Pronounced cohabitation of active immunoglobulin genes from three different chromosomes in transcription factories during maximal antibody synthesis

Genes and Development

Volumn 28, Issue 11, 2014, Pages 1159-1164

  Park, Sung Kyun ^a   Xiang, Yougui ^a,b   Feng, Xin ^c   Garrard, William T ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b TIANJIN MEDICAL UNIVERSITY   (China)

^c BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Enhancers; Immunoglobulin genes; Long range interactions; Nuclear organization; RNA trafficking; Transcription factories

Indexed keywords

IMMUNOGLOBULIN G; POLYMER;

ANIMAL CELL; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE; CELL NUCLEUS; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME; COHABITATION; CYTOPLASM; GENE EXPRESSION; GENETIC TRANSCRIPTION; IMMUNOGLOBULIN GENE; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; THREE DIMENSIONAL IMAGING;

ENHANCERS; IMMUNOGLOBULIN GENES; LONG-RANGE INTERACTIONS; NUCLEAR ORGANIZATION; RNA TRAFFICKING; TRANSCRIPTION FACTORIES;

ALLELES; ANIMALS; ANTIBODY FORMATION; B-LYMPHOCYTES; CELL NUCLEUS; CHROMOSOMES; CYTOPLASM; GENE EXPRESSION REGULATION; GENES, IMMUNOGLOBULIN; IN SITU HYBRIDIZATION, FLUORESCENCE; MICE;

EID: 84901779165     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.237479.114     Document Type: Article

References (33)

