Chromatin Architecture near a Potential 3′ End of the Igh Locus Involves Modular Regulation of Histone Modifications during B-Cell Development and In Vivo Occupancy at CTCF Sites

REFERENCES

• Alt, F., N. Rosenberg, S. Lewis, E. Thomas, and D. Baltimore. 1981. Organization and reorganization of immunoglobulin genes in A-MuLV-transformed cells: rearrangement of heavy but not light chain genes. Cell 27:381–390.
   PubMed Web of Science ®Google Scholar
• Barlev, N. A., A. V. Emelyanov, P. Castagnino, P. Zegerman, A. J. Bannister, M. A. Sepulveda, F. Robert, L. Tora, T. Kouzarides, B. K. Birshtein, and S. L. Berger. 2003. A novel human Ada2 homologue functions with Gcn5 or Brg1 to coactivate transcription. Mol. Cell. Biol. 23:6944–6957.
   PubMedGoogle Scholar
• Bell, A. C., A. G. West, and G. Felsenfeld. 1999. The protein CTCF is required for the enhancer blocking activity of vertebrate insulators. Cell 98:387–396.
   PubMed Web of Science ®Google Scholar
• Bradney, C., M. Hjelmeland, Y. Komatsu, M. Yoshida, T. P. Yao, and Y. Zhuang. 2003. Regulation of E2A activities by histone acetyltransferases in B lymphocyte development. J. Biol. Chem. 278:2370–2376.
   PubMedGoogle Scholar
• Bulger, M., D. Schubeler, M. A. Bender, J. Hamilton, C. M. Farrell, R. C. Hardison, and M. Groudine. 2003. A complex chromatin landscape revealed by patterns of nuclease sensitivity and histone modification within the mouse β-globin locus. Mol. Cell. Biol. 23:5234–5244.
   PubMedGoogle Scholar
• Calvo, C.-F., S. L. Giannini, N. Martinez, and B. K. Birshtein. 1991. DNA sequences 3′ of the IgH chain cluster rearrange in mouse B cell lines. J. Immunol. 146:1353–1360.
   PubMedGoogle Scholar
• Chauveau, C., and M. Cogne. 1996. Palindromic structure of the IgH 3′ locus control region. Nat. Genet. 14:15–16.
   PubMedGoogle Scholar
• Chauveau, C., E. A. Jansson, S. Muller, M. Cogne, and S. Pettersson. 1999. Cutting edge: Ig heavy chain 3′ HS1-4 directs correct spatial position-independent expression of a linked transgene to B lineage cells. J. Immunol. 163:4637–4641.
   PubMedGoogle Scholar
• Chen, C., and B. K. Birshtein. 1997. Virtually identical enhancers containing a segment of homology to murine 3′IgH-E(hs1,2) lie downstream of human Ig C alpha 1 and C alpha 2 genes. J. Immunol. 159:1310–1318.
   PubMedGoogle Scholar
• Chowdhury, D., and R. Sen. 2001. Stepwise activation of the immunoglobulin mu heavy chain gene locus. EMBO J. 20:6394–6403.
   PubMed Web of Science ®Google Scholar
• Chowdhury, D., and R. Sen. 2003. Transient IL-7/IL-7R signaling provides a mechanism for feedback inhibition of immunoglobulin heavy chain gene rearrangements. Immunity 18:229–241.
   PubMed Web of Science ®Google Scholar
• Cogne, M., R. Lansford, A. Bottaro, J. Zhang, J. Gorman, F. Young, H. L. Cheng, and F. W. Alt. 1994. A class switch control region at the 3′ end of the immunoglobulin heavy chain locus. Cell 77:737–747.
   PubMedGoogle Scholar
• de Laat, W., and F. Grosveld. 2003. Spatial organization of gene expression: the active chromatin hub. Chromosome Res. 11:447–459.
   PubMedGoogle Scholar
• Felsenfeld, G., and M. Groudine. 2003. Controlling the double helix. Nature 421:448–453.
   PubMed Web of Science ®Google Scholar
• Fernandez, L. A., M. Winkler, and R. Grosschedl. 2001. Matrix attachment region-dependent function of the immunoglobulin μ enhancer involves histone acetylation at a distance without changes in enhancer occupancy. Mol. Cell. Biol. 21:196–208.
