David G. Schatz, PhD
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Research Summary
Generating a Diverse and Effective Repertoire of Antibodies During an Immune Response:
The Schatz laboratory studies V(D)J recombination and somatic hypermutation, reactions that create and optimize antibody genes. Antibodies are blood proteins produced by B cells that are important for fighting infectious disease. V(D)J recombination puts antibody genes together from small pieces of chromosomal DNA, while somatic hypermutation makes mutations in antibody genes and allows for the generation of antibodies that bind viruses and bacteria very tightly. We study these reactions using a wide variety of molecular, genetic, cellular, and biochemical approaches. The focus of our research is understanding the underlying mechanisms of these reactions and how they are targeted specifically to antibody genes. We are also interested in understanding why V(D)J recombination and somatic hypermutation sometimes affect the wrong genes, and how such mistakes contribute to the development of B cell cancers known as lymphomas and leukemias. Finally, we are interested in the evolutionary origins of V(D)J recombination, and study transposons that are thought to be evolutionary relatives of RAG1 and RAG2.
Extensive Research Description
Generating a Diverse and Effective Repertoire of Antigen-Specific Receptors During Development of the Immune System
The B and T lymphocytes that constitute the adaptive immune system make use of antigen receptor molecules, known as immunoglobulins and T cell receptors, to combat viral and bacterial infections. Each of the hundreds of millions of lymphocytes expresses a different antigen receptor on its surface, indicative of an extraordinary level of diversity in these receptors. The fundamental interest of our lab is to understand the two major processes that generate this diversity: V(D)J recombination and somatic hypermutation.
V(D)J recombination assembles immunoglobulin and T cell receptor genes from component V (variable), D (diversity), and J (joining) gene segments in developing B and T cells. In the first phase of the reaction, two DNA segments are bound by the recombination machinery, brought into close physical proximity, and the DNA is cleaved. In the second phase, the DNA ends are processed and joined by the cellular DNA repair machinery to form the reaction products.
One of our major interests is the enzymatic mechanism of the first phase of V(D)J recombination, which is catalyzed by the proteins encoded by the recombination-activating genes, RAG1 and RAG2. We are studying how the RAG proteins bend and twist the substrate DNA during DNA cleavage and are using a variety of ensemble and single molecule biophysical assays to characterize the structure, composition, and stability of the DNA complexes formed by RAG1/RAG2.
We have used chromatin immunoprecipitation (ChIP) to demonstrate that the RAG proteins associate with one small, discrete region of each antigen receptor locus. These regions, which we refer to as recombination centers, are rich in activating histone modifications and RNA polymerase II. We propose that recombination centers are specialized sites within which the RAG proteins bind one DNA segment and then capture a second to allow for recombination. We have also demonstrated that RAG1 and RAG2 bind to thousands of other sites in the genome, almost entirely at active promoters and enhancers. Computational analysis suggests that RAG binding is driven by interactions with chromatin proteins including modified histone tails, and that this is mediated by regulatory regions in both RAG1 and RAG2. We are now working to understand the molecular interactions that mediate RAG binding patterns and the implications of wide-spread RAG binding for genome stability in developing lymphocytes.
We have a long standing interest in the evolutionary origins of RAG1 and RAG2, beginning with our demonstration in 1998 that these proteins possess cut-and-paste DNA transposase activity. We are studying evolutionarily related transposases from a wide range of invertebrate species, which has led to significant progress in understanding the steps that led to domestication of the ancient RAG transposase and evolution of our adaptive immune system.
Somatic hypermutation (SHM) introduces point mutations into the variable regions of immunoglobulin genes in B cells during an immune response. These mutations allow for the generation of B cells expressing antibodies with high affinity for an invading microorganism, a process known as affinity maturation. This process is important for the "memory" of the immune system, which helps protect individuals from recurrent infections with the same microorganism, and underlies the success of many vaccines.
SHM is initiated by an enzyme known as activation-induced deaminase (AID), which deaminates cytosine to create uracil in immunoglobulin genes. The uracil is then processed by the mismatch and base excision repair pathways to create mutations at the site of deamination and at nearby sites in the DNA. SHM has been linked to genomic instability and B cell cancers, and our lab is interested in understanding how the reaction is targeted to immunoglobulin loci and how the rest of the genome is protected from its deleterious effects. We have demonstrated that immunoglobulin enhancer elements function as SHM targeting elements (which we refer to as DIVAC--diversification activator) and are very likely responsible for the high efficiency with which immunoglobulin genes undergo SHM. We are studying the protein factors that bind to DIVAC and attempting to understand the mechanism by which they enhance SHM. In addition, we have developed rapid cell based assays for SHM that have opened the door for CRISPR screens and degron approaches for discovery and analysis of factors involved in SHM. We make use of epigenetic, genome architecture, and computational approaches to determine the rules that dictate susceptibility to AID/SHM.
