Transcriptional profiling of mouse B cell terminal differentiation defines a signature for antibody-secreting plasma cells

Nature Immunology

Volumn 16, Issue 6, 2015, Pages 663-673

  Shi, Wei ^a,b   Liao, Yang ^a,c   Willis, Simon N ^a,c   Taubenheim, Nadine ^a,c   Inouye, Michael ^a,c,d   Tarlinton, David M ^a,c   Smyth, Gordon K ^a,e   Hodgkin, Philip D ^a,c   Nutt, Stephen L ^a,c   Corcoran, Lynn M ^a,c  

^a WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF MELBOURNE   (Australia)

^e UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTOME; B CELL MATURATION ANTIGEN; PRDM1 PROTEIN, MOUSE; RNA; SOCS2 PROTEIN, MOUSE; SUPPRESSOR OF CYTOKINE SIGNALING; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANTIBODY SECRETING CELL; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; CELL POPULATION; EPIGENETIC REPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; HISTONE MODIFICATION; IMMUNOGLOBULIN GENE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PLASMA CELL; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL DIFFERENTIATION; CELL DIVISION; CELL MOTION; CYTOLOGY; GENETICS; HISTONE CODE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION;

ANIMALS; B-CELL MATURATION ANTIGEN; CELL DIFFERENTIATION; CELL DIVISION; CELL MOVEMENT; CELLS, CULTURED; GENE EXPRESSION PROFILING; HISTONE CODE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLASMA CELLS; RNA; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTOME;

EID: 84929966586     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3154     Document Type: Article

References (50)