   PubMed Web of Science ®Google Scholar
• Filippova, G. N., S. Fagerlie, E. M. Klenova, C. Myers, Y. Dehner, G. Goodwin, P. E. Neiman, S. J. Collins, and V. V. Lobanenkov. 1996. An exceptionally conserved transcriptional repressor, CTCF, employs different combinations of zinc fingers to bind diverged promoter sequences of avian and mammalian c-myc oncogenes. Mol. Cell. Biol. 16:2802–2813.
   PubMed Web of Science ®Google Scholar
• Filippova, G. N., C. F. Qi, J. E. Ulmer, J. M. Moore, M. D. Ward, Y. J. Hu, D. I. Loukinov, E. M. Pugacheva, E. M. Klenova, P. E. Grundy, A. P. Feinberg, A. M. Cleton-Jansen, E. W. Moerland, C. J. Cornelisse, H. Suzuki, A. Komiya, A. Lindblom, F. Dorion-Bonnet, P. E. Neiman, H. C. Morse III, S. J. Collins, and V. V. Lobanenkov. 2002. Tumor-associated zinc finger mutations in the CTCF transcription factor selectively alter its DNA-binding specificity. Cancer Res. 62:48–52.
   PubMed Web of Science ®Google Scholar
• Forsberg, E. C., K. M. Downs, H. M. Christensen, H. Im, P. A. Nuzzi, and E. H. Bresnick. 2000. Developmentally dynamic histone acetylation pattern of a tissue-specific chromatin domain. Proc. Natl. Acad. Sci. USA 97:14494–14499.
   PubMedGoogle Scholar
• Giannini, S. L., M. Singh, C.-F. Calvo, G. Ding, and B. K. Birshtein. 1993. DNA regions flanking the mouse Ig 3′α enhancer are differentially methylated and DNAse I hypersensitive during B cell differentiation. J. Immunol. 150:1772–1780.
   PubMedGoogle Scholar
• Gombert, W. M., S. D. Farris, E. D. Rubio, K. M. Morey-Rosler, W. H. Schubach, and A. Krumm. 2003. The c-myc insulator element and matrix attachment regions define the c-myc chromosomal domain. Mol. Cell. Biol. 23:9338–9348.
   PubMedGoogle Scholar
• Gordon, S. J., S. Saleque, and B. K. Birshtein. 2003. Yin Yang 1 is a lipopolysaccharide-inducible activator of the murine 3′ Igh enhancer, hs3. J. Immunol. 170:5549–5557.
   PubMed Web of Science ®Google Scholar
• Greenbaum, S., and Y. Zhuang. 2002. Identification of E2A target genes in B lymphocyte development by using a gene tagging-based chromatin immunoprecipitation system. Proc. Natl. Acad. Sci. USA 99:15030–15035.
   PubMedGoogle Scholar
• Gregor, P. D., and S. L. Morrison. 1986. Myeloma mutant with a novel 3′ flanking region: loss of normal sequence and insertion of repetitive elements leads to decreased transcription but normal processing of the alpha heavy-chain gene products. Mol. Cell. Biol. 6:1903–1916.
   PubMedGoogle Scholar
• Hark, A. T., C. J. Schoenherr, D. J. Katz, R. S. Ingram, J. M. Levorse, and S. M. Tilghman. 2000. CTCF mediates methylation-sensitive enhancer-blocking activity at the H19/Igf2 locus. Nature 405:486–489.
   PubMed Web of Science ®Google Scholar
• Hebbes, T. R., A. L. Clayton, A. W. Thorne, and C. Crane-Robinson. 1994. Core histone hyperacetylation co-maps with generalized DNase I sensitivity in the chicken beta-globin chromosomal domain. EMBO J. 13:1823–1830.
   PubMed Web of Science ®Google Scholar
• Hesslein, D. G., D. L. Pflugh, D. Chowdhury, A. L. Bothwell, R. Sen, and D. G. Schatz. 2003. Pax5 is required for recombination of transcribed, acetylated, 5′ IgH V gene segments. Genes Dev. 17:37–42.
   PubMedGoogle Scholar
• Jenuwein, T., and C. D. Allis. 2001. Translating the histone code. Science 293:1074–1080.