Coauthors
Research Interests
Antibody Diversity; Antibody Formation; Biological Evolution; Genes, Immunoglobulin; Leukemia, Lymphoid; Lymphoma, Non-Hodgkin; Molecular Biology; Gene Rearrangement, B-Lymphocyte; Gene Rearrangement, T-Lymphocyte; Developmental Biology; Somatic Hypermutation, Immunoglobulin
Research Image
Structures of Transib Transposase, an early ancestor of RAG1 (PMID 31723264)
Selected Publications
- HMCES protects immunoglobulin genes specifically from deletions during somatic hypermutationWu L, Shukla V, Yadavalli AD, Dinesh RK, Xu D, Rao A, Schatz DG. HMCES protects immunoglobulin genes specifically from deletions during somatic hypermutation Genes & Development 2022, 36: 433-450. PMID: 35450882, PMCID: PMC9067407, DOI: 10.1101/gad.349438.122.
- Abstract PO-23: Somatic hypermutation is perturbed in ABC-DLBCL lymphoma cell lines expressing high levels of activation-induced deaminaseSaribasak H, Dinesh R, Wu L, Schatz D. Abstract PO-23: Somatic hypermutation is perturbed in ABC-DLBCL lymphoma cell lines expressing high levels of activation-induced deaminase Blood Cancer Discovery 2020, 1: po-23-po-23. DOI: 10.1158/2643-3249.lymphoma20-po-23.
- Topologically Associated Domains Delineate Susceptibility to Somatic HypermutationSenigl F, Maman Y, Dinesh RK, Alinikula J, Seth RB, Pecnova L, Omer AD, Rao SSP, Weisz D, Buerstedde JM, Aiden EL, Casellas R, Hejnar J, Schatz DG. Topologically Associated Domains Delineate Susceptibility to Somatic Hypermutation Cell Reports 2019, 29: 3902-3915.e8. PMID: 31851922, PMCID: PMC6980758, DOI: 10.1016/j.celrep.2019.11.039.
- Structures of a RAG-like transposase during cut-and-paste transpositionLiu C, Yang Y, Schatz DG. Structures of a RAG-like transposase during cut-and-paste transposition Nature 2019, 575: 540-544. PMID: 31723264, PMCID: PMC6872938, DOI: 10.1038/s41586-019-1753-7.
- Transposon molecular domestication and the evolution of the RAG recombinaseZhang Y, Cheng TC, Huang G, Lu Q, Surleac MD, Mandell JD, Pontarotti P, Petrescu AJ, Xu A, Xiong Y, Schatz DG. Transposon molecular domestication and the evolution of the RAG recombinase Nature 2019, 569: 79-84. PMID: 30971819, PMCID: PMC6494689, DOI: 10.1038/s41586-019-1093-7.
- Skewing the Playing Field: A Single-Molecule Study on how RSS Sequence Influences Gene Segment SelectionHirokawa S, Belliveau N, Lovely G, Anaya M, Schatz D, Baltimore D, Phillips R. Skewing the Playing Field: A Single-Molecule Study on how RSS Sequence Influences Gene Segment Selection Biophysical Journal 2018, 114: 86a. DOI: 10.1016/j.bpj.2017.11.511.
- The Role of RAG in V(D)J RecombinationCarmona L, Schatz D. The Role of RAG in V(D)J Recombination 2016, 99-106. DOI: 10.1016/b978-0-12-374279-7.05012-8.
- Abstract A180: Topologically associated domains genome-wide restrict the off-target activity of recombination activating gene 1/2 endonucleaseHu J, Zhang Y, Zhao L, Frock R, Du Z, Meyers R, Meng F, Schatz D, Alt F. Abstract A180: Topologically associated domains genome-wide restrict the off-target activity of recombination activating gene 1/2 endonuclease Cancer Immunology Research 2016, 4: a180-a180. DOI: 10.1158/2326-6074.cricimteatiaacr15-a180.
