopus IgH Mu switch region mediates orientation-dependent class switch recombination.. Zhang ZZ, Pannunzio NR, Lu Z, Hsu E, Yu K, Lieber MR. (2015) Mol Immunol. 67(2 Pt B):524-31. PMID:26277278

Convergent BCL6 and lncRNA promoters demarcate the major breakpoint region for BCL6 translocations.. Lu Z, Pannunzio NR, Greisman HA, Casero D, Parekh C, Lieber MR. (2015) Blood. 126(14):1730-1. PMID:26276666

Unifying the DNA End-processing Roles of the Artemis Nuclease: KU-DEPENDENT ARTEMIS RESECTION AT BLUNT DNA ENDS.. Chang HH, Watanabe G, Lieber MR. (2015) J Biol Chem. 290(40):24036-50. PMID:26276388

Mechanisms of clonal evolution in childhood acute lymphoblastic leukemia.. 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. Nat Immunol. 16(7): 766-74, 2015. PMID:25985233

Organization and dynamics of the nonhomologous end-joining machinery during DNA double-strand break repair. Reid DA, Keegan S, Leo-Macias A, Watanabe G, Strande NT, Chang HH, Oksuz BA, Fenyo D, Lieber MR, Ramsden DA, Rothenberg E. Proc Natl Acad Sci 112(20): E2575-84, 2015. PMID:25941401

Effect of CpG dinucleotides within IgH switch region repeats on immunoglobulin class switch recombination. Zhang ZZ, Hsieh CL, Okitsu CY, Han L, Yu K, Lieber MR. Mol Immunol. 66(2):284-9,2015. PMID:25899867

Complexities due to single-stranded RNA during antibody detection of genomic rna:dna hybrids. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber MR BMC Res Notes 8;8:127,2015. PMID:25890199

Human lymphoid translocation fragile zones are hypomethylated and have accessible chromatin. Lu Z, Lieber MR, Tsai AG, Pardo CE, Müschen M, Kladde MP, Hsieh CL. Mol Cell Biol. 35(7): 1209-22, 2015. PMID: 25624348

The role of G-density in switch region repeats for immunoglobulin class switch recombination. Zhang ZZ, Pannunzio NR, Hsieh CL, Yu K, Lieber MR. Nucleic Acids Res. 42(21): 13186-93, 2014. PMID: 25378327

The Strength of an Ig Switch Region Is Determined by Its Ability to Drive R Loop Formation and Its Number of WGCW Sites. Zhang ZZ, Pannunzio NR, Han L, Hsieh CL, Yu K, Lieber MR. Cell Rep. 2014 Jul 24;8(2):557-69. doi: 10.1016/j.celrep.2014.06.021. Epub 2014 Jul 10. PMID 25017067

Modeling of the RAG reaction mechanism. Askary A, Shimazaki N, Bayat N, Lieber MR. Cell Rep. 2014 Apr 24;7(2):307-15. PMID 24703851

Evidence that the DNA Endonuclease ARTEMIS also has Intrinsic 5' Exonuclease Activity. Li S, Chang HH, Niewolik D, Hedrick MP, Pinkerton AB, Hassig C, Schwarz K, Lieber MR. J Biol Chem. 2014 Feb 5. [Epub ahead of print] PMID 24500713

A noncatalytic function of the ligation complex during nonhomologous end joining. Cottarel J, Frit P, Bombarde O, Salles B, Négrel A, Bernard S, Jeggo PA, Lieber MR, Modesti M, Calsou P. J Cell Biol. 2013 Jan 21;200(2):173-86. doi: 10.1083/jcb.201203128. PMID: 23337116

Detection and characterization of R-loops at the murine immunoglobulin Sα region. Kao YP, Hsieh WC, Hung ST, Huang CW, Lieber MR., Huang FT. Mol Immunol. 2013 Jun;54(2):208-16. PMID: 23287599

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. Cui X, Lu Z, Kurosawa A, Klemm L, Bagshaw AT, Tsai AG, Gemmell N, Müschen M, Adachi N, Hsieh CL, Lieber MR.. Mol Cell Biol. 2013 Mar;33(5):947-57. PMID: 23263985

IgH partner breakpoint sequences provide evidence that AID initiates t(11;14) and t(8;14) chromosomal breaks in mantle cell and Burkitt lymphomas. Greisman HA, Lu Z, Tsai AG, Greiner TC, Yi HS, Lieber MR.. Blood. 2012 Oct 4;120(14):2864-7. PMID:22915650

Mechanistic basis for RAG discrimination between recombination sites and the off-target sites of human lymphomas. Shimazaki N, Askary A, Swanson PC, Lieber MR. Mol Cell Biol. 2012 Jan;32(2):365-75. doi: 10.1128/MCB.06187-11. Epub 2011 Nov 7. PMID 22064481

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. Li S, Kanno S, Watanabe R, Ogiwara H, Kohno T, Watanabe G, Yasui A, Lieber MR. J Biol Chem. 2011 Oct 21;286(42):36368-77. PMID: 21885877 [PubMed - in process]