   PubMed Web of Science ®Google Scholar
• Johnson, K., C. Angelin-Duclos, S. Park, and K. L. Calame. 2003. Changes in histone acetylation are associated with differences in accessibility of VH gene segments to V-DJ recombination during B-cell ontogeny and development. Mol. Cell. Biol. 23:2438–2450.
   PubMedGoogle Scholar
• Johnson, K., D. L. Pflugh, D. Yu, D. G. Hesslein, K. I. Lin, A. L. Bothwell, A. Thomas-Tikhonenko, D. G. Schatz, and K. Calame. 2004. B cell-specific loss of histone 3 lysine 9 methylation in the V(H) locus depends on Pax5. Nat. Immunol. 5:853–861.
   PubMedGoogle Scholar
• Kanda, K., H. M. Hu, L. Zhang, J. Grandchamps, and L. M. Boxer. 2000. NF-kappa B activity is required for the deregulation of c-myc expression by the immunoglobulin heavy chain enhancer. J. Biol. Chem. 275:32338–32346.
   PubMed Web of Science ®Google Scholar
• Kanduri, C., V. Pant, D. Loukinov, E. Pugacheva, C. F. Qi, A. Wolffe, R. Ohlsson, and V. V. Lobanenkov. 2000. Functional association of CTCF with the insulator upstream of the H19 gene is parent of origin-specific and methylation-sensitive. Curr. Biol. 10:853–856.
   PubMed Web of Science ®Google Scholar
• Kanduri, M., C. Kanduri, P. Mariano, A. A. Vostrov, W. Quitschke, V. Lobanenkov, and R. Ohlsson. 2002. Multiple nucleosome positioning sites regulate the CTCF-mediated insulator function of the H19 imprinting control region. Mol. Cell. Biol. 22:3339–3344.
   PubMedGoogle Scholar
• Khamlichi, A. A., E. Pinaud, C. Decourt, C. Chauveau, and M. Cogne. 2000. The 3′ IgH regulatory region: a complex structure in search of a function. Adv. Immunol. 75:317–345.
   PubMed Web of Science ®Google Scholar
• Kim, K. J., C. Kanellopoulos-Langevin, R. M. Merwin, D. H. Sachs, and R. Asofsky. 1979. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J. Immunol. 122:549–554.
   PubMed Web of Science ®Google Scholar
• Klenova, E. M., H. C. Morse III, R. Ohlsson, and V. V. Lobanenkov. 2002. The novel BORIS + CTCF gene family is uniquely involved in the epigenetics of normal biology and cancer. Semin. Cancer Biol. 12:399–414.
   PubMedGoogle Scholar
• Kuehl, W. M., and P. L. Bergsagel. 2002. Multiple myeloma: evolving genetic events and host interactions. Nat. Rev. Cancer 2:175–187.
   PubMed Web of Science ®Google Scholar
• Kuo, M. H., and C. D. Allis. 1999. In vivo cross-linking and immunoprecipitation for studying dynamic protein:DNA associations in a chromatin environment. Methods 19:425–433.
   PubMed Web of Science ®Google Scholar
• Lee, S. C., A. Bottaro, and R. A. Insel. 2003. Activation of terminal B cell differentiation by inhibition of histone deacetylation. Mol. Immunol. 39:923–932.
   PubMed Web of Science ®Google Scholar
• Li, Z., Z. Luo, and M. D. Scharff. 2004. Differential regulation of histone acetylation and generation of mutations in switch regions is associated with Ig class switching. Proc. Natl. Acad. Sci. USA 101:15428–15433.
   PubMedGoogle Scholar
• Lieberson, R., J. Ong, X. Shi, and L. A. Eckhardt. 1995. Immunoglobulin gene transcription ceases upon deletion of a distant enhancer. EMBO J. 14:6229–6238.
   PubMed Web of Science ®Google Scholar
• Litt, M. D., M. Simpson, M. Gaszner, C. D. Allis, and G. Felsenfeld. 2001. Correlation between histone lysine methylation and developmental changes at the chicken beta-globin locus. Science 293:2453–2455.
   PubMedGoogle Scholar
• Litt, M. D., M. Simpson, F. Recillas-Targa, M. N. Prioleau, and G. Felsenfeld. 2001. Transitions in histone acetylation reveal boundaries of three separately regulated neighboring loci. EMBO J. 20:2224–2235.