- Exposure to Inflammatory Immune Responses As Driver of Clonal Evolution in Childhood Acute Lymphoblastic LeukemiaKlemm L, Swaminathan S, Papaemmanuil E, Ford A, Greaves M, Casellas R, Schatz D, Lieber M, Muschen M. Exposure to Inflammatory Immune Responses As Driver of Clonal Evolution in Childhood Acute Lymphoblastic Leukemia Blood 2015, 126: 166-166. DOI: 10.1182/blood.v126.23.166.166.
- RAG Represents a Widespread Threat to the Lymphocyte GenomeTeng G, Maman Y, Resch W, Kim M, Yamane A, Qian J, Kieffer-Kwon KR, Mandal M, Ji Y, Meffre E, Clark MR, Cowell LG, Casellas R, Schatz DG. RAG Represents a Widespread Threat to the Lymphocyte Genome Cell 2015, 162: 751-765. PMID: 26234156, PMCID: PMC4537821, DOI: 10.1016/j.cell.2015.07.009.
- Chapter 2 The Mechanism of V(D)J RecombinationLittle A, Matthews A, Oettinger M, Roth D, Schatz D. Chapter 2 The Mechanism of V(D)J Recombination 2015, 13-34. DOI: 10.1016/b978-0-12-397933-9.00002-3.
- Mechanisms of Clonal Evolution of Pre-Leukemic Clones in Childhood Pre-B Acute Lymphoblastic LeukemiaSwaminathan S, Klemm L, Park E, Ford A, Kweon S, Trageser D, Hasselfeld B, Henke N, Geng H, Schwarz K, Casellas R, Schatz D, Lieber M, Papaemmanuil E, Greaves M, Muschen M. Mechanisms of Clonal Evolution of Pre-Leukemic Clones in Childhood Pre-B Acute Lymphoblastic Leukemia Blood 2014, 124: 861-861. DOI: 10.1182/blood.v124.21.861.861.
- Targeting Of Somatic Hypermutation By immunoglobulin Enhancer And Enhancer-Like SequencesBuerstedde JM, Alinikula J, Arakawa H, McDonald JJ, Schatz DG. Targeting Of Somatic Hypermutation By immunoglobulin Enhancer And Enhancer-Like Sequences PLOS Biology 2014, 12: e1001831. PMID: 24691034, PMCID: PMC3972084, DOI: 10.1371/journal.pbio.1001831.
- Single Molecule Dynamics Governing the Initiation of V(D)J RecombinationLovely G, Linden M, Ramesh P, Schatz D, Baltimore D, Phillips R. Single Molecule Dynamics Governing the Initiation of V(D)J Recombination Biophysical Journal 2014, 106: 692a. DOI: 10.1016/j.bpj.2013.11.3826.
- Protecting the Genome: Mechanisms Targeting Somatic HypermutationSchatz D, Buerstedde J, Alinikula J, McDonald J, Kohler K, Arakawa H. Protecting the Genome: Mechanisms Targeting Somatic Hypermutation Blood 2013, 122: sci-13-sci-13. DOI: 10.1182/blood.v122.21.sci-13.sci-13.
- Recombination in the Immune SystemTeng G, Schatz D. Recombination in the Immune System 2013, 89-91. DOI: 10.1016/b978-0-12-374984-0.01279-1.
- Cooperation Between Aid and the Rag1/Rag2 V(D)J Recombinase Drives Clonal Evolution of Childhood Acute Lymphoblastic LeukemiaSwaminathan S, Klemm L, Ford A, Schwarz K, Casellas R, Hennighausen L, Geng H, Schatz D, Lieber M, Greaves M, Muschen M. Cooperation Between Aid and the Rag1/Rag2 V(D)J Recombinase Drives Clonal Evolution of Childhood Acute Lymphoblastic Leukemia Blood 2012, 120: 519-519. DOI: 10.1182/blood.v120.21.519.519.
- Abstract 309: Induction of activation-induced cytidine deaminase (AID) by dendritic cells leads to genomic instability in human myelomaKoduru S, Wong E, Strowig T, Sundaram R, Zhang L, Strout M, Flavell R, Schatz D, Dhodapkar K, Dhodapkar M. Abstract 309: Induction of activation-induced cytidine deaminase (AID) by dendritic cells leads to genomic instability in human myeloma Cancer Research 2012, 72: 309-309. DOI: 10.1158/1538-7445.am2012-309.
