Stage-specific binding profiles of cohesin in resting and activated B lymphocytes suggest a role for cohesin in immunoglobulin class switching and maturation

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Günal Sadik, Gamze ^a   Paszkowski Rogacz, Maciej ^a   Singaravelu, Kalaimathy ^b   Beyer, Andreas ^b,c   Buchholz, Frank ^a   Jessberger, Rolf ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COHESIN; IMMUNOGLOBULIN CLASS; INTERLEUKIN 4; CELL CYCLE PROTEIN; CHROMATIN; IMMUNOGLOBULIN HEAVY CHAIN; LIPOPOLYSACCHARIDE; NONHISTONE PROTEIN;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE ACTIVATION; BINDING SITE; BLIMP 1 GENE; CELL MATURATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; GENE; GENE LOCUS; GENE SEQUENCE; GENE SWITCHING; GENETIC ANALYSIS; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PAX5 GENE; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROCESSING; REGULATORY MECHANISM; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; ANIMAL; B LYMPHOCYTE; C57BL MOUSE; CELL CULTURE; CHROMATIN; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE REARRANGEMENT; GENETICS; LYMPHOCYTE ACTIVATION; METABOLISM; REGULATORY SEQUENCE; SPLEEN;

ANIMALS; B-LYMPHOCYTES; BINDING SITES; CELL CYCLE PROTEINS; CELLS, CULTURED; CHROMATIN; CHROMOSOMAL PROTEINS, NON-HISTONE; GENE EXPRESSION REGULATION; IMMUNOGLOBULIN CLASS SWITCHING; IMMUNOGLOBULIN HEAVY CHAINS; INTERLEUKIN-4; LIPOPOLYSACCHARIDES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; REGULATORY SEQUENCES, NUCLEIC ACID; SPLEEN;

EID: 84910624115     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0111748     Document Type: Article

References (42)