   PubMedGoogle Scholar
• Madisen, L., and M. Groudine. 1994. Identification of a locus control region in the immunoglobulin heavy-chain locus that deregulates c-myc expression in plasmacytoma and Burkitt's lymphoma cells. Genes Dev. 8:2212–2226.
   PubMed Web of Science ®Google Scholar
• Maes, J., L. P. O'Neill, P. Cavelier, B. M. Turner, F. Rougeon, and M. Goodhardt. 2001. Chromatin remodeling at the Ig loci prior to V(D)J recombination. J. Immunol. 167:866–874.
   PubMedGoogle Scholar
• Manis, J. P., J. S. Michaelson, B. K. Birshtein, and F. W. Alt. 2003. Elucidation of a downstream boundary of the 3′ IgH regulatory region. Mol. Immunol. 39:753–760.
   PubMedGoogle Scholar
• Manis, J. P., N. van der Stoep, M. Tian, R. Ferrini, L. Davidson, A. Bottaro, and F. W. Alt. 1998. Class switching in B cells lacking 3′ immunoglobulin heavy chain enhancers. J. Exp. Med. 188:1421–1431.
   PubMedGoogle Scholar
• Max, E. E. 2003. Immunoglobulins: molecular genetics, p. 107–158. In W. E. Paul (ed.), Fundamental immunology, 5th ed. Lippincott Williams & Wilkins, Philadelphia, Pa.
   Google Scholar
• Michaelson, J. S., S. L. Giannini, and B. K. Birshtein. 1995. Identification of 3′ alpha-hs4, a novel Ig heavy chain enhancer element regulated at multiple stages of B cell differentiation. Nucleic Acids Res. 23:975–981.
   PubMedGoogle Scholar
• Mills, F. C., N. Harindranath, M. Mitchell, and E. E. Max. 1997. Enhancer complexes located downstream of both human immunoglobulin Ca genes. J. Exp. Med. 186:845–858.
   PubMed Web of Science ®Google Scholar
• Mombaerts, P., J. Iacomini, R. S. Johnson, K. Herrup, S. Tonegawa, and V. E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869–877.
   PubMed Web of Science ®Google Scholar
• Morshead, K. B., D. N. Ciccone, S. D. Taverna, C. D. Allis, and M. A. Oettinger. 2003. Antigen receptor loci poised for V(D)J rearrangement are broadly associated with BRG1 and flanked by peaks of histone H3 dimethylated at lysine 4. Proc. Natl. Acad. Sci. USA 100:11577–11582.
   PubMed Web of Science ®Google Scholar
• Mukhopadhyay, R., W.-Q. Yu, J. Whitehead, J.-W. Xu, M. Lezcano, S. D. Pack, C. Kanduri, M. Kanduri, V. Ginjala, A. A. Vostrov, W. Quitschke, I. Chernukhin, E. Klenova, V. Lobanenkov, and R. Ohlsson. 2004. The binding sites for the chromatin insulator protein CTCF map to DNA methylation-free domains genomewide. Genome Res. 14:1594–1602.
   PubMed Web of Science ®Google Scholar
• Muramatsu, M., K. Kinoshita, S. Fagarasan, S. Yamada, Y. Shinkai, and T. Honjo. 2000. Class switch recombination and hypermutation require activation-induced cytidine deaminase (AID), a potential RNA editing enzyme. Cell 102:553–563.
   PubMed Web of Science ®Google Scholar
• Nambu, Y., M. Sugai, H. Gonda, C. G. Lee, T. Katakai, Y. Agata, Y. Yokota, and A. Shimizu. 2003. Transcription-coupled events associating with immunoglobulin switch region chromatin. Science 302:2137–2140.
   PubMed Web of Science ®Google Scholar
• Nesset, A. L., and D. M. Bader. 2002. Hole is a novel gene product expressed in the developing heart and brain. Mech. Dev. 117:347–350.
   PubMedGoogle Scholar
• Ng, H. H., D. N. Ciccone, K. B. Morshead, M. A. Oettinger, and K. Struhl. 2003. Lysine-79 of histone H3 is hypomethylated at silenced loci in yeast and mammalian cells: a potential mechanism for position-effect variegation. Proc. Natl. Acad. Sci. USA 100:1820–1825.