- The Role of DNA Repair in the Pathogenesis of Activation Induced Cytidine Deaminase Dependent B Cell LymphomaGu X, Booth C, Schatz D, Strout M. The Role of DNA Repair in the Pathogenesis of Activation Induced Cytidine Deaminase Dependent B Cell Lymphoma Blood 2011, 118: 397-397. DOI: 10.1182/blood.v118.21.397.397.
- Regulation of the Mutation Threshold During Immune Diversification by Activation Induced Cytidine Deaminase,Strout M, Philip N, Schatz D. Regulation of the Mutation Threshold During Immune Diversification by Activation Induced Cytidine Deaminase, Blood 2011, 118: 3244-3244. DOI: 10.1182/blood.v118.21.3244.3244.
- Infectious Origins of Childhood LeukemiaKlemm L, Swaminathan S, Ford A, Schwarz K, Schatz D, Lieber M, Greaves M, Muschen M. Infectious Origins of Childhood Leukemia Blood 2011, 118: 751-751. DOI: 10.1182/blood.v118.21.751.751.
- IL7Rα Signaling Prevents Premature Expression of AID In Human Pre-B Cells: Implications for Clonal Evolution of Childhood LeukemiaSwaminathan S, Klemm L, Kweon S, Ford A, Schwarz K, Casellas R, Hennighausen L, Schatz D, Lieber M, Greaves M, Muschen M. IL7Rα Signaling Prevents Premature Expression of AID In Human Pre-B Cells: Implications for Clonal Evolution of Childhood Leukemia Blood 2010, 116: 26-26. DOI: 10.1182/blood.v116.21.26.26.
- The In Vivo Pattern of Binding of RAG1 and RAG2 to Antigen Receptor LociJi Y, Resch W, Corbett E, Yamane A, Casellas R, Schatz D. The In Vivo Pattern of Binding of RAG1 and RAG2 to Antigen Receptor Loci Cell 2010, 143: 170. DOI: 10.1016/j.cell.2010.09.020.
- The In Vivo Pattern of Binding of RAG1 and RAG2 to Antigen Receptor LociJi Y, Resch W, Corbett E, Yamane A, Casellas R, Schatz DG. The In Vivo Pattern of Binding of RAG1 and RAG2 to Antigen Receptor Loci Cell 2010, 141: 419-431. PMID: 20398922, PMCID: PMC2879619, DOI: 10.1016/j.cell.2010.03.010.
- Erratum: Corrigendum: RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin lociHewitt S, Yin B, Ji Y, Chaumeil J, Marszalek K, Tenthorey J, Salvagiotto G, Steinel N, Ramsey L, Ghysdael J, Farrar M, Sleckman B, Schatz D, Busslinger M, Bassing C, Skok J. Erratum: Corrigendum: RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin loci Nature Immunology 2010, 11: 356-356. DOI: 10.1038/ni0410-356.
- Addendum: RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin lociHewitt S, Yin B, Ji Y, Chaumeil J, Marszalek K, Tenthorey J, Salvagiotto G, Steinel N, Ramsey L, Ghysdael J, Farrar M, Sleckman B, Schatz D, Busslinger M, Bassing C, Skok J. Addendum: RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin loci Nature Immunology 2010, 11: 355-356. DOI: 10.1038/ni0410-355.
- Negative Regulation of Activation-Induced Cytidine Deaminase Protein Prevents Aberrant Somatic Hypermutation and Lymphomagenesis.Strout M, Schatz D. Negative Regulation of Activation-Induced Cytidine Deaminase Protein Prevents Aberrant Somatic Hypermutation and Lymphomagenesis. Blood 2009, 114: 94-94. DOI: 10.1182/blood.v114.22.94.94.
- Erratum: Corrigendum: RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin lociHewitt S, Yin B, Ji Y, Chaumeil J, Marszalek K, Tenthorey J, Salvagiotto G, Steinel N, Ramsey L, Ghysdael J, A Farrar M, Sleckman B, Schatz D, Busslinger M, Bassing C, Skok J. Erratum: Corrigendum: RAG-1 and ATM coordinate monoallelic recombination and nuclear positioning of immunoglobulin loci Nature Immunology 2009, 10: 1034-1034. DOI: 10.1038/ni0909-1034.
- A Role for Small RNA Molecules during the DNA Repair Phase of Somatic HypermutationStrout M, Schatz D. A Role for Small RNA Molecules during the DNA Repair Phase of Somatic Hypermutation Blood 2008, 112: 785-785. DOI: 10.1182/blood.v112.11.785.785.