1. Peters JM, Tedeschi A, Schmitz J (2008) The cohesin complex and its roles in chromosome biology. Genes Dev 22: 3089-3114.
2. Jessberger R (2009) Cohesin's dual role in the DNA damage response: repair and checkpoint activation. EMBO J 28: 2491-2493.
3. Nasmyth K (2011) Cohesin: a catenase with separate entry and exit gates? Nat Cell Biol 13: 1170-1177.
4. Nasmyth K, Haering CH (2009) Cohesin: its roles and mechanisms. Annu Rev Genet 43: 525-558.
5. Haering CH, Jessberger R (2012) Cohesin in determining chromosome architecture. Exp Cell Res 318: 1386-1393.
6. Shintomi K, Hirano T (2010) Sister chromatid resolution: a cohesin releasing network and beyond. Chromosoma 119: 459-467.
7. Peric-Hupkes D, van Steensel B (2008) Linking cohesin to gene regulation. Cell 132: 925-928.
8. Feeney KM, Wasson CW, Parish JL (2010) Cohesin: a regulator of genome integrity and gene expression. Biochem J 428: 147-161.
9. Degner SC, Wong TP, Jankevicius G, Feeney AJ (2009) Cutting edge: Developmental stage-specific recruitment of cohesin to CTCF sites throughout immunoglobulin loci during B lymphocyte development. J Immunol 182: 44-48.
10. Schmidt D, Schwalie PC, Ross-Innes CS, Hurtado A., Brown GD, et al. (2010) A CTCF-independent role for cohesin in tissue-specific transcription. Genome Res 20: 578-588.
11. Hou C, Dale R, Dean A (2010) Cell type specificity of chromatin organization mediated by CTCF and cohesin. Proc Natl Acad Sci U S A 107: 3651-3656.
12. Parelho V, Hadjur S, Spivakov M., Leleu M, Sauer S, et al. (2008) Cohesins functionally associate with CTCF on mammalian chromosome arms. Cell 132: 422-433.
13. Wendt KS, Yoshida K, Itoh T., Bando M, Koch B, et al. (2008) Cohesin mediates transcriptional insulation by CCCTC-binding factor. Nature 451: 796-801.
14. Kagey MH, Newman JJ, Bilodeau S, Zhan Y., Orlando DA, et al. (2010) Mediator and cohesin connect gene expression and chromatin architecture. Nature 467: 430-435.
15. Nitzsche A, Paszkowski-Rogacz M, Matarese F., Janssen-Megens EM, Hubner NC, et al. (2011) RAD21 cooperates with pluripotency transcription factors in the maintenance of embryonic stem cell identity. PLoS One 6: e19470.
16. Seitan VC, Hao B, Tachibana-Konwalski K, Lavagnolli T., Mira-Bontenbal H, et al. (2011) A role for cohesin in T-cell-receptor rearrangement and thymocyte differentiation. Nature 476: 467-471.
17. Guo C, Gerasimova T, Hao H., Ivanova I, Chakraborty T, et al. (2011) Two forms of loops generate the chromatin conformation of the immunoglobulin heavy-chain gene locus. Cell 147: 332-343.
18. Meffre E, Casellas R, Nussenzweig MC (2000) Antibody regulation of B cell development. Nat Immunol 1: 379-385.
19. Guo C, Yoon HS, Franklin A, Jain S., Ebert A, et al. (2011) CTCF-binding elements mediate control of V(D)J recombination. Nature 477: 424-430.
20. Yamane A, Resch W, Kuo N., Kuchen S, Li Z, et al. (2011) Deep-sequencing identification of the genomic targets of the cytidine deaminase AID and its cofactor RPA in B lymphocytes. Nat Immunol 12: 62-69.
21. Jhunjhunwala S, van Zelm MC, Peak MM, Cutchin S, Riblet R, et al. (2008) The 3D structure of the immunoglobulin heavy-chain locus: implications for long-range genomic interactions. Cell 133: 265-279.
22. Chaumeil J, Skok JA (2012) The role of CTCF in regulating V(D)J recombination. Curr Opin Immunol 24: 153-159.
23. Stavnezer J, Guikema JE, Schrader CE (2008) Mechanism and regulation of class switch recombination. Annu Rev Immunol 26: 261-292.
24. Wuerffel R, Wang L, Grigera F., Manis J, Selsing E, et al. (2007) S-S synapsis during class switch recombination is promoted by distantly located transcriptional elements and activation-induced deaminase. Immunity 27: 711-722.
25. Thomas-Claudepierre AS, Schiavo E, Heyer V., Fournier M, Page A, et al. (2013) The cohesin complex regulates immunoglobulin class switch recombination. J Exp Med 210: 2495-2502.
26. Shin H, Liu T, Manrai A.K., Liu XS (2009) CEAS: cis-regulatory element annotation system. Bioinformatics 25: 2605-2606.
27. Gyory I, Boller S, Nechanitzky R., Mandel E, Pott S, et al. (2012) Transcription factor Ebf1 regulates differentiation stage-specific signaling, proliferation, and survival of B cells. Genes Dev 26: 668-682.
28. Degner SC, Verma-Gaur J, Wong T.P., Bossen C., Iverson GM, et al. (2011) CCCTC-binding factor (CTCF) and cohesin influence the genomic architecture of the Igh locus and antisense transcription in pro-B cells. Proc Natl Acad Sci U S A 108: 9566-9571.
29. Rouaud P, Vincent-Fabert C, Fiancette R., Cogne M, Pinaud E, et al. (2012) Enhancers located in heavy chain regulatory region (hs3a, hs1,2, hs3b, and hs4) are dispensable for diversity of VDJ recombination. J Biol Chem 287: 8356-8360.
30. Chatterjee S, Ju Z, Hassan R., Volpi SA, Emelyanov AV, et al. (2011) Dynamic changes in binding of immunoglobulin heavy chain 3' regulatory region to protein factors during class switching. J Biol Chem 286: 29303-29312.
31. Volpi SA, Verma-Gaur J, Hassan R., Ju Z, Roa S, et al. (2012) Germline deletion of Igh 3' regulatory region elements hs 5, 6, 7 (hs5-7) affects B cell-specific regulation, rearrangement, and insulation of the Igh locus. J Immunol 188: 2556-2566.
32. Pawlitzky I, Angeles CV, Siegel A.M., Stanton ML, Riblet R, et al. (2006) Identification of a candidate regulatory element within the 5' flanking region of the mouse Igh locus defined by pro-B cell-specific hypersensitivity associated with binding of PU.1, Pax5, and E2A. J Immunol 176: 6839-6851.
33. Perlot T, Pawlitzky I, Manis J.P., Zarrin AA, Brodeur PH, et al. (2010) Analysis of mice lacking DNaseI hypersensitive sites at the 5' end of the IgH locus. PLoS One 5: e13992.
34. Nera KP, Kohonen P, Narvi E., Peippo A, Mustonen L, et al. (2006) Loss of Pax5 promotes plasma cell differentiation. Immunity 24: 283-293.
35. Decker T, Pasca di Magliano M, McManus S, Sun Q, Bonifer C, et al. (2009) Stepwise activation of enhancer and promoter regions of the B cell commitment gene Pax5 in early lymphopoiesis. Immunity 30: 508-520.
36. Shaffer AL, Lin KI, Kuo T.C., Yu X., Hurt EM, et al. (2002) Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17: 51-62.
37. Schliephake DE, Schimpl A (1996) Blimp-1 overcomes the block in IgM secretion in lipopolysaccharide/anti-mu F(ab')2-co-stimulated B lymphocytes. Eur J Immunol 26: 268-271.
38. Ramiro AR, Jankovic M, Callen E., Difilippantonio S, Chen HT, et al. (2006) Role of genomic instability and p53 in AID-induced c-myc-Igh translocations. Nature 440: 105-109.
39. Donze D, Adams CR, Rine J, Kamakaka RT (1999) The boundaries of the silenced HMR domain in Saccharomyces cerevisiae. Genes Dev 13: 698-708.
40. Enervald E, Du L, Visnes T., Bjorkman A, Lindgren E, et al. (2013) A regulatory role for the cohesin loader NIPBL in nonhomologous end joining during immunoglobulin class switch recombination. J Exp Med 210: 2503-2513.
41. Vincent-Fabert C, Fiancette R, Pinaud E., Truffinet V, Cogne N, et al. (2010) Genomic deletion of the whole IgH 3' regulatory region (hs3a, hs1,2, hs3b, and hs4) dramatically affects class switch recombination and Ig secretion to all isotypes. Blood 116: 1895-1898.
42. Jyonouchi S, Orange J, Sullivan K.E., Krantz I., Deardorff M (2013) Immunologic features of cornelia de lange syndrome. Pediatrics 132: e484-489.