   PubMedGoogle Scholar
• Nossal, G. J. 2003. The double helix and immunology. Nature 421:440–444.
   PubMedGoogle Scholar
• Ohlsson, R., R. Renkawitz, and V. Lobanenkov. 2001. CTCF is a uniquely versatile transcription regulator linked to epigenetics and disease. Trends Genet. 17:520–527.
   PubMed Web of Science ®Google Scholar
• Ong, J., S. Stevens, R. G. Roeder, and L. A. Eckhardt. 1998. 3′ IgH enhancer elements shift synergistic interactions during B cell development. J. Immunol. 160:4896–4903.
   PubMed Web of Science ®Google Scholar
• Palstra, R. J., B. Tolhuis, E. Splinter, R. Nijmeijer, F. Grosveld, and W. de Laat. 2003. The beta-globin nuclear compartment in development and erythroid differentiation. Nat. Genet. 35:190–194.
   PubMed Web of Science ®Google Scholar
• Pant, V., S. Kurukuti, E. Pugacheva, S. Shamsuddin, P. Mariano, R. Renkawitz, E. Klenova, V. Lobanenkov, and R. Ohlsson. 2004. Mutation of a single CTCF target site within the H19 imprinting control region leads to loss of Igf2 imprinting and complex patterns of de novo methylation upon maternal inheritance. Mol. Cell. Biol. 24:3497–3504.
   PubMed Web of Science ®Google Scholar
• Pinaud, E., C. Aupetit, C. Chauveau, and M. Cogne. 1997. Identification of a homolog of the C alpha 3′/hs3 enhancer and of an allelic variant of the 3′IgH/hs1,2 enhancer downstream of the human immunoglobulin alpha 1 gene. Eur. J. Immunol. 27:2981–2985.
   PubMedGoogle Scholar
• Pinaud, E., A. A. Khamlichi, C. Le Morvan, M. Drouet, V. Nalesso, M. Le Bert, and M. Cogne. 2001. Localization of the 3′ IgH locus elements that effect long-distance regulation of class switch recombination. Immunity 15:187–199.
   PubMed Web of Science ®Google Scholar
• Potter, M. 1967. The plasma cell tumors and myeloma proteins of mice, vol. 2. Academic Press Inc., New York, N.Y.
   Google Scholar
• Reina-San-Martin, B., S. Difilippantonio, L. Hanitsch, R. F. Masilamani, A. Nussenzweig, and M. C. Nussenzweig. 2003. H2AX is required for recombination between immunoglobulin switch regions but not for intra-switch region recombination or somatic hypermutation. J. Exp. Med. 197:1767–1778.
   PubMed Web of Science ®Google Scholar
• Saleque, S., M. Singh, R. D. Little, S. L. Giannini, J. S. Michaelson, and B. K. Birshtein. 1997. Dyad symmetry within the mouse 3′ IgH regulatory region includes two virtually identical enhancers (C alpha3′E and hs3). J. Immunol. 158:4780–4787.
   PubMedGoogle Scholar
• Schubeler, D., C. Francastel, D. M. Cimbora, A. Reik, D. I. Martin, and M. Groudine. 2000. Nuclear localization and histone acetylation: a pathway for chromatin opening and transcriptional activation of the human beta-globin locus. Genes Dev. 14:940–950.
   PubMed Web of Science ®Google Scholar
• Sepulveda, M. A., A. V. Emelyanov, and B. K. Birshtein. 2004. NF-kappaB and Oct-2 synergize to activate the human 3′ Igh hs4 enhancer in B cells. J. Immunol. 172:1054–1064.
   PubMed Web of Science ®Google Scholar
• Sepulveda, M. A., F. E. Garrett, A. Price-Whelan, and B. K. Birshtein. 2005. Comparative analysis of human and mouse 3′ Igh regulatory regions identifies distinctive structural features. Mol. Immunol. 42:605–615.
   PubMedGoogle Scholar
• Shi, X., and L. A. Eckhardt. 2001. Deletional analyses reveal an essential role for the hs3b/hs4 IgH 3′ enhancer pair in an Ig-secreting but not an earlier-stage B cell line. Int. Immunol. 13:1003–1012.
   PubMedGoogle Scholar
• Shinkai, Y., G. Rathbun, K. P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, et al. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:855–867.