- Understanding the spread of mutations during somatic hypermutationUnniraman S, Schatz D. Understanding the spread of mutations during somatic hypermutation The FASEB Journal 2008, 22: 849.3-849.3. DOI: 10.1096/fasebj.22.1_supplement.849.3.
- Two levels of protection for the B cell genome during somatic hypermutationLiu M, Duke JL, Richter DJ, Vinuesa CG, Goodnow CC, Kleinstein SH, Schatz DG. Two levels of protection for the B cell genome during somatic hypermutation Nature 2008, 451: 841-845. PMID: 18273020, DOI: 10.1038/nature06547.
- Probing the structure of RAG protein‐DNA intermediates in V(D)J recombinationSchatz D, Ciubotaru M. Probing the structure of RAG protein‐DNA intermediates in V(D)J recombination The FASEB Journal 2007, 21: a44-a44. DOI: 10.1096/fasebj.21.5.a44-d.
- Response to 'Amplifying Igh translocations'Unniraman S, Zhou S, Schatz D. Response to 'Amplifying Igh translocations' Nature Immunology 2005, 6: 118-118. DOI: 10.1038/ni0205-118.
- Cloning of Apoptosis-Related Genes by Representational Difference Analysis of cDNAHubank M, Bryntesson F, Regan J, Schatz D. Cloning of Apoptosis-Related Genes by Representational Difference Analysis of cDNA 2004, 282: 255-273. DOI: 10.1385/1-59259-812-9:255.
- Charles A. Janeway, Jr. (1943-2003)Bottomly K, Cresswell P, Flavell R, Ghosh S, Pober J, Schatz D. Charles A. Janeway, Jr. (1943-2003) Immunity 2003, 18: 591-592. DOI: 10.1016/s1074-7613(03)00123-7.
- Charles A. Janeway, Jr. (1943-2003)Bottomly K, Cresswell P, Flavell R, Ghosh S, Pober J, Schatz D. Charles A. Janeway, Jr. (1943-2003) Cell 2003, 113: 433-434. DOI: 10.1016/s0092-8674(03)00361-1.
- Lymphocyte developmentSchatz D, Malissen B. Lymphocyte development Current Opinion In Immunology 2002, 14: 183-185. DOI: 10.1016/s0952-7915(02)00319-9.
- V(D)J RecombinationSchatz D. V(D)J Recombination 2002 DOI: 10.1002/0471203076.emm0506.
- Recombination Activating Genes, RAG1 and RAG2Schatz D. Recombination Activating Genes, RAG1 and RAG2 2002 DOI: 10.1002/0471203076.emm0505.
- Identification of Basic Residues in RAG2 Critical for DNA Binding by the RAG1-RAG2 ComplexFugmann S, Schatz D. Identification of Basic Residues in RAG2 Critical for DNA Binding by the RAG1-RAG2 Complex Molecular Cell 2001, 8: 899-910. PMID: 11684024, DOI: 10.1016/s1097-2765(01)00352-5.
- Location, location, location: the cell biology of immunoglobulin allelic controlHesslein D, Fields P, Schatz D. Location, location, location: the cell biology of immunoglobulin allelic control Nature Immunology 2001, 2: 825-826. PMID: 11526394, DOI: 10.1038/ni0901-825.
- Factors and Forces Controlling V(D)J RecombinationHesslein D, Schatz D. Factors and Forces Controlling V(D)J Recombination 2001, 78: 169-232. PMID: 11432204, DOI: 10.1016/s0065-2776(01)78004-2.
- Cell-cycle-regulated DNA double-strand breaks in somatic hypermutation of immunoglobulin genesPapavasiliou F, Schatz D. Cell-cycle-regulated DNA double-strand breaks in somatic hypermutation of immunoglobulin genes Nature 2000, 408: 216-221. PMID: 11089977, DOI: 10.1038/35041599.
- Genetic Modulation of T Cell Receptor Gene Segment Usage during Somatic RecombinationLivak F, Burtrum D, Rowen L, Schatz D, Petrie H. Genetic Modulation of T Cell Receptor Gene Segment Usage during Somatic Recombination Journal Of Experimental Medicine 2000, 192: 1191-1196. PMID: 11034609, PMCID: PMC2195867, DOI: 10.1084/jem.192.8.1191.
- The RAG Proteins and V(D)J Recombination: Complexes, Ends, and TranspositionFugmann S, Lee A, Shockett P, Villey I, Schatz D. The RAG Proteins and V(D)J Recombination: Complexes, Ends, and Transposition Annual Review Of Immunology 2000, 18: 495-527. PMID: 10837067, DOI: 10.1146/annurev.immunol.18.1.495.