Formation of a G-quadruplex at the BCL2 major breakpoint region of the t(14;18) translocation in follicular lymphoma. Nambiar M, Goldsmith G, Moorthy BT, Lieber MR, Joshi MV, Choudhary B, Hosur RV, Raghavan SC. Nucleic Acids Res. 2011 Feb;39(3):936-48. PMID: 20880994 [PubMed - indexed for MEDLINE] Free PMC Article

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. Tsai AG, Yoda A, Weinstock DM, Lieber MR. Blood. 2010 Sep 16;116(11):1993-4. PMID: 20847213 [PubMed - indexed for MEDLINE] Free Article

SnapShot: Nonhomologous DNA end joining (NHEJ). Lieber MR, Wilson TE. Cell. 2010 Aug 6;142(3):496-496.e1. PMID: 20691907

Is there any genetic instability in human cancer? Shibata D, Lieber MR. DNA Repair (Amst). 2010 Aug 5;9(8):858; discussion 859-60. Epub 2010 Jun 3. No abstract available. PMID: 20605538 [PubMed - indexed for MEDLINE] Free PMC Article

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. Tsai AG, Lu Z, Lieber MR. Blood. 2010 Apr 29;115(17):3640-1; author reply 3641-2. No abstract available. PMID: 20430965 [PubMed - indexed for MEDLINE] Free PMC Article Related citations

NHEJ and its backup pathways in chromosomal translocations. Lieber MR. Nat Struct Mol Biol. 2010 Apr;17(4):393-5. No abstract available. PMID: 20368722 [PubMed - indexed for MEDLINE] Free PMC Article Related citations

The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Lieber MR. Annu Rev Biochem. 2010;79:181-211. Review. PMID: 20192759 [PubMed - indexed for MEDLINE] Free PMC Article Related citations

Mechanisms of chromosomal rearrangement in the human genome. Tsai AG, Lieber MR. BMC Genomics. 2010 Feb 10;11 Suppl 1:S1. Review. PMID: 20158866 [PubMed - indexed for MEDLINE]

DNA-PKcs regulates a single-stranded DNA endonuclease activity of Artemis. Gu J, Li S, Zhang X, Wang LC, Niewolik D, Schwarz K, Legerski RJ, Zandi E, Lieber MR. 2010 DNA Repair (Amst). 9(4):429-37.

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. Roy D, Zhang Z, Lu Z, Hsieh CL, Lieber MR. 2010 Mol Cell Biol. 30(1):146-59.

H3K4me3 stimulates the V(D)J RAG complex for both nicking and hairpinning in trans in addition to tethering in cis: implications for translocations. Shimazaki N, Tsai AG, Lieber MR. 2009 Mol Cell. 34(5):535-44.

G clustering is important for the initiation of transcription-induced R-loops in vitro, whereas high G density without clustering is sufficient thereafter. Roy D, Lieber MR. 2009 Mol Cell Biol. 29(11):3124-33.

Conformational variants of duplex DNA correlated with cytosine-rich chromosomal fragile sites. Tsai AG, Engelhart AE, Hatmal MM, Houston SI, Hud NV, Haworth IS, Lieber MR. 2009 J Biol Chem. 284(11):7157-64.

Human chromosomal translocations at CpG sites and a theoretical basis for their lineage and stage specificity. Tsai AG, Lu H, Raghavan SC, Muschen M, Hsieh CL, Lieber MR. 2008 Cell. 135(6):1130-42.

A biochemically defined system for coding joint formation in V(D)J recombination. Lu H, Shimazaki N, Raval P, Gu J, Watanabe G, Schwarz K, Swanson PC, Lieber MR. 2008 Mol Cell. 31(4):485-97.

Mechanism of R-loop formation at immunoglobulin class switch sequences. Roy D, Yu K, Lieber MR. 2008 Mol Cell Biol. 28(1):50-60.

Extent to which hairpin opening by the Artemis:DNA-PKcs complex can contribute to junctional diversity in V(D)J recombination. Lu H, Schwarz K, Lieber MR. 2007 Nucleic Acids Res. 35(20):6917-23.

Single-stranded DNA ligation and XLF-stimulated incompatible DNA end ligation by the XRCC4-DNA ligase IV complex: influence of terminal DNA sequence. Gu J, Lu H, Tsai AG, Schwarz K, Lieber MR. 2007 Nucleic Acids Res. 35(17):5755-62.

Sequence dependence of chromosomal R-loops at the immunoglobulin heavy-chain Smu class switch region. Huang FT, Yu K, Balter BB, Selsing E, Oruc Z, Khamlichi AA, Hsieh CL, Lieber MR. 2007 Mol Cell Biol. 27(16):5921-32.

Length-dependent binding of human XLF to DNA and stimulation of XRCC4.DNA ligase IV activity. Lu H, Pannicke U, Schwarz K, Lieber MR. 2007 J Biol Chem. 282(15):11155-62.