   PubMed Web of Science ®Google Scholar
• Siden, E. J., D. Baltimore, D. Clark, and N. E. Rosenberg. 1979. Immunoglobulin synthesis by lymphoid cells transformed in vitro by Abelson murine leukemia virus. Cell 16:389–396.
   PubMedGoogle Scholar
• Singh, M., and B. K. Birshtein. 1993. NF-HB (BSAP) is a repressor of the murine immunoglobulin heavy-chain 3′ α enhancer at early stages of B-cell differentiation. Mol. Cell. Biol. 13:3611–3622.
   PubMed Web of Science ®Google Scholar
• Southern, E. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:503–517.
   PubMed Web of Science ®Google Scholar
• Stavnezer, J. 2000. Molecular processes that regulate class switching. Curr. Top. Microbiol. Immunol. 245:127–168.
   PubMed Web of Science ®Google Scholar
• Strahl, B. D., and C. D. Allis. 2000. The language of covalent histone modifications. Nature 403:41–45.
   PubMed Web of Science ®Google Scholar
• Su, I. H., A. Basavaraj, A. N. Krutchinsky, O. Hobert, A. Ullrich, B. T. Chait, and A. Tarakhovsky. 2003. Ezh2 controls B cell development through histone H3 methylation and Igh rearrangement. Nat. Immunol. 4:124–131.
   PubMed Web of Science ®Google Scholar
• Takahashi, N., A. Roach, D. B. Teplow, S. B. Prusiner, and L. Hood. 1985. Cloning and characterization of the myelin basic protein gene from mouse: one gene can encode both 14 kd and 18.5 kd MBPs by alternate use of exons. Cell 42:139–148.
   PubMedGoogle Scholar
• Takahashi, Y., J. B. Rayman, and B. D. Dynlacht. 2000. Analysis of promoter binding by the E2F and pRB families in vivo: distinct E2F proteins mediate activation and repression. Genes Dev. 14:804–816.
   PubMed Web of Science ®Google Scholar
• Tanimoto, K., A. Sugiura, A. Omori, G. Felsenfeld, J. D. Engel, and A. Fukamizu. 2003. Human β-globin locus control region HS5 contains CTCF- and developmental stage-dependent enhancer-blocking activity in erythroid cells. Mol. Cell. Biol. 23:8946–8952.
   PubMedGoogle Scholar
• Vostrov, A. A., and W. W. Quitschke. 1997. The zinc finger protein CTCF binds to the APBbeta domain of the amyloid beta-protein precursor promoter. Evidence for a role in transcriptional activation. J. Biol. Chem. 272:33353–33359.
   PubMedGoogle Scholar
• West, A. G., M. Gaszner, and G. Felsenfeld. 2002. Insulators: many functions, many mechanisms. Genes Dev. 16:271–288.
   PubMed Web of Science ®Google Scholar
• Woo, C. J., A. Martin, and M. D. Scharff. 2003. Induction of somatic hypermutation is associated with modifications in immunoglobulin variable region chromatin. Immunity 19:479–489.
   PubMedGoogle Scholar
• Yamasaki, H., I. B. Weinstein, E. Fibach, R. A. Rifkind, and P. Marks. 1979. Tumor promoter-induced adhesion of the DS19 clone of murine erythroleukemia cells. Cancer Res. 39:1989–1994.
   PubMedGoogle Scholar
• Yang, Y., W. W. Quitschke, A. A. Vostrov, and G. J. Brewer. 1999. CTCF is essential for up-regulating expression from the amyloid precursor protein promoter during differentiation of primary hippocampal neurons. J. Neurochem. 73:2286–2298.
   PubMedGoogle Scholar
• Zhong, X. P., and M. S. Krangel. 1997. An enhancer-blocking element between alpha and delta gene segments within the human T cell receptor alpha/delta locus. Proc. Natl. Acad. Sci. USA 94:5219–5224.
   PubMed Web of Science ®Google Scholar
• Zhou, J., N. Ashouian, M. Delepine, F. Matsuda, C. Chevillard, R. Riblet, C. L. Schildkraut, and B. K. Birshtein. 2002. The origin of a developmentally regulated Igh replicon is located near the border of regulatory domains for Igh replication and expression. Proc. Natl. Acad. Sci. USA 99:13693–13698.
   PubMedGoogle Scholar