- Intermolecular V(D)J Recombination*Tevelev A, Schatz D. Intermolecular V(D)J Recombination* Journal Of Biological Chemistry 2000, 275: 8341-8348. PMID: 10722664, DOI: 10.1074/jbc.275.12.8341.
- Identification of Two Catalytic Residues in RAG1 that Define a Single Active Site within the RAG1/RAG2 Protein ComplexFugmann S, Villey I, Ptaszek L, Schatz D. Identification of Two Catalytic Residues in RAG1 that Define a Single Active Site within the RAG1/RAG2 Protein Complex Molecular Cell 2000, 5: 97-107. PMID: 10678172, DOI: 10.1016/s1097-2765(00)80406-2.
- Developing B-cell theoriesSchatz D. Developing B-cell theories Nature 1999, 400: 615-617. PMID: 10458155, DOI: 10.1038/23134.
- A dimer of the lymphoid protein RAG1 recognizes the recombination signal sequence and the complex stably incorporates the high mobility group protein HMG2Rodgers K, Villey I, Ptaszek L, Corbett E, Schatz D, Coleman J. A dimer of the lymphoid protein RAG1 recognizes the recombination signal sequence and the complex stably incorporates the high mobility group protein HMG2 Nucleic Acids Research 1999, 27: 2938-2946. PMID: 10390537, PMCID: PMC148510, DOI: 10.1093/nar/27.14.2938.
- DNA Hairpin Opening Mediated by the RAG1 and RAG2 ProteinsShockett P, Schatz D. DNA Hairpin Opening Mediated by the RAG1 and RAG2 Proteins Molecular And Cellular Biology 1999, 19: 4159-4166. PMID: 10330156, PMCID: PMC104375, DOI: 10.1128/mcb.19.6.4159.
- Transposition mediated by RAG1 and RAG2 and the evolution of the adaptive immune systemSchatz D. Transposition mediated by RAG1 and RAG2 and the evolution of the adaptive immune system Immunologic Research 1999, 19: 169-182. PMID: 10493171, DOI: 10.1007/bf02786485.
- Detection of RAG Protein-V(D)J Recombination Signal Interactions Near the Site of DNA Cleavage by UV Cross-LinkingEastman Q, Villey I, Schatz D. Detection of RAG Protein-V(D)J Recombination Signal Interactions Near the Site of DNA Cleavage by UV Cross-Linking Molecular And Cellular Biology 1999, 19: 3788-3797. PMID: 10207102, PMCID: PMC84213, DOI: 10.1128/mcb.19.5.3788.
- Developmental neurobiology: Alternative ends for a familiar story?Chun J, Schatz D. Developmental neurobiology: Alternative ends for a familiar story? Current Biology 1999, 9: r251-r253. PMID: 10209111, DOI: 10.1016/s0960-9822(99)80156-0.
- Rearranging Views on Neurogenesis Neuronal Death in the Absence of DNA End-Joining ProteinsChun J, Schatz D. Rearranging Views on Neurogenesis Neuronal Death in the Absence of DNA End-Joining Proteins Neuron 1999, 22: 7-10. PMID: 10027282, DOI: 10.1016/s0896-6273(00)80671-6.
- Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune systemAgrawal A, Eastman Q, Schatz D. Transposition mediated by RAG1 and RAG2 and its implications for the evolution of the immune system Nature 1998, 394: 744-751. PMID: 9723614, DOI: 10.1038/29457.
- Alternative splicing of rearranged T cell receptor δ sequences to the constant region of the α locusLivák F, Schatz D. Alternative splicing of rearranged T cell receptor δ sequences to the constant region of the α locus Proceedings Of The National Academy Of Sciences Of The United States Of America 1998, 95: 5694-5699. PMID: 9576946, PMCID: PMC20441, DOI: 10.1073/pnas.95.10.5694.
- Nicking is asynchronous and stimulated by synapsis in 12/23 rule-regulated V(D)J cleavageEastman Q, Schatz D. Nicking is asynchronous and stimulated by synapsis in 12/23 rule-regulated V(D)J cleavage Nucleic Acids Research 1997, 25: 4370-4378. PMID: 9336470, PMCID: PMC147051, DOI: 10.1093/nar/25.21.4370.