The structure-specific nicking of small heteroduplexes by the RAG complex: implications for lymphoid chromosomal translocations. Raghavan SC, Gu J, Swanson PC, Lieber MR. 2007 DNA Repair (Amst). 6(6):751-9.

XRCC4:DNA ligase IV can ligate incompatible DNA ends and can ligate across gaps. Gu J, Lu H, Tippin B, Shimazaki N, Goodman MF, Lieber MR. 2007 EMBO J. 26(4):1010-23.

Downstream boundary of chromosomal R-loops at murine switch regions: implications for the mechanism of class switch recombination. Huang FT, Yu K, Hsieh CL, Lieber MR. 2006 Proc Natl Acad Sci U S A. 103(13):5030-5.

Hybrid joint formation in human V(D)J recombination requires nonhomologous DNA end joining. Raghavan SC, Tong J, Lieber MR. 2006 DNA Repair (Amst). 5(2):278-85.

The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. Ma Y, Pannicke U, Lu H, Niewolik D, Schwarz K, Lieber MR. 2005 J Biol Chem. 280(40):33839-46.

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. Raghavan SC, Hsieh CL, Lieber MR. 2005 Mol Cell Biol. 25(15):6475-84.

Double-strand break formation by the RAG complex at the bcl-2 major breakpoint region and at other non-B DNA structures in vitro. Raghavan SC, Swanson PC, Ma Y, Lieber MR. 2005 Mol Cell Biol. 25(14):5904-19.

The Artemis:DNA-PKcs endonuclease cleaves DNA loops, flaps, and gaps. Ma Y, Schwarz K, Lieber MR. 2005 DNA Repair (Amst). 4(7):845-51.

Evidence for a triplex DNA conformation at the bcl-2 major breakpoint region of the t(14;18) translocation. Raghavan SC, Chastain P, Lee JS, Hegde BG, Houston S, Langen R, Hsieh CL, Haworth IS, Lieber MR. 2005 J Biol Chem. 280(24):22749-60.

Fine-structure analysis of activation-induced deaminase accessibility to class switch region R-loops. Yu K, Roy D, Bayramyan M, Haworth IS, Lieber MR. 2005 Mol Cell Biol. 25(5):1730-6.

Generation and characterization of endonuclease G null mice. Irvine RA, Adachi N, Shibata DK, Cassell GD, Yu K, Karanjawala ZE, Hsieh CL, Lieber MR. 2005 Mol Cell Biol. 25(1):294-302.

A biochemically defined system for mammalian nonhomologous DNA end joining. Ma Y, Lu H, Tippin B, Goodman MF, Shimazaki N, Koiwai O, Hsieh CL, Schwarz K, Lieber MR. 2004 Mol Cell. 16(5):701-13.

A non-B-DNA structure at the Bcl-2 major breakpoint region is cleaved by the RAG complex. Raghavan SC, Swanson PC, Wu X, Hsieh CL, Lieber MR. 2003 Nature. 428(6978):88-93.

Kinetic analysis of the nicking and hairpin formation steps in V(D)J recombination. Yu K, Taghva A, Ma Y, Lieber MR. 2003 DNA Repair (Amst). 3(1):67-75.

Developmental retinal apoptosis in Ku86-/- mice. Karanjawala ZE, Hinton DR, Oh E, Hsieh CL, Lieber MR. 2003 DNA Repair (Amst). 2(12):1429-34.

DNA substrate length and surrounding sequence affect the activation-induced deaminase activity at cytidine. Yu K, Huang FT, Lieber MR. 2003 J Biol Chem. 279(8):6496-500.

R-loops at immunoglobulin class switch regions in the chromosomes of stimulated B cells. Yu K, Chedin F, Hsieh CL, Wilson TE, Lieber MR. 2003 Nat Immunol. 4(5):442-51.

Overexpression of Cu/Zn superoxide dismutase is lethal for mice lacking double-strand break repair. Karanjawala ZE, Hsieh CL, Lieber MR. 2003 DNA Repair (Amst). 2(3):285-94.

The embryonic lethality in DNA ligase IV-deficient mice is rescued by deletion of Ku: implications for unifying the heterogeneous phenotypes of NHEJ mutants. Karanjawala ZE, Adachi N, Irvine RA, Oh EK, Shibata D, Schwarz K, Hsieh CL, Lieber MR. 2002 DNA Repair (Amst). 1(12):1017-26.

Two overlapping divergent transcription units in the human genome: the FEN1/C11orf10 locus. Adachi N, Karanjawala ZE, Matsuzaki Y, Koyama H, Lieber MR. 2002 OMICS. 6(3):273-9.

Bidirectional gene organization: a common architectural feature of the human genome. Adachi N, Lieber MR. 2002 Cell. 109(7):807-9.

Hairpin opening and overhang processing by an Artemis/DNA-dependent protein kinase complex in nonhomologous end joining and V(D)J recombination. Ma Y, Pannicke U, Schwarz K, Lieber MR. 2002 Cell. 108(6):781-94.