1. Nutt, S. L. , Hodgkin, P. D. , Tarlinton, D. M. & Corcoran, L. M. The generation of antibody-secreting plasma cells. Nat. Rev. Immunol. 15, 160-171 (2015).
2. Fujio, K. , Okamura, T. , Sumitomo, S. & Yamamoto, K. Regulatory cell subsets in the control of autoantibody production related to systemic autoimmunity. Ann. Rheum. Dis. 72 (suppl. 2) ii85-ii89 (2013).
3. Potter, M. Neoplastic development in plasma cells. Immunol. Rev. 194, 177-195 (2003).
4. Fairfax, K. A. et al. Different kinetics of blimp-1 induction in B cell subsets revealed by reporter gene. J. Immunol. 178, 4104-4111 (2007).
5. Radbruch, A. et al. Competence and competition: the challenge of becoming a long-lived plasma cell. Nat. Rev. Immunol. 6, 741-750 (2006).
6. Tarlinton, D. & Good-Jacobson, K. Diversity among memory B cells: origin, consequences, and utility. Science 341, 1205-1211 (2013).
7. Nutt, S. L. , Taubenheim, N. , Hasbold, J. , Corcoran, L. M. & Hodgkin, P. D. The genetic network controlling plasma cell differentiation. Semin. Immunol. 23, 341-349 (2011).
8. Shapiro-Shelef, M. & Calame, K. Regulation of plasma-cell development. Nat. Rev. Immunol. 5, 230-242 (2005).
9. Shaffer, A. L. et al. Blimp-1 orchestrates plasma cell differentiation by extinguishing the mature B cell gene expression program. Immunity 17, 51-62 (2002).
10. Shaffer, A. L. et al. XBP1, downstream of Blimp-1, expands the secretory apparatus and other organelles, and increases protein synthesis in plasma cell differentiation. Immunity 21, 81-93 (2004).
11. Cocco, M. et al. In vitro generation of long-lived human plasma cells. J. Immunol. 189, 5773-5785 (2012).
12. Jourdan, M. et al. An in vitro model of differentiation of memory B cells into plasmablasts and plasma cells in cluding detailed phenotypic and molecular characterization. Blood 114, 5173-5181 (2009).
13. Peperzak, V. et al. Mcl-1 is essential for the survival of plasma cells. Nat. Immunol. 14, 290-297 (2013).
14. Sciammas, R. et al. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity 25, 225-236 (2006).
15. Kallies, A. et al. Plasma cell ontogeny defined by quantitative changes in blimp-1 expression. J. Exp. Med. 200, 967-977 (2004).
16. Liao, Y. , Smyth, G. K. & Shi, W. The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 41, e108 (2013).
17. Liao, Y. , Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923-930 (2014).
18. O'Connor, B. P. et al. BCMA is essential for the survival of long-lived bone marrow plasma cells. J. Exp. Med. 199, 91-98 (2004).
19. Delogu, A. et al. Gene repression by Pax5 in B cells is essential for blood cell homeostasis and is reversed in plasma cells. Immunity 24, 269-281 (2006).
20. Wrammert, J. , Kallberg, E. , Agace, W. W. & Leanderson, T. Ly6C expression differentiates plasma cells from other B cell subsets in mice. Eur. J. Immunol. 32, 97-103 (2002).
21. Nakayama, T. et al. Cutting edge: profile of chemokine receptor expression on human plasma cells accounts for their efficient recruitment to target tissues. J. Immunol. 170, 1136-1140 (2003).
22. Hauser, A. E. et al. Chemotactic responsiveness toward ligands for CXCR3 and CXCR4 is regulated on plasma blasts during the time course of a memory immune response. J. Immunol. 169, 1277-1282 (2002).
23. Kunkel, E. J. et al. CCR10 expression is a common feature of circulating and mucosal epithelial tissue IgA Ab-secreting cells. J. Clin. Invest. 111, 1001-1010 (2003).
24. Cerutti, A. , Cols, M. & Puga, I. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat. Rev. Immunol. 13, 118-132 (2013).
25. Jeong, H. D. & Teale, J. M. Contribution of the CD5+ B cell to D-proximal VH family expression early in ontogeny. J. Immunol. 145, 2725-2729 (1990).
26. Herzenberg, L. A. , Baumgarth, N. & Wilshire, J. A. B-1 cell origins and VH repertoire determination. Curr. Top. Microbiol. Immunol. 252, 3-13 (2000).
27. Metcalf, D. et al. Gigantism in mice lacking suppressor of cytokine signalling-2. Nature 405, 1069-1073 (2000).
28. Hasbold, J. , Corcoran, L. M. , Tarlinton, D. M. , Tangye, S. G. & Hodgkin, P. D. Evidence from the generation of immunoglobulin G-secreting cells that stochastic mechanisms regulate lymphocyte differentiation. Nat. Immunol. 5, 55-63 (2004).
29. Hodgkin, P. D. , Lee, J. H. & Lyons, A. B. B cell differentiation and isotype switching is related to division cycle number. J. Exp. Med. 184, 277-281 (1996).
30. Rush, J. S. , Liu, M. , Odegard, V. H. , Unniraman, S. & Schatz, D. G. Expression of activation-induced cytidine deaminase is regulated by cell division, providing a mechanistic basis for division-linked class switch recombination. Proc. Natl. Acad. Sci. USA 102, 13242-13247 (2005).
31. Heinz, S. et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38, 576-589 (2010).
32. Hnisz, D. et al. Super-enhancers in the control of cell identity and disease. Cell 155, 934-947 (2013).
33. Whyte, W. A. et al. Master transcription factors and mediator establish super-enhancers at key cell identity genes. Cell 153, 307-319 (2013).
34. Lovén, J. et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 153, 320-334 (2013).
35. Chu, V. T. & Berek, C. The establishment of the plasma cell survival niche in the bone marrow. Immunol. Rev. 251, 177-188 (2013).
36. Kurtz, J. E. & Dufour, P. Adecatumumab: an anti-EpCAM monoclonal antibody, from the bench to the bedside. Expert Opin. Biol. Ther. 10, 951-958 (2010).
37. Lu, R. & Wang, G. G. Tudor: a versatile family of histone methylation 'readers'. Trends Biochem. Sci. 38, 546-555 (2013).
38. Xiao, W. et al. U19/Eaf2 knockout causes lung adenocarcinoma, B-cell lymphoma, hepatocellular carcinoma and prostatic intraepithelial neoplasia. Oncogene 27, 1536-1544 (2008).
39. Korthuis, P. M. et al. CITED2-mediated human hematopoietic stem cell maintenance is critical for acute myeloid leukemia. Leukemia 29, 625-635 (2015).
40. Knosp, C. A. et al. SOCS2 regulates Thelper type 2 differentiation and the generation of type 2 allergic responses. J. Exp. Med. 208, 1523-1531 (2011).
41. Zak, D. E. , Tam, V. C. & Aderem, A. Systems-level analysis of innate immunity. Annu. Rev. Immunol. 32, 547-577 (2014).
42. Basso, K. et al. Reverse engineering of regulatory networks in human B cells. Nat. Genet. 37, 382-390 (2005).
43. Yosef, N. et al. Dynamic regulatory network controlling TH17 cell differentiation. Nature 496, 461-468 (2013).
44. Perfetti, V. et al. Membrane CD22 defines circulating myeloma-related cells as mature or later B cells. Lab. Invest. 77, 333-344 (1997).
45. Zhang, J. A. , Mortazavi, A. , Williams, B. A. , Wold, B. J. & Rothenberg, E. V. Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell 149, 467-482 (2012).
46. Ritchie, M. E. et al. limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, doi:10. 1093/nar/gkv007 (2015).
47. Law, C. W. , Chen, Y. , Shi, W. & Smyth, G. K. voom: precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, R29 (2014).
48. Smyth, G. K. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, Article3 (2004).
49. McCarthy, D. J. & Smyth, G. K. Testing significance relative to a fold-change threshold is a TREAT. Bioinformatics 25, 765-771 (2009).
50. Wu, D. et al. ROAST: rotation gene set tests for complex microarray experiments. Bioinformatics 26, 2176-2182 (2010).