- αβ Lineage‐committed thymocytes can be rescued by the γδ T cell receptor (TCR) in the absence of TCR β chainLivák F, Wilson A, MacDonald H, Schatz D. αβ Lineage‐committed thymocytes can be rescued by the γδ T cell receptor (TCR) in the absence of TCR β chain European Journal Of Immunology 1997, 27: 2948-2958. PMID: 9394823, DOI: 10.1002/eji.1830271130.
- Coding Joint Formation in a Cell-Free V(D)J Recombination SystemLeu T, Eastman Q, Schatz D. Coding Joint Formation in a Cell-Free V(D)J Recombination System Immunity 1997, 7: 303-314. PMID: 9285414, DOI: 10.1016/s1074-7613(00)80532-4.
- Crystal structure of the RAG1 dimerization domain reveals multiple zinc-binding motifs including a novel zinc binuclear clusterBellon S, Rodgers K, Schatz D, Coleman J, Steitz T. Crystal structure of the RAG1 dimerization domain reveals multiple zinc-binding motifs including a novel zinc binuclear cluster Nature Structural & Molecular Biology 1997, 4: 586-591. PMID: 9228952, DOI: 10.1038/nsb0797-586.
- V(D)J recombination movesin vitroSchatz D. V(D)J recombination movesin vitro Seminars In Immunology 1997, 9: 149-159. PMID: 9200326, DOI: 10.1006/smim.1997.0068.
- RAG1 and RAG2 Form a Stable Postcleavage Synaptic Complex with DNA Containing Signal Ends in V(D)J RecombinationAgrawal A, Schatz D. RAG1 and RAG2 Form a Stable Postcleavage Synaptic Complex with DNA Containing Signal Ends in V(D)J Recombination Cell 1997, 89: 43-53. PMID: 9094713, DOI: 10.1016/s0092-8674(00)80181-6.
- Switching on gene expressionShockett P, Schatz D. Switching on gene expression Nature Biotechnology 1997, 15: 219-221. PMID: 9062915, DOI: 10.1038/nbt0397-219.
- Identification of V(D)J recombination coding end intermediates in normal thymocytes 11Edited by K. YamamotoLivák F, Schatz D. Identification of V(D)J recombination coding end intermediates in normal thymocytes 11Edited by K. Yamamoto Journal Of Molecular Biology 1997, 267: 1-9. PMID: 9096202, DOI: 10.1006/jmbi.1996.0834.
- Neoteny in Lymphocytes: Rag1 and Rag2 Expression in Germinal Center B CellsHan S, Zheng B, Schatz D, Spanopoulou E, Kelsoe G. Neoteny in Lymphocytes: Rag1 and Rag2 Expression in Germinal Center B Cells Science 1996, 274: 2094-2097. PMID: 8953043, DOI: 10.1126/science.274.5295.2094.
- RAG1 Mediates Signal Sequence Recognition and Recruitment of RAG2 in V(D)J RecombinationDifilippantonio M, McMahan C, Eastman Q, Spanopoulou E, Schatz D. RAG1 Mediates Signal Sequence Recognition and Recruitment of RAG2 in V(D)J Recombination Cell 1996, 87: 253-262. PMID: 8861909, DOI: 10.1016/s0092-8674(00)81343-4.
- A Zinc-binding Domain Involved in the Dimerization of RAG1Rodgers K, Bu Z, Fleming K, Schatz D, Engelman D, Coleman J. A Zinc-binding Domain Involved in the Dimerization of RAG1 Journal Of Molecular Biology 1996, 260: 70-84. PMID: 8676393, DOI: 10.1006/jmbi.1996.0382.
- Initiation of V(D)J recombination in vitro obeying the 12/23 ruleEastman Q, Leu T, Schatz D. Initiation of V(D)J recombination in vitro obeying the 12/23 rule Nature 1996, 380: 85-88. PMID: 8598914, DOI: 10.1038/380085a0.
- rag-1 and rag-2: Biochemistry and Protein InteractionsSchatz D, Leu T. rag-1 and rag-2: Biochemistry and Protein Interactions 1996, 217: 11-29. PMID: 8787615, DOI: 10.1007/978-3-642-50140-1_2.
- Down-regulation of RAG1 and RAG2 gene expression in PreB cells after functional immunoglobulin heavy chain rearrangementGrawunder U, Leu T, Schatz D, Werner A, Rolink A, Melchers F, Winkler T. Down-regulation of RAG1 and RAG2 gene expression in PreB cells after functional immunoglobulin heavy chain rearrangement Immunity 1995, 3: 601-608. PMID: 7584150, DOI: 10.1016/1074-7613(95)90131-0.