Oxygen metabolism causes chromosome breaks and is associated with the neuronal apoptosis observed in DNA double-strand break repair mutants. Karanjawala ZE, Murphy N, Hinton DR, Hsieh CL, Lieber MR. 2002 Curr Biol. 12(5):397-402.

Binding of inositol hexakisphosphate (IP6) to Ku but not to DNA-PKcs. Ma Y, Lieber MR. 2002 J Biol Chem. 277(13):10756-9.

Analysis of the kinetic and equilibrium binding of Ku protein to DNA. Taghva A, Ma Y, Lieber MR. 2002 J Theor Biol. 214(1):85-97.

The cleavage efficiency of the human immunoglobulin heavy chain VH elements by the RAG complex: implications for the immune repertoire. Yu K, Taghva A, Lieber MR. 2002 J Biol Chem. 277(7):5040-6.

DNA length-dependent cooperative interactions in the binding of Ku to DNA. Ma Y, Lieber MR. 2001 Biochemistry. 40(32):9638-46.

Analysis of the V(D)J recombination efficiency at lymphoid chromosomal translocation breakpoints. Raghavan SC, Kirsch IR, Lieber MR. 2001 J Biol Chem. 276(31):29126-33.

The mammalian FEN-1 locus: structure and conserved sequence features. Karanjawala ZE, Shi X, Hsieh CL, Lieber MR. 2000 Microb Comp Genomics. 5(3):173-7.

The nicking step in V(D)J recombination is independent of synapsis: implications for the immune repertoire. Yu K, Lieber MR. 2000 Mol Cell Biol. 20(21):7914-21.

The nonhomologous DNA end joining pathway is important for chromosome stability in primary fibroblasts. Karanjawala ZE, Grawunder U, Hsieh CL, Lieber MR. 1999 Curr Biol. 9(24):1501-4.

Mechanistic basis for coding end sequence effects in the initiation of V(D)J recombination. Yu K, Lieber MR. 1999 Mol Cell Biol. 19(12):8094-102.

Efficient processing of DNA ends during yeast nonhomologous end joining. Evidence for a DNA polymerase beta (Pol4)-dependent pathway. Wilson TE, Lieber MR. 1999 J Biol Chem. 274(33):23599-609.

A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Wu X, Wilson TE, Lieber MR. 1999 Proc Natl Acad Sci U S A. 96(4):1303-8.

DNA ligase IV is essential for V(D)J recombination and DNA double-strand break repair in human precursor lymphocytes. Grawunder U, Zimmer D, Fugmann S, Schwarz K, Lieber MR. 1998 Mol Cell. 2(4):477-84.

The RAG-HMG1 complex enforces the 12/23 rule of V(D)J recombination specifically at the double-hairpin formation step. West RB, Lieber MR. 1998 Mol Cell Biol. 18(11):6408-15.

Productive and nonproductive complexes of Ku and DNA-dependent protein kinase at DNA termini. West RB, Yaneva M, Lieber MR. 1998 Mol Cell Biol. 18(10):5908-20.

Requirement for an interaction of XRCC4 with DNA ligase IV for wild-type V(D)J recombination and DNA double-strand break repair in vivo. Grawunder U, Zimmer D, Kulesza P, Lieber MR. 1998 J Biol Chem. 273(38):24708-14.

DNA-PK is essential only for coding joint formation in V(D)J recombination. Kulesza P, Lieber MR. 1998 Nucleic Acids Res. 26(17):3944-8.

V(D)J recombination activity in human hematopoietic cells: correlation with developmental stage and genome stability. Gauss GH, Domain I, Hsieh CL, Lieber MR. 1998 Eur J Immunol. 28(1):351-8.

Interaction between DNA-dependent protein kinase and a novel protein, KIP. Wu X, Lieber MR. 1997 Mutat Res. 385(1):13-20.

Interaction of DNA-dependent protein kinase with DNA and with Ku: biochemical and atomic-force microscopy studies. Yaneva M, Kowalewski T, Lieber MR. 1997 EMBO J. 16(16):5098-112.

Yeast DNA ligase IV mediates non-homologous DNA end joining. Wilson TE, Grawunder U, Lieber MR. 1997 Nature. 388(6641):495-8.

Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammalian cells. Grawunder U, Wilm M, Wu X, Kulesza P, Wilson TE, Mann M, Lieber MR. 1997 Nature. 388(6641):492-5.

A complex of RAG-1 and RAG-2 proteins persists on DNA after single-strand cleavage at V(D)J recombination signal sequences. Grawunder U, Lieber MR. 1997 Nucleic Acids Res. 25(7):1375-82.

Protein-protein and protein-DNA interaction regions within the DNA end-binding protein Ku70-Ku86. Wu X, Lieber MR. 1996 Mol Cell Biol. 16(9):5186-93.