1. Benson M.J., Aijo T, Chang X, Gagnon J, Pape UJ, Anantharaman V, Aravind L., Pursiheimo P, Oberdoerffer S, Liu XS, et al. 2012. Heterogenous nuclear ribonucleoprotein L-like (hnRNPLL) and elongation factor, RNA polymerase II, 2 (ELL2) are regulators of mRNA processing in plasma cells. Proc Natl Acad Sci 109: 16252-16257.
2. Blobel G. 1985. Gene gating: a hypothesis. Proc Natl Acad Sci 82: 8527-8529.
3. Blobel G. 2010. Three-dimensional organization of chromatids by nuclear envelope-associated structures. Cold Spring Harb Symp Quant Biol 75: 545-554
4. Bossen C., Mansson R, Murre C. 2012. Chromatin topology and the regulation of antigen receptor assembly. Annu Rev Immunol 30: 337-356.
5. Cisse I.I., Izeddin I, Causse SZ, Boudarene L, Senecal A, Muresan L, Dugast-Darzacq L, Hajj B, Dahan M, Darzacq X. 2013. Real-time dynamics of RNA polymerase II clustering in live human cells. Science 341: 664-667.
6. Cook PR. 1999. The organization of replication and transcription. Science 284: 1790-1795.
7. Dekker J., Rippe K, Dekker M, Kleckner N. 2002. Capturing chromosome conformation. Science 295: 1306-1311.
8. Edelman L.B., Fraser P. 2012. Transcription factories: genetic programming in three dimensions. Curr Opin Genet Dev 22: 110-114.
9. Fricker M., Hollinshead M, White N, Vaux D. 1997. Interphase nuclei of many cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J Cell Biol 136: 531-544.
10. Ghamari A., van de Corput MPC, Thongjuea S, van Cappellen WA, van Ijcken W., van Haren J, Soler E, Eick D, Lenhard B, Grosveld FG. 2013. In vivo live imaging of RNA polymerase II transcription factories in primary cells. Genes Dev 27: 767-777.
11. Gorman J.R., van der Stoep N, Monroe R, Cogne M, Davidson L, Alt FW. 1996. The Igk 39 enhancer influences the ratio of Igk versus Igλ{crossed} B lymphocytes. Immunity 5: 241-252.
12. Grü nwald D, Singer RH. 2010. In vivo imaging of labeled endogenous β-actin mRNA during nucleocytoplasmic transport. Nature 467: 604-607.
13. Hendershot L.M., Sitia R. 2004. Immunoglobulin assembly and secretion. In Molecular biology of B cells (ed. T Honjo T, et al.), pp. 261-273. Elsevier, London.
14. Hü bner MR, Spector DL. 2010. Chromatin dynamics. Ann Rev Biophys 39: 471-489.
15. Kang J., Xu B, Yao Y, Lin W, Hennessy C, Fraser P, Feng J. 2011. A dynamical model reveals gene co-localizations in nucleus. Plos Comp Biol 7: e1002094.
16. Kosak S.T., Skok JA, Medina KL, Riblet R, Le Beau MM, Fisher AG, Singh H. 2002. Subnuclear compartmentalization of immunoglobulin loci during lymphocyte development. Science 296: 158-162.
17. Lim J-H, Kim H-G, Park S-K, Kang C-J. 2009. The promoter of the immunoglobulin J chain gene receives its authentic enhancer activity through the abutting Mef2 and PU.1 sites in a DNA-looping interaction. J Mol Biol 390: 339-352.
18. Lin Y.C., Benner C, Mansson R, Heinz S, Miyazaki K, Miyazaki M, Chandra V., Bossen C, Glass CK, Murre C. 2012. Global changes in the nuclear positioning of genes and intra-and interdomain genomic interactions that orchestrate B cell fate. Nat Immunol 13: 1196-1204.
19. Martincic K., Alkan SA, Cheatle A, Borghesi L, Milcarek C. 2009. Transcription elongation factor ELL2 directs immunoglobulin secretion in plasma cells by stimulating altered RNA processing. Nat Immunol 10: 1102-1109.
20. Mor A., Suliman S, Ben-Yishay R, Yunger S, Brody Y, Shav-Tal Y. 2010. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat Cell Biol 12: 543-552.
21. Noble K.N., Wente SR. 2010. Nuclear RNA on the move. Nat Cell Biol 12: 525-527.
22. Ochiai K., Maienschein-Cline M, Simonetti G, Chen J, Rosenthal R, Brink R, Chong AS, Klein U, Dinner AR, Singh H, et al. 2013. Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4. Immunity 38: 918-929.
23. Osborne C.S., Chakalova L, Mitchell JA, Horton A, Wood AL, Bolland DJ, Corcoran A.E., Fraser P. 2007. Myc dynamically and preferentially relocates to a transcription factory occupied by Igh. PLoS Biol 5: 1763-1772.
24. Pederson T. 2011. The nucleus introduced. In The nucleus (ed. Misteli T and Spector DL), pp. 1-16. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
25. Schatz D.G., Ji Y. 2011. Recombination centres and the orchestration of V(D)J recombination. Nat Rev Immunol 11: 251-263.
26. Schoenfelder S., Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S., Mitchell JA, Umlauf D, Dimitrova DS, et al. 2010. Preferential associations between co-regulated genes reveal a transcriptional interactome in erythroid cells. Nat Genet 42: 53-61.
27. Shimizu Y., Meunier L, Hendershot LM. 2009. pERp1 is significantly upregulated during plasma cell differentiation and contributes to the oxidative folding of immunoglobulin. Proc Natl Acad Sci 106: 17013-17018.
28. Stewart M. 2010. Nuclear export of mRNA. Trends Biochem Sci 36: 609-617.
29. Takizawa T., Meaburn KJ, Misteli T. 2008. The meaning of gene positioning. Cell 135: 9-13.
30. Tinguely A., Chemin G, Péron S, Sirac C, Reynaud S, Cogné M, Delpy L. 2012. Cross talk between immunoglobulin heavy-chain transcription and RNA surveillance during B cell development. Mol Cell Biol 32: 107-117.
31. Vettermann C., Schlissel MS. 2010. Allelic exclusion of immunoglobulin genes: models and mechanisms. Immunol Rev 237: 22-42.
32. Zhou X., Xiang Y, Ding X, Garrard WT. 2012. A new hypersensitive site, HS10, and the enhancers, E39 and Ed, differentially regulate Igk gene expression. J Immunol 188: 2722-2732.
33. Zullo J.M., Demarco IA, Piqué-Regi R, Gaffney DJ, Epstein CB, Spooner CJ, Luperchio T.R., Bernstein BE, Pritchard JK, Reddy KL, et al. 2012. DNA sequence-dependent compartmentalization and silencing at the nuclear lamina. Cell 149: 1474-1487.