- In-frame TCR δ gene rearrangements play a critical role in the αβ/γδ T cell lineage decisionLivak F, Petrie H, Crisps I, Schatz D. In-frame TCR δ gene rearrangements play a critical role in the αβ/γδ T cell lineage decision Immunity 1995, 2: 617-627. PMID: 7796295, DOI: 10.1016/1074-7613(95)90006-3.
- CHAPTER 22 Recombination activating gene-1 (RAG-1) transcription in the mammalian CNSChun J, Schatz D. CHAPTER 22 Recombination activating gene-1 (RAG-1) transcription in the mammalian CNS 1993, 283-295. DOI: 10.1016/b978-0-444-81470-8.50027-2.
- V(D)J Recombination: Molecular Biology and RegulationSchatz D, Oettinger M, Schlissel M. V(D)J Recombination: Molecular Biology and Regulation Annual Review Of Immunology 1992, 10: 359-383. PMID: 1590991, DOI: 10.1146/annurev.iy.10.040192.002043.
- The recombination activating genes, RAG 1 and RAG 2, are on chromosome 11p in humans and chromosome 2p in miceOettinger M, Stanger B, Schatz D, Glaser T, Call K, Housman D, Baltimore D. The recombination activating genes, RAG 1 and RAG 2, are on chromosome 11p in humans and chromosome 2p in mice Immunogenetics 1992, 35: 97-101. PMID: 1735560, DOI: 10.1007/bf00189518.
- Thymocyte Expression of RAG-1 and RAG-2: Termination by T Cell Receptor Cross-LinkingTurka L, Schatz D, Oettinger M, Chun J, Gorka C, Lee K, McCormack W, Thompson C. Thymocyte Expression of RAG-1 and RAG-2: Termination by T Cell Receptor Cross-Linking Science 1991, 253: 778-781. PMID: 1831564, DOI: 10.1126/science.1831564.
- The recombination activating gene-1 (RAG-1) transcript is present in the murine central nervous systemChun J, Schatz D, Oettinger M, Jaenisch R, Baltimore D. The recombination activating gene-1 (RAG-1) transcript is present in the murine central nervous system Cell 1991, 64: 189-200. PMID: 1986864, DOI: 10.1016/0092-8674(91)90220-s.
- Selective expression of RAG-2 in chicken B cells undergoing immunoglobulin gene conversionCarlson L, Oettinger M, Schatz D, Masteller E, Hurley E, McCormack W, Baltimore D, Thompson C. Selective expression of RAG-2 in chicken B cells undergoing immunoglobulin gene conversion Cell 1991, 64: 201-208. PMID: 1986866, DOI: 10.1016/0092-8674(91)90221-j.
- RAG-1 and RAG-2, Adjacent Genes That Synergistically Activate V(D)J RecombinationOettinger M, Schatz D, Gorka C, Baltimore D. RAG-1 and RAG-2, Adjacent Genes That Synergistically Activate V(D)J Recombination Science 1990, 248: 1517-1523. PMID: 2360047, DOI: 10.1126/science.2360047.
- The V(D)J recombination activating gene, RAG-1Schatz D, Oettinger M, Baltimore D. The V(D)J recombination activating gene, RAG-1 Cell 1989, 59: 1035-1048. PMID: 2598259, DOI: 10.1016/0092-8674(89)90760-5.
- The Recombination Activating Gene and Lymphoid DifferentiationBaltimore D, Oettinger M, Schatz D. The Recombination Activating Gene and Lymphoid Differentiation 1989, 385-388. DOI: 10.1007/978-3-642-83755-5_50.
- Stable expression of immunoglobulin gene V(D)J recombinase activity by gene transfer into 3T3 fibroblastsSchatz D, Baltimore D. Stable expression of immunoglobulin gene V(D)J recombinase activity by gene transfer into 3T3 fibroblasts Cell 1988, 53: 107-115. PMID: 3349523, DOI: 10.1016/0092-8674(88)90492-8.
- Increased frequency of N-region insertion in a murine pre-B-cell line infected with a terminal deoxynucleotidyl transferase retroviral expression vectorLandau N, Schatz D, Rosa M, Baltimore D. Increased frequency of N-region insertion in a murine pre-B-cell line infected with a terminal deoxynucleotidyl transferase retroviral expression vector Molecular And Cellular Biology 1987, 7: 3237-3243. DOI: 10.1128/mcb.7.9.3237-3243.1987.