Asymmetric mutation around the recombination break point of immunoglobulin class switch sequences on extrachromosomal substrates. Li J, Daniels GA, Lieber MR. 1996 Nucleic Acids Res. 24(11):2104-11.

Processing of branched DNA intermediates by a complex of human FEN-1 and PCNA. Wu X, Li J, Li X, Hsieh CL, Burgers PM, Lieber MR. 1996 Nucleic Acids Res. 24(11):2036-43.

Transcription targets recombination at immunoglobulin switch sequences in a strand-specific manner. Daniels GA, Lieber MR. 1996 Curr Top Microbiol Immunol. 217:171-89.

Mechanistic constraints on diversity in human V(D)J recombination. Gauss GH, Lieber MR. 1996 Mol Cell Biol. 16(1):258-69.

RNA:DNA complex formation upon transcription of immunoglobulin switch regions: implications for the mechanism and regulation of class switch recombination. Daniels GA, Lieber MR. 1995 Nucleic Acids Res. 23(24):5006-11.

Mechanistic properties of immunoglobulin somatic mutation. Ford JE, McHeyzer-Williams MG, Lieber MR. 1995 Ann N Y Acad Sci. 764:187-8.

Lagging strand DNA synthesis at the eukaryotic replication fork involves binding and stimulation of FEN-1 by proliferating cell nuclear antigen. Li X, Li J, Harrington J, Lieber MR, Burgers PM. 1995 J Biol Chem. 270(38):22109-12.

Strand specificity in the transcriptional targeting of recombination at immunoglobulin switch sequences. Daniels GA, Lieber MR. 1995 Proc Natl Acad Sci U S A. 92(12):5625-9.

The scid factor on human chromosome 8 restores V(D)J recombination in addition to double-strand break repair. Komatsu K, Kubota N, Gallo M, Okumura Y, Lieber MR. 1995 Cancer Res. 55(8):1774-9.

DNA structural elements required for FEN-1 binding. Harrington JJ, Lieber MR. 1995 J Biol Chem. 270(9):4503-8.

Distinct roles for RAG-1 in the initiation of V(D)J recombination and in the resolution of coding ends. Gallo ML, Pergola F, Daniels GA, Lieber MR. 1994 J Biol Chem. 269(35):22188-92.

Analysis of individual immunoglobulin lambda light chain genes amplified from single cells is inconsistent with variable region gene conversion in germinal-center B cell somatic mutation. Ford JE, McHeyzer-Williams MG, Lieber MR. 1994 Eur J Immunol. 24(8):1816-22.

Functional domains within FEN-1 and RAD2 define a family of structure-specific endonucleases: implications for nucleotide excision repair. Harrington JJ, Lieber MR. 1994 Genes Dev. 8(11):1344-55.

Chimeric molecules created by gene amplification interfere with the analysis of somatic hypermutation of murine immunoglobulin genes. Ford JE, McHeyzer-Williams MG, Lieber MR. 1994 Gene. 142(2):279-83.

The characterization of a mammalian DNA structure-specific endonuclease. Harrington JJ, Lieber MR. 1994 EMBO J. 13(5):1235-46.

V(D)J recombination in ataxia telangiectasia, Bloom's syndrome, and a DNA ligase I-associated immunodeficiency disorder. Hsieh CL, Arlett CF, Lieber MR. 1993 J Biol Chem. 268(27):20105-9.

Coding end sequence can markedly affect the initiation of V(D)J recombination. Gerstein RM, Lieber MR. 1993 Genes Dev. 7(7B):1459-69.

Unequal signal and coding joint formation in human V(D)J recombination. Gauss GH, Lieber MR. 1993 Mol Cell Biol. 13(7):3900-6.

Extent to which homology can constrain coding exon junctional diversity in V(D)J recombination. Gerstein RM, Lieber MR. 1993 Nature. 363(6430):625-7.

V(D)J recombination in mammalian cell mutants defective in DNA double-strand break repair. Pergola F, Zdzienicka MZ, Lieber MR. 1993 Mol Cell Biol. 13(6):3464-71.

V(D)J recombination: signal and coding joint resolution are uncoupled and depend on parallel synapsis of the sites. Sheehan KM, Lieber MR. 1993 Mol Cell Biol. 13(3):1363-70.

Lymphoid V(D)J recombination. Functional analysis of the spacer sequence within the recombination signal. Wei Z, Lieber MR. 1993 J Biol Chem. 268(5):3180-3.

DEAE-dextran enhances electroporation of mammalian cells. Gauss GH, Lieber MR. 1992 Nucleic Acids Res. 20(24):6739-40.

Analysis of the defect in DNA end joining in the murine scid mutation. Harrington J, Hsieh CL, Gerton J, Bosma G, Lieber MR. 1992 Mol Cell Biol. 12(10):4758-68.

V(D)J recombination on minichromosomes is not affected by transcription. Hsieh CL, McCloskey RP, Lieber MR. 1992 J Biol Chem. 267(22):15613-9.

