Katarina Ochodnicka

2 Role of RAG1 and RAG2 in B-cell development | 31 ensuring active is in an extended state and promotes Ig locus contraction124. CCCTC-binding factor (CTCF) is a zinc-finger protein with various functions in transcriptional regulation, was also shown to influence chromosomal contacts genome-wide and on the Ig locus through CTCF-binding elements (CBEs), a 14bp conserved regions within the Ig loci. Deletion of CTCF hampers the B-cell maturation and arrests the cell at pre-B cell stage125,126. Protein aggregation Protein aggregation and condensation were proposed to be an additional layer of regulation of RAG expression and activity. In the absence of RAG2, the human RAG1 has been shown to form aggregates scattered throughout the nucleus. RAG2 by itself does not aggregate but interacts with RAG1 aggregates. The disruption of the RAG1 oligomers leads to initiation of V(D)J recombination, as only the dimeric RAG1 form has the ability to interact with RAG2 and RSS and thus exhibits the catalytic activity127. In addition, temperature plays also a role in the self-association properties of RAG1128. Transcriptional regulation Multiple cis-regulatory elements have been identified in the RAG locus, which restrict the Rag expression during the development of B and T cells. Interestingly, these regulatory elements differ in B and the T cells. While the murine and human Rag1 promoters were found to be active in lymphoid and non-lymphoid cell lines,129 the Alt group showed that the 2-kb and 2-7kb 5’ regions upstream of the Rag2 promoter can independently drive the development of murine B cells but not T cells.130. Multiple transcription factors binding both promoters were identified, including PAX5, specificity protein1 (SP1), lymphoid enhancer-binding factor-1 (LEF1), myoblastosis viral oncogene homolog (c-MYB), nuclear transcription factor Y (NF-Y), the longest isoform of B-cell lymphoma/leukemia 11A (BCL11A-XL) and Myc-associated zinc finger protein (MAZ)131–135. Similar to the previous finding, the Muraguchi group identified, using a gene reporter assay, two enhancer elements in the 5’-upstream region of Rag2, one of which (D3) was not active in CD4+CD8+ or CD4+CD8− thymocytes, but only in CD4−CD8− lymphocytes, specifically in B220+IgM−, but not in B220+IgM+, cells in the bone marrow. This suggests a strict lineage and developmental stage-specific regulation of Rag2 by the cis-regulatory enhancer elements136. Erag was discovered to be a bona fide B cell-specific Rag enhancer, identified ~22kb upstream from the Rag2 promoter. Deletion of Erag results in a dramatic decrease of Rag expression and a partial block in the development of B cells, but not T cells137. Multiple transcription factors were shown to bind the Erag enhancer and positively regulate its activity such as forkhead box O1 (FOXO1), forkhead box P1 (FOXP1), and E2A138. Loss of FOXP1 transcription resulted in severe impairment of B-cell development and function139. Decreased FOXO1 protein levels diminished the transcription of the Rag locus, impaired development and receptor editing of primary bone-marrow B-cells140. The Erag is nega-

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