The basis for the mechanistic bias for deletional over inversional V(D)J recombination. Gauss GH, Lieber MR. 1992 Genes Dev. 6(8):1553-61.

CpG methylated minichromosomes become inaccessible for V(D)J recombination after undergoing replication. Hsieh CL, Lieber MR. 1992 EMBO J. 11(1):315-25.

V(D)J recombination: evidence that a replicative mechanism is not required. Hsieh CL, McCloskey RP, Radany E, Lieber MR. 1991 Mol Cell Biol. 11(8):3972-7.

 

Ancient Publications

Abnormal V(D)J recombination in murine severe combined immune deficiency: absence of coding joints and formation of alternative products. Lieber MR, Hesse JE, Lewis S, Bosma GC, Rosenberg N, Mizuuchi K, Bosma MJ, Gellert M. 1989 Curr Top Microbiol Immunol. 152:69-75.

Hemolytic holes in human erythrocyte membrane ghosts. Lieber MR, Steck TL. 1989 Methods Enzymol. 173:356-67.

Lymphoid V(D)J recombination: nucleotide insertion at signal joints as well as coding joints. Lieber MR, Hesse JE, Mizuuchi K, Gellert M. 1988 Proc Natl Acad Sci U S A. 85(22):8588-92.

The defect in murine severe combined immune deficiency: joining of signal sequences but not coding segments in V(D)J recombination. Lieber MR, Hesse JE, Lewis S, Bosma GC, Rosenberg N, Mizuuchi K, Bosma MJ, Gellert M. 1988 Cell. 55(1):7-16.

Studies of V(D)J recombination with extrachromosomal substrates. Lieber MR, Hesse JE, Mizuuchi K, Gellert M. 1988 Curr Top Microbiol Immunol. 137:94-9.

Developmental stage specificity of the lymphoid V(D)J recombination activity. Lieber MR, Hesse JE, Mizuuchi K, Gellert M. 1987 Genes Dev. 1(8):751-61.

The mechanism of osmotic transfection of avian embryonic erythrocytes: analysis of a system for studying developmental gene expression. Lieber MR, Hesse JE, Nickol JM, Felsenfeld G. 1987 J Cell Biol. 105(3):1055-65.

Solid and papillary epithelial neoplasm of the pancreas. An ultrastructural and immunocytochemical study of six cases. Lieber MR, Lack EE, Roberts JR Jr, Merino MJ, Patterson K, Restrepo C, Solomon D, Chandra R, Triche TJ. 1987 Am J Surg Pathol. 11(2):85-93.

Interaction of chlorpromazine with the human erythrocyte membrane. Lieber MR, Lange Y, Weinstein RS, Steck TL. 1984 J Biol Chem. 259(14):9225-34.

A description of the holes in human erythrocyte membrane ghosts. Lieber MR, Steck TL. 1984 J Biol Chem. 257(19):11651-9.

Dynamics of the holes in human erythrocyte membrane ghosts. Lieber MR, Steck TL. 1982 J Biol Chem. 257(19):11660-6.

 

Reviews and Commentaries

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. Tsai AG, Lu Z, Lieber MR. 2010 Blood. 115(17):3640-1

NHEJ and its backup pathways in chromosomal translocations. Lieber MR. 2010 Nat Struct Mol Biol. 17(4):393-5.

The Mechanism of Double-Strand DNA Break Repair by the Nonhomologous DNA End-Joining Pathway. Lieber MR. 2010 Annu Rev Biochem. Epub ahead of print

Mechanisms of chromosomal rearrangement in the human genome. Tsai AG, Lieber MR. 2010 BMC Genomics. 11 Suppl 1:S1.

Nonhomologous DNA End Joining (NHEJ) and Chromosomal Translocations in Humans. Lieber MR, Gu J, Lu H, Shimazaki N, Tsai AG. 2010 Subcell Biochem. 50:279-96.

Mechanistic aspects of lymphoid chromosomal translocations. Lieber MR, Raghavan SC, Yu K. 2008 J Natl Cancer Inst Monogr. (39):8-11

DNA-PKcs at 7A: insights for DNA repair. Shimazaki N, Lieber MR. 2008 Structure. 16(3):334-6.

Mechanistic flexibility as a conserved theme across 3 billion years of nonhomologous DNA end-joining. Gu J, Lieber MR. 2008 Genes Dev. 22(4):411-5.

RAGs found "not guilty": cleared by DNA evidence. Tsai AG, Lieber MR. 2008 Blood. 111(4):1750.

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. Lieber MR, Lu H, Gu J, Schwarz K. 2008 Cell Res. 18(1):125-33.

The mechanism of human nonhomologous DNA end joining. Lieber MR. 2008 J Biol Chem. 283(1):1-5.

DNA structure and human diseases. Raghavan SC, Lieber MR. 2007 Front Biosci. 12:4402-8.

The polymerases for V(D)J recombination. Lieber MR. 2006 Immunity. 25(1):7-9.

Detection and structural analysis of R-loops. Yu K, Roy D, Huang FT, Lieber MR. 2006 Methods Enzymol. 409:316-29.

Analysis of non-B DNA structure at chromosomal sites in the mammalian genome. Raghavan SC, Tsai A, Hsieh CL, Lieber MR. 2006 Methods Enzymol. 409:301-16.

Roles of nonhomologous DNA end joining, V(D)J recombination, and class switch recombination in chromosomal translocations. Lieber MR, Yu K, Raghavan SC. 2006 DNA Repair (Amst). 5(9-10):1234-45.

DNA structures at chromosomal translocation sites. Raghavan SC, Lieber MR. 2006 Bioessays. 28(5):480-94.

In vitro nonhomologous DNA end joining system. Ma Y, Lieber MR. 2006 Methods Enzymol. 408:502-10.

Repair of double-strand DNA breaks by the human nonhomologous DNA end joining pathway: the iterative processing model. Ma Y, Lu H, Schwarz K, Lieber MR. 2005 Cell Cycle. 4(9):1193-200.

The mechanism of vertebrate nonhomologous DNA end joining and its role in V(D)J recombination. Lieber MR, Ma Y, Pannicke U, Schwarz K. 2004 DNA Repair (Amst). 3(8-9):817-26.

DNA damage and aging. Karanjawala ZE, Lieber MR. 2004 Mech Ageing Dev. 125(6):405-16.

Chromosomal translocations and non-B DNA structures in the human genome. Raghavan SC, Lieber MR. 2004 Cell Cycle. 3(6):762-8.

Ageing, repetitive genomes and DNA damage. Lieber MR, Karanjawala ZE. 2004 Nat Rev Mol Cell Biol. 5(1):69-75.

Nucleic acid structures and enzymes in the immunoglobulin class switch recombination mechanism. Yu K, Lieber MR. 2003 DNA Repair (Amst). 2(11):1163-74.

Human severe combined immune deficiency and DNA repair. Schwarz K, Ma Y, Pannicke U, Lieber MR. 2003 Bioessays. 25(11):1061-70.

Mechanism and regulation of human non-homologous DNA end-joining. Lieber MR, Ma Y, Pannicke U, Schwarz K. 2003 Nat Rev Mol Cell Biol. 4(9):712-20.

The biochemistry and biological significance of nonhomologous DNA end joining: an essential repair process in multicellular eukaryotes. Lieber MR. 1999 Genes Cells. 4(2):77-85.

Warner-Lambert/Parke-Davis Award Lecture. Pathological and physiological double-strand breaks: roles in cancer, aging, and the immune system. Lieber MR. 1998 Am J Pathol. 153(5):1323-32.

Antigen receptor gene rearrangement. Grawunder U, West RB, Lieber MR. 1998 Curr Opin Immunol. 10(2):172-80.

The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. Lieber MR. 1997 Bioessays. 19(3):233-40.

Tying loose ends: roles of Ku and DNA-dependent protein kinase in the repair of double-strand breaks. Lieber MR, Grawunder U, Wu X, Yaneva M. 1997 Curr Opin Genet Dev. 7(1):99-104.

The mechanism of V(D)J recombination: site-specificity, reaction fidelity and immunologic diversity. Lieber MR, Chang CP, Gallo M, Gauss G, Gerstein R, Islas A. 1994 Semin Immunol. 6(3):143-53.

The mechanism of V(D)J recombination: a balance of diversity, specificity, and stability. Lieber MR. 1992 Cell. 70(6):873-6.

Replication, transcription, CpG methylation and DNA topology in V(D)J recombination. Hsieh CL, Gauss G, Lieber MR. 1992 Curr Top Microbiol Immunol. 182:125-35.

Site-specific recombination in the immune system. Lieber MR. 1991 FASEB J. 5(14):2934-44.

 

Coauthorships

Cytosines, but not purines, determine RAG induced breaks on heteroduplex DNA structures: Implications for genomic instability. Naik AK, Lieber MR, Raghavan SC. 2010 J Biol Chem. 285(10):7587-97.

The B cell mutator AID promotes B lymphoid blast crisis and drug resistance in chronic myeloid leukemia. 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. 2009 Cancer Cell. 16(3):232-45.

Turning anti-ageing genes against cancer. Longo VD, Lieber MR, Vijg J. 2008 Nat Rev Mol Cell Biol. 9(11):903-10.

Unexpected complexity at breakpoint junctions in phenotypically normal individuals and mechanisms involved in generating balanced translocations t(1;22)(p36;q13). Gajecka M, Gentles AJ, Tsai A, Chitayat D, Mackay KL, Glotzbach CD, Lieber MR, Shaffer LG. 2008 Genome Res. 18(11):1733-42.

FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Heo K, Kim H, Choi SH, Choi J, Kim K, Gu J, Lieber MR, Yang AS, An W. 2008 Mol Cell. 30(1):86-97.

DNA-PKcs dependence of Artemis endonucleolytic activity, differences between hairpins and 5' or 3' overhangs. Niewolik D, Pannicke U, Lu H, Ma Y, Wang LC, Kulesza P, Zandi E, Lieber MR, Schwarz K. 2006 J Biol Chem. 281(45):33900-9.

Severe combined immunodeficiency and microcephaly in siblings with hypomorphic mutations in DNA ligase IV. Buck D, Moshous D, de Chasseval R, Ma Y, le Deist F, Cavazzana-Calvo M, Fischer A, Casanova JL, Lieber MR, de Villartay JP. 2006 Eur J Immunol. 36(1):224-35.

Omenn syndrome due to ARTEMIS mutations. Ege M, Ma Y, Manfras B, Kalwak K, Lu H, Lieber MR, Schwarz K, Pannicke U. 2005 Blood. 105(11):4179-86.

Genetic interactions between BLM and DNA ligase IV in human cells. So S, Adachi N, Lieber MR, Koyama H. 2004 J Biol Chem. 279(53):55433-42.

Stability and strand asymmetry in the non-B DNA structure at the bcl-2 major breakpoint region. Raghavan SC, Houston S, Hegde BG, Langen R, Haworth IS, Lieber MR. 2004 J Biol Chem. 279(44):46213-25.

Functional and biochemical dissection of the structure-specific nuclease ARTEMIS. Pannicke U, Ma Y, Hopfner KP, Niewolik D, Lieber MR, Schwarz K. 2004 EMBO J. 23(9):1987-97.

Impact of DNA ligase IV on the fidelity of end joining in human cells. Smith J, Riballo E, Kysela B, Baldeyron C, Manolis K, Masson C, Lieber MR, Papadopoulo D, Jeggo P. 2003 Nucleic Acids Res. 31(8):2157-67.

The DNA methyltransferase-like protein DNMT3L stimulates de novo methylation by Dnmt3a. Chedin F, Lieber MR, Hsieh CL. 2002 Proc Natl Acad Sci U S A. 99(26):16916-21.

Prevalent involvement of illegitimate V(D)J recombination in chromosome 9p21 deletions in lymphoid leukemia. Kitagawa Y, Inoue K, Sasaki S, Hayashi Y, Matsuo Y, Lieber MR, Mizoguchi H, Yokota J, Kohno T. 2002 J Biol Chem. 277(48):46289-97.

The role of recombination signal sequences in the preferential joining by deletion in DH-JH recombination and in the ordered rearrangement of the IgH locus. Pan PY, Lieber MR, Teale JM. 1997 Int Immunol. 9(4):515-22.

RAG mutations in human B cell-negative SCID. Schwarz K, Gauss GH, Ludwig L, Pannicke U, Li Z, Lindner D, Friedrich W, Seger RA, Hansen-Hagge TE, Desiderio S, Lieber MR, Bartram CR. 1996 Science. 274(5284):97-9.

Human DNA-activated protein kinase (DNA-PK) is homologous to phosphatidylinositol kinases. Poltoratsky VP, Shi X, York JD, Lieber MR, Carter TH. 1995 J Immunol. 155(10):4529-33.

Sequence of human FEN-1, a structure-specific endonuclease, and chromosomal localization of the gene (FEN1) in mouse and human. Hiraoka LR, Harrington JJ, Gerhard DS, Lieber MR, Hsieh CL. 1995 Genomics. 25(1):220-5.

Restoration of X-ray resistance and V(D)J recombination in mutant cells by Ku cDNA. Smider V, Rathmell WK, Lieber MR, Chu G. 1994 Science. 266(5183):288-91.

Transcription, topoisomerases and recombination. Gangloff S, Lieber MR, Rothstein R. 1994 Experientia. 50(3):261-9.

V(D)J recombination: a functional definition of the joining signals. Hesse JE, Lieber MR, Mizuuchi K, Gellert M. 1989 Genes Dev. 3(7):1053-61.

Extrachromosomal DNA substrates in pre-B cells undergo inversion or deletion at immunoglobulin V-(D)-J joining signals. Hesse JE, Lieber MR, Gellert M, Mizuuchi K. 1987 Cell. 49(6):775-83.

Electropore diameters, lifetimes, numbers, and locations in individual erythrocyte ghosts. Sowers AE, Lieber MR. 1986 FEBS Lett. 205(2):179-84.

Regulated gene expression in transfected primary chicken erythrocytes. Hesse JE, Nickol JM, Lieber MR, Felsenfeld G. 1986 Proc Natl Acad Sci U S A. 83(12):4312-6.

Effects of cyclosporine A on biomembranes. Vibrational spectroscopic, calorimetric and hemolysis studies. O'Leary TJ, Ross PD, Lieber MR, Levin IW. 1986 Biophys J. 49(4):795-801.

Malignant thoracopulmonary small-cell ("Askin") tumor. Fink IJ, Kurtz DW, Cazenave L, Lieber MR, Miser JS, Chandra R, Triche TJ. 1985 AJR Am J Roentgenol. 145(3):517-